Axon guidance factor netrin-1 and its receptors regulate angiogenesis after cerebral ischemia

Neuroscience Bulletin

Volumn 30, Issue 4, 2014, Pages 683-691

  Ding, Qiao ^a   Liao, Song Jie ^a   Yu, Jian ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

angiogenesis; cerebral ischemia; netrin 1; neuronal recovery

Indexed keywords

CELL SURFACE RECEPTOR; NERVE GROWTH FACTOR; NETRIN RECEPTORS; NETRIN-1; TUMOR SUPPRESSOR PROTEIN;

ANGIOGENESIS; ANIMAL; BRAIN; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL MOTION; CEREBROVASCULAR ACCIDENT; HUMAN; METABOLISM; NERVE FIBER; VASCULARIZATION;

ANIMALS; AXONS; BRAIN; BRAIN ISCHEMIA; CELL MOVEMENT; CEREBRAL INFARCTION; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE GROWTH FACTORS; RECEPTORS, CELL SURFACE; STROKE; TUMOR SUPPRESSOR PROTEINS;

EID: 84905962963     PISSN: 16737067     EISSN: 19958218     Source Type: Journal    
DOI: 10.1007/s12264-013-1441-9     Document Type: Article

References (74)

1. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, et al. Heart disease and stroke statistics - 2013 update: a report from the American Heart Association. Circulation 2013, 127: e6 -e245.
2. Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, Guidetti D, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008, 359: 1317-1329.
3. Liu Y, Stein E, Oliver T, Li Y, Brunken WJ, Koch M, et al. Novel role for Netrins in regulating epithelial behavior during lung branching morphogenesis. Curr Biol 2004, 14: 897-905. (Pubitemid 38800912)
4. De Breuck S, Lardon J, Rooman I, Bouwens L. Netrin-1 expression in fetal and regenerating rat pancreas and its effect on the migration of human pancreatic duct and porcine islet precursor cells. Diabetologia 2003, 46: 926-933. (Pubitemid 36961315)
5. Strizzi L, Mancino M, Bianco C, Raafat A, Gonzales M, Booth BW, et al. Netrin-1 can affect morphogenesis and differentiation of the mouse mammary gland. J Cell Physiol 2008, 216: 824-834.
6. Salminen M, Meyer BI, Bober E, Gruss P. Netrin 1 is required for semicircular canal formation in the mouse inner ear. Development 2000, 127: 13-22.
7. Mehlen P, Guenebeaud C. Netrin-1 and its dependence receptors as original targets for cancer therapy. Curr Opin Oncol 2010, 22: 46-54.
8. Ly NP, Komatsuzaki K, Fraser IP, Tseng AA, Prodhan P, Moore KJ, et al. Netrin-1 inhibits leukocyte migration in vitro and in vivo. Proc Natl Acad Sci U S A 2005, 102: 14729-14734. (Pubitemid 41457124)
9. Ranganathan PV, Jayakumar C, Mohamed R, Dong Z, Ramesh G. Netrin-1 regulates the inflammatory response of neutrophils and macrophages, and suppresses ischemic acute kidney injury by inhibiting COX-2-mediated PGE2 production. Kidney Int 2013, 83: 1087-1098.
10. Son TW, Yun SP, Yong MS, Seo BN, Ryu JM, Youn HY, et al. Netrin-1 protects hypoxia-induced mitochondrial apoptosis through HSP27 expression via DCC- and integrin alpha6beta4-dependent Akt, GSK-3beta, and HSF-1 in mesenchymal stem cells. Cell Death Dis 2013, 4: e563.
11. Reeves WB, Kwon O, Ramesh G. Netrin-1 and kidney injury. II. Netrin-1 is an early biomarker of acute kidney injury. Am J Physiol Renal Physiol 2008, 294: F731-738.
12. Ramesh G, Berg A, Jayakumar C. Plasma netrin-1 is a diagnostic biomarker of human cancers. Biomarkers 2011, 16: 172-180.
13. Bayat M, Baluchnejadmojarad T, Roghani M, Goshadrou F, Ronaghi A, Mehdizadeh M. Netrin-1 improves spatial memory and synaptic plasticity impairment following global ischemia in the rat. Brain Res 2012, 1452: 185-194.
14. Wu TW, Li WW, Li H. Netrin-1 attenuates ischemic stroke-induced apoptosis. Neuroscience 2008, 156: 475-482.
15. Lu H, Wang Y, Yuan F, Liu J, Zeng L, Yang GY. Overexpression of netrin-1 improves neurological outcomes in mice following transient middle cerebral artery occlusion. Front Med 2011, 5: 86-93.
16. Liao SJ, Gong Q, Chen XR, Ye LX, Ding Q, Zeng JS, et al. Netrin-1 rescues neuron loss by attenuating secondary apoptosis in ipsilateral thalamic nucleus following focal cerebral infarction in hypertensive rats. Neuroscience 2013, 231: 225-232.
17. Cirulli V, Yebra M. Netrins: beyond the brain. Nat Rev Mol Cell Biol 2007, 8: 296-306. (Pubitemid 46474658)
18. Bradford D, Cole SJ, Cooper HM. Netrin-1: diversity in development. Int J Biochem Cell Biol 2009, 41: 487-493.
19. Rajasekharan S, Kennedy TE. The netrin protein family. Genome Biol 2009, 10: 239.
20. Lai Wing Sun K, Correia JP, Kennedy TE. Netrins: versatile extracellular cues with diverse functions. Development 2011, 138: 2153-2169.
21. Eichmann A, M akinen T, Alitalo K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev 2005, 19: 1013-1021. (Pubitemid 40632446)
22. Engelkamp D. C loning of three mouse Unc5 genes and their expression patterns at mid-gestation. Mech Dev 2002, 118: 191-197. (Pubitemid 35292137)
23. Yang B, Peng G, Gao J. Expression of unc5 family genes in zebrafish brain during embryonic development. Gene Expr Patterns 2013, 13: 311-318.
24. Dakouane-Giudicelli M, Duboucher C, Fortemps J, Missey-Kolb H, Brule D, Giudicelli Y, et al. Characterization and expression of netrin-1 and its receptors UNC5B and DCC in human placenta. J Histochem Cytochem 2010, 58: 73-82.
25. Castets M, Coissieux MM, Delloye-Bourgeois C, Bernard L, Delcros JG, Bernet A, et al. Inhibition of endothelial cell apoptosis by netrin-1 during angiogenesis. Dev Cell 2009, 16: 614-620.
26. Navankasattusas S, Whitehead KJ, Suli A, Sorensen LK, Lim AH, Zhao J, et al. The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 2008, 135: 659-667. (Pubitemid 351405019)
27. Lu X, Le Noble F, Y uan L, Jiang Q, De Lafarge B, Sugiyama D, et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 2004, 432: 179-186. (Pubitemid 39545842)
28. Larrivee B, Freitas C, Trombe M, Lv X, Delafarge B, Yuan L, et al. Activation of the UNC5B receptor by Netrin-1 inhibits sprouting angiogenesis. Genes Dev 2007, 21: 2433-2447. (Pubitemid 47533561)
29. Corset V, Nguyen-Ba-Charvet KT, Forcet C, Moyse E, Chedotal A, Mehlen P. Netrin-1-mediated axon outgrowth and cAMP production requires interaction with adenosine A2b receptor. Nature 2000, 407: 747-750.
30. Stein E, Zou Y, Poo M, Tessier-Lavigne M. Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 2001, 291: 1976-1982. (Pubitemid 32217000)
31. McKenna WL, Wong-Staal C, Kim GC, Macias H, Hinck L, Bartoe JL. Netrin-1-independent adenosine A2b receptor activation regulates the response of axons to netrin-1 by controlling cell surface levels of UNC5A receptors. J Neurochem 2008, 104: 1081-1090. (Pubitemid 351143644)
32. Yebra M, Montgomery AM, Diaferia GR, Kaido T, Silletti S, Perez B, et al. Recognition of the neural chemoattractant Netrin-1 by integrins alpha6beta4 and alpha3beta1 regulates epithelial cell adhesion and migration. Dev Cell 2003, 5: 695-707. (Pubitemid 37362214)
33. Ishii N, Wadsworth WG, Stern BD, Culotti JG, Hedgecock EM. UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron 1992, 9: 873-881.
34. Serafini T, Kennedy TE, Ga lko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 1994, 78: 409-424. (Pubitemid 24250806)
35. Moon C, Ahn M, Jeong C, Kim H, Shin T. Immunohistochemical study of netrin-1 in the spinal cord with rat experimental autoimmune encephalomyelitis. Immunol Invest 2011, 40: 160-171.
36. Livesey FJ, Hunt SP. Netrin and netrin receptor expression in the embryonic mammalian nervous system suggests roles in retinal, striatal, nigral, and cerebellar development. Mol Cell Neurosci 1997, 8: 417-429. (Pubitemid 127796479)
37. Shatzmiller RA, Goldman JS, Simard-Emond L, Rymar V, Manitt C, Sadikot AF, et al. Graded expression of netrin-1 by specific neuronal subtypes in the adult mammalian striatum. Neuroscience 2008, 157: 621-636.
38. Dalvin S, Anselmo MA, Prodhan P, Komatsuzaki K, Schnitzer JJ, Kinane TB. Expression of Netrin-1 and its two receptors DCC and UNC5H2 in the developing mouse lung. Gene Expr Patterns 2003, 3: 279-283. (Pubitemid 36675993)
39. Chen J, Cai QP, Shen PJ, Yan RL, Wang CM, Yang DJ, et al. Netrin-1 protects against L-Arginine-induced acute pancreatitis in mice. PLoS One 2012, 7: e46201.
40. Srinivasan K, Strickland P, Val des A, Shin GC, Hinck L. Netrin-1/neogenin interaction stabilizes multipotent progenitor cap cells during mammary gland morphogenesis. Dev Cell 2003, 4: 371-382. (Pubitemid 36342362)
41. Llambi F, Causeret F, Bloch-Gall ego E, Mehlen P. Netrin-1 acts as a survival factor via its receptors UNC5H and DCC. EMBO J 2001, 20: 2715-2722. (Pubitemid 32938556)
42. Mei F, Christin Chong SY, Chan JR. Myelin-based inhibitors of oligodendrocyte myelination: clues from axonal growth and regeneration. Neurosci Bull 2013, 29: 177-188.
43. Serafini T, Colamarino SA, Leonard o ED, Wang H, Beddington R, Skarnes WC, et al. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 1996, 87: 1001-1014. (Pubitemid 26427984)
44. 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.
45. Carmeliet P, Tessier-Lavigne M. Comm on mechanisms of nerve and blood vessel wiring. Nature 2005, 436: 193 -200.
46. Dickson BJ. Molecular mechanisms of a xon guidance. Science 2002, 298: 1959-1964.
47. Klagsbrun M, Eichmann A. A role for ax on guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev 2005, 16: 535-548. (Pubitemid 41022016)
48. Semenza GL. Vasculogenesis, angiogenesi s, and arteriogenesis: mechanisms of blood vessel formation and remodeling. J Cell Biochem 2007, 102: 840-847. (Pubitemid 350036924)
49. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146: 873-887.
50. Chavakis E, Dimmeler S. Regulation of end othelial cell survival and apoptosis during angiogenesis. Arterioscler Thromb Vasc Biol 2002, 22: 887-893. (Pubitemid 34655213)
51. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011, 473: 298-307.
52. Park KW, Crouse D, Lee M, Karnik SK, Sorens en LK, Murphy KJ, et al. The axonal attractant Netrin-1 is an angiogenic factor. Proc Natl Acad Sci U S A 2004, 101: 16210-16215. (Pubitemid 39552824)
53. Wilson BD, Ii M, Park KW, Suli A, Sorensen L K, Larrieu-Lahargue F, et al. Netrins promote developmental and therapeutic angiogenesis. Science 2006, 313: 640-644. (Pubitemid 44201136)
54. Fan Y, Shen F, Chen Y, Hao Q, Liu W, Su H, et al. Overexpression of netrin-1 induces neovascularization in the adult mouse brain. J Cereb Blood Flow Metab 2008, 28: 1543-1551.
55. Nguyen A, Cai H. Netrin-1 induces angiogenesis via a DCC-dependent ERK1/2-eNOS feed-forward mechanism. Proc Natl Acad Sci U S A 2006, 103: 6530-6535.
56. Yang Y, Zou L, Wang Y, Xu KS, Zhang JX, Zhang J H. Axon guidance cue Netrin-1 has dual function in angiogenesis. Cancer Biol Ther 2007, 6: 743-748. (Pubitemid 47328356)
57. Krupinski J, Kaluza J, Kumar P, Kumar S, Wang JM. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 1994, 25: 1794-1798. (Pubitemid 24274974)
58. Sbarbati A, Pietra C, Baldassarri AM, Guerrini U, Ziviani L, Reggiani A, et al. The microvascular system in ischemic cortical lesions. Acta Neuropathol 1996, 92: 56-63. (Pubitemid 26192083)
59. Hayashi T, Noshita N, Sugawara T, Chan PH. Tempora l profile of angiogenesis and expression of related genes in the brain after ischemia. J Cereb Blood Flow Metab 2003, 23: 166-180. (Pubitemid 36188455)
60. Beck H, Acker T, Wiessner C, Allegrini PR, Plate KH. Expression of angiopoietin-1, angiopoietin-2, and tie receptors after middle cerebral artery occlusion in the rat. Am J Pathol 2000, 157: 1473-1483.
61. Tian HL, Chen H, Cui YH, Xu T, Zhou LF. Increased pr otein and mRNA expression of endostatin in the ischemic brain tissue of rabbits after middle cerebral artery occlusion. Neurosci Bull 2007, 23: 35-40. (Pubitemid 46392295)
62. Seevinck PR, Deddens LH, Dijkhuizen RM. Magnetic reso nance imaging of brain angiogenesis after stroke. Angiogenesis 2010, 13: 101-111.
63. Yu SW, Friedman B, Cheng Q, Lyden PD. Stroke-evoked an giogenesis results in a transient population of microvessels. J Cereb Blood Flow Metab 2007, 27: 755-763. (Pubitemid 46474610)
64. Wei L, Erinjeri JP, Rovainen CM, Woolsey TA. Collateral growth and angiogenesis around cortical stroke. Stroke 2001, 32: 2179-2184. (Pubitemid 32868119)
65. Le Magueresse C, Alfonso J, Bark C, Eliava M, Khrulev S, Monyer H. Subventricular zone-derived neuroblasts use vasculature as a scaffold to migrate radially to the cortex in neonatal mice. Cereb Cortex 2012, 22: 2285-2296.
66. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lind vall O. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 2007, 38: 3032-3039. (Pubitemid 350035699)
67. Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, et al. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells 2010, 28: 545-554.
68. Xiong Y, Mahmood A, Chopp M. Angiogenesis, neurogenesis and brain recovery of function following injury. Curr Opin Investig Drugs 2010, 11: 298-308.
69. Liman TG, Endres M. New vessels after stroke: postischemic n eovascularization and regeneration. Cerebrovasc Dis 2012, 33: 492-499.
70. Liu N, Huang H, Lin F, Chen A, Zhang Y, Chen R, et al. Effect s of treadmill exercise on the expression of netrin-1 and its receptors in rat brain after cerebral ischemia. Neuroscience 2011, 194: 349-358.
71. Tsuchiya A, Hayashi T, Deguchi K, Sehara Y, Yamashita T, Zhang H, et al. Expression of netrin-1 and its receptors DCC and neogenin in rat brain after ischemia. Brain Res 2007, 1159: 1-7. (Pubitemid 47058023)
72. Eichmann A, Thomas JL. Molecular parallels between neural and v ascular development. Cold Spring Harb Perspect Med 2013, 3: a006551.
73. Sun H, Le T, Chang TT, Habib A, Wu S, Shen F, et al. AAV-mediat ed netrin-1 overexpression increases peri-infarct blood vessel density and improves motor function recovery after experimental stroke. Neurobiol Dis 2011, 44: 73-83.
74. Lu H, Wang Y, He X, Yuan F, Lin X, Xie B, et al. Netrin-1 hypere xpression in mouse brain promotes angiogenesis and long-term neurological recovery after transient focal ischemia. Stroke 2012, 43: 838-843.