Enhancement of human antigen-specific memory T-cell responses by interleukin-7 may improve accuracy in diagnosing tuberculosis

Clinical and Vaccine Immunology

Volumn 15, Issue 10, 2008, Pages 1616-1622

  Feske, Marsha ^a,b   Nudelman, Rodolfo J ^b   Medina, Miguel ^b   Lew, Justin ^b   Singh, Manisha ^b   Couturier, Jacob ^b   Graviss, Edward A ^b   Lewis, Dorothy E ^b,c  

^a UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN P24; CULTURE FILTRATE PROTEIN 10; EARLY SECRETORY ANTIGENIC TARGET 6; GAMMA INTERFERON; INTERLEUKIN 7; KEYHOLE LIMPET HEMOCYANIN; PHYTOHEMAGGLUTININ; TETANUS TOXOID; BACTERIAL ANTIGEN; GAG PROTEIN;

ADULT; ANTIGEN SPECIFICITY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; HIGH RISK POPULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOSTIMULATION; LYMPHOCYTE ACTIVATION; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; TUBERCULOSIS; ADOLESCENT; BIOSYNTHESIS; CELL CULTURE; IMMUNOLOGY; T LYMPHOCYTE;

ADOLESCENT; ADULT; ANTIGENS, BACTERIAL; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIV CORE PROTEIN P24; HUMANS; INTERFERON TYPE II; INTERLEUKIN-7; SENSITIVITY AND SPECIFICITY; T-LYMPHOCYTES; TUBERCULOSIS;

EID: 55449108986     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00185-08     Document Type: Article

References (49)

1. Arend, S. M., A. Geluk, K. E. van Meijgaarden, J. T. van Dissel, M. Theisen, P. Andersen, and T. H. Ottenhoff. 2000. Antigenic equivalence of human T-cell responses to Mycobacterium tuberculosis-specific RD1-encoded protein antigens ESAT-6 and culture filtrate protein 10 and to mixtures of synthetic peptides. Infect. Immun. 68:3314-3321.
2. Arend, S. M., S. F. T. Thijsen, E. M. S. Leyten, J. J. M. Bouwman, W. P. J. Franken, B. F. Koster, F. G. J. Cobelens, A. J. van Houte, and A. W. J. Bossink. 2007. Comparison of two interferon-gamma assays and tuberculin skin test for tracing tuberculosis contacts. Am. J. Respir. Crit. Care Med. 175:618-627.
3. + T cells from human immunodeficiency virus-infected persons. J. Virol. 81:12670-12674.
4. Borger, P., H. F. Kauffman, D. S. Postma, and E. Vellenga. 1996. IL-7 differentially modulates the expression of IFN-gamma and IL-4 in activated human T lymphocytes by transcriptional and post-transcriptional mechanisms. J. Immunol. 156:1333-1338.
5. Chapman, A. L. N., M. Munkanta, K. A. Wilkinson, A. A. Pathan, K. Ewer, H. Ayles, W. H. Reece, A. Mwinga, P. Godfrey-Faussett, and A. Lalvani. 2002. Rapid detection of active and latent tuberculosis infection in HIVpositive individuals by enumeration of Mycobacterium tuberculosis-specific T cells. AIDS 16:2285-2293.
6. Chung, I. Y., H. F. Dong, X. Zhang, N. M. A. Hassanein, O. M. Z. Howard, J. J. Oppenheim, and X. Chen. 2004. Effects of IL-7 and dexamethasone: induction of CD25, the high affinity IL-2 receptor, on human CD4+ cells. Cell. Immunol. 232:57-63.
7. Connell, T. G., N. Ritz, G. A. Paxton, J. P. Buttery, N. Curtis, and S. C. Ranganathan. 2008. A three-way comparison of tuberculin skin testing, QuantiFERON-TB Gold and T-SPOT, TB in children. PLoS ONE 3:1-8.
8. Detjen, A. K., T. Keil, S. Roll, B. Hauer, H. Mauch, U. Wahn, and K. Magdorf. 2007. Interferon-γ release assays improve the diagnosis of tuberculosis and nontuberculous mycobacterial disease in children in a country with a low incidence of tuberculosis. Clin. Infect. Dis. 45:322-328.
9. Doherty, T. M., A. Demissie, D. Menzies, P. Andersen, G. Rook, and A. Zumla. 2005. Effect of sample handling on analysis of cytokine responses to Mycobacterium tuberculosis in clinical samples using ELISA, ELISPOT and quantitative PCR. J. Immunol. Methods 298:129-141.
10. Ewer, K., J. Deeks, L. Alvarez, G. Bryant, S. Waller, P. Andersen, P. Monk, and A. Lalvani. 2003. Comparison of T-cell-based assay with tuberculin skin test for diagnosis of Mycobacterium tuberculosis infection in a school tuberculosis outbreak. Lancet 361:1168-1173.
11. Fry, T. J., E. Connick, J. Falloon, M. M. Lederman, D. J. Liewehr, J. Spritzler, S. M. Steinberg, L. V. Wood, R. Yarchoan, J. Zuckerman, A. Landay, and C. L. Mackall. 2001. A potential role for interleukin-7 in T-cell homeostasis. Blood 97:2983-2990.
12. Fry, T. J., and C. L. Mackall. 2002. Interleukin-7: from bench to clinic. Blood 99:3892-3904.
13. Goletti, D., D. Vincenti, S. Carrara, O. Butera, F. Bizzoni, G. Bernardini, M. Amicosante, and E. Girardi. 2005. Selected RD1 peptides for active tuberculosis diagnosis: comparison of a gamma interferon whole-blood enzyme-linked immunosorbent assay and an enzyme-linked immunospot assay. Clin. Diagn. Lab. Immunol. 12:1311-1316.
14. Guyot-Revol, V., J. A. Innes, S. Hackforth, T. Hinks, and A. Lalvani. 2006. Regulatory T cells are expanded in blood and disease sites in patients with tuberculosis. Am. J. Respir. Crit. Care Med. 173:803-810.
15. Harris, J. R., and J. Markl. 1999. Keyhole limpet hemocyanin (KLH): a biomedical review. Micron 30:597-623.
16. Hertoghe, T., A. Wajja, L. Ntambi, A. Okwera, M. A. Aziz, C. Hirsch, J. Johnson, Z. Toossi, R. Mugerwa, P. Mugyenyi, R. Colebunders, J. Ellner, and G. Vanham. 2000. T cell activation, apoptosis and cytokine dysregulation in the (co)pathogenesis of HIV and pulmonary tuberculosis (TB). Clin. Exp. Immunol. 122:350-357.
17. Hirsch, C. S., Z. Toossi, J. L. Johnson, H. Luzze, L. Ntambi, P. Peters, M. McHugh, A. Okwera, M. Joloba, P. Mugyenyi, R. D. Mugerwa, P. Terebuh, and J. J. Ellner. 2001. Augmentation of apoptosis and interferon-gamma production at sites of active Mycobacterium tuberculosis infection in human tuberculosis. J. Infect. Dis. 183:779-788.
18. Hirsch, C. S., Z. Toossi, C. Othieno, J. L. Johnson, S. K. Schwander, S. Robertson, R. S. Wallis, K. Edmonds, A. Okwera, R. Mugerwa, P. Peters, and J. J. Ellner. 1999. Depressed T-cell interferon-gamma responses in pulmonary tuberculosis: analysis of underlying mechanisms and modulation with therapy. J. Infect. Dis. 180:2069-2073.
19. Hougardy, J., S. Place, M. Hildebrand, A. Drowart, A. Debrie, C. Locht, and F. Mascart. 2007. Regulatory T cells depress immune responses to protective antigens in active tuberculosis. Am. J. Respir. Crit. Care Med. 176:409-416.
20. Huang, M., S. Sharma, L. X. Zhu, M. P. Keane, J. Luo, L. Zhang, M. D. Burdick, Y. Q. Lin, M. Dohadwala, B. Gardner, R. K. Batra, R. M. Strieter, and S. M. Dubinett. 2002. IL-7 inhibits fibroblast TGF-beta production and signaling in pulmonary fibrosis. J. Clin. Investig. 109:931-937.
21. Institute of Medicine. 2000. Ending neglect: the elimination of tuberculosis in the United States. National Academy Press, Washington, DC.
22. Jennes, W., L. Kestens, D. F. Nixon, and B. L. Shacklett. 2002. Enhanced ELISPOT detection of antigen-specific T cell responses from cryopreserved specimens with addition of both IL-7 and IL-15 - the Amplispot assay. J. Immunol. Methods 270:99-108.
23. + HIV-specific T cell immune response in vitro and are associated with favorable clinical markers of disease status. J. Exp. Med. 200:331-343.
24. Kondrack, R. M., J. Harbertson, J. T. Tan, M. E. McBreen, C. D. Surh, and L. M. Bradley. 2003. Interleukin 7 regulates the survival and generation of memory CD4 cells. J. Exp. Med. 198:1797-1806.
25. Lalvani, A., and K. A. Millington. 2007. T cell-based diagnosis of childhood tuberculosis infection. Curr. Opin. Infect. Dis. 20:264-271.
26. Leyten, E. M. S., S. M. Arend, C. Prins, F. G. J. Cobelens, T. H. M. Ottenhoff, and J. T. van Dissel. 2007. Discrepancy between Mycobacterium tuberculosis-specific gamma interferon release assays using short and prolonged in vitro incubation. Clin. Vaccine Immunol. 14:880-885.
27. Li, J., G. Huston, and S. L. Swain. 2003. IL-7 promotes the transition of CD4 effectors to persistent memory cells. J. Exp. Med. 198:1807-1815.
28. Lobato, M. N., J. C. Mohle-Boetani, and S. E. Royce. 2000. Missed opportunities for preventing tuberculosis among children younger than five years of age. Pediatrics 106:e75.
29. Managlia, E. Z., A. Landay, and L. Al-Harthi. 2005. Interleukin-7 signaling is sufficient to phenotypically and functionally prime human CD4 naïve T cells. Immunology 114:322-335.
30. Marais, B. J., S. M. Graham, M. F. Cotton, and N. Beyers. 2007. Diagnostic and management challenges for childhood tuberculosis in the era of HIV. J. Infect. Dis. 196(Suppl. 1):S76-S85.
31. Mazurek, G. H., P. A. LoBue, C. L. Daley, J. Bernardo, A. A. Lardizabal, W. R. Bishai, M. F. Iademarco, and J. S. Rothel. 2001. Comparison of a whole-blood interferon gamma assay with tuberculin skin testing for detecting latent Mycobacterium tuberculosis infection. JAMA 286:1740-1747.
32. Mazurek, G. H., J. Jereb, P. Lobue, M. F. Iademarco, B. Metchock, and A. Vernon. 2005. Guidelines for using the QuantiFERON-TB Gold test for detecting Mycobacterium tuberculosis infection, United States. MMWR Recommend. Rep. 54:49-55.
33. Mazurek, G. H., S. E. Weis, P. K. Moonan, C. L. Daley, J. Bernardo, A. A. Lardizabal, R. R. Reves, S. R. Toney, L. J. Daniels, and P. A. LoBue. 2007. Prospective comparison of the tuberculin skin test and 2 whole-blood interferon-gamma release assays in persons with suspected tuberculosis. Clin. Infect. Dis. 45:837-845.
34. Pai, M., L. W. Riley, and J. M. Colford. 2004. Interferon-gamma assays in the immunodiagnosis of tuberculosis: a systematic review. Lancet Infect. Dis. 4:761-776.
35. Piana, F., L. R. Codecasa, G. Besozzi, G. B. Migliori, and D. M. Cirillo. 2006. Use of commercial interferon-gamma assays in immunocompromised patients for tuberculosis diagnosis. Am. J. Respir. Crit. Care Med. 173:130.
36. + T cells are detectable in most individuals with active HIV-1 infection, but decline with prolonged viral suppression. Nat. Med. 5:518-525.
37. Rathmell, J. C., E. A. Farkash, W. Gao, and C. B. Thompson. 2001. IL-7 enhances the survival and maintains the size of naive T cells. J. Immunol. 167:6869-6876.
38. Ribeiro-Rodrigues, R., T. Resende Co, R. Rojas, Z. Toossi, R. Dietze, W. H. Boom, E. Maciel, and C. S. Hirsch. 2006. A role for CD4+CD25+ T cells in regulation of the immune response during human tuberculosis. Clin. Exp. Immunol. 144:25-34.
39. Rosenberg, S. A., C. Sportès, M. Ahmadzadeh, T. J. Fry, L. T. Ngo, S. L. Schwarz, M. Stetler-Stevenson, K. E. Morton, S. A. Mavroukakis, M. Morre, R. Buffet, C. L. Mackall, and R. E. Gress. 2006. IL-7 administration to humans leads to expansion of CD8+ and CD4+ cells but a relative decrease of CD4+ T-regulatory cells. J. Immunother. 29:313-319.
40. Scarpellini, P., S. Tasca, L. Galli, A. Beretta, A. Lazzarin, and C. Fortis. 2004. Selected pool of peptides from ESAT-6 and CFP-10 proteins for detection of Mycobacterium tuberculosis infection. J. Clin. Microbiol. 42:3469-3474.
41. Scripture-Adams, D. D., D. G. Brooks, Y. D. Korin, and J. A. Zack. 2002. Interleukin-7 induces expression of latent human immunodeficiency virus type 1 with minimal effects on T-cell phenotype. J. Virol. 76:13077- 13082.
42. Sharp, E. R., J. D. Barbour, R. K. Karlsson, K. A. Jordan, J. K. Sandberg, A. Wiznia, M. G. Rosenberg, and D. F. Nixon. 2005. Higher frequency of HIV-1-specific T cell immune responses in African American children vertically infected with HIV-1. J. Infect. Dis. 192:1772-1780.
43. Soini, H., X. Pan, A. Amin, E. A. Graviss, A. Siddiqui, and J. M. Musser. 2000. Characterization of Mycobacterium tuberculosis isolates from patients in Houston, Texas, by spoligotyping. J. Clin. Microbiol. 38:669-676.
44. Sonnenberg, P., J. R. Glynn, K. Fielding, J. Murray, P. Godfrey-Faussett, and S. Shearer. 2005. How soon after infection with HIV does the risk of tuberculosis start to increase? A retrospective cohort study in South African gold miners. J. Infect. Dis. 191:150-158.
45. Sportes, C., F. T. Hakim, S. A. Memon, H. Zhang, K. S. Chua, M. R. Brown, T. A. Fleisher, M. C. Krumlauf, R. R. Babb, C. K. Chow, T. J. Fry, J. Engels, R. Buffet, M. Morre, R. J. Amato, D. J. Venzon, R. Korngold, A. Pecora, R. E. Gress, and C. L. Mackall. 2008. Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naïve T cell subsets. J. Exp. Med. 205:1701-1714.
46. Subramanyam, S., L. E. Hanna, P. Venkatesan, K. Sankaran, P. R. Narayanan, and S. Swaminathan. 2004. HIV alters plasma and M. tuberculosis-induced cytokine production in patients with tuberculosis. J. Interferon Cytokine Res. 24:101-106.
47. Talayev, V. Y., I. Y. Zaichenko, O. N. Babaykina, M. A. Lomunova, E. B. Talayeva, and M. F. Nikonova. 2005. Ex vivo stimulation of cord blood mononuclear cells by dexamethasone and interleukin-7 results in the maturation of interferon-gamma-secreting effector memory T cells. Clin. Exp. Immunol. 141:440-448.
48. Taylor, R. E. B., A. J. Cant, and J. E. Clark. 2008. Potential effect of NICE tuberculosis guidelines on pediatric tuberculosis screening. Arch. Dis. Child. 93:200-203.
49. Vassena, L., M. Proschan, A. S. Fauci, and P. Lusso. 2007. Interleukin 7 reduces the levels of spontaneous apoptosis in CD4+ and CD8+ T cells from HIV-1-infected individuals. Proc. Natl. Acad. Sci. USA 104:2355-2360.