Chapter 4 : Mechanisms for Establishing Persistence: Immune Modulation

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Mechanisms for Establishing Persistence: Immune Modulation, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818104/9781555811594_Chap04-1.gif /docserver/preview/fulltext/10.1128/9781555818104/9781555811594_Chap04-2.gif


This chapter examines the increasingly common scenarios in which bacteria actively modulate the immune response to ensure their persistence. The mechanisms of protection against infectious agents may be divided into two complementary components: innate, or natural, immunity and specific, or acquired, immunity. It is important to mention that nonprotein antigens, such as microbial (particularly mycobacterial) lipid and glycolipid antigens, can be presented to T cells in a restricted fashion by nonclassical major histocompatibility complex (MHC) molecules, such as CD1, that are differentially expressed on antigen-presenting cells (APC) and cells of the gastrointestinal epithelium. Inhibition of mitogen-induced lymphocyte proliferation by whole live bacteria, soluble or particulate preparations of the bacteria, and sometimes purified molecules is arguably the most common observation in the literature concerning inhibition of the host's immune response. The induction of apoptosis in monocytes/macrophages has been shown to be triggered by a number of bacteria or purified bacterial products in vivo, as well as in vitro in primary and short-term cultures. Through an in-depth examination of the mechanisms used by the microbial adversaries to evade or otherwise subvert the host's immune response, we may be able to devise more effective live vaccines and develop novel therapeutic strategies for the treatment of persistent infections, as well as to discover valuable immunomodulatory agents.

Citation: Samandari T, Levine M, Sztein M. 2000. Mechanisms for Establishing Persistence: Immune Modulation, p 53-78. In Nataro J, Blaser M, Cunningham-Rundles S (ed), Persistent Bacterial Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818104.ch4
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Alder, J. D.,, L. Friess,, M. Tengowski,, and R. F. Schell. 1990. Phagocytosis of opsonized Treponema pallidum subsp. pallidum proceeds slowly. Infect. Immun. 58: 1167 1173.
2. al-Ramadi, B. K.,, Y. W. Chen,, J. J. J. Meissler,, and T. K. Eisenstein. 1991. Immunosuppression induced by attenuated Salmonella. Reversal by IL-4. J. Immunol. 147: 1954 1961.
3. al-Ramadi, B. K.,, J. J. J. Meissler,, D. Huang,, and T. K. Eisenstein. 1992. Immunosuppression induced by nitric oxide and its inhibition by interleukin-4. Eur. J. Immunol. 22: 2249 2254.
4. Andersson, K.,, N. Carballeira,, K. E. Magnusson,, C. Persson,, O. Stendahl,, H. Wolf- Watz,, and M. Fallman. 1996. YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol. Microbiol. 20: 1057 1069.
5. Baker, P. J.,, T. Hraba,, C. E. Taylor,, P. W. Stashak,, M. B. Fauntleroy,, U. Zahringer,, K. Takayama,, T. R. Sievert,, X. Hronowski,, and R. J. Cotter. 1994. Molecular structures that influence the immunomodulatory properties of the lipid A and inner core region oligosaccharides of bacterial lipopolysaccharides. Infect. Immun. 62: 2257 2269.
6. Balcewicz-Sablinska, M. K.,, J. Keane,, H. Kornfeld,, and H. G. Remold. 1998. Pathogenie Mycobacterium tuberculosis evades apoptosis of host macrophages by release o f TNFR2, resulting in inactivation of TNF-alpha. J. Immunol. 161: 2636 2641.
7. Baran, J.,, K. Guzik,, W. Hryniewicz,, M. Ernst,, H. D. Flad,, and J. Pryjma. 1996. Apoptosis of monocytes and prolonged survival of granulocytes as a result of phagocytosis of bacteria. Infect. Immun. 64: 4242 4248.
8. Beuscher, H. U.,, F. Rodel,, A. Forsberg,, and M. Rollinghoff. 1995. Bacterial evasion of host immune defense: Yersinia enterocolitica encodes a suppressor for tumor necrosis factor alpha expression. Infect. Immun. 63: 1270 1277.
9. Bignold, L. P.,, S. D. Rogers,, T. M. Siaw,, and J. Bahnisch. 1991. Inhibition of chemotaxis of neutrophil leukocytes to interleukin-8 by endotoxins of various bacteria. Infect. Immun. 59: 4255 4258.
10. Bjerknes, R.,, H. K. Guttormsen,, C. O. Solberg,, and L. M. Wetzler. 1995. Neisserial porins inhibit human neutrophil actin polymerization, degranulation, opsonin receptor expression, and phagocytosis but prime the neutrophils to increase their oxidative burst. Infect. Immun. 63: 160 167.
11. Blackwood, L. L.,, T. Lin,, and J. I. Rowe. 1987. Suppression of the delayed-type hypersensitivity and cell-mediated immune responses to Listeria monocytogenes induced by Pseudomonas aeruginosa. Infect. Immun. 55: 639 644.
12. Bodger, K.,, J. I. Wyatt,, and R. V. Heatley. 1997. Gastric mucosal secretion of interleukin-10: relations to histopathology, Helicobacter pylori status, and tumour necrosis factor-alpha secretion. Gut 40: 739 744.
13. Boland, A.,, and G. R. Cornells. 1998. Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect. Immun. 66: 1878 1884.
14. Boschwitz, J. S.,, J. W. Batanghari,, H. Kedem,, and D. A. Relman. 1997. Bordetella pertussis infection of human monocytes inhibits antigen-dependent CD4 T cell proliferation. J. Infect. Dis. 176: 678 686.
15. Braun, M. C.,, J. H e,, C. Y. Wu,, and B. L. Kelsall. 1999. Cholera toxin suppresses interleukin (IL)-12 production and IL-12 receptor betal and beta2 chain expression. J. Exp. Med. 189: 541 552.
16. Brown, M. C.,, and S. M. Taffet. 1995. Lipoarabinomannans derived from different strains of Mycobacterium tuberculosis differentially stimulate the activation of NF-KB and KBF1 in murine macrophages. Infect. Immun. 63: 1960 1968.
17. Bukholm, G.,, G. Kapperud,, and M. Skurnik. 1990. Genetic evidence that the yop A gene-encoded Yersinia outer membrane protein Yopl mediates inhibition of the anti-invasive effect of interferon. Infect. Immun. 58: 2245 2251.
18. Castro, A.,, V. Bemer,, A. Nobrega,, A. Coutinho,, and P. TrufTa-Bachi. 1998. Administration to mouse of endotoxin from gram-negative bacteria leads to activation and apoptosis of T lymphocytes. Eur. J. Immunol. 28: 488 495.
19. Chiao, J. W.,, C. Pavia,, M. Riley,, W. Altmann- Lasekan,, M. Abolhassani,, K. Liegner,, and A. Mittelman. 1994. Antigens of Lyme disease of spirochaete Borrelia burgdorferi inhibits antigen or mitogen-induced lymphocyte proliferation. FEMS Immunol. Med. Microbiol. 8: 151 155.
20. Chmiela, M.,, J. A. Lelwala-Guruge,, T. Wadstrom,, and W. Rudnicka. 1996. The stimulation and inhibition of T cell proliferation by Helicobacter pylori components. J. Physiol. Pharmacol. 47: 195 202.
21. Chmiela, M.,, B. Paziak-Domanska,, A. Ljungh,, T. Wadstrom,, and W. Rudnicka. 1996. The proliferation of human T lymphocytes stimulated by Helicobacter pylori antigens. Immunobiology 195: 199 208.
22. Clemens, D. L.,, and M. A. Horwitz. 1993. Hypoexpression of major histocompatibility complex molecules on Legionella pneumophila phagosomes and phagolysosomes. Infect. Immun. 61: 2803 2812.
23. Cole, B. C.,, and D. J. Wells. 1990. Immunosuppressive properties of the Mycoplasma arthritidis T-cell mitogen in vivo: inhibition of proliferative responses to T-cell mitogens. Infect. Immun. 58: 228 236.
24. Damle, N. K.,, G. Leytze,, K. Klussman,, and J. A. Ledbetter. 1993. Activation with superantigens induces programmed death in antigenprimed CD4 + class II -h major histocompatibility complex T lymphocytes via a CD1 l a / CD 18-dependent mechanism. Eur. J. Immunol. 23: 1513 1522.
25. Darji, A.,, B. Stockinger,, J. Wehland,, T. Chakraborty,, and S. Weiss. 1997. Antigenspecific T cell receptor antagonism by antigenpresenting cells treated with the hemolysin of Listeria monocytogenes: a novel type of immune escape. Eur. J. Immunol. 27: 1696 1703.
26. Darwin, P. E.,, M. B. Sztein,, Q. X. Zheng,, S. P. James,, and G. T. Fantry. 1996. Immune evasion by Helicobacter pylori: gastric spiral bacteria lack surface immunoglobulin deposition and reactivity with homologous antibodies. Helicobacter 1: 20 27.
27. Demuth, A.,, W. Goebel,, H. U. Beuscher,, and M. Kuhn. 1996. Differential regulation of cytokine and cytokine receptor m R N A expression upon infection of bone marrow-derived macrophages with Listeria monocytogenes. Infect. Immun. 64: 3475 3483.
28. D'Souza, C. D.,, A. M. Cooper,, A. A. Frank,, R. J. Mazzaccaro,, B. R. Bloom,, and I. M. Orme. 1997. An anti-inflammatory role for gamma delta T lymphocytes in acquired immunity to Mycobacterium tuberculosis. J. Immunol. 158: 1217 1221.
29. Durrbaum-Landmann, I.,, J. Gercken,, H. D. Flad,, and M. Ernst. 1996. Effect of in vitro infection of human monocytes with low numbers of Mycobacterium tuberculosis bacteria on monocyte apoptosis. Infect. Immun. 64: 5384 5389.
30. Eftimiadi, C.,, P. Stashenko,, M. Tonetti,, P. E. Mangiante,, R. Massara,, S. Zupo,, and M. Ferrarini. 1991. Divergent effect of the anaerobic bacteria by-product butyric acid on the immune response: suppression of T-lymphocyte proliferation and stimulation of interleukin-1 beta production. Oral Microbiol. Immunol. 6: 17 23.
31. Eftimiadi, C.,, S. Valente,, S. Mangiante,, and M. Ferrarini. 1995. Butyric acid, a metabolic end product of anaerobic bacteria, inhibits B-lymphocyte function. Minerva Stomatol. 44: 445 447.
32. Eriks, I. S.,, and C. L. Emerson. 1997. Temporal effect of tumor necrosis factor alpha on murine macrophages infected with Mycobacterium avium. Infect. Immun. 65: 2100 2106.
33. Fratazzi, C.,, R. D. Arbeit,, C. Carini,, and H. G. Remold. 1997. Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J. Immunol. 158: 4320 4327.
34. Frisch, M.,, G. Gradehandt,, and P. F. Muhlradt. 1996. Mycoplasma fermentans-derived lipid inhibits class II major histocompatibility complex expression without mediation by interleukin-6, interleukin-10, tumor necrosis factor, transforming growth factor-beta, type I interferon, prostaglandins or nitric oxide. Eur. J. Immunol. 26: 1050 1057.
35. Fumarola, D.,, S. Pece,, R. Fumarulo,, R. Petruzzelli,, B. Greco,, G. Giuliani,, A. B. Maffione,, and E. Jirillo. 1994. Downregulation of human polymorphonuclear cell activities exerted by microorganisms belonging to the alpha-2 subgroup of Proteobacteria (Aftpia felis and Rochalimaea henselae). Immunopharmacol. Immunotoxicol. 16: 449 461.
36. Goosney, D. L.,, J. Celli,, B. Kenny,, and B. B. Finlay. 1999. Enteropathogenic Escherichia coli inhibits phagocytosis. Infect. Immun. 67: 490 495.
37. Granowitz, E. V.,, R. Porat,, J. W. Mier,, S. F. Orencole,, G. Kaplanski,, E. A. Lynch,, K. Ye,, E. Vannier,, S. M. Wolff,, and C. A. D inarello. 1993. Intravenous endotoxin suppresses the cytokine response of peripheral blood mononuclear cells of healthy humans. J. Immunol. 151: 1637 1645.
38. Gregory, S. H.,, E. J. Wing,, R. A. Hoffinan,, and R. L. Simmons. 1993. Reactive nitrogen intermediates suppress the primary immunologic response to Listeria. J. Immunol. 150: 2901 2909.
39. Gueirard, P.,, A. Druilhe,, M. Pretolani,, and N. Guiso. 1998. Role of adenylate cyclase-hemolysin in alveolar macrophage apoptosis during Bordetella pertussis infection in vivo. Infect. Immun. 66: 1718 1725.
40. Guichon, A.,, and A. Zychlinsky. 1997. Clinical isolates of Shigella species induce apoptosis in macrophages. J. Infect. Dis. 175: 470 473.
41. Guzman, C. A.,, E. Domann,, M. Rohde,, D. Bruder,, A. Darji,, S. Weiss,, J. Wehland,, T. Chakraborty,, and K. N. Timmis. 1996. Apoptosis of mouse dendritic cells is triggered by listeriolysin, the major virulence determinant of Listeria monocytogenes. Mol. Microbiol. 20: 119 126.
42. Hage-Chahine, C. M.,, G. Del Giudice,, P. H. Lambert,, and J. C. Pechere. 1992. Hemolysinproducing Listeria monocytogenes affects the immune response to T-cell-dependent and T-cellindependent antigens. Infect. Immun. 60: 1415 1421.
43. Hauf, N.,, W. Goebel,, F. Fiedler,, Z. Sokolovic,, and M. Kuhn. 1997. Listeria monocytogenes infection of P388D1 macrophages results in a biphasic NF-kappaB (RelA/p50) activation induced by lipoteichoic acid and bacterial phospholipases and mediated by IkappaBalpha and IkappaBbeta degradation. Proc. Natl. Acad. Sci. USA 94: 9394 9399.
44. Hayashi, T.,, A. Catanzaro,, and S. P. Rao. 1997. Apoptosis o f human monocytes and macrophages by Mycobacterium avium sonicate. Infect. Immun. 65: 5262 5271.
45. Henderson, B.,, M. Wilson,, and B. Wren. 1997. Are bacterial exotoxins cytokine network regulators? Trends. Microbiol. 5: 454 458.
46. Hersh, D.,, D. M. Monack,, M. R. Smith,, N. Ghori,, S. Falkow,, and A. Zychlinsky. 1999. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. USA 96: 2396 2401.
47. Herzenberg, L. A.,, D. M. Weir,, and C. Blackwell. 1996. Weir's Handbook of Experimental Immunology. Blackwell Science, Inc., Cambridge, Mass.
48. Hilbi, H.,, Y. Chen,, K. Thirumalai,, and A. Zychlinsky. 1997. The interleukinip-converting enzyme, caspase 1, is activated during Shigella flexneri-induced apoptosis in human monocytederived macrophages. Infect. Immun. 65: 5165 5170.
49. Hiltbold, E. M.,, and H. K. Ziegler. 1996. Interferon- gamma and interleukin-10 have crossregulatory roles in modulating the class I and class II MHC-mediated presentation of epitopes of Listeria monocytogenes by infected macrophages. J. Interferon Cytokine Res. 16: 547 554.
50. Hofer, M. F.,, K. Newell,, R. C. Duke,, P. M. Schlievert,, J. H. Freed,, and D. Y. Leung. 1996. Differential effects of staphylococcal toxic shock syndrome toxin-1 on B cell apoptosis. Proc. Natl. Acad. Sci. USA 93: 5425 5430.
51. Holt, P. S.,, and M. L. Misfeldt. 1984. Alteration o f murine immune response by Pseudomonas aeruginosa exotoxin A. Infect. Immun. 45: 227 233.
52. Holt, P. S.,, and M. L. Misfeldt. 1986. Variables which affect suppression of the immune response induced by Pseudomonas aeruginosa exotoxin A. Infect. Immun. 52: 96 100.
53. Huang, D.,, M. G. Schwacha,, and T. K. Eisenstein. 1996. Attenuated Salmonella vaccineinduced suppression of murine spleen cell responses to mitogen is mediated by macrophage nitric oxide: quantitative aspects. Infect. Immun. 64: 3786 3792.
53a. Hughes, H. P.,, M. Campos,, L. McDougall,, T. K. Beskorwayne,, A. A. Potter,, and L. A. Babiuk. 1994. Regulation o f major histocompatibility complex class II expression by Pasteurella haemolytica leukotoxin. Infect. Immun. 62: 1609 1615.
54. Hutchison, M. L.,, I. R. Poxton,, and J. R. Govan. 1998. Burkholderia cepacia produces a hemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect. Immun. 66: 2033 2039.
55. Isogai, E.,, H. Isogal,, K. Kimura,, N. Fujii,, S. Takagi,, K. Hirose,, and M. Hayashi. 1996. In vivo induction o f apoptosis and immune responses in mice by administration of lipopolysaccharide from Porphyromonas gingivalis. Infect. Immun. 64: 1461 1466.
56. Issekutz, T. B.,, and J. M. Stoltz. 1985. Suppression of lymphocyte proliferation by Pseudomonas aeruginosa: mediation by Pseudomonas-zctivated suppressor monocytes. Infect. Immun. 48: 832 838 .
57. Janeway, C. A.,, P. Travers,, M. Walport,, and J. D. Capra. 1999. Immunobiology: the Immune System in Health and Disease. Elsevier Science, Ltd., London, United Kingdom.
58. Kaplan, G.,, R. R. Gandhi,, D. E. Weinstein,, W. R. Levis,, M. E. Patarroyo,, P. J. Brennan,, and Z. A. Cohn. 1987. Mycobacterium leprae antigen- induced suppression of T cell proliferation in vitro. J. Immunol. 138: 3028 3034.
59. Kasuya, S.,, I. Nagano,, T. Ikeda,, C. Goto,, K. Shimokawa,, and Y. Takahashi. 1996. Apoptosis of lymphocytes in mice induced by infection with Rickettsia tsutsugamushi. Infect. Immun. 64: 3937 3941.
60. Kato, S.,, M. Muro,, S. Akifusa,, N. Hanada,, I. Semba,, T. Fujii,, Y. Kowashi,, and T. Nishihara. 1995. Evidence for apoptosis of murine macrophages by Actinobacillus actinomycetemcomitans infection. Infect. Immun. 63: 3914 3919.
61. Keane, J.,, M. K. Balcewicz-Sablinska,, H. G. Remold,, G. L. Chupp,, B. B. Meek,, M. J. Fenton,, and H. Kornfeld. 1997. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect. Immun. 65: 298 304.
62. Khelef, N.,, A. Zychlinsky,, and N. Guiso. 1993. Bordetella pertussis induces apoptosis in macrophages: role o f adenylate cyclase-hemolysin. Infect. Immun. 61: 4064 4071.
63. Kim, J. M.,, L. Eckmann,, T. C. Savidge,, D. C. Lowe,, T. Witthoft,, and M. F. Kagnoflf. 1998. Apoptosis of human intestinal epithelial cells after bacterial invasion. J. Clin. Investig. 102: 1815 1823.
64. Klapproth, J. M.,, M. S. Donnenberg,, J. M. Abraham,, and S. P. James. 1996. Products of enteropathogenic E. coli inhibit lymphokine production by gastrointestinal lymphocytes. Am. J. Physiol. 271: G841 G848.
65. Klapproth, J. M.,, M. S. Donnenberg,, J. M. Abraham,, H. L. Mobley,, and S. P. James. 1995. Products of enteropathogenic Escherichia coli inhibit lymphocyte activation and lymphokine production. Infect. Immun. 63: 2248 2254.
66. Knipp, U.,, S. Birkholz,, W. Kaup,, K. Mahnke,, and W. Opferkuch. 1994. Suppression of human mononuclear cell response by Helicobacter pylori: effects on isolated monocytes and lymphocytes. FEMS Immunol. Med. Microbiol. 8: 157 166.
67. Knipp, U.,, S. Birkholz,, W. Kaup,, and W. Opferkuch. 1996. Partial characterization of a cell proHferation-inhibiting protein produced by Helicobacter pylori. Infect. Immun. 64: 3491 3496.
68. Konig, B.,, and W. Konig. 1993. Induction and suppression of cytokine release (tumour necrosis factor-alpha; interleukin-6, interleukin-1 beta) by Escherichia coli pathogenicity factors (adhesins, alpha-haemolysin). Immunology 78: 526 533.
69. Korostoff, J.,, J. F. Wang,, I. Kieba,, M. Miller,, B.J. Shenker,, and E. T. Lally. 1998. Actinobacillus actinomycetemcomitans leukotoxin induces apoptosis in HL-60 cells. Infect. Immun. 66: 4474 4483.
70. Koster, F. T.,, J. C. Williams,, and J. S. Goodwin. 1985. Cellular immunity in Q fever: modulation of responsiveness by a suppressor T cellmonocyte circuit. J. Immunol. 135: 1067 1072.
71. Kremer, L.,, J. Estaquier,, E. Brandt,, J. C. Ameisen,, and C. Locht. 1997. Mycobacterium bovis Bacillus Calmette Guerin infection prevents apoptosis of resting human monocytes. Eur. J. Immunol 27: 2450 2456.
72. Kuhn, M.,, and W. Goebel. 1998. Host cell signalling during Listeria monocytogenes infection. Trends Microbiol. 6: 11 15.
73. Kuo, C. F.,, J. J. Wu,, P. J. Tsai,, F. J. Kao,, H. Y. Lei,, M. T. Lin,, and Y. S. Lin. 1999. Streptococcal pyrogenic exotoxin B induces apoptosis and reduces phagocytic activity in U937 cells. Inject. Immun. 67: 126 130.
74. Kurita-Ochiai, T.,, K. Fukushima,, and K. Ochiai. 1997. Butyric acid-induced apoptosis of murine thymocytes, splenic T cells, and human Jurkat T cells. Infect. Immun. 65: 35 41.
75. Ladel, C. H.,, C. Blum,, A. Dreher,, K. Reifenberg,, and S. H. Kaufmann. 1995. Protective role of gamma/delta T cells and alpha/beta T cells in tuberculosis. Eur. J. Immunol 25: 2877 2881. (Erratum, 25: 3525.)
76. Laffineur, E.,, N. Genetet,, and J. Leonil. 1996. Immunomodulatory activity of beta-casein permeate medium fermented by lactic acid bacteria. J. Dairy. Sci. 79: 2112 2120.
77. Lagowska-Zlotorzycka, M.,, A. Czarny,, and M. Mulczyk. 1987. Effect of slime extract from Pseudomonas aeruginosa on cell mediated immunity induced in mice by Salmonella typhimurium. Arch. Immunol. Titer. Exp. 35: 277 281.
78. Lee, E. H.,, and Y. Rikihisa. 1996. Absence of tumor necrosis factor alpha, interleukin-6 (IL-6), and granulocyte-macrophage colony-stimulating factor expression but presence of IL-1 p, IL-8, and IL-10 expression in human monocytes exposed to viable or killed Ehrlichia chaffeensis. Infect. Immun. 64: 4211 4219.
79. Lee, W. T.,, and E. S. Vitetta. 1992. Memory T cells are anergic to the superantigen staphylococcal enterotoxin B. J. Exp. Med. 176: 575 579.
80. Levitt, D.,, and R. Corlett. 1988. Patterns of immunoenhancement and suppression induced by Chlamydia trachomatis in vivo and in vitro. J. Immunol 140: 273 276.
81. Li, B.,, H. Bassiri,, M. D. Rossman,, P. Kramer,, A. F. Eyuboglu,, M. Torres,, E. Sada,, T. Imir,, and S. R. Carding. 1998. Involvement of the Fas/Fas ligand pathway in activation-induced cell death of mycobacteria-reactive human gamma delta T cells: a mechanism for the loss of gamma delta T cells in patients with pulmonary tuberculosis. J. Immunol 161: 1558 1567.
82. Lingwood, C. A. 1996. Role of verotoxin receptors in pathogenesis. Trends Microbiol 4: 147 153.
83. Luo, G.,, D. W. Niesel,, R. A. Shaban,, E. A. Grimm,, and G. R. Klimpel. 1993. Tumor necrosis factor alpha binding to bacteria: evidence for a high-affinity receptor and alteration ofbacterial virulence properties. Infect. Immun. 61: 830 835.
84. MacFarlane, A. S.,, D. Huang,, M. G. Schwacha,, J. J. J. Meissler,, J. P. Gaughan,, and T. K. Eisenstein. 1998. Nitric oxide mediates immunosuppression induced by Listeria monocytogenes infection: quantitative studies. Microb. Pathog. 25: 267 277.
85. Mahida, Y. R.,, A. Galvin,, S. Makh,, S. H yde,, L. Sanfilippo,, S. P. Bordello,, and H. F. Sewell. 1998. Effect of Clostridium difficile toxin A on human colonic lamina propria cells: early loss of macrophages followed by T-cell apoptosis. Infect. Immun. 66: 5462 5469.
86. Manfredi, A. A.,, S. Heltai,, P. Rovere,, C. Sciorati,, C. Paolucci,, G. Galati,, C. Rugarli,, R. Vaiani,, E. Clementi,, and M. Ferrarini. 1998. Mycobacterium tuberculosis exploits the CD95/CD95 ligand system of gammadelta T cells to cause apoptosis. Eur. J. Immunol 28: 1798 1806.
87. Mangan, D. F.,, S. M. Wahl,, B. M. Sultzer,, and S. E. Mergenhagen. 1992. Stimulation of human monocytes by endotoxin -associated protein: inhibition of programmed cell death (apoptosis) and potential significance in adjuvanticity. Infect. Immun. 60: 1684 1686.
88. Marshall, J. C.,, N. V. Christou,, and J. L. Meakins. 1988. Immunomodulation by altered gastrointestinal tract flora. The effects of orally administered, killed Staphylococcus epidermidis, Candida, and Pseudomonas on systemic immune responses. Arch. Surg. 123: 1465 1469.
89. Matsui, K. 1996. Purification of a product from Salmonella typhimurium with the ability to inhibit mitogen-induced proliferation of murine splenic T-lymphocytes. FEMS Immunol Med. Microbiol 13: 155 160.
90. Matsui, K. 1996. Purified protein from Salmonella typhimurium inhibits the interleukin-2 response of murine splenic T-lymphocytes activated with anti-CD3 antibody. Microbiol Immunol 40: 681 684 .
91. Mehra, V.,, P. J. Brennan,, E. Rada,, J. Convit,, and B. R. Bloom. 1984. Lymphocyte suppression in leprosy induced by unique M. leprae glycolipid. Nature 308: 194 196.
92. Merien, F.,, G. Baranton,, and P. Perolat. 1997. Invasion of Vero cells and induction of apoptosis in macrophages by pathogenic Leptospira interrogans are correlated with virulence. Infect. Immun. 65: 729 738.
93. Mills, S. D.,, A. Boland,, M. P. Sory,, P. van der Smissen,, C. Kerbourch,, B. B. Finlay,, and G. R. Cornells. 1997. Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc. Natl. Acad. Sci. USA 94: 12638 12643.
94. Mims, C. A.,, N. J. Dimmock,, A. Nash,, and J. Stephen. 1995. Mints' Pathogenesis of Infectious Disease. Academic Press, Ltd., London, United Kingdom.
95. Mintz, C. S.,, R. D. Miller,, N. S. Gutgsell,, and T. Malek. 1993. Legionella pneumophila protease inactivates interleukin-2 and cleaves CD4 on human T cells. Infect. Immun. 61: 3416 3421.
96. Modlin, R. L.,, C. Pirmez,, F. M. Hofman,, V. Torigian,, K. Uyemura,, T. H. Rea,, B. R. Bloom,, and M. B. Brenner. 1989. Lymphocytes bearing antigen-specific gamma delta Tcell receptors accumulate in human infectious disease lesions. Nature 339: 544 548.
97. Molloy, A.,, P. Laochumroonvorapong,, and G. Kaplan. 1994. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J. Exp. Med. 180: 1499 1509.
98. Monack, D. M.,, J. Mecsas,, D. Bouley,, and S. Falkow. 1998. Yersm/d-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J. Exp. Med. 188: 2127 2137.
99. Monack, D. M.,, B. Raupach,, A. E. Hromockyj,, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93: 9833 9838.
100. Muller, A.,, J. Hacker,, and B. C. Brand. 1996. Evidence for apoptosis of human macrophage- like HL-60 cells by Legionella pneumophila infection. Infect. Immun. 64: 4900 4906.
101. Muraille, E.,, T. De Smedt,, F. Andris,, B. Pajak,, M. Armant,, J. Urbain,, M. Moser,, and O. Leo. 1997. Staphylococcal enterotoxinB induces an early and transient state of immunosuppression characterized by V beta-unrestricted T cell unresponsiveness and defective antigen-presenting cell functions. J. Immunol. 158: 2638 2647.
102. Murray, P. J.,, L. Wang,, C. Onufiyk,, R. I. Tepper,, and R. A. Young. 1997. T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J. Immunol. 158: 315 321.
103. Nakajima, R.,, and R. R. Brubaker. 1993. Association between virulence of Yersinia pestis and suppression of gamma interferon and tumor necrosis factor alpha. Infect. Immun. 61: 23 31.
104. Noble, A.,, G. A. Pestano,, and H. Cantor. 1998. Suppression of immune responses by CD8 cells. I. Superantigen-activated CD8 cells induce unidirectional Fas-mediated apoptosis of antigen- activated CD4 cells. J. Immunol. 160: 559 565 .
105. Norimatsu, M.,, T. Ono,, A. Aoki,, K. Ohishi,, T. Takahashi,, G. Watanabe,, K. Taya,, S. Sasamoto,, and Y. Tamura. 1995. Lipopolysaccharide-induced apoptosis in swine lymphocytes in vivo. Infect. Immun. 63: 1122 1126.
106. Nutman, J.,, M. Berger,, P. A. Chase,, D. G. Dearborn,, K. M. Miller,, R. L. Waller,, and R. U. Sorensen. 1987. Studies on the mechanism o f T cell inhibition by the Pseudomonas aeruginosa phenazine pigment pyocyanine. J. Immunol. 138: 3481 3487.
107. Ohguchi, M.,, A. Ishisaki,, N. Okahashi,, M. Koide,, T. Koseki,, K. Yamato,, T. Noguchi,, and T. Nishihara. 1998. Actinohacillus actinomycetemcomitans toxin induces both cell cycle arrest in the G2/M phase and apoptosis. Infect. Immun. 66: 5980 5987.
108. Ojcius, D. M.,, P. Souque,, J. L. Perfettini,, and A. Dautry-Varsat. 1998. Apoptosis of epithelial cells and macrophages due to infection with the obligate intracellular pathogen Chlamydia psittaci. J. Immunol. 161: 4220 4226.
108a. Orme, I. M.,, and F. M. Collins. 1984. Immune response to atypical mycobacteria: immunocompetence of heavily infected mice measured in vivo fails to substantiate immunosuppression data obtained in vitro. Infect. Immun. 43: 32 37 .
109. Palmer, L. E.,, S. Hobbie,, J. E. Galan,, and J. B. Bliska. 1998. YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-alpha production and downregulation of the MAP kinases p38 and JNK. Mol. Microbiol. 27: 953 965.
110. Parmely, M.,, A. Gale,, M. Clabaugh,, R. Horvat,, and W. W. Zhou. 1990. Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect. Immun. 58: 3009 3014.
111. Paul, W. E. 1998. Fundamental Immunology. Lippincott- Raven, Philadelphia, Pa.
112. Petit, J. C.,, and G. L. Daguet. 1983. Interference of Pseudomonas aeruginosa with immunospecific host defenses. Biomed. Pharmacother. 37: 422 428 .
113. Pryjma, J.,, J. Baran,, M. Ernst,, M. Woloszyn,, and H. D. Flad. 1994. Altered antigenpresenting capacity of human monocytes after phagocytosis of bacteria. Infect. Immun. 62: 1961 1967.
114. Rabie, G.,, E. T. Lally,, and B. J. Shenker. 1988. Immunosuppressive properties of Actinobacillus actinomycetemcomitans leukotoxin. Infect. Immun. 56: 122 127.
115. Renno, T.,, M. Hahne,, and H. R. MacDonald. 1995. Proliferation is a prerequisite for bacterial superantigen-induced T cell apoptosis in vivo. J. Exp. Med. 181: 2283 2287.
116. Rodloff, A. C.,, P. Widera,, S. Ehlers,, T. Montag,, M. Lucas,, G. Schmidt,, and H. Hahn. 1990. Suppression of blastogenic transformation of lymphocytes by Bacteroidesfragilis in vitro and in vivo. Zentbl. Bakteriol. 274: 406 416.
117. Rosenbaum, J. T.,, K. T. Hartiala,, R. O. Webster,, E. L. J. Howes,, and I. M. Goldstein. 1983. Antiinflammatory effects of endotoxin. Inhibition of rabbit polymorphonuclear leukocyte responses to complement (C5)-derived peptides in vivo and in vitro. Am. J. Pathol. 113: 291 299.
118. Ruckdeschel, K.,, S. Harb,, A. Roggen-kamp,, M. Hornef,, R. Zumbihl,, S. Kohler,, J. Heesemann,, and B. Rouot. 1998. Yersinia enterocolitica impairs activation of transcription factor NF-kappaB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor alpha production. J. Exp. Med. 187: 1069 1079.
119. Ruckdeschel, K.,, J. Machold,, A. Roggenkamp,, S. Schubert,, J. Pierre,, R. Zumbihl,, J. P. Liautard,, J. Heesemann,, and B. Rouot. 1997. Yersinia enterocolitica promotes deactivation of macrophage mitogen-activated protein kinases extracellular signal-regulated kinase-1/2, p38, and c-Jun NH2-terminal kinase. Correlation with its inhibitory effect on tumor necrosis factor-alpha production. J. Biol. Chem. 272: 15920 15927.
120. Saha, B.,, G. Das,, H. Vohra,, N. K. Ganguly,, and G. C. Mishra. 1994. Macrophage-T cell interaction in experimental mycobacterial infection. Selective regulation of co-stimulatory molecules on Mycobacterium-infected macrophages and its implication in the suppression of cell-mediated immune response. Eur. J. Immunol. 24: 2618 2624.
120a. Satnandari, T.,, K. L. Kotloff,, G. A. Losonsky,, W. D. Picking,, M. M. Levine,, and M. B. Sztein. Production of interferon-gamma and IL-10 to Shigella invasins by mononuclear cells from volunteers orally inoculated with a Shiga toxin-deleted Shigella dysenteriae strain. J. Immun., in press.
121. Schesser, K.,, A. K. Spiik,, J. M. Dukuzu-muremyi,, M. F. Neurath,, S. Pettersson,, and H. Wolf-W atz. 1998. The yopjlocus is required for Ymm/a-mediated inhibition of NF-kappaB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol. Microbiol. 28: 1067 1079.
122. Schwacha, M. G.,, J. J. J. Meissler,, and T. K. Eisenstein. 1998. Salmonella typhimurium infection in mice induces nitric oxide-mediated immunosuppression through a natural killer celldependent pathway. Infect. Immun. 66: 5862 5866.
123. Schwan, W. R.,, and D. J. Kopecko. 1997. Uptake of pathogenic intracellular bacteria into human and murine macrophages downregulates the eukaryotic 26S protease complex ATPase gene. Infect. Immun. 65: 4754 4760.
124. Shenker, B. J.,, and J. M. DiRienzo. 1984. Suppression of human peripheral blood lymphocytes by Fusobacterium nucleatum. J. Immunol. 132: 2357 2362.
125. Shenker, B. J.,, L. Vitale,, and J. Slots. 1991. Immunosuppressive effects oiPrevotella intermedia on in vitro human lymphocyte activation. Infect. Immun. 59: 4583 4589.
126. Shenker, B. J.,, L. A. Vitale,, and D. A. Welham. 1990. Immune suppression induced by Actinobacillus actinomycetemcomitans: effects on immunoglobulin production by human B cells. Infect. Immun. 58: 3856 3862.
127. Staugas, R. E.,, D. P. Harvey,, A. Ferrante,, M. Nandoskar,, and A. C. Allison. 1992. Induction of tumor necrosis factor (TNF) and interleukin- 1 (IL-1) by Pseudomonas aeruginosa and exotoxin A-induced suppression of lymphoproliferation and TNF, lymphotoxin, gamma interferon, and IL-1 production in human leukocytes. Infect. Immun. 60: 3162 3168.
128. Stenger, S.,, K. R. Niazi,, and R. L. Modlin. 1998. Down-regulation of CD1 on antigen-presenting cells by infection with Mycobacterium tuberculosis. J. Immunol. 161: 3582 3588.
129. Stevens, P. K.,, and C. J. Czuprynski. 1996. Pasteurella haemolytica leukotoxin induces bovine leukocytes to undergo morphologic changes consistent with apoptosis in vitro. Infect. Immun. 64: 2687 2694.
130. Sztein, M. B.,, and G. F. Mitchell,. 1997. Recent advances in immunology: impact on vaccine development, p. 99 126. In M. M. Levine,, G. C. Woodrow,, J. B. Kaper,, and G. S. Cobon (ed.), New Generation Vaccines. Marcel Dekker, Inc., New York, N.Y.
131. Taylor, C. E.,, and R. Bright. 1989. T-cell modulation of the antibody response to bacterial polysaccharide antigens. Infect. Immun. 57: 180 185.
132. Thern, A.,, L. Stenberg,, B. Dahlback,, and G. Lindahl. 1995. Ig-binding surface proteins of Streptococcus pyogenes also bind human C4bbinding protein (C4BP), a regulatory component of the complement system. J. Immunol. 154: 375 386.
133. Thomson, A. 1998. The Cytokine Handbook. Academic Press, Ltd., London, United Kingdom.
134. Tomai, M. A.,, and T. J. Fitzgerald. 1991. Splenic macrophage function in early syphilitic infection is complex. Stimulation versus downregulation. J. Immunol. 146: 3171 3176.
135. Tsuyuguchi, I.,, H. Kawasumi,, T. Takashima,, T. Tsuyuguchi,, and S. Kishimoto. 1990. Mycobacterium avium-Mycobacterium intracellular complex-induced suppression of T-cell proliferation in vitro by regulation of monocyte accessory cell activity. Infect. Immun. 58: 1369 1378.
136. Tufano, M. A.,, F. Rossano,, P. Catalanotti,, G. Liguori,, A. Marinelli,, A. Baroni,, and P. Marinelli. 1994. Properties of Yersinia enterocolitica porins: interference with biological functions of phagocytes, nitric oxide production and selective cytokine release. Res. Microbiol. 145: 297 307.
137. Ulmer, A. J.,, J. Pryjma,, Z. Tarnok,, M. Ernst,, and H. D. Flad. 1990. Inhibitory and stimulatory effects o f Pseudomonas aeruginosa pyocyanine on human T and B lymphocytes and human monocytes. Infect. Immun. 58: 808 815.
138. Valisena, S.,, P. E. Varaldo,, and G. Satta. 1991. Staphylococcal endo-beta-N-acetylglucosaminidase inhibits response of human lymphocytes to mitogens and interferes with production of antibodies in mice. J. Clin. Investig. 87: 1969 1976.
139. Van Heyningen, T. K.,, H. L. Collins,, and D. G. Russell. 1997. IL-6 produced by macrophages infected with Mycobacterium species suppresses T cell responses. J. Immunol. 158: 330 337.
140. Virgin, H. W.,, G. F. Wittenberg,, G.J. Bancroft,, and E. R. Unanue. 1985. Suppression of immune response to Listeria monocytogenes: mechanism(s) of immune complex suppression. Infect. Immun. 50: 343 353.
141. Vollmer, P.,, I. Walev,, S. Rose-John,, and S. Bhakdi. 1996. Novel pathogenic mechanism of microbial metalloproteinases: liberation of membrane- anchored molecules in biologically active form exemplified by studies with the human interleukin- 6 receptor. Infect. Immun. 64: 3646 3651.
142. Wang, S. D.,, K. J. Huang,, Y. S. Lin,, and H. Y. Lei. 1994. Sepsis-induced apoptosis o f the thymocytes in mice. J. Immunol. 152: 5014 5021.
143. Watson, R. W.,, H. P. Redmond,, J. H. Wang,, C. Condron,, and D. Bouchier- Hayes. 1996. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J. Immunol. 156: 3986 3992.
144. Welkos, S.,, A. Friedlander,, D. McDowell,, J. Weeks,, and S. Tobery. 1998. V antigen of Yersinia pestis inhibits neutrophil chemotaxis. Microb. Pathog. 24: 185 196.
145. Wick, M. J.,, C. V. Harding,, N. J. Twesten,, S. J. Normark,, and J. D. Pfeifer. 1995. The phoP locus influences processing and presentation of Salmonella typhimurium antigens by activated macrophages. Mol. Microbiol. 16: 465 476.
146. Wilson, K. T.,, K. S. Ramanujam,, H. L. Mobley,, R. F. Musselman,, S. P. James,, and S.J. Meltzer. 1996. Helicobacter pylori stimulates inducible nitric oxide synthase expression and activity in a murine macrophage cell line. Gastroenterology 111: 1524 1533.
147. Wilson, M.,, R. Seymour,, and B. Henderson. 1998. Bacterial perturbation of cytokine networks. Infect. Immun. 66: 2401 2409.
148. Wyant, T. L.,, M. K. Tanner,, and M. B. Sztein. 1999. Potent immunoregulatory effects of Salmonella typhi flagella on antigenic stimulation of human peripheral blood mononuclear cells. Infect. Immun. 67: 1338 1346.
149. Zav'yalov, V. P.,, T. V. Chernovskaya,, E. V. Navolotskaya,, A. V. Karlyshev,, S. Mac- Intyre,, A. M. Vasiliev,, and V. M. Abramov. 1995. Specific high affinity binding of human interleukin 1 beta by CafLA usher protein of Yersinia pestis. FEBS Lett. 371: 65 68.
150. Zeidner, N.,, M. L. Mbow,, M. D olan,, R. Massung,, E. Baca,, and J. Piesman. 1997. Effects of Ixodes scapularis and Borrelia burgdorferi on modulation of the host immune response: induction o f a TH2 cytokine response in Lyme diseasesusceptible (C3H/HeJ) mice but not in diseaseresistant (BALB/c) mice. Infect. Immun. 65: 3100 3106.
151. Zychlinsky, A.,, M. C. Prevost,, and P. J. Sansonetti. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167 169.
152. Zychlinsky, A.,, K. Thirumalai,, J. Arondel,, J. R. Cantey,, A. O. Aliprantis,, and P. J. Sansonetti. 1996. In vivo apoptosis in Shigella flexneri infections. Infect. Immun. 64: 5357 5365.


Generic image for table

Bacterial disruption of selected immune mechanisms

Citation: Samandari T, Levine M, Sztein M. 2000. Mechanisms for Establishing Persistence: Immune Modulation, p 53-78. In Nataro J, Blaser M, Cunningham-Rundles S (ed), Persistent Bacterial Infections. ASM Press, Washington, DC. doi: 10.1128/9781555818104.ch4

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error