Early interferon-γ production in human lymphocyte subsets in response to nontyphoidal salmonella demonstrates inherent capacity in innate cells

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Nyirenda, Tonney S ^a,b   Seeley, Anna E ^a   Mandala, Wilson L ^b   Drayson, Mark T ^a   MacLennan, Calman A ^a,c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF MALAWI   (Malawi)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTERFERON PRODUCTION; INTRACELLULAR BACTERIUM; LYMPHOCYTE COUNT; MALE; MONOCYTE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; PERIPHERAL LYMPHOCYTE; SALMONELLA TYPHIMURIUM; T LYMPHOCYTE; BIOSYNTHESIS; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE; LYMPHOCYTE SUBPOPULATION; METABOLISM; SALMONELLA;

SALMONELLA; SALMONELLA TYPHIMURIUM;

HUMANS; IMMUNITY, INNATE; IMMUNOPHENOTYPING; INTERFERON-GAMMA; LYMPHOCYTE SUBSETS; LYMPHOCYTES; SALMONELLA;

EID: 78149423923     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013667     Document Type: Article

References (77)

1. Morpeth SC, Ramadhani HO, Crump JA (2009) Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis 49: 606-611.
2. Sigauque B, Roca A, Mandomando I, Morais L, Quinto L, et al. (2009) Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 28: 108-113.
3. MacLennan CA, Gondwe EN, Msefula CL, Kingsley RA, Thomson NR, et al. (2008) The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J Clin Invest 118: 1553-1562.
4. Gordon MA, Graham SM, Walsh AL, Wilson L, Phiri A, et al. (2008) Epidemics of invasive Salmonella enterica serovar Enteritidis and S. enterica serovar Typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 46: 963-969.
5. Kariuki S, Revathi G, Kariuki N, Kiiru J, Mwituria J, et al. (2006) Characterisation of community acquired non-typhoidal Salmonella from bacter-aemia and diarrhoeal infections in children admitted to hospital in Nairobi, Kenya. BMC Microbiol 6: 101.
6. Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, et al. (2006) Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J 25: 230-236.
7. Gordon MA, Banda HT, Gondwe M, Gordon SB, Boeree MJ, et al. (2002) Non-typhoidal Salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. AIDS 16: 1633-1641.
8. Graham SM, Molyneux EM, Walsh AL, Cheesbrough JS, Molyneux ME, et al. (2000) Nontyphoidal Salmonella infections of children in tropical Africa. Pediatr Infect Dis J 19: 1189-1196.
9. Gilks CF, Brindle RJ, Otieno LS, Simani PM, Newnham RS, et al. (1990) Life-threatening bacteraemia in HIV-1 seropositive adults admitted to hospital in Nairobi, Kenya. Lancet 336: 545-549.
10. Mtove G, Amos B, von Seidlein L, Hendriksen I, Mwambuli A, et al. (2010) Invasive salmonellosis among children admitted to a rural Tanzanian hospital and a comparison with previous studies. PLoS One 5: e9244.
11. Nadjm B, Amos B, Mtove G, Ostermann J, Chonya S, et al. (2010) WHO guidelines for antimicrobial treatment in children admitted to hospital in an area of intense Plasmodium falciparum transmission: prospective study. BMJ 340: c1350.
12. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, et al. (2009) Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 19: 2279-2287.
13. MacLennan CA, Gilchrist JJ, Gordon MA, Cunningham AF, Cobbold M, et al. (2010) Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 328: 508-512.
14. Fields PI, Swanson RV, Haidaris CG, Heffron F (1986) Mutants of Salmonella Typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A 83: 5189-5193.
15. Mouy R, Fischer A, Vilmer E, Seger R, Griscelli C (1989) Incidence, severity, and prevention of infections in chronic granulomatous disease. J Pediatr 114: 555-560.
16. Lazarus GM, Neu HC (1975) Agents responsible for infection in chronic granulomatous disease of childhood. J Pediatr 86: 415-417.
17. Gondwe EN, Molyneux ME, Goodall M, Graham SM, Mastroeni P, et al. (2010) Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. Proc Natl Acad Sci U S A in press.
18. Kagaya K, Watanabe K, Fukazawa Y (1989) Capacity of recombinant c-interferon to activate macrophages for Salmonella-killing activity. Infect Immun 57: 609-615.
19. Vazquez-Torres A, Jones-Carson J, Mastroeni P, Ischiropoulos H, Fang FC (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J Exp Med 192: 227-236.
20. Foster N, Hulme SD, Barrow PA (2003) Induction of antimicrobial pathways during early-phase immune response to Salmonella spp. in murine macrophages: c-interferon (IFNc) and upregulation of IFNc receptor alpha expression are required for NADPH phagocytic oxidase gp91-stimulated oxidative burst and control of virulent Salmonella spp. Infect Immun 71: 4733-4741.
21. Janssen R, Van Wengen A, Verhard E, De Boer T, Zomerdijk T, et al. (2002) Divergent role for TNF-a in IFN-c-induced killing of Toxoplasma gondii and Salmonella Typhimurium contributes to selective susceptibility of patients with partial IFNc receptor 1 deficiency. J Immunol 169: 3900-3907.
22. Gordon MA, Jack DL, Dockrell DH, Lee ME, Read RC (2005) c-interferon enhances internalization and early nonoxidative killing of Salmonella enterica serovar Typhimurium by human macrophages and modifies cytokine responses. Infect Immun 73: 3445-3452.
23. Jouanguy E, Doffinger R, Dupuis S, Pallier A, Altare F, et al. (1999) IL-12 and IFNc in host defense against mycobacteria and Salmonella in mice and men. Curr Opin Immunol 11: 346-351.
24. MacLennan C, Fieschi C, Lammas DA, Picard C, Dorman SE, et al. (2004) Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J Infect Dis 190: 1755-1757.
25. Bustamante J, Boisson-Dupuis S, Jouanguy E, Picard C, Puel A, et al. (2008) Novel primary immunodeficiencies revealed by the investigation of paediatric infectious diseases. Curr Opin Immunol 20: 39-48.
26. van de Vosse E, van Dissel JT, Ottenhoff TH (2009) Genetic deficiencies of innate immune signalling in human infectious disease. Lancet Infect Dis 9: 688-698.
27. Altare F, Lammas D, Revy P, Jouanguy E, Doffinger R, et al. (1998) Inherited interleukin 12 deficiency in a child with Bacille Calmette-Guerin and Salmonella Enteritidis disseminated infection. J Clin Invest 102: 2035-2040.
28. de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, et al. (1998) Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 280: 1435-1438.
29. Picard C, Fieschi C, Altare F, Al-Jumaah S, Al-Hajjar S, et al. (2002) Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds. Am J Hum Genet 70: 336-348.
30. Ezekowitz RA, Dinauer MC, Jaffe HS, Orkin SH, Newburger PE (1988) Partial correction of the phagocyte defect in patients with X-linked chronic granulomatous disease by subcutaneous interferon-c. N Engl J Med 319: 146-151.
31. + TCR-ab cells and IFNc in bacterial clearance independent of intracellular location. J Immunol 156: 3321-3326.
32. Muotiala A, Makela PH (1990) The role of IFNc in murine Salmonella Typhimurium infection. Microb Pathog 8: 135-141.
33. - Salmonella vaccines. Microb Pathog 13: 477-491.
34. Gulig PA, Doyle TJ, Clare-Salzler MJ, Maiese RL, Matsui H (1997) Systemic infection of mice by wild-type but not Spv- Salmonella Typhimurium is enhanced by neutralization of c-interferon and tumor necrosis factor-a. Infect Immun 65: 5191-5197.
35. Nauciel C, Espinasse-Maes F (1992) Role of c-interferon and tumor necrosis factor-a in resistance to Salmonella Typhimurium infection. Infect Immun 60: 450-454.
36. Mastroeni P, Harrison JA, Robinson JH, Clare S, Khan S, et al. (1998) Interleukin-12 is required for control of the growth of attenuated aromatic-compound-dependent Salmonellae in BALB/c mice: role of c-interferon and macrophage activation. Infect Immun 66: 4767-4776.
37. Ramarathinam L, Shaban RA, Niesel DW, Klimpel GR (1991) c-interferon (IFNc) production by gut-associated lymphoid tissue and spleen following oral Salmonella Typhimurium challenge. Microb Pathog 11: 347-356.
38. Matsui K, Arai T (1992) The comparison of cell-mediated immunity induced by immunization with porin, viable cells and killed cells of Salmonella Typhimurium. Microbiol Immunol 36: 269-278.
39. Thatte J, Rath S, Bal V (1993) Immunization with live versus killed Salmonella Typhimurium leads to the generation of an IFNc-dominant versus an IL-4-dominant immune response. Int Immunol 5: 1431-1436.
40. Eckmann L, Fierer J, Kagnoff MF (1996) Genetically resistant (Ityr) and susceptible (Itys) congenic mouse strains show similar cytokine responses following infection with Salmonella Dublin. J Immunol 156: 2894-2900.
41. Pie S, Truffa-Bachi P, Pla M, Nauciel C (1997) Th1 response in Salmonella Typhimurium-infected mice with a high or low rate of bacterial clearance. Infect Immun 65: 4509-4514.
42. Mizuno Y, Takada H, Nomura A, Jin CH, Hattori H, et al. (2003) Th1 and Th1-inducing cytokines in Salmonella infection. Clin Exp Immunol 131: 111-117.
43. Kedzierska K, Crowe SM (2001) Cytokines and HIV-1: interactions and clinical implications. Antivir Chem Chemother 12: 133-150.
44. Bailer RT, Holloway A, Sun J, Margolick JB, Martin M, et al. (1999) IL-13 and IFNc secretion by activated T cells in HIV-1 infection associated with viral suppression and a lack of disease progression. J Immunol 162: 7534-7542.
45. Imami N, Antonopoulos C, Hardy GA, Gazzard B, Gotch FM (1999) Assessment of type 1 and type 2 cytokines in HIV type 1-infected individuals: impact of highly active antiretroviral therapy. AIDS Res Hum Retroviruses 15: 1499-1508.
46. Clerici M, Shearer GM (1993) A TH1-.TH2 switch is a critical step in the etiology of HIV infection. Immunol Today 14: 107-111.
47. Fan J, Li P, Kok TW, Burrell CJ (1997) AZT blocks down-regulation of IL-2 and IFNc gene expression in HIV acutely infected cells. Arch Virol 142: 1035-1043.
48. Kelleher AD, Sewell WA, Cooper DA (1999) Effect of protease therapy on cytokine secretion by peripheral blood mononuclear cells (PBMC) from HIV-infected subjects. Clin Exp Immunol 115: 147-152.
49. Cunningham AF, Gaspal F, Serre K, Mohr E, Henderson IR, et al. (2007) Salmonella induces a switched antibody response without germinal centers that impedes the extracellular spread of infection. J Immunol 178: 6200-6207.
50. Pashine A, John B, Rath S, George A, Bal V (1999) Th1 dominance in the immune response to live Salmonella Typhimurium requires bacterial invasiveness but not persistence. Int Immunol 11: 481-489.
51. John B, Rajagopal D, Pashine A, Rath S, George A, et al. (2002) Role of IL-12-independent and IL-12-dependent pathways in regulating generation of the IFNc component of T cell responses to Salmonella Typhimurium. J Immunol 169: 2545-2552.
52. Musso T, Deaglio S, Franco L, Calosso L, Badolato R, et al. (2001) CD38 expression and functional activities are up-regulated by IFNc on human monocytes and monocytic cell lines. J Leukoc Biol 69: 605-612.
53. Mandala WL, MacLennan JM, Gondwe EN, Ward SA, Molyneux ME, et al. (2010) Lymphocyte subsets in healthy Malawians: implications for immunologic assessment of HIV infection in Africa. J Allergy Clin Immunol 125: 203-208.
54. Mittrucker HW, Kohler A, Kaufmann SH (2002) Characterization of the murine T-lymphocyte response to Salmonella enterica serovar Typhimurium infection. Infect Immun 70: 199-203.
55. Srinivasan A, Foley J, McSorley SJ (2004) Massive number of antigen-specific CD4 T cells during vaccination with live attenuated Salmonella causes interclonal competition. J Immunol 172: 6884-6893.
56. Ugrinovic S, Menager N, Goh N, Mastroeni P (2003) Characterization and development of T-Cell immune responses in B-cell-deficient (Igh-6(-/-)) mice with Salmonella enterica serovar Typhimurium infection. Infect Immun 71: 6808-6819.
57. Ramarathinam L, Niesel DW, Klimpel GR (1993) Salmonella Typhimurium induces IFNc production in murine splenocytes. Role of natural killer cells and macrophages. J Immunol 150: 3973-3981.
58. Schafer R, Eisenstein TK (1992) Natural killer cells mediate protection induced by a Salmonella aroA mutant. Infect Immun 60: 791-797.
59. Harrington L, Srikanth CV, Antony R, Shi HN, Cherayil BJ (2007) A role for natural killer cells in intestinal inflammation caused by infection with Salmonella enterica serovar Typhimurium. FEMS Immunol Med Microbiol 51: 372-380.
60. Hirose K, Nishimura H, Matsuguchi T, Yoshikai Y (1999) Endogenous IL-15 might be responsible for early protection by natural killer cells against infection with an avirulent strain of Salmonella Choleraesuis in mice. J Leukoc Biol 66: 382-390.
61. Lapaque N, Walzer T, Meresse S, Vivier E, Trowsdale J (2009) Interactions between human NK cells and macrophages in response to Salmonella infection. J Immunol 182: 4339-4348.
62. Hara T, Mizuno Y, Takaki K, Takada H, Akeda H, et al. (1992) Predominant activation and expansion of Vc9-bearing cd-T cells in vivo as well as in vitro in Salmonella infection. J Clin Invest 90: 204-210.
63. Jason J, Buchanan I, Archibald LK, Nwanyanwu OC, Bell M, et al. (2000) Natural T, cd, and NK cells in mycobacterial, Salmonella, and human immunodeficiency virus infections. J Infect Dis 182: 474-481.
64. Emoto M, Danbara H, Yoshikai Y (1992) Induction of cd-T cells in murine salmonellosis by an avirulent but not by a virulent strain of Salmonella Choleraesuis. J Exp Med 176: 363-372.
65. Nishimura H, Hiromatsu K, Kobayashi N, Grabstein KH, Paxton R, et al. (1996) IL-15 is a novel growth factor for murine cd-T cells induced by Salmonella infection. J Immunol 156: 663-669.
66. Skeen MJ, Ziegler HK (1993) Induction of murine peritoneal cd-T cells and their role in resistance to bacterial infection. J Exp Med 178: 971-984.
67. Mixter PF, Camerini V, Stone BJ, Miller VL, Kronenberg M (1994) Mouse T lymphocytes that express a cd-T cell antigen receptor contribute to resistance to Salmonella infection in vivo. Infect Immun 62: 4618-4621.
68. Harrison JA, Villarreal-Ramos B, Mastroeni P, Demarco de Hormaeche R, Hormaeche CE (1997) Correlates of protection induced by live Aro- Salmonella Typhimurium vaccines in the murine typhoid model. Immunology 90: 618-625.
69. Hormaeche CE, Mastroeni P, Arena A, Uddin J, Joysey HS (1990) T cells do not mediate the initial suppression of a Salmonella infection in the RES. Immunology 70: 247-250.
70. Weintraub BC, Eckmann L, Okamoto S, Hense M, Hedrick SM, et al. (1997) Role of ab- and cd-T cells in the host response to Salmonella infection as demonstrated in T-cell-receptor-deficient mice of defined Ity genotypes. Infect Immun 65: 2306-2312.
71. Mastroeni P, Clare S, Khan S, Harrison JA, Hormaeche CE, et al. (1999) Interleukin 18 contributes to host resistance and c-interferon production in mice infected with virulent Salmonella Typhimurium. Infect Immun 67: 478-483.
72. O'Brien AD, Metcalf ES (1982) Control of early Salmonella Typhimurium growth in innately Salmonella-resistant mice does not require functional T lymphocytes. J Immunol 129: 1349-1351.
73. Mittrucker HW, Kohler A, Mak TW, Kaufmann SH (1999) Critical role of CD28 in protective immunity against Salmonella Typhimurium. J Immunol 163: 6769-6776.
74. Sinha K, Mastroeni P, Harrison J, de Hormaeche RD, Hormaeche CE (1997) Salmonella Typhimurium aroA, htrA, and aroD htrA mutants cause progressive infections in athymic (nu/nu) BALB/c mice. Infect Immun 65: 1566-1569.
75. + T cells and T-independent mechanisms in acquired resistance to Salmonella Typhimurium infection. J Immunol 145: 1265-1269.
76. Muotiala A, Makela PH (1993) Role of c-interferon in late stages of murine salmonellosis. Infect Immun 61: 4248-4253.
77. al-Ramadi BK, Al-Dhaheri MH, Mustafa N, Abouhaidar M, Xu D, et al. (2001) Influence of vector-encoded cytokines on anti-Salmonella immunity: divergent effects of interleukin-2 and tumor necrosis factor-a. Infect Immun 69: 3980-3988.