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Chapter 6 : Animal Models of Tuberculosis: An Overview

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Abstract:

Animal models are an integral part of the scientific process, reflecting the physiological and anatomical similarities between many animal species and human beings. In the context of infectious diseases, multiple animal models have been used to extend our understanding of their pathophysiology and the host response to them. This is the backbone also of vaccine research, producing vaccines against once-dreaded multiple diseases that in previous centuries claimed the lives of many millions of people. Animal models are also invaluable in designing therapies, particularly drugs, with which to combat these diseases.

Citation: Williams A, Orme I. 2017. Animal Models of Tuberculosis: An Overview, p 131-142. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0004-2015
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Figure 1

The theoretical relationship among virulence, immunogenicity, and fitness, and its importance in the assessment of vaccine efficacy. In assessing whether a vaccine is active, the vaccine to challenge (or boost) interval is critical. In most protocols, this interval is relatively short, and so a boosting candidate, or the challenge infection itself, is given before the effector immune response has completely contracted and the subsequent memory immune response (the true target) has become fully established. After challenge, the change in CFU levels versus time indicates the intrinsic virulence of the strain used. If the vaccine has induced memory immunity, the growth of the challenge infection is slowed, but the rapidity with which this happens also depends on the immunogenicity of the organism. Finally, recent studies (see reference , for example) indicate that certain clinical strains, despite high virulence, are very effectively controlled by BCG vaccination, suggesting low fitness, whereas others are transiently inhibited but after a while continue to grow progressively.

Citation: Williams A, Orme I. 2017. Animal Models of Tuberculosis: An Overview, p 131-142. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0004-2015
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References

/content/book/10.1128/9781555819569.chap6
1. Russell WMS,, Burch RL . 1959. The Principles of Humane Experimental Technique. Methuen, London, United Kingdom. [PubMed]
2. Lefford MJ . 1975. Transfer of adoptive immunity to tuberculosis in mice. Infect Immun 11 : 11741181.
3. North RJ . 1973. Importance of thymus-derived lymphocytes in cell-mediated immunity to infection. Cell Immunol 7 : 166176.[CrossRef] [PubMed] [CrossRef]
4. Orme IM . 1987. The kinetics of emergence and loss of mediator T lymphocytes acquired in response to infection with Mycobacterium tuberculosis . J Immunol 138 : 293298.[PubMed]
5. Orme IM,, Collins FM . 1983. Protection against Mycobacterium tuberculosis infection by adoptive immunotherapy. Requirement for T cell-deficient recipients. J Exp Med 158 : 7483.[CrossRef] [CrossRef]
6. Driver ER,, Ryan GJ,, Hoff DR,, Irwin SM,, Basaraba RJ,, Kramnik I,, Lenaerts AJ . 2012. Evaluation of a mouse model of necrotic granuloma formation using C3HeB/FeJ mice for testing of drugs against Mycobacterium tuberculosis . Antimicrob Agents Chemother 56 : 31813195.[CrossRef] [CrossRef]
7. Cooper AM,, Dalton DK,, Stewart TA,, Griffin JP,, Russell DG,, Orme IM . 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178 : 22432247.[CrossRef] [PubMed] [CrossRef]
8. Flynn JL,, Chan J,, Triebold KJ,, Dalton DK,, Stewart TA,, Bloom BR . 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178 : 22492254.[CrossRef] [PubMed] [CrossRef]
9. Flynn JL,, Goldstein MM,, Chan J,, Triebold KJ,, Pfeffer K,, Lowenstein CJ,, Schreiber R,, Mak TW,, Bloom BR . 1995. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2 : 561572.[CrossRef] [CrossRef]
10. Saunders BM,, Frank AA,, Orme IM,, Cooper AM . 2002. CD4 is required for the development of a protective granulomatous response to pulmonary tuberculosis. Cell Immunol 216 : 6572.[CrossRef] [PubMed] [CrossRef]
11. Turner J,, D’Souza CD,, Pearl JE,, Marietta P,, Noel M,, Frank AA,, Appelberg R,, Orme IM,, Cooper AM . 2001. CD8- and CD95/95L-dependent mechanisms of resistance in mice with chronic pulmonary tuberculosis. Am J Respir Cell Mol Biol 24 : 203209.[CrossRef] [PubMed] [CrossRef]
12. Basaraba RJ . 2008. Experimental tuberculosis: the role of comparative pathology in the discovery of improved tuberculosis treatment strategies. Tuberculosis (Edinb) 88(Suppl 1): S35S47.[CrossRef] [CrossRef]
13. McMurray DN,, Collins FM,, Dannenberg AM Jr,, Smith DW . 1996. Pathogenesis of experimental tuberculosis in animal models. Curr Top Microbiol Immunol 215 : 157179. [CrossRef] [PubMed] [CrossRef]
14. McMurray DN . 2001. A coordinated strategy for evaluating new vaccines for human and animal tuberculosis. Tuberculosis (Edinb) 81 : 141146.[CrossRef] [PubMed] [CrossRef]
15. McMurray DN . 2001. Determinants of vaccine-induced resistance in animal models of pulmonary tuberculosis. Scand J Infect Dis 33 : 175178.[CrossRef] [PubMed] [CrossRef]
16. Orme IM . 2011. Development of new vaccines and drugs for TB: limitations and potential strategic errors. Future Microbiol 6 : 161177.[CrossRef] [PubMed] [CrossRef]
17. Orme IM . 2013. Vaccine development for tuberculosis: current progress. Drugs 73 : 10151024.[CrossRef] [PubMed] [CrossRef]
18. Henao-Tamayo M,, Shanley CA,, Verma D,, Zilavy A,, Stapleton MC,, Furney SK,, Podell B,, Orme IM . 2015. The efficacy of the BCG vaccine against newly emerging clinical strains of Mycobacterium tuberculosis . PLoS One 10 : e0136500. [CrossRef] [PubMed] [CrossRef]
19. Shanley CA,, Streicher EM,, Warren RM,, Victor TC,, Orme IM . 2013. Characterization of W-Beijing isolates of Mycobacterium tuberculosis from the Western Cape. Vaccine 31 : 59345939. [CrossRef] [PubMed] [CrossRef]
20. Ordway DJ,, Shanley CA,, Caraway ML,, Orme EA,, Bucy DS,, Hascall-Dove L,, Henao-Tamayo M,, Harton MR,, Shang S,, Ackart D,, Kraft SL,, Lenaerts AJ,, Basaraba RJ,, Orme IM . 2010. Evaluation of standard chemotherapy in the guinea pig model of tuberculosis. Antimicrob Agents Chemother 54 : 18201833.[CrossRef] [PubMed] [CrossRef]
21. Shang S,, Shanley CA,, Caraway ML,, Orme EA,, Henao-Tamayo M,, Hascall-Dove L,, Ackart D,, Lenaerts AJ,, Basaraba RJ,, Orme IM,, Ordway DJ . 2011. Activities of TMC207, rifampin, and pyrazinamide against Mycobacterium tuberculosis infection in guinea pigs. Antimicrob Agents Chemother 55 : 124131. [CrossRef]
22. Peña JC,, Ho WZ . 2015. Monkey models of tuberculosis: lessons learned. Infect Immun 83 : 852862.[CrossRef] [PubMed] [CrossRef]
23. Flynn JL,, Gideon HP,, Mattila JT,, Lin PL . 2015. Immunology studies in non-human primate models of tuberculosis. Immunol Rev 264 : 6073.[CrossRef] [PubMed] [CrossRef]
24. Scanga CA,, Flynn JL . 2014. Modeling tuberculosis in nonhuman primates. Cold Spring Harb Perspect Med 4 : a018564.[CrossRef] [PubMed] [CrossRef]
25. Takaki K,, Davis JM,, Winglee K,, Ramakrishnan L . 2013. Evaluation of the pathogenesis and treatment of Mycobacterium marinum infection in zebrafish. Nat Protoc 8 : 11141124.[CrossRef] [PubMed] [CrossRef]
26. Swaim LE,, Connolly LE,, Volkman HE,, Humbert O,, Born DE,, Ramakrishnan L . 2006. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect Immun 74 : 61086117.[CrossRef] [PubMed] [CrossRef]
27. Davis JM,, Clay H,, Lewis JL,, Ghori N,, Herbomel P,, Ramakrishnan L . 2002. Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17 : 693702.[CrossRef] [CrossRef]
28. Cosma CL,, Swaim LE,, Volkman H,, Ramakrishnan L,, Davis JM . 2006. Zebrafish and frog models of Mycobacterium marinum infection. Curr Protoc Immunol Chapter 10 : Unit 10B. 2. [PubMed]
29. Ramakrishnan L . 2013. The zebrafish guide to tuberculosis immunity and treatment. Cold Spring Harb Symp Quant Biol 78 : 179192.[CrossRef] [PubMed] [CrossRef]
30. Yang CT,, Cambier CJ,, Davis JM,, Hall CJ,, Crosier PS,, Ramakrishnan L . 2012. Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 12 : 301312.[CrossRef] [CrossRef]
31. Turner OC,, Basaraba RJ,, Frank AA,, Orme IM, . 2003. Granuloma formation in mouse and guinea pig models of experimental tuberculosis, p 6584. In Boros DL (ed), Granulomatous Infections and Inflammation: Cellular and Molecular Mechanisms. ASM Press, Washington, DC.[CrossRef] [CrossRef]
32. Berry MP,, Graham CM,, McNab FW,, Xu Z,, Bloch SA,, Oni T,, Wilkinson KA,, Banchereau R,, Skinner J,, Wilkinson RJ,, Quinn C,, Blankenship D,, Dhawan R,, Cush JJ,, Mejias A,, Ramilo O,, Kon OM,, Pascual V,, Banchereau J,, Chaussabel D,, O’Garra A . 2010. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466 : 973977.[CrossRef] [CrossRef]
33. Eum SY,, Kong JH,, Hong MS,, Lee YJ,, Kim JH,, Hwang SH,, Cho SN,, Via LE,, Barry CE III . 2010. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 137 : 122128.[CrossRef] [PubMed] [CrossRef]
34. Orme IM . 2014. A new unifying theory of the pathogenesis of tuberculosis. Tuberculosis (Edinb) 94 : 814.[CrossRef]
35. Lurie MB . 1939. Studies on the mechanism of immunity in tuberculosis: the mobilization of mononuclear phagocytes in normal and immunized animals and their relative capacities for division and phagocytosis. J Exp Med 69 : 579599.[CrossRef] [CrossRef]
36. Lurie MB . 1939. Studies on the mechanism of immunity in tuberculosis: the role of extracellular factors and local immunity in the fixation and inhibition of growth of tubercle bacilli. J Exp Med 69 : 555578.[CrossRef] [PubMed] [CrossRef]
37. Lurie MB,, Zappasodi P,, Cardona-Lynch E,, Dannenberg AM Jr . 1952. The response to the intracutaneous inoculation of BCG as an index of native resistance to tuberculosis. J Immunol 68 : 369387.[PubMed]
38. Dannenberg AM Jr . 1968. Cellular hypersensitivity and cellular immunity in the pathogensis of tuberculosis: specificity, systemic and local nature, and associated macrophage enzymes. Bacteriol Rev 32 : 85102.[PubMed]
39. Dannenberg AM Jr . 1970. Pathogenesis of tuberculosis: local and systemic immunity and cellular hypersensitivity. Bull Int Union Tuberc 43 : 177178.[PubMed]
40. Dannenberg AM Jr . 1991. Delayed-type hypersensitivity and cell-mediated immunity in the pathogenesis of tuberculosis. Immunol Today 12 : 228233.[CrossRef] [PubMed] [CrossRef]
41. Manabe YC,, Dannenberg AM Jr,, Tyagi SK,, Hatem CL,, Yoder M,, Woolwine SC,, Zook BC,, Pitt ML,, Bishai WR . 2003. Different strains of Mycobacterium tuberculosis cause various spectrums of disease in the rabbit model of tuberculosis. Infect Immun 71 : 60046011.[CrossRef] [PubMed] [CrossRef]
42. Nedeltchev GG,, Raghunand TR,, Jassal MS,, Lun S,, Cheng QJ,, Bishai WR . 2009. Extrapulmonary dissemination of Mycobacterium bovis but not Mycobacterium tuberculosis in a bronchoscopic rabbit model of cavitary tuberculosis. Infect Immun 77 : 598603.[CrossRef] [CrossRef]
43. Hunter RL,, Jagannath C,, Actor JK . 2007. Pathology of postprimary tuberculosis in humans and mice: contradiction of long-held beliefs. Tuberculosis (Edinb) 87 : 267278.[CrossRef] [PubMed] [CrossRef]
44. Tsenova L,, Ellison E,, Harbacheuski R,, Moreira AL,, Kurepina N,, Reed MB,, Mathema B,, Barry CE III,, Kaplan G . 2005. Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis 192 : 98106.[CrossRef] [CrossRef]
45. Gray DF,, Noble JL,, O’Hara M . 1961. Allergy in experimental rat tuberculosis. J Hyg (Lond) 59 : 427436.[CrossRef]
46. Gray DF . 1961. The relative natural resistance of rats and mice to experimental pulmonary tuberculosis. J Hyg (Lond) 59 : 471477.[CrossRef] [PubMed] [CrossRef]
47. Gray DF,, Graham-Smith H,, Noble JL . 1960. Variations in natural resistance to tuberculosis. J Hyg (Lond) 58 : 215227. [CrossRef] [PubMed] [CrossRef]
48. Lefford MJ,, McGregor DD,, Mackaness GB . 1973. Properties of lymphocytes which confer adoptive immunity to tuberculosis in rats. Immunology 25 : 703715.[PubMed]
49. Lefford MJ,, McGregor DD,, Mackaness GB . 1973. Immune response to Mycobacterium tuberculosis in rats. Infect Immun 8 : 182189.[PubMed]
50. Sugawara I,, Mizuno S . 2008. Higher susceptibility of type 1 diabetic rats to Mycobacterium tuberculosis infection. Tohoku J Exp Med 216 : 363370.[CrossRef] [PubMed] [CrossRef]
51. Vordermeier HM,, Villarreal-Ramos B,, Cockle PJ,, McAulay M,, Rhodes SG,, Thacker T,, Gilbert SC,, McShane H,, Hill AV,, Xing Z,, Hewinson RG . 2009. Viral booster vaccines improve Mycobacterium bovis BCG-induced protection against bovine tuberculosis. Infect Immun 77 : 33643373.[CrossRef] [CrossRef]
52. Gil O,, Díaz I,, Vilaplana C,, Tapia G,, Díaz J,, Fort M,, Cáceres N,, Pinto S,, Caylà J,, Corner L,, Domingo M,, Cardona PJ . 2010. Granuloma encapsulation is a key factor for containing tuberculosis infection in minipigs. PLoS One 5 : e10030. [CrossRef] [PubMed] [CrossRef]
53. Margulies DH . 2014. The in-betweeners: MAIT cells join the innate-like lymphocytes gang. J Exp Med 211 : 15011502.[CrossRef] [PubMed] [CrossRef]
54. Cowley SC . 2014. MAIT cells and pathogen defense. Cell Mol Life Sci 71 : 48314840.[CrossRef] [PubMed] [CrossRef]
55. Henao-Tamayo M,, Ordway DJ,, Orme IM . 2014. Memory T cell subsets in tuberculosis: what should we be targeting? Tuberculosis (Edinb) 94 : 455461.[CrossRef] [PubMed] [CrossRef]
56. Fletcher HA . 2007. Correlates of immune protection from tuberculosis. Curr Mol Med 7 : 319325.[CrossRef] [CrossRef]
57. Orme IM,, Basaraba RJ . 2014. The formation of the granuloma in tuberculosis infection. Semin Immunol 26 : 601609.[CrossRef] [PubMed] [CrossRef]
58. Basaraba RJ,, Smith EE,, Shanley CA,, Orme IM . 2006. Pulmonary lymphatics are primary sites of Mycobacterium tuberculosis infection in guinea pigs infected by aerosol. Infect Immun 74 : 53975401.[CrossRef] [PubMed] [CrossRef]
59. Davis JM,, Ramakrishnan L . 2009. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136 : 3749.[CrossRef] [PubMed] [CrossRef]
60. Urdahl KB,, Shafiani S,, Ernst JD . 2011. Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol 4 : 288293. [CrossRef] [PubMed] [CrossRef]
61. Dharmadhikari AS,, Basaraba RJ,, Van Der Walt ML,, Weyer K,, Mphahlele M,, Venter K,, Jensen PA,, First MW,, Parsons S,, McMurray DN,, Orme IM,, Nardell EA . 2011. Natural infection of guinea pigs exposed to patients with highly drug-resistant tuberculosis. Tuberculosis (Edinb) 91 : 329338. [CrossRef] [PubMed] [CrossRef]
62. McShane H,, Jacobs WR,, Fine PE,, Reed SG,, McMurray DN,, Behr M,, Williams A,, Orme IM . 2012. BCG: myths, realities, and the need for alternative vaccine strategies. Tuberculosis (Edinb) 92 : 283288.[CrossRef] [PubMed] [CrossRef]
63. Williams A,, Hall Y,, Orme IM . 2009. Evaluation of new vaccines for tuberculosis in the guinea pig model. Tuberculosis (Edinb) 89 : 389397.[CrossRef] [PubMed] [CrossRef]
64. Orme IM . 2015. Tuberculosis vaccine types and timings. Clin Vaccine Immunol 22 : 249257.[CrossRef] [PubMed] [CrossRef]
65. Orme I . 2014. Letter to the editor. Tuberculosis (Edinb) 94 : 717.[CrossRef] [CrossRef]
66. Lenaerts AJ,, Gruppo V,, Brooks JV,, Orme IM . 2003. Rapid in vivo screening of experimental drugs for tuberculosis using gamma interferon gene-disrupted mice. Antimicrob Agents Chemother 47 : 783785.[CrossRef] [PubMed] [CrossRef]
67. Woolhiser LK,, Hoff DR,, Marietta KS,, Orme IM,, Lenaerts AJ . 2009. Testing of experimental compounds in a relapse model of tuberculosis using granulocyte-macrophage colony-stimulating factor gene-disrupted mice. Antimicrob Agents Chemother 53 : 306308.[CrossRef] [PubMed] [CrossRef]
68. Lanoix JP,, Lenaerts AJ,, Nuermberger EL . 2015. Heterogeneous disease progression and treatment response in a C3HeB/FeJ mouse model of tuberculosis. Dis Model Mech 8 : 603610. [CrossRef] [PubMed] [CrossRef]
69. Brooks JV,, Furney SK,, Orme IM . 1999. Metronidazole therapy in mice infected with tuberculosis. Antimicrob Agents Chemother 43 : 12851288.[PubMed]
70. Hoff DR,, Caraway ML,, Brooks EJ,, Driver ER,, Ryan GJ,, Peloquin CA,, Orme IM,, Basaraba RJ,, Lenaerts AJ . 2008. Metronidazole lacks antibacterial activity in guinea pigs infected with Mycobacterium tuberculosis . Antimicrob Agents Chemother 52 : 41374140. [CrossRef]
71. Klinkenberg LG,, Sutherland LA,, Bishai WR,, Karakousis PC . 2008. Metronidazole lacks activity against Mycobacterium tuberculosis in an in vivo hypoxic granuloma model of latency. J Infect Dis 198 : 275283.[CrossRef] [CrossRef]
72. De Groote MA,, Gilliland JC,, Wells CL,, Brooks EJ,, Woolhiser LK,, Gruppo V,, Peloquin CA,, Orme IM,, Lenaerts AJ . 2011. Comparative studies evaluating mouse models used for efficacy testing of experimental drugs against Mycobacterium tuberculosis . Antimicrob Agents Chemother 55 : 12371247.[CrossRef] [CrossRef]
73. De Groote MA,, Gruppo V,, Woolhiser LK,, Orme IM,, Gilliland JC,, Lenaerts AJ . 2012. Importance of confirming data on the in vivo efficacy of novel antibacterial drug regimens against various strains of Mycobacterium tuberculosis . Antimicrob Agents Chemother 56 : 731738.[CrossRef] [PubMed] [CrossRef]
74. Tameris MD,, Hatherill M,, Landry BS,, Scriba TJ,, Snowden MA,, Lockhart S,, Shea JE,, McClain JB,, Hussey GD,, Hanekom WA,, Mahomed H,, McShane H ; MVA85A 020 Trial Study Team . 2013. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 381 : 10211028.[CrossRef] [CrossRef]
75. McShane H,, Williams A . 2014. A review of preclinical animal models utilised for TB vaccine evaluation in the context of recent human efficacy data. Tuberculosis (Edinb) 94 : 105110. [CrossRef]
76. Brighenti S,, Andersson J . 2012. Local immune responses in human tuberculosis: learning from the site of infection. J Infect Dis 205(Suppl 2): S316S324.[CrossRef] [PubMed] [CrossRef]
77. Jacobs WR Jr,, McShane H,, Mizrahi V,, Orme IM (ed). Tuberculosis and the Tubercle Bacillus, 2nd ed. ASM Press, Washington, DC, in press.

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