Parathyroid hormone mediates hematopoietic cell expansion through interleukin-6

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Pirih, Flavia Q ^a   Michalski, Megan N ^a   Cho, Sun W ^a   Koh, Amy J ^a   Berry, Janice E ^a   Ghaname, Eduardo ^a   Kamarajan, Pachiyappan ^a   Bonnelye, Edith ^b   Ross, Charles W ^c   Kapila, Yvonne L ^a   Jurdic, Pierre ^b   McCauley, Laurie K ^a,c  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; FLT3 LIGAND; INTERLEUKIN 6; PARATHYROID HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BONE MARROW CULTURE; CELL ADHESION; CELL COUNT; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL; HORMONE ACTION; IN VIVO STUDY; MOUSE; NONHUMAN; OSTEOCLAST; WILD TYPE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL DIVISION; CELL LINEAGE; CYTOLOGY; DRUG EFFECT; FLOW CYTOMETRY; OSTEOBLAST; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MUS;

ANIMALS; BLOTTING, WESTERN; BONE MARROW CELLS; CELL ADHESION; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; FLOW CYTOMETRY; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; OSTEOBLASTS; PARATHYROID HORMONE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78149461750     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013657     Document Type: Article

References (52)

1. Philbrick WM, Dreyer BE, Nakchbandi IA, Karaplis AC (1998) Parathyroid hormone-related protein is required for tooth eruption. Proc Natl Acad Sci USA 95: 11846-11851
2. Bryden AA, Hoyland JA, Freemont AJ, Clarke NW, George NJ (2002) Parathyroid hormone related peptide and receptor expression in paired primary prostate cancer and bone metastases. BrJCancer 86: 322-325.
3. Wysolmerski JJ, Stewart AF, Kovacs CS (2008) Physiological Actions of parathyroid hormone and parathyroid hormone related protein. In: Bilezikian J, Raisz LG, Rodan GA, eds. Principles of Bone Biology. San Diego: Academic Press. 713-31 p.
4. Adams GB, Martin RP, Alley IR, Chabner KT, Cohen KS, et al. (2007) Therapeutic targeting of a stem cell niche. Nat Biotechnol 25: 238-243.
5. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, et al. (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425: 841-846.
6. Ballen KK, Shpall EJ, Avigan D, Yeap BY, Fisher DC, et al. (2007) Phase I trial of parathyroid hormone to facilitate stem cell mobilization. Biol Blood Marrow Transplant 13: 838-843.
7. Lee SK, Lorenzo JA (1999) Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology 140: 3552-3561.
8. Gay CV (1991) Avian osteoclasts. Calcif Tissue Int 49: 153-154.
9. Gay CV, Zheng B, Gilman VR (2003) Co-detection of PTH/PTHrP receptor and tartrate resistant acid phosphatase in osteoclasts. J Cell Biochem 89: 902-908.
10. Komarova SV (2005) Mathematical model of paracrine interactions between osteoclasts and osteoblasts predicts anabolic action of parathyroid hormone on bone. Endocrinology 146: 3589-3595.
11. Terauchi M, Li JY, Bedi B, Baek KH, Tawfeek H, et al. (2009) T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab 10: 229-240.
12. McCauley LK, Rosol TJ, Merryman JI, Capen CC (1992) Parathyroid hormone-related protein binding to human T-cell lymphotropic virus type I-infected lymphocytes. Endocrinology 130: 300-306.
13. Hory BG, Roussanne MC, Rostand S, Bourdeau A, Drueke TB, et al. (2000) Absence of response to human parathyroid hormone in athymic mice grafted with human parathyroid adenoma, hyperplasia or parathyroid cells maintained in culture. J Endocrinol Invest 23: 273-279.
14. Greenfield EM, Gornik SA, Horowitz MC, Donahue HJ, Shaw SM (1993) Regulation of cytokine expression in osteoblasts by parathyroid hormone: rapid stimulation of interleukin-6 and leukemia inhibitory factor mRNA. J Bone Miner Res 8: 1163-1171.
15. Kishimoto T, Akira S, Narazaki M, Taga T (1995) Interleukin-6 family of cytokines and gp130. Blood 86: 1243-1254.
16. Michalevicz R, Lifshitz D, Revel M (1989) Interferon beta 2/interleukin-6 and interleukin-3 synergize in stimulating proliferation of human early hematopoietic progenitor cells. Scanning Microsc 3: 1143-1149. discussion 1149-1150.
17. O'Brien CA, Jilka RL, Fu Q, Stewart S, Weinstein RS, et al. (2005) IL-6 is not required for parathyroid hormone stimulation of RANKL expression, osteoclast formation, and bone loss in mice. Am J Physiol Endocrinol Metab 289: E784-793.
18. Poli V, Balena R, Fattori E, Markatos A, Yamamoto M, et al. (1994) Interleukin-6 deficient mice are protected from bone loss caused by estrogen depletion. Embo J 13: 1189-1196.
19. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, et al. (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342.
20. Demiralp B, Chen HL, Koh AJ, Keller ET, McCauley LK (2002) Anabolic actions of parathyroid hormone during bone growth are dependent on c-fos. Endocrinology 143: 4038-4047.
21. Servet-Delprat C, Arnaud S, Jurdic P, Nataf S, Grasset MF, et al. (2002) Flt3+ macrophage precursors commit sequentially to osteoclasts, dendritic cells and microglia. BMC Immunol 3: 15.
22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
23. Saltel F, Chabadel A, Zhao Y, Lafage-Proust MH, Clezardin P, et al. (2006) Transmigration: a new property of mature multinucleated osteoclasts. J Bone Miner Res 21: 1913-1923.
24. Shibutani T, Iwanaga H, Imai K, Kitago M, Doi Y, et al. (2000) Use of glass slides coated with apatite-collagen complexes for measurement of osteoclastic resorption activity. J Biomed Mater Res 50: 153-159.
25. Brasel K, McKenna HJ, Morrissey PJ, Charrier K, Morris AE, et al. (1996) Hematologic effects of flt3 ligand in vivo in mice. Blood 88: 2004-2012.
26. Dempster DW, Hughes-Begos CE, Plavetic-Chee K, Brandao-Burch A, Cosman F, et al. (2005) Normal human osteoclasts formed from peripheral blood monocytes express PTH type 1 receptors and are stimulated by PTH in the absence of osteoblasts. J Cell Biochem 95: 139-148.
27. Jurdic P, Saltel F, Chabadel A, Destaing O (2006) Podosome and sealing zone: specificity of the osteoclast model. Eur J Cell Biol 85: 195-202.
28. Bernad A, Kopf M, Kulbacki R, Weich N, Koehler G, et al. (1994) Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system. Immunity 1: 725-731.
29. Blaskovich MA, Sun J, Cantor A, Turkson J, Jove R, et al. (2003) Discovery of JSI-124 (cucurbitacin I), a selective Janus kinase/signal transducer and activator of transcription 3 signaling pathway inhibitor with potent antitumor activity against human and murine cancer cells in mice. Cancer Res 63: 1270-1279.
30. Drexler HG, Quentmeier H (2004) FLT3: receptor and ligand. Growth Factors 22: 71-73.
31. Rusten LS, Lyman SD, Veiby OP, Jacobsen SE (1996) The FLT3 ligand is a direct and potent stimulator of the growth of primitive and committed human CD34+ bone marrow progenitor cells in vitro. Blood 87: 1317-1325.
32. Brunner S, Theiss HD, Murr A, Negele T, Franz WM (2007) Primary hyperparathyroidism is associated with increased circulating bone marrow-derived progenitor cells. Am J Physiol Endocrinol Metab 293: E1670-1675.
33. Zaruba MM, Huber BC, Brunner S, Deindl E, David R, et al. (2008) Parathyroid hormone treatment after myocardial infarction promotes cardiac repair by enhanced neovascularization and cell survival. Cardiovasc Res 77: 722-731.
34. Jilka RL, Weinstein RS, Bellido T, Roberson P, Parfitt AM, et al. (1999) Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 104: 439-446.
35. Chen HL, Demiralp B, Schneider A, Koh AJ, Silve C, et al. (2002) Parathyroid hormone and parathyroid hormone-related protein exert both pro- and anti-apoptotic effects in mesenchymal cells. J Biol Chem 277: 19374-19381.
36. Chauhan D, Kharbanda S, Ogata A, Urashima M, Teoh G, et al. (1997) Interleukin-6 inhibits Fas-induced apoptosis and stress-activated protein kinase activation in multiple myeloma cells. Blood 89: 227-234.
37. Kawano MM, Mihara K, Huang N, Tsujimoto T, Kuramoto A (1995) Differentiation of early plasma cells on bone marrow stromal cells requires interleukin-6 for escaping from apoptosis. Blood 85: 487-494.
38. Phinney DG, Kopen G, Isaacson RL, Prockop DJ (1999) Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J Cell Biochem 72: 570-585.
39. Way KJ, Dinh H, Keene MR, White KE, Clanchy FI, et al. (2009) The generation and properties of human macrophage populations from hemopoietic stem cells. J Leukoc Biol 85: 766-778.
40. Lean JM, Fuller K, Chambers TJ (2001) FLT3 ligand can substitute for macrophage colony-stimulating factor in support of osteoclast differentiation and function. Blood 98: 2707-2713.
41. Chang MK, Raggatt LJ, Alexander KA, Kuliwaba JS, Fazzalari NL, et al. (2008) Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol 181: 1232-1244.
42. Pettway GJ, Meganck JA, Koh AJ, Keller ET, Goldstein SA, et al. (2008) Parathyroid hormone mediates bone growth through the regulation of osteoblast proliferation and differentiation. Bone 42: 806-818.
43. Koh AJ, Demiralp B, Neiva KG, Hooten J, Nohutcu RM, et al. (2005) Cells of the osteoclast lineage as mediators of the anabolic actions of parathyroid hormone in bone. Endocrinology 146: 4584-4596.
44. Ikebuchi K, Wong GG, Clark SC, Ihle JN, Hirai Y, et al. (1987) Interleukin 6 enhancement of interleukin 3-dependent proliferation of multipotential hemo-poietic progenitors. Proc Natl Acad Sci USA 84: 9035-9039.
45. Hirayama F, Lyman SD, Clark SC, Ogawa M (1995) The flt3 ligand supports proliferation of lymphohematopoietic progenitors and early B-lymphoid progenitors. Blood 85: 1762-1768.
46. Peters M, Solem F, Goldschmidt J, Schirmacher P, Rose-John S (2001) Interleukin-6 and the soluble interleukin-6 receptor induce stem cell factor and Flt-3L expression in vivo and in vitro. Exp Hematol 29: 146-155.
47. Taichman RS, Emerson SG (1994) Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med 179: 1677-1682.
48. Jung Y, Song J, Shiozawa Y, Wang J, Wang Z, et al. (2008) Hematopoietic stem cells regulate mesenchymal stromal cell induction into osteoblasts thereby participating in the formation of the stem cell niche. Stem Cells 26: 2042-2051.
49. Palmqvist P, Persson E, Conaway HH, Lerner UH (2002) IL-6, leukemia inhibitory factor, and oncostatin M stimulate bone resorption and regulate the expression of receptor activator of NF-kappa B ligand, osteoprotegerin, and receptor activator of NF-kappa B in mouse calvariae. J Immunol 169: 3353-3362.
50. Erices A, Conget P, Rojas C, Minguell JJ (2002) Gp130 activation by soluble interleukin-6 receptor/interleukin-6 enhances osteoblastic differentiation of human bone marrow-derived mesenchymal stem cells. Exp Cell Res 280: 24-32.
51. Rodriguez Mdel C, Bernad A, Aracil M (2004) Interleukin-6 deficiency affects bone marrow stromal precursors, resulting in defective hematopoietic support. Blood 103: 3349-3354.
52. Schirmacher P, Peters M, Ciliberto G, Blessing M, Lotz J, et al. (1998) Hepatocellular hyperplasia, plasmacytoma formation, and extramedullary hematopoiesis in interleukin (IL)-6/soluble IL-6 receptor double-transgenic mice. Am J Pathol 153: 639-648.