Abstract
Zinc (Zn) is a common essential component for all organisms because this metal serves as a cofactor or structural element for enzymes and metalloproteins involved in several important biological processes. However, excess levels of Zn can be toxic, as a consequence, the cells have evolved homeostatic mechanisms to regulate intracellular levels of this trace mineral. Zinc efflux and sequestration into internal cellular compartments from cells are mediated, in large part, by the ZNT/SLC30 proteins, which belong to the CDF family of ion transporters. The CDF family has evolved in prokaryotes and has been reported in several organisms, such as fungi, plants, and animals. Zn has been shown to regulate expression of proteins involved in metabolism and pathogenicity mechanisms in the protozoan pathogenTrichomonas vaginalis, in contrast high concentrations of this element were also found to be toxic forT. vaginalis trophozoites. Until now, Zn homeostasis mechanisms are not yet clear in this parasite. We performed a genome-wide analysis and localized eight members of the CDF gene family inT. vaginalis (TvCDF1-8). With the use of in silico analyses, the TvCDF protein sequences revealed high conservation and show similar properties to the reported in other CDF orthologs. We analyzed the expression patterns ofTvCDF1-8 transcripts in trophozoites growth under high zinc concentrations, which showed down-regulation in expression. These results indicate thatTvCDF genes encode membrane transporters and strongly supported their identity as members of CDF-like gene family, and further suggest the function in Zn efflux and sequestration inT. vaginalis.
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References
Maret W (2013) Zinc and the zinc proteome. In: Banci L (ed) Metallomics and the cell. Springer, Dordrecht, pp 479–501
Prashanth L, Kattapagari KK, Chitturi RT, Baddam VRR, Prasad LK (2015) A review on role of essential trace elements in health and disease. J NTR Univ Health Sci 4(2):75
Blindauer CA (2015) Advances in the molecular understanding of biological zinc transport. Chem Commun 51(22):4544–4563
Wang D, Fierke CA (2013) The BaeSR regulon is involved in defense against zinc toxicity inE. coli. Metallomics 5:372–383
Abu Kwaik Y, Bumann D (2013) Microbial quest for food in vivo: ‘nutritional virulence’as an emerging paradigm. Cell Microbiol 15(6):882–890
Cerasi M, Ammendola S, Battistoni A (2013) Competition for zinc binding in the host-pathogen interaction. Front Cell Infect Microbiol 3:108
Porcheron G, Garénaux A, Proulx J, Sabri M, Dozois CM (2013) Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. In: Veyrier F, Cellier M (eds) Metal economy in host-microbe interactions. Frontiers Media SA, Lausanne, pp 172–195
Nies DH (2007) How cells control zinc homeostasis. Science 317:1695–1696
Kambe T, Yamaguchi-Iwai Y, Sasaki R, Nagao M (2004) Overview of mammalian zinc transporters. Cell Mol Life Sci 61:49–68
Nadadur SS, Srirama K, Mudipalli A (2008) Iron transport and homeostasis mechanisms: their role in health and disease. Indian J Med Res 128:533–544
Dean P, Major P, Nakjang S, Hirt RP, Embley TM (2014) Transport proteins of parasitic protists and their role in nutrient salvage. Front Plant Sci 5:153
North M, Steffen J, Loguinov AV, Zimmerman GR, Vulpe CD, Eide DJ (2012) Genome-wide functional profiling identifies genes and processes important for zinc-limited growth ofSaccharomyces cerevisiae. PLoS Genet 8(6):e1002699
Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14:186–199.https://doi.org/10.1007/BF01569902
Kolaj-Robin O, Russell D, Hayes KA, Pembroke JT, Soulimane T (2015) Cation diffusion facilitator family: structure and function. FEBS Lett 589(12):1283–1295
Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8(1):107
Palmiter RD, Huang L (2004) Efflux and compartmentalization of zinc by members of the SLC30 family of solute carriers. Pflugers Arch 447(5):744–751
Kambe T, Tsuji T, Hashimoto A, Itsumura N (2015) The physiological, biochemical, and molecular roles of zinc transporters in zinc homeostasis and metabolism. Physiol Rev 95(3):749–784
Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27(2-3):313–339
Cubillas C, Vinuesa P, Tabche ML, García-de los Santos A (2013) Phylogenomic analysis of cation diffusion facilitator proteins uncovers Ni2+/Co2+ transporters. Metallomics 5(12):1634–1643
Cragg RA, Christie GR, Phillips SR, Russi RM, Küry S, Mathers JC et al (2002) A novel zinc-regulated human zinc transporter, hZTL1, is localized to the enterocyte apical membrane. J Biol Chem 277(25):22789–22797
Kambe T, Narita H, Yamaguchi-Iwai Y, Hirose J, Amano T, Sugiura N et al (2002) Cloning and characterization of a novel mammalian zinc transporter, zinc transporter 5, abundantly expressed in pancreatic β cells. J Biol Chem 277(21):19049–19055
Li L, Kaplan J (2001) The yeast gene MSC2, a member of the cation diffusion facilitator family, affects the cellular distribution of zinc. J Biol Chem 276(7):5036–5043
Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. In: Zinc biochemistry, physiology, and homeostasis. Springer, Dordrecht, pp 65–84
Gustin JL, Zanis MJ, Salt DE (2011) Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11(1):76
Hoch E, Lin W, Chai J, Hershfinkel M, Fu D, Sekler I (2012) Histidine pairing at the metal transport site of mammalian ZnT transporters controls Zn2+ over Cd2+ selectivity. Proc Natl Acad Sci 109(19):7202–7207
Lee SM, Grass G, Haney CJ, Fan B, Rosen BP, Anton A et al (2002) Functional analysis of theEscherichia coli zinc transporter ZitB. FEMS Microbiol Lett 215(2):273–278
Menezes CB, Frasson AP, Tasca T (2016) Trichomoniasis-are we giving the deserved attention to the most common non-viral sexually transmitted disease worldwide? Microb Cell 3(9):404
Crouch ML, Benchimol M, Alderete JF (2001) Binding of fibronectin byTrichomonas vaginalis is influenced by iron and calcium. Microb Pathog 31(3):131–144
Figueroa-Angulo EE, Rendón-Gandarilla FJ, Puente-Rivera J, Calla-Choque JS, Cárdenas-Guerra RE, Ortega-López J et al (2012) The effects of environmental factors on the virulence ofTrichomonas vaginalis. Microbes Infect 14:1411–1427
Torres-Romero JC, Arroyo R (2009) Responsiveness ofTrichomonas vaginalis to iron concentrations: evidence for a post-transcriptional iron regulation by an IRE/IRP-like system. Infect Genet Evol 9:1065–1074
Krieger JN, Rein MF (1982) Zinc sensitivity of Trichomonas vaginalis: in vitro studies and clinical implications. J Infect Dis 146(3):341–345
Vazquez Carrillo LI, Quintas Granados LI, Arroyo R, Mendoza Hernández G, González Robles A, Carvajal Gamez BI, Alvarez Sánchez ME (2011) The effect of Zn2+ on prostatic cell cytotoxicity caused byTrichomonas vaginalis. J Integr OMICS 1(2):198–210
Garcia AF, Chang TH, Benchimol M, Klumpp DJ, Lehker MW, Alderete JF (2003) Iron and contact with host cells induce expression of adhesins on surface ofTrichomonas vaginalis. Mol Microbiol 47(5):1207–1224
Moreno-Brito V, Yanez-Gomez C, Meza-Cervantez P, Avila-Gonzalez L, Rodriguez MA, Ortega-Lopez J, Gonzalez-Robles A, Arroyo R (2005) A trichomonas vaginalis 120 kDa protein with identity to hydrogenosome pyruvate:ferredoxin oxidoreductase is a surface adhesin induced by iron. Cell Microbiol 7:245–258
Hernández-Gutiérrez R, Avila-González L, Ortega-López J, Cruz-Talonia F, Gómez-Gutierrez G, Arroyo R (2004) Trichomonas vaginalis: characterization of a 39-kDa cysteine proteinase found in patient vaginal secretions. Exp Parasitol 107(3):125–135
Ma L, Meng Q, Cheng W, Sung Y, Tang P, Hu S, Yu J (2011) Involvement of the GP63 protease in infection of Trichomonas vaginalis. Parasitol Res 109(1):71–79
Quan JH, Kang BH, Cha GH, Zhou W, Koh YB, Yang JB et al (2014) Trichonomas vaginalis metalloproteinase induces apoptosis of SiHa cells through disrupting the Mcl-1/Bim and Bcl-xL/Bim complexes. PLoS One 9(10):e110659
Quintas-Granados L, Villalpando J, Vázquez-Carrillo L, Arroyo R, Mendoza-Hernández G, Alvarez-Sánchez ME (2013) TvMP50 is an immunogenic metalloproteinase during male trichomoniasis. Mol Cell Proteomics 12:1953–1964
Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q et al (2007) Draft genome sequence of the sexually transmitted pathogenTrichomonas vaginalis. Science 315(5809):207–212
Dyall SD, Lester DC, Schneider RE, Delgadillo-Correa MG, Plümper E, Martinez A et al (2003)Trichomonas vaginalis Hmp35, a putative pore-forming hydrogenosomal membrane protein, can form a complex in yeast mitochondria. J Biol Chem 278(33):30548–30561
Fernández-Martín KG, Alvarez-Sánchez ME, Arana-Argáez VE, Alvarez-Sánchez LC, Lara-Riegos JC, Torres-Romero JC (2017) Genome-wide identification, in silico characterization and expression analysis of ZIP-like genes fromTrichomonas vaginalis in response to zinc and iron. Biometals 30(5):663–675.https://doi.org/10.1007/s10534-017-0034-x
Conrad MD, Bradic M, Warring SD, Gorman AW, Carlton JM (2013) Getting trichy: tools and approaches to interrogatingTrichomonas vaginalis in a post-genome world. Trends Parasitol 29(1):17–25
Singh S, Singh G, Singh AK, Gautam G, Farmer R, Lodhi SS, Wadhwa G (2011) Prediction and analysis of paralogous proteins inTrichomonas vaginalis genome. Bioinformation 6:31–34
Leong IU, Stuckey A, Lai D, Skinner JR, Love DR (2015) Assessment of the predictive accuracy of five in silico prediction tools, alone or in combination, and two metaservers to classify long QT syndrome gene mutations. BMC Med Genet 16:34
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95(11):5857–5864
Krogh A, Larsson B, Heijne G, Sonnhammer E (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J Mol Biol 305(3):567–580
Buchan DWA, Minneci F, Nugent TCO, Bryson K, Jones DT (2013) Scalable web services for the PSIPRED protein analysis workbench. Nucleic Acids Res 41:W340–W348
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server issue):W202–W208
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins R, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, NJ, pp 571–607
Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64:643–651
Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci U S A 97:12356–12360
Huang L, Tepaamorndech S (2013) The SLC30 family of zinc transporters - a review of current understanding of their biological and pathophysiological roles. Mol Asp Med 34(2-3):548–560
Acknowledgments
This work was undertaken as part of a research project supported by grant 237990 (to J. C. Torres-Romero) from Consejo Nacional de Ciencia y Tecnología (CONACYT), México. K. G. Fernández-Martín is a scholarship recipient from CONACYT.
Conflict of Interest: The authors declare that they have no conflict of interest regarding the publication of this paper.
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Laboratorio de Bioquímica y Genética Molecular, Facultad de Química de la Universidad Autónoma de Yucatán, Mérida, Yucatán, Mexico
J. C. Torres-Romero, K. Fernández-Martín & J. Lara-Riegos
Posgrado en Ciencias Genómicas, Universidad Autónoma de la Ciudad de México (UACM), Ciudad de México, Mexico
María Elizbeth Alvarez-Sánchez
Laboratorio de Virología, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi” de la Universidad Autónoma de Yucatán, Mérida, Yucatán, Mexico
L. C. Alvarez-Sánchez
Laboratorio de Farmacología, Facultad de Química de la Universidad Autónoma de Yucatán, Mérida, Yucatán, Mexico
V. Arana-Argáez
Centro de Información de Medicamentos, Facultad de Química de la Universidad Autónoma de Yucatán, Mérida, Yucatán, Mexico
M. Ramírez-Camacho
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Universidad Autónoma de la Ciudad de México (UACM), Mexico City, Mexico
Luis Olivares-Quiroz
Human Systems Biology Laboratory, Instituto Nacional de Medicina Genómica (INMEGEN), México City, Mexico
Osbaldo Resendis-Antonio
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Torres-Romero, J.C.et al. (2018). Zinc Efflux inTrichomonas vaginalis: In Silico Identification and Expression Analysis of CDF-Like Genes. In: Olivares-Quiroz, L., Resendis-Antonio, O. (eds) Quantitative Models for Microscopic to Macroscopic Biological Macromolecules and Tissues. Springer, Cham. https://doi.org/10.1007/978-3-319-73975-5_8
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