Heme oxygenase-1: Redox regulation of a stress protein in lung and cell culture models

Antioxidants and Redox Signaling

Volumn 7, Issue 1-2, 2005, Pages 80-91

  Ryter, Stefan W ^a,b   Choi, Augustine M K ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 33; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR BACH 1; TRANSCRIPTION FACTOR NF E2; UNCLASSIFIED DRUG;

CELL CULTURE; CHELATION; ENHANCER REGION; GENE CONTROL; GENE EXPRESSION; HUMAN; LUNG; MODEL; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; OXYGEN TENSION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY; TRANSCRIPTION INITIATION;

ANIMALS; ANTIOXIDANTS; BACTERIAL PHYSIOLOGY; BACTERIAL PROTEINS; CELLS, CULTURED; DISULFIDES; ENHANCER ELEMENTS (GENETICS); FUNGAL PROTEINS; FUNGI; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTATHIONE; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; LUNG; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; OXIDANTS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC;

EID: 13244256816     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2005.7.80     Document Type: Review

References (100)

1. Alam J. Multiple elements within the 5′ distal enhancer of the mouse heme oxygenase-1 gene mediate induction by heavy metals. J Biol Chem 269: 25049-25056, 1994.
2. Alam J, Shibahara S, and Smith A. Transcriptional activation of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. J Biol Chem 264: 6371-6375, 1989.
3. Alam J, Camhi S, and Choi AM. Identification of a second region upstream of the mouse heme oxygenase-1 gene that functions as a basal level and inducer-dependent transcription enhancer. J Biol Chem 270: 11977-11984, 1995.
4. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, and Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274: 26071-26078, 1999.
5. Alam J, Wicks C, Stewart D, Gong P, Touchard C, Otterbein S, Choi AM, Burow ME, and Tou J. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J Biol Chem 275: 27694-27702, 2000.
6. Amabile-Cuevas CF and Demple B. Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon. Nucleic Acids Res 19: 4479-4484, 1991.
7. Applegate LA, Luscher P, and Tyrrell RM. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 51: 974-978, 1991.
8. Aruoma OI and Halliwell B (Eds). Molecular Biology of Free Radicals in Human Diseases. Saint Lucia, London: Oica International, 1998.
9. Balla G, Vercellotti GM, Eaton JW, and Jacob HS. Iron loading of endothelial cells augments oxidant damage. J Lab Clin Med 116: 546-554, 1990.
10. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, and Vercellotti GM. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA 90: 9285-9289, 1993.
11. Balogun E, Hoque M, Gong P, Killeen E, Green CJ, Foresti R, Alam J, and Motterlini R. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J 371: 887-895, 2003.
12. Basu-Modak S and Tyrrell RM. Singlet oxygen: a primary effector in the ultraviolet A/near-visible light induction of the human heme oxygenase gene. Cancer Res 53: 4505-4510, 1993.
13. Basu-Modak S, Luscher P, and Tyrrell RM. Lipid metabolite involvement in the activation of the human heme oxygenase-1 gene. Free Radic Biol Med 20: 887-897, 1996.
14. Camhi SL, Alam J, Wiegand GW, Chin BY, and Choi AM. Transcriptional activation of the HO-1 gene by lipopolysaccharide is mediated by 5′ distal enhancers: role of reactive oxygen intermediates and AP-1. Am J Respir Cell Mol Biol 18: 226-234, 1998.
15. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, and Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 95: 11715-11720, 1998.
16. Chen JX, Zeng H, Chen X, Su CY, and Lai CC. Induction of heme oxygenase-1 by Ginkgo biloba extract but not its terpenoids partially mediated its protective effect against lysophosphatidylcholine-induced damage. Pharmacol Res 43: 63-69, 2001.
17. Chen K and Maines MD. Nitric oxide induces heme oxygenase-1 via mitogen-activated protein kinases ERK and p38. Cell Mol Biol (Noisy-le-grand) 46: 609-617, 2000.
18. Christman M, Morgan RW, Jacobson FS, and Ames BN. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41: 753-762, 1985.
19. 2 sensing through the oxidation of the Yap1 transcription factor. EMBO J 19: 5157-5166, 2000.
20. 2 receptor and redox transducer in gene activation. Cell 111: 478-481, 2002.
21. Durante W, Peyton KJ, and Schafer AI. Platelet-derived growth factor stimulates heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 19: 2666-2672, 1999.
22. Elbirt KK, Whitmarsh AJ, Davis RJ, and Bonkovsky HL. Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogen-activated protein kinases. J Biol Chem 273: 8922-8931, 1998.
23. Fogg S, Agarwal A, Nick HS, and Visner GA. Iron regulates hyperoxia-dependent human heme oxygenase 1 gene expression in pulmonary endothelial cells. Am J Respir Cell Mol Biol 20: 797-804, 1999.
24. Foresti R, Clark JE, Green CJ, and Motterlini R. Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of superoxide and peroxynitrite anions. J Biol Chem 272: 18411-18417, 1997.
25. Foresti R, Sarathchandra P, Clark JE, Green CJ, and Motterlini R. Peroxynitrite induces haem oxygenase-1 in vascular endothelial cells: a link to apoptosis. Biochem J 339: 729-736, 1999.
26. Freeman BA and Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 256: 10986-10992, 1981.
27. Fujita T, Toda K, Karimova A, Van SF, Naka Y, Yet SF, and Pinsky DJ. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat Med 7: 598-604, 2001.
28. Gohil K, Moy RK, Farzin S, Maguire JJ, and Packer L. mRNA expression profile of a human cancer cell line in response to Ginkgo biloba extract: induction of antioxidant response and the Golgi system. Free Radic Res 33: 831-849, 2000.
29. Gomer CJ, Luna M, Ferrario A, and Rucker N. Increased transcription and translation of heme oxygenase in Chinese hamster fibroblasts following photodynamic stress or Photofrin 11 incubation. Photochem Photobiol 53: 275-279, 1991.
30. Gong Q and Hart BA. Effect of thiols on cadmium-induced expression of metallothionein and other oxidant stress genes in rat lung epithelial cells. Toxicology 119: 179-191, 1997.
31. Greenberg JT, Monach P, Chou JH, Josephy PD, and Demple B. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci USA 87: 6181-6185, 1990.
32. Guy GR, Cairns J, Ng SB, and Tan YH. Inactivation of a redox-sensitive protein phosphatase during the early events of tumor necrosis factor/interleukin-1 signal transduction. J Biol Chem 268: 2141-2148, 1993.
33. 2. Role in cell survival following oxidant injury. J Biol Chem 271: 4138-4142, 1996.
34. Halliwell B and Gutteridge JMC (Eds). Free Radicals in Biology and Medicine. New York: Oxford University Press, 1999.
35. Hartsfield CL, Alam J, Cook JL, and Choi AM. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol 273: L980-L988, 1997.
36. Hartsfield CL, Alam J, and Choi AM. Transcriptional regulation of the heme oxygenase 1 gene by pyrrolidine dithiocarbamate. FASEB J 12: 1675-1682, 1998.
37. Hartsfield CL, Alam J, and Choi AM. Differential signaling pathways of HO-1 gene expression in pulmonary and systemic vascular cells. Am J Physiol 211: L1133-L1141, 1999.
38. He CH, Gong P, Hu B, Stewart D, Choi ME, Choi AM, and Alam J. Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J Biol Chem 276: 20858-20865, 2001.
39. Inamdar NM, Ahn YI, and Alam J. The heme-responsive element of the mouse heme oxygenase-1 gene is an extended AP-1 binding site that resembles the recognition sequences for MAF and NF-E2 transcription factors. Biochem Biophys Res Commun 221: 570-576, 1996.
40. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, and Nabeshima Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236: 313-322, 1997.
41. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, and Yamamoto M. Keapl represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13: 76-86, 1999.
42. 2 sensing. Science 292: 464-468, 2001.
43. Jakob U, Muse W, Eser M, and Bardwell JCA. Chaperone activity with a redox switch. Cell 96: 341-352, 1999.
44. Jakob U, Eser M, and Bardwell JCA. Redox switch of Hsp33 has a novel zinc-binding motif. J Biol Chem 275: 38302-38310, 2000.
45. Kacimi R, Chentoufi J, Honbo N, Long CS, and Karliner JS. Hypoxia differentially regulates stress proteins in cultured cardiomyocytes: role of the p38 stress-activated kinase signaling cascade, and relation to cytoprotection. Cardiovasc Res 46: 139-150, 2000.
46. Keyse SM and Tyrrell RM. 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 86: 99-103, 1989.
47. Keyse SM and Tyrrell RM. Induction of the heme oxygenase gene in human skin fibroblasts by hydrogen peroxide and UVA (365nm) radiation: evidence for the involvement of hydroxyl radical. Carcinogenesis 11: 787-791, 1990.
48. Keyse SM, Applegate LA, Tromvoukis Y, and Tyrrell RM. Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured skin fibroblasts. Mol Cell Biol 10: 4967-4969, 1990.
49. Kietzmann T, Samoylenko A, and Immenschuh S. Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes. J Biol Chem 278: 17927-17936, 2003.
50. Kim SO, Merchant K, Nudelman R, Beyer WF Jr, Keng T, DeAngelo J, Hausladen A, and Stamler JS. Oxy R: a molecular code for redox-related signaling. Cell 109: 383-396, 2002.
51. Kitamuro T, Takahashi K, Ogawa K, Udono-Fujimori R, Takeda K, Furuyama K, Nakayama M, Sun J, Fujita H, Hida W, Hattori T, Shirato K, Igarashi K, and Shibahara S. Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J Biol Chem 278: 9125-9133, 2003.
52. Kuge S, Jones N, and Nomoto A. Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J 16: 1710-1720, 1997.
53. Kutty RK, Nagineni CN, Kutty G, Hooks JJ, Chader GJ, and Wiggert B. Increased expression of heme oxygenase-1 in human retinal pigment epithelial cells by transforming growth factor-beta. J Cell Physiol 159: 371-378, 1994.
54. Kyriakis JM and Avruch J. Sounding the alarm: protein kinase cascades activated by stress and inflammation. J Biol Chem 271: 24313-24316, 1996.
55. Lautier D, Luscher P, and Tyrrell RM. Endogenous glutathione levels modulate both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene. Carcinogenesis 13: 227-232, 1992.
56. Lee PJ, Alam J, Sylvester SL, Inamdar N, Otterbein L, and Choi AM. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am J Respir Cell Mol Biol 14: 556-568, 1996.
57. Lee PJ, Alam J, Wiegand GW, and Choi AM. Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci USA 93: 10393-10398, 1996.
58. Lee PJ, Jiang BH, Chin BY, Iyer NV, Alam J, Semenza GL, and Choi AM. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 272: 5375-5381, 1997.
59. Lee PJ, Camhi SL, Chin BY, Alam J, and Choi AM. AP-1 and STAT mediate hyperoxia-induced gene transcription of heme oxygenase-1. Am J Physiol Lung Cell Mol Physiol 279: L175-L182, 2002.
60. Li N, Venkatesan MI, Miguel A, Kaplan R, Gujuluva C, Alam J, and Nel A. Induction of heme oxygenase-1 expression in macrophages by diesel exhaust particle chemicals and quinones via the antioxidant-responsive element. J Immunol 165: 3393-3401, 2000.
61. Maines MD. Heme oxygenase: Clinical Applications and Functions. Boca Raton, FL: CRC Press, 1992.
62. Meier B, Radeke HH, Selle S, Younes M, Sies H, Resch K, and Habermehl GG. Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumour necrosis factor-alpha. Biochem J 263: 539-545, 1989.
63. Minamino T, Christou H, Hsieh CM, Liu Y, Dhawan V, Abraham NG, Perrella MA, Mitsialis SA, and Kourembanas S. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc Natl Acad Sci USA 98: 8798-8803, 2001.
64. Motterlini R, Foresti R, Bassi R, Calabrese V, Clark JE, and Green CJ. Endothelial heme oxygenase-1 induction by hypoxia. Modulation by inducible nitric-oxide synthase and S-nitrosothiols. J Biol Chem 275: 13613-13620, 2000.
65. Motterlini R, Green CJ, and Foresti R. Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid Redox Signal 4: 615-624, 2002.
66. Murphy BJ, Laderoute KR, Short SM, and Sutherland RM. The identification of heme oxygenase as a major hypoxic stress protein in Chinese hamster ovary cells. Br J Cancer 64: 69-73, 1991.
67. Nakayama M, Takahashi K, Kitamuro T, Yasumoto K, Katayose D, Shirato K, Fujii-Kuriyama Y, and Shibahara S. Repression of heme oxygenase-1 by hypoxia in vascular endothelial cells. Biochem Biophys Res Commun 271: 665-671, 2000.
68. Naughton P, Foresti R, Bains SK, Hoque M, Green CJ, and Motterlini R. Induction of heme oxygenase 1 by nitrosative stress. A role for nitroxyl anion. J Biol Chem 277: 40666-40674, 2002.
69. Naughton P, Hoque M, Green CJ, Foresti R, and Motterlini R. Interaction of heme with nitroxyl or nitric oxide amplifies heme oxygenase-1 induction: involvement of the transcription factor Nrf2. Cell Mol Biol (Noisy-le-grand) 48: 885-894, 2002.
70. Ning W, Song R, Li C, Park E, Mohsenin A, Choi AM, and Choi ME. TGF-beta1 stimulates HO-1 via the p38 mitogen-activated protein kinase in A549 pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 283: L1094-L1102, 2002.
71. Nunoshiba T, Hidalgo E, Amabile Cuevas CF, and Demple B. Two-stage control of an oxidative stress regulon: the Escherichia coli SoxR protein triggers redox-inducible expression of the soxS regulatory gene. J Bacteriol 174: 6054-6060, 1992.
72. Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C, Sassa S, Hayashi N, Yamamoto M, Shibahara S, Fujita H, and Igarashi K. Heme mediates derepression of Maf recognition element through direct binding to transcription represser Bach1. EMBO J 20: 2835-2843, 2001.
73. Otterbein L, Sylvester SL, and Choi AM. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am J Respir Cell Mol Biol 13: 595-601, 1995.
74. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, and Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin invest 103: 1047-1054, 1999.
75. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, and Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6: 422-428, 2000.
76. Paget MS and Buttner MJ. Thiol-based regulatory switches. Annu Rev Genet 37: 91-121, 2003.
77. Petrache I, Choi ME, Otterbein LE, Chin BY, Mantell LL, Horowitz S, and Choi AM. Mitogen-activated protein kinase pathway mediates hyperoxia-induced apoptosis in cultured macrophage cells. Am J Physiol 277: L589-L595, 1999.
78. Richardson DR and Ponka P. The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta 1331: 1-40, 1997.
79. Rizzardini M, Carelli M, Cabello Porras MR, and Cantoni L. Mechanisms of endotoxin-induced haem oxygenase mRNA accumulation in mouse liver: synergism by glutathione depletion and protection by N-acetylcysteine. Biochem J 304: 477-483, 1994.
80. Ryter SW and Choi AMK. Heme oxygenase-1: molecular mechanisms of gene expression in oxygen-related stress. Antioxid Redox Signal 4: 625-632, 2002.
81. Ryter SW and Tyrrell RM. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and anti-oxidant properties. Free Radic Biol Med 28: 289-309, 2000.
82. Ryter SW, Si ML, Lai C-C, and Su CY. Regulation of endothelial heme oxygenase activity during hypoxia is dependent on intracellular chelatable iron. Am J Physiol Heart Circ Physiol 279: H2889-H2897, 2000.
83. Ryter SW, Otterbein LE, Morse D, and Choi AMK. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem 234/235: 249-263, 2002.
84. Ryter SW, Xi S, Hartsfield C, and Choi AM. Mitogen activated protein kinase (MAPK) pathway regulates heme oxygenase-1 gene expression by hypoxia in vascular cells. Antioxid Redox Signal 4: 587-592, 2002.
85. Saunders EL, Maines MD, Meredith MJ, and Freeman ML. Enhancement of heme oxygenase-1 synthesis by glutathione depletion in Chinese hamster ovary cells. Arch Biochem Biophys 288: 368-373, 1991.
86. Scapagnini G, Foresti R, Calabrese V, Giuffrida Stella AM, Green CJ, and Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol Pharmacol 61: 554-561, 2002.
87. Schipper HM. Glial HO-1 expression, iron deposition and oxidative stress in neurodegenerative diseases. Neurotox Res 1: 57-70, 1999.
88. 2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15: 551-578, 1999.
89. Soriani M, Rice-Evans C, and Tyrrell RM. Modulation of the UVA activation of haem oxygenase, collagenase and cyclooxygenase gene expression by epigallocatechin in human skin cells. FEBS Lett 439: 253-257, 1998.
90. Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, Taketo MM, Yamamoto M, and Igarashi K. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 21: 5216-5224, 2002.
91. Tenhunen R, Marver H, and Schmid R. Microsomal heme oxygenase, characterization of the enzyme. J Biol Chem 244: 6388-6394, 1969.
92. 2+, and phospholipase A2 in endothelial cells. Am J Physiol 276: H1493-H1501, 1999.
93. Trekli MC, Riss G, Goralczyk R, and Tyrrell RM. Beta-carotene suppresses UVA-induced HO-1 gene expression in cultured FEK4. Free Radic Biol Med 34: 456-464, 2003.
94. Tyrrell RM. Approaches to define pathways of redox regulation of a eukaryotic gene: The heme oxygenase 1 example. Methods 11: 313-318, 1997.
95. Venugopal R and Jaiswal AK. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17: 3145-3156, 1998.
96. Yu R, Chen C, Mo YY, Hebbar V, Owuor ED, Tan TH, and Kong AN. Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism. J Biol Chem 275: 39907-39913, 2000.
97. Zhang X, Bedard EL, Potter R, Zhong R, Alam J, Choi AM, and Lee PJ. Mitogen-activated protein kinases regulate HO-1 gene transcription after ischemia-reperfusion lung injury. Am J Physiol Lung Cell Mol Physiol 283: L815-L829, 2002.
98. Zheng M, Åslund F, and Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1722, 1998.
99. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, and Storz G. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562-4570, 2001.
100. Zhuang H, Pin S, Christen Y, and Dore S. Induction of heme oxygenase 1 by Ginkgo biloba in neuronal cultures and potential implications in ischemia. Cell Mol Biol (Noisy-le-grand) 48: 647-653, 2002.