The trans-sialidase, the major Trypanosoma cruzi virulence factor: Three decades of studies

Glycobiology

Volumn 25, Issue 11, 2015, Pages 1142-1149

  Freire De Lima, L ^a   Fonseca, L M ^a   Oeltmann, T ^b   Mendonca Previato L ^a   Previato, J O ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

chagas disease; glycoimmunology; sialic acid; trans sialidase; Trypanosoma cruzi

Indexed keywords

SIALIC ACID; TRANS SIALIDASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; GLYCOPROTEIN; PROTOZOAL PROTEIN; SIALIDASE; TRANS-SIALIDASE;

BIOLOGICAL ACTIVITY; CD8+ T LYMPHOCYTE; CELL CONTACT; CHAGAS DISEASE; CONTROLLED STUDY; HOST; IMMUNE SYSTEM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TRYPANOSOMA CRUZI; ANIMAL; ENZYMOLOGY; HUMAN; IMMUNOLOGY; PARASITOLOGY; PATHOGENICITY;

ANIMALS; CHAGAS DISEASE; GLYCOPROTEINS; HUMANS; NEURAMINIDASE; PROTOZOAN PROTEINS; TRYPANOSOMA CRUZI; VIRULENCE FACTORS;

EID: 84946147687     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwv057     Document Type: Review

References (96)

1. Alcantara-Neves NM, Pontes-de-Carvalho LC. 1995. Circulating transsialidase activity and trans-sialidase-inhibiting antibodies in Trypanosoma cruzi-infected mice. Parasitol Res. 81:560-564.
2. Alvarez P, Buscaglia CA, Campetella O. 2004. Improving protein pharmacokinetics by genetic fusion to simple amino acid sequences. J Biol Chem. 279:3375-3381.
3. Amaya MF, Watts AG, Damager I, Wehenkel A, Nguyen T, Buschiazzo A, Paris G, Frasch AC, Withers SG, Alzari PM. 2004. Structural insights into the catalytic mechanism of Trypanosoma cruzi trans-sialidase. Structure. 12:775-784.
4. Amon R, Reuven EM, Leviatan Ben-Arye S, Padler-Karavani V. 2014. Glycans in immune recognition and response. Carbohydr Res. 389:115-122.
5. Angata K, Fukuda M. 2010. Roles of polysialic acid in migration and differentiation of neural stem cells. Methods Enzymol. 479:25-36.
6. Argibay PF, Di Noia JM, Hidalgo A, Mocetti E, Barbich M, Lorenti AS, Bustos D, Tambutti M, Hyon SH, Frasch AC, et al. 2002. Trypanosoma cruzi surface mucin TcMuc-e2 expressed on higher eukaryotic cells induces human T cell anergy, which is reversible. Glycobiology. 12:25-32.
7. Aridgides D, Salvador R, PereiraPerrin M. 2013. Trypanosoma cruzi coaxes cardiac fibroblasts into preventing cardiomyocyte death by activating nerve growth factor receptor TrkA. PLoS ONE. 8:e57450.
8. Azuma Y, Taniguchi A, Matsumoto K. 2000. Decrease in cell surface sialic acid in etoposide-treated Jurkat cells and the role of cell surface sialidase. Glycoconj J. 17:301-306.
9. Barrias ES, de Carvalho TM, De SouzaW. 2013. Trypanosoma cruzi: Entry into mammalian host cells and parasitophorous vacuole formation. Front Immunol. 4:186.
10. Begum-Haque S, Haque A, Kasper LH. 2009. Apoptosis in Toxoplasma gondii activated T cells: The role of IFNgamma in enhanced alteration of Bcl-2 expression and mitochondrial membrane potential. Microb Pathog. 47:281-288.
11. Bermejo DA, Jackson SW, Gorosito-Serran M, Acosta-Rodriguez EV, Amezcua-Vesely MC, Sather BD, Singh AK, Khim S, Mucci J, Liggitt D, et al. 2013. Trypanosoma cruzi trans-sialidase initiates a program independent of the transcription factors RORgammat and Ahr that leads to IL-17 production by activated B cells. Nat Immunol. 14:514-522.
12. Brandt B, Abou-Eladab EF, Tiedge M, Walzel H. 2010. Role of the JNK/c-Jun/AP-1 signaling pathway in galectin-1-induced T-cell death. Cell Death Dis. 1:e23.
13. Buchini S, Buschiazzo A, Withers SG. 2008. A new generation of specific Trypanosoma cruzi trans-sialidase inhibitors. Angew Chem Int Ed Engl. 47:2700-2703.
14. Burgos JM, Risso MG, Breniere SF, Barnabe C, Campetella O, Leguizamon MS. 2013. Differential distribution of genes encoding the virulence factor transsialidase along Trypanosoma cruzi discrete typing units. PLoS ONE. 8: e58967.
15. Burleigh BA, Andrews NW. 1995. The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Annu Rev Microbiol. 49:175-200.
16. Buschiazzo A, Amaya MF, Cremona ML, Frasch AC, Alzari PM. 2002. The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Mol Cell. 10:757-768.
17. Buschiazzo A, Muia R, Larrieux N, Pitcovsky T, Mucci J, Campetella O. 2012. Trypanosoma cruzi trans-sialidase in complex with a neutralizing antibody: Structure/function studies towards the rational design of inhibitors. PLoS Pathog. 8:e1002474.
18. Buschiazzo A, Tavares GA, Campetella O, Spinelli S, Cremona ML, Paris G, Amaya MF, Frasch AC, Alzari PM. 2000. Structural basis of sialyltransferase activity in trypanosomal sialidases. EMBO J. 19:16-24.
19. Butler CE, de Carvalho TM, Grisard EC, Field RA, Tyler KM. 2013. Transsialidase stimulates eat me response from epithelial cells. Traffic. 14:853-869.
20. Caradonna KL, Burleigh BA. 2011. Mechanisms of host cell invasion by Trypanosoma cruzi. Adv Parasitol. 76:33-61.
21. Carvalho ST, Sola-Penna M, Oliveira IA, Pita S, Goncalves AS, Neves BC, Sousa FR, Freire-de-Lima L, Kurogochi M, Hinou H, et al. 2010. A new class of mechanism-based inhibitors for Trypanosoma cruzi trans-sialidase and their influence on parasite virulence. Glycobiology. 20:1034-1045.
22. Chang YC, Nizet V. 2014. The interplay between Siglecs and sialylated pathogens. Glycobiology. 24:818-825.
23. Chen GY, Brown NK, Zheng P, Liu Y. 2014. Siglec-G/10 in self-nonself discrimination of innate and adaptive immunity. Glycobiology. 24:800-806.
24. Chen X, Varki A. 2010. Advances in the biology and chemistry of sialic acids. ACS Chem Biol. 5:163-176.
25. Chuenkova M, Pereira ME. 1995. Trypanosoma cruzi trans-sialidase: Enhancement of virulence in a murine model of Chagas' disease. J Exp Med. 181:1693-1703.
26. Chuenkova MV, PereiraPerrin M. 2004. Chagas' disease parasite promotes neuron survival and differentiation through TrkA nerve growth factor receptor. J Neurochem. 91:385-394.
27. Chuenkova MV, PereiraPerrin M. 2005. A synthetic peptide modeled on PDNF, Chagas' disease parasite neurotrophic factor, promotes survival and differentiation of neuronal cells through TrkA receptor. Biochemistry. 44:15685-15694.
28. Chuenkova MV, Pereiraperrin M. 2011. Neurodegeneration and neuroregeneration in Chagas disease. Adv Parasitol. 76:195-233.
29. Cohen M, Varki A. 2010. The sialome-far more than the sum of its parts. OMICS. 14:455-464.
30. Cremona ML, Sanchez DO, Frasch AC, Campetella O. 1995. A single tyrosine differentiates active and inactive Trypanosoma cruzi trans-sialidases. Gene. 160:123-128.
31. Crespo HJ, Cabral MG, Teixeira AV, Lau JT, Trindade H, Videira PA. 2009. Effect of sialic acid loss on dendritic cell maturation. Immunology. 128: e621-e631.
32. Dc-Rubin SS, Schenkman S. 2012. T rypanosoma cruzi trans-sialidase as a multifunctional enzyme in Chagas' disease. Cell Microbiol. 14: 1522-1530.
33. de Melo-Jorge M, PereiraPerrin M. 2007. The Chagas' disease parasite Trypanosoma cruzi exploits nerve growth factor receptor TrkA to infect mammalian hosts. Cell Host Microbe. 1:251-261.
34. de Souza W, de Carvalho TM. 2013. Active penetration of Trypanosoma cruzi into host cells:Historical considerations and current concepts. Front Immunol. 4:2.
35. de SouzaW, de Carvalho TM, Barrias ES. 2010. Review on Trypanosoma cruzi: Host cell interaction. Int J Cell Biol. 2010:1-18.
36. de Titto EH, Araujo FG. 1988. Serum neuraminidase activity and hematological alterations in acute human Chagas' disease. Clin Immunol Immunopathol. 46:157-161.
37. DosReis GA. 2011. Evasion of immune responses by Trypanosoma cruzi, the etiological agent of Chagas disease. Braz J Med Biol Res. 44:84-90.
38. Bouhdidi A, Truyens C, RiveraMT, Bazin H, Carlier Y. 1994. Trypanosoma cruzi infection in mice induces a polyisotypic hypergammaglobulinaemia and parasite-specific response involving high IgG2a concentrations and highly avid IgG1 antibodies. Parasite Immunol. 16:69-76.
39. Francelin C, Paulino LC, Gameiro J, Verinaud L. 2011. Effects of Plasmodium berghei on thymus: High levels of apoptosis and premature egress of CD4(+) CD8(+) thymocytes in experimentally infected mice. Immunobiology. 216:1148-1154.
40. Frasch AC. 1994. Trans-sialidase, SAPA amino acid repeats and the relationship between Trypanosoma cruzi and the mammalian host. Parasitology. 108 Suppl.:S37-S44.
41. Frasch AC. 2000. Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol Today. 16:282-286.
42. Freire-de-Lima L, Alisson-Silva F, Carvalho ST, Takiya CM, Rodrigues MM, DosReis GA, Mendonca-Previato L, Previato JO, Todeschini AR. 2010. Trypanosoma cruzi subverts host cell sialylation and may compromise antigen-specific CD8+ T cell responses. J Biol Chem. 285:13388-13396.
43. Galvan M, Murali-Krishna K, Ming LL, Baum L, Ahmed R. 1998. Alterations in cell surface carbohydrates on T cells from virally infected mice can distinguish effector/memory CD8+ T cells from naive cells. J Immunol. 161:641-648.
44. Gao W, Pereira MA. 2001. Trypanosoma cruzi trans-sialidase potentiates T cell activation through antigen-presenting cells: Role of IL-6 and Bruton's tyrosine kinase. Eur J Immunol. 31:1503-1512.
45. Gao W, Wortis HH, Pereira MA. 2002. The Trypanosoma cruzi trans-sialidase is a T cell-independent B cell mitogen and an inducer of non-specific Ig secretion. Int Immunol. 14:299-308.
46. Ghrici M, El Zowalaty M, Omar AR, Ideris A. 2013. Induction of apoptosis in MCF-7 cells by the hemagglutinin-neuraminidase glycoprotein of Newcastle disease virus Malaysian strain AF2240. Oncol Rep. 30: 1035-1044.
47. Hedlund M, Aschenbrenner LM, Jensen K, Larson JL, Fang F. 2010. Sialidasebased anti-influenza virus therapy protects against secondary pneumococcal infection. J Infect Dis. 201:1007-1015.
48. Hinou H, Kurogochi M, Shimizu H, Nishimura S. 2005. Characterization of Vibrio cholerae neuraminidase by a novel mechanism-based fluorescent labeling reagent. Biochemistry. 44:11669-11675.
49. Lee YK, Lin TH, Chang CF, Lo YL. 2013. Galectin-3 silencing inhibits epirubicin-induced ATP binding cassette transporters and activates the mitochondrial apoptosis pathway via beta-catenin/GSK-3beta modulation in colorectal carcinoma. PLoS ONE. 8:e82478.
50. Leguizamon MS, Mocetti E, Garcia Rivello H, Argibay P, Campetella O. 1999. Trans-sialidase from Trypanosoma cruzi induces apoptosis in cells from the immune system in vivo. J Infect Dis. 180:1398-1402.
51. Lepletier A, de Frias Carvalho V, Morrot A, SavinoW. 2012. Thymic atrophy in acute experimental Chagas disease is associated with an imbalance of stress hormones. Ann N Y Acad Sci. 1262:45-50.
52. Lieke T, Grobe D, Blanchard V, Grunow D, Tauber R, Zimmermann-Kordmann M, Jacobs T, Reutter W. 2011. Invasion of Trypanosoma cruzi into host cells is impaired by N-propionylmannosamine and other N-acylmannosamines. Glycoconj J. 28:31-37.
53. Mendoncą-Previato L, Penha L, Garcez TC, Jones C, Previato JO. 2013. Addition of alpha-O-GlcNAc to threonine residues define the post-translational modification of mucin-like molecules in Trypanosoma cruzi. Glycoconj J. 30:659-666.
54. Mendoncą-Previato L, Todeschini AR, de Lima LF, Previato JO. 2010. The trans-sialidase from Trypanosoma cruzi a putative target for trypanocidal agents. Open Parasitol J. 4:111-115.
55. Moody AM, Chui D, Reche PA, Priatel JJ, Marth JD, Reinherz EL. 2001. Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell. 107:501-512.
56. Morrot A, Barreto de Albuquerque J, Berbert LR, de Carvalho Pinto CE, de Meis J, Savino W. 2012. Dynamics of lymphocyte populations during Trypanosoma cruzi infection: From thymocyte depletion to differential cell expansion/contraction in peripheral lymphoid organs. J Trop Med. 2012:747185.
57. Mucci J, Hidalgo A, Mocetti E, Argibay PF, Leguizamon MS, Campetella O. 2002. Thymocyte depletion in Trypanosoma cruzi infection is mediated by trans-sialidase-induced apoptosis on nurse cells complex. Proc Natl Acad Sci USA. 99:3896-3901.
58. Mucci J, Mocetti E, Leguizamon MS, Campetella O. 2005. A sexual dimorphism in intrathymic sialylation survey is revealed by the trans-sialidase from Trypanosoma cruzi. J Immunol. 174:4545-4550.
59. Mucci J, Risso MG, Leguizamon MS, Frasch AC, Campetella O. 2006. The trans-sialidase from Trypanosoma cruzi triggers apoptosis by target cell sialylation. Cell Microbiol. 8:1086-1095.
60. Muia RP, Yu H, Prescher JA, Hellman U, Chen X, Bertozzi CR, Campetella O. 2010. Identification of glycoproteins targeted by Trypanosoma cruzi transsialidase, a virulence factor that disturbs lymphocyte glycosylation. Glycobiology. 20:833-842.
61. Neu U, Bauer J, Stehle T. 2011. Viruses and sialic acids: Rules of engagement. Curr Opin Struct Biol. 21:610-618.
62. Nishikawa Y, Ogiso A, Kameyama K, Nishimura M, Xuan X, Ikehara Y. 2013. Alpha2-3 sialic acid glycoconjugate loss and its effect on infection with Toxoplasma parasites. Exp Parasitol. 135:479-485.
63. Ostberg JR, Barth RK, Frelinger JG. 1998. The Roman god Janus: A paradigm for the function of CD43. Immunol Today. 19:546-550.
64. Pappu BP, Shrikant PA. 2004. Alteration of cell surface sialylation regulates antigen-induced naive CD8+ T cell responses. J Immunol. 173: 275-284.
65. Paris G, Ratier L, Amaya MF, Nguyen T, Alzari PM, Frasch AC. 2005. A sialidase mutant displaying trans-sialidase activity. J Mol Biol. 345:923-934.
66. Parodi AJ, Pollevick GD, Mautner M, Buschiazzo A, Sanchez DO, Frasch AC. 1992. Identification of the gene(s) coding for the trans-sialidase of Trypanosoma cruzi. EMBO J. 11:1705-1710.
67. Pereira ME. 1983. A developmentally regulated neuraminidase activity in Trypanosoma cruzi. Science. 219:1444-1446.
68. Pereira ME, Loures MA, Villalta F, Andrade AF. 1980. Lectin receptors as markers for Trypanosoma cruzi. Developmental stages and a study of the interaction of wheat germ agglutinin with sialic acid residues on epimastigote cells. J Exp Med. 152:1375-1392.
69. Pereira ME, Mejia JS, Ortega-Barria E, Matzilevich D, Prioli RP. 1991. The Trypanosoma cruzi neuraminidase contains sequences similar to bacterial neuraminidases, YWTD repeats of the low density lipoprotein receptor, and type III modules of fibronectin. J Exp Med. 174:179-191.
70. Previato JO, Andrade AF, Pessolani MC, Mendonca-Previato L. 1985. Incorporation of sialic acid into Trypanosoma cruzi macromolecules. A proposal for a new metabolic route. Mol Biochem Parasitol. 16:85-96.
71. Previato J, Andrade A, Vermelho A, Firmino J, Mendoncą-Previato L. 1990. Evidence for N-glycolylneuraminic acid incorporation by Trypanosoma cruzi from infected animal. Mem Inst Oswaldo Cruz. 85:38-39.
72. Priatel JJ, Chui D, Hiraoka N, Simmons CJ, Richardson KB, Page DM, Fukuda M, Varki NM, Marth JD. 2000. The ST3Gal-I sialyltransferase controls CD8+ T lymphocyte homeostasis by modulating O-glycan biosynthesis. Immunity. 12:273-283.
73. Ribeirao M, Pereira-Chioccola VL, Eichinger D, Rodrigues MM, Schenkman S. 1997. Temperature differences for trans-glycosylation and hydrolysis reaction reveal an acceptor binding site in the catalytic mechanism of Trypanosoma cruzi trans-sialidase. Glycobiology. 7:1237-1246.
74. Risso MG, Garbarino GB, Mocetti E, Campetella O, Gonzalez Cappa SM, Buscaglia CA, Leguizamon MS. 2004. Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages. J Infect Dis. 189:2250-2259.
75. Rubin-de-Celis SS, Uemura H, Yoshida N, Schenkman S. 2006. Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell Microbiol. 8:1888-1898.
76. Ruiz Diaz P, Mucci J, Meira MA, Bogliotti Y, Musikant D, Leguizamon MS, Campetella O. 2015. Trypanosoma cruzi trans-sialidase prevents elicitation of Th1 cell response via interleukin 10 and downregulates Th1 effector cells. Infect Immun. 83:2099-2108.
77. Sadighi Akha AA, Berger SB, Miller RA. 2006. Enhancement of CD8 T-cell function through modifying surface glycoproteins in young and old mice. Immunology. 119:187-194.
78. Savino W. 2006. The thymus is a common target organ in infectious diseases. PLoS Pathog. 2:e62.
79. Schauer R, Reuter G, Muhlpfordt H, Andrade AF, Pereira ME. 1983. The occurrence of N-acetyl-and N-glycoloylneuraminic acid in Trypanosoma cruzi. Hoppe Seylers Z Physiol Chem. 364:1053-1057.
80. Schenkman S, Jiang MS, Hart GW, Nussenzweig V. 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.
81. Schenkman RP, Vandekerckhove F, Schenkman S. 1993. Mammalian cell sialic acid enhances invasion by Trypanosoma cruzi. Infect Immun. 61:898-902.
82. Todeschini AR, Dias WB, Girard MF, Wieruszeski JM, Mendoncą-Previato L, Previato JO. 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.
83. Todeschini AR, Girard MF, Wieruszeski JM, Nunes MP, DosReis GA, Mendoncą-Previato L, Previato JO. 2002a. trans-Sialidase from Trypanosoma cruzi binds host T-lymphocytes in a lectin manner. J Biol Chem. 277:45962-45968.
84. Todeschini AR, Nunes MP, Pires RS, Lopes MF, Previato JO, Mendoncą-Previato L, DosReis GA. 2002b. Costimulation of host T lymphocytes by a trypanosomal trans-sialidase: Involvement of CD43 signaling. J Immunol. 168:5192-5198.
85. Traving C, Schauer R. 1998. Structure, function and metabolism of sialic acids. Cell Mol Life Sci. 54:1330-1349.
86. Tribulatti MV, Mucci J, Cattaneo V, Aguero F, Gilmartin T, Head SR, Campetella O. 2007. Galectin-8 induces apoptosis in the CD4(high) CD8(high) thymocyte subpopulation. Glycobiology. 17:1404-1412.
87. Tribulatti MV, Mucci J, Van Rooijen N, Leguizamon MS, Campetella O. 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.
88. Tringali C, Lupo B, Anastasia L, Papini N, Monti E, Bresciani R, Tettamanti G, Venerando B. 2007. Expression of sialidase Neu2 in leukemic K562 cells induces apoptosis by impairing Bcr-Abl/Src kinases signaling. J Biol Chem. 282:14364-14372.
89. Uemura H, Schenkman S, Nussenzweig V, Eichinger D. 1992. Only some members of a gene family in Trypanosoma cruzi encode proteins that express both trans-sialidase and neuraminidase activities. EMBO J. 11:3837-3844.
90. Varki A, Gagneux P. 2012. Multifarious roles of sialic acids in immunity. AnnN Y Acad Sci. 1253:16-36.
91. Varki A, Schauer R. 2009. Sialic acids. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of Glycobiology. Cold Spring Harbor (NY).
92. Watts AG, Damager I, Amaya ML, Buschiazzo A, Alzari P, Frasch AC, Withers SG. 2003. Trypanosoma cruzi trans-sialidase operates through a covalent sialyl-enzyme intermediate: Tyrosine is the catalytic nucleophile. J Am Chem Soc. 125:7532-7533.
93. Wiggins R, Hicks SJ, Soothill PW, Millar MR, Corfield AP. 2001. Mucinases and sialidases: Their role in the pathogenesis of sexually transmitted infections in the female genital tract. Sex Transm Infect. 77:402-408.
94. Woronowicz A, De Vusser K, Laroy W, Contreras R, Meakin SO, Ross GM, Szewczuk MR. 2004. Trypanosome trans-sialidase targets TrkA tyrosine kinase receptor and induces receptor internalization and activation. Glycobiology. 14:987-998.
95. Wu W, Harley PH, Punt JA, Sharrow SO, Kearse KP. 1996. Identification of CD8 as a peanut agglutinin (PNA) receptor molecule on immature thymocytes. J Exp Med. 184:759-764.
96. Zingales B, Carniol C, de Lederkremer RM, Colli W. 1987. Direct sialic acid transfer from a protein donor to glycolipids of trypomastigote forms of Trypanosoma cruzi. Mol Biochem Parasitol. 26:135-144.