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Article ; Online: Investigating how clathrin adaptor complex AP-2 participates in Giardia lamblia encystation.

Feliziani, Constanza / Rivero, Maria R / Quassollo, Gonzalo / Rópolo, Andrea S / Touz, María C

2022 Volume 52, Issue 7, Page(s) 399–406

Abstract: The protozoan parasite Giardia lamblia acquires cholesterol from the environment since it is unable to synthesise cholesterol de novo and this is vital for trophozoite growth. Conversely, the lack of cholesterol was described as an essential event to ... ...

Abstract	The protozoan parasite Giardia lamblia acquires cholesterol from the environment since it is unable to synthesise cholesterol de novo and this is vital for trophozoite growth. Conversely, the lack of cholesterol was described as an essential event to trigger encystation, the differentiation of trophozoites to mature cysts. During the G. lamblia cell cycle, cholesterol is acquired as a free molecule as well as through receptor-mediated endocytosis (RME) of lipoproteins. In this work, we describe the involvement of RME in the cell differentiation process of G. lamblia. We found that a reduction in the expression of the medium subunit (Glµ2) of the giardial adaptin protein GlAP2 impaired RME, triggering the process of encystation in growing cells. Contrary to expectations, decreasing Glµ2 expression produced a cohort of trophozoites that yielded significantly less mature cysts when cells were induced to encyst. Analysis of the subcellular localization of Glµ2 and the cyst wall protein 1 (CWP1) during encystation was later performed, to dissect the process. Our results showed, on one hand, that blocking RME by inhibiting Glµ2 expression, and probably cholesterol entry, is sufficient to induce cell differentiation but not to complete the process of encystation. On the other hand, we observed that GlAP2 is necessary to accomplish the final steps of encystation by sorting CWP1 to the plasma membrane for cyst wall formation. The understanding of the mechanisms involved in cyst formation should provide novel insights into the control of giardiasis, an endemic worldwide neglected disease.
MeSH term(s)	Adaptor Proteins, Vesicular Transport/metabolism ; Animals ; Cholesterol ; Giardia lamblia/genetics ; Giardia lamblia/metabolism ; Giardiasis/parasitology ; Humans ; Protozoan Proteins/genetics ; Protozoan Proteins/metabolism ; Trophozoites/metabolism
Chemical Substances	Adaptor Proteins, Vesicular Transport ; Protozoan Proteins ; Cholesterol (97C5T2UQ7J)
Language	English
Publishing date	2022-03-30
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	120518-3
ISSN	1879-0135 ; 0020-7519
ISSN (online)	1879-0135
ISSN	0020-7519
DOI	10.1016/j.ijpara.2022.02.003
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Article ; Online: Unusual proteins in Giardia duodenalis and their role in survival.

Rópolo, Andrea S / Feliziani, Constanza / Touz, María C

Advances in parasitology

2019 Volume 106, Page(s) 1–50

Abstract: ... proteins with an extra independent function(s). In this chapter, we provide an overview of unusual proteins ...

Abstract	The capacity of the parasite Giardia duodenalis to perform complex functions with minimal amounts of proteins and organelles has attracted increasing numbers of scientists worldwide, trying to explain how this parasite adapts to internal and external changes to survive. One explanation could be that G. duodenalis evolved from a structurally complex ancestor by reductive evolution, resulting in adaptation to its parasitic lifestyle. Reductive evolution involves the loss of genes, organelles, and functions that commonly occur in many parasites, by which the host renders some structures and functions redundant. However, there is increasing data that Giardia possesses proteins able to perform more than one function. During recent decades, the concept of moonlighting was described for multitasking proteins, which involves only proteins with an extra independent function(s). In this chapter, we provide an overview of unusual proteins in Giardia that present multifunctional properties depending on the location and/or parasite requirement. We also discuss experimental evidence that may allow some giardial proteins to be classified as moonlighting proteins by examining the properties of moonlighting proteins in general. Up to date, Giardia does not seem to require the numerous redundant proteins present in other organisms to accomplish its normal functions, and thus this parasite may be an appropriate model for understanding different aspects of moonlighting proteins, which may be helpful in the design of drug targets.
MeSH term(s)	Animals ; Giardia/physiology ; Host-Parasite Interactions/physiology ; Protozoan Proteins/genetics ; Protozoan Proteins/metabolism
Chemical Substances	Protozoan Proteins
Language	English
Publishing date	2019-08-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	165-x
ISSN	2163-6079 ; 0065-308X
ISSN (online)	2163-6079
ISSN	0065-308X
DOI	10.1016/bs.apar.2019.07.001
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Article: Membrane-Associated Proteins in

Touz, María C / Feliziani, Constanza / Rópolo, Andrea S

Genes

2018 Volume 9, Issue 8

Abstract: The manner in which membrane-associated proteins interact with the membrane defines their subcellular fate and function. This interaction relies on the characteristics of the proteins, their journey after synthesis, and their interaction with other ... ...

Abstract	The manner in which membrane-associated proteins interact with the membrane defines their subcellular fate and function. This interaction relies on the characteristics of the proteins, their journey after synthesis, and their interaction with other proteins or enzymes. Understanding these properties may help to define the function of a protein and also the role of an organelle. In the case of microorganisms like protozoa parasites, it may help to understand singular features that will eventually lead to the design of parasite-specific drugs. The protozoa parasite
Language	English
Publishing date	2018-08-10
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2527218-4
ISSN	2073-4425
ISSN	2073-4425
DOI	10.3390/genes9080404
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Article ; Online: The Exosome-like Vesicles of

Natali, Lautaro / Luna Pizarro, Gabriel / Moyano, Sofía / de la Cruz-Thea, Benjamin / Musso, Juliana / Rópolo, Andrea S / Eichner, Norbert / Meister, Gunter / Musri, Melina M / Feliziani, Constanza / Touz, María C

International journal of molecular sciences

2023 Volume 24, Issue 11

Abstract: The genetically related assemblages of the intestinal protozoa ... ...

Abstract	The genetically related assemblages of the intestinal protozoa parasite
MeSH term(s)	Humans ; Animals ; Giardia/genetics ; Parasites ; RNA/metabolism ; Exosomes/genetics ; Exosomes/metabolism ; Giardiasis/parasitology ; RNA, Transfer/metabolism ; RNA, Ribosomal/metabolism
Chemical Substances	RNA (63231-63-0) ; RNA, Transfer (9014-25-9) ; RNA, Ribosomal
Language	English
Publishing date	2023-05-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24119559
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Article: Investigating how clathrin adaptor complex AP-2 participates in Giardia lamblia encystation

Feliziani, Constanza / Rivero, Maria R. / Quassollo, Gonzalo / Rópolo, Andrea S. / Touz, María C.

Australian Society for Parasitology International journal for parasitology. 2022 Feb. 16,

2022

Abstract	The protozoan parasite Giardia lamblia acquires cholesterol from the environment since it is unable to synthesise cholesterol de novo and this is vital for trophozoite growth. Conversely, the lack of cholesterol was described as an essential event to trigger encystation, the differentiation of trophozoites to mature cysts. During the G. lamblia cell cycle, cholesterol is acquired as a free molecule as well as through receptor-mediated endocytosis (RME) of lipoproteins. In this work, we describe the involvement of RME in the cell differentiation process of G. lamblia. We found that a reduction in the expression of the medium subunit (Glµ2) of the giardial adaptin protein GlAP2 impaired RME, triggering the process of encystation in growing cells. Contrary to expectations, decreasing Glµ2 expression produced a cohort of trophozoites that yielded significantly less mature cysts when cells were induced to encyst. Analysis of the subcellular localization of Glµ2 and the cyst wall protein 1 (CWP1) during encystation was later performed, to dissect the process. Our results showed, on one hand, that blocking RME by inhibiting Glµ2 expression, and probably cholesterol entry, is sufficient to induce cell differentiation but not to complete the process of encystation. On the other hand, we observed that GlAP2 is necessary to accomplish the final steps of encystation by sorting CWP1 to the plasma membrane for cyst wall formation. The understanding of the mechanisms involved in cyst formation should provide novel insights into the control of giardiasis, an endemic worldwide neglected disease.
Keywords	Giardia lamblia ; cell cycle ; cell differentiation ; cholesterol ; clathrin ; encystment ; endocytosis ; giardiasis ; lipoproteins ; parasites ; parasitology ; plasma membrane ; trophozoites
Language	English
Dates of publication	2022-0216
Publishing place	Elsevier Ltd
Document type	Article
Note	Pre-press version
ZDB-ID	120518-3
ISSN	1879-0135 ; 0020-7519
ISSN (online)	1879-0135
ISSN	0020-7519
DOI	10.1016/j.ijpara.2022.02.003
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: The Exosome-like Vesicles of Giardia Assemblages A, B, and E Are Involved in the Delivering of Distinct Small RNA from Parasite to Parasite

Lautaro Natali / Gabriel Luna Pizarro / Sofía Moyano / Benjamin de la Cruz-Thea / Juliana Musso / Andrea S. Rópolo / Norbert Eichner / Gunter Meister / Melina M. Musri / Constanza Feliziani / María C. Touz

International Journal of Molecular Sciences, Vol 24, Iss 9559, p

2023 Volume 9559

Abstract: The genetically related assemblages of the intestinal protozoa parasite Giardia lamblia are morphologically indistinguishable and are often derived from specific hosts. The Giardia assemblages are separated by large genetic distances, which might account ...

Abstract	The genetically related assemblages of the intestinal protozoa parasite Giardia lamblia are morphologically indistinguishable and are often derived from specific hosts. The Giardia assemblages are separated by large genetic distances, which might account for their relevant biological and pathogenic differences. In this work, we analyzed the RNAs cargo released into exosomal-like vesicles (ElVs) by the assemblages A and B, which differentially infect humans, and the assemblage E, which infects hoofed animals. The RNA sequencing analysis revealed that the ElVs of each assemblage contained distinct small RNA (sRNA) biotypes, suggesting a preference for specific packaging in each assemblage. These sRNAs were classified into three categories, ribosomal-small RNAs (rsRNAs), messenger-small RNAs (msRNAs), and transfer-small RNAs (tsRNAs), which may play a regulatory role in parasite communication and contribute to host-specificity and pathogenesis. Uptake experiments showed, for the first time, that ElVs were successfully internalized by the parasite trophozoites. Furthermore, we observed that the sRNAs contained inside these ElVs were first located below the plasma membrane but then distributed along the cytoplasm. Overall, the study provides new insights into the molecular mechanisms underlying the host-specificity and pathogenesis of G. lamblia and highlights the potential role of sRNAs in parasite communication and regulation.
Keywords	Giardia lamblia ; parasite to parasite communication ; exosomal-like vesicles (ElVs) ; small RNAs (sRNA) ; msRNA ; tsRNA ; Biology (General) ; QH301-705.5 ; Chemistry ; QD1-999
Subject code	572
Language	English
Publishing date	2023-05-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
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Article ; Online: A lesson in survival, by Giardia lamblia.

Rópolo, Andrea S / Touz, Maria C

TheScientificWorldJournal

2010 Volume 10, Page(s) 2019–2031

Abstract: In the relationships between host and parasites, there is a cross-talk that involves diverse mechanisms developed by two different genetic systems during years of evolution. On the one hand, immunocompetent hosts have developed effective innate and ... ...

Abstract	In the relationships between host and parasites, there is a cross-talk that involves diverse mechanisms developed by two different genetic systems during years of evolution. On the one hand, immunocompetent hosts have developed effective innate and acquired immune responses that are used to restrict or avoid parasitism. On the other hand, parasites evade the immune response, expressing different antigens on their surface or by using other specific mechanisms, such as nutrient depletion. In this review, we analyze the survival mechanisms used by the protozoan parasite Giardia lamblia during infection. In particular, we examine the multiple roles played by the enzyme arginine deiminase during colonization of the gut, also involving the parasite's mechanism of antigenic variation. Potential drug targets for the treatment of giardiasis are also discussed.
MeSH term(s)	Animals ; Antigenic Variation/immunology ; Arginine/metabolism ; Giardia lamblia/immunology ; Giardia lamblia/metabolism ; Giardia lamblia/physiology ; Giardiasis/immunology ; Giardiasis/metabolism ; Giardiasis/parasitology ; Host-Parasite Interactions ; Humans ; Hydrolases/metabolism ; Models, Biological ; Protozoan Proteins/metabolism
Chemical Substances	Protozoan Proteins ; Arginine (94ZLA3W45F) ; Hydrolases (EC 3.-) ; arginine deiminase (EC 3.5.3.6)
Language	English
Publishing date	2010-10-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2075968-X
ISSN	1537-744X ; 1537-744X
ISSN (online)	1537-744X
ISSN	1537-744X
DOI	10.1100/tsw.2010.200
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Article ; Online: Histone methyltransferase 1 regulates the encystation process in the parasite Giardia lamblia.

Salusso, Agostina / Zlocowski, Natacha / Mayol, Gonzalo F / Zamponi, Nahuel / Rópolo, Andrea S

The FEBS journal

2017 Volume 284, Issue 15, Page(s) 2396–2409

Abstract: In eukaryotes, histone lysine methylation is associated with either active or repressed chromatin states, depending on the status of methylation. Even when the amino-terminus of Giardia lamblia histones diverges from other organisms, these regions ... ...

Abstract	In eukaryotes, histone lysine methylation is associated with either active or repressed chromatin states, depending on the status of methylation. Even when the amino-terminus of Giardia lamblia histones diverges from other organisms, these regions contain lysine residues that are potential targets for methylation. When we examined the role of the histone methyltransferase 1 (HMT1) in the regulation of the encystation process by giardial histone methyltransferase 1 (GlHMT1) overexpression or downregulation, we observed an increase or a decrease in cyst production, respectively, compared to wild-type trophozoites. A time-lapse analysis of encystation showed that overexpression of GlHMT1 induced an earlier and faster process than in wild-type cells together with an upregulation of mRNA expression of cyst wall proteins. Subcellular localization studies indicated that GlHMT1-hemaglutinin was mainly associated with the nuclear and perinuclear region in both growing and encysting parasites, in agreement with bioinformatics analyses showing that GlHMT-1 possesses nuclear localization signals in addition to the classical SU(var)3-9, Enhancer-of-Zeste, Trithorax (SET), and post-SET domains. Altogether, these findings suggest that the function of HMT1 is critical for the success and timing of the encystation process, and reinforce the idea that epigenetic marks are critical for cyst formation in G. lamblia.
MeSH term(s)	Crystallography, X-Ray ; Data Mining ; Databases, Nucleic Acid ; Databases, Protein ; Epigenesis, Genetic ; Gene Expression Regulation, Developmental ; Giardia lamblia/enzymology ; Giardia lamblia/growth & development ; Histone-Lysine N-Methyltransferase/chemistry ; Histone-Lysine N-Methyltransferase/genetics ; Histone-Lysine N-Methyltransferase/metabolism ; Isoenzymes/chemistry ; Isoenzymes/genetics ; Isoenzymes/metabolism ; Lysine ; Models, Molecular ; Nuclear Localization Signals ; Parasite Encystment ; Phylogeny ; Protein Conformation ; Protein Transport ; Protozoan Proteins/chemistry ; Protozoan Proteins/genetics ; Protozoan Proteins/metabolism ; Recombinant Proteins/chemistry ; Recombinant Proteins/metabolism ; Sequence Homology, Amino Acid ; Structural Homology, Protein
Chemical Substances	Isoenzymes ; Nuclear Localization Signals ; Protozoan Proteins ; Recombinant Proteins ; Histone-Lysine N-Methyltransferase (EC 2.1.1.43) ; Lysine (K3Z4F929H6)
Language	English
Publishing date	2017-08
Publishing country	England
Document type	Journal Article
ZDB-ID	2173655-8
ISSN	1742-4658 ; 1742-464X
ISSN (online)	1742-4658
ISSN	1742-464X
DOI	10.1111/febs.14131
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Article ; Online: Lactoferrin and lactoferricin endocytosis halt Giardia cell growth and prevent infective cyst production.

Frontera, Lorena S / Moyano, Sofía / Quassollo, Gonzalo / Lanfredi-Rangel, Adriana / Rópolo, Andrea S / Touz, María C

Scientific reports

2018 Volume 8, Issue 1, Page(s) 18020

Abstract: Lactoferrin (LF) is an 80 KDa iron-binding glycoprotein that plays a significant role in the innate immune system and is considered to be an important microbicide molecule. It has been suggested to be effective in the treatment of giardiasis, an ... ...

Abstract	Lactoferrin (LF) is an 80 KDa iron-binding glycoprotein that plays a significant role in the innate immune system and is considered to be an important microbicide molecule. It has been suggested to be effective in the treatment of giardiasis, an intestinal disease caused by the protozoan parasite G. lamblia. However, the molecular mechanisms by which LF exerts its effect on this parasite are unknown. Most of the microbicidal activity of human or bovine LF (hLF or bLF) has been associated with the N-terminal region of the mature LF - lactoferricin (LFcin). LFcin is produced by pepsin cleavage of the native protein in vitro and likely in vivo. In this work, we analyse the participation of the endocytic machinery of G. lamblia in the internalization of bLF and bLFcin and their effects on cell homeostasis. Our results show that, when bLF or bLFcin are internalized by receptor-mediated endocytosis, cell growth stops, and morphological changes are produced in the trophozoites, which ultimately will produce immature cysts. Our findings contribute to disclose the fine mechanism by which bLF and bLFcin may function as an antigiardial molecule and why they have therapeutic potential to eradicate giardiasis.
MeSH term(s)	Animals ; Cattle ; Cell Proliferation/drug effects ; Cells, Cultured ; Cysts/metabolism ; Cysts/parasitology ; Cysts/pathology ; Cysts/prevention & control ; Dose-Response Relationship, Drug ; Endocytosis/physiology ; Giardia/drug effects ; Giardia/growth & development ; Giardia/metabolism ; Giardiasis/parasitology ; Giardiasis/pathology ; Humans ; Lactoferrin/pharmacokinetics ; Lactoferrin/pharmacology ; Protein Binding ; Receptors, LDL/metabolism
Chemical Substances	LTF protein, human ; Receptors, LDL ; lactoferricin B (146897-68-9) ; Lactoferrin (EC 3.4.21.-)
Language	English
Publishing date	2018-12-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-018-36563-1
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Article: The giardial ENTH protein participates in lysosomal protein trafficking and endocytosis.

Feliziani, Constanza / Zamponi, Nahuel / Gottig, Natalia / Rópolo, Andrea S / Lanfredi-Rangel, Adriana / Touz, Maria C

Biochimica et biophysica acta

2015 Volume 1853, Issue 3, Page(s) 646–659

Abstract: In the protozoa parasite Giardia lamblia, endocytosis and lysosomal protein trafficking are vital parasite-specific processes that involve the action of the adaptor complexes AP-1 and AP-2 and clathrin. In this work, we have identified a single gene in ... ...

Abstract	In the protozoa parasite Giardia lamblia, endocytosis and lysosomal protein trafficking are vital parasite-specific processes that involve the action of the adaptor complexes AP-1 and AP-2 and clathrin. In this work, we have identified a single gene in Giardia encoding a protein containing an ENTH domain that defines monomeric adaptor proteins of the epsin family. This domain is present in the epsin or epsin-related (epsinR) adaptor proteins, which are implicated in endocytosis and Golgi-to-endosome protein trafficking, respectively, in other eukaryotic cells. We found that GlENTHp (for G. lamblia ENTH protein) localized in the cytosol, strongly interacted with PI3,4,5P3, was associated with the alpha subunit of AP-2, clathrin and ubiquitin and was involved in receptor-mediated endocytosis. It also bonded PI4P, the gamma subunit of AP-1 and was implicated in ER-to-PV trafficking. Alteration of the GlENTHp function severely affected trophozoite growth showing an unusual accumulation of dense material in the lysosome-like peripheral vacuoles (PVs), indicating that GlENTHp might be implicated in the maintenance of PV homeostasis. In this study, we showed evidence suggesting that GlENTHp might function as a monomeric adaptor protein supporting the findings of other group indicating that GlENTHp might be placed at the beginning of the ENTH family.
MeSH term(s)	Amino Acid Sequence ; Animals ; Cells, Cultured ; Endocytosis/genetics ; Giardia lamblia/enzymology ; Giardia lamblia/genetics ; Giardia lamblia/metabolism ; Lysosomes/metabolism ; Mice ; Mice, Inbred BALB C ; Models, Molecular ; Molecular Sequence Data ; Organisms, Genetically Modified ; Protein Structure, Tertiary ; Protein Transport/genetics ; Sequence Homology, Amino Acid ; Thiolester Hydrolases/chemistry ; Thiolester Hydrolases/physiology
Chemical Substances	Thiolester Hydrolases (EC 3.1.2.-)
Language	English
Publishing date	2015-03
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	60-7
ISSN	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650
ISSN	0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbamcr.2014.12.034
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