Introduction of Caveolae Structural Proteins into the Protozoan Toxoplasma Results in the Formation of Heterologous Caveolae but Not Caveolar Endocytosis

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Lige, Bao ^a   Romano, Julia D ^a   Sampels, Vera ^a   Sonda, Sabrina ^b   Joiner, Keith A ^c   Coppens, Isabelle ^a  

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

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CAVIN 1; UNCLASSIFIED DRUG;

ARTICLE; CAVEOLA; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MORPHOGENESIS; NONHUMAN; PALMITOYLATION; PLASMID; PROTEIN EXPRESSION; PROTEIN INTERACTION; SKIN FIBROBLAST; TOXOPLASMA GONDII; WILD TYPE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAVEOLAE; CAVEOLIN 1; CELL LINE; CELL MEMBRANE; CELL NUCLEUS; CYTOPLASMIC VESICLES; ENDOCYTOSIS; GENE EXPRESSION; GOLGI APPARATUS; HUMANS; MEMBRANE PROTEINS; PROTEIN TRANSPORT; TOXOPLASMA;

MAMMALIA; METAZOA; PROTOZOA; TOXOPLASMA;

EID: 84871332427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051773     Document Type: Article

References (71)

1. Parkar NS, Akpa BS, Nitsche LC, Wedgewood LE, Place AT, et al. (2009) Vesicle formation and endocytosis: function, machinery, mechanisms, and modeling. Antioxid Redox Signal 11: 1301-1312.
2. Parton RG, Richards AA, (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4: 724-738.
3. Kirkham M, Parton RG (2005) Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta 1746, 349-363.
4. Parat MO, (2009) The biology of caveolae: Achievements and perspectives. Int Rev Cell Mol Biol 273: 117-192.
5. Sandvig K, Pust S, Skotland T, van Deurs B (2011) Clathrin-independent endocytosis: mechanisms and function. Curr Opin Cell Biol 23, 413-420.
6. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1, 31-39.
7. Parton RG, Simons K, (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8: 185-194.
8. Chidlow JH Jr, Sessa WC, (2010) Caveolae, caveolins, and cavins: complex control of cellular signalling and inflammation. Cardiovasc Res 86: 219-225.
9. Li S, Song KS, Lisanti MP, (1996a) Expression and characterization of recombinant caveolin. Purification by polyhistidine tagging and cholesterol-dependent incorporation into defined lipid membranes. J Biol Chem 271: 568-573.
10. Ikonen E, Heino S, Lusa S, (2004) Caveolins and membrane cholesterol. Biochem Soc Trans 32: 121-123.
11. Murata M, Peranen J, Schreiner R, Weiland F, Kurzchalia T, et al. (1995) VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci U S A 92: 10339-10343.
12. Li S, Okamoto T, Chun M, Sargiacomo M, Casanova JE, et al. (1995) Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 270: 15693-15701.
13. Li S, Couet J, Lisanti MP, (1996b) Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 271: 29182-29190.
14. Kirkham M, Nixon SJ, Howes MT, Abi-Rached L, Wakeham DE, et al. (2008) Evolutionary analysis and molecular dissection of caveola biogenesis. J Cell Sci 121: 2075-2086.
15. Hayer A, Stoeber M, Bissig C, Helenius A, (2010) Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 11: 361-382.
16. Parton RG, Hanzal-Bayer M, Hancock JF, (2006) Biogenesis of caveolae: a structural model for caveolin-induced domain formation. J Cell Sci 119: 787-796.
17. Liu L, Pilch PF, (2008) A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J Biol Chem 283: 4314-4322.
18. Liu P, Rudick M, Anderson RG, (2002) Multiple functions of caveolin-1. J Biol Chem 277: 41295-41298.
19. Cohen AW, Combs TP, Scherer PE, Lisanti MP, (2003) Role of caveolin and caveolae in insulin signaling and diabetes. Am J Physiol Endocrinol Metab 285: E1151-1160.
20. Kiss AL, (2012) Caveolae and the regulation of endocytosis. Adv Exp Med Biol 729: 14-28.
21. Williams TM, Lisanti MP, (2005) Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 288: C494-506.
22. Engelman JA, Zhang XL, Galbiati F, Lisanti MP, (1998) Chromosomal localization, genomic organization, and developmental expression of the murine caveolin gene family (Cav-1,-2, and-3). Cav-1 and Cav-2 genes map to a known tumor suppressor locus (6-A2/7q31). FEBS Lett 429: 330-336.
23. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, et al. (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168: 465-476.
24. Tang Z, Okamoto T, Boontrakulpoontawee P, Katada T, Otsuka AJ, et al. (1997) Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implications for the molecular evolution of mammalian caveolin genes. J Biol Chem 272: 2437-2445.
25. Spisni E, Tomasi V, Cestaro A, Tosatto SC, (2005) Structural insights into the function of human caveolin 1. Biochem Biophys Res Commun 338: 1383-1390.
26. Field MC, Gabernet-Castello C, Dacks JB (2007) Reconstructing the evolution of the endocytic system: Insights from genomic and molecular cell biology. In: Eukaryotic Membranes and Cytoskeleton: Origins and Evolution. Jekely, G. (ed.) New York: Landes Bioscience and Springer Science+Business Media, 84-96.
27. Fra AM, Williamson E, Simons K, Parton RG, (1995) De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci U S A 92: 8655-8659.
28. Hatanaka M, Maeda T, Ikemoto T, Mori H, Seya T, et al. (1998) Expression of caveolin-1 in human T cell leukemia cell lines. Biochem Biophys Res Commun 253: 382-387.
29. Verkade P, Harder T, Lafont F, Simons K, (2000) Induction of caveolae in the apical plasma membrane of Madin-Darby canine kidney cells. J Cell Biol 148: 727-739.
30. Drab M, Verkade P, Elger M, Kasper M, Lohn M, et al. (2001) Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449-2452.
31. Li S, Song KS, Koh SS, Kikuchi A, Lisanti MP, (1996c) Baculovirus-based expression of mammalian caveolin in Sf21 insect cells. A model system for the biochemical and morphological study of caveolae biogenesis. J Biol Chem 271: 28647-28654.
32. Waiser PJ, Ariotti N, Howes M, Ferguson C, Webb R, et al. (2012) Constitutive formation of caveolae in a bacterium. Cell 150: 752-763.
33. Azzouz N, Rauscher B, Gerold P, Cesbron-Delauw MF, Dubremetz JF, et al. (2002) Evidence for de novo sphingolipid biosynthesis in Toxoplasma gondii. Int J Parasitol 32: 677-684.
34. Sonda S, Sala G, Ghidoni R, Hemphill A, Pieters J, (2005) Inhibitory effect of aureobasidin A on Toxoplasma gondii. Antimicrob Agents Chemother 49: 1794-1801.
35. Lige B, Romano JD, Bandaru VV, Ehrenman K, Levitskaya, et al, (2011) Deficiency of a Niemann-Pick, type C1-related protein in Toxoplasma is associated with multiple lipidoses and increased pathogenicity. PLoS Pathog 12: e1002410.
36. Coppens I, Joiner KA, (2003) Host but not parasite cholesterol controls Toxoplasma cell entry by modulating organelle discharge. Mol Biol Cell 14: 3804-3820.
37. Assossou O, Besson F, Rouault JP, Persat F, Brisson C, et al. (2003) Subcellular localization of 14-3-3 proteins in Toxoplasma gondii tachyzoites and evidence for a lipid raft-associated form. FEMS Microbiol Lett 224: 161-168.
38. Johnson TM, Rajfur Z, Jacobson K, Beckers CJ, (2007) Immobilization of the type XIV myosin complex in Toxoplasma gondii. Mol Biol Cell 18: 3039-3046.
39. Coppens I, Sinai AP, Joiner KA, (2000) Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 149: 167-180.
40. Roos DS, Donald RGK, Morissette NS, Moulton ALC, (1994) Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 45: 27-63.
41. Uittenbogaard A, Smart EJ, (2000) Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J Biol Chem 275: 25595-25549.
42. Munoz-Olaya JM, Matabosch X, Bedia C, Egido-Gabás M, Casas J, et al. (2008) Synthesis and biological activity of a novel inhibitor of dihydroceramide desaturase. ChemMedChem 3: 946-953.
43. Merrill AH Jr, Sullards MC, Allegood JC, Kelly S, Wang E, (2005) Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry. Methods 36: 207-224.
44. McFarlane AS, (1958) Efficient trace-labelling of proteins with iodine. Nature 182: 53.
45. Fölsch H, Pypaert M, Schu P, Mellman I, (2001) Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J Cell Biol 152: 595-606.
46. Quittnat F, Nishikawa Y, Stedman TT, Voelker DR, Choi JY, et al. (2004) On the biogenesis of lipid bodies in ancient eukaryotes: synthesis of triacylglycerols by a Toxoplasma DGAT1-related enzyme. Mol Biochem Parasitol 138: 107-122.
47. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartne FH, et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
48. Sargiacomo M, Scherer PE, Tang Z, Kübler E, Song KS, et al. (1995) Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci U S A 92: 9407-9411.
49. Choudhury A, Marks DL, Proctor KM, Gould GW, Pagano RE, (2006) Regulation of caveolar endocytosis by syntaxin 6-dependent delivery of membrane components to the cell surface. Nat Cell Biol 8: 317-328.
50. Palade GE, (1953) Fine structure of blood capillaries. J. Appl. Physics 24: 1424.
51. Morrissette NS, Sibley LD, (2002) Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 66: 21-38.
52. Mann T, Beckers C, (2001) Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol Biochem Parasitol 115: 257-268.
53. Foussard F, Leriche MA, Dubremetz JF, (1991) Characterization of the lipid content of Toxoplasma gondii rhoptries. Parasitology 102: 367-370.
54. Parussini F, Coppens I, Shah PP, Diamond SL, Carruthers VB, (2010) Cathepsin L occupies a vacuolar compartment and is a protein maturase within the endo/exocytic system of Toxoplasma gondii. Mol Microbiol 76: 1340-1357.
55. Miranda K, Pace DA, Cintron R, Rodrigues JC, Fang J, et al. (2010) Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Mol Microbiol 76: 1358-1375.
56. Nam HW, (2009) GRA proteins of Toxoplasma gondii: maintenance of host-parasite interactions across the parasitophorous vacuolar membrane. Korean J Parasitol 47: S29-37.
57. Karsten V, Qi H, Beckers CJ, Reddy A, Dubremetz JF, et al. (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.
58. Chaturvedi S, Qi H, Coleman D, Rodriguez A, Hanson PI, et al. (1999) Constitutive calcium-independent release of Toxoplasma gondii dense granules occurs through the NSF/SNAP/SNARE/Rab machinery. J Biol Chem 274: 2424-2431.
59. Puri V, Watanabe R, Singh RD, Dominguez M, Brown JC, et al. (2001) Clathrin-dependent and-independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J Cell Biol 154: 535-547.
60. Rodighiero C, Fujinaga Y, Hirst TR, Lencer WI, (2001) A cholera toxin B-subunit variant that binds ganglioside G(M1) but fails to induce toxicity. J Biol Chem 276: 36939-36945.
61. Fujinaga Y, Wolf AA, Rodighiero C, Wheeler H, Tsai B, et al. (2003) Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulum. Mol Biol Cell 14: 4783-4793.
62. Hill MM, Bastiani M, Luetterforst R. Kirkham M, Kirkham A, et al. (2008) PTRF-cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132: 113-124.
63. Aboulaich N, Vainonen JP, Strålfors P, Vener A, (2004) Vectorial proteomics reveal targeting, phosphorylation and specific fragmentation of polymerase I and transcript release factor (PTRF) at the surface of caveolae in human adipocytes. Biochem J 383: 237-248.
64. Bai L, Deng X, Li J, Wang M, Li Q, et al. (2011) Regulation of cellular senescence by the essential caveolar component PTRF/Cavin-1. Cell Res 21: 1088-1101.
65. Pelkmans L, Zerial M, (2005) Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436: 128-133.
66. Li S, Galbiati F, Volonte D, Sargiacomo M, Engelman JA, et al. (1998) Mutational analysis of caveolin-induced vesicle formation. Expression of caveolin-1 recruits caveolin-2 to caveolae membranes. FEBS Lett 434: 127-134.
67. Robibaro B, Hoppe HC, Yang M, Coppens I, Ngô HM, et al. (2001) Endocytosis in different lifestyles of protozoan parasitism: role in nutrient uptake with special reference to Toxoplasma gondii. Int J Parasitol 31: 1343-1353.
68. Simionescu M, Popov D, Sima A, (2009) Endothelial transcytosis in health and disease. Cell Tissue Res 335: 27-40.
69. Verma P, Ostermeyer-Fay AG, Brown DA, (2010) Caveolin-1 induces formation of membrane tubules that sense actomyosin tension and are inhibited by polymerase I and transcript release factor/cavin-1. Mol Biol Cell 21: 2226-2240.
70. Yamaguchi H, Takeo Y, Yoshida S, Kouchi Z, Nakamur Y, et al. (2009) Lipid rafts and caveolin-1 are required for invadopodia formation and extracellular matrix degradation by human breast cancer cells. Cancer Res 69: 8594-8602.
71. Sinha B, Köster D, Ruez R, Gonnord P, Bastiani M, et al. (2011) Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144: 402-413.