In vivo phosphoproteomics analysis reveals the cardiac targets of β-adrenergic receptor signaling

Science Signaling

Volumn 6, Issue 278, 2013, Pages

  Lundby, Alicia ^a,b,c   Andersen, Martin N ^c   Steffensen, Annette B ^c   Horn, Heiko ^a   Kelstrup, Christian D ^a   Francavilla, Chiara ^a   Jensen, Lars J ^a   Schmitt, Nicole ^c   Thomsen, Morten B ^c   Olsen, Jesper V ^a  

^a University of Copenhagen   (Denmark)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c DANISH NATIONAL RESEARCH FOUNDATION   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE 5' MONOPHOSPHATE ACTIVATED PROTEIN KINASE; BETA ADRENERGIC RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; MAMMALIAN TARGET OF RAPAMYCIN; METOPROLOL; MUTANT PROTEIN; POTASSIUM CHANNEL KV7.1; PROTEIN KINASE; PROTEIN KINASE B; PROTEOME; RHO KINASE; SERINE; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

AMINO ACID SEQUENCE; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA ADRENERGIC STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; HEART RATE; IN VIVO STUDY; ION TRANSPORT; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANIMALS; HEART; MICE; PHOSPHOPROTEINS; PROTEOMICS; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION;

MAMMALIA; MURINAE;

EID: 84878953405     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003506     Document Type: Article

References (62)

1. H. A. Rockman, W. J. Koch, R. J. Lefkowitz, Seven-transmembrane-spanning receptors and heart function. Nature 415, 206-212 (2002).
2. O. E. Osadchii, Cardiac hypertrophy induced by sustained b-adrenoreceptor activation: Pathophysiological aspects. Heart Fail. Rev. 12, 66-86 (2007).
3. F. Waagstein, K. Caidahl, I.Wallentin, C. H. Bergh, A. Hjalmarson, Long-term β-blockade in dilated cardiomyopathy. Effects of short- and long-term metoprolol treatment followed by withdrawal and readministration of metoprolol. Circulation 80, 551-563 (1989).
4. J. V. Olsen, B. Blagoev, F. Gnad, B. Macek, C. Kumar, P. Mortensen, M. Mann, Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (2006).
5. E. L.Huttlin, M. P. Jedrychowski, J.E. Elias, T. Goswami, R. Rad, S. A. Beausoleil, J.Villén, W. Haas, M. E. Sowa, S. P. Gygi, A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189 (2010).
6. A. Lundby, A. Secher, K. Lage, N. B. Nordsborg, A. Dmytriyev, C. Lundby, J. V. Olsen, Quantitative maps of protein phosphorylation sites across 14 different rat organs and tissues. Nat. Commun. 3, 876 (2012).
7. J. R. WiŚniewski, N. Nagaraj, A. Zougman, F. Gnad, M. Mann, Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology. J. Proteome Res. 9, 3280-3289 (2010).
8. 2 adrenoceptors in the human heart. Am. J. Cardiol. 62, 24C-29C (1988).
9. R. A. Hall, β-Adrenergic receptors and their interacting proteins. Semin. Cell Dev. Biol. 15, 281-288 (2004).
10. M. W. Pinkse, P. M. Uitto, M. J. Hilhorst, B. Ooms, A. J. Heck, Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns. Anal. Chem. 76, 3935-3943 (2004).
11. N. Sugiyama, T. Masuda, K. Shinoda, A. Nakamura, M. Tomita, Y. Ishihama, Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Mol. Cell. Proteomics 6, 1103-1109 (2007).
12. N. C. Hubner, A. W. Bird, J. Cox, B. Splettstoesser, P. Bandilla, I. Poser, A. Hyman, M. Mann, Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189, 739-754 (2010).
13. K. Lage, E. O. Karlberg, Z.M. Størling, P. I. Olason, A. G. Pedersen, O. Rigina, A.M. Hinsby, Z. Tümer, F. Pociot, N. Tommerup, Y. Moreau, S. Brunak, A human phenome-interactome network of protein complexes implicated in genetic disorders. Nat. Biotechnol. 25, 309-316 (2007).
14. E. J. Rossin, K. Lage, S. Raychaudhuri, R. J. Xavier, D. Tatar, Y. Benita, C. Cotsapas, M. J. Daly, Proteins encoded in genomic regions associated with immune-mediated disease physically interact and suggest underlying biology. PLoS Genet. 7, e1001273 (2011).
15. D. J. Lynn, G. L. Winsor, C. Chan, N. Richard, M. R. Laird, A. Barsky, J. L. Gardy, F. M. Roche, T. H. Chan, N. Shah, R. Lo, M. Naseer, J. Que, M. Yau, M. Acab, D. Tulpan, M. D. Whiteside, A. Chikatamarla, B. Mah, T. Munzner, K. Hokamp, R. E. Hancock, F. S. Brinkman, InnateDB: Facilitating systems-level analyses of the mammalian innate immune response. Mol. Syst. Biol. 4, 218 (2008).
16. R. Linding, L. J. Jensen, G. J. Ostheimer, M. A. van Vugt, C. Jørgensen, I. M. Miron, F. Diella, K. Colwill, L. Taylor, K. Elder, P. Metalnikov, V. Nguyen, A. Pasculescu, J. Jin, J. G. Park, L. D. Samson, J. R.Woodgett, R. B. Russell, P. Bork, M. B. Yaffe, T. Pawson, Systematic discovery of in vivo phosphorylation networks. Cell 129, 1415-1426 (2007).
17. B. Nolen, S. Taylor, G. Ghosh, Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 15, 661-675 (2004).
18. T. Schmelzle, M. N. Hall, TOR, a central controller of cell growth. Cell 103, 253-262 (2000).
19. 1-subtype in the rat heart. J. Mol. Cell. Cardiol. 33, 561-573 (2001).
20. 2+/calmodulin kinase signaling pathway. Circ. Res. 95, 798-806 (2004).
21. J. V. Olsen, M. Vermeulen, A. Santamaria, C. Kumar, M. L. Miller, L. J. Jensen, F. Gnad, J. Cox, T. S. Jensen, E. A. Nigg, S. Brunak, M. Mann, Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3 (2010).
22. v1.2 phosphorylation site S1928A mutant mice. J. Biol. Chem. 283, 34738-34744 (2008).
23. Ks current (hKCNQ1/hKCNE1) stably expressed in HEK-293 cells. Am. J. Physiol. Heart Circ. Physiol. 295, H1867-H1881 (2008).
24. S. O. Marx, J. Kurokawa, S. Reiken, H. Motoike, J. D'Armiento, A. R. Marks, R. S. Kass, Requirement of a macromolecular signaling complex for β adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel. Science 295, 496-499 (2002).
25. O. Cerda, J. S. Trimmer, Analysis and functional implications of phosphorylation of neuronal voltage-gated potassium channels. Neurosci. Lett. 486, 60-67 (2010).
26. V7.1 surface expression is regulated by epithelial cell polarization. Am. J. Physiol. Cell Physiol. 300, C814-C824 (2011).
27. Ks potassium channel. Nature 384, 80-83 (1996).
28. C. L. Antos, T. A. McKinsey, N. Frey, W. Kutschke, J. McAnally, J. M. Shelton, J. A. Richardson, J. A. Hill, E. N. Olson, Activated glycogen synthase-3β suppresses cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. U.S.A. 99, 907-912 (2002).
29. K. Inoki, H. Ouyang, T. Zhu, C. Lindvall, Y. Wang, X. Zhang, Q. Yang, C. Bennett, Y. Harada, K. Stankunas, C. Y.Wang, X. He, O. A. MacDougald, M. You, B. O. Williams, K. L. Guan, TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126, 955-968 (2006).
30. J. V. Olsen, B. Macek, O. Lange, A. Makarov, S. Horning, M. Mann, Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 4, 709-712 (2007).
31. B. M. Bolstad, R. A. Irizarry, M. Astrand, T. P. Speed, A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193 (2003).
32. T. Geiger, J. Cox, M. Mann, Proteomic changes resulting from gene copy number variations in cancer cells. PLoS Genet. 6, e1001090 (2010).
33. N. Colaert, K. Helsens, L. Martens, J. Vandekerckhove, K. Gevaert, Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 6, 786-787 (2009).
34. M. L. Miller, L. J. Jensen, F. Diella, C. Jørgensen, M. Tinti, L. Li, M. Hsiung, S. A. Parker, J. Bordeaux, T. Sicheritz-Ponten, M. Olhovsky, A. Pasculescu, J. Alexander, S. Knapp, N. Blom, P. Bork, S. Li, G. Cesareni, T. Pawson, B. E. Turk, M. B. Yaffe, S. Brunak, R. Linding, Linear motif atlas for phosphorylation-dependent signaling. Sci. Signal. 1, ra2 (2008).
35. D. Szklarczyk, A. Franceschini, M. Kuhn, M. Simonovic, A. Roth, P. Minguez, T. Doerks, M. Stark, J. Muller, P. Bork, L. J. Jensen, C. von Mering, The STRING database in 2011: Functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568 (2011).
36. M. N. Andersen, K. Krzystanek, T. Jespersen, S. P. Olesen, H. B. Rasmussen, AMP-activated protein kinase downregulates Kv7.1 cell surface expression. Traffic 13, 143-156 (2012).
37. A. Lundby, J. V. Olsen, GeLCMS for in-depth protein characterization and advanced analysis of proteomes. Methods Mol. Biol. 753, 143-155 (2011).
38. A. Lundby, L. S. Ravn, J. H. Svendsen, S. P. Olesen, N. Schmitt, KCNQ1 mutation Q147R is associated with atrial fibrillation and prolonged QT interval. Heart Rhythm 4, 1532-1541 (2007).
39. L. E. Morrison, H. E. Hoover, D. J. Thuerauf, C. C. Glembotski, Mimicking phosphorylation of aB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ. Res. 92, 203-211 (2003).
40. N. S. Rajasekaran, P. Connell, E. S. Christians, L. J. Yan, R. P. Taylor, A. Orosz, X. Q. Zhang, T. J. Stevenson, R. M. Peshock, J. A. Leopold, W. H. Barry, J. Loscalzo, S. J. Odelberg, I. J. Benjamin, Human a B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 130, 427-439 (2007).
41. B. A. Colson, T. Bekyarova, M. R. Locher, D. P. Fitzsimons, T. C. Irving, R. L. Moss, Protein kinase A-mediated phosphorylation of cMyBP-C increases proximity of myosin heads to actin in resting myocardium. Circ. Res. 103, 244-251 (2008).
42. M. Gautel, O. Zuffardi, A. Freiburg, S. Labeit, Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: A modulator of cardiac contraction? EMBO J. 14, 1952-1960 (1995).
43. K. S. Walker, M. Deak, A. Paterson, K. Hudson, P. Cohen, D. R. Alessi, Activation of protein kinase B β and γ isoforms by insulin in vivo and by 3-phosphoinositide-dependent protein kinase-1 in vitro: Comparison with protein kinase B a. Biochem. J. 331 (Pt. 1), 299-308 (1998).
44. R. Ramakrishnan, A. P. Rice, Cdk9 T-loop phosphorylation is regulated by the calcium signaling pathway. J. Cell. Physiol. 227, 609-617 (2012).
45. C. E. McCoy, D. G. Campbell, M. Deak, G. B. Bloomberg, J. S. Arthur, MSK1 activity is controlled by multiple phosphorylation sites. Biochem. J. 387, 507-517 (2005).
46. P. P. Roux, D. Shahbazian, H. Vu, M. K. Holz, M. S. Cohen, J. Taunton, N. Sonenberg, J. Blenis, RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J. Biol. Chem. 282, 14056-14064 (2007).
47. 2+-mediated regulation of NDR protein kinase through autophosphorylation and phosphorylation by an upstream kinase. J. Biol. Chem. 278, 6710-6718 (2003).
48. S. Kumar, M. M. McLaughlin, P. C. McDonnell, J. C. Lee, G. P. Livi, P. R. Young, Human mitogen-activated protein kinase CSBP1, but not CSBP2, complements a hog1 deletion in yeast. J. Biol. Chem. 270, 29043-29046 (1995).
49. C. M. Dreiza, P. Komalavilas, E. J. Furnish, C. R. Flynn, M. R. Sheller, C. C. Smoke, L. B. Lopes, C. M. Brophy, The small heat shock protein, HSPB6, in muscle function and disease. Cell Stress Chaperones 15, 1-11 (2010).
50. H. Sano, S. Kane, E. Sano, C. P. Mîinea, J. M. Asara, W. S. Lane, C. W. Garner, G. E. Lienhard, Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem. 278, 14599-14602 (2003).
51. C. Morisco, G. Condorelli, V. Trimarco, A. Bellis, C. Marrone, J. Sadoshima, B. Trimarco, Akt mediates the cross-talk between β-adrenergic and insulin receptors in neonatal cardiomyocytes. Circ. Res. 96, 180-188 (2005).
52. L. D. Aicher, J. S. Campbell, R. S. Yeung, Tuberin phosphorylation regulates its interaction with hamartin. Two proteins involved in tuberous sclerosis. J. Biol. Chem. 276, 21017- 21021 (2001).
53. B. C. Mak, K. Takemaru, H. L. Kenerson, R. T. Moon, R. S. Yeung, The tuberin-hamartin complex negatively regulates β-catenin signaling activity. J. Biol. Chem. 278, 5947-5951 (2003).
54. M. Nellist, P. C. Burgers, A. M. van den Ouweland, D. J. Halley, T. M. Luider, Phosphorylation and binding partner analysis of the TSC1-TSC2 complex. Biochem. Biophys. Res. Commun. 333, 818-826 (2005).
55. D. Shahbazian, P. P. Roux, V. Mieulet, M. S. Cohen, B. Raught, J. Taunton, J. W. Hershey, J. Blenis, M. Pende, N. Sonenberg, The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. EMBO J. 25, 2781-2791 (2006).
56. A. C. Gingras, B. Raught, N. Sonenberg, Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15, 807-826 (2001).
57. +-ATPase. Am. J. Physiol. Cell Physiol. 299, C1363- C1369 (2010).
58. X. H. Wehrens, S. E. Lehnart, S. Reiken, J. A. Vest, A.Wronska, A. R. Marks, Ryanodine receptor/calcium release channel PKA phosphorylation: A critical mediator of heart failure progression. Proc. Natl. Acad. Sci. U.S.A. 103, 511-518 (2006).
59. A. Kumar, T. E. Harris, S. R. Keller, K. M. Choi, M. A. Magnuson, J. C. Lawrence Jr., Muscle-specific deletion of rictor impairs insulin-stimulated glucose transport and enhances Basal glycogen synthase activity. Mol. Cell. Biol. 28, 61-70 (2008).
60. S. Grably, A. Rossi, Changes in cardiac glycogen synthase and phosphorylase activities following stimulation of b-adrenergic receptors in rats. Basic Res. Cardiol. 80, 175-181 (1985).
61. J. Layland, R. J. Solaro, A. M. Shah, Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc. Res. 66, 12-21 (2005).
62. A. E. Messer, A. M. Jacques, S. B. Marston, Troponin phosphorylation and regulatory function in human heart muscle: Dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J. Mol. Cell. Cardiol. 42, 247-259 (2007).