Skip to main content

Advertisement

SpringerLink
Log in

Parathyroid Hormone Induces Receptor Activity Modifying Protein-3 (RAMP3) Expression Primarily Via 3′,5′-Cyclic Adenosine Monophosphate Signaling in Osteoblasts

  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Parathyroid hormone (PTH) has significant anabolic and catabolic effects on bone. We hypothesize that PTH-induced primary response genes are important determinants of osteoblast function. PTH induces osteoblastic gene expression through PTHR1, a heptahelical receptor that triggers cyclic adenosine monophosphate (cAMP)–protein kinase A (PKA), protein kinase C (PKC), and calcium signaling. By using representational difference analysis we found that receptor activity modifying protein-3 (RAMP3) is a PTH-induced primary response gene in osteoblastic cells. RAMP3 is a coactivator that directs calcitonin receptor (CTR) and CTR-like receptor (CRLR) glycosylation, trafficking, and ligand-binding specificity. Our purpose was to characterize PTH-induced RAMP3 messenger ribonucleic acid (mRNA) levels in primary mouse osteoblasts (MOBs) and to determine which signaling pathway mediates this effect. 10 nM PTH maximally induced RAMP3 mRNA levels in MOBs at 4 hours. Protein synthesis inhibition with 3 μg/mL cycloheximide did not affect PTH-induced RAMP3 mRNA levels. Selective activation of cAMP-PKA signaling with, 10 μM forskolin (FSK) and PKC signaling with 1 μM phorbol 12-myristate 13-acetate (PMA) significantly increased RAMP3 mRNA levels, whereas 1 μM ionomycin (a calcium ionophore) had no effect. Pretreatment with 30 μM H89, a PKA inhibitor, significantly blocked PTH- and FSK-induced RAMP3 mRNA levels. Pretreatment with 1 μM PMA, which depletes PKC, had no effect on PTH- and FSK-induced RAMP3 mRNA levels but blocked PMA-induced RAMP3 mRNA levels. 100 nM PTH (3-34), which activates PKC and calcium but not PKA, had no effect on RAMP3 mRNA levels. These findings indicate that RAMP3 is a PTH-induced primary response gene in primary MOBs and that PTH regulates RAMP3 gene expression primarily through the cAMP-PKA pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. CJ Rosen (2003) ArticleTitleThe cellular and clinical parameters of anabolic therapy for osteoporosis Crit Rev Eukaryot Gene Expr 13 25–38 Occurrence Handle10.1615/CritRevEukaryotGeneExpr.v13.i1.30 Occurrence Handle12839095

    Article  PubMed  Google Scholar 

  2. JS Finkelstein A Klibanski AL Arnold TL Toth MD Hornstein RM Neer (1998) ArticleTitlePrevention of estrogen deficiency-related bone loss with human parathyroid hormone-(1-34): a randomized controlled trial JAMA 280 1067–1073 Occurrence Handle10.1001/jama.280.12.1067 Occurrence Handle9757854

    Article  PubMed  Google Scholar 

  3. AB Hodsman LJ Fraher PH Watson T Ostbye LW Stitt JD Adachi DH Taves D Drost (1997) ArticleTitleA randomized controlled trial to compare the efficacy of cyclical parathyroid hormone versus cyclical parathyroid hormone and sequential calcitonin to improve bone mass in postmenopausal women with osteoporosis J Clin Endocrinol Metab 82 620–628 Occurrence Handle10.1210/jc.82.2.620 Occurrence Handle9024265

    Article  PubMed  Google Scholar 

  4. NE Lane S Sanchez GW Modin HK Genant E Pierini CD Arnaud (1998) ArticleTitleParathyroid hormone treatment can reverse corticosteroid-induced osteoporosis Results of a randomized controlled clinical trial. J Clin Invest 102 1627–1633

    Google Scholar 

  5. R Lindsay J Nieves C Formica E Henneman L Woelfert V Shen D Dempster F Cosman (1997) ArticleTitleRandomised controlled study of effect of parathyroid hormone on vertebral-bone mass and fracture incidence among postmenopausal women on oestrogen with osteoporosis Lancet 350 550–555 Occurrence Handle10.1016/S0140-6736(97)02342-8 Occurrence Handle9284777

    Article  PubMed  Google Scholar 

  6. R Neer D Slovic M Daly C Lo SH Doppelt JTJ Potts S Nussbaum (1991) ArticleTitleTreatment of postmenopausal osteoporosis with daily PTH plus calcitrol. J Endocrinol Invest (Suppl) 3 50

    Google Scholar 

  7. J Reeve A Mitchell M Tellez P Hulme JR Green B Wardley-Smith R Mitchell (2001) ArticleTitleTreatment with parathyroid peptides and estrogen replacement for severe postmenopausal vertebral osteoporosis: prediction of long-term responses in spine and femur J Bone Miner Metab 19 102–114 Occurrence Handle10.1007/s007740170048 Occurrence Handle11281158

    Article  PubMed  Google Scholar 

  8. T Sone M Fukunaga S Ono T Nishiyama (1995) ArticleTitleA small dose of human parathyroid hormone(1-34) increased bone mass in the lumbar vertebrae in patients with senile osteoporosis Miner Electrolyte Metab 21 232–235 Occurrence Handle7565456

    PubMed  Google Scholar 

  9. C Deal (2004) ArticleTitleThe use of intermittent human parathyroid hormone as a treatment for osteoporosis Curr Rheumatol Rep 6 49–58 Occurrence Handle14713402

    PubMed  Google Scholar 

  10. JM Hock I Gera (1992) ArticleTitleEffects 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 Occurrence Handle1532281

    PubMed  Google Scholar 

  11. H Juppner AB Abou-Samra M Freeman XF Kong E Schipani J Richards LF Kolakowski SuffixJr. J Hock JT Potts SuffixJr. HM Kronenberg (1991) ArticleTitleA G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide Science 254 1024–1026 Occurrence Handle1658941

    PubMed  Google Scholar 

  12. AB Abou-Samra H Juppner T Force MW Freeman XF Kong E Schipani P Urena J Richards JV Bonventre JT Potts SuffixJr. HM Kronenberg GV Segre (1992) ArticleTitleExpression cloning of a common receptor for parathyroid hormone and parathyroid hormone-related peptide from rat osteoblast-like cells: a single receptor stimulates intracellular accumulation of both cAMP and inositol trisphosphates and increases intracellular free calcium Proc Natl Acad Sci USA 89 2732–2736 Occurrence Handle1313566

    PubMed  Google Scholar 

  13. FR Bringhurst H Juppner J Guo P Urena JT Potts SuffixJr. HM Kronenberg AB Abou-Samra GV Segre (1993) ArticleTitleCloned, 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 Occurrence Handle10.1210/en.132.5.2090 Occurrence Handle8386606

    Article  PubMed  Google Scholar 

  14. WF Schwindinger J Fredericks L Watkins H Robinson JM Bathon M Pines LJ Suva MA Levine (1998) ArticleTitleCoupling of the PTH/PTHrP receptor to multiple G-proteins Direct demonstration of receptor activation of Gs, Gq/11, and Gi(1) by [alpha-32P]GTP-gama-azidoanilide photoaffinity labeling. Endocrine 8 201–209

    Google Scholar 

  15. NC Partridge SR Bloch AT Pearman (1994) ArticleTitleSignal transduction pathways mediating parathyroid hormone regulation of osteoblastic gene expression J Cell Biochem 55 321–327 Occurrence Handle10.1002/jcb.240550308 Occurrence Handle7962163

    Article  PubMed  Google Scholar 

  16. JT Swarthout RC D’Alonzo N Selvamurugan NC Partridge (2002) ArticleTitleParathyroid hormone-dependent signaling pathways regulating genes in bone cells Gene 282 1–17 Occurrence Handle11814673

    PubMed  Google Scholar 

  17. JC Clohisy DK Scott KD Brakenhoff CO Quinn NC Partridge (1992) ArticleTitleParathyroid hormone induces c-fos and c-jun messenger RNA in rat osteoblastic cells Mol Endocrinol 6 1834–1842 Occurrence Handle10.1210/me.6.11.1834 Occurrence Handle1480173

    Article  PubMed  Google Scholar 

  18. R Civitelli KA Hruska JJ Jeffrey AJ Kahn LV Avioli NC Partridge (1989) ArticleTitleSecond messenger signaling in the regulation of collagenase production by osteogenic sarcoma cells Endocrinology 124 IssueID6 2928–2934 Occurrence Handle2542004

    PubMed  Google Scholar 

  19. DK Scott KD Brakenhoff JC Clohisy CO Quinn NC Partridge (1992) ArticleTitleParathyroid hormone induces transcription of collagenase in rat osteoblastic cells by a mechanism using cyclic adenosine 3′,5′-monophosphate and requiring protein synthesis Mol Endocrinol 6 2153–2159 Occurrence Handle10.1210/me.6.12.2153 Occurrence Handle1337147

    Article  PubMed  Google Scholar 

  20. EM Greenfield SM Shaw SA Gornik MA Banks (1995) ArticleTitleAdenyl cyclase and interleukin 6 are downstream effectors of parathyroid hormone resulting in stimulation of bone resorption J Clin Invest 96 1238–1244 Occurrence Handle7657797

    PubMed  Google Scholar 

  21. J Kano T Sugimoto M Fukase K Chihara (1992) ArticleTitleThe direct involvement of cAMP-dependent protein kinase in the regulation of collagen synthesis by parathyroid hormone (PTH) and PTH-related peptide in osteoblast-like osteosarcoma cells (UMR-106) Biochem Biophys Res Commun 184 525–529 Occurrence Handle10.1016/0006-291X(92)91226-G Occurrence Handle1314599

    Article  PubMed  Google Scholar 

  22. BE Kream D LaFrancis DN Petersen C Woody S Clark DW Rowe A Lichtler (1993) ArticleTitleParathyroid hormone represses α 1(1) collagen promoter activity in cultured calvariae from neonatal transgenic mice Mol Endocrinol 7 399–408 Occurrence Handle10.1210/me.7.3.399 Occurrence Handle8483479

    Article  PubMed  Google Scholar 

  23. S Tetradis O Bezouglaia A Tsingotjidou (2001) ArticleTitleParathyroid hormone induces expression of the nuclear orphan receptor Nurr1 in bone cells Endocrinology 142 663–670 Occurrence Handle10.1210/en.142.2.663 Occurrence Handle11159837

    Article  PubMed  Google Scholar 

  24. S Tetradis O Bezouglaia A Tsingotjidou A Vila (2001) ArticleTitleRegulation of the nuclear orphan receptor Nur77 in bone by parathyroid hormone Biochem Biophys Res Commun 281 913–916 Occurrence Handle10.1006/bbrc.2001.4459 Occurrence Handle11237747

    Article  PubMed  Google Scholar 

  25. FQ Pirih JM Nervina L Pham T Aghaloo S Tetradis (2003) ArticleTitleParathyroid hormone induces the nuclear orphan receptor NOR-1 in osteoblasts Biochem Biophys Res Commun 306 144–150 Occurrence Handle10.1016/S0006-291X(03)00931-8 Occurrence Handle12788080

    Article  PubMed  Google Scholar 

  26. IC Ozkurt FQ Pirih S Tetradis (2004) ArticleTitleParathyroid hormone induces E4bp4 messenger ribonucleic acid expression primarily through cyclic adenosine 3′,5′-monophosphate signaling in osteoblasts Endocrinology 145 3696–3703 Occurrence Handle10.1210/en.2003-1436 Occurrence Handle15087429

    Article  PubMed  Google Scholar 

  27. A Tsingotjidou JM Nervina L Pham O Bezouglaia S Tetradis (2002) ArticleTitleParathyroid hormone induces RGS-2 expression by a cyclic adenosine 3′,5′-monophosphate-mediated pathway in primary neonatal murine osteoblasts Bone 30 677–684 Occurrence Handle10.1016/S8756-3282(02)00698-1 Occurrence Handle11996904

    Article  PubMed  Google Scholar 

  28. S Tetradis JM Nervina K Nemoto BE Kream (1998) ArticleTitleParathyroid hormone induces expression of the inducible cAMP early represser in osteoblastic MC3T3-E1 cells an mouse calvariae J Bone Miner Res 13 1846–1851 Occurrence Handle9844102

    PubMed  Google Scholar 

  29. JM Nervina S Tetradis YF Huang D Harrison C Molina BE Kream (2003) ArticleTitleExpression of inducible cAMP early represser is coupled to the cAMP-protein kinase A signaling pathway in osteoblasts Bone 32 483–490 Occurrence Handle10.1016/S8756-3282(03)00056-5 Occurrence Handle12753864

    Article  PubMed  Google Scholar 

  30. PM Sexton A Albiston M Morfis N Tilakaratne (2001) ArticleTitleReceptor activity modifying proteins Cell Signal 13 73–83 Occurrence Handle10.1016/S0898-6568(00)00143-1 Occurrence Handle11257451

    Article  PubMed  Google Scholar 

  31. D Naot KE Callon A Grey GJ Cooper IR Reid J Cornish (2001) ArticleTitleA potential role for adrenomedullin as a local regulator of bone growth Endocrinology 142 1849–1857 Occurrence Handle10.1210/en.142.5.1849 Occurrence Handle11316750

    Article  PubMed  Google Scholar 

  32. B Uzan MC Vernejoul Particlede M Cressent (2004) ArticleTitleRAMPs and CRLR expressions in osteoblastic cells after dexamethasone treatment Biochem Biophys Res Commun 321 802–808 Occurrence Handle10.1016/j.bbrc.2004.07.037 Occurrence Handle15358098

    Article  PubMed  Google Scholar 

  33. HR Herschman (1991) ArticleTitlePrimary response genes induced by growth factors and tumor promoters Annu Rev Biochem 60 281–319 Occurrence Handle10.1146/annurev.bi.60.070191.001433 Occurrence Handle1883198

    Article  PubMed  Google Scholar 

  34. T Chijiwa A Mishima M Hagiwara M Sano K Hayashi T Inoue K Naito T Toshioka H Hidaka (1990) ArticleTitleInhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-Bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H89), of PC12D pheochromocytoma cells J Biol Chem 265 5267–5272 Occurrence Handle2156866

    PubMed  Google Scholar 

  35. PJ Blackshear LA Witters PA Girard JF Kuo SN Quamo (1985) ArticleTitleGrowth factor-stimulated protein phosphorylation in 3T3-L1 cells Evidence for protein kinase C-dependent and independent pathways. J Biol Chem 260 13304–13315

    Google Scholar 

  36. S Tetradis CC Pilbeam Y Liu HR Herschman BE Kream (1997) ArticleTitleParathyroid hormone increases prostaglandin G/H synthase-2 transcription by a cyclic adenosine 3′5′-monophosphate-mediated pathway in murine osteoblastic MC3T3-E1 cells Endocrinology 138 3594–3600 Occurrence Handle10.1210/en.138.9.3594 Occurrence Handle9275040

    Article  PubMed  Google Scholar 

  37. A Fujimori S Cheng LV Avioli R Civitelli (1991) ArticleTitleDissociation of second messenger activation by parathyroid hormone fragments in osteosarcoma cells Endocrinology 128 3032–3039 Occurrence Handle1645259

    PubMed  Google Scholar 

  38. EM Greenfield MC Horowitz SA Lavish (1996) ArticleTitleStimulation by parathyroid hormone of interleukin-6 and leukemia inhibitory factor expression in osteoblasts is an immediate-early gene response induced by cAMP signal transduction J Biol Chem 271 10984–10989 Occurrence Handle10.1074/jbc.271.18.10984 Occurrence Handle8631918

    Article  PubMed  Google Scholar 

  39. IC Ozkurt S Tetradis (2003) ArticleTitleParathyroid hormone-induced E4BP4/NFIL3 down-regulates transcription in osteoblasts J Biol Chem 278 26803–26809 Occurrence Handle10.1074/jbc.M212652200 Occurrence Handle12743120

    Article  PubMed  Google Scholar 

  40. S Tetradis CC Pilbeam Y Liu BE Kream (1996) ArticleTitleParathyroid hormone induces prostaglandin G/H synthase-2 expression by a cyclic adenosine 3′,5′-monophosphate-mediated pathway in the murine osteoblastic cell line MC3T3-E1 Endocrinology 137 5435–5440 Occurrence Handle10.1210/en.137.12.5435 Occurrence Handle8940368

    Article  PubMed  Google Scholar 

  41. JD Clohisy DK Scott KD Brakenhoff NC Partridge (1991) ArticleTitleParathyroid hormone stimulation of c-Fos and cJun mRNA in osteoblastic cells: an immediate early response J Bone Miner Res 6 IssueIDS1 S:134

    Google Scholar 

  42. NJ Fraser A Wise J Brown LM McLatchie MJ Main SM Foord (1999) ArticleTitleThe amino terminus of receptor activity modifying proteins is a critical determinant of glycosylation state and ligand binding of calcitonin receptor-like receptor Mol Pharmacol 55 1054–1059 Occurrence Handle10347248

    PubMed  Google Scholar 

  43. K Kuwasako K Kitamura K Ito T Uemura Y Yanagita J Kato T Sakata T Eto (2001) ArticleTitleThe seven amino acids of human RAMP2 (86) and RAMP3 (59) are critical for agonist binding to human adrenomedullin receptors J Biol Chem 276 49459–49465 Occurrence Handle10.1074/jbc.M108369200 Occurrence Handle11591721

    Article  PubMed  Google Scholar 

  44. ET Zumpe N Tilakaratne NJ Fraser G Christopoulos SM Foord TM Sexton (2000) ArticleTitleMultiple ramp domains are required for generation of amylin receptor phenotype from the calcitonin receptor gene product Biochem Biophys Res Commun 267 368–372 Occurrence Handle10.1006/bbrc.1999.1943 Occurrence Handle10623626

    Article  PubMed  Google Scholar 

  45. K Husmann PM Sexton JA Fischer W Born (2000) ArticleTitleMouse receptor-activity-modifying proteins 1, -2 and -3: amino acid sequence, expression and function Mol Cell Endocrinol 162 35–43 Occurrence Handle10.1016/S0303-7207(00)00212-4 Occurrence Handle10854696

    Article  PubMed  Google Scholar 

  46. LM McLatchie NJ Fraser MJ Main A Wise J Brown N Thompson R Solari MG Lee SM Foord (1998) ArticleTitleRAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor Nature 393 333–339 Occurrence Handle10.1038/30666 Occurrence Handle9620797

    Article  PubMed  Google Scholar 

  47. DR Poyner PM Sexton I Marshall DM Smith R Quirion W Born R Muff JA Fischer SM Foord (2002) ArticleTitleInternational Union of Pharmacology XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev 54 233–246

    Google Scholar 

  48. G Christopoulos KJ Perry M Morfis N Tilakaratne Y Gao NJ Fraser MJ Main SM Foord PM Sexton (1999) ArticleTitleMultiple amylin receptors arise from receptor activity-modifying protein interaction with the calcitonin receptor gene product Mol Pharmacol 56 235–242 Occurrence Handle10385705

    PubMed  Google Scholar 

  49. DL Hay G Christopoulos A Christopoulos PM Sexton (2004) ArticleTitleAmylin receptors: molecular composition and pharmacology Biochem Soc Trans 32 865–867 Occurrence Handle10.1042/BST0320865 Occurrence Handle15494035

    Article  PubMed  Google Scholar 

  50. N Tilakaratne G Christopoulos ET Zumpe SM Foord PM Sexton (2000) ArticleTitleAmylin receptor phenotypes derived from human calcitonin receptor/RAMP coexpression exhibit pharmacological differences dependent on receptor isoform and host cell environment J Pharmacol Exp Ther 294 61–72 Occurrence Handle10871296

    PubMed  Google Scholar 

  51. K Kuwasako Y Shimekake M Masuda K Nakahara T Yoshida M Kitaura K Kitamura T Eto T Sakata (2000) ArticleTitleVisualization of the calcitonin receptor-like receptor and its receptor activity-modifying proteins during internalization and recycling J Biol Chem 275 29602–29609 Occurrence Handle10.1074/jbc.M004534200 Occurrence Handle10882736

    Article  PubMed  Google Scholar 

  52. R Muff K Leuthauser N Buhlmann SM Foord JA Fischer W Born (1998) ArticleTitleReceptor activity modifying proteins regulate the activity of a calcitonin gene-related peptide receptor in rabbit aortic endothelial cells FEES Lett 441 366–368 Occurrence Handle10.1016/S0014-5793(98)01587-7

    Article  Google Scholar 

  53. R Neher B Riniker R Maier PG Byfield TV Gudmundsson I MacIntyre (1968) ArticleTitleHuman calcitonin Nature 220 984–986 Occurrence Handle5701856

    PubMed  Google Scholar 

  54. GC Nicholson JM Moseley PM Sexton FA Mendelsohn TJ Martin (1986) ArticleTitleAbundant calcitonin receptors in isolated rat osteoclasts Biochemical and autoradiographic characterization. J Clin Invest 78 355–360

    Google Scholar 

  55. JM Quinn M Morfis MH Lam J Elliott V Kartsogiannis ED Williams MT Gillespie TJ Martin PM Sexton (1999) ArticleTitleCalcitonin receptor antibodies in the identification of osteoclasts Bone 25 1–8 Occurrence Handle10.1016/S8756-3282(99)00094-0 Occurrence Handle10423015

    Article  PubMed  Google Scholar 

  56. J Cornish KE Callon U Bava SA Kamona GJ Cooper IR Reid (2001) ArticleTitleEffects of calcitonin, amylin, and calcitonin gene-related peptide on osteoclast development Bone 29 162–168 Occurrence Handle10.1016/S8756-3282(01)00494-X Occurrence Handle11502478

    Article  PubMed  Google Scholar 

  57. J Cornish KE Callon CQ Lin CL Xiao GD Gamble GJ Cooper IR Reid (1999) ArticleTitleComparison of the effects of calcitonin gene-related peptide and amylin on osteoblasts J Bone Miner Res 14 1302–1309 Occurrence Handle10457262

    PubMed  Google Scholar 

  58. J Cornish KE Callon CQ Lin CL Xiao TB Mulvey DH Coy GJ Cooper IR Reid (1998) ArticleTitleDissociation of the effects of amylin on osteoblast proliferation and bone resorption Am J Physiol 274 E827–833 Occurrence Handle9612240

    PubMed  Google Scholar 

  59. J Cornish KE Callon GJ Cooper IR Reid (1995) ArticleTitleAmylin stimulates osteoblast proliferation and increases mineralized bone volume in adult mice Biochem Biophys Res Commun 207 133–139 Occurrence Handle10.1006/bbrc.1995.1163 Occurrence Handle7857256

    Article  PubMed  Google Scholar 

  60. R Ballica K Valentijn A Khachatryan S Guerder S Kapadia C Gundberg J Gilligan RA Flavell A Vignery (1999) ArticleTitleTargeted expression of calcitonin gene-related peptide to osteoblasts increases bone density in mice J Bone Miner Res 14 1067–1074 Occurrence Handle10404006

    PubMed  Google Scholar 

  61. NE Lane S Sanchez GW Modin HK Genant E Pierini CD Arnaud (2000) ArticleTitleBone mass continues to increase at the hip after parathyroid hormone treatment is discontinued in glucocorticoid-induced osteoporosis: results of a randomized controlled clinical trial J Bone Miner Res 15 944–951 Occurrence Handle10804025

    PubMed  Google Scholar 

  62. DW Dempster F Cosman ES Kurland H Zhou J Nieves L Woelfert E Shane K Plavetic R Muller J Bilezikian R Lindsay (2001) ArticleTitleEffects of daily treatment with parathyroid hormone on bone micro architecture and turnover in patients with osteoporosis: a paired biopsy study J Bone Miner Res 16 1846–1853 Occurrence Handle11585349

    PubMed  Google Scholar 

  63. LM Montuenga A Martinez MJ Miller EJ Unsworth F Cuttitta (1997) ArticleTitleExpression of adrenomedullin and its receptor during embryogenesis suggests autocrine or paracrine modes of action Endocrinology 138 440–451 Occurrence Handle10.1210/en.138.1.440 Occurrence Handle8977434

    Article  PubMed  Google Scholar 

  64. J Cornish KE Callon DH Coy NY Jiang L Xiao GJ Cooper IR Reid (1997) ArticleTitleAdrenomedullin is a potent stimulator of osteoblastic activity in vitro and in vivo Am J Physiol 273 E1113–1120 Occurrence Handle9435526

    PubMed  Google Scholar 

  65. A Christopoulos G Christopoulos M Morfis M Udawela M Laburthe A Couvineau K Kuwasako N Tilakaratne PM Sexton (2003) ArticleTitleNovel receptor partners and function of receptor activity-modifying proteins J Biol Chem 278 3293–3297 Occurrence Handle10.1074/jbc.C200629200 Occurrence Handle12446722

    Article  PubMed  Google Scholar 

  66. M Flahaut BC Rossier D Firsov (2002) ArticleTitleRespective roles of calcitonin receptor-like receptor (CRLR) and receptor activity-modifying proteins (RAMP) in cell surface expression of CRLR/RAMP heterodimeric receptors J Biol Chem 277 14731–14737 Occurrence Handle11854283

    PubMed  Google Scholar 

  67. A Bisello Z Greenberg V Behar M Rosenblatt LJ Suva M Chorev (1996) ArticleTitleRole of glycosylation in expression and function of the human parathyroid hormone/parathyroid hormone-related protein receptor Biochemistry 35 15890–15895 Occurrence Handle10.1021/bi962111+ Occurrence Handle8961954

    Article  PubMed  Google Scholar 

  68. R Rizzoli JP Bonjour (1989) ArticleTitleEffects of lectins and tunicamycin on cAMP response to parathyroid hormone Am J Physiol 256 E80–86 Occurrence Handle2536232

    PubMed  Google Scholar 

  69. AT Zhou I Assil AB Abou-Samra (2000) ArticleTitleRole of asparagine-linked oligosaccharides in the function of the rat PTH/PTHrP receptor Biochemistry 39 6514–6520 Occurrence Handle10.1021/bi992706f Occurrence Handle10828967

    Article  PubMed  Google Scholar 

  70. Bomberger JM, Parameswaran N, Hall CS, Aiyar N, Spielman WS (2004) Novel function for receptor activity modifying proteins (RAMPs) in post-endocytic receptor trafficking. J Biol Chem Epub Dec 21

Download references

Acknowledgement

This research was supported by NIH/NIDCR training grant K08 DE0 14881 (J.M.N.) and AADR Student Research Fellowship (E.P.).

Author information

Authors and Affiliations

  1. Section of Orthodontics, UCLA School of Dentistry, Los Angeles, CA 90095-1668, USA

    E. Phelps & J. M. Nervina

  2. Division of Diagnostic and Surgical Sciences, UCLA School of Dentistry, Los Angeles, CA 90095-1668, USA

    O. Bezouglaia & S. Tetradis

Authors
  1. E. Phelps
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. Bezouglaia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Tetradis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. Nervina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. M. Nervina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Phelps, E., Bezouglaia, O., Tetradis, S. et al. Parathyroid Hormone Induces Receptor Activity Modifying Protein-3 (RAMP3) Expression Primarily Via 3′,5′-Cyclic Adenosine Monophosphate Signaling in Osteoblasts. Calcif Tissue Int 77, 96–103 (2005). https://doi.org/10.1007/s00223-004-0239-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-004-0239-1

Keywords

Search

Navigation