Rab11 Regulates Trafficking of -sialidase to the Plasma Membrane through the Contractile Vacuole Complex of
Several free-living protozoa possess a contractile vacuole complex (CVC) that protects them from the hyposmotic environments where they live. Interestingly, the intracellular parasite Trypanosoma cruzi, the etiologic agent of Chagas disease, has conserved a CVC in all its developmental stages, where it has an osmoregulatory role under both hyposmotic and hyperosmotic conditions. We found here that the CVC of T. cruzi has an additional unconventional role in traffic of glycosylphosphatidylinositol (GPI)-anchored proteins to the plasma membrane of the parasite. A combination of genetic and biochemical approaches revealed the role of TcRab11, a protein localized to the CVC, in traffic of trans-sialidase (TcTS), a GPI-anchored protein important for host cell invasion, but not of other GPI-anchored proteins or integral membrane proteins, to the plasma membrane. Demonstration of the role of TcTS in infection has been previously difficult given the large number of genes encoding for this protein distributed through the genome of the parasite. However, by constructing dominant negative TcRab11 we were able to prevent traffic of TcTS to the plasma membrane and demonstrate its role in host invasion.
Vyšlo v časopise:
Rab11 Regulates Trafficking of -sialidase to the Plasma Membrane through the Contractile Vacuole Complex of. PLoS Pathog 10(6): e32767. doi:10.1371/journal.ppat.1004224
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004224
Souhrn
Several free-living protozoa possess a contractile vacuole complex (CVC) that protects them from the hyposmotic environments where they live. Interestingly, the intracellular parasite Trypanosoma cruzi, the etiologic agent of Chagas disease, has conserved a CVC in all its developmental stages, where it has an osmoregulatory role under both hyposmotic and hyperosmotic conditions. We found here that the CVC of T. cruzi has an additional unconventional role in traffic of glycosylphosphatidylinositol (GPI)-anchored proteins to the plasma membrane of the parasite. A combination of genetic and biochemical approaches revealed the role of TcRab11, a protein localized to the CVC, in traffic of trans-sialidase (TcTS), a GPI-anchored protein important for host cell invasion, but not of other GPI-anchored proteins or integral membrane proteins, to the plasma membrane. Demonstration of the role of TcTS in infection has been previously difficult given the large number of genes encoding for this protein distributed through the genome of the parasite. However, by constructing dominant negative TcRab11 we were able to prevent traffic of TcTS to the plasma membrane and demonstrate its role in host invasion.
Zdroje
1. AllenRD, NaitohY (2002) Osmoregulation and contractile vacuoles of protozoa. Int Rev Cytol 215: 351–394.
2. DocampoR, JimenezV, LanderN, LiZH, NiyogiS (2013) New insights into roles of acidocalcisomes and contractile vacuole complex in osmoregulation in protists. Int Rev Cell Mol Biol 305: 69–113.
3. MontalvettiA, RohloffP, DocampoR (2004) A functional aquaporin co-localizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi. J Biol Chem 279: 38673–38682.
4. RohloffP, MontalvettiA, DocampoR (2004) Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi. J Biol Chem 279: 52270–52281.
5. FigarellaK, UzcateguiNL, ZhouY, LeFurgeyA, OuelletteM, et al. (2007) Biochemical characterization of Leishmania major aquaglyceroporin LmAQP1: possible role in volume regulation and osmotaxis. Mol Microbiol 65: 1006–1017.
6. NishiharaE, YokotaE, TazakiA, OriiH, KatsuharaM, et al. (2008) Presence of aquaporin and V-ATPase on the contractile vacuole of Amoeba proteus. Biol Cell 100: 179–188.
7. Komsic-BuchmannK, StephanLM, BeckerB (2012) The SEC6 protein is required for contractile vacuole function in Chlamydomonas reinhardtii. J Cell Sci 125: 2885–2895.
8. ClarkTB (1959) Comparative morphology of four genera of trypanosomatidae. J Protozool 6: 227–232.
9. Girard-DiasW, AlcantaraCL, CunhaESN, de SouzaW, MirandaK (2012) On the ultrastructural organization of Trypanosoma cruzi using cryopreparation methods and electron tomography. Histochem Cell Biol 138: 821–831.
10. LiZH, AlvarezVE, De GaudenziJG, Sant'AnnaC, FraschAC, et al. (2011) Hyperosmotic stress induces aquaporin-dependent cell shrinkage, polyphosphate synthesis, amino acid accumulation, and global gene expression changes in Trypanosoma cruzi. J Biol Chem 286: 43959–43971.
11. PatelS, DocampoR (2010) Acidic calcium stores open for business: expanding the potential for intracellular Ca2+ signaling. Trends Cell Biol 20: 277–286.
12. MoniakisJ, CoukellMB, JaniecA (1999) Involvement of the Ca2+-ATPase PAT1 and the contractile vacuole in calcium regulation in Dictyostelium discoideum. J Cell Sci 112: 405–414.
13. MalchowD, LuscheDF, SchlattererC, De LozanneA, Muller-TaubenbergerA (2006) The contractile vacuole in Ca2+-regulation in Dictyostelium: its essential function for cAMP-induced Ca2+-influx. BMC Dev Biol 6: 31.
14. LadenburgerEM, KornI, KasielkeN, WassmerT, PlattnerH (2006) An Ins(1,4,5)P3 receptor in Paramecium is associated with the osmoregulatory system. J Cell Sci 119: 3705–3717.
15. LudlowMJ, DuraiL, EnnionSJ (2009) Functional characterization of intracellular Dictyostelium discoideum P2X receptors. J Biol Chem 284: 35227–35239.
16. SivaramakrishnanV, FountainSJ (2012) A mechanism of intracellular P2X receptor activation. J Biol Chem 287: 28315–28326.
17. HeuserJ, ZhuQ, ClarkeM (1993) Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J Cell Biol 121: 1311–1327.
18. SesakiH, WongEF, SiuCH (1997) The cell adhesion molecule DdCAD-1 in Dictyostelium is targeted to the cell surface by a nonclassical transport pathway involving contractile vacuoles. J Cell Biol 138: 939–951.
19. HeuserJ (2006) Evidence for recycling of contractile vacuole membrane during osmoregulation in Dictyostelium amoebae–a tribute to Gunther Gerisch. Eur J Cell Biol 85: 859–871.
20. SriskanthadevanS, LeeT, LinZ, YangD, SiuCH (2009) Cell adhesion molecule DdCAD-1 is imported into contractile vacuoles by membrane invagination in a Ca2+- and conformation-dependent manner. J Biol Chem 284: 36377–36386.
21. HasneMP, CoppensI, SoysaR, UllmanB (2010) A high-affinity putrescine-cadaverine transporter from Trypanosoma cruzi. Mol Microbiol 76: 78–91.
22. MacroL, JaiswalJK, SimonSM (2012) Dynamics of clathrin-mediated endocytosis and its requirement for organelle biogenesis in Dictyostelium. J Cell Sci 125: 5721–5732.
23. KellyEE, HorganCP, McCaffreyMW (2012) Rab11 proteins in health and disease. Biochem Soc Trans 40: 1360–1367.
24. JeffriesTR, MorganGW, FieldMC (2001) A developmentally regulated Rab11 homologue in Trypanosoma brucei is involved in recycling processes. J Cell Sci 114: 2617–2626.
25. HarrisE, YoshidaK, CardelliJ, BushJ (2001) Rab11-like GTPase associates with and regulates the structure and function of the contractile vacuole system in Dictyostelium. J Cell Sci 114: 3035–3045.
26. UlrichPN, JimenezV, ParkM, MartinsVP, AtwoodJ3rd, et al. (2011) Identification of contractile vacuole proteins in Trypanosoma cruzi. PloS One 6: e18013.
27. PalA, HallBS, JeffriesTR, FieldMC (2003) Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem J 374: 443–451.
28. GrunfelderCG, EngstlerM, WeiseF, SchwarzH, StierhofYD, et al. (2003) Endocytosis of a glycosylphosphatidylinositol-anchored protein via clathrin-coated vesicles, sorting by default in endosomes, and exocytosis via Rab11-positive carriers. Mol Biol Cell 14: 2029–2040.
29. El-SayedNM, MylerPJ, BartholomeuDC, NilssonD, AggarwalG, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409–415.
30. FreitasLM, dos SantosSL, Rodrigues-LuizGF, MendesTA, RodriguesTS, et al. (2011) Genomic analyses, gene expression and antigenic profile of the trans-sialidase superfamily of Trypanosoma cruzi reveal an undetected level of complexity. PloS One 6: e25914.
31. Di NoiaJM, BuscagliaCA, De MarchiCR, AlmeidaIC, FraschAC (2002) A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas' disease is due to a single parasite lineage. J Exp Med 195: 401–413.
32. CremonaML, CampetellaO, SanchezDO, FraschAC (1999) Enzymically inactive members of the trans-sialidase family from Trypanosoma cruzi display beta-galactose binding activity. Glycobiology 9: 581–587.
33. TomlinsonS, Pontes de CarvalhoLC, VandekerckhoveF, NussenzweigV (1994) Role of sialic acid in the resistance of Trypanosoma cruzi trypomastigotes to complement. J Immunol 153: 3141–3147.
34. BuscagliaCA, CampoVA, FraschAC, Di NoiaJM (2006) Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat Rev Microbiol 4: 229–236.
35. Pereira-ChioccolaVL, Acosta-SerranoA, Correia de AlmeidaI, FergusonMA, Souto-PadronT, et al. (2000) Mucin-like molecules form a negatively charged coat that protects Trypanosoma cruzi trypomastigotes from killing by human anti-alpha-galactosyl antibodies. J Cell Sci 113: 1299–1307.
36. SchenkmanS, JiangMS, HartGW, NussenzweigV (1991) A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell 65: 1117–1125.
37. BuschiazzoA, MuiaR, LarrieuxN, PitcovskyT, MucciJ, et al. (2012) Trypanosoma cruzi trans-sialidase in complex with a neutralizing antibody: structure/function studies towards the rational design of inhibitors. PLoS Path 8: e1002474.
38. Rubin-de-CelisSS, UemuraH, YoshidaN, SchenkmanS (2006) Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell Microbiol 8: 1888–1898.
39. TribulattiMV, MucciJ, Van RooijenN, LeguizamonMS, CampetellaO (2005) The trans-sialidase from Trypanosoma cruzi induces thrombocytopenia during acute Chagas' disease by reducing the platelet sialic acid contents. Infect Immun 73: 201–207.
40. MucciJ, HidalgoA, MocettiE, ArgibayPF, LeguizamonMS, et al. (2002) Thymocyte depletion in Trypanosoma cruzi infection is mediated by trans-sialidase-induced apoptosis on nurse cells complex. Proc Nat Acad Sci USA 99: 3896–3901.
41. Freire-de-LimaL, Alisson-SilvaF, CarvalhoST, TakiyaCM, RodriguesMM, et al. (2010) Trypanosoma cruzi subverts host cell sialylation and may compromise antigen-specific CD8+ T cell responses. J Biol Chem 285: 13388–13396.
42. CanepaGE, DegeseMS, BuduA, GarciaCR, BuscagliaCA (2012) Involvement of TSSA (trypomastigote small surface antigen) in Trypanosoma cruzi invasion of mammalian cells. Biochem J 444: 211–218.
43. AlmeidaIC, FergusonMA, SchenkmanS, TravassosLR (1994) Lytic anti-alpha-galactosyl antibodies from patients with chronic Chagas' disease recognize novel O-linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem J 304: 793–802.
44. AlmeidaIC, KrautzGM, KrettliAU, TravassosLR (1993) Glycoconjugates of Trypanosoma cruzi: a 74 kD antigen of trypomastigotes specifically reacts with lytic anti-alpha-galactosyl antibodies from patients with chronic Chagas disease. J Clin Lab Anal 7: 307–316.
45. AlmeidaIC, MilaniSR, GorinPA, TravassosLR (1991) Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-alpha-galactosyl antibodies. J Immunol 146: 2394–2400.
46. Di NoiaJM, D'OrsoI, AslundL, SanchezDO, FraschAC (1998) The Trypanosoma cruzi mucin family is transcribed from hundreds of genes having hypervariable regions. J Biol Chem 273: 10843–10850.
47. YoshidaN, MortaraRA, AraguthMF, GonzalezJC, RussoM (1989) Metacyclic neutralizing effect of monoclonal antibody 10D8 directed to the 35- and 50-kilodalton surface glycoconjugates of Trypanosoma cruzi. Infect Immun 57: 1663–1667.
48. FujitaM, KinoshitaT (2012) GPI-anchor remodeling: potential functions of GPI-anchors in intracellular trafficking and membrane dynamics. Biochim Biophys Acta 1821: 1050–1058.
49. FukudaM (2010) How can mammalian Rab small GTPases be comprehensively analyzed?: Development of new tools to comprehensively analyze mammalian Rabs in membrane traffic. Histol Histopathol 25: 1473–1480.
50. DocampoR (2011) Molecular parasitology in the 21st century. Essays Biochem 51: 1–13.
51. FeigLA (1999) Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat Cell Biol 1: E25–27.
52. StenmarkH (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513–525.
53. RohloffP, RodriguesCO, DocampoR (2003) Regulatory volume decrease in Trypanosoma cruzi involves amino acid efflux and changes in intracellular calcium. Mol Biochem Parasitol 126: 219–230.
54. PereiraME (1983) A developmentally regulated neuraminidase activity in Trypanosoma cruzi. Science 219: 1444–1446.
55. FrevertU, SchenkmanS, NussenzweigV (1992) Stage-specific expression and intracellular shedding of the cell surface trans-sialidase of Trypanosoma cruzi. Infec Immun 60: 2349–2360.
56. GiorgiME, de LederkremerRM (2011) Trans-sialidase and mucins of Trypanosoma cruzi: an important interplay for the parasite. Carbohydr Res 346: 1389–1393.
57. BuscagliaCA, CampetellaO, LeguizamonMS, FraschAC (1998) The repetitive domain of Trypanosoma cruzi trans-sialidase enhances the immune response against the catalytic domain. J Infect Dis 177: 431–436.
58. Souto-PadronT, ReyesMB, LeguizamonS, CampetellaOE, FraschAC, et al. (1989) Trypanosoma cruzi proteins which are antigenic during human infections are located in defined regions of the parasite. Eur J Cell Biol 50: 272–278.
59. EllgaardL, MolinariM, HeleniusA (1999) Setting the standards: quality control in the secretory pathway. Science 286: 1882–1888.
60. ParodiAJ, PollevickGD, MautnerM, BuschiazzoA, SanchezDO, et al. (1992) Identification of the gene(s) coding for the trans-sialidase of Trypanosoma cruzi. EMBO J 11: 1705–1710.
61. VanderheydenN, BenaimG, DocampoR (1996) The role of a H+-ATPase in the regulation of cytoplasmic pH in Trypanosoma cruzi epimastigotes. Biochem J 318: 103–109.
62. LuoS, ScottDA, DocampoR (2002) Trypanosoma cruzi H+-ATPase 1 (TcHA1) and 2 (TcHA2) genes complement yeast mutants defective in H+ pumps and encode plasma membrane P-type H+-ATPases with different enzymatic properties. J Biol Chem 277: 44497–44506.
63. VieiraM, RohloffP, LuoS, Cunha-e-SilvaNL, de SouzaW, et al. (2005) Role for a P-type H+-ATPase in the acidification of the endocytic pathway of Trypanosoma cruzi. Biochem J 392: 467–474.
64. YoshidaN (2006) Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An Acad Bras Cienc 78: 87–111.
65. TylerKM, FridbergA, TorielloKM, OlsonCL, CieslakJA, et al. (2009) Flagellar membrane localization via association with lipid rafts. J Cell Sci 122: 859–866.
66. MaricD, McGwireBS, BuchananKT, OlsonCL, EmmerBT, et al. (2011) Molecular determinants of ciliary membrane localization of Trypanosoma cruzi flagellar calcium-binding protein. J Biol Chem 286: 33109–33117.
67. CampetellaOE, UttaroAD, ParodiAJ, FraschAC (1994) A recombinant Trypanosoma cruzi trans-sialidase lacking the amino acid repeats retains the enzymatic activity. Mol Biochem Parasitol 64: 337–340.
68. OppezzoP, ObalG, BaraibarMA, PritschO, AlzariPM, et al. (2011) Crystal structure of an enzymatically inactive trans-sialidase-like lectin from Trypanosoma cruzi: the carbohydrate binding mechanism involves residual sialidase activity. Biochim Biophys Acta 1814: 1154–1161.
69. CremonaML, SanchezDO, FraschAC, CampetellaO (1995) A single tyrosine differentiates active and inactive Trypanosoma cruzi trans-sialidases. Gene 160: 123–128.
70. TodeschiniAR, DiasWB, GirardMF, WieruszeskiJM, Mendonca-PreviatoL, et al. (2004) Enzymatically inactive trans-sialidase from Trypanosoma cruzi binds sialyl and beta-galactopyranosyl residues in a sequential ordered mechanism. J Biol Chem 279: 5323–5328.
71. TodeschiniAR, GirardMF, WieruszeskiJM, NunesMP, DosReisGA, et al. (2002) Trans-sialidase from Trypanosoma cruzi binds host T-lymphocytes in a lectin manner. J Biol Chem 277: 45962–45968.
72. SilvermanJS, BangsJD (2012) Form and function in the trypanosomal secretory pathway. Curr Opin Microbiol 15: 463–468.
73. SoaresMJ, Souto-PadronT, De SouzaW (1992) Identification of a large pre-lysosomal compartment in the pathogenic protozoon Trypanosoma cruzi. J Cell Sci 102: 157–167.
74. ChiribaoML, LibischMG, OsinagaE, Parodi-TaliceA, RobelloC (2012) Cloning, localization and differential expression of the Trypanosoma cruzi TcOGNT-2 glycosyl transferase. Gene 498: 147–154.
75. Bayer-SantosE, Aguilar-BonavidesC, RodriguesSP, CorderoEM, MarquesAF, et al. (2013) Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. J Proteome Res 12: 883–897.
76. MaedaY, KinoshitaT (2011) Structural remodeling, trafficking and functions of glycosylphosphatidylinositol-anchored proteins. Prog Lipid Res 50: 411–424.
77. CorderoEM, NakayasuES, GentilLG, YoshidaN, AlmeidaIC, et al. (2009) Proteomic analysis of detergent-solubilized membrane proteins from insect-developmental forms of Trypanosoma cruzi. J Proteome Res 8: 3642–3652.
78. Gabernet-CastelloC, DuboisKN, NimmoC, FieldMC (2011) Rab11 function in Trypanosoma brucei: identification of conserved and novel interaction partners. Eukaryotic cell 10: 1082–1094.
79. EssidM, GopaldassN, YoshidaK, MerrifieldC, SoldatiT (2012) Rab8a regulates the exocyst-mediated kiss-and-run discharge of the Dictyostelium contractile vacuole. Mol Biol Cell 23: 1267–1282.
80. LangF, BuschGL, VolklH (1998) The diversity of volume regulatory mechanisms. Cell Physiol Biochem 8: 1–45.
81. GoWY, LiuX, RotiMA, LiuF, HoSN (2004) NFAT5/TonEBP mutant mice define osmotic stress as a critical feature of the lymphoid microenvironment. Proc Natl Acad Sci USA 101: 10673–10678.
82. KollienAH, GrospietschT, KleffmannT, Zerbst-BoroffkaI, SchaubGA (2001) Ionic composition of the rectal contents and excreta of the reduviid bug Triatoma infestans. J Insect Physiol 47: 739–747.
83. SchmatzDM, MurrayPK (1982) Cultivation of Trypanosoma cruzi in irradiated muscle cells: improved synchronization and enhanced trypomastigote production. Parasitology 85: 115–125.
84. MorenoSN, SilvaJ, VercesiAE, DocampoR (1994) Cytosolic-free calcium elevation in Trypanosoma cruzi is required for cell invasion. J Exp Med 180: 1535–1540.
85. BourguignonSC, de SouzaW, Souto-PadronT (1998) Localization of lectin-binding sites on the surface of Trypanosoma cruzi grown in chemically defined conditions. Histochem Cell Biol 110: 527–534.
86. de Paulo MartinsV, OkuraM, MaricD, EngmanDM, VieiraM, et al. (2010) Acylation-dependent export of Trypanosoma cruzi phosphoinositide-specific phospholipase C to the outer surface of amastigotes. J Biol Chem 285: 30906–30917.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 6
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Fungal Nail Infections (Onychomycosis): A Never-Ending Story?
- Profilin Promotes Recruitment of Ly6C CCR2 Inflammatory Monocytes That Can Confer Resistance to Bacterial Infection
- Cytoplasmic Viral RNA-Dependent RNA Polymerase Disrupts the Intracellular Splicing Machinery by Entering the Nucleus and Interfering with Prp8
- HopW1 from Disrupts the Actin Cytoskeleton to Promote Virulence in Arabidopsis