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Of Mice, Whales, Jellyfish and Men: In Pursuit of Increased Longevity

  • Paul C. Guest
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1178)

Abstract

The quest for increased human longevity has been a goal of mankind throughout recorded history. Recent molecular studies are now providing potentially useful insights into the aging process which may help to achieve at least some aspects of this quest. This chapter will summarize the main findings of these studies with a focus on long-lived mutant mice and worms, and the longest living natural species including Galapagos giant tortoises, bowhead whales, Greenland sharks, quahog clams and the immortal jellyfish.

Keywords

Longevity Lifespan Model organisms Tortoise Whale Shark Quahog Jellyfish 

References

  1. 1.
    Whitney CR (1997) Jeanne Calment, World’s Elder, Dies at 122. The New York Times (5 August 1997). New York, NY, USA. Retrieved 16 January 2019. https://www.nytimes.com/1997/08/05/world/jeanne-calment-world-s-elder-dies-at-122.html
  2. 2.
    Allard M, Lèbre V, Calment J, Robine J-M, Calment J (1999) Jeanne Calment: from Van Gogh’s time to ours, 122 extraordinary years. Thorndike Press. ISBN: 0786217774Google Scholar
  3. 3.
    Tower J (2017) Sex-specific gene expression and life span regulation. Trends Endocrinol Metab 28(10):735–747CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
  5. 5.
    Bein MA, Unlucan D, Olowu G, Kalifa W (2017) Healthcare spending and health outcomes: evidence from selected East African countries. Afr Health Sci 17(1):247–254CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Bilas V, Franc S, Bosnjak M (2014) Determinant factors of life expectancy at birth in the European union countries. Coll Antropol 38(1):1–9PubMedGoogle Scholar
  7. 7.
  8. 8.
  9. 9.
  10. 10.
    Hill TR, Mendonça N, Granic A, Siervo M, Jagger C, Seal CJ et al (2016) What do we know about the nutritional status of the very old? Insights from three cohorts of advanced age from the UK and New Zealand. Proc Nutr Soc 75(3):420–430CrossRefPubMedGoogle Scholar
  11. 11.
    Evert J, Lawler E, Bogan H, Perls T (2003) Morbidity profiles of centenarians: survivors, delayers, and escapers. J Gerontol A Biol Sci Med Sci 58(3):232–237CrossRefPubMedGoogle Scholar
  12. 12.
    Andersen SL, Sebastiani P, Dworkis DA, Feldman L, Perls TT (2012) Health span approximates life span among many supercentenarians: compression of morbidity at the approximate limit of life span. J Gerontol A Biol Sci Med Sci 67(4):395–405CrossRefPubMedGoogle Scholar
  13. 13.
    Sebastiani P, Sun FX, Andersen SL, Lee JH, Wojczynski MK, Sanders JL et al (2013) Families enriched for exceptional longevity also have increased health-span: findings from the long life family study. Front Public Health 1:38.  https://doi.org/10.3389/fpubh.2013.00038CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Martin P, Kelly N, Kahana B, Kahana E, Willcox BJ, Willcox DC et al (2015) Defining successful aging: a tangible or elusive concept? Gerontologist 55(1):14–25CrossRefPubMedGoogle Scholar
  15. 15.
    Ha MK, Soo Cho J, Baik OR, Lee KH, Koo HS, Chung KY (2006) Caenorhabditis elegans as a screening tool for the endothelial cell-derived putative aging-related proteins detected by proteomic analysis. Proteomics 6(11):3339–3351CrossRefPubMedGoogle Scholar
  16. 16.
    Bell R, Hubbard A, Chettier R, Chen D, Miller JP, Kapahi P et al (2009) A human protein interaction network shows conservation of aging processes between human and invertebrate species. PLoS Genet 5(3):e1000414.  https://doi.org/10.1371/journal.pgen.1000414CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Austad SN (2010) Methusaleh’s zoo: how nature provides us with clues for extending human health span. J Comp Pathol 142 Suppl 1:S10–S21.  https://doi.org/10.1016/j.jcpa.2009.10.024CrossRefPubMedGoogle Scholar
  18. 18.
    Semeiks J, Grishin NV (2012) A method to find longevity-selected positions in the mammalian proteome. PLoS One 7(6):e38595.  https://doi.org/10.1371/journal.pone.0038595CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Bodnar A (2013) Proteomic profiles reveal age-related changes in coelomic fluid of sea urchin species with different life spans. Exp Gerontol 48(5):525–530CrossRefPubMedGoogle Scholar
  20. 20.
    De Waal EM, Liang H, Pierce A, Hamilton RT, Buffenstein R, Chaudhuri AR (2013) Elevated protein carbonylation and oxidative stress do not affect protein structure and function in the long-living naked-mole rat: a proteomic approach. Biochem Biophys Res Commun 434(4):815–819CrossRefPubMedGoogle Scholar
  21. 21.
    Seim I, Ma S, Zhou X, Gerashchenko MV, Lee SG, Suydam R et al (2014) The transcriptome of the bowhead whale Balaena mysticetus reveals adaptations of the longest-lived mammal. Aging (Albany NY) 6(10):879–899CrossRefGoogle Scholar
  22. 22.
    Keane M, Semeiks J, Webb AE, Li YI, Quesada V, Craig T et al (2015) Insights into the evolution of longevity from the bowhead whale genome. Cell Rep 10(1):112–122CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Triplett JC, Swomley A, Kirk J, Lewis K, Orr M, Rodriguez K et al (2015) Metabolic clues to salubrious longevity in the brain of the longest-lived rodent: the naked mole-rat. J Neurochem 134(3):538–550CrossRefPubMedGoogle Scholar
  24. 24.
    Ma S, Gladyshev VN (2017) Molecular signatures of longevity: insights from cross-species comparative studies. Semin Cell Dev Biol 70:190–203CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Willcox DC, Willcox BJ, Hsueh WC, Suzuki M (2006) Genetic determinants of exceptional human longevity: insights from the Okinawa Centenarian Study. Age 28(4):313–332CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Arnold J, Dai J, Nahapetyan L, Arte A, Johnson MA, Hausman D et al (2010) Predicting successful aging in a population-based sample of Georgia centenarians. Curr Gerontol Geriatr Res. pii:989315.  https://doi.org/10.1155/2010/989315CrossRefGoogle Scholar
  27. 27.
    Cho J, Martin P, Poon LW (2012) The older they are, the less successful they become? findings from the Georgia Centenarian Study. J Aging Res 2012:695854.  https://doi.org/10.1155/2012/695854CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Brooks-Wilson AR (2013) Genetics of healthy aging and longevity. Hum Genet 132(12):1323–1338CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Newman AB, Murabito JM (2013) The epidemiology of longevity and exceptional survival. Epidemiol Rev 35:181–197CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Flachsbart F, Caliebe A, Kleindorp R, Blanché H, von Eller-Eberstein H, Nikolaus S et al (2009) Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc Natl Acad Sci U S A 106(8):2700–2705CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Jacobsen R, Martinussen T, Christiansen L, Jeune B, Andersen-Ranberg K, Vaupel JW et al (2010) Increased effect of the ApoE gene on survival at advanced age in healthy and long-lived Danes: two nationwide cohort studies. Aging Cell 9(6):1004–1009CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Beekman M, Blanché H, Perola M, Hervonen A, Bezrukov V, Sikora E et al (2013) Genome-wide linkage analysis for human longevity: genetics of healthy aging study. Aging Cell 12(2):184–193CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Humphreys V, Martin RM, Ratcliffe B, Duthie S, Wood S, Gunnell D et al (2007) Age-related increases in DNA repair and antioxidant protection: a comparison of the Boyd Orr cohort of elderly subjects with a younger population sample. Age Ageing 36(5):521–526CrossRefPubMedGoogle Scholar
  34. 34.
    Chevanne M, Calia C, Zampieri M, Cecchinelli B, Caldini R, Monti D et al (2007) Oxidative DNA damage repair and parp 1 and parp 2 expression in Epstein-Barr virus-immortalized B lymphocyte cells from young subjects, old subjects, and centenarians. Rejuvenation Res 10(2):191–204CrossRefPubMedGoogle Scholar
  35. 35.
    Franzke B, Neubauer O, Wagner KH (2015) Super DNAging—new insights into DNA integrity, genome stability and telomeres in the oldest old. Mutat Res Rev Mutat Res 766:48–57CrossRefPubMedGoogle Scholar
  36. 36.
    Kim YJ, Kim HS, Seo YR (2018) Genomic approach to understand the association of DNA repair with longevity and healthy aging using genomic databases of oldest-old population. Oxidative Med Cell Longev 2018:2984730–2984712.  https://doi.org/10.1155/2018/2984730CrossRefGoogle Scholar
  37. 37.
    Levine ME, Crimmins EM (2016) A genetic network associated with stress resistance, longevity, and cancer in humans. J Gerontol A Biol Sci Med Sci 71(6):703–712CrossRefPubMedGoogle Scholar
  38. 38.
    Westermark B, Nister M, Heldin CH (1985) Growth factors and oncogenes in human malignant glioma. Neurol Clin 3(4):785–799CrossRefPubMedGoogle Scholar
  39. 39.
    Haliotis T, Trimble W, Chow S, Mills G, Girard P, Kuo JF et al (1988) The cell biology of ras-induced transformation: insights from studies utilizing an inducible hybrid oncogene system. Anticancer Res 8(5A):935–945PubMedGoogle Scholar
  40. 40.
    Hattori M, Minato N (2003) Rap1 GTPase: functions, regulation, and malignancy. J Biochem 134(4):479–484CrossRefPubMedGoogle Scholar
  41. 41.
    Nagano I, Murakami T, Manabe Y, Abe K (2002) Early decrease of survival factors and DNA repair enzyme in spinal motor neurons of presymptomatic transgenic mice that express a mutant SOD1 gene. Life Sci 72(4–5):541–548CrossRefPubMedGoogle Scholar
  42. 42.
    Gems D, Partridge L (2001) Insulin/IGF signalling and ageing: seeing the bigger picture. Curr Opin Genet Dev 11(3):287–292CrossRefPubMedGoogle Scholar
  43. 43.
    Richardson A, Liu F, Adamo ML, Van Remmen H, Nelson JF (2004) The role of insulin and insulin-like growth factor-I in mammalian ageing. Best Pract Res Clin Endocrinol Metab 18(3):393–406CrossRefPubMedGoogle Scholar
  44. 44.
    Mathew R, Pal Bhadra M, Bhadra U (2017) Insulin/insulin-like growth factor-1 signalling (IIS) based regulation of lifespan across species. Biogerontology 18(1):35–53CrossRefPubMedGoogle Scholar
  45. 45.
    Morris BJ, Donlon TA, He Q, Grove JS, Masaki KH, Elliott A et al (2014) Association analyses of insulin signaling pathway gene polymorphisms with healthy aging and longevity in Americans of Japanese ancestry. J Gerontol A Biol Sci Med Sci 69(3):270–273CrossRefPubMedGoogle Scholar
  46. 46.
    Kolovou V, Diakoumakou O, Papazafiropoulou AK, Katsiki N, Fragopoulou E, Vasiliadis I et al (2018) Biomarkers and gene polymorphisms in members of long- and short-lived families: a longevity study. Open Cardiovasc Med J 12:59–70CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Ryo M, Nakamura T, Kihara S, Kumada M, Shibazaki S, Takahashi M et al (2004) Adiponectin as a biomarker of the metabolic syndrome. Circ J 68(11):975–981CrossRefPubMedGoogle Scholar
  48. 48.
    Bik W, Baranowska B (2009) Adiponectin - a predictor of higher mortality in cardiovascular disease or a factor contributing to longer life? Neuro Endocrinol Lett 30(2):180–184PubMedGoogle Scholar
  49. 49.
    Cardoso AL, Fernandes A, Aguilar-Pimentel JA, de Angelis MH, Guedes JR, Brito MA et al (2018) Towards frailty biomarkers: candidates from genes and pathways regulated in aging and age-related diseases. Ageing Res Rev 47:214–277CrossRefPubMedGoogle Scholar
  50. 50.
    Barron E, Lara J, White M, Mathers JC (2015) Blood-borne biomarkers of mortality risk: systematic review of cohort studies. PLoS One 10(6):e0127550.  https://doi.org/10.1371/journal.pone.0127550CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Dellago H, Bobbili MR, Grillari J (2017) MicroRNA-17-5p: at the crossroads of cancer and aging - a mini-review. Gerontology 63(1):20–28CrossRefPubMedGoogle Scholar
  52. 52.
    Du WW, Yang W, Fang L, Xuan J, Li H, Khorshidi A et al (2014) miR-17 extends mouse lifespan by inhibiting senescence signaling mediated by MKP7. Cell Death Dis 5:e1355.  https://doi.org/10.1038/cddis.2014.305CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Arai Y, Hirose N, Yamamura K, Shimizu K, Takayama M, Ebihara Y et al (2001) Serum insulin-like growth factor-1 in centenarians: implications of IGF-1 as a rapid turnover protein. J Gerontol A Biol Sci Med Sci 56(2):M79–M82CrossRefPubMedGoogle Scholar
  54. 54.
    Pennington CALERIE Team, Heilbronn LK, de Jonge L, Frisard MI, JP DL, Larson-Meyer DE et al (2006) Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA 295(13):1539–1548CrossRefGoogle Scholar
  55. 55.
    Everitt AV, Le Couteur DG (2007) Life extension by calorie restriction in humans. Ann N Y Acad Sci 1114:428–433CrossRefPubMedGoogle Scholar
  56. 56.
    Lettieri-Barbato D, Giovannetti E, Aquilano K (2016) Effects of dietary restriction on adipose mass and biomarkers of healthy aging in human. Aging (Albany NY) 8(12):3341–3355CrossRefGoogle Scholar
  57. 57.
    Arai Y, Takayama M, Gondo Y, Inagaki H, Yamamura K, Nakazawa S et al (2008) Adipose endocrine function, insulin-like growth factor-1 axis, and exceptional survival beyond 100 years of age. J Gerontol A Biol Sci Med Sci 63(11):1209–1218CrossRefPubMedGoogle Scholar
  58. 58.
    Barbieri M, Paolisso G, Kimura M, Gardner JP, Boccardi V, Papa M et al (2009) Higher circulating levels of IGF-1 are associated with longer leukocyte telomere length in healthy subjects. Mech Ageing Dev 130(11–12):771–776CrossRefPubMedGoogle Scholar
  59. 59.
    Vaziri H, Benchimol S (1996) From telomere loss to p53 induction and activation of a DNA-damage pathway at senescence: the telomere loss/DNA damage model of cell aging. Exp Gerontol 31(1–2):295–301CrossRefPubMedGoogle Scholar
  60. 60.
    Djojosubroto MW, Choi YS, Lee HW, Rudolph KL (2003) Telomeres and telomerase in aging, regeneration and cancer. Mol Cells 15(2):164–175PubMedGoogle Scholar
  61. 61.
    Lenart P, Krejci L (2016) DNA, the central molecule of aging. Mutat Res 786:1–7CrossRefPubMedGoogle Scholar
  62. 62.
    Stenholm S, Metter EJ, Roth GS, Ingram DK, Mattison JA, Taub DD et al (2011) Relationship between plasma ghrelin, insulin, leptin, interleukin 6, adiponectin, testosterone and longevity in the Baltimore Longitudinal Study of Aging. Aging Clin Exp Res 23(2):153–158CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Gonzalez-Covarrubias V, Beekman M, Uh HW, Dane A, Troost J, Paliukhovich I et al (2013) Lipidomics of familial longevity. Aging Cell 12(3):426–434CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Montoliu I, Scherer M, Beguelin F, DaSilva L, Mari D, Salvioli S et al (2014) Serum profiling of healthy aging identifies phospho- and sphingolipid species as markers of human longevity. Aging (Albany NY) 6(1):9–25CrossRefGoogle Scholar
  65. 65.
    Bookheimer SY, Renner BA, Ekstrom A, Li Z, Henning SM, Brown JA et al (2013) Pomegranate juice augments memory and FMRI activity in middle-aged and older adults with mild memory complaints. Evid Based Complement Alternat Med 2013:946298.  https://doi.org/10.1155/2013/946298CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Semba RD, Ferrucci L, Bartali B, Urpí-Sarda M, Zamora-Ros R, Sun K et al (2014) Resveratrol levels and all-cause mortality in older community-dwelling adults. JAMA Intern Med 174(7):1077–1084CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Chen YF, Wu CY, Kao CH, Tsai TF (2010) Longevity and lifespan control in mammals: lessons from the mouse. Ageing Res Rev 9 Suppl 1:S28–S35CrossRefPubMedGoogle Scholar
  68. 68.
    Brown-Borg HM, Bartke A (2012) GH and IGF1: roles in energy metabolism of long-living GH mutant mice. J Gerontol A Biol Sci Med Sci 67(6):652–660CrossRefPubMedGoogle Scholar
  69. 69.
    Bartke A, Westbrook R, Sun L, Ratajczak M (2013) Links between growth hormone and aging. Endokrynol Pol 64(1):46–52PubMedPubMedCentralGoogle Scholar
  70. 70.
    Carter CS, Ramsey MM, Ingram RL, Cashion AB, Cefalu WT, Wang ZQ et al (2002) Models of growth hormone and IGF-1 deficiency: applications to studies of aging processes and life-span determination. J Gerontol A Biol Sci Med Sci 57(5):B177–B188CrossRefPubMedGoogle Scholar
  71. 71.
    Parr T (1999) Insulin exposure and unifying aging. Gerontology 45(3):121–135CrossRefPubMedGoogle Scholar
  72. 72.
    Katic M, Kahn CR (2005) The role of insulin and IGF-1 signaling in longevity. Cell Mol Life Sci 62(3):320–343CrossRefPubMedGoogle Scholar
  73. 73.
    Amrit FR, May RC (2010) Younger for longer: insulin signalling, immunity and ageing. Curr Aging Sci 3(3):166–176CrossRefPubMedGoogle Scholar
  74. 74.
    Selman C, Lingard S, Choudhury AI, Batterham RL, Claret M, Clements M et al (2008) Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J 22(3):807–188CrossRefPubMedGoogle Scholar
  75. 75.
    Taguchi A, Wartschow LM, White MF (2007) Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317:369–372CrossRefPubMedGoogle Scholar
  76. 76.
    Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI et al (2009) Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326:140–144CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H et al (2002) mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110(2):163–175CrossRefPubMedGoogle Scholar
  78. 78.
    Hayashi AA, Proud CG (2007) The rapid activation of protein synthesis by growth hormone requires signaling through mTOR. Am J Physiol Endocrinol Metab 292(6):E1647–E1655CrossRefPubMedGoogle Scholar
  79. 79.
    Cheng Z, Tseng Y, White MF (2010) Insulin signaling meets mitochondria in metabolism. Trends Endocrinol Metab 21(10):589–598CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11(3):298–300CrossRefGoogle Scholar
  81. 81.
    Jang YC, Van Remmen H (2009) The mitochondrial theory of aging: insight from transgenic and knockout mouse models. Exp Gerontol 44(4):256–260CrossRefPubMedGoogle Scholar
  82. 82.
    Yan LJ, Levine RL, Sohal RS (1997) Oxidative damage during aging targets mitochondrial aconitase. Proc Natl Acad Sci U S A 94(21):11168–11172CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Edrey YH, Salmon AB (2014) Revisiting an age-old question regarding oxidative stress. Free Radic Biol Med 71:368–378CrossRefPubMedGoogle Scholar
  84. 84.
    Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR et al (2003) Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics 16(1):29–37CrossRefPubMedGoogle Scholar
  85. 85.
    Richters L, Lange N, Renner R, Treiber N, Ghanem A, Tiemann K et al (2006) Exercise-induced adaptations of cardiac redox homeostasis and remodeling in heterozygous SOD2-knockout mice. J Appl Physiol (1985) 111(5):1431–1440CrossRefGoogle Scholar
  86. 86.
    Hoehn KL, Salmon AB, Hohnen-Behrens C, Turner N, Hoy AJ, Maghzal GJ et al (2009) Insulin resistance is a cellular antioxidant defense mechanism. Proc Natl Acad Sci U S A 106:17787–17792CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Yang H, Roberts LJ, Shi MJ, Zhou LC, Ballard BR, Richardson A et al (2004) Retardation of atherosclerosis by overexpression of catalase or both cu/Zn-superoxide dismutase and catalase in mice lacking apolipoprotein E. Circ Res 95(11):1075–1081CrossRefPubMedGoogle Scholar
  88. 88.
    Liu Y, Qi W, Richardson A, Van Remmen H, Ikeno Y, Salmon AB (2013) Oxidative damage associated with obesity is prevented by overexpression of CuZn- or Mn-superoxide dismutase. Biochem Biophys Res Commun 438(1):78–83CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Borg J, Chereul E (2008) Differential MRI patterns of brain atrophy in double or single transgenic mice for APP and/or SOD. J Neurosci Res 86(15):3275–3284CrossRefGoogle Scholar
  90. 90.
    Thiruchelvam M, Prokopenko O, Cory-Slechta DA, Richfield EK, Buckley B, Mirochnitchenko O (2005) Overexpression of superoxide dismutase or glutathione peroxidase protects against the paraquat + maneb-induced parkinson disease phenotype. J Biol Chem 280(23):22530–22539CrossRefPubMedGoogle Scholar
  91. 91.
    Shen X, Zheng S, Metreveli NS, Epstein PN (2006) Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes 55(3):798–805CrossRefPubMedGoogle Scholar
  92. 92.
    Dumont M, Wille E, Stack C, Calingasan NY, Beal MF, Lin MT (2009) Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer’s disease. FASEB J 23(8):2459–2466CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Heilbronn LK, Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr 78(3):361–369CrossRefGoogle Scholar
  94. 94.
    Smith JV, Heilbronn LK, Ravussin E (2004) Energy restriction and aging. Curr Opin Clin Nutr Metab Care 7(6):615–622CrossRefPubMedGoogle Scholar
  95. 95.
    Mahoney LB, Denny CA, Seyfried TN (2006) Caloric restriction in C57BL/6J mice mimics therapeutic fasting in humans. Lipids Health Dis 5:13.  https://doi.org/10.1186/1476-511X-5-13CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Silberberg R (1972) Articular aging and osteoarthrosis in dwarf mice. Pathol Microbiol (Basel) 38(6):417–430Google Scholar
  97. 97.
    Brown-Borg HM, Borg KE, Meliska CJ, Bartke A (1996) Dwarf mice and the aging process. Nature 384(6604):33.  https://doi.org/10.1038/384033a0CrossRefPubMedGoogle Scholar
  98. 98.
    Bartke A, Brown-Borg HM, Bode AM, Carlson J, Hunter WS, Bronson RT (1998) Does growth hormone prevent or accelerate aging? Exp Gerontol 33(7–8):675–687CrossRefPubMedGoogle Scholar
  99. 99.
    Hauck S, Bartke A (2000) Effects of growth hormone on hypothalamic Catalase and Cu/Zn superoxide dismutase. Free Rad Biol Med 28(6):970–978CrossRefPubMedGoogle Scholar
  100. 100.
    Hunter WS, Croson WB, Bartke A, Gentry MV, Meliska CJ (1999) Low body temperature in long-lived Ames dwarf mice at rest and during stress. Physiol Behav 67(3):433–437CrossRefPubMedGoogle Scholar
  101. 101.
    Borg KE, Brown-Borg HM, Bartke A (1995) Assessment of the primary adrenal cortical and pancreatic hormone basal levels in relation to plasma glucose and age in the unstressed Ames dwarf mouse. Proc Soc Exp Biol Med 210(2):126–133CrossRefPubMedGoogle Scholar
  102. 102.
    Holder AT, Wallis M, Biggs P, Preece MA (1980) Effects of growth hormone, prolactin and thyroxine on body weight, somatomedin-like activity and in-vivo sulphation of cartilage in hypopituitary dwarf mice. J Endocrinol 85(1):35–47CrossRefPubMedGoogle Scholar
  103. 103.
    Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A et al (2007) SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6(6):759–767CrossRefPubMedGoogle Scholar
  104. 104.
    Bordone L, Guarente L (2005) Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol 6(4):298–305CrossRefPubMedGoogle Scholar
  105. 105.
    Chen D, Steele AD, Lindquist S, Guarente L (2005) Increase in activity during calorie restriction requires Sirt1. Science 310(5754):1641CrossRefPubMedGoogle Scholar
  106. 106.
    Accili D, Arden KC (2004) FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117(4):421–426CrossRefPubMedGoogle Scholar
  107. 107.
    Albert PS, Riddle DL (1988) Mutants of Caenorhabditis elegans that form dauer-like larvae. Dev Biol 126(2):270–293CrossRefPubMedGoogle Scholar
  108. 108.
    Gottlieb S, Ruvkun G (1994) daf-2, daf-16 and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. Genetics 137(1):107–120PubMedPubMedCentralGoogle Scholar
  109. 109.
    Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366(6454):461–464CrossRefPubMedGoogle Scholar
  110. 110.
    Lakowski B, Hekimi S (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci U S A 95(22):13091–13096CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Panowski SH, Wolff S, Aguilaniu H, Durieux J, Dillin A (2007) PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans. Nature 447(7144):550–555CrossRefPubMedGoogle Scholar
  112. 112.
    Fuchs S, Bundy JG, Davies SK, Viney JM, Swire JS, Leroi AM (2010) A metabolic signature of long life in Caenorhabditis elegans. BMC Biol 8:14.  https://doi.org/10.1186/1741-7007-8-14CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Altintas O, Park S, Lee SJ (2016) The role of insulin/IGF-1 signaling in the longevity of model invertebrates, C. elegans and D. melanogaster. BMB Rep 49(2):81–92CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Ewald CY, Castillo-Quan JI, Blackwell TK (2018) Untangling longevity, dauer, and healthspan in Caenorhabditis elegans insulin/IGF-1-signalling. Gerontology 64(1):96–104CrossRefPubMedGoogle Scholar
  115. 115.
    Cuong VT, Chen W, Shi J, Zhang M, Yang H, Wang N et al (2019) The anti-oxidation and anti-aging effects of Ganoderma lucidum in Caenorhabditis elegans. Exp Gerontol 117:99–105.  https://doi.org/10.1016/j.exger.2018.11.016CrossRefPubMedGoogle Scholar
  116. 116.
    Meng F, Li J, Rao Y, Wang W, Fu Y (2018) Gengnianchun extends the lifespan of Caenorhabditis elegans via the insulin/IGF-1 signalling pathway. Oxidative Med Cell Longev 2018:4740739.  https://doi.org/10.1155/2018/4740739CrossRefGoogle Scholar
  117. 117.
    Kim SH, Kim BK, Park SK (2018) Selenocysteine mimics the effect of dietary restriction on lifespan via SKN-1 and retards age-associated pathophysiological changes in Caenorhabditis elegans. Mol Med Rep 18(6):5389–5398PubMedPubMedCentralGoogle Scholar
  118. 118.
    Wollenhaupt SG, Soares AT, Salgueiro WG, Noremberg S, Reis G, Viana C et al (2014) Seleno- and telluro-xylofuranosides attenuate Mn-induced toxicity in C. elegans via the DAF-16/FOXO pathway. Food Chem Toxicol 64:192–199CrossRefPubMedGoogle Scholar
  119. 119.
    Kim JS, Kim SH, Park SK (2017) Selenocysteine modulates resistance to environmental stress and confers anti-aging effects in C. elegans. Clinics (Sao Paulo) 72:491–498CrossRefGoogle Scholar
  120. 120.
    Zhang Y, Zhang W, Dong M (2018) The miR-58 microRNA family is regulated by insulin signaling and contributes to lifespan regulation in Caenorhabditis elegans. Sci China Life Sci 61(9):1060–1070CrossRefPubMedGoogle Scholar
  121. 121.
    Smith-Vikos T, Slack FJ (2012) MicroRNAs and their roles in aging. Cell Sci 125(Pt 1):7–17CrossRefGoogle Scholar
  122. 122.
    de Lencastre A, Pincus Z, Zhou K, Kato M, Lee SS, Slack FJ (2010) MicroRNAs both promote and antagonize longevity in C. elegans. Curr Biol 20(24):2159–2168CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Hubbard EJ (2011) Insulin and germline proliferation in Caenorhabditis elegans. Vitam Horm 87:61–77CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Klotz LO, Sánchez-Ramos C, Prieto-Arroyo I, Urbánek P, Steinbrenner H, Monsalve M (2015) Redox regulation of FoxO transcription factors. Redox Biol 6:51–72CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
  126. 126.
  127. 127.
    Loire E, Chiari Y, Bernard A, Cahais V, Romiguier J, Nabholz B et al (2013) Population genomics of the endangered giant Galápagos tortoise. Genome Biol 14(12):R136.  https://doi.org/10.1186/gb-2013-14-12-r136CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
  129. 129.
    Quesada V, Freitas-Rodríguez S, Miller J, Pérez-Silva JG, Jiang ZF, Tapia W et al (2019) Giant tortoise genomes provide insights into longevity and age-related disease. Nat Ecol Evol 3(1):87–95CrossRefPubMedGoogle Scholar
  130. 130.
    Frigerio NA, Sacher GA (1968) The determination of whale life-spans. ANL-7535. ANL Rep:116–118Google Scholar
  131. 131.
    Austad SN (2010) Methusaleh’s Zoo: how nature provides us with clues for extending human health span. J Comp Pathol 142(Suppl 1):S10–S21CrossRefPubMedGoogle Scholar
  132. 132.
    George JC, Bada J, Zeh J, Scott L, Brown SE, O’Hara T et al (1999) Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Can J Zool 77(4):571–580CrossRefGoogle Scholar
  133. 133.
    George JC, Bockstoce JR (2008) Two historical weapon fragments as an aid to estimating the longevity and movements of bowhead whales. Polar Biol 31:751–754CrossRefGoogle Scholar
  134. 134.
  135. 135.
    Philo LM, Shotts EB, George JC (1993) Morbidity and mortality. In: Burns JJ, Montague JJ, Cowles CJ (eds) The bowhead whale. Allen Press, Lawrence, KS, pp 275–312. ISBN-10: 0935868623Google Scholar
  136. 136.
    Tacutu R, Craig T, Budovsky A, Wuttke D, Lehmann G, Taranukha D et al (2013) Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res 41(Database issue):D1027–D1033.  https://doi.org/10.1093/nar/gks1155CrossRefPubMedGoogle Scholar
  137. 137.
    Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208(Pt 9):1717–1730CrossRefPubMedGoogle Scholar
  138. 138.
    Blagosklonny MV (2013) Big mice die young but large animals live longer. Aging (Albany NY) 5(4):227–233CrossRefGoogle Scholar
  139. 139.
    Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4(12):e1000304.  https://doi.org/10.1371/journal.pgen.1000304CrossRefPubMedPubMedCentralGoogle Scholar
  140. 140.
    Yim HS, Cho YS, Guang X, Kang SG, Jeong JY, Cha SS et al (2014) Minke whale genome and aquatic adaptation in cetaceans. Nat Genet 46(1):88–92CrossRefPubMedGoogle Scholar
  141. 141.
    Cornu M, Albert V, Hall MN (2013) mTOR in aging, metabolism, and cancer. Curr Opin Genet Dev 23(1):53–62CrossRefPubMedGoogle Scholar
  142. 142.
    Erez A, Nagamani SC, Shchelochkov OA, Premkumar MH, Campeau PM, Chen Y et al (2011) Requirement of argininosuccinate lyase for systemic nitric oxide production. Nat Med 17(12):1619–1626CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Yano K, Stevens JD, Compagno LJV (2007) Distribution, reproduction and feeding of the Greenland shark Somniosus (Somniosus) microcephalus, with notes on two other sleeper sharks, Somniosus (Somniosus) pacificus and Somniosus (Somniosus) antarcticus. J Fish Biol 70:374–390.  https://doi.org/10.1111/j.1095-8649.2007.01308.xCrossRefGoogle Scholar
  144. 144.
    MacNeil MA, McMeans BC, Hussey NE, Vecsei P, Svavarsson J, Kovacs KM et al (2012) Biology of the Greenland shark Somniosus microcephalus. J Fish Biol 80(5):991–1018CrossRefPubMedGoogle Scholar
  145. 145.
    Nielsen J, Hedeholm RB, Heinemeier J, Bushnell PG, Christiansen JS, Olsen J et al (2016) Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus). Science 353(6300):702–704CrossRefPubMedGoogle Scholar
  146. 146.
    Costantini D, Smith S, Killen SS, Nielsen J, Steffensen JF (2017) The Greenland shark: a new challenge for the oxidative stress theory of ageing? Comp Biochem Physiol A Mol Integr Physiol 203:227–232CrossRefPubMedGoogle Scholar
  147. 147.
  148. 148.
    Strahl J, Philipp EE, Brey T, Broeg K, Abele D (2007) Physiological aging in the Icelandic population of the ocean quahog Arctica islandica. Aquat Biol 1:77–84CrossRefGoogle Scholar
  149. 149.
    Ridgway ID, Richardson CA (2011) Arctica islandica: the longest lived non colonial animal known to science. Rev Fish Biol Fisheries 21:297.  https://doi.org/10.1007/s11160-010-9171-9CrossRefGoogle Scholar
  150. 150.
    Wanamaker AD, Heinemeier J, Scourse JD, Richardson CA (2008) Very long-lived molluscs confirm 17th century AD tephra-based radiocarbon reservoir ages for north Icelandic shelf waters. Radiocarbon 50:1–14CrossRefGoogle Scholar
  151. 151.
    Butler PG, Wanamaker ADJ, Scourse JD, Richardson CA, Reynolds DJ (2013) Variability of marine climate on the North Icelandic Shelf in a 1357-year proxy archive based on growth increments in the bivalve Arctica islandica. Palaeogeogr Palaeoclimatol Palaeoecol 373:141–151CrossRefGoogle Scholar
  152. 152.
    Abele D, Strahl J, Brey T, Philipp EE (2008) Imperceptible senescence: ageing in the ocean quahog Arctica islandica. Free Radic Res 42:474–480CrossRefPubMedGoogle Scholar
  153. 153.
    Ungvari Z, Ridgway I, Philipp EE, Campbell CM, McQuary P, Chow T et al (2011) Extreme longevity is associated with increased resistance to oxidative stress in Arctica islandica, the longest-living non-colonial animal. J Gerontol A Biol Sci Med Sci 66(7):741–750CrossRefPubMedGoogle Scholar
  154. 154.
    Munro D, Blier PU (2012) The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranes. Aging Cell 11(5):845–855CrossRefPubMedGoogle Scholar
  155. 155.
    Ungvari Z, Sosnowska D, Mason JB, Gruber H, Lee SW, Schwartz TS et al (2013) Resistance to genotoxic stresses in Arctica islandica, the longest living noncolonial animal: is extreme longevity associated with a multistress resistance phenotype? J Gerontol A Biol Sci Med Sci 68(5):521–529CrossRefPubMedGoogle Scholar
  156. 156.
    Sosnowska D, Richardson C, Sonntag WE, Csiszar A, Ungvari Z, Ridgway I (2014) A heart that beats for 500 years: age-related changes in cardiac proteasome activity, oxidative protein damage and expression of heat shock proteins, inflammatory factors, and mitochondrial complexes in Arctica islandica, the longest-living noncolonial animal. J Gerontol A Biol Sci Med Sci 69(12):1448–1461CrossRefPubMedGoogle Scholar
  157. 157.
  158. 158.
  159. 159.
    Carla’ EC, Pagliara P, Piraino S, Boero F, Dini L (2003) Morphological and ultrastructural analysis of Turritopsis nutricula during life cycle reversal. Tissue Cell 35(3):213–222CrossRefPubMedGoogle Scholar
  160. 160.
    Petralia RS, Mattson MP, Yao PJ (2014) Aging and longevity in the simplest animals and the quest for immortality. Ageing Res Rev 16:66–82CrossRefPubMedGoogle Scholar
  161. 161.
    Tanaka EM, Reddien PW (2011) The cellular basis for animal regeneration. Dev Cell 21(1):172–185CrossRefPubMedPubMedCentralGoogle Scholar
  162. 162.
    Devarapalli P, Kumavath RN, Barh D, Azevedo V (2014) The conserved mitochondrial gene distribution in relatives of Turritopsis nutricula, an immortal jellyfish. Bioinformation 10(9):586–591CrossRefPubMedPubMedCentralGoogle Scholar
  163. 163.
    Lisenkova AA, Grigorenko AP, Tyazhelova TV, Andreeva TV, Gusev FE, Manakhov AD et al (2017) Complete mitochondrial genome and evolutionary analysis of Turritopsis dohrnii, the “immortal” jellyfish with a reversible life-cycle. Mol Phylogenet Evol 107:232–238CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Paul C. Guest
    • 1
  1. 1.Laboratory of Neuroproteomics, Department of Biochemistry and Tissue Biology, Institute of BiologyUniversity of Campinas (UNICAMP)CampinasBrazil

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