Plasma oxidative stress in reproduction of two eusocial African mole-rat species, the naked mole-rat and the Damaraland mole-rat

Frontiers in Zoology - Tập 18 - Trang 1-9 - 2021
Paul Juan Jacobs1, Daniel William Hart1, Nigel Charles Bennett1
1Department of Zoology and Entomology, Mammal Research Institute, University of Pretoria, Pretoria, South Africa

Tóm tắt

One of the most prominent life-history trade-offs involves the cost of reproduction. Oxidative stress has been proposed to be involved in this trade-off and has been associated with reduced life span. There is currently an unclear relationship between oxidative cost and the reproduction-longevity trade-off. The current study, using a non-lethal and minimally invasive (only a single blood sample and no euthanasia) method, investigated whether an oxidative cost (oxidative stress) to reproduction would be apparent in two long-lived eusocial mole-rats, the naked mole-rat (NMR), Heterocephalus glaber, and the Damaraland mole-rat (DMR), Fukomys damarensis, where breeding colony members live longer than non-breeder conspecifics. We measured the direct redox balance in plasma by measuring the oxidative stress index (OSI) based on the ratio of total oxidant status and total antioxidant activity in breeders and non-breeders of both sexes, in the two species. NMR had significantly higher OSI between breeders and non-breeders of each sex, whereas DMR showed no significant differences except for total antioxidant capacity (TAC). The mode of reproductive suppression and the degree of reproductive investment in NMR may explain to some degree the redox balance difference between breeders and non-breeders. DMR show minimal physiological changes between breeders and non-breeders except for the mode of reproduction, which may explain some variations in TAC and TOS values, but similar OSI between breeders and non-breeders.

Tài liệu tham khảo

Speakman JR, Blount JD, Bronikowski AM, Buffenstein R, Isaksson C, Kirkwood TB, Monaghan P, Ozanne SE, Beaulieu M, Briga M. Oxidative stress and life histories: unresolved issues and current needs. Ecol Evol. 2015;5:5745–57. Garratt M, Vasilaki A, Stockley P, McArdle F, Jackson M, Hurst JL. Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc R Soc B Biol Sci. 2010;278:1098–106. Blount JD, Vitikainen EI, Stott I, Cant MA. Oxidative shielding and the cost of reproduction. Biol Rev. 2016;91:483–97. Sies H. Oxidative stress: oxidants and antioxidants. Cambridge: Academic Press; 1991. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000;408:239. Costantini D. Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett. 2008;11:1238–51. Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47–95. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest. 2005;115:500–8. Blair AS, Hajduch E, Litherland GJ, Hundal HS. Regulation of glucose transport and glycogen synthesis in L6 muscle cells during oxidative stress evidence for cross-talk between the insulin and sapk2/p38 mitogen-activated protein kinase signaling pathways. J Biol Chem. 1999;274:36293–9. Sies H. Oxidative stress: a concept in redox biology and medicine. Redox Biol. 2015;4:180–3. Oliveira MF, Geihs MA, França TF, Moreira DC, Hermes-Lima M. Is “preparation for oxidative stress” a case of physiological conditioning hormesis? Front Physiol. 2018;9:945. Burg MB, Ferraris JD, Dmitrieva NI. Cellular response to hyperosmotic stresses. Physiol Rev. 2007;87:1441–74. Williams GC. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat. 1966;100:687–90. Benton T. The evolution of Life-histories. J Anim Ecol. 1993;62:796–7. Lemaître JF, Gaillard JM. Reproductive senescence: new perspectives in the wild. Biol Rev. 2017;92:2182–99. Brooks RC, Garratt MG. Life history evolution, reproduction, and the origins of sex-dependent aging and longevity. Annal NY Acad Sci. 2017;1389:92–107. Speakman JR. The physiological costs of reproduction in small mammals. Philos Trans R Soc B. 2008;363:375–98. Harshman LG, Zera AJ. The cost of reproduction: the devil in the details. Trends Ecol Evol. 2007;22:80–6. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G. Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett. 2004;7:363–8. Stier A, Reichert S, Massemin S, Bize P, Criscuolo F. Constraint and cost of oxidative stress on reproduction: correlative evidence in laboratory mice and review of the literature. Front Zool. 2012;9:37. Sainz R, Reiter R, Mayo J, Cabrera J, Tan D, Qi W, Garcia J. Changes in lipid peroxidation during pregnancy and after delivery in rats: effect of pinealectomy. J Reprod Fertil. 2000;119:143–50. Metcalfe NB, Monaghan P. Does reproduction cause oxidative stress? An open question. Trend Ecol Evol. 2013;28:347–50. Costantini D. Commentary: oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. Front Ecol Evol. 2016;4:10. Speakman JR, Garratt M. Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. BioEssays. 2014;36:93–106. Wiersma P, Selman C, Speakman JR, Verhulst S. Birds sacrifice oxidative protection for reproduction. Proc R Soc Lond B Biol Sci. 2004;271:S360–3. Costantini D. Oxidative stress and hormesis in evolutionary ecology and physiology: a marriage between mechanistic and evolutionary approaches. Berlin: Springer; 2014. Novikov E, Kondratyuk E, Petrovski D, Titova T, Zadubrovskaya I, Zadubrovskiy P, Moshkin M. Reproduction, aging and mortality rate in social subterranean mole voles (Ellobius talpinus Pall.). Biogerontology. 2015;16:723–32. Fischer D, Patchev V, Hellbach S, Hassan A, Almeida O. Lactation as a model for naturally reversible hypercorticalism plasticity in the mechanisms governing hypothalamo-pituitary-adrenocortical activity in rats. J Clin Invest. 1995;96:1208–15. Palmer C. Animal ethics in context. New York: Columbia University Press; 2010. Norris DO, Lopez KH. Hormones and reproduction of vertebrates. Cambridge: Academic Press; 2010. Buffenstein R. Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Comp Physiol B. 2008;178:439–45. Buffenstein R. The naked mole-rat: a new long-living model for human aging research. J Gerontol A Biol Sci Med Sci. 2005;60:1369–77. Schmidt CM, Blount JD, Bennett NC. Reproduction is associated with a tissue-dependent reduction of oxidative stress in eusocial female Damaraland mole-rats (Fukomys damarensis). PLOS ONE. 2014;9:e103286. Schmidt CM, Jarvis JU, Bennett NC. The long-lived queen: reproduction and longevity in female eusocial Damaraland mole-rats (Fukomys damarensis). Afr Zool. 2013;48:193–6. Jarvis J, Bennett N. Eusociality has evolved independently in two genera of bathyergid mole-rats—but occurs in no other subterranean mammal. Behav Ecol Sociobiol. 1993;33:253–60. Bennett NC, Faulkes CG. African mole-rats: ecology and eusociality. Cambridge: Cambridge University Press; 2000. Sherman PW, Lacey EA, Reeve HK, Keller L. The eusociality continuum. Behav Ecol. 1995;6:102–8. Burland TM, Bennett NC, Jarvis JU, Faulkes CG. Colony structure and parentage in wild colonies of co-operatively breeding Damaraland mole-rats suggest incest avoidance alone may not maintain reproductive skew. Mol Ecol. 2004;13:2371–9. Clarke F, Faulkes C. Dominance and queen succession in captive colonies of the eusocial naked mole–rat, Heterocephalus glaber. Proc R Soc Lond B Biol Sci. 1997;264:993–1000. Clarke F, Miethe G, Bennett N. Reproductive suppression in female Damaraland mole–rats Cryptomys damarensis: dominant control or self–restraint? Proc R Soc Lond B Biol Sci. 2001;268:899–909. Sahm A, Platzer M, Koch P, Henning Y, Bens M, Groth M, Burda H, Begall S, Ting S, Goetz M, et al. Increased longevity due to sexual activity in mole-rats is associated with transcriptional changes in the HPA stress axis. Elife. 2021;10:e57843. Bennett NC, Faulkes CG, Molteno AJ. Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: two components to a lifetime of socially induced infertility. Proc Biol Sci. 1996;263:1599–603. Faulkes CG, Bennett NC. Plasticity and constraints on social evolution in African mole-rats: ultimate and proximate factors. Philos Trans R Soc B. 2013;368:20120347. Lewis KN, Andziak B, Yang T, Buffenstein R. The naked mole-rat response to oxidative stress: just deal with it. Antioxid Redox Sign. 2013;19:1388–99. Dammann P, Šumbera R, Maßmann C, Scherag A, Burda H. Extended longevity of reproductives appears to be common in Fukomys mole-rats (Rodentia, Bathyergidae). PLOS ONE. 2011;6:e18757. Dammann P, Burda H: Senescence patterns in African mole-rats (Bathyergidae, Rodentia). In: Subterranean rodents. Springer; 2007; pp. 251–263. Michener CD. Comparative social behavior of bees. Annu Rev Entomol. 1969;14:299–342. Faulkes C, Trowell S, Jarvis J, Bennett N. Investigation of numbers and motility of spermatozoa in reproductively active and socially suppressed males of two eusocial African mole-rats, the naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Cryptomys damarensis). Reproduction. 1994;100:411–6. Bennett NC, Ganswindt A, Ganswindt SB, Jarvis J, Zöttl M, Faulkes C. Evidence for contrasting roles for prolactin in eusocial naked mole-rats, Heterocephalus glaber and Damaraland mole-rats Fukomys damarensis. Biol Lett. 2018;14:20180150. Medger K, Bennett NC, Ganswindt SB, Ganswindt A, Hart DW. Changes in prolactin, cortisol and testosterone concentrations during queen succession in a colony of naked mole-rats (Heterocephalus glaber): a case study. Sci Nat. 2019;106:1–7. Voigt C, Medger K, Bennett N. The oestrous cycle of the Damaraland mole-rat revisited: evidence for induced ovulation. J Zool. 2021;314:85–95. Lutermann H, Young AJ, Bennett NC. Reproductive status and testosterone among females in cooperative mole-rat societies. Gen Comp Endocr. 2013;187:60–5. Voigt C, Bennett NC. Reproductive status-dependent kisspeptin and RF amide-related peptide (Rfrp) gene expression in female Damaraland mole-rats. J Neuroendocrinol. 2018;30:e12571. Rickard C, Bennett N. Recrudescence of sexual activity in a reproductively quiescent colony of the Damaraland mole-rat (Cryptomys damarensis), by the introduction of an unfamiliar and genetically unrelated male—a case of incest avoidance in ‘queenless’ colonies. J Zool. 1997;241:185–202. Christensen LL, Selman C, Blount JD, Pilkington JG, Watt KA, Pemberton JM, Reid JM, Nussey DH. Plasma markers of oxidative stress are uncorrelated in a wild mammal. Ecol Evol. 2015;5:5096–108. Giustarini D, Tsikas D, Colombo G, Milzani A, Dalle-Donne I, Fanti P, Rossi R. Pitfalls in the analysis of the physiological antioxidant glutathione (GSH) and its disulfide (GSSG) in biological samples: An elephant in the room. J Chromatogr B. 2016;1019:21–8. Giustarini D, Dalle-Donne I, Milzani A, Fanti P, Rossi R. Analysis of GSH and GSSG after derivatization with N-ethylmaleimide. Nat Protoc. 2013;8:1660. Zöttl M, Vullioud P, Mendonça R, Ticó MT, Gaynor D, Mitchell A, Clutton-Brock T. Differences in cooperative behavior among Damaraland mole rats are consequences of an age-related polyethism. Proc Natl Acad Sci. 2016;113:10382–7. Faulkes C, Abbott D, Jarvis J. Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats Heterocephalus glaber. Reproduction. 1990;88:559–68. Bennett NC, Jarvis JU. The social structure and reproductive biology of colonies of the mole-rat, Cryptomys damarensis (Rodentia, Bathyergidae). J Mammal. 1988;69:293–302. Oosthuizen MK, Cooper HM, Bennett NC. Circadian rhythms of locomotor activity in solitary and social species of African mole-rats (family: Bathyergidae). J Biol Rhythms. 2003;18:481–90. Erel O. A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem. 2004;37:112–9. Bitiren M, Karakilcik AZ, Zerin M, Ozardalı I, Selek S, Nazlıgül Y, Ozgonul A, Musa D, Uzunkoy A. Protective effects of selenium and vitamin E combination on experimental colitis in blood plasma and colon of rats. Biol Trace Elem Res. 2010;136:87–95. Team RDC: R Foundation for Statistical Computing, Vienna, available at: http://www.R-project.org 2018. Bates D, Kliegl R, Vasishth S, Baayen H: Parsimonious mixed models. arXiv:150604967; 2015. Ivy CM, Sprenger RJ, Bennett NC, van Jaarsveld B, Hart DW, Kirby AM, Yaghoubi D, Storey KB, Milsom WK, Pamenter ME. The hypoxia tolerance of eight related African mole-rat species rivals that of naked mole-rats, despite divergent ventilatory and metabolic strategies in severe hypoxia. Acta Physiol. 2020;228:13436. Garland T Jr, Adolph SC. Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool. 1994;67:797–828. Andziak B, O’Connor TP, Qi W, DeWaal EM, Pierce A, Chaudhuri AR, Van Remmen H, Buffenstein R. High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell. 2006;5:463–71. Sherman PW, Braude S, Jarvis JU. Litter sizes and mammary numbers of naked mole-rats: breaking the one-half rule. J Mammal. 1999;80:720–33. Alonso-Alvarez C, Canelo T, Romero-Haro AÁ. The oxidative cost of reproduction: theoretical questions and alternative mechanisms. Bioscience. 2017;67:258–70. Nna V, Akpan U, Osim E. Hyperprolactinemia contributes to reproductive deficit in male rats chronically administered PDE5 inhibitors (sildenafil and tadalafil) and opioid (tramadol). Asian Pac J Reprod. 2016;5:381–6. Levine S, Muneyyirci-Delale O. Stress-induced hyperprolactinemia: pathophysiology and clinical approach. Obstet Gynecol Int. 2018;2018:1–6. Miller AA, De Silva TM, Jackman KA, Sobey CG. Effect of gender and sex hormones on vascular oxidative stress. Clin Exp Pharmacol P. 2007;34:1037–43. Strehlow K, Rotter S, Wassmann S, Adam O, Grohé C, Laufs K, Böhm M, Nickenig G. Modulation of antioxidant enzyme expression and function by estrogen. Circ Res. 2003;93:170–7. Wassmann K, Wassmann S, Nickenig G. Progesterone antagonizes the vasoprotective effect of estrogen on antioxidant enzyme expression and function. Circ Res. 2005;97:1046–54. Yuan X-H, Fan Y-Y, Yang C-R, Gao X-R, Zhang L-L, Hu Y, Wang Y-Q, Jun H. Progesterone amplifies oxidative stress signal and promotes NO production via H2O2 in mouse kidney arterial endothelial cells. J Steroid Biochem Mol Biol. 2016;155:104–11. Metcalfe NB, Alonso-Alvarez C. Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol. 2010;24:984–96. Ismail DI, Yousry MM. The effectiveness of resveratrol in protection against histological alterations induced by hyperprolactinemia in reproductive organs of female albino rats. Egypt J Histol. 2018;41:123–39. Ahmadi A, Mostafavi M: Dose hyperprolactinemia induce reactive oxygen species (ROS) generation in the testis of adult male mice?. Cell J (Yakhteh) 2013, 15. Un-Nahar Z, Ali M, Biswas S, Kamrun N, Bashar T, Arslan M. Study of seminal MDA level as a oxidative stress marker in infertile male. J Sci Found. 2011;9:85–93. Lewis KN, Mele J, Hayes JD, Buffenstein R. Nrf2, a guardian of healthspan and gatekeeper of species longevity. Integr Comp Biol. 2010;50:829–43. Lewis KN, Wason E, Edrey YH, Kristan DM, Nevo E, Buffenstein R. Regulation of Nrf2 signaling and longevity in naturally long-lived rodents. Proc Natl Acad Sci. 2015;112:3722–7. De Waal EM, Liang H, Pierce A, Hamilton RT, Buffenstein R, Chaudhuri AR. Elevated protein carbonylation and oxidative stress do not affect protein structure and function in the long-living naked-mole rat: a proteomic approach. Biochem Biophys Res Commun. 2013;434:815–9. Pérez VI, Buffenstein R, Masamsetti V, Leonard S, Salmon AB, Mele J, Andziak B, Yang T, Edrey Y, Friguet B. Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc Natl Acad Sci. 2009;106:3059–64. Hulbert AJ, Turner N, Hinde J, Else P, Guderley H. How might you compare mitochondria from different tissues and different species? J Comp Physiol B. 2006;176:93–105. Mitchell TW, Buffenstein R, Hulbert A. Membrane phospholipid composition may contribute to exceptional longevity of the naked mole-rat (Heterocephalus glaber): a comparative study using shotgun lipidomics. Exp Gerontol. 2007;42:1053–62. MacRae SL, Croken MM, Calder R, Aliper A, Milholland B, White RR, Zhavoronkov A, Gladyshev VN, Seluanov A, Gorbunova V. DNA repair in species with extreme lifespan differences. Aging (Albany NY). 2015;7:1171. Zuo L, Christofi FL, Wright VP, Liu CY, Merola AJ, Berliner LJ, Clanton TL. Intra-and extracellular measurement of reactive oxygen species produced during heat stress in diaphragm muscle. Am J Physiol Cell Ph. 2000;279:C1058–66. Lee B, Smith M, Buffenstein R, Harries L: Negligible senescence in naked mole rats may be a consequence of well-maintained splicing regulation. GeroScience 2020; pp. 1–19. Lewis KN, Buffenstein R: The naked mole-rat: a resilient rodent model of aging, longevity, and healthspan. In: Handbook of the biology of aging. Elsevier; 2016; pp. 179–204 Young AJ, Oosthuizen MK, Lutermann H, Bennett NC. Physiological suppression eases in Damaraland mole-rat societies when ecological constraints on dispersal are relaxed. Horm Behav. 2010;57:177–83. Council NR. Guide for the care and use of laboratory animals. Washington, DC: National Academies Press; 2010.