Sphingolipids, Lipid Rafts, and Giardial Encystation: The Show Must Go On

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• 作者：Tavis L. Mendez ; Atasi De Chatterjee ; Trevor Duarte…
• 关键词：Giardia ; Lipid ; Sphingolipid ; Lipid rafts ; Encystation ; Cyst
• 刊名：Current Tropical Medicine Reports
• 出版年：2015
• 出版时间：September 2015
• 年：2015
• 卷：2
• 期：3
• 页码：136-143
• 全文大小：2651KB
• 参考文献：Papers of particular interest, published recently, have been highlighted as: 鈥?Of importance1.Adam RD. Biology of Giardia lamblia. Clin Microbiol Rev. 2001;14(3):447鈥?5.PubMed Central PubMed CrossRef
  2.Painter JE, Gargano JW, Collier SA, Yoder JS. Giardiasis surveillance鈥擴nited States, 2011鈥?012. MMWR Surveill Summ. 2015;64 Suppl 3:15鈥?5.PubMed
  3.Yoder JS, Gargano JW, Wallace RM, Beach MJ. Centers for Disease Control and Prevention. Giardiasis surveillance鈥擴nited States, 2009鈥?010. MMWR Surveill Summ. 2012;61(5):13鈥?3.PubMed
  4.Yoder JS, Harral C, Beach MJ. Centers for Disease Control and Prevention. Giardiasis surveillance鈥擴nited States, 2006鈥?008. MMWR Surveill Summ. 2010;59(6):15鈥?5.PubMed
  5.Ekdahl K, Andersson Y. Imported giardiasis: impact of international travel, immigration, and adoption. Am J Trop Med Hyg. 2005;72(6):825鈥?0.PubMed
  6.Dorny P, Praet N, Deckers N, Gabriel S. Emerging food-borne parasites. Vet Parasitol. 2009;163(3):196鈥?06.
  7.Bingham AK, Meyer EA. Giardia excystation can be induced in vitro in acidic solutions. Nature. 1979;277(5694):301鈥?.PubMed CrossRef
  8.Boucher SE, Gillin FD. Excystation of in vitro-derived Giardia lamblia cysts. Infect Immun. 1990;58(11):3516鈥?2.PubMed Central PubMed
  9.Gillin FD, Reiner DS, Gault MJ, Douglas H, Das S, Wunderlich A, et al. Encystation and expression of cyst antigens by Giardia lamblia in vitro. Science. 1987;235(4792):1040鈥?.PubMed CrossRef
  10.Kane AV, Ward HD, Keusch GT, Pereira ME. In vitro encystation of Giardia lamblia: large-scale production of in vitro cysts and strain and clone differences in encystation efficiency. J Parasitol. 1991;77(6):974鈥?1.PubMed CrossRef
  11.Dawson SC, House SA. Imaging and analysis of the microtubule cytoskeleton in Giardia. Methods Cell Biol. 2010;97:307鈥?9.PubMed CrossRef
  12.Ghosh S, Frisardi M, Rogers R, Samuelson J. How Giardia swim and divide. Infect Immun. 2001;69(12):7866鈥?2.PubMed Central PubMed CrossRef
  13.Halliez MC, Buret AG. Extra-intestinal and long term consequences of Giardia duodenalis infections. World J Gastroenterol. 2013;19(47):8974鈥?5.PubMed Central PubMed CrossRef
  14.Holberton DV. Mechanism of attachment of Giardia to the wall of the small intestine. Trans R Soc Trop Med Hyg. 1973;67(1):29鈥?0.PubMed CrossRef
  15.Benchimol MDS, De Souza W. The ultrastructure of giardia during growth and differentiation. In: Hugo D, Luj谩n SS, editors. Giardia: a model organism. Vienna: Springer; 2011.
  16.Sener K, Shen Z, Newburg DS, Jarroll EL. Amino sugar phosphate levels in Giardia change during cyst wall formation. Microbiology. 2004;150(Pt 5):1225鈥?0.PubMed CrossRef
  17.Ratner DM, Cui J, Steffen M, Moore LL, Robbins PW, Samuelson J. Changes in the N-glycome, glycoproteins with Asn-linked glycans, of Giardia lamblia with differentiation from trophozoites to cysts. Eukaryot Cell. 2008;7(11):1930鈥?0.PubMed Central PubMed CrossRef
  18.Erlandsen SL, Bemrick WJ, Schupp DE, Shields JM, Jarroll EL, Sauch JF, et al. High-resolution immunogold localization of Giardia cyst wall antigens using field emission SEM with secondary and backscatter electron imaging. J Histochem Cytochem. 1990;38(5):625鈥?2.PubMed CrossRef
  19.Chatterjee A, Carpentieri A, Ratner DM, Bullitt E, Costello CE, Robbins PW, et al. Giardia cyst wall protein 1 is a lectin that binds to curled fibrils of the GalNAc homopolymer. PLoS Pathog. 2010;6(8):e1001059.PubMed Central PubMed CrossRef
  20.Morf L, Spycher C, Rehrauer H, Fournier CA, Morrison HG, Hehl AB. The transcriptional response to encystation stimuli in Giardia lamblia is restricted to a small set of genes. Eukaryot Cell. 2010;9(10):1566鈥?6.PubMed Central PubMed CrossRef
  21.Birkeland SR, Preheim SP, Davids BJ, Cipriano MJ, Palm D, Reiner DS, et al. Transcriptome analyses of the Giardia lamblia life cycle. Mol Biochem Parasitol. 2010;174(1):62鈥?.PubMed Central PubMed CrossRef
  22.Faso C, Bischof S, Hehl AB. The proteome landscape of Giardia lamblia encystation. PLoS One. 2013;8(12):e83207.PubMed Central PubMed CrossRef
  23.Lauwaet T, Davids BJ, Torres-Escobar A, Birkeland SR, Cipriano MJ, Preheim SP, et al. Protein phosphatase 2A plays a crucial role in Giardia lamblia differentiation. Mol Biochem Parasitol. 2007;152(1):80鈥?.PubMed Central PubMed CrossRef
  24.Mowatt MR, Lujan HD, Cotten DB, Bowers B, Yee J, Nash TE, et al. Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol. 1995;15(5):955鈥?3.PubMed CrossRef
  25.Lujan HD, Mowatt MR, Conrad JT, Bowers B, Nash TE. Identification of a novel Giardia lamblia cyst wall protein with leucine-rich repeats: implications for secretory granule formation and protein assembly into the cyst wall. J Biol Chem. 1995;270(49):29307鈥?3.PubMed CrossRef
  26.Gottig N, Elias EV, Quiroga R, Nores MJ, Solari AJ, Touz MC, et al. Active and passive mechanisms drive secretory granule biogenesis during differentiation of the intestinal parasite Giardia lamblia. J Biol Chem. 2006;281(26):18156鈥?6.PubMed CrossRef
  27.Sun CH, Palm D, McArthur AG, Svard SG, Gillin FD. A novel Myb-related protein involved in transcriptional activation of encystation genes in Giardia lamblia. Mol Microbiol. 2002;46(4):971鈥?4.PubMed CrossRef
  28.Chen YH, Su LH, Huang YC, Wang YT, Kao YY, Sun CH. UPF1, a conserved nonsense-mediated mRNA decay factor, regulates cyst wall protein transcripts in Giardia lamblia. PLoS One. 2008;3(10):e3609.PubMed Central PubMed CrossRef
  29.Reiner DS, Hetsko ML, Meszaros JG, Sun CH, Morrison HG, Brunton LL, et al. Calcium signaling in excystation of the early diverging eukaryote, Giardia lamblia. J Biol Chem. 2003;278(4):2533鈥?0.PubMed CrossRef
  30.Faso C, Hehl AB. Membrane trafficking and organelle biogenesis in Giardia lamblia: use it or lose it. Int J Parasitol. 2011;41(5):471鈥?0.PubMed CrossRef
  31.Reiner DS, McCaffery M, Gillin FD. Sorting of cyst wall proteins to a regulated secretory pathway during differentiation of the primitive eukaryote, Giardia lamblia. Eur J Cell Biol. 1990;53(1):142鈥?3.PubMed
  32.Hehl AB, Marti M. Secretory protein trafficking in Giardia intestinalis. Mol Microbiol. 2004;53(1):19鈥?8.PubMed CrossRef
  33.Marti M, Hehl AB. Encystation-specific vesicles in Giardia: a primordial Golgi or just another secretory compartment? Trends Parasitol. 2003;19(10):440鈥?.PubMed CrossRef
  34.de Souza W. Secretory organelles of pathogenic protozoa. An Acad Bras Cienc. 2006;78(2):271鈥?1.PubMed CrossRef
  35.McCaffery JM, Faubert GM, Gillin FD. Giardia lamblia: traffic of a trophozoite variant surface protein and a major cyst wall epitope during growth, encystation, and antigenic switching. Exp Parasitol. 1994;79(3):236鈥?9.PubMed CrossRef
  36.McCaffery JM, Gillin FD. Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp Parasitol. 1994;79(3):220鈥?5.PubMed CrossRef
  37.Bittencourt-Silvestre J, Lemgruber L, de Souza W. Encystation process of Giardia lamblia: morphological and regulatory aspects. Arch Microbiol. 2010;192(4):259鈥?5.PubMed CrossRef
  38.鈥?/div>Hernandez Y, Shpak M, Duarte TT, Mendez TL, Maldonado RA, Roychowdhury S, et al. Novel role of sphingolipid synthesis genes in regulating giardial encystation. Infect Immun. 2008;76(7):2939鈥?9. This paper describes the differential expressions of sphingolipid genes during encystation. Also, the inhibitors of serine-palmitoyltransferase and glucosylceramide transferase are shown to inhibit ceamide endocytsosis and cyst production.PubMed Central PubMed CrossRef
  39.鈥?/div>Sonda S, Stefanic S, Hehl AB. A sphingolipid inhibitor induces a cytokinesis arrest and blocks stage differentiation in Giardia lamblia. Antimicrob Agents Chemother. 2008;52(2):563鈥?. The authors show here that PPMP, an inhibitor of glucosylceramide synthase, arrests cytokinesis of the trophozoite and its transformation into a cyst.PubMed Central PubMed CrossRef
  40.Liu YY, Hill RA, Li YT. Ceramide glycosylation catalyzed by glucosylceramide synthase and cancer drug resistance. Adv Cancer Res. 2013;117:59鈥?9.PubMed Central PubMed CrossRef
  41.Liour SS, Yu RK. Differential effects of three inhibitors of glycosphingolipid biosynthesis on neuronal differentiation of embryonal carcinoma stem cells. Neurochem Res. 2002;27(11):1507鈥?2.PubMed CrossRef
  42.Lee L, Abe A, Shayman JA. Improved inhibitors of glucosylceramide synthase. J Biol Chem. 1999;274(21):14662鈥?.PubMed CrossRef
  43.Kok JW, Babia T, Filipeanu CM, Nelemans A, Egea G, Hoekstra D. PDMP blocks brefeldin A-induced retrograde membrane transport from golgi to ER: evidence for involvement of calcium homeostasis and dissociation from sphingolipid metabolism. J Cell Biol. 1998;142(1):25鈥?8.PubMed Central PubMed CrossRef
  44.Reiner DS, Ankarklev J, Troell K, Palm D, Bernander R, Gillin FD, et al. Synchronisation of Giardia lamblia: identification of cell cycle stage-specific genes and a differentiation restriction point. Int J Parasitol. 2008;38(8-9):935鈥?4.PubMed CrossRef
  45.Farthing MJ, Keusch GT, Carey MC. Effects of bile and bile salts on growth and membrane lipid uptake by Giardia lamblia: possible implications for pathogenesis of intestinal disease. J Clin Invest. 1985;76(5):1727鈥?2.PubMed Central PubMed CrossRef
  46.Gillin FD, Gault MJ, Hofmann AF, Gurantz D, Sauch JF. Biliary lipids support serum-free growth of Giardia lamblia. Infect Immun. 1986;53(3):641鈥?.PubMed Central PubMed
  47.Mohareb EW, Rogers EJ, Weiner EJ, Bruce JI. Giardia lamblia: phospholipid analysis of human isolates. Ann Trop Med Parasitol. 1991;85(6):591鈥?.PubMed
  48.Lanfredi-Rangel A, Kattenbach WM, Diniz Jr JA, de Souza W. Trophozoites of Giardia lamblia may have a Golgi-like structure. FEMS Microbiol Lett. 1999;181(2):245鈥?1.PubMed CrossRef
  49.Stevens TL, Gibson GR, Adam R, Maier J, Allison-Ennis M, Das S. Uptake and cellular localization of exogenous lipids by Giardia lamblia, a primitive eukaryote. Exp Parasitol. 1997;86(2):133鈥?3.PubMed CrossRef
  50.Stefanic S, Morf L, Kulangara C, Regos A, Sonda S, Schraner E, et al. Neogenesis and maturation of transient Golgi-like cisternae in a simple eukaryote. J Cell Sci. 2009;122(Pt 16):2846鈥?6.PubMed CrossRef
  51.鈥?/div>Hernandez Y, Castillo C, Roychowdhury S, Hehl A, Aley SB, Das S. Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia. Int J Parasitol. 2007;37(1):21鈥?2. This paper demonstrates that Giardia uses clathrin-dependent endocytic pathways to import exogenous ceramide from the culture medium.PubMed Central PubMed CrossRef
  52.鈥?/div>Stefanic S, Spycher C, Morf L, Fabrias G, Casas J, Schraner E, et al. Glucosylceramide synthesis inhibition affects cell cycle progression, membrane trafficking, and stage differentiation in Giardia lamblia. J Lipid Res. 2010;51(9):2527鈥?5. This paper describes how glucosylceramide synthesis is important for giardial encystation and blocking of its synthesis by PPMP (an inhibitor of glucosylceramide synthase) affects cell cycle progression, membrane trafficking, and encystation.PubMed Central PubMed CrossRef
  53.Das S, Reiner DS, Zenian J, Hogan DL, Koss MA, Wang CS, et al. Killing of Giardia lamblia trophozoites by human intestinal fluid in vitro. J Infect Dis. 1988;157(6):1257鈥?0.PubMed CrossRef
  54.Deguchi M, Gillin FD, Gigli I. Mechanism of killing of Giardia lamblia trophozoites by complement. J Clin Invest. 1987;79(5):1296鈥?02.PubMed Central PubMed CrossRef
  55.Lauwaet T, Davids BJ, Reiner DS, Gillin FD. Encystation of Giardia lamblia: a model for other parasites. Curr Opin Microbiol. 2007;10(6):554鈥?.PubMed Central PubMed CrossRef
  56.Isaac-Renton JL, Philion JJ. Factors associated with acquiring giardiasis in British Columbia residents. Can J Public Health. 1992;83(2):155鈥?.PubMed
  57.鈥?/div>Mendez TL, De Chatterjee A, Duarte TT, Gazos-Lopes F, Robles-Martinez L, Roy D, et al. Glucosylceramide transferase activity is critical for encystation and viable cyst production by an intestinal protozoan, Giardia lamblia. J Biol Chem. 2013;288(23):16747鈥?0. This paper illustrates that glucosylceramide synthase (also known as glucosylceramide tranferase) regulates ESV biogenesis and viable cyst production by Giardia.PubMed Central PubMed CrossRef
  58.Gillin FD, Boucher SE, Rossi SS, Reiner DS. Giardia lamblia: the roles of bile, lactic acid, and pH in the completion of the life cycle in vitro. Exp Parasitol. 1989;69(2):164鈥?4.PubMed CrossRef
  59.Cary LA, Cooper JA. Molecular switches in lipid rafts. Nature. 2000;404(6781):945鈥?47.
  60.Simons K, Ehehalt R. Cholesterol, lipid rafts, and disease. J Clin Invest. 2002;110(5):597鈥?03.PubMed Central PubMed CrossRef
  61.Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000;1(1):31鈥?.PubMed CrossRef
  62.Stuermer CA. Microdomain-forming proteins and the role of the reggies/flotillins during axon regeneration in zebrafish. Biochim Biophys Acta. 2011;1812(3):415鈥?2.PubMed CrossRef
  63.Sonnino S, Prinetti A, Mauri L, Chigorno V, Tettamanti G. Dynamic and structural properties of sphingolipids as driving forces for the formation of membrane domains. Chem Rev. 2006;106(6):2111鈥?5.PubMed CrossRef
  64.鈥?/div>De Chatterjee A, Mendez TL, Roychowdhury S, Das S. The assembly of GM1 glycolipid- and cholesterol-enriched raft-like membrane microdomains is important for giardial encystation. Infect Immun. 2015;83(5):2030鈥?2. This paper demonstrates that Giardia has the ability to assemble cholesterol and glycolipid-enriched lipid rafts and that disassembly of lipid rafts inhibits encystation.PubMed CrossRef
  65.Jarroll EL, Bingham AK, Meyer EA. Effect of chlorine on Giardia lamblia cyst viability. Appl Environ Microbiol. 1981;41(2):483鈥?.PubMed Central PubMed
  66.Yichoy M, Duarte TT, De Chatterjee A, Mendez TL, Aguilera KY, Roy D, et al. Lipid metabolism in Giardia: a post-genomic perspective. Parasitology. 2011;138(3):267鈥?8.PubMed Central PubMed CrossRef
  
• 作者单位：Tavis L. Mendez (1) (2)
  Atasi De Chatterjee (1) (2)
  Trevor Duarte (1) (2)
  Joaquin De Leon (1) (2)
  Leobarda Robles-Martinez (1) (2)
  Siddhartha Das (1) (2)
  
  1. Infectious Disease and Immunology Cluster, The Border Biomedical Research Center, University of Texas at El Paso, El Paso, TX, 79968, USA
  2. Department of Biological Sciences, University of Texas at El Paso, 500 W. University Avenue, El Paso, TX, 79968-0519, USA
  
• 刊物类别：Tropical Medicine; Parasitology; Behavioral Sciences; Infectious Diseases;
• 刊物主题：Tropical Medicine; Parasitology; Behavioral Sciences; Infectious Diseases;
• 出版者：Springer International Publishing
• ISSN：2196-3045

文摘

Sphingolipids are sphingosine-based phospholipids, which are present in the plasma and endomembranes of many eukaryotic cells. These lipids are involved in various cellular functions, including cell growth, differentiation, and apoptosis. In addition, sphingolipid and cholesterol-enriched membrane microdomains (also called 鈥渓ipid rafts鈥? contain a set of proteins and lipids, which take part in the signaling process in response to intra- or extracellular stimuli. Recent findings suggest that sphingolipids, especially glucosylceramide, play a critical role in inducing encystation and maintaining the cyst viability in Giardia. Similarly, the assembly/disassembly of lipid rafts modulates the encystation and cyst production of this ubiquitous enteric parasite. In this review article, we discuss the overall progress in the field and examine whether sphingolipids and lipid rafts can be used as novel targets for designing therapies to control infection by Giardia, which is rampant in developing countries, where children are especially vulnerable. Keywords Giardia Lipid Sphingolipid Lipid rafts Encystation Cyst