期刊论文详细信息
BMC Evolutionary Biology
Endogenous ROS levels in C. elegans under exogenous stress support revision of oxidative stress theory of life-history tradeoffs
Suzanne Estes4  Dee R Denver3  Leigh C Latta1  Samson W Smith2 
[1] Biology Department, Reed College, Portland, 97202, OR, USA;Current address: Department of Biology and Microbiology, South Dakota State University, Brookings, 57007, SD, USA;Department of Zoology, Oregon State University, Corvallis, 97331, OR, USA;Department of Biology, Portland State University, Portland, 97201, OR, USA
关键词: Resource allocation;    Lifespan;    Free radicals;    Fitness;    Aging;   
Others  :  1118122
DOI  :  10.1186/s12862-014-0161-8
 received in 2014-04-22, accepted in 2014-07-14,  发布年份 2014
PDF
【 摘 要 】

Background

The oxidative stress theory of life-history tradeoffs states that oxidative stress caused by damaging free radicals directly underpins tradeoffs between reproduction and longevity by altering the allocation of energetic resources between these tasks. We test this theory by characterizing the effects of exogenous oxidative insult and its interaction with thermal stress and diet quality on a suite of life-history traits and correlations in Caenorhabditis elegans nematodes. We also quantify demographic aging rates and endogenous reactive oxygen species (ROS) levels in live animals.

Results

Our findings indicate a tradeoff between investment in reproduction and antioxidant defense (somatic maintenance) consistent with theoretical predictions, but correlations between standard life-history traits yield little evidence that oxidative stress generates strict tradeoffs. Increasing oxidative insult, however, shows a strong tendency to uncouple positive phenotypic correlations and, in particular, to reduce the correlation between reproduction and lifespan. We also found that mild oxidative insult results in lower levels of endogenous ROS accompanied by hormetic changes in lifespan, demographic aging, and reproduction that disappear in combined-stress treatments--consistent with the oxidative stress theory of aging.

Conclusions

Our findings demonstrate that oxidative stress is a direct contributor to life-history trait variation and that traditional tradeoffs are not necessary to invoke oxidative stress as a mediator of relationships between life-history traits, supporting previous calls for revisions to theory.

【 授权许可】

   
2014 Smith et al.; licensee BioMed Central Ltd

【 预 览 】
附件列表
Files Size Format View
20150206020924234.pdf 497KB PDF download
Figure 3. 17KB Image download
Figure 2. 51KB Image download
Figure 1. 14KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】
  • [1]Stearns SC: Trade-offs in life-history evolution. Funct Ecol 1989, 3:259-268.
  • [2]Zera AJ, Harshman LG: The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 2001, 32:95-126.
  • [3]Monaghan P, Metcalfe NB, Torres R: Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 2009, 12:75-92.
  • [4]Blount JD: Carotenoids and life-history evolution in animals. Arch Biochem Biophys 2004, 430:10-15.
  • [5]Kirkwood TBL: Evolution of ageing. Nature 1977, 270:301-304.
  • [6]Kirkwood TBL: Understanding the odd science of aging. Cell 2005, 120:437-447.
  • [7]Kirkwood TB, Austad SN: Why do we age? Nature 2000, 408:233-238.
  • [8]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, 7:363-368.
  • [9]Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Chastel O, Sorci G: An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution (N Y) 2006, 60:1913-1924.
  • [10]Klass MR: Aging in the nematodeCaenorhabditis elegans: major biological and environmental factors influencing life span.Mech Ageing Dev 1977, 6:413–429.
  • [11]Reznick D, Nunney L, Tessier A: Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 2000, 15:421-425.
  • [12]Van Noordwijk AJ, De Jong G: Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 1986, 128:137-142.
  • [13]Wang Y, Salmon AB, Harshman LG: A cost of reproduction: oxidative stress susceptibility is associated with increased egg production inDrosophila melanogaster.Exp Gerontol 2001, 36:1349–1359.
  • [14]Chippindale AK, Chu TJF, Rose MR: Complex trade-offs and the evolution of starvation resistance inDrosophila melanogaster.Evolution (N Y) 1996, 50:753–766.
  • [15]Speakman JR, Garratt M: Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. Bioessays 2014, 36:93-106.
  • [16]Dowling DK, Simmons LW: Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 2009, 276:1737-1745.
  • [17]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, 24:984-996.
  • [18]Harshman LG, Zera AJ: The cost of reproduction: the devil in the details. Trends Ecol Evol 2007, 22:80-86.
  • [19]Selman C, Blount JD, Nussey DH, Speakman JR: Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 2012, 27:570-577.
  • [20]Gems D, Doonan R: Antioxidant defense and aging inC. elegans: Is the oxidative damage theory of aging wrong?Cell Cycle 2009, 8:1681–1687.
  • [21]Metcalfe NB, Monaghan P: Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 2013, 28:347-350.
  • [22]Murphy MP: How mitochondria produce reactive oxygen species. Biochem J 2009, 417:1-13.
  • [23]Cabiscol E, Tamarit J, Ros J: Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 2000, 3:3-8.
  • [24]Wenk J, Brenneisen P, Meewes C, Wlaschek M, Peters T, Blaudschun R, Ma W, Kuhr L, Schneider L, Scharffetter-Kochanek K: UV-induced oxidative stress and photoaging. Curr Probl Dermatol 2001, 29:83-94.
  • [25]Finkel T, Holbrook NJ: Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
  • [26]Beckman KB, Ames BN: The free radical theory of aging matures. Physiol Rev 1998, 78:547-581.
  • [27]Klass M, Nguyen PN, Dechavigny A: Age-correlated changes in the DNA template in the nematodeCaenorhabditis elegans.Mech Ageing Dev 1983, 22:253–263.
  • [28]Richter C, Park JW, Ames BN: Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci U S A 1988, 85:6465-6467.
  • [29]Anson R, Bohr V: Mitochondria, oxidative DNA damage, and aging. J Am Aging Assoc 2000, 23:199-218.
  • [30]Hartman PS, Ishii N, Kayser EB, Morgan PG, Sedensky MM: Mitochondrial mutations differentially affect aging, mutability and anesthetic sensitivity inCaenorhabditis elegans.Mech Ageing Dev 2001, 122:1187–1201.
  • [31]Tzou P, De Gregorio E, Lemaitre B: How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr Opin Microbiol 2002, 5:102-110.
  • [32]Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J: Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007, 39:44-84.
  • [33]Van Raamsdonk JM, Hekimi S: Reactive oxygen species and aging inCaenorhabditis elegans: causal or casual relationship?Antioxid Redox Signal 2010, 13:1911–1953.
  • [34]Van Raamsdonk JM, Hekimi S: Superoxide dismutase is dispensable for normal animal lifespan. Proc Natl Acad Sci U S A 2012, 109:5785-5790.
  • [35]Doonan R, McElwee JJ, Matthijssens F, Walker GA, Houthoofd K, Back P, Matscheski A, Vanfleteren JR, Gems D: Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span inCaenorhabditis elegans.Genes Dev 2008, 22:3236–3241.
  • [36]Burmeister C, Luersen K, Heinick A, Hussein A, Domagalski M, Walter RD, Liebau E: Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1). FASEB J 2008, 22:343-354.
  • [37]Yen K, Patel HB, Lublin AL, Mobbs CV: SOD isoforms play no role in lifespan in ad lib or dietary restricted conditions, but mutational inactivation of SOD-1 reduces life extension by cold. Mech Ageing Dev 2009, 130:173-178.
  • [38]Van Raamsdonk JM, Hekimi S: Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan inCaenorhabditis elegans.PloS Genet 2009, 5:e1000361.
  • [39]Pun PB, Gruber J, Tang SY, Schaffer S, Ong RL, Fong S, Ng LF, Cheah I, Halliwell B: Ageing in nematodes: do antioxidants extend lifespan inCaenorhabditis elegans?Biogerontology 2010, 11:17–30.
  • [40]Gruber J, Ng LF, Poovathingal SK, Halliwell B: Deceptively simple but simply deceptive–Caenorhabditis eleganslifespan studies: considerations for aging and antioxidant effects.FEBS Lett 2009, 583:3377–3387.
  • [41]Keaney M, Matthijssens F, Sharpe M, Vanfleteren J, Gems D: Superoxide dismutase mimetics elevate superoxide dismutase activity in vivo but do not retard aging in the nematodeCaenorhabditis elegans.Free Radic Biol Med 2004, 37:239–250.
  • [42]Bronikowski A, Flatt T: Aging and its demographic measurement. Nat Educ Knowl 2010, 3:1-6.
  • [43]Walker DW, McColl G, Jenkins NL, Harris J, Lithgow GJ: Evolution of lifespan inC. elegans.Nature 2000, 405:296–297.
  • [44]Wu D, Tedesco PM, Phillips PC, Johnson TE: Fertility/longevity trade-offs under limiting-male conditions in mating populations ofCaenorhabditis elegans.Exp Gerontol 2012, 47:759–763.
  • [45]Yang W, Tiffany-Castiglioni E: The bipyridyl herbicide paraquat produces oxidative stress-mediated toxicity in human neuroblastoma SH-SY5Y cells: relevance to the dopaminergic pathogenesis. J Toxicol Env Heal A 2005, 68:1939-1961.
  • [46]Bus JS, Aust SD, Gibson JE: Paraquat toxicity: proposed mechanism of action involving lipid peroxidation. Environ Health Perspect 1976, 16:139-146.
  • [47]Joyner-Matos J, Hicks KA, Cousins D, Keller M, Denver DR, Baer CF, Estes S: Evolution of a higher intracellular oxidizing environment inCaenorhabditis elegansunder relaxed selection.PLoS One 2013, 8:e65604.
  • [48][http://www.wormbook.org] webcite Stiernagle T: Maintenance ofC. elegans. In WormBook. Edited by The C. elegans Research Community. 2006. doi/10.1895/wormbook.1.101.1, .
  • [49]Winterbourn CC: Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 2008, 4:278-286.
  • [50]Ishii N, Takahashi K, Tomita S, Keino T, Honda S, Yoshino K, Suzuki K: A methyl viologen-sensitive mutant of the nematodeCaenorhabditis elegans.Mutat Res 1990, 237:165–171.
  • [51]Hassan HM, Fridovich I: Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds. Arch Biochem Biophys 1979, 196:385-395.
  • [52]Gems D, Doonan R: Oxidative stress and ageing in the nematodeCaenorhabditis elegans. In Oxidative Stress in Aging. Humana Press, New York, NY; 2008:81–110.
  • [53]Anderson JL, Albergotti L, Ellebracht B, Huey RB, Phillips PC: Does thermoregulatory behavior maximize reproductive fitness of natural isolates ofCaenorhabditis elegans?BMC Evol Biol 2011, 11:157.
  • [54]Anderson JL, Albergotti L, Proulx S, Peden C, Huey RB, Phillips PC: Thermal preference ofCaenorhabditis elegans: a null model and empirical tests.J Exp Biol 2007, 210(Pt 17):3107–3116.
  • [55]Zuo W, Moses ME, West GB, Hou C, Brown JH: A general model for effects of temperature on ectotherm ontogenetic growth and development. Proc Biol Sci 2011, 279:1840-1846.
  • [56]Harvey SC, Viney ME: Thermal variation reveals natural variation between isolates ofCaenorhabditis elegans.J Exp Zool B Mol Dev Evol 2007, 308:409–416.
  • [57]Byerly L, Cassada RC, Russell RL: The life cycle of the nematodeCaenorhabditis elegans, I: wild-type growth and reproduction.Dev Biol 1976, 51:23–33.
  • [58]Goranson N, Ebersole J, Brault S: Resolving an adaptive conundrum: reproduction inCaenorhabditis elegansis not sperm-limited when food is scarce.Evol Ecol Res 2005, 7:325–333.
  • [59][http://www.wormbook.org] webcite Hubbard EJA, Greenstein D, The C. elegans Research Community: Introduction to the Germ line. In WormBook, WormBook 2005.;. doi:10.1895/wormbook.1.18.1, .
  • [60]Cutter AD: Sperm-limited fecundity in nematodes: how many sperm are enough? Evolution 2004, 58:651-655.
  • [61]Garigan D, Hsu A-L, Fraser AG, Kamath RS, Ahringer J, Kenyon C: Genetic analysis of tissue aging inCaenorhabditis elegans: a role for heat-shock factor and bacterial proliferation.Genetics 2002, 161:1101–1112.
  • [62]Gems D, Riddle DL: Genetic, behavioral and environmental determinants of male longevity inCaenorhabditis elegans.Genetics 2000, 154:1597–1610.
  • [63]Sutphin GL, Kaeberlein M: MeasuringCaenorhabditis eleganslife span on solid media.J Vis Exp 2009, 27:1152.
  • [64]Walker G, Houthoofd K, Vanfleteren JR, Gems D: Dietary restriction inC. elegans: from rate-of-living effects to nutrient sensing pathways.Mech Ageing Dev 2005, 126:929–937.
  • [65]Hicks KA, Howe DK, Leung A, Denver DR, Estes S: In vivo quantification reveals extensive natural variation in mitochondrial form and function in Caenorhabditis briggsae. PLoS One 2012, 7:e43837.
  • [66]Hicks KA, Denver DR, Estes S: Natural variation in Caenorhabditis briggsae mitochondrial form and function suggests a novel model of organelle dynamics. Mitochondrion 2013, 13:44-51.
  • [67]Zielonka J, Kalyanaraman B: Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth. Free Radic Biol Med 2010, 48:983-1001.
  • [68]Estes S, Phillips PC, Denver DR, Thomas WK, Lynch M: Mutation accumulation in populations of varying size: the distribution of mutational effects for fitness correlates inCaenorhabditis elegans.Genetics 2004, 166:1269–1279.
  • [69]Keightley PD, Davies EK, Peters AD, Shaw RG: Properties of ethylmethane sulfonate-induced mutations affecting life-history traits inCaenorhabditis elegansand inferences about bivariate distributions of mutation effects.Genetics 2000, 156:143–154.
  • [70]Pletcher SD, Neuhauser C: Biological aging—criteria for modeling and a new mechanistic model. Int J Mod Phys C 2000, 11:525-546.
  • [71]Bronikowski AM, Morgan TJ, Garland T, Carter PA: The evolution of aging and age-related physical decline in mice selectively bred for high voluntary exercise. Evolution (N Y) 2006, 60:1494-1508.
  • [72]Philips PC, Arnold SJ: Hierarchical comparison of genetic variance-covariance matrices, I: using the Flury hierarchy. Evolution (N Y) 1999, 53:1506-1515.
  • [73]Altun ZF, Hall DH: Introduction toC. elegansanatomy. In WormAtlas. 2009. doi:10.3908/wormatlas.1.1.
  • [74]Gems D, Riddle DL: Defining wild-type life span inCaenorhabditis elegans.J Gerontol A Biol Sci Med Sci 2000, 55:B215–B219.
  • [75]Tawe WN, Eschbach ML, Walter RD, Henkle-Duhrsen K: Identification of stress-responsive genes inCaenorhabditis elegansusing RT-PCR differential display.Nucleic Acids Res 1998, 26:1621–1627.
  • [76][http://www.wormbook.org] webcite Braeckman BP, Houthoofd K, Vanfleteren JR, The C. elegans Research Community: Intermediary Metabolism. In WormBook. ᅟWormBook 2009; ᅟ. doi:10.1895/wormbook.1.101.1, .
  • [77]Hartman P, Childress E, Beyer T: Nematode development is inhibited by methyl viologen and high oxygen concentrations at a rate inversely proportional to life span. J Gerontol A Biol Sci Med Sci 1995, 50:B322-B326.
  • [78]Jonassen T, Marbois BN, Faull KF, Clarke CF, Larsen PL: Development and fertility inCaenorhabditis elegansclk-1 mutants depend upon transport of dietary coenzyme Q8 to mitochondria.J Biol Chem 2002, 277:45020–45027.
  • [79]Goerlich O, Quillardet P, Hofnung M: Induction of the SOS response by hydrogen peroxide in variousEscherichia colimutants with altered protection against oxidative DNA damage.J Bacteriol 1989, 171:6141–6147.
  • [80]Blanchard JL, Wholey W-Y, Conlon EM, Pomposiello PJ: Rapid changes in gene expression dynamics in response to superoxide reveal SoxRS-dependent and independent transcriptional networks. PLoS One 2007, 2:e1186.
  • [81]Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B: Positive control of a global antioxidant defense regulon activated by superoxide-generating agents inEscherichia coli.Proc Natl Acad Sci U S A 1990, 87:6181–6185.
  • [82]Davison CL, Papirmeister B: Bacteriostasis ofEscherichia coliby the Herbicide Paraquat.Exp Biol Med 1971, 136:359–364.
  • [83]Hodgkin J, Barnes TM: More is not better: brood size and population growth in a self-fertilizing nematode. Proc Biol Sci 1991, 246:19-24.
  • [84]McElwee J, Bubb K, Thomas JH: Transcriptional outputs of theCaenorhabditis elegansforkhead protein DAF-16.Aging Cell 2003, 2:111–121.
  • [85]Henderson ST, Johnson TE: daf-16 integrates developmental and environmental inputs to mediate aging in the nematodeCaenorhabditis elegans.Curr Biol 2001, 11:1975–1980.
  • [86]Speakman JR, Selman C: The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bioessays 2011, 33:255-259.
  文献评价指标  
  下载次数:34次 浏览次数:20次