Proteomic profiling of nuclear fractions from native renal inner medullary collecting duct cells

Physiological Genomics

Volumn 48, Issue 2, 2016, Pages 154-166

  Pickering, Christina M ^a   Grady, Cameron ^a   Medvar, Barbara ^a   Emamian, Milad ^a   Sandoval, Pablo C ^a   Zhao, Yue ^a   Yang, Chin Rang ^a   Jun Jung, Hyun ^a   Chou, Chung Lin ^a   Knepper, Mark A ^a  

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

Author keywords

Aquaporin 2; Chromatin; Kidney; LC MS MS; mRNA splicing; Transcription; Transcription factor

Indexed keywords

DESMOPRESSIN; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYOSIN LIGHT CHAIN KINASE; PROTEIN SERINE THREONINE KINASE; PROTEOME; TRANSCRIPTION FACTOR; VASOPRESSIN; CHROMATIN; MESSENGER RNA; VASOPRESSIN DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; KIDNEY COLLECTING TUBULE; KIDNEY INNER MEDULLA; MALE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEOMICS; RAT; ANIMAL; BIOLOGY; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION PROFILING; KIDNEY; KIDNEY MEDULLA; METABOLISM; SPRAGUE DAWLEY RAT; TANDEM MASS SPECTROMETRY;

ANIMALS; CELL NUCLEUS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; KIDNEY; KIDNEY MEDULLA; KIDNEY TUBULES, COLLECTING; MALE; MASS SPECTROMETRY; PROTEOME; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TANDEM MASS SPECTROMETRY; VASOPRESSINS;

EID: 84961367931     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00090.2015     Document Type: Article

References (70)

1. Bansal AD, Hoffert JD, Pisitkun T, Hwang S, Chou CL, Boja ES, Wang G, Knepper MA. Phosphoproteomic profiling reveals vasopressin-regulated phosphorylation sites in collecting duct. J Am Soc Nephrol 21: 303-315, 2010.
2. Barile M, Pisitkun T, Yu MJ, Chou CL, Verbalis MJ, Shen RF, Knepper MA. Large scale protein identification in intracellular aqua-porin-2 vesicles from renal inner medullary collecting duct. Mol Cell Proteom 4: 1095-1106, 2005.
3. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837, 2007.
4. Barski A, Zhao K. Genomic location analysis by ChIP-Seq. J Cell Biochem 107: 11-18, 2009.
5. 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.
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. Bulyk ML. Analysis of sequence specificities of DNA-binding proteins with protein binding microarrays. Meth Enzymol 410: 279-299, 2006.
8. Busser BW, Bulyk ML, Michelson AM. Toward a systems-level under-standing of developmental regulatory networks. Curr Opin Genet Dev 18: 521-529, 2008.
9. Champigneulle A, Siga E, Vassent G, Imbert-Teboul M. V2-like vasopressin receptor mobilizes intracellular Ca2 in medullary collecting tubules. Am J Physiol Renal Fluid Electrolyte Physiol 265: F35-F45, 1993.
10. Chou CL, DiGiovanni SR, Luther A, Lolait SJ, Knepper MA. Oxytocin as an antidiuretic hormone. II. Role of V2 vasopressin receptor. Am J Physiol Renal Fluid Electrolyte Physiol 269: F78-F85, 1995.
11. Chou CL, Rapko SI, Knepper MA. Phosphoinositide signaling in rat inner medullary collecting duct. Am J Physiol Renal Physiol 274: F564-F572, 1998.
12. Chou CL, Yip KP, Michea L, Kador K, Ferraris J, Wade JB, Knepper MA. Regulation of aquaporin-2 trafficking by vasopressin in renal collecting duct: roles of ryanodine-sensitive Ca2 stores and calmodulin. J Biol Chem 275: 36839-36846, 2000.
13. Davis TA, Loos B, Engelbrecht AM. AHNAK: the giant jack of all trades. Cell Signal 26: 2683-2693, 2014.
14. Ecelbarger CA, Chou CL, Lolait SJ, Knepper MA, DiGiovanni SR. Evidence for dual signaling pathways for V2 vasopressin receptor in rat inner medullary collecting duct. Am J Physiol Renal Fluid Electrolyte Physiol 270: F623-F633, 1996.
15. Ecelbarger CA, Nielsen S, Olson BR, Murase T, Baker EA, Kneppe MA, Verbalis JG. Role of renal aquaporins in escape from vasopressin-induced antidiuresis in rat. J Clin Invest 99: 1852-1863, 1997.
16. Elias JE, Gygi SP. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Meth 4: 207-214, 2007.
17. Gaj T, Gersbach CA, Barbas CF 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31: 397-405, 2013.
18. Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19: 1720-1730, 1999.
19. Hasler U, Jeon US, Kim JA, Mordasini D, Kwon HM, Feraille E, Martin PY. Tonicity-responsive enhancer binding protein is an essential regulator of aquaporin-2 expression in renal collecting duct principal cells. J Am Soc Nephrol 17: 1521-1531, 2006.
20. Hayashi M, Sasaki S, Tsuganezawa H, Monkawa T, Kitajima W, Konishi K, Fushimi K, Marumo F, Saruta T. Expression and distribution of aquaporin of collecting duct are regulated by V2 receptor in rat kidney. J Clin Invest 94: 1778-1783, 1994.
21. Hoffert JD, Pisitkun T, Saeed F, Song JH, Chou CL, Knepper MA. Dynamics of the G protein-coupled vasopressin V2 receptor signaling network revealed by quantitative phosphoproteomics. Mol Cell Proteom 11: M111, 2012.
22. Hoffert JD, Pisitkun T, Saeed F, Wilson JL, Knepper MA. Global analysis of the effects of the V2 receptor antagonist satavaptan on protein phosphorylation in collecting duct. Am J Physiol Renal Physiol 306: F410-F421, 2014.
23. 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.
24. Hoffert JD, van Balkom BW, Chou CL, Knepper MA. Application of difference gel electrophoresis to the identification of inner medullary collecting duct proteins. Am J Physiol Renal Physiol 286: F170-F179, 2004.
25. Hoorn EJ, Hoffert JD, Knepper MA. Combined proteomics and path-ways analysis of collecting duct reveals a protein regulatory network activated in vasopressin escape. J Am Soc Nephrol 16: 2852-2863, 2005.
26. Hozawa S, Holtzman EJ, Ausiello DA. cAMP motifs regulating transcription in the aquaporin-2 gene. Am J Physiol Cell Physiol 270: C1695-C1702, 1996.
27. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57, 2009.
28. Ideker T, Thorsson V, Ranish JA, Christmas R, Buhler J, Eng JK, Bumgarner R, Goodlett DR, Aebersold R, Hood L. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292: 929-934, 2001.
29. 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 Proteom 10: M110, 2011.
30. Knepper MA. Systems biology in physiology: the vasopressin signaling network in kidney. Am J Physiol Cell Physiol 303: C1115-C1124, 2012.
31. Knepper MA. Systems biology of diuretic resistance. J Clin Invest 125: 1793-1795, 2015.
32. Lee JW, Chou CL, Knepper MA. Deep sequencing in microdissected renal tubules identifies nephron segment-specific transcriptomes. J Am Soc Nephrol 26: 2669-2677, 2015.
33. Li SZ, McDill BW, Kovach PA, Ding L, Go WY, Ho SN, Chen F. Calcineurin-NFATc signaling pathway regulates AQP2 expression in response to calcium signals and osmotic stress. Am J Physiol Cell Physiol 292: C1606-C1616, 2007.
34. Matsumura Y, Uchida S, Rai T, Sasaki S, Marumo F. Transcriptional regulation of aquaporin-2 water channel gene by cAMP. J Am Soc Nephrol 8: 861-867, 1997.
35. Mundade R, Ozer HG, Wei H, Prabhu L, Lu T. Role of ChIP-seq in the discovery of transcription factor binding sites, differential gene regulation mechanism, epigenetic marks and beyond. Cell Cycle 13: 2847-2852, 2014.
36. 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.
37. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knep-per 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.
38. 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.
39. Pisitkun T, Bieniek J, Tchapyjnikov D, Wang G, Wu WW, Shen RF, Knepper MA. High-throughput identification of IMCD proteins using LC-MS/MS. Physiol Genomics 25: 263-276, 2006.
40. 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.
41. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 101: 13368-13373, 2004.
42. Rai T, Uchida S, Marumo F, Sasaki S. Cloning of rat and mouse aquaporin-2 gene promoters and identification of a negative cis-regulatory element. Am J Physiol Renal Physiol 273: F264-F273, 1997.
43. Rinschen MM, Yu MJ, Wang G, Boja ES, Hoffert JD, Pisitkun T, Knepper MA. Quantitative phosphoproteomic analysis reveals vasopres- sin V2-receptor-dependent signaling pathways in renal collecting duct cells. Proc Natl Acad Sci USA 107: 3887, 2010.
44. Robert-Nicoud M, Flahaut M, Elalouf JM, Nicod M, Salinas M, Bens M, Doucet A, Wincker P, Artiguenave F, Horisberger JD, Vandewalle A, Rossier BC, Firsov D. Transcriptome of a mouse kidney cortical collecting duct cell line: effects of aldosterone and vasopressin. Proc Natl Acad Sci USA 98: 2712-2716, 2001.
45. 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.
46. 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.
47. 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.
48. Savitski MM, Lemeer S, Boesche M, Lang M, Mathieson T, Bantscheff M, Kuster B. Confident phosphorylation site localization using the Mascot Delta Score. Mol Cell Proteom 10: M110, 2011.
49. 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.
50. Simons BL, Wang G, Shen RF, Knepper MA. In vacuo isotope coded alkylation technique (IVICAT); an N-terminal stable isotopic label for quantitative liquid chromatography/mass spectrometry proteomics. Rapid Commun Mass Spectrom 20: 2463-2477, 2006.
51. Star RA, Nonoguchi H, Balaban R, Knepper MA. Calcium and cyclic adenosine monophosphate as second messengers for vasopressin in the rat inner medullary collecting duct. J Clin Invest 81: 1879-1888, 1988.
52. Strange K, Spring KR. Cell membrane water permeability of rabbit cortical collecting duct. J Membr Biol 96: 27-43, 1987.
53. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von MC. STRING v10: protein-protein interation networks, integrated over the tree of life. Nucleic Acids Res 43: D447-D452, 2015.
54. Tanner S, Shu H, Frank A, Wang LC, Zandi E, Mumby M, Pevzner PA, Bafna V. InsPecT: identification of posttranslationally modified peptides from tandem mass spectra. Anal Chem 77: 4626-4639, 2005.
55. Tchapyjnikov D, Li Y, Pisitkun T, Hoffert JD, Yu MJ, Knepper MA. Proteomic profiling of nuclei from native renal inner medullary collecting duct cells using LC-MS/MS. Physiol Genomics 40: 167-183, 2010.
56. Trepiccione F, Pisitkun T, Hoffert JD, Poulsen SB, Capasso G, Nielsen S, Knepper MA, Fenton RA, Christensen BM. Early targets of lithium in rat kidney inner medullary collecting duct include p38 and ERK1/2. Kidney Int 86: 757-767, 2014.
57. Uawithya P, Pisitkun T, Ruttenberg BE, Knepper MA. Transcriptional profiling of native inner medullary collecting duct cells from rat kidney. Physiol Genomics 32: 229-253, 2008.
58. Uchida S, Matsumura Y, Rai T, Sasaki S, Marumo F. Regulation of aquaporin-2 gene transcription by GATA-3. Biochem Biophys Res Com-mun 232: 65-68, 1997.
59. van Balkom BW, Hoffert JD, Chou CL, Knepper MA. Proteomic analysis of long-term vasopressin action in the inner medullary collecting duct of the Brattleboro rat. Am J Physiol Renal Physiol 286: F216-F224, 2004.
60. Vizcaino JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Rios D, Dianes JA, Sun Z, Farrah T, Bandeira N, Binz PA, Xenarios I, Eisenacher M, Mayer G, Gatto L, Campos A, Chalkley RJ, Kraus HJ, Albar JP, Martinez-Bartolome S, Apweiler R, Omenn GS, Martens L, Jones AR, Hermjakob H. ProteomeXchange provides globally coordi- nated proteomics data submission and dissemination. Nat Biotechnol 32: 223-226, 2014.
61. Washburn MP, Koller A, Oshiro G, Ulaszek RR, Plouffe D, Deciu C, Winzeler E, Yates JR 3rd. Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100: 3107-3112, 2003.
62. Wilson JL, Miranda CA, Knepper MA. Vasopressin and the regulation of aquaporin-2. Clin Exp Nephrol 17: 751-764, 2013.
63. Yang CR, Raghuram V, Emamian M, Sandoval PC, Knepper MA. Deep proteomic profiling of vasopressin-sensitive collecting duct cells. II. Bioinformatic analysis of vasopressin signaling. Am J Physiol Cell Physiol 309: C799-C812, 2015.
64. 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 309: C785-C798, 2015.
65. Yasui M, Zelenin SM, Celsi G, Aperia A. Adenylate cyclase-coupled vasopressin receptor activates AQP2 promoter via a dual effect on CRE and AP1 elements. Am J Physiol Renal Physiol 272: F443-F450, 1997.
66. Yates JR 3rd, Eng JK, McCormack AL, Schieltz D. Method to correlatetandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67: 1426-1436, 1995.
67. Yip KP. Coupling of vasopressin-induced intracellular Ca2 mobilization and apical exocytosis in perfused rat kidney collecting duct. J Physiol 538: 891-899, 2002.
68. 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.
69. Yu MJ, Pisitkun T, Wang G, Shen RF, Knepper MA. LC-MS/MS analysis of apical and basolateral plasma membranes of rat renal collecting duct cells. Mol Cell Proteom 5: 2131-2145, 2006.
70. Zhao B, Knepper MA, Chou CL, Pisitkun T. Large-scale phosphoty rosine proteomic profiling of rat renal collecting duct epithelium reveals predominance of proteins involved in cell polarity determination. Am J Physiol Cell Physiol 302: C27-C45, 2012.