Highly pathogenic influenza virus infection of the thymus interferes with T lymphocyte development

Journal of Immunology

Volumn 185, Issue 8, 2010, Pages 4824-4834

  Vogel, Annette B ^a   Haasbach, Emanuel ^a   Reiling, Sarah J ^a   Droebner, Karoline ^a   Klingel, Karin ^b   Planz, Oliver ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNE SYSTEM; LUNG COMPLICATION; LYMPHOCYTOPENIA; MOUSE; NONHUMAN; ORGAN INJURY; PRIORITY JOURNAL; T LYMPHOCYTE; THYMUS; THYMUS DISEASE; ANIMAL; C57BL MOUSE; CELL COUNT; CELL SEPARATION; CYTOLOGY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INFLUENZA VIRUS A; LUNG; LYMPHOCYTE ACTIVATION; NEUTROPHIL CHEMOTAXIS; ORTHOMYXOVIRUS INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; CELL COUNT; CELL SEPARATION; CHEMOTAXIS, LEUKOCYTE; DENDRITIC CELLS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; INFLUENZA A VIRUS; LUNG; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORTHOMYXOVIRIDAE INFECTIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; THYMUS GLAND;

EID: 78049494052     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903631     Document Type: Article

References (48)

1. Maines, T. R., K. J. Szretter, L. Perrone, J. A. Belser, R. A. Bright, H. Zeng, T. M. Tumpey, and J. M. Katz. 2008. Pathogenesis of emerging avian influenza virusesinmammals and the host innate immune response. Immunol. Rev. 225:68-84.
2. Smallman-Raynor, M., and A. D. Cliff. 2007. Avian influenza A (H5N1) age distribution in humans. Emerg. Infect. Dis. 13:510-512.
3. Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza A (H5N1) Virus, Abdel-Ghafar A. N., T. Chotpitayasunondh, Z. Gao, F. G. Hayden, D. H. Nguyen, M. D. de Jong, A. Naghdaliyev, J. S. Peiris, N. Shindo, S. Soeroso, and T. M. Uyeki. 2008. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 358:261-273.
4. Tran, T. H., T. L. Nguyen, T. D. Nguyen, T. S. Luong, P. M. Pham, V. C. Nguyen, T. S. Pham, C. D. Vo, T. Q. Le, T. T. Ngo, et al; World Health Organization International Avian Influenza Investigative Team. 2004. Avian influenza A (H5N1) in 10 patients in Vietnam. N. Engl. J. Med. 350:1179-1188.
5. Kandun, I. N., H. Wibisono, E. R. Sedyaningsih, Yusharmen, W. Hadisoedarsuno, W. Purba, H. Santoso, C. Septiawati, E. Tresnaningsih, B. Heriyanto, et al. 2006. Three Indonesian clusters of H5N1 virus infection in 2005. N. Engl. J. Med. 355:2186-2194.
6. Taubenberger, J. K., A. H. Reid, T. A. Janczewski, and T. G. Fanning. 2001. Integrating historical, clinical and molecular genetic data in order to explain the origin and virulence of the 1918 Spanish influenza virus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:1829-1839.
7. Centers for Disease Control and Prevention (CDC). 2009. Update: novel influenza A (H1N1) virus infection - Mexico, March-May, 2009. MMWR Morb. Mortal. Wkly. Rep. 58:585-589.
8. Chuang, V. W., T. Y. Wong, Y. H. Leung, E. S. Ma, Y. L. Law, O. T. Tsang, K. M. Chan, I. H. Tsang, T. L. Que, R. W. Yung, and S. H. Liu. 2008. Review ofdengue fever cases in Hong Kong during 1998 to 2005. Hong Kong Med. J. 14:170-177.
9. Baize, S., P. Marianneau, P. Loth, S. Reynard, A. Journeaux, M. Chevallier, N. Tordo, V. Deubel, and H. Contamin. 2009. Early and strong immune responses are associated with control of viral replication and recovery in Lassa virus-infected cynomolgus monkeys. J. Virol. 83:5890-5903.
10. Hsieh, S. M., and S. C. Chang. 2006. Insufficient perforin expression in CD8+ T cells in response to hemagglutinin from avian influenza (H5N1) virus. J. Immunol. 176:4530-4533.
11. Korteweg, C., and J. Gu. 2008. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172:1155-1170.
12. Geenen, V., J. F. Poulin, M. L. Dion, H. Martens, E. Castermans, I. Hansenne, M. Moutschen, R. P. Sékaly, and R. Cheynier. 2003. Quantification of T cell receptor rearrangement excision circles to estimate thymic function: an important new tool for endocrine-immune physiology. J. Endocrinol. 176:305-311.
13. Hale, J. S., T. E. Boursalian, G. L. Turk, and P. J. Fink. 2006. Thymic output in aged mice. Proc. Natl. Acad. Sci. USA 103:8447-8452.
14. Holländer, G. A., and P. Peterson. 2009. Learning to be tolerant: how T cells keep out of trouble. J. Intern. Med. 265:541-561.
15. Li, J., J. Park, D. Foss, and I. Goldschneider. 2009. Thymus-homing peripheral dendritic cells constitute two of the three major subsets of dendritic cells in the steady-state thymus. J. Exp. Med. 206:607-622.
16. Bonasio, R., M. L. Scimone, P. Schaerli, N. Grabie, A. H. Lichtman, and U. H. von Andrian. 2006. Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat. Immunol. 7:1092-1100.
17. Perrone, L. A., J. K. Plowden, A. García-Sastre, J. M. Katz, and T. M. Tumpey. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4: e1000115.
18. Harari, A., F. B. Enders, C. Cellerai, P. A. Bart, and G. Pantaleo. 2009. Distinct profiles of cytotoxic granules in memory CD8 T cells correlate with function, differentiation stage, and antigen exposure. J. Virol. 83:2862-2871.
19. Savino, W., M. Dardenne, L. A. Velloso, and S. Dayse Silva-Barbosa. 2007. The thymus is a common target in malnutrition and infection. Br. J. Nutr. 98 (Suppl 1): S11-S16.
20. Borgherini, G., P. Poubeau, F. Staikowsky, M. Lory, N. Le Moullec, J. P. Becquart, C. Wengling, A. Michault, and F. Paganin. 2007. Outbreak of chikungunya on Reunion Island: early clinical and laboratory features in 157 adult patients. Clin. Infect. Dis. 44:1401-1407.
21. Salguero, F. J., M. A. Sánchez-Martín, F. Díaz-San Segundo, A. de Avila, and N. Sevilla. 2005. Foot-and-mouth disease virus (FMDV) causes an acute disease that can be lethal for adult laboratory mice. Virology 332:384-396.
22. Panesar, N. S. 2008. What caused lymphopenia in SARS and how reliable is the lymphokine status in glucocorticoid-treated patients? Med. Hypotheses 71:298-301.
23. Law, H. K., C. Y. Cheung, H. Y. Ng, S. F. Sia, Y. O. Chan, W. Luk, J. M. Nicholls, J. S. Peiris, and Y. L. Lau. 2005. Chemokine up-regulation in SARS-coronavirus-infected, monocyte-derived human dendritic cells. Blood 106:2366-2374.
24. Cunha, B. A. 2004. Differential diagnosis of West Nile encephalitis. Curr. Opin. Infect. Dis. 17:413-420.
25. Droebner, K., E. Haasbach, C. Fuchs, A. O. Weinzierl, S. Stevanovic, M. Büttner, and O. Planz. 2008. Antibodies and CD4 (+) T-cells mediate crossprotection against H5N1 influenza virus infection in mice after vaccination with a low pathogenic H5N2 strain. Vaccine 26:6965-6974.
26. Spackman, E., D. A. Senne, T. J. Myers, L. L. Bulaga, L. P. Garber, M. L. Perdue, K. Lohman, L. T. Daum, and D. L. Suarez. 2002. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J. Clin. Microbiol. 40:3256-3260.
27. Planz, O., T. Bilzer, M. Sobbe, and L. Stitz. 1993. Lysis of major histocompatibility complex class I-bearing cells in Borna disease virus-induced degenerative encephalopathy. J. Exp. Med. 178:163-174.
28. Gabriel, G., K. Klingel, O. Planz, K. Bier, A. Herwig, M. Sauter, and H. D. Klenk. 2009. Spread of infection and lymphocyte depletion in mice depends on polymerase of influenza virus. Am. J. Pathol. 175:1178-1186.
29. Klingel, K., C. Hohenadl, A. Canu, M. Albrecht, M. Seemann, G. Mall, and R. Kandolf. 1992. Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proc. Natl. Acad. Sci. USA 89:314-318.
30. Hao, X., T. S. Kim, and T. J. Braciale. 2008. Differential response of respiratory dendritic cell subsets to influenza virus infection. J. Virol. 82:4908-4919.
31. Droebner, K., C. Ehrhardt, A. Poetter, S. Ludwig, and O. Planz. 2007. CYS-TUS052, a polyphenol-rich plant extract, exerts anti-influenza virus activity in mice. Antiviral Res. 76:1-10.
32. Coskun, O., I. Y. Avci, K. Sener, H. Yaman, R. Ogur, H. Bodur, and C. P. Eyigün. 2010. Relative lymphopenia and monocytosis may be considered as a surrogate marker of pandemic influenza a (H1N1). J. Clin. Virol. 47:388-389.
33. Savino, W., D. A. Mendes-da-Cruz, J. S. Silva, M. Dardenne, and V. Cotta-de-Almeida. 2002. Intrathymic T-cell migration: a combinatorial interplay of extracellular matrix and chemokines? Trends Immunol. 23:305-313.
34. Ara, T., M. Itoi, K. Kawabata, T. Egawa, K. Tokoyoda, T. Sugiyama, N. Fujii, T. Amagai, and T. Nagasawa. 2003. A role of CXC chemokine ligand 12/stromal cell-derived factor-1/pre-B cell growth stimulating factor and its receptor CXCR4 in fetal and adult T cell development in vivo. J. Immunol. 170:4649-4655.
35. Suzuki, G., H. Sawa, Y. Kobayashi, Y. Nakata, K. Nakagawa, A. Uzawa, H. Sakiyama, S. Kakinuma, K. Iwabuchi, and K. Nagashima. 1999. Pertussis toxin-sensitive signal controls the trafficking of thymocytes across the corticomedullary junction in the thymus. J. Immunol. 162:5981-5985.
36. Mendes-da-Cruz, D. A., J. S. Silva, V. Cotta-de-Almeida, and W. Savino. 2006. Altered thymocyte migration during experimental acute Trypanosoma cruzi infection: combined role of fibronectin and the chemokines CXCL12 and CCL4. Eur. J. Immunol. 36:1486-1493.
37. Cao, B., X. W. Li, Y. Mao, J. Wang, H. Z. Lu, Y. S. Chen, Z. A. Liang, L. Liang, S. J. Zhang, B. Zhang, et al; National Influenza A Pandemic (H1N1) 2009 Clinical Investigation Group of China. 2009. Clinical features of the initial cases of 2009 pandemic influenza A (H1N1) virus infection in China. N. Engl. J. Med. 361:2507-2517.
38. Hale, J. S., and P. J. Fink. 2009. Back to the thymus: peripheral T cells come home. Immunol. Cell Biol. 87:58-64.
39. Hardy, C. L., D. I. Godfrey, and R. Scollay. 2001. The effect of antigen stimulation on the migration of mature T cells from the peripheral lymphoid tissues to the thymus. Dev. Immunol. 8:123-131.
40. Mori, K., M. Itoi, N. Tsukamoto, H. Kubo, and T. Amagai. 2007. The perivascular space as a path of hematopoietic progenitor cells and mature T cells between the blood circulation and the thymic parenchyma. Int. Immunol. 19:745-753.
41. Song, F., Z. Guan, I. E. Gienapp, T. Shawler, J. Benson, and C. C. Whitacre. 2006. The thymus plays a role in oral tolerance in experimental autoimmune encephalomyelitis. J. Immunol. 177:1500-1509.
42. Liblau, R. S., R. Tisch, K. Shokat, X. Yang, N. Dumont, C. C. Goodnow, and H. O. McDevitt. 1996. Intravenous injection of soluble antigen induces thymic and peripheral T-cells apoptosis. Proc. Natl. Acad. Sci. USA 93:3031-3036.
43. Marodon, G., S. Fisson, B. Levacher, M. Fabre, B. L. Salomon, and D. Klatzmann. 2006. Induction of antigen-specific tolerance by intrathymic injection of lentiviral vectors. Blood 108:2972-2978.
44. Cabarrocas, J., C. Cassan, F. Magnusson, E. Piaggio, L. Mars, J. Derbinski, B. Kyewski, D. A. Gross, B. L. Salomon, K. Khazaie, et al. 2006. Foxp3+ CD25+ regulatory T cells specific for a neo-self-antigen develop at the double-positive thymic stage. Proc. Natl. Acad. Sci. USA 103:8453-8458.
45. Proietto, A. I., S. van Dommelen, P. Zhou, A. Rizzitelli, A. D'Amico, R. J. Steptoe, S. H. Naik, M. H. Lahoud, Y. Liu, P. Zheng, et al. 2008. Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc. Natl. Acad. Sci. USA 105:19869-19874.
46. Coombes, J. L., K. R. Siddiqui, C. V. Arancibia-Cárcamo, J. Hall, C. M. Sun, Y. Belkaid, and F. Powrie. 2007. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204:1757-1764.
47. Proietto, A. I., S. van Dommelen, and L. Wu. 2009. The impact of circulating dendritic cells on the development and differentiation of thymocytes. Immunol. Cell Biol. 87:39-45.
48. Perez-Padilla, R., D. de la Rosa-Zamboni, L. S. Ponce de Leon, M. Hernandez, F. Quiñones-Falconi, E. Bautista, A. Ramirez-Venegas, J. Rojas-Serrano, C. E. Ormsby, A. Corrales, et al. INER Working Group on Influenza. 2009. Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N. Engl. J. Med. 361:680-689.