Proteomic comparison of historic and recently emerged hypervirulent clostridium difficile strains

Journal of Proteome Research

Volumn 12, Issue 3, 2013, Pages 1151-1161

  Chen, Jenn Wei ^a   Scaria, Joy ^a   Mao, Chunhong ^b   Sobral, Bruno ^b   Zhang, Sheng ^a   Lawley, Trevor ^c   Chang, Yung Fu ^a  

^a Department of Molecular Biology and Genetics   (United States)

^b VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Clostridium difficile; comparative proteomic analysis

Indexed keywords

CHAPERONIN 60; CSPF PROTEIN; CSPG PROTEIN; HEAT SHOCK PROTEIN; PHOSPHOTRANSFERASE; PURG PROTEIN; RECA PROTEIN; SERA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIOPHAGE; CARBON SOURCE; CATABOLITE REPRESSION; CLOSTRIDIUM DIFFICILE; CONTROLLED STUDY; LIQUID CHROMATOGRAPHY; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 84874605070     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3007528     Document Type: Article

References (67)

1. Gerding, D. N. Global epidemiology of Clostridium difficile infection in 2010 Infect. Control Hosp. Epidemiol. 2010, 31 (Suppl 1) S32-4
2. Leffler, D. A.; Lamont, J. T. Editorial: not so nosocomial anymore: the growing threat of community-acquired Clostridium difficile Am. J. Gastroenterol. 2012, 107 (1) 96-8
3. Rupnik, M.; Wilcox, M. H.; Gerding, D. N. Clostridium difficile infection: new developments in epidemiology and pathogenesis Nat. Rev. Microbiol. 2009, 7 (7) 526-36
4. Elixhauser, A.; Jhung, M. Clostridium difficile -Associated Disease in U.S. Hospitals, 1993-2005: Statistical Brief #50. In Healthcare Cost and Utilization Project (HCUP) Statistical Briefs; Agency for Health Care Policy and Research: Rockville, MD, 2008.
5. O'Brien, J. A.; Lahue, B. J.; Caro, J. J.; Davidson, D. M. The emerging infectious challenge of Clostridium difficile -associated disease in Massachusetts hospitals: clinical and economic consequences Infect. Control Hosp. Epidemiol. 2007, 28 (11) 1219-27
6. Stabler, R. A.; Gerding, D. N.; Songer, J. G.; Drudy, D.; Brazier, J. S.; Trinh, H. T.; Witney, A. A.; Hinds, J.; Wren, B. W. Comparative phylogenomics of Clostridium difficile reveals clade specificity and microevolution of hypervirulent strains J. Bacteriol. 2006, 188 (20) 7297-305
7. Janvilisri, T.; Scaria, J.; Thompson, A. D.; Nicholson, A.; Limbago, B. M.; Arroyo, L. G.; Songer, J. G.; Grohn, Y. T.; Chang, Y. F. Microarray identification of Clostridium difficile core components and divergent regions associated with host origin J. Bacteriol. 2009, 191 (12) 3881-91
8. McDonald, L. C.; Killgore, G. E.; Thompson, A.; Owens, R. C., Jr.; Kazakova, S. V.; Sambol, S. P.; Johnson, S.; Gerding, D. N. An epidemic, toxin gene-variant strain of Clostridium difficile N. Engl. J. Med. 2005, 353 (23) 2433-41
9. Gerding, D. N. Clostridium difficile infection prevention: biotherapeutics, immunologics, and vaccines Discovery Med. 2012, 13 (68) 75-83
10. Stabler, R. A.; He, M.; Dawson, L.; Martin, M.; Valiente, E.; Corton, C.; Lawley, T. D.; Sebaihia, M.; Quail, M. A.; Rose, G.; Gerding, D. N.; Gibert, M.; Popoff, M. R.; Parkhill, J.; Dougan, G.; Wren, B. W. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium Genome Biol. 2009, 10 (9) R102
11. He, M.; Sebaihia, M.; Lawley, T. D.; Stabler, R. A.; Dawson, L. F.; Martin, M. J.; Holt, K. E.; Seth-Smith, H. M.; Quail, M. A.; Rance, R.; Brooks, K.; Churcher, C.; Harris, D.; Bentley, S. D.; Burrows, C.; Clark, L.; Corton, C.; Murray, V.; Rose, G.; Thurston, S.; van Tonder, A.; Walker, D.; Wren, B. W.; Dougan, G.; Parkhill, J. Evolutionary dynamics of Clostridium difficile over short and long time scales Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (16) 7527-32
12. Forgetta, V.; Oughton, M. T.; Marquis, P.; Brukner, I.; Blanchette, R.; Haub, K.; Magrini, V.; Mardis, E. R.; Gerding, D. N.; Loo, V. G.; Miller, M. A.; Mulvey, M. R.; Rupnik, M.; Dascal, A.; Dewar, K. Fourteen-genome comparison identifies DNA markers for severe-disease-associated strains of Clostridium difficile J. Clin. Microbiol. 2011, 49 (6) 2230-8
13. Scaria, J.; Ponnala, L.; Janvilisri, T.; Yan, W.; Mueller, L. A.; Chang, Y. F. Analysis of ultra low genome conservation in Clostridium difficile PloS ONE 2010, 5 (12) e15147
14. Wright, A.; Wait, R.; Begum, S.; Crossett, B.; Nagy, J.; Brown, K.; Fairweather, N. Proteomic analysis of cell surface proteins from Clostridium difficile Proteomics 2005, 5 (9) 2443-52
15. Lawley, T. D.; Croucher, N. J.; Yu, L.; Clare, S.; Sebaihia, M.; Goulding, D.; Pickard, D. J.; Parkhill, J.; Choudhary, J.; Dougan, G. Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores J. Bacteriol. 2009, 191 (17) 5377-86
16. Jain, S.; Graham, C.; Graham, R. L.; McMullan, G.; Ternan, N. G. Quantitative proteomic analysis of the heat stress response in Clostridium difficile strain 630 J. Proteome Res. 2011, 10 (9) 3880-90
17. Emerson, J. E.; Stabler, R. A.; Wren, B. W.; Fairweather, N. F. Microarray analysis of the transcriptional responses of Clostridium difficile to environmental and antibiotic stress J. Med. Microbiol. 2008, 57 (Pt 6) 757-64
18. Ternan, N. G.; Jain, S.; Srivastava, M.; McMullan, G. Comparative transcriptional analysis of clinically relevant heat stress response in Clostridium difficile strain 630 PLoS ONE 2012, 7 (7) e42410
19. Sebaihia, M.; Wren, B. W.; Mullany, P.; Fairweather, N. F.; Minton, N.; Stabler, R.; Thomson, N. R.; Roberts, A. P.; Cerdeño-Tárraga, A. M.; Wang, H.; Holden, M. T. G.; Wright, A.; Churcher, C.; Quail, M. A.; Baker, S.; Bason, N.; Brooks, K.; Chillingworth, T.; Cronin, A.; Davis, P.; Dowd, L.; Fraser, A.; Feltwell, T.; Hance, Z.; Holroyd, S.; Jagels, K.; Moule, S.; Mungall, K.; Price, C.; Rabbinowitsch, E.; Sharp, S.; Simmonds, M.; Stevens, K.; Unwin, L.; Whithead, S.; Dupuy, B.; Dougan, G.; Barrell, B.; Parkhill, J. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome Nat. Genet. 2006, 38 (7) 779-86
20. Karasawa, T.; Ikoma, S.; Yamakawa, K.; Nakamura, S. A defined growth medium for Clostridium difficile Microbiology 1995, 141 (Pt 2) 371-5
21. Sorg, J. A.; Dineen, S. S. Laboratory maintenance of Clostridium difficile Curr. Protoc. Microbiol. 2009, 9, 9A.1.1-9A.1.10
22. Yaeger, M. J.; Kinyon, J. M.; Glenn Songer, J. A prospective, case control study evaluating the association between Clostridium difficile toxins in the colon of neonatal swine and gross and microscopic lesions J. Vet. Diagn. Invest. 2007, 19 (1) 52-9
23. Wang, Y.; Yang, F.; Gritsenko, M. A.; Wang, Y.; Clauss, T.; Liu, T.; Shen, Y.; Monroe, M. E.; Lopez-Ferrer, D.; Reno, T.; Moore, R. J.; Klemke, R. L.; Camp, D. G., 2nd; Smith, R. D. Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells Proteomics 2011, 11 (10) 2019-26
24. Gillespie, J. J.; Wattam, A. R.; Cammer, S. A.; Gabbard, J. L.; Shukla, M. P.; Dalay, O.; Driscoll, T.; Hix, D.; Mane, S. P.; Mao, C.; Nordberg, E. K.; Scott, M.; Schulman, J. R.; Snyder, E. E.; Sullivan, D. E.; Wang, C.; Warren, A.; Williams, K. P.; Xue, T.; Yoo, H. S.; Zhang, C.; Zhang, Y.; Will, R.; Kenyon, R. W.; Sobral, B. W. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species Infect. Immun. 2011, 79 (11) 4286-98
25. Li, L.; Stoeckert, C. J., Jr.; Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes Genome Res. 2003, 13 (9) 2178-89
26. Paley, S. M.; Karp, P. D. The Pathway Tools cellular overview diagram and Omics Viewer Nucleic Acids Res. 2006, 34 (13) 3771-8
27. Karp, P. D.; Paley, S.; Romero, P. The Pathway Tools software Bioinformatics 2002, 18 (Suppl 1) S225-32
28. Szklarczyk, D.; Franceschini, A.; Kuhn, M.; Simonovic, M.; Roth, A.; Minguez, P.; Doerks, T.; Stark, M.; Muller, J.; Bork, P.; Jensen, L. J.; von Mering, C. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Nucleic Acids Res. 2011, 39 (Database issue) D561-8
29. Smoot, M. E.; Ono, K.; Ruscheinski, J.; Wang, P. L.; Ideker, T. Cytoscape 2.8: new features for data integration and network visualization Bioinformatics 2011, 27 (3) 431-2
30. Mao, F.; Dam, P.; Chou, J.; Olman, V.; Xu, Y. DOOR: a database for prokaryotic operons Nucleic Acids Res. 2009, 37 (Database issue) D459-63
31. Karlsson, S.; Burman, L. G.; Akerlund, T. Induction of toxins in Clostridium difficile is associated with dramatic changes of its metabolism Microbiology 2008, 154 (Pt 11) 3430-6
32. Antunes, A.; Martin-Verstraete, I.; Dupuy, B. CcpA-mediated repression of Clostridium difficile toxin gene expression Mol. Microbiol. 2011, 79 (4) 882-99
33. Waligora, A. J.; Barc, M. C.; Bourlioux, P.; Collignon, A.; Karjalainen, T. Clostridium difficile cell attachment is modified by environmental factors Appl. Environ. Microbiol. 1999, 65 (9) 4234-8
34. Hennequin, C.; Porcheray, F.; Waligora-Dupriet, A.; Collignon, A.; Barc, M.; Bourlioux, P.; Karjalainen, T. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence Microbiology 2001, 147 (Pt 1) 87-96
35. Corfield, A. P.; Myerscough, N.; Longman, R.; Sylvester, P.; Arul, S.; Pignatelli, M. Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease Gut 2000, 47 (4) 589-94
36. Gaynor, E. C.; Cawthraw, S.; Manning, G.; MacKichan, J. K.; Falkow, S.; Newell, D. G. The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes J. Bacteriol. 2004, 186 (2) 503-17
37. Fine, D. H.; Furgang, D.; Schreiner, H. C.; Goncharoff, P.; Charlesworth, J.; Ghazwan, G.; Fitzgerald-Bocarsly, P.; Figurski, D. H. Phenotypic variation in Actinobacillus actinomycetemcomitans during laboratory growth: implications for virulence Microbiology 1999, 145 (Pt 6) 1335-47
38. Thompson, A.; Schafer, J.; Kuhn, K.; Kienle, S.; Schwarz, J.; Schmidt, G.; Neumann, T.; Johnstone, R.; Mohammed, A. K.; Hamon, C. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS Anal. Chem. 2003, 75 (8) 1895-904
39. Varga, J.; Stirewalt, V. L.; Melville, S. B. The CcpA protein is necessary for efficient sporulation and enterotoxin gene (cpe) regulation in Clostridium perfringens J. Bacteriol. 2004, 186 (16) 5221-9
40. Muthukrishnan, G.; Quinn, G. A.; Lamers, R. P.; Diaz, C.; Cole, A. L.; Chen, S.; Cole, A. M. Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage J. Proteome Res. 2011, 10 (4) 2064-78
41. Janvilisri, T.; Scaria, J.; Teng, C.-H.; McDonough, S. P.; Gleed, R. D.; Fubini, S. L.; Zhang, S.; Akey, B.; Chang, Y.-F. Temporal Differential Proteomes of Clostridium difficile in the Pig Ileal-Ligated Loop Model PLoS ONE 2012, 7 (9) e45608
42. Vohra, P.; Poxton, I. R. Comparison of toxin and spore production in clinically relevant strains of Clostridium difficile Microbiology 2011, 157 (Pt 5) 1343-53
43. Scaria, J.; Janvilisri, T.; Fubini, S.; Gleed, R. D.; McDonough, S. P.; Chang, Y. F. Clostridium difficile transcriptome analysis using pig ligated loop model reveals modulation of pathways not modulated in vitro J. Infect. Dis. 2011, 203 (11) 1613-20
44. Deutscher, J.; Francke, C.; Postma, P. W. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria Microbiol. Mol. Biol. Rev. 2006, 70 (4) 939-1031
45. Randle, C. L.; Albro, P. W.; Dittmer, J. C. The phosphoglyceride composition of Gram-negative bacteria and the changes in composition during growth Biochim. Biophys. Acta 1969, 187 (2) 214-20
46. Roof, D. M.; Roth, J. R. Ethanolamine utilization in Salmonella typhimurium J. Bacteriol. 1988, 170 (9) 3855-63
47. Garsin, D. A. Ethanolamine utilization in bacterial pathogens: roles and regulation Nat. Rev. Microbiol. 2010, 8 (4) 290-5
48. Janvilisri, T.; Scaria, J.; Chang, Y. F. Transcriptional profiling of Clostridium difficile and Caco-2 cells during infection J. Infect. Dis. 2010, 202 (2) 282-90
49. Merrigan, M.; Venugopal, A.; Mallozzi, M.; Roxas, B.; Viswanathan, V. K.; Johnson, S.; Gerding, D. N.; Vedantam, G. Human hypervirulent Clostridium difficile strains exhibit increased sporulation as well as robust toxin production J. Bacteriol. 2010, 192 (19) 4904-11
50. Antunes, A.; Camiade, E.; Monot, M.; Courtois, E.; Barbut, F.; Sernova, N. V.; Rodionov, D. A.; Martin-Verstraete, I.; Dupuy, B. Global transcriptional control by glucose and carbon regulator CcpA in Clostridium difficile Nucleic Acids Res. 2012, 40 (21) 10701-18
51. Wang, J. Y.; Syvanen, M. DNA twist as a transcriptional sensor for environmental changes Mol. Microbiol. 1992, 6 (14) 1861-6
52. Rocha, E. P.; Matic, I.; Taddei, F. Over-representation of repeats in stress response genes: a strategy to increase versatility under stressful conditions? Nucleic Acids Res. 2002, 30 (9) 1886-94
53. Karjalainen, T.; Waligora-Dupriet, A. J.; Cerquetti, M.; Spigaglia, P.; Maggioni, A.; Mauri, P.; Mastrantonio, P. Molecular and genomic analysis of genes encoding surface-anchored proteins from Clostridium difficile Infect. Immun. 2001, 69 (5) 3442-6
54. Cacalano, G.; Kays, M.; Saiman, L.; Prince, A. Production of the Pseudomonas aeruginosa neuraminidase is increased under hyperosmolar conditions and is regulated by genes involved in alginate expression J. Clin. Invest. 1992, 89 (6) 1866-74
55. Kunin, C. M.; Hua, T. H.; Guerrant, R. L.; Bakaletz, L. O. Effect of salicylate, bismuth, osmolytes, and tetracycline resistance on expression of fimbriae by Escherichia coli Infect. Immun. 1994, 62 (6) 2178-86
56. Tartera, C.; Metcalf, E. S. Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells Infect. Immun. 1993, 61 (7) 3084-9
57. Rapala-Kozik, M.; Wolak, N.; Kujda, M.; Banas, A. K. The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response BMC Plant Biol. 2012, 12, 2
58. Ueda, A.; Kathiresan, A.; Inada, M.; Narita, Y.; Nakamura, T.; Shi, W.; Takabe, T.; Bennett, J. Osmotic stress in barley regulates expression of a different set of genes than salt stress does J. Exp. Bot. 2004, 55 (406) 2213-8
59. Fuentes, D. E.; Fuentes, E. L.; Castro, M. E.; Perez, J. M.; Araya, M. A.; Chasteen, T. G.; Pichuantes, S. E.; Vasquez, C. C. Cysteine metabolism-related genes and bacterial resistance to potassium tellurite J. Bacteriol. 2007, 189 (24) 8953-60
60. Cartman, S. T.; Heap, J. T.; Kuehne, S. A.; Cockayne, A.; Minton, N. P. The emergence of 'hypervirulence' in Clostridium difficile Int. J. Med. Microbiol. 2010, 300 (6) 387-95
61. Warny, M.; Pepin, J.; Fang, A.; Killgore, G.; Thompson, A.; Brazier, J.; Frost, E.; McDonald, L. C. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe Lancet 2005, 366 (9491) 1079-84
62. Dupuy, B.; Govind, R.; Antunes, A.; Matamouros, S. Clostridium difficile toxin synthesis is negatively regulated by TcdC J. Med. Microbiol. 2008, 57 (Pt 6) 685-9
63. Kuijper, E. J.; Coignard, B.; Tull, P. Emergence of Clostridium difficile -associated disease in North America and Europe Clin. Microbiol. Infec. 2006, 12 (Suppl 6) 2-18
64. McDonald, L. C.; Coignard, B.; Dubberke, E.; Song, X.; Horan, T.; Kutty, P. K. Recommendations for surveillance of Clostridium difficile -associated disease Infect. Control Hosp. Epidemiol. 2007, 28 (2) 140-5
65. Burns, D. A.; Heap, J. T.; Minton, N. P. The diverse sporulation characteristics of Clostridium difficile clinical isolates are not associated with type Anaerobe 2010, 16 (6) 618-22
66. Heeg, D.; Burns, D. A.; Cartman, S. T.; Minton, N. P. Spores of Clostridium difficile clinical isolates display a diverse germination response to bile salts PloS ONE 2012, 7 (2) e32381
67. Deneve, C.; Janoir, C.; Poilane, I.; Fantinato, C.; Collignon, A. New trends in Clostridium difficile virulence and pathogenesis Int. J. Antimicrob. Agents 2009, 33 (Suppl 1) S24-8