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Exploring Epigenetic and Genetic Modulation in Animal Responses to Thermal Stress

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Abstract

There is increasing evidence indicating that global temperatures are rising significantly, a phenomenon commonly referred to as ‘global warming’, which in turn is believed to be causing drastic changes to the global climate. Global warming (GW) directly impacts animal health, reproduction, production, and welfare, presenting several challenges to livestock enterprises. Thermal stress (TS) is one of the key consequences of GW, and all animal species, including livestock, have diverse physiological, epigenetic and genetic mechanisms to respond to TS. As a result, TS can significantly affect an animals’ health, immune responsiveness, metabolic pathways etc. which can also influence the productivity, performance, and welfare of animals. Moreover, prolonged exposure to TS can lead to transgenerational and intergenerational changes that are mediated by epigenetic changes. For example, in several animal species, the effects of TS are encoded epigenetically during the animals’ growth or productive stage, and these epigenetic changes can be transmitted intergenerationally. Such epigenetic changes can affect animal productivity by changing the phenotype so that it aligns with its ancestors’ environment, irrespective of its immediate environment. Furthermore, epigenetic and genetic changes can also help protect cells from the adverse effects of TS by modulating the transcriptional status of heat-responsive genes in animals. This review focuses on the genetic and epigenetic modulation and regulation that occurs in TS conditions via HSPs, histone alterations and DNA methylation.

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Data Availability

All data are available within the manuscript.

Abbreviations

GW:

Global warming

TS:

Thermal stress

HSPs:

Heat shock proteins

HSF1:

Heat shock factor

OS:

Oxidative stress

ERS:

Endoplasmic reticulum stress

HSP60, HSP70, and HSP90:

Heat shock proteins 60, 70 and 90

αB-crystallin:

HSPB5

HSP25/27:

HSPB1

ASK1-p38:

Apoptosis signal-regulating kinase 1 (ASK1)-p38

ROS:

Reactive oxygen species

G6PDH:

Glucose 6-phosphate dehydrogenase

GSH:

Glutathione

HMOX1:

Heme oxygenase-1

SQSTM1:

Sequestosome-1

ATF3:

Transcription factor 3

Nrf2:

Nuclear erythroid factor 2

ER:

Endoplasmic reticulum

UPR:

Unfolded protein response

IER1α:

Inositol-requiring protein 1α

XBP1:

Spliced X-box binding protein

SIRT3:

Sirtuin 3

NOXA:

Bcl-2 family proteins

TDAG51:

T-cell death-associated gene 51

MEFs:

Mouse embryonic fibroblasts

IP3R:

Inositol trisphosphate receptor

Cas-9:

Capase9

Apaf-1:

Apoptotic protease activating factor 1

Cas-3:

Capsae3

MPTP:

Mitochondria permeability transition pore

HATs:

Acetyltransferases

HDACs:

Deacetylases

DNMTs:

DNA methyltransferases

HIF-1α:

Hypoxia-inducible factor-1α

HM:

Histone methylation

cytochrome c oxidase:

COX-respiratory complex IV

OXPHOS:

Oxidative phosphorylation

PKM2:

Methylated pyruvate kinase M2

References

  1. Soravia, C., Ashton, B. J., Thornton, A., & Ridley, A. R. (2021). The impacts of heat stress on animal cognition: Implications for adaptation to a changing climate. Wiley Interdisciplinary Reviews: Climate Change, 12(4), e713.

    Google Scholar 

  2. Dutta, S. M., Mustafi, S. B., Raha, S., & Chakraborty, S. K. (2018). Biomonitoring role of some cellular markers during heat stress-induced changes in highly representative fresh water mollusc, Bellamya bengalensis: Implication in climate change and biological adaptation. Ecotoxicology and Environmental Safety, 157, 482–490.

    Article  CAS  PubMed  Google Scholar 

  3. Pecl, G. T., Araújo, M. B., Bell, J. D., Blanchard, J., Bonebrake, T. C., Chen, I. C., & Williams, S. E. (2017). Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science, 355(6332), eaai9214.

    Article  PubMed  Google Scholar 

  4. Solomon, B. D. (2023). Intergovernmental panel on climate change (IPCC). In Dictionary of ecological economics (pp. 302–302). Edward Elgar Publishing.

  5. Gershoni, M. (2023). Transgenerational transmission of environmental effects in livestock in the age of global warming. Cell Stress and Chaperones, 28(5), 445–454.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kok, J. F., Storelvmo, T., Karydis, V. A., Adebiyi, A. A., Mahowald, N. M., Evan, A. T., He, C., & Leung, D. M. (2023). Mineral dust aerosol impacts on global climate and climate change. Nature Reviews Earth & Environment, 4(2), 71–86.

    Article  Google Scholar 

  7. Naaz, F., Samuchiwal, S., Dalvi, V., Bhattacharya, A., Pant, K. K., & Malik, A. (2023). Hydrothermal liquefaction could be a sustainable approach for valorization of wastewater grown algal biomass into cleaner fuel. Energy Conversion and Management, 283, 116887.

    Article  CAS  Google Scholar 

  8. Soravia, C., Ashton, B. J., Thornton, A., & Ridley, A. R. (2021). Investigating the relationship between heat stress and cognition in a wild animal. WIREs Climate Change, 12, e713.

    Article  Google Scholar 

  9. Abdelnour, S. A., Al-Gabri, N. A., Hashem, N. M., & Gonzalez-Bulnes, A. (2021). Supplementation with proline improves haemato-biochemical and reproductive indicators in male rabbits affected by environmental heat-stress. Animals, 11(2), 373.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Taylor, S. K., Minhas, M. H., Tong, J., Selvaganapathy, P. R., Mishra, R. K., & Gupta, B. P. (2021). C. elegans electrotaxis behavior is modulated by heat shock response and unfolded protein response signaling pathways. Scientific Reports, 11, 1–17.

    Article  Google Scholar 

  11. Sejian, V., Bhatta, R., Gaughan, J. B., Dunshea, F. R., & Lacetera, N. (2018). Adaptation of animals to heat stress. Animal, 12(s2), s431–s444.

    Article  CAS  PubMed  Google Scholar 

  12. Seebacher, F., White, C. R., & Franklin, C. E. (2015). Physiological plasticity increases resilience of ectothermic animals to climate change. Nature Climate Change, 5, 61–66.

    Article  Google Scholar 

  13. Pian, A. K., Foong, C. P., & Abd Hamid, R. (2022). S-phase arrest and apoptosis in human breast adenocarcinoma MCF-7 cells via mitochondrial dependent pathway induced by tricyclohexylphosphine gold (I) n-mercaptobenzoate complexes. Life Sciences, 311, 121161.

    Article  CAS  PubMed  Google Scholar 

  14. Wang, Y., Fang, J., Zeng, H.-F., Zhong, J.-F., Li, H.-X., & Chen, K.-L. (2022). Identification and bioinformatics analysis of differentially expressed milk exosomal microRNAs in milk exosomes of heat-stressed Holstein cows. Functional & Integrative Genomics, 22, 77–87.

    Article  CAS  Google Scholar 

  15. Chan, J. Y., Cheng, H.-L., Chou, J. L., Li, F. C., Dai, K.-Y., Chan, S. H., & Chang, A. Y. (2007). Heat shock protein 60 or 70 activates nitric-oxide synthase (NOS) I- and inhibits NOS II-associated signaling and depresses the mitochondrial apoptotic cascade during brain stem death. Journal of Biological Chemistry, 282, 4585–4600.

    Article  CAS  PubMed  Google Scholar 

  16. Elolimy, A., Vailati-Riboni, M., Liang, Y., & Loor, J. J. (2019). Cellular mechanisms and epigenetic changes: Role of nutrition in livestock. Veterinary Clinics: Food Animal Practice, 35, 249–263.

    PubMed  Google Scholar 

  17. Perrella, G., Bäurle, I., & van Zanten, M. (2022). Epigenetic regulation of thermomorphogenesis and heat stress tolerance. New Phytologist, 234, 1144–1160.

    Article  PubMed  Google Scholar 

  18. Ibeagha-Awemu, E. M., & Zhao, X. (2015). Epigenetic marks: Regulators of livestock phenotypes and conceivable sources of missing variation in livestock improvement programs. Frontiers in Genetics, 6, 302.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Yakovlev, A. F. (2018). Epigenetic effects in livestock breeding. Russian Journal of Genetics, 54, 897–909.

    Article  CAS  Google Scholar 

  20. Wang, M., & Ibeagha-Awemu, E. M. (2021). Impacts of epigenetic processes on the health and productivity of livestock. Frontiers in Genetics, 11, 613636.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Waddington, C. H. (1956). Embryology, epigenetics and biogenetics. Nature, 177, 1241–1241.

    Article  Google Scholar 

  22. Waddington, C. H. (1957). The genetic basis of the assimilated bithorax stock. Journal of Genetics, 55, 241–245.

    Article  Google Scholar 

  23. Triantaphyllopoulos, K. A., Ikonomopoulos, I., & Bannister, A. J. (2016). Epigenetics and inheritance of phenotype variation in livestock. Epigenetics & Chromatin, 9, 31.

    Article  Google Scholar 

  24. He, L., Huang, H., Bradai, M., Zhao, C., You, Y., Ma, J., Zhao, L., Lozano-Durán, R., & Zhu, J.-K. (2022). DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development. Nature Communications, 13, 1335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Vinoth, A., Thirunalasundari, T., Shanmugam, M., Uthrakumar, A., Suji, S., & Rajkumar, U. (2018). Evaluation of DNA methylation and mRNA expression of heat shock proteins in thermal manipulated chicken. Cell Stress and Chaperones, 23, 235–252.

    Article  CAS  PubMed  Google Scholar 

  26. Lyon, M. F. (1993). Epigenetic inheritance in mammals. Trends in Genetics, 9, 123–128.

    Article  CAS  PubMed  Google Scholar 

  27. Zhang, X., Wang, D., & Liu, J. (2023). Hypoxia-inducible factor-1α is involved in the response to heat stress in lactating dairy cows. Journal of Thermal Biology, 112, 103460.

    Article  CAS  PubMed  Google Scholar 

  28. Ahmad, S. M., De Donato, M., Bhat, B. A., Diallo, A. B., & Peters, S. O. (2023). Omics technologies in livestock improvement: From selection to breeding decisions. Frontiers in Genetics, 13, 1113417.

  29. Johnson, C. (2023). Epigenetics: A new challenge in the post-genomic era while controversial, epigenetics does appear to offer potentially significant value to livestock genetic programmes. Frontiers in Genetics, 9, 1.

    CAS  Google Scholar 

  30. Capra, E., Lazzari, B., Milanesi, M., Nogueira, G., Garcia, J. F., Utsunomiya, Y., Ajmone-Marsan, P., & Stella, A. (2023). Comparison between indicine and taurine cattle DNA methylation reveals epigenetic variation associated to differences in morphological adaptive traits. Epigenetics. https://doi.org/10.1080/15592294.2022.2163363

    Article  PubMed  PubMed Central  Google Scholar 

  31. Macciotta, N. P. P., Dimauro, C., Degano, L., Vicario, D., & Cesarani, A. (2023). A transgenerational study on the effect of great-granddam birth month on granddaughter EBV for production traits in Italian Simmental cattle. Journal of Dairy Science. https://doi.org/10.3168/jds.2022-22455

    Article  PubMed  Google Scholar 

  32. Hu, J., & Barrett, R. (2017). Epigenetics in natural animal populations. Journal of Evolutionary Biology, 30, 1612–1632.

    Article  CAS  PubMed  Google Scholar 

  33. David, S.-A., Vitorino Carvalho, A., Gimonnet, C., Brionne, A., Hennequet-Antier, C., Piégu, B., Crochet, S., Couroussé, N., Bordeau, T., Bigot, Y., Collin, A., & Coustham, V. (2019). Thermal manipulation during embryogenesis impacts H3K4me3 and H3K27me3 histone marks in chicken hypothalamus. Frontiers in Genetics. https://doi.org/10.3389/fgene.2019.01207

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ghaffari, M. H. (2022). Developmental programming: Prenatal and postnatal consequences of hyperthermia in dairy cows and calves. Domestic Animal Endocrinology, 80, 106723.

    Article  PubMed  Google Scholar 

  35. Riddihough, G., & Pennisi, E. (2001). The evolution of epigenetics (pp. 1063–1063). American Association for the Advancement of Science.

    Google Scholar 

  36. Abdelnour, S. A., Abd El-Hack, M. E., Khafaga, A. F., Arif, M., Taha, A. E., & Noreldin, A. E. (2019). Stress biomarkers and proteomics alteration to thermal stress in ruminants: A review. Journal of Thermal Biology, 79, 120–134.

    Article  CAS  PubMed  Google Scholar 

  37. Abd El-Hack, M. E., Abdelnour, S. A., Swelum, A. A., & Arif, M. (2018). The application of gene marker-assisted selection and proteomics for the best meat quality criteria and body measurements in Qinchuan cattle breed. Molecular Biology Reports, 45, 1445–1456.

    Article  CAS  PubMed  Google Scholar 

  38. Waddington, C. H. (1940). Organisers and genes. https://www.cabidigitallibrary.org/doi/full/10.5555/19412202515

  39. Horowitz, M. (2016). Epigenetics and cytoprotection with heat acclimation. Journal of Applied Physiology, 120, 702–710.

    Article  CAS  PubMed  Google Scholar 

  40. Waddington, C. H. (1956). Embryology, epigenetics and biogenetics. Nature, 177(4522), 1241–1241.

    Article  Google Scholar 

  41. Wang, M., & Ibeagha-Awemu, E. M. (2021). Impacts of epigenetic processes on the health and productivity of livestock. Frontiers in Genetics, 11, 613636.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Xu, P., Lin, H., Jiao, H., Zhao, J., & Wang, X. (2022). Advances in epigenetic mechanisms of chick embryo heat acclimation. World’s Poultry Science Journal, 78, 953–969.

    Article  Google Scholar 

  43. Borges, J. V., de Freitas, B. S., Antoniazzi, V., de Souza dos Santos, C., Vedovelli, K., Pires, V. N., Paludo, L., de Lima, M. N. M., & Bromberg, E. (2019). Social isolation and social support at adulthood affect epigenetic mechanisms, brain-derived neurotrophic factor levels and behavior of chronically stressed rats. Behavioural Brain Research, 366, 36–44.

    Article  Google Scholar 

  44. Norouzitallab, P., Baruah, K., Vandegehuchte, M., Van Stappen, G., Catania, F., Bussche, J. V., Vanhaecke, L., Sorgeloos, P., & Bossier, P. (2014). Environmental heat stress induces epigenetic transgenerational inheritance of robustness in parthenogenetic Artemia model. The FASEB Journal, 28, 3552–3563.

    Article  CAS  PubMed  Google Scholar 

  45. Del Corvo, M., Lazzari, B., Capra, E., Zavarez, L., Milanesi, M., Utsunomiya, Y. T., Utsunomiya, A. T. H., Stella, A., de Paula Nogueira, G., & Garcia, J. F. (2021). Methylome patterns of cattle adaptation to heat stress. Frontiers in Genetics, 12, 633132.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Murray, K. O., Clanton, T. L., & Horowitz, M. (2022). Epigenetic responses to heat: From adaptation to maladaptation. Experimental Physiology, 107, 1144–1158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Islam, S., & Mukherjee, C. (2022). Molecular regulation of hypoxia through the lenses of noncoding RNAs and epitranscriptome. Wiley Interdisciplinary Reviews: RNA, 14, e1750.

    Article  PubMed  Google Scholar 

  48. Pan, J., Wei, Y., Ni, L., Li, X., Deng, Y., Xu, B., Yang, T., Sun, J., & Liu, W. (2022). Unbalanced ER-mitochondrial calcium homeostasis promotes mitochondrial dysfunction and associated apoptotic pathways activation in methylmercury exposed rat cortical neurons. Journal of Biochemical and Molecular Toxicology, 36, e23136.

    Article  CAS  PubMed  Google Scholar 

  49. Paschou, M., Papazafiri, P., Charalampous, C., Zachariadis, M., Dedos, S. G., & Doxakis, E. (2022). Neuronal microRNAs safeguard ER Ca2+ homeostasis and attenuate the unfolded protein response upon stress. Cellular and Molecular Life Sciences, 79, 373.

    Article  CAS  PubMed  Google Scholar 

  50. Nowakowska, M., Gualtieri, F., von Rüden, E.-L., Hansmann, F., Baumgärtner, W., Tipold, A., & Potschka, H. (2020). Profiling the expression of endoplasmic reticulum stress associated heat shock proteins in animal epilepsy models. Neuroscience, 429, 156–172.

    Article  CAS  PubMed  Google Scholar 

  51. Te Pas, M. F. W., Park, W., Srikanth, K., Kumar, H., Kemp, S., Kim, J.-M., Lim, D., Madsen, O., van den Brand, H., & Park, J.-E. (2023). Chapter 12—Transcriptomic and epigenomic network analysis reveals chicken physiological reactions against heat stress. In M. Ajmal Ali & J. Lee (Eds.), Transcriptome profiling (pp. 333–359). Academic Press.

    Chapter  Google Scholar 

  52. Masroor, S., Aalam, M. T., Khan, O., Tanuj, G. N., Gandham, R. K., Dhara, S. K., Gupta, P. K., Mishra, B. P., Dutt, T., Singh, G., & Sajjanar, B. K. (2022). Effect of acute heat shock on stress gene expression and DNA methylation in zebu (Bos indicus) and crossbred (Bos indicus × Bos taurus) dairy cattle. International Journal of Biometeorology, 66, 1797–1809.

    Article  PubMed  Google Scholar 

  53. Raza, S. H. A., Hassanin, A. A., Dhshan, A. I., Abdelnour, S. A., Khan, R., Mei, C., & Zan, L. (2021). In silico genomic and proteomic analyses of three heat shock proteins (HSP70, HSP90-α, and HSP90-β) in even-toed ungulates. Electronic Journal of Biotechnology, 53, 61–70.

    Article  CAS  Google Scholar 

  54. Uçar, E. Ö., Şengelen, A., & Kamalı, E. M. (2023). Hsp27, Hsp60, Hsp70, or Hsp90 depletion enhances the antitumor effects of resveratrol via oxidative and ER stress response in human glioblastoma cells. Biochemical Pharmacology, 208, 115409.

    Article  Google Scholar 

  55. Fanti, L., Piacentini, L., Cappucci, U., Casale, A. M., & Pimpinelli, S. (2017). Canalization by selection of de novo induced mutations. Genetics, 206(4), 1995–2006.

  56. Gore, A. V., Tomins, K. A., Iben, J., Ma, L., Castranova, D., Davis, A. E., Parkhurst, A., Jeffery, W. R., & Weinstein, B. M. (2018). An epigenetic mechanism for cavefish eye degeneration. Nature Ecology & Evolution, 2, 1155–1160.

    Article  Google Scholar 

  57. Alvarado, S., Rajakumar, R., Abouheif, E., & Szyf, M. (2015). Epigenetic variation in the Egfr gene generates quantitative variation in a complex trait in ants. Nature Communications, 6, 6513.

    Article  CAS  PubMed  Google Scholar 

  58. Chen, X., Duan, X., Chong, Q., Li, C., Xiao, H., & Chen, S. (2023). Genome-wide DNA methylation differences between Bos indicus and Bos taurus. Animals, 13, 203.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Ko, M., Bandukwala, H. S., An, J., Lamperti, E. D., Thompson, E. C., Hastie, R., Tsangaratou, A., Rajewsky, K., Koralov, S. B., & Rao, A. (2011). Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proceedings of the National Academy of Sciences, 108(35), 14566–14571.

    Article  CAS  Google Scholar 

  60. Pastor, W. A., Aravind, L., & Rao, A. (2013). TETonic shift: Biological roles of TET proteins in DNA demethylation and transcription. Nature Reviews Molecular Cell Biology, 14(6), 341–356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Williams, K., Christensen, J., Pedersen, M. T., Johansen, J. V., Cloos, P. A., Rappsilber, J., & Helin, K. (2011). TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature, 473(7347), 343–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kisliouk, T., Cramer, T., & Meiri, N. (2017). Methyl CpG level at distal part of heat-shock protein promoter HSP 70 exhibits epigenetic memory for heat stress by modulating recruitment of POU 2F1-associated nucleosome-remodeling deacetylase (Nu RD) complex. Journal of Neurochemistry, 141, 358–372.

    Article  CAS  PubMed  Google Scholar 

  63. Jambhekar, A., Dhall, A., & Shi, Y. (2019). Roles and regulation of histone methylation in animal development. Nature Reviews Molecular Cell Biology, 20, 625–641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Andreu-Vieyra, C. V., Chen, R., Agno, J. E., Glaser, S., Anastassiadis, K., Stewart, A. F., & Matzuk, M. M. (2010). MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biology, 8, e1000453.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Zheng, H.-T., Zhuang, Z.-X., Chen, C.-J., Liao, H.-Y., Chen, H.-L., Hsueh, H.-C., Chen, C.-F., Chen, S.-E., & Huang, S.-Y. (2021). Effects of acute heat stress on protein expression and histone modification in the adrenal gland of male layer-type country chickens. Scientific Reports, 11, 1–13.

    Google Scholar 

  66. Godbole, A. A., Gopalan, S., Nguyen, T.-K., Munden, A. L., Lui, D. S., Fanelli, M. J., Vo, P., Lewis, C. A., Spinelli, J. B., Fazzio, T. G., & Walker, A. K. (2023). S-Adenosylmethionine synthases specify distinct H3K4me3 populations and gene expression patterns during heat stress. eLife, 12, e79511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Özdemir, I., & Steiner, F. A. (2022). Transmission of chromatin states across generations in C. elegans. Seminars in Cell & Developmental Biology. https://doi.org/10.1016/j.semcdb.2021.11.008

    Article  Google Scholar 

  68. Wang, S. Y., Kim, K., O’Brown, Z. K., Levan, A., Dodson, A. E., Kennedy, S. G., Chernoff, C., & Greer, E. L. (2022). Hypoxia induces transgenerational epigenetic inheritance of small RNAs. Cell Reports, 41, 111800.

    Article  CAS  PubMed  Google Scholar 

  69. Raza, S. H. A., Kaster, N., Khan, R., Abdelnour, S. A., El-Hack, M. E. A., Khafaga, A. F., Taha, A., Ohran, H., Swelum, A. A., Schreurs, N. M., & Zan, L. (2020). The role of MicroRNAs in muscle tissue development in beef cattle. Genes, 11, 295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Raza, S. H. A., Abdelnour, S. A., Dhshan, A. I., Hassanin, A. A., Noreldin, A. E., Albadrani, G. M., Abdel-Daim, M. M., Cheng, G., & Zan, L. (2021). Potential role of specific microRNAs in the regulation of thermal stress response in livestock. Journal of Thermal Biology, 96, 102859.

    Article  CAS  PubMed  Google Scholar 

  71. O’Brien, J., Hayder, H., Zayed, Y., & Peng, C. (2018). Overview of microRNA biogenesis, mechanisms of actions, and circulation. Frontiers in Endocrinology, 9, 388354.

    Article  Google Scholar 

  72. Huo, D., Su, F., Yang, H., & Sun, L. (2023). Exosomal microRNAs regulate the heat stress response in sea cucumber Apostichopus japonicus. Ecotoxicology and Environmental Safety, 249, 114419.

    Article  CAS  PubMed  Google Scholar 

  73. Kalluri, R., & LeBleu, V. S. (2020). The biology, function, and biomedical applications of exosomes. Science, 367(6478), eaau6977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Zhang, Y., Liu, Y., Liu, H., & Tang, W. H. (2019). Exosomes: Biogenesis, biologic function and clinical potential. Cell & Bioscience, 9, 1–18.

    Article  Google Scholar 

  75. Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S. D., Gregersen, L. H., Munschauer, M., Loewer, A., Ziebold, U., Landthaler, M., Kocks, C., le Noble, F., & Rajewsky, N. (2013). Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 495(7441), 333–338.

    Article  CAS  PubMed  Google Scholar 

  76. Raza, S. H. A., Wijayanti, D., Pant, S. D., Abdelnour, S. A., Hashem, N. M., Amin, A., Wani, A. K., Prakash, A., Dawood, M. A. O., & Zan, L. (2022). Exploring the physiological roles of circular RNAs in livestock animals. Research in Veterinary Science, 152, 726–735.

    Article  CAS  PubMed  Google Scholar 

  77. Zeng, H., Xia, H., Wang, X., Wang, Y., Fang, J., Li, S., Zhai, Y., & Han, Z. (2023). Comprehensive profiling of ceRNA (circRNA-miRNA-mRNA) networks in hypothalamic-pituitary-mammary gland axis of dairy cows under heat stress. International Journal of Molecular Sciences, 24, 888.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Zeng, H., Li, S., Zhai, Y., Chang, H., & Han, Z. (2023). Preliminary transcriptome analysis of long noncoding RNA in hypothalamic-pituitary-mammary gland axis of dairy cows under heat stress. Biomolecules, 13, 390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Zhang, H., Hu, B., Xiong, J., Chen, T., Xi, Q., Luo, J., Jiang, Q., Sun, J., & Zhang, Y. (2019). Genomewide analysis of circular RNA in pituitaries of normal and heat-stressed sows. BMC Genomics, 20, 1013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Qi, Y., Zhang, L., Guo, Y., Wang, J., Chu, M., Zhang, Y., Guo, J., & Li, Q. (2022). Genome-wide identification and functional prediction of circular RNAs in response to heat stress in Chinese Holstein cows. Animal Biotechnology, 33, 1170–1180.

    Article  CAS  PubMed  Google Scholar 

  81. Abdelnour, S. A., El-Ratel, I. T., Peris, S. I., El-Raghi, A. A., & Fouda, S. F. (2022). Effects of dietary thyme essential oil on blood haematobiochemical, redox status, immunological and reproductive variables of rabbit does exposed to high environmental temperature. Italian Journal of Animal Science, 21, 51–61.

    Article  CAS  Google Scholar 

  82. Saghir, S. A., Al Hroob, A. M., Majrashi, K. A., Jaber, F. A., Abduh, M. S., Al-Gabri, N., Albaqami, N. M., Abdelnour, S. A., Alqhtani, A. H., Abd El-Hack, M. E., Swelum, A. A., & Simal-Gandara, J. (2023). Effects of alginates on the growth, haematological, immunity, antioxidant and pro-inflammatory responses of rabbits under high temperature. Research in Veterinary Science, 155, 36–43.

    Article  CAS  PubMed  Google Scholar 

  83. Lu, R., Hu, J., Liu, X., Yu, L., Hu, J., Jiang, H., Liu, S., Li, M., He, J., & Yang, X. (2023). Mogroside-rich extract from Siraitia grosvenorii fruits protects against heat stress-induced intestinal damage by ameliorating oxidative stress and inflammation in mice. Food & Function. https://doi.org/10.1039/D2FO02179J

    Article  PubMed Central  Google Scholar 

  84. Abdelnour, S. A., Metwally, M. G. E., Bahgat, L. B., & Naiel, M. A. E. (2023). Pumpkin seed oil–supplemented diets promoted the growth productivity, antioxidative capacity, and immune response in heat-stressed growing rabbits. Tropical Animal Health and Production, 55, 55.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Chauhan, S. S., Rashamol, V., Bagath, M., Sejian, V., & Dunshea, F. R. (2021). Impacts of heat stress on immune responses and oxidative stress in farm animals and nutritional strategies for amelioration. International Journal of Biometeorology, 65, 1231–1244.

    Article  PubMed  Google Scholar 

  86. Akin, A. T., Kaymak, E., Ceylan, T., Ozturk, E., Basaran, K. E., Karabulut, D., Ozdamar, S., & Yakan, B. (2022). Chloroquine attenuates chronic hypoxia-induced testicular damage via suppressing endoplasmic reticulum stress and apoptosis in experimental rat model. Clinical and Experimental Pharmacology and Physiology, 49, 813–823.

    Article  CAS  PubMed  Google Scholar 

  87. Gao, P.-C., Wang, A.-Q., Chen, X.-W., Cui, H., Li, Y., & Fan, R.-F. (2023). Selenium alleviates endoplasmic reticulum calcium depletion-induced endoplasmic reticulum stress and apoptosis in chicken myocardium after mercuric chloride exposure. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-023-25970-1

    Article  PubMed  Google Scholar 

  88. Solarz-Andrzejewska, A., Majcher-Maślanka, I., Kryst, J., & Chocyk, A. (2023). Modulation of the endoplasmic reticulum stress and unfolded protein response mitigates the behavioral effects of early-life stress. Pharmacological Reports. https://doi.org/10.1007/s43440-023-00456-6

    Article  PubMed  PubMed Central  Google Scholar 

  89. Miao, Q., Si, X., Xie, Y., Chen, L., Tang, X., & Zhang, H. (2022). Acute heat stress alters the expression of genes and proteins associated with the unfolded protein response pathway in the liver of broilers. British Poultry Science, 63, 125–132.

    Article  CAS  PubMed  Google Scholar 

  90. Beaudoin-Chabot, C., Wang, L., Celik, C., Abdul Khalid, A.T.-F., Thalappilly, S., Xu, S., Koh, J. H., Lim, V. W. X., Low, A. D., & Thibault, G. (2022). The unfolded protein response reverses the effects of glucose on lifespan in chemically-sterilized C. elegans. Nature Communications, 13, 5889.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Sharma, V. K., Stark, M., Fridman, N., Assaraf, Y. G., & Gross, Z. (2022). Doubly stimulated corrole for organelle-selective antitumor cytotoxicity. Journal of Medicinal Chemistry, 65, 6100–6115.

    Article  CAS  PubMed  Google Scholar 

  92. Hu, C., Yang, J., Qi, Z., Wu, H., Wang, B., Zou, F., Mei, H., Liu, J., Wang, W., & Liu, Q. (2022). Heat shock proteins: Biological functions, pathological roles, and therapeutic opportunities. MedComm, 3, e161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Zgajnar, N., Lagadari, M., Gallo, L. I., Piwien-Pilipuk, G., & Galigniana, M. D. (2023). Mitochondrial–nuclear communication by FKBP51 shuttling. Journal of Cellular Biochemistry. https://doi.org/10.1039/D2FO02179J

    Article  PubMed  Google Scholar 

  94. Hu, B., Wang, P., Zhang, S., Liu, W., Lv, X., Shi, D., Zhao, L., Liu, H., Wang, B., Chen, S., & Shao, Z. (2022). HSP70 attenuates compression-induced apoptosis of nucleus pulposus cells by suppressing mitochondrial fission via upregulating the expression of SIRT3. Experimental & Molecular Medicine, 54, 309–323.

    Article  CAS  Google Scholar 

  95. Ritossa, F. (1962). A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia, 18(12), 571–573.

    Article  CAS  Google Scholar 

  96. Pei, Q., Ni, W., Yuan, Y., Yuan, J., Zhang, X., & Yao, M. (2022). HSP70 ameliorates septic lung injury via inhibition of apoptosis by interacting with KANK2. Biomolecules, 12, 410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Du, X., Liu, H., Liu, X., Chen, X., Yuan, L., Ma, Y., Huang, H., Wang, Y., Wang, R., & Zhang, S. (2021). Microcystin-LR induces ovarian injury and apoptosis in mice via activating apoptosis signal-regulating kinase 1-mediated P38/JNK pathway. Ecotoxicology and Environmental Safety, 213, 112066.

    Article  CAS  PubMed  Google Scholar 

  98. Hayashida, N., Inouye, S., Fujimoto, M., Tanaka, Y., Izu, H., Takaki, E., Ichikawa, H., Rho, J., & Nakai, A. (2006). A novel HSF1-mediated death pathway that is suppressed by heat shock proteins. The EMBO Journal, 25, 4773–4783.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Chao, D., Tran, H., Hogan, Q., & Pan, B. (2022). Analgesic dorsal root ganglion field stimulation blocks both afferent and efferent spontaneous activity in sensory neurons of rats with monosodium iodoacetate-induced osteoarthritis. Osteoarthritis and Cartilage, 30, 1468–1481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Park, E.-S., Kim, J., Ha, T.-U., Choi, J.-S., Soo Hong, K., & Rho, J. (2013). TDAG51 deficiency promotes oxidative stress-induced apoptosis through the generation of reactive oxygen species in mouse embryonic fibroblasts. Experimental & Molecular Medicine, 45, e35.

    Article  Google Scholar 

  101. Hsu, Y.-L., Yu, H.-S., Lin, H.-C., Wu, K.-Y., Yang, R.-C., & Kuo, P.-L. (2011). Heat shock induces apoptosis through reactive oxygen species involving mitochondrial and death receptor pathways in corneal cells. Experimental Eye Research, 93, 405–412.

    Article  CAS  PubMed  Google Scholar 

  102. Yao, P. P., Sheng, M. J., Weng, W. H., Long, Y., Liu, H., Chen, L., Lu, J. J., Rong, A., & Li, B. (2019). High glucose causes apoptosis of rabbit corneal epithelial cells involving activation of PERK-eIF2α-CHOP-caspase-12 signaling pathway. International Journal of Ophthalmology, 12, 1815–1822.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Bhandary, B., Marahatta, A., Kim, H.-R., & Chae, H.-J. (2012). An involvement of oxidative stress in endoplasmic reticulum stress and its associated diseases. International Journal of Molecular Sciences, 14, 434–456.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Luna-Ramirez, R. I., Limesand, S. W., Goyal, R., Pendleton, A. L., Rincón, G., Zeng, X., Luna-Nevárez, G., Reyna-Granados, J. R., & Luna-Nevárez, P. (2023). Blood transcriptomic analyses reveal functional pathways associated with thermotolerance in pregnant ewes exposed to environmental heat stress. Genes, 14, 1590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Zhang, B., Sun, H., Sun, Z., Liu, N., Liu, R., & Zhong, Q. (2023). Glutamine alleviated heat stress-induced damage of porcine intestinal epithelium associated with the mitochondrial apoptosis pathway mediated by heat shock protein 70. Journal of Animal Science. https://doi.org/10.1093/jas/skad127

    Article  PubMed  PubMed Central  Google Scholar 

  106. Song, J.-H., Kim, K.-J., Choi, S.-Y., Koh, E.-J., Park, J., & Lee, B.-Y. (2019). Korean ginseng extract ameliorates abnormal immune response through the regulation of inflammatory constituents in Sprague Dawley rat subjected to environmental heat stress. Journal of Ginseng Research, 43, 252–260.

    Article  PubMed  Google Scholar 

  107. Petronis, A., & Petroniene, R. (2000). Epigenetics of inflammatory bowel disease. Gut, 47, 302–306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Hassan, F.-U., Nawaz, A., Rehman, M. S., Ali, M. A., Dilshad, S. M., & Yang, C. (2019). Prospects of HSP70 as a genetic marker for thermo-tolerance and immuno-modulation in animals under climate change scenario. Animal Nutrition, 5, 340–350.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Raza, S. H. A., Khan, R., Abdelnour, S. A., Abd El-Hack, M. E., Khafaga, A. F., Taha, A., Ohran, H., Mei, C., Schreurs, N. M., & Zan, L. (2019). Advances of molecular markers and their application for body variables and carcass traits in Qinchuan cattle. Genes, 10, 717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Guerreiro, E., Giachetto, P., Givisiez, P., Ferro, J., Ferro, M., Gabriel, J. E., Furlan, R. L., & Macari, M. (2004). Brain and hepatic Hsp70 protein levels in heat-acclimated broiler chickens during heat stress. Brazilian Journal of Poultry Science, 6, 201–206.

    Article  Google Scholar 

  111. Gu, L.-L., Li, M.-Z., Wang, G.-R., & Liu, X.-D. (2019). Multigenerational heat acclimation increases thermal tolerance and expression levels of Hsp70 and Hsp90 in the rice leaf folder larvae. Journal of Thermal Biology, 81, 103–109.

    Article  CAS  PubMed  Google Scholar 

  112. Afsal, A., Bagath, M., Sejian, V., Krishnan, G., Beena, V., & Bhatta, R. (2021). Effect of heat stress on HSP70 gene expression pattern in different vital organs of Malabari goats. Biological Rhythm Research, 52, 380–394.

    Article  CAS  Google Scholar 

  113. Badri, T., Alsiddig, M., Lian, L., Cai, Y., & Wang, G. (2021). Single nucleotide polymorphisms in HSP70–1 gene associated with cellular heat tolerance in Chinese Holstein cows. Animal Gene, 20, 200114.

    Article  CAS  Google Scholar 

  114. Tetievsky, A., Assayag, M., Ben-Hamo, R., Efroni, S., Cohen, G., Abbas, A., & Horowitz, M. (2014). Heat acclimation memory: Do the kinetics of the deacclimated transcriptome predispose to rapid reacclimation and cytoprotection? Journal of Applied Physiology (Bethesda, Md.: 1985), 117, 1262–1277.

    Article  CAS  PubMed  Google Scholar 

  115. Radom-Aizik, S., Zaldivar, F. P., Nance, D. M., Haddad, F., Cooper, D. M., & Adams, G. R. (2013). Growth inhibition and compensation in response to neonatal hypoxia in rats. Pediatric Research, 74, 111–120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Gao, J., Zhang, S., Li, B., Wang, Z., Liu, W., & Zhang, L. (2023). Sub-chronic aluminum exposure in rats’ learning-memory capability and hippocampal histone H4 acetylation modification: Effects and mechanisms. Biological Trace Element Research. https://doi.org/10.1007/s12011-023-03602-6

    Article  PubMed  PubMed Central  Google Scholar 

  117. Oellermann, M., Fitzgibbon, Q. P., Twiname, S., & Pecl, G. T. (2022). Metabolic plasticity improves lobster’s resilience to ocean warming but not to climate-driven novel species interactions. Scientific Reports, 12, 4412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Sun, B., Williams, C. M., Li, T., Speakman, J. R., Jin, Z., Lu, H., Luo, L., & Du, W. (2022). Higher metabolic plasticity in temperate compared to tropical lizards suggests increased resilience to climate change. Ecological Monographs, 92, e1512.

    Article  CAS  Google Scholar 

  119. Wang, L., Schumann, U., Liu, Y., Prokopchuk, O., & Steinacker, J. M. (2012). Heat shock protein 70 (Hsp70) inhibits oxidative phosphorylation and compensates ATP balance through enhanced glycolytic activity. Journal of Applied Physiology, 113, 1669–1676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Paital, B., Panda, S. K., Hati, A. K., Mohanty, B., Mohapatra, M. K., Kanungo, S., & Chainy, G. B. (2016). Longevity of animals under reactive oxygen species stress and disease susceptibility due to global warming. World Journal of Biological Chemistry, 7, 110–127.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Bastías-Pérez, M., Zagmutt, S., Soler-Vázquez, M. C., Serra, D., Mera, P., & Herrero, L. (2020). Impact of adaptive thermogenesis in mice on the treatment of obesity. Cells, 9, 316.

    Article  PubMed  PubMed Central  Google Scholar 

  122. Liu, F., Ma, F., Wang, Y., Hao, L., Zeng, H., Jia, C., Wang, Y., Liu, P., Ong, I. M., & Li, B. (2017). PKM2 methylation by CARM1 activates aerobic glycolysis to promote tumorigenesis. Nature Cell Biology, 19, 1358–1370.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

All the authors acknowledge and thank their respective Institutes and Universities.

Funding

This study was funded by the National Beef and Yak Industrial Technology System Project (CARS-37), the Key Research and Development Program of Shaanxi Province (2022NY-050, 2022ZDLNY01-01), Key Project of “Two Chains” Integration of Livestock and Poultry Breeding in Western Shaanxi Province (2022 GD-TSLD-46-0102), Science and Technology Project of the Ministry of Agriculture and Rural Areas (19211178).

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Authors and Affiliations

  1. College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Wang Jianfang, Sayed Haidar Abbas Raza & Linsen Zan

  2. Guangdong Provincial Key Laboratory of Food Quality and Safety/Nation-Local Joint Engineering Research Center for Machining and Safety of Livestock and Poultry Products, South China Agricultural University, Guangzhou, 510642, China

    Sayed Haidar Abbas Raza

  3. Guangdong Provincial Key Laboratory of Utilization and Conservation of Food and Medicinal Resources in Northern Region, Shaoguan University, Shaoguan, 512005, China

    Sayed Haidar Abbas Raza

  4. Gulbali Institute, Charles Sturt University, Wagga Wagga, NSW, 2678, Australia

    Sameer D. Pant

  5. College of Animal Science and Technology, South China Agricultural University, Guangzhou, 510642, China

    Zhao Juan

  6. Department of Biochemistry and Biophysics, University of North Carolina, School of Medicine, Chapel Hill, USA

    Ajit Prakash

  7. Department of Animal Production, Faculty of Agriculture, Zagazig University, Zagazig, 44519, Egypt

    Sameh A. Abdelnour

  8. Biology Department, Faculty of Science, University of Ha’il, Ha’il, Saudi Arabia

    Bandar Hamad Aloufi

  9. Department of Animal Production, School of Agriculture, University of Jordan, Amman, Jordan

    Zeinab M. H. Mahasneh

  10. Department of Animal Production, Faculty of Agriculture, Cairo University, Giza, Egypt

    Ahmed A. Amin

  11. Hanwoo Research Institute, National Institute of Animal Science, Pyeongchang-gun, 25340, Republic of Korea

    Borhan Shokrollahi

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  1. Wang Jianfang
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Contributions

Wang Jianfang, Sayed Haidar Abbas Raza: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Writing—original draft, Writing—review & editing. Sameer D. Pant, Zhao Juan, Ajit Prakash: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Writing—review & editing. Sameh A. Abdelnour, Bandar Hamad Aloufi, Zeinab M. H. Mahasneh: Conceptualization, Data curation, Formal analysis, Methodology, Software, Validation, Writing—review & editing. Formal analysis, Writing—review & editing. Data curation, Formal analysis. Borhan Shokrollahi: Writing—review & editing. Ahmed A. Amin: Software, Methodology, Visualization. Software, Methodology, Visualization. Borhan Shokrollahi: Writing—review & editing. Software, Methodology. Linsen Zan: Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Visualization, Writing—review & editing. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Linsen Zan.

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Jianfang, W., Raza, S.H.A., Pant, S.D. et al. Exploring Epigenetic and Genetic Modulation in Animal Responses to Thermal Stress. Mol Biotechnol (2024). https://doi.org/10.1007/s12033-024-01126-5

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