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Identification of heat shock protein gene expression in hair follicles as a novel indicator of heat stress in beef calves

Published online by Cambridge University Press:  10 February 2020

W. S. Kim Open the ORCID record for W. S. Kim [Opens in a new window] ,
J. Ghassemi Nejad Open the ORCID record for J. Ghassemi Nejad [Opens in a new window] ,
D. Q. Peng Open the ORCID record for D. Q. Peng [Opens in a new window] ,
U. S. Jung Open the ORCID record for U. S. Jung [Opens in a new window] ,
M. J. Kim Open the ORCID record for M. J. Kim [Opens in a new window] ,
Y. H. Jo Open the ORCID record for Y. H. Jo [Opens in a new window] ,
J. H. Jo Open the ORCID record for J. H. Jo [Opens in a new window] ,
J. S. Lee Open the ORCID record for J. S. Lee [Opens in a new window]  and
H. G. Lee Open the ORCID record for H. G. Lee [Opens in a new window]
W. S. Kim
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea Team of an Educational Program for Specialists in Global Animal Science, Brain Korea 21 Plus Project, Sanghuh College of Life Science, Konkuk University, Seoul05029, Republic of Korea
J. Ghassemi Nejad
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea Team of an Educational Program for Specialists in Global Animal Science, Brain Korea 21 Plus Project, Sanghuh College of Life Science, Konkuk University, Seoul05029, Republic of Korea
D. Q. Peng
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea Team of an Educational Program for Specialists in Global Animal Science, Brain Korea 21 Plus Project, Sanghuh College of Life Science, Konkuk University, Seoul05029, Republic of Korea
U. S. Jung
Affiliation:
Department of Animal Science, University of Tennessee, 2506 River Drive, Brehm Animal Science, Knoxville, TN37996, USA
M. J. Kim
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea Department of Animal Science, University of Tennessee, 2506 River Drive, Brehm Animal Science, Knoxville, TN37996, USA
Y. H. Jo
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea Team of an Educational Program for Specialists in Global Animal Science, Brain Korea 21 Plus Project, Sanghuh College of Life Science, Konkuk University, Seoul05029, Republic of Korea
J. H. Jo
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea Team of an Educational Program for Specialists in Global Animal Science, Brain Korea 21 Plus Project, Sanghuh College of Life Science, Konkuk University, Seoul05029, Republic of Korea
J. S. Lee
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea
H. G. Lee*
Affiliation:
Department of Animal Science and Technology, Konkuk University, Seoul05029, Republic of Korea Team of an Educational Program for Specialists in Global Animal Science, Brain Korea 21 Plus Project, Sanghuh College of Life Science, Konkuk University, Seoul05029, Republic of Korea
*
†E-mail: [email protected]
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Abstract

Heat shock proteins (HSPs) consist of highly preserved stress proteins that are expressed in response to stress. Two studies were carried out to investigate whether HSP genes in hair follicles from beef calves can be suggested as indicators of heat stress (HS). In study 1, hair follicles were harvested from three male Hanwoo calves (aged 172.2 ± 7.20 days) on six dates over the period of 10 April to 9 August 2017. These days provided varying temperature–humidity indices (THIs). In study 2, 16 Hanwoo male calves (aged 169.6 ± 4.60 days, with a BW of 136.9 ± 6.23 kg) were maintained (4 calves per experiment) in environmentally controlled chambers. A completely randomized design with a 2 × 4 factorial arrangement involving two periods (thermoneutral: TN; HS) and four THI treatment groups (threshold: THI = 68 to 70; mild: THI = 74 to 76; moderate THI = 81 to 83; severe: THI = 88 to 90). The calves in the different group were subjected to ambient temperature (22°C) for 7 days (TN) and subsequently to the temperature and humidity corresponding to the target THI level for 21 days (HS). Every three days (at 1400 h) during both the TN and HS periods, the heart rate (HR) and rectal temperature (RT) of each individual were measured, and hair follicles were subsequently collected from the tails of each individual. In study 1, the high variation (P < 0.0001) in THI indicated that the external environment influenced the HS to different extents. The expression levels of the HSP70 and HSP90 genes at the high-THI level were higher (P = 0.0120, P = 0.0002) than those at the low-THI level. In study 2, no differences in the THI (P = 0.2638), HR (P = 0.2181) or RT (P = 0.3846) were found among the groups during the TN period, whereas differences in these indices (P < 0.0001, P < 0.0001 and P < 0.0001, respectively) were observed during the HS period. The expression levels of the HSP70 (P = 0.0010, moderate; P = 0.0065, severe) and HSP90 (P = 0.0040, severe) genes were increased after rapid exposure to heat-stress conditions (moderate and severe levels). We conclude that HSP gene expression in hair follicles provides precise and accurate data for evaluating HS and can be considered a novel indicator of HS in Hanwoo calves maintained in both external and climatic chambers.

Keywords

climate-controlled chamberheat-stress indicatorexternal environmentHanwoophysiological parameter
Type
Research Article
Information
animal , Volume 14 , Issue 7 , July 2020 , pp. 1502 - 1509
Copyright
© The Animal Consortium 2020

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References

Ananthan, J, Goldberg, AL and Voellmy, R 1986. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232, 522–524.CrossRefGoogle ScholarPubMed
Botchkarev, VA 2003. Stress and the hair follicle: exploring the connections. American Journal of Pathology 162, 709–712.CrossRefGoogle ScholarPubMed
Collier, RJ, Collier, JL, Rhoads, RP and Baumgard, LH 2008. Invited Review: Genes involved in the bovine heat stress response. Journal of Dairy Science 91, 445–454.CrossRefGoogle ScholarPubMed
Ghassemi Nejad, J, Lohakare, JD, Son, JK, Kwon, EG, West, JW and Sung, KI 2014. Wool cortisol is a better indicator of stress than blood cortisol in ewes exposed to heat stress and water restriction. Animal 8, 128–132.CrossRefGoogle ScholarPubMed
Ghassemi Nejad, J and Sung, KI 2017. Behavioral and physiological changes during heat stress in Corriedale ewes exposed to water deprivation. Journal of Animal Science and Technology 59, 13.CrossRefGoogle ScholarPubMed
Givskov, SJ, Nygaard, KT and Volker, L 2003. The evolutionary and ecological role of heat shock proteins. Ecology Letters 6, 1025–1037.Google Scholar
Hansen, PJ 2004. Physiological and cellular adaptations of zebu cattle to thermal stress. Animal Reproduction Science 82–83, 349–360.CrossRefGoogle ScholarPubMed
Jakob, U and Buchner, J 1994. Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones. Trends in Biochemical Sciences 19, 205–211.CrossRefGoogle ScholarPubMed
Johnson, HD and Vanjonack, WJ 1976. Effects of environmental and other stressors on blood hormone patterns in lactating animals. Journal of Dairy Science 59, 1603–1617.CrossRefGoogle ScholarPubMed
Kadzere, CT, Murphy, MR, Silanikove, N and Maltz, E 2002. Heat stress in lactating dairy cows: a review. Livestock Production Science 77, 59–91.CrossRefGoogle Scholar
Kang, HJ, Lee, IK, Piao, MY, Gu, MJ, Yun, CH, Kim, HJ, Kim, KH and Baik, M 2016. Effects of ambient temperature on growth performance, blood metabolites, and immune cell populations in Korean cattle steers. Asian-Australasian Journal of Animal Science 29, 436–443.CrossRefGoogle ScholarPubMed
Kim, WS, Lee, JS, Jeon, SW, Peng, DQ, Kim, YS, Bae, MH, Jo, YH and Lee, HG 2018b. Correlation between blood, physiological and behavioral parameters in beef calves under heat stress. Asian-Australasian Journal of Animal Science 31, 919–925.CrossRefGoogle ScholarPubMed
Kim, WS, Lee, JS, Peng, DQ, Ronel, JRV, Jo, YH, Jo, JH, Seo, JK, Choi, WT, Kim, JE, Kim, TB and Lee, HG 2018a. PSXVI-39 Responses of growth performance, physiological and blood parameter to long-term heat stress in beef calves. Journal of Animal Science 96, 384–385.CrossRefGoogle Scholar
Kristensen, TN, Løvendahl, P, Berg, P and Loeschcke, V 2004. Hsp72 is present in plasma from Holstein-Friesian dairy cattle, and the concentration level is repeatable across days and age classes. Cell Stress & Chaperones 9, 143–149.CrossRefGoogle ScholarPubMed
Kumar, A, Ashraf, S, Goud, TS, Grewal, A, Singh, SV, Yadav, BR and Upadhyay, RC 2015. Expression profiling of major heat shock protein genes during different seasons in cattle (Bos indicus) and buffalo (Bubalus bubalis) under tropical climatic condition. Journal of Thermal Biology 51, 55–64.CrossRefGoogle ScholarPubMed
Lacetera, N, Bernabucci, U, Scalia, D, Basiricò, L, Morera, P and Nardone, A 2006. Heat stress elicits different responses in peripheral blood mononuclear cells from brown Swiss and Holstein cows. Journal of Dairy Science 89, 4606–4612.CrossRefGoogle ScholarPubMed
Li, D, Ren, W, Wang, X, Wang, F, Gao, Y, Ning, Q, Han, Y, Song, T and Lu, S 2009. A modified method using TRIzol® reagent and liquid nitrogen produces high-quality RNA from rat pancreas. Applied Biochemistry and Biotechnology 158, 253–261.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.CrossRefGoogle Scholar
McArthur, AJ and Clark, JA 1988. Body temperature of homeotherms and the conservation of energy and water. Journal of Thermal Biology 13, 9–13.CrossRefGoogle Scholar
McDowell, RE, Hooven, NW and Camoens, JK 1976. Effect of climate on performance of Holsteins in first lactation. Journal of Dairy Science 59, 965–971.CrossRefGoogle Scholar
National Research Council (NRC ) 1971. A guide to environmental research on animals. National Academy of Sciences, Washington, DC, USA.Google Scholar
O’Brien, MD, Rhoads, RP, Sanders, SR, Duff, GC and Baumgard, LH 2010. Metabolic adaptations to heat stress in growing cattle. Domestic Animal Endocrinology 38, 86–94.CrossRefGoogle ScholarPubMed
Parsell, DA and Lindquist, S 1993. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annual Review of Genetics 27, 437–496.CrossRefGoogle ScholarPubMed
Purwanto, BP, Abo, Y, Sakamoto, R, Furumoto, F and Yamamoto, S 2009. Diurnal patterns of heat production and heart rate under thermoneutral conditions in Holstein Friesian cows differing in milk production. The Journal of Agricultural Science 114, 139–142.CrossRefGoogle Scholar
Richards, JI 1985. Milk production of Friesian cows subjected to high daytime temperatures when allowed food either ad lib or at night-time only. Tropical Animal Health and Production 17, 141–152.CrossRefGoogle ScholarPubMed
Schmittgen, TD and Livak, KJ 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.CrossRefGoogle Scholar
Silanikove, N 2000. Effects of heat stress on the welfare of extensively managed domestic ruminants. Livestock Production Science 67, 1–18.CrossRefGoogle Scholar
Spiers, DE, Spain, JN, Sampson, JD and Rhoads, RP 2004. Use of physiological parameters to predict milk yield and feed intake in heat-stressed dairy cows. Journal of Thermal Biology 29, 759–764.CrossRefGoogle Scholar
Tao, S, Monteiro, APA, Thompson, IM, Hayen, MJ and Dahl, GE 2012. Effect of late-gestation maternal heat stress on growth and immune function of dairy calves. Journal of Dairy Science 95, 7128–7136.CrossRefGoogle ScholarPubMed
Voellmy, R 1996. Sensing stress and responding to stress. In Stress-Inducible Cellular Responses (ed. Feige, U, Morimoto, RI, Yahara, I and Polla, BS), pp. 121–138. Birkhäuser, Basel, Switzerland.CrossRefGoogle Scholar
Voellmy, R, Zürcher, O, Zürcher, M, de Viragh, PA, Hall, AK and Roberts, SM 2018. Targeted heat activation of HSP promoters in the skin of mammalian animals and humans. Cell Stress & Chaperones 23, 455–466.CrossRefGoogle ScholarPubMed
West, JW 1994. Interactions of energy and bovine somatotropin with heat stress. Journal of Dairy Science 77, 2091–2102.CrossRefGoogle ScholarPubMed
West, JW 2003. Effects of heat-stress on production in dairy cattle. Journal of Dairy Science 86, 2131–2144.CrossRefGoogle ScholarPubMed
Yamada, J, Stevens, B, de Silva, N, Gibbins, S, Beyene, J, Taddio, A, Newman, C and Koren, G 2007. Hair cortisol as a potential biologic marker of chronic stress in hospitalized neonates. Neonatology 92, 42–49.CrossRefGoogle ScholarPubMed
Zou, J, Guo, Y, Guettouche, T, Smith, DF and Voellmy, R 1998. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94, 471–480.CrossRefGoogle ScholarPubMed
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