Nitric oxide donor up-regulation of SDF1/CXCR4 and Ang1/Tie2 promotes neuroblast cell migration after stroke

Journal of Neuroscience Research

Volumn 87, Issue 1, 2009, Pages 86-95

  Cui, Xu ^a   Chen, Jieli ^a   Zacharek, Alex ^a   Roberts, Cynthia ^a   Yang, Yuping ^a   Chopp, Michael ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

Angiopoietin 1 Tie2; Neural progenitor cells; Nitric oxide donor; Stroke; Stromal cell derived factor 1 chemokine (CXC motif) receptor 4

Indexed keywords

3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; CHEMOKINE RECEPTOR CXCR4; DOUBLECORTIN; STROMAL CELL DERIVED FACTOR 1; STROMAL CELL DERIVED FACTOR 1ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL MIGRATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DRUG MECHANISM; MALE; MOUSE; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBVENTRICULAR ZONE; UPREGULATION;

ADULT STEM CELLS; ANALYSIS OF VARIANCE; ANGIOPOIETIN-1; ANIMALS; CELL MOVEMENT; CEREBRAL VENTRICLES; CHEMOKINE CXCL12; DISEASE MODELS, ANIMAL; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE DONORS; NITROSO COMPOUNDS; RECEPTOR, TIE-2; RECEPTORS, CXCR4; UP-REGULATION;

EID: 63049104675     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21836     Document Type: Article

References (55)

1. Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M, Pleasure SJ. 2002. The chemokine SDF1 regulates migration of dentate granule cells. Development 129:4249-4260.
2. Belmadani A, Tran PB, Ren D, Assimacopoulos S, Grove EA, Miller RJ. 2005. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J Neurosci 25:3995-4003.
3. Bernal GM, Peterson DA. 2004. Neural stem cells as therapeutic agents for age-related brain repair. Aging Cell 3:345-351. Bhakta S, Hong P, Koc O. 2006. The surface adhesion molecule, CXCR4 stimulates mesenchymal stem cell migration to stromal cell-derived factor-1 in vitro but does not decrease apoptosis under serum deprivation. Cardiovasc Revasc Med 7:19-24.
4. Bicker G. 2001. Nitric oidde: an unconventional messenger in the nervous system of an orthopteroid insect. Arch Insect Biochem Physiol 48:100-110.
5. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10:858-864.
6. Chen J, Li Y, Katakowski M, Chen X, Wang L, Lu D, Lu M, Gautam SC, Chopp M. 2003. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 73:778-786.
7. Chen J, Li Y, Zhang R, Katakowski M, Gautam SC, Xu Y, Lu M, Zhang Z, Chopp M. 2004. Combination therapy, of stroke in rats with a nitric oxide donor and human bone marrow stromal cells enhances angiogenesis and neurogenesis. Brain Res 1005:21-28.
8. Chen J, Zacharek A, Zhang C, Jiang H, Li Y, Roberts C, Lu M, Kapke A, Chopp M. 2005a. Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J Neurosci 25:2366-2375.
9. Chen J, Zhang C, Jiang H, Li Y, Zhang L, Robin A, Katakowski M, Lu M, Chopp M. 2005b. Atorvastatin induction of VEGF and BDNF promotes brain plasticity after stroke in mice. J Cereb Blood Flow Metab 25:281-290.
10. Chen J, Zacharek A, Li A, Zhang C, Ding J, Roberts C, Lu M, Kapke A, Chopp M. 2006a. Vascular endothelial growth factor mediates atorvastatin-induced mammalian achaete-scute homologue-1 gene expression and neuronal differentiation after stroke in retired breeder rats. Neuroscience 141:737-744.
11. Chen J, Zacharek A, Li Y, Li A, Wang L, Katakowski M, Roberts C, Lu M, Chopp M. 2006b. N-cadherin mediates nitric oxide-induced neurogenesis in young and retired breeder neurospheres. Neuroscience 140:377-388.
12. Cheng A, Wang S, Caij, Rao MS, Mattson MP. 2003. Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev Biol 258:319-333.
13. Cherla RP, Ganju RK. 2001. Stromal cell-derived factor 1 alpha-induced chemotaxis in T cells is mediated by nitric oxide signaling pathways. J Immunol 166:3067-3074.
14. Ciani E, Severi S, Contestabile A, Bartesaghi R. 2004. Nitric oxide negatively regulates proliferation and promotes neuronal differentiation through N-Myc down-regulation. J Cell Sci 117:4727-4737.
15. Cui X, Chen J, Zacharek A, Li Y, Roberts C, Kapke A, Savant-Bhonsale S, Chopp M. 2007. Nitric oxide donor up-regulation of stromal cell-derived factor-1/chemokine (CXC motif) receptor 4 enhances bone marrow stromal cell migration into ischemic brain after stroke. Stem Cells 25:2777-2785.
16. Darsalia V, Heldmann U, Lindvall O, Kokaia Z. 2005. Stroke-induced neurogenesis in aged brain. Stroke 36:1790-1795
17. Englund U, Bjorklund A, Wictorin K. 2002. Migration patterns and phenotypic differentiation of long-term expanded human neural progenitor cells after transplantation into the adult rat brain. Brain Res Dev Brain Res 134:123-141.
18. Gleeson JG, Lin PT, Flanagan LA, Walsh CA. 1999. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271.
19. Goldman S. 2005. Stem and progenitor cell-based therapy of the human central nervous system. Nat Biotechnol 23:862-871.
20. Hill WD, Hess DC, Martin-Studdard A, Carothers JJ, Zheng J, Hale D, Maeda M, Fagan SC, Carroll JE, Conway SJ. 2004. SDF-1 (CXCL12) is up-regulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 63:84-96.,
21. Hwang IK, Yoon YS, Choi JH, Yoo KY, Yi SS, Chung DW, Kim HJ, Kim CS, Do SG, Seong JK, Lee IS, Won MH. 2008. Doublecortin-immunoreactive neuronal precursors in the dentate gyrus of spontaneously hypertensive rats at various age stages: comparison with Sprague-Dawley rats. J Vet Med Sci/ Jpn Soc Vet Sci 70:373-377.
22. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD, Frenkel D, Li J, Sidman RL, Walsh CA, Snyder EY, Khoury SJ. 2004. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 101:18117-18122.
23. Ji JF, He BP, Dheen ST, Tay SS. 2004a. Expression of chemokine receptors CXCR4, CCR2, CCR5 and CX3CR1 in neural progenitor cells isolated from the subventricular zone of the adult rat brain. Neurosci Lett 355:236-240.
24. Ji JF, He BP, Dheen ST, Tay SS. 2004b. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells 22:415-427.
25. Kobayashi H, DeBusk LM, Babichev YO, Dumont DJ, Lin PC. 2006. Hepatocyte growth factor mediates angiopoietin-induced smooth muscle cell recruitment. Blood 108:1260-1266.
26. Kucia M, Reca k, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, Ratajczak J, Ratajczak MZ. 2005. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells 23:879-894.
27. Li Y, Jiang N, Powers C, Chopp M. 1998. Neuronal damage and plasticity identified by microtubule-associated protein 2, growth-associated protein 43, and cyclin D1 immunoreactivity after focal cerebral ischemia in rats. Stroke 29:1972-1980.
28. Metheny-Barlow LJ, Tian S, Hayes AJ, Li LY. 2004. Direct chemotactic action of angiopoietin-1 on mesenchymal cells in the presence of VEGF. Microvasc Res 68:221-230.
29. Moreno-Lopez B, Romero-Grimaldi C, Noval JA, Murillo-Carretero M, Matarredona ER, Estrada C. 2004. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J Neurosci 24:85-95.
30. Ni HT, Hu S, Sheng WS, Olson JM, Cheeran MC, Chan AS, Lokensgard JR, Peterson PK. 2004. High-level expression of functional chemokine receptor CXCR4 on human neural precursor cells. Brain Res Dev Brain Res 152:159-169.
31. +/-mice is associated with enhanced recovery of motor performance and increased neuroblast number following experimental stroke. J Neurosci Res 84:626-631.
32. Ohab JJ, Fleming S, Blesch A, Carmichael ST. 2006. A neurovascular niche for neurogenesis after stroke: J Neurosci 26:13007-13016.
33. Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, Goldman SA, Enikolopov G. 2003. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci U S A 100:9566-9571.
34. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. 2002. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802-813.
35. Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M. 2006. Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 26:125-134.
36. Seidel C, Bicker G. 2000. Nitric oxide and cGMP influence axonogenesis of antennal pioneer neurons. Development 127:4541-4549.
37. Stumm R, Kolodziej A, Schulz S, Kohtz JD, Hollt V. 2007. Patterns of SDF-1alpha and SDF-1gamma mRNAs, migration pathways, and phenotypes of CXCR4-expressing neurons in the developing rat telencephalon. J Comp Neurol 502:382-399.
38. Sun Y, Jin K, Xie L, Childs J, Mao XO, Logvinova A, Greenberg DA. 2003. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111:1843-1851.
39. Sunico CR, Portillo F, Gonzalez-Forero D, Moreno-Lopez B. 2005. Nitric oxide-directed synaptic remodeling in the adult mammal CNS. J Neurosci 25:1448-1458.
40. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. 1990. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10:290-293.
41. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z, Lindvall O. 2006. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24:739-747.
42. Tiveron MC, Rossel M, Moepps B, Zhang YL, Seidenfaden R, Favor J, Konig N, Cremer H. 2006. Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/ intermediate zone. J Neurosci 26:13273-13278.
43. Tran PB, Ren D, Veldhouse TJ, Miller RJ. 2004. Chemokine receptors are expressed widely by embryonic and adult neural progenitor cells. J Neurosci Res 76:20-34.
44. Tran PB, Banisadr G, Ren D, Chenn A, Miller RJ. 2007. Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. J Comp Neurol 500:1007-1033.
45. Truman JW, De Vente J, Ball EE. 1996. Nitric oxide-sensitive guanylate cyclase activity is associated with the maturational phase of neuronal development in insects. Development 122:3949-3958.
46. Watanabe MMW, Shirahama Y, Mitsuyama H, Oonakahara K, Noma S, Higashimoto I, Osame M, Arimura K. 2007. Dual effect of AMD3100, a CXCR4 antagonist, on bleomycin-induced lung inflammation. J Immunol 178:11.
47. Yamashita T; Ninomiya M, Hernandez Acosta P, Garcia-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K. 2006. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the poststroke adult striatum. J Neurosci 26:6627-6636.
48. Zacharek A, Chen J, Zhang C, Cui X, Roberts C, Jiang H, Teng H, Chopp M. 2006. Nitric oxide regulates angiopoietin1/Tie2 expression after stroke. Neurosci Lett 404:28-32.
49. Zacharek A, Chen J, Cui X, Li A, Li Y, Roberts C, Feng Y, Gao Q, Chopp M. 2007. Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J Cereb Blood Flow Metab 27:1684-1691.
50. Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, Lapointe M, Chopp M. 2001a. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50:602-611.
51. Zhang RL, Zhang ZG, Zhang L, Chopp M. 2001b. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105:33-41.
52. Zhang RL, Zhang L, Zhang ZG, Morris D, Jiang Q, Wang L, Zhang LJ, Chopp M. 2003. Migration and differentiation of adult rat subventricular zone progenitor cells transplanted into the adult rat striatum. Neuroscience 116:373-382.
53. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C, Chopp A. 2004. Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24:441-448.
54. Zhang RL, LeTourneau Y, Gregg SR, Wang Y, Toh Y, Robin AM, Zhang ZG, Chopp M. 2007a. Neuroblast division during migration toward the ischemic striatum: a study of dynamic migratory and proliferative characteristics of neuroblasts from the subventricular zone. J Neurosci 27:3157-3162.
55. Zhang RL, Zhang ZG, Chopp M. 2007b. Gene profiles within the adult subventricular zone niche: proliferation, differentiation and migration of neural progenitor cells in the ischemic brain. Curr Mol Med 7:459-462.