Hypoxia-Induced Changes in the Fibroblast Secretome, Exosome, and Whole-Cell Proteome Using Cultured, Cardiac-Derived Cells Isolated from Neonatal Mice

Journal of Proteome Research

Volumn 16, Issue 8, 2017, Pages 2836-2847

  Cosme, Jake ^a   Guo, Hongbo ^a   Hadipour Lakmehsari, Sina ^a   Emili, Andrew ^a   Gramolini, Anthony O ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

cardiac fibroblast; cardiovascular; exosome; paracrine factors; secretome

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ALPHA TUBULIN; CD81 ANTIGEN; FLOTILLIN 1; OXYGEN; PROTEOME; VIMENTIN; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIAC MUSCLE CELL; CELL COMMUNICATION; CELL HYPOXIA; CELL LYSATE; CELL VIABILITY; CONDITIONED MEDIUM; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EXOSOME; EXTRACELLULAR MATRIX; GOLGI MEMBRANE; HEART DEVELOPMENT; HEART FIBROBLAST; HYDROPHILIC INTERACTION CHROMATOGRAPHY; IN VITRO STUDY; INTRACELLULAR SIGNALING; MITOCHONDRIAL MEMBRANE; MOUSE; NEWBORN; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; REOXYGENATION; WHOLE CELL; ANIMAL; CARDIAC MUSCLE; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; FIBROBLAST; HYPOXIA; METABOLISM; PATHOLOGY; SECRETION (PROCESS);

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; EXOSOMES; FIBROBLASTS; HYPOXIA; MICE; MYOCARDIUM; OXYGEN; PROTEINS; PROTEOME;

EID: 85027218455     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.7b00144     Document Type: Article

References (50)

1. Nakazato, K.; Naganuma, W.; Ogawa, K.; Yaoita, H.; Mizuno, S.; Nakamura, T.; Maruyama, Y. Attenuation of ischemic myocardial injury and dysfunction by cardiac fibroblast-derived factor(s) Fukushima J. Med. Sci. 2010, 56, 1-16 10.5387/fms.56.1
2. Abrial, M.; Da Silva, C. C.; Pillot, B.; Augeul, L.; Ivanes, F.; Teixeira, G.; Cartier, R.; Angoulvant, D.; Ovize, M.; Ferrera, R. Cardiac fibroblasts protect cardiomyocytes against lethal ischemia-reperfusion injury J. Mol. Cell. Cardiol. 2014, 68, 56-65 10.1016/j.yjmcc.2014.01.005
3. Pedrotty, D. M.; Klinger, R. Y.; Kirkton, R. D.; Bursac, N. Cardiac fibroblast paracrine factors alter impulse conduction and ion channel expression of neonatal rat cardiomyocytes Cardiovasc. Res. 2009, 83, 688-697 10.1093/cvr/cvp164
4. Bang, C.; Batkai, S.; Dangwal, S.; Gupta, S. K.; Foinquinos, A.; Holzmann, A.; Just, A.; Remke, J.; Zimmer, K.; Zeug, A.; Ponimaskin, E.; Schmiedl, A.; Yin, X.; Mayr, M.; Halder, R.; Fischer, A.; Engelhardt, S.; Wei, Y.; Schober, A.; Fiedler, J.; Thum, T. Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy J. Clin. Invest. 2014, 124, 2136-2146 10.1172/JCI70577
5. Ieda, M.; Tsuchihashi, T.; Ivey, K. N.; Ross, R. S.; Hong, T.-T.; Shaw, R. M.; Srivastava, D. Cardiac Fibroblasts Regulate Myocardial Proliferation through β1 Integrin Signaling Dev. Cell 2009, 16, 233-244 10.1016/j.devcel.2008.12.007
6. Jonsson, M. K. B.; Hartman, R. J. G.; Ackers-Johnson, M.; Tan, W. L. W.; Lim, B.; van Veen, T. A. B.; Foo, R. S. A Transcriptomic and Epigenomic Comparison of Fetal and Adult Human Cardiac Fibroblasts Reveals Novel Key Transcription Factors in Adult Cardiac Fibroblasts JACC: Basic to Translational Science 2016, 1 (7) 590-602 10.1016/j.jacbts.2016.07.007
7. Malik, Z. A.; Kott, K. S.; Poe, A. J.; Kuo, T.; Chen, L.; Ferrara, K. W.; Knowlton, A. A. Cardiac myocyte exosomes: stability, HSP60, and proteomics Am. J. Physiol-Heart and Circulatory Physiology 2013, 304, H954-H965 10.1152/ajpheart.00835.2012
8. Stastna, M.; Chimenti, I.; Marbán, E.; Van Eyk, J. E. Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes Proteomics 2010, 10, 245-253 10.1002/pmic.200900515
9. Cosme, J.; Liu, P. P.; Gramolini, A. O. The cardiovascular exosome: Current perspectives and potential Proteomics 2013, 13 (10-11) 1654-1659 10.1002/pmic.201200441
10. Johnstone, R. M.; Adam, M.; Hammond, J. R.; Orr, L.; Turbide, C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes) J. Biol. Chem. 1987, 262, 9412-9420
11. Gupta, S.; Knowlton, A. A. HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway Am. J. Physiol-Heart and Circulatory Physiology 2007, 292 (6) H3052 10.1152/ajpheart.01355.2006
12. Watson, C. J.; Collier, P.; Tea, I.; Neary, R.; Watson, J. A.; Robinson, C.; Phelan, D.; Ledwidge, M. T.; McDonald, K. M.; McCann, A.; Sharaf, O.; Baugh, J. A. Hypoxia-induced epigenetic modifications are associated with cardiac tissue fibrosis and the development of a myofibroblast-like phenotype Hum. Mol. Genet. 2014, 23, 2176-2188 10.1093/hmg/ddt614
13. Chis, R.; Sharma, P.; Bousette, N.; Miyake, T.; Wilson, A.; Backx, P. H.; Gramolini, A. O. α-Crystallin B prevents apoptosis after H2O2 exposure in mouse neonatal cardiomyocytes Am. J. Physiol-Heart and Circulatory Physiology 2012, 303, H967-H978 10.1152/ajpheart.00040.2012
14. Ackers-Johnson, M.; Li, P. Y.; Holmes, A. P.; O'Brien, S.-M.; Pavlovic, D.; Foo, R. S. A Simplified, Langendorff-Free Method for Concomitant Isolation of Viable Cardiac Myocytes and Nonmyocytes From the Adult Mouse Heart- Novelty and Significance Circ. Res. 2016, 119, 909-920 10.1161/CIRCRESAHA.116.309202
15. Théry, C.; Amigorena, S.; Raposo, G.; Clayton, A., Isolation and Characterization of Exosomes from Cell Culture Supernatants and Biological Fluids. In Current Protocols in Cell Biology; John Wiley & Sons, Inc., 2006.
16. Mathivanan, S.; Ji, H.; Simpson, R. J. Exosomes: Extracellular organelles important in intercellular communication J. Proteomics 2010, 73, 1907-1920 10.1016/j.jprot.2010.06.006
17. Sinha, A.; Ignatchenko, V.; Ignatchenko, A.; Mejia-Guerrero, S.; Kislinger, T. In-depth proteomic analyses of ovarian cancer cell line exosomes reveals differential enrichment of functional categories compared to the NCI 60 proteome Biochem. Biophys. Res. Commun. 2014, 445, 694-701 10.1016/j.bbrc.2013.12.070
18. Gramolini, A. O.; Kislinger, T.; Liu, P.; MacLennan, D. H.; Emili, A. Analyzing the cardiac muscle proteome by liquid chromatography-mass spectrometry-based expression proteomics Methods Mol. Biol. (Clifton, N.J.) 2006, 357, 15-32 10.1385/1-59745-214-9:15
19. Washburn, M. P.; Wolters, D.; Yates, J. R. Large-scale analysis of the yeast proteome by multidimensional protein identification technology Nat. Biotechnol. 2001, 19, 242-247 10.1038/85686
20. Kim, Y.; Ignatchenko, V.; Yao, C. Q.; Kalatskaya, I.; Nyalwidhe, J. O.; Lance, R. S.; Gramolini, A. O.; Troyer, D. A.; Stein, L. D.; Boutros, P. C.; Medin, J. A.; Semmes, O. J.; Drake, R. R.; Kislinger, T. Identification of differentially expressed proteins in direct expressed prostatic secretions of men with organ-confined versus extracapsular prostate cancer Mol. Cell. Proteomics 2012, 11, 1870-84 10.1074/mcp.M112.017889
21. Guo, H.; Garcia-Vedrenne, A. E.; Isserlin, R.; Lugowski, A.; Morada, A.; Sun, A.; Miao, Y.; Kuzmanov, U.; Wan, C.; Ma, H.; Foltz, K.; Emili, A. Phosphoproteomic Network Analysis in the Sea Urchin Strongylocentrotus purpuratus Reveals New Candidates in Egg Activation Proteomics 2015, 15 (23-24) 4080-4095 10.1002/pmic.201500159
22. Guo, H.; Isserlin, R.; Chen, X.; Wang, W.; Phanse, S.; Zandstra, P. W.; Paddison, P. J.; Emili, A. Integrative network analysis of signaling in human CD34+ hematopoietic progenitor cells by global phosphoproteomic profiling using TiO2 enrichment combined with 2D LC-MS/MS and pathway mapping Proteomics 2013, 13 (8) 1325-1333 10.1002/pmic.201200369
23. Sepiashvili, L.; Waggott, D.; Hui, A.; Shi, W.; Su, S.; Ignatchenko, A.; Ignatchenko, V.; Laureano, M.; Huang, S. H.; Xu, W.; Weinreb, I.; Waldron, J.; O'Sullivan, B.; Irish, J. C.; Boutros, P. C.; Liu, F.-F.; Kislinger, T. Integrated Omic Analysis of Oropharyngeal Carcinomas Reveals Human Papillomavirus (HPV)-dependent Regulation of the Activator Protein 1 (AP-1) Pathway Mol. Cell. Proteomics 2014, 13, 3572-3584 10.1074/mcp.M114.041764
24. Choi, H.; Fermin, D.; Nesvizhskii, A. I. Significance Analysis of Spectral Count Data in Label-free Shotgun Proteomics Mol. Cell. Proteomics 2008, 7, 2373-2385 10.1074/mcp.M800203-MCP200
25. Eisen, M. B.; Spellman, P. T.; Brown, P. O.; Botstein, D. Cluster analysis and display of genome-wide expression patterns Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 14863-14868 10.1073/pnas.95.25.14863
26. Saldanha, A. J. Java Treeview-extensible visualization of microarray data Bioinformatics 2004, 20, 3246-3248 10.1093/bioinformatics/bth349
27. Huang, D. W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2008, 4, 44-57 10.1038/nprot.2008.211
28. Huang, D. W.; Sherman, B. T.; Lempicki, R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res. 2009, 37, 1-13 10.1093/nar/gkn923
29. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26, 1367-1372 10.1038/nbt.1511
30. Kuzmanov, U.; Guo, H.; Buchsbaum, D.; Cosme, J.; Abbasi, C.; Isserlin, R.; Sharma, P.; Gramolini, A. O.; Emili, A. Global phosphoproteomic profiling reveals perturbed signaling in a mouse model of dilated cardiomyopathy Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 12592-12597 10.1073/pnas.1606444113
31. Ignatchenko, V.; Ignatchenko, A.; Sinha, A.; Boutros, P. C.; Kislinger, T. VennDIS: A JavaFX-based Venn and Euler diagram software to generate publication quality figures Proteomics 2015, 15, 1239-1244 10.1002/pmic.201400320
32. Abonnenc, M.; Nabeebaccus, A. A.; Mayr, U.; Barallobre-Barreiro, J.; Dong, X.; Cuello, F.; Sur, S.; Drozdov, I.; Langley, S. R.; Lu, R.; Stathopoulou, K.; Didangelos, A.; Yin, X.; Zimmermann, W.-H.; Shah, A. M.; Zampetaki, A.; Mayr, M. Extracellular Matrix Secretion by Cardiac Fibroblasts: Role of MicroRNA-29b and MicroRNA-30c Circ. Res. 2013, 113, 1138-1147 10.1161/CIRCRESAHA.113.302400
33. Lyu, L.; Wang, H.; Li, B.; Qin, Q.; Qi, L.; Nagarkatti, M.; Nagarkatti, P.; Janicki, J. S.; Wang, X. L.; Cui, T. A critical role of cardiac fibroblast-derived exosomes in activating renin angiotensin system in cardiomyocytes J. Mol. Cell. Cardiol. 2015, 89, 268-279 10.1016/j.yjmcc.2015.10.022
34. de Jong, O. G.; Verhaar, M. C.; Chen, Y.; Vader, P.; Gremmels, H.; Posthuma, G.; Schiffelers, R. M.; Gucek, M.; van Balkom, B. W. M. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes J. Extracell. Vesicles 2012, 1, 18396 10.3402/jev.v1i0.18396
35. Principe, S.; Jones, E. E.; Kim, Y.; Sinha, A.; Nyalwidhe, J. O.; Brooks, J.; Semmes, O. J.; Troyer, D. A.; Lance, R. S.; Kislinger, T.; Drake, R. R. In-depth proteomic analyses of exosomes isolated from expressed prostatic secretions in urine Proteomics 2013, 13, 1667-1671 10.1002/pmic.201200561
36. Nonnis, S.; Maffioli, E.; Zanotti, L.; Santagata, F.; Negri, A.; Viola, A.; Elliman, S.; Tedeschi, G. Effect of fetal bovine serum in culture media on MS analysis of mesenchymal stromal cells secretome EuPa Open Proteomics 2016, 10, 28-30 10.1016/j.euprot.2016.01.005
37. Santiago, J.-J.; Dangerfield, A. L.; Rattan, S. G.; Bathe, K. L.; Cunnington, R. H.; Raizman, J. E.; Bedosky, K. M.; Freed, D. H.; Kardami, E.; Dixon, I. M. C. Cardiac fibroblast to myofibroblast differentiation in vivo and in vitro: Expression of focal adhesion components in neonatal and adult rat ventricular myofibroblasts Dev. Dyn. 2010, 239, 1573-1584 10.1002/dvdy.22280
38. Biniecka, M.; Fox, E.; Gao, W.; Ng, C. T.; Veale, D. J.; Fearon, U.; O'Sullivan, J. Hypoxia induces mitochondrial mutagenesis and dysfunction in inflammatory arthritis Arthritis Rheum. 2011, 63, 2172-2182 10.1002/art.30395
39. Quackenbush, J.; Cassidy, P.; Pfeffer, L.; Boucher, K.; Hawkes, J.; Pfeffer, S.; Kopelovich, L.; Leachman, S. Isolation of Circulating MicroRNAs from Microvesicles Found in Human Plasma Methods Mol. Biol. 2014, 1102, 641-53 10.1007/978-1-62703-727-3-34
40. Lamparski, H. G.; Metha-Damani, A.; Yao, J.-Y.; Patel, S.; Hsu, D.-H.; Ruegg, C.; Le Pecq, J.-B. Production and characterization of clinical grade exosomes derived from dendritic cells J. Immunol. Methods 2002, 270, 211-226 10.1016/S0022-1759(02)00330-7
41. Anderson, N. L.; Anderson, N. G. The Human Plasma Proteome Mol. Cell. Proteomics 2002, 1, 845-867 10.1074/mcp.R200007-MCP200
42. Chugh, S.; Ouzounian, M.; Lu, Z.; Mohamed, S.; Li, W.; Bousette, N.; Liu, P. P.; Gramolini, A. O. Pilot study identifying myosin heavy chain 7, desmin, insulin-like growth factor 7, and annexin A2 as circulating biomarkers of human heart failure Proteomics 2013, 13, 2324-2334 10.1002/pmic.201200455
43. González-Juanatey, J. R.; Iglesias, M. J.; Alcaide, C.; Piñeiro, R.; Lago, F. Doxazosin Induces Apoptosis in Cardiomyocytes Cultured In Vitro by a Mechanism That Is Independent of α-Adrenergic Blockade Circulation 2003, 107, 127 10.1161/01.CIR.0000043803.20822.D1
44. Taimor, G.; Lorenz, H.; Hofstaetter, B.; Schlüter, K.-D.; Piper, H. M. Induction of necrosis but not apoptosis after anoxia and reoxygenation in isolated adult cardiomyocytes of rat Cardiovasc. Res. 1999, 41, 147-156 10.1016/S0008-6363(98)00209-0
45. Guo, M.; Song, L. P.; Jiang, Y.; Liu, W.; Yu, Y.; Chen, G. Q. Hypoxia-mimetic agents desferrioxamine and cobalt chloride induce leukemic cell apoptosis through different hypoxia-inducible factor-1α independent mechanisms Apoptosis 2006, 11, 67-77 10.1007/s10495-005-3085-3
46. Bang, C.; Thum, T. Exosomes: New players in cell-cell communication Int. J. Biochem. Cell Biol. 2012, 44, 2060-2064 10.1016/j.biocel.2012.08.007
47. Furtado, M. B.; Nim, H. T.; Boyd, S. E.; Rosenthal, N. A. View from the heart: cardiac fibroblasts in development, scarring and regeneration Development 2016, 143, 387-397 10.1242/dev.120576
48. Porrello, E. R.; Mahmoud, A. I.; Simpson, E.; Hill, J. A.; Richardson, J. A.; Olson, E. N.; Sadek, H. A. Transient regenerative potential of the neonatal mouse heart Science 2011, 331, 1078-80 10.1126/science.1200708
49. Porrello, E. R.; Mahmoud, A. I.; Simpson, E.; Johnson, B. A.; Grinsfelder, D.; Canseco, D.; Mammen, P. P.; Rothermel, B. A.; Olson, E. N.; Sadek, H. A. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 187-92 10.1073/pnas.1208863110
50. Giordano, F. J. Oxygen, oxidative stress, hypoxia, and heart failure J. Clin. Invest. 2005, 115, 500-8 10.1172/JCI200524408