Spontaneous histologic lesions of the adult naked mole rat (Heterocephalus glaber): A retrospective survey of lesions in a zoo population

Veterinary Pathology

Volumn 50, Issue 4, 2013, Pages 607-621

  Delaney, M A ^a   Nagy, L ^b   Kinsel, M J ^a   Treuting, P M ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Aging; Animal model; Calcinosis; Hemosiderosis; Heterocephalus glaber; Naked mole rat; Neoplasia; Trauma

Indexed keywords

AGING; ANIMAL; FEMALE; MALE; MOLE RAT; MORTALITY; PATHOLOGY; RAT; RETROSPECTIVE STUDY; RODENT DISEASE; ZOO ANIMAL;

AGING; ANIMALS; ANIMALS, ZOO; FEMALE; MALE; MOLE RATS; RATS; RETROSPECTIVE STUDIES; RODENT DISEASES;

EID: 84880512646     PISSN: 03009858     EISSN: 15442217     Source Type: Journal    
DOI: 10.1177/0300985812471543     Document Type: Article

References (101)

1. Alpers CE. The kidney. In: Robbins SL, Kumar V, Cotran RS, eds. Robbins and Cotran Pathologic Basis of Disease. 8th ed. Philadelphia, PA: Saunders/Elsevier; 2010:905-970.
2. Andziak B, Buffenstein R. Disparate patterns of age-related changes in lipid peroxidation in long-lived naked mole-rats and shorter-lived mice. Aging Cell. 2006;5(6):525-532.
3. Andziak B, O'Connor TP, Buffenstein R. Antioxidants do not explain the disparate longevity between mice and the longestliving rodent, the naked mole-rat. Mechanisms of ageing and development. 2005;126(11):1206-1212.
4. 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.
5. Austad SN. Comparative biology of aging. J Gerontol A Biol Sci Med Sci. 2009;64(2):199-201.
6. Austad SN. Methusaleh's zoo: how nature provides us with clues for extending human health span. JCompar Pathol. 2010;142(suppl 1): S10-S21.
7. Bennett NC, Faulkes CG. The Evolution of Sociality in African Mole-Rats. Cambridge, UK: Cambridge University Press; 2000.
8. Bennett NC, Faulkes CG. Social Organisation in African Mole-Rats. Cambridge, UK: Cambridge University Press; 2000.
9. Bennett NC, Jarvis JUM. The social structure and reproductive biology of colonies of the mole-rat Cryptomys damarensis (Rodentia: Bathyergidae). J Mammal. 1988;69:293-302.
10. Bhattacharya A, Leonard S, Tardif S, et al. Attenuation of liver insoluble protein carbonyls: indicator of a longevity determinant? Aging Cell. 2011;10:720-723.
11. Bonar CJ, Trupkiewicz JG, Toddes B, et al. Iron storage disease in tapirs. J Zoo Wildl Med. 2006;37(1):49-52.
12. Brayton CF, Treuting PM, Ward JM. Pathobiology of aging mice and GEM: background strains and experimental design. Vet Pathol. 2012;49(1):85-105.
13. Brett RA. The Population Structure of Naked Mole-Rat Colonies. Princeton, NJ: Princeton University Press; 1991.
14. Buffenstein R. Ecological and Physiological Responses to Underground Habitats. Chicago, IL: University of Chicago Press; 2000.
15. Buffenstein R. The naked mole-rat: A new long-living model for human aging research. J Gerontol Bio Sci. 2005;60(11): 1369-1377.
16. Buffenstein R. Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Compar Physiol B. 2008;178(4):439-445.
17. Buffenstein R, Edrey YH, Yang T, et al. The oxidative stress theory of aging: embattled or invincible? Insights from nontraditional model organisms. Age. 2008;30(2-3):99-109.
18. Buffenstein R, Jarvis JUM. The naked mole rat: a new record for the oldest living rodent. Sci Aging Knowl Environ. 2002; 2002(21):4.
19. Buffenstein R, Kang HJ, Biney A. Glucose tolerance and insulin sensitivity in an extremely long-living rodent, the naked mole-rat. FASEB J. 2007;21:A1423-A1423.
20. Buffenstein R, Laundy MT, Pitcher T, et al. Vitamin D3 intoxication in naked mole-rats (Heterocephalus glaber) leads to hypercalcaemia and increased calcium deposition in teeth with evidence of abnormal skin calcification. Gen Compar Endocrinol. 1995;99(1):35-40.
21. Buffenstein R, Park T, Hanes M, et al. Naked mole rat. In: Suckow MA, Stevens KA, Wilson RP, eds. The Laboratory Rabbit, Guinea Pig, Hamster, and Other Rodents. London, England: Elsevier; 2012:1055-1074.
22. Buffenstein R, Pinto M. Endocrine function in naturally longliving small mammals. Mol Cell Endocrinol. 2009;299:101-111.
23. Buffenstein R, Skinner DC, Yahav S, et al. Effect of oral cholecalciferol supplementation at physiological and supraphysiological doses in naturally vitamin D3-deficient subterranean damara mole rats (Cryptomys damarensis). J Endocrinol. 1991;131(2):197-202.
24. Buffenstein R, Yahav S. The effect of diet on microfaunal population and function in the caecum of a subterranean naked mole-rat, Heterocephalus glaber. Br J Nutr. 1991;65(2):249-258.
25. Cardiff RD, Anver MR, Boivin GP, et al. Precancer in mice: animal models used to understand, prevent, and treat human precancers. Toxicol Pathol. 2006;34(6):699-707.
26. Cardiff RD, Ward JM, Barthold SW. "One medicine-one pathology": are veterinary and human pathology prepared? Lab Invest. 2008;88(1):18-26.
27. Cesta MF. Normal structure, function, and histology of the spleen. Toxicol Pathol. 2006;34:455-465.
28. Chamanza R, Marxfield HA, Blanco AI, et al. Incidences and range of spontaneous findings in control cynomolgus monkeys (Macaca fascicularis) used in toxicity studies. Toxicol Pathol. 2010;38:642-657.
29. Clarke FM, Faulkes CG. Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc Biol Sci. 1997;264:993-1000.
30. 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; 264(1404):1391-1399.
31. Clarke FM, Faulkes CG. Intra-colony aggression in the naked mole-rat, Heterocephalus glaber. Anim Behav. 2001;61:311-324.
32. Csiszar A, Labinsky N, Orosz Z, et al. Vascular aging in the longest-living rodent, the naked mole rat. Am J Physiol. 2007; 293:H919-H927.
33. Cullen J, Brown, DL. Hepatobiliary system and exocrine pancreas. In: Zachary JF, McGavin MD, eds. Pathologic Basis of Veterinary Disease. 5th ed. St Louis, MO: Elsevier; 2012:437-442.
34. Deugnier Y, Turlin B. Pathology of hepatic iron overload. World J Gastroenterol. 2007;13(35):4655-4760.
35. Edrey YH, Casper D, Huchon D, et al. Sustained high levels of neuregulin-1 in the longest-lived rodents; a key determinant of rodent longevity. Aging Cell. 2012;11(2):213-222.
36. Edrey YH, Hanes M, Pinto M, et al. 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.
37. Elmore SA. Enhanced histopathology of the thymus. Toxicol Pathol. 2006;34:656-665.
38. Endo H, Okanoya K, Park TJ, et al. Localization of the cytochrome p450 side-chain cleavage enzyme in the inactive testis of the naked mole-rat. Zoo Sci. 2002;19(6):673-678.
39. Estivarez FE, Lowry PJ, Jackson S. Control of Adrenal Growth. New York, NY: Raven Press; 1992.
40. Farina LL, Heard DJ, LeBlanc DM, et al. Iron storage disease in captive Egyptian fruit bats (Rousettus aegyptiacus): relationship of blood iron parameters to hepatic iron concentrations and hepatic histopathology. J Zoo Wildl Med. 2005;36(2):212-221.
41. Faulkes CG, Abbott DH. Social control of reproduction in breeding and non-breeding male naked mole-rats (Heterocephalus glaber). J Reprod Fertil. 1991;93(2):427-435.
42. 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.
43. Faulkes CG, Abbott DH, Jarvis JUM. Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber. J Reprod Fertil. 1991;91:593-604.
44. Faulkes CG, Trowell SN, Jarvis JU, Bennett NC. Investigation of numbers and motility of spermatozoa in reproductively active and socially suprressed males of two eusocial African mole-rats, the naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Cryptomys damarensis). J Reprod Fertil. 1994;100: 411-416.
45. Fawcett DW, Neaves WB, Flores MN. Comparative observations on intertubular lymphatics and the organization of the interstitial tissue of the mammalian testis. Biol Reprod. 1973;9(5):500-532.
46. Finch CE. Update on slow aging and negligible senescence: a mini-review. Gerontology. 2009;55:307-313.
47. Frith CH, Ward JM, Chandra M. The morphology, immunohistochemistry, and incidence of hematopoietic neoplasms in mice and rats. Toxicol Pathol. 1993;21(2):206-218.
48. Frith CH, Ward JM, Harleman JH, et al. Hematopoietic system. In: Mohr U, ed. International Classification of Rodent Tumors: Part II. The Mouse. New York, NY: Springer; 2001:417-451.
49. Frith CH, Wiley LD. Morphologic classification and correlation of incidence of hyperplastic and neoplastic hematopoietic lesions in mice with age. J Gerontol. 1981;36(5):534-545.
50. Gonzales J, Benirschke K, Saltman P, et al. Hemosiderosis in lemurs. Zoo Biol. 1984;3(3):255-265.
51. Gorbunova V, Bozzella MJ, Seluanov A. Rodent for comparative aging studies: from mice to beavers. Age. 2008;30:111-119.
52. Grimes KM, Lindsey ML, Gelfond JAL, et al. Getting to the heart of the matter: age-related changes in diastolic heart function in the longest-lived rodent, the naked mole rat. J Gerontol A Biol Sci Med Sci. 2012;67(4):384-394.
53. Hard GC, Betz LJ, Seely JC. Association of advanced chronic progressive nephropathy (CPN) with renal tubule tumors and precursor hyperplasia in control F344 rats from two-year carcinogenicity studies. Toxicol Pathol. 2011;40(3):473-481.
54. Hard GC, Johnson KJ, Cohen SM. A comparison of rat chronic progressive nephropathy with human renal disease-implications for human risk assessment. Crit Rev Toxicol. 2009;39(4):332-346.
55. Hard GC, Seely JC. Recommendations for the interpretation of renal tubule proliferative lesions occurring in rat kidneys with advanced chronic progressive nephropathy (CPN). Toxicol Pathol. 2005;33:641-649.
56. Hulbert AJ, Faulks SC, Buffenstein R. Oxidation-resistant membrane phospholipids can explain longevity differences among the longest-living rodents and similarly-sized mice. J Gerontol A Biol Sci Med Sci. 2006;61(10):1009-1018.
57. Jarvis JUM. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science. 1981;212(4494):571-573.
58. 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.
59. Kock N, Foggin C, Kock MD, et al. Hemosiderosis in the black rhinoceros (Diceros bicornis): a omparison of free-ranging and recently captured with recently captured with translocated and captive animals. J Zoo Wildl Med. 1992;23(2):230-234.
60. Kramer B, Buffenstein R. The pancreas of the naked mole-rat (Heterocephalus glaber): an ultrastructural and immunocytochemical study of the endocrine component of thermoneutral and cold acclimated animals Gen Compar Endocrinol. 2004;139:206-214.
61. Lacey EA, Alexander RD, Braude SH, et al. An Ethogram for the Naked Mole-Rat: Nonvocal Behaviors. Princeton, NJ: Princeton University Press; 1991.
62. Lacey EA, Patton JL, Cameron GN. Life Underground: The Biology of Subterranean Rodents. Chicago, IL: University of Chicago Press; 2000.
63. LaPerle KMD. Endocrine System. St Loius, MO: Elsevier; 2012.
64. Larson J, Park TJ. Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport. 2009;20(18):1634-1637.
65. Lewis KN, Mele J, Hayes JD, et al. Nrf2, a guardian of healthspan and gatekeeper of species longevity. Integr Compar Biol. 2010; 50(5):829-843.
66. Liang S, Mele J, Wu Y, et al. Resistance to experimental tumorigenesis in cells of a long-lived mammal, the naked molerat (Heterocephalus glaber). Aging Cell. 2010;9:626-635.
67. Linden M, Ward JM, Cherian S. Hematopoietic and lymphoid tissues. In: Treuting PAD, ed. Comparative Anatomy and Histology: A Mouse and Human Atlas. London, England: Academic Press; 2012:309-338.
68. Lowenstine LJ, Munson L. Iron Overload in the Animal Kingdom. Philadelphia, PA: WB Saunders; 1999.
69. Maina JN, Gebreegziabher Y, Woodley R, et al. Effects of change in environmental temperature and natural shifts in carbon dioxide and oxygen concentrations on the lungs of captive naked molerats (Heterocephalus glaber): a morphological and morphometric study. J Zoo. 2001;253:371-382.
70. Mitchell TW, Buffenstein R, Hulbert AJ. Membrane phospholipids composition may contribute to exceptional longeivity of the naked mole-rat (Hetercephalus glaber): a comparative study using shotgun lipidomics. Experim Gerontol. 2007;42:1053-1062.
71. Morse HC, 3rd, Anver MR, Fredrickson TN, et al. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood. 2002;100(1):246-258.
72. Myers RK, McGavin MD, Zachary JF. Cellular Adaptations, Injury, and Death: Morphologic, Biochemical, and Genetic Bases. St Louis, MO: Elsevier; 2012.
73. Nadon NL. Maintaining aged rodents for biogerontology research. Lab An. 2004;33(8):36-41.
74. O'Connor TP, Lee A, Jarvis JUM, et al. Prolonged longevity in naked mole rats: age-related changes in the metabolism, body composition and gastrointestinal function. Compar Biochem Physiol. 2002;133:835-842.
75. Onyango DW, Oduor-Okelo D, Otiang'a-Owiti GE. Ultrastructural study of the testis of non-breeding naked mole-rat (Heterocephalus glaber, Ruppell). Ann Anat. 1993;175(5):447-452.
76. Park TJ, Lu Y, Juttner R, et al. Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). PLoS Biol. 2008;6(1): e13.
77. Pearce G. Normal structure, function, and histology of the thymus. Toxicol Pathol. 2006;34:504-514.
78. Percy DH, Barthold SW. Mouse. In: Percy DH, Barthold SW, eds. Pathology of Laboratory Rodents and Rabbits. 3rd ed. Ames, IA: Blackwell; 2007:3-124.
79. Percy DH, Barthold SW. Rat. In: Percy DH, Barthold SW, eds. Pathology of Laboratory Rodents and Rabbits. 3rd ed. Ames, IA: Blackwell; 2007:125-178.
80. 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 U S A. 2009;106(9):3059-3064.
81. Pettan-Brewer C, Treuting PM. Practical pathology of aging mice. Pathobiol Aging Age Relat Dis. 2011;1(7202).
82. Pinto M, Jespen KJ, Terranova CJ, et al. 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.
83. Pitcher T, Buffenstein R. Intestinal calcium transport in mole-rats (Cryptomys damarensis and Heterocephalus glaber) is independent of both genomic and non-genomic vitamin D mediation. Experim Physiol. 1995;80:597-608.
84. Pitcher T, Pettifor JM, Buffenstein R. The effect of dietary calcium content and oral vitamin D3 supplementation on mineral homeostasis in a subterranean mole-rat Cryptomys damarensis. Bone Mineral. 1994;27:145-157.
85. Rehg JE, Bush D, Ward JM. The utility of immunohistochemistry for the identification of hematopoietic and lymphoid cells in normal tissues and interpretation of proliferative and inflammatory lesions of mice and rats. Toxicol Pathol. 2012;40(2):345-374.
86. 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.
87. Ross-Gillespie A, O'Riain MJ, Keller LF. Viral epizootic reveals inbreeding depression in a habitually inbreeding mammal. Evolution. 2007;61(9):2268-2273.
88. Salmon AB, Sadighi Akha AA, Buffenstein R, et al. Fibroblasts from naked mole-rats are resistant to multiple forms of cell injury, but sensistive to peroxide, UV light, and ER stress. J Gerontol A Biol Sci Med Sci. 2008;63(3):232-241.
89. Schriner SE, Linford NJ, Martin GM, et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science. 2005;308(5730):1909-1911.
90. Seluanov A, Hine C, Azpurua J, et al. Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat. Proc Natl Acad Sci U S A. 2009;106(46):19352-19357.
91. Seney ML, Kelly DA, Goldman BD, et al. Social structure predicts genital morphology in African mole-rats. PLoS One. 2009;4(10).
92. Sherman PW, Jarvis JUM, Alexander RD. The Biology of the Naked Mole-Rat. Princeton, NJ: Princeton University Press; 1991.
93. Shoieb A, Allavena R, Swallow J, et al. Peritoneal sarcomatosis associated with telemetry implants in Sprague Dawley CD rats. Toxicol Pathol. 2012;40(1):113-121.
94. Staker MJ, Hayes MA. Liver and Biliary System. Vol 2. Philadelphia, PA: WB Saunders; 2007.
95. Thoolen B, Maronpot RR, Harada T, et al. Proliferative and nonproliferative lesions of the rat and mouse hepatobiliary system. Toxicol Pathol. 2010;38(7):5S-81S.
96. Treuting P, Dintzis, SM, et al. Introduction. In: Treuting PAD, ed. Comparative Anatomy and Histology: A Mouse and Human Atlas. London, England: Academic Press; 2012:1-6.
97. Ungvari Z, Buffenstein R, Austad SN, et al. Oxidative stress in vascular senescence: lessons from a successfully aging species. Front Biosci. 2008;13:5056-5070.
98. Ward JM, Rehg JE, Morse HC 3rd. Differentiation of rodent immune and hematopoietic system reactive lesions from neoplasias. Toxicol Pathol. 2012;40(3):425-434.
99. Yahav S, Buffenstein R, Pettifor JM. Calcium and inorganic phosphorus metabolism in naked mole rats Heterocephalus glaber is only indirectly affected by cholecalciferol. Gen Comp Endocrinol. 1993;89:161-166.
100. Yang T, Buffenstein R. Disparate age effects on gastrointestinal enzymes in naked mole-rats. Integr Comp Biol. 2002;42: 1340-1341.
101. 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. 2011;6(11).