Mammalian Genome

, Volume 29, Issue 7–8, pp 507–522 | Cite as

Host genetics in malaria: lessons from mouse studies

  • Hong Ming Huang
  • Brendan J. McMorran
  • Simon J. Foote
  • Gaetan Burgio


Malaria remains a deadly parasitic disease caused by Plasmodium, claiming almost half a million lives every year. While parasite genetics and biology are often the major targets in many studies, it is becoming more evident that host genetics plays a crucial role in the outcome of the infection. Similarly, Plasmodium infections in mice also rely heavily on the genetic background of the mice, and often correlate with observations in human studies, due to their high genetic homology with humans. As such, murine models of malaria are a useful tool for understanding host responses during Plasmodium infections, as well as dissecting host-parasite interactions through various genetic manipulation techniques. Reverse genetic approach such as quantitative trait loci studies and random mutagenesis screens have been employed to discover novel host genes that affect malaria susceptibility in mouse models, while other targeted studies utilize mouse models to validate observation from human studies. Herein, we review the findings from the past and present studies on murine models of hepatic and erythrocytic stages of malaria and speculate on how the current mouse models benefit from the recent development in CRISPR/Cas9 gene editing technology.



The authors thank National Health and Medical Research Council of Australia, Australian Society of Parasitology (ASP), OzEMalaR, National Collaborative Research Infrastructure Strategy (NCRIS), the Education Investment Fund from the Department of Education and Training, the Australian Phenomics Network, Howard Hughes Medical Institute and the Bill and Melinda Gates Foundation, the Japan Society for Promotion of Science (JSPS) and the Australian Research Council (ARC) for the funding, and Lora Starrs for the proofreading of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. Albuisson J, Murthy SE, Bandell M, Coste B, Louis-Dit-Picard H, Mathur J, Feneant-Thibault M, Tertian G, de Jaureguiberry JP, Syfuss PY, Cahalan S, Garcon L, Toutain F, Simon Rohrlich P, Delaunay J, Picard V, Jeunemaitre X, Patapoutian A (2013) Dehydrated hereditary stomatocytosis linked to gain-of-function mutations in mechanically activated PIEZO1 ion channels. Nat Commun 4:1884PubMedPubMedCentralGoogle Scholar
  2. Allison AC (1954) Protection afforded by sickle-cell trait against subtertian malareal infection. Br Med J 1:290–294PubMedPubMedCentralGoogle Scholar
  3. Alonso PL, Sacarlal J, Aponte JJ, Leach A, Macete E, Milman J, Mandomando I, Spiessens B, Guinovart C, Espasa M, Bassat Q, Aide P, Ofori-Anyinam O, Navia MM, Corachan S, Ceuppens M, Dubois MC, Demoitie MA, Dubovsky F, Menendez C, Tornieporth N, Ballou WR, Thompson R, Cohen J (2004) Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364:1411–1420PubMedGoogle Scholar
  4. Arita M, Nomura K, Arai H, Inoue K (1997) Alpha-tocopherol transfer protein stimulates the secretion of alpha-tocopherol from a cultured liver cell line through a brefeldin A-insensitive pathway. Proc Natl Acad Sci USA 94:12437–12441PubMedGoogle Scholar
  5. Atamni HJA, Ziner Y, Mott R, Wolf L, Iraqi FA (2017) Glucose tolerance female-specific QTL mapped in collaborative cross mice. Mamm Genome 28:20–30Google Scholar
  6. Auclair SR, Roth KE, Saunders BL, Ogborn KM, Sheikh AA, Naples J, Young AM, Boisen DK, Tavangar AT, Welch JE, Lantz CS (2014) Interleukin-3-deficient mice have increased resistance to blood-stage malaria. Infect Immun 82:1308–1314PubMedPubMedCentralGoogle Scholar
  7. Ayi K, Min-Oo G, Serghides L, Crockett M, Kirby-Allen M, Quirt I, Gros P, Kain KC (2008) Pyruvate kinase deficiency and malaria. N Engl J Med 358:1805–1810PubMedGoogle Scholar
  8. Ayi K, Liles WC, Gros P, Kain KC (2009) Adenosine triphosphate depletion of erythrocytes simulates the phenotype associated with pyruvate kinase deficiency and confers protection against Plasmodium falciparum in vitro. J Infect Dis 200:1289–1299PubMedGoogle Scholar
  9. Badell E, Pasquetto V, Vanrooijen N, Druilhe P (1995) A mouse model for human malaria erythrocytic stages. Parasitol Today 11:235–237Google Scholar
  10. Bae C, Gnanasambandam R, Nicolai C, Sachs F, Gottlieb PA (2013) Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1. Proc Natl Acad Sci USA 110:E1162–E1168Google Scholar
  11. Baldwin MR, Li X, Hanada T, Liu S-C, Chishti AH (2015) Merozoite surface protein 1 recognition of host glycophorin A mediates malaria parasite invasion of red blood cells. Blood 125:2704–2711PubMedPubMedCentralGoogle Scholar
  12. Bauer DC, McMorran BJ, Foote SJ, Burgio G (2015) Genome-wide analysis of chemically induced mutations in mouse in phenotype-driven screens. BMC Genom 16:1–8Google Scholar
  13. Beutler E, Dern R, Flanagan C (1955) Effect of sickle-cell trait on resistance to malaria. Br Med J 1:1189PubMedPubMedCentralGoogle Scholar
  14. Billo MA, Johnson ES, Doumbia SO, Poudiougou B, Sagara I, Diawara SI, Diakite M, Diallo M, Doumbo OK, Tounkara A, Rice J, James MA, Krogstad DJ (2012) Sickle cell trait protects against Plasmodium falciparum infection. American journal of epidemiology 176(Suppl 7):S175–S185Google Scholar
  15. Bongfen SE, Rodrigue-Gervais IG, Berghout J, Torre S, Cingolani P, Wiltshire SA, Leiva-Torres GA, Letourneau L, Sladek R, Blanchette M, Lathrop M, Behr MA, Gruenheid S, Vidal SM, Saleh M, Gros P (2012) An N-ethyl-N-nitrosourea (ENU)-induced dominant negative mutation in the JAK3 kinase protects against cerebral malaria. PLoS ONE 7:e31012PubMedPubMedCentralGoogle Scholar
  16. Bopp SE, Ramachandran V, Henson K, Luzader A, Lindstrom M, Spooner M, Steffy BM, Suzuki O, Janse C, Waters AP, Zhou Y, Wiltshire T, Winzeler EA (2010) Genome wide analysis of inbred mouse lines identifies a locus containing Ppar-gamma as contributing to enhanced malaria survival. PLoS ONE 5:e10903PubMedPubMedCentralGoogle Scholar
  17. Bopp SE, Rodrigo E, Gonzalez-Paez GE, Frazer M, Barnes SW, Valim C, Watson J, Walker JR, Schmedt C, Winzeler EA (2013) Identification of the Plasmodium berghei resistance locus 9 linked to survival on chromosome 9. Malar J 12:316PubMedPubMedCentralGoogle Scholar
  18. Burt RA, Baldwin TM, Marshall VM, Foote SJ (1999) Temporal expression of an H2-linked locus in host response to mouse malaria. Immunogenetics 50:278–285PubMedGoogle Scholar
  19. Burt RA, Marshall VM, Wagglen J, Rodda FR, Senyschen D, Baldwin TM, Buckingham LA, Foote SJ (2002) Mice that are congenic for the char2 locus are susceptible to malaria. Infect Immun 70:4750–4753PubMedPubMedCentralGoogle Scholar
  20. Carlson J, Nash GB, Gabutti V, al Yaman F, Wahlgren M (1994) Natural protection against severe Plasmodium falciparum malaria due to impaired rosette formation. Blood 84:3909–3914Google Scholar
  21. Carter R, Walliker D (1975) New observations on the malaria parasites of rodents of the Central African Republic—Plasmodium vinckei petteri subsp. nov. and Plasmodium chabaudi Landau, 1965. Ann Trop Med Parasitol 69:187–196PubMedGoogle Scholar
  22. Chen S, Lee B, Lee AY, Modzelewski AJ, He L (2016) Highly efficient mouse genome editing by CRISPR ribonucleoprotein electroporation of zygotes. J Biol Chem 291:14457–14467PubMedPubMedCentralGoogle Scholar
  23. Cholera R, Brittain NJ, Gillrie MR, Lopera-Mesa TM, Diakité SAS, Arie T (2008) Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc Natl Acad Sci USA 105:991–996PubMedGoogle Scholar
  24. Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, Beatty J, Beavis WD, Belknap JK, Bennett B, Berrettini W, Bleich A, Bogue M, Broman KW, Buck KJ, Buckler E, Burmeister M, Chesler EJ, Cheverud JM, Clapcote S, Cook MN, Cox RD, Crabbe JC, Crusio WE, Darvasi A, Deschepper CF, Doerge RW, Farber CR, Forejt J, Gaile D, Garlow SJ, Geiger H, Gershenfeld H, Gordon T, Gu J, Gu W, de Haan G, Hayes NL, Heller C, Himmelbauer H, Hitzemann R, Hunter K, Hsu HC, Iraqi FA, Ivandic B, Jacob HJ, Jansen RC, Jepsen KJ, Johnson DK, Johnson TE, Kempermann G, Kendziorski C, Kotb M, Kooy RF, Llamas B, Lammert F, Lassalle JM, Lowenstein PR, Lu L, Lusis A, Manly KF, Marcucio R, Matthews D, Medrano JF, Miller DR, Mittleman G, Mock BA, Mogil JS, Montagutelli X, Morahan G, Morris DG, Mott R, Nadeau JH, Nagase H, Nowakowski RS, O’Hara BF, Osadchuk AV, Page GP, Paigen B, Paigen K, Palmer AA, Pan HJ, Peltonen-Palotie L, Peirce J, Pomp D, Pravenec M, Prows DR, Qi Z, Reeves RH, Roder J, Rosen GD, Schadt EE, Schalkwyk LC, Seltzer Z, Shimomura K, Shou S, Sillanpaa MJ, Siracusa LD, Snoeck HW, Spearow JL, Svenson K, Tarantino LM, Threadgill D, Toth LA, Valdar W, de Villena FP, Warden C, Whatley S, Williams RW, Wiltshire T, Yi N, Zhang D, Zhang M, Zou F, Complex Trait C (2004) The collaborative cross, a community resource for the genetic analysis of complex traits. Nat Genet 36:1133–1137PubMedGoogle Scholar
  25. Clark MA, Goheen MM, Fulford A, Prentice AM, Elnagheeb MA, Patel J, Fisher N, Taylor SM, Kasthuri RS, Cerami C (2014) Host iron status and iron supplementation mediate susceptibility to erythrocytic stage Plasmodium falciparum. Nat Commun 5:4446PubMedPubMedCentralGoogle Scholar
  26. Coatney GR (1963) Pitfalls in a discovery: the chronicle of chloroquine. Am J Trop Med Hyg 12:121–128PubMedGoogle Scholar
  27. Cowman AF, Crabb BS (2006) Invasion of red blood cells by malaria parasites. Cell 124:755–766PubMedGoogle Scholar
  28. Cowman AF, Morry MJ, Biggs BA, Cross GA, Foote SJ (1988) Amino acid changes linked to pyrimethamine resistance in the dihydrofolate reductase-thymidylate synthase gene of Plasmodium falciparum. Proc Natl Acad Sci USA 85:9109–9113PubMedGoogle Scholar
  29. Cowman AF, Healer J, Marapana D, Marsh K (2016) Malaria: biology and disease. Cell 167:610–624PubMedGoogle Scholar
  30. Crabb BS, Cowman AF (2002) Plasmodium falciparum virulence determinants unveiled. Genome Biol 3:REVIEWS1031PubMedPubMedCentralGoogle Scholar
  31. Craig AG, Grau GE, Janse C, Kazura JW, Milner D, Barnwell JW, Turner G, Langhorne J, participants of the Hinxton Retreat meeting on Animal Models for Research on Severe M (2012) The role of animal models for research on severe malaria. PLoS Pathog 8:e1002401PubMedPubMedCentralGoogle Scholar
  32. Crompton PD, Pierce SK, Miller LH (2010) Advances and challenges in malaria vaccine development. J Clin Invest 120:4168–4178PubMedPubMedCentralGoogle Scholar
  33. Cunningham DA, Lin JW, Brugat T, Jarra W, Tumwine I, Kushinga G, Ramesar J, Franke-Fayard B, Langhorne J (2017) ICAM-1 is a key receptor mediating cytoadherence and pathology in the Plasmodium chabaudi malaria model. Malar J 16:185PubMedPubMedCentralGoogle Scholar
  34. Cytlak UM, Hannemann A, Rees DC, Gibson JS (2013) Identification of the Ca2+ entry pathway involved in deoxygenation-induced phosphatidylserine exposure in red blood cells from patients with sickle cell disease. Pflugers Arch 465:1651–1660PubMedPubMedCentralGoogle Scholar
  35. de Oliveira RB, Wang JP, Ram S, Gazzinelli RT, Finberg RW, Golenbock DT (2014) Increased survival in B-cell-deficient mice during experimental cerebral malaria suggests a role for circulating immune complexes. mBio 5:e00949–e00914Google Scholar
  36. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Silamut K, Imwong M, Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NPJ, Lindegardh N, Socheat D, White NJ (2009) Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361:455–467PubMedPubMedCentralGoogle Scholar
  37. Donoghue LJ, Livraghi-Butrico A, McFadden KM, Thomas JM, Chen G, Grubb BR, O’Neal WK, Boucher RC, Kelada SNP (2017) Identification of trans protein QTL for secreted airway mucins in mice and a causal role for Bpifb1. Genetics 207:801–812PubMedGoogle Scholar
  38. Durand PM, Coetzer TL (2008) Pyruvate kinase deficiency protects against malaria in humans. Haematologica 93:939–940PubMedGoogle Scholar
  39. Durrant C, Tayem H, Yalcin B, Cleak J, Goodstadt L, de Villena FPM, Mott R, Iraqi FA (2011) Collaborative cross mice and their power to map host susceptibility to Aspergillus fumigatus infection. Genome Res 21:1239–1248PubMedPubMedCentralGoogle Scholar
  40. Eber SW, Gonzalez JM, Lux ML, Scarpa AL, Tse WT, Dornwell M, Herbers J, Kugler W, Ozcan R, Pekrun A, Gallagher PG, Schroter W, Forget BG, Lux SE (1996) Ankyrin-1 mutations are a major cause of dominant and recessive hereditary spherocytosis. Nat Genet 13:214–218PubMedGoogle Scholar
  41. Emes RD, Goodstadt L, Winter EE, Ponting CP (2003) Comparison of the genomes of human and mouse lays the foundation of genome zoology. Hum Mol Genet 12:701–709PubMedGoogle Scholar
  42. Epiphanio S, Mikolajczak SA, Goncalves LA, Pamplona A, Portugal S, Albuquerque S, Goldberg M, Rebelo S, Anderson DG, Akinc A, Vornlocher HP, Kappe SH, Soares MP, Mota MM (2008) Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine plasmodium liver infection. Cell Host Microbe 3:331–338PubMedGoogle Scholar
  43. Erdman LK, Cosio G, Helmers AJ, Gowda DC, Grinstein S, Kain KC (2009) CD36 and TLR interactions in inflammation and phagocytosis: implications for malaria. J Immunol 183:6452–6459PubMedPubMedCentralGoogle Scholar
  44. Facer CA (1983) Merozoites of P. falciparum require glycophorin for invasion into red cells. Bull Soc Pathol Exot Filiales 76:463–469PubMedGoogle Scholar
  45. Facer CA (1995) Erythrocytes carrying mutations in spectrin and protein 4.1 show differing sensitivities to invasion by Plasmodium falciparum. Parasitol Res 81:52–57PubMedGoogle Scholar
  46. Favre N, Da Laperousaz C, Ryffel B, Weiss NA, Imhof BA, Rudin W, Lucas R, Piguet PF (1999) Role of ICAM-1 (CD54) in the development of murine cerebral malaria. Microbes Infect 1:961–968Google Scholar
  47. Ferreira A, Marguti I, Bechmann I, Jeney V, Chora A, Palha NR, Rebelo S, Henri A, Beuzard Y, Soares MP (2011) Sickle hemoglobin confers tolerance to Plasmodium infection. Cell 145:398–409PubMedGoogle Scholar
  48. Ferris MT, Aylor DL, Bottomly D, Whitmore AC, Aicher LD, Bell TA, Bradel-Tretheway B, Bryan JT, Buus RJ, Gralinski LE, Haagmans BL, McMillan L, Miller DR, Rosenzweig E, Valdar W, Wang J, Churchill GA, Threadgill DW, McWeeney SK, Katze MG, de Villena FPM, Baric RS, Heise MT (2013) Modeling host genetic regulation of influenza pathogenesis in the collaborative cross. PLoS Pathog 9:e1003196PubMedPubMedCentralGoogle Scholar
  49. Foote SJ, Burt RA, Baldwin TM, Presente A, Roberts AW, Laural YL, Lew AM, Marshall VM (1997) Mouse loci for malaria-induced mortality and the control of parasitaemia. Nat Genet 17:380–381PubMedGoogle Scholar
  50. Fortin A, Belouchi A, Tam MF, Cardon L, Skamene E, Stevenson MM, Gros P (1997) Genetic control of blood parasitaemia in mouse malaria maps to chromosome 8. Nat Genet 17:382–383PubMedGoogle Scholar
  51. Fortin A, Cardon LR, Tam M, Skamene E, Stevenson MM, Gros P (2001a) Identification of a new malaria susceptibility locus (Char4) in recombinant congenic strains of mice. Proc Natl Acad Sci USA 98:10793–10798PubMedGoogle Scholar
  52. Fortin A, Diez E, Rochefort D, Laroche L, Malo D, Rouleau GA, Gros P, Skamene E (2001b) Recombinant congenic strains derived from A/J and C57BL/6J: a tool for genetic dissection of complex traits. Genomics 74:21–35PubMedGoogle Scholar
  53. Franke-Fayard B, Janse CJ, Cunha-Rodrigues M, Ramesar J, Buscher P, Que I, Lowik C, Voshol PJ, den Boer MA, van Duinen SG, Febbraio M, Mota MM, Waters AP (2005) Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc Natl Acad Sci USA 102:11468–11473PubMedGoogle Scholar
  54. Friedman M (1978) Erythrocytic mechanism of sickle cell resistance to malaria. Proc Natl Acad Sci USA 75:1994–1997Google Scholar
  55. Gallagher PG (2005) Hematologically important mutations: ankyrin variants in hereditary spherocytosis. Blood Cells Mol Dis 35:345–347PubMedGoogle Scholar
  56. Goheen MM, Wegmuller R, Bah A, Darboe B, Danso E, Affara M, Gardner D, Patel JC, Prentice AM, Cerami C (2016) Anemia offers stronger protection than sickle cell trait against the erythrocytic stage of falciparum malaria and this protection is reversed by iron supplementation. EBioMedicine 14:123–130PubMedPubMedCentralGoogle Scholar
  57. Goncalves LA, Almeida P, Mota MM, Penha-Goncalves C (2008) Malaria liver stage susceptibility locus identified on mouse chromosome 17 by congenic mapping. PLoS ONE 3:e1874PubMedPubMedCentralGoogle Scholar
  58. Goncalves LA, Rodrigues-Duarte L, Rodo J, Vieira de Moraes L, Marques I, Penha-Goncalves C (2013) TREM2 governs Kupffer cell activation and explains belr1 genetic resistance to malaria liver stage infection. Proc Natl Acad Sci USA 110:19531–19536PubMedGoogle Scholar
  59. Greth A, Lampkin S, Mayura-Guru P, Rodda F, Drysdale K, Roberts-Thomson M, McMorran BJ, Foote SJ, Burgio G (2012) A novel ENU-mutation in ankyrin-1 disrupts malaria parasite maturation in red blood cells of mice. PLoS ONE 7:e38999PubMedPubMedCentralGoogle Scholar
  60. Gundry MC, Brunetti L, Lin A, Mayle AE, Kitano A, Wagner D, Hsu JI, Hoegenauer KA, Rooney CM, Goodell MA, Nakada D (2016) Highly efficient genome editing of murine and human hematopoietic progenitor cells by CRISPR/Cas9. Cell Rep 17:1453–1461PubMedPubMedCentralGoogle Scholar
  61. Gwamaka M, Kurtis JD, Sorensen BE, Holte S, Morrison R, Mutabingwa TK (2012) Iron deficiency protects against severe Plasmodium falciparum malaria and death in young children. Clin Infect Dis. PubMedPubMedCentralGoogle Scholar
  62. Hammond A, Galizi R, Kyrou K, Simoni A, Siniscalchi C, Katsanos D, Gribble M, Baker D, Marois E, Russell S, Burt A, Windbichler N, Crisanti A, Nolan T (2016) A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat Biotechnol 34:78–83PubMedGoogle Scholar
  63. Herbas MS, Okazaki M, Terao E, Xuan X, Arai H, Suzuki H (2010a) Alpha-tocopherol transfer protein inhibition is effective in the prevention of cerebral malaria in mice. Am J Clin Nutr 91:200–207PubMedGoogle Scholar
  64. Herbas MS, Ueta YY, Ichikawa C, Chiba M, Ishibashi K, Shichiri M, Fukumoto S, Yokoyama N, Takeya M, Xuan X, Arai H, Suzuki H (2010b) Alpha-tocopherol transfer protein disruption confers resistance to malarial infection in mice. Malar J 9:101PubMedPubMedCentralGoogle Scholar
  65. Herbas MS, Shichiri M, Ishida N, Kume A, Hagihara Y, Yoshida Y, Suzuki H (2015) Probucol-induced alpha-tocopherol deficiency protects mice against malaria infection. PLoS ONE 10:e0136014PubMedPubMedCentralGoogle Scholar
  66. Hernandez-Valladares M, Naessens J, Gibson JP, Musoke AJ, Nagda S, Rihet P, Ole-MoiYoi OK, Iraqi FA (2004a) Confirmation and dissection of QTL controlling resistance to malaria in mice. Mamm Genome 15:390–398PubMedGoogle Scholar
  67. Hernandez-Valladares M, Rihet P, Ole-MoiYoi OK, Iraqi FA (2004b) Mapping of a new quantitative trait locus for resistance to malaria in mice by a comparative mapping approach with human chromosome 5q31-q33. Immunogenetics 56:115–117PubMedGoogle Scholar
  68. Hood AT, Fabry ME, Costantini F, Nagel RL, Shear HL (1996) Protection from lethal malaria in transgenic mice expressing sickle hemoglobin. Blood 87:1600–1603PubMedGoogle Scholar
  69. Hortle E, Nijagal B, Bauer DC, Jensen LM, Ahn SB, Cockburn IA, Lampkin S, Tull D, McConville MJ, McMorran BJ, Foote SJ, Burgio G (2016) Adenosine monophosphate deaminase 3 activation shortens erythrocyte half-life and provides malaria resistance in mice. Blood. PubMedPubMedCentralGoogle Scholar
  70. Huang HM, Bauer DC, Lelliott PM, Greth A, McMorran BJ, Foote SJ, Burgio G (2016) A novel ENU-induced ankyrin-1 mutation impairs parasite invasion and increases erythrocyte clearance during malaria infection in mice. Sci Rep 6:37197PubMedPubMedCentralGoogle Scholar
  71. Huang HM, Bauer DC, Lelliott PM, Dixon MWA, Tilley L, McMorran BJ, Foote SJ, Burgio G (2017) Ankyrin-1 gene exhibits allelic heterogeneity in conferring protection against malaria. G3 7:3133–3144PubMedGoogle Scholar
  72. Ibrahim HA, Fouda MI, Yahya RS, Abousamra NK, Abd Elazim RA (2014) Erythrocyte phosphatidylserine exposure in beta-thalassemia. Lab Hematol 20:9–14PubMedGoogle Scholar
  73. Iyer J, Gruner AC, Renia L, Snounou G, Preiser PR (2007) Invasion of host cells by malaria parasites: a tale of two protein families. Mol Microbiol 65:231–249PubMedGoogle Scholar
  74. Jarolim P, Palek J, Amato D, Hassan K, Sapak P, Nurse GT, Rubin HL, Zhai S, Sahr KE, Liu SC (1991) Deletion in erythrocyte band 3 gene in malaria-resistant Southeast Asian ovalocytosis. Proc Natl Acad Sci USA 88:11022–11026PubMedGoogle Scholar
  75. Jonker FA, Calis JC, van Hensbroek MB, Phiri K, Geskus RB, Brabin BJ, Leenstra T (2012) Iron status predicts malaria risk in Malawian preschool children. PLoS ONE 7:e42670PubMedPubMedCentralGoogle Scholar
  76. Kassa FA, Van Den Ham K, Rainone A, Fournier S, Boilard E, Olivier M (2016) Absence of apolipoprotein E protects mice from cerebral malaria. Sci Rep 6:33615PubMedPubMedCentralGoogle Scholar
  77. Ke HJ, Sigala PA, Miura K, Morrisey JM, Mather MW, Crowley JR, Henderson JP, Goldberg DE, Long CA, Vaidya AB (2014) The heme biosynthesis pathway is essential for Plasmodium falciparum development in mosquito stage but not in blood stages. J Biol Chem 289:34827–34837PubMedPubMedCentralGoogle Scholar
  78. Kume A, Anh DT, Shichiri M, Ishida N, Suzuki H (2016) Probucol dramatically enhances dihydroartemisinin effect in murine malaria. Malar J 15:472PubMedPubMedCentralGoogle Scholar
  79. LaMonte G, Philip N, Reardon J, Lacsina JR, Majoros W, Chapman L, Thornburg CD, Telen MJ, Ohler U, Nicchitta CV, Haystead T, Chi JT (2012) Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe 12:187–199PubMedPubMedCentralGoogle Scholar
  80. Laroque A, Min-Oo G, Tam M, Radovanovic I, Stevenson MM, Gros P (2012) Genetic control of susceptibility to infection with Plasmodium chabaudi chabaudi AS in inbred mouse strains. Genes Immun 13:155–163PubMedGoogle Scholar
  81. Laroque A, Min-Oo G, Tam M, Ponka P, Stevenson MM, Gros P (2017) The mouse Char10 locus regulates severity of pyruvate kinase deficiency and susceptibility to malaria. PLoS ONE 12:e0177818PubMedPubMedCentralGoogle Scholar
  82. Lelliott PM, McMorran BJ, Foote SJ, Burgio G (2015) Erythrocytic iron deficiency enhances susceptibility to Plasmodium chabaudi infection in mice carrying a missense mutation in transferrin receptor 1. Infect Immun 83:4322–4334PubMedPubMedCentralGoogle Scholar
  83. Lelliott PM, Huang HM, Dixon MW, Namvar A, Blanch AJ, Rajagopal V, Tilley L, Coban C, McMorran BJ, Foote SJ, Burgio G (2017) Erythrocyte beta can be genetically targeted to protect mice from malaria. Blood Adv 1:2624–2636PubMedPubMedCentralGoogle Scholar
  84. Lessard S, Gatof ES, Beaudoin M, Schupp PG, Sher F, Ali A, Prehar S, Kurita R, Nakamura Y, Baena E, Ledoux J, Oceandy D, Bauer DE, Lettre G (2017) An erythroid-specific ATP2B4 enhancer mediates red blood cell hydration and malaria susceptibility. J Clin Invest 127:3065–3074PubMedPubMedCentralGoogle Scholar
  85. Levander OA, Fontela R, Morris VC, Ager AL Jr. (1995) Protection against murine cerebral malaria by dietary-induced oxidative stress. J Parasitol 81:99–103PubMedGoogle Scholar
  86. Levy JE, Jin O, Fujiwara Y, Kuo F, Andrews NC (1999) Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat Genet 21:396–399PubMedGoogle Scholar
  87. Li J, Chang WL, Sun G, Chen HL, Specian RD, Berney SM, Kimpel D, Granger DN, van der Heyde HC (2003) Intercellular adhesion molecule 1 is important for the development of severe experimental malaria but is not required for leukocyte adhesion in the brain. J Invest Med 51:128–140Google Scholar
  88. Lin E, Pappenfuss T, Tan RB, Senyschyn D, Bahlo M, Speed TP, Foote SJ (2006) Mapping of the Plasmodium chabaudi resistance locus char2. Infect Immun 74:5814–5819PubMedPubMedCentralGoogle Scholar
  89. Ma S, Cahalan S, Lohia R, LaMonte G, Zeng W, Murthy S, Paytas E, Grubaugh ND, Gamini R, Berry L, Lukacs V, Whitwam T, Loud M, Su AI, Andersen KG, Winzeler EA, Honore E, Wengelnik K, Patapoutian A (2017) Common Piezo1 allele in African populations causes xerocytosis and attenuates Plasmodium infection. Cell. Google Scholar
  90. Mahnke DK, Sabina RL (2005) Calcium activates erythrocyte AMP deaminase [isoform E (AMPD3)] through a protein-protein interaction between calmodulin and the N-terminal domain of the AMPD3 polypeptide. Biochemistry 44:5551–5559PubMedGoogle Scholar
  91. Maier AG, Duraisingh MT, Reeder JC, Patel SS, Kazura JW, Zimmerman PA, Cowman AF (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9:87–92PubMedGoogle Scholar
  92. McNamara HA, Cai Y, Wagle MV, Sontani Y, Roots CM, Miosge LA, O’Connor JH, Sutton HJ, Ganusov VV, Heath WR, Bertolino P, Goodnow CG, Parish IA, Enders A, Cockburn IA (2017) Up-regulation of LFA-1 allows liver-resident memory T cells to patrol and remain in the hepatic sinusoids. Sci Immunol. PubMedPubMedCentralGoogle Scholar
  93. Medeiros MM, da Silva HB, Reis AS, Barboza R, Thompson J, Lima MR, Marinho CR, Tadokoro CE (2013) Liver accumulation of Plasmodium chabaudi-infected red blood cells and modulation of regulatory T cell and dendritic cell responses. PLoS ONE 8:e81409PubMedPubMedCentralGoogle Scholar
  94. Mian-McCarthy S, Agnandji ST, Lell B, Fernandes JF, Abossolo BP, Methogo BGNO, Kabwende AL, Adegnika AA, Mordmuller B, Issifou S, Kremsner PG, Sacarlal J, Aide P, Lanaspa M, Aponte JJ, Machevo S, Acacio S, Bulo H, Sigauque B, Macete E, Alonso P, Abdulla S, Salim N, Minja R, Mpina M, Ahmed S, Ali AM, Mtoro AT, Hamad AS, Mutani P, Tanner M, Tinto H, D’Alessandro U, Sorgho H, Valea I, Bihoun B, Guiraud I, Kabore B, Sombie O, Guiguemde RT, Ouedraogo JB, Hamel MJ, Kariuki S, Oneko M, Odero C, Otieno K, Awino N, McMorrow M, Muturi-Kioi V, Laserson KF, Slutsker L, Otieno W, Otieno L, Otsyula N, Gondi S, Otieno A, Owira V, Oguk E, Odongo G, Ben Woods J, Ogutu B, Njuguna P, Chilengi R, Akoo P, Kerubo C, Maingi C, Lang T, Olotu A, Bejon P, Marsh K, Mwanbingu G, Owusu-Agyei S, Asante KP, Osei-Kwakye K, Boahen O, Dosoo D, Asante I, Adjei G, Kwara E, Chandramohan D, Greenwood B, Lusingu J, Gesase S, Malabeja A, Abdul O, Mahende C, Liheluka E, Malle L, Lemnge M, Theander TG, Drakeley C, Ansong D, Agbenyega T, Adjei S, Boateng HO, Rettig T, Bawa J, Sylverken J, Sambian D, Sarfo A, Agyekum A, Martinson F, Hoffman I, Mvalo T, Kamthunzi P, Nkomo R, Tembo T, Tegha G, Tsidya M, Kilembe J, Chawinga C, Ballou WR, Cohen J, Guerra Y, Jongert E, Lapierre D, Leach A, Lievens M, Ofori-Anyinam O, Olivier A, Vekemans J, Carter T, Kaslow D, Leboulleux D, Loucq C, Radford A, Savarese B, Schellenberg D, Sillman M, Vansadia P, Partnership RSCT (2012) A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med 367:2284–2295Google Scholar
  95. Mikolajczak SA, Jacobs-Lorena V, MacKellar DC, Camargo N, Kappe SHI (2007) L-FABP is a critical host factor for successful malaria liver stage development. Int J Parasitol 37:483–489PubMedGoogle Scholar
  96. Milet J, Nuel G, Watier L, Courtin D, Slaoui Y, Senghor P, Migot-Nabias F, Gaye O, Garcia A (2010) Genome wide linkage study, using a 250K SNP map, of Plasmodium falciparum infection and mild malaria attack in a Senegalese population. PLoS ONE 5:e11616PubMedPubMedCentralGoogle Scholar
  97. Miller JL (2013) Iron deficiency anemia: a common and curable disease. Cold Spring Harb Perspect Med. Google Scholar
  98. Miller J, Golenser J, Spira DT, Kosower NS (1984) Plasmodium falciparum: thiol status and growth in normal and glucose-6-phosphate dehydrogenase deficient human erythrocytes. Exp Parasitol 57:239–247PubMedGoogle Scholar
  99. Min-Oo G, Fortin A, Tam MF, Nantel A, Stevenson MM, Gros P (2003) Pyruvate kinase deficiency in mice protects against malaria. Nat Genet 35:357–362PubMedGoogle Scholar
  100. Min-Oo G, Fortin A, Tam MF, Gros P, Stevenson MM (2004) Phenotypic expression of pyruvate kinase deficiency and protection against malaria in a mouse model. Genes Immun 5:168–175PubMedGoogle Scholar
  101. Min-Oo G, Fortin A, Pitari G, Tam M, Stevenson MM, Gros P (2007a) Complex genetic control of susceptibility to malaria: positional cloning of the Char9 locus. J Exp Med 204:511–524PubMedPubMedCentralGoogle Scholar
  102. Min-Oo G, Tam M, Stevenson MM, Gros P (2007b) Pyruvate kinase deficiency: correlation between enzyme activity, extent of hemolytic anemia and protection against malaria in independent mouse mutants. Blood Cells Mol Dis 39:63–69PubMedGoogle Scholar
  103. Min-Oo G, Ayi K, Bongfen SE, Tam M, Radovanovic I, Gauthier S, Santiago H, Rothfuchs AG, Roffe E, Sher A, Mullick A, Fortin A, Stevenson MM, Kain KC, Gros P (2010a) Cysteamine, the natural metabolite of pantetheinase, shows specific activity against Plasmodium. Exp Parasitol 125:315–324PubMedPubMedCentralGoogle Scholar
  104. Min-Oo G, Willemetz A, Tam M, Canonne-Hergaux F, Stevenson MM, Gros P (2010b) Mapping of Char10, a novel malaria susceptibility locus on mouse chromosome 9. Genes Immun 11:113–123PubMedGoogle Scholar
  105. Nagaraj VA, Sundaram B, Varadarajan NM, Subramani PA, Kalappa DM, Ghosh SK, Padmanaban G (2013) Malaria parasite-synthesized heme is essential in the mosquito and liver stages and complements host heme in the blood stages of infection. PLoS Pathog 9:e1003522PubMedPubMedCentralGoogle Scholar
  106. Nagel RL (1990) Innate resistance to malaria: the intraerythrocytic cycle. Blood Cells 16:321–339 (discussion 340–329)PubMedGoogle Scholar
  107. Naka I, Nishida N, Patarapotikul J, Nuchnoi P, Tokunaga K, Hananantachai H, Tsuchiya N, Ohashi J (2009) Identification of a haplotype block in the 5q31 cytokine gene cluster associated with the susceptibility to severe malaria. Malar J 8:232PubMedPubMedCentralGoogle Scholar
  108. Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM (2008) Evidence of artemisinin-resistant malaria in Western Cambodia. N Engl J Med 359:2619–2620PubMedGoogle Scholar
  109. Nosten F, van Vugt M, Price R, Luxemburger C, Thway KL, Brockman A, McGready R, Ter Kuile F, Looareesuwan S, White NJ (2000) Effects of artesunate-mefloquine combination on incidence of Plasmodium falciparum malaria and mefloquine resistance in Western Thailand: a prospective study. Lancet 356:297–302PubMedGoogle Scholar
  110. O’Meara WP, Noor A, Gatakaa H, Tsofa B, McKenzie FE, Marsh K (2009) The impact of primary health care on malaria morbidity—defining access by disease burden. Trop Med Int Health 14:29–35PubMedGoogle Scholar
  111. Ohno T, Ishih A, Kohara Y, Yonekawa H, Terada M, Nishimura M (2001) Chromosomal mapping of the host resistance locus to rodent malaria (Plasmodium yoelii) infection in mice. Immunogenetics 53:736–740PubMedGoogle Scholar
  112. Omi K, Ohashi J, Patarapotikul J, Hananantachai H, Naka I, Looareesuwan S, Tokunaga K (2003) CD36 polymorphism is associated with protection from cerebral malaria. Am J Hum Genet 72:364–374PubMedGoogle Scholar
  113. Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, Epiphanio S, Chora A, Rodrigues CD, Gregoire IP, Cunha-Rodrigues M, Portugal S, Soares MP, Mota MM (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 13:703–710PubMedGoogle Scholar
  114. Payne D (1987) Spread of chloroquine resistance in Plasmodium falciparum. Parasitol Today 3:241–246PubMedGoogle Scholar
  115. Penet MF, Abou-Hamdan M, Coltel N, Cornille E, Grau GE, de Reggi M, Gharib B (2008) Protection against cerebral malaria by the low-molecular-weight thiol pantethine. Proc Natl Acad Sci USA 105:1321–1326PubMedGoogle Scholar
  116. Peters AL, Van Noorden CJ (2009) Glucose-6-phosphate dehydrogenase deficiency and malaria: cytochemical detection of heterozygous G6PD deficiency in women. J Histochem Cytochem 57:1003–1011PubMedPubMedCentralGoogle Scholar
  117. Qin W, Dion SL, Kutny PM, Zhang Y, Cheng AW, Jillette NL, Malhotra A, Geurts AM, Chen YG, Wang H (2015) Efficient CRISPR/Cas9-mediated genome editing in mice by zygote electroporation of nuclease. Genetics 200:423–430PubMedPubMedCentralGoogle Scholar
  118. Rank G, Sutton R, Marshall V, Lundie RJ, Caddy J, Romeo T, Fernandez K, McCormack MP, Cooke BM, Foote SJ, Crabb BS, Curtis DJ, Hilton DJ, Kile BT, Jane SM (2009) Novel roles for erythroid Ankyrin-1 revealed through an ENU-induced null mouse mutant. Blood 113:3352–3362PubMedPubMedCentralGoogle Scholar
  119. Rihet P, Traore Y, Abel L, Aucan C, Traore-Leroux T, Fumoux F (1998) Malaria in humans: Plasmodium falciparum blood infection levels are linked to chromosome 5q31-q33. Am J Hum Genet 63:498–505PubMedPubMedCentralGoogle Scholar
  120. Riopel J, Tam M, Mohan K, Marino MW, Stevenson MM (2001) Granulocyte-macrophage colony-stimulating factor-deficient mice have impaired resistance to blood-stage malaria. Infect Immun 69:129–136PubMedPubMedCentralGoogle Scholar
  121. Roberts A, Pardo-Manuel de Villena F, Wang W, McMillan L, Threadgill DW (2007) The polymorphism architecture of mouse genetic resources elucidated using genome-wide resequencing data: implications for QTL discovery and systems genetics. Mamm Genome 18:473–481PubMedPubMedCentralGoogle Scholar
  122. Rodrigues CD, Hannus M, Prudencio M, Martin C, Goncalves LA, Portugal S, Epiphanio S, Akinc A, Hadwiger P, Jahn-Hofmann K, Rohl I, van Gemert GJ, Franetich JF, Luty AJ, Sauerwein R, Mazier D, Koteliansky V, Vornlocher HP, Echeverri CJ, Mota MM (2008) Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4:271–282PubMedGoogle Scholar
  123. Rommelaere S, Millet V, Rihet P, Atwell S, Helfer E, Chasson L, Beaumont C, Chimini G, Sambo Mdo R, Viallat A, Penha-Goncalves C, Galland F, Naquet P (2015) Serum pantetheinase/vanin levels regulate erythrocyte homeostasis and severity of malaria. Am J Pathol 185:3039–3052PubMedGoogle Scholar
  124. Savvides P, Shalev O, John KM, Lux SE (1993) Combined spectrin and ankyrin deficiency is common in autosomal dominant hereditary spherocytosis. Blood 82:2953–2960PubMedGoogle Scholar
  125. Scherf A, Lopez-Rubio JJ, Riviere L (2008) Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62:445–470PubMedGoogle Scholar
  126. Schulman S, Roth EF Jr., Cheng B, Rybicki AC, Sussman II, Wong M, Wang W, Ranney HM, Nagel RL, Schwartz RS (1990) Growth of Plasmodium falciparum in human erythrocytes containing abnormal membrane proteins. Proc Natl Acad Sci USA 87:7339–7343PubMedGoogle Scholar
  127. Seixas E, Gozzelino R, Chora A, Ferreira A, Silva G, Larsen R, Rebelo S, Penido C, Smith NR, Coutinho A, Soares MP (2009) Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proc Natl Acad Sci USA 106:15837–15842PubMedGoogle Scholar
  128. Serghides L, Smith TG, Patel SN, Kain KC (2003) CD36 and malaria: friends or foes? Trends Parasitol 19:461–469PubMedGoogle Scholar
  129. Shear HL, Roth EF Jr., Fabry ME, Costantini FD, Pachnis A, Hood A, Nagel RL (1993) Transgenic mice expressing human sickle hemoglobin are partially resistant to rodent malaria. Blood 81:222–226PubMedGoogle Scholar
  130. Silvie O, Rubinstein E, Franetich JF, Prenant M, Belnoue E, Renia L, Hannoun L, Eling W, Levy S, Boucheix C, Mazier D (2003) Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med 9:93–96PubMedGoogle Scholar
  131. Siu E, Ploss A (2015) Modeling malaria in humanized mice: opportunities and challenges. Ann N Y Acad Sci 1342:29–36PubMedGoogle Scholar
  132. Smith CM, Jerkovic A, Puy H, Winship I, Deybach JC, Gouya L, van Dooren G, Goodman CD, Sturm A, Manceau H, McFadden GI, David P, Mercereau-Puijalon O, Burgio G, McMorran BJ, Foote SJ (2015) Red cells from ferrochelatase-deficient erythropoietic protoporphyria patients are resistant to growth of malarial parasites. Blood 125:534–541PubMedPubMedCentralGoogle Scholar
  133. Stephens R, Culleton RL, Lamb TJ (2012) The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol 28:73–82PubMedGoogle Scholar
  134. Stevenson MM, Lyanga JJ, Skamene E (1982) Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect Immun 38:80–88PubMedPubMedCentralGoogle Scholar
  135. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, Moore KJ (2010) CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 11:155–161PubMedGoogle Scholar
  136. Tavazzi B, Di Pierro D, Amorini AM, Fazzina G, Tuttobene M, Giardina B, Lazzarino G (2000) Energy metabolism and lipid peroxidation of human erythrocytes as a function of increased oxidative stress. Eur J Biochem 267:684–689PubMedGoogle Scholar
  137. Threadgill DW, Churchill GA (2012) Ten years of the collaborative cross. G3 2:153–156PubMedGoogle Scholar
  138. Thylur RP, Wu X, Gowda NM, Punnath K, Neelgund SE, Febbraio M, Gowda DC (2017) CD36 receptor regulates malaria-induced immune responses primarily at early blood stage infection contributing to parasitemia control and resistance to mortality. J Biol Chem 292:9394–9408PubMedPubMedCentralGoogle Scholar
  139. Timmann C, Thye T, Vens M, Evans J, May J, Ehmen C, Sievertsen J, Muntau B, Ruge G, Loag W, Ansong D, Antwi S, Asafo-Adjei E, Nguah SB, Kwakye KO, Akoto AO, Sylverken J, Brendel M, Schuldt K, Loley C, Franke A, Meyer CG, Agbenyega T, Ziegler A, Horstmann RD (2012) Genome-wide association study indicates two novel resistance loci for severe malaria. Nature 489:443–446PubMedGoogle Scholar
  140. Torre S, Faucher SP, Fodil N, Bongfen SE, Berghout J, Schwartzentruber JA, Majewski J, Lathrop M, Cooper AM, Vidal SM, Gros P (2015) THEMIS is required for pathogenesis of cerebral malaria and protection against pulmonary tuberculosis. Infect Immun 83:759–768PubMedPubMedCentralGoogle Scholar
  141. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B et al (1994) An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol 145:1057–1069PubMedPubMedCentralGoogle Scholar
  142. Van Eck M, Hoekstra M, Hildebrand RB, Yaong Y, Stengel D, Kruijt JK, Sattler W, Tietge UJ, Ninio E, Van Berkel TJ, Pratico D (2007) Increased oxidative stress in scavenger receptor BI knockout mice with dysfunctional HDL. Arterioscler Thromb Vasc Biol 27:2413–2419PubMedGoogle Scholar
  143. van Bruggen R, Gualtieri C, Iliescu A, Louicharoen Cheepsunthorn C, Mungkalasut P, Trape JF, Modiano D, Sirima BS, Singhasivanon P, Lathrop M, Sakuntabhai A, Bureau JF, Gros P (2015) Modulation of malaria phenotypes by pyruvate kinase (PKLR) variants in a Thai population. PLoS ONE 10:e0144555PubMedPubMedCentralGoogle Scholar
  144. Vercauteren K, Leroux-Roels G, Meuleman P (2012) Blocking HCV entry as potential antiviral therapy. Future Virol 7:547–561Google Scholar
  145. Vered K, Durrant C, Mott R, Iraqi FA (2014) Susceptibility to klebsiella pneumonaie infection in collaborative cross mice is a complex trait controlled by at least three loci acting at different time points. BMC Genom 15:865Google Scholar
  146. Weiss WR (1990) Host-parasite interactions and immunity to irradiated sporozoites. Immunol Lett 25:39–42PubMedGoogle Scholar
  147. Wellems TE, Plowe CV (2001) Chloroquine-resistant malaria. J Infect Dis 184:770–776PubMedGoogle Scholar
  148. Wykes MN, Good MF (2009) What have we learnt from mouse models for the study of malaria? Eur J Immunol 39:2004–2007PubMedGoogle Scholar
  149. Yadav K, Dhiman S, Rabha B, Saikia P, Veer V (2014) Socio-economic determinants for malaria transmission risk in an endemic primary health centre in Assam, India. Infect Dis Poverty 3:19PubMedPubMedCentralGoogle Scholar
  150. Yalaoui S, Huby T, Franetich JF, Gego A, Rametti A, Moreau M, Collet X, Siau A, van Gemert GJ, Sauerwein RW, Luty AJF, Vaillant JC, Hannoun L, Chapman J, Mazier D, Froissard P (2008) Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe 4:283–292PubMedGoogle Scholar
  151. Yang H, Wang H, Jaenisch R (2014) Generating genetically modified mice using CRISPR/Cas-mediated genome engineering. Nat Protoc 9:1956–1968PubMedGoogle Scholar
  152. Yawata Y, Kanzaki A, Yawata A, Doerfler W, Ozcan R, Eber SW (2000) Characteristic features of the genotype and phenotype of hereditary spherocytosis in the Japanese population. Int J Hematol 71:118–135PubMedGoogle Scholar
  153. Yiangou L, Montandon R, Modrzynska K, Rosen B, Bushell W, Hale C, Billker O, Rayner JC, Pance A (2016) A stem cell strategy identifies glycophorin C as a major erythrocyte receptor for the rodent malaria parasite Plasmodium berghei. PLoS ONE 11:e0158238PubMedPubMedCentralGoogle Scholar
  154. Zarychanski R, Schulz VP, Houston BL, Maksimova Y, Houston DS, Smith B, Rinehart J, Gallagher PG (2012) Mutations in the mechanotransduction protein PIEZO1 are associated with hereditary xerocytosis. Blood 120:1908–1915PubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Immunology and Infectious Disease, John Curtin School of Medical ResearchAustralian National UniversityCanberraAustralia

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