Proteomic analysis reveals distinct metabolic differences between granulocyte-macrophage colony stimulating factor (GM-CSF) and macrophage colony stimulating factor (M-CSF) grown macrophages derived from murine bone marrow cells

Molecular and Cellular Proteomics

Volumn 14, Issue 10, 2015, Pages 2722-2732

  Na, Yi Rang ^a   Hong, Ji Hye ^b   Lee, Min Yong ^b   Jung, Jae Hun ^b   Jung, Daun ^a   Kim, Young Won ^a   Son, Dain ^a   Choi, Murim ^a   Kim, Kwang Pyo ^b   Seok, Seung Hyeok ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ACTIVATING TRANSCRIPTION FACTOR 4; CD71 ANTIGEN; COLONY STIMULATING FACTOR 1; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCOSE TRANSPORTER 1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GUANOSINE TRIPHOSPHATASE; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HEPATOCYTE NUCLEAR FACTOR 1BETA; HEPATOCYTE NUCLEAR FACTOR 3BETA; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; LACTOFERRIN; MYC PROTEIN; NITROGEN DERIVATIVE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; RAS PROTEIN; REGULATOR PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RIBOSE 5 PHOSPHATE; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FKHR; TRANSFERRIN RECEPTOR; TUMOR NECROSIS FACTOR; CYTOKINE; MICROSPHERE; PROTEOME;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; BIOSYNTHESIS; BONE MARROW DERIVED MACROPHAGE; CELL METABOLISM; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DENDRITIC CELL; DNA REPLICATION; ENDOCYTOSIS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; IMMUNE RESPONSE; INFLAMMATION; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; UPREGULATION; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CYTOLOGY; MACROPHAGE; METABOLISM; PHAGOCYTOSIS; TUMOR CELL LINE;

ANIMALS; BONE MARROW CELLS; CELL LINE, TUMOR; CYTOKINES; GLYCOLYSIS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MALE; MICE, INBRED C57BL; MICROSPHERES; PHAGOCYTOSIS; PROTEOME; PROTEOMICS;

EID: 84942866021     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.048744     Document Type: Article

References (51)

1. Gordon, S., and Taylor, P. R. (2005) Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964
2. Mosser, D. M., and Edwards, J. P. (2008) Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958-969
3. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35
4. Fleetwood, A. J., Cook, A. D., and Hamilton, J. A. (2005) Functions of granulocyte-macrophage colony-stimulating factor. Crit. Rev. Immunol. 25, 405-428
5. Hamilton, J. A. (2008) Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 8, 533-544
6. Fleetwood, A. J., Lawrence, T., Hamilton, J. A., and Cook, A. D. (2007) Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J. Immunol. 178, 5245-5252
7. Murray, P. J., Allen, J. E., Biswas, S. K., Fisher, E. A., Gilroy, D. W., Goerdt, S., Gordon, S., Hamilton, J. A., Ivashkiv, L. B., Lawrence, T., Locati, M., Mantovani, A., Martinez, F. O., Mege, J. L., Mosser, D. M., Natoli, G., Saeij, J. P., Schultze, J. L., Shirey, K. A., Sica, A., Suttles, J., Udalova, I., van Ginderachter, J. A., Vogel, S. N., and Wynn, T. A. (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14-20
8. Martinez, F. O., Gordon, S., Locati, M., and Mantovani, A. (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177, 7303-7311
9. McDermott, J. E., Archuleta, M., Thrall, B. D., Adkins, J. N., and Waters, K. M. (2011) Controlling the response: predictive modeling of a highly central, pathogen-targeted core response module in macrophage activation. PloS One 6, e14673
10. Nau, G. J., Richmond, J. F., Schlesinger, A., Jennings, E. G., Lander, E. S., and Young, R. A. (2002) Human macrophage activation programs induced by bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 99, 1503-1508
11. Ramsey, S. A., Klemm, S. L., Zak, D. E., Kennedy, K. A., Thorsson, V., Li, B., Gilchrist, M., Gold, E. S., Johnson, C. D., Litvak, V., Navarro, G., Roach, J. C., Rosenberger, C. M., Rust, A. G., Yudkovsky, N., Aderem, A., and Shmulevich, I. (2008) Uncovering a macrophage transcriptional program by integrating evidence from motif scanning and expression dynamics. PLoS Comput. Biol. 4, e1000021
12. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033
13. Raffaello, A. and Rizzuto, R. (2011) Mitochondrial longevity pathways. Biochim Biophys Acta. 1813, 260-268
14. Pearce, E. L., and Pearce, E. J. (2013) Metabolic pathways in immune cell activation and quiescence. Immunity 38, 633-643
15. Dayon, L., and Sanchez, J. C. (2012) Relative protein quantification by MS/MS using the tandem mass tag technology. Methods Mol. Biol. 893, 115-127
16. Na, Y. R., Yoon, Y. N., Son, D. I., and Seok, S. H. (2013) Cyclooxygenase-2 inhibition blocks M2 macrophage differentiation and suppresses metastasis in murine breast cancer model. PloS One 8, e63451
17. AM, V. O. s., Dominin, S. G., Kutepov, E. N., Leonov, A. V., Lobov, A. V., Maimulov, V. G., Nesvizhskii Iu, V., Semenova, V. V., Fokin, M. V., and Tselykovskaia, N. (2003) [Training physicians in medical prevention specialty: problems and prospects]. Gigiena i Sanitariia, 1, 13-15
18. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
19. Vizcaino, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Ríos, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P. A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H. J., Albar, J. P., Martinez-Bartolome, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223-226
20. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
21. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., Lin, J., Minguez, P., Bork, P., von Mering, C., and Jensen, L. J. (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-815
22. Scardoni, G., Petterlini, M., and Laudanna, C. (2009) Analyzing biological network parameters with CentiScaPe. Bioinformatics 25, 2857-2859
23. Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L., and Ideker, T. (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27, 431-432
24. Son, D., Na, Y. R., Hwang, E. S., and Seok, S. H. (2014) Platelet-derived growth factor-C (PDGF-C) induces anti-apoptotic effects on macrophages through Akt and Bad phosphorylation. J. Biol. Chem. 289, 6225-6235
25. Spolarics, Z., and Wu, J. X. (1997) Role of glutathione and catalase in H2O2 detoxification in LPS-activated hepatic endothelial and Kupffer cells. Am. J. Physiol. 273, G1304-1311
26. Gautier, E. L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K. G., Gordonov, S., Mazloom, A. R., Ma'ayan, A., Chua, W. J., Hansen, T. H., Turley, S. J., Merad, M., Randolph, G. J., and Immunological Genome, C. (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118-1128
27. Zizzo, G., Hilliard, B. A., Monestier, M., and Cohen, P. L. (2012) Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J. Immunol. 189, 3508-3520
28. Gnad, F., Gunawardena, J., and Mann, M. (2011) PHOSIDA 2011: the post-translational modification database. Nucleic Acids Res. 39, D253-260
29. Hornbeck, P. V., Kornhauser, J. M., Tkachev, S., Zhang, B., Skrzypek, E., Murray, B., Latham, V., and Sullivan, M. (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40, D261-270
30. Dinkel, H., Chica, C., Via, A., Gould, C. M., Jensen, L. J., Gibson, T. J., and Diella, F. (2011) Phospho.ELM: a database of phosphorylation sites-update 2011. Nucleic Acids Res. 39, D261-267
31. Imamura, K., Ogura, T., Kishimoto, A., Kaminishi, M., and Esumi, H. (2001) Cell cycle regulation via p53 phosphorylation by a 5-AMP activated protein kinase activator, 5-aminoimidazole-4-carboxamide-1-beta-Dribofuranoside, in a human hepatocellular carcinoma cell line. Biochem. Biophys. Res. Commun. 287, 562-567
32. Lokeshwar, B. L., and Lin, H. S. (1990) Growth factor-dependent regulation of transferrin receptor in proliferating and quiescent macrophages. Cell. Immunol. 130, 401-415
33. Rolfe, D. F., and Brown, G. C. (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758
34. Mazurek, S., and Eigenbrodt, E. (2003) The tumor metabolome. Anticancer Res. 23, 1149-1154
35. Becker, L., Liu, N. C., Averill, M. M., Yuan, W., Pamir, N., Peng, Y., Irwin, A. D., Fu, X., Bornfeldt, K. E., and Heinecke, J. W. (2012) Unique proteomic signatures distinguish macrophages and dendritic cells. PloS One 7, e33297
36. Cook, A. D., Pobjoy, J., Steidl, S., Dürr, M., Braine, E. L., Turner, A. L., Lacey, D. C., and Hamilton, J. A. (2012) Granulocyte-macrophage colony-stimulating factor is a key mediator in experimental osteoarthritis pain and disease development. Arthritis Res. Ther. 14, R199
37. O'Neill, L. A. (2014) Glycolytic reprogramming by TLRs in dendritic cells. Nat. Immunol. 15, 314-315
38. Everts, B., and Pearce, E. J. (2014) Metabolic control of dendritic cell activation and function: recent advances and clinical implications. Front. Immunol. 5, 203
39. Wang, H., Antinozzi, P. A., Hagenfeldt, K. A., Maechler, P., and Wollheim, C. B. (2000) Molecular targets of a human HNF1 alpha mutation responsible for pancreatic beta-cell dysfunction. EMBO J. 19, 4257-4264
40. Wolfrum, C., Shih, D. Q., Kuwajima, S., Norris, A. W., Kahn, C. R., and Stoffel, M. (2003) Role of Foxa-2 in adipocyte metabolism and differentiation. J. Clin. Invest. 112, 345-356
41. Kc, W., Satpathy, A. T., Rapaport, A. S., Briseño, C. G., Wu, X., Albring, J. C., Russler-Germain, E. V., Kretzer, N. M., Durai, V., Persaud, S. P., Edelson, B. T., Loschko, J., Cella, M., Allen, P. M., Nussenzweig, M. C., Colonna, M., Sleckman, B. P., Murphy, T. L., and Murphy, K. M. (2014) L-Myc expression by dendritic cells is required for optimal T-cell priming. Nature 507, 243-247
42. Gordan, J. D., Thompson, C. B., and Simon, M. C. (2007) HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 12, 108-113
43. Brissette, W. H., Baker, D. A., Stam, E. J., Umland, J. P., and Griffiths, R. J. (1995) GM-CSF rapidly primes mice for enhanced cytokine production in response to LPS and TNF. Cytokine 7, 291-295
44. Clendening, J. W., Pandyra, A., Boutros, P. C., El Ghamrasni, S., Khosravi, F., Trentin, G. A., Martirosyan, A., Hakem, A., Hakem, R., Jurisica, I., and Penn, L. Z. (2010) Dysregulation of the mevalonate pathway promotes transformation. Proc. Natl. Acad. Sci. U.S.A. 107, 15051-15056
45. Swanson, K. M., and Hohl, R. J. (2006) Anti-cancer therapy: targeting the mevalonate pathway. Curr. Cancer Drug Targets 6, 15-37
46. Feingold, K. R., Shigenaga, J. K., Kazemi, M. R., McDonald, C. M., Patzek, S. M., Cross, A. S., Moser, A., and Grunfeld, C. (2012) Mechanisms of triglyceride accumulation in activated macrophages. J. Leukocyte Biol. 92, 829-839
47. Ham, M., Lee, J. W., Choi, A. H., Jang, H., Choi, G., Park, J., Kozuka, C., Sears, D. D., Masuzaki, H., and Kim, J. B. (2013) Macrophage glucose-6-phosphate dehydrogenase stimulates proinflammatory responses with oxidative stress. Mol. Cell. Biol. 33, 2425-2435
48. Haschemi, A., Kosma, P., Gille, L., Evans, C. R., Burant, C. F., Starkl, P., Knapp, B., Haas, R., Schmid, J. A., Jandl, C., Amir, S., Lubec, G., Park, J., Esterbauer, H., Bilban, M., Brizuela, L., Pospisilik, J. A., Otterbein, L. E., and Wagner, O. (2012) The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism. Cell Metab. 15, 813-826
49. Vats, D., Mukundan, L., Odegaard, J. I., Zhang, L., Smith, K. L., Morel, C. R., Wagner, R. A., Greaves, D. R., Murray, P. J., and Chawla, A. (2006) Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 4, 13-24
50. Yoshida, S., Tsutsumi, S., Muhlebach, G., Sourbier, C., Lee, M. J., Lee, S., Vartholomaiou, E., Tatokoro, M., Beebe, K., Miyajima, N., Mohney, R. P., Chen, Y., Hasumi, H., Xu, W., Fukushima, H., Nakamura, K., Koga, F., Kihara, K., Trepel, J., Picard, D., and Neckers, L. (2013) Molecular chaperone TRAP1 regulates a metabolic switch between mitochondrial respiration and aerobic glycolysis. Proc. Natl. Acad. Sci. U.S.A. 110, E1604-1612
51. Freemerman, A. J., Johnson, A. R., Sacks, G. N., Milner, J. J., Kirk, E. L., Troester, M. A., Macintyre, A. N., Goraksha-Hicks, P., Rathmell, J. C., and Makowski, L. (2014) Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J. Biol. Chem. 289, 7884-7896