Insights into the structure and function of membrane-integrated processive glycosyltransferases

Bi, Yunchen; Hubbard, Caitlin; Purushotham, Pallinti; Zimmer, Jochen

doi:10.1016/j.sbi.2015.07.008

Title: Insights into the structure and function of membrane-integrated processive glycosyltransferases

Abstract

Complex carbohydrates perform essential functions in life, including energy storage, cell signaling, protein targeting, quality control, as well as supporting cell structure and stability. Extracellular polysaccharides (EPS) represent mainly structural polymers and are found in essentially all kingdoms of life. For example, EPS are important biofilm and capsule components in bacteria, represent major constituents in cell walls of fungi, algae, arthropods and plants, and modulate the extracellular matrix in vertebrates. Different mechanisms evolved by which EPS are synthesized. In this paper, we review the structures and functions of membrane-integrated processive glycosyltransferases (GTs) implicated in the synthesis and secretion of chitin, alginate, hyaluronan and poly-N-acetylglucosamine (PNAG).

Authors:

^[1]; Hubbard, Caitlin ^[1]; Purushotham, Pallinti ^[1]; Zimmer, Jochen ^[1]

Univ. of Virginia, Charlottesville, VA (United States)

Publication Date:: Wed Sep 02 00:00:00 EDT 2015

Research Org.:: Univ. of Virginia, Charlottesville, VA (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1344504

Alternate Identifier(s):: OSTI ID: 1250108

Grant/Contract Number:: SC0001090

Resource Type:: Journal Article: Accepted Manuscript

Journal Name:: Current Opinion in Structural Biology

Additional Journal Information:: Journal Volume: 34; Journal ID: ISSN 0959-440X

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Bi, Yunchen, Hubbard, Caitlin, Purushotham, Pallinti, and Zimmer, Jochen. Insights into the structure and function of membrane-integrated processive glycosyltransferases.  United States: N. p., 2015. 
        Web.  doi:10.1016/j.sbi.2015.07.008.

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                    Bi, Yunchen, Hubbard, Caitlin, Purushotham, Pallinti, & Zimmer, Jochen. Insights into the structure and function of membrane-integrated processive glycosyltransferases.  United States.  https://doi.org/10.1016/j.sbi.2015.07.008

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                    Bi, Yunchen, Hubbard, Caitlin, Purushotham, Pallinti, and Zimmer, Jochen. 2015.  
        "Insights into the structure and function of membrane-integrated processive glycosyltransferases".  United States.  https://doi.org/10.1016/j.sbi.2015.07.008.  https://www.osti.gov/servlets/purl/1344504.

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@article{osti_1344504,

  title        = {Insights into the structure and function of membrane-integrated processive glycosyltransferases},

  author       = {Bi, Yunchen and Hubbard, Caitlin and Purushotham, Pallinti and Zimmer, Jochen},

  abstractNote = {Complex carbohydrates perform essential functions in life, including energy storage, cell signaling, protein targeting, quality control, as well as supporting cell structure and stability. Extracellular polysaccharides (EPS) represent mainly structural polymers and are found in essentially all kingdoms of life. For example, EPS are important biofilm and capsule components in bacteria, represent major constituents in cell walls of fungi, algae, arthropods and plants, and modulate the extracellular matrix in vertebrates. Different mechanisms evolved by which EPS are synthesized. In this paper, we review the structures and functions of membrane-integrated processive glycosyltransferases (GTs) implicated in the synthesis and secretion of chitin, alginate, hyaluronan and poly-N-acetylglucosamine (PNAG).},

  doi          = {10.1016/j.sbi.2015.07.008},

  url          = {https://www.osti.gov/biblio/1344504},
  journal      = {Current Opinion in Structural Biology},

  issn         = {0959-440X},

  number       = ,

  volume       = 34,

  place        = {United States},

  year         = {Wed Sep 02 00:00:00 EDT 2015},

  month        = {Wed Sep 02 00:00:00 EDT 2015}

}

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The considerable utility of glycoside phosphorylases (GPs) has led to substantial efforts over the past two decades to expand the breadth of known GP activities. Driven largely by the increase of available genomic DNA sequence data, the gap between the number of sequences in the carbohydrate active enzyme database (CAZy DB) and its functionally characterized members continues to grow. This wealth of sequence data presented an exciting opportunity to explore the ever-expanding CAZy DB to discover new GPs with never-before-described functionalities. Utilizing an in silico sequence analysis of CAZy family GH94, we discovered and then functionally and structurally characterized themore »« less
https://doi.org/10.1021/acscentsci.1c01570
The TPR domain of PgaA is a multifunctional scaffold that binds PNAG and modulates PgaB-dependent polymer processing

Journal Article Pfoh, Roland; Subramanian, Adithya; Huang, Jingjing; ... - PLoS Pathogens

The synthesis of exopolysaccharides as biofilm matrix components by pathogens is a crucial factor for chronic infections and antibiotic resistance. Many periplasmic proteins involved in polymer processing and secretion in Gram-negative synthase dependent exopolysaccharide biosynthetic systems have been individually characterized. The operons responsible for the production of PNAG, alginate, cellulose and the Pel polysaccharide each contain a gene that encodes an outer membrane associated tetratricopeptide repeat (TPR) domain containing protein. While the TPR domain has been shown to bind other periplasmic proteins, the functional consequences of these interactions for the polymer remain poorly understood. Herein, we show that the C-terminalmore »« less
https://doi.org/10.1371/journal.ppat.1010750

Full Text Available
Glycosyltransferase family 47 (GT47) proteins in plants and animals

Journal Article Zhang, Liang; Prabhakar, Pradeep Kumar; Bharadwaj, Vivek S; ... - Essays in Biochemistry

Glycosyltransferases (GTs) are carbohydrate-active enzymes that are encoded by the genomes of organisms spanning all domains of life. GTs catalyze glycosidic bond formation, transferring a sugar monomer from an activated donor to an acceptor substrate, often another saccharide. GTs from family 47 (GT47, PF03016) are involved in the synthesis of complex glycoproteins in mammals and insects and play a major role in the synthesis of almost every class of polysaccharide in plants, with the exception of cellulose, callose, and mixed linkage β-1,3/1,4-glucan. GT47 enzymes adopt a GT-B fold and catalyze the formation of glycosidic bonds through an inverting mechanism. Unlikemore »« less
https://doi.org/10.1042/ebc20220152

Full Text Available
Solid-State NMR Investigations of Extracellular Matrixes and Cell Walls of Algae, Bacteria, Fungi, and Plants

Journal Article Ghassemi, Nader; Poulhazan, Alexandre; Deligey, Fabien; ... - Chemical Reviews

Extracellular matrixes (ECMs), such as the cell walls and biofilms, are important for supporting cell integrity and function and regulating intercellular communication. These biomaterials are also of significant interest to the production of biofuels and the development of antimicrobial treatment. Solid-state nuclear magnetic resonance (ssNMR) and magic-angle spinning-dynamic nuclear polarization (MAS-DNP) are uniquely powerful for understanding the conformational structure, dynamical characteristics, and supramolecular assemblies of carbohydrates and other biomolecules in ECMs. This review highlights the recent high-resolution investigations of intact ECMs and native cells in many organisms spanning across plants, bacteria, fungi, and algae. We spotlight the structural principles identifiedmore »« less
https://doi.org/10.1021/acs.chemrev.1c00669
Bismuth Dimercaptopropanol (BisBAL) Inhibits the Expression of Extracellular Polysaccharides and Proteins by Brevundimonas diminuta: Implications for Membrane Microfiltration

Journal Article Badireddy, Appala; Chellam, Shankararaman; Yanina, Svetlana; ... - Biotechnology and Bioengineering, 99(3):634-643

A 2:1 molar ratio preparation of bismuth with a lipophilic dithiol (3-dimercapto-1-propanol, BAL)significantly reduced extracellular polymeric substances (EPS) expression by Brevundimonas diminuta in suspended cultures at levels just below the minimum inhibitory concentration (MIC). Total polysaccharides and proteins secreted by B. diminuta decreased by approximately 95% over a 5-day period when exposed to the bismuth-BAL chelate (BisBAL) at near MIC (12 μM). Fourier-transform infrared spectroscopy (FTIR) suggested that a possible mechanism of biofilm disruption by BisBAL is the inhibition of carbohydrate Oacetylation. FTIR also revealed extensive homology between EPS samples with and without BisBAL treatment, with proteins, polysaccharides, and peptidesmore »« less
https://doi.org/10.1002/bit.21615

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Title: Insights into the structure and function of membrane-integrated processive glycosyltransferases

Abstract

Citation Formats

Glycosyltransferases: Structures, Functions, and Mechanisms journal, June 2008

The Cell Biology of Cellulose Synthesis journal, April 2014

A Molecular Description of Cellulose Biosynthesis journal, June 2015

Crystallographic snapshot of cellulose synthesis and membrane translocation journal, December 2012

Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP journal, April 2014

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal, January 2009

BcsA and BcsB form the catalytically active core of bacterial cellulose synthase sufficient for in vitro cellulose synthesis journal, October 2013

Characterization of the Purified Hyaluronan Synthase from Streptococcus equisimilis † journal, July 2004

Insect chitin synthases: a review journal, August 2005

The Hyaluronan Synthase Catalyzes the Synthesis and Membrane Translocation of Hyaluronan journal, April 2012

Purification and Lipid Dependence of the Recombinant Hyaluronan Synthases from Streptococcus pyogenes andStreptococcus equisimilis journal, February 1999

A Structural and Biochemical Model of Processive Chitin Synthesis journal, August 2014

Structure–function characterization of cellulose synthase: relationship to other glycosyltransferases journal, August 2001

Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi journal, January 2002

Chitin Oligosaccharide Synthesis by Rhizobia and Zebrafish Embryos Starts by Glycosyl Transfer to O4 of the Reducing-Terminal Residue † journal, March 1999

Molecular directionality of β-chitin biosynthesis journal, February 1999

The structure of α-chitin journal, April 1978

The cellular basis of chitin synthesis in fungi and insects: Common principles and differences journal, September 2011

Update on Mechanisms of Plant Cell Wall Biosynthesis: How Plants Make Cellulose and Other (1→4)-β-d-Glycans journal, November 2010

Genetics and Molecular Biology of Chitin Synthesis in Fungi journal, October 1993

Similar and different domains of chitin synthases 1 and 2 ofS. cerevisiae: Two isozymes with distinct functions journal, November 1989

Saccharomyces cerevisiae chitin biosynthesis activation by N-acetylchitooses depends on size and structure of chito-oligosaccharides journal, October 2011

The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle journal, July 1991

Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites journal, September 2009

Yeast chitin synthase 2 activity is modulated by proteolysis and phosphorylation journal, December 2008

The genetic complexity of chitin synthesis in fungi journal, September 2002

The magic glue hyaluronan and its eraser hyaluronidase: A biological overview journal, May 2007

Hyaluronan Synthases: A Decade-plus of Novel Glycosyltransferases journal, November 2007

Hyaluronan: from extracellular glue to pericellular cue journal, July 2004

Hyaluronidase and its substrate hyaluronan: biochemistry, biological activities and therapeutic uses journal, September 1998

Microbial glycosaminoglycan glycosyltransferases journal, January 2002

Hyaluronan Synthase of Chlorella Virus PBCV-1 journal, December 1997

Molecular Cloning, Expression, and Characterization of the Authentic Hyaluronan Synthase from Group C Streptococcus equisimilis journal, December 1997

The Active Streptococcal Hyaluronan Synthases (HASs) Contain a Single HAS Monomer and Multiple Cardiolipin Molecules journal, October 1998

Molecular cloning, identification, and sequence of the hyaluronan synthase gene from group A Streptococcus pyogenes. journal, September 1993

Identification and Molecular Cloning of a Unique Hyaluronan Synthase from Pasteurella multocida journal, April 1998

Synthesis of hyaluronate in differentiated teratocarcinoma cells. Mechanism of chain growth journal, April 1983

Hyaluronan Biosynthesis by Class I Streptococcal Hyaluronan Synthases Occurs at the Reducing End journal, April 2005

Biosynthesis of hyaluronan: direction of chain elongation journal, August 2006

Hyaluronan synthase assembles chitin oligomers with -GlcNAc( 1->)UDP at the reducing end journal, January 2015

Biosynthesis of Hyaluronan journal, March 2005

Three Isoforms of Mammalian Hyaluronan Synthases Have Distinct Enzymatic Properties journal, August 1999

Expression of human hyaluronan synthases in response to external stimuli journal, May 2000

Metabolic engineering of Escherichia coli for biosynthesis of hyaluronic acid journal, January 2008

Mutation of Two Intramembrane Polar Residues Conserved within the Hyaluronan Synthase Family Alters Hyaluronan Product Size journal, April 2006

Alteration of Polysaccharide Size Distribution of a Vertebrate Hyaluronan Synthase by Mutation journal, May 2003

Transcriptional and post-translational regulation of hyaluronan synthesis: Regulation of hyaluronan synthesis journal, March 2011

The Activity of Hyaluronan Synthase 2 Is Regulated by Dimerization and Ubiquitination journal, July 2010

Recombinant human hyaluronan synthase 3 is phosphorylated in mammalian cells journal, May 2006

Role of UDP-N-Acetylglucosamine (GlcNAc) and O-GlcNAcylation of Hyaluronan Synthase 2 in the Control of Chondroitin Sulfate and Hyaluronan Synthesis journal, October 2012

Biosynthesis of alginate. Epimerisation of d-mannuronic to l-guluronic acid residues in the polymer chain journal, December 1969

The dual roles of AlgG in C-5-epimerization and secretion of alginate polymers in Pseudomonas aeruginosa: Alginate secretion in P. aeruginosa journal, February 2003

Characterization of Mannuronan C-5-Epimerase Genes from the Brown Alga Laminaria digitata journal, October 2003

Uronic acid sequence in alginate from different sources journal, February 1974

Localization of O-Acetyl Groups of Bacterial Alginate journal, February 1977

Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria journal, February 2013

Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization journal, June 2008

Structural basis for alginate secretion across the bacterial outer membrane journal, July 2011

Deletion of algK in Mucoid Pseudomonas aeruginosa Blocks Alginate Polymer Formation and Results in Uronic Acid Secretion journal, February 1998

Insights into the Assembly of the Alginate Biosynthesis Machinery in Pseudomonas aeruginosa journal, May 2013

Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa journal, June 2006

Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger journal, March 2013

Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid journal, January 1987

The pgaABCD Locus of Acinetobacter baumannii Encodes the Production of Poly-β-1-6- N -Acetylglucosamine, Which Is Critical for Biofilm Formation journal, October 2009

Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects journal, February 2015

Roles of pgaABCD Genes in Synthesis, Modification, and Export of the Escherichia coli Biofilm Adhesin Poly- -1,6-N-Acetyl-D-Glucosamine journal, March 2008

The pgaABCD Locus of Escherichia coli Promotes the Synthesis of a Polysaccharide Adhesin Required for Biofilm Formation journal, May 2004

Structural Basis for the De-N-acetylation of Poly-β-1,6-N-acetyl-d-glucosamine in Gram-positive Bacteria journal, December 2014

Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein–protein interaction journal, November 2012

Topological Organization of the Hyaluronan Synthase fromStreptococcus pyogenes journal, January 2001

TOPCONS: consensus prediction of membrane protein topology journal, May 2009

Clustal W and Clustal X version 2.0 journal, September 2007

Mineral-Chitin Composites in Molluscs book, January 2019

Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression journal, July 2019

The chaperone Chs7 forms a stable complex with Chs3 and promotes its activity at the cell surface journal, March 2018

The Complex Interplay Between Extracellular Matrix and Cells in Tissues book, January 2019

Differences in protein structural regions that impact functional specificity in GT2 family β-glucan synthases journal, October 2019

Glycosyltransferases: Structures, Functions, and Mechanisms
journal, June 2008

The Cell Biology of Cellulose Synthesis
journal, April 2014

A Molecular Description of Cellulose Biosynthesis
journal, June 2015

Crystallographic snapshot of cellulose synthesis and membrane translocation
journal, December 2012

Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP
journal, April 2014

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

BcsA and BcsB form the catalytically active core of bacterial cellulose synthase sufficient for in vitro cellulose synthesis
journal, October 2013

Characterization of the Purified Hyaluronan Synthase from Streptococcus equisimilis ^†
journal, July 2004

Insect chitin synthases: a review
journal, August 2005

The Hyaluronan Synthase Catalyzes the Synthesis and Membrane Translocation of Hyaluronan
journal, April 2012

Purification and Lipid Dependence of the Recombinant Hyaluronan Synthases from Streptococcus pyogenes andStreptococcus equisimilis
journal, February 1999

A Structural and Biochemical Model of Processive Chitin Synthesis
journal, August 2014

Structure–function characterization of cellulose synthase: relationship to other glycosyltransferases
journal, August 2001

Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi
journal, January 2002

Chitin Oligosaccharide Synthesis by Rhizobia and Zebrafish Embryos Starts by Glycosyl Transfer to O4 of the Reducing-Terminal Residue ^†
journal, March 1999

Molecular directionality of β-chitin biosynthesis
journal, February 1999

The structure of α-chitin
journal, April 1978

The cellular basis of chitin synthesis in fungi and insects: Common principles and differences
journal, September 2011

Update on Mechanisms of Plant Cell Wall Biosynthesis: How Plants Make Cellulose and Other (1→4)-β-d-Glycans
journal, November 2010

Genetics and Molecular Biology of Chitin Synthesis in Fungi
journal, October 1993

Similar and different domains of chitin synthases 1 and 2 ofS. cerevisiae: Two isozymes with distinct functions
journal, November 1989

Saccharomyces cerevisiae chitin biosynthesis activation by N-acetylchitooses depends on size and structure of chito-oligosaccharides
journal, October 2011

The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle
journal, July 1991

Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites
journal, September 2009

Yeast chitin synthase 2 activity is modulated by proteolysis and phosphorylation
journal, December 2008

The genetic complexity of chitin synthesis in fungi
journal, September 2002

The magic glue hyaluronan and its eraser hyaluronidase: A biological overview
journal, May 2007

Hyaluronan Synthases: A Decade-plus of Novel Glycosyltransferases
journal, November 2007

Hyaluronan: from extracellular glue to pericellular cue
journal, July 2004

Hyaluronidase and its substrate hyaluronan: biochemistry, biological activities and therapeutic uses
journal, September 1998

Microbial glycosaminoglycan glycosyltransferases
journal, January 2002

Hyaluronan Synthase of Chlorella Virus PBCV-1
journal, December 1997

Molecular Cloning, Expression, and Characterization of the Authentic Hyaluronan Synthase from Group C Streptococcus equisimilis
journal, December 1997

The Active Streptococcal Hyaluronan Synthases (HASs) Contain a Single HAS Monomer and Multiple Cardiolipin Molecules
journal, October 1998

Molecular cloning, identification, and sequence of the hyaluronan synthase gene from group A Streptococcus pyogenes.
journal, September 1993

Identification and Molecular Cloning of a Unique Hyaluronan Synthase from Pasteurella multocida
journal, April 1998

Synthesis of hyaluronate in differentiated teratocarcinoma cells. Mechanism of chain growth
journal, April 1983

Hyaluronan Biosynthesis by Class I Streptococcal Hyaluronan Synthases Occurs at the Reducing End
journal, April 2005

Biosynthesis of hyaluronan: direction of chain elongation
journal, August 2006

Hyaluronan synthase assembles chitin oligomers with -GlcNAc( 1->)UDP at the reducing end
journal, January 2015

Biosynthesis of Hyaluronan
journal, March 2005

Three Isoforms of Mammalian Hyaluronan Synthases Have Distinct Enzymatic Properties
journal, August 1999

Expression of human hyaluronan synthases in response to external stimuli
journal, May 2000

Metabolic engineering of Escherichia coli for biosynthesis of hyaluronic acid
journal, January 2008

Mutation of Two Intramembrane Polar Residues Conserved within the Hyaluronan Synthase Family Alters Hyaluronan Product Size
journal, April 2006

Alteration of Polysaccharide Size Distribution of a Vertebrate Hyaluronan Synthase by Mutation
journal, May 2003

Transcriptional and post-translational regulation of hyaluronan synthesis: Regulation of hyaluronan synthesis
journal, March 2011

The Activity of Hyaluronan Synthase 2 Is Regulated by Dimerization and Ubiquitination
journal, July 2010

Recombinant human hyaluronan synthase 3 is phosphorylated in mammalian cells
journal, May 2006

Role of UDP-N-Acetylglucosamine (GlcNAc) and O-GlcNAcylation of Hyaluronan Synthase 2 in the Control of Chondroitin Sulfate and Hyaluronan Synthesis
journal, October 2012

Biosynthesis of alginate. Epimerisation of d-mannuronic to l-guluronic acid residues in the polymer chain
journal, December 1969

The dual roles of AlgG in C-5-epimerization and secretion of alginate polymers in Pseudomonas aeruginosa: Alginate secretion in P. aeruginosa
journal, February 2003

Characterization of Mannuronan C-5-Epimerase Genes from the Brown Alga Laminaria digitata
journal, October 2003

Uronic acid sequence in alginate from different sources
journal, February 1974

Localization of O-Acetyl Groups of Bacterial Alginate
journal, February 1977

Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria
journal, February 2013

Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization
journal, June 2008

Structural basis for alginate secretion across the bacterial outer membrane
journal, July 2011

Deletion of algK in Mucoid Pseudomonas aeruginosa Blocks Alginate Polymer Formation and Results in Uronic Acid Secretion
journal, February 1998

Insights into the Assembly of the Alginate Biosynthesis Machinery in Pseudomonas aeruginosa
journal, May 2013

Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa
journal, June 2006

Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger
journal, March 2013

Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid
journal, January 1987

The pgaABCD Locus of Acinetobacter baumannii Encodes the Production of Poly-β-1-6- N -Acetylglucosamine, Which Is Critical for Biofilm Formation
journal, October 2009

Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects
journal, February 2015

Roles of pgaABCD Genes in Synthesis, Modification, and Export of the Escherichia coli Biofilm Adhesin Poly- -1,6-N-Acetyl-D-Glucosamine
journal, March 2008

The pgaABCD Locus of Escherichia coli Promotes the Synthesis of a Polysaccharide Adhesin Required for Biofilm Formation
journal, May 2004

Structural Basis for the De-N-acetylation of Poly-β-1,6-N-acetyl-d-glucosamine in Gram-positive Bacteria
journal, December 2014

Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein–protein interaction
journal, November 2012

Topological Organization of the Hyaluronan Synthase fromStreptococcus pyogenes
journal, January 2001

TOPCONS: consensus prediction of membrane protein topology
journal, May 2009

Clustal W and Clustal X version 2.0
journal, September 2007

Mineral-Chitin Composites in Molluscs
book, January 2019

Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression
journal, July 2019

The chaperone Chs7 forms a stable complex with Chs3 and promotes its activity at the cell surface
journal, March 2018

The Complex Interplay Between Extracellular Matrix and Cells in Tissues
book, January 2019

Differences in protein structural regions that impact functional specificity in GT2 family β-glucan synthases
journal, October 2019

Hyaluronan synthase control of synthesis rate and hyaluronan product size are independent functions differentially affected by mutations in a conserved tandem B-X ₇ -B motif
journal, August 2016

Biosynthesis of Hyaluronic acid polymer: Dissecting the role of sub structural elements of hyaluronan synthase
journal, August 2019

Differences in protein structural regions that impact functional specificity in GT2 family β- Glucan synthases
text, January 2021