The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
Housekeeping enzymes as virulence factors for pathogens
Abstract
Housekeeping enzymes are ubiquitously present in almost all living beings to perform essential metabolic functions for the purpose of survival. These enzymes have been characterized in detail for many years. In recent years, there has been a number of reports indicating that some of these enzymes perform a variety of other functions. In case of many pathogens, certain enzymes play a role to enhance virulence. To perform such a function, enzymes must be located on the surface of pathogens. Although they do not have the typical signal sequence or membrane anchoring mechanisms, they do get secreted and are displayed on the surface, probably by their reassociation. Once on the surface, these enzymes interact with host components, such as fibronectin and plasminogen, or interact directly with the host cells, to trigger signal transduction and thereby enable the pathogens to colonize, persist and invade the host tissue. Therefore, certain housekeeping enzymes may act as putative virulence factors and targets for the development of new strategies to control the infection by using agents that can block their secretion and/or reassociation.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“For example, enolase and glyceraldehyde-3-phosphate dehydrogenase are well-known metabolic enzymes that also act as RNA-binding proteins or surface adhesins in diverse bacterial species (33, 34).”
From Adaptive evolution of Pseudomonas putida in the presence of fluoride exposes novel functions of a benzoate transporter (2026) · cites this paper as [34]
Citations
Cites
Candida albicans binds human plasminogen: identification of eight plasminogen‐binding proteins
Crowe, J. D., Sievwright, I. K., Auld, G. C., Moore, N. R., Gow, N. A. R., & Booth, N. A. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03390.x · Cited by 246
Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors
Chhatwal, G. S. (2002) · Trends in Microbiology · doi:10.1016/s0966-842x(02)02351-x · Cited by 167
Self-citation
Research works printed but not linked: 74
- Alderete, 2001, Enzymes on microbial pathogens and Trichomonas vaginalis: molecular mimicry and functional diversity, Cell. Microbiol., 3, 359, 10.1046/j.1462-5822.2001.00126.x · DOI
- Allen, 1995, Case study: a new infection-triggered, autoimmune subtype of pediatric OCD and Tourette's syndrome, J. Am. Acad. Child Adolesc. Psychiatry, 34, 307, 10.1097/00004583-199503000-00015 · DOI
- Alloush, 1997, 3-Phosphoglycerate kinase: a glycolytic enzyme protein present in the cell wall of Candida albicans, Microbiology, 143, 321, 10.1099/00221287-143-2-321 · DOI
- Angiolella, 1996, Identification of a glucanassociated enolase as a main cell wall protein of Candida albicans and an indirect target of lipopeptide antimycotics, J. Infect. Dis., 173, 684, 10.1093/infdis/173.3.684 · DOI
- Baldo, 1988, Inhalant allergies to fungi: reactions to bakers' yeast (Saccharomyces cerevisiae) and identification of bakers' yeast enolase as an important allergen, Int. Arch. Allergy Appl. Immunol, 86, 201, 10.1159/000234572 · DOI
- Baseman, 1997, Mycoplasmas: sophisticated, reemerging, and burdened by their notoriety, Emerg. Infect. Dis., 3, 21, 10.3201/eid0301.970103 · DOI
- Berge, 1993, PAM, a novel plasminogen-binding protein from Streptococcus pyogenenes, J. Biol. Chem., 268, 25417, 10.1016/S0021-9258(19)74408-1 · DOI
- Bergmann, 2001, Alpha-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface, Mol. Microbiol., 40, 1273, 10.1046/j.1365-2958.2001.02448.x · DOI
- Bergmann, 2003, Identification of a novel plasmin(ogen)-binding motif in surface-displayed alpha-enolase of Streptococcus pneumoniae, Mol Microbiol., 49, 411, 10.1046/j.1365-2958.2003.03557.x · DOI
- Bermudez, 1996, Epidermal growth factor-binding protein in Mycobacterium avium and Mycobacterium tuberculosis: a possible role in the mechanism of infection, Infect. Immun., 64, 2917, 10.1128/iai.64.8.2917-2922.1996 · DOI
- Boyle, 1997, Plasminogen activation by invasive human pathogens, Thromb. Haemost., 77, 1, 10.1055/s-0038-1655727 · DOI
- Brewer, 1997, Current perspectives on the mechanism of catalysis by the enzyme enolase, Adv. Biophys. Chem., 6, 111
- Broeseker, 1988, Characterization of the interaction of human plasmin with its specific receptor on a group A streptococcus, Microb. Pathog., 5, 19, 10.1016/0882-4010(88)90077-0 · DOI
- Camara, 1994, A neuraminidase from Streptococcus pneumoniae has the features of a surface protein, Infect. Immun., 62, 3688, 10.1128/iai.62.9.3688-3695.1994 · DOI
- Cash, 1999, A proteomic analysis of erythromycin resistance in Streptococcus pneumoniae, Electrophoresis, 20, 2259, 10.1002/(SICI)1522-2683(19990801)20:11<2259::AID-ELPS2259>3.0.CO;2-F · DOI
- Clewell, 1995, Unconstrained bacterial promiscuity: the Tn916-Tn1545 family of conjugative transposons, Trends Microbiol., 3, 229, 10.1016/S0966-842X(00)88930-1 · DOI
- Dallo, 2002, Elongation factor Tu and E1 alpha subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae, Mol. Microbiol., 46, 1041, 10.1046/j.1365-2958.2002.03207.x · DOI
- Degado, 2001, The glyceraldehyde-3-phosphate dehydrogenase polypeptides encoded by the Saccharomyces cerevisiae TDH1, TDH2 and TDH3 genes are also cell wall proteins, Microbiology, 147, 411, 10.1099/00221287-147-2-411 · DOI
- D'Costa, 2000, Analysis of expression of a cytosolic enzyme on the surface of Streptococcus pyogenes, Biophys. Res Commun., 278, 826, 10.1006/bbrc.2000.3884 · DOI
- Engbring, 1998, Three genes encode distinct AP33 proteins involved in Trichomonas vaginalis cytoadherence, Mol. Microbiol., 28, 305, 10.1046/j.1365-2958.1998.00784.x · DOI
- Engbring, 1996, Trichomonas vaginalis adhesin proteins display molecular mimicry to metabolic enzymes, Adv. Exp. Med. Biol., 408, 207, 10.1007/978-1-4613-0415-9_25 · DOI
- Espinosa-Urgel, 1998, Escherichia coli expressed preferentially in an aquatic environment, Mol. Microbiol., 28, 325, 10.1046/j.1365-2958.1998.00796.x · DOI
- Facinelli, 2001, Association between erythromycin resistance and ability to enter human respiratory cells in group A streptococci, Lancet, 358, 30, 10.1016/S0140-6736(00)05253-3 · DOI
- Fernandes, 1992, A protein homologous to glyceraldehyde-3-phosphate dehydrogenase is induced in the cell wall of a flocculent Kluyveromyces marxianus, Biochim. Biophys. Acta, 1159, 67, 10.1016/0167-4838(92)90076-P · DOI
- Fletcher, 2001, Analysis of the effect of changing environmental conditions on the expression patterns of exported surface-associated proteins of the oral pathogen Actinobacillus actinomycetemcomitans, Microb. Pathog., 30, 359, 10.1006/mpat.2000.0439 · DOI
- Fontan, 2000, Antibodies to streptococcal surface enolase react with human alpha-enolase: Implications in poststreptococcal sequelae, J. Infect. Dis., 182, 1712, 10.1086/317604 · DOI
- Fox, 2001, Plasminogen-binding activity of enolase in the opportunistic pathogen Pneumocystis carinii, Med. Mycol., 39, 495, 10.1080/mmy.39.6.495.507 · DOI
- Gil-Navarro, 1997, The glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is a surface antigen, J. Bacteriol, 179, 4992, 10.1128/jb.179.16.4992-4999.1997 · DOI
- Goudot-Crozel, 1989, The major parasite surface antigen associated with human resistance to schistosomiasis is a 37-kD glyceraldehyde-3P-dehydrogenase, J. Exp. Med., 170, 2065, 10.1084/jem.170.6.2065 · DOI
- Gozalbo, 1998, The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein, Infect. Immun., 66, 2052, 10.1128/IAI.66.5.2052-2059.1998 · DOI
- Grifantini, 2002, Gene expression profile in Neisseria meningitidis and Neisseria lactamica upon host-cell contact: from basic research to vaccine development, Ann. N.Y. Acad. Sci., 975, 202, 10.1111/j.1749-6632.2002.tb05953.x · DOI
- Guzman, 1990, Role of neuraminidase-dependent adherence in Bacteroides fragilis attachment to human epithelial cells, FEMS Microbiol. Lett., 59, 187, 10.1111/j.1574-6968.1990.tb03820.x · DOI
- Hara, 2000, Cell surface-associated enolase in Actinobacillus actinomycetemcomitans, Microbiol. Immunol., 44, 349, 10.1111/j.1348-0421.2000.tb02505.x · DOI
- Ishiguro, 1992, Identification of Candida albicans antigens reactive with immunoglobulin E antibody of human sera, Infect. Immun., 60, 1550, 10.1128/iai.60.4.1550-1557.1992 · DOI
- Jolodar, 2003, Molecular cloning of an alpha-enolase from the human filarial parasite Onchocerca volvulus that binds human plasminogen, Biochim. Biophys. Acta, 1627, 111, 10.1016/S0167-4781(03)00083-6 · DOI · Paper page
- Jones, 2000, Reactivity of rheumatic fever and scarlet fever patients' sera with group A streptococcal M protein, cardiac myosin, and cardiac tropomyosin: a retrospective study, Infect. Immun., 68, 7132, 10.1128/IAI.68.12.7132-7136.2000 · DOI
- Kaufmann, 1992, Purification, characterization and inhibition by fluoride of enolase from Streptococcus mutans DSM 320523, Caries Res., 26, 110, 10.1159/000261494 · DOI
- Kenny, 1995, Protein secretion by enteropathogenic Escherichia coli is essential for transducting signals to epithelial cells, Proc. Natl. Acad. Sci. USA, 92, 7791, 10.1073/pnas.92.17.7991 · DOI
- Konings, 1983, Energy transduction and solute transport in streptococci, Antonie van Leeuwenhoek, 49, 247, 10.1007/BF00399501 · DOI
- Lee, 1995, Cloning of the gene for phosphoglycerate kinase from Schistosoma mansoni and characterization of its gene product, Mol. Biochem. Parasitol., 71, 221, 10.1016/0166-6851(95)91598-O · DOI
- Lee, 1995, Immune response to Schistosoma mansoni phosphoglycerate kinase during natural and experimental infection: Identification of a schistosome-specific B-cell epitope, Infect. Immun., 63, 4307, 10.1128/iai.63.11.4307-4311.1995 · DOI
- Lei, 2000, Identification and immunogenicity of group A Streptococcus culture supernatant proteins, Infect. Immun., 68, 6807, 10.1128/IAI.68.12.6807-6818.2000 · DOI
- Lottenberg, 1992, Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor, J. Bacteriol., 174, 5204, 10.1128/jb.174.16.5204-5210.1992 · DOI
- Lottenberg, 1994, Capturing host plasmin(ogen): a common mechanism for invasive pathogens?, Trends Microbiol., 2, 20, 10.1016/0966-842X(94)90340-9 · DOI
- Miles, 1991, Role of cell-surface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor, Biochemistry, 30, 1682, 10.1021/bi00220a034 · DOI · Paper page
- Modun, 2000, The staphylococcal transferrin receptor: a glycolytic enzyme with novel functions, Trends Microbiol., 8, 231, 10.1016/S0966-842X(00)01728-5 · DOI
- Modun, 1999, The staphylococcal transferrinbinding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase, Infect. Immun., 67, 1086, 10.1128/IAI.67.3.1086-1092.1999 · DOI · Paper page
- Morgan, 1979, Studies on the mechanism of iron release from transferrin, Biochim. Biophys. Acta, 580, 312, 10.1016/0005-2795(79)90144-2 · DOI
- Moss, 1988, ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins, Adv. Enzymol., 61, 303
- Nakajima, 1994, Plasminogen binds specifically to alpha-enolase on rat neuronal plasma membrane, J. Neurochem., 63, 2048, 10.1046/j.1471-4159.1994.63062048.x · DOI
- Nelson, 2001, pH-regulated secretion of a glyceraldehyde-3-phosphate dehydrogenase from Streptococcus gordonii FSS2: Purification, characterization, and cloning of the gene encoding this enzyme, J. Dent. Res., 80, 371, 10.1177/00220345010800011301 · DOI
- Pancholi, 2001, Multifunctional alpha-enolase: its role in diseases, Cell. Mol. Life Sci., 58, 902, 10.1007/PL00000910 · DOI
- Pancholi, 1992, A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate dehydrogenase with multiple binding activity, J. Exp. Med., 176, 415, 10.1084/jem.176.2.415 · DOI
- Pancholi, 1993, Glyceraldehyde-3-phosphate dehydrogenase on the surface of group A streptococci is also an ADP-ribosylating enzyme, Proc. Natl. Acad. Sci. USA, 90, 8154, 10.1073/pnas.90.17.8154 · DOI
- Pancholi, 1997, Regulation of the phosphorylation of human pharyngeal cell proteins by group A streptococcal surface dehydrogenase(SDH): Signal transduction between streptococci and pharyngeal cells, J. Exp. Med., 186, 1633, 10.1084/jem.186.10.1633 · DOI · Paper page
- Pancholi, 1998, Alpha-Enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci, J. Biol. Chem., 273, 14503, 10.1074/jbc.273.23.14503 · DOI
- Pancholi, 2003, Plasminogen-mediated group A streptococcal adherence to and pericellular invasion of human pharyngeal cells, Microb. Pathog, 35, 293, 10.1016/j.micpath.2003.08.004 · DOI
- Plow, 1995, The cell biology of the plasminogen system, FASEB. J., 9, 939, 10.1096/fasebj.9.10.7615163 · DOI
- Redlitz, 1995, The role of an enolase-related molecule in plasminogen binding to cells, Eur. J. Biochem., 227, 407, 10.1111/j.1432-1033.1995.tb20403.x · DOI
- Roberts, 1980, Phosphoenolpyruvate-dependent glucose phosphotransferase activity in Streptococcus mitis ATCC 903, Scand. J. Dent. Res., 88, 316
- Sha, 2003, Differential expression of the enolase gene under in vivo versus in vitro growth conditions of Aeromonas hydrophila, Microb. Pathog., 34, 195, 10.1016/S0882-4010(03)00028-7 · DOI
- Shoemaker, 1992, cDNA cloning and functional expression of the Schistosoma mansoni protective antigen triose-phosphate isomerase, Proc. Natl. Acad. Sci. USA, 89, 1842, 10.1073/pnas.89.5.1842 · DOI
- Sirover, 1999, New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase, Biochim. Biophys. Acta, 1432, 159, 10.1016/S0167-4838(99)00119-3 · DOI
- Smalheiser, 1996, Proteins in unexpected locations, Mol. Biol. Cell, 7, 1003, 10.1091/mbc.7.7.1003 · DOI
- Sundstrom, 1992, Molecular cloning of cDNA and analysis of protein secondary structure of Candida albicans enolase, an abundant, immunodominant glycolytic enzyme, J. Bacteriol., 174, 6789, 10.1128/jb.174.21.6789-6799.1992 · DOI
- Sutcliffe, 1996, Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin: a common resistance pattern mediated by an efflux system, Antimicrob. Agents Chemother, 40, 1817, 10.1128/AAC.40.8.1817 · DOI
- Swoboda, 1993, Glycolytic enzymes of Candida albicans are nonubiquitous immunogens during candidiasis, Infect. Immun., 61, 4263, 10.1128/iai.61.10.4263-4271.1993 · DOI
- Taylor, 2002, Transferrin binding in Staphylococcus aureus: involvement of a cell wallanchored protein, Mol. Microbiol., 43, 1603, 10.1046/j.1365-2958.2002.02850.x · DOI
- Vacca-Smith, 1994, Glucosyltransferase mediates adhesion of Streptococcus gordonii to human endothelial cells in vitro, Infect. Immun., 62, 2187, 10.1128/iai.62.6.2187-2194.1994 · DOI
- Wistow, 1987, Recruitment of enzymes as lens structural proteins, Science, 236, 1554, 10.1126/science.3589669 · DOI
- Wistow, 1988, Taucrystallin/alpha-enolase: one gene encodes both an enzyme and a lens structural protein, J. Cell Biol., 107, 2729, 10.1083/jcb.107.6.2729 · DOI
- Yamakami, 2000, The potential role for nephritis-associated plasmin receptor in acute poststreptococcal glomerulonephritis, Methods, 21, 185, 10.1006/meth.2000.0990 · DOI
- Yang, 1994, Entamoeba histolytica has an alcohol dehydrogenase homologous to the multifuctional adhE gene product of Escherichia coli, Mol. Biochem. Parasitol., 64, 253, 10.1016/0166-6851(93)00020-A · DOI
- Yeung, 1993, Complete nucleotide sequence of the Actinomyces viscosus T14V sialidase gene: presence of a conserved repeating sequence among strains of Actinomyces spp, Infect. Immun., 61, 109, 10.1128/iai.61.1.109-116.1993 · DOI
Cited by
Sorted by citations
Elongation factor Tu is a multifunctional and processed moonlighting protein
Widjaja, M., Harvey, K. L., Hagemann, L., Berry, I. J., Jarocki, V. M., Raymond, B. B. A., Tacchi, J. L., Gründel, A., Steele, J. R., Padula, M. P., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-10644-z · Cited by 131
Streptococcus pyogenes adhesion and colonization
Brouwer, S., Barnett, T. C., Rivera‐Hernandez, T., Rohde, M., & Walker, M. J. (2016) · FEBS Letters · doi:10.1002/1873-3468.12254 · Cited by 113
“The most important anchorless adhesins in GAS are housekeeping enzymes that not only perform important virulence roles on the surface but also carry out essential catalytic functions within the cytoplasm [172].”
BackgroundBoradia, V. M., Malhotra, H., Thakkar, J. S., Tillu, V. A., Vuppala, B., Patil, P., Sheokand, N., Sharma, P., Chauhan, A. S., Raje, M., et al. (2014) · Nature Communications · doi:10.1038/ncomms5730 · Cited by 108
Casaburi, G., & Frese, S. A. (2018) · Human Microbiome Journal · doi:10.1016/j.humic.2018.05.001 · Cited by 38
Ets, L., Ilves, H., Juhe, L., Ilmjärv, T., Puiggené, Ò., Nikel, P. I., & Kivisaar, M. (2026) · Journal of Bacteriology · doi:10.1128/jb.00479-25 · Cited by 1
Metadata
- Authors
- Pancholi, V., & Chhatwal, G. S.
- Venue
- International Journal of Medical Microbiology
- Publisher
- Elsevier BV
- Published
- 2003
- Volume
- 293
- Issue
- 6
- Pages
- 391-401
- ISSN
- 1438-4221
- Cited by
- 251
- References
- 2
- Language
- en
- Funders
- National Institutes of Health (AI-42827)
- American Heart Association (EI-9940228N)
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review