• Wiley Online Library will be disrupted on 26 May from 10:00-12:00 BST (05:00-07:00 EDT) for essential maintenance

Original Article

You have full text access to this OnlineOpen article

The role of mast cells in parathyroid bone disease

  1. Russell T Turner1,*,
  2. Urszula T Iwaniec1,
  3. Kevin Marley1,
  4. Jean D Sibonga2

Article first published online: 29 JAN 2010

DOI: 10.1002/jbmr.49

Issue

Journal of Bone and Mineral Research

Journal of Bone and Mineral Research

Volume 25, Issue 7, pages 1637–1649, July 2010

Additional Information

How to Cite

Turner, R. T., Iwaniec, U. T., Marley, K. and Sibonga, J. D. (2010), The role of mast cells in parathyroid bone disease. J Bone Miner Res, 25: 1637–1649. doi: 10.1002/jbmr.49

Author Information

  1. 1

    Department of Nutrition and Exercise Sciences, Oregon State University, Corvallis, OR, USA

  2. 2

    Division of Space Life Sciences, Universities Space Research Association, Houston, TX, USA

*Department of Nutrition and Exercise Sciences, 107B Milam Hall, Oregon State University, Corvallis, OR 97331, USA.

Publication History

  1. Issue published online: 30 JUN 2010
  2. Article first published online: 29 JAN 2010
  3. Manuscript Accepted: 19 JAN 2010
  4. Manuscript Revised: 22 NOV 2009
  5. Manuscript Received: 4 MAY 2009

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (655K)

References

  • 1
    Mosekilde L. Primary hyperparathyroidism and the skeleton. Clin Endocrinol (Oxf). 2008; 69: 1–19.
    Direct Link:
  • 2
    Rudser KD, de Boer IH, Dooley A, Young B, Kestenbaum B. Fracture risk after parathyroidectomy among chronic hemodialysis patients. J Am Soc Nephrol. 2007; 18: 2401–2407.
  • 3
    Duan Y, De Luca V, Seeman E. Parathyroid hormone deficiency and excess: similar effects on trabecular bone but differing effects on cortical bone. J Clin Endocrinol Metab. 1999; 84: 718–722.
  • 4
    Tejwani NC, Schachter AK, Immerman I, Achan P. Renal osteodystrophy. J Am Acad Orthop Surg. 2006; 14: 303–311.
  • 5
    Parfitt AM. Renal bone disease: a new conceptual framework for the interpretation of bone histomorphometry. Curr Opin Nephrol Hypertens. 2003; 12: 387–403.
  • 6
    Gal-Moscovici A, Popovtzer MM. New worldwide trends in presentation of renal osteodystrophy and its relationship to parathyroid hormone levels. Clin Nephrol. 2005; 63: 284–289.
  • 7
    Jokihaara J, Porsti IH, Koobi P, et al. Treatment of experimental renal osteodystrophy with pamidronate. Kidney Int. 2008; 74: 319–327.
  • 8
    Dobnig H, Turner RT. The effects of programmed administration of human parathyroid hormone fragment (1-34) on bone histomorphometry and serum chemistry in rats. Endocrinology. 1997; 138: 4607–4612.
  • 9
    Golder R, Delmez JA, Klahr S. Bone disease in long-term dialysis. Am J Kidney Dis. 1996; 28: 918–923.
  • 10
    Ubara Y. Bone histomorphometrical analysis in patients on long-term dialysis treatment for more than ten years. Osaka City Med J. 1998; 44: 133–153.
  • 11
    Dobnig H, Turner RT. Evidence that intermittent treatment with parathyroid hormone increases bone formation in adult rats by activation of bone lining cells. Endocrinology. 1995; 136: 3632–3638.
  • 12
    Jilka RL. Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone. 2007; 40: 1434–1446.
  • 13
    Lindsay R, Zhou H, Cosman F, Nieves J, Dempster DW, Hodsman AB. Effects of a one-month treatment with PTH(1-34) on bone formation on cancellous, endocortical, and periosteal surfaces of the human ilium. J Bone Miner Res. 2007; 22: 495–502.
    Direct Link:
  • 14
    Lotinun S, Sibonga JD, Turner RT. Evidence that the cells responsible for marrow fibrosis in a rat model for hyperparathyroidism are preosteoblasts. Endocrinology. 2005; 146: 4074–4081.
  • 15
    Stanislaus D, Yang X, Liang JD, et al. In vivo regulation of apoptosis in metaphyseal trabecular bone of young rats by synthetic human parathyroid hormone (1-34) fragment. Bone. 2000; 27: 209–218.
  • 16
    Lotinun S, Sibonga JD, Turner RT. Triazolopyrimidine (trapidil), a platelet-derived growth factor antagonist, inhibits parathyroid bone disease in an animal model for chronic hyperparathyroidism. Endocrinology. 2003; 144: 2000–2007.
  • 17
    Daniel TO, Kumjian DA. Platelet-derived growth factor in renal development and disease. Semin Nephrol. 1993; 13: 87–95.
  • 18
    Katoh O, Kimura A, Itoh T, Kuramoto A. Platelet derived growth factor messenger RNA is increased in bone marrow megakaryocytes in patients with myeloproliferative disorders. Am J Hematol. 1990; 35: 145–150.
    Direct Link:
  • 19
    Kimura A, Nakata Y, Hyodo H, Kuramoto A, Satow Y. Platelet-derived growth factor expression in accelerated and blastic phase of chronic myelogenous leukaemia with myelofibrosis. Br J Haematol. 1994; 86: 303–307.
    Direct Link:
  • 20
    Nagaoka I, Trapnell BC, Crystal RG. Upregulation of platelet-derived growth factor-A and -B gene expression in alveolar macrophages of individuals with idiopathic pulmonary fibrosis. J Clin Invest. 1990; 85: 2023–2027.
  • 21
    Rameshwar P, Denny TN, Stein D, Gascon P. Monocyte adhesion in patients with bone marrow fibrosis is required for the production of fibrogenic cytokines. Potential role for interleukin-1 and TGF-beta. J Immunol. 1994; 153: 2819–2830.
  • 22
    Reilly JT, Idiopathic myelofibrosis: pathogenesis, natural history and management. Blood Rev. 1997; 11: 233–242.
  • 23
    Lowry MB, Lotinun S, Leontovich AA, et al. Osteitis fibrosa is mediated by PDGF-A via a PI3K-dependent signaling pathway in a rat model for chronic hyperparathyroidism. Endocrinology. 2008.
  • 24
    Guichelaar MM, Malinchoc M, Sibonga JD, Clarke BL, Hay JE. Bone histomorphometric changes after liver transplantation for chronic cholestatic liver disease. J Bone Miner Res. 2003; 18: 2190–2199.
    Direct Link:
  • 25
    Iwaniec UT, Wronski TJ, Turner RT. Histological analysis of bone. Methods Mol Biol. 2008; 447: 325–341.
  • 26
    Hawse JR, Iwaniec UT, Bensamoun SF, et al. TIEG-null mice display an osteopenic gender-specific phenotype. Bone. 2008; 42: 1025–1031.
  • 27
    Turner RT, Bell NH, Duvall P, et al. Spaceflight results in formation of defective bone. Proc Soc Exp Biol Med. 1985; 180: 544–549.
  • 28
    Daddow LY. An abbreviated method of the double lead stain technique. J Submicrosc Cytol. 1986; 18: 221–224.
  • 29
    Torring O, Turner RT, Carter WB, Firek AF, Jacobs CA, Heath H 3rd. Inhibition by human interleukin-1 alpha of parathyroid hormone-related peptide effects on renal calcium and phosphorus metabolism in the rat. Endocrinology. 1992; 131: 5–13.
  • 30
    Brunner S, Theiss HD, Murr A, Negele T, Franz WM. Primary hyperparathyroidism is associated with increased circulating bone marrow-derived progenitor cells. Am J Physiol Endocrinol Metab. 2007; 293: E1670–5.
  • 31
    Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003; 425: 841–846.
  • 32
    Kollet O, Dar A, Shivtiel S, et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med. 2006; 12: 657–664.
  • 33
    Kumbasar B, Taylan I, Kazancioglu R, Agan M, Yenigun M, Sar F. Myelofibrosis secondary to hyperparathyroidism. Exp Clin Endocrinol Diabetes. 2004; 112: 127–130.
  • 34
    Sikole A. Pathogenesis of anaemia in hyperparathyroidism. Med Hypotheses. 2000; 54: 236–238.
  • 35
    Smogorzewski M, Massry SG. Defects in B-cell function and metabolism in uremia: role of parathyroid hormone. Kidney Int Suppl. 2001; 78: S186–9.
  • 36
    Tzanno-Martins C, Futata E, Jorgetti V, Duarte AJ. Restoration of impaired T-cell proliferation after parathyroidectomy in hemodialysis patients. Nephron. 2000; 84: 224–227.
  • 37
    Blair HC, Dong SS, Julian BA. Expression of stem cell factor by osteoblasts in normal and hyperparathyroid bone: relation to ectopic mast cell differentiation. Virchows Arch. 1999; 435: 50–57.
  • 38
    Nakamura M, Kuroda H, Narita K, Endo Y. Parathyroid hormone induces a rapid increase in the number of active osteoclasts by releasing histamine from mast cells. Life Sci. 1996; 58: 1861–1868.
  • 39
    Tsakalos ND, Theoharides TC, Kops SK, Askenase PW. Induction of mast cell secretion by parathormone. Biochem Pharmacol. 1983; 32: 355–360.
  • 40
    Biosse-Duplan M, Baroukh B, Dy M, de Vernejoul MC, Saffar JL. Histamine promotes osteoclastogenesis through the differential expression of histamine receptors on osteoclasts and osteoblasts. Am J Pathol. 2009; 174: 1426–1434.
  • 41
    Fouilloux I, Duplan MB, Baroukh B, Cherruau M, Saffar JL, Lesclous P. Mast cell activation and degranulation occur early during induction of periosteal bone resorption. Bone. 2006; 38: 59–66.
  • 42
    Lesclous P, Guez D, Baroukh B, Vignery A, Saffar JL. Histamine participates in the early phase of trabecular bone loss in ovariectomized rats. Bone. 2004; 34: 91–99.
  • 43
    Lesclous P, Guez D, Saffar JL. Short-term prevention of osteoclastic resorption and osteopenia in ovariectomized rats treated with the H(2) receptor antagonist cimetidine. Bone. 2002; 30: 131–136.
  • 44
    Lesclous P, Schramm F, Gallina S, Baroukh B, Guez D, Saffar JL. Histamine mediates osteoclastic resorption only during the acute phase of bone loss in ovariectomized rats. Exp Physiol. 2006; 91: 561–570.
    Direct Link:
  • 45
    Ellis HA, Peart KM. Iliac bone marrow mast cells in relation to the renal osteodystrophy of patients treated by haemodialysis. J Clin Pathol. 1976; 29: 502–516.
  • 46
    Ellis HA, Peart KM, Pierides AM. Effect of renal transplantation on marrow mast cell hyperplasia of chronic renal failure. J Clin Pathol. 1977; 30: 960–965.
  • 47
    Onyia JE, Helvering LM, Gelbert L, et al. Molecular profile of catabolic versus anabolic treatment regimens of parathyroid hormone (PTH) in rat bone: an analysis by DNA microarray. J Cell Biochem. 2005; 95: 403–418.
    Direct Link:
  • 48
    Samayawardhena LA, Kapur R, Craig AW. Involvement of Fyn kinase in Kit and integrin-mediated Rac activation, cytoskeletal reorganization, and chemotaxis of mast cells. Blood. 2007; 109: 3679–3686.
  • 49
    Li B, Boast S, de los Santos K, et al. Mice deficient in Abl are osteoporotic and have defects in osteoblast maturation. Nat Genet. 2000; 24: 304–308.
  • 50
    O'Sullivan S, Naot D, Callon K, et al. Imatinib promotes osteoblast differentiation by inhibiting PDGFR signaling and inhibits osteoclastogenesis by both direct and stromal cell-dependent mechanisms. J Bone Miner Res. 2007; 22: 1679–1689.
    Direct Link:
  • 51
    Ueda S, Mizuki M, Ikeda H, et al. Critical roles of c-Kit tyrosine residues 567 and 719 in stem cell factor-induced chemotaxis: contribution of src family kinase and PI3-kinase on calcium mobilization and cell migration. Blood. 2002; 99: 3342–3349.
  • 52
    Sato M, Bryant HU, Dodge JA, Davis H, Matter WF, Vlahos CJ. Effects of wortmannin analogs on bone in vitro and in vivo. J Pharmacol Exp Ther. 1996; 277: 543–550.
  • 53
    Iwaniec UT, Wronski TJ, Liu J, et al. PTH stimulates bone formation in mice deficient in Lrp5. J Bone Miner Res. 2007; 22: 394–402.
    Direct Link:
  • 54
    Zhou H, Iida-Klein A, Lu SS, et al. Anabolic action of parathyroid hormone on cortical and cancellous bone differs between axial and appendicular skeletal sites in mice. Bone. 2003; 32: 513–520.
  • 55
    Pierroz DD, Bouxsein ML, Rizzoli R, Ferrari SL. Combined treatment with a beta-blocker and intermittent PTH improves bone mass and microarchitecture in ovariectomized mice. Bone. 2006; 39: 260–267.
  • 56
    Turner RT, Lotinun S, Hefferan TE, Morey-Holton E. Disuse in adult male rats attenuates the bone anabolic response to a therapeutic dose of parathyroid hormone. J Appl Physiol. 2006; 101: 881–886.
  • 57
    Miyakoshi N. Effects of parathyroid hormone on cancellous bone mass and structure in osteoporosis. Curr Pharm Des. 2004; 10: 2615–2627.
  • 58
    Abdollahi A, Li M, Ping G, et al. Inhibition of platelet-derived growth factor signaling attenuates pulmonary fibrosis. J Exp Med. 2005; 201: 925–935.
  • 59
    Geremias AT, Carvalho MA, Borojevic R, Monteiro AN. TGF beta1 and PDGF AA override collagen type I inhibition of proliferation in human liver connective tissue cells. BMC Gastroenterol. 2004; 4: 30.
  • 60
    Malizia G, Brunt EM, Peters MG, Rizzo A, Broekelmann TJ, McDonald JA. Growth factor and procollagen type I gene expression in human liver disease. Gastroenterology. 1995; 108: 145–156.
  • 61
    Agarwal G, Mishra SK, Kar DK, et al. Recovery pattern of patients with osteitis fibrosa cystica in primary hyperparathyroidism after successful parathyroidectomy. Surgery. 2002; 132: 1075–1083 discussion 1083–5.
View Full Article (HTML) Get PDF (655K)