Discoidin domain receptor functions in physiological and pathological conditions

International Review of Cell and Molecular Biology

Volumn 310, Issue , 2014, Pages 39-87

  Leitinger, Birgit ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Cell signaling; Cell matrix interactions; Receptor activation; Receptor tyrosine kinase; Therapeutic target; Transmembrane collagen receptor

Indexed keywords

COLLAGEN BINDING PROTEIN; COLLAGEN RECEPTOR; DISCOIDIN; DISCOIDIN DOMAIN RECEPTOR 1; DISCOIDIN DOMAIN RECEPTOR 2; INTEGRIN; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; COLLAGEN; DDR1 PROTEIN, HUMAN; DISCOIDIN RECEPTOR; LECTIN RECEPTOR; LIGAND;

ARTHRITIS; ARTICLE; ATHEROSCLEROSIS; BINDING SITE; BONE GROWTH; DISEASE COURSE; ENDOCYTOSIS; FIBROSIS; HUMAN; KIDNEY DISEASE; LIGAND BINDING; NEOPLASM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RECEPTOR DOWN REGULATION; TRANSCRIPTION REGULATION; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

AMINO ACID SEQUENCE; ANIMALS; ARTHRITIS; ATHEROSCLEROSIS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; COLLAGEN; EXTRACELLULAR MATRIX; FIBROSIS; GENE EXPRESSION REGULATION; HUMANS; KIDNEY DISEASES; LIGANDS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

EID: 84898029568     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800180-6.00002-5     Document Type: Chapter

References (181)

1. Abbonante V., Gruppi C., Rubel D., Gross O., Moratti R., Balduini A. Discoidin domain receptor 1 protein is a novel modulator of megakaryocyte-collagen interactions. J. Biol. Chem. 2013, 288:16738-16746.
2. Abdulhussein R., McFadden C., Fuentes-Prior P., Vogel W.F. Exploring the collagen-binding site of the DDR1 tyrosine kinase receptor. J. Biol. Chem. 2004, 279:31462-31470.
3. Afonso P.V., McCann C.P., Kapnick S.M., Parent C.A. Discoidin domain receptor 2 regulates neutrophil chemotaxis in 3D collagen matrices. Blood 2013, 121:1644-1650.
4. Agarwal G., Kovac L., Radziejewski C., Samuelsson S.J. Binding of discoidin domain receptor 2 to collagen I: an atomic force microscopy investigation. Biochemistry 2002, 41:11091-11098.
5. Agarwal G., Mihai C., Iscru D.F. Interaction of discoidin domain receptor 1 with collagen type 1. J. Mol. Biol. 2007, 367:443-455.
6. Ahmad P.J., Trcka D., Xue S., Franco C., Speer M.Y., Giachelli C.M., Bendeck M.P. Discoidin domain receptor-1 deficiency attenuates atherosclerotic calcification and smooth muscle cell-mediated mineralization. Am. J. Pathol. 2009, 175:2686-2696.
7. Ali B.R., Xu H., Akawi N.A., John A., Karuvantevida N.S., Langer R., Al-Gazali L., Leitinger B. Trafficking defects and loss of ligand binding are the underlying causes of all reported DDR2 missense mutations found in SMED-SL patients. Hum. Mol. Genet. 2010, 19:2239-2250.
8. Alves F., Vogel W., Mossie K., Millauer B., Hofler H., Ullrich A. Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 1995, 10:609-618.
9. Alves F., Saupe S., Ledwon M., Schaub F., Hiddemann W., Vogel W.F. Identification of two novel, kinase-deficient variants of discoidin domain receptor 1: differential expression in human colon cancer cell lines. Faseb J. 2001, 15:1321-1323.
10. Aronson R.B., Sinex F.M., Franzblau C., Van Slyke D.D. The oxidation of protein-bound hydroxylysine by periodate. J. Biol. Chem. 1967, 242:809-812.
11. Arribas J., Borroto A. Protein ectodomain shedding. Chem. Rev. 2002, 102:4627-4638.
12. Avivi-Green C., Singal M., Vogel W.F. Discoidin domain receptor 1-deficient mice are resistant to bleomycin-induced lung fibrosis. Am. J. Respir. Crit. Care Med. 2006, 174:420-427.
13. Bargal R., Cormier-Daire V., Ben-Neriah Z., Le Merrer M., Sosna J., Melki J., Zangen D.H., Smithson S.F., Borochowitz Z., Belostotsky R., Raas-Rothschild A. Mutations in DDR2 gene cause SMED with short limbs and abnormal calcifications. Am. J. Hum. Genet. 2009, 84:80-84.
14. Barker K.T., Martindale J.E., Mitchell P.J., Kamalati T., Page M.J., Phippard D.J., Dale T.C., Gusterson B.A., Crompton M.R. Expression patterns of the novel receptor-like tyrosine kinase, DDR, in human breast tumours. Oncogene 1995, 10:569-575.
15. Baumgartner S., Hofmann K., Chiquet-Ehrismann R., Bucher P. The discoidin domain family revisited: new members from prokaryotes and a homology-based fold prediction. Protein Sci. 1998, 7:1626-1631.
16. Bhadriraju K., Chung K.H., Spurlin T.A., Haynes R.J., Elliott J.T., Plant A.L. 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 2009, 30:6687-6694.
17. Bonifacino J.S., Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 2003, 72:395-447.
18. Borochowitz Z., Langer L.O., Gruber H.E., Lachman R., Katznelson M.B., Rimoin D.L. Spondylo-meta-epiphyseal dysplasia (SMED), short limb-hand type: a congenital familial skeletal dysplasia with distinctive features and histopathology. Am. J. Med. Genet. 1993, 45:320-326.
19. Cader F.Z., Vockerodt M., Bose S., Nagy E., Brundler M.A., Kearns P., Murray P.G. The EBV oncogene LMP1 protects lymphoma cells from cell death through the collagen-mediated activation of DDR1. Blood 2013, 122:4237-4245.
20. Carafoli F., Hohenester E. Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim. Biophys. Acta 2013, 1834:2187-2194.
21. Carafoli F., Bihan D., Stathopoulos S., Konitsiotis A.D., Kvansakul M., Farndale R.W., Leitinger B., Hohenester E. Crystallographic insight into collagen recognition by discoidin domain receptor 2. Structure 2009, 17:1573-1581.
22. Carafoli F., Mayer M.C., Shiraishi K., Pecheva M.A., Chan L.Y., Nan R., Leitinger B., Hohenester E. Structure of the discoidin domain receptor 1 extracellular region bound to an inhibitory Fab fragment reveals features important for signaling. Structure 2012, 20:688-697.
23. Chen J., Diacovo T.G., Grenache D.G., Santoro S.A., Zutter M.M. The a2 integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am. J. Pathol. 2002, 161:337-344.
24. Chen S.C., Wang B.W., Wang D.L., Shyu K.G. Hypoxia induces discoidin domain receptor-2 expression via the p38 pathway in vascular smooth muscle cells to increase their migration. Biochem. Biophys. Res. Commun. 2008, 374:662-667.
25. Chetoui N., El Azreq M.A., Boisvert M., Bergeron M.E., Aoudjit F. Discoidin domain receptor 1 expression in activated T cells is regulated by the ERK MAP kinase signaling pathway. J. Cell. Biochem. 2011, 112:3666-3674.
26. Clementz A.G., Mutolo M.J., Leir S.H., Morris K.J., Kucybala K., Harris H., Harris A. Collagen XV inhibits epithelial to mesenchymal transition in pancreatic adenocarcinoma cells. PLoS One 2013, 8:e72250.
27. Comoglio P.M., Boccaccio C., Trusolino L. Interactions between growth factor receptors and adhesion molecules: breaking the rules. Curr. Opin. Cell Biol. 2003, 15:565-571.
28. Curat C.A., Vogel W.F. Discoidin domain receptor 1 controls growth and adhesion of mesangial cells. J. Am. Soc. Nephrol. 2002, 13:2648-2656.
29. Curat C.A., Eck M., Dervillez X., Vogel W.F. Mapping of epitopes in discoidin domain receptor 1 critical for collagen binding. J. Biol. Chem. 2001, 276:45952-45958.
30. Das S., Ongusaha P.P., Yang Y.S., Park J.M., Aaronson S.A., Lee S.W. Discoidin domain receptor 1 receptor tyrosine kinase induces cyclooxygenase-2 and promotes chemoresistance through nuclear factor-{kappa}B pathway activation. Cancer Res. 2006, 66:8123-8130.
31. Day E., Waters B., Spiegel K., Alnadaf T., Manley P.W., Buchdunger E., Walker C., Jarai G. Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib and dasatinib. Eur. J. Pharmacol. 2008, 599:44-53.
32. Dejmek J., Dib K., Jonsson M., Andersson T. Wnt-5a and G-protein signaling are required for collagen-induced DDR1 receptor activation and normal mammary cell adhesion. Int. J. Cancer 2003, 103:344-351.
33. Di Marco E., Cutuli N., Guerra L., Cancedda R., De Luca M. 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. 1993, 268:24290-24295.
34. Edelhoff S., Sweetser D.A., Disteche C.M. Mapping of the NEP receptor tyrosine kinase gene to human chromosome 6p21.3 and mouse chromosome 17C. Genomics 1995, 25:309-311.
35. Faraci-Orf E., McFadden C., Vogel W.F. DDR1 signaling is essential to sustain Stat5 function during lactogenesis. J. Cell. Biochem. 2006, 97:109-121.
36. Farndale R.W., Lisman T., Bihan D., Hamaia S., Smerling C.S., Pugh N., Konitsiotis A., Leitinger B., de Groot P.G., Jarvis G.E., Raynal N. Cell-collagen interactions: the use of peptide Toolkits to investigate collagen-receptor interactions. Biochem. Soc. Trans. 2008, 36:241-250.
37. Favreau A.J., Cross E.L., Sathyanarayana P. miR-199b-5p directly targets PODXL and DDR1 and decreased levels of miR-199b-5p correlate with elevated expressions of PODXL and DDR1 in acute myeloid leukemia. Am. J. Hematol. 2012, 87:442-446.
38. Ferri N., Carragher N.O., Raines E.W. Role of discoidin domain receptors 1 and 2 in human smooth muscle cell-mediated collagen remodeling: potential implications in atherosclerosis and lymphangioleiomyomatosis. Am. J. Pathol. 2004, 164:1575-1585.
39. Finger C., Escher C., Schneider D. The single transmembrane domains of human receptor tyrosine kinases encode self-interactions. Sci. Signal. 2009, 2:ra56.
40. Flamant M., Placier S., Rodenas A., Curat C.A., Vogel W.F., Chatziantoniou C., Dussaule J.C. Discoidin domain receptor 1 null mice are protected against hypertension-induced renal disease. J. Am. Soc. Nephrol. 2006, 17:3374-3381.
41. Flynn L.A., Blissett A.R., Calomeni E.P., Agarwal G. Inhibition of collagen fibrillogenesis by cells expressing soluble extracellular domains of DDR1 and DDR2. J. Mol. Biol. 2010, 395:533-543.
42. Ford C.E., Lau S.K., Zhu C.Q., Andersson T., Tsao M.S., Vogel W.F. Expression and mutation analysis of the discoidin domain receptors 1 and 2 in non-small cell lung carcinoma. Br. J. Cancer 2007, 96:808-814.
43. Franco C., Hou G., Ahmad P.J., Fu E.Y., Koh L., Vogel W.F., Bendeck M.P. Discoidin domain receptor 1 (ddr1) deletion decreases atherosclerosis by accelerating matrix accumulation and reducing inflammation in low-density lipoprotein receptor-deficient mice. Circ. Res. 2008, 102:1202-1211.
44. Franco C., Britto K., Wong E., Hou G., Zhu S.N., Chen M., Cybulsky M.I., Bendeck M.P. Discoidin domain receptor 1 on bone marrow-derived cells promotes macrophage accumulation during atherogenesis. Circ. Res. 2009, 105:1141-1148.
45. Franco C., Ahmad P.J., Hou G., Wong E., Bendeck M.P. Increased cell and matrix accumulation during atherogenesis in mice with vessel wall-specific deletion of discoidin domain receptor 1. Circ. Res. 2010, 106:1775-1783.
46. Friedl P., Weigelin B. Interstitial leukocyte migration and immune function. Nat. Immunol. 2008, 9:960-969.
47. Fu H.L., Sohail A., Valiathan R.R., Wasinski B.D., Kumarasiri M., Mahasenan K.V., Bernardo M.M., Tokmina-Roszyk D., Fields G.B., Mobashery S., Fridman R. Shedding of discoidin domain receptor 1 by membrane-type matrix metalloproteinases. J. Biol. Chem. 2013, 288:12114-12129.
48. Gao M., Duan L., Luo J., Zhang L., Lu X., Zhang Y., Zhang Z., Tu Z., Xu Y., Ren X., Ding K. Discovery and optimization of 3-(2-(Pyrazolo[1,5-a]pyrimidin-6-yl)ethynyl)benzamides as novel selective and orally bioavailable discoidin domain receptor 1 (DDR1) inhibitors. J. Med. Chem. 2013, 56:3281-3295.
49. Ghosh S., Ashcraft K., Jahid M.J., April C., Ghajar C.M., Ruan J., Wang H., Foster M., Hughes D.C., Ramirez A.G., Huang T., Fan J.B., Hu Y., Li R. Regulation of adipose oestrogen output by mechanical stress. Nat. Commun. 2013, 4:1821.
50. Girgert R., Martin M., Kruegel J., Miosge N., Temme J., Eckes B., Muller G.A., Gross O. Integrin alpha2-deficient mice provide insights into specific functions of collagen receptors in the kidney. Fibrogenesis Tissue Repair 2010, 3:19.
51. Gross O., Beirowski B., Harvey S.J., McFadden C., Chen D., Tam S., Thorner P.S., Smyth N., Addicks K., Bloch W., Ninomiya Y., Sado Y., Weber M., Vogel W.F. DDR1-deficient mice show localized subepithelial GBM thickening with focal loss of slit diaphragms and proteinuria. Kidney Int. 2004, 66:102-111.
52. Gross O., Girgert R., Beirowski B., Kretzler M., Kang H.G., Kruegel J., Miosge N., Busse A.C., Segerer S., Vogel W.F., Muller G.A., Weber M. Loss of collagen-receptor DDR1 delays renal fibrosis in hereditary type IV collagen disease. Matrix Biol. 2010, 29:346-356.
53. Gschwind A., Fischer O.M., Ullrich A. The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat. Rev. Cancer 2004, 4:361-370.
54. Guerrot D., Kerroch M., Placier S., Vandermeersch S., Trivin C., Mael-Ainin M., Chatziantoniou C., Dussaule J.C. Discoidin domain receptor 1 is a major mediator of inflammation and fibrosis in obstructive nephropathy. Am. J. Pathol. 2011, 179:83-91.
55. Hachehouche L.N., Chetoui N., Aoudjit F. Implication of discoidin domain receptor 1 in T cell migration in three-dimensional collagen. Mol. Immunol. 2010, 47:1866-1869.
56. Hahn W.H., Suh J.S., Cho B.S., Kim S.D. Linkage and association study of discoidin domain receptor 1 as a novel susceptibility gene for childhood IgA nephropathy. Int. J. Mol. Med. 2010, 25:785-791.
57. Hammerman P.S., Sos M.L., Ramos A.H., Xu C., Dutt A., Zhou W., Brace L.E., Woods B.A., Lin W., Zhang J., Deng X., Lim S.M., Heynck S., Peifer M., Simard J.R., Lawrence M.S., Onofrio R.C., Salvesen H.B., Seidel D., Zander T., Heuckmann J.M., Soltermann A., Moch H., Koker M., Leenders F., Gabler F., Querings S., Ansen S., Brambilla E., Brambilla C., Lorimier P., Brustugun O.T., Helland A., Petersen I., Clement J.H., Groen H., Timens W., Sietsma H., Stoelben E., Wolf J., Beer D.G., Tsao M.S., Hanna M., Hatton C., Eck M.J., Janne P.A., Johnson B.E., Winckler W., Greulich H., Bass A.J., Cho J., Rauh D., Gray N.S., Wong K.K., Haura E.B., Thomas R.K., Meyerson M. Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer. Cancer Discov. 2011, 1:78-89.
58. Hidalgo-Carcedo C., Hooper S., Chaudhry S.I., Williamson P., Harrington K., Leitinger B., Sahai E. Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat. Cell Biol. 2011, 13:49-58.
59. Higashiyama S., Nanba D., Nakayama H., Inoue H., Fukuda S. Ectodomain shedding and remnant peptide signalling of EGFRs and their ligands. J. Biochem. 2011, 150:15-22.
60. Hilton H.N., Stanford P.M., Harris J., Oakes S.R., Kaplan W., Daly R.J., Ormandy C.J. KIBRA interacts with discoidin domain receptor 1 to modulate collagen-induced signalling. Biochim. Biophys. Acta 2008, 1783:383-393.
61. Holt D.W., Henderson M.L., Stockdale C.E., Farrell J.T., Kooyman D.L., Bridgewater L.C., Seegmiller R.E. Osteoarthritis-like changes in the heterozygous sedc mouse associated with the HtrA1-Ddr2-Mmp-13 degradative pathway: a new model of osteoarthritis. Osteoarthr. Cartil. 2012, 20:430-439.
62. Hou G., Vogel W., Bendeck M.P. The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J. Clin. Invest. 2001, 107:727-735.
63. Hou G., Vogel W.F., Bendeck M.P. Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ. Res. 2002, 90:1147-1149.
64. Hou G., Wang D., Bendeck M.P. Deletion of discoidin domain receptor 2 does not affect smooth muscle cell adhesion, migration, or proliferation in response to type I collagen. Cardiovasc. Pathol. 2012, 21:214-218.
65. Hu K., Xu L., Cao L., Flahiff C.M., Brussiau J., Ho K., Setton L.A., Youn I., Guilak F., Olsen B.R., Li Y. Pathogenesis of osteoarthritis-like changes in the joints of mice deficient in type IX collagen. Arthritis Rheum. 2006, 54:2891-2900.
66. Hu Y., Potts M.B., Colosimo D., Herrera-Herrera M.L., Legako A.G., Yousufuddin M., White M.A., Macmillan J.B. Discoipyrroles A-D: isolation, structure determination, and synthesis of potent migration inhibitors from Bacillus hunanensis. J. Am. Chem. Soc. 2013, 135:13387-13392.
67. Hubbard S.R. Juxtamembrane autoinhibition in receptor tyrosine kinases. Nat. Rev. Mol. Cell Biol. 2004, 5:464-471.
68. Hynes R. Integrins. Bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
69. Ichikawa O., Osawa M., Nishida N., Goshima N., Nomura N., Shimada I. Structural basis of the collagen-binding mode of discoidin domain receptor 2. Embo J. 2007, 26:4168-4176.
70. 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., Lin H.C. Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen. J. Biol. Chem. 2002, 277:19206-19212.
71. Iwai L.K., Chang F., Huang P.H. Phosphoproteomic analysis identifies insulin enhancement of discoidin domain receptor 2 phosphorylation. Cell Adh. Migr. 2013, 7:161-164.
72. Iwai L.K., Payne L.S., Luczynski M.T., Chang F., Xu H., Clinton R.W., Paul A., Esposito E.A., Gridley S., Leitinger B., Naegle K.M., Huang P.H. Phosphoproteomics of collagen receptor networks reveals SHP-2 phosphorylation downstream of wild-type DDR2 and its lung cancer mutants. Biochem. J. 2013, 454:501-513.
73. Jian Z.X., Sun J., Chen W., Jin H.S., Zheng J.H., Wu Y.L. Involvement of discoidin domain 1 receptor in recurrence of hepatocellular carcinoma by genome-wide analysis. Med. Oncol. 2012, 29:3077-3082.
74. Johnson J.D., Edman J.C., Rutter W.J. A receptor tyrosine kinase found in breast carcinoma cells has an extracellular discoidin I-like domain. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:5677-5681.
75. Jonsson M., Andersson T. Repression of Wnt-5a impairs DDR1 phosphorylation and modifies adhesion and migration of mammary cells. J. Cell Sci. 2001, 114:2043-2053.
76. Jura N., Endres N.F., Engel K., Deindl S., Das R., Lamers M.H., Wemmer D.E., Zhang X., Kuriyan J. Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 2009, 137:1293-1307.
77. Kadler K.E., Baldock C., Bella J., Boot-Handford R.P. Collagens at a glance. J. Cell Sci. 2007, 120:1955-1958.
78. Kamohara H., Yamashiro S., Galligan C., Yoshimura T. Discoidin domain receptor 1 isoform-a (DDR1a) promotes migration of leukocytes in three-dimensional collagen lattices. Faseb J. 2001, 15:2724-2726.
79. Kano K., Marin de Evsikova C., Young J., Wnek C., Maddatu T.P., Nishina P.M., Naggert J.K. A novel dwarfism with gonadal dysfunction due to loss-of-function allele of the collagen receptor gene, Ddr2, in the mouse. Mol. Endocrinol. 2008, 22:1866-1880.
80. Karn T., Holtrich U., Brauninger A., Bohme B., Wolf G., Rubsamen-Waigmann H., Strebhardt K. Structure, expression and chromosomal mapping of TKT from man and mouse: a new subclass of receptor tyrosine kinases with a factor VIII-like domain. Oncogene 1993, 8:3433-3440.
81. Kawai I., Matsumura H., Fujii W., Naito K., Kusakabe K., Kiso Y., Kano K. Discoidin domain receptor 2 (DDR2) regulates body size and fat metabolism in mice. Transgenic Res. 2014, 23:165-175.
82. Kerroch M., Guerrot D., Vandermeersch S., Placier S., Mesnard L., Jouanneau C., Rondeau E., Ronco P., Boffa J.J., Chatziantoniou C., Dussaule J.C. Genetic inhibition of discoidin domain receptor 1 protects mice against crescentic glomerulonephritis. Faseb J. 2012, 26:4079-4091.
83. Khosravi R., Sodek K.L., Faibish M., Trackman P.C. Collagen advanced glycation inhibits its discoidin domain receptor 2 (DDR2)-mediated induction of lysyl oxidase in osteoblasts. Bone 2014, 58:33-41.
84. Kiedzierska A., Smietana K., Czepczynska H., Otlewski J. Structural similarities and functional diversity of eukaryotic discoidin-like domains. Biochim. Biophys. Acta 2007, 1774:1069-1078.
85. Kim H.G., Hwang S.Y., Aaronson S.A., Mandinova A., Lee S.W. DDR1 receptor tyrosine kinase promotes prosurvival pathway through Notch1 activation. J. Biol. Chem. 2011, 286:17672-17681.
86. Kim H.G., Tan L., Weisberg E.L., Liu F., Canning P., Choi H.G., Ezell S.A., Wu H., Zhao Z., Wang J., Mandinova A., Griffin J.D., Bullock A.N., Liu Q., Lee S.W., Gray N.S. Discovery of a potent and selective DDR1 receptor tyrosine kinase inhibitor. ACS Chem. Biol. 2013, 8:2145-2150.
87. Konitsiotis A.D., Raynal N., Bihan D., Hohenester E., Farndale R.W., Leitinger B. Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen. J. Biol. Chem. 2008, 283:6861-6868.
88. Koo D.H., McFadden C., Huang Y., Abdulhussein R., Friese-Hamim M., Vogel W.F. Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett. 2006, 580:15-22.
89. Labrador J.P., Azcoitia V., Tuckermann J., Lin C., Olaso E., Manes S., Bruckner K., Goergen J.L., Lemke G., Yancopoulos G., Angel P., Martinez A.C., Klein R. The collagen receptor DDR2 regulates proliferation and its elimination leads to dwarfism. EMBO Rep. 2001, 2:446-452.
90. Lai C., Lemke G. Structure and expression of the Tyro 10 receptor tyrosine kinase. Oncogene 1994, 9:877-883.
91. Laval S., Butler R., Shelling A.N., Hanby A.M., Poulsom R., Ganesan T.S. Isolation and characterization of an epithelial-specific receptor tyrosine kinase from an ovarian cancer cell line. Cell Growth Differ. 1994, 5:1173-1183.
92. Leitinger B. Molecular analysis of collagen binding by the human discoidin domain receptors, DDR1 and DDR2. Identification of collagen binding sites in DDR2. J. Biol. Chem. 2003, 278:16761-16769.
93. Leitinger B. Transmembrane collagen receptors. Annu. Rev. Cell Dev. Biol. 2011, 27:265-290.
94. Leitinger B., Kwan A.P. The discoidin domain receptor DDR2 is a receptor for type X collagen. Matrix Biol. 2006, 25:355-364.
95. Leitinger B., Steplewski A., Fertala A. The D2 period of collagen II contains a specific binding site for the human discoidin domain receptor, DDR2. J. Mol. Biol. 2004, 344:993-1003.
96. Lemeer S., Bluwstein A., Wu Z., Leberfinger J., Muller K., Kramer K., Kuster B. Phosphotyrosine mediated protein interactions of the discoidin domain receptor 1. J. Proteomics 2012, 75:3465-3477.
97. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
98. L'Hote C.G., Thomas P.H., Ganesan T.S. Functional analysis of discoidin domain receptor 1: effect of adhesion on DDR1 phosphorylation. Faseb J. 2002, 16:234-236.
99. Lin K.L., Chou C.H., Hsieh S.C., Hwa S.Y., Lee M.T., Wang F.F. Transcriptional upregulation of DDR2 by ATF4 facilitates osteoblastic differentiation through p38 MAPK-mediated Runx2 activation. J. Bone Miner. Res. 2010, 25:2489-2503.
100. Lu K.K., Trcka D., Bendeck M.P. Collagen stimulates discoidin domain receptor 1-mediated migration of smooth muscle cells through Src. Cardiovasc. Pathol. 2011, 20:71-76.
101. Luo B.H., Carman C.V., Springer T.A. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 2007, 25:619-647.
102. Luo Z., Liu H., Sun X., Guo R., Cui R., Ma X., Yan M. RNA interference against discoidin domain receptor 2 ameliorates alcoholic liver disease in rats. PLoS One 2013, 8:e55860.
103. Martinez-Marignac V.L., Rodrigue A., Davidson D., Couillard M., Al-Moustafa A.E., Abramovitz M., Foulkes W.D., Masson J.Y., Aloyz R. The effect of a DNA repair gene on cellular invasiveness: XRCC3 over-expression in breast cancer cells. PLoS One 2011, 6:e16394.
104. Meyer zum Gottesberge A.M., Gross O., Becker-Lendzian U., Massing T., Vogel W.F. Inner ear defects and hearing loss in mice lacking the collagen receptor DDR1. Lab. Invest. 2008, 88:27-37.
105. Miao L., Zhu S., Wang Y., Li Y., Ding J., Dai J., Cai H., Zhang D., Song Y. Discoidin domain receptor 1 is associated with poor prognosis of non-small cell lung cancer and promotes cell invasion via epithelial-to-mesenchymal transition. Med. Oncol. 2013, 30:626.
106. Mihai C., Chotani M., Elton T.S., Agarwal G. Mapping of DDR1 distribution and oligomerization on the cell surface by FRET microscopy. J. Mol. Biol. 2009, 385:432-445.
107. Murphy J.E., Padilla B.E., Hasdemir B., Cottrell G.S., Bunnett N.W. Endosomes: a legitimate platform for the signaling train. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17615-17622.
108. Natarajan K., Berk B.C. Crosstalk coregulation mechanisms of G protein-coupled receptors and receptor tyrosine kinases. Methods Mol. Biol. 2006, 332:51-77.
109. Neuhaus B., Buhren S., Bock B., Alves F., Vogel W.F., Kiefer F. Migration inhibition of mammary epithelial cells by Syk is blocked in the presence of DDR1 receptors. Cell. Mol. Life Sci. 2011, 68:3757-3770.
110. Noordeen N.A., Carafoli F., Hohenester E., Horton M.A., Leitinger B. A transmembrane leucine zipper is required for activation of the dimeric receptor tyrosine kinase DDR1. J. Biol. Chem. 2006, 281:22744-22751.
111. Olaso E., Ikeda K., Eng F.J., Xu L., Wang L.H., Lin H.C., Friedman S.L. DDR2 receptor promotes MMP-2-mediated proliferation and invasion by hepatic stellate cells. J. Clin. Invest. 2001, 108:1369-1378.
112. Olaso E., Labrador J.P., Wang L., Ikeda K., Eng F.J., Klein R., Lovett D.H., Lin H.C., Friedman S.L. 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. 2002, 277:3606-3613.
113. Olaso E., Arteta B., Benedicto A., Crende O., Friedman S.L. Loss of discoidin domain receptor 2 promotes hepatic fibrosis after chronic carbon tetrachloride through altered paracrine interactions between hepatic stellate cells and liver-associated macrophages. Am. J. Pathol. 2011, 179:2894-2904.
114. Olaso E., Lin H.C., Wang L.H., Friedman S.L. Impaired dermal wound healing in discoidin domain receptor 2-deficient mice associated with defective extracellular matrix remodeling. Fibrogenesis Tissue Repair 2011, 4:5.
115. Ongusaha P.P., Kim J.I., Fang L., Wong T.W., Yancopoulos G.D., Aaronson S.A., Lee S.W. p53 induction and activation of DDR1 kinase counteract p53-mediated apoptosis and influence p53 regulation through a positive feedback loop. Embo J. 2003, 22:1289-1301.
116. Page-McCaw A., Ewald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8:221-233.
117. Perez J.L., Shen X., Finkernagel S., Sciorra L., Jenkins N.A., Gilbert D.J., Copeland N.G., Wong T.W. Identification and chromosomal mapping of a receptor tyrosine kinase with a putative phospholipid binding sequence in its ectodomain. Oncogene 1994, 9:211-219.
118. Perez J.L., Jing S.Q., Wong T.W. Identification of two isoforms of the Cak receptor kinase that are coexpressed in breast tumor cell lines. Oncogene 1996, 12:1469-1477.
119. Phan T.N., Wong E.L., Sun X., Kim G., Jung S.H., Yoon C.N., Yang B.S. Low stability and a conserved N-glycosylation site are associated with regulation of the discoidin domain receptor family by glucose via post-translational N-glycosylation. Biosci. Biotechnol. Biochem. 2013, 77:1907-1916.
120. Playford M.P., Butler R.J., Wang X.C., Katso R.M., Cooke I.E., Ganesan T.S. The genomic structure of discoidin receptor tyrosine kinase. Genome Res. 1996, 6:620-627.
121. Poudel B., Ki H.H., Lee Y.M., Kim D.K. Induction of IL-12 production by the activation of discoidin domain receptor 2 via NF-kappaB and JNK pathway. Biochem. Biophys. Res. Commun. 2013, 434:584-588.
122. Pulsatelli L., Addimanda O., Brusi V., Pavloska B., Meliconi R. New findings in osteoarthritis pathogenesis: therapeutic implications. Ther. Adv. Chronic Dis. 2013, 4:23-43.
123. Ram R., Lorente G., Nikolich K., Urfer R., Foehr E., Nagavarapu U. Discoidin domain receptor-1a (DDR1a) promotes glioma cell invasion and adhesion in association with matrix metalloproteinase-2. J. Neurooncol 2006, 76:239-248.
124. Ren T., Zhang J., Liu X., Yao L. Increased expression of discoidin domain receptor 2 (DDR2): a novel independent prognostic marker of worse outcome in breast cancer patients. Med. Oncol. 2013, 30:397.
125. Ricard-Blum S. The collagen family. Cold Spring Harb. Perspect. Biol. 2011, 3:a004978.
126. Rikova K., Guo A., Zeng Q., Possemato A., Yu J., Haack H., Nardone J., Lee K., Reeves C., Li Y., Hu Y., Tan Z., Stokes M., Sullivan L., Mitchell J., Wetzel R., Macneill J., Ren J.M., Yuan J., Bakalarski C.E., Villen J., Kornhauser J.M., Smith B., Li D., Zhou X., Gygi S.P., Gu T.L., Polakiewicz R.D., Rush J., Comb M.J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131:1190-1203.
127. Rix U., Hantschel O., Durnberger G., Remsing Rix L.L., Planyavsky M., Fernbach N.V., Kaupe I., Bennett K.L., Valent P., Colinge J., Kocher T., Superti-Furga G. Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood 2007, 110:4055-4063.
128. Roarty K., Serra R. Wnt5a is required for proper mammary gland development and TGF-beta-mediated inhibition of ductal growth. Development 2007, 134:3929-3939.
129. Roberts M.E., Magowan L., Hall I.P., Johnson S.R. Discoidin domain receptor 1 regulates bronchial epithelial repair and matrix metalloproteinase production. Eur. Respir. J. 2011, 37:1482-1493.
130. Roig B., Moyano S., Martorell L., Costas J., Vilella E. The discoidin domain receptor 1 gene has a functional A2RE sequence. J. Neurochem. 2012, 120:408-418.
131. Ruiz P.A., Jarai G. 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. 2011, 286:12912-12923.
132. Russ W.P., Engelman D.M. TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:863-868.
133. Sakuma S., Saya H., Tada M., Nakao M., Fujiwara T., Roth J.A., Sawamura Y., Shinohe Y., Abe H. Receptor protein tyrosine kinase DDR is up-regulated by p53 protein. FEBS Lett. 1996, 398:165-169.
134. Sanchez M.P., Tapley P., Saini S.S., He B., Pulido D., Barbacid M. 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. U. S. A. 1994, 91:1819-1823.
135. Sekiya Y., Ogawa T., Yoshizato K., Ikeda K., Kawada N. Suppression of hepatic stellate cell activation by microRNA-29b. Biochem. Biophys. Res. Commun. 2011, 412:74-79.
136. Shen Q., Cicinnati V.R., Zhang X., Iacob S., Weber F., Sotiropoulos G.C., Radtke A., Lu M., Paul A., Gerken G., Beckebaum S. Role of microRNA-199a-5p and discoidin domain receptor 1 in human hepatocellular carcinoma invasion. Mol. Cancer 2010, 9:227.
137. Shintani Y., Fukumoto Y., Chaika N., Svoboda R., Wheelock M.J., Johnson K.R. Collagen I-mediated up-regulation of N-cadherin requires cooperative signals from integrins and discoidin domain receptor 1. J. Cell Biol. 2008, 180:1277-1289.
138. Shrivastava A., Radziejewski C., Campbell E., Kovac L., McGlynn M., Ryan T.E., Davis S., Goldfarb M.P., Glass D.J., Lemke G., Yancopoulos G.D. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell 1997, 1:25-34.
139. Shyu K.G., Wang B.W., Kuan P., Chang H. RNA interference for discoidin domain receptor 2 attenuates neointimal formation in balloon injured rat carotid artery. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1447-1453.
140. Shyu K.G., Wang B.W., Chang H. Hyperbaric oxygen activates discoidin domain receptor 2 via tumour necrosis factor-alpha and the p38 MAPK pathway to increase vascular smooth muscle cell migration through matrix metalloproteinase 2. Clin. Sci. (Lond.) 2009, 116:575-583.
141. Siddiqui K., Kim G.W., Lee D.H., Shin H.R., Yang E.G., Lee N.T., Yang B.S. Actinomycin D identified as an inhibitor of discoidin domain receptor 2 interaction with collagen through an insect cell based screening of a drug compound library. Biol. Pharm. Bull. 2009, 32:136-141.
142. Slack B.E., Siniaia M.S., Blusztajn J.K. Collagen type I selectively activates ectodomain shedding of the discoidin domain receptor 1: involvement of Src tyrosine kinase. J. Cell. Biochem. 2006, 98:672-684.
143. Soung Y.H., Clifford J.L., Chung J. Crosstalk between integrin and receptor tyrosine kinase signaling in breast carcinoma progression. BMB Rep. 2010, 43:311-318.
144. Staudinger L.A., Spano S.J., Lee W., Coelho N., Rajshankar D., Bendeck M.P., Moriarty T., McCulloch C.A. Interactions between the discoidin domain receptor 1 and b1 integrin regulate attachment to collagen. Biol. Open 2013, 2:1148-1159.
145. Su J., Yu J., Ren T., Zhang W., Zhang Y., Liu X., Sun T., Lu H., Miyazawa K., Yao L. Discoidin domain receptor 2 is associated with the increased expression of matrix metalloproteinase-13 in synovial fibroblasts of rheumatoid arthritis. Mol. Cell. Biochem. 2009, 330:141-152.
146. Suh H.N., Han H.J. Collagen I regulates the self-renewal of mouse embryonic stem cells through alpha2beta1 integrin- and DDR1-dependent Bmi-1. J. Cell. Physiol. 2011, 226:3422-3432.
147. Sunk I.G., Bobacz K., Hofstaetter J.G., Amoyo L., Soleiman A., Smolen J., Xu L., Li Y. Increased expression of discoidin domain receptor 2 is linked to the degree of cartilage damage in human knee joints: a potential role in osteoarthritis pathogenesis. Arthritis Rheum. 2007, 56:3685-3692.
148. Taube J.H., Herschkowitz J.I., Komurov K., Zhou A.Y., Gupta S., Yang J., Hartwell K., Onder T.T., Gupta P.B., Evans K.W., Hollier B.G., Ram P.T., Lander E.S., Rosen J.M., Weinberg R.A., Mani S.A. Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15449-15454.
149. Torban E., Goodyer P. The kidney and ear: emerging parallel functions. Annu. Rev. Med. 2009, 60:339-353.
150. Unsoeld T., Park J.O., Hutter H. Discoidin domain receptors guide axons along longitudinal tracts in C. elegans. Dev. Biol. 2013, 374:142-152.
151. Valencia K., Ormazabal C., Zandueta C., Luis-Ravelo D., Anton I., Pajares M.J., Agorreta J., Montuenga L.M., Martinez-Canarias S., Leitinger B., Lecanda F. Inhibition of collagen receptor discoidin domain receptor-1 (DDR1) reduces cell survival, homing, and colonization in lung cancer bone metastasis. Clin. Cancer Res. 2012, 18:969-980.
152. Valiathan R.R., Marco M., Leitinger B., Kleer C.G., Fridman R. Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev. 2012, 31:295-321.
153. van Kilsdonk J.W., van Kempen L.C., van Muijen G.N., Ruiter D.J., Swart G.W. Soluble adhesion molecules in human cancers: sources and fates. Eur. J. Cell Biol. 2010, 89:415-427.
154. Vogel W.F. Ligand-induced shedding of discoidin domain receptor 1. FEBS Lett. 2002, 514:175-180.
155. Vogel W., Gish G.D., Alves F., Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1997, 1:13-23.
156. Vogel W., Brakebusch C., Fassler R., Alves F., Ruggiero F., Pawson T. Discoidin domain receptor 1 is activated independently of b1 integrin. J. Biol. Chem. 2000, 275:5779-5784.
157. Vogel W.F., Aszodi A., Alves F., Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol. Cell. Biol. 2001, 21:2906-2917.
158. von Zastrow M., Sorkin A. Signaling on the endocytic pathway. Curr. Opin. Cell Biol. 2007, 19:436-445.
159. Vonk L.A., Doulabi B.Z., Huang C., Helder M.N., Everts V., Bank R.A. Collagen-induced expression of collagenase-3 by primary chondrocytes is mediated by integrin & α1 and discoidin domain receptor 2: a protein kinase C-dependent pathway. Rheumatology 2011, 50:463-472.
160. Wall S.J., Werner E., Werb Z., DeClerck Y.A. Discoidin domain receptor 2 mediates tumor cell cycle arrest induced by fibrillar collagen. J. Biol. Chem. 2005, 280:40187-40194.
161. Wang J., Lu H., Liu X., Deng Y., Sun T., Li F., Ji S., Nie X., Yao L. Functional analysis of discoidin domain receptor 2 in synovial fibroblasts in rheumatoid arthritis. J. Autoimmun. 2002, 19:161-168.
162. Wang C.Z., Hsu Y.M., Tang M.J. Function of discoidin domain receptor I in HGF-induced branching tubulogenesis of MDCK cells in collagen gel. J. Cell. Physiol. 2005, 203:295-304.
163. Wang C.Z., Su H.W., Hsu Y.C., Shen M.R., Tang M.J. A discoidin domain receptor 1/SHP-2 signaling complex inhibits {alpha}2beta1-integrin-mediated signal transducers and activators of transcription 1/3 activation and cell migration. Mol. Biol. Cell 2006, 17:2839-2852.
164. Wang C.Z., Yeh Y.C., Tang M.J. DDR1/E-cadherin complex regulates the activation of DDR1 and cell spreading. Am. J. Physiol. Cell Physiol. 2009, 297:C419-C429.
165. Xu L., Peng H., Wu D., Hu K., Goldring M.B., Olsen B.R., Li Y. Activation of the discoidin domain receptor 2 induces expression of matrix metalloproteinase 13 associated with osteoarthritis in mice. J. Biol. Chem. 2005, 280:548-555.
166. Xu L., Peng H., Glasson S., Lee P.L., Hu K., Ijiri K., Olsen B.R., Goldring M.B., Li Y. Increased expression of the collagen receptor discoidin domain receptor 2 in articular cartilage as a key event in the pathogenesis of osteoarthritis. Arthritis Rheum. 2007, 56:2663-2673.
167. Xu L., Servais J., Polur I., Kim D., Lee P.L., Chung K., Li Y. Attenuation of osteoarthritis progression by reduction of discoidin domain receptor 2 in mice. Arthritis Rheum. 2010, 62:2736-2744.
168. Xu H., Raynal N., Stathopoulos S., Myllyharju J., Farndale R.W., Leitinger B. Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol. 2011, 30:16-26.
169. Xu L., Polur I., Servais J.M., Hsieh S., Lee P.L., Goldring M.B., Li Y. Intact pericellular matrix of articular cartilage is required for unactivated discoidin domain receptor 2 in the mouse model. Am. J. Pathol. 2011, 179:1338-1346.
170. Xu H., Bihan D., Chang F., Huang P.H., Farndale R.W., Leitinger B. Discoidin domain receptors promote α1β1- and α2β1-integrin mediated cell adhesion to collagen by enhancing integrin activation. PLoS One 2012, 7:e52209.
171. Yang K., Kim J.H., Kim H.J., Park I.S., Kim I.Y., Yang B.S. Tyrosine 740 phosphorylation of discoidin domain receptor 2 by Src stimulates intramolecular autophosphorylation and Shc signaling complex formation. J. Biol. Chem. 2005, 280:39058-39066.
172. Yang G., Li Q., Ren S., Lu X., Fang L., Zhou W., Zhang F., Xu F., Zhang Z., Zeng R., Lottspeich F., Chen Z. Proteomic, functional and motif-based analysis of C-terminal Src kinase-interacting proteins. Proteomics 2009, 9:4944-4961.
173. Yang S.H., Baek H.A., Lee H.J., Park H.S., Jang K.Y., Kang M.J., Lee D.G., Lee Y.C., Moon W.S., Chung M.J. Discoidin domain receptor 1 is associated with poor prognosis of non-small cell lung carcinomas. Oncol. Rep. 2010, 24:311-319.
174. Yang J., Wheeler S.E., Velikoff M., Kleaveland K.R., Lafemina M.J., Frank J.A., Chapman H.A., Christensen P.J., Kim K.K. Activated alveolar epithelial cells initiate fibrosis through secretion of mesenchymal proteins. Am. J. Pathol. 2013, 183:1559-1570.
175. Yeh Y.C., Wang C.Z., Tang M.J. Discoidin domain receptor 1 activation suppresses alpha2beta1 integrin-dependent cell spreading through inhibition of Cdc42 activity. J. Cell. Physiol. 2009, 218:146-156.
176. Yeh Y.C., Wu C.C., Wang Y.K., Tang M.J. DDR1 triggers epithelial cell differentiation by promoting cell adhesion through stabilization of E-cadherin. Mol. Biol. Cell 2011, 22:940-953.
177. Yoshida D., Teramoto A. Enhancement of pituitary adenoma cell invasion and adhesion is mediated by discoidin domain receptor-1. J. Neurooncol 2007, 82:29-40.
178. Zerlin M., Julius M.A., Goldfarb M. NEP: a novel receptor-like tyrosine kinase expressed in proliferating neuroepithelia. Oncogene 1993, 8:2731-2739.
179. Zhang X.H., Yan M., Liu L., Wu T.J., Ma L.L., Wang L.X. Expression of discoidin domain receptors (DDR2) in alcoholic liver fibrosis in rats. Arch. Med. Res. 2010, 41:586-592.
180. Zhang Y., Su J., Yu J., Bu X., Ren T., Liu X., Yao L. An essential role of discoidin domain receptor 2 (DDR2) in osteoblast differentiation and chondrocyte maturation via modulation of Runx2 activation. J. Bone Miner. Res. 2011, 26:604-617.
181. Zhang K., Corsa C.A., Ponik S.M., Prior J.L., Piwnica-Worms D., Eliceiri K.W., Keely P.J., Longmore G.D. The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat. Cell Biol. 2013, 15:677-687.