Innate immunity induced by Plasmodium liver infection inhibits malaria reinfections

Infection and Immunity

Volumn 83, Issue 3, 2015, Pages 1172-1180

  Liehl, Peter ^a   Meireles, Patrícia ^a   Albuquerque, Inês S ^a   Pinkevych, Mykola ^b   Baptista, Fernanda ^a   Mota, Maria M ^a   Davenport, Miles P ^b   Prudêncio, Miguel ^a  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; CHLOROQUINE; GAMMA INTERFERON; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; ALPHA BETA INTERFERON RECEPTOR; CARRIER PROTEIN; GREEN FLUORESCENT PROTEIN; IFIT1 PROTEIN, MOUSE; IFIT3 PROTEIN, MOUSE; IFNAR1 PROTEIN, MOUSE; IRF7 PROTEIN, MOUSE; PROTEIN; UBIQUITIN THIOLESTERASE; USP18 PROTEIN, MOUSE;

ACTIVE IMMUNIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; HEPATITIS; HOST RESISTANCE; INDUCED RESISTANCE; INFECTION PREVENTION; INFECTION RATE; INFECTION RESISTANCE; INNATE IMMUNITY; MALARIA FALCIPARUM; MATHEMATICAL MODEL; MEROZOITE; MOSQUITO BITE; MOUSE; NONHUMAN; PARASITE CLEARANCE; PARASITE IMMUNITY; PARASITE LOAD; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REINFECTION; RNA ISOLATION; RODENT MALARIA; SPOROZOITE; STOCHASTIC MODEL; ADAPTIVE IMMUNITY; ANIMAL; ANOPHELES; C57BL MOUSE; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; KNOCKOUT MOUSE; LIVER; MALARIA; METABOLISM; PARASITOLOGY; REPORTER GENE; STATISTICAL MODEL;

ADAPTIVE IMMUNITY; ANIMALS; ANOPHELES; CARRIER PROTEINS; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; INTERFERON REGULATORY FACTOR-7; INTERFERON-GAMMA; LIVER; MALARIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, STATISTICAL; PARASITE LOAD; PLASMODIUM BERGHEI; PROTEINS; RECEPTOR, INTERFERON ALPHA-BETA; SPOROZOITES; UBIQUITIN THIOLESTERASE;

EID: 84923059786     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02796-14     Document Type: Article

References (56)

1. Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD. 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379:413-431. http://dx.doi.org/10.1016/S0140-6736(12)60034-8.
2. Prudêncio M, Rodriguez A, Mota MM. 2006. The silent path to thousands of merozoites: the Plasmodium liver stage. Nat Rev Microbiol 4:849-856. http://dx.doi.org/10.1038/nrmicro1529.
3. Amino R, Giovannini D, Thiberge S, Gueirard P, Boisson B, Dubremetz JF, Prevost MC, Ishino T, Yuda M, Menard R. 2008. Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe 3:88-96. http://dx.doi.org/10.1016/j.chom.2007.12.007.
4. Tavares J, Formaglio P, Thiberge S, Mordelet E, Van Rooijen N, Medvinsky A, Menard R, Amino R. 2013. Role of host cell traversal by the malaria sporozoite during liver infection. J Exp Med 210:905-915. http://dx.doi.org/10.1084/jem.20121130.
5. Mota MM, Pradel G, Vanderberg JP, Hafalla JC, Frevert U, Nussenzweig RS, Nussenzweig V, Rodriguez A. 2001. Migration of Plasmodium sporozoites through cells before infection. Science 291:141-144. http://dx.doi.org/10.1126/science.291.5501.141.
6. Sturm A, Amino R, van de Sand C, Regen T, Retzlaff S, Rennenberg A, Krueger A, Pollok JM, Menard R, Heussler VT. 2006. Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313:1287-1290. http://dx.doi.org/10.1126/science.1129720.
7. Haldar K, Murphy SC, Milner DA, Taylor TE. 2007. Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu Rev Pathol 2:217-249. http://dx.doi.org/10.1146/annurev.pathol.2.010506.091913.
8. Takala SL, Plowe CV. 2009. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming 'vaccine resistant malaria'. Parasite Immunol 31:560-573. http://dx.doi.org/10.1111/j.1365-3024.2009.01138.x.
9. Marsh K, Kinyanjui S. 2006. Immune effector mechanisms in malaria. Parasite Immunol 28:51-60. http://dx.doi.org/10.1111/j.1365-3024.2006.00808.x.
10. Langhorne J, Ndungu FM, Sponaas AM, Marsh K. 2008. Immunity to malaria: more questions than answers. Nat Immunol 9:725-732. http://dx.doi.org/10.1038/ni.f.205.
11. Stevenson MM, Riley EM. 2004. Innate immunity to malaria. Nat Rev Immunol 4:169-180. http://dx.doi.org/10.1038/nri1311.
12. Portugal S, Carret C, Recker M, Armitage AE, Goncalves LA, Epiphanio S, Sullivan D, Roy C, Newbold CI, Drakesmith H, Mota MM. 2011. Host-mediated regulation of superinfection in malaria. Nat Med 17:732-737. http://dx.doi.org/10.1038/nm.2368.
13. Pinkevych M, Petravic J, Chelimo K, Vulule J, Kazura JW, Moormann AM, Davenport MP. 9 September 2013, posting date. Density-dependent blood stage Plasmodium falciparum suppresses malaria super-infection in a malaria holoendemic population. Am J Trop Med Hyg http://dx.doi.org/10.4269/ajtmh.13-0049.
14. Sokhna CS, Rogier C, Dieye A, Trape JF. 2000. Host factors affecting the delay of reappearance of Plasmodium falciparum after radical treatment among a semi-immune population exposed to intense perennial transmission. Am J Trop Med Hyg 62:266-270.
15. Tall A, Sokhna C, Perraut R, Fontenille D, Marrama L, Ly AB, Sarr FD, Toure A, Trape JF, Spiegel A, Rogier C, Druilhe P. 2009. Assessment of the relative success of sporozoite inoculations in individuals exposed to moderate seasonal transmission. Malar J 8:161. http://dx.doi.org/10.1186/1475-2875-8-161.
16. Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, Tanner M. 2006. Relationship between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg 75(2 Suppl):11-18.
17. Liehl P, Mota MM. 2012. Innate recognition of malarial parasites by mammalian hosts. Int J Parasitol 42:557-566. http://dx.doi.org/10.1016/j.ijpara.2012.04.006.
18. Offeddu V, Thathy V, Marsh K, Matuschewski K. 2012. Naturally acquired immune responses against Plasmodium falciparum sporozoites and liver infection. Int J Parasitol 42:535-548. http://dx.doi.org/10.1016/j.ijpara.2012.03.011.
19. Liehl P, Zuzarte-Luis V, Chan J, Zillinger T, Baptista F, Carapau D, Konert M, Hanson KK, Carret C, Lassnig C, Muller M, Kalinke U, Saeed M, Chora AF, Golenbock DT, Strobl B, Prudencio M, Coelho LP, Kappe SH, Superti-Furga G, Pichlmair A, Vigario AM, Rice CM, Fitzgerald KA, Barchet W, Mota MM. 2014. Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nat Med 20:47-53. http://dx.doi.org/10.1038/nm.3424.
20. Macdonald G. 1956. Epidemiological basis of malaria control. Bull World Health Organ 15:613-626.
21. Charlwood JD, Smith T, Lyimo E, Kitua AY, Masanja H, Booth M, Alonso PL, Tanner M. 1998. Incidence of Plasmodium falciparum infection in infants in relation to exposure to sporozoite-infected anophelines. Am J Trop Med Hyg 59:243-251.
22. Beier JC, Killeen GF, Githure JI. 1999. Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg 61:109-113.
23. Rogier C, Tall A, Diagne N, Fontenille D, Spiegel A, Trape JF. 1999. Plasmodium falciparum clinical malaria: lessons from longitudinal studies in Senegal. Parassitologia 41:255-259.
24. Bloland PB, Boriga DA, Ruebush TK, McCormick JB, Roberts JM, Oloo AJ, Hawley W, Lal A, Nahlen B, Campbell CC. 1999. Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission II. Descriptive epidemiology of malaria infection and disease among children. Am J Trop Med Hyg 60:641-648.
25. Epstein JE, Rao S, Williams F, Freilich D, Luke T, Sedegah M, de la Vega P, Sacci J, Richie TL, Hoffman SL. 2007. Safety and clinical outcome of experimental challenge of human volunteers with Plasmodium falciparum-infected mosquitoes: an update. J Infect Dis 196:145-154. http://dx.doi.org/10.1086/518510.
26. Verhage DF, Telgt DS, Bousema JT, Hermsen CC, van Gemert GJ, van der Meer JW, Sauerwein RW. 2005. Clinical outcome of experimental human malaria induced by Plasmodium falciparum-infected mosquitoes. Neth J Med 63:52-58.
27. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742. http://dx.doi.org/10.1126/science.8456300.
28. Franke-Fayard B, Trueman H, Ramesar J, Mendoza J, van der Keur M, van der Linden R, Sinden RE, Waters AP, Janse CJ. 2004. A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol 137:23-33. http://dx.doi.org/10.1016/j.molbiopara.2004.04.007.
29. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
30. Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, Diggs CL, Hoffman SL. 1994. Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg 50:529-536.
31. Bekessy A, Molineaux L, Storey J. 1976. Estimation of incidence and recovery rates of Plasmodium falciparum parasitaemia from longitudinal data. Bull World Health Organ 54:685-693.
32. Pull JH, Grab B. 1974. A simple epidemiological model for evaluating the malaria inoculation rate and the risk of infection in infants. Bull World Health Organ 51:507-516.
33. Smith DL, Drakeley CJ, Chiyaka C, Hay SI. 2010. A quantitative analysis of transmission efficiency versus intensity for malaria. Nat Commun 1:108. http://dx.doi.org/10.1038/ncomms1107.
34. Pinkevych M, Petravic J, Chelimo K, Kazura JW, Moormann AM, Davenport MP. 2012. The dynamics of naturally acquired immunity to Plasmodium falciparum infection. PLoS Comput Biol 8:e1002729. http://dx.doi.org/10.1371/journal.pcbi.1002729.
35. Pinkevych M, Petravic J, Chelimo K, Vulule J, Kazura JW, Moormann AM, Davenport MP. 2014. Decreased growth rate of P. falciparum blood stage parasitemia with age in a holoendemic population. J Infect Dis 209: 1136-1143. http://dx.doi.org/10.1093/infdis/jit613.
36. Peters W. 1974. Recent advances in antimalarial chemotherapy and drug resistance. Adv Parasitol 12:69-114. http://dx.doi.org/10.1016/S0065-308X(08)60387-5.
37. Yayon A, Vande Waa JA, Yayon M, Geary TG, Jensen JB. 1983. Stage-dependent effects of chloroquine on Plasmodium falciparum in vitro. J Protozool 30:642-647. http://dx.doi.org/10.1111/j.1550-7408.1983.tb05336.x.
38. Belnoue E, Costa FT, Frankenberg T, Vigario AM, Voza T, Leroy N, Rodrigues MM, Landau I, Snounou G, Renia L. 2004. Protective T cell immunity against malaria liver stage after vaccination with live sporozoites under chloroquine treatment. J Immunol 172:2487-2495. http://dx.doi.org/10.4049/jimmunol.172.4.2487.
39. Decker T, Muller M, Stockinger S. 2005. The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 5:675-687. http://dx.doi.org/10.1038/nri1684.
40. Schofield L, Ferreira A, Altszuler R, Nussenzweig V, Nussenzweig RS. 1987. Interferon-gamma inhibits the intrahepatocytic development of malaria parasites in vitro. J Immunol 139:2020-2025.
41. Vergara U, Ferreira A, Schellekens H, Nussenzweig V. 1987. Mechanism of escape of exoerythrocytic forms (EEF) of malaria parasites from the inhibitory effects of interferon-gamma. J Immunol 138:4447-4449.
42. Mellouk S, Green SJ, Nacy CA, Hoffman SL. 1991. IFN-gamma inhibits development of Plasmodium berghei exoerythrocytic stages in hepatocytes by an L-arginine-dependent effector mechanism. J Immunol 146: 3971-3976.
43. Zuzarte-Luis V, Sales-Dias J, Mota MM. 2014. Simple, sensitive and quantitative bioluminescence assay for determination of malaria prepatent period. Malar J 13:15. http://dx.doi.org/10.1186/1475-2875-13-15.
44. Owusu-Agyei S, Koram KA, Baird JK, Utz GC, Binka FN, Nkrumah FK, Fryauff DJ, Hoffman SL. 2001. Incidence of symptomatic and asymptomatic Plasmodium falciparum infection following curative therapy in adult residents of northern Ghana. Am J Trop Med Hyg 65:197-203.
45. Moormann AM, Sumba PO, Chelimo K, Fang H, Tisch DJ, Dent AE, John CC, Long CA, Vulule J, Kazura JW. 2013. Humoral and cellular immunity to Plasmodium falciparum merozoite surface protein 1 and protection from infection with blood-stage parasites. J Infect Dis 208: 149-158. http://dx.doi.org/10.1093/infdis/jit134.
46. Sokhna CS, Faye FBK, Spiegel A, Dieng H, Trape JF. 2001. Rapid reappearance of Plasmodium falciparum after drug treatment among Senegalese adults exposed to moderate seasonal transmission. Am J Trop Med Hyg 65:167-170.
47. Sagara I, Sangare D, Dolo G, Guindo A, Sissoko M, Sogoba M, Niambele MB, Yalcoue D, Kaslow DC, Dicko A, Klion AD, Diallo D, Miller LH, Toure Y, Doumbo O. 2002. A high malaria reinfection rate in children and young adults living under a low entomological inoculation rate in a periurban area of Bamako, Mali. Am J Trop Med Hyg 66:310-313.
48. Miller JL, Sack BK, Baldwin M, Vaughan AM, Kappe SH. 3 April 2014, posting date. Interferon-mediated innate immune responses against malaria parasite liver stages. Cell Rep http://dx.doi.org/10.1016/j.celrep.2014.03.018.
49. Richie TL. 1988. Interactions between malaria parasites infecting the same vertebrate host. Parasitology 96(Pt 3):607-639.
50. Greenhouse B, Myrick A, Dokomajilar C, Woo JM, Carlson EJ, Rosenthal PJ, Dorsey G. 2006. Validation of microsatellite markers for use in genotyping polyclonal Plasmodium falciparum infections. Am J Trop Med Hyg 75:836-842.
51. Juliano JJ, Porter K, Mwapasa V, Sem R, Rogers WO, Ariey F, Wongsrichanalai C, Read A, Meshnick SR. 2010. Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc Natl Acad Sci USA 107:20138-20143. http://dx.doi.org/10.1073/pnas.1007068107.
52. Black J, Hommel M, Snounou G, Pinder M. 1994. Mixed infections with Plasmodium falciparum and P malariae and fever in malaria. Lancet 343: 1095.
53. Bruce MC, Macheso A, Kelly-Hope LA, Nkhoma S, McConnachie A, Molyneux ME. 2008. Effect of transmission setting and mixed species infections on clinical measures of malaria in Malawi. PLoS One 3:e2775. http://dx.doi.org/10.1371/journal.pone.0002775.
54. Doolan DL, Dobano C, Baird JK. 2009. Acquired immunity to malaria. Clin Microbiol Rev 22:13-36, table of contents. http://dx.doi.org/10.1128/CMR.00025-08.
55. Horras CJ, Lamb CL, Mitchell KA. 2011. Regulation of hepatocyte fate by interferon-gamma. Cytokine Growth Factor Rev 22:35-43. http://dx.doi.org/10.1016/j.cytogfr.2011.01.001.
56. Schoenborn JR, Wilson CB. 2007. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol 96:41-101. http://dx.doi.org/10.1016/S0065-2776(07)96002-2.