Sepsis induces increased apoptosis in lamina propria mononuclear cells which is associated with altered cytokine gene expression

Journal of Surgical Research

Volumn 77, Issue 1, 1998, Pages 63-70

  Chung, Chun Shiang ^a   Xu, Ying Xin ^a   Chaudry, Irshad H ^a   Ayala, Alfred ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Apoptosis; Cytokine mRNA; Intestinal lamina propria; Lymphocytes; Macrophage; Mouse; Sepsis

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 9; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DIGESTIVE SYSTEM INFLAMMATION; FLOW CYTOMETRY; GENE EXPRESSION; HELPER CELL; IMMUNE DEFICIENCY; LAMINA PROPRIA; MACROPHAGE; MALE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEPSIS;

EID: 0031928035     PISSN: 00224804     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsre.1998.5339     Document Type: Article

References (51)

1. Nichols, R. L., Smith, J. W., Klein, D. B., Trunkey, D. D., Cooper, R. H., Adinolfi, M. F., and Mills, J. Risk of infection after penetrating abdominal trauma. N. Engl. J. Med. 311: 1065, 1984.
2. Carrico, C. J., Meakins, J. L., Marshall, J. C., Fry, D., and Maier, R. V. Multiple organ failure syndrome. Arch. Surg. 121: 196, 1986.
3. Deitch, E. A., Winterton, J., Li, M., and Berg, R. The gut as a portal of entry for bacteremia. Ann. Surg. 205: 681, 1987.
4. Fink, M. P., Antonsson, J. B., Wang, H., and Rothschild, H. R. Increased intestinal permeability in endotoxic pigs. Arch. Surg. 126: 211, 1991.
5. Wells, C. L., Maddaus, M. A., and Simmons, R. L. Proposed mechanisms for the translocation of intestinal bacteria. Rev. Infect. Dis. 10: 958, 1988.
6. Sori, A. J., Rush, B. F., Lysz, T. W., Smith, S., and Machiedo, G. W. The gut as source of sepsis after hemorrhagic shock. Am. J. Surg. 155: 187, 1988.
7. Kagnoff, M. F. Immunology of the intestinal tract. Gastroenterology 105: 1275, 1993.
8. Cohen, J. J., Duke, R. C., Fadok, V. A., and Sellins, K. S. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10: 267, 1992.
9. Ayala, A., Herdon, C. D., Lehman, D. L., DeMaso, C. M., Ayala, C. A., and Chaudry, I. H. The induction of accelerated thymic programmed cell death during polymicrobial sepsis: Control by corticosteroids but not tumor necrosis factor. Shock 3: 259, 1995.
10. Brandtzaeg, P., Halstesen, T. S., Kett, K., Krajci, P., Kvvale, D., Rognum, T. O., Scott, H., and Sollid, L. M. Immunobiology and immunopathology of human gut mucosa: Humoral immunity and intraepithelial lymphocytes. Gastroenterology 97: 1562, 1989.
11. Zeitz, M., Quinn, T. C., Graeff, A. S., and James, S. P. Mucosal T cells provide helper function but do not proliferate when stimulated by specific antigen in lymphogranuloma venerum porctitis in non-human primates. Gastroenterology 94: 353, 1988.
12. Ayala, A., Herdon, C. D., Lehman, D. L., Ayala, C. A., and Chaudry, I. H. Differential induction of apoptosis in lymphoid tissues during sepsis: Variation in onset, frequency, and the nature of the mediators. Blood 87: 4261, 1996.
13. Ayala, A., Xu, Y. X., Ayala, C. A., Sonefeld, D. E., Karr, S. M., Evans, T. A., and Chaudry, I. H. Increased mucosal B-lymphocyte apoptosis during polymicrobial sepsis is a Fas ligand but not an endotoxin mediated process. Blood 91: 1362, 1998.
14. Baker, C. C., Chaudry, I. H., Gaines, H. O., and Baue, A. E. Evaluation of factors affecting mortality rate after sepsis in murine cecal ligation and puncture model. Surgery 94: 331, 1983.
15. Ayala, A., Perrin, M. M., Kisala, J. M., Ertel, W., and Chaudry, I. H. Polymicrobial sepsis selectively activates peritoneal but not alveolar macrophage to release inflammatory mediators (IL-1, IL-6 and TNF). Circ. Shock 36: 191, 1992.
16. Davies, M. D. J., and Parrott, D. M. V. Preparation and purification of lymphocytes from the epithelium and lamina propria of murine small intestine. Gut 22: 481, 1981.
17. Gorczyca, W., Tuziak, T., Kram, A., Melamed, M. R., and Darzynkiewicz, Z. Detection of apoptosis-associated DNA strand breaks in fine-needle aspiration biopsies by in situ end labeling of fragmented DNA. Cytometry 15: 169, 1994.
18. Kabelitz, D., Pohl, T., and Pechhold, K. Activation-induced cell death (apoptosis) of mature peripheral T lymphocytes. Immunol. Today 14: 338, 1993.
19. + T cells in vivo after exposure to the superantigenic lectin Urtica dioica agglutinin. J. Immunol. 154: 2600, 1995.
20. Rodgers, V. D., Fffassett, R., and Kagnoff, M. F. Abnormalities in intestinal mucosal T cells in homosexual populations including those with the lymphadenopathy syndrome and AIDS. Gastroenterology 169: 1277, 1986.
21. Weiner, H. L., Friedman, A., Miller, A., Khoury, S. J., and al-Sabbagh, A. Oral tolerance: immunologic mechanisms and treatment of animal and human organ-specific autoimmune disease by oral administration of autoantigens. Annu. Rev. Immunol. 12: 809, 1994.
22. Fryer, J., Grant, D., Jiang, J., Metrakos, P., Ozcay, N., Ford, C., Garcia, B., Behme, R., and Zhong, R. Influnce of macrophage depletion on bacterial translocation and rejection in small bowel transplantation. Transplantation 62: 553, 1996.
23. Nagashima, R., Maeda, K., Imai, Y., and Takahashi, T. Lamina propria macrophages in the human gastrointestinal mucosa: Their distribution, immunohistological phenotype, and function. J. Histochem. Cytochem. 44: 721, 1996.
24. Wang, P., Zhou, M., Rana, M. W., Ba, Z. F., and Chaudry, I. H. Differential alterations in microvascular perfusion in various organs during early and late sepsis. Am. J. Physiol. 263: G38, 1992.
25. Ayala, A., and Chaudry, I. H. Immune dysfunction in murine polymicrobial sepsis: Mediators, macrophages, lymphocytes and apoptosis. Shock 6: S27, 1996.
26. Afford, S. C., Pongracz, J., Stockley, R. A., Crocker, J., and Burnett, D. The induction by human IL-6 of apoptosis in the promonocytic cell line U937 and Human neutrophils. J. Biol. Chem. 267: 21612, 1992.
27. Liu, Z. H., and Striker, G. E. TNFa and IL-1 a induce mannose receptors and apoptosis in glomerular mesangial but not endothelial cells. Am. J. Physiol. 270 C: 1595, 1996.
28. Ayala, A., Karr, S. M., Evans, T. A., and Chaudry, I. H. Factors responsible for peritoneal granulocyte apoptosis during sepsis. J. Surg. Res. 69: 67, 1997.
29. Zhang, Y., Takahashi, K., Jiang, G., Kawai, M., Fukada, M., and Yokochi, T. In vivo induction of apoptosis (programmed cell death) in mouse thymus by administration of lipopolysaccharide. Infect. Immun. 61: 5044, 1993.
30. + T cells, modulated by cytokines and effected by lymphotoxin. AIDS 10: 603, 1996.
31. Yamamoto, M., Fujihashi, K., Amano, M., McGhee, J. R., Beagley, K. W., and Kiyono, H. Cytokine synthesis and apoptosis by intestinal intraepithelial lymphocytes: Signaling of high density ab T cell receptor+ and rd T cell receptor+ T cells via T cell receptor-CD3 complex results in interferon-r and interleukin-5 production, while low density T cells undergo DNA fragmentation. Eur. J. Immunol. 24: 1301, 1994.
32. Boirivant, M., Pica, R., DeMaria, R., Testi, R., Pallone, F., and Strober, W. Stimulated human lamina propria T cells manifest enhanced Fas-mediated apoptosis. J. Clin. Invest. 98: 2616, 1996.
33. Haendeler, J., MeBmer, U. K., Brune, B., Neugebauer, E., and Dimmeler, S. Endotoxic shock leads to apoptosis in vivo and reduces Bcl-2. Shock 6: 405, 1996.
34. Okuda, Y., Sakada, S., Shimaoka, M., and Yanagihara, T. Nitric oxide induces apoptosis in mouse splenic T lymphocytes. Immunol. Letters 52: 135, 1996.
35. Illera, V. A., Perandones, C. E., Stunz, L. L., Mower, D. A. J., and Ashman, R. F. Apoptosis in splenic B lymphocytes: Regulation by protein kinase C and IL-4. J. Immunol. 151: 2965, 1993.
36. Messmer, U. K., Reed, U. K., and Brune, B. Bcl-2 protects macrophages from nitric oxide-induced apoptosis. J. Biol. Chem. 271: 20192, 1997.
37. Albina, J. E., Cui, S., Mateo, R. B., and Reichner, J. S. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J. Immunol. 150: 5080, 1993.
38. Monack, D. M., Raupach, B., Hromockyj, A. E., and Falkow, S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93: 9833, 1996.
39. Williams, T. E., Ayala, A., and Chaudry, I. H. Inducible macrophage apoptosis following sepsis is mediated by cysteine protease activation and nitric oxide release. J. Surg. Res. 70: 113, 1997.
40. James, S. P., Kwan, W. C., and Sneller, M. C. T cells in inductive and effector compartments of the intestinal mucosal immune system of nonhuman primates differ in lymphokine mRNA expression, lymphokine utilization, and regulatory function. J. Immunol. 144: 1251, 1990.
41. Daynes, R. A., Araneo, B. A., Dowell, T. A., Huang, K., and Dudley, D. Regulation of murine lymphokine production in vivo. III. The lymphoid tissue microenvironment exerts regulatory influences over T helper cell function. J. Exp. Med. 171: 979, 1990.
42. Meeusen, E. N. T., Premier, R. R., and Brandon, M. R. Tissue-specific migration of lymphocytes: a key role for Th1 and Th2 cells? Immunol. Today 17: 421, 1996.
43. Ayala, A., Urbanich, M. A., Herdon, C. D., and Chaudry, I. H. Is sepsis-induced apoptosis associated with macrophage dysfunction? J. Trauma 40: 568, 1996.
44. Bingisser, R., Stey, C., Weller, M., Groscurth, P., Russi, E., and Frei, K. Apoptosis in human alveolar macrophages is induced by endotoxin and is modulated by cytokines. Am. J. Resp. Cell Mol. Biol. 15: 64, 1996.
45. Matthys, P., Froyen, G., Verdot, L., Huang, S., Sobis, H., Damme, J. V., Vray, B., Aguet, M., and Billiau, A. IFN-r receptor-deficient mice are hypersensitive to the anti-CD3-induced cytokine release syndrome and thymocyte apoptosis. J. Immunol. 155: 3823, 1995.
46. Jewell, A. P., Lydyard, P. M., Worman, C. P., Giles, F. J., and Goldstone, A. H. Growth factors can protect B-chronic lymphocytic leukemia cells against programmed cell death without stimulating proliferation. Leuk. Lymph. 18: 159, 1995.
47. Liu, Y., and Janeway, C. A., Jr. IFN-r plays a critical role in induced cell death of effector T cell: a possible 3rd mechanism of self-tolerance. J. Expl. Med. 172: 1735, 1990.
48. + T cells from human immunodeficiency virus-infected asymptomatic individuals. J. Exp. Med. 175: 331, 1992.
49. + T cells. J. Clin. Invest. 95: 564, 1995.
50. Cohen, J. J. Apoptosis. Immunol. Today 14: 126, 1993.
51. Grabsteinn, K. H., Eisenman, J., Shanebeck, K., Rauch, C., Srinivasan, S., Fung, V., Beers, C., Richardson, J., Schoenborn, M. A., Ahdieh, M., Johnson, L., Alderson, M. R., Watson, J. D., Anderson, D. M., and Giri, J. G. Cloning of a T cell growth factor that interacts with the b chain of the interleukin-2 receptor. Science 264: 965, 1994.