Issue
Organic chromium modifies the expression of orexin and glucose transporters of ovarian in heat-stressed laying hens
Corresponding Author(s) : K. Sahin
Cellular and Molecular Biology,
Vol. 63 No. 10: Issue 10
Abstract
In this study, the effect of the supplemental organic chromium (Cr) forms on the expression of ovarian orexin(hypocretin), glucose transporters (GLUTs), heat shock proteins (HSPs) andnuclear factor-kappaB (NF-κB)were investigated in laying hens (HS). Laying hens (n=1800; 16-wk-old; Lohmann LSL-Lite) were allocated to 6 random groups according to a 2"‰í—"‰3 factorial trial scheme with two different environmental temperatures [Thermoneutral (TN groups; at either 22±2 °C 24 h/d) and heat stress (HS groups; at 34±2 °C for 8 h/d, 08:00 to 17:00 h, followed by 22°C for 16 h for a period of 12 wks)], andhens reared under both environmental conditions were fed either a basal diet or the basal diet supplemented with 1.600 mg of chromium-picolinate (CrPic, 12.43% Cr) and 0.788 mg of chromium-histidinate (CrHis, 25.22% Cr) per kg of diet, delivering 200 µg elemental Cr per kg diet. HS groups showed decreased levels of orexin and GLUTs(GLUT1, GLUT4), and increased NFκB, HSP60, HSP70 and HSP90 levels compared to the TN groups in ovarian tissue of hens (P < 0.0001 for all).However, dietary chromium supplementation (CrPic–CrHis) increasedorexin and GLUTs levels and significantly reduced the NF-κB and HSPs levels making them closer to those of thermoneutral group (P < 0.0001).In conclusion, CrPic and CrHis showed supported the relief and treatment of stress complications.
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- References
- Sahin K, Orhan C, Tuzcu M, Ali S, Sahin N, Hayirli A. Epigallocatechin 3-gallate prevents lipid peroxidation and enhances antioxidant defense system via modulating hepatic nuclear transcription factors in heat-stressed quails. Poult Sci 2010; 89: 2251-8.
- Tang S, Yin B, Song E, Chen H, Cheng Y, Zhang X et al. Aspirin upregulates αB-Crystallin to protect the myocardium against heat stress in broiler chicken. Sci Rep 2016; 6: 372–73.
- Santos RR, Awati A, Roubos-van den Hil PJ, Tersteeg-Zijderveld MH, Koolmees PA, Fink-Gremmels J. Quantitative histo-morphometric analysis of heat-stress related damage in the small intestines of broiler chickens. Avian Pathol 2014; 20: 1–14.
- Sahin K, and Kucuk O: Heat stress and dietary vitamin supplementation of poultry diets, Nutrition Abstracts and Reviews. Series B: Livestock Feeds and Feeding 2003; 73: 41–50.
- Orhan C, Akdemir F, Sahin N, Tuzcu M, Komorowski JR, Hayirli A et al. Chromium histidinate protects against heat stress by modulating the expression of hepatic nuclear transcription factors in quail. Br Poult Sci 2012; 53: 828–835.
- Chen Z, Gan J, Xiao X, Jiang L, Zhang X, Luo Q. The association of SNPs in Hsp90b gene 50 flanking region with thermo tolerance traits and tissue mRNA expression in two chicken breeds. Mol Biol Rep 2013; 40: 5295–5306.
- Bernabò P, Rebecchi L, Jousson O, Martínez-Guitarte JL, Lencioni V. Thermotolerance and hsp70 heat shock response in the cold-stenothermal chironomid Pseudodiamesa branickii (NE Italy). Cell Stress Chaperones 2011; 16: 403–10.
- Greene E, Khaldi S, Ishola P, Bottje W, Ohkubo T, Anthony N et al. Heat and oxidative stress alter the expression of orexin and its related receptors in avian liver cells. Comp Biochem Physiol A Mol Integr Physiol 2016; 191:18–24.
- González JA, Jensen LT, Iordanidou P, Strom M, Fugger L, Burdakov D. Inhibitory interplay between orexin neurons and eating. Curr Biol 2016; 26: 2486–2491.
- Nakamura K. Neural circuit for psychological stress-induced hyperthermia. Temperature (Austin) 2015; 2:352–361.
- Elbaz I, Levitas-Djerbi T, Appelbaum L. The Hypocretin/Orexin neuronal networks in zebrafish. Curr Topics Behav Neurosci 2016; 1-18.
- Goforth PB and Myers MG. Roles for orexin/hypocretin in the control of energy balance and metabolism. Curr Topics Behav Neurosci 2016; 1–20.
- Zhang NCW, Wang Z, Wang X, Xia G. The effect of gonadotropin on glucose transport and apoptosis in rat ovary. Plos One 2012; 7: 1–8.
- Rudlowski C, Moser M, Becker AJ, Rath W, Buttner R, Schroder W et al. GLUT1 mrna and protein expression in ovarian borderline tumors and cancer. Oncology 2003; 66: 404–410.
- Kodaman PH and Behrman HR. Hormone-regulated and glucose-sensitive transport of dehydroascorbic acid in immature rat granulosa cells. Endocrinology 1999; 140: 3659–3665.
- Williams SA, Blache, D, Martin GB, Foot R, Blackberry MA, Scaramuzzi RJ. Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction 2001; 122: 947–956.
- An L, Lei K, Zheng B. Use of heat shock protein mRNA expressions asbiomarkers in wild crucian carp for monitoringwater quality. Environmental Toxicology and Pharmacology 2014; 37: 247-255.
- Kennedy D, Jeager R, Mosser DD, Samali A. Regulation of apoptosis by heat shock proteins. IUBMB Life 2014; 66: 327–338.
- Akdemir F, Sahin N, Orhan C, Tuzcu M, Sahin K, Hayirli A. Chromium-histidinate ameliorates productivity in heat-stressed Japanese quails through reducing oxidative stress and inhibiting heat-shock protein expression. Br Poult Sci 2015; 56: 247–254.
- Khandia R, Munjal AK, Iqbal HM, Dhama K. Heat Shock Proteins: Therapeutic perspectives in inflammatory disorders. Recent Pat Inflamm Allergy Drug Discov 2016; 10 Doi: 10.2174/1872213X10666161213163301.
- Kero D, Govorko DK, Mikic IM, Vukojevic K, Cigic L, Saraga-Babic M. Analysis of expression patterns of IGF-1, caspase-3 and HSP-70 in developing human tooth germs. Arch Oral Biol 2015; 60: 1533–1544.
- Khoso PA, Liu C, Liu C, Khoso MH, Li S. Selenium deficiency activates heat shock protein expression in chicken spleen and thymus. Biol Trace Elem Res 2016; 173: 492–500.
- Bellaye P, Burgy O, Causse S, Garrido C, Bonniaud P. Heat shock proteins in fibrosis and wound healing: Good or evil?. Pharmacology & Therapeutics 2014; 143: 119–132.
- Nennig SE and Schank JR. The role of NFkB in drug addiction: Beyond inflammation. Alcohol Alcohol 2017; 52: 172–179.
- Sahin K. Modulation of NF-κB and Nrf2 pathways by lycopene supplementation in heat-stressed poultry. World's Poult Sci J 2015; 71: 271–284.
- Vilcek J and Lee TH. Tumor necrosis factor. J Biol Chem 1991; 266: 7313–7316.
- Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers. FASEB J 1995; 9: 899–909.
- Chen F, Castranova V, Shi X. New insights into the role of nuclear factor-kappaB in cell growth regulation. Am J Pathol 2001; 159: 387–97.
- Huang Y, Yang J, Xiao F, Lloyd K, Lin X. Effects of supplemental chromium source and concentration on growth performance, carcass traits, and meat quality of broilers under heat stress conditions. Biol Trace Elem Res 2016; 170: 216–223.
- Samanta S, Haldar S, Bahadur V, Ghosh TK. Chromium picolinate can ameliorate the negative effects of heat stress and enhance performance, carcass and meat traits in broiler chickens by reducing the circulatory cortisol concentration. J Sci Food Agric 2008; 88: 787–796.
- Xiao F, Ao D, Zhou B, Spears JW, Lin X, Huang Y. Effects of supplemental chromium propionate on serum lipids, carcass traits, and meat quality of heat-stressed broilers. Biol Trace Elem Res 2016; Doi: 10.1007/S12011-016-0852-7.
- El-Kholy MS, El-Hindawy MM, Alagawany M, Abd El-Hack ME, El-Sayed SA. Dietary supplementation of chromium can alleviate negative impacts of heat stress on performance, carcass yield, and some blood hematology and chemistry indices of growing japanese quail. Biol Trace Elem Res 2017; doi: 10.1007/s12011-017-0936-z.
- Sahin N, Akdemir F, Tuzcu M, Hayirli A, Smith MO, Sahin K. Effects of supplemental chromium sources and levels on performance, lipid peroxidation and proinflammatory markers in heat-stressed quails. Anim Feed Sci Technol 2010; 159: 143–149.
- Sahin K, Orhan C, Tuzcu M, Sahin N, Hayirli A, Bilgili S et al. Lycopene activates antioxidant enzymes and nuclear transcription factor systems in heat-stressed broilers. Poult Sci 2016; 95: 1088–1095.
- Rafiee F, Mazhari M, Ghoreishi M, Esmaeilipour O. Effect of lemon verbena powder and vitamin C on performance and immunity of heat-stressed broilers. J Anim Physiol Anim Nutr 2016; 100: 807–812.
- Rimoldi S, Lasagna E, Sarti FM, Marelli SP, Cozzi MC, Bernardini G et al. Expression profile of six stress-related genes and productive performances of fast and slow growing broiler strains reared under heat stress conditions. Meta Gene 2015; 6: 17–25.
- Vinoth A, Thirunalasundari T, Tharian JA, Shanmugam M, Rajkumar U. Effect of thermal manipulation during embryogenesis on liver heat shock protein expression in chronic heat stressed colored broiler chickens. J Therm Biol 2015; 53: 162–171.
- Wu D, Zhang M, Xu J, Song E, Lv Y, Tang S et al. In vitro evaluation of aspirin-induced HspB1 against heat stress damage in chicken myocardial cells. Cell Stress and Chaperones 2016; 21: 405–413.
- Zeferino CP, Komiyama CM, Pelícia VC, Fascina VB, Aoyagi MM, Coutinho LL et al. Carcass and meat quality traits of chickens fed diets concurrently supplemented with vitamins C and E under constant heat stress. Animal 2016; 10: 163–171.
- Ryu S, Park B, Bang H, Kang H, Hwangbo J. Effects of anti-heat diet and inverse lighting on growth performance, immune organ, microorganism and short chain fatty acids of broiler chickens under heat stress. J Environ Biol 2016; 37: 185–192.
- Zhang X, Qian Z, Zhu H, Tang S, Wu D, Zhang M et al. HSP90 gene expression induced by aspirin is associated with damage remission in a chicken myocardial cell culture exposed to heat stress. Br Poult Sci 2016; 57: 1–12.
- Sahin K, Orhan C, Akdemir F, Tuzcu M, Ali S, Sahin N. Tomato powder supplementation activates Nrf-2 via ERK/Akt signaling pathway and attenuates heat stress-related responses in quails. Animal Feed Sci Technol 2011; 65: 230–237.
- Akbari M and Torki M. Effects of dietary chromium picolinate and peppermint essential oil on growth performance and blood biochemical parameters of broiler chicks reared under heat stress conditions. Int J Biometeorol 2014; 58: 1383–1391.
- Buyukleblebici O and Karagul H. The biochemical effects of dietary chromium in experimental diabetic rats with streptozotocin. J Fac Vet Med Kafkas Univ 2012; 18: 21–26.
- Sahin K, Tuzcu M, Orhan C, Ali S, Sahin N, Gencoglu H et al. Chromium modulates expressions of neuronal plasticity markers and glial fibrillary acidic proteins in hypoglycemia-induced brain injury. Life Sci 2013; 93: 1039–1048.
- Torki M, Zangeneh S, Habibian M. Performance, egg quality traits, and serum metabolite concentrations of laying hens affected by dietary supplemental chromium picolinate and vitamin C under a heat-stress condition. Biol Trace Elem Res 2014; 157: 120–9.
- Grafe LA, Cornfeld A, Luz S, Valentino R, Bhatnagar S. Orexins mediate sex differences in the stress response and in cognitive flexibility. Biol Psychiatry 2017; 15:683-692.
- Wang H, Li S, Kirouac GJ. Role of the orexin (hypocretin) system in contextual fear conditioning in rats. Behav Brain Res 2017; 316: 47–53.
- Lei L, Hepeng L, Xianlei L, Hongchao J, Hai L, Sheikhahmadi A et al. Effects of acute heat stress on gene expression of brain–gut neuropeptides in broiler chickens. J Anim Sci 2014; 91: 5194–5201.
- Ulas M, Orhan C, Tuzcu M, Ozercan IH, Sahin N, Gencoglu H et al. Anti-diabetic potential of chromium histidinate in diabetic retinopathy rats. BMC Complement Altern Med 2015; 5:15–16.
- Won M, Byun HS, Park KA, Hur GM. Post-translational control of NF-kB signaling by ubiquitination. Arch Pharm Res 2016; 39: 1075–1084.
- Bossola M, Pacelli F, Tortorelli A. Skeletal muscle in cancer cachexia: the ideal target of drug therapy. Curr Cancer Drug Targets 2008; 8: 285–298.
- Orhan C, Tuzcu M, Gencoglu H, Sahin N, Hayirli A, Sahin K. Epigallocatechin-3-gallate exerts protective effects against heat stress through modulating stress-responsive transcription factors in poultry. Br Poult Sci 2013; 54: 447–53.
- Dogukan A, Tuzcu M, Juturu V, Cikim G, Ozercan I, Komorowski J et al. Effects of chromium histidinate on renal function, oxidative stress, and heat-shock proteins in fat-fed and streptozotocin-treated rats. J Ren Nutr 2010; 20: 112–120.
References
References
Sahin K, Orhan C, Tuzcu M, Ali S, Sahin N, Hayirli A. Epigallocatechin 3-gallate prevents lipid peroxidation and enhances antioxidant defense system via modulating hepatic nuclear transcription factors in heat-stressed quails. Poult Sci 2010; 89: 2251-8.
Tang S, Yin B, Song E, Chen H, Cheng Y, Zhang X et al. Aspirin upregulates αB-Crystallin to protect the myocardium against heat stress in broiler chicken. Sci Rep 2016; 6: 372–73.
Santos RR, Awati A, Roubos-van den Hil PJ, Tersteeg-Zijderveld MH, Koolmees PA, Fink-Gremmels J. Quantitative histo-morphometric analysis of heat-stress related damage in the small intestines of broiler chickens. Avian Pathol 2014; 20: 1–14.
Sahin K, and Kucuk O: Heat stress and dietary vitamin supplementation of poultry diets, Nutrition Abstracts and Reviews. Series B: Livestock Feeds and Feeding 2003; 73: 41–50.
Orhan C, Akdemir F, Sahin N, Tuzcu M, Komorowski JR, Hayirli A et al. Chromium histidinate protects against heat stress by modulating the expression of hepatic nuclear transcription factors in quail. Br Poult Sci 2012; 53: 828–835.
Chen Z, Gan J, Xiao X, Jiang L, Zhang X, Luo Q. The association of SNPs in Hsp90b gene 50 flanking region with thermo tolerance traits and tissue mRNA expression in two chicken breeds. Mol Biol Rep 2013; 40: 5295–5306.
Bernabò P, Rebecchi L, Jousson O, Martínez-Guitarte JL, Lencioni V. Thermotolerance and hsp70 heat shock response in the cold-stenothermal chironomid Pseudodiamesa branickii (NE Italy). Cell Stress Chaperones 2011; 16: 403–10.
Greene E, Khaldi S, Ishola P, Bottje W, Ohkubo T, Anthony N et al. Heat and oxidative stress alter the expression of orexin and its related receptors in avian liver cells. Comp Biochem Physiol A Mol Integr Physiol 2016; 191:18–24.
González JA, Jensen LT, Iordanidou P, Strom M, Fugger L, Burdakov D. Inhibitory interplay between orexin neurons and eating. Curr Biol 2016; 26: 2486–2491.
Nakamura K. Neural circuit for psychological stress-induced hyperthermia. Temperature (Austin) 2015; 2:352–361.
Elbaz I, Levitas-Djerbi T, Appelbaum L. The Hypocretin/Orexin neuronal networks in zebrafish. Curr Topics Behav Neurosci 2016; 1-18.
Goforth PB and Myers MG. Roles for orexin/hypocretin in the control of energy balance and metabolism. Curr Topics Behav Neurosci 2016; 1–20.
Zhang NCW, Wang Z, Wang X, Xia G. The effect of gonadotropin on glucose transport and apoptosis in rat ovary. Plos One 2012; 7: 1–8.
Rudlowski C, Moser M, Becker AJ, Rath W, Buttner R, Schroder W et al. GLUT1 mrna and protein expression in ovarian borderline tumors and cancer. Oncology 2003; 66: 404–410.
Kodaman PH and Behrman HR. Hormone-regulated and glucose-sensitive transport of dehydroascorbic acid in immature rat granulosa cells. Endocrinology 1999; 140: 3659–3665.
Williams SA, Blache, D, Martin GB, Foot R, Blackberry MA, Scaramuzzi RJ. Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction 2001; 122: 947–956.
An L, Lei K, Zheng B. Use of heat shock protein mRNA expressions asbiomarkers in wild crucian carp for monitoringwater quality. Environmental Toxicology and Pharmacology 2014; 37: 247-255.
Kennedy D, Jeager R, Mosser DD, Samali A. Regulation of apoptosis by heat shock proteins. IUBMB Life 2014; 66: 327–338.
Akdemir F, Sahin N, Orhan C, Tuzcu M, Sahin K, Hayirli A. Chromium-histidinate ameliorates productivity in heat-stressed Japanese quails through reducing oxidative stress and inhibiting heat-shock protein expression. Br Poult Sci 2015; 56: 247–254.
Khandia R, Munjal AK, Iqbal HM, Dhama K. Heat Shock Proteins: Therapeutic perspectives in inflammatory disorders. Recent Pat Inflamm Allergy Drug Discov 2016; 10 Doi: 10.2174/1872213X10666161213163301.
Kero D, Govorko DK, Mikic IM, Vukojevic K, Cigic L, Saraga-Babic M. Analysis of expression patterns of IGF-1, caspase-3 and HSP-70 in developing human tooth germs. Arch Oral Biol 2015; 60: 1533–1544.
Khoso PA, Liu C, Liu C, Khoso MH, Li S. Selenium deficiency activates heat shock protein expression in chicken spleen and thymus. Biol Trace Elem Res 2016; 173: 492–500.
Bellaye P, Burgy O, Causse S, Garrido C, Bonniaud P. Heat shock proteins in fibrosis and wound healing: Good or evil?. Pharmacology & Therapeutics 2014; 143: 119–132.
Nennig SE and Schank JR. The role of NFkB in drug addiction: Beyond inflammation. Alcohol Alcohol 2017; 52: 172–179.
Sahin K. Modulation of NF-κB and Nrf2 pathways by lycopene supplementation in heat-stressed poultry. World's Poult Sci J 2015; 71: 271–284.
Vilcek J and Lee TH. Tumor necrosis factor. J Biol Chem 1991; 266: 7313–7316.
Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers. FASEB J 1995; 9: 899–909.
Chen F, Castranova V, Shi X. New insights into the role of nuclear factor-kappaB in cell growth regulation. Am J Pathol 2001; 159: 387–97.
Huang Y, Yang J, Xiao F, Lloyd K, Lin X. Effects of supplemental chromium source and concentration on growth performance, carcass traits, and meat quality of broilers under heat stress conditions. Biol Trace Elem Res 2016; 170: 216–223.
Samanta S, Haldar S, Bahadur V, Ghosh TK. Chromium picolinate can ameliorate the negative effects of heat stress and enhance performance, carcass and meat traits in broiler chickens by reducing the circulatory cortisol concentration. J Sci Food Agric 2008; 88: 787–796.
Xiao F, Ao D, Zhou B, Spears JW, Lin X, Huang Y. Effects of supplemental chromium propionate on serum lipids, carcass traits, and meat quality of heat-stressed broilers. Biol Trace Elem Res 2016; Doi: 10.1007/S12011-016-0852-7.
El-Kholy MS, El-Hindawy MM, Alagawany M, Abd El-Hack ME, El-Sayed SA. Dietary supplementation of chromium can alleviate negative impacts of heat stress on performance, carcass yield, and some blood hematology and chemistry indices of growing japanese quail. Biol Trace Elem Res 2017; doi: 10.1007/s12011-017-0936-z.
Sahin N, Akdemir F, Tuzcu M, Hayirli A, Smith MO, Sahin K. Effects of supplemental chromium sources and levels on performance, lipid peroxidation and proinflammatory markers in heat-stressed quails. Anim Feed Sci Technol 2010; 159: 143–149.
Sahin K, Orhan C, Tuzcu M, Sahin N, Hayirli A, Bilgili S et al. Lycopene activates antioxidant enzymes and nuclear transcription factor systems in heat-stressed broilers. Poult Sci 2016; 95: 1088–1095.
Rafiee F, Mazhari M, Ghoreishi M, Esmaeilipour O. Effect of lemon verbena powder and vitamin C on performance and immunity of heat-stressed broilers. J Anim Physiol Anim Nutr 2016; 100: 807–812.
Rimoldi S, Lasagna E, Sarti FM, Marelli SP, Cozzi MC, Bernardini G et al. Expression profile of six stress-related genes and productive performances of fast and slow growing broiler strains reared under heat stress conditions. Meta Gene 2015; 6: 17–25.
Vinoth A, Thirunalasundari T, Tharian JA, Shanmugam M, Rajkumar U. Effect of thermal manipulation during embryogenesis on liver heat shock protein expression in chronic heat stressed colored broiler chickens. J Therm Biol 2015; 53: 162–171.
Wu D, Zhang M, Xu J, Song E, Lv Y, Tang S et al. In vitro evaluation of aspirin-induced HspB1 against heat stress damage in chicken myocardial cells. Cell Stress and Chaperones 2016; 21: 405–413.
Zeferino CP, Komiyama CM, Pelícia VC, Fascina VB, Aoyagi MM, Coutinho LL et al. Carcass and meat quality traits of chickens fed diets concurrently supplemented with vitamins C and E under constant heat stress. Animal 2016; 10: 163–171.
Ryu S, Park B, Bang H, Kang H, Hwangbo J. Effects of anti-heat diet and inverse lighting on growth performance, immune organ, microorganism and short chain fatty acids of broiler chickens under heat stress. J Environ Biol 2016; 37: 185–192.
Zhang X, Qian Z, Zhu H, Tang S, Wu D, Zhang M et al. HSP90 gene expression induced by aspirin is associated with damage remission in a chicken myocardial cell culture exposed to heat stress. Br Poult Sci 2016; 57: 1–12.
Sahin K, Orhan C, Akdemir F, Tuzcu M, Ali S, Sahin N. Tomato powder supplementation activates Nrf-2 via ERK/Akt signaling pathway and attenuates heat stress-related responses in quails. Animal Feed Sci Technol 2011; 65: 230–237.
Akbari M and Torki M. Effects of dietary chromium picolinate and peppermint essential oil on growth performance and blood biochemical parameters of broiler chicks reared under heat stress conditions. Int J Biometeorol 2014; 58: 1383–1391.
Buyukleblebici O and Karagul H. The biochemical effects of dietary chromium in experimental diabetic rats with streptozotocin. J Fac Vet Med Kafkas Univ 2012; 18: 21–26.
Sahin K, Tuzcu M, Orhan C, Ali S, Sahin N, Gencoglu H et al. Chromium modulates expressions of neuronal plasticity markers and glial fibrillary acidic proteins in hypoglycemia-induced brain injury. Life Sci 2013; 93: 1039–1048.
Torki M, Zangeneh S, Habibian M. Performance, egg quality traits, and serum metabolite concentrations of laying hens affected by dietary supplemental chromium picolinate and vitamin C under a heat-stress condition. Biol Trace Elem Res 2014; 157: 120–9.
Grafe LA, Cornfeld A, Luz S, Valentino R, Bhatnagar S. Orexins mediate sex differences in the stress response and in cognitive flexibility. Biol Psychiatry 2017; 15:683-692.
Wang H, Li S, Kirouac GJ. Role of the orexin (hypocretin) system in contextual fear conditioning in rats. Behav Brain Res 2017; 316: 47–53.
Lei L, Hepeng L, Xianlei L, Hongchao J, Hai L, Sheikhahmadi A et al. Effects of acute heat stress on gene expression of brain–gut neuropeptides in broiler chickens. J Anim Sci 2014; 91: 5194–5201.
Ulas M, Orhan C, Tuzcu M, Ozercan IH, Sahin N, Gencoglu H et al. Anti-diabetic potential of chromium histidinate in diabetic retinopathy rats. BMC Complement Altern Med 2015; 5:15–16.
Won M, Byun HS, Park KA, Hur GM. Post-translational control of NF-kB signaling by ubiquitination. Arch Pharm Res 2016; 39: 1075–1084.
Bossola M, Pacelli F, Tortorelli A. Skeletal muscle in cancer cachexia: the ideal target of drug therapy. Curr Cancer Drug Targets 2008; 8: 285–298.
Orhan C, Tuzcu M, Gencoglu H, Sahin N, Hayirli A, Sahin K. Epigallocatechin-3-gallate exerts protective effects against heat stress through modulating stress-responsive transcription factors in poultry. Br Poult Sci 2013; 54: 447–53.
Dogukan A, Tuzcu M, Juturu V, Cikim G, Ozercan I, Komorowski J et al. Effects of chromium histidinate on renal function, oxidative stress, and heat-shock proteins in fat-fed and streptozotocin-treated rats. J Ren Nutr 2010; 20: 112–120.