Role of discoidin domain receptor 2 in wound healing

Histology and Histopathology

Volumn 29, Issue 11, 2014, Pages 1355-1364

  Márquez, Joana ^a   Olaso, Elvira ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Collagen; Discoidin domain receptors; Myofibroblast; Receptor; Tyrosine kinase; Wound healing

Indexed keywords

COLLAGEN; DISCOIDIN RECEPTOR; INTEGRIN; LECTIN RECEPTOR; PROTEIN TYROSINE KINASE;

ANIMAL; CELL PROLIFERATION; CHEMISTRY; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION; SKIN; WOUND HEALING;

ANIMALS; CELL PROLIFERATION; COLLAGEN; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; INTEGRINS; MICE; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; SIGNAL TRANSDUCTION; SKIN; WOUND HEALING;

EID: 84929928524     PISSN: 02133911     EISSN: 16995848     Source Type: Journal    
DOI: None     Document Type: Review

References (92)

1. Abangan R., Williams C., Mehrotra M., Duncan J. and LaRue A. (2010). MCP1 directs trafficking of hematopoietic stem cell-derived fibroblast precursors in solid tumor. Exp. Hematol. 34, 219-229.
2. Alves F., Vogel W., Mossie K., Millauer B., Höfler H. and Ullrich (1995). A. Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10, 609-618.
3. Aplin A., Howe A., Alahari S. and Juliano R. (1998). Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol. Rev. 50, 197-263.
4. Avivi-Green C., Singal M. and Vogel W.F. (2006). Discoidin domain receptor 1 deficient mice are resistant to bleomycin-induced lung fibrosis. Am. J. Respir. Crit. Care Med. 174, 420-427.
5. Barczyk M., Carracedo S. and Gullberg D. (2010). Integrins. Cell Tissue Res. 339, 269-280.
6. Barker K.T., Martindale J.E., Mitchell P.J., Kamalati T., Page M.J., Phippard D.J., Dale T.C., Gusterson B.A. and Crompton M.R. (1995). Expression patterns of the novel receptor-like tyrosine kinase, DDR, in human breast tumours. Oncogene 10, 569575.
7. Baum C. and Arpey C. (2005). Normal cutaneous wound healing: Clinical correlation with cellular and molecular events. Dermatol. Surg. 31, 6.
8. Beare A., O’Kane S., Krane S. and Ferguson M. (2003). Severely impaired wound healing in the collagenase-resistant mouse. J. Invest. Dermatol. 120, 153-163.
9. Bhadriraju K., Chung K., Spurlin T., Haynes R., Elliott J. and Plant A. (2009). The relative roles of collagen adhesive receptor DDR2 activation and matrix stiffness on the downregulation of focal adhesion kinase in vascular smooth muscle cells. Biomaterials 30, 6687-6694.
10. Boudreau N. and Bissell M. (1998). Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr. Opin. Cell Biol. 10, 640-646.
11. Bullard K., Lund L., Mudgett J., Mellin T., Hunt T., Murphy B., Ronan J., Werb Z. and Banda M. (1999). Impaired wound contraction in stromelysin-1- deficient mice. Ann. Surg. 230, 260-265.
12. Carafoli F., Bihan D., Stathopoulos S., Konitsiotis A., Kvansakul M., Farndale R., Leitinger B. and Hohenester E. (2009). Crystallographic insight into collagen recognition by discoidin domain receptor 2. Structure 1, 1573-1581.
13. Day E., Waters B., Spiegel K., Alnadaf T., Manley P., Buchdunger E., Walker C. and Jarai G. (2008). Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib and dasatinib. Eur. J. Pharmacol. 3, 599 44-53.
14. Dejmek J., Dib K., Jönsson M., and Andersson T. (2003). Wnt-5a and G-protein signaling are required for collagen-induced DDR1 receptor activation and normal mammary cell adhesion. Int. J. Cancer 103, 344-351.
15. Delavary B., Van der Veer W., Van Egmond M., Niessen F. and Beelen R. (2011). Macrophages in skin injury and repair. Immunobiology 216, 753-762.
16. Di Marco E., Cutuli N.. Guerra L., Cancedda R. and De Luca M. (1993). Molecular cloning of trkE, a novel trk-related putative tyrosine kinase receptor isolated from normal human keratinocytes and widely expressed by normal human tissues, J. Biol. Chem. 268, 24290-24295.
17. Duffield J., Lupher M., Thannickal V. and Wynn T. (2013) Host responses in tissue repair and fibrosis. Annu. Rev. Pathol. 8, 241-76.
18. Ebihara Y., Masuyaa M., LaRue A., Fleming P., Visconti R., Minamiguchi H., Drake C. and Ogawa M. (2006). Hematopoietic origins of fibroblasts: II. In vitro studies of fibroblasts, CFU-F and fibrocytes. Exp. Hemat. 34, 219-229.
19. Eitinger B. (2011). Transmembrane collagen receptors. Annu. Rev. Cell Dev. Biol. 27, 265-290.
20. Exposito J., Valcourt U., Cluzel C. and Lethias C. (2010). The fibrillar collagen family. Int. J. Mol. Sci. 11, 407-426.
21. Faraci E., Eck M., Gerstmayer B., Bosio A. and Vogel W.F. (2003). An extracellular matrix specific microarray allowed the identification of target genes downstream of discoidin domain receptors. Matrix Biol. 22, 373-381.
22. Feezor R.J., Paddock H.N., Baker H.V., Varela J.C., Barreda J., Moldawer L.L., Schultz G.S. and Mozingo D.W. (2004). Temporal patterns of gene expression in murine cutaneous burn wound healing. Physiol Genomics. 16, 41-48.
23. Gabbiani G., Ryan G., Badonnel M. and Majno G. (1972). Smooth muscle antigens in platelets: immunofluorescent detection using human anti-smooth muscle serum. Pathol. Biol. Supple, 6-10.
24. Gamble J., Matthias L., Meyer G., Kaur P., Russ G., Faull R., Berndt M. and Vadas M. (1993). Regulation of in vitro capillary tube formation by anti-integrin antibodies. J. Cell Biol. 121, 931-943.
25. Gurtner G., Werner S., Barrandon Y. and Longaker M. (2008). Wound repair and regeneration. Nature 453, 314-421.
26. Huang P. (2012). Phosphoproteomic studies of receptor tyrosine kinases: future perspectives. Mol. Biosyst. 8, 1100-1107.
27. Hynes R. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
28. Ikeda K., Wang L.H., Torres R., Zhao H., Olaso E., Eng F.J., Labrador P., Klein R., Lovett D., Yancopoulos G.D., Friedman S.L. and Lin H.C. (2002). Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen. J. Biol. Chem. 277, 19206-11922.
29. Ingber D. (2006). Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20, 811-827.
30. Iwai L., Chang F. and Huang P. (2013). Phosphoproteomic analysis identifies insulin enhancement of discoidin domain receptor 2 phosphorylation. Cell Adh. Migr. 7, 1-4.
31. Iwaisako K., David A., Brenner D.A. and Kisseleva T. (2012). What’s new in liver fibrosis? The origin of myofibroblasts in liver fibrosis. J. Gastroenterol. Hepatol. 27 (Suppl. 2), 65-68
32. Johnson J., Edman J. and Rutter W. (1993). A receptor tyrosine kinase found in breast carcinoma cells has an extracellular discoidin I-like domain. Proc. Natl. Acad. Sci. USA 90, 5677-5681.
33. Johnson M., Lu N. Denessiouk K., Heino J. and Gullberg D. (2009). Integrins during evolution: Evolutionary trees and model organisms. Biochim. Biophysic. Acta 4, 779-789.
34. Jönsson M. and Andersson T. (2001). Repression of Wnt-5a impairs DDR1 phosphorylation and modifies adhesion and migration of mammary cells. J. Cell Sci. 114, 2043-2053.
35. Kagan H. and Li W. (2003). Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J. Cell. Biochem. 88, 660-672.
36. Kano K., Marín de Evsikova C., Young J., Wnek C., Maddatu T.P., Nishina P.M. and Naggert J.K. (2008). A novel dwarfism with gonadal dysfunction due to loss-of-function allele of the collagen receptor gene, Ddr2, in the mouse. Mol. Endocrinol. 22, 1866-1880.
37. Kim H., Hwang S., Aaronson S., Mandinova A. and Lee S. (2011), DDR1 receptor tyrosine kinase promotes prosurvival pathway through Notch1 activation. J. Biol. Chem. 286, 17672-17681.
38. Koo D., McFadden C., Huang Y., Abdulhussein R., Friese-Hamim M. and Vogel W. (2006). Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett. 580, 15e 22.
39. Labrador J., Azcoitia V., Tuckermann J., Lin C., Olaso E., Mañes S., Brückner K., Goergen J., Lemke G., Yancopoulos G., Angel P., Martínez C. and Klein R. (2001). The collagen receptor DDR2 regulates proliferation and its elimination leads to dwarfism. EMBO Rep. 2, 446-452.
40. Lai C. and Lemke G. (1994). Structure and expression of the Tyro 10 receptor tyrosine kinase. Oncogene. 9, 877-883.
41. Larjava H., Salo T., Haapasalmi K., Kramer R. and Heino J. (1993), Expression of integrins and basement membrane components by wound keratinocytes. J. Clin. Invest. 92, 1425-1435.
42. Laval S., Butler R., Shelling A., Hanby A., Poulsom R. and Ganesan T. (1994). Isolation and characterization of an epithelial-specific receptor tyrosine kinase from an ovarian cancer cell line. Cell Growth Differ. 5, 1173-1183.
43. Lelievre S., Weaver V., Nickerson J., Larabell C., Bhaumik A., Etersen O. and Bissell M. (1998). Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proc. Natl. Acad. Sci. USA 95, 14711-14716.
44. Lemeer S., Bluwstein A., Wu Z., Leberfinger J., Müller K., Kramer K. and Kuster B. (2012). Phosphotyrosine mediated protein interactions of the discoidin domain receptor 1. J. Proteomics 75, 3465-3477.
45. Lemmon M. and Schlessinger J. (2010). Cell signaling by receptor tyrosine kinases. Cell. 141, 1117-1134.
46. Lu K., Trcka D. and Bendeck M. (2011). Collagen stimulates discoidin domain receptor 1-mediated migration of smooth muscle cells through Src. Cardiovasc. Pathol. 20, 71-76.
47. Lucas T., Waisman A., Ranjan R., Roes J., Krieg T., Muller W., Roers A. and Eming S. (2010). Differential roles of macrophages in diverse phases of skin repair. J. Immunol. 184, 3964-3397.
48. Martin P. (1997). Wound healing-aiming for perfect skin regeneration. Science 276, 75-81.
49. Mirastschijskia U., Haaksmab C., James J., Tomasekb J. and Magnus S. (2004). Matrix metalloproteinase inhibitor GM 6001 attenuates keratinocyte migration, contraction and myofibroblast formation in skin wounds. Exp. Cell Res. 299, 465-475.
50. McClain S., Simon M., Jones E., Nandi A., Gailit J., Tonnesen M., Newman D. and Clark R. (1996). Mesenchymal cell activation is the rate-limiting step of granulation tissue induction. Am. J. Pathol. 149, 1257-1270.
51. Müller A., Meyer M. and Werner S. (2012). The roles of receptor tyrosine kinases and their ligands in the wound repair process. Semin. Cell Dev. Biol. 23, 963-970.
52. Okada A., Tomassetto C., Lutz Y., Bellocq J., Rio M. and Basset P. (1997). Expression of matrix metalloproteinases during rat skin wound healing: evidence that membrane type-1 matrix metalloproteinase is a stromal activator of pro-gelatinase A. J. Cell Biol. 137, 67-77.
53. Olaso E., Ikeda K., Eng F., Xu L., Wang L., Lin H. and Friedman S. (2001). DDR2 receptor promotes MMP-2-mediated proliferation and invasion by hepatic stellate cells. J. Clin. Invest. 108, 1369-1378.
54. Olaso E., Labrador J., Wang L., Ikeda K., Eng F., Klein R., Lovett D., Lin H. and Friedman S. (2002). Discoidin domain receptor 2 regulates fibroblast proliferation and migration through the extracellular matrix in association with transcriptional activation of matrix metalloproteinase-2. J Biol Chem. 277, 3606-3613.
55. Olaso E., Lin H., Wang L. and Friedman S. (2011). Impaired dermal wound healing in discoidin domain receptor 2-deficient mice associated with defective extracellular matrix remodeling Fibrogenesis Tissue Repair 4, 5.
56. Ongusaha P., Kim J., Fang L., Wong T., Yancopoulos G., Aaronson S. and Lee S. (2003). p53 induction and activation of DDR1 kinase counteract p53-mediated apoptosis and influence p53 regulation through a positive feedback loop. EMBO J. 22, 1289-1301.
57. Parks W.C. (2007). What is the α2β1 integrin doing in the epidermis? J. Invest. Dermatol. 127, 264-266.
58. Parsons J. and Parsons S. (1997). Src family protein tyrosine kinases: cooperating with growth factor and adhesion signaling pathways. Curr. Opin. Cell Biol. 9, 187-192
59. Payne S., Hendrix M. and Kirschmann D. (2007). Paradoxical roles for lysyl oxidases in cancer - a prospect. J Cell. Biochem. 101, 1338-1354.
60. Pelicci G., Lanfrancone L., Grignani F., McGlade J., Cavallo F., Forni G., Nicoletti I., Pawson T. and Pelicci P. (1992). A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70, 93-104.
61. Perez J., Shen X., Finkernagel S., Sciorra L., Jenkins N., Gilbert D., Copeland N. and Wong T. (1994). Identification and chromosomal mapping of a receptor tyrosine kinase with a putative phospholipid binding sequence in its ectodomain, Oncogene 9, 211-219.
62. Popova S.N., Lundgren-Akerlund E., Wiig H. and Gullberg D. (2007). Physiology and pathology of collagen receptors. Acta Physiol (Oxf). 190, 179-187.
63. Roarty K. and Serra R. (2007). Wnt5a is required for proper mammary gland development and TGF-β-mediated inhibition of ductal growth. Development 134, 3929-3939.
64. Rocnik E. Chan B. and Pickering J. (1998). Evidence for a role of collagen synthesis in arterial smooth muscle cell migration. J. Clin. Invest. 101, 1889-1898.
65. Rubel D., Kruegel J., Martin M., Leibnitz A., Girgert R., Miosge N., Eckes B., Müller G. 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. S0945-053X.
66. Ruiz P.A. and Jarai G. (2011). Collagen I induces discoidin domain receptor (DDR) 1 expression through DDR2 and a JAK2-ERK1/2- mediated mechanism in primary human lung fibroblasts. J. Biol. Chem. 286, 12912-12923.
67. Sanchez M., Tapley P., Saini S.S., Pulido B. and Barbacid M. (1994). Multiple tyrosine protein kinases in rat hippocampal neurons: isolation of Ptk-3, a receptor expressed in proliferative zones of the developing brain. Proc. Natl. Acad. Sci. USA 91, 1819-1823.
68. Shrivastava A., Radziejewski C., Campbell E., Kovac L., McGlynn M., Ryan T., Davis S., Goldfarb M., Glass D., Lemke G. and Yancopoulos G. (1997). An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell. 1, 25-34.
69. Singer A. and Clark R. (1999). Cutaneous wound healing. N. Engl. J. Med. 341, 738-746.
70. Staudinger L., Spano S., Lee W., Coelho N., Rajshankar D., Bendeck M., Moriarty T. and McCulloch C. (2013). Interactions between the discoidin domain receptor 1 and β1 integrin regulate attachment to collagen. Biol. Open 2, 1148-1159.
71. Suh H. and Han H. (2011). Collagen I regulates the self-renewal of mouse embryonic stem cells through α2β1 integrin- and DDR1- dependent Bmi-1. J. Cell. Phyisiol. 226, 3422-3432.
72. Sweeney S., Orgel J., Fertala A., McAuliffe J., Turner K., Di G., Chen S., Antipova O., Perumal S., Ala-Kokko L., Forlino A., Cabral W., Barnes A., Marini J. and San Antonio J. (2008). Candidate cell and matrix interaction domains on the collagen fibril, the predominant protein of vertebrates. J. Biol. Chem. 283, 21187-21197.
73. Takeichi M. (1995). Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627.
74. Théret N., Lehti K., Musso O. and Clément B. (1999). MMP2 activation by collagen I and Concanavalin A in cultured human hepatic stellate cells. Hepatology 2, 462-468.
75. Thomas S. and Brugge J. (1997). Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13, 513-609.
76. Ullrich A. and Schlessinger J. (1990). Signal transduction by receptors with tyrosine kinase activity. Cell 61, 203-212.
77. Valiathan R., Marco M., Leitinger B., Kleer C. and Fridman R. (2012). Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev. 31, 295-321.
78. Van der Geer P., Wiley S., Gish G.D. and Pawson T. (1996). The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions. Curr. Biol. 6, 1435-1444.
79. Vogel W. (1999) Discoidin domain receptors: structural relations and functional implications. FASEB J. 13, S77-82.
80. Vogel W., Gish G, Alves F. and Pawson T. (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell.1, 13-23.
81. Vogel W., Brakebusch C., Fässler R., Alves F., Ruggiero F. and Pawson T. (2000). Discoidin domain receptor 1 is activated independently of beta(1) integrin. J. Biol. Chem. 275, 5779-5784.
82. Wang F., Weaver V.M., Petersen O.W., Larabell C.A., Dedhar S., Briand P., Lupu R. and Bissell M.J. (1998). Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc. Natl. Acad. Sci. USA 95, 14821-14826.
83. Wang J., Lu H., Liu X., Deng Y., Sun T., Li F., Ji S., Nie S. and Yao L (2002). Functional analysis of discoidin domain receptor 2 in synovial fibroblasts in rheumatoid arthritis. J. Autoimmun. 19, 161-168.
84. Wang C., Su H. Hsu Y. Shen M. and Tang M. (2006). Discoidin domain receptor 1/SHP-2 signaling complex inhibits α2β1-integrin- mediated signal transducers and activators of transcription 1/3 activation and cell migration. Mol. Biol. Cell. 17, 2839-2852.
85. Wang C., Yeh Y. and Tang M. (2009). DDR1/E-cadherin complex regulates the activation of DDR1 and cell spreading. Am. J. Physiol. Cell Physiol. 297, C419-C429.
86. Wehrle-Haller B. and Imhof B.A. (2003). Integrin-dependent pathologies. J. Pathol. 200, 481-487.
87. Wells R.G. (2008). The role of matrix stiffness in regulating cell behavior. Hepatology 47, 1394-1400.
88. Werner S. and Grose R. (2003). Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83, 835-870.
89. Wong M., Gurtner M. and Longaker M. (2013). Wound healing: A paradigm for regeneration. Clin. Proc. 88, 1022-1031.
90. Xu L., Peng H., Wu D., Hu K., Mary B., Goldring M.B., Olsen B.R. and Li Y. (2005). Osteoarthritis in mice metalloproteinase 13 associated with receptor 2 induces expression of matrix activation of the discoidin domain. J. Biol. Chem. 280, 548-555.
91. Yang K., Kim J., Kim H., Park I., Kim I. and Yang B. (2005). Tyrosine 740 phosphorylation of discoidin domain receptor 2 by Src stimulates intramolecular autophosphorylation and Shc signaling complex formation. J. Biol. Chem. 280, 39058-39066.
92. Zerlin M., Julius M. and Goldfarb M. (1993). NEP: a novel receptor-like tyrosine kinase expressed in proliferating neuroepithelia. Oncogene 8, 2731-2739.