HIERARCHICALLY ORGANIZED MODEL OF INTERCONNECTED CELLULAR AND TISSUE MECHANISMS OF CALCIUM EXCHANGE BETWEEN BONE AND BLOOD



Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

The objective of this study was to propose, on the basis of the results of authors’ own research and literature data, the hierarchically organized model of the interrelation of morphological mechanisms with the participation of biochemical bases of Са 2+ exchange between bone and blood. It is shown that osteocytes control the activity of main known mechanism of skeleton architecture remodeling (osteoclast-osteoblast remodeling, modeling, osteocyte remodeling etc.), that is the destruction and formation of mineral matrix component, thus influencing calcium turnover between bone and blood. The hierarchical organization of the mechanisms of this exchange is established. The first level of Са 2+ metabolism corresponds to the borderline between bone and takes place without bone matrix disintegration by paracellular energy-free Са 2+ diffusion from blood to bone and transcellular energy-dependent Са 2+ transfer from bone to blood. At the second level, calcium exchanger takes place at the borderline between between bone matrix and extracellular fluid by osteocyte remodeling during resorption or formation of the matrix of lacunar-canalicular system walls. The third level includes the mechanisms of osteoclast-osteoblast remodeling acting at the borderline between bone and blood. The mass of rapidly exchanging calcium pool was calculated to reach 58,5 g, thus being 11 times higher than previously suggected.

Full Text

Restricted Access

About the authors

A. S. Avrunin

R. R. Vreden Scientific Research Institute of Traumatology and Orthopedics

Email: a_avrunin@mail.ru

L. K. Parshin

St. Petersburg State Polytechnical University

Email: kafedra@ksm.spbstu.ru

References

  1. Аврунин А. С. и Тихилов Р. М. Остеоцитарное ремоделирование костной ткани: история вопроса, морфологические маркеры. Морфология, 2011, т. 139, вып. 1, с. 86–94.
  2. Аврунин А. С., Тихилов Р. М., Аболин А. Б. и Щербак И. Г. Уровни организации минерального матрикса костной ткани и механизмы, определяющие параметры их формирования (аналитический обзор). Морфология, 2005, т. 127, вып. 2, с. 78–82.
  3. Аврунин А. С., Тихилов Р. М. и Шубняков И. И. Медицинские и околомедицинские причины высокого внимания общества к проблеме потери костной массы. Анализ динамики и структуры публикаций по остеопорозу. Гений ортопедии, 2009, № 3, с. 59–66.
  4. Аврунин А. С., Тихилов Р. М., Шубняков И. И. и др. Критический анализ теории механостата. Часть I. Механизмы реорганизации архитектуры скелета. Травматол. ортопед. России, 2012, № 2, с. 105–115.
  5. Берталанфи Л. Общая теория систем — критический обзор. В кн.: Исследования по общей теории систем. М., Прогресс, 1969, с. 23–82.
  6. Данильченко С. Н. Структура и свойства апатитов кальция с точки зрения биоминералогии и биоматериаловедения. Вісн. СумДУ. Серія фізика, математика, механіка, 2007, № 2, с. 33–59.
  7. Корнилов Н. В. и Аврунин А. С. Адаптационные процессы в органах скелета. СПб., МОРСАР АВ, 2001.
  8. Ньюмен У. и Ньюмен М. Минеральный обмен кости. М., Издво иностр. лит-ры, 1961.
  9. Эшби У. Р. Конструкция мозга. М., Мир, 1962.
  10. Aarden E. M., Wassenaar A. M., Alblas M. J. and Nijweide P. J. Immunocytochemical demonstration of extracellular matrix proteins in isolated osteocytes. Histochem. Cell Biol., 1996, v. 106, p. 495–501.
  11. Adachi T., Aonuma Y., Ito S. et al. Osteocyte calcium signaling response to bone matrix deformation. J. Biomech., 2009, v. 42, p. 2507–2512.
  12. Adachi T., Aonuma Y., Taira K. et al. Asymmetric intercellular communication between bone cells: propagation of the calcium signaling. Biochem. Biophys. Res. Commun., 2009, v. 389, p. 495–500.
  13. Adachi T., Aonuma Y., Tanaka M. et al. Calcium response in single osteocytes to locally applied mechanical stimulus: Differences in cell process and cell body. J. Biomech., 2009, v. 42, p. 1989– 1995.
  14. Addison W. N., Nakano Y., Loisel T. et al. MEPE-ASARM peptides control extracellular matrix mineralization by binding to hydroxyapatite: an inhibition regulated by phex cleavage of as arm. J. Bone Miner. Res., 2008, v. 23, № 10, p. 1638–1649.
  15. Ajubi N. E., Klein-Nulend J., Nijweide P. J. et al. Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes-A cytoskeleton-dependent process. Biochem. Biophys. Res. Commun., 1996, v. 225, № 1131, p. 62–68.
  16. Amir L. R., Jovanovic A., Perdijk F. B. et al. Immunolocalization of sibling and RUNX2 proteins during vertical distraction osteogenesis in the human mandible. J. Histochem. Cytochem., 2007, v. 55, № 11б p. 1095–1104.
  17. Anderson E. J. and Knothe Tate M. L. Idealization of pericellular fluid space geometry and dimension results in a profound under-prediction of nano-microscale stresses imparted by fluid drag on osteocytes. J. Biomech., 2008, v. 41, p. 1736–1746.
  18. Arnold J. S., Jee W. S. S. and Johnson K. Observations and quantitative radioautographic studies of calcium48 deposited in vivo in forming haveesian systems and old bone of rabbit. Am. J. Anat., 1956, v. 99, № 2, p. 291–313.
  19. Ascenzi A., Bonucci E. and Bocciarelli D. S. An electron microscope stud on primary periosteal bone. J. Ultrastr. Res., 1967, v. 18, p. 605–618.
  20. Aubert J.-P., Bronner F. and Richelle L. J. Quantitation of calcium metabolism. Theory. J. Clin. Invest., 1963, v. 42, № 6, p. 885–897.
  21. Baron R. Molecular mechanisms of bone resorption. Acta Orthop. Scand., 1995, v. 66, Suppl. 266, p. 66–70.
  22. Baud C. A. Morphologie et structure inframicroscopique des osteocytes. Acta anat., 1962. v. 51, № 3. p. 209–225.
  23. Baud C. A. Submicroscopic structure and functional aspects of the osteocyte. Clin. Orthop., 1968, № 56, p. 227–236.
  24. Baud C. A. and Auil E. Osteocyte differential count in normal human alveolar bone. Acta Anat., 1971, v. 78, p. 321–327.
  25. Belanger L. F. and Robichon J. Parathormone-induced osteolysis in dogs. A Microradiographic and alpharadiographic survey. J. Bone Joint Surg. Am., 1964, v. 46, p.1008–1012.
  26. Berger C. E. M., Rathod H., Gillespie J. I. et al. Scanning electr ochemical microscopy at the surface of bone-resorbing osteoclasts: evidence for steady-state disposal and intracellular functional compartmentalization of calcium. J. Bone Miner. Res., 2001, v. 16, № 11, p. 2092–2102.
  27. Bershadsky A. D., Balaban N. Q. and Geiger B. Adhesion-dependent cell mechanosensittvity. Annu. Rev. Cell Dev. Biol., 2003, v. 19, p. 677–995.
  28. Bonewald L. F. Establishment and characterization of an osteocyte-like cell line, MLO-Y4. J. Bone Miner. Metab., 1999, v. 17, p 61–65.
  29. Bonewald L. F. Osteocytes: A proposed multifunctional bone cell. J. Musculoskelet Neuronal Interact., 2002, v. 2, № 3, p. 239–241.
  30. Bonewald L. F. Osteocyte biology: Its implications for osteoporosis. J. Musculoskelet Neuronal Interact., 2004, v. 4, № 1, p. 101–104.
  31. Bonewald L. F. Generation and function of osteocyte dendritic processes. J. Musculoskelet Neuronal Interact., 2005, v. 5, № 4, p. 321–324.
  32. Bonewald L. F. Osteocytes and mechanotransduction. J. Musculoskelet Neuronal Interact., 2005, v. 5, № 4, p. 333–334.
  33. Bonewald L. F. The amazing osteocyte. J. Bone Miner. Res., 2011, v. 26, № 2, p. 229–238.
  34. Bonewald L. F. and Johnson M. L. Osteocytes, mechanosensing and Wnt signaling. Bone, 2008, v. 42, p. 606–615.
  35. Bordat C., Guerquin-Kern J.-L., Lieberherr M. and Cournot G. Direct visualization of intracellular calcium in rat osteoblasts by energy-filtering transmission electron microscopy. Histochem. Cell Biol., 2004, v. 121, p. 31–38.
  36. Borle A. B., Nichols N. and Nichols G. Metabolic studies of bone in vitro II. The metabolic patterns of accretion and resorption. J. Biol. Chem., 1960, v. 235, № 4, p. 1211–1214.
  37. Borle A. B., Nichols N. and Nichols G. Metabolic studies of bone in vitro I. Normal bone. J. Biol. Chem., 1960, v. 235, № 4, p. 1226–1230.
  38. Bretscher A., Edwards K. and Fehon R. G. ERM proteins and merlin: integrators at the cell cortex. Mol. Cell Biol., 2002, v. 3, p. 586–599.
  39. Brighton C. T., Fisher J. R. S., Levine S. E. et al. The biochemical pathway mediating the proliferative response of bone cells to a mechanical stimulus. J. Bone Joint Surg. Am., 1996, v. 78, № 9, p. 1337–1347.
  40. Bronner F. and Aubert J.-P. Bone metabolism and regulation of the blood calcium level in rats. Am. J. Physiol., 1965, v. 209, № 5, p. 887–890.
  41. Bronner F., Harris R. S., Maletskos C. J. and Benda C. E. Studies in calcium metabolism. The fate of intravenously injected radio-calcium in human beings. J. Clin. Jnvest., 1956, v. 35, p. 78–88.
  42. Bronner F. and Lemaike R. Comparison of calcium kinetics in man and the rat. Calcit. Tissue Res., 1969, v. 3, p. 238–248.
  43. Bronner F., Richellef L. J., Saville P. D. et al. Quantitation of calcium metabolism in postmenopausal osteoporosis and in scoliosis. J. Clin. Invest., 1963. v. 42, № 6, p. 898–905.
  44. Cooper R. R., Milgram J. W. and Robinson R. A. Morphology of the osteon. J. Bone Joint Surg. Am., 1966, v. 48, № 7, p. 1239– 1271.
  45. Feng J. Q., Ward L. M., Liu S. et al. Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat. Genet., 2006, v. 38, № 11, p. 1310–1315.
  46. Feng J. Q., Ye L. and Schiavi S. Do osteocytes contribute to phosphate homeostasis? Curr. Opin. Nephrol. Hypertens., 2009, v. 18 p. 285–291.
  47. Franz-Odendaal T. A., Hall B. K. and Witten P. E. Buried alive: how osteoblasts become osteocytes. Dev. Dyn., 2006, v. 235, № 1, p. 176–190.
  48. Frost H. M. Micropetrosis. J. Bone Joint Surg. Am., 1960, v. 42, № 1, p. 144–150.
  49. Goulet G. C., Cooper D. M. L., Coombe D. and Zernicke R. F. Influence of cortical canal architecture on lacunocanalicular pore pressure and fluid flow. Comput. Methods Biomech. Biomed. Engin., 2008. v. 11, № 4, p. 379–387.
  50. Halstead B. L. Are mitochondria directly involved in biological mineralisation? The mitochondrion and the origin of bone. Calc. Tissue. Res., 1969, v. 3, p. 103–104.
  51. Ingram R. T., Yong-Koo Park, Clarke B. L. and Fitzpatrick L. A. Age- and gender-related changes in the distribution of osteocalcin in the extracellular matrix of normal male and female bone. Possible involvement of osteocalcin in bone remodeling. J. Clin. Invest., 1994, v. 93, p. 989–997.
  52. Jowsey J., and Riggs B. L. Mineral metabolism in osteocytes. Mayo Clin. Proc., 1964, v. 39, № 7, p. 480–484.
  53. Kitahama S., Gibson M. A., Hatzinikolas G. et al. Expression of fibrillins and other microfibril-associated proteins in human bone and osteoblast-like cells. Bone, 2000, v. 27, № 1, p. 61–67.
  54. Marenzana M., Shipley A. M., Squitiero P. et al. Bone as an ion exchange organ: Evidence for instantaneous cell-dependent calcium efflux from bone not due to resorption. Bone, 2005, v. 37, p. 545–554.
  55. Marotti G., Ferretti M., Muglia M. A. et al. A quantitative evaluation of osteoblast-osteocyte on growing endosteal surface of rabbit tibiae. Bone, 1992, v. 13, p. 363–368.
  56. Martin B. Mathematical model for the mineralization of bone. J. Orthop. Res., 1994, v. 12 № 3, p. 375–383.
  57. Martin R. B. Toward a unifying theory of bone remodeling. Bone, 2000, v. 26, № 1, p. 1–6.
  58. Neuman W. F., Terepka A. R., Canas P. and Triffitt J. T. The cycling concept of exchange in bone. Calc. Tissue Res., 1968, v. 2, p. 262–270.
  59. Nichols G. and Rogers P. Mechanisms for the transfer of calcium into and out of the skeleton. Pediatrics, 1971, v. 47, № 1, Part II, p. 211–228.
  60. Palumbo C., Palazzini S., Zaffe D. and Marotti G. Osteocyte differentiation in the tibia of newborn rabbit: an ultrastractural study of the formation of cytoplasmic processes. Acta Anat., 1990, v. 137. p. 350–358.
  61. Parfitt A. M. Progress in endocrinology and metabolism. The actions of parathyroid hormone on bone: relation to bone remodeling and turnover, calcium homeostasis, and metabolic bone disease. Part I of IV Parts: mechanisms of calcium transfer between blood and bone and their cellular basis: morphological and kinetic approaches to bone turnover. Metabolism, 1976, v. 25, № 7, p. 809–844.
  62. Reilly G. C., Knapp H. F., Stemmer A. et al. Investigation of the morphology of the lacunocanalicular systemof cortical bone using atomic force microscopy. Ann. Biomed. Eng., 2001, v. 29, p. 1074–1081.
  63. Remagen W., Caesar R. and Heuck F. Elektronenmikroskopische und mikroradiographische Befunde am Knochen der mit Dihydrotachysterin behandelten Ratten. Virch. Arch. Abt. A. Path. Anat., 1968, Bd. 345, S. 245–254.
  64. Remagen W., Hohling H. J. and Hall T. A. Electron microscopical and microprobe observations on the cell sheath of stimulated osteocytes. Calc. Tissue Res., 1969, v. 4, p. 60–68.
  65. Rowland R. E. The deposition and the removal of radium in bone by a long-term exchange process. Clin. Orthopaed., 1960, № 17. p. 146–153.
  66. Rowland R. E. Exchangeable bone calcium. Clin. Orthopaed., 1966, № 49, p. 233–248.
  67. Rubinacci A., Covini M., Bisogni C. et al. Bone as an ion exchange system: evidence for a link between mechanotransduction and metabolic needs. Am. J. Physiol. Endocrinol. Metab., 2002, v. 282, p. E851–E864.
  68. Scarpace P. J. and Neuman W. F. The blood: bone disequilibrium. II. Evidence against the active accumulation of calcium or phosphate into the bone extracellular fluid. Calc. Tissue Res., 1976, v. 20, p. 151–158.
  69. Schartum S. and Nichols G. Calcium metabolism of bone in vitro. Influence of bone cellular metabolism and parathyroid hormone. J. Clin. Invest., 1961, v. 40, № 11, p. 2083–2091.
  70. Shapiro I. M. and Greenspan J. S. Are mitochondria directly involved in biological mineralisation. Calc. Tissue Res., 1969, v. 3, 100–102.
  71. Staub, J. F., Tracqui P., Brezillon P. et al. Calcium metabolism in the rat: a temporal self-organized model. Am. J. Physiol., 1988, v. 254, p. R134–R149.
  72. Strehler E. E. and Treiman M. Calcium pumps of plasma membrane and cell interior. Curr. Molecular Medicine, 2004, v. 4, p. 323–335.
  73. Talmage R. V. A study of the effect of parathyroid hormone on bone remodeling and on calcium homeostasis. Clin. Orthopaed., 1967, № 54, p. 163–173.
  74. Tanaka Y., Nakayamada S. and Okada Y. Osteoblasts and osteoclasts in bone remodeling and inflammation current drug targets. Inflammation and Allergy, 2005, v. 4, p. 325–328.
  75. Tomlinson R. W. S., Wall M., Osbobn S. B. and Anderson J. Radiocalcium studies in normal subjects cab. Tissue Res., 1967, v. 1, p. 197–203.
  76. Wang X. and Puram S. The toughness of cortical bone and its relationship with age. Ann. Biomed. Eng., 2004, v. 32, № 1, p. 123–135.
  77. Whitfield J. F. Primary cilium — is it an osteocyte’s strain-sensing flowmeter? J. Cell. Biochem., 2003, v. 89, p. 233–237.
  78. Yang W., Kalajzic I., Lu Y. et al. In vitro and in vivo study on osteocyte-specific mechanical signaling pathways. J. Musculoskelet Neuronal Interact., 2004, v. 4, № 4, p. 386–387.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2013 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: № 0110212 от 08.02.1993.

This website uses cookies

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

About Cookies