MicroRNA-146a constrains multiple parameters of intestinal immunity and increases susceptibility to DSS colitis

Oncotarget

Volumn 6, Issue 30, 2015, Pages 28556-28572

  Runtsch, Marah C ^a   Hu, Ruozhen ^a   Alexander, Margaret ^a   Wallace, Jared ^a   Kagele, Dominique ^a   Petersen, Charisse ^a   Valentine, John F ^a   Welker, Noah C ^b   Bronner, Mary P ^b   Chen, Xinjian ^a   Smith, Daniel P ^c   Ajami, Nadim J ^c   Petrosino, Joseph F ^c   Round, June L ^a   O'Connell, Ryan M ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b ARUP LABORATORIES   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Colitis; Intestine; Microbiota; MiR 146a; MiRNA

Indexed keywords

DEXTRAN SULFATE; IMMUNOGLOBULIN A; INDUCIBLE T CELL COSTIMULATOR; MESSENGER RNA; MICRORNA 146A; AUTACOID; MICRORNA; MIRN146 MICRORNA, HUMAN; MIRN146 MICRORNA, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE PREDISPOSITION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC SUSCEPTIBILITY; HOMEOSTASIS; IMMUNE DYSREGULATION; IMMUNOGLOBULIN PRODUCTION; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; INTESTINE MUCOSA PERMEABILITY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PEYER PATCH; PROTEIN EXPRESSION; T LYMPHOCYTE; TH17 CELL; ULCERATIVE COLITIS; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; COLON; DISEASE MODEL; FECAL MICROBIOTA TRANSPLANTATION; GENETIC PREDISPOSITION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTESTINE FLORA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MUCOSAL IMMUNITY; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TIME FACTOR;

ANIMALS; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; FECAL MICROBIOTA TRANSPLANTATION; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; HOST-PATHOGEN INTERACTIONS; IMMUNITY, MUCOSAL; INFLAMMATION MEDIATORS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; PHENOTYPE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TIME FACTORS;

EID: 84945152093     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5597     Document Type: Article

References (88)

1. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9:313-323.
2. Hooper L V, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 2010; 10:159-169.
3. Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol 2014; 16:1024-1033.
4. Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med 2009; 361:2066-2078.
5. Bollrath J, Powrie FM. Controlling the frontier: Regulatory T-cells and intestinal homeostasis. Semin Immunol 2013; 25:352-357.
6. Peterson D a, McNulty NP, Guruge JL, Gordon JI. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2007; 2:328-39.
7. Ahmad S. Antibody responses: IgA-peacemaker in the gut. Nat Rev Immunol 2008; 8:6-7.
8. Kato LM, Kawamoto S, Maruya M, Fagarasan S. Gut TFH and IgA: key players for regulation of bacterial communities and immune homeostasis. Immunol Cell Biol 2014; 92:49-56.
9. Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol 2014; 14:329-42.
10. Shale M, Schiering C, Powrie F. CD4+ T-cell subsets in intestinal inflammation. Immunol Rev 2013; 252:164-182.
11. Maloy KJ, Kullberg MC. IL-23 and Th17 cytokines in intestinal homeostasis. Mucosal Immunol 2008; 1:339-349.
12. Cao AT, Yao S, Gong B, Elson CO, Cong Y. Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis. J Immunol 2012; 189:4666-73.
13. Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014; 14:141-53.
14. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008; 8:411-20.
15. Reynolds JM, Dong C. Toll-like receptor regulation of effector T lymphocyte function. Trends Immunol 2013; 34:511-519.
16. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004; 118:229-41.
17. Frantz AL, Rogier EW, Weber CR, Shen L, Cohen DA, Fenton LA, Bruno ME, Kaetzel CS. Targeted deletion of MyD88 in intestinal epithelial cells results in compromised antibacterial immunity associated with downregulation of polymeric immunoglobulin receptor, mucin-2, and antibacterial peptides. Mucosal Immunol 2012; 5:501-512.
18. Kirkland D, Benson A, Mirpuri J, Pifer R, Hou B, DeFranco AL, Yarovinsky F. B Cell-Intrinsic MyD88 Signaling Prevents the Lethal Dissemination of Commensal Bacteria during Colonic Damage. Immunity 2012; 36:228-238.
19. Atreya I, Atreya R, Neurath MF. NF-kappaB in inflammatory bowel disease. J Intern Med 2008; 263:591-596.
20. O'Connell RM, Rao DS, Baltimore D. microRNA regulation of inflammatory responses. Annu Rev Immunol 2012; 30:295-312.
21. Baltimore D, Boldin MP, O'Connell RM, Rao DS, Taganov KD. MicroRNAs: new regulators of immune cell development and function. Nat Immunol 2008; 9:839-45.
22. O'Connell RM, Rao DS, Chaudhuri A a, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010; 10:111-22.
23. Zhao JL, Rao DS, Boldin MP, Taganov KD, O'Connell RM, Baltimore D. NF-kappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc Natl Acad Sci U S A 2011; 108:9184-9189.
24. Runtsch MC, Round JL, OConnell RM. MicroRNAs and the regulation of intestinal homeostasis. Front Genet 2014; 5:1-10.
25. Chivukula RR, Shi G, Acharya A, Mills EW, Zeitels LR, Anandam JL, Abdelnaby A a, Balch GC, Mansour JC, Yopp AC, Maitra A, Mendell JT. An essential mesenchymal function for miR-143/145 in intestinal epithelial regeneration. Cell 2014; 157:1104-16.
26. Taganov KD, Boldin MP, Chang K-J, Baltimore D. NFkappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006; 103:12481-12486.
27. Boldin MP, Taganov KD, Rao DS, Yang L, Zhao JL, Kalwani M, Garcia-Flores Y, Luong M, Devrekanli A, Xu J, Sun G, Tay J, et al. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 2011; 208:1189-1201.
28. Yang L, Boldin MP, Yu Y, Liu CS, Ea CK, Ramakrishnan P, Taganov KD, Zhao JL, Baltimore D. miR-146a controls the resolution of T cell responses in mice. J Exp Med 2012; 209:1655-1670.
29. Zhao JL, Rao DS, O'Connell RM, Garcia-Flores Y, Baltimore D. MicroRNA-146a acts as a guardian of the quality and longevity of hematopoietic stem cells in mice. Elife 2013; 2:e00537.
30. Chassin C, Hempel C, Stockinger S, Dupont A, Kübler JF, Wedemeyer J, Vandewalle A, Hornef MW. MicroRNA-146a-mediated downregulation of IRAK1 protects mouse and human small intestine against ischemia/reperfusion injury. EMBO Mol Med 2012; 4:1308-19.
31. Lu LF, Boldin MP, Chaudhry A, Lin LL, Taganov KD, Hanada T, Yoshimura A, Baltimore D, Rudensky AY. Function of miR-146a in Controlling Treg Cell-Mediated Regulation of Th1 Responses. Cell 2010; 142:914-929.
32. Pratama A, Srivastava M, Williams NJ, Papa I, Lee SK, Dinh XT, Hutloff A, Jordan M a., Zhao JL, Casellas R, Athanasopoulos V, Vinuesa CG. MicroRNA-146a regulates ICOS-ICOSL signalling to limit accumulation of T follicular helper cells and germinal centres. Nat Commun 2015; 6:6436.
33. Lochhead RB, Ma Y, Zachary JF, Baltimore D, Zhao JL, Weis JH, O'Connell RM, Weis JJ. MicroRNA-146a Provides Feedback Regulation of Lyme Arthritis but Not Carditis during Infection with Borrelia burgdorferi. PLoS Pathog 2014; 10.
34. Chassin C, Kocur M, Pott J, Duerr CU, Gütle D, Lotz M, Hornef MW. MiR-146a mediates protective innate immune tolerance in the neonate intestine. Cell Host Microbe 2010; 8:358-368.
35. Ghorpade DS, Sinha AY, Holla S, Singh V, Balaji KN. NOD2-nitric oxide-responsive microRNA-146a activates Sonic hedgehog signaling to orchestrate inflammatory responses in murine model of inflammatory bowel disease. J Biol Chem 2013; 288:33037-33048.
36. Rusca N, Monticelli S. MiR-146a in Immunity and Disease. Mol Biol Int 2011; 2011:437301.
37. Cash HL, Whitham C V, Behrendt CL, Hooper L V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006; 313:1126-1130.
38. Brandl K, Plitas G, Schnabl B, DeMatteo RP, Pamer EG. MyD88-mediated signals induce the bactericidal lectin RegIII gamma and protect mice against intestinal Listeria monocytogenes infection. J Exp Med 2007; 204:1891-1900.
39. Kolls JK, McCray PB, Chan YR. Cytokine-mediated regulation of antimicrobial proteins. Nat Rev Immunol 2008; 8:829-835.
40. Vaishnava S, Yamamoto M, Severson KM, Ruhn K a, Yu X, Koren O, Ley R, Wakeland EK, Hooper L V. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 2011; 334:255-8.
41. Uhlar CM, Whitehead AS. Serum amyloid A, the major vertebrate acute-phase reactant. Eur J Biochem 1999; 265:501-523.
42. Eckhardt ERM, Witta J, Zhong J, Arsenescu R, Arsenescu V, Wang Y, Ghoshal S, de Beer MC, de Beer FC, de Villiers WJS. Intestinal epithelial serum amyloid A modulates bacterial growth in vitro and pro-inflammatory responses in mouse experimental colitis. BMC Gastroenterol 2010; 10:133.
43. Kim YS, Ho SB. Intestinal goblet cells and mucins in health and disease: Recent insights and progress. Curr Gastroenterol Rep 2010; 12:319-330.
44. Cho H, Kelsall BL. The role of type I interferons in intestinal infection, homeostasis, and inflammation. Immunol Rev 2014; 260:145-167.
45. Katakura K, Lee J, Rachmilewitz D, Li G, Eckmann L, Raz E. Toll-like receptor 9-induced type I IFN protects mice from experimental colitis. J Clin Invest 2005; 115:695-702.
46. Long TM, Nisa S, Donnenberg MS, Hassel BA. Enteropathogenic Escherichia coli inhibits type I interferonand RNase L-mediated host defense to disrupt intestinal epithelial cell Barrier function. Infect Immun 2014; 82:2802-2814.
47. Roda G, Dahan S, Mezzanotte L, Caponi A, Roth-Walter F, Pinn D, Mayer L. Defect in CEACAM family member expression in Crohn's disease IECS is regulated by the transcription factor SOX9. Inflamm Bowel Dis 2009; 15:1775-1783.
48. Chen L, Chen Z, Baker K, Halvorsen EM, Pires da Cunha A, Flak MB, Gerber G, Huang YH, Hosomi S, Arthur JC, Dery KJ, Nagaishi T, et al. The Short Isoform of the CEACAM1 Receptor in Intestinal T Cells Regulates Mucosal Immunity and Homeostasis via Tfh Cell Induction. Immunity 2012; 37:930-946.
49. Lei Z, Maeda T, Tamura A, Nakamura T, Yamazaki Y, Shiratori H, Yashiro K, Tsukita S, Hamada H. EpCAM contributes to formation of functional tight junction in the intestinal epithelium by recruiting claudin proteins. Dev Biol 2012; 371:136-145.
50. Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 2011; 141:769-776.
51. Siegmund B. Interleukin-18 in Intestinal Inflammation: Friend and Foe? Immunity 2010; 32:300-302.
52. Zaki MH, Boyd KL, Vogel P, Kastan MB, Lamkanfi M, Kanneganti TD. The NLRP3 Inflammasome Protects against Loss of Epithelial Integrity and Mortality during Experimental Colitis. Immunity 2010; 32:379-391.
53. Ciorba MA, Bettonville EE, McDonald KG, Metz R, Prendergast GC, Newberry RD, Stenson WF. Induction of IDO-1 by immunostimulatory DNA limits severity of experimental colitis. J Immunol 2010; 184:3907-3916.
54. Brandl K, Sun L, Neppl C, Siggs OM, Le Gall SM, Tomisato W, Li X, Du X, Maennel DN, Blobel CP, Beutler B. MyD88 signaling in nonhematopoietic cells protects mice against induced colitis by regulating specific EGF receptor ligands. Proc Natl Acad Sci U S A 2010; 107:19967-19972.
55. Kubinak JL, Petersen C, Stephens WZ, Soto R, Bake E, O'Connell RM, Round JL. MyD88 Signaling in T Cells Directs IgA-Mediated Control of the Microbiota to Promote Health. Cell Host Microbe 2015; 17:153-163.
56. Hu R, Kagele DA, Huffaker TB, Runtsch MC, Alexander M, Liu J, Bake E, Su W, Williams MA, Rao DS, Möller T, Garden GA, et al. miR-155 Promotes T Follicular Helper Cell Accumulation during Chronic, Low-Grade Inflammation. Immunity 2014; 41:605-619.
57. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol 2011; 29:621-663.
58. Choi YS, Kageyama R, Eto D, Escobar TC, Johnston RJ, Monticelli L, Lao C, Crotty S. ICOS Receptor Instructs T Follicular Helper Cell versus Effector Cell Differentiation via Induction of the Transcriptional Repressor Bcl6. Immunity 2011; 34:932-946.
59. Pabst O. New concepts in the generation and functions of IgA. Nat Rev Immunol 2012.
60. Wei M, Shinkura R, Doi Y, Maruya M, Fagarasan S, Honjo T. Mice carrying a knock-in mutation of Aicda resulting in a defect in somatic hypermutation have impaired gut homeostasis and compromised mucosal defense. Nat Immunol 2011; 12:264-270.
61. Barone F, Vossenkamper A, Boursier L, Su W, Watson A, John S, Dunn-Walters DK, Fields P, Wijetilleka S, Edgeworth JD, Spencer J. IgA-producing plasma cells originate from germinal centers that are induced by B-cell receptor engagement in humans. Gastroenterology 2011; 140:947-956.
62. Yazbeck R, Howarth GS, Butler RN, Geier MS, Abbott CA. Biochemical and histological changes in the small intestine of mice with dextran sulfate sodium colitis. J Cell Physiol 2011; 226:3219-3224.
63. Rose WA, Sakamoto K, Leifer CA. Multifunctional role of dextran sulfate sodium for in vivo modeling of intestinal diseases. BMC Immunol 2012; 13:41.
64. Okayasu I, Hatakeyama S, Yamada M. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990; 98:694-702.
65. Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1977; 31:107-133.
66. Gazouli M, Papaconstantinou I, Stamatis K, Vaiopoulou A, Zeglinas C, Vassiliou I, Giokas G, Tzathas C. Association Study of Genetic Variants in miRNAs in Patients with Inflammatory Bowel Disease: Preliminary Results. Dig Dis Sci 2013; 58:2324-8.
67. Lin J, Welker NC, Zhao Z, Li Y, Zhang J, Reuss S a, Zhang X, Lee H, Liu Y, Bronner MP. Novel specific microRNA biomarkers in idiopathic inflammatory bowel disease unrelated to disease activity. Mod Pathol 2014; 27:602-8.
68. Schaefer JS, Attumi T, Opekun AR, Abraham B, Hou J, Shelby H, Graham DY, Streckfus C, Klein JR. MicroRNA signatures differentiate Crohn's disease from ulcerative colitis. BMC Immunol 2015; 16:1-13.
69. Yang L, Boldin MP, Yu Y, Liu CS, Ea C-K, Ramakrishnan P, Taganov KD, Zhao JL, Baltimore D. miR-146a controls the resolution of T cell responses in mice. J Exp Med 2012; 209:1655-1670.
70. Moncada DM, Kammanadiminti SJ, Chadee K. Mucin and Toll-like receptors in host defense against intestinal parasites. Trends Parasitol 2003; 19:305-311.
71. Kamada N, Seo S-U, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013; 13:321-35.
72. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444:1027-31.
73. Kemppainen KM, Ardissone AN, Davis-Richardson AG, Fagen JR, Gano KA, León-Novelo LG, Vehik K, Casella G, Simell O, Ziegler AG, Rewers MJ, Lernmark Å, et al. Early Childhood Gut Microbiomes Show Strong Geographic Differences Among Subjects at High Risk for Type 1 Diabetes: Figure1. Diabetes Care 2015; 38:329-332.
74. Giongo A, Gano KA, Crabb DB, Mukherjee N, Novelo LL, Casella G, Drew JC, Ilonen J, Knip M, Hyöty H, Veijola R, Simell T, et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J 2011; 5:82-91.
75. Cantarel BL, Waubant E, Chehoud C, Kuczynski J, Desantis TZ, Warrington J, Venkatesan A, Fraser CM., Mowry EM. Gut Microbiota in Multiple Sclerosis: Possible Influence of Immunomodulators. J Investig Med 2015; 63:1-6.
76. Schubert AM, Rogers MAM, Ring C, Mogle J, Petrosino JP, Young VB, Aronoff DM, Schloss PD. Microbiome Data Distinguish Patients with Clostridium difficile Infection and Non-C. difficile-Associated Diarrhea from Healthy. MBio 2014; 5:1-9.
77. Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH. Communicable Ulcerative Colitis Induced by T-bet Deficiency in the Innate Immune System. Cell 2007; 131:33-45.
78. Saulnier DM, Riehle K, Mistretta T-A, Diaz M-A, Mandal D, Raza S, Weidler EM, Qin X, Coarfa C, Milosavljevic A, Petrosino JF, Highlander S, et al. Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology 2011; 141:1782-91.
79. Caporaso JG, Lauber CL, Walters W a, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J a, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012; 6:1621-1624.
80. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013; 10:996-8.
81. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: Improved data processing and webbased tools. Nucleic Acids Res 2013; 41:590-596.
82. Chao A, Chazdon RL, Colwell RK, Shen TJ. Abundancebased similarity indices and their estimation when there are unseen species in samples. Biometrics 2006; 62:361-371.
83. Shannon CE. A mathematical theory of communication. Bell Syst Tech J 1948; 27:379-423.
84. Lozupone C, Hamady M, Knight R. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 2006; 7:371.
85. R Development Core Team R. R: A Language and Environment for Statistical Computing. R Found Stat Comput 2014; 1:409.
86. McMurdie PJ, Holmes S. Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS One 2013; 8.
87. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley G a, Kelley ST, et al. correspondence QIIME allows analysis of high-throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr 2010; 7:335-336.
88. Viennois E, Chen F, Laroui H, Baker MT, Merlin D. Dextran sodium sulfate inhibits the activities of both polymerase and reverse transcriptase: lithium chloride purification, a rapid and efficient technique to purify RNA. BMC Res Notes 2013; 6:360.