Systems analysis of the transcriptional response of human ileocecal epithelial cells to Clostridium difficile toxins and effects on cell cycle control

BMC Systems Biology

Volumn 6, Issue , 2012, Pages

  D'Auria, Kevin M ^a   Donato, Gina M ^b   Gray, Mary C ^b   Kolling, Glynis L ^b   Warren, Cirle A ^b   Cave, Lauren M ^b   Solga, Michael D ^c   Lannigan, Joanne A ^c   Papin, Jason A ^a   Hewlett, Erik L ^b  

^a University of Virginia   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Cell cycle; Clostridium difficile; Epithelial cell; Gene expression; Toxin a; Toxin b

Indexed keywords

CLOSTRIDIUM DIFFICILE;

BACTERIAL PROTEIN; BACTERIAL TOXIN; ENTEROTOXIN; TCDA PROTEIN, CLOSTRIDIUM DIFFICILE; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE;

APOPTOSIS; ARTICLE; CECUM; CELL CULTURE; CELL CYCLE; CELL PROLIFERATION; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HUMAN; ILEUM; METABOLISM; METHODOLOGY; MICROARRAY ANALYSIS; SYSTEMS BIOLOGY; TIME;

APOPTOSIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CECUM; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; ENTEROTOXINS; EPITHELIAL CELLS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; ILEUM; MICROARRAY ANALYSIS; SYSTEMS BIOLOGY; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84855458187     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-2     Document Type: Article

References (49)

1. Freeman J, Bauer MP, Baines SD, Corver J, Fawley WN, Goorhuis B, Kuijper EJ, Wilcox MH. The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev 2010, 23(3):529-549. 10.1128/CMR.00082-09, 2901659, 20610822.
2. Warny M, Pepin J, Fang A, Killgore G, Thompson A, Brazier J, Frost E, McDonald LC. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 2005, 366(9491):1079-1084. 10.1016/S0140-6736(05)67420-X, 16182895.
3. Zilberberg MD, Shorr AF, Kollef MH. Increase in adult Clostridium difficile-related hospitalizations and case-fatality rate, United States, 2000-2005. Emerg Infect Dis 2008, 14(6):929-931. 10.3201/eid1406.071447, 2600276, 18507904.
4. Dubberke ER, Wertheimer AI. Review of current literature on the economic burden of Clostridium difficile infection. Infect Control Hosp Epidemiol 2009, 30(1):57-66. 10.1086/592981, 19049438.
5. 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(3):706-711. 10.1016/S0006-291X(02)02919-4, 12507507.
6. Papatheodorou P, Zamboglou C, Genisyuerek S, Guttenberg G, Aktories K. Clostridial glucosylating toxins enter cells via clathrin-mediated endocytosis. PLoS One 2010, 5(5):e10673. 10.1371/journal.pone.0010673, 2871790, 20498856.
7. Egerer M, Giesemann T, Jank T, Satchell KJ, Aktories K. Auto-catalytic cleavage of Clostridium difficile toxins A and B depends on cysteine protease activity. J Biol Chem 2007, 282(35):25314-25321. 10.1074/jbc.M703062200, 17591770.
8. Nusrat A, von Eichel-Streiber C, Turner JR, Verkade P, Madara JL, Parkos CA. Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Infect Immun 2001, 69(3):1329-1336. 10.1128/IAI.69.3.1329-1336.2001, 98024, 11179295.
9. Tompkins WA, Watrach AM, Schmale JD, Schultz RM, Harris JA. Cultural and antigenic properties of newly established cell strains derived from adenocarcinomas of the human colon and rectum. J Natl Cancer Inst 1974, 52(4):1101-1110.
10. Comer JE, Galindo CL, Chopra AK, Peterson JW. GeneChip analyses of global transcriptional responses of murine macrophages to the lethal toxin of Bacillus anthracis. Infect Immun 2005, 73(3):1879-1885. 10.1128/IAI.73.3.1879-1885.2005, 1064962, 15731093.
11. Comer JE, Galindo CL, Zhang F, Wenglikowski AM, Bush KL, Garner HR, Peterson JW, Chopra AK. Murine macrophage transcriptional and functional responses to Bacillus anthracis edema toxin. Microb Pathog 2006, 41:(2-3):96-110.
12. Lu C, Pelech S, Zhang H, Bond J, Spach K, Noubade R, Blankenhorn EP, Teuscher C. Pertussis toxin induces angiogenesis in brain microvascular endothelial cells. J Neurosci Res 2008, 86(12):2624-2640. 10.1002/jnr.21716, 18500752.
13. Leyva-Illades D, Cherla RP, Galindo CL, Chopra AK, Tesh VL. Global transcriptional response of macrophage-like THP-1 cells to Shiga toxin type 1. Infect Immun 2010, 78(6):2454-2465. 10.1128/IAI.01341-09, 2876531, 20351145.
14. Nougayrede JP, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005, 13(3):103-110. 10.1016/j.tim.2005.01.002, 15737728.
15. Fiorentini C, Fabbri A, Falzano L, Fattorossi A, Matarrese P, Rivabene R, Donelli G. Clostridium difficile toxin B induces apoptosis in intestinal cultured cells. Infect Immun 1998, 66(6):2660-2665. 108253, 9596731.
16. Kim H, Kokkotou E, Na X, Rhee SH, Moyer MP, Pothoulakis C, Lamont JT. Clostridium difficile toxin A-induced colonocyte apoptosis involves p53-dependent p21(WAF1/CIP1) induction via p38 mitogen-activated protein kinase. Gastroenterology 2005, 129(6):1875-1888. 10.1053/j.gastro.2005.09.011, 16344056.
17. Gerhard R, Nottrott S, Schoentaube J, Tatge H, Olling A, Just I. Glucosylation of Rho GTPases by Clostridium difficile toxin A triggers apoptosis in intestinal epithelial cells. J Med Microbiol 2008, 57(Pt 6):765-770.
18. Nottrott S, Schoentaube J, Genth H, Just I, Gerhard R. Clostridium difficile toxin A-induced apoptosis is p53-independent but depends on glucosylation of Rho GTPases. Apoptosis 2007, 12(8):1443-1453. 10.1007/s10495-007-0074-8, 17437185.
19. Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F. A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 2004, 99(468):909-917.
20. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
21. Smyth GK. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. Springer, New York, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, edn.
22. Barrell D, Dimmer E, Huntley RP, Binns D, O'Donovan C, Apweiler R. The GOA database in 2009--an integrated Gene Ontology Annotation resource. Nucleic Acids Res 2009, (37 Database):D396-403.
23. Alexa A, Rahnenfuhrer J, Lengauer T. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 2006, 22(13):1600-1607. 10.1093/bioinformatics/btl140, 16606683.
24. George TC, Basiji DA, Hall BE, Lynch DH, Ortyn WE, Perry DJ, Seo MJ, Zimmerman CA, Morrissey PJ. Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer. Cytometry A 2004, 59(2):237-245.
25. Henery S, George T, Hall B, Basiji D, Ortyn W, Morrissey P. Quantitative image based apoptotic index measurement using multispectral imaging flow cytometry: a comparison with standard photometric methods. Apoptosis 2008, 13(8):1054-1063. 10.1007/s10495-008-0227-4, 18543109.
26. 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(7):1734-1741. 10.1172/JCI119698, 508356, 9312171.
27. Qa'Dan M, Ramsey M, Daniel J, Spyres LM, Safiejko-Mroczka B, Ortiz-Leduc W, Ballard JD. Clostridium difficile toxin B activates dual caspase-dependent and caspase-independent apoptosis in intoxicated cells. Cell Microbiol 2002, 4(7):425-434. 10.1046/j.1462-5822.2002.00201.x, 12102688.
28. Carneiro BA, Fujii J, Brito GA, Alcantara C, Oria RB, Lima AA, Obrig T, Guerrant RL. Caspase and bid involvement in Clostridium difficile toxin A-induced apoptosis and modulation of toxin A effects by glutamine and alanyl-glutamine in vivo and in vitro. Infect Immun 2006, 74(1):81-87. 10.1128/IAI.74.1.81-87.2006, 1346681, 16368960.
29. Brito GA, Fujji J, Carneiro-Filho BA, Lima AA, Obrig T, Guerrant RL. Mechanism of Clostridium difficile toxin A-induced apoptosis in T84 cells. J Infect Dis 2002, 186(10):1438-1447. 10.1086/344729, 12404159.
30. Matarrese P, Falzano L, Fabbri A, Gambardella L, Frank C, Geny B, Popoff MR, Malorni W, Fiorentini C. Clostridium difficile toxin B causes apoptosis in epithelial cells by thrilling mitochondria. Involvement of ATP-sensitive mitochondrial potassium channels. J Biol Chem 2007, 282(12):9029-9041. 10.1074/jbc.M607614200, 17220295.
31. He D, Hagen SJ, Pothoulakis C, Chen M, Medina ND, Warny M, LaMont JT. Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology 2000, 119(1):139-150. 10.1053/gast.2000.8526, 10889163.
32. He D, Sougioultzis S, Hagen S, Liu J, Keates S, Keates AC, Pothoulakis C, Lamont JT. Clostridium difficile toxin A triggers human colonocyte IL-8 release via mitochondrial oxygen radical generation. Gastroenterology 2002, 122(4):1048-1057. 10.1053/gast.2002.32386, 11910356.
33. Qiu B, Pothoulakis C, Castagliuolo I, Nikulasson S, LaMont JT. Participation of reactive oxygen metabolites in Clostridium difficile toxin A-induced enteritis in rats. Am J Physiol 1999, 276(2 Pt 1):G485-490.
34. Flegel WA, Muller F, Daubener W, Fischer HG, Hadding U, Northoff H. Cytokine response by human monocytes to Clostridium difficile toxin A and toxin B. Infect Immun 1991, 59(10):3659-3666. 258935, 1910012.
35. Meyer GK, Neetz A, Brandes G, Tsikas D, Butterfield JH, Just I, Gerhard R. Clostridium difficile toxins A and B directly stimulate human mast cells. Infect Immun 2007, 75(8):3868-3876. 10.1128/IAI.00195-07, 1951994, 17517880.
36. Lee JY, Park HR, Oh YK, Kim YJ, Youn J, Han JS, Kim JM. Effects of transcription factor activator protein-1 on interleukin-8 expression and enteritis in response to Clostridium difficile toxin A. J Mol Med 2007, 85(12):1393-1404. 10.1007/s00109-007-0237-7, 17639289.
37. Na X, Zhao D, Koon HW, Kim H, Husmark J, Moyer MP, Pothoulakis C, LaMont JT. Clostridium difficile toxin B activates the EGF receptor and the ERK/MAP kinase pathway in human colonocytes. Gastroenterology 2005, 128(4):1002-1011. 10.1053/j.gastro.2005.01.053, 15825081.
38. Murray AW. Recycling the cell cycle: cyclins revisited. Cell 2004, 116(2):221-234. 10.1016/S0092-8674(03)01080-8, 14744433.
39. Denicourt C, Dowdy SF. Cip/Kip proteins: more than just CDKs inhibitors. Genes Dev 2004, 18(8):851-855. 10.1101/gad.1205304, 15107401.
40. Huelsenbeck SC, May M, Schmidt G, Genth H. Inhibition of cytokinesis by Clostridium difficile toxin B and cytotoxic necrotizing factors--reinforcing the critical role of RhoA in cytokinesis. Cell Motil Cytoskeleton 2009, 66(11):967-975. 10.1002/cm.20390, 19504561.
41. Riegler M, Sedivy R, Pothoulakis C, Hamilton G, Zacherl J, Bischof G, Cosentini E, Feil W, Schiessel R, LaMont JT, et al. Clostridium difficile toxin B is more potent than toxin A in damaging human colonic epithelium in vitro. J Clin Invest 1995, 95(5):2004-2011. 10.1172/JCI117885, 295778, 7738167.
42. Kuehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A, Minton NP. The role of toxin A and toxin B in Clostridium difficile infection. Nature 2010,
43. Lyras D, O'Connor JR, Howarth PM, Sambol SP, Carter GP, Phumoonna T, Poon R, Adams V, Vedantam G, Johnson S, et al. Toxin B is essential for virulence of Clostridium difficile. Nature 2009, 458(7242):1176-1179. 10.1038/nature07822, 2679968, 19252482.
44. Janvilisri T, Scaria J, Chang YF. Transcriptional profiling of Clostridium difficile and Caco-2 cells during infection. J Infect Dis 2010, 202(2):282-290. 10.1086/653484, 2891111, 20521945.
45. Ameyar M, Wisniewska M, Weitzman JB. A role for AP-1 in apoptosis: the case for and against. Biochimie 2003, 85(8):747-752. 10.1016/j.biochi.2003.09.006, 14585541.
46. Welsh CF, Roovers K, Villanueva J, Liu Y, Schwartz MA, Assoian RK. Timing of cyclin D1 expression within G1 phase is controlled by Rho. Nat Cell Biol 2001, 3(11):950-957. 10.1038/ncb1101-950, 11715015.
47. Huelsenbeck J, Dreger S, Gerhard R, Barth H, Just I, Genth H. Difference in the cytotoxic effects of toxin B from Clostridium difficile strain VPI 10463 and toxin B from variant Clostridium difficile strain 1470. Infect Immun 2007, 75(2):801-809. 10.1128/IAI.01705-06, 1828479, 17145947.
48. Kim M, Ashida H, Ogawa M, Yoshikawa Y, Mimuro H, Sasakawa C. Bacterial interactions with the host epithelium. Cell Host Microbe 2010, 8(1):20-35. 10.1016/j.chom.2010.06.006, 20638639.
49. Resnik P. Semantic similarity in a taxonomy: An information-based measure and its application to problems of ambiguity in natural language. J Artif Intell Res 1999, 11:95-130.