Deletion of MyD88 markedly attenuates sepsis-induced T and B lymphocyte apoptosis but worsens survival

Journal of Leukocyte Biology

Volumn 83, Issue 4, 2008, Pages 1009-1018

  Peck Palmer, Octavia M ^a   Unsinger, Jacqueline ^a   Chang, Katherine C ^a   Davis, Christopher G ^a   McDunn, Jonathan E ^a   Hotchkiss, Richard S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell death; Cell signaling; Cytokines; Endotoxin

Indexed keywords

CASPASE 3; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; CYTOKINE; MYD88 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DISEASE EXACERBATION; GENE DELETION; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; SEPSIS; SURVIVAL; T LYMPHOCYTE; ANIMAL; DEATH; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MUS;

ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CASPASE 3; CYTOKINES; DEATH; IN SITU NICK-END LABELING; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; SEPSIS; T-LYMPHOCYTES;

EID: 44449165650     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0807528     Document Type: Article

References (53)

1. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J., Pinsky, M. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310.
2. Ayala, A., Herdon, C. D., Lehman, D. L., Ayala, C. A., Chaudry, I. H. (1996) Differential induction of apoptosis in lymphoid tissues during sepsis: variation in onset, frequency, and the nature of the mediators. Blood 87, 4261-4275.
3. Efron, P. A., Tinsley, K., Minnich, D. J., Monterroso, V., Wagner, J., Lainee, P., Lorre, K., Swanson, P. E., Hotchkiss, R., Moldawer, L. L. (2004) Increased lymphoid tissue apoptosis in baboons with bacteremic shock. Shock 21, 566-571.
4. Hotchkiss, R. S., Swanson, P. E., Freeman, B. D., Tinsley, K. W., Cobb, J. P., Matuschak, G. M., Buchman, T. G., Karl, I. E. (1999) Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit. Care Med. 27, 1230-1251.
5. Wesche-Soldato, D. E., Swan, R. Z., Chung, C. S., Ayala, A. (2007) The apoptotic pathway as a therapeutic target in sepsis. Curr. Drug Targets 8, 493-500.
6. Wesche, D. E., Lomas-Neira, J. L., Perl, M., Chung, C. S., Ayala, A. (2005) Leukocyte apoptosis and its significance in sepsis and shock. J. Leukoc. Biol. 78, 325-337.
7. Lederer, J. A., Rodrick, M., Mannick, J. (1999) The effects of injury on the adaptive immune\response. Shock 11, 153-159.
8. Felmet, K. A., Hall, M. W., Clark, R. S., Jaffe, R., Carcillo, J. A. (2005) Prolonged lymphopenia, lymphoid depletion, and hypoprolactinemia in children with nosocomial sepsis and multiple organ failure. J. Immunol. 174, 3765-3772.
9. Hotchkiss, R. S., Karl, I. E. (2003) The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348, 138-150.
10. Medzhitov, R., Preston-Hurlburt, P., Janeway Jr., C. A. (1997) A human homologue of the Drosphilia Toll protein signals activation of adaptive immunity. Nature 388, 394-397.
11. Akira, S., Takeda, K., Kaisho, T. (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-690.
12. Warren, H. S. (2005) Toll-like receptors. Crit. Care Med. 33 (Suppl. 12), S457-S459.
13. Shimazu, R., Akashi, S., Ogata, H., Nagai, Y., Fukudome, K., Miyake, K., Kimoto, M. (1999) MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 189, 1777-1782.
14. Medzhitov, R., Preston-Hurlburt, P., Kopp, E., Stadlen, A., Chen, C., Ghosh, S., Janeway, C. A. (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2, 253-258.
15. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., Nakanishi, K., Akira, S. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143-150.
16. Zhou, S., Kurt-Jones, E. A., Mandell, L., Cerny, A., Chan, M., Golenbock, D. T., Finberg, R. W. (2005) MyD88 is critical for the development of innate and adaptive immunity during acute lymphocytic choriomeningitis virus infection. Eur. J. Immunol. 35, 822-830.
17. Takeda, K., Akira, S. (2004) TLR signaling pathways. Semin. Immunol. 16, 3-9.
18. Kawai, T., Takeuchi, O., Fujita, T., Inoue, J., Muhlradt, P., Sato, S., Hoshino, K., Akira, S. (2001) Lipopolysaccharide stimulates the MyD88-dependent pathway and results in activation of IRF-3 and the expression of a subset of LPS-inducible genes. J. Immunol. 167, 5887-5894.
19. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J., Greenberg, M. E. (1995) Opposing effects of ERK, JNK and p38 MAP kinases on apoptosis. Science 270, 1326-1331.
20. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K., Akira, S. (2003) Role of adaptor TRIF in MyD88-independent Toll-like receptor signaling pathway. Science 301, 640-643.
21. Sato, S., Sugiyama, M., Yamamoto, M., Watanabe, Y., Kawai, T., Takeda, K., Akira, S. (2003) TRIF associates with TNF receptor associated factor 6 and TANK binding kinase 1, and activates two distinct transcription factors, NFκB and IFN-regulatory factor 3, in the Toll-like receptor signaling. J. Immunol. 171, 4304-4310.
22. Schindler, C. (1998) STATs as activators of apoptosis. Trends Cell Biol. 8, 97-98.
23. Akira, S. (1999) Functional roles of STAT family proteins: lessons from knockout mice. Stem Cells 17, 138-146.
24. Matsukawa, A., Kaplan, M. H., Hogaboam, C. M., Lukacs, N. W., Kunkel, S. L. (2001) Pivotal role of signal transducer and activator of transcription (Stat) 4 and Stat6 in the innate immune response during sepsis. J. Exp. Med. 193, 679-688.
25. Baker, C. C., Chaudry, I. H., Gaines, H. O., Baue, A. E. (1983) Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery 94, 331-335.
26. Hotchkiss, R. S., Chang, K. C., Swanson, P. E., Tinsley, K. W., Hui, J. J., Klender, P., Xanthoudakis, S., Roy, S., Black, C., Grimm, E., Aspiotis, R., Han, Y., Nicholson, D. W., Karl, I. E. (2000) Caspase inhibitors improve survival in sepsis: a critical role of the lymphocyte. Nat. Immunol. 1, 496-501.
27. Hotchkiss, R. S., Tinsley, K. W., Swanson, P. E., Schmieg Jr., R. E., Hui, J. J., Chang, K. C., Osborne, D. F., Freeman, B. D., Cobb, J. P., Buchman, T. G., Karl, I. E. (2001) Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans. J. Immunol. 166, 6952-6963.
28. Chang, K. C., Unsinger, J., Davis, C. G., Schwulst, S. J., Muenzer, J. T., Strasser, A., Hotchkiss, R. S. (2007) Multiple triggers of cell death in sepsis: death receptor and mitochondrial-mediated apoptosis. FASEB J. 21, 708-719.
29. Riedemann, N. C., Guo, R., Ward, P. A. (2003) Novel strategies for the treatment of sepsis. Nat. Med. 9, 517-524.
30. Refaeli, Y., Van Parijs, L., Alexander, S. I., Abbas, A. K. (2002) Interferon γ is required for activation-induced death of T lymphocytes. J. Exp. Med. 196, 999-1005.
31. Ruckdeschel, K., Pfaffinger, G., Haase, R., Sing, A., Weighardt, H., Hacker, G., Holzmann, B., Heesemann, J. (2004) Signaling of apoptosis through TLRs critically involves Toll/IL-1 receptor domain-containing adapter inducing IFN-β, but not MyD88, in bacteria-infected murine macrophages. J. Immunol. 173, 3320-3328.
32. Haase, R., Kirschning, C. J., Sing, A., Schröttner, P., Fukase, K., Kusumoto, S., Wagner, H., Heesemann, H., Ruckdeschel, K. (2003) A dominant role of Toll-like receptor 4 in the signaling of apoptosis in bacteria-faced macrophages. J. Immunol. 171, 4294-4303.
33. Colino, J., Snapper, C. M. (2003) Two distinct mechanisms for induction of dendritic cell apoptosis in response to intact Streptococcus pneumoniae. J. Immunol. 171, 2354-2365.
34. De Trez, C., Pajak, B., Brait, M., Glaichenhaus, N., Urbain, J., Moser, M., Lauvau, G., Muraille, E. (2005) TLR4 and Toll-IL-1 receptor domain-containing adapter-inducing IFN-γ, but not MyD88, regulate Escherichia coli-induced dendritic cell maturation and apoptosis in vivo. J. Immunol. 175, 839-846.
35. Dear, J. W., Yasuda, H., Hu, X., Hieny, S., Yuen, P. S. T., Hewitt, S. M., Sher, A., Star, R. A. (2006) Sepsis-induced organ failure is mediated by different pathways in the kidney and liver: acute renal failure is dependent on MyD88 but not renal cell apoptosis. Kidney Int. 69, 832-836.
36. Caramalho, I., Lopes-Carvalho, T., Ostler, D., Zelenay, S., Haury, M., Demengeot, J. (2003) Regulatory T cells selectively express Toll-like receptors and are activated by lipopolysaccharide. J. Exp. Med. 197, 403-411.
37. Komai-Koma, M., Jones, L., Ogg, G. S., Xu, D., Liew, F. Y. (2004) TLR2 is expressed on activated T cells as a costimulatory receptor. Proc. Natl. Acad. Sci. USA 101, 3029-3034.
38. + regulatory T cell function. Science 309, 1380-1384.
39. Pasare, C., Medzhitov, R. (2005) Control of B-cell responses by Toll-like receptors. Nature 438, 364-368.
40. Gelman, A. E., LaRosa, D., Zhang, J., Walsh, P., Choi, Y., Sunyer, J. O., Turka, L. A. (2006) The adaptor molecule MyD88 activates PI-3 kinase signaling in CD+ T cells and enables CpG oligodeoxynucleotide-medicated costimulation. Immunity 25, 783-793.
41. Hiramatsu, M., Hotchkiss, R. S., Karl, I. E., Buckman, T. G. (1997) Cecal ligation and puncture (CLP) induced apoptosis in thymus spleen, lung and gut by endotoxin and TNF-independent pathway. Shock 7, 247-253.
42. Kaiser, W. J., Offermann, M. (2005) Apoptosis induced by the Toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol. 174, 4942-4952.
43. Lin, A., Dibling, B. (2002) The true face of JNK activation in apoptosis. Aging Cell 1, 112-116.
44. Weston, C. R., Wong, A., Hall, J. P., Goad, M. E. P., Flavell, R. A., Davis, R. J. (2004) The c-Jun NH2-terminal kinase is essential for epidermal growth factor expression during epidermal morphogenesis. Proc. Natl. Acad. Sci. USA 101, 14114-14119.
45. Dong, C., Yang, D. D., Wysk, M., Whitmarsh, A. J., Davis, R. J., Flavell, R. A. (1998) Defective T cell differentiation in the absence of Jnk1. Science 282, 2092-2095.
46. Cross, T. G., Scheel-Toellner, D., Henriquez, N., Deacon, E., Salmon, M., Lord, J. (2000) Serine/threonine protein kinases and apoptosis. Exp. Cell Res. 256, 34-41.
47. Zhang, J., Gao, J., Salojin, K., Shao, Q., Grattan, M., Meagher, C., Laird, D. (2000) Regulation of Fas ligand expression during activation-induced cell death in T cells by p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase. J. Exp. Med. 191, 1017-1029.
48. Kawai, T., Adachi, O., Ogawa, T., Takeda, K., Akira, S. (1999) Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11, 115-122.
49. Albiger, B., Sandgren, A., Katsuragi, H., Meyer-Hoffert, U., Beiter, K., Wartha, F., Hornef, M., Normark, S., Normark, B. (2005) Myeloid differentiation factor 88-dependent signaling controls bacterial growth during colonization and systemic pneumococcal disease in mice. Cell. Microbiol. 7, 1603-1615.
50. Weighardt, H., Kaiser-Moore, S., Vabulas, R. M., Kirschning, C. J., Wagner, H., Holzmann, B. (2002) Cutting edge: myeloid differentiation factor 88 deficiency improves resistance against sepsis caused by polymicrobial infection. J. Immunol. 169, 2823-2827.
51. Maier, S., Traeger, T., Entleutner, M., Westerholt, A., Kleist, B., Huser, N., Holzmann, B., Stier, A., Pfeffer, K., Heidecke, C. (2004) Cecal ligation and puncture versus colon ascendens stent peritonitis: two distinct animal models for polymicrobrial sepsis. Shock 21, 505-512.
52. + population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med. 204, 1463-1474.
53. Hotchkiss, R. S., Tinsley, K. W., Hui, J., Chang, K. C., Swanson, P. E., Drewry, A. M., Buchman, T. G., Karl, I. E. (2000) p53-dependent and -independent pathways of apoptotic cell death in sepsis. J. Immunol. 164, 3675-3680.