Insufficiently defined genetic background confounds phenotypes in transgenic studies as exemplified by malaria infection in Tlr9 knockout mice

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Geurts, Nathalie ^a   Martens, Erik ^a   Verhenne, Sebastien ^a,c   Lays, Natacha ^a   Thijs, Greet ^a   Magez, Stefan ^b   Cauwe, Bénédicte ^a   Li, Sandra ^a   Heremans, Hubertine ^a   Opdenakker, Ghislain ^a   van den Steen, Philippe E ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

TOLL LIKE RECEPTOR 9; TLR9 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACKCROSSING; CONTROLLED STUDY; FEMALE; GENE; GENE FUNCTION; GENE INACTIVATION; GENE MUTATION; GENETIC ANALYSIS; GENETIC HETEROGENEITY; INFECTION SENSITIVITY; KNOCKOUT MOUSE; MALARIA; MALE; MORTALITY; MOUSE; NONHUMAN; PARASITEMIA; PHENOTYPIC VARIATION; POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TOLL LIKE RECEPTOR 9 GENE; TRANSGENIC ORGANISM; ANIMAL; GENETICS; METABOLISM; MOUSE MUTANT; PARASITOLOGY; PATHOGENICITY; PLASMODIUM CHABAUDI; TRANSGENIC MOUSE;

ANIMALIA; MUS; PLASMODIUM CHABAUDI CHABAUDI;

ANIMALS; MALARIA; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PLASMODIUM CHABAUDI; POLYMORPHISM, SINGLE NUCLEOTIDE; TOLL-LIKE RECEPTOR 9;

EID: 80855156788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027131     Document Type: Article

References (80)

1. Thorsby E, Lie BA, (2005) HLA associated genetic predisposition to autoimmune diseases: Genes involved and possible mechanisms. Transpl Immunol 14: 175-182.
2. Hafler DA, Compston A, Sawcer S, Lander ES, Daly MJ, et al. (2007) Risk alleles for multiple sclerosis identified by a genomewide study. N Engl J Med 357: 851-862.
3. Nejentsev S, Howson JM, Walker NM, Szeszko J, Field SF, et al. (2007) Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 450: 887-892.
4. MacKay K, Eyre S, Myerscough A, Milicic A, Barton A, et al. (2002) Whole-genome linkage analysis of rheumatoid arthritis susceptibility loci in 252 affected sibling pairs in the United Kingdom. Arthritis Rheum 46: 632-639.
5. Lyke KE, Fernandez-Vina MA, Cao K, Hollenbach J, Coulibaly D, et al. (2011) Association of HLA alleles with Plasmodium falciparum severity in Malian children. Tissue Antigens 77: 562-571.
6. Jepson A, Sisay-Joof F, Banya W, Hassan-King M, Frodsham A, et al. (1997) Genetic linkage of mild malaria to the major histocompatibility complex in Gambian children: study of affected sibling pairs. BMJ 315: 96-97.
7. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, et al. (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603.
8. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, et al. (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 42: 1118-1125.
9. Schroder NW, Schumann RR, (2005) Single nucleotide polymorphisms of Toll-like receptors and susceptibility to infectious disease. Lancet Infect Dis 5: 156-164.
10. Mockenhaupt FP, Hamann L, von Gaertner C, Bedu-Addo G, von Kleinsorgen C, et al. (2006) Common polymorphisms of toll-like receptors 4 and 9 are associated with the clinical manifestation of malaria during pregnancy. J Infect Dis 194: 184-188.
11. Hamann L, Bedu-Addo G, Eggelte TA, Schumann RR, Mockenhaupt FP, (2010) The toll-like receptor 1 variant S248N influences placental malaria. Infect Genet Evol 10: 785-789.
12. Basu M, Maji AK, Chakraborty A, Banerjee R, Mullick S, et al. (2010) Genetic association of Toll-like-receptor 4 and tumor necrosis factor-alpha polymorphisms with Plasmodium falciparum blood infection levels. Infect Genet Evol 10: 686-696.
13. Lopez C, Saravia C, Gomez A, Hoebeke J, Patarroyo MA, (2010) Mechanisms of genetically-based resistance to malaria. Gene 467: 1-12.
14. McCall MB, Netea MG, Hermsen CC, Jansen T, Jacobs L, et al. (2007) Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. J Immunol 179: 162-171.
15. Franklin BS, Parroche P, Ataide MA, Lauw F, Ropert C, et al. (2009) Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Natl Acad Sci U S A 106: 5789-5794.
16. Franklin BS, Ishizaka ST, Lamphier M, Gusovsky F, Hansen H, et al. (2011) Therapeutical targeting of nucleic acid-sensing Toll-like receptors prevents experimental cerebral malaria. Proc Natl Acad Sci U S A 108: 3689-3694.
17. Perry JA, Olver CS, Burnett RC, Avery AC, (2005) Cutting edge: the acquisition of TLR tolerance during malaria infection impacts T cell activation. J Immunol 174: 5921-5925.
18. Griffith JW, O'Connor C, Bernard K, Town T, Goldstein DR, et al. (2007) Toll-like receptor modulation of murine cerebral malaria is dependent on the genetic background of the host. J Infect Dis 196: 1553-1564.
19. Sigmund CD, (2000) Viewpoint: are studies in genetically altered mice out of control? Arterioscler Thromb Vasc Biol 20: 1425-1429.
20. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, et al. (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269: 230-234.
21. Sanford LP, Kallapur S, Ormsby I, Doetschman T, (2001) Influence of genetic background on knockout mouse phenotypes. Methods Mol Biol 158: 217-225.
22. Coban C, Ishii KJ, Uematsu S, Arisue N, Sato S, et al. (2007) Pathological role of Toll-like receptor signaling in cerebral malaria. Int Immunol 19: 67-79.
23. Togbe D, Schofield L, Grau GE, Schnyder B, Boissay V, et al. (2007) Murine cerebral malaria development is independent of toll-like receptor signaling. Am J Pathol 170: 1640-1648.
24. Lepenies B, Cramer JP, Burchard GD, Wagner H, Kirschning CJ, et al. (2008) Induction of experimental cerebral malaria is independent of TLR2/4/9. Med Microbiol Immunol 197: 39-44.
25. Kordes M, Matuschewski K, Hafalla JC, (2011) Caspase-1 Activation of Interleukin-1{beta} (IL-1{beta}) and IL-18 Is Dispensable for Induction of Experimental Cerebral Malaria. Infect Immun 79: 3633-3641.
26. Gowda DC, (2007) TLR-mediated cell signaling by malaria GPIs. Trends Parasitol 23: 596-604.
27. Pichyangkul S, Yongvanitchit K, Kum-arb U, Hemmi H, Akira S, et al. (2004) Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. J Immunol 172: 4926-4933.
28. Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, et al. (2005) Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 201: 19-25.
29. Coban C, Yagi M, Ohata K, Igari Y, Tsukui T, et al. (2010) The malarial metabolite hemozoin and its potential use as a vaccine adjuvant. Allergol Int 59: 115-124.
30. Coban C, Igari Y, Yagi M, Reimer T, Koyama S, et al. (2010) Immunogenicity of whole-parasite vaccines against Plasmodium falciparum involves malarial hemozoin and host TLR9. Cell Host Microbe 7: 50-61.
31. Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, et al. (2007) Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci U S A 104: 1919-1924.
32. Gowda NM, Wu X, Gowda DC, (2011) The Nucleosome (Histone-DNA Complex) Is the TLR9-Specific Immunostimulatory Component of Plasmodium falciparum That Activates DCs. PLoS One 6: e20398.
33. Barrera V, Skorokhod OA, Baci D, Gremo G, Arese P, et al. (2011) Host fibrinogen stably bound to hemozoin rapidly activates monocytes via TLR-4 and CD11b/CD18-integrin: a new paradigm of hemozoin action. Blood 117: 5674-5682.
34. Taylor-Robinson AW, (2010) Regulation of immunity to Plasmodium: implications from mouse models for blood stage malaria vaccine design. Exp Parasitol 126: 406-414.
35. Seixas E, Moura Nunes JF, Matos I, Coutinho A, (2009) The interaction between DC and Plasmodium berghei/chabaudi-infected erythrocytes in mice involves direct cell-to-cell contact, internalization and TLR. Eur J Immunol 39: 1850-1863.
36. Franklin BS, Rodrigues SO, Antonelli LR, Oliveira RV, Goncalves AM, et al. (2007) MyD88-dependent activation of dendritic cells and CD4(+) T lymphocytes mediates symptoms, but is not required for the immunological control of parasites during rodent malaria. Microbes Infect 9: 881-890.
37. Cadman ET, Abdallah AY, Voisine C, Sponaas AM, Corran P, et al. (2008) Alterations of splenic architecture in malaria are induced independently of Toll-like receptors 2, 4, and 9 or MyD88 and may affect antibody affinity. Infect Immun 76: 3924-3931.
38. Voisine C, Mastelic B, Sponaas AM, Langhorne J, (2010) Classical CD11c+ dendritic cells, not plasmacytoid dendritic cells, induce T cell responses to Plasmodium chabaudi malaria. Int J Parasitol 40: 711-719.
39. von der Weid T, Honarvar N, Langhorne J, (1996) Gene-targeted mice lacking B cells are unable to eliminate a blood stage malaria infection. J Immunol 156: 2510-2516.
40. Langhorne J, Quin SJ, Sanni LA, (2002) Mouse models of blood-stage malaria infections: immune responses and cytokines involved in protection and pathology. Chem Immunol 80: 204-228.
41. Taylor-Robinson AW, Phillips RS, (1994) B cells are required for the switch from Th1- to Th2-regulated immune responses to Plasmodium chabaudi chabaudi infection. Infect Immun 62: 2490-2498.
42. Mota MM, Brown KN, Holder AA, Jarra W, (1998) Acute Plasmodium chabaudi chabaudi malaria infection induces antibodies which bind to the surfaces of parasitized erythrocytes and promote their phagocytosis by macrophages in vitro. Infect Immun 66: 4080-4086.
43. Jegerlehner A, Maurer P, Bessa J, Hinton HJ, Kopf M, et al. (2007) TLR9 signaling in B cells determines class switch recombination to IgG2a. J Immunol 178: 2415-2420.
44. Lin L, Gerth AJ, Peng SL, (2004) CpG DNA redirects class-switching towards "Th1-like" Ig isotype production via TLR9 and MyD88. Eur J Immunol 34: 1483-1487.
45. Kwiatkowski D, (2000) Genetic susceptibility to malaria getting complex. Curr Opin Genet Dev 10: 320-324.
46. Rihet P, Traore Y, Abel L, Aucan C, Traore-Leroux T, et al. (1998) Malaria in humans: Plasmodium falciparum blood infection levels are linked to chromosome 5q31-q33. Am J Hum Genet 63: 498-505.
47. Beck JA, Lloyd S, Hafezparast M, Lennon-Pierce M, Eppig JT, et al. (2000) Genealogies of mouse inbred strains. Nat Genet 24: 23-25.
48. Stevenson MM, Lyanga JJ, Skamene E, (1982) Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect Immun 38: 80-88.
49. Fortin A, Stevenson MM, Gros P, (2002) Complex genetic control of susceptibility to malaria in mice. Genes Immun 3: 177-186.
50. Chang KH, Tam M, Stevenson MM, (2004) Inappropriately low reticulocytosis in severe malarial anemia correlates with suppression in the development of late erythroid precursors. Blood 103: 3727-3735.
51. Fortin A, Belouchi A, Tam MF, Cardon L, Skamene E, et al. (1997) Genetic control of blood parasitaemia in mouse malaria maps to chromosome 8. Nat Genet 17: 382-383.
52. Min-Oo G, Fortin A, Pitari G, Tam M, Stevenson MM, et al. (2007) Complex genetic control of susceptibility to malaria: positional cloning of the Char9 locus. J Exp Med 204: 511-524.
53. Hernandez-Valladares M, Rihet P, ole-MoiYoi OK, Iraqi FA, (2004) Mapping of a new quantitative trait locus for resistance to malaria in mice by a comparative mapping approach with human Chromosome 5q31-q33. Immunogenetics 56: 115-117.
54. Foote SJ, Burt RA, Baldwin TM, Presente A, Roberts AW, et al. (1997) Mouse loci for malaria-induced mortality and the control of parasitaemia. Nat Genet 17: 380-381.
55. Montagutelli X, (2000) Effect of the genetic background on the phenotype of mouse mutations. J Am Soc Nephrol 11 (Suppl 16): S101-S105.
56. Yoshiki A, Moriwaki K, (2006) Mouse phenome research: implications of genetic background. ILAR J 47: 94-102.
57. Gerlai R, (1996) Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci 19: 177-181.
58. Banbury Conference on genetic background in mice (1997) Mutant mice and neuroscience: recommendations concerning genetic background. Neuron 19: 755-759.
59. Wolfer DP, Crusio WE, Lipp HP, (2002) Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends Neurosci 25: 336-340.
60. Crusio WE, (2004) Flanking gene and genetic background problems in genetically manipulated mice. Biol Psychiatry 56: 381-385.
61. Hu J, Van den Steen PE, Sang QX, Opdenakker G, (2007) Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 6: 480-498.
62. Taft RA, Davisson M, Wiles MV, (2006) Know thy mouse. Trends Genet 22: 649-653.
63. Stevens JC, Banks GT, Festing MF, Fisher EM, (2007) Quiet mutations in inbred strains of mice. Trends Mol Med 13: 512-519.
64. Kiselycznyk C, Holmes A, (2011) All (C57BL/6) Mice are not Created Equal. Front Neurosci 5: 10.
65. Bygrave AE, Rose KL, Cortes-Hernandez J, Warren J, Rigby RJ, et al. (2004) Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in gene-targeted mice. PLoS Biol 2: E243.
66. Li C, Seixas E, Langhorne J, (2001) Rodent malarias: the mouse as a model for understanding immune responses and pathology induced by the erythrocytic stages of the parasite. Med Microbiol Immunol 189: 115-126.
67. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, et al. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485-498.
68. Hisaeda H, Tetsutani K, Imai T, Moriya C, Tu L, et al. (2008) Malaria parasites require TLR9 signaling for immune evasion by activating regulatory T cells. J Immunol 180: 2496-2503.
69. Wunderlich F, Marinovski P, Benten WP, Schmitt-Wrede HP, Mossmann H, (1991) Testosterone and other gonadal factor(s) restrict the efficacy of genes controlling resistance to Plasmodium chabaudi malaria. Parasite Immunol 13: 357-367.
70. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, et al. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
71. Van den Steen PE, Geurts N, Deroost K, Van Aelst I, Verhenne S, et al. (2010) Immunopathology and dexamethasone therapy in a new model for malaria-associated acute respiratory distress syndrome. Am J Respir Crit Care Med 181: 957-968.
72. Akanmori BD, Kawai S, Suzuki M, (1996) Recombinant mouse IL-6 boosts specific serum anti-plasmodial IgG subtype titres and suppresses parasitaemia in Plasmodium chabaudi chabaudi infection. Parasite Immunol 18: 193-199.
73. Sanni LA, Jarra W, Li C, Langhorne J, (2004) Cerebral edema and cerebral hemorrhages in interleukin-10-deficient mice infected with Plasmodium chabaudi. Infect Immun 72: 3054-3058.
74. Meding SJ, Cheng SC, Simon-Haarhaus B, Langhorne J, (1990) Role of gamma interferon during infection with Plasmodium chabaudi chabaudi. Infect Immun 58: 3671-3678.
75. The Jackson Laboratory (2007) Breeding strategies for Maintaining Colonies of Laboratory Mice. Available: http://iacuc.ucsd.edu/PDF_References/BreedingStrategiesManual.pdf. Accessed 2011 April 17.
76. CLEA Japan (2011) Japan mouse/rat strain resources database. Available: http://www.shigen.nig.ac.jp/mouse/jmsr/top.jsp. Accessed 2011 April 17.
77. Yoshida S, Araki H, Yokomine T, (2010) Baculovirus-based nasal drop vaccine confers complete protection against malaria by natural boosting of vaccine-induced antibodies in mice. Infect Immun 78: 595-602.
78. Griffith JW, Sun T, McIntosh MT, Bucala R, (2009) Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol 183: 5208-5220.
79. Wu X, Gowda NM, Kumar S, Gowda DC, (2010) Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J Immunol 184: 4338-4348.
80. Yasuda K, Yu P, Kirschning CJ, Schlatter B, Schmitz F, et al. (2005) Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and-independent pathways. J Immunol 174: 6129-6136.