Acellular haemoglobin attenuates hypoxia-inducible factor-1α (HIF-1α) and its target genes in haemodiluted rats

Biochemical Journal

Volumn 414, Issue 3, 2008, Pages 461-469

  Manalo, Dominador J ^a   Buehler, Paul W ^a   Baek, Jin Hyen ^a   Butt, Omer ^a   D'Agnillo, Felice ^a   Alayash, Abdu I ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

Erythropoiesis; Haematocrit; Haemodilution; Haemoglobin (Hb); Hypoxia inducible factor 1 (HIF 1 ); Kidney

Indexed keywords

BLOOD; CHEMOTHERAPY; GENES; HYDRAULIC STRUCTURES; NITRIC OXIDE; NONMETALS; OXYGEN; RATS;

BLOOD LOSS; CELL-FREE; ERYTHROPOIESIS; GENE TRANSCRIPTIONS; HAEMATOCRIT; HAEMODILUTION; HAEMOGLOBIN; HAEMOGLOBIN (HB); HYPOXIA-INDUCIBLE FACTOR 1; KIDNEY; NITRIC-OXIDE SYNTHASE; OXYGEN DEFICITS; OXYGEN-SENSING; OXYGENASE; SHARP INCREASE; TARGET GENES;

TRANSCRIPTION;

BLOOD SUBSTITUTE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ERYTHROPOIETIN; HEME OXYGENASE 1; HEMOGLOBIN; HEMOGLOBIN GLUTAMER 200; HETASTARCH; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ERYTHROPOIESIS; EXCHANGE BLOOD TRANSFUSION; GENE TARGETING; GUINEA PIG; HEMODILUTION; HYPOXIA; KIDNEY PARENCHYMA; MALE; NONHUMAN; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION;

ANIMALS; BLOOD SUBSTITUTES; CELL HYPOXIA; ERYTHROPOIETIN; HEME OXYGENASE (DECYCLIZING); HEMODILUTION; HEMOGLOBINS; HETASTARCH; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY; NITRIC OXIDE SYNTHASE; OXYGEN; RATS; TRANSCRIPTION, GENETIC;

ANIMALIA; RATTUS;

EID: 52449129502     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20080313     Document Type: Article

References (50)

1. Manalo, D. J., Rowan, A., Lavoie, T., Natarajan, L,, Kelly, B. D., Ye. S. Q., Garcia, J. G. N. and Semenza, G. L. (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105, 659-669
2. Elvidge, G. P., Glenny, L., Appelhoff, R. J., Ratcliffe, P. J., Ragoussis, J. and Gleadle, J. M. (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J. Biol. Chem. 281, 15215-15226
3. Semenza, G. L. (2006) Regulation of physiological responses to continuous and intermittent hypoxia by hypoxia-inducible factor 1. Exp. Physiol. 91, 803-806
4. Semenza, G. L. and Prabhakar, N. R. (2007) HIF-1-dependent respiratory, cardiovascular, and redox responses to chronic intermittent hypoxia. Antioxid. Redox Signal. 9, 1391-1396
5. 2 tension. Am. J. Physiol. 271, C1172-C1180
6. 2 tension. Proc. Natl. Acad. Sci. U.S.A. 92, 5510-5514
7. 2-regulated gene expression. FASEB J. 6, 1151-1162
8. Schofield, C. J. and Ratcliffe, P. J. (2004) Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354
9. Schofield, C. J. and Ratcliffe, P. J. (2005) Signalling hypoxia by HIF hydroxylases. Biochem. Biophys. Res. Commun. 338, 617-626
10. Salceda, S. and Caro, J. (1997) Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions: its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272, 22642-22647
11. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 7987-7992
12. Kallio. P. J., Wilson, W. J., O'Brien, S., Makino, Y. and Poellinger, L. (1999) Regulation of the hypoxia-inducible transcription factor 1α by the ubiquitin-proteasome pathway. J. Biol. Chem. 274, 6519-6525
13. Buehler, P. W. and Alayash, A. I. (2005) Redox biology of blood revisited: the role of red blood cells in maintaining circulatory reductive capacity. Antioxid. Redox Signal. 7, 1755-1760
14. McLaren, A. T., Marsden, F. A., Mazer, C. D., Baker, A. J., Stewart, D. J., Tsui, A. K., Li, X., Yucel, Y., Boyd, II, R. M., Liu, E. et al. (2007) Increased expression of HIF-1alpha, nNOS, and VEGF in the cerebral cortex of anemic rats. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 292, R403-R414
15. Kieda, C., Greferath, R., Crola da Silva, C., Fylaktakidou, K. C., Lehn, J. M. and Nicolau, C. (2006) Suppression of hypoxia-induced HIF-1alpha and of angiogenesis in endothelial cells by myo-inositol trispyrophosphate-treated erythrocytes. Proc. Natl. Acad. Sci. U.S.A. 103, 15576-15581
16. Buehler, P. W.. D'Agnillo, F., Hoffman, V. and Alayash, A. I. (2007) Effects of endogenous ascorbate on oxidation, oxygenation, and toxicokinetics of cell-free modified hemoglobin after exchange transfusion in rat and Guinea pig. J. Pharmacol. Exp. Ther, 323, 49-60
17. Henkel-Honke, T. and Oleck, M. (2007) Artificial oxygen carriers: a current review. AANA J. 75, 205-211
18. Lee, H. B. and Blaufox, M. D. (1985) Blood volume in the rat. J. Nucl. Med. 26, 72-76
19. Alayash, A. I., Summers, A. G., Wood, F, and Jia, Y. (2001) Effects of glutaraldehyde polymerization on oxygen transport and redox properties of bovine hemoglobin. Arch. Biochem. Biophys. 391, 225-234
20. Buehler, P. W., Boykins, R. A., Jia, Y., Norris, S., Freedberg, D. I. and Alayash, A. I. (2005) Structural and functional characterization of glutaraldehyde-polymerized bovine hemoglobin and its isolated fractions. Anal. Chem. 77, 3466-3478
21. Salmon, J. B. and Mythen, M. G. (1993) Pharmacology and physiology of colloids. Blood Rev. 7, 114-120
22. Winterbourn, C. C. (1985) Free-radical production and oxidative reactions of hemoglobin. Environ. Health Perspect. 64, 321-330
23. Yeh, L. H. and Alayash, A. I. (2004) Effects of cell-free hemoglobin on hypoxia-inducible factor (HIF-1alpha) and heme oxygenase (HO1) expressions in endothelial cells subjected to hypoxia. Antioxid. Redox Signal. 6, 944-953
24. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12, 149-162
25. Yeo, E. J,, Cho, Y. S., Kim, M. S. and Park, J. W. (2008) Contribution of HIF-1alpha or HIF-2alpha to erythropoietin expression: in vivo evidence based on chromatin immunoprecipitation. Ann. Hematol. 87, 11-17
26. Koury, S, T., Koury, M. J., Bondurant, M. C.. Caro, J. and Gralber, S. E. (1989) Quantitation of erythropoietin-producing cells in kidneys of mice by in situ hybridization: correlation with hematocrit, renal erythropoietin mRNA, and serum erythropoietin concentration. Blood 74, 645-651
27. Cai, Z., Manalo, D. J., Wei, G., Rodriguez, E. R., Fox-Talbot, K., Lu, H., Zweier, J. L. and Semenza, G. L. (2003) Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation 108, 79-85
28. Liu, J., Narasimhan, P., Yu, F. and Chan, P. H. (2005) Neuroprotection by hypoxic preconditioning involves oxidative stress-mediated expression of hypoxia-inducible factor and erythropoietin. Stroke 36, 1264-1269
29. Katz, O., Gil, L., Lifshitz, L., Prutchi-Sagiv, S., Gassmann, M., Mittelman, M. and Neumann, D. (2007) Erythropoietin enhances immune responses in mice. Eur. J. Immunol. 37, 1584-1593
30. Soliz, J., Soulage, C., Hermann, D. M. and Gassmann, M. (2007) Acute and chronic exposure to hypoxia alters ventilatory pattern but not minute ventilation of mice overexpressing erythropoietin. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 293, R1702-R1710
31. Rankin, E. B., Biju, M. R, Liu, O., Unger, T. L., Rha, J., Johnson, R. S., Simon, M. C., Keith, B. and Haase, V. H. (2007) Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J. Clin. Invest. 117, 1068-1077
32. Ou, L. C., Kim, D., Layton, Jr, W. M. and Smith, R. P. (1980) Splenic erythropoiesis in polycythemic response of the rat to high-altitude exposure. J. Appl. Physiol. 48, 857-861
33. Willis, D., Moore, A. R. and Frederick, R. (1996) Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat. Med. 2, 87-90
34. Kapturczak, M. H., Wasserfall, C., Brusko, T., Campbell-Thompson. M., Ellis, T. M., Atkinson, M. A. and Agarwal, A. (2004) Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am. J. Pathol. 165, 1045-1053
35. Nakaso, K., Yano, H., Fukuhara, Y., Takeshima, T., Wada-Isoe, K. and Nakashima, K. (2003) P13K is a key molecule in the Nrf2-mediated regulation of antioxidative proteins by hemin in human neuroblastoma cells. FEBS Left. 546, 181-184
36. Otterbein, L. E., Scares, M. P., Yamashita, K. and Bach, F. H. (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24, 449-455
37. Poss, K. D. and Tonegawa, S. (1997) Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci, U.S.A. 94, 10919-10924
38. Zou, A. P., Yang. Z. Z., Li, P. L. and Cowley, II, A. W. (2001) Oxygen-dependent expression of hypoxia-inducible factor-1alpha in renal medullary cells of rats. Physiol. Genomics 6, 159-168
39. Rosenberger, C., Heyman, S. N., Rosen, S., Shina, A., Goldfarb, M., Griethe, W., Frei, U., Reinke, P., Bachmann, S. and Eckardt, K. U. (2005) Up-regulation of HIF in experimental acute renal failure: evidence for a protective transcriptional response to hypoxia. Kidney Int. 67, 531-542
40. Lee, P. J., Jiang, B. H., Chin, B. Y., Iyer, N. V., Alam, J., Semenza, G. L. and Choi, A. M. (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272, 5375-5381
41. Hill-Kapturczak, N., Thamilselvan, V., Liu, F., Nick, H. S. and Agarwal, A. (2001) Mechanism of heme oxygenase-1 gene induction by curcumin in human renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 281, F851-F859
42. Tsai, P. S., Chen, C. C., Tsai, P. S., Yang, L. C., Huang, W. Y. and Huang, C. J. (2006) Heme oxygenase 1, nuclear factor E2-related factor 2, and nuclear factor kappa B are involved in hemin inhibition of type 2 cationic amino acid transporter expression and L-arginine transport in stimulated macrophages. Anesthesiology 105, 1201-1210
43. Chou, Y. H., Ho, F. M.. Liu, D. Z., Lin, S. Y., Tsai, L. H., Chen, C. H., Ho, Y. S., Hung, L. F. and Liang, Y. C. (2005) The possible role of heat shock factor-1 in the negative regulation of heme oxygenase-1. Int. J. Biochem. Cell Biol. 37, 604-615
44. Vercellotti, G. M., Balla, G., Balla, J., Nath, K., Eaton, J. W. and Jacob, H. S. (1994) Heme and the vasculature: an oxidative hazard that induces antioxidant defenses in the endothelium. Artif. Cells Blood Substit. Immobil. Biotechnol. 22, 207-213
45. John, J. L., Moore, E. E., Gonzales, R. J., Fedel, N., Patrick, D. A. and Silliman. C. C. (2003) Alteration of the post injury hyper-inflammatory response of resuscitation with red cell substitutes. J. Trauma 14, 241-246
46. Palmer, L. A.. Semenza, G. L., Stoler, M. H. and Johns, R. A. (1998) Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am. J. Physiol. 274, L212-L219
47. Coulet, F., Nadaud, S., Agrapar, M. and Soubrier, F. (2003) Identification of hypoxia-response element in the human endothelial nitric-oxide synthase gene promoter. J. Biol. Chem. 278, 46230-46240
48. Lee, R., Neya, K., Svizzero, T. A. and Vlahakes, G. J. (1995) Limitations of the efficacy of hemoglobin-based oxygen-carrying solutions. J. Appl. Physiol. 79, 236-242
49. Bonaventura, C., Henkens, R., Alayash, A. I. and Crumbliss, A. L. (2007) Allosteric effects on oxidative and nitrosative reactions of cell-free hemoglobins. IUBMB Life 59, 498-505
50. Eckardt, K. U., Bernhardt, W., Willam, C. and Wiesener, M. (2007) Hypoxia-inducible transcription factors and their role in renal disease. Semin. Nephrol. 27, 363-372