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Microbiology and Molecular Biology Reviews : MMBR logoLink to Microbiology and Molecular Biology Reviews : MMBR
. 1997 Sep;61(3):294–304. doi: 10.1128/mmbr.61.3.294-304.1997

Mechanisms of Giardia lamblia differentiation into cysts.

H D Luján 1, M R Mowatt 1, T E Nash 1
PMCID: PMC232612  PMID: 9293183

Abstract

Microbiologists have long been intrigued by the ability of parasitic organisms to adapt to changes in the environment. Since most parasites occupy several niches during their journey between vectors and hosts, they have developed adaptive responses which allow them to survive under adverse conditions. Therefore, the life cycles of protozoan and helminthic parasites are excellent models with which to study numerous mechanisms involved in cell differentiation, such as the regulation of gene expression, signal transduction pathways, and organelle biogenesis. Unfortunately, many of these studies are very difficult because the conditions needed to elicit developmental changes in parasites remain undetermined in most cases. Recently, several interesting findings were reported on the process of differentiation of Giardia lamblia trophozoites into cysts. G. lamblia is a flagellated protozoan that inhabits the upper small intestine of its vertebrate host and is a major cause of enteric disease worldwide. It belongs to the earliest identified lineage among eukaryotes and therefore offers a unique insight into the progression from primitive to more complex eukaryotic cells. The discovery of a specific stimulus that induces trophozoites to differentiate into cysts, the identification and characterization of encystation-specific molecules, the elucidation of novel biochemical pathways, and the development of useful reagents and techniques have made this parasite an excellent model with which to study differentiation in eukaryotic cells. In this review, we summarize the most recent fundings on several aspects of Giardia differentiation and discuss the significance of these findings within the context of current knowledge in the field.

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Selected References

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  1. Adam R. D. The biology of Giardia spp. Microbiol Rev. 1991 Dec;55(4):706–732. doi: 10.1128/mr.55.4.706-732.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bauerfeind R., Huttner W. B. Biogenesis of constitutive secretory vesicles, secretory granules and synaptic vesicles. Curr Opin Cell Biol. 1993 Aug;5(4):628–635. doi: 10.1016/0955-0674(93)90132-a. [DOI] [PubMed] [Google Scholar]
  3. Beinfeld M. C., Bourdais J., Kuks P., Morel A., Cohen P. Characterization of an endoprotease from rat small intestinal mucosal secretory granules which generates somatostatin-28 from prosomatostatin by cleavage after a single arginine residue. J Biol Chem. 1989 Mar 15;264(8):4460–4465. [PubMed] [Google Scholar]
  4. Bockman D. E., Winborn W. B. Electron microscopic localization of exogenous ferritin within vacuoles of Giardia muris. J Protozool. 1968 Feb;15(1):26–30. doi: 10.1111/j.1550-7408.1968.tb02085.x. [DOI] [PubMed] [Google Scholar]
  5. Braun T., Schofield P. R., Sprengel R. Amino-terminal leucine-rich repeats in gonadotropin receptors determine hormone selectivity. EMBO J. 1991 Jul;10(7):1885–1890. doi: 10.1002/j.1460-2075.1991.tb07714.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Briggs M. R., Yokoyama C., Wang X., Brown M. S., Goldstein J. L. Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. I. Identification of the protein and delineation of its target nucleotide sequence. J Biol Chem. 1993 Jul 5;268(19):14490–14496. [PubMed] [Google Scholar]
  7. Burgess T. L., Kelly R. B. Constitutive and regulated secretion of proteins. Annu Rev Cell Biol. 1987;3:243–293. doi: 10.1146/annurev.cb.03.110187.001331. [DOI] [PubMed] [Google Scholar]
  8. Buser C. A., Kim J., McLaughlin S., Peitzsch R. M. Does the binding of clusters of basic residues to acidic lipids induce domain formation in membranes? Mol Membr Biol. 1995 Jan-Mar;12(1):69–75. doi: 10.3109/09687689509038498. [DOI] [PubMed] [Google Scholar]
  9. Byrd L. G., Conrad J. T., Nash T. E. Giardia lamblia infections in adult mice. Infect Immun. 1994 Aug;62(8):3583–3585. doi: 10.1128/iai.62.8.3583-3585.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Campbell J. D., Faubert G. M. Comparative studies on Giardia lamblia encystation in vitro and in vivo. J Parasitol. 1994 Feb;80(1):36–44. [PubMed] [Google Scholar]
  11. Campbell J. D., Faubert G. M. Recognition of Giardia lamblia cyst-specific antigens by monoclonal antibodies. Parasite Immunol. 1994 Apr;16(4):211–219. doi: 10.1111/j.1365-3024.1994.tb00342.x. [DOI] [PubMed] [Google Scholar]
  12. Carey M. C., Small D. M., Bliss C. M. Lipid digestion and absorption. Annu Rev Physiol. 1983;45:651–677. doi: 10.1146/annurev.ph.45.030183.003251. [DOI] [PubMed] [Google Scholar]
  13. Carmena M. J., Hueso C., Guijarro L. G., Prieto J. C. Cholesterol modulation of membrane fluidity and VIP receptor/effector system in rat prostatic epithelial cells. Regul Pept. 1991 May 17;33(3):287–297. doi: 10.1016/0167-0115(91)90231-5. [DOI] [PubMed] [Google Scholar]
  14. Coggins J. R., Schaefer F. W., 3rd Giardia muris: ultrastructural analysis of in vitro excystation. Exp Parasitol. 1986 Apr;61(2):219–228. doi: 10.1016/0014-4894(86)90155-4. [DOI] [PubMed] [Google Scholar]
  15. Cohen G. B., Ren R., Baltimore D. Modular binding domains in signal transduction proteins. Cell. 1995 Jan 27;80(2):237–248. doi: 10.1016/0092-8674(95)90406-9. [DOI] [PubMed] [Google Scholar]
  16. Dierks T., Klappa P., Wiech H., Zimmermann R. The role of molecular chaperones in protein transport into the endoplasmic reticulum. Philos Trans R Soc Lond B Biol Sci. 1993 Mar 29;339(1289):335–341. doi: 10.1098/rstb.1993.0032. [DOI] [PubMed] [Google Scholar]
  17. Draper M. P., Liu H. Y., Nelsbach A. H., Mosley S. P., Denis C. L. CCR4 is a glucose-regulated transcription factor whose leucine-rich repeat binds several proteins important for placing CCR4 in its proper promoter context. Mol Cell Biol. 1994 Jul;14(7):4522–4531. doi: 10.1128/mcb.14.7.4522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ellis J. E., Setchell K. D., Kaneshiro E. S. Detection of ubiquinone in parasitic and free-living protozoa, including species devoid of mitochondria. Mol Biochem Parasitol. 1994 Jun;65(2):213–224. doi: 10.1016/0166-6851(94)90073-6. [DOI] [PubMed] [Google Scholar]
  19. Ellis J. E., Wyder M. A., Jarroll E. L., Kaneshiro E. S. Changes in lipid composition during in vitro encystation and fatty acid desaturase activity of Giardia lamblia. Mol Biochem Parasitol. 1996 Oct 18;81(1):13–25. doi: 10.1016/0166-6851(96)02677-1. [DOI] [PubMed] [Google Scholar]
  20. Engelke M., Diehl H., Tähti H. Effects of toluene and n-hexane on rat synaptosomal membrane fluidity and integral enzyme activities. Pharmacol Toxicol. 1992 Nov;71(5):343–347. doi: 10.1111/j.1600-0773.1992.tb00559.x. [DOI] [PubMed] [Google Scholar]
  21. Erlandsen S. L., Bemrick W. J., Pawley J. High-resolution electron microscopic evidence for the filamentous structure of the cyst wall in Giardia muris and Giardia duodenalis. J Parasitol. 1989 Oct;75(5):787–797. [PubMed] [Google Scholar]
  22. Erlandsen S. L., Bemrick W. J., Schupp D. E., Shields J. M., Jarroll E. L., Sauch J. F., Pawley J. B. High-resolution immunogold localization of Giardia cyst wall antigens using field emission SEM with secondary and backscatter electron imaging. J Histochem Cytochem. 1990 May;38(5):625–632. doi: 10.1177/38.5.2332623. [DOI] [PubMed] [Google Scholar]
  23. Erlandsen S. L., Macechko P. T., van Keulen H., Jarroll E. L. Formation of the Giardia cyst wall: studies on extracellular assembly using immunogold labeling and high resolution field emission SEM. J Eukaryot Microbiol. 1996 Sep-Oct;43(5):416–429. doi: 10.1111/j.1550-7408.1996.tb05053.x. [DOI] [PubMed] [Google Scholar]
  24. Esfahani M., Bigler R. D., Alfieri J. L., Lund-Katz S., Baum J. D., Scerbo L. Cholesterol regulates the cell surface expression of glycophospholipid-anchored CD14 antigen on human monocytes. Biochim Biophys Acta. 1993 Jul 4;1149(2):217–223. doi: 10.1016/0005-2736(93)90204-d. [DOI] [PubMed] [Google Scholar]
  25. Farthing M. J., Keusch G. T., Carey M. C. 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 Nov;76(5):1727–1732. doi: 10.1172/JCI112162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Farthing M. J., Varon S. R., Keusch G. T. Mammalian bile promotes growth of Giardia lamblia in axenic culture. Trans R Soc Trop Med Hyg. 1983;77(4):467–469. doi: 10.1016/0035-9203(83)90115-3. [DOI] [PubMed] [Google Scholar]
  27. Faubert G., Reiner D. S., Gillin F. D. Giardia lamblia: regulation of secretory vesicle formation and loss of ability to reattach during encystation in vitro. Exp Parasitol. 1991 May;72(4):345–354. doi: 10.1016/0014-4894(91)90080-g. [DOI] [PubMed] [Google Scholar]
  28. Feely D. E., Dyer J. K. Localization of acid phosphatase activity in Giardia lamblia and Giardia muris trophozoites. J Protozool. 1987 Feb;34(1):80–83. doi: 10.1111/j.1550-7408.1987.tb03137.x. [DOI] [PubMed] [Google Scholar]
  29. Feely D. E. Morphology of the cyst of Giardia microti by light and electron microscopy. J Protozool. 1988 Feb;35(1):52–54. doi: 10.1111/j.1550-7408.1988.tb04075.x. [DOI] [PubMed] [Google Scholar]
  30. Field F. J., Kam N. T., Mathur S. N. Regulation of cholesterol metabolism in the intestine. Gastroenterology. 1990 Aug;99(2):539–551. doi: 10.1016/0016-5085(90)91040-d. [DOI] [PubMed] [Google Scholar]
  31. Fraser D. Epidemiology of Giardia lamblia and Cryptosporidium infections in childhood. Isr J Med Sci. 1994 May-Jun;30(5-6):356–361. [PubMed] [Google Scholar]
  32. Friend D. S. The fine structure of Giardia muris. J Cell Biol. 1966 May;29(2):317–332. doi: 10.1083/jcb.29.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Gasic G. P. Basic-helix-loop-helix transcription factor and sterol sensor in a single membrane-bound molecule. Cell. 1994 Apr 8;77(1):17–19. doi: 10.1016/0092-8674(94)90230-5. [DOI] [PubMed] [Google Scholar]
  34. Gillin F. D., Boucher S. E., Rossi S. S., Reiner D. S. Giardia lamblia: the roles of bile, lactic acid, and pH in the completion of the life cycle in vitro. Exp Parasitol. 1989 Aug;69(2):164–174. doi: 10.1016/0014-4894(89)90185-9. [DOI] [PubMed] [Google Scholar]
  35. Gillin F. D., Gault M. J., Hofmann A. F., Gurantz D., Sauch J. F. Biliary lipids support serum-free growth of Giardia lamblia. Infect Immun. 1986 Sep;53(3):641–645. doi: 10.1128/iai.53.3.641-645.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Gillin F. D., Reiner D. S., Gault M. J., Douglas H., Das S., Wunderlich A., Sauch J. F. Encystation and expression of cyst antigens by Giardia lamblia in vitro. Science. 1987 Feb 27;235(4792):1040–1043. doi: 10.1126/science.3547646. [DOI] [PubMed] [Google Scholar]
  37. Gillin F. D., Reiner D. S., McCaffery J. M. Cell biology of the primitive eukaryote Giardia lamblia. Annu Rev Microbiol. 1996;50:679–705. doi: 10.1146/annurev.micro.50.1.679. [DOI] [PubMed] [Google Scholar]
  38. Gillin F. D., Reiner D. S., McCaffery M. Organelles of protein transport in Giardia lamblia. Parasitol Today. 1991 May;7(5):113–116. doi: 10.1016/0169-4758(91)90169-o. [DOI] [PubMed] [Google Scholar]
  39. Goldstein J. L., Basu S. K., Brown M. S. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 1983;98:241–260. doi: 10.1016/0076-6879(83)98152-1. [DOI] [PubMed] [Google Scholar]
  40. Goldstein J. L., Brown M. S. Regulation of the mevalonate pathway. Nature. 1990 Feb 1;343(6257):425–430. doi: 10.1038/343425a0. [DOI] [PubMed] [Google Scholar]
  41. Gozalbo D., Elorza M. V., Sanjuan R., Marcilla A., Valentín E., Sentandreu R. Critical steps in fungal cell wall synthesis: strategies for their inhibition. Pharmacol Ther. 1993 Nov;60(2):337–345. doi: 10.1016/0163-7258(93)90015-6. [DOI] [PubMed] [Google Scholar]
  42. Griffiths G., Simons K. The trans Golgi network: sorting at the exit site of the Golgi complex. Science. 1986 Oct 24;234(4775):438–443. doi: 10.1126/science.2945253. [DOI] [PubMed] [Google Scholar]
  43. Gupta R. S., Aitken K., Falah M., Singh B. Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2895–2899. doi: 10.1073/pnas.91.8.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Halban P. A., Irminger J. C. Sorting and processing of secretory proteins. Biochem J. 1994 Apr 1;299(Pt 1):1–18. doi: 10.1042/bj2990001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Halliday C. E., Clark C., Farthing M. J. Giardia-bile salt interactions in vitro and in vivo. Trans R Soc Trop Med Hyg. 1988;82(3):428–432. doi: 10.1016/0035-9203(88)90153-8. [DOI] [PubMed] [Google Scholar]
  46. Halliday C. E., Inge P. M., Farthing M. J. Characterization of bile salt uptake by Giardia lamblia. Int J Parasitol. 1995 Sep;25(9):1089–1097. doi: 10.1016/0020-7519(95)00029-2. [DOI] [PubMed] [Google Scholar]
  47. Hashimoto T., Nakamura Y., Nakamura F., Shirakura T., Adachi J., Goto N., Okamoto K., Hasegawa M. Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol Biol Evol. 1994 Jan;11(1):65–71. doi: 10.1093/oxfordjournals.molbev.a040093. [DOI] [PubMed] [Google Scholar]
  48. Haucke V., Lithgow T., Rospert S., Hahne K., Schatz G. The yeast mitochondrial protein import receptor Mas20p binds precursor proteins through electrostatic interaction with the positively charged presequence. J Biol Chem. 1995 Mar 10;270(10):5565–5570. doi: 10.1074/jbc.270.10.5565. [DOI] [PubMed] [Google Scholar]
  49. Hay D. W., Carey M. C. Chemical species of lipids in bile. Hepatology. 1990 Sep;12(3 Pt 2):6S–16S. [PubMed] [Google Scholar]
  50. Hill C. S., Treisman R. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell. 1995 Jan 27;80(2):199–211. doi: 10.1016/0092-8674(95)90403-4. [DOI] [PubMed] [Google Scholar]
  51. Hua X., Sakai J., Ho Y. K., Goldstein J. L., Brown M. S. Hairpin orientation of sterol regulatory element-binding protein-2 in cell membranes as determined by protease protection. J Biol Chem. 1995 Dec 8;270(49):29422–29427. doi: 10.1074/jbc.270.49.29422. [DOI] [PubMed] [Google Scholar]
  52. Hua X., Yokoyama C., Wu J., Briggs M. R., Brown M. S., Goldstein J. L., Wang X. SREBP-2, a second basic-helix-loop-helix-leucine zipper protein that stimulates transcription by binding to a sterol regulatory element. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11603–11607. doi: 10.1073/pnas.90.24.11603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Hurtley S. M. Recycling of a secretory granule membrane protein after stimulated secretion. J Cell Sci. 1993 Oct;106(Pt 2):649–655. doi: 10.1242/jcs.106.2.649. [DOI] [PubMed] [Google Scholar]
  54. Januschka M. M., Erlandsen S. L., Bemrick W. J., Schupp D. G., Feely D. E. A comparison of Giardia microti and Spironucleus muris cysts in the vole: an immunocytochemical, light, and electron microscopic study. J Parasitol. 1988 Jun;74(3):452–458. [PubMed] [Google Scholar]
  55. Jarroll E. L., Manning P., Lindmark D. G., Coggins J. R., Erlandsen S. L. Giardia cyst wall-specific carbohydrate: evidence for the presence of galactosamine. Mol Biochem Parasitol. 1989 Jan 15;32(2-3):121–131. doi: 10.1016/0166-6851(89)90063-7. [DOI] [PubMed] [Google Scholar]
  56. Jarroll E. L., Muller P. J., Meyer E. A., Morse S. A. Lipid and carbohydrate metabolism of Giardia lamblia. Mol Biochem Parasitol. 1981 Feb;2(3-4):187–196. doi: 10.1016/0166-6851(81)90099-2. [DOI] [PubMed] [Google Scholar]
  57. Jarroll E. L., Paget T. A. Carbohydrate and amino acid metabolism in Giardia: a review. Folia Parasitol (Praha) 1995;42(2):81–89. [PubMed] [Google Scholar]
  58. Kane A. V., Ward H. D., Keusch G. T., Pereira M. E. In vitro encystation of Giardia lamblia: large-scale production of in vitro cysts and strain and clone differences in encystation efficiency. J Parasitol. 1991 Dec;77(6):974–981. [PubMed] [Google Scholar]
  59. Kattenbach W. M., Pimenta P. F., de Souza W., Pinto da Silva P. Giardia duodenalis: a freeze-fracture, fracture-flip and cytochemistry study. Parasitol Res. 1991;77(8):651–658. doi: 10.1007/BF00928678. [DOI] [PubMed] [Google Scholar]
  60. Kaul D., Singh J. Exogenous cholesterol--initiated transmembrane signalling pathway regulates cholesterogenesis in human platelets. Cell Signal. 1994 Feb;6(2):141–145. doi: 10.1016/0898-6568(94)90070-1. [DOI] [PubMed] [Google Scholar]
  61. Keister D. B. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg. 1983;77(4):487–488. doi: 10.1016/0035-9203(83)90120-7. [DOI] [PubMed] [Google Scholar]
  62. Klausner R. D., Donaldson J. G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol. 1992 Mar;116(5):1071–1080. doi: 10.1083/jcb.116.5.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Klis F. M. Review: cell wall assembly in yeast. Yeast. 1994 Jul;10(7):851–869. doi: 10.1002/yea.320100702. [DOI] [PubMed] [Google Scholar]
  64. Kobe B., Deisenhofer J. Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature. 1993 Dec 23;366(6457):751–756. doi: 10.1038/366751a0. [DOI] [PubMed] [Google Scholar]
  65. Kobe B., Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci. 1994 Oct;19(10):415–421. doi: 10.1016/0968-0004(94)90090-6. [DOI] [PubMed] [Google Scholar]
  66. Krag E., Phillips S. F. Active and passive bile acid absorption in man. Perfusion studies of the ileum and jejunum. J Clin Invest. 1974 Jun;53(6):1686–1694. doi: 10.1172/JCI107720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Kresse H., Hausser H., Schönherr E., Bittner K. Biosynthesis and interactions of small chondroitin/dermatan sulphate proteoglycans. Eur J Clin Chem Clin Biochem. 1994 Apr;32(4):259–264. [PubMed] [Google Scholar]
  68. Kresse H., Hausser H., Schönherr E. Small proteoglycans. Experientia. 1993 May 15;49(5):403–416. doi: 10.1007/BF01923585. [DOI] [PubMed] [Google Scholar]
  69. Lange Y., Steck T. L. Cholesterol homeostasis. Modulation by amphiphiles. J Biol Chem. 1994 Nov 25;269(47):29371–29374. [PubMed] [Google Scholar]
  70. Laughon B. E., Druckman D. A., Vernon A., Quinn T. C., Polk B. F., Modlin J. F., Yolken R. H., Bartlett J. G. Prevalence of enteric pathogens in homosexual men with and without acquired immunodeficiency syndrome. Gastroenterology. 1988 Apr;94(4):984–993. doi: 10.1016/0016-5085(88)90557-4. [DOI] [PubMed] [Google Scholar]
  71. Lecompte M. F., Bouix G., Mann K. G. Electrostatic and hydrophobic interactions are involved in factor Va binding to membranes containing acidic phospholipids. J Biol Chem. 1994 Jan 21;269(3):1905–1910. [PubMed] [Google Scholar]
  72. Lengerich E. J., Addiss D. G., Juranek D. D. Severe giardiasis in the United States. Clin Infect Dis. 1994 May;18(5):760–763. doi: 10.1093/clinids/18.5.760. [DOI] [PubMed] [Google Scholar]
  73. Lindmark D. G. Giardia lamblia: localization of hydrolase activities in lysosome-like organelles of trophozoites. Exp Parasitol. 1988 Feb;65(1):141–147. doi: 10.1016/0014-4894(88)90116-6. [DOI] [PubMed] [Google Scholar]
  74. Luchtel D. L., Lawrence W. P., DeWalle F. B. Electron microscopy of Giardia lamblia cysts. Appl Environ Microbiol. 1980 Oct;40(4):821–832. doi: 10.1128/aem.40.4.821-832.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Lujan H. D., Byrd L. G., Mowatt M. R., Nash T. E. Serum Cohn fraction IV-1 supports the growth of Giardia lamblia in vitro. Infect Immun. 1994 Oct;62(10):4664–4666. doi: 10.1128/iai.62.10.4664-4666.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Lujan H. D., Mowatt M. R., Nash T. E. Lipid requirements and lipid uptake by Giardia lamblia trophozoites in culture. J Eukaryot Microbiol. 1996 May-Jun;43(3):237–242. doi: 10.1111/j.1550-7408.1996.tb01398.x. [DOI] [PubMed] [Google Scholar]
  77. Luján H. D., Marotta A., Mowatt M. R., Sciaky N., Lippincott-Schwartz J., Nash T. E. Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J Biol Chem. 1995 Mar 3;270(9):4612–4618. doi: 10.1074/jbc.270.9.4612. [DOI] [PubMed] [Google Scholar]
  78. Luján H. D., Mowatt M. R., Byrd L. G., Nash T. E. Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7628–7633. doi: 10.1073/pnas.93.15.7628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Luján H. D., Mowatt M. R., Chen G. Z., Nash T. E. Isoprenylation of proteins in the protozoan Giardia lamblia. Mol Biochem Parasitol. 1995 Jun;72(1-2):121–127. doi: 10.1016/0166-6851(94)00070-4. [DOI] [PubMed] [Google Scholar]
  80. Luján H. D., Mowatt M. R., Conrad J. T., Bowers B., Nash T. E. 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 Dec 8;270(49):29307–29313. doi: 10.1074/jbc.270.49.29307. [DOI] [PubMed] [Google Scholar]
  81. Luján H. D., Mowatt M. R., Conrad J. T., Nash T. E. Increased expression of the molecular chaperone BiP/GRP78 during the differentiation of a primitive eukaryote. Biol Cell. 1996;86(1):11–18. doi: 10.1111/j.1768-322x.1996.tb00950.x. [DOI] [PubMed] [Google Scholar]
  82. Luján H. D., Mowatt M. R., Wu J. J., Lu Y., Lees A., Chance M. R., Nash T. E. Purification of a variant-specific surface protein of Giardia lamblia and characterization of its metal-binding properties. J Biol Chem. 1995 Jun 9;270(23):13807–13813. doi: 10.1074/jbc.270.23.13807. [DOI] [PubMed] [Google Scholar]
  83. Macechko P. T., Steimle P. A., Lindmark D. G., Erlandsen S. L., Jarroll E. L. Galactosamine-synthesizing enzymes are induced when Giardia encyst. Mol Biochem Parasitol. 1992 Dec;56(2):301–309. doi: 10.1016/0166-6851(92)90179-n. [DOI] [PubMed] [Google Scholar]
  84. Manning P., Erlandsen S. L., Jarroll E. L. Carbohydrate and amino acid analyses of Giardia muris cysts. J Protozool. 1992 Mar-Apr;39(2):290–296. doi: 10.1111/j.1550-7408.1992.tb01317.x. [DOI] [PubMed] [Google Scholar]
  85. McCaffery J. M., Faubert G. M., Gillin F. D. Giardia lamblia: traffic of a trophozoite variant surface protein and a major cyst wall epitope during growth, encystation, and antigenic switching. Exp Parasitol. 1994 Nov;79(3):236–249. doi: 10.1006/expr.1994.1087. [DOI] [PubMed] [Google Scholar]
  86. McCaffery J. M., Gillin F. D. Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp Parasitol. 1994 Nov;79(3):220–235. doi: 10.1006/expr.1994.1086. [DOI] [PubMed] [Google Scholar]
  87. McDonald J. A. Extracellular matrix assembly. Annu Rev Cell Biol. 1988;4:183–207. doi: 10.1146/annurev.cb.04.110188.001151. [DOI] [PubMed] [Google Scholar]
  88. McLaughlin S., Aderem A. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem Sci. 1995 Jul;20(7):272–276. doi: 10.1016/s0968-0004(00)89042-8. [DOI] [PubMed] [Google Scholar]
  89. Mellman I., Simons K. The Golgi complex: in vitro veritas? Cell. 1992 Mar 6;68(5):829–840. doi: 10.1016/0092-8674(92)90027-A. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Meyer E. A. Isolation and axenic cultivation of Giardia trophozoites from the rabbit, chinchilla, and cat. Exp Parasitol. 1970 Apr;27(2):179–183. doi: 10.1016/0014-4894(70)90023-8. [DOI] [PubMed] [Google Scholar]
  91. Moe K. T., Singh M., Howe J., Ho L. C., Tan S. W., Ng G. C., Chen X. Q., Yap E. H. Observations on the ultrastructure and viability of the cystic stage of Blastocystis hominis from human feces. Parasitol Res. 1996;82(5):439–444. doi: 10.1007/s004360050142. [DOI] [PubMed] [Google Scholar]
  92. Mowatt M. R., Luján H. D., Cotten D. B., Bowers B., Yee J., Nash T. E., Stibbs H. H. Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol. 1995 Mar;15(5):955–963. doi: 10.1111/j.1365-2958.1995.tb02364.x. [DOI] [PubMed] [Google Scholar]
  93. Nash T. E., Aggarwal A., Adam R. D., Conrad J. T., Merritt J. W., Jr Antigenic variation in Giardia lamblia. J Immunol. 1988 Jul 15;141(2):636–641. [PubMed] [Google Scholar]
  94. Nash T. Surface antigen variability and variation in Giardia lamblia. Parasitol Today. 1992 Jul;8(7):229–234. doi: 10.1016/0169-4758(92)90119-m. [DOI] [PubMed] [Google Scholar]
  95. Ohsumi T., Ichimura T., Sugano H., Omata S., Isobe T., Kuwano R. Ribosome-binding protein p34 is a member of the leucine-rich-repeat-protein superfamily. Biochem J. 1993 Sep 1;294(Pt 2):465–472. doi: 10.1042/bj2940465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Ortega-Barria E., Ward H. D., Evans J. E., Pereira M. E. N-acetyl-D-glucosamine is present in cysts and trophozoites of Giardia lamblia and serves as receptor for wheatgerm agglutinin. Mol Biochem Parasitol. 1990 Dec;43(2):151–165. doi: 10.1016/0166-6851(90)90141-8. [DOI] [PubMed] [Google Scholar]
  97. Osborne T. F. Single nucleotide resolution of sterol regulatory region in promoter for 3-hydroxy-3-methylglutaryl coenzyme A reductase. J Biol Chem. 1991 Jul 25;266(21):13947–13951. [PubMed] [Google Scholar]
  98. Owen R. L., Nemanic P. C., Stevens D. P. Ultrastructural observations on giardiasis in a murine model. I. Intestinal distribution, attachment, and relationship to the immune system of Giardia muris. Gastroenterology. 1979 Apr;76(4):757–769. [PubMed] [Google Scholar]
  99. Palade G. Intracellular aspects of the process of protein synthesis. Science. 1975 Aug 1;189(4200):347–358. doi: 10.1126/science.1096303. [DOI] [PubMed] [Google Scholar]
  100. Parks L. W., Casey W. M. Physiological implications of sterol biosynthesis in yeast. Annu Rev Microbiol. 1995;49:95–116. doi: 10.1146/annurev.mi.49.100195.000523. [DOI] [PubMed] [Google Scholar]
  101. Pelham H. R. Multiple targets for brefeldin A. Cell. 1991 Nov 1;67(3):449–451. doi: 10.1016/0092-8674(91)90517-3. [DOI] [PubMed] [Google Scholar]
  102. Pelham H. R., Munro S. Sorting of membrane proteins in the secretory pathway. Cell. 1993 Nov 19;75(4):603–605. doi: 10.1016/0092-8674(93)90479-A. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Poley J. R., Rosenfield S. Malabsorption in giardiasis: presence of a luminal barrier (mucoid pseudomembrane). A scanning and transmission electron microscopic study. J Pediatr Gastroenterol Nutr. 1982;1(1):63–80. [PubMed] [Google Scholar]
  104. Porter J. A., Young K. E., Beachy P. A. Cholesterol modification of hedgehog signaling proteins in animal development. Science. 1996 Oct 11;274(5285):255–259. doi: 10.1126/science.274.5285.255. [DOI] [PubMed] [Google Scholar]
  105. Pryer N. K., Wuestehube L. J., Schekman R. Vesicle-mediated protein sorting. Annu Rev Biochem. 1992;61:471–516. doi: 10.1146/annurev.bi.61.070192.002351. [DOI] [PubMed] [Google Scholar]
  106. RENDTORFF R. C. The experimental transmission of human intestinal protozoan parasites. II. Giardia lamblia cysts given in capsules. Am J Hyg. 1954 Mar;59(2):209–220. doi: 10.1093/oxfordjournals.aje.a119634. [DOI] [PubMed] [Google Scholar]
  107. Rajavashisth T. B., Taylor A. K., Andalibi A., Svenson K. L., Lusis A. J. Identification of a zinc finger protein that binds to the sterol regulatory element. Science. 1989 Aug 11;245(4918):640–643. doi: 10.1126/science.2562787. [DOI] [PubMed] [Google Scholar]
  108. Rao K. N. The significance of the cholesterol biosynthetic pathway in cell growth and carcinogenesis (review). Anticancer Res. 1995 Mar-Apr;15(2):309–314. [PubMed] [Google Scholar]
  109. Reiner D. S., Douglas H., Gillin F. D. Identification and localization of cyst-specific antigens of Giardia lamblia. Infect Immun. 1989 Mar;57(3):963–968. doi: 10.1128/iai.57.3.963-968.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Reiner D. S., Hetsko M. L., Das S., Ward H. D., McCaffery M., Gillin F. D. Giardia lamblia: absence of cyst antigens and reduced secretory vesicle formation and bile salt uptake in an encystation-deficient subline. Exp Parasitol. 1993 Dec;77(4):461–472. doi: 10.1006/expr.1993.1107. [DOI] [PubMed] [Google Scholar]
  111. Reiner D. S., McCaffery M., Gillin F. D. Sorting of cyst wall proteins to a regulated secretory pathway during differentiation of the primitive eukaryote, Giardia lamblia. Eur J Cell Biol. 1990 Oct;53(1):142–153. [PubMed] [Google Scholar]
  112. Reiss E., Hearn V. M., Poulain D., Shepherd M. G. Structure and function of the fungal cell wall. J Med Vet Mycol. 1992;30 (Suppl 1):143–156. doi: 10.1080/02681219280000841. [DOI] [PubMed] [Google Scholar]
  113. Rothman J. E., Orci L. Molecular dissection of the secretory pathway. Nature. 1992 Jan 30;355(6359):409–415. doi: 10.1038/355409a0. [DOI] [PubMed] [Google Scholar]
  114. Sakai J., Duncan E. A., Rawson R. B., Hua X., Brown M. S., Goldstein J. L. Sterol-regulated release of SREBP-2 from cell membranes requires two sequential cleavages, one within a transmembrane segment. Cell. 1996 Jun 28;85(7):1037–1046. doi: 10.1016/s0092-8674(00)81304-5. [DOI] [PubMed] [Google Scholar]
  115. Sato R., Yang J., Wang X., Evans M. J., Ho Y. K., Goldstein J. L., Brown M. S. Assignment of the membrane attachment, DNA binding, and transcriptional activation domains of sterol regulatory element-binding protein-1 (SREBP-1). J Biol Chem. 1994 Jun 24;269(25):17267–17273. [PubMed] [Google Scholar]
  116. Schupp D. G., Januschka M. M., Sherlock L. A., Stibbs H. H., Meyer E. A., Bemrick W. J., Erlandsen S. L. Production of viable Giardia cysts in vitro: determination by fluorogenic dye staining, excystation, and animal infectivity in the mouse and Mongolian gerbil. Gastroenterology. 1988 Jul;95(1):1–10. doi: 10.1016/0016-5085(88)90283-1. [DOI] [PubMed] [Google Scholar]
  117. Sheffield H. G., Bjorvat B. Ultrastructure of the cyst of Giardia lamblia. Am J Trop Med Hyg. 1977 Jan;26(1):23–30. doi: 10.4269/ajtmh.1977.26.23. [DOI] [PubMed] [Google Scholar]
  118. Shipley G. G. Structural studies of the lipid components of bile. Hepatology. 1990 Sep;12(3 Pt 2):33S–38S. [PubMed] [Google Scholar]
  119. Sigal C. T., Zhou W., Buser C. A., McLaughlin S., Resh M. D. Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12253–12257. doi: 10.1073/pnas.91.25.12253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Sogin M. L., Gunderson J. H., Elwood H. J., Alonso R. A., Peattie D. A. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science. 1989 Jan 6;243(4887):75–77. doi: 10.1126/science.2911720. [DOI] [PubMed] [Google Scholar]
  121. Soltys B. J., Falah M., Gupta R. S. Identification of endoplasmic reticulum in the primitive eukaryote Giardia lamblia using cryoelectron microscopy and antibody to Bip. J Cell Sci. 1996 Jul;109(Pt 7):1909–1917. doi: 10.1242/jcs.109.7.1909. [DOI] [PubMed] [Google Scholar]
  122. Spear D. H., Ericsson J., Jackson S. M., Edwards P. A. Identification of a 6-base pair element involved in the sterol-mediated transcriptional regulation of farnesyl diphosphate synthase. J Biol Chem. 1994 Oct 7;269(40):25212–25218. [PubMed] [Google Scholar]
  123. Spear D. H., Kutsunai S. Y., Correll C. C., Edwards P. A. Molecular cloning and promoter analysis of the rat liver farnesyl diphosphate synthase gene. J Biol Chem. 1992 Jul 15;267(20):14462–14469. [PubMed] [Google Scholar]
  124. Spinedi A., Luly P., Farias R. N. Does the fluidity of the lipid environment modulate membrane-bound acetylcholinesterase? Effects of temperature, membrane composition and amphiphiles. Biochem Pharmacol. 1993 Nov 2;46(9):1521–1527. doi: 10.1016/0006-2952(93)90318-q. [DOI] [PubMed] [Google Scholar]
  125. Steinmayr M., Motte P., Sommer H., Saedler H., Schwarz-Sommer Z. FIL2, an extracellular Leucine-Rich Repeat protein, is specifically expressed in Antirrhinum flowers. Plant J. 1994 Apr;5(4):459–467. doi: 10.1046/j.1365-313x.1994.5040459.x. [DOI] [PubMed] [Google Scholar]
  126. Stibbs H. H. Monoclonal antibody-based enzyme immunoassay for Giardia lamblia antigen in human stool. J Clin Microbiol. 1989 Nov;27(11):2582–2588. doi: 10.1128/jcm.27.11.2582-2588.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Stratford M. Another brick in the wall? Recent developments concerning the yeast cell envelope. Yeast. 1994 Dec;10(13):1741–1752. doi: 10.1002/yea.320101307. [DOI] [PubMed] [Google Scholar]
  128. Suzuki N., Choe H. R., Nishida Y., Yamawaki-Kataoka Y., Ohnishi S., Tamaoki T., Kataoka T. Leucine-rich repeats and carboxyl terminus are required for interaction of yeast adenylate cyclase with RAS proteins. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8711–8715. doi: 10.1073/pnas.87.22.8711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Thompson R. C., Reynoldson J. A., Mendis A. H. Giardia and giardiasis. Adv Parasitol. 1993;32:71–160. doi: 10.1016/s0065-308x(08)60207-9. [DOI] [PubMed] [Google Scholar]
  130. Thompson S. C. Giardia lamblia in children and the child care setting: a review of the literature. J Paediatr Child Health. 1994 Jun;30(3):202–209. doi: 10.1111/j.1440-1754.1994.tb00620.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Thomson A. B., Schoeller C., Keelan M., Smith L., Clandinin M. T. Lipid absorption: passing through the unstirred layers, brush-border membrane, and beyond. Can J Physiol Pharmacol. 1993 Aug;71(8):531–555. doi: 10.1139/y93-078. [DOI] [PubMed] [Google Scholar]
  132. Tooze S. A. Biogenesis of secretory granules. Implications arising from the immature secretory granule in the regulated pathway of secretion. FEBS Lett. 1991 Jul 22;285(2):220–224. doi: 10.1016/0014-5793(91)80805-d. [DOI] [PubMed] [Google Scholar]
  133. Towle H. C. Metabolic regulation of gene transcription in mammals. J Biol Chem. 1995 Oct 6;270(40):23235–23238. doi: 10.1074/jbc.270.40.23235. [DOI] [PubMed] [Google Scholar]
  134. Veazie L. Epidemic giardiasis. N Engl J Med. 1969 Oct 9;281(15):853–853. doi: 10.1056/nejm196910092811521. [DOI] [PubMed] [Google Scholar]
  135. Walker J. C. Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J. 1993 Mar;3(3):451–456. doi: 10.1111/j.1365-313x.1993.tb00164.x. [DOI] [PubMed] [Google Scholar]
  136. Wang X., Briggs M. R., Hua X., Yokoyama C., Goldstein J. L., Brown M. S. Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. II. Purification and characterization. J Biol Chem. 1993 Jul 5;268(19):14497–14504. [PubMed] [Google Scholar]
  137. Wang X., Sato R., Brown M. S., Hua X., Goldstein J. L. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell. 1994 Apr 8;77(1):53–62. doi: 10.1016/0092-8674(94)90234-8. [DOI] [PubMed] [Google Scholar]
  138. Ward H. D., Alroy J., Lev B. I., Keusch G. T., Pereira M. E. Biology of Giardia lamblia. Detection of N-acetyl-D-glucosamine as the only surface saccharide moiety and identification of two distinct subsets of trophozoites by lectin binding. J Exp Med. 1988 Jan 1;167(1):73–88. doi: 10.1084/jem.167.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  139. Ward H. D., Alroy J., Lev B. I., Keusch G. T., Pereira M. E. Identification of chitin as a structural component of Giardia cysts. Infect Immun. 1985 Sep;49(3):629–634. doi: 10.1128/iai.49.3.629-634.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. Ward H. D., Kane A. V., Ortega-Barria E., Keusch G. T., Pereira M. E. Identification of developmentally regulated Giardia lamblia cyst antigens using GCSA-1, a cyst-specific monoclonal antibody. Mol Microbiol. 1990 Dec;4(12):2095–2102. doi: 10.1111/j.1365-2958.1990.tb00570.x. [DOI] [PubMed] [Google Scholar]
  141. Ware J., Russell S. R., Marchese P., Murata M., Mazzucato M., De Marco L., Ruggeri Z. M. Point mutation in a leucine-rich repeat of platelet glycoprotein Ib alpha resulting in the Bernard-Soulier syndrome. J Clin Invest. 1993 Sep;92(3):1213–1220. doi: 10.1172/JCI116692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Wieder S. C., Keister D. B., Reiner D. S. Mass cultivation of Giardia lamblia in a serum-free medium. J Parasitol. 1983 Dec;69(6):1181–1182. [PubMed] [Google Scholar]
  143. Williams A. G., Coombs G. H. Multiple protease activities in Giardia intestinalis trophozoites. Int J Parasitol. 1995 Jul;25(7):771–778. doi: 10.1016/0020-7519(94)00201-x. [DOI] [PubMed] [Google Scholar]
  144. Wilson F. A., Treanor L. L. Characterization of the passive and active transport mechanisms for bile acid uptake into rat isolated intestinal epithelial cells. Biochim Biophys Acta. 1975 Oct 6;406(2):280–293. doi: 10.1016/0005-2736(75)90010-3. [DOI] [PubMed] [Google Scholar]
  145. Yee J., Dennis P. P. Isolation and characterization of a NADP-dependent glutamate dehydrogenase gene from the primitive eucaryote Giardia lamblia. J Biol Chem. 1992 Apr 15;267(11):7539–7544. [PubMed] [Google Scholar]
  146. Yee J., Nash T. E. Transient transfection and expression of firefly luciferase in Giardia lamblia. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5615–5619. doi: 10.1073/pnas.92.12.5615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. Yu D. C., Wang A. L., Wu C. H., Wang C. C. Virus-mediated expression of firefly luciferase in the parasitic protozoan Giardia lamblia. Mol Cell Biol. 1995 Sep;15(9):4867–4872. doi: 10.1128/mcb.15.9.4867. [DOI] [PMC free article] [PubMed] [Google Scholar]

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