Journal of Animal Reproduction and Biotechnology (한국동물생명공학회지)

The Korean Society of Animal Reproduction and Biotechnology (한국동물생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Differential expression of circulating microRNAs in lactating Holstein and Jersey cows exposed to heat stress

  • Jihwan Lee (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Doosan Kim (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Byeonghwi Lim (Department of Animal Science and Technology, Chung-Ang University) ;
  • Gyeonglim Ryu (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Hyeonguk Baek (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Joohwan Kim (Dairy Biotechnology R&D Center, Seoul Milk Cooperation) ;
  • Seungmin Ha (Animal Genetic Resources Research Center, National Institute of Animal Science, Rural Development Administration) ;
  • Sangbum Kim (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Seunghwan Lee (Division of Animal and Dairy Science, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Taejeong Choi (Dairy Science Division, National Institute of Animal Science, Rural Development Administration) ;
  • Inchul Choi (Division of Animal and Dairy Science, College of Agriculture and Life Sciences, Chungnam National University)
  • Received : 2024.10.03
  • Accepted : 2024.11.26
  • Published : 2024.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Background: South Korea has recently faced record-high temperatures, which have adversely affected dairy production. Holstein cows, the primary dairy breed globally, are particularly sensitive to heat stress. In contrast, Jersey cows have shown greater heat tolerance, as demonstrated by phenotypic studies. Methods: We investigated physiological and molecular responses to heat stress in Holstein and Jersey cows by measuring rectal temperature, milk yield, and average daily gain, confirming Holstein cows' greater vulnerability. To explore molecular mechanisms, we analyzed circulating microRNA profiles from whole blood samples collected under heat stress and normal conditions using microRNA-sequencing. Differential expression patterns were compared between the two breeds to identify biological pathways associated with heat stress. Results: Four microRNAs (bta-miR-20b, bta-miR-1246, bta-miR-2284x, and bta-miR-2284y) were significantly differentially expressed in both breeds under heat stress (|FC| ≥ 2, p < 0.05). Notably, bta-miR-20b and bta-miR-1246 were linked to corpus luteum function and progesterone biosynthesis, while bta-miR-2284x and bta-miR-2284y were associated with immune responses. A comparison of 11 potential heat stress-related microRNAs identified in previous studies of Holstein cows revealed consistent expression trends in Jersey cows, albeit with lower fold changes, suggesting their superior heat resilience. Conclusions: Our study highlights the physiological and microRNA-based differences in heat stress responses between Holstein and Jersey cows. Jersey cows exhibited greater resilience, supported by more stable microRNA expression profiles and improved heat stress indicators, making them a promising breed for dairy production in increasingly hot climates.

Keywords

Acknowledgement

This research was supported by the National Institute of Animal Science, Project (PJ015006), with the goal of improving productivity and sustainability in the dairy sector through innovative research and development efforts.

References

  1. Armstrong DV. 1994. Heat stress interaction with shade and cooling. J. Dairy Sci. 77:2044-2050. https://doi.org/10.3168/jds.S0022-0302(94)77149-6
  2. Baumgard LH, Rhoads RP, Rhoads ML, Gabler NK, Ross JW, Keating AF, Boddicker RL, Lenka S, Sejian V. 2012. Impact of climate change on livestock production. In: Sejian V, Naqvi S, Ezeji T, Lakritz J, Lal R (Eds.), Environmental Stress and Amelioration in Livestock Production. Springer, Berlin, pp. 413-468.
  3. Bohmanova J, Misztal I, Cole JB. 2007. Temperature-humidity indices as indicators of milk production losses due to heat stress. J. Dairy Sci. 90:1947-1956. https://doi.org/10.3168/jds.2006-513
  4. Council on Dairy Cattle Breeding (CDCB). 2020. Summary of 2020 DHI herd averages: DHI report K-3. CDCB. Retrieved September 29, 2024, from https://queries.uscdcb.com/publish/dhi/dhi21/haall.html
  5. Dash S, Chakravarty AK, Singh A, Upadhyay A, Singh M, Yousuf S. 2016. Effect of heat stress on reproductive performances of dairy cattle and buffaloes: a review. Vet. World 9:235-244. https://doi.org/10.14202/vetworld.2016.235-244
  6. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4:P3.
  7. Dikmen S and Hansen PJ. 2009. Is the temperature-humidity index the best indicator of heat stress in lactating dairy cows in a subtropical environment? J. Dairy Sci. 92:109-116. https://doi.org/10.3168/jds.2008-1370
  8. Donovan MR and Marr MT 2nd. 2016. dFOXO activates large and small heat shock protein genes in response to oxidative stress to maintain proteostasis in Drosophila. J. Biol. Chem. 291:19042-19050. https://doi.org/10.1074/jbc.M116.723049
  9. Farhan M, Wang H, Gaur U, Little PJ, Xu J, Zheng W. 2017. FOXO signaling pathways as therapeutic targets in cancer. Int. J. Biol. Sci. 13:815-827. https://doi.org/10.7150/ijbs.20052
  10. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. 2007. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell. 27:91-105. https://doi.org/10.1016/j.molcel.2007.06.017
  11. Ha M and Kim VN. 2014. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15:509-524. https://doi.org/10.1038/nrm3838
  12. Habeeb AA, Gad AE, Atta MA. 2018. Temperature-humidity indices as indicators to heat stress of climatic conditions with relation to production and reproduction of farm animals. Int. J. Biotechnol. Recent Adv. 1:35-50. https://doi.org/10.18689/ijbr-1000107
  13. Hansen PJ. 2019. Reproductive physiology of the heat-stressed dairy cow: implications for fertility and assisted reproduction. Anim. Reprod. 16:497-507. https://doi.org/10.21451/1984-3143-AR2019-0053
  14. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Lee ML, Schmittgen TD, Nana-Sinkam SP, Jarjoura D, Marsh CB. 2008. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3:e3694. https://doi.org/10.1371/journal.pone.0003694
  15. Ioannidis J and Donadeu FX. 2016. Circulating microRNA profiles during the bovine oestrous cycle. PLoS One 11: e0158160. https://doi.org/10.1371/journal.pone.0158160
  16. Ioannidis J and Donadeu FX. 2017. Changes in circulating microRNA levels can be identified as early as day 8 of pregnancy in cattle. PLoS One 12:e0174892. https://doi.org/10.1371/journal.pone.0174892
  17. Ioannidis J, Sánchez-Molano E, Psifidi A, Donadeu FX, Banos G. 2018. Association of plasma microRNA expression with age, genetic background and functional traits in dairy cattle. Sci. Rep. 8:12955.
  18. Jonsson NN, McGowan MR, McGuigan K, Davison TM, Hussain AM, Kafi M, Matschoss A. 1997. Relationships among calving season, heat load, energy balance and postpartum ovulation of dairy cows in a subtropical environment. Anim. Reprod. Sci. 47:315-326. https://doi.org/10.1016/S0378-4320(97)00014-6
  19. Jurkovich V, Somoskői B, Kovács L, Bakony M. 2023. The effects of heat stress in Jersey, Hungarian Simmental and Holstein Friesian cows. J. Anim. Feed Sci. 32:68-75. https://doi.org/10.22358/jafs/155410/2022
  20. Kim VN, Han J, Siomi MC. 2009. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10:126-139. https://doi.org/10.1038/nrm2632
  21. Kim VN and Nam JW. 2006. Genomics of microRNA. Trends Genet. 22:165-173. https://doi.org/10.1016/j.tig.2006.01.003
  22. KTimes. 2024. Korea sees highest average summer temperature on record. The Korea Times. https://www.koreatimes.co.kr/www/nation/2024/12/371_381933.html
  23. Kupfer GM. 2013. Fanconi anemia: a signal transduction and DNA repair pathway. Yale J. Biol. Med. 86:491-497.
  24. Lee J, Kim D, Son J, Kim D, Jeon E, Jung D, Han M, Ha S, Hwang S, Choi I. 2023. Effects of heat stress on conception in Holstein and Jersey cattle and oocyte maturation in vitro. J. Anim. Sci. Technol. 65:324-335.
  25. Lee J, Lee S, Ryu G, Kim D, Baek HU, Kim J, Lee K, Kim S, Kim S, Dang CG, Choi T, Choi I. 2024. A retrospective analysis of conception per embryo transfer in dairy cattle in South Korea. Theriogenology 226:363-368. https://doi.org/10.1016/j.theriogenology.2024.07.001
  26. Lee J, Lee S, Son J, Lim H, Kim E, Kim D, Ha S, Hur T, Lee S, Choi I. 2020. Analysis of circulating-microRNA expression in lactating Holstein cows under summer heat stress. PLoS One 15:e0231125. https://doi.org/10.1371/journal.pone.0231125
  27. Li J, Duan Y, Kong W, Gao H, Fu S, Li H, Zhou Y, Liu H, Yuan D, Zhou C. 2024. Heat stress affects swimming performance and induces biochemical, structural, and transcriptional changes in the heart of Gymnocypris eckloni. Aquacult. Rep. 35:101998.
  28. Liu H, Zhang B, Li F, Liu L, Yang T, Zhang H, Li F. 2022. Effects of heat stress on growth performance, carcass traits, serum metabolism, and intestinal microflora of meat rabbits. Front Microbiol. 13:998095.
  29. Liu J, Li L, Chen X, Lu Y, Wang D. 2019. Effects of heat stress on body temperature, milk production, and reproduction in dairy cows: a novel idea for monitoring and evaluation of heat stress—a review. Asian-Australas J. Anim. Sci. 32:1332-1339. https://doi.org/10.5713/ajas.18.0743
  30. Mader TL, Davis MS, Brown-Brandl T. 2006. Environmental factors influencing heat stress in feedlot cattle. J. Anim. Sci. 84:712-719. https://doi.org/10.2527/2006.843712x
  31. Mi H, Muruganujan A, Thomas PD. 2013. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic. Acids Res. 41:D377-D386.
  32. Muller CJC and Botha JA. 1993. Effect of summer climatic conditions on different heat tolerance indicators in primiparous Friesian and Jersey cows. S. Afr. J. Anim. Sci. 23:98-103.
  33. National Research Council. 2001. Nutrient requirements of dairy cattle. 7th ed, The National Academies Press, Washington.
  34. Nebel RL, Jobst SM, Dransfield MBG, Pandolfi SM, Bailey TL. 1997. Use of radio frequency data communication system, HeatWatch®, to describe behavioral estrus in dairy cattle. J. Dairy Sci. 80(Suppl 1):179.
  35. Norman HD, Guinan FL, Megonigal JH, Dürr JW. 2020. Reproductive status of cows in Dairy Herd Improvement programs and bred using artificial insemination (2020). Council on Dairy Cattle Breeding. Retrieved September 29, 2024, from https://queries.uscdcb.com/publish/dhi/current/reproall.html
  36. Norman HD, Wright JR, Hubbard SM, Miller RH, Hutchison JL. 2009. Reproductive status of Holstein and Jersey cows in the United States. J. Dairy Sci. 92:3517-3528. https://doi.org/10.3168/jds.2008-1768
  37. Pragna P, Archana PR, Aleena J, Sejian V, Krishnan G, Bagath M, Manimaran A, Beena V, Kurien EK, Varma G, Bhatta R. 2017. Heat stress and dairy cow: impact on both milk yield and composition. Int. J. Dairy Sci. 12:1-11. https://doi.org/10.3923/ijds.2017.1.11
  38. Putney DJ, Drost M, Thatcher WW. 1989. Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination. Theriogenology 31:765-778. https://doi.org/10.1016/0093-691X(89)90022-8
  39. Reid G, Kirschner MB, van Zandwijk N. 2011. Circulating microRNAs: association with disease and potential use as biomarkers. Crit. Rev. Oncol. Hematol. 80:193-208. https://doi.org/10.1016/j.critrevonc.2010.11.004
  40. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. https://doi.org/10.1093/bioinformatics/btp616
  41. Roche JR. 2003. Effect of pregnancy on milk production and bodyweight from identical twin study. J. Dairy Sci. 86:777-783. https://doi.org/10.3168/jds.S0022-0302(03)73659-5
  42. Roth C, Rack B, Müller V, Janni W, Pantel K, Schwarzenbach H. 2010. Circulating microRNAs as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res. 12:R90. https://doi.org/10.1186/bcr2766
  43. Roth Z. 2020. Influence of heat stress on reproduction in dairy cows-physiological and practical aspects. J. Anim. Sci. 98(Suppl 1):S80-S87. https://doi.org/10.1093/jas/skaa139
  44. Smith DL, Smith T, Rude BJ, Ward SH. 2013. Short communication: comparison of the effects of heat stress on milk and component yields and somatic cell score in Holstein and Jersey cows. J. Dairy Sci. 96:3028-3033. https://doi.org/10.3168/jds.2012-5737
  45. Sørensen AE, Wissing ML, Salö S, Englund AL, Dalgaard LT. 2014. MicroRNAs related to polycystic ovary syndrome (PCOS). Genes (Basel) 5:684-708. https://doi.org/10.3390/genes5030684
  46. Tao S, Dahl GE, Laporta J, Bernard JK, Orellana Rivas RM, Marins TN. 2019. PHYSIOLOGY SYMPOSIUM: effects of heat stress during late gestation on the dam and its calf12. J. Anim. Sci. 97:2245-2257. https://doi.org/10.1093/jas/skz061
  47. Thatcher WW and Roman-Ponce H. 1981. Effects of climate on bovine reproduction. WB Saunders Company, Philadelphia, PA, pp. 301-309.
  48. Trout JP, McDowell LR, Hansen PJ. 1998. Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress. J. Dairy Sci. 81:1244-1250. https://doi.org/10.3168/jds.S0022-0302(98)75685-1
  49. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. 2011. Characterization of extracellular circulating microRNA. Nucleic. Acids Res. 39:7223-7233. https://doi.org/10.1093/nar/gkr254
  50. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9:654-659. https://doi.org/10.1038/ncb1596
  51. Vejnar CE and Zdobnov EM. 2012. MiRmap: comprehensive prediction of microRNA target repression strength. Nucleic. Acids Res. 40:11673-11683. https://doi.org/10.1093/nar/gks901
  52. West JW. 1999. Nutritional strategies for managing the heat stressed dairy cow. J. Anim. Sci. 77 Suppl 2:21-35. https://doi.org/10.2527/1997.77suppl_221x
  53. Wiggans GR. 2000. USDA summary of 2000 herd averages. Retrived September 29, 2024, from https://queries.uscdcb.com/publish/dhi/dhi01/k3.shtml
  54. Wise ME, Armstrong DV, Huber JT, Hunter R, Wiersma F. 1988a. Hormonal alterations in the lactating dairy cow in response to thermal stress. J. Dairy Sci. 71:2480-2485. https://doi.org/10.3168/jds.S0022-0302(88)79834-3
  55. Wise ME, Rodriguez RE, Armstrong DV, Huber JT, Wiersma F, Hunter R. 1988b. Fertility and hormonal responses to temporary relief of heat stress in lactating dairy cows. Theriogenology 29:1027-1035. https://doi.org/10.1016/S0093-691X(88)80026-8
  56. Witwer KW. 2015. Circulating microRNA biomarker studies: pitfalls and potential solutions. Clin. Chem. 61:56-63. https://doi.org/10.1373/clinchem.2014.221341
  57. Wolfenson D, Flamenbaum I, Berman A. 1988. Hyperthermia and body energy store effects on estrous behavior, conception rate, and corpus luteum function in dairy cows. J. Dairy Sci. 71:3497-3504. https://doi.org/10.3168/jds.S0022-0302(88)79956-7
  58. Wolfenson D and Roth Z. 2018. Impact of heat stress on cow reproduction and fertility. Anim. Front. 9:32-38. https://doi.org/10.1093/af/vfy027
  59. Wolfenson D, Roth Z, Meidan R. 2000. Impaired reproduction in heat-stressed cattle: basic and applied aspects. Anim. Reprod. Sci. 60-61:535-547. https://doi.org/10.1016/S0378-4320(00)00102-0
  60. Yoshimoto K, Mizoguchi M, Hata N, Murata H, Hatae R, Amano T, Nakamizo A, Sasaki T. 2012. Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma. Front. Oncol. 2:186. https://doi.org/10.3389/fonc.2012.00186