Tenascin-x promotes epithelial-to-mesenchymal transition by activating latent TGF-β

Journal of Cell Biology

Volumn 205, Issue 3, 2014, Pages 409-428

  Alcaraz, Lindsay B ^a,b,d,e,f   Exposito, Jean Yves ^c,d,e   Chuvin, Nicolas ^a,b,d,e,f   Pommier, Roxane M ^a,b,d,e,f   Cluzel, Caroline ^c,d,e   Martel, Sylvie ^a,b,d,e,f   Sentis, Stéphanie ^a,b,d,e,f   Bartholin, Laurent ^a,b,d,e,f   Lethias, Claire ^c,d,e   Valcourt, Ulrich ^a,b,d,e,f  

^a INSERM   (France)

^b CNRS   (France)

^c INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^d UNIVERSITÉ DE LYON   (France)

^e UNIVERSITÉ LYON 1   (France)

^f CENTRE LÉON BÉRARD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA11BETA1 INTEGRIN; CELL SURFACE RECEPTOR; CYTOKINE; FIBRINOGEN; GLYCOPROTEIN; INTEGRIN; TENASCIN; TENASCIN X; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; BIOAVAILABILITY; CONFORMATIONAL TRANSITION; CYTOKINE PRODUCTION; EPITHELIAL MESENCHYMAL TRANSITION; HOMEOSTASIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION;

ANIMALS; CATTLE; CELL ADHESION; CELL LINE, TUMOR; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HEK293 CELLS; HUMANS; INTEGRINS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MICE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PRECURSORS; RECEPTORS, COLLAGEN; RECOMBINANT PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMAD PROTEINS; TENASCIN; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84900441844     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201308031     Document Type: Article

References (66)

1. Ambort, D., F. Brellier, C. Becker-Pauly, W. Stöcker, S. Andrejevic-Blant, M. Chiquet, and E.E. Sterchi. 2010. Specific processing of tenascin-C by the metalloprotease meprinbeta neutralizes its inhibition of cell spreading. Matrix Biol. 29:31-42. http://dx.doi.org/10.1016/j.matbio.2009.08.007
2. Asano, Y., H. Ihn, K. Yamane, M. Jinnin, Y. Mimura, and K. Tamaki. 2005. Involvement of alphavbeta5 integrin-mediated activation of latent transforming growth factor beta1 in autocrine transforming growth factor beta signaling in systemic sclerosis fibroblasts. Arthritis Rheum. 52:2897- 2905. http://dx.doi.org/10.1002/art.21246
3. Asano, Y., H. Ihn, K. Yamane, M. Jinnin, and K. Tamaki. 2006. Increased expression of integrin alphavbeta5 induces the myofibroblastic differentiation of dermal fibroblasts. Am. J. Pathol. 168:499-510. http://dx.doi.org/10.2353/ajpath.2006.041306
4. Brown, P.D., L.M. Wakefield, A.D. Levinson, and M.B. Sporn. 1990. Physicochemical activation of recombinant latent transforming growth factor-beta's 1, 2, and 3. Growth Factors. 3:35-43. http://dx.doi.org/10.3109/08977199009037500
5. Crawford, S.E., V. Stellmach, J.E. Murphy-Ullrich, S.M. Ribeiro, J. Lawler, R.O. Hynes, G.P. Boivin, and N. Bouck. 1998. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell. 93:1159-1170. http://dx.doi.org/10.1016/S0092-8674(00)81460-9
6. DeMaio, L., S.T. Buckley, M.S. Krishnaveni, P. Flodby, M. Dubourd, A. Banfalvi, Y. Xing, C. Ehrhardt, P. Minoo, B. Zhou, et al. 2012. Ligand-independent transforming growth factor-β type I receptor signalling mediates type I collagen-induced epithelial-mesenchymal transition. J. Pathol. 226:633- 644. http://dx.doi.org/10.1002/path.3016
7. Dennler, S., S. Itoh, D. Vivien, P. ten Dijke, S. Huet, and J.M. Gauthier. 1998. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17:3091-3100. http://dx.doi.org/10.1093/emboj/17.11.3091
8. Egging, D., F. van den Berkmortel, G. Taylor, J. Bristow, and J. Schalkwijk. 2007a. Interactions of human tenascin-X domains with dermal extracellular matrix molecules. Arch. Dermatol. Res. 298:389-396. http://dx.doi.org/10.1007/s00403-006-0706-9
9. Egging, D.F., A.C.T.M. Peeters, N. Grebenchtchikov, A. Geurts-Moespot, C.G.J. Sweep, M. den Heijer, and J. Schalkwijk. 2007b. Identification and characterization of multiple species of tenascin-X in human serum. FEBS J. 274:1280-1289. http://dx.doi.org/10.1111/j.1742-4658.2007.05671.x
10. Elefteriou, F., J.Y. Exposito, R. Garrone, and C. Lethias. 1999. Cell adhesion to tenascin-X mapping of cell adhesion sites and identification of integrin receptors. Eur. J. Biochem. 263:840-848. http://dx.doi.org/10.1046/j.1432-1327.1999.00563.x
11. Elefteriou, F., J.Y. Exposito, R. Garrone, and C. Lethias. 2001. Binding of tenascin-X to decorin. FEBS Lett. 495:44-47. http://dx.doi.org/10.1016/S0014-5793(01)02361-4
12. Fujie, S., H. Maita, H. Ariga, and K. Matsumoto. 2009. Tenascin-X induces cell detachment through p38 mitogen-activated protein kinase activation. Biol. Pharm. Bull. 32:1795-1799. http://dx.doi.org/10.1248/bpb.32.1795
13. Goodwin, A.E., and B.U. Pauli. 1995. A new adhesion assay using buoyancy to remove non-adherent cells. J. Immunol. Methods. 187:213-219. http://dx.doi.org/10.1016/0022-1759(95)00187-6
14. Hogg, P.J. 2003. Disulfide bonds as switches for protein function. Trends Biochem. Sci. 28:210-214. http://dx.doi.org/10.1016/S0968-0004(03)00057-4
15. Hynes, R.O. 2009. The extracellular matrix: not just pretty fibrils. Science. 326:1216-1219. http://dx.doi.org/10.1126/science.1176009
16. Inman, G.J., F.J. Nicolás, J.F. Callahan, J.D. Harling, L.M. Gaster, A.D. Reith, N.J. Laping, and C.S. Hill. 2002. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62:65-74. http://dx.doi.org/10.1124/mol.62.1.65
17. Kang, J.S., C. Liu, and R. Derynck. 2009. New regulatory mechanisms of TGFbeta receptor function. Trends Cell Biol. 19:385-394. http://dx.doi.org/10.1016/j.tcb.2009.05.008
18. Kim, S.-H., J. Turnbull, and S. Guimond. 2011. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J. Endocrinol. 209:139-151. http://dx.doi.org/10.1530/JOE-10-0377
19. Koenig, A., C. Mueller, C. Hasel, G. Adler, and A. Menke. 2006. Collagen type I induces disruption of E-cadherin-mediated cell-cell contacts and promotes proliferation of pancreatic carcinoma cells. Cancer Res. 66:4662- 4671. http://dx.doi.org/10.1158/0008-5472.CAN-05-2804
20. Lethias, C., F. Elefteriou, G. Parsiegla, J.Y. Exposito, and R. Garrone. 2001. Identification and characterization of a conformational heparin-binding site involving two fibronectin type III modules of bovine tenascin-X. J. Biol. Chem. 276:16432-16438. http://dx.doi.org/10.1074/jbc.M010210200
21. Lethias, C., A. Carisey, J. Comte, C. Cluzel, and J.-Y. Exposito. 2006. A model of tenascin-X integration within the collagenous network. FEBS Lett. 580:6281-6285. http://dx.doi.org/10.1016/j.febslet.2006.10.037
22. Mao, J.R., G. Taylor, W.B. Dean, D.R. Wagner, V. Afzal, J.C. Lotz, E.M. Rubin, and J. Bristow. 2002. Tenascin-X deficiency mimics Ehlers-Danlos syndrome in mice through alteration of collagen deposition. Nat. Genet. 30:421-425. http://dx.doi.org/10.1038/ng850
23. Margaron, Y., L. Bostan, J.-Y. Exposito, M. Malbouyres, A.-M. Trunfio-Sfarghiu, Y. Berthier, and C. Lethias. 2010. Tenascin-X increases the stiffness of collagen gels without affecting fibrillogenesis. Biophys. Chem. 147:87- 91. http://dx.doi.org/10.1016/j.bpc.2009.12.011
24. Massagué, J. 2012. TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 13:616-630. http://dx.doi.org/10.1038/nrm3434
25. Matsumoto, K., N. Takayama, J. Ohnishi, E. Ohnishi, Y. Shirayoshi, N. Nakatsuji, and H. Ariga. 2001. Tumour invasion and metastasis are promoted in mice deficient in tenascin-X. Genes Cells. 6:1101-1111. http://dx.doi.org/10.1046/j.1365-2443.2001.00482.x
26. Matsumoto, K., T. Kinoshita, T. Hirose, and H. Ariga. 2006. Characterization of mouse serum tenascin-X. DNA Cell Biol. 25:448-456. http://dx.doi.org/10.1089/dna.2006.25.448
27. Miyazono, K., A. Olofsson, P. Colosetti, and C.H. Heldin. 1991. A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGFbeta 1. EMBO J. 10:1091-1101.
28. Morissette, R., D.P. Merke, and N.B. McDonnell. 2014. Transforming growth factor-β (TGF-β) pathway abnormalities in tenascin-X deficiency associated with CAH-X syndrome. Eur. J. Med. Genet. 57:95-102. http://dx.doi.org/10.1016/j.ejmg.2013.12.004
29. Moustakas, A., and C.-H. Heldin. 2009. The regulation of TGFbeta signal transduction. Development. 136:3699-3714. http://dx.doi.org/10.1242/dev.030338
30. Mu, D., S. Cambier, L. Fjellbirkeland, J.L. Baron, J.S. Munger, H. Kawakatsu, D. Sheppard, V.C. Broaddus, and S.L. Nishimura. 2002. The integrin βvβ8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-β1. J. Cell Biol. 157:493-507. http://dx.doi.org/10.1083/jcb.200109100
31. Munger, J.S., X. Huang, H. Kawakatsu, M.J.D. Griffiths, S.L. Dalton, J. Wu, J.-F. Pittet, N. Kaminski, C. Garat, M.A. Matthay, et al. 1999. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell. 96:319-328. http://dx.doi.org/10.1016/S0092-8674(00)80545-0
32. Murphy-Ullrich, J.E., S. Schultz-Cherry, and M. Höök. 1992. Transforming growth factor-beta complexes with thrombospondin. Mol. Biol. Cell. 3:181-188. http://dx.doi.org/10.1091/mbc.3.2.181
33. Nakao, A., M. Afrakhte, A. Morén, T. Nakayama, J.L. Christian, R. Heuchel, S. Itoh, M. Kawabata, N.E. Heldin, C.H. Heldin, and P. ten Dijke. 1997. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature. 389:631-635. http://dx.doi.org/10.1038/39369
34. Nelson, C.M., and M.J. Bissell. 2006. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 22:287-309. http://dx.doi.org/10.1146/annurev.cellbio.22.010305.104315
35. Nunes, I., P.E. Gleizes, C.N. Metz, and D.B. Rifkin. 1997. Latent transforming growth factor-β binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-β. J. Cell Biol. 136:1151-1163. http://dx.doi.org/10.1083/jcb.136.5.1151
36. Piek, E., A. Moustakas, A. Kurisaki, C.H. Heldin, and P. ten Dijke. 1999. TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J. Cell Sci. 112:4557-4568.
37. Pommier, R.M., J. Gout, D.F. Vincent, C.E. Cano, B. Kaniewski, S. Martel, J. Rodriguez, G. Fourel, U. Valcourt, J.C. Marie, et al. 2012. The human NUPR1/P8 gene is transcriptionally activated by transforming growth factor β via the SMAD signalling pathway. Biochem. J. 445:285-293.
38. Popova, S.N., M. Barczyk, C.-F. Tiger, W. Beertsen, P. Zigrino, A. Aszodi, N. Miosge, E. Forsberg, and D. Gullberg. 2007. Alpha11 beta1 integrin-dependent regulation of periodontal ligament function in the erupting mouse incisor. Mol. Cell. Biol. 27:4306-4316. http://dx.doi.org/10.1128/MCB.00041-07
39. Ribeiro, S.M., M. Poczatek, S. Schultz-Cherry, M. Villain, and J.E. Murphy-Ullrich. 1999. The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J. Biol. Chem. 274:13586-13593. http://dx.doi.org/10.1074/jbc.274.19.13586
40. Rogier, E., A. Durrbach, L. Abecassis, S. Ferlicot, R. Snanoudj, S. Baudreuil, N. Arzouk, A. Vazquez, B. Charpentier, and M.-F. Bourgeade. 2005. A novel biological assay to detect the active form of TGF-beta in urine to monitor renal allograft rejection. Kidney Int. 68:1875-1883. http://dx.doi.org/10.1111/j.1523-1755.2005.00607.x
41. Schalkwijk, J., M.C. Zweers, P.M. Steijlen, W.B. Dean, G. Taylor, I.M. van Vlijmen, B. van Haren, W.L. Miller, and J. Bristow. 2001. A recessive form of the Ehlers-Danlos syndrome caused by tenascin-X deficiency. N. Engl. J. Med. 345:1167-1175. http://dx.doi.org/10.1056/NEJMoa002939
42. Schmittgen, T.D., and K.J. Livak. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101-1108. http://dx.doi.org/10.1038/nprot.2008.73
43. Schultz-Cherry, S., and J.E. Murphy-Ullrich. 1993. Thrombospondin causes activation of latent transforming growth factor-β secreted by endothelial cells by a novel mechanism. J. Cell Biol. 122:923-932. (published erratum appears in J. Cell Biol. 1993.122:1149) http://dx.doi.org/10.1083/jcb.122.4.923
44. Schultz-Cherry, S., J. Lawler, and J.E. Murphy-Ullrich. 1994. The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J. Biol. Chem. 269:26783-26788.
45. Shintani, Y., M.J. Wheelock, and K.R. Johnson. 2006. Phosphoinositide-3 kinase-Rac1-c-Jun NH2-terminal kinase signaling mediates collagen I-induced cell scattering and up-regulation of N-cadherin expression in mouse mammary epithelial cells. Mol. Biol. Cell. 17:2963-2975. http://dx.doi.org/10.1091/mbc.E05-12-1123
46. Shintani, Y., Y. Fukumoto, N. Chaika, R. Svoboda, M.J. Wheelock, and K.R. Johnson. 2008a. Collagen I-mediated up-regulation of N-cadherin requires cooperative signals from integrins and discoidin domain receptor 1. J. Cell Biol. 180:1277-1289. http://dx.doi.org/10.1083/jcb.200708137
47. Shintani, Y., M. Maeda, N. Chaika, K.R. Johnson, and M.J. Wheelock. 2008b. Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-beta signaling. Am. J. Respir. Cell Mol. Biol. 38:95-104. http://dx.doi.org/10.1165/rcmb.2007-0071OC
48. Stegemann, C., A. Didangelos, J. Barallobre-Barreiro, S.R. Langley, K. Mandal, M. Jahangiri, and M. Mayr. 2013. Proteomic identification of matrix metalloproteinase substrates in the human vasculature. Circ. Cardiovasc. Genet. 6:106-117. http://dx.doi.org/10.1161/CIRCGENETICS.112.964452
49. Taipale, J., K. Miyazono, C.H. Heldin, and J. Keski-Oja. 1994. Latent transforming growth factor-β1 associates to fibroblast extracellular matrix via latent TGF-β binding protein. J. Cell Biol. 124:171-181. http://dx.doi.org/10.1083/jcb.124.1.171
50. Taipale, J., J. Saharinen, K. Hedman, and J. Keski-Oja. 1996. Latent transforming growth factor-beta 1 and its binding protein are components of extracellular matrix microfibrils. J. Histochem. Cytochem. 44:875-889. http://dx.doi.org/10.1177/44.8.8756760
51. ten Dijke, P., and H.M. Arthur. 2007. Extracellular control of TGFbeta signalling in vascular development and disease. Nat. Rev. Mol. Cell Biol. 8:857-869. http://dx.doi.org/10.1038/nrm2262
52. Thiery, J.P., H. Acloque, R.Y.J. Huang, and M.A. Nieto. 2009. Epithelial-mesenchymal transitions in development and disease. Cell. 139:871-890. http://dx.doi.org/10.1016/j.cell.2009.11.007
53. Thuault, S., U. Valcourt, M. Petersen, G. Manfioletti, C.-H. Heldin, and A. Moustakas. 2006. Transforming growth factor-β employs HMGA2 to elicit epithelial-mesenchymal transition. J. Cell Biol. 174:175-183. http://dx.doi.org/10.1083/jcb.200512110
54. Thuault, S., E.-J. Tan, H. Peinado, A. Cano, C.-H. Heldin, and A. Moustakas. 2008. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. J. Biol. Chem. 283:33437-33446. http://dx.doi.org/10.1074/jbc.M802016200
55. Tiger, C.F., F. Fougerousse, G. Grundström, T. Velling, and D. Gullberg. 2001. alpha11beta1 integrin is a receptor for interstitial collagens involved in cell migration and collagen reorganization on mesenchymal nonmuscle cells. Dev. Biol. 237:116-129. http://dx.doi.org/10.1006/dbio.2001.0363
56. Tucker, R.P., K. Drabikowski, J.F. Hess, J. Ferralli, R. Chiquet-Ehrismann, and J.C. Adams. 2006. Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage. BMC Evol. Biol. 6:60. http://dx.doi.org/10.1186/1471-2148-6-60
57. Valcourt, U., M. Kowanetz, H. Niimi, C.-H. Heldin, and A. Moustakas. 2005. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol. Biol. Cell. 16:1987-2002. http://dx.doi.org/10.1091/mbc.E04-08-0658
58. Valcourt, U., S. Thuault, K. Pardali, C.-H. Heldin, and A. Moustakas. 2007. Functional role of Meox2 during the epithelial cytostatic response to TGF-beta. Mol. Oncol. 1:55-71. http://dx.doi.org/10.1016/j.molonc.2007.02.002
59. Veit, G., U. Hansen, D.R. Keene, P. Bruckner, R. Chiquet-Ehrismann, M. Chiquet, and M. Koch. 2006. Collagen XII interacts with avian tenascin-X through its NC3 domain. J. Biol. Chem. 281:27461-27470. http://dx.doi.org/10.1074/jbc.M603147200
60. Velling, T., M. Kusche-Gullberg, T. Sejersen, and D. Gullberg. 1999. cDNA cloning and chromosomal localization of human alpha(11) integrin. A collagen-binding, I domain-containing, beta(1)-associated integrin alphachain present in muscle tissues. J. Biol. Chem. 274:25735-25742. http://dx.doi.org/10.1074/jbc.274.36.25735
61. Verrecchia, F., and A. Mauviel. 2002. Transforming growth factor-beta signaling through the Smad pathway: role in extracellular matrix gene expression and regulation. J. Invest. Dermatol. 118:211-215. http://dx.doi.org/10.1046/j.1523-1747.2002.01641.x
62. Wipff, P.-J., and B. Hinz. 2008. Integrins and the activation of latent transforming growth factor beta1 -an intimate relationship. Eur. J. Cell Biol. 87:601-615. http://dx.doi.org/10.1016/j.ejcb.2008.01.012
63. Wipff, P.-J., D.B. Rifkin, J.-J. Meister, and B. Hinz. 2007. Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix. J. Cell Biol. 179:1311-1323. http://dx.doi.org/10.1083/jcb.200704042
64. Wu, M.Y., and C.S. Hill. 2009. Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev. Cell. 16:329-343. http://dx.doi.org/10.1016/j.devcel.2009.02.012
65. Zhang, W.-M., J. Kapyla, J.S. Puranen, C.G. Knight, C.-F. Tiger, O.T. Pentikainen, M.S. Johnson, R.W. Farndale, J. Heino, and D. Gullberg. 2003. alpha 11beta 1 integrin recognizes the GFOGER sequence in interstitial collagens. J. Biol. Chem. 278:7270-7277. http://dx.doi.org/10.1074/jbc.M210313200
66. Zweers, M.C., I.M. van Vlijmen-Willems, T.H. van Kuppevelt, R.P. Mecham, P.M. Steijlen, J. Bristow, and J. Schalkwijk. 2004. Deficiency of tenascin-X causes abnormalities in dermal elastic fiber morphology. J. Invest. Dermatol. 122:885-891. http://dx.doi.org/10.1111/j.0022-202X.2004.22401.x