EBP50 inhibits the anti-mitogenic action of the parathyroid hormone type 1 receptor in vascular smooth muscle cells

Journal of Molecular and Cellular Cardiology

Volumn 49, Issue 6, 2010, Pages 1012-1021

  Song, Gyun Jee ^a   Barrick, Stacey ^a   Leslie, Kristen L ^a   Sicari, Brian ^a   Fiaschi Taesch, Nathalie M ^a   Bisello, Alessandro ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Cyclic AMP; Ezrin radixin moesin binding phosphoprotein (EBP50); Neointima; Parathyroid hormone type 1 receptor; Parathyroid hormone related protein; Proliferation; Restenosis; Vascular smooth muscle cell

Indexed keywords

ADAPTOR PROTEIN; CYCLIC AMP; CYCLIN DEPENDENT KINASE INHIBITOR 1B; EZRIN RADIXIN MOESIN BINDING PHOSPHOPROTEIN; PARATHYROID HORMONE RECEPTOR 1; PARATHYROID HORMONE RELATED PROTEIN; UNCLASSIFIED DRUG;

ANGIOPLASTY; ANIMAL CELL; AORTA MEDIA; ARTICLE; BLOOD VESSEL INJURY; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CELL LINE; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM; HUMAN; HUMAN CELL; INTERNALIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN MOTIF; PROTEIN TRANSPORT; RAT; RESTENOSIS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASCULAR TISSUE;

ANGIOPLASTY; ANIMALS; CAROTID ARTERIES; CARRIER PROTEINS; CELL PROLIFERATION; ENDOCYTOSIS; HEK293 CELLS; HUMANS; MALE; MITOGENS; MODELS, BIOLOGICAL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; PHOSPHOPROTEINS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PARATHYROID HORMONE, TYPE 1; SIGNAL TRANSDUCTION; UP-REGULATION;

RATTUS;

EID: 78149407938     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2010.08.025     Document Type: Article

References (42)

1. Hongo T., Kupfer J., Enomoto H., Sharifi B., Giannella-Neto D., Forrester J.S., et al. Abundant expression of parathyroid hormone-related protein in primary rat aortic smooth muscle cells accompanies serum-induced proliferation. J Clin Invest Dec 1991, 88(6):1841-1847.
2. Okano K., Wu S., Huang X., Pirola C.J., Juppner H., Abou-Samra A.B., et al. Parathyroid hormone (PTH)/PTH-related protein (PTHrP) receptor and its messenger ribonucleic acid in rat aortic vascular smooth muscle cells and UMR osteoblast-like cells: cell-specific regulation by angiotensin-II and PTHrP. Endocrinology Sep 1994, 135(3):1093-1099.
3. Fiaschi-Taesch N.M., Stewart A.F. Minireview: parathyroid hormone-related protein as an intracrine factor-trafficking mechanisms and functional consequences. Endocrinology Feb 2003, 144(2):407-411.
4. Orloff J.J., Reddy D., de Papp A.E., Yang K.H., Soifer N.E., Stewart A.F. Parathyroid hormone-related protein as a prohormone: posttranslational processing and receptor interactions. Endocr Rev Feb 1994, 15(1):40-60.
5. Massfelder T., Dann P., Wu T.L., Vasavada R., Helwig J.J., Stewart A.F. Opposing mitogenic and anti-mitogenic actions of parathyroid hormone-related protein in vascular smooth muscle cells: a critical role for nuclear targeting. Proc Natl Acad Sci USA Dec 9 1997, 94(25):13630-13635.
6. Ozeki S., Ohtsuru A., Seto S., Takeshita S., Yano H., Nakayama T., et al. Evidence that implicates the parathyroid hormone-related peptide in vascular stenosis. Increased gene expression in the intima of injured carotid arteries and human restenotic coronary lesions. Arterioscler Thromb Vasc Biol Apr 1996, 16(4):565-575.
7. Nakayama T., Ohtsuru A., Enomoto H., Namba H., Ozeki S., Shibata Y., et al. Coronary atherosclerotic smooth muscle cells overexpress human parathyroid hormone-related peptides. Biochem Biophys Res Commun Apr 29 1994, 200(2):1028-1035.
8. Fiaschi-Taesch N., Sicari B., Ubriani K., Cozar-Castellano I., Takane K.K., Stewart A.F. Mutant parathyroid hormone-related protein, devoid of the nuclear localization signal, markedly inhibits arterial smooth muscle cell cycle and neointima formation by coordinate up-regulation of p15Ink4b and p27kip1. Endocrinology Mar 2009, 150(3):1429-1439.
9. de Miguel F., Fiaschi-Taesch N., Lopez-Talavera J.C., Takane K.K., Massfelder T., Helwig J.J., et al. The C-terminal region of PTHrP, in addition to the nuclear localization signal, is essential for the intracrine stimulation of proliferation in vascular smooth muscle cells. Endocrinology Sep 2001, 142(9):4096-4105.
10. Ishikawa M., Akishita M., Kozaki K., Toba K., Namiki A., Yamaguchi T., et al. Expression of parathyroid hormone-related protein in human and experimental atherosclerotic lesions: functional role in arterial intimal thickening. Atherosclerosis Sep 2000, 152(1):97-105.
11. Abou-Samra A.B., Juppner H., Force T., Freeman M.W., Kong X.F., Schipani E., 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 USA Apr 1 1992, 89(7):2732-2736.
12. Maeda S., Wu S., Juppner H., Green J., Aragay A.M., Fagin J.A., et al. Cell-specific signal transduction of parathyroid hormone (PTH)-related protein through stably expressed recombinant PTH/PTHrP receptors in vascular smooth muscle cells. Endocrinology Aug 1996, 137(8):3154-3162.
13. Wu S., Pirola C.J., Green J., Yamaguchi D.T., Okano K., Jueppner H., et al. Effects of N-terminal, midregion, and C-terminal parathyroid hormone-related peptides on adenosine 3',5'-monophosphate and cytoplasmic free calcium in rat aortic smooth muscle cells and UMR-106 osteoblast-like cells. Endocrinology Dec 1993, 133(6):2437-2444.
14. Mahon M.J., Donowitz M., Yun C.C., Segre G.V. Na(+)/H(+) exchanger regulatory factor 2 directs parathyroid hormone 1 receptor signalling. Nature Jun 20 2002, 417(6891):858-861.
15. Mahon M.J., Segre G.V. Stimulation by parathyroid hormone of a NHERF-1-assembled complex consisting of the parathyroid hormone I receptor, phospholipase Cbeta, and actin increases intracellular calcium in opossum kidney cells. J Biol Chem May 28 2004, 279(22):23550-23558.
16. Fiaschi-Taesch N., Takane K.K., Masters S., Lopez-Talavera J.C., Stewart A.F. Parathyroid-hormone-related protein as a regulator of pRb and the cell cycle in arterial smooth muscle. Circulation Jul 13 2004, 110(2):177-185.
17. Behar V., Bisello A., Bitan G., Rosenblatt M., Chorev M. Photoaffinity cross-linking identifies differences in the interactions of an agonist and an antagonist with the parathyroid hormone/parathyroid hormone-related protein receptor. J Biol Chem Jan 7 2000, 275(1):9-17.
18. Song G.J., Fiaschi-Taesch N., Bisello A. Endogenous parathyroid hormone-related protein regulates the expression of PTH type 1 receptor and proliferation of vascular smooth muscle cells. Mol Endocrinol Oct 2009, 23(10):1681-1690.
19. Bisello A., Chorev M., Rosenblatt M., Monticelli L., Mierke D.F., Ferrari S.L. Selective ligand-induced stabilization of active and desensitized parathyroid hormone type 1 receptor conformations. J Biol Chem Oct 11 2002, 277(41):38524-38530.
20. Salomon Y., Londos C., Rodbell M. A highly sensitive adenylate cyclase assay. Anal Biochem Apr 1974, 58(2):541-548.
21. Sneddon W.B., Syme C.A., Bisello A., Magyar C.E., Rochdi M.D., Parent J.L., et al. Activation-independent parathyroid hormone receptor internalization is regulated by NHERF1 (EBP50). J Biol Chem Oct 31 2003, 278(44):43787-43796.
22. Ishikawa M., Akishita M., Kozaki K., Toba K., Namiki A., Yamaguchi T., et al. Amino-terminal fragment (1-34) of parathyroid hormone-related protein inhibits migration and proliferation of cultured vascular smooth muscle cells. Atherosclerosis Jan 1998, 136(1):59-66.
23. Fiaschi-Taesch N., Sicari B.M., Ubriani K., Bigatel T., Takane K.K., Cozar-Castellano I., et al. Cellular mechanism through which parathyroid hormone-related protein induces proliferation in arterial smooth muscle cells: definition of an arterial smooth muscle PTHrP/p27kip1 pathway. Circ Res Oct 27 2006, 99(9):933-942.
24. Clemens T.L., Cormier S., Eichinger A., Endlich K., Fiaschi-Taesch N., Fischer E., et al. Parathyroid hormone-related protein and its receptors: nuclear functions and roles in the renal and cardiovascular systems, the placental trophoblasts and the pancreatic islets. Br J Pharmacol Nov 2001, 134(6):1113-1136.
25. Schluter K.D., Piper H.M. Cardiovascular actions of parathyroid hormone and parathyroid hormone-related peptide. Cardiovasc Res Jan 1998, 37(1):34-41.
26. Koyama H., Bornfeldt K.E., Fukumoto S., Nishizawa Y. Molecular pathways of cyclic nucleotide-induced inhibition of arterial smooth muscle cell proliferation. J Cell Physiol Jan 2001, 186(1):1-10.
27. Ediger T.R., Kraus W.L., Weinman E.J., Katzenellenbogen B.S. Estrogen receptor regulation of the Na+/H+ exchange regulatory factor. Endocrinology Jul 1999, 140(7):2976-2982.
28. Wang B., Yang Y., Abou-Samra A.B., Friedman P.A. NHERF1 regulates parathyroid hormone receptor desensitization: interference with beta-arrestin binding. Mol Pharmacol May 2009, 75(5):1189-1197.
29. Wang B., Bisello A., Yang Y., Romero G.G., Friedman P.A. NHERF1 regulates parathyroid hormone receptor membrane retention without affecting recycling. J Biol Chem Dec 14 2007, 282(50):36214-36222.
30. Wheeler D., Sneddon W.B., Wang B., Friedman P.A., Romero G. NHERF-1 and the cytoskeleton regulate the traffic and membrane dynamics of G protein-coupled receptors. J Biol Chem Aug 24 2007, 282(34):25076-25087.
31. Cao T.T., Deacon H.W., Reczek D., Bretscher A., von Zastrow M. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor. Nature Sep 16 1999, 401(6750):286-290.
32. Kishi M., Liu X., Hirakawa T., Reczek D., Bretscher A., Ascoli M. Identification of two distinct structural motifs that, when added to the C-terminal tail of the rat LH receptor, redirect the internalized hormone-receptor complex from a degradation to a recycling pathway. Mol Endocrinol Sep 2001, 15(9):1624-1635.
33. Li J.G., Chen C., Liu-Chen L.Y. Ezrin-radixin-moesin-binding phosphoprotein-50/Na+/H+ exchanger regulatory factor (EBP50/NHERF) blocks U50, 488H-induced down-regulation of the human kappa opioid receptor by enhancing its recycling rate. J Biol Chem Jul 26 2002, 277(30):27545-27552.
34. Moyer B.D., Denton J., Karlson K.H., Reynolds D., Wang S., Mickle J.E., et al. A PDZ-interacting domain in CFTR is an apical membrane polarization signal. J Clin Invest Nov 1999, 104(10):1353-1361.
35. Shenolikar S., Voltz J.W., Minkoff C.M., Wade J.B., Weinman E.J. Targeted disruption of the mouse NHERF-1 gene promotes internalization of proximal tubule sodium-phosphate cotransporter type IIa and renal phosphate wasting. Proc Natl Acad Sci USA Aug 20 2002, 99(17):11470-11475.
36. Wang B., Ardura J.A., Romero G., Yang Y.S., Hall R.A., Friedman P.A. Na/H exchanger regulatory factors control PTH receptor signaling by facilitating differential activation of G{alpha} protein subunits. The J Biol Chem Aug 2010, 285(35):26976-26986.
37. Capuano P., Bacic D., Roos M., Gisler S.M., Stange G., Biber J., et al. Defective coupling of apical PTH receptors to phospholipase C prevents internalization of the Na+-phosphate cotransporter NaPi-IIa in Nherf1-deficient mice. Am J Physiol Cell Physiol Feb 2007, 292(2):C927-C934.
38. Stuart W.D., Maeda S., Khera P., Fagin J.A., Clemens T.L. Parathyroid hormone-related protein induces G1 phase growth arrest of vascular smooth muscle cells. Am J Physiol Endocrinol Metab Jul 2000, 279(1):E60-E67.
39. Berk B.C., Corson M.A. Angiotensin II signal transduction in vascular smooth muscle: role of tyrosine kinases. Circ Res May 1997, 80(5):607-616.
40. Hu Z.W., Shi X.Y., Lin R.Z., Chen J., Hoffman B.B. Alpha1-adrenergic receptor stimulation of mitogenesis in human vascular smooth muscle cells: role of tyrosine protein kinases and calcium in activation of mitogen-activated protein kinase. J Pharmacol Exp Ther Jul 1999, 290(1):28-37.
41. Munoz U., Bartolome F., Bermejo F., Martin-Requero A. Enhanced proteasome-dependent degradation of the CDK inhibitor p27(kip1) in immortalized lymphocytes from Alzheimer's dementia patients. Neurobiol Aging Oct 2008, 29(10):1474-1484.
42. Hassan G.S., Williams T.M., Frank P.G., Lisanti M.P. Caveolin-1-deficient aortic smooth muscle cells show cell autonomous abnormalities in proliferation, migration, and endothelin-based signal transduction. Am J Physiol Jun 2006, 290(6):H2393-H2401.