Wide genetic variation in the native pial collateral circulation is a major determinant of variation in severity of stroke

Journal of Cerebral Blood Flow and Metabolism

Volumn 30, Issue 5, 2010, Pages 923-934

  Zhang, Hua ^a   Prabhakar, Pranay ^b   Sealock, Robert ^b   Faber, James E ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

Arteriole anastomoses; Cerebral circulation; Collaterals; Infarction; Mouse strain

Indexed keywords

ANIMAL EXPERIMENT; ANTERIOR CEREBRAL ARTERY; ARTICLE; BRAIN CIRCULATION; BRAIN INFARCTION; COLLATERAL CIRCULATION; GENETIC VARIABILITY; HEMISPHERE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MORPHOMETRICS; MOUSE; NONHUMAN; POSTERIOR CEREBRAL ARTERY; PRIORITY JOURNAL; STROKE;

ANIMALS; BLOOD VESSELS; CEREBROVASCULAR CIRCULATION; COLLATERAL CIRCULATION; GENETIC VARIATION; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; MICE, INBRED STRAINS; NEOVASCULARIZATION, PHYSIOLOGIC; PIA MATER; REGIONAL BLOOD FLOW; STROKE;

EID: 77952011657     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2010.10     Document Type: Article

References (41)

1. Bang OY, Saver JL, Buck BH, Alger JR, Starkman S, Ovbiagele B, Kim D, Jahan R, Duckwiler GR, Yoon SR, Vinuela F, Liebeskind DS (2008) Impact of collateral flow on tissue fate in acute ischaemic stroke. J Neurol Neurosurg Psychiatry 79:625-9
2. Brozici M, van der Zwan A, Hillen B (2003) Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 34:2750-62
3. Busch HJ, Buschmann IR, Mies G, Bode C, Hossmann KA (2003) Arteriogenesis in hypoperfused rat brain. J Cereb Blood Flow Metab 23:621-8
4. Buschmann IR, Busch HJ, Mies G, Hossmann KA (2003) Therapeutic induction of arteriogenesis in hypoperfused rat brain via granulocyte-macrophage colonystimulating factor. Circulation 108:610-5
5. Carmichael ST (2005) Rodent models of focal stroke: size, mechanism and purpose. NeuroRx 2:396-409
6. Chalothorn D, Clayton JA, Zhang H, Pomp D, Faber JE (2007) Collateral density, remodeling, and VEGF-A expression differ widely between mouse strains. Physiol Genomics 30:179-91
7. Chalothorn D, Faber JE (2009) Differences in collateral formation in the embryo are associated with genetic variation in patterning and maturation of the cerebral cortical circulation. Atheroscler Thromb Vasc Biol 29:e57
8. Chalothorn D, Zhang H, Smith JE, Edwards JE, Faber JE (2009) Chloride intracellular channel-4 is a determinant of native collateral formation in skeletal muscle and brain. Circ Res 105:89-98
9. Christoforidis GA, Karakasis C, Mohammad Y, Caragine LP, Yang M, Slivka AP (2009) Predictors of hemorrhage following intra-arterial thrombolysis for acute ischemic stroke: the role of pial collateral formation. AJNR Am J Neuroradiol 30:165-70
10. Clayton JA, Chalothorn D, Faber JE (2008) Vascular endothelial growth factor-A specifies formation of native collaterals and regulates collateral growth in ischemia. Circ Res 103:1027-36
11. Coyle P (1984) Diameter and length changes in cerebral collaterals after middle cerebral artery occlusion in the young rat. Anat Rec 210:357-64
12. Dodd-o JM, Hristopoulos ML, Welsh-Servinsky LE, Tankersley CG, Pearse DB (2006) Strain-specific differences in sensitivity to ischemia-reperfusion lung injury in mice. J Appl Physiol 100:1590-5
13. Duvernoy HM (1999) Vascularization of the cerebral cortex. Rev Neurol (Paris) 155:684-7
14. Heil M, Eitenmuller I, Schmitz-Rixen T, Schaper W (2006) Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med 10:45-55
15. Heinzer S, Krucker T, Stampanoni M, Abela R, Meyer EP, Schuler A, Schneider P, Muller R (2006) Heirarchical microimaging for multiscale analysis of large vascular networks. Neuroimage 32:626-36
16. Herz RC, Hillen B, Versteeg DH, De Wildt DJ (1998) Collateral hemodynamics after middle cerebral artery occlusion in Wistar and Fischer-344 rats. Brain Res 793:289-96 (Pubitemid 28294096)
17. Heubner O (1874) Die leutischen Erkrankungen der Hirnarterien. Leipzig, Germany: FC Vogel pp 170-214
18. Hoover-Plow J, Shchurin A, Hart E, Sha J, Hill AE, Singer JB, Nadeau JH (2006) Genetic background determines response to hemostasis and thrombosis. BMC Blood Disord 6:6-18
19. Hoover-Plow JL, Gong Y, Shchurin A, Busuttil SJ, Schneeman TA, Hart E (2008) Strain and model dependent differences in inflammatory cell recruitment in mice. Inflamm Res 57:457-63
20. Hossmann KA (2006) Pathophysiology and therapy of experimental stroke. Cell Mol Neurobiol 26:1057-83
21. Hossmann KA, Buschmann IR (2005) Granulocyte-macrophage colony-stimulating factor as an arteriogenic factor in the treatment of ischaemic stroke. Expert Opin Biol Ther 5:1547-56
22. Keum S, Marchuk DA (2009) A locus mapping to murine chromosome 7 determines infarct volume in a mouse model of ischemic stroke. Circ Cardiovasc Genet 2:591-598
23. Liebeskind DS (2005) Collaterals in acute stroke: beyond the clot. Neuroimaging Clin N Am 15:553-73
24. Maeda K, Hata R, Hossmann KA (1998) Differences in the cerebrovascular anatomy of C57black/6 and SV129 mice. Neuroreport 9:1317-9
25. Meier P, Gloekler S, Zbinden R, Beckh S, de Marchi SF, Zbinden S, Wustmann K, Billinger M, Vogel R, Cook S, Wenaweser P, Togni M, Windecker S, Meier B, Seiler C (2007) Beneficial effect of recruitable collaterals: a 10-year follow-up study in patients with stable coronary artery disease undergoing quantitative collateral measurements. Circulation 116:975-83
26. Mohr JP, Choi DW, Grottra JC, Weir B, Wolf PA (2004) Stroke. Pathophysiology, Diagnosis, and Management. Philadelphia, PA: Churchill Livingstone
27. Nakai K, Rogers MS, Baba T, Funakoshi T, Birsner AE, Luyindula DS, D'Amato RJ (2009) Genetic loci that control the size of laser-induced choroidal neovascularization. FASEB J 23:2235-43
28. Payseur BA, Place M (2007) Prospects for association mapping in classical inbred mouse strains. Genetics 175:1999-2008
29. Ringelstein EB, Biniek R, Weiller C, Ammeling B, Nolte PN, Thron A (1992) Type and extent of hemispheric brain infarctions and clinical outcome in early and delayed middle cerebral artery recanalization. Neurology 42:289-98
30. Sa Q, Hart E, Hill AE, Nadeau JH, Hoover-Plow JL (2008) Quantitative trait locus analysis for hemostasis and thrombosis. Mamm Genome 19:406-12
31. Tomita Y, Kubis N, Calando Y, Dinh AT, Meric P, Seylaz J, Pinard E (2005) Long-term in vivo investigation of mouse cerebral microcirculation by fluorescence confocal microscopy in the area of focal ischemia. J Cereb Blood Flow Metab 25:858-67
32. van den Borne SW, van de Schans VA, Strzelecka AE, Vervoort-Peters HT, Lijnen PM, Cleutjens JP, Smits JF, Daemen MJ, Janssen BJ, Blankesteijn WM (2009) Mouse strain determines the outcome of wound healing after myocardial infarction. Cardiovasc Res 84:273-82
33. Van Gieson EJ, Murfee WL, Skalak TC, Price RJ (2003) Enhanced smooth muscle cell coverage of microvessels exposed to increased hemodynamic stresses in vivo. Circ Res 92:929-36
34. + T-cells modulate collateral artery development. Atheroscler Thromb Vasc Biol 27:2310-8
35. Virley D (2005) Choice, methodology, and characterization of focal ischemic stroke models: the search for clinical relevance. Methods Mol Med 104:19-48
36. Wang S, Zhang H, Dai X, Sealock RW, Faber JE (2010) Genetic architecture underlying the native collateral circulation. FASEB J 24 (Suppl 4) : (in press)
37. Wei L, Erinjeri JP, Rovainen CM, Woolsey TA (2001) Collateral growth and angiogenesis around cortical stroke. Stroke 32:2179-84
38. Wellons JC, Sheng H, Laskowitz DT, Machensen GB, Peralstein RD, Warner DS (2000) A comparison of strain-related susceptibility in two murine recovery models of global cerebral ischemia. Brain Res 868:14-21
39. White TA, Pan S, Witt TA, Simari RD (2009) Murine strain differences in hemostasis and thrombosis and tissue factor pathway inhibitor. Thromb Res; gdoi:10.1016/j.thromres.2009.03.006
40. Yamaguchi S, Kobayashi S, Murata A, Yamashita K, Tsunematsu T (1988) Effect of aging on collateral circulation via pial anastomoses in cats. Gerontology 34:157-64
41. Yasargil MG (1987) AVM of the brain-history. In: Microneurosurgery, Vol IIIA (Yasargil MG, ed), New York, NY: Thieme Medical Publ Inc, 12-22