Pulmonary Tuberculosis in Humanized Mice Infected with HIV-1

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Nusbaum, Rebecca J ^a   Calderon, Veronica E ^b   Huante, Matthew B ^a   Sutjita, Putri ^a   Vijayakumar, Sudhamathi ^a   Lancaster, Katrina L ^a   Hunter, Robert L ^c   Actor, Jeffrey K ^c   Cirillo, Jeffrey D ^d   Aronson, Judith ^a   Gelman, Benjamin B ^a   Lisinicchia, Joshua G ^a   Valbuena, Gustavo ^a   Endsley, Janice J ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b UNIVERSITY OF TEXAS AT EL PASO   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; DISEASE MODEL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; LUNG; LUNG TUBERCULOSIS; MICROBIOLOGY; MIXED INFECTION; MOUSE; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; VIROLOGY;

ANIMALS; COINFECTION; DISEASE MODELS, ANIMAL; HIV INFECTIONS; HIV-1; IMMUNOCOMPROMISED HOST; LUNG; MICE; NEUTROPHIL INFILTRATION; TUBERCULOSIS, PULMONARY;

EID: 84959422471     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21522     Document Type: Article

References (62)

1. Organization, W. H. (World Health Organization, Geneva, 2014).
2. Harries, A. D., Lawn, S. D., Getahun, H., Zachariah, R. & Havlir, D. V. HIV and tuberculosis-science and implementation to turn the tide and reduce deaths. J Int AIDS Soc 15, 17396 (2012).
3. Khan, F. A. et al. Treatment of active tuberculosis in HIV-coinfected patients: a systematic review and meta-analysis. Clin Infect Dis 50, 1288-99 (2010).
4. Law, K. F., Jagirdar, J., Weiden, M. D., Bodkin, M. & Rom, W. N. Tuberculosis in HIV-positive patients: cellular response and immune activation in the lung. Am J Respir Crit Care Med 153, 1377-84 (1996).
5. Markowitz, N. et al. Incidence of tuberculosis in the United States among HIV-infected persons. The Pulmonary Complications of HIV Infection Study Group. Ann Intern Med 126, 123-32 (1997).
6. Mukadi, Y. et al. Spectrum of immunodeficiency in HIV-1-infected patients with pulmonary tuberculosis in Zaire. Lancet 342, 143-6 (1993).
7. Naidoo, K., Baxter, C. & Abdool Karim, S. S. When to start antiretroviral therapy during tuberculosis treatment? Curr Opin Infect Dis 26, 35-42 (2013).
8. McShane, H. Co-infection with HIV and TB: double trouble. Int J STD AIDS 16, 95-100; quiz 101 (2005).
9. Diedrich, C. R. & Flynn, J. L. HIV-1/mycobacterium tuberculosis coinfection immunology: how does HIV-1 exacerbate tuberculosis? Infect Immun 79, 1407-17 (2011).
10. Diedrich, C. R. et al. Reactivation of latent tuberculosis in cynomolgus macaques infected with SIV is associated with early peripheral T cell depletion and not virus load. PLoS One 5, e9611 (2010).
11. Mehra, S. et al. Reactivation of latent tuberculosis in rhesus macaques by coinfection with simian immunodeficiency virus. J Med Primatol 40, 233-43 (2011).
12. Hanson, D. L., Chu, S. Y., Farizo, K. M. & Ward, J. W. Distribution of CD4 + T lymphocytes at diagnosis of acquired immunodeficiency syndrome-defining and other human immunodeficiency virus-related illnesses. The Adult and Adolescent Spectrum of HIV Disease Project Group. Arch Intern Med 155, 1537-42 (1995).
13. Bezuidenhout, J., Roberts, T., Muller, L., van Helden, P. & Walzl, G. Pleural tuberculosis in patients with early HIV infection is associated with increased TNF-alpha expression and necrosis in granulomas. PLoS One 4, e4228 (2009).
14. de Noronha, A. L., Bafica, A., Nogueira, L., Barral, A. & Barral-Netto, M. Lung granulomas from Mycobacterium tuberculosis/HIV- 1 co-infected patients display decreased in situ TNF production. Pathol Res Pract 204, 155-61 (2008).
15. Plaza, V. et al. Bronchoalveolar lavage cell analysis in patients with human immunodeficiency virus related diseases. Thorax 44, 289-91 (1989).
16. Brainard, D. M. et al. Induction of robust cellular and humoral virus-specific adaptive immune responses in human immunodeficiency virus-infected humanized BLT mice. J Virol 83, 7305-21 (2009).
17. Choudhary, S. K. et al. Latent HIV-1 infection of resting CD4(+) T cells in the humanized Rag2(-)/(-) gammac(-)/(-) mouse. J Virol 86, 114-20 (2012).
18. Dudek, T. E. et al. Rapid evolution of HIV-1 to functional CD8(+) T cell responses in humanized BLT mice. Sci Transl Med 4, 143ra98 (2012).
19. Melkus, M. W. et al. Humanized mice mount specific adaptive and innate immune responses to EBV and TSST-1. Nat Med 12, 1316-22 (2006).
20. Calderon, V. E. et al. A humanized mouse model of tuberculosis. PLoS One 8, e63331 (2013).
21. Orme, I. M. A new unifying theory of the pathogenesis of tuberculosis. Tuberculosis (Edinb) 94, 8-14 (2014).
22. Hunter, R. L., Actor, J. K., Hwang, S. A., Karev, V. & Jagannath, C. Pathogenesis of post primary tuberculosis: immunity and hypersensitivity in the development of cavities. Ann Clin Lab Sci 44, 365-87 (2014).
23. Houben, R. M. et al. Human immunodeficiency virus associated tuberculosis more often due to recent infection than reactivation of latent infection. Int J Tuberc Lung Dis 15, 24-31 (2011).
24. Crampin, A. C. et al. Recurrent TB: relapse or reinfection? The effect of HIV in a general population cohort in Malawi. AIDS 24, 417-26 (2010).
25. Sonnenberg, P. et al. HIV-1 and recurrence, relapse, and reinfection of tuberculosis after cure: a cohort study in South African mineworkers. Lancet 358, 1687-93 (2001).
26. Berges, B. K. & Rowan, M. R. The utility of the new generation of humanized mice to study HIV-1 infection: transmission, prevention, pathogenesis, and treatment. Retrovirology 8, 65 (2011).
27. Sun, Z. et al. Intrarectal transmission, systemic infection, and CD4 + T cell depletion in humanized mice infected with HIV-1. J Exp Med 204, 705-14 (2007).
28. Orme, I. M. Development of new vaccines and drugs for TB: limitations and potential strategic errors. Future Microbiol 6, 161-77 (2011).
29. Hoff, D. R. et al. Location of intra- and extracellular M. tuberculosis populations in lungs of mice and Guinea pigs during disease progression and after drug treatment. PLoS One 6, e17550 (2011).
30. Ridley, D. S. & Ridley, M. J. Rationale for the histological spectrum of tuberculosis. A basis for classification. Pathology 19, 186-92 (1987).
31. Mattila, J. T. et al. Microenvironments in tuberculous granulomas are delineated by distinct populations of macrophage subsets and expression of nitric oxide synthase and arginase isoforms. J Immunol 191, 773-84 (2013).
32. Pedrosa, J. et al. Neutrophils play a protective nonphagocytic role in systemic Mycobacterium tuberculosis infection of mice. Infect Immun 68, 577-83 (2000).
33. Yang, C. T. et al. Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 12, 301-12 (2012).
34. Fullerton, D. G. et al. Pulmonary tuberculosis presenting with central retinal vein occlusion. Br J Ophthalmol 91, 1714-5 (2007).
35. Elkeslassy, A. et al. Dilatation of deep medullary veins in cortical venous occlusion due to focal tuberculous leptomeningitis. Neuroradiology 39, 705-7 (1997).
36. Sheen-Chen, S. M. et al. Computed tomography and angiography in hepatic tuberculosis mimicking liver tumor. Int J Tuberc Lung Dis 5, 876-8 (2001).
37. Equi, A. et al. Pulmonary artery occlusion from tuberculous lymphadenopathy in a child. Pediatr Pulmonol 31, 311-3 (2001).
38. Takeuchi, H. et al. Splenic vein occlusion secondary to tuberculous lymphadenitis at the splenic hilum: report of a case. Surg Today 30, 383-5 (2000).
39. Collins, J., Blankenbaker, D. & Stern, E. J. CT patterns of bronchiolar disease: what is "tree-in-bud"? AJR Am J Roentgenol 171, 365-70 (1998).
40. Hunter, R. L., Jagannath, C. & Actor, J. K. Pathology of postprimary tuberculosis in humans and mice: contradiction of long-held beliefs. Tuberculosis (Edinb) 87, 267-78 (2007).
41. Ghiglione, Y. & Turk, G. Nef performance in macrophages: the master orchestrator of viral persistence and spread. Curr HIV Res 9, 505-13 (2011).
42. Li, J. C., Yim, H. C. & Lau, A. S. Role of HIV-1 Tat in AIDS pathogenesis: its effects on cytokine dysregulation and contributions to the pathogenesis of opportunistic infection. AIDS 24, 1609-23 (2010).
43. Imperiali, F. G. et al. Increased Mycobacterium tuberculosis growth in HIV-1-infected human macrophages: role of tumour necrosis factor-alpha. Clin Exp Immunol 123, 435-42 (2001).
44. Jambo, K. C. et al. Small alveolar macrophages are infected preferentially by HIV and exhibit impaired phagocytic function. Mucosal Immunol 7, 1116-26 (2014).
45. Polyak, S. et al. Impaired class II expression and antigen uptake in monocytic cells after HIV-1 infection. J Immunol 159, 2177-88 (1997).
46. Caccamo, N. et al. Analysis of Mycobacterium tuberculosis-specific CD8 T-cells in patients with active tuberculosis and in individuals with latent infection. PLoS One 4, e5528 (2009).
47. Fahey, J. L. et al. Prognostic significance of plasma markers of immune activation, HIV viral load and CD4 T-cell measurements. AIDS 12, 1581-90 (1998).
48. Ongaya, A. et al. Mycobacterium tuberculosis-specific CD8 + T cell recall in convalescing TB subjects with HIV co-infection. Tuberculosis (Edinb) 93 Suppl, S60-5 (2013).
49. Mellors, J. W. et al. Plasma viral load and CD4 + lymphocytes as prognostic markers of HIV-1 infection. Ann Intern Med 126, 946-54 (1997).
50. Nakata, K. et al. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am J Respir Crit Care Med 155, 996-1003 (1997).
51. Seiler, P. et al. Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol 33, 2676-86 (2003).
52. Marzo, E. et al. Damaging role of neutrophilic infiltration in a mouse model of progressive tuberculosis. Tuberculosis (Edinb) 94, 55-64 (2014).
53. Cardona, P. J. et al. Towards a 'human-like' model of tuberculosis: intranasal inoculation of LPS induces intragranulomatous lung necrosis in mice infected aerogenically with Mycobacterium tuberculosis. Scand J Immunol 53, 65-71 (2001).
54. Kerkhoff, A. D., Wood, R., Lowe, D. M., Vogt, M. & Lawn, S. D. Blood neutrophil counts in HIV-infected patients with pulmonary tuberculosis: association with sputum mycobacterial load. PLoS One 8, e67956 (2013).
55. Cooper, A. M. et al. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178, 2243-7 (1993).
56. Ottenhoff, T. H., Kumararatne, D. & Casanova, J. L. Novel human immunodeficiencies reveal the essential role of type-I cytokines in immunity to intracellular bacteria. Immunol Today 19, 491-4 (1998).
57. Tobin, D. M., Roca, F. J., Ray, J. P., Ko, D. C. & Ramakrishnan, L. An enzyme that inactivates the inflammatory mediator leukotriene b4 restricts mycobacterial infection. PLoS One 8, e67828 (2013).
58. Vilaplana, C. et al. Ibuprofen therapy resulted in significantly decreased tissue bacillary loads and increased survival in a new murine experimental model of active tuberculosis. J Infect Dis 208, 199-202 (2013).
59. Kong, Y. et al. Whole-body imaging of infection using fluorescence. Curr Protoc Microbiol Chapter 2, Unit 2C 3 (2011).
60. Endsley, J. J. et al. Mycobacterium bovis BCG vaccination induces memory CD4 + T cells characterized by effector biomarker expression and anti-mycobacterial activity. Vaccine 25, 8384-94 (2007).
61. Hwang, S. A., Wilk, K., Kruzel, M. L. & Actor, J. K. A novel recombinant human lactoferrin augments the BCG vaccine and protects alveolar integrity upon infection with Mycobacterium tuberculosis in mice. Vaccine 27, 3026-34 (2009).
62. Massey, S. et al. Comparative Burkholderia pseudomallei natural history virulence studies using an aerosol murine model of infection. Sci Rep 4, 4305 (2014).