Clostridium difficile infection in diabetes

Diabetes Research and Clinical Practice

Volumn 105, Issue 3, 2014, Pages 285-294

  Qu, Hui Qi ^a   Jiang, Zhi Dong ^a  

^a UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Clostridium difficile; Diabetes; Gut microbiota; Host immunity

Indexed keywords

CLOSTRIDIUM DIFFICILE TOXIN A; CLOSTRIDIUM DIFFICILE TOXIN B; VIRULENCE FACTOR;

BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CARRIER; BACTERIUM DETECTION; BACTERIUM ISOLATE; CDTA GENE; CDTB GENE; CLOSTRIDIUM DIFFICILE INFECTION; DIABETES MELLITUS; DISEASE ASSOCIATION; ENZYME IMMUNOASSAY; GENE EXPRESSION; HOSPITAL INFECTION; HUMAN; INFECTION RISK; MOLECULAR PATHOLOGY; MOLECULAR TYPING; MULTILOCUS SEQUENCE TYPING; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PALOC GENE; PEPTOCLOSTRIDIUM DIFFICILE; POLYMERASE CHAIN REACTION; RECURRENT INFECTION; REVIEW; RISK FACTOR; TCDA GENE; TCDB GENE; TCDC GENE; TCDE GENE; TCDR GENE; ADULT; CLASSIFICATION; FECES; INFANT; MICROBIOLOGY; PATHOGENICITY; PROCEDURES; PSEUDOMEMBRANOUS COLITIS;

ADULT; CLOSTRIDIUM DIFFICILE; DIABETES COMPLICATIONS; ENTEROCOLITIS, PSEUDOMEMBRANOUS; FECES; HUMANS; INFANT; POLYMERASE CHAIN REACTION; VIRULENCE FACTORS;

EID: 84921626110     PISSN: 01688227     EISSN: 18728227     Source Type: Journal    
DOI: 10.1016/j.diabres.2014.06.002     Document Type: Review

References (134)

1. Archibald L.K., Banerjee S.N., Jarvis W.R. Secular trends in hospital-acquired Clostridium difficile disease in the United States 1987-2001. J Infect Dis 2004, 189:1585-1589.
2. Britton R.A., Young V.B. Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol 2012, 20:313-319.
3. Bartlett J.G. Clostridium difficile: clinical considerations. Rev Infect Dis 1990, 12(Suppl 2):S243-S251.
4. Rupnik M., Wilcox M.H., Gerding D.N. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 2009, 7:526-536.
5. McFarland L.V., Mulligan M.E., Kwok R.Y., Stamm W.E. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989, 320:204-210.
6. Dial S., Delaney J.A., Barkun A.N., Suissa S. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA 2005, 294:2989-2995.
7. Kelly C.P., LaMont J.T. Clostridium difficile infection. Annu Rev Med 1998, 49:375-390.
8. 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-S28.
9. Cohen Stuart H., Gerding Dale N., Stuart Johnson, Kelly Ciaran P., Loo Vivian G., McDonald L.C., Pepin J., Wilcox Mark H. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA). Infect Control Hosp Epidemiol 2010, 31:431-455.
10. Reller M.E., Lema C.A., Perl T.M., Cai M., Ross T.L., Speck K.A., Carroll K.C. Yield of stool culture with isolate toxin testing versus a two-step algorithm including stool toxin testing for detection of toxigenic Clostridium difficile. J Clin Microbiol 2007, 45:3601-3605.
11. Crobach M.J.T., Dekkers O.M., Wilcox M.H., Kuijper E.J. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): data review and recommendations for diagnosing Clostridium difficile-infection (CDI). Clin Microbiol Infect 2009, 15:1053-1066.
12. Srivastava A., Talaue M., Liu S., Degen D., Ebright R.Y., Sineva E., Chakraborty A., Druzhinin S.Y., Chatterjee S., Mukhopadhyay J., Ebright Y.W., Zozula A., Shen J., Sengupta S., Niedfeldt R.R., Xin C., Kaneko T., Irschik H., Jansen R., Donadio S., Connell N., Ebright R.H. New target for inhibition of bacterial RNA polymerase: 'switch region'. Curr Opin Microbiol 2011, 14:532-543.
13. Shue Y.K., Sears P.S., Shangle S., Walsh R.B., Lee C., Gorbach S.L., Okumu F., Preston R.A. Safety, tolerance, and pharmacokinetic studies of OPT-80 in healthy volunteers following single and multiple oral doses. Antimicrob Agents Chemother 2008, 52:1391-1395.
14. Drekonja D.M., Butler M., MacDonald R., Bliss D., Filice G.A., Rector T.S., Wilt T.J. Comparative effectiveness of Clostridium difficile treatments: a systematic review. Ann Intern Med 2011, 155:839-847.
15. Gough E., Shaikh H., Manges A.R. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis 2011, 53:994-1002.
16. Surawicz C.M., Alexander J. Treatment of refractory and recurrent Clostridium difficile infection. Nat Rev Gastroenterol Hepatol 2011, 8:330-339.
17. Borody T.J., Khoruts A. Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 2012, 9:88-96.
18. van Nood E., Vrieze A., Nieuwdorp M., Fuentes S., Zoetendal E.G., de Vos W.M., Visser C.E., Kuijper E.J., Bartelsman J.F.W.M., Tijssen J.G.P., Speelman P., Dijkgraaf M.G.W., Keller J.J. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013, 368:407-415.
19. Lowy I., Molrine D.C., Leav B.A., Blair B.M., Baxter R., Gerding D.N., Nichol G., Thomas W.D., Leney M., Sloan S., Hay C.A., Ambrosino D.M. Treatment with monoclonal antibodies against Clostridium difficile toxins. N Engl J Med 2010, 362:197-205.
20. Kim K.H., Fekety R., Batts D.H., Brown D., Cudmore M., Silva J., Waters D. Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated colitis. J Infect Dis 1981, 143:42-50.
21. 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, 191:5377-5386.
22. Cookson B. Hypervirulent strains of Clostridium difficile. Postgrad Med J 2007, 83:291-295.
23. Dubberke Erik R., Wertheimer Albert I. Review of current literature on the economic burden of Clostridium difficile infection. Infect Control Hosp Epidemiol 2009, 30:57-66.
24. Aubert R.E., Geiss L.S., Ballard D.J., Cocanougher B., Herman W.H. Diabetes-related hospitalization and hospital utilization. Diabetes Am 1995, 2:553-569.
25. Boyle J.P., Thompson T.J., Gregg E.W., Barker L.E., Williamson D.F. Projection of the year 2050 burden of diabetes in the US adult population: dynamic modeling of incidence, mortality, and prediabetes prevalence. Popul Health Metrics 2010, 8:29.
26. Geerlings S.E., Hoepelman A.I. Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunol Med Microbiol 1999, 26:259-265.
27. Molina M.F., Qu H.Q., Rentfro A.R., Nair S., Lu Y., Hanis C.L., McCormick J.B., Fisher-Hoch S.P. Decreased expression of ATP6V1H in type 2 diabetes: a pilot report on the diabetes risk study in Mexican Americans. Biochem Biophys Res Commun 2011, 412:728-731.
28. Qu H.Q., Rentfro A.R., Lu Y., Nair S., Hanis C.L., McCormick J.B., Fisher-Hoch S.P. Host susceptibility to tuberculosis: insights from a longitudinal study of gene expression in diabetes. Int J Tuberc Lung Dis 2012, 16:370-372.
29. Shakov R., Salazar R.S., Kagunye S.K., Baddoura W.J., DeBari V.A. Diabetes mellitus as a risk factor for recurrence of Clostridium difficile infection in the acute care hospital setting. Am J Infect Control 2011, 39:194-198.
30. Dial S., Alrasadi K., Manoukian C., Huang A., Menzies D. Risk of Clostridium difficile diarrhea among hospital inpatients prescribed proton pump inhibitors: cohort and case-control studies. Can Med Assoc J 2004, 171:33-38.
31. Jung K.S., Park J.J., Chon Y.E., Jung E.S., Lee H.J., Jang H.W., Lee K.J., Lee S.H., Moon C.M., Lee J.H., Shin J.K., Jeon S.M., Hong S.P., Kim T.I., Kim W.H., Cheon J.H. Risk factors for treatment failure and recurrence after metronidazole treatment for Clostridium difficile-associated diarrhea. Gut Liver 2010, 4:332-337.
32. Rodrigues M.A., Brady R.R., Rodrigues J., Graham C., Gibb A.P. Clostridium difficile infection in general surgery patients; identification of high-risk populations. Int J Surg 2010, 8:368-372.
33. Hall I.C., O'Toole E. Intestinal flora in new-born infants: with a description of a new pathogenic anaerobe, bacillus difficilis. Am J Dis Child 1935, 49:390-402.
34. Tedesco F.J., Barton R.W., Alpers D.H. Clindamycin-associated colitis. A prospective study. Ann Intern Med 1974, 81:429-433.
35. Bartlett J.G. Historical perspectives on studies of Clostridium difficile and C. difficile infection. Clin Infect Dis 2008, 46:S4-S11.
36. Bartlett J.G., Onderdonk A.B., Cisneros R.L., Kasper D.L. Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters. J Infect Dis 1977, 136:701-705.
37. Bartlett J.G., Chang T.W., Gurwith M., Gorbach S.L., Onderdonk A.B. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 1978, 298:531-534.
38. Al Saif N., BRAZIER J.S. The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 1996, 45:133-137.
39. Kato H., Kita H., Karasawa T., Maegawa T., Koino Y., Takakuwa H., Saikai T., Kobayashi K., Yamagishi T., Nakamura S. Colonisation and transmission of Clostridium difficile in healthy individuals examined by PCR ribotyping and pulsed-field gel electrophoresis. J Med Microbiol 2001, 50:720-727.
40. Rousseau C., Poilane I., De Pontual L., Maherault A.-C., Le Monnier A., Collignon A. Clostridium difficile carriage in healthy infants in the community: a potential reservoir for pathogenic strains. Clin Infect Dis 2012, 55:1209-1215.
41. Sebaihia M., Wren B.W., Mullany P., Fairweather N.F., Minton N., Stabler R., Thomson N.R., Roberts A.P., Cerdeno-Tarraga 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, 38:779-786.
42. 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, 188:7297-7305.
43. Killgore G., Thompson A., Johnson S., Brazier J., Kuijper E., Pepin J., Frost E.H., Savelkoul P., Nicholson B., Van Den Berg R.J., Kato H., Sambol S.P., Zukowski W., Woods C., Limbago B., Gerding D.N., McDonald L.C. Comparison of seven techniques for typing international epidemic strains of Clostridium difficile: restriction endonuclease analysis, pulsed-field gel electrophoresis, PCR-ribotyping, multilocus sequence typing, multilocus variable-number tandem-repeat analysis, amplified fragment length polymorphism, and surface layer protein A gene sequence typing. J Clin Microbiol 2008, 46:431-437.
44. Janezic S., Rupnik M. Molecular typing methods for Clostridium difficile: pulsed-field gel electrophoresis and PCR ribotyping. Methods Mol Biol 2010, 646:55-65.
45. Clabots C.R., Johnson S., Bettin K.M., Mathie P.A., Mulligan M.E., Schaberg D.R., Peterson L.R., Gerding D.N. Development of a rapid and efficient restriction endonuclease analysis typing system for Clostridium difficile and correlation with other typing systems. J Clin Microbiol 1993, 31:1870-1875.
46. Bidet P., Lalande V., Salauze B., Burghoffer B., Avesani V., Delmee M., Rossier A., Barbut F., Petit J.C. Comparison of PCR-ribotyping, arbitrarily primed PCR, and pulsed-field gel electrophoresis for typing Clostridium difficile. J Clin Microbiol 2000, 38:2484-2487.
47. Schwartz D.C., Cantor C.R. Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 1984, 37:67-75.
48. Gal M., Northey G., Brazier J.S. A modified pulsed-field gel electrophoresis (PFGE) protocol for subtyping previously non-PFGE typeable isolates of Clostridium difficile polymerase chain reaction ribotype 001. J Hosp Infect 2005, 61:231-236.
49. Bouchet V., Huot H., Goldstein R. Molecular genetic basis of ribotyping. Clin Microbiol Rev 2008, 21:262-273.
50. Grimont F., Grimont P.A.D. Ribosomal ribonucleic acid gene restriction patterns as potential taxonomic tools. Ann Inst Pasteur/Microbiol 1986, 137:165-175.
51. Kostman J.R., Alden M.B., Mair M., Edlind T.D., LiPuma J.J., Stull T.L. A universal approach to bacterial molecular epidemiology by polymerase chain reaction ribotyping. J Infect Dis 1995, 171:204-208.
52. Stubbs S.L.J., Brazier J.S., O'Neill G.L., Duerden B.I. PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J Clin Microbiol 1999, 37:461-463.
53. Bidet P., Barbut F., Lalande V., Burghoffer B., Petit J.C. Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett 1999, 175:261-266.
54. Didelot X., Eyre D., Cule M., Ip C., Ansari A., Griffiths D., Vaughan A., O'Connor L., Golubchik T., Batty E., Piazza P., Wilson D., Bowden R., Donnelly P., Dingle K., Wilcox M., Walker S., Crook D., Peto T., Harding R. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol 2012, 13:R118.
55. Rupnik M., Dupuy B., Fairweather N.F., Gerding D.N., Johnson S., Just I., Lyerly D.M., Popoff M.R., Rood J.I., Sonenshein A.L., Thelestam M., Wren B.W., Wilkins T.D., von Eichel-Streiber C. Revised nomenclature of Clostridium difficile toxins and associated genes. J Med Microbiol 2005, 54:113-117.
56. Voth D.E., Ballard J.D. Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev 2005, 18:247-263.
57. 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 Nat Acad Sci USA 2010, 107:7527-7532.
58. von Eichel-Streiber C., Laufenberg-Feldmann R., Sartingen S., Schulze J., Sauerborn M. Comparative sequence analysis of the Clostridium difficile toxins A and B. Mol Gen Genet 1992, 233:260-268.
59. von Eichel-Streiber C., Boquet P., Sauerborn M., Thelestam M. Large clostridial cytotoxins-a family of glycosyltransferases modifying small GTP-binding proteins. Trends Microbiol 1996, 4:375-382.
60. Just I., Gerhard R. Large clostridial cytotoxins. Rev Physiol Biochem Pharmacol 2004, 152:23-47.
61. Jank T., Aktories K. Structure and mode of action of clostridial glucosylating toxins: the ABCD model. Trends Microbiol 2008, 16:222-229.
62. Albesa-Jové D., Bertrand T., Carpenter E.P., Swain G.V., Lim J., Zhang J., Haire L.F., Vasisht N., Braun V., Lange A., von Eichel-Streiber C., Svergun D.I., Fairweather N.F., Brown K.A. Four distinct structural domains in Clostridium difficile toxin B visualized using SAXS. J Mol Biol 2010, 396:1260-1270.
63. Frisch C., Gerhard R., Aktories K., Hofmann F., Just I. The complete receptor-binding domain of Clostridium difficile toxin A is required for endocytosis. Biochem Biophys Res Commun 2003, 300:706-711.
64. Pruitt R.N., Chambers M.G., Ng K.K.-S., Ohi M.D., Lacy D.B. Structural organization of the functional domains of Clostridium difficile toxins A and B. Proc Nat Acad Sci 2010, 107:13467-13472.
65. Qa'Dan M., Spyres L.M., Ballard J.D. pH-Induced Conformational Changes in Clostridium difficile toxin B. Infect Immun 2000, 68:2470-2474.
66. Egerer M., Giesemann T., Jank T., Satchell K.J.F., Aktories K. Auto-catalytic cleavage of Clostridium difficile toxins A and B depends on cysteine protease activity. J Biol Chem 2007, 282:25314-25321.
67. Just I., Selzer J., Wilm M., Eichel-Streiber Cv, Mann M., Aktories K. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 1995, 375:500-503.
68. Chaves-Olarte E., Weidmann M., Eichel-Streiber C., Thelestam M. Toxins A and B from Clostridium difficile differ with respect to enzymatic potencies, cellular substrate specificities, and surface binding to cultured cells. J Clin Invest 1997, 100:1734-1741.
69. Pruitt R.N., Chumbler N.M., Rutherford S.A., Farrow M.A., Friedman D.B., Spiller B., Lacy D.B. Structural determinants of Clostridium difficile toxin A glucosyltransferase activity. J Biol Chem 2012, 287:8013-8020.
70. Raaijmakers J.H., Bos J.L. Specificity in Ras and Rap signaling. J Biol Chem 2009, 284:10995-10999.
71. Lyerly D.M., Saum K.E., MacDonald D.K., Wilkins T.D. Effects of Clostridium difficile toxins given intragastrically to animals. Infect Immun 1985, 47:349-352.
72. al-Barrak A., Embil J., Dyck B., Olekson K., Nicoll D., Alfa M., Kabani A. An outbreak of toxin A negative, toxin B positive Clostridium difficile-associated diarrhea in a Canadian tertiary-care hospital. Can Commun Dis Rep 1999, 25:65-69.
73. Alfa M.J., Kabani A., Lyerly D., Moncrief S., Neville L.M., Al-Barrak A., Harding G.K., Dyck B., Olekson K., Embil J.M. Characterization of a toxin A-negative, toxin B-positive strain of Clostridium difficile responsible for a nosocomial outbreak of Clostridium difficile-associated diarrhea. J Clin Microbiol 2000, 38:2706-2714.
74. Lyras D., O'Connor J.R., Howarth P.M., Sambol S.P., Carter G.P., Phumoonna T., Poon R., Adams V., Vedantam G., Johnson S., Gerding D.N., Rood J.I. Toxin B is essential for virulence of Clostridium difficile. Nature 2009, 458:1176-1179.
75. Kuehne S.A., Cartman S.T., Heap J.T., Kelly M.L., Cockayne A., Minton N.P. The role of toxin A and toxin B in Clostridium difficile infection. Nature 2010, 467:711-713.
76. Karen C.C., John G.B. Biology of Clostridium difficile: implications for epidemiology and diagnosis. Annu Rev Microbiol 2011, 65:501-521.
77. Mani N., Dupuy B. Regulation of toxin synthesis in Clostridium difficile by an alternative RNA polymerase sigma factor. Proc Nat Acad Sci 2001, 98:5844-5849.
78. Mani N., Lyras D., Barroso L., Howarth P., Wilkins T., Rood J.I., Sonenshein A.L., Dupuy B. Environmental response and autoregulation of Clostridium difficile TxeR, a sigma factor for toxin gene expression. J Bacteriol 2002, 184:5971-5978.
79. Govind R., Dupuy B. Secretion of Clostridium difficile toxins A and B requires the holin-like protein TcdE. PLoS Pathog 2012, 8:e1002727.
80. Tan K.S., Wee B.Y., Song K.P. Evidence for holin function of tcdE gene in the pathogenicity of Clostridium difficile. J Med Microbiol 2001, 50:613-619.
81. Matamouros S., England P., Dupuy B. Clostridium difficile toxin expression is inhibited by the novel regulator TcdC. Mol Microbiol 2007, 64:1274-1288.
82. Carter G.P., Douce G.R., Govind R., Howarth P.M., Mackin K.E., Spencer J., Buckley A.M., Antunes A., Kotsanas D., Jenkin G.A., Dupuy B., Rood J.I., Lyras D. The anti-sigma factor TcdC modulates hypervirulence in an epidemic BI/NAP1/027 clinical isolate of Clostridium difficile. PLoS Pathog 2011, 7:e1002317.
83. 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, 366:1079-1084.
84. Murray R., Boyd D., Levett P.N., Mulvey M.R., Alfa M.J. Truncation in the tcdC region of the Clostridium difficile PathLoc of clinical isolates does not predict increased biological activity of Toxin B or Toxin A. BMC Infect Dis 2009, 9:103.
85. Cartman S.T., Kelly M.L., Heeg D., Heap J.T., Minton N.P. Precise manipulation of the Clostridium difficile chromosome reveals a lack of association between the tcdC genotype and toxin production. Appl Environ Microbiol 2012, 78:4683-4690.
86. Olling A., Seehase S., Minton N.P., Tatge H., Schröter S., Kohlscheen S., Pich A., Just I., Gerhard R. Release of TcdA and TcdB from Clostridium difficile cdi 630 is not affected by functional inactivation of the tcdE gene. Microb Pathog 2012, 52:92-100.
87. Popoff M.R., Rubin E.J., Gill D.M., Boquet P. Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infect Immun 1988, 56:2299-2306.
88. Sundriyal A., Roberts A.K., Ling R., McGlashan J., Shone C.C., Acharya K.R. Expression, purification and cell cytotoxicity of actin-modifying binary toxin from Clostridium difficile. Protein Expression Purif 2010, 74:42-48.
89. Carter G.P., Lyras D., Allen D.L., Mackin K.E., Howarth P.M., O'Connor J.R., Rood J.I. Binary toxin production in Clostridium difficile is regulated by CdtR, a LytTR family response regulator. J Bacteriol 2007, 189:7290-7301.
90. Considine R.V., Simpson L.L. Cellular and molecular actions of binary toxins possessing ADP-ribosyltransferase activity. Toxicon 1991, 29:913-936.
91. Perelle S., Gibert M., Bourlioux P., Corthier G., Popoff M.R. Production of a complete binary toxin (actin-specific ADP-ribosyltransferase) by Clostridium difficile CD196. Infect Immun 1997, 65:1402-1407.
92. Schwan C., Stecher B., Tzivelekidis T., van Ham M., Rohde M., Hardt W.D., Wehland J., Aktories K. Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria. PLoS Pathog 2009, 5:e1000626.
93. Poilane I., Fantinato C., Cruaud P., Collignon A. [Epidemiological study of Clostridium difficile strains isolated in Jean-Verdier-Rene-Muret hospitals from 2001 to 2007]. Pathol Biol (Paris) 2008, 56:412-416.
94. Goncalves C., Decre D., Barbut F., Burghoffer B., Petit J.C. Prevalence and characterization of a binary toxin (actin-specific ADP-ribosyltransferase) from Clostridium difficile. J Clin Microbiol 2004, 42:1933-1939.
95. Geric B., Johnson S., Gerding D.N., Grabnar M., Rupnik M. Frequency of binary toxin genes among Clostridium difficile strains that do not produce large clostridial toxins. J Clin Microbiol 2003, 41:5227-5232.
96. Geric B., Carman R.J., Rupnik M., Genheimer C.W., Sambol S.P., Lyerly D.M., Gerding D.N., Johnson S. Binary toxin-producing, large clostridial toxin-negative Clostridium difficile strains are enterotoxic but do not cause disease in hamsters. J Infect Dis 2006, 193:1143-1150.
97. Barbut F., Decré D., Lalande V., Burghoffer B., Noussair L., Gigandon A., Espinasse F., Raskine L., Robert J., Mangeol A., Branger C., Petit J.-C. Clinical features of Clostridium difficile-associated diarrhoea due to binary toxin (actin-specific ADP-ribosyltransferase)-producing strains. J Med Microbiol 2005, 54:181-185.
98. Elliott B., Reed R., Chang B.J., Riley T.V. Bacteremia with a large clostridial toxin-negative, binary toxin-positive strain of Clostridium difficile. Anaerobe 2009, 15:249-251.
99. Fry P.R., Thakur S., Abley M., Gebreyes W.A. Antimicrobial resistance, toxinotype, and genotypic profiling of Clostridium difficile isolates of swine origin. J Clin Microbiol 2012, 50:2366-2372.
100. Calabi E., Calabi F., Phillips A.D., Fairweather N.F. Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. Infect Immun 2002, 70:5770-5778.
101. Janoir C., Péchiné S., Grosdidier C., Collignon A. Cwp84, a surface-associated protein of Clostridium difficile is a cysteine protease with degrading activity on extracellular matrix proteins. J Bacteriol 2007, 189:7174-7180.
102. Barbut F., Kajzer C., Planas N., Petit J.C. Comparison of three enzyme immunoassays, a cytotoxicity assay, and toxigenic culture for diagnosis of Clostridium difficile-associated diarrhea,. J Clin Microbiol 1993, 31:963-967.
103. Rupnik M., Avesani V., Janc M., von Eichel-Streiber C., Delmée M. A novel toxinotyping scheme and correlation of toxinotypes with serogroups of Clostridium difficile isolates. J Clin Microbiol 1998, 36:2240-2247.
104. Rupnik M. Clostridium difficile toxinotyping. Methods Mol Biol 2010, 646:67-76.
105. Stubbs S., Rupnik M., Gibert M., Brazier J., Duerden B., Popoff M. Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. FEMS Microbiol Lett 2000, 186:307-312.
106. Persson S., Torpdahl M., Olsen K.E. New multiplex PCR method for the detection of Clostridium difficile toxin A (tcdA) and toxin B (tcdB) and the binary toxin (cdtA/cdtB) genes applied to a Danish strain collection. Clin Microbiol Infect 2008, 14:1057-1064.
107. 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, 191:3881-3891.
108. 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, 40:10701-10718.
109. 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:e42410.
110. Paredes-Sabja D., Cofre-Araneda G., Brito-Silva C., Pizarro-Guajardo M., Sarker M.R. Clostridium difficile @@spore-macrophage interactions: spore survival. PLoS One 2012, 7:e43635.
111. Paredes-Sabja D., Sarker M.R. Interactions between Clostridium perfringens spores and Raw 264.7 macrophages. Anaerobe 2012, 18:148-156.
112. Stevens T.H., Forgac M. Structure, function and regulation of the vacuolar (H+)-ATPase. Annu Rev Cell Dev Biol 1997, 13:779-808.
113. Geyer M., Fackler O.T., Peterlin B.M. Subunit H of the V-ATPase involved in endocytosis shows homology to beta-adaptins. Mol Biol Cell 2002, 13:2045-2056.
114. Lee B.Y., Jethwaney D., Schilling B., Clemens D.L., Gibson B.W., Horwitz M.A. The Mycobacterium bovis bacille Calmette-Guerin phagosome proteome. Mol Cell Proteomics (United States) 2010, 9:32-53.
115. Ip W.K., Sokolovska A., Charriere G.M., Boyer L., Dejardin S., Cappillino M.P., Yantosca L.M., Takahashi K., Moore K.J., Lacy-Hulbert A., Stuart L.M. Phagocytosis and phagosome acidification are required for pathogen processing and MyD88-dependent responses to Staphylococcus aureus. J Immunol (United States) 2010, 184:7071-7081.
116. Berry M.P., Graham C.M., McNab F.W., Xu Z., Bloch S.A., Oni T., Wilkinson K.A., Banchereau R., Skinner J., Wilkinson R.J. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010, 466:973-977.
117. Wolf A., Agnihotri S., Micallef J., Mukherjee J., Sabha N., Cairns R., Hawkins C., Guha A. Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme. J Exp Med 2011, 208:313-326.
118. Rist R., Naftalin R.J. Dexamethasone inhibits the hexose monophosphate shunt in activated rat peritoneal macrophages by reducing hexokinase-dependent sugar uptake. Biochem J 1991, 278:129-135.
119. von Bernuth H., Picard C., Jin Z., Pankla R., Xiao H., Ku C.-L., Chrabieh M., Mustapha I.B., Ghandil P., Camcioglu Y. Pyogenic bacterial infections in humans with MyD88 deficiency. Science 2008, 321:691-696.
120. Warner N., Núñez G. MyD88: a critical adaptor protein in innate immunity signal transduction. J Immunol 2013, 190:3-4.
121. Lawley T.D., Clare S., Walker A.W., Goulding D., Stabler R.A., Croucher N., Mastroeni P., Scott P., Raisen C., Mottram L. Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun 2009, 77:3661-3669.
122. Hosoi T., Yokoyama S., Matsuo S., Akira S., Ozawa K. Myeloid differentiation factor 88 (MyD88)-deficiency increases risk of diabetes in mice. PLoS One 2010, 5:e12537.
123. Ryan A., Lynch M., Smith S.M., Amu S., Nel H.J., McCoy C.E., Dowling J.K., Draper E., O'Reilly V., McCarthy C. A role for TLR4 in Clostridium difficile infection and the recognition of surface layer proteins. PLoS Pathog 2011, 7:e1002076.
124. Dasu M.R., Devaraj S., Park S., Jialal I. Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care 2010, 33:861-868.
125. Merrigan M.M., Sambol S.P., Johnson S., Gerding D.N. Prevention of fatal Clostridium difficile-associated disease during continuous administration of clindamycin in hamsters. J Infect Dis 2003, 188:1922-1927.
126. Sambol S.P., Merrigan M.M., Tang J.K., Johnson S., Gerding D.N. Colonization for the prevention of Clostridium difficile disease in hamsters. J Infect Dis 2002, 186:1781-1789.
127. Chang J.Y., Antonopoulos D.A., Kalra A., Tonelli A., Khalife W.T., Schmidt T.M., Young V.B. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008, 197:435-438.
128. Larsen N., Vogensen F.K., Van Den Berg F.W.J., Nielsen D.S., Andreasen A.S., Pedersen B.K., Al-Soud W.A., Sørensen S.J., Hansen L.H., Jakobsen M. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 2010, 5:e9085.
129. Wu X., Ma C., Han L., Nawaz M., Gao F., Zhang X., Yu P., Zhao C., Li L., Zhou A., Wang J., Moore J.E., Millar B.C., Xu J. Molecular characterisation of the faecal microbiota in patients with type II diabetes. Curr Microbiol 2010, 61:69-78.
130. Ley R.E., Bäckhed F., Turnbaugh P., Lozupone C.A., Knight R.D., Gordon J.I. Obesity alters gut microbial ecology. Proc Nat Acad Sci USA 2005, 102:11070-11075.
131. Ananthakrishnan A.N. Clostridium difficile infection: epidemiology, risk factors and management. Nat Rev Gastroenterol Hepatol 2010, 8:17-26.
132. Vrieze A., Van Nood E., Holleman F., Salojarvi J., Kootte R.S., Bartelsman J.F., Dallinga-Thie G.M., Ackermans M.T., Serlie M.J., Oozeer R., Derrien M., Druesne A., Van Hylckama Vlieg J.E., Bloks V.W., Groen A.K., Heilig H.G., Zoetendal E.G., Stroes E.S., de Vos W.M., Hoekstra J.B., Nieuwdorp M. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012, 143:913-916. e917.
133. Monot M., Boursaux-Eude C., Thibonnier M., Vallenet D., Moszer I., Medigue C., Martin-Verstraete I., Dupuy B. Reannotation of the genome sequence of Clostridium difficile strain 630. J Med Microbiol 2011, 60:1193-1199.
134. 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:R102.