Cooperativity of catalytic and lectin-like domain of Trypanosoma congolense trans-sialidase modulates its catalytic activity.

Acetylgalactosamine / metabolism Binding Sites Catalysis Galactose / metabolism Glycoproteins / chemistry Neuraminidase / chemistry Oligosaccharides / metabolism Protozoan Proteins / chemistry Sialic Acids / metabolism Trypanosoma congolense / chemistry

Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
02 2022
Historique:
received: 29 07 2021
accepted: 23 01 2022
revised: 23 02 2022
pubmed: 8 2 2022
medline: 12 3 2022
entrez: 7 2 2022
Statut: epublish

Résumé

Trans-sialidases (TS) represent a multi-gene family of unusual enzymes, which catalyse the transfer of terminal sialic acids (Sia) from sialoglycoconjugates to terminal galactose or N-acetylgalactosamine residues of oligosaccharides without the requirement of CMP-Neu5Ac, the activated Sia used by typical sialyltransferases. Enzymes comprise a N-terminal catalytic domain (CD) followed by a lectin-like domain (LD). Most work on trypanosomal TS has been done on enzymatic activities focusing on the CD of TS from Trypanosoma cruzi (causing Chagas disease in Latin America), subspecies of Trypanosoma brucei, (causing human sleeping sickness in Africa) and Trypanosoma congolense (causing African Animal Trypanosomosis in livestock). Previously, we demonstrated that T. congolense TS (TconTS)-LD binds to several carbohydrates, such as 1,4-β-mannotriose. In this study we investigated the influence of TconTS3-LD on Sia transfer efficiency of TconTS1a-CD by swapping domains. in silico analysis on structure models of TconTS enzymes revealed the potential of domain swaps between TconTS1a and TconTS3 without structural disruptions of the enzymes overall topologies. Recombinant domain swapped TconTS1a/TS3 showed clear Sia transfer activity, when using fetuin and lactose as Sia donor and acceptor substrates, respectively. While Sia transfer activity remained unchanged from the level of TconTS1a, hydrolytic release of free Neu5Ac as a side product was suppressed resulting in increased transfer efficiency. Presence of 1,4-β-mannotriose during TS reactions modulates enzyme activities enhancing transfer efficiency possibly due to occupation of the binding site in TconTS1a-LD. Interestingly this effect was in the same range as that observed when swapping TconTS1a-CD and TconTS3-LD. In summary, this study demonstrate the proof-of-principle for swapping CDs and LDs of TconTS and that TconTS3-LD influences enzymatic activity of TconTS1a-CD providing evidence that LDs play pivotal roles in modulating activities and biological functions of TconTS and possibly other TS.

Identifiants

DOI: 10.1371/journal.pntd.0009585 PMID: 35130274 PMC: PMC8865650
pubmed: 35130274
doi: 10.1371/journal.pntd.0009585
pii: PNTD-D-21-01140
pmc: PMC8865650
doi:

Substances chimiques

Glycoproteins 0
Oligosaccharides 0
Protozoan Proteins 0
Sialic Acids 0
trans-sialidase EC 3.2.1.-
Neuraminidase EC 3.2.1.18
Acetylgalactosamine KM15WK8O5T
Galactose X2RN3Q8DNE

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0009585

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist. Author Thaddeus Termulun Gbem was unable to confirm their authorship contributions. On their behalf, the corresponding author has reported their contributions to the best of their knowledge.

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Auteurs

Mario Waespy (M)

Centre for Biomolecular Interactions Bremen, Faculty for Biology and Chemistry, University Bremen, Bremen, Germany.
ORCID: 0000-0003-0039-5770

Thaddeus Termulun Gbem (TT)

Africa Centre of Excellence for Neglected Tropical Diseases and Forensic Biotechnology, Ahmadu Bello University, Zaria, Nigeria, Africa.
Department of Biology, Ahmadu Bello University, Zaria, Nigeria, Africa.
ORCID: 0000-0002-2366-0082

Nilima Dinesh Kumar (N)

Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, University of Groningen, Groningen, Netherlands.
ORCID: 0000-0003-2788-0303

Shanmugam Solaiyappan Mani (S)

Centre for Biomolecular Interactions Bremen, Faculty for Biology and Chemistry, University Bremen, Bremen, Germany.
ORCID: 0000-0002-9341-8187

Jana Rosenau (J)

Centre for Biomolecular Interactions Bremen, Faculty for Biology and Chemistry, University Bremen, Bremen, Germany.
ORCID: 0000-0003-2757-0786

Frank Dietz (F)

Centre for Biomolecular Interactions Bremen, Faculty for Biology and Chemistry, University Bremen, Bremen, Germany.

Sørge Kelm (S)

Centre for Biomolecular Interactions Bremen, Faculty for Biology and Chemistry, University Bremen, Bremen, Germany.
Africa Centre of Excellence for Neglected Tropical Diseases and Forensic Biotechnology, Ahmadu Bello University, Zaria, Nigeria, Africa.
ORCID: 0000-0001-5277-9421

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Classifications MeSH

Recherchemedicale.com › Glucides › Osamines › Hexosamine › Galactosamine › Acétyl-galactosamine › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Phénomènes chimiques › Phénomènes biochimiques › Sites de fixation › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Phénomènes chimiques › Catalyse › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Glucides › Sucres › Oses › Hexose › Galactose › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Glycoprotéines › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Enzymes et coenzymes › Enzymes › Hydrolases › Glycosidases › Sialidase › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Glucides › Polyosides › Oligosaccharides › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines de protozoaire › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Glucides › Oses acides › Acides neuraminiques › Acides sialiques › Cooperativity of catalytic and lectin-like...
Recherchemedicale.com › Eucaryotes › Euglénozoaires › Kinetoplastida › Trypanosomatina › Trypanosoma › Trypanosoma congolense › Cooperativity of catalytic and lectin-like...