Chapter 8
Non-Human Primate Models of Tuberculosis
Juliet C. Peña,
Wen-Zhe Ho,
Juliet C. Peña
Department of Pathology and Laboratory Medicine, Temple University Lewis Katz School of Medicine, Philadelphia, PA, 19140
Search for more papers by this authorWen-Zhe Ho
Department of Pathology and Laboratory Medicine, Temple University Lewis Katz School of Medicine, Philadelphia, PA, 19140
Animal Biosafety Level III Laboratory at the Center for Animal Experiment, State Key Laboratory of Virology, Wuhan University, Wuhan, China
Search for more papers by this authorJuliet C. Peña,
Wen-Zhe Ho,
Juliet C. Peña
Department of Pathology and Laboratory Medicine, Temple University Lewis Katz School of Medicine, Philadelphia, PA, 19140
Search for more papers by this authorWen-Zhe Ho
Department of Pathology and Laboratory Medicine, Temple University Lewis Katz School of Medicine, Philadelphia, PA, 19140
Animal Biosafety Level III Laboratory at the Center for Animal Experiment, State Key Laboratory of Virology, Wuhan University, Wuhan, China
Search for more papers by this authorBook Editor(s):William R. Jacobs Jr.,
Helen McShane,
Valerie Mizrahi,
Ian M. Orme,
William R. Jacobs Jr.
Department of Immunology and Microbiology, Albert Einstein School of Medicine, Bronx, New York
Search for more papers by this authorHelen McShane
Cellular Immunology and Vaccine Development Group, Nuffield Department of Medicine, Jenner Institute, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorValerie Mizrahi
Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Faculty of Health Sciences, Rondebosch, South Africa
Search for more papers by this authorIan M. Orme
Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado
Search for more papers by this authorFirst published: 01 September 2017
Summary
Among the animal models of tuberculosis (TB), the non-human primates (NHPs), particularly rhesus macaques (Macaca fascicularis) and cynomolgus macaques (Macaca mulatta), share the greatest anatomical and physiological similarities with humans. Macaques are highly susceptible to Mycobacterium tuberculosis infection and manifest the complete spectrum of clinical and pathological manifestations of TB as seen in humans. Therefore, the macaque models have been used extensively for investigating the pathogenesis of M. tuberculosis infection and for preclinical testing of drugs and vaccines against TB. This review focuses on published major studies that exemplify how the rhesus and cynomolgus macaques have enhanced and may continue to advance global efforts in TB research.
References
- Ackermann, RR (ed). 2003. A comparative primate dissection guide, version 1.0. See more at http://www.archaeology.uct.ac.za/age/faculty-and-staff/rebecca-rogers-ackermann#sthash.M7Y7sPzv.dpuf.
- Carlsson, HE, Schapiro, SJ, Farah, I, Hau, J. 2004. Use of primates in research: a global overview. Am J Primatol 63: 225–237.
- O'Neil, RM, Ashack, RJ, Goodman, FR. 1981. A comparative study of the respiratory responses to bronchoactive agents in rhesus and cynomolgus monkeys. J Pharmacol Methods 5: 267–273.
- Capuano, SV III, Croix, DA, Pawar, S, Zinovik, A, Myers, A, Lin, PL, Bissel, S, Fuhrman, C, Klein, E, Flynn, JL. 2003. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect Immun 71: 5831–5844.
- Flynn, JL. 2006. Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect 8: 1179–1188.
- Wolf, RH, Gibson, SV, Watson, EA, Baskin, GB. 1988. Multidrug chemotherapy of tuberculosis in rhesus monkeys. Lab Anim Sci 38: 25–33.
- Schmidt, LH. 1966. Studies on the antituberculous activity of ethambutol in monkeys. Ann N Y Acad Sci 135(2 New Antituber): 747–758.
- Darrah, PA, Bolton, DL, Lackner, AA, Kaushal, D, Aye, PP, Mehra, S, Blanchard, JL, Didier, PJ, Roy, CJ, Rao, SS, Hokey, DA, Scanga, CA, Sizemore, DR, Sadoff, JC, Roederer, M, Seder, RA. 2014. Aerosol vaccination with AERAS-402 elicits robust cellular immune responses in the lungs of rhesus macaques but fails to protect against high-dose Mycobacterium tuberculosis challenge. J Immunol 193: 1799–1811.
- Mehra, S, Alvarez, X, Didier, PJ, Doyle, LA, Blanchard, JL, Lackner, AA, Kaushal, D. 2013. Granuloma correlates of protection against tuberculosis and mechanisms of immune modulation by Mycobacterium tuberculosis . J Infect Dis 207: 1115–1127.
- Larsen, MH, Biermann, K, Chen, B, Hsu, T, Sambandamurthy, VK, Lackner, AA, Aye, PP, Didier, P, Huang, D, Shao, L, Wei, H, Letvin, NL, Frothingham, R, Haynes, BF, Chen, ZW, Jacobs, WR Jr. 2009. Efficacy and safety of live attenuated persistent and rapidly cleared Mycobacterium tuberculosis vaccine candidates in non-human primates. Vaccine 27: 4709–4717.
- McMurray, DN. 2000. A nonhuman primate model for preclinical testing of new tuberculosis vaccines. Clin Infect Dis 30(Suppl 3): S210–S212.
- Good, RC. 1968. Biology of the mycobacterioses. Simian tuberculosis: immunologic aspects. Ann N Y Acad Sci 154(1 Biology of My): 200–213.
- Barclay, WR, Anacker, RL, Brehmer, W, Leif, W, Ribi, E. 1970. Aerosol-induced tuberculosis in subhuman primates and the course of the disease after intravenous BCG vaccination. Infect Immun 2: 574–582.
- Baram, P, Soltysik, L, Condoulis, W. 1971. The in vitro assay of tuberculin hypersensitivity in Macaca mulatta sensitized with bacille Calmette Guerin cell wall vaccine and-or infected with virulent Mycobacterium tuberculosis . Lab Anim Sci 21: 727–733.
- Ribi, E, Anacker, RL, Barclay, WR, Brehmer, W, Harris, SC, Leif, WR, Simmons, J. 1971. Efficacy of mycobacterial cell walls as a vaccine against airborne tuberculosis in the Rheusus monkey. J Infect Dis 123: 527–538.
- Barclay, WR, Busey, WM, Dalgard, DW, Good, RC, Janicki, BW, Kasik, JE, Ribi, E, Ulrich, CE, Wolinsky, E. 1973. Protection of monkeys against airborne tuberculosis by aerosol vaccination with bacillus Calmette-Guerin. Am Rev Respir Dis 107: 351–358.
- Janicki, BW, Good, RC, Minden, P, Affronti, LF, Hymes, WF. 1973. Immune responses in rhesus monkeys after bacillus Calmette-Guerin vaccination and aerosol challenge with Mycobacterium tuberculosis . Am Rev Respir Dis 107: 359–366.
- Chaparas, SD, Good, RC, Janicki, BW. 1975. Tuberculin-induced lymphocyte transformation and skin reactivity in monkeys vaccinated or not vaccinated with Bacille Calmette-Guérin, then challenged with virulent Mycobacterium tuberculosis . Am Rev Respir Dis 112: 43–47.
- Harper, GJ, Morton, JD. 1953. The respiratory retention of bacterial aerosols: experiments with radioactive spores. J Hyg (Lond) 51: 372–385.
- Walsh, GP, Tan, EV, dela Cruz, EC, Abalos, RM, Villahermosa, LG, Young, LJ, Cellona, RV, Nazareno, JB, Horwitz, MA. 1996. The Philippine cynomolgus monkey (Macaca fasicularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med 2: 430–436.
- Gormus, BJ, Blanchard, JL, Alvarez, XH, Didier, PJ. 2004. Evidence for a rhesus monkey model of asymptomatic tuberculosis. J Med Primatol 33: 134–145.
- Lewinsohn, DM, Tydeman, IS, Frieder, M, Grotzke, JE, Lines, RA, Ahmed, S, Prongay, KD, Primack, SL, Colgin, LM, Lewis, AD, Lewinsohn, DA. 2006. High resolution radiographic and fine immunologic definition of TB disease progression in the rhesus macaque. Microbes Infect 8: 2587–2598.
- Magalhaes, I, Sizemore, DR, Ahmed, RK, Mueller, S, Wehlin, L, Scanga, C, Weichold, F, Schirru, G, Pau, MG, Goudsmit, J, Kühlmann-Berenzon, S, Spångberg, M, Andersson, J, Gaines, H, Thorstensson, R, Skeiky, YA, Sadoff, J, Maeurer, M. 2008. rBCG induces strong antigen-specific T cell responses in rhesus macaques in a prime-boost setting with an adenovirus 35 tuberculosis vaccine vector. PLoS One 3:e3790.
- Rahman, S, Magalhaes, I, Rahman, J, Ahmed, RK, Sizemore, DR, Scanga, CA, Weichold, F, Verreck, F, Kondova, I, Sadoff, J, Thorstensson, R, Spångberg, M, Svensson, M, Andersson, J, Maeurer, M, Brighenti, S. 2012. Prime-boost vaccination with rBCG/rAd35 enhances CD8+ cytolytic T-cell responses in lesions from Mycobacterium tuberculosis-infected primates. Mol Med 18: 647–658.
- Verreck, FA, Vervenne, RA, Kondova, I, van Kralingen, KW, Remarque, EJ, Braskamp, G, van der Werff, NM, Kersbergen, A, Ottenhoff, TH, Heidt, PJ, Gilbert, SC, Gicquel, B, Hill, AV, Martin, C, McShane, H, Thomas, AW. 2009. MVA.85A boosting of BCG and an attenuated, phoP deficient M. tuberculosis vaccine both show protective efficacy against tuberculosis in rhesus macaques. PLoS One 4:e5264. (Erratum 6: doi:10.1371/annotation/e599dafd-8208-4655-a792-21cb125f7f66).
- Sharpe, SA, McShane, H, Dennis, MJ, Basaraba, RJ, Gleeson, F, Hall, G, McIntyre, A, Gooch, K, Clark, S, Beveridge, NE, Nuth, E, White, A, Marriott, A, Dowall, S, Hill, AV, Williams, A, Marsh, PD. 2010. Establishment of an aerosol challenge model of tuberculosis in rhesus macaques and an evaluation of endpoints for vaccine testing. Clin Vaccine Immunol 17: 1170–1182.
- Mehra, S, Pahar, B, Dutta, NK, Conerly, CN, Philippi-Falkenstein, K, Alvarez, X, Kaushal, D. 2010. Transcriptional reprogramming in nonhuman primate (rhesus macaque) tuberculosis granulomas. PLoS One 5:e12266.
- Dutta, NK, Mehra, S, Didier, PJ, Roy, CJ, Doyle, LA, Alvarez, X, Ratterree, M, Be, NA, Lamichhane, G, Jain, SK, Lacey, MR, Lackner, AA, Kaushal, D. 2010. Genetic requirements for the survival of tubercle bacilli in primates. J Infect Dis 201: 1743–1752.
- Zhang, J, Ye, YQ, Wang, Y, Mo, PZ, Xian, QY, Rao, Y, Bao, R, Dai, M, Liu, JY, Guo, M, Wang, X, Huang, ZX, Sun, LH, Tang, ZJ, Ho, WZ. 2011. M. tuberculosis H37Rv infection of Chinese rhesus macaques. J Neuroimmune Pharmacol 6: 362–370.
- Zhang, J, Xian, Q, Guo, M, Huang, Z, Rao, Y, Wang, Y, Wang, X, Bao, R, Evans, TG, Hokey, D, Sizemore, D, Ho, WZ. 2014. Mycobacterium tuberculosis Erdman infection of rhesus macaques of Chinese origin. Tuberculosis (Edinb) 94: 634–643.
- Mehra, S, Golden, NA, Dutta, NK, Midkiff, CC, Alvarez, X, Doyle, LA, Asher, M, Russell-Lodrigue, K, Monjure, C, Roy, CJ, Blanchard, JL, Didier, PJ, Veazey, RS, Lackner, AA, Kaushal, D. 2011. Reactivation of latent tuberculosis in rhesus macaques by coinfection with simian immunodeficiency virus. J Med Primatol 40: 233–243.
- Luciw, PA, Oslund, KL, Yang, XW, Adamson, L, Ravindran, R, Canfield, DR, Tarara, R, Hirst, L, Christensen, M, Lerche, NW, Offenstein, H, Lewinsohn, D, Ventimiglia, F, Brignolo, L, Wisner, ER, Hyde, DM. 2011. Stereological analysis of bacterial load and lung lesions in nonhuman primates (rhesus macaques) experimentally infected with Mycobacterium tuberculosis . Am J Physiol Lung Cell Mol Physiol 301: L731–L738.
- Dutta, NK, Mehra, S, Martinez, AN, Alvarez, X, Renner, NA, Morici, LA, Pahar, B, Maclean, AG, Lackner, AA, Kaushal, D. 2012. The stress-response factor SigH modulates the interaction between Mycobacterium tuberculosis and host phagocytes. PLoS One 7:e28958.
- Mehra, S, Golden, NA, Stuckey, K, Didier, PJ, Doyle, LA, Russell-Lodrigue, KE, Sugimoto, C, Hasegawa, A, Sivasubramani, SK, Roy, CJ, Alvarez, X, Kuroda, MJ, Blanchard, JL, Lackner, AA, Kaushal, D. 2012. The Mycobacterium tuberculosis stress response factor SigH is required for bacterial burden as well as immunopathology in primate lungs. J Infect Dis 205: 1203–1213.
- Cepeda, M, Salas, M, Folwarczny, J, Leandro, AC, Hodara, VL, de la Garza, MA, Dick, EJ Jr, Owston, M, Armitige, LY, Gauduin, MC. 2013. Establishment of a neonatal rhesus macaque model to study Mycobacterium tuberculosis infection. Tuberculosis (Edinb) 93(Suppl): S51–S59.
- Luo, Q, Mehra, S, Golden, NA, Kaushal, D, Lacey, MR. 2014. Identification of biomarkers for tuberculosis susceptibility via integrated analysis of gene expression and longitudinal clinical data. Front Genet 5:240.
- Langermans, JA, Andersen, P, van Soolingen, D, Vervenne, RA, Frost, PA, van der Laan, T, van Pinxteren, LA, van den Hombergh, J, Kroon, S, Peekel, I, Florquin, S, Thomas, AW. 2001. Divergent effect of bacillus Calmette-Guérin (BCG) vaccination on Mycobacterium tuberculosis infection in highly related macaque species: implications for primate models in tuberculosis vaccine research. Proc Natl Acad Sci USA 98: 11497–11502.
- Ravindran, R, Krishnan, VV, Dhawan, R, Wunderlich, ML, Lerche, NW, Flynn, JL, Luciw, PA, Khan, IH. 2014. Plasma antibody profiles in non-human primate tuberculosis. J Med Primatol 43: 59–71.
- Phillips, BL, Mehra, S, Ahsan, MH, Selman, M, Khader, SA, Kaushal, D. 2015. LAG3 expression in active Mycobacterium tuberculosis infections. Am J Pathol 185: 820–833.
- Mehra, S, Foreman, TW, Didier, PJ, Ahsan, MH, Hudock, TA, Kissee, R, Golden, NA, Gautam, US, Johnson, AM, Alvarez, X, Russell-Lodrigue, KE, Doyle, LA, Roy, CJ, Niu, T, Blanchard, JL, Khader, SA, Lackner, AA, Sherman, DR, Kaushal, D. 2015. The DosR regulon modulates adaptive immunity and is essential for Mycobacterium tuberculosis persistence. Am J Respir Crit Care Med 191: 1185–1196.
- Sibley, L, Dennis, M, Sarfas, C, White, A, Clark, S, Gleeson, F, McIntyre, A, Rayner, E, Pearson, G, Williams, A, Marsh, P, Sharpe, S. 2016. Route of delivery to the airway influences the distribution of pulmonary disease but not the outcome of Mycobacterium tuberculosis infection in rhesus macaques. Tuberculosis (Edinb) 96: 141–149.
- Kita, Y, Tanaka, T, Yoshida, S, Ohara, N, Kaneda, Y, Kuwayama, S, Muraki, Y, Kanamaru, N, Hashimoto, S, Takai, H, Okada, C, Fukunaga, Y, Sakaguchi, Y, Furukawa, I, Yamada, K, Inoue, Y, Takemoto, Y, Naito, M, Yamada, T, Matsumoto, M, McMurray, DN, Cruz, EC, Tan, EV, Abalos, RM, Burgos, JA, Gelber, R, Skeiky, Y, Reed, S, Sakatani, M, Okada, M. 2005. Novel recombinant BCG and DNA-vaccination against tuberculosis in a cynomolgus monkey model. Vaccine 23: 2132–2135.
- Okada, M, Kita, Y, Nakajima, T, Kanamaru, N, Hashimoto, S, Nagasawa, T, Kaneda, Y, Yoshida, S, Nishida, Y, Fukamizu, R, Tsunai, Y, Inoue, R, Nakatani, H, Namie, Y, Yamada, J, Takao, K, Asai, R, Asaki, R, Matsumoto, M, McMurray, DN, Dela Cruz, EC, Tan, EV, Abalos, RM, Burgos, JA, Gelber, R, Sakatani, M. 2007. Evaluation of a novel vaccine (HVJ-liposome/HSP65 DNA+IL-12 DNA) against tuberculosis using the cynomolgus monkey model of TB. Vaccine 25: 2990–2993.
- Reed, SG, Coler, RN, Dalemans, W, Tan, EV, Dela Cruz, EC, Basaraba, RJ, Orme, IM, Skeiky, YA, Alderson, MR, Cowgill, KD, Prieels, JP, Abalos, RM, Dubois, MC, Cohen, J, Mettens, P, Lobet, Y. 2009. Defined tuberculosis vaccine, Mtb72F/AS02A, evidence of protection in cynomolgus monkeys. Proc Natl Acad Sci USA 106: 2301–2306 (Erratum 106:7678).
- Lin, PL, Rodgers, M, Smith, L, Bigbee, M, Myers, A, Bigbee, C, Chiosea, I, Capuano, SV, Fuhrman, C, Klein, E, Flynn, JL. 2009. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect Immun 77: 4631–4642.
- Lin, PL, Myers, A, Smith, L, Bigbee, C, Bigbee, M, Fuhrman, C, Grieser, H, Chiosea, I, Voitenek, NN, Capuano, SV, Klein, E, Flynn, JL. 2010. Tumor necrosis factor neutralization results in disseminated disease in acute and latent Mycobacterium tuberculosis infection with normal granuloma structure in a cynomolgus macaque model. Arthritis Rheum 62: 340–350.
- Green, AM, Mattila, JT, Bigbee, CL, Bongers, KS, Lin, PL, Flynn, JL. 2010. CD4(+) regulatory T cells in a cynomolgus macaque model of Mycobacterium tuberculosis infection. J Infect Dis 202: 533–541.
- Diedrich, CR, Mattila, JT, Klein, E, Janssen, C, Phuah, J, Sturgeon, TJ, Montelaro, RC, Lin, PL, Flynn, JL. 2010. 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 (Erratum PLoS One 2015).
- Mattila, JT, Diedrich, CR, Lin, PL, Phuah, J, Flynn, JL. 2011. Simian immunodeficiency virus-induced changes in T cell cytokine responses in cynomolgus macaques with latent Mycobacterium tuberculosis infection are associated with timing of reactivation. J Immunol 186: 3527–3537.
- Lin, PL, Dietrich, J, Tan, E, Abalos, RM, Burgos, J, Bigbee, C, Bigbee, M, Milk, L, Gideon, HP, Rodgers, M, Cochran, C, Guinn, KM, Sherman, DR, Klein, E, Janssen, C, Flynn, JL, Andersen, P. 2012. The multistage vaccine H56 boosts the effects of BCG to protect cynomolgus macaques against active tuberculosis and reactivation of latent Mycobacterium tuberculosis infection. J Clin Invest 122: 303–314.
- Phuah, JY, Mattila, JT, Lin, PL, Flynn, JL. 2012. Activated b cells in the granulomas of nonhuman primates infected with Mycobacterium tuberculosis . Am J Pathol 181: 508–514.
- Ragheb, MN, Ford, CB, Chase, MR, Lin, PL, Flynn, JL, Fortune, SM. 2013. The mutation rate of mycobacterial repetitive unit loci in strains of M. tuberculosis from cynomolgus macaque infection. BMC Genomics 14:145.
- Chen, CY, Yao, SY, Huang, D, Wei, HY, Sicard, H, Zeng, GC, Jomaa, H, Larsen, MH, Jacobs, WR, Wang, R, Letvin, N, Shen, Y, Qiu, LY, Shen, L, Chen, ZW. 2013. Phosphoantigen/IL2 expansion and differentiation of Vγ2Vδ2 T cells increase resistance to tuberculosis in nonhuman primates. PLoS Pathog 9:e1003501.
- Lin, PL, Coleman, T, Carney, JP, Lopresti, BJ, Tomko, J, Fillmore, D, Dartois, V, Scanga, C, Frye, LJ, Janssen, C, Klein, E, Barry, CE III, Flynn, JL. 2013. Radiologic responses in cynomolgous macaques for assessing tuberculosis chemotherapy regimens. Antimicrob Agents Chemother 57: 4237–4244.
- Lin, PL, Ford, CB, Coleman, MT, Myers, AJ, Gawande, R, Ioerger, T, Sacchettini, J, Fortune, SM, Flynn, JL. 2014. Sterilization of granulomas is common in active and latent tuberculosis despite within-host variability in bacterial killing. Nat Med 20: 75–79.
- Roodgar, M, Lackner, A, Kaushal, D, Sankaran, S, Dandekar, S, Trask, JS, Drake, C, Smith, DG. 2013. Expression levels of 10 candidate genes in lung tissue of vaccinated and TB-infected cynomolgus macaques. J Med Primatol 42: 161–164.
- Dutta, NK, McLachlan, J, Mehra, S, Kaushal, D. 2014. Humoral and lung immune responses to Mycobacterium tuberculosis infection in a primate model of protection. Trials Vaccinol 3: 47–51.
- Marino, S, Cilfone, NA, Mattila, JT, Linderman, JJ, Flynn, JL, Kirschner, DE. 2015. Macrophage polarization drives granuloma outcome during Mycobacterium tuberculosis infection. Infect Immun 83: 324–338.
- Sharpe, S, White, A, Gleeson, F, McIntyre, A, Smyth, D, Clark, S, Sarfas, C, Laddy, D, Rayner, E, Hall, G, Williams, A, Dennis, M. 2016. Ultra low dose aerosol challenge with Mycobacterium tuberculosis leads to divergent outcomes in rhesus and cynomolgus macaques. Tuberculosis (Edinb) 96: 1–12.
- Sharpe, SA, Eschelbach, E, Basaraba, RJ, Gleeson, F, Hall, GA, McIntyre, A, Williams, A, Kraft, SL, Clark, S, Gooch, K, Hatch, G, Orme, IM, Marsh, PD, Dennis, MJ. 2009. Determination of lesion volume by MRI and stereology in a macaque model of tuberculosis. Tuberculosis (Edinb) 89: 405–416.
- Vervenne, RA, Jones, SL, van Soolingen, D, van der Laan, T, Andersen, P, Heidt, PJ, Thomas, AW, Langermans, JA. 2004. TB diagnosis in non-human primates: comparison of two interferon-gamma assays and the skin test for identification of Mycobacterium tuberculosis infection. Vet Immunol Immunopathol 100: 61–71.
- Kanaujia, GV, Motzel, S, Garcia, MA, Andersen, P, Gennaro, ML. 2004. Recognition of ESAT-6 sequences by antibodies in sera of tuberculous nonhuman primates. Clin Diagn Lab Immunol 11: 222–226.
- Lyashchenko, KP, Greenwald, R, Esfandiari, J, Greenwald, D, Nacy, CA, Gibson, S, Didier, PJ, Washington, M, Szczerba, P, Motzel, S, Handt, L, Pollock, JM, McNair, J, Andersen, P, Langermans, JA, Verreck, F, Ervin, S, Ervin, F, McCombs, C. 2007. PrimaTB STAT-PAK assay, a novel, rapid lateral-flow test for tuberculosis in nonhuman primates. Clin Vaccine Immunol 14: 1158–1164.
- Khan, IH, Ravindran, R, Yee, J, Ziman, M, Lewinsohn, DM, Gennaro, ML, Flynn, JL, Goulding, CW, DeRiemer, K, Lerche, NW, Luciw, PA. 2008. Profiling antibodies to Mycobacterium tuberculosis by multiplex microbead suspension arrays for serodiagnosis of tuberculosis. Clin Vaccine Immunol 15: 433–438.
- Rivera-Hernandez, T, Carnathan, DG, Moyle, PM, Toth, I, West, NP, Young, PR, Silvestri, G, Walker, MJ. 2014. The contribution of non-human primate models to the development of human vaccines. Discov Med 18: 313–322.
- Huang, D, Qiu, L, Wang, R, Lai, X, Du, G, Seghal, P, Shen, Y, Shao, L, Halliday, L, Fortman, J, Shen, L, Letvin, NL, Chen, ZW. 2007. Immune gene networks of mycobacterial vaccine-elicited cellular responses and immunity. J Infect Dis 195: 55–69.
- Philips, JA, Ernst, JD. 2012. Tuberculosis pathogenesis and immunity. Annu Rev Pathol 7: 353–384.
- Guo, M, Ho, WZ. 2014. Animal models to study Mycobacterium tuberculosis and HIV co-infection. Dongwuxue Yanjiu 35: 163–169.
- Shen, Y, Shen, L, Sehgal, P, Zhou, D, Simon, M, Miller, M, Enimi, EA, Henckler, B, Chalifoux, L, Sehgal, N, Gastron, M, Letvin, NL, Chen, ZW. 2001. Antiretroviral agents restore Mycobacterium-specific T-cell immune responses and facilitate controlling a fatal tuberculosis-like disease in Macaques coinfected with simian immunodeficiency virus and Mycobacterium bovis BCG. J Virol 75: 8690–8696.
- Shen, Y, Zhou, D, Chalifoux, L, Shen, L, Simon, M, Zeng, X, Lai, X, Li, Y, Sehgal, P, Letvin, NL, Chen, ZW. 2002. Induction of an AIDS virus-related tuberculosis-like disease in macaques: a model of simian immunodeficiency virus- Mycobacterium coinfection. Infect Immun 70: 869–877.
- Via, LE, Weiner, DM, Schimel, D, Lin, PL, Dayao, E, Tankersley, SL, Cai, Y, Coleman, MT, Tomko, J, Paripati, P, Orandle, M, Kastenmayer, RJ, Tartakovsky, M, Rosenthal, A, Portevin, D, Eum, SY, Lahouar, S, Gagneux, S, Young, DB, Flynn, JL, Barry, CE III. 2013. Differential virulence and disease progression following Mycobacterium tuberculosis complex infection of the common marmoset (Callithrix jacchus). Infect Immun 81: 2909–2919.
- Lerche, NW, Yee, JL, Capuano, SV, Flynn, JL. 2008. New approaches to tuberculosis surveillance in nonhuman primates. ILAR J 49: 170–178.
- Foreman, TW, Mehra, S, Lackner, AA, Kaushal, D. 2017. Translational research in the nonhuman primate model of tuberculosis. ILAR J 1–9.
- Sharpe, SA, Eschelbach, E, Basaraba, RJ, Gleeson, F, Hall, GA, McIntyre Williams, A, Kraft, SL, Clark, S, Gooch, K, Hatch, G, Orme, IM, Marsh, PD, Dennis, MJ. 2009. Determination of lesion volume by MRI and stereology in a macaque model of tuberculosis. Tuberculosis 89: 405–416.
- Sharpe, S, White, A, Sarfas, C, Sibley, L, Gleeson, F, McIntyre, A, Basaraba, R, Clark, S, Hall, G, Rayner, E, Williams, A, Marsh, PD, Dennis, M. 2016. Alternative BCG delivery strategies improve protection against Mycobacterium tuberculosis in non-human primates: protection associated with mycobacterial antigen-specific CD4 effector memory T-cell populations. Tuberculosis (Edinb) 101: 174–190.
- Guo, M, Xian, QY, Rao, Y, Zhang, J, Wang, Y, Huang, ZX, Wang, X, Bao, R, Zhou, L, Liu, JB, Tang, ZJ, Guo, DY, Qin, C, Li, JL, Ho, WZ. 2017. SIV infection facilitates Mycobacterium tuberculosis infection of rhesus macaques. Front Microbiol 7: 2174.
- Verreck, FAW, Tchilian, EZ, Vervenne, RAW, Sombroek, CC, Kondova, I, Eissen, OA, Sommandas, V, van der Werff, NM, Verschoor, E, Braskamp, G, Bakker, J, Langermans, JAM, Heidt, PJ, Ottenhoff, THM, van Kralingen, KW, Thomas, AW, Beverley, PCL, Kocken, CHM. 2017. Variable BCG efficacy in rhesus populations: pulmonary BCG provides protection where standard intra-dermal vaccination fails. Tuberculosis (Edinb) 104: 46–57.
- Billeskov, R, Tan, EV, Cang, M, Abalos, RM, Burgos, J, Pedersen, BV, Christensen, D, Agger, EM, Andersen, P. 2016. Testing the H56 vaccine delivered in four different adjuvants as a BCG-booster in a non-human primate model of tuberculosis. PLoS One 11: e0161217.
- Sharpe, SA, White, AD, Sibley, L, Gleeson, F, Hall, GA, Basaraba, RJ, McIntyre, A, Clark, SO, Gooch, K, Marsh, PD, Williams, A, Dennis, MJ. 2017. An aerosol challenge model of tuberculosis in Mauritian cynomolgus macaques. PLoS One 12: e0171906.
- Mattila, JT, Beaino, W, Maiello, P, Coleman, MT, White, AG, Scanga, CA, Flynn, JL, Anderson, CJ. 2017. Positron emission tomography imaging of macaques with tuberculosis identifies temporal changes in granuloma glucose metabolism and integrin α4β1-expressing immune cells. J Immunol.
