Selection and refinement: 0The malaria parasite's infection and exploitation of host hepatocytes

Current Opinion in Microbiology

Volumn 26, Issue , 2015, Pages 71-78

  Kaushansky, Alexis ^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

HEPATITIS; HOST CELL; HOST PARASITE INTERACTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIFE CYCLE; LIVER CELL; MALARIA; NONHUMAN; REVIEW; SPOROZOITE; ANIMAL; BIOLOGICAL MODEL; DISEASE MODEL; HOST PATHOGEN INTERACTION; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM; PROCEDURES;

PLASMODIUM PARASITES;

ANIMALS; DISEASE MODELS, ANIMAL; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; PARASITOLOGY; PLASMODIUM;

EID: 84934942847     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2015.05.013     Document Type: Review

References (70)

1. Kappe S.H., Vaughan A.M., Boddey J.A., Cowman A.F. That was then but this is now: malaria research in the time of an eradication agenda. Science 2010, 328:862-866.
2. Tavares J., Formaglio P., Thiberge S., Mordelet E., Van Rooijen N., Medvinsky A., Menard R., Amino R. Role of host cell traversal by the malaria sporozoite during liver infection. J Exp Med 2013, 210:905-915.
3. Baer K., Roosevelt M., Clarkson A.B., van Rooijen N., Schnieder T., Frevert U. Kupffer cells are obligatory for Plasmodium yoelii sporozoite infection of the liver. Cell Microbiol 2007, 9:397-412.
4. Lindner S.E., Swearingen K.E., Harupa A., Vaughan A.M., Sinnis P., Moritz R.L., Kappe S.H. Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol Cell Proteomics 2013, 12:1127-1143.
5. Cochrane A.H., Aikawa M., Jeng M., Nussenzweig R.S. Antibody-induced ultrastructural changes of malarial sporozoites. J Immunol 1976, 116:859-867.
6. Mota M.M., Pradel G., Vanderberg J.P., Hafalla J.C., Frevert U., Nussenzweig R.S., Nussenzweig V., Rodriguez A. Migration of Plasmodium sporozoites through cells before infection. Science 2001, 291:141-144.
7. Arias I.M., Harvey J.A., Boyer J.L., Cohen D.E., Fausto N., Shafritz D.A., Wolkoff A.W. The Liver Biology and Pathobiology 2009, Wiley-Blackwell. edn 5.
8. Crispe I.N. The liver as a lymphoid organ. Annu Rev Immunol 2009, 27:147-163.
9. Mehal W.Z., Juedes A.E., Crispe I.N. Selective retention of activated CD8+ T cells by the normal liver. J Immunol 1999, 163:3202-3210.
10. Liehl P., Zuzarte-Luis 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.
11. Miller J.L., Sack B.K., Baldwin M., Vaughan A.M., Kappe S.H. Interferon-mediated innate immune responses against malaria parasite liver stages. Cell Rep 2014, 7:436-447.
12. Liehl P., Meireles P., Albuquerque I.S., Pinkevych M., Baptista F., Mota M.M., Davenport M.P., Prudencio M. Innate immunity induced by Plasmodium liver infection inhibits malaria reinfections, 83. Infect Immun 2015, 83:1172-1180.
13. Shortt H.E., Garnham P.C. Pre-erythrocytic stage in mammalian malaria parasites. Nature 1948, 161:126.
14. Gueirard P., Tavares J., Thiberge S., Bernex F., Ishino T., Milon G., Franke-Fayard B., Janse C.J., Menard R., Amino R. Development of the malaria parasite in the skin of the mammalian host. Proc Natl Acad Sci U S A 2010, 107:18640-18645.
15. 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.
16. Vaughan A.M., Aly A.S., Kappe S.H. Malaria parasite pre-erythrocytic stage infection: gliding and hiding. Cell Host Microbe 2008, 4:209-218.
17. Coppi A., Natarajan R., Pradel G., Bennett B.L., James E.R., Roggero M.A., Corradin G., Persson C., Tewari R., Sinnis P. The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito to mammalian host. J Exp Med 2011, 208:341-356.
18. Coppi A., Pinzon-Ortiz C., Hutter C., Sinnis P. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 2005, 201:27-33.
19. Matuschewski K., Nunes A.C., Nussenzweig V., Menard R. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J 2002, 21:1597-1606.
20. Hemler M.E. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 2003, 19:397-422.
21. Silvie O., Rubinstein E., Franetich J.F., Prenant M., Belnoue E., Renia L., Hannoun L., Eling W., Levy S., Boucheix C., et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med 2003, 9:93-96.
22. Valacchi G., Sticozzi C., Lim Y., Pecorelli A. Scavenger receptor class B type I: a multifunctional receptor. Ann N Y Acad Sci 2011, 1229:E1-E7.
23. Yalaoui S., Huby T., Franetich J.F., Gego A., Rametti A., Moreau M., Collet X., Siau A., van Gemert G.J., Sauerwein R.W., et al. Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe 2008, 4:283-292.
24. Rodrigues C.D., Hannus M., Prudencio M., Martin C., Goncalves L.A., Portugal S., Epiphanio S., Akinc A., Hadwiger P., Jahn-Hofmann K., et al. Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 2008, 4:271-282.
25. Foquet L., Hermsen C.C., Verhoye L., van Gemert G.J., Cortese R., Nicosia A., Sauerwein R.W., Leroux-Roels G., Meuleman P. Anti-CD81 but not anti-SR-BI blocks Plasmodium falciparum liver infection in a humanized mouse model. J Antimicrob Chemother 2015, 70:1784-1787.
26. Ploss A., Evans M.J., Gaysinskaya V.A., Panis M., You H., de Jong Y.P., Rice C.M. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009, 457:882-886.
27. Pileri P., Uematsu Y., Campagnoli S., Galli G., Falugi F., Petracca R., Weiner A.J., Houghton M., Rosa D., Grandi G., et al. Binding of hepatitis C virus to CD81. Science 1998, 282:938-941.
28. Lupberger J., Zeisel M.B., Xiao F., Thumann C., Fofana I., Zona L., Davis C., Mee C.J., Turek M., Gorke S., et al. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 2011, 17:589-595.
29. Yalaoui S., Zougbede S., Charrin S., Silvie O., Arduise C., Farhati K., Boucheix C., Mazier D., Rubinstein E., Froissard P. Hepatocyte permissiveness to Plasmodium infection is conveyed by a short and structurally conserved region of the CD81 large extracellular domain. PLoS Pathog 2008, 4:e1000010.
30. Carrolo M., Giordano S., Cabrita-Santos L., Corso S., Vigario A.M., Silva S., Leiriao P., Carapau D., Armas-Portela R., Comoglio P.M., et al. Hepatocyte growth factor and its receptor are required for malaria infection. Nat Med 2003, 9:1363-1369.
31. Kaushansky A., Kappe S.H. The crucial role of hepatocyte growth factor receptor during liver-stage infection is not conserved among Plasmodium species. Nat Med 2011, 17:1180-1181. author reply 1181.
32. Robson K.J., Hall J.R., Jennings M.W., Harris T.J., Marsh K., Newbold C.I., Tate V.E., Weatherall D.J. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 1988, 335:79-82.
33. Pihlajamaa T., Kajander T., Knuuti J., Horkka K., Sharma A., Permi P. Structure of Plasmodium falciparum TRAP (thrombospondin-related anonymous protein) A domain highlights distinct features in apicomplexan von Willebrand factor A homologues. Biochem J 2013, 450:469-476.
34. van Dijk M.R., Douradinha B., Franke-Fayard B., Heussler V., van Dooren M.W., van Schaijk B., van Gemert G.J., Sauerwein R.W., Mota M.M., Waters A.P., et al. Genetically attenuated. P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci U S A 2005, 102:12194-12199.
35. Labaied M., Harupa A., Dumpit R.F., Coppens I., Mikolajczak S.A., Kappe S.H. Plasmodium yoelii sporozoites with simultaneous deletion of P52 and P36 are completely attenuated and confer sterile immunity against infection. Infect Immun 2007, 75:3758-3768.
36. Arredondo S.A., Cai M., Takayama Y., MacDonald N.J., Anderson D.E., Aravind L., Clore G.M., Miller L.H. Structure of the Plasmodium 6-cysteine s48/45 domain. Proc Natl Acad Sci U S A 2012, 109:6692-6697.
37. Wright G.J., Rayner J.C. Plasmodium falciparum erythrocyte invasion: combining function with immune evasion. PLoS Pathog 2014, 10:e1003943.
38. Walker D.M., Oghumu S., Gupta G., McGwire B.S., Drew M.E., Satoskar A.R. Mechanisms of cellular invasion by intracellular parasites. Cell Mol Life Sci 2014, 71:1245-1263.
39. Bano N., Romano J.D., Jayabalasingham B., Coppens I. Cellular interactions of Plasmodium liver stage with its host mammalian cell. Int J Parasitol 2007, 37:1329-1341.
40. Kaushansky A., Metzger P.G., Douglass A.N., Mikolajczak S.A., Lakshmanan V., Kain H.S., Kappe S.H. Malaria parasite liver stages render host hepatocytes susceptible to mitochondria-initiated apoptosis. Cell Death Dis 2013, 4:e762.
41. van de Sand C., Horstmann S., Schmidt A., Sturm A., Bolte S., Krueger A., Lutgehetmann M., Pollok J.M., Libert C., Heussler V.T. The liver stage of Plasmodium berghei inhibits host cell apoptosis. Mol Microbiol 2005, 58:731-742.
42. Deschermeier C., Hecht L.S., Bach F., Rutzel K., Stanway R.R., Nagel A., Seeber F., Heussler V.T. Mitochondrial lipoic acid scavenging is essential for Plasmodium berghei liver stage development. Cell Microbiol 2012, 14:416-430.
43. Albuquerque S.S., Carret C., Grosso A.R., Tarun A.S., Peng X., Kappe S.H., Prudencio M., Mota M.M. Host cell transcriptional profiling during malaria liver stage infection reveals a coordinated and sequential set of biological events. BMC Genomics 2009, 10:270.
44. Kaushansky A., Ye A.S., Austin L.S., Mikolajczak S.A., Vaughan A.M., Camargo N., Metzger P.G., Douglass A.N., MacBeath G., Kappe S.H. Suppression of host p53 is critical for Plasmodium liver-stage infection. Cell Rep 2013, 3:630-637.
45. Douglass A.N., Kain H.S., Abdullahi M., Arang N., Austin L.S., Mikolajczak S.A., Billman Z.P., Hume J.C., Murphy S.C., Kappe S.H., et al. Host-based prophylaxis successfully targets liver stage malaria parasites. Mol Ther 2015, 23:857-865.
46. Ng S., March S., Galstian A., Hanson K., Carvalho T., Mota M.M., Bhatia S.N. Hypoxia promotes liver-stage malaria infection in primary human hepatocytes in vitro. Dis Model Mech 2014, 7:215-224.
47. Pflaum J., Schlosser S., Muller M. p53 family and cellular stress responses in cancer. Front Oncol 2014, 4:285.
48. Mikolajczak S.A., Jacobs-Lorena V., MacKellar D.C., Camargo N., Kappe S.H. L-FABP is a critical host factor for successful malaria liver stage development. Int J Parasitol 2007, 37:483-489.
49. Favretto F., Assfalg M., Molinari H., D'Onofrio M. Evidence from NMR interaction studies challenges the hypothesis of direct lipid transfer from L-FABP to malaria sporozoite protein UIS3. Protein Sci 2013, 22:133-138.
50. Itoe M.A., Sampaio J.L., Cabal G.G., Real E., Zuzarte-Luis V., March S., Bhatia S.N., Frischknecht F., Thiele C., Shevchenko A., et al. Host cell phosphatidylcholine is a key mediator of malaria parasite survival during liver stage infection. Cell Host Microbe 2014, 16:778-786.
51. Thieleke-Matos C., da Silva M.L., Cabrita-Santos L., Pires C.F., Ramalho J.S., Ikonomov O., Seixas E., Shisheva A., Seabra M.C., Barral D.C. Host PI(3,5)P2 activity is required for Plasmodium berghei growth during liver stage infection. Traffic 2014, 15:1066-1082.
52. Lopes da Silva M., Thieleke-Matos C., Cabrita-Santos L., Ramalho J.S., Wavre-Shapton S.T., Futter C.E., Barral D.C., Seabra M.C. The host endocytic pathway is essential for Plasmodium berghei late liver stage development. Traffic 2012, 13:1351-1363.
53. Grutzke J., Rindte K., Goosmann C., Silvie O., Rauch C., Heuer D., Lehmann M.J., Mueller A.K., Brinkmann V., Matuschewski K., et al. The spatiotemporal dynamics and membranous features of the Plasmodium liver stage tubovesicular network. Traffic 2014, 15:362-382.
54. Trager W., Rudzinska M.A., Bradbury P.C. The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man. Bull World Health Organ 1966, 35:883-885.
55. Maurer G. Die malaria perniciosa. Zentralbl Bakteriol Parasitenkunde 1902, 23:695-719.
56. Akinyi S., Hanssen E., Meyer E.V., Jiang J., Korir C.C., Singh B., Lapp S., Barnwell J.W., Tilley L., Galinski M.R. A 95 kDa protein of Plasmodium vivax and P. cynomolgi visualized by three-dimensional tomography in the caveola-vesicle complexes (Schuffner's dots) of infected erythrocytes is a member of the PHIST family. Mol Microbiol 2012, 84:816-831.
57. Schüffner W. Beitrag zur Kenntniss der Malaria. Deutsch Archiv Klin Med 1899, 64:428-449.
58. Kulzer S., Rug M., Brinkmann K., Cannon P., Cowman A., Lingelbach K., Blatch G.L., Maier A.G., Przyborski J.M. Parasite-encoded Hsp40 proteins define novel mobile structures in the cytosol of the P. falciparum-infected erythrocyte. Cell Microbiol 2010, 12:1398-1420.
59. Tamez P.A., Bhattacharjee S., van Ooij C., Hiller N.L., Llinas M., Balu B., Adams J.H., Haldar K. An erythrocyte vesicle protein exported by the malaria parasite promotes tubovesicular lipid import from the host cell surface. PLoS Pathog 2008, 4:e1000118.
60. Smith J.D. The role of PfEMP1 adhesion domain classification in Plasmodium falciparum pathogenesis research. Mol Biochem Parasitol 2014, 195:82-87.
61. Vaughan A.M., Mikolajczak S.A., Wilson E.M., Grompe M., Kaushansky A., Camargo N., Bial J., Ploss A., Kappe S.H. Complete Plasmodium falciparum liver-stage development in liver-chimeric mice. J Clin Invest 2012, 122:3618-3628.
62. Morosan S., Hez-Deroubaix S., Lunel F., Renia L., Giannini C., Van Rooijen N., Battaglia S., Blanc C., Eling W., Sauerwein R., et al. Liver-stage development of Plasmodium falciparum, in a humanized mouse model. J Infect Dis 2006, 193:996-1004.
63. Sacci J.B., Schriefer M.E., Resau J.H., Wirtz R.A., Detolla L.J., Markham R.B., Azad A.F. Mouse model for exoerythrocytic stages of Plasmodium falciparum malaria parasite. Proc Natl Acad Sci U S A 1992, 89:3701-3705.
64. March S., Ng S., Velmurugan S., Galstian A., Shan J., Logan D.J., Carpenter A.E., Thomas D., Sim B.K., Mota M.M., et al. A microscale human liver platform that supports the hepatic stages of Plasmodium falciparum and vivax. Cell Host Microbe 2013, 14:104-115.
65. Ng S., Schwartz R.E., March S., Galstian A., Gural N., Shan J., Prabhu M., Mota M.M., Bhatia S.N. Human iPSC-derived hepatocyte-like cells support Plasmodium liver-stage infection in vitro. Stem Cell Rep 2015, 4:348-359.
66. Shanks G.D., White N.J. The activation of vivax malaria hypnozoites by infectious diseases. Lancet Infect Dis 2013, 13:900-906.
67. Riehle K.J., Dan Y.Y., Campbell J.S., Fausto N. New concepts in liver regeneration. J Gastroenterol Hepatol 2011, 26(Suppl. 1):203-212.
68. Mikolajczak S.A., Vaughan A.M., Kangwanrangsan N., Roobsoong W., Fishbaugher M., Yimamnuaychok N., Rezakhani N., Lakshmanan V., Singh N., Kaushansky A., et al. Plasmodium vivax liver stage development and hypnozoite persistence in human liver-chimeric mice. Cell Host Microbe 2015, 17:526-535.
69. Austin L.S., Kaushansky A., Kappe S.H. Susceptibility to Plasmodium liver stage infection is altered by hepatocyte polyploidy. Cell Microbiol 2014, 16:784-795.
70. Kaushansky A., Austin L.S., Mikolajczak S.A., Lo F.Y., Miller J.L., Douglass A.N., Arang N., Vaughan A.M., Gardner M.J., Kappe S.H. Susceptibility to Plasmodium yoelii preerythrocytic infection in BALB/c substrains is determined at the point of hepatocyte invasion. Infect Immun 2015, 83:39-47.