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

Volumn 46, Issue 1, 2010, Pages 112-120

  Pinto, M ^a,b   Jepsen, K J ^a,c   Terranova, C J ^c   Buffenstein, R ^a,b  

^a CITY COLLEGE OF NEW YORK   (United States)

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

^c Mount Sinai   (United States)

Author keywords

Aging; Bone quality; Bone strength; Delayed puberty; Hypogonadic; Naked mole rats

Indexed keywords

SEX HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BONE DENSITY; BONE DEVELOPMENT; BONE STRESS; BONE STRUCTURE; CONTROLLED STUDY; DELAYED PUBERTY; DIAPHYSIS; FEMALE; FEMUR; HORMONE INHIBITION; HORMONE RELEASE; HYPOGONADISM; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MALE; METAPHYSIS; MICRO-COMPUTED TOMOGRAPHY; MOLE RAT; NONHUMAN; PHENOTYPE; RAT; SEX DIFFERENCE;

ANIMALS; BONE AND BONES; DISEASE MODELS, ANIMAL; FEMALE; FEMUR; HYPOGONADISM; MALE; MOLE RATS; PUBERTY, DELAYED; SEX CHARACTERISTICS;

EID: 72049085789     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2009.08.060     Document Type: Article

References (64)

1. Falahati-Nini A., Riggs B.L., Atkinson E.J., O'Fallon W.M., Eastell R., and Khosla S. Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J. Clin. Invest. 106 (2000) 1553-1560
2. Zirilli L., Rochira V., Diazzi C., Caffagni G., and Carani C. Human models of aromatase deficiency. J. Steroid. Biochem. Mol. Biol. 109 (2008) 212-218
3. Garn S. The Earlier Gain and the Later Loss of Cortical Bone (1970), Charles C Thomas, Springfield, IL
4. Golden N.H., and Carlson J.L. The pathophysiology of amenorrhea in the adolescent. Ann. N.Y. Acad. Sci. 1135 (2008) 163-178
5. Yingling V.R., and Taylor G. Delayed pubertal development by hypothalamic suppression causes an increase in periosteal modeling but a reduction in bone strength in growing female rats. Bone 42 (2008) 1137-1143
6. Bennell K.L., Brukner P.D., and Malcolm S.A. Effect of altered reproductive function and lowered testosterone levels on bone density in male endurance athletes. Br. J. Sports Med. 30 (1996) 205-208
7. Cools B.L., Rooman R., Op De Beeck L., and Du Caju M.V. Boys with a simple delayed puberty reach their target height. Horm. Res. 70 (2008) 209-214
8. Ambler G.R. Androgen therapy for delayed male puberty. Curr. Opin. Endocrinol. Diabetes Obes. 16 (2009) 232-239
9. Finkelstein J.S., Neer R.M., Biller B.M., Crawford J.D., and Klibanski A. Osteopenia in men with a history of delayed puberty. N. Engl. J. Med. 326 (1992) 600-604
10. Rochira V., Balestrieri A., Madeo B., Zirilli L., Granata A.R., and Carani C. Osteoporosis and male age-related hypogonadism: role of sex steroids on bone (patho)physiology. Eur. J. Endocrinol. 154 (2006) 175-185
11. Kohrt W.M., Van Pelt R.E., and Gozansky W.S. Effects of estrogen replacement on metabolic factors that influence physical performance in female hypogonadism. J. Endocrinol. Invest. 26 (2003) 902-910
12. Chevalley T., Bonjour J.P., Ferrari S., and Rizzoli R. Deleterious effect of late menarche on distal tibia microstructure in healthy 20-year-old and premenopausal middle-aged women. J. Bone Miner. Res. 24 (2009) 144-152
13. Rosenthal D.I., Mayo-Smith W., Hayes C.W., Khurana J.S., Biller B.M., Neer R.M., and Klibanski A. Age and bone mass in premenopausal women. J. Bone Miner. Res. 4 (1989) 533-538
14. Johnell O., Gullberg B., Kanis J.A., Allander E., Elffors L., Dequeker J., Dilsen G., Gennari C., Lopes Vaz A., Lyritis G., et al. Risk factors for hip fracture in European women: the MEDOS Study. Mediterranean Osteoporosis Study. J. Bone Miner. Res. 10 (1995) 1802-1815
15. Park K.H., Lee S.J., Kim J.Y., Kim J.Y., Bai S.W., and Kim J.W. A concomitant decrease in cortical and trabecular bone mass in isolated hypogonadotropic hypogonadism and gonadal dysgenesis. Yonsei Med. J. 40 (1999) 444-449
16. Silman A.J. Risk factors for Colles' fracture in men and women: results from the European Prospective Osteoporosis Study. Osteoporos. Int. 14 (2003) 213-218
17. Jarvis J.U. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212 (1981) 571-573
18. Buffenstein R. The naked mole-rat: a new long-living model for human aging research. J. Gerontol. A Biol. Sci. Med. Sci. 60 (2005) 1369-1377
19. O'Riain M.J., Jarvis J.U., Alexander R., Buffenstein R., and Peeters C. Morphological castes in a vertebrate. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 13194-13197
20. Dengler-Crish C.M., and Catania K.C. Phenotypic plasticity in female naked mole-rats after removal from reproductive suppression. J. Exp. Biol. 210 (2007) 4351-4358
21. Faulkes C.G., and Bennett N.C. Family values: group dynamics and social control of reproduction in African mole-rats. Trends Ecol. Evol. 16 (2001) 184-190
22. Faulkes C.G., Abbott D.H., Jarvis J.U., and Sherriff F.E. LH responses of female naked mole-rats, Heterocephalus glaber, to single and multiple doses of exogenous GnRH. J. Reprod. Fertil. 89 (1990) 317-323
23. Jarvis J.U. Reproduction in naked mole-rats. In: Sherman P.W., Jarvis J.U., and Alexander R.D. (Eds). The Biology of the Naked Mole-Rat New Jersey (1991) 384-425
24. Clarke F.M., and Faulkes C.G. Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. Proc. Biol. Sci. 265 (1998) 1391-1399
25. Buffenstein R., Sergeev I.N., and Pettifor J.M. Vitamin D hydroxylases and their regulation in a naturally vitamin D-deficient subterranean mammal, the naked mole rat (Heterocephalus glaber). J. Endocrinol. 138 (1993) 59-64
26. Flor-Cisneros A., Roemmich J.N., Rogol A.D., and Baron J. Bone age and onset of puberty in normal boys. Mol. Cell. Endocrinol. 254-255 (2006) 202-206
27. Holmes M.M., Rosen G.J., Jordan C.L., de Vries G.J., Goldman B.D., and Forger N.G. Social control of brain morphology in a eusocial mammal. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 10548-10552
28. Holmes M.M., Goldman B.D., and Forger N.G. Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain. Horm. Behav. 54 (2008) 278-285
29. Bass S., Delmas P.D., Pearce G., Hendrich E., Tabensky A., and Seeman E. The differing tempo of growth in bone size, mass, and density in girls is region-specific. J. Clin. Invest. 104 (1999) 795-804
30. Seeman E. Invited review: pathogenesis of osteoporosis. J. Appl. Physiol. 95 (2003) 2142-2151
31. Faulkes C.G., Abbott D.H., and Jarvis J.U. Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber. J. Reprod. Fertil. 91 (1991) 593-604
32. Faulkes C.G., Abbott D.H., and Jarvis J.U. Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber. J. Reprod. Fertil. 88 (1990) 559-568
33. Otsu N.A. threshold selection mothod from gray-level histograms. IEEE Transactions on Systems. Man and Cybernetics 9 (1979) 62-66
34. Faulkes C.G., and Bennett N.C. African Mole-rats Ecology and Eusociality (2000), Press Syndicate of the University of Cambridge, Cambridge
35. Buffenstein R. Ecophysiological responses to an underground habitat. In: Lacey E., Patton J., and Cameron G. (Eds). The Biology of Subterranean Rodents (2000), Chicago University Press, Chicago 62-110
36. Stein B.R. Morphology of subterranean rodents. In: Lacey E., Patton J., and Cameron G. (Eds). The Biology of Subterranean Rodents (2000), Chicago University Press, Chicago 19-91
37. Biknevicius A.R. Biomechanical scaling of limb bones and differential limb use in the caviomorph rodents. J. Mammal. 74 (1993) 95-107
38. Buffenstein R., Jarvis J.U., Opperman L.A., Cavaleros M., Ross F.P., and Pettifor J.M. Subterranean mole-rats naturally have an impoverished calciol status, yet synthesize calciol metabolites and calbindins. Eur. J. Endocrinol. 130 (1994) 402-409
39. Pitcher T., Pettifor J.M., and Buffenstein R. The effect of dietary calcium content and oral vitamin-D-3 supplementation on mineral homeostasis in a subterranean mole-rat Cryptomys damarensis. Bone and Mineral 27 (1994) 145-157
40. Pitcher T., Sergeev I.N., and Buffenstein R. Vitamin-D Metabolism in the damara mole-rat is altered by exposure to sunlight yet mineral metabolism is unaffected. J. Endocrinol. 143 (1994) 367-374
41. Lacey E.A., Alexander R.D., Braude S.H., Sherman P.W., and Jarvis J.U. An ethogram for the naked mole-rat: nonvocal behaviors. In: Sherman P.W., Jarvis J.U., and Alexander R.D. (Eds). The Biology of the Naked Mole-Rat (1991), Princeton University Press, New Jersey 209-242
42. Lacey E.A., and Sherman P.W. Social organization of naked mole-rat colonies: evidence for divisions of labor. In: Sherman P.W., Jarvis J.U., and Alexander R.D. (Eds). The Biology of the Naked Mole-Rat (1991), Princeton University Press, Princeton, New Jersey 275-336
43. Peroulakis M.E., Goldman B., and Forger N.G. Perineal muscles and motoneurons are sexually monomorphic in the naked mole-rat (Heterocephalus glaber). J. Neurobiol. 51 (2002) 33-42
44. Henry E.C., Dengler-Crish C.M., and Catania K.C. Growing out of a caste-reproduction and the making of the queen mole-rat. J. Exp. Biol. 210 (2007) 261-268
45. Seeman E. Estrogen, androgen, and the pathogenesis of bone fragility in women and men. Curr. Osteoporos. Rep. 2 (2004) 90-96
46. Turner R.T., Vandersteenhoven J.J., and Bell N.H. The effects of ovariectomy and 17 beta-estradiol on cortical bone histomorphometry in growing rats. J. Bone Miner. Res. 2 (1987) 115-122
47. Zhang X.Z., Kalu D.N., Erbas B., Hopper J.L., and Seeman E. The effects of gonadectomy on bone size, mass, and volumetric density in growing rats are gender-, site-, and growth hormone-specific. J. Bone Miner. Res. 14 (1999) 802-809
48. Urison N.T., and Buffenstein R. Metabolic and body-temperature changes during pregnancy and lactation in the naked mole-rat (Heterocephalus-glaber). Physiol. Zool. 68 (1995) 402-420
49. Seney M., Goldman B.D., and Forger N.G. Breeding status affects motoneuron number and muscle size in naked mole-rats: recruitment of perineal motoneurons?. J. Neurobiol. 66 (2006) 1354-1364
50. Holmes M.M., Goldman B.D., Goldman S.L., Seney M.L., and Forger N.G. Neuroendocrinology and sexual differentiation in eusocial mammals. Front Neuroendocrinol. 30 (2009) 519-533
51. Daniels E.D., Pettifor J.M., Schnitzler C.M., Moodley G.P., and Zachen D. Differences in mineral homeostasis, volumetric bone mass and femoral neck axis length in black and white South African women. Osteoporos. Int. 7 (1997) 105-112
52. Schnitzler C.M., Pettifor J.M., Mesquita J.M., Bird M.D., Schnaid E., and Smyth A.E. Histomorphometry of iliac crest bone in 346 normal black and white South African adults. Bone Miner. 10 (1990) 183-199
53. Price C., Herman B.C., Lufkin T., Goldman H.M., and Jepsen K.J. Genetic variation in bone growth patterns defines adult mouse bone fragility. J. Bone Miner. Res. 20 (2005) 1983-1991
54. Ramanadham S., Yarasheski K.E., Silva M.J., Wohltmann M., Novack D.V., Christiansen B., Tu X., Zhang S., Lei X., and Turk J. Age-related changes in bone morphology are accelerated in group VIA phospholipase A2 (iPLA2beta)-null mice. Am. J. Pathol. 172 (2008) 868-881
55. Glatt V., Canalis E., Stadmeyer L., and Bouxsein M.L. Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J. Bone Miner. Res. 22 (2007) 1197-1207
56. Buffenstein R. Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J. Comp. Physiol. [B] 178 (2008) 439-445
57. Warren M.P., Brooks-Gunn J., Fox R.P., Holderness C.C., Hyle E.P., and Hamilton W.G. Osteopenia in exercise-associated amenorrhea using ballet dancers as a model: a longitudinal study. J. Clin. Endocrinol. Metab. 87 (2002) 3162-3168
58. Ito M., Yamada M., Hayashi K., Ohki M., Uetani M., and Nakamura T. Relation of early menarche to high bone mineral density. Calcif. Tissue Int. 57 (1995) 11-14
59. Yingling V.R., Xiang Y., Raphan T., Schaffler M.B., Koser K., and Malique R. The effect of a short-term delay of puberty on trabecular bone mass and structure in female rats: a texture-based and histomorphometric analysis. Bone 40 (2007) 419-424
60. Krewson T.D., Supelak P.J., Hill A.E., Singer J.B., Lander E.S., Nadeau J.H., and Palmert M.R. Chromosomes 6 and 13 harbor genes that regulate pubertal timing in mouse chromosome substitution strains. Endocrinology 145 (2004) 4447-4451
61. Jepsen K.J., Akkus O.J., Majeska R.J., and Nadeau J.H. Hierarchical relationship between bone traits and mechanical properties in inbred mice. Mamm. Genome 14 (2003) 97-104
62. Yingling V.R., and Khaneja A. Short-term delay of puberty causes a transient reduction in bone strength in growing female rats. Bone 38 (2006) 67-73
63. Roth C., Leonhardt S., Seidel C., Luft H., Wuttke W., and Jarry H. Comparative analysis of different puberty inhibiting mechanisms of two GnRH agonists and the GnRH antagonist cetrorelix using a female rat model. Pediatr. Res. 48 (2000) 468-474
64. Clarke F.M., and Faulkes C.G. Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc. Biol. Sci. 264 (1997) 993-1000