Genetic and epigenetic underpinnings of eosinophilic esophagitis

Gastroenterology Clinics of North America

Volumn 43, Issue 2, 2014, Pages 269-280

  Sherrill, Joseph D ^a   Rothenberg, Marc E ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Eotaxin 3; Epigenetics; Genetic variant; MicroRNA; Thymic stromal lymphopoietin

Indexed keywords

DESMOGLEIN 1; DNA; EOTAXIN 3; HISTONE; MICRORNA; STEROID; TRANSCRIPTION FACTOR RUNX2;

DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EOSINOPHILIC ESOPHAGITIS; EPIGENETICS; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HISTONE MODIFICATION; HUMAN; MOLECULAR GENETICS; MOLECULAR PATHOLOGY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTOMICS; GENETIC EPIGENESIS; GENETICS;

EOSINOPHILIC ESOPHAGITIS; EPIGENESIS, GENETIC; HUMANS;

EID: 84899956835     PISSN: 08898553     EISSN: 15581942     Source Type: Journal    
DOI: 10.1016/j.gtc.2014.02.003     Document Type: Review

References (62)

1. Sherrill J.D., Rothenberg M.E. Genetic dissection of eosinophilic esophagitis provides insight into disease pathogenesis and treatment strategies. J Allergy Clin Immunol 2011, 128:23-32.
2. Blanchard C., Wang N., Rothenberg M.E. Eosinophilic esophagitis: pathogenesis, genetics, and therapy. J Allergy Clin Immunol 2006, 118:1054-1059.
3. Lu T.X., Sherrill J.D., Wen T., et al. MicroRNA signature in patients with eosinophilic esophagitis, reversibility with glucocorticoids, and assessment as disease biomarkers. J Allergy Clin Immunol 2012, 129:1064-1075.e1069.
4. Blanchard C., Wang N., Stringer K.F., et al. Eotaxin-3 and a uniquely conserved gene-expression profile in eosinophilic esophagitis. J Clin Invest 2006, 116:536-547.
5. Bochner B.S., Book W., Busse W.W., et al. Workshop report from the National Institutes of Health Taskforce on the Research Needs of Eosinophil-Associated Diseases (TREAD). J Allergy Clin Immunol 2012, 130:587-596.
6. Kagalwalla A.F., Shah A., Li B.U., et al. Identification of specific foods responsible for inflammation in children with eosinophilic esophagitis successfully treated with empiric elimination diet. J Pediatr Gastroenterol Nutr 2011, 53:145-149.
7. Jensen E.T., Kappelman M.D., Kim H., et al. Early life exposures as risk factors for pediatric eosinophilic esophagitis. J Pediatr Gastroenterol Nutr 2013, 57:67-71.
8. Almansa C., Krishna M., Buchner A.M., et al. Seasonal distribution in newly diagnosed cases of eosinophilic esophagitis in adults. Am J Gastroenterol 2009, 104:828-833.
9. Spergel J.M., Book W.M., Mays E., et al. Variation in prevalence, diagnostic criteria, and initial management options for eosinophilic gastrointestinal diseases in the United States. J Pediatr Gastroenterol Nutr 2011, 52:300-306.
10. Hurrell J.M., Genta R.M., Dellon E.S. Prevalence of esophageal eosinophilia varies by climate zone in the United States. Am J Gastroenterol 2012, 107:698-706.
11. Dellon E.S., Peery A.F., Shaheen N.J., et al. Inverse association of esophageal eosinophilia with Helicobacter pylori based on analysis of a US pathology database. Gastroenterology 2011, 141:1586-1592.
12. Rayapudi M., Mavi P., Zhu X., et al. Indoor insect allergens are potent inducers of experimental eosinophilic esophagitis in mice. J Leukoc Biol 2010, 88:337-346.
13. Pope S.M., Fulkerson P.C., Blanchard C., et al. Identification of a cooperative mechanism involving interleukin-13 and eotaxin-2 in experimental allergic lung inflammation. J Biol Chem 2005, 280:13952-13961.
14. Noti M., Wojno E.D., Kim B.S., et al. Thymic stromal lymphopoietin-elicited basophil responses promote eosinophilic esophagitis. Nat Med 2013, 19:1005-1013.
15. The International HapMap Project. Nature 2003, 426:789-796. International HapMap Consortium.
16. Blanchard C., Stucke E.M., Burwinkel K., et al. Coordinate interaction between IL-13 and epithelial differentiation cluster genes in eosinophilic esophagitis. J Immunol 2010, 184:4033-4041.
17. Aceves S.S., Newbury R.O., Chen D., et al. Resolution of remodeling in eosinophilic esophagitis correlates with epithelial response to topical corticosteroids. Allergy 2010, 65:109-116.
18. Abonia J.P., Wen T., Stucke E.M., et al. High prevalence of eosinophilic esophagitis in patients with inherited connective tissue disorders. J Allergy Clin Immunol 2013, 132:378-386.
19. Frischmeyer-Guerrerio P.A., Guerrerio A.L., Oswald G., et al. TGFbeta receptor mutations impose a strong predisposition for human allergic disease. Sci Transl Med 2013, 5:195ra194.
20. Rothenberg M.E., Spergel J.M., Sherrill J.D., et al. Common variants at 5q22 associate with pediatric eosinophilic esophagitis. Nat Genet 2010, 42:289-291.
21. Ziegler S.F. The role of thymic stromal lymphopoietin (TSLP) in allergic disorders. Curr Opin Immunol 2010, 22:795-799.
22. Siracusa M.C., Saenz S.A., Tait Wojno E.D., et al. Thymic stromal lymphopoietin-mediated extramedullary hematopoiesis promotes allergic inflammation. Immunity 2013, 39:1158-1170.
23. Sherrill J.D., Gao P.S., Stucke E.M., et al. Variants of thymic stromal lymphopoietin and its receptor associate with eosinophilic esophagitis. J Allergy Clin Immunol 2010, 126:160-165.e163.
24. Gudbjartsson D.F., Bjornsdottir U.S., Halapi E., et al. Sequence variants affecting eosinophil numbers associate with asthma and myocardial infarction. Nat Genet 2009, 41:342-347.
25. Collins M.H., Blanchard C., Abonia J.P., et al. Clinical, pathologic, and molecular characterization of familial eosinophilic esophagitis compared with sporadic cases. Clin Gastroenterol Hepatol 2008, 6:621-629.
26. Wen T., Stucke E.M., Grotjan T.M., et al. Molecular diagnosis of eosinophilic esophagitis by gene expression profiling. Gastroenterology 2013, 145:1289-1299.
27. Blanchard C., Mingler M.K., Vicario M., et al. IL-13 involvement in eosinophilic esophagitis: transcriptome analysis and reversibility with glucocorticoids. J Allergy Clin Immunol 2007, 120:1292-1300.
28. Lucendo A.J., De Rezende L., Comas C., et al. Treatment with topical steroids downregulates IL-5, eotaxin-1/CCL11, and eotaxin-3/CCL26 gene expression in eosinophilic esophagitis. Am J Gastroenterol 2008, 103:2184-2193.
29. Bhattacharya B., Carlsten J., Sabo E., et al. Increased expression of eotaxin-3 distinguishes between eosinophilic esophagitis and gastroesophageal reflux disease. Hum Pathol 2007, 38:1744-1753.
30. Blanchard C., Durual S., Estienne M., et al. Eotaxin-3/CCL26 gene expression in intestinal epithelial cells is up-regulated by interleukin-4 and interleukin-13 via the signal transducer and activator of transcription 6. Int J Biochem Cell Biol 2005, 37:2559-2573.
31. Hoeck J., Woisetschlager M. Activation of eotaxin-3/CCLl26 gene expression in human dermal fibroblasts is mediated by STAT6. J Immunol 2001, 167:3216-3222.
32. Goenka S., Boothby M. Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. Proc Natl Acad Sci U S A 2006, 103:4210-4215.
33. Krishnamurthy P., Sherrill J.D., Parashette K., et al. Correlation of increased PARP14 and CCL26 expression in biopsies from children with eosinophilic esophagitis. J Allergy Clin Immunol 2014, 133:577-580.
34. Mishra A., Hogan S.P., Brandt E.B., et al. An etiological role for aeroallergens and eosinophils in experimental esophagitis. J Clin Invest 2001, 107:83-90.
35. Mishra A., Rothenberg M.E. Intratracheal IL-13 induces eosinophilic esophagitis by an IL-5, eotaxin-1, and STAT6-dependent mechanism. Gastroenterology 2003, 125:1419-1427.
36. Kudo A. Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 2011, 68:3201-3207.
37. Masuoka M., Shiraishi H., Ohta S., et al. Periostin promotes chronic allergic inflammation in response to Th2 cytokines. J Clin Invest 2012, 122:2590-2600.
38. Jia G., Erickson R.W., Choy D.F., et al. Periostin is a systemic biomarker of eosinophilic airway inflammation in asthmatic patients. J Allergy Clin Immunol 2012, 130:647-654.e610.
39. Wong G.S., Lee J.S., Park Y.Y., et al. Periostin cooperates with mutant p53 to mediate invasion through the induction of STAT1 signaling in the esophageal tumor microenvironment. Oncogenesis 2013, 2:e59.
40. Blanchard C., Mingler M.K., McBride M., et al. Periostin facilitates eosinophil tissue infiltration in allergic lung and esophageal responses. Mucosal Immunol 2008, 1:289-296.
41. Corren J., Lemanske R.F., Hanania N.A., et al. Lebrikizumab treatment in adults with asthma. N Engl J Med 2011, 365:1088-1098.
42. Hanania N.A., Wenzel S., Rosen K., et al. Exploring the effects of omalizumab in allergic asthma: an analysis of biomarkers in the EXTRA study. Am J Respir Crit Care Med 2013, 187:804-811.
43. Chavanas S., Bodemer C., Rochat A., et al. Mutations in SPINK5, encoding a serine protease inhibitor, cause Netherton syndrome. Nat Genet 2000, 25:141-142.
44. Amagai M., Matsuyoshi N., Wang Z.H., et al. Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nat Med 2000, 6:1275-1277.
45. Sherrill J.D., Kc K., Wu D., et al. Desmoglein-1 regulates esophageal epithelial barrier function and immune responses in eosinophilic esophagitis. Mucosal Immunol 2013, [Epub ahead of print].
46. Samuelov L., Sarig O., Harmon R.M., et al. Desmoglein 1 deficiency results in severe dermatitis, multiple allergies and metabolic wasting. Nat Genet 2013, 45:1244-1248.
47. Bonasio R., Tu S., Reinberg D. Molecular signals of epigenetic states. Science 2010, 330:612-616.
48. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
49. Bernstein B.E., Kamal M., Lindblad-Toh K., et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005, 120:169-181.
50. Lim E.J., Lu T.X., Blanchard C., et al. Epigenetic regulation of the IL-13-induced human eotaxin-3 gene by CREB-binding protein-mediated histone 3 acetylation. J Biol Chem 2011, 286:13193-13204.
51. Zhang X., Cheng E., Huo X., et al. Omeprazole blocks STAT6 binding to the eotaxin-3 promoter in eosinophilic esophagitis cells. PLoS One 2012, 7:e50037.
52. Dohil R., Newbury R.O., Aceves S. Transient PPI responsive esophageal eosinophilia may be a clinical sub-phenotype of pediatric eosinophilic esophagitis. Dig Dis Sci 2012, 57:1413-1419.
53. Jones P.A. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012, 13:484-492.
54. Lim E., Rothenberg M.E. Demethylation of the human Eotaxin-3 gene promoter leads to the elevated expression of Eotaxin-3. J Immunol 2014, 192(1):466-474.
55. Behm-Ansmant I., Rehwinkel J., Izaurralde E. MicroRNAs silence gene expression by repressing protein expression and/or by promoting mRNA decay. Cold Spring Harb Symp Quant Biol 2006, 71:523-530.
56. Lu T.X., Munitz A., Rothenberg M.E. MicroRNA-21 is up-regulated in allergic airway inflammation and regulates IL-12p35 expression. J Immunol 2009, 182:4994-5002.
57. Lu T.X., Lim E.J., Itskovich S., et al. Targeted ablation of miR-21 decreases murine eosinophil progenitor cell growth. PLoS One 2013, 8:e59397.
58. Lu T.X., Lim E.J., Besse J.A., et al. MiR-223 deficiency increases eosinophil progenitor proliferation. J Immunol 2013, 190:1576-1582.
59. Lu T.X., Lim E.J., Wen T., et al. MiR-375 is downregulated in epithelial cells after IL-13 stimulation and regulates an IL-13-induced epithelial transcriptome. Mucosal Immunol 2012, 5:388-396.
60. Biton M., Levin A., Slyper M., et al. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol 2011, 12:239-246.
61. Lu S., Mukkada V.A., Mangray S., et al. MicroRNA profiling in mucosal biopsies of eosinophilic esophagitis patients pre and post treatment with steroids and relationship with mRNA targets. PLoS One 2012, 7:e40676.
62. Henderson C.J., Ngeow J., Collins M.H., et al. Increased prevalence of eosinophilic gastrointestinal disorders (EGID) in pediatric PTEN hamartoma tumor syndromes (PHTS). J Pediatr Gastroenterol Nutr 2013, [Epub ahead of print].