Multiple metazoan life-span interventions exhibit a sexspecific strehler-mildvan inverse relationship between initial mortality rate and age-dependent mortality rate acceleration

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 72, Issue 1, 2017, Pages 44-53

  Shen, Jie ^a   Landis, Gary N ^b   Tower, John ^b  

^a HANGZHOU DIANZI UNIVERSITY   (China)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Aging; Drosophila; Sexual antagonistic pleiotropy; Trade offs

Indexed keywords

MIFEPRISTONE; ORAL CONTRACEPTIVE AGENT;

AGE; ANIMAL; DROSOPHILA MELANOGASTER; FEMALE; LONGEVITY; MALE; REPRODUCTION; SEX DIFFERENCE; SURVIVAL RATE;

AGE FACTORS; ANIMALS; CONTRACEPTIVES, ORAL, SYNTHETIC; DROSOPHILA MELANOGASTER; FEMALE; LONGEVITY; MALE; MIFEPRISTONE; REPRODUCTION; SEX FACTORS; SURVIVAL RATE;

EID: 85014615899     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glw005     Document Type: Article

References (74)

1. Tower J. Mitochondrial maintenance failure in aging and role of sexual dimorphism. Arch Biochem Biophys. 2015;576:17-31. doi:10.1016/j. abb.2014.10.008
2. Morrow EH. The evolution of sex differences in disease. Biology of Sex Differences. 2015;6:5. doi:10.1186/s13293-015-0023-0
3. Burger JM, Promislow DE. Sex-specific effects of interventions that extend fly life span. Sci Aging Knowledge Environ. 2004;2004:pe30. doi:10.1126/sageke.2004.28.pe30
4. Tower J. Sex-specific regulation of aging and apoptosis. Mech Ageing Dev. 2006;127:705-718. doi:10.1016/j.mad.2006.05.001
5. Promislow D. Mate choice, sexual conflict, and evolution of senescence. Behav Genet. 2003;33:191-201. doi:10.1023/A:1022562103669
6. Pletcher SD. Model fitting and hypothesis testing for age-specific mortality data. J Evol Biol. 1999;12:430-439. doi:10.1046/j.1420-9101.1999.00058.x
7. Finch CE. Longevity, senescence and the genome. Chicago, IL: University of Chicago Press; 1990.
8. Ren C, Webster P, Finkel SE, Tower J. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab. 2007;6:144-152. doi:10.1016/j.cmet.2007.06.006
9. Wu JJ, Liu J, Chen EB, et al. Increased mammalian lifespan and a segmental and tissue-specific slowing of aging after genetic reduction of mTOR expression. Cell Rep. 2013;4:913-920. doi:10.1016/j.celrep.2013.07.030
10. Strehler BL, Mildvan AS. General theory of mortality and aging. Science. 1960;132:14-21. doi:10.1126/science.132.3418.14
11. Yashin AI, Begun AS, Boiko SI, Ukraintseva SV, Oeppen J. New age patterns of survival improvement in Sweden: do they characterize changes in individual aging? Mech Ageing Dev. 2002;123:637-647. doi:10.1016/S0047-6374(01)00410-9
12. Gavrilov LA, Gavrilova NS. The reliability theory of aging and longevity. J Theor Biol. 2001;213:527-545. doi:10.1006/jtbi.2001.2430
13. Hawkes K, Smith KR, Robson SL. Mortality and fertility rates in humans and chimpanzees: How within-species variation complicates cross-species comparisons. Am J Hum Biol. 2009;21:578-586. doi:10.1002/ajhb.20890
14. Zheng H, Yang Y, Land KC. Heterogeneity in the Strehler-Mildvan general theory of mortality and aging. Demography. 2011;48:267-290. doi:10.1007/s13524-011-0013-8
15. Beltran-Sancheza H, Crimmins E, Finch C. Early cohort mortality predicts the rate of aging in the cohort: a historical analysis. J Dev Orig Health Dis. 2012;3:380-386. doi:10.1017/S2040174412000281
16. Finch CE, Beltrán-Sánchez H, Crimmins EM. Uneven futures of human lifespans: reckonings from Gompertz mortality rates, climate change, and air pollution. Gerontology. 2014;60:183-188. doi:10.1159/000357672
17. Krementsova AV, Roshina NV, Tsybul'ko EA, Rybina OY, Symonenko AV, Pasyukova EG. Reproducible effects of the mitochondria-targeted plastoquinone derivative SkQ1 on Drosophila melanogaster lifespan under different experimental scenarios. Biogerontology. 2012;13:595-607. doi:10.1007/s10522-012-9404-5
18. Zhikrevetskaya S, Peregudova D, Danilov A, et al. Effect of low doses (5-40 cGy) of gamma-irradiation on lifespan and stress-related genes expression profile in Drosophila melanogaster. PLoS One. 2015;10:e0133840. doi:10.1371/journal.pone.0133840
19. Kirkwood TB, Shanley DP. Food restriction, evolution and ageing. Mech Ageing Dev. 2005;126:1011-1016. doi:10.1016/j.mad.2005.03.021
20. Masoro EJ. Caloric restriction-induced life extension of rats and mice: a critique of proposed mechanisms. Biochim Biophys Acta. 2009;1790:1040-1048. doi:10.1016/j.bbagen.2009.02.01
21. Yu BP, Masoro EJ, Murata I, Bertrand HA, Lynd FT. Life span study of SPF Fischer 344 male rats fed ad libitum or restricted diets: longevity, growth, lean body mass and disease. J Gerontol. 1982;37:130-141. doi:10.1093/geronj/37.2.130
22. Pletcher SD, Khazaeli AA, Curtsinger JW. Why do life spans differ? Partitioning mean longevity differences in terms of age-specific mortality parameters. J Gerontol A Biol Sci Med Sci. 2000;55:B381-B389. doi:10.1093/gerona/55.8.B381
23. Nakagawa S, Lagisz M, Hector KL, Spencer HG. Comparative and metaanalytic insights into life extension via dietary restriction. Aging Cell. 2012;11:401-409. doi:10.1111/j.1474-9726.2012.00798.x
24. Simons MJ, Koch W, Verhulst S. Dietary restriction of rodents decreases aging rate without affecting initial mortality rate-a meta-analysis. Aging Cell. 2013;12:410-414. doi:10.1111/acel.12061
25. Swindell WR. Dietary restriction in rats and mice: a meta-analysis and review of the evidence for genotype-dependent effects on lifespan. Ageing Res Rev. 2012;11:254-270. doi:10.1016/j.arr.2011.12.006
26. Liao CY, Johnson TE, Nelson JF. Genetic variation in responses to dietary restriction-an unbiased tool for hypothesis testing. Exp Gerontol. 2013;48:1025-1029. doi:10.1016/j.exger.2013.03.010
27. Magwere T, Chapman T, Partridge L. Sex differences in the effect of dietary restriction on life span and mortality rates in female and male Drosophila melanogaster. J Gerontol A Biol Sci Med Sci. 2004;59:3-9. doi:10.1093/gerona/59.1.B3
28. Mair W, Goymer P, Pletcher SD, Partridge L. Demography of dietary restriction and death in Drosophila. Science. 2003;301:1731-1733. doi:10.1126/science.1086016
29. Good TP, Tatar M. Age-specific mortality and reproduction respond to adult dietary restriction in Drosophila melanogaster. J Insect Physiol. 2001;47:1467-1473. doi:10.1016/S0022-1910(01)00138-X
30. Skorupa DA, Dervisefendic A, Zwiener J, Pletcher SD. Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell. 2008;7:478-490. doi:10.1111/j.1474-9726.2008.00400.x
31. Tatar M, Post S, Yu K. Nutrient control of Drosophila longevity. Trends Endocrinol Metab. 2014;25:509-517. doi:10.1016/j.tem.2014.02.006
32. Sun X, Komatsu T, Lim J, et al. Nutrient-dependent requirement for SOD1 in lifespan extension by protein restriction in Drosophila melanogaster. Aging Cell. 2012;11:783-793. doi:10.1111/j.1474-9726.2012.00842.x
33. Zajitschek F, Zajitschek SR, Friberg U, Maklakov AA. Interactive effects of sex, social environment, dietary restriction, and methionine on survival and reproduction in fruit flies. Age (Dordr). 2013;35:1193-1204. doi:10.1007/s11357-012-9445-3
34. Wolfner MF. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity (Edinb). 2002;88:85-93. doi:10.1038/sj.hdy.6800017
35. Landis GN, Salomon MP, Keroles D, Brookes N, Sekimura T, Tower J. The progesterone antagonist mifepristone/RU486 blocks the negative effect on life span caused by mating in female Drosophila. Aging (Albany NY). 2015;7:53-69.
36. Baulieu EE. RU 486 (mifepristone). A short overview of its mechanisms of action and clinical uses at the end of 1996. Ann N Y Acad Sci. 1997;828:47-58. doi:10.1111/j.1749-6632.1997.tb48523.x
37. Sieber MH, Spradling AC. Steroid signaling establishes a female metabolic state and regulates SREBP to control oocyte lipid accumulation. Curr Biol. 2015;25:993-1004. doi:10.1016/j.cub.2015.02.019
38. Fagegaltier D, König A, Gordon A, et al. A genome-wide survey of sexually dimorphic expression of Drosophila miRNAs identifies the steroid hormone-induced miRNA let-7 as a regulator of sexual identity. Genetics. 2014;198:647-668. doi:10.1534/genetics.114.169268
39. Waskar M, Landis GN, Shen J, et al. Drosophila melanogaster p53 has developmental stage-specific and sex-specific effects on adult life span indicative of sexual antagonistic pleiotropy. Aging (Albany NY). 2009;1:903-936.
40. Shen J, Ford D, Landis GN, Tower J. Identifying sexual differentiation genes that affect Drosophila life span. BMC Geriatr. 2009;9:56. doi:10.1186/1471-2318-9-56
41. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2009.
42. Kirkwood TB. Understanding the odd science of aging. Cell. 2005;120:437-447. doi:10.1016/j.cell.2005.01.027
43. Flatt T. Survival costs of reproduction in Drosophila. Exp Gerontol. 2011;46:369-375. doi:10.1016/j.exger.2010.10.008
44. Tatar M. The plate half-full: status of research on the mechanisms of dietary restriction in Drosophila melanogaster. Exp Gerontol. 2011;46:363-368. doi:10.1016/j.exger.2010.12.002
45. Mair W, Sgro CM, Johnson AP, Chapman T, Partridge L. Lifespan extension by dietary restriction in female Drosophila melanogaster is not caused by a reduction in vitellogenesis or ovarian activity. Exp Gerontol. 2004;39:1011-1019. doi:10.1016/j.exger.2004.03.018
46. Ueyama M, Fuyama Y. Enhanced cost of mating in female sterile mutants of Drosophila melanogaster. Genes Genet Syst. 2003;78:29-36. doi:10.1266/ggs.78.29
47. Feng Z, Lin M, Wu R. The regulation of aging and longevity: a new and complex role of p53. Genes Cancer. 2011;2:443-452. doi:10.1177/1947601911410223
48. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol. 2004;14:885-890. doi:10.1016/j.cub.2004.03.059
49. Zhou S, Mackay T, Anholt RR. Transcriptional and epigenetic responses to mating and aging in Drosophila melanogaster. BMC Genomics. 2014;15:927. doi:10.1186/1471-2164-15-927
50. Short SM, Wolfner MF, Lazzaro BP. Female Drosophila melanogaster suffer reduced defense against infection due to seminal fluid components. J Insect Physiol. 2012;58:1192-1201. doi:10.1016/j.jinsphys.2012.06.002
51. Fedorka KM, Linder JE, Winterhalter W, Promislow D. Post-mating disparity between potential and realized immune response in Drosophila melanogaster. Proc Biol Sci. 2007;274:1211-1217. doi:10.1098/rspb.2006.0394
52. Shen J, Tower J. Drosophila foxo acts in males to cause sexual-dimorphism in tissue-specific p53 life span effects. Exp Gerontol. 2010;45:97-105. doi:10.1016/j.exger.2009.10.009
53. Carey JR, Liedo P, Orozco D, Vaupel JW. Slowing of mortality rates at older ages in large medfly cohorts. Science. 1992;258:457-461. doi:10.1126/science. 1411540
54. Curtsinger JW, Fukui HH, Townsend DR, Vaupel JW. Demography of genotypes: failure of the limited life-span paradigm in Drosophila melanogaster. Science. 1992;258:461-463. doi:10.1126/science.1411541
55. Tatar M, Carey JR, Vaupel JW. Long-term cost of reproduction with and without accelerated senescence in Callosobruchus maculatus: analysis of agespecific mortality. Evolution. 1993;47:1302-1312. doi:10.2307/2410149
56. Vaupel JW, Johnson TE, Lithgow GJ. Rates of mortality in populations of Caenorhabditis elegans. Science. 1994;266:826. doi:10.1126/science. 7973640
57. Vaupel JW, Carey JR, Christensen K, et al. Biodemographic trajectories of longevity. Science. 1998;280:855-860. doi:10.1126/science.280.5365.855
58. Koopman JJ, Rozing MP, Kramer A, et al. Calculating the Rate of Senescence From Mortality Data: An Analysis of Data From the ERA-EDTA Registry. J Gerontol A Biol Sci Med Sci. 2015. doi: 10.1093/gerona/glv042
59. Gavrilov LA, Gavrilova NS. Mortality Measurement at Advanced Ages: A Study of the Social Security Administration Death Master File. North American actuarial journal: NAAJ. 2011;15:432-447.
60. Missov TI, Vaupel JW. Mortality Implications of Mortality Plateaus. SIAM Review. 2015;57:61-70. doi:10.1137/130912992
61. Kirkwood TB. Deciphering death: a commentary on Gompertz (1825) 'On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life contingencies'. Philos Trans R Soc Lond B Biol Sci. 2015;370. doi:10.1098/rstb.2014.0379
62. Clark RI, Salazar A, Yamada R, et al. Distinct Shifts in Microbiota Composition during Drosophila Aging Impair Intestinal Function and Drive Mortality. Cell Rep. 2015;12:1656-1667. doi:10.1016/j.celrep. 2015.08.004
63. Chen HY, Zajitschek F, Maklakov AA. Why ageing stops: heterogeneity explains late-life mortality deceleration in nematodes. Biol Lett. 2013;9:20130217. doi:10.1098/rsbl.2013.0217
64. Wu D, Rea SL, Yashin AI, Johnson TE. Visualizing hidden heterogeneity in isogenic populations of C. elegans. Exp Gerontol. 2006;41:261-270. doi:10.1016/j.exger.2006.01.003
65. Yang J, Tower J. Expression of hsp22 and hsp70 transgenes is partially predictive of drosophila survival under normal and stress conditions. J Gerontol A Biol Sci Med Sci. 2009;64:828-838. doi:10.1093/gerona/glp054
66. Landis GN, Abdueva D, Skvortsov D, et al. Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci USA. 2004;101:7663-7668. doi:10.1073/pnas.0307605101
67. Khazaeli AA, Pletcher SD, Curtsinger JW. The fractionation experiment: reducing heterogeneity to investigate age-specific mortality in Drosophila. Mech Ageing Dev. 1998;105:301-317. doi:10.1073/pnas.0307605101
68. Gurven M, Kaplan H, Supa AZ. Mortality experience of Tsimane Amerindians of Bolivia: regional variation and temporal trends. Am J Hum Biol. 2007;19:376-398. doi:10.1002/ajhb.20600
69. Vasunilashorn S, Crimmins EM, Kim JK, et al. Blood lipids, infection, and inflammatory markers in the Tsimane of Bolivia. Am J Hum Biol. 2010;22:731-740. doi:10.1002/ajhb.21074
70. Gurven M, Kaplan H, Winking J, et al. Inflammation and infection do not promote arterial aging and cardiovascular disease risk factors among lean horticulturalists. PLoS One. 2009;4:e6590. doi:10.1371/journal.pone.0006590
71. Chang SF, Lin PL. Frail phenotype and mortality prediction: a systematic review and meta-analysis of prospective cohort studies. Int J Nurs Stud. 2015;52:1362-1374. doi:10.1016/j.ijnurstu.2015.04.005
72. Chen X, Mao G, Leng SX. Frailty syndrome: an overview. Clin Interv Aging. 2014;9:433-441. doi:10.2147/CIA.S45300
73. Christiansen L, Lenart A, Tan Q, et al. DNA methylation age is associated with mortality in a longitudinal Danish twin study. Aging Cell. 2015. doi: 10.1111/acel.12421
74. Moore AZ, Hernandez DG, Tanaka T, et al. Change in epigenome-wide DNA methylation over 9 years and subsequent mortality: results from the InCHIANTI Study. J Gerontol A Biol Sci Med Sci. 2015. doi: 10.1093/gerona/glv118