Dysregulated immune profiles for skin and dendritic cells are associated with increased host susceptibility to Haemophilus ducreyi infection in human volunteers

Infection and Immunity

Volumn 75, Issue 12, 2007, Pages 5686-5697

  Humphreys, Tricia L ^a,d   Li, Lang ^a   Li, Xiaoman ^a,b   Janowicz, Diane M ^a   Fortney, Kate R ^a   Zhao, Qianqian ^a   Li, Wei ^a   McClintick, Jeanette ^a   Katz, Barry P ^a   Wilkes, David S ^a   Edenberg, Howard J ^a   Spinola, Stanley M ^a,c  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Grinnell College ^*  (United States)

^d GRINNELL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TOLL LIKE RECEPTOR 4;

ADULT; ARTICLE; BACTERIAL INFECTION; DENDRITIC CELL; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HAEMOPHILUS DUCREYI; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNE RESPONSE; INFECTION SENSITIVITY; INFLAMMATION; MACROPHAGE; MALE; MICROARRAY ANALYSIS; MONOCYTE; NEUTROPHIL; NORMAL HUMAN; OXIDATIVE STRESS; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PUSTULE; REGULATORY T LYMPHOCYTE; SKIN CELL; T LYMPHOCYTE; TH1 CELL;

ADULT; CELL PROLIFERATION; CHANCROID; CYTOKINES; DISEASE SUSCEPTIBILITY; FEMALE; HAEMOPHILUS DUCREYI; HUMANS; LANGERHANS CELLS; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 36749086426     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00777-07     Document Type: Article

References (86)

1. Abdullah, M., I. Nepluev, G. Afonina, S. Ram, P. Rice, W. Cade, and C. Elkins. 2005. Killing of dsrA mutants of Haemophilus ducreyi by normal human serum occurs via the classical complement pathway and is initiated by immunoglobulin M binding. Infect. Immun. 73:3431-3439.
2. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8:942-949.
3. Ahmed, H. J., C. Johansson, L. A. Svensson, K. Ahlman, M. Verdrengh, and T. Lagergard. 2002. In vitro and in vivo interactions of Haemophilus ducreyi with host phagocytes. Infect. Immun. 70:899-908.
4. Al-Tawfiq, J. A., A. C. Thornton, B. P. Katz, K. R. Fortney, K. D. Todd, A. F. Hood, and S. M. Spinola. 1998. Standardization of the experimental model of Haemophilus ducreyi infection in human subjects. J. Infect. Dis. 178:1684-1687.
5. Alter, O., P. O. Brown, and D. Botstein. 2000. Singular value decomposition for genome-wide expression data processing and modeling. Proc. Natl. Acad. Sci. USA 97:10101-10106.
6. Banks, K. E., T. L. Humphreys, W. Li, B. P. Katz, D. S. Wilkes, and S. M. Spinola. 2007. Haemophilus ducreyi partially activates human myeloid dendritic cells. Infect. Immun. 75:5678-5685.
7. Bastos, K. R. B., C. R. F. Marhino, R. Barboza, M. Russe, J. M. Alvarez, and M. R. D'Imperio Lima. 2004. What kind of message does IL-12/IL-23 bring to macrophages and dendritic cells? Microbes Infect. 6:630-636.
8. Bauer, M. E., M. P. Goheen, C. A. Townsend, and S. M. Spinola. 2001. Haemophilus ducreyi associates with phagocytes, collagen, and fibrin and remains extracellular throughout infection of human volunteers. Infect. Immun. 69:2549-2557.
9. Bauer, M. E., C. A. Townsend, A. R. Ronald, and S. M. Spinola. 2006. Localization of Haemophilus ducreyi in naturally acquired chancroidal ulcers. Microbes Infect. 8:2465-2468.
10. Bleharski, J. R., H. Li, C. Meinken, T. G. Graeber, M.-T. Ochoa, M. Yamamura, A. Burdick, E. N. Sarno, M. Wagner, M. Rollinghoff, T. H. Rea, M. Colonna, S. Stenger, B. R. Bloom, D. Eisenberg, and R. L. Modlin. 2003. Use of genetic profiling in leprosy to discriminate clinical forms of the disease. Science 301:1527-1530.
11. Bochud, P.-Y., T. R. Hawn, and A. Aderem. 2003. Cutting edge: a Toll-like receptor 2 polymorphism that is associated with lepromatous leprosy is unable to mediate mycobacterial signaling. J. Immunol. 170:3451-3454.
12. Boldrick, J. C., A. A. Alizadeh, M. Diehn, S. Dudoit, C. L. Liu, C. E. Belcher, D. Botstein, L. M. Staudt, P. O. Brown, and D. A. Relman. 2002. Stereotyped and specific gene expression programs in human innate immune responses to bacteria. Proc. Natl. Acad. Sci. USA 99:972-977.
13. Bolstad, B. M., R. A. Irizarry, M. Amstrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193.
14. Bong, C. T. H., M. E. Bauer, and S. M. Spinola. 2002. Haemophilus ducreyi: clinical features, epidemiology, and prospects for disease control. Microbes Infect. 4:1141-1148.
15. Bong, C. T. H., J. Harezlak, B. P. Katz, and S. M. Spinola. 2002. Men are more susceptible to pustule formation than women in the experimental model of Haemophilus ducreyi infection. Sex. Transm. Dis. 29:114-118.
16. Bong, C. T. H., R. E. Throm, K. R. Fortney, B. P. Katz, A. F. Hood, C. Elkins, and S. M. Spinola. 2001. A DsrA-deficient mutant of Haemophilus ducreyi is impaired in its ability to infect human volunteers. Infect. Immun. 69:1488-1491.
17. Chaussabel, D., R. T. Semnani, M. A. McDowell, D. Sacks, A. Sher, and T. B. Nutman. 2003. Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood 102:672-681.
18. Clark, D. A. 2005. Tolerance signaling molecules. Chem. Immunol. Allergy 89:36-48.
19. de Jong, E. C., H. H. Smits, and M. L. Kapsenberg. 2005. Dendritic cell-mediated T cell polarization. Springer Semin. Immunopathol. 26:289-307.
20. Elkins, C., K. J. Morrow, and B. Olsen. 2000. Serum resistance in Haemophilus ducreyi requires outer membrane protein DsrA. Infect. Immun. 68:1608-1619.
21. Emonts, M., J. A. Hazelzet, R. deGroot, and P. W. M. Hermans. 2003. Host genetic determinants of Meissera meningitidis infections. Lancet 3:565-577.
22. Fabriek, B. O., C. D. Dijkstra, and T. K. van den Berg. 2005. The macrophage scavenger receptor CD163. Immunobiology 210:153-160.
23. Fulcher, R. A., L. E. Cole, D. M. Janowicz, K. L. Toffer, K. R. Fortney, B. P. Katz, P. E. Orndorff, S. M. Spinola, and T. H. Kawula. 2006. Expression of Haemophilus ducreyi collagen binding outer membrane protein NcaA is required for virulence in swine and human challenge models of chancroid. Infect. Immun. 74:2651-2658.
24. Geijtenbeek, T. B. H., S. J. van Vliet, E. A. Koppel, M. Sanchez-Hernandez, C. M. J. E. Vandenbroucke-Grauls, B. Appelmelk, and Y. van Kooyk. 2003. Mycobacteria target DC-sign to suppress dendritic cell function. J. Exp. Med. 197:7-17.
25. Geisler, W. M., J. Tang, C. Wang, C. M. Wilson, and R. A. Kaslow. 2004. Epidemiological and genetic correlates of incident Chlamydia trachomatis infection in North American adolescents. J. Infect. Dis. 190:1723-1729.
26. Gelfanova, V., T. L. Humphreys, and S. M. Spinola. 2001. Characterization of Haemophilus ducreyi-specific T-cell lines from lesions of experimentally infected human subjects. Infect. Immun. 69:4224-4231.
27. Greenwell-Wild, T., N. Vazquez, D. Sim, M. Schito, D. Chatterjee, J. M. Orenstein, and S. M. Wahl. 2002. Mycobacterium avium infection and modulation of human macrophage gene expression. J. Immunol. 169:6286- 6297.
28. Hammond, G. W., M. Slutchuk, J. Scatliff, E. Sherman, J. C. Wilt, and A. R. Ronald. 1980. Epidemiologic, clinical, laboratory, and therapeutic features of an urban outbreak of chancroid in North America. Rev. Infect. Dis. 2:867-879.
29. Hawn, T. R., A. Verbon, M. Janer, L. P. Zhao, B. Beutler, and A. Aderem. 2005. Toll-like receptor 4 polymorphisms are associated with resistance to Legionnaires' disease. Proc. Natl. Acad. Sci. USA 102:2487-2489.
30. Higgins, S. C., E. C. Lavelle, C. McCann, B. Keogh, E. McNeela, P. Byrne, B. O'Gorman, A. Jarnicki, P. McGuirk, and K. H. G. Mills. 2003. Toll-like receptor 4-mediated innate IL-10 activates antigen-specific regulatory T cells and confers resistance to Bordetella pertussis by inhibiting inflammatory pathology. J. Immunol. 171:3119-3127.
31. Huang, Q., D. Liu, P. Majewski, L. C. Schulte, J. M. Korn, R. A. Young, E. S. Lander, and N. Hacohen. 2001. The plasticity of dendritic cell responses to pathogens and their components. Science 294:870-875.
32. Humphreys, T. L., L. A. Baldridge, S. D. Billings, J. J. Campbell, and S. M. Spinola. 2005. Trafficking pathways and characterization of CD4 and CD8 cells recruited to the skin of humans experimentally infected with Haemophilus ducreyi. Infect. Immun. 73:3896-3902.
33. Humphreys, T. L., C. T. Schnizlein-Bick, B. P. Katz, L. A. Baldridge, A. F. Hood, R. A. Hromas, and S. M. Spinola. 2002. Evolution of the cutaneous immune response to experimental Haemophilus ducreyi infection and its relevance to HIV-1 acquisition. J. Immunol. 169:6316-6323.
34. Itano, A. A., and M. K. Jenkins. 2003. Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 4:733-739.
35. Janowicz, D., I. Leduc, K. R. Fortney, B. P. Katz, C. Elkins, and S. M. Spinola. 2006. A DltA mutant of Haemophilus ducreyi is partially attenuated in its ability to cause pustules in human volunteers. Infect. Immun. 74:1394-1397.
36. Janowicz, D. M., K. R. Fortney, B. P. Katz, J. L. Latimer, K. Deng, E. J. Hansen, and S. M. Spinola. 2004. Expression of the LspA1 and LspA2 proteins by Haemophilus ducreyi is required for virulence in human volunteers. Infect. Immun. 72:4528-4533.
37. Janowicz, D. M., K. Tenner-Racz, P. Racz, T. L. Humphreys, C. Schnizlein-Bick, K. R. Fortney, B. Zwickl, B. P. Katz, J. J. Campbell, D. D. Ho, and S. M. Spinola. 2007. Experimental infection with Haemophilus ducreyi in persons who are infected with HIV does not cause local or augment systemic viral replication. J. Infect. Dis. 195:1443-1451.
38. Kluppel, M., and J. L. Wrana. 2005. Turning it up a Notch: cross-talk between TGF beta and Notch signaling. Bioessays 27:115-118.
39. Kolls, J. K. 2006. Oxidative stress in sepsis: a redox redux. J. Clin. Investig. 116:860-863.
40. Krutzik, S. R., M. T. Ochoa, P. A. Sieling, S. Uematsu, Y. W. Ng, A. Legaspi, P. T. Liu, S. T. Cole, P. J. Godowski, Y. Maeda, E. N. Sarno, M. V. Norgard, P. J. Brennan, S. Akira, T. H. Rea, and R. L. Modlin. 2003. Activation and regulation of Toll-like receptors 2 and 1 in human leprosy. Nat. Med. 9:525-532.
41. Laurence, A., and J. O'Shea. 2007. TH-17 differentiation: of mice and men. Nat. Immunol. 8:903-905.
42. Leduc, I., P. Richards, C. Davis, B. Schilling, and C. Elkins. 2004. A novel lectin, DltA, is required for expression of a full serum resistance phenotype in Haemophilus ducreyi. Infect. Immun. 72:3418-3428.
43. Liu, Y.-J. 2001. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106:259-262.
44. Lorenz, E., J. P. Mira, K. L. Cornish, N. C. Arbour, and D. A. Schwartz. 2000. A novel polymorphism in the Toll-like receptor 2 gene and its potential association with staphylococcal infection. Infect. Immun. 68:6398-6401.
45. Mannering, S. I., J. S. Morris, K. P. Jensen, A. W. Purcell, M. C. Honeyman, P. M. vanEndert, and L. C. Harrison. 2003. A sensitive method for detecting proliferation of rare autoantigen-specific human T cells. J. Immunol. Methods 283:173-183.
46. McClintick, J. N., and H. J. Edenberg. 2006. Effects of filtering by present call on analysis of microarray experiments. BMC Bioinformatics 7:49.
47. McClintick, J. N., R. E. Jerome, C. R. Nicholson, D. W. Crabb, and H. J. Edenberg. 2003. Reproducibility of oligonucleotide arrays using small samples. BMC Genomics 4:1-15.
48. McGuirk, P., and K. H. G. Mills. 2002. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends Immunol. 23:450-455.
49. Mellor, A. L., B. Baban, P. Chandler, B. Marshall, K. Jhaver, A. Hansen, P. A. Koni, M. Iwashima, and D. H. Munn. 2003. Induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J. Immunol. 171:1652-1655.
50. Mills, K. H. G. 2004. Regulatory T cells: friend or foe in immunity to infection? Nat. Rev. Immunol. 4:841-855.
51. Mock, J. R., M. Vakevainen, K. Deng, J. L. Latimer, J. A. Young, N. S. van Oers, S. Greenberg, and E. J. Hansen. 2005. Haemophilus ducreyi targets Src family protein tyrosine kinases to inhibit phagocytic signaling. Infect. Immun. 73:7808-7816.
52. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765.
53. Morse, S. A. 1989. Chancroid and Haemophilus ducreyi. Clin. Microbiol. Rev. 2:137-157.
54. Murphy, T. F., L. C. Bartos, A. A. Campagnari, M. B. Nelson, and M. A. Apicella. 1986. Antigenic characterization of the P6 protein of nontypable Haemophilus influenzae. Infect. Immun. 54:774-779.
55. Niessen, F. B., M. P. Andriessen, J. Schalkwijk, L. Visser, and W. Timens. 2001. Keratinocyte-derived growth factors play a role in the formation of hypertrophic scars. J. Pathol. 194:207-216.
56. Opdal, S. H. 2004. IL-10 gene polymorphisms in infectious disease and SIDS. FEMS Immunol. Med. Microbiol. 42:48-52.
57. Palmer, K. L., C. T. Schnizlein-Bick, A. Orazi, K. John, C.-Y. Chen, A. F. Hood, and S. M. Spinola. 1998. The immune response to Haemophilus ducreyi resembles a delayed-type hypersensitivity reaction throughout experimental infection of human subjects. J. Infect. Dis. 178:1688-1697.
58. Post, D. M. B., R. S. Munson, Jr., B. Baker, H. Zhong, J. A. Bozue, and B. W. Gibson. 2007. Identification of genes involved in the expression of atypical lipooligosaccharide structures from a second class of Haemophilus ducreyi. Infect. Immun. 75:113-121.
59. Pulendran, B., K. Palucka, and J. Banchereau. 2001. Sensing pathogens and tuning immune responses. Science 293:253-256.
60. Scheffler, N. K., A. M. Falick, S. C. Hall, W. C. Ray, D. M. Post, R. S. Munson, Jr., and B. W. Gibson. 2003. Proteome of Haemophilus ducreyi by 2-D SDS-PAGE and mass spectrometry: strain variation, virulence, and carbohydrate expression. J. Proteome Res. 2:523-533.
61. Smirnova, I., N. Mann, A. Dols, H. H. Derkx, M. L. Hibberd, M. Levin, and B. Beutler. 2003. Assay of locus-specific genetic load implicates rare Toll-like receptor 4 mutations in meningococcal susceptibility. Proc. Natl. Acad. Sci. USA 100:6075-6080.
62. Spellberg, B., and J. E. Edwards, Jr. 2001. Type1/type2 immunity in infectious diseases. Clin. Infect. Dis. 32:76-102.
63. Spinola, S. M., M. E. Bauer, and R. S. Munson, Jr. 2002. Immunopathogenesis of Haemophilus ducreyi infection (chancroid). Infect. Immun. 70:1667-1676.
64. Spinola, S. M., C. T. H. Bong, A. L. Faber, K. R. Fortney, S. L. Bennett, C. A. Townsend, B. E. Zwkkl, S. D. Billings, T. L. Humphreys, M. E. Bauer, and B. P. Katz. 2003. Differences in host susceptibility to disease progression in the human challenge model of Haemophilus ducreyi infection. Infect. Immun. 71:6658-6663.
65. Spinola, S. M., K. R. Fortney, B. P. Katz, J. L. Latimer, J. R. Mock, M. Vakevainen, and E. J. Hansen. 2003. Haemophilus ducreyi requires an intact flp gene cluster for virulence in humans. Infect. Immun. 71:7178-7182.
66. Spinola, S. M., A. Orazi, J. N. Arno, K. Fortney, P. Kotylo, C.-Y. Chen, A. A. Campagnari, and A. F. Hood. 1996. Haemophilus ducreyi elicits a cutaneous infiltrate of CD4 cells during experimental human infection. J. Infect. Dis. 173:394-402.
67. Spinola, S. M., L. M. Wild, M. A. Apicella, A. A. Gaspari, and A. A. Campagnari. 1994. Experimental human infection with Haemophilus ducreyi. J. Infect. Dis. 169:1146-1150.
68. Steen, R. 2001. Eradicating chancroid. Bull. W. H. O. 79:818-826.
69. Steinman, L. 2007. A brief history of TH17, the first major revision in the TH1/TH2 hypothesis of T cell-mediated tissue damage. Nat. Med. 13:139-145.
70. Strengell, M., A. Lehtonen, S. Matikainen, and I. Julkunen. 2006. IL-21 enhances SOCS gene expression and inhibits LPS-induced cytokine production in human monocyte-derived dendritic cells. J. Leukoc. Biol. 79:1279-1285.
71. Sullivan, M. 1940. Chancroid. Am. J. Syph. Gon. Vener. Dis. 24:482-521.
72. Tenca, C., A. Merlo, E. Merck, E. E. M. Bates, D. Saverino, R. Simone, D. Zarcone, G. Trinchieri, C. E. Grossi, and E. Ciccone. 2005. CD85i (leukocyte Ig-like receptor-1/Ig-like transcript 2) inhibits human osteoclast-associated receptor-mediated activation of human dendritic cells. J. Immunol. 174:6757-6763.
73. Thimmulappa, R. K., H. Lee, T. Rangasamy, S. P. Reddy, M. Yamamoto, T. W. Kensler, and S. Biswal. 2006. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Investig. 116:984-995.
74. Throm, R. E., and S. M. Spinola. 2001. Transcription of candidate virulence genes of Haemophilus ducreyi during infection of human volunteers. Infect. Immun. 69:1483-1487.
75. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 133:133-146.
76. + T-cell activation via the CD28-B7-2 costimulatory pathway. Infect. Immun. 68:6650-6655.
77. Tzianabos, A. O., and D. L. Kasper. 2002. Role of T cells in abscess formation. Curr. Opin. Microbiol. 5:92-96.
78. Tzianabos, A. O., P. R. Russell, A. B. Onderdonk, F. C. Gibson III, C. Cywes, M. Chan, R. W. Finberg, and D. L. Kasper. 1999. IL-2 mediates protection against abscess formation in an experimental model of sepsis. J. Immunol. 163:893-897.
79. Vakevainen, M., S. Greenberg, and E. J. Hansen. 2003. Inhibition of phagocytosis by Haemophilus ducreyi requires expression of the LspA1 and LspA2 proteins. Infect. Immun. 71:5994-6003.
80. Visintin, A., A. Mazzoni. J. H. Spitzer, D. H. Wyllie, S. K. Dower, and D. M. Segal. 2001. Regulation of toll-like receptors in human monocytes and dendritic cells. J. Immunol. 166:249-255.
81. Wang, C., J. Tang, W. M. Geisler, P. A. Crowley-Nowick, C. M. Wilson, and R. A. Kaslow. 2005. Human leukocyte antigen and cytokine gene variants as predictors of recurrent Chlamydia trachomatis infection in high-risk adolescents. J. Infect. Dis. 191:1084-1092.
82. Wells, A. D., H. Gudmundsdottir, and L. A. Turka. 1997. Following the fate of individual T cells throughout activation and clonal expansion. Signals from T cell receptor and CD28 differentially regulate the induction and duration of a proliferative response. J. Clin. Investig. 100:3173-3183.
83. White, C. D., I. Leduc, C. Jeter, C. Harris, and C. Elkins. 2005. Haemophilus ducreyi outer membrane determinants, including DsrA, define two clonal populations. Infect. Immun. 73:2387-2399.
84. Wilson, N. J., K. Boniface, J. R. Chan, B. S. McKenzie, W. M. Blumenschein, J. D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, J. C. Lecron, R. A. Kastelein, D. J. Cua, T. K. McClanahan, E. P. Bowman, and R. de Waal Malefyt. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8:950-957.
85. Wood, G. E., S. M. Dutro, and P. A. Totten. 2001. Haemophilus ducreyi inhibits phagocytosis by U-937 cells, a human macrophage-like cell line. Infect. Immun. 69:4726-4733.
86. Zou, G. M., and Y. K. Tam. 2002. Cytokines in the generation and maturation of dendritic cells: recent advances. Eur. Cytokine Netw. 13:186-199.