Inflammatory bowel disease: factors involved in pathogenesis

 1. Cammarota G., Ianiro G., Cianci R., Bibbò S., Gasbarrini A., Currò F. The involvement of gut microbiota in inflammatory bowel disease pathogenesis: Potential for therapy. Pharmacol. Therapeut. 2015; 149, 191–212.  

2. de Souza H. S. P., Fiocchi C. Immunopathogenesis of IBD: current state of the art. Nat Rev. Gastroenterol. Hepatol. 2016; 13, 13–27.

3. Pandolfi F., Cianci R., Pagliari D., Landolfi R., Cammarota G. Cellular mediators of inflammation: Tregs and TH17 cells in gastrointestinal diseases. Mediator. Inflamm. 2009; 132028, 1149–1155.

 4. Geremia A., Biancheri P., Allan P., Corazza G. R., Di Sabatino A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun. Rev. 2014; 13, 3–10. 

 5. Bernstein C. N., Banerjee A., Targownik L. E., Singh H., Ghia J. E., Burchill C., Chateau D., Roos L. L. Caesarean section delivery is not a risk factor for development of inflammatory bowel disease: a population-based analysis. Clin. Gastroenterol. Hepatol. 2016; 14, 50–57. 

6. Salminen S., Gibson G. R., McCartney A. L., Isolauri E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut 2004; 53, 1388–1389.

 7. Ng S. C., Tang W., Leong R. W., Chen M., Ko Y., Studd C., Niewiadomski O., Bell S., Kamm M. A., de Silva H. J., Kasturiratne A., Senanayake Y. U., Ooi C. J., Ling K. L., Ong D., Goh K. L., Hilmi I., Ouyang Q., Wang Y. F., Hu P., Zhu Z., Zeng Z., Wu K, Wang X., Xia B., Li J., Pisespongsa P., Manatsathit S., Aniwan S., Simadibrata M., Abdullah M., Tsang S. W., Wong T. C., Hui A. J., Chow C. M., Yu H. H., Li M. F., Ng K. K., Ching J., Wu J. C., Chan F. K., Sung J. J., Asia-Pacific Crohn’s and Colitis Epidemiology Study ACCESS Group. Environmental risk factors in inflammatory bowel disease: a population-based case-control study in Asia-Pacific. Gut 2015; 64, 1063–1071.

8. Guo A. Y., Stevens B. W., Wilson R. G., Russell C. N., Cohen M. A., Sturgeon H. C., Thornton A., Giallourakis C., Khalili H., Nguyen D. D., Sauk J., Yajnik V., Xavier R. J., Ananthakrishnan A. N. Early life environmental and natural history of inflammatory bowel diseases. BMC Gastroenterol. 2014; 14, 216.

 9. Hviid A., Svanstrom H., Frisch M. Antibiotic use and inflammatory bowel diseases in childhood. Gut 2011; 60, 49–54.  

10. Garcia-Rodriguez L. A., Ruigomez A., Panes J. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology 2006; 130, 1588–1594.

11. Benchimol E. I., Kaplan G. G., Otley A. R., Nguyen G. C., Underwood F. E., Guttmann A., Jones J. L., Potter B. K., Catley C. A., Nugent Z. J., Cui Y., Tanyingoh D., Mojaverian N., Bitton A., Carroll M. W., deBruyn J., Dummer T. J. B., El-Matary W., Griffiths A. M., Jacobson K., Kuenzig M. E., Leddin D., Lix L. M., Mack D. R., Murthy S. K., Sánchez J. N. P., Singh H., Targownik L. E., Vutcovici M., Bernstein C. N. Rural and urban residence during early life is associated with lower risk of inflammatory bowel disease: a population-based inception and birth cohort study. Am. J. Gastroenterol. 2017; 112, 1412–1422.

 12. Ananthakrishnan A. N., Bernstein C. N., Iliopoulos D., Macpherson A., Neurath M. F., Raja Ali R. A., Vavricka S. R., Fiocchi C. Environmental triggers in IBD: a review of progress and evidence. Nat. Rev.  Gastroenterol. Hepatol. 2018; 15, 39–49.    

 13. Kaplan G. G., Hubbard J., Korzenik J., Sands B. E., Panaccione R., Ghosh S., Wheeler A. J., Villeneuve P. J. The inflammatory bowel diseases and ambient air pollution: a novel association. Am. J. Gastroenterol. 2010; 105, 2412–2419.  

14. Opstelten JL Beelen R. M. J., Leenders M., Hoek G., Brunekreef B., van Schaik F. D. M., Siersema P. D., Eriksen K. T., Raaschou-Nielsen O., Tjønneland A., Overvad K., Boutron-Ruault M. C., Carbonnel F., de Hoogh K., Key T. J., Luben R., Chan S. S. M., Hart A. R., Bueno-de-Mesquita H. B., Oldenburg B. Exposure to ambient air pollution and the risk of inflammatory bowel disease: a European nested case-control study. Dig. Dis. Sci. 2016; 61, 2963–2971.

15. Dubeau M. F., Iacucci M., Beck P. L., Moran G. W., Kaplan G. G., Ghosh S., Panaccione R. Drug-induced inflammatory bowel disease and IBD-like conditions. Inflamm. Bowel Dis. 2013; 19, 445–456.

16. Jostins L., Ripke S., Weersma R. K., Duerr R. H., McGovern D. P., Hui K. Y., Lee J. C., Schumm L. P., Sharma Y., Anderson C. A., Essers J., Mitrovic M., Ning K., Cleynen I., Theatre E., Spain S. L., Raychaudhuri S., Goyette P., Wei Z., Abraham C., Achkar J. P., Ahmad T., Amininejad L., Ananthakrishnan A. N., Andersen V., Andrews J. M., Baidoo L., Balschun T., Bampton P. A., Bitton A., Boucher G., Brand S., Büning C., Cohain A., Cichon S., D’Amato M., De Jong D., Devaney K. L., Dubinsky M., Edwards C., Ellinghaus D., Ferguson L. R., Franchimont D., Fransen K., Gearry R., Georges M., Gieger C., Glas J., Haritunians T., Hart A., Hawkey C., Hedl M., Hu X., Karlsen T. H., Kupcinskas L., Kugathasan S., Latiano A., Laukens D., Lawrance I. C., Lees C. W., Louis E., Mahy G., Mansfield J., Morgan A. R., Mowat C., Newman W., Palmieri O., Ponsioen C. Y., Potocnik U., Prescott N. J., Regueiro M., Rotter J. I., Russell R. K., Sanderson J. D., Sans M., Satsangi J., Schreiber S., Simms L. A., Sventoraityte J., Targan S. R., Taylor K. D., Tremelling M., Verspaget H. W., De Vos M., Wijmenga C., Wilson D. C., Winkelmann J., Xavier R. J., Zeiss   ig S., Zhang B., Zhang C. K., Zhao H., International IBD Genetics Consortium (IIBDGC), Silverberg M. S., Annese V         ., Hakonarson H., Brant S. R., Radford-Smith G., Mathew C. G., Rioux J. D., Schadt E. E., Daly M. J., Franke A., Parkes M., Vermeire S., Barrett J. C., Cho J. H. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012; 491, 119–124.

17. Shaw M. H., Kamada N., Warner N., Kim Y. G., Nuñez G. The ever-expanding function of NOD2: autophagy, viral recognition and T cell activation. Trends Immunol. 2011; 32, 73–79.

18. Hugot J. P., Chamaillard M., Zouali H., Lesage S., Cézard J. P., Belaiche J., Almer S., Tysk C., O’Morain C. A., Gassull M., Binder V., Finkel Y., Cortot A., Modigliani R., Laurent-Puig P., Gower-Rousseau C., Macry J., Colombel J. F., Sahbatou M., Thomas G. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature 2001; 411, 599–603.

19. Swidsinski A., Landhoff A., Pernthaler A., Swidsinski S., Loening-Baucke V., Ortner M., Weber J., Hoffmann U., Schreiber S., Dietel M., Lochs H. Mucosal flora in inflammatory bowel disease. Gastroenterology 2002; 122, 44–54.

20. Voss E., Wehkamp J., Wehkamp K., Stange E. F., Schröder J. M., Harder J. NOD2/CARD15 mediates induction of the antimicrobial peptide human betadefensis-2. J. Bio. Chem. 2006; 281, 2005–2011.

21. Noguchi E., Homma Y., Kang X., Netea M. G., Ma X. A Crohn’s disease-associated NOD2 mutation supresses transcription of human IL10 by inhibiting activity of the nucleoprotein hnRNP-A1. Nat. Immunol. 2009; 10, 471–179.

22. Levine B., Mizushima N., Virgin H. Autophagy in immunity and inflammation. Nature 2011; 469, 323–335.

23. Lapaquette P., Bringer M. A., Darfeuille-Michaud A. Defect in autophagy favour adherent-invasive Escherichia coli persistence within macrophages leading to increased pro-inflammatory response. Cell Microbiol. 2012; 14, 791–807.

24. Banerjee A., Gerondakis S. Coordinating TLR-activated signalling pathways in cells of the immune system. Immunol. Cell Biol. 2007; 85, 420–424.

25. Qiu F., Maniar A., Diaz M., Chapoval A. I., Medvedev A. E. Activation of cytokine-producing and antitumor activities of natural killer cells and macrophages by engagement of Toll-like and NOD-like receptors. Innate Immunol. 2011; 17, 375–387.

26. Chassaing B., Darfeuille-Michaud A. The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology 2011; 140, 1720–1728.

27. Ott S. J., Kuchbacher T., Musfeldt M., Rosenstiel P., Hellmig S., Rehman A., Drews O., Weichert W., Timmis K. N., Schreiber S. Fungi and inflammatory bowel diseases: alteration of composition and diversity. Scand. J. Gastroenterol. 2008; 43, 831–841.

28. Walker A. W., Sanderson J. D., Churcher C., Parkes G. C., Hudspith B. N., Rayment N., Brostoff J., Parkhill J., Dougan G., Petrovska L. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the          intestine in            inflammatory bowel disease. BMC Microbiol. 2011; 11, 7.

29. Frank D. N., St. Amand A. L., Feldman R. A., Boedeker E. C., Harpaz N., Pace N. R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007; 104, 13780–13785.

30. Andoh A., Tsujikawa T., Sasaki M., Mitsuyama K., Suzuki Y., Matsui T., Matsumoto T., Benno Y., Fujiyama Y. Faecal microbiota profile of Crohn’s disease determined by terminal restriction fragment length polymorphism analysis. Aliment Pharmacol. Ther. 2009; 29, 75–82.

31. Andoh A, Kuzuoka H, Tsujikawa T Nakamura S., Hirai F., Suzuki Y., Matsui T., Fujiyama Y., Matsumoto T. Multicenter analysis of fecal microbiota profiles in Japanese patients with Crohn’s disease. J. Gastroenterol. 2012; 47, 1298–1307.

32. Seksik P., Rigottier-Gois L., Gramet G., Sutren M., Pochart P., Marteau P., Jian R., Doré J. Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut 2003; 52, 237–242.

33. Willing B. P., Dicksved J., Halfvarson J., Andersson A. F., Lucio M., Zheng Z., Järnerot G., Tysk C., Jansson J. K., Engstrand L. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 2010; 139, 1844–1854.

34. Bull T. J., McMinn E. J., Sidi-Boumedine K., Skull A., Durkin D., Neild P., Rhodes G., Pickup R., Hermon-Taylor J. Detection and verification of Mycobacterium avium subsp. paratuberculosis in fresh ileocolonic mucosal biopsy specimens from individuals with and without Crohn’s disease. J. Clin. Microbiol. 2003; 41, 2915–2923.

35. Nemoto H., Kataoka K., Ishikawa H., Ikata K., Arimochi H., Iwasaki T., Ohnishi Y., Kuwahara T., Yasutomo K. Reduced diversity and imbalance of fecal microbiota in patients with ulcerative colitis. Dig. Dis. Sci. 2012; 57, 2955–2964.

36. Ott S. J., Musfeld M., Wenderoth D. F., Hampe J., Brant O., Fölsch U. R., Timmis K. N., Schreiber S. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 2004; 53, 685–693.

37. Rausch P., Rehman A., Künzel S., Häsler R., Ott S. J., Schreiber S., Rosenstiel P., Franke A., Baines J. F. Colonic mucosa-associated microbiota is influenced by interaction of Crohn disease and FUT2 (Secretor) genotype. Proc. Natl. Acad. Sci. USA 2011; 108, 19030–19035.

37. Bernstein C. N., Shanagan F. Disorders of a modern lifestyle: reconciling the epidemiology of inflammatory bowel disease. Gut 2008; 57, 1185–1191.

39. Lupp C., Robertson M. L., Wickham M. E., Sekirov I., Champion O. L., Gaynor E. C., Finlay B. B. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007; 2, 119–129.

40. Brazil J. C., Louis N. A., Parkos C. A. The role of polymorhponuclear leukocyte trafficking in the perpetuation of inflammation during inflammatory bowel disease. Inflamm. Bowel. Dis. 2013; 19, 1556–1565.

41. Rimoldi M Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 2005; 6, 507–514.

42. Hart A. L. Al-Hassi H. O., Rigby R. J., Bell S. J., Emmanuel A. V., Knight S. C., Kamm M. A., Stagg A. J. Characteristics of intestinal dendritic cells in inflammatory bowel disease. Gastroenterology 2005; 129, 50–65.

43. Scott M. G., Nahm M. H., Macke K., Nash G. S., Bertovich M. J., MacDermott R. P. Spontaneous secretion of IgG subclasses by intestinal mononuclear cell            s: differences between ulcerative colitis, Crohn’s disease and control. Clin. Exp. Immunol. 1986; 66, 209–215.          

44. MacDermott R. P., Nash G. S., Nahm M. H. Antibody secretion by human intestinal mononuclear cells from normal controls and inflammatory bowel disease patients. Immunol. Invest. 1989; 18, 449–457.

45. Takahashi F., Das K. M. Isolation and characterization of a colonic autoantigen specifically recognized by colon tissue-bounded immunoglobulin G from idiopathic ulcerative colitis. J. Clin. Invest. 76; 1985, 311–318.

46. Marineaţă A., Rezus E., Mihai C., Prelipcean C. C. Extra intestinal manifestations and complications in inflammatory bowel disease. Rev. Med. Chir. Soc. Med. Nat. Iasi 2014; 118, 279–288.

47. Halstensen T. S., Das K. M., Brandtzaeg P. Epithelial deposits of immunoglobulin G1 and activated complement colocalise with the Mr 40kD putative autoantigen in ulcerative colitis. Gut 1998; 34, 650–657.

48. Murphy K. M., Stockinger B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat. Immunol. 2010; 11, 674–680.

49. O’Connor W., Zenewicz L. A., Flavell R. A. The dual function of TH17 cells: shifting the focus to function. Nat. Immunol. 2010; 11, 471–476.

50. Weaver C. T., Hatton R. D. Interplay between the TH17 and Treg cell lineages: a (co-)evolutionary perspective. Nat. Rev. Immunol. 2009; 9, 883–889.

51. Harrison O. J., Powrie F. M. Regulatory T cells and immune tolerance in the intestine. Cold Spring. Harb. Perspect. Biol. 2013; 5, a018341.

52. Mayne C. G., Williams C. B. Induced and natural regulatory T cells in the development of inflammatory bowel disease. Inflamm. Bowel Dis. 2013; 19, 1772–1788.

53. Huibregste I. L., van Lent A. U., van Deventer S. J. H. Immunopathogenesis of IBD: insufficient suppressor function in the gut? Gut 2007; 56, 584–592.

54. Takayama T., Kamada N., Chinen H., Okamoto S., Kitazume M. T., Chang J., Matuzaki Y., Suzuki S., Sugita A., Koganei K., Hisamatsu T., Kanai T., Hibi T. Imbalance of NKp44+NKp46– and NKp44–NKp46+ natural killer cells in the intestinal mucosa of patients with Crohn’s disease. Gastroenterology 2010; 139, 882–892, e1–e3.           

 55. Fuss I. J., Joshi B., Yang Z., Degheidy H., Fichtner-Feigl S., de Souza H., Rieder F., Scaldaferri F., Schirbel A., Scarpa M., West G., Yi C., Xu L., Leland P., Yao M., Mannon P., Puri R. K., Fiocchi C., Strober W. IL-13Rα2-bearing, type II NKT cells reactive to sulfatide self-antigen populate the mucosa of ulcerative colitis. Gut 2014; 63, 1728–1736.        

56. Tait Wojno E. D., Artis D. Innate lymphoid cells: balancing immunity, inflammation and tissue repair in the intestine. Cell Host Microbe 2012; 12, 445–457.

57. Goldberg R., Prescott N., Lord G. M., MacDonald T. T., Powell N. The unusual suspects – innate lymphoid cells as novel therapeutic targets in IBD. Nat. Rev. Gastroenterol. Hepatol. 2015; 12, 271–283.

58. Kaser A., Zeissig S., Blumberg R. S. Inflammatory bowel disease. Annu. Rev. Immunol. 2010; 28, 573–621.

59. Kim D. H., Cheon J. H. Pathogenesis of inflammatory bowel disease and recent advances in biologic therapies. Immune Network 2017; 17, 25–40.

60. Kaser A., Blumberg R. S. Endoplasmatic reticulum stress and intestinal inflammation. Mucosal. Immunol. 2010; 3, 11–16.

61. Jass J. R., Walsh M. D. Altered mucin expression in the gastrointestinal tract: a review. J. Cell Mol. Med. 2001; 5, 327–351.

62. Wallace K. L., Zheng L. B., Kanazawa Y., Shih D. Q. Immunopathology of inflammatory bowel disease. Worl. J. Gastroenterol. 2014; 20, 6–21.

63. Sartor R. B. Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat. Clin. Pract. Gastreoetnterol. He  patol. 2006; 3, 390–407.