Cellular connections, microenvironment and brain angiogenesis in diabetes: Lost communication signals in the post-stroke period

Brain Research

Volumn 1623, Issue , 2015, Pages 81-96

  Ergul, Adviye ^a,b,c   Valenzuela, John Paul ^b   Fouda, Abdelrahman Y ^a,c   Fagan, Susan C ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Angiogenesis; Diabetes; Stroke; Vascular restoration

Indexed keywords

ANGIOGENESIS; APOPTOSIS; BONE MARROW STROMA CELL; BRAIN BLOOD VESSEL; BRAIN CAPILLARY; CELL COMMUNICATION; CELL FUNCTION; CELL INTERACTION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; DIABETES MELLITUS; DIABETIC PATIENT; DIABETIC RETINOPATHY; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; GLIA CELL; HUMAN; IMMUNOCOMPETENT CELL; MEMBRANE MICROPARTICLE; NERVE CELL; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PERICYTE; PRIORITY JOURNAL; REVIEW; ANIMAL; BRAIN; NEOVASCULARIZATION (PATHOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; BRAIN; CELL COMMUNICATION; DIABETES MELLITUS; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; STROKE;

EID: 84941317467     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.02.045     Document Type: Review

References (191)

1. A. Abaci, and et al. Effect of diabetes mellitus on formation of coronary collateral vessels Circulation 99 1999 2239 2242
2. M. Abdelsaid, and et al. Metformin treatment in post-stroke period prevents nitrative stress and restores angiogenic signaling in the brain in diabetes Diabetes 2014 [Epub ahead of print]
3. M.M. Al-Gayyar, and et al. Thioredoxin interacting protein is a novel mediator of retinal inflammation and neurotoxicity Br. J. Pharmacol. 164 2011 170 180
4. A. Alhusban, and et al. AT1 receptor antagonism is proangiogenic in the brain: BDNF a novel mediator J. Pharmacol. Exp. Ther. 344 2013 348 359
5. American Diabetes Association, 2014. National Diabetes Fact Sheet. (http://www.diabetes.org/diabetes-statistics.jsp).
6. K. Arai, and E.H. Lo An oligovascular niche: cerebral endothelial cells promote the survival and proliferation of oligodendrocyte precursor cells J. Neurosci. 29 2009 4351 4355
7. A. Armulik, and et al. Pericytes regulate the blood-brain barrier Nature 468 2010 557 561
8. T. Arnold, and C. Betsholtz Correction: the importance of microglia in the development of the vasculature in the central nervous system Vasc. Cell 5 2013 12
9. D. Attwell, and et al. Glial and neuronal control of brain blood flow Nature 468 2010 232 243
10. Y.Y. Bai, and et al. Image-guided pro-angiogenic therapy in diabetic stroke mouse models using a multi-modal nanoprobe Theranostics 4 2014 787 797
11. B.A. Barres The mystery and magic of glia: a perspective on their roles in health and disease Neuron 60 2008 430 440
12. H. Beck, and et al. Cell type-specific expression of neuropilins in an MCA-occlusion model in mice suggests a potential role in post-ischemic brain remodeling J. Neuropathol. Exp. Neurol. 61 2002 339 350
13. R.D. Bell, and et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging Neuron 68 2010 409 427
14. S. Bocker-Meffert, and et al. Erythropoietin and VEGF promote neural outgrowth from retinal explants in postnatal rats Investig. Ophthalmol. Vis. Sci. 43 2002 2021 2026
15. D. Bonkowski, and et al. The CNS microvascular pericyte: pericyte-astrocyte crosstalk in the regulation of tissue survival Fluids Barriers CNS 8 2011 8
16. A. Brockington, and et al. Expression of vascular endothelial growth factor and its receptors in the central nervous system in amyotrophic lateral sclerosis J. Neuropathol. Exp. Neurol. 65 2006 26 36
17. M.A. Bruno, and A.C. Cuello Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade Proc. Natl. Acad. Sci. USA 103 2006 6735 6740
18. K. Buraczynska, and et al. Monocyte chemoattractant protein (MCP-1) A-2518G gene polymorphism in stroke patients with different comorbidities Clin. Biochem. 43 2010 1421 1426
19. I.R. Buschmann, and et al. GM-CSF: a strong arteriogenic factor acting by amplification of monocyte function Atherosclerosis 159 2001 343 356
20. I.R. Buschmann, and et al. Therapeutic induction of arteriogenesis in hypoperfused rat brain via granulocyte-macrophage colony-stimulating factor Circulation 108 2003 610 615
21. C.L. Carr, and et al. Dysregulated selectin expression and monocyte recruitment during ischemia-related vascular remodeling in diabetes mellitus Arterioscler. Thromb. Vasc. Biol. 31 2011 2526 2533
22. J. Chen, and et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats Stroke 32 2001 1005 1011
23. J. Chen, and et al. Circulating endothelial progenitor cells and cellular membrane microparticles in db/db diabetic mouse: possible implications in cerebral ischemic damage Am. J. Physiol. Endocrinol. Metab. 301 2011 E62 E71
24. J. Chen, and et al. Adverse effects of bone marrow stromal cell treatment of stroke in diabetic rats Stroke 42 2011 3551 3558
25. J. Chen, and et al. Transfusion of CXCR4-primed endothelial progenitor cells reduces cerebral ischemic damage and promotes repair in db/db diabetic mice PLoS One 7 2012 e50105
26. X. Cui, and et al. Angiopoietin/Tie2 pathway mediates type 2 diabetes induced vascular damage after cerebral stroke Neurobiol. Dis. 43 2011 285 292
27. T. Dalkara, Y. Gursoy-Ozdemir, and M. Yemisci Brain microvascular pericytes in health and disease Acta Neuropathol. 122 2011 1 9
28. D. Dewar, S.M. Underhill, and M.P. Goldberg Oligodendrocytes and ischemic brain injury J. Cereb. Blood Flow Metab. 23 2003 263 274
29. L. Diaz-Flores, and et al. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche Histol. Histopathol. 24 2009 909 969
30. P. Dore-Duffy, and J.C. LaManna Physiologic angiodynamics in the brain Antioxid. Redox Signal. 9 2007 1363 1371
31. P. Dore-Duffy Pericytes and adaptive angioplasticity: the role of tumor necrosis factor-like weak inducer of apoptosis (TWEAK) Methods Mol. Biol. 1135 2014 35 52
32. D.J. Dumont, and et al. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development Dev. Dyn. 203 1995 80 92
33. S. Ejaz, and et al. Importance of pericytes and mechanisms of pericyte loss during diabetes retinopathy Diabetes Obes. Metab. 10 2008 53 63
34. M. Enge, and et al. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy EMBO J. 21 2002 4307 4316
35. A. Ergul, A. Alhusban, and S.C. Fagan Angiogenesis: a harmonized target for recovery after stroke Stroke 43 2012 2270 2274
36. A. Ergul, and et al. Cerebrovascular complications of diabetes: focus on stroke Endocr. Metab. Immune Disord. Drug Targets 12 2012 148 158
37. A. Ergul, and et al. Cerebral neovascularization in diabetes: implications for stroke recovery and beyond J. Cereb. Blood Flow Metab. 2014
38. L. Erskine, and et al. VEGF signaling through neuropilin 1 guides commissural axon crossing at the optic chiasm Neuron 70 2011 951 965
39. A. Fantin, and et al. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction Blood 116 2010 829 840
40. J.R. Faulkner, and et al. Reactive astrocytes protect tissue and preserve function after spinal cord injury J. Neurosci. 24 2004 2143 2155
41. B. Feng, and et al. Circulating level of microparticles and their correlation with arterial elasticity and endothelium-dependent dilation in patients with type 2 diabetes mellitus Atherosclerosis 208 2010 264 269
42. J.A. Forsythe, and et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1 Mol. Cell Biol. 16 1996 4604 4613
43. S.F. Freedman, and D.L. Hatchell Enhanced superoxide radical production by stimulated polymorphonuclear leukocytes in a cat model of diabetes Exp. Eye Res. 55 1992 767 773
44. C.G. Fulmer, and et al. Astrocyte-derived BDNF supports myelin protein synthesis after cuprizone-induced demyelination J. Neurosci. 34 2014 8186 8196
45. K.A. Gallagher, and et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha J. Clin. Invest. 117 2007 1249 1259
46. C.M. Garcia, and et al. Endothelial cell-astrocyte interactions and TGF beta are required for induction of blood-neural barrier properties Brain Res. Dev. Brain Res. 152 2004 25 38
47. J.M. Gensert, and J.E. Goldman Endogenous progenitors remyelinate demyelinated axons in the adult CNS Neuron 19 1997 197 203
48. P. Geraldes, and et al. Activation of PKC-delta and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy Nat. Med. 15 2009 1298 1306
49. H. Gerhardt, and C. Betsholtz Endothelial-pericyte interactions in angiogenesis Cell Tissue Res. 314 2003 15 23
50. H. Gerhardt, and et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia J. Cell Biol. 161 2003 1163 1177
51. C. Giaume, and et al. Glia: the fulcrum of brain diseases Cell Death Differ. 14 2007 1324 1335
52. Y. Gonzalez, and et al. High glucose concentrations induce TNF-alpha production through the down-regulation of CD33 in primary human monocytes BMC Immunol. 13 2012 19
53. W. Guan, and et al. Vascular protection by angiotensin receptor antagonism involves differential VEGF expression in both hemispheres after experimental stroke PLoS One 6 2011 e24551
54. S. Guo, and et al. Neuroprotection via matrix-trophic coupling between cerebral endothelial cells and neurons Proc. Natl. Acad. Sci. USA 105 2008 7582 7587
55. J. Hai, and et al. Vascular endothelial growth factor expression and angiogenesis induced by chronic cerebral hypoperfusion in rat brain Neurosurgery 53 2003 963 970 (discussion 970-2)
56. C.N. Hall, and et al. Capillary pericytes regulate cerebral blood flow in health and disease Nature 508 2014 55 60
57. H.P. Hammes, H.J. Federoff, and M. Brownlee Nerve growth factor prevents both neuroretinal programmed cell death and capillary pathology in experimental diabetes Mol. Med. 1 1995 527 534
58. E. Hansson, and L. Ronnback Glial neuronal signaling in the central nervous system FASEB J. 17 2003 341 348
59. T.E. Hartog, and et al. Brain-derived neurotrophic factor signaling in the HVC is required for testosterone-induced song of female canaries J. Neurosci. 29 2009 15511 15519
60. Y. Hayon, and et al. Platelet microparticles induce angiogenesis and neurogenesis after cerebral ischemia Curr. Neurovasc. Res. 9 2012 185 192
61. Y. Hayon, and et al. Platelet microparticles promote neural stem cell proliferation, survival and differentiation J. Mol. Neurosci. 47 2012 659 665
62. N. Hellbach, and et al. Neural deletion of Tgfbr2 impairs angiogenesis through an altered secretome Hum. Mol. Genet. 23 2014 6177 6190
63. M.T. Heneka, and et al. Neuroinflammatory processes in Alzheimers disease J. Neural Transm. 117 2010 919 947
64. D.M. Hermann, A.M. Buga, and A. Popa-Wagner Neurovascular remodeling in the aged ischemic brain J. Neural Transm. 2013 Epub ahead of print] DOI 10.1007/s00702-013-1148-0
65. J. Hill, and et al. Emerging roles of pericytes in the regulation of the neurovascular unit in health and disease J. Neuroimmune Pharmacol. 9 2014 591 605
66. I.E. Hoefer, J.J. Piek, and G. Pasterkamp Pharmaceutical interventions to influence arteriogenesis: new concepts to treat ischemic heart disease Curr. Med. Chem. 13 2006 979 987
67. J.P. Ingraham, and et al. Aging reduces hypoxia-induced microvascular growth in the rodent hippocampus J. Gerontol. Ser. A Biol. Sci. Med. Sci. 63 2008 12 20
68. T. Ishibashi, and et al. Astrocytes promote myelination in response to electrical impulses Neuron 49 2006 823 832
69. H. Ishikawa, and et al. Vasculogenesis in experimental stroke after human cerebral endothelial cell transplantation Stroke 44 2013 3473 3481
70. W.D. Ito, and et al. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion Circ. Res. 80 1997 829 837
71. Y. Itoh, and et al. Astrocytes and pericytes cooperatively maintain a capillary-like structure composed of endothelial cells on gel matrix Brain Res. 1406 2011 74 83
72. K.L. Jin, and et al. Induction of vascular endothelial growth factor and hypoxia-inducible factor-1alpha by global ischemia in rat brain Neuroscience 99 2000 577 585
73. K. Jin, and et al. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat Proc. Natl. Acad. Sci. USA 98 2001 4710 4715
74. K. Jin, and et al. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo Proc. Natl. Acad. Sci. USA 99 2002 11946 11950
75. R. Jin, G. Yang, and G. Li Inflammatory mechanisms in ischemic stroke: role of inflammatory cells J. Leukoc. Biol. 87 2010 779 789
76. L. Jing, and et al. Temporal profile of astrocytes and changes of oligodendrocyte-based myelin following middle cerebral artery occlusion in diabetic and non-diabetic rats Int. J. Biol. Sci. 9 2013 190 199
77. I. Jojart, and et al. Immunoelectronhistochemical evidence for innervation of brain microvessels by vasopressin-immunoreactive neurons in the rat Neurosci. Lett. 51 1984 259 264
78. J.S. Joyal, and et al. Ischemic neurons prevent vascular regeneration of neural tissue by secreting semaphorin 3A Blood 117 2011 6024 6035
79. M. Karima, and et al. Enhanced superoxide release and elevated protein kinase C activity in neutrophils from diabetic patients: association with periodontitis J. Leukoc. Biol. 78 2005 862 870
80. J.B. Kearney, and et al. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis Blood 103 2004 4527 4535
81. P. Kermani, and et al. Neurotrophins promote revascularization by local recruitment of TrkB+ endothelial cells and systemic mobilization of hematopoietic progenitors J. Clin. Invest. 115 2005 653 663
82. A.A. Khaibullina, J.M. Rosenstein, and J.M. Krum Vascular endothelial growth factor promotes neurite maturation in primary CNS neuronal cultures Brain Res. Dev. Brain Res. 148 2004 59 68
83. H. Kim, and et al. Paracrine and autocrine functions of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in brain-derived endothelial cells J. Biol. Chem. 279 2004 33538 33546
84. J. Kim, and et al. Different prognostic value of white blood cell subtypes in patients with acute cerebral infarction Atherosclerosis 222 2012 464 467
85. E. Kim, A.T. Tolhurst, and S. Cho Deregulation of inflammatory response in the diabetic condition is associated with increased ischemic brain injury J. Neuroinflamm. 11 2014 83
86. M. Klagsbrun, and A. Eichmann A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis Cytokine Growth Factor Rev. 16 2005 535 548
87. R. Kumari, and et al. Impaired wound healing after cerebral hypoxia-ischemia in the diabetic mouse J. Cereb. Blood Flow Metab. 27 2007 710 718
88. U. Kummer, and et al. Elevated glucose concentrations promote receptor-independent activation of adherent human neutrophils: an experimental and computational approach Biophys. J. 92 2007 2597 2607
89. N. Kuriyama, and et al. Evaluation of factors associated with elevated levels of platelet-derived microparticles in the acute phase of cerebral infarction Clin. Appl. Thromb. Hemost. 16 2010 26 32
90. M. Lalancette-Hebert, and et al. Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury J. Neurosci. 32 2012 10383 10395
91. S.W. Lee, and et al. SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier Nat. Med. 9 2003 900 906
92. H.S. Lee, and et al. Brain angiogenesis in developmental and pathological processes: regulation, molecular and cellular communication at the neurovascular interface FEBS J. 276 2009 4622 4635
93. Y. Lee, and et al. Therapeutically targeting neuroinflammation and microglia after acute ischemic stroke Biomed. Res. Int. 2014 2014 297241
94. F. Lennmyr, and et al. Expression of vascular endothelial growth factor (VEGF) and its receptors (Flt-1 and Flk-1) following permanent and transient occlusion of the middle cerebral artery in the rat J. Neuropathol. Exp. Neurol. 57 1998 874 882
95. F. Lennmyr, and et al. Vascular endothelial growth factor gene expression in middle cerebral artery occlusion in the rat Acta Anaesthesiol. Scand. 49 2005 488 493
96. A.F. Li, and et al. High glucose alters connexin 43 expression and gap junction intercellular communication activity in retinal pericytes Invest. Ophthalmol. Vis. Sci. 44 2003 5376 5382
97. S.F. Li, and et al. Recombinant adeno-associated virus serotype 1-vascular endothelial growth factor promotes neurogenesis and neuromigration in the subventricular zone and rescues neuronal function in ischemic rats Neurosurgery 65 2009 771 779 (discussion 779)
98. J. Li, and et al. Neurovascular recovery via co-transplanted neural and vascular progenitors leads to improved functional restoration after ischemic stroke in rats Stem Cell Rep. 3 2014 101 114
99. W. Li, and et al. Adaptive cerebral neovascularization in a model of type 2 diabetes: relevance to focal cerebral ischemia Diabetes 59 2010 228 235
100. J. Li, and et al. SMAD4-mediated WNT signaling controls the fate of cranial neural crest cells during tooth morphogenesis Development 138 2011 1977 1989
101. W. Li, and et al. Comparative analysis of the neurovascular injury and functional outcomes in experimental stroke models in diabetic Goto-Kakizaki rats Brain Res. 1541 2013 106 114
102. Y.N. Li, and et al. Ischemic neurons activate astrocytes to disrupt endothelial barrier via increasing VEGF expression J. Neurochem. 129 2014 120 129
103. Y. Li, and et al. Ephrin-A3 and ephrin-A4 contribute to microglia-induced angiogenesis in brain endothelial cells Anat. Rec. (Hoboken) 297 2014 1908 1918
104. Y. Li, and et al. The role of astrocytes in mediating exogenous cell-based restorative therapy for stroke Glia 62 2014 1 16
105. J. Liauw, and et al. Thrombospondins 1 and 2 are necessary for synaptic plasticity and functional recovery after stroke J. Cereb. Blood Flow Metab. 28 2008 1722 1732
106. S. Liebner, C.J. Czupalla, and H. Wolburg Current concepts of blood-brain barrier development Int. J. Dev. Biol. 55 2011 467 476
107. T.N. Lin, and et al. Differential regulation of thrombospondin-1 and thrombospondin-2 after focal cerebral ischemia/reperfusion Stroke 34 2003 177 186
108. O.R. Lindberg, A. Brederlau, and H.G. Kuhn Epidermal growth factor treatment of the adult brain subventricular zone leads to focal microglia/macrophage accumulation and angiogenesis Stem Cell Rep. 2 2014 440 448
109. Z. Liu, and et al. Higher numbers of circulating endothelial progenitor cells in stroke patients with intracranial arterial stenosis BMC Neurol. 13 2013 161
110. Z. Liu, and et al. Beneficial effects of gfap/vimentin reactive astrocytes for axonal remodeling and motor behavioral recovery in mice after stroke Glia 62 2014 2022 2033
111. C. Lopez-Lopez, D. LeRoith, and I. Torres-Aleman Insulin-like growth factor I is required for vessel remodeling in the adult brain Proc. Natl. Acad. Sci. USA 101 2004 9833 9838
112. A. Louissaint Jr.; and et al. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain Neuron 34 2002 945 960
113. H. Lu, and et al. Overexpression of netrin-1 improves neurological outcomes in mice following transient middle cerebral artery occlusion Front. Med 5 2011 86 93
114. H. Lu, and et al. Netrin-1 hyperexpression in mouse brain promotes angiogenesis and long-term neurological recovery after transient focal ischemia Stroke 43 2012 838 843
115. R. Mamluk, and et al. Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain J. Biol. Chem. 277 2002 24818 24825
116. J. Marti-Fabregas, and et al. Endothelial progenitor cells in acute ischemic stroke Brain Behav. 3 2013 649 655
117. M. Masuda, and et al. Decreased fluidity of polymorphonuclear leukocyte membrane in streptozocin-induced diabetic rats Diabetes 39 1990 466 470
118. Y. Matsuo, and et al. Correlation between myeloperoxidase-quantified neutrophil accumulation and ischemic brain injury in the rat. Effects of neutrophil depletion Stroke 25 1994 1469 1475
119. S.F. Mause, and C. Weber Microparticles: protagonists of a novel communication network for intercellular information exchange Circ. Res. 107 2010 1047 1057
120. M. Mazzanti, J.Y. Sul, and P.G. Haydon Glutamate on demand: astrocytes as a ready source Neuroscientist 7 2001 396 405
121. H.Q. Miao, and et al. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165 J. Cell Biol. 146 1999 233 242
122. I. Micu, and et al. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia Nature 439 2006 988 992
123. O. Morel, and et al. Sustained elevated amounts of circulating procoagulant membrane microparticles and soluble GPV after acute myocardial infarction in diabetes mellitus Thromb. Haemost. 91 2004 345 353
124. D. Navaratna, and et al. Mechanisms and targets for angiogenic therapy after stroke Cell Adhes. Migr. 3 2009 216 223
125. D. Navaratna, and et al. Cerebrovascular degradation of TRKB by MMP9 in the diabetic brain J. Clin. Invest. 123 2013 3373 3377
126. S. Nomura, and et al. Platelet-derived microparticles may influence the development of atherosclerosis in diabetes mellitus Atherosclerosis 116 1995 235 240
127. S. Nomura Dynamic role of microparticles in type 2 diabetes mellitus Curr. Diabetes Rev. 5 2009 245 251
128. N. Ogata, and et al. Increased levels of platelet-derived microparticles in patients with diabetic retinopathy Diabetes Res. Clin. Pract. 68 2005 193 201
129. N. Ogata, and et al. Elevation of monocyte-derived microparticles in patients with diabetic retinopathy Diabetes Res. Clin. Pract. 73 2006 241 248
130. S. Omoto, and et al. Significance of platelet-derived microparticles and activated platelets in diabetic nephropathy Nephron 81 1999 271 277
131. U. Ozerdem, and W.B. Stallcup Early contribution of pericytes to angiogenic sprouting and tube formation Angiogenesis 6 2003 241 249
132. J. Panes, and et al. Diabetes exacerbates inflammatory responses to ischemia-reperfusion Circulation 93 1996 161 167
133. K.W. Park, and et al. The axonal attractant Netrin-1 is an angiogenic factor Proc. Natl. Acad. Sci. USA 101 2004 16210 16215
134. J.A. Park, and et al. Meteorin regulates angiogenesis at the gliovascular interface Glia 56 2008 247 258
135. S.W. Park, and et al. Angiopoietin 2 induces pericyte apoptosis via alpha3beta1 integrin signaling in diabetic retinopathy Diabetes 63 2014 3057 3068
136. M. Poittevin Diabetic microangiopathy: impact of impaired cerebral vasoreactivity and delayed angiogenesis after permanent middle cerebral artery occlusion on stroke damage and cerebral repair in mice Diabetes 64 3 2015 999 1010
137. R. Prakash, and et al. Enhanced cerebral but not peripheral angiogenesis in the Goto-Kakizaki model of type 2 diabetes involves VEGF and peroxynitrite signaling Diabetes 61 2012 1533 1542
138. R. Prakash, and et al. Cerebral neovascularization and remodeling patterns in two different models of type 2 diabetes PLoS One 8 2013 e56264
139. R. Prakash, and et al. Vascularization pattern after ischemic stroke is different in control versus diabetic rats: relevance to stroke recovery Stroke 44 2013 2875 2882
140. C.J. Price, and et al. Cerebral neutrophil recruitment, histology, and outcome in acute ischemic stroke: an imaging-based study Stroke 35 2004 1659 1664
141. B.R. Ransom, and C.B. Ransom Astrocytes: multitalented stars of the central nervous system Methods Mol. Biol. 814 2012 3 7
142. S. Rasika, F. Nottebohm, and A. Alvarez-Buylla Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries Proc. Natl. Acad. Sci. USA 91 1994 7854 7858
143. P. Rieckmann, and B. Engelhardt Building up the blood-brain barrier Nat. Med. 9 2003 828 829
144. L. Ritter, and et al. Exaggerated neutrophil-mediated reperfusion injury after ischemic stroke in a rodent model of type 2 diabetes Microcirculation 18 2011 552 561
145. A. Rosell, and et al. Factors secreted by endothelial progenitor cells enhance neurorepair responses after cerebral ischemia in mice PLoS One 8 2013 e73244
146. J.M. Rosenstein, and et al. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons J. Neurosci. 23 2003 11036 11044
147. L.L. Rubin, and et al. A cell culture model of the blood-brain barrier J. Cell Biol. 115 1991 1725 1735
148. C. Ruhrberg Growing and shaping the vascular tree: multiple roles for VEGF Bioessays 25 2003 1052 1060
149. C. Ruiz de Almodovar, and et al. Matrix-binding vascular endothelial growth factor (VEGF) isoforms guide granule cell migration in the cerebellum via VEGF receptor Flk1 J. Neurosci. 30 2010 15052 15066
150. C. Ruiz de Almodovar, and et al. VEGF mediates commissural axon chemoattraction through its receptor Flk1 Neuron 70 2011 966 978
151. I. Sa-Pereira, D. Brites, and M.A. Brito Neurovascular unit: a focus on pericytes Mol. Neurobiol. 45 2012 327 347
152. C. Schmidt-Lucke, and et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair Circulation 111 2005 2981 2987
153. F. Shalaby, and et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice Nature 376 1995 62 66
154. L.Y. Shan, and et al. Platelet-derived microparticles are implicated in remote ischemia conditioning in a rat model of cerebral infarction CNS Neurosci. Ther. 19 2013 917 925
155. Y. Shiga, and et al. Neutrophil as a mediator of ischemic edema formation in the brain Neurosci. Lett. 125 1991 110 112
156. J.W. Shin, R. Huggenberger, and M. Detmar Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis Blood 112 2008 2318 2326
157. W.F. Silverman, and et al. Vascular, glial and neuronal effects of vascular endothelial growth factor in mesencephalic explant cultures Neuroscience 90 1999 1529 1541
158. T. Sobrino, and et al. The increase of circulating endothelial progenitor cells after acute ischemic stroke is associated with good outcome Stroke 38 2007 2759 2764
159. T. Sobrino, and et al. Increased levels of circulating endothelial progenitor cells in patients with ischaemic stroke treated with statins during acute phase Eur. J. Neurol. 19 2012 1539 1546
160. W.E. Sonntag, and et al. Alterations in insulin-like growth factor-1 gene and protein expression and type 1 insulin-like growth factor receptors in the brains of ageing rats Neuroscience 88 1999 269 279
161. A.N. Stratman, and et al. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation Blood 114 2009 5091 5101
162. H. Sun, and et al. AAV-mediated netrin-1 overexpression increases peri-infarct blood vessel density and improves motor function recovery after experimental stroke Neurobiol. Dis. 44 2011 73 83
163. V. Tchaikovski, and et al. Diabetes mellitus activates signal transduction pathways resulting in vascular endothelial growth factor resistance of human monocytes Circulation 120 2009 150 159
164. K. Todo, and et al. Granulocyte-macrophage colony-stimulating factor enhances leptomeningeal collateral growth induced by common carotid artery occlusion Stroke 39 2008 1875 1882
165. L. Tolosa, and et al. Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase J. Neurochem. 105 2008 1080 1090
166. N.W. Tsai, and et al. The association between circulating endothelial progenitor cells and outcome in different subtypes of acute ischemic stroke Clin. Chim. Acta 427 2014 6 10
167. G. Tsimerman, and et al. Involvement of microparticles in diabetic vascular complications Thromb. Haemost. 106 2011 310 321
168. E.M. Ullian, and et al. Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture Mol. Cell. Neurosci. 25 2004 241 251
169. X. Urra, and et al. Monocyte subtypes predict clinical course and prognosis in human stroke J. Cereb. Blood Flow Metab. 29 2009 994 1002
170. D. Virgintino, and et al. An intimate interplay between precocious, migrating pericytes and endothelial cells governs human fetal brain angiogenesis Angiogenesis 10 2007 35 45
171. J. Waltenberger Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications Cardiovasc. Res. 49 2001 554 560
172. L. Wang, and et al. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats Stroke 35 2004 1732 1737
173. Y.Q. Wang, and et al. VEGF overexpression enhances striatal neurogenesis in brain of adult rat after a transient middle cerebral artery occlusion J. Neurosci. Res. 85 2007 73 82
174. N. Werner, and et al. Circulating endothelial progenitor cells and cardiovascular outcomes N. Engl. J. Med. 353 2005 999 1007
175. U.V. Wesley, and et al. Galectin-3 enhances angiogenic and migratory potential of microglial cells via modulation of integrin linked kinase signaling Brain Res. 1496 2013 1 9
176. B. Wierusz-Wysocka, and et al. Evidence of polymorphonuclear neutrophils (PMN) activation in patients with insulin-dependent diabetes mellitus J. Leukoc. Biol. 42 1987 519 523
177. E.A. Winkler, R.D. Bell, and B.V. Zlokovic Central nervous system pericytes in health and disease Nat. Neurosci. 14 2011 1398 1405
178. T.W. Wu, W.W. Li, and H. Li Netrin-1 attenuates ischemic stroke-induced apoptosis Neuroscience 156 2008 475 482
179. Y. Xiong, A. Mahmood, and M. Chopp Angiogenesis, neurogenesis and brain recovery of function following injury Curr. Opin. Investig. Drugs 11 2010 298 308
180. Y.P. Yan, and et al. Galectin-3 mediates post-ischemic tissue remodeling Brain Res. 1288 2009 116 124
181. T. Yan, and et al. Niaspan attenuates the adverse effects of bone marrow stromal cell treatment of stroke in type one diabetic rats PLoS One 8 2013 e81199
182. T. Yan, and et al. HUCBCs increase angiopoietin 1 and induce neurorestorative effects after stroke in T1DM rats CNS Neurosci. Ther. 20 2014 935 944
183. J. Yang, and et al. proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus Cell Rep. 7 2014 796 806
184. X. Ye, and et al. Niaspan enhances vascular remodeling after stroke in type 1 diabetic rats Exp. Neurol. 232 2011 299 308
185. X. Ye, and et al. Combination BMSC and niaspan treatment of stroke enhances white matter remodeling and synaptic protein expression in diabetic rats Int. J. Mol. Sci. 14 2013 22221 22232
186. M. Yemisci, and et al. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery Nat. Med. 15 2009 1031 1037
187. M.C. Yoder Human endothelial progenitor cells Cold Spring Harb. Perspect. Med. 2 2012 a006692
188. A. Zacharek, and et al. Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke J. Cereb. Blood Flow Metab. 27 2007 1684 1691
189. L. Zhang, and Q. Xu Stem/progenitor cells in vascular regeneration Arterioscler. Thromb. Vasc. Biol. 34 2014 1114 1119
190. Z.G. Zhang, and et al. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse Circ. Res. 90 2002 284 288
191. Y.H. Zhao, and et al. Endothelial progenitor cells: therapeutic perspective for ischemic stroke CNS Neurosci. Ther. 19 2013 67 75