Dry period heat stress induces microstructural changes in the lactating mammary gland


Autoři: Bethany Dado-Senn aff001;  Amy L. Skibiel aff001;  Thiago F. Fabris aff001;  Geoffrey E. Dahl aff001;  Jimena Laporta aff001
Působiště autorů: Department of Animal Sciences, University of Florida, Gainesville, FL, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222120

Souhrn

The bovine dry period is a non-lactating period between consecutive lactations characterized by mammary gland involution and redevelopment phases to replace senescent mammary epithelial cells with active cells primed for the next lactation. Dairy cows exposed to heat stress during the dry period experience milk yield reductions between 3–7.5 kg/d in the next lactation, partially attributed to processes associated with mammary cell growth and turnover during the dry period. However, the carry-over impact of dry period heat stress on mammary morphology during lactation has yet to be determined. In the current study, we hypothesized that exposure to heat stress during the dry period would alter alveolar microstructure and cellular turnover (i.e. proliferation and apoptosis) during lactation. Cows were either subjected to heat stress (HT, access to shade; n = 12) or cooling (CL, access to shade, fans, and soakers; n = 12) for a 46 d dry period. Upon calving, all cows were treated similarly with access to cooling for their entire lactation. Six cows per treatment were randomly selected for mammary gland biopsies at 14, 42, and 84 days in milk. Tissues were sectioned and stained for histological analysis. During lactation, HT cows produced 4 kg less colostrum and 3.7 kg less milk compared with CL cows. Lactating mammary gland microstructure was impacted after exposure to dry period heat stress; HT cows had fewer alveoli and a higher proportion of connective tissue in the mammary gland relative to CL cows, however alveolar area was similar between treatments. Rates of mammary epithelial cell proliferation and apoptosis were similar between treatment groups. This suggests that heat stress exposure during the dry period leads to reductions in milk yield that could be caused, in part, by a reduction in alveoli number in the lactating mammary gland but not to dynamic alterations in cellular turnover once lactation is established.

Klíčová slova:

Medicine and health sciences – Endocrinology – Endocrine physiology – Breast tissue – Mammary glands – Diagnostic medicine – Signs and symptoms – Hyperthermia – Pathology and laboratory medicine – Surgical and invasive medical procedures – Biopsy – Biology and life sciences – Physiology – Reproductive physiology – Nutrition – Diet – Beverages – Milk – Anatomy – Body fluids – Reproductive system – Exocrine glands – Biological tissue – Connective tissue – Cell biology – Cell processes – Cell death – Apoptosis – Physical sciences – Physics – Classical mechanics – Mechanical stress – Thermal stresses


Zdroje

1. Yousef MK. Stress physiology in livestock. Volume I. Basic principles. 1st ed. Yousef MK, editor. Boca Raton, FL: CRC Press; 1985.

2. Gebremedhin KG, Wu B. A model of evaporative cooling of wet skin surface and fur layer. J Therm Biol. 2001;26: 537–545. doi: 10.1016/S0306-4565(00)00048-6

3. Zimbelman RB, Rhoads RP, Collier RJ, Duff GC. A re-evaluation of the impact of temperature humidity index (THI) and black globe humidity index (BGHI) on milk production in high producing dairy cows. Proceedings of the Western Dairy Management Conference. 2009. pp. 158–169. Available: http://animal.cals.arizona.edu/swnmc/Proceedings/2009/14Collier_09.pdf

4. Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A. Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal. 2010;4: 1167–1183. doi: 10.1017/S175173111000090X 22444615

5. Baumgard LH, Rhoads RP. Effects of Heat Stress on Postabsorptive Metabolism and Energetics. Annu Rev Anim Biosci. 2013;1: 311–337. doi: 10.1146/annurev-animal-031412-103644 25387022

6. Wheelock JB, Rhoads RP, VanBaale MJ, Sanders SR, Baumgard LH. Effects of heat stress on energetic metabolism in lactating Holstein cows1. J Dairy Sci. Elsevier; 2010;93: 644–655. doi: 10.3168/jds.2009-2295 20105536

7. St-Pierre NR, Cobanov B, Schnitkey G. Economic Losses from Heat Stress by US Livestock Industries. J Dairy Sci. Elsevier; 2003;86: E52–E77. doi: 10.3168/jds.S0022-0302(03)74040-5

8. do Amaral BC, Connor EE, Tao S, Hayen J, Bubolz J, Dahl GE. Heat-stress abatement during the dry period: Does cooling improve transition into lactation? J Dairy Sci. Elsevier; 2009;92: 5988–5999. doi: 10.3168/jds.2009-2343 19923602

9. Tao S, Bubolz JW, do Amaral BC, Thompson IM, Hayen MJ, Johnson SE, et al. Effect of heat stress during the dry period on mammary gland development. J Dairy Sci. Elsevier; 2011;94: 5976–5986. doi: 10.3168/jds.2011-4329 22118086

10. Tao S, Dahl GE. Invited review: Heat stress effects during late gestation on dry cows and their calves. J Dairy Sci. Elsevier; 2013;96: 4079–4093. doi: 10.3168/jds.2012-6278 23664343

11. Thompson IM, Dahl GE. Dry-period seasonal effects on the subsequent lactation. The Professional Animal Scientist; 2012;28: 628–631.

12. Ferreira FC, Gennari RS, Dahl GE, De Vries A. Economic feasibility of cooling dry cows across the United States. J Dairy Sci. Elsevier; 2016;99: 9931–9941. doi: 10.3168/jds.2016-11566 27743663

13. Hurley WL. Mammary Gland Function During Involution. J Dairy Sci. Elsevier; 1989;72: 1637–1646. doi: 10.3168/jds.S0022-0302(89)79276-6 2668360

14. Capuco AV, Akers RM, Smith JJ. Mammary Growth in Holstein Cows During the Dry Period: Quantification of Nucleic Acids and Histology. J Dairy Sci. Elsevier; 1997;80: 477–487. doi: 10.3168/jds.S0022-0302(97)75960-5 9098797

15. Capuco AV., Ellis SE, Hale SA, Long E, Erdman RA, Zhao X, et al. Lactation persistency: insights from mammary cell proliferation studies. J Anim Sci. 2003;81 Suppl 3: 18–31. doi:/2003.81suppl_318x doi: 10.2527/2003.81suppl_318x 15000403

16. Welch W. J., Suhan JP. Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol. 1985;101: 1198–1211. doi: 10.1083/jcb.101.4.1198 3900086

17. Laszlo A. The effects of hyperthermia on mammalian cell structure and function. Cell Prolif. 1992;25: 59–87. doi: 10.1111/j.1365-2184.1992.tb01482.x 1554820

18. Dado-Senn B, Skibiel AL, Fabris TF, Zhang Y, Dahl GE, Peñagaricano F, et al. RNA-Seq reveals novel genes and pathways involved in bovine mammary involution during the dry period and under environmental heat stress. Sci Rep. 2018;8: 1–11. doi: 10.1038/s41598-017-17765-5

19. Collier RJ, Collier JL, Rhoads RP, Baumgard LH. Invited Review: Genes Involved in the Bovine Heat Stress Response. J Dairy Sci. Elsevier; 2008;91: 445–454. doi: 10.3168/jds.2007-0540 18218730

20. Li L, Sun Y, Wu J, Li X, Luo M, Wang G. The global effect of heat on gene expression in cultured bovine mammary epithelial cells. Cell Stress Chaperones. 2015;20: 381–389. doi: 10.1007/s12192-014-0559-7 25536930

21. Shyy TT, Asch BB, Asch HL. Concurrent collapse of keratin filaments, aggregation of organelles, and inhibition of protein synthesis during the heat shock response in mammary epithelial cells. J Cell Biol. 1989;108: 997–1008. doi: 10.1083/jcb.108.3.997 2466040

22. Hu H, Wang J, Gao H, Li S, Zhang Y, Zheng N. Heat-induced apoptosis and gene expression in bovine mammary epithelial cells. Anim Prod Sci. 2016;56: 918–926. doi: 10.1071/AN14420

23. Sonna LA, Fujita J, Gaffin S, Lilly CM. Effect of heat and cold stress on mammalian gene expression. J Appl Physiol. 2002;92: 1725–1742. doi: 10.1152/japplphysiol.01143.2001 11896043

24. Skibiel AL, Dado-Senn B, Fabris TF, Dahl GE, Laporta J. In utero exposure to thermal stress has longterm effects on mammary gland microstructure and function in dairy cattle. PLoS One. 2018;13: 1–13. doi: 10.1371/journal.pone.0206046 30325972

25. Wohlgemuth SE, Ramirez-Lee Y, Tao S, Monteiro APA, Ahmed BM, Dahl GE. Short communication: Effect of heat stress on markers of autophagy in the mammary gland during the dry period. J Dairy Sci. 2016;99: 4875–4880. doi: 10.3168/jds.2015-10649 27060813

26. Dikmen S, Pontes E, Olson TA, Alava E, Hansen PJ, Fear JM, et al. Differences in Thermoregulatory Ability Between Slick-Haired and Wild-Type Lactating Holstein Cows in Response to Acute Heat Stress. J Dairy Sci. Elsevier; 2008;91: 3395–3402. doi: 10.3168/jds.2008-1072 18765598

27. Farr VC, Stelwagen K, Cate LR, Molenaar AJ, McFadden TB, Davis SR. An Improved Method for the Routine Biopsy of Bovine Mammary Tissue. J Dairy Sci. Elsevier; 1996;79: 543–549. doi: 10.3168/jds.S0022-0302(96)76398-1 8744218

28. Adin G, Gelman A, Solomon R, Flamenbaum I, Nikbachat M, Yosef E, et al. Effects of cooling dry cows under heat load conditions on mammary gland enzymatic activity, intake of food and water, and performance during the dry period and after parturition. Livest Sci. Elsevier B.V.; 2009;124: 189–195. doi: 10.1016/j.livsci.2009.01.014

29. Wolfenson D, Flamenbaum I, Berman A. Dry period heat stress relief effects on prepartum progesterone, calf birth weight, and milk production. J Dairy Sci. 1988;71: 809–818. doi: 10.3168/jds.S0022-0302(88)79621-6 3372821

30. Avendaño-Reyes L, Alvarez-Valenzuela FD, Correa-Calderón A, Saucedo-Quintero JS, Robinson PH, Fadel JG. Effect of cooling Holstein cows during the dry period on postpartum performance under heat stress conditions. Livest Sci. 2006;105: 198–206. doi: 10.1016/j.livsci.2006.06.009

31. Fabris TF, Laporta J, Corra FN, Torres YM, Kirk DJ, McLean DJ, et al. Effect of nutritional immunomodulation and heat stress during the dry period on subsequent performance of cows. J Dairy Sci. 2017;100: 6733–6742. doi: 10.3168/jds.2016-12313 28624274

32. Robertshaw D. Thermal regulation and the thermal environment. In: Reece WO, editor. Dukes’ Physiology of Domestic Animals. 12th ed. Ithaca, NY: Cornell University Press; 2004. pp. 962–973.

33. Collier RJ, Doelger SG, Head HH, Thatcher WW, Wilcox CJ. Effects of heat stress during pregnancy on maternal hormone concentrations, calf birth weight and postpartum milk yield of Holstein cows. J Anim Sci. 1982;54: 309–319. doi: 10.2527/jas1982.542309x 7076593

34. Tao S, Monteiro APA, Thompson IM, Hayen MJ, Dahl GE. Effect of late-gestation maternal heat stress on growth and immune function of dairy calves. J Dairy Sci. Elsevier; 2012;95: 7128–7136. doi: 10.3168/jds.2012-5697 23021751

35. Monteiro APA, Tao S, Thompson IMT, Dahl GE. In utero heat stress decreases calf survival and performance through the first lactation. J Dairy Sci. Elsevier; 2016;99: 8443–8450. doi: 10.3168/jds.2016-11072 27522427

36. do Amaral BC, Connor EE, Tao S, Hayen MJ, Bubolz JW, Dahl GE. Heat stress abatement during the dry period influences metabolic gene expression and improves immune status in the transition period of dairy cows. J Dairy Sci. Elsevier; 2011;94: 86–96. doi: 10.3168/jds.2009-3004 21183020

37. Val-Arreola D, Kebreab E, Dijkstra J, France J. Study of the Lactation Curve in Dairy Cattle on Farms in Central Mexico. J Dairy Sci. Elsevier; 2004;87: 3789–3799. doi: 10.3168/jds.S0022-0302(04)73518-3 15483163

38. Laporta J, Ferreira FC, Dado-Senn B, De Vries A, Dahl GE. Dry period heat stress reduces dam, daughter, and granddaughter productivity. American Dairy Science Association Annual Meeting. Knoxville, TN; 2018. p. 151.

39. Skibiel AL, Peñagaricano F, Amorín R, Ahmed BM, Dahl GE, Laporta J. In Utero Heat Stress Alters the Offspring Epigenome. Sci Rep. 2018;8:1–15. doi: 10.1038/s41598-017-17765-5

40. Lang SLC, Iverson SJ, Bowen WD. Primiparous and multiparous females differ in mammary gland alveolar development: implications for milk production. J Exp Biol. 2012;215: 2904–2911. doi: 10.1242/jeb.067058 22837465

41. Miller N, Delbecchi L, Talbot BG, Petitclerc D, Wagner GF, Lacasse P. Effect of Stage of Lactation and Parity on Mammary Gland Cell Renewal. J Dairy Sci. Elsevier; 2006;89: 4669–4677. doi: 10.3168/jds.S0022-0302(06)72517-6 17106099

42. Safayi S, Sejrsen K, Elbrønd VS, Nørgaard JV, Nielsen MO, Hou L, et al. Mammary remodeling in primiparous and multiparous dairy goats during lactation. J Dairy Sci. Elsevier; 2010;93: 1478–1490. doi: 10.3168/jds.2009-2422 20338425

43. Akers RM. Lactation and the mammary gland. Iowa: Blackwell Publishing; 2002.

44. Capuco AV, Wood DL, Baldwin R, Mcleod K, Paape MJ. Mammary Cell Number, Proliferation, and Apoptosis During a Bovine Lactation: Relation to Milk Production and Effect of bST. J Dairy Sci. Elsevier; 2001;84: 2177–2187. doi: 10.3168/jds.S0022-0302(01)74664-4 11699449

45. Davis SR, Farr VC, Copeman PJA, Stelwagen K, Carruthers VR, Knight CH. Partitioning of milk accumulation between cisternal and alveolar compartments of the bovine udder: relationship to production loss during once daily milking. J Dairy Res. 1998;65: 1–8. doi: 10.1017/s0022029997002562 9513051

46. Holst BD, Hurley WL, Nelson DR. Involution of the Bovine Mammary Gland: Histological and Ultrastructural Changes. J Dairy Sci. 1987;70: 935–944. doi: 10.3168/jds.S0022-0302(87)80097-8 3597934

47. Enger BD, Crutchfield CE, Yohe TT, Enger KM, Nickerson SC, Parsons CLM, et al. Staphylococcus aureus intramammary challenge in non-lactating mammary glands stimulated to rapidly grow and develop with estradiol and progesterone. Vet Res. BioMed Central; 2018;49: 1–14. doi: 10.1186/s13567-018-0542-x 29866164

48. Trinidad P, Nickerson SC, Adkinson RW. Histopathology of Staphylococcal Mastitis in Unbred Dairy Heifers. J Dairy Sci. Elsevier; 2010;73: 639–647. doi: 10.3168/jds.s0022-0302(90)78715-2

49. De Vries LD, Dover H, Casey T, Vandehaar MJ, Plaut K. Characterization of mammary stromal remodeling during the dry period. J Dairy Sci. Elsevier; 2010;93: 2433–2443. doi: 10.3168/jds.2009-2764 20494151


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden