The integrin-collagen connection - a glue for tissue repair?

Journal of Cell Science

Volumn 129, Issue 4, 2016, Pages 653-664

  Zeltz, Cédric ^a   Gullberg, Donald ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Collagen; Fibrosis; Integrins; Tumor; Wound repair

Indexed keywords

ALPHA10BETA1 INTEGRIN; ALPHA11BETA1 INTEGRIN; CAVEOLIN 1; COLLAGEN; COLLAGEN BINDING PROTEIN; COLLAGEN RECEPTOR; COLLAGEN TYPE 1; COLLAGEN TYPE 13; COLLAGEN TYPE 16; COLLAGEN TYPE 3; COLLAGEN TYPE 4; DISCOIDIN; DISCOIDIN DOMAIN RECEPTOR TYROSINE KINASE 1; DISCOIDIN DOMAIN RECEPTOR TYROSINE KINASE 2; FIBRILLAR COLLAGEN; FOCAL ADHESION KINASE; G PROTEIN COUPLED RECEPTOR 56; GLYCOPROTEIN VI; INTEGRIN; INTERLEUKIN 7 RECEPTOR; LEUKOCYTE ASSOCIATED IMMUNOGLOBULIN LIKE RECEPTOR 1; MITOGEN ACTIVATED PROTEIN KINASE P38; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 2; OSTEOCLAST ASSOCIATED IMMUNOGLOBULIN LIKE RECEPTOR; OSTEONECTIN; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2; PROTEIN BINDING;

ALPORT SYNDROME; ANGIOGENESIS; ARTICLE; BASEMENT MEMBRANE; BINDING SITE; BREAST CANCER; CARCINOGENESIS; CARTILAGE CELL; CELL ADHESION; CELL DEDIFFERENTIATION; CELL MIGRATION; COLLAGEN SYNTHESIS; COLON CANCER; DIABETIC CARDIOMYOPATHY; DIABETIC FOOT; ENDOTHELIUM CELL; FIBROBLAST; HEART FIBROBLAST; HOMEOSTASIS; HUMAN; KERATINOCYTE; LUNG CARCINOMA; MEGAKARYOCYTE; MELANOMA; MESENCHYMAL STEM CELL; METASTASIS; MONOCYTE; MYOFIBROBLAST; NON SMALL CELL LUNG CANCER; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE TUMOR; RHEUMATOID ARTHRITIS; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN FIBROSIS; STOMACH CANCER; STROMA; TH17 CELL; TISSUE REPAIR; TUMOR STROMA INTERACTION; WOUND HEALING; WOUND HEALING IMPAIRMENT; ANIMAL; CHEMISTRY; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE;

ANIMALS; CELL ADHESION; COLLAGEN; HUMANS; INTEGRINS; NEOPLASMS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; WOUND HEALING;

EID: 84961230948     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.180992     Document Type: Article

References (181)

1. Abbonante, V., Gruppi, C., Rubel, D., Gross, O., Moratti, R. and Balduini, A. (2013). Discoidin domain receptor 1 protein is a novel modulator of megakaryocyte-collagen interactions. J. Biol. Chem. 288, 16738-16746.
2. Alshehri, O. M., Hughes, C. E., Montague, S., Watson, S. K., Frampton, J., Bender, M. andWatson, S. P. (2015). Fibrin activates GPVI in human and mouse platelets. Blood 126, 1601-1608.
3. Barczyk, M., Carracedo, S. and Gullberg, D. (2010). Integrins. Cell Tissue Res. 339, 269-280.
4. Barczyk, M. M., Lu, N., Popova, S. N., Bolstad, A. I. and Gullberg, D. (2013). alpha11beta1 integrin-mediated MMP-13-dependent collagen lattice contraction by fibroblasts: Evidence for integrin-coordinated collagen proteolysis. J. Cell Physiol. 228, 1108-1119.
5. Baronas-Lowell, D., Lauer-Fields, J. L., Borgia, J. A., Sferrazza, G. F., Al-Ghoul, M., Minond, D. and Fields, G. B. (2004). Differential modulation of human melanoma cell metalloproteinase expression by alpha2beta1 integrin and CD44 triple-helical ligands derived from type IV collagen. J. Biol. Chem. 279, 43503-43513.
6. Barrow, A. D., Raynal, N., Andersen, T. L., Slatter, D. A., Bihan, D., Pugh, N., Cella, M., Kim, T., Rho, J., Negishi-Koga, T. et al. (2011). OSCAR is a collagen receptor that costimulates osteoclastogenesis in DAP12-deficient humans and mice. J. Clin. Invest. 121, 3505-3516.
7. Barrow, A. D., Palarasah, Y., Bugatti, M., Holehouse, A. S., Byers, D. E., Holtzman, M. J., Vermi, W., Skjodt, K., Crouch, E. and Colonna, M. (2015). OSCAR is a receptor for surfactant protein D that activates TNF-alpha release from human CCR2+ inflammatory monocytes. J. Immunol. 194, 3317-3326.
8. Bartolomé, R. A., Barderas, R., Torres, S., Fernandez-Aceñero, M. J., Mendes, M., García-Foncillas, J., Lopez-Lucendo, M. and Casal, J. I. (2014). Cadherin-17 interacts with alpha2beta1 integrin to regulate cell proliferation and adhesion in colorectal cancer cells causing liver metastasis. Oncogene 33, 1658-1669.
9. Bengtsson, T., Aszodi, A., Nicolae, C., Hunziker, E. B., Lundgren-Akerlund, E. and Fassler, R. (2005). Loss of alpha10beta1 integrin expression leads to moderate dysfunction of growth plate chondrocytes. J. Cell Sci. 118, 929-936.
10. Bix, G., Fu, J., Gonzalez, E. M., Macro, L., Barker, A., Campbell, S., Zutter, M. M., Santoro, S. A., Kim, J. K., Hook, M. et al. (2004). Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through alpha2beta1 integrin. J. Cell Biol. 166, 97-109.
11. Blumbach, K., Niehoff, A., Belgardt, B. F., Ehlen, H. W. A, Schmitz, M., Hallinger, R., Schulz, J.-N., Bruning, J. C., Krieg, T., Schubert, M. et al. (2012). Dwarfism in mice lacking collagen-binding integrins alpha2beta1 and alpha11beta1 is caused by severely diminished IGF-1 levels. J. Biol. Chem. 287, 6431-6440.
12. Borza, C. M., Chen, X., Mathew, S., Mont, S., Sanders, C. R., Zent, R. and Pozzi, A. (2010). Integrin alpha1beta1 promotes caveolin-1 dephosphorylation by activating T cell protein-tyrosine phosphatase. J. Biol. Chem. 285, 40114-40124.
13. Borza, C. M., Su, Y., Chen, X., Yu, L., Mont, S., Chetyrkin, S., Voziyan, P., Hudson, B. G., Billings, P. C., Jo, H. et al. (2012). Inhibition of integrin alpha2beta1 ameliorates glomerular injury. J. Am. Soc. Nephrol. 23, 1027-1038.
14. Boudjadi, S., Carrier, J. C. and Beaulieu, J.-F. (2013). Integrin alpha1 subunit is up-regulated in colorectal cancer. Biomark Res. 1, 16.
15. Boudjadi, S., Carrier, J. C., Groulx, J.-F. and Beaulieu, J.-F. (2015). Integrin alpha1beta1 expression is controlled by c-MYC in colorectal cancer cells. Oncogene. doi:10.1038/onc.2015.231
16. Boudjadi, S., Carrier, J. C. and Beaulieu, J. F. (2013). Integrin alpha1 subunit is up-regulated in colorectal cancer. Biomark Res 1, 16.
17. Camper, L., Hellman, U. and Lundgren-Akerlund, E. (1998). Isolation, cloning, and sequence analysis of the integrin subunit alpha10, a beta1-associated collagen binding integrin expressed on chondrocytes. J. Biol. Chem. 273, 20383-20389.
18. Camper, L., Holmvall, K., Wängnerud, C., Aszódi, A. and Lundgren-Akerlund, E. (2001). Distribution of the collagen-binding integrin alpha10beta1 during mouse development. Cell Tissue Res. 306, 107-116.
19. Carracedo, S., Lu, N., Popova, S. N., Jonsson, R., Eckes, B. and Gullberg, D. (2010). The fibroblast integrin alpha11beta1 is induced in a mechanosensitive manner involving activin A and regulates myofibroblast differentiation. J. Biol. Chem. 285, 10434-10445.
20. Chen, J., Diacovo, T. G., Grenache, D. G., Santoro, S. A. and Zutter, M. M. (2002). The alpha(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am. J. Pathol. 161, 337-344.
21. Chen, X., Moeckel, G., Morrow, J. D., Cosgrove, D., Harris, R. C., Fogo, A. B., Zent, R. and Pozzi, A. (2004). Lack of integrin alpha1beta1 leads to severe glomerulosclerosis after glomerular injury. Am. J. Pathol. 165, 617-630.
22. Chen, X., Su, Y., Fingleton, B., Acuff, H., Matrisian, L. M., Zent, R. and Pozzi, A. (2005). An orthotopic model of lung cancer to analyze primary and metastatic NSCLC growth in integrin alpha1-null mice. Clin. Exp. Metastasis 22, 185-193.
23. Chen, X., Abair, T. D., Ibanez, M. R., Su, Y., Frey, M. R., Dise, R. S., Polk, D. B., Singh, A. B., Harris, R. C., Zent, R. et al. (2007). Integrin alpha1beta1 controls reactive oxygen species synthesis by negatively regulating epidermal growth factor receptor-mediated Rac activation. Mol. Cell. Biol. 27, 3313-3326.
24. Chen, X., Whiting, C., Borza, C., Hu, W., Mont, S., Bulus, N., Zhang, M. Z., Harris, R. C., Zent, R. and Pozzi, A. (2010). Integrin alpha1beta1 regulates epidermal growth factor receptor activation by controlling peroxisome proliferator-activated receptor gamma-dependent caveolin-1 expression. Mol. Cell. Biol. 30, 3048-3058.
25. Chen, X., Wang, H., Liao, H.-J., Hu, W., Gewin, L., Mernaugh, G., Zhang, S., Zhang, Z.-Y., Vega-Montoto, L., Vanacore, R. M. et al. (2014). Integrin-mediated type II TGF-beta receptor tyrosine dephosphorylation controls SMAD-dependent profibrotic signaling. J. Clin. Invest. 124, 3295-3310.
26. Chen, P., Cescon, M. and Bonaldo, P. (2015). Lack of collagen VI promotes wound-induced hair growth. J. Invest. Dermatol. 135, 2358-2367.
27. Chiang, N.-Y., Hsiao, C.-C., Huang, Y.-S., Chen, H.-Y., Hsieh, I.-J., Chang, G.-W. and Lin, H.-H. (2011). Disease-associated GPR56 mutations cause bilateral frontoparietal polymicrogyria via multiple mechanisms. J. Biol. Chem. 286, 14215-14225.
28. Clemetson, J. M., Polgar, J., Magnenat, E., Wells, T. N. C. and Clemetson, K. J. (1999). The platelet collagen receptor glycoprotein VI is a member of the immunoglobulin superfamily closely related to FcalphaR and the natural killer receptors. J. Biol. Chem. 274, 29019-29024.
29. Cosgrove, D., Meehan, D. T., Delimont, D., Pozzi, A., Chen, X., Rodgers, K. D., Tempero, R. M., Zallocchi, M. and Rao, V. H. (2008). Integrin alpha1beta1 regulates matrix metalloproteinases via P38 mitogen-activated protein kinase in mesangial cells: implications for Alport syndrome. Am. J. Pathol. 172, 761-773.
30. de Fougerolles, A. R., Sprague, A. G., Nickerson-Nutter, C. L., Chi-Rosso, G., Rennert, P. D., Gardner, H., Gotwals, P. J., Lobb, R. R. and Koteliansky, V. E. (2000). Regulation of inflammation by collagen-binding integrins alpha1beta1 and alpha2beta1 in models of hypersensitivity and arthritis. J. Clin. Invest. 105, 721-729.
31. Dennis, J., Meehan, D. T., Delimont, D., Zallocchi, M., Perry, G. A., O'Brien, S., Tu, H., Pihlajaniemi, T. and Cosgrove, D. (2010). Collagen XIII induced in vascular endotheliummediates alpha1beta1 integrin-dependent transmigration of monocytes in renal fibrosis. Am. J. Pathol. 177, 2527-2540.
32. Driskell, R. R., Lichtenberger, B. M., Hoste, E., Kretzschmar, K., Simons, B. D., Charalambous, M., Ferron, S. R., Herault, Y., Pavlovic, G., Ferguson-Smith, A. C. et al. (2013). Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504, 277-281.
33. Eble, J. A., Golbik, R., Mann, K. and Kuhn, K. (1993). The alpha 1 beta 1 integrin recognition site of the basement membrane collagen molecule [alpha 1(IV)]2 alpha 2(IV). EMBO J. 12, 4795-4802.
34. Eble, J. A., Kassner, A., Niland, S., Morgelin, M., Grifka, J. and Grassel, S. (2006). Collagen XVI harbors an integrin alpha1 beta1 recognition site in its C-terminal domains. J. Biol. Chem. 281, 25745-25756.
35. Edelson, B. T., Li, Z., Pappan, L. K. and Zutter, M. M. (2004). Mast cell-mediated inflammatory responses require the alpha2beta1 integrin. Blood 103, 2214-2220.
36. Ekholm, E., Hankenson, K. D., Uusitalo, H., Hiltunen, A., Gardner, H., Heino, J. and Penttinen, R. (2002). Diminished callus size and cartilage synthesis in alpha 1 beta 1 integrin-deficient mice during bone fracture healing. Am. J. Pathol. 160, 1779-1785.
37. El Azreq, M. A., Arseneault, C., Boisvert, M., Page, N., Allaeys, I., Poubelle, P. E., Tessier, P. A. and Aoudjit, F. (2015). Cooperation between IL-7 receptor and integrin alpha2beta1 (CD49b) drives Th17-mediated bone loss. J. Immunol. 195, 4198-4209.
38. Emsley, J., Knight, C. G., Farndale, R. W., Barnes, M. J. and Liddington, R. C. (2000). Structural basis of collagen recognition by integrin alpha2beta1. Cell 101, 47-56.
39. Engel, B. E., Welsh, E., Emmons, M. F., Santiago-Cardona, P. G. and Cress, W. D. (2013). Expression of integrin alpha 10 is transcriptionally activated by pRb in mouse osteoblasts and is downregulated in multiple solid tumors. Cell Death Dis. 4, e938.
40. Fernando, R. I., Litzinger, M., Trono, P., Hamilton, D. H., Schlom, J. and Palena, C. (2010). The T-box transcription factor Brachyury promotes epithelial-mesenchymal transition in human tumor cells. J. Clin. Invest. 120, 533-544.
41. Fiedler, L. R., Schonherr, E., Waddington, R., Niland, S., Seidler, D. G., Aeschlimann, D. and Eble, J. A. (2008). Decorin regulates endothelial cell motility on collagen I through activation of insulin-like growth factor I receptor and modulation of alpha2beta1 integrin activity. J. Biol. Chem. 283, 17406-17415.
42. Gardner, H. (2014). Integrin alpha1beta1. Adv. Exp. Med. Biol. 819, 21-39.
43. Gardner, H., Kreidberg, J., Koteliansky, V. and Jaenisch, R. (1996). Deletion of integrin α1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. Dev. Biol. 175, 301-313.
44. Gardner, H., Broberg, A., Pozzi, A., Laato, M. and Heino, J. (1999). Absence of integrin alpha1beta1 in the mouse causes loss of feedback regulation of collagen synthesis in normal and wounded dermis. J. Cell Sci. 112, 263-272.
45. Giera, S., Deng, Y., Luo, R., Ackerman, S. D., Mogha, A., Monk, K. R., Ying, Y., Jeong, S.-J., Makinodan, M., Bialas, A. R. et al. (2015). The adhesion G protein-coupled receptor GPR56 is a cell-autonomous regulator of oligodendrocyte development. Nat. Commun. 6, 6121.
46. Gillberg, L., Berg, S., de Verdier, P. J., Lindbom, L., Werr, J. and Hellström, P. M. (2013). Effective treatment of mouse experimental colitis by alpha 2 integrin antibody: comparison with alpha 4 antibody and conventional therapy. Acta Physiol. 207, 326-336.
47. Grenache, D. G., Zhang, Z., Wells, L. E., Santoro, S. A., Davidson, J. M. and Zutter, M. M. (2007). Wound healing in the a2ß1 integrin-deficient mouse: altered keratinocyte biology and dysregulated matrix metalloproteinase expression. J. Invest. Dermatol. 127, 455-466.
48. Gullberg, D. and Lundgren-Åkerlund, E. (2002). Collagen-binding I domain integrins - what do they do? Prog. Histochem. Cytochem. 37, 3-54.
49. Gullberg, D., Turner, D. C., Borg, T. K., Terracio, L. and Rubin, K. (1990). Different beta1-integrin collagen receptors on rat hepatocytes and cardiac fibroblasts. Exp. Cell Res. 190, 254-264.
50. Gullberg, D., Velling, T., Sjöberg, G. and Sejersen, T. (1995). Up-regulation of a novel integrin alpha-chain (alpha mt) on human fetal myotubes. Dev. Dyn. 204, 57-65.
51. Habart, D., Cheli, Y., Nugent, D. J., Ruggeri, Z. M. and Kunicki, T. J. (2013). Conditional knockout of integrin alpha2beta1 in murine megakaryocytes leads to reduced mean platelet volume. PLoS ONE 8, e55094.
52. Hall, C. L., Dai, J., van Golen, K. L., Keller, E. T. and Long, M. W. (2006). Type I collagen receptor (alpha 2 beta 1) signaling promotes the growth of human prostate cancer cells within the bone. Cancer Res. 66, 8648-8654.
53. Hall, C. L., Dubyk, C. W., Riesenberger, T. A., Shein, D., Keller, E. T. and van Golen, K. L. (2008). Type I collagen receptor (alpha2beta1) signaling promotes prostate cancer invasion through RhoC GTPase. Neoplasia 10, 797-803.
54. Hamaia, S. W., Pugh, N., Raynal, N., Nemoz, B., Stone, R., Gullberg, D., Bihan, D. and Farndale, R. W. (2012). Mapping of potent and specific binding motifs, GLOGEN and GVOGEA, for integrin alpha1beta1 using collagen toolkits II and III. J. Biol. Chem. 287, 26019-26028.
55. Harburger, D. S. and Calderwood, D. A. (2009). Integrin signalling at a glance. J. Cell Sci. 122, 159-163.
56. He, L., Pappan, L. K., Grenache, D. G., Li, Z., Tollefsen, D. M., Santoro, S. A. and Zutter, M. M. (2003). The contributions of the alpha 2 beta 1 integrin to vascular thrombosis in vivo. Blood 102, 3652-3657.
57. Heino, J. (2000). The collagen receptor integrins have distinct ligand recognition and signaling functions. Matrix Biol. 19, 319-323.
58. Hemler, M. E., Jacobson, J. G., Brenner, M. B., Mann, D. and Strominger, J. L. (1985a). VLA-1: a T cell surface antigen which defines a novel late stage of human T cell activation. Eur. J. Immunol. 15, 502-508.
59. Hemler, M. E., Jacobson, J. G. and Strominger, J. L. (1985b). Biochemical characterization of VLA-1 and VLA-2. Cell surface heterodimers on activated T cells. J. Biol. Chem. 260, 15246-15252.
60. Henderson, N. C., Arnold, T. D., Katamura, Y., Giacomini, M. M., Rodriguez, J. D., McCarty, J. H., Pellicoro, A., Raschperger, E., Betsholtz, C., Ruminski, P. G. et al. (2013). Targeting of alphav integrin identifies a core molecular pathway that regulates fibrosis in several organs. Nat. Med. 19, 1617-1624.
61. Hewitt, A. T., Varner, H. H., Silver, M. H., Dessau, W., Wilkes, C. M. and Martin, G. R. (1982). The isolation and partial characterization of chondronectin, an attachment factor for chondrocytes. J. Biol. Chem. 257, 2330-2334.
62. Holtkotter, O., Nieswandt, B., Smyth, N., Muller, W., Hafner, M., Schulte, V., Krieg, T. and Eckes, B. (2002). Integrin alpha 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J. Biol. Chem. 277, 10789-10794.
63. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
64. Hynes, R. O. (2007). Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 5 Suppl. 1, 32-40.
65. Hynes, R. O. (2009). The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219.
66. Ianaro, A., Cicala, C., Calignano, A., Koteliansky, V., Gotwals, P., Bucci, M., Gerli, R., Santucci, L., Fiorucci, S. and Cirino, G. (2000). Anti-very late antigen-1 monoclonal antibody modulates the development of secondary lesion and T-cell response in experimental arthritis. Lab. Invest. 80, 73-80.
67. Ignatius, M. J., Large, T. H., Houde, M., Tawil, J. W., Barton, A., Esch, F., Carbonetto, S. and Reichardt, L. F. (1990). Molecular cloning of the rat integrin alpha 1-subunit: a receptor for laminin and collagen. J. Cell Biol. 111, 709-720.
68. Inoue, O., Suzuki-Inoue, K., McCarty, O. J., Moroi, M., Ruggeri, Z. M., Kunicki, T. J., Ozaki, Y. and Watson, S. P. (2006). Laminin stimulates spreading of platelets through integrin alpha6beta1-dependent activation of GPVI. Blood 107, 1405-1412.
69. Ivaska, J., Reunanen, H., Westermarck, J., Koivisto, L., Kähäri, V. M. and Heino, J. (1999). Integrin alpha2beta1 mediates isoform-specific activation of p38 and upregulation of collagen gene transcription by a mechanism involving the alpha2 cytoplasmic tail. J. Cell Biol. 147, 401-416.
70. Jablonski, C. L., Ferguson, S., Pozzi, A. and Clark, A. L. (2014). Integrin alpha1beta1 participates in chondrocyte transduction of osmotic stress. Biochem. Biophys. Res. Commun. 445, 184-190.
71. Jeong, S.-J., Luo, R., Singer, K., Giera, S., Kreidberg, J., Kiyozumi, D., Shimono, C., Sekiguchi, K. and Piao, X. (2013). GPR56 functions together with alpha3beta1 integrin in regulating cerebral cortical development. PLoS ONE 8, e68781.
72. Jokinen, J., Dadu, E., Nykvist, P., Kapyla, J., White, D. J., Ivaska, J., Vehvilainen, P., Reunanen, H., Larjava, H., Hakkinen, L. et al. (2004). Integrin-mediated cell adhesion to type I collagen fibrils. J. Biol. Chem. 279, 31956-31963.
73. Kaltz, N., Ringe, J., Holzwarth, C., Charbord, P., Niemeyer, M., Jacobs, V. R., Peschel, C., Häupl, T. and Oostendorp, R. A. (2010). Novel markers of mesenchymal stem cells defined by genome-wide gene expression analysis of stromal cells from different sources. Exp. Cell Res. 316, 2609-2617.
74. Kang, L., Ayala, J. E., Lee-Young, R. S., Zhang, Z., James, F. D., Neufer, P. D., Pozzi, A., Zutter, M. M. and Wasserman, D. H. (2011). Diet-induced muscle insulin resistance is associated with extracellular matrix remodeling and interaction with integrin alpha2beta1 in mice. Diabetes 60, 416-426.
75. Käpylä, J., Ivaska, J., Riikonen, R., Nykvist, P., Pentikäinen, O., Johnson, M. and Heino, J. (2000). Integrin alpha2 I domain recognizes type I and type IV collagens by different mechanisms. J. Biol. Chem. 275, 3348-3354.
76. Kapyla, J., Jaalinoja, J., Tulla, M., Ylostalo, J., Nissinen, L., Viitasalo, T., Vehvilainen, P., Marjomaki, V., Nykvist, P., Saamanen, A.-M. et al. (2004). The fibril-associated collagen IX provides a novel mechanism for cell adhesion to cartilaginous matrix. J. Biol. Chem. 279, 51677-51687.
77. Ke, X.-S., Qu, Y., Goldfinger, N., Rostad, K., Hovland, R., Akslen, L., Rotter, V., Øyan, A. and Kalland, K. (2008). Epithelial to mesenchymal transition of a primary prostate cell line with switches of cell adhesion modules but without malignant transformation. PLoS ONE 3, e3368.
78. Kehrel, B., Wierwille, S., Clemetson, K. J., Anders, O., Steiner, M., Knight, C. G., Farndale, R.W., Okuma, M. and Barnes, M. J. (1998). Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet-activating quaternary structure of collagen, whereas CD36, glycoprotein IIb/IIIa, and von Willebrand factor do not. Blood 91, 491-499.
79. Kern, A., Eble, J., Golbik, R. and Kuhn, K. (1993). Interaction of type IV collagen with the isolated integrins alpha1beta1 and alpha2beta1. Eur. J. Biochem. 215, 151-159.
80. Kramer, R. H. and Marks, N. (1989). Identification of integrin collagen receptors on human melanoma cells. J. Biol. Chem. 264, 4684-4688.
81. Krieglstein, C. F., Cerwinka, W. H., Sprague, A. G., Laroux, F. S., Grisham, M. B., Koteliansky, V. E., Senninger, N., Granger, D. N. and de Fougerolles, A. R. (2002). Collagen-binding integrin alpha1beta1 regulates intestinal inflammation in experimental colitis. J. Clin. Invest. 110, 1773-1782.
82. Kuijpers, M. J., Pozgajova, M., Cosemans, J. M., Munnix, I. C., Eckes, B., Nieswandt, B. and Heemskerk, J. W. (2007). Role of murine integrin alpha2beta1 in thrombus stabilization and embolization: contribution of thromboxane A2. Thromb. Haemost. 98, 1072-1080.
83. Kunicki, T. J. and Nugent, D. J. (2010). The genetics of normal platelet reactivity. Blood 116, 2627-2634.
84. Kyöstilä, K., Lappalainen, A. K. and Lohi, H. (2013). Canine chondrodysplasia caused by a truncating mutation in collagen-binding integrin alpha subunit 10. PLoS ONE 8, e75621.
85. Labrador, J. P., Azcoitia, V., Tuckermann, J., Lin, C., Olaso, E., Manes, S., Bruckner, K., Goergen, J.-L., Lemke, G., Yancopoulos, G. et al. (2001). The collagen receptor DDR2 regulates proliferation and its elimination leads to dwarfism. EMBO Rep. 2, 446-452.
86. Leitinger, B. (2011). Transmembrane collagen receptors. Annu. Rev. Cell Dev. Biol. 27, 265-290.
87. Leitinger, B. (2014). Discoidin domain receptor functions in physiological and pathological conditions. Int. Rev. Cell Mol. Biol. 310, 39-87.
88. Lenci, R. E., Rachakonda, P. S., Kubarenko, A. V., Weber, A. N. R., Brandt, A., Gast, A., Sucker, A., Hemminki, K., Schadendorf, D. and Kumar, R. (2012). Integrin genes and susceptibility to human melanoma. Mutagenesis 27, 367-373.
89. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F. T., Csiszar, K., Giaccia, A., Weninger, W. et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906.
90. Lu, N., Carracedo, S., Ranta, J., Heuchel, R., Soininen, R. and Gullberg, D. (2010). The human alpha11 integrin promoter drives fibroblast-restricted expression in vivo and is regulated by TGF-beta1 in a Smad- and Sp1-dependent manner. Matrix Biol. 29, 166-176.
91. Lu, N., Karlsen, T. V., Reed, R. K., Kusche-Gullberg, M. and Gullberg, D. (2014). Fibroblast alpha11beta1 integrin regulates tensional homeostasis in fibroblast/A549 carcinoma heterospheroids. PLoS ONE 9, e103173.
92. Lundberg, S., Lindholm, J., Lindbom, L., Hellström, P. M. and Werr, J. (2006). Integrin alpha2beta1 regulates neutrophil recruitment and inflammatory activity in experimental colitis in mice. Inflamm. Bowel Dis. 12, 172-177.
93. Lundgren-Åkerlund, E. and Aszòdi, A. (2014). Integrin alpha10beta1: a collagen receptor critical in skeletal development. Adv. Exp. Med. Biol. 819, 61-71.
94. Luo, R., Jin, Z., Deng, Y., Strokes, N. and Piao, X. (2012). Disease-associated mutations prevent GPR56-collagen III interaction. PLoS ONE 7, e29818.
95. Macias-Perez, I., Borza, C., Chen, X., Yan, X., Ibanez, R., Mernaugh, G., Matrisian, L. M., Zent, R. and Pozzi, A. (2008). Loss of integrin alpha1beta1 ameliorates Kras-induced lung cancer. Cancer Res. 68, 6127-6135.
96. Madamanchi, A., Capozzi, M., Geng, L., Li, Z., Friedman, R. D., Dickeson, S. K., Penn, J. S. and Zutter, M. M. (2014a). Mitigation of oxygen-induced retinopathy in alpha2beta1 integrin-deficient mice. Invest. Ophthalmol. Vis. Sci. 55, 4338-4347.
97. Madamanchi, A., Santoro, S. A. and Zutter, M. M. (2014b). alpha2beta1 Integrin. Adv. Exp. Med. Biol. 819, 41-60.
98. Marjoram, R. J., Li, Z., He, L., Tollefsen, D. M., Kunicki, T. J., Dickeson, S. K., Santoro, S. A. and Zutter, M. M. (2014). alpha2beta1 integrin, GPVI receptor, and common FcRgamma chain on mouse platelets mediate distinct responses to collagen in models of thrombosis. PLoS ONE 9, e114035.
99. Matsuoka, T., Yashiro, M., Nishimura, S., Inoue, T., Fujihara, T., Sawada, T., Kato, Y., Seki, S. and Hirakawa-Ys Chung, K. (2000). Increased expression of alpha2beta1-integrin in the peritoneal dissemination of human gastric carcinoma. Int. J. Mol. Med. 5, 21-25.
100. Mattila, E., Pellinen, T., Nevo, J., Vuoriluoto, K., Arjonen, A. and Ivaska, J. (2005). Negative regulation of EGFR signalling through integrin-alpha1beta1-mediated activation of protein tyrosine phosphatase TCPTP. Nat. Cell Biol. 7, 78-85.
101. Mattila, E., Auvinen, K., Salmi, M. and Ivaska, J. (2008). The protein tyrosine phosphatase TCPTP controls VEGFR2 signalling. J. Cell Sci. 121, 3570-3580.
102. Merkel, J. R., DiPaolo, B. R., Hallock, G. G. and Rice, D. C. (1988). Type I and type III collagen content of healing wounds in fetal and adult rats. Exp. Biol. Med. 187, 493-497.
103. Meyaard, L. (2008). The inhibitory collagen receptor LAIR-1 (CD305). J. Leukoc. Biol. 83, 799-803.
104. Meyaard, L. (2010). LAIR and collagens in immune regulation. Immunol. Lett. 128, 26-28.
105. Mita, M., Kelly, K. R., Mita, A., Ricart, A. D., Romero, O., Tolcher, A., Hook, L., Okereke, C., Krivelevich, I., Rossignol, D. P. et al. (2011). Phase I study of E7820, an oral inhibitor of integrin alpha-2 expression with antiangiogenic properties, in patients with advanced malignancies. Clin. Cancer Res. 17, 193-200.
106. Moeckel, G. W., Zhang, L., Chen, X., Rossini, M., Zent, R. and Pozzi, A. (2006). Role of integrin alpha1beta1 in the regulation of renal medullary osmolyte concentration. Am. J. Physiol. Renal Physiol. 290, F223-F231.
107. Mu, Y., Gudey, S. K. and Landström, M. (2012). Non-Smad signaling pathways. Cell Tissue Res. 347, 11-20.
108. Munger, J. S. and Sheppard, D. (2011). Cross talk among TGF-beta signaling pathways, integrins, and the extracellular matrix. Cold Spring Harb. Perspect. Biol. 3, a005017.
109. Navab, R., Strumpf, D., Bandarchi, B., Zhu, C.-Q., Pintilie, M., Ramnarine, V. R., Ibrahimov, E., Radulovich, N., Leung, L., Barczyk, M. et al. (2011). Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer. Proc. Natl. Acad. Sci. USA 108, 7160-7165.
110. Navab, R., Strumpf, D., To, C., Pasko, E., Kim, K. S., Park, C. J., Hai, J., Liu, J., Jonkman, J., Barczyk, M. et al. (2015). Integrin alpha11beta1 regulates cancer stromal stiffness and promotes tumorigenicity and metastasis in non-small cell lung cancer. Oncogene. doi:10.1038/onc.2015.254
111. Nissinen, L., Koivunen, J., Käpylä, J., Salmela, M., Nieminen, J., Jokinen, J., Sipilä, K., Pihlavisto, M., Pentikäinen, O. T., Marjamäki, A. et al. (2012). Novel alpha2beta1 integrin inhibitors reveal that integrin binding to collagen under shear stress conditions does not require receptor preactivation. J. Biol. Chem. 287, 44694-44702.
112. Nykvist, P., Tu, H., Ivaska, J., Käpylä, J., Pihlajaniemi, T. and Heino, J. (2000). Distinct recognition of collagen subtypes by alpha1beta1 and alpha2beta1 integrins. Alpha1beta1 mediates cell adhesion to type XIII collagen. J. Biol. Chem. 275, 8255-8261.
113. Olde Nordkamp, M. J. M., van Eijk, M., Urbanus, R. T., Bont, L., Haagsman, H. P. and Meyaard, L. (2014). Leukocyte-associated Ig-like receptor-1 is a novel inhibitory receptor for surfactant protein D. J. Leukoc. Biol. 96, 105-111.
114. Parekh, R., Lorenzo, M. K., Shin, S. Y., Pozzi, A. and Clark, A. L. (2014). Integrin alpha1beta1 differentially regulates cytokine-mediated responses in chondrocytes. Osteoarthritis Cartilage 22, 499-508.
115. Parks, W. C. (2007). What is the alpha2beta1 integrin doing in the epidermis? J. Invest. Dermatol. 127, 264-266.
116. Peng, Y.-M., van de Garde, M. D. B., Cheng, K.-F., Baars, P. A., Remmerswaal, E. B. M., van Lier, R. A. W., Mackay, C. R., Lin, H.-H. and Hamann, J. (2011). Specific expression of GPR56 by human cytotoxic lymphocytes. J. Leukoc. Biol. 90, 735-740.
117. Peters, M. A., Wendholt, D., Strietholt, S., Frank, S., Pundt, N., Korb-Pap, A., Joosten, L. A. B., van den Berg, W. B., Kollias, G., Eckes, B. et al. (2012). The loss of alpha2beta1 integrin suppresses joint inflammation and cartilage destruction in mouse models of rheumatoid arthritis. Arthritis Rheum. 64, 1359-1368.
118. Popov, C., Radic, T., Haasters, F., Prall, W. C., Aszodi, A., Gullberg, D., Schieker, M. and Docheva, D. (2011). Integrins alpha2beta1 and alpha11beta1 regulate the survival of mesenchymal stem cells on collagen I. Cell Death Dis. 2, e186.
119. Popova, S. N., Rodriguez-Sánchez, B., Lidén, A., Betsholtz, C., van Den Bos, T. and Gullberg, D. (2004). The mesenchymal alpha11beta1 integrin attenuates PDGF-BB-stimulated chemotaxis of embryonic fibroblasts on collagens. Dev. Biol. 270, 427-442.
120. Popova, S. N., Barczyk, M., Tiger, C.-F., Beertsen, W., Zigrino, P., Aszodi, A., Miosge, N., Forsberg, E. and Gullberg, D. (2007a). Alpha11 beta1 integrindependent regulation of periodontal ligament function in the erupting mouse incisor. Mol. Cell. Biol. 27, 4306-4316.
121. Popova, S. N., Lundgren-Åkerlund, E., Wiig, H. and Gullberg, D. (2007b). Physiology and pathology of collagen receptors. Acta Physiol. 190, 179-187.
122. Pozzi, A., Wary, K. K., Giancotti, F. G. and Gardner, H. A. (1998). Integrin alpha1beta1 mediates a unique collagen-dependent proliferation pathway in vivo. J. Cell Biol. 142, 587-594.
123. Pozzi, A., Moberg, P. E., Miles, L. A., Wagner, S., Soloway, P. and Gardner, H. A. (2000). Elevated matrix metalloprotease and angiostatin levels in integrin alpha1 knockout mice cause reduced tumor vascularization. Proc. Natl. Acad. Sci. USA 97, 2202-2207.
124. Provenzano, P. P., Eliceiri, K.W., Campbell, J. M., Inman, D. R., White, J. G. and Keely, P. J. (2006). Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 4, 38.
125. Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Knittel, J. G., Yan, L., Rueden, C. T., White, J. G. and Keely, P. J. (2008). Collagen density promotes mammary tumor initiation and progression. BMC Med. 6, 11.
126. Provenzano, P. P., Eliceiri, K. W. and Keely, P. J. (2009). Shining new light on 3D cell motility and the metastatic process. Trends Cell Biol. 19, 638-648.
127. Ramirez, N. E., Zhang, Z., Madamanchi, A., Boyd, K. L., O'Rear, L. D., Nashabi, A., Li, Z., Dupont, W. D., Zijlstra, A. and Zutter, M. M. (2011). The alpha2beta1 integrin is a metastasis suppressor in mouse models and human cancer. J. Clin. Invest. 121, 226-237.
128. Ravanti, L., Heino, J., Lopez-Otin, C. and Kahari, V.-M. (1999). Induction of collagenase-3 (MMP-13) expression in human skin fibroblasts by three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J. Biol. Chem. 274, 2446-2455.
129. Reed, N. I., Jo, H., Chen, C., Tsujino, K., Arnold, T. D., DeGrado, W. F. and Sheppard, D. (2015). The alphavbeta1 integrin plays a critical in vivo role in tissue fibrosis. Sci Transl Med 7, 288ra79.
130. Reinisch, A., Etchart, N., Thomas, D., Hofmann, N. A., Fruehwirth, M., Sinha, S., Chan, C. K., Senarath-Yapa, K., Seo, E.-Y., Wearda, T. et al. (2015). Epigenetic and in vivo comparison of diverse MSC sources reveals an endochondral signature for human hematopoietic niche formation. Blood 125, 249-260.
131. Rinkevich, Y., Walmsley, G. G., Hu, M. S., Maan, Z. N., Newman, A. M., Drukker, M., Januszyk, M., Krampitz, G. W., Gurtner, G. C., Lorenz, H. P. et al. (2015). Skin fibrosis. Identification and isolation of a dermal lineage with intrinsic fibrogenic potential. Science 348, aaa2151.
132. Rodriguez, A., Karen, J., Gardner, H., Gerdin, B., Rubin, K. and Sundberg, C. (2009). Integrin alpha1beta1 is involved in the differentiation into myofibroblasts in adult reactive tissues in vivo. J. Cell. Mol. Med. 13, 3449-3462.
133. Ronzière, M.-C., Aubert-Foucher, E., Gouttenoire, J., Bernaud, J., Herbage, D. and Mallein-Gerin, F. (2005). Integrin alpha1beta1 mediates collagen induction of MMP-13 expression in MC615 chondrocytes. Biochim. Biophys. Acta 1746, 55-64.
134. Rubel, D., Frese, J., Martin, M., Leibnitz, A., Girgert, R., Miosge, N., Eckes, B., Müller, G.-A. and Gross, O. (2014). Collagen receptors integrin alpha2beta1 and discoidin domain receptor 1 regulate maturation of the glomerular basement membrane and loss of integrin alpha2beta1 delays kidney fibrosis in COL4A3 knockout mice. Matrix Biol. 34, 13-21.
135. Rybinski, B., Franco-Barraza, J. and Cukierman, E. (2014). The wound healing, chronic fibrosis, and cancer progression triad. Physiol. Genomics 46, 223-244.
136. Santoro, S. A. (1986). Identification of a 160,000 dalton platelet membrane protein that mediates the initial divalent cation-dependent adhesion of platelets to collagen. Cell 46, 913-920.
137. Santoso, S., Kunicki, T. J., Kroll, H., Haberbosch, W. and Gardemann, A. (1999). Association of the platelet glycoprotein Ia C807T gene polymorphism with nonfatal myocardial infarction in younger patients. Blood 93, 2449-2453.
138. Schäfer, M. and Werner, S. (2008). Cancer as an overhealing wound: an old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 9, 628-638.
139. Schapira, K., Lutgens, E., de Fougerolles, A., Sprague, A., Roemen, A., Gardner, H., Koteliansky, V., Daemen, M. and Heeneman, S. (2005). Genetic deletion or antibody blockade of alpha1beta1 integrin induces a stable plaque phenotype in ApoE-/- mice. Arterioscler. Thromb. Vasc. Biol. 25, 1917-1924.
140. Schultz, G. S., Davidson, J. M., Kirsner, R. S., Bornstein, P. and Herman, I. M. (2011). Dynamic reciprocity in the wound microenvironment. Wound Repair Regen. 19, 134-148.
141. Schultz, H. S., Nitze, L. M., Zeuthen, L. H., Keller, P., Gruhler, A., Pass, J., Chen, J., Guo, L., Fleetwood, A. J., Hamilton, J. A. et al. (2015). Collagen induces maturation of human monocyte-derived dendritic cells by signaling through osteoclast-associated receptor. J. Immunol. 194, 3169-3179.
142. Schulz, J.-N., Zeltz, C., Sørensen, I. W., Barczyk, M., Carracedo, S., Hallinger, R., Niehoff, A., Eckes, B. and Gullberg, D. (2015). Reduced granulation tissue and wound strength in the absence of alpha11beta1 integrin. J. Invest. Dermatol. 135, 1435-1444.
143. Seong, J., Tajik, A., Sun, J., Guan, J.-L., Humphries, M. J., Craig, S. E., Shekaran, A., Garcia, A. J., Lu, S., Lin, M. Z. et al. (2013). Distinct biophysical mechanisms of focal adhesion kinase mechanoactivation by different extracellular matrix proteins. Proc. Natl. Acad. Sci. USA 110, 19372-19377.
144. Siljander, P. R.-M., Hamaia, S., Peachey, A. R., Slatter, D. A., Smethurst, P. A., Ouwehand, W. H., Knight, C. G. and Farndale, R. W. (2004). Integrin activation state determines selectivity for novel recognition sites in fibrillar collagens. J. Biol. Chem. 279, 47763-47772.
145. Sipilä, K., Haag, S., Denessiouk, K., Käpylä, J., Peters, E. C., Denesyuk, A., Hansen, U., Konttinen, Y., Johnson, M. S., Holmdahl, R. et al. (2014). Citrullination of collagen II affects integrin-mediated cell adhesion in a receptor-specific manner. FASEB J. 28, 3758-3768.
146. Sodek, J. and Ferrier, J. M. (1988). Collagen remodelling in rat periodontal tissues: compensation for precursor reutilization confirms rapid turnover of collagen. Coll. Relat. Res. 8, 11-21.
147. Staatz, W. D., Rajpara, S. M., Wayner, E. A., Carter, W. G. and Santoro, S. A. (1989). The membrane glycoprotein Ia-IIa (VLA-2) complex mediates the Mg++-dependent adhesion of platelets to collagen. J. Cell Biol. 108, 1917-1924.
148. Stange, R., Kronenberg, D., Timmen, M., Everding, J., Hidding, H., Eckes, B., Hansen, U., Holtkamp, M., Karst, U., Pap, T. et al. (2013). Age-related bone deterioration is diminished by disrupted collagen sensing in integrin alpha2beta1 deficient mice. Bone 56, 48-54.
149. Staudinger, L. A., Spano, S. J., Lee, W., Coelho, N., Rajshankar, D., Bendeck, M. P., Moriarty, T. and McCulloch, C. A. (2013). Interactions between the discoidin domain receptor 1 and beta1 integrin regulate attachment to collagen. Biol. Open 2, 1148-1159.
150. Sulem, P., Helgason, H., Oddson, A., Stefansson, H., Gudjonsson, S. A., Zink, F., Hjartarson, E., Sigurdsson, G. T., Jonasdottir, A., Jonasdottir, A. et al. (2015). Identification of a large set of rare complete human knockouts. Nat. Genet. 47, 448-452.
151. Suzuki, K., Okuno, T., Yamamoto, M., Pasterkamp, R. J., Takegahara, N., Takamatsu, H., Kitao, T., Takagi, J., Rennert, P. D., Kolodkin, A. L. et al. (2007). Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin. Nature 446, 680-684.
152. Talior-Volodarsky, I., Connelly, K. A., Arora, P. D., Gullberg, D. and McCulloch, C. A. (2012). alpha11 integrin stimulates myofibroblast differentiation in diabetic cardiomyopathy. Cardiovasc. Res. 96, 265-275.
153. Talior-Volodarsky, I., Arora, P. D., Wang, Y., Zeltz, C., Connelly, K. A., Gullberg, D. and McCulloch, C. A. (2015). Glycated collagen induces alpha11 integrin expression through TGF-beta2 and Smad3. J. Cell. Physiol. 230, 327-336.
154. Termine, J. D., Kleinman, H. K., Whitson, S. W., Conn, K. M., McGarvey, M. L. and Martin, G. R. (1981). Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26, 99-105.
155. Tiger, C.-F., Fougerousse, F., Grundström, G., Velling, T. and Gullberg, D. (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.
156. Tran, T., Barlow, B., O'Rear, L., Jarvis, B., Li, Z., Dickeson, K., Dupont, W. and Zutter, M. (2011). Loss of the alpha2beta1 integrin alters human papilloma virus-induced squamous carcinoma progression in vivo and in vitro. PLoS ONE 6, e26858.
157. Varas, L., Ohlsson, L. B., Honeth, G., Olsson, A., Bengtsson, T., Wiberg, C., Bockermann, R., Järnum, S., Richter, J., Pennington, D. et al. (2007). Alpha10 integrin expression is up-regulated on fibroblast growth factor-2-treated mesenchymal stem cells with improved chondrogenic differentiation potential. Stem Cells Dev. 16, 965-978.
158. Velling, T., Kusche-Gullberg, M., Sejersen, T. and Gullberg, D. (1999). cDNA cloning and chromosomal localization of human alpha11 integrin. A collagen-binding, I domain-containing, beta1-associated integrin alpha-chain present in muscle tissues. J. Biol. Chem. 274, 25735-25742.
159. Vogel, W., Gish, G. D., Alves, F. and Pawson, T. (1997). The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1, 13-23.
160. Vogel, W. F., Aszodi, A., Alves, F. and Pawson, T. (2001). Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol. Cell. Biol. 21, 2906-2917.
161. Wang, K.-k., Liu, N., Radulovich, N., Wigle, D. A., Johnston, M. R., Shepherd, F. A., Minden, M. D. and Tsao, M.-S. (2002). Novel candidate tumor marker genes for lung adenocarcinoma. Oncogene 21, 7598-7604.
162. Wary, K. K., Mainiero, F., Isakoff, S. J., Marcantonio, E. E. and Giancotti, F. G. (1996). The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87, 733-743.
163. Wenke, A. K., Kjellman, C., Lundgren-Akerlund, E., Uhlmann, C., Haass, N. K., Herlyn, M. and Bosserhoff, A. K. (2007). Expression of integrin alpha10 is induced in malignant melanoma. Cell Oncol. 29, 373-386.
164. Westcott, J. M., Prechtl, A. M., Maine, E. A., Dang, T. T., Esparza, M. A., Sun, H., Zhou, Y., Xie, Y. and Pearson, G. W. (2015). An epigenetically distinct breast cancer cell subpopulation promotes collective invasion. J. Clin. Invest. 125, 1927-1943.
165. Williams, A. S., Kang, L., Zheng, J., Grueter, C., Bracy, D. P., James, F. D., Pozzi, A. andWasserman, D. H. (2015). Integrin alpha1-null mice exhibit improved fatty liver when fed a high fat diet despite severe hepatic insulin resistance. J. Biol. Chem. 290, 6546-6557.
166. Wondimu, Z., Gorfu, G., Kawataki, T., Smirnov, S., Yurchenco, P., Tryggvason, K. and Patarroyo, M. (2006). Characterization of commercial laminin preparations from human placenta in comparison to recombinant laminins 2 (alpha2beta1gamma1), 8 (alpha4beta1gamma1), 10 (alpha5beta1gamma1). Matrix Biol. 25, 89-93.
167. Woodall, B. P., Nystrom, A., Iozzo, R. A., Eble, J. A., Niland, S., Krieg, T., Eckes, B., Pozzi, A. and Iozzo, R. V. (2008). Integrin alpha2beta1 is the required receptor for endorepellin angiostatic activity. J. Biol. Chem. 283, 2335-2343.
168. Xiong, G., Deng, L., Zhu, J., Rychahou, P. G. and Xu, R. (2014). Prolyl-4-hydroxylase alpha subunit 2 promotes breast cancer progression and metastasis by regulating collagen deposition. BMC Cancer 14, 1.
169. Xu, H., Bihan, D., Chang, F., Huang, P. H., Farndale, R. W. and Leitinger, B. (2012). Discoidin domain receptors promote alpha1beta1-and alpha2beta1-integrin mediated cell adhesion to collagen by enhancing integrin activation. PLoS ONE 7, e52209.
170. Yang, L. and Xu, L. (2012). GPR56 in cancer progression: current status and future perspective. Future Oncol. 8, 431-440.
171. Yang, L., Friedland, S., Corson, N. and Xu, L. (2014). GPR56 inhibits melanoma growth by internalizing and degrading its ligand TG2. Cancer Res. 74, 1022-1031.
172. Yazlovitskaya, E. M., Tseng, H.-Y., Viquez, O., Tu, T., Mernaugh, G., McKee, K. K., Riggins, K., Quaranta, V., Pathak, A., Carter, B. D. et al. (2015). Integrin alpha3beta1 regulates kidney collecting duct development via TRAF6-dependent K63-linked polyubiquitination of Akt. Mol. Biol. Cell 26, 1857-1874.
173. Zahid, M., Mangin, P., Loyau, S., Hechler, B., Billiald, P., Gachet, C. and Jandrot-Perrus, M. (2012). The future of glycoprotein VI as an antithrombotic target. J. Thromb. Haemost. 10, 2418-2427.
174. Zeltz, C. and Gullberg, D. (2014). Post-translational modifications of integrin ligands as pathogenic mechanisms in disease. Matrix Biol. 40, 5-9.
175. Zeltz, C., Brézillon, S., Käpylä, J., Eble, J. A., Bobichon, H., Terryn, C., Perreau, C., Franz, C. M., Heino, J., Maquart, F.-X. et al. (2010). Lumican inhibits cell migration through alpha2beta1 integrin. Exp. Cell Res. 316, 2922-2931.
176. Zeltz, C., Orgel, J. and Gullberg, D. (2014). Molecular composition and function of integrin-based collagen glues-introducing COLINBRIs. Biochim. Biophys. Acta 1840, 2533-2548.
177. Zemmyo, M., Meharra, E. J., Kühn, K., Creighton-Achermann, L. and Lotz, M. (2003). Accelerated, aging-dependent development of osteoarthritis in alpha1 integrin-deficient mice. Arthritis Rheum. 48, 2873-2880.
178. Zent, R., Yan, X., Su, Y., Hudson, B. G., Borza, D. B., Moeckel, G. W., Qi, Z., Sado, Y., Breyer, M. D., Voziyan, P. et al. (2006). Glomerular injury is exacerbated in diabetic integrin alpha1-null mice. Kidney Int. 70, 460-470.
179. Zhang, Z.-G., Bothe, I., Hirche, F., Zweers, M., Gullberg, D., Pfitzer, G., Krieg, T., Eckes, B. and Aumailley, M. (2006). Interactions of primary fibroblasts and keratinocytes with extracellular matrix proteins: contribution of alpha2beta1 integrin. J. Cell Sci. 119, 1886-1895.
180. Zhu, C.-Q., Popova, S. N., Brown, E. R. S., Barsyte-Lovejoy, D., Navab, R., Shih, W., Li, M., Lu, M., Jurisica, I., Penn, L. Z. et al. (2007). Integrin alpha 11 regulates IGF2 expression in fibroblasts to enhance tumorigenicity of human non-small-cell lung cancer cells. Proc. Natl. Acad. Sci. USA 104, 11754-11759.
181. Zweers, M. C., Davidson, J. M., Pozzi, A., Hallinger, R., Janz, K., Quondamatteo, F., Leutgeb, B., Krieg, T. and Eckes, B. (2007). Integrin alpha2beta1 is required for regulation of murine wound angiogenesis but is dispensable for reepithelialization. J. Invest. Dermatol. 127, 467-478.