Semaphorin 4D/plexin-B1 induces endothelial cell migration through the activation of PYK2, Src, and the phosphatidylinositol 3-kinase-Akt pathway

Molecular and Cellular Biology

Volumn 25, Issue 16, 2005, Pages 6889-6898

  Basile, John R ^a   Afkhami, Talayeh ^b   Gutkind, J Silvio ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; FOCAL ADHESION KINASE 2; PHOSPHATIDYLINOSITOL 3 KINASE; PLEXIN; PLEXIN B1; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; SCATTER FACTOR RECEPTOR; SEMAPHORIN; SEMAPHORIN 4D; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL TYPE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD; CELL LINE; CELL MEMBRANE; CELL MOVEMENT; CYTOPLASM; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; FOCAL ADHESION KINASE 2; GENES, DOMINANT; HEPATOCYTE GROWTH FACTOR; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NEOVASCULARIZATION, PATHOLOGIC; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, TRKA; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; SEMAPHORINS; SRC-FAMILY KINASES; SWINE; TIME FACTORS; TYROSINE;

ANIMALIA;

EID: 23344446919     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.16.6889-6898.2005     Document Type: Article

References (64)

1. Alessi, D. R., M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and B. A. Hemmings. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15:6541-6551.
2. Anonymous. 1999. Unified nomenclature for the semaphorins/collapsins. Semaphorin Nomenclature Committee. Cell 97:551-552.
3. Aurandt, J., H. G. Vikis, J. S. Gutkind, N. Ahn, and K. L. Guan. 2002. The semaphorin receptor plexin-B1 signals through a direct interaction with the Rho-specific nucleotide exchange factor, LARG. Proc. Natl. Acad. Sci. USA 99:12085-12090.
4. Avraham, H., S. Y. Park, K. Schinkmann, and S. Avraham. 2000. RAFTK/Pyk2-mediated cellular signalling. Cell Signal. 12:123-133.
5. Basile, J. R., A. Barac, T. Zhu, K. L. Guan, and J. S. Gutkind. 2004. Class IV semaphorins promote angiogenesis by stimulating Rho-initiated pathways through plexin-B. Cancer Res. 64:5212-5224.
6. Bates, D., G. I. Taylor, J. Minichiello, P. Farlie, A. Cichowitz, N. Watson, M. Klagsbrun, R. Mamluk, and D. F. Newgreen. 2003. Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev. Biol. 255:77-98.
7. Birchmeier, C., F. Bladt, and T. Yamaai. 1997. The functions of HGF/SF and its receptor, the c-Met tyrosine kinase, in mammalian development. Ciba Found. Symp. 212:169-182.
8. Birchmeier, W., V. Brinkmann, C. Niemann, S. Meiners, S. DiCesare, H. Naundorf, and M. Sachs. 1997. Role of HGF/SF and c-Met in morphogenesis and metastasis of epithelial cells. Ciba Found. Symp. 212:230-246.
9. Bismuth, G., and L. Boumsell. 2002. Controlling the immune system through semaphorins. Science STKE 2002:RE4.
10. Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296:1655-1657.
11. Castellani, V., and G. Rougon. 2002. Control of semaphorin signaling. Curr. Opin. Neurobiol. 12:532-541.
12. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
13. Chikumi, H., S. Fukuhara, and J. S. Gutkind. 2002. Regulation of G protein-linked guanine nucleotide exchange factors for Rho, PDZ-RhoGEF, and LARG by tyrosine phosphorylation: evidence of a role for focal adhesion kinase. J. Biol. Chem. 277:12463-12473.
14. Comoglio, P. M., and L. Trusolino. 2002. Invasive growth: from development to metastasis. J. Clin. Investig. 109:857-862.
15. Dikic, I., G. Tokiwa, S. Lev, S. A. Courtneidge, and J. Schlessinger. 1996. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383:547-550.
16. Driessens, M. H., H. Hu, C. D. Nobes, A. Self, I. Jordens, C. S. Goodman, and A. Hall. 2001. Plexin-B semaphorin receptors interact directly with active Rac and regulate the actin cytoskeleton by activating Rho. Curr. Biol. 11:339-344.
17. Driessens, M. H., C. Olivo, K. Nagata, M. Inagaki, and J. G. Collard. 2002. B plexins activate Rho through PDZ-RhoGEF. FEBS Lett. 529:168-172.
18. Ebens, A., K. Brose, E. D. Leonardo, M. G. Hanson, Jr., F. Bladt, C. Birchmeier, B. A. Barres, and M. Tessier-Lavigne. 1996. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17:1157-1172.
19. Etienne-Manneville, S., and A. Hall. 2002. Rho GTPases in cell biology. Nature 420:629-635.
20. Fujisawa, H., T. Kitsukawa, A. Kawakami, S. Takagi, M. Shimizu, and T. Hirata. 1997. Roles of a neuronal cell-surface molecule, neuropilin, in nerve fiber fasciculation and guidance. Cell Tissue Res. 290:465-470.
21. Giordano, S., S. Corso, P. Conrotto, S. Artigiani, G. Gilestro, D. Barberis, L. Tamagnone, and P. M. Comoglio. 2002. The semaphorin 4D receptor controls invasive growth by coupling with Met. Nat. Cell. Biol. 4:720-724.
22. Hanke, J. H., J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, and P. A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271:695-70l.
23. Hanks, S. K., and T. R. Polte. 1997. Signaling through focal adhesion kinase. Bioessays 19:137-145.
24. Hu, H., T. F. Marton, and C. S. Goodman. 2001. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32:39-51.
25. Igishi, T., and J. S. Gutkind. 1998. Tyrosine kinases of the Src family participate in signaling to MAP kinase from both Gq and Gi-coupled receptors. Biochem. Biophys. Res. Commun. 244:5-10.
26. Kawakami, A., T. Kitsukawa, S. Takagi, and H. Fujisawa. 1996. Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J. Neurobiol. 29:1-17.
27. Kolodkin, A. L., D. V. Levengood, E. G. Rowe, Y. T. Tai, R. J. Giger, and D. D. Ginty. 1997. Neuropilin is a semaphorin III receptor. Cell 90:753-762.
28. Kolodkin, A. L., D. J. Matthes, and C. S. Goodman. 1993. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389-1399.
29. Kuwabara, K., T. Nakaoka, K. Sato, T. Nishishita, T. Sasaki, and N. Yamashita. 2004. Differential regulation of cell migration and proliferation through proline-rich tyrosine kinase 2 in endothelial cells. Endocrinology 145:3324-3330.
30. Maina, F., M. C. Hilton, R. Andres, S. Wyatt, R. Klein, and A. M. Davies. 1998. Multiple roles for hepatocyte growth factor in sympathetic neuron development. Neuron 20:835-846.
31. Merlot, S., and R. A. Firtel. 2003. Leading the way: directional sensing through phosphatidylinositol 3-kinase and other signaling pathways. J. Cell Sci. 116:3471-3478.
32. Miyazawa, K., T. Shimomura, D. Naka, and N. Kitamura. 1994. Proteolytic activation of hepatocyte growth factor in response to tissue injury. J. Biol. Chem. 269:8966-8970.
33. Neufeld, G., T. Cohen, N. Shraga, T. Lange, O. Kessler, and Y. Herzog. 2002. The neuropilins: multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis. Trends Cardiovasc. Med. 12:13-19.
34. Ohta, K., A. Mizutani, A. Kawakami, Y. Murakami, Y. Kasuya, S. Takagi, H. Tanaka, and H. Fujisawa. 1995. Plexin: a novel neuronal cell surface molecule that mediates cell adhesion via a homophilic binding mechanism in the presence of calcium ions. Neuron 14:1189-1199.
35. Oinuma, I., Y. Ishikawa, H. Katoh, and M. Negishi. 2004. The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 305:862-865.
36. Oinuma, I., H. Katoh, A. Harada, and M. Negishi. 2003. Direct interaction of Rnd1 with Plexin-B1 regulates PDZ-RhoGEF-mediated Rho activation by Plexin-Bl and induces cell contraction in COS-7 cells. J. Biol. Chem. 278:25671-25677.
37. Oinuma, I., H. Katoh, and M. Negishi. 2004. Molecular dissection of the semaphorin 4D receptor plexin-B1-stimulated R-Ras GTPase-activating protein activity and neurite remodeling in hippocampal neurons. J. Neurosci. 24:11473-11480.
38. Panetti, T. S. 2002. Tyrosine phosphorylation of paxillin, FAK, and p130CAS: effects on cell spreading and migration. Front. Biosci. 7:d143-d150.
39. Perrot, V., J. Vazquez-Prado, and J. S. Gutkind. 2002. Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J. Biol. Chem. 277:43115-43120.
40. Raftopoulou, M., and A. Hall. 2004. Cell migration: Rho GTPases lead the way. Dev. Biol. 265:23-32.
41. Raper, J. A. 2000. Semaphorins and their receptors in vertebrates and invertebrates. Curr. Opin. Neurobiol. 10:88-94.
42. Rocic, P., G. Govindarajan, A. Sabri, and P. A. Lucchesi. 2001. A role for PYK2 in regulation of ERK1/2 MAP kinases and PI 3-kinase by ANG II in vascular smooth muscle. Am. J. Physiol. Cell. Physiol. 280:C90-C99.
43. Rohm, B., A. Ottemeyer, M. Lohrum, and A. W. Puschel. 2000. Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech. Dev. 93:95-104.
44. Rohm, B., B. Rahim, B. Kleiber, I. Hovatta, and A. W. Puschel. 2000. The semaphorin 3A receptor may directly regulate the activity of small GTPases. FEBS Lett. 486:68-72.
45. Scheffzek, K., A. Lautwein, W. Kabsch, M. R. Ahmadian, and A. Wittinghofer. 1996. Crystal structure of the GTPase-activating domain of human p120GAP and implications for the interaction with Ras. Nature 384:591-596.
46. Schlaepfer, D. D., and T. Hunter. 1998. Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell. Biol. 8:151-157.
47. Serini, G., D. Valdembri, S. Zanivan, G. Morterra, C. Burkhardt, F. Caccavari, L. Zammataro, L. Primo, L. Tamagnone, M. Logan, M. Tessier-Lavigne, M. Taniguchi, A. W. Puschel, and F. Bussolino. 2003. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424:391-397.
48. Shoji, W., S. Isogai, M. Sato-Maeda, M. Obinata, and J. Y. Kuwada. 2003. Semaphorin3a1 regulates angioblast migration and vascular development in zebrafish embryos. Development 130:3227-3236.
49. Sieg, D. J., D. Ilic, K. C. Jones, C. H. Damsky, T. Hunter, and D. D. Schlaepfer. 1998. Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK-cell migration. EMBO J. 17:5933-5947.
50. Swiercz, J. M., R. Kuner, J. Behrens, and S. Offermanns. 2002. Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35:51-63.
51. Swiercz, J. M., R. Kuner, and S. Offermanns. 2004. Plexin-B1/RhoGEF- mediated RhoA activation involves the receptor tyrosine kinase ErbB-2. J. Cell Biol. 165:869-880.
52. Takahashi, T., A. Fournier, F. Nakamura, L. H. Wang, Y. Murakami, R. G. Kalb, H. Fujisawa, and S. M. Strittmatter. 1999. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59-69.
53. Tamagnone, L., S. Artigiani, H. Chen, Z. He, G. I. Ming, H. Song, A. Chedotal, M. L. Winberg, C. S. Goodman, M. Poo, M. Tessier-Lavigne, and P. M. Comoglio. 1999. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80.
54. Tamagnone, L., and P. M. Comoglio. 2000. Signalling by semaphorin receptors: cell guidance and beyond. Trends Cell. Biol. 10:377-383.
55. Tamagnone, L., and P. M. Comoglio. 2004. To move or not to move? Semaphorin signalling in cell migration. EMBO Rep. 5:356-361.
56. Tang, H., Q. Hao, T. Fitzgerald, T. Sasaki, E. J. Landon, and T. Inagami. 2002. Pyk2/CAKbeta tyrosine kinase activity-mediated angiogenesis of pulmonary vascular endothelial cells. J. Biol. Chem. 277:5441-5447.
57. Tessier-Lavigne, M., and C. S. Goodman. 1996, The molecular biology of axon guidance. Science 274:1123-1133.
58. Thomas, S. M., and J. S. Brugge. 1997. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13:513-609.
59. Trusolino, L., and P. M. Comoglio. 2002. Scatter-factor and semaphorin receptors: cell signalling for invasive growth. Nat. Rev. Cancer 2:289-300.
60. Ueki, K., D. A. Fruman, S. M. Brachmann, Y. H. Tseng, L. C. Cantley, and C. R. Kahn. 2002. Molecular balance between the regulatory and catalytic subunits of phosphoinositide 3-kinase regulates cell signaling and survival. Mol. Cell. Biol. 22:965-977.
61. Vikis, H. G., W. Li, and K. L. Guan. 2002. The plexin-B1/Rac interaction inhibits PAK activation and enhances Sema4D ligand binding. Genes Dev. 16:836-845.
62. Vikis, H. G., W. Li, Z. He, and K. L. Guan. 2000. The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc. Natl. Acad. Sci. USA 97:12457-12462.
63. Vlahos, C. J., W. F. Matter, K. Y. Hui, and R. F. Brown. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1- benzopyran-4-one (LY294002). J. Biol. Chem. 269:5241-5248.
64. Winberg, M. L., J. N. Noordermeer, L. Tamagnone, P. M. Comoglio, M. K. Spriggs, M. Tessier-Lavigne, and C. S. Goodman. 1998. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95:903-916.