Abstract
The nucleus is a complex organelle with functions beyond being a simple repository for genomic material. For example, its actions in biomechanical sensing, protein synthesis, and epigenomic regulation showcase how the nucleus integrates multiple signaling modalities to intricately regulate gene expression. This innate dynamism is underscored by subnuclear components that facilitate these roles, with elements of the nucleoskeleton, phase-separated nuclear bodies, and chromatin safeguarding by nuclear envelope proteins providing examples of this functional diversity. Among these, one of the lesser characterized nuclear organelles is the nucleolar channel system (NCS), first reported several decades ago in human endometrial biopsies. This tubular structure, believed to be derived from the inner nuclear membrane of the nuclear envelope, was first observed in secretory endometrial cells during a specific phase of the menstrual cycle. Reported as a consistent, yet transient, nuclear organelle, current interpretations of existing data suggest that it serves as a marker of a window for optimal implantation. In spite of this available data, the NCS remains incompletely characterized structurally and functionally, due in part to its transient spatial and temporal expression. As a further complication, evidence exists showing NCS expression in fetal tissue, suggesting that it may not act exclusively as a marker of uterine receptivity, but rather as a hormone sensor sensitive to estrogen and progesterone ratios. To gain a better understanding of the NCS, current technologies can be applied to profile rare cell populations or capture transient structural dynamics, for example, at a level of sensitivity and resolution not previously possible. Moving forward, advanced characterization of the NCS will shed light on an uncharacterized aspect of reproductive physiology, with the potential to refine assisted reproductive techniques.
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References
Aflatoonian A, Baradaran Bagheri R, Hosseinisadat R (2016) The effect of endometrial injury on pregnancy rate in frozen-thawed embryo transfer: A randomized control trial. Int J Reprod Biomed. 14(7):453–158. Epub 2016/08/16. PubMed PMID: 27525329; PMCID: PMC4971562
Malashicheva A, Perepelina K (2021) Diversity of nuclear lamin A/C action as a key to tissue-specific regulation of cellular identity in health and disease. Front Cell Dev Biol 9:761469. Epub 2021/11/02. https://doi.org/10.3389/fcell.2021.761469. PubMed PMID: 34722546; PMCID: PMC8548693
Pawar S, Kutay U (2021) The diverse cellular functions of inner nuclear membrane proteins. Cold Spring Harb Perspect Biol 13(9):a040477. Epub 2021/03/24. https://doi.org/10.1101/cshperspect.a040477. PubMed PMID: 33753404; PMCID: PMC8411953
Antoku S, Gundersen GG (2018) Analysis of Nesprin-2 interaction with its binding partners and actin. Methods Mol Biol 1840:35–43. Epub 2018/08/25. https://doi.org/10.1007/978-1-4939-8691-0_4
Banerjee I, Zhang J, Moore-Morris T, Pfeiffer E, Buchholz KS, Liu A, Ouyang K, Stroud MJ, Gerace L, Evans SM, McCulloch A, Chen J (2014) Targeted ablation of nesprin 1 and nesprin 2 from murine myocardium results in cardiomyopathy, altered nuclear morphology and inhibition of the biomechanical gene response. PLoS Genet 10(2):e1004114. Epub 2014/03/04. https://doi.org/10.1371/journal.pgen.1004114. PubMed PMID: 24586179; PMCID: PMC3930490
Jahed Z, Domkam N, Ornowski J, Yerima G, Mofrad MRK (2021) Molecular models of LINC complex assembly at the nuclear envelope. J Cell Sci 134(12):jcs258194. Epub 2021/06/22. https://doi.org/10.1242/jcs.258194
Preston CC, Faustino RS (2018) Nuclear envelope regulation of oncogenic processes: roles in pancreatic cancer. Epigenomes 2(3):15. Epub 2018/09/01. https://doi.org/10.3390/epigenomes2030015. PubMed PMID: 31867128; PMCID: PMC6924619
Secondo A, Petrozziello T, Tedeschi V, Boscia F, Pannaccione A, Molinaro P, Annunziato L (2020) Nuclear localization of NCX: role in ca(2+) handling and pathophysiological implications. Cell Calcium 86:102143. Epub 2019/12/23. https://doi.org/10.1016/j.ceca.2019.102143
Mauger JP (2012) Role of the nuclear envelope in calcium signalling. Biol Cell 104(2):70–83. Epub 2011/12/23. https://doi.org/10.1111/boc.201100103
Alonso MT, Villalobos C, Chamero P, Alvarez J, Garcia-Sancho J (2006) Calcium microdomains in mitochondria and nucleus. Cell Calcium 40(5–6):513–525. Epub 2006/10/28. https://doi.org/10.1016/j.ceca.2006.08.013
Chowdhury R, Sau A, Musser SM (2022) Super-resolved 3D tracking of cargo transport through nuclear pore complexes. Nat Cell Biol 24(1):112–22. Epub 2022/01/12. https://doi.org/10.1038/s41556-021-00815-6. PubMed PMID: 35013558; PMCID: PMC8820391
Burdine RD, Preston CC, Leonard RJ, Bradley TA, Faustino RS (2020) Nucleoporins in cardiovascular disease. J Mol Cell Cardiol 141:43–52. Epub 2020/03/27. https://doi.org/10.1016/j.yjmcc.2020.02.010. PubMed PMID: 32209327; PMCID: PMC7394472
Pascual-Garcia P, Capelson M (2021) The nuclear pore complex and the genome: organizing and regulatory principles. Curr Opin Genet Dev 67:142–50. Epub 2021/02/09. https://doi.org/10.1016/j.gde.2021.01.005. PubMed PMID: 33556822; PMCID: PMC8084963
Guglielmi V, Sakuma S, D'Angelo MA (2020) Nuclear pore complexes in development and tissue homeostasis. Development 147(23):dev183442. Epub 2020/12/17. https://doi.org/10.1242/dev.183442. PubMed PMID: 33323374; PMCID: PMC7758637
Capitanchik C, Dixon CR, Swanson SK, Florens L, Kerr ARW, Schirmer EC (2018) Analysis of RNA-Seq datasets reveals enrichment of tissue-specific splice variants for nuclear envelope proteins. Nucleus 9(1):410–30. Epub 2018/06/19. https://doi.org/10.1080/19491034.2018.1469351. PubMed PMID: 29912636; PMCID: PMC7000147
Sakuma S, Zhu EY, Raices M, Zhang P, Murad R, D'Angelo MA (2022) Loss of Nup210 results in muscle repair delays and age-associated alterations in muscle integrity. Life Sci Alliance 5(3):e202101216. Epub 2021/12/17. https://doi.org/10.26508/lsa.202101216. PubMed PMID: 34911810; PMCID: PMC8711851
Srivastava LK, Ju Z, Ghagre A, Ehrlicher AJ (2021) Spatial distribution of lamin A/C determines nuclear stiffness and stress-mediated deformation. J Cell Sci 134(10):jcs248559. Epub 2021/05/25. https://doi.org/10.1242/jcs.248559. PubMed PMID: 34028539; PMCID: PMC8186481
Fiserova J, Maninova M, Sieger T, Uhlirova J, Sebestova L, Efenberkova M, Capek M, Fiser K, Hozak P (2019) Nuclear pore protein TPR associates with Lamin B1 and affects nuclear lamina organization and nuclear pore distribution. Cell Mol Life Sci 76(11):2199–2216. Epub 2019/02/15. https://doi.org/10.1007/s00018-019-03037-0
Goelzer M, Goelzer J, Ferguson ML, Neu CP, Uzer G (2021) Nuclear envelope mechanobiology: linking the nuclear structure and function. Nucleus 12(1):90–114. Epub 2021/08/31. https://doi.org/10.1080/19491034.2021.1962610. PubMed PMID: 34455929; PMCID: PMC8432354
Wong X, Loo TH, Stewart CL (2021) LINC complex regulation of genome organization and function. Curr Opin Genet Dev 67:130–141. Epub 2021/02/02. https://doi.org/10.1016/j.gde.2020.12.007
Khilan AA, Al-Maslamani NA, Horn HF (2021) Cell stretchers and the LINC complex in mechanotransduction. Arch Biochem Biophys 702:108829. Epub 2021/03/16. https://doi.org/10.1016/j.abb.2021.108829
Haque F, Mazzeo D, Patel JT, Smallwood DT, Ellis JA, Shanahan CM, Shackleton S (2010) Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J Biol Chem 285(5):3487–98. Epub 2009/11/26. https://doi.org/10.1074/jbc.M109.071910. PubMed PMID: 19933576; PMCID: PMC2823409
Cruz VE, Esra Demircioglu F, Schwartz TU (2020) Structural analysis of different LINC complexes reveals distinct binding modes. J Mol Biol 432(23):6028–6041. Epub 2020/10/16. https://doi.org/10.1016/j.jmb.2020.09.019
Jahed Z, Fadavi D, Vu UT, Asgari E, Luxton GWG, Mofrad MRK (2018) Molecular insights into the mechanisms of SUN1 oligomerization in the nuclear envelope. Biophys J 114(5):1190–203. Epub 2018/03/15. https://doi.org/10.1016/j.bpj.2018.01.015. PubMed PMID: 29539404; PMCID: PMC5883562
Cornillie FJ, Lauweryns JM, Brosens IA (1985) Normal human endometrium. An ultrastructural survey. Gynecol Obstet Investig 20(3):113–129. Epub 1985/01/01. https://doi.org/10.1159/000298983
More IA, Armstrong EM, McSeveney D, Chatfield WR (1974) The morphogenesis and fate of the nucleolar channel system in the human endometrial glandular cell. J Ultrastruct Res 47(20):74–85. Epub 1974/04/01. https://doi.org/10.1016/s0022-5320(74)90027-6
Clyman MJ (1963) A new structure observed in the nucleolus of the human endometrial epithelial cell. Am J Obstet Gynecol 86:430–432. Epub 1963/06/15. https://doi.org/10.1016/0002-9378(63)90166-2
Terzakis JA (1965) The nucleolar channel system of human endometrium. J Cell Biol 27(2):293–304. Epub 1965/11/01. https://doi.org/10.1083/jcb.27.2.293. PubMed PMID: 5884628; PMCID: PMC2106727
Kohorn EI, Rice SI, Gordon M (1970) In vitro production of nucleolar channel system by progesterone in human endometrium. Nature 228(5272):671–672. Epub 1970/11/14. https://doi.org/10.1038/228671a0
Kittur N, Zapantis G, Aubuchon M, Santoro N, Bazett-Jones DP, Meier UT (2007) The nucleolar channel system of human endometrium is related to endoplasmic reticulum and R-rings. Mol Biol Cell 18(6):2296–304. Epub 2007/04/13. https://doi.org/10.1091/mbc.e07-02-0154. PubMed PMID: 17429075; PMCID: PMC1877118
Wang T, Schneider J (1992) Origin and fate of the nucleolar channel system of normal human endometrium. Cell Res 2(2):97–102. https://doi.org/10.1038/cr.1992.10
Guffanti E, Kittur N, Brodt ZN, Polotsky AJ, Kuokkanen SM, Heller DS, Young SL, Santoro N, Meier UT (2008) Nuclear pore complex proteins mark the implantation window in human endometrium. J Cell Sci 121(Pt 12):2037–45. Epub 2008/05/29. https://doi.org/10.1242/jcs.030437. PubMed PMID: 18505792; PMCID: PMC2657873
Ryder TA, Mobberley MA, Whitehead MI (1995) The endometrial nucleolar channel system as an indicator of progestin potency in HRT. Maturitas 22(1):31–36. Epub 1995/06/01. https://doi.org/10.1016/0378-5122(95)00912-5
Gerber RS, Buyuk E, Zapantis G, Lieman H, Meier UT (2021) Presence of endometrial nucleolar channel systems at the time of frozen embryo transfer in hormone replacement cycles with successful implantation. F S Sci 2(1):80–7. Epub 2022/02/15. https://doi.org/10.1016/j.xfss.2021.01.001. PubMed PMID: 35156063; PMCID: PMC8829816
More IA, McSeveney D (1980) The three dimensional structure of the nucleolar channel system in the endometrial glandular cell: serial sectioning and high voltage electron microscopic studies. J Anat 130(Pt 4):673–82. Epub 1980/06/01. PubMed PMID: 7000735; PMCID: PMC1233194
Wang T (1987) Nucleolar channel system in the human fetal endometrium. Eur J Obstet Gynecol Reprod Biol 24(4):271–275. Epub 1987/04/01. https://doi.org/10.1016/0028-2243(87)90151-1
Wang T (1989) Human fetal endometrium--light and electron microscopic study. Arch Gynecol Obstet 246(3):169–179. Epub 1989/01/01. https://doi.org/10.1007/bf00934078
Zapantis G, Szmyga MJ, Rybak EA, Meier UT (2013) Premature formation of nucleolar channel systems indicates advanced endometrial maturation following controlled ovarian hyperstimulation. Hum Reprod 28(12):3292–300. Epub 2013/09/21. https://doi.org/10.1093/humrep/det358. PubMed PMID: 24052503; PMCID: PMC3895983
Sarmento MJ, Oneto M, Pelicci S, Pesce L, Scipioni L, Faretta M, Furia L, Dellino GI, Pelicci PG, Bianchini P, Diaspro A, Lanzano L (2018) Exploiting the tunability of stimulated emission depletion microscopy for super-resolution imaging of nuclear structures. Nat Commun 9(1):3415. Epub 2018/08/26. https://doi.org/10.1038/s41467-018-05963-2. PubMed PMID: 30143630; PMCID: PMC6109149
Rybak EA, Szmyga MJ, Zapantis G, Rausch M, Beshay VE, Polotsky AJ, Coutifaris C, Carr BR, Santoro N, Meier UT (2011) The nucleolar channel system reliably marks the midluteal endometrium regardless of fertility status: a fresh look at an old organelle. Fertil Steril 95(4):1385–9 e1. Epub 2010/11/12. https://doi.org/10.1016/j.fertnstert.2010.10.030. PubMed PMID: 21067716; PMCID: PMC3347775
Meng F, Zapantis G, Williams SZ, Lieman HJ, Buyuk E, Meier UT (2018) Status of nucleolar channel systems in uterine secretions accurately reflects their prevalence-a marker for the window of implantation-in simultaneously obtained endometrial biopsies. Fertil Steril 109(1):165–171. Epub 2017/11/28. https://doi.org/10.1016/j.fertnstert.2017.10.005
Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, Kner P, Burke B, Cardoso MC, Agard DA, Gustafsson MG, Leonhardt H, Sedat JW (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320(5881):1332–6. Epub 2008/06/07. https://doi.org/10.1126/science.1156947. PubMed PMID: 18535242; PMCID: PMC2916659
Bilokapic S, Schwartz TU (2012) 3D ultrastructure of the nuclear pore complex. Curr Opin Cell Biol 24(1):86–91. Epub 2012/01/17. https://doi.org/10.1016/j.ceb.2011.12.011. PubMed PMID: 22244612; PMCID: PMC3398480
Ma J, Kelich JM, Junod SL, Yang W (2017) Super-resolution mapping of scaffold nucleoporins in the nuclear pore complex. J Cell Sci 130(7):1299–306. Epub 2017/02/17. https://doi.org/10.1242/jcs.193912. PubMed PMID: 28202688; PMCID: PMC5399779
Schlichthaerle T, Strauss MT, Schueder F, Auer A, Nijmeijer B, Kueblbeck M, Jimenez Sabinina V, Thevathasan JV, Ries J, Ellenberg J, Jungmann R (2019) Direct visualization of single nuclear pore complex proteins using genetically-encoded probes for DNA-PAINT. Angew Chem Int Ed Engl 58(37):13004–8. Epub 2019/07/18. https://doi.org/10.1002/anie.201905685. PubMed PMID: 31314157; PMCID: PMC6771475
Sabinina VJ, Hossain MJ, Heriche JK, Hoess P, Nijmeijer B, Mosalaganti S, Kueblbeck M, Callegari A, Szymborska A, Beck M, Ries J, Ellenberg J (2021) Three-dimensional superresolution fluorescence microscopy maps the variable molecular architecture of the nuclear pore complex. Mol Biol Cell 32(17):1523–33. Epub 2021/07/01. https://doi.org/10.1091/mbc.E20-11-0728. PubMed PMID: 34191541; PMCID: PMC8351745
Gustafsson MG, Shao L, Carlton PM, Wang CJ, Golubovskaya IN, Cande WZ, Agard DA, Sedat JW (2008) Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 94(12):4957–70. Epub 2008/03/11. https://doi.org/10.1529/biophysj.107.120345. PubMed PMID: 18326650; PMCID: PMC2397368
Gustafsson MG (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198(Pt 2):82–87. Epub 2000/05/16. https://doi.org/10.1046/j.1365-2818.2000.00710.x
Gustafsson MG (2008) Super-resolution light microscopy goes live. Nat Methods 5(5):385–387. Epub 2008/05/01. https://doi.org/10.1038/nmeth0508-385
Kraus F, Miron E, Demmerle J, Chitiashvili T, Budco A, Alle Q, Matsuda A, Leonhardt H, Schermelleh L, Markaki Y (2017) Quantitative 3D structured illumination microscopy of nuclear structures. Nat Protoc 12(5):1011–1028. Epub 2017/04/14. https://doi.org/10.1038/nprot.2017.020
Lin R, Kipreos ET, Zhu J, Khang CH, Kner P (2021) Subcellular three-dimensional imaging deep through multicellular thick samples by structured illumination microscopy and adaptive optics. Nat Commun 12(1):3148. Epub 2021/05/27. https://doi.org/10.1038/s41467-021-23449-6. PubMed PMID: 34035309; PMCID: PMC8149693
Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R, Hell SW (2008) Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320(5873):246–249. Epub 2008/02/23. https://doi.org/10.1126/science.1154228
Hein B, Willig KI, Hell SW (2008) Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell. Proc Natl Acad Sci U S A 105(38):14271–6. Epub 2008/09/18. https://doi.org/10.1073/pnas.0807705105. PubMed PMID: 18796604; PMCID: PMC2538451
Mitchell-Jordan S, Chen H, Franklin S, Stefani E, Bentolila LA, Vondriska TM (2012) Features of endogenous cardiomyocyte chromatin revealed by super-resolution STED microscopy. J Mol Cell Cardiol 53(4):552–8. Epub 2012/08/01. https://doi.org/10.1016/j.yjmcc.2012.07.009. PubMed PMID: 22846883; PMCID: PMC3704345
Okada Y, Nakagawa S (2015) Super-resolution imaging of nuclear bodies by STED microscopy. Methods Mol Biol 1262:21–35. Epub 2015/01/06. https://doi.org/10.1007/978-1-4939-2253-6_2
Lelek M, Gyparaki MT, Beliu G, Schueder F, Griffié J, Manley S, Jungmann R, Sauer M, Lakadamyali M, Zimmer C (2021) Single-molecule localization microscopy. Nature Rev Methods Primers 1(1):39. https://doi.org/10.1038/s43586-021-00038-x
Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3(10):793–5. Epub 2006/08/10. https://doi.org/10.1038/nmeth929. PubMed PMID: 16896339; PMCID: PMC2700296
Bohn M, Diesinger P, Kaufmann R, Weiland Y, Muller P, Gunkel M, von Ketteler A, Lemmer P, Hausmann M, Heermann DW, Cremer C (2010) Localization microscopy reveals expression-dependent parameters of chromatin nanostructure. Biophys J 99(5):1358–67. Epub 2010/09/08. https://doi.org/10.1016/j.bpj.2010.05.043. PubMed PMID: 20816047; PMCID: PMC2931727
Wombacher R, Heidbreder M, van de Linde S, Sheetz MP, Heilemann M, Cornish VW, Sauer M (2010) Live-cell super-resolution imaging with trimethoprim conjugates. Nat Methods 7(9):717–719. Epub 2010/08/10. https://doi.org/10.1038/nmeth.1489
Ricci MA, Manzo C, Garcia-Parajo MF, Lakadamyali M, Cosma MP (2015) Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160(6):1145–1158. Epub 2015/03/15. https://doi.org/10.1016/j.cell.2015.01.054
Henriques R, Mhlanga MM (2009) PALM and STORM: what hides beyond the Rayleigh limit? Biotechnol J 4(6):846–857. Epub 2009/06/24. https://doi.org/10.1002/biot.200900024
Wolter S, Schuttpelz M, Tscherepanow M, Van De Linde S, Heilemann M, Sauer M (2010) Real-time computation of subdiffraction-resolution fluorescence images. J Microsc 237(1):12–22. Epub 2010/01/09. https://doi.org/10.1111/j.1365-2818.2009.03287.x
Huang B, Babcock H, Zhuang X (2010) Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143(7):1047–58. Epub 2010/12/21. https://doi.org/10.1016/j.cell.2010.12.002. PubMed PMID: 21168201; PMCID: PMC3272504
Miyazaki K, Dyson MT, Coon VJ, Furukawa Y, Yilmaz BD, Maruyama T, Bulun SE (2018) Generation of progesterone-responsive endometrial stromal fibroblasts from human induced pluripotent stem cells: role of the WNT/CTNNB1 pathway. Stem Cell Rep 11(5):1136–55. Epub 2018/11/06. https://doi.org/10.1016/j.stemcr.2018.10.002. PubMed PMID: 30392973; PMCID: PMC6234962
Isaac C, Pollard JW, Meier UT (2001) Intranuclear endoplasmic reticulum induced by Nopp140 mimics the nucleolar channel system of human endometrium. J Cell Sci 114(Pt 23):4253–4264. Epub 2001/12/12. https://doi.org/10.1242/jcs.114.23.4253
Myhill N, Lynes EM, Nanji JA, Blagoveshchenskaya AD, Fei H, Carmine Simmen K, Cooper TJ, Thomas G, Simmen T (2008) The subcellular distribution of calnexin is mediated by PACS-2. Mol Biol Cell 19(7):2777–88. Epub 2008/04/18. https://doi.org/10.1091/mbc.E07-10-0995. PubMed PMID: 18417615; PMCID: PMC2441662
Forrester A, De Leonibus C, Grumati P, Fasana E, Piemontese M, Staiano L, Fregno I, Raimondi A, Marazza A, Bruno G, Iavazzo M, Intartaglia D, Seczynska M, van Anken E, Conte I, De Matteis MA, Dikic I, Molinari M, Settembre C (2019) A selective ER-phagy exerts procollagen quality control via a Calnexin-FAM134B complex. EMBO J 38(2):e99847. Epub 2018/12/19. https://doi.org/10.15252/embj.201899847. PubMed PMID: 30559329; PMCID: PMC6331724
Guo XY, Liu YS, Gao XD, Kinoshita T, Fujita M (2020) Calnexin mediates the maturation of GPI-anchors through ER retention. J Biol Chem 295(48):16393–410. Epub 2020/09/25. https://doi.org/10.1074/jbc.RA120.015577. PubMed PMID: 32967966; PMCID: PMC7705322
Pauwels E, Schulein R, Vermeire K (2021) Inhibitors of the Sec61 complex and novel high throughput screening strategies to target the protein translocation pathway. Int J Mol Sci 22(21):12007. Epub 2021/11/14. https://doi.org/10.3390/ijms222112007. PubMed PMID: 34769437; PMCID: PMC8585047
Hwang Fu YH, Chandrasekar S, Lee JH, Shan SO (2019) A molecular recognition feature mediates ribosome-induced SRP-receptor assembly during protein targeting. J Cell Biol 218(10):3307–19. Epub 2019/09/21. https://doi.org/10.1083/jcb.201901001. PubMed PMID: 31537711; PMCID: PMC6781444
Deng Y, You L, Lu Y, Han S, Wang J, Vicas N, Chen C, Ye J (2021) Identification of TRAMs as sphingolipid-binding proteins using a photoactivatable and clickable short-chain ceramide analog. J Biol Chem 297(6):101415. Epub 2021/11/19. https://doi.org/10.1016/j.jbc.2021.101415. PubMed PMID: 34793833; PMCID: PMC8665359
Ng CL, Oresic K, Tortorella D (2010) TRAM1 is involved in disposal of ER membrane degradation substrates. Exp Cell Res 316(13):2113–22. Epub 2010/05/01. https://doi.org/10.1016/j.yexcr.2010.04.010. PubMed PMID: 20430023; PMCID: PMC2900547
Huang Y, Xu X, Arvan P, Liu M (2021) Deficient endoplasmic reticulum translocon-associated protein complex limits the biosynthesis of proinsulin and insulin. FASEB J 35(5):e21515. Epub 2021/04/04. https://doi.org/10.1096/fj.202002774R. PubMed PMID: 33811688; PMCID: PMC8106808
Xu X, Huang Y, Li X, Arvan P, Liu M (2021) The role of TRAPgamma/SSR3 in Preproinsulin translocation into the endoplasmic reticulum. Diabetes Epub 2021/12/04. https://doi.org/10.2337/db21-0638
Mesbah K, Camus A, Babinet C, Barra J (2006) Mutation in the Trapalpha/Ssr1 gene, encoding translocon-associated protein alpha, results in outflow tract morphogenetic defects. Mol Cell Biol 26(20):7760–71. Epub 2006/10/04. https://doi.org/10.1128/MCB.00913-06. PubMed PMID: 17015483; PMCID: PMC1636874
Audas TE, Jacob MD, Lee S (2012) The nucleolar detention pathway: a cellular strategy for regulating molecular networks. Cell Cycle 11(11):2059–62. Epub 2012/05/15. https://doi.org/10.4161/cc.20140. PubMed PMID: 22580471; PMCID: PMC3368857
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Preston, C.C., Stoddard, A.C., Faustino, R.S. (2022). A Transient Mystery: Nucleolar Channel Systems. In: Kloc, M., Kubiak, J.Z. (eds) Nuclear, Chromosomal, and Genomic Architecture in Biology and Medicine. Results and Problems in Cell Differentiation, vol 70. Springer, Cham. https://doi.org/10.1007/978-3-031-06573-6_20
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