The axonal repellent Slit2 inhibits pericyte migration: Potential implications in angiogenesis

Experimental Cell Research

Volumn 318, Issue 4, 2012, Pages 371-378

  Guijarro Munoz I ^a   Cuesta, A M ^a   Alvarez Cienfuegos, A ^a   Geng, J G ^b   Alvarez Vallina, L ^a   Sanz, L ^a  

^a HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^b UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

Author keywords

Angiogenesis; Cell migration; Pericyte; Robo; Slit2

Indexed keywords

MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; ROUNDABOUT RECEPTOR; SLIT2 PROTEIN;

ANGIOGENESIS; ARTICLE; CELL INTERACTION; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MIGRATION INHIBITION; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA EXTRACTION; UMBILICAL VEIN ENDOTHELIAL CELL;

EID: 84856108037     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.12.005     Document Type: Article

References (37)

1. Ahmed Z., Bicknell R. Angiogenic signaling pathways. Methods Mol. Biol. 2009, 467(3-24):3-24.
2. Larrivee B., Freitas C., Suchting S., Brunet I., Eichmann A. Guidance of vascular development: lessons from the nervous system. Circ. Res. 2009, 104:428-441.
3. Ypsilanti A.R., Zagar Y., Chedotal A. Moving away from the midline: new developments for Slit and Robo. Development 2010, 137:1939-1952.
4. Legg J.A., Herbert J.M., Clissold P., Bicknell R. Slits and roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 2008, 11:13-21.
5. Wang B., Xiao Y., Ding B.B., Zhang N., Yuan X., Gui L., Qian K.X., Duan S., Chen Z., Rao Y., Geng J.G. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell. 2003, 4:19-29.
6. Yang X.M., Han H.X., Sui F., Dai Y.M., Chen M., Geng J.G. Slit-Robo signaling mediates lymphangiogenesis and promotes tumor lymphatic metastasis. Biochem. Biophys. Res. Commun. 2010, 396:571-577.
7. Bedell V.M., Yeo S.Y., Park K.W., Chung J., Seth P., Shivalingappa V., Zhao J., Obara T., Sukhatme V.P., Drummond I.A., Li D.Y., Ramchandran R. Roundabout4 is essential for angiogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:6373-6378.
8. Park K.W., Morrison C.M., Sorensen L.K., Jones C.A., Rao Y., Chien C.B., Wu J.Y., Urness L.D., Li D.Y. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Dev. Biol. 2003, 261:251-267.
9. Seth P., Lin Y., Hanai J., Shivalingappa V., Duyao M.P., Sukhatme V.P. Magic roundabout, a tumor endothelial marker: expression and signaling. Biochem. Biophys. Res. Commun. 2005, 332:533-541.
10. Jones C.A., London N.R., Chen H., Park K.W., Sauvaget D., Stockton R.A., Wythe J.D., Suh W., Larrieu-Lahargue F., Mukouyama Y.S., Lindblom P., Seth P., Frias A., Nishiya N., Ginsberg M.H., Gerhardt H., Zhang K., Li D.Y. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 2008, 14:448-453.
11. Jones C.A., Nishiya N., London N.R., Zhu W., Sorensen L.K., Chan A.C., Lim C.J., Chen H., Zhang Q., Schultz P.G., Hayallah A.M., Thomas K.R., Famulok M., Zhang K., Ginsberg M.H., Li D.Y. Slit2-Robo4 signaling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 2009, 11:1325-1331.
12. Marlow R., Binnewies M., Sorensen L.K., Monica S.D., Strickland P., Forsberg E.C., Li D.Y., Hinck L. Vascular Robo4 restricts proangiogenic VEGF signaling in breast. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10520-10525.
13. Suchting S., Heal P., Tahtis K., Stewart L.M., Bicknell R. Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. FASEB J. 2005, 19:121-123.
14. Sheldon H., Andre M., Legg J.A., Heal P., Herbert J.M., Sainson R., Sharma A.S., Kitajewski J.K., Heath V.L., Bicknell R. Active involvement of Robo1 and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors. FASEB J. 2009, 23:513-522.
15. Kaur S., Samant G.V., Pramanik K., Loscombe P.W., Pendrak M.L., Roberts D.D., Ramchandran R. Silencing of directional migration in roundabout4 knockdown endothelial cells. BMC Cell Biol. 2008, 9(61):61.
16. Kaur S., Castellone M.D., Bedell V.M., Konar M., Gutkind J.S., Ramchandran R. Robo4 signaling in endothelial cells implies attraction guidance mechanisms. J. Biol. Chem. 2006, 281:11347-11356.
17. Zhang B., Dietrich U.M., Geng J.G., Bicknell R., Esko J.D., Wang L. Repulsive axon guidance molecule Slit3 is a novel angiogenic factor. Blood 2009, 114:4300-4309.
18. Jain R.K. Molecular regulation of vessel maturation. Nat. Med. 2003, 9:685-693.
19. Liu D., Hou J., Hu X., Wang X., Xiao Y., Mou Y., De Leon H. Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ. Res. 2006, 98:480-489.
20. Ning Y., Sun Q., Dong Y., Xu W., Zhang W., Huang H., Li Q. Slit2-N inhibits PDGF-induced migration in rat airway smooth muscle cells: WASP and Arp2/3 involved. Toxicology 2011, 283:32-40.
21. Bergers G., Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro. Oncol. 2005, 7:452-464.
22. Armulik A., Abramsson A., Betsholtz C. Endothelial/pericyte interactions. Circ. Res. 2005, 97:512-523.
23. Sanz L., Santos-Valle P., Alonso-Camino V., Salas C., Serrano A., Vicario J.L., Cuesta A.M., Compte M., Sanchez-Martin D., Alvarez-Vallina L. Long-term in vivo imaging of human angiogenesis: critical role of bone marrow-derived mesenchymal stem cells for the generation of durable blood vessels. Microvasc. Res. 2008, 75:308-314.
24. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., Andriolo G., Sun B., Zheng B., Zhang L., Norotte C., Teng P.N., Traas J., Schugar R., Deasy B.M., Badylak S., Buhring H.J., Giacobino J.P., Lazzari L., Huard J., Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008, 3:301-313.
25. Raza A., Franklin M.J., Dudek A.Z. Pericytes and vessel maturation during tumor angiogenesis and metastasis. Am. J. Hematol. 2010, 85:593-598.
26. Ballabh P., Braun A., Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 2004, 16:1-13.
27. Nehls V., Denzer K., Drenckhahn D. Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res. 1992, 270:469-474.
28. Ozerdem U., Stallcup W.B. Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 2003, 6:241-249.
29. Anderson C.R., Ponce A.M., Price R.J. Immunohistochemical identification of an extracellular matrix scaffold that microguides capillary sprouting in vivo. J. Histochem. Cytochem. 2004, 52:1063-1072.
30. Gaengel K., Genove G., Armulik A., Betsholtz C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2009, 29:630-638.
31. Tole S., Mukovozov I.M., Huang Y.W., Magalhaes M.A., Yan M., Crow M.R., Liu G.Y., Sun C.X., Durocher Y., Glogauer M., Robinson L.A. The axonal repellent, Slit2, inhibits directional migration of circulating neutrophils. J. Leukoc. Biol. 2009, 86:1403-1415.
32. Ye B.Q., Geng Z.H., Ma L., Geng J.G. Slit2 regulates attractive eosinophil and repulsive neutrophil chemotaxis through differential srGAP1 expression during lung inflammation. J. Immunol. 2010, 185:6294-6305.
33. Guan H., Zu G., Xie Y., Tang H., Johnson M., Xu X., Kevil C., Xiong W.C., Elmets C., ao Y., Wu J.Y., Xu H. Neuronal repellent Slit2 inhibits dendritic cell migration and the development of immune responses. J. Immunol. 2003, 171:6519-6526.
34. Morlot C., Thielens N.M., Ravelli R.B., Hemrika W., Romijn R.A., Gros P., Cusack S., McCarthy A.A. Structural insights into the Slit-Robo complex. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14923-14928.
35. Koch A.W., Mathivet T., Larrivee B., Tong R.K., Kowalski J., Pibouin-Fragner L., Bouvree K., Stawicki S., Nicholes K., Rathore N., Scales S.J., Luis E., del Toro R., Freitas C., Breant C., Michaud A., Corvol P., Thomas J.L., Wu Y., Peale F., Watts R.J., Tessier-Lavigne M., Bagri A., Eichmann A. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev. Cell. 2011, 20:33-46.
36. London N.R., Zhu W., Bozza F.A., Smith M.C., Greif D.M., Sorensen L.K., Chen L., Kaminoh Y., Chan A.C., Passi S.F., Day C.W., Barnard D.L., Zimmerman G.A., Krasnow M.A., Li D.Y. Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza. Sci. Transl. Med. 2010, 2:23ra19.
37. Huminiecki L., Gorn M., Suchting S., Poulsom R., Bicknell R. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics 2002, 79:547-552.