Melatonin attenuates hypochlorous acid-mediated heme destruction, free iron release, and protein aggregation in hemoglobin

Journal of Pineal Research

Volumn 53, Issue 2, 2012, Pages 198-205

  Maitra, Dhiman ^a   Abdulhamid, Ibrahim ^b   Diamond, Michael P ^a   Saed, Ghassan M ^a   Abu Soud, Husam M ^a,c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Chlidren's Hospital of Michigan   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

free iron; hemoglobin; hypochlorous acid; inflammation; mammalian peroxidase; myeloperoxidase; oxidative stress; RBCs

Indexed keywords

FERROZINE; HEME; HEMOGLOBIN; HEMOPROTEIN; HYPOCHLOROUS ACID; IRON; MELATONIN; MYELOPEROXIDASE; PORPHYRIN;

ARTICLE; CHRONIC INFLAMMATORY DEMYELINATING POLYNEUROPATHY; COLORIMETRY; CONTROLLED STUDY; ERYTHROCYTE; HUMAN; HUMAN CELL; IRON KINETICS; NORMAL HUMAN; PROTEIN AGGREGATION; SCAVENGING SYSTEM; STAINING; ULTRAVIOLET SPECTROPHOTOMETRY;

ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEME; HEMOGLOBINS; HYPOCHLOROUS ACID; IRON; MELATONIN; OXIDATIVE STRESS; PEROXIDASE; SPECTROPHOTOMETRY;

EID: 84865000736     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2012.00988.x     Document Type: Article

References (58)

1. Gastel JA, Roseboom PH, Rinaldi PA, et al., Melatonin production: proteasomal proteolysis in serotonin N-acetyltransferase regulation. Science 1998; 279: 1358-1360.
2. Stehle JH, Saade A, Rawashdeh O, et al., A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases. J Pineal Res 2011; 51: 17-43.
3. Hardeland R,. Melatonin: signaling mechanisms of a pleiotropic agent. BioFactors 2009; 35: 183-192.
4. Yu HS, Yee RW, Howes KA, et al., Diurnal rhythms of immunoreactive melatonin in the aqueous humor and serum of male pigmented rabbits. Neurosci Lett 1990; 116: 309-314.
5. Skinner DC, Malpaux B,. High melatonin concentrations in third ventricular cerebrospinal fluid are not due to Galen vein blood recirculating through the choroid plexus. Endocrinology 1999; 140: 4399-4405.
6. Tan D, Manchester LC, Reiter RJ, et al., High physiological levels of melatonin in the bile of mammals. Life Sci 1999; 65: 2523-2529.
7. Nakamura Y, Tamura H, Takayama H, et al., Increased endogenous level of melatonin in preovulatory human follicles does not directly influence progesterone production. Fertil Steril 2003; 80: 1012-1016.
8. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
9. Carrillo-Vico A, Guerrero J, Lardone P, et al., A review of the multiple actions of melatonin on the immune system. Endocrine 2005; 27: 189-200.
10. Markus RP, Ferreira ZS, Fernandes PA, et al., The immune-pineal axis: a shuttle between endocrine and paracrine melatonin sources. Neuroimmunomodulation 2007; 14: 126-133.
11. Reiter RJ,. Melatonin: the chemical expression of darkness. Mol Cell Endocrinol 1991; 79: C153-C158.
12. Jung KH, Hong SW, Zheng HM, et al., Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats. J Pineal Res 2010; 48: 239-250.
13. Chahbouni M, Escames G, Venegas C, et al., Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/oxidative stress in patients suffering from Duchenne muscular dystrophy. J Pineal Res 2010; 48: 282-289.
14. Jung-Hynes B, Reiter RJ, Ahmad N,. Sirtuins, melatonin and circadian rhythms: building a bridge between aging and cancer. J Pineal Res 2010; 48: 9-19.
15. Park SY, Jang WJ, Yi EY, et al., Melatonin suppresses tumor angiogenesis by inhibiting HIF-1alpha stabilization under hypoxia. J Pineal Res 2010; 48: 178-184.
16. Jung-Hynes B, Huang W, Reiter RJ, et al., Melatonin resynchronizes dysregulated circadian rhythm circuitry in human prostate cancer cells. J Pineal Res 2010; 49: 60-68.
17. Reiter RJ,. Pineal melatonin: cell biology of its synthesis and of its physiological interactions. Endocr Rev 1991; 12: 151-180.
18. Reiter RJ, Tan DX, Fuentes-Broto L,. Melatonin: a multitasking molecule. Prog Brain Res 2010; 181: 127-151.
19. Dellegar SM, Murphy SA, Bourne AE, et al., Identification of the factors affecting the rate of deactivation of hypochlorous acid by melatonin. Biochem Biophys Res Commun 1999; 257: 431-439.
20. Tesoriere L, D'Arpa D, Conti S, et al., Melatonin protects human red blood cells from oxidative hemolysis: new insights into the radical-scavenging activity. J Pineal Res 1999; 27: 95-105.
21. Galijasevic S, Abdulhamid I, Abu-Soud HM,. Melatonin is a potent inhibitor for myeloperoxidase. Biochemistry 2008; 47: 2668-2677.
22. Lu T, Galijasevic S, Abdulhamid I, et al., Analysis of the mechanism by which melatonin inhibits human eosinophil peroxidase. Br J Pharmacol 2008; 154: 1308-1317.
23. Tesoriere L, Avellone G, Ceraulo L, et al., Oxidation of melatonin by oxoferryl hemoglobin: a mechanistic study. Free Radical Res 2001; 35: 633-642.
24. Davies MJ, Hawkins CL, Pattison DI, et al., Mammalian heme peroxidases: from molecular mechanisms to health implications. Antioxid Redox Signal 2008; 10: 1199-1234.
25. Pennathur S, Maitra D, Byun J, et al., Potent antioxidative activity of lycopene: a potential role in scavenging hypochlorous acid. Free Radic Biol Med 2010; 49: 205-213.
26. Mohamed AO, Hashim MS, Nilsson UR, et al., Increased in vivo activation of neutrophils and complement in sickle cell disease. Am J Trop Med Hyg 1993; 49: 799-803.
27. Maitra D, Byun J, Andreana PR, et al., Reaction of hemoglobin with HOCl: mechanism of heme destruction and free iron release. Free Radic Biol Med 2011; 51: 374-386.
28. Maitra D, Byun J, Andreana PR, et al., Mechanism of hypochlorous acid-mediated heme destruction and free iron release. Free Radic Biol Med 2011; 51: 364-373.
29. Souza CE, Maitra D, Saed GM, et al., Hypochlorous Acid-induced heme degradation from lactoperoxidase as a novel mechanism of free iron release and tissue injury in inflammatory diseases. PLoS ONE 2011; 6: e27641.
30. Ong WY, Halliwell B,. Iron, atherosclerosis, and neurodegeneration: a key role for cholesterol in promoting iron-dependent oxidative damage? Ann N Y Acad Sci 2004; 1012: 51-64.
31. Trinder D, Fox C, Vautier G, et al., Molecular pathogenesis of iron overload. Gut 2002; 51: 290-295.
32. Defrere S, Lousse JC, Gonzalez-Ramos R, et al., Potential involvement of iron in the pathogenesis of peritoneal endometriosis. Mol Hum Reprod 2008; 14: 377-385.
33. Chau LY,. Iron and atherosclerosis. Proc Natl Sci Counc Repub China B 2000; 24: 151-159.
34. Clark RA,. Oxidative stress and "senescent" fibroblasts in non-healing wounds as potential therapeutic targets. J Invest Dermatol 2008; 128: 2361-2364.
35. Carter P,. Spectrophotometric determination of serum iron at the submicrogram level with a new reagent (ferrozine). Anal Biochem 1971; 40: 450-458.
36. Laemmli UK,. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685.
37. Thomas PE, Ryan D, Levin W,. An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 1976; 75: 168-176.
38. Galijasevic S, Maitra D, Lu T, et al., Myeloperoxidase interaction with peroxynitrite: chloride deficiency and heme depletion. Free Radic Biol Med 2009; 47: 431-439.
39. Fonseca AM, Porto G, Uchida K, et al., Red blood cells inhibit activation-induced cell death and oxidative stress in human peripheral blood T lymphocytes. Blood 2001; 97: 3152-3160.
40. Wang L, Bassiri M, Najafi R, et al., Hypochlorous acid as a potential wound care agent: part I. Stabilized hypochlorous acid: a component of the inorganic armamentarium of innate immunity. J Burns Wounds 2007; 6: e5.
41. Chapman AL, Winterbourn CC, Brennan SO, et al., Characterization of non-covalent oligomers of proteins treated with hypochlorous acid. Biochem J 2003; 375: 33-40.
42. Nagababu E, Chrest FJ, Rifkind JM,. Hydrogen-peroxide-induced heme degradation in red blood cells: the protective roles of catalase and glutathione peroxidase. Biochim Biophys Acta 2003; 1620: 211-217.
43. Nagababu E, Rifkind JM,. Heme degradation by reactive oxygen species. Antioxid Redox Signal 2004; 6: 967-978.
44. Marshall KA, Reiter RJ, Poeggeler B, et al., Evaluation of the antioxidant activity of melatonin in vitro. Free Radic Biol Med 1996; 21: 307-315.
45. Maitra D, Banerjee J, Shaeib F, et al., Melatonin can mediate its vascular protective effect by modulating free iron level by inhibiting hypochlorous acid-mediated hemoprotein heme destruction. Hypertension 2011; 57: e22; author reply e23.
46. Herzog P, Feig SA,. Methaemoglobinaemia in the newborn infant. Clin Haematol 1978; 7: 75-83.
47. Kumar S, Bandyopadhyay U,. Free heme toxicity and its detoxification systems in human. Toxicol Lett 2005; 157: 175-188.
48. Crichton RR, Wilmet S, Legssyer R, et al., Molecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells. J Inorg Biochem 2002; 91: 9-18.
49. Guerrero JM, Reiter RJ, Ortiz GG, et al., Melatonin prevents increases in neural nitric oxide and cyclic GMP production after transient brain ischemia and reperfusion in the Mongolian gerbil (Meriones unguiculatus). J Pineal Res 1997; 23: 24-31.
50. Tan DX, Manchester LC, Reiter RJ, et al., Ischemia/reperfusion-induced arrhythmias in the isolated rat heart: prevention by melatonin. J Pineal Res 1998; 25: 184-191.
51. Bertuglia S, Marchiafava PL, Colantuoni A,. Melatonin prevents ischemia reperfusion injury in hamster cheek pouch microcirculation. Cardiovasc Res 1996; 31: 947-952.
52. Kang JW, Koh EJ, Lee SM,. Melatonin protects liver against ischemia and reperfusion injury through inhibition of toll-like receptor signaling pathway. J Pineal Res 2011; 50: 403-411.
53. Ross CA, Poirier MA,. What is the role of protein aggregation in neurodegeneration? Nat Rev Mol Cell Biol 2005; 6: 891-898.
54. David DC, Ollikainen N, Trinidad JC, et al., Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 2010; 8: e1000450.
55. Gilad E, Zisapel N,. High-affinity binding of melatonin to hemoglobin. Biochem Mol Med 1995; 56: 115-120.
56. Ames BN, Cathcart R, Schwiers E, et al., Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: a hypothesis. Proc Natl Acad Sci U S A 1981; 78: 6858-6862.
57. Patel RP, Hogg N, Kim-Shapiro DB,. The potential role of the red blood cell in nitrite-dependent regulation of blood flow. Cardiovasc Res 2011; 89: 507-515.
58. Huang Z, Shiva S, Kim-Shapiro DB, et al., Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J Clin Invest 2005; 115: 2099-2107.