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Review Article

Unifying mechanism for metals in toxicity, carcinogenicity and therapeutic action: integrated approach involving electron transfer, oxidative stress, antioxidants, cell signaling and receptors

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Pages 51-60 | Received 09 Nov 2009, Accepted 09 Dec 2009, Published online: 10 Feb 2010

References

  • Kovacic P, Becvar LE. Mode of action of anti-infective agents: emphasis on oxidative stress and electron transfer. Curr Pharmaceut Des 2000;6:143–67.
  • Kovacic P, Osuna JA. Mechanisms of anticancer agents: emphasis on oxidative stress and electron transfer. Curr Pharmaceut Des 2000;6:277–309.
  • Kovacic P, Jacintho JD. Mechanisms of carcinogenesis: focus on oxidative stress and electron transfer. Curr Med Chem 2001;8:773–96.
  • Kovacic P, Jacintho JD. Reproductive toxins: pervasive theme of oxidative stress and electron transfer. Curr Med Chem 2001;8:863–92.
  • Kovacic P, Sacman A, Wu-Weis M. Nephrotoxins: widespread role of oxidative stress and electron transfer. Curr Med Chem 2002;9:823–47.
  • Poli G, Cheesman KH, Dianzani MU, Slater TF. Free Radicals in the Pathogenesis of Liver Injury. New York: Pergamon Press, 1989:1–330.
  • Kovacic P, Thurn LA. Cardiovascular toxicity from the perspective of oxidative stress, electron transfer, and prevention by antioxidants. Curr Vasc Pharmacol 2005;3:107–17.
  • Kovacic P, Somanathan R. Neurotoxicity: the broad framework of electron transfer, oxidative stress and protection by antioxidants. Curr Med Chem-CNS Agents 2005;5:249–58.
  • Kovacic P, Pozos RS, Somanathan R, Shangari N, O’Brien PJ. Mechanism of mitochondrial uncouplers, inhibitors, and toxins: focus on electron transfer, free radicals, and structure-activity relationships. Curr Med Chem 2005;12:2601–23.
  • Kovacic P, Cooksy AL. Unifying mechanism for toxicity and addiction by abused drugs: electron transfer and reactive oxygen species. Med Hypotheses 2005;64:366–7.
  • Kovacic P, Somanathan R. Ototoxicity and noise trauma: electron transfer, reactive oxygen species, cell signaling, electrical effects, and protection by antioxidants: practical medical aspects. Med Hypotheses 2008;70:914–23.
  • Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. New York: Oxford University Press, 1999:1–897.
  • Bard AJ (ed.). Encyclopedia of Electrochemistry of the Elements. Vol I–IX. New York: Marcel Dekker, 1973–1986.
  • Huang X. Iron overload and its association with cancer risk in humans: evidence for iron as a carcinogenic metal. Mutat Res 2003;533:153–71.
  • Yen HC, Chang HM, Majima HJ, Chen FY, Li SH. Levels of reactive oxygen species and primary antioxidant enzymes in WI38 versus transformed WI38 cells following bleomcyin treatment. Free Radic Biol Med 2005;38:950–9.
  • Asai T, Ohno Y, Minatoguchi S, Funaguchi N, Yuhgetsu H, Sawada M, Takemura G, Komada A, Fujiwara T, Fujiwara H. The specific free radical scavenger edaravone suppresses bleomycin-induced acute pulmonary injury in rabbits. Clin Exp Pharmacol Physiol 2007;34:22–6.
  • Reeder BJ, Hider RC, Wilson MT. Iron chelators can protect against oxidative stress through ferryl heme reduction. Free Radic Biol Med 2008;44:264–73.
  • Kalinowski DS, Richardson DR. Future of toxicology—iron chelators and differing modes of action and toxicity: the changing face of iron chelation therapy. Chem Res Toxicol 2007;20:715–20.
  • Stanley N, Stadler N, Woods AA, Bannon PG, Davies MJ. Concentrations of iron correlate with the extent of protein, but not lipid, oxidation in advanced human atherosclerotic lesions. Free Radic Biol Med 2006;40:1636–43.
  • Kallianpur AR. Iron and oxidative injury—a commentary on “Fatty acid-mediated iron translocation: a synergistic mechanism of oxidative injury” by D. Yao et al. Free Radic Biol Med 2005;39:1305–9.
  • Waldman WJ, Kristovich R, Knight DA, Dutta PK. Inflammatory properties of iron-containing carbon nanoparticles. Chem Res Toxicol 2007;20:1149–54.
  • Gazzano E, Turci F, Foresti E, Putzu MG, Aldieri E, Silvagno F, Lesci IG, Tomatis M, Riganti C, Romano C, Fubini B, Roveri N, Ghigo D. Iron-loaded synthetic chrysotile: a new model solid for studying the role of iron in asbestos toxicity. Chem Res Toxicol 2007;20:380–7.
  • Van Campenhout A, Van Campenhout C, Lagrou A, Manuel-y-Keenoy B. Iron-induced oxidative stress in haemodialysis patients: a pilot study on the impact of diabetes. Biometals 2008;21:159–70.
  • Yang PM, Chen HC, Tsai JS, Lin LY. Cadmium induces Ca2+-dependent necrotic cell death through calpain-triggered mitochondrial depolarization and reactive oxygen species-mediated inhibition of nuclear factor-kappaB activity. Chem Res Toxicol 2007;20:406–15.
  • Monroe RK, Halvorsen SW. Cadmium blocks receptor-mediated Jak/STAT signaling in neurons by oxidative stress. Free Radic Biol Med 2006;41:493–502.
  • López E, Arce C, Oset-Gasque MJ, Cañadas S, González MP. Cadmium induces reactive oxygen species generation and lipid peroxidation in cortical neurons in culture. Free Radic Biol Med 2006;40:940–51.
  • Yano CL, Marcondes MC. Cadmium chloride-induced oxidative stress in skeletal muscle cells in vitro. Free Radic Biol Med 2005;39:1378–84.
  • Yang Z, Yang S, Qian SY, Hong JS, Kadiiska MB, Tennant RW, Waalkes MP, Liu J. Cadmium-induced toxicity in rat primary mid-brain neuroglia cultures: role of oxidative stress from microglia. Toxicol Sci 2007;98:488–94.
  • Filipic M, Fatur T, Vudrag M. Molecular mechanisms of cadmium induced mutagenicity. Hum Exp Toxicol 2006;25:67–77.
  • Hsu YT, Kao CH. Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil 2007;298:231–41.
  • Yang HS, Han DK, Kim JR, Sim JC. Effects of alpha-tocopherol on cadmium-induced toxicity in rat testis and spermatogenesis. J Korean Med Sci 2006;21:445–51.
  • Amin A, Hamza AA, Daoud S, Hamza W. Spirulina protects against cadmium-induced hepatotoxicity in rats. Am J Pharmacol Toxicol 2006;1:21–5.
  • Pathak N, Khandelwal S. Impact of cadmium in T lymphocyte subsets and cytokine expression: differential regulation by oxidative stress and apoptosis. Biometals 2008;21:179–87.
  • Doreswamy K, Shrilatha B, Rajeshkumar T, Muralidhara. Nickel-induced oxidative stress in testis of mice: evidence of DNA damage and genotoxic effects. J Androl 2004;25:996–1003.
  • Lu H, Shi X, Costa M, Huang C. Carcinogenic effect of nickel compounds. Mol Cell Biochem 2005;279:45–67.
  • Kang J, Zhang Y, Chen J, Chen H, Lin C, Wang Q, Ou Y. Nickel-induced histone hypoacetylation: the role of reactive oxygen species. Toxicol Sci 2003;74:279–286.
  • Kasprzak KS, Bal W, Karaczyn AA. The role of chromatin damage in nickel-induced carcinogenesis. A review of recent developments. J Environ Monit 2003;5:183–7.
  • Randhawa VK, Zhou F, Jin X, Nalewajko C, Kushner DJ. Role of oxidative stress and thiol antioxidant enzymes in nickel toxicity and resistance in strains of the green alga Scenedesmus acutus f. alternans. Can J Microbiol 2001;47:987–93.
  • Kelly MC, Whitaker G, White B, Smyth MR. Nickel(II)-catalysed oxidative guanine and DNA damage beyond 8-oxoguanine. Free Radic Biol Med 2007;42:1680–9.
  • Das KK, Gupta AD, Dhundasi SA, Patil AM, Das SN, Ambekar JG. Protective role of L-ascorbic acid on antioxidant defense system in erythrocytes of albino rats exposed to nickel sulfate. Biometals 2007;20:177–84.
  • Nurminen M. Overview of the human carcinogenicity risk assessment of metallic chromium and trivalent chromium. Internet J Epidemiol 2005;2:1.
  • Porter R, Jáchymová M, Martásek P, Kalyanaraman B, Vásquez-Vivar J. Reductive activation of Cr(Vi) by nitric oxide synthase. Chem Res Toxicol 2005;18:834–43.
  • Borthiry GR, Antholine WE, Kalyanaraman B, Myers JM, Myers CR. Reduction of hexavalent chromium by human cytochrome b5: generation of hydroxyl radical and superoxide. Free Radic Biol Med 2007;42:738–55; discussion 735.
  • Yang PH, Gao HY, Cai J, Chiu JF, Sun H, He QY. The stepwise process of chromium-induced DNA breakage: characterization by electrochemistry, atomic force microscopy, and DNA electrophoresis. Chem Res Toxicol 2005;18:1563–6.
  • Zhitkovich A. Importance of chromium-DNA adducts in mutagenicity and toxicity of chromium(VI). Chem Res Toxicol 2005;18:3–11.
  • Levina A, Lay PA. Chemical properties and toxicity of chromium(III) nutritional supplements. Chem Res Toxicol 2008;21:563–71.
  • Shi H, Hudson LG, Ding W, Wang S, Cooper KL, Liu S, Chen Y, Shi X, Liu KJ. Arsenite causes DNA damage in keratinocytes via generation of hydroxyl radicals. Chem Res Toxicol 2004;17:871–8.
  • Naranmandura H, Ibata K, Suzuki KT. Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem Res Toxicol 2007;20:1120–5.
  • Hei TK, Filipic M. Role of oxidative damage in the genotoxicity of arsenic. Free Radic Biol Med 2004;37:574–81.
  • Habib GM, Shi ZZ, Lieberman MW. Glutathione protects cells against arsenite-induced toxicity. Free Radic Biol Med 2007;42:191–201.
  • Bower JJ, Leonard SS, Chen F, Shi X. As(III) transcriptionally activates the gadd45a gene via the formation of H2O2. Free Radic Biol Med 2006;41:285–94.
  • Mishra D, Mehta A, Flora SJ. Reversal of arsenic-induced hepatic apoptosis with combined administration of DMSA and its analogues in guinea pigs: role of glutathione and linked enzymes. Chem Res Toxicol 2008;21:400–7.
  • Franco JL, Braga HC, Stringari J, Missau FC, Posser T, Mendes BG, Leal RB, Santos AR, Dafre AL, Pizzolatti MG, Farina M. Mercurial-induced hydrogen peroxide generation in mouse brain mitochondria: protective effects of quercetin. Chem Res Toxicol 2007;20:1919–26.
  • Aschner M, Syversen T, Souza DO, Rocha JB. Metallothioneins: mercury species-specific induction and their potential role in attenuating neurotoxicity. Exp Biol Med (Maywood) 2006;231:1468–73.
  • Cargnelutti D, Tabaldi LA, Spanevello RM, de Oliveira Jucoski G, Battisti V, Redin M, Linares CE, Dressler VL, de Moraes Flores EM, Nicoloso FT, Morsch VM, Schetinger MR. Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 2006;65:999–1006.
  • Patrick L. Lead toxicity part II: the role of free radical damage and the use of antioxidants in the pathology and treatment of lead toxicity. Altern Med Rev 2006;11:114–27.
  • Yedjou CG, Tchounwou PB. N-acetyl-l-cysteine affords protection against lead-induced cytotoxicity and oxidative stress in human liver carcinoma (HepG2) cells. Int J Environ Res Public Health 2007;4:132–7.
  • Bokara KK, Brown E, McCormick R, Yallapragada PR, Rajanna S, Bettaiya R. Lead-induced increase in antioxidant enzymes and lipid peroxidation products in developing rat brain. Biometals 2008;21:9–16.
  • Hayashi T, Shishido N, Nakayama K, Nunomura A, Smith MA, Perry G, Nakamura M. Lipid peroxidation and 4-hydroxy-2-nonenal formation by copper ion bound to amyloid-beta peptide. Free Radic Biol Med 2007;43:1552–9.
  • Hong H, Cao H, Wang Y, Wang Y. Identification and quantification of a guanine-thymine intrastrand cross-link lesion induced by Cu(II)/H2O2/ascorbate. Chem Res Toxicol 2006;19:614–21.
  • Cai X, Pan N, Zou G. Copper-1,10-phenanthroline-induced apoptosis in liver carcinoma Bel-7402 cells associates with copper overload, reactive oxygen species production, glutathione depletion and oxidative DNA damage. Biometals 2007;20:1–11.
  • Yao X, Panichpisal K, Kurtzman N, Nugent K. Cisplatin nephrotoxicity: a review. Am J Med Sci 2007;334:115–24.
  • Lu Y, Cederbaum A. The mode of cisplatin-induced cell death in CYP2E1-overexpressing HepG2 cells: modulation by ERK, ROS, glutathione, and thioredoxin. Free Radic Biol Med 2007;43:1061–75.
  • Huang HL, Fang LW, Lu SP, Chou CK, Luh TY, Lai MZ. DNA-damaging reagents induce apoptosis through reactive oxygen species-dependent Fas aggregation. Oncogene 2003;22:8168–77.
  • Kim JS, Lee JH, Jeong WW, Choi DH, Cha HJ, Kim do H, Kwon JK, Park SE, Park JH, Cho HR, Lee SH, Park SK, Lee BJ, Min YJ, Park JW. Reactive oxygen species-dependent EndoG release mediates cisplatin-induced caspase-independent apoptosis in human head and neck squamous carcinoma cells. Int J Cancer 2008;122:672–80.
  • Berndtsson M, Hägg M, Panaretakis T, Havelka AM, Shoshan MC, Linder S. Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int J Cancer 2007;120:175–80.
  • Kawai Y, Gemba M. Cisplatin-induced renal injury in LLC-PK1 cells. AATEX 2007;14:453–6.
  • Kawai Y, Nakao T, Kunimura N, Kohda Y, Gemba M. Relationship of intracellular calcium and oxygen radicals to Cisplatin-related renal cell injury. J Pharmacol Sci 2006;100:65–72.
  • Preston TJ, Henderson JT, McCallum GP, Wells PG. Cellular models of altered base excision repair reveal a differential contribution of reactive oxygen species-induced 7,8-dihydro-8-oxo-2′-deoxyguanosine to the cytotoxic mechanisms of platinum anticancer drugs cisplatin and oxaliplatin. FASEB J 2007;21:890.11.
  • Rybak LP. Mechanisms of cisplatin ototoxicity and progress in otoprotection. Curr Opin Otolaryngol Head Neck Surg 2007;15:364–9.
  • Sheen N, Ajith TA, Janardhanan KK. Prevention of nephrotoxicity induced by the anticancer drug cisplatin, using Ganoderma lucidum, a medicinal mushroom occurring in South India. Current Sci 2003;85:478–82.
  • Fukutomi J, Fukuda A, Fukuda S, Hara M, Terada A, Yoshida M. Scavenging activity of indole compounds against cisplatin-induced reactive oxygen species. Life Sci 2006;80:254–7.
  • Ray S, Roy K, Sengupta C. Cisplatin-induced lipid peroxidation and its inhibition with ascorbic acid. Indian J Pharmaceut Sci 2006;68:199–204.
  • Ali BH, Al-Moundhri M, Eldin MT, Nemmar A, Al-Siyabi S, Annamalai K. Amelioration of cisplatin-induced nephrotoxicity in rats by tetramethylpyrazine, a major constituent of the Chinese herb Ligusticum wallichi. Exp Biol Med (Maywood) 2008;233:891–6.
  • Milaeva E, Petrosyan V, Berberova N, Pimenov Y, Pellerito L. Organic derivatives of mercury and tin as promoters of membrane lipid peroxidation. Bioinorg Chem Appl 2004;2:69–91.
  • Dwivedi RS, Kaur G, Srivastava RC, Krishna Murti CR. Lipid peroxidation in tin intoxicated partially hepatectomized rats. Bull Environ Contam Toxicol 1984;33:200–9.
  • O’Connor K, Gill C, Tacke M, Rehmann FJ, Strohfeldt K, Sweeney N, Fitzpatrick JM, Watson RW. Novel titanocene anti-cancer drugs and their effect on apoptosis and the apoptotic pathway in prostate cancer cells. Apoptosis 2006;11:1205–14.
  • Hogan M, Claffey J, Pampillón C, Tacke M. Synthesis and cytotoxicity studies of new morpholino-functionalised and N-heteroaryl-substituted titanocene anticancer drugs. Med Chem 2008;4:91–9.
  • Kovacic P, Popp WJ, Ames JR, Ryan MD. Anti-cancer action of metal complexes: electron transfer and oxidative stress? Anticancer Drug Des 1988;3:205–16.
  • Bishop GM, Dringen R, Robinson SR. Zinc stimulates the production of toxic reactive oxygen species (ROS) and inhibits glutathione reductase in astrocytes. Free Radic Biol Med 2007;42:1222–30.
  • Oikawa S, Hirosawa I, Tada-Oikawa S, Furukawa A, Nishiura K, Kawanishi S. Mechanism for manganese enhancement of dopamine-induced oxidative DNA damage and neuronal cell death. Free Radic Biol Med 2006;41:748–56.
  • Yoshimaru T, Suzuki Y, Inoue T, Niide O, Ra C. Silver activates mast cells through reactive oxygen species production and a thiol-sensitive store-independent Ca2+ influx. Free Radic Biol Med 2006;40:1949–59.
  • Sawyer RT, Dobis DR, Goldstein M, Velsor L, Maier LA, Fontenot AP, Silveira L, Newman LS, Day BJ. Beryllium-stimulated reactive oxygen species and macrophage apoptosis. Free Radic Biol Med 2005;38:928–37.
  • Rose S, Melnyk S, Savenka A, Hubanks A, Jernigan S, Cleves M, James SJ. The frequency of polymorphisms affecting lead and mercury toxicity among children with autism. Am J Biochem Biotechnol 2008;4:85–94.
  • Mahmodabady ABZ, Saberi M, Eimani H, Pyrzad J, Sharifabady RR. Cytotoxic and oxidative stress caused by cadmium and lead on human skin fibroblast cells. Yakhteh Med J 2006;8:172–7.
  • Hegedűs A, Harrach BD, Bárdos G, Erdei S. What is the crucial difference between the metabolic consequences of cadmium and zinc treatment of the plants? Acta Biolog Szeged 2005;49:55–60.
  • Jimi S, Uchiyama M, Takaki A, Suzumiya J, Hara S. Mechanisms of cell death induced by cadmium and arsenic. Ann N Y Acad Sci 2004;1011:325–31.
  • Agarwal R, Behari JR. Role of selenium in mercury intoxication in mice. Ind Health 2007;45:388–95.
  • Chen C, Yu H, Zhao J, Li B, Qu L, Liu S, Zhang P, Chai Z. The roles of serum selenium and selenoproteins on mercury toxicity in environmental and occupational exposure. Environ Health Perspect 2006;114:297–301.
  • Company R, Serafim A, Bebianno MJ, Cosson R, Shillito B, Fiala-Médioni A. Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 2004;58:377–81.
  • Eichler T, Ma Q, Kelly C, Mishra J, Parikh S, Ransom RF, Devarajan P, Smoyer WE. Single and combination toxic metal exposures induce apoptosis in cultured murine podocytes exclusively via the extrinsic caspase 8 pathway. Toxicol Sci 2006;90:392–9.
  • Harris GK, Shi X. Signaling by carcinogenic metals and metal-induced reactive oxygen species. Mutat Res 2003;533:183–200.
  • Mehta A, Shaha C. Mechanism of metalloid-induced death in Leishmania spp.: role of iron, reactive oxygen species, Ca2+, and glutathione. Free Radic Biol Med 2006;40:1857–68.
  • Desoize B. Cancer and metals and metal compounds, Part I—Carcinogenesis (Editorial). Critical Rev Oncol/Hematol 2002;42:1–3.
  • Hartwig A. Recent advances in metal carcinogenicity. Pure Appl Chem 2000;72:1007–14.
  • Pourahmad J, O’Brien PJ, Jokar F, Daraei B. Carcinogenic metal induced sites of reactive oxygen species formation in hepatocytes. Toxicol In Vitro 2003;17:803–10.
  • Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006;160:1–40.
  • Valavanidis A, Vlahoyianni T, Fiotakis K. Comparative study of the formation of oxidative damage marker 8-hydroxy-2′-deoxyguanosine (8-OHdG) adduct from the nucleoside 2′-deoxyguanosine by transition metals and suspensions of particulate matter in relation to metal content and redox reactivity. Free Radic Res 2005;39:1071–81.
  • Stavrides JC. Lung carcinogenesis: pivotal role of metals in tobacco smoke. Free Radic Biol Med 2006;41:1017–30.
  • Li N, Xia T, Nel AE. The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic Biol Med 2008;44:1689–99.
  • Sabolic I. Common mechanisms in nephropathy induced by toxic metals. Nephron Physiol 2006;104: p 107–14.
  • Malešev D, Kuntić V. Investigation of metal-flavonoid chelates and the determination of flavonoids via metal-flavonoid complexing reactions. J Serb Chem Soc 2007;72:921–39.
  • Ragan CI. Metal ions in neuroscience. Met Based Drugs 1997;4:125–32.
  • Anonymous. Diabetes and mercury poisoning. Medical News Commentaries October 2006.
  • Wu W, Jaspers I, Zhang W, Graves LM, Samet JM. Role of Ras in metal-induced EGF receptor signaling and NF-kappaB activation in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2002;282:L1040–8.
  • Kovacic P, Pozos RS, Draskovich CD. Unifying electrostatic mechanism for receptor-ligand activity. J Recept Signal Transduct Res 2007;27:411–31.
  • Kovacic P, Pozos RS. Bioelectronome. Integrated approach to receptor chemistry, radicals, electrochemistry, cell signaling, and physiological effects based on electron transfer. J Recept Signal Transduct Res 2007;27:261–94.
  • Samet JM, Graves LM, Quay J, Dailey LA, Devlin RB, Ghio AJ, Wu W, Bromberg PA, Reed W. Activation of MAPKs in human bronchial epithelial cells exposed to metals. Am J Physiol 1998;275:L551–8.
  • Hetland RB, Myhre O, Låg M, Hongve D, Schwarze PE, Refsnes M. Importance of soluble metals and reactive oxygen species for cytokine release induced by mineral particles. Toxicology 2001;165:133–44.
  • Smith JB, Smith L, Pijuan V, Zhuang Y, Chen YC. Transmembrane signals and protooncogene induction evoked by carcinogenic metals and prevented by zinc. Environ Health Perspect 1994;102(Suppl 3):181–9.
  • Samet JM, Silbajoris R, Wu W, Graves LM. Tyrosine phosphatases as targets in metal-induced signaling in human airway epithelial cells. Am J Respir Cell Mol Biol 1999;21:357–64.
  • Turski ML, Thiele DJ. New roles for copper metabolism in cell proliferation, signaling, and disease. J Biol Chem 2009;284:717–21.
  • Kitagaki M, Hirota M. Auricular chondritis caused by metal ear tagging in C57BL/6 mice. Vet Pathol 2007;44:458–66.
  • Kovacic P, Pozos RS. Cell signaling (mechanism and reproductive toxicity): redox chains, radicals, electrons, relays, conduit, electrochemistry, and other medical implications. Birth Defects Res C Embryo Today 2006;78:333–44.
  • Kovacic P, Draskovich CD, Pozos RS. Unifying electrostatic mechanism for phosphates and sulfates in cell signaling. J Recept Signal Transduct Res 2007;27:433–43.
  • Kovacic P. Unifying electrostatic mechanism for metal cations in receptors and cell signaling. J Recept Signal Transduct, 2008;66:153–62.
  • Kovacic P. Bioelectrostatics: review of widespread importance in biochemistry. J Electrostat 2008;66:124–9.
  • Forman HG, Caddenas E (eds.). Oxidative Stress and Signal Transduction. New York: Springer, 1997:475.
  • Hancock GT. Cell Signaling. New York, NY: Oxford University Press, 2005:296.
  • Kovacic P. Protein electron transfer (mechanism and reproductive toxicity): iminium, hydrogen bonding, homoconjugation, amino acid side chains (redox and charged), and cell signaling. Birth Defects Res Part C 2007;81:51–64.
  • Campbell NA. Biology. New York: Benjamin/Cummings, 1993:99.
  • Dong J, Ye P, Schade AJ, Gao S, Romo GM, Turner NT, McIntire LV, López JA. Tyrosine sulfation of glycoprotein I(b)alpha. Role of electrostatic interactions in von Willebrand factor binding. J Biol Chem 2001;276:16690–4.
  • Duisit G, Saleun S, Douthe S, Barsoum J, Chadeuf G, Moullier P. Baculovirus vector requires electrostatic interactions including heparan sulfate for efficient gene transfer in mammalian cells. J Gene Med 1999;1:93–102.
  • Gomperte BD, Tathem PER, Kramer IM. Signal Transduction. New York, NY: Academic Press, 2002:173–82.

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