International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Hypertonicity Down-regulates the $1{\alpha},25(OH)_2$ Vitamin $D_3$-induced Osteoclastogenesis Via the Modulation of RANKL Expression in Osteoblast

  • Jeong, Hyun-Joo (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Yushun, Tian (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Kim, Bo-Hye (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Nam, Mi-Young (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Lee, Hyun-A (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Yoo, Yun-Jung (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Seo, Jeong-Taeg (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Shin, Dong-Min (Department of Oral Biology, Yonsei University, College of Dentistry) ;
  • Ohk, Seung-Ho (Department of Oral Microbiology, Dental Science Research Institute, Chonnam National University) ;
  • Lee, Syng-Ill (Department of Oral Biology, Yonsei University, College of Dentistry)
  • Published : 2005.03.31
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Abstract

Bone remodeling is a process controlled by the action of two major bone cells; the bone forming osteoblast and the bone resorbing osteoclast. In the process of osteoclastogenesis, stromal cells and osteoblast produce RANKL, OPG, and M-CSF, which in turn regulate the osteoclastogenesis. During the bone resorption by activated osteoclasts, extracellular $Ca^{2+}/{PO_4}^{2-}$ concentration and degraded organic materials goes up, providing the hypertonic microenvironment. In this study, we tested the effects of hypertonicity due to the degraded organic materials on osteoclastogenesis in co-culture system. It was examined the cellular response of osteoblastic cell in terms of osteoclastogenesis by applying the sucrose, and mannitol, as a substitute of degraded organic materials to co-culture system. Apart from the sucrose, mannitol, and NaCl was tested to be compared to the effect of organic osmotic particles. The addition of sucrose and mannitol (25, 50, 100, 150, or 200 mM) to co-culture medium inhibited the number of tartrate-resistant acid phosphatase (TRAP) positive multinucleated cells induced by 10 nM $1{\alpha},25(OH)_2vitaminD_3$ ($1{\alpha},25(OH)_2D_3$). However, NaCl did exert harmful effect upon the cells in this co-culture system, which is attributed to DNA damage in high concentration of NaCl. To further investigate the mechanism by which hypertonicity inhibits $1{\alpha},25(OH)_2D_3$-induced osteoclastogenesis, the mRNA expressions of receptor activator of nuclear factor (NF)-kB ligand (RANKL) and osteoprotegerin (OPG) were monitored by RT-PCR. In the presence of sucrose (50 mM), RANKL mRNA expression was decreased in a dose-dependent manner, while the change in OPG and M-CSF mRNA were not occurred in significantly. The RANKL mRNA expression was inhibited for 48 hours in the presence of sucrose (50 mM), but such a decrement recovered after 72 hours. However, there were no considerable changes in the expression of OPG and M-CSF mRNA. Conclusively, these findings strongly suggest that hypertonic stress down-regulates $1{\alpha},25(OH)_2D_3$-induced osteoclastogenesis via RANKL signal pathway in osteoblastic cell, and may playa pivotal role as a regulator that modulates osteoclastogenesis.

Keywords

References

  1. Al-Habori M.: Cell volume and ion transport regulation. International journal of Biochemistry and cell biology. 26:319, 1994
  2. Anbari K. and Schultz RM.: Effect of sodium and betaine in culture media on development and relative rates of protein synthesis in preimplantation mouse embryos in vitro. Molecular Reproduction and Development. 35(1):24, 1993 https://doi.org/10.1002/mrd.1080350105
  3. Aubin JE.: Bone stem cells. Journal of cellular biochemistry. (supplements) 30:73, 1998 https://doi.org/10.1002/(SICI)1097-4644(1998)72:30/31+<73::AID-JCB11>3.0.CO;2-L
  4. Baron R, Neff I, Louvard D. and Courtoy PJ.: Cell-mediated extracellular acidification and bone resorption: Evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. Journal of Cell Biology. 101:2210, 1985 https://doi.org/10.1083/jcb.101.6.2210
  5. Blair HC, Teitelbaum SL, Ghiselli R. and Gluck S.: Osteoclastic bone resorption by a polarized vacuolar proton pump. Science. 245: 855, 1989 https://doi.org/10.1126/science.2528207
  6. Burgess TL, Qian Y, Kaufman S, Ring BD, Van G, Capparelli C, Kelley M, Hsu H, Boyle WJ, Dunstan CR, Hu S and Lacey DL.: The ligand for osteoprotegerin (OPGL) directly activates mature osteoclasts. Journal of Cell Biology. 145:527, 1999 https://doi.org/10.1083/jcb.145.3.527
  7. Choi BK, Ohk SH, Lee HJ, Kang JH, Jeong GJ and Yoo YJ.: Effects of whole cell sonicateds of Treponema lecithinolyticum on osteoclast differentiation. Journal of Periodontology. 72: 1172, 2001 https://doi.org/10.1902/jop.2000.72.9.1172
  8. Cossins AR.: Cell physiology. A sense of cell size. Nature. 352:667, 1991 https://doi.org/10.1038/352667a0
  9. Dmitrieva NI, Cai Q and Burg MB. : Cells adapted to high NaCl have many DNA breaks and impaired DNA repair both in cell culture and in vivo. Proc. Natl. Acad. Sci. USA. 101(8):2317, 2004 https://doi.org/10.1073/pnas.0308463100
  10. Ducy P, Schinke T and Karsenty G.: The osteoblast : A sophisticated fibroblast under central surveillance. Science. 289:1501, 2000 https://doi.org/10.1126/science.289.5484.1501
  11. Eveloff JL and Warnock DG. : Activation of ion transport systems during cell volume regulation. American journal of Physiology. 252:10, 1987
  12. Everts V, Delaisse JM, Korper W, Niehof A, Vaes G and Beertsen W.: Degradation of collagen in the bone-resorbing compartment underlying the osteoclast involves both cysteineproteinases and matrix metalloproteinases. Joumal of Cellular Physiology. 150(2):221, 1992 https://doi.org/10.1002/jcp.1041500202
  13. Fuller K, Wong B, Fox S, Choi Y and Chambers TJ.: TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts. Journal of Experimental Medicine. 188:997, 1998 https://doi.org/10.1084/jem.188.5.997
  14. Gravallese EM, Galson DL, Goldring SR and Auron PE.: The role of TNF-receptor family members and other TRAF-dependent receptors in bone resorption. Arthritis Research. 3(1):6, 2001 https://doi.org/10.1186/ar134
  15. Handler J.S. and Kwon H.M.: Transcriptional regulation by changes in tonicity. Kidney International. 60(2):408, 2001 https://doi.org/10.1046/j.1523-1755.2001.060002408.x
  16. Hernandez CJ, Beaupre GS and Carter DR.: A model of nuclear factor-kB ligand and osteoprotegerin in the pathogenesis and treatment of metabolic bone diseases. Journal of Rehablilitation Researh and Development. 37(2):234, 2000
  17. Hofbauer LC and Heufelder AE. : Clinical review 114: hot topic. The role of receptor activator of nuclear factorkappaB ligand and osteoprotegerin in the pathogenesis and treatment of metabolic bone diseases. The Journal of Clinical Endocrinology & Metabolism. 85(7):2355, 2000 https://doi.org/10.1210/jc.85.5.2000
  18. Hoffmann EK and Dunham PB. : Membrane mechanisms and intracellular signalling in cell volume regulation. International Review of Cytology. 161: 173, 1995 https://doi.org/10.1016/S0074-7696(08)62498-5
  19. Jimi E, Nakamura I, Duong LT, Ikebe T, Takahashi N, Rodan GA and Suda T.: Interleukin-l induces multinucleation and bone-resorbing activity of osteoclasts in the absence of osteoblasts/stromal cells. Experimental Cell Research. 247(1): 84, 1999 https://doi.org/10.1006/excr.1998.4320
  20. Jimi E, Nakamura I, Ikebe T, Akiyama S, Takahashi N and Suda T: Activation of NF-kappaB is involved in the survival of osteoclasts promoted by interleukin-1. The Journal of Biological Chemistry. 273(15):8799, 1998 https://doi.org/10.1074/jbc.273.15.8799
  21. Jimi E, Shuto T and Koga T : Macrophage colony-stimulating factor and interleukin-1 alpha maintain the survival of osteoclast-like cells. Endocrinology. 136(2):808, 1995 https://doi.org/10.1210/en.136.2.808
  22. Jones SJ and Boyde A.: Scanning microscopic observations on dental caries. Scanning Microsc.1(4):1991, 1987
  23. Kameda T, Ishikawa H. and Tsutsui T.: Detection and characterization of apoptosis in osteoclasts in vitro. Biochemical and Biophysical Research Communications. 207(2):753, 1995 https://doi.org/10.1006/bbrc.1995.1251
  24. Kanatani M, Sugimoto T, Kanzawa M, Yano S and Chihara K.: High extracellular calcium inhibits osteoclast-like cell formation by directly acting on the calcium-sensing receptor existing in osteoclast precursor cells. Biochemical and Biophysical Research Communications. 261(1):144, 1999 https://doi.org/10.1006/bbrc.1999.0932
  25. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G; Hie A, Khoo W, Wakeham A, Dunstan CR, Lacey DL, Mak TW, Boyle WJ and Penninger JM.: OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymphnode organogenesis. Nature. 397 :315, 1999 https://doi.org/10.1038/16852
  26. Kultz D and Chakravarty D.: Hyperosmolality in the form of elevated NaCl but not urea causes DNA damage in murine kidney cells. Proc. Natl. Acad. Sci. USA. 98(4):1999, 2001 https://doi.org/10.1073/pnas.98.4.1999
  27. Kultz D and Csonka L.: What sets the TonE during osmotic stress? Proc. Natl. Acad. Sci. USA. 96(5):1814, 1999 https://doi.org/10.1073/pnas.96.5.1814
  28. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G; Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G; Guo J, Delaney J and Boyle WJ.: Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell, 93(2): 165, 1998 https://doi.org/10.1016/S0092-8674(00)81569-X
  29. Lorget F, Kamel S, Mentaverri R, Wattel A, Naassila M, Maamer M and Brazier M.: High extracellular calcium concentrations directly stimulate osteoclast apoptosis. Biochemical and Biophysical Research Communications. 268(3):899, 2000 https://doi.org/10.1006/bbrc.2000.2229
  30. Malgaroli A, Meldolesi J, Zallone AZ and Teti A.: Control of cytosolic free calcium in rat and chicken osteoclasts. The role of extracellular calcium and calcitonin. Journal of Biological Chemistry. 264(24):14342, 1989
  31. Raisz LG.: Physiology and pathophysiology of bone remodeling. Clinical Chemistry. 45:1353, 1999
  32. Rani CS and MacDougall M.: Dental cells express factors that regulate bone resorption. Molecular Cell Biology Research Communication. 3(3):145, 2000 https://doi.org/10.1006/mcbr.2000.0205
  33. Roodman GD.: Biology of osteoclast activation in cancer. Journal of clinical Oncology. 19(15):3562, 2001 https://doi.org/10.1200/JCO.2001.19.15.3562
  34. Sarkadi, B. and Parker, J.C.: Activation of ion transport pathways by changes in cell volume. Biochimica et Biophysica Acta. 1071(4):407
  35. Salo J, Metsikko K, Palokangas H, Lehenkari P and Vaananen HK.: Bone-resorbing osteoclasts reveal a dynamic division of basal plasma membrane into two different domains. Journal of Cell Science. 109:301, 1996
  36. Sheikh-Hamad D, Di Mari J, Suki WN, Safirstein R, Watts BA 3rd and Rouse D.: p38 kinase activity is essential for osmotic induction of mRNAs for HPS 70 and transpoter for organic solute betaine in Madin-Darby Canine Kidney cells. The Journal of Biological Chemistry. 273(3): 1832, 1998 https://doi.org/10.1074/jbc.273.3.1832
  37. Shirai Y, Yoshimura Y, Yawaka Y, Hasegawa T, Kikuiri T, Takeyama S, Matsumoto A and Oguchi H.: Effect of extracellular calcium concentrations on osteoclast differentiation in vitro. Biochemical and Biophysical Research Communications. 265(2):484, 1999 https://doi.org/10.1006/bbrc.1999.1664
  38. Silver lA, Murrills RJ and Etherington DJ.: Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Experimental Cell Reserch. 175(2):266, 1988 https://doi.org/10.1016/0014-4827(88)90191-7
  39. Strange K, Emma F and Jackson PS.: Cellular and molecular physiology of volume-sensitive anion channels. American Journal of Physiology. 270:C711, 1996 https://doi.org/10.1152/ajpcell.1996.270.3.C711
  40. Suda T, Takahashi N and Martin TJ.: Modulation of osteoclast differentiation. Endocrine Review. 13(1):66, 1992 https://doi.org/10.1210/edrv-13-1-66
  41. Suda T, Udagawa N, Nakamura I, Miyaura C and Takahashi N.: Modulation of osteoclast differentiation by local factors. Bone, 17:87, 1995 https://doi.org/10.1016/8756-3282(95)00185-G
  42. Takahashi N, Udagawa, N and Suda T.: A new member of tumor necrosis factor ligand family, ODF/OPGL/TRANCE/RANKL, regulates osteoclast differentiation and function. Biochemical and Biophysical Research Communications. 256:449, 1999 https://doi.org/10.1006/bbrc.1999.0252
  43. Takeyama, S., Yoshimura, Y, Shirai, Y, Deyama, Y, Hasegawa, T., Yawaka, Y, Kikuiri, T., Matsumoto, A. and Fukuda, H.: Low calcium environment effects osteoprotegerin ligandl osteoclast differentiation factor. Biochemical and Biophysical Research Communications. 276:524, 2000 https://doi.org/10.1006/bbrc.2000.3498
  44. Tsukii K, Shima N, Mochizuki S, Yamaguchi K, Kinosaki M, Yano K, Shibata O, Udagawa N, Yasuda H, Suda T and Higashio K.: Osteoclast differentiation factor mediates an essential signal for bone resorption induced by 1 alpha, 25-dihydroxyvitamin D3, prostaglandin E2, or parathyroid hormone in the microenvironment of bone. Biochemical and Biophysical Research Communications 146:337, 1998 https://doi.org/10.1006/bbrc.1998.8610
  45. Vaes G.: Cellular biology and biochemical mechanism of bone resorption. A review of recent developments on the formation, activation, and mode of action of osteoclasts. Clinical Orthopaedics and Related Research. 231:239, 1988
  46. Vaananen HK, Karhukorpi EK, Sundquist K, Wallmark B, Roininen I, Hentunen T, Tuukkanen J. and Lakkakorpi P.: Evidence for the presence of a proton pump of the vacuolar H+-ATPase type in the ruffled borders of osteoclasts. Journal of Cell Biology. 111:1305, 1990 https://doi.org/10.1083/jcb.111.3.1305
  47. Woo SK, Lee SD and Kwon HM.: TonEBP transcriptional activator in the cellular response to increased osmolality. Pflugers Archiv European Journal of Physiology. 444(5): 579, 2002 https://doi.org/10.1007/s00424-002-0849-2
  48. Yancey PH, Burg MB and Bagnasco SM.: Effects of NaCl, glucose, and aldose reductase inhibitors on cloning efficiency of renal medullary cells. (1990) American Journal of Physiology. 258:198, 1990