Biological Trace Element Research

, Volume 187, Issue 1, pp 151–162 | Cite as

Carnosine and Histidine Supplementation Blunt Lead-Induced Reproductive Toxicity through Antioxidative and Mitochondria-Dependent Mechanisms

  • Mohammad Mehdi Ommati
  • Akram Jamshidzadeh
  • Reza HeidariEmail author
  • Zilong Sun
  • Mohammad Javad Zamiri
  • Forouzan Khodaei
  • Saeed Mousapour
  • Fatemeh Ahmadi
  • Nafiseh Javanmard
  • Babak Shirazi Yeganeh


Lead (Pb)-induced reproductive toxicity is a well-characterized adverse effect associated with this heavy metal. It has been found that Pb exposure is associated with altered spermatogenesis, increased testicular degeneration, and pathological sperm alterations. On the other hand, it has been reported that Pb-induced reproductive toxicity is associated with increased reactive oxygen species (ROS) formation and diminished antioxidant capacity in the reproductive system. Hence, administration of antioxidants as protective agents might be of value against Pb-induced reproductive toxicity. This study was designed to investigate whether carnosine (CAR) and histidine (HIS) supplementation would mitigate the Pb-induced reproductive toxicity in male rats. Animals received Pb (20 mg/kg/day, oral, 14 consecutive days) alone or in combination with CAR (250 and 500 mg/kg/day, oral, 14 consecutive days) or HIS (250 and 500 mg/kg/day, oral, 14 consecutive days). Pb toxicity was evident in the reproductive system by a significant increase in tissue markers of oxidative stress along with severe histopathological changes, seminal tubule damage, tubular desquamation, low spermatogenesis index, poor sperm parameters, and impaired sperm mitochondrial function. It was found that CAR and HIS supplementation blunted the Pb-induced oxidative stress and mitochondrial dysfunction in the rat reproductive system. Thereby, antioxidative and mitochondria-protective properties serve as primary mechanisms for CAR and HIS against Pb-induced reproductive toxicity.


Heavy metals Infertility Oxidative stress Peptide Protective 


Funding information

The authors gratefully acknowledge the Pharmaceutical Sciences Research Center and the Vice Chancellor for Research, Shiraz University of Medical Sciences for the financial support (grant no. 95-01-36-11290).

Compliance with Ethical Standards

The rats were killed according to an animal protocol that was approved by the Institutional Animal Ethics Committee of Shiraz University of Medicine (Shiraz, Iran; no. 11290).

Conflict of Interest

The authors declare that they have no conflicts of interest.


  1. 1.
    Wirth JJ, Mijal RS (2010) Adverse effects of low level heavy metal exposure on male reproductive function. Syst Biol Reprod Med 56:147–167PubMedPubMedCentralGoogle Scholar
  2. 2.
    Yu Y, Han Y, Niu R, Wang J, Manthari RK, Ommati MM et al (2017) Ameliorative effect of VE, IGF-I, and hCG on the fluoride-induced testosterone release suppression in mice Leydig cells via the up-regulation of Star and Cyp11a expression. Biol Trace Elem Res 181:95–103PubMedPubMedCentralGoogle Scholar
  3. 3.
    Sun Z, Li S, Yu Y, Chen H, Ommati MM, Manthari RK et al (2017) Alterations in epididymal proteomics and antioxidant activity of mice exposed to fluoride. Arch Toxicol 92:169–180PubMedPubMedCentralGoogle Scholar
  4. 4.
    Elgawish RAR, Abdelrazek HMA (2014) Effects of lead acetate on testicular function and caspase-3 expression with respect to the protective effect of cinnamon in albino rats. Toxicol Rep 1:795–801PubMedPubMedCentralGoogle Scholar
  5. 5.
    Kalia K, Flora SJ (2005) Strategies for safe and effective therapeutic measures for chronic arsenic and lead poisoning. J Occup Health 47:1–21PubMedPubMedCentralGoogle Scholar
  6. 6.
    Hsu PC, Guo YL (2002) Antioxidant nutrients and lead toxicity. Toxicology 180:33–44PubMedPubMedCentralGoogle Scholar
  7. 7.
    Bressler J, Kim KA, Chakraborti T, Goldstein G (1999) Molecular mechanisms of lead neurotoxicity. Neurochem Res 24:595–600PubMedPubMedCentralGoogle Scholar
  8. 8.
    Patra RC, Swarup D, Dwivedi SK (2001) Antioxidant effects of alpha tocopherol, ascorbic acid and L-methionine on lead induced oxidative stress to the liver, kidney and brain in rats. Toxicology 162:81–88PubMedPubMedCentralGoogle Scholar
  9. 9.
    Sandhir R, Gill KD (1995) Effect of lead on lipid peroxidation in liver of rats. Biol Trace Elem Res 48:91–97PubMedPubMedCentralGoogle Scholar
  10. 10.
    Othman AI, El Missiry MA (1998) Role of selenium against lead toxicity in male rats. J Biochem Mol Toxicol 12:345–349PubMedPubMedCentralGoogle Scholar
  11. 11.
    Humphreys DJ (1991) Effects of exposure to excessive quantities of lead on animals. Br Vet J 147:18–30PubMedPubMedCentralGoogle Scholar
  12. 12.
    Ercal N, Neal R, Treeratphan P, Lutz PM, Hammond TC, Dennery PA et al (2000) A role for oxidative stress in suppressing serum immunoglobulin levels in lead-exposed Fisher 344 rats. Arch Environ Contam Toxicol 39:251–256PubMedPubMedCentralGoogle Scholar
  13. 13.
    Skoczynska A, Smolik R, Jelen M (1993) Lipid abnormalities in rats given small doses of lead. Arch Toxicol 67:200–204PubMedPubMedCentralGoogle Scholar
  14. 14.
    Adonaylo VN, Oteiza PI (1999) Lead intoxication: antioxidant defenses and oxidative damage in rat brain. Toxicology 135:77–85PubMedPubMedCentralGoogle Scholar
  15. 15.
    Abdel-Moneim AE, Dkhil MA, Al-Quraishy S (2011) The redox status in rats treated with flaxseed oil and lead-induced hepatotoxicity. Biol Trace Elem Res 143:457–467PubMedPubMedCentralGoogle Scholar
  16. 16.
    Oberley TD, Friedman AL, Moser R, Siegel FL (1995) Effects of lead administration on developing rat kidney. II. Functional, morphologic, and immunohistochemical studies. Toxicol Appl Pharmacol 131:94–107PubMedPubMedCentralGoogle Scholar
  17. 17.
    Hsu PC, Hsu CC, Liu MY, Chen LY, Guo YL (1998) Lead-induced changes in spermatozoa function and metabolism. J Toxicol Environ Health A 55:45–64PubMedPubMedCentralGoogle Scholar
  18. 18.
    Shastri D, Kumar M, Kumar A (1999) Modulation of lead toxicity by Spirulina fusiformis. Phytother Res 13:258–260PubMedPubMedCentralGoogle Scholar
  19. 19.
    Batra N, Nehru B, Bansal MP (1998) The effect of zinc supplementation on the effects of lead on the rat testis. Reprod Toxicol 12:535–540PubMedPubMedCentralGoogle Scholar
  20. 20.
    Wang J, Yang Z, Zhu H, Lin L, Liu Z (2012) Lead-induced oxidative stress and protective effect of naringenin on testis tissues of rats. CNKI 19:2012–2019Google Scholar
  21. 21.
    Xu J, Ji LD, Xu LH (2006) Lead-induced apoptosis in PC 12 cells: involvement of p53, Bcl-2 family and caspase-3. Toxicol Lett 166:160–167PubMedPubMedCentralGoogle Scholar
  22. 22.
    Yin S-T, Tang M-L, Su L, Chen L, Hu P, Wang H-L et al (2008) Effects of Epigallocatechin-3-gallate on lead-induced oxidative damage. Toxicology 249:45–54PubMedPubMedCentralGoogle Scholar
  23. 23.
    Ma L, Liu J-Y, Dong J-X, Xiao Q, Zhao J, Jiang F-L (2017) Toxicity of Pb2+ on rat liver mitochondria induced by oxidative stress and mitochondrial permeability transition. Toxicol Res 6:822–830Google Scholar
  24. 24.
    Amaral A, Lourenço B, Marques M, Ramalho-Santos J (2013) Mitochondria functionality and sperm quality. Reproduction 146:R163–RR74PubMedPubMedCentralGoogle Scholar
  25. 25.
    Piomboni P, Focarelli R, Stendardi A, Ferramosca A, Zara V (2012) The role of mitochondria in energy production for human sperm motility. Int J Androl 35:109–124PubMedPubMedCentralGoogle Scholar
  26. 26.
    Margolis FL, Grillo M, Hempstead J, Morgan JI (1987) Monoclonal antibodies to mammalian carnosine synthetase. J Neurochem 48:593–600PubMedPubMedCentralGoogle Scholar
  27. 27.
    Roberts PR, Zaloga GP (2000) Cardiovascular effects of carnosine. Biochemistry (Mosc) 65:856–861Google Scholar
  28. 28.
    Horinishi H, Grillo M, Margolis FL (1978) Purification and characterization of carnosine synthetase from mouse olfactory bulbs. J Neurochem 31:909–919PubMedPubMedCentralGoogle Scholar
  29. 29.
    Aydın AF, Küçükgergin C, Özdemirler-Erata G, Koçak-Toker N, Uysal M (2009) The effect of carnosine treatment on prooxidant–antioxidant balance in liver, heart and brain tissues of male aged rats. Biogerontology 11:103–109PubMedPubMedCentralGoogle Scholar
  30. 30.
    Fu H, Katsumura Y, Lin M, Muroya Y, Hata K, Fujii K et al (2009) Free radical scavenging and radioprotective effects of carnosine and anserine. Radiat Phys Chem 78:1192–1197Google Scholar
  31. 31.
    Guiotto A, Calderan A, Ruzza P, Borin G (2005) Carnosine and carnosine-related antioxidants: a review. Curr Med Chem 12:2293–2315PubMedPubMedCentralGoogle Scholar
  32. 32.
    Kohen R, Yamamoto Y, Cundy KC, Ames BN (1988) Antioxidant activity of carnosine, homocarnosine, and anserine present in muscle and brain. Proc Nat Acad Sci 85:3175–3179PubMedPubMedCentralGoogle Scholar
  33. 33.
    Nagasawa T, Yonekura T, Nishizawa N, Kitts DD (2001) In vitro and in vivo inhibition of muscle lipid and protein oxidation by carnosine. Mol Cell Biochem 225:29–34PubMedGoogle Scholar
  34. 34.
    Aldini G, Granata P, Carini M (2002) Detoxification of cytotoxic alpha,beta-unsaturated aldehydes by carnosine: characterization of conjugated adducts by electrospray ionization tandem mass spectrometry and detection by liquid chromatography/mass spectrometry in rat skeletal muscle. J Mass Spectrom 37:1219–1228PubMedPubMedCentralGoogle Scholar
  35. 35.
    Abbasoğlu L, Kalaz EB, Soluk-Tekkeşin M, Olgaç V, Doğru-Abbasoğlu S, Uysal M (2012) Beneficial effects of taurine and carnosine in experimental ischemia/reperfusion injury in testis. Pediatr Surg Int 28:1125–1131PubMedPubMedCentralGoogle Scholar
  36. 36.
    Aydın AF, Küçükgergin C, Çoban J, Doğan-Ekici I, Doğru-Abbasoğlu S, Uysal M et al (2018) Carnosine prevents testicular oxidative stress and advanced glycation end product formation in D-galactose-induced aged rats. Andrologia 50.
  37. 37.
    Trimeche A, Yvon JM, Vidament M, Palmer E, Magistrini M (1999) Effects of glutamine, proline, histidine and betaine on post-thaw motility of stallion spermatozoa. Theriogenology 52:181–191PubMedPubMedCentralGoogle Scholar
  38. 38.
    Akahane T, Tsuchiya T, Matsumoto JJ (1981) Freeze denaturation of carp myosin and its prevention by sodium glutamate. Cryobiology 18:426–435PubMedPubMedCentralGoogle Scholar
  39. 39.
    Tsuchiya T, Tsuchiya Y, Nonomura Y, Matsumoto JJ (1975) Prevention of freeze denaturation of carp actomyosin by sodium glutamate. J Biochem 77:853–862PubMedPubMedCentralGoogle Scholar
  40. 40.
    Heinz KA, Glofcheski DJ, Lepock JR, Kruuv J (1990) Mechanism of freeze-thaw damage to liver alcohol dehydrogenase and protection by cryoprotectants and amino acids. Cryobiology 27:521–538PubMedPubMedCentralGoogle Scholar
  41. 41.
    Carpenter JF, Crowe JH (1988) The mechanism of cryoprotection of proteins by solutes. Cryobiology 25:244–255PubMedPubMedCentralGoogle Scholar
  42. 42.
    Lalonde RJ, Lepock JR, Kruuv J (1991) Site of freeze-thaw damage and cryoprotection by amino acids of the calcium ATPase of sarcoplasmic reticulum. Biochim Biophys Acta 1079:128–138PubMedPubMedCentralGoogle Scholar
  43. 43.
    Carpenter JF, Hand SC, Crowe LM, Crowe JH (1986) Cryoprotection of phosphofructokinase with organic solutes: characterization of enhanced protection in the presence of divalent cations. Arch Biochem Biophys 250:505–512PubMedPubMedCentralGoogle Scholar
  44. 44.
    Griveau JF, Dumont E, Renard P, Callegari JP, Le Lannou D (1995) Reactive oxygen species, lipid peroxidation and enzymatic defence systems in human spermatozoa. J Reprod Fertil 103:17–26PubMedPubMedCentralGoogle Scholar
  45. 45.
    El-Batch M, Ibrahim W, Said S (2011) Effect of histidine on autotaxin activity in experimentally induced liver fibrosis. J Biochem Mol Toxicol 25:143–150PubMedPubMedCentralGoogle Scholar
  46. 46.
    Farshid AA, Tamaddonfard E, Belasius MS, Hamzeh-Gooshchi N et al (2009) Histopathological comparison of the effects of histidine and ketotifen in a rat model of colitis. Bull Vet Inst Pulawy 53:795–800Google Scholar
  47. 47.
    Farshid AA, Tamaddonfard E, Yahyaee F (2010) Effects of histidine and N-acetylcysteine on diclofenac-induced anti-inflammatory response in acute inflammation in rats. Indian J Exp Biol 48:1136–1142PubMedPubMedCentralGoogle Scholar
  48. 48.
    Ommati MM, Zamiri MJ, Akhlaghi A, Atashi H, Jafarzadeh MR, Rezvani MR et al (2013) Seminal characteristics, sperm fatty acids, and blood biochemical attributes in breeder roosters orally administered with sage (Salvia officinalis) extract. Anim Prod Sci 53:548–554Google Scholar
  49. 49.
    Fonseca JF, Torres CAA, Maffili VV, Borges AM, Santos ADF, Rodrigues MT et al (2005) The hypoosmotic swelling test in fresh goat spermatozoa. Anim Reprod 2:139–144Google Scholar
  50. 50.
    Ommati MM, Heidari R, Zamiri MJ, Shojaee S, Akhlaghi A, Sabouri S (2017) Association of open field behavior with blood and semen characteristics in roosters: as an alternative animal model. Int Androl.
  51. 51.
    Pursel VG, Johnson LA, Rampacek GB (1972) Acrosome morphology of boar spermatozoa incubated before cold shock. J Anim Sci 34:278–283PubMedPubMedCentralGoogle Scholar
  52. 52.
    Ommati MM, Heidari R, Jamshidzadeh A, Zamiri MJ, Sun Z, Sabouri S et al (2018) Dual effects of sulfasalazine on rat sperm characteristics, spermatogenesis, and steroidogenesis in two experimental models. Toxicol Lett 284:46–55PubMedPubMedCentralGoogle Scholar
  53. 53.
    Ommati MM, Tanideh N, Rezakhaniha B, Wang J, Sabouri S, Vahedi M et al (2018) Is immunosuppression, induced by neonatal thymectomy, compatible with poor reproductive performance in adult male rats? Andrology 6:199–213PubMedPubMedCentralGoogle Scholar
  54. 54.
    Niknahad H, Jamshidzadeh A, Heidari R, Abdoli N, Ommati MM, Jafari F et al (2016) The postulated hepatotoxic metabolite of methimazole causes mitochondrial dysfunction and energy metabolism disturbances in liver. Pharm Sci 22:217–226Google Scholar
  55. 55.
    Jamshidzadeh A, Heidari R, Abasvali M, Zarei M, Ommati MM, Abdoli N et al (2017) Taurine treatment preserves brain and liver mitochondrial function in a rat model of fulminant hepatic failure and hyperammonemia. Biomed Pharmacother 86:514–520PubMedPubMedCentralGoogle Scholar
  56. 56.
    Caro AA, Adlong LW, Crocker SJ, Gardner MW, Luikart EF, Gron LU (2012) Effect of garlic-derived organosulfur compounds on mitochondrial function and integrity in isolated mouse liver mitochondria. Toxicol Lett 214:166–174PubMedPubMedCentralGoogle Scholar
  57. 57.
    Niknahad H, Jamshidzadeh A, Heidari R, Hosseini Z, Mobini K, Khodaei F et al (2016) Paradoxical effect of methimazole on liver mitochondria: in vitro and in vivo. Toxicol Lett 259:108–115PubMedPubMedCentralGoogle Scholar
  58. 58.
    Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Esfandiari A, Azarpira N et al (2018) Dithiothreitol supplementation mitigates hepatic and renal injury in bile duct ligated mice: potential application in the treatment of cholestasis-associated complications. Biomed Pharmacother 99:1022–1032PubMedPubMedCentralGoogle Scholar
  59. 59.
    Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Ommati MM, Abdoli N et al (2018) Mitochondria protection as a mechanism underlying the hepatoprotective effects of glycine in cholestatic mice. Biomed Pharmacother 97:1086–1095PubMedPubMedCentralGoogle Scholar
  60. 60.
    Jamshidzadeh A, Niknahad H, Heidari R, Zarei M, Ommati MM, Khodaei F (2017) Carnosine protects brain mitochondria under hyperammonemic conditions: relevance to hepatic encephalopathy treatment. PharmaNutrition 5:58–63Google Scholar
  61. 61.
    Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205PubMedGoogle Scholar
  62. 62.
    Niknahad H, Heidari R, Mohammadzadeh R, Ommati MM, Khodaei F, Azarpira N et al (2017) Sulfasalazine induces mitochondrial dysfunction and renal injury. Ren Fail 39:745–753PubMedPubMedCentralGoogle Scholar
  63. 63.
    Heidari R, Jamshidzadeh A, Niknahad H, Mardani E, Ommati MM, Azarpira N et al (2016) Effect of taurine on chronic and acute liver injury: focus on blood and brain ammonia. Toxicol Rep 3:870–879PubMedPubMedCentralGoogle Scholar
  64. 64.
    Katalinic V, Modun D, Music I, Boban M (2005) Gender differences in antioxidant capacity of rat tissues determined by 2,2′-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays. Comp Biochem Physiol 140:47–52Google Scholar
  65. 65.
    Heidari R, Moezi L, Asadi B, Ommati MM, Azarpira N (2017) Hepatoprotective effect of boldine in a bile duct ligated rat model of cholestasis/cirrhosis. PharmaNutrition 5:109–117Google Scholar
  66. 66.
    Heidari R, Jamshidzadeh A, Niknahad H, Safari F, Azizi H, Abdoli N et al (2016) The hepatoprotection provided by taurine and glycine against antineoplastic drugs induced liver injury in an ex vivo model of normothermic recirculating isolated perfused rat liver. Trends Pharmacol Sci 2:59–76Google Scholar
  67. 67.
    Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedPubMedCentralGoogle Scholar
  68. 68.
    Blank ML, O'Neill PJ, Steigman CK, Cobb LM, Wilde RA, Havenstein PJ et al (1993) Reperfusion injury following testicular torsion and detorsion in prepubertal rats. Urol Res 21:389–393PubMedPubMedCentralGoogle Scholar
  69. 69.
    Kianifard D, Sadrkhanlou R-A, Hasanzadeh S (2011) The histological, histomorphometrical and histochemical changes of testicular tissue in the metformin treated and untreated streptozotocin-induced adult diabetic rats. Vet Res Forum 3:13–24Google Scholar
  70. 70.
    Dkhil MA, Moneim AEA, Al-Quraishy S (2016) Indigofera oblongifolia ameliorates lead acetate-induced testicular oxidative damage and apoptosis in a rat model. Biol Trace Elem Res 173:354–361PubMedPubMedCentralGoogle Scholar
  71. 71.
    Acharya UR, Acharya S, Mishra M (2003) Lead acetate induced cytotoxicity in male germinal cells of Swiss mice. Ind Health 41:291–294PubMedPubMedCentralGoogle Scholar
  72. 72.
    Graca A, Ramalho-Santos J, de Lourdes PM (2004) Effect of lead chloride on spermatogenesis and sperm parameters in mice. Asian J Androl 6:237–241PubMedPubMedCentralGoogle Scholar
  73. 73.
    Baumber J, Ball BA, Gravance CG, Medina V, Davies-Morel MC (2000) The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential and membrane lipid peroxidation. J Androl 21:895–902PubMedPubMedCentralGoogle Scholar
  74. 74.
    Bazrgar M, Goudarzi I, Lashkarbolouki T, Elahdadi Salmani M (2015) Melatonin ameliorates oxidative damage induced by maternal lead exposure in rat pups. Physiol Behav 151:178–188PubMedPubMedCentralGoogle Scholar
  75. 75.
    Mate JM, Aledo JC, Perez-Gomez C, Esteban del Valle A, Segura JM (2000) Interrelationship between oxidative damage and antioxidant enzyme activities: an easy and rapid experimental approach. Biochem Educ 28:93–95PubMedPubMedCentralGoogle Scholar
  76. 76.
    Kasperczyk A, Kasperczyk S, Horak S, Ostałowska A, Grucka-Mamczar E, Romuk E et al (2008) Assessment of semen function and lipid peroxidation among lead exposed men. Toxicol Appl Pharmacol 228:378–384PubMedPubMedCentralGoogle Scholar
  77. 77.
    Chen L, Yang X, Jiao H, Zhao B (2003) Tea catechins protect against lead-induced ROS formation, mitochondrial dysfunction, and calcium dysregulation in PC12 cells. Chem Res Toxicol 16:1155–1161PubMedPubMedCentralGoogle Scholar
  78. 78.
    Szynaka B, Andrzejewska A, Tomasiak M, Augustynowicz A (1999) Exocrine cell mitochondria of the rat pancreas after lead intoxication. Exp Toxicol Pathol 51:559–564PubMedPubMedCentralGoogle Scholar
  79. 79.
    Xu J, Lian L-j WC, Wang X-f, Fu W-y, Xu L-h (2008) Lead induces oxidative stress, DNA damage and alteration of p53, Bax and Bcl-2 expressions in mice. Food Chem Toxicol 46:1488–1494PubMedPubMedCentralGoogle Scholar
  80. 80.
    Hipkiss AR (2010) Aging, proteotoxicity, mitochondria, glycation, NAD+ and carnosine: possible inter-relationships and resolution of the oxygen paradox. Front Aging Neurosci 2:10PubMedPubMedCentralGoogle Scholar
  81. 81.
    Corona C, Frazzini V, Silvestri E, Lattanzio R, Sorda RL, Piantelli M et al (2011) Effects of dietary supplementation of carnosine on mitochondrial dysfunction, amyloid pathology, and cognitive deficits in 3xTg-AD mice. PLoS One 6:e17971PubMedPubMedCentralGoogle Scholar
  82. 82.
    Kang K-S, Yun J-W, Lee Y-S (2002) Protective effect of l-carnosine against 12-O-tetradecanoylphorbol-13-acetate- or hydrogen peroxide-induced apoptosis on v-myc transformed rat liver epithelial cells. Cancer Lett 178:53–62PubMedPubMedCentralGoogle Scholar
  83. 83.
    Kukreja RC, Loesser KE, Kearns AA, Naseem SA, Hess ML (1993) Protective effects of histidine during ischemia-reperfusion in isolated perfused rat hearts. Am J Phys 264:H1370–H1H81Google Scholar
  84. 84.
    Alves MG, Oliveira PJ, Carvalho RA (2009) Mitochondrial preservation in celsior versus histidine buffer solution during cardiac ischemia and reperfusion. Cardiovasc Toxicol 9:185–193PubMedPubMedCentralGoogle Scholar
  85. 85.
    Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu S-S (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Phys 287:C817–CC33Google Scholar
  86. 86.
    Schaffer SW, Suleiman MS (2010) Mitochondria: the dynamic organelle. Springer Science & Business Media, New York 359 pGoogle Scholar
  87. 87.
    Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183PubMedPubMedCentralGoogle Scholar
  88. 88.
    Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913–922PubMedPubMedCentralGoogle Scholar
  89. 89.
    Canabady-Rochelle LLS, Harscoat-Schiavo C, Kessler V, Aymes A, Fournier F, Girardet J-M (2015) Determination of reducing power and metal chelating ability of antioxidant peptides: revisited methods. Food Chem 183:129–135PubMedPubMedCentralGoogle Scholar
  90. 90.
    Leberman R, Rabin BR (1959) Metal complexes of histidine. Trans Faraday Soc 55:1660–1670Google Scholar
  91. 91.
    Sundberg RJ, Martin RB (1974) Interactions of histidine and other imidazole derivatives with transition metal ions in chemical and biological systems. Chem Rev 74:471–517Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Mohammad Mehdi Ommati
    • 1
    • 2
  • Akram Jamshidzadeh
    • 1
  • Reza Heidari
    • 1
    Email author return OK on get
  • Zilong Sun
    • 2
  • Mohammad Javad Zamiri
    • 3
  • Forouzan Khodaei
    • 1
  • Saeed Mousapour
    • 3
  • Fatemeh Ahmadi
    • 1
  • Nafiseh Javanmard
    • 1
  • Babak Shirazi Yeganeh
    • 4
  1. 1.Pharmaceutical Sciences Research CenterShiraz University of Medical SciencesShirazIran
  2. 2.Shanxi Key Laboratory of Ecological Animal Science and Environmental MedicineAgricultural UniversityTaiguPeople’s Republic of China
  3. 3.Department of Animal Science, College of AgricultureShiraz UniversityShirazIran
  4. 4.Department of Pathology, School of MedicineShiraz University of Medical SciencesShirazIran

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