Defining the critical hypoxic threshold that promotes vascular remodeling in the brain

Experimental Neurology

Volumn 263, Issue , 2015, Pages 132-140

  Boroujerdi, Amin ^a   Milner, Richard ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Angiogenesis; Arteriogenesis; Blood brain barrier (BBB); Dose response; Endothelial cells; Fibronectin; Hypoxic threshold; Vascular remodeling; 5 integrin

Indexed keywords

CLAUDIN 5; ENDOGLIN; FIBRONECTIN; VERY LATE ACTIVATION ANTIGEN 5;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HYPOXIA; CELL HYPERPLASIA; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CEREBROVASCULAR REMODELING; CONTROLLED STUDY; ENDOTHELIUM CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BRAIN; C57BL MOUSE; IMMUNOHISTOCHEMISTRY; ISCHEMIC PRECONDITIONING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; VASCULAR REMODELING; VASCULARIZATION;

ANIMALS; BRAIN; CELL PROLIFERATION; ENDOTHELIAL CELLS; HYPOXIA, BRAIN; IMMUNOHISTOCHEMISTRY; ISCHEMIC PRECONDITIONING; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; VASCULAR REMODELING;

EID: 84949117598     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.10.007     Document Type: Article

References (39)

1. Ainslie P.N., Ogoh S. Regulation of cerebral blood flow in mammals during chronic hypoxia: a matter of balance. Exp. Physiol. 2009, 95:251-262.
2. Ballabh P., Braun A., Nedergaard M. The blood-brain barrier: an overview. Structure, regulation and clinical implications. Neurobiol. Dis. 2004, 16:1-13.
3. Boroujerdi A., Welser-Alves J., Tigges U., Milner R. Chronic cerebral hypoxia promotes arteriogenic remodeling events that can be identified by reduced endoglin (CD105) expression and a switch in β1 integrins. J. Cereb. Blood Flow Metab. 2012, 32:1820-1830.
4. Brown W.R., Moody D.M., Thore C.R., Anstrom J.A., Challa V.R. Microvascular changes in the white matter in dementia. J. Neurol. Sci. 2009, 283:28-31.
5. Buschmann I.R., Busch H.-J., Mies G., Hossmann K.-A. Therapeutic induction of arteriogenesis in hypoperfused rat brain via granulocyte-macrophage colony-stimulating factor. Circulation 2003, 108:610-615.
6. Chavez J.C., Agani F., Pichiule P., LaManna J.C. Expression of hypoxic inducible factor 1α in the brain of rats during chronic hypoxia. J. Appl. Physiol. 2000, 89:1937-1942.
7. del Zoppo G.J., Hallenbeck J.M. Advances in the vascular pathophysiology of ischemic stroke. Thromb. Res. 2000, 98:V73-V81.
8. del Zoppo G.J., Copeland B.R., Harker L.A., Waltz T.A., Zyroff J., Hanson S.R., Battenberg E. Experimental acute thrombotic stroke in baboons. Stroke 1986, 17:1254-1265.
9. Dirnagl U., Iadecola C., Moskowitz M.A. Pathophysiology of ischemic stroke: an integrated view. Trends Neurosci. 1999, 22:391-397.
10. Dirnagl U., Simon R.P., Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 2003, 26:248-254.
11. Dore-Duffy P., Wencel M., Katyshev V., Cleary K. Chronic mild hypoxia ameliorates chronic inflammatory activity in myelin oligodendrocyte glycoprotein (MOG) peptide induced experimental autoimmune encephalomyelitis (EAE). Adv. Exp. Med. Biol. 2011, 701:165-173.
12. Dunn J.F., Wu Y., Zhao Z., Srinivasan S., Natah S.J. Training the brain to survive stroke. PLoS ONE 2012, 7:e45108.
13. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1995, 1:27-31.
14. Freitas-Andrade M., Carmeliet P., Charlebois C., Stanimirovic D.B., Moreno M.J. PlGF knockout delays brain vessel growth and maturation upon systemic hypoxic challenge. J. Cereb. Blood Flow Metab. 2011, 32:663-675.
15. Gay D., Esiri M. Blood-brain barrier damage in acute multiple sclerosis plaques. Brain 1991, 114:557-572.
16. Ju X., Mallet R.T., Metzger D.B., Jung M.E. Intermittent hypoxia conditioning protects mitochondrial cytochrome c oxidase od rat cerebellum from ethanol withdrawal stress. J. Appl. Physiol. 2012, 112:1706-1714.
17. Kirk J., Plumb J., Mirakhur M., McQuaid S. Tight junction abnormality in multiple sclerosis white matter affects all calibres of vessel and is associated with blood-brain barrier leakage and active demyelination. J. Pathol. 2003, 201:319-327.
18. Kuo N.-T., Benhayon D., Przybylski R.J., Martin R.J., LaManna J.C. Prolonged hypoxia increases vascular endothelial growth factor mRNA and protein in adult mouse brain. J. Appl. Physiol. 1999, 86:260-264.
19. Kupper T., Milledge J.S., Hillebrandt D., Kubalova J., Hefti U., Basnyat B., Giesler U., Pullan R., Schoffl V. Work in hypoxic conditions-consensus statement of the medical commission of the Union Internationale des Associations d'Alpinisme (UIAA MedCom). Ann. Occup. Hyg. 2011, 55:369-386.
20. LaManna J.C., Vendel L.M., Farrell R.M. Brain adaptation to chronic hypobaric hypoxia in rats. J. Appl. Physiol. 1992, 72:2238-2243.
21. LaManna J.C., Chavez J.C., Pichiule P. Structural and functional adaptation to hypoxia in the rat brain. J. Exp. Biol. 2004, 207:3163-3169.
22. Li L., Welser J.V., Dore-Duffy P., Del Zoppo G.J., LaManna J.C., Milner R. In the hypoxic central nervous system, endothelial cell proliferation is followed by astrocyte activation, proliferation, and increased expression of the α6β4 integrin and dystroglycan. Glia 2010, 58:1157-1167.
23. Li L., Welser-Alves J.V., van der Flier A., Boroujerdi A., Hynes R.O., Milner R. An angiogenic role for the α5β1 integrin in promoting endothelial cell proliferation during cerebral hypoxia. Exp. Neurol. 2012, 237:46-54.
24. McCaffrey G., Willis C.L., Staatz W.D., Nametz N., Quigley C.A., Hom S., Lochhead J.J., Davis T.P. Occludin oligomeric assemblies at tight junctions of the blood-brain barrier are altered by hypoxia and reoxygenation stress. J. Neurochem. 2009, 110:58-71.
25. Miller B.A., Perez R.S., Shah A.R., Gonzales E.R., Park T.S., Gidday J.M. Cerebral protection by hypoxic preconditioning in a murine model of focal ischemia-reperfusion. Neuroreport 2001, 12:1663-1669.
26. Milner R., Campbell I.L. Developmental regulation of β1 integrins during angiogenesis in the central nervous system. Mol. Cell. Neurosci. 2002, 20:616-626.
27. Milner R., Hung S., Erokwu B., Dore-Duffy P., LaManna J.C., del Zoppo G.J. Increased expression of fibronectin and the α5β1 integrin in angiogenic cerebral blood vessels of mice subject to hypobaric hypoxia. Mol. Cell. Neurosci. 2008, 38:43-52.
28. Minhajat R., Mori D., Yamasaki F., Sugita Y., Satoh T., Tokunaga O. Organ-specific endoglin (CD105) expression in the angiogenesis of human cancers. Pathol. Int. 2006, 56:717-723.
29. Pardridge W.M. Blood-brain barrier drug targeting: the future of brain drug development. Mol. Med. 2003, 3:90-105.
30. Persson A.B., Buschmann I.R. Vascular growth in health and disease. Fronts Mol. Neurosci. 2011, 4:1-15.
31. Pichiule P., LaManna J.C. Angiopoietin-2 and rat brain capillary remodeling during adaptation and de-adaptation to prolonged mild hypoxia. J. Appl. Physiol. 2002, 93:1131-1139.
32. Pichiule P., Chávez J.C., Xu K., LaManna J.C. Vascular endothelial growth factor upregulation in transient global ischemia induced by cardiac arrest and resuscitation in rat brain. Brain Res. Mol. Brain Res. 1999, 74:83-90.
33. Sidky Y.A., Borden E.C. Inhibition of angiogenesis by interferons: effects on tumor- and lymphocyte-induced vascular responses. Cancer Res. 1987, 47:5155-5161.
34. Stowe A.M., Altay T., Freie A.B., Gidday J.M. Repetitive hypoxia extends endogenous neurovascular protection for stroke. Ann. Neurol. 2011, 69:975-985.
35. 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.
36. Willis C.L., Meske D.S., Davis T.P. Protein kinase C activation modulates reversible increase in cortical blood-brain barrier permeability and tight junction protein expression during hypoxia and posthypoxic reoxygenation. J. Cereb. Blood Flow Metab. 2010, 30:1847-1859.
37. Yao Y., Kubota T., Takeuchi H., Sato K. Prognostic significance of microvessel density determined by an anti-CD105/endoglin monoclonal antibody in astrocytic tumors: comparison with an anti-CD31 monoclonal antibody. Neuropathology 2005, 25:201-206.
38. Zhu X.H., Yan H.C., Zhang J., Qu H.D., Qiu X.S., Chen L., Li S.J., Cao X., Bean J.C., Chen L.H., others Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J. Neurosci. 2010, 30:12653-12663.
39. Zlokovic B.V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 2011, 12:723-738.