Impairment of VEGF-A-stimulated lamellipodial extensions and motility of vascular endothelial cells by chondromodulin-I, a cartilage-derived angiogenesis inhibitor

Experimental Cell Research

Volumn 316, Issue 5, 2010, Pages 775-788

  Miura, Shigenori ^a   Mitsui, Kaori ^b   Heishi, Takahiro ^c   Shukunami, Chisa ^a   Sekiguchi, Kiyotoshi ^d   Kondo, Jun ^e   Sato, Yasufumi ^c   Hiraki, Yuji ^a  

^a KYOTO UNIVERSITY   (Japan)

^b MITSUBISHI CHEMICAL CORPORATION   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e MITSUBISHI TANABE PHARMA CORPORATION   (Japan)

Author keywords

Angiogenesis inhibitor; Cell migration; Chondromodulin I; Vascular endothelial cell; VEGF A

Indexed keywords

CHONDROMODULIN I; FIBROBLAST GROWTH FACTOR 2; GLYCOPROTEIN; PROTEIN CDC42; RAC1 PROTEIN; RECOMBINANT PROTEIN; SOMATOMEDIN C; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL SPECIFICITY; CELL SPREADING; CONTROLLED STUDY; CORNEA VASCULARIZATION; CYTOSKELETON; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LAMELLIPODIUM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

EID: 76749155507     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.12.009     Document Type: Article

References (47)

1. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1 (1995) 27-31
2. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev., Cancer 3 (2003) 422-433
3. O'Reilly M.S., Boehm T., Shing Y., Fukai N., Vasios G., Lane W.S., Flynn E., Birkhead J.R., Olsen B.R., and Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88 (1997) 277-285
4. Mundel T.M., and Kalluri R. Type IV collagen-derived angiogenesis inhibitors. Microvasc. Res 74 (2007) 85-89
5. Hiraki Y., Tanaka H., Inoue H., Kondo J., Kamizono A., and Suzuki F. Molecular cloning of a new class of cartilage-specific matrix, chondromodulin-I, which stimulates growth of cultured chondrocytes. Biochem. Biophys. Res. Commun. 175 (1991) 971-977
6. Shukunami C., and Hiraki Y. Chondromodulin-I and tenomodulin: the negative control of angiogenesis in connective tissue. Curr. Pharm. Des. 13 (2007) 2101-2112
7. Hiraki Y., Kono T., Sato M., Shukunami C., and Kondo J. Inhibition of DNA synthesis and tube morphogenesis of cultured vascular endothelial cells by chondromodulin-I. FEBS Lett. 415 (1997) 321-324
8. Hiraki Y., Inoue H., Iyama K., Kamizono A., Ochiai M., Shukunami C., Iijima S., Suzuki F., and Kondo J. Identification of chondromodulin I as a novel endothelial cell growth inhibitor. Purification and its localization in the avascular zone of epiphyseal cartilage. J. Biol. Chem. 272 (1997) 32419-32426
9. Hiraki Y., Mitsui K., Endo N., Takahashi K., Hayami T., Inoue H., Shukunami C., Tokunaga K., Kono T., Yamada M., Takahashi H.E., and Kondo J. Molecular cloning of human chondromodulin-I, a cartilage-derived growth modulating factor, and its expression in Chinese hamster ovary cells. Eur. J. Biochem. 260 (1999) 869-878
10. Shukunami C., Iyama K., Inoue H., and Hiraki Y. Spatiotemporal pattern of the mouse chondromodulin-I gene expression and its regulatory role in vascular invasion into cartilage during endochondral bone formation. Int. J. Dev. Biol. 43 (1999) 39-49
11. Dietz U.H., Ziegelmeier G., Bittner K., Bruckner P., and Balling R. Spatio-temporal distribution of chondromodulin-I mRNA in the chicken embryo: expression during cartilage development and formation of the heart and eye. Dev. Dyn. 216 (1999) 233-243
12. Funaki H., Sawaguchi S., Yaoeda K., Koyama Y., Yaoita E., Funaki S., Shirakashi M., Oshima Y., Shukunami C., Hiraki Y., Abe H., and Yamamoto T. Expression and localization of angiogenic inhibitory factor, chondromodulin-I, in adult rat eye. Invest. Ophthalmol. Vis. Sci. 42 (2001) 1193-1200
13. Yoshioka M., Yuasa S., Matsumura K., Kimura K., Shiomi T., Kimura N., Shukunami C., Okada Y., Mukai M., Shin H., Yozu R., Sata M., Ogawa S., Hiraki Y., and Fukuda K. Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis. Nat. Med. 12 (2006) 1151-1159
14. Shukunami C., Takimoto A., Miura S., Nishizaki Y., and Hiraki Y. Chondromodulin-I and tenomodulin are differentially expressed in the avascular mesenchyme during mouse and chick development. Cell Tissue Res. 332 (2008) 111-122
15. Nakamichi Y., Shukunami C., Yamada T., Aihara K., Kawano H., Sato T., Nishizaki Y., Yamamoto Y., Shindo M., Yoshimura K., Nakamura T., Takahashi N., Kawaguchi H., Hiraki Y., Kato S., and Chondromodulin I. is a bone remodeling factor. Mol. Cell. Biol. 23 (2003) 636-644
16. Risau W. Mechanisms of angiogenesis. Nature 386 (1997) 671-674
17. Niwa H., Yamamura K., and Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108 (1991) 193-199
18. Oshima Y., Sato K., Tashiro F., Miyazaki J., Nishida K., Hiraki Y., Tano Y., and Shukunami C. Anti-angiogenic action of the C-terminal domain of tenomodulin that shares homology with chondromodulin-I. J. Cell Sci. 117 (2004) 2731-2744
19. Watanabe K., Hasegawa Y., Yamashita H., Shimizu K., Ding Y., Abe M., Ohta H., Imagawa K., Hojo K., Maki H., Sonoda H., and Sato Y. Vasohibin as an endothelium-derived negative feedback regulator of angiogenesis. J. Clin. Invest. 114 (2004) 898-907
20. Yanai N., Satoh T., and Obinata M. Endothelial cells create a hematopoietic inductive microenvironment preferential to erythropoiesis in the mouse spleen. Cell Struct. Funct. 16 (1991) 87-93
21. Namba K., Abe M., Saito S., Satake M., Ohmoto T., Watanabe T., and Sato Y. Indispensable role of the transcription factor PEBP2/CBF in angiogenic activity of a murine endothelial cell MSS31. Oncogene 19 (2000) 106-114
22. Shukunami C., Shigeno C., Atsumi T., Ishizeki K., Suzuki F., and Hiraki Y. Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J. Cell Biol. 133 (1996) 457-468
23. Chomczynski P., and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 (1987) 156-159
24. Wickstrom S.A., Alitalo K., and Keski-Oja J. An endostatin-derived peptide interacts with integrins and regulates actin cytoskeleton and migration of endothelial cells. J. Biol. Chem. 279 (2004) 20178-20185
25. Nyberg P., Xie L., and Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res 65 (2005) 3967-3979
26. Yamaguchi N., Anand-Apte B., Lee M., Sasaki T., Fukai N., Shapiro R., Que I., Lowik C., Timpl R., and Olsen B.R. Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding. EMBO J. 18 (1999) 4414-4423
27. Montesano R., and Orci L. Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell 42 (1985) 469-477
28. English D., Welch Z., Kovala A.T., Harvey K., Volpert O.V., Brindley D.N., and Garcia J.G. Sphingosine 1-phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and angiogenesis. FASEB J. 14 (2000) 2255-2265
29. Wang F., Van Brocklyn J.R., Hobson J.P., Movafagh S., Zukowska-Grojec Z., Milstien S., and Spiegel S. Sphingosine 1-phosphate stimulates cell migration through a G(i)-coupled cell surface receptor. Potential involvement in angiogenesis. J. Biol. Chem. 274 (1999) 35343-35350
30. Boilly B., Vercoutter-Edouart A.S., Hondermarck H., Nurcombe V., and Le Bourhis X. FGF signals for cell proliferation and migration through different pathways. Cytokine Growth Factor Rev. 11 (2000) 295-302
31. Calalb M.B., Polte T.R., and Hanks S.K. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol. 15 (1995) 954-963
32. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., and Horwitz A.R. Cell migration: integrating signals from front to back. Science 302 (2003) 1704-1709
33. Abedi H., and Zachary I. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J. Biol. Chem. 272 (1997) 15442-15451
34. Soga N., Namba N., McAllister S., Cornelius L., Teitelbaum S.L., Dowdy S.F., Kawamura J., and Hruska K.A. Rho family GTPases regulate VEGF-stimulated endothelial cell motility. Exp. Cell Res. 269 (2001) 73-87
35. Garrett T.A., Van Buul J.D., and Burridge K. VEGF-induced Rac1 activation in endothelial cells is regulated by the guanine nucleotide exchange factor Vav2. Exp. Cell Res. 313 (2007) 3285-3297
36. Ji W.R., Castellino F.J., Chang Y., Deford M.E., Gray H., Villarreal X., Kondri M.E., Marti D.N., Llinas M., Schaller J., Kramer R.A., and Trail P.A. Characterization of kringle domains of angiostatin as antagonists of endothelial cell migration, an important process in angiogenesis. FASEB J 12 (1998) 1731-1738
37. Short S.M., Derrien A., Narsimhan R.P., Lawler J., Ingber D.E., and Zetter B.R. Inhibition of endothelial cell migration by thrombospondin-1 type-1 repeats is mediated by beta1 integrins. J. Cell Biol. 168 (2005) 643-653
38. Dixelius J., Cross M., Matsumoto T., Sasaki T., Timpl R., and Claesson-Welsh L. Endostatin regulates endothelial cell adhesion and cytoskeletal organization. Cancer Res. 62 (2002) 1944-1947
39. Sudhakar A., Sugimoto H., Yang C., Lively J., Zeisberg M., and Kalluri R. Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by alpha v beta 3 and alpha 5 beta 1 integrins. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4766-4771
40. Bix G., Fu J., Gonzalez E.M., Macro L., Barker A., Campbell S., Zutter M.M., Santoro S.A., Kim J.K., Hook M., Reed C.C., and Iozzo R.V. Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through alpha2beta1 integrin. J. Cell Biol. 166 (2004) 97-109
41. Sudhakar A., Nyberg P., Keshamouni V.G., Mannam A.P., Li J., Sugimoto H., Cosgrove D., and Kalluri R. Human alpha1 type IV collagen NC1 domain exhibits distinct antiangiogenic activity mediated by alpha1beta1 integrin. J. Clin. Invest. 115 (2005) 2801-2810
42. Kolsch V., Charest P.G., and Firtel R.A. The regulation of cell motility and chemotaxis by phospholipid signaling. J. Cell Sci. 121 (2008) 551-559
43. Vicente-Manzanares M., Choi C.K., and Horwitz A.R. Integrins in cell migration-the actin connection. J. Cell Sci. 122 (2009) 199-206
44. Aase K., Ernkvist M., Ebarasi L., Jakobsson L., Majumdar A., Yi C., Birot O., Ming Y., Kvanta A., Edholm D., Aspenstrom P., Kissil J., Claesson-Welsh L., Shimono A., and Holmgren L. Angiomotin regulates endothelial cell migration during embryonic angiogenesis. Genes Dev. 21 (2007) 2055-2068
45. Ridley A.J. Rho GTPases and cell migration. J. Cell Sci. 114 (2001) 2713-2722
46. Vicente-Manzanares M., Webb D.J., and Horwitz A.R. Cell migration at a glance. J. Cell Sci. 118 (2005) 4917-4919
47. Keezer S.M., Ivie S.E., Krutzsch H.C., Tandle A., Libutti S.K., and Roberts D.D. Angiogenesis inhibitors target the endothelial cell cytoskeleton through altered regulation of heat shock protein 27 and cofilin. Cancer Res 63 (2003) 6405-6412