The IL-23 axis in Salmonella gastroenteritis

Cellular Microbiology

Volumn 13, Issue 11, 2011, Pages 1639-1647

  Godinez, Ivan ^a   Keestra, A Marijke ^a   Spees, Alanna ^a   Bäumler, Andreas J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; GAMMA INTERFERON RECEPTOR 1; GAMMA INTERFERON RECEPTOR 2; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 22 RECEPTOR; INTERLEUKIN 23; MYELOID DIFFERENTIATION FACTOR 88; STAT1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

BACTEREMIA; CYTOKINE PRODUCTION; GASTROENTERITIS; HUMAN; IMMUNE DEFICIENCY; IMMUNOCOMPETENCE; INFECTION RISK; INNATE IMMUNITY; LOSS OF FUNCTION MUTATION; NON TYPHOIDAL SALMONELLA; NONHUMAN; PRIORITY JOURNAL; SALMONELLA; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SEROTYPE; SHORT SURVEY;

ANIMALS; DISEASE MODELS, ANIMAL; GASTROENTERITIS; HUMANS; INTERLEUKIN-23; SALMONELLA; SALMONELLA INFECTIONS; SEPSIS;

ANIMALIA; SALMONELLA;

EID: 80054095579     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01637.x     Document Type: Short Survey

References (84)

1. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., etal. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
2. Altare, F., Lammas, D., Revy, P., Jouanguy, E., Doffinger, R., Lamhamedi, S., etal. (1998) Inherited interleukin 12 deficiency in a child with bacille Calmette-Guerin and Salmonella enteritidis disseminated infection. J Clin Invest 102: 2035-2040.
3. Angel, J.B., High, K., Rhame, F., Brand, D., Whitmore, J.B., Agosti, J.M., etal. (2000) Phase III study of granulocyte-macrophage colony-stimulating factor in advanced HIV disease: effect on infections, CD4 cell counts and HIV suppression. Leukine/HIV Study Group. Aids 14: 387-395.
4. Barthel, M., Hapfelmeier, S., Quintanilla-Martinez, L., Kremer, M., Rohde, M., Hogardt, M., etal. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71: 2839-2858.
5. de Beaucoudrey, L., Puel, A., Filipe-Santos, O., Cobat, A., Ghandil, P., Chrabieh, M., etal. (2008) Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J Exp Med 205: 1543-1550.
6. de Beaucoudrey, L., Samarina, A., Bustamante, J., Cobat, A., Boisson-Dupuis, S., Feinberg, J., etal. (2010) Revisiting human IL-12Rbeta1 deficiency: a survey of 141 patients from 30 countries. Medicine (Baltimore) 89: 381-402.
7. van Beelen, A.J., Zelinkova, Z., Taanman-Kueter, E.W., Muller, F.J., Hommes, D.W., Zaat, S.A., etal. (2007) Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity 27: 660-669.
8. Bergsbaken, T., Fink, S.L., and Cookson, B.T. (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7: 99-109.
9. Bustamante, J., Boisson-Dupuis, S., Jouanguy, E., Picard, C., Puel, A., Abel, L., and Casanova, J.L. (2008) Novel primary immunodeficiencies revealed by the investigation of paediatric infectious diseases. Curr Opin Immunol 20: 39-48.
10. Cleary, A.M., Tu, W., Enright, A., Giffon, T., Dewaal-Malefyt, R., Gutierrez, K., and Lewis, D.B. (2003) Impaired accumulation and function of memory CD4 T cells in human IL-12 receptor beta 1 deficiency. J Immunol 170: 597-603.
11. Cromwell, O., Hamid, Q., Corrigan, C.J., Barkans, J., Meng, Q., Collins, P.D., and Kay, A.B. (1992) Expression and generation of interleukin-8, IL-6 and granulocyte-macrophage colony-stimulating factor by bronchial epithelial cells and enhancement by IL-1 beta and tumour necrosis factor-alpha. Immunology 77: 330-337.
12. Diz Dios, P., Ocampo Hermida, A., Rayo Llerena, N., Otero Varela, I., Iglesias Martin, I., and Martinez Vazquez, C. (1999) [The oxidative metabolic activity of the polymorphonuclear neutrophilic leukocytes in patients infected with the human immunodeficiency virus]. Med Clin (Barc) 113: 652-654.
13. Elbim, C., Prevot, M.H., Bouscarat, F., Franzini, E., Chollet-Martin, S., Hakim, J., and Gougerot-Pocidalo, M.A. (1994) Polymorphonuclear neutrophils from human immunodeficiency virus-infected patients show enhanced activation, diminished fMLP-induced L-selectin shedding, and an impaired oxidative burst after cytokine priming. Blood 84: 2759-2766.
14. Fieschi, C., Dupuis, S., Catherinot, E., Feinberg, J., Bustamante, J., Breiman, A., etal. (2003) Low penetrance, broad resistance, and favorable outcome of interleukin 12 receptor beta1 deficiency: medical and immunological implications. J Exp Med 197: 527-535.
15. Forlow, S.B., Schurr, J.R., Kolls, J.K., Bagby, G.J., Schwarzenberger, P.O., and Ley, K. (2001) Increased granulopoiesis through interleukin-17 and granulocyte colony-stimulating factor in leukocyte adhesion molecule-deficient mice. Blood 98: 3309-3314.
16. Geddes, K., Rubino, S., Streutker, C., Cho, J.H., Magalhaes, J.G., Le Bourhis, L., etal. (2010) Nod1 and Nod2 regulation of inflammation in the Salmonella colitis model. Infect Immun 78: 5107-5115.
17. George, S., Coffey, M., Cinti, S., Collins, J., Brown, M., and Kazanjian, P. (1998) Neutrophils from AIDS patients treated with granulocyte colony-stimulating factor demonstrate enhanced killing of Mycobacterium avium. J Infect Dis 178: 1530-1533.
18. Godinez, I., Haneda, T., Raffatellu, M., George, M.D., Paixao, T.A., Rolan, H.G., etal. (2008) T cells help to amplify inflammatory responses induced by Salmonella enterica serotype Typhimurium in the intestinal mucosa. Infect Immun 76: 2008-2017.
19. Godinez, I., Raffatellu, M., Chu, H., Paixao, T.A., Haneda, T., Santos, R.L., etal. (2009) Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype Typhimurium in the intestine. Infect Immun 77: 387-398.
20. Gordon, M.A. (2008) Salmonella infections in immunocompromised adults. J Infect 56: 413-422.
21. Guadalupe, M., Reay, E., Sankaran, S., Prindiville, T., Flamm, J., McNeil, A., and Dandekar, S. (2003) Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 77: 11708-11717.
22. Guo, L., Wei, G., Zhu, J., Liao, W., Leonard, W.J., Zhao, K., and Paul, W. (2009) IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc Natl Acad Sci USA 106: 13463-13468.
23. Hapfelmeier, S., Stecher, B., Barthel, M., Kremer, M., Muller, A.J., Heikenwalder, M., etal. (2005) The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 174: 1675-1685.
24. Harrington, L., Srikanth, C.V., Antony, R., Shi, H.N., and Cherayil, B.J. (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.
25. Harris, J.C., Dupont, H.L., and Hornick, R.B. (1972) Fecal leukocytes in diarrheal illness. Ann Intern Med 76: 697-703.
26. Israel, D.S., and Plaisance, K.I. (1991) Neutropenia in patients infected with human immunodeficiency virus. Clin Pharm 10: 268-279.
27. Jones, C.E., and Chan, K. (2002) Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-alpha, and granulocyte-colony-stimulating factor by human airway epithelial cells. Am J Respir Cell Mol Biol 26: 748-753.
28. de Jong, R., Altare, F., Haagen, I.A., Elferink, D.G., Boer, T., van Breda Vriesman, P.J., etal. (1998) Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 280: 1435-1438.
29. Keestra, A.M., Godinez, I., Xavier, M.N., Winter, M.G., Winter, S.E., Tsolis, R.M., and Bäumler, A.J. (2011) Early, MyD88-dependent induction of interleukin-17A expression during Salmonella colitis. Infect Immun published ahead of print on 16 May 2011, doi 10.1128/IAI.00018-11
30. Kimura, S., Matsuda, J., Ikematsu, S., Miyazono, K., Ito, A., Nakahata, T., etal. (1990) Efficacy of recombinant human granulocyte colony-stimulating factor on neutropenia in patients with AIDS. Aids 4: 1251-1255.
31. Knodler, L.A., Vallance, B.A., Celli, J., Winfree, S., Hansen, B., Montero, M., and Steele-Mortimer, O. (2010) Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci USA 107: 17733-17738.
32. Lammas, D.A., De Heer, E., Edgar, J.D., Novelli, V., Ben-Smith, A., Baretto, R., etal. (2002) Heterogeneity in the granulomatous response to mycobacterial infection in patients with defined genetic mutations in the interleukin 12-dependent interferon-gamma production pathway. Int J Exp Pathol 83: 1-20.
33. Landro, L., Damas, J.K., Flo, T.H., Heggelund, L., Ueland, T., Tjonnfjord, G.E., etal. (2008) Decreased serum lipocalin-2 levels in human immunodeficiency virus-infected patients: increase during highly active anti-retroviral therapy. Clin Exp Immunol 152: 57-63.
34. Le Bourhis, L., Magalhaes, J.G., Selvanantham, T., Travassos, L.H., Geddes, K., Fritz, J.H., etal. (2009) Role of Nod1 in mucosal dendritic cells during Salmonella pathogenicity island 1-independent Salmonella enterica serovar Typhimurium infection. Infect Immun 77: 4480-4486.
35. Levin, M., Newport, M.J., D'Souza, S., Kalabalikis, P., Brown, I.N., Lenicker, H.M., etal. (1995) Familial disseminated atypical mycobacterial infection in childhood: a human mycobacterial susceptibility gene? Lancet 345: 79-83.
36. Littman, D.R., and Rudensky, A.Y. (2010) Th17 and regulatory T cells in mediating and restraining inflammation. Cell 140: 845-858.
37. Macal, M., Sankaran, S., Chun, T.W., Reay, E., Flamm, J., Prindiville, T.J., and Dandekar, S. (2008) Effective CD4+ T-cell restoration in gut-associated lymphoid tissue of HIV-infected patients is associated with enhanced Th17 cells and polyfunctional HIV-specific T-cell responses. Mucosal Immunol 1: 475-488.
38. MacLennan, C., Fieschi, C., Lammas, D.A., Picard, C., Dorman, S.E., Sanal, O., etal. (2004) Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J Infect Dis 190: 1755-1757.
39. Majowicz, S.E., Musto, J., Scallan, E., Angulo, F.J., Kirk, M., O'Brien, S.J., etal. (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50: 882-889.
40. Mansouri, D., Adimi, P., Mirsaeidi, M., Mansouri, N., Khalilzadeh, S., Masjedi, M.R., etal. (2005) Inherited disorders of the IL-12-IFN-gamma axis in patients with disseminated BCG infection. Eur J Pediatr 164: 753-757.
41. Mayuzumi, H., Inagaki-Ohara, K., Uyttenhove, C., Okamoto, Y., and Matsuzaki, G. (2010) Interleukin-17A is required to suppress invasion of Salmonella enterica serovar Typhimurium to enteric mucosa. Immunology 131: 377-385.
42. Medzhitov, R., Preston-Hurlburt, P., Kopp, E., Stadlen, A., Chen, C., Ghosh, S., and Janeway, C.A., Jr (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2: 253-258.
43. Meyer, C.N., and Nielsen, H. (1996) Priming of neutrophil and monocyte activation in human immunodeficiency virus infection. Comparison of granulocyte colony-stimulating factor, granulocyte-macrophage colony-stimulating factor and interferon-gamma. APMIS 104: 640-646.
44. Miao, E.A., Alpuche-Aranda, C.M., Dors, M., Clark, A.E., Bader, M.W., Miller, S.I., and Aderem, A. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575.
45. Miao, E.A., Mao, D.P., Yudkovsky, N., Bonneau, R., Lorang, C.G., Warren, S.E., etal. (2010a) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 107: 3076-3080.
46. Miao, E.A., Leaf, I.A., Treuting, P.M., Mao, D.P., Dors, M., Sarkar, A., etal. (2010b) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11: 1136-1142.
47. Muller, A.J., Hoffmann, C., Galle, M., Van Den Broeke, A., Heikenwalder, M., Falter, L., etal. (2009) The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 6: 125-136.
48. Muzio, M., Ni, J., Feng, P., and Dixit, V.M. (1997) IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278: 1612-1615.
49. Nairz, M., Theurl, I., Schroll, A., Theurl, M., Fritsche, G., Lindner, E., etal. (2009) Absence of functional Hfe protects mice from invasive Salmonella enterica serovar Typhimurium infection via induction of lipocalin-2. Blood 114: 3642-3651.
50. Oppmann, B., Lesley, R., Blom, B., Timans, J.C., Xu, Y., Hunte, B., etal. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
51. Pedraza-Sanchez, S., Herrera-Barrios, M.T., Aldana-Vergara, R., Neumann-Ordonez, M., Gonzalez-Hernandez, Y., Sada-Diaz, E., etal. (2010) Bacille Calmette-Guerin infection and disease with fatal outcome associated with a point mutation in the interleukin-12/interleukin-23 receptor beta-1 chain in two Mexican families. Int J Infect Dis 14 (Suppl. 3): e256-e260.
52. Picard, C., Fieschi, C., Altare, F., Al-Jumaah, S., Al-Hajjar, S., Feinberg, J., etal. (2002) Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds. Am J Hum Genet 70: 336-348.
53. Pitrak, D.L., Bak, P.M., DeMarais, P., Novak, R.M., and Andersen, B.R. (1993) Depressed neutrophil superoxide production in human immunodeficiency virus infection. J Infect Dis 167: 1406-1410.
54. Prendergast, A., Prado, J.G., Kang, Y.H., Chen, F., Riddell, L.A., Luzzi, G., etal. (2010) HIV-1 infection is characterized by profound depletion of CD161+ Th17 cells and gradual decline in regulatory T cells. Aids 24: 491-502.
55. Rabsch, W., Tschape, H., and Baumler, A.J. (2001) Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3: 237-247.
56. Rachitskaya, A.V., Hansen, A.M., Horai, R., Li, Z., Villasmil, R., Luger, D., etal. (2008) Cutting edge: NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J Immunol 180: 5167-5171.
57. Raffatellu, M., Santos, R.L., Chessa, D., Wilson, R.P., Winter, S.E., Rossetti, C.A., etal. (2007) The capsule encoding the viaB locus reduces interleukin-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect Immun 75: 4342-4350.
58. Raffatellu, M., Santos, R.L., Verhoeven, D.E., George, M.D., Wilson, R.P., Winter, S.E., etal. (2008) Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 14: 421-428.
59. Raffatellu, M., George, M.D., Akiyama, Y., Hornsby, M.J., Nuccio, S.P., Paixao, T.A., etal. (2009) Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5: 476-486.
60. Reddy, E.A., Shaw, A.V., and Crump, J.A. (2010) Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis 10: 417-432.
61. Roilides, E., Holmes, A., Blake, C., Pizzo, P.A., and Walsh, T.J. (1993) Impairment of neutrophil antifungal activity against hyphae of Aspergillus fumigatus in children infected with human immunodeficiency virus. J Infect Dis 167: 905-911.
62. Rout, W.R., Formal, S.B., Dammin, G.J., and Giannella, R.A. (1974) Pathophysiology of Salmonella diarrhea in the Rhesus monkey: intestinal transport, morphological and bacteriological studies. Gastroenterology 67: 59-70.
63. Sanal, O., Turul, T., De Boer, T., Van de Vosse, E., Yalcin, I., Tezcan, I., etal. (2006) Presentation of interleukin-12/-23 receptor beta1 deficiency with various clinical symptoms of Salmonella infections. J Clin Immunol 26: 1-6.
64. Santos, R.L., Zhang, S., Tsolis, R.M., Kingsley, R.A., Adams, L.G., and Bäumler, A.J. (2001) Animal models of Salmonella infections: enteritis vs. typhoid fever. Microb Infect 3: 1335-1344.
65. Schneider, T., Jahn, H.U., Schmidt, W., Riecken, E.O., Zeitz, M., and Ullrich, R. (1995) Loss of CD4 T lymphocytes in patients infected with human immunodeficiency virus type 1 is more pronounced in the duodenal mucosa than in the peripheral blood. Berlin Diarrhea/Wasting Syndrome Study Group. Gut 37: 524-529.
66. Schulz, S.M., Kohler, G., Schutze, N., Knauer, J., Straubinger, R.K., Chackerian, A.A., etal. (2008) Protective immunity to systemic infection with attenuated Salmonella enterica serovar enteritidis in the absence of IL-12 is associated with IL-23-dependent IL-22, but not IL-17. J Immunol 181: 7891-7901.
67. Schwarzenberger, P., La Russa, V., Miller, A., Ye, P., Huang, W., Zieske, A., etal. (1998) IL-17 stimulates granulopoiesis in mice: use of an alternate, novel gene therapy-derived method for in vivo evaluation of cytokines. J Immunol 161: 6383-6389.
68. Schwarzenberger, P., Huang, W., Ye, P., Oliver, P., Manuel, M., Zhang, Z., etal. (2000) Requirement of endogenous stem cell factor and granulocyte-colony-stimulating factor for IL-17-mediated granulopoiesis. J Immunol 164: 4783-4789.
69. Sharifi Mood, B., Mohraz, M., Mansouri, S.D., Alavi Naini, R., Kouhpayeh, H.R., Naderi, M., etal. (2004) Recurrent non-typhoidal salmonella bacteremia in a patient with interleukin-12p40 deficiency. Iran J Allergy Asthma Immunol 3: 197-200.
70. Siegemund, S., Schutze, N., Freudenberg, M.A., Lutz, M.B., Straubinger, R.K., and Alber, G. (2007) Production of IL-12, IL-23 and IL-27p28 by bone marrow-derived conventional dendritic cells rather than macrophages after LPS/TLR4-dependent induction by Salmonella Enteritidis. Immunobiology 212: 739-750.
71. de Silva, T.I., Cope, A., Goepel, J., and Greig, J.M. (2007) The use of adjuvant granulocyte-macrophage colony-stimulating factor in HIV-related disseminated atypical mycobacterial infection. J Infect 54: e207-e210.
72. Smith, E., Zarbock, A., Stark, M.A., Burcin, T.L., Bruce, A.C., Foley, P., and Ley, K. (2007) IL-23 is required for neutrophil homeostasis in normal and neutrophilic mice. J Immunol 179: 8274-8279.
73. Songhet, P., Barthel, M., Rohn, T.A., Van Maele, L., Cayet, D., Sirard, J.C., etal. (2010) IL-17A/F-signaling does not contribute to the initial phase of mucosal inflammation triggered by S. Typhimurium. PLoS ONE 5: e13804.
74. Srinivasan, A., Salazar-Gonzalez, R.M., Jarcho, M., Sandau, M.M., Lefrancois, L., and McSorley, S.J. (2007) Innate immune activation of CD4 T cells in salmonella-infected mice is dependent on IL-18. J Immunol 178: 6342-6349.
75. Staretz-Haham, O., Melamed, R., Lifshitz, M., Porat, N., Fieschi, C., Casanova, J.L., and Levy, J. (2003) Interleukin-12 receptor beta1 deficiency presenting as recurrent Salmonella infection. Clin Infect Dis 37: 137-140.
76. Sutton, C.E., Lalor, S.J., Sweeney, C.M., Brereton, C.F., Lavelle, E.C., and Mills, K.H. (2009) Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31: 331-341.
77. Takahashi, N., Vanlaere, I., de Rycke, R., Cauwels, A., Joosten, L.A., Lubberts, E., etal. (2008) IL-17 produced by Paneth cells drives TNF-induced shock. J Exp Med 205: 1755-1761.
78. Tsolis, R.M., Adams, L.G., Ficht, T.A., and Baumler, A.J. (1999) Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 67: 4879-4885.
79. Tsolis, R.M., Xavier, M.N., Santos, R.L., and Baumler, A.J. (2011) How to become a top model: impact of animal experimentation on human salmonella disease research. Infect Immun 79: 1806-1814.
80. von Vietinghoff, S., and Ley, K. (2009) IL-17A controls IL-17F production and maintains blood neutrophil counts in mice. J Immunol 183: 865-873.
81. Wesche, H., Henzel, W.J., Shillinglaw, W., Li, S., and Cao, Z. (1997) MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7: 837-847.
82. Winter, S.E., Thiennimitr, P., Nuccio, S.P., Haneda, T., Winter, M.G., Wilson, R.P., etal. (2009) Contribution of flagellin pattern recognition to intestinal inflammation during Salmonella enterica serotype Typhimurium infection. Infect Immun 77: 1904-1916.
83. Winter, S.E., Keestra, A.M., Tsolis, R.M., and Baumler, A.J. (2010) The blessings and curses of intestinal inflammation. Cell Host Microbe 8: 36-43.
84. Zuccotti, G.V., Plebani, A., Biasucci, G., Clerici-Schoeller, M., Banderali, G., Decarlis, S., etal. (1996) Granulocyte-colony stimulating factor and erythropoietin therapy in children with human immunodeficiency virus infection. J Int Med Res 24: 115-121.