Advancements in Genetic Biomarkers and Exogenous Antioxidant Supplementation for Safeguarding Mammalian Cells against Heat-Induced Oxidative Stress and Apoptosis.

Muhammad Zahoor Khan, Adnan Khan, Wenting Chen, Wenqiong Chai, Changfa Wang
Author Information
  1. Muhammad Zahoor Khan: Liaocheng Research Institute of Donkey High-Efficiency Breeding and Ecological Feeding, Liaocheng University, Liaocheng 522000, China. ORCID
  2. Adnan Khan: Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 511464, China. ORCID
  3. Wenting Chen: Liaocheng Research Institute of Donkey High-Efficiency Breeding and Ecological Feeding, Liaocheng University, Liaocheng 522000, China.
  4. Wenqiong Chai: Liaocheng Research Institute of Donkey High-Efficiency Breeding and Ecological Feeding, Liaocheng University, Liaocheng 522000, China.
  5. Changfa Wang: Liaocheng Research Institute of Donkey High-Efficiency Breeding and Ecological Feeding, Liaocheng University, Liaocheng 522000, China.

Abstract

Heat stress represents a pervasive global concern with far-reaching implications for the reproductive efficiency of both animal and human populations. An extensive body of published research on heat stress effects utilizes controlled experimental environments to expose cells and tissues to heat stress and its disruptive influence on the physiological aspects of reproductive phenotypic traits, encompassing parameters such as sperm quality, sperm motility, viability, and overall competence. Beyond these immediate effects, heat stress has been linked to embryo losses, compromised oocyte development, and even infertility across diverse species. One of the primary mechanisms underlying these adverse reproductive outcomes is the elevation of reactive oxygen species (ROS) levels precipitating oxidative stress and apoptosis within mammalian reproductive cells. Oxidative stress and apoptosis are recognized as pivotal biological factors through which heat stress exerts its disruptive impact on both male and female reproductive cells. In a concerted effort to mitigate the detrimental consequences of heat stress, supplementation with antioxidants, both in natural and synthetic forms, has been explored as a potential intervention strategy. Furthermore, reproductive cells possess inherent self-protective mechanisms that come into play during episodes of heat stress, aiding in their survival. This comprehensive review delves into the multifaceted effects of heat stress on reproductive phenotypic traits and elucidates the intricate molecular mechanisms underpinning oxidative stress and apoptosis in reproductive cells, which compromise their normal function. Additionally, we provide a succinct overview of potential antioxidant interventions and highlight the genetic biomarkers within reproductive cells that possess self-protective capabilities, collectively offering promising avenues for ameliorating the negative impact of heat stress by restraining apoptosis and oxidative stress.

Keywords

References

  1. Vet Sci. 2023 Mar 10;10(3): [PMID: 36977253]
  2. J Nutr. 2023 Dec;153(12):3373-3381 [PMID: 37923224]
  3. Theriogenology. 2023 Jan 15;196:79-87 [PMID: 36401935]
  4. Animals (Basel). 2019 Sep 24;9(10): [PMID: 31554289]
  5. Int J Mol Sci. 2023 Oct 11;24(20): [PMID: 37894737]
  6. Reprod Biol Endocrinol. 2013 Mar 21;11:23 [PMID: 23514035]
  7. Front Biosci (Schol Ed). 2010 Jan 01;2(2):685-96 [PMID: 20036977]
  8. Animals (Basel). 2021 Mar 12;11(3): [PMID: 33809236]
  9. J Trace Elem Med Biol. 2024 Jan;81:127320 [PMID: 37913559]
  10. Sci Rep. 2022 Sep 12;12(1):15322 [PMID: 36097009]
  11. Reprod Sci. 2021 Feb;28(2):371-380 [PMID: 32780358]
  12. Anim Reprod Sci. 2016 Jul;170:25-37 [PMID: 27095614]
  13. Reprod Fertil. 2023 Jul 07;4(3): [PMID: 37276172]
  14. J Biol Chem. 2011 Nov 11;286(45):39387-402 [PMID: 21908612]
  15. Theriogenology. 2018 Jan 15;106:117-126 [PMID: 29049923]
  16. Food Chem. 2022 Jan 1;366:130611 [PMID: 34388403]
  17. Int J Mol Sci. 2023 May 16;24(10): [PMID: 37240155]
  18. Mol Cell Biol. 2013 Jun;33(12):2436-46 [PMID: 23589329]
  19. Cell Stress Chaperones. 2023 Nov;28(6):749-759 [PMID: 37610501]
  20. Trop Anim Health Prod. 2023 Oct 26;55(6):380 [PMID: 37882945]
  21. J Therm Biol. 2020 Oct;93:102683 [PMID: 33077109]
  22. J Dairy Sci. 2020 Oct;103(10):9525-9533 [PMID: 32747095]
  23. Reprod Fertil Dev. 2021 Jan;33(2):66-75 [PMID: 38769677]
  24. Cell Death Dis. 2019 Jul 17;10(8):541 [PMID: 31316051]
  25. Biol Reprod. 2005 Mar;72(3):667-77 [PMID: 15548731]
  26. J Biol Chem. 2010 May 28;285(22):16782-8 [PMID: 20378532]
  27. Biol Reprod. 2021 Nov 15;105(5):1114-1125 [PMID: 34296252]
  28. Theriogenology. 2024 Jan 15;214:148-156 [PMID: 37875054]
  29. Animals (Basel). 2021 Jun 16;11(6): [PMID: 34208520]
  30. J Anim Sci Biotechnol. 2020 Feb 18;11:25 [PMID: 32095238]
  31. Pharm Biol. 2016;54(5):905-18 [PMID: 26459670]
  32. J Hazard Mater. 2020 Apr 5;387:121706 [PMID: 31796358]
  33. Animals (Basel). 2020 Feb 27;10(3): [PMID: 32120945]
  34. Theriogenology. 2023 Apr 1;200:33-42 [PMID: 36739670]
  35. Antioxidants (Basel). 2022 Feb 02;11(2): [PMID: 35204189]
  36. Front Genet. 2021 Oct 29;12:699920 [PMID: 34777457]
  37. Vet Sci. 2021 Dec 13;8(12): [PMID: 34941853]
  38. Theriogenology. 2023 Apr 15;201:41-52 [PMID: 36827868]
  39. J Ginseng Res. 2019 Jan;43(1):135-142 [PMID: 30662302]
  40. Br Poult Sci. 2012;53(5):708-14 [PMID: 23281767]
  41. Pharm Biol. 2023 Dec;61(1):986-999 [PMID: 37386769]
  42. Environ Sci Pollut Res Int. 2019 Nov;26(33):34575-34583 [PMID: 31650475]
  43. Antioxidants (Basel). 2023 Aug 04;12(8): [PMID: 37627554]
  44. Anim Biotechnol. 2023 Dec;34(7):2626-2635 [PMID: 36000985]
  45. Crit Rev Food Sci Nutr. 2019;59(6):921-946 [PMID: 29993258]
  46. Biol Trace Elem Res. 2021 Feb;199(2):611-621 [PMID: 32385716]
  47. J Therm Biol. 2018 Jan;71:142-152 [PMID: 29301683]
  48. Theriogenology. 2023 Feb;197:127-132 [PMID: 36502590]
  49. Anim Reprod Sci. 2023 Sep;256:107319 [PMID: 37633109]
  50. J Equine Vet Sci. 2024 Jan;132:104961 [PMID: 37925113]
  51. J Res Health Sci. 2007 Jul 28;7(1):43-8 [PMID: 23343870]
  52. Biol Trace Elem Res. 2022 Feb;200(2):728-739 [PMID: 33738683]
  53. Front Immunol. 2022 Jan 18;12:820853 [PMID: 35116042]
  54. Reproduction. 2017 Jun;153(6):737-747 [PMID: 28428445]
  55. J Anim Sci. 2020 Aug 18;98(Suppl 1):S80-S87 [PMID: 32810254]
  56. Cell Tissue Res. 2022 Oct;390(1):23-33 [PMID: 35788899]
  57. J Reprod Dev. 2018 Jun 22;64(3):243-251 [PMID: 29553057]
  58. Front Endocrinol (Lausanne). 2022 Feb 24;13:838858 [PMID: 35282467]
  59. Theriogenology. 2018 Nov;121:42-52 [PMID: 30125827]
  60. Animals (Basel). 2023 Sep 06;13(18): [PMID: 37760231]
  61. Cells. 2022 Apr 25;11(9): [PMID: 35563749]
  62. Nat Commun. 2023 Apr 25;14(1):2152 [PMID: 37185667]
  63. Nat Rev Urol. 2017 Aug;14(8):470-485 [PMID: 28508879]
  64. Reprod Fertil Dev. 2023 May;35(8):492 [PMID: 37224073]
  65. Antioxidants (Basel). 2023 Oct 04;12(10): [PMID: 37891907]
  66. Biosci Biotechnol Biochem. 2023 Dec 19;88(1):53-62 [PMID: 37863837]
  67. Mol Cell Endocrinol. 2016 Mar 5;423:96-112 [PMID: 26772142]
  68. Int J Environ Res Public Health. 2015 Jul 15;12(7):8034-74 [PMID: 26184272]
  69. Animal. 2023 May;17 Suppl 1:100847 [PMID: 37567679]
  70. Theriogenology. 2023 Mar 15;199:131-137 [PMID: 36738591]
  71. J Dev Biol. 2023 Aug 29;11(3): [PMID: 37754838]
  72. Theriogenology. 2020 Dec;158:84-96 [PMID: 32947064]
  73. Arch Physiol Biochem. 2023 Oct 23;:1-11 [PMID: 37870938]
  74. Int J Mol Sci. 2021 Apr 28;22(9): [PMID: 33924958]
  75. J Dairy Sci. 2020 Oct;103(10):9502-9514 [PMID: 32713696]
  76. Int J Mol Sci. 2023 Jul 06;24(13): [PMID: 37446340]
  77. Food Funct. 2022 Mar 21;13(6):3247-3257 [PMID: 35233585]
  78. J Reprod Dev. 2016 Dec 20;62(6):561-569 [PMID: 27478062]
  79. Animals (Basel). 2022 Sep 09;12(18): [PMID: 36139219]
  80. Int J Reprod Biomed. 2018 Jul;16(7):447-454 [PMID: 30234185]
  81. J Biomed Sci. 2017 Sep 2;24(1):66 [PMID: 28865467]
  82. Int J Mol Sci. 2023 May 24;24(11): [PMID: 37298157]
  83. Reprod Sci. 2021 Nov;28(11):3123-3136 [PMID: 34231174]
  84. Food Funct. 2023 Feb 21;14(4):2200-2211 [PMID: 36756975]
  85. Reprod Fertil Dev. 2012;24(5):649-55 [PMID: 22697115]
  86. J Dairy Sci. 2020 Aug;103(8):6751-6770 [PMID: 32448584]
  87. Theriogenology. 2017 Mar 15;91:145-153 [PMID: 28215679]
  88. J Therm Biol. 2023 Jan;111:103403 [PMID: 36585082]
  89. Int J Mol Sci. 2022 Sep 22;23(19): [PMID: 36232461]
  90. Anim Reprod Sci. 2020 Feb;213:106277 [PMID: 31987328]
  91. J Therm Biol. 2023 Dec;118:103737 [PMID: 37944301]
  92. Br Poult Sci. 2009 Sep;50(5):641-7 [PMID: 19904644]
  93. Anim Biotechnol. 2023 Dec;34(8):3519-3532 [PMID: 36688617]
  94. Theriogenology. 2021 Mar 1;162:22-31 [PMID: 33418161]
  95. Theriogenology. 2023 Dec;212:181-188 [PMID: 37742481]
  96. Antioxidants (Basel). 2021 Nov 24;10(12): [PMID: 34942974]
  97. Animals (Basel). 2022 Apr 09;12(8): [PMID: 35454222]
  98. Earths Future. 2022 Nov;10(11):e2022EF002803 [PMID: 36582412]
  99. Biochim Biophys Acta Mol Basis Dis. 2023 Aug;1869(6):166742 [PMID: 37146914]
  100. Cells. 2022 Dec 16;11(24): [PMID: 36552837]
  101. Reprod Biol Endocrinol. 2015 Apr 26;13:37 [PMID: 25928197]
  102. Reprod Sci. 2021 Oct;28(10):2895-2905 [PMID: 33861392]
  103. Theriogenology. 2021 Apr 1;164:65-73 [PMID: 33556906]
  104. Anim Reprod Sci. 2020 Oct;221:106550 [PMID: 32861112]
  105. Molecules. 2020 Jan 28;25(3): [PMID: 32012916]
  106. Antioxidants (Basel). 2020 Nov 05;9(11): [PMID: 33167396]
  107. Reprod Toxicol. 2015 Nov;57:196-203 [PMID: 26103447]
  108. Andrologia. 2021 Oct;53(9):e14169 [PMID: 34197007]
  109. J Cell Physiol. 2019 Apr;234(4):3961-3972 [PMID: 30191981]
  110. J Therm Biol. 2018 Oct;77:14-23 [PMID: 30196893]
  111. Antioxidants (Basel). 2020 Feb 04;9(2): [PMID: 32033035]
  112. Zool Res. 2021 Jul 18;42(4):514-524 [PMID: 34254745]
  113. Front Cell Dev Biol. 2020 Nov 19;8:593005 [PMID: 33330475]
  114. Cell. 2014 Jul 3;158(1):25-40 [PMID: 24995976]
  115. J Therm Biol. 2019 May;82:63-69 [PMID: 31128660]
  116. J Dairy Sci. 2019 Dec;102(12):10695-10710 [PMID: 31521355]
  117. Pharm Biol. 2013 Feb;51(2):206-12 [PMID: 23116244]
  118. Anim Reprod Sci. 2012 Oct;134(3-4):125-34 [PMID: 22898494]
  119. Br J Pharmacol. 2024 Feb;181(3):393-412 [PMID: 37580308]
  120. Oxid Med Cell Longev. 2023 Feb 17;2023:1708251 [PMID: 36846717]
  121. Cell Stress Chaperones. 2018 Nov;23(6):1193-1204 [PMID: 29943101]
  122. Phytother Res. 2021 Jan;35(1):311-323 [PMID: 32767418]
  123. Mol Reprod Dev. 2019 Jun;86(6):673-685 [PMID: 30989754]
  124. J Reprod Dev. 2019 Apr 12;65(2):139-146 [PMID: 30686791]
  125. Theriogenology. 2022 Aug;188:100-107 [PMID: 35688039]
  126. J Pineal Res. 2022 Oct;73(3):e12819 [PMID: 35906194]
  127. Theriogenology. 2018 Jun;113:102-112 [PMID: 29477908]
  128. Biol Reprod. 2012 Nov 16;87(5):118 [PMID: 23018185]
  129. Andrologia. 2015 Dec;47(10):1109-19 [PMID: 25521483]
  130. J Biol Chem. 2007 Aug 17;282(33):24131-45 [PMID: 17580304]
  131. Anim Reprod Sci. 2014 Apr;146(1-2):55-62 [PMID: 24613013]
  132. J Ovarian Res. 2022 Mar 17;15(1):34 [PMID: 35300716]
  133. Antioxidants (Basel). 2022 Sep 12;11(9): [PMID: 36139870]
  134. Am J Physiol Endocrinol Metab. 2013 Jan 1;304(1):E87-99 [PMID: 23132297]
  135. Theriogenology. 2022 Jan 1;177:183-194 [PMID: 34715543]
  136. PeerJ. 2023 Apr 7;11:e15112 [PMID: 37065702]
  137. Andrologia. 2019 Apr;51(3):e13203 [PMID: 30467869]
  138. Syst Biol Reprod Med. 2020 Dec;66(6):400-409 [PMID: 32981384]
  139. Am J Reprod Immunol. 2012 May;67(5):376-82 [PMID: 22133191]
  140. J Ginseng Res. 2019 Jan;43(1):125-134 [PMID: 30662301]
  141. Animals (Basel). 2021 Nov 29;11(12): [PMID: 34944184]
  142. Theriogenology. 2017 Jan 15;88:215-227 [PMID: 27771118]
  143. Environ Int. 2023 Mar;173:107809 [PMID: 36805156]
  144. Reprod Domest Anim. 2020 Dec;55(12):1774-1783 [PMID: 33047406]
  145. Aging (Albany NY). 2019 Aug 12;11(15):5535-5547 [PMID: 31404912]
  146. Free Radic Biol Med. 2021 Feb 20;164:410-416 [PMID: 33482333]
  147. Theriogenology. 2022 Jun;185:6-15 [PMID: 35344833]
  148. Acta Histochem. 2014 Jun;116(5):883-90 [PMID: 24698288]
  149. Mol Hum Reprod. 2019 Sep 1;25(9):538-549 [PMID: 31553448]
  150. Biol Trace Elem Res. 2024 Jan;202(1):161-174 [PMID: 37127784]
  151. Reprod Sci. 2024 May;31(5):1311-1322 [PMID: 38180610]
  152. Animals (Basel). 2023 Jun 01;13(11): [PMID: 37889768]
  153. Vet Sci. 2022 Aug 18;9(8): [PMID: 36006354]
  154. Reprod Domest Anim. 2022 Jun;57(6):567-576 [PMID: 35147249]
  155. Antioxidants (Basel). 2023 Jul 11;12(7): [PMID: 37507946]
  156. J Anim Sci. 2017 Apr;95(4):1660-1668 [PMID: 28464088]
  157. Mol Cell Endocrinol. 2019 Dec 1;498:110546 [PMID: 31422101]
  158. Antioxid Redox Signal. 2022 Sep;37(7-9):481-500 [PMID: 34913729]
  159. J Hazard Mater. 2022 Mar 5;425:127571 [PMID: 34986559]
  160. Mol Cell Biol. 2010 Jul;30(13):3275-85 [PMID: 20421418]
  161. Antioxidants (Basel). 2019 Aug 02;8(8): [PMID: 31382427]
  162. Front Vet Sci. 2020 Jun 12;7:290 [PMID: 32596265]
  163. Reprod Fertil Dev. 2001;13(2-3):187-92 [PMID: 11720136]
  164. Reprod Domest Anim. 2023 Mar;58(3):423-430 [PMID: 36510757]
  165. Sci Rep. 2023 May 24;13(1):8427 [PMID: 37225872]
  166. Cell Biosci. 2013 Feb 06;3(1):9 [PMID: 23388203]
  167. J Anim Sci Technol. 2023 Jul;65(4):683-697 [PMID: 37970501]
  168. J Steroid Biochem Mol Biol. 2023 Jan;225:106181 [PMID: 36150639]
  169. Sci Rep. 2023 Sep 21;13(1):15671 [PMID: 37735181]
  170. Animal. 2018 Aug;12(8):1611-1620 [PMID: 29198215]
  171. Front Public Health. 2023 Oct 03;11:1282497 [PMID: 37854241]
  172. J Trace Elem Med Biol. 2023 Dec;80:127296 [PMID: 37659125]
  173. Biol Rev Camb Philos Soc. 2023 Apr;98(2):603-622 [PMID: 36412227]
  174. Theriogenology. 2020 Dec;158:477-489 [PMID: 33080451]
  175. Life (Basel). 2021 Mar 09;11(3): [PMID: 33803103]
  176. Theriogenology. 2018 Apr 1;110:130-141 [PMID: 29396041]
  177. Environ Pollut. 2024 Jan 15;341:122927 [PMID: 37977357]
  178. Front Endocrinol (Lausanne). 2019 Apr 16;10:224 [PMID: 31040821]
  179. Antioxidants (Basel). 2023 Feb 17;12(2): [PMID: 36830066]
  180. Blood. 2007 Jul 15;110(2):661-9 [PMID: 17420286]
  181. J Therm Biol. 2023 Feb;112:103438 [PMID: 36796894]
  182. Int J Mol Sci. 2014 Nov 14;15(11):21090-104 [PMID: 25405739]
  183. Environ Res. 2023 Nov 1;236(Pt 2):116665 [PMID: 37451571]
  184. Pharmaceuticals (Basel). 2023 Apr 10;16(4): [PMID: 37111327]
  185. Mol Hum Reprod. 2020 Feb 29;26(2):65-79 [PMID: 31943111]
  186. Sci Rep. 2022 May 25;12(1):8857 [PMID: 35614303]
  187. Theriogenology. 2023 Mar 1;198:61-68 [PMID: 36563629]
  188. J Therm Biol. 2023 Feb;112:103465 [PMID: 36796910]
  189. Toxicology. 2020 Sep;442:152556 [PMID: 32758512]
  190. Crit Care. 2016 Jul 14;20(1):199 [PMID: 27411704]
  191. J Dairy Sci. 2024 Apr;107(4):2111-2128 [PMID: 37923214]
  192. Exp Gerontol. 2014 May;53:57-66 [PMID: 24594315]
  193. Front Endocrinol (Lausanne). 2023 Apr 05;14:1149284 [PMID: 37091849]
  194. Mol Cell Biol. 2004 Oct;24(19):8477-86 [PMID: 15367669]
  195. Theriogenology. 2020 Oct 1;155:150-156 [PMID: 32679440]
  196. Theriogenology. 2017 Oct 15;102:48-53 [PMID: 28743027]
  197. Int J Hyperthermia. 2014 Nov;30(7):513-23 [PMID: 25354680]
  198. Front Cell Dev Biol. 2023 Apr 06;11:1142629 [PMID: 37091982]
  199. Biosci Rep. 2021 Jun 25;41(6): [PMID: 34060622]
  200. Animals (Basel). 2023 Jul 19;13(14): [PMID: 37508136]
  201. Ecotoxicol Environ Saf. 2023 Mar 1;252:114598 [PMID: 36774800]
  202. J Occup Environ Hyg. 2016 Nov;13(11):847-65 [PMID: 27115294]
  203. Theriogenology. 2020 Sep 1;153:62-67 [PMID: 32442741]
  204. Redox Rep. 2022 Dec;27(1):45-52 [PMID: 35213291]
  205. Anim Reprod Sci. 2020 May;216:106348 [PMID: 32414470]
  206. Res Vet Sci. 2022 Dec 20;152:717-725 [PMID: 36270181]
  207. Theriogenology. 2020 May;148:112-121 [PMID: 32171970]
  208. Gen Comp Endocrinol. 2014 Nov 1;208:12-20 [PMID: 25260249]
  209. J Therm Biol. 2018 Jan;71:32-40 [PMID: 29301698]
  210. Animals (Basel). 2023 Apr 05;13(7): [PMID: 37048516]
  211. Theriogenology. 2022 Jan 15;178:85-94 [PMID: 34808561]
  212. Reprod Sci. 2023 Jun;30(6):1938-1951 [PMID: 36538028]
  213. Mol Reprod Dev. 2019 Oct;86(10):1307-1323 [PMID: 30767310]
  214. Hum Reprod. 2022 May 30;37(6):1207-1228 [PMID: 35459945]
  215. Reprod Fertil Dev. 2020 Jun;32(10):885-892 [PMID: 32586418]
  216. Anim Reprod Sci. 2021 Jan;224:106665 [PMID: 33307488]

Word Cloud

Created with Highcharts 10.0.0stressreproductiveheatcellsapoptosisoxidativeeffectsmechanismsdisruptivephenotypictraitsspermspecieswithinmammalianOxidativeimpactantioxidantspotentialpossessself-protectiveHeatrepresentspervasiveglobalconcernfar-reachingimplicationsefficiencyanimalhumanpopulationsextensivebodypublishedresearchutilizescontrolledexperimentalenvironmentsexposetissuesinfluencephysiologicalaspectsencompassingparametersqualitymotilityviabilityoverallcompetenceBeyondimmediatelinkedembryolossescompromisedoocytedevelopmenteveninfertilityacrossdiverseOneprimaryunderlyingadverseoutcomeselevationreactiveoxygenROSlevelsprecipitatingrecognizedpivotalbiologicalfactorsexertsmalefemaleconcertedeffortmitigatedetrimentalconsequencessupplementationnaturalsyntheticformsexploredinterventionstrategyFurthermoreinherentcomeplayepisodesaidingsurvivalcomprehensivereviewdelvesmultifacetedelucidatesintricatemolecularunderpinningcompromisenormalfunctionAdditionallyprovidesuccinctoverviewantioxidantinterventionshighlightgeneticbiomarkerscapabilitiescollectivelyofferingpromisingavenuesamelioratingnegativerestrainingAdvancementsGeneticBiomarkersExogenousAntioxidantSupplementationSafeguardingMammalianCellsHeat-InducedStressApoptosisfertility

Similar Articles

Cited By