Deep proteomic profiling of vasopressin-sensitive collecting duct cells. II. bioinformatic analysis of vasopressin signaling

American Journal of Physiology - Cell Physiology

Volumn 309, Issue 12, 2015, Pages C799-C812

  Yang, Chin Rang ^a   Raghuram, Viswanathan ^a   Emamian, Milad ^a   Sandoval, Pablo C ^a   Knepper, Mark A ^a  

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

Author keywords

Aquaporin 2; Mass spectrometry; Phosphorylation; Protein kinase; Ribosome; Small GTPase; Translation

Indexed keywords

AQUAPORIN 2; ARGININE; DESMOPRESSIN; INITIATION FACTOR 3; LYSINE; PROTEIN KINASE; VASOPRESSIN; AQP2 PROTEIN, MOUSE; VASOPRESSIN DERIVATIVE;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; CELL CULTURE; CENTRIFUGATION; COLLECTING DUCT CELL; CONTROLLED STUDY; ISOTOPE LABELING; KIDNEY CELL; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEOMICS; QUANTITATIVE STUDY; RIBOSOME; ROUGH ENDOPLASMIC RETICULUM; WESTERN BLOTTING; ANIMAL; BAYES THEOREM; BIOLOGY; CELL LINE; EPITHELIUM CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; KIDNEY COLLECTING TUBULE; LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR WEIGHT; PHOSPHORYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; TANDEM MASS SPECTROMETRY;

ANIMALS; AQUAPORIN 2; BAYES THEOREM; BLOTTING, WESTERN; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPITHELIAL CELLS; KIDNEY TUBULES, COLLECTING; MICE; MOLECULAR WEIGHT; PHOSPHORYLATION; PROTEOMICS; TANDEM MASS SPECTROMETRY; VASOPRESSINS;

EID: 84980000233     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00214.2015     Document Type: Article

References (40)

1. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell. New York: Garland Science, 2002.
2. Barile M, Pisitkun T, Yu MJ, Chou CL, Verbalis MJ, Shen RF, Knepper MA. Large scale protein identification in intracellular aquaporin- 2 vesicles from renal inner medullary collecting duct. Mol Cell Proteomics 4: 1095–1106, 2005.
3. Beznoskova P, Cuchalova L, Wagner S, Shoemaker CJ, Gunisova S, von der HT, Valasek LS. Translation initiation factors eIF3 and HCR1 control translation termination and stop codon read-through in yeast cells. PLos Genet 9: e1003962, 2013.
4. Bolger SJ, Hurtado PA, Hoffert JD, Saeed F, Pisitkun T, Knepper MA. Quantitative phosphoproteomics in nuclei of vasopressin-sensitive renal collecting duct cells. Am J Physiol Cell Physiol 303: C1006–C1020, 2012.
5. Bonifacino JS. Adaptor proteins involved in polarized sorting. J Cell Biol 204: 7–17, 2014.
6. Bradford D, Raghuram V, Wilson JL, Chou CL, Hoffert JD, Knepper MA, Pisitkun T. Use of LC-MS/MS and Bayes’ theorem to identify protein kinases that phosphorylate aquaporin-2 at Ser256. Am J Physiol Cell Physiol 307: C123–C139, 2014.
7. Caenepeel S, Charydczak G, Sudarsanam S, Hunter T, Manning G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci USA 101: 11707–11712, 2004.
8. Christensen BM, Zelenina M, Aperia A, Nielsen S. Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment. Am J Physiol Renal Physiol 278: F29–F42, 2000.
9. Fenton RA, Moeller HB, Hoffert JD, Yu MJ, Nielsen S, Knepper MA. Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vasopressin. Proc Natl Acad Sci USA 105: 3134–3139, 2008.
10. Hasler U, Vinciguerra M, Vandewalle A, Martin PY, Feraille E. Dual effects of hypertonicity on aquaporin-2 expression in cultured renal collecting duct principal cells. J Am Soc Nephrol 16: 1571–1582, 2005.
11. Hinnebusch AG. The scanning mechanism of eukaryotic translation initiation. Annu Rev Biochem 83: 779–812, 2014.
12. Hoffert JD, Fenton RA, Moeller HB, Simons B, Tchapyjnikov D, McDill BW, Yu MJ, Pisitkun T, Chen F, Knepper MA. Vasopressinstimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J Biol Chem 283: 24617–24627, 2008.
13. Hoffert JD, Nielsen J, Yu MJ, Pisitkun T, Schleicher SM, Nielsen S, Knepper MA. Dynamics of aquaporin-2 serine-261 phosphorylation in response to short-term vasopressin treatment in collecting duct. Am J Physiol Renal Physiol 292: F691–F700, 2007.
14. 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.
15. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57, 2009.
16. Jan CH, Williams CC, Weissman JS. Principles of ER cotranslational translocation revealed by proximity-specific ribosome profiling. Science 346: 1257521, 2014.
17. Kato JY, Yoneda-Kato N. Mammalian COP9 signalosome. Genes Cells 14: 1209–1225, 2009.
18. Khositseth S, Pisitkun T, Slentz DH, Wang G, Hoffert JD, Knepper MA, Yu MJ. Quantitative protein and mRNA profiling shows selective post-transcriptional control of protein expression by vasopressin in kidney cells. Mol Cell Proteomics 10: M110, 2011.
19. Knepper MA. Systems biology in physiology: the vasopressin signaling network in kidney. Am J Physiol Cell Physiol 303: C1115–C1124, 2012.
20. Li Y, Shaw S, Kamsteeg EJ, Vandewalle A, Deen PM. Development of lithium-induced nephrogenic diabetes insipidus is dissociated from adenylyl cyclase activity. J Am Soc Nephrol 17: 1063–1072, 2006.
21. Marples D, Knepper MA, Christensen EI, Nielsen S. Redistribution of aquaporin-2 water channels induced by vasopressin in rat kidney inner medullary collecting duct. Am J Physiol Cell Physiol 269: C655–C664, 1995.
22. Moeller HB, Knepper MA, Fenton RA. Serine 269 phosphorylated aquaporin-2 is targeted to the apical membrane of collecting duct principal cells. Kidney Int 75: 295–303, 2008.
23. Nedvetsky PI, Tabor V, Tamma G, Beulshausen S, Skroblin P, Kirschner A, Mutig K, Boltzen M, Petrucci O, Vossenkamper A, Wiesner B, Bachmann S, Rosenthal W, Klussmann E. Reciprocal regulation of aquaporin-2 abundance and degradation by protein kinase A and p38-MAP kinase. J Am Soc Nephrol 21: 1645–1656, 2010.
24. 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.
25. Novikoff AB. Electron microscopy: cytology of cell fractions. Science 124: 969–972, 1956.
26. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1: 376–386, 2002.
27. Rinschen MM. Water transport running deep. Focus on “Deep proteomic profiling of vasopressin-sensitive collecting duct cells.” Am J Physiol Cell Physiol (September 30, 2015). doi:10.1152/ajpcell.00280.2015.
28. Rinschen MM, Yu MJ, Wang G, Boja ES, Hoffert JD, Pisitkun T, Knepper MA. Quantitative phosphoproteomic analysis reveals vasopressin V2-receptor-dependent signaling pathways in renal collecting duct cells. Proc Natl Acad Sci USA 107: 3887, 2010.
29. Sabolic I, Katsura T, Verbabatz JM, Brown D. The AQP2 water channel: effect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats. J Membr Biol 143: 165–177, 1995.
30. Sachs AN, Pisitkun T, Hoffert JD, Yu MJ, Knepper MA. LC-MS/MS analysis of differential centrifugation fractions from native inner medullary collecting duct of rat. Am J Physiol Renal Physiol 295: F1799–F1806, 2008.
31. Sandoval PC, Slentz DH, Pisitkun T, Saeed F, Hoffert JD, Knepper MA. Proteome-wide measurement of protein half-lives and translation rates in vasopressin-sensitive collecting duct cells. J Am Soc Nephrol 24: 1793–1805, 2013.
32. Sanghi A, Zaringhalam M, Corcoran CC, Saeed F, Hoffert JD, Sandoval P, Pisitkun T, Knepper MA. A knowledge base of vasopressin actions in the kidney. Am J Physiol Renal Physiol 307: F747–F755, 2014.
33. Schenk LK, Bolger SJ, Luginbuhl K, Gonzales PA, Rinschen MM, Yu MJ, Hoffert JD, Pisitkun T, Knepper MA. Quantitative proteomics identifies vasopressin-responsive nuclear proteins in collecting duct cells. J Am Soc Nephrol 23: 1008–1018, 2012.
34. Segev N. GTPases in intracellular trafficking: an overview. Semin Cell Dev Biol 22: 1–2, 2011.
35. Siekevitz P, Palade GE. A cytochemical study on the pancreas of the guinea pig. I. Isolation and enzymatic activities of cell fractions. J Biophys Biochem Cytol 4: 203–218, 1958.
36. Tamma G, Klussmann E, Procino G, Svelto M, Rosenthal W, Valenti G. cAMP-induced AQP2 translocation is associated with RhoA inhibition through RhoA phosphorylation and interaction with RhoGDI. J Cell Sci 116: 1519–1525, 2003.
37. Tamma G, Lasorsa D, Trimpert C, Ranieri M, Di MA, Mola MG, Mastrofrancesco L, Devuyst O, Svelto M, Deen PM, Valenti G. A protein kinase A-independent pathway controlling aquaporin 2 trafficking as a possible cause for the syndrome of inappropriate antidiuresis associated with polycystic kidney disease 1 haploinsufficiency. J Am Soc Nephrol 25: 2241–2253, 2014.
38. Yamamoto N, Sasaki S, Fushimi K, Ishibashi K, Yaiota E, Kawasaki K, Marumo F, Kihara I. Vasopressin increases AQP-CD water channel in the apical membrane of collecting duct cells without affecting AQP3 distribution in Brattleboro rat. Am J Physiol Cell Physiol 268: C1546–C1551, 1995.
39. Yang CR, Tongyoo P, Emamian M, Sandoval PC, Raghuram V, Knepper MA. Deep proteomic profiling of vasopressin-sensitive collecting duct cells. I. Virtual Western blots and molecular weight distributions. Am J Physiol Cell Physiol (August 26, 2015). doi: 10.1152/ajpcell.00213.2015.
40. Yu MJ, Miller RL, Uawithya P, Rinschen MM, Khositseth S, Braucht DW, Chou CL, Pisitkun T, Nelson RD, Knepper MA. Systems-level analysis of cell-specific AQP2 gene expression in renal collecting duct. Proc Natl Acad Sci USA 106: 2441–2446, 2009.