Interferon-Mediated Innate Immune Responses against Malaria Parasite Liver Stages

Cell Reports

Volumn 7, Issue 2, 2014, Pages 436-447

  Miller, Jessica L ^a   Sack, Brandon K ^a   Baldwin, Michael ^a   Vaughan, Ashley M ^a   Kappe, Stefan H I ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; GAMMA INTERFERON; ALPHA2 INTEGRIN; CD1D ANTIGEN; CD1D ANTIGEN, MOUSE; INTERFERON; INTERFERON REGULATORY FACTOR 3; IRF3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CYTOKINE RELEASE; DOWN REGULATION; GENE EXPRESSION; HEPATITIS; IMMUNE RESPONSE; INNATE IMMUNITY; LIVER CELL; LYMPHOCYTE SUBPOPULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PARASITE CLEARANCE; PLASMODIUM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA SEQUENCE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; FEMALE; GENETICS; IMMUNOLOGY; LIVER; MALARIA; METABOLISM; PARASITOLOGY; PATHOGENICITY; SPOROZOITE;

ANIMALS; ANTIGENS, CD1D; FEMALE; IMMUNITY, INNATE; INTEGRIN ALPHA2; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LIVER; MALARIA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PLASMODIUM; RECEPTOR, INTERFERON ALPHA-BETA; SPOROZOITES;

EID: 84899626405     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.018     Document Type: Article

References (35)

1. Azuma H., Paulk N., Ranade A., Dorrell C., Al-Dhalimy M., Ellis E., Strom S., Kay M.A., Finegold M., Grompe M. Robust expansion of human hepatocytes in Fah-/-/Rag2-/-/Il2rg-/- mice. Nat. Biotechnol. 2007, 25:903-910.
2. Boisvert M., Chetoui N., Gendron S., Aoudjit F. Alpha2beta1 integrin is the major collagen-binding integrin expressed on human Th17 cells. Eur. J. Immunol. 2010, 40:2710-2719.
3. Calvo-Calle J.M., Moreno A., Eling W.M., Nardin E.H. Invitro development of infectious liver stages of P. yoelii and P. berghei malaria in human cell lines. Exp. Parasitol. 1994, 79:362-373.
4. Cavlar T., Ablasser A., Hornung V. Induction of type I IFNs by intracellular DNA-sensing pathways. Immunol. Cell Biol. 2012, 90:474-482.
5. Crispe I.N. Isolation of mouse intrahepatic lymphocytes. Curr. Protoc. Immunol. 2001, Chapter 3:21.
6. Diercks A., Aderem A. Systems approaches to dissecting immunity. Curr. Top. Microbiol. Immunol. 2013, 363:1-19.
7. Gagliani N., Magnani C.F., Huber S., Gianolini M.E., Pala M., Licona-Limon P., Guo B., Herbert D.R., Bulfone A., Trentini F., et al. Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells. Nat. Med. 2013, 19:739-746.
8. Gantt S.M., Myung J.M., Briones M.R., Li W.D., Corey E.J., Omura S., Nussenzweig V., Sinnis P. Proteasome inhibitors block development of Plasmodium spp. Antimicrob. Agents Chemother. 1998, 42:2731-2738.
9. Gao B., Radaeva S., Park O. Liver natural killer and natural killer Tcells: immunobiology and emerging roles in liver diseases. J.Leukoc. Biol. 2009, 86:513-528.
10. Gonzalez-Aseguinolaza G., de Oliveira C., Tomaska M., Hong S., Bruna-Romero O., Nakayama T., Taniguchi M., Bendelac A., Van Kaer L., Koezuka Y., Tsuji M. alpha -galactosylceramide-activated Valpha 14 natural killer Tcells mediate protection against murine malaria. Proc. Natl. Acad. Sci. USA 2000, 97:8461-8466.
11. Groom J.R., Luster A.D. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 2011, 89:207-215.
12. Gueirard P., Tavares J., Thiberge S., Bernex F., Ishino T., Milon G., Franke-Fayard B., Janse C.J., Ménard R., Amino R. Development of the malaria parasite in the skin of the mammalian host. Proc. Natl. Acad. Sci. USA 2010, 107:18640-18645.
13. Honda K., Takaoka A., Taniguchi T. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 2006, 25:349-360.
14. Kassiotis G., Gray D., Kiafard Z., Zwirner J., Stockinger B. Functional specialization of memory Th cells revealed by expression of integrin CD49b. J.Immunol. 2006, 177:968-975.
15. Khan Z.M., Vanderberg J.P. Eosinophil-rich, granulomatous inflammatory response to Plasmodium berghei hepatic schizonts in nonimmunized rats is age-related. Am. J. Trop. Med. Hyg. 1991, 45:190-201.
16. Khan Z.M., Vanderberg J.P. Specific inflammatory cell infiltration of hepatic schizonts in BALB/c mice immunized with attenuated Plasmodium yoelii sporozoites. Int. Immunol. 1992, 4:711-718.
17. Kim S., Iizuka K., Aguila H.L., Weissman I.L., Yokoyama W.M. Invivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc. Natl. Acad. Sci. USA 2000, 97:2731-2736.
18. Kim S., Song Y.J., Higuchi D.A., Kang H.P., Pratt J.R., Yang L., Hong C.M., Poursine-Laurent J., Iizuka K., French A.R., et al. Arrested natural killer cell development associated with transgene insertion into the Atf2 locus. Blood 2006, 107:1024-1030.
19. Liehl P., Mota M.M. Innate recognition of malarial parasites by mammalian hosts. Int. J. Parasitol. 2012, 42:557-566.
20. Liehl P., Zuzarte-Luís V., Chan J., Zillinger T., Baptista F., Carapau D., Konert M., Hanson K.K., Carret C., Lassnig C., et al. Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nat. Med. 2014, 20:47-53.
21. Lindner S.E., Miller J.L., Kappe S.H. Malaria parasite pre-erythrocytic infection: preparation meets opportunity. Cell. Microbiol. 2012, 14:316-324.
22. Mack S.R., Vanderberg J.P., Nawrot R. Column separation of Plasmodium berghei sporozoites. J.Parasitol. 1978, 64:166-168.
23. Mellouk S., Green S.J., Nacy C.A., Hoffman S.L. IFN-gamma inhibits development of Plasmodium berghei exoerythrocytic stages in hepatocytes by an L-arginine-dependent effector mechanism. J.Immunol. 1991, 146:3971-3976.
24. Miller J.L., Murray S., Vaughan A.M., Harupa A., Sack B., Baldwin M., Crispe I.N., Kappe S.H. Quantitative bioluminescent imaging ofpre-erythrocytic malaria parasite infection using luciferase-expressing Plasmodium yoelii. PLoS ONE 2013, 8:e60820.
25. Pied S., Roland J., Louise A., Voegtle D., Soulard V., Mazier D., Cazenave P.A. Liver CD4-CD8- NK1.1+ TCR alpha beta intermediate cells increase during experimental malaria infection and are able to exhibit inhibitory activity against the parasite liver stage invitro. J.Immunol. 2000, 164:1463-1469.
26. Riley E.M., Stewart V.A. Immune mechanisms in malaria: new insights in vaccine development. Nat. Med. 2013, 19:168-178.
27. Roland J., Soulard V., Sellier C., Drapier A.M., Di Santo J.P., Cazenave P.A., Pied S. NK cell responses to Plasmodium infection and control of intrahepatic parasite development. J.Immunol. 2006, 177:1229-1239.
28. Schoenborn J.R., Wilson C.B. Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 2007, 96:41-101.
29. Schofield L., Ferreira A., Altszuler R., Nussenzweig V., Nussenzweig R.S. Interferon-gamma inhibits the intrahepatocytic development of malaria parasites invitro. J.Immunol. 1987, 139:2020-2025.
30. Soulard V., Roland J., Sellier C., Gruner A.C., Leite-de-Moraes M., Franetich J.F., Rénia L., Cazenave P.A., Pied S. Primary infection of C57BL/6 mice with Plasmodium yoelii induces a heterogeneous response of NKT cells. Infect. Immun. 2007, 75:2511-2522.
31. Stark G.R., Darnell J.E. The JAK-STAT pathway at twenty. Immunity 2012, 36:503-514.
32. Tarun A.S., Dumpit R.F., Camargo N., Labaied M., Liu P., Takagi A., Wang R., Kappe S.H. Protracted sterile protection with Plasmodium yoelii pre-erythrocytic genetically attenuated parasite malaria vaccines is independent of significant liver-stage persistence and is mediated by CD8+ Tcells. J.Infect. Dis. 2007, 196:608-616.
33. Vaughan A.M., O'Neill M.T., Tarun A.S., Camargo N., Phuong T.M., Aly A.S., Cowman A.F., Kappe S.H. Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell. Microbiol. 2009, 11:506-520.
34. Voza T., Miller J.L., Kappe S.H., Sinnis P. Extrahepatic exoerythrocytic forms of rodent malaria parasites at the site of inoculation: clearance after immunization, susceptibility to primaquine, and contribution to blood-stage infection. Infect. Immun. 2012, 80:2158-2164.
35. World Health Organization (WHO) (2013). World Malaria Report 2013. http://www.who.int/malaria/publications/world_malaria_report_2013/report/en/.