Humanized Mouse Models to Study Cell-Mediated Immune Responses to Liver-Stage Malaria Vaccines

Trends in Parasitology

Volumn 31, Issue 11, 2015, Pages 583-594

  Good, Michael F ^a,b   Hawkes, Michael T ^b   Yanow, Stephanie K ^b,c  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITY OF ALBERTA   (Canada)

^c Provincial Laboratory for Public Health   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MALARIA VACCINE;

ADAPTIVE IMMUNITY; CELL MATURATION; CELLULAR IMMUNITY; CHIMERA; ENGRAFTMENT; ERYTHROCYTE; GRAFT VERSUS HOST REACTION; HUMAN; HUMANIZED LEUKOCYTE LIVER MOUSE; IMMUNOCOMPETENT CELL; LEUKOCYTE; LIFE CYCLE; LIVER CELL; LYMPHOID TISSUE; MALARIA FALCIPARUM; MOUSE; MOUSE STRAIN; NONHUMAN; PARASITE IMMUNITY; REVIEW; STEM CELL; T LYMPHOCYTE; ANIMAL; DISEASE MODEL; IMMUNOLOGY; LIVER; PARASITOLOGY; PLASMODIUM FALCIPARUM;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNITY, CELLULAR; LIVER; MALARIA VACCINES; MALARIA, FALCIPARUM; MICE; PLASMODIUM FALCIPARUM; T-LYMPHOCYTES;

EID: 84946493319     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2015.06.008     Document Type: Review

References (66)

1. Murray C.J., et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012, 379:413-431.
2. Schwartz L., et al. A review of malaria vaccine clinical projects based on the WHO rainbow table. Malar. J. 2012, 11:11.
3. Efficacy and safety of the RTS,S/AS01 malaria vaccine during 18 months after vaccination: a Phase 3 randomized, controlled trial in children and young infants at 11 African sites. PLoS Med. 2014, 11:e1001685. RTS,S Clinical Trials Partnership.
4. Hill A.V. Vaccines against malaria. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2011, 366:2806-2814.
5. + T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat. Commun. 2013, 4:2836.
6. Hoffman S.L., et al. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 2002, 185:1155-1164.
7. Seder R.A., et al. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 2013, 341:1359-1365.
8. + T cell immunity. Science 2011, 334:475-480.
9. Nussenzweig R.S., et al. Protective immunity produced by the injection of X-irradiated sporozoites of Plasmodium berghei. Nature 1967, 216:160-162.
10. Clyde D.F., et al. Immunization of man against sporozoite-induced falciparum malaria. Am. J. Med. Sci. 1973, 266:169-177.
11. + T cells and antibodies required for immunity to malaria sporozoites. Nature 1987, 330:664-666.
12. + T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:573-576.
13. + T cell responses to liver stage malaria parasite antigens. Front. Immunol. 2014, 5:527.
14. + T cells against malaria liver stages: implications for vaccine development. Mem. Inst. Oswaldo Cruz 2011, 106(Suppl. 1):172-178.
15. + T cell-mediated elimination of malaria liver stages. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:9090-9095.
16. Brehm M.A., et al. Humanized mouse models to study human diseases. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17:120-125.
17. Legrand N., et al. Humanized mice for modeling human infectious disease: challenges, progress, and outlook. Cell Host Microbe 2009, 6:5-9.
18. Ploemen I.H., et al. Visualisation and quantitative analysis of the rodent malaria liver stage by real time imaging. PLoS ONE 2009, 4:e7881.
19. Purcell L.A., et al. Chemical attenuation of Plasmodium berghei sporozoites induces sterile immunity in mice. Infect. Immun. 2008, 76:1193-1199.
20. Mueller A.K., et al. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 2005, 433:164-167.
21. Bijker E.M., et al. Protection against malaria after immunization by chloroquine prophylaxis and sporozoites is mediated by preerythrocytic immunity. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7862-7867.
22. Good M.F., et al. Cross-species malaria immunity induced by chemically attenuated parasites. J. Clin. Invest. 2013, 123:3353-3362.
23. Mosier D.E., et al. Transfer of a functional human immune system to mice with severe combined immunodeficiency. Nature 1988, 335:256-259.
24. Mercer D.F., et al. Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 2001, 7:927-933.
25. Yamauchi T., et al. Polymorphic Sirpa is the genetic determinant for NOD-based mouse lines to achieve efficient human cell engraftment. Blood 2013, 121:1316-1325.
26. Takenaka K., et al. Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells. Nat. Immunol. 2007, 8:1313-1323.
27. Kaushansky A., et al. Of men in mice: the success and promise of humanized mouse models for human malaria parasite infections. Cell. Microbiol. 2014, 16:602-611.
28. Brehm M.A., et al. Generation of improved humanized mouse models for human infectious diseases. J. Immunol. Methods 2014, 410:3-17.
29. Klein L., et al. Positive and negative selection of the T cell repertoire: what thymocytes see (and don't see). Nat. Rev. Immunol. 2014, 14:377-391.
30. Sacci J.B., et al. Plasmodium falciparum infection and exoerythrocytic development in mice with chimeric human livers. Int. J. Parasitol. 2006, 36:353-360.
31. VanBuskirk K.M., et al. Preerythrocytic, live-attenuated Plasmodium falciparum vaccine candidates by design. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13004-13009.
32. Morosan S., et al. Liver-stage development of Plasmodium falciparum, in a humanized mouse model. J. Infect. Dis. 2006, 193:996-1004.
33. Gutti T.L., et al. Human hepatocytes and hematolymphoid dual reconstitution in treosulfan-conditioned uPA-NOG mice. Am. J. Pathol. 2014, 184:101-109.
34. -/- mice. Nat. Biotechnol. 2007, 25:903-910.
35. Vaughan A.M., et al. Complete Plasmodium falciparum liver-stage development in liver-chimeric mice. J. Clin. Invest. 2012, 122:3618-3628.
36. Vaughan A.M., et al. Development of humanized mouse models to study human malaria parasite infection. Future Microbiol. 2012, 7:657-665.
37. Wilson E.M., et al. Extensive double humanization of both liver and hematopoiesis in FRGN mice. Stem Cell Res. 2014, 13:404-412.
38. Hasegawa M., et al. The reconstituted 'humanized liver' in TK-NOG mice is mature and functional. Biochem. Biophys. Res. Commun. 2011, 405:405-410.
39. Washburn M.L., et al. A humanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology 2011, 140:1334-1344.
40. Bility M.T., et al. Hepatitis B virus infection and immunopathogenesis in a humanized mouse model: induction of human-specific liver fibrosis and M2-like macrophages. PLoS Pathog. 2014, 10:e1004032.
41. Tsuji M., et al. Establishment of a SCID mouse model having circulating human red blood cells and a possible growth of Plasmodium falciparum in the mouse. Vaccine 1995, 13:1389-1392.
42. Moore J.M., et al. Maintenance of the human malarial parasite, Plasmodium falciparum, in scid mice and transmission of gametocytes to mosquitoes. J. Exp. Med. 1995, 181:2265-2270.
43. Badell E., et al. Human Plasmodium liver stages in SCID mice: a feasible model?. Parasitol. Today 1995, 11:169-171.
44. Badell E., et al. Human malaria in immunocompromised mice: an in vivo model to study defense mechanisms against Plasmodium falciparum. J. Exp. Med. 2000, 192:1653-1660.
45. Moreno A., et al. Human malaria in immunocompromised mice: new in vivo model for chemotherapy studies. Antimicrob. Agents Chemother. 2001, 45:1847-1853.
46. Moreno Sabater A., et al. Experimental infection of immunomodulated NOD/LtSz-SCID mice as a new model for Plasmodium falciparum erythrocytic stages. Parasitol. Res. 2005, 95:97-105.
47. Rochford R., et al. Humanized mouse model of glucose 6-phosphate dehydrogenase deficiency for in vivo assessment of hemolytic toxicity. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:17486-17491.
48. Angulo-Barturen I., et al. A murine model of falciparum-malaria by in vivo selection of competent strains in non-myelodepleted mice engrafted with human erythrocytes. PLoS ONE 2008, 3:e2252.
49. null mice engrafted with human erythrocytes. Antimicrob. Agents Chemother. 2009, 53:4533-4536.
50. Arnold L., et al. Further improvements of the P. falciparum humanized mouse model. PLoS ONE 2011, 6:e18045.
51. Chen Q., et al. Human natural killer cells control Plasmodium falciparum infection by eliminating infected red blood cells. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:1479-1484.
52. Chen Q., et al. Expression of human cytokines dramatically improves reconstitution of specific human-blood lineage cells in humanized mice. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:21783-21788.
53. Wijayalath W., et al. Humanized HLA-DR4.RagKO.IL2RγcKO. NOD (DRAG) mice sustain the complex vertebrate life cycle of Plasmodium falciparum malaria. Malar. J. 2014, 13:386.
54. + T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat. Med. 2007, 13:1035-1041.
55. -/- mice are resistant to GVHD and develop B- and T-cell immunity to HIV infection. Blood 2013, 122:4013-4020.
56. King M.A., et al. Human peripheral blood leucocyte non-obese diabetic-severe combined immunodeficiency interleukin-2 receptor gamma chain gene mouse model of xenogeneic graft-versus-host-like disease and the role of host major histocompatibility complex. Clin. Exp. Immunol. 2009, 157:104-118.
57. Abraham S., et al. IL-10 exacerbates xenogeneic GVHD by inducing massive human T cell expansion. Clin. Immunol. 2015, 156:58-64.
58. null mice display a T-effector memory phenotype. PLoS ONE 2012, 7:e44219.
59. null H2-Ab1 (tm1Gru) Tg (human leucocyte antigen D-related 4) mice: a mouse model of human allogeneic graft-versus-host disease. Clin. Exp. Immunol. 2011, 166:269-280.
60. + T-cell responses in humanized mice vaccinated with influenza virus vaccines. Blood 2008, 112:3671-3678.
61. Gorin N.C., et al. Increased risk of lethal graft-versus-host disease-like syndrome after transplantation into NOD/SCID mice of human mobilized peripheral blood stem cells, as compared to bone marrow or cord blood. J. Hematother. Stem Cell Res. 2002, 11:277-292.
62. Wege A.K., et al. Functional and phenotypic characterization of the humanized BLT mouse model. Curr. Top. Microbiol. Immunol. 2008, 324:149-165.
63. Schmidt N.W., et al. Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:14017-14022.
64. + T cells in mice. PLoS ONE 2014, 9:e88205.
65. + T lymphocytes. Nature 2003, 421:852-856.
66. Good M.F. Immunology. Pasteur approach to a malaria vaccine may take the lead. Science 2013, 341:1352-1353.