Phosphoproteomic profiling reveals vasopressin-regulated phosphorylation sites in collecting duct

Journal of the American Society of Nephrology

Volumn 21, Issue 2, 2010, Pages 303-315

  Bansal, Amar D ^a   Hoffert, Jason D ^a   Pisitkun, Trairak ^a   Hwang, Shelly ^a   Chou, Chung Lin ^a   Boja, Emily S ^b   Wang, Guanghui ^b   Knepper, Mark A ^a  

^a Epithelial Systems Biology Laboratory   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 2; BETA CATENIN; CALNEXIN; CALPASTATIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DESMOPLAKIN; EPSIN; HEAT SHOCK PROTEIN 90; KINESIN; PHOSPHOPEPTIDE; PROSTAGLANDIN E SYNTHASE; SEPTIN; SERINE; TENSIN; VASOPRESSIN; ARGIPRESSIN[1 DEAMINO]; PHOSPHOPROTEIN; VASOPRESSIN DERIVATIVE;

ANIMAL TISSUE; ARTICLE; DATA BASE; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMUNOBLOTTING; IN VITRO STUDY; KIDNEY COLLECTING TUBULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; RAT; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; URINE; ALGORITHM; ANIMAL; ANIMAL MODEL; BRATTLEBORO RAT; DRUG EFFECT; GENETICS; METABOLISM; PHOSPHORYLATION; SPRAGUE DAWLEY RAT;

ALGORITHMS; ANIMALS; BETA CATENIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DEAMINO ARGININE VASOPRESSIN; KIDNEY TUBULES, COLLECTING; MODELS, ANIMAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; RATS; RATS, BRATTLEBORO; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; VASOPRESSINS;

EID: 77949381906     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2009070728     Document Type: Article

References (52)

1. Nielsen S, Frokiaer J, Marples D, Kwon TH, Agre P, Knepper MA: Aquaporins in the kidney: From molecules to medicine. Physiol Rev 82: 205-244, 2002
2. Brown D: The ins and outs of aquaporin-2 trafficking. Am J Physiol Renal Physiol 284: F893-F901, 2003
3. Uawithya P, Pisitkun T, Ruttenberg BE, Knepper MA: Transcriptiona profiling of native inner medullary collecting duct cells from rat kidney. Physiol Genomics 32: 229-253, 2008
4. Yano Y, Rodrigues AC, Jr., de Braganca AC, Andrade LC, Magaldi AJ: PKC stimulated by glucagon decreases UT-A1 urea transporter expression in rat IMCD. Pflugers Arch 456: 1229-1237, 2008
5. O'Connor PM, Cowley AW, Jr.: Vasopressin-induced nitric oxide production in rat inner medullary collecting duct is dependent on V2 receptor activation of the phosphoinositide pathway. Am J Physiol Renal Physiol 293: F526-F532, 2007
6. Umenishi F, Narikiyo T, Vandewalle A, Schrier RW: cAMP regulates vasopressin-induced AQP2 expression via protein kinase A-indepen-dent pathway. Biochim Biophys Acta 1758: 1100-1105, 2006
7. Mordasini D, Bustamante M, Rousselot M, Martin PY, Hasler U, Feraille E: Stimulation of Na+ transport by AVP is independent of PKA phosphorylation of the Na-K-ATPase in collecting duct principal cells. Am J Physiol Renal Physiol 289: F1031-F1039, 2005
8. Tamma G, Klussmann E, Maric K, Aktories K, Svelto M, Rosenthal W, Valenti G: Rho inhibits cAMP-induced translocation of aquaporin-2 into the apical membrane of renal cells. Am J Physiol Renal Physiol 281: F1092-F1101, 2001
9. Pisitkun T, Jacob V, Schleicher SM, Chou CL, Yu MJ, Knepper MA: Akt and ERK1/2 pathways are components of the vasopressin signaling network in rat native IMCD. Am J Physiol Renal Physiol 295: F1030-F1043, 2008
10. Chou CL, Christensen BM, Frische S, Vorum H, Desai RA, Hoffert JD, de Lanerolle P, Nielsen S, Knepper MA: Non-muscle myosin II and myosin light chain kinase are downstream targets for vasopressin signaling in the renal collecting duct. J Biol Chem 279: 49026-49035, 2004
11. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA: Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92: 1013-1017, 1995
12. 2O transport in inner medullary collecting duct subsegments. Am J Physiol 253: F823-F832, 1987
13. + channel trafficking. Endocrinology 146: 5079-5085, 2005
14. Tomita K, Pisano JJ, Knepper MA: Control of sodium and potassium transport in the cortical collecting duct of the rat. Effects of bradykinin, vasopressin, and deoxycorticosterone. J Clin Invest 76: 132-136, 1985
15. DiGiovanni SR, Nielsen S, Christensen EI, Knepper MA: Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat. Proc Natl Acad Sci USA 91: 8984-8988, 1994
16. TerrisJ, Ecelbarger CA, Nielsen S, Knepper MA: Long-term regulation of four renal aquaporins in rats. Am J Physiol 271: F414-F422, 1996
17. Hoffert JD, Pisitkun T, Wang G, Shen RF, Knepper MA: Quantitative phosphoproteomics of vasopressin-sensitive renal cells: Regulation of aquaporin-2 phosphorylation at two sites. Proc Natl Acad Sci USA 103: 7159-7164, 2006
18. Hoffert JD, Fenton RA, Moeller HB, Simons B, Tchapyjnikov D, McDil BW, Yu MJ, Pistikun T, Chen F, Knepper MA: Vasopressin-stimulated increase in phosphorylation at ser-269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 283: 24617-24627, 2008
19. Blount MA, Klein JD, Martin CF, Tchapyjnikov D, Sands JM: Forskolin stimulates phosphorylation and membrane accumulation of UT-A3. Am J Physiol Renal Physiol 293: F1308-F1313, 2007
20. Blount MA, Mistry AC, Frohlich O, Price SR, Chen G, Sands JM, Klein JD: Phosphorylation of UT-A1 urea transporter at serines 486 and 499 is important for vasopressin-regulated activity and membrane accumulation. Am J Physiol Renal Physiol 295: F295-F299, 2008
21. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP: Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: The yeast proteome. J Proteome Res 2: 43-50, 2003
22. Wang G, Wu WW, Zeng W, Chou CL, Shen RF: Label-free protein quantification using LC-coupled ion trap or FT mass spectrometry: Reproducibility, linearity, and application with complex proteomes. J Proteome Res 5: 1214-1223, 2006
23. Nielsen J, Hoffert JD, Knepper MA, Agre P, Nielsen S, Fenton RA: Proteomic analysis of lithium-induced nephrogenic diabetes insipidus: Mechanisms for aquaporin 2 down-regulation and cellular proliferation. Proc Natl Acad Sci USA 105: 3634-3639, 2008
24. Bradford AD, Terris JM, Ecelbarger CA, Klein JD, Sands JM, Chou CL, Knepper MA: 97-and 117-kDa forms of collecting duct urea transporter UT-A1 are due to different states of glycosylation. Am J Physiol Renal Physiol 281: F133-F143, 2001
25. Karakashian A, Timmer RT, Klein JD, Gunn RB, Sands JM, Bagnasco SM: Cloning and characterization of two new isoforms of the rat kidney urea transporter: UT-A3 and UT-A4. J Am Soc Nephrol 10: 230-237, 1999
26. Zhang C, Sands JM, Klein JD: Vasopressin rapidly increases phosphor-ylation of UT-A1 urea transporter in rat IMCDs through PKA. Am J Physiol Renal Physiol 282: F85-F90, 2002
27. Miller ML, Jensen LJ, Diella F, Jorgensen C, Tinti M, Li L, Hsiung M, Parker SA, Bordeaux J, Sicheritz-Ponten T, Olhovsky M, Pasculescu A, Alexander J, Knapp S, Blom N, Bork P, Li S, Cesareni G, Pawson T, Turk BE, Yaffe MB, Brunak S, Linding R: Linear motif atlas for phos-phorylation-dependent signaling. Sci Signal 1: ra2, 2008
28. Wang Y, Klein JD, Blount MA, Martin CF, Kent KJ, Pech V, Wall SM, Sands JM: Epac regulates UT-A1 to increase urea transport in inner medullary collecting ducts. J Am Soc Nephrol 20: 2018-2024, 2009
29. Brown D, Hasler U, Nunes P, Bouley R, Lu HA: Phosphorylation events and the modulation of aquaporin 2 cell surface expression. Curr Opin Nephrol Hypertens 17: 491-498, 2008
30. Clevers H: Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480, 2006
31. Schmidt-Ott KM, Barasch J: WNT/beta-catenin signaling in nephron progenitors and their epithelial progeny. Kidney Int 74: 1004-1008, 2008
32. Yu J, Carroll TJ, Rajagopal J, Kobayashi A, Ren Q, McMahon AP: A Wnt7b-dependent pathway regulates the orientation of epithelial cell division and establishes the cortico-medullary axis of the mammalian kidney. Development 136: 161-171, 2009
33. Lyons JP, Miller RK, Zhou X, Weidinger G, Deroo T, Denayer T, Park JI, Ji H, Hong JY, Li A, Moon RT, Jones EA, Vleminckx K, Vize PD, McCrea PD: Requirement of Wnt/beta-catenin signaling in pronephric kidney development. Mech Dev 126: 142-159, 2009
34. Taurin S, Sandbo N, Qin Y, Browning D, Dulin NO: Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J Biol Chem 281: 9971-9976, 2006
35. Taurin S, Sandbo N, Yau DM, Sethakorn N, Dulin NO: Phosphorylation of beta-catenin by PKA promotes ATP-induced proliferation of vascular smooth muscle cells. Am J Physiol Cell Physiol 294: C1169-C1174, 2008
36. Palmer KJ, Konkel JE, Stephens DJ: PCTAIRE protein kinases interact directly with the COPII complex and modulate secretory cargo transport. J Cell Sci 118: 3839-3847, 2005
37. Nanda A, Buckhaults P, Seaman S, Agrawal N, Boutin P, Shankara S, Nacht M, Teicher B, Stampfl J, Singh S, Vogelstein B, Kinzler KW, St Croix B: Identification of a binding partner for the endothelial cell surface proteins TEM7 and TEM7R. Cancer Res 64: 8507-8511, 2004
38. Spiliotis ET, Nelson WJ: Here come the septins: Novel polymers that coordinate intracellular functions and organization. J Cell Sci 119: 4-10, 2006
39. Kang-Decker N, Mantchev GT, Juneja SC, McNiven MA, van Deursen JM: Lack of acrosome formation in Hrb-deficient mice. Science 294: 1531-1533, 2001
40. Wang H, Traub LM, Weixel KM, Hawryluk MJ, Shah N, Edinger RS, Perry CJ, Kester L, Butterworth MB, Peters KW, Kleyman TR, Frizzell RA, Johnson JP: Clathrin-mediated endocytosis of the epithelial sodium channel. Role of epsin. J Biol Chem 281: 14129-14135, 2006
41. Chou CL, DiGiovanni SR, Luther A, Lolait SJ, Knepper MA: Oxytocin as an antidiuretic hormone. II. Role of V2 vasopressin receptor. Am J Physiol 269: F78-F85, 1995
42. Stokes JB, Grupp C, Kinne RK: Purification of rat papillary collecting duct cells: functional and metabolic assessment. Am J Physiol 253: F251-F262, 1987
43. Swaney DL, McAlister GC, Coon JJ: Decision tree-driven tandem mass spectrometry for shotgun proteomics. Nat Methods 5: 959-964, 2008
44. Yates JR, 3rd, Eng JK, McCormack AL, Schieltz D: Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67: 1426-1436, 1995
45. Tanner S, Shu H, Frank A, Wang LC, Zandi E, Mumby M, Pevzner PA, Bafna V: InsPecT: Identification of posttranslationally modified pep-tides from tandem mass spectra. Anal Chem 77: 4626-4639, 2005
46. Payne SH, Yau M, Smolka MB, Tanner S, Zhou H, Bafna V: Phospho-rylation-specific MS/MS scoring for rapid and accurate phosphopro-teome analysis. J Proteome Res 7: 3373-3381, 2008
47. Geer LY, Markey SP, Kowalak JA, Wagner L, Xu M, Maynard DM, Yang X, Shi W, Bryant SH: Open mass spectrometry search algorithm. J Proteome Res 3: 958-964, 2004
48. Yu MJ, Pisitkun T, Wang G, Aranda JF, Gonzales PA, Tchapyjnikov D, Shen RF, Alonso MA, Knepper MA: Large-scale quantitative LC-MS/MS analysis of detergent-resistant membrane proteins from rat renal collecting duct. Am J Physiol Cell Physiol 295: C661-C678, 2008
49. Hoffert JD, Wang G, Pisitkun T, Shen RF, Knepper MA: An automated platform for analysis of phosphoproteomic datasets: Application to kidney collecting duct phosphoproteins. J Proteome Res 6: 3501-3508, 2007
50. Beausoleil SA, Villen J, Gerber SA, Rush J, Gygi SP: A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 24: 1285-1292, 2006
51. Ruttenberg BE, Pisitkun T, Knepper MA, Hoffert JD: PhosphoScore: An open-source phosphorylation site assignment tool for MSn data. J Proteome Res 7: 3054-3059, 2008
52. Fenton RA, Moeller HB, Hoffert JD, Yu MJ, Nielsen S, Knepper MA: Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vaso-pressin. Proc Natl Acad Sci USA 105: 3134-3139, 2008