Global phosphoproteomic profiling reveals perturbed signaling in a mouse model of dilated cardiomyopathy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 44, 2016, Pages 12592-12597

  Kuzmanov, Uros ^a,b   Guo, Hongbo ^a   Buchsbaum, Diana ^a   Cosme, Jake ^a   Abbasi, Cynthia ^a   Isserlin, Ruth ^a   Sharma, Parveen ^a   Gramolini, Anthony O ^a,b   Emili, Andrew ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bioinformatics; Heart disease; Phospholamban; Proteomic; Signaling

Indexed keywords

HEART MUSCLE EXTRACT; NOTCH1 RECEPTOR; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; CALCIUM BINDING PROTEIN; PHOSPHOLAMBAN; PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONFERENCE PAPER; CONFOCAL MICROSCOPY; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE COURSE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PHOSPHOPROTEOMICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CARDIAC MUSCLE; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; PROCEDURES; PROTEOMICS; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CARDIOMYOPATHY, DILATED; DISEASE MODELS, ANIMAL; HUMANS; MICE, TRANSGENIC; MUTATION; MYOCARDIUM; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 84994229296     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1606444113     Document Type: Article

References (51)

1. Mozaffarian D, et al.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2015) Heart disease and stroke statistics. 2015 update: A report from the American Heart Association. Circulation 131(4):e29. e322.
2. Schmitt JP, et al. (2003) Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban. Science 299(5611):1410-1413.
3. MacLennan DH, Kranias EG (2003) Phospholamban: A crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4(7):566-577.
4. Pan Y, et al. (2004) Identification of biochemical adaptations in hyper- or hypocontractile hearts from phospholamban mutant mice by expression proteomics. Proc Natl Acad Sci USA 101(8):2241-2246.
5. Gramolini AO, et al. (2008) Comparative proteomics profiling of a phospholamban mutant mouse model of dilated cardiomyopathy reveals progressive intracellular stress responses. Mol Cell Proteomics 7(3):519-533.
6. Isserlin R, et al. (2015) Systems analysis reveals down-regulation of a network of prosurvival miRNAs drives the apoptotic response in dilated cardiomyopathy. Mol Biosyst 11(1):239-251.
7. Engholm-Keller K, Larsen MR (2013) Technologies and challenges in large-scale phosphoproteomics. Proteomics 13(6):910-931.
8. Lundby A, et al. (2013) In vivo phosphoproteomics analysis reveals the cardiac targets of α-adrenergic receptor signaling. Sci Signal 6(278):rs11.
9. Scholten A, et al. (2013) Phosphoproteomics study based on in vivo inhibition reveals sites of calmodulin-dependent protein kinase II regulation in the heart. J Am Heart Assoc 2(4):e000318.
10. Huttlin EL, et al. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143(7):1174-1189.
11. Sharma P, et al. (2015) Evolutionarily conserved intercalated disc protein Tmem65 regulates cardiac conduction and connexin 43 function. Nat Commun 6:8391.
12. Terrin A, et al. (2012) PKA and PDE4D3 anchoring to AKAP9 provides distinct regulation of cAMP signals at the centrosome. J Cell Biol 198(4):607-621.
13. Vary TC, Lang CH (2008) Differential phosphorylation of translation initiation regulators 4EBP1, S6k1, and Erk 1/2 following inhibition of alcohol metabolism in mouse heart. Cardiovasc Toxicol 8(1):23-32.
14. Venkatesan B, et al. (2010) EMMPRIN activates multiple transcription factors in cardiomyocytes, and induces interleukin-18 expression via Rac1-dependent PI3K/Akt/IKK/NF-kappaB and MKK7/JNK/AP-1 signaling. J Mol Cell Cardiol 49(4):655-663.
15. Bousset K, Henriksson M, Luscher-Firzlaff JM, Litchfield DW, Luscher B (1993) Identification of casein kinase II phosphorylation sites in Max: Effects on DNA-binding kinetics of Max homo- and Myc/Max heterodimers. Oncogene 8(12):3211-3220.
16. Gupta MP, Amin CS, Gupta M, Hay N, Zak R (1997) Transcription enhancer factor 1 interacts with a basic helix-loop-helix zipper protein, Max, for positive regulation of cardiac alpha-myosin heavy-chain gene expression. Mol Cell Biol 17(7):3924-3936.
17. Karin M, Gallagher E (2005) From JNK to pay dirt: Jun. kinases, their biochemistry, physiology and clinical importance. IUBMB Life 57(4-5):283-295.
18. Wang Q, Lin JL, Chan SY, Lin JJ (2013) The Xin repeat-containing protein, mXinα, initiates the maturation of the intercalated discs during postnatal heart development. Dev Biol 374(2):264-280.
19. Chou MF, Schwartz D (2011) Using the scan-x web site to predict protein posttranslational modifications. Curr Protoc Bioinformatics Chapter 13: Unit 13-16.
20. Keshava Prasad TS, et al. (2009) Human Protein Reference Database. 2009 update. Nucleic Acids Res 37(Database issue):D767-D772.
21. Wang Y (2007) Mitogen-activated protein kinases in heart development and diseases. Circulation 116(12):1413-1423.
22. Juhaszova M, et al. (2009) Role of glycogen synthase kinase-3beta in cardioprotection. Circ Res 104(11):1240-1252.
23. Isserlin R, Merico D, Voisin V, Bader GD (2014) Enrichment Map. A Cytoscape app to visualize and explore OMICs pathway enrichment results. F1000Res 3:141.
24. Burke MA, et al. (2016) Molecular profiling of dilated cardiomyopathy that progresses to heart failure. JCI Insight 1(6):e86898.
25. Zhou S, et al. (2000) SKIP, a CBF1-associated protein, interacts with the ankyrin repeat domain of NotchIC to facilitate NotchIC function. Mol Cell Biol 20(7):2400-2410.
26. Espinosa L, Santos S, Ingles-Esteve J, Munoz-Canoves P, Bigas A (2002) p65-NFkappaB synergizes with Notch to activate transcription by triggering cytoplasmic translocation of the nuclear receptor corepressor N-CoR. J Cell Sci 115(Pt 6):1295-1303.
27. Sun Z, Hamilton KL, Reardon KF (2012) Phosphoproteomics and molecular cardiology: Techniques, applications and challenges. J Mol Cell Cardiol 53(3):354-368.
28. Ren J, et al. (2011) Computational analysis of phosphoproteomics: Progresses and perspectives. Curr Protein Pept Sci 12(7):591-601.
29. Morrisey EE (2010) Weary of the stress: Time to put another notch in cardiomyopathy. Circ Res 106(7):1187-1189.
30. Rizzo P, et al. (2015) The role of Notch in the cardiovascular system: Potential adverse effects of investigational Notch inhibitors. Front Oncol 4:384.
31. Ryu HW, Park CW, Ryu KY (2014) Disruption of polyubiquitin gene Ubb causes dysregulation of neural stem cell differentiation with premature gliogenesis. Sci Rep 4:7026.
32. Tang Y, Boucher JM, Liaw L (2012) Histone deacetylase activity selectively regulates Notch-mediated smooth muscle differentiation in human vascular cells. J Am Heart Assoc 1(3):e000901.
33. Chapman G, Sparrow DB, Kremmer E, Dunwoodie SL (2011) Notch inhibition by the ligand DELTA-LIKE 3 defines the mechanism of abnormal vertebral segmentation in spondylocostal dysostosis. Hum Mol Genet 20(5):905-916.
34. Wu M, Li J (2015) Numb family proteins: Novel players in cardiac morphogenesis and cardiac progenitor cell differentiation. Biomol Concepts 6(2):137-148.
35. Fedak PW, et al. (2006) Altered expression of disintegrin metalloproteinases and their inhibitor in human dilated cardiomyopathy. Circulation 113(2):238-245.
36. Urbanek K, et al. (2010) Inhibition of Notch1-dependent cardiomyogenesis leads to a dilated myopathy in the neonatal heart. Circ Res 107(3):429-441.
37. Croquelois A, et al. (2008) Control of the adaptive response of the heart to stress via the Notch1 receptor pathway. J Exp Med 205(13):3173-3185.
38. Metrich M, et al. (2015) Jagged1 intracellular domain-mediated inhibition of Notch1 signalling regulates cardiac homeostasis in the postnatal heart. Cardiovasc Res 108(1):74-86.
39. Gude N, Sussman M (2012) Notch signaling and cardiac repair. J Mol Cell Cardiol 52(6):1226-1232.
40. D'Amato G, Luxan G, de la Pompa JL (2016) Notch signalling in ventricular chamber development and cardiomyopathy. FEBS J, 10.1111/febs.13773.
41. Dvorakova MC, Kruzliak P, Rabkin SW (2014) Role of neuropeptides in cardiomyopathies. Peptides 61:1-6.
42. Zaidi S, et al. (2013) De novo mutations in histone-modifying genes in congenital heart disease. Nature 498(7453):220-223.
43. Cordero-Reyes AM, et al. (2016) Full expression of cardiomyopathy is partly dependent on B-cells: A pathway that involves cytokine activation, immunoglobulin deposition, and activation of apoptosis. J Am Heart Assoc 5(1):e002484.
44. Hofmann U, Frantz S (2015) Role of lymphocytes in myocardial injury, healing, and remodeling after myocardial infarction. Circ Res 116(2):354-367.
45. Dobaczewski M, Chen W, Frangogiannis NG (2011) Transforming growth factor (TGF)-α signaling in cardiac remodeling. J Mol Cell Cardiol 51(4):600-606.
46. Finck BN (2007) The PPAR regulatory system in cardiac physiology and disease. Cardiovasc Res 73(2):269-277.
47. Vallejo JG (2011) Role of Toll-like receptors in cardiovascular diseases. Clin Sci (Lond) 121(1):1-10.
48. Dawson K, Aflaki M, Nattel S (2013) Role of the Wnt-Frizzled system in cardiac pathophysiology: A rapidly developing, poorly understood area with enormous potential. J Physiol 591(6):1409-1432.
49. Beausoleil SA, Villen J, Gerber SA, Rush J, Gygi SP (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 24(10):1285-1292.
50. Chawade A, Alexandersson E, Levander F (2014) Normalyzer: A tool for rapid evaluation of normalization methods for omics data sets. J Proteome Res 13(6):3114-3120.
51. Schwartz D, Chou MF, Church GM (2009) Predicting protein post-translational modifications using meta-analysis of proteome scale data sets. Mol Cell Proteomics 8(2):365-379.