Molecular Characterization of N-glycan Degradation and Transport in Streptococcus pneumoniae and Its Contribution to Virulence

Robb, Melissa; Hobbs, Joanne K.; Woodiga, Shireen A.; Shapiro-Ward, Sarah; Suits, Michael D. L.; McGregor, Nicholas; Brumer, Harry; Yesilkaya, Hasan; King, Samantha J.; Boraston, Alisdair B.

doi:10.1371/journal.ppat.1006090

Molecular Characterization of N-glycan Degradation and Transport in Streptococcus pneumoniae and Its Contribution to Virulence

Journal Article · Wed Jan 04 23:00:00 EST 2017 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1006090· OSTI ID:1903992

Robb, Melissa ^[1]; Hobbs, Joanne K. ^[2]; ^[3]; ^[2]; Suits, Michael D. L. ^[4]; McGregor, Nicholas ^[5]; Brumer, Harry ^[5]; Yesilkaya, Hasan ^[6]; ^[3]; Boraston, Alisdair B. ^[2]

Univ. of Victoria, BC (Canada); Max Planck Institute for Marine Microbiology (Germany); OSTI
Univ. of Victoria, BC (Canada)
Research Institute at Nationwide Children's Hospital, Columbus, OH (United States)
Univ. of Victoria, BC (Canada); , Wilfrid Laurier University, Waterloo, ON (Canada)
Univ. of British Columbia, Vancouver, BC (Canada)
Univ. of Leicester (United Kingdom)

The carbohydrate-rich coating of human tissues and cells provide a first point of contact for colonizing and invading bacteria. Commensurate with N-glycosylation being an abundant form of protein glycosylation that has critical functional roles in the host, some host-adapted bacteria possess the machinery to process N-linked glycans. The human pathogen Streptococcus pneumoniae depolymerizes complex N-glycans with enzymes that sequentially trim a complex N-glycan down to the Man₃GlcNAc₂ core prior to the release of the glycan from the protein by endo-β-N-acetylglucosaminidase (EndoD), which cleaves between the two GlcNAc residues. Here we examine the capacity of S. pneumoniae to process high-mannose N-glycans and transport the products. Through biochemical and structural analyses we demonstrate that S. pneumoniae also possesses an α-(1,2)-mannosidase (SpGH92). This enzyme has the ability to trim the terminal α-(1,2)-linked mannose residues of high-mannose N-glycans to generate Man₅GlcNAc₂. Through this activity SpGH92 is able to produce a substrate for EndoD, which is not active on high-mannose glycans with α-(1,2)-linked mannose residues. Binding studies and X-ray crystallography show that NgtS, the solute binding protein of an ABC transporter (ABC_NG), is able to bind Man₅GlcNAc, a product of EndoD activity, with high affinity. Finally, we evaluated the contribution of EndoD and ABC_NG to growth of S. pneumoniae on a model N-glycosylated glycoprotein, and the contribution of these enzymes and SpGH92 to virulence in a mouse model. We found that both EndoD and ABC_NG contribute to growth of S. pneumoniae, but that only SpGH92 and EndoD contribute to virulence. Therefore, N-glycan processing, but not transport of the released glycan, is required for full virulence in S. pneumoniae. To conclude, we synthesize our findings into a model of N-glycan processing by S. pneumoniae in which both complex and high-mannose N-glycans are targeted, and in which the two arms of this degradation pathway converge at ABC_NG.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1903992

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 1 Vol. 13; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (104)

Separation and analysis of the glycoform populations of ribonuclease B using capillary electrophoresis Rudd, Pauline M.; Scragg, Ian G.; Coghill, Eva Glycoconjugate Journal, Vol. 9, Issue 2 https://doi.org/10.1007/bf00731704	journal	April 1992
Mutational studies on endo-β-N-acetylglucosaminidase D which hydrolyzes core portion of asparagine-linked complex type oligosaccharides Yamamoto, Satoshi; Muramatsu, Hisako; Muramatsu, Takashi Glycoconjugate Journal, Vol. 22, Issue 1-2 https://doi.org/10.1007/s10719-005-0847-7	journal	February 2005
Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension Horton, Robert M.; Hunt, Henry D.; Ho, Steffan N. Gene, Vol. 77, Issue 1, p. 61-68 https://doi.org/10.1016/0378-1119(89)90359-4	journal	April 1989
A structural classification of substrate-binding proteins Berntsson, Ronnie P. -A.; Smits, Sander H. J.; Schmitt, Lutz FEBS Letters, Vol. 584, Issue 12 https://doi.org/10.1016/j.febslet.2010.04.043	journal	April 2010
Specific Recognition of Saturated and 4,5-Unsaturated Hexuronate Sugars by a Periplasmic Binding Protein Involved in Pectin Catabolism Abbott, D. Wade; Boraston, Alisdair B. Journal of Molecular Biology, Vol. 369, Issue 3 https://doi.org/10.1016/j.jmb.2007.03.045	journal	June 2007
How bacterial pathogens colonize their hosts and invade deeper tissues Ribet, David; Cossart, Pascale Microbes and Infection, Vol. 17, Issue 3 https://doi.org/10.1016/j.micinf.2015.01.004	journal	March 2015
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Inhibition of the Pneumococcal Virulence Factor StrH and Molecular Insights into N-Glycan Recognition and Hydrolysis Pluvinage, Benjamin; Higgins, Melanie A.; Abbott, D. Wade Structure, Vol. 19, Issue 11 https://doi.org/10.1016/j.str.2011.08.011	journal	November 2011
Pneumococcal carbohydrate transport: food for thought Buckwalter, Carolyn M.; King, Samantha J. Trends in Microbiology, Vol. 20, Issue 11 https://doi.org/10.1016/j.tim.2012.08.008	journal	November 2012
Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor Quiocho, Florante A.; Spurlino, John C.; Rodseth, Lynn E. Structure, Vol. 5, Issue 8 https://doi.org/10.1016/s0969-2126(97)00253-0	journal	August 1997
Carbohydrate–Aromatic Interactions Asensio, Juan Luis; Ardá, Ana; Cañada, Francisco Javier Accounts of Chemical Research, Vol. 46, Issue 4 https://doi.org/10.1021/ar300024d	journal	June 2012
The Extracellular Glycosidases of Diplococcus pneumoniae. I. Purification and Properties of a Neuraminidase and a β-Galactosidase. Action on the α₁-Acid Glycoprotein of Human Plasma^* Hughes, R. Colin; Jeanloz, Roger W. Biochemistry, Vol. 3, Issue 10 https://doi.org/10.1021/bi00898a025	journal	October 1964
Free R value: a novel statistical quantity for assessing the accuracy of crystal structures Brünger, Axel T. Nature, Vol. 355, Issue 6359 https://doi.org/10.1038/355472a0	journal	January 1992
Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism Cuskin, Fiona; Lowe, Elisabeth C.; Temple, Max J. Nature, Vol. 517, Issue 7533 https://doi.org/10.1038/nature13995	journal	January 2015
Mechanistic insights into a Ca2+-dependent family of α-mannosidases in a human gut symbiont Zhu, Yanping; Suits, Michael D. L.; Thompson, Andrew J. Nature Chemical Biology, Vol. 6, Issue 2 https://doi.org/10.1038/nchembio.278	journal	December 2009
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S. Nature Protocols, Vol. 3, Issue 7 https://doi.org/10.1038/nprot.2008.91	journal	June 2008
Proteome-wide post-translational modification statistics: frequency analysis and curation of the swiss-prot database Khoury, George A.; Baliban, Richard C.; Floudas, Christodoulos A. Scientific Reports, Vol. 1, Issue 1 https://doi.org/10.1038/srep00090	journal	September 2011
Structural analysis of the asparagine-linked oligosaccharides of human complement component C3 Hirani, S.; Lambris, J. D.; Müller-Eberhard, H. J. Biochemical Journal, Vol. 233, Issue 2 https://doi.org/10.1042/bj2330613	journal	January 1986
Efficient utilization of complex N-linked glycans is a selective advantage for Bacteroides fragilis in extraintestinal infections Cao, Y.; Rocha, E. R.; Smith, C. J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1407344111	journal	August 2014
α-Enolase, a Novel Strong Plasmin(ogen) Binding Protein on the Surface of Pathogenic Streptococci Pancholi, Vijaykumar; Fischetti, Vincent A. Journal of Biological Chemistry, Vol. 273, Issue 23 https://doi.org/10.1074/jbc.273.23.14503	journal	June 1998
Analysis of a New Family of Widely Distributed Metal-independent α-Mannosidases Provides Unique Insight into the Processing of N -Linked Glycans Gregg, Katie J.; Zandberg, Wesley F.; Hehemann, Jan-Hendrik Journal of Biological Chemistry, Vol. 286, Issue 17 https://doi.org/10.1074/jbc.m111.223172	journal	March 2011
A Novel Secreted Endoglycosidase from Enterococcus faecalis with Activity on Human Immunoglobulin G and Ribonuclease B Collin, Mattias; Fischetti, Vincent A. Journal of Biological Chemistry, Vol. 279, Issue 21 https://doi.org/10.1074/jbc.m402156200	journal	March 2004
Structural and Thermodynamic Analyses of Solute-binding Protein from Bifidobacterium longum Specific for Core 1 Disaccharide and Lacto-N-biose I Suzuki, Ryuichiro; Wada, Jun; Katayama, Takane Journal of Biological Chemistry, Vol. 283, Issue 19 https://doi.org/10.1074/jbc.m709777200	journal	May 2008
Streptococcus pneumoniae Endohexosaminidase D, Structural and Mechanistic Insight into Substrate-assisted Catalysis in Family 85 Glycoside Hydrolases Abbott, D. Wade; Macauley, Matthew S.; Vocadlo, David J. Journal of Biological Chemistry, Vol. 284, Issue 17 https://doi.org/10.1074/jbc.m809663200	journal	January 2009
The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion Uchiyama, Satoshi; Carlin, Aaron F.; Khosravi, Arya Journal of Experimental Medicine, Vol. 206, Issue 9 https://doi.org/10.1084/jem.20090386	journal	August 2009
STRING v10: protein–protein interaction networks, integrated over the tree of life Szklarczyk, Damian; Franceschini, Andrea; Wyder, Stefan Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1003	journal	October 2014
Molecular Cloning and Expression of Endo- -N-Acetylglucosaminidase D, Which Acts on the Core Structure of Complex Type Asparagine-Linked Oligosaccharides Muramatsu, H.; Tachikui, H.; Ushida, H. Journal of Biochemistry, Vol. 129, Issue 6 https://doi.org/10.1093/oxfordjournals.jbchem.a002938	journal	June 2001
BgaA acts as an adhesin to mediate attachment of some pneumococcal strains to human epithelial cells Limoli, Dominique H.; Sladek, Julie A.; Fuller, Lindsey A. Microbiology, Vol. 157, Issue 8 https://doi.org/10.1099/mic.0.045609-0	journal	August 2011
To have neighbour's fare: extending the molecular toolbox for Streptococcus pneumoniae Kloosterman, Tomas G.; Bijlsma, Jetta J. E.; Kok, Jan Microbiology, Vol. 152, Issue 2 https://doi.org/10.1099/mic.0.28521-0	journal	February 2006
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/s0907444905036693	journal	December 2005
Solving structures of protein complexes by molecular replacement with Phaser McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1 https://doi.org/10.1107/s0907444906045975	journal	December 2006
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/s0907444909042073	journal	December 2009
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/s0907444910048675	journal	March 2011
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/s0907444911001314	journal	March 2011
Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae King, Samantha J.; Hippe, Karen R.; Weiser, Jeffrey N. Molecular Microbiology, Vol. 59, Issue 3 https://doi.org/10.1111/j.1365-2958.2005.04984.x	journal	February 2006
The genome and surface proteome of Capnocytophaga canimorsus reveal a key role of glycan foraging systems in host glycoproteins deglycosylation: Sus-like systems of C. canimorsus Manfredi, Pablo; Renzi, Francesco; Mally, Manuela Molecular Microbiology, Vol. 81, Issue 4 https://doi.org/10.1111/j.1365-2958.2011.07750.x	journal	July 2011
Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont Sonnenburg, J. L. Science, Vol. 307, Issue 5717 https://doi.org/10.1126/science.1109051	journal	March 2005
Intracellular Functions of N-Linked Glycans Helenius, A. Science, Vol. 291, Issue 5512 https://doi.org/10.1126/science.291.5512.2364	journal	March 2001
An rpsL Cassette, Janus, for Gene Replacement through Negative Selection in Streptococcus pneumoniae Sung, C. K.; Li, H.; Claverys, J. P. Applied and Environmental Microbiology, Vol. 67, Issue 11 https://doi.org/10.1128/aem.67.11.5190-5196.2001	journal	November 2001
Identification of a Candidate Streptococcus pneumoniae Core Genome and Regions of Diversity Correlated with Invasive Pneumococcal Disease Obert, Caroline; Sublett, Jack; Kaushal, Deepak Infection and Immunity, Vol. 74, Issue 8 https://doi.org/10.1128/iai.00316-06	journal	August 2006
Three Surface Exoglycosidases from Streptococcus pneumoniae , NanA, BgaA, and StrH, Promote Resistance to Opsonophagocytic Killing by Human Neutrophils Dalia, Ankur B.; Standish, Alistair J.; Weiser, Jeffrey N. Infection and Immunity, Vol. 78, Issue 5 https://doi.org/10.1128/iai.01125-09	journal	May 2010
Identification of a Pneumococcal Glycosidase That Modifies O-Linked Glycans Marion, Carolyn; Limoli, Dominique H.; Bobulsky, Gregory S. Infection and Immunity, Vol. 77, Issue 4 https://doi.org/10.1128/iai.01215-08	journal	April 2009
Lactate Dehydrogenase Is the Key Enzyme for Pneumococcal Pyruvate Metabolism and Pneumococcal Survival in Blood Gaspar, Paula; Al-Bayati, Firas A. Y.; Andrew, Peter W. Infection and Immunity, Vol. 82, Issue 12 https://doi.org/10.1128/iai.02005-14	journal	December 2014
Identification of an ATPase, MsmK, Which Energizes Multiple Carbohydrate ABC Transporters in Streptococcus pneumoniae Marion, Carolyn; Aten, Andrew E.; Woodiga, Shireen A. Infection and Immunity, Vol. 79, Issue 10 https://doi.org/10.1128/iai.05290-11	journal	October 2011
Streptococcus pneumoniae Can Utilize Multiple Sources of Hyaluronic Acid for Growth Marion, Carolyn; Stewart, Jason M.; Tazi, Mia F. Infection and Immunity, Vol. 80, Issue 4 https://doi.org/10.1128/iai.05756-11	journal	April 2012
Effect of SpeB and EndoS from Streptococcus pyogenes on Human Immunoglobulins Collin, Mattias; Olsén, Arne Infection and Immunity, Vol. 69, Issue 11 https://doi.org/10.1128/iai.69.11.7187-7189.2001	journal	November 2001
Microarray Analysis of Pneumococcal Gene Expression during Invasive Disease Orihuela, Carlos J.; Radin, Jana N.; Sublett, Jack E. Infection and Immunity, Vol. 72, Issue 10 https://doi.org/10.1128/iai.72.10.5582-5596.2004	journal	October 2004
Glyceraldehyde-3-Phosphate Dehydrogenase of Streptococcus pneumoniae Is a Surface-Displayed Plasminogen-Binding Protein Bergmann, Simone; Rohde, Manfred; Hammerschmidt, Sven Infection and Immunity, Vol. 72, Issue 4 https://doi.org/10.1128/iai.72.4.2416-2419.2004	journal	April 2004
Growth of Streptococcus pneumoniae on Human Glycoconjugates Is Dependent upon the Sequential Activity of Bacterial Exoglycosidases Burnaugh, Amanda M.; Frantz, Laura J.; King, Samantha J. Journal of Bacteriology, Vol. 190, Issue 1 https://doi.org/10.1128/jb.01251-07	journal	January 2008
The ABC Transporter Encoded at the Pneumococcal Fructooligosaccharide Utilization Locus Determines the Ability To Utilize Long- and Short-Chain Fructooligosaccharides Linke, C. M.; Woodiga, S. A.; Meyers, D. J. Journal of Bacteriology, Vol. 195, Issue 5 https://doi.org/10.1128/jb.01560-12	journal	December 2012
Characterization of the Streptococcus pneumoniae BgaC Protein as a Novel Surface β-Galactosidase with Specific Hydrolysis Activity for the Galβ1-3GlcNAc Moiety of Oligosaccharides Jeong, Jae Kap; Kwon, Ohsuk; Lee, Yun Mi Journal of Bacteriology, Vol. 191, Issue 9 https://doi.org/10.1128/jb.01601-08	journal	May 2009
Localization of competence-induced proteins in Streptococcus pneumoniae Vijayakumar, M. N.; Morrison, D. A. Journal of Bacteriology, Vol. 165, Issue 3 https://doi.org/10.1128/jb.165.3.689-695.1986	journal	March 1986
Genetic Diversity of the Streptococcal Competence ( com ) Gene Locus Whatmore, Adrian M.; Barcus, Victoria A.; Dowson, Christopher G. Journal of Bacteriology, Vol. 181, Issue 10 https://doi.org/10.1128/jb.181.10.3144-3154.1999	journal	May 1999
Structure and Kinetic Investigation of Streptococcus pyogenes Family GH38 α-Mannosidase Suits, Michael D. L.; Zhu, Yanping; Taylor, Edward J. PLoS ONE, Vol. 5, Issue 2 https://doi.org/10.1371/journal.pone.0009006	journal	February 2010
A Functional Genomics Approach to Establish the Complement of Carbohydrate Transporters in Streptococcus pneumoniae Bidossi, Alessandro; Mulas, Laura; Decorosi, Francesca PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033320	journal	March 2012
The N-glycan Glycoprotein Deglycosylation Complex (Gpd) from Capnocytophaga canimorsus Deglycosylates Human IgG Renzi, Francesco; Manfredi, Pablo; Mally, Manuela PLoS Pathogens, Vol. 7, Issue 6 https://doi.org/10.1371/journal.ppat.1002118	journal	June 2011
Automated Structure Solution With autoSHARP Vonrhein, Clemens; Blanc, Eric; Roversi, Pietro Macromolecular Crystallography Protocols, Volume 2 https://doi.org/10.1385/1-59745-266-1:215	book	January 2006
Molecular pathogenesis of pneumococcal pneumonia McCullers, Jonathan, A. Frontiers in Bioscience, Vol. 6, Issue 1 https://doi.org/10.2741/mccullers	journal	January 2001
Separation and analysis of the glycoform populations of ribonuclease B using capillary electrophoresis Rudd, Pauline M.; Scragg, Ian G.; Coghill, Eva Glycoconjugate Journal, Vol. 9, Issue 2 https://doi.org/10.1007/BF00731704	journal	April 1992
The endothelial glycocalyx: composition, functions, and visualization Reitsma, Sietze; Slaaf, Dick W.; Vink, Hans Pflügers Archiv - European Journal of Physiology, Vol. 454, Issue 3 https://doi.org/10.1007/s00424-007-0212-8	journal	January 2007
A study of the genetic material determining an enzyme activity in Pneumococcus Lacks, Sanford; Hotchkiss, Rollin D. Biochimica et Biophysica Acta, Vol. 39, Issue 3 https://doi.org/10.1016/0006-3002(60)90205-5	journal	April 1960
Endo-β-N-acetylglucosaminidase Acting on Carbohydrate Moieties of Glycoproteins Koide, Norio; Muramatsu, Takashi Journal of Biological Chemistry, Vol. 249, Issue 15 https://doi.org/10.1016/S0021-9258(19)42406-X	journal	August 1974
Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor Quiocho, Florante A.; Spurlino, John C.; Rodseth, Lynn E. Structure, Vol. 5, Issue 8 https://doi.org/10.1016/S0969-2126(97)00253-0	journal	August 1997
A general, robust method for the quality control of intact proteins using LC–ESI-MS Sundqvist, Gustav; Stenvall, Maria; Berglund, Helena Journal of Chromatography B, Vol. 852, Issue 1-2 https://doi.org/10.1016/j.jchromb.2007.01.011	journal	June 2007
Blood Group Antigen Recognition by a Solute-Binding Protein from a Serotype 3 Strain of Streptococcus pneumoniae Higgins, Melanie A.; Abbott, D. Wade; Boulanger, Martin J. Journal of Molecular Biology, Vol. 388, Issue 2 https://doi.org/10.1016/j.jmb.2009.03.012	journal	May 2009
The Extracellular Glycosidases of Diplococcus pneumoniae. II. Purification and Properties of a β-N-Acetylglucosaminidase. Action on a Derivative of the α₁-Acid Glycoprotein of Human Plasma^* Hughes, R. Colin; Jeanloz, Roger W. Biochemistry, Vol. 3, Issue 10 https://doi.org/10.1021/bi00898a026	journal	October 1964
Binding Specificity and Thermodynamics of a Family 9 Carbohydrate-Binding Module from Thermotoga maritima Xylanase 10A ^† Boraston, Alisdair B.; Creagh, A. Louise; Alam, Md. Mustafa Biochemistry, Vol. 40, Issue 21 https://doi.org/10.1021/bi0101695	journal	May 2001
The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence Holmes, Ann R.; McNab, Roderick; Millsap, Kevin W. Molecular Microbiology, Vol. 41, Issue 6 https://doi.org/10.1046/j.1365-2958.2001.02610.x	journal	September 2001
Analysis of a New Family of Widely Distributed Metal-independent α-Mannosidases Provides Unique Insight into the Processing of N -Linked Glycans Gregg, Katie J.; Zandberg, Wesley F.; Hehemann, Jan-Hendrik Journal of Biological Chemistry, Vol. 286, Issue 17 https://doi.org/10.1074/jbc.M111.223172	journal	March 2011
A Second β-Hexosaminidase Encoded in the Streptococcus pneumoniae Genome Provides an Expanded Biochemical Ability to Degrade Host Glycans Robb, Melissa; Robb, Craig S.; Higgins, Melanie A. Journal of Biological Chemistry, Vol. 290, Issue 52 https://doi.org/10.1074/jbc.M115.688630	journal	December 2015
A Novel Secreted Endoglycosidase from Enterococcus faecalis with Activity on Human Immunoglobulin G and Ribonuclease B Collin, Mattias; Fischetti, Vincent A. Journal of Biological Chemistry, Vol. 279, Issue 21 https://doi.org/10.1074/jbc.M402156200	journal	March 2004
Streptococcus pneumoniae Endohexosaminidase D, Structural and Mechanistic Insight into Substrate-assisted Catalysis in Family 85 Glycoside Hydrolases Abbott, D. Wade; Macauley, Matthew S.; Vocadlo, David J. Journal of Biological Chemistry, Vol. 284, Issue 17 https://doi.org/10.1074/jbc.M809663200	journal	January 2009
The Role of Complement in the Host's Defense Against Streptococcus pneumoniae Winkelstein, J. A. Clinical Infectious Diseases, Vol. 3, Issue 2 https://doi.org/10.1093/clinids/3.2.289	journal	March 1981
Sequential deglycosylation and utilization of the N-linked, complex- type glycans of human alpha1-acid glycoprotein mediates growth of Streptococcus oralis Byers, H. Glycobiology, Vol. 9, Issue 5 https://doi.org/10.1093/glycob/9.5.469	journal	May 1999
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
Solving structures of protein complexes by molecular replacement with Phaser McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1 https://doi.org/10.1107/S0907444906045975	journal	December 2006
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Pneumococcal surface proteins: when the whole is greater than the sum of its parts Pérez-Dorado, I.; Galan-Bartual, S.; Hermoso, J. A. Molecular Oral Microbiology, Vol. 27, Issue 4 https://doi.org/10.1111/j.2041-1014.2012.00655.x	journal	June 2012
Pneumococcal neuraminidase A: an essential upper airway colonization factor for Streptococcus pneumoniae Brittan, J. L.; Buckeridge, T. J.; Finn, A. Molecular Oral Microbiology, Vol. 27, Issue 4 https://doi.org/10.1111/j.2041-1014.2012.00658.x	journal	July 2012
Pyruvate Formate Lyase Is Required for Pneumococcal Fermentative Metabolism and Virulence Yesilkaya, Hasan; Spissu, Francesca; Carvalho, Sandra M. Infection and Immunity, Vol. 77, Issue 12 https://doi.org/10.1128/IAI.00178-09	journal	December 2009
Identification of a Candidate Streptococcus pneumoniae Core Genome and Regions of Diversity Correlated with Invasive Pneumococcal Disease Obert, Caroline; Sublett, Jack; Kaushal, Deepak Infection and Immunity, Vol. 74, Issue 8 https://doi.org/10.1128/IAI.00316-06	journal	August 2006
Three Surface Exoglycosidases from Streptococcus pneumoniae , NanA, BgaA, and StrH, Promote Resistance to Opsonophagocytic Killing by Human Neutrophils Dalia, Ankur B.; Standish, Alistair J.; Weiser, Jeffrey N. Infection and Immunity, Vol. 78, Issue 5 https://doi.org/10.1128/IAI.01125-09	journal	May 2010
Identification of a Pneumococcal Glycosidase That Modifies O-Linked Glycans Marion, Carolyn; Limoli, Dominique H.; Bobulsky, Gregory S. Infection and Immunity, Vol. 77, Issue 4 https://doi.org/10.1128/IAI.01215-08	journal	April 2009
Lactate Dehydrogenase Is the Key Enzyme for Pneumococcal Pyruvate Metabolism and Pneumococcal Survival in Blood Gaspar, Paula; Al-Bayati, Firas A. Y.; Andrew, Peter W. Infection and Immunity, Vol. 82, Issue 12 https://doi.org/10.1128/IAI.02005-14	journal	December 2014
Identification of an ATPase, MsmK, Which Energizes Multiple Carbohydrate ABC Transporters in Streptococcus pneumoniae Marion, Carolyn; Aten, Andrew E.; Woodiga, Shireen A. Infection and Immunity, Vol. 79, Issue 10 https://doi.org/10.1128/IAI.05290-11	journal	October 2011
Streptococcus pneumoniae Can Utilize Multiple Sources of Hyaluronic Acid for Growth Marion, Carolyn; Stewart, Jason M.; Tazi, Mia F. Infection and Immunity, Vol. 80, Issue 4 https://doi.org/10.1128/IAI.05756-11	journal	April 2012
Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci Courtney, H. S.; Li, Y.; Dale, J. B. Infection and Immunity, Vol. 62, Issue 9 https://doi.org/10.1128/IAI.62.9.3937-3946.1994	journal	September 1994
Large-Scale Identification of Virulence Genes from Streptococcus pneumoniae Polissi, Alessandra; Pontiggia, Andrea; Feger, Georg Infection and Immunity, Vol. 66, Issue 12 https://doi.org/10.1128/IAI.66.12.5620-5629.1998	journal	December 1998
Effect of SpeB and EndoS from Streptococcus pyogenes on Human Immunoglobulins Collin, Mattias; Olsén, Arne Infection and Immunity, Vol. 69, Issue 11 https://doi.org/10.1128/IAI.69.11.7187-7189.2001	journal	November 2001
Microarray Analysis of Pneumococcal Gene Expression during Invasive Disease Orihuela, Carlos J.; Radin, Jana N.; Sublett, Jack E. Infection and Immunity, Vol. 72, Issue 10 https://doi.org/10.1128/IAI.72.10.5582-5596.2004	journal	October 2004
Glyceraldehyde-3-Phosphate Dehydrogenase of Streptococcus pneumoniae Is a Surface-Displayed Plasminogen-Binding Protein Bergmann, Simone; Rohde, Manfred; Hammerschmidt, Sven Infection and Immunity, Vol. 72, Issue 4 https://doi.org/10.1128/IAI.72.4.2416-2419.2004	journal	April 2004
Growth of Streptococcus pneumoniae on Human Glycoconjugates Is Dependent upon the Sequential Activity of Bacterial Exoglycosidases Burnaugh, Amanda M.; Frantz, Laura J.; King, Samantha J. Journal of Bacteriology, Vol. 190, Issue 1 https://doi.org/10.1128/JB.01251-07	journal	January 2008
The ABC Transporter Encoded at the Pneumococcal Fructooligosaccharide Utilization Locus Determines the Ability To Utilize Long- and Short-Chain Fructooligosaccharides Linke, C. M.; Woodiga, S. A.; Meyers, D. J. Journal of Bacteriology, Vol. 195, Issue 5 https://doi.org/10.1128/JB.01560-12	journal	December 2012
Characterization of the Streptococcus pneumoniae BgaC Protein as a Novel Surface β-Galactosidase with Specific Hydrolysis Activity for the Galβ1-3GlcNAc Moiety of Oligosaccharides Jeong, Jae Kap; Kwon, Ohsuk; Lee, Yun Mi Journal of Bacteriology, Vol. 191, Issue 9 https://doi.org/10.1128/JB.01601-08	journal	May 2009
Genetic Requirement for Pneumococcal Ear Infection Chen, Huaiqing; Ma, Yueyun; Yang, Jun PLoS ONE, Vol. 3, Issue 8 https://doi.org/10.1371/journal.pone.0002950	journal	August 2008
Peptidoglycan Branched Stem Peptides Contribute to Streptococcus pneumoniae Virulence by Inhibiting Pneumolysin Release Greene, Neil G.; Narciso, Ana R.; Filipe, Sergio R. PLOS Pathogens, Vol. 11, Issue 6 https://doi.org/10.1371/journal.ppat.1004996	journal	June 2015
Molecular pathogenesis of pneumococcal pneumonia McCullers, Jonathan A. Frontiers in Bioscience, Vol. 6, Issue 3 https://doi.org/10.2741/A649	journal	January 2001

Cited By (4)

A bioactive mammalian disaccharide associated with autoimmunity activates STING-TBK1-dependent immune response Fermaintt, Charles S.; Sano, Kanae; Liu, Zhida Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10319-5	journal	May 2019
The Human Lung Glycome Reveals Novel Glycan Ligands for Influenza A Virus Jia, Nan; Byrd-Leotis, Lauren; Matsumoto, Yasuyuki Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-62074-z	journal	March 2020
Unique Microbial Catabolic Pathway for the Human Core N -Glycan Constituent Fucosyl-α-1,6- N -Acetylglucosamine-Asparagine Becerra, Jimmy E.; Rodríguez-Díaz, Jesús; Gozalbo-Rovira, Roberto mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mbio.02804-19	journal	February 2020
Host-glycan metabolism is regulated by a species-conserved two-component system in Streptococcus pneumoniae Andreassen, Patrick Rosendahl; Trappetti, Claudia; Minhas, Vikrant PLOS Pathogens, Vol. 16, Issue 3 https://doi.org/10.1371/journal.ppat.1008332	journal	March 2020

Similar Records

Isolation of a mutant Arabidopsis plant that lacks N-aetyl glucosaminyl transferase I and is unable to synthesize Golgi-modified complex N-linked glycans

Journal Article · Sun Aug 01 00:00:00 EDT 1993 · Plant Physiology; (United States) · OSTI ID:5815233

Mammalian O-mannosylation of cadherins and plexins is independent of protein O-mannosyltransferases 1 and 2

Journal Article · Tue May 16 00:00:00 EDT 2017 · Journal of Biological Chemistry · OSTI ID:1406611

Subcellular localization of glycosidases and glycosyltransferases involved in the processing of N-linked oligosaccharides

Journal Article · Sat Oct 31 23:00:00 EST 1987 · Plant Physiol.; (United States) · OSTI ID:5642213

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
carbohydrates
crystal structure
gene prediction
host-pathogen interactions
mannose
mouse models
pneumococcus
ribonucleases

Molecular Characterization of N-glycan Degradation and Transport in Streptococcus pneumoniae and Its Contribution to Virulence

Citation Formats

References (104)

Cited By (4)

Similar Records

Related Subjects