Abstract
The Golgi apparatus is an essential cellular organelle that mediates homeostatic functions, including vesicle trafficking and the post-translational modification of macromolecules. Its unique stacked structure and dynamic functions are tightly regulated, and several Golgi proteins play key roles in the functioning of unconventional protein secretory pathways triggered by cellular stress responses. Recently, an increasing number of studies have implicated defects in Golgi functioning in human diseases such as cancer, neurodegenerative, and immunological disorders. Understanding the extraordinary characteristics of Golgi proteins is important for elucidating its associated intracellular signaling mechanisms and has important ramifications for human health. Therefore, analyzing the mechanisms by which the Golgi participates in disease pathogenesis may be useful for developing novel therapeutic strategies. This review articulates the structural features and abnormalities of the Golgi apparatus reported in various diseases and the suspected mechanisms underlying the Golgi-associated pathologies. Furthermore, we review the potential therapeutic strategies based on Golgi function.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahat E, Li J, Wang Y (2019) New insights into the Golgi stacking proteins. Front Cell Dev Biol 7:131. https://doi.org/10.3389/fcell.2019.00131
Alshammari MJ, Al-Otaibi L, Alkuraya FS (2012) Mutation in RAB33B, which encodes a regulator of retrograde Golgi transport, defines a second Dyggve–Melchior–Clausen locus. J Med Genet 49:455–461. https://doi.org/10.1136/jmedgenet-2011-100666
Annadurai N, De Sanctis JB, Hajdúch M, Das V (2021) Tau secretion and propagation: perspectives for potential preventive interventions in Alzheimer’s disease and other tauopathies. Exp Neurol 343:113756. https://doi.org/10.1016/j.expneurol.2021.113756
Antón-Fernández A, Aparicio-Torres G, Tapia S, Defelipe J, Muñoz A (2017) Morphometric alterations of Golgi apparatus in Alzheimer’s disease are related to tau hyperphosphorylation. Neurobiol Dis 97:11–23. https://doi.org/10.1016/j.nbd.2016.10.005
Aoh QL, Hung CW, Duncan MC (2013) Energy metabolism regulates clathrin adaptors at the trans-Golgi network and endosomes. Mol Biol Cell 24:832–847. https://doi.org/10.1091/mbc.E12-10-0750
Aridor M (2022) A tango for coats and membranes: new insights into ER-to-Golgi traffic. Cell Rep 38:110258. https://doi.org/10.1016/j.celrep.2021.110258
Arrazola Sastre A, Luque Montoro M, Lacerda HM, Llavero F, Zugaza JL (2021) Small GTPases of the Rab and Arf families: key regulators of intracellular trafficking in neurodegeneration. Int J Mol Sci 22:4425. https://doi.org/10.3390/ijms22094425
Artan M, Sohn J, Lee C, Park SY, Lee SV (2022) MON-2, a Golgi protein, promotes longevity by upregulating autophagy through mediating inter-organelle communications. Autophagy. https://doi.org/10.1080/15548627.2022.2039523
Ayala I, Colanzi A (2017) Alterations of Golgi organization in Alzheimer’s disease: a cause or a consequence? Tissue Cell 49:133–140. https://doi.org/10.1016/j.tice.2016.11.007
Bagal AA, Kao JP, Tang CM, Thompson SM (2005) Long-term potentiation of exogenous glutamate responses at single dendritic spines. Proc Natl Acad Sci USA 102:14434–14439. https://doi.org/10.1073/pnas.0501956102
Bala S, Babuta M, Catalano D, Saiju A, Szabo G (2021) Alcohol promotes exosome biogenesis and release via modulating Rabs and miR-192 expression in human hepatocytes. Front Cell Dev Biol 9:787356. https://doi.org/10.3389/fcell.2021.787356
Baloyannis SJ (2014) Golgi apparatus and protein trafficking in Alzheimer’s disease. J Alzheimers Dis 42(Suppl 3):S153–S162. https://doi.org/10.3233/jad-132660
Baron O, Boudi A, Dias C, Schilling M, Nölle A, Vizcay-Barrena G, Rattray I, Jungbluth H, Scheper W, Fleck RA, Bates GP, Fanto M (2017) Stall in canonical autophagy-lysosome pathways prompts nucleophagy-based nuclear breakdown in neurodegeneration. Curr Biol 27:3626-3642.e6. https://doi.org/10.1016/j.cub.2017.10.054
Barr FA, Puype M, Vandekerckhove J, Warren G (1997) GRASP65, a protein involved in the stacking of Golgi cisternae. Cell 91:253–262. https://doi.org/10.1016/s0092-8674(00)80407-9
Baumann J, Ignashkova TI, Chirasani SR, Ramírez-Peinado S, Alborzinia H, Gendarme M, Kuhnigk K, Kramer V, Lindemann RK, Reiling JH (2018) Golgi stress-induced transcriptional changes mediated by MAPK signaling and three ETS transcription factors regulate MCL1 splicing. Mol Biol Cell 29:42–52. https://doi.org/10.1091/mbc.E17-06-0418
Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39. https://doi.org/10.1038/361031a0
Brandizzi F, Barlowe C (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14:382–392. https://doi.org/10.1038/nrm3588
Cao Q, Wang Z, Wan H, Xu L, You X, Liao L, Chen Y (2018) PAQR3 regulates endoplasmic reticulum-to-Golgi trafficking of COPII vesicle via interaction with Sec13/Sec31 coat proteins. iScience 9:382–398. https://doi.org/10.1016/j.isci.2018.11.002
Chakrabarti R, Lee M, Higgs HN (2021) Multiple roles for actin in secretory and endocytic pathways. Curr Biol 31:R603-r618. https://doi.org/10.1016/j.cub.2021.03.038
Chan WL, Steiner M, Witkos T, Egerer J, Busse B, Mizumoto S, Pestka JM, Zhang H, Hausser I, Khayal LA, Ott CE, Kolanczyk M, Willie B, Schinke T, Paganini C, Rossi A, Sugahara K, Amling M, Knaus P, Chan D, Lowe M, Mundlos S, Kornak U (2018) Impaired proteoglycan glycosylation, elevated TGF-β signaling, and abnormal osteoblast differentiation as the basis for bone fragility in a mouse model for gerodermia osteodysplastica. PLoS Genet 14:e1007242. https://doi.org/10.1371/journal.pgen.1007242
Chang CC, Chen CJ, Grauffel C, Pien YC, Lim C, Tsai SY, Hsia KC (2019) Ran pathway-independent regulation of mitotic Golgi disassembly by Importin-α. Nat Commun 10:4307. https://doi.org/10.1038/s41467-019-12207-4
Chen Z, Yu Q, Yu Q, Johnson J, Shipman R, Zhong X, Huang J, Asthana S, Carlsson C, Okonkwo O, Li L (2021) In-depth Site-specific analysis of N-glycoproteome in human cerebrospinal fluid and glycosylation landscape changes in Alzheimer’s disease. Mol Cell Proteomics 20:100081. https://doi.org/10.1016/j.mcpro.2021.100081
Chiritoiu M, Brouwers N, Turacchio G, Pirozzi M, Malhotra V (2019) GRASP55 and UPR control interleukin-1β aggregation and secretion. Dev Cell 49:145–155. https://doi.org/10.1016/j.devcel.2019.02.011
Chiu R, Novikov L, Mukherjee S, Shields D (2002) A caspase cleavage fragment of p115 induces fragmentation of the Golgi apparatus and apoptosis. J Cell Biol 159:637–648. https://doi.org/10.1083/jcb.200208013
Cho Y, Bae HG, Okun E, Arumugam TV, Jo DG (2022) Physiology and pharmacology of amyloid precursor protein. Pharmacol Ther 235:108122. https://doi.org/10.1016/j.pharmthera.2022.108122
Chung CG, Kwon MJ, Jeon KH, Hyeon DY, Han MH, Park JH, Cha IJ, Cho JH, Kim K, Rho S, Kim GR, Jeong H, Lee JW, Kim T, Kim K, Kim KP, Ehlers MD, Hwang D, Lee SB (2017) Golgi outpost synthesis impaired by toxic polyglutamine proteins contributes to dendritic pathology in neurons. Cell Rep 20:356–369. https://doi.org/10.1016/j.celrep.2017.06.059
Cleyrat C, Darehshouri A, Steinkamp MP, Vilaine M, Boassa D, Ellisman MH, Hermouet S, Wilson BS (2014) Mpl traffics to the cell surface through conventional and unconventional routes. Traffic 15:961–982. https://doi.org/10.1111/tra.12185
Corbett MA, Schwake M, Bahlo M, Dibbens LM, Lin M, Gandolfo LC, Vears DF, O’sullivan JD, Robertson T, Bayly MA, Gardner AE, Vlaar AM, Korenke GC, Bloem BR, De Coo IF, Verhagen JM, Lehesjoki AE, Gecz J, Berkovic SF (2011) A mutation in the Golgi Qb-SNARE gene GOSR2 causes progressive myoclonus epilepsy with early ataxia. Am J Hum Genet 88:657–663. https://doi.org/10.1016/j.ajhg.2011.04.011
Cornejo VH, González C, Campos M, Vargas-Saturno L, Juricic M, Miserey-Lenkei S, Pertusa M, Madrid R, Couve A (2020) Non-conventional axonal organelles control TRPM8 ion channel trafficking and peripheral cold sensing. Cell Rep 30:4505–4517. https://doi.org/10.1016/j.celrep.2020.03.017
Custer SK, Foster JN, Astroski JW, Androphy EJ (2019) Abnormal Golgi morphology and decreased COPI function in cells with low levels of SMN. Brain Res 1706:135–146. https://doi.org/10.1016/j.brainres.2018.11.005
D’souza Z, Taher FS, Lupashin VV (2020) Golgi inCOGnito: From vesicle tethering to human disease. Biochim Biophys Acta Gen Subj 1864:129694. https://doi.org/10.1016/j.bbagen.2020.129694
Day KJ, Staehelin LA, Glick BS (2013) A three-stage model of Golgi structure and function. Histochem Cell Biol 140:239–249. https://doi.org/10.1007/s00418-013-1128-3
Demaretz S, Seaayfan E, Bakhos-Douaihy D, Frachon N, Kömhoff M, Laghmani K (2021) Golgi Alpha 1,2-Mannosidase IA promotes efficient endoplasmic reticulum-associated degradation of NKCC2. Cells. https://doi.org/10.3390/cells11010101
Deng H, Xiao H (2017) The role of the ATP2C1 gene in Hailey-Hailey disease. Cell Mol Life Sci 74:3687–3696. https://doi.org/10.1007/s00018-017-2544-7
Deng S, Liu J, Wu X, Lu W (2020) Golgi apparatus: a potential therapeutic target for autophagy-associated neurological diseases. Front Cell Dev Biol 8:564975. https://doi.org/10.3389/fcell.2020.564975
Deng D, Qu Y, Sun L, Jia L, Bu J, Ye M, Chen Z, Geng Y, Zhou S, Fang B (2021) Fuyuan Xingnao decoction promotes angiogenesis through the Rab1/AT1R pathway in diabetes mellitus complicated with cerebral infarction. Front Pharmacol 12:616165. https://doi.org/10.3389/fphar.2021.616165
Diao A, Rahman D, Pappin DJ, Lucocq J, Lowe M (2003) The coiled-coil membrane protein golgin-84 is a novel rab effector required for Golgi ribbon formation. J Cell Biol 160:201–212. https://doi.org/10.1083/jcb.200207045
Diniz F, Coelho P, Duarte HO, Sarmento B, Reis CA, Gomes J (2022) Glycans as targets for drug delivery in cancer. Cancers. https://doi.org/10.3390/cancers14040911
Du W, Hua F, Li X, Zhang J, Li S, Wang W, Zhou J, Wang W, Liao P, Yan Y, Li G, Wei S, Grove S, Vatan L, Zgodziński W, Majewski M, Wallner G, Chen H, Kryczek I, Fang JY, Zou W (2021) Loss of optineurin drives cancer immune evasion via palmitoylation-dependent IFNGR1 lysosomal sorting and degradation. Cancer Discov 11:1826–1843. https://doi.org/10.1158/2159-8290.Cd-20-1571
Dulary E, Potelle S, Legrand D, Foulquier F (2017) TMEM165 deficiencies in Congenital Disorders of Glycosylation type II (CDG-II): Clues and evidences for roles of the protein in Golgi functions and ion homeostasis. Tissue Cell 49:150–156. https://doi.org/10.1016/j.tice.2016.06.006
Dupont N, Jiang S, Pilli M, Ornatowski W, Bhattacharya D, Deretic V (2011) Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β. Embo J 30:4701–4711. https://doi.org/10.1038/emboj.2011.398
Dupuis N, Lebon S, Kumar M, Drunat S, Graul-Neumann LM, Gressens P, El El Ghouzzi V (2013) A novel RAB33B mutation in Smith-McCort dysplasia. Hum Mutat 34:283–286. https://doi.org/10.1002/humu.22235
Eisenberg-Lerner A, Benyair R, Hizkiahou N, Nudel N, Maor R, Kramer MP, Shmueli MD, Zigdon I, Cherniavsky Lev M, Ulman A, Sagiv JY, Dayan M, Dassa B, Rosenwald M, Shachar I, Li J, Wang Y, Dezorella N, Khan S, Porat Z, Shimoni E, Avinoam O, Merbl Y (2020) Golgi organization is regulated by proteasomal degradation. Nat Commun 11:409. https://doi.org/10.1038/s41467-019-14038-9
Ernst AM, Syed SA, Zaki O, Bottanelli F, Zheng H, Hacke M, Xi Z, Rivera-Molina F, Graham M, Rebane AA, Björkholm P, Baddeley D, Toomre D, Pincet F, Rothman JE (2018) S-palmitoylation sorts membrane cargo for anterograde transport in the Golgi. Dev Cell 47:479–493. https://doi.org/10.1016/j.devcel.2018.10.024
Esmail S, Manolson MF (2021) Advances in understanding N-glycosylation structure, function, and regulation in health and disease. Eur J Cell Biol 100:151186. https://doi.org/10.1016/j.ejcb.2021.151186
Farber-Katz SE, Dippold HC, Buschman MD, Peterman MC, Xing M, Noakes CJ, Tat J, Ng MM, Rahajeng J, Cowan DM, Fuchs GJ, Zhou H, Field SJ (2014) DNA damage triggers Golgi dispersal via DNA-PK and GOLPH3. Cell 156:413–427. https://doi.org/10.1016/j.cell.2013.12.023
Fonseca D, Carvalho P (2019) EGAD! There is an ERAD doppelganger in the Golgi. EMBO J 38:e102679. https://doi.org/10.15252/embj.2019102679
Foulquier F, Amyere M, Jaeken J, Zeevaert R, Schollen E, Race V, Bammens R, Morelle W, Rosnoblet C, Legrand D, Demaegd D, Buist N, Cheillan D, Guffon N, Morsomme P, Annaert W, Freeze HH, Van Schaftingen E, Vikkula M, Matthijs G (2012) TMEM165 deficiency causes a congenital disorder of glycosylation. Am J Hum Genet 91:15–26. https://doi.org/10.1016/j.ajhg.2012.05.002
Fourriere L, Gleeson PA (2021) Amyloid β production along the neuronal secretory pathway: dangerous liaisons in the Golgi? Traffic 22:319–327. https://doi.org/10.1111/tra.12808
Fourriere L, Cho EH, Gleeson PA (2022) Segregation of the membrane cargoes, BACE1 and amyloid precursor protein (APP) throughout the Golgi apparatus. Traffic 23:158–173. https://doi.org/10.1111/tra.12831
Frappaolo A, Karimpour-Ghahnavieh A, Sechi S, Giansanti MG (2020) The close relationship between the Golgi trafficking machinery and protein glycosylation. Cells 9:2652. https://doi.org/10.3390/cells9122652
Fu MM, Mcalear TS, Nguyen H, Oses-Prieto JA, Valenzuela A, Shi RD, Perrino JJ, Huang TT, Burlingame AL, Bechstedt S, Barres BA (2019) The Golgi outpost protein TPPP nucleates microtubules and is critical for myelination. Cell 179:132–146. https://doi.org/10.1016/j.cell.2019.08.025
Fujita Y, Okamoto K, Sakurai A, Gonatas NK, Hirano A (2000) Fragmentation of the Golgi apparatus of the anterior horn cells in patients with familial amyotrophic lateral sclerosis with SOD1 mutations and posterior column involvement. J Neurol Sci 174:137–140. https://doi.org/10.1016/s0022-510x(00)00265-3
Fujita Y, Ohama E, Takatama M, Al-Sarraj S, Okamoto K (2006) Fragmentation of Golgi apparatus of nigral neurons with alpha-synuclein-positive inclusions in patients with Parkinson’s disease. Acta Neuropathol 112:261–265. https://doi.org/10.1007/s00401-006-0114-4
Galenkamp KMO, Commisso C (2021) The Golgi as a “Proton Sink” in Cancer. Front Cell Dev Biol 9:664295. https://doi.org/10.3389/fcell.2021.664295
Galenkamp KMO, Sosicka P, Jung M, Recouvreux MV, Zhang Y, Moldenhauer MR, Brandi G, Freeze HH, Commisso C (2020) Golgi acidification by NHE7 regulates cytosolic pH homeostasis in pancreatic cancer cells. Cancer Discov 10:822–835. https://doi.org/10.1158/2159-8290.Cd-19-1007
Gao J, Gao A, Liu W, Chen L (2021) Golgi stress response: A regulatory mechanism of Golgi function. BioFactors 47:964–974. https://doi.org/10.1002/biof.1780
Gerbino V, Kaunga E, Ye J, Canzio D, O’keeffe S, Rudnick ND, Guarnieri P, Lutz CM, Maniatis T (2020) The loss of TBK1 kinase activity in motor neurons or in all cell types differentially impacts ALS disease progression in SOD1 mice. Neuron 106:789-805.e5. https://doi.org/10.1016/j.neuron.2020.03.005
Gillingham AK, Munro S (2016) Finding the Golgi: Golgin coiled-coil proteins show the way. Trends Cell Biol 26:399–408. https://doi.org/10.1016/j.tcb.2016.02.005
Gonatas NK, Stieber A, Gonatas JO (2006) Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J Neurol Sci 246:21–30. https://doi.org/10.1016/j.jns.2006.01.019
Gopal Krishnan PD, Golden E, Woodward EA, Pavlos NJ, Blancafort P (2020) Rab GTPases: emerging oncogenes and tumor suppressive regulators for the editing of survival pathways in cancer. Cancers 12:259. https://doi.org/10.3390/cancers12020259
Goud B, Liu S, Storrie B (2018) Rab proteins as major determinants of the Golgi complex structure. Small GTPases 9:66–75. https://doi.org/10.1080/21541248.2017.1384087
Goytain A, Quamme GA (2008) Identification and characterization of a novel family of membrane magnesium transporters, MMgT1 and MMgT2. Am J Physiol Cell Physiol 294:C495-502. https://doi.org/10.1152/ajpcell.00238.2007
Guo H, Wei JH, Zhang Y, Seemann J (2021) Importin α phosphorylation promotes TPX2 activation by GM130 to control astral microtubules and spindle orientation. J Cell Sci 134:jcs258356. https://doi.org/10.1242/jcs.258356
Häuselmann I, Borsig L (2014) Altered tumor-cell glycosylation promotes metastasis. Front Oncol 4:28. https://doi.org/10.3389/fonc.2014.00028
Halloran M, Ragagnin AMG, Vidal M, Parakh S, Yang S, Heng B, Grima N, Shahheydari H, Soo KY, Blair I, Guillemin GJ, Sundaramoorthy V, Atkin JD (2020) Amyotrophic lateral sclerosis-linked UBQLN2 mutants inhibit endoplasmic reticulum to Golgi transport, leading to Golgi fragmentation and ER stress. Cell Mol Life Sci 77:3859–3873. https://doi.org/10.1007/s00018-019-03394-w
Hannun YA, Obeid LM (2018) Sphingolipids and their metabolism in physiology and disease. Nat Rev Mol Cell Biol 19:175–191. https://doi.org/10.1038/nrm.2017.107
Hansen MD, Johnsen IB, Stiberg KA, Sherstova T, Wakita T, Richard GM, Kandasamy RK, Meurs EF, Anthonsen MW (2017) Hepatitis C virus triggers Golgi fragmentation and autophagy through the immunity-related GTPase M. Proc Natl Acad Sci USA 114:E3462–E3471. https://doi.org/10.1073/pnas.1616683114
Hardiman O, Al-Chalabi A, Chio A, Corr EM, Logroscino G, Robberecht W, Shaw PJ, Simmons Z, Van Den Berg LH (2017) Amyotrophic lateral sclerosis. Nat Rev Dis Primers 3:17071. https://doi.org/10.1038/nrdp.2017.71
Harvald EB, Olsen AS, Færgeman NJ (2015) Autophagy in the light of sphingolipid metabolism. Apoptosis 20:658–670. https://doi.org/10.1007/s10495-015-1108-2
He Q, Liu H, Huang C, Wang R, Luo M, Lu W (2020) Herpes simplex virus 1 induced blood-brain barrier damage involves apoptosis associated with GM130-mediated Golgi stress. Front Mol Neurosci 13:2. https://doi.org/10.3389/fnmol.2020.00002
Hjelmqvist L, Tuson M, Marfany G, Herrero E, Balcells S, Gonzàlez-Duarte R (2002) ORMDL proteins are a conserved new family of endoplasmic reticulum membrane proteins. Genome Biol 3:1–16. https://doi.org/10.1186/gb-2002-3-6-research0027
Honda S, Arakawa S, Nishida Y, Yamaguchi H, Ishii E, Shimizu S (2014) Ulk1-mediated Atg5-independent macroautophagy mediates elimination of mitochondria from embryonic reticulocytes. Nat Commun 5:4004. https://doi.org/10.1038/ncomms5004
Hsu RM, Zhong CY, Wang CL, Liao WC, Yang C, Lin SY, Lin JW, Cheng HY, Li PY, Yu CJ (2018) Golgi tethering factor golgin-97 suppresses breast cancer cell invasiveness by modulating NF-κB activity. Cell Commun Signal 16:19. https://doi.org/10.1186/s12964-018-0230-5
Husni RE, Shiba-Ishii A, Nakagawa T, Dai T, Kim Y, Hong J, Sakashita S, Sakamoto N, Sato Y, Noguchi M (2019) DNA hypomethylation-related overexpression of SFN, GORASP2 and ZYG11A is a novel prognostic biomarker for early stage lung adenocarcinoma. Oncotarget 10:1625–1636. https://doi.org/10.18632/oncotarget.26676
Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T, Fukuda M (2008) Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 19:2916–2925. https://doi.org/10.1091/mbc.e07-12-1231
Jackson CL (2009) Mechanisms of transport through the Golgi complex. J Cell Sci 122:443–452. https://doi.org/10.1242/jcs.032581
Jamaludin MI, Wakabayashi S, Taniguchi M, Sasaki K, Komori R, Kawamura H, Takase H, Sakamoto M, Yoshida H (2019) MGSE regulates crosstalk from the mucin pathway to the TFE3 pathway of the Golgi stress response. Cell Struct Funct 44:137–151. https://doi.org/10.1247/csf.19009
Jesenberger V, Procyk KJ, Yuan J, Reipert S, Baccarini M (2000) Salmonella-induced caspase-2 activation in macrophages: a novel mechanism in pathogen-mediated apoptosis. J Exp Med 192:1035–1046. https://doi.org/10.1084/jem.192.7.1035
Jeyifous O, Waites CL, Specht CG, Fujisawa S, Schubert M, Lin EI, Marshall J, Aoki C, De Silva T, Montgomery JM, Garner CC, Green WN (2009) SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway. Nat Neurosci 12:1011–1019. https://doi.org/10.1038/nn.2362
Jiang Q, Wang L, Guan Y, Xu H, Niu Y, Han L, Wei YP, Lin L, Chu J, Wang Q, Yang Y, Pei L, Wang JZ, Tian Q (2014) Golgin-84-associated Golgi fragmentation triggers tau hyperphosphorylation by activation of cyclin-dependent kinase-5 and extracellular signal-regulated kinase. Neurobiol Aging 35:1352–1363. https://doi.org/10.1016/j.neurobiolaging.2013.11.022
Jin H, Tang Y, Yang L, Peng X, Li B, Fan Q, Wei S, Yang S, Li X, Wu B, Huang M, Tang S, Liu J, Li H (2021a) Rab GTPases: central coordinators of membrane trafficking in cancer. Front Cell Dev Biol 9:648384. https://doi.org/10.3389/fcell.2021.648384
Jin J, Zhi X, Wang X, Meng D (2021b) Protein palmitoylation and its pathophysiological relevance. J Cell Physiol 236:3220–3233. https://doi.org/10.1002/jcp.30122
Jones KA, Eng AG, Raval P, Srivastava DP, Penzes P (2014) Scaffold protein X11α interacts with kalirin-7 in dendrites and recruits it to Golgi outposts. J Biol Chem 289:35517–35529. https://doi.org/10.1074/jbc.M114.587709
Joshi G, Bekier ME 2nd, Wang Y (2015) Golgi fragmentation in Alzheimer’s disease. Front Neurosci 9:340. https://doi.org/10.3389/fnins.2015.00340
Joshi G, Chi Y, Huang Z, Wang Y (2014) Aβ-induced Golgi fragmentation in Alzheimer’s disease enhances Aβ production. Proc Natl Acad Sci U S A 111:E1230–E1239. https://doi.org/10.1073/pnas.1320192111
Kellokumpu S (2019) Golgi pH, Ion and redox homeostasis: how much do they really matter? Front Cell Dev Biol 7:93. https://doi.org/10.3389/fcell.2019.00093
Kennedy MJ, Ehlers MD (2006) Organelles and trafficking machinery for postsynaptic plasticity. Annu Rev Neurosci 29:325–362. https://doi.org/10.1146/annurev.neuro.29.051605.112808
Khan S, Sbeity M, Foulquier F, Barré L, Ouzzine M (2021) TMEM165 a new player in proteoglycan synthesis: loss of TMEM165 impairs elongation of chondroitin- and heparan-sulfate glycosaminoglycan chains of proteoglycans and triggers early chondrocyte differentiation and hypertrophy. Cell Death Dis 13:11. https://doi.org/10.1038/s41419-021-04458-1
Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, Burrell JR, Zoing MC (2011) Amyotrophic lateral sclerosis. Lancet 377:942–955. https://doi.org/10.1016/s0140-6736(10)61156-7
Kim J, Gee HY, Lee MG (2018) Unconventional protein secretion—new insights into the pathogenesis and therapeutic targets of human diseases. J Cell Sci 131:jcs211201. https://doi.org/10.1242/jcs.213686
Kim J, Kim H, Noh SH, Jang DG, Park SY, Min D, Kim H, Kweon HS, Kim H, Aum S, Seo S, Choi CS, Kim H, Kim JW, Moon SJ, Gee HY, Lee MG (2020) Grasp55(-/-) mice display impaired fat absorption and resistance to high-fat diet-induced obesity. Nat Commun 11:1418. https://doi.org/10.1038/s41467-020-14912-x
Kim J, Noh SH, Piao H, Kim DH, Kim K, Cha JS, Chung WY, Cho HS, Kim JY, Lee MG (2016) Monomerization and ER relocalization of GRASPis a requisite for unconventional secretion of CFTR. Traffic 17:733–753. https://doi.org/10.1111/tra.12403
Kjos I, Vestre K, Guadagno NA, Borg Distefano M, Progida C (2018) Rab and Arf proteins at the crossroad between membrane transport and cytoskeleton dynamics. Biochim Biophys Acta Mol Cell Res 1865:1397–1409. https://doi.org/10.1016/j.bbamcr.2018.07.009
Klute MJ, Melançon P, Dacks JB (2011) Evolution and diversity of the Golgi. Cold Spring Harb Perspect Biol 3:a007849. https://doi.org/10.1101/cshperspect.a007849
Kokkonen N, Khosrowabadi E, Hassinen A, Harrus D, Glumoff T, Kietzmann T, Kellokumpu S (2019) Abnormal Golgi pH homeostasis in cancer cells impairs apical targeting of carcinoembryonic antigen by inhibiting its glycosyl-phosphatidylinositol anchor-mediated association with lipid rafts. Antioxid Redox Signal 30:5–21. https://doi.org/10.1089/ars.2017.7389
Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169:425–434. https://doi.org/10.1083/jcb.200412022
König P, Eckstein M, Jung R, Abdulrahman A, Guzman J, Weigelt K, Serrero G, Hayashi J, Geppert C, Stöhr R, Hartmann A, Wullich B, Wach S, Taubert H, Lieb V (2020) Expression of AR-V7 (Androgen Receptor Variant 7) Protein in granular cytoplasmic structures is an independent prognostic factor in prostate cancer patients. Cancers 12:2639. https://doi.org/10.3390/cancers12092639
Kovacs L, Chao-Chu J, Schneider S, Gottardo M, Tzolovsky G, Dzhindzhev NS, Riparbelli MG, Callaini G, Glover DM (2018) Gorab is a Golgi protein required for structure and duplication of Drosophila centrioles. Nat Genet 50:1021–1031. https://doi.org/10.1038/s41588-018-0149-1
Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N (2004) The role of autophagy during the early neonatal starvation period. Nature 432:1032–1036. https://doi.org/10.1038/nature03029
Kuna RS, Field SJ (2019) GOLPH3: a Golgi phosphatidylinositol(4)phosphate effector that directs vesicle trafficking and drives cancer. J Lipid Res 60:269–275. https://doi.org/10.1194/jlr.R088328
Kuo SH, Tasset I, Cheng MM, Diaz A, Pan MK, Lieberman OJ, Hutten SJ, Alcalay RN, Kim S, Ximénez-Embún P, Fan L, Kim D, Ko HS, Yacoubian T, Kanter E, Liu L, Tang G, Muñoz J, Sardi SP, Li A, Gan L, Cuervo AM, Sulzer D (2022) Mutant glucocerebrosidase impairs α-synuclein degradation by blockade of chaperone-mediated autophagy. Sci Adv 8:eabm6393. https://doi.org/10.1126/sciadv.abm6393
Lane JD, Lucocq J, Pryde J, Barr FA, Woodman PG, Allan VJ, Lowe M (2002) Caspase-mediated cleavage of the stacking protein GRASP65 is required for Golgi fragmentation during apoptosis. J Cell Biol 156:495–509. https://doi.org/10.1083/jcb.200110007
Lee YH, Kim J, Park K, Lee MS (2019) β-cell autophagy: Mechanism and role in β-cell dysfunction. Mol Metab 27s:S92–S103. https://doi.org/10.1016/j.molmet.2019.06.014
Leidenheimer NJ, Ryder KG (2014) Pharmacological chaperoning: a primer on mechanism and pharmacology. Pharmacol Res 83:10–19. https://doi.org/10.1016/j.phrs.2014.01.005
Lekszas C, Foresti O, Raote I, Liedtke D, König EM, Nanda I, Vona B, De Coster P, Cauwels R, Malhotra V, Haaf T (2020) Biallelic TANGO1 mutations cause a novel syndromal disease due to hampered cellular collagen secretion. Elife. https://doi.org/10.7554/eLife.51319
Lemberg MK, Strisovsky K (2021) Maintenance of organellar protein homeostasis by ER-associated degradation and related mechanisms. Mol Cell 81:2507–2519. https://doi.org/10.1016/j.molcel.2021.05.004
Li H, Zhang P, Luo J, Hu D, Huang Y, Zhang ZR, Fu Y, Gong T (2019) Chondroitin sulfate-linked prodrug nanoparticles target the Golgi apparatus for cancer metastasis treatment. ACS Nano 13:9386–9396. https://doi.org/10.1021/acsnano.9b04166
Li J, Wang Y (2022) Golgi metal ion homeostasis in human health and diseases. Cells 11:289. https://doi.org/10.3390/cells11020289
Li X, Yu J, Gong L, Zhang Y, Dong S, Shi J, Li C, Li Y, Zhang Y, Li H (2021) Heme oxygenase-1(HO-1) regulates Golgi stress and attenuates endotoxin-induced acute lung injury through hypoxia inducible factor-1α (HIF-1α)/HO-1 signaling pathway. Free Radic Biol Med 165:243–253. https://doi.org/10.1016/j.freeradbiomed.2021.01.028
Lin YC, Chiang TC, Liu YT, Tsai YT, Jang LT, Lee FJ (2011) ARL4A acts with GCC185 to modulate Golgi complex organization. J Cell Sci 124:4014–4026. https://doi.org/10.1242/jcs.086892
Linders PTA, Gerretsen ECF, Ashikov A, Vals MA, De Boer R, Revelo NH, Arts R, Baerenfaenger M, Zijlstra F, Huijben K, Raymond K, Muru K, Fjodorova O, Pajusalu S, ×unap K, Ter Beest M, Lefeber D, Van Den Bogaart G (2021) Congenital disorder of glycosylation caused by starting site-specific variant in syntaxin-5. Nat Commun 12:6227. https://doi.org/10.1038/s41467-021-26534-y
Linders PTA, Peters E, Ter Beest M, Lefeber DJ, Van Den Bogaart G (2020) Sugary logistics gone wrong: Membrane trafficking and congenital disorders of glycosylation. Int J Mol Sci 21:4654. https://doi.org/10.3390/ijms21134654
Liu C, Mei M, Li Q, Roboti P, Pang Q, Ying Z, Gao F, Lowe M, Bao S (2017) Loss of the golgin GM130 causes Golgi disruption, Purkinje neuron loss, and ataxia in mice. Proc Natl Acad Sci USA 114:346–351. https://doi.org/10.1073/pnas.1608576114
Liu J, Huang Y, Li T, Jiang Z, Zeng L, Hu Z (2021) The role of the Golgi apparatus in disease (Review). Int J Mol Med. https://doi.org/10.3892/ijmm.2021.4871
Liu Y, Snedecor ER, Choi YJ, Yang N, Zhang X, Xu Y, Han Y, Jones EC, Shroyer KR, Clark RA, Zhang L, Qin C, Chen J (2016) Gorab is required for dermal condensate cells torespond to hedgehog signals during hair follicle morphogenesis. J Investig Dermatol 136:378–386. https://doi.org/10.1016/j.jid.2015.10.067
Lock JG, Hammond LA, Houghton F, Gleeson PA, Stow JL (2005) E-cadherin transport from the trans-Golgi network in tubulovesicular carriers is selectively regulated by golgin-97. Traffic 6:1142–1156. https://doi.org/10.1111/j.1600-0854.2005.00349.x
Lowe M, Lane JD, Woodman PG, Allan VJ (2004) Caspase-mediated cleavage of syntaxin 5 and giantin accompanies inhibition of secretory traffic during apoptosis. J Cell Sci 117:1139–1150. https://doi.org/10.1242/jcs.00950
Lu L, Tai G, Hong W (2004) Autoantigen Golgin-97, an effector of Arl1 GTPase, participates in traffic from the endosome to the trans-golgi network. Mol Biol Cell 15:4426–4443. https://doi.org/10.1091/mbc.e03-12-0872
Lu Q, Wang PS, Yang L (2021) Golgi-associated Rab GTPases implicated in autophagy. Cell Biosci 11:35. https://doi.org/10.1186/s13578-021-00543-2
Machamer CE (2015) The Golgi complex in stress and death. Front Neurosci 9:421. https://doi.org/10.3389/fnins.2015.00421
Magalhães A, Duarte HO, Reis CA (2021) The role of O-glycosylation in human disease. Mol Aspects Med 79:100964. https://doi.org/10.1016/j.mam.2021.100964
Makhoul C, Gosavi P, Duffield R, Delbridge B, Williamson NA, Gleeson PA (2019) Intersectin-1 interacts with the golgin GCC88 to couple the actin network and Golgi architecture. Mol Biol Cell 30:370–386. https://doi.org/10.1091/mbc.E18-05-0313
Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5–21. https://doi.org/10.1016/j.neuron.2004.09.012
Malenka RC, Nicoll RA (1999) Long-term potentiation–a decade of progress? Science 285:1870–1874. https://doi.org/10.1126/science.285.5435.1870
Mancini M, Machamer CE, Roy S, Nicholson DW, Thornberry NA, Casciola-Rosen LA, Rosen A (2000) Caspase-2 is localized at the Golgi complex and cleaves golgin-160 during apoptosis. J Cell Biol 149:603–612. https://doi.org/10.1083/jcb.149.3.603
Mareninova OA, Dillon DL, Wightman CJM, Yakubov I, Takahashi T, Gaisano HY, Munson K, Ohmuraya M, Dawson D, Gukovsky I, Gukovskaya AS (2022) Rab9 mediates pancreatic autophagy switch from canonical to noncanonical, aggravating experimental pancreatitis. Cell Mol Gastroenterol Hepatol 13:599–622. https://doi.org/10.1016/j.jcmgh.2021.09.017
Martínez-Menárguez J, Martínez-Alonso E, Cara-Esteban M, Tomás M (2021) Focus on the small GTPase Rab1: A key player in the pathogenesis of Parkinson’s disease. Int J Mol Sci. https://doi.org/10.3390/ijms222112087
Martínez-Menárguez J, Tomás M, Martínez-Martínez N, Martínez-Alonso E (2019) Golgi fragmentation in neurodegenerative diseases: is there a common cause? Cells 8:748. https://doi.org/10.3390/cells8070748
Mascanzoni F, Iannitti R, Colanzi A (2022) Functional coordination among the Golgi complex, the centrosome and the microtubule cytoskeleton during the cell cycle. Cells 11:354. https://doi.org/10.3390/cells11030354
Micaroni M, Giacchetti G, Plebani R, Xiao GG, Federici L (2016) ATP2C1 gene mutations in Hailey-Hailey disease and possible roles of SPCA1 isoforms in membrane trafficking. Cell Death Dis 7:e2259. https://doi.org/10.1038/cddis.2016.147
Migliano SM, Teis D (2018) ESCRT and membrane protein ubiquitination. Prog Mol Subcell Biol 57:107–135. https://doi.org/10.1007/978-3-319-96704-2_4
Miyata S, Mizuno T, Koyama Y, Katayama T, Tohyama M (2013) The endoplasmic reticulum-resident chaperone heat shock protein 47 protects the Golgi apparatus from the effects of O-glycosylation inhibition. PLoS ONE 8:e69732. https://doi.org/10.1371/journal.pone.0069732
Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451:1069–1075. https://doi.org/10.1038/nature06639
Morishita H, Eguchi S, Kimura H, Sasaki J, Sakamaki Y, Robinson ML, Sasaki T, Mizushima N (2013) Deletion of autophagy-related 5 (Atg5) and Pik3c3 genes in the lens causes cataract independent of programmed organelle degradation. J Biol Chem 288:11436–11447. https://doi.org/10.1074/jbc.M112.437103
Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O’carroll C (2003) Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773–786. https://doi.org/10.1098/rstb.2002.1264
Mourelatos Z, Adler H, Hirano A, Donnenfeld H, Gonatas JO, Gonatas NK (1990) Fragmentation of the Golgi apparatus of motor neurons in amyotrophic lateral sclerosis revealed by organelle-specific antibodies. Proc Natl Acad Sci USA 87:4393–4395. https://doi.org/10.1073/pnas.87.11.4393
Mourelatos Z, Hirano A, Rosenquist AC, Gonatas NK (1994) Fragmentation of the Golgi apparatus of motor neurons in amyotrophic lateral sclerosis (ALS). Clinical studies in ALS of Guam and experimental studies in deafferented neurons and in beta, beta’-iminodipropionitrile axonopathy. Am J Pathol 144:1288–1300
Nardi F, Franco OE, Fitchev P, Morales A, Vickman RE, Hayward SW, Crawford SE (2019) DGAT1 Inhibitor suppresses prostate tumor growth and migration by regulating intracellular lipids and non-centrosomal MTOC protein GM130. Sci Rep 9:3035. https://doi.org/10.1038/s41598-019-39537-z
Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, Shimizu S (2009) Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461:654–658. https://doi.org/10.1038/nature08455
Noguchi S, Shimizu S (2021) Molecular mechanisms and biological roles of GOMED. FEBS J. https://doi.org/10.1111/febs.16281
Nüchel J, Tauber M, Nolte JL, Mörgelin M, Türk C, Eckes B, Demetriades C, Plomann M (2021) An mTORC1-GRASP55 signaling axis controls unconventional secretion to reshape the extracellular proteome upon stress. Mol Cell 81:3275–3293. https://doi.org/10.1016/j.molcel.2021.06.017
Núñez-Olvera SI, Chávez-Munguía B, Del Rocío Terrones-Gurrola MC, Marchat LA, Puente-Rivera J, Ruíz-García E, Campos-Parra AD, Vázquez-Calzada C, Lizárraga-Verdugo ER, Ramos-Payán R, Salinas-Vera YM, López-Camarillo C (2020) A novel protective role for microRNA-3135b in Golgi apparatus fragmentation induced by chemotherapy via GOLPH3/AKT1/mTOR axis in colorectal cancer cells. Sci Rep 10:10555. https://doi.org/10.1038/s41598-020-67550-0
Ohno Y, Kihara A, Sano T, Igarashi Y (2006) Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim Biophys Acta 1761:474–483. https://doi.org/10.1016/j.bbalip.2006.03.010
Oka OBV, Pierre AS, Pringle MA, Tungkum W, Cao Z, Fleming B, Bulleid NJ (2022) Activation of the UPR sensor ATF6α is regulated by its redox-dependent dimerization and ER retention by ERp18. Proc Natl Acad Sci U S A 119:e2122657119. https://doi.org/10.1073/pnas.2122657119
Oliveira-Ferrer L, Legler K, Milde-Langosch K (2017) Role of protein glycosylation in cancer metastasis. Semin Cancer Biol 44:141–152. https://doi.org/10.1016/j.semcancer.2017.03.002
Osaka M, Ito D, Yagi T, Nihei Y, Suzuki N (2015) Evidence of a link between ubiquilin 2 and optineurin in amyotrophic lateral sclerosis. Hum Mol Genet 24:1617–1629. https://doi.org/10.1093/hmg/ddu575
Pachikov AN, Gough RR, Christy CE, Morris ME, Casey CA, Lagrange CA, Bhat G, Kubyshkin AV, Fomochkina Ii, Zyablitskaya EY, Makalish TP, Golubinskaya EP, Davydenko KA, Eremenko SN, Riethoven JM, Maroli AS, Payne TS, Powers R, Lushnikov AY, Macke AJ, Petrosyan A (2021) The non-canonical mechanism of ER stress-mediated progression of prostate cancer. J Exp Clin Cancer Res 40:289. https://doi.org/10.1186/s13046-021-02066-7
Padmanabhan S, Manjithaya R (2020) Facets of autophagy based unconventional protein secretion-the road less traveled. Front Mol Biosci 7:586483. https://doi.org/10.3389/fmolb.2020.586483
Pang Q, Liu C, Qiao Y, Zhao J, Lam SM, Mei M, Shui G, Bao S, Li Q (2022) GM130 regulates pulmonary surfactant protein secretion in alveolar type II cells. Sci China Life Sci 65:193–205. https://doi.org/10.1007/s11427-020-1875-x
Patterson GH, Hirschberg K, Polishchuk RS, Gerlich D, Phair RD, Lippincott-Schwartz J (2008) Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133:1055–1067. https://doi.org/10.1016/j.cell.2008.04.044
Paul BD (2021) Signaling overlap between the Golgi stress response and cysteine metabolism in Huntington’s disease. Antioxidants. https://doi.org/10.3390/antiox10091468
Petrosyan A (2015) Onco-Golgi: is fragmentation a gate to cancer progression? Biochem Mol Biol J. https://doi.org/10.21767/2471-8084.100006
Pinho SS, Reis CA (2015) Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer 15:540–555. https://doi.org/10.1038/nrc3982
Pizzo P, Lissandron V, Pozzan T (2010) The trans-golgi compartment: a new distinct intracellular Ca store. Commun Integr Biol 3:462–464. https://doi.org/10.4161/cib.3.5.12473
Pothukuchi P, Agliarulo I, Pirozzi M, Rizzo R, Russo D, Turacchio G, Nüchel J, Yang JS, Gehin C, Capolupo L, Hernandez-Corbacho MJ, Biswas A, Vanacore G, Dathan N, Nitta T, Henklein P, Thattai M, Inokuchi JI, Hsu VW, Plomann M, Obeid LM, Hannun YA, Luini A, D’angelo G, Parashuraman S (2021) GRASP55 regulates intra-Golgi localization of glycosylation enzymes to control glycosphingolipid biosynthesis. Embo J. https://doi.org/10.15252/embj.2021107766
Prashar A, Schnettger L, Bernard EM, Gutierrez MG (2017) Rab GTPases in Immunity and Inflammation. Front Cell Infect Microbiol 7:435. https://doi.org/10.3389/fcimb.2017.00435
Qiao S, Yang D, Li X, Li W, Zhang Y, Liu W (2021) Silencing PAQR3 protects against oxygen-glucose deprivation/reperfusion-induced neuronal apoptosis via activation of PI3K/AKT signaling in PC12 cells. Life Sci 265:118806. https://doi.org/10.1016/j.lfs.2020.118806
Rajanala K, Klayman LM, Wedegaertner PB (2021) Gβγ regulates mitotic Golgi fragmentation and G2/M cell cycle progression. Mol Biol Cell 32:br2. https://doi.org/10.1091/mbc.E21-04-0175
Ranftler C, Meisslitzer-Ruppitsch C, Neumüller J, Ellinger A, Pavelka M (2017) Golgi apparatus dis- and reorganizations studied with the aid of 2-deoxy-D-glucose and visualized by 3D-electron tomography. Histochem Cell Biol 147:415–438. https://doi.org/10.1007/s00418-016-1515-7
Reiling JH, Olive AJ, Sanyal S, Carette JE, Brummelkamp TR, Ploegh HL, Starnbach MN, Sabatini DM (2013) A CREB3-ARF4 signalling pathway mediates the response to Golgi stress and susceptibility to pathogens. Nat Cell Biol 15:1473–1485. https://doi.org/10.1038/ncb2865
Reily C, Stewart TJ, Renfrow MB, Novak J (2019) Glycosylation in health and disease. Nat Rev Nephrol 15:346–366. https://doi.org/10.1038/s41581-019-0129-4
Rendón WO, Martínez-Alonso E, Tomás M, Martínez-Martínez N, Martínez-Menárguez JA (2013) Golgi fragmentation is Rab and SNARE dependent in cellular models of Parkinson’s disease. Histochem Cell Biol 139:671–684. https://doi.org/10.1007/s00418-012-1059-4
Rivinoja A, Pujol FM, Hassinen A, Kellokumpu S (2012) Golgi pH, its regulation and roles in human disease. Ann Med 44:542–554. https://doi.org/10.3109/07853890.2011.579150
Roboti P, Sato K, Lowe M (2015) The golgin GMAP-210 is required for efficient membrane trafficking in the early secretory pathway. J Cell Sci 128:1595–1606. https://doi.org/10.1242/jcs.166710
Rong X, Liu C, Li M, Zhu H, Zhang Y, Su M, Wang X, Li X, Wang K, Yu M, Sheng W, Zhu B (2021) An integrated fluorescent probe for ratiometric detection of glutathione in the Golgi apparatus and activated organelle-targeted therapy. Anal Chem 93:16105–16112. https://doi.org/10.1021/acs.analchem.1c03836
Saito T, Nah J, Oka SI, Mukai R, Monden Y, Maejima Y, Ikeda Y, Sciarretta S, Liu T, Li H, Baljinnyam E, Fraidenraich D, Fritzky L, Zhai P, Ichinose S, Isobe M, Hsu CP, Kundu M, Sadoshima J (2019) An alternative mitophagy pathway mediated by Rab9 protects the heart against ischemia. J Clin Investig 129:802–819. https://doi.org/10.1172/jci122035
Sakurai A, Okamoto K, Fujita Y, Nakazato Y, Wakabayashi K, Takahashi H, Gonatas NK (2000) Fragmentation of the Golgi apparatus of the ballooned neurons in patients with corticobasal degeneration and Creutzfeldt-Jakob disease. Acta Neuropathol 100:270–274. https://doi.org/10.1007/s004010000182
Saraceno C, Marcello E, Di Marino D, Borroni B, Claeysen S, Perroy J, Padovani A, Tramontano A, Gardoni F, Di Luca M (2014) SAP97-mediated ADAM10 trafficking from Golgi outposts depends on PKC phosphorylation. Cell Death Dis 5:e1547. https://doi.org/10.1038/cddis.2014.492
Saraste J, Prydz K (2019) A new look at the functional organization of the Golgi ribbon. Front Cell Dev Biol 7:171. https://doi.org/10.3389/fcell.2019.00171
Sasaki K, Yoshida H (2015) Organelle autoregulation-stress responses in the ER, Golgi, mitochondria and lysosome. J Biochem 157:185–195. https://doi.org/10.1093/jb/mvv010
Sasaki K, Yoshida H (2019) Golgi stress response and organelle zones. FEBS Lett 593:2330–2340. https://doi.org/10.1002/1873-3468.13554
Satoh A, Hayashi-Nishino M, Shakuno T, Masuda J, Koreishi M, Murakami R, Nakamura Y, Nakamura T, Abe-Kanoh N, Honjo Y, Malsam J, Yu S, Nishino K (2019) The golgin protein giantin regulates interconnections between Golgi stacks. Front Cell Dev Biol 7:160. https://doi.org/10.3389/fcell.2019.00160
Sbodio JI, Snyder SH, Paul BD (2018) Golgi stress response reprograms cysteine metabolism to confer cytoprotection in Huntington’s disease. Proc Natl Acad Sci USA 115:780–785. https://doi.org/10.1073/pnas.1717877115
Schedin-Weiss S, Gaunitz S, Sui P, Chen Q, Haslam SM, Blennow K, Winblad B, Dell A, Tjernberg LO (2020) Glycan biomarkers for Alzheimer disease correlate with T-tau and P-tau in cerebrospinal fluid in subjective cognitive impairment. FEBS J 287:3221–3234. https://doi.org/10.1111/febs.15197
Schmidt O, Weyer Y, Baumann V, Widerin MA, Eising S, Angelova M, Schleiffer A, Kremser L, Lindner H, Peter M, Fröhlich F, Teis D (2019) Endosome and Golgi-associated degradation (EGAD) of membrane proteins regulates sphingolipid metabolism. EMBO J 38:e101433. https://doi.org/10.15252/embj.2018101433
Schultz MJ, Holdbrooks AT, Chakraborty A, Grizzle WE, Landen CN, Buchsbaum DJ, Conner MG, Arend RC, Yoon KJ, Klug CA, Bullard DC, Kesterson RA, Oliver PG, O’connor AK, Yoder BK, Bellis SL (2016) The tumor-associated glycosyltransferase ST6Gal-I regulates stem cell transcription factors and confers a cancer stem cell phenotype. Cancer Res 76:3978–3988. https://doi.org/10.1158/0008-5472.Can-15-2834
Sechi S, Frappaolo A, Karimpour-Ghahnavieh A, Piergentili R, Giansanti MG (2020) Oncogenic roles of GOLPH3 in the physiopathology of cancer. Int J Mol Sci. https://doi.org/10.3390/ijms21030933
Sehgal K, Barbie DA (2021) Targeting the mutant p53 secretome. J Clin Investig. https://doi.org/10.1172/jci143945
Seo BA, Cho T, Lee DZ, Lee JJ, Lee B, Kim SW, Shin HS, Kang MG (2018) LARGE, an intellectual disability-associated protein, regulates AMPA-type glutamate receptor trafficking and memory. Proc Natl Acad Sci USA 115:7111–7116. https://doi.org/10.1073/pnas.1805060115
Shestakova A, Zolov S, Lupashin V (2006) COG complex-mediated recycling of Golgi glycosyltransferases is essential for normal protein glycosylation. Traffic 7:191–204. https://doi.org/10.1111/j.1600-0854.2005.00376.x
Shorter J, Watson R, Giannakou ME, Clarke M, Warren G, Barr FA (1999) GRASP55, a second mammalian GRASP protein involved in the stacking of Golgi cisternae in a cell-free system. EMBO J 18:4949–4960. https://doi.org/10.1093/emboj/18.18.4949
Sicari D, Igbaria A, Chevet E (2019) Control of protein homeostasis in the early secretory pathway: current status and challenges. Cells. https://doi.org/10.3390/cells8111347
Stalder D, Gershlick DC (2020) Direct trafficking pathways from the Golgi apparatus to the plasma membrane. Semin Cell Dev Biol 107:112–125. https://doi.org/10.1016/j.semcdb.2020.04.001
Stanley P (2011) Golgi glycosylation. Cold Spring Harb Perspect Biol 3:a005199. https://doi.org/10.1101/cshperspect.a005199
Starr T, Sun Y, Wilkins N, Storrie B (2010) Rab33b and Rab6 are functionally overlapping regulators of Golgi homeostasis and trafficking. Traffic 11:626–636. https://doi.org/10.1111/j.1600-0854.2010.01051.x
Steele S, Brunton J, Ziehr B, Taft-Benz S, Moorman N, Kawula T (2013) Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLoS Pathog 9:e1003562. https://doi.org/10.1371/journal.ppat.1003562
Stevenson NL, Bergen DJM, Lu Y, Prada-Sanchez ME, Kadler KE, Hammond CL, Stephens DJ (2021) Giantin is required for intracellular N-terminal processing of type I procollagen. J Cell Biol 220:e202005166. https://doi.org/10.1083/jcb.202005166
Stieber A, Chen Y, Wei S, Mourelatos Z, Gonatas J, Okamoto K, Gonatas NK (1998) The fragmented neuronal Golgi apparatus in amyotrophic lateral sclerosis includes the trans-Golgi-network: functional implications. Acta Neuropathol 95:245–253. https://doi.org/10.1007/s004010050794
Stieber A, Mourelatos Z, Gonatas NK (1996) In Alzheimer’s disease the Golgi apparatus of a population of neurons without neurofibrillary tangles is fragmented and atrophic. Am J Pathol 148:415–426
Storrie B (2005) Maintenance of Golgi apparatus structure in the face of continuous protein recycling to the endoplasmic reticulum: making ends meet. Int Rev Cytol 244:69–94. https://doi.org/10.1016/s0074-7696(05)44002-4
Szabo MP, Mishra S, Knupp A, Young JE (2022) The role of Alzheimer’s disease risk genes in endolysosomal pathways. Neurobiol Dis 162:105576. https://doi.org/10.1016/j.nbd.2021.105576
Tammineni P, Ye X, Feng T, Aikal D, Cai Q (2017) Impaired retrograde transport of axonal autophagosomes contributes to autophagic stress in Alzheimer’s disease neurons. Elife 6:e21776. https://doi.org/10.7554/eLife.21776
Tan X, Banerjee P, Guo HF, Ireland S, Pankova D, Ahn YH, Nikolaidis IM, Liu X, Zhao Y, Xue Y, Burns AR, Roybal J, Gibbons DL, Zal T, Creighton CJ, Ungar D, Wang Y, Kurie JM (2017) Epithelial-to-mesenchymal transition drives a pro-metastatic Golgi compaction process through scaffolding protein PAQR11. J Clin Investig 127:117–131. https://doi.org/10.1172/jci88736
Tan X, Shi L, Banerjee P, Liu X, Guo HF, Yu J, Bota-Rabassedas N, Rodriguez BL, Gibbons DL, Russell WK, Creighton CJ, Kurie JM (2021) A protumorigenic secretory pathway activated by p53 deficiency in lung adenocarcinoma. J Clin Investig. https://doi.org/10.1172/jci137186
Tang CX, Luan L, Zhang L, Wang Y, Liu XF, Wang J, Xiong Y, Wang D, Huang LY, Gao DS (2019) Golgin-160 and GMAP210 play an important role in U251 cells migration and invasion initiated by GDNF. PLoS ONE 14:e0211501. https://doi.org/10.1371/journal.pone.0211501
Thomas LL, Fromme JC (2020) Extensive GTPase crosstalk regulates Golgi trafficking and maturation. Curr Opin Cell Biol 65:1–7. https://doi.org/10.1016/j.ceb.2020.01.014
Tie HC, Mahajan D, Chen B, Cheng L, Vandongen AM, Lu L (2016) A novel imaging method for quantitative Golgi localization reveals differential intra-Golgi trafficking of secretory cargoes. Mol Biol Cell 27:848–861. https://doi.org/10.1091/mbc.E15-09-0664
Tomás M, Martínez-Alonso E, Martínez-Martínez N, Cara-Esteban M, Martínez-Menárguez JA (2021) Fragmentation of the Golgi complex of dopaminergic neurons in human substantia nigra: New cytopathological findings in Parkinson’s disease. Histol Histopathol 36:47–60. https://doi.org/10.14670/hh-18-270
Utar Z, Majid MIA, Adenan MI, Jamil MFA, Lan TM (2011) Mitragynine inhibits the COX-2 mRNA expression and prostaglandin E2 production induced by lipopolysaccharide in RAW264.7 macrophage cells. J Ethnopharmacol 136:75–82. https://doi.org/10.1016/j.jep.2011.04.011
Valenzuela A, Meservey L, Nguyen H, Fu MM (2020) Golgi outposts nucleate microtubules in cells with specialized shapes. Trends Cell Biol 30:792–804. https://doi.org/10.1016/j.tcb.2020.07.004
Van Ziel AM, Largo-Barrientos P, Wolzak K, Verhage M, Scheper W (2019) Unconventional secretion factor GRASP55 is increased by pharmacological unfolded protein response inducers in neurons. Sci Rep 9:1567. https://doi.org/10.1038/s41598-018-38146-6
Verhage M, Sørensen JB (2020) SNAREopathies: diversity in mechanisms and symptoms. Neuron 107:22–37. https://doi.org/10.1016/j.neuron.2020.05.036
Verheijen J, Tahata S, Kozicz T, Witters P, Morava E (2020) Therapeutic approaches in Congenital Disorders of Glycosylation (CDG) involving N-linked glycosylation: an update. Genet Med 22:268–279. https://doi.org/10.1038/s41436-019-0647-2
Viettri M, Zambrano JL, Rosales R, Caraballo GI, Gutiérrez-Escolano AL, Ludert JE (2021) Flavivirus infections induce a Golgi stress response in vertebrate and mosquito cells. Sci Rep 11:23489. https://doi.org/10.1038/s41598-021-02929-1
Vitória JJM, Trigo D, Da Cruz ESOAB (2022) Revisiting APP secretases: an overview on the holistic effects of retinoic acid receptor stimulation in APP processing. Cell Mol Life Sci 79:101. https://doi.org/10.1007/s00018-021-04090-4
Walker A, Ward C, Sheldrake TA, Dransfield I, Rossi AG, Pryde JG, Haslett C (2004) Golgi fragmentation during Fas-mediated apoptosis is associated with the rapid loss of GM130. Biochem Biophys Res Commun 316:6–11. https://doi.org/10.1016/j.bbrc.2004.02.015
Wang B, Stanford KR, Kundu M (2020a) ER-to-Golgi trafficking and its implication in neurological diseases. Cells 9:408. https://doi.org/10.3390/cells9020408
Wang F, Chen X, Yuan D, Yi Y, Luo Y (2019) Golgi reassembly and stacking protein 65 downregulation is required for the anti-cancer effect of dihydromyricetin on human ovarian cancer cells. PLoS ONE 14:e0225450. https://doi.org/10.1371/journal.pone.0225450
Wang J, Fourriere L, Gleeson PA (2020b) Local secretory yrafficking pathways in neurons and the role of dendritic Golgi outposts in different cell models. Front Mol Neurosci 13:597391. https://doi.org/10.3389/fnmol.2020.597391
Wang M, Zhang Y, Komaniecki GP, Lu X, Cao J, Zhang M, Yu T, Hou D, Spiegelman NA, Yang M, Price IR, Lin H (2022) Golgi stress induces SIRT2 to counteract Shigella infection via defatty-acylation. Nat Commun 13:4494. https://doi.org/10.1038/s41467-022-32227-x
Watkin LB, Jessen B, Wiszniewski W, Vece TJ, Jan M, Sha Y, Thamsen M, Santos-Cortez RL, Lee K, Gambin T, Forbes LR, Law CS, Stray-Pedersen A, Cheng MH, Mace EM, Anderson MS, Liu D, Tang LF, Nicholas SK, Nahmod K, Makedonas G, Canter DL, Kwok PY, Hicks J, Jones KD, Penney S, Jhangiani SN, Rosenblum MD, Dell SD, Waterfield MR, Papa FR, Muzny DM, Zaitlen N, Leal SM, Gonzaga-Jauregui C, Boerwinkle E, Eissa NT, Gibbs RA, Lupski JR, Orange JS, Shum AK (2015) COPA mutations impair ER-Golgi transport and cause hereditary autoimmune-mediated lung disease and arthritis. Nat Genet 47:654–660. https://doi.org/10.1038/ng.3279
Wei JH, Seemann J (2017) Golgi ribbon disassembly during mitosis, differentiation and disease progression. Curr Opin Cell Biol 47:43–51. https://doi.org/10.1016/j.ceb.2017.03.008
Welch LG, Peak-Chew SY, Begum F, Stevens TJ, Munro S (2021) GOLPH3 and GOLPH3L are broad-spectrum COPI adaptors for sorting into intra-Golgi transport vesicles. J Cell Biol. https://doi.org/10.1083/jcb.202106115
Witkos TM, Lowe M (2017) Recognition and tethering of transport vesicles at the Golgi apparatus. Curr Opin Cell Biol 47:16–23. https://doi.org/10.1016/j.ceb.2017.02.003
Wu H, Li T, Zhao J (2020) GRASP55: A multifunctional protein. Curr Protein Pept Sci 21:544–552. https://doi.org/10.2174/1389203721666200218105302
Wu H, Zhao J (2019) Disruption of the Golgi apparatus mediates zinc deficiency-induced impairment of cognitive function in mice. Metallomics 11:1984–1987. https://doi.org/10.1039/c9mt00252a
Xiang Y, Zhang X, Nix DB, Katoh T, Aoki K, Tiemeyer M, Wang Y (2013) Regulation of protein glycosylation and sorting by the Golgi matrix proteins GRASP55/65. Nat Commun 4:1659. https://doi.org/10.1038/ncomms2669
Xue F, Wen Y, Wei P, Gao Y, Zhou Z, Xiao S, Yi T (2017) A smart drug: a pH-responsive photothermal ablation agent for Golgi apparatus activated cancer therapy. Chem Commun (camb) 53:6424–6427. https://doi.org/10.1039/c7cc03168h
Yadav S, Puthenveedu MA, Linstedt AD (2012) Golgin160 recruits the dynein motor to position the Golgi apparatus. Dev Cell 23:153–165. https://doi.org/10.1016/j.devcel.2012.05.023
Yamaguchi H, Arakawa S, Kanaseki T, Miyatsuka T, Fujitani Y, Watada H, Tsujimoto Y, Shimizu S (2016) Golgi membrane-associated degradation pathway in yeast and mammals. EMBO J 35:1991–2007. https://doi.org/10.15252/embj.201593191
Yamaguchi H, Honda S, Torii S, Shimizu K, Katoh K, Miyake K, Miyake N, Fujikake N, Sakurai HT, Arakawa S, Shimizu S (2020) Wipi3 is essential for alternative autophagy and its loss causes neurodegeneration. Nat Commun 11:5311. https://doi.org/10.1038/s41467-020-18892-w
Yamaguchi H, Meyer MD, He L, Komatsu Y (2022) Disruption of Trip11 in cranial neural crest cells is associated with increased ER and Golgi stress contributing to skull defects in mice. Dev Dyn. https://doi.org/10.1002/dvdy.461
Yamashita S, Ando Y (2015) Genotype-phenotype relationship in hereditary amyotrophic lateral sclerosis. Transl Neurodegener 4:13. https://doi.org/10.1186/s40035-015-0036-y
Yan R, Chen K, Wang B, Xu K (2022) SURF4-induced tubular ERGIC selectively expedites ER-to-Golgi transport. Dev Cell 57:512–525. https://doi.org/10.1016/j.devcel.2021.12.018
Yang K, Liu M, Feng Z, Rojas M, Zhou L, Ke H, Pastor-Pareja JC (2021a) ER exit sites in Drosophila display abundant ER-Golgi vesicles and pearled tubes but no megacarriers. Cell Rep 36:109707. https://doi.org/10.1016/j.celrep.2021.109707
Yang L, Liu G, Li X, Xia Z, Wang Y, Lin W, Zhang W, Zhang W, Li X (2020) Small GTPase RAB6 deficiency promotes alveolar progenitor cell renewal and attenuates PM2.5-induced lung injury and fibrosis. Cell Death Dis 11:827. https://doi.org/10.1038/s41419-020-03027-2
Yang X, Reist L, Chomchai DA, Chen L, Arines FM, Li M (2021b) ESCRT, not intralumenal fragments, sorts ubiquitinated vacuole membrane proteins for degradation. J Cell Biol 220:e202012104. https://doi.org/10.1083/jcb.202012104
Zhang M, Zhou L, Xu Y, Yang M, Xu Y, Komaniecki GP, Kosciuk T, Chen X, Lu X, Zou X, Linder ME, Lin H (2020a) A STAT3 palmitoylation cycle promotes T(H)17 differentiation and colitis. Nature 586:434–439. https://doi.org/10.1038/s41586-020-2799-2
Zhang Q, Ma C, Chin LS, Li L (2020b) Integrative glycoproteomics reveals protein N-glycosylation aberrations and glycoproteomic network alterations in Alzheimer’s disease. Sci Adv 6:eabc5802. https://doi.org/10.1126/sciadv.abc5802
Zhang X, Wang L, Lak B, Li J, Jokitalo E, Wang Y (2018) GRASP55 senses glucose deprivation through O-GlcNAcylation to promote autophagosome-lysosome fusion. Dev Cell 45:245–61.e6. https://doi.org/10.1016/j.devcel.2018.03.023
Zhang X, Wang Y (2016) Glycosylation quality control by the Golgi structure. J Mol Biol 428:3183–3193. https://doi.org/10.1016/j.jmb.2016.02.030
Zhang X, Wang Y (2018) The Golgi stacking protein GORASP2/GRASP55 serves as an energy sensor to promote autophagosome maturation under glucose starvation. Autophagy 14:1649–1651. https://doi.org/10.1080/15548627.2018.1491214
Zhang X, Wang Y (2020) Nonredundant roles of GRASP55 and GRASP65 in the Golgi apparatus and beyond. Trends Biochem Sci 45:1065–1079. https://doi.org/10.1016/j.tibs.2020.08.001
Zhang Y, Seemann J (2021) Rapid degradation of GRASP55 and GRASP65 reveals their immediate impact on the Golgi structure. J Cell Biol. https://doi.org/10.1083/jcb.202007052
Zhou A, Zhang W, Dong X, Tang B (2021) Porcine genome-wide CRISPR screen identifies the Golgi apparatus complex protein COG8 as a pivotal regulator of influenza virus infection. CRISPR J 4:872–883. https://doi.org/10.1089/crispr.2021.0054
Zhu BL, Xie CL, Hu NN, Zhu XB, Liu CF (2018) Inhibiting of GRASP65 phosphorylation by DL-3-N-Butylphthalide protects against cerebral ischemia-reperfusion injury via ERK signaling. Behav Neurol 2018:5701719. https://doi.org/10.1155/2018/5701719
Acknowledgements
This work was supported by the National Research Foundation (NRF) funded by the Ministry of Science and ICT, Republic of Korea (No. 2021R1C1C1008587), the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) and Korea Dementia Research Center (KDRC) funded by the Ministry of Health & Welfare and Ministry of Science and ICT, Republic of Korea (No. HU22C0069), and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health & Welfare, Republic of Korea (No. HI22C1236). We thank Dong Soo Chang for providing assistance with the illustrations.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interest
The authors declare no competing or financial interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Choi, W., Kang, S. & Kim, J. New insights into the role of the Golgi apparatus in the pathogenesis and therapeutics of human diseases. Arch. Pharm. Res. 45, 671–692 (2022). https://doi.org/10.1007/s12272-022-01408-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12272-022-01408-z