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Secretory Events During Giardia Encystation

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Part of the book series: Microbiology Monographs ((MICROMONO,volume 17))

Abstract

Giardia lamblia, a flagellate protozoan that parasitizes the upper small intestine of humans, is one of the most common causes of diarrheal disease worldwide. Giardia has a simple life cycle, alternating between the disease-causing trophozoites and the infective cysts. Giardia is a true eukaryotic organism since it has two nuclei, an endomembranous system including the nuclear envelope/endoplasmic reticulum, transport vesicles and lysosomes-like peripheral vacuoles, as well as a complex cytoskeleton. However, trophozoites possess several prokaryotic features, including bacterial metabolic pathways and the lack of organelles typical of higher eukaryotes, such as mitochondria, peroxisomes, and a recognizable Golgi apparatus. Despite these characteristics, Giardia carries out secretory events implying both constitutive and regulated trafficking pathways. Here we describe the secretory machinery employed by Giardia for intracellular transport of cyst wall materials, their exocytosis, and the extracellular assembly of the protective cyst wall. These processes are essential for both the survival of the parasite outside the host’s intestine and transmission of the disease among susceptible individuals.

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  • Adam RD (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14:447–475

    PubMed  CAS  Google Scholar 

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2007) Molecular biology of the cell, 5th edn. Garland Science, New York

    Google Scholar 

  • Appenzeller-Herzog C, Hauri HP (2006) The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J Cell Sci 119:2173–2183

    PubMed  CAS  Google Scholar 

  • Arguello-Garcia R, Arguello-Lopez C, Gonzalez-Robles A, Castillo-Figueroa AM, Ortega-Pierres MG (2002) Sequential exposure and assembly of cyst wall filaments on the surface of encysting Giardia duodenalis. Parasitology 125:209–219

    PubMed  CAS  Google Scholar 

  • Bannykh SI, Rowe T, Balch WE (1996) The organization of endoplasmic reticulum export complexes. J Cell Biol 135:19–35

    PubMed  CAS  Google Scholar 

  • Barlowe C (2000) Traffic COPs of the early secretory pathway. Traffic 1:371–377

    PubMed  CAS  Google Scholar 

  • Becker B, Melkonian M (1996) The secretory pathway of protists: spatial and functional organization and evolution. Microbiol Rev 60:697–721

    PubMed  CAS  Google Scholar 

  • Benchimol M (2002) A new set of vesicles in Giardia lamblia. Exp Parasitol 102:30–37

    PubMed  Google Scholar 

  • Benchimol M (2004a) Giardia lamblia: behavior of the nuclear envelope. Parasitol Res 94:254–264

    PubMed  Google Scholar 

  • Benchimol M (2004b) The release of secretory vesicle in encysting Giardia lamblia. FEMS Microbiol Lett 235:81–87

    PubMed  CAS  Google Scholar 

  • Bole DG, Dowin R, Doriaux M, Jamieson JD (1989) Immunocytochemical localization of BiP to the rough endoplasmic reticulum: evidence for protein sorting by selective retention. J Histochem Cytochem 37:1817–1823

    PubMed  CAS  Google Scholar 

  • Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166

    PubMed  CAS  Google Scholar 

  • Boucher SE, Gillin FD (1990) Excystation of in vitro-derived Giardia lamblia cysts. Infect Immun 58:3516–3522

    PubMed  CAS  Google Scholar 

  • Braakman I, Helenius J, Helenius A (1992) Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J 11:1717–1722

    PubMed  CAS  Google Scholar 

  • Buchel LA, Gorenflot A, Chochillon C, Savel J, Gobert JG (1987) In vitro excystation of Giardia from humans: a scanning electron microscopy study. J Parasitol 73:487–493

    PubMed  CAS  Google Scholar 

  • Cabral CM, Liu Y, Moremen KW, Sifers RN (2002) Organizational diversity among distinct glycoprotein endoplasmic reticulum-associated degradation programs. Mol Biol Cell 13:2639–2650

    PubMed  CAS  Google Scholar 

  • Caccio SM, Sprong H (2010) Giardia duodenalis: genetic recombination and its implications for taxonomy and molecular epidemiology. Exp Parasitol 124:107–112

    PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (1987) The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci 503:17–54

    PubMed  CAS  Google Scholar 

  • Cooper MA, Adam RD, Worobey M, Sterling CR (2007) Population genetics provides evidence for recombination in Giardia. Curr Biol 17:1984–1988

    PubMed  CAS  Google Scholar 

  • Dacks JB, Davis LA, Sjogren AM, Andersson JO, Roger AJ, Doolittle WF (2003) Evidence for Golgi bodies in proposed “Golgi-lacking” lineages. Proc Biol Sci 270(Suppl 2):S168–S171

    PubMed  Google Scholar 

  • Davids BJ, Mehta K, Fesus L, McCaffery JM, Gillin FD (2004) Dependence of Giardia lamblia encystation on novel transglutaminase activity. Mol Biochem Parasitol 136:173–180

    PubMed  CAS  Google Scholar 

  • Davids BJ, Reiner DS, Birkeland SR, Preheim SP, Cipriano MJ, McArthur AG, Gillin FD (2006) A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PLoS ONE 1:e44

    PubMed  Google Scholar 

  • de Souza W (2006) Secretory organelles of pathogenic protozoa. An Acad Bras Cienc 78:271–291

    PubMed  Google Scholar 

  • Donaldson JG, Lippincott-Schwartz J (2000) Sorting and signaling at the Golgi complex. Cell 101:693–696

    PubMed  CAS  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    PubMed  CAS  Google Scholar 

  • Elias EV, Quiroga R, Gottig N, Nakanishi H, Nash TE, Neiman A, Lujan HD (2008) Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J Biol Chem 283:35996–36010

    PubMed  CAS  Google Scholar 

  • Elmendorf HG, Dawson SC, McCaffery JM (2003) The cytoskeleton of Giardia lamblia. Int J Parasitol 33:3–28

    PubMed  Google Scholar 

  • Embley TM, Hirt RP (1998) Early branching eukaryotes? Curr Opin Genet Dev 8:624–629

    PubMed  CAS  Google Scholar 

  • Erlandsen SL, Bemrick WJ, Schupp DE, Shields JM, Jarroll EL, Sauch JF, Pawley JB (1990) High-resolution immunogold localization of Giardia cyst wall antigens using field emission SEM with secondary and backscatter electron imaging. J Histochem Cytochem 38:625–632

    PubMed  CAS  Google Scholar 

  • Erlandsen SL, Macechko PT, van Keulen H, Jarroll EL (1996) Formation of the Giardia cyst wall: studies on extracellular assembly using immunogold labeling and high resolution field emission SEM. J Eukaryot Microbiol 43:416–429

    PubMed  CAS  Google Scholar 

  • Faubert G, Reiner DS, Gillin FD (1991) Giardia lamblia: regulation of secretory vesicle formation and loss of ability to reattach during encystation in vitro. Exp Parasitol 72:345–354

    PubMed  CAS  Google Scholar 

  • Feely DE, Dyer JK (1987) Localization of acid phosphatase activity in Giardia lamblia and Giardia muris trophozoites. J Protozool 34:80–83

    PubMed  CAS  Google Scholar 

  • Feely DE, Schollmeyer JV, Erlandsen SL (1982) Giardia spp.: distribution of contractile proteins in the attachment organelle. Exp Parasitol 53:145–154

    PubMed  CAS  Google Scholar 

  • Freedman RB, Bulleid NJ, Hawkins HC, Paver JL (1989) Role of protein disulphide-isomerase in the expression of native proteins. Biochem Soc Symp 55:167–192

    PubMed  CAS  Google Scholar 

  • Gaechter V, Schraner E, Wild P, Hehl AB (2008) The single dynamin family protein in the primitive protozoan Giardia lamblia is essential for stage conversion and endocytic transport. Traffic 9:57–71

    PubMed  CAS  Google Scholar 

  • Gething MJ (1999) Role and regulation of the ER chaperone BiP. Semin Cell Dev Biol 10:465–472

    PubMed  CAS  Google Scholar 

  • Gillin FD, Reiner DS, McCaffery M (1991) Organelles of protein transport in Giardia lamblia. Parasitol Today 7:113–116

    PubMed  CAS  Google Scholar 

  • Gillin FD, Reiner DS, McCaffery JM (1996) Cell biology of the primitive eukaryote Giardia lamblia. Annu Rev Microbiol 50:679–705

    PubMed  CAS  Google Scholar 

  • Gottig N, Elias EV, Quiroga R, Nores MJ, Solari AJ, Touz MC, Lujan HD (2006) Active and passive mechanisms drive secretory granule biogenesis during differentiation of the intestinal parasite Giardia lamblia. J Biol Chem 281:18156–18166

    PubMed  CAS  Google Scholar 

  • Graczyk TK (2005) Is Giardia a living fossil? Trends Parasitol 21:104–107

    PubMed  Google Scholar 

  • Gupta RS, Aitken K, Falah M, Singh B (1994) Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc Natl Acad Sci USA 91:2895–2899

    PubMed  CAS  Google Scholar 

  • Haas IG (1994) BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia 50:1012–1020

    PubMed  CAS  Google Scholar 

  • Hager KM, Striepen B, Tilney LG, Roos DS (1999) The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J Cell Sci 112(Pt 16):2631–2638

    PubMed  CAS  Google Scholar 

  • Hammond AT, Glick BS (2000) Dynamics of transitional endoplasmic reticulum sites in vertebrate cells. Mol Biol Cell 11:3013–3030

    PubMed  CAS  Google Scholar 

  • Hauri HP, Kappeler F, Andersson H, Appenzeller C (2000) ERGIC-53 and traffic in the secretory pathway. J Cell Sci 113(Pt 4):587–596

    PubMed  CAS  Google Scholar 

  • Hehl AB, Marti M (2004) Secretory protein trafficking in Giardia intestinalis. Mol Microbiol 53:19–28

    PubMed  CAS  Google Scholar 

  • Hehl AB, Marti M, Kohler P (2000) Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol Biol Cell 11:1789–1800

    PubMed  CAS  Google Scholar 

  • Helenius A, Trombetta ES, Hebert DN (1997) Simons JF. Calnexin, calreticulin and the folding of glycoproteins Trends in Cell Biology 7:193–200

    CAS  Google Scholar 

  • Hwang C, Sinskey AJ, Lodish HF (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257:1496–1502

    PubMed  CAS  Google Scholar 

  • Jackson CL (2009) Mechanisms of transport through the Golgi complex. J Cell Sci 122:443–452

    PubMed  CAS  Google Scholar 

  • Jarroll EL, Manning P, Lindmark DG, Coggins JR, Erlandsen SL (1989) Giardia cyst wall-specific carbohydrate: evidence for the presence of galactosamine. Mol Biochem Parasitol 32:121–131

    PubMed  CAS  Google Scholar 

  • Jarroll EL, Macechko PT, Steimle PA, Bulik D, Karr CD, van Keulen H, Paget TA, Gerwig G, Kamerling J, Vliegenthart J, Erlandsen S (2001) Regulation of carbohydrate metabolism during Giardia encystment. J Eukaryot Microbiol 48:22–26

    PubMed  CAS  Google Scholar 

  • Kabnick KS, Peattie DA (1990) In situ analyses reveal that the two nuclei of Giardia lamblia are equivalent. J Cell Sci 95(Pt 3):353–360

    PubMed  Google Scholar 

  • Klis FM (1994) Review: cell wall assembly in yeast. Yeast 10:851–869

    PubMed  CAS  Google Scholar 

  • Klumperman J, Schweizer A, Clausen H, Tang BL, Hong W, Oorschot V, Hauri HP (1998) The recycling pathway of protein ERGIC-53 and dynamics of the ER-Golgi intermediate compartment. J Cell Sci 111(Pt 22):3411–3425

    PubMed  CAS  Google Scholar 

  • Knodler LA, Noiva R, Mehta K, McCaffery JM, Aley SB, Svard SG, Nystul TG, Reiner DS, Silberman JD, Gillin FD (1999) Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J Biol Chem 274:29805–29811

    PubMed  CAS  Google Scholar 

  • Lanfredi-Rangel A, Attias M, de Carvalho TM, Kattenbach WM, de Souza W (1998) The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia may correspond to early and late endosomes and to lysosomes. J Struct Biol 123:225–235

    PubMed  CAS  Google Scholar 

  • Lanfredi-Rangel A, Kattenbach WM, Diniz JA Jr, de Souza W (1999) Trophozoites of Giardia lamblia may have a Golgi-like structure. FEMS Microbiol Lett 181:245–251

    PubMed  CAS  Google Scholar 

  • Lanfredi-Rangel A, Attias M, Reiner DS, Gillin FD, de Souza W (2003) Fine structure of the biogenesis of Giardia lamblia encystation secretory vesicles. J Struct Biol 143:153–163

    PubMed  CAS  Google Scholar 

  • Lauwaet T, Davids BJ, Reiner DS, Gillin FD (2007) Encystation of Giardia lamblia: a model for other parasites. Curr Opin Microbiol 10:554–559

    PubMed  Google Scholar 

  • Letourneur F, Gaynor EC, Hennecke S, Demolliere C, Duden R, Emr SD, Riezman H, Cosson P (1994) Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79:1199–1207

    PubMed  CAS  Google Scholar 

  • Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34:D257–D260

    PubMed  CAS  Google Scholar 

  • Liewen H, Meinhold-Heerlein I, Oliveira V, Schwarzenbacher R, Luo G, Wadle A, Jung M, Pfreundschuh M, Stenner-Liewen F (2005) Characterization of the human GARP (Golgi associated retrograde protein) complex. Exp Cell Res 306:24–34

    PubMed  CAS  Google Scholar 

  • Lipsky NG, Pagano RE (1983) Sphingolipid metabolism in cultured fibroblasts: microscopic and biochemical studies employing a fluorescent ceramide analogue. Proc Natl Acad Sci USA 80:2608–2612

    PubMed  CAS  Google Scholar 

  • Lloyd D, Harris JC (2002) Giardia: highly evolved parasite or early branching eukaryote? Trends Microbiol 10:122–127

    PubMed  CAS  Google Scholar 

  • Lujan HD, Touz MC (2003) Protein trafficking in Giardia lamblia. Cell Microbiol 5:427–434

    PubMed  CAS  Google Scholar 

  • Lujan HD, Marotta A, Mowatt MR, Sciaky N, Lippincott-Schwartz J, Nash TE (1995a) Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J Biol Chem 270:4612–4618

    PubMed  CAS  Google Scholar 

  • Lujan HD, Mowatt MR, Conrad JT, Bowers B, Nash TE (1995b) 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 270:29307–29313

    PubMed  CAS  Google Scholar 

  • Lujan HD, Mowatt MR, Wu JJ, Lu Y, Lees A, Chance MR, Nash TE (1995c) Purification of a variant-specific surface protein of Giardia lamblia and characterization of its metal-binding properties. J Biol Chem 270:13807–13813

    PubMed  CAS  Google Scholar 

  • Lujan HD, Mowatt MR, Byrd LG, Nash TE (1996a) Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proc Natl Acad Sci U S A 93:7628–7633

    PubMed  CAS  Google Scholar 

  • Lujan HD, Mowatt MR, Conrad JT, Nash TE (1996b) Increased expression of the molecular chaperone BiP/GRP78 during the differentiation of a primitive eukaryote. Biol Cell 86:11–18

    PubMed  CAS  Google Scholar 

  • Lujan HD, Mowatt MR, Nash TE (1997) Mechanisms of Giardia lamblia differentiation into cysts. Microbiol Mol Biol Rev 61:294–304

    PubMed  CAS  Google Scholar 

  • Lujan HD, Mowatt MR, Nash TE (1998) The molecular mechanisms of Giardia encystation. Parasitol Today 14:446–450

    PubMed  CAS  Google Scholar 

  • Marti M, Hehl AB (2003) Encystation-specific vesicles in Giardia: a primordial Golgi or just another secretory compartment? Trends Parasitol 19:440–446

    PubMed  Google Scholar 

  • Marti M, Li Y, Schraner EM, Wild P, Kohler P, Hehl AB (2003a) The secretory apparatus of an ancient eukaryote: protein sorting to separate export pathways occurs before formation of transient Golgi-like compartments. Mol Biol Cell 14:1433–1447

    PubMed  CAS  Google Scholar 

  • Marti M, Regos A, Li Y, Schraner EM, Wild P, Muller N, Knopf LG, Hehl AB (2003b) An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis. J Biol Chem 278:24837–24848

    PubMed  CAS  Google Scholar 

  • McArthur AG, Knodler LA, Silberman JD, Davids BJ, Gillin FD, Sogin ML (2001) The evolutionary origins of eukaryotic protein disulfide isomerase domains: new evidence from the Amitochondriate protist Giardia lamblia. Mol Biol Evol 18:1455–1463

    PubMed  CAS  Google Scholar 

  • McCaffery JM, Gillin FD (1994) Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp Parasitol 79:220–235

    PubMed  CAS  Google Scholar 

  • McCaffery JM, Faubert GM, Gillin FD (1994) Giardia lamblia: traffic of a trophozoite variant surface protein and a major cyst wall epitope during growth, encystation, and antigenic switching. Exp Parasitol 79:236–249

    PubMed  CAS  Google Scholar 

  • Mehlotra RK (1993) Cultivation, encystation and excystation of Entamoeba histolytica: present status and future prospects. Biol Membr 19:59–84

    Google Scholar 

  • Midlej V, Benchimol M (2009) Giardia lamblia behavior during encystment: how morphological changes in shape occur. Parasitol Int 58:72–80

    PubMed  Google Scholar 

  • Morrison HG, Roger AJ, Nystul TG, Gillin FD, Sogin ML (2001) Giardia lamblia expresses a proteobacterial-like DnaK homolog. Mol Biol Evol 18:530–541

    PubMed  CAS  Google Scholar 

  • Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JE, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921–1926

    PubMed  CAS  Google Scholar 

  • Mowatt MR, Lujan HD, Cotten DB, Bowers B, Yee J, Nash TE, Stibbs HH (1995) Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol 15:955–963

    PubMed  CAS  Google Scholar 

  • Munro S, Pelham HR (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46:291–300

    PubMed  CAS  Google Scholar 

  • Munro S, Pelham HR (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48:899–907

    PubMed  CAS  Google Scholar 

  • Nickel W, Weber T, McNew JA, Parlati F, Sollner TH, Rothman JE (1999) Content mixing and membrane integrity during membrane fusion driven by pairing of isolated v-SNAREs and t-SNAREs. Proc Natl Acad Sci U S A 96:12571–12576

    PubMed  CAS  Google Scholar 

  • Nigam SK, Goldberg AL, Ho S, Rohde MF, Bush KT, Sherman M (1994) A set of endoplasmic reticulum proteins possessing properties of molecular chaperones includes Ca(2+)-binding proteins and members of the thioredoxin superfamily. J Biol Chem 269:1744–1749

    PubMed  CAS  Google Scholar 

  • Orci L, Ravazzola M, Amherdt M, Perrelet A, Powell SK, Quinn DL, Moore HP (1987) The trans-most cisternae of the Golgi complex: a compartment for sorting of secretory and plasma membrane proteins. Cell 51:1039–1051

    PubMed  CAS  Google Scholar 

  • Pelham HR (1995) Sorting and retrieval between the endoplasmic reticulum and Golgi apparatus. Curr Opin Cell Biol 7:530–535

    PubMed  CAS  Google Scholar 

  • Poxleitner MK, Carpenter ML, Mancuso JJ, Wang CJ, Dawson SC, Cande WZ (2008) Evidence for karyogamy and exchange of genetic material in the binucleate intestinal parasite Giardia intestinalis. Science 319:1530–1533

    PubMed  CAS  Google Scholar 

  • Pozzan T, Rizzuto R, Volpe P, Meldolesi J (1994) Molecular and cellular physiology of intracellular calcium stores. Physiol Rev 74:595–636

    PubMed  CAS  Google Scholar 

  • Rambourg A, Clermont Y, Hermo L (1988) Formation of secretion granules in the Golgi apparatus of pancreatic acinar cells of the rat. Am J Anat 183:187–199

    PubMed  CAS  Google Scholar 

  • Randazzo PA, Nie Z, Miura K, Hsu VW (2000) Molecular aspects of the cellular activities of ADP-ribosylation factors. Sci STKE 2000:RE1

    Google Scholar 

  • Ratner DM, Cui J, Steffen M, Moore LL, Robbins PW, Samuelson J (2008) Changes in the N-glycome, glycoproteins with Asn-linked glycans, of Giardia lamblia with differentiation from trophozoites to cysts. Eukaryot Cell 7:1930–1940

    PubMed  CAS  Google Scholar 

  • Regoes A, Hehl AB (2005) SNAP-tag mediated live cell labeling as an alternative to GFP in anaerobic organisms. Biotechniques 39:809–810, 812

    PubMed  CAS  Google Scholar 

  • Reiner DS, McCaffery M, Gillin FD (1990) Sorting of cyst wall proteins to a regulated secretory pathway during differentiation of the primitive eukaryote, Giardia lamblia. Eur J Cell Biol 53:142–153

    PubMed  CAS  Google Scholar 

  • Reiner DS, McCaffery JM, Gillin FD (2001) Reversible interruption of Giardia lamblia cyst wall protein transport in a novel regulated secretory pathway. Cell Microbiol 3:459–472

    PubMed  CAS  Google Scholar 

  • Reiss E, Hearn VM, Poulain D, Shepherd MG (1992) Structure and function of the fungal cell wall. J Med Vet Mycol 30(Suppl 1):143–156

    PubMed  Google Scholar 

  • Samuelson J, Banerjee S, Magnelli P, Cui J, Kelleher DJ, Gilmore R, Robbins PW (2005) The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc Natl Acad Sci U S A 102:1548–1553

    PubMed  CAS  Google Scholar 

  • Sheffield HG, Bjorvat B (1977) Ultrastructure of the cyst of Giardia lamblia. Am J Trop Med Hyg 26:23–30

    PubMed  CAS  Google Scholar 

  • Simpson AG, Roger AJ, Silberman JD, Leipe DD, Edgcomb VP, Jermiin LS, Patterson DJ, Sogin ML (2002) Evolutionary history of "early-diverging" eukaryotes: the excavate taxon Carpediemonas is a close relative of Giardia. Mol Biol Evol 19:1782–1791

    PubMed  CAS  Google Scholar 

  • Sitia R, Meldolesi J (1992) Endoplasmic reticulum: a dynamic patchwork of specialized subregions. Mol Biol Cell 3:1067–1072

    PubMed  CAS  Google Scholar 

  • Slavin I, Saura A, Carranza PG, Touz MC, Nores MJ, Lujan HD (2002) Dephosphorylation of cyst wall proteins by a secreted lysosomal acid phosphatase is essential for excystation of Giardia lamblia. Mol Biochem Parasitol 122:95–98

    PubMed  CAS  Google Scholar 

  • Smith RD, Lupashin VV (2008) Role of the conserved oligomeric Golgi (COG) complex in protein glycosylation. Carbohydr Res 343:2024–2031

    PubMed  CAS  Google Scholar 

  • Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248

    PubMed  Google Scholar 

  • Sogin ML, Silberman JD (1998) Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int J Parasitol 28:11–20

    PubMed  CAS  Google Scholar 

  • Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA (1989) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75–77

    PubMed  CAS  Google Scholar 

  • Solari AJ, Rahn MI, Saura A, Lujan HD (2003) A unique mechanism of nuclear division in Giardia lamblia involves components of the ventral disk and the nuclear envelope. Biocell 27:329–346

    PubMed  Google Scholar 

  • Soltys BJ, Falah M, Gupta RS (1996) Identification of endoplasmic reticulum in the primitive eukaryote Giardia lamblia using cryoelectron microscopy and antibody to Bip. J Cell Sci 109(Pt 7):1909–1917

    PubMed  CAS  Google Scholar 

  • Stefanic S, Palm D, Svard SG, Hehl AB (2006) Organelle proteomics reveals cargo maturation mechanisms associated with Golgi-like encystation vesicles in the early-diverged protozoan Giardia lamblia. J Biol Chem 281:7595–7604

    PubMed  CAS  Google Scholar 

  • Sun CH, McCaffery JM, Reiner DS, Gillin FD (2003) Mining the Giardia lamblia genome for new cyst wall proteins. J Biol Chem 278:21701–21708

    PubMed  CAS  Google Scholar 

  • TerBush DR, Maurice T, Roth D, Novick P (1996) The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15:6483–6494

    PubMed  CAS  Google Scholar 

  • Touz MC, Gottig N, Nash TE, Lujan HD (2002a) Identification and characterization of a novel secretory granule calcium-binding protein from the early branching eukaryote Giardia lamblia. J Biol Chem 277:50557–50563

    PubMed  CAS  Google Scholar 

  • Touz MC, Nores MJ, Slavin I, Carmona C, Conrad JT, Mowatt MR, Nash TE, Coronel CE, Lujan HD (2002b) The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote Giardia lamblia. J Biol Chem 277:8474–8481

    PubMed  CAS  Google Scholar 

  • Touz MC, Lujan HD, Hayes SF, Nash TE (2003) Sorting of encystation-specific cysteine protease to lysosome-like peripheral vacuoles in Giardia lamblia requires a conserved tyrosine-based motif. J Biol Chem 278:6420–6426

    PubMed  CAS  Google Scholar 

  • Touz MC, Kulakova L, Nash TE (2004) Adaptor protein complex 1 mediates the transport of lysosomal proteins from a Golgi-like organelle to peripheral vacuoles in the primitive eukaryote Giardia lamblia. Mol Biol Cell 15:3053–3060

    PubMed  CAS  Google Scholar 

  • Tovar J, Leon-Avila G, Sanchez LB, Sutak R, Tachezy J, van der Giezen M, Hernandez M, Muller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172–176

    PubMed  CAS  Google Scholar 

  • Turano C, Coppari S, Altieri F, Ferraro A (2002) Proteins of the PDI family: unpredicted non-ER locations and functions. J Cell Physiol 193:154–163

    PubMed  CAS  Google Scholar 

  • Wang CH, Su LH, Sun CH (2007) A novel ARID/Bright-like protein involved in transcriptional activation of cyst wall protein 1 gene in Giardia lamblia. J Biol Chem 282:8905–8914

    PubMed  CAS  Google Scholar 

  • Ward W, Alvarado L, Rawlings ND, Engel JC, Franklin C, McKerrow JH (1997) A primitive enzyme for a primitive cell: the protease required for excystation of Giardia. Cell 89:437–444

    PubMed  CAS  Google Scholar 

  • Wilson DW, Lewis MJ, Pelham HR (1993) pH-dependent binding of KDEL to its receptor in vitro. J Biol Chem 268:7465–7468

    PubMed  CAS  Google Scholar 

  • Yu LZ, Birky CW Jr, Adam RD (2002) The two nuclei of Giardia each have complete copies of the genome and are partitioned equationally at cytokinesis. Eukaryot Cell 1:191–199

    PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the Agencia Nacional para la Promoción de la Ciencia y la Tecnología (ANPCYT), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Católica de Córdoba (UCC), and the Howard Hughes Medical Institute (HHMI). H.D.L. is an HHMI International Research Scholar and a Member of the Scientific Investigator’s Career of the CONICET.

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Correspondence to Hugo D. Lujan .

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Rivero, F.D., Müller, D., Lujan, H.D. (2010). Secretory Events During Giardia Encystation. In: de Souza, W. (eds) Structures and Organelles in Pathogenic Protists. Microbiology Monographs, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12863-9_9

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