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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2002; 48(5): 79-92


HEME OXYGENASE AND CARBON MONOXIDE: THE PROTECTION OR THE INJURY OF THE CELLS?

T.V.Kukoba, A.A.Moibenko

    A.A.Bogomoletz Institute of Physiology, National Academy of Sciences of Ukraine, Kiуv.


Abstract

Heme oxygenase (HO) catalyzes the conversion of heme to carbon monoxide, iron, and biliverdin, which is immediately reduced to bilirubin. Three HO active isozymes exist: HO-1, an inducible heat shock protein (HSP32), and HO-2 and HO-3, which are constitutive and highly concentrated in neurons, spleen and liver. Heme oxygenase-1 is an inducible enzyme that catalyzes heme degradation and has been proposed to play a role in protecting cells against oxidative stress-related injury. The mechanism(s) of protection is not completely elucidated, although it is suggested that one or more of the catalytic by-products provide antioxidant functions either directly or indirectly. The role played by heme oxygenase in tissue pathology is determined by a delicate balance between the injurious and protective actions of heme, bilirubin, CO, and Fe2+. Autors review the functional role of HO and its derivates in cells biology and its real potential application to pathological conditions.

Keywords: HEME OXYGENASE, CARBON MONOXIDE, PROTECTION OR THE INJURY

References

  1. Agarwal A., Kim Y., Matas A.J. et al. Gas-generating systems in acute renal allograft rejection in the rat: co-induction of heme oxygenase and nitric oxide synthase // Transplantation. – 1996. – 61, № 1. – P. 93-98.
  2. Balla J., Jacob H.S., Balla G. et al. Endothelialcell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage // Proc. Natl. Acad. Sci. USA – 1993. –90, № 20. – P. 9285-9289.
  3. Balla G., Jacob H.S., Balla J. Induction of endothelial ferritin: a cytoprotective antioxidant stratagem of the vessel wall // J. Biol. Chem. – 1992. –267, № 25. – P. 18148-18153.
  4. Baraсano D.E., Snyder H.H. Neural roles for heme oxygenase: Contrasts to nitric oxide synthase //Proc. Natl. Acad. Sci. USA. – 2001. – 98, Issue 20, September 25. – P. 10996-11002.
  5. Baraсano D.E., Wolosker H., Bae B.-Il. et al. Mammalian Iron ATPase Induced by Iron // J. Biol. Chem. – 2000. – 275, Issue 20, May, 19. –P. 15166-15173.
  6. Battish R., Cao G-Y., Lynn R.B. et al. Heme Oxygenase-2 distribution in anorectum: colocalisation with neuronal nitric oxide synthase // Amer. J. Physiol. Gasterointest. Liver Prysiol. –2000. – 278. – P. G 148-G155.
  7. Benjamin I.J., McMillan D.R. Stress (Heat Shock )Proteins Molecular Chaperones in Cardiovascular Biology and Disease // Circulat. Res. – 1998. –83, № 2. – P. 117–132.
  8. Brouard S., Otterbein L.E., Anrather J. et al. Carbon Monoxide Generated by Heme Oxygenase 1 Suppresses Endothelial Cell Apoptosis //J. Exp. Med. – 2000. – 192, № 7. – P. 1015–1026.
  9. 9. Cardell L.O., Lou Y.P., Takeyama K. et al. Carbon monoxide, a cyclic GMP-related messenger, involved in hypoxic bronchodilation in vivo // Pulm.Pharmacol. Therap. – 1998. – 11, № 4. – P. 309-315.
  10. 10. Carraway M.S., Ghio A.J., Carter J.D. et al. Expression of heme oxygenase-1 in the lung in chronic hypoxia // Amer. J. Physiol. Lung.Cell. Mol. Physiol. – 2000. – 278, № 4. –P. L806–L812.
  11. Chen K., Gunter K., Maines M.D. Neurons overexpressing heme oxygenase-1 resist oxidative stressmediated cell death // J. Neurochem. – 2000. –75, № 1. – P. 304–313.
  12. Chen W., Hunt D.M., Lu H. et al. Expression of antioxidant protective proteins in the rat retina during prenatal and postnatal development //Invest. Opthalmol. Vis. Sci. – 1999. – 40, № 3. –P. 744–751.
  13. Choi, A. M.K. Heme Oxygenase-1 Protects the Heart / Circulat.Res. – 2001. – 89, July,20. – P. 105–107.
  14. Clark J.E., Foresti R., Sarathchandra P. et al.Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction // Amer.J.Physiol. – 2000. – 278, Issue 2. – P. H643–H651.
  15. Coceani F. Carbon Monoxide in Vasoregulation.The Promise and the Challenge // Circulat. Res. –2000. – 86, № 12. – P. 1184 – 1186.
  16. Cruse I., Maines M.D. Evidence suggesting that the two forms of heme oxygenase are products of different genes // J. Biol. Chem. – 1988. – 263,№ 7. – P. 3348-3353.
  17. Csonka C., Varga E., Kovacs. P. et al. Heme oxygenase and cardiac function in ischemic/reperfused rat hearts // Free Rad. Biol. Med. – 1999. –27, № 1–2. – P. 119–126.
  18. Ding Y., McCoubrey W.K., Maines M.D. Interaction of heme oxygenase-2 with nitric oxide donors // Eur.J. Biochem. – 1999. – 264, № 9. – P. 854–861.
  19. 19. Doi K., Akaike T., Fujii S. et al. Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth // Brit. J. Cancer. – 1999. – 80,№ 12. – P. 1945–1954.
  20. 20. Dong Z., Lavrovsky Y., Venkatachalam M.A. et al. Heme Oxygenase-1 in Tissue Pathology // Amer.J. Phatol. – 2000. – 156, № 5. – P. 1485–1488.
  21. Dorй S., Takahashi M., Ferris C.D. et al. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury // Neurobiology. – 1999. – 96, Issue 5,March 2. – P. 2445–2450.
  22. Downard P.J., Wilson M.A., Spain D.A. et al. Heme oxygenase-dependent carbon monoxide production is a hepatic adaptive response to sepsis //J. Surg. Res. – 1997. – 71, № 1. – P. 7–12.
  23. Durante W., Kroll M.H., Christodoulides N. et al. Nitric Oxide Induces Heme Oxigenase-1 Gene Expression and Carbon Monoxide Production in Vascular Smooth Muscle Cells // Circulat. Res. –1997 – 80, № 4. – P. 557-564.
  24. Duke H.N., Killick E.M. Pulmonary vasomotor responses of isolated perfused cat lungs to anoxia // J. Physiol. – 1952. – 117. – P. 303–316.
  25. Eisenstein R.S., Garcia-Mayol D., Pettingell W. et al. Regulation of ferritin and heme oxygenase in rat fibroblasts by different forms of iron // Proc. Natl.Acad. Sci. USA. – 1991. - 88, № 2. – P. 688-692.
  26. Elbirt K.K., Whitmarsh A.J., Davis R.J. et al. Mechanism of Sodium Arsenite-mediated Induction of Heme Oxygenase-1 in Hepatoma Cells. Role of mitogen-activated protein kinases // J. Biol. Chem. –1998. – 273, Issue 15, April 10. – P. 8922–8931.
  27. Ernst A., Zibrak J.D. Carbon monoxide poisoning // N. Engl. J. Med. – 1998. – 339, № 22. – P. 1603–1608.
  28. Foresti R., Clark J.E., Green C.J. et al. Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells.Involvement of superoxide and peroxynitrite anions// J. Biol. Chem. – 1997. – 272, Issue 7. –P. 18411-18417.
  29. 29. Foresti, R., Sarathchandra P., Clark J.E. et al. Peroxynitrite induces haem oxygenase-1 in vascular endothelial cells: a link to apoptosis // Biochem. J. – 1999. – 339, May 1 (Pt 3). – P. 729–736.
  30. 30. Furchgott R.F., Jothianandan D. Endotheliumdependent and independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide,carbon monoxide and light // Blood. Vessels. –1991. – 28, № 1–3. – P. 52–61.
  31. Geddes J.W., Pettigrew L.C., Holtz M.L. et al. Permanent focal and transient global cerebral ischemia increase glial and neuronal expression of heme oxygenase1, but not heme oxygenase-2, protein in rat brain //Neurosci. Lett. – 1996. – 210, № 3. – P.205- 208.
  32. Gong P., Hu B., Stewart D. et al. Cobalt induceheme oxygenase-1 expression by a hypoxia-inducible factor-independent mechanism in Chinese hamster ovary cells: regulation by Nrf2 and MafG transcription factors // J.Biol.Chem.–2001. – 276(29), № 8 – P. 27018–27025.
  33. Gopinathan V., Miller N.J., Milner A.D. et al.Bilirubin and ascorbate antioxidant activity in neonatal plasma // FEBS Lett. – 1994. – 349,№ 2. – P. 197–200.
  34. Hangaishi M, Ishizaka N, Aizawa T. et al. Induction of heme oxygenase-1 can act protectively against cardiac ischemia/reperfusion in vivo // Biochem. and Biophys. Res. Commun. – 2000. – 279,№ 2. – P. 582–588.
  35. Henningsson R., Alm P., Lundquist I. Occurrence and putative hormone regulatory function of a constitutive heme oxygenase in rat pancreatic islets // Amer. J. Physiol. Cell. Physiol. – 1997. –273, № 2 (Pt 1). – P. C703-C709.
  36. Horvath I., Donnelly L.E., Kiss A. et al. Raised levels of exhaled carbon monoxide are associated with an increased expression of heme oxygenase-1 in airway macrophages in asthma: a new marker of oxidative stress // Thorax. – 1998. – 53,№ 8. – P. 668-672.
  37. Ishizaka N., de Leon H., Laursen J.B. et al. Angiotensin II-induced hypertension increases heme oxygenase-1 expression in rat aorta // Circulation. – 1997. – 96, № 6. – P. 1923–1929.
  38. Jandl J.H. Physiology of red cells. – In: Blood. –textbook of hematology / Ed. J.H.Jandl. – Boston:Mass, 1987. – P. 89–92.
  39. 39. Johnson R.A., Lavesa M., Askari B. et al. A heme oxygenase product, presumably carbon monoxide, mediates a vasodepressor function in rats //Hypertension. – 1995. – 25, №2. – P.166–169.
  40. 40. Keyse S.M. Tyrrell R.M. Heme oxygenase is the major 32-KDA stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite // Proc. Natl. Acad.Sci. USA. – 1989. – 86, № 1. – P. 99–103.
  41. Lee P.J., Alam J., Wiegand G.W. et al. Overexpression of heme oxygenase-1 expression in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia //Ibid. – 1996. – 93, № 19. – P. 10393–10398.
  42. Levere R.D., Staudinger R., Loewy G. et al. Elevated levels of heme oxygenase activity and mRNA in peripheral blood adherent cells of acquired immunodeficiency syndrome patients // Amer. J. Hematol. – 1993. – 43, № 1. – P. 19–23.
  43. Llesuy S.F., Tomaro M.L. Heme oxygenase and oxidative stress. Evidence of involvement of bilirubin as physiological protector against oxidative damage // Biochim. and Biophys. Acta. –1994. –1223, № 1. – P. 9–14.
  44. Maines M.D., Mayer R.D., Ewing J.F. et al. Induction of kidney heme oxygenase-1 (HSP32) mRNA and protein by ischemia/reperfusion: possible role of heme as both promotor of tissue damage and regulator of HSP32 // J.Pharmacol. Exp.Therap. 1993. – 264, № 1. – P. 457–462.
  45. Maines M.D. Heme Oxygenase: Clinical Applications and Functions. Inc. Boca Ration, FL: Press CRC, – 1992. – 266 p.
  46. Maines M.D., Panahian N. The heme oxygenase system and cellular defense mechanisms. Do HO-1and HO-2 have different functionsα // Adv. Exp.Med. Biol. – 2001. – 502, № 2. – P. 49–72.
  47. Maines M. D. The heme oxygenase system: a regulator of second messenger gases // Ann. Rev. Pharmacol.Toxicol. – 1997. – 37, № 1. – P. 517–554.
  48. Maines M.D., Trakshel G.M. Kutty R.K. Characterization of two constitutive forms of rat liver microsomal heme oxygenase: Only one molecular species of the enzyme is inducible // J. Biol.Chem. – 1986. – 261, № 1. – P. 411–419.
  49. 49. Maines M.D., Raju V.S., Panahian N. Spin Trap (N-t-butil-a-phenylnitrone)-Mediated Suprainduction of Heme Oxigenase-1 in Kidney Ischemia / Reperfusion Model: Role of the Oxygenase in Protection against Oxidative Injury // Pharmacology. – 1999. – 291, № 2. – P. 911–919.
  50. 50. Marber M. S., Latchman D. S., Walker J. M. et al. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction // Circulation. – 1993. – 88, № 3. – P. 1264–1272.
  51. Marks G.S. Heme oxygenase: the physiological role of one of its metabolites, carbon monoxide and interactions with zinc protoporphyrin, cobalt protoporphyrin and other metalloporphyrins // Cell. Mol. Biol. – 1994. – 40, № 7. – P. 863–870.
  52. Maulik N., Sharma H.S., Das D.K. Induction of the haem oxygenase gene expression during the reperfusion of ischemic rat myocardium // J. Mol.Cell. Cardiol. – 1996. – 28, № 6. – P. 1261–1270.
  53. Mautes A.E., Kim D.H., Sharp F.R. et al. Induction of heme oxygenase-1 (HO-1) in the contused spinal cord of the rat // Brain Res. – 1998. –795, № 1-2. – P. 17-24.
  54. McCoubrey W.K., Huang T.J., Maines M.D. Isolatoin and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3 // Eur. J. Biochem. – 1997. – 247, № 2. –P. 725-732.
  55. Mireles L.C., Lum M.A., Dennery P.A. Anti- oxidant and cytotoxic effects of bilirubin on neonatal erythrocytes // Pediatr. Res. 1999. – 45,№ 3. – P. 355–436.
  56. Moray R. A relation of persons killed with subterraneous damps // Phil. Trans. Roy. Soc. London. - 1665. – 1. – P. 44-45.
  57. Motterlini R., Foresti R., Bassi R. et al. Endothelial Heme Oxygenase-1 Induction by Hypoxia // J. Biol. Chem. – 2000. - 275, Issue 18, № 5. –P. 13613–13620.
  58. Motterlini R., Foresti R., Intaglietta M. et al. Oxidative-stress response in vascular endothelial cells exposed to acellular hemoglobin solutions //Amer. J. Physiol. Heart Circulat. Physiol. – 1995. –269, № 2 (Pt 2). – P. H648–H655.
  59. 59. Motterlini R., Foresti R, Intaglietta M. et al. NOmediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium // Ibid. – 1996 – 270, № 1 (Pt 2). –P. H107–H114.
  60. 60. Motterlini R., Gonzales A., Foresti R. et al. Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo // Circulat. Res. – 1998. – 83, № 9. –P. 568–577.
  61. Nathanson J.A., Scavone C., Scalon C. et al. The cellular Na+ pump as a site of action for carbon monoxide and glutamate: for long-term modulation of cellular activity // Neuron.. – 1995. – 14,№ 1. – P. 781–794.
  62. Nath K.A., Balla G., Vercellotti G.M. et al. Induction of heme oxygenase is a rapid protectiveresponse in rhabdomyolysis in the rat // J. Clin. Invest. – 1992. – 90, № 1. – P. 267-270.
  63. Nath K.A., Grande J.P., Croatt A.J. et al. Intracellular targets in heme protein-induced renal injury // Kidney Int. – 1998. – 53, № 1. –P. 100–111.
  64. Nath K.A., Haggard J.J., Croatt A.J. et al. The indispensability of heme oxygenase-1 (HO-1) in protecting against acute protein-induced toxity in vivo // Amer. Pathol. – 2000. – 156, № 5 –P. 1527–1535.
  65. Ndisang J.F., Wang R., Vannacci A. et al. Haeme oxygenase-1 and cardiac anaphylaxis // Brit. J.Pharmacol. – 2001. – 134, № 8. – P. 1689–1696.
  66. Neuzil J., Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for alphatocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation // J. Biol. Chem.– 1994. – 269, № 24. – P. 16712–16719.
  67. Otterbein L.E., Bach F.H., Alam J. et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway //Natur. Med. – 2000. – 6, № 4. – P. 422–428.
  68. Otterbein L.E., Choi A.M.K. Heme oxygenase: colors of defense against cellular stress // Amer.J. Physiol. – 2000. - 279, Issue 6. –P. L1029–L1037.
  69. 69. Otterbein L.E., Kolls J.K., Mantell L.L. et al. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxiainduced lung injury // J. Clin. Invest. – 1999. –103, № 7. – P. 1047–1054.
  70. 70. Otterbein L., Sylvester S.L., Choi A.M.K. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1 //Amer. J.Respirat. Cell. Mol. Biol. – 1995. – 13,№ 5. – P. 595–601.
  71. Panchenko M.V., Farber H.W., Korn J.H. Induction of heme oxygenase-1 by hypoxia and free radicals in human dermal fibroblasts // Amer. J.Physiol. – 2000. – 278, Issue 1. – P. C92–C101.
  72. Pataki T., Bak I., Csonka C. et al. Regulation of ventricular fibrillation by heme oxygenase in ischemic/reperfused hearts // Antioxid. Redox. Signal. – 2001. – 3, № 1. – P. 125–34.
  73. Petrache I., Otterbein LE., Alam J. et al. Heme oxygenase-1 inhibits TNF-a-induced apoptosis in cultured fibroblast // Amer. J. Physiol. Lung Cell Mol. Physiol. – 2000. – 278, Issue 2. – P. 312L-319.
  74. Polte T., Abate A., Dennery P.A. et al. Heme oxygenase-1 is a cGMP-inducible endothelial protein and mediates the cytoprotective action of nitric oxide // Arterioscler. Thromb. Vascular. Biol. –2000. – 20, № 5. – P. 1209–1215.
  75. Ponka P., Beaumont C., Richardson D.R. Function and regulation of transferrin and ferritin // Semin.Hematol. – 1998. – 35, № 1. – P. 35–54.
  76. Poss K.D., Tonegawa S. Reduced stress defense in heme oxygenase-1 deficient cells // Proc. Natl. Acad.Sci. USA. – 1997. – 94, № 9. – P. 10925–10930.
  77. Premkumar D.R., Smith M.A., Richey P.L. et al. Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer’s disease // J. Neurochem. – 1995. – 65, № 3 . –P. 1399–1402.
  78. Rattan S., Fan Y.P., Chakder S. Mechanism of inhibition of VIP-induced LES relaxation by heme oxygenase inhibitor zinc protoporphyrin IX //Amer. J. Physiol. – 1999. – 276, №1 ( Pt 1). –P. G138–45.
  79. 79. Rizzardini M., Terao M., Falciani F. et al. Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin-1 transcriptionally activates the haem oxygenase gene // Biochem. J. – 1993. –290, March 1(Pt 2). – P. 343–347.
  80. 80. Rotgers P.A., Vreman H.J., Dennery P.A. et al. Sources of carbon monoxide (CO) in biological system and applications of CO detection technologies // Semin. Perinatol. – 1994. – 18, № 1. –P. 2–10.
  81. Ryter S.W., Tyrrell R.M. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidantproperties // Free Rad. Biol. Med. – 2000. – 28,№ 2. – P. 289–309.
  82. Sammut I. A., Foresti R., Clark J.E. et al. Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1 // Brit. J. Pharmacol. – 1998. –125, № 7. – P. 1437–1444.
  83. Sato H., Siow R.C., Bartlett S. et al. Expression of stress proteins heme oxygenase-1 and -2 in acute pancreatitis and pancreatic islet betaTC3 and acinar AR42J cells // FEBS Lett. – 1997. – 405,№ 2. – P. 219–223.
  84. Siow R.C.M., Sata H., Mann G.E. Heme oxygenasecarbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxideα // Cardiovascular. Res. –1999. – 41, № 2. – P. 385–394.
  85. Smith M.A., Kutty R.K., Richey P.L.et al. Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer’s disease // Amer. J.Pathol. – 1994. – 145, № 1. – P. 42–47.
  86. Snyder S.H., Jaffrey S.R., Zakhary R. Nitric oxide and carbon monoxide: parallel roles as neural messengers // Brain. Res. Rev. – 1998. – № 2-3. –P. 167-175.
  87. Soares M.P., Lin Y., Anrather J. et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival // Natur. Med. – 1998. - 4, № 9. – P. 1073–1077.
  88. Stocker R., Yamamoto Y., McDonagh A.F. et al. Bilirubin is an antioxidant of possible physiological importance // Science. – 1987. – 235, Feb. 27 (4792). – P. 1043–1046.
  89. 89. Stupfel M., Bouley G. Physiological and biochemical effects on rats and mice exposed to small concentrations of carbon monoxide for long periods // Ann. NY Acad. Sci. – 1970. – 174, № 1. –P. 342–368.
  90. 90. Suttner D.M., Dennery P.A. Reversal of HO-1related cytoprotection with increased expression is due to reactive iron // FASEB J. – 1999. – 13,№ 13. – P. 1800–1809.
  91. 91. Suttner D.M., Sridhar K., Lee C.S. et al. P.A. Protective effects of transient HO-1 overexpression on susceptibility to oxygen toxicity in lung cells // Amer. J. Physiol. Lung Cell. Mol. Physiol. –1999. – 276, № 3 (Pt 1). – P. L443–L451.
  92. 92. Thorup C., Jones S.L, Gross S.S. et al. Carbon monoxide induces vasodilation and nitric oxide release but suppresses endothelial NOS // Amer.J. Physiol. – 1999. – 277, Issue 6. – P. F882–F889.
  93. 93. Vachharajani T.J., Work J., Sekutz A.C. et al. Heme oxygenase modulates selectin expression in different regional vascular beds // Amer. J. Physiol. Heart Circulat. Physiol. – 2000. – 278, № 5. –P. H1613–H1617.
  94. 94. Verma A., Hirsch D.J., Glatt C.E. et al. Carbon monoxide: a putative neural messenger // Science. – 1993. – 259, Jan 15 (5093). – P. 381–384.
  95. 95. Vile G.F., Tyrrell R.M. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin // J. Biol. Chem. – 1993. – 268,№ 2. – P. 14678–14681.
  96. 96. Vreman H.J., Wong R.J., Sanesi C.A. et al. Simultaneous production of carbon monoxide and thiobarbituric acid reactive substances in rat tissue preparations by an iron-ascorbate system // Can. J. Physiol.and Pharmacol. – 1998. – 76, №12. – P. 1057–1065.
  97. 97. Wang L.J., Lee T.S., Lee F.Y. et al. Expression of heme oxygenase-1 in atherosclerotic lesions //Amer. J. Pathol. – 1998. – 152, № 3. – P. 711–720.
  98. 98. Wang R., Wang Z., Wu L. et al. Reduced Vasorelaxant Effect of Carbon Monoxide in Diabetes and the Underlying Mechanisms // Diabetes. –2001. – 50, № 1. – P. 166–174.
  99. 99. Wang R. Resurgence of carbon monoxide: an endogenous gaseous vasorelaxig factor // Can.J. Pharmacol. – 1998. – 76, p.1. – P. 1–15.
  100. 100. Yamada N., Yamaya M., Okinaga S. et al. Protective Effects of Heme Oxygenase-1 against Oxidant-Induced Injury in the Cultured Human Tracheal Epithelium // Amer. J. Respirat. Cell. MolBoil., – 1999. – 21, № 3. – p. 428 –435.
  101. 101. Yamada N., Yamaya M., Okinaga S. et al. Microsatellite polymorphism in the heme oxygenase-1 ene promoter is associated with susceptibility to emphysema // Amer. J. Hum. Genet. – 2000. –66, № 1. – P. 187–195.
  102. 102. Yachie A., Niida Y., Wada T. et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency // J. Clin.Invest. – 1999. – 103, № 1. – P. 129–135.
  103. 103. Yet S.F., Pellacani A., Patterson C. et al. Induction of heme oxygenase-1 expression in vascular smooth uscle cells: a link to endotoxic shock // J. Biol. Chem. - 1997. – 272, № 7. – P. 4295–4301.
  104. 104. Yet S.F., Tian R., Layne M.D. et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in trans-genic mice // Circulat. Res. – 2001. – 89, № 7. – P. 168–173.

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