Fluorescent ligand-directed co-localization of the parathyroid hormone 1 receptor with the brush-border scaffold complex of the proximal tubule reveals hormone-dependent changes in ezrin immunoreactivity consistent with inactivation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 12, 2012, Pages 2243-2253

  Guo, Jun ^a   Song, Lige ^a   Liu, Minlin ^a   Mahon, Matthew J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Ezrin; Megalin; NHERF1; NHERF2; Parathyroid hormone; Parathyroid hormone receptor

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; EZRIN; MEGALIN; PARATHYROID HORMONE RECEPTOR 1; POLYCLONAL ANTIBODY; POLYCLONAL ANTIBODY CS 3145; TETRAMETHYLRHODAMINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; ENDOSOME; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE EPITHELIUM; MICROVILLUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SECONDARY HYPERPARATHYROIDISM;

ANIMALS; CELL MEMBRANE; CYTOSKELETAL PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HETEROCYCLIC COMPOUNDS, 3-RING; KIDNEY TUBULES, PROXIMAL; MICE; MICE, INBRED C57BL; MICROVILLI; PARATHYROID HORMONE; RECEPTOR, PARATHYROID HORMONE, TYPE 1;

MUS;

EID: 84867597641     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.09.010     Document Type: Article

References (50)

1. Potts J.T., Gardella T.J. Progress, paradox, and potential: parathyroid hormone research over five decades. Ann. N. Y. Acad. Sci. 2007, 1117:196-208.
2. Kronenberg H.M., Karaplis A.C., Lanske B. Role of parathyroid hormone-related protein in skeletal development. Ann. N. Y. Acad. Sci. 1996, 785:119-123.
3. Mahon M.J. The parathyroid hormone receptorsome and the potential for therapeutic intervention. Curr. Drug Targets 2012, 13:116-128.
4. Amizuka N., Lee H.S., Khan M.Y., Arazani A., Warhawsky H., Hendy G.N., Ozawa H., White J.H., Goltzman D. Cell-specific expression of the parathyroid hormone (PTH)PTH-related peptide receptor gene in kidney from kidney-specific and ubiquitous promoters. Endocrinology 1997, 138:469-481.
5. Traebert M., Volkl H., Biber J., Murer H., Kaissling B. Luminal and contraluminal action of 1-34 and 3-34 PTH peptides on renal type IIa Na-P(i) cotransporter. Am. J. Physiol. Renal Physiol. 2000, 278:F792-F798.
6. Ba J., Brown D., Friedman P.A. Calcium-sensing receptor regulation of PTH-inhibitable proximal tubule phosphate transport. Am. J. Physiol. Renal Physiol. 2003, 285:F1233-F1243.
7. Capuano P., Bacic D., Roos M., Gisler S.M., Stange G., Biber J., Kaissling B., Weinman E.J., Shenolikar S., Wagner C.A., Murer H. 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. 2007, 292:C927-C934.
8. Reshkin S., Forgo J., Murer H. Apical and basolateral effects of PTH in OK cells: transport inhibition, messenger production, effects of pertussis toxin, and interaction with a PTH analog. J. Membr. Biol. 1991, 124:227-237.
9. + exchanger-regulatory factor 1 mediates inhibition of phosphate transport by parathyroid hormone and second messengers by acting at multiple sites in opossum kidney cells. Mol. Endocrinol. 2003, 17:2355-2364.
10. Mahon M.J. The parathyroid hormone 1 receptor directly binds to the FERM domain of ezrin, an interaction that supports apical receptor localization and signaling in LLC-PK1 cells. Mol. Endocrinol. 2009, 23:1691-1701.
11. Mahon M., Donowitz M., Yun C., Segre G. Na(+)/H(+) exchanger regulatory factor 2 directs parathyroid hormone 1 receptor signalling. Nature 2002, 417:858-861.
12. Mahon M., Segre G. 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. 2004, 279:23550-23558.
13. Sneddon W.B., Syme C.A., Bisello A., Magyar C.E., Rochdi M.D., Parent J.L., Weinman E.J., Abou-Samra A.B., Friedman P.A. Activation-independent parathyroid hormone receptor internalization is regulated by NHERF1 (EBP50). J. Biol. Chem. 2003, 278:43787-43796.
14. 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. 2007, 282:36214-36222.
15. 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. 2007, 282:25076-25087.
16. + exchanger regulatory factor-1 in rat osteosarcoma ROS 17/2.8 cells. Mol. Endocrinol. 2008, 22:1163-1170.
17. Mori T., Kitano K., Terawaki S., Maesaki R., Fukami Y., Hakoshima T. Structural basis for CD44 recognition by ERM proteins. J. Biol. Chem. 2008, 283:29602-29612.
18. Wade J.B., Welling P.A., Donowitz M., Shenolikar S., Weinman E.J. Differential renal distribution of NHERF isoforms and their colocalization with NHE3, ezrin, and ROMK. Am. J. Physiol. Cell Physiol. 2001, 280:C192-C198.
19. Ingraffea J., Reczek D., Bretscher A. Distinct cell type-specific expression of scaffolding proteins EBP50 and E3KARP: EBP50 is generally expressed with ezrin in specific epithelia, whereas E3KARP is not. Eur. J. Cell Biol. 2002, 81:61-68.
20. Biber J., Stieger B., Stange G., Murer H. Isolation of renal proximal tubular brush-border membranes. Nat. Protoc. 2007, 2:1356-1359.
21. Mahon M.J. Apical membrane segregation of phosphatidylinositol-4,5-bisphosphate influences parathyroid hormone 1 receptor compartmental signaling and localization via direct regulation of ezrin in LLC-PK1 cells. Cell. Signal. 2011, 23:1659-1668.
22. Okazaki M., Ferrandon S., Vilardaga J.P., Bouxsein M.L., Potts J.T., Gardella T.J. Prolonged signaling at the parathyroid hormone receptor by peptide ligands targeted to a specific receptor conformation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16525-16530.
23. Hilpert J., Nykjaer A., Jacobsen C., Wallukat G., Nielsen R., Moestrup S.K., Haller H., Luft F.C., Christensen E.I., Willnow T.E. Megalin antagonizes activation of the parathyroid hormone receptor. J. Biol. Chem. 1999, 274:5620-5625.
24. Gary R., Bretscher A. Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol. Biol. Cell 1995, 6:1061-1075.
25. Matsui T., Maeda M., Doi Y., Yonemura S., Amano M., Kaibuchi K., Tsukita S. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 1998, 140:647-657.
26. Fievet B.T., Gautreau A., Roy C., Del Maestro L., Mangeat P., Louvard D., Arpin M. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 2004, 164:653-659.
27. Yao X., Thibodeau A., Forte J.G., Ezrin-calpain I. Interactions in gastric parietal cells. Am. J. Physiol. 1993, 265:C36-C46.
28. Ranganathan R., Ross E.M. PDZ domain proteins: scaffolds for signaling complexes. Curr. Biol. 1997, 7:R770-R773.
29. Bezprozvanny I., Maximov A. PDZ domains: more than just a glue. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:787-789.
30. Neisch A.L., Fehon R.G. Ezrin, radixin and moesin: key regulators of membrane-cortex interactions and signaling. Curr. Opin. Cell Biol. 2011, 23:377-382.
31. Schreiner R., Frindt G., Diaz F., Carvajal-Gonzalez J.M., Perez Bay A.E., Palmer L.G., Marshansky V., Brown D., Philp N.J., Rodriguez-Boulan E. The absence of a clathrin adapter confers unique polarity essential to proximal tubule function. Kidney Int. 2010, 78:382-388.
32. Sato T., Garcia-Bunuel R., Brandes D. Ultrastructural cytochemical localization of adenylate cyclase in the rat nephron. Lab. Invest. 1974, 30:222-229.
33. Stow J.L., Sabolic I., Brown D. Heterogeneous localization of G protein alpha-subunits in rat kidney. Am. J. Physiol. 1991, 261:F831-F840.
34. Lea J.P., Ertoy D., Hollis J.L., Marrero M.B., Sands J.M. Immunolocalization of phospholipase C isoforms in rat kidney. Kidney Int. 1998, 54:1484-1490.
35. +/phosphate cotransporter NaPi-IIa is internalized via the receptor-mediated endocytic route in response to parathyroid hormone. Kidney Int. 2006, 69:495-503.
36. Picard N., Capuano P., Stange G., Mihailova M., Kaissling B., Murer H., Biber J., Wagner C.A. Acute parathyroid hormone differentially regulates renal brush border membrane phosphate cotransporters. Pflugers Arch. 2010, 460:677-687.
37. Urena P., Kong X.F., Abou-Samra A.B., Jüppner H., Kronenberg H.M., Potts J.T., Segre G.V. Parathyroid hormone (PTH)/PTH-related peptide (PTHrP) receptor mRNA are widely distributed in rat tissues. Endocrinology 1993, 133:617-623.
38. + exchanger regulatory factor-1 association and dissociation regulate parathyroid hormone receptor trafficking at membrane microdomains. J. Biol. Chem. 2011, 286:35020-35029.
39. Weinman E.J., Biswas R.S., Peng Q., Shen L., Turner C.L., Xiafoei E., Steplock D., Shenolikar S., Cunningham R. Parathyroid hormone inhibits renal phosphate transport by phosphorylation of serine 77 of sodium-hydrogen exchanger regulatory factor-1. J. Clin. Invest. 2007, 117:3412-3420.
40. Bretscher A., Reczek D., Berryman M. Ezrin: a protein requiring conformational activation to link microfilaments to the plasma membrane in the assembly of cell surface structures. J. Cell Sci. 1997, 110(Pt 24):3011-3018.
41. Yonemura S., Hirao M., Doi Y., Takahashi N., Kondo T., Tsukita S. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J. Cell Biol. 1998, 140:885-895.
42. Nashiki K., Taketani Y., Takeichi T., Sawada N., Yamamoto H., Ichikawa M., Arai H., Miyamoto K., Takeda E. Role of membrane microdomains in PTH-mediated down-regulation of NaPi-IIa in opossum kidney cells. Kidney Int. 2005, 68:1137-1147.
43. Zhou R., Cao X., Watson C., Miao Y., Guo Z., Forte J.G., Yao X. Characterization of protein kinase A-mediated phosphorylation of ezrin in gastric parietal cell activation. J. Biol. Chem. 2003, 278:35651-35659.
44. Dransfield D.T., Bradford A.J., Smith J., Martin M., Roy C., Mangeat P.H., Goldenring J.R. Ezrin is a cyclic AMP-dependent protein kinase anchoring protein. EMBO J. 1997, 16:35-43.
45. Khundmiri S.J., Rane M.J., Lederer E.D. Parathyroid hormone regulation of type II sodium-phosphate cotransporters is dependent on an A kinase anchoring protein. J. Biol. Chem. 2003, 278:10134-10141.
46. Hirao M., Sato N., Kondo T., Yonemura S., Monden M., Sasaki T., Takai Y., Tsukita S. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway. J. Cell Biol. 1996, 135:37-51.
47. Yonemura S., Matsui T., Tsukita S. Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 2002, 115:2569-2580.
48. Goligorsky M.S., Menton D.N., Hruska K.A. Parathyroid hormone-induced changes of the brush border membrane topography and cytosketelon in cultured renal proximal tubular cells. J. Membr. Biol. 1986, 92:151-162.
49. Mahon M.J. Ezrin promotes functional expression and parathyroid hormone-mediated regulation of the sodium-phosphate cotransporter 2a in LLC-PK1 cells. Am. J. Physiol. Renal Physiol. 2008, 294:F667-F675.
50. Egan J.J., Gronowicz G., Rodan G.A. Parathyroid hormone promotes the disassembly of cytoskeletal actin and myosin in cultured osteoblastic cells: mediation by cyclic AMP. J. Cell. Biochem. 1991, 45:101-111.