Increased PTHrP and decreased estrogens alter bone turnover but do not reproduce the full effects of lactation on the skeleton

Endocrinology

Volumn 151, Issue 12, 2010, Pages 5591-5601

  Ardeshirpour, Laleh ^a   Brian, Susan ^a   Dann, Pamela ^a   VanHouten, Joshua ^a   Wysolmerski, John ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; ESTROGEN; LEUPRORELIN; PARATHYROID HORMONE; PARATHYROID HORMONE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE STRUCTURE; BONE TURNOVER; CALCIUM MOBILIZATION; CALCIUM URINE LEVEL; CELL COUNT; CONTROLLED STUDY; ESTROGEN DEFICIENCY; FEMALE; FEMUR; LACTATION; MORPHOMETRICS; MOUSE; NONHUMAN; OSMOTIC MINIPUMP; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OVARIECTOMY; PRIORITY JOURNAL; SPINE; TRABECULAR BONE;

ANIMALS; BONE AND BONES; BONE DENSITY; ESTROGENS; FEMALE; FERTILITY AGENTS, FEMALE; LACTATION; LEUPROLIDE; MICE; OVARIECTOMY; PARATHYROID HORMONE-RELATED PROTEIN;

EID: 78649816939     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0566     Document Type: Article

References (68)

1. Kovacs CS, Kronenberg HM 1997 Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr Rev 18:832-872 (Pubitemid 28009569)
2. VanHouten J 2005 Maternal calcium and bone metabolism during lactation. Curr Opin Endocrinol Diabetes 12:477-482
3. Wysolmerski JJ 2010 Interactions between breast, bone, and brain regulate mineral and skeletal metabolism during lactation. Ann NY Acad Sci 1192:161-169
4. Ardeshirpour L, Dann P, Adams DJ, Nelson T, VanHouten J, Horowitz MC, Wysolmerski JJ 2007 Weaning triggers a decrease in receptor activator of nuclear factor-κB ligand expression, widespread osteoclast apoptosis, and rapid recovery of bone mass after lactation in mice. Endocrinology 148:3875-3886
5. Peng TC, Garner SC, Kusy RP, Hirsch PF 1988 Effect of number of suckling pups and dietary calcium on bone mineral content and mechanical properties of femurs of lactating rats. Bone Miner 3:293-304
6. Miller SC, Bowman BM 1998 Comparison of bone loss during normal lactation with estrogen deficiency osteopenia and immobilization osteopenia in the rat. Anat Rec 251:265-274
7. Miller SC, Halloran BP, DeLuca HF, Jee WS 1982 Role of vitamin D in maternal skeletal changes during pregnancy and lactation: a histomorphometric study. Calcif Tissue Int 34:245-252
8. Sowers M, Eyre D, Hollis BW, Randolph JF, Shapiro B, Jannausch ML, Crutchfield M 1995 Biochemical markers of bone turnover in lactating and nonlactating postpartum women. J Clin Endocrinol Metab 80:2210-2216
9. VanHouten JN, Wysolmerski JJ 2003 Low estrogen and high parathyroid hormone-related peptide levels contribute to accelerated bone resorption and bone loss in lactating mice. Endocrinology 144: 5521-5529
10. Bowman BM, Siska CC, Miller SC 2002 Greatly increased cancellous bone formation with rapid improvements in bone structure in the rat maternal skeleton after lactation. J Bone Miner Res 17:1954-1960
11. Karlsson C, Obrant KJ, Karlsson M 2001 Pregnancy and lactation confer reversible bone loss in humans. Osteoporos Int 12:828-834
12. Laskey MA, Prentice A 1999 Bone mineral changes during and after lactation. Obstet Gynecol 94:608-615
13. Miller SC, Bowman BM 2007 Rapid inactivation and apoptosis of osteoclasts in the maternal skeleton during the bone remodeling reversal at the end of lactation. Anat Rec (Hoboken) 290:65-73
14. McNeilly AS, Tay CC, Glasier A 1994 Physiological mechanisms underlying lactational amenorrhea. Ann NY Acad Sci 709:145-155
15. Smith MS, Grove KL 2002 Integration of the regulation of reproductive function and energy balance: lactation as a model. Front Neuroendocrinol 23:225-256
16. Xu J, Kirigiti MA, Cowley MA, Grove KL, Smith MS 2009 Suppression of basal spontaneous gonadotropin-releasing hormone neuronal activity during lactation: role of inhibitory effects of neuropeptide Y. Endocrinology 150:333-340
17. Xu J, Kirigiti MA, Grove KL, Smith MS 2009 Regulation of food intake and gonadotropin-releasing hormone/luteinizing hormone during lactation: role of insulin and leptin. Endocrinology 150:4231-4240
18. Riggs BL 2000 The mechanisms of estrogen regulation of bone resorption. J Clin Invest 106:1203-1204
19. Smith EP, Specker B, Korach KS 2010 Recent experimental and clinical findings in the skeleton associated with loss of estrogen hormone or estrogen receptor activity. J Steroid Biochem Mol Biol 118: 264-272
20. Sowers MF, Hollis BW, Shapiro B, Randolph J, Janney CA, Zhang D, Schork A, Crutchfield M, Stanczyk F, Russell-Aulet M 1996 Elevated parathyroid hormone-related peptide associated with lactation and bone density loss. JAMA 276:549-554
21. VanHouten JN, Dann P, Stewart AF, Watson CJ, Pollak M, Karaplis AC, Wysolmerski JJ 2003 Mammary-specific deletion of parathyroid hormone-related protein preserves bone mass during lactation. J Clin Invest 112:1429-1436 (Pubitemid 38057696)
22. Cosman F, Shen V, Xie F, Seibel M, Ratcliffe A, Lindsay R 1993 Estrogen protection against bone resorbing effects of parathyroid hormone infusion. Assessment by use of biochemical markers. Ann Intern Med 118:337-343
23. Grey AB, Stapleton JP, Evans MC, Tatnell MA, Reid IR 1996 Effect of hormone replacement therapy on bone mineral density in post-menopausal women with mild primary hyperparathyroidism. A randomized, controlled trial. Ann Intern Med 125:360-368 (Pubitemid 126449705)
24. Masiukiewicz US, Mitnick M, Grey AB, Insogna KL 2000 Estrogen modulates parathyroid hormone-induced interleukin-6 production in vivo and in vitro. Endocrinology 141:2526-2531 (Pubitemid 32269072)
25. Strewler GJ 2000 The physiology of parathyroid hormone-related protein. N Engl J Med 342:177-185
26. Plawner LL, Philbrick WM, Burtis WJ, Broadus AE, Stewart AF 1995 Cell type-specific secretion of parathyroid hormone-related protein via the regulated versus the constitutive secretory pathway. J Biol Chem 270:14078-14084
27. Garner C 1994 Uses of GnRH agonists. J Obstet Gynecol Neonatal Nurs 23:563-570
28. Frenkel B, Hong A, Baniwal SK, Coetzee GA, Ohlsson C, Khalid O, Gabet Y 2010 Regulation of adult bone turnover by sex steroids. J Cell Physiol 224:305-310
29. Nakamura T, Imai Y, Matsumoto T, Sato S, Takeuchi K, Igarashi K, Harada Y, Azuma Y, Krust A, Yamamoto Y, Nishina H, Takeda S, Takayanagi H, Metzger D, Kanno J, Takaoka K, Martin TJ, Chambon P, Kato S 2007 Estrogen prevents bone loss via estrogen receptor α and induction of Fas ligand in osteoclasts. Cell 130:811-823
30. Datta NS, Abou-Samra AB 2009 PTH and PTHrP signaling in osteoblasts. Cell Signal 21:1245-1254
31. Kurabayashi T, Fujimaki T, Yasuda M, Yamamoto Y, Tanaka K 1993 Time-course of vertebral and femoral bone loss in rats administered gonadotrophin-releasing hormone agonist. J Endocrinol 138:115-125
32. Sakamoto S, Sassa S, Mitamura T, Kudo H, Suzuki S, Yoshimura S, Zhou Y, Kikuchi T, Shinoda H 1999 Prevention of osteopenia induced with a gonadotropin-releasing hormone agonist in rats. Calcif Tissue Int 65:152-155
33. Wang Y, Yano T, Kikuchi A, Yano N, Matsumi H, Ando K, Kasai Y, Watanabe M, Okagaki R, Osuga Y, Taketani Y 2000 Comparison of the effects of add-back therapy with various natural oestrogens on bone metabolism in rats administered a long-acting gonadotrophin- releasing hormone agonist. J Endocrinol 165:467-473
34. Gilbert AN 1984 Postpartum and lactational estrus: a comparative analysis in rodentia. J Comp Psychol 98:232-245
35. Sun L, Peng Y, Sharrow AC, Iqbal J, Zhang Z, Papachristou DJ, Zaidi S, Zhu LL, Yaroslavskiy BB, Zhou H, Zallone A, Sairam MR, Kumar TR, Bo W, Braun J, Cardoso-Landa L, Schaffler MB, Moonga BS, Blair HC, Zaidi M 2006 FSH directly regulates bone mass. Cell 125:247-260
36. Iwaniec UT, Yuan D, Power RA, Wronski TJ 2006 Strain-dependent variations in the response of cancellous bone to ovariectomy in mice. J Bone Miner Res 21:1068-1074 (Pubitemid 43962835)
37. Adami S, Gatti D, Bertoldo F, Rossini M, Fratta-Pasini A, Zamberlan N, Facci E, Lo Cascio V 1992 The effects of menopause and estrogen replacement therapy on the renal handling of calcium. Osteoporos Int 2:180-185
38. Dick IM, Devine A, Beilby J, Prince RL 2005 Effects of endogenous estrogen on renal calcium and phosphate handling in elderlywomen. Am J Physiol Endocrinol Metab 288:E430-E435
39. Oz OK, Hajibeigi A, Howard K, Cummins CL, van Abel M, Bindels RJ, Word RA, Kuro-o M, Pak CY, Zerwekh JE 2007 Aromatase deficiency causes altered expression of molecules critical for calcium reabsorption in the kidneys of female mice. J Bone Miner Res 22: 1893-1902
40. Horwitz MJ, Tedesco MB, Sereika SM, Hollis BW, Garcia-Ocaña A, Stewart AF 2003 Direct comparison of sustained infusion of human parathyroid hormone-related protein-(1-36) [hPTHrP-(1- 36)] versus hPTH-(1-34) on serum calcium, plasma 1,25-dihydroxyvitamin D concentrations, and fractional calcium excretion in healthy human volunteers. J Clin Endocrinol Metab 88:1603-1609
41. Syed MA, Horwitz MJ, Tedesco MB, Garcia-Ocaña A, Wisniewski SR, Stewart AF 2001 Parathyroid hormone-related protein-(1-36) stimulates renal tubular calcium reabsorption in normal human volunteers: implications for the pathogenesis of humoral hypercalcemia of malignancy. J Clin Endocrinol Metab 86:1525-1531 (Pubitemid 32374898)
42. Lorget F, Kamel S, Mentaverri R, Wattel A, Naassila M, Maamer M, Brazier M 2000 High extracellular calcium concentrations directly stimulate osteoclast apoptosis. Biochem Biophys Res Commun 268: 899-903 (Pubitemid 30150888)
43. Mentaverri R, Yano S, Chattopadhyay N, Petit L, Kifor O, Kamel S, Terwilliger EF, Brazier M, Brown EM 2006 The calcium sensing receptor is directly involved in both osteoclast differentiation and apoptosis. FASEB J 20:2562-2564 (Pubitemid 44953781)
44. Fudge NJ, Kovacs CS 2004 Physiological studies in heterozygous calcium sensing receptor (CaSR) gene-ablated mice confirm that the CaSR regulates calcitonin release in vivo. BMC Physiol 4:5
45. Garrett JE, Tamir H, Kifor O, Simin RT, Rogers KV, Mithal A, Gagel RF, Brown EM 1995 Calcitonin-secreting cells of the thyroid express an extracellular calcium receptor gene. Endocrinology 136: 5202-5211
46. Woodrow JP, Sharpe CJ, Fudge NJ, Hoff AO, Gagel RF, Kovacs CS 2006 Calcitonin plays a critical role in regulating skeletal mineral metabolism during lactation. Endocrinology 147:4010-4021
47. Thiede MA 1989 Them RNA encoding a parathyroid hormone-like peptide is produced in mammary tissue in response to elevations in serum prolactin. Mol Endocrinol 3:1443-1447
48. Yamamoto M, Fisher JE, Thiede MA, Caulfield MP, Rosenblatt M, Duong LT 1992 Concentrations of parathyroid hormone-related protein in rat milk change with duration of lactation and interval from previous suckling, but not with milk calcium. Endocrinology 130:741-747
49. Markov AG 1991 [The duration of feedings and the intervals between them in mice during established lactation]. Fiziol Zh SSSR Im I M Sechenova 77:142-148
50. Speakman JR, Gidney A, Bett J, Mitchell IP, Johnson MS 2001 Limits to sustained energy intake. IV. Effect of variation in food quality on lactating mice Mus musculus. J Exp Biol 204:1957-1965
51. Zhao ZJ, Chi QS, Cao J 2010 Milk energy output during peak lactation in shaved Swiss mice. Physiol Behav 101:59-66
52. Laskey MA, Prentice A, Hanratty LA, Jarjou LM, Dibba B, Beavan SR, Cole TJ 1998 Bone changes after 3 mo of lactation: influence of calcium intake, breast-milk output, and vitamin D-receptor genotype. Am J Clin Nutr 67:685-692 (Pubitemid 28153170)
53. Burger HG, Hee JP, Mamers P, Bangah M, Zissimos M, McCloud PI 1994 Serum inhibin during lactation: relation to the gonadotrophins and gonadal steroids. Clin Endocrinol (Oxf) 41:771-777
54. Kremer JA, Schellekens LA, Segers MF, Thomas CM, Rolland R 1994 Circulating inhibin levels in lactating and nonlactating women. Fertil Steril 62:1150-1156 (Pubitemid 24369778)
55. Yohkaichiya T, O'Connor A, de Kretser DM 1991 Circulating immunoreactive inhibin, gonadotropin, and prolactin levels during pregnancy, lactation, and postweaning estrous cycle in the rat. Biol Reprod 44:6-12
56. Nicks KM, Fowler TW, Gaddy D 2010 Reproductive hormones and bone. Curr Osteoporos Rep 8:60-67
57. Elabd C, Basillais A, Beaupied H, Breuil V, Wagner N, Scheideler M, Zaragosi LE, Massiéra F, Lemichez E, Trajanoski Z, Carle G, Euller- Ziegler L, Ailhaud G, Benhamou CL, Dani C, Amri EZ 2008 Oxytocin controls differentiation of human mesenchymal stem cells and reverses osteoporosis. Stem Cells 26:2399-2407
58. Tamma R, Colaianni G, Zhu LL, DiBenedetto A, Greco G, Montemurro G, Patano N, Strippoli M, Vergari R, Mancini L, Colucci S, Grano M, Faccio R, Liu X, Li J, Usmani S, Bachar M, Bab I, Nishimori K, Young LJ, Buettner C, Iqbal J, Sun L, Zaidi M, Zallone A 2009 Oxytocin is an anabolic bone hormone. Proc Natl Acad Sci USA 106:7149-7154
59. Seriwatanachai D, Krishnamra N, van Leeuwen JP 2009 Evidence for direct effects of prolactin on human osteoblasts: Inhibition of cell growth and mineralization. J Cell Biochem 107:677-685
60. Seriwatanachai D, Thongchote K, Charoenphandhu N, Pandaranandaka J, Tudpor K, Teerapornpuntakit J, Suthiphongchai T, Krishnamra N 2008 Prolactin directly enhances bone turnover by raising osteoblast-expressed receptor activator of nuclear factor κB ligand/osteoprotegerin ratio. Bone 42:535-546
61. Takeda S, Karsenty G 2008 Molecular bases of the sympathetic regulation of bone mass. Bone 42:837-840
62. Wong IP, Zengin A, Herzog H, Baldock PA 2008 Central regulation of bone mass. Semin Cell Dev Biol 19:452-458
63. Zengin A, Zhang L, Herzog H, Baldock PA, Sainsbury A 2010 Neuropeptide Y and sex hormone interactions in humoral and neuronal regulation of bone and fat. Trends Endocrinol Metab 21:411-418
64. Chen P, Smith MS 2003 Suckling-induced activation of neuronal input to the dorsomedial nucleus of the hypothalamus: possible candidates for mediating the activation of DMH neuropeptide Y neurons during lactation. Brain Res 984:11-20 (Pubitemid 36976790)
65. Crowley WR, Ramoz G, Torto R, Keefe KA, Wang JJ, Kalra SP 2007 Neuroendocrine actions and regulation of hypothalamic neuropeptide Y during lactation. Peptides 28:447-452 (Pubitemid 46176253)
66. Baldock PA, Lee NJ, Driessler F, Lin S, Allison S, Stehrer B, Lin EJ, Zhang L, Enriquez RF, Wong IP, McDonald MM, During M, Pierroz DD, Slack K, Shi YC, Yulyaningsih E, Aljanova A, Little DG, Ferrari SL, Sainsbury A, Eisman JA, Herzog H 2009 Neuropeptide Y knockout mice reveal a central role of NPY in the coordination of bone mass to body weight. PLoS One 4:e8415
67. Baldock PA, Sainsbury A, Couzens M, Enriquez RF, Thomas GP, Gardiner EM, Herzog H 2002 Hypothalamic Y2 receptors regulate bone formation. J Clin Invest 109:915-921 (Pubitemid 34275112)
68. Gammie SC, Hasen NS, Awad TA, Auger AP, Jessen HM, Panksepp JB, Bronikowski AM 2005 Gene array profiling of large hypothalamic CNS regions in lactating and randomly cycling virgin mice. Brain Res Mol Brain Res 139:201-211