Abstract
Laminins are a major constituent of the extracellular matrix (ECM). Laminin-111, the most extensively studied laminin isoform, consists of the α1, the β1 and the γ1 chain, and is involved in many cellular processes, like adhesion, migration and differentiation. Given the regulatory role of phosphorylation in protein function, it is important to identify the phosphorylation sites of human laminin β1-chain sequence (LAMB1). Therefore, we computationally predicted all possible phosphorylation sites in LAMB1. For the first time, we identified the possibly responsible kinases for already in vitro experimentally observed phosphorylated residues in LAMB1. All known functional (active) sites of LAMB1, were recorded after an extensive literature search and combined with the experimentally observed and our predicted phosphorylated residues. This generated a detailed phosphorylation map of LAMB1. Five kinases (PKA, PKC, CKII, CKI and GPCR1) were indicated important, while the role of PKA, PKC and CKII, kinases known for ecto-phosphorylation activity, was highlighted. The activity of PKA and PKC was associated with the active site RIQNLLKITNLRIKFVKLHTLGDNLLDS. Also, predicted phosphorylations inside two amyloidogenic (DSITKYFQMSLE, VILQHSAADIAR) and two anti-cancerous (YIGSR and PDSGR) sites suggested a possible role in the development of the corresponding diseases.
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Abbreviations
- AD:
-
Alzheimer disease
- Akt:
-
Ak strain transforming (alternative name, protein kinase B)
- ALK:
-
anaplastic lymphoma kinase
- AMPK:
-
5′ adenosine monophosphate-activated protein kinase
- APP:
-
β–amyloid precursor protein
- ATM:
-
ataxia telangiectasia mutated
- Aβ:
-
amyloid-β peptides
- BARK1:
-
beta-adrenergic receptor kinase
- CaMKII:
-
calmodulin-dependent kinase II
- CaMKIV:
-
calmodulin-dependent kinase IV
- CDK5:
-
cyclin-dependent kinase 5
- Chk1:
-
checkpoint kinase 1
- CKI:
-
casein kinase I
- CKII:
-
casein kinase II
- CLK1:
-
dual specificity protein kinase CLK1 (alternative name, CDC-like kinase 1)
- COB:
-
cobblestone brain malformation
- DNA-PK:
-
deoxyribonucleic acid protein kinase
- ECM:
-
extracellular matrix
- EGFR:
-
epidermal growth factor receptor
- ERK1:
-
extracellular signal-regulated kinase 1
- ERK2:
-
extracellular signal-regulated kinase 2
- GPCR1:
-
G-coupled protein receptor 1
- GSK-3:
-
glycogen synthase kinase-3
- H1K:
-
growth-associated histone H1 kinase
- HTP:
-
high-throughput (option in PhosphositePlus®)
- JAK2:
-
janus kinase 2
- La/SSB:
-
Sjögren syndrome type B antigen (alternative name, lupus La protein)
- MAPKAPK1:
-
mitogen-activated protein (MAP) kinase-activated protein kinase 1
- MAPKAPK2:
-
mitogen-activated protein (MAP) kinase-activated protein kinase 2
- MMP-2:
-
matrix metalloproteinase-2
- ONH:
-
optic nerve hypoplasia
- p70S6K:
-
ribosomal protein S6 kinase
- PAK2:
-
P21 (RAC1) activated kinase 2
- PDGFRα:
-
platelet-derived growth factor receptor alpha
- PDK:
-
pyruvate dehydrogenase kinase
- PKA:
-
protein kinase A
- PKC:
-
protein kinase C
- PLK1:
-
polo-like kinase 1
- PO3 2− :
-
phosphoryl group
- PO4 3− :
-
phosphate group
- PTKs:
-
protein tyrosine kinases
- PTM:
-
post-translational modification
References
Altschul S, Gish W, Miller W, Myers E and Lipman D 1990 Basic local alignment search tool. J. Mol. Biol. 215 403–410
Amanchy R, Periaswamy B, Mathivanan S, Reddy R, Tattikota SG and Pandey A 2007 A compendium of curated phosphorylation-based substrate and binding motifs. Nat. Biotechnol. 25 285–286
Apasov SG, Smith PT, Jelonek MT, Margulies DH and Sitkovsky MV 1996 Phosphorylation of extracellular domains of T-lymphocyte surface proteins. Constitutive serine and threonine phosphorylation of the T cell antigen receptor ectodomains. J. Biol. Chem. 271 25677–25683
Ashcroft M, Kubbutat MH and Vousden KH 1999 Regulation of p53 function and stability by phosphorylation. Mol. Cel. Biol. 19 1751–1758
Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P and Yurchenco PD 2005 A simplified laminin nomenclature. Matrix Biol. 24 326–332
Babiker AA, Ronquist G, Nilsson B and Ekdahl KN 2006 Overexpression of ecto-protein kinases in prostasomes of metastatic cell origin. Prostate 66 675–686
Babinska A, Ehrlich YH and Kornecki E 1996 Activation of human platelets by protein kinase C antibody: Role for surface phosphorylation in homeostasis. Am. J. Physiol. 271 H2134–H2144
Beck K, Hunter I and Engel J 1990 Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 4 148–160
Berthel J, Sutherland EW and Rall TW 1957 The relationship of epinephrine and glucagon to liver phosphorylase. IV. Effect of epinephrine and glucagon on the reactivation of phosphorylase in liver homogenates. J. Biol. Chem. 224 463–475
Bohana-Kashtan O, Pinna LA and Fishelson Z 2005 Extracellular phosphorylation of C9 by protein kinase CK2 regulates complement-mediated lysis. Eur. J. Immunol. 35 1939–1948
Bronfman F, Alvarez A, Morgan C and Inestrosa N 1998 Laminin blocks the assembly of wild-type Aβ and the Dutch variant peptide into Alzheimer’s fibrils. Amyloid 5 16–23
Bronfman F, Garrido J, Alvarez A, Morgan C and Inestrosa N 1996 Laminin inhibits amyloid-β-peptide fibrillation. Neurosci. Lett. 218 201–203
Brooks P, Strömblad S, Sanders L, von Schalscha T, Aimes R, Stetler-Stevenson W, Quigley JP and Cheresh DA 1996 Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin αvβ3. Cell 85 683–693
Bruckner-Tuderman L and Bruckner P 1998 Genetic diseases of the extracellular matrix: more than just connective tissue disorders. J. Mol. Med. 76 226–237
Canese K and Weis S 2002 PubMed: The Bibliographic Database; in The NCBI Handbook (second ed) (Bethesda (MD): National Center for Biotechnology Information) https://www.ncbi.nlm.nih.gov/pubmed
Chakraborti S, Chakraborti T and Dhalla N 2017 Proteases in human diseases. (Singapore: Springer Verlag)
Charonis AS, Skubitz APN, Koliakos G, Reger LA, Dege J, Vogel AM, Wohlhueter R and Furcht LT 1988 A novel synthetic peptide from the B1 chain of laminin with heparin-binding and cell adhesion-promoting activities. J.Cell Biol. 107 1253–1260
Colognato H and Yurchenco P 2000 Form and function: the laminin family of heterotrimers. Dev. Dyn. 218 213–234
Cori GT and Cori CF 1945 The enzymatic conversion of phosphorylase a to b. J. Biol. Chem. 158 321–332
Cori GT and Green AA 1943 Crystalline muscle phosphorylase II. Prosthetic group. J. Biol. Chem. 151 31–38
Devisme L, Bouchet C, Gonzalès M, Alanio E, Bazin A, Bessières B, Bigi N, Blanchet P, et al. 2012 Cobblestone lissencephaly: neuropathological subtypes and correlations with genes of dystroglycanopathies. Brain 135 469–482
Dubey PK, Singodia D and Vyas SP 2010 Liposomes modified with YIGSR peptide for tumor targeting. J. Drug Target. 18 373–380
Dusenbery K, Mendiola J and Skubitz KM 1988 Evidence for ecto-protein kinase activity on the surface of human neutrophils. Biochem. Biophys. Res. Commun. 153 7–13
Ehrlich Y, Davis T, Bock E, Kornecki E and Lenox R 1986 Ecto-protein kinase activity on the external surface of neural cells. Nature 320 67–70
Eisenberg D and Jucker M 2012 The Amyloid State of Proteins in Human Diseases. Cell 148 1188–1203
Ekblom M, Falk M, Salmivirta K, Durbeej M and Ekblom P 1998 Laminin isoforms and epithelial development. Ann. N.Y. Acad. Sci. 857 194–211
Ekblom P, Lonai P and Talts JF 2003 Expression and biological role of laminin-1. Matrix Biol. 22 35–47
Engel J, Odermatt E, Engel A, Madri J, Furthmayr H, Rohde H and Timpl R 1981 Shapes, domain organizations and flexibility of laminin and fibronectin, two multifunctional proteins of the extracellular matrix. J. Mol. Biol. 150 97–120
Fischer A 1946 Mechanism of the proteolytic activity of malignant tissue cells. Nature 157 442–442
Fowler D, Koulov A, Balch W and Kelly J 2007 Functional amyloid – from bacteria to humans. Trends Biochem. Sci. 32 217–224
Gandy S, Czernik A and Greengard P 1988 Phosphorylation of Alzheimer disease amyloid precursor peptide by protein kinase C and Ca2+/calmodulin-dependent protein kinase II. Proc. Natl. Acad. Sci. USA 85 6218–6221
Gauci S, Helbig A, Slijper M, Krijgsveld J, Heck A and Mohammed S 2009 Lys-N and Trypsin cover complementary parts of the phosphoproteome in a refined SCX-based approach. Anal. Chem. 81 4493–4501
Geberhiwot T and Skoglund G 1997 Cell surface and serum protein phosphorylation by U-937 cell ectoprotein kinases. Biochem. Mol. Biol. Int. 41 269–278
Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson W and Quaranta V 1997 Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277 225–228
Govaere O, Petz M, Wouters J, Vandewynckel Y, Scott E, Topal B, Nevens F, Verslype C, Anstee QM, Van Vlierberghe H, Mikulits W and Roskams T 2017 The PDGFRα-laminin B1-keratin 19 cascade drives tumor progression at the invasive front of human hepatocellular carcinoma. Oncogene 36 6605–6616
Graf J, Iwamoto Y, Sasaki M, Martin GR, Kleinman HK, Robey FA and Yamada Y 1987b Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell 48 989–996
Graf J, Ogle RC, Robey FA, Sasaki M, Martin GR, Yamada Y and Kleinman HK 1987a A pentapeptide from the laminin B1 chain mediates cell adhesion and binds the 67000 laminin receptor. Biochemistry 26 6896–6900
Grant D, Tashiro K, Segui-Real B, Yamada Y, Martin G and Kleinman HK 1989 Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell 58 933–943
Haass C 1999 The presenilins in Alzheimer’s disease–proteolysis holds the key. Science 286 916–919
Haass C and Selkoe DJ 2007 Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 8 101–112
Hogan MV, Pawlowska Z, Yang HA, Kornecki E and Ehrlich YH 1995 Surface phosphorylation by ecto-protein kinase C in brain neurons: a target for Alzheimer’s beta-amyloid peptides. J. Neurochem. 65 2022–2030
Hohenester E and Yurchenco PD 2013 Laminins in basement membrane assembly. Cell Adhes. Migr. 7 56–63
Hopker VH, Shewan D, Tessier-Lavigne M, Poo M and Holt C 1999 Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401 69–73
Hornbeck PV, Zhang B, Murray B, Kornhauser JM, Latham V and Skrzypek E 2014 PhosphoSitePlus: mutations, PTMs and recalibrations. Nucleic Acids Res. 43 D512–D520
Hsu P, Kang S, Rameseder J, Zhang Y, Ottina K, Lim D, Peterson T, Choi Y, Gray N, Yaffe M, Marto J and Sabatini D 2011 The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 332 1317–1322
Imada S, Sugiyama Y and Imada M 1988 Fibronectin phosphorylation by ecto-protein kinase. Exp. Cell Res. 179 554–564
Iwamoto Y, Nomizu M, Yamada Y, Ito Y, Tanaka K and Sugioka Y 1996 Inhibition of angiogenesis, tumour growth and experimental metastasis of human fibrosarcoma cells HT1080 by a multimeric form of the laminin sequence Tyr-lle-Gly-Ser-Arg (YIGSR). Br. J. Cancer 73 589–595
Iwamoto Y, Robey FA, Graf J, Sasaki M, Kleinman HK, Yamada Y and Martin GR 1987 YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation. Science 238 1132–134
Kasai S, Urushibata S, Hozumi K, Yokoyama K, Ichikawa N, Kadoya Y, Nishi N, Watanabe N, Yamada Y and Nomizu M 2007 Identification of multiple amyloidogenic sequences in laminin-1. Biochemistry 46 3966–3974
Khoury GA, Baliban RC and Floudas CA 2011 Proteome-wide post-translational modification statistics: frequency analysis and curation of the Swiss-prot database. Sci. Rep. 1 90
Kibbey MC, Jucker M, Weeks BS, Neve RL, Van Nostrand WE and Kleinman HK 1993 Amyloid precursor protein binds to the neurite-promoting IKVAV site of laminin. Proc. Natl. Acad. Sci. USA 90 10150–10153
Klammer M, Kaminski M, Zedler A, Oppermann F, Blencke S, Marx S, Müller S, Tebbe A, Godl K and Schaab C 2012 phosphosignature predicts dasatinib response in non-small cell lung cancer. Mol. Cell. Proteomics 11 651–668
Kleinman H, Graf J, Iwamoto Y, Sasaki M, Schasteen C, Yamada Y, Martin G and Robey F 1989 Identification of a second active site in laminin for promotion of cell adhesion and migration and inhibition of in vivo melanoma lung colonization. Arch. Biochem. Biophys. 272 39–45
Koliakos G, Kouzi-Koliakos K, Triantos A, Trachana V, Kavoukopoulos E, Gaitatzi M and Dimitriadou A 2000 Laminin-1 phosphorylation by protein kinase A: effect on self assembly and heparin binding. J. Biochem. Mol. Biol. 33 370–378
Koliakos G, Trachana V, Gaitatzi M and Dimitriadou A 2001 Phosphorylation of laminin-1 by protein kinase C. Mol. Cells 11 179–185
Koliakos G, Trontzos C, Kouzi-Koliakos K, Kanellaki M and Grammaticos P 1997 Lung carcinoma imaging using a synthetic laminin derivative radioiodinated peptide YIGSR. J. Nucl. Med. 38 1940–1994
Kondrashin A, Nesterova M and Cho-Chung Y 1999 Cyclic Adenosine 3′:5′-monophosphate dependent protein kinase on the external surface of LS-174T human colon carcinoma cells. Biochemistry 38 172–179
Kouzi-Koliakos K, Koliakos G, Trontzos C, Papageorgiou A, Iliadis S, Triantos A, Dimitriadou A and Kanellaki M 1996 In vivo binding of the radioiodinated peptide YIGSR on B16 melanoma cells. Invasion Metastasis 16 322–329
Kouzi-Koliakos K, Koliakos GG, Tsilibary EC, Furcht LT and Charonis AS 1989 Mapping of three major heparin-binding sites on laminin and identification of a novel heparin-binding site on the B1 chain. J. Biol. Chem. 264 17971–17978
Krebs EG and Fischer EH 1956 The phosphorylase b to a converting enzyme of rabbit skeletal muscle. Biochim. Biophys. Acta 20 150–157
Krebs EG, Graves DJ and Fischer EH 1959 Factors affecting the activity of muscle phosphorylase b kinase. J. Biol. Chem. 234 2867–2873
Kumar S and Walter J 2011 Phosphorylation of amyloid beta (Aβ) peptides – A trigger for formation of toxic aggregates in Alzheimer’s disease. Aging 3 803–812
Kumar S, Rezaei-Ghaleh N, Terwel D, Thal DR, Richard M, Hoch M, Mc Donald JM, Wüllner U, Glebov K, Heneka MT, Walsh DM, Zweckstetter M and Walter J 2011 Extracellular phosphorylation of the amyloid-β peptide promotes formation of toxic aggregates during the pathogenesis of Alzheimer disease. EMBO J. 30 2255–2265
Kumar S, Singh S, Hinze D, Josten M, Sahl H, Siepmann M and Walter J 2012 Phosphorylation of amyloid-β peptide at serine 8 attenuates its clearance via insulin-degrading and angiotensin-converting enzymes. J. Biol. Chem. 287 8641–8651
Lee H, Na K, Kwon M, Kim H, Kim K and Paik Y 2009 Quantitative analysis of phosphopeptides in search of the disease biomarker from the hepatocellular carcinoma specimen. Proteomics 9 3395–3408
Li S, Harrison D, Carbonetto S, Fässler R, Smyth N, Edgar D and Yurchenco P 2002 Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J. Cell Biol. 157 1279–1290
Li Y 2011 [dataset] CST Curation Set: 10527; Year: 2011; Biosample/Treatment: tissue, heart/untreated; Disease: ventricular tachycardia; SILAC: -; Specificities of Antibodies Used to Purify Peptides prior to LCMS: pY Antibodies Used to Purify Peptides prior to LCMS: Phospho-Tyrosine Mouse mAb (P-Tyr-100) Cat#: 9411, PTMScan(R) Phospho-Tyr Motif (Y*) Immunoaffinity Beads Cat#: 1991
Liesi P, Narvlnen A, Soos J, Sariola H and Snounou G 1989 Identification of a neurite outgrowth-promoting domain of laminin using synthetic peptides. FEBS Lett. 244 141–148
Lodish H, Berk A, Matsudaira P, Kaiser CA, Krieger M, Scott MP, Zipursky SL and Darnell J 2000 Integrating cells into tissues; in Molecular Cell Biology (fifth ed) (New York: WH Freeman and Company) pp 197–234
Lopez-Barcons LA, Polo D, Reig F and Fabra A 2004 Pentapeptide YIGSR-mediated HT-1080 fibrosarcoma cells targeting of adriamycin encapsulated in sterically stabilized liposomes. Biomed. Mater. Res. A. 69 155–163.
Lundby A, Andersen M, Steffensen A, Horn H, Kelstrup C, Francavilla C, Jensen LJ, Schmitt N, Thomsen MB and Olsen, JV 2013 In vivo phosphoproteomics analysis reveals the cardiac targets of adrenergic receptor signaling. Sci. Signal. 6 rs11
Malinda KM, Nomizu M, Chung M, Delgado M, Kuratoni Y, Yamada Y, Kleinman HK and Ponce ML 1999 Identification of laminin a1 and b1 chain peptides active for endothelial cell adhesion, tube formation, and aortic sprouting. FASEB J. 13 53–62
Mecham R 1991 Laminin receptors. Annu. Rev. Cell Dev. Biol. 7 71–91
Mecham RP, Hinek A, Griffin GL, Senior RM and Liotta LA 1989 The elastin receptor shows structural and functional similarities to the 67-kDa tumor cell laminin receptor. J. Biol. Chem. 264 16652–16657
Mertins P, Mani D, Ruggles K, Gillette M, Clauser K, Wang P, Wang X, Qiao JW, et al. 2016 Proteogenomics connects somatic mutations to signalling in breast cancer. Nature 534 55–62
Miner JH, Li C, Mudd JL, Go G and Sutherland A 2004 Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 131 2247–2256
Ming GL, Song HJ, Berninger B, Holt CE, Tessier-Lavigne M and Poo MM 1997 cAMP-dependent growth cone guidance by netrin-1. Neuron 19 1225–1235
Morgan C, Bugueño M, Garrido J and Inestrosa N 2002 Laminin affects polymerization, depolymerization and neurotoxicity of Aβ peptide. Peptides 23 1229–1240
Murata J, Saiki I, Azuma I and Nishi N 1989 Inhibitory effect of a synthetic polypeptide, poly(Tyr-Ile-Gly-Ser-Arg), on the metastatic formation of malignant tumour cells. Int. J. Biol. Macromol. 11 97–99
Murtomaki S, Risteli J, Risteli L, Koivisto UM, Johansson S and Liesi P 1992 Laminin and its neurite outgrowth- promoting domain in the brain in Alzheimer’ s disease and Down’ s syndrome patients. J. Neurosci. Res. 32 261–273
Nakai M, Mundy GR, Williams PJ, Boyce B and Yoneda, T 1992. A synthetic antagonist to laminin inhibits the formation of osteolytic metastases by human melanoma cells in nude mice. Cancer Res. 52 5395–5399
Narindrasorasak S, Lowery DE, Altman RA, Gonzalez-DeWhitt PA, Greenberg BD and Kisilevsky R 1992 Characterization of high affinity binding between laminin and Alzheimer’s disease amyloid precursor proteins. Lab. Investig. 67 643–652
Nomizu M, Kuratomi Y, Ponce M, Song S, Miyoshi K, Otaka A, Powell S, Hoffman M, Kleinman HK and Yamada Y 2000 Cell adhesive sequences in mouse laminin β1 chain. Arch. Biochem. Biophys. 378 311–320
O’Leary N, Wright M, Brister J, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, et al. 2015 Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44 D733–D745
Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P and Mann M 2006 Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127 635–648
Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller M, Jensen L, Nigg EA, Brunak S and Mann M 2010 Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3 ra3
Ott U, Odermatt E, Engel J, Furthmayr H and Timpl R 1982 Protease resistance and conformation of laminin. Eur. J. Biochem. 123 63–72
Perlmutter LS, Barron E, Saperia D and Chui HC 1991. Association between vascular basement membrane components and the lesions of Alzheimer’s disease. J. Neurosci. Res. 30 673–681
Petz M, Kozina D, Huber H, Siwiec T, Seipelt J, Sommergruber W and Mikulits W 2007 The leader region of Laminin B1 mRNA confers cap-independent translation. Nucleic Acids Res. 35 2473–2482
Plopper G 2007 The extracellular matrix and cell adhesion; in Cells (eds) B Lewin, L Cassimeris, V Lingappa and G Plopper (Sudbury, MA: Jones and Bartlett)
Powell SK, Rao J, Roque E, Nomizu M, Kuratomi Y, Yamada Y and Kleinman HK 2000 Neural cell response to multiple novel sites on laminin-1. J. Neurosci. Res. 61 302–312
Pruitt KD, Harrow J, Harte RA, Wallin C, Diekhans M, Maglott DR, Searle S, Farrell CM, et al. 2009 The consensus coding sequence (CCDS) project: Identifying a common protein-coding gene set for the human and mouse genomes. Genome Res. 19 1316–1323
Radmanesh F, Caglayan A, Silhavy J, Yilmaz C, Cantagrel V, Omar T, Rosti B, Kaymakcalan H, Gabriel S, Li M, Sestan N, Bilguvar K, Dobyns W, Zaki M, Gunel M and Gleeson J 2013 Mutations in LAMB1 cause cobblestone brain malformation without muscular or ocular abnormalities. Am. J. Hum. Genet. 92 468–474
Raijmakers R, Kraiczek K, de Jong A, Mohammed S and Heck A 2010 Exploring the human leukocyte phosphoproteome using a microfluidic reversed-phase-TiO2-reversed-phase high-performance liquid chromatography phosphochip coupled to a quadrupole time-of-flight mass spectrometer. Anal. Chem. 82 824–832
Rakash S, Rana F, Rafiq S, Masood A and Amin S 2012 Role of proteases in cancer: a review. Biotechnol. Mol. Biol. Rev. 7 90–101
Rao CN, Castronovo, V, Schmitt MC, Wewer UM, Claysmith AP, Liotta LA and Sobel ME 1989 Evidence for a precursor of the high-affinity metastasis-associated murine laminin receptor. Biochemistry 28 7476–7486
Rigbolt K, Prokhorova T, Akimov V, Henningsen J, Johansen P, Kratchmarova I, Kassem M, Mann M, Olsen JV and Blagoev B 2011 system-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci. Signal. 4 rs3
Ritz-Gold C, Cooke R, Blumenthal D and Stull J 1980 Light chain phosphorylation alters the conformation of skeletal muscle myosin. Biochem. Biophys. Res. Commun. 93 209–214
Roach PJ 1991 Multiple and hierarchal protein phosphorylation. J. Biol. Chem. 266 14139–14142
Sakamoto N, Iwahana M, Tanaka NG and Osada Y 1991 Inhibition of angiogenesis and tumor growth by synthetic laminin peptide, CDPYIGSR-NH2. Cancer Res. 51 903–906
Sarfati G, Dvir T, Elkabets M, Apte RN and Cohen S 2011 Targeting of polymeric nanoparticles to lung metastases by surface-attachment of YIGSR peptide from laminin. Biomaterials 32 152–161
Sariahmetoglu M, Crawford BD, Leon H, Sawicka J, Li L, Ballermann BJ, Holmes C, Berthiaume LG, Holt A, Sawicki G and Schulz R 2007 Regulation of matrix metalloproteinase-2 (MMP-2) activity by phosphorylation. FASEB J. 21 2486–2495
Sasaki M, Kato S, Kohno K, Martin G and Yamada Y 1987 Sequence of the cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats. Proc. Natl. Acad. Sci. USA 84 935–939
Sasaki M, Kleinman H, Huber H, Deutzmann R and Yamada Y 1988 Laminin, a multidomain protein. The A chain has a unique globular domain and homology with the basement membrane proteoglycan and the laminin B chains. J. Biol. Chem. 263 16536–16544
Seger D, Gechtman Z and Shaltiel S 1998 Phosphorylation of vitronectin by casein kinase II. Identification of the sites and their promotion of cell adhesion and spreading. J. Biol. Chem. 273 24805–24813
Silverberg M, Cho J, Rioux J, McGovern D, Wu J, Annese V, Achkar J, Goyette P, et al. 2009 Ulcerative colitis–risk loci on chromosomes 1p36 and 12q15 found by genome-wide association study. Nat. Genet. 41 216–220
Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, Paulsson M and Edgar D 1999 Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J. Cell Biol. 144 151–160
Soba P, Eggert S, Wagner K, Zentgraf H, Siehl K, Kreger S, Löwer A, Langer A, Merdes G, Paro R, Masters CL, Müller U, Kins S and Beyreuther K 2005 Homo- and heterodimerization of APP family members promotes intercellular adhesion. EMBO J. 24 3624–3634
Soto C, Estrada L and Castilla J 2006 Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. Trends Biochem. Sci. 31 150–155
Stallmach A, Orzechowski HD, Feldmann P, Riecken EO, Zeitz M and Herbst H 1999 32/67-kD laminin receptor expression in human colonic neoplasia: elevated transcript levels correlate with the degree of epithelial dysplasia. Am. J. Gastroenterol. 94 3341–3347
Streuli CH, Schmidhauser C, Bailey N, Yurchenco P, Skubitz APN, Roskelley C and Bissell MJ 1995 Laminin mediates tissue-specific gene expression in mammary epithelia. J. Cell Biol. 129 591–603
Stuart S, Houel S, Lee T, Wang N, Old W and Ahn N 2015 A Phosphoproteomic Comparison of B-RAFV600E and MKK1/2 inhibitors in melanoma cells. Mol. Cell. Proteomics 14 1599–1615
Sutherland EW Jr and Wosilait WD 1955 Inactivation and activation of liver phosphorylase. Nature 175 169–171
Suzuki T, Ando K, Isohara T, Oishi M, Lim GS, Satoh Y, Wasco W, Tanzi RE, Nairn AC, Greengard P, Gandy SE and Kirino Y 1997 Phosphorylation of Alzheimer beta-amyloid precursor-like proteins. Biochemistry 36 4643–4649
Tessier-Lavigne M and Goodman CS 1996 The molecular biology of axon guidance. Science 274 1123–1133
The UniProt Consortium 2017 UniProt: the universal protein knowledgebase. Nucleic Acids Res. 32 D158–D169. http://uniprot.org
Timpl R and Brown J 1996 Supramolecular assembly of basement membranes. BioEssays 18 123–132
Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM and Martin GR 1979 Laminin—a glycoprotein from basement membranes. J. Biol. Chem. 254 9933–9937
Trachana V, Christophorides E, Kouzi-Koliakos K and Koliakos G 2005 Laminin-1 is phosphorylated by ecto-protein kinases of monocytes. Int. J. Biochem. Cell Biol. 37 478–492
Tsai CF, Wang Y, Yen H, Tsou C, Ku W, Lin P, Chen H, Nesvizhskii A, Ishihama Y and Chen Y 2015 Large-scale determination of absolute phosphorylation stoichiometries in human cells by motif-targeting quantitative proteomics. Nat. Commun. 6 6622
Ukawala M, Chaudhari K, Rajyaguru T, Manjappa AS, Murthy RS and Gude R 2012 Laminin receptor-targeted etoposide loaded polymeric micelles: a novel approach for the effective treatment of tumor metastasis. J. Drug Target. 20 55–66
Underwood P, Bennett F, Kirkpatrick A, Bean P and Moss B 1995 Evidence for the location of a binding sequence for the α2β1 integrin of endothelial cells, in the β1 subunit of laminin. Biochem. J. 309 765–771
Wang H, Li M, Lin W, Wang W, Zhang Z, Rayburn ER, Lu J, Chen D, Yue X, Shen F, Jiang F, He J, Wei W, Zeng X and Zhang R 2007 Extracellular activity of cyclic AMP-dependent protein kinase as a biomarker for human cancer detection: distribution characteristics in a normal population and cancer patients. Cancer Epidemiol. Biomarkers Prev. 16 789–795
Wu Y, Wang XF, Mo XA, Li JM, Yuan J, Zheng JO, Feng Y and Tang M 2001 Expression of laminin β1 and integrin α2 in the anterior temporal neocortex tissue of patients with intractable epilepsy. Int. J. Neurosci. 121 323–328
Yalak G and Vogel V 2014 Ectokinases as novel cancer markers and drug targets in cancer therapy. Cancer Med. 4 404–414
Yamamura K, Kibbey MC, Jun SH and Kleinman HK 1993 Effect of Matrigel and laminin peptide YIGSR on tumor growth and metastasis. Semin. Cancer Biol. 4 259–265
Yu HN, Zhang LC, Yang JG, Das UN and Shen SR 2009 Effect of laminin tyrosine-isoleucine-glycine-serine-arginine peptide on the growth of human prostate cancer (PC-3) cells in vitro. Eur. J. Pharmacol. 616 251–255
Yurchenco PD, Cheng YS and Colognato H 1992 Laminin forms an independent network in basement membranes. J. Cell Biol. 117 1119–1133
Zerbino D, Achuthan P, Akanni W, Amode M, Barrell D, Bhai J, Billis K, Cummins C, et al. 2018 Ensembl 2018. Nucleic Acids Res. 46 D754–D761
Zhou J 2010 [dataset] CST Curation Set: 9686; Year: 2010; Biosample/Treatment: cell line, PY2/untreated; Disease: -; SILAC: -; Specificities of Antibodies Used to Purify Peptides prior to LCMS: RRXp[ST] Antibodies Used to Purify Peptides prior to LCMS: Phospho-PKA Substrate (RRXS/T) (100G7) Rabbit mAb Cat#: 9624, PTMScan(R) Phospho-PKA Substrate Motif (K/RK/RXS*/T*) Immunoaffinity Beads Cat#: 1984
Zhou J 2011 [dataset] CST Curation Set: 12497; Year: 2011; Biosample/Treatment: cell line, Jurkat/calyculin_A & pervanadate; Disease: T cell leukemia; SILAC: -; Specificities of Antibodies Used to Purify Peptides prior to LCMS: pY Antibodies Used to Purify Peptides prior to LCMS: Phospho-Tyrosine Mouse mAb (P-Tyr-100) Cat#: 9411, PTMScan(R) Phospho-Tyr Motif (Y*) Immunoaffinity Beads Cat#: 1991
Zimina EP, Fritsch A, Schermer B, Bakulina AY, Bashkurov M, Benzing T and Bruckner-Tuderman L 2007. Extracellular phosphorylation of collagen XVII by ecto-casein kinase 2 inhibits ectodomain shedding. J. Biol. Chem. 282 22737–22746
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We thank Papavramidis Theodosis for his assistance and constructive advice in preparing figure 2.
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Communicated by Kundan Sengupta.
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Verrou, KM., Galliou, P.A., Papaioannou, M. et al. Phosphorylation mapping of Laminin β1-chain: Kinases in association with active sites. J Biosci 44, 55 (2019). https://doi.org/10.1007/s12038-019-9871-9
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DOI: https://doi.org/10.1007/s12038-019-9871-9