Toxoplasma gondii exploits host low-density lipoprotein receptor- mediated endocytosis for cholesterol acquisition

Journal of Cell Biology

Volumn 149, Issue 1, 2000, Pages 167-180

  Coppens, Isabelle ^a   Sinai, Anthony P ^a,b   Joiner, Keith A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Cholesterol transport; LDL endocytic pathway; Parasitophorous vacuole; Somatic cell mutant; Toxoplasma gondii

Indexed keywords

CHOLESTEROL; LOW DENSITY LIPOPROTEIN;

ARTICLE; BIOGENESIS; CELL PROLIFERATION; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; ENDOCYTOSIS; GOLGI COMPLEX; HOST CELL; HUMAN; HUMAN CELL; LIPOGENESIS; LYSOSOME; NUCLEOTIDE SEQUENCE; PARASITE; PRIORITY JOURNAL; PROTEIN ISOLATION; TOXOPLASMA GONDII;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHOLESTEROL; CRICETINAE; CYTOSKELETON; ENDOCYTOSIS; FARNESYL-DIPHOSPHATE FARNESYLTRANSFERASE; GOLGI APPARATUS; HUMANS; HYDROXYMETHYLGLUTARYL COA REDUCTASES; LIPOPROTEINS, LDL; LYSOSOMES; MEVALONIC ACID; MODELS, BIOLOGICAL; MUTATION; RECEPTORS, LDL; REPRODUCTION; TOXOPLASMA; VACUOLES;

PROTOZOA; TOXOPLASMA GONDII;

EID: 0034599991     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.1.167     Document Type: Article

References (67)

1. Bradfute, D.L., C.J. Silva, and R.D. Simoni. 1992. Squalene synthase-deficient mutant of Chinese hamster ovary cells. J. Biol. Chem. 267:18308-18314.
2. Brown, M.S., S.E. Dana, and J.L. Goldstein. 1975. Receptor-dependent hydrolysis of cholesteryl esters contained in plasma low density lipoprotein. Proc. Natl. Acad. Sci. USA. 72:2925-2929.
3. Brown, M.S., and J.L. Goldstein. 1999. A proteolytic pathway that controls the cholesterol content of membranes, cell, and blood. Proc. Natl. Acad. Sci. USA. 96:11041-11048.
4. Butler, J.D., J. Blanchette-Mackie, E. Goldin, R.R. O'Neill, G. Carstea, C.F. Roff, M.C. Patterson, S. Patel, M.E. Comly, A. Cooney, M.T. Vanier, R.O. Brady, and P.G. Pentchev. 1992. Progesterone blocks cholesterol translocation from lysosomes. J. Biol. Chem. 267:23797-23805.
5. Coppens, I., M. Andries, J.L. Liu, and M.F. Cesbron-Delauw. 1999. Intracellular trafficking of dense granule proteins in Toxoplasma gondii and experimental evidences for a regulated exocytosis. Eur. J. Cell Biol. 78:463-472.
6. Coppens, I., T. Levade, and P.J. Courtoy. 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.
7. Craig, I.F., D.P. Via, W.W. Mantulin, H.J. Pownall, A.M. Gotto, Jr., and L.C. Smith. 1981. Low density lipoprotein reconstituted with steroids containing the nitrobenzoxadiazole fluorophore. J. Lipid Res. 22:687-696.
8. Dabl, N.K., W.G. Gutheil, and L. Liscum. 1993. Abnormal regulation of low density lipoprotein-sensitive events in a cholesterol transport mutant. J. Biol. Chem. 268:16979-16986.
9. Dahl, N.K., K.L. Reed, M.A. Daunais, J.R. Faust, and L. Liscum. 1992. Isolation and characterization of Chinese hamster ovary cells defective in the intracellular metabolism of LDL-derived cholesterol. J. Biol. Chem. 267:4889-4896.
10. de Duve, C. 1983. Lysosomes revisited. Eur. J. Biochem. 137:391-397.
11. de Duve, C., T. de Barsy, B. Poole, A. Trouet, P. Tulkens, and F. Van Hoof. 1974. Lysosomotropic agents. Biochem. Pharmacol. 23:2495-2531.
12. El-Jack, A.K., K.V. Kandror, and P.F. Pilch. 1999. The formation of an insulin-responsive vesicular cargo compartment is an early event in 3T3-L1 adipocyte differentiation. Mol. Biol. Cell. 10:1581-1594.
13. Ernst, J.D., L.-M. Ting, S. Novak, and R.V. Farese. 1999. Fifth Toxoplasmosis Conference. Marshall, CA.
14. Foussard, F., M.A. Leriche, and J.F. Dubremetz. 1991a. Characterization of the lipid content of Toxoplasma gondii rhoptries. Parasitology. 102:367-370.
15. Foussard, F., Y. Gallois, A. Girault, and J.F. Menez. 1991b. Lipids and fatty acids of tachyzoites and purified pellicles of Toxoplasma gondii. Parasitol. Res. 77:475-477.
16. Gallois, Y., F. Foussard, A. Girault, J. Hodberg, A. Tricaud, G. Mauras, and C. Motta. 1988. Membrane fluidity of Toxoplasma gondii: a fluorescence polarization study. Biol. Cell. 62:11-15.
17. Geelen, M.J.H., J.S. Papiez, K. Girgis, and D.M. Gibson. 1991. In situ measurement of HMG-CoA reductase activity in digitonin-permeabilized hepatocytes. Biochim. Biophys. Res. Commun. 180:525-530.
18. Goldstein, J.L., and M.S. Brown. 1990. Regulation of the mevalonate pathway. Nature. 343:425-430.
19. Greenspan, P., E.P. Mayer, and S.D. Fower. 1985. Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 100:965-973.
20. Hackstadt, T., D.D. Rockey, R.A. Heinzen, and M.A. Scidmore. 1996. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO (Eur. Mol. Biol. Organ.) J. 15:964-977.
21. Hackstadt, T., M.A. Scidmore, and D.D. Rockey. 1995. Lipid metabolism in Chlamydia trachomatis-infected cell: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. USA. 92: 4877-4881.
22. Havel, R.J., H.A. Eder, and J.H. Bragdon. 1955. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 34:1345-1351.
23. Joiner, K.A., S.A. Fuhrman, H. Mietinnen, L.L. Kasper, and I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor transfected fibroblasts. Science. 249:641-646.
24. Jomaa, H., J. Wiesner, S. Sanderbrand, B. Altincicek, C. Weidemeyer, M. Hintz, I. Turbachova, M. Eberl, J. Zeidler, H.K. Lichtenthaler, et al. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science. 285:1573-1576.
25. Jones, T.C., S. Yeh, and J.G. Hirsch. 1972. The interaction between Toxoplasma gondii and mammalian cells. I. Mechanism of entry and intracellular fate of the parasite. J. Exp. Med. 136:1157-1172.
26. Kalayoglu, M.V., G.S. Miranpuri, D.T. Golenbock, and G.I. Byrne. 1999. Characterisation of low-density lipoprotein uptake by murine macrophages exposed to Chlamydia pneumoniae. Microb. Infect. 1:409-418.
27. Klausner, R.D., J.G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
28. Kobayashi, T., M.H. Beuchat, M. Lindsay, S. Frias, R.D. Palmiter, H. Sakuraba, R.G. Parton, and J. Gruenberg. 1999. Late endosomes membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat. Cell Biol. 1:113-118.
29. Lange, Y., and T.L. Steck. 1996. The role of intracellular cholesterol transport in cholesterol homeostasis. Trends Cell Biol. 6:205-208.
30. Leonard, D.A., and H.W. Chen. 1987. ATP-dependent degradation of 3-hydroxy-3-methylglutaryl coenzyme A reductase in permeabilized cells. J. Biol. Chem. 262:7914-7919.
31. Lindsay, D.S., R.R. Mitscher, M.A. Toivio-Kinnucan, S.J. Upton, J.P. Dubey, and B.L. Blagburn. 1993. Association of host cell mitochondria with developing Toxoplasma gondii tissue cysts. Am. J. Vet. Res. 54:1663-1667.
32. Lingelbach, K., and K.A. Joiner. 1998. The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J. Cell Sci. 111:1467-1475.
33. Liscum, L., and J.J. Klansek. 1998. Niemann-Pick disease type C. Curr. Opin. Lipidol. 9:131-135.
34. Liscum, L., and J.R. Faust. 1989. The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-β-[2-(diethylamino)ethoxy]androst-5-en-17-one. J. Biol. Chem. 264:11796-11806.
35. Liscum, L., and N.J. Munn. 1999. Intracellular cholesterol transport. Biochim. Biophys. Acta. 1438:19-37.
36. Liscum, L., R.M. Ruggiero, and J.R. Faust. 1989. The intracellular transport of low density lipoprotein-derived cholesterol is defective in Niemann-Pick type C fibroblasts. J. Cell Biol. 108:1625-1636.
37. Luskey, K.L., J.R. Faust, D.J. Chin, M.S. Brown, and J.L. Goldstein. 1983. Amplification of the gene for 3-hydroxy-3-methylglutaryl coenzyme A reductase, but not for the 53-kDa protein, in UT-1 cells. J. Biol. Chem. 258:8462-8469.
38. McFadden, G.I., and D.S. Roos. 1999. Apicomplexan plastids as drug targets. Trends Microbiol. 7:328-333.
39. McFarlane, A.S. 1958. Efficient trace-labelling of proteins with iodine. Nature. 182:53.
40. McGookey, D.J., and G.W. Anderson. 1983. Morphological characterization of the cholesteryl ester cycle in cultured mouse macrophage foam cells. J. Cell Biol. 97:1156-1165.
41. Melo, E.J.T., T.U. Carvalho, and W. de Souza. 1992. Penetration of Toxoplasma gondii into host cells induces changes in the distribution of mitochondria and the endoplasmic reticulum. Cell Struct. Funct. 17:311-317.
42. Melo, E.J.T, and W. de Souza. 1996. Pathway of C6-NBD-ceramide on the host cell infected with Toxoplasma gondii. Cell Struct. Funct. 21:47-52.
43. Metherall, J.E., J.L. Goldstein, K.L. Luskey, and M.S. Brown. 1989. Loss of transcriptional repression of three-sterol-regulated genes in mutant hamster cells. J. Biol. Chem. 264:15634-15641.
44. Misumi, Y., Y. Misumi, K. Miki, A. Takatsuki, G. Tamura, and Y. Ikehara. 1986. Novel blockade by Brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem. 261:11398-11403.
45. Monteiro Cintra, W., and W. de Souza. 1985. Distribution of intramembranous particles and filipin-sterol complexes in the cell membranes of Toxoplasma gondii. Eur. J. Cell Biol. 37:63-69.
46. Montgomery, R.R., P. Webster, and I. Mellman. 1991. Accumulation of indigestible substances reduces fusion competence of macrophage lysosomes. J. Immunol. 147:3087-3095.
47. Mordue, D.G., S. Hakansson, I. Niesman, and L.D. Sibley. 1999. Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp. Parasitol. 92:87-99.
48. Mukherjee, S., X. Zha, I. Tabas, and F.R. Maxfield. 1998. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent analog. Biophys. J. 75:1915-1925.
49. Nakaar, V., B.U. Samuel, E.O., and K.A. Joiner. 1999. Targeted reduction of nucleoside triphosphate hydrolase by antisense RNA inhibits Toxoplasma gondii proliferation. J. Biol. Chem. 274:5083-5087.
50. Neufeld, E.B., A.M. Cooney, J. Pitha, E.A. Dawidowicz, N.K. Dwyer, P.G. Pentchev, and E.J. Blanchette-Mackie. 1996. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271:21604-21613.
51. Ohashi, M., M. Murata, and S. Ohnishi. 1992. A novel fluorescence method to monitor the lysosomal disintegration of low density lipoprotein. Eur. J. Cell Biol. 59:116-126.
52. Pentchev, P.G., H.S. Kruth, M.E. Comly, J.D. Butler, M.T. Vanier, D.A. Wenger, and S. Patel. 1986. Type C Niemann-Pick disease. A parallel loss of regulatory responses in both the uptake and esterification of low density lipoprotein-derived cholesterol in cultured fibroblasts. J. Biol. Chem. 261: 16775-16780.
53. Porchet-Hennere, E., and G. Torpier. 1983. Relations entre Toxoplasma et sa cellule-hote. Protistologica. 19:357-370.
54. Poumay, Y., and M.F. Ronveaux-Dupal. 1984. Rapid preparative isolation of concentrated low-density lipoproteins and of lipoprotein-deficient serum using vertical rotor gradient ultracentrifugation. J. Lipid Res. 26:1476-1480.
55. Roff, C.F., E. Goldin, M.E. Comly, A. Cooney, A. Brown, M.T. Vanier, S.P.F. Miller, R.O. Brady, and P.O. Pentchev. 1991. Type C Niemann-Pick disease: use of Hydrophobic amines to study defective cholesterol transport. Dev. Nenrosci. 13:315-320.
56. Roos, D.S., R.G.K. Donald, N.S. Morissette, and A.L.C. Maullon. 1994. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell. Biol 45:27-63.
57. Schwab, J.C., C.J.M. Beckers, and K.A. Joiner. 1994. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc. Natl. Acad. Sci. USA. 91:509-513.
58. Sibley, L.D., I.R. Niesman, S.F. Parmley, and M.F. Cesbron-Delauw. 1995. Regulated secretion of multilamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J. Cell. Sci. 108:1669-1677.
59. Sibley, L.D., E. Weidner, and J.L. Krahenbulh. 1985. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature. 315:416-419.
60. Silverman, J.A., M.L. Haynes, B.J. Luft, and K.A. Joiner. 1997. Characterization of anti-Toxoplasma activity of SDZ 215-918, a cyctosporin derivative lacking immunosuppressive and peptidyl-prolyl-isomerase-inhibiting activity: possible role of a P glycoprotein in Toxoplasma physiology. Antimicrob. Agents Chemother. 41:1859-1866.
61. Sinai, A.P., and K.A. Joiner. 1997. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51:415-462.
62. Sinai, A.P., P. Webster, and K.A. Joiner. 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.
63. Smith, P.K., R.I. Krohn, G.T. Hermanson, A.K. Mallia, F.H. Gartner, M.D. Provenzano, E.K. Fujimoto, N.M. Goeke, B.J. Olson, and D.C. Klenk. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:76-85.
64. Sokol, J., J. Blanchette-Mackie, H.S. Kruth, N.K. Dwyer, L.M. Amende, J.D. Butler, E. Robinson, S. Patel, R.O. Brady, M.E. Comly, et al. 1988. Type C Niemann-Pick disease. Lysosomal accumulation and defective intracellular mobilization of low density lipoprotein. J. Hiol. Chem. 263:3411-3417.
65. Speer, C.A., S. Clark, and J.P. Duney. 1998. Ultrastructure of the oocysts, sporocysts, and sporozites of Toxoplasma gondii. J. Parasitol. 84:505-512.
66. Steinman, R.M., S.E. Brodie, and Z.A. Cohn. 1976. Membrane flow during pinocytosis. J. Cell Biol. 68:665-687.
67. Torii, S., B. Tomohiro, T. Watanabes, Y. Ikehara, K. Murakami, and K. Nakayama. 1995. Cytotoxicity of Brefeldin A correlates with its inhibitory effect on membrane binding of COP coat proteins. J. Biol. Chem. 270:11574-11580.