Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Protective effects of 5-aminolevulinic acid on heat stress in bovine mammary epithelial cells

  • Received : 2020.05.18
  • Accepted : 2020.07.27
  • Published : 2021.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Cells have increased susceptibility to activation of apoptosis when suffering heat stress (HS). An effective supplementation strategy to mimic heat-induced apoptosis of bovine mammary epithelial cells (MECs) is necessary to maintain optimal milk production. This study aimed to investigate possible protective effects of the anti-apoptotic activity of 5-aminolevulinic acid (5-ALA) against HS-induced damage of bovine MECs. Methods: Bovine MECs were pretreated with or without 5-ALA at concentrations of 10, 100, and 500 µM for 24 h followed by HS (42.5℃ for 24 h and 48 h). Cell viability was measured with 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assays. Real-time quantitative polymerase chain reaction and Western blotting were used to explore the regulation of genes associated with apoptosis, oxidative stress, and endoplasmic reticulum (ER) stress genes. Results: We found that 5-ALA induces cytoprotection via inhibition of apoptosis markers after HS-induced damage. Pretreatment of bovine MECs with 5-ALA resulted in dramatic upregulation of mRNA for nuclear factor erythroid-derived 2-like factor 2, heme oxygenase-1, and NAD(P)H quinone oxidoreductase 1, all of which are antioxidant stress genes. Moreover, 5-ALA pretreatment significantly suppressed HS-induced ER stress-associated markers, glucose-regulated protein 78, and C/EBP homologous protein expression levels. Conclusion: 5-ALA can ameliorate the ER stress in heat stressed bovine MEC via enhancing the expression of antioxidant gene.

Keywords

References

  1. St-Pierre NR, Cobanov B, Schnitkey G. Economic losses from heat stress by US livestock industries. J Dairy Sci 2003;86(Suppl):E52-77. https://doi.org/10.3168/jds.S0022-0302(03)74040-5
  2. West JW. Effects of heat-stress on production in dairy cattle. J Dairy Sci 2003;86:2131-44. https://doi.org/10.3168/jds.S0022-0302(03)73803-X
  3. Wheelock JB, Rhoads RP, VanBaale MJ, Sanders SR, Baumgard LH. Effects of heat stress on energetic metabolism in lactating Holstein cows. J Dairy Sci 2010;93:644-55. https://doi.org/10.3168/jds.2009-2295
  4. 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 2001;84:2177-87. https://doi.org/10.3168/jds.S0022-0302(01)74664-4
  5. Kadzere CT, Murphy MR, Silanikove N, Maltz E. Heat stress in lactating dairy cows: a review. Livest Prod Sci 2002;77:59-91. https://doi.org/10.1016/S0301-6226(01)00330-X
  6. Takayama S, Reed JC, Homma S. Heat-shock proteins as regulators of apoptosis. Oncogene 2003;22:9041-7. https://doi.org/10.1038/sj.onc.1207114
  7. Jin XL, Wang K, Liu L, Liu HY, Zhao FQ, Liu JX. Nuclear factor-like factor 2-antioxidant response element signaling activation by tert-butylhydroquinone attenuates acute heat stress in bovine mammary epithelial cells. J Dairy Sci 2016;99:9094-103. https://doi.org/10.3168/jds.2016-11031
  8. Cao SS, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal 2014;21:396-413. https://doi.org/10.1089/ars.2014.5851
  9. Patil C, Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 2001;13:349-55. https://doi.org/10.1016/S0955-0674(00)00219-2
  10. Spaan CN, Smit WL, van Lidth de Jeude JF, et al. Expression of UPR effector proteins ATF6 and XBP1 reduce colorectal cancer cell proliferation and stemness by activating PERK signaling. Cell Death Dis 2019;10:490. https://doi.org/10.1038/s41419-019-1729-4
  11. Xu X, Gupta S, Hu W, McGrath BC, Cavener DR. Hyperthermia induces the ER stress pathway. PLoS One 2011;6:e23740. https://doi.org/10.1371/journal.pone.0023740
  12. Yonekura S, Tsuchiya M, Tokutake Y, et al. The unfolded protein response is involved in both differentiation and apoptosis of bovine mammary epithelial cells. J Dairy Sci 2018;101:3568-78. https://doi.org/10.3168/jds.2017-13718
  13. Rodriguez BL, Curb JD, Davis J, et al. Use of the dietary supplement 5-aminiolevulinic acid (5-ALA) and its relationship with glucose levels and hemoglobin A1C among individuals with prediabetes. Clin Transl Sci 2012;5:314-20. https://doi.org/10.1111/j.1752-8062.2012.00421.x
  14. Fujino M, Nishio Y, Ito H, Tanaka T, Li XK. 5-Aminolevulinic acid regulates the inflammatory response and alloimmune reaction. Int Immunopharmacol 2016;37:71-8. https://doi.org/10.1016/j.intimp.2015.11.034
  15. Liu C, Fujino M, Zhu S, et al. 5-ALA/SFC enhances HO-1 expression through the MAPK/Nrf2 antioxidant pathway and attenuates murine tubular epithelial cell apoptosis. FEBS Open Bio 2019;9:1928-38. https://doi.org/10.1002/2211-5463.12729
  16. Uchida A, Kidokoro K, Sogawa Y, et al. 5-Aminolevulinic acid exerts renoprotective effect via Nrf2 activation in murine rhabdomyolysis-induced acute kidney injury. Nephrology 2019;24:28-38. https://doi.org/10.1111/nep.13189
  17. Liu C, Zhu P, Fujino M, et al. 5-aminolaevulinic acid (ALA), enhances heme oxygenase (HO)-1 expression and attenuates tubulointerstitial fibrosis and renal apoptosis in chronic cyclosporine nephropathy. Biochem Biophys Res Commun 2019;508:583-9. https://doi.org/10.1016/j.bbrc.2018.11.175
  18. Zhao M, Zhu P, Fujino M, et al. 5-Aminolevulinic acid with sodium ferrous citrate induces autophagy and protects cardiomyocytes from hypoxia-induced cellular injury through MAPK-Nrf-2-HO-1 signaling cascade. Biochem Biophys Res Commun 2016;479:663-9. https://doi.org/10.1016/j.bbrc.2016.09.156
  19. Terada Y, Inoue K, Matsumoto T, et al. 5-Aminolevulinic acid protects against cisplatin-induced nephrotoxicity without compromising the anticancer efficiency of cisplatin in rats in vitro and in vivo. PLoS One 2013;8:e80850. https://doi.org/10.1371/journal.pone.0080850
  20. Hou J, Cai S, Kitajima Y, et al. 5-Aminolevulinic acid combined with ferrous iron induces carbon monoxide generation in mouse kidneys and protects from renal ischemia-reperfusion injury. Am J Physiol Renal Physiol 2013;305:F1149-57. https://doi.org/10.1152/ajprenal.00275.2013
  21. Li C, Wang Y, Li L, Han Z, Mao S, Wang G. Betaine protects against heat exposure-induced oxidative stress and apoptosis in bovine mammary epithelial cells via regulation of ROS production. Cell Stress Chaperones 2019;24:453-60. https://doi.org/10.1007/s12192-019-00982-4
  22. Sharmin MM, Mizusawa M, Hayashi S, Arai W, Sakata S, Yonekura S. Effects of fatty acids on inducing endoplasmic reticulum stress in bovine mammary epithelial cells. J Dairy Sci 2020;103:8643-54. https://doi.org/10.3168/jds.2019-18080
  23. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000;2:326-32. https://doi.org/10.1038/35014014
  24. Zinszner H, Kuroda M, Wang XZ, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998;12:982-95. https://doi.org/10.1101/gad.12.7.982
  25. Hou CH, Lin FL, Hou SM, Liu JF. Hyperthermia induces apoptosis through endoplasmic reticulum and reactive oxygen species in human osteosarcoma cells. Int J Mol Sci 2014;15:17380-95. https://doi.org/10.3390/ijms151017380
  26. Alemu TW, Pandey HO, Wondim DS, et al. Oxidative and endoplasmic reticulum stress defense mechanisms of bovine granulosa cells exposed to heat stress. Theriogenology 2018;110:130-41. https://doi.org/10.1016/j.theriogenology.2017.12.042
  27. Iurlaro R, Munoz-Pinedo C. Cell death induced by endoplasmic reticulum stress. FEBS J 2016;283:2640-52. https://doi.org/10.1111/febs.13598
  28. Gan L, Johnson JA. Oxidative damage and the Nrf2-ARE pathway in neurodegenerative diseases. Biochim Biophys Acta Mol Basis Dis 2014;1842:1208-18. https://doi.org/10.1016/j.bbadis.2013.12.011
  29. Stefanson AL, Bakovic M. Dietary regulation of Keap1/Nrf2/ARE pathway: focus on plant-derived compounds and trace minerals. Nutrients 2014;6:3777-801. https://doi.org/10.3390/nu6093777
  30. Han MH, Park C, Lee DS, et al. Cytoprotective effects of esculetin against oxidative stress are associated with the up-regulation of Nrf2-mediated NQO1 expression via the activation of the ERK pathway. Int J Mol Med 2017;39:380-6. https://doi.org/10.3892/ijmm.2016.2834

Cited by

  1. Cytoprotective Effects of Taurine on Heat-Induced Bovine Mammary Epithelial Cells In Vitro vol.10, pp.2, 2021, https://doi.org/10.3390/cells10020258
  2. 5-ALA Attenuates the Palmitic Acid-Induced ER Stress and Apoptosis in Bovine Mammary Epithelial Cells vol.26, pp.4, 2021, https://doi.org/10.3390/molecules26041183
  3. 5-Aminolevulinic Acid Attenuates Glucose-Regulated Protein 78 Expression and Hepatocyte Lipoapoptosis via Heme Oxygenase-1 Induction vol.22, pp.21, 2021, https://doi.org/10.3390/ijms222111405