Trichomonas vaginalis lipophosphoglycan exploits binding to galectin-1 and -3 to modulate epithelial immunity

Journal of Biological Chemistry

Volumn 291, Issue 2, 2016, Pages 998-1013

  Fichorova, Raina N ^a   Yamamoto, Hidemi S ^a   Fashemi, Titilayo ^a   Foley, Evan ^a   Ryan, Stanthia ^a   Beatty, Noah ^a   Dawood, Hassan ^a   Hayes, Gary R ^b   St Pierre, Guillaume ^c   Sato, Sachiko ^c   Singh, Bibhuti N ^b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; PROTOZOA; T-CELLS;

ADAPTIVE IMMUNITY; CHEMOKINE EXPRESSION; EXTRACELLULAR LEVELS; MOLECULAR MECHANISM; PARASITIC INFECTIONS; PATHOGEN RECOGNITION; PROTOZOAN PARASITES; SEXUALLY TRANSMITTED INFECTIONS;

BINS;

CHEMOKINE; GALECTIN 1; GALECTIN 3; INTERLEUKIN 8; LIPOPHOSPHOGLYCAN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; RANTES; SMALL INTERFERING RNA; GLYCOSPHINGOLIPID; PROTEIN BINDING; RECOMBINANT PROTEIN;

ADAPTIVE IMMUNITY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; INNATE IMMUNITY; NONHUMAN; PARASITE SURVIVAL; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRICHOMONAS VAGINALIS; TRICHOMONIASIS; UTERINE CERVIX EPITHELIUM; VAGINA EPITHELIUM; BIOLOGICAL MODEL; CELL LINE; GENE SILENCING; IMMUNE EVASION; IMMUNITY; IMMUNOLOGY; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MUTATION; PARASITOLOGY; PATHOLOGY; SOLUBILITY; UTERINE CERVIX; VAGINA;

CELL LINE; CERVIX UTERI; CHEMOKINES; EPITHELIAL CELLS; FEMALE; GALECTIN 1; GALECTIN 3; GENE KNOCKDOWN TECHNIQUES; GLYCOSPHINGOLIPIDS; HUMANS; IMMUNE EVASION; IMMUNITY; KINETICS; MODELS, BIOLOGICAL; MUTATION; PROTEIN BINDING; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SOLUBILITY; TRICHOMONAS VAGINALIS; VAGINA;

EID: 84954091555     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.651497     Document Type: Article

References (63)

1. World Health Organization (2012) Global incidence and prevalence of selected curable sexually transmitted infections-2008. World Health Organization, Geneva, Switzerland, http://apps.who.int/iris/bitstream/10665/75181/1/9789241503839-eng.pdf
2. Fichorova, R. N. (2009) Impact of T. vaginalis infection on innate immune responses and reproductive outcome. J. Reprod. Immunol. 83, 185-189
3. Nyame, A. K., Kawar, Z. S., and Cummings, R. D. (2004) Antigenic glycans in parasitic infections: implications for vaccines and diagnostics. Arch. Biochem. Biophys. 426, 182-200
4. Turco, S. J., and Descoteaux, A. (1992) The lipophosphoglycan of Leishmania parasites. Annu. Rev. Microbiol. 46, 65-94
5. Ferguson, M. A. (1999) The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J. Cell Sci. 112, 2799-2809
6. Guha-Niyogi, A., Sullivan, D. R., and Turco, S. J. (2001) Glycoconjugate structures of parasitic protozoa. Glycobiology 11, 45R-59R
7. Singh, B. N., Beach, D. H., Lindmark, D. G., and Costello, C. E. (1994) Identification of the lipid moiety and further characterization of the novel lipophosphoglycan-like glycoconjugates of Trichomonas vaginalis and Trichomonas foetus. Arch. Biochem. Biophys. 309, 273-280
8. Singh, B. N. (1993) Lipophosphoglycan-like glycoconjugate of Trichomonas foetus and Trichomonas vaginalis. Mol. Biochem. Parasitol. 57, 281-294
9. Fichorova, R. N., Trifonova, R. T., Gilbert, R. O., Costello, C. E., Hayes, G. R., Lucas, J. J., and Singh, B. N. (2006) Trichomonas vaginalis lipophosphoglycan triggers a selective upregulation of cytokines by human female reproductive tract epithelial cells. Infect. Immun. 74, 5773-5779
10. Huppert, J. S., Huang, B., Chen, C., Dawood, H. Y., and Fichorova, R. N. (2013) Clinical evidence for the role of Trichomonas vaginalis in regulation of secretory leukocyte protease inhibitor in the female genital tract. J. Infect. Dis. 207, 1462-1470
11. Fichorova, R. N., Lee, Y., Yamamoto, H. S., Takagi, Y., Hayes, G. R., Goodman, R. P., Chepa-Lotrea, X., Buck, O. R., Murray, R., Kula, T., Beach, D. H., Singh, B. N., and Nibert, M. L. (2012) Endobiont viruses sensed by the human host-beyond conventional antiparasitic therapy. PLoS One 7, e48418
12. Singh, B. N., Hayes, G. R., Lucas, J. J., Sommer, U., Viseux, N., Mirgorodskaya, E., Trifonova, R. T., Sassi, R. R., Costello, C. E., and Fichorova, R. N. (2009) Structural details and composition of Trichomonas vaginalis lipophosphoglycan in relevance to the epithelial immune function. Glyco-conj. J. 26, 3-17
13. Fichorova, R. N., Buck, O. R., Yamamoto, H. S., Fashemi, T., Dawood, H. Y., Fashemi, B., Hayes, G. R., Beach, D. H., Takagi, Y., Delaney, M. L., Nibert, M. L., Singh, B. N., and Onderdonk, A. B. (2013) The Villain Team-Up or how Trichomonas vaginalis and bacterial vaginosis alter innate immunity in concert. Sex. Transm. Infect. 89, 460-466
14. Elola, M. T., Wolfenstein-Todel, C., Troncoso, M. F., Vasta, G. R., and Rabinovich, G. A. (2007) Galectins: matricellular glycan-binding proteins linking cell adhesion, migration, and survival. Cell. Mol. Life Sci. 64, 1679-1700
15. Sato, S., St-Pierre, C., Bhaumik, P., and Nieminen, J. (2009) Galectins in innate immunity: dual functions of host soluble β-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol. Rev. 230, 172-187
16. Sato, S., Bhaumik, P., St-Pierre, G., and Pelletier, I. (2014) Role of galectin-3 in the initial control of Leishmania infection. Crit. Rev. Immunol. 34, 147-175
17. Okumura, C. Y., Baum, L. G., and Johnson, P. J. (2008) Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis. Cell. Microbiol. 10, 2078-2090
18. Rabinovich, G. A., and Gruppi, A. (2005) Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunol. 27, 103-114
19. Stowell, S. R., Qian, Y., Karmakar, S., Koyama, N. S., Dias-Baruffi, M., Leffler, H., McEver, R. P., and Cummings, R. D. (2008) Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J. Immunol. 180, 3091-3102
20. Gilbert, R. O., Elia, G., Beach, D. H., Klaessig, S., and Singh, B. N. (2000) Cytopathogenic effect of Trichomonas vaginalis on human vaginal epithelial cells cultured in vitro. Infect. Immun. 68, 4200-4206
21. Bhaumik, P., St-Pierre, G., Milot, V., St-Pierre, C., and Sato, S. (2013) Galectin-3 facilitates neutrophil recruitment as an innate immune response to a parasitic protozoa cutaneous infection. J. Immunol. 190, 630-640
22. Nieminen, J., St-Pierre, C., Bhaumik, P., Poirier, F., and Sato, S. (2008) Role of galectin-3 in leukocyte recruitment in a murine model of lung infection by Streptococcus pneumoniae. J. Immunol. 180, 2466-2473
23. St-Pierre, C., Ouellet, M., Tremblay, M. J., and Sato, S. (2010) Galectin-1 and HIV-1 infection. Methods Enzymol. 480, 267-294
24. St-Pierre, C., Manya, H., Ouellet, M., Clark, G. F., Endo, T., Tremblay, M. J., and Sato, S. (2011) Host-soluble galectin-1 promotes HIV-1 replication through a direct interaction with glycans of viral gp120 and host CD4. J. Virol. 85, 11742-11751
25. Pelletier, I., Hashidate, T., Urashima, T., Nishi, N., Nakamura, T., Futai, M., Arata, Y., Kasai K-, Hirashima, M., Hirabayashi, J., and Sato, S. (2003) Specific recognition of Leishmania major poly-β-galactosyl epitopes by galectin-9: possible implication of galectin-9 in interaction between L. major and host cells. J. Biol. Chem. 278, 22223-22230
26. Pelletier, I., and Sato, S. (2002) Specific recognition and cleavage of galectin-3. J. Biol. Chem. 277, 17633-17670
27. Fichorova, R. N., Rheinwald, J. G., and Anderson, D. J. (1997) Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol. Reprod. 57, 847-855
28. Fichorova, R. N., Yamamoto, H. S., Delaney, M. L., Onderdonk, A. B., and Doncel, G. F. (2011) Novel vaginal microflora colonization model providing new insight into microbicide mechanism of action. MBio. 2, e00168-00111
29. Jain, A., Kumar, L., Kushwaha, B., Sharma, M., Pandey, A., Verma, V., Sharma, V., Singh, V., Rawat, T., Sharma, V. L., Maikhuri, J. P., and Gupta, G. (2014) Combining a synthetic spermicide with a natural trichomonacide for safe, prophylactic contraception. Hum. Reprod. 29, 242-252
30. Bastida-Corcuera, F. D., Okumura, C. Y., Colocoussi, A., and Johnson, P. J. (2005) Trichomonas vaginalis lipophosphoglycan mutants have reduced adherence and cytotoxicity to human ectocervical cells. Eukaryot. Cell 4, 1951-1958
31. Lustig, G., Ryan, C. M., Secor, W. E., and Johnson, P. J. (2013) Trichomonas vaginalis contact-dependent cytolysis of epithelial cells. Infect. Immun. 81, 1411-1419
32. Fichorova, R. N., and Anderson, D. J. (1999) Differential expression of immunobiological mediators by immortalized human cervical and vaginal epithelial cells. Biol. Reprod. 60, 508-514
33. Fichorova, R. N., Cronin, A. O., Lien, E., Anderson, D. J., and Ingalls, R. R. (2002) Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of toll-like receptor 4-mediated signaling. J. Immunol. 168, 2424-2432
34. Canny, G. O., Trifonova, R. T., Kindelberger, D. W., Colgan, S. P., and Fichorova, R. N. (2006) Expression and function of bactericidal/permeability-increasing protein in human genital tract epithelial cells. J. Infect. Dis. 194, 498-502
35. Trifonova, R. T., Doncel, G. F., and Fichorova, R. N. (2009) Polyanionic microbicides modify Toll-like receptor-mediated cervicovaginal immune responses. Antimicrob. Agents Chemother. 53, 1490-1500
36. Fichorova, R. N., Bajpai, M., Chandra, N., Hsiu, J. G., Spangler, M., Ratnam, V., and Doncel, G. F. (2004) Interleukin (IL)-1, IL-6, and IL-8 predict mucosal toxicity of vaginal microbicidal contraceptives. Biol. Reprod. 71, 761-769
37. Trifonova, R. T., Pasicznyk, J. M., and Fichorova, R. N. (2006) Biocompatibility of solid-dosage forms of anti-human immunodeficiency virus type 1 microbicides with the human cervicovaginal mucosa modeled ex vivo. Antimicrob. Agents Chemother. 50, 4005-4010
38. Fichorova, R. N., Richardson-Harman, N., Alfano, M., Belec, L., Carbonneil, C., Chen, S., Cosentino, L., Curtis, K., Dezzutti, C. S., Donoval, B., Doncel, G. F., Donaghay, M., Grivel, J. C., Guzman, E., Hayes, M., et al. (2008) Biological and technical variables affecting immunoassay recovery of cytokines from human serum and simulated vaginal fluid: a multicenter study. Anal. Chem. 80, 4741-4751
39. Ahmad, N., Gabius, H.-J., André, S., Kaltner, H., Sabesan, S., Roy, R., Liu, B., Macaluso, F., and Brewer, C. F. (2004) Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J. Biol. Chem. 279, 10841-10847
40. Stowell, S. R., Arthur, C. M., Mehta, P., Slanina, K. A., Blixt, O., Leffler, H., Smith, D. F., and Cummings, R. D. (2008) Galectin-1,-2, and-3 exhibit differential recognition of sialylated glycans and blood group antigens. J. Biol. Chem. 283, 10109-10123
41. Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hirashima, M., Urashima, T., Oka, T., Futai, M., Muller, W. E., Yagi, F., and Kasai, K. (2002) Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim. Biophys. Acta 1572, 232-254
42. Merkle, R. K., and Cummings, R. D. (1987) Relationship of the terminal sequences to the length of poly-N-acetyllactosamine chains in asparaginelinked oligosaccharides from the mouse lymphoma cell line BW5147. Immobilized tomato lectin interacts with high affinity with glycopeptides containing long poly-N-acetyllactosamine chains. J. Biol. Chem. 262, 8179-8189
43. Sato, S., and Hughes, R. C. (1994) Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J. Biol. Chem. 269, 4424-4430
44. Appay, V., and Rowland-Jones, S. L. (2001) RANTES: a versatile and controversial chemokine. Trends Immunol. 22, 83-87
45. Barondes, S. H., Castronovo, V., Cooper, D. N., Cummings, R. D., Drickamer, K., Feizi, T., Gitt, M. A., Hirabayashi, J., Hughes, C., and Kasai, K. (1994) Galectins: a family of animalβ-galactoside-binding lectins. Cell 76, 597-598
46. Rabinovich, G. A., and Toscano, M. A. (2009) Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 9, 338-352
47. Vasta, G. R. (2009) Roles of galectins in infection. Nat. Rev. Microbiol. 7, 424-438
48. Blois, S. M., and Barrientos, G. (2014) Galectin signature in normal pregnancy and preeclampsia. J. Reprod. Immunol. 101, 127-134
49. Demmert, M., Faust, K., Bohlmann, M. K., Tröger, B., Göpel, W., Herting, E., and Härtel, C. (2012) Galectin-3 in cord blood of term and preterm infants. Clin. Exp. Immunol. 167, 246-251
50. Nio-Kobayashi, J., and Iwanage, T. (2010) Specific recognition and cleav-age of galectin-3 by Leishmania major through species-specific polygalactose epitope. Kaibougaku Zasshi 85, 58
51. Liu, F. T., and Rabinovich, G. A. (2010) Galectins: regulators of acute and chronic inflammation. Ann. N.Y. Acad. Sci. 1183, 158-182
52. Chen, H. Y., Weng, I. C., Hong, M. H., and Liu, F. T. (2014) Galectins as bacterial sensors in the host innate response. Curr. Opin. Microbiol. 17, 75-81
53. Paz, I., Sachse, M., Dupont, N., Mounier, J., Cederfur, C., Enninga, J., Leffler, H., Poirier, F., Prevost, M. C., Lafont, F., and Sansonetti, P. (2010) Galectin-3, a marker for vacuole lysis by invasive pathogens. Cell. Microbiol. 12, 530-544
54. Maier, O., Marvin, S. A., Wodrich, H., Campbell, E. M., and Wiethoff, C. M. (2012) Spatiotemporal dynamics of adenovirus membrane rupture and endosomal escape. J. Virol. 86, 10821-10828
55. Sano, H., Hsu, D. K., Apgar, J. R., Yu, L., Sharma, B. B., Kuwabara, I., Izui, S., and Liu, F. T. (2003) Critical role of galectin-3 in phagocytosis by macrophages. J. Clin. Invest. 112, 389-397
56. Farnworth, S. L., Henderson, N. C., Mackinnon, A. C., Atkinson, K. M., Wilkinson, T., Dhaliwal, K., Hayashi, K., Simpson, A. J., Rossi, A. G., Haslett, C., and Sethi, T. (2008) Galectin-3 reduces the severity of pneumococcal pneumonia by augmenting neutrophil function. Am. J. Pathol. 172, 395-405
57. Sato, S., Ouellet, M., St-Pierre, C., and Tremblay, M. J. (2012) Glycans, galectins, and HIV-1 infection. Ann. N.Y. Acad. Sci. 1253, 133-148
58. Thurston, T. L., Wandel, M. P., von Muhlinen, N., Foeglein, A., and Randow, F. (2012) Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414-418
59. van der Leij, J., van den Berg, A., Blokzijl, T., Harms, G., van Goor, H., Zwiers, P., van Weeghel, R., Poppema, S., and Visser, L. (2004) Dimeric galectin-1 induces IL-10 production in T-lymphocytes: an important tool in the regulation of the immune response. J. Pathol. 204, 511-518
60. Cooper, D., Iqbal, A. J., Gittens, B. R., Cervone, C., and Perretti, M. (2012) The effect of galectins on leukocyte trafficking in inflammation: sweet or sour? Ann. N.Y. Acad. Sci. 1253, 181-192
61. van Kooyk, Y., and Rabinovich, G. A. (2008) Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 9, 593-601
62. Almkvist, J., Dahlgren, C., Leffler, H., and Karlsson, A. (2002) Activation of the neutrophil nicotinamide adenine dinucleotide phosphate oxidase by galectin-1. J. Immunol. 168, 4034-4041
63. Li, Y., Komai-Koma, M., Gilchrist, D. S., Hsu, D. K., Liu, F.-T., Springall, T., and Xu, D. (2008) Galectin-3 is a negative regulator of lipopolysaccharidemediated inflammation. J. Immunol. 181, 2781-2789