Alpha lipoic acid supplementation ameliorates the wrath of simulated tropical heat and humidity stress in male Murrah buffaloes

  • H. A. Samad
  • Y. Y. Konyak
  • S. K. Latheef
  • A. Kumar
  • I. A. Khan
  • V. Verma
  • V. S. Chouhan
  • M. R. Verma
  • V. P. Maurya
  • Puneet Kumar
  • M. Sarkar
  • G. SinghEmail author
Original Paper


A supplement which ameliorates temperature-humidity menace in food producing livestock is a prerequisite to develop climate smart agricultural packages. A study was conducted to investigate the heat stress ameliorative efficacy of alpha lipoic acid (ALA) in male Murrah water buffaloes (Bubalus bubalis). Eighteen animals (293.61 ± 4.66Kg Bwt) were randomly allocated into three groups (n = 6); NHSC (non-heat-stressed control), HS (heat-stressed) and HSLA (heat-stressed-supplemented with ALA@32 mg/kg Bwt orally) based on the temperature humidity index (THI) and ALA supplementation. HS and HSLA were exposed to simulated heat challenge in a climatically controlled chamber (40 °C) for 21 consecutive days, 6 h daily. Physiological responses viz. Respiration rate (RR), Pulse rate (PR) and Rectal temperature (RT) were recorded daily before and after heat exposure. Blood samples were collected at the end of heat exposure on days 1, 6, 11, 16, and 21 and on day 28 (7th day post exposure which is considered as recovery) for peripheral blood mononuclear cells (PBMCs) separation, followed by RNA and Protein extraction for Real time quantitative PCR and Western blot analysis respectively, of heat shock proteins (HSPs). Two-way repeated measure ANOVA was performed between groups at different experimental periods. RR (post exposure) in HS and HSLA was significantly higher (P < 0.05) than NHSC from day 1 onwards but HSLA varied significantly from the HS 8th day onwards. Post exposure RT and PR in both HS and HSLA varied (P < 0.05) from NHSC throughout the study; but between HS and HSLA, RT significantly varied on initial 2 days and last 6 days (from days 16 to 21). HSP70 mRNA expression significantly up regulated in high THI groups with respect to the low THI group throughout the experimental period. During chronic stress (days 16 and 21) HSP70 significantly (P < 0.05) increased in HS but not in HSLA (P > 0.05) with respect to NHSC. ALA supplementation up-regulates and sustains (P < 0.05) the expression of HSP90 in HSLA in comparison to the HS and NHSC. HSP105 expression was significantly up-regulated (P < 0.05) in HS on days 16 and 21 (during long-term exposure) but only on day 21 (P < 0.05) in HSLA. HSP70, HSP90, and HSP105 protein expression dynamics were akin to the mRNA transcript data between the study groups. In conclusion, supplementing ALA ameliorates the deleterious effect of heat stress as reflected by improved physiological and cellular responses. ALA supplementation improved cellular antioxidant status and sustained otherwise easily decaying heat shock responses which concertedly hasten the baton change from a limited window of thermo tolerance to long run acclimatization.


Alpha lipoic acid Murrah buffaloes Heat stress HSPs Physiological responses 


Funding information

The National Initiative on Climate Resilient Agriculture (NICRA)—Indian Council of Agricultural Research (ICAR) project entitled “Adaptation strategies in livestock to thermal stress through nutritional and environmental manipulations” financially assisted to carry out the study.

Compliance with ethical standards

Permission and ethical clearance for animal experimentation had been granted by Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA), Ministry of environment, Forest and climate change Government of India and institute animal ethics committee(IAEC) of the ICAR-Indian Veterinary Research Institute (IVRI), Izzatnagar, UP, India.


  1. Abadi A, Crane JD, Ogborn D, Hettinga B, Akhtar M, Stokl M, MacNeil L, Safdar A, Tarnopolsky M (2013) Supplementation with α-lipoic acid, CoQ10, and vitamin E augments running performance and mitochondrial function in female mice. PLoS One 8(4):e60722CrossRefGoogle Scholar
  2. Agarwal A, Upadhyay R (2013) Heat stress and reproduction. In: Heat stress and animal productivity, pp.79–111Google Scholar
  3. Agnew LL, Colditz IG (2008) Development of a method of measuring cellular stress in cattle and sheep. Vet Immunol Immunopathol 123(3–4):197–204CrossRefGoogle Scholar
  4. Akbarian A, Michiels J, Degroote J, Majdeddin M, Golian A, Smet S (2016) Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals. J Anim Sci Biotechno 7(1):37CrossRefGoogle Scholar
  5. Aleena J, Sejian V, Bagath M, Krishnan G, Beena V, Bhatta R (2018) Resilience of three indigenous goat breeds to heat stress based on phenotypic traits and PBMC HSP70 expression. Int J Biometeorol 62:1995–2005CrossRefGoogle Scholar
  6. Almeida L, Barajas R (2001) Effect of Cr-methionine level supplementation on immune response of bull claves recently arrived to feedlot. J Anim Sci 79(Suppl. 1:390CrossRefGoogle Scholar
  7. Ambrosi N, Guerrieri D, Caro F, Sanchez F, Haeublein G, Casadei D, Incardona C, Chuluyan E (2018) Alpha lipoic acid: a therapeutic strategy that tend to limit the action of free radicals in transplantation. Int J Mol Sci 19(1):102CrossRefGoogle Scholar
  8. Armstrong CG, Kenney WL (1993) Effects of age and acclimation on responses to passive heat exposure. J Appl Physiol 75(5):2162–2167CrossRefGoogle Scholar
  9. Baumgard LH, Rhoads RP, Rhoads ML, Gabler NK, Ross JW, Keating AF, Boddicker RL, Lenka S, Sejian V (2012) Impact of climate change on livestock production. In: Sejian V, Naqvi SMK, Ezeji T, Lakritz J Lal R (eds) Environmental stress and amelioration in livestock production. Springer-Verlag, Berlin, pp 413–468CrossRefGoogle Scholar
  10. Beckham JT, Mackanos MA, Crooke C, Takahashi T, O'Connell-Rodwell C, Contag CH, Jansen ED (2004) Assessment of cellular response to thermal laser injury through bioluminescence imaging of heat shock protein 70. Photochem Photobiol 79:76–85CrossRefGoogle Scholar
  11. Beis LY, Polyviou T, Malkova D, Pitsiladis YP (2011) The effects of creatine and glycerol hyperhydration on running economy in well trained endurance runners. JISSN 8(1):24Google Scholar
  12. Bharati J, Dangi SS, Bag S, Maurya VP, Singh G, Kumar P, Sarkar M (2017) Expression dynamics of HSP90 and nitric oxide synthase (NOS) isoforms during heat stress acclimation in Tharparkar cattle. Int J Biometeorol 61(8):1461–1469CrossRefGoogle Scholar
  13. Collier RJ, Collier JL, Rhoads RP, Baumgard LH (2008) Genes involved in the bovine heat stress response. J Dairy Sci 91(2):445–454Google Scholar
  14. Collier RJ, Stiening CM, Pollard BC, VanBaale MJ, Baumgard LH, Gentry PC, Coussens PM (2006) Use of gene expression microarrays for evaluating environmental stress tolerance at the cellular level in cattle. J Anim Sci 84(suppl_13):E1–E3CrossRefGoogle Scholar
  15. Craig EA, Gross CA (1991) Is hsp70 the cellular thermometer? TIBS 16:135–140Google Scholar
  16. Dangi SS, Dangi SK, Chouhan VS, Verma MR, Kumar P, Singh G, Sarkar M (2016) Modulatory effect of betaine on expression dynamics of HSPs during heat stress acclimation in goat (Capra hircus). Gene 575(2):543–550CrossRefGoogle Scholar
  17. Dangi SS, Gupta M, Nagar V, Yadav VP, Dangi SK, Shankar O, Chouhan VS, Kumar P, Singh G, Sarkar M (2014) Impact of short-term heat stress on physiological responses and expression profile of HSPs in Barbari goats. Int J Biometeorol 58(10):2085–2093CrossRefGoogle Scholar
  18. Dash S, Chakravarty AK, Singh A, Sah V, Shivahre PR, Panmei A (2015) Identification of best temperature humidity index model for pregnancy rate of Murrah buffaloes in a subtropical climate. Indian J Dairy Sci 68(1):45–49Google Scholar
  19. Deb R, Sajjanar B, Singh U, Kumar S, Singh R, Sengar G, Sharma A (2014) Effect of heat stress on the expression profile of Hsp90 among Sahiwal (Bos indicus) and Frieswal (Bos indicus× Bos taurus) breed of cattle: a comparative study. Gene 536(2):435–440CrossRefGoogle Scholar
  20. Ducray HA, Globa L, Pustovyy O, Reeves S, Robinson L, Vodyanoy V, Sorokulova I (2016) Mitigation of heat stress-related complications by a yeast fermentate product. J Therm Biol 60:26–32CrossRefGoogle Scholar
  21. Easton C, Turner S, Pitsiladis YP (2007) Creatine and glycerol hyperhydration in trained subjects before exercise in the heat. Int J Sport Nutr Exerc Metab 17(1):70–91CrossRefGoogle Scholar
  22. Fuchs J, Schofer H, Milbradt R (1993) Studies on lipoate effects on blood redox state in human immunodeficiency virus infected patients. Arznei-Forschung 43:1359–1362Google Scholar
  23. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 286(3):433–442CrossRefGoogle Scholar
  24. Gaughan JB, Bonner SL, Loxton I, Mader TL (2013) Effects of chronic heat stress on plasma concentration of secreted heat shock protein 70 in growing feedlot cattle. J Anim Sci 91(1):120–129CrossRefGoogle Scholar
  25. Grad I, Picard D (2007) The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol 275(1–2):2–12CrossRefGoogle Scholar
  26. Gyanendra S, Hooda OK, Mahapatra RK, Meur SK, Varshney VP (2009) Ameliorative effect of zinc and manganese supplementation in buffalo calves during hot climatic conditions. Indian J Anim Sci 79(11):1153–1155Google Scholar
  27. Haak E, Usadel KH, Kusterer K, Amini P, Frommeyer R, Tritschler HJ, Haak T (2000) Effects of alpha-lipoic acid on microcirculation in patients with peripheral diabetic neuropathy. Exp Clin Endocrinol Diabetes 108(3):168–174CrossRefGoogle Scholar
  28. Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV (2001) Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am J Physiol Heart Circ Physiol 280(2):H509–H521CrossRefGoogle Scholar
  29. Hall DM, Xu L, Drake VJ, Oberley LW, Oberley TD, Moseley PL, Kregel KC (2000) Aging reduces adaptive capacity and stress protein expression in the liver after heat stress. J Appl Physiol 89(2):749–759CrossRefGoogle Scholar
  30. Hansen PJ (2004) Physiological and cellular adaptations of zebu cattle to thermal stress. Anim Reprod Sci 82:349–360CrossRefGoogle Scholar
  31. Hao LY, Wang J, Sun P, Bu DP (2016) The effect of heat stress on the metabolism of dairy cows: updates & review. Austin J Nutr Metab 3(1):1036Google Scholar
  32. Heitzer T, Finckh B, Albers S, Krohn K, Kohlschutter A, Meinertz T (2001) Beneficial effects of alpha-lipoic acid and ascorbic acid on endothelium-dependent, nitric oxide-mediated vasodilation in diabetic patients: relation to parameters of oxidative stress. Free Radic Biol Med 31:53–61CrossRefGoogle Scholar
  33. Horowitz M (2001) Heat acclimation: phenotypic plasticity and cues to the underlying molecular mechanism. J Therm Biol 26:357–363CrossRefGoogle Scholar
  34. Horowitz M (2007) Heat acclimation and cross-tolerance against novel stressors: genomic–physiological linkage. Prog Brain Res 162:373–392CrossRefGoogle Scholar
  35. Ishihara K, Yasuda K, Hatayama T (1999) Molecular cloning, expression and localization of human 105 kDa heat shock protein, hsp105. Biochim Biophys Acta 1444(1):138–142CrossRefGoogle Scholar
  36. Kenney WL, Morgan AL, Farquhar WB, Brooks EM, Pierzga JM, Derr JA (1997) Decreased active vasodilator sensitivity in aged skin. Am J Physiol Heart Circ Physiol 272(4):H1609–H1614CrossRefGoogle Scholar
  37. Kenney WL, Tankersley CG, Newswanger DL, Hyde DE, Puhl SM, Turner NL (1990) Age and hypohydration independently influence the peripheral vascular response to heat stress. J Appl Physiol 68:1902–1908CrossRefGoogle Scholar
  38. Kishore A, Sodhi M, Khate K, Kapila N, Kumari P, Mukesh M (2013) Selection of stable reference genes in heat stressed peripheral blood mononuclear cells of tropically adapted Indian cattle and buffaloes. Mol Cell Probes 27(3–4):140–144CrossRefGoogle Scholar
  39. Kishore A, Sodhi M, Kumari P, Mohanty AK, Sadana DK, Kapila N, Khate K, Shandilya U, Kataria RS, Mukesh M (2014) Peripheral blood mononuclear cells: a potential cellular system to understand differential heat shock response across native cattle (Bos indicus) exotic cattle (Bos taurus), and riverine buffaloes (Bubalus bubalis) of India. Cell Stress Chaperones 19(5):613–662CrossRefGoogle Scholar
  40. Kregel KC (2002) Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92(5):2177–2186CrossRefGoogle Scholar
  41. Kumar A, Ashraf S, Goud TS, Grewal A, Singh SV, Yadav BR, Upadhyay RC (2015a) Expression profiling of major heat shock protein genes during different seasons in cattle (Bos indicus) and buffalo (Bubalus bubalis) under tropical climatic condition. J Therm Biol 51:55–64CrossRefGoogle Scholar
  42. Kumar M, Kaur H, Deka RS, Mani V, Tyagi AK, Chandra (2015b) Dietary inorganic chromium in summer exposed buffalo calves (Bubalus bubalis): effects on biomarkers of heat stress, immune status and endocrine variables. Biol Trace Elem Res 167:18–27CrossRefGoogle Scholar
  43. Lacetera N, Bernabucci U, Scalia D, Basirico L, Morera P, Nardone A (2006) Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. J Dairy Sci 89:4606–4612CrossRefGoogle Scholar
  44. Landry J, Bernier D, Chrétien P, Nicole LM, Tanguay RM, Marceau N (1982) Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 42(6):2457–2461Google Scholar
  45. Leiva T, Cooke RF, Brandão AP, Schubach KM, Batista LF, Miranda MF, Colombo EA, Rodrigues RO, Junior JR, Cerri RL, Vasconcelos JL (2017) Supplementing an immunomodulatory feed ingredient to modulate thermoregulation, physiologic, and production responses in lactating dairy cows under heat stress conditions. J Dairy Sci 100(6):4829–4838CrossRefGoogle Scholar
  46. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22(1):631–677CrossRefGoogle Scholar
  47. Liu Z, Patil I, Sancheti H, Yin F, Cadenas E (2017) Effects of lipoic acid on high-fat diet-induced alteration of synaptic plasticity and brain glucose metabolism: a PET/CT and 13 C-NMR study. Sci Rep 7(1):5391CrossRefGoogle Scholar
  48. Luo S, Wang T, Qin H, Lei H, Xia Y (2011) Obligatory role of heat shock protein 90 in iNOS induction. Am J Phys Cell Phys 301(1):C227–C233CrossRefGoogle Scholar
  49. Maibam U, Hooda OK, Sharma PS, Mohanty AK, Singh SV, Upadhyay RC (2017) Expression of HSP70 genes in skin of zebu (Tharparkar) and crossbred (Karan fries) cattle during different seasons under tropical climatic conditions. J Therm Biol 63:58–64CrossRefGoogle Scholar
  50. Manjari R, Yadav M, Ramesh K, Uniyal S, Rastogi SK, Sejian V, Hyder I (2015) HSP70 as a marker of heat and humidity stress in Tarai buffalo. Trop Anim Health Prod 47(1):111–116CrossRefGoogle Scholar
  51. McDowell RE (1972) Improvement of livestock production in warm climate. WH Freeman and Co., San Francisco, pp 51–53Google Scholar
  52. Mishra A, Hooda OK, Singh G, Meur SK (2011) Influence of induced heat stress on HSP70 in buffalo lymphocytes. J Anim Physiol Anim Nutr 95(4):540–544CrossRefGoogle Scholar
  53. Mishra SR, Thakur N, Somal A, Parmar MS, Yadav VP, Bharati J, Bharti MK, Paul A, Verma MR, Chouhan VS, Sharma GT (2016) Expression and localization of angiopoietin family in buffalo ovarian follicles during different stages of development and modulatory role of angiopoietins on steroidogenesis and survival of cultured buffalo granulosa cells. Theriogenol 86(7):1818–1833CrossRefGoogle Scholar
  54. Mujahid A, Akiba Y, Toyomizu M (2009) Olive oil-supplemented diet alleviates acute heat stress-induced mitochondrial ROS production in chicken skeletal muscle. Am J Physio Regul Integr Comp Physiol 297:R690–R698CrossRefGoogle Scholar
  55. Nizar AN, Mudasir S, Hina AW (2013) Oxidative stress – threat to animal health and production. Int J Livest Res 3:76–83Google Scholar
  56. NRC (1981) Effect of Environment on nutrient requirements of domestic animals. National Academy Press, Washington, DCGoogle Scholar
  57. Olson TA, Lucena C, Chase CC, Hammond AC (2003) Evidence of a major gene influencing hair length and heat tolerance in Bos taurus cattle. J Anim Sci 81(1):80–90CrossRefGoogle Scholar
  58. Packer L (1998) Alpha-lipoic acid: a metabolic antioxidant which regulates NF-kappa B signal transduction and protects against oxidative injury. Drug Metab Rev 30:245–275CrossRefGoogle Scholar
  59. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27(1):437–496CrossRefGoogle Scholar
  60. Pasha TN, Hayat Z (2012) Present situation and future perspective of buffalo production in Asia. J Anim Plant Sci 22(3 Suppl):250–256Google Scholar
  61. Patir H, Upadhyay RC (2010) Purification, characterization and expression kinetics of heat shock protein 70 from Bubalus bubalis. Res Vet Sci 88(2):258–262CrossRefGoogle Scholar
  62. Pearl LH, Prodromou C, Workman P (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 410(3):439–453CrossRefGoogle Scholar
  63. Pfaffl M (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007CrossRefGoogle Scholar
  64. Polsky L, von Keyserlingk MA (2017) Invited review: effects of heat stress on dairy cattle welfare. J Dairy Sci 100(11):8645–8657CrossRefGoogle Scholar
  65. Polyviou TP, Pitsiladis YP, Lee WC, Pantazis T, Hambly C, Speakman JR, Malkova D (2012) Thermoregulatory and cardiovascular responses to creatine, glycerol and alpha lipoic acid in trained cyclists. JISSN 9(1):29Google Scholar
  66. Renaudeau D, Collin A, Yahav S, de Basilio V, Gourdine JL, Collier RJ (2012) Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 6(5):707–728CrossRefGoogle Scholar
  67. Renis M, Cardile V, Grasso S, Palumbo M, Scifo C (2003) Switching off HSP70 and i-NOS to study their role in normal and H2O2-stressed human fibroblasts. Life Sci 74(6):757–769CrossRefGoogle Scholar
  68. Rhoads RP, Baumgard LH, Suagee JK, Sanders SR (2013) Nutritional interventions to alleviate the negative consequences of heat stress. Adv Nutr 4:267–276CrossRefGoogle Scholar
  69. Rojas-Downing MM, Nejadhashemi AP, Harrigan T, Woznicki SA (2017) Climate change and livestock: impacts, adaptation, and mitigation. Clim Risk Manag 16:145–163CrossRefGoogle Scholar
  70. Ryan AJ, Gisolfi CV, Moseley PL (1991) Synthesis of 70K stress protein by human leukocytes: effect of exercise in the heat. J Appl Physiol 70(1):466–471CrossRefGoogle Scholar
  71. Schmidt TB, Brown MS, Larson RL, Kleiboeker SB, Olson KC, Keisler D, Carroll JA, Berg EP (2005) Effect of dietary lipoic acid on metabolic hormones and acute phase proteins during challenge with infectious bovine rhinotrachitis virus in cattle. AJVR 67(7):1192–1198CrossRefGoogle Scholar
  72. Sejian V, Singh AK, Sahoo A, Naqvi SM (2014) Effect of mineral mixture and antioxidant supplementation on growth, reproductive performance and adaptive capability of M alpura ewes subjected to heat stress. J Anim Physiol Anim Nutr 98(1):72–83CrossRefGoogle Scholar
  73. Sethi RK, Nagarcenkar R (1981) Inheritance of heat tolerance in buffaloes. Indian J Anim Sci 51:591–595Google Scholar
  74. Shilja S, Sejian V, Bagath M, Mech A, David ICG, Kurien EK, Varma G, Bhatta R (2016) Adaptive capability as indicated by behavioral and physiological responses, plasma HSP70 level and PBMC HSP70 mRNA expression in Osmanabadi goats subjected to combined (heat and nutritional) stressors. Int J Biomateriol 60:1311–1323Google Scholar
  75. Singh M, Chaudhari BK, Singh JK, Singh AK, Maurya PK (2013) Effects of thermal load on buffalo reproductive performance during summer season. J Biol Sci 1(1):1–8Google Scholar
  76. Sola S, Mir MQ, Cheema FA, Khan-Merchant N, Menon RG, Parthasarathy S, Khan BV (2005) Irbesartan and lipoic acid improve endothelial function and reduce markers of inflammation in the metabolic syndrome: results of the Irbesartan and lipoic acid in endothelial dysfunction (ISLAND) study. Circulation 111(3):343–348CrossRefGoogle Scholar
  77. Sorensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037CrossRefGoogle Scholar
  78. Vidyalekshmi GM (2016) Effect of chromium supplementation on physiological, biochemichal responses and expression of HSP & TLR in buffaloes during heat stress. Thesis, M.V.Sc. Deemed University, Indian Veterinary Research Institute, Izatnagar, IndiaGoogle Scholar
  79. Vilela RA, Titto CG, Leme TMDC, Sommavilla R, Silva SDL, Pereira RMF (2015) Behaviour of adaptive buffaloes with access to thermal comfort resources. XVII Congresso Latino-americano deBuiatria e XIcongresso Brasileiro de BuiatriaGoogle Scholar
  80. Wallen ES, Buettner GR, Moseley PL (1997) Oxidants differentially regulate the heat shock response. Int J Hyperth 13(5):517–524CrossRefGoogle Scholar
  81. Yamagishi N, Ishihara K, Saito Y, Hatayama T (2003) Hsp105 but not Hsp70 family proteins suppress the aggregation of heat denatured protein in the presence of ADP. FEBS Lett 555(2):390–396CrossRefGoogle Scholar
  82. Yamagishi N, Nishihori H, Ishihara K, Ohtsuka K, Hatayama T (2000) Modulation of the chaperone activities of Hsc70/Hsp40 by Hsp105alpha and Hsp105beta. Biochem Biophys Res Commun 272(3):850–855CrossRefGoogle Scholar
  83. Zhang HJ, Doctrow SR, Xu L, Oberley LW, Beecher B, Morrison J, Oberley TD, Kregel KC (2004) Redox modulation of the liver with chronic antioxidant enzyme mimetic treatment prevents age-related oxidative damage associated with environmental stress. FASEB 18(13):1547–1549CrossRefGoogle Scholar
  84. Zhang HJ, Xu L, Drake VJ, Xie L, Oberley LW, Kregel KC (2003) Heat-induced liver injury in old rats is associated with exaggerated oxidative stress and altered transcription factor activation. FASEB 17(15):2293–2295CrossRefGoogle Scholar
  85. Zhang H, Doctrow SR, Oberley LW, Kregel KC (2006) Chronic antioxidant enzyme mimetic treatment differentially modulates hyperthermia-induced liver HSP70 expression with aging. J Appl Physiol 100:1385–1391CrossRefGoogle Scholar
  86. Zuo L, Christofi FL, Wright VP, Liu CY, Merola AJ, Berliner LJ, Clanton TL (2000) Intra- and extracellular measurement of reactive oxygen species produced during heat stress in diaphragm muscle. Am J Phys Cell Phys 279:C1058–C1066CrossRefGoogle Scholar

Copyright information

© ISB 2019

Authors and Affiliations

  • H. A. Samad
    • 1
  • Y. Y. Konyak
    • 1
  • S. K. Latheef
    • 2
  • A. Kumar
    • 1
  • I. A. Khan
    • 3
  • V. Verma
    • 1
  • V. S. Chouhan
    • 1
  • M. R. Verma
    • 4
  • V. P. Maurya
    • 1
  • Puneet Kumar
    • 1
  • M. Sarkar
    • 1
  • G. Singh
    • 1
    Email author
  1. 1.Division of Physiology & ClimatologyICAR-IndianVeterinary Research InstituteBareillyIndia
  2. 2.Division of PathologyICAR-IndianVeterinary Research InstituteBareillyIndia
  3. 3.Dolphin PG Institue of Biomedical & Natural ScienceDehradunIndia
  4. 4.Division of Livestock economics and statisticsICAR-IndianVeterinary Research InstituteBareillyIndia

Personalised recommendations