Navegar

Colección

Datos Estadísticas

Artículo

Lantos, A.B.; Carlevaro, G.; Araoz, B.; Ruiz Diaz, P.; Camara, M.D.L.M.; Buscaglia, C.A.; Bossi, M.; Yu, H.; Chen, X.; Bertozzi, C.R.; Mucci, J.; Campetella, O. "Sialic Acid Glycobiology Unveils Trypanosoma cruzi Trypomastigote Membrane Physiology" (2016) PLoS Pathogens. 12(4)
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Trypanosoma cruzi, the flagellate protozoan agent of Chagas disease or American trypanosomiasis, is unable to synthesize sialic acids de novo. Mucins and trans-sialidase (TS) are substrate and enzyme, respectively, of the glycobiological system that scavenges sialic acid from the host in a crucial interplay for T. cruzi life cycle. The acquisition of the sialyl residue allows the parasite to avoid lysis by serum factors and to interact with the host cell. A major drawback to studying the sialylation kinetics and turnover of the trypomastigote glycoconjugates is the difficulty to identify and follow the recently acquired sialyl residues. To tackle this issue, we followed an unnatural sugar approach as bioorthogonal chemical reporters, where the use of azidosialyl residues allowed identifying the acquired sugar. Advanced microscopy techniques, together with biochemical methods, were used to study the trypomastigote membrane from its glycobiological perspective. Main sialyl acceptors were identified as mucins by biochemical procedures and protein markers. Together with determining their shedding and turnover rates, we also report that several membrane proteins, including TS and its substrates, both glycosylphosphatidylinositol-anchored proteins, are separately distributed on parasite surface and contained in different and highly stable membrane microdomains. Notably, labeling for α(1,3)Galactosyl residues only partially colocalize with sialylated mucins, indicating that two species of glycosylated mucins do exist, which are segregated at the parasite surface. Moreover, sialylated mucins were included in lipid-raft-domains, whereas TS molecules are not. The location of the surface-anchored TS resulted too far off as to be capable to sialylate mucins, a role played by the shed TS instead. Phosphatidylinositol-phospholipase-C activity is actually not present in trypomastigotes. Therefore, shedding of TS occurs via microvesicles instead of as a fully soluble form. © 2016 Lantos et al.

Registro:

Documento: Artículo
Título:Sialic Acid Glycobiology Unveils Trypanosoma cruzi Trypomastigote Membrane Physiology
Autor:Lantos, A.B.; Carlevaro, G.; Araoz, B.; Ruiz Diaz, P.; Camara, M.D.L.M.; Buscaglia, C.A.; Bossi, M.; Yu, H.; Chen, X.; Bertozzi, C.R.; Mucci, J.; Campetella, O.
Filiación:Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín, San Martín, Buenos Aires and Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Laboratorio de Nanoscopías Fotónicas, INQUIMAE, Facultad de Ciencias Exactas y NaturalesFacultad de Ciencias Exactas y Natura, Universidad de Buenos Aires, Buenos Aires, Argentina
Department of Chemistry, University of California, Davis, Davis, CA, United States
Department of Chemistry, Stanford University and Howard Hughes Medical Institute, Stanford, CA, United States
Palabras clave:glycosylphosphatidylinositol anchored protein; mucin; phosphatidylinositol diacylglycerol lyase; sialic acid; sialidase; glycoprotein; mucin; n acetylneuraminic acid; sialidase; trans-sialidase; affinity chromatography; Article; atomic force microscopy; cell migration; cell proliferation; Chagas disease; controlled study; enzyme activity; glycobiology; immunofluorescence microscopy; mass spectrometry; membrane fluidity; membrane microparticle; nonhuman; parasite survival; parasite virulence; protein expression; protein purification; sialylation; transmission electron microscopy; Trypanosoma cruzi; trypomastigote; ultracentrifugation; Western blotting; animal; Bagg albino mouse; Chagas disease; disease model; fluorescence microscopy; host parasite interaction; image processing; metabolism; microscopy; mouse; parasitology; pathogenicity; physiology; procedures; Trypanosoma cruzi; virulence; Animals; Cell-Derived Microparticles; Chagas Disease; Disease Models, Animal; Glycoproteins; Host-Parasite Interactions; Image Processing, Computer-Assisted; Mass Spectrometry; Mice; Mice, Inbred BALB C; Microscopy; Microscopy, Fluorescence; Mucins; N-Acetylneuraminic Acid; Neuraminidase; Trypanosoma cruzi; Virulence
Año:2016
Volumen:12
Número:4
DOI: http://dx.doi.org/10.1371/journal.ppat.1005559
Título revista:PLoS Pathogens
Título revista abreviado:PLoS Pathog.
ISSN:15537366
CAS:phosphatidylinositol diacylglycerol lyase, 37288-19-0; sialidase, 9001-67-6; n acetylneuraminic acid, 131-48-6; Glycoproteins; Mucins; N-Acetylneuraminic Acid; Neuraminidase; trans-sialidase
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_15537366_v12_n4_p_Lantos

Referencias:

  • Oliveira, I.A., Freire-de-Lima, L., Penha, L.L., Dias, W.B., Todeschini, A.R., Trypanosoma cruzi trans-sialidase: structural features and biological implications (2014) Subcell Biochem, 74, pp. 181-201. , 24264246
  • Rubin de Celis, S.S., Schenkman, S., Trypanosoma cruzi trans-sialidase as a multifunctional enzyme in Chagas' disease (2012) Cell Microbiol, 14, pp. 1522-1530. , 22747789
  • Ruiz Diaz, P., Mucci, J., Meira, M.A., Bogliotti, Y., Musikant, D., Leguizamon, M.S., Trypanosoma cruzi trans-sialidase prevents elicitation of Th1 cell response via Interleukin 10 and downregulates Th1 effector cells (2015) Infect Immun, 83, pp. 2099-2108. , 25754197, .;:–
  • Risso, M.G., Garbarino, G.B., Mocetti, E., Campetella, O., González Cappa, S.M., Buscaglia, C.A., Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages (2004) J Infect Dis, 189, pp. 2250-2259. , 15181573, .;:–
  • Leguizamón, M.S., Campetella, O.E., González Cappa, S.M., Frasch, A.C., Mice infected with Trypanosoma cruzi produce antibodies against the enzymatic domain of trans-sialidase that inhibit its activity (1994) Infect Immun, 62, pp. 3441-3446. , 8039915
  • Muiá, R.P., Yu, H., Prescher, J.A., Hellman, U., Chen, X., Bertozzi, C.R., Identification of glycoproteins targeted by Trypanosoma cruzi trans-sialidase, a virulence factor that disturbs lymphocyte glycosylation (2010) Glycobiology, 20, pp. 833-842. , 20354005, .;:–
  • De Pablos, L.M., Osuna, A., Multigene families in Trypanosoma cruzi and their role in infectivity (2012) Infect Immun, 80, pp. 2258-2264. , 22431647, .;:–. [pii
  • Pereira-Chioccola, V.L., Acosta-Serrano, A., Correia de Almeida, I., Ferguson, M.A., Souto-Padron, T., Rodrigues, M.M., Mucin-like molecules form a negatively charged coat that protects Trypanosoma cruzi trypomastigotes from killing by human anti-α-galactosyl antibodies (2000) J Cell Sci, 113, pp. 1299-1307. , 10704380, .;:–
  • Tomlinson, S., Pontes de Carvalho, L.C., Vandekerckhove, F., Nussenzweig, V., Role of sialic acid in the resistance of Trypanosoma cruzi trypomastigotes to complement (1994) J Immunol, 153, pp. 3141-3147. , 8089492
  • Schenkman, S., Ferguson, M.A., Heise, N., de Almeida, M.L., Mortara, R.A., Yoshida, N., Mucin-like glycoproteins linked to the membrane by glycosylphosphatidylinositol anchor are the major acceptors of sialic acid in a reaction catalyzed by trans-sialidase in metacyclic forms of Trypanosoma cruzi (1993) Mol Biochem Parasitol, 59, pp. 293-303. , 8341326
  • Buscaglia, C.A., Campo, V.A., Frasch, A.C., Di Noia, J.M., Trypanosoma cruzi surface mucins: host-dependent coat diversity (2006) Nat Rev Microbiol, 4, pp. 229-236. , 16489349
  • de Lederkremer, R.M., Agusti, R., Glycobiology of Trypanosoma cruzi (2009) Adv Carbohydr Chem Biochem, 62, pp. 311-366. , 19501708
  • Camargo, M.M., Almeida, I.C., Pereira, M.E., Ferguson, M.A., Travassos, L.R., Gazzinelli, R.T., Glycosylphosphatidylinositol-anchored mucin-like glycoproteins isolated from Trypanosoma cruzi trypomastigotes initiate the synthesis of proinflammatory cytokines by macrophages (1997) J Immunol, 158, pp. 5890-5901. , 9190942
  • Almeida, I.C., Camargo, M.M., Procopio, D.O., Silva, L.S., Mehlert, A., Travassos, L.R., Highly purified glycosylphosphatidylinositols from Trypanosoma cruzi are potent proinflammatory agents (2000) EMBO J, 19, pp. 1476-1485. , 10747016, .;:–
  • Trocoli, T.A.C., Tonelli, R.R., Pavanelli, W.R., da Silva, J.S., Schumacher, R.I., de Souza, W., Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response (2009) Microbes Infect, 11, pp. 29-39. , 19028594, .;:–
  • Di Noia, J.M., D'Orso, I., Aslund, L., Sanchez, D.O., Frasch, A.C., The Trypanosoma cruzi mucin family is transcribed from hundreds of genes having hypervariable regions (1998) J Biol Chem, 273, pp. 10843-10850. , 9556557
  • Buscaglia, C.A., Campo, V.A., Di Noia, J.M., Torrecilhas, A.C., De Marchi, C.R., Ferguson, M.A., The surface coat of the mammal-dwelling infective trypomastigote stage of Trypanosoma cruzi is formed by highly diverse immunogenic mucins (2004) J Biol Chem, 279, pp. 15860-15869. , 14749325, .;:–
  • Bernabo, G., Levy, G., Ziliani, M., Caeiro, L.D., Sanchez, D.O., Tekiel, V., TcTASV-C, a protein family in Trypanosoma cruzi that is predominantly trypomastigote-stage specific and secreted to the medium (2013) PLoS One, 8, p. 71192. , 23923058, .;:
  • Giorgi, M.E., de Lederkremer, R.M., trans-Sialidase and mucins of Trypanosoma cruzi: an important interplay for the parasite (2011) Carbohydr Res, 346, pp. 1389-1393. , 21645882
  • Almeida, I.C., Ferguson, M.A., Schenkman, S., Travassos, L.R., Lytic anti-α-galactosyl antibodies from patients with chronic Chagas' disease recognize novel O-linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi (1994) Biochem J, 304, pp. 793-802. , 7818483
  • Acosta-Serrano, A., Almeida, I.C., Freitas-Junior, L.H., Yoshida, N., Schenkman, S., The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles (2001) Mol Biochem Parasitol, 114, pp. 143-150. , 11378194
  • Prescher, J.A., Dube, D.H., Bertozzi, C.R., Chemical remodelling of cell surfaces in living animals (2004) Nature, 430, pp. 873-877. , 15318217
  • Prescher, J.A., Bertozzi, C.R., Chemistry in living systems (2005) Nat Chem Biol, 1, pp. 13-21. , 16407987
  • de Souza, W., Macro, micro and nano domains in the membrane of parasitic protozoa (2007) Parasitol Int, 56, pp. 161-170. , 17347028
  • Niyogi, S., Mucci, J., Campetella, O., Docampo, R., Rab11 regulates trafficking of trans-sialidase to the plasma membrane through the contractile vacuole complex of Trypanosoma cruzi (2014) PLoS Pathog, 10, p. 1004224. , 24968013, .;:
  • Di Noia, J.M., Buscaglia, C.A., De Marchi, C.R., Almeida, I.C., Frasch, A.C., A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas' disease is due to a single parasite lineage (2002) J Exp Med, 195, pp. 401-413. , 11854354
  • Couto, A.S., Goncalves, M.F., Colli, W., de Lederkremer, R.M., The N-linked carbohydrate chain of the 85-kilodalton glycoprotein from Trypanosoma cruzi trypomastigotes contains sialyl, fucosyl and galactosyl (α1–3)galactose units (1990) Mol Biochem Parasitol, 39, pp. 101-107. , 2106074
  • Schenkman, S., Eichinger, D., Pereira, M.E., Nussenzweig, V., Structural and functional properties of Trypanosoma trans-sialidase (1994) Annu Rev Microbiol, 48, pp. 499-523. , 7826016
  • Buschiazzo, A., Muiá, R., Larrieux, N., Pitcovsky, T., Mucci, J., Campetella, O., Trypanosoma cruzi trans-sialidase in complex with a neutralizing antibody: structure/function studies towards the rational design of inhibitors (2012) PLoS Pathog, 8, p. 1002474. , 22241998, .;:
  • Jewett, J.C., Sletten, E.M., Bertozzi, C.R., Rapid Cu-free click chemistry with readily synthesized biarylazacyclooctynones (2010) J Am Chem Soc, 132, pp. 3688-3690. , 20187640
  • Baskin, J.M., Prescher, J.A., Laughlin, S.T., Agard, N.J., Chang, P.V., Miller, I.A., Copper-free click chemistry for dynamic in vivo imaging (2007) Proc Natl Acad Sci U S A, 104, pp. 16793-16797. , 17942682, .;:–
  • Folling, J., Bossi, M., Bock, H., Medda, R., Wurm, C.A., Hein, B., Fluorescence nanoscopy by ground-state depletion and single-molecule return (2008) Nat Methods, 5, pp. 943-945. , 18794861, .;:–
  • Simons, K., Sampaio, J.L., Membrane organization and lipid rafts (2011) Cold Spring Harb Perspect Biol, 3, p. a004697. , 21628426, .;:
  • Diaz-Rohrer, B.B., Levental, K.R., Simons, K., Levental, I., Membrane raft association is a determinant of plasma membrane localization (2014) Proc Natl Acad Sci U S A, 111, pp. 8500-8505. , 24912166
  • Tyler, K.M., Fridberg, A., Toriello, K.M., Olson, C.L., Cieslak, J.A., Hazlett, T.L., Flagellar membrane localization via association with lipid rafts (2009) J Cell Sci, 122, pp. 859-866. , 19240119, .;:–
  • Urban, I., Santurio, L.B., Chidichimo, A., Yu, H., Chen, X., Mucci, J., Molecular diversity of the Trypanosoma cruzi TcSMUG family of mucin genes and proteins (2011) Biochem J, 438, pp. 303-313. , 21651499, .;:–
  • Campo, V.A., Buscaglia, C.A., Di Noia, J.M., Frasch, A.C., Immunocharacterization of the mucin-type proteins from the intracellular stage of Trypanosoma cruzi (2006) Microbes Infect, 8, pp. 401-409. , 16253534
  • Lumb, J.H., Field, M.C., Rab23 is a flagellar protein in Trypanosoma brucei (2011) BMC Res Notes, 4, p. 190. , 21676215, .;:
  • Camara, M.L., Bouvier, L.A., Miranda, M.R., Pereira, C.A., The flagellar adenylate kinases of Trypanosoma cruzi (2015) FEMS Microbiol Lett, 362, pp. 1-5. , .;:–
  • Quanquin, N.M., Galaviz, C., Fouts, D.L., Wrightsman, R.A., Manning, J.E., Immunization of mice with a TolA-like surface protein of Trypanosoma cruzi generates CD4(+) T-cell-dependent parasiticidal activity (1999) Infect Immun, 67, pp. 4603-4612. , 10456906
  • Ulrich, P.N., Jimenez, V., Park, M., Martins, V.P., Atwood, J., 3rd, Moles, K., Identification of contractile vacuole proteins in Trypanosoma cruzi (2011) PLoS One, 6, p. 18013. , 21437209
  • Finkelsztein, E.J., Diaz-Soto, J.C., Vargas-Zambrano, J.C., Suesca, E., Guzman, F., Lopez, M.C., Altering the motility of Trypanosoma cruzi with rabbit polyclonal anti-peptide antibodies reduces infection to susceptible mammalian cells (2015) Exp Parasitol, 150, pp. 36-43. , 25633439, .;:–
  • Hashimoto, M., Enomoto, M., Morales, J., Kurebayashi, N., Sakurai, T., Hashimoto, T., Inositol 1,4,5-trisphosphate receptor regulates replication, differentiation, infectivity and virulence of the parasitic protist Trypanosoma cruzi (2013) Mol Microbiol, 87, pp. 1133-1150. , 23320762, .;:–
  • Freitas, L.M., dos Santos, S.L., Rodrigues-Luiz, G.F., Mendes, T.A., Rodrigues, T.S., Gazzinelli, R.T., Genomic analyses, gene expression and antigenic profile of the trans-sialidase superfamily of Trypanosoma cruzi reveal an undetected level of complexity (2011) PLoS One, 6, p. 25914. , 22039427
  • Bartholomeu, D.C., Cerqueira, G.C., Leao, A.C., daRocha, W.D., Pais, F.S., Macedo, C., Genomic organization and expression profile of the mucin-associated surface protein (MASP) family of the human pathogen Trypanosoma cruzi (2009) Nucleic Acids Res, 37, pp. 3407-3417. , 19336417, .;:–
  • Bayer-Santos, E., Aguilar-Bonavides, C., Rodrigues, S.P., Cordero, E.M., Marques, A.F., Varela-Ramirez, A., Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins (2013) J Proteome Res, 12, pp. 883-897. , 23214914, .;:–
  • Galetovic, A., Souza, R.T., Santos, M.R., Cordero, E.M., Bastos, I.M., Santana, J.M., The repetitive cytoskeletal protein H49 of Trypanosoma cruzi is a calpain-like protein located at the flagellum attachment zone (2011) PLoS One, 6, p. 27634. , 22096606
  • Jimenez, V., Docampo, R., Molecular and electrophysiological characterization of a novel cation channel of Trypanosoma cruzi (2012) PLoS Pathog, 8, p. 1002750. , 22685407, .;:
  • Rocha, G.M., Miranda, K., Weissmuller, G., Bisch, P.M., de Souza, W., Ultrastructure of Trypanosoma cruzi revisited by atomic force microscopy (2008) Microsc Res Tech, 71, pp. 133-139. , 17992694
  • Rocha, G.M., Miranda, K., Weissmuller, G., Bisch, P.M., de Souza, W., Visualization of the flagellar surface of protists by atomic force microscopy (2010) Micron, 41, pp. 939-944. , 20719525
  • Schenkman, S., Pontes de Carvalho, L., Nussenzweig, V., Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzymes (1992) J Exp Med, 175, pp. 567-575. , 1732417
  • Furuya, T., Kashuba, C., Docampo, R., Moreno, S.N., A novel phosphatidylinositol-phospholipase C of Trypanosoma cruzi that is lipid modified and activated during trypomastigote to amastigote differentiation (2000) J Biol Chem, 275, pp. 6428-6438. , 10692446
  • Martins, V.P., Galizzi, M., Salto, M.L., Docampo, R., Moreno, S.N., Developmental expression of a Trypanosoma cruzi phosphoinositide-specific phospholipase C in amastigotes and stimulation of host phosphoinositide hydrolysis (2010) Infect Immun, 78, pp. 4206-4212. , 20643853
  • Frevert, U., Schenkman, S., Nussenzweig, V., Stage-specific expression and intracellular shedding of the cell surface trans-sialidase of Trypanosoma cruzi (1992) Infect Immun, 60, pp. 2349-2360. , 1375197
  • Andrews, N.W., Robbins, E.S., Ley, V., Hong, K.S., Nussenzweig, V., Developmentally regulated, phospholipase C-mediated release of the major surface glycoprotein of amastigotes of Trypanosoma cruzi (1988) J Exp Med, 167, pp. 300-314. , 3279152
  • de Paulo Martins, V., Okura, M., Maric, D., Engman, D.M., Vieira, M., Docampo, R., Acylation-dependent export of Trypanosoma cruzi phosphoinositide-specific phospholipase C to the outer surface of amastigotes (2010) J Biol Chem, 285, pp. 30906-30917. , 20647312, .;:–
  • Salto, M.L., Bertello, L.E., Vieira, M., Docampo, R., Moreno, S.N., de Lederkremer, R.M., Formation and remodeling of inositolphosphoceramide during differentiation of Trypanosoma cruzi from trypomastigote to amastigote (2003) Eukaryot Cell, 2, pp. 756-768. , 12912895
  • Goncalves, M.F., Umezawa, E.S., Katzin, A.M., de Souza, W., Alves, M.J., Zingales, B., Trypanosoma cruzi: shedding of surface antigens as membrane vesicles (1991) Exp Parasitol, 72, pp. 43-53. , 1993464, .;:–
  • de Souza, W., Structural organization of Trypanosoma cruzi (2009) Mem Inst Oswaldo Cruz, 104, pp. 89-100. , 19753463
  • Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C., London, E., Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide (2001) J Biol Chem, 276, pp. 33540-33546. , 11432870
  • Levental, I., Grzybek, M., Simons, K., Raft domains of variable properties and compositions in plasma membrane vesicles (2011) Proc Natl Acad Sci U S A, 108, pp. 11411-11416. , 21709267
  • Gudheti, M.V., Curthoys, N.M., Gould, T.J., Kim, D., Gunewardene, M.S., Gabor, K.A., Actin mediates the nanoscale membrane organization of the clustered membrane protein influenza hemagglutinin (2013) Biophys J, 104, pp. 2182-2192. , 23708358, .;:–
  • Huttner, W.B., Zimmerberg, J., Implications of lipid microdomains for membrane curvature, budding and fission (2001) Curr Opin Cell Biol, 13, pp. 478-484. , 11454455
  • Zimmerberg, J., Kozlov, M.M., How proteins produce cellular membrane curvature (2006) Nat Rev Mol Cell Biol, 7, pp. 9-19. , 16365634
  • McMahon, H.T., Boucrot, E., Membrane curvature at a glance (2015) J Cell Sci, 128, pp. 1065-1070. , 25774051
  • McMahon, H.T., Gallop, J.L., Membrane curvature and mechanisms of dynamic cell membrane remodelling (2005) Nature, 438, pp. 590-596. , 16319878
  • Yu, H., Chokhawala, H., Karpel, R., Wu, B., Zhang, J., Zhang, Y., A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries (2005) J Am Chem Soc, 127, pp. 17618-17619. , 16351087, .;:–
  • Dempsey, G.T., Vaughan, J.C., Chen, K.H., Bates, M., Zhuang, X., Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging (2011) Nat Methods, 8, pp. 1027-1036. , 22056676
  • Thompson, R.E., Larson, D.R., Webb, W.W., Precise nanometer localization analysis for individual fluorescent probes (2002) Biophys J, 82, pp. 2775-2783. , 11964263
  • Egner, A., Geisler, C., von Middendorff, C., Bock, H., Wenzel, D., Medda, R., Fluorescence nanoscopy in whole cells by asynchronous localization of photoswitching emitters (2007) Biophys J, 93, pp. 3285-3290. , 17660318, .;:–
  • Gould, T.J., Verkhusha, V.V., Hess, S.T., Imaging biological structures with fluorescence photoactivation localization microscopy (2009) Nat Protoc, 4, pp. 291-308. , 19214181

Citas:

---------- APA ----------
Lantos, A.B., Carlevaro, G., Araoz, B., Ruiz Diaz, P., Camara, M.D.L.M., Buscaglia, C.A., Bossi, M.,..., Campetella, O. (2016) . Sialic Acid Glycobiology Unveils Trypanosoma cruzi Trypomastigote Membrane Physiology. PLoS Pathogens, 12(4).
http://dx.doi.org/10.1371/journal.ppat.1005559
---------- CHICAGO ----------
Lantos, A.B., Carlevaro, G., Araoz, B., Ruiz Diaz, P., Camara, M.D.L.M., Buscaglia, C.A., et al. "Sialic Acid Glycobiology Unveils Trypanosoma cruzi Trypomastigote Membrane Physiology" . PLoS Pathogens 12, no. 4 (2016).
http://dx.doi.org/10.1371/journal.ppat.1005559
---------- MLA ----------
Lantos, A.B., Carlevaro, G., Araoz, B., Ruiz Diaz, P., Camara, M.D.L.M., Buscaglia, C.A., et al. "Sialic Acid Glycobiology Unveils Trypanosoma cruzi Trypomastigote Membrane Physiology" . PLoS Pathogens, vol. 12, no. 4, 2016.
http://dx.doi.org/10.1371/journal.ppat.1005559
---------- VANCOUVER ----------
Lantos, A.B., Carlevaro, G., Araoz, B., Ruiz Diaz, P., Camara, M.D.L.M., Buscaglia, C.A., et al. Sialic Acid Glycobiology Unveils Trypanosoma cruzi Trypomastigote Membrane Physiology. PLoS Pathog. 2016;12(4).
http://dx.doi.org/10.1371/journal.ppat.1005559