Plasmodium salvages cholesterol internalized by LDL and synthesized de novo in the liver

Cellular Microbiology

Volumn 13, Issue 4, 2011, Pages 569-586

  Labaied, Mehdi ^a,c   Jayabalasingham, Bamini ^a,d   Bano, Nazneen ^a   Cha, Sung Jae ^a   Sandoval, Juan ^a   Guan, Guimin ^b   Coppens, Isabelle ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c Seattle BioMed   (United States)

^d Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CHOLESTEROL; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; SQUALENE SYNTHASE; STEROL;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; INTERNALIZATION; LIPOPROTEIN BLOOD LEVEL; LIVER CELL; MEROZOITE; MOUSE; NONHUMAN; PARASITE DEVELOPMENT; PLASMODIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTOZOAL INFECTION; SURVIVAL;

ANIMALS; CELL LINE; CHOLESTEROL; CULICIDAE; FARNESYL-DIPHOSPHATE FARNESYLTRANSFERASE; FEMALE; HEPATOCYTES; HUMANS; LIPOPROTEINS, LDL; LIVER; MEROZOITES; MICE; MICE, INBRED C57BL; PLASMODIUM; RECEPTORS, LDL; RNA INTERFERENCE; STEROLS;

ANIMALIA;

EID: 79952650952     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01555.x     Document Type: Article

References (67)

1. Albuquerque, S.S., Carret, C., Grosso, A.R., Tarun, A.S., Peng, X., Kappe, S.H., etal. (2009) Host cell transcriptional profiling during malaria liver stage infection reveals a coordinated and sequential set of biological events. BMC Genomics 10: 270-283.
2. Atella, G.C., Silva-Neto, M.A., Golodne, D.M., Arefin, S., and Shahabuddin, M. (2006) Anopheles gambiae lipophorin: characterization and role in lipid transport to developing oocyte. Insect Biochem Mol Biol 36: 375-386.
3. Atella, G.C., Bittencourt-Cunha, P.R., Nunes, R.D., Shahabuddin, M., and Silva-Neto, M.A. (2009) The major insect lipoprotein is a lipid source to mosquito stages of malaria parasite. Acta Trop 109: 159-162.
4. Bano, N., Romano, J.D., Jayabalasingham, B., and Coppens, I. (2007) Cellular interactions of Plasmodium liver stage with its host mammalian cell. Int J Parasitol 37: 1329-1341.
5. Bergstrom, J.D., Dufresne, C., Bills, G.F., Nallin-Omstead, M., and Byrne, K. (1995) Discovery, biosynthesis, and mechanism of action of the zaragozic acids: potent inhibitors of squalene synthase. Annu Rev Microbiol 49: 607-639.
6. Butler, J.D., Blanchette-Mackie, J., Goldin, E., O'Neill, R.R., Carstea, G., Roff, C.F., etal. (1992) Progesterone blocks cholesterol translocation from lysosomes. J Biol Chem 267: 23797-23805.
7. Carabeo, R.A., Mead, D.J., and Hackstadt, T. (2003) Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci USA 100: 6771-6776.
8. Cascio, M. (2005) Connexins and their environment: effects of lipids composition on ion channels. Biochim Biophys Acta 1711: 142-153.
9. Catron, D.M., Lange, Y., Borensztajn, J., Sylvester, M.D., Jones, B.D., and Haldar, K. (2004) Salmonella enterica serovar Typhimurium requires nonsterol precursors of the cholesterol biosynthetic pathway for intracellular proliferation. Infect Immun 72: 1036-1042.
10. Charneau, S., Bastos, I.M., Mouray, E., Ribeiro, B.M., Santana, J.M., Grellier, P., and Florent, I. (2007) Characterization of PfDYN2, a dynamin-like protein of Plasmodium falciparum expressed in schizonts. Microbes Infect 9: 797-805.
11. Coppens, I., Levade, T., and Courtoy, P.J. (1995) Host plasma low density lipoprotein particles as an essential source of lipids for the bloodstream forms of Trypanosoma brucei. J Biol Chem 270: 5736-5741.
12. Coppens, I., Sinai, A.P., and Joiner, K.A. (2000) Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 149: 167-180.
13. Coppens, I., Dunn, J.D., Romano, J.D., Pypaert, M., Zhang, H., Boothroyd, J.C., and Joiner, K.A. (2006) Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125: 261-274.
14. Dart, C. (2010) Lipid microdomains and the regulation of ion channel function. J Physiol 588: 3169-3178.
15. Desai, S.A., and Rosenberg, R.L. (1997) Pore size of the malaria parasite's nutrient channel. Proc Natl Acad Sci USA 94: 2045-2049.
16. Dufourc, E.J. (2008) Sterols and membrane dynamics. J Chem Biol 1: 63-77.
17. Florent, I., Charneau, S., and Grellier, P. (2004) Plasmodium falciparum genes differentially expressed during merozoite morphogenesis. Mol Biochem Parasitol 135: 143-148.
18. Franke-Fayard, B., Trueman, H., Ramesar, J., Mendoza, J., van der Keur, M., van der Linden, R., etal. (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.
19. Gilk, S.D., Beare, P.A., and Heinzen, R.A. (2010) Coxiella burnetii expresses a functional {Delta}24 sterol reductase. J Bacteriol 192: 6154-6159.
20. Goldstein, J.L., and Brown, M.S. (1990) Regulation of the mevalonate pathway. Nature 343: 425-430.
21. Goldstein, J.L., Brown, M.S., Anderson, R.G.W., Russell, D.W., and Schneider, W.J. (1985) Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu Rev Cell Biol 1: 1-39.
22. Grellier, P., Rigomier, D., and Schrével, J. (1990) In vitro induction of Plasmodium falciparum schizogony by human high density lipoproteins (HDL). C R Acad Sci III 311: 361-367.
23. Grellier, P., Rigomier, D., Clavey, V., Fruchart, J.C., and Schrevel, J. (1991) Lipid traffic between high density lipoproteins and Plasmodium falciparum-infected red blood cells. J Cell Biol 112: 267-277.
24. Haldar, K., Uyetake, L., Ghori, N., Elmendorf, H.G., and Li, W.L. (1991) The accumulation and metabolism of a fluorescent ceramide derivative in Plasmodium falciparum-infected erythrocytes. Mol Biochem Parasitol 49: 143-156.
25. Havel, R.J., Eder, H.A., and Bragdon, J.H. (1955) The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 34: 1345-1351.
26. Hiller, N.L., Akompong, T., Morrow, J.S., Holder, A.A., and Haldar, K. (2003) Identification of a stomatin orthologue in vacuoles induced in human erythrocytes by malaria parasites. A role for microbial raft proteins in apicomplexan vacuole biogenesis. J Biol Chem 278: 48413-48421.
27. Hsiao, L.L., Howard, R.J., Aikawa, M., and Taraschi, T.F. (1991) Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum. Biochem J 274: 121-132.
28. Hsuchen, C.C., and Feingold, D.S. (1973) Selective membrane toxicity of the polyene antibiotics: studies on lecithin membrane models (liposomes). Antimicrob Agents Chemother 4: 309-315.
29. Jackson, K.E., Spielmann, T., Hanssen, E., Adisa, A., Separovic, F., Dixon, M.W., etal. (2007) Selective permeabilization of the host cell membrane of Plasmodium falciparum-infected red blood cells with streptolysin O and equinatoxin II. Biochem J 403: 167-175.
30. Jayabalasingham, B., Bano, N., and Coppens, I. (2010) Metamorphosis of the malaria parasite in the liver is associated with organelle clearance. Cell Res 20: 1043-1059.
31. Kaiser, K., Camargo, N., and Kappe, S.H. (2003) Transformation of sporozoites into early exoerythrocytic malaria parasites does not require host cells. J Exp Med 197: 1045-1050.
32. Karsten, V., Qi, H., Beckers, C.J., Reddy, A., Dubremetz, J.F., Webster, P., and Joiner, K.A. (1998) The protozoan parasite Toxoplasma gondii targets proteins to dense granules and the vacuolar space using both conserved and unusual mechanisms. J Cell Biol 141: 1323-1333.
33. Keller, R.K. (1996) Squalene synthase inhibition alters metabolism of nonsterols in rat liver. Biochim Biophys Acta 1303: 169-179.
34. Klover, P.J., and Mooney, R.A. (2004) Hepatocytes: critical for glucose homeostasis. Int J Biochem Cell Biol 36: 753-758.
35. Krieger, M. (1999) Charting the fate of the 'good cholesterol': identification and characterization of the high-density lipoprotein receptor SR-BI. Annu Rev Biochem 68: 523-558.
36. Krukemyer, J.J., and Talbert, R.L. (1987) Lovastatin: a new cholesterol-lowering agent. Pharmacotherapy 7: 198-210.
37. Kumar, K.A., Oliveira, G.A., Edelman, R., Nardin, E., and Nussenzweig, V. (2004) Quantitative Plasmodium sporozoite neutralization assay (TSNA). J Immunol Methods 292: 157-164.
38. Kumar, Y., Cocchiaro, J., and Valdivia, R.H. (2006) The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr Biol 16: 1646-1651.
39. Lauer, S., VanWye, J., Harrison, T., McManus, H., Samuel, B.U., Hiller, N.L., etal. (2000) Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J 19: 3556-3564.
40. Leonard, D.A., and Chen, H.W. (1987) ATP-dependent degradation of 3-hydroxy-3-methylglutaryl coenzyme A reductase in permeabilized cells. J Biol Chem 262: 7914-7919.
41. Mikolajczak, S.A., Jacobs-Lorena, V., MacKellar, D.C., Camargo, N., and Kappe, S.H. (2007) L-FABP is a critical host factor for successful malaria liver stage development. Int J Parasitol 37: 483-489.
42. Morgan, E.H., and Baker, E. (1986) Iron uptake and metabolism by hepatocytes. Fed Proc 45: 2810-2816.
43. Mueller, A.K., Camargo, N., Kaiser, K., Andorfer, C., Frevert, U., Matuschewski, K., and Kappe, S.H. (2005) Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 102: 3022-3027.
44. Murphy, D.J., and Vance, J. (1999) Mechanisms of lipid-body formation. Trends Biochem Sci 24: 109-115.
45. Nakabayashi, H., Taketa, K., Miyano, K., Yamane, T., and Sato, J. (1982) Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858-3863.
46. Nguyen, P., Leray, V., Diez, M., Serisier, S., Le Bloc'h, J., Siliart, B., and Dumon, H. (2008) Liver lipid metabolism. J Anim Physiol Anim Nutr (Berl) 92: 272-283.
47. Nilsson-Ehle, I., and Nilsson-Ehle, P. (1990) Changes in plasma lipoproteins in acute malaria. J Intern Med 227: 151-155.
48. Olofsson, S.O., and Boren, J. (2005) Apolipoprotein B: a clinically important apolipoprotein which assembles atherogenic lipoproteins and promotes the development of atherosclerosis. J Intern Med 258: 395-410.
49. Pagler, T.A., Rhode, S., Neuhofer, A., Laggner, H., Strobl, W., Hinterndorfer, C., etal. (2006) SR-BI-mediated high density lipoprotein (HDL) endocytosis leads to HDL resecretion facilitating cholesterol efflux. J Biol Chem 281: 11193-11204.
50. Pels Rijcken, W.R., Overdijk, B., Van den Eijnden, D.H., and Ferwerda, W. (1993) Pyrimidine nucleotide metabolism in rat hepatocytes: evidence for compartmentation of nucleotide pools. Biochem J 293: 207-213.
51. Poumay, Y., and Ronveaux-Dupal, M.F. (1985) Rapid preparative isolation of concentrated low-density lipoproteins and of lipoprotein-deficient serum using vertical rotor gradient ultracentrifugation. J Lipid Res 26: 1476-1480.
52. Pradel, G., and Frevert, U. (2001) Malaria sporozoites actively enter and pass through rat Kupffer cells prior to hepatocyte invasion. Hepatology 33: 1154-1165.
53. Rodrigues, C.D., Hannus, M., Prudêncio, M., Martin, C., Gonçalves, L.A., Portugal, S., etal. (2008) Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4: 271-282.
54. Rothwell, C., Lebreton, A., Young Ng, C., Lim, J.Y., Liu, W., Vasudevan, S., etal. (2009) Cholesterol biosynthesis modulation regulates dengue viral replication. Virology 389: 8-19.
55. Shakibaei, M., and Frevert, U. (1996) Dual interaction of the malaria circumsporozoite protein with the low density lipoprotein receptor-related protein (LRP) and heparan sulfate proteoglycans. J Exp Med 184: 1699-1711.
56. Shechter, I., Klinger, E., Rucker, M.L., Engstrom, R.G., Spirito, J.A., Islam, M.A., etal. (1992) Solubilization, purification, and characterization of a truncated form of rat hepatic squalene synthetase. J Biol Chem 267: 8628-8635.
57. Silvie, O., Charrin, S., Billard, M., Franetich, J.F., Clark, K.L., van Gemert, G.J., etal. (2006) Cholesterol contributes to the organization of tetraspanin-enriched microdomains and to CD81-dependent infection by malaria sporozoites. J Cell Sci 119: 1992-2002.
58. Sinai, A.P., Webster, P., and Joiner, K.A. (1997) Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci 110: 2117-2128.
59. Singh, A.P., Buscaglia, C.A., Wang, Q., Levay, A., Nussenzweig, D.R., Walker, J.R., etal. (2007) Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 131: 492-504.
60. Sinnis, P., and Sim, B.K. (1997) Cell invasion by the vertebrate stages of Plasmodium. Trends Microbiol 5: 52-58.
61. Sinnis, P., Willnow, T.E., Briones, M.R., Herz, J., and Nussenzweig, V. (1996) Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J Exp Med 184: 945-954.
62. Sturm, A., Amino, R., van de Sand, C., Regen, T., Retzlaff, S., Rennenberg, A., etal. (2006) Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313: 1287-1290.
63. Tleyjeh, I.M., Kashour, T., Hakim, F.A., Zimmerman, V.A., Erwin, P.J., Sutton, A.J., and Ibrahim, T. (2009) Statins for the prevention and treatment of infections: a systematic review and meta-analysis. Arch Intern Med 169: 1658-1667.
64. Volpon, L., and Lancelin, J. (2000) Solution NMR structures of the polyene macrolide antibiotic filipin III. FEBS Lett 478: 137-140.
65. Wilkening, S., Stahl, F., and Bader, A. (2003) Comparison of primary human hepatocytes and hepatoma cell line Hepg2 with regard to their biotransformation properties. Drug Metab Dispos 31: 1035-1042.
66. Wilson, H.M., Griffin, B.A., Watt, C., and Skinner, E.R. (1992) The isolation and characterization of high-density-lipoprotein subfractions containing apolipoprotein E from human plasma. Biochem J 284: 477-481.
67. Yalaoui, S., Huby, T., Franetich, J.F., Gego, A., Rametti, A., Moreau, M., etal. (2008) Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe 4: 283-292.