Advertisement

pp 1-22 | Cite as

Mitochondria Inspire a Lifestyle

  • Peter Kramer
  • Paola Bressan
Chapter
Part of the Advances in Anatomy, Embryology and Cell Biology book series

Abstract

Tucked inside our cells, we animals (and plants, and fungi) carry mitochondria, minuscule descendants of bacteria that invaded our common ancestor 2 billion years ago. This unplanned breakthrough endowed our ancestors with a convenient, portable source of energy, enabling them to progress towards more ambitious forms of life. Mitochondria still manufacture most of our energy; we have evolved to invest it to grow and produce offspring, and to last long enough to make it all happen. Yet because the continuous generation of energy is inevitably linked to that of toxic free radicals, mitochondria give us life and give us death. Stripping away clutter and minutiae, here we present a big-picture perspective of how mitochondria work, how they are passed on virtually only by mothers, and how they shape the lifestyles of species and individuals. We discuss why restricting food prolongs lifespan, why reproducing shortens it, and why moving about protects us from free radicals despite increasing their production. We show that our immune cells use special mitochondria to keep control over our gut microbes. And we lay out how the fabrication of energy and free radicals sets the internal clocks that command our everyday rhythms—waking, eating, sleeping. Mitochondria run the show.

Keywords

Antioxidants Circadian rhythms Dietary restriction Free radicals Longevity Mitochondria 

References

  1. Adler MI, Bonduriansky R (2014) Why do the well-fed appear to die young? Bioessays 36:439–450.  https://doi.org/10.1002/bies.201300165CrossRefGoogle Scholar
  2. Allen JF (1996) Separate sexes and the mitochondrial theory of ageing. J Theor Biol 180:135–140.  https://doi.org/10.1006/jtbi.1996.0089CrossRefGoogle Scholar
  3. Allen JF, de Paula WBM (2013) Mitochondrial genome function and maternal inheritance. Biochem Soc Trans 41:1298–1304.  https://doi.org/10.1042/BST20130106CrossRefGoogle Scholar
  4. Angajala A, Lim S, Phillips JB et al (2018) Diverse roles of mitochondria in immune responses: novel insights into immuno-metabolism. Front Immunol 9:1605.  https://doi.org/10.3389/fimmu.2018.01605CrossRefGoogle Scholar
  5. Anthony TG, Morrison CD, Gettys TW (2013) Remodeling of lipid metabolism by dietary restriction of essential amino acids. Diabetes 62:2635–2644.  https://doi.org/10.2337/db12-1613CrossRefGoogle Scholar
  6. Aschoff J (1993) On the relationship between motor activity and the sleep-wake cycle in humans during temporal isolation. J Biol Rhythm 8:33–46.  https://doi.org/10.1177/074873049300800103CrossRefGoogle Scholar
  7. Aschoff J, von Goetz C, Wildgruber C et al (1986) Meal timing in humans during isolation without time cues. J Biol Rhythm 1:151–162.  https://doi.org/10.1177/074873048600100206CrossRefGoogle Scholar
  8. Banerjee R, Chiku T, Kabil O et al (2015) Assay methods for H2S biogenesis and catabolism enzymes. In: Cadenas E, Packer L (eds) Hydrogen sulfide in redox biology, part A. Methods in enzymology, vol 554. Elsevier, Amsterdam, pp 189–200Google Scholar
  9. Barja G (2013) Updating the mitochondrial free radical theory of aging: an integrated view, key aspects, and confounding concepts. Antioxid Redox Signal 19:1420–1445.  https://doi.org/10.1089/ars.2012.5148CrossRefGoogle Scholar
  10. Bartke A (2017) Somatic growth, aging, and longevity. NPJ Aging Mech Dis 3:14.  https://doi.org/10.1038/s41514-017-0014-yCrossRefGoogle Scholar
  11. Bartke A, Sun LY, Longo V (2013) Somatotropic signaling: trade-offs between growth, reproductive development, and longevity. Physiol Rev 93:571–598.  https://doi.org/10.1152/physrev.00006.2012CrossRefGoogle Scholar
  12. Bastiaanssen TF, Cowan CS, Claesson MJ et al (2018) Making sense of … the microbiome in psychiatry. Int J Neuropsychopharmacol.  https://doi.org/10.1093/ijnp/pyy067/25437947/pyy067.pdf
  13. Björkman M, Klingen I, Birch AN et al (2011) Phytochemicals of Brassicaceae in plant protection and human health – influences of climate, environment and agronomic practice. Phytochemistry 72:538–556.  https://doi.org/10.1016/j.phytochem.2011.01.014CrossRefGoogle Scholar
  14. Blachier F, Mariotti F, Huneau JF et al (2007) Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 33:547–562.  https://doi.org/10.1007/s00726-006-0477-9CrossRefGoogle Scholar
  15. Blagosklonny MV (2013) Big mice die young but large animals live longer. Aging 5:227–233.  https://doi.org/10.18632/aging.100551CrossRefGoogle Scholar
  16. Borbély AA, Daan S, Wirz-Justice A et al (2016) The two-process model of sleep regulation: a reappraisal. J Sleep Res 25:131–143.  https://doi.org/10.1111/jsr.12371CrossRefGoogle Scholar
  17. Boyer PD (1975) A model for conformational coupling of membrane potential and proton translocation to ATP synthesis and to active transport. FEBS Lett 58:1–6Google Scholar
  18. Branco AF, Ferreira A, Simões RF et al (2016) Ketogenic diets: from cancer to mitochondrial diseases and beyond. Eur J Clin Investig 46:285–298.  https://doi.org/10.1111/eci.12591CrossRefGoogle Scholar
  19. Brand MD, Couture P, Else PL et al (1991) Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 275:81–86Google Scholar
  20. Bressan P (2018) Inside a mitochondrion [Figure]. Figshare.  https://doi.org/10.6084/m9.figshare.6877205. https://figshare.com/s/5d90908b41fe3524efc0. Accessed 1 Aug 2018
  21. Bressan P, Kramer P (2016) Bread and other edible agents of mental disease. Front Hum Neurosci 10:130Google Scholar
  22. Camberos-Luna L, Gerónimo-Olvera C, Montiel T et al (2016) The ketone body, β-hydroxybutyrate stimulates the autophagic flux and prevents neuronal death induced by glucose deprivation in cortical cultured neurons. Neurochem Res 41:600–609.  https://doi.org/10.1007/s11064-015-1700-4CrossRefGoogle Scholar
  23. Camus MF, Wolf JB, Morrow EH et al (2015) Single nucleotides in the mtDNA sequence modify mitochondrial molecular function and are associated with sex-specific effects on fertility and aging. Curr Biol 25:2717–2722.  https://doi.org/10.1016/j.cub.2015.09.012CrossRefGoogle Scholar
  24. Cann RL, Stoneking M, Wilson AC (1987) Mitochondrial DNA and human evolution. Nature 325:31–36.  https://doi.org/10.1038/325031a0CrossRefGoogle Scholar
  25. Cao R, Lee B, Cho H-Y et al (2008) Photic regulation of the mTOR signaling pathway in the suprachiasmatic circadian clock. Mol Cell Neurosci 38:312–324.  https://doi.org/10.1016/j.mcn.2008.03.005CrossRefGoogle Scholar
  26. Cao R, Li A, Cho H-Y et al (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.5482-09.2010CrossRefGoogle Scholar
  27. Cao X, Zhao Z-W, Zhou H-Y et al (2012) Effects of exercise intensity on copy number and mutations of mitochondrial DNA in gastrocnemus muscles in mice. Mol Med Rep 6:426–428.  https://doi.org/10.3892/mmr.2012.913CrossRefGoogle Scholar
  28. Clark A, Mach N (2017) The crosstalk between the gut microbiota and mitochondria during exercise. Front Physiol 8:319.  https://doi.org/10.3389/fphys.2017.00319CrossRefGoogle Scholar
  29. Daan S, Honma S, Honma K-I (2013) Body temperature predicts the direction of internal desynchronization in humans isolated from time cues. J Biol Rhythm 28:403–411.  https://doi.org/10.1177/0748730413514357CrossRefGoogle Scholar
  30. de Paula WBM, Lucas CH, Agip A-NA et al (2013) Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template. Philos Trans R Soc Lond Ser B Biol Sci 368:20120263.  https://doi.org/10.1098/rstb.2012.0263CrossRefGoogle Scholar
  31. Depner CM, Melanson EL, McHill AW et al (2018) Mistimed food intake and sleep alters 24-hour time-of-day patterns of the human plasma proteome. Proc Natl Acad Sci U S A 115:E5390–E5399.  https://doi.org/10.1073/pnas.1714813115CrossRefGoogle Scholar
  32. Dong Z, Sinha R, Richie JP (2018) Disease prevention and delayed aging by dietary sulfur amino acid restriction: translational implications. Ann N Y Acad Sci 1418:44–55.  https://doi.org/10.1111/nyas.13584CrossRefGoogle Scholar
  33. Ellison PT (2017) Endocrinology, energetics, and human life history: a synthetic model. Horm Behav 91:97–106.  https://doi.org/10.1016/j.yhbeh.2016.09.006CrossRefGoogle Scholar
  34. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span – from yeast to humans. Science 328:321–326.  https://doi.org/10.1126/science.1172539CrossRefGoogle Scholar
  35. Forney LA, Stone KP, Wanders D et al (2017a) Sensing and signaling mechanisms linking dietary methionine restriction to the behavioral and physiological components of the response. Front Neuroendocrinol 51:36–45.  https://doi.org/10.1016/j.yfrne.2017.12.002CrossRefGoogle Scholar
  36. Forney LA, Wanders D, Stone KP et al (2017b) Concentration-dependent linkage of dietary methionine restriction to the components of its metabolic phenotype. Obesity 25:730–738.  https://doi.org/10.1002/oby.21806CrossRefGoogle Scholar
  37. Gano LB, Patel M, Rho JM (2014) Ketogenic diets, mitochondria, and neurological diseases. J Lipid Res 55:2211–2228Google Scholar
  38. Gilbert JA, Quinn RA, Debelius J et al (2016) Microbiome-wide association studies link dynamic microbial consortia to disease. Nature 535:94–103.  https://doi.org/10.1038/nature18850CrossRefGoogle Scholar
  39. Goto S, Naito H, Kaneko T et al (2007) Hormetic effects of regular exercise in aging: correlation with oxidative stress. Appl Physiol Nutr Metab 32:948–953.  https://doi.org/10.1139/H07-092CrossRefGoogle Scholar
  40. Gradari S, Pallé A, McGreevy KR et al (2016) Can exercise make you smarter, happier, and have more neurons? A hormetic perspective. Front Neurosci 10:93.  https://doi.org/10.3389/fnins.2016.00093CrossRefGoogle Scholar
  41. Green J, Pollak CP, Smith GP (1987) Meal size and intermeal interval in human subjects in time isolation. Physiol Behav 41:141–147Google Scholar
  42. Haldane JBS (1926) On being the right size. Harper Mag 152:424–427Google Scholar
  43. Hao S, Sharp JW, Ross-Inta CM et al (2005) Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science 307:1776–1778.  https://doi.org/10.1126/science.1104882CrossRefGoogle Scholar
  44. Hasek BE, Stewart LK, Henagan TM et al (2010) Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states. Am J Physiol Regul Integr Comp Physiol 299:R728–R739.  https://doi.org/10.1152/ajpregu.00837.2009CrossRefGoogle Scholar
  45. He Q, Morris BJ, Grove JS et al (2014) Shorter men live longer: association of height with longevity and FOXO3 genotype in American men of Japanese ancestry. PLoS One 9:e94385.  https://doi.org/10.1371/journal.pone.0094385CrossRefGoogle Scholar
  46. He F, Li J, Liu Z et al (2016) Redox mechanism of reactive oxygen species in exercise. Front Physiol 7:486.  https://doi.org/10.3389/fphys.2016.00486CrossRefGoogle Scholar
  47. Herbert M, Turnbull D (2018) Progress in mitochondrial replacement therapies. Nat Rev Mol Cell Biol 19:71–72.  https://doi.org/10.1038/nrm.2018.3CrossRefGoogle Scholar
  48. Hernández-Julián R, Mansour H, Peters C (2014) The effects of intrauterine malnutrition on birth and fertility outcomes: evidence from the 1974 Bangladesh famine. Demography 51:1775–1796.  https://doi.org/10.1007/s13524-014-0326-5CrossRefGoogle Scholar
  49. Herrero A, Barja G (1997) ADP-regulation of mitochondrial free radical production is different with complex I- or complex II-linked substrates: implications for the exercise paradox and brain hypermetabolism. J Bioenerg Biomembr 29:241–249Google Scholar
  50. Hiendleder S (2007) Mitochondrial DNA inheritance after SCNT. Adv Exp Med Biol 591:103–116.  https://doi.org/10.1007/978-0-387-37754-4_8CrossRefGoogle Scholar
  51. Hirose M, Künstner A, Schilf P et al (2017) Mitochondrial gene polymorphism is associated with gut microbial communities in mice. Sci Rep 7:15293.  https://doi.org/10.1038/s41598-017-15377-7CrossRefGoogle Scholar
  52. Hood DA, Uguccioni G, Vainshtein A et al (2011) Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle: implications for health and disease. Compr Physiol 1:1119–1134.  https://doi.org/10.1002/cphy.c100074CrossRefGoogle Scholar
  53. Hugon P, Dufour J-C, Colson P et al (2015) A comprehensive repertoire of prokaryotic species identified in human beings. Lancet Infect Dis 15:1211–1219.  https://doi.org/10.1016/s1473-3099(15)00293-5CrossRefGoogle Scholar
  54. Hull KL, Harvey S (2014) Growth hormone and reproduction: a review of endocrine and autocrine/paracrine interactions. Int J Endocrinol 2014:1–24.  https://doi.org/10.1155/2014/234014CrossRefGoogle Scholar
  55. Ikeda M, Ikeda-Sagara M, Okada T et al (2005) Brain oxidation is an initial process in sleep induction. Neuroscience 130:1029–1040.  https://doi.org/10.1016/j.neuroscience.2004.09.057CrossRefGoogle Scholar
  56. Inoué S, Honda K, Komoda Y (1995) Sleep as neuronal detoxification and restitution. Behav Brain Res 69:91–96Google Scholar
  57. Jansen RP (2000) Germline passage of mitochondria: quantitative considerations and possible embryological sequelae. Hum Reprod 15(Suppl 2):112–128Google Scholar
  58. Johnston IG, Williams BP (2016) Evolutionary inference across eukaryotes identifies specific pressures favoring mitochondrial gene retention. Cell Syst 2:101–111.  https://doi.org/10.1016/j.cels.2016.01.013CrossRefGoogle Scholar
  59. Kalghatgi S, Spina CS, Costello JC et al (2013) Bactericidal antibiotics induce mitochondrial dysfunction and oxidative damage in mammalian cells. Sci Transl Med 5:192ra85.  https://doi.org/10.1126/scitranslmed.3006055CrossRefGoogle Scholar
  60. Karami-Mohajeri S, Abdollahi M (2013) Mitochondrial dysfunction and organophosphorus compounds. Toxicol Appl Pharmacol 270:39–44.  https://doi.org/10.1016/j.taap.2013.04.001CrossRefGoogle Scholar
  61. Kauppila JH, Stewart JB (2015) Mitochondrial DNA: radically free of free-radical driven mutations. Biochim Biophys Acta 1847:1354–1361.  https://doi.org/10.1016/j.bbabio.2015.06.001CrossRefGoogle Scholar
  62. Keeney KM, Yurist-Doutsch S, Arrieta MC et al (2014) Effects of antibiotics on human microbiota and subsequent disease. Annu Rev Microbiol 68:217–235.  https://doi.org/10.1146/annurev-micro-091313-103456CrossRefGoogle Scholar
  63. Kellingray L, Tapp HS, Saha S et al (2017) Consumption of a diet rich in Brassica vegetables is associated with a reduced abundance of sulphate-reducing bacteria: a randomised crossover study. Mol Nutr Food Res 61:1600992.  https://doi.org/10.1002/mnfr.201600992CrossRefGoogle Scholar
  64. Klein EY, Van Boeckel TP, Martinez EM et al (2018) Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A 115:E3463–E3470.  https://doi.org/10.1073/pnas.1717295115CrossRefGoogle Scholar
  65. Kondratova AA, Kondratov RV (2012) The circadian clock and pathology of the ageing brain. Nat Rev Neurosci 13:325–335.  https://doi.org/10.1038/nrn3208CrossRefGoogle Scholar
  66. Konjar S, Frising UC, Ferreira C et al (2018) Mitochondria maintain controlled activation state of epithelial-resident T lymphocytes. Sci Immunol 3:eaan2543.  https://doi.org/10.1126/sciimmunol.aan2543CrossRefGoogle Scholar
  67. Kramer P, Bressan P (2015) Humans as superorganisms: how microbes, viruses, imprinted genes, and other selfish entities shape our behavior. Perspect Psychol Sci 10:464–481.  https://doi.org/10.1177/1745691615583131CrossRefGoogle Scholar
  68. Kramer P, Bressan P (2018) Our (mother’s) mitochondria and our mind. Perspect Psychol Sci 13:88–100.  https://doi.org/10.1177/174569161771835CrossRefGoogle Scholar
  69. Laje R, Agostino PV, Golombek DA (2018) The times of our lives: interaction among different biological periodicities. Front Integr Neurosci 12:10.  https://doi.org/10.3389/fnint.2018.00010CrossRefGoogle Scholar
  70. Lane N (2005) Power, sex, suicide: mitochondria and the meaning of life. Oxford University Press, OxfordGoogle Scholar
  71. Lane N (2011) The costs of breathing. Science 334:184–185.  https://doi.org/10.1126/science.1214012CrossRefGoogle Scholar
  72. Lane N (2015) The vital question: why is life the way it is? Profile Books, LondonGoogle Scholar
  73. Lemaître JF, Berger V, Bonenfant C et al (2015) Early-late life trade-offs and the evolution of ageing in the wild. Proc Biol Sci 282:20150209.  https://doi.org/10.1098/rspb.2015.0209CrossRefGoogle Scholar
  74. Lewin N, Swanson EM, Williams BL et al (2017) Juvenile concentrations of IGF-1 predict life-history trade-offs in a wild mammal. Funct Ecol 31:894–902.  https://doi.org/10.1111/1365-2435.12808CrossRefGoogle Scholar
  75. Linden DR (2014) Hydrogen sulfide signaling in the gastrointestinal tract. Antioxid Redox Signal 20:818–830.  https://doi.org/10.1089/ars.2013.5312CrossRefGoogle Scholar
  76. Liu C, Chung M (2015) Genetics and epigenetics of circadian rhythms and their potential roles in neuropsychiatric disorders. Neurosci Bull 31:141–159.  https://doi.org/10.1007/s12264-014-1495-3CrossRefGoogle Scholar
  77. Longo VD, Mattson MP (2014) Fasting: molecular mechanisms and clinical applications. Cell Metab 19:181–192.  https://doi.org/10.1016/j.cmet.2013.12.008CrossRefGoogle Scholar
  78. López-Armada MJ, Riveiro-Naveira RR, Vaamonde-García C et al (2013) Mitochondrial dysfunction and the inflammatory response. Mitochondrion 13:106–118.  https://doi.org/10.1016/j.mito.2013.01.003CrossRefGoogle Scholar
  79. López-Torres M, Barja G (2008) Lowered methionine ingestion as responsible for the decrease in rodent mitochondrial oxidative stress in protein and dietary restriction. Biochim Biophys Acta 1780:1337–1347.  https://doi.org/10.1016/j.bbagen.2008.01.007CrossRefGoogle Scholar
  80. Martin WF, Neukirchen S, Zimorski V et al (2016) Energy for two: new archaeal lineages and the origin of mitochondria. Bioessays 38:850–856.  https://doi.org/10.1002/bies.201600089CrossRefGoogle Scholar
  81. Martínez-Redondo D, Marcuello A, Casajús JA et al (2010) Human mitochondrial haplogroup H: the highest VO2max consumer – is it a paradox? Mitochondrion 10:102–107.  https://doi.org/10.1016/j.mito.2009.11.005CrossRefGoogle Scholar
  82. Maruszak A, Adamczyk JG, Siewierski M et al (2014) Mitochondrial DNA variation is associated with elite athletic status in the Polish population. Scand J Med Sci Sports 24:311–318.  https://doi.org/10.1111/sms.12012CrossRefGoogle Scholar
  83. Matheu A, Maraver A, Klatt P et al (2007) Delayed ageing through damage protection by the Arf/p53 pathway. Nature 448:375–379.  https://doi.org/10.1038/nature05949CrossRefGoogle Scholar
  84. Merry TL, Ristow M (2016) Do antioxidant supplements interfere with skeletal muscle adaptation to exercise training? J Physiol 594:5135–5147.  https://doi.org/10.1113/jp270654CrossRefGoogle Scholar
  85. Meyer JN, Leung MC, Rooney JP et al (2013) Mitochondria as a target of environmental toxicants. Toxicol Sci 134:1–17.  https://doi.org/10.1093/toxsci/kft102CrossRefGoogle Scholar
  86. Miller VJ, Villamena FA, Volek JS (2018) Nutritional ketosis and mitohormesis: potential implications for mitochondrial function and human health. J Nutr Metab 2018:1–27.  https://doi.org/10.1155/2018/5157645CrossRefGoogle Scholar
  87. Mostafalou S, Abdollahi M (2013) Pesticides and human chronic diseases: evidences, mechanisms, and perspectives. Toxicol Appl Pharmacol 268:157–177.  https://doi.org/10.1016/j.taap.2013.01.025CrossRefGoogle Scholar
  88. Mottawea W, Chiang C-K, Mühlbauer M et al (2016) Altered intestinal microbiota–host mitochondria crosstalk in new onset Crohn’s disease. Nat Commun 7:13419.  https://doi.org/10.1038/ncomms13419CrossRefGoogle Scholar
  89. Myers JH (1978) Sex ratio adjustment under food stress: maximization of quality or numbers of offspring. Am Nat 112:381–388Google Scholar
  90. Navara KJ (2014) Low gestational weight gain skews human sex ratios towards females. PLoS One 9:e114304.  https://doi.org/10.1371/journal.pone.0114304CrossRefGoogle Scholar
  91. Newman JC, Verdin E (2014) Ketone bodies as signaling metabolites. Trends Endocrinol Metab 25:42–52.  https://doi.org/10.1016/j.tem.2013.09.002CrossRefGoogle Scholar
  92. Omote H, Sambonmatsu N, Saito K et al (1999) The γ-subunit rotation and torque generation in F1-ATPase from wild-type or uncoupled mutant Escherichia coli. Proc Natl Acad Sci U S A 96:7780–7784Google Scholar
  93. O’Neill JS, Reddy AB (2011) Circadian clocks in human red blood cells. Nature 469:498–503.  https://doi.org/10.1038/nature09702CrossRefGoogle Scholar
  94. Pal VK, Bandyopadhyay P, Singh A (2018) Hydrogen sulfide in physiology and pathogenesis of bacteria and viruses. IUBMB Life 70:393–410.  https://doi.org/10.1002/iub.1740CrossRefGoogle Scholar
  95. Pamplona R, Barja G (2006) Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection. Biochim Biophys Acta 1757:496–508.  https://doi.org/10.1016/j.bbabio.2006.01.009CrossRefGoogle Scholar
  96. Penn DJ, Smith KR (2007) Differential fitness costs of reproduction between the sexes. Proc Natl Acad Sci U S A 104:553–558.  https://doi.org/10.1073/pnas.0609301103CrossRefGoogle Scholar
  97. Peternelj TT, Coombes JS (2011) Antioxidant supplementation during exercise training: beneficial or detrimental? Sports Med 41:1043–1069.  https://doi.org/10.2165/11594400-000000000-00000CrossRefGoogle Scholar
  98. Pitnick S, Karr TL (1998) Paternal products and by-products in Drosophila development. Proc Biol Sci 265:821–826.  https://doi.org/10.1098/rspb.1998.0366CrossRefGoogle Scholar
  99. Powers SK, Jackson MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243–1276.  https://doi.org/10.1152/physrev.00031.2007CrossRefGoogle Scholar
  100. Pyle A, Hudson G, Wilson IJ et al (2015) Extreme-depth re-sequencing of mitochondrial DNA finds no evidence of paternal transmission in humans. PLoS Genet 11:e1005040.  https://doi.org/10.1371/journal.pgen.1005040CrossRefGoogle Scholar
  101. Radak Z, Chung HY, Koltai E et al (2008) Exercise, oxidative stress and hormesis. Ageing Res Rev 7:34–42.  https://doi.org/10.1016/j.arr.2007.04.004CrossRefGoogle Scholar
  102. Radak Z, Zhao Z, Koltai E et al (2013) Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid Redox Signal 18:1208–1246.  https://doi.org/10.1089/ars.2011.4498CrossRefGoogle Scholar
  103. Radak Z, Ishihara K, Tekus E et al (2017) Exercise, oxidants, and antioxidants change the shape of the bell-shaped hormesis curve. Redox Biol 12:285–290.  https://doi.org/10.1016/j.redox.2017.02.015CrossRefGoogle Scholar
  104. Rahman J, Rahman S (2018) Mitochondrial medicine in the omics era. Lancet 391:2560–2574.  https://doi.org/10.1016/S0140-6736(18)30727-XCrossRefGoogle Scholar
  105. Ramanathan C, Kathale ND, Liu D et al (2018) mTOR signaling regulates central and peripheral circadian clock function. PLoS Genet 14:e1007369.  https://doi.org/10.1371/journal.pgen.1007369CrossRefGoogle Scholar
  106. Reddy AB, Rey G (2014) Metabolic and nontranscriptional circadian clocks: eukaryotes. Annu Rev Biochem 83:165–189.  https://doi.org/10.1146/annurev-biochem-060713-035623CrossRefGoogle Scholar
  107. Redman LM, Smith SR, Burton JH et al (2018) Metabolic slowing and reduced oxidative damage with sustained caloric restriction support the rate of living and oxidative damage theories of aging. Cell Metab 27:805–815.e4.  https://doi.org/10.1016/j.cmet.2018.02.019CrossRefGoogle Scholar
  108. Reiter RJ, Rosales-Corral S, Tan DX et al (2017) Melatonin as a mitochondria-targeted antioxidant: one of evolution’s best ideas. Cell Mol Life Sci 74:3863–3881.  https://doi.org/10.1007/s00018-017-2609-7CrossRefGoogle Scholar
  109. Rich P (2003) The cost of living. Nature 421:583.  https://doi.org/10.1038/421583aCrossRefGoogle Scholar
  110. Ristow M, Zarse K, Oberbach A et al (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 106:8665–8670.  https://doi.org/10.1073/pnas.0903485106CrossRefGoogle Scholar
  111. Roenneberg T, Merrow M (2016) The circadian clock and human health. Curr Biol 26:R432–R443.  https://doi.org/10.1016/j.cub.2016.04.011CrossRefGoogle Scholar
  112. Rogers GB, Keating DJ, Young RL et al (2016) From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol Psychiatry 21:738–748.  https://doi.org/10.1038/mp.2016.50CrossRefGoogle Scholar
  113. Rutter J, Reick M, McKnight SL (2002) Metabolism and the control of circadian rhythms. Annu Rev Biochem 71:307–331.  https://doi.org/10.1146/annurev.biochem.71.090501.142857CrossRefGoogle Scholar
  114. Sato M, Sato K (2013) Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochim Biophys Acta 1833:1979–1984.  https://doi.org/10.1016/j.bbamcr.2013.03.010CrossRefGoogle Scholar
  115. Schulz TJ, Zarse K, Voigt A et al (2007) Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 6:280–293.  https://doi.org/10.1016/j.cmet.2007.08.011CrossRefGoogle Scholar
  116. Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14:e1002533.  https://doi.org/10.1371/journal.pbio.1002533CrossRefGoogle Scholar
  117. Sharpley MS, Marciniak C, Eckel-Mahan K et al (2012) Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell 151:333–343.  https://doi.org/10.1016/j.cell.2012.09.004CrossRefGoogle Scholar
  118. Song S (2012) Does famine influence sex ratio at birth? Evidence from the 1959–1961 great leap forward famine in China. Proc Biol Sci 279:2883–2890.  https://doi.org/10.1098/rspb.2012.0320CrossRefGoogle Scholar
  119. Song S (2015) Privation, stress, and human sex ratio at birth. Early Hum Dev 91:823–827.  https://doi.org/10.1016/j.earlhumdev.2015.10.009CrossRefGoogle Scholar
  120. Soong RK, Bachand GD, Neves HP et al (2000) Powering an inorganic nanodevice with a biomolecular motor. Science 290:1555–1558Google Scholar
  121. Stojković B, Sayadi A, Đorđević M et al (2017) Divergent evolution of life span associated with mitochondrial DNA evolution. Evolution 71:160–166.  https://doi.org/10.1111/evo.13102CrossRefGoogle Scholar
  122. Strong M (2004) Protein nanomachines. PLoS Biol 2:e73Google Scholar
  123. Stuart JA, Page MM (2010) Plasma IGF-1 is negatively correlated with body mass in a comparison of 36 mammalian species. Mech Ageing Dev 131:591–598.  https://doi.org/10.1016/j.mad.2010.08.005CrossRefGoogle Scholar
  124. Suh Y, Atzmon G, Cho MO et al (2008) Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc Natl Acad Sci U S A 105:3438–3442.  https://doi.org/10.1073/pnas.0705467105CrossRefGoogle Scholar
  125. Sulak M, Fong L, Mika K et al (2016) TP53 copy number expansion is associated with the evolution of increased body size and an enhanced DNA damage response in elephants. Elife 5:e11994Google Scholar
  126. Sutovsky P, Moreno RD, Ramalho-Santos J et al (1999) Ubiquitin tag for sperm mitochondria. Nature 402:371–372.  https://doi.org/10.1038/46466CrossRefGoogle Scholar
  127. Swanson EM, Dantzer B (2014) Insulin-like growth factor-1 is associated with life-history variation across Mammalia. Proc R Soc Lond B Biol Sci 281:20132458.  https://doi.org/10.1098/rspb.2013.2458CrossRefGoogle Scholar
  128. Tabatabaie V, Atzmon G, Rajpathak SN et al (2011) Exceptional longevity is associated with decreased reproduction. Aging 3:1202–1205.  https://doi.org/10.18632/aging.100415CrossRefGoogle Scholar
  129. Templeman NM, Murphy CT (2018) Regulation of reproduction and longevity by nutrient-sensing pathways. J Cell Biol 217:93–106.  https://doi.org/10.1083/jcb.201707168CrossRefGoogle Scholar
  130. Tian X, Seluanov A, Gorbunova V (2017) Molecular mechanisms determining lifespan in short- and long-lived species. Trends Endocrinol Metab 28:722–734.  https://doi.org/10.1016/j.tem.2017.07.004CrossRefGoogle Scholar
  131. Trewin A, Berry B, Wojtovich A (2018) Exercise and mitochondrial dynamics: keeping in shape with ROS and AMPK. Antioxidants 7:7.  https://doi.org/10.3390/antiox7010007CrossRefGoogle Scholar
  132. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92Google Scholar
  133. Ueno H, Suzuki T, Kinosita K et al (2005) ATP-driven stepwise rotation of FoF1-ATP synthase. Proc Natl Acad Sci U S A 102:1333–1338.  https://doi.org/10.1073/pnas.0407857102CrossRefGoogle Scholar
  134. Villanueva C, Kross RD (2012) Antioxidant-induced stress. Int J Mol Sci 13:2091–2109.  https://doi.org/10.3390/ijms13022091CrossRefGoogle Scholar
  135. Vitale G, Brugts MP, Ogliari G et al (2012) Low circulating IGF-I bioactivity is associated with human longevity: findings in centenarians’ offspring. Aging 4:580–589.  https://doi.org/10.18632/aging.100484CrossRefGoogle Scholar
  136. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407.  https://doi.org/10.1146/annurev.genet.39.110304.095751CrossRefGoogle Scholar
  137. Wanders D, Burk DH, Cortez CC et al (2015) UCP1 is an essential mediator of the effects of methionine restriction on energy balance but not insulin sensitivity. FASEB J 29:2603–2615.  https://doi.org/10.1096/fj.14-270348CrossRefGoogle Scholar
  138. Wang X, Ryu D, Houtkooper RH et al (2015) Antibiotic use and abuse: a threat to mitochondria and chloroplasts with impact on research, health, and environment. Bioessays 37:1045–1053.  https://doi.org/10.1002/bies.201500071CrossRefGoogle Scholar
  139. Yao CK, Muir JG, Gibson PR (2016) Review article: insights into colonic protein fermentation, its modulation and potential health implications. Aliment Pharmacol Ther 43:181–196.  https://doi.org/10.1111/apt.13456CrossRefGoogle Scholar
  140. Zarse K, Schmeisser S, Groth M et al (2012) Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab 15:451–465.  https://doi.org/10.1016/j.cmet.2012.02.013CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Dipartimento di Psicologia GeneraleUniversity of PadovaPadovaItaly

Personalised recommendations