Complex genetic control of susceptibility to malaria in mice

Genes and Immunity

Volumn 3, Issue 4, 2002, Pages 177-186

  Fortin, A ^a   Stevenson, M M ^a   Gros, P ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Complex trait; Genetic susceptibility; Host defense; Malaria; Mouse model; Recombinant congenic

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; TUMOR NECROSIS FACTOR ALPHA;

CHROMOSOME 17; CHROMOSOME 3; CHROMOSOME 8; CHROMOSOME 9; DISEASE SEVERITY; ERYTHROPOIESIS; GENE CONTROL; GENE LOCUS; GENE MAPPING; GENETIC LINKAGE; GENETIC PREDISPOSITION; GENETIC SUSCEPTIBILITY; GENETIC TRAIT; GENETIC VARIABILITY; HEREDITY; IMMUNE RESPONSE; MALARIA; MOLECULAR GENETICS; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; RETICULOCYTOSIS; REVIEW; ANIMAL; CONGENIC STRAIN; CROSS BREEDING; GENETICS; HUMAN; MOUSE STRAIN; PHYSIOLOGY; SPECIES DIFFERENCE;

PLASMODIUM CHABAUDI;

ANIMALS; CROSSES, GENETIC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALARIA; MICE; MICE, CONGENIC; MICE, INBRED STRAINS; SPECIES SPECIFICITY;

EID: 0036615515     PISSN: 14664879     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.gene.6363841     Document Type: Review

References (81)

1. Butler D. Time to put malaria control on the global agenda. Nature 1997; 386: 535-536.
2. www.who.ch.
3. Marsh K. 30 years of science and technology: the example of malaria. The Lancet 1997; 349: SIII1-SIII2.
4. Hill AV. The immunogenetics of human infectious diseases. Annu Rev Immunol 1998; 16: 593-617.
5. Mohan K, Stevenson MM. In: Sherman IW (ed). Malaria. American Society for Microbiology: Washington, DC, 1998, pp 467-493.
6. Kwiatkowski D. Genetic susceptibility to malaria getting complex. Curr Opin Genet Dev 2000; 10: 320-324.
7. Taylor JG, Ferdig MT, Su XZ, Wellems TE. Toward quantitative genetic analysis of host and parasite traits in the manifestations of Plasmodium falciparum malaria. Curr Opin Genet Dev 2000; 10: 314-319.
8. Modiano D, Petrarca V, Sirima BS et al. Different response to Plasmodium falciparum malaria in west African sympatric ethnic groups. Proc Natl Acad Sci USA 1996; 93: 13206-13211.
9. Abel L, Cot M, Mulder L, Carnevale P, Feingold J. Segregation analysis detects a major gene controlling blood infection levels in human malaria. Am J Hum Genet 1992; 50: 1308-1317.
10. Garcia A, Cot M, Chippaux JP et al. Genetic control of blood infection levels in human malaria: evidence for a complex genetic model. Am J Trop Med Hyg 1998; 58: 480-488.
11. Rihet P, Abel L, Traore Y, Traore-Leroux T, Aucan C, Fumoux F. Human malaria: segregation analysis of blood infection levels in a suburban area and a rural area in Burkina Faso. Genet Epidemiol 1998; 15: 435-450.
12. Rihet P, Traore Y, Abel L, Aucan C, Traore-Leroux T, Fumoux F. Malaria in humans: Plasmodium falciparum blood infection levels are linked to chromosome 5q31-q33. Am J Hum Genet 1998; 63: 498-505.
13. Stirnadel HA, Beek HP, Alpers MP, Smith TA. Heritability and segregation analysis of immune responses to specific malaria antigens in Papua New Guinea. Genet Epidemiol 1999; 17: 16-34.
14. Sjoberg K, Lepers JP, Raharimalala L et al. Genetic regulation of human anti-malarial antibodies in twins. Proc Natl Acad Sci USA 1992; 89: 2101-2104.
15. Aucan C, Traore Y, Fumoux F, Rihet P. Familial correlation of immunoglobulin G subclass responses to Plasmodium flaciparum antigens in Burkina Faso. Infect Immun 2001; 69: 996-1001.
16. Jepson AP, Banya WA, Sisay-Joof F, Hassan-King M, Bennett S, Whittle HC. Genetic regulation of fever in Plasmodium falciparum malaria in Gambian twin children. J Infect Dis 1995; 172: 316-319.
17. Jepson A, Sisay-Joof F, Banya W et al. Genetic linkage of mild malaria to the major histocompatibility complex in Gambian children: study of affected sibling pairs. BMJ 1997; 315: 96-97.
18. Tournamille C, Colin Y, Cartron JP, Le Van Kim C. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet 1995; 10: 224-228.
19. Pasvol G, Weatherall DJ, Wilson RJ. Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature 1978; 274: 701-703.
20. Hill AV, Allsopp CE, Kwiatkowski D et al. Common west African HLA antigens are associated with protection from severe malaria. Nature 1991; 352: 595-600.
21. Chippaux JP, Massougbodji A, Boulard JC, Akogbeto M. Morbidity and severity of malaria attacks in carriers of sickle-cell trait. Rev Epidemiol Sante Publique 1992; 40: 240-245.
22. Shear HL, Roth Jr EF, Fabry ME et al. Transgenic mice expressing human sickle hemoglobin are partially resistant to rodent malaria. Blood 1993; 81: 222-226.
23. Williams TN, Maitland K, Bennett S et al. High incidence of malaria in alpha-thalassaemic children. Nature 1996; 383: 522-525.
24. Allen SJ, O'Donnell A, Alexander ND et al. alpha+-Thalassemia protects children against disease caused by other infections as well as malaria. Proc Natl Acad Sci USA 1997; 94: 14736-14741.
25. Weatherall DJ. Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat Rev Genet 2001; 2: 245-255.
26. Ruwende C, Khoo SC, Snow RW et al. Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 1995; 376: 246-249.
27. Tishkoff SA, Varkonyi R, Cahinhinan N et al. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 2001; 293: 455-462.
28. Wilson AG, Symons JA, McDowell TL, McDevitt HO, Duff GW. Effects of a polymorphism in the human tumor necrosis factor alpha promoter on transcriptional activation. Proc Natl Acad Sci USA 1997; 94: 3195-3199.
29. McGuire W, Hill AV, Allsopp CE, Greenwood BM, Kwiatkowski D. Variation in the TNF-alpha promoter region associated with susceptibility to cerebral malaria. Nature 1994; 371: 508-510.
30. McGuire W, Knight JC, Hill AV, Allsopp CE, Greenwood BM, Kwiatkowski D. Severe malarial anemia annd cerebral malaria are associated with different tumor necrosis factor promoter alleles. J Infect Dis 1999; 179: 287-290.
31. Knight JC, Udalova I, Hill AV et al. A polymorphism that affects OCT-1 binding to the TNF promoter region is associated with severe malaria. Nat Genet 1999; 22: 145-150.
32. Vidal SM, Malo D, Vogan K, Skamene E, Gros P. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 1993; 73: 469-485.
33. Poltorak A, He X, Smirnova I et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998; 282: 2085-2088.
34. Qureshi ST, Lariviere L, Leveque G et al. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J Exp Med 1999; 189: 615-625.
35. Lee SH, Girard S, Macina D et al. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat Genet 2001; 28: 42-45.
36. Brown MG, Dokun AO, Heusel JW et al. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 2001; 292: 934-937.
37. Taylor-Robinson AW. Regulation of immunity to malaria: valuable lessons learned from murine models. Parasitol Today 1995; 11: 334-342.
38. Langhorne J, Meding SJ, Eichmann K, Gillard SS. The response of CD4+ T cells to Plasmodium chabaudi chabaudi. Immunol Rev 1989; 112: 71-94.
39. Podoba JE, Stevenson MM. CD4+ and CD8+ T lymphocytes both contribute to acquired immunity to blood-stage Plasmodium chabaudi AS. Infect Immun 1991; 59: 51-58.
40. Stevenson MM, Skamene E. Modulation of primary antibody responses to sheep erythrocytes in Plasmodium chabaudi-infected resistant and susceptible mouse strains. Infect Immun 1986; 54: 600-602.
41. Ahvazi BC, Jacobs P, Stevenson MM. Role of macrophage-derived nitric oxide in suppression of lymphocyte proliferation during blood-stage malaria. J Leukoc Biol 1995; 58: 23-31.
42. Cox J, Semoff S, Hommel M. Plasmodium chabaudi: a rodent malaria model for in-vivo and in-vitro cytoadherence of malaria parasites in the absence of knobs. Parasite Immunol 1987; 9: 543-561.
43. Eugui EM, Allison AC. Differences in susceptibility of various mouse strains to haemoprotozoan infections: possible correlation with natural killer activity. Parasite Immunol 1980; 2: 277-292.
44. Stevenson MM, Lyanga JJ, Skamene E. Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect Immun 1982; 38: 80-88.
45. Stevenson MM, Ghadirian E, Phillips NC, Rae D, Podoba JE. Role of mononuclear phagocytes in elimination of Plasmodium chabaudi AS infection. Parasite Immunol 1989; 11: 529-544.
46. Stevenson MM, Tam MF, Rae D. Dependence on cell-mediated mechanisms for the appearance of crisis forms during Plasmodium chabaudi AS infection in C57BL/6 mice. Microb Pathog 1990; 9: 303-314.
47. Meding SJ, Langhorne J. CD4+ T cells and B cells are necessary for the transfer of protective immunity to Plasmodium chabaudi chabaudi. Eur J Immunol 1991; 21: 1433-1438.
48. Suss G, Eichmann K, Kury E, Linke A, Langhorne J. Roles of CD4- and CD8- bearing T lymphocytes in the immune response to the erythrocytic stages of Plasmodium chabaudi. Infect Immun 1988; 56: 3081-3088.
49. Riopel J, Tam M, Mohan K, Marino MW, Stevenson MM. Granulocyte-macrophage colony-stimulating factor-deficient mice have impaired resistance to blood-stage malaria. Infect Immun 2001; 69: 129-136.
50. Su Z, Stevenson MM. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect Immun 2000; 68: 4399-4406.
51. Sam H, Su Z, Stevenson MM. Deficiency in tumor necrosis factor alpha activity does not impair early protective Th1 responses against blood-stage malaria. Infect Immun 1999; 67: 2660-2664.
52. Nogami S, Watanabe J, Nakagaki K et al. Involvement of macrophage scavenger receptors in protection against murine malaria. Am J Trop Med Hyg 1998; 59: 843-845.
53. Foote SJ, Burt RA, Baldwin TM et al. Mouse loci for malaria-induced mortality and the control of parasitaemia (letter). Nat Genet 1997; 17: 380-381.
54. Wunderlich F, Mossmann H, Helwig M, Schillinger G. Resistance to Plasmodium chabaudi in B10 mice: influence of the H-2 complex and testosterone. Infect Immun 1988; 56: 2400-2406.
55. Fortin A, Belouchi A, Tam MF et al. Genetic control of blood parasitaemia in mouse malaria maps to chromsome 8 (letter). Nat Genet 1997; 17: 382-383.
56. Yap GS, Stevenson MM. Plasmodium chabaudi AS: erythropoietic responses during infection in resistant and susceptible mice. Exp Parasitol 1992; 75: 340-352.
57. Stevenson MM, Tam MF. Differential induction of helper T cell subsets during blood-stage Plasmodium chabaudi AS infection in resistant and susceptible mice. Clin Exp Immunol 1993; 92: 77-83.
58. Jacobs P, Radzioch D, Stevenson MM. A Th1-associated increase in tumor necrosis factor alpha expression in the spleen correlates with resistance to blood-stage malaria in mice. Infect Immun 1996; 64: 535-541.
59. Stevenson MM, Tam MF, Wolf SF, Sher A. IL-12 induced protection against blood-stage Plasmodium chabaudi AS requires IFN-gamma and TNF-alpha and occurs via a nitric oxide-dependent mechanism. J Immunol 1995; 155: 2545-2556.
60. Mohan K, Stevenson MM. Interleukin-12 corrects severe anemia during blood-stage Plasmodium chabaudi AS in susceptible A/J mice. Exp Hematol 1998; 26: 45-52.
61. Stevenson MM, Tam MF, Belosevic M, van der Meide PH, Podoba JE. Role of endogenous gamma interferon in host response to infection with blood-stage Plasmodium chabaudi AS. Infect Immun 1990; 58: 3225-3232.
62. www.jax.org.
63. Burt RA, Baldwin TM, Marshall VM, Foote SJ. Temporal expression of an H2-linked locus in host response to mouse malaria. Immunogenetics 1999, 50: 278-285.
64. Suzuki H, Kurihara Y, Takeya M et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 1997; 386: 292-296.
65. Fortin A, Penman M, Stevenson MM, Krieger M, Gros P. Identification and characterization of naturally occurring variants of the macrophage scavenger receptor (SR-A). Mamm Genome 2000; 11: 779-785.
66. Daugherty A, Whitman SC, Block AE, Rateri DL. Polymorphism of class A scavenger receptors in C57BL/6 mice. J Lipid Res 2000; 41: 1568-1577.
67. Demant P, Hart AA. Recombinant congenic strains - a new tool for analyzing genetic traits determined by more than one gene. Immunogenetics 1986; 24: 416-422.
68. Fortin A, Diez E, Rochefort D et al. Recombinant congenic strains derived from A/J and C57B1/6J: a tool for genetic dissection of complex traits. Genomics 2001; 74: 21-35.
69. Fortin A, Cardon LR, Tam M, Skamene E, Stevenson MM, Gros P. Identification of a new malaria susceptibility locus (Char4) in recombinant congenic strains of mice. Proc Natl Acad Sci USA 2001; 98: 10793-10798.
70. Oosterwegel M, van de Wetering M, Timmerman J et al. Differential expression of the HMG box factors TCF-1 and LEF-1 during murine embryogenesis. Development 1993; 118: 439-448.
71. Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R. Wnt3a(-/-)-like phenotype and limb deficiency in Lefl(-/-)Tcfl(-/-) mice. Genes Dev 1999; 13: 709-717.
72. Minta JO, Wong MJ, Kozak CA, Kunnath-Muglia LM, Goldberger G. cDNA cloning, sequencing and chromosomal assignment of the gene for mouse complement factor I (C3b/C4b inactivator): identification of a species specific divergent segment in factor I. Mol Immunol 1996; 33: 101-112.
73. Gervais F, Stevenson M, Skamene E. Genetic control of resistance to Listeria monocytogenes: regulation of leukocyte inflammatory responses by the Hc locus. J Immunol 1984; 132: 2078-2083.
74. Gervais F, Desforges C, Skamene E. The C5-sufficient A/J congenic mouse strain. Inflammatory response and resistance to Listeria monocytogenes. J Immunol 1989; 142: 2057-2060.
75. Sha WC, Liou HC, Toumanen EI, Baltimore D. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 1995; 80: 321-330.
76. Yoshida H, Hayashi S, Kunisada T et al. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 1990; 345: 442-444.
77. Guleria I, Pollard JW. Aberrant macrophage and neutrophil population dynamics and impaired Th1 response to Listeria monocytogenes in colony-stimulating factor 1-deficient mice. Infect Immun 2001; 69: 1795-1807.
78. Gurtner GC, Davis V, Li H, McCoy MJ, Sharpe A, Cybulsky MI. Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev 1995; 9: 1-14.
79. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice. Impaired lymphocyte migration to bone marrow. J Exp Med 2001; 193: 741-754.
80. Benten WP, Bettenhaeuser U, Wunderlich F, Van Vliet E, Mossmann H. Testosterone-induced abrogation of self-healing of Plasmodium chabaudi malaria in B10 mice: mediation by spleen cells. Infect Immun 1991; 59: 4486-4490.
81. Flint J, Mott R. Finding the molecular basis of quantitative traits: Successes and pitfalls. Nat Rev Genet 2001; 2: 437-445.