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Mahin Maines

TitleProfessor
InstitutionSchool of Medicine and Dentistry
DepartmentBiochemistry and Biophysics
AddressUniversity of Rochester Medical Center
School of Medicine and Dentistry
601 Elmwood Ave, Box 712
Rochester NY 14642
 
 Overview
The protein kinases mediate eukaryotic cells' response to internal and external stimuli such as a growth and differentiation factors, hormones, drugs and chemicals. The cell signaling pathways that transduce stimuli depend on cascades of phosphorylation /dephosphorylation events and kinase activities. The heme metabolic pathway, which converts, sequentially, heme to biliverdin plus CO, and bilirubin, reflects activities of heme oxygenase (HO) isozymes 1,2and 3, which constitute the HSP32 (heat shock/stress protein) family of proteins, and biliverdin reductase (BVR). Our recent studies have identified the heme metabolic pathway as a component of the cell signal transduction pathways.We have described CO as a signaling molecule; HO proteins as an intracellular sink for NO and potentially an intracellular oxygen sensor, bilirubin and biliverdin as modulators of protein phosphorylation. We have recently described biliverdin reductase as a new member of the dual specificity kinase (serine/threonine/tyrosine kinase) family, a leucine zipper-type transcription factor for cAMP and AP-1 regulated genes and an inhibitor of apoptosis. We are further investigating how the HO/BVR pathway modulates cell signaling and cell cycle processes.

 
 Selected Publications
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  1. Kapitulnik J, Maines MD. The role of bile pigments in health and disease: effects on cell signaling, cytotoxicity, and cytoprotection. Front Pharmacol. 2012; 3:136.
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  2. Miralem T, Lerner-Marmarosh N, Gibbs PE, Tudor C, Hagen FK, Maines MD. The human biliverdin reductase-based peptide fragments and biliverdin regulate protein kinase Cd activity: the peptides are inhibitors or substrate for the protein kinase C. J Biol Chem. 2012 Jul 13; 287(29):24698-712.
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  3. Gibbs PE, Tudor C, Maines MD. Biliverdin reductase: more than a namesake - the reductase, its Peptide fragments, and biliverdin regulate activity of the three classes of protein kinase C. Front Pharmacol. 2012; 3:31.
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  4. Gibbs PE, Miralem T, Lerner-Marmarosh N, Tudor C, Maines MD. Formation of ternary complex of human biliverdin reductase-protein kinase Cd-ERK2 protein is essential for ERK2-mediated activation of Elk1 protein, nuclear factor-?B, and inducible nitric-oxidase synthase (iNOS). J Biol Chem. 2012 Jan 6; 287(2):1066-79.
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  5. Maines MD. Potential application of biliverdin reductase and its fragments to modulate insulin/IGF-1/MAPK/PI3-K signaling pathways in therapeutic settings. Curr Drug Targets. 2010 Dec; 11(12):1586-94.
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  6. Ding B, Gibbs PE, Brookes PS, Maines MD. The coordinated increased expression of biliverdin reductase and heme oxygenase-2 promotes cardiomyocyte survival: a reductase-based peptide counters ß-adrenergic receptor ligand-mediated cardiac dysfunction. FASEB J. 2011 Jan; 25(1):301-13.
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  7. Gibbs PE, Miralem T, Maines MD. Characterization of the human biliverdin reductase gene structure and regulatory elements: promoter activity is enhanced by hypoxia and suppressed by TNF-alpha-activated NF-kappaB. FASEB J. 2010 Sep; 24(9):3239-54.
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  8. Miralem T, Gibbs PE, Revert F, Saus J, Maines MD. Human biliverdin reductase suppresses Goodpasture antigen-binding protein (GPBP) kinase activity: the reductase regulates tumor necrosis factor-alpha-NF-kappaB-dependent GPBP expression. J Biol Chem. 2010 Apr 23; 285(17):12551-8.
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  9. Kapitulnik J, Maines MD. Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin. Trends Pharmacol Sci. 2009 Mar; 30(3):129-37.
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  10. Tudor C, Lerner-Marmarosh N, Engelborghs Y, Gibbs PE, Maines MD. Biliverdin reductase is a transporter of haem into the nucleus and is essential for regulation of HO-1 gene expression by haematin. Biochem J. 2008 Aug 1; 413(3):405-16.
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  11. Lerner-Marmarosh N, Miralem T, Gibbs PE, Maines MD. Human biliverdin reductase is an ERK activator; hBVR is an ERK nuclear transporter and is required for MAPK signaling. Proc Natl Acad Sci U S A. 2008 May 13; 105(19):6870-5.
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  12. Gibbs PE, Maines MD. Biliverdin inhibits activation of NF-kappaB: reversal of inhibition by human biliverdin reductase. Int J Cancer. 2007 Dec 1; 121(11):2567-74.
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  13. Maines MD. Biliverdin reductase: PKC interaction at the cross-talk of MAPK and PI3K signaling pathways. Antioxid Redox Signal. 2007 Dec; 9(12):2187-95.
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  14. Lerner-Marmarosh N, Miralem T, Gibbs PE, Maines MD. Regulation of TNF-alpha-activated PKC-zeta signaling by the human biliverdin reductase: identification of activating and inhibitory domains of the reductase. FASEB J. 2007 Dec; 21(14):3949-62.
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  15. Maines MD, Miralem T, Lerner-Marmarosh N, Shen J, Gibbs PE. Human biliverdin reductase, a previously unknown activator of protein kinase C betaII. J Biol Chem. 2007 Mar 16; 282(11):8110-22.
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  16. Calabrese V, Maines MD. Antiaging medicine: antioxidants and aging. Antioxid Redox Signal. 2006 Mar-Apr; 8(3-4):362-4.
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  17. Calabrese V, Butterfield DA, Scapagnini G, Stella AM, Maines MD. Redox regulation of heat shock protein expression by signaling involving nitric oxide and carbon monoxide: relevance to brain aging, neurodegenerative disorders, and longevity. Antioxid Redox Signal. 2006 Mar-Apr; 8(3-4):444-77.
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  18. Ewing JF, Maines MD. Regulation and expression of heme oxygenase enzymes in aged-rat brain: age related depression in HO-1 and HO-2 expression and altered stress-response. J Neural Transm. 2006 Apr; 113(4):439-54.
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  19. Maines MD. New insights into biliverdin reductase functions: linking heme metabolism to cell signaling. Physiology (Bethesda). 2005 Dec; 20:382-9.
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  20. Maines MD. The heme oxygenase system: update 2005. Antioxid Redox Signal. 2005 Nov-Dec; 7(11-12):1761-6.
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  21. Maines MD, Gibbs PE. 30 some years of heme oxygenase: from a "molecular wrecking ball" to a "mesmerizing" trigger of cellular events. Biochem Biophys Res Commun. 2005 Dec 9; 338(1):568-77.
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  22. Lerner-Marmarosh N, Shen J, Torno MD, Kravets A, Hu Z, Maines MD. Human biliverdin reductase: a member of the insulin receptor substrate family with serine/threonine/tyrosine kinase activity. Proc Natl Acad Sci U S A. 2005 May 17; 102(20):7109-14.
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  23. Miralem T, Hu Z, Torno MD, Lelli KM, Maines MD. Small interference RNA-mediated gene silencing of human biliverdin reductase, but not that of heme oxygenase-1, attenuates arsenite-mediated induction of the oxygenase and increases apoptosis in 293A kidney cells. J Biol Chem. 2005 Apr 29; 280(17):17084-92.
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  24. Maines MD. The heme oxygenase system: past, present, and future. Antioxid Redox Signal. 2004 Oct; 6(5):797-801.
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  25. Kravets A, Hu Z, Miralem T, Torno MD, Maines MD. Biliverdin reductase, a novel regulator for induction of activating transcription factor-2 and heme oxygenase-1. J Biol Chem. 2004 May 7; 279(19):19916-23.
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  26. Mayer RD, Wang X, Maines MD. Nitric oxide inhibitor N omega -nitro-l-arginine methyl ester potentiates induction of heme oxygenase-1 in kidney ischemia/reperfusion model: a novel mechanism for regulation of the oxygenase. J Pharmacol Exp Ther. 2003 Jul; 306(1):43-50.
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  27. Wang X, Hauptmann N, Taylor E, Foreman M, Khawli LA, Maines MD. Neotrofin increases heme oxygenase-1 selectively in neurons. Brain Res. 2003 Feb 7; 962(1-2):1-14.
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  28. Maines MD. Bile pigments: newcomers to the cell signaling arena. Toxicol Sci. 2003 Jan; 71(1):9-10.
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  29. Whitby FG, Phillips JD, Hill CP, McCoubrey W, Maines MD. Crystal structure of a biliverdin IXalpha reductase enzyme-cofactor complex. J Mol Biol. 2002 Jun 21; 319(5):1199-210.
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  30. Maines MD. Heme oxygenase 1 transgenic mice as a model to study neuroprotection. Methods Enzymol. 2002; 353:374-88.
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  31. Ahmad Z, Salim M, Maines MD. Human biliverdin reductase is a leucine zipper-like DNA-binding protein and functions in transcriptional activation of heme oxygenase-1 by oxidative stress. J Biol Chem. 2002 Mar 15; 277(11):9226-32.
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  32. Huang TJ, McCoubrey WK, Maines MD. Heme oxygenase-2 interaction with metalloporphyrins: function of heme regulatory motifs. Antioxid Redox Signal. 2001 Aug; 3(4):685-96.
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  33. Maines MD. Overview of heme degradation pathway. Curr Protoc Toxicol. 2001 May; Chapter 9:Unit 9.1.
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  34. Maines MD, Ewing JF, Huang TJ, Panahian N. Nuclear localization of biliverdin reductase in the rat kidney: response to nephrotoxins that induce heme oxygenase-1. J Pharmacol Exp Ther. 2001 Mar; 296(3):1091-7.
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  35. Salim M, Brown-Kipphut BA, Maines MD. Human biliverdin reductase is autophosphorylated, and phosphorylation is required for bilirubin formation. J Biol Chem. 2001 Apr 6; 276(14):10929-34.
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  36. Maines MD, Panahian N. The heme oxygenase system and cellular defense mechanisms. Do HO-1 and HO-2 have different functions? Adv Exp Med Biol. 2001; 502:249-72.
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  37. Panahian N, Maines MD. Site of injury-directed induction of heme oxygenase-1 and -2 in experimental spinal cord injury: differential functions in neuronal defense mechanisms? J Neurochem. 2001 Jan; 76(2):539-54.
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  38. Panahian N, Maines MD. Assessment of induction of biliverdin reductase in a mouse model of middle cerebral artery occlusion. Brain Res Brain Res Protoc. 2000 Nov; 6(1-2):53-70.
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  39. Chen K, Gunter K, Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem. 2000 Jul; 75(1):304-13.
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  40. Chen K, Maines MD. Nitric oxide induces heme oxygenase-1 via mitogen-activated protein kinases ERK and p38. Cell Mol Biol (Noisy-le-grand). 2000 May; 46(3):609-17.
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  41. Maines MD. The heme oxygenase system and its functions in the brain. Cell Mol Biol (Noisy-le-grand). 2000 May; 46(3):573-85.
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  42. Liu N, Wang X, McCoubrey WK, Maines MD. Developmentally regulated expression of two transcripts for heme oxygenase-2 with a first exon unique to rat testis: control by corticosterone of the oxygenase protein expression. Gene. 2000 Jan 4; 241(1):175-83.
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  43. Panahian N, Huang T, Maines MD. Enhanced neuronal expression of the oxidoreductase--biliverdin reductase--after permanent focal cerebral ischemia. Brain Res. 1999 Dec 11; 850(1-2):1-13.
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  44. Maines MD, Raju VS, Panahian N. Spin trap (N-t-butyl-alpha-phenylnitrone)-mediated suprainduction of heme oxygenase-1 in kidney ischemia/reperfusion model: role of the oxygenase in protection against oxidative injury. J Pharmacol Exp Ther. 1999 Nov; 291(2):911-9.
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  45. Maines MD, Mayer RD, Erturk E, Huang TJ, Disantagnese A. The oxidoreductase, biliverdin reductase, is induced in human renal carcinoma--pH and cofactor-specific increase in activity. J Urol. 1999 Oct; 162(4):1467-72.
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  46. Ding Y, McCoubrey WK, Maines MD. Interaction of heme oxygenase-2 with nitric oxide donors. Is the oxygenase an intracellular 'sink' for NO? Eur J Biochem. 1999 Sep; 264(3):854-61.
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  47. Panahian N, Yoshiura M, Maines MD. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem. 1999 Mar; 72(3):1187-203.
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  48. Morgan D, Holcomb L, Saad I, Gordon M. Impaired spatial navigation learning in transgenic mice over-expressing heme oxygenase-1. Brain Res. 1998 Oct 12; 808(1):110-2.
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  49. Woo J, Iyer S, Cornejo MC, Mori N, Gao L, Sipos I, Maines M, Buelow R. Stress protein-induced immunosuppression: inhibition of cellular immune effector functions following overexpression of haem oxygenase (HSP 32). Transpl Immunol. 1998 Jun; 6(2):84-93.
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  50. Maines MD, Polevoda B, Coban T, Johnson K, Stoliar S, Huang TJ, Panahian N, Cory-Slechta DA, McCoubrey WK. Neuronal overexpression of heme oxygenase-1 correlates with an attenuated exploratory behavior and causes an increase in neuronal NADPH diaphorase staining. J Neurochem. 1998 May; 70(5):2057-69.
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  51. Miller SM, Farrugia G, Schmalz PF, Ermilov LG, Maines MD, Szurszewski JH. Heme oxygenase 2 is present in interstitial cell networks of the mouse small intestine. Gastroenterology. 1998 Feb; 114(2):239-44.
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  52. Farrugia G, Miller SM, Rich A, Liu X, Maines MD, Rae JL, Szurszewski JH. Distribution of heme oxygenase and effects of exogenous carbon monoxide in canine jejunum. Am J Physiol. 1998 Feb; 274(2 Pt 1):G350-8.
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  53. Iyer S, Woo J, Cornejo MC, Gao L, McCoubrey W, Maines M, Buelow R. Characterization and biological significance of immunosuppressive peptide D2702.75-84(E --> V) binding protein. Isolation of heme oxygenase-1. J Biol Chem. 1998 Jan 30; 273(5):2692-7.
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  54. McCoubrey WK, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem. 1997 Jul 15; 247(2):725-32.
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  55. Sturgill MG, Grasing KW, Rosen RC, Thomas TJ, Kulkarni GD, Trout JR, Maines M, Seibold JR. Yohimbine elimination in normal volunteers is characterized by both one- and two-compartment behavior. J Cardiovasc Pharmacol. 1997 Jun; 29(6):697-703.
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  56. McCoubrey WK, Huang TJ, Maines MD. Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem. 1997 May 9; 272(19):12568-74.
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  57. Ewing JF, Maines MD. Histochemical localization of heme oxygenase-2 protein and mRNA expression in rat brain. Brain Res Brain Res Protoc. 1997 May; 1(2):165-74.
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  58. Lagarias DM, Crepeau MW, Maines MD, Lagarias JC. Regulation of photomorphogenesis by expression of mammalian biliverdin reductase in transgenic Arabidopsis plants. Plant Cell. 1997 May; 9(5):675-88.
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  59. Raju VS, McCoubrey WK, Maines MD. Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain: characterization of a functional glucocorticoid response element. Biochim Biophys Acta. 1997 Mar 20; 1351(1-2):89-104.
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  60. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997; 37:517-54.
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  61. Geddes JW, Pettigrew LC, Holtz ML, Craddock SD, Maines MD. Permanent focal and transient global cerebral ischemia increase glial and neuronal expression of heme oxygenase-1, but not heme oxygenase-2, protein in rat brain. Neurosci Lett. 1996 Jun 7; 210(3):205-8.
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  62. Raju VS, Maines MD. Renal ischemia/reperfusion up-regulates heme oxygenase-1 (HSP32) expression and increases cGMP in rat heart. J Pharmacol Exp Ther. 1996 Jun; 277(3):1814-22.
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  63. Maines MD, Eke BC, Zhao X. Corticosterone promotes increased heme oxygenase-2 protein and transcript expression in the newborn rat brain. Brain Res. 1996 May 25; 722(1-2):83-94.
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  64. Maines MD, Abrahamsson PA. Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic, and tumor tissue distribution. Urology. 1996 May; 47(5):727-33.
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  65. Maines MD, Ewing JF. Stress response of the rat testis: in situ hydridization and immunohistochemical analysis of heme oxygenase-1 (HSP32) induction by hyperthermia. Biol Reprod. 1996 May; 54(5):1070-9.
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  66. Maines MD, Polevoda BV, Huang TJ, McCoubrey WK. Human biliverdin IXalpha reductase is a zinc-metalloprotein. Characterization of purified and Escherichia coli expressed enzymes. Eur J Biochem. 1996 Jan 15; 235(1-2):372-81.
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  67. Maines M. Carbon monoxide and nitric oxide homology: differential modulation of heme oxygenases in brain and detection of protein and activity. Methods Enzymol. 1996; 268:473-88.
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  68. McCoubrey WK, Eke B, Maines MD. Multiple transcripts encoding heme oxygenase-2 in rat testis: developmental and cell-specific regulation of transcripts and protein. Biol Reprod. 1995 Dec; 53(6):1330-8.
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  69. McCoubrey WK, Cooklis MA, Maines MD. The structure, organization and differential expression of the rat gene encoding biliverdin reductase. Gene. 1995 Jul 28; 160(2):235-40.
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  70. Ewing JF, Maines MD. Distribution of constitutive (HO-2) and heat-inducible (HO-1) heme oxygenase isozymes in rat testes: HO-2 displays stage-specific expression in germ cells. Endocrinology. 1995 May; 136(5):2294-302.
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  71. Maines MD, Eke BC, Weber CM, Ewing JF. Corticosterone has a permissive effect on expression of heme oxygenase-1 in CA1-CA3 neurons of hippocampus in thermal-stressed rats. J Neurochem. 1995 Apr; 64(4):1769-79.
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  72. Ewing JF, Maines MD. Immunohistochemical localization of biliverdin reductase in rat brain: age related expression of protein and transcript. Brain Res. 1995 Feb 20; 672(1-2):29-41.
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  73. Vincent SR, Das S, Maines MD. Brain heme oxygenase isoenzymes and nitric oxide synthase are co-localized in select neurons. Neuroscience. 1994 Nov; 63(1):223-31.
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  74. Rublevskaya I, Maines MD. Interaction of Fe-protoporphyrin IX and heme analogues with purified recombinant heme oxygenase-2, the constitutive isozyme of the brain and testes. J Biol Chem. 1994 Oct 21; 269(42):26390-5.
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  75. Ewing JF, Raju VS, Maines MD. Induction of heart heme oxygenase-1 (HSP32) by hyperthermia: possible role in stress-mediated elevation of cyclic 3':5'-guanosine monophosphate. J Pharmacol Exp Ther. 1994 Oct; 271(1):408-14.
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  76. Weber CM, Eke BC, Maines MD. Corticosterone regulates heme oxygenase-2 and NO synthase transcription and protein expression in rat brain. J Neurochem. 1994 Sep; 63(3):953-62.
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  77. McCoubrey WK, Maines MD. Site-directed mutagenesis of cysteine residues in biliverdin reductase. Roles in substrate and cofactor binding. Eur J Biochem. 1994 Jun 1; 222(2):597-603.
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  78. Raju VS, Maines MD. Coordinated expression and mechanism of induction of HSP32 (heme oxygenase-1) mRNA by hyperthermia in rat organs. Biochim Biophys Acta. 1994 Apr 6; 1217(3):273-80.
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  79. McCoubrey WK, Maines MD. The structure, organization and differential expression of the gene encoding rat heme oxygenase-2. Gene. 1994 Feb 25; 139(2):155-61.
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  80. Terry MJ, Maines MD, Lagarias JC. Inactivation of phytochrome- and phycobiliprotein-chromophore precursors by rat liver biliverdin reductase. J Biol Chem. 1993 Dec 15; 268(35):26099-106.
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  81. Maines MD. Carbon Monoxide: An Emerging Regulator of cGMP in the Brain. Mol Cell Neurosci. 1993 Oct; 4(5):389-97.
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  82. Maines MD, Mark JA, Ewing JF. Heme Oxygenase, a Likely Regulator of cGMP Production in the Brain: Induction in Vivo of HO-1 Compensates for Depression in NO Synthase Activity. Mol Cell Neurosci. 1993 Oct; 4(5):396-405.
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  83. Ewing JF, Weber CM, Maines MD. Biliverdin reductase is heat resistant and coexpressed with constitutive and heat shock forms of heme oxygenase in brain. J Neurochem. 1993 Sep; 61(3):1015-23.
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  84. McCoubrey WK, Maines MD. Domains of rat heme oxygenase-2: the amino terminus and histidine 151 are required for heme oxidation. Arch Biochem Biophys. 1993 May; 302(2):402-8.
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  85. Ewing JF, Maines MD. Glutathione depletion induces heme oxygenase-1 (HSP32) mRNA and protein in rat brain. J Neurochem. 1993 Apr; 60(4):1512-9.
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  86. Maines MD, Mayer RD, Ewing JF, McCoubrey WK. 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 Ther. 1993 Jan; 264(1):457-62.
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  87. Maines MD, Trakshel GM. Purification and characterization of human biliverdin reductase. Arch Biochem Biophys. 1993 Jan; 300(1):320-6.
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  88. Ewing JF, Maines MD. In situ hybridization and immunohistochemical localization of heme oxygenase-2 mRNA and protein in normal rat brain: Differential distribution of isozyme 1 and 2. Mol Cell Neurosci. 1992 Dec; 3(6):559-70.
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  89. Mark JA, Maines MD. Tin-protoporphyrin-mediated disruption in vivo of heme oxygenase-2 protein integrity and activity in rat brain. Pediatr Res. 1992 Sep; 32(3):324-9.
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  90. Maines MD, Trakshel GM. Differential regulation of heme oxygenase isozymes by Sn- and Zn-protoporphyrins: possible relevance to suppression of hyperbilirubinemia. Biochim Biophys Acta. 1992 Jun 15; 1131(2):166-74.
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  91. McCoubrey WK, Ewing JF, Maines MD. Human heme oxygenase-2: characterization and expression of a full-length cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of polyadenylation signal. Arch Biochem Biophys. 1992 May 15; 295(1):13-20.
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  92. Ewing JF, Haber SN, Maines MD. Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: hyperthermia causes rapid induction of mRNA and protein. J Neurochem. 1992 Mar; 58(3):1140-9.
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  93. Fakhrai H, Maines MD. Expression and characterization of a cDNA for rat kidney biliverdin reductase. Evidence suggesting the liver and kidney enzymes are the same transcript product. J Biol Chem. 1992 Feb 25; 267(6):4023-9.
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  94. Trakshel GM, Sluss PM, Maines MD. Comparative effects of tin- and zinc-protoporphyrin on steroidogenesis: tin-protoporphyrin is a potent inhibitor of cytochrome P-450-dependent activities in the rat adrenals. Pediatr Res. 1992 Feb; 31(2):196-201.
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  95. Maines MD, Trakshel GM. Tin-protoporphyrin: a potent inhibitor of hemoprotein-dependent steroidogenesis in rat adrenals and testes. J Pharmacol Exp Ther. 1992 Feb; 260(2):909-16.
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  96. Rotenberg MO, Maines MD. Characterization of a cDNA-encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes: possible heme-binding site? Arch Biochem Biophys. 1991 Nov 1; 290(2):336-44.
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  97. Krueger BA, Trakshel GM, Sluss PM, Maines MD. Cyclosporin-mediated depression of luteinizing hormone receptors and heme biosynthesis in rat testes: a possible mechanism for decrease in serum testosterone. Endocrinology. 1991 Nov; 129(5):2647-54.
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  98. Saunders EL, Maines MD, Meredith MJ, Freeman ML. Enhancement of heme oxygenase-1 synthesis by glutathione depletion in Chinese hamster ovary cells. Arch Biochem Biophys. 1991 Aug 1; 288(2):368-73.
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  99. Ewing JF, Maines MD. Rapid induction of heme oxygenase 1 mRNA and protein by hyperthermia in rat brain: heme oxygenase 2 is not a heat shock protein. Proc Natl Acad Sci U S A. 1991 Jun 15; 88(12):5364-8.
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  100. Trakshel GM, Ewing JF, Maines MD. Heterogeneity of haem oxygenase 1 and 2 isoenzymes. Rat and primate transcripts for isoenzyme 2 differ in number and size. Biochem J. 1991 Apr 1; 275 ( Pt 1):159-64.
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  101. Sun Y, Maines MD. Heme oxygenase-2 mRNA: developmental expression in the rat liver and response to cobalt chloride. Arch Biochem Biophys. 1990 Nov 1; 282(2):340-5.
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  102. Maines MD. Multiple forms of biliverdin reductase: age-related change in pattern of expression in rat liver and brain. Mol Pharmacol. 1990 Oct; 38(4):481-5.
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  103. Iscan M, Reuhl K, Weiss B, Maines MD. Regional and subcellular distribution of cytochrome P-450-dependent drug metabolism in monkey brain: the olfactory bulb and the mitochondrial fraction have high levels of activity. Biochem Biophys Res Commun. 1990 Jun 29; 169(3):858-63.
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  104. Sun Y, Rotenberg MO, Maines MD. Developmental expression of heme oxygenase isozymes in rat brain. Two HO-2 mRNAs are detected. J Biol Chem. 1990 May 15; 265(14):8212-7.
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  105. Mayer RD, Maines MD. Promotion of trans-platinum in vivo effects on renal heme and hemoprotein metabolism by D,L-buthionine-S,R-sulfoximine. Possible role of glutathione. Biochem Pharmacol. 1990 May 15; 39(10):1565-71.
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  106. Rotenberg MO, Maines MD. Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J Biol Chem. 1990 May 5; 265(13):7501-6.
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  107. Maines MD, Sluss PM, Iscan M. cis-platinum-mediated decrease in serum testosterone is associated with depression of luteinizing hormone receptors and cytochrome P-450scc in rat testis. Endocrinology. 1990 May; 126(5):2398-406.
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  108. Iscan M, Maines MD. Differential regulation of heme and drug metabolism in rat testis and prostate: response to cis-platinum and human chorionic gonadotropin. J Pharmacol Exp Ther. 1990 Apr; 253(1):73-9.
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  109. Maines MD. Effect of cis-platinum on heme, drug, and steroid metabolism pathways: possible involvement in nephrotoxicity and infertility. Crit Rev Toxicol. 1990; 21(1):1-20.
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  110. Huang TJ, Maines MD. Bromobenzene-mediated alteration in activity and electrophoretic pattern of biliverdin reductase variants in rat kidney. Mol Pharmacol. 1990 Jan; 37(1):25-9.
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  111. Huang TJ, Trakshel GM, Maines MD. Microheterogeneity of biliverdin reductase in rat liver and spleen: selective suppression of enzyme variants in liver by bromobenzene. Arch Biochem Biophys. 1989 Nov 1; 274(2):617-25.
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  112. Huang TJ, Trakshel GM, Maines MD. Detection of 10 variants of biliverdin reductase in rat liver by two-dimensional gel electrophoresis. J Biol Chem. 1989 May 15; 264(14):7844-9.
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  113. Huang TJ, Trakshel GM, Maines MD. Multiple forms of biliverdin reductase: modification of the pattern of expression in rat liver by bromobenzene. Arch Biochem Biophys. 1989 May 1; 270(2):513-20.
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  114. Mayer RD, Berman S, Cockett AT, Maines MD. Differential effects of cyclosporin on hepatic and renal heme, cytochrome P-450 and drug metabolism. Possible role in nephrotoxicity of the drug. Biochem Pharmacol. 1989 Mar 15; 38(6):1001-7.
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  115. Trakshel GM, Maines MD. Multiplicity of heme oxygenase isozymes. HO-1 and HO-2 are different molecular species in rat and rabbit. J Biol Chem. 1989 Jan 15; 264(2):1323-8.
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  116. Liccione JJ, Maines MD. Manganese-mediated increase in the rat brain mitochondrial cytochrome P-450 and drug metabolism activity: susceptibility of the striatum. J Pharmacol Exp Ther. 1989 Jan; 248(1):222-8.
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  117. Kutty RK, Maines MD. Selective induction of heme oxygenase-1 isozyme in rat testis by human chorionic gonadotropin. Arch Biochem Biophys. 1989 Jan; 268(1):100-7.
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  118. Liccione JJ, Maines MD. Selective vulnerability of glutathione metabolism and cellular defense mechanisms in rat striatum to manganese. J Pharmacol Exp Ther. 1988 Oct; 247(1):156-61.
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  119. Trakshel GM, Maines MD. Detection of two heme oxygenase isoforms in the human testis. Biochem Biophys Res Commun. 1988 Jul 15; 154(1):285-91.
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  120. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 1988 Jul; 2(10):2557-68.
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  121. Trakshel GM, Maines MD. Characterization of glutathione S-transferases in rat kidney. Alteration of composition by cis-platinum. Biochem J. 1988 May 15; 252(1):127-36.
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  122. Bell JE, Maines MD. Kinetic properties and regulation of biliverdin reductase. Arch Biochem Biophys. 1988 May 15; 263(1):1-9.
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  123. Cruse I, Maines MD. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem. 1988 Mar 5; 263(7):3348-53.
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  124. Kutty RK, Daniel RF, Ryan DE, Levin W, Maines MD. Rat liver cytochrome P-450b, P-420b, and P-420c are degraded to biliverdin by heme oxygenase. Arch Biochem Biophys. 1988 Feb 1; 260(2):638-44.
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  125. Trakshel GM, Kutty RK, Maines MD. Resolution of the rat brain heme oxygenase activity: absence of a detectable amount of the inducible form (HO-1). Arch Biochem Biophys. 1988 Feb 1; 260(2):732-9.
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  126. Trakshel GM, Rowley PT, Maines MD. Regulation of the activity of heme degradative enzymes in K562 erythroleukemic cells: induction by thymidine. Exp Hematol. 1987 Sep; 15(8):859-63.
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  127. Kutty RK, Maines MD. Characterization of an NADH-dependent haem-degrading system in ox heart mitochondria. Biochem J. 1987 Sep 1; 246(2):467-74.
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  128. Chung AS, Maines MD. Differential effect of cadmium on GSH-peroxidase activity in the Leydig and the Sertoli cells of rat testis. Suppression by selenium and the possible relationship to heme concentration. Biochem Pharmacol. 1987 Apr 15; 36(8):1367-72.
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  129. Braggins PE, Trakshel GM, Kutty RK, Maines MD. Characterization of two heme oxygenase isoforms in rat spleen: comparison with the hematin-induced and constitutive isoforms of the liver. Biochem Biophys Res Commun. 1986 Dec 15; 141(2):528-33.
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  130. Trakshel GM, Kutty RK, Maines MD. Cadmium-mediated inhibition of testicular heme oxygenase activity: the role of NADPH-cytochrome c (P-450) reductase. Arch Biochem Biophys. 1986 Nov 15; 251(1):175-87.
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  131. Veltman JC, Maines MD. Regulatory effect of copper on rat adrenal cytochrome P-450 and steroid metabolism. Biochem Pharmacol. 1986 Sep 1; 35(17):2903-9.
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  132. Trakshel GM, Kutty RK, Maines MD. Purification and characterization of the major constitutive form of testicular heme oxygenase. The noninducible isoform. J Biol Chem. 1986 Aug 25; 261(24):11131-7.
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  133. Veltman JC, Maines MD. Alterations of heme, cytochrome P-450, and steroid metabolism by mercury in rat adrenal. Arch Biochem Biophys. 1986 Aug 1; 248(2):467-78.
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  134. Maines MD. Differential effect of cis-platinum (cis-diamminedichloroplatinum) on regulation of liver and kidney haem and haemoprotein metabolism. Possible involvement of gamma-glutamyl-cycle enzymes. Biochem J. 1986 Aug 1; 237(3):713-21.
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  135. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem. 1986 Jan 5; 261(1):411-9.
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  136. Veltman JC, Maines MD. Sex difference in adrenal heme and cytochrome P-450 metabolism: evidence for the repressive regulatory role of testosterone. J Pharmacol Exp Ther. 1985 Oct; 235(1):71-5.
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  137. Jollie DR, Maines MD. Effect of cis-platinum on kidney cytochrome P-450 and heme metabolism: evidence for the regulatory role of the pituitary hormones. Arch Biochem Biophys. 1985 Jul; 240(1):51-9.
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  138. Maines MD, Mayer RD. Inhibition of testicular cytochrome P-450-dependent steroid biosynthesis by cis-platinum. Reversal by human chorionic gonadotropin. J Biol Chem. 1985 May 25; 260(10):6063-8.
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  139. Qato MK, Maines MD. Regulation of heme and drug metabolism activities in the brain by manganese. Biochem Biophys Res Commun. 1985 Apr 16; 128(1):18-24.
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  140. Qato MK, Maines MD. Prevention of neonatal hyperbilirubinaemia in non-human primates by Zn-protoporphyrin. Biochem J. 1985 Feb 15; 226(1):51-7.
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  141. Kutty RK, Maines MD. Effects of induction of heme oxygenase by cobalt and tin on the in vivo degradation of myoglobin. Biochem Pharmacol. 1984 Sep 15; 33(18):2924-6.
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  142. Maines MD, Jollie DR. Dissociation of heme metabolic activities from the microsomal cytochrome P-450 turnover in testis of hypophysectomized rats. J Biol Chem. 1984 Aug 10; 259(15):9557-62.
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  143. Kutty RK, Maines MD. Hepatic heme metabolism: possible role of biliverdin in the regulation of heme oxygenase activity. Biochem Biophys Res Commun. 1984 Jul 18; 122(1):40-6.
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  144. Maines MD. Characterization of heme oxygenase activity in Leydig and Sertoli cells of the rat testes. Differential distribution of activity and response to cadmium. Biochem Pharmacol. 1984 May 1; 33(9):1493-502.
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  145. Maines MD, Veltman JC. Phenylhydrazine-mediated induction of haem oxygenase activity in rat liver and kidney and development of hyperbilirubinaemia. Inhibition by zinc-protoporphyrin. Biochem J. 1984 Jan 15; 217(2):409-17.
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  146. Maines MD. New developments in the regulation of heme metabolism and their implications. Crit Rev Toxicol. 1984; 12(3):241-314.
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  147. Maines MD, Kutty RK. Differential response of testicular and ovarian heme oxygenase activity to metal ions. Arch Biochem Biophys. 1983 Oct 1; 226(1):134-44.
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  148. Kutty RK, Maines MD. Biliverdin reductase: characterization in the rat kidney and the inhibition of activity by mercuric chloride. Biochem Pharmacol. 1983 Jul 1; 32(13):2095-102.
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  149. Maines MD, Chung AS, Kutty RK. The inhibition of testicular heme oxygenase activity by cadmium. A novel cellular response. J Biol Chem. 1982 Dec 10; 257(23):14116-21.
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  150. Chung AS, Maines MD, Reynolds WA. Inhibition of the enzymes of glutathione metabolism by mercuric chloride in the rat kidney: reversal by selenium. Biochem Pharmacol. 1982 Oct 1; 31(19):3093-100.
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  151. Kutty RK, Maines MD. Oxidation of heme c derivatives by purified heme oxygenase. Evidence for the presence of one molecular species of heme oxygenase in the rat liver. J Biol Chem. 1982 Sep 10; 257(17):9944-52.
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  152. Maines MD. Enhancement and inhibition of enzymes of heme metabolism by diethyl maleate in the rat kidney. Arch Biochem Biophys. 1982 Jun; 216(1):17-26.
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  153. Chung AS, Maines MD. Effect of selenium on glutathione metabolism. Induction of gamma-glutamylcysteine synthetase and glutathione reductase in the rat liver. Biochem Pharmacol. 1981 Dec 1; 30(23):3217-23.
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  154. Maines MD, Senft AW. Host heme biosynthesis and degradation in schistosomiasis. Am J Trop Med Hyg. 1981 Sep; 30(5):1010-9.
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  155. Maines MD. Enzymatic basis of metal ion alterations of cellular heme and glutathione metabolism. Fundam Appl Toxicol. 1981 Sep-Oct; 1(5):358-67.
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  156. Kutty RK, Maines MD. Purification and characterization of biliverdin reductase from rat liver. J Biol Chem. 1981 Apr 25; 256(8):3956-62.
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  157. Maines MD. Effect of allylisopropylacetamide on glutathione metabolism in the rat liver. The possible role of glutathione in the induction of 5-aminolaevulinate synthase. Biochem J. 1981 Apr 15; 196(1):285-92.
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  158. Maines MD. Zinc . protoporphyrin is a selective inhibitor of heme oxygenase activity in the neonatal rat. Biochim Biophys Acta. 1981 Mar 18; 673(3):339-50.
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  159. Maines MD. Regional distribution of the enzymes of haem biosynthesis and the inhibition of 5-aminolaevulinate synthase by manganese in the rat brain. Biochem J. 1980 Aug 15; 190(2):315-21.
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  160. Maines MD. Evidence for the catalytic activity of endogenous iron in the lipid peroxidative destruction of heme by allylisopropylacetamide in the rat liver. Int J Biochem. 1980; 12(5-6):781-5.
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  161. Maines MD. Role of trace metals in regulation of cellular heme and hemoprotein metabolism: sensitizing effects of chronic iron treatment on acute gold toxicity. Drug Metab Rev. 1979; 9(2):237-55.
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  162. Maines MD, Kappas A. Prematurely evoked synthesis and induction of delta-aminolevulinate synthetase in neonatal liver. Evidence for metal ion repression of enzyme formation. J Biol Chem. 1978 Apr 10; 253(7):2321-6.
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  163. Maines MD, Kappas A. Metals as regulators of heme metabolism. Science. 1977 Dec 23; 198(4323):1215-21.
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  164. Maines MD, Kappas A. Regulation of cytochrome P-450-dependent microsomal drug-metabolizing enzymes by nickel, cobalt, and iron. Clin Pharmacol Ther. 1977 Nov; 22(5 Pt 2):780-90.
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  165. Maines MD, Kappas A. Enzymes of heme metabolism in the kidney: regulation by trace metals which do not form heme complexes. J Exp Med. 1977 Nov 1; 146(5):1286-93.
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  166. Maines MD, Ibrahim NG, Kappas A. Solubilization and partial purification of heme oxygenase from rat liver. J Biol Chem. 1977 Aug 25; 252(16):5900-3.
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  167. Maines MD, Kappas A. Regulation of heme pathway enzymes and cellular glutathione content by metals that do not chelate with tetrapyrroles: blockade of metal effects by thiols. Proc Natl Acad Sci U S A. 1977 May; 74(5):1875-8.
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  168. Maines MD, Cohn J. Bile pigment formation by skin heme oxygenase: studies on the response of the enzyme to heme compounds and tissue injury. J Exp Med. 1977 Apr 1; 145(4):1054-9.
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  169. Maines MD, Kappas A. Enzymatic oxidation of cobalt protoporphyrin IX: observations on the mechanism of heme oxygenase action. Biochemistry. 1977 Feb 8; 16(3):419-23.
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  170. Maines MD, Sinclair P. Cobalt regulation of heme synthesis and degradation in avian embryo liver cell culture. J Biol Chem. 1977 Jan 10; 252(1):219-23.
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  171. Maines MD, Kappas A. Selenium regulation of hepatic heme metabolism: induction of delta-aminolevulinate synthase and heme oxygenase. Proc Natl Acad Sci U S A. 1976 Dec; 73(12):4428-31.
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  172. Maines MD. Evidence for the catabolism of polychlorinated biphenyl-induced cytochrome P-448 by microsomal heme oxygenase, and the inhibition of delta-aminolevulinate dehydratase by polychlorinated biphenyls. J Exp Med. 1976 Dec 1; 144(6):1509-19.
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  173. Maines MD, Janousek V, Tomio JM, Kappas A. Cobalt inhibition of synthesis and induction of delta-aminolevulinate synthase in liver. Proc Natl Acad Sci U S A. 1976 May; 73(5):1499-503.
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  174. Kappas A, Maines MD. Tin: a potent inducer of heme oxygenase in kidney. Science. 1976 Apr 2; 192(4234):60-2.
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  175. Maines MD, Kappas A. Studies on the mechanism of induction of haem oxygenase by cobalt and other metal ions. Biochem J. 1976 Jan 15; 154(1):125-31.
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  176. Maines MD, Kappas A. The induction of heme oxidation in various tissues by trace metals: evidence for the catabolism of endogenous heme by hepatic heme oxygenase. Ann Clin Res. 1976; 8 Suppl 17:39-46.
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  177. Maines MD, Kappas A. Cobalt stimulation of heme degradation in the liver. Dissociation of microsomal oxidation of heme from cytochrome P-450. J Biol Chem. 1975 Jun 10; 250(11):4171-7.
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  178. Maines MD, Kappas A. Study of the developmental pattern of heme catabolism in liver and the effects of cobalt on cytochrome P-450 and the rate of heme oxidation during the neonatal period. J Exp Med. 1975 Jun 1; 141(6):1400-10.
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  179. Maines MD, Kappas A. The degradative effects of porphyrins and heme compounds on components of the microsomal mixed function oxidase system. J Biol Chem. 1975 Mar 25; 250(6):2363-9.
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  180. Maines MD, Kappas A. Cobalt induction of hepatic heme oxygenase; with evidence that cytochrome P-450 is not essential for this enzyme activity. Proc Natl Acad Sci U S A. 1974 Nov; 71(11):4293-7.
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  181. Maines MD, Anders MW, Muller-Eberhard U. Studies on heme transfer from microsomal hemoproteins to heme-binding plasma proteins. Mol Pharmacol. 1974 Mar; 10(2):204-13.
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  182. Maines MD, Anders MW. Characterization of the heme of cytochrome P-450 using gas chromatography-mass spectrometry. Arch Biochem Biophys. 1973 Nov; 159(1):201-5.
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  183. Maines MD, Anders MW. Reconstitution of carbon monoxide-binding particles after removal of heme by serum albumin. Mol Pharmacol. 1973 Mar; 9(2):219-28.
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  184. Maines MD, Anders MW. The possible implication of heme transfer from cytochrome P-420 to albumin in the metabolism of cytochrome P-450. Drug Metab Dispos. 1973 Jan-Feb; 1(1):293-8.
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  185. Short CR, Maines MD, Davis LE. Preparation of hepatic microsomal fraction for drug metabolism studies by rapid decompression homogenization. Proc Soc Exp Biol Med. 1972 May; 140(1):58-65.
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  186. Short CR, Maines MD, Westfall BA. Postnatal development of drug-metabolizing enzyme activity in liver and extrahepatic tissues of swine. Biol Neonate. 1972; 21(1):54-68.
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  187. Maines MD, Westfall BA. Sex difference in the metabolism of hexobarbital in the mongolian gerbil (Meriones unguiculatus). Proc Soc Exp Biol Med. 1971 Dec; 138(3):820-2.
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  188. Maines MD, Westfall BA. Effect of water deprivation on the metabolism of hexobarbital in the Mongolian gerbil (Meriones unguiculatus). Comp Gen Pharmacol. 1971 Sep; 2(7):311-6.
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  189. Maines MD, Wosilait WD. An autoradiographic study of the distribution and excretion of 14C-dicoumarol in the rat. Comp Gen Pharmacol. 1971 Jun; 2(6):184-8.
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