The PTH/PTHrP receptor can delay chondrocyte hypertrophy in vivo without activating phospholipase C

Developmental Cell

Volumn 3, Issue 2, 2002, Pages 183-194

  Guo, Jun ^a   Chung, Ung Il ^a   Kondo, Hisatomo ^a   Bringhurst, F Richard ^a   Kronenberg, Henry M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; PARATHYROID HORMONE RECEPTOR; PARATHYROID HORMONE RELATED PROTEIN; PARATHYROID HORMONE[1-34]; PHORBOL ESTER; PHOSPHOLIPASE C;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENCHONDRAL OSSIFICATION; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; METATARSAL BONE; MOUSE; MOUSE MUTANT; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0036696005     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(02)00218-6     Document Type: Article

References (60)

1. Amizuka, N., Kwan, M.Y., Goltzman, D., Ozawa, H., and White, J.H. (1999). Vitamin D3 differentially regulates parathyroid hormone/parathyroid hormone-related peptide receptor expression in bone and cartilage. J. Clin. Invest. 103, 373-381.
2. Bos, M.P., van der Meer, J.M., Feyen, J.H., and Herrmann-Erlee, M.P. (1996). Expression of the parathyroid hormone receptor and correlation with other osteoblastic parameters in fetal rat osteoblasts. Calcif. Tissue Int. 58, 95-100.
3. Bringhurst, F.R., Juppner, H., Guo, J., Urena, P., Potts, J.T., Jr., Kronenberg, H.M., Abou-Samra, A.B., and Segre, G.V. (1993). Cloned, stably expressed parathyroid hormone (PTH)/PTH-related peptide receptors activate multiple messenger signals and biological responses in LLC-PK1 kidney cells. Endocrinology 132, 2090-2098.
4. Calvi, L.M., Sims, N.A., Hunzelman, J.L., Knight, M.C., Giovannetti, A., Saxton, J.M., Kronenberg, H.M., Baron, R., and Schipani, E. (2001). Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J. Clin. Invest. 107, 277-286.
5. Chung, U.-L., Lanske, B., Lee, K., Li, E., and Kronenberg, H.M. (1998). The parathyroid hormone/parathyroid hormone-related peptide receptor coordinates endochondral bone development by directly controlling chondrocyte differentiation. Proc. Natl. Acad. Sci. USA 95, 13030-13035.
6. Chung, U.-L., Wei, W., Schipani, E., Hunzelman, J., Weinstein, L., and Kronenberg, H.M. (2000). In vivo function of stimulatory G protein (Gs) in the growth plate. J. Bone Miner. Res. 15, S175.
7. Chung, U.-L., Schipani, E., McMahon, A.P., and Kronenberg, H.M. (2001). Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J. Clin. Invest. 107, 295-304.
8. Dobnig, H., and Turner, R.T. (1995). Evidence that intermittent treatment with parathyroid hormone increases bone formation in adult rats by activation of bone lining cells. Endocrinology 136, 3632-3638.
9. Dobnig, H., and Turner, R.T. (1997). The effects of programmed administration of human parathyroid hormone fragment (1-34) on bone histomorphometry and serum chemistry in rats. Endocrinology 138, 4607-4612.
10. Francesconi, A., and Duvoisin, R.M. (1998). Role of the second and third intracellular loops of metabotropic glutamate receptors in mediating dual signal transduction activation. J. Biol. Chem. 273, 5615-5624.
11. Friedman, P.A., Coutermarsh, B.A., Kennedy, S.M., and Gesek, F.A. (1996). Parathyroid hormone stimulation of calcium transport is mediated by dual signaling mechanisms involving protein kinase A and protein kinase C. Endocrinology 137, 13-20.
12. Fujimori, A., Cheng, S.L., Avioli, L.V., and Civitelli, R. (1991). Dissociation of second messenger activation by parathyroid hormone fragments in osteosarcoma cells. Endocrinology 128, 3032-3039.
13. Fujimori, A., Cheng, S.L., Avioli, L.V., and Civitelli, R. (1992). Structure-function relationship of parathyroid hormone: activation of phospholipase-C, protein kinase-A and -C in osteosarcoma cells. Endocrinology 130, 29-36.
14. Gether, U. (2000). Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr. Rev. 21, 90-113.
15. Gudermann, T., Kalkbrenner, F., and Schultz, G. (1996). Diversity and selectivity of receptor-G protein interaction. Annu. Rev. Pharmacol. Toxicol. 36, 429-459.
16. Guo, J., Iida-Klein, A., Huang, X., Abou-Samra, A.B., Segre, G.V., and Bringhurst, F.R. (1995). Parathyroid hormone (PTH)/PTH-related peptide receptor density modulates activation of phospholipase C and phosphate transport by PTH in LLC-PK1 cells. Endocrinology 136, 3884-3891.
17. Guo, J., Liu, B.-Y., and Bringhurst, F.R. (1997). Mechanisms of homologous and heterologous desensitization of PTH/PTHrP receptor signaling in LLC-PK1 cells. Am. J. Physiol. 273, E383-E393.
18. Guo, J., Lanske, B., Liu, B.-Y., Divieti, P., Kronenberg, H.M., and Bringhurst, F.R. (2001). Signal-selectivity of parathyroid hormone (PTH)/PTH-related peptide receptor-mediated regulation of differentiation in conditionally immortalized growth-plate chondrocytes. Endocrinology 142, 1260-1268.
19. Haaijman, A., Karperien, M., Lanske, B., Hendriks, J., Lowik, C., Bronckers, A.L., and Burger, E.H. (1999). Inhibition of terminal chondrocyte differentiation by bone morphogenetic protein 7 (OP-1) in vitro depends on the periarticular region but is independent of parathyroid hormone-related peptide. Bone 25, 397-404.
20. Hock, J.M., and Gera, I. (1992). Effects of continuous and intermittent administration and inhibition of resorption on the anabolic response of bone to parathyroid hormone. J. Bone Miner. Res. 7, 65-72.
21. Iida-Klein, A., Guo, J., Takemura, M.D., Drake, M.T., Potts, J.T., Jr., Abou-Samra, A.B., Bringhurst, F.R., and Segre, G.V. (1997). Mutations in the second cytoplasmic loop of the rat parathyroid hormone (PTH)/PTH-related protein receptor result in selective loss of PTH-stimulated phospholipase C activity. J. Biol. Chem. 272, 6882-6889.
22. Janulis, M., Wong, M.S., and Favus, M.J. (1993). Structure-function requirements of parathyroid hormone for stimulation of 1, 25-dihydroxyvitamin D3 production by rat renal proximal tubules. Endocrinology 133, 713-719.
23. Jouishomme, H., Whitfield, J.F., Gagnon, L., Maclean, S., Isaacs, R., Chakravarthy, B., Durkin, J., Neugebauer, W., Willick, G., and Rixon, R.H. (1994). Further definition of the protein kinase C activation domain of the parathyroid hormone. J. Bone Miner. Res. 9, 943-949.
24. Karaplis, A.C., Luz, A., Glowacki, J., Bronson, R.T., Tybulewicz, V.L., Kronenberg, H.M., and Mulligan, R.C. (1994). Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev. 8, 277-289.
25. Karp, S.J., Schipani, E., St-Jacques, B., Hunzelman, J., Kronenberg, H.M., and McMahon, A.P. (2000). Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development 127, 543-548.
26. Kato, Y., Koike, T., Iwamoto, M., Kinoshita, M., Sato, K., Hiraki, Y., and Suzuki, F. (1988). Effects of limited exposure of rabbit chondrocyte cultures to parathyroid hormone and dibutyryl adenosine 3′, 5′-monophosphate on cartilage-characteristic proteoglycan synthesis. Endocrinology 122, 1991-1997.
27. Kawashima-Ohya, Y., Kuruta, Y., Yan, W., Kawamoto, T., Noshiro, M., and Kato, Y. (1999). Retinol-binding protein is produced by rabbit chondrocytes and responds to parathyroid hormone (PTH)/PTH-related peptide-cyclic adenosine monophosphate pathway. Endocrinology 140, 1075-1081.
28. Kitazawa, R., Imai, Y., Fukase, M., and Fujita, T. (1991). Effects of continuous infusion of parathyroid hormone and parathyroid hormone-related peptide on rat bone in vivo: comparative study by histomorphometry. Bone Miner. 12, 157-166.
29. Klaus, G., von Eichel, B., May, T., Hugel, U., Mayer, H., Ritz, E., and Mehls, O. (1994). Synergistic effects of parathyroid hormone and 1, 25-dihydroxyvitamin D3 on proliferation and vitamin D receptor expression of rat growth cartilage cells. Endocrinology 135, 1307-1315.
30. Koike, T., Iwamoto, M., Shimazu, A., Nakashima, K., Suzuki, F., and Kato, Y. (1990). Potent mitogenic effects of parathyroid hormone (PTH) on embryonic chick and rabbit chondrocytes. Differential effects of age on growth, proteoglycan, and cyclic AMP responses of chondrocytes to PTH. J. Clin. Invest. 85, 626-631.
31. Komori, T., Yagi, H., Nomura, S., Yamaguchi, A., Sasaki, K., Deguchi, K., Shimizu, Y., Bronson, R.T., Gao, Y., Inada, M., et al. (1997). Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89, 755-764.
32. Kukkonen, J.P., Nasman, J., and Akerman, K.E. (2001). Modelling of promiscuous receptor-Gi/Gs-protein coupling and effector response. Trends Pharmacol. Sci. 22, 616-622.
33. Langub, M.C., Monier-Faugere, M.C., Qi, Q., Geng, Z., Koszewski, N.J., and Malluche, H.H. (2001). Parathyroid hormone/parathyroid hormone-related peptide type 1 receptor in human bone. J. Bone Miner. Res. 16, 448-456.
34. Lanske, B., Karaplis, A.C., Lee, K., Luz, A., Vortkamp, A., Pirro, A., Karperien, M., Defize, L.H.K., Ho, C., Mulligan, R.C., et al. (1996). PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 273, 663-666.
35. Lee, K., Deeds, J.D., and Segre, G.V. (1995). Expression of parathyroid hormone-related peptide and its receptor messenger ribonucleic acids during fetal development of rats. Endocrinology 136, 453-463.
36. Li, E., Bestor, T.H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926.
37. Miao, D., Tong, X.K., Chan, G.K., Panda, D., McPherson, P.S., and Goltzman, D. (2001). Parathyroid hormone-related peptide stimulates osteogenic cell proliferation through protein kinase C activation of the Ras/mitogen-activated protein kinase signaling pathway. J. Biol. Chem. 276, 32204-32213.
38. Mitlak, B.H., Burdette-Miller, P., Schoenfeld, D., and Neer, R.M. (1996). Sequential effects of chronic human PTH (1-84) treatment of estrogen-deficiency osteopenia in the rat. J. Bone Miner. Res. 11, 430-439.
39. Nishida, S., Yamaguchi, A., Tanizawa, T., Endo, N., Mashiba, T., Uchiyama, Y., Suda, T., Yoshiki, S., and Takahashi, H.E. (1994). Increased bone formation by intermittent parathyroid hormone administration is due to the stimulation of proliferation and differentiation of osteoprogenitor cells in bone marrow. Bone 15, 717-723.
40. Offermanns, S., Iida-Klein, A., Segre, G.V., and Simon, M.I. (1996). G α q family members couple parathyroid hormone (PTH)/PTH-related peptide and calcitonin receptors to phospholipase C in COS-7 cells. Mol. Endocrinol. 10, 566-574.
41. Pisegna, J.R., and Wank, S.A. (1996). Cloning and characterization of the signal transduction of four splice variants of the human pituitary adenylate cyclase activating polypeptide receptor. Evidence for dual coupling to adenylate cyclase and phospholipase C. J. Biol. Chem. 271, 17267-17274.
42. Radeff, J.M., Nagy, Z., and Stern, P.H. (2001). Involvement of PKC-β in PTH, TNF-α, and IL-1 β effects on IL-6 promoter in osteoblastic cells and on PTH-stimulated bone resorption. Exp. Cell Res. 268, 179-188.
43. Rappaport, M.S., and Stern, P.H. (1986). Parathyroid hormone and calcitonin modify inositol phospholipid metabolism in fetal rat limb bones. J. Bone Miner. Res. 1, 173-179.
44. Schipani, E., Lanske, B., Hunzelman, J., Luz, A., Kovacs, C.S., Lee, K., Pirro, A., Kronenberg, H.M., and Juppner, H. (1997). Targeted expression of constitutively active receptors for parathyroid hormone and parathyroid hormone-related peptide delays endochondral bone formation and rescues mice that lack parathyroid hormone-related peptide. Proc. Natl. Acad. Sci. USA 94, 13689-13694.
45. Schluter, K.D., Hellstern, H., Wingender, E., and Mayer, H. (1989). The central part of parathyroid hormone stimulates thymidine incorporation of chondrocytes. J. Biol. Chem. 264, 11087-11092.
46. Schneider, H., Feyen, J.H., and Seuwen, K. (1994). A C-terminally truncated human parathyroid hormone receptor is functional and activates multiple G proteins. FEBS Lett. 351, 281-285.
47. Schwartz, Z., Semba, S., Graves, D., Dean, D.D., Sylvia, V.L., and Boyan, B.D. (1997). Rapid and long-term effects of PTH(1-34) on growth plate chondrocytes are mediated through two different pathways in a cell-maturation-dependent manner. Bone 21, 249-259.
48. Shukunami, C., Ishizeki, K., Atsumi, T., Ohta, Y., Suzuki, F., and Hiraki, Y. (1997). Cellular hypertrophy and calcification of embryonal carcinoma-derived chondrogenic cell line ATDC5 in vitro. J. Bone Miner. Res. 12, 1174-1188.
49. St-Jacques, B., Hammerschmidt, M., and McMahon, A.P. (1999). Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13, 2072-2086.
50. Swarthout, J.T., Doggett, T.A., Lemker, J.L., and Partridge, N.C. (2001). Stimulation of extracellular signal-regulated kinases and proliferation in rat osteoblastic cells by parathyroid hormone is protein kinase C-dependent. J. Biol. Chem. 276, 7586-7592.
51. Takasu, H., Gardella, T.J., Luck, M.D., Potts, J.T., Jr., and Bringhurst, F.R. (1999a). Amino-terminal modifications of human parathyroid hormone (PTH) selectively alter phospholipase C signaling via the type 1 PTH receptor: implications for design of signal-specific PTH ligands. Biochemistry 38, 13453-13460.
52. Takasu, H., Guo, J., and Bringhurst, F.R. (1999b). Dual signaling and ligand selectivity of the human PTH/PTHrP receptor. J. Bone Miner. Res. 14, 11-20.
53. Tam, C.S., Heersche, J.N., Murray, T.M., and Parsons, J.A. (1982). Parathyroid hormone stimulates the bone apposition rate independently of its resorptive action: differential effects of intermittent and continuous administration. Endocrinology 110, 506-512.
54. Uzawa, T., Hori, M., Ejiri, S., and Ozawa, H. (1995). Comparison of the effects of intermittent and continuous administration of human parathyroid hormone(1-34) on rat bone. Bone 16, 477-484.
55. Vortkamp, A., Lee, K., Lanske, B., Segre, G.V., Kronenberg, H.M., and Tabin, C.J. (1996). Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273, 613-622.
56. Weir, E.C., Philbrick, W.M., Amling, M., Neff, L.A., Baron, R., and Broadus, A.E. (1996). Targeted overexpression of parathyroid hormone-related peptide in chondrocytes causes chondrodysplasia and delayed endochondral bone formation. Proc. Natl. Acad. Sci. USA 93, 10240-10245.
57. Wess, J. (1998). Molecular basis of receptor/G-protein-coupling selectivity. Pharmacol. Ther. 80, 231-264.
58. Yoshida, E., Noshiro, M., Kawamoto, T., Tsutsumi, S., Kuruta, Y., and Kato, Y. (2001). Direct inhibition of Indian hedgehog expression by parathyroid hormone (PTH)/PTH-related peptide and up-regulation by retinoic acid in growth plate chondrocyte cultures. Exp. Cell Res. 265, 64-72.
59. Zhen, X., Wei, L., Wu, Q., Zhang, Y., and Chen, Q. (2001). Mitogen-activated protein kinase p38 mediates regulation of chondrocyte differentiation by parathyroid hormone. J. Biol. Chem. 276, 4879-4885.
60. Zuscik, M.J., Puzas, J.E., Rosier, R.N., Gunter, K.K., and Gunter, T.E. (1994). Cyclic-AMP-dependent protein kinase activity is not required by parathyroid hormone to stimulate phosphoinositide signaling in chondrocytes but is required to transduce the hormone's proliferative effect. Arch. Biochem. Biophys. 315, 352-361.