Polymicrobial sepsis diminishes dendritic cell numbers and function directly contributing to impaired primary CD8 T cell responses in vivo

Journal of Immunology

Volumn 197, Issue 11, 2016, Pages 4301-4311

  Strother, Robert K ^a   Danahy, Derek B ^a,b   Kotov, Dmitri I ^c,d   Kucaba, Tamara A ^c   Zacharias, Zeb R ^a,b   Griffith, Thomas S ^c,d,e   Legge, Kevin L ^a,b   Badovinac, Vladimir P ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLT3 LIGAND; INTERLEUKIN 12; ANTIGEN; CYTOKINE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CECAL LIGATION AND PUNCTURE-INDUCED SEPSIS; CELL EXPANSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; IN VITRO STUDY; IN VIVO STUDY; LISTERIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPSIS; ANIMAL; ANTIGEN PRESENTATION; GENETICS; IMMUNOLOGY; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; MICE; MICE, TRANSGENIC; SEPSIS;

EID: 84996538210     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1601463     Document Type: Article

References (71)

1. Fleischmann, C., A. Scherag, N. K. Adhikari, C. S. Hartog, T. Tsaganos, P. Schlattmann, D. C. Angus, and K. Reinhart, International Forum of Acute Care Trialists. 2016. Assessment of global incidence and mortality of hospital-treated sepsis. Current estimates and limitations. Am. J. Respir. Crit. Care Med. 193: 259-272.
2. Donnelly, J. P., S. F. Hohmann, and H. E. Wang. 2015. Unplanned readmissions after hospitalization for severe sepsis at academic medical center-affiliated hospitals. Crit. Care Med. 43: 1916-1927.
3. Hotchkiss, R. S., C. M. Coopersmith, J. E. McDunn, and T. A. Ferguson. 2009. The sepsis seesaw: tilting toward immunosuppression. Nat. Med. 15: 496-497.
4. Limaye, A. P., K. A. Kirby, G. D. Rubenfeld, W. M. Leisenring, E. M. Bulger, M. J. Neff, N. S. Gibran, M. L. Huang, T. K. Santo Hayes, L. Corey, and M. Boeckh. 2008. Cytomegalovirus reactivation in critically ill immunocom-petent patients. JAMA 300: 413-422.
5. Luyt, C. E., A. Combes, C. Deback, M. H. Aubriot-Lorton, A. Nieszkowska, J. L. Trouillet, F. Capron, H. Agut, C. Gibert, and J. Chastre. 2007. Herpes simplex virus lung infection in patients undergoing prolonged mechanical ventilation. Am. J. Respir. Crit. Care Med. 175: 935-942.
6. Quartin, A. A., R. M. Schein, D. H. Kett, and P. N. Peduzzi, Department of Veterans Affairs Systemic Sepsis Cooperative Studies Group. 1997. Magnitude and duration of the effect of sepsis on survival. JAMA 277: 1058-1063.
7. Hotchkiss, R. S., P. E. Swanson, B. D. Freeman, K. W. Tinsley, J. P. Cobb, G. M. Matuschak, T. G. Buchman, and I. E. Karl. 1999. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit. Care Med. 27: 1230-1251.
8. Le Tulzo, Y., C. Pangault, A. Gacouin, V. Guilloux, O. Tribut, L. Amiot, P. Tattevin, R. Thomas, R. Fauchet, and B. Drénou. 2002. Early circulating lymphocyte apo-ptosis in human septic shock is associated with poor outcome. Shock 18: 487-494.
9. Hotchkiss, R. S., S. B. Osmon, K. C. Chang, T. H. Wagner, C. M. Coopersmith, and I. E. Karl. 2005. Accelerated lymphocyte death in sepsis occurs by both the death receptor and mitochondrial pathways. J. Immunol. 174: 5110-5118.
10. Condotta, S. A., D. Rai, B. R. James, T. S. Griffith, and V. P. Badovinac. 2013. Sustained and incomplete recovery of naive CD8+ T cell precursors after sepsis contributes to impaired CD8+ T cell responses to infection. J. Immunol. 190: 1991-2000.
11. Condotta, S. A., S. H. Khan, D. Rai, T. S. Griffith, and V. P. Badovinac. 2015. Polymicrobial sepsis increases susceptibility to chronic viral infection and ex-acerbates CD8+ T cell exhaustion. J. Immunol. 195: 116-125.
12. Duong, S., S. A. Condotta, D. Rai, M. D. Martin, T. S. Griffith, and V. P. Badovinac. 2014. Polymicrobial sepsis alters antigen-dependent and-independent memory CD8 T cell functions. J. Immunol. 192: 3618-3625.
13. Danahy, D. B., R. K. Strother, V. P. Badovinac, and T. S. Griffith. 2016. Clinical and experimental sepsis impairs CD8 T-cell-mediated immunity. Crit. Rev. Immunol. 36: 57-74.
14. Chang, J. T., E. J. Wherry, and A. W. Goldrath. 2014. Molecular regulation of effector and memory T cell differentiation. Nat. Immunol. 15: 1104-1115.
15. Haring, J. S., V. P. Badovinac, and J. T. Harty. 2006. Inflaming the CD8+ T cell response. Immunity 25: 19-29.
16. Mescher, M. F., J. M. Curtsinger, P. Agarwal, K. A. Casey, M. Gerner, C. D. Hammerbeck, F. Popescu, and Z. Xiao. 2006. Signals required for program-ming effector and memory development by CD8+ T cells. Immunol. Rev. 211: 81-92.
17. Harty, J. T., and V. P. Badovinac. 2008. Shaping and reshaping CD8+ T-cell memory. Nat. Rev. Immunol. 8: 107-119.
18. Curtsinger, J. M., C. S. Schmidt, A. Mondino, D. C. Lins, R. M. Kedl, M. K. Jenkins, and M. F. Mescher. 1999. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J. Immunol. 162: 3256-3262.
19. Schmidt, C. S., and M. F. Mescher. 1999. Adjuvant effect of IL-12: conversion of peptide antigen administration from tolerizing to immunizing for CD8+ T cells in vivo. J. Immunol. 163: 2561-2567.
20. Schmidt, C. S., and M. F. Mescher. 2002. Peptide antigen priming of naive, but not memory, CD8 T cells requires a third signal that can be provided by IL-12. J. Immunol. 168: 5521-5529.
21. Turley, S. J., A. L. Fletcher, and K. G. Elpek. 2010. The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat. Rev. Immunol. 10: 813-825.
22. Merad, M., P. Sathe, J. Helft, J. Miller, and A. Mortha. 2013. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31: 563-604.
23. Shortman, K., and Y. J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2: 151-161.
24. Lanzavecchia, A., and F. Sallusto. 2001. Antigen decoding by T lymphocytes: from synapses to fate determination. Nat. Immunol. 2: 487-492.
25. Hotchkiss, R. S., K. W. Tinsley, P. E. Swanson, M. H. Grayson, D. F. Osborne, T. H. Wagner, J. P. Cobb, C. Coopersmith, and I. E. Karl. 2002. Depletion of dendritic cells, but not macrophages, in patients with sepsis. J. Immunol. 168: 2493-2500.
26. Poehlmann, H., J. C. Schefold, H. Zuckermann-Becker, H. D. Volk, and C. Meisel. 2009. Phenotype changes and impaired function of dendritic cell subsets in patients with sepsis: a prospective observational analysis. Crit. Care 13: R119.
27. Guisset, O., M. S. Dilhuydy, R. Thiébaut, J. Lefèvre, F. Camou, A. Sarrat, C. Gabinski, J. F. Moreau, and P. Blanco. 2007. Decrease in circulating dendritic cells predicts fatal outcome in septic shock. Intensive Care Med. 33: 148-152.
28. Tinsley, K. W., M. H. Grayson, P. E. Swanson, A. M. Drewry, K. C. Chang, I. E. Karl, and R. S. Hotchkiss. 2003. Sepsis induces apoptosis and profound depletion of splenic interdigitating and follicular dendritic cells. J. Immunol. 171: 909-914.
29. Ding, Y., C. S. Chung, S. Newton, Y. Chen, S. Carlton, J. E. Albina, and A. Ayala. 2004. Polymicrobial sepsis induces divergent effects on splenic and peritoneal dendritic cell function in mice. Shock 22: 137-144.
30. Flohé, S. B., H. Agrawal, D. Schmitz, M. Gertz, S. Flohé, and F. U. Schade. 2006. Dendritic cells during polymicrobial sepsis rapidly mature but fail to initiate a protective Th1-type immune response. J. Leukoc. Biol. 79: 473-481.
31. Scumpia, P. O., P. F. McAuliffe, K. A. O'Malley, R. Ungaro, T. Uchida, T. Matsumoto, D. G. Remick, M. J. Clare-Salzler, L. L. Moldawer, and P. A. Efron. 2005. CD11c+ dendritic cells are required for survival in murine polymicrobial sepsis. J. Immunol. 175: 3282-3286.
32. Efron, P. A., A. Martins, D. Minnich, K. Tinsley, R. Ungaro, F. R. Bahjat, R. Hotchkiss, M. Clare-Salzler, and L. L. Moldawer. 2004. Characterization of the systemic loss of dendritic cells in murine lymph nodes during polymicrobial sepsis. J. Immunol. 173: 3035-3043.
33. Pastille, E., S. Didovic, D. Brauckmann, M. Rani, H. Agrawal, F. U. Schade, Y. Zhang, and S. B. Flohé. 2011. Modulation of dendritic cell differentiation in the bone marrow mediates sustained immunosuppression after polymicrobial sepsis. J. Immunol. 186: 977-986.
34. Wen, H., Y. Dou, C. M. Hogaboam, and S. L. Kunkel. 2008. Epigenetic regu-lation of dendritic cell-derived interleukin-12 facilitates immunosuppression after a severe innate immune response. Blood 111: 1797-1804.
35. Benjamim, C. F., S. K. Lundy, N. W. Lukacs, C. M. Hogaboam, and S. L. Kunkel. 2005. Reversal of long-term sepsis-induced immunosuppression by dendritic cells. Blood 105: 3588-3595.
36. Pène, F., B. Zuber, E. Courtine, C. Rousseau, F. Ouaaz, J. Toubiana, A. Tazi, J. P. Mira, and J. D. Chiche. 2008. Dendritic cells modulate lung response to Pseudomonas aeruginosa in a murine model of sepsis-induced immune dys-function. J. Immunol. 181: 8513-8520.
37. Wen, H., C. M. Hogaboam, J. Gauldie, and S. L. Kunkel. 2006. Severe sepsis exacerbates cell-mediated immunity in the lung due to an altered dendritic cell cytokine profile. Am. J. Pathol. 168: 1940-1950.
38. Wang, H. W., W. Yang, L. Gao, J. R. Kang, J. J. Qin, Y. P. Liu, and J. Y. Lu. 2015. Adoptive transfer of bone marrow-derived dendritic cells decreases inhibitory and regulatory T-cell differentiation and improves survival in murine polymicrobial sepsis. Immunology 145: 50-59.
39. Toliver-Kinsky, T. E., W. Cui, E. D. Murphey, C. Lin, and E. R. Sherwood. 2005. Enhancement of dendritic cell production by fms-like tyrosine kinase-3 ligand increases the resistance of mice to a burn wound infection. J. Immunol. 174: 404-410.
40. Bohannon, J., W. Cui, R. Cox, R. Przkora, E. Sherwood, and T. Toliver-Kinsky. 2008. Prophylactic treatment with fms-like tyrosine kinase-3 ligand after burn injury enhances global immune responses to infection. J. Immunol. 180: 3038-3048.
41. Wang, H. W., W. Yang, J. Y. Lu, G. Tian, F. Li, X. H. Wang, J. R. Kang, and Y. Yang. 2012. Treatment with Fms-like tyrosine kinase 3 ligand reverses lung dendritic cell immunoparalysis and ameliorates zymosan-induced secondary lung injury in mice. Clin. Exp. Immunol. 170: 156-166.
42. Badovinac, V. P., and J. T. Harty. 2000. Adaptive immunity and enhanced CD8+ T cell response to Listeria monocytogenes in the absence of perforin and IFN-gamma. J. Immunol. 164: 6444-6452.
43. Rittirsch, D., M. S. Huber-Lang, M. A. Flierl, and P. A. Ward. 2009. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 4: 31-36.
44. Gurung, P., D. Rai, S. A. Condotta, J. C. Babcock, V. P. Badovinac, and T. S. Griffith. 2011. Immune unresponsiveness to secondary heterologous bacterial infection after sepsis induction is TRAIL dependent. J. Immunol. 187: 2148-2154.
45. De Smedt, T., B. Pajak, E. Muraille, L. Lespagnard, E. Heinen, P. De Baetselier, J. Urbain, O. Leo, and M. Moser. 1996. Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J. Exp. Med. 184: 1413-1424.
46. Pulendran, B., P. Kumar, C. W. Cutler, M. Mohamadzadeh, T. Van Dyke, and J. Banchereau. 2001. Lipopolysaccharides from distinct pathogens induce dif-ferent classes of immune responses in vivo. J. Immunol. 167: 5067-5076.
47. Auerbuch, V., D. G. Brockstedt, N. Meyer-Morse, M. O'Riordan, and D. A. Portnoy. 2004. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 200: 527-533.
48. Martin, M. D., and V. P. Badovinac. 2015. Antigen-dependent and-independent contributions to primary memory CD8 T cell activation and protection following infection. Sci. Rep. 5: 18022.
49. Bonifaz, L., D. Bonnyay, K. Mahnke, M. Rivera, M. C. Nussenzweig, and R. M. Steinman. 2002. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell toler-ance. J. Exp. Med. 196: 1627-1638.
50. Jiang, W., W. J. Swiggard, C. Heufler, M. Peng, A. Mirza, R. M. Steinman, and M. C. Nussenzweig. 1995. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 375: 151-155.
51. Maraskovsky, E., K. Brasel, M. Teepe, E. R. Roux, S. D. Lyman, K. Shortman, and H. J. McKenna. 1996. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell sub-populations identified. J. Exp. Med. 184: 1953-1962.
52. Hotchkiss, R. S., G. Monneret, and D. Payen. 2013. Sepsis-induced immuno-suppression: from cellular dysfunctions to immunotherapy. Nat. Rev. Immunol. 13: 862-874.
53. Dinarello, C. A. 1997. Proinflammatory and anti-inflammatory cytokines as mediators in the pathogenesis of septic shock. Chest 112(Suppl.)321S-329S.
54. Dinarello, C. A. 2000. Proinflammatory cytokines. Chest 118: 503-508.
55. Hotchkiss, R. S., K. W. Tinsley, P. E. Swanson, R. E. Schmieg, Jr., J. J. Hui, K. C. Chang, D. F. Osborne, B. D. Freeman, J. P. Cobb, T. G. Buchman, and I. E. Karl. 2001. Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans. J. Immunol. 166: 6952-6963.
56. Hiramatsu, M., R. S. Hotchkiss, I. E. Karl, and T. G. Buchman. 1997. Cecal ligation and puncture (CLP) induces apoptosis in thymus, spleen, lung, and gut by an endotoxin and TNF-independent pathway. Shock 7: 247-253.
57. Condotta, S. A., J. Cabrera-Perez, V. P. Badovinac, and T. S. Griffith. 2013. T-cell-mediated immunity and the role of TRAIL in sepsis-induced immuno-suppression. Crit. Rev. Immunol. 33: 23-40.
58. Hotchkiss, R. S., and D. W. Nicholson. 2006. Apoptosis and caspases regulate death and inflammation in sepsis. Nat. Rev. Immunol. 6: 813-822.
59. Mellman, I., and R. M. Steinman. 2001. Dendritic cells: specialized and regu-lated antigen processing machines. Cell 106: 255-258.
60. Badovinac, V. P., A. R. Tvinnereim, and J. T. Harty. 2000. Regulation of antigen-specific CD8+ T cell homeostasis by perforin and interferon-gamma. Science 290: 1354-1358.
61. Whitmire, J. K., J. T. Tan, and J. L. Whitton. 2005. Interferon-gamma acts di-rectly on CD8+ T cells to increase their abundance during virus infection. J. Exp. Med. 201: 1053-1059.
62. Lynch, D. H., A. Andreasen, E. Maraskovsky, J. Whitmore, R. E. Miller, and J. C. Schuh. 1997. Flt3 ligand induces tumor regression and antitumor immune responses in vivo. Nat. Med. 3: 625-631.
63. Lyman, S. D. 1995. Biology of flt3 ligand and receptor. Int. J. Hematol. 62: 63-73.
64. Maraskovsky, E., E. Daro, E. Roux, M. Teepe, C. R. Maliszewski, J. Hoek, D. Caron, M. E. Lebsack, and H. J. McKenna. 2000. In vivo generation of human dendritic cell subsets by Flt3 ligand. Blood 96: 878-884.
65. Pulendran, B., J. Banchereau, S. Burkeholder, E. Kraus, E. Guinet, C. Chalouni, D. Caron, C. Maliszewski, J. Davoust, J. Fay, and K. Palucka. 2000. Flt3-ligand and granulocyte colony-stimulating factor mobilize distinct human dendritic cell subsets in vivo. J. Immunol. 165: 566-572.
66. Freedman, R. S., S. Vadhan-Raj, C. Butts, C. Savary, B. Melichar, C. Verschraegen, J. J. Kavanagh, M. E. Hicks, L. B. Levy, J. K. Folloder, and M. E. Garcia. 2003. Pilot study of Flt3 ligand comparing intraperitoneal with subcutaneous routes on hematologic and immunologic responses in patients with peritoneal carcinomatosis and mesotheliomas. Clin. Cancer Res. 9: 5228-5237.
67. Higano, C. S., N. J. Vogelzang, J. A. Sosman, A. Feng, D. Caron, and E. J. Small. 2004. Safety and biological activity of repeated doses of recombinant human Flt3 ligand in patients with bone scan-negative hormone-refractory prostate cancer. Clin. Cancer Res. 10: 1219-1225.
68. Marroquin, C. E., J. A. Westwood, R. Lapointe, A. Mixon, J. R. Wunderlich, D. Caron, S. A. Rosenberg, and P. Hwu. 2002. Mobilization of dendritic cell precursors in patients with cancer by flt3 ligand allows the generation of higher yields of cultured dendritic cells. J. Immunother. 25: 278-288.
69. Morse, M. A., S. Nair, M. Fernandez-Casal, Y. Deng, M. St Peter, R. Williams, A. Hobeika, P. Mosca, T. Clay, R. I. Cumming, et al. 2000. Preoperative mobilization of circulating dendritic cells by Flt3 ligand administration to patients with metastatic colon cancer. J. Clin. Oncol. 18: 3883-3893.
70. Gasparetto, C., M. Gasparetto, M. Morse, B. Rooney, J. J. Vredenburgh, G. D. Long, D. A. Rizzieri, J. Loftis, N. J. Chao, and C. Smith. 2002. Mobilization of dendritic cells from patients with breast cancer into peripheral blood stem cell leukapheresis samples using Flt-3-Ligand and G-CSF or GM-CSF. Cytokine 18: 8-19.
71. Anandasabapathy, N., G. Breton, A. Hurley, M. Caskey, C. Trumpfheller, P. Sarma, J. Pring, M. Pack, N. Buckley, I. Matei, et al. 2015. Efficacy and safety of CDX-301, recombinant human Flt3L, at expanding dendritic cells and he-matopoietic stem cells in healthy human volunteers. Bone Marrow Transplant. 50: 924-930.