Triggering receptor expressed on myeloid cells 1 (TREM-1)- Mediated Bcl-2 induction prolongs macrophage survival

Journal of Biological Chemistry

Volumn 289, Issue 21, 2014, Pages 15118-15129

  Yuan, Zhihong ^a,b   Syed, Mansoor Ali ^c   Panchal, Dipti ^c   Joo, Myungsoo ^d   Colonna, Marco ^e   Brantly, Mark ^b   Sadikot, Ruxana T ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d Department of Immunology Pusan University ^*  (South Korea)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PATHOLOGY;

ANTI-APOPTOTIC PROTEIN; INFLAMMATORY CELLS; MYELOID CELLS;

MACROPHAGES;

CASPASE 3; EARLY GROWTH RESPONSE FACTOR 2; MITOFUSIN 1; MITOFUSIN 2; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION;

CELL DEATH; INFLAMMATION; LIPOPOLYSACCHARIDE (LPS); MACROPHAGE; MACROPHAGES; TUMOR;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CASPASE 3; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; EARLY GROWTH RESPONSE PROTEIN 2; ENZYME INHIBITORS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; MACROPHAGES; MAP KINASE KINASE 1; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, IMMUNOLOGIC; RNA INTERFERENCE;

EID: 84901406054     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.536490     Document Type: Article

References (70)

1. Cohen, H. B., and Mosser, D. M. (2013) Extrinsic and intrinsic control of macrophage inflammatory responses. J. Leukocyte Biol. 94, 913-919
2. Byrne, A. J., Jones, C. P., Gowers, K., Rankin, S. M., and Lloyd, C. M. (2013) Lung macrophages contribute to house dust mite driven airway remodeling via HIF-1 α. PLoS One 8, e69246
3. Wynn, T. A., Chawla, A., and Pollard, J. W. (2013) Macrophage biology in development, homeostasis and disease. Nature 496, 445-455
4. Galdiero, M. R., Bonavita, E., Barajon, I., Garlanda, C., Mantovani, A., and Jaillon, S. (2013) Tumor associated macrophages and neutrophils in cancer. Immunobiology 218, 1402-1410
5. Galdiero, M. R., Garlanda, C., Jaillon, S., Marone, G., and Mantovani, A. (2013) Tumor associated macrophages and neutrophils in tumor progression. J. Cell Physiol. 228, 1404-1412
6. Gordon, S., and Taylor, P. R. (2005) Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964 (Pubitemid 41746764)
7. Mantovani, A., Biswas, S. K., Galdiero, M. R., Sica, A., and Locati, M. (2013) Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 229, 176-185
8. Lichtnekert, J., Kawakami, T., Parks, W. C., and Duffield, J. S. (2013) Changes in macrophage phenotype as the immune response evolves. Curr. Opin. Pharmacol. 13, 555-564
9. Byers, D. E., and Holtzman, M. J. (2011) Alternatively activated macrophages and airway disease. Chest 140, 768-774
10. Fullerton, J. N., O'Brien, A. J., and Gilroy, D. W. (2013) Pathways mediating resolution of inflammation: when enough is too much. J. Pathol. 231, 8-20
11. Bouchon, A., Dietrich, J., and Colonna, M. (2000) Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J. Immunol. 164, 4991-4995 (Pubitemid 30305166)
12. Bouchon, A., Facchetti, F., Weigand, M. A., and Colonna, M. (2001) TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 410, 1103-1107 (Pubitemid 32391042)
13. Gibot, S., Kolopp-Sarda, M. N., Béné, M. C., Bollaert, P. E., Lozniewski, A., Mory, F., Levy, B., and Faure, G. C. (2004) A soluble form of the triggering receptor expressed on myeloid cells-1 modulates the inflammatory response in murine sepsis. J. Exp. Med. 200, 1419-1426 (Pubitemid 39657289)
14. Yuan, Z., Syed, M. A., Panchal, D., Rogers, D., Joo, M., and Sadikot, R. T. (2012) Curcumin-mediated epigenetic modulation inhibits TREM-1 expression in response to lipopolysaccharide. Int. J. Biochem. Cell Biol. 44, 2032-2043
15. Zeng, H., Ornatowska, M., Joo, M. S., and Sadikot, R. T. (2007) TREM-1 expression in macrophages is regulated at transcriptional level by NF-κB and PU.1. Eur. J. Immunol. 37, 2300-2308 (Pubitemid 47250221)
16. Ornatowska, M., Azim, A. C., Wang, X., Christman, J. W., Xiao, L., Joo, M., and Sadikot, R. T. (2007) Functional genomics of silencing TREM-1 on TLR4 signaling in macrophages. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L1377-1384 (Pubitemid 350255020)
17. Zheng, H., Heiderscheidt, C. A., Joo, M., Gao, X., Knezevic, N., Mehta, D., and Sadikot, R. T. (2010) MYD88-dependent and -independent activation of TREM-1 via specific TLR ligands. Eur. J. Immunol. 40, 162-171
18. Syed, M. A., Joo, M., Abbas, Z., Rodger, D., Christman, J. W., Mehta, D., and Sadikot, R. T. (2010) Expression of TREM-1 is inhibited by PGD2 and PGJ2 in macrophages. Exp. Cell Res. 316, 3140-3149
19. Zhou, J., Chai, F., Lu, G., Hang, G., Chen, C., Chen, X., and Shi, J. (2013) TREM-1 inhibition attenuates inflammation and tumor within the colon. Int. Immunopharmacol. 17, 155-161
20. Wu, J., Li, J., Salcedo, R., Mivechi, N. F., Trinchieri, G., and Horuzsko, A. (2012) The proinflammatory myeloid cell receptor TREM-1 controls Kupffer cell activation and development of hepatocellular carcinoma. Cancer Res. 72, 3977-3986
21. Liao, R., Sun, T. W., Yi, Y., Wu, H., Li, Y. W., Wang, J. X., Zhou, J., Shi, Y. H., Cheng, Y. F., Qiu, S. J., and Fan, J. (2012) Expression of TREM-1 in hepatic stellate cells and prognostic value in hepatitis B-related hepatocellular carcinoma. Cancer Sci. 103, 984-992
22. Ho, C. C., Liao, W. Y., Wang, C. Y., Lu, Y. H., Huang, H. Y., Chen, H. Y., Chan, W. K., Chen, H. W., and Yang, P. C. (2008) TREM-1 expression in tumor-associated macrophages and clinical outcome in lung cancer. Am. J. Respir. Crit. Care Med. 177, 763-770
23. Wyllie, A. H. (2010) "Where, O death, is thy sting?" A brief review of apoptosis biology. Mol. Neurobiol. 42, 4-9
24. Peter, M. E. (2011) Programmed cell death: apoptosis meets necrosis. Nature 471, 310-312
25. Hensley, P., Mishra, M., and Kyprianou, N. (2013) Targeting caspases in cancer therapeutics. Biol. Chem. 394, 831-843
26. Fiandalo, M. V., and Kyprianou, N. (2012) Caspase control: protagonists of cancer cell apoptosis. Exp. Oncol. 34, 165-175
27. Lauritsen, J. P., Kurella, S., Lee, S. Y., Lefebvre, J. M., Rhodes, M., Alberola- Ila, J., and Wiest, D. L. (2008) Egr2 is required for Bcl-2 induction during positive selection. J. Immunol. 181, 7778-7785
28. Joseph, L. J., Le Beau, M. M., Jamieson, G. A., Jr., Acharya, S., Shows, T. B., Rowley, J. D., and Sukhatme, V. P. (1988) Molecular cloning, sequencing, and mapping of EGR2, a human early growth response gene encoding a protein with "zinc-binding finger" structure. Proc. Natl. Acad. Sci. U.S.A. 85, 7164-7168
29. Lawson, V. J., Weston, K., and Maurice, D. (2010) Early growth response 2 regulates the survival of thymocytes during positive selection. Eur. J. Immunol. 40, 232-241
30. Lazarevic, V., Zullo, A. J., Schweitzer, M. N., Staton, T. L., Gallo, E. M., Crabtree, G. R., and Glimcher, L. H. (2009) The gene encoding early growth response 2, a target of the transcription factor NFAT, is required for the development and maturation of natural killer T cells. Nat. Immunol. 10, 306-313
31. Klesney-Tait, J., Keck, K., Li, X., Gilfillan, S., Otero, K., Baruah, S., Meyerholz, D. K., Varga, S. M., Knudson, C. J., Moninger, T. O., Moreland, J., Zabner, J., and Colonna, M. (2013) Transepithelial migration of neutrophils into the lung requires TREM-1. J. Clin. Invest. 123, 138-149
32. Sadikot, R. T., Jansen, E. D., Blackwell, T. R., Zoia, O., Yull, F., Christman, J. W., and Blackwell, T. S. (2001) High-dose dexamethasone accentuates nuclear factor-κ B activation in endotoxin-treated mice. Am. J. Respir. Crit. Care Med. 164, 873-878 (Pubitemid 32881927)
33. phox deficiency impairs NF-κB activation and host defense in Pseudomonas pneumonia. J. Immunol. 172, 1801-1808 (Pubitemid 38116828)
34. Dower, K., Ellis, D. K., Saraf, K., Jelinsky, S. A., and Lin, L. L. (2008) Innate immune responses to TREM-1 activation: overlap, divergence, and positive and negative cross-talk with bacterial lipopolysaccharide. J. Immunol. 180, 3520-3534
35. Hu, W., Xie, J., Zhao, J., Xu, Y., Yang, S., and Ni, W. (2009) Involvement of Bcl-2 family in apoptosis and signal pathways induced by cigarette smoke extract in the human airway smooth muscle cells. DNA Cell Biol. 28, 13-22
36. Kao, S. C., Wu, H., Xie, J., Chang, C. P., Ranish, J. A., Graef, I. A., and Crabtree, G. R. (2009) Calcineurin/NFAT signaling is required for neu-regulin-regulated Schwann cell differentiation. Science 323, 651-654
37. Ford, J. W., and McVicar, D. W. (2009)TREMand TREM-like receptors in inflammation and disease. Curr. Opin. Immunol. 21, 38-46
38. Cookson, B. T., and Brennan, M. A. (2001) Pro-inflammatory programmed cell death. Trends Microbiol. 9, 113-114
39. LaRock, C. N., and Cookson, B. T. (2013) Burning down the house: cellular actions during pyroptosis. PLoS Pathog. 9, e1003793
40. Chen, H., Detmer, S. A., Ewald, A. J., Griffin, E. E., Fraser, S. E., and Chan, D. C. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160, 189-200 (Pubitemid 36254953)
41. Cerveny, K. L., Tamura, Y., Zhang, Z., Jensen, R. E., and Sesaki, H. (2007) Regulation of mitochondrial fusion and division. Trends Cell Biol. 17, 563-569 (Pubitemid 350087661)
42. Zhang, Y., and Chan, D. C. (2007) New insights into mitochondrial fusion. FEBS Lett. 581, 2168-2173 (Pubitemid 46709902)
43. Brooks, C., Wei, Q., Feng, L., Dong, G., Tao, Y., Mei, L., Xie, Z. J., and Dong, Z. (2007) Bak regulates mitochondrial morphology and pathology during apoptosis by interacting with mitofusins. Proc. Natl. Acad. Sci. U.S.A. 104, 11649-11654 (Pubitemid 47175067)
44. Cleland, M. M., Norris, K. L., Karbowski, M., Wang, C., Suen, D. F., Jiao, S., George, N. M., Luo, X., Li, Z., and Youle, R. J. (2011) Bcl-2 family interaction with the mitochondrial morphogenesis machinery. Cell Death Differ. 18, 235-247
45. Rodrigues, M. F., Alves, C. C., Figueiredo, B. B., Rezende, A. B., Wohlres- Viana, S., Silva, V. L., Machado, M. A., and Teixeira, H. C. (2013) Tumour necrosis factor receptors and apoptosis of alveolar macrophages during early infection with attenuated and virulent Mycobacterium bovis. Immunology 139, 503-512
46. Nathan, C., and Ding, A. (2001) TREM-1: A new regulator of innate immunity in sepsis syndrome. Nat. Med. 7, 530-532 (Pubitemid 32448309)
47. Tessarz, A. S., and Cerwenka, A. (2008) The TREM-1/DAP12 pathway. Immunol. Lett. 116, 111-116
48. Colonna, M., and Facchetti, F. (2003) TREM-1 (triggering receptor expressed on myeloid cells): A new player in acute inflammatory responses. J. Infect. Dis. 187, S397-401 (Pubitemid 36724514)
49. Klesney-Tait, J., Turnbull, I. R., and Colonna, M. (2006) The TREM receptor family and signal integration. Nat. Immunol. 7, 1266-1273 (Pubitemid 46111244)
50. Elmore, S. (2007) Apoptosis: A review of programmed cell death. Toxicol. Pathol. 35, 495-516 (Pubitemid 46911891)
51. Taylor, R. C., Cullen, S. P., and Martin, S. J. (2008) Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9, 231-241 (Pubitemid 351301823)
52. Adams, J. M., and Cory, S. (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322-1326 (Pubitemid 28406819)
53. Liston, P., Fong, W. G., and Korneluk, R. G. (2003) The inhibitors of apoptosis: there is more to life than Bcl2. Oncogene 22, 8568-8580 (Pubitemid 38019194)
54. Busca, A., Saxena, M., Kryworuchko, M., and Kumar, A. (2009) Antiapoptotic genes in the survival of monocytic cells during infection. Curr. Genomics 10, 306-317
55. O'Donovan, K. J., Tourtellotte, W. G., Millbrandt, J., and Baraban, J. M. (1999) The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci. 22, 167-173 (Pubitemid 29166785)
56. Bassiri, H., and Nichols, K. E. (2009) It's up to you Egr2. Immunol. Cell Biol. 87, 361-363
57. Laslo, P., Spooner, C. J., Warmflash, A., Lancki, D. W., Lee, H. J., Sciammas, R., Gantner, B. N., Dinner, A. R., and Singh, H. (2006) Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126, 755-766 (Pubitemid 44233633)
58. + T cells. J. Immunol. 173, 7331-7338 (Pubitemid 39628171)
59. Hirano, S., Anuradha, C. D., and Kanno, S. (2002) krox-20/egr-2 is upregulated following non-specific and homophilic adhesion in rat macrophages. Immunology 107, 86-92
60. Keeton, A. B., Bortoff, K. D., Bennett, W. L., Franklin, J. L., Venable, D. Y., and Messina, J. L. (2003) Insulin-regulated expression of Egr-1 and Krox20: dependence on ERK1/2 and interaction with p38 and PI3-kinase pathways. Endocrinology 144, 5402-5410 (Pubitemid 37476069)
61. Kumbrink, J., Kirsch, K. H., and Johnson, J. P. (2010) EGR1, EGR2, and EGR3 activate the expression of their coregulator NAB2 establishing a negative feedback loop in cells of neuroectodermal and epithelial origin. J. Cell Biochem. 111, 207-217
62. Mager, G. M., Ward, R. M., Srinivasan, R., Jang, S. W., Wrabetz, L., and Svaren, J. (2008) Active gene repression by the Egr2.NAB complex during peripheral nerve myelination. J. Biol. Chem. 283, 18187-18197
63. Droin, N. M., Pinkoski, M. J., Dejardin, E., and Green, D. R. (2003) Egr family members regulate nonlymphoid expression of Fas ligand, TRAIL, and tumor necrosis factor during immune responses. Mol. Cell Biol. 23, 7638-7647 (Pubitemid 37271462)
64. Myouzen, K., Kochi, Y., Shimane, K., Fujio, K., Okamura, T., Okada, Y., Suzuki, A., Atsumi, T., Ito, S., Takada, K., Mimori, A., Ikegawa, S., Yamada, R., Nakamura, Y., and Yamamoto, K. (2010) Regulatory polymorphisms in EGR2 are associated with susceptibility to systemic lupus erythematosus. Hum. Mol. Genet. 19, 2313-2320
65. Venken, K., Di Maria, E., Bellone, E., Balestra, P., Cassandrini, D., Mandich, P., De Jonghe, P., Timmerman, V., and Svaren, J. (2002) Search for mutations in the EGR2 corepressor proteins, NAB1 and NAB2, in human peripheral neuropathies. Neurogenetics 4, 37-41 (Pubitemid 36401757)
66. Rolland, S. G., and Conradt, B. (2010) New role of the BCL2 family of proteins in the regulation of mitochondrial dynamics. Curr. Opin. Cell Biol. 22, 852-858
67. Rolland, S. G., Lu, Y., David, C. N., and Conradt, B. (2009) The BCL-2-like protein CED-9 of C. Elegans promotes FZO-1/Mfn1,2- and EAT-3/Opa1- dependent mitochondrial fusion. J. Cell Biol. 186, 525-540
68. Vander Heiden, M. G., Li, X. X., Gottleib, E., Hill, R. B., Thompson, C. B., and Colombini, M. (2001) Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J. Biol. Chem. 276, 19414-19419
69. + T cell-dependent xenoantibody production in innate tolerant nude rats after hamster islet grafting but not after hamster heart grafting. Transplantation 85, 1489-1495
70. Waxman, A. B., and Kolliputi, N. (2009) IL-6 protects against hyperoxiainduced mitochondrial damage via Bcl-2-induced Bak interactions with mitofusins. Am. J. Respir. Cell Mol. Biol. 41, 385-396