Biologically-active laminin-111 fragment that modulates the epithelial-to-mesenchymal transition in embryonic stem cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages 5908-5913

  Horejs, Christine Maria ^a   Serio, Andrea ^a   Purvis, Alan ^a   Gormley, Adam J ^a   Bertazzo, Sergio ^a   Poliniewicz, Anna ^a   Wang, Alex J ^a   DiMaggio, Peter ^a   Hohenester, Erhard ^a   Stevens, Molly M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD147 ANTIGEN; GELATINASE A; GELATINASE B; LAMININ; LAMININ 111; UNCLASSIFIED DRUG; UVOMORULIN; VERY LATE ACTIVATION ANTIGEN 3;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; UPREGULATION;

ANIMALS; ANTIGENS, CD147; BINDING SITES; CADHERINS; CELL ADHESION; EMBRYONIC STEM CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMANS; INTEGRIN ALPHA3BETA1; LAMININ; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; PEPTIDE FRAGMENTS; PROTEIN BINDING; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

EID: 84899100701     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1403139111     Document Type: Article

References (54)

1. Aumailley M (2013) The laminin family. Cell Adhes Migr 7(1):48-55.
2. Ekblom P, Lonai P, Talts JF (2003) Expression and biological role of laminin-1. Matrix Biol 22(1):35-47. (Pubitemid 36444505)
3. Li S, Edgar D, Fässler R, Wadsworth W, Yurchenco PD (2003) The role of laminin in embryonic cell polarization and tissue organization. Dev Cell 4(5):613-624. (Pubitemid 36564893)
4. Miner JH, Yurchenco PD (2004) Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20(1):255-284. (Pubitemid 39488639)
5. Hohenester E, Yurchenco PD (2013) Laminins in basement membrane assembly. Cell Adhes Migr 7(1):56-63.
6. Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V (1997) Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277(5323):225-228. (Pubitemid 27446075)
7. Lah TT, et al. (1989) Degradation of laminin by human tumor cathepsin B. Clin Exp Metastasis 7(4):461-468. (Pubitemid 19114020)
8. Mydel P, et al. (2008) Neutrophil elastase cleaves laminin-332 (laminin-5) generating peptides that are chemotactic for neutrophils. J Biol Chem 283(15):9513-9522.
9. Shapiro SD (1998) Matrix metalloproteinase degradation of extracellular matrix: Biological consequences. Curr Opin Cell Biol 10(5):602-608.
10. Mott JD, Werb Z (2004) Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 16(5):558-564. (Pubitemid 39201241)
11. Clark IM, Swingler TE, Sampieri CL, Edwards DR (2008) The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol 40(6-7):1362-1378.
12. Faisal Khan KM, Laurie GW, McCaffrey TA, Falcone DJ (2002) Exposure of cryptic domains in the α 1-chain of laminin-1 by elastase stimulates macrophages urokinase and matrix metalloproteinase-9 expression. J Biol Chem 277(16):13778-13786. (Pubitemid 34967981)
13. Koshikawa N, Giannelli G, Cirulli V, Miyazaki K, Quaranta V (2000) Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148(3):615-624.
14. Schenk S, Quaranta V (2003) Tales from the crypt[ic] sites of the extracellular matrix. Trends Cell Biol 13(7):366-375. (Pubitemid 36776714)
15. Kinoh H, et al. (1996) MT-MMP, the cell surface activator of proMMP-2 (pro-gelatinase A), is expressed with its substrate in mouse tissue during embryogenesis. J Cell Sci 109(Pt 5):953-959. (Pubitemid 26168248)
16. Wartenberg M, et al. (2003) Inhibition of tumor-induced angiogenesis and matrix-metalloproteinase expression in confrontation cultures of embryoid bodies and tumor spheroids by plant ingredients used in traditional Chinese medicine. Lab Invest 83(1):87-98. (Pubitemid 36126053)
17. Spencer HL, et al. (2007) E-cadherin inhibits cell surface localization of the pro-migratory 5T4 oncofetal antigen in mouse embryonic stem cells. Mol Biol Cell 18(8):2838-2851. (Pubitemid 47235292)
18. Thiery JP, Acloque H, Huang RYJ, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139(5):871-890.
19. Lee JM, Dedhar S, Kalluri R, Thompson EW (2006) The epithelial- mesenchymal transition: New insights in signaling, development, and disease. J Cell Biol 172(7):973-981.
20. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7(2):131-142. (Pubitemid 43278296)
21. Eastham AM, et al. (2007) Epithelial-mesenchymal transition events during human embryonic stem cell differentiation. Cancer Res 67(23):11254-11262. (Pubitemid 350248551)
22. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR (2008) Cadherin switching. J Cell Sci 121(Pt 6):727-735. (Pubitemid 351578108)
23. Liu G, et al. (2006) Effects of E-cadherin on mouse embryo implantation and expression of matrix metalloproteinase-2 and -9. Biochem Biophys Res Commun 343(3):832-838.
24. Ullmann U, et al. (2007) Epithelial-mesenchymal transition process in human embryonic stem cells cultured in feeder-free conditions. Mol Hum Reprod 13(1):21-32. (Pubitemid 44942721)
25. Wang Z, et al. (1999) (Alpha)3(beta)1 integrin regulates epithelial cytoskeletal organization. J Cell Sci 112(Pt 17):2925-2935. (Pubitemid 29430038)
26. Markowski MC, Brown AC, Barker TH (2012) Directing epithelial to mesenchymal transition through engineered microenvironments displaying orthogonal adhesive and mechanical cues. J Biomed Mater Res A 100(8):2119-2127.
27. Altroff H, et al. (2004) Interdomain tilt angle determines integrin-dependent function of the ninth and tenth FIII domains of human fibronectin. J Biol Chem 279(53):55995-56003. (Pubitemid 40066607)
28. Brown AC, Rowe JA, Barker TH (2011) Guiding epithelial cell phenotypes with engineered integrin-specific recombinant fibronectin fragments. Tissue Eng Part A 17(1-2):139-150.
29. Chen L, Nakai M, Belton RJ, Jr., Nowak RA (2007) Expression of extracellular matrix metalloproteinase inducer and matrix metalloproteinases during mouse embryonic development. Reproduction 133(2):405-414. (Pubitemid 46359528)
30. Lemaître V, D'Armiento J (2006) Matrix metalloproteinases in development and disease. Birth Defects Res C Embryo Today 78(1):1-10. (Pubitemid 43726172)
31. Yurchenco PD, Cheng YS (1993) Self-assembly and calcium-binding sites in laminin. A three-arm interaction model. J Biol Chem 268(23):17286-17299. (Pubitemid 23236966)
32. Purvis A, Hohenester E (2012) Laminin network formation studied by reconstitution of ternary nodes in solution. J Biol Chem 287(53):44270-44277.
33. Rodin S, et al. (2010) Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat Biotechnol 28(6):611-615.
34. Domogatskaya A, Rodin S, Boutaud A, Tryggvason K (2008) Laminin-511 but not -332, -111, or -411 enables mouse embryonic stem cell self-renewal in vitro. Stem Cells 26(11):2800-2809.
35. Miyazaki T, et al. (2012) Laminin E8 fragments support efficient adhesion and expansion of dissociated human pluripotent stem cells. Nat Commun 3:1236.
36. Miyazaki T, et al. (2008) Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells. Biochem Biophys Res Commun 375(1):27-32.
37. Hall PE, Lathia JD, Caldwell MA, Ffrench-Constant C (2008) Laminin enhances the growth of human neural stem cells in defined culture media. BMC Neurosci 9(1):71.
38. Nishiuchi R, et al. (2006) Ligand-binding specificities of laminin-binding integrins: A comprehensive survey of laminin-integrin interactions using recombinant α3β1, α6β1, α7β1 and α6β4 integrins. Matrix Biol 25(3):189-197.
39. Colognato-Pyke H, et al. (1995) Mapping of network-forming, heparin-binding, and alpha 1 beta 1 integrin-recognition sites within the alpha-chain short arm of laminin-1. J Biol Chem 270(16):9398-9406.
40. Prowse ABJ, Chong F, Gray PP, Munro TP (2011) Stem cell integrins: implications for ex-vivo culture and cellular therapies. Stem Cell Res (Amst) 6(1):1-12.
41. Kreidberg JA (2000) Functions of α3β1 integrin. Curr Opin Cell Biol 12(5):548-553.
42. Bökel C, Brown NH (2002) Integrins in development: Moving on, responding to, and sticking to the extracellular matrix. Dev Cell 3(3):311-321.
43. Berditchevski F, Chang S, Bodorova J, Hemler ME (1997) Generation of monoclonal antibodies to integrin-associated proteins. Evidence that α3β1 complexes with EMMPRIN/basigin/OX47/M6. J Biol Chem 272(46):29174-29180. (Pubitemid 27498208)
44. Zhang F, et al. (2003) Distinct ligand binding sites in integrin α3β1 regulate matrix adhesion and cell-cell contact. J Cell Biol 163(1):177-188. (Pubitemid 37271444)
45. Iyer V, Pumiglia K, DiPersio CM (2005) α3β1 integrin regulates MMP-9 mRNA stability in immortalized keratinocytes: A novel mechanism of integrin-mediated MMP gene expression. J Cell Sci 118(Pt 6):1185-1195. (Pubitemid 40528689)
46. Kim Y, et al. (2009) Integrin α3β1-dependent β-catenin phosphorylation links epithelial Smad signaling to cell contacts. J Cell Biol 184(2):309-322.
47. Takayama K, et al. (2013) Long-term self-renewal of human ES/iPS-derived hepatoblast-like cells on human laminin 111-coated dishes. Stem Cell Rev 1(4):322-335.
48. Meng Y, et al. (2010) Characterization of integrin engagement during defined human embryonic stem cell culture. FASEB J 24(4):1056-1065.
49. Braam SR, et al. (2008) Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via alphavbeta5 integrin. Stem Cells 26(9):2257-2265.
50. Biswas C, et al. (1995) The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 55(2):434-439.
51. Kubota S, Ito H, Ishibashi Y, Seyama Y (1997) Anti-α3 integrin antibody induces the activated form of matrix metalloprotease-2 (MMP-2) with concomitant stimulation of invasion through matrigel by human rhabdomyosarcoma cells. Int J Cancer 70(1):106-111. (Pubitemid 27059713)
52. Agrawal SM, Silva C, Tourtellotte WW, Yong VW (2011) EMMPRIN: A novel regulator of leukocyte transmigration into the CNS in multiple sclerosis and experimental autoimmune encephalomyelitis. J Neurosci 31(2):669-677.
53. Sasaki T, Fässler R, Hohenester E (2004) Laminin: The crux of basement membrane assembly. J Cell Biol 164(7):959-963. (Pubitemid 38429121)
54. McKee KK, Harrison D, Capizzi S, Yurchenco PD (2007) Role of laminin terminal globular domains in basement membrane assembly. J Biol Chem 282(29):21437-21447. (Pubitemid 47099937)