Vascular remodeling after ischemic stroke: Mechanisms and therapeutic potentials

Progress in Neurobiology

Volumn 115, Issue C, 2014, Pages 138-156

  Liu, Jialing ^a,b   Wang, Yongting ^c,d   Akamatsu, Yosuke ^a,b,e   Lee, Chih Cheng ^a,b   Stetler, R Anne ^f   Lawton, Michael T ^a   Yang, Guo Yuan ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Neuroscience and Neuroengineering Research Center Med X Research Institute and School of Biomedical Engineering   (China)

^d SHANGHAI JIAO TONG UNIVERSITY   (China)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Arteriogenesis; Collateral flow; Fluid shear stress; Macrophage polarization; Pro angiogenic factors

Indexed keywords

ANGIOGENESIS; ANIMAL; BRAIN CIRCULATION; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; COLLATERAL CIRCULATION; CONVALESCENCE; HUMAN; MACROPHAGE POLARIZATION; PATHOLOGY; PHYSIOLOGY; PRO-ANGIOGENIC FACTORS; REVIEW; SHEAR STRESS;

ANGIOGENESIS; ARTERIOGENESIS; COLLATERAL FLOW; FLUID SHEAR STRESS; MACROPHAGE POLARIZATION; PRO-ANGIOGENIC FACTORS;

ANIMALS; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; HUMANS; RECOVERY OF FUNCTION; STROKE;

EID: 84889840797     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2013.11.004     Document Type: Review

References (272)

1. Akamatsu Y., Lee C.C., Liu J. Impaired acute collateral flow dynamics following experimental stroke in Type 2 diabetic mice. Stroke 2013, 44:ATP146.
2. Akamatsu Y., Shimizu H., Saito A., Fujimura M., Tominaga T. Consistent focal cerebral ischemia without posterior cerebral artery occlusion and its real-time monitoring in an intraluminal suture model in mice. J. Neurosurg. 2012, 116:657-664.
3. Alpers B.J., Berry R.G., Paddison R.M. Anatomical studies of the circle of Willis in normal brain. AMA Arch. Neurol. Psychiatry 1959, 81:409-418.
4. Anand S., Majeti B.K., Acevedo L.M., Murphy E.A., Mukthavaram R., Scheppke L., Huang M., Shields D.J., Lindquist J.N., Lapinski P.E., King P.D., Weis S.M., Cheresh D.A. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat. Med. 2010, 16:909-914.
5. Arai K., Jin G., Navaratna D., Lo E.H. Brain angiogenesis in developmental and pathological processes: neurovascular injury and angiogenic recovery after stroke. FASEB J. 2009, 276:4644-4652.
6. Armitage G.A., Todd K.G., Shuaib A., Winship I.R. Laser speckle contrast imaging of collateral blood flow during acute ischemic stroke. J. Cereb. Blood Flow Metab. 2010, 30:1432-1436.
7. Armulik A., Genove G., Mae M., Nisancioglu M.H., Wallgard E., Niaudet C., He L., Norlin J., Lindblom P., Strittmatter K., Johansson B.R., Betsholtz C. Pericytes regulate the blood-brain barrier. Nature 2010, 468:557-561.
8. Arras M., Ito W.D., Scholz D., Winkler B., Schaper J., Schaper W. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J. Clin. Invest. 1998, 101:40-50.
9. Asahara T., Bauters C., Zheng L.P., Takeshita S., Bunting S., Ferrara N., Symes J.F., Isner J.M. Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation 1995, 92:II365-II371.
10. Aslanyan S., Fazekas F., Weir C.J., Horner S., Lees K.R., Committee G.I.S., Investigators Effect of blood pressure during the acute period of ischemic stroke on stroke outcome: a tertiary analysis of the GAIN International Trial. Stroke 2003, 34:2420-2425.
11. Augustin H.G., Koh G.Y., Thurston G., Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 2009, 10:165-177.
12. Ayajiki K., Fujioka H., Shinozaki K., Okamura T. Effects of capsaicin and nitric oxide synthase inhibitor on increase in cerebral blood flow induced by sensory and parasympathetic nerve stimulation in the rat. J. Appl. Physiol. 2005, 98:1792-1798.
13. Ayata C., Dunn A.K., Gursoy O.Y., Huang Z., Boas D.A., Moskowitz M.A. Laser speckle flowmetry for the study of cerebrovascular physiology in normal and ischemic mouse cortex. J. Cereb. Blood Flow Metab. 2004, 24:744-755.
14. Ayata C., Shin H.K., Salomone S., Ozdemir-Gursoy Y., Boas D.A., Dunn A.K., Moskowitz M.A. Pronounced hypoperfusion during spreading depression in mouse cortex. J. Cereb. Blood Flow Metab. 2004, 24:1172-1182.
15. Ballabh P. Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr. Res. 2010, 67:1-8.
16. Banai S., Jaklitsch M.T., Shou M., Lazarous D.F., Scheinowitz M., Biro S., Epstein S.E., Unger E.F. Angiogenic-induced enhancement of collateral blood flow to ischemic myocardium by vascular endothelial growth factor in dogs. Circulation 1994, 89:2183-2189.
17. Bang O.Y., Saver J.L., Buck B.H., Alger J.R., Starkman S., Ovbiagele B., Kim D., Jahan R., Duckwiler G.R., Yoon S.R., Vinuela F., Liebeskind D.S., Investigators U.C. Impact of collateral flow on tissue fate in acute ischaemic stroke. J. Neurol. Neurosurg. Psychiatry 2008, 79:625-629.
18. Bang O.Y., Saver J.L., Kim S.J., Kim G.M., Chung C.S., Ovbiagele B., Lee K.H., Liebeskind D.S. Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke 2011, 42:693-699.
19. Bang O.Y., Saver J.L., Kim S.J., Kim G.M., Chung C.S., Ovbiagele B., Lee K.H., Liebeskind D.S., Collaborators UC-SS Collateral flow averts hemorrhagic transformation after endovascular therapy for acute ischemic stroke. Stroke 2011, 42:2235-2239.
20. Bar-Shir A., Shemesh N., Nossin-Manor R., Cohen Y. Late stimulation of the sphenopalatine-ganglion in ischemic rats: improvement in N-acetyl-aspartate levels and diffusion weighted imaging characteristics as seen by MR. J. Magn. Reson. Imaging 2010, 31:1355-1363.
21. Beenken A., Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat. Rev. Drug Discov. 2009, 8:235-253.
22. Belayev L., Busto R., Zhao W., Clemens J.A., Ginsberg M.D. Effect of delayed albumin hemodilution on infarction volume and brain edema after transient middle cerebral artery occlusion in rats. J. Neurosurg. 1997, 87:595-601.
23. Belayev L., Pinard E., Nallet H., Seylaz J., Liu Y., Riyamongkol P., Zhao W., Busto R., Ginsberg M.D. Albumin therapy of transient focal cerebral ischemia: in vivo analysis of dynamic microvascular responses. Stroke 2002, 33:1077-1084.
24. Belayev L., Saul I., Huh P.W., Finotti N., Zhao W., Busto R., Ginsberg M.D. Neuroprotective effect of high-dose albumin therapy against global ischemic brain injury in rats. Brain Res. 1999, 845:107-111.
25. Belayev L., Zhao W., Pattany P.M., Weaver R.G., Huh P.W., Lin B., Busto R., Ginsberg M.D. Diffusion-weighted magnetic resonance imaging confirms marked neuroprotective efficacy of albumin therapy in focal cerebral ischemia. Stroke 1998, 29:2587-2599.
26. Bell R.D., Winkler E.A., Sagare A.P., Singh I., LaRue B., Deane R., Zlokovic B.V. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010, 68:409-427.
27. Bergmann C.E., Hoefer I.E., Meder B., Roth H., van Royen N., Breit S.M., Jost M.M., Aharinejad S., Hartmann S., Buschmann I.R. Arteriogenesis depends on circulating monocytes and macrophage accumulation and is severely depressed in op/op mice. J. Leukoc. Biol. 2006, 80:59-65.
28. Boas D.A., Dunn A.K. Laser speckle contrast imaging in biomedical optics. J. Biomed. Opt. 2010, 15:011109.
29. Bobbie M.W., Roy S., Trudeau K., Munger S.J., Simon A.M., Roy S. Reduced connexin 43 expression and its effect on the development of vascular lesions in retinas of diabetic mice. Invest. Ophthalmol. Vis. Sci. 2010, 51:3758-3763.
30. Boehm T., Folkman J., Browder T., O'Reilly M.S. Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature 1997, 390:404-407.
31. Bogoslovsky T., Happola O., Salonen O., Lindsberg P.J. Induced hypertension for the treatment of acute MCA occlusion beyond the thrombolysis window: case report. BMC Neurol. 2006, 6:46.
32. Bose P., Holter J.L., Selby G.B. Bevacizumab in hereditary hemorrhagic telangiectasia. N. Engl. J. Med. 2009, 360:2143-2144.
33. Braun A., Xu H., Hu F., Kocherlakota P., Siegel D., Chander P., Ungvari Z., Csiszar A., Nedergaard M., Ballabh P. Paucity of pericytes in germinal matrix vasculature of premature infants. J. Neurosci. 2007, 27:12012-12024.
34. Bremer A.M., Yamada K., West C.R. Ischemic cerebral edema in primates: effects of acetazolamide, phenytoin, sorbitol, dexamethasone, and methylprednisolone on brain water and electrolytes. Neurosurgery 1980, 6:149-154.
35. Brozici M., van der Zwan A., Hillen B. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 2003, 34:2750-2762.
36. Buschmann I., Heil M., Jost M., Schaper W. Influence of inflammatory cytokines on arteriogenesis. Microcirculation 2003, 10:371-379.
37. Buschmann I.R., Hoefer I.E., van Royen N., Katzer E., Braun-Dulleaus R., Heil M., Kostin S., Bode C., Schaper W. GM-CSF: a strong arteriogenic factor acting by amplification of monocyte function. Atherosclerosis 2001, 159:343-356.
38. Bussmann J., Wolfe S.A., Siekmann A.F. Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development 2011, 138:1717-1726.
39. Cao R., Brakenhielm E., Pawliuk R., Wariaro D., Post M.J., Wahlberg E., Leboulch P., Cao Y. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat. Med. 2003, 9:604-613.
40. Capoccia B.J., Gregory A.D., Link D.C. Recruitment of the inflammatory subset of monocytes to sites of ischemia induces angiogenesis in a monocyte chemoattractant protein-1-dependent fashion. J. Leukoc. Biol. 2008, 84:760-768.
41. Carmeliet P. Angiogenesis in health and disease. Nat. Med. 2003, 9:653-660.
42. Carmeliet P., Jain R.K. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011, 473:298-307.
43. Carmeliet P., Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature 2005, 436:193-200.
44. Chalela J.A., Alsop D.C., Gonzalez-Atavales J.B., Maldjian J.A., Kasner S.E., Detre J.A. Magnetic resonance perfusion imaging in acute ischemic stroke using continuous arterial spin labeling. Stroke 2000, 31:680-687.
45. Chalela J.A., Dunn B., Todd J.W., Warach S. Induced hypertension improves cerebral blood flow in acute ischemic stroke. Neurology 2005, 64:1979.
46. Chen C., Parangi S., Tolentino M.J., Folkman J. A strategy to discover circulating angiogenesis inhibitors generated by human tumors. Cancer Res. 1995, 55:4230-4233.
47. Chen C.C., Chen Y.C., Hsiao H.Y., Chang C., Chern Y. Neurovascular abnormalities in brain disorders: highlights with angiogenesis and magnetic resonance imaging studies. J. Biomed. Sci. 2013, 20:47.
48. Chileuitt L., Leber K., McCalden T., Weinstein P.R. Induced hypertension during ischemia reduces infarct area after temporary middle cerebral artery occlusion in rats. Surg. Neurol. 1996, 46:229-234.
49. Christoforidis G.A., Karakasis C., Mohammad Y., Caragine L.P., Yang M., Slivka A.P. Predictors of hemorrhage following intra-arterial thrombolysis for acute ischemic stroke: the role of pial collateral formation. Am. J. Neuroradiol. 2009, 30:165-170.
50. Culotti J.G., Merz D.C. DCC and netrins. Curr. Opin. Cell Biol. 1998, 10:609-613.
51. D'Amore P.A., Ng Y.S. Tales of the cryptic: unveiling more angiogenesis inhibitors. Trends Mol. Med. 2002, 8:313-315.
52. Daneman R., Zhou L., Kebede A.A., Barres B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010, 468:562-566.
53. Defazio R.A., Levy S., Morales C.L., Levy R.V., Dave K.R., Lin H.W., Abaffy T., Watson B.D., Perez-Pinzon M.A., Ohanna V. A protocol for characterizing the impact of collateral flow after distal middle cerebral artery occlusion. Transl. Stroke Res. 2011, 2:112-127.
54. Derdeyn C.P., Shaibani A., Moran C.J., Cross D.T., Grubb R.L., Powers W.J. Lack of correlation between pattern of collateralization and misery perfusion in patients with carotid occlusion. Stroke 1999, 30:1025-1032.
55. Derdeyn C.P., Videen T.O., Fritsch S.M., Carpenter D.A., Grubb R.L., Powers W.J. Compensatory mechanisms for chronic cerebral hypoperfusion in patients with carotid occlusion. Stroke 1999, 30:1019-1024.
56. Diansan S., Shifen Z., Zhen G., Heming W., Xiangrui W. Resection of the nerves bundle from the sphenopalatine ganglia tend to increase the infarction volume following middle cerebral artery occlusion. Neurol. Sci. 2010, 31:431-435.
57. Diaz-Flores L., Gutierrez R., Madrid J.F., Varela H., Valladares F., Acosta E., Martin-Vasallo P., Diaz-Flores L. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol. Histopathol. 2009, 24:909-969.
58. Ding G., Jiang Q., Li L., Zhang L., Zhang Z.G., Ledbetter K.A., Gollapalli L., Panda S., Li Q., Ewing J.R., Chopp M. Angiogenesis detected after embolic stroke in rat brain using magnetic resonance T2* WI. Stroke 2008, 39:1563-1568.
59. Dirnagl U., Becker K., Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol. 2009, 8:398-412.
60. Duda D.G., Kozin S.V., Kirkpatrick N.D., Xu L., Fukumura D., Jain R.K. CXCL12 (SDF1alpha)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies?. Clin. Cancer Res. 2011, 17:2074-2080.
61. Dunn A.K., Bolay H., Moskowitz M.A., Boas D.A. Dynamic imaging of cerebral blood flow using laser speckle. J. Cereb. Blood Flow Metab. 2001, 21:195-201.
62. Dupuis-Girod S., Bailly S., Plauchu H. Hereditary hemorrhagic telangiectasia: from molecular biology to patient care. J. Thromb. Haemost. 2010, 8:1447-1456.
63. Eilken H.M., Adams R.H. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 2010, 22:617-625.
64. Eitenmuller I., Volger O., Kluge A., Troidl K., Barancik M., Cai W.J., Heil M., Pipp F., Fischer S., Horrevoets A.J., Schmitz-Rixen T., Schaper W. The range of adaptation by collateral vessels after femoral artery occlusion. Circ. Res. 2006, 99:656-662.
65. Emery D.J., Schellinger P.D., Selchen D., Douen A.G., Chan R., Shuaib A., Butcher K.S. Safety and feasibility of collateral blood flow augmentation after intravenous thrombolysis. Stroke 2011, 42:1135-1137.
66. Erdo F., Buschmann I.R. Arteriogenesis: a new strategy of therapeutic intervention in chronic arterial disorders. Cellular mechanism and experimental models. Orv. Hetil. 2007, 148:633-642.
67. Fagan S.C., Cronic L.E., Hess D.C. Minocycline development for acute ischemic stroke. Transl. Stroke Res. 2011, 2:202-208.
68. Fan Y., Shen F., Frenzel T., Zhu W., Ye J., Liu J., Chen Y., Su H., Young W.L., Yang G.Y. Endothelial progenitor cell transplantation improves long-term stroke outcome in mice. Ann. Neurol. 2010, 67:488-497.
69. Fan Y., Yang G.Y. Therapeutic angiogenesis for brain ischemia: a brief review. J. Neuroimmune Pharmacol. 2007, 2:284-289.
70. Fazeli A., Dickinson S.L., Hermiston M.L., Tighe R.V., Steen R.G., Small C.G., Stoeckli E.T., Keino-Masu K., Masu M., Rayburn H., Simons J., Bronson R.T., Gordon J.I., Tessier-Lavigne M., Weinberg R.A. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 1997, 386:796-804.
71. Ferrara N. VEGF-A: a critical regulator of blood vessel growth. Eur. Cytokine Netw. 2009, 20:158-163.
72. Fonarow G.C., Smith E.E., Saver J.L., Reeves M.J., Bhatt D.L., Grau-Sepulveda M.V., Olson D.M., Hernandez A.F., Peterson E.D., Schwamm L.H. Timeliness of tissue-type plasminogen activator therapy in acute ischemic stroke: patient characteristics, hospital factors, and outcomes associated with door-to-needle times within 60minutes. Circulation 2011, 123:750-758.
73. Fujita M., Cha Y.R., Pham V.N., Sakurai A., Roman B.L., Gutkind J.S., Weinstein B.M. Assembly and patterning of the vascular network of the vertebrate hindbrain. Development 2011, 138:1705-1715.
74. Fukui M., Kono S., Sueishi K., Ikezaki K. Moyamoya disease. Neuropathology 2000, 20(Suppl.):S61-S64.
75. Fung E., Helisch A. Macrophages in collateral arteriogenesis. Front Physiol. 2012, 3:353.
76. 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.
77. Geeganage C., Tracy M., England T., Sare G., Moulin T., Woimant F., Christensen H., De Deyn P.P., Leys D., O'Neill D., Ringelstein E.B., Bath P.M., for T.I. Relationship between baseline blood pressure parameters (including mean pressure, pulse pressure, and variability) and early outcome after stroke: data from the Tinzaparin in Acute Ischaemic Stroke Trial (TAIST). Stroke 2011, 42:491-493.
78. Geelen G., Arbeille P., Saumet J.L., Cottet-Emard J.M., Patat F., Vincent M. Hemodynamic and hormonal effects of prolonged anti-G suit inflation in humans. J. Appl. Physiol. 1992, 72:977-984.
79. George A.L., Bangalore-Prakash P., Rajoria S., Suriano R., Shanmugam A., Mittelman A., Tiwari R.K. Endothelial progenitor cell biology in disease and tissue regeneration. J. Hematol. Oncol. 2011, 4:24.
80. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., Jeltsch M., Mitchell C., Alitalo K., Shima D., Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 2003, 161:1163-1177.
81. Gerhardt H., Wolburg H., Redies C. N-cadherin mediates pericytic-endothelial interaction during brain angiogenesis in the chicken. Dev. Dyn. 2000, 218:472-479.
82. Ginsberg M.D. Neuroprotection for ischemic stroke: past, present and future. Neuropharmacology 2008, 55:363-389.
83. Ginsberg M.D., Palesch Y.Y., Hill M.D. The ALIAS (ALbumin In Acute Stroke) Phase III randomized multicentre clinical trial: design and progress report. Biochem. Soc. Trans. 2006, 34:1323-1326.
84. Goldberg J.S., Hirschi K.K. Diverse roles of the vasculature within the neural stem cell niche. Regen. Med. 2009, 4:879-897.
85. Gorski D.H., Mauceri H.J., Salloum R.M., Gately S., Hellman S., Beckett M.A., Sukhatme V.P., Soff G.A., Kufe D.W., Weichselbaum R.R. Potentiation of the antitumor effect of ionizing radiation by brief concomitant exposures to angiostatin. Cancer Res. 1998, 58:5686-5689.
86. Guan Y., Wang Y., Yuan F., Lu H., Ren Y., Xiao T., Chen K., Greenberg D.A., Jin K., Yang G.Y. Effect of suture properties on stability of middle cerebral artery occlusion evaluated by synchrotron radiation angiography. Stroke 2012, 43:888-891.
87. Haass A., Kroemer H., Jager H., Muller K., Decker I., Wagner E.M., Schimrigk K. Dextran 40 or HES 200/0.5? Hemorheology of the long-term treatment of ischemic cerebral attacks. Dtsch. Med. Wochenschr. 1986, 111:1681-1686.
88. Halliwell B. Albumin - an important extracellular antioxidant?. Biochem. Pharmacol. 1988, 37:569-571.
89. Hammer M.D., Schwamm L., Starkman S., Schellinger P.D., Jovin T., Nogueira R., Burgin W.S., Sen S., Diener H.C., Watson T., Michel P., Shuaib A., Dillon W., Liebeskind D.S. Safety and feasibility of NeuroFlo use in eight- to 24-hour ischemic stroke patients. Int. J. Stroke 2012, 7:655-661.
90. Hammes H.P., Lin J., Wagner P., Feng Y., Vom Hagen F., Krzizok T., Renner O., Breier G., Brownlee M., Deutsch U. Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy. Diabetes 2004, 53:1104-1110.
91. Hartkamp M.J., van Der Grond J., van Everdingen K.J., Hillen B., Mali W.P. Circle of Willis collateral flow investigated by magnetic resonance angiography. Stroke 1999, 30:2671-2678.
92. Hawkins B.T., Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005, 57:173-185.
93. Hayashi T., Noshita N., Sugawara T., Chan P.H. Temporal profile of angiogenesis and expression of related genes in the brain after ischemia. J. Cereb. Blood Flow Metab. 2003, 23:166-180.
94. i. Am. J. Physiol. 1993, 265:H74-H82.
95. Heil M., Schaper W. Influence of mechanical, cellular, and molecular factors on collateral artery growth (arteriogenesis). Circ. Res. 2004, 95:449-458.
96. Heil M., Ziegelhoeffer T., Pipp F., Kostin S., Martin S., Clauss M., Schaper W. Blood monocyte concentration is critical for enhancement of collateral artery growth. Am. J. Physiol. Heart Circ. Physiol. 2002, 283:H2411-H2419.
97. Hellberg C., Ostman A., Heldin C.H. PDGF and vessel maturation. Recent Results Cancer Res. 2010, 180:103-114.
98. Henderson R.D., Eliasziw M., Fox A.J., Rothwell P.M., Barnett H.J. Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. North American Symptomatic Carotid Endarterectomy Trial (NASCET) Group. Stroke 2000, 31:128-132.
99. Henninger N., Fisher M. Stimulating circle of Willis nerve fibers preserves the diffusion-perfusion mismatch in experimental stroke. Stroke 2007, 38:2779-2786.
100. Hermier M., Nighoghossian N., Derex L., Wiart M., Nemoz C., Berthezene Y., Froment J.C. Hypointense leptomeningeal vessels at T2*-weighted MRI in acute ischemic stroke. Neurology 2005, 65:652-653.
101. Hill M.D., Moy C.S., Palesch Y.Y., Martin R., Dillon C.R., Waldman B.D., Patterson L., Mendez I.M., Ryckborst K.J., Tamariz D., Ginsberg M.D., Investigators A. The albumin in acute stroke trial (ALIAS); design and methodology. Int. J. Stroke 2007, 2:214-219.
102. Hillis A.E., Wityk R.J., Barker P.B., Ulatowski J.A., Jacobs M.A. Change in perfusion in acute nondominant hemisphere stroke may be better estimated by tests of hemispatial neglect than by the National Institutes of Health Stroke Scale. Stroke 2003, 34:2392-2396.
103. Hinshaw D.B., Thompson J.R., Hasso A.N. Adult arteriosclerotic moyamoya. Radiology 1976, 118:633-636.
104. Hong K., Hinck L., Nishiyama M., Poo M.M., Tessier-Lavigne M., Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999, 97:927-941.
105. Huang J., Li Y., Tang Y., Tang G., Yang G.Y., Wang Y. CXCR4 antagonist AMD3100 protects blood-brain barrier integrity and reduces inflammatory response after focal ischemia in mice. Stroke 2013, 44:190-197.
106. Huber A.B., Kolodkin A.L., Ginty D.D., Cloutier J.F. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu. Rev. Neurosci. 2003, 26:509-563.
107. Huh P.W., Belayev L., Zhao W., Busto R., Saul I., Ginsberg M.D. The effect of high-dose albumin therapy on local cerebral perfusion after transient focal cerebral ischemia in rats. Brain Res. 1998, 804:105-113.
108. Iadecola C., Anrather J. Stroke research at a crossroad: asking the brain for directions. Nat. Neurosci. 2011, 14:1363-1368.
109. Ikeda H., Sasaki T., Yoshimoto T., Fukui M., Arinami T. Mapping of a familial moyamoya disease gene to chromosome 3p24.2-p26. Am. J. Hum. Genet. 1999, 64:533-537.
110. Ingraham J.P., Forbes M.E., Riddle D.R., Sonntag W.E. Aging reduces hypoxia-induced microvascular growth in the rodent hippocampus. J. Gerontol. A: Biol. Sci. Med. Sci. 2008, 63:12-20.
111. Ito W.D., Arras M., Winkler B., Scholz D., Schaper J., Schaper W. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ. Res. 1997, 80:829-837.
112. Jakobsson L., Franco C.A., Bentley K., Collins R.T., Ponsioen B., Aspalter I.M., Rosewell I., Busse M., Thurston G., Medvinsky A., Schulte-Merker S., Gerhardt H. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 2010, 12:943-953.
113. Kadoglou N.P., Daskalopoulou S.S., Perrea D., Liapis C.D. Matrix metalloproteinases and diabetic vascular complications. Angiology 2005, 56:173-189.
114. Kang H.S., Kim S.K., Cho B.K., Kim Y.Y., Hwang Y.S., Wang K.C. Single nucleotide polymorphisms of tissue inhibitor of metalloproteinase genes in familial moyamoya disease. Neurosurgery 2006, 58:1074-1080. (discussion 1074-1080).
115. Kato H., Shimosegawa E., Oku N., Kimura Y., Kajimoto K., Tanaka M., Hori M., Kitagawa K., Hatazawa J. Cerebral hemodynamics and oxygen metabolism in patients with moyamoya syndrome associated with atherosclerotic steno-occlusive arterial lesions. Cerebrovasc. Dis. 2008, 26:9-15.
116. Keaney J.F., Gaziano J.M., Xu A., Frei B., Curran-Celentano J., Shwaery G.T., Loscalzo J., Vita J.A. Dietary antioxidants preserve endothelium-dependent vessel relaxation in cholesterol-fed rabbits. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11880-11884.
117. Keaney J.F., Simon D.I., Stamler J.S., Jaraki O., Scharfstein J., Vita J.A., Loscalzo J. NO forms an adduct with serum albumin that has endothelium-derived relaxing factor-like properties. J. Clin. Invest. 1993, 91:1582-1589.
118. Keino-Masu K., Masu M., Hinck L., Leonardo E.D., Chan S.S., Culotti J.G., Tessier-Lavigne M. Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell 1996, 87:175-185.
119. Khurana D., Kaul S., Bornstein N.M., Imp ACTSG Implant for augmentation of cerebral blood flow trial 1: a pilot study evaluating the safety and effectiveness of the Ischaemic Stroke System for treatment of acute ischaemic stroke. Int. J. Stroke 2009, 4:480-485.
120. Kirsch M., Strasser J., Allende R., Bello L., Zhang J., Black P.M. Angiostatin suppresses malignant glioma growth in vivo. Cancer Res. 1998, 58:4654-4659.
121. Koga M., Toyoda K., Naganuma M., Kario K., Nakagawara J., Furui E., Shiokawa Y., Hasegawa Y., Okuda S., Yamagami H., Kimura K., Okada Y., Minematsu K. Nationwide survey of antihypertensive treatment for acute intracerebral hemorrhage in Japan. Hypertens. Res. 2009, 32:759-764. Stroke Acute Management with Urgent Risk-factor A, Improvement Study I.
122. Koh G.Y. Orchestral actions of angiopoietin-1 in vascular regeneration. Trends Mol. Med. 2013, 19:31-39.
123. Kravik S.E., Keil L.C., Geelen G., Wade C.E., Barnes P.R., Spaul W.A., Elder C.A., Greenleaf J.E. Effect of antigravity suit inflation on cardiovascular, PRA, and PVP responses in humans. J. Appl. Physiol. 1986, 61:766-774.
124. Krishnaswamy A., Klein J.P., Kapadia S.R. Clinical cerebrovascular anatomy. Catheter. Cardiovasc. Interv. 2010, 75:530-539.
125. Kroemer H., Haass A., Muller K., Jager H., Wagner E.M., Heimburg P., Klotz U. Haemodilution therapy in ischaemic stroke: plasma concentrations and plasma viscosity during long-term infusion of dextran 40 or hydroxyethyl starch 200/0.5. Eur. J. Clin. Pharmacol. 1987, 31:705-710.
126. Krupinski J., Kaluza J., Kumar P., Kumar S., Wang J.M. Some remarks on the growth-rate and angiogenesis of microvessels in ischemic stroke. Morphometric and immunocytochemical studies. Patol. Pol. 1993, 44:203-209.
127. Krupinski J., Kaluza J., Kumar P., Kumar S., Wang J.M. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 1994, 25:1794-1798.
128. Krupinski J., Kaluza J., Kumar P., Wang M., Kumar S. Prognostic value of blood vessel density in ischaemic stroke. Lancet 1993, 342:742.
129. Krupinski J., Stroemer P., Slevin M., Marti E., Kumar P., Rubio F. Three-dimensional structure and survival of newly formed blood vessels after focal cerebral ischemia. Neuroreport 2003, 14:1171-1176.
130. Kucinski T., Koch C., Eckert B., Becker V., Kromer H., Heesen C., Grzyska U., Freitag H.J., Rother J., Zeumer H. Collateral circulation is an independent radiological predictor of outcome after thrombolysis in acute ischaemic stroke. Neuroradiology 2003, 45:11-18.
131. 2O positron emission tomography. Stroke 1995, 26:1825-1829.
132. la Sala A., Pontecorvo L., Agresta A., Rosano G., Stabile E. Regulation of collateral blood vessel development by the innate and adaptive immune system. Trends Mol. Med. 2012, 18:494-501.
133. Lanahan A.A., Hermans K., Claes F., Kerley-Hamilton J.S., Zhuang Z.W., Giordano F.J., Carmeliet P., Simons M. VEGF receptor 2 endocytic trafficking regulates arterial morphogenesis. Dev. Cell 2010, 18:713-724.
134. Lannutti B.J., Gately S.T., Quevedo M.E., Soff G.A., Paller A.S. Human angiostatin inhibits murine hemangioendothelioma tumor growth in vivo. Cancer Res. 1997, 57:5277-5280.
135. 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.
136. Leblanc G.G., Golanov E., Awad I.A., Young W.L. Biology of vascular malformations of the brain. Stroke 2009, 40:e694-e702.
137. Lebrin F., Deckers M., Bertolino P., Ten Dijke P. TGF-beta receptor function in the endothelium. Cardiovasc. Res. 2005, 65:599-608.
138. Lebrin F., Srun S., Raymond K., Martin S., van den Brink S., Freitas C., Breant C., Mathivet T., Larrivee B., Thomas J.L., Arthur H.M., Westermann C.J., Disch F., Mager J.J., Snijder R.J., Eichmann A., Mummery C.L. Thalidomide stimulates vessel maturation and reduces epistaxis in individuals with hereditary hemorrhagic telangiectasia. Nat. Med. 2010, 16:420-428.
139. Lee C.W., Stabile E., Kinnaird T., Shou M., Devaney J.M., Epstein S.E., Burnett M.S. Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development. J. Am. Coll. Cardiol. 2004, 43:474-482.
140. Lee K.Y., Latour L.L., Luby M., Hsia A.W., Merino J.G., Warach S. Distal hyperintense vessels on FLAIR: an MRI marker for collateral circulation in acute stroke?. Neurology 2009, 72:1134-1139.
141. Lee S., Chen T.T., Barber C.L., Jordan M.C., Murdock J., Desai S., Ferrara N., Nagy A., Roos K.P., Iruela-Arispe M.L. Autocrine VEGF signaling is required for vascular homeostasis. Cell 2007, 130:691-703.
142. Leonardo E.D., Hinck L., Masu M., Keino-Masu K., Ackerman S.L., Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 1997, 386:833-838.
143. Li F., Lan Y., Wang Y., Wang J., Yang G., Meng F., Han H., Meng A., Yang X. Endothelial Smad4 maintains cerebrovascular integrity by activating N-cadherin through cooperation with Notch. Dev. Cell 2011, 20:291-302.
144. Liebeskind D.S. Collateral circulation. Stroke 2003, 34:2279-2284.
145. Liebeskind D.S. Collaterals in acute stroke: beyond the clot. Neuroimag. Clin. N. Am. 2005, 15:553-573.
146. Liebeskind D.S. Neuroprotection from the collateral perspective. IDrugs 2005, 8:222-228.
147. Liebeskind D.S. Of mice and men: essential considerations in the translation of collateral therapeutics. Stroke 2008, 39:e187-e188. (author reply e189).
148. Liebeskind D.S. Imaging the future of stroke: I. Ischemia. Ann. Neurol. 2009, 66:574-590.
149. Liebeskind D.S. Reperfusion for acute ischemic stroke: arterial revascularization and collateral therapeutics. Curr. Opin. Neurol. 2010, 23:36-45.
150. Liebeskind D.S. Collateral perfusion: time for novel paradigms in cerebral ischemia. Int. J. Stroke 2012, 7:309-310.
151. Liebeskind D.S. Trials of endovascular therapies or collaterals?. Int. J. Stroke 2013, 8:258-259.
152. Liebeskind D.S., Cotsonis G.A., Saver J.L., Lynn M.J., Cloft H.J., Chimowitz M.I. Collateral circulation in symptomatic intracranial atherosclerosis. J. Cereb. Blood Flow Metab. 2011, 31:1293-1301. Warfarin-Aspirin Symptomatic Intracranial Disease I.
153. Liebeskind D.S., Cotsonis G.A., Saver J.L., Lynn M.J., Turan T.N., Cloft H.J., Chimowitz M.I. Collaterals dramatically alter stroke risk in intracranial atherosclerosis. Ann. Neurol. 2011, 69:963-974. Warfarin-Aspirin Symptomatic Intracranial Disease I.
154. Lima F.O., Furie K.L., Silva G.S., Lev M.H., Camargo E.C., Singhal A.B., Harris G.J., Halpern E.F., Koroshetz W.J., Smith W.S., Yoo A.J., Nogueira R.G. The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke 2010, 41:2316-2322.
155. Lin C.Y., Chang C., Cheung W.M., Lin M.H., Chen J.J., Hsu C.Y., Chen J.H., Lin T.N. Dynamic changes in vascular permeability, cerebral blood volume, vascular density, and size after transient focal cerebral ischemia in rats: evaluation with contrast-enhanced magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2008, 28:1491-1501.
156. Lin T.N., Sun S.W., Cheung W.M., Li F., Chang C. Dynamic changes in cerebral blood flow and angiogenesis after transient focal cerebral ischemia in rats. Evaluation with serial magnetic resonance imaging. Stroke 2002, 33:2985-2991.
157. Lin W., Xiong L., Han J., Leung T.W., Soo Y.O., Chen X., Wong K.S. External counterpulsation augments blood pressure and cerebral flow velocities in ischemic stroke patients with cerebral intracranial large artery occlusive disease. Stroke 2012, 43:3007-3011.
158. Liu Y., Belayev L., Zhao W., Busto R., Belayev A., Ginsberg M.D. Neuroprotective effect of treatment with human albumin in permanent focal cerebral ischemia: histopathology and cortical perfusion studies. Eur. J. Pharmacol. 2001, 428:193-201.
159. Lo E.H. Experimental models, neurovascular mechanisms and translational issues in stroke research. Br. J. Pharmacol. 2008, 153(Suppl 1):S396-S405.
160. Lo E.H., Dalkara T., Moskowitz M.A. Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosci. 2003, 4:399-415.
161. Lu H., Wang Y., He X., Yuan F., Lin X., Xie B., Tang G., Huang J., Tang Y., Jin K., Chen S., Yang G.Y. Netrin-1 hyperexpression in mouse brain promotes angiogenesis and long-term neurological recovery after transient focal ischemia. Stroke 2012, 43:838-843.
162. Maas M.B., Lev M.H., Ay H., Singhal A.B., Greer D.M., Smith W.S., Harris G.J., Halpern E., Kemmling A., Koroshetz W.J., Furie K.L. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke 2009, 40:3001-3005.
163. Marchal G., Serrati C., Rioux P., Petit-Taboue M.C., Viader F., de la Sayette V., Le Doze F., Lochon P., Derlon J.M., Orgogozo J.M., et al. PET imaging of cerebral perfusion and oxygen consumption in acute ischaemic stroke: relation to outcome. Lancet 1993, 341:925-927.
164. Marti H.J., Bernaudin M., Bellail A., Schoch H., Euler M., Petit E., Risau W. Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am. J. Pathol. 2000, 156:965-976.
165. McVerry F., Liebeskind D.S., Muir K.W. Systematic review of methods for assessing leptomeningeal collateral flow. Am. J. Neuroradiol. 2012, 33:576-582.
166. Meisner J.K., Price R.J. Spatial and temporal coordination of bone marrow-derived cell activity during arteriogenesis: regulation of the endogenous response and therapeutic implications. Microcirculation 2010, 17:583-599.
167. Menon B.K., Smith E.E., Coutts S.B., Welsh D.G., Faber J.E., Goyal M., Hill M.D., Demchuk A.M., Damani Z., Cho K.H., Chang H.W., Hong J.H., Sohn S.I. Leptomeningeal collaterals are associated with modifiable metabolic risk factors. Ann. Neurol. 2013.
168. Moore S.W., Tessier-Lavigne M., Kennedy T.E. Netrins and their receptors. Adv. Exp. Med. Biol. 2007, 621:17-31.
169. Morioka M., Hamada J., Kawano T., Todaka T., Yano S., Kai Y., Ushio Y. Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients. Stroke 2003, 34:90-95.
170. Moskowitz M.A. Brain protection: maybe yes, maybe no. Stroke 2010, 41:S85-S86.
171. Moskowitz M.A., Lo E.H., Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010, 67:181-198.
172. Muller M., Schimrigk K. Vasomotor reactivity and pattern of collateral blood flow in severe occlusive carotid artery disease. Stroke 1996, 27:296-299.
173. Murakami M., Nguyen L.T., Zhuang Z.W., Moodie K.L., Carmeliet P., Stan R.V., Simons M. The FGF system has a key role in regulating vascular integrity. J. Clin. Invest. 2008, 118:3355-3366.
174. Nagy J.A., Dvorak A.M., Dvorak H.F. VEGF-A and the induction of pathological angiogenesis. Annu. Rev. Pathol. 2007, 2:251-275.
175. Nakagawa T., Suga S., Kawase T., Toda M. Intracarotid injection of granulocyte-macrophage colony-stimulating factor induces neuroprotection in a rat transient middle cerebral artery occlusion model. Brain Res. 2006, 1089:179-185.
176. Nanba R., Tada M., Kuroda S., Houkin K., Iwasaki Y. Sequence analysis and bioinformatics analysis of chromosome 17q25 in familial moyamoya disease. Childs Nerv. Syst. 2005, 21:62-68.
177. Navaratna D., Guo S., Arai K., Lo E.H. Mechanisms and targets for angiogenic therapy after stroke. Cell Adh. Migr. 2009, 3:216-223.
178. Nimmagadda A., Park H.P., Prado R., Ginsberg M.D. Albumin therapy improves local vascular dynamics in a rat model of primary microvascular thrombosis: a two-photon laser-scanning microscopy study. Stroke 2008, 39:198-204.
179. Nishimura N., Schaffer C.B., Friedman B., Lyden P.D., Kleinfeld D. Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:365-370.
180. 2+ channels sets the polarity of nerve growth-cone turning. Nature 2003, 423:990-995.
181. O'Reilly M.S., Boehm T., Shing Y., Fukai N., Vasios G., Lane W.S., Flynn E., Birkhead J.R., Olsen B.R., Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997, 88:277-285.
182. Omura-Matsuoka E., Yagita Y., Sasaki T., Terasaki Y., Oyama N., Sugiyama Y., Todo K., Sakoda S., Kitagawa K. Hypertension impairs leptomeningeal collateral growth after common carotid artery occlusion: restoration by antihypertensive treatment. J. Neurosci. Res. 2011, 89:108-116.
183. Ovbiagele B., Saver J.L., Starkman S., Kim D., Ali L.K., Jahan R., Duckwiler G.R., Vinuela F., Pineda S., Liebeskind D.S. Statin enhancement of collateralization in acute stroke. Neurology 2007, 68:2129-2131.
184. Ozgur H.T., Kent Walsh T., Masaryk A., Seeger J.F., Williams W., Krupinski E., Melgar M., Labadie E. Correlation of cerebrovascular reserve as measured by acetazolamide-challenged SPECT with angiographic flow patterns and intra- or extracranial arterial stenosis. Am. J. Neuroradiol. 2001, 22:928-936.
185. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 2000, 425:479-494.
186. Pardali E., Goumans M.J., ten Dijke P. Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol. 2010, 20:556-567.
187. Parthasarathy A.B., Tom W.J., Gopal A., Zhang X., Dunn A.K. Robust flow measurement with multi-exposure speckle imaging. Opt. Express 2008, 16:1975-1989.
188. The penumbra pivotal stroke trial: safety and effectiveness of a new generation of mechanical devices for clot removal in intracranial large vessel occlusive disease. Stroke 2009, 40:2761-2768. Penumbra Pivotal Stroke Trial I.
189. Peppiatt C.M., Howarth C., Mobbs P., Attwell D. Bidirectional control of CNS capillary diameter by pericytes. Nature 2006, 443:700-704.
190. Petcu E.B., Smith R.A., Miroiu R.I., Opris M.M. Angiogenesis in old-aged subjects after ischemic stroke: a cautionary note for investigators. J. Angiogenes Res. 2010, 2:26.
191. Phng L.K., Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev. Cell 2009, 16:196-208.
192. Pipp F., Boehm S., Cai W.J., Adili F., Ziegler B., Karanovic G., Ritter R., Balzer J., Scheler C., Schaper W., Schmitz-Rixen T. Elevated fluid shear stress enhances postocclusive collateral artery growth and gene expression in the pig hind limb. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1664-1668.
193. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
194. Quaegebeur A., Lange C., Carmeliet P. The neurovascular link in health and disease: molecular mechanisms and therapeutic implications. Neuron 2011, 71:406-424.
195. Quaegebeur A., Segura I., Carmeliet P. Pericytes: blood-brain barrier safeguards against neurodegeneration?. Neuron 2010, 68:321-323.
196. Redlitz A., Daum G., Sage E.H. Angiostatin diminishes activation of the mitogen-activated protein kinases ERK-1 and ERK-2 in human dermal microvascular endothelial cells. J. Vasc. Res. 1999, 36:28-34.
197. Reinhart W.H., Nagy C. Albumin affects erythrocyte aggregation and sedimentation. Eur. J. Clin. Invest. 1995, 25:523-528.
198. Ribo M., Flores A., Rubiera M., Pagola J., Sargento-Freitas J., Rodriguez-Luna D., Coscojuela P., Maisterra O., Pineiro S., Romero F.J., Alvarez-Sabin J., Molina C.A. Extending the time window for endovascular procedures according to collateral pial circulation. Stroke 2011, 42:3465-3469.
199. Ricard N., Bidart M., Mallet C., Lesca G., Giraud S., Prudent R., Feige J.J., Bailly S. Functional analysis of the BMP9 response of ALK1 mutants from HHT2 patients: a diagnostic tool for novel ACVRL1 mutations. Blood 2010, 116:1604-1612.
200. Robin A.M., Zhang Z.G., Wang L., Zhang R.L., Katakowski M., Zhang L., Wang Y., Zhang C., Chopp M. Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2006, 26:125-134.
201. Rordorf G., Cramer S.C., Efird J.T., Schwamm L.H., Buonanno F., Koroshetz W.J. Pharmacological elevation of blood pressure in acute stroke. Clinical effects and safety. Stroke 1997, 28:2133-2138.
202. Rordorf G., Koroshetz W.J., Ezzeddine M.A., Segal A.Z., Buonanno F.S. A pilot study of drug-induced hypertension for treatment of acute stroke. Neurology 2001, 56:1210-1213.
203. Rosell A., Lo E.H. Multiphasic roles for matrix metalloproteinases after stroke. Curr. Opin. Pharmacol. 2008, 8:82-89.
204. Saharinen P., Eklund L., Miettinen J., Wirkkala R., Anisimov A., Winderlich M., Nottebaum A., Vestweber D., Deutsch U., Koh G.Y., Olsen B.R., Alitalo K. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat. Cell Biol. 2008, 10:527-537.
205. Santisakultarm T.P., Schaffer C.B. Optically quantified cerebral blood flow. J. Cereb. Blood Flow Metab. 2011, 31:1337-1338.
206. Scalzo F., Liebeskind D., Hu X. Reducing false intracranial pressure alarms using morphological waveform features. IEEE Trans. Biomed. Eng. 2013, 60:235-239.
207. Schabitz W.R., Kruger C., Pitzer C., Weber D., Laage R., Gassler N., Aronowski J., Mier W., Kirsch F., Dittgen T., Bach A., Sommer C., Schneider A. A neuroprotective function for the hematopoietic protein granulocyte-macrophage colony stimulating factor (GM-CSF). J. Cereb. Blood Flow Metab. 2008, 28:29-43.
208. Schaffer C.B., Friedman B., Nishimura N., Schroeder L.F., Tsai P.S., Ebner F.F., Lyden P.D., Kleinfeld D. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 2006, 4:e22.
209. Schaper W. Collateral circulation: past and present. Basic Res. Cardiol. 2009, 104:5-21.
210. Schaper W., Buschmann I. Arteriogenesis, the good and bad of it. Cardiovasc. Res. 1999, 43:835-837.
211. Schatteman G.C., Hanlon H.D., Jiao C., Dodds S.G., Christy B.A. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J. Clin. Invest. 2000, 106:571-578.
212. Schellinger P.D., Shuaib A., Kohrmann M., Liebeskind D.S., Jovin T., Hammer M.D., Sen S., Huang D.Y., Solander S., Gupta R., Leker R.R., Saver J.L., for the S.T.I. Reduced mortality and severe disability rates in the SENTIS trial. Am. J. Neuroradiol. 2013.
213. Schiekofer S., Galasso G., Sato K., Kraus B.J., Walsh K. Impaired revascularization in a mouse model of type 2 diabetes is associated with dysregulation of a complex angiogenic-regulatory network. Arterioscler. Thromb. Vasc. Biol. 2005, 25:1603-1609.
214. Schierling W., Troidl K., Apfelbeck H., Troidl C., Kasprzak P.M., Schaper W., Schmitz-Rixen T. Cerebral arteriogenesis is enhanced by pharmacological as well as fluid-shear-stress activation of the Trpv4 calcium channel. Eur. J. Vasc. Endovasc. Surg. 2011, 41:589-596.
215. Schierling W., Troidl K., Mueller C., Troidl C., Wustrack H., Bachmann G., Kasprzak P.M., Schaper W., Schmitz-Rixen T. Increased intravascular flow rate triggers cerebral arteriogenesis. J. Cereb. Blood Flow Metab. 2009, 29:726-737.
216. Schierling W., Troidl K., Troidl C., Schmitz-Rixen T., Schaper W., Eitenmuller I.K. The role of angiogenic growth factors in arteriogenesis. J. Vasc. Res. 2009, 46:365-374.
217. Schirmer S.H., van Royen N., Moerland P.D., Fledderus J.O., Henriques J.P., van der Schaaf R.J., Vis M.M., Baan J., Koch K.T., Horrevoets A.J., Hoefer I.E., Piek J.J. Local cytokine concentrations and oxygen pressure are related to maturation of the collateral circulation in humans. J. Am. Coll. Cardiol. 2009, 53:2141-2147.
218. Schneider U.C., Schilling L., Schroeck H., Nebe C.T., Vajkoczy P., Woitzik J. Granulocyte-macrophage colony-stimulating factor-induced vessel growth restores cerebral blood supply after bilateral carotid artery occlusion. Stroke 2007, 38:1320-1328.
219. Scholz D., Ito W., Fleming I., Deindl E., Sauer A., Wiesnet M., Busse R., Schaper J., Schaper W. Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch. 2000, 436:257-270.
220. Schwarz S., Georgiadis D., Aschoff A., Schwab S. Effects of induced hypertension on intracranial pressure and flow velocities of the middle cerebral arteries in patients with large hemispheric stroke. Stroke 2002, 33:998-1004.
221. Scott R.M., Smith E.R. Moyamoya disease and moyamoya syndrome. N. Engl. J. Med. 2009, 360:1226-1237.
222. Scott R.M., Smith J.L., Robertson R.L., Madsen J.R., Soriano S.G., Rockoff M.A. Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J. Neurosurg. 2004, 100:142-149.
223. Shen F., Fan Y., Su H., Zhu Y., Chen Y., Liu W., Young W.L., Yang G.Y. Adeno-associated viral vector-mediated hypoxia-regulated VEGF gene transfer promotes angiogenesis following focal cerebral ischemia in mice. Gene Ther. 2008, 15:30-39.
224. Shin H.K., Nishimura M., Jones P.B., Ay H., Boas D.A., Moskowitz M.A., Ayata C. Mild induced hypertension improves blood flow and oxygen metabolism in transient focal cerebral ischemia. Stroke 2008, 39:1548-1555.
225. Shovlin C.L. Hereditary haemorrhagic telangiectasia: pathophysiology, diagnosis and treatment. Blood Rev. 2010, 24:203-219.
226. Shuaib A., Bornstein N.M., Diener H.C., Dillon W., Fisher M., Hammer M.D., Molina C.A., Rutledge J.N., Saver J.L., Schellinger P.D., Shownkeen H., Investigators S.T. Partial aortic occlusion for cerebral perfusion augmentation: safety and efficacy of NeuroFlo in Acute Ischemic Stroke trial. Stroke 2011, 42:1680-1690.
227. Shuaib A., Butcher K., Mohammad A.A., Saqqur M., Liebeskind D.S. Collateral blood vessels in acute ischaemic stroke: a potential therapeutic target. Lancet Neurol. 2011, 10:909-921.
228. Sieczkiewicz G.J., Herman I.M. TGF-beta 1 signaling controls retinal pericyte contractile protein expression. Microvasc. Res. 2003, 66:190-196.
229. Smith E.R., Scott R.M. Surgical management of moyamoya syndrome. Skull Base 2005, 15:15-26.
230. Smrcka M., Ogilvy C.S., Crow R.J., Maynard K.I., Kawamata T., Ames A. Induced hypertension improves regional blood flow and protects against infarction during focal ischemia: time course of changes in blood flow measured by laser Doppler imaging. Neurosurgery 1998, 42:617-624. (discussion 615-624).
231. Srinivasan V.J., Atochin D.N., Radhakrishnan H., Jiang J.Y., Ruvinskaya S., Wu W., Barry S., Cable A.E., Ayata C., Huang P.L., Boas D.A. Optical coherence tomography for the quantitative study of cerebrovascular physiology. J. Cereb. Blood Flow Metab. 2011, 31:1339-1345.
232. Stockmann C., Doedens A., Weidemann A., Zhang N., Takeda N., Greenberg J.I., Cheresh D.A., Johnson R.S. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 2008, 456:814-818.
233. Storkebaum E., Quaegebeur A., Vikkula M., Carmeliet P. Cerebrovascular disorders: molecular insights and therapeutic opportunities. Nat. Neurosci. 2011, 14:1390-1397.
234. Stratman A.N., Malotte K.M., Mahan R.D., Davis M.J., Davis G.E. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 2009, 114:5091-5101.
235. Suchting S., Bicknell R., Eichmann A. Neuronal clues to vascular guidance. Exp. Cell Res. 2006, 312:668-675.
236. Sugiyama Y., Yagita Y., Oyama N., Terasaki Y., Omura-Matsuoka E., Sasaki T., Kitagawa K. Granulocyte colony-stimulating factor enhances arteriogenesis and ameliorates cerebral damage in a mouse model of ischemic stroke. Stroke 2011, 42:770-775.
237. Suzuki J., Takaku A. Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch. Neurol. 1969, 20:288-299.
238. Suzuki N., Gotoh F., Gotoh J., Koto A. Evidence for in vivo cerebrovascular neurogenic vasodilatation in the rat. Clin. Auton. Res. 1991, 1:23-26.
239. Taguchi A., Soma T., Tanaka H., Kanda T., Nishimura H., Yoshikawa H., Tsukamoto Y., Iso H., Fujimori Y., Stern D.M., Naritomi H., Matsuyama T. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest. 2004, 114:330-338.
240. Takeda Y., Costa S., Delamarre E., Roncal C., Leite de Oliveira R., Squadrito M.L., Finisguerra V., Deschoemaeker S., Bruyere F., Wenes M., Hamm A., Serneels J., Magat J., Bhattacharyya T., Anisimov A., Jordan B.F., Alitalo K., Maxwell P., Gallez B., Zhuang Z.W., Saito Y., Simons M., De Palma M., Mazzone M. Macrophage skewing by Phd2 haplodeficiency prevents ischaemia by inducing arteriogenesis. Nature 2011, 479:122-126.
241. Takeshita S., Zheng L.P., Brogi E., Kearney M., Pu L.Q., Bunting S., Ferrara N., Symes J.F., Isner J.M. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J. Clin. Invest. 1994, 93:662-670.
242. Takeuchi K., Shimizu K. Hypoplasia of the bilateral internal carotid arteries. Brain Nerve 1957, 9:37-43.
243. Tanghetti B., Capra R., Giunta F., Marini G., Orlandini A. Moyamoya syndrome in only one of two identical twins. Case report. J. Neurosurg. 1983, 59:1092-1094.
244. Tchaikovski V., Olieslagers S., Bohmer F.D., Waltenberger J. Diabetes mellitus activates signal transduction pathways resulting in vascular endothelial growth factor resistance of human monocytes. Circulation 2009, 120:150-159.
245. Todo K., Kitagawa K., Sasaki T., Omura-Matsuoka E., Terasaki Y., Oyama N., Yagita Y., Hori M. Granulocyte-macrophage colony-stimulating factor enhances leptomeningeal collateral growth induced by common carotid artery occlusion. Stroke 2008, 39:1875-1882.
246. Tomita M., Suzuki N., Hamel E., Busija D., Lauritzen M. Regulation of cerebral microcirculation - update. Keio J. Med. 2000, 49:26-34.
247. Troidl C., Jung G., Troidl K., Hoffmann J., Mollmann H., Nef H., Schaper W., Hamm C.W., Schmitz-Rixen T. The temporal and spatial distribution of macrophage subpopulations during arteriogenesis. Curr. Vasc. Pharmacol. 2013, 11:5-12.
248. Troidl C., Nef H., Voss S., Schilp A., Kostin S., Troidl K., Szardien S., Rolf A., Schmitz-Rixen T., Schaper W., Hamm C.W., Elsasser A., Mollmann H. Calcium-dependent signalling is essential during collateral growth in the pig hind limb-ischemia model. J. Mol. Cell. Cardiol. 2010, 49:142-151.
249. Troidl C., Troidl K., Schierling W., Cai W.J., Nef H., Mollmann H., Kostin S., Schimanski S., Hammer L., Elsasser A., Schmitz-Rixen T., Schaper W. Trpv4 induces collateral vessel growth during regeneration of the arterial circulation. J. Cell. Mol. Med. 2009, 13:2613-2621.
250. Troidl K., Ruding I., Cai W.J., Mucke Y., Grossekettler L., Piotrowska I., Apfelbeck H., Schierling W., Volger O.L., Horrevoets A.J., Grote K., Schmitz-Rixen T., Schaper W., Troidl C. Actin-binding rho activating protein (Abra) is essential for fluid shear stress-induced arteriogenesis. Arterioscler. Thromb. Vasc. Biol. 2009, 29:2093-2101.
251. Troidl K., Schaper W. Arteriogenesis versus angiogenesis in peripheral artery disease. Diabetes Metab. Res. Rev. 2012, 28(Suppl. 1):27-29.
252. Troidl K., Tribulova S., Cai W.J., Ruding I., Apfelbeck H., Schierling W., Troidl C., Schmitz-Rixen T., Schaper W. Effects of endogenous nitric oxide and of DETA NONOate in arteriogenesis. J. Cardiovasc. Pharmacol. 2010, 55:153-160.
253. van Laar P.J., Hendrikse J., Klijn C.J., Kappelle L.J., van Osch M.J., van der Grond J. Symptomatic carotid artery occlusion: flow territories of major brain-feeding arteries. Radiology 2007, 242:526-534.
254. van Oostrom M.C., van Oostrom O., Quax P.H., Verhaar M.C., Hoefer I.E. Insights into mechanisms behind arteriogenesis: what does the future hold?. J. Leukoc. Biol. 2008, 84:1379-1391.
255. Vander Eecken H.M. Morphological significance of leptomeningeal anastomoses confined to the territory of cerebral arteries. Acta Neurol. Psychiatr. Belg. 1954, 54:525-532.
256. Vinukonda G., Dummula K., Malik S., Hu F., Thompson C.I., Csiszar A., Ungvari Z., Ballabh P. Effect of prenatal glucocorticoids on cerebral vasculature of the developing brain. Stroke 2010, 41:1766-1773.
257. Walshe T.E., Saint-Geniez M., Maharaj A.S., Sekiyama E., Maldonado A.E., D'Amore P.A. TGF-beta is required for vascular barrier function, endothelial survival and homeostasis of the adult microvasculature. PLoS ONE 2009, 4:e5149.
258. Waltenberger J., Lange J., Kranz A. Vascular endothelial growth factor-A-induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus: a potential predictor for the individual capacity to develop collaterals. Circulation 2000, 102:185-190.
259. Wang R.K., An L. Doppler optical micro-angiography for volumetric imaging of vascular perfusion in vivo. Opt. Express 2009, 17:8926-8940.
260. Wang Y., Huang J., Li Y., Yang G.Y. Roles of chemokine CXCL12 and its receptors in ischemic stroke. Curr. Drug Targets 2012, 13:166-172.
261. Wayner D.D., Burton G.W., Ingold K.U., Locke S. Quantitative measurement of the total, peroxyl radical-trapping antioxidant capability of human blood plasma by controlled peroxidation. The important contribution made by plasma proteins. FEBS Lett. 1985, 187:33-37.
262. Weber M., Baker M.B., Moore J.P., Searles C.D. MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem. Biophys. Res. Commun. 2010, 393:643-648.
263. Wesley R.C., Morgan D.B. Effect of continuous intra-aortic balloon inflation in canine open chest cardiopulmonary resuscitation. Crit. Care Med. 1990, 18:630-633.
264. Winkler E.A., Bell R.D., Zlokovic B.V. Central nervous system pericytes in health and disease. Nat. Neurosci. 2011, 14:1398-1405.
265. Winkler E.A., Bell R.D., Zlokovic B.V. Lack of Smad or Notch leads to a fatal game of brain pericyte hopscotch. Dev. Cell 2011, 20:279-280.
266. Wityk R.J. Blood pressure augmentation in acute ischemic stroke. J. Neurol. Sci. 2007, 261:63-73.
267. Yamada I., Himeno Y., Suzuki S., Matsushima Y. Posterior circulation in moyamoya disease: angiographic study. Radiology 1995, 197:239-246.
268. Yarnitsky D., Lorian A., Shalev A., Zhang Z.D., Takahashi M., Agbaje-Williams M., Macdonald R.L. Reversal of cerebral vasospasm by sphenopalatine ganglion stimulation in a dog model of subarachnoid hemorrhage. Surg. Neurol. 2005, 64:5-11. (discussion 11).
269. Yin K.J., Hamblin M., Chen Y.E. Angiogenesis-regulating microRNAs and ischemic stroke. Curr. Vasc. Pharmacol. 2013.
270. Yuan F., Wang Y., Guan Y., Ren Y., Lu H., Xiao T., Xie H., Vosler P.S., Chen J., Yang G.Y. Real-time imaging of mouse lenticulostriate artery following brain ischemia. Front Biosci. (Elite Ed.) 2013, 5:517-524.
271. Zbinden R., Vogel R., Meier B., Seiler C. Coronary collateral flow and peripheral blood monocyte concentration in patients treated with granulocyte-macrophage colony stimulating factor. Heart 2004, 90:945-946.
272. Zhao B.Q., Wang S., Kim H.Y., Storrie H., Rosen B.R., Mooney D.J., Wang X., Lo E.H. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat. Med. 2006, 12:441-445.