Increased expression of HIF-1α, nNOS, and VEGF in the cerebral cortex of anemic rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 1, 2007, Pages

  McLaren, Anya T ^a,b   Marsden, Philip A ^a   Mazer, C David ^a,b   Baker, Andrew J ^a   Stewart, Duncan J ^a   Tsui, Albert K Y ^a,b   Li, Xiaomao ^a,c   Yucel, Yeni ^a   Robb, Malcolm ^a   Boyd, Shelley R ^a   Liu, Elaine ^a   Yu, Julie ^a   Hare, Gregory M T ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c SENECA COLLEGE   (Canada)

Author keywords

Cerebral hypoxia; Hemodilution

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; ERYTHROPOIETIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HEMOGLOBIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NEURONAL NITRIC OXIDE SYNTHASE; VASCULOTROPIN;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VOLUME; BRAIN BLOOD VESSEL; BRAIN CELL; BRAIN CORTEX; CONTROLLED STUDY; HEMODILUTION; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANEMIA; ANIMALS; BLOOD PRESSURE; BLOTTING, WESTERN; CEREBRAL CORTEX; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEMODILUTION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; MALE; NITRIC OXIDE SYNTHASE TYPE I; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33846148683     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00403.2006     Document Type: Article

References (53)

1. Agani FH, Puchowicz M, Chavez JC, Pichiule P, LaManna J. Role of nitric oxide in the regulation of HIF-1α expression during hypoxia. Am J Physiol Cell Physiol 283: C178-C186, 2002.
2. Bernaudin M, Nedelec AS, Divoux D, Mackenzie ET, Petit E, Schumann-Bard P. Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. J Cereb Blood Flow Metab 22: 393-403, 2002.
3. Brune B, Zhou J. The role of nitric oxide (NO) in stability regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Curr Med Chem 10: 845-855, 2003.
4. Cabrales P, Intaglietta M, Tsai AG. Increase plasma viscosity sustains microcirculation after resuscitation from hemorrhagic shock and continuous bleeding. Shock 23: 549-555, 2005.
5. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36: 827-835, 2004.
6. Carson JL, Poses RM, Spence RK, Bonavita G. Severity of anaemia and operative mortality and morbidity. Lancet 1: 727-729, 1988.
7. Castro-Blanco S, Encinas JM, Serrano J, Alonso D, Gomez MB, Sanchez J, Rios-Tejada F, Fernandez-Vizarra P, Fernandez AP, Martinez-Murillo R, Rodrigo J. Expression of nitrergic system and protein nitration in adult rat brains submitted to acute hypobaric hypoxia. Nitric Oxide 8: 182-201, 2003.
8. Cholet N, Seylaz J, Lacombe P, Bonvento G. Local uncoupling of the cerebrovascular and metabolic responses to somatosensory stimulation after neuronal nitric oxide synthase inhibition. J Cereb Blood Flow Metab 17: 1191-1201, 1997.
9. Chow J, Ogunshola O, Fan SY, Li Y, Ment LR, Madri JA. Astrocyte-derived VEGF mediates survival and tube stabilization of hypoxic brain microvascular endothelial cells in vitro. Brain Res Dev Brain Res 130: 123-132, 2001.
10. Dery MA, Michaud MD, Richard DE. Hypoxia-inducible factor 1: regulation by hypoxic and nonhypoxic activators. Int J Biochem Cell Biol 37: 535-540, 2005.
11. Di GC, Bianchi G, Cacchio M, Macri MA, Ferrero G, Rapino C, Verratti V, Piccirilli M, Artese L. Carotid body HIF-1alpha, VEGF and NOS expression during aging and hypoxia. Adv Exp Med Biol 536: 603-610, 2003.
12. Dunne JR, Malone D, Tracy JK, Gannon C, Napolitano LM. Perioperative anemia: an independent risk factor for infection, mortality, and resource utilization in surgery. J Surg Res 102: 237-244, 2002.
13. Dunst J, Becker A, Lautenschlager C, Markau S, Becker H, Fischer K, Haensgen G. Anemia and elevated systemic levels of vascular endothelial growth factor (VEGF). Strahlenther Onkol 178: 436-441, 2002.
14. Encinas JM, Fernandez AP, Salas E, Castro-Blanco S, Munoz P, Rodrigo J, Serrano J. Nitric oxide synthase and NADPH-diaphorase after acute hypobaric hypoxia in the rat caudate putamen. Exp Neurol 186: 33-45, 2004.
15. Fischer S, Wobben M, Marti HH, Renz D, Schaper W. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc Res 63: 70-80, 2002.
16. Garthwaite G, Bartus K, Malcolm D, Goodwin D, Kollb-Sielecka M, Dooldeniya C, Garthwaite J. Signaling from blood vessels to CNS axons through nitric oxide. J Neurosci 26: 7730-7740, 2006.
17. Guo Y, Ward ME, Beasjours S, Mori M, Hussain SN. Regulation of cerebellar nitric oxide production in response to prolonged in vivo hypoxia. J Neurosci Res 49: 89-97, 1997.
18. Habib RH, Zacharias A, Schwann TA, Riordan CJ, Durham SJ, Shah A. Adverse effects of low hematocrit during cardiopulmonary bypass in the adult: should current practice be changed? J Thorac Cardiovasc Surg 125: 1438-1450, 2003.
19. Hagen T, Taylor CT, Lam F, Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302: 1975-1978, 2003.
20. Hare GMT, Mazer CD, Mak W, Gorczynski RM, Hum KM, Kim SY, Wyard L, Barr A, Qu R, Baker AJ. Hemodilutional anemia is associated with increased cerebral neuronal nitric oxide synthase gene expression. J Appl Physiol 94: 2058-2067, 2003.
21. Homi HM, Yang H, Pearlstein RD, Grocott HP. Hemodilution during cardiopulmonary bypass increases cerebral infarct volume after middle cerebral artery occlusion in rats. Anesth Analg 99: 974-981, 2004.
22. Huang LE, Willmore WG, Gu J, Goldberg MA, Bunn HF. Inhibition of hypoxia-inducible factor 1 activation by carbon monoxide and nitric oxide. Implications for oxygen sensing and signaling. J Biol Chem 274: 9038-9044, 1999.
23. Hudetz AG, Wood JD, Kampine JP. 7-Nitroindazole impedes erythrocyte flow response to isovolemic hemodilution in the cerebral capillary circulation. J Cereb Blood Flow Metab 20: 220-224, 2000.
24. Jin KL, Mao XO, Greenberg DA. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci USA 97: 10242-10247, 2000.
25. Jonas RA, Wypij D, Roth SJ, Bellinger DC, Visconti KJ, du Plessis AJ, Goodkin H, Laussen PC, Farrell DM, Bartlett J, McGrath E, Rappaport LJ, Bacha EA, Forbess JM, del Nido PJ, Mayer JE Jr, and Newburger JW. The influence of hemodilution on outcome after hypothermic cardiopulmonary bypass: results of a randomized trial in infants. J Thorac Cardiovasc Surg 126: 1765-1774, 2003.
26. Kalaria RN, Spoors L, Laude EA, Emery CJ, Thwaites-Bee D, Fairlie J, Oakley AE, Barer DH, Barer GR. Hypoxia of sleep apnoea: cardiopulmonary and cerebral changes after intermittent hypoxia in rats. Respir Physiol Neurobiol 140: 53-62, 2004.
27. Kido M, Du L, Sullivan CC, Li X, Deutsch R, Jamieson SW, Thistlethwaite PA. Hypoxia-inducible factor 1-alpha reduces infarction and attenuates progression of cardiac dysfunction after myocardial infarction in the mouse. J Am Coll Cardiol 46: 2116-2124, 2005.
28. Lipton AJ, Johnson MA, MacDonald T, Lieberman MW, Gozal D, Gaston B. S-nitrosothiols signal the ventilatory response to hypoxia. Nature 413: 171-174, 2001.
29. Marti HJ, 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 156: 965-976, 2000.
30. Matsuoka T, Saiki C, Mortola JP. Metabolic and ventilatory responses to anemic hypoxia in conscious rats. J Appl Physiol 77: 1067-1072, 1994.
31. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 182: 1683-1693, 1995.
32. Metzen E, Zhou J, Jelkmann W, Fandrey J, Brune B. Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases. Mol Biol Cell 14: 3470-3481, 2003.
33. Nag S, Eskandarian MR, Davis J, Eubanks JH. Differential expression of vascular endothelial growth factor-A (VEGF-A) and VEGF-B after brain injury. J Neuropathol Exp Neurol 61: 778-788, 2002.
34. Ogunshola OO, Stewart WB, Mihalcik V, Solli T, Madri JA, Ment LR. Neuronal VEGF expression correlates with angiogenesis in postnatal developing rat brain. Brain Res Dev Brain Res 119: 139-153, 2000.
35. Ortiz PA, Garvin JL. Cardiovascular and renal control in NOS-deficient mouse models. Am J Physiol Regul Integr Comp Physiol 284: R628-R638, 2003.
36. Palmer LA, Gaston B, Johns RA. Normoxic stabilization of hypoxia-inducible factor-1 expression and activity: redox-dependent effect of nitrogen oxides. Mol Pharmacol 58: 1197-1203, 2000.
37. Pichiule P, LaManna JC. Angiopoietin-2 and rat brain capillary remodeling during adaptation and deadaptation to prolonged mild hypoxia. J Appl Physiol 93: 1131-1139, 2002.
38. Rakusan K, Cicutti N, Kolar F. Effect of anemia on cardiac function, microvascular structure, and capillary hematocrit in rat hearts. Am J Physiol Heart Circ Physiol 280: H1407-H1414, 2001.
39. Renshaw GM, Dyson SE. Increased nitric oxide synthase in the vasculature of the epaulette shark brain following hypoxia. Neuroreport 10: 1707-1712, 1999.
40. Scharte M, Han X, Bertges DJ, Fink MP, Delude RL. Cytokines induce HIF-1 DNA binding and the expression of HIF-1-dependent genes in cultured rat enterocytes. Am J Physiol Gastrointest Liver Physiol 284: G373-G384, 2003.
41. Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, Rapisarda A, Bernasconi S, Saccani S, Nebuloni M, Vago L, Mantovani A, Melillo G, Sica A. Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 198: 1391-1402, 2003.
42. Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 125: 2549-2557, 2002.
43. Shen H, Greene AS, Stein EA, Hudetz AG. Functional cerebral hyperemia is unaffected by isovolemic hemodilution. Anesthesiology 96: 142-147, 2002.
44. Sogawa K, Numayama-Tsuruta K, Ema M, Abe M, Abe H, Fujii-Kuriyama Y. Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc Natl Acad Sci USA 95: 7368-7373, 1998.
45. Thompson JK, Peterson MR, Freeman RD. Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299: 1070-1072, 2003.
46. Tsai AG, Acero C, Nance PR, Cabrales P, Frangos JA, Buerk DG, Intaglietta M. Elevated plasma viscosity in extreme hemodilution increases perivascular nitric oxide concentration and microvascular perfusion. Am J Physiol Heart Circ Physiol 288: H1730-H1739, 2005.
47. Van Bommel J, Trouwborst A, Schwarte L, Siegemund M, Ince C, Henny C. Intestinal and cerebral oxygenation during severe isovolemic hemodilution and subsequent hyperoxic ventilation in a pig model. Anesthesiology 97: 660-670, 2002.
48. Wang FS, Kuo YR, Wang CJ, Yang KD, Chang PR, Huang YT, Huang HC, Sun YC, Yang YJ, Chen YJ. Nitric oxide mediates ultrasound-induced hypoxia-inducible factor-1alpha activation and vascular endothelial growth factor-A expression in human osteoblasts. Bone 35: 114-123, 2004.
49. Wang Y, Liu XF, Cornish KG, Zucker IH, Patel KP. Effects of nNOS antisense in the paraventricular nucleus on blood pressure and heart rate in rats with heart failure. Am J Physiol Heart Circ Physiol 288: H205-H213, 2005.
50. Ward ME, Toporsian M, Scott JA, Teoh H, Govindaraju V, Quan A, Wener AD, Wang G, Bevan SC, Newton DC, Marsden PA. Hypoxia induces a functionally significant and translationally efficient neuronal NO synthase mRNA variant. J Clin Invest 115: 3128-3139, 2005.
51. Weiskopf RB, Kramer JH, DP, Viele M, Neumann M, Feiner JR, Watson JJ, Hopf HW, Toy P. Acute severe isovolemic anemia impairs cognitive function and memory in humans. Anesthesiology 92: 1646-1652, 2000.
52. Yang G, Zhang Y, Ross ME, Iadecola C. Attenuation of activity-induced increases in cerebellar blood flow in mice lacking neuronal nitric oxide synthase. Am J Physiol Heart Circ Physiol 285: H298-H304, 2003.
53. Zhang ZG, Zhang L, Tsang W, Soltanian-Zadeh H, Morris D, Zhang R, Goussev A, Powers C, Yeich T, Chopp M. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 22: 379-392, 2002.