Expression of PTH1R constructs in LLC-PK1 cells: Protein nuclear targeting is mediated by the PTH1R NLS

Bone

Volumn 41, Issue 4, 2007, Pages 603-610

  Patterson, Eric K ^a   Watson, Patricia H ^a   Hodsman, Anthony B ^a   Hendy, Geoffrey N ^b   Canaff, Lucie ^b   Bringhurst, F Richard ^c   Poschwatta, Clare H ^d   Fraher, Laurence J ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b ROYAL VICTORIA HOSPITAL   (Canada)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d NONE

Author keywords

G protein coupled receptors; Nuclear localization sequence; Nuclear trafficking; Parathyroid hormone receptor

Indexed keywords

COMPLEMENTARY DNA; CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; GREEN FLUORESCENT PROTEIN; PARATHYROID HORMONE RECEPTOR; PARATHYROID HORMONE RECEPTOR 1; PHENYLALANYLPHENYLALANYLVALYLALANYLISOLEUCYLTYROSYLCYSTEINYLPHENYLALANYLCYSTEINY LASPARAGINYLGLYCYLGLUTAMYLVALYLGLUTAMINYLALANYLGLUTAMYLISOLEUCINAMIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DECONVOLUTION FLUORESCENCE MICROSCOPY; EXPRESSION VECTOR; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; IN VITRO STUDY; INTESTINE; KIDNEY; LIVER; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OSTEOBLAST; OVARY; PARATHYROID HORMONE RELEASE; PROTEIN EXPRESSION; PROTEIN TARGETING; RAT; TISSUE DISTRIBUTION; UTERUS;

ANIMALS; CELL LINE; CYCLIC AMP; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; RATS; RECEPTOR, PARATHYROID HORMONE, TYPE 1;

EID: 34548526137     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2007.04.201     Document Type: Article

References (38)

1. Gardella T.J., and Juppner H. Molecular properties of the PTH/PTHrP receptor. Trends Endocrinol. Metab. 12 (2001) 210-217
2. Abou-Samra A.B., Juppner H., Force T., et al. Expression 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. U. S. A. 89 (1992) 2732-2736
3. Bringhurst F.R., Juppner H., Guo J., et al. Cloned, stably expressed parathyroid hormone (PTH)/PTH-related peptide receptors activate multiple messenger signals and biological responses in LLC-PK1 kidney cells. Endocrinology 132 (1993) 2090-2098
4. Jouishomme H., Whitfield J.F., Gagnon L., et al. Further definition of the protein kinase C activation domain of the parathyroid hormone. J. Bone Miner. Res. 9 (1994) 943-949
5. Neugebauer W., Barbier J.R., Sung W.L., Whitfield J.F., and Willick G.E. Solution structure and adenylyl cyclase stimulating activities of C-terminal truncated human parathyroid hormone analogues. Biochemistry 34 (1995) 8835-8842
6. Whitfield J.F., Isaacs R.J., Chakravarthy B., et al. Stimulation of protein kinase C activity in cells expressing human parathyroid hormone receptors by C- and N-terminally truncated fragments of parathyroid hormone 1-34. J. Bone Miner. Res. 16 (2001) 441-447
7. Kronenberg HM, Lanske B, Kovacs CS, et al. Functional analysis of the PTH/PTHrP network of ligands and receptors. Recent Prog Horm Res 1998;53:283, 301 [discussion 301-3].
8. Calvi L.M., Sims N.A., Hunzelman J.L., et al. Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J. Clin. Invest. 107 (2001) 277-286
9. Watson P.H., Fraher L.J., Hendy G.N., et al. Nuclear localization of the type 1 PTH/PTHrP receptor in rat tissues. J. Bone Miner. Res. 15 (2000) 1033-1044
10. Watson P.H., Fraher L.J., Natale B.V., Kisiel M., Hendy G.N., and Hodsman A.B. Nuclear localization of the type 1 parathyroid hormone/parathyroid hormone-related peptide receptor in MC3T3-E1 cells: association with serum-induced cell proliferation. Bone 26 (2000) 221-225
11. Faucheux C., Horton M.A., and Price J.S. Nuclear localization of type I parathyroid hormone/parathyroid hormone-related protein receptors in deer antler osteoclasts: evidence for parathyroid hormone-related protein and receptor activator of NF-kappaB-dependent effects on osteoclast formation in regenerating mammalian bone. J. Bone Miner. Res. 17 (2002) 455-464
12. Lu D., Yang H., Shaw G., and Raizada M.K. Angiotensin II-induced nuclear targeting of the angiotensin type 1 (AT1) receptor in brain neurons. Endocrinology 139 (1998) 365-375
13. Chen R., Mukhin Y.V., Garnovskaya M.N., et al. A functional angiotensin II receptor-GFP fusion protein: evidence for agonist-dependent nuclear translocation. Am. J. Physiol.: Renal Physiol. 279 (2000) F440-F448
14. Lee D.K., Lanca A.J., Cheng R., et al. Agonist-independent nuclear localization of the apelin, angiotensin AT1, and bradykinin B2 receptors. J. Biol. Chem. 279 (2004) 7901-7908
15. O'Malley K.L., Jong Y.J., Gonchar Y., Burkhalter A., and Romano C. Activation of metabotropic glutamate receptor mGlu5 on nuclear membranes mediates intranuclear Ca2+ changes in heterologous cell types and neurons. J. Biol. Chem. 278 (2003) 28210-28219
16. Boivin B., Chevalier D., Villeneuve L.R., Rousseau E., and Allen B.G. Functional endothelin receptors are present on nuclei in cardiac ventricular myocytes. J. Biol. Chem. 278 (2003) 29153-29163
17. Boivin B., Lavoie C., Vaniotis G., et al. Functional beta-adrenergic receptor signalling on nuclear membranes in adult rat and mouse ventricular cardiomyocytes. Cardiovasc. Res. 71 (2006) 69-78
18. Robbins J., Dilworth S.M., Laskey R.A., and Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64 (1991) 615-623
19. Moroianu J. Molecular mechanisms of nuclear protein transport. Crit. Rev. Eukaryot. Gene Expr. 7 (1997) 61-72
20. Jans D.A., and Hubner S. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol. Rev. 76 (1996) 651-685
21. Kitamura R., Sekimoto T., Ito S., et al. Nuclear import of Epstein-Barr virus nuclear antigen 1 mediated by NPI-1 (importin alpha5) is up- and down-regulated by phosphorylation of the nuclear localization signal for which Lys379 and Arg380 are essential. J. Virol. 80 (2006) 1979-1991
22. Goldring S.R., Dayer J.M., Ausiello D.A., and Krane S.M. A cell strain cultured from porcine kidney increases cyclic AMP content upon exposure to calcitonin or vasopressin. Biochem. Biophys. Res. Commun. 83 (1978) 434-440
23. Hull R.N., Cherry W.R., and Weaver G.W. The origin and characteristics of a pig kidney cell strain, LLC-PK. In Vitro 12 (1976) 670-677
24. Pausova Z., Bourdon J., Clayton D., et al. Cloning of a parathyroid hormone/parathyroid hormone-related peptide receptor (PTHR) cDNA from a rat osteosarcoma (UMR 106) cell line: chromosomal assignment of the gene in the human, mouse, and rat genomes. Genomics 20 (1994) 20-26
25. Higuchi R. Using PCR to engineer DNA. In: Erlich H.A. (Ed). PCR technology: principles and applications for DNA amplification. First ed (1989), Stockton Press, New York 61-70
26. Gardella T.J., Juppner H., Wilson A.K., et al. Determinants of [Arg2]PTH-(1-34) binding and signaling in the transmembrane region of the parathyroid hormone receptor. Endocrinology 135 (1994) 1186-1194
27. Lee C., Luck M.D., Juppner H., Potts Jr. J.T., Kronenberg H.M., and Gardella T.J. Homolog-scanning mutagenesis of the parathyroid hormone (PTH) receptor reveals PTH-(1-34) binding determinants in the third extracellular loop. Mol. Endocrinol. 9 (1995) 1269-1278
28. Gardella T.J., Luck M.D., Fan M.H., and Lee C. Transmembrane residues of the parathyroid hormone (PTH)/PTH-related peptide receptor that specifically affect binding and signaling by agonist ligands. J. Biol. Chem. 271 (1996) 12820-12825
29. Adams A.E., Bisello A., Chorev M., Rosenblatt M., and Suva L.J. Arginine 186 in the extracellular N-terminal region of the human parathyroid hormone 1 receptor is essential for contact with position 13 of the hormone. Mol. Endocrinol. 12 (1998) 1673-1683
30. Mannstadt M., Juppner H., and Gardella T.J. Receptors for PTH and PTHrP: their biological importance and functional properties. Am. J. Physiol. 277 (1999) F665-F675
31. Huang H.D., Lee T.Y., Tzeng S.W., and Horng J.T. KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites. Nucleic Acids Res. 33 (2005) W226-W229
32. Huang H.D., Lee T.Y., Tzeng S.W., et al. Incorporating hidden Markov models for identifying protein kinase-specific phosphorylation sites. J. Comput. Chem. 26 (2005) 1032-1041
33. Tawfeek H.A., Qian F., and Abou-Samra A.B. Phosphorylation of the receptor for PTH and PTHrP is required for internalization and regulates receptor signaling. Mol. Endocrinol. 16 (2002) 1-13
34. Malecz N., Bambino T., Bencsik M., and Nissenson R.A. Identification of phosphorylation sites in the G protein-coupled receptor for parathyroid hormone. Receptor phosphorylation is not required for agonist-induced internalization. Mol. Endocrinol. 12 (1998) 1846-1856
35. Tazawa H., Takahashi S., and Zilliacus J. Interaction of the parathyroid hormone receptor with the 14-3-3 protein. Biochim. Biophys. Acta 1620 (2003) 32-38
36. Robinson K., Jones D., Patel Y., et al. Mechanism of inhibition of protein kinase C by 14-3-3 isoforms. 14-3-3 isoforms do not have phospholipase A2 activity. Biochem. J. 299 Pt 3 (1994) 853-861
37. Aitken A., Howell S., Jones D., et al. Post-translationally modified 14-3-3 isoforms and inhibition of protein kinase C. Mol. Cell. Biochem. 149-150 (1995) 41-49
38. Joun H., Lanske B., Karperien M., Qian F., Defize L., and Abou-Samra A. Tissue-specific transcription start sites and alternative splicing of the parathyroid hormone (PTH)/PTH-related peptide (PTHrP) receptor gene: a new PTH/PTHrP receptor splice variant that lacks the signal peptide. Endocrinology 138 (1997) 1742-1749