Cancer cell-derived exosomes induce mitogen-activated protein kinase-dependent monocyte survival by transport of functional receptor tyrosine kinases

Journal of Biological Chemistry

Volumn 291, Issue 16, 2016, Pages 8453-8464

  Song, Xiao ^a   Ding, Yanping ^a   Liu, Gang ^a   Yang, Xiao ^a,b   Zhao, Ruifang ^a   Zhang, Yinlong ^a,b   Zhao, Xiao ^a,c   Anderson, Gregory J ^d,e,f   Nie, Guangjun ^a  

^a NATIONAL CENTER FOR NANOSCIENCE AND TECHNOLOGY   (China)

^b JILIN UNIVERSITY   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^e NATIONAL HEALTH AND MEDICAL RESEARCH COUNCIL   (Australia)

^f INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BODY FLUIDS; CELL DEATH; CHEMICAL ACTIVATION; CYTOLOGY; DISEASES; ENZYME ACTIVITY; ENZYMES; PHOSPHORYLATION; PROTEINS; TUMORS;

EPIDERMAL GROWTH FACTOR RECEPTORS; EXTRACELLULAR SIGNAL-REGULATED KINASE; FUNCTIONAL RECEPTORS; HUMAN EPIDERMAL GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHORYLATED RECEPTORS; TUMOR ASSOCIATED MACROPHAGES; TUMOR MICROENVIRONMENT;

CELLS;

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; CASPASE; EGFR PROTEIN, HUMAN; ERBB2 PROTEIN, HUMAN;

ANALYSIS OF VARIANCE; APOPTOSIS; ARTICLE; CANCER CELL; CELL COUNTING; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CELL VIABILITY; CENTRIFUGATION; CONTROLLED STUDY; DENSITOMETRY; ENZYME ACTIVATION; ENZYME INACTIVATION; EXOSOME; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENETIC TRANSFECTION; HOMEOSTASIS; HUMAN; HUMAN CELL; LIFESPAN; MONOCYTE; PLASMID; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR MICROENVIRONMENT; GENETICS; HEP-G2 CELL LINE; MCF-7 CELL LINE; METABOLISM; NEOPLASM;

APOPTOSIS; CASPASES; CELL SURVIVAL; EXOSOMES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEP G2 CELLS; HUMANS; MCF-7 CELLS; MONOCYTES; NEOPLASMS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2;

EID: 84964923714     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.716316     Document Type: Article

References (49)

1. Mantovani, A., Schioppa, T., Porta, C., Allavena, P., and Sica, A. (2006) Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 25, 315-322
2. Solinas, G., Germano, G., Mantovani, A., and Allavena, P. (2009) Tumorassociated macrophages (TAM) as major players of the cancer-related inflammation. J. Leukocyte Biol. 86, 1065-1073
3. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., and Sica, A. (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549-555
4. Musson, R. A., Shafran, H., and Henson, P. M. (1980) Intracellular levels and stimulated release of lysosomal enzymes from human peripheral blood monocytes and monocyte-derived macrophages. J. Reticuloendothel. Soc. 28, 249-264
5. Fahy, R. J., Doseff, A. I., and Wewers, M. D. (1999) Spontaneous human monocyte apoptosis utilizes a caspase-3-dependent pathway that is blocked by endotoxin and is independent of caspase-1. J. Immunol. 163, 1755-1762
6. Tsakalos, N. D., Lachman, L. B., Newhouse, Y. G., and Whisler, R. L. (1984) Lipopolysaccharide (LPS) modulation of human monocyte accessory cell function in promoting T-cell colonies: inability of LPS and IL-1 to abrogate the need for monocytes with high HLA-DR expression. Cell. Immunol. 83, 229-241
7. Musson, R. A. (1983) Human serum induces maturation of human monocytes in vitro: changes in cytolytic activity, intracellular lysosomal enzymes, and nonspecific esterase activity. Am. J. Pathol. 111, 331-340
8. Becker, S., Warren, M. K., and Haskill, S. (1987) Colony-stimulating factor-induced monocyte survival and differentiation into macrophages in serum-free cultures. J. Immunol. 139, 3703-3709
9. Warren, M. K., and Ralph, P. (1986) Macrophage growth factor CSF-1 stimulates human monocyte production of interferon, tumor necrosis factor, and colony stimulating activity. J. Immunol. 137, 2281-2285
10. Mangan, D. F., Welch, G. R., and Wahl, S. M. (1991) Lipopolysaccharide, tumor necrosis factor-α, and IL-1 β prevent programmed cell death (apoptosis) in human peripheral blood monocytes. J. Immunol. 146, 1541-1546
11. Henson, P. M., and Hume, D. A. (2006) Apoptotic cell removal in development and tissue homeostasis. Trends Immunol. 27, 244-250
12. Mangan, D. F., Robertson, B., and Wahl, S. M. (1992) IL-4 enhances programmed cell death (apoptosis) in stimulated human monocytes. J. Immunol. 148, 1812-1816
13. Whiteside, T. L. (2002) Apoptosis of immune cells in the tumor microenvironment and peripheral circulation of patients with cancer: implications for immunotherapy. Vaccine 20, A46-A51
14. Hazlehurst, L. A., Landowski, T. H., and Dalton, W. S. (2003) Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death. Oncogene 22, 7396-7402
15. Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S. D., Ntzouni, M., Margaritis, L. H., Stefanis, L., and Vekrellis, K. (2010) Cellproduced β-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 30, 6838-6851
16. Ohshima, K., Inoue, K., Fujiwara, A., Hatakeyama, K., Kanto, K., Watanabe, Y., Muramatsu, K., Fukuda, Y., Ogura, S., Yamaguchi, K., and Mochizuki, T. (2010) Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS ONE 5, e13247
17. Kostelansky, M. S., Schluter, C., Tam, Y. Y., Lee, S., Ghirlando, R., Beach, B., Conibear, E., and Hurley, J. H. (2007) Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129, 485-498
18. Wollert, T., Wunder, C., Lippincott-Schwartz, J., and Hurley, J. H. (2009) Membrane scission by the ESCRT-III complex. Nature 458, 172-177
19. Simons, M., and Raposo, G. (2009) Exosomes: vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581
20. Weiss, G., Bogdan, C., and Hentze, M. W. (1997) Pathways for the regulation of macrophage iron metabolism by the anti-inflammatory cytokines IL-4 and IL-13. J. Immunol. 158, 420-425
21. Pink, J. J., Jiang, S.-Y., Fritsch, M., and Jordan, V. C. (1995) An estrogenindependent MCF-7 breast cancer cell line which contains a novel 80-kilodalton estrogen receptor-related protein. Cancer Res. 55, 2583-2590
22. Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., and Zhang, F. (2013) Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308
23. Li, H., Zhu, H., Xu, C. J., and Yuan, J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501
24. Haile, S., Estevez, A. M., and Clayton, C. (2003) A role for the exosome in the in vivo degradation of unstable mRNAs. RNA 9, 1491-1501
25. Ostrowski, M., Carmo, N. B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., Moita, C. F., Schauer, K., Hume, A. N., Freitas, R. P., Goud, B., Benaroch, P., Hacohen, N., Fukuda, M., Densnos, C., et al. (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12, 19-30
26. Pegtel, D. M., Cosmopoulos, K., Thorley-Lawson, D. A., van Eijndhoven, M. A., Hopmans, E. S., Lindenberg, J. L., de Gruijl, T. D., Würdinger, T., and Middeldorp, J. M. (2010) Functional delivery of viral miRNAs via exosomes. Proc. Natl. Acad. Sci. U.S.A. 107, 6328-6333
27. Goyal, A., Wang, Y., Graham, M. M., Doseff, A. I., Bhatt, N. Y., and Marsh, C. B. (2002) Monocyte survival factors induce Akt activation and suppress caspase-3. Am. J. Respir. Cell Mol. Biol. 26, 224-230
28. Kelley, T. W., Graham, M. M., Doseff, A. I., Pomerantz, R. W., Lau, S. M., Ostrowski, M. C., Franke, T. F., and Marsh, C. B. (1999) Macrophage colony-stimulating factor promotes cell survival through Akt/protein kinase B. J. Biol. Chem. 274, 26393-26398
29. Kang, I., Yoon, D. W., Braun, K. R., and Wight, T. N. (2014) Expression of versican V3 by arterial smooth muscle cells alters tumor growth factor α (TGFβ)-, epidermal growth factor (EGF)-, and nuclear factor κB (NFκB)-dependent signaling pathways, creating a microenvironment that resists monocyte adhesion. J. Biol. Chem. 289, 15393-15404
30. Dondi, E., Pattyn, E., Lutfalla, G., Van Ostade, X., Uzé, G., Pellegrini, S., and Tavernier, J. (2001) Down-modulation of type 1 interferon responses by receptor cross-competition for a shared Jak kinase. J. Biol. Chem. 276, 47004-47012
31. Scherle, P. A., Jones, E. A., Favata, M. F., Daulerio, A. J., Covington, M. B., Nurnberg, S. A., Magolda, R. L., and Trzaskos, J. M. (1998) Inhibition of MAP kinase kinase prevents cytokine and prostaglandin E2 production in lipopolysaccharide-stimulated monocytes. J. Immunol. 161, 5681-5686
32. Tran, S. E., Holmstrom, T. H., Ahonen, M., Kahari, V.-M., and Eriksson, J. E. (2001) MAPK/ERK overrides the apoptotic signaling from Fas, TNF, and TRAIL receptors. J. Biol. Chem. 276, 16484-16490
33. Anido, J., Matar, P., Albanell, J., Guzmán, M., Rojo, F., Arribas, J., Averbuch, S., and Baselga, J. (2003) ZD1839, a specific epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor, induces the formation of inactive EGFR/HER2 and EGFR/HER3 heterodimers and prevents heregulin signaling in HER2-overexpressing breast cancer cells. Clin. Cancer Res. 9, 1274-1283
34. Mantovani, A., Sica, A., and Locati, M. (2005) Macrophage polarization comes of age. Immunity 23, 344-346
35. Gordon, S., and Taylor, P. R. (2005) Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964
36. Staubach, S., Razawi, H., and Hanisch, F. G. (2009) Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 9, 2820-2835
37. King, H. W., Michael, M. Z., and Gleadle, J. M. (2012) Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 12, 421
38. Heidenreich, S., Schmidt, M., August, C., Cullen, P., Rademaekers, A., and Pauels, H.-G. (1997) Regulation of human monocyte apoptosis by the CD14 molecule. J. Immunol. 159, 3178-3188
39. Burysek, L., Syrovets, T., and Simmet, T. (2002) The serine protease plasmin triggers expression of MCP-1 and CD40 in human primary monocytes via activation of p38 MAPK and Janus kinase (JAK)/STAT signaling pathways. J. Biol. Chem. 277, 33509-33517
40. Najib, S., and Sánchez-Margalet, V. (2002) Human leptin promotes survival of human circulating blood monocytes prone to apoptosis by activation of p42/44 MAPK pathway. Cell. Immunol. 220, 143-149
41. Goodsell, D. S. (1999) The molecular perspective: the ras oncogene. Oncologist 4, 263-264
42. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J., and Carbone, F. R. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27
43. Twaddle, G. M., Turbov, J., Liu, N., and Murthy, S. (1999) Tyrosine kinase inhibitors as antiproliferative agents against an estrogen-dependent breast cancer cell line in vitro. J. Surg. Oncol. 70, 83-90
44. Endres, N. F., Das, R., Smith, A. W., Arkhipov, A., Kovacs, E., Huang, Y., Pelton, J. G., Shan, Y., Shaw, D. E., Wemmer, D. E., Groves, J. T., and Kuriyan, J. (2013) Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 152, 543-556
45. Nagy, P., Claus, J., Jovin, T. M., and Arndt-Jovin, D. J. (2010) Distribution of resting and ligand-bound ErbB1 and ErbB2 receptor tyrosine kinases in living cells using number and brightness analysis. Proc. Natl. Acad. Sci. U.S.A. 107, 16524-16529
46. Akers, J. C., Gonda, D., Kim, R., Carter, B. S., and Chen, C. C. (2013) Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J. Neurooncol. 113, 1-11
47. Spector, N. L., Xia, W., Burris, H., 3rd, Hurwitz, H., Dees, E. C., Dowlati, A., O'Neil, B., Overmoyer, B., Marcom, P. K., Blackwell, K. L., Smith, D. A., Koch, K. M., Stead, A., Mangum, S., Ellis, M. J., et al. (2005) Study of the biologic effects of lapatinib, a reversible inhibitor of ErbB1 and ErbB2 tyrosine kinases, on tumor growth and survival pathways in patients with advanced malignancies. J. Clin. Oncol. 23, 2502-2512
48. Johnston, S. R., and Leary, A. (2006) Lapatinib: a novel EGFR/HER2 tyrosine kinase inhibitor for cancer. Drugs Today 42, 441-453
49. Spivak-Kroizman, T., Rotin, D., Pinchasi, D., Ullrich, A., Schlessinger, J., and Lax, I. (1992) Heterodimerization of c-erbB2 with different epidermal growth factor receptor mutants elicits stimulatory or inhibitory responses. J. Biol. Chem. 267, 8056-8063