Modeling the Role of Peroxisome Proliferator-Activated Receptor γ and MicroRNA-146 in Mucosal Immune Responses to Clostridium difficile

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Viladomiu, Monica ^a,b   Hontecillas, Raquel ^a,b   Pedragosa, Mireia ^a,b   Carbo, Adria ^a,b   Hoops, Stefan ^a,b   Michalak, Pawel ^a,b   Michalak, Katarzyna ^a   Guerrant, Richard L ^b,c   Roche, James K ^b,c   Warren, Cirle A ^b,c   Bassaganya Riera, Josep ^a,b  

^a VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 17; MICRORNA; MICRORNA 146B; NUCLEAR RECEPTOR COACTIVATOR; NUCLEAR RECEPTOR COACTIVATOR 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE EXACERBATION; DOWN REGULATION; GENE OVEREXPRESSION; LAMINA PROPRIA; MATHEMATICAL MODEL; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SPLEEN; TH17 CELL; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; BASE SEQUENCE; CLOSTRIDIUM DIFFICILE; COLON; DNA PRIMERS; ENTEROCOLITIS, PSEUDOMEMBRANOUS; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HISTOLOGICAL TECHNIQUES; IMMUNOPHENOTYPING; INTERLEUKIN-10; INTERLEUKIN-17; MICE; MICE, INBRED C57BL; MICRORNAS; MODELS, IMMUNOLOGICAL; MOLECULAR SEQUENCE DATA; PPAR GAMMA; REAL-TIME POLYMERASE CHAIN REACTION; TH17 CELLS; THIAZOLIDINEDIONES;

EID: 84867423956     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047525     Document Type: Article

References (53)

1. Vaishnavi C, (2010) Clinical spectrum & pathogenesis of Clostridium difficile associated diseases. Indian J Med Res 131: 487-499.
2. Hookman P, Barkin JS, (2009) Clostridium difficile associated infection, diarrhea and colitis. World J Gastroenterol 15: 1554-1580.
3. Bartlett JG, Onderdonk AB, Cisneros RL, Kasper DL, (1977) Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters. J Infect Dis 136: 701-705.
4. George RH, Symonds JM, Dimock F, Brown JD, Arabi Y, et al. (1978) Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J 1: 695.
5. Kim JW, Lee KL, Jeong JB, Kim BG, Shin S, et al. (2010) Proton pump inhibitors as a risk factor for recurrence of Clostridium-difficile-associated diarrhea. World J Gastroenterol 16: 3573-3577.
6. Lim PL, Barkham TM, Ling LM, Dimatatac F, Alfred T, et al. (2008) Increasing incidence of Clostridium difficile-associated disease, Singapore. Emerg Infect Dis 14: 1487-1489.
7. Khanna S, Pardi DS, (2010) The growing incidence and severity of Clostridium difficile infection in inpatient and outpatient settings. Expert Rev Gastroenterol Hepatol 4: 409-416.
8. Zilberberg MD, Shorr AF, Kollef MH, (2008) Increase in adult Clostridium difficile-related hospitalizations and case-fatality rate, United States, 2000-2005. Emerg Infect Dis 14: 929-931.
9. Khanna S, Pardi DS, Aronson SL, Kammer PP, Orenstein R, et al. (2012) The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol 107: 89-95.
10. Kuehn BM, (2011) Scientists seek strategies to prevent Clostridium difficile infections. JAMA 306: 1849-1850.
11. Barbut F, Jones G, Eckert C, (2011) Epidemiology and control of Clostridium difficile infections in healthcare settings: an update. Curr Opin Infect Dis 24: 370-376.
12. Akerlund T, Persson I, Unemo M, Noren T, Svenungsson B, et al. (2008) Increased sporulation rate of epidemic Clostridium difficile Type 027/NAP1. J Clin Microbiol 46: 1530-1533.
13. Merrigan M, Venugopal A, Mallozzi M, Roxas B, Viswanathan VK, et al. (2010) Human hypervirulent Clostridium difficile strains exhibit increased sporulation as well as robust toxin production. J Bacteriol 192: 4904-4911.
14. Pawlowski SW, Archbald-Pannone L, Carman RJ, Alcantara-Warren C, Lyerly D, et al. (2009) Elevated levels of intestinal inflammation in Clostridium difficile infection associated with fluoroquinolone-resistant C. difficile. J Hosp Infect 73: 185-187.
15. McFarland LV, (2005) Alternative treatments for Clostridium difficile disease: what really works? J Med Microbiol 54: 101-111.
16. Ryan A, Lynch M, Smith SM, Amu S, Nel HJ, et al. (2011) A role for TLR4 in Clostridium difficile infection and the recognition of surface layer proteins. PLoS Pathog 7: e1002076.
17. Bassaganya-Riera J, Reynolds K, Martino-Catt S, Cui Y, Hennighausen L, et al. (2004) Activation of PPAR gamma and delta by conjugated linoleic acid mediates protection from experimental inflammatory bowel disease. Gastroenterology 127: 777-791.
18. Li M, Pascual G, Glass CK, (2000) Peroxisome proliferator-activated receptor gamma-dependent repression of the inducible nitric oxide synthase gene. Mol Cell Biol 20: 4699-4707.
19. Hontecillas R, Bassaganya-Riera J, (2007) Peroxisome proliferator-activated receptor gamma is required for regulatory CD4+ T cell-mediated protection against colitis. J Immunol 178: 2940-2949.
20. Bassaganya-Riera J, Hontecillas R, (2006) CLA and n-3 PUFA differentially modulate clinical activity and colonic PPAR-responsive gene expression in a pig model of experimental IBD. Clin Nutr 25: 454-465.
21. Lewis JD, Lichtenstein GR, Deren JJ, Sands BE, Hanauer SB, et al. (2008) Rosiglitazone for active ulcerative colitis: a randomized placebo-controlled trial. Gastroenterology 134: 688-695.
22. Bassaganya-Riera J, Hontecillas R, Horne WT, Sandridge M, Herfarth HH, et al. (2012) Conjugated linoleic acid modulates immune responses in patients with mild to moderately active Crohn's disease. Clin Nutr.
23. Guri AJ, Mohapatra SK, Horne WT, 2nd, Hontecillas R, Bassaganya-Riera J (2010) The role of T cell PPAR gamma in mice with experimental inflammatory bowel disease. BMC Gastroenterol 10: 60.
24. Hontecillas R, Horne WT, Climent M, Guri AJ, Evans C, et al. (2011) Immunoregulatory mechanisms of macrophage PPAR-gamma in mice with experimental inflammatory bowel disease. Mucosal Immunol 4: 304-313.
25. Mohapatra SK, Guri AJ, Climent M, Vives C, Carbo A, et al. (2010) Immunoregulatory actions of epithelial cell PPAR gamma at the colonic mucosa of mice with experimental inflammatory bowel disease. PLoS One 5: e10215.
26. Klotz L, Burgdorf S, Dani I, Saijo K, Flossdorf J, et al. (2009) The nuclear receptor PPAR gamma selectively inhibits Th17 differentiation in a T cell-intrinsic fashion and suppresses CNS autoimmunity. J Exp Med 206: 2079-2089.
27. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
28. Hassan T, McKiernan PJ, McElvaney NG, Cryan SA, Greene CM, (2012) Therapeutic modulation of miRNA for the treatment of proinflammatory lung diseases. Expert Rev Anti Infect Ther 10: 359-368.
29. Papaioannou MD, Nef S, (2010) microRNAs in the testis: building up male fertility. J Androl 31: 26-33.
30. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
31. Dalal SR, Kwon JH, (2010) The Role of MicroRNA in Inflammatory Bowel Disease. Gastroenterol Hepatol (N Y) 6: 714-722.
32. Chen CZ, Li L, Lodish HF, Bartel DP, (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303: 83-86.
33. Sonkoly E, Stahle M, Pivarcsi A, (2008) MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin Cancer Biol 18: 131-140.
34. Oertli M, Engler DB, Kohler E, Koch M, Meyer TF, et al. (2011) MicroRNA-155 is essential for the T cell-mediated control of Helicobacter pylori infection and for the induction of chronic Gastritis and Colitis. J Immunol 187: 3578-3586.
35. Akiyama TE, Sakai S, Lambert G, Nicol CJ, Matsusue K, et al. (2002) Conditional disruption of the peroxisome proliferator-activated receptor gamma gene in mice results in lowered expression of ABCA1, ABCG1, and apoE in macrophages and reduced cholesterol efflux. Mol Cell Biol 22: 2607-2619.
36. Wagner KU, McAllister K, Ward T, Davis B, Wiseman R, et al. (2001) Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res 10: 545-553.
37. Cui Y, Miyoshi K, Claudio E, Siebenlist UK, Gonzalez FJ, et al. (2002) Loss of the peroxisome proliferation-activated receptor gamma (PPARgamma) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. J Biol Chem 277: 17830-17835.
38. Wohlfert EA, Nichols FC, Nevius E, Clark RB, (2007) Peroxisome proliferator-activated receptor gamma (PPARgamma) and immunoregulation: enhancement of regulatory T cells through PPARgamma-dependent and-independent mechanisms. J Immunol 178: 4129-4135.
39. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, et al. (2008) A mouse model of Clostridium difficile-associated disease. Gastroenterology 135: 1984-1992.
40. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ, (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-158.
41. Artzi S, Kiezun A, Shomron N, (2008) miRNAminer: a tool for homologous microRNA gene search. BMC Bioinformatics 9: 39.
42. Garbacki N, Di Valentin E, Huynh-Thu VA, Geurts P, Irrthum A, et al. (2011) MicroRNAs profiling in murine models of acute and chronic asthma: a relationship with mRNAs targets. PLoS One 6: e16509.
43. John B, Enright AJ, Aravin A, Tuschl T, Sander C, et al. (2004) Human MicroRNA targets. PLoS Biol 2: e363.
44. Hontecillas R, Wannemeulher MJ, Zimmerman DR, Hutto DL, Wilson JH, et al. (2002) Nutritional regulation of porcine bacterial-induced colitis by conjugated linoleic acid. J Nutr 132: 2019-2027.
45. Funahashi A, Jouraku A, Matsuoka Y, Kitano H, (2007) Integration of CellDesigner and SABIO-RK. In Silico Biol 7: S81-90.
46. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, et al. (2006) COPASI-a COmplex PAthway SImulator. Bioinformatics 22: 3067-3074.
47. Kuntz JL, Chrischilles EA, Pendergast JF, Herwaldt LA, Polgreen PM, (2011) Incidence of and risk factors for community-associated Clostridium difficile infection: a nested case-control study. BMC Infect Dis 11: 194.
48. Blondeau JM, (2009) What have we learned about antimicrobial use and the risks for Clostridium difficile-associated diarrhoea? J Antimicrob Chemother 63: 238-242.
49. Kyne L, Sougioultzis S, McFarland LV, Kelly CP, (2002) Underlying disease severity as a major risk factor for nosocomial Clostridium difficile diarrhea. Infect Control Hosp Epidemiol 23: 653-659.
50. Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, et al. (2007) Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 8: 240.
51. Schmidt WM, Spiel AO, Jilma B, Wolzt M, Muller M, (2009) In vivo profile of the human leukocyte microRNA response to endotoxemia. Biochem Biophys Res Commun 380: 437-441.
52. Lederhuber H, Baer K, Altiok I, Sadeghi K, Herkner KR, et al. (2011) MicroRNA-146: tiny player in neonatal innate immunity? Neonatology 99: 51-56.
53. Taganov KD, Boldin MP, Chang KJ, Baltimore D, (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 103: 12481-12486.