Гормональная регуляция остеогенеза



Cite item

Abstract

Введение. Эндокринная система занимает ведущее место не только в регуляции механизмов роста и развития, но и в компенсации при воздействии экстремальных факторов на организм. Скоординированная гормональная регуляция способствует правильному ответу различных приспособительных процессов макроорганизма, которые направлены на восстановление и поддержание гомеостаза. Каскад эндокринных изменений сопровождает процессы физиологической и репаративной регенерации костной ткани на всех ее стадиях. Цель исследования – определение механизмов гормональной регуляции физиологической и репаративной регенерации на современном этапе. Материал и методы. Поиск и анализ научных литературных источников проводился в электронных базах данных PubMed и eLIBRARY. Глубина поиска — 20 лет. Результаты. В обзоре рассмотрены как фундаментальные аспекты, так и новые данные основных гистогенетических механизмов гормональной регуляции остеогенеза. Выделены пути и точки взаимодействия эндокринной и костной систем, а также определены основные функции гормонов в участии костного ремоделирования на различных этапах развития макроорганизма. Заключение. В нарушениях физиологической регуляции гормональному дисбалансу во многом отводится ключевая роль, в то время как в условиях репаративного остеогенеза роль качественных и динамических изменений эндокринной системы изучены недостаточно. Гормональная регуляция репаративной регенерации до настоящего времени не имеет четких критериев оценки и требует дальнейшего исследования.

About the authors

ФГБОУ ВО "Читинская государственная медицинская академия" Минздрава России

Author for correspondence.
Email: miromanov_a@mail.ru
ORCID iD: 0000-0003-1432-1844

д.м.н., профессор, заведующий кафедрой травматологии и ортопедии

Russian Federation

ФГБОУ ВО "Читинская государственная медицинская академия" Минздрава России

Email: kirill.gusev.86@mail.ru
ORCID iD: 0000-0003-3375-9956

к.м.н., ассистент кафедры травматологии и ортопедии

Russian Federation

References

  1. Charmandari E., Tsigos C., Chrousos G. Endocrinology of the stress response. J Annu Rev Physiol. 2005;67:259–284. doi: 10.1146/annurev.physiol.67.040403.120816.
  2. Дедов И.И., Мельниченко Г.А. Эндокринология. Москва: ГЭОТАР-Медиа, 2019. 1112 с. ISBN 978-5-9704-5083-3.
  3. Dedov I.I., Melnichenko G.A. Endocrinology. Moscow: GEOTAR-Media, 2019.1112 p. ISBN 978-5-9704-5083-3 (In Russian).
  4. Nicholls J.J., Brassill N.J., Williams G.R., Bassett J.H.D. The skeletal consequences of thyrotoxicosis. J Endocrinol. 2012;213(3):209-221. doi: 10.1530/JOE-12-0059.
  5. Мироманов А.М., Гусев К.А., Мироманова Н.А., Витковский Ю.А. Полиморфизм гена EGFR-2073A>T и экспрессия ростового фактора EGF у больных с нарушением консолидации переломов длинных костей конечностей. Забайкальский медицинский вестник. 2016;3:25-29. Режим доступа: http://zabmedvestnik.ru/arhiv-nomerov/nomer-3-za-2016-god (дата обращения: 30.03.2021).
  6. Gusev K.A., Miromanov A.M., Miromanova N.A., Vitkovsky Yu.A. [Influence of polymorphism of gene EGFR-2073A>T on expression transforming growth factor EGF at patients with disturbance of consolidation of fractures of long bones of extremities]. Zabaykal'skiy meditsinskiy vestnik [The Transbaikalian Medical Bulletin]. 2016;3:25-29. Access mode: http://zabmedvestnik.ru/arhiv-nomerov/nomer-3-za-2016-god (date of the application: 30.03.2021) (In Russian).
  7. Корж Н.А., Дедух Н.В. Репаративная регенерация кости: современный взгляд на проблему. Стадии регенерации. Ортопедия, травматология и протезирование. 2006;1:77–84.
  8. Korzh N.A., Dedukh N.V. [Reparative bone regeneration: a modern perspective on the problem. Regeneration stages]. Ortopediia Travmatologiia i Protezirovanie [Orthopedics, traumatology and prosthetics]. 2006;1:77–84 (In Russian).
  9. Kawai M., De Paula F.J.A., Rosen C.J. New insights into osteoporosis: the bone-fat connection. J Intern Med. 2012;272(4):317–329. doi: 10.1111/j.1365-2796.2012.02564.x
  10. Mak W., Shao X., Dunstan C.R., Seibel M.J., Zhou H. Biphasic glucocorticoid-dependent regulation of Wnt expression and its inhibitors in mature osteoblastic cells. Calcif Tissue Int. 2009;85(6):538-545. doi: 10.1007/s00223-009-9303-1.
  11. Hartmann K., Koenen M., Schauer S., Wittig-Blaich S., Ahmad M., Baschant U., Tuckermann J.P. Molecular Actions of Glucocorticoids in Cartilage and Bone During Health, Disease, and Steroid Therapy. Physiol Rev. 2016;96(2):409-447. doi: 10.1152/physrev.00011.2015.
  12. Weinstein R.S., Hogan E.A., Borrelli M.J., Liachenko S., O'Brien C.A., Manolagas S.C. The Pathophysiological Sequence of Glucocorticoid-Induced Osteonecrosis of the Femoral Head in Male Mice. Endocrinology. 2017;158(11):3817-3831. doi: 10.1210/en.2017-00662.
  13. Tu J., Henneicke H., Zhang Y., Stoner S., Cheng T.L., Schindeler A. et all. Disruption of glucocorticoid signaling in chondrocytes delays metaphyseal fracture healing but does not affect normal cartilage and bone, development. Bone. 2014;69:12-22. doi: 10.1016/j.bone.2014.08.016.
  14. Rapp A.E., Hachemi Y., Kemmler J., Koenen M., Tuckermann J., Ignatius A. Induced global deletion of glucocorticoid receptor impairs fracture healing. FASEB J. 2018;32(4):2235-2245. doi: 10.1096/fj.201700459RR.
  15. Jilka R.L. Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone. 2007;40:1434–1446. doi: 10.1016/j.bone.2007.03.017.
  16. Kim J.-M., Choi J.S., Kim Y.-H., Jin S.H., Lim S., Jang H.-J. et all. An activator of the cAMP/PKA/CREB pathway promotes osteogenesis from human mesenchymal stem cells. J Cell Physiol. 2013;228(3):617-626. doi: 10.1002/jcp.24171.
  17. Kousteni S., Bilezikian J.P. The cell biology of parathyroid hormone in osteoblasts. Curr Osteoporos Rep. 2008;6(2):72–76. doi: 10.1007/s11914-008-0013-9.
  18. Yu B., Zhao X., Yang C., Crane J., Xian L., Lu W. et al. Parathyroid hormone induces differentiation of mesenchymal stromal/stem cells by enhancing bone morphogenetic protein signaling. J Bone Miner Res. 2012;27(9):2001–2014. doi: 10.1002/jbmr.1663.
  19. Teitelbaum S.L. Bone resorption by osteoclasts. Science. 2000;289(5484):1504–1508. doi: 10.1126/science.289.5484.1504.
  20. Chiavistelli S., Giustina A., Mazziotti G. Parathyroid hormone pulsatility: physiological and clinical aspects. Bone Res. 2015;3:14049. doi: 10.1038/boneres.2014.49.
  21. Parisien M., Silverberg S.J., Shane E., de la Cruz L., Lindsay R., Bilezikian J.P., Dempster D.W. The histomorphometry of bone in primary hyperparathyroidism: preservation of cancellous bone structure. J Clin Endocrinol Metab. 1990;70(4):930–938. doi: 10.1210/jcem-70-4-930.
  22. Wojda S.J., Donahue S.W. Parathyroid hormone for bone regeneration. J. Orthop. Res. 2018;36(10):2586-2594. doi: 10.1002/jor.24075.
  23. Hirsch P.F., Lester G.E., Talmage R.V. Calcitonin, an enigmatic hormone: does it have a function? J Musculoskelet Neuronal Interact. 2001;1(4):299-305.
  24. Keller J., Catala-Lehnen P., Huebner A.K., Jeschke A., Heckt T., Lueth A. et all. Calcitonin controls bone formation by inhibiting the release of sphingosine 1-phosphate from osteoclasts. Nat Commun. 2014;5:5215. doi: 10.1038/ncomms6215.
  25. Davies J. Procalcitonin. J Clin Pathol. 2015;68(9):675–679. doi: 10.1136/jclinpath-2014-202807.
  26. Vijayan A.L., Vanimaya, Ravindran S., Saikant R., Lakshmi S., Kartik R., Manoj G. Procalcitonin: a promising diagnostic marker for sepsis and antibiotic therapy. J Intensive Care. 2017;5:51. doi: 10.1186/s40560-017-0246-8.
  27. Shen C.-J., Wu M.-S., Lin K.-H., Lin W.-L., Chen H.-C., Wu J.-Y., Lee M.C.-H., Lee C.-C. The use of procalcitonin in the diagnosis of bone and joint infection: a systemic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2013;32(6):807–814. doi: 10.1007/s10096-012-1812-6.
  28. Khosla S. Update on estrogens and the skeleton. J Clin Endocrinol Metab. 2010;95(8):3569–3577. doi: 10.1210/jc.2010-0856.
  29. Vanderschueren D., Laurent M.R., Claessens F., Gielen E., Lagerquist M.K., Vandenput L., Borjesson A.E., Ohlsson C. Sex steroid actions in male bone. Endocr Rev. 2014;35(6):906–960. doi: 10.1210/er.2014-1024.
  30. Khosla S., Melton L.J. 3rd, Riggs B.L. The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone Miner Res. 2011;26(3):441-451. doi: 10.1002/jbmr.262.
  31. Khosla S., Amin S., Orwoll E. Osteoporosis in men. Endocr Rev. 2008;29(4):441-464. doi: 10.1210/er.2008-0002.
  32. Falahati-Nini A., Riggs B.L., Atkinson E.J., O'Fallon W.M., Eastell R., Khosla S. Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J Clin Invest. 2000;106(12):1553-1560. doi: 10.1172/JCI10942.
  33. Manolagas S.C. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000;21(2):115-137. doi: 10.1210/edrv.21.2.0395.
  34. Riggs B.L. The mechanisms of estrogen regulation of bone resorption. J Clin Investig. 2000;106(10):1203–1204. doi: 10.1172/JCI11468.
  35. Cenci S., Weitzmann M.N., Roggia C., Namba N., Novack D., Woodring J., Pacifici R. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest. 2000;106(10):1229-1237. doi: 10.1172/JCI11066.
  36. Hofbauer L.C., Khosla S., Dunstan C.R., Lacey D.L., Boyle W.J., Riggs B.L. The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J Bone Miner Res. 2000;15(1):2-12. doi: 0.1359/jbmr.2000.15.1.2.
  37. Pacifici R. Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J Bone Miner Res. 1996;11(8):1043-1051. doi: 10.1002/jbmr.5650110802.
  38. Riggs B.L. The mechanisms of estrogen regulation of bone resorption. J Clin Invest. 2000;106(10):1203–1204. doi: 10.1172/JCI11468.
  39. Hadji P., Colli E., Regidor P.-A. Bone health in estrogen-free contraception. Osteoporos Int. 2019;30(12):2391–2400. doi: 10.1007/s00198-019-05103-6.
  40. Berger C., Goltzman D., Langsetmo L., Joseph L., Jackson S., Kreiger N. et all. Peak bone mass from longitudinal data: implications for the prevalence, pathophysiology, and diagnosis of osteoporosis. J Bone Miner Res. 2010;25(9):1948–1957. doi: 10.1002/jbmr.95.
  41. Kerrigan J.R., Rogol A.D. The impact of gonadal steroid hormone action on growth hormone secretion during childhood and adolescence. Endocr Rev. 1992;13(2):281-298. doi: 10.1210/edrv-13-2-281.
  42. Clarke B.L., Khosla S. Androgens and Bone. Steroids. 2009;74(3):296–305. doi: 10.1016/j.steroids.2008.10.003.
  43. Hofbauer L.C., Hicok K.C., Khosla S. Effects of gonadal and adrenal androgens in a novel androgen-responsive human osteoblastic cell line. J Cell Biochem. 1998;71(1):96-108.
  44. Hofbauer L.C., Hicok K.C., Chen D., Khosla S. Regulation of osteoprotegerin production by androgens and anti-androgens in human osteoblastic lineage cells. Eur J Endocrinol. 2002;147(2):269-273. doi: 10.1530/eje.0.1470269.
  45. Suda T., Takahashi N., Udagawa N., Jimi E., Gillespie M.T., Martin T.J. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand 3families. Endocr Rev. 1999;20(3):345-357. doi: 10.1210/edrv.20.3.0367.
  46. Veldhuis J.D., Bowers C.Y. Human GH pulsatility: an ensemble property regulated by age and gender. J Endocrinol Invest. 2003;26(9):799-813. doi: 10.1007/BF03345229.
  47. Wang J., Zhou J., Cheng C.M., Kopchick J.J., Bondy C.A. Evidence supporting dual, IGF-I-independent and IGF-I-dependent, roles for GH in promoting longitudinal bone growth. J Endocrinol. 2004;180(2):247-255. doi: 10.1677/joe.0.1800247.
  48. Lindsey R.C., Mohan S. Skeletal Effects of Growth Hormone and Insulin-like Growth Factor-I Therapy. Mol Cell Endocrinol. 2016;432:44–55. doi: 10.1016/j.mce.2015.09.017.
  49. Locatelli V., Bianchi V.E. Effect of GH/IGF-1 on Bone Metabolism and Osteoporsosis. Int J Endocrinol. 2014;2014:235060. doi: 10.1155/2014/235060.
  50. Yakar S., Courtland H.-W., Clemmons D. IGF-1 and bone: New discoveries from mouse models. J Bone Miner Res. 2010;25(12):2543-2552. doi: 10.1002/jbmr.234.
  51. Singhal V., Goh B.C., Bouxsein M.L., Faugere M.-C., DiGirolamo D.J. Osteoblast-restricted Disruption of the Growth Hormone Receptor in Mice Results in Sexually Dimorphic Skeletal Phenotypes. Bone Res. 2013;1(1):85-97. doi: 10.4248/BR201301006.
  52. Wu S., Yang W., De Luca F. Insulin-Like Growth Factor-Independent Effects of Growth Hormone on Growth Plate Chondrogenesis and Longitudinal Bone Growth. Endocrinology. 2015;156(7):2541-2551. doi: 10.1210/en.2014-1983.
  53. Zhang M., Faugere M.-C., Malluche H., Rosen C.J., Chernausek S.D., Clemens T.L. Paracrine overexpression of IGFBP-4 in osteoblasts of transgenic mice decreases bone turnover and causes global growth retardation. J Bone Miner Res. 2003;18(5):836-843. doi: 10.1359/jbmr.2003.18.5.836.
  54. Honda Y., Landale E.C., Strong D.D., Baylink D.J., Mohan S. Recombinant synthesis of insulin-like growth factor-binding protein-4 (IGFBP-4): Development, validation, and application of a radioimmunoassay for IGFBP-4 in human serum and other biological fluids. J Clin Endocrinol Metab. 1996;81(4):1389-1396. doi: 10.1210/jcem.81.4.8636339.
  55. Chevalley T., Strong D.D., Mohan S., Baylink D., Linkhart T.A. Evidence for a role for insulin-like growth factor binding proteins in glucocorticoid inhibition of normal human osteoblast-like cell proliferation. Eur J Endocrinol. 1996;134(5):591-601. doi: 10.1530/eje.0.1340591.
  56. Gabbitas B., Canalis E. Cortisol enhances the transcription of insulin-like growth factor-binding protein-6 in cultured osteoblasts. Endocrinology. 1996;137(5):1687-92. doi: 10.1210/endo.137.5.8612502.
  57. Denger S., Bähr-Ivacevic T., Brand H., Reid G., Blake J., Seifert M. et all. Transcriptome profiling of estrogen-regulated genes in human primary osteoblasts reveals an osteoblast-specific regulation of the insulin-like growth factor binding protein 4 gene. Mol Endocrinol. 2008;22(2):361-379. doi: 10.1210/me.2007-0292.
  58. Qin X., Wergedal J.E., Rehage M., Tran K., Newton J., Lam P., Baylink D.J., Mohan S. Pregnancy-associated plasma protein-A increases osteoblast proliferation in vitro and bone formation in vivo. Endocrinology. 2006;147(12):5653-5661. doi: 10.1210/en.2006-1055.
  59. Christians J.K., de Zwaan D.R., Fung S.H.Y. Pregnancy associated plasma protein A2 (PAPP-A2) affects bone size and shape and contributes to natural variation in postnatal growth in mice. PLoS One. 2013;8(2):e56260. doi: 10.1371/journal.pone.0056260.
  60. Mohan S., Bautista C.M., Wergedal J., Baylink D.J. Isolation of an inhibitory insulin-like growth factor (IGF) binding protein from bone cell-conditioned medium: a potential local regulator of IGF action. Proc Natl Acad Sci USA. 1989;86(21):8338-8342. doi: 10.1073/pnas.86.21.8338.
  61. Devlin R.D., Du Z., Buccilli V., Jorgetti V., Canalis E. Transgenic mice overexpressing insulin-like growth factor binding protein-5 display transiently decreased osteoblastic function and osteopenia. Endocrinology. 2002;143(10):3955-3962. doi: 10.1210/en.2002-220129.
  62. Zhao G., Monier-Faugere M.C., Langub M.C., Geng Z., Nakayama T., Pike J.W. et all. Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: increased trabecular bone volume without increased osteoblast proliferation. Endocrinology. 2000;141(7):2674-82. doi: 10.1210/endo.141.7.7585.
  63. DiGirolamo D.J., Mukherjee A., Fulzele K., Gan Y., Cao X., Frank S.J., Clemens T.L. Mode of growth hormone action in osteoblasts. J Biol Chem. 2007;282(43):31666-31674. doi: 10.1074/jbc.M705219200.
  64. Simpson H., Savine R., Sönksen P., Bengtsson B.A., Carlsson L., Christiansen J.S. et all. Growth hormone replacement therapy for adults: into the new millennium. Growth Horm IGF Res. 2002;12(1):1-33. doi: 10.1054/ghir.2001.0263.
  65. Laron Z., Kauli R. Fifty seven years of follow-up of the Israeli cohort of Laron Syndrome patients-From discovery to treatment. Growth Horm IGF Res. 2016;28:53-56. doi: 10.1016/j.ghir.2015.08.004.
  66. Bikle D., Majumdar S., Laib A., Powell-Braxton L., Rosen C., Beamer W. et all. The skeletal structure of insulin-like growth factor I-deficient mice. J Bone Miner Res. 2001;16(12):2320-2329. doi: 10.1359/jbmr.2001.16.12.2320.
  67. Zhang W., Zhang L.C., Chen H., Tang P.F., Zhang L.H. Association between polymorphisms in insulin-like growth factor-1 and risk of osteoporosis. Genet Mol Res. 2015;14(3):7655-7660. doi: 10.4238/2015.July.13.10.
  68. Thomas J.D.J., Monson J.P. Adult GH deficiency throughout lifetime. Eur J Endocrinol. 2009;161(1):S97-S106. doi: 10.1530/EJE-09-0258.
  69. Claessen K.M., Kroon H.M., Pereira A.M., Appelman-Dijkstra N.M., Verstegen M.J., Kloppenburg M. et all. Progression of vertebral fractures despite long-term biochemical control of acromegaly: a prospective follow-up study. J Clin Endocrinol Metab. 2013;98(12):4808-4815. doi: 10.1210/jc.2013-2695.
  70. Mazziotti G., Bianchi A., Porcelli T., Mormando M., Maffezzoni F., Cristiano A. et all. Vertebral fractures in patients with acromegaly: a 3-year prospective study. J Clin Endocrinol Metab. 2013;98(8):3402-3410. doi: 10.1210/jc.2013-1460.
  71. Mormando M., Nasto L.A., Bianchi A., Mazziotti G., Giampietro A., Pola E. et all. GH receptor isoforms and skeletal fragility in acromegaly. Eur J Endocrinol. 2014;171(2):237-245. doi: 10.1530/EJE-14-0205.
  72. Nicholls J.J., Brassill M.J., Williams G.R., Bassett J.H. The skeletal consequences of thyrotoxicosis. J Endocrinol. 2012;213(3):209-221. doi: 10.1530/JOE-12-0059.
  73. Gorka J., Taylor-Gjevre R.M., Arnason T. Metabolic and clinical consequences of hyperthyroidism on bone density. Int J Endocrinol. 2013;2013:638727. doi: 10.1155/2013/638727.
  74. Harvey C.B., Bassett J.H., Maruvada P., Yen P.M., Williams G.R. The rat thyroid hormone receptor (TR) Deltabeta3 displays cell-, TR isoform-, and thyroid hormone response element-specific actions. Endocrinology. 2007;148(4):1764-1773. doi: 10.1210/en.2006-1248.
  75. Gouveia C. The molecular and structural effects of thyroid hormone in bones. Arq Bras Endocrinol Metab. 2004;48(1):183-195.
  76. Wexler J.A., Sharretts J. Thyroid and bone. Endocrinol Metab Clin North Am. 2007;36(3):673-705. doi: 10.1016/j.ecl.2007.04.005.
  77. O’Shea P., Harvey C., Suzuki H., Kaneshige M., Kaneshige K., Cheng S., Williams G. A thyrotoxic skeletal phenotype of advanced bone formation in mice with resistance to thyroid hormone. Mol Endocrinol. 2005;19:3045–3059. doi: 10.1210/me.2005-0224.
  78. Bassett J.H., Williams G.R. The skeletal phenotypes of TRalpha and TRbeta mutant mice. J Mol Endocrinol. 2009;42(4):269-282. doi: 10.1677/JME-08-0142.
  79. Harvey C.B., O'Shea P.J., Scott A.J., Robson H., Siebler T., Shalet S.M. et all. Molecular mechanisms of thyroid hormone effects on bone growth and function. Genet Mol Metab. 2002;75(1):17-30. doi: 10.1006/mgme.2001.3268.
  80. Bassett J.H., Williams G.R. The molecular actions of thyroid hormone in bone. Trends Endocrinol Metab. 2003;14(8):356-364. doi: 10.1016/s1043-2760(03)00144-9.
  81. Gauthier K., Plateroti M., Harvey C.B., Williams G.R., Weiss R.E., Refetoff S. et all. Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus. Mol Cell Biol. 2001;21(14):4748-4760. doi: 10.1128/MCB.21.14.4748-4760.2001.
  82. Gu W.X., Stern P.H., Madison L.D., Du G.G. Mutual up-regulation of thyroid hormone and parathyroid hormone receptors in rat osteoblastic osteosarcoma 17/2.8 cells. Endocrinology. 2001;142(1):157-164. doi: 10.1210/endo.142.1.7905.
  83. Gruber R., Czerwenka K., Wolf F., Ho G.M., Willheim M., Peterlik M. Expression of vitamin D receptor, of estrogen and thyroid hormone receptor alpha- and beta-isoforms, and the androgen receptor in cultures of native mouse bone marrow and of stromal/osteoblastic cells. Bone. 1999;24:465-473. doi: 10.1016/s8756-3282(99)00017-4.
  84. Basset J., Williams G. Critical role of the hypothalamic-pituitary-thyroid axis in bone. Bone. 2008;43:418–426. doi: 10.1016/j.bone.2008.05.007.
  85. Bassett J., Williams G. Role of Thyroid Hormones in Skeletal Development and Bone Maintenance. Endocrine Reviews. 2016;37(2):135–187. doi: 10.1210/er.2015-1106.
  86. Kosińska A., Syrenicz A., Kosiński B., Garanty-Bogacka B., Syrenicz M., Gromiak E. Osteoporosis in thyroid diseases. Endokrynol Pol. 2005;2:185–193.
  87. Hypponen E., Laara E., Reunanen A., Jarvelin M., Pouta A. Intake of vitamin D and risk of type 1 diabetes: a birth-cohort study. Lancet. 2001;358:1500–1503. doi: 10.1016/S0140-6736(01)06580-1.
  88. Reddy P., Harinarayan C., Sachan A., Suresh V., Rajagopal G. Bone disease in thyrotoxicosis. Indian J Med Res. 2012;135:277–286.
  89. Abe E., Marians R., Yu W., Wu X., Ando T., Li Y. et all. TSH is a negative regulator of skeletal remodelling. Cell. 2003;115(2):151–162. doi: 10.1016/S0092-8674(03)00771-2.
  90. Tsai J., Janson A., Bucht E., Kindmark H., Marcus C., Stark A., Zemack H., Torring O. Weak evidence of thyrotropin receptors in primary cultures of human osteoblast-like cells. Calcif Tissue Int. 2004;74(5):486–491. doi: 10.1007/s00223-003-0108-3.
  91. Vestergaard P., Rejnmark L., Mosekilde L. Influence of hyper- and hypothyroidism, and the effects of treatment with antithyroid drugs and levothyroxine on fracture risk. Calcif Tissue Int. 2005;77:139–144. doi: 10.1007/s00223-005-0068-x.
  92. Gonzalez-Rodriguez L., Felici-Giovanini M., Haddock L. Thyroid Dysfunction in an Adult Population: a population-based study of Latin American Vertebral Osteoporosis Study (LAVOS) – Puerto Rico Site Hypothyroidism in LAVOS-Puerto Rico site. Health Sci. 2013;32(2):57–62.
  93. Clement-Lacroix P., Ormandy C., Lepescheux L., Ammann P., Damotte D., Goffin V. et all. Osteoblasts are a new target for prolactin: analysis of bone formation in prolactin receptor knockout mice. Endocrinology. 1999;140(1):96-105. doi: 10.1210/endo.140.1.6436.
  94. Charoenphandhu N., Tudpor K., Thongchote K., Saengamnart W., Puntheeranurak S., Krishnamara N. High-calcium diet modulates effects of long-term prolactin exposure on the cortical bone calcium content in ovariectomized rats. Am. J. Physiol: Endocrinol. Metab. 2007;292(2):E443-452. doi: 10.1152/ajpendo.00333.2006.
  95. Holt E., Lupsa B., Lee G., Bassyouni H., Peery H.E. Goodman's Basic Medical Endocrinology, 5rd edn. Elsevier, 2021. 552 p. ISBN: 9780128158449
  96. Momsen G., Schwarz P. A mathematical/physiological model of parathyroid hormone secretion in response to blood-ionized calcium lowering in vivo. Scand J Clin Lab Invest. 1997;57(5):381-394. doi: 10.3109/00365519709084585.
  97. Krishnamra N., Seemoung J. Effects of acute and long-term administration of prolactin on bone 45Ca uptake, calcium deposit, and calcium resorption in weaned, young, and mature rats. Can J Physiol Pharmacol. 1996;74(10):1157–1165.
  98. Thongchote K., Charoenphandhu N., Krishnamra N. High physiological prolactin induced by pituitary transplantation decreases BMD and BMC in the femoral metaphysis, but not in the diaphysis of adult female rats. J Physiol Sci. 2008;58(1):39–45. doi: 10.2170/physiolsci.RP015007.
  99. Mazziotti G., Frara S., Giustina A. Pituitary Diseases and Bone. Endocrine Reviews. 2018;39(4):440–488 doi: 10.1210/er.2018-00005.
  100. Wildburger R., Zarkovic N., Tonkovic G., Skoric T., Frech S., Hartleb M. et al. Post-traumatic hormonal disturbances: prolactin as a link between head injury and enhanced osteogenesis. J Endocrinol Invest. 1998;21(2):78–86. doi: 10.1007/BF03350319.

Supplementary files

There are no supplementary files to display.


Copyright (c)



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies