Getting to the heart of the matter: Age-related changes in diastolic heart function in the longest-lived rodent, the naked mole rat

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 67 A, Issue 4, 2012, Pages 384-394

  Grimes, Kelly M ^a   Lindsey, Merry L ^a,b   Gelfond, Jonathan A L ^a   Buffenstein, Rochelle ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b University of Texas Health Science Center   (United States)

Author keywords

Cardiac imaging; Diastolic dysfunction; Hypogonadic; Left ventricular function; Naked mole rat

Indexed keywords

HETEROCEPHALUS GLABER; RATTUS; RODENTIA;

ESTROGEN;

ANIMAL; ARTICLE; BLOOD; DIASTOLE; DOPPLER FLOWMETRY; ECHOCARDIOGRAPHY; FEMALE; HEART; HEART LEFT VENTRICLE FUNCTION; LONGEVITY; MALE; MOLE RAT; PHYSIOLOGY; RAT; SEX DIFFERENCE;

ANIMALS; DIASTOLE; ECHOCARDIOGRAPHY; ESTROGENS; FEMALE; HEART; LONGEVITY; MALE; MOLE RATS; RATS; SEX FACTORS; ULTRASONOGRAPHY, DOPPLER; VENTRICULAR FUNCTION, LEFT;

EID: 84859072242     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glr222     Document Type: Article

References (88)

1. Barzilai N, Shuldiner AR. Searching for human longevity genes: the future history of gerontology in the post-genomic era. J Gerontol A Med Sci. 2001;56(2):M83-M87. (Pubitemid 32121422)
2. Weigl R. Longevity of Mammals in Captivity; From the Living Collections of the World. Stuttgart, Germany: Stuttgart Kleine Senckenberg-Reihe; 2005.
3. Jarvis J, Bennett N. Ecology and behavior of the Family Bathyergidae. In: Sherman P, Jarvis J, Alexander R, eds. The Biology of the Naked Mole-Rat. Princeton, NJ: Princeton University Press; 1991:66-96.
4. Sherman PW, Jarvis JUM. Extraordinary life spans of naked mole-rats (Heterocephalus glaber). J Zool. 2002;258:307-311. (Pubitemid 35374565)
5. Buffenstein R. The naked mole-rat? A new long-living model for human aging research. J Gerontol A Biol Sci Med Sci. 2005;60(11):1369-1377. (Pubitemid 41798442)
6. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA. Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev. 2007;87(4):1175-1213. (Pubitemid 350033823)
7. Edrey YH, Park TJ, Kang H, Biney A, Buffenstein R. Endocrine function and neurobiology of the longest-living rodent, the naked mole-rat. Exp Gerontol. 2011;46(2-3):116-123.
8. Bennett NC, Faulkes CG. African Mole-Rats: Ecology and Eusociality. Cambridge, UK: Cambridge University Press; 2000.
9. Blanga-Kanfi S, Miranda H, Penn O, Pupko T, DeBry RW, Huchon D. Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol Biol. 2009;9:71.
10. Deuve JL, Bennett NC, Britton-Davidian J, Robinson TJ. Chromosomal phylogeny and evolution of the African mole-rats (Bathyergidae). Chromosome Res. 2008;16(1):57-74. (Pubitemid 351297687)
11. Michener CD. Comparative social behavior of bees. Annu Rev Entomol. 1969;14:299.
12. Jarvis JU. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science. 1981;212(4494):571-573. (Pubitemid 11068562)
13. Holmes MM, Goldman BD, Goldman SL, Seney ML, Forger NG. Neuroendocrinology and sexual differentiation in eusocial mammals. Front Neuroendocrinol. 2009;30(4):519-533.
14. Pinto M, Jepsen KJ, Terranova CJ, Buffenstein R. Lack of sexual dimorphism in femora of the eusocial and hypogonadic naked mole-rat: a novel animal model for the study of delayed puberty on the skeletal system. Bone. 2010;46(1):112-120.
15. Faulkes CG, Abbott DH, Jarvis JU. Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber. J Reprod Fertil. 1990;88(2):559-568. (Pubitemid 20109934)
16. Clarke FM, Faulkes CG. Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. Proc Biol Sci. 1998;265(1404):1391-1399. (Pubitemid 28395890)
17. Westlin LM, Bennett NC, Jarvis JUM. Relaxation of reproductive suppression in non-breeding female naked mole-rats, Heterocephalus glaber. J Zool. 1994;234:177-188. (Pubitemid 2146844)
18. Buffenstein R. Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Comp Physiol B. 2008;178(4):439-445. (Pubitemid 351550303)
19. Buffenstein R, Pinto M. Endocrine function in naturally long-living small mammals. Mol Cell Endocrinol. 2009;299(1):101-111.
20. Honeycutt R, Nelson K, Schlitter D, Sherman P. Genetic variation within and among populations of the naked mole-rat: evidence from mitochondrial and nuclear genomes. In: Sherman P, Jarvis J, Alexander R, eds. The Biology of the Naked Mole-Rat. Princeton, NJ: Princeton University Press; 1991:195-208.
21. Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF. DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proc Natl Acad Sci USA. 1990;87(7):2496-2500.
22. Bennett NC, Jarvis JUM, Davies KC. Daily and seasonal temperatures in the burrows of African rodent moles. S Afr J Zool. 1988;23(3):189-195.
23. Larson J, Park TJ. Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport. 2009;20(18):1634-1637.
24. Carnes BA, Olshansky SJ. A biologically motivated partitioning of mortality. Exp Gerontol. 1997;32(6):615-631. (Pubitemid 27518244)
25. Brett R. The population structure of naked mole-rat colonies. In: Sherman P, Jarvis J, Alexander R, eds. The Biology of the Naked Mole-Rat. Princeton, NJ: Princeton University Press; 1991:97-136.
26. Lacey E, Sherman P. Social organization of naked mole-rat colonies: evidence for division of labor. In: Sherman P, Jarvis J, Alexander R, eds. The Biology of the Naked Mole-Rat. Princeton, NJ: Princeton University Press; 1991:275-336.
27. Edrey YH, Hanes M, Pinto M, Mele J, Buffenstein R. Successful aging and sustained good health in the naked mole rat: a long-lived mammalian model for biogerontology and biomedical research. ILAR J. 2011;52(1):41-53.
28. O'Connor TP, Lee A, Jarvis JU, Buffenstein R. Prolonged longevity in naked mole-rats: age-related changes in metabolism, body composition and gastrointestinal function. Comp Biochem Physiol A Mol Integr Physiol. 2002;133(3):835-842. (Pubitemid 35351476)
29. Fries JF. Frailty, heart disease, and stroke: the compression of morbidity paradigm. Am J Prev Med. 2005;29(5 suppl 1):164-168. (Pubitemid 43021833)
30. Ikeno Y, Hubbard GB, Lee S, et al. Housing density does not influence the longevity effect of calorie restriction. J Gerontol A Biol Sci Med Sci. 2005;60(12):1510-1517. (Pubitemid 43146456)
31. 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;9(4):626-635.
32. Heidenreich PA, Trogdon JG, Khavjou OA, et al. Forecasting the future of cardiovascular disease in the United States: a policy statement from the American Heart Association. Circulation. 2011;123(8):933-944.
33. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010;60(5):277-300.
34. Lakatta EG. Age-associated cardiovascular changes in health: impact on cardiovascular disease in older persons. Heart Fail Rev. 2002;7(1):29-49. (Pubitemid 34154898)
35. McKee PA, Castelli WP, McNamara PM, Kannel WB. The natural history of congestive heart failure: the Framingham study. N Engl J Med. 1971;285(26):1441-1446.
36. Miller V, Best P. Implications for reproductive medicine: sex differences in cardiovascular disease. Sex Reprod Menopause. 2011;9(3):21-28.
37. Furman RH. Are gonadal hormones (estrogens and androgens) of significance in the development of ischemic heart disease. Ann N Y Acad Sci. 1968;149(2):822-833.
38. Kuhl H. Mechanisms of sex steroids. Future developments. Maturitas. 2004;47(4):285-291. (Pubitemid 38520114)
39. Pal L, Kallen AN. Cardiovascular disease and ovarian function. Curr Opin Obstet Gyn. 2011;23(4):258-267.
40. Huhtaniemi I, Forti G. Male late-onset hypogonadism: pathogenesis, diagnosis and treatment. Nat Rev Urol. 2011;8(6):335-344.
41. Evert J, Lawler E, Bogan H, Perls T. Morbidity profiles of centenarians: survivors, delayers, and escapers. J Gerontol A Biol Sci Med Sci. 2003;58(3):232-237. (Pubitemid 36307594)
42. Terry DF, Wilcox M, McCormick MA, Lawler E, Perls TT. Cardiovascular advantages among the offspring of centenarians. J Gerontol Med Sci. 2003;58(5):M425-M431.
43. Barzilai N, Gabriely I, Gabriely M, Iankowitz N, Sorkin JD. Offspring of centenarians have a favorable lipid profile. J Am Geriatr Soc. 2001;49(1):76-79. (Pubitemid 32197302)
44. Gillebert TC, Van de Veire N, De Buyzere ML, De Sutter J. Time intervals and global cardiac function. Use and limitations. Eur Heart J. 2004;25(24):2185-2186. (Pubitemid 39592418)
45. Groban L, Kitzman DW. Diastolic function: a barometer for cardiovascular risk? Anesthesiology. 2010;112(6):1303-1306.
46. Mandinov L, Eberli FR, Seiler C, Hess OM. Diastolic heart failure. Cardiovasc Res. 2000;45(4):813-825. (Pubitemid 30089643)
47. Basu R, Oudit GY, Wang X, et al. Type 1 diabetic cardiomyopathy in the Akita (Ins2WT/C96Y) mouse model is characterized by lipotoxicity and diastolic dysfunction with preserved systolic function. Am J Physiol Heart Circ Physiol. 2009;297(6):H2096-H2108.
48. Salmasi AM, Alimo A, Jepson E, Dancy M. Age-associated changes in left ventricular diastolic function are related to increasing left ventricular mass. Am J Hypertens. 2003;16(6):473-477. (Pubitemid 36667802)
49. Wilkenshoff UM, Hatle L, Sovany A, Wranne B, Sutherland GR. Age-dependent changes in regional diastolic function evaluated by color Doppler myocardial imaging: a comparison with pulsed Doppler indexes of global function. J Am Soc Echocardiogr. 2001;14(10):959-969. (Pubitemid 33095607)
50. Park HS, Naik SD, Aronow WS, Ahn CW, McClung JA, Belkin RN. Age-and sex-related differences in the tissue Doppler imaging parameters of left ventricular diastolic dysfunction. Echocardiography. 2007;24(6):567-571. (Pubitemid 46956603)
51. Flu WJ, van Kuijk JP, Hoeks SE, et al. Prognostic implications of asymptomatic left ventricular dysfunction in patients undergoing vascular surgery. Anesthesiology. 2010;112(6):1316-1324.
52. Halley CM, Houghtaling PL, Khalil MK, Thomas JD, Jaber WA. Mortality rate in patients with diastolic dysfunction and normal systolic function. Arch Intern Med. 2011;171(12):1082-1087.
53. Hartley CJ, Taffet GE, Reddy AK, Entman ML, Michael LH. Noninvasive cardiovascular phenotyping in mice. ILAR J. 2002;43(3):147-158. (Pubitemid 34495369)
54. Tanaka N, Dalton N, Mao L, et al. Transthoracic echocardiography in models of cardiac disease in the mouse. Circulation. 1996;94(5):1109-1117. (Pubitemid 26292868)
55. Takimoto E, Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension. 2007;49(2):241-248. (Pubitemid 46142995)
56. Andziak B, O'Connor TP, Buffenstein R. Antioxidants do not explain the disparate longevity between mice and the longest-living rodent, the naked mole-rat. Mech Ageing Dev. 2005;126(11):1206-1212. (Pubitemid 41356522)
57. Andziak B, O'Connor TP, Qi W, et al. High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell. 2006;5(6):463-471. (Pubitemid 44782615)
58. Rodriguez KA, Wywial E, Perez VI, et al. Walking the oxidative stress tightrope: a perspective from the naked mole-rat, the longest living rodent. Curr Pharm Des. 2011;17(22):2290-2307.
59. Lambert AJ, Boysen HM, Buckingham JA, et al. Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell. 2007;6(5):607-618. (Pubitemid 47400043)
60. Willcox BJ, Curb JD, Rodriguez BL. Antioxidants in cardiovascular health and disease: key lessons from epidemiologic studies. Am J Cardiol. 2008;101(10A):75D-86D.
61. Labinskyy N, Csiszar A, Orosz Z, et al. Comparison of endothelial function, O2-* and H2O2 production, and vascular oxidative stress resistance between the longest-living rodent, the naked mole rat, and mice. Am J Physiol Heart Circ Physiol. 2006;291(6):H2698-H2704. (Pubitemid 44904069)
62. Choy JC, Granville DJ, Hunt DW, McManus BM. Endothelial cell apoptosis: biochemical characteristics and potential implications for atherosclerosis. J Mol Cell Cardiol. 2001;33(9):1673-1690. (Pubitemid 32844225)
63. Ungvari Z, Buffenstein R, Austad SN, Podlutsky A, Kaley G, Csiszar A. Oxidative stress in vascular senescence: lessons from successfully aging species. Front Biosci. 2008;13:5056-5070. (Pubitemid 351599658)
64. Csiszar A, Pacher P, Kaley G, Ungvari Z. Role of oxidative and nitrosative stress, longevity genes and poly(ADP-ribose) polymerase in cardiovascular dysfunction associated with aging. Curr Vasc Pharmacol. 2005;3(3):285-291. (Pubitemid 40933050)
65. Csiszar A, Labinskyy N, Orosz Z, Xiangmin Z, Buffenstein R, Ungvari Z. Vascular aging in the longest-living rodent, the naked mole rat. Am J Physiol Heart Circ Physiol. 2007;293(2):H919-H927. (Pubitemid 47254187)
66. Hill W, Porter A, Bloom R, Seago J, Southwick M. Field and laboratory studies on the naked mole rat, Heterocephalus glaber. Proc Zool Soc Lond. 1955;128(4):455-514.
67. Whitesall SE, Hoff JB, Vollmer AP, D'Alecy LG. Comparison of simultaneous measurement of mouse systolic arterial blood pressure by radiotelemetry and tail-cuff methods. Am J Physiol Heart Circ Physiol. 2004;286(6):H2408-H2415. (Pubitemid 38685259)
68. Savage VM, Gillooly JF, Woodruff WH, et al. The predominance of quarter-power scaling in biology. Funct Ecol. 2004;18(2):257-282. (Pubitemid 38504290)
69. McArdle W, Katch F, Katch V. Essentials of Exercise Physiology. New York: Lippincott Williams & Wilkins; 2010.
70. Zhang WG, Zhang GQ. Heart rate, lifespan, and mortality risk. Ageing Res Rev. 2009;8(1):52-60.
71. Giannuzzi P, Imparato A, Temporelli PL, et al. Doppler-derived mitral deceleration time of early filling as a strong predictor of pulmonary capillary wedge pressure in postinfarction patients with left ventricular systolic dysfunction. J Am Coll Cardiol. 1994;23(7):1630-1637. (Pubitemid 24182130)
72. Vasan RS, Larson MG, Benjamin EJ, Evans JC, Reiss CK, Levy D. Congestive heart failure in subjects with normal versus reduced left ventricular ejection fraction: prevalence and mortality in a population-based cohort. J Am Coll Cardiol. 1999;33(7):1948-1955.
73. Redfield MM, Jacobsen SJ, Burnett JC Jr, Mahoney DW, Bailey KR, Rodeheffer RJ. Burden of systolic and diastolic ventricular dysfunction in the community: appreciating the scope of the heart failure epidemic. JAMA. 2003;289(2):194-202. (Pubitemid 36068707)
74. Kim EB, Fang X, Fushan AA, et al. Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature. 2011;479(7372):223-227.
75. Edrey Y, Buffenstein R. Animal models in aging and Alzheimer's disease. In: Hau J, Schapiro S, eds. Handbook of Laboratory Animal Science, Volume II, Third Edition: Animal Models. New York: Taylor & Francis Group. In press:97-121.
76. de Magalhaes JP, Costa J, Church GM. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J Gerontol A Biol Sci Med Sci. 2007;62(2):149-160. (Pubitemid 47065738)
77. Rabinovitch PS, Dai DF. Cardiac aging in mice and humans: the role of mitochondrial oxidative stress. Trends Cardiovas Med. 2009;19(7):213-220.
78. Taffet GE, Pham TT, Hartley CJ. The age-associated alterations in late diastolic function in mice are improved by caloric restriction. J Gerontol Biol Sci. 1997;52(6):B285-B290. (Pubitemid 28006991)
79. Meyer TE, Kovacs SJ, Ehsani AA, Klein S, Holloszy JO, Fontana L. Long-term caloric restriction ameliorates the decline in diastolic function in humans. J Am Coll Cardiol. 2006;47(2):398-402. (Pubitemid 43063261)
80. Bokov AF, Lindsey ML, Khodr C, Sabia MR, Richardson A. Long-lived ames dwarf mice are resistant to chemical stressors. J Gerontol A Biol Sci Med Sci. 2009;64(8):819-827.
81. Reddy AK, Amador-Noguez D, Darlington GJ, et al. Cardiac function in young and old Little mice. J Gerontol A Biol Sci Med Sci. 2007;62(12):1319-1325. (Pubitemid 351158360)
82. Perez VI, Buffenstein R, Masamsetti V, et al. Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc Natl Acad Sci USA. 2009;106(9):3059-3064.
83. Salmon AB, Sadighi Akha AA, Buffenstein R, Miller RA. Fibroblasts from naked mole-rats are resistant to multiple forms of cell injury, but sensitive to peroxide, ultraviolet light, and endoplasmic reticulum stress. J Gerontol A Biol Sci Med Sci. 2008;63(3):232-241. (Pubitemid 351738427)
84. Lewis KN, Mele J, Hayes JD, Buffenstein R. Nrf2, a guardian of healthspan and gatekeeper of species longevity. Integr Comp Biol. 2010;50(5):829-843.
85. Sykiotis GP, Habeos IG, Samuelson AV, Bohmann D. The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr Opin Clin Nutr. 2011;14(1):41-48.
86. Martin-Montalvo A, Villalba JM, Navas P, de Cabo R. NRF2, cancer and calorie restriction. Oncogene. 2011;30(5):505-520.
87. Tullet JMA, Hertweck M, An JH, et al. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell. 2008;132(6):1025-1038. (Pubitemid 351391953)
88. Yu C, Li Y, Holmes A, et al. RNA sequencing reveals differential expression of mitochondrial and oxidation reduction genes in the long-lived naked mole-rat when compared to mice. PLoS One. In press.