Brain-derived neurotrophic factor induces migration of endothelial cells through a TrkB-ERK-integrin α Vβ 3-FAK cascade

Journal of Cellular Physiology

Volumn 227, Issue 5, 2012, Pages 2123-2129

  Matsuda, Shinji ^a   Fujita, Tsuyoshi ^a   Kajiya, Mikihito ^a   Takeda, Katsuhiro ^a   Shiba, Hideki ^a   Kawaguchi, Hiroyuki ^a   Kurihara, Hidemi ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FOCAL ADHESION KINASE; K 252A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UMBILICAL VEIN ENDOTHELIAL CELL; WOUND HEALING;

BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIAL CELLS; ENZYME ACTIVATION; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; INTEGRIN ALPHAVBETA3; PHOSPHORYLATION; RECEPTOR, TRKB; SIGNAL TRANSDUCTION;

EID: 84856139781     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22942     Document Type: Article

References (62)

1. Alavi A, Hood JD, Frausto R, Stupack DG, Cheresh DA. 2003. Role of Raf in vascular protection from distinct apoptotic stimuli. Science 301: 94-96.
2. Asaumi K, Nakanishi T, Asahara H, Inoue H, Takigawa M. 2000. Expression of neurotrophins and their receptors (Trk) during fracture healing. Bone 26: 625-633.
3. Barbacid M. 1994. The Trk family of neurotrophin receptors. J Neurobiol 25: 1386-1403.
4. Bibel M, Barde YA. 2000. Neurotrophins: Key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14: 2919-2937.
5. 3 for angiogenesis. Science 264: 569-571.
6. 3 regulates cell adhesion and migration to bone sialoprotein. Exp Cell Res 254: 299-308.
7. Calalb MB, Polte TR, Hanks SK. 1995. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: A role for src family kinase. Mol Cell Biol 15: 954-963.
8. 3 and induces blood vessel formation in vivo. J Biol Chem 277: 17281-17290.
9. Defilippi P, Silengo L, Tarone G. 1993. Regulation of adhesion receptors expression in endothelial cells. Curr Top Microbiol Immunol 184: 87-98.
10. Donovan MJ, Lin MI, Wiegn P, Ringstedt T, Kraemer R, Hahn R, Wang S, Ibanez CF, Rafii S, Hempstead BL. 2000. Brain derived neurotrophic factor is an endothelial cell survival factor requird for intramyocardial vessel stabilization. Development 127: 4531-4540.
11. Ebendal T. 1992. Function and evolution in the NGF family and its receptors. J Neurosci Res 32: 461-470.
12. Eliceiri BP, Cheresh DA. 1999. The role of alphav integrins during angiogenesis: Insights into potential mechanisms of action and clinical development. J Clin Invest 103: 1227-1230.
13. 3 requirement for sustained mitogen-activated protein kinase activity during angiogenesis. J Cell Biol 140: 1255-1263.
14. Fassler R, Meyer M. 1995. Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 9: 1896-1908.
15. Folkman J. 1995. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27-31.
16. Folkman J, Shing Y. 1992. Angiogenesis. J Biol Chem 267: 10931-10934.
17. Furukawa Y, Furukawa S, Satoyoshi E, Hayashi K. 1984. Nerve growth factor secreted by mouse heart cells in culture. J Biol Chem 259: 1259-1264.
18. 3-integrin in TNF-α-induced endothelial cell migration. Am J Physiol Cell Physiol 283: C1196-C1205.
19. Giancotti FG, Ruoslahti E. 1999. Integrin signaling. Science 285: 1028-1032.
20. NTR. Curr Opin Neurobiol 12: 260-267.
21. Hood JD, Bednarski M, Frausto R, Guccione S, Reisfeld RA, Xiang R, Cheresh DA. 2002. Tumor regression by targeted gene delivery to the neovasculature. Science 296: 2404-2407.
22. V integrin-mediated Ras-ERK signaling during two pathways of angiogenesis. J Cell Biol 162: 933-943.
23. Horwitz AR, Parsons JT. 1999. Cell migration-Movin' on. Science 286: 1102-1103.
24. Huang EJ, Reichardt LF. 2003. Trk receptors: Role in neuronal signal transduction. Annu Rev Biochem 72: 609-642.
25. Huttenlocher A, Ginsberg MH, Horwitz AF. 1996. Modulation of cell migration by integrin-mediated cytoskeletal linkages and ligand-binding affinity. J Cell Biol 134: 1551-1562.
26. Hynes RO, Bader BL. 1997. Targeted mutations in integrins and their ligands: Their implications for vascular biology. Thromb Haemost 78: 83-87.
27. Johnson D, Lanahan A, Buck CR, Sehgal A, Morgan C, Mercer E, Bothwell M, Chao M. 1986. Expression and structure of the human NGF receptor. Cell 47: 545-554.
28. Kajiya M, Shiba H, Fujita T, Ouhara K, Takeda K, Mizuno N, Kawaguchi H, Kitagwa M, Takata T, Tsuji K, Kurihara H. 2008. Brain-derived neurotrophic factor stimulates bone/cementum-related protein gene expression in cementoblasts. J Biol Chem 283: 16259-16267.
29. Kajiya M, Shiba H, Fujita T, Takeda K, Uchida Y, Kawaguchi H, Kitagwa M, Takata T, Kurihara H. 2009. Brain-derived neurotrophic factor protects cementoblasts from serum starvation-induced cell death. J Cell Physiol 221: 696-706.
30. Katz M, Amit I, Yarden Y. 2007. Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim Biophys Acta 1773: 1161-1176.
31. Kermani P, Hempstead B. 2007. Brain-derived Neurotrophic factor: A newly described mediator of angiogenesis. Trends Cardiovasc Med 17: 140-143.
32. Kerschensteiner M, Gallmeier E, Behrens L, Leal VV, Misgeld T, Klinkert WE, Kolbeck R, Hoppe E, Oropeza-Wekerle RL, Bartke I, Stadelmann C, Lassmann H, Wekerle H, Hohlfeld R. 1999. Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: A neuroprotective role of inflammation? J Exp Med 189: 865-870.
33. Klemke RL, Cai S, Giannini AL, Gallagher PJ, Lanerolle P, Cheresh DA. 1997. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137: 481-492.
34. Kurihara H, Shinohara H, Yoshino H, Takeda K, Shiba H. 2003. Neurotrophins in cultured cells from periodontal tissues. J Periodontol 74: 76-84.
35. Lampugnani MG, Resnati M, Dejana E, Marchisio PC. 1991. The role of integrins in the maintenance of endothelial monolayer integrity. J Cell Biol 112: 479-490.
36. Lauffenburger DA, Horwitz AF. 1996. Cell migration: A physically integrated molecular process. Cell 84: 359-369.
37. MacGrogan D, Saint-Andre JP, Dicou E. 1992. Expression of nerve growth factor and nerve growth factor receptor genes in human tissues and in prostatic adenocarcinoma cell lines. J Neurochem 59: 1381-1391.
38. Mavria G, Vercoulen Y, Yeo M, Paterson H, Karasarides M, Marais R, Bird D, Marshall CJ. 2006. ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9: 33-44.
39. Murphy DA, Makonnen S, Lassoued W, Feldman MD, Carter C, Lee WM. 2006. Inhibition of tumor endothelial ERK activation, angiogenesis, and tumor growth by sorafenib. Am J Pathol 169: 1875-1885.
40. Nakahashi T, Fujimura H, Altar CA, Li J, Kambayashi J, Tandon NN, Sun B. 2000. Vascular emdothelial cells synthesize and secrete brain-derived neurotrophic factor. FEBS Lett 470: 113-117.
41. Nakanishi T, Takahashi K, Aoki C, Nishikawa K, Hattori T, Taniguchi S. 1994. Expression of nerve growth factor family neurotrophins in a mouse osteoblastic cell line. Biochem Biophys Res Commun 198: 891-897.
42. Nosrat CA, Fried K, Lindskog S, Olson L. 1997. Cellular expression of neurotrophin mRNAs during tooth development. Cell Tissue Res 290: 569-580.
43. Otten U, Ehrhard P, Peck R. 1989. Nerve growth factor induces growth and differentiation of human B lymphocytes. Proc Natl Acad Sci USA 86: 10059-10063.
44. Park MJ, Kwak HJ, Lee HC, Yoo DH, Park IC, Kim MS, Lee SH, Rhee CH, Hong SI. 2007. Nerve growth factor induces endothelial cell invasion and cord formation by promoting matrix metalloproteinase-2 expression through the phosphatidylinositol 3-kinase/Akt signaling pathway and AP-2 transcription factor. J Biol Chem 282: 30485-30496.
45. Parsons JT, Martin KH, Slack JK, Taylor JM, Weed SA. 2000. Focal adhesion kinase: A regulator of focal adhesion dynamics and cell movement. Oncogene 19: 5606-5613.
46. Pechkovsky DV, Scaffidi AK, Hackett TL, Ballard J, Shaheen F, Thompson PJ, Thannickal VJ, Knight DA. 2008. Transforming growth factor beta1 induces alphavbeta3 integrin expression in human lung fibroblasts via a beta3 integrin-, c-Src-, and p38 MAPK-dependent pathway. J Biol Chem 283: 12898-12908.
47. Pintucci G, Moscatelli D, Saponara F, Biernacki PR, Baumanr FG, Bizekis C, Galloway AC, Basilico C, Mignatti P. 2002. Lack of ERK activation and cell migration in FGF-2-deficient endothelial cells. FASEB J 16: 598-600.
48. Radeke MJ, Misko TP, Hsu C, Herzenberg LA, Shooter EM. 1987. Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 325: 593-597.
49. Rasband WS. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, 1997-2011.
50. 3 integrin and regulates cell spreading on vitronectin. J Biol Chem 278: 1975-1985.
51. Rousseau S, Houle F, Kotanides H, Witte L, Waltenberger J, Landry J, Huot J. 2000. Vascular endothelial growth factor (VEGF)-driven actin-based motility is mediated by VEGFR2 and requires concerted activation of stress-activated protein kinase 2 (SAPK2/p38) and geldanamycin-sensitive phosphorylation of focal adhesion kinase. J Biol Chem 275: 10661-10672.
52. Ruoslahti E. 1988. Fibronectin and its receptors. Annu Rev Biochem 57: 375-413.
53. FAK, a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci USA 89: 5192-5196.
54. Serban D, Leng J, Cheresh DA. 2008. H-Ras regulates angiogenesis and vascular permeability by activation of distinct downstream effectors. Circ Res 102: 1350-1358.
55. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, Schlaepfer D. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2: 249-256.
56. Son SH, Kim MJ, Chung WY, Son JA, Kim YS, Kim YC, Kang SK, Park KK. 2009. Decursin and decurdinol inhibit VEGF-induced angiogenesis by blocking the activation of extracellular signal-regulated kinase and c-Jun N-terminal kinase. Cancer 280: 86-92.
57. Srinivasan R, Zabuawala T, Huang H, Zhang J, Gulati P, Fernandez S, Karlo JC, Landreth GE, Leone G, Ostrowski MC. 2009. Erk1 and Erk2 regulate endothelial cell proliferation and migration during mouse embryonic angiogenesis. PLOS One 12: e8283.
58. Takeda K, Shiba H, Mizuno N, Hasegawa N, Mouri Y, Hirachi A, Yoshino H, Kawaguchi H, Kurihara H. 2005. Brain-derived neurotrophic factor enhances periodontal tissue regeneration. Tissue Eng 11: 1618-1629.
59. Takeda K, Sakai N, Shiba H, Nagahara T, Fujita T, Kajiya M, Iwata T, Matsuda S, Kawahara K, Kawaguchi H, Kurihara H. 2010. Characteristics of high-molecular-weight hyaluronic acid as a brain-derived neurotrophic factor scaffold in periodontal tissue regeneration. Tissue Eng Part A 17: 955-967.
60. Wijelath ES, Murray J, Rahman S, Patel Y, Ishida A, Strand K, Aziz S, Cardona C, Hammond WP, Savidge GF, Rafii S, Sobel M. 2002. Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ Res 91: 25-31.
61. Yamashiro T, Fukunaga T, Yamashita K, Kobashi N, Yamamoto T. 2001. Gene and protein expression of brain-derived neurotrophic factor and TrkB in bone and cartlage. Bone 28: 404-409.
62. Zou JX, Liu Y, Pasquale EB, Ruoslahti E. 2002. Activated SRC oncogene phosphorylates R-ras and suppresses integrin activity. J Biol Chem 277: 1824-1827.