Analyze Diet
Nature reviews. Cancer2018; 18(7); 433-441; doi: 10.1038/s41568-018-0004-9

Mechanisms of cancer resistance in long-lived mammals.

Abstract: Cancer researchers have traditionally used the mouse and the rat as staple model organisms. These animals are very short-lived, reproduce rapidly and are highly prone to cancer. They have been very useful for modelling some human cancer types and testing experimental treatments; however, these cancer-prone species offer little for understanding the mechanisms of cancer resistance. Recent technological advances have expanded bestiary research to non-standard model organisms that possess unique traits of very high value to humans, such as cancer resistance and longevity. In recent years, several discoveries have been made in non-standard mammalian species, providing new insights on the natural mechanisms of cancer resistance. These include mechanisms of cancer resistance in the naked mole rat, blind mole rat and elephant. In each of these species, evolution took a different path, leading to novel mechanisms. Many other long-lived mammalian species display cancer resistance, including whales, grey squirrels, microbats, cows and horses. Understanding the molecular mechanisms of cancer resistance in all these species is important and timely, as, ultimately, these mechanisms could be harnessed for the development of human cancer therapies.
Publication Date: 2018-04-07 PubMed ID: 29622806PubMed Central: PMC6015544DOI: 10.1038/s41568-018-0004-9Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research explores mechanisms of cancer resistance in long-lived mammals such as the naked mole rat, blind mole rat, elephant, whales, grey squirrels, microbats, cows, and horses. The findings can contribute to the development of human cancer therapies.

Overview of the Research

  • The study addresses an issue in cancer research — using animals like rats and mice, that are prone to cancer, as model organisms is useful for testing treatments, but not for gaining insights on how to resist or prevent cancer.
  • Recent technological advances have allowed researchers to study non-standard mammalian species that exhibit resistance to cancer, creating an opportunity to learn and borrow techniques from these species for humans.

Discoveries

  • Research on non-standard mammalian species such as the naked mole rat, blind mole rat, and elephants has opened up new findings on natural resistance to cancer.
  • Each mentioned species has evolved uniquely, developing their own methods of resisting cancer.
  • Other long-lived species like whales, grey squirrels, microbats, cows, and horses also exhibit cancer resistance, opening up multiple lines of inquiry for understanding these mechanisms.

Implications and Next Steps

  • Understanding these molecular mechanisms of cancer resistance in multiple species is essential.
  • Findings from these studies are not just of academic interest – they have real, practical applications, as they could be applied to develop therapies to treat cancer in humans.
  • While the study does not specifically state it, the next reasonable steps would be to carry out detailed studies on these mechanisms, followed by lab and, eventually, clinical trials to test how effective these natural methods of cancer resistance can be when applied to humans.

Cite This Article

APA
Seluanov A, Gladyshev VN, Vijg J, Gorbunova V. (2018). Mechanisms of cancer resistance in long-lived mammals. Nat Rev Cancer, 18(7), 433-441. https://doi.org/10.1038/s41568-018-0004-9

Publication

ISSN: 1474-1768
NlmUniqueID: 101124168
Country: England
Language: English
Volume: 18
Issue: 7
Pages: 433-441

Researcher Affiliations

Seluanov, Andrei
  • University of Rochester, Department of Biology, Rochester, NY, USA.
Gladyshev, Vadim N
  • Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Vijg, Jan
  • Department of Genetics, Albert Einstein College of Medicine, Bronx, NY, USA.
Gorbunova, Vera
  • University of Rochester, Department of Biology, Rochester, NY, USA. vera.gorbunova@rochester.edu.

MeSH Terms

  • Animals
  • Body Size
  • Cattle
  • Chiroptera
  • Disease Resistance / genetics
  • Disease Resistance / physiology
  • Elephants
  • Horses
  • Humans
  • Longevity
  • Mammals
  • Mice
  • Mole Rats
  • Mutation
  • Mutation Rate
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Rats
  • Sciuridae
  • Whales

Grant Funding

  • R01 AG031227 / NIA NIH HHS
  • P01 AG047200 / NIA NIH HHS
  • R37 GM065204 / NIGMS NIH HHS
  • R03 AG052365 / NIA NIH HHS
  • R01 AG027237 / NIA NIH HHS
  • DP1 AG047745 / NIA NIH HHS

Conflict of Interest Statement

. The authors declare no competing interests.

References

This article includes 93 references
  1. Center for Disease Control and Prevention. United States Cancer Statistics: 1999-2014 Incidence and Mortality Web-based Report
  2. Cleeland CS, Allen JD, Roberts SA, Brell JM, Giralt SA, Khakoo AY, Kirch RA, Kwitkowski VE, Liao Z, Skillings J. Reducing the toxicity of cancer therapy: recognizing needs, taking action.. Nat Rev Clin Oncol 2012 Jul 3;9(8):471-8.
    doi: 10.1038/nrclinonc.2012.99pubmed: 22751283google scholar: lookup
  3. Lipman R, Galecki A, Burke DT, Miller RA. Genetic loci that influence cause of death in a heterogeneous mouse stock.. J Gerontol A Biol Sci Med Sci 2004 Oct;59(10):977-83.
    pmc: PMC7110326pubmed: 15528770doi: 10.1093/gerona/59.10.b977google scholar: lookup
  4. Szymanska H, Lechowska-Piskorowska J, Krysiak E, Strzalkowska A, Unrug-Bielawska K, Grygalewicz B, Skurzak HM, Pienkowska-Grela B, Gajewska M. Neoplastic and nonneoplastic lesions in aging mice of unique and common inbred strains contribution to modeling of human neoplastic diseases.. Vet Pathol 2014 May;51(3):663-79.
    doi: 10.1177/0300985813501334pubmed: 24019352google scholar: lookup
  5. Ikeno Y, Hubbard GB, Lee S, Cortez LA, Lew CM, Webb CR, Berryman DE, List EO, Kopchick JJ, Bartke A. Reduced incidence and delayed occurrence of fatal neoplastic diseases in growth hormone receptor/binding protein knockout mice.. J Gerontol A Biol Sci Med Sci 2009 May;64(5):522-9.
    doi: 10.1093/gerona/glp017pmc: PMC2667132pubmed: 19228785google scholar: lookup
  6. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016.. CA Cancer J Clin 2016 Jan-Feb;66(1):7-30.
    doi: 10.3322/caac.21332pubmed: 26742998google scholar: lookup
  7. Rangarajan A, Hong SJ, Gifford A, Weinberg RA. Species- and cell type-specific requirements for cellular transformation.. Cancer Cell 2004 Aug;6(2):171-83.
    pubmed: 15324700doi: 10.1016/j.ccr.2004.07.009google scholar: lookup
  8. Gonzalez CA, Riboli E. Diet and cancer prevention: Contributions from the European Prospective Investigation into Cancer and Nutrition (EPIC) study.. Eur J Cancer 2010 Sep;46(14):2555-62.
    doi: 10.1016/j.ejca.2010.07.025pubmed: 20843485google scholar: lookup
  9. Key TJ, Schatzkin A, Willett WC, Allen NE, Spencer EA, Travis RC. Diet, nutrition and the prevention of cancer.. Public Health Nutr 2004 Feb;7(1A):187-200.
    pubmed: 14972060doi: 10.1079/phn2003588google scholar: lookup
  10. Prowse KR, Greider CW. Developmental and tissue-specific regulation of mouse telomerase and telomere length.. Proc Natl Acad Sci U S A 1995 May 23;92(11):4818-22.
    pmc: PMC41798pubmed: 7761406doi: 10.1073/pnas.92.11.4818google scholar: lookup
  11. de Lange T. How telomeres solve the end-protection problem.. Science 2009 Nov 13;326(5955):948-52.
    doi: 10.1126/science.1170633pmc: PMC2819049pubmed: 19965504google scholar: lookup
  12. Shippen-Lentz D, Blackburn EH. Functional evidence for an RNA template in telomerase.. Science 1990 Feb 2;247(4942):546-52.
    pubmed: 1689074doi: 10.1126/science.1689074google scholar: lookup
  13. Campisi J, Kim SH, Lim CS, Rubio M. Cellular senescence, cancer and aging: the telomere connection.. Exp Gerontol 2001 Nov;36(10):1619-37.
    pubmed: 11672984doi: 10.1016/s0531-5565(01)00160-7google scholar: lookup
  14. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW. Specific association of human telomerase activity with immortal cells and cancer.. Science 1994 Dec 23;266(5193):2011-5.
    pubmed: 7605428doi: 10.1126/science.7605428google scholar: lookup
  15. Seluanov A, Chen Z, Hine C, Sasahara TH, Ribeiro AA, Catania KC, Presgraves DC, Gorbunova V. Telomerase activity coevolves with body mass not lifespan.. Aging Cell 2007 Feb;6(1):45-52.
  16. Seluanov A, Hine C, Bozzella M, Hall A, Sasahara TH, Ribeiro AA, Catania KC, Presgraves DC, Gorbunova V. Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan.. Aging Cell 2008 Dec;7(6):813-23.
  17. Gomes NM, Ryder OA, Houck ML, Charter SJ, Walker W, Forsyth NR, Austad SN, Venditti C, Pagel M, Shay JW, Wright WE. Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination.. Aging Cell 2011 Oct;10(5):761-8.
  18. Tian X, Doerig K, Park R, Can Ran Qin A, Hwang C, Neary A, Gilbert M, Seluanov A, Gorbunova V. Evolution of telomere maintenance and tumour suppressor mechanisms across mammals.. Philos Trans R Soc Lond B Biol Sci 2018 Mar 5;373(1741).
    pmc: PMC5784063pubmed: 29335367doi: 10.1098/rstb.2016.0443google scholar: lookup
  19. Buffenstein R, Jarvis JU. The naked mole rat--a new record for the oldest living rodent.. Sci Aging Knowledge Environ 2002 May 29;2002(21):pe7.
    doi: 10.1126/sageke.2002.21.pe7pubmed: 14602989google scholar: lookup
  20. Buffenstein R. Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species.. J Comp Physiol B 2008 May;178(4):439-45.
    pubmed: 18180931doi: 10.1007/s00360-007-0237-5google scholar: lookup
  21. Liang S, Mele J, Wu Y, Buffenstein R, Hornsby PJ. Resistance to experimental tumorigenesis in cells of a long-lived mammal, the naked mole-rat (Heterocephalus glaber).. Aging Cell 2010 Aug;9(4):626-35.
  22. Delaney MA, Nagy L, Kinsel MJ, Treuting PM. Spontaneous histologic lesions of the adult naked mole rat (Heterocephalus glaber): a retrospective survey of lesions in a zoo population.. Vet Pathol 2013 Jul;50(4):607-21.
    doi: 10.1177/0300985812471543pubmed: 23355517google scholar: lookup
  23. Delaney MA, Ward JM, Walsh TF, Chinnadurai SK, Kerns K, Kinsel MJ, Treuting PM. Initial Case Reports of Cancer in Naked Mole-rats (Heterocephalus glaber).. Vet Pathol 2016 May;53(3):691-6.
    doi: 10.1177/0300985816630796pubmed: 26846576google scholar: lookup
  24. Seluanov A, Hine C, Azpurua J, Feigenson M, Bozzella M, Mao Z, Catania KC, Gorbunova V. Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat.. Proc Natl Acad Sci U S A 2009 Nov 17;106(46):19352-7.
    doi: 10.1073/pnas.0905252106pmc: PMC2780760pubmed: 19858485google scholar: lookup
  25. Hanahan D, Weinberg RA. The hallmarks of cancer.. Cell 2000 Jan 7;100(1):57-70.
    pubmed: 10647931doi: 10.1016/s0092-8674(00)81683-9google scholar: lookup
  26. Tian X, Azpurua J, Ke Z, Augereau A, Zhang ZD, Vijg J, Gladyshev VN, Gorbunova V, Seluanov A. INK4 locus of the tumor-resistant rodent, the naked mole rat, expresses a functional p15/p16 hybrid isoform.. Proc Natl Acad Sci U S A 2015 Jan 27;112(4):1053-8.
    doi: 10.1073/pnas.1418203112pmc: PMC4313802pubmed: 25550505google scholar: lookup
  27. Kim EB, Fang X, Fushan AA, Huang Z, Lobanov AV, Han L, Marino SM, Sun X, Turanov AA, Yang P, Yim SH, Zhao X, Kasaikina MV, Stoletzki N, Peng C, Polak P, Xiong Z, Kiezun A, Zhu Y, Chen Y, Kryukov GV, Zhang Q, Peshkin L, Yang L, Bronson RT, Buffenstein R, Wang B, Han C, Li Q, Chen L, Zhao W, Sunyaev SR, Park TJ, Zhang G, Wang J, Gladyshev VN. Genome sequencing reveals insights into physiology and longevity of the naked mole rat.. Nature 2011 Oct 12;479(7372):223-7.
    doi: 10.1038/nature10533pmc: PMC3319411pubmed: 21993625google scholar: lookup
  28. Sharpless NE. INK4a/ARF: a multifunctional tumor suppressor locus.. Mutat Res 2005 Aug 25;576(1-2):22-38.
    doi: 10.1016/j.mrfmmm.2004.08.021pubmed: 15878778google scholar: lookup
  29. Tian X, Azpurua J, Hine C, Vaidya A, Myakishev-Rempel M, Ablaeva J, Mao Z, Nevo E, Gorbunova V, Seluanov A. High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat.. Nature 2013 Jul 18;499(7458):346-9.
    doi: 10.1038/nature12234pmc: PMC3720720pubmed: 23783513google scholar: lookup
  30. Toole BP. Hyaluronan: from extracellular glue to pericellular cue.. Nat Rev Cancer 2004 Jul;4(7):528-39.
    pubmed: 15229478doi: 10.1038/nrc1391google scholar: lookup
  31. Miyawaki S, Kawamura Y, Oiwa Y, Shimizu A, Hachiya T, Bono H, Koya I, Okada Y, Kimura T, Tsuchiya Y, Suzuki S, Onishi N, Kuzumaki N, Matsuzaki Y, Narita M, Ikeda E, Okanoya K, Seino K, Saya H, Okano H, Miura K. Tumour resistance in induced pluripotent stem cells derived from naked mole-rats.. Nat Commun 2016 May 10;7:11471.
    doi: 10.1038/ncomms11471pmc: PMC4866046pubmed: 27161380google scholar: lookup
  32. Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ, Dzeja PP, Ikeda Y, Perez-Terzic C, Terzic A. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming.. Cell Metab 2011 Aug 3;14(2):264-71.
    doi: 10.1016/j.cmet.2011.06.011pmc: PMC3156138pubmed: 21803296google scholar: lookup
  33. Suvà ML, Riggi N, Bernstein BE. Epigenetic reprogramming in cancer.. Science 2013 Mar 29;339(6127):1567-70.
    doi: 10.1126/science.1230184pmc: PMC3821556pubmed: 23539597google scholar: lookup
  34. Ben-David U, Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells.. Nat Rev Cancer 2011 Apr;11(4):268-77.
    doi: 10.1038/nrc3034pubmed: 21390058google scholar: lookup
  35. Tan L, Ke Z, Tombline G, Macoretta N, Hayes K, Tian X, Lv R, Ablaeva J, Gilbert M, Bhanu NV, Yuan ZF, Garcia BA, Shi YG, Shi Y, Seluanov A, Gorbunova V. Naked Mole Rat Cells Have a Stable Epigenome that Resists iPSC Reprogramming.. Stem Cell Reports 2017 Nov 14;9(5):1721-1734.
  36. Lee SG, Mikhalchenko AE, Yim SH, Lobanov AV, Park JK, Choi KH, Bronson RT, Lee CK, Park TJ, Gladyshev VN. Naked Mole Rat Induced Pluripotent Stem Cells and Their Contribution to Interspecific Chimera.. Stem Cell Reports 2017 Nov 14;9(5):1706-1720.
  37. Park TJ, Reznick J, Peterson BL, Blass G, Omerbašić D, Bennett NC, Kuich PHJL, Zasada C, Browe BM, Hamann W, Applegate DT, Radke MH, Kosten T, Lutermann H, Gavaghan V, Eigenbrod O, Bégay V, Amoroso VG, Govind V, Minshall RD, Smith ESJ, Larson J, Gotthardt M, Kempa S, Lewin GR. Fructose-driven glycolysis supports anoxia resistance in the naked mole-rat.. Science 2017 Apr 21;356(6335):307-311.
    doi: 10.1126/science.aab3896pubmed: 28428423google scholar: lookup
  38. Liu H, Huang D, McArthur DL, Boros LG, Nissen N, Heaney AP. Fructose induces transketolase flux to promote pancreatic cancer growth.. Cancer Res 2010 Aug 1;70(15):6368-76.
    doi: 10.1158/0008-5472.CAN-09-4615pubmed: 20647326google scholar: lookup
  39. Azpurua J, Ke Z, Chen IX, Zhang Q, Ermolenko DN, Zhang ZD, Gorbunova V, Seluanov A. Naked mole-rat has increased translational fidelity compared with the mouse, as well as a unique 28S ribosomal RNA cleavage.. Proc Natl Acad Sci U S A 2013 Oct 22;110(43):17350-5.
    doi: 10.1073/pnas.1313473110pmc: PMC3808608pubmed: 24082110google scholar: lookup
  40. Lewis KN, Wason E, Edrey YH, Kristan DM, Nevo E, Buffenstein R. Regulation of Nrf2 signaling and longevity in naturally long-lived rodents.. Proc Natl Acad Sci U S A 2015 Mar 24;112(12):3722-7.
    doi: 10.1073/pnas.1417566112pmc: PMC4378420pubmed: 25775529google scholar: lookup
  41. Zhao S, Lin L, Kan G, Xu C, Tang Q, Yu C, Sun W, Cai L, Xu C, Cui S. High autophagy in the naked mole rat may play a significant role in maintaining good health.. Cell Physiol Biochem 2014;33(2):321-32.
    doi: 10.1159/000356672pubmed: 24525846google scholar: lookup
  42. Rodriguez KA, Osmulski PA, Pierce A, Weintraub ST, Gaczynska M, Buffenstein R. A cytosolic protein factor from the naked mole-rat activates proteasomes of other species and protects these from inhibition.. Biochim Biophys Acta 2014 Nov;1842(11):2060-72.
  43. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification.. Science 2011 Oct 28;334(6055):521-4.
    doi: 10.1126/science.1211028pubmed: 21940861google scholar: lookup
  44. Edrey YH, Casper D, Huchon D, Mele J, Gelfond JA, Kristan DM, Nevo E, Buffenstein R. Sustained high levels of neuregulin-1 in the longest-lived rodents; a key determinant of rodent longevity.. Aging Cell 2012 Apr;11(2):213-22.
  45. Gorbunova V, Hine C, Tian X, Ablaeva J, Gudkov AV, Nevo E, Seluanov A. Cancer resistance in the blind mole rat is mediated by concerted necrotic cell death mechanism.. Proc Natl Acad Sci U S A 2012 Nov 20;109(47):19392-6.
    doi: 10.1073/pnas.1217211109pmc: PMC3511137pubmed: 23129611google scholar: lookup
  46. Shams I, Avivi A, Nevo E. Hypoxic stress tolerance of the blind subterranean mole rat: expression of erythropoietin and hypoxia-inducible factor 1 alpha.. Proc Natl Acad Sci U S A 2004 Jun 29;101(26):9698-703.
    doi: 10.1073/pnas.0403540101pmc: PMC470738pubmed: 15210955google scholar: lookup
  47. Ashur-Fabian O, Avivi A, Trakhtenbrot L, Adamsky K, Cohen M, Kajakaro G, Joel A, Amariglio N, Nevo E, Rechavi G. Evolution of p53 in hypoxia-stressed Spalax mimics human tumor mutation.. Proc Natl Acad Sci U S A 2004 Aug 17;101(33):12236-41.
    doi: 10.1073/pnas.0404998101pmc: PMC514462pubmed: 15302922google scholar: lookup
  48. Manov I, Hirsh M, Iancu TC, Malik A, Sotnichenko N, Band M, Avivi A, Shams I. Pronounced cancer resistance in a subterranean rodent, the blind mole-rat, Spalax: in vivo and in vitro evidence.. BMC Biol 2013 Aug 9;11:91.
    doi: 10.1186/1741-7007-11-91pmc: PMC3750378pubmed: 23937926google scholar: lookup
  49. Fang X, Nevo E, Han L, Levanon EY, Zhao J, Avivi A, Larkin D, Jiang X, Feranchuk S, Zhu Y, Fishman A, Feng Y, Sher N, Xiong Z, Hankeln T, Huang Z, Gorbunova V, Zhang L, Zhao W, Wildman DE, Xiong Y, Gudkov A, Zheng Q, Rechavi G, Liu S, Bazak L, Chen J, Knisbacher BA, Lu Y, Shams I, Gajda K, Farré M, Kim J, Lewin HA, Ma J, Band M, Bicker A, Kranz A, Mattheus T, Schmidt H, Seluanov A, Azpurua J, McGowen MR, Ben Jacob E, Li K, Peng S, Zhu X, Liao X, Li S, Krogh A, Zhou X, Brodsky L, Wang J. Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax.. Nat Commun 2014 Jun 3;5:3966.
    doi: 10.1038/ncomms4966pubmed: 24892994google scholar: lookup
  50. Nasser NJ, Avivi A, Shafat I, Edovitsky E, Zcharia E, Ilan N, Vlodavsky I, Nevo E. Alternatively spliced Spalax heparanase inhibits extracellular matrix degradation, tumor growth, and metastasis.. Proc Natl Acad Sci U S A 2009 Feb 17;106(7):2253-8.
    pmc: PMC2650141pubmed: 19164514doi: 10.1073/pnas.0812846106google scholar: lookup
  51. Siegal-Willott J, Heard D, Sliess N, Naydan D, Roberts J. Microchip-associated leiomyosarcoma in an Egyptian fruit bat (Rousettus aegyptiacus).. J Zoo Wildl Med 2007 Jun;38(2):352-6.
  52. McLelland DJ, Dutton CJ, Barker IK. Sarcomatoid carcinoma in the lung of an Egyptian fruit bat (Rousettus aegyptiacus).. J Vet Diagn Invest 2009 Jan;21(1):160-3.
    doi: 10.1177/104063870902100129pubmed: 19139522google scholar: lookup
  53. Bradford C, Jennings R, Ramos-Vara J. Gastrointestinal leiomyosarcoma in an Egyptian fruit bat (Rousettus aegyptiacus).. J Vet Diagn Invest 2010 May;22(3):462-5.
    doi: 10.1177/104063871002200324pubmed: 20453229google scholar: lookup
  54. Crameri G, Todd S, Grimley S, McEachern JA, Marsh GA, Smith C, Tachedjian M, De Jong C, Virtue ER, Yu M, Bulach D, Liu JP, Michalski WP, Middleton D, Field HE, Wang LF. Establishment, immortalisation and characterisation of pteropid bat cell lines.. PLoS One 2009 Dec 11;4(12):e8266.
  55. Wang LF, Walker PJ, Poon LL. Mass extinctions, biodiversity and mitochondrial function: are bats 'special' as reservoirs for emerging viruses?. Curr Opin Virol 2011 Dec;1(6):649-57.
  56. Brook CE, Dobson AP. Bats as 'special' reservoirs for emerging zoonotic pathogens.. Trends Microbiol 2015 Mar;23(3):172-80.
    doi: 10.1016/j.tim.2014.12.004pmc: PMC7126622pubmed: 25572882google scholar: lookup
  57. Huang Z, Jebb D, Teeling EC. Blood miRNomes and transcriptomes reveal novel longevity mechanisms in the long-lived bat, Myotis myotis.. BMC Genomics 2016 Nov 10;17(1):906.
    doi: 10.1186/s12864-016-3227-8pmc: PMC5103334pubmed: 27832764google scholar: lookup
  58. Seim I, Fang X, Xiong Z, Lobanov AV, Huang Z, Ma S, Feng Y, Turanov AA, Zhu Y, Lenz TL, Gerashchenko MV, Fan D, Hee Yim S, Yao X, Jordan D, Xiong Y, Ma Y, Lyapunov AN, Chen G, Kulakova OI, Sun Y, Lee SG, Bronson RT, Moskalev AA, Sunyaev SR, Zhang G, Krogh A, Wang J, Gladyshev VN. Genome analysis reveals insights into physiology and longevity of the Brandt's bat Myotis brandtii.. Nat Commun 2013;4:2212.
    doi: 10.1038/ncomms3212pmc: PMC3753542pubmed: 23962925google scholar: lookup
  59. Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA, Fang X, Wynne JW, Xiong Z, Baker ML, Zhao W, Tachedjian M, Zhu Y, Zhou P, Jiang X, Ng J, Yang L, Wu L, Xiao J, Feng Y, Chen Y, Sun X, Zhang Y, Marsh GA, Crameri G, Broder CC, Frey KG, Wang LF, Wang J. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity.. Science 2013 Jan 25;339(6118):456-60.
    doi: 10.1126/science.1230835pubmed: 23258410google scholar: lookup
  60. David A, Hwa V, Metherell LA, Netchine I, Camacho-Hübner C, Clark AJ, Rosenfeld RG, Savage MO. Evidence for a continuum of genetic, phenotypic, and biochemical abnormalities in children with growth hormone insensitivity.. Endocr Rev 2011 Aug;32(4):472-97.
    doi: 10.1210/er.2010-0023pubmed: 21525302google scholar: lookup
  61. Guevara-Aguirre J, Balasubramanian P, Guevara-Aguirre M, Wei M, Madia F, Cheng CW, Hwang D, Martin-Montalvo A, Saavedra J, Ingles S, de Cabo R, Cohen P, Longo VD. Growth hormone receptor deficiency is associated with a major reduction in pro-aging signaling, cancer, and diabetes in humans.. Sci Transl Med 2011 Feb 16;3(70):70ra13.
  62. Peto R. In: Origins of Human Cancer. Hiatt HH, Watson JD, Winsten JA, editors. Cold Spring Harbor Publications; 1977.
  63. NORDLING CO. A new theory on cancer-inducing mechanism.. Br J Cancer 1953 Mar;7(1):68-72.
    pmc: PMC2007872pubmed: 13051507doi: 10.1038/bjc.1953.8google scholar: lookup
  64. Nunney L. Lineage selection and the evolution of multistage carcinogenesis.. Proc Biol Sci 1999 Mar 7;266(1418):493-8.
    doi: 10.1098/rspb.1999.0664pmc: PMC1689794pubmed: 10189713google scholar: lookup
  65. Tollis M, Boddy AM, Maley CC. Peto's Paradox: how has evolution solved the problem of cancer prevention?. BMC Biol 2017 Jul 13;15(1):60.
    doi: 10.1186/s12915-017-0401-7pmc: PMC5513346pubmed: 28705195google scholar: lookup
  66. Sulak M, Fong L, Mika K, Chigurupati S, Yon L, Mongan NP, Emes RD, Lynch VJ. TP53 copy number expansion is associated with the evolution of increased body size and an enhanced DNA damage response in elephants.. Elife 2016 Sep 19;5.
    doi: 10.7554/eLife.11994pmc: PMC5061548pubmed: 27642012google scholar: lookup
  67. Abegglen LM, Caulin AF, Chan A, Lee K, Robinson R, Campbell MS, Kiso WK, Schmitt DL, Waddell PJ, Bhaskara S, Jensen ST, Maley CC, Schiffman JD. Potential Mechanisms for Cancer Resistance in Elephants and Comparative Cellular Response to DNA Damage in Humans.. JAMA 2015 Nov 3;314(17):1850-60.
    doi: 10.1001/jama.2015.13134pmc: PMC4858328pubmed: 26447779google scholar: lookup
  68. Tyner SD, Venkatachalam S, Choi J, Jones S, Ghebranious N, Igelmann H, Lu X, Soron G, Cooper B, Brayton C, Park SH, Thompson T, Karsenty G, Bradley A, Donehower LA. p53 mutant mice that display early ageing-associated phenotypes.. Nature 2002 Jan 3;415(6867):45-53.
    pubmed: 11780111doi: 10.1038/415045agoogle scholar: lookup
  69. Maier B, Gluba W, Bernier B, Turner T, Mohammad K, Guise T, Sutherland A, Thorner M, Scrable H. Modulation of mammalian life span by the short isoform of p53.. Genes Dev 2004 Feb 1;18(3):306-19.
    pmc: PMC338283pubmed: 14871929doi: 10.1101/gad.1162404google scholar: lookup
  70. García-Cao I, García-Cao M, Martín-Caballero J, Criado LM, Klatt P, Flores JM, Weill JC, Blasco MA, Serrano M. "Super p53" mice exhibit enhanced DNA damage response, are tumor resistant and age normally.. EMBO J 2002 Nov 15;21(22):6225-35.
    pmc: PMC137187pubmed: 12426394doi: 10.1093/emboj/cdf595google scholar: lookup
  71. Matheu A, Maraver A, Klatt P, Flores I, Garcia-Cao I, Borras C, Flores JM, Viña J, Blasco MA, Serrano M. Delayed ageing through damage protection by the Arf/p53 pathway.. Nature 2007 Jul 19;448(7151):375-9.
    doi: 10.1038/nature05949pubmed: 17637672google scholar: lookup
  72. Yim HS, Cho YS, Guang X, Kang SG, Jeong JY, Cha SS, Oh HM, Lee JH, Yang EC, Kwon KK, Kim YJ, Kim TW, Kim W, Jeon JH, Kim SJ, Choi DH, Jho S, Kim HM, Ko J, Kim H, Shin YA, Jung HJ, Zheng Y, Wang Z, Chen Y, Chen M, Jiang A, Li E, Zhang S, Hou H, Kim TH, Yu L, Liu S, Ahn K, Cooper J, Park SG, Hong CP, Jin W, Kim HS, Park C, Lee K, Chun S, Morin PA, O'Brien SJ, Lee H, Kimura J, Moon DY, Manica A, Edwards J, Kim BC, Kim S, Wang J, Bhak J, Lee HS, Lee JH. Minke whale genome and aquatic adaptation in cetaceans.. Nat Genet 2014 Jan;46(1):88-92.
    doi: 10.1038/ng.2835pmc: PMC4079537pubmed: 24270359google scholar: lookup
  73. Foote AD, Liu Y, Thomas GW, Vinař T, Alföldi J, Deng J, Dugan S, van Elk CE, Hunter ME, Joshi V, Khan Z, Kovar C, Lee SL, Lindblad-Toh K, Mancia A, Nielsen R, Qin X, Qu J, Raney BJ, Vijay N, Wolf JB, Hahn MW, Muzny DM, Worley KC, Gilbert MT, Gibbs RA. Convergent evolution of the genomes of marine mammals.. Nat Genet 2015 Mar;47(3):272-5.
    doi: 10.1038/ng.3198pmc: PMC4644735pubmed: 25621460google scholar: lookup
  74. Foote AD, Vijay N, Ávila-Arcos MC, Baird RW, Durban JW, Fumagalli M, Gibbs RA, Hanson MB, Korneliussen TS, Martin MD, Robertson KM, Sousa VC, Vieira FG, Vinař T, Wade P, Worley KC, Excoffier L, Morin PA, Gilbert MTP, Wolf JBW. Genome-culture coevolution promotes rapid divergence of killer whale ecotypes.. Nat Commun 2016 May 31;7:11693.
    doi: 10.1038/ncomms11693pmc: PMC4895049pubmed: 27243207google scholar: lookup
  75. Keane M, Semeiks J, Webb AE, Li YI, Quesada V, Craig T, Madsen LB, van Dam S, Brawand D, Marques PI, Michalak P, Kang L, Bhak J, Yim HS, Grishin NV, Nielsen NH, Heide-Jørgensen MP, Oziolor EM, Matson CW, Church GM, Stuart GW, Patton JC, George JC, Suydam R, Larsen K, López-Otín C, O'Connell MJ, Bickham JW, Thomsen B, de Magalhães JP. Insights into the evolution of longevity from the bowhead whale genome.. Cell Rep 2015 Jan 6;10(1):112-22.
  76. George JC. Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Can J Zool 1999;77(4):571–580.
  77. Tacutu R, Craig T, Budovsky A, Wuttke D, Lehmann G, Taranukha D, Costa J, Fraifeld VE, de Magalhães JP. Human Ageing Genomic Resources: integrated databases and tools for the biology and genetics of ageing.. Nucleic Acids Res 2013 Jan;41(Database issue):D1027-33.
    doi: 10.1093/nar/gks1155pmc: PMC3531213pubmed: 23193293google scholar: lookup
  78. Seim I, Ma S, Zhou X, Gerashchenko MV, Lee SG, Suydam R, George JC, Bickham JW, Gladyshev VN. The transcriptome of the bowhead whale Balaena mysticetus reveals adaptations of the longest-lived mammal.. Aging (Albany NY) 2014 Oct;6(10):879-99.
    doi: 10.18632/aging.100699pmc: PMC4247388pubmed: 25411232google scholar: lookup
  79. FAILLA G. The aging process and cancerogenesis.. Ann N Y Acad Sci 1958 Sep 30;71(6):1124-40.
  80. Baer CF, Miyamoto MM, Denver DR. Mutation rate variation in multicellular eukaryotes: causes and consequences.. Nat Rev Genet 2007 Aug;8(8):619-31.
    doi: 10.1038/nrg2158pubmed: 17637734google scholar: lookup
  81. Lynch M. Evolution of the mutation rate.. Trends Genet 2010 Aug;26(8):345-52.
    doi: 10.1016/j.tig.2010.05.003pmc: PMC2910838pubmed: 20594608google scholar: lookup
  82. Britten RJ. Rates of DNA sequence evolution differ between taxonomic groups.. Science 1986 Mar 21;231(4744):1393-8.
    pubmed: 3082006doi: 10.1126/science.3082006google scholar: lookup
  83. Thomas GW, Hahn MW. The human mutation rate is increasing, even as it slows.. Mol Biol Evol 2014 Feb;31(2):253-7.
    doi: 10.1093/molbev/mst218pubmed: 24202611google scholar: lookup
  84. MacRae SL, Zhang Q, Lemetre C, Seim I, Calder RB, Hoeijmakers J, Suh Y, Gladyshev VN, Seluanov A, Gorbunova V, Vijg J, Zhang ZD. Comparative analysis of genome maintenance genes in naked mole rat, mouse, and human.. Aging Cell 2015 Apr;14(2):288-91.
    doi: 10.1111/acel.12314pmc: PMC4364841pubmed: 25645816google scholar: lookup
  85. Milholland B, Dong X, Zhang L, Hao X, Suh Y, Vijg J. Differences between germline and somatic mutation rates in humans and mice.. Nat Commun 2017 May 9;8:15183.
    doi: 10.1038/ncomms15183pmc: PMC5436103pubmed: 28485371google scholar: lookup
  86. Milholland B, Dong X, Zhang L, Hao X, Suh Y, Vijg J. Differences between germline and somatic mutation rates in humans and mice.. Nat Commun 2017 May 9;8:15183.
    pmc: PMC5436103pubmed: 28485371doi: 10.1038/ncomms15183google scholar: lookup
  87. Tollis M, Schiffman JD, Boddy AM. Evolution of cancer suppression as revealed by mammalian comparative genomics.. Curr Opin Genet Dev 2017 Feb;42:40-47.
    doi: 10.1016/j.gde.2016.12.004pubmed: 28161621google scholar: lookup
  88. Croco E, Marchionni S, Bocchini M, Angeloni C, Stamato T, Stefanelli C, Hrelia S, Sell C, Lorenzini A. DNA Damage Detection by 53BP1: Relationship to Species Longevity.. J Gerontol A Biol Sci Med Sci 2017 Jun 1;72(6):763-770.
    doi: 10.1093/gerona/glw170pubmed: 27573809google scholar: lookup
  89. MacRae SL, Croken MM, Calder RB, Aliper A, Milholland B, White RR, Zhavoronkov A, Gladyshev VN, Seluanov A, Gorbunova V, Zhang ZD, Vijg J. DNA repair in species with extreme lifespan differences.. Aging (Albany NY) 2015 Dec;7(12):1171-84.
    doi: 10.18632/aging.100866pmc: PMC4712340pubmed: 26729707google scholar: lookup
  90. Ma S, Upneja A, Galecki A, Tsai YM, Burant CF, Raskind S, Zhang Q, Zhang ZD, Seluanov A, Gorbunova V, Clish CB, Miller RA, Gladyshev VN. Cell culture-based profiling across mammals reveals DNA repair and metabolism as determinants of species longevity.. Elife 2016 Nov 22;5.
    doi: 10.7554/eLife.19130pmc: PMC5148604pubmed: 27874830google scholar: lookup
  91. de Magalhães JP, Kean M. Endless paces of degeneration--applying comparative genomics to study evolution's moulding of longevity.. EMBO Rep 2013 Aug;14(8):661-2.
    doi: 10.1038/embor.2013.96pmc: PMC3736137pubmed: 23846314google scholar: lookup
  92. Dial KP. Wing-assisted incline running and the evolution of flight.. Science 2003 Jan 17;299(5605):402-4.
    doi: 10.1126/science.1078237pubmed: 12532020google scholar: lookup
  93. Munson L, Moresco A. Comparative Pathobiology of od Mammary Gland Cancers in Wild and Domestic Animals. IOS Press; 2007. pp. 7–21.

Citations

This article has been cited 157 times.