Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans

Journal of Immunology

Volumn 166, Issue 11, 2001, Pages 6952-6963

  Hotchkiss, Richard S ^a,b   Tinsley, Kevin W ^a   Swanson, Paul E ^a   Schmieg Jr , Robert E ^a   Hui, Jia Ji ^a   Chang, Katherine C ^a   Osborne, Dale F ^a   Freeman, Bradley D ^a   Cobb, J Perren ^a   Buchman, Timothy G ^a   Karl, Irene E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Anesthesiology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 9; CD4 ANTIGEN;

ADULT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL LOSS; CELL TYPE; CONTROLLED STUDY; CRITICAL ILLNESS; EFFECTOR CELL; FEMALE; HELPER CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; LETHALITY; LYMPHOCYTE CLONE; LYMPHOCYTE DEPLETION; LYMPHOCYTE SUBPOPULATION; MAJOR CLINICAL STUDY; MALE; NATURAL KILLER CELL; PRIORITY JOURNAL; SEPSIS; SPLEEN; T LYMPHOCYTE;

EID: 0035338993     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.166.11.6952     Document Type: Article

References (43)

1. Hoyert, D. L., K. D. Kochanek, and S. L. Murphy. 1999. Deaths: final data for 1997. Natl. Vital Stat. Rep. 47:1.
2. Bone, R.C. Sir Isaac Newton, sepsis, SIRS, and CARS. 1996. Crit. Care Med. 24:1125.
3. Natanson, C., W. D. Hoffman, A. F. Suffredini, P. Q. Eichacker, and R. L. Danner. 1994. Selected treatment strategies for septic shock based on proposed mechanisms of pathogenesis. Ann. Intern. Med. 120:771.
4. Bone, R. C., R. A. Balk, F. B. Cerra, R. P. Dellinger, A. M. Fein, W. A. Knaus, R. M. Schein, and W. J. Sibbald. 1992. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Chest 101:1644.
5. Eli. Lilly and company. 2000. Lilly stops enrollment in phase III study of recombinant human activated protein C in severe sepsis. PRNewswire 6/29/2000.
6. Bernard, G. R. 1999. Research in sepsis and acute respiratory distress syndrome: are we changing course? Crit. Care Med. 7:434.
7. O'Reilly, M., D. E. Newcomb, and D. Remick. 1999. Endotoxin, sepsis, and the primrose path. Shock 12:411.
8. Ayala, A., C. Herndon, D. Lehman, and I. H. Chaudry. 1996. Differential induction of apoptosis in lymphoid tissue during sepsis: variation in onset, frequency and nature of the mediators. Blood 87:4261.
9. Hotchkiss, R. S., P. E. Swanson, J. P. Cobb, A. Jacobson, T. G. Buchman, and I. E. Karl. 1997. Apoptosis in lymphoid and parenchymal cells during sepsis: Findings in normal and T- and B-cell deficient mice. Crit. Care Med. 25:1298.
10. 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.
11. Ayala, A., Y. X. Xu, C. S. Chung, and I. H. Chaudry. 1999. Does Fas ligand or endotoxin contribute to thymic apoptosis during polymicrobial sepsis? Shock 11:211.
12. Moldawer, L. L. 1999. Organ apoptosis in the septic patient: a potential therapeutic target? Crit. Care Med. 27:1381.
13. Meakins, J. L., J. B. Pietsch, O. Bubenick, R. Kelly, H. Rode, J. Gordon, and L.D. MacClean. 1977. Delayed hypersensitivity: indicator of acquired failure of host defenses in sepsis and trauma. Ann. Surg. 186:241.
14. Pietsch, J. B., J. L. Meakins, and L.D. MacLean. 1977. The delayed hypersensitivity response: application in clinical surgery. Surgery 82:349.
15. Cheadle, W. G., R. M. Pemberton, D. Robinson, D. H. Livingston, J. L. Rodriguez, and H. C. Polk, Jr. 1993. Lymphocyte subset responses to trauma and sepsis. J. Trauma 35:844.
16. Rajan, G., and J. W. Sleigh. 1997. Lymphocyte counts and the development of nosocomial sepsis. Intensive Care 23:1187.
17. Hotchkiss, R. S., K. W. Tinsley, P. E. Swanson, K. C. Chang, J. P. Cobb, T. G. Buchman, S. J. Korsmeyer, and I. E. Karl. 1999. Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc. Natl. Acad. Sci. USA 96: 14541.
18. Thornberry, N. A., and Y. Lazebnik. 1998. Caspases: enemies within. Science 281:1312.
19. Roy, S., and D.W. Nicholson 2000. Cross-talk in cell death signaling. J. Exp. Med. 192:F21.
20. Hotchkiss, R. S., P. E. Swanson, C. M. Knudson, K. C. Chang, J. P. Cobb, D. F. Osborne, K. M. Zollner, T. G. Buchman, S. J. Korsmeyer, and I. E. Karl. 1999. Overexpression of Bcl-2 in transgenic mice decreases apoptosis and improves survival in sepsis. J. Immunol. 162:4148.
21. Hotchkiss, R. S., K. W. Tinsley, J. Hui, K. C. Chang, P. E. Swanson, J. P. Cobb, A. M. Drewry, T. G. Buchman, and I. E. Karl. 2000. p53-dependent and -independent pathways of apoptotic cell death in sepsis. J. Immunol. 164:3675.
22. Paul, W. E. Fundamental Immunology, 4th Ed. 1999. Lippincott-Raven Press, Philadelphia, p. 183.
23. Janeway, C. A., P. Travers, M. Walport, and J. D. Capra. 1999. Immunobiology: the Immune System in Health and Disease, 4th Ed. Current Biology Publications, London, p. 219.
24. Voll, R. E., M. Herrmann, E. A. Roth, C. Stach, J. R. Kalden, and I. Girkontaite. 1997. Immunosuppressive effects of apoptotic cells. Nature 390:350.
25. Barker, R. M., L-P. Erwig, W. P. Pearce, and A. Devine. 2000. Differential effects of necrotic or apoptotic cell uptake on antigen presentation by macrophages. Pathobiology 67:302.
26. Fadok, V. A., D. L. Bratton, D. M. Rose, A. Pearson, R. A. B. Ezekewitz, and P. M. Henson. 2000. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85.
27. Ayala, A., C. Herndon, D. Lehman, C.M. DeMaso, C. A. Ayala, and I. H. Chaudry. 1995. The induction of accelerated thymic programmed cell death during polymicrobial sepsis: control by corticosteroids but not tumor necrosis factor. Shock 3:259.
28. Braun, J. S., R. Novak, K.-H. Herzog, S. M. Bodner, J. L. Cleveland, and E. I. Tuomanen. 1999. Neuroprotection by a caspase inhibitor in acute bacterial meningitis. Nat. Med. 5:298.
29. Chung, C., X. X. Ying, W. Wang, I. H. Chaudry, and A. Ayala. 1998. Is Fas ligand or endotoxin responsible for mucosal lymphocyte apoptosis in sepsis? Arch. Surg. 133:1213.
30. Hotchkiss, R. S., K. C. Chang, P. E. Swanson, K. W. Tinsley, J. J. Hui, P. Klender, S. Xanthoudakis, S. Roy, C. Black, E. Grimm, R., et al. 2000. Caspase inhibitors improve survival in sepsis: a critical role of the lymphocyte. Nat. Immunol. 1:496.
31. Grobmeyer, S. R., R. C. Armstrong, S. C. Nicholson, C. Gabay, W. P. Arend, S. H. Potter, M. Melchior, L. C. Fritz, and C. F. Nathan. 1999. Peptidomimetic fluoromethylketone rescues mice from lethal endotoxic shock. Mol. Med. 5:585.
32. Coopersmith, C. M., D. O'Donnell, and J. I. Gordon. 1999. Bcl-2 inhibits ischemia-reperfusion-induced apoptosis in the intestinal epithelium of transgenic mice. Am. J. Physiol. 276:G677.
33. Black, S. C., J. Q. Huang, P. Rezaiefar, S. Radinovic, A. Eberhart, D. W. Nicholson, and I. W. Rodger. 1998. Co-localization of the cysteine protease caspase-3 with apoptotic myocytes after in vivo myocardial ischemia and reperfusion in the rat. J. Mol. Cell. Cardiol. 30:733.
34. Schumer, M., M. C. Colombel, I. S. Sawczuk, G. Gobe, J. Connor, K. M. O'Toole, C. A. Olsson, G. J. Wise, and R. Buttyan. 1992. Morphologic, biochemical, and molecular evidence of apoptosis during the reperfusion phase after brief periods of renal ischemia. Am. J. Pathol. 140:831.
35. Martinou, J.-C., M. Dubois-Dauphin, J. K. Staple, I. Rodriguez, H. Frankowski, M. Missotten, P. Albetini, D. Talabot, S. Catsicas, C. Pietra, et al. 1994. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017.
36. Kuwano, K., and N. Hara. 2000. Signal transduction pathways of apoptosis and inflammation induced by the tumor necrosis factor receptor family. Am. J. Respir. Cell Mol. Biol. 22:147
37. Oberholzer, A., C. Oberholzer, and L. L. Moldawer. 2000. Cytokine signaling: regulation of the immune response in normal and critically ill states. Crit. Care Med. Suppl. 28:N3.
38. Lederer, J. A., M. L. Roderick, and J. A. Mannick. 1999. The effects of injury on the adaptive immune response. Shock 11:153.
39. Pellegrini, J. D., A. K. De, K. Kodys, J. C. Puyana, R. K. Furse, and C. Miller-Graziano. 2000. Relationships between T lymphocyte apoptosis and anergy following trauma. J. Surg. Res. 88:200.
40. Wichmann, M. W., A. Ayala, and I. H. Chaudry. 1998. Severe depression of host immune functions following closed-bone fracture, soft-tissue trauma, and hemorrhagic shock. Crit. Care Med. 26:1372.
41. Puyana, J. C., J. D. Pellegrini, A. K. De, K. Kodys, W. E. Silva, and C. L. Miller. 1998. Both T-helper-1 and T-helper-2 type lymphokines are depressed in post-trauma anergy. J. Trauma 44:1037.
42. Lyons, A., J. L. Kelly, M. L. Rodrick, J. A. Mannick, and J. A. Lederer. 1997. Major injury induces increased production of interleukin-10 by cells of the immune system with a negative impact on resistance to infection. Ann. Surg. 226: 450.
43. Grassme, H., S. Kirschnek, J. Riethmueller, A. Riehle, G. von Kurthy, F. Lang, M. Weller, and E. Gulbins. 2000. CD95/CD95 ligand interactions on epithelial cells in host defense to Pseudomonas aeruginosa. Science 290:527.