Inhibition of Collagen Fibrillogenesis by Cells Expressing Soluble Extracellular Domains of DDR1 and DDR2

Journal of Molecular Biology

Volumn 395, Issue 3, 2010, Pages 533-543

  Flynn, Lisa A ^a   Blissett, Angela R ^a   Calomeni, Edward P ^b   Agarwal, Gunjan ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

collagen fibrillogenesis; DDR1; DDR2; ECD; TEM

Indexed keywords

COLLAGEN BINDING PROTEIN; COLLAGEN FIBER; COLLAGEN RECEPTOR; DISCOIDIN DOMAIN RECEPTOR 1; DISCOIDIN DOMAIN RECEPTOR 2; HYDROXYPROLINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CELL SECRETION; CELL ULTRASTRUCTURE; CHEMICAL ANALYSIS; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; MINERALIZATION; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; TRANSMISSION ELECTRON MICROSCOPY;

EID: 73249126900     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.073     Document Type: Article

References (51)

1. Jepsen K.J., Schaffler M.B., Kuhn J.L., Goulet R.W., Bonadio J., and Goldstein S.A. Type I collagen mutation alters the strength and fatigue behavior of Mov13 cortical tissue. J. Biomech. 30 (1997) 1141-1147
2. Blissett A.R., Garbellini D., Calomeni E.P., Mihai C., Elton T.S., and Agarwal G. Regulation of collagen fibrillogenesis by cell-surface expression of kinase dead DDR2. J. Mol. Biol. 385 (2009) 902-911
3. Neame P.J., Kay C.J., McQuillan D.J., Beales M.P., and Hassell J.R. Independent modulation of collagen fibrillogenesis by decorin and lumican. Cell. Mol. Life Sci. 57 (2000) 859-863
4. Wiesmann H.P., Meyer U., Plate U., and Hohling H.J. Aspects of collagen mineralization in hard tissue formation. Int. Rev. Cytol. 242 (2005) 121-156
5. Ferri N., Carragher N.O., and 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. 164 (2004) 1575-1585
6. Hou G., Vogel W., and Bendeck M.P. The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J. Clin. Invest. 107 (2001) 727-735
7. Vogel W.F. Collagen-receptor signaling in health and disease. Eur. J. Dermatol. 11 (2001) 506-514
8. Sunk I.G., Bobacz K., Hofstaetter J.G., Amoyo L., Soleiman A., Smolen J., Xu L., and 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. 56 (2007) 3685-3692
9. Xu L., Peng H., Glasson S., Lee P.L., Hu K., Ijiri K., Olsen B.R., Goldring M.B., and 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. 56 (2007) 2663-2673
10. Lam N.P., Li Y., Waldman A.B., Brussiau J., Lee P.L., Olsen B.R., and Xu L. Age-dependent increase of discoidin domain receptor 2 and matrix metalloproteinase 13 expression in temporomandibular joint cartilage of type IX and type XI collagen-deficient mice. Arch. Oral Biol. 52 (2007) 579-584
11. Vogel W., Gish G.D., Alves F., and Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1 (1997) 13-23
12. Alves F., Saupe S., Ledwon M., Schaub F., Hiddemann W., and 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. 15 (2001) 1321-1323
13. Vogel W.F. Ligand-induced shedding of discoidin domain receptor 1. FEBS Lett. 514 (2002) 175-180
14. Slack B.E., Siniaia M.S., and Blusztajn J.K. Collagen type I selectively activates ectodomain shedding of the discoidin domain receptor 1: involvement of Src tyrosine kinase. J. Cell Biochem. 98 (2006) 672-684
15. Alves F., Vogel W., Mossie K., Millauer B., Hofler H., and Ullrich A. Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10 (1995) 609-618
16. Karn T., Holtrich U., Brauninger A., Bohme B., Wolf G., Rubsamen-Waigmann H., and 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 8 (1993) 3433-3440
17. Lai C., and Lemke G. Structure and expression of the Tyro 10 receptor tyrosine kinase. Oncogene 9 (1994) 877-883
18. Agarwal G., Mihai C., and Iscru D.F. Interaction of discoidin domain receptor 1 with collagen type 1. J. Mol. Biol. 367 (2007) 443-455
19. Mihai C., Iscru D.F., Druhan L.J., Elton T.S., and Agarwal G. Discoidin domain receptor 2 inhibits fibrillogenesis of collagen type 1. J. Mol. Biol. 361 (2006) 864-876
20. Alberts B. Molecular Biology of the Cell. Reference Edition. 5th edit (2008), Garland Science, New York
21. Pornprasertsuk S., Duarte W.R., Mochida Y., and Yamauchi M. Overexpression of lysyl hydroxylase-2b leads to defective collagen fibrillogenesis and matrix mineralization. J. Bone Miner. Res. 20 (2005) 81-87
22. 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. 278 (2003) 16761-16769
23. Olaso E., Labrador J.P., Wang L., Ikeda K., Eng F.J., Klein R., et al. 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 (2002) 3606-3613
24. Ikeda K., Wang L.H., Torres R., Zhao H., Olaso E., Eng F.J., et al. Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen. J. Biol. Chem. 277 (2002) 19206-19212
25. Reddy G.K., and Enwemeka C.S. A simplified method for the analysis of hydroxyproline in biological tissues. Clin. Biochem. 29 (1996) 225-229
26. Coetzee M., Haag M., and Kruger M.C. Effects of arachidonic acid and docosahexaenoic acid on differentiation and mineralization of MC3T3-E1 osteoblast-like cells. Cell Biochem. Funct. 27 (2009) 3-11
27. Laval S., Butler R., Shelling A.N., Hanby A.M., Poulsom R., and Ganesan T.S. Isolation and characterization of an epithelial-specific receptor tyrosine kinase from an ovarian cancer cell line. Cell Growth Differ. 5 (1994) 1173-1183
28. Noordeen N.A., Carafoli F., Hohenester E., Horton M.A., and Leitinger B. A transmembrane leucine zipper is required for activation of the dimeric receptor tyrosine kinase DDR1. J. Biol. Chem. 281 (2006) 22744-22751
29. Abdulhussein R., McFadden C., Fuentes-Prior P., and Vogel W.F. Exploring the collagen-binding site of the DDR1 tyrosine kinase receptor. J. Biol. Chem. 279 (2004) 31462-31470
30. Abdulhussein R., Koo D.H., and Vogel W.F. Identification of disulfide-linked dimers of the receptor tyrosine kinase DDR1. J. Biol. Chem. 283 (2008) 12026-12033
31. Mihai C., Chotani M., Elton T.S., and Agarwal G. Mapping of DDR1 distribution and oligomerization on the cell surface by FRET microscopy. J. Mol. Biol. 385 (2009) 432-445
32. Velleman S.G. The role of the extracellular matrix in skeletal muscle development. Poult. Sci. 78 (1999) 778-784
33. Reed C.C., and Iozzo R.V. The role of decorin in collagen fibrillogenesis and skin homeostasis. Glycoconjugate J. 19 (2002) 249-255
34. Yoon J.H., and Halper J. Tendon proteoglycans: biochemistry and function. J. Musculoskeletal Neuronal Interact. 5 (2005) 22-34
35. Chakravarti S. Functions of lumican and fibromodulin: lessons from knockout mice. Glycoconjugate J. 19 (2002) 287-293
36. Ameye L., Aria D., Jepsen K., Oldberg A., Xu T., and Young M.F. Abnormal collagen fibrils in tendons of biglycan/fibromodulin-deficient mice lead to gait impairment, ectopic ossification, and osteoarthritis. FASEB J. 16 (2002) 673-680
37. Norris R.A., Damon B., Mironov V., Kasyanov V., Ramamurthi A., Moreno-Rodriguez R., et al. Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J. Cell Biochem. 101 (2007) 695-711
38. Vogel K.G., and Trotter J.A. The effect of proteoglycans on the morphology of collagen fibrils formed in vitro. Collagen Relat. Res. 7 (1987) 105-114
39. Danielson K.G., Baribault H., Holmes D.F., Graham H., Kadler K.E., and Iozzo R.V. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136 (1997) 729-743
40. Kadler K.E., Hill A., and Canty-Laird E.G. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr. Opin. Cell Biol. 20 (2008) 495-501
41. Jokinen J., Dadu E., Nykvist P., Kapyla J., White D.J., Ivaska J., et al. Integrin-mediated cell adhesion to type I collagen fibrils. J. Biol. Chem. 279 (2004) 31956-31963
42. Louis H., Kakou A., Regnault V., Labat C., Bressenot A., Gao-Li J., et al. Role of alpha1beta1-integrin in arterial stiffness and angiotensin-induced arterial wall hypertrophy in mice. Am. J. Physiol. Heart Circ. Physiol. 293 (2007) H2597-2604
43. Holtkotter O., Nieswandt B., Smyth N., Muller W., Hafner M., Schulte V., et al. Integrin alpha 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J. Biol. Chem. 277 (2002) 10789-10794
44. Weng J., Luo J., Cheng X., Jin C., Zhou X., Qu J., et al. Deletion of G protein-coupled receptor 48 leads to ocular anterior segment dysgenesis (ASD) through down-regulation of Pitx2. Proc. Natl Acad. Sci. USA 105 (2008) 6081-6086
45. Kvist A.P., Latvanlehto A., Sund M., Eklund L., Vaisanen T., Hagg P., et al. Lack of cytosolic and transmembrane domains of type XIII collagen results in progressive myopathy. Am. J. Pathol. 159 (2001) 1581-1592
46. Kadler K.E., Holmes D.F., Trotter J.A., and Chapman J.A. Collagen fibril formation. Biochem. J. 316 Pt. 1 (1996) 1-11
47. Bargal R., Cormier-Daire V., Ben-Neriah Z., Le Merrer M., Sosna J., Melki J., et al. Mutations in DDR2 gene cause SMED with short limbs and abnormal calcifications. Am. J. Hum. Genet. 84 (2009) 80-84
48. Vogel W.F., Aszodi A., Alves F., and Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol. Cell Biol. 21 (2001) 2906-2917
49. Di Lullo G.A., Sweeney S.M., Korkko J., Ala-Kokko L., and San Antonio J.D. Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. J. Biol. Chem. 277 (2002) 4223-4231
50. Shrivastava A., Radziejewski C., Campbell E., Kovac L., McGlynn M., Ryan T.E., et al. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell 1 (1997) 25-34
51. Murad S., Grove D., Lindberg K.A., Reynolds G., Sivarajah A., and Pinnell S.R. Regulation of collagen synthesis by ascorbic acid. Proc. Natl Acad. Sci. USA 78 (1981) 2879-2882