Abstract
Commercial poultry production is associated with various stresses decreasing productive and reproductive performance of layers. A growing body of evidence indicates that most of stresses in poultry production at the cellular level are associated with oxidative stress due to excess of free radical production or inadequate antioxidant protection. Recently, a concept of the cellular antioxidant defence has been revised with a special attention paid to cell signalling. Antioxidant systems of the living cell is based on three major levels of defence and include several options and vitagene activation in stress conditions is considered as a fundamental adaptive mechanism. The vitagene family includes various genes responsible for synthesis of protective molecules such as thioredoxins, SOD, sirtuins and heat shock proteins (HSP). Indeed, HSP70, HSP90 and HSP32 (heme oxygenase) are among important elements of the antioxidant system network. However, by the time of writing no comprehensive review on the roles and effects of HSP in poultry biology has appeared. Therefore, the aim of this review is a critical analysis of the role of HSP in poultry biology with a specific emphasis to their functions as an essential part of the vitagene network. From the analysis of the recent data related to HSP in poultry physiology and adaptation to stresses it is possible to conclude that: a) HSP as important vitagenes are main driving force in cell/body adaptation to various stress conditions. Indeed, in stress conditions synthesis of most cellular proteins decreases while HSP expression is usually significantly increased; b) HSP as cellular chaperones are responsible for proteostasis and involved in protein quality control in the cell to prevent misfolding or to facilitate degradation, making sure that proteins are in optimal structure for their biological activities; c) there are tissue-specific differences in HSP expression which also depends on the strength of such stress-factors as heat, heavy metals, mycotoxins and other toxicants; d) HSP70, HSP90 and HSP32 are shown to be protective in heat stress, toxicity stress as well as in other oxidative-stress related conditions in poultry production; e) molecular mechanisms of HSP participation in acquisition of thermotolerance need further detailed investigation; f) there are complex interactions inside the antioxidant network of the cell/body to ensure an effective maintenance of homeostasis in stress conditions. Indeed, in many cases nutritional antioxidants (vitamin E, ascorbic acid, selenium) in the feed can decrease oxidative stress and as a result HSP expression could be decreased as well; g) regulating effects of various phytochemicals on HSP need further investigation; h) protective effects of HSP in immunity in stress conditions await practical applications in poultry production; i) nutritional means of additional HSP upregulation in stress conditions of poultry production and physiological and commercial consequences await investigation; j) vitagene upregulation in stress conditions is emerging as an effective means for stress management.
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References
Abdul, H. M., Calabrese, V., Calvani, M., & Butterfield, D. A. (2006). Acetyl-L-carnitine-induced up-regulation of heat shock proteins protects cortical neurons against amyloid-beta peptide 1-42-mediated oxidative stress and neurotoxicity: Implications for Alzheimer’s disease. Journal of Neuroscience Research, 84, 398–408.
Aggarwal, A., Ashutosh Chandra, G., & Singh, A. K. (2013). Heat shock protein 70, oxidative stress, and antioxidant status in periparturient crossbred cows supplemented with α-tocopherol acetate. Tropical Animal Health and Production, 45, 239–245.
Alirezaei, M., Khoshdel, Z., Dezfoulian, O., Rashidipour, M., & Taghadosi, V. (2015). Beneficial antioxidant properties of betaine against oxidative stress mediated by levodopa/benserazide in the brain of rats. The Journal of Physiological Sciences, 65, 243–252.
Al-Zghoul, M. B., Ismail, Z. B., Dalab, A. E., et al. (2015). Hsp90, Hsp60 and HSF-1 genes expression in muscle, heart and brain of thermally manipulated broiler chicken. Research in Veterinary Science, 99, 105–111.
Andrés, D., Alvarez, A. M., Díez-Fernández, C., Zaragoza, A., & Cascales, M. (2000). HSP70 induction by cyclosporine A in cultured rat hepatocytes: effect of vitamin E succinate. Journal of Hepatology, 33, 570–579.
Atkinson, B. G., Dean, R. L., & Blaker, T. W. (1986). Heat shock induced changes in the geneexpression of terminally differentiating avian red blood cells. Canadian Journal of Genetics and Cytology, 28, 1053–1063.
Aujame, L., & Firko, H. (1988). The major inducible heat shock protein hsp68 is not required for acquisition of thermal resistance in mouse plasmacytoma cell lines. Journal of Molecular Cell Biology, 8, 5486–5494.
Bag, J. (1983a). Regulation of heat-shock protein synthesis in chicken muscle culture during recovery from heat shock. European Journal of Biochemistry, 135, 373–378.
Bag, J. (1983b). Free messenger ribonucleoprotein complexes of chicken primary muscle cells following modification of protein synthesis by heat-shock treatment. European Journal of Biochemistry, 135, 187–196.
Bagatell, R., Paine-Murrieta, G. D., Taylor, C. W., et al. (2000). Induction of a heat shock factor 1-dependent stress response alters the cytotoxic activity of hsp90-binding agents. Clinical Cancer Research, 6, 3312–3318.
Banerji, S. S., Theodorakis, N. G., & Morimoto, R. I. (1984). Heat shock-induced translational control of HSP70 and globin synthesis in chicken reticulocytes. Journal of Molecular Cell Biology, 4, 2437–2448.
Banerji, S. S., Laing, K., & Morimoto, R. I. (1987). Erythroid lineage-specific expression and inducibility of the major heat shock protein HSP70 during avian embryogenesis. Genes, 1, 946–953.
Barbagallo, I., Galvano, F., Frigiola, A., et al. (2013). Potential therapeutic effects of natural heme oxygenase-1 inducers in cardiovascular diseases. Antioxid Redox Signal, 18, 507–521.
Barrott, J. J., & Haystead, T. A. (2013). Hsp90, an unlikely ally in the war on cancer. FEBS Journal, 280, 1381–1396.
Barve, A., Khor, T. O., Nair, S., et al. (2009). Gamma-tocopherol-enriched mixed tocopherol diet inhibits prostate carcinogenesis in TRAMP mice. International Journal of Cancer, 124, 1693–1699.
Bellezza, I., Tucci, A., Galli, F., et al. (2012). Inhibition of NF-κB nuclear translocation via HO-1 activation underlies α-tocopheryl succinate toxicity. The Journal of Nutritional Biochemistry, 23, 1583–1591.
Bhat, A., Gomis, S., Potter, A., & Tikoo, S. K. (2010). Role of Hsp90 in CpG ODN mediated immunostimulation in avian macrophages. Molecular Immunology, 47, 1337–1346.
Bilban, M., Haschemi, A., Wegiel, B., Chin, B. Y., Wagner, O., & Otterbein, L. E. (2008). Heme oxygenase and carbon monoxide initiate homeostatic signaling. Journal of Molecular Medicine (Berlin, Germany), 86, 267–279.
Binart, N., Chambraud, B., Dumas, B. et al. (1989) The cDNA-derived amino acid sequence of chick heat shock protein Mr 90,000 (HSP 90) reveals a "DNA like" structure: potential site of interaction with steroid receptors. Biochem. Biophysical Research Communications 159, 140–147.
Bissell, D. M., Hammaker, L., & Schmid, R. (1972). Liver sinusoidal cells Identification of a subpopulation for erythrocyte catabolism. The Journal of Cell Biology, 54, 107–119.
Bongiovanni, G. A., Soria, E. A., & Eynard, A. R. (2007). Effects of the plant flavonoids silymarin and quercetin on arsenite-induced oxidative stress in CHO-K1 cells. Food and Chemical Toxicology, 45, 971–976.
Bonkovsky, H. L., Healey, J. F., & Pohl, J. (1990). Purification and characterization of heme oxygenase from chick liver. Comparison of the avian and mammalian enzymes. European Journal of Biochemistry, 189, 155–166.
Bouhouche-Chatelier, L., Chadli, A., & Catelli, M. G. (2001). The N-terminal adenosine triphosphate binding domain of Hsp90 is necessary and sufficient for interaction with estrogen receptor. Cell Stress Chaperones, 6, 297–305.
Bozaykut, P., Ozer, N. K., & Karademir, B. (2014). Regulation of protein turnover by heat shock proteins. Free Radical Biology & Medicine, 77, 195–209.
Cable, E., Greene, Y., Healey, J., Evans, C. O., & Bonkovsky, H. (1990). Mechanism of synergistic induction of hepatic heme oxygenase by glutethimide and iron: studies in cultured chick embryo liver cells. Biochem. Biophysical Research Communications, 168, 176–181.
Cable, E. E., Cable, J. W., & Bonkovsky, H. L. (1993). Repression of hepatic delta-aminolevulinate synthase by heme and metalloporphyrins: relationship to inhibition of heme oxygenase. Hepatology, 18, 119–127.
Calabrese, V., Ravagna, A., Colombrita, C., et al. (2005). Acetylcarnitine induces heme oxygenase in rat astrocytes and protects against oxidative stress: Involvement of the transcription factor Nrf2. Journal of Neuroscience Research, 79, 509–521.
Calabrese, V., Cornelius, C., Dinkova-Kostova, A. T., et al. (2011). Cellular stress responses, hermetic phytochemicals and vitagenes in aging and longevity. Biochimica et Biophysica Acta, 1822, 753–783.
Calabrese, E. J., Dhawan, G., Kapoor, R., Iavicoli, I., & Calabrese, V. (2015a). What is hormesis and its relevance to healthy aging and longevity? Biogerontology, 16, 693–707.
Calabrese, V., Dattilo, S., Petralia, A., et al. (2015b). Analytical approaches to the diagnosis and treatment of aging and aging-related disease: Redox status and proteomics. Free Radical Research, 49, 511–524.
Calò, L. A., Pagnin, E., Davis, P. A., et al. (2006). Antioxidant effect of L-carnitine and its short chain esters: Relevance for the protection from oxidative stress related cardiovascular damage. International Journal of Cardiology, 107, 54–60.
Calò, L. A., Davis, P. A., Pagnin, E., et al. (2008). Carnitine-mediated improved response to erythropoietin involves induction of haem oxygenase-1: Studies in humans and in an animal model. Nephrology Dialysis Transplantation, 23, 890–895.
Cao, Y., Li, X., Wang, C. J., et al. (2015). Role of NF-E2-relatedfactor 2 in neuroprotective effect of l-carnitine against high glucose-induced oxidative stress in the retinal ganglion cells. Biomedicine & Pharmacotherapy, 69, 345–348.
Catelli, M. G., Binart, N., Feramisco, J. R., & Helfman, D. M. (1985a). Cloning of the chick hsp 90 cDNA in expression vector. Nucleic Acids Research, 13, 6035–6047.
Catelli, M. G., Binart, N., Jung-Testas, I., et al. (1985b). The common 90-kd protein component of non-transformed ‘8S’ steroid receptors is a heat-shock protein. The EMBO Journal, 4, 3131–3135.
Cerný, D., Canová, N. K., Martínek, J., et al. (2009). Effects of resveratrol pretreatment on tert-butylhydroperoxide induced hepatocyte toxicity in immobilized perifused hepatocytes: Involvement of inducible nitric oxide synthase and hemoxygenase-1. Nitric Oxide, 20, 1–8.
Chakraborthy, A., Ramani, P., Sherlin, H. J., Premkumar, P., & Natesan, A. (2014). Antioxidant and pro-oxidant activity of Vitamin C in oral environment. Indian Journal of Dental Research, 25, 499–504.
Chang, A. Y., Chan, J. Y., Cheng, H.-L., Tsai, C.-Y., & Chan, S. H. (2009). Hypoxia-inducible factor 1/heme oxygenase 1 cascade as upstream signals in the prolife role of heat shock protein 70 at rostral ventrolateral medulla during experimental brain stem death. Shock, 32, 651–658.
Chauveau, C., Remy, S., Royer, P. J., et al. (2005). Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood, 106, 1694–1702.
Chen, X., Zhu, Y. H., Cheng, X. Y., Zhang, Z. W., & Xu, S. W. (2012). The protection of selenium against cadmium-induced cytotoxicity via the heat shock protein pathway in chicken splenic lymphocytes. Molecules, 17, 14565–14572.
Chen, X., Yao, H., Yao, L., et al. (2014). Selenium deficiency influences the gene expressions of heat shock proteins and nitric oxide levels in neutrophils of broilers. Biological Trace Element Research, 161, 334–340.
Chiosis, G., Vilenchik, M., Kim, J., & Solit, D. (2004). Hsp90: The vulnerable chaperone. Drug Discovery Today, 9, 881–888.
Choi, K. M., Kashyap, P. C., Dutta, N., et al. (2010). CD206-positive M2 macrophages that express heme oxygenase-1 protect against diabetic gastroparesis in mice. Gastroenterology, 138, 2399–2409.
Choi, M. K., Han, J. M., Kim, H. G., et al. (2013). Aqueous extract of Artemisia capillaries exerts hepatoprotective action in alcohol-pyrazole-fed rat model. Journal of Ethnopharmacology, 147, 662–670.
Clerico, E. M., Tilitsky, J. M., Meng, W., & Gierasch, L. M. (2015). How hsp70 molecular machines interact with their substrates to mediate diverse physiological functions. Journal of Molecular Biology, 427, 1575–1588.
Collier, N. C., & Schlesinger, M. J. (1986a). Induction of heat-shock proteins in the embryonic chicken lens. Experimental Eye Research, 43, 103–117.
Collier, N. C., & Schlesinger, M. J. (1986b). The dynamic state of heat shock proteins in chicken embryo fibroblasts. The Journal of Cell Biology, 103, 1495–1507.
Collin, A., Picard, M., & Yahav, S. (2005). The effect of duration of thermal manipulation during chick’s embryogenesis on body weight and body temperature of post hatched chicks. Animal Research, 54, 105–112.
Collin, A., Berri, C., Tesseraud, S., et al. (2007). Effects of thermal manipulation during early and late embryogenesis on thermotolerance and breast muscle characteristics in broiler chickens. Poultry Science, 86, 795–800.
Csermely, P., Schnaider, T., Soti, C., Prohászka, Z., & Nardai, G. (1998). The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacology & Therapeutics, 79, 129–168.
Czar, M. J., Welsh, M. J., & Pratt, W. B. (1996). Immunofluorescence localization of the 90-kDa heat-shock protein to cytoskeleton. European Journal of Cell Biology, 70, 322–330.
Dangi, S. S., Gupta, M., Dangi, S. K., et al. (2015). Expression of HSPs: An adaptive mechanism during long-term heat stress in goats (Capra hircus). International Journal of Biometeorology, 59, 1095–1106.
Daniel, S., Bradley, G., Longshaw, V. M., et al. (2008). Nuclear translocation of the phosphoprotein Hop (Hsp70/Hsp90 organizing protein) occurs under heat shock, and its proposed nuclear localization signal is involved in Hsp90 binding. Biochimica et Biophysica Acta, 1783, 1003–1014.
Das, S., Pan, D., Bera, A. K., et al. (2010). Stress inducible heat shock protein 70: A potent molecular and toxicological signature in arsenic exposed broiler chickens. Molecular Biology Reports, 37, 3151–3155.
Dash, A., Chung, S., & Zelenka, P. S. (1994). Expression of HSP70 mRNA in the embryonic chicken lens: Association with differentiation. Experimental Eye Research, 58, 381–387.
Daugaard, M., Rohde, M., & Jäättelä, M. (2007). The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Letters, 581, 3702–3710.
De Backer, O., Elinck, E., Blanckaert, B., Leybaert, L., Motterlini, R., & Lefebvre, R. A. (2009). Water-soluble CO-releasing molecules Hemeoxygenase-1 in gastrointestinal diseases reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress. Gut, 58, 347–356.
de Roos, B., & Duthie, G. G. (2015). Role of dietary pro-oxidants in the maintenance of health and resilience to oxidative stress. Molecular Nutrition & Food Research, 59, 1229–1248.
de Thonel, A., Le Mouël, A., & Mezger, V. (2012). Transcriptional regulation of small HSP-HSF1 and beyond. The International Journal of Biochemistry & Cell Biology, 44, 1593–1612.
Decuypere, E. (1984). Incubation temperature in relation to postnatal performance in chickens. Archiv Fur Experimentelle Veterinarmedizin, 38, 439–449.
Demir, M., Amanvermez, R., Kamalı Polat, A., et al. (2014). The effect of silymarin on mesenteric ischemia-reperfusion injury. Medical Principles and Practice, 23, 140–144.
Dennery, P. A. (2000). Regulation and role of heme oxygenase in oxidative injury. Current Topics in Cellular Regulation, 36, 181–199.
Druyan, S., Cahaner, A., & Ashwell, C. M. (2007). The expression patterns of hypoxia-inducing factor subunit alpha-1, heme oxygenase, hypoxia upregulated protein 1, and cardiac troponin T during development of the chicken heart. Poultry Science, 86, 2384–2389.
Duncan, E. J., Cheetham, M. E., Chapple, J. P., & van der Spuy, J. (2015). The role of HSP70 and its co-chaperones in protein misfolding, aggregation and disease. Subcellular Biochemistry, 78, 243–273.
Durante, W. (2010). Targeting heme oxygenase-1 in vascular disease. Current Drug Targets, 11, 1504–1516.
Ebrahimi, R., Faseleh Jahromi, M., Liang, J. B., Soleimani Farjam, A., Shokryazdan, P., & Idrus, Z. (2015). Effect of dietary lead on intestinal nutrient transporters mRNA expression in broiler chickens. BioMed Research International, 149745. https://doi.org/10.1155/2015/149745.
Edens, F. W., Hill, C. H., & Wang, S. (1992). Heat shock protein response in phosphorus-deficient heat-stressed broiler chickens. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 103, 827–831.
El Golli, E., Hassen, W., Bouslimi, A., Bouaziz, C., Ladjimi, M. M., & Bacha, H. (2006). Induction of Hsp 70 in Vero cells in response to mycotoxins cytoprotection by sub-lethal heat shock and by Vitamin E. Toxicol Letters, 166, 122–130.
Elbirt, K. K., Whitmarsh, A. J., Davis, R., & Bonkovsky, H. L. (1998). Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogen-activated protein kinases. The Journal of Biological Chemistry, 273, 8922–8931.
Erlejman, A. G., Lagadari, M., Toneatto, J., Piwien-Pilipuk, G., & Galigniana, M. D. (2014). Regulatory role of the 90-kDa-heat-shock protein (Hsp90) and associated factors on gene expression. Biochimica et Biophysica Acta, 1839, 71–87.
Evans, C. O., Healey, J. F., Greene, Y., & Bonkovsky, H. L. (1991). Cloning, sequencing and expression of cDNA for chick liver haem oxygenase. Comparison of avian and mammalian cDNAs and deduced proteins. The Biochemical Journal, 273, 659–666.
Felver-Gant, J. N., Mack, L. A., Dennis, R. L., Eicher, S. D., & Cheng, H. W. (2012). Genetic variations alter physiological responses following heat stress in 2 strains of laying hens. Poultry Science, 91, 1542–1551.
Feng, Z., Liu, Z., Li, X., et al. (2010). α-Tocopherol is an effective Phase II enzyme inducer: protective effects on acrolein-induced oxidative stress and mitochondrial dysfunction in human retinal pigment epithelial cells. The Journal of Nutritional Biochemistry, 21, 1222–1231.
Fernandez, M., & Bonkovsky, H. L. (2003). Vascular endothelial growth factor increases heme oxygenase-1 protein expression in the chick embryo chorioallantoic membrane. British Journal of Pharmacology, 139, 634–640.
Figueiredo, D., Gertler, A., Cabello, G., Decuypere, E., Buyse, J., & Dridi, S. (2007). Leptin downregulates heat shock protein-70 (HSP-70) gene expression in chicken liver and hypothalamus. Cell and Tissue Research, 329, 91–101.
Fischer, C. P., Hiscock, N. J., Basu, S., et al. (2006). Vitamin E isoform-specific inhibition of the exercise-induced heat shock protein 72 expression in humans. Journal of Applied Physiology, 100, 1679–1687.
Fotina, A., Fotina, T.I. and Surai, P.F. (2014). Effect of a water-soluble antistress composition on broiler chickens”. In Proceedings of the XIVth European Poultry Conference, Stavanger, Norway. p. 555.
Fredenburgh, L. E., Merz, A. A., & Cheng, S. (2015). Haeme oxygenase signalling pathway: Implications for cardiovascular disease. European Heart Journal, 36, 1512–1518.
Fujimoto, M., & Nakai, A. (2010). The heat shock factor family and adaptation to proteotoxic stress. The FEBS Journal, 277, 4112–4125.
Gabis, K. K., Gildemeister, O. S., Pepe, J. A., Lambrecht, R. W., & Bonkovsky, H. L. (1996). Induction of heme oxygenase-1 in LMH cells. Comparison of LMH cells to primary cultures of chick embryo liver cells. Biochimica et Biophysica Acta, 1290, 113–120.
Gabriel, J. E., Ferro, J. A., Stefani, R. M., Ferro, M. I., Gomes, S. L., & Macari, M. (1996). Effect of acute heat stress on heat shock protein 70 messenger RNA and on heat shock protein expression in the liver of broilers. British Poultry Science, 37, 443–449.
Gabriel, J. E., da Mota, A. F., Boleli, I. C., Macari, M., & Coutinho, L. L. (2002). Effect of moderate and severe heat stress on avian embryonic hsp70 gene expression. Growth, Development, and Aging, 66, 27–33.
Gan, F., Ren, F., Chen, X., et al. (2013a). Effects of selenium-enriched probiotics on heat shock protein mRNA levels in piglet under heat stress conditions. Journal of Agricultural and Food Chemistry, 61, 2385–2391.
Gan, J. K., Zhang, D. X., He, D. L., Zhang, X. Q., Chen, Z. Y., & Luo, Q. B. (2013b). Promoter methylation negatively correlated with mRNA expression but not tissue differential expression after heat stress. Genetics and Molecular Research, 12, 809–819.
Gan, J. K., Jiang, L. Y., Kong, L. N., Zhang, X. Q., & Luo, Q. B. (2015). Analysis of genetic diversity of the heat shock protein 70 gene on the basis of abundant sequence polymorphisms in chicken breeds. Genetics and Molecular Research, 14, 1538–1545.
Garcia-Carbonero, R., Carnero, A., & Paz-Ares, L. (2013). Inhibition of HSP90 molecular chaperones: Moving into the clinic. The Lancet Oncology, 14, e358–e369.
Garnier, C., Lafitte, D., Tsvetkov, P. O., et al. (2002). Binding of ATP to heat shock protein 90: Evidence for an ATP-binding site in the C-terminal domain. The Journal of Biological Chemistry, 277, 12208–12214.
Garrido, C., Gurbuxani, S., Ravagnan, L., & Kroemer, G. (2001). Heat shock proteins: Endogenous modulators of apoptotic cell death. Biochemical and Biophysical Research Communications, 286, 433–442.
Garrido, C., Brunet, M., Didelot, C., Zermati, Y., Schmitt, E., & Kroemer, G. (2006). Heat shock proteins 27 and 70: Anti-apoptotic proteins with tumorigenic properties. Cell Cycle, 5, 2592–2601.
Gaviol, H. C., Gasparino, E., Prioli, A. J., & Soares, M. A. (2008). Genetic evaluation of the HSP70 protein in the Japanese quail (Coturnix japonica). Genetics and Molecular Research, 7, 133–139.
George, J. F., Braun, A., Brusko, T. M., et al. (2008). Suppression by CD4+CD25+ regulatory t cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells. The American Journal of Pathology, 173, 154–160.
Gildemeister, O. S., Pepe, J. A., Lambrecht, R. W., & Bonkovsky, H. L. (2001). Induction of heme oxygenase-1 by phenylarsine oxide. Studies in cultured primary liver cells. Journal of Molecular Cell Biology, 226, 17–26.
Givisiez, P. E., Ferro, J. A., Ferro, M. I., Kronka, S. N., Decuypere, E., & Macari, M. (1999). Hepatic concentration of heat shock protein 70 kD (Hsp70) in broilers subjected to different thermal treatments. British Poultry Science, 40, 292–296.
Green, M., Schuetz, T. J., Sullivan, E. K., & Kingston, R. E. (1995). A heat shock-responsive domain of human HSF1 that regulates transcription activation domain function. Journal of Molecular Cell Biology, 15, 3354–3362.
Greene, Y. J., Healey, J. F., & Bonkovsky, H. L. (1991). Immunochemical studies of haem oxygenase. Preparation and characterization of antibodies to chick liver haem oxygenase and their use in detecting and quantifying amounts of haem oxygenase protein. The Biochemical Journal, 279, 849–854.
Grenert, J. P., Johnson, B. D., & Toft, D. O. (1999). The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes. The Biochemical Journal, 274, 17525–17533.
Gu, X. H., Hao, Y., & Wang, X. L. (2012). Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 2. Intestinal oxidative stress. Poultry Science, 91, 790–799.
Guerriero, V., Jr., & Raynes, D. A. (1990). Synthesis of heat stress proteins in lymphocytes from livestock. Journal of Animal Sciences, 68, 2779–2883.
Guo, Y., Zhao, P., Guo, G., et al. (2016). Effects of arsenic trioxide exposure on heat shock protein response in the immune organs of chickens. Biological Trace Element Research, 169, 134–141.
Gupta, S. C., Sharma, A., Mishra, M., Mishra, R. K., & Chowdhuri, D. K. (2010). Heat shock proteins in toxicology: how close and how far? Life Sciences, 86, 377–384.
Haines, D. D., Lekli, I., Teissier, P., Bak, I., & Tosaki, A. (2012). Role of haeme oxygenase-1 in resolution of oxidative stress-related pathologies: Focus on cardiovascular, lung, neurological and kidney disorders. Acta Physiologica (Oxford, England), 204, 487–501.
Hao, Y., & Gu, X. H. (2014). Effects of heat shock protein 90 expression on pectoralis major oxidation in broilers exposed to acute heat stress. Poultry Science, 93, 2709–2717.
Hao, Y., Gu, X. H., & Wang, X. L. (2012). Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 1. Intestinal structure and digestive function. Poultry Science, 91, 781–789.
Henstridge, D. C., Whitham, M., & Febbraio, M. A. (2014). Chaperoning to the metabolic party: The emerging therapeutic role of heat-shock proteins in obesity and type 2 diabetes. Molecular Metabolism, 3, 781–793.
Herring, G., & Gawlik, D. E. (2007). The role of stress proteins in the study of allostatic overload in birds: Use and applicability to current studies in avian ecology. ScientificWorld Journal, 28, 1596–1602.
Holley, S. J., & Yamamoto, K. R. (1995). A role for Hsp90 in retinoid receptor signal transduction. Molecular Biology of the Cell, 6, 1833–1842.
Hong, D. S., Banerji, U., Tavana, B., George, G. C., Aaron, J., & Kurzrock, R. (2013). Targeting the molecular chaperone heat shock protein 90 (HSP90): Lessons learned and future directions. Cancer Treatment Reviews, 39, 375–387.
Horowitz, M. (2014). Heat acclimation, epigenetics, and cytoprotection memory. Comprehensive Physiology, 4, 199–230.
Iannotti, A. M., Rabideau, D. A., & Dougherty, J. J. (1988). Characterization of purified avian 90,000-Da heat shock protein. Archives of Biochemistry and Biophysics, 264, 54–60.
Igarashi, K., & Sun, J. (2006). The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxidants & Redox Signaling, 8, 107–118.
Immenschuh, S., Tan, M., & Ramadori, G. (1999). Nitric oxide mediates the lipopolysaccharide dependent upregulation of the heme oxygenase-1 gene expression in cultured rat Kupffer cells. Journal of Hepatology, 30, 61–69.
Inouye, S., Katsuki, K., Izu, H., et al. (2003). Activation of heat shock genes is not necessary for protection by heat shock transcription factor 1 against cell death due to a single exposure to high temperatures. Journal of Molecular Cell Biology, 23, 5882–5895.
Jackson, S. E. (2013). Hsp90: Structure and function. Topics in Current Chemistry, 328, 155–240.
Jacobs, J. M., Marek, D., Walton, H. S., Sinclair, P. R., & Sinclair, J. F. (1999). Effect of sodium arsenite on heme metabolism in cultured chick embryo hepatocytes. Archives of Biochemistry and Biophysics, 371, 8–14.
Jang, J. S., Piao, S., Cha, Y.-N., & Kim, C. (2009). Taurine chloramine activates Nrf2, increases HO-1 expression and protects cells from death caused by hydrogen peroxide. Journal of Clinical Biochemistry and Nutrition, 45, 37–43.
Janisch, S., Sharifi, A. R., Wicke, M., & Krischek, C. (2015). Changing the incubation temperature during embryonic myogenesis influences the weight performance and meat quality of male and female broilers. Poultry Science, 94, 2581–2588.
Jérôme, V., Léger, J., Devin, J., Baulieu, E. E., & Catelli, M. G. (1991). Growth factors acting via tyrosine kinase receptors induce HSP90 alpha gene expression. Growth Factors, 4, 317–327.
Jérôme, V., Vourch, C., Baulieu, E. E., & Catelli, M. G. (1993). Cell cycle regulation of the chicken hsp90 alpha expression. Experimental Cell Research, 205, 44–51.
Ji, Y. L., Wang, Z., Wang, H., et al. (2012). Ascorbic acid protects against cadmium-induced endoplasmic reticulum stress and germ cell apoptosis in testes. Reproductive Toxicology, 34, 357–363.
Johnson, B. D., Chadli, A., Felts, S. J., Bouhouche, I., Catelli, M. G., & Toft, D. O. (2000). Hsp90 chaperone activity requires the full-length protein and interaction among its multiple domains. The Journal of Biological Chemistry, 275, 32499–32507.
Kalmar, B., & Greensmith, L. (2009). Induction of heat shock proteins for protection against oxidative stress. Advanced Drug Delivery Reviews, 61, 310–318.
Kamanli, S., Durmuş, I., Yalçın, S., Yıldırım, U., & Meral, Ö. (2015). Effect of prenatal temperature conditioning of laying hen embryos: Hatching, live performance and response to heat and cold stress during laying period. Journal of Theoretical Biology, 51, 96–104.
Kantidze, O. L., Velichko, A. K., & Razin, S. V. (2015). Heat stress-induced transcriptional repression. Biochemistry (Moscow), 80, 990–993.
Kapturczak, M. H., Wasserfall, C., Brusko, T., et al. (2004). Campbell-Thompson M, Ellis TM, Atkinson MA and Agarwal A. Heme oxygenase-1 modulates early inflammatory responses: Evidence from the heme oxygenase-1-deficient mouse. The American Journal of Pathology, 165, 1045–1053.
Karagöz, G. E., & Rüdiger, S. G. (2015). Hsp90 interaction with clients. Trends in Biochemical Sciences, 40, 117–125.
Kaur, P., & Bansal, M. P. (2003). Effect of oxidative stress on the spermatogenic process and hsp70 expressions in mice testes. Indian Journal of Biochemistry & Biophysics, 40, 246–251.
Kaushal, N., & Bansal, M. P. (2009). Diminished reproductive potential of male mice in response to selenium-induced oxidative stress: Involvement of HSP70, HSP70-2, and MSJ-1. Journal of Biochemical and Molecular Toxicology, 23, 125–136.
Kawazoe, Y., Tanabe, M., Sasai, N., Nagata, K., & Nakai, A. (1999). HSF3 is a major heat shock responsive factor during chicken embryonic development. European Journal of Biochemistry, 265, 688–697.
Kelley, P. M., & Schlesinger, M. J. (1978). The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell, 15, 1277–1286.
Kelley, P. M., & Schlesinger, M. J. (1982). Antibodies to two major chicken heat shock proteins cross-react with similar proteins in widely divergent species. Molecular and Cellular Biochemistry, 2, 267–274.
Kennedy, D., Jäger, R., Mosser, D. D., & Samali, A. (2014). Regulation of apoptosis by heat shock proteins. IUBMB Life, 66, 327–338.
Khalil, A. A., Kabapy, N. F., Deraz, S. F., & Smith, C. (2011). Heat shock proteins in oncology: Diagnostic biomarkers or therapeutic targets? Biochimica et Biophysica Acta, 1816, 89–104.
Khassaf, M., McArdle, A., Esanu, C., et al. (2003). Effect of vitamin C supplements on antioxidant defence and stress proteins in human lymphocytes and skeletal muscle. Journal of Physiology, 549, 645–652.
Khoso, P. A., Yang, Z., Liu, C., & Li, S. (2015). Selenoproteins and heat shock proteins play important roles in immunosuppression in the bursa of Fabricius of chickens with selenium deficiency. Cell Stress Chaperones, 20, 967–978.
Khurana, N., & Bhattacharyya, S. (2015). Hsp90, the concertmaster: Tuning transcription. Frontiers in Oncology, 5, 100.
Kim, H. R., Kang, K. I., Kang, H. S., & Kim, H. D. (1999). Identification of heat shock protein 90-associated 84-kDa phosphoprotein. Journal of Biochemistry, 126, 1025–1032.
Kiruthiga, P. V., Karthikeyan, K., Archunan, G., Karutha Pandian, S., & Pandima Devi, K. (2015). Silymarin prevents benzo(a)pyrene-induced toxicity in Wistar rats by modulating xenobiotic-metabolizing enzymes. Toxicology and Industrial Health, 31, 523–541.
Krischek, C., Kuembet, U., Wicke, M., & Gerken, M. (2013). A higher incubation temperature between embryonic day 3 and 6 influences growth and meat quality characteristics of broiler after hatch. European Poultry Science, 77, 59–65.
Kutuzova, G. D., & DeLuca, H. F. (2007). 1,25-Dihydroxyvitamin D3 regulates genes responsible for detoxification in intestine. Toxicology and Applied Pharmacology, 218, 37–44.
Leandro, N. S., Gonzales, E., Ferro, J. A., Ferro, M. I., Givisiez, P. E., & Macari, M. (2004). Expression of heat shock protein in broiler embryo tissues after acute cold or heat stress. Molecular Reproduction and Development, 67, 172–177.
Lee, T.-S., & Chau, L.-Y. (2002). Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nature Medicine, 8, 240–246.
Lei, L., Yu, J., & Bao, E. (2009). Expression of heat shock protein 90 (Hsp90) and transcription of its corresponding mRNA in broilers exposed to high temperature. British Poultry Science, 50, 504–511.
Li, J., Sun, L., Xu, C., et al. (2012a). Structure insights into mechanisms of ATP hydrolysis and the activation of human heat-shock protein 90. Acta Biochimica et Biophysica Sinica, 44, 300–306.
Li, J., Soroka, J., & Buchner, J. (2012b). The Hsp90 chaperone machinery: Conformational dynamics and regulation by co-chaperones. Biochimica et Biophysica Acta, 1823, 624–635.
Li, C., Guo, S., Zhang, M., Gao, J., & Guo, Y. (2015). DNA methylation and histone modification patterns during the late embryonic and early postnatal development of chickens. Poultry Science, 94, 706–721.
Liew, P. K., Zulkifli, I., Hair-Bejo, M., Omar, A. R., & Israf, D. A. (2003). Effects of early age feed restriction and heat conditioning on heat shock protein 70 expression, resistance to infectious bursal disease, and growth in male broiler chickens subjected to heat stress. Poultry Science, 82, 1879–1885.
Lincoln, B. C., Healey, J. F., & Bonkovsky, H. L. (1988). Regulation of hepatic haem metabolism. Disparate mechanisms of induction of haem oxygenase by drugs and metals. Biochemical Journal, 250, 189–196.
Lincoln, B. C., Aw, T. Y., & Bonkovsky, H. L. (1989). Heme catabolism in cultured hepatocytes: Evidence that heme oxygenase is the predominant pathway and that a proportion of synthesized heme is converted rapidly to biliverdin. Biochimica et Biophysica Acta, 992, 49–58.
Liu, Y., & Chang, A. (2008). Heat shock response relieves ER stress. EMBO Journal, 27, 1049–1059.
Liu, X., Wei, J., Peng, D. H., Layne, M. D., & Yet, S. F. (2005). Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes, 54, 778–784.
Liu, L. L., He, J. H., Xie, H. B., Yang, Y. S., Li, J. C., & Zou, Y. (2014). Resveratrol induces antioxidant and heat shock protein mRNA expression in response to heat stress in black-boned chickens. Poultry Science, 93, 54–62.
Liu, C. P., Fu, J., Xu, F. P., Wang, X. S., & Li, S. (2015a). The role of heat shock proteins in oxidative stress damage induced by Se deficiency in chicken livers. Biometals, 28, 163–173.
Liu, H., Liu, J., Yan, X., et al. (2015b). Impact of thermal stress during incubation on gene expression in embryonic muscle of Peking Ducks (Anasplatyrhynchos domestica). Journal of Thermal Biology, 53, 80–89.
Lordnejad, M. R., Schliess, F., Wettstein, M., & Häussinger, D. (2001). Modulation of the hemeoxygenase HO-1 expression by hyperosmolarity and betaine in primary rat hepatocytes. Archives of Biochemistry and Biophysics, 388, 285–292.
Lourens, A., van den Brand, H., Meijerhof, R., & Kemp, B. (2005). Effect of eggshell temperature during incubation on embryo development, hatchability, and posthatch development. Poultry Science, 84, 914–920.
Loyau, T., Berri, C., & Bedrani, L. (2013). Thermal manipulation of the embryo modifies the physiology and body composition of broiler chickens reared in floor pens without affecting breast meat processing quality. Journal of Animal Science, 91, 3674–3685.
Loyau, T., Bedrani, L., Berri, C., et al. (2015). Cyclic variations in incubation conditions induce adaptive responses to later heat exposure in chickens: A review. Animal, 9, 76–85.
Lu, T. H., Pepe, J. A., Gildemeister, O. S., Tyrrell, R. M., & Bonkovsky, H. L. (1997). Regulation of expression of the human heme oxygenase-1 gene in transfected chick embryo liver cell cultures. Biochimica et Biophysica Acta, 1352, 293–302.
Lu, T. H., Lambrecht, R. W., Pepe, J., Shan, Y., Kim, T., & Bonkovsky, H. L. (1998). Molecular cloning, characterization, and expression of the chicken heme oxygenase-1 gene in transfected primary cultures of chick embryo liver cells. Gene, 207, 177–186.
Lu, T. H., Shan, Y., Pepe, J., Lambrecht, R. W., & Bonkovsky, H. L. (2000). Upstream regulatory elements in chick heme oxygenase-1 promoter: A study in primary cultures of chick embryo liver cells. Molecular and Cellular Biochemistry, 209, 17–27.
Luo, Q. B., Song, X. Y., Ji, C. L., Zhang, X. Q., & Zhang, D. X. (2014). Exploring the molecular mechanism of acute heat stress exposure in broiler chickens using gene expression profiling. Gene, 546, 200–205.
Maak, S., Melesse, A., Schmidt, R., Schneider, F., & Von Lengerken, G. (2003). Effect of long-term heat exposure on peripheral concentrations of heat shock protein 70 (Hsp70) and hormones in laying hens with different genotypes. British Poultry Science, 44, 133–138.
Mahalka, A. K., Kirkegaard, T., Jukola, L. T., Jäättelä, M., & Kinnunen, P. K. (2014). Human heat shock protein 70 (Hsp70) as a peripheral membrane protein. Biochimica et Biophysica Acta, 1838, 1344–1361.
Mahmoud, K. Z., & Edens, F. W. (2003). Influence of selenium sources on age-related and mild heat stress-related changes of blood and liver glutathione redox cycle in broiler chickens (Gallus domesticus). Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 136, 921–934.
Mahmoud, K. Z., & Edens, F. W. (2005). Influence of organic selenium on hsp70 response of heat-stressed and enteropathogenic Escherichia coli-challenged broiler chickens (Gallus gallus). Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 141, 69–75.
Mahmoud, K. Z., Edens, F. W., Eisen, E. J., & Havenstein, G. B. (2003). Effect of ascorbic acid and acute heat exposure on heat shock protein 70 expression by young white Leghorn chickens. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 136, 329–335.
Mahmoud, K. Z., Edens, F. W., Eisen, E. J., & Havenstein, G. B. (2004a). The effect of dietary phosphorus on heat shock protein mRNAs during acute heat stress in male broiler chickens (Gallus gallus). Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 137, 11–18.
Mahmoud, K. Z., Edens, F. W., Eisen, E. J., & Havenstein, G. B. (2004b). Ascorbic acid decreases heat shock protein 70 and plasma corticosterone response in broilers (Gallus gallus domesticus) subjected to cyclic heat. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 137, 35–42.
Maines, M. D., & Sinclair, P. (1977). Cobalt regulation of heme synthesis and degradation in avian embryo liver cell culture. The Journal of Biological Chemistry, 252, 219–223.
Marcu, M. G., Chadli, A., Bouhouche, I., Catelli, M., & Neckers, L. M. (2000). The heat shock protein 90 antagonist novobiocin interacts with a previously unrecognized ATP-binding domain in the carboxyl terminus of the chaperone. The Journal of Biological Chemistry, 275, 37181–37186.
Mattson, M. P., & Cheng, A. (2006). Neurohormetic phytochemicals: Low-dose toxins that induce adaptive neuronal stress responses. Trends in Neurosciences, 29, 632–639.
Mayer, M. P. (2013). Hsp70 chaperone dynamics and molecular mechanism. Trends in Biochemical Sciences, 38, 507–514.
Mayer, M. P., & Le Breton, L. (2015). Hsp90: breaking the symmetry. Molecular Cell, 58, 8–20.
Meijering, R. A., Henning, R. H., & Brundel, B. J. (2015). Reviving the protein quality control system: |Therapeutic target for cardiac disease in the elderly. Trends in Cardiovascular Medicine, 25, 243–247.
Meimaridou, E., Gooljar, S. B., & Chapple, J. P. (2009). From hatching to dispatching: the multiple cellular roles of the Hsp70 molecular chaperone machinery. Journal of Molecular Endocrinology, 42, 1–9.
Meng, X., Jérôme, V., Devin, J., Baulieu, E. E., & Catelli, M. G. (1993). Cloning of chicken hsp90 beta: The only vertebrate hsp90 insensitive to heat shock. Biochemical and Biophysical Research Communications, 190, 630–636.
Meng, X., Baulieu, E. E., & Catelli, M. G. (1995). Isolation of chicken hsp90 beta gene promoter. Biochemical and Biophysical Research Communications, 206, 644–651.
Mezquita, B., Mezquita, C., & Mezquita, J. (1998). Marked differences between avian and mammalian testicular cells in the heat shock induction and polyadenylation of Hsp70 and ubiquitin transcripts. FEBS Letters, 436, 382–386.
Miller, L., & Qureshi, M. A. (1992a). Heat-shock protein synthesis in chicken macrophages: Influence of and in vitro heat shock, lead acetate, and lipopolysaccharide. Poultry Science, 71, 988–998.
Miller, L., & Qureshi, M. A. (1992b). Comparison of heat-shock-induced and lipopolysaccharide-induced protein changes and tumoricidal activity in a chicken mononuclear cell line. Poultry Science, 71, 979–987.
Miller, L., & Qureshi, M. A. (1992c). Molecular changes associated with heat-shock treatment in avian mononuclear and lymphoid lineage cells. Poultry Science, 71, 473–481.
Miller, L., & Qureshi, M. A. (1992d). Induction of heat-shock proteins and phagocytic function of chicken macrophage following in vitro heat exposure. Veterinary Immunology and Immunopathology, 30, 179–191.
Minne, B., & Decuypere, E. (1984). Effects of late prenatal temperatures on some thermoregulatory aspects in young chickens. Archiv für Experimentelle Veterinärmedizin, 38, 374–383.
Moraes, V. M. B., Malheirosb, R. D., Bruggeman, V., et al. (2004). The effect of timing of thermal conditioning during incubation on embryo physiological parameters and its relationship to thermotolerance in adult broiler chickens. Journal of Thermal Biology, 29, 55–61.
Moreau, A., Hill, M., & Thebault, P. (2009). Tolerogenic dendritic cells actively inhibit T cells through heme oxygenase-1 in rodents and in nonhuman primates. FASEB Journal, 23, 3070–3077.
Morimoto, R., & Fodor, E. (1984). Cell-specific expression of heat shock proteins in chicken reticulocytes and lymphocytes. The Journal of Cell Biology, 99, 1316–1323.
Morimoto, R. I., Hunt, C., Huang, S. Y., Berg, K. L., & Banerji, S. S. (1986). Organization, nucleotide sequence, and transcription of the chicken HSP70 gene. The Journal of Biological Chemistry, 261, 12692–12699.
Morse, D., Lin, L., Choi, A. M., & Ryter, S. W. (2009). Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease. Free Radical Biology & Medicine, 47, 1–12.
Mueller, K., Blum, N. M., Kluge, H., & Mueller, A. S. (2012). Influence of broccoli extract and various essential oils on performance and expression of xenobiotic- and antioxidant enzymes in broiler chickens. British Journal of Nutrition, 108, 588–602.
Murakami, A. (2013). Modulation of protein quality control systems by food phytochemicals. Journal of Clinical Biochemistry and Nutrition, 52, 215–227.
Murakami, A. (2014). Dose-dependent functionality and toxicity of green tea polyphenols in experimental rodents. Archives of Biochemistry and Biophysics, 557, 3–10.
Muthumani, M., & Prabu, S. M. (2014). Silibinin potentially attenuates arsenic-induced oxidative stress mediated cardiotoxicity and dyslipidemia in rats. Cardiovascular Toxicology, 14, 83–97.
Nagahori, K., Iwamoto, S., Maruyama, A., et al. (2010). Basic characterization of 90 kDa heat shock protein genes HSP90AA1, HSP90AB1, HSP90B1 and TRAP1 expressed in Japanese quail (Coturnix japonica). Animal Science Journal, 81, 513–518.
Nakai, A., & Ishikawa, T. (2000). A nuclear localization signal is essential for stress-induced dimer-to-trimer transition of heat shock transcription factor 3. The Journal of Biological Chemistry, 275, 34665–34671.
Nakai, A., & Ishikawa, T. (2001). Cell cycle transition under stress conditions controlled by vertebrate heat shock factors. EMBO Journal, 20, 2885–2895.
Nakai, A., & Morimoto, R. I. (1993). Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway. Molecular and Cellular Biology, 13, 1983–1997.
Nakai, A., Kawazoe, Y., Tanabe, M., Nagata, K., & Morimoto, R. I. (1995). The DNA-binding properties of two heat shock factors, HSF1 and HSF3, are induced in the avian erythroblast cell line HD6. Molecular and Cellular Biology, 15, 5268–5278.
Nakamichi, I., Habtezion, A., Zhong, B., Contag, C. H., Butcher, E. C., & Omary, M. B. (2005). Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. The Journal of Clinical Investigation, 115, 3007–3014.
Ndisang, J. F. (2014). Cross-talk between heme oxygenase and peroxisome proliferator-activated receptors in the regulation of physiological functions. Frontiers in Bioscience (Landmark Ed.), 19, 916–935.
Niess, A. M., Passek, F., Lorenz, I., et al. (1999). Expression of the antioxidant stress protein heme oxygenase-1 (HO-1) in human leukocytes: acute and adaptational responses to endurance exercise. Free Radical Biology and Medicine, 26, 184–192.
O’Neill, S., Harrison, E. M., Ross, J. A., Wigmore, S. J., & Hughes, J. (2014). Heat-shock proteins and acute ischaemic kidney injury. Nephron Experimental Nephrology, 126, 167–174.
Oermann, E., Bidmon, H. J., Witte, O. W., & Zilles, K. (2004). Effects of 1alpha,25dihydroxyvitamin D3 on the expression of HO-1 and GFAP in glial cells of the photothrombotically lesioned cerebral cortex. Journal of Chemical Neuroanatomy, 28, 225–238.
Oksala, N. K., Ekmekçi, F. G., Ozsoy, E., et al. (2014). Natural thermal adaptation increases heat shock protein levels and decreases oxidative stress. Redox Biology, 3, 25–28.
Oommen, D., Giricz, Z., Srinivas, U. K., & Samali, A. (2013). Atypical heat shock response and acquisition of thermotolerance in P388D1 cells. Biochemical and Biophysical Research Communications, 430, 236–240.
Oskoueian, E., Abdullah, N., Idrus, Z., et al. (2014). Palm kernel cake extract exerts hepatoprotective activity in heat-induced oxidative stress in chicken hepatocytes. BMC Complementary and Alternative Medicine, 14, 368.
Owen, B. A., Sullivan, W. P., Felts, S. J., & Toft, D. O. (2002). Regulation of heat shock protein 90 ATPase activity by sequences in the carboxyl terminus. The Journal of Biological Chemistry, 277, 7086–7091.
Pae, H. O., & Chung, H. T. (2009). Heme oxygenase-1: Its therapeutic roles in inflammatory diseases. Immune Network, 9, 12–19.
Passinen, S., Valkila, J., Manninen, T., Syvälä, H., & Ylikomi, T. (2001). The C-terminal half of Hsp90 is responsible for its cytoplasmic localization. European Journal of Biochemistry, 268, 5337–5342.
Pekki, A. K. (1991). Different immunoelectron microscopic locations of progesterone receptor and HSP90 in chick oviduct epithelial cells. Journal of Histochemistry & Cytochemistry, 39, 1095–1101.
Peng, Y. Z., Wang, Y. W., Ning, D., & Guo, Y. M. (2013). Changes of haematic parameters, redox status and mitochondrial complex activity in the heart and liver of broilers fed with different density diets under low ambient temperature. Avian Pathology, 42, 327–334.
Piestun, Y., Shinder, D., Ruzal, M., Halevy, O., Brake, J., & Yahav, S. (2008). Thermal manipulations during broiler embryogenesis: Effect on the acquisition of thermotolerance. Poultry Science, 87, 1516–1525.
Piestun, Y., Harel, M., Barak, M., Yahav, S., & Halevy, O. (2009). Thermal manipulations in late-term chick embryos have immediate and longer term effects on myoblast proliferation and skeletal muscle hypertrophy. Journal of Applied Physiology, 106, 233–240.
Piestun, Y., Druyan, S., Brake, J., & Yahav, S. (2013). Thermal manipulations during broiler incubation alter performance of broilers to 70 days of age. Poultry Science, 92, 1155–1163.
Piestun, Y., Zimmerman, I., & Yahav, S. (2015a). Thermal manipulations of turkey embryos: The effect on thermoregulation and development during embryogenesis. Poultry Science, 94, 273–280.
Piestun, Y., Yahav, S., & Halevy, O. (2015b). Thermal manipulation during embryogenesis affects myoblast proliferation and skeletal muscle growth in meat-type chickens. Poultry Science, 94, 2528–2536.
Pockley, A.G. and Multhoff, G. (2008). Cell stress proteins in extracellular fluids: Friend or foe? Novartis Foundation Symposium 291, 86–95.
Poss, K. D., & Tonegawa, S. (1997). Reduced stress defense in heme oxygenase 1-deficient cells. Proceedings of the National Academy of Sciences of the United States of America, 94, 10925–10930.
Prakasam, R., Fujimoto, M., Takii, R., et al. (2013). Chicken IL-6 is a heat-shock gene. FEBS Letters, 587, 3541–3547.
Prasad, A. R., & Datta, K. (1984). Altered regulation of hepatic heme metabolism in cadmium exposed chick embryo. Biochemistry International, 8, 289–298.
Pratt, W. B., Morishima, Y., Peng, H. M., & Osawa, Y. (2010). Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Experimental Biology and Medicine (Maywood), 235, 278–289.
Qu, B., Jia, Y., Liu, Y., Wang, H., Ren, G., & Wang, H. (2015). The detection and role of heat shock protein 70 in various nondisease conditions and disease conditions: A literature review. Cell Stress & Chaperones, 20, 885–892.
Radanyi, C., Renoir, J. M., Sabbah, M., & Baulieu, E. E. (1989). Chick heat-shock protein of Mr =90,000, free or released from progesterone receptor, is in a dimeric form. The Journal of Biological Chemistry, 264, 2568–2573.
Rajkumar, U., Vinoth, A., Shanmugam, M., Rajaravindra, K. S., & Rama Rao, S. V. (2015). Effect of Embryonic Thermal Exposure on Heat Shock Proteins (HSPs) Gene Expression and Serum T3 Concentration in Two Broiler Populations. Animal Biotechnology, 26, 260–267.
Ravagnan, L., Gurbuxani, S., Susin, S. A., et al. (2001). Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nature Cell Biology, 3, 839–843.
Reed, D. K., Hall, S., & Arany, I. (2015). α-Tocopherol protects renal cells from nicotine- or oleic acid-provoked oxidative stress via inducing heme oxygenase-1. Journal of Physiology and Biochemistry, 71, 1–7.
Remy, S., Blancou, P., & Tesson, L. (2009). Carbon monoxide inhibits TLR-induced dendritic cell immunogenicity. The Journal of Immunology, 182, 1877–1884.
Revathi, B., & Prashanth, K. (2015). Potential Hsp90 Inhibitors: A novel target for cancer therapy. Chemotherapy, 4, 146.
Richter, K., Haslbeck, M., & Buchner, J. (2010). The heat shock response: Life on the verge of death. Molecular Cell, 40, 253–266.
Ritossa, F. (1962). A new puffing pattern induced by temperature shock and DNP in drosophila. Cellular and Molecular Life Sciences, 18, 571–573.
Rivera, R. E., Christensen, V. L., Edens, F. W., & Wineland, M. J. (2005). Influence of selenium on heat shock protein 70 expression in heat stressed turkey embryos (Meleagris gallopavo). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 427–432.
Roth, C. L., Elfers, C. T., Figlewicz, D. P., et al. (2012). Vitamin D deficiency in obese rats exacerbates NAFLD and increases hepatic resistin and toll-like receptor activation. Hepatology, 55, 1103–1111.
Ryter, S. W., & Choi, A. M. (2016). Targeting heme oxygenase-1 and carbon monoxide for therapeutic modulation of inflammation. Translational Research, 167, 7–34.
Sahin, N., Tuzcu, M., Orhan, C., Onderci, M., Eroksuz, Y., & Sahin, K. (2009). The effects of vitamin C and E supplementation on heat shock protein 70 response of ovary and brain in heat-stressed quail. British Poultry Science, 50, 259–265.
Sakurai, H., & Enoki, Y. (2010). Novel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression. FEBS Journals, 277, 4140–4149.
Salinas, M., Wang, J., Rosa de Sagarra, M., et al. (2004). Protein kinase Akt/PKB phosphorylates heme oxygenase-1 in vitro and in vivo. FEBS Letters, 578, 90–94.
Sánchez-Moreno, C., Paniagua, M., Madrid, A., & Martín, A. (2003). Protective effect of vitamin C against the ethanol mediated toxic effects on human brain glial cells. The Journal of Nutritional Biochemistry, 14, 606–613.
Sardana, M. K., Drummond, G. S., Sassa, S., & Kappas, A. (1981). The potent heme oxygenase inducing action of arsenic and parasiticidal arsenicals. Pharmacology, 23, 247–253.
Sardana, M. K., Sassa, S., & Kappas, A. (1982). Metal ion-mediated regulation of heme oxygenase induction in cultured avian liver cells. The Journal of Biological Chemistry, 257, 4806–4811.
Sardana, M. K., Sassa, S., & Kappas, A. (1985). Hormonal regulation of heme oxygenase induction in avian hepatocyte culture. Biochem Pharmacol, 34, 2937–2944.
Sass, J. B., & Krone, P. H. (1997). HSP90alpha gene expression may be a conserved feature of vertebrate somitogenesis. Experimental Cell Research, 233, 391–394.
Schipper, H. M., & Song, W. (2015). A heme oxygenase-1 transducer model of degenerative and developmental brain disorders. International Journal of Molecular Sciences, 16, 5400–5419.
Selim, M. E., Rashedel, H. A., Aleisa, N. A., & Daghestani, M. H. (2012). The protection role of heat shock protein 70 (HSP-70) in the testes of cadmium-exposed rats. Bioinformation, 8, 58–64.
Semenza, G. L. (2010). Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochimica et Biophysica Acta, 1813, 1263–1268.
Shabtay, A., & Arad, Z. (2006). Reciprocal activation of HSF1 and HSF3 in brain and blood tissues: Is redundancy developmentally related? American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 291, R566–R572.
Shan, Y., Lambrecht, R. W., Hong Lu, T., & Bonkovsky, H. L. (1999). Effects of phenylarsine oxide on expression of heme oxygenase-1 reporter constructs in transiently transfected cultures of chick embryo liver cells. Archives of Biochemistry and Biophysics, 372, 224–229.
Shan, Y., Pepe, J., Lambrecht, R. W., & Bonkovsky, H. L. (2002). Mapping of the chick heme oxygenase-1 proximal promoter for responsiveness to metalloporphyrins. Archives of Biochemistry and Biophysics, 399, 159–166.
Shan, Y., Lambrecht, R. W., & Bonkovsky, H. L. (2004). Identification of key elements that are responsible for heme-mediated induction of the avian heme oxygenase-1 gene. Biochimica et Biophysica Acta, 1679, 87–94.
Shatskih, E., Latipova, E., Fisinin, V., Denev, S., & Surai, P. (2015). Molecular mechanisms and new strategies to fight stresses in egg-producing birds. Agriculture Science and Technology, 7, 3–10.
Shiber, A., & Ravid, T. (2014). Chaperoning proteins for destruction: diverse roles of Hsp70 chaperones and their co-chaperones in targeting misfolded proteins to the proteasome. Biomolecules, 4, 704–724.
Shih, P. K., Chen, Y. C., Huang, Y. C., et al. (2011). Pretreatment of vitamin D3 ameliorates lung and muscle injury induced by reperfusion of bilateral femoral vessels in a rat model. The Journal of Surgical Research, 171, 323–328.
Shinkawa, T., Tan, K., Fujimoto, M., et al. (2011). Heat shock factor 2 is required for maintaining proteostasis against febrile-range thermal stress and polyglutamine aggregation. Molecular Biology of the Cell, 22, 3571–3583.
Shinozaki, F., Minami, M., Chiba, T., et al. (2006). Depletion of hsp90beta induces multiple defects in B cell receptor signaling. The Journal of Biological Chemistry, 281, 16361–16369.
Simar, D., Malatesta, D., Mas, E., Delage, M., & Caillaud, C. (2012). Effect of an 8-weeks aerobic training program in elderly on oxidative stress and HSP72 expression in leukocytes during antioxidant supplementation. The Journal of Nutrition, Health & Aging, 16, 155–161.
Soares, M. P., & Bach, F. H. (2009). Heme oxygenase-1: From biology to therapeutic potential. Trends in Molecular Medicine, 15, 50–58.
Soares, M. P., Usheva, A., Brouard, S., et al. (2002). Modulation of endothelial cell apoptosis by heme oxygenase-1-derived carbon monoxide. Antioxid Redox Signal, 4, 321–329.
Soleimani, A. F., Zulkifli, I., Omar, A. R., & Raha, A. R. (2011). Physiological responses of 3 chicken breeds to acute heat stress. Poultry Science, 90, 1435–1440.
Soleimani, A. F., Zulkifli, I., Omar, A. R., & Raha, A. R. (2012). The relationship between adrenocortical function and Hsp70 expression in socially isolated Japanese quail. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 16, 140–144.
Sozcu, A., & Ipek, A. (2015). Acute and chronic eggshell temperature manipulations during hatching term influence hatchability, broiler performance, and ascites incidence. Poultry Science, 94, 319–327.
Spiro, I. J., Sapareto, S. A., Raaphorst, G. P., & Dewey, W. C. (1982). The effect of chronic and acute heat conditioning on the development of thermal tolerance. International Journal of Radiation Oncology Biology Physics, 8, 53–58.
Sreedhar, A. S., Kalmár, E., Csermely, P., & Shen, Y. F. (2004). Hsp90 isoforms: Functions, expression and clinical importance. FEBS Letters, 562, 11–15.
Stetler, R. A., Gan, Y., Zhang, W., et al. (2010). Heat shock proteins: Cellular and molecular mechanisms in the central nervous system. Progress in Neurobiology, 92, 184–211.
Sun, H., Jiang, R., Xu, S., et al. (2015a). Transcriptome responses to heat stress in hypothalamus of a meat-type chicken. Journal of Animal Science and Biotechnology, 6, 6.
Sun, L., Lamont, S. J., Cooksey, A. M., et al. (2015b). Transcriptome response to heat stress in a chicken hepatocellular carcinoma cell line. Cell Stress Chaperones, 20, 939–950.
Surai, P. F. (1999a). Tissue-specific changes in the activities of antioxidant enzymes during the development of the chicken embryo. British Poultry Science, 40, 397–405.
Surai, P. F. (1999b). Vitamin E in avian reproduction. Poultry and Avian Biology Reviews, 10, 1–60.
Surai, P. F. (2002). Natural antioxidants in avian nutrition and reproduction. Nottingham: Nottingham University Press.
Surai, P. F. (2006). Selenium in nutrition and Health. Nottingham: Nottingham University Press.
Surai, P. F. (2014). Polyphenol compounds in the chicken/animal diet: From the past to the future. Journal of Animal Physiology and Animal Nutrition, 98, 19–31.
Surai, P. F. (2015a). Antioxidant Action of Carnitine: Molecular Mechanisms and Practical Applications. EC Veterinary Science, 2, 66–84.
Surai, P. F. (2015b). Silymarin as a Natural Antioxidant: An overview of the current evidence and perspectives. Antioxidants, 4, 204–247.
Surai, P. F. (2015c). Antioxidant systems in poultry biology: Heat shock proteins. Journal of Science, 5, 1188–1222.
Surai, P. F., & Fisinin, V. I. (2012). The modern anti-stress technologies in poultry: From antioxidants to vitagenes. Agricultural Biology (Sel’skokhozyaistvennaya Biologiya, Moscow), 4, 3–13.
Surai, P.F. and Fisinin, V.I. (2014) Antioxidant systems of the body: From vitamin E to polyphenols and beyond. Proceedings of the 35th Western Nutrition Conference, Edmonton, Alberta, 265–277.
Surai, P. F., & Fisinin, V. I. (2015). Antioxidant-Prooxidant Balance in the Intestine: Applications in chick placement and pig weaning. Journal of Veterinary Science and Medicine, 3, 1–16.
Surai, P. F., Noble, R. C., & Speake, B. K. (1996). Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochimica et Biophysica Acta, 1304, 1–10.
Taipale, M., Jarosz, D. F., & Lindquist, S. (2010). HSP90 at the hub of protein homeostasis: Emerging mechanistic insights. Nature Reviews Molecular Cell Biology, 11, 515–528.
Takii, R., Fujimoto, M., Tan, K., et al. (2015). ATF1 modulates the heat shock response by regulating the stress-inducible heat shock factor 1 transcription complex. Molecular and Cellular Biology, 35, 11–25.
Tanabe, M., Nakai, A., Kawazoe, Y., & Nagata, K. (1997). Different thresholds in the responses of two heat shock transcription factors, HSF1 and HSF3. The Journal of Biological Chemistry, 272, 15389–15395.
Tanabe, M., Kawazoe, Y., Takeda, S., Morimoto, R. I., Nagata, K., & Nakai, A. (1998). Disruption of the HSF3 gene results in the severe reduction of heat shock gene expression and loss of thermotolerance. EMBO Journal, 17, 1750–1758.
Terry, C. M., Clikeman, J. A., Hoidal, J. R., & Callahan, K. S. (1998). Effect of tumor necrosis factor-α and interleukin-1a on heme oxygenase-1 expression in human endothelial cells. American Journal of Physiology-Heart and Circulatory Physiology, 274, H883–H891.
Tona, K., Onagbesan, O., Bruggeman, V., et al. (2008). Effects of heat conditioning at d16–18 of incubation or during early broiler rearing on embryophysiology, post-hatch growth performance and heat tolerance. Arch Geflug, 72, 75–83.
Trinklein, N. D., Chen, W. C., Kingston, R. E., & Myers, R. M. (2004). Transcriptional regulation and binding of heat shock factor 1 and heat shock factor 2 to 32 human heat shock genes during thermal stress and differentiation. Cell Stress Chaperones, 9, 21–28.
True, A. L., Olive, M., Boehm, M., et al. (2007). Heme oxygenase-1 deficiency accelerates formation of arterial thrombosis through oxidative damage to the endothelium, which is rescued by inhaled carbon monoxide. Circulation Research, 101, 893–901.
Tzima, S., Victoratos, P., Kranidioti, K., Alexiou, M., & Kollias, G. (2009). Myeloid heme oxygenase–1 regulates innate immunity and autoimmunity by modulating IFN-b production. The Journal of Experimental Medicine, 206, 1167–1179.
Vachharajani, T. J., Work, J., Issekutz, A. C., & Granger, D. N. (2000). Heme oxygenase modulates selectin expression in different regional vascular beds. American Journal of Physiology-Heart and Circulatory Physiology, 278, H1613–H1617.
Velichko, O. and Surai, P.F. (2014). Effect of an antistress composition supplied with water on chick growth and development. In Proceedings of the XIVth European Poultry Conference, Stavanger, Norway, p. 551.
Velichko, A. K., Markova, E. N., Petrova, N. V., Razin, S. V., & Kantidze, O. L. (2013). Mechanisms of heat shock response in mammals. Cellular and Molecular Life Sciences, 70, 4229–4241.
Venditti, C. C., & Smith, G. N. (2014). Involvement of the heme oxygenase system in the development of preeclampsia and as a possible therapeutic target. Women’s Health (London, England), 10, 623–643.
Vihervaara, A., & Sistonen, L. (2014). HSF1 at a glance. Journal of Cell Science, 127, 261–266.
Voellmy, R., & Bromley, P. A. (1982). Massive heat-shock polypeptide synthesis in late chicken embryos: Convenient system for study of protein synthesis in highly differentiated organisms. Molecular and Cellular Biology, 2, 479–483.
Voellmy, R., Bromley, P., & Kocher, H. P. (1983). Structural similarities between corresponding heat-shock proteins from different eukaryotic cells. The Journal of Biological Chemistry, 258, 3516–3522.
Vourch, C., Binart, N., Chambraud, B., et al. (1989). Isolation and functional analysis of chicken 90-kDa heat shock protein gene promoter. Nucleic Acids Research, 17, 5259–5272.
Walstra, I., Ten Napel, J., Kemp, B., & van den Brand, H. (2010). Temperature manipulation during layer chick embryogenesis. Poultry Science, 89, 1502–1508.
Wang, S., & Edens, F. W. (1998). Heat conditioning induces heat shock proteins in broiler chickens and turkey poults. Poultry Science, 77, 1636–1645.
Wang, S. H., Cheng, C. Y., Tang, P. C., et al. (2013). Differential gene expressions in testes of L2 strain Taiwan country chicken in response to acute heat stress. Theriogenology, 79, 374–382.
Wang, S. H., Cheng, C. Y., Chen, C. J., et al. (2014). Changes in protein expression in testes of L2 strain Taiwan country chickens in response to acute heat stress. Theriogenology, 82, 80–94.
Wayne, N., Mishra, P., & Bolon, D. N. (2011). Hsp90 and client protein maturation. Methods in Molecular Biology, 787, 33–44.
Webb, D. R. (1987). Thermal tolerance of avian embryos: A review. Condor, 89, 874–898.
Wegiel, B., Hedblom, A., Li, M., et al. (2014a). Heme oxygenase-1 derived carbon monoxide permits maturation of myeloid cells. Cell Death & Disease, 5, e1139.
Wegiel, B., Nemeth, Z., Correa-Costa, M., Bulmer, A. C., & Otterbein, L. E. (2014b). Heme oxygenase-1: A metabolic nike. Antioxid Redox Signal, 20, 1709–1722.
Werner, C., Wecke, C., Liebert, F., & Wicke, M. (2010). Increasing the incubation temperature between embryonic day 7 and 10 has no influence on the growth and slaughter characteristics as well as meat quality of broilers. Animal, 4, 810–816.
White, C. N., & Hightower, L. E. (1984). Stress mRNA metabolism in canavanine-treated chicken embryo cells. Molecular and Cellular Biology, 4, 1534–1541.
Whitesell, L., & Lindquist, S. L. (2005). HSP90 and the chaperoning of cancer. Nature Reviews Cancer, 5, 761–772.
Widelitz, R. B., Magun, B. E., & Gerner, E. W. (1986). Effects of cycloheximide on thermotolerance expression, heat shock protein synthesis, and heat shock protein mRNA accumulation in rat fibroblasts. Molecular and Cellular Biology, 6, 1088–1094.
Wijayanti, N., Huber, S., Samoylenko, A., Kietzmann, T., & Immenschuh, S. (2004). Role of NF-kB and p38 MAP kinase signaling pathways in the lipopolysaccharide-dependent activation of heme oxygenase-1 gene expression. Antioxid Redox Signal, 6, 802–810.
Wolfe, M. S., & Zatz, M. (1994). Synthesis of heat shock proteins in cultured chick pineal cells. Brain Research, 662, 273–277.
Wu, M. L., Ho, Y. C., Lin, C. Y., & Yet, S. F. (2011). Heme oxygenase-1 in inflammation and cardiovascular disease. American Journal of Cardiovascular Disease, 1, 150–158.
Xia, M., Gan, J., Luo, Q., Zhang, X., & Yang, G. (2013). Identification of duck HSP70 gene, polymorphism analysis and tissue expression under control and heat stress conditions. British Poultry Science, 54, 562–566.
Xie, J., Tang, L., Lu, L., et al. (2014). Differential expression of heat shock transcription factors and heat shock proteins after acute and chronic heat stress in laying chickens (Gallus gallus). PLoS One, 9, e102204.
Xu, Z., Wang, Z., Li, J. J., et al. (2013). Protective effects of selenium on oxidative damage and oxidative stress related gene expression in rat liver under chronic poisoning of arsenic. Food and Chemical Toxicology, 58, 1–7.
Xu, D., Li, W., Huang, Y., He, J., & Tian, Y. (2014). The effect of selenium and polysaccharide of Atractylodes macrocephala Koidz. (PAMK) on immune response in chicken spleen under heat stress. Biological Trace Element Research, 160, 232–237.
Xu, S., Chen, Y. H., Tan, Z. X., et al. (2015). Vitamin D3 pretreatment alleviates renal oxidative stress in lipopolysaccharide-induced acute kidney injury. The Journal of Steroid Biochemistry and Molecular Biology, 152, 133–141.
Yahav, S., Shamai, A., Haberfeld, A., Horev, G., Hurwitz, S., & Einat, M. (1997a). Induction of thermotolerance in chickens by temperature conditioning: Heat shock protein expression. Annals of the New York Academy of Sciences, 813, 628–636.
Yahav, S., Shamay, A., Horev, G., Bar-Ilan, D., Genina, O., & Friedman-Einat, M. (1997b). Effect of acquisition of improved thermotolerance on the induction of heat shock proteins in broiler chickens. Poultry Science, 76, 1428–1434.
Yahav, S., Sasson Rath, R., & Shinder, D. (2004a). The effect of thermal manipulations during embryogenesis of broiler chicks (Gallus domesticus) on hatchability, body weight and thermoregulation after hatch. Journal of Thermal Biology, 29, 245–250.
Yahav, S., Collin, A., Shinder, D., & Picard, M. (2004b). Thermal manipulations during broiler embryogenesis: Effects of timing and temperature. Poultry Science, 83, 245–250.
Yalçın, S., Çabuk, M., Bruggeman, V., et al. (2008). Acclimation to heat during incubation. 1. Embryonic morphological traits, blood biochemistry, and hatching performance. Poultry Science, 87, 1219–1228.
Yalçın, S., Özkan, S., Sigel, P. B., Yenisey, Ç., & Akşit, M. (2012). Manipulation of in cubation temperatures to increase cold resistance of broilers: Influence on embryo development, organ weights, hormones and body composition. Japan Poultry Science, 49, 133–139.
Yang, Z., Liu, C., Zheng, W., Teng, X., & Li, S. (2016). The functions of antioxidants and heat shock proteins are altered in the immune organs of selenium-deficient broiler chickens. Biological Trace Element Research, 169, 341–351.
Yazama, F., Furuta, K., Fujimoto, M., et al. (2006). Abnormal spermatogenesis in mice unable to synthesize ascorbic acid. Anatomical Science International, 81, 115–125.
Yet, S. F., Perrella, M. A., Layne, M. D., et al. (1999). Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. The Journal of Clinical Investigation, 103, R23–R29.
Yousuf, S., Atif, F., Ahmad, M., et al. (2007). Selenium plays a modulatory role against cerebral ischemia-induced neuronal damage in rat hippocampus. Brain Research, 1147, 218–225.
Yu, J., Bao, E., Yan, J., & Lei, L. (2008). Expression and localization of Hsps in the heart and blood vessel of heat-stressed broilers. Cell Stress Chaperones, 13, 327–335.
Yun, S. H., Moon, Y. S., Sohn, S. H., & Jang, I. S. (2012). Effects of cyclic heat stress or vitamin C supplementation during cyclic heat stress on HSP70, inflammatory cytokines, and the antioxidant defense system in Sprague Dawley rats. Experimental Animals, 61, 543–553.
Zahir, F., Rabbani, G., Khan, R. H., Rizvi, S. J., Jamal, M. S., & Abuzenadah, A. M. (2015). The pharmacological features of bilirubin: the question of the century. Cellular and Molecular Biology Letters, 20, 418–447.
Zhang, H., & Burrows, F. (2004). Targeting multiple signal transduction pathways through inhibition of Hsp90. Journal of Molecular Medicine (Berlin, Germany), 82, 488–499.
Zhang, B., Tanaka, J., Yang, L., et al. (2004). Protective effect of vitamin E against focal brain ischemia and neuronal death through induction of target genes of hypoxia-inducible factor-1. Neuroscience, 126, 433–440.
Zhang, W. W., Kong, L. N., Zhang, X. Q., & Luo, Q. B. (2014). Alteration of HSF3 and HSP70 mRNA expression in the tissues of two chicken breeds during acute heat stress. Genetics and Molecular Research, 13, b9787–b9794.
Zhao, H., Brandt, G. E., Galam, L., Matts, R. L., & Blagg, B. S. (2011). Identification and initial SAR of silybin: An Hsp90 inhibitor. Bioorganic & Medicinal Chemistry Letters, 21, 2659–2664.
Zhao, B., Fei, J., Chen, Y., et al. (2014). Vitamin C treatment attenuates hemorrhagic shock related multi-organ injuries through the induction of heme oxygenase-1. BMC Complementary and Alternative Medicine, 14, 442.
Zhen, F. S., Du, H. L., Xu, H. P., Luo, Q. B., & Zhang, X. Q. (2006). Tissue and allelic-specific expression of hsp70 gene in chickens: Basal and heat-stress-induced mRNA level quantified with real-time reverse transcriptase polymerase chain reaction. British Poultry Science, 47, 449–455.
Zhong, W., Gu, B., Gu, Y., Groome, L. J., Sun, J., & Wang, Y. (2014). Activation of vitamin D receptor promotes VEGF and CuZn-SOD expression in endothelial cells. The Journal of Steroid Biochemistry and Molecular Biology, 140, 56–62.
Zhu, X., Guo, K., & Lu, Y. (2011). Selenium effectively inhibits 1,2-dihydroxynaphthalene-induced apoptosis in human lens epithelial cells through activation of PI3-K/Akt pathway. Molecular Vision, 17, 2019–2027.
Zhu, Y., Lu, X., Wu, D., Cai, S., Li, S., & Teng, X. (2013). The effect of manganese-induced cytotoxicity on mRNA expressions of HSP27, HSP40, HSP60, HSP70 and HSP90 in chicken spleen lymphocytes in vitro. Biological Trace Element Research, 156, 144–152.
Zhu, L., Kong, M., Han, Y. P., et al. (2015). Spontaneous liver fibrosis induced by long term dietary vitamin D deficiency in adult mice is related to chronic inflammation and enhanced apoptosis. Canadian Journal of Physiology and Pharmacology, 93, 385–394.
Zilaee, M., Ferns, G. A., & Ghayour-Mobarhan, M. (2014). Heat shock proteins and cardiovascular disease. Advances in Clinical Chemistry, 64, 73–115.
Zulkifli, I., Che Norma, M. T., Israf, D. A., & Omar, A. R. (2002). The effect of early-age food restriction on heat shock protein 70 response in heat-stressed female broiler chickens. British Poultry Science, 43, 141–145.
Zuo, J., Xu, M., Abdullahi, Y. A., Ma, L., Zhang, Z., & Feng, D. (2015). Constant heat stress reduces skeletal muscle protein deposition in broilers. Journal of the Science of Food and Agriculture, 95, 429–436.
Acknowledgements
Peter F. Surai and Ivan I. Kochish are supported by a grant of the Government of Russian Federation (Contract No. 14.W03.31.0013).
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Surai, P.F., Kochish, I.I. (2017). Antioxidant Systems and Vitagenes in Poultry Biology: Heat Shock Proteins. In: Asea, A., Kaur, P. (eds) Heat Shock Proteins in Veterinary Medicine and Sciences. Heat Shock Proteins, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-319-73377-7_5
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