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How Justified is the Assumption of Programmed Aging in Reminiscence of Weismann’s Theories?

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Abstract

Theories about the benefits of death and the resulting increased likelihood of programmed aging are controversial, advocated only by a minority. The extent to which their assumptions might be justified should be investigated. To this end, various approaches to the possible utility or origin were considered, particularly potential benefits of the faster generational change caused by possible evolutionary compound interest. Reference was made to the thinking of Weismann, the father of regulated aging theories, who advocated non-adaptive concepts at the end of his career. In a thought experiment, circadian rhythms are discussed as a possible molecular source of aging regulation.

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Additional information

Programs. MinuteLabs.io & PRIMER on https://labs.minutelabs.io/evolution-simulator. Available programming code at https://github.com/minutelabsio/evolution-simulator. Thanks to the authors for providing the MASON aging model and for its user-friendliness 2.

References

  1. Cohen, A. A., Kennedy, B. K., Anglas, U., Bronikowski, A. M., Deelen, J., et al. (2020) Lack of consensus on an aging biology paradigm? A global survey reveals an agreement to disagree, and the need for an interdisciplinary framework, Mech. Ageing Dev., 191, 111316, https://doi.org/10.1016/j.mad.2020.111316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kowald, A., and Kirkwood, T. B. L. (2016) Can aging be programmed? A critical literature review, Aging Cell, 15, 986-998, https://doi.org/10.1111/acel.12510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. De Grey, A. D. (2007) Calorie restriction, post-reproductive life span, and programmed aging: A plea for rigor, Ann. N. Y. Acad. Sci., 1119, 296-305, https://doi.org/10.1196/annals.1404.029.

    Article  PubMed  Google Scholar 

  4. Hughes, P. W. (2017) Between semelparity and iteroparity: Empirical evidence for a continuum of modes of parity, Ecol. Evol., 7, 8232-8261, https://doi.org/10.1002/ece3.3341.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Oakwood, M., Bradley, A. J., and Cockburn, A. (2001) Semelparity in a large marsupial, Proc. Biol. Sci., 268, 407-411, https://doi.org/10.1098/rspb.2000.1369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kraaijeveld, K., Kraaijeveld-Smit, F. J., and Adcock, G. J. (2003) Does female mortality drive male semelparity in dasyurid marsupials?, Proc. Biol. Sci., 270 Suppl 2, S251-253, https://doi.org/10.1098/rsbl.2003.0082.

    Article  PubMed  Google Scholar 

  7. Leopold, A. C. (1961) Senescence in plant development: The death of plants or plant parts may be of positive ecological or physiological value, Science, 134, 1727-1732, https://doi.org/10.1126/science.134.3492.1727.

    Article  CAS  PubMed  Google Scholar 

  8. Dawkins, R. (2003) The Evolution of Evolvability, in On Growth, Form and Computers (Kumar, S., and Bentley, P. J., eds) Academic Press, pp. 239-255, https://doi.org/10.1016/B978-012428765-5/50046-3.

  9. Kirschner, M., and Gerhart, J. (1998) Evolvability, Proc. Natl. Acad. Sci. USA, 95, 8420-8427, https://doi.org/10.1073/pnas.95.15.8420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Wagner, G. P., and Altenberg, L. (1996) Perspective: Complex adaptations and the evolution of evolvability, Evolution, 50, 967-976, https://doi.org/10.1111/j.1558-5646.1996.tb02339.x.

    Article  PubMed  Google Scholar 

  11. Brakefield, P. M. (2006) Evo–devo and constraints on selection, Trends Ecol. Evol., 21, 362-368, https://doi.org/10.1016/j.tree.2006.05.001.

    Article  PubMed  Google Scholar 

  12. Landry, C. R., Lemos, B., Rifkin, S. A., Dickinson, W. J., and Hartl, D. L. (2007) Genetic properties influencing the evolvability of gene expression, Science, 317, 118-121, https://doi.org/10.1126/science.1140247.

    Article  CAS  PubMed  Google Scholar 

  13. Goldsmith, T. C. (2004) Aging as an evolved characteristic – Weismann’s theory reconsidered, Med. Hypotheses, 62, 304-308, https://doi.org/10.1016/S0306-9877(03)00337-2.

    Article  PubMed  Google Scholar 

  14. Goldsmith, T. C. (2008) Aging, evolvability, and the individual benefit requirement; medical implications of aging theory controversies, J. Theor. Biol., 252, 764-768, https://doi.org/10.1016/j.jtbi.2008.02.035.

    Article  PubMed  Google Scholar 

  15. Libertini, G. (1988) An adaptive theory of increasing mortality with increasing chronological age in populations in the wild, J. Theor. Biol., 132, 145-162, https://doi.org/10.1016/s0022-5193(88)80153-x.

    Article  CAS  PubMed  Google Scholar 

  16. Skulachev, V. P. (1997) Aging is a specific biological function rather than the result of a disorder in complex living systems: biochemical evidence in support of Weismann’s hypothesis, Biochemistry (Moscow), 62, 1191-1195.

    CAS  Google Scholar 

  17. Skulachev, V. P. (1999) Phenoptosis: programmed death of an organism, Biochemistry (Moscow), 64, 1418-1426.

    CAS  Google Scholar 

  18. Skulachev, M. V., and Skulachev, V. P. (2014) New data on programmed aging – slow phenoptosis, Biochemistry (Moscow), 79, 977-993, https://doi.org/10.1134/S0006297914100010.

    Article  CAS  Google Scholar 

  19. Vyssokikh, M. Y., Holtze, S., Averina, O. A., Lyamzaev, K. G., Panteleeva, A. A., et al. (2020) Mild depolarization of the inner mitochondrial membrane is a crucial component of an anti-aging program, Proc. Natl. Acad. Sci. USA, 117, 6491-6501, https://doi.org/10.1073/pnas.1916414117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Blackburn, E. H. (2000) Telomere states and cell fates, Nature, 408, 53-56, https://doi.org/10.1038/35040500.

    Article  CAS  PubMed  Google Scholar 

  21. Libertini, G. (2015) Phylogeny of aging and related phenoptotic phenomena, Biochemistry (Moscow), 80, 1529-1546, https://doi.org/10.1134/S0006297915120019.

    Article  CAS  Google Scholar 

  22. Libertini, G., Corbi, G., and Nicola, F. (2020) Importance and meaning of TERRA sequences for aging mechanisms, Biochemistry (Moscow), 85, 1505-1517, https://doi.org/10.1134/S0006297920120044.

    Article  CAS  Google Scholar 

  23. Weismann, A. (1882) Ueber die Dauer des Lebens; ein Vortrag, G. Fischer, Jena.

  24. Weismann, A. (1891) Amphimixis; oder: die Vermischung der Individuen, G. Fischer, Jena.

  25. Weismann, A. (1886) Die Bedeutung der sexuellen Fortpflanzung für die Selektions-Theorie, G. Fischer, Jena.

  26. Smith, J. M. (1976) Group selection, Quarterly Rev. Biol., 51, 277-283.

    Article  Google Scholar 

  27. Wilson, D. S. (1975) A theory of group selection, Proc. Natl. Acad. Sci. USA, 72, 143-146, https://doi.org/10.1073/pnas.72.1.143.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hamilton, W. D. (1964) The genetical evolution of social behaviour. I, J. Theor. Biol., 7, 1-16, https://doi.org/10.1016/0022-5193(64)90038-4.

    Article  CAS  PubMed  Google Scholar 

  29. Nowak, M. A., Tarnita, C. E., and Wilson, E. O. (2010) The evolution of eusociality, Nature, 466, 1057-1062, https://doi.org/10.1038/nature09205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Briolat, E. S., Burdfield-Steel, E. R., Paul, S. C., Ronka, K. H., Seymoure, B. M., et al. (2019) Diversity in warning coloration: Selective paradox or the norm?, Biol. Rev. Camb. Philos. Soc., 94, 388-414, https://doi.org/10.1111/brv.12460.

    Article  PubMed  Google Scholar 

  31. Kadri, S., Metcalfe, N., Huntingford, F., and Thorpe, J. E. (1995) What controls the onset of anorexia in maturing adult female atlantic salmon, Funct. Ecol., 9, 790-797.

    Article  Google Scholar 

  32. Naeger, N. L., Peso, M., Even, N., Barron, A. B., and Robinson, G. E. (2013) Altruistic behavior by egg-laying worker honeybees, Curr. Biol., 23, 1574-1578, https://doi.org/10.1016/j.cub.2013.06.045.

    Article  CAS  PubMed  Google Scholar 

  33. Carter, G. G., Farine, D. R., Crisp, R. J., Vrtilek, J. K., Ripperger, S. P., et al. (2020) Development of new food-sharing relationships in vampire bats, Curr. Biol., 30, 1275-1279.e1273, https://doi.org/10.1016/j.cub.2020.01.055.

    Article  CAS  PubMed  Google Scholar 

  34. Roberts, J. D., Bebenek, K., and Kunkel, T. A. (1988) The accuracy of reverse transcriptase from HIV-1, Science, 242, 1171-1173, https://doi.org/10.1126/science.2460925.

    Article  CAS  PubMed  Google Scholar 

  35. Weismann, A. (1887) Ueber die Zahl der Richtungskörper und über ihre Bedeutung für die Vererbung, G. Fischer, Jena.

  36. Bi, K., and Bogart, J. P. (2010) Time and time again: unisexual salamanders (genus Ambystoma) are the oldest unisexual vertebrates, BMC Evol. Biol., 10, 238, https://doi.org/10.1186/1471-2148-10-238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Smith, J. M. (1971) What use is sex?, J. Theor. Biol., 30, 319-335, https://doi.org/10.1016/0022-5193(71)90058-0.

    Article  CAS  PubMed  Google Scholar 

  38. Trivers, R. (1983) The evolution of sex: The masterpiece of nature: the evolution and genetics of sexuality. Graham Bell, Quarterly Rev. Biol., 58, 62-67, https://doi.org/10.1086/413059.

    Article  Google Scholar 

  39. Hamilton, W. D. (1980) Sex versus non-sex versus parasite, Oikos, 35, 282-290, https://doi.org/10.2307/3544435.

    Article  Google Scholar 

  40. Jaenike, J. (1977) A hypothesis to account for the maintenance of sex in populations, Evol. Theory, 3, 191-194.

    Google Scholar 

  41. Hartung, J. (1981) Genome Parliaments and Sex with the Red Queen, in Natural Selection and Social Behavior (Alexander, R. D., and Tinkle, D., eds.) Chiron, N.Y., pp. 382-404.

  42. Lively, C., Craddock, C., and Vrijenhoek, R. (1990) Red Queen hypothesis supported by parasitism in sexual and clonal fish, Nature, 344, 864-866, https://doi.org/10.1038/344864a0.

    Article  Google Scholar 

  43. Quattro, J. M., Avise, J. C., and Vrijenhoek, R. C. (1992) An ancient clonal lineage in the fish genus Poeciliopsis (Atheriniformes: Poeciliidae), Proc. Natl. Acad. Sci. USA, 89, 348-352, https://doi.org/10.1073/pnas.89.1.348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Libertini, G. (2017) Sex and Aging: A Comparison between Two Phenoptotic Phenomena, Biochemistry (Moscow), 82, 1435-1455, https://doi.org/10.1134/S0006297917120045.

    Article  CAS  Google Scholar 

  45. Dobrowolski, P., Fischer, M., and Naumann, R. (2018) Novel insights into the genetic background of genetically modified mice, Transgenic Res., 27, 265-275, https://doi.org/10.1007/s11248-018-0073-2.

    Article  CAS  PubMed  Google Scholar 

  46. Lenart, P., and Bienertova-Vasku, J. (2017) Keeping up with the Red Queen: the pace of aging as an adaptation, Biogerontology, 18, 693-709, https://doi.org/10.1007/s10522-016-9674-4.

    Article  PubMed  Google Scholar 

  47. Mitteldorf, J., and Pepper, J. (2009) Senescence as an adaptation to limit the spread of disease, J. Theor. Biol., 260, 186-195, https://doi.org/10.1016/j.jtbi.2009.05.013.

    Article  PubMed  Google Scholar 

  48. May, R. M., and Anderson, R. M. (1983) Epidemiology and genetics in the coevolution of parasites and hosts, Proc. R. Soc. Lond. B Biol. Sci., 219, 281-313, https://doi.org/10.1098/rspb.1983.0075.

    Article  CAS  PubMed  Google Scholar 

  49. Howard, R. S., and Lively, C. M. (1994) Parasitism, mutation accumulation and the maintenance of sex, Nature, 367, 554-557, https://doi.org/10.1038/367554a0.

    Article  CAS  PubMed  Google Scholar 

  50. Otto, S. P., and Nuismer, S. L. (2004) Species interactions and the evolution of sex, Science, 304, 1018-1020, https://doi.org/10.1126/science.1094072.

    Article  CAS  PubMed  Google Scholar 

  51. Lively, C. M. (2010) Parasite virulence, host life history, and the costs and benefits of sex, Ecology, 91, 3-6, https://doi.org/10.1890/09-1158.1.

    Article  PubMed  Google Scholar 

  52. Martins, A. C. (2011) Change and aging senescence as an adaptation, PLoS One, 6, e24328, https://doi.org/10.1371/journal.pone.0024328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Mitteldorf, J., and Martins, A. C. (2014) Programmed life span in the context of evolvability, Am. Nat., 184, 289-302, https://doi.org/10.1086/677387.

    Article  PubMed  Google Scholar 

  54. Keightley, P. D., Ness, R. W., Halligan, D. L., and Haddrill, P. R. (2014) Estimation of the spontaneous mutation rate per nucleotide site in a Drosophila melanogaster full-sib family, Genetics, 196, 313-320, https://doi.org/10.1534/genetics.113.158758.

    Article  CAS  PubMed  Google Scholar 

  55. Blount, Z. D., Barrick, J. E., Davidson, C. J., and Lenski, R. E. (2012) Genomic analysis of a key innovation in an experimental Escherichia coli population, Nature, 489, 513-518, https://doi.org/10.1038/nature11514.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Cohain, J. S., Buxbaum, R. E., and Mankuta, D. (2017) Spontaneous first trimester miscarriage rates per woman among parous women with 1 or more pregnancies of 24 weeks or more, BMC Pregnancy Childbirth, 17, 437, https://doi.org/10.1186/s12884-017-1620-1.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Keightley, P. D., and Otto, S. P. (2006) Interference among deleterious mutations favours sex and recombination in finite populations, Nature, 443, 89-92, https://doi.org/10.1038/nature05049.

    Article  CAS  PubMed  Google Scholar 

  58. Grieshop, K., Maurizio, P. L., Arnqvist, G., and Berger, D. (2021) Selection in males purges the mutation load on female fitness, Evol. Lett., 5, 328-343, https://doi.org/10.1002/evl3.239.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Felsenstein, J. (1974) The evolutionary advantage of recombination, Genetics, 78, 737-756, https://doi.org/10.1093/genetics/78.2.737.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Luke, S., Cioffi-Revilla, C., Panait, L., Sullivan, K., and Balan, G. (2005) MASON: A multiagent simulation environment, Simulation, 81, 517-527, https://doi.org/10.1177/0037549705058073.

    Article  Google Scholar 

  61. Medawar, P. B. (1952) An Unsolved Problem of Biology: An Inaugural Lecture Delivered at University College, London, 6 December, 1951, H. K. Lewis and Company, London.

  62. Williams, G. C. (1957) Pleiotropy, Natural Selection, and the Evolution of Senescence, Evolution, 11, 398-411, https://doi.org/10.2307/2406060.

    Article  Google Scholar 

  63. Weismann, A. (1892) Aufsätze über Vererbung und Verwandte Biologische Fragen, G. Fischer, Jena.

  64. Weismann, A. (1884) Ueber Leben und Tod: Eine Biologische Untersuchung, G. Fischer, Jena.

  65. Weismann, A. (1904) Vorträge über Deszendenztheorie; Band 2, G. Fischer, Jena.

  66. Sergiev, P. V., Dontsova, O. A., and Berezkin, G. V. (2015) Theories of aging: an ever-evolving field, Acta Naturae, 7, 9-18.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Kirkwood, T. B., and Cremer, T. (1982) Cytogerontology since 1881: a reappraisal of August Weismann and a review of modern progress, Hum. Genet., 60, 101-121, https://doi.org/10.1007/BF00569695.

    Article  CAS  PubMed  Google Scholar 

  68. Libertini, G. (2015) Non-programmed versus programmed aging paradigm, Curr. Aging Sci., 8, 56-68.

    Article  PubMed  Google Scholar 

  69. Goldsmith, T. C. (2012) On the programmed/non-programmed aging controversy, Biochemistry (Moscow), 77, 729-732, https://doi.org/10.1134/S000629791207005X.

    Article  CAS  Google Scholar 

  70. Olovnikov, A. M. (2003) The redusome hypothesis of aging and the control of biological time during individual development, Biochemistry (Moscow), 68, 2-33, https://doi.org/10.1023/a:1022185100035.

    Article  CAS  Google Scholar 

  71. Schaible, R., Sussman, M., and Kramer, B. H. (2014) Aging and potential for self-renewal: hydra living in the age of aging – a mini-review, Gerontology, 60, 548-556, https://doi.org/10.1159/000360397.

    Article  PubMed  Google Scholar 

  72. Chmielewski, P. (2017) Rethinking modern theories of ageing and their classification: the proximate mechanisms and the ultimate explanations, Anthropol. Rev., 80, 259-272, https://doi.org/10.1515/anre-2017-0021.

    Article  Google Scholar 

  73. Voituron, Y., de Fraipont, M., Issartel, J., Guillaume, O., and Clobert, J. (2011) Extreme lifespan of the human fish (Proteus anguinus): A challenge for ageing mechanisms, Biol. Lett., 7, 105-107, https://doi.org/10.1098/rsbl.2010.0539.

    Article  PubMed  Google Scholar 

  74. Andrews, A. H., Tracey, D. M., and Dunn, M. R. (2009) Lead-radium dating of orange roughy (Hoplostethus atlanticus): validation of a centenarian life span, Can. J. Fish. Aquat. Sci., 66, 1130-1140, https://doi.org/10.1139/f09-059.

    Article  CAS  Google Scholar 

  75. Nielsen, J., Hedeholm, R. B., Heinemeier, J., Bushnell, P. G., Christiansen, J. S., et al. (2016) Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus), Science, 353, 702-704, https://doi.org/10.1126/science.aaf1703.

    Article  CAS  PubMed  Google Scholar 

  76. Goldsmith, T. C. (2016) Emerging programmed aging mechanisms and their medical implications, Med. Hypotheses, 86, 92-96, https://doi.org/10.1016/j.mehy.2015.10.015.

    Article  PubMed  Google Scholar 

  77. Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V., and Antoch, M. P. (2006) Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock, Genes Dev., 20, 1868-1873, https://doi.org/10.1101/gad.1432206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Khapre, R. V., Kondratova, A. A., Susova, O., and Kondratov, R. V. (2011) Circadian clock protein BMAL1 regulates cellular senescence in vivo, Cell Cycle, 10, 4162-4169, https://doi.org/10.4161/cc.10.23.18381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Nakahata, Y., Sahar, S., Astarita, G., Kaluzova, M., and Sassone-Corsi, P. (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1, Science, 324, 654-657, https://doi.org/10.1126/science.1170803.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Bonaconsa, M., Malpeli, G., Montaruli, A., Carandente, F., Grassi-Zucconi, G., et al. (2014) Differential modulation of clock gene expression in the suprachiasmatic nucleus, liver and heart of aged mice, Exp. Gerontol., 55, 70-79, https://doi.org/10.1016/j.exger.2014.03.011.

    Article  CAS  PubMed  Google Scholar 

  81. Hood, S., and Amir, S. (2017) The aging clock: Circadian rhythms and later life, J. Clin. Invest., 127, 437-446, https://doi.org/10.1172/JCI90328.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Vallee, A., Lecarpentier, Y., and Vallee, J. N. (2019) Curcumin: a therapeutic strategy in cancers by inhibiting the canonical WNT/beta-catenin pathway, J. Exp. Clin. Cancer Res., 38, 323, https://doi.org/10.1186/s13046-019-1320-y.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Shilovsky, G. A., Putyatina, T. S., Morgunova, G. V., Seliverstov, A. V., Ashapkin, V. V., et al. (2021) A Crosstalk between the biorhythms and gatekeepers of longevity: Dual role of glycogen synthase kinase-3, Biochemistry (Moscow), 86, 433-448, https://doi.org/10.1134/S0006297921040052.

    Article  CAS  Google Scholar 

  84. Lewis, K. N., Wason, E., Edrey, Y. H., Kristan, D. M., Nevo, E., et al. (2015) Regulation of Nrf2 signaling and longevity in naturally long-lived rodents, Proc. Natl. Acad. Sci. USA, 112, 3722-3727, https://doi.org/10.1073/pnas.1417566112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Early, J. O., Menon, D., Wyse, C. A., Cervantes-Silva, M. P., Zaslona, Z., et al. (2018) Circadian clock protein BMAL1 regulates IL-1beta in macrophages via NRF2, Proc. Natl. Acad. Sci. USA, 115, E8460-E8468, https://doi.org/10.1073/pnas.1800431115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wible, R. S., Ramanathan, C., Sutter, C. H., Olesen, K. M., Kensler, T. W., et al. (2018) NRF2 regulates core and stabilizing circadian clock loops, coupling redox and timekeeping in Mus musculus, Elife, 7, e31656, https://doi.org/10.7554/eLife.31656.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Dubrovsky, Y. V., Samsa, W. E., and Kondratov, R. V. (2010) Deficiency of circadian protein CLOCK reduces lifespan and increases age-related cataract development in mice, Aging (Albany NY), 2, 936-944, https://doi.org/10.18632/aging.100241.

    Article  CAS  Google Scholar 

  88. Ulgherait, M., Chen, A., McAllister, S. F., Kim, H. X., Delventhal, R., et al. (2020) Circadian regulation of mitochondrial uncoupling and lifespan, Nat. Commun., 11, 1927, https://doi.org/10.1038/s41467-020-15617-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Kucerova, L., Kubrak, O. I., Bengtsson, J. M., Strnad, H., Nylin, S., et al. (2016) Slowed aging during reproductive dormancy is reflected in genome-wide transcriptome changes in Drosophila melanogaster, BMC Genomics, 17, 50, https://doi.org/10.1186/s12864-016-2383-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. McCay, C. M., Crowell, M. F., and Maynard, L. A. (1935) The effect of retarded growth upon the length of life span and upon the ultimate body size. 1935, Nutrition, 5, 63-79, https://doi.org/10.1093/jn/10.1.63.

    Article  Google Scholar 

  91. Bauer, J., Antosh, M., Chang, C., Schorl, C., Kolli, S., et al. (2010) Comparative transcriptional profiling identifies takeout as a gene that regulates life span, Aging (Albany NY), 2, 298-310, https://doi.org/10.18632/aging.100146.

    Article  CAS  Google Scholar 

  92. Patel, S. A., Velingkaar, N., Makwana, K., Chaudhari, A., and Kondratov, R. (2016) Calorie restriction regulates circadian clock gene expression through BMAL1 dependent and independent mechanisms, Sci. Rep., 6, 25970, https://doi.org/10.1038/srep25970.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Sato, S., Solanas, G., Peixoto, F. O., Bee, L., Symeonidi, A., et al. (2017) Circadian reprogramming in the liver identifies metabolic pathways of aging, Cell, 170, 664-677.e11, https://doi.org/10.1016/j.cell.2017.07.042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Schumacher, A. (2009) An Epigenetic Clock: Anticorrelation & DNA Methylation as Biomarker for Aging, https://doi.org/10.13140/RG.2.2.12457.83042.

  95. Bocklandt, S., Lin, W., Sehl, M. E., Sanchez, F. J., Sinsheimer, J. S., et al. (2011) Epigenetic predictor of age, PLoS One, 6, e14821, https://doi.org/10.1371/journal.pone.0014821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Oh, G., Ebrahimi, S., Carlucci, M., Zhang, A., Nair, A., et al. (2018) Cytosine modifications exhibit circadian oscillations that are involved in epigenetic diversity and aging, Nat. Commun., 9, 644, https://doi.org/10.1038/s41467-018-03073-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Yi, S. J., and Kim, K. (2020) New Insights into the role of histone changes in aging, Int. J. Mol. Sci., 21, 8241, https://doi.org/10.3390/ijms21218241.

    Article  CAS  PubMed Central  Google Scholar 

  98. Zarse, K., Terao, T., Tian, J., Iwata, N., Ishii, N., et al. (2011) Low-dose lithium uptake promotes longevity in humans and metazoans, Eur. J. Nutr., 50, 387-389, https://doi.org/10.1007/s00394-011-0171-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Castillo-Quan, J. I., Li, L., Kinghorn, K. J., Ivanov, D. K., Tain, L. S., et al. (2016) Lithium promotes longevity through GSK3/NRF2-dependent hormesis, Cell Rep., 15, 638-650, https://doi.org/10.1016/j.celrep.2016.03.041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Besing, R. C., Paul, J. R., Hablitz, L. M., Rogers, C. O., Johnson, R. L., et al. (2015) Circadian rhythmicity of active GSK3 isoforms modulates molecular clock gene rhythms in the suprachiasmatic nucleus, J. Biol. Rhythms, 30, 155-160, https://doi.org/10.1177/0748730415573167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Yin, L., Wang, J., Klein, P. S., and Lazar, M. A. (2006) Nuclear receptor Rev-erbalpha is a critical lithium-sensitive component of the circadian clock, Science, 311, 1002-1005, https://doi.org/10.1126/science.1121613.

    Article  CAS  PubMed  Google Scholar 

  102. Noguchi, T., Lo, K., Diemer, T., and Welsh, D. K. (2016) Lithium effects on circadian rhythms in fibroblasts and suprachiasmatic nucleus slices from Cry knockout mice, Neurosci. Lett., 619, 49-53, https://doi.org/10.1016/j.neulet.2016.02.030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Evason, K., Collins, J. J., Huang, C., Hughes, S., and Kornfeld, K. (2008) Valproic acid extends Caenorhabditis elegans lifespan, Aging Cell, 7, 305-317, https://doi.org/10.1111/j.1474-9726.2008.00375.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Johansson, A. S., Brask, J., Owe-Larsson, B., Hetta, J., and Lundkvist, G. B. (2011) Valproic acid phase shifts the rhythmic expression of Period2::Luciferase, J. Biol. Rhythms, 26, 541-551, https://doi.org/10.1177/0748730411419775.

    Article  CAS  PubMed  Google Scholar 

  105. Griggs, C. A., Malm, S. W., Jaime-Frias, R., and Smith, C. L. (2018) Valproic acid disrupts the oscillatory expression of core circadian rhythm transcription factors, Toxicol. Appl. Pharmacol., 339, 110-120, https://doi.org/10.1016/j.taap.2017.12.005.

    Article  CAS  PubMed  Google Scholar 

  106. Tang, Y., and Cheng, L. (2017) Cocktail of chemical compounds robustly promoting cell reprogramming protects liver against acute injury, Protein Cell, 8, 273-283, https://doi.org/10.1007/s13238-017-0373-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Zmijewski, J. W., and Jope, R. S. (2004) Nuclear accumulation of glycogen synthase kinase-3 during replicative senescence of human fibroblasts, Aging Cell, 3, 309-317, https://doi.org/10.1111/j.1474-9728.2004.00117.x.

    Article  CAS  PubMed  Google Scholar 

  108. Zhai, Y., Chen, X., Yu, D., Li, T., Cui, J., et al. (2015) Histone deacetylase inhibitor valproic acid promotes the induction of pluripotency in mouse fibroblasts by suppressing reprogramming-induced senescence stress, Exp. Cell Res., 337, 61-67, https://doi.org/10.1016/j.yexcr.2015.06.003.

    Article  CAS  PubMed  Google Scholar 

  109. Leng, Y., Liang, M. H., Ren, M., Marinova, Z., Leeds, P., et al. (2008) Synergistic neuroprotective effects of lithium and valproic acid or other histone deacetylase inhibitors in neurons: roles of glycogen synthase kinase-3 inhibition, J. Neurosci., 28, 2576-2588, https://doi.org/10.1523/JNEUROSCI.5467-07.2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Wu, S., Zheng, S. D., Huang, H. L., Yan, L. C., Yin, X. F., et al. (2013) Lithium down-regulates histone deacetylase 1 (HDAC1) and induces degradation of mutant huntingtin, J. Biol. Chem., 288, 35500-35510, https://doi.org/10.1074/jbc.M113.479865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Wakayama, S., Kohda, T., Obokata, H., Tokoro, M., Li, C., et al. (2013) Successful serial recloning in the mouse over multiple generations, Cell Stem Cell, 12, 293-297, https://doi.org/10.1016/j.stem.2013.01.005.

    Article  CAS  PubMed  Google Scholar 

  112. Cao, R., Li, A., Cho, H. Y., Lee, B., and Obrietan, K. (2010) Mammalian target of rapamycin signaling modulates photic entrainment of the suprachiasmatic circadian clock, J. Neurosci., 30, 6302-6314, https://doi.org/10.1523/JNEUROSCI.5482-09.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Chaves, I., van der Horst, G. T., Schellevis, R., Nijman, R. M., Koerkamp, M. G., et al. (2014) Insulin-FOXO3 signaling modulates circadian rhythms via regulation of clock transcription, Curr. Biol., 24, 1248-1255, https://doi.org/10.1016/j.cub.2014.04.018.

    Article  CAS  PubMed  Google Scholar 

  114. Lee, Y., and Kim, E. K. (2013) AMP-activated protein kinase as a key molecular link between metabolism and clockwork, Exp. Mol. Med., 45, e33, https://doi.org/10.1038/emm.2013.65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Lamia, K. A., Sachdeva, U. M., DiTacchio, L., Williams, E. C., Alvarez, J. G., et al. (2009) AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation, Science, 326, 437-440, https://doi.org/10.1126/science.1172156.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Brown-Borg, H. M., Borg, K. E., Meliska, C. J., and Bartke, A. (1996) Dwarf mice and the ageing process, Nature, 384, 33, https://doi.org/10.1038/384033a0.

    Article  CAS  PubMed  Google Scholar 

  117. Martin-Montalvo, A., Mercken, E. M., Mitchell, S. J., Palacios, H. H., Mote, P. L., et al. (2013) Metformin improves healthspan and lifespan in mice, Nat. Commun., 4, 2192, https://doi.org/10.1038/ncomms3192.

    Article  CAS  PubMed  Google Scholar 

  118. Stein-Behrens, B. A., and Sapolsky, R. M. (1992) Stress, glucocorticoids, and aging, Aging (Milano), 4, 197-210, https://doi.org/10.1007/BF03324092.

    Article  CAS  Google Scholar 

  119. Dracott, B. N., and Smith, C. E. (1979) Hydrocortisone and the antibody response in mice. I. Correlations between serum cortisol levels and cell numbers in thymus, spleen, marrow and lymph nodes, Immunology, 38, 429-435.

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Franceschi, C., Bonafe, M., Valensin, S., Olivieri, F., De Luca, M., et al. (2000) Inflamm-aging. An evolutionary perspective on immunosenescence, Ann. N. Y. Acad. Sci., 908, 244-254, https://doi.org/10.1111/j.1749-6632.2000.tb06651.x.

    Article  CAS  PubMed  Google Scholar 

  121. De Jesus, E. G., and Hirano, T. (1992) Changes in whole body concentrations of cortisol, thyroid hormones, and sex steroids during early development of the chum salmon, Oncorhynchus keta, Gen. Comp. Endocrinol., 85, 55-61, https://doi.org/10.1016/0016-6480(92)90171-f.

    Article  CAS  PubMed  Google Scholar 

  122. Atwood, C. S., Hayashi, K., Meethal, S. V., Gonzales, T., and Bowen, R. L. (2017) Does the degree of endocrine dyscrasia post-reproduction dictate post-reproductive lifespan? Lessons from semelparous and iteroparous species, Geroscience, 39, 103-116, https://doi.org/10.1007/s11357-016-9955-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Jeffries, K. M., Hinch, S. G., Donaldson, M. R., Gale, M. K., Burt, J. M., et al. (2011) Temporal changes in blood variables during final maturation and senescence in male sockeye salmon Oncorhynchus nerka: reduced osmoregulatory ability can predict mortality, J. Fish Biol., 79, 449-465, https://doi.org/10.1111/j.1095-8649.2011.03042.x.

    Article  CAS  PubMed  Google Scholar 

  124. Poskittt, D. C., Barnett, J., Duffey, K., Kimpton, W. G., and Muller, H. K. (1984) Involution of the thymus in marsupial mice, Dev. Comp. Immunol., 8, 483-488, https://doi.org/10.1016/0145-305x(84)90056-9.

    Article  CAS  PubMed  Google Scholar 

  125. McQuillan, H. J., Lokman, P. M., and Young, G. (2003) Effects of sex steroids, sex, and sexual maturity on cortisol production: An in vitro comparison of chinook salmon and rainbow trout interrenals, Gen. Comp. Endocrinol., 133, 154-163, https://doi.org/10.1016/s0016-6480(03)00163-1.

    Article  CAS  PubMed  Google Scholar 

  126. Matos, L., Gouveia, A., and Almeida, H. (2012) Copper ability to induce premature senescence in human fibroblasts, Age (Dordr), 34, 783-794, https://doi.org/10.1007/s11357-011-9276-7.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to Claudia Rubie (Medizinische Fakultät der Universität des Saarlandes) for reinforcing the assumption of the possibilities on regulated aging in a personal talk during the Conference Dinner at the Symposium of the Heart Centre University Hospital of Halle (Saale) in September 2019.

We are grateful to the Biodiversity Heritage Library and the University of Toronto – Gerstein Science Information Centre as well as to the University Library of Freiburg for providing public access to Weismann’s work.

Funding

This study was financially supported by the Deutsche Forschungsgemeinschaft (DFG) in the Research Training Group 2155 (ProMoAge).

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  1. Martin-Luther-University of Halle-Wittenberg, 06120, Halle (Saale), Germany

    Patrick R. Winterhalter & Andreas Simm

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  1. Patrick R. Winterhalter
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PRW is responsible for the drafting of the manuscript. AS corrected the manuscript and provided access to the field of aging research.

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Correspondence to Patrick R. Winterhalter.

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The authors declare no conflicts of interest in financial or any other sphere. This article does not contain description of studies with the involvement of humans or animal subjects performed by any of the authors.

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Winterhalter, P.R., Simm, A. How Justified is the Assumption of Programmed Aging in Reminiscence of Weismann’s Theories?. Biochemistry Moscow 87, 35–53 (2022). https://doi.org/10.1134/S0006297922010047

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