Systems modeling of interactions between mucosal immunity and the gut microbiome during Clostridium difficile infection

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Leber, Andrew ^a   Viladomiu, Monica ^a   Hontecillas, Raquel ^a   Abedi, Vida ^a   Philipson, Casandra ^a   Hoops, Stefan ^a   Howard, Brad ^a   Bassaganya Riera, Josep ^a  

^a VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; CLOSTRIDIUM DIFFICILE INFECTION; COMMENSALISM; CONTROLLED STUDY; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; INTESTINE FLORA; LAMINA PROPRIA; LEUKOCYTE ACTIVATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; REGULATORY T LYMPHOCYTE; SIMULATION; TH17 CELL; BIOLOGICAL MODEL; CLOSTRIDIUM INFECTION; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; PATHOGENICITY; PEPTOCLOSTRIDIUM DIFFICILE;

CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; IMMUNITY, MUCOSAL; MICROBIOTA; MODELS, BIOLOGICAL;

EID: 84942254105     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134849     Document Type: Article

References (59)

1. Lo Vecchio A, Zacur GM. Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options. Curr Opin Gastroenterol. 2012 Jan; 28(1):1-9. doi: 10.1097/MOG.0b013e32834bc9a9 PMID: 22134217
2. Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, et al. Burden ofClostridium difficileInfection in the United States. New England Journal of Medicine. 2015; 372(9):825-34. doi: 10.1056/NEJMoa1408913 PMID: 25714160
3. Hall AJ, Curns AT, McDonald LC, Parashar UD, Lopman BA. The Roles of Clostridium difficile and Norovirus Among Gastroenteritis-Associated Deaths in the United States, 1999-2007. Clinical Infectious Diseases. 2012; 55(2):216-23. doi: 10.1093/cid/cis386 PMID: 22491338
4. See I, Mu Y, Cohen J, Beldavs ZG, Winston LG, Dumyati G, et al. NAP1 strain type predicts outcomes from Clostridium difficile infection. Clin Infect Dis. 2014 May; 58(10):1394-400. doi: 10.1093/cid/ciu125 PMID: 24604900
5. Suwantarat N, Bobak DA. Current Status of Nonantibiotic and Adjunct Therapies for Clostridium difficile Infection. Current Infectious Disease Reports. 2010; 13(1):21-7.
6. Lowy I, Molrine DC, Leav BA, Blair BM, Baxter R, Gerding DN, et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N Engl J Med. 2010 Jan 21; 362(3):197-205. doi: 10.1056/NEJMoa0907635 PMID: 20089970
7. Gilmore MS, Lawley TD, Clare S, Walker AW, Stares MD, Connor TR, et al. Targeted Restoration of the Intestinal Microbiota with a Simple, Defined Bacteriotherapy Resolves Relapsing Clostridium difficile Disease in Mice. PLoS Pathogens. 2012; 8(10):e1002995. doi: 10.1371/journal.ppat.1002995 PMID: 23133377
8. Holmes E, Li JV, Marchesi JR, Nicholson JK. Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab. 2012 Nov 7; 16(5):559-64. doi: 10.1016/j.cmet.2012.10.007 PMID: 23140640
9. Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature. 2014; 517(7533):205-8. doi: 10.1038/nature13828 PMID: 25337874
10. Iapichino G, Callegari ML, Marzorati S, Cigada M, Corbella D, Ferrari S, et al. Impact of antibiotics on the gut microbiota of critically ill patients. J Med Microbiol. 2008 Aug; 57(Pt 8):1007-14.
11. Hecht G, Pothoulakis C, LaMont JT, Madara JL. Clostridium difficile toxin A perturbs cytoskeletal structure and tight junction permeability of cultured human intestinal epithelial monolayers. J Clin Invest. 1988 Nov; 82(5):1516-24. PMID: 3141478
12. Jafari NV, Kuehne SA, Bryant CE, Elawad M, Wren BW, Minton NP, et al. Clostridium difficile modulates host innate immunity via toxin-independent and dependent mechanism(s). PLoS One. 2013; 8(7): e69846. doi: 10.1371/journal.pone.0069846 PMID: 23922820
13. Jarchum I, Liu M, Shi C, Equinda M, Pamer EG. Critical role for MyD88-mediated neutrophil recruitment during Clostridium difficile colitis. Infect Immun. 2012 Sep; 80(9):2989-96. doi: 10.1128/IAI.00448-12 PMID: 22689818
14. Brazil JC, Lee WY, Kolegraff KN, Nusrat A, Parkos CA, Louis NA. Neutrophil migration across intestinal epithelium: evidence for a role of CD44 in regulating detachment of migrating cells from the luminal surface. J Immunol. 2010 Dec 1; 185(11):7026-36. doi: 10.4049/jimmunol.1001293 PMID: 20974992
15. Ausiello CM, Cerquetti M, Fedele G, Spensieri F, Palazzo R, Nasso M, et al. Surface layer proteins from Clostridium difficile induce inflammatory and regulatory cytokines in human monocytes and dendritic cells. Microbes Infect. 2006 Sep; 8(11):2640-6. PMID: 16935543
16. Stagg AJ, Hart AL, Knight SC, Kamm MA. The dendritic cell: its role in intestinal inflammation and relationship with gut bacteria. Gut. 2003 Oct; 52(10):1522-9. PMID: 12970149
17. Carbo A, Hontecillas R, Kronsteiner B, Viladomiu M, Pedragosa M, Lu P, et al. Systems Modeling of Molecular Mechanisms Controlling Cytokine-driven CD4+ T Cell Differentiation and Phenotype Plasticity. PLoS Computational Biology. 2013; 9(4):e1003027. doi: 10.1371/journal.pcbi.1003027 PMID: 23592971
18. Barnes MJ, Powrie F. Regulatory T cells reinforce intestinal homeostasis. Immunity. 2009 Sep 18; 31(3):401-11. doi: 10.1016/j.immuni.2009.08.011 PMID: 19766083
19. Miao H, Hollenbaugh JA, Zand MS, Holden-Wiltse J, Mosmann TR, Perelson AS, et al. Quantifying the early immune response and adaptive immune response kinetics in mice infected with influenza A virus. J Virol. 2010 Jul; 84(13):6687-98. doi: 10.1128/JVI.00266-10 PMID: 20410284
20. Carbo A, Bassaganya-Riera J, Pedragosa M, Viladomiu M, Marathe M, Eubank S, et al. Predictive computational modeling of the mucosal immune responses during Helicobacter pylori infection. PLoS One. 2013; 8(9):e73365. doi: 10.1371/journal.pone.0073365 PMID: 24039925
21. Wendelsdorf K, Bassaganya-Riera J, Hontecillas R, Eubank S. Model of colonic inflammation: Immune modulatory mechanisms in inflammatory bowel disease. Journal of Theoretical Biology. 2010; 264(4):1225-39. doi: 10.1016/j.jtbi.2010.03.027 PMID: 20362587
22. Pflughoeft KJ, Versalovic J. Human microbiome in health and disease. Annu Rev Pathol. 2012; 7:99-122. doi: 10.1146/annurev-pathol-011811-132421 PMID: 21910623
23. Viladomiu M, Hontecillas R, Pedragosa M, Carbo A, Hoops S, Michalak P, et al. Modeling the Role of Peroxisome Proliferator-Activated Receptor gamma and MicroRNA-146 in Mucosal Immune Responses to Clostridium difficile. PLoS One. 2012; 7(10):e47525. doi: 10.1371/journal.pone.0047525 PMID: 23071818
24. Blake KM, Carrigan SO, Issekutz AC, Stadnyk AW. Neutrophils migrate across intestinal epithelium using beta2 integrin (CD11b/CD18)-independent mechanisms. Clinical and Experimental Immunology. 2004; 136(2):262-8. PMID: 15086389
25. Mahida YR, Makh S., Hyde S., Gray T., and Borriello S.P. Effect of Clostridium difficile toxin A on human intestinal epithelial cells: induction of interleukin 8 production and apoptosis after cell detachment. Gut. 1996; 38:337-47. PMID: 8675084
26. Riegler MS, R., Pothoulakis C., Hamilton G., Zacherl J., Bischof G., Cosentini E., Feil W., Schiessel R., Lamont J.T., and Wenzl E. Clostridium difficile Toxin B is more potent than Toxin A in damaging human colonic epithleium in vitro. J Clin Invest. 1995; 95:2004-11. PMID: 7738167
27. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, Simus N, et al. COPASI - a COmplex PAthway SImulator. Bioinformatics. 2006 Dec 15; 22(24):3067-74. PMID: 17032683
28. Terrier MCZ, Simonet M.L., Bichard P. and Frossard J.L. Recurrent Clostridium difficile infections. World J Gastroenterol. 2014; 20(23):7416-23. doi: 10.3748/wjg.v20.i23.7416 PMID: 24966611
29. Hussack G, Arbabi-Ghahroudi M, van Faassen H, Songer JG, Ng KKS, MacKenzie R, et al. Neutralization of Clostridium difficile Toxin A with Single-domain Antibodies Targeting the Cell Receptor Binding Domain. Journal of Biological Chemistry. 2011; 286(11):8961-76. doi: 10.1074/jbc.M110.198754 PMID: 21216961
30. Foglia G, Shah S, Luxemburger C, Pietrobon PJF. Clostridium difficile: Development of a novel candidate vaccine. Vaccine. 2012; 30(29):4307-9. doi: 10.1016/j.vaccine.2012.01.056 PMID: 22682287
31. McDermott AJ, Higdon KE, Muraglia R, Erb-Downward JR, Falkowski NR, McDonald RA, et al. The role of Gr-1+cells and tumour necrosis factor-αsignalling duringClostridium difficilecolitis in mice. Immunology. 2015; 144(4):704-16. doi: 10.1111/imm.12425 PMID: 25399934
32. Pothoulakis C, Lamont JT. Microbes and microbial toxins: paradigms for microbial-mucosal interactions II. The integrated response of the intestine to Clostridium difficile toxins. Am J Physiol Gastrointest Liver Physiol. 2001 Feb; 280(2):G178-83. PMID: 11208538
33. Kasendra M, Barrile R, Leuzzi R, Soriani M. Clostridium difficile toxins facilitate bacterial colonization by modulating the fence and gate function of colonic epithelium. J Infect Dis. 2014 Apr 1; 209(7):1095-104. doi: 10.1093/infdis/jit617 PMID: 24273043
34. McLoughlin RM, Mills KH. Influence of gastrointestinal commensal bacteria on the immune responses that mediate allergy and asthma. J Allergy Clin Immunol. 2011 May; 127(5):1097-107; quiz 108-9. doi: 10.1016/j.jaci.2011.02.012 PMID: 21420159
35. Longman RS, Diehl GE, Victorio DA, Huh JR, Galan C, Miraldi ER, et al. CX(3)CR1(+) mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J Exp Med. 2014 Jul 28; 211(8):1571-83. doi: 10.1084/jem.20140678 PMID: 25024136
36. Scott KP, Antoine J-M, Midtvedt T, van Hemert S. Manipulating the gut microbiota to maintain health and treat disease. Microbial Ecology in Health & Disease. 2015; 26(0).
37. Marteau PR, de Vrese M., Cellier C.J., and Schrezenmeir J. Protection from gastrointestinal diseases with the use of probiotics. Am J Clin Nutr. 2001; 73(2):430-6.
38. Sorg JA, Sonenshein AL. Bile Salts and Glycine as Cogerminants for Clostridium difficile Spores. Journal of Bacteriology. 2008; 190(7):2505-12. doi: 10.1128/JB.01765-07 PMID: 18245298
39. Sorg JA, Sonenshein AL. Chenodeoxycholate Is an Inhibitor of Clostridium difficile Spore Germination. Journal of Bacteriology. 2008; 191(3):1115-7. doi: 10.1128/JB.01260-08 PMID: 19060152
40. Weingarden AR, Chen C., Bobr A., Yao D. Lu Y, Nelson V.M., Sadowsky M.J., and Khoruts A. Microbiota transplantation restores normal fecal bile acid composition in recurrent Clostridium difficile infection. Am J Physiol Gastrointest Liver Physiol. 2014; 306:G310-G9. doi: 10.1152/ajpgi.00282.2013 PMID: 24284963
41. Prado-Montes de Oca E. Human β-defensin 1: A restless warrior against allergies, infections and cancer. The International Journal of Biochemistry & Cell Biology. 2010; 42(6):800-4.
42. Pazgier M, Hoover DM, Yang D, Lu W, Lubkowski J. Human β-defensins. Cellular and Molecular Life Sciences. 2006; 63(11):1294-313. PMID: 16710608
43. Nacken W, Roth J, Sorg C, Kerkhoff C. S100A9/S100A8: Myeloid representatives of the S100 protein family as prominent players in innate immunity. Microscopy Research and Technique. 2003; 60(6):569-80. PMID: 12645005
44. Louie TJ, Miller MA, Mullane KM, Weiss K, Lentnek A, Golan Y, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med. 2011 Feb 3; 364(5):422-31. doi: 10.1056/NEJMoa0910812 PMID: 21288078
45. Buffie CG, Jarchum I, Equinda M, Lipuma L, Gobourne A, Viale A, et al. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect Immun. 2012 Jan; 80(1):62-73. doi: 10.1128/IAI.05496-11 PMID: 22006564
46. Ishida Y, Maegawa T, Kondo T, Kimura A, Iwakura Y, Nakamura S, et al. Essential Involvement of IFN-in Clostridium difficile Toxin A-Induced Enteritis. The Journal of Immunology. 2004; 172(5):3018-25. PMID: 14978106
47. Schlackow I, Walker AS, Dingle K, Griffiths D, Oakley S, Finney J, et al. Surveillance of infection severity: a registry study of laboratory diagnosed Clostridium difficile. PLoS Med. 2012; 9(7):e1001279. doi: 10.1371/journal.pmed.1001279 PMID: 22859914
48. Gasch M, Goroll T, Bauer M, Hinz D, Schütze N, Polte T, et al. Generation of IL-8 and IL-9 Producing CD4+ T Cells Is Affected by Th17 Polarizing Conditions and AHR Ligands. Mediators of Inflammation. 2014; 2014:1-14.
49. Rao K, Walk ST, Micic D, Chenoweth E, Deng L, Galecki AT, et al. Procalcitonin levels associate with severity of Clostridium difficile infection. PLoS One. 2013; 8(3):e58265. doi: 10.1371/journal.pone.0058265 PMID: 23505476
50. Rao K, Erb-Downward JR, Walk ST, Micic D, Falkowski N, Santhosh K, et al. The systemic inflammatory response to Clostridium difficile infection. PLoS One. 2014; 9(3):e92578. doi: 10.1371/journal.pone.0092578 PMID: 24643077
51. Swale A, Miyajima F, Roberts P, Hall A, Little M, Beadsworth MB, et al. Calprotectin and lactoferrin faecal levels in patients with Clostridium difficile infection (CDI): a prospective cohort study. PLoS One. 2014; 9(8):e106118. doi: 10.1371/journal.pone.0106118 PMID: 25170963
52. Mei Y, Abedi V, Carbo A, Zhang X, Lu P, Philipson CW, et al. Multiscale modeling of mucosal immune responses. BMC Bioinformatics. 2015;In press.
53. Beard DA, Lu J, Hübner K, Nanjee MN, Brinton EA, Mazer NA. An In-Silico Model of Lipoprotein Metabolism and Kinetics for the Evaluation of Targets and Biomarkers in the Reverse Cholesterol Transport Pathway. PLoS Computational Biology. 2014; 10(3):e1003509. doi: 10.1371/journal.pcbi.1003509 PMID: 24625468
54. Mathew S, Bartels J, Banerjee I, Vodovotz Y. Global sensitivity analysis of a mathematical model of acute inflammation identifies nonlinear dependence of cumulative tissue damage on host interleukin-6 responses. Journal of Theoretical Biology. 2014; 358:132-48. doi: 10.1016/j.jtbi.2014.05.036 PMID: 24909493
55. Shapira Y, Agmon-Levin N, Shoenfeld Y. Defining and analyzing geoepidemiology and human autoimmunity. J Autoimmun. 2010 May; 34(3):J168-77. doi: 10.1016/j.jaut.2009.11.018 PMID: 20034761
56. Okada H, Kuhn C, Feillet H, Bach JF. The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin Exp Immunol. 2010 Apr; 160(1):1-9. doi: 10.1111/j.1365-2249.2010.04139.x PMID: 20415844
57. Smyth DJ, Cooper JD, Howson JM, Clarke P, Downes K, Mistry T, et al. FUT2 nonsecretor status links type 1 diabetes susceptibility and resistance to infection. Diabetes. 2011 Nov; 60(11):3081-4. doi: 10.2337/db11-0638 PMID: 22025780
58. McGovern DP, Jones MR, Taylor KD, Marciante K, Yan X, Dubinsky M, et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet. 2010 Sep 1; 19(17):3468-76. doi: 10.1093/hmg/ddq248 PMID: 20570966
59. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, Gerding DN, et al. A Mouse Model of Clostridium difficile-Associated Disease. Gastroenterology. 2008; 135(6):1984-92. doi: 10.1053/j.gastro.2008.09.002 PMID: 18848941