Slit2-Robo signaling: A novel regulator of vascular injury

Current Opinion in Nephrology and Hypertension

Volumn 22, Issue 4, 2013, Pages 445-451

  Yuen, Darren A ^a,b,c   Robinson, Lisa A ^a,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

Angiogenesis; Permeability; Roundabout; Slit2; Thrombosis

Indexed keywords

ROUNDABOUT RECEPTOR; SLIT2 PROTEIN;

ACTIN FILAMENT; ANGIOGENESIS; BLOOD VESSEL INJURY; BLOOD VESSEL WALL; CELL INTERACTION; CELL MIGRATION; CHRONIC KIDNEY DISEASE; HEMATOPOIETIC CELL; HUMAN; KIDNEY DISEASE; LIGAND BINDING; MEMBRANE PERMEABILITY; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; THROMBOSIS;

ANIMALS; BLOOD VESSELS; CAPILLARY PERMEABILITY; HEMATOPOIETIC STEM CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY DISEASES; NEOVASCULARIZATION, PATHOLOGIC; NERVE TISSUE PROTEINS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; VASCULAR DISEASES;

EID: 84879207547     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0b013e32836235f4     Document Type: Review

References (59)

1. Go AS, Chertow GM, Fan D, et al. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 2004; 351:1296-1305.
2. Bolton CH, Downs LG, Victory JG, et al. Endothelial dysfunction in chronic renal failure: roles of lipoprotein oxidation and pro-inflammatory cytokines. Nephrol Dial Transplant 2001; 16:1189-1197.
3. Kang DH, Kanellis J, Hugo C, et al. Role of the microvascular endothelium in progressive renal disease. J Am Soc Nephrol 2002; 13:806-816.
4. Amann K, Breitbach M, Ritz E, et al. Myocyte/capillary mismatch in the heart of uremic patients. J Am Soc Nephrol 1998; 9:1018-1022.
5. Amann K, Wiest G, Zimmer G, et al. Reduced capillary density in the myocardium of uremic rats: a stereological study. Kidney Int 1992; 42:1079-1085.
6. Massy ZA, Ivanovski O, Nguyen-Khoa T, et al. Uremia accelerates both atherosclerosis and arterial calcification in apolipoprotein E knockout mice. J Am Soc Nephrol 2005; 16:109-116.
7. Brose K, Bland KS, Wang KH, et al. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 1999; 96:795-806.
8. Kidd T, Bland K, Goodman C. Slit is the midline repellent for the Robo receptor in Drosophila. Cell 1999; 96:785-794.
9. Kidd T, Brose K, Mitchell KJ, et al. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 1998; 92:205-215.
10. Wu W, Wong K, Chen J, et al. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 1999; 400: 331-336.
11. Hohenester E. Structural insight into Slit-Robo signalling. Biochem Soc Trans 2008; 36:251-256.
12. Wong K, Ren XR, Huang YZ, et al. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 2001; 107:209-221.
13. Tole S, Mukovozov IM, Huang YW, et al. The axonal repellent, Slit2, inhibits directional migration of circulating neutrophils. J Leukoc Biol 2009; 86: 1403-1415.
14. Jones CA, Nishiya N, London NR, et al. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat Cell Biol 2009; 11:1325-1331.
15. Patel S, Huang YW, Reheman A, et al. The cell motility modulator Slit2 is a potent inhibitor of platelet function. Circulation 2012; 126:1385-1395.
16. Prasad A, Qamri Z, Wu J, et al. Slit-2/Robo-1 modulates the CXCL12/CXCR4-induced chemotaxis of T cells. J Leukoc Biol 2007; 82:465-476.
17. Bashaw GJ, Kidd T, Murray D, et al. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 2000; 101:703-715.
18. Ypsilanti AR, Zagar Y, Chedotal A. Moving away from the midline: new developments for Slit and Robo. Development 2010; 137:1939-1952.
19. Mommersteeg MT, Andrews WD, Ypsilanti AR, et al. Slit-roundabout signaling regulates the development of the cardiac systemic venous return and pericardium. Circ Res 2013; 112:465-475.
20. Fish JE, Wythe JD, Xiao T, et al. A Slit/miR-218/Robo regulatory loop is required during heart tube formation in zebrafish. Development 2011; 138:1409-1419.
21. Guijarro-Munoz I, Cuesta AM, Alvarez-Cienfuegos A, et al. The axonal repellent Slit2 inhibits pericyte migration: potential implications in angiogenesis. Exp Cell Res 2012; 318:371-378.
22. Huminiecki L, Gorn M, Suchting S, et al. 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.
23. Sheldon H, Andre M, Legg JA, et al. 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.
24. Liu D, Hou J, Hu X, et al. Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ Res 2006; 98:480-489.
25. Jones CA, London NR, Chen H, et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med 2008; 14:448-453.
26. Ye BQ, Geng ZH, Ma L, et al. Slit2 regulates attractive eosinophil and repulsive neutrophil chemotaxis through differential srGAP1 expression during lung inflammation. J Immunol 2010; 185:6294-6305.
27. Guan H, Zu G, Xie Y, et al. Neuronal repellent Slit2 inhibits dendritic cell migration and the development of immune responses. J Immunol 2003; 171:6519-6526.
28. Kang DH, Joly AH, Oh SW, et al. Impaired angiogenesis in the remnant kidney model: I. Potential role of vascular endothelial growth factor and thrombospondin-1. J Am Soc Nephrol 2001; 12:1434-1447.
29. Ribatti D, Crivellato E. 'Sprouting angiogenesis', a reappraisal. Development Biol 2012; 372:157-165.
30. Wang B, Xiao Y, Ding BB, et al. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 2003; 4:19-29.
31. Suchting S, Heal P, Tahtis K, et al. Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. FASEB J 2005; 19:121-123.
32. Koch AW, Mathivet T, Larrivee B, et al. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev Cell 2011; 20:33-46.
33. Marlow R, Binnewies M, Sorensen LK, et al. Vascular Robo4 restricts proangiogenic VEGF signaling in breast. Proc Natl Acad Sci U S A 2010; 107:10520-10525.
34. Bedell VM, Yeo SY, Park KW, et al. roundabout4 is essential for angiogenesis in vivo. Proc Natl Acad Sci U S A 2005; 102:6373-6378.
35. London NR, Li DY. Robo4-dependent Slit signaling stabilizes the vasculature during pathologic angiogenesis and cytokine storm. Curr Opin Hematol 2011; 18:186-190.
36. Dunaway CM, Hwang Y, Lindsley CW, et al. Cooperative signaling between Slit2 and Ephrin-A1 regulates a balance between angiogenesis and angiostasis. Mol Cell Biol 2011; 31:404-416.
37. Chi JT, Chang HY, Haraldsen G, et al. Endothelial cell diversity revealed by global expression profiling. Proc Natl Acad Sci U S A 2003; 100:10623-10628.
38. Obeidat M, Ballermann BJ. Glomerular endothelium: a porous sieve and formidable barrier. Exp Cell Res 2012; 318:964-972.
39. Dvorak HF, Brown LF, Detmar M, et al. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 1995; 146:1029-1039.
40. Lee WL, Slutsky AS. Sepsis and endothelial permeability. N Engl JMed 2010; 363:689-691.
41. London NR, Zhu W, Bozza FA, et al. Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza. Sci Transl Med 2010; 2:23ra19.
42. Dejana E, Orsenigo F, Lampugnani MG. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 2008; 121:2115-2122.
43. Hashimoto A, Hashimoto S, Ando R, et al. GEP100-Arf6-AMAP1-cortactin pathway frequently used in cancer invasion is activated by VEGFR2 to promote angiogenesis. PLoS ONE 2011; 6:e23359.
44. Zhu W, London NR, Gibson CC, et al. Interleukin receptor activates a MYD88-ARNO-ARF6 cascade to disrupt vascular stability. Nature 2012; 492:252-255.
45. Palacios F, Price L, Schweitzer J, et al. An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J 2001; 20:4973-4986.
46. Lindenmeyer MT, Eichinger F, Sen K, et al. Systematic analysis of a novel human renal glomerulus-enriched gene expression dataset. PLoS ONE 2010; 5:e11545.
47. Kanellis J, Garcia GE, Li P, et al. Modulation of inflammation by Slit protein in vivo in experimental crescentic glomerulonephritis. Am J Pathol 2004; 165:341-352.
48. Satchell SC, Anderson KL, Mathieson PW. Angiopoietin 1 and vascular endothelial growth factor modulate human glomerular endothelial cell barrier properties. J Am Soc Nephrol 2004; 15:566-574.
49. Gamble JR, Drew J, Trezise L, et al. Angiopoietin-1 is an antipermeability and anti-inflammatory agent in vitro and targets cell junctions. Circ Res 2000; 87:603-607.
50. Bates DO, Hillman NJ, Williams B, et al. Regulation of microvascular permeability by vascular endothelial growth factors. J Anat 2002; 200:581-597.
51. Deen WM, Lazzara MJ, Myers BD. Structural determinants of glomerular permeability. Am J Physiol Renal Physiol 2001; 281:F579-596.
52. Satchell SC, Tasman CH, Singh A, et al. Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF. Kidney Int 2006; 69:1633-1640.
53. Newby AC, Zaltsman AB. Molecular mechanisms in intimal hyperplasia. J Pathol 2000; 190:300-309.
54. Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 2005; 7:452-464.
55. Wu JY, Feng L, Park HT, et al. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 2001; 410:948-952.
56. Geutskens SB, Hordijk PL, van Hennik PB. The chemorepellent Slit3 promotes monocyte migration. J Immunol 2010; 185:7691-7698.
57. Chaturvedi S, Yuen DA, Bajwa A, et al. Slit2 prevents neutrophil recruitment and renal ischemia-reperfusion injury in mice. J Am Soc Nephrol 2013. (in press).
58. Croce K, Libby P. Intertwining of thrombosis and inflammation in atherosclerosis. Curr Opin Hematol 2007; 14:55-61.
59. Woulfe D, Jiang H, Morgans A, et al. Defects in secretion, aggregation, and thrombus formation in platelets from mice lacking Akt2. J Clin Invest 2004; 113:441-450.