Abstract
Animal geneticists and breeders have the impending challenge of enhancing the resilience of Indian livestock to heat stress through better selection strategies. Climate change’s impact on livestock is more intense in tropical countries like India where dairy cattle crossbreeds are more sensitive to heat stress. The main reason for this study was to find the missing relative changes in transcript levels in thermo-neutral and heat stress conditions in crossbred cattle through whole-transcriptome analysis of RNA-Seq data. Differentially expressed genes (DEGs) identified based on the minimum log twofold change value and false discovery rate 0.05 revealed 468 up-regulated genes and 2273 down-regulated significant genes. Functional annotation and pathway analysis of these significant DEGs were compared based on Gene Ontology (Biological process), Kyoto Encyclopedia of Genes and Genome (KEGG), and Reactome pathways using g: Profiler, ShinyGO v0.76, and iDEP.951 web tools. On finding network visualization, the most over-represented and correlated pathways were neuronal and sensory organ development, calcium signalling pathway, Mitogen-activated protein kinase (MAPK) and Smad signalling pathway, Ras-proximate-1, or Ras-related protein 1 (Rap 1) signalling pathway, apoptosis, and oxidative stress. Similarly, down-regulated genes were most expressed in mRNA processing, immune system, B-cell receptor signalling pathway, Nucleotide oligomerization domain (NOD)-like receptors (NLRs) signalling pathway and nonsense-mediated decay (NMD) pathway. The heat stress-responsive genes identified in this study will facilitate our understanding of the molecular basis for climate resilience and heat tolerance in Indian dairy crossbreeds.
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References
20th Livestock Census (2019) (https://dahd.nic.in/documents/statistics/livestock-census)
Akbarinejad V, Gharagozlou F, Vojgani M (2017) Temporal effect of maternal heat stress during gestation on the fertility and anti-Müllerian hormone concentration of offspring in bovine. Theriogenology 99:69–78
Amaral CDS, Correa GRE, Serrano Mujica LK, Fiorenza MF, Rosa SG, Nogueira CW, Portela VM, Comim FV, Schoenau W, Smirnova NP, Antoniazzi AQ (2021) Heat stress modulates polymorphonuclear cell response in early pregnancy cows: I. interferon pathway and oxidative stress. Plos one 16(9):e0257418
Andrews S, Krueger F, Segonds-Pichon A, Biggins L, Krueger C, Wingett S (2010) FastQC. A quality control tool for high throughput sequence data, p 370
Bader GD, Hogue CW (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4(1):1–27
BAHS (2019) (https://dahd.nic.in/circulars/basic-animal-husbandry-statistics-2019)
Bebbere D, Arav A, Nieddu SM, Burrai GP, Succu S, Patrizio P, Ledda S (2021) Molecular and histological evaluation of sheep ovarian tissue subjected to lyophilization. Animals 11(12):3407
Bernabucci U, Biffani S, Buggiotti L, Vitali A, Lacetera N, Nardone A (2014) The effects of heat stress in Italian Holstein dairy cattle. J Dairy Sci 97(1):471–486
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinform 34(17):i884–i890
Chin CH, Chen SH, Wu HH, Ho CW, Ko MT, Lin CY (2014) cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol 8(4):1–7
Council NR (1971) A guide to environmental research on animals. National Academies: Washington, DC, USA
De Rensis F, Scaramuzzi RJ (2003) Heat stress and seasonal effects on reproduction in the dairy cow—a review. Theriogenology 60(6):1139–1151
Deb R, Sengar GS (2021) Comparative miRNA signatures among Sahiwal and Frieswal cattle breeds during summer stress. 3 Biotech 11(2):1–10
Dikmen S, Cole JB, Null DJ, Hansen PJ (2013) Genome-wide association mapping for identification of quantitative trait loci for rectal temperature during heat stress in Holstein cattle. PLoS One 8:e69202. https://doi.org/10.1371/journal.pone.0069202
Dikmen S, Wang XZ, Ortega MS, Cole JB, Null DJ, Hansen PJ (2015) Single nucleotide polymorphisms associated with thermoregulation in lactating dairy cows exposed to heat stress. J Anim Breeding Genet = Zeitschrift fur Tierzuchtung und Zuchtungsbiologie 132(6):409–419. https://doi.org/10.1111/jbg.12176
Doyle JL, Berry DP, Veerkamp RF, Carthy TR, Evans RD, Walsh SW, Purfield DC (2020) Genomic regions associated with muscularity in beef cattle differ in five contrasting cattle breeds. Genet Sel Evol 52:1–18
Ewels P, Magnusson M, Lundin S, Käller M (2016) MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32(19):3047–3048
Flick K, Kaiser P (2012) Protein degradation and the stress response. In Semin Cell Dev Biol 23(5):515–522
Ge SX, Jung D, Yao R (2020) ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics 36(8):2628–2629. https://doi.org/10.1093/bioinformatics/btz931
Ge SX, Son EW, Yao R (2018) iDEP: an integrated web application for differential expression and pathway analysis of RNA-Seq data. BMC Bioinformatics 19:534. https://doi.org/10.1186/s12859-018-2486-6
Goetz AE, Wilkinson M (2017) Stress and the nonsense-mediated RNA decay pathway. Cell Mol Life Sci 74:3509–3531
Goodale BC, Rayack EJ, Stanton BA (2017) Arsenic alters transcriptional responses to Pseudomonas aeruginosa infection and decreases antimicrobial defense of human airway epithelial cells. Toxicol Appl Pharmacol 331:154–163
Gupta M, Kumar S, Dangi SS, Jangir BL (2013) Physiological, biochemical, and molecular responses to thermal stress in goats. Int J Livest Res 3(2):27–38
Gurnani M, Sethi RK, Nagarcenkar R (1986) Development of Karan Fries cattle at NDRI, Karnal. Dairy Inf Bull 3:1–2
Hahn GL (1999) Dynamic responses of cattle to thermal heat loads. J Anim Sci 77(suppl_2):10–20
Han C, Alkhater R, Froukh T, Minassian AG, Galati M, Liu RH, McPherson PS (2016) Epileptic encephalopathy caused by mutations in the guanine nucleotide exchange factor DENND5A. Am J Hum Genet 99(6):1359–1367
Hao Y, Cui Y, Gu X (2016) Genome-wide DNA methylation profiles changes associated with constant heat stress in pigs as measured by bisulfite sequencing. Sci Rep 6(1):1–13
He P, Talukder MH, Gao F (2020) Oxidative stress and microvessel barrier dysfunction. Front Physiol 11:472
He B, Chen D, Zhang X, Yang R, Yang Y, Chen P, Shen Z (2022) Oxidative Stress and Ginsenosides: An Update on the Molecular Mechanisms. Oxid Med Cell Longev 20(2022):9299574
Heffler M, Golubovskaya VM, Conroy J, Liu S, Wang D, Cance WG, Dunn KB (2013) FAK and HAS inhibition synergistically decreased colon cancer cell viability and affect expression of critical genes. Anti-Cancer Agents Med Chem (Formerly Current Medicinal Chemistry-Anti-Cancer Agents) 13(4):584–594
Herbut P, Angrecka S, Walczak J (2018) Environmental parameters to assessing of heat stress in dairy cattle—a review. Int J Biometeorol 62:2089–2097. https://doi.org/10.1007/s00484-018-1629-9
Hirunsai M, Srikuea R, Yimlamai T (2015) Heat stress promotes extracellular matrix remodelling via TGF-β 1 and MMP-2/TIMP-2 modulation in tenotomised soleus and plantaris muscles. Int J Hyperthermia 31(4):336–348
Howard JT, Kachman SD, Snelling WM, Pollak EJ, Ciobanu DC, Kuehn LA, Spangler ML (2014) Beef cattle body temperature during climatic stress: a genome-wide association study. Int J Biometeorol 58(7):1665–1672. https://doi.org/10.1007/s00484-013-0773-5
Hu ZL, Park CA, Fritz ER, Reecy JM (2010) QTLdb: A comprehensive database tool building bridges between genotypes and phenotypes. In: Proceedings of the 9th world congress on genetics applied to livestock production, pp 1–6
Hu ZL, Park CA, Wu XL, Reecy JM (2013) Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era. Nucleic Acids Res 41(D1):D871–D879
Huang D, Wang Y, Xu L, Chen L, Cheng M, Shi W, Luo S (2018) GLI2 promotes cell proliferation and migration through transcriptional activation of ARHGEF16 in human glioma cells. J Exp Clin Cancer Res 37(1):1–17
Hulsegge I, Woelders H, Smits M, Schokker D, Jiang L, Sørensen P (2013) Prioritization of candidate genes for cattle reproductive traits, based on protein-protein interactions, gene expression, and text-mining. Physiol Genomics 45(10):400–406
Jalmi SK, Sinha AK (2015) ROS mediated MAPK signalling in abiotic and biotic stress- striking similarities and differences. Front Plant Sci 6:769. https://doi.org/10.3389/fpls.2015.00769
Jitprasutwit S, Ong C, Juntawieng N, Ooi WF, Hemsley CM, Vattanaviboon P, Korbsrisate S (2014) Transcriptional profiles of Burkholderiapseudomallei reveal the direct and indirect roles of Sigma E under oxidative stress conditions. BMC Genomics 15(1):1–11
Kadzere CT, Murphy MR, Silanikove N, Maltz E (2002) Heat stress in lactating dairy cows: a review. Livest Prod Sci 77(1):59–91
Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M (2021) KEGG: integrating viruses and cellular organisms. Nucleic Acids Res 49(D1):D545–D551. https://doi.org/10.1093/nar/gkaa970
Khan RIN, Sahu AR, Malla WA, Praharaj MR, Hosamani N, Kumar S, Tiwari AK (2021) Systems biology under heat stress in Indian cattle. Gene 805:145908
Khudyakov JI, Champagne CD, Meneghetti LM, Crocker DE (2017) Blubber transcriptome response to acute stress axis activation involves transient changes in adipogenesis and lipolysis in a fasting-adapted marine mammal. Sci Rep 7(1):1–12
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37(8):907–915
Kim J, Hanotte O, Mwai OA, Dessie T, Bashir S, Diallo B (2017) The genome landscape of indigenous African cattle. Genome Biol 18:34. https://doi.org/10.1186/s13059-017-1153-y
Kim J, Han KY, Khanna N, Ha T, Belmont AS (2019) Nuclear speckle fusion via long-range directional motion regulates speckle morphology after transcriptional inhibition. J Cell Sci 132(8):jcs226563
Kolli V, Upadhyay RC, Singh D (2014) Peripheral blood leukocytes transcriptomic signature highlights the altered metabolic pathways by heat stress in zebu cattle. Res Vet Sci 96(1):102–110
Lacoste A, De Cian MC, Cueff A, Poulet SA (2001) Noradrenaline and α-adrenergic signalling induce the hsp70 gene promoter in mollusc immune cells. J Cell Sci 114(19):3557–3564
Lakhani P, Kumar P, Lakhani N, Naif Alhussien M (2020) The influence of tropical thermal stress on the seasonal and diurnal variations in the physiological and oxidative status of Karan Fries heifers. Biol Rhythm Res 51(6):837–846
Laufer H, Schwed-Gross A, Neugebauer KM, Shav-Tal Y (2019) Uncoupling of nucleo-cytoplasmic RNA export and localization during stress. Nucleic Acids Res 47(9):4778–4797
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li HB, Liu YA, Gu ZT, Li L, Liu YS, Wang L et al (2018) p38 MAPK-MK2 pathway regulates the heat-stress-induced accumulation of reactive oxygen species that mediates apoptotic cell death in glial cells. Onco Lett 15:775–782. https://doi.org/10.3892/ol.2017.7360
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general-purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7):923–930
Liu RM, Desai LP (2015) Reciprocal regulation of TGF-β and reactive oxygen species: a perverse cycle for fibrosis. Redox Biol 6:565–577. https://doi.org/10.1016/j.redox.2015.09.009
Liu YX, Zhou X, Li DQ, Cui QW, Wang GL (2010) Association of ATP1A1 gene polymorphism with heat tolerance traits in dairy cattle. Genet Mol Res: GMR 9(2):891–896. https://doi.org/10.4238/vol9-2gmr769
Liu D, Chen Z, Zhao W, Guo L, Sun H, Zhu K, Pan Y (2021) Genome-wide selection signatures detection in Shanghai Holstein cattle population identified genes related to adaption, health, and reproduction traits. BMC Genomics 22(1):1–19
Logan CA, Somero GN (2011) Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am J Physiol Regul Integr Comp Physiol 300:R1373–R1383. https://doi.org/10.1152/ajpregu.00689.2010
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):1–21
Lu X, Duan A, Liang S, Ma X, Deng T (2020) Genomic identification, evolution, and expression analysis of collagen genes family in water buffalo during lactation. Genes 11(5):515
Luo W, Brouwer C (2013) Pathview: An R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics 29(14):1830–1831. https://doi.org/10.1093/bioinformatics/btt285
Luo H, Li X, Hu L, Xu W, Chu Q, Liu A (2021) Genomic analyses and biological validation of candidate genes for rectal temperature as an indicator of heat stress in Holstein cattle. J Dairy Sci 104:4441–4451. https://doi.org/10.3168/jds.2020-18725
Luo H, Hu L, Brito LF, Dou J, Sammad A, Chang Y (2022) 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 13:108. https://doi.org/10.1186/s40104-022-00748-6
Luo H, Xu W, Liu A, Li X, Liu L, Wang Y (2018) Genome-wide association study for rectal temperature in chinese holstein population. In: Proceedings of the World Congress on Genetics Applied to Livestock Production, p 587
Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63(2):599–616
Macciotta NPP, Biffani S, Bernabucci U, Lacetera N, Vitali A, Ajmone-Marsan P, Nardone A (2017) Derivation and genome-wide association study of a principal component-based measure of heat tolerance in dairy cattle. J Dairy Sci 100(6):4683–4697. https://doi.org/10.3168/jds.2016-12249
Nagao K, Togawa N, Fujii K, Uchikawa H, Kohno Y, Yamada M, Miyashita T (2005) Detecting tissue-specific alternative splicing and disease-associated aberrant splicing of the PTCH gene with exon junction microarrays. Hum Mol Genet 14(22):3379–3388
Nakashima T, Ishii T, Tagaya H, Seike T, Nakagawa H, Kanda Y, Akinaga S, Soga S, Shiotsu Y (2010) New molecular and biological mechanism of antitumor activities of KW-2478, a novel nonansamycin heat shock protein 90 inhibitor, in multiple myeloma cells. Clin Cancer Res 16(10):2792–2802
Nayan V, Onteru SK, Singh D (2012) Genomic technologies: a way forward for learning climate resilience through cellular responses to heat stress. Climate Resilient Livestock & Production System 1(5)
Nayan V, Singh K, Iquebal MA, Jaiswal S, Bhardwaj A, Singh C, Bhatia T, Kumar S, Singh R, Swaroop MN, Kumar R (2022) Genome-wide DNA methylation and its effect on gene expression during subclinical mastitis in water buffalo. Front Genet 13:828292
Okado-Matsumoto A, Fridovich I (2002) Amyotrophic lateral sclerosis: a proposed mechanism. Proc Natl Acad Sci 99(13):9010–9014
Orzheshkovskyi VV, Trishchynska MA (2019) Ceruloplasmin: Its role in the physiological and pathological processes. Neurophysiology 51:141–149
Osei-Amponsah R, Chauhan SS, Leury BJ, Cheng L, Cullen B, Clarke IJ, Dunshea FR (2019) Genetic selection for thermotolerance in ruminants. Animals 9(11):948
Otto PI, Guimarães SEF, Verardo LL, Azevedo ALS, Vandenplas J, Sevillano CA (2019) Genome-wide association studies for heat stress response in Bos taurus×Bos indicus crossbred cattle. J Dairy Sci 102:8148–8158. https://doi.org/10.3168/jds.2018-15305
Paredes-Sánchez FA, Sifuentes-Rincón AM, Casas E, Arellano-Vera W, Parra-Bracamonte GM, Riley DG, Randel RD (2020) Novel genes involved in the genetic architecture of temperament in Brahman cattle. PLoS One 15(8):e0237825
Park S (2017) Adhesion-controlled proliferation revealing anti-cancer drug resistance of breast cancer cells. Biophys J 112(3):122a–123a
Pocknee BR (2007) The impact of heat stress on mastitis. In British Mastitis Conference 2007, Warwickshire, UK, 10th October 2007. Institute of Animal Health, pp 43–52
Pragna P, Archana PR, Aleena J, Sejian V, Krishnan G, Bagath M, Manimaran A, Beena V, Kurien EK, Varma G and Bhatta R (2017) Heat stress and dairy cow: impact on both milk yield and composition. Int J Dairy Sci 12:1–11
Ranjbar MM, Yousefi AR, Motedayen MH, Molazadeh S, Karimi G (2022) Disease prevention, genetic selection, and vaccination based on BoLA-DRB3. 2 polymorphism: a model for immunogenetic studies. Journal of Advanced Biomedical Sciences 12(1):1–11
Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, Vilo J (2019) g: Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update) Nucleic Acids Res. https://doi.org/10.1093/nar/gkz369
Reimand J, Isserlin R, Voisin V, Kucera M, Tannus-Lopes C, Rostamianfar A, Wadi L, Meyer M, Wong J, Xu C, Merico D (2019) Pathway enrichment analysis and visualization of omics data using g: Profiler, GSEA, Cytoscape and EnrichmentMap. Nat Protoc 14(2):482–517
Ren Y, Cowan RG, Harman RM, Quirk SM (2009) Dominant activation of the hedgehog signaling pathway in the ovary alters theca development and prevents ovulation. Mol Endocrinol 23(5):711–723
Ryu KY, Maehr R, Gilchrist CA, Long MA, Bouley DM, Mueller B, Ploegh HL, Kopito RR (2007) The mouse polyubiquitin gene UbC is essential for fetal liver development, cell‐cycle progression and stress tolerance. EMBO J 26(11):2693–2706
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504
Sharma A, Mandal DK, Singh U (2013) Development of synthetic breeds/strains of cattle for milk. sustainable utilization of indigenous animal genetic resources of India, p 46
Shiota Y, Nozaki T, Bonell F, Murakami S, Shinjo T, Suzuki Y (2012) Induction of coherent magnetization switching in a few atomic layers of FeCo using voltage pulses. Nat Mater 11(1):39–43
Sigdel A, Abdollahi-Arpanahi R, Aguilar I, Peñagaricano F (2019) Whole genome mapping reveals novel genes and pathways involved in milk production under heat stress in US Holstein cows. Front Genet 10:928
Singh K, Bhattacharyya NK (1991) Thermosensitivity of Bos indicus cattle and their F1, crosses with three breeds of Bos taurus. Anim Sci 52(1):57–65
Singh S, Brocker C, Koppaka V, Chen Y, Jackson BC, Matsumoto A, Thompson DC, Vasiliou V (2013) Aldehyde dehydrogenases in cellular responses to oxidative/electrophilicstress. Free Radic Biol Med 56:89–101
Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K, Tignor M, Miller H (2007) IPCC fourth assessment report (AR4). Clim Change 374
Srikanth K, Lee E, Kwan A, Lim Y, Lee J, Jang G, Chung H (2017) Transcriptome analysis and identification of significantly differentially expressed genes in Holstein calves subjected to severe thermal stress. Int J Biometeorol 61:1993–2008
St-Pierre NR, Cobanov B, Schnitkey G (2003) Economic losses from heat stress by US livestock industries. J Dairy Sci 86:E52–E77
Tang M, Miyamoto Y, Huang EJ (2009) Multiple roles of β-catenin in controlling the neurogenic niche for midbrain dopamine neurons. Development 136:2027–2038
Tang X, Meng Q, Gao J, Zhang S, Zhang H, Zhang M (2015) Label-free quantitative analysis of changes in broiler liver proteins under heat stress using SWATH-MS technology. Sci Rep 5(1):15119
Tong DL, Kempsell KE, Szakmany T, Ball G (2020) Development of a bioinformatics framework for identification and validation of genomic biomarkers and key immunopathology processes and controllers in infectious and non-infectious severe inflammatory response syndrome. Front Immunol 11:380
Vazquez A, Flammini A, Maritan A et al (2003) Global protein function prediction from protein-protein interaction networks. Nat Biotechnol 21:697–700. https://doi.org/10.1038/nbt825
Wada T, Penninger JM (2004) Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23:2838–2849. https://doi.org/10.1038/sj.onc.1207556
West JW (2003) Effects of heat-stress on production in dairy cattle. J Dairy Sci 86(6):2131–2144
Wheelock JB, Rhoads RP, VanBaale MJ, Sanders SR, Baumgard LH (2010) Effects of heat stress on energetic metabolism in lactating Holstein cows. J Dairy Sci 93(2):644–655
Wolc A, Arango J, Settar P, Fulton JE, O’Sullivan NP, Dekkers JCM (2019) Genome wide association study for heat stress induced mortality in a white egg layer line. Poult Sci 98(1):92–96
Worku D, Hussen J, De Matteis G, Schusser B, Alhussien MN (2023) Candidate genes associated with heat stress and breeding strategies to relieve its effects in dairy cattle: a deeper insight into the genetic architecture and immune response to heat stress. Front Vet Sci 10:1151241. https://doi.org/10.3389/fvets.2023.1151241
Xian D, Song J, Yang L, Xiong X, Lai R, Zhong J (2019) Emerging roles of redox-mediated angiogenesis and oxidative stress in dermatoses. Oxidative medicine and cellular longevity, 2019
Yang YL, Rong Z, Kui L (2017) Future livestock breeding: Precision breeding based on multi-omics information and population personalization. J Integr Agric 16(12):2784–2791
Yigit M, Sogut O, Tataroglu Ö, Yamanoglu A, Yigit E, Güler EM, Kocyigit A (2018) Oxidative/antioxidative status, lymphocyte DNA damage, and urotensin-2 receptor level in patients with migraine attacks. Neuropsychiatr Dis Treat 14:367
Zachut M, Sood P, Levin Y, Moallem U (2016) Proteomic analysis of preovulatory follicular fluid reveals differentially abundant proteins in less fertile dairy cows. J Proteomics 139:122–129
Zeng L, Chen N, Ning Q, Yao Y, Chen H, Dang R, Zhang H, Lei C (2018) PRLH and SOD1 gene variations associated with heat tolerance in Chinese cattle. Anim Genet 49(5):447–451. https://doi.org/10.1111/age.12702
Zhang W, Liu HT (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 12(1):9–18
Zhang LY, Yam GHF, Tam POS, Lai RYK, Lam DSC, Pang CP, Fan DSP (2009) An αA-crystallin gene mutation, Arg12Cys, causing inherited cataract-microcornea exhibits an altered heat-shock response. Mol vis 15:1127
Zhang L, Liu X, Jia H (2022) WGCNA Analysis of Important Modules and Hub Genes of Compound Probiotics Regulating Lipid Metabolism in Heat-Stressed Broilers. Animals 12(19):2644. MDPI AG. Retrieved from. https://doi.org/10.3390/ani12192644
Zhao X, Balaji P, Pachon R, Beniamen DM, Vatner DE, Graham RM, Vatner SF (2015) Overexpression of cardiomyocyte α1A-adrenergic receptors attenuates postinfarct remodeling by inducing angiogenesis through heterocellular signaling. Arterioscler Thromb Vasc Biol 35(11):2451–2459
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The authors acknowledge the Director, ICAR-National Dairy Research Institute (NDRI), Karnal, and, Incharge NICRA, ICAR-NDRI for providing the necessary facilities to carry out the research work.
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This research was carried out under a project funded by National Innovations in Climate Resilient Agriculture (NICRA). The author received financial aid under the ICAR-NDRI Institute Fellowship program.
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Conceptualization: S.D. and R.A.; Methodology: G.D. and A.V.; Formal analysis and investigation: G.D., A.S. and R.A.; Writing original draft preparation: G.D. and R.A. and: Writing—review and editing: G.R.G. and V.V.; Funding acquisition and resources: A
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Dutta, G., Alex, R., Singh, A. et al. Functional transcriptome analysis revealed upregulation of MAPK-SMAD signalling pathways in chronic heat stress in crossbred cattle. Int J Biometeorol (2024). https://doi.org/10.1007/s00484-024-02672-y
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DOI: https://doi.org/10.1007/s00484-024-02672-y