Drafting the proteome landscape of myeloid-derived suppressor cells

Proteomics

Volumn 16, Issue 2, 2016, Pages 367-378

  Gato, María ^a   Blanco Luquin, Idoia ^a   Zudaire, Maribel ^a   de Morentin, Xabier Martínez ^a   Perez Valderrama, Estela ^a   Zabaleta, Aintzane ^b   Kochan, Grazyna ^a   Escors, David ^a   Fernandez Irigoyen, Joaquín ^a   Santamaría, Enrique ^a  

^a Atención Primaria Y Promoción de La Salud   (Spain)

^b CIC BIOMAGUNE   (Spain)

Author keywords

Biomedicine; Mass spectrometry; Myeloid derived suppressor cell; Pathway; Proteomics

Indexed keywords

PROTEOME;

CANCER IMMUNOTHERAPY; CELL DIFFERENTIATION; CELL LINEAGE; HUMAN; MASS SPECTROMETRY; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEOMICS; REVIEW; SUPPRESSOR CELL; ANIMAL; BONE MARROW CELL; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; NEOPLASMS; TUMOR MICROENVIRONMENT;

ANIMALS; HUMANS; IMMUNOTHERAPY; MYELOID CELLS; NEOPLASMS; PROTEOME; PROTEOMICS; TUMOR MICROENVIRONMENT;

EID: 84956596864     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201500229     Document Type: Review

References (96)

1. Young, M. R., Newby, M., Wepsic, H. T., Hematopoiesis and suppressor bone marrow cells in mice bearing large metastatic Lewis lung carcinoma tumors. Cancer Res. 1987, 47, 100-105.
2. Bennett, J. A., Rao, V. S., Mitchell, M. S., Systemic bacillus Calmette-Guerin (BCG) activates natural suppressor cells. Proc. Natl. Acad. Sci. USA 1978, 75, 5142-5144.
3. Sinha, P., Clements, V. K., Bunt, S. K., Albelda, S. M., Ostrand-Rosenberg, S., Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol. 2007, 179, 977-983.
4. Yang, L., DeBusk, L. M., Fukuda, K., Fingleton, B. et al., Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004, 6, 409-421.
5. Talmadge, J. E., Pathways mediating the expansion and immunosuppressive activity of myeloid-derived suppressor cells and their relevance to cancer therapy. Clin. Cancer Res. 2007, 13, 5243-5248.
6. Gabrilovich, D. I., Ostrand-Rosenberg, S., Bronte, V., Coordinated regulation of myeloid cells by tumors. Nat. Rev. Immunol. 2012, 12, 253-268.
7. Movahedi, K., Guilliams, M., Van den Bossche, J., Van den Bergh, R. et al., Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008, 111, 4233-4244.
8. Youn, J. I., Nagaraj, S., Collazo, M., Gabrilovich, D. I., Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 2008, 181, 5791-5802.
9. Mandruzzato, S., Solito, S., Falisi, E., Francescato, S. et al., IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 2009, 182, 6562-6568.
10. Vuk-Pavlovic, S., Bulur, P. A., Lin, Y., Qin, R. et al., Immunosuppressive CD14+HLA-DRlow/- monocytes in prostate cancer. Prostate 2010, 70, 443-455.
11. Damuzzo, V., Pinton, L., Desantis, G., Solito, S. et al., Complexity and challenges in defining myeloid-derived suppressor cells. Cytometry B Clin. Cytom. 2015, 88, 77-91.
12. Liechtenstein, T., Perez-Janices, N., Gato, M., Caliendo, F. et al., A highly efficient tumor-infiltrating MDSC differentiation system for discovery of anti-neoplastic targets, which circumvents the need for tumor establishment in mice. Oncotarget 2014, 5, 7843-7857.
13. Kodumudi, K. N., Woan, K., Gilvary, D. L., Sahakian, E. et al., A novel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers. Clin. Cancer Res. 2010, 16, 4583-4594.
14. Vincent, J., Mignot, G., Chalmin, F., Ladoire, S. et al., 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 2010, 70, 3052-3061.
15. Alizadeh, D., Trad, M., Hanke, N. T., Larmonier, C. B. et al., Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer. Cancer Res. 74, 104-118.
16. Maenhout, S. K., Thielemans, K., Aerts, J. L., Location, location, location: functional and phenotypic heterogeneity between tumor-infiltrating and non-infiltrating myeloid-derived suppressor cells. Oncoimmunology 2014, 3, e956579.
17. Solito, S., Marigo, I., Pinton, L., Damuzzo, V. et al., Myeloid-derived suppressor cell heterogeneity in human cancers. Ann. NY Acad. Sci. 2014, 1319, 47-65.
18. Escors, D., Liechtenstein, T., Perez-Janices, N., Schwarze, J. et al., Assessing T-cell responses in anticancer immunohterapy: dendritic cells or myeloid-derived suppressor cells? Oncoimmunology 2013, 12, e26148.
19. Alizadeh, D., Larmonier, N., Chemotherapeutic targeting of cancer-induced immunosuppressive cells. Cancer Res. 2014, 74, 2663-2668.
20. Trikha, P., Carson, W. E., 3rd, signaling pathways involved in MDSC regulation. Biochim. Biophys. Acta 2014, 1846, 55-65.
21. Condamine, T., Gabrilovich, D. I., Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 2011, 32, 19-25.
22. Gabrilovich, D. I., Nagaraj, S., Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9, 162-174.
23. Condamine, T., Kumar, V., Ramachandran, I. R., Youn, J. I. et al., ER stress regulates myeloid-derived suppressor cell fate through TRAIL-R-mediated apoptosis. J. Clin. Invest. 2014, 124, 2626-2639.
24. Corzo, C. A., Condamine, T., Lu, L., Cotter, M. J. et al., HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 2010, 207, 2439-2453.
25. Maenhout, S. K., Van Lint, S., Emeagi, P. U., Thielemans, K., Aerts, J. L., Enhanced suppressive capacity of tumor-infiltrating myeloid-derived suppressor cells compared to their peripheral counterparts. Int. J. Cancer 2013, 134, 1077-1090.
26. Lutz, M. B., Kukutsch, N. A., Menges, M., Rossner, S., Schuler, G., Culture of bone marrow cells in GM-CSF plus high doses of lipopolysaccharide generates exclusively immature dendritic cells which induce alloantigen-specific CD4 T cell anergy in vitro. Eur. J. Immunol. 2000, 30, 1048-1052.
27. Morales, J. K., Kmieciak, M., Knutson, K. L., Bear, H. D., Manjili, M. H., GM-CSF is one of the main breast tumor-derived soluble factors involved in the differentiation of CD11b-Gr1- bone marrow progenitor cells into myeloid-derived suppressor cells. Breast Cancer Res. Treatment 2010, 123, 39-49.
28. Dolcetti, L., Peranzoni, E., Ugel, S., Marigo, I. et al., Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur. J. Immunol. 2010, 40, 22-35.
29. Marigo, I., Bosio, E., Solito, S., Mesa, C. et al., Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 2010, 32, 790-802.
30. Lechner, M. G., Liebertz, D. J., Epstein, A. L., Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J. Immunol. 2010, 185, 2273-2284.
31. Highfill, S. L., Rodriguez, P. C., Zhou, Q., Goetz, C. A. et al., Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13. Blood 2010, 116, 5738-5747.
32. Xiang, X., Poliakov, A., Liu, C., Liu, Y. et al., Induction of myeloid-derived suppressor cells by tumor exosomes. Int. J. Cancer 2009, 124, 2621-2633.
33. Valenti, R., Huber, V., Filipazzi, P., Pilla, L. et al., Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res. 2006, 66, 9290-9298.
34. Obermajer, N., Muthuswamy, R., Lesnock, J., Edwards, R. P., Kalinski, P., Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells. Blood 2013, 118, 5498-5505.
35. Apolloni, E., Bronte, V., Mazzoni, A., Serafini, P. et al., Immortalized myeloid suppressor cells trigger apoptosis in antigen-activated T lymphocytes. J. Immunol. 2000, 165, 6723-6730.
36. Zhou, Z., French, D. L., Ma, G., Eisenstein, S. et al., Development and function of myeloid-derived suppressor cells generated from mouse embryonic and hematopoietic stem cells. Stem Cells (Dayton, Ohio) 2010, 28, 620-632.
37. Ding, X., Wu, L., Yan, C., Du, H., Establishment of lal-/- myeloid lineage cell line that resembles myeloid-derived suppressive cells. PLoS ONE 2015, 10, e0121001.
38. Breckpot, K., Escors, D., Dendritic cells for active anti-cancer immunotherapy: targeting activation pathways through genetic modification. Endocrine, Metabolic & Immune Disorders Drug Targets 2009, 9, 328-343.
39. Arce, F., Kochan, G., Breckpot, K., Stephenson, H., Escors, D., Selective activation of intracellular signalling pathways in dendritic cells for cancer immunotherapy. Anti-cancer Agents Medicinal Chemistry 2012, 1, 29-39.
40. Liechtenstein, T., Perez-Janices, N., Blanco-Luquin, I., Schwarze, J. et al., Anti-melanoma vaccines engineered to simultaneously modulate cytokine priming and silence PD-L1 characterized using ex vivo myeloid-derived suppressor cells as a readout of therapeutic efficacy. Oncoimmunology 2014, 3, e29178.
41. Dufait, I., Schwarze, J. K., Liechtenstein, T., Leonard, W. et al., Ex vivo generation of myeloid-derived suppressor cells that model the tumor immunosuppressive environment in colorectal cancer, Oncotarget 2015, 6, 12369-12382.
42. Van der Jeught, K., Joe, P. T., Bialkowski, L., Heirman, C. et al., Intratumoral administration of mRNA encoding a fusokine consisting of IFN-beta and the ectodomain of the TGF-beta receptor II potentiates antitumor immunity. Oncotarget 2014, 5, 10100-10113.
43. Meissner, F., Mann, M., Quantitative shotgun proteomics: considerations for a high-quality workflow in immunology. Nat. Immunol. 2014, 15, 112-117.
44. Tannu, N. S., Hemby, S. E., Two-dimensional fluorescence difference gel electrophoresis for comparative proteomics profiling. Nat. Protoc. 2006, 1, 1732-1742.
45. Boutte, A. M., Friedman, D. B., Bogyo, M., Min, Y. et al., Identification of a myeloid-derived suppressor cell cystatin-like protein that inhibits metastasis. FASEB J. 2011, 25, 2626-2637.
46. Boutte, A. M., McDonald, W. H., Shyr, Y., Yang, L., Lin, P. C., Characterization of the MDSC proteome associated with metastatic murine mammary tumors using label-free mass spectrometry and shotgun proteomics. PLoS ONE 2011, 6, e22446.
47. Schroder, P. C., Fernandez-Irigoyen, J., Bigaud, E., Serna, A. et al., Proteomic analysis of human hepatoma cells expressing methionine adenosyltransferase I/III: Characterization of DDX3X as a target of S-adenosylmethionine. J. Proteomics 2012, 75, 2855-2868.
48. Wolters, D. A., Washburn, M. P., Yates, J. R., 3rd, An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 2001, 73, 5683-5690.
49. Neilson, K. A., Ali, N. A., Muralidharan, S., Mirzaei, M. et al., Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 2011, 11, 535-553.
50. Filiou, M. D., Martins-de-Souza, D., Guest, P. C., Bahn, S., Turck, C. W., To label or not to label: applications of quantitative proteomics in neuroscience research. Proteomics 2012, 12, 736-747.
51. Chornoguz, O., Grmai, L., Sinha, P., Artemenko, K. A. et al., Proteomic pathway analysis reveals inflammation increases myeloid-derived suppressor cell resistance to apoptosis. Mol. Cell Proteomics 2011, 10, M110 002980.
52. Iero, M., Valenti, R., Huber, V., Filipazzi, P. et al., Tumor-released exosomes and their implications in cancer immunity. Cell Death Differentiation 2008, 15, 80-88.
53. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M. et al., Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9, 654-659.
54. Geis-Asteggiante, L., Dhabaria, A., Edwards, N., Ostrand-Rosenberg, S., Fenselau, C., Top-down analysis of low mass proteins in exosomes shed by murine myeloid-derived suppressor cells. Int. J. Mass Spectrom. 2015, 378, 264-269.
55. Burke, M., Choksawangkarn, W., Edwards, N., Ostrand-Rosenberg, S., Fenselau, C., Exosomes from myeloid-derived suppressor cells carry biologically active proteins. J. Proteome Res. 2014, 13, 836-843.
56. Piper, R. C., Lehner, P. J., Endosomal transport via ubiquitination. Trends Cell Biol. 2011, 21, 647-655.
57. Tanno, H., Komada, M., The ubiquitin code and its decoding machinery in the endocytic pathway. J. Biochem. 2013, 153, 497-504.
58. Burke, M. C., Oei, M. S., Edwards, N. J., Ostrand-Rosenberg, S., Fenselau, C., Ubiquitinated proteins in exosomes secreted by myeloid-derived suppressor cells. J. Proteome Res. 2014, 13, 5965-5972.
59. Villarroya-Beltri, C., Baixauli, F., Gutierrez-Vazquez, C., Sanchez-Madrid, F., Mittelbrunn, M., Sorting it out: regulation of exosome loading. Seminars Cancer Biol. 2014, 28, 3-13.
60. Unwin, R. D., Griffiths, J. R., Whetton, A. D., Simultaneous analysis of relative protein expression levels across multiple samples using iTRAQ isobaric tags with 2D nano LC-MS/MS. Nat. Protoc. 2010, 5, 1574-1582.
61. Mudunuri, U., Che, A., Yi, M., Stephens, R. M., bioDBnet: the biological database network. Bioinformatics 2009, 25, 555-556.
62. Bochmann, I., Ebstein, F., Lehmann, A., Wohlschlaeger, J. et al., T lymphocytes export proteasomes by way of microparticles: a possible mechanism for generation of extracellular proteasomes. J. Cell. Mol. Med. 2013, 18, 59-68.
63. Zanker, D., Otto, W., Chen, W., von Bergen, M., Tomm, J. M., Compartment resolved reference proteome map from highly purified naive, activated, effector, and memory CD8 murine immune cells. Proteomics 2015, 15, 1808-1812.
64. Gupta, N., Wollscheid, B., Watts, J. D., Scheer, B. et al., Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat. Immunol. 2006, 7, 625-633.
65. Brown, K. J., Formolo, C. A., Seol, H., Marathi, R. L. et al., Advances in the proteomic investigation of the cell secretome. Expert Rev. Proteomics 2012, 9, 337-345.
66. Mukherjee, P., Mani, S., Methodologies to decipher the cell secretome. Biochim. Biophys. Acta 2013, 1834, 2226-2232.
67. Groessl, M., Luksch, H., Rosen-Wolff, A., Shevchenko, A., Gentzel, M., Profiling of the human monocytic cell secretome by quantitative label-free mass spectrometry identifies stimulus-specific cytokines and proinflammatory proteins. Proteomics 2012, 12, 2833-2842.
68. Meissner, F., Scheltema, R. A., Mollenkopf, H. J., Mann, M., Direct proteomic quantification of the secretome of activated immune cells. Science 2013, 340, 475-478.
69. Obenauf, A. C., Zou, Y., Ji, A. L., Vanharanta, S. et al., Therapy-induced tumor secretomes promote resistance and tumor progression. Nature 2015, 520, 368-372.
70. Hennrich, M. L., Gavin, A. C., Quantitative mass spectrometry of posttranslational modifications: keys to confidence. Sci. Signal. 2015, 8, re5.
71. Kamath, K. S., Vasavada, M. S., Srivastava, S., Proteomic databases and tools to decipher post-translational modifications. J. Proteomics 2011, 75, 127-144.
72. Olsen, J. V., Mann, M., Status of large-scale analysis of post-translational modifications by mass spectrometry. Mol. Cell Proteomics 2013, 12, 3444-3452.
73. Junger, M. A., Aebersold, R., Mass spectrometry-driven phosphoproteomics: patterning the systems biology mosaic. Wiley Interdiscip. Rev. Dev. Biol. 2014, 3, 83-112.
74. Morris, M. K., Chi, A., Melas, I. N., Alexopoulos, L. G., Phosphoproteomics in drug discovery. Drug Discovery Today 2014, 19, 425-432.
75. Sylvestersen, K. B., Young, C., Nielsen, M. L., Advances in characterizing ubiquitylation sites by mass spectrometry. Curr. Opin. Chem. Biol. 2013, 17, 49-58.
76. Pan, S., Chen, R., Aebersold, R., Brentnall, T. A., Mass spectrometry based glycoproteomics-from a proteomics perspective. Mol. Cell Proteomics 2011, 10, R110 003251.
77. Choudhary, C., Weinert, B. T., Nishida, Y., Verdin, E., Mann, M., The growing landscape of lysine acetylation links metabolism and cell signalling. Nat. Rev. Mol. Cell Biol. 2014, 15, 536-550.
78. Andersen, J. S., Matic, I., Vertegaal, A. C., Identification of SUMO target proteins by quantitative proteomics. Methods Mol. Biol. 2009, 497, 19-31.
79. Thinon, E., Serwa, R. A., Broncel, M., Brannigan, J. A. et al., Global profiling of co- and post-translationally N-myristoylated proteomes in human cells. Nat. Commun. 2014, 5, 4919.
80. Raju, K., Doulias, P. T., Tenopoulou, M., Greene, J. L., Ischiropoulos, H., Strategies and tools to explore protein S-nitrosylation. Biochim. Biophys. Acta 2012, 1820, 684-688.
81. Gajadhar, A. S., White, F. M., System level dynamics of post-translational modifications. Curr. Opin. Biotechnol. 2014, 28, 83-87.
82. Gingras, A. C., Gstaiger, M., Raught, B., Aebersold, R., Analysis of protein complexes using mass spectrometry. Nat. Rev. Mol. Cell Biol. 2007, 8, 645-654.
83. Lambert, J. P., Ivosev, G., Couzens, A. L., Larsen, B. et al., Mapping differential interactomes by affinity purification coupled with data-independent mass spectrometry acquisition. Nat. Meth. 2013, 10, 1239-1245.
84. Li, S., Wang, L., Berman, M., Kong, Y. Y., Dorf, M. E., Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 2011, 35, 426-440.
85. Gato, M., Martinez de Morentin, X., Blanco-Luquin, I., Fernandez-Irigoyen, J. et al., A core of kinase-regulated interactomes defines the neoplastic MDSC lineage. Oncotarget 2015, DOI: 10.18632/oncotarget.4746.
86. Osen, W., Soltek, S., Song, M., Leuchs, B. et al., Screening of human tumor antigens for CD4 T cell epitopes by combination of HLA-transgenic mice, recombinant adenovirus and antigen peptide libraries. PLoS ONE 2010, 5, e14137.
87. Van den Eynde, B. J., van der Bruggen, P., T cell defined tumor antigens. Curr. Opin. Immunol. 1997, 9, 684-693.
88. Sengupta, N., MacFie, T. S., MacDonald, T. T., Pennington, D., Silver, A. R., Cancer immunoediting and "spontaneous" tumor regression. Pathol. Res. Pract. 2010, 206, 1-8.
89. Escors, D., Tumor immunogenicity, antigen presentation and immunological barriers in cancer immunotherapy. New J. Sci. 2014, 2014, pii734515.
90. Karwacz, K., Arce, F., Bricogne, C., Kochan, G., Escors, D., PD-L1 co-stimulation, ligand-induced TCR down-modulation and anti-tumor immunotherapy. Oncoimmunology 2012, 1, 86-88.
91. Wolchok, J. D., Hodi, F. S., Weber, J. S., Allison, J. P. et al., Development of ipilimumab: a novel immunotherapeutic approach for the treatment of advanced melanoma. Ann. NY Acad. Sci. 2013, 1291, 1-13.
92. Brahmer, J. R., Tykodi, S. S., Chow, L. Q., Hwu, W. J. et al., Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 2012, 366, 2455-2465.
93. Topalian, S. L., Hodi, F. S., Brahmer, J. R., Gettinger, S. N. et al., Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 2012, 366, 2443-2454.
94. Onizuka, S., Tawara, I., Shimizu, J., Sakaguchi, S. et al., Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res. 1999, 59, 3128-3133.
95. Talmadge, J. E., Gabrilovich, D. I., History of myeloid-derived suppressor cells. Nat. Rev. 2013, 13, 739-752.
96. Aliper, A. M., Frieden-Korovkina, V. P., Buzdin, A., Roumiantsev, S. A., Zhavoronkov, A., Interactome analysis of myeloid-derived suppressor cells in murine models of colon and breast cancer. Oncotarget 2014, 5, 11345-11353.