[en] Heat stress implies unfavorable effects on primary and functional traits in dairy cattle and, in consequence, on the profitability of the whole production system. The increasing number of days with extreme hot temperatures suggests that it is imperative to detect the heat stress status of animals based on adequate measures. However, confirming the heat stress status of an individual is still challenging, and, in consequence, the identification of novel heat stress biomarkers, including molecular biomarkers, remains a very relevant issue. Currently, it is known that heat stress seems to have unfavorable effects on immune system mechanisms, but this information is of limited use in the context of heat stress phenotyping. In addition, there is a lack of knowledge addressing the molecular mechanisms linking the relevant genes to the observed phenotype. In this review, we explored the potential molecular mechanisms explaining how heat stress affects the immune system and, therefore, increases the occurrence of immune-related diseases in cattle. In this regard, 2 relatively opposite hypotheses are under focus: the immunosuppressive action of cortisol, and the proinflammatory effect of heat stress. In both hypotheses, the modulation of the immune response during heat stress is highlighted. Moreover, it is possible to link candidate genes to these potential mechanisms. In this context, immune markers are very valuable indicators for the detection of heat stress in dairy cattle, broadening the portfolio of potential biomarkers for heat stress.
F.R.S.-FNRS - Fonds de la Recherche Scientifique ULiège - Université de Liège Interreg North-West Europe SPW - Service Public de Wallonie DFG - Deutsche Forschungsgemeinschaft
Funding text :
Sven König and Katharina May acknowledge funding from the German National Science Foundation (DFG, Bonn, Germany), through grant number KO 3520/8-1. Nicolas Gengler and Pauline Lemal acknowledge the INTERREG NWE HappyMoo project, grant agreement NWE 730, co-financed by the Walloon Government (Service Public de Wallonie, Namur, Belgium). Pauline Lemal acknowledges her special scholarship of the University of Liège–Gembloux Agro-Bio Tech (Gembloux, Belgium) and Katrien Wijnrocx ((University of Liège, Gembloux Agro-Bio Tech, Gembloux, Belgium) for her proofreading and her daily help. Nicolas Gengler, as a former senior research associate, acknowledges the support of the National Fund for Scientific Research (Brussels, Belgium) also through grant number T.W005.23 (WEAVE-DFG “HTwoTHI”). Because no human or animal subjects were used, this analysis did not require approval by an Institutional Animal Care and Use Committee or Institutional Review Board. The authors have not stated any conflicts of interest.
Abbas, A.K., Lichtman, A.H., Pillai, S., Baker, D.L., Baker, A., Cellular and Molecular Immunology. 9th ed., 2018, Elsevier.
Ahlawat, S., Arora, R., Sharma, U., Sharma, A., Girdhar, Y., Sharma, R., Kumar, A., Vijh, R.K., Comparative gene expression profiling of milk somatic cells of Sahiwal cattle and Murrah buffaloes. Gene, 764, 2021, 145101 https://doi.org/10.1016/j.gene.2020.145101 32877747.
Alhussien, M.N., Dang, A.K., Impact of different seasons on the milk somatic and differential cell counts, milk cortisol and neutrophils functionality of three Indian native breeds of cattle. J. Therm. Biol. 78 (2018), 27–35 https://doi.org/10.1016/j.jtherbio.2018.08.020 30509646.
Almeida, R.A., Kerro-Dego, O., Rius, A.G., Effect of heat stress on the interaction of Streptococcus uberis with bovine mammary epithelial cells. J. Dairy Res. 85 (2018), 53–56 https://doi.org/10.1017/S0022029917000875 29468999.
Amin, R., Bhat, G.R., Ahmad, A., Swain, P., Arunakumari, G., Understanding patho-physiology of retained placenta and its management in cattle: A review. Vet. Med. Sci. 1 (2013), 1–9.
Archana, P.R., Aleena, J., Pragna, P., Vidya, M.K., Niyas, A.P.A., Bagath, M., Krishnan, G., Manimaran, A., Beena, V., Kurien, E.K., Sejian, V., Bhatta, R., Role of heat shock proteins in livestock adaptation to heat stress. J. Dairy Vet. Anim. Res., 5, 2017, 00127 https://doi.org/10.15406/jdvar.2017.05.00127.
Arlt, W., Stewart, P.M., Adrenal corticosteroid biosynthesis, metabolism, and action. Endocrinol. Metab. Clin. North Am. 34 (2005), 293–313 https://doi.org/10.1016/j.ecl.2005.01.002 15850843.
Bagath, M., Krishnan, G., Devaraj, C., Rashamol, V.P., Pragna, P., Lees, A.M., Sejian, V., The impact of heat stress on the immune system in dairy cattle: A review. Res. Vet. Sci. 126 (2019), 94–102 https://doi.org/10.1016/j.rvsc.2019.08.011 31445399.
Belhadj Slimen, I., Najar, T., Ghram, A., Abdrrabba, M., Heat stress effects on livestock: Molecular, cellular and metabolic aspects, a review. J. Anim. Physiol. Anim. Nutr. (Berl.) 100 (2016), 401–412 https://doi.org/10.1111/jpn.12379 26250521.
Bharati, J., Dangi, S.S., Bag, S., Maurya, V.P., Singh, G., Kumar, P., Sarkar, M., Expression dynamics of HSP90 and nitric oxide synthase (NOS) isoforms during heat stress acclimation in Tharparkar cattle. Int. J. Biometeorol. 61 (2017), 1461–1469 https://doi.org/10.1007/s00484-017-1323-3 28265771.
Billing, A.M., Fack, F., Turner, J.D., Muller, C.P., Cortisol is a potent modulator of lipopolysaccharide-induced interferon signaling in macrophages. Innate Immun. 17 (2011), 302–320 https://doi.org/10.1177/1753425910369269 20501517.
Billings, E.A., Lee, C.S., Owen, K.A., D'Souza, R.S., Ravichandran, K.S., Casanova, J.E., The adhesion GPCR BAI1 mediates macrophage ROS production and microbicidal activity against Gram-negative bacteria. Sci. Signal., 9, 2016 https://doi.org/10.1126/scisignal.aac6250 26838550.
Bohlouli, M., Halli, K., Yin, T., Gengler, N., König, S., Genome-wide associations for heat stress response suggest potential candidate genes underlying milk fatty acid composition in dairy cattle. J. Dairy Sci. 105 (2022), 3323–3340 https://doi.org/10.3168/jds.2021-21152 35094857.
Bronzo, V., Lopreiato, V., Riva, F., Amadori, M., Curone, G., Addis, M.F., Cremonesi, P., Moroni, P., Trevisi, E., Castiglioni, B., The role of innate immune response and microbiome in resilience of dairy cattle to disease: The mastitis model. Animals (Basel), 10, 2020, 1397 https://doi.org/10.3390/ani10081397 32796642.
Burton, J.L., Kehrli, M.E. Jr., Kapil, S., Horst, R.L., Regulation of L-selectin and CD18 on bovine neutrophils by glucocorticoids: Effects of cortisol and dexamethasone. J. Leukoc. Biol. 57 (1995), 317–325 https://doi.org/10.1002/jlb.57.2.317 7531748.
Cannarile, L., Delfino, D.V., Adorisio, S., Riccardi, C., Ayroldi, E., Implicating the role of GILZ in glucocorticoid modulation of T-cell activation. Front. Immunol., 10, 2019, 1823 https://doi.org/10.3389/fimmu.2019.01823 31440237.
Carroll, J.A., Forsberg, N.E., Influence of stress and nutrition on cattle immunity. Vet. Clin. North Am. Food Anim. Pract. 23 (2007), 105–149 https://doi.org/10.1016/j.cvfa.2007.01.003 17382844.
Cartwright, S.L., McKechnie, M., Schmied, J., Livernois, A.M., Mallard, B.A., Effect of in vitro heat stress challenge on the function of blood mononuclear cells from dairy cattle ranked as high, average and low immune responders. BMC Vet. Res., 17, 2021, 233 https://doi.org/10.1186/s12917-021-02940-8 34210328.
Catozzi, C., Ávila, G., Zamarian, V., Pravettoni, D., Sala, G., Ceciliani, F., Lacetera, N., Lecchi, C., In vitro effect of heat stress on bovine monocytes lifespan and polarization. Immunobiology, 225, 2020, 151888 https://doi.org/10.1016/j.imbio.2019.11.023 31843259.
Chaudhry, A., Rudra, D., Treuting, P., Samstein, R.M., Liang, Y., Kas, A., Rudensky, A.Y., CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 326 (2009), 986–991 https://doi.org/10.1126/science.1172702 19797626.
Chen, L., Flies, D.B., Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 13 (2013), 227–242 https://doi.org/10.1038/nri3405 23470321.
Chen, S., Wang, J., Peng, D., Li, G., Chen, J., Gu, X., Exposure to heat-stress environment affects the physiology, circulation levels of cytokines, and microbiome in dairy cows. Sci. Rep., 8, 2018, 14606 https://doi.org/10.1038/s41598-018-32886-1 30279428.
Chen, Y.-J., Hsieh, M.-Y., Chang, M.Y., Chen, H.-C., Jan, M.-S., Maa, M.-C., Leu, T.-H., Eps8 protein facilitates phagocytosis by increasing TLR4-MyD88 protein interaction in lipopolysaccharide-stimulated macrophages. J. Biol. Chem. 287 (2012), 18806–18819 https://doi.org/10.1074/jbc.M112.340935 22493489.
Cheng, W.N., Han, S.G., Bovine mastitis: Risk factors, therapeutic strategies, and alternative treatments—A review. Asian-Australas. J. Anim. Sci. 33 (2020), 1699–1713 https://doi.org/10.5713/ajas.20.0156 32777908.
Cheruiyot, E.K., Haile-Mariam, M., Cocks, B.G., MacLeod, I.M., Xiang, R., Pryce, J.E., New loci and neuronal pathways for resilience to heat stress in cattle. Sci. Rep., 11, 2021, 16619 https://doi.org/10.1038/s41598-021-95816-8 34404823.
Chung, S., Son, G.H., Kim, K., Circadian rhythm of adrenal glucocorticoid: Its regulation and clinical implications. Biochim. Biophys. Acta. 1812 (2011), 581–591 https://doi.org/10.1016/j.bbadis.2011.02.003 21320597.
Collier, R.J., Collier, J.L., Rhoads, R.P., Baumgard, L.H., Invited review: Genes involved in the bovine heat stress response. J. Dairy Sci. 91 (2008), 445–454 https://doi.org/10.3168/jds.2007-0540 18218730.
Contreras, G.A., Sordillo, L.M., Lipid mobilization and inflammatory responses during the transition period of dairy cows. Comp. Immunol. Microbiol. Infect. Dis. 34 (2011), 281–289 https://doi.org/10.1016/j.cimid.2011.01.004 21316109.
Cruz-Topete, D., Cidlowski, J.A., One hormone, two actions: Anti- and pro-inflammatory effects of glucocorticoids. Neuroimmunomodulation 22 (2015), 20–32 https://doi.org/10.1159/000362724 25227506.
Czech, B., Szyda, J., Wang, K., Luo, H., Wang, Y., Fecal microbiota and their association with heat stress in Bos taurus. BMC Microbiol., 22, 2022, 171 https://doi.org/10.1186/s12866-022-02576-0 35790909.
Dahl, G.E., Tao, S., Laporta, J., Heat stress impacts immune status in cows across the life cycle. Front. Vet. Sci., 7, 2020, 116 https://doi.org/10.3389/fvets.2020.00116 32211430.
Davidson, B.D., Dado-Senn, B., Ouellet, V., Dahl, G.E., Laporta, J., Effect of late-gestation heat stress in nulliparous heifers on postnatal growth, passive transfer of immunoglobulin G, and thermoregulation of their calves. JDS Commun. 2 (2021), 165–169 https://doi.org/10.3168/jdsc.2020-0069 36339508.
Diaz-Jimenez, D., Kolb, J.P., Cidlowski, J.A., Glucocorticoids as regulators of macrophage-mediated tissue homeostasis. Front. Immunol., 12, 2021, 669891 https://doi.org/10.3389/fimmu.2021.669891 34079551.
Dikmen, S., Cole, J.B., Null, D.J., Hansen, P.J., Genome-wide association mapping for identification of quantitative trait loci for rectal temperature during heat stress in Holstein cattle. PLoS One, 8, 2013, e69202 https://doi.org/10.1371/journal.pone.0069202 23935954.
Dikmen, S., Hansen, P.J., Is the temperature-humidity index the best indicator of heat stress in lactating dairy cows in a subtropical environment?. J. Dairy Sci. 92 (2009), 109–116 https://doi.org/10.3168/jds.2008-1370 19109269.
Edwards, P.T., Smith, B.P., McArthur, M.L., Hazel, S.J., Fearful Fido: Investigating dog experience in the veterinary context in an effort to reduce distress. Appl. Anim. Behav. Sci. 213 (2019), 14–25 https://doi.org/10.1016/j.applanim.2019.02.009.
Elvinger, F., Hansen, P.J., Natzke, R.P., Modulation of function of bovine polymorphonuclear leukocytes and lymphocytes by high temperature in vitro and in vivo. Am. J. Vet. Res. 52 (1991), 1692–1698 1662922.
Fayad, T., Lefebvre, R., Nimpf, J., Silversides, D.W., Lussier, J.G., Low-density lipoprotein receptor-related protein 8 (LRP8) is upregulated in granulosa cells of bovine dominant follicle: Molecular characterization and spatio-temporal expression studies. Biol. Reprod. 76 (2007), 466–475 https://doi.org/10.1095/biolreprod.106.057216 17108332.
Feher, J., The adrenal cortex. Quantitative Human Physiology: An Introduction, 2012, Academic Press, 810–819 https://doi.org/10.1016/B978-0-12-382163-8.00088-8.
Fontoura, A.B.P., Javaid, A., Sáinz de la Maza-Escolà, V., Salandy, N.S., Fubini, S.L., Grilli, E., McFadden, J.W., Heat stress develops with increased total-tract gut permeability, and dietary organic acid and pure botanical supplementation partly restores lactation performance in Holstein dairy cows. J. Dairy Sci. 105 (2022), 7842–7860 https://doi.org/10.3168/jds.2022-21820 35931486.
Frittoli, E., Matteoli, G., Palamidessi, A., Mazzini, E., Maddaluno, L., Disanza, A., Yang, C., Svitkina, T., Rescigno, M., Scita, G., The signaling adaptor Eps8 is an essential actin capping protein for dendritic cell migration. Immunity 35 (2011), 388–399 https://doi.org/10.1016/j.immuni.2011.07.007 21835647.
Furze, R.C., Rankin, S.M., Neutrophil mobilization and clearance in the bone marrow. Immunology 125 (2008), 281–288 https://doi.org/10.1111/j.1365-2567.2008.02950.x 19128361.
Galac, S., Kool, M.M.J., Naan, E.C., Daminet, S., Mol, J.A., Kooistra, H.S., Expression of the ACTH receptor, steroidogenic acute regulatory protein, and steroidogenic enzymes in canine cortisol-secreting adrenocortical tumors. Domest. Anim. Endocrinol. 39 (2010), 259–267 https://doi.org/10.1016/j.domaniend.2010.07.001 20920783.
Gao, S.T., Ma, L., Zhou, Z., Zhou, Z.K., Baumgard, L.H., Jiang, D., Bionaz, M., Bu, D.P., Heat stress negatively affects the transcriptome related to overall metabolism and milk protein synthesis in mammary tissue of midlactating dairy cows. Physiol. Genomics 51 (2019), 400–409 https://doi.org/10.1152/physiolgenomics.00039.2019 31298615.
Garner, J.B., Chamberlain, A.J., Vander Jagt, C., Nguyen, T.T.T., Mason, B.A., Marett, L.C., Leury, B.J., Wales, W.J., Hayes, B.J., Gene expression of the heat stress response in bovine peripheral white blood cells and milk somatic cells in vivo. Sci. Rep., 10, 2020, 19181 https://doi.org/10.1038/s41598-020-75438-2 33154392.
Gregg, R.K., Implications of microgravity-induced cell signaling alterations upon cancer cell growth, invasiveness, metastatic potential, and control by host immunity. Int. Rev. Cell Mol. Biol. 361 (2021), 107–164 https://doi.org/10.1016/bs.ircmb.2021.01.004.
Guerriero, V., Raynes, D.A., Synthesis of heat stress proteins in lymphocytes from livestock. J. Anim. Sci., 68, 1990, 2779 https://doi.org/10.2527/1990.6892779x 2211407.
Halli, K., Vanvanhossou, S.F., Bohlouli, M., König, S., Yin, T., Identification of candidate genes on the basis of SNP by time-lagged heat stress interactions for milk production traits in German Holstein cattle. PLoS One, 16, 2021, e0258216 https://doi.org/10.1371/journal.pone.0258216 34648531.
Hamel, J., Zhang, Y., Wente, N., Krömker, V., Heat stress and cow factors affect bacteria shedding pattern from naturally infected mammary gland quarters in dairy cattle. J. Dairy Sci. 104 (2021), 786–794 https://doi.org/10.3168/jds.2020-19091 33189273.
Hammami, H., Vandenplas, J., Vanrobays, M.-L., Rekik, B., Bastin, C., Gengler, N., Genetic analysis of heat stress effects on yield traits, udder health, and fatty acids of Walloon Holstein cows. J. Dairy Sci. 98 (2015), 4956–4968 https://doi.org/10.3168/jds.2014-9148 25958288.
Hamza, T., Barnett, J.B., Li, B., Interleukin 12 a key immunoregulatory cytokine in infection applications. Int. J. Mol. Sci. 11 (2010), 789–806 https://doi.org/10.3390/ijms11030789 20479986.
Haselager, M.V., Kater, A.P., Eldering, E., Proliferative signals in chronic lymphocytic leukemia; What are we missing?. Front. Oncol., 10, 2020, 592205 https://doi.org/10.3389/fonc.2020.592205 33134182.
Hayes, B.J., Bowman, P.J., Chamberlain, A.J., Savin, K., van Tassell, C.P., Sonstegard, T.S., Goddard, M.E., A validated genome wide association study to breed cattle adapted to an environment altered by climate change. PLoS One, 4, 2009, e6676 https://doi.org/10.1371/journal.pone.0006676 19688089.
Herbut, P., Angrecka, S., Walczak, J., Environmental parameters to assessing of heat stress in dairy cattle—A review. Int. J. Biometeorol. 62 (2018), 2089–2097 https://doi.org/10.1007/s00484-018-1629-9 30368680.
Hirsch, G., Lavoie-Lamoureux, A., Beauchamp, G., Lavoie, J.-P., Neutrophils are not less sensitive than other blood leukocytes to the genomic effects of glucocorticoids. PLoS One, 7, 2012, e44606 https://doi.org/10.1371/journal.pone.0044606 22984532.
Howard, J.T., Kachman, S.D., Snelling, W.M., Pollak, E.J., Ciobanu, D.C., Kuehn, L.A., Spangler, M.L., Beef cattle body temperature during climatic stress: A genome-wide association study. Int. J. Biometeorol. 58 (2014), 1665–1672 https://doi.org/10.1007/s00484-013-0773-5 24362770.
Hsiao, C.C., van der Poel, M., van Ham, T.J., Hamann, J., Macrophages do not express the phagocytic receptor BAI1/ADGRB1. Front. Immunol., 10, 2019, 962 https://doi.org/10.3389/fimmu.2019.00962 31130954.
Hunter, P., The inflammation theory of disease: The growing realization that chronic inflammation is crucial in many diseases opens new avenues for treatment. EMBO Rep. 13 (2012), 968–970 https://doi.org/10.1038/embor.2012.142 23044824.
Inbaraj, S., Sejian, V., Bagath, M., Bhatta, R., Impact of heat stress on immune responses of livestock: A review. Pertanika, J. Trop. Agric. Sci. 39 (2016), 459–482.
Infante-Duarte, C., Kamradt, T., Th1/Th2 balance in infection. Springer Seminars in Immunopathology 21 (1999), 317–338 https://doi.org/10.1007/BF00812260 10666776.
Jee, H., Size dependent classification of heat shock proteins: A mini-review. J. Exerc. Rehabil. 12 (2016), 255–259 https://doi.org/10.12965/jer.1632642.321 27656620.
Johnson, J.D., Fleshner, M., Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J. Leukoc. Biol. 79 (2006), 425–434 https://doi.org/10.1189/jlb.0905523 16387837.
Joo, S.S., Lee, S.J., Park, D.S., Kim, D.H., Gu, B.-H., Park, Y.J., Rim, C.Y., Kim, M., Kim, E.T., Changes in blood metabolites and immune cells in Holstein and Jersey dairy cows by heat stress. Animals (Basel), 11, 2021, 974 https://doi.org/10.3390/ani11040974 33807443.
Kadzere, C.T., Murphy, M.R., Silanikove, N., Maltz, E., Heat stress in lactating dairy cows: A review. Livest. Prod. Sci. 77 (2002), 59–91 https://doi.org/10.1016/S0301-6226(01)00330-X.
Kapila, N., Sharma, A., Kishore, A., Sodhi, M., Tripathi, P.K., Mohanty, A.K., Mukesh, M., Impact of heat stress on cellular and transcriptional adaptation of mammary epithelial cells in riverine buffalo (Bubalus bubalis). PLoS One, 11, 2016, e0157237 https://doi.org/10.1371/journal.pone.0157237 27682256.
Khan, A., Dou, J., Wang, Y., Jiang, X., Khan, M.Z., Luo, H., Usman, T., Zhu, H., Evaluation of heat stress effects on cellular and transcriptional adaptation of bovine granulosa cells. J. Anim. Sci. Biotechnol., 11, 2020, 25 https://doi.org/10.1186/s40104-019-0408-8 32095238.
Kim, W.-S., Ghassemi Nejad, J., Roh, S.-G., Lee, H.-G., Heat-shock proteins gene expression in peripheral blood mononuclear cells as an indicator of heat stress in beef calves. Animals (Basel), 10, 2020, 895 https://doi.org/10.3390/ani10050895 32455563.
Kim, E.T., Joo, S.S., Kim, D.H., Gu, B.-H., Park, D.S., Atikur, R.M., Son, J.K., Park, B.Y., Kim, S.B., Hur, T.-Y., Kim, M., Common and differential dynamics of the function of peripheral blood mononuclear cells between Holstein and Jersey cows in heat-stress environment. Animals (Basel), 11, 2020, 19 https://doi.org/10.3390/ani11010019 33374309.
Kim, S.H., Ramos, S.C., Valencia, R.A., Cho, Y.I., Lee, S.S., Heat stress: Effects on rumen microbes and host physiology, and strategies to alleviate the negative impacts on lactating dairy cows. Front. Microbiol., 13, 2022, 804562 https://doi.org/10.3389/fmicb.2022.804562 35295316.
Koch, F., Thom, U., Albrecht, E., Weikard, R., Nolte, W., Kuhla, B., Kuehn, C., Heat stress directly impairs gut integrity and recruits distinct immune cell populations into the bovine intestine. Proc. Natl. Acad. Sci. USA 116 (2019), 10333–10338 https://doi.org/10.1073/pnas.1820130116 31064871.
König, S., May, K., Invited review: Phenotyping strategies and quantitative-genetic background of resistance, tolerance and resilience associated traits in dairy cattle. Animal 13 (2019), 897–908 https://doi.org/10.1017/S1751731118003208 30523776.
Krawczyk, C., Penninger, J.M., Molecular motors involved in T cell receptor clusterings. J. Leukoc. Biol. 69 (2001), 317–330 https://doi.org/10.1189/jlb.69.3.317 11261777.
Kruk, J., Kotarska, K., Aboul-Enein, B.H., Physical exercise and catecholamines response: Benefits and health risk: Possible mechanisms. Free Radic. Res. 54 (2020), 105–125 https://doi.org/10.1080/10715762.2020.1726343 32020819.
Kwek, S.S., Cha, E., Fong, L., Unmasking the immune recognition of prostate cancer with CTLA4 blockade. Nat. Rev. Cancer 12 (2012), 289–297 https://doi.org/10.1038/nrc3223 22378189.
Lacetera, N., Impact of climate change on animal health and welfare. Anim. Front. 9 (2018), 26–31 https://doi.org/10.1093/af/vfy030 32002236.
Lacetera, N., Bernabucci, U., Scalia, D., Basiricò, L., Morera, P., Nardone, A., Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. J. Dairy Sci. 89 (2006), 4606–4612 https://doi.org/10.3168/jds.S0022-0302(06)72510-3 17106092.
Lacetera, N., Bernabucci, U., Scalia, D., Ronchi, B., Kuzminsky, G., Nardone, A., Lymphocyte functions in dairy cows in hot environment. Int. J. Biometeorol. 50 (2005), 105–110 https://doi.org/10.1007/s00484-005-0273-3 15991017.
Lau, D., Mollnau, H., Eiserich, J.P., Freeman, B.A., Daiber, A., Gehling, U.M., Brümmer, J., Rudolph, V., Münzel, T., Heitzer, T., Meinertz, T., Baldus, S., Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins. Proc. Natl. Acad. Sci. USA 102 (2005), 431–436 https://doi.org/10.1073/pnas.0405193102 15625114.
Lecchi, C., Rota, N., Vitali, A., Ceciliani, F., Lacetera, N., In vitro assessment of the effects of temperature on phagocytosis, reactive oxygen species production and apoptosis in bovine polymorphonuclear cells. Vet. Immunol. Immunopathol. 182 (2016), 89–94 https://doi.org/10.1016/j.vetimm.2016.10.007 27863557.
Lefcourt, A.M., Bitman, J., Kahl, S., Wood, D.L., Circadian and ultradian rhythms of peripheral cortisol concentrations in lactating dairy cows. J. Dairy Sci. 76 (1993), 2607–2612 https://doi.org/10.3168/jds.S0022-0302(93)77595-5 8227661.
Lendez, P.A., Martinez Cuesta, L., Nieto Farias, M.V., Vater, A.A., Ghezzi, M.D., Mota-Rojas, D., Dolcini, G.L., Ceriani, M.C., Alterations in TNF-α and its receptors expression in cows undergoing heat stress. Vet. Immunol. Immunopathol., 235, 2021, 110232 https://doi.org/10.1016/j.vetimm.2021.110232 33799007.
Ley, K., Integration of inflammatory signals by rolling neutrophils. Immunol. Rev. 186 (2002), 8–18 https://doi.org/10.1034/j.1600-065X.2002.18602.x 12234358.
Li, Q., Wang, B., Mu, K., Zhang, J., The pathogenesis of thyroid autoimmune diseases: New T lymphocytes—Cytokines circuits beyond the Th1–Th2 paradigm. J. Cell. Physiol. 234 (2019), 2204–2216 https://doi.org/10.1002/jcp.27180 30246383.
Li, Q.-L., Ju, Z.-H., Huang, J.-M., Li, J.-B., Li, R.-L., Hou, M.-H., Wang, C.-F., Zhong, J.-F., Two novel SNPs in HSF1 gene are associated with thermal tolerance traits in Chinese Holstein cattle. DNA Cell Biol. 30 (2011), 247–254 https://doi.org/10.1089/dna.2010.1133 21189066.
Löwenberg, M., Verhaar, A.P., van den Brink, G.R., Hommes, D.W., Glucocorticoid signaling: A nongenomic mechanism for T-cell immunosuppression. Trends Mol. Med. 13 (2007), 158–163 https://doi.org/10.1016/j.molmed.2007.02.001 17293163.
Luo, H., Hu, L., Brito, L.F., Dou, J., Sammad, A., Chang, Y., Ma, L., Guo, G., Liu, L., Zhai, L., Xu, Q., Wang, Y., Weighted single-step GWAS and RNA sequencing reveals key candidate genes associated with physiological indicators of heat stress in Holstein cattle. J. Anim. Sci. Biotechnol., 13, 2022, 108 https://doi.org/10.1186/s40104-022-00748-6 35986427.
Luo, H., Li, X., Hu, L., Xu, W., Chu, Q., Liu, A., Guo, G., Liu, L., Brito, L.F., Wang, Y., Genomic analyses and biological validation of candidate genes for rectal temperature as an indicator of heat stress in Holstein cattle. J. Dairy Sci. 104 (2021), 4441–4451 https://doi.org/10.3168/jds.2020-18725 33589260.
Macciotta, N.P.P., Biffani, S., Bernabucci, U., Lacetera, N., Vitali, A., Ajmone-Marsan, P., Nardone, A., Derivation and genome-wide association study of a principal component-based measure of heat tolerance in dairy cattle. J. Dairy Sci. 100 (2017), 4683–4697 https://doi.org/10.3168/jds.2016-12249 28365122.
Maciuszek, M., Klak, K., Rydz, L., Verburg-van Kemenade, B.M.L., Chadzinska, M., Cortisol metabolism in carp macrophages: A role for macrophage-derived cortisol in M1/M2 polarization. Int. J. Mol. Sci., 21, 2020, 8954 https://doi.org/10.3390/ijms21238954 33255713.
Mani, V., Weber, T.E., Baumgard, L.H., Gabler, N.K., Growth and Development Symposium: Endotoxin, inflammation, and intestinal function in livestock. J. Anim. Sci. 90 (2012), 1452–1465 https://doi.org/10.2527/jas.2011-4627 22247110.
Martínez, R.S., Palladino, R.A., Banchero, G., Fernández-Martín, R., Nanni, M., Juliano, N., Iorio, J., La Manna, A., Providing heat-stress abatement to late-lactation Holstein cows affects hormones, metabolite blood profiles, and hepatic gene expression but not productive responses. Appl. Anim. Sci. 37 (2021), 490–503 https://doi.org/10.15232/aas.2020-02109.
Menta, P.R., Machado, V.S., Piñeiro, J.M., Thatcher, W.W., Santos, J.E.P., Vieira-Neto, A., Heat stress during the transition period is associated with impaired production, reproduction, and survival in dairy cows. J. Dairy Sci. 105 (2022), 4474–4489 https://doi.org/10.3168/jds.2021-21185 35282913.
Mishra, S.R., Behavioural, physiological, neuro-endocrine and molecular responses of cattle against heat stress: An updated review. Trop. Anim. Health Prod., 53, 2021, 400 https://doi.org/10.1007/s11250-021-02790-4 34255188.
Monteiro, A.P.A., Tao, S., Thompson, I.M., Dahl, G.E., Effect of heat stress during late gestation on immune function and growth performance of calves: Isolation of altered colostral and calf factors. J. Dairy Sci. 97 (2014), 6426–6439 https://doi.org/10.3168/jds.2013-7891 25108869.
Most, M.S., Yates, D.T., Inflammatory mediation of heat stress-induced growth deficits in livestock and its potential role as a target for nutritional interventions: A review. Animals (Basel), 11, 2021, 3539 https://doi.org/10.3390/ani11123539 34944316.
Möstl, E., Maggs, J.L., Schrötter, G., Besenfelder, U., Palme, R., Measurement of cortisol metabolites in faeces of ruminants. Vet. Res. Commun. 26 (2002), 127–139 https://doi.org/10.1023/A:1014095618125 11922482.
Nguyen, T.T., Bowman, P.J., Haile-Mariam, M., Pryce, J.E., Hayes, B.J., Genomic selection for tolerance to heat stress in Australian dairy cattle. J. Dairy Sci. 99 (2016), 2849–2862 https://doi.org/10.3168/jds.2015-9685 27037467.
Nicolaides, N. C., G. Chrousos, and T. Kino. 2020. Glucocorticoid receptor. In Endotext. K. R. Feingold, B. Anawalt, M. R. Blackman, ed. MDText.com. Accessed Apr. 13, 2023. https://www.ncbi.nlm.nih.gov/books/NBK279171/.
Niedzielska, M., Bodendorfer, B., Münch, S., Eichner, A., Derigs, M., da Costa, O., Schweizer, A., Neff, F., Nitschke, L., Sparwasser, T., Keyse, S.M., Lang, R., Gene trap mice reveal an essential function of dual specificity phosphatase Dusp16/MKP-7 in perinatal survival and regulation of toll-like receptor (TLR)-induced cytokine production. J. Biol. Chem. 289 (2014), 2112–2126 https://doi.org/10.1074/jbc.M113.535245 24311790.
Ohms, M., Möller, S., Laskay, T., An attempt to polarize human neutrophils toward N1 and N2 phenotypes in vitro. Front. Immunol., 11, 2020, 532 https://doi.org/10.3389/fimmu.2020.00532 32411122.
Otto, P.I., Guimarães, S.E.F., Verardo, L.L., Azevedo, A.L.S., Vandenplas, J., Sevillano, C.A., Marques, D.B.D., Pires, M., de Freitas, C., Verneque, R.S., Martins, M.F., Panetto, J.C.C., Carvalho, W.A., Gobo, D.O.R., da Silva, M.V.G.B., Machado, M.A., Genome-wide association studies for heat stress response in Bos taurus × Bos indicus crossbred cattle. J. Dairy Sci. 102 (2019), 8148–8158 https://doi.org/10.3168/jds.2018-15305 31279558.
Owen, D.R., Fan, J., Campioli, E., Venugopal, S., Midzak, A., Daly, E., Harlay, A., Issop, L., Libri, V., Kalogiannopoulou, D., Oliver, E., Gallego-Colon, E., Colasanti, A., Huson, L., Rabiner, E.A., Suppiah, P., Essagian, C., Matthews, P.M., Papadopoulos, V., TSPO mutations in rats and a human polymorphism impair the rate of steroid synthesis. Biochem. J. 474 (2017), 3985–3999 https://doi.org/10.1042/BCJ20170648 29074640.
Pandey, P., Hooda, O.K., Kumar, S., Impact of heat stress and hypercapnia on physiological, hematological, and behavioral profile of Tharparkar and Karan Fries heifers. Vet. World 10 (2017), 1149–1155 https://doi.org/10.14202/vetworld.2017.1149-1155 29062208.
Park, D.S., Gu, B.-H., Park, Y.J., Joo, S.S., Lee, S.-S., Kim, S.-H., Kim, E.T., Kim, D.H., Lee, S.S., Lee, S.J., Kim, B.-W., Kim, M., Dynamic changes in blood immune cell composition and function in Holstein and Jersey steers in response to heat stress. Cell Stress Chaperones 26 (2021), 705–720 https://doi.org/10.1007/s12192-021-01216-2 34080136.
Patra, A.K., Kar, I., Heat stress on microbiota composition, barrier integrity, and nutrient transport in gut, production performance, and its amelioration in farm animals. J. Anim. Sci. Technol. 63 (2021), 211–247 https://doi.org/10.5187/jast.2021.e48 33987600.
Rakib, M.R.H., Zhou, M., Xu, S., Liu, Y., Khan, M.A., Han, B., Gao, J., Effect of heat stress on udder health of dairy cows. J. Dairy Res. 87 (2020), 315–321 https://doi.org/10.1017/S0022029920000886.
Rees, A., Fischer-Tenhagen, C., Heuwieser, W., Effect of heat stress on concentrations of faecal cortisol metabolites in dairy cows. Reprod. Domest. Anim. 51 (2016), 392–399 https://doi.org/10.1111/rda.12691 27091101.
Ricci, E., Ronchetti, S., Gabrielli, E., Pericolini, E., Gentili, M., Roselletti, E., Vecchiarelli, A., Riccardi, C., GILZ restrains neutrophil activation by inhibiting the MAPK pathway. J. Leukoc. Biol. 105 (2019), 187–194 https://doi.org/10.1002/JLB.3AB0718-255R 30371949.
Ronchetti, S., Ricci, E., Migliorati, G., Gentili, M., Riccardi, C., How glucocorticoids affect the neutrophil life. Int. J. Mol. Sci., 19, 2018, 4090 https://doi.org/10.3390/ijms19124090 30563002.
Rong, Y., Zeng, M., Guan, X., Qu, K., Liu, J., Zhang, J., Chen, H., Huang, B., Lei, C., Association of HSF1 genetic variation with heat tolerance in Chinese cattle. Animals (Basel), 9, 2019, 1027 https://doi.org/10.3390/ani9121027 31775331.
Salak-Johnson, J.L., McGlone, J.J., Making sense of apparently conflicting data: Stress and immunity in swine and cattle. J. Anim. Sci. 85:Suppl. 13 (2007), E81–E88 https://doi.org/10.2527/jas.2006-538 17085721.
Salama, A.A.K., Duque, M., Wang, L., Shahzad, K., Olivera, M., Loor, J.J., Enhanced supply of methionine or arginine alters mechanistic target of rapamycin signaling proteins, messenger RNA, and microRNA abundance in heat-stressed bovine mammary epithelial cells in vitro. J. Dairy Sci. 102 (2019), 2469–2480 https://doi.org/10.3168/jds.2018-15219 30639019.
Sanchez-Bermejo, E., Zhu, W., Tasset, C., Eimer, H., Sureshkumar, S., Singh, R., Sundaramoorthi, V., Colling, L., Balasubramanian, S., Genetic architecture of natural variation in thermal responses of Arabidopsis. Plant Physiol. 169 (2015), 647–659 https://doi.org/10.1104/pp.15.00942 26195568.
Schmidt, S., Rainer, J., Ploner, C., Presul, E., Riml, S., Kofler, R., Glucocorticoid-induced apoptosis and glucocorticoid resistance: Molecular mechanisms and clinical relevance. Cell Death Differ. 11:Suppl. 1 (2004), S45–S55 https://doi.org/10.1038/sj.cdd.4401456 15243581.
Selvaraj, V., Stocco, D.M., Tu, L.N., Minireview: Translocator protein (TSPO) and steroidogenesis: A reappraisal. Mol. Endocrinol. 29 (2015), 490–501 https://doi.org/10.1210/me.2015-1033 25730708.
Shodell, M., Shah, K., Siegal, F.P., Circulating human plasmacytoid dendritic cells are highly sensitive to corticosteroid administration. Lupus 12 (2003), 222–230 https://doi.org/10.1191/0961203303lu362xx 12708787.
Sigdel, A., Abdollahi-Arpanahi, R., Aguilar, I., Peñagaricano, F., Whole genome mapping reveals novel genes and pathways involved in milk production under heat stress in US Holstein cows. Front. Genet., 10, 2019, 928 https://doi.org/10.3389/fgene.2019.00928 31636656.
Sigdel, A., Liu, L., Abdollahi-Arpanahi, R., Aguilar, I., Peñagaricano, F., Genetic dissection of reproductive performance of dairy cows under heat stress. Anim. Genet. 51 (2020), 511–520 https://doi.org/10.1111/age.12943 32363588.
Singh, J., Murray, R.D., Mshelia, G., Woldehiwet, Z., The immune status of the bovine uterus during the peripartum period. Vet. J. 175 (2008), 301–309 https://doi.org/10.1016/j.tvjl.2007.02.003 17400489.
Sölzer, N., May, K., Yin, T., König, S., Genomic analyses of claw disorders in Holstein cows: Genetic parameters, trait associations, and genome-wide associations considering interactions of SNP and heat stress. J. Dairy Sci. 105 (2022), 8218–8236 https://doi.org/10.3168/jds.2022-22087 36028345.
Somal, A., Aggarwal, A., Upadhyay, R.C., Effect of thermal stress on expression profile of apoptosis related genes in peripheral blood mononuclear cells of transition Sahiwal cow. Iran. J. Vet. Res. 16 (2015), 137–143 27175165.
Srikanth, K., Kwon, A., Lee, E., Chung, H., Characterization of genes and pathways that respond to heat stress in Holstein calves through transcriptome analysis. Cell Stress Chaperones 22 (2017), 29–42 10.1007/s12192-016-0739-8.
Stevens, A., White, A., ACTH: Cellular peptide hormone synthesis and secretory pathways. Rehfeld, J.F., Bundgaard, J.R., (eds.) Cellular Peptide Hormone Synthesis and Secretory Pathways, 2010, Springer, 63–84.
Stocki, P., Wang, X.N., Dickinson, A.M., Inducible heat shock protein 70 reduces T cell responses and stimulatory capacity of monocyte-derived dendritic cells. J. Biol. Chem. 287 (2012), 12387–12394 https://doi.org/10.1074/jbc.M111.307579 22334699.
Tejaswi, V., Balachander, B., Samad, H.A., Sarkar, M., Maurya, V.P., Singh, G., Assessment of heat stress induced alterations in polymorphonuclear (PMN) cell activity in native and crossbred cows. J. Appl. Anim. Res. 48 (2020), 549–552 https://doi.org/10.1080/09712119.2020.1829629.
Tejaswi, V., Balamurugan, B., Samad, H.A., Sarkar, M., Maurya, V.P., Singh, G., Short communication: Differential endocrine and antioxidant responses to heat stress among native and crossbred cattle. J. Vet. Behav. 39 (2020), 1–5 https://doi.org/10.1016/j.jveb.2020.06.001.
Thiriet, M., Mitogen-activated protein kinase module. Intracellular Signaling Mediators in the Circulatory and Ventilatory Systems, 2013, Springer, 311–378.
Thompson, I.M.T., Tao, S., Monteiro, A.P.A., Jeong, K.C., Dahl, G.E., Effect of cooling during the dry period on immune response after Streptococcus uberis intramammary infection challenge of dairy cows. J. Dairy Sci. 97 (2014), 7426–7436 https://doi.org/10.3168/jds.2013-7621 25459905.
Torres-Farfan, C., Abarzua-Catalan, L., Valenzuela, F.J., Mendez, N., Richter, H.G., Valenzuela, G.J., Serón-Ferré, M., Cryptochrome 2 expression level is critical for adrenocorticotropin stimulation of cortisol production in the capuchin monkey adrenal. Endocrinology 150 (2009), 2717–2722 https://doi.org/10.1210/en.2008-1683 19246533.
Toscano, M.A., Commodaro, A.G., Ilarregui, J.M., Bianco, G.A., Liberman, A., Serra, H.M., Hirabayashi, J., Rizzo, L.V., Rabinovich, G.A., Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses. J. Immunol. 176 (2006), 6323–6332 https://doi.org/10.4049/jimmunol.176.10.6323 16670344.
Tugal, D., Liao, X., Jain, M.K., Transcriptional control of macrophage polarization. Arterioscler. Thromb. Vasc. Biol. 33 (2013), 1135–1144 https://doi.org/10.1161/ATVBAHA.113.301453 23640482.
Uzhachenko, R.V., Shanker, A., CD8+ T lymphocyte and NK cell network: Circuitry in the cytotoxic domain of immunity. Front. Immunol., 10, 2019, 1906 https://doi.org/10.3389/fimmu.2019.01906 31456803.
Vatrella, A., Fabozzi, I., Calabrese, C., Maselli, R., Pelaia, G., Dupilumab: A novel treatment for asthma. J. Asthma Allergy, 7, 2014, 123 https://doi.org/10.2147/JAA.S52387 25214796.
Waeber, G., Delplanque, J., Bonny, C., Mooser, V., Steinmann, M., Widmann, C., Maillard, A., Miklossy, J., Dina, C., Hani, E.H., The gene MAPK8IP1, encoding islet-brain-1, is a candidate for type 2 diabetes. Nat. Genet. 24 (2000), 291–295 https://doi.org/10.1038/73523 10700186.
Walsh, K.P., Mills, K.H.G., Dendritic cells and other innate determinants of T helper cell polarisation. Trends Immunol. 34 (2013), 521–530 https://doi.org/10.1016/j.it.2013.07.006 23973621.
Welsh, M.D., Cunningham, R.T., Corbett, D.M., Girvin, R.M., McNair, J., Skuce, R.A., Bryson, D.G., Pollock, J.M., Influence of pathological progression on the balance between cellular and humoral immune responses in bovine tuberculosis. Immunology 114 (2005), 101–111 https://doi.org/10.1111/j.1365-2567.2004.02003.x 15606800.
Widdison, S., Coffey, T.J., Cattle and chemokines: Evidence for species-specific evolution of the bovine chemokine system. Anim. Genet. 42 (2011), 341–353 https://doi.org/10.1111/j.1365-2052.2011.02200.x 21749416.
Willoughby, E.A., Perkins, G.R., Collins, M.K., Whitmarsh, A.J., The JNK-interacting protein-1 scaffold protein targets MAPK phosphatase-7 to dephosphorylate JNK. J. Biol. Chem. 278 (2003), 10731–10736 https://doi.org/10.1074/jbc.M207324200 12524447.
Xavier, A.M., Anunciato, A.K.O., Rosenstock, T.R., Glezer, I., Gene expression control by glucocorticoid receptors during innate immune responses. Front. Endocrinol. (Lausanne), 7, 2016 https://doi.org/10.3389/fendo.2016.00031 27148162.
Young, R., Bush, S.J., Lefevre, L., McCulloch, M.E.B., Lisowski, Z.M., Muriuki, C., Waddell, L.A., Sauter, K.A., Pridans, C., Clark, E.L., Hume, D.A., Species-specific transcriptional regulation of genes involved in nitric oxide production and arginine metabolism in macrophages. Immunohorizons 2 (2018), 27–37 https://doi.org/10.4049/immunohorizons.1700073 30467554.
