#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

An explorative study identifies miRNA signatures for the diagnosis of non-celiac wheat sensitivity


Autoři: Emanuela Clemente aff001;  Konstantinos Efthymakis aff002;  Erminia Carletti aff001;  Vanessa Capone aff001;  Samantha Sperduti aff001;  Giuseppina Bologna aff002;  Marco Marchisio aff002;  Marta Di Nicola aff001;  Matteo Neri aff002;  Michele Sallese aff001
Působiště autorů: Department of Medical, Oral and Biotechnological Sciences, “G. d'Annunzio” University of Chieti–Pescara, Chieti, Italy aff001;  Centre for Advanced Studies and Technology (CAST), “G. d'Annunzio” University of Chieti-Pescara, Chieti, Italy aff002;  Department of Medicine and Ageing Sciences, “G. d'Annunzio” University of Chieti–Pescara, Chieti, Italy aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226478

Souhrn

Non-celiac wheat sensitivity (NCWS), also referred to as non-celiac gluten sensitivity, is a recently described disorder triggered by wheat/gluten ingestion. NCWS elicits a wide range of symptoms including diarrhoea, intestinal discomfort, and fatigue in analogy with other wheat/gluten-related disorders and celiac disease in particular. From the pathological standpoint, NCWS patients only have a slight increase of intraepithelial lymphocytes, while antibodies to tissue transglutaminase (tTG) and villous atrophy, otherwise diagnostic features of celiac disease, are absent. To date, the diagnosis of NCWS relies on symptoms and exclusion of confounding diseases, since biomarkers are not yet available. Here, the expression levels of selected miRNAs were examined in duodenal biopsies and peripheral blood leukocytes collected from newly diagnosed patients with NCWS and, as controls, from patients with celiac disease and gluten-independent gastrointestinal problems. We identified a few miRNAs whose expression is higher in the intestinal mucosa of patients affected by NCWS in comparison to control patients affect by gluten-independent dyspeptic symptoms (Helicobacter pylori-negative) and celiac disease. The present study provided the first evidence that NCWS patients have a characteristic miRNA expression patterns, such peculiarity could be exploited as a biomarker to the diagnosis of this disease.

Klíčová slova:

Principal component analysis – Wheat – Diet – Gastrointestinal tract – MicroRNAs – RNA extraction – Biopsy – Gluten


Zdroje

1. Skodje GI, Sarna VK, Minelle IH, Rolfsen KL, Muir JG, Gibson PR, et al. Fructan, Rather Than Gluten, Induces Symptoms in Patients With Self-Reported Non-Celiac Gluten Sensitivity. Gastroenterology. 2018;154(3):529–39 e2. doi: 10.1053/j.gastro.2017.10.040 29102613.

2. Caminero A, McCarville JL, Zevallos VF, Pigrau M, Yu XB, Jury J, et al. Lactobacilli Degrade Wheat Amylase Trypsin Inhibitors to Reduce Intestinal Dysfunction Induced by Immunogenic Wheat Proteins. Gastroenterology. 2019;156(8):2266–80. doi: 10.1053/j.gastro.2019.02.028 30802444.

3. Carroccio A, Mansueto P, Iacono G, Soresi M, D'Alcamo A, Cavataio F, et al. Non-celiac wheat sensitivity diagnosed by double-blind placebo-controlled challenge: exploring a new clinical entity. Am J Gastroenterol. 2012;107(12):1898–906; quiz 907. doi: 10.1038/ajg.2012.236 22825366.

4. Hujoel IA, Reilly NR, Rubio-Tapia A. Celiac Disease: Clinical Features and Diagnosis. Gastroenterol Clin North Am. 2019;48(1):19–37. doi: 10.1016/j.gtc.2018.09.001 30711209.

5. Lundin KE, Alaedini A. Non-celiac gluten sensitivity. Gastrointest Endosc Clin N Am. 2012;22(4):723–34. Epub 2012/10/23. doi: 10.1016/j.giec.2012.07.006 23083989.

6. Sapone A, Bai JC, Ciacci C, Dolinsek J, Green PH, Hadjivassiliou M, et al. Spectrum of gluten-related disorders: consensus on new nomenclature and classification. BMC Med. 2012;10:13. Epub 2012/02/09. doi: 10.1186/1741-7015-10-13 22313950; PubMed Central PMCID: PMC3292448.

7. Schuppan D, Junker Y, Barisani D. Celiac disease: from pathogenesis to novel therapies. Gastroenterology. 2009;137(6):1912–33. Epub 2009/09/22. doi: 10.1053/j.gastro.2009.09.008 19766641.

8. Patel N, Samant H. Wheat Allergy. StatPearls. Treasure Island (FL)2019.

9. Lionetti E, Catassi C. New clues in celiac disease epidemiology, pathogenesis, clinical manifestations, and treatment. Int Rev Immunol. 2011;30(4):219–31. Epub 2011/07/27. doi: 10.3109/08830185.2011.602443 21787227.

10. Green PH, Cellier C. Celiac disease. N Engl J Med. 2007;357(17):1731–43. Epub 2007/10/26. doi: 10.1056/NEJMra071600 17960014.

11. Louka AS, Sollid LM. HLA in coeliac disease: unravelling the complex genetics of a complex disorder. Tissue Antigens. 2003;61(2):105–17. doi: 10.1034/j.1399-0039.2003.00017.x 12694579.

12. Ferguson A, MacDonald TT, McClure JP, Holden RJ. Cell-mediated immunity to gliadin within the small-intestinal mucosa in coeliac disease. Lancet. 1975;1(7912):895–7. doi: 10.1016/s0140-6736(75)91689-x PubMed PMID: 47539.

13. Marsh MN. Grains of truth: evolutionary changes in small intestinal mucosa in response to environmental antigen challenge. Gut. 1990;31(1):111–4. doi: 10.1136/gut.31.1.111 2180789; PubMed Central PMCID: PMC1378351.

14. Oberhuber G, Granditsch G, Vogelsang H. The histopathology of coeliac disease: time for a standardized report scheme for pathologists. Eur J Gastroenterol Hepatol. 1999;11(10):1185–94. Epub 1999/10/19. doi: 10.1097/00042737-199910000-00019 10524652.

15. Corazza GR, Villanacci V. Coeliac disease. J Clin Pathol. 2005;58(6):573–4. doi: 10.1136/jcp.2004.023978 15917404; PubMed Central PMCID: PMC1770677.

16. Bai JC, Fried M, Corazza GR, Schuppan D, Farthing M, Catassi C, et al. World Gastroenterology Organisation global guidelines on celiac disease. J Clin Gastroenterol. 2013;47(2):121–6. Epub 2013/01/15. doi: 10.1097/MCG.0b013e31827a6f83 23314668.

17. Catassi C, Elli L, Bonaz B, Bouma G, Carroccio A, Castillejo G, et al. Diagnosis of Non-Celiac Gluten Sensitivity (NCGS): The Salerno Experts' Criteria. Nutrients. 2015;7(6):4966–77. doi: 10.3390/nu7064966 26096570; PubMed Central PMCID: PMC4488826.

18. Uhde M, Ajamian M, Caio G, De Giorgio R, Indart A, Green PH, et al. Intestinal cell damage and systemic immune activation in individuals reporting sensitivity to wheat in the absence of coeliac disease. Gut. 2016;65(12):1930–7. doi: 10.1136/gutjnl-2016-311964 27459152; PubMed Central PMCID: PMC5136710.

19. Sapone A, Lammers KM, Casolaro V, Cammarota M, Giuliano MT, De Rosa M, et al. Divergence of gut permeability and mucosal immune gene expression in two gluten-associated conditions: celiac disease and gluten sensitivity. BMC Med. 2011;9:23. Epub 2011/03/12. doi: 10.1186/1741-7015-9-23 21392369; PubMed Central PMCID: PMC3065425.

20. DiGiacomo DV, Tennyson CA, Green PH, Demmer RT. Prevalence of gluten-free diet adherence among individuals without celiac disease in the USA: results from the Continuous National Health and Nutrition Examination Survey 2009–2010. Scand J Gastroenterol. 2013;48(8):921–5. doi: 10.3109/00365521.2013.809598 23834276.

21. Volta U, Bardella MT, Calabro A, Troncone R, Corazza GR, Study Group for Non-Celiac Gluten S. An Italian prospective multicenter survey on patients suspected of having non-celiac gluten sensitivity. BMC Med. 2014;12:85. doi: 10.1186/1741-7015-12-85 24885375; PubMed Central PMCID: PMC4053283.

22. Bragde H, Jansson U, Jarlsfelt I, Soderman J. Gene expression profiling of duodenal biopsies discriminates celiac disease mucosa from normal mucosa. Pediatr Res. 2011;69(6):530–7. Epub 2011/03/08. doi: 10.1203/PDR.0b013e318217ecec 21378598.

23. Volinia S, Croce CM. Prognostic microRNA/mRNA signature from the integrated analysis of patients with invasive breast cancer. Proc Natl Acad Sci U S A. 2013;110(18):7413–7. Epub 2013/04/17. doi: 10.1073/pnas.1304977110 23589849; PubMed Central PMCID: PMC3645522.

24. Pauley KM, Cha S, Chan EK. MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun. 2009;32(3–4):189–94. Epub 2009/03/24. doi: 10.1016/j.jaut.2009.02.012 19303254; PubMed Central PMCID: PMC2717629.

25. Capuano M, Iaffaldano L, Tinto N, Montanaro D, Capobianco V, Izzo V, et al. MicroRNA-449a overexpression, reduced NOTCH1 signals and scarce goblet cells characterize the small intestine of celiac patients. PLoS One. 2011;6(12):e29094. Epub 2011/12/24. doi: 10.1371/journal.pone.0029094 22194996; PubMed Central PMCID: PMC3240641.

26. Vidigal JA, Ventura A. The biological functions of miRNAs: lessons from in vivo studies. Trends Cell Biol. 2015;25(3):137–47. doi: 10.1016/j.tcb.2014.11.004 25484347; PubMed Central PMCID: PMC4344861.

27. Shukla GC, Singh J, Barik S. MicroRNAs: Processing, Maturation, Target Recognition and Regulatory Functions. Mol Cell Pharmacol. 2011;3(3):83–92. 22468167; PubMed Central PMCID: PMC3315687.

28. Vaira V, Roncoroni L, Barisani D, Gaudioso G, Bosari S, Bulfamante G, et al. microRNA profiles in coeliac patients distinguish different clinical phenotypes and are modulated by gliadin peptides in primary duodenal fibroblasts. Clin Sci (Lond). 2014;126(6):417–23. doi: 10.1042/CS20130248 24063611.

29. Felli C, Baldassarre A, Masotti A. Intestinal and Circulating MicroRNAs in Coeliac Disease. Int J Mol Sci. 2017;18(9). doi: 10.3390/ijms18091907 28878141; PubMed Central PMCID: PMC5618556.

30. Magni S, Buoli Comani G, Elli L, Vanessi S, Ballarini E, Nicolini G, et al. miRNAs affect the expression of innate and adaptive immunity proteins in celiac disease. Am J Gastroenterol. 2014;109(10):1662–74. doi: 10.1038/ajg.2014.203 25070052.

31. Catassi C, Bai JC, Bonaz B, Bouma G, Calabro A, Carroccio A, et al. Non-Celiac Gluten sensitivity: the new frontier of gluten related disorders. Nutrients. 2013;5(10):3839–53. Epub 2013/10/01. doi: 10.3390/nu5103839 24077239; PubMed Central PMCID: PMC3820047.

32. Garcia A, Niubo J, Benitez MA, Viqueira M, Perez JL. Comparison of two leukocyte extraction methods for cytomegalovirus antigenemia assay. J Clin Microbiol. 1996;34(1):182–4. 8748299; PubMed Central PMCID: PMC228756.

33. Mandourah AY, Ranganath L, Barraclough R, Vinjamuri S, Hof RV, Hamill S, et al. Circulating microRNAs as potential diagnostic biomarkers for osteoporosis. Sci Rep. 2018;8(1):8421. doi: 10.1038/s41598-018-26525-y 29849050; PubMed Central PMCID: PMC5976644.

34. Pedroza-Torres A, Fernandez-Retana J, Peralta-Zaragoza O, Jacobo-Herrera N, Cantu de Leon D, Cerna-Cortes JF, et al. A microRNA expression signature for clinical response in locally advanced cervical cancer. Gynecol Oncol. 2016;142(3):557–65. doi: 10.1016/j.ygyno.2016.07.093 27423381.

35. Sperveslage J, Hoffmeister M, Henopp T, Kloppel G, Sipos B. Establishment of robust controls for the normalization of miRNA expression in neuroendocrine tumors of the ileum and pancreas. Endocrine. 2014;46(2):226–30. doi: 10.1007/s12020-014-0202-5 24535468.

36. Mase M, Grasso M, Avogaro L, D'Amato E, Tessarolo F, Graffigna A, et al. Selection of reference genes is critical for miRNA expression analysis in human cardiac tissue. A focus on atrial fibrillation. Sci Rep. 2017;7:41127. doi: 10.1038/srep41127 28117343; PubMed Central PMCID: PMC5259703.

37. Sen A, Ren S, Lerchenmuller C, Sun J, Weiss N, Most P, et al. MicroRNA-138 regulates hypoxia-induced endothelial cell dysfunction by targeting S100A1. PLoS One. 2013;8(11):e78684. doi: 10.1371/journal.pone.0078684 24244340; PubMed Central PMCID: PMC3823839.

38. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. doi: 10.1006/meth.2001.1262 11846609.

39. Faresjo T, Faresjo A. To match or not to match in epidemiological studies—same outcome but less power. Int J Environ Res Public Health. 2010;7(1):325–32. doi: 10.3390/ijerph7010325 20195449; PubMed Central PMCID: PMC2819792.

40. Benjamini Y, Krieger AM, Yekutieli D. Adaptive linear step-up procedures that control the false discovery rate. Biometrika. 2006;93(3):491–507. doi: 10.1093/biomet/93.3.491 WOS:000241271700001.

41. Orr M, Liu P. Sample Size Estimation while Controlling False Discovery Rate for Microarray Experiments Using the ssize.fdr Package. The R Journal. 2009;1(1):6. doi: 10.32614/RJ-2009-019

42. Fasano A, Sapone A, Zevallos V, Schuppan D. Nonceliac gluten sensitivity. Gastroenterology. 2015;148(6):1195–204. Epub 2015/01/15. doi: 10.1053/j.gastro.2014.12.049 25583468.

43. Leonard MM, Sapone A, Catassi C, Fasano A. Celiac Disease and Nonceliac Gluten Sensitivity: A Review. JAMA. 2017;318(7):647–56. doi: 10.1001/jama.2017.9730 28810029.

44. Zanini B, Basche R, Ferraresi A, Ricci C, Lanzarotto F, Marullo M, et al. Randomised clinical study: gluten challenge induces symptom recurrence in only a minority of patients who meet clinical criteria for non-coeliac gluten sensitivity. Aliment Pharmacol Ther. 2015;42(8):968–76. doi: 10.1111/apt.13372 26310131.

45. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–33. doi: 10.1016/j.cell.2009.01.002 19167326; PubMed Central PMCID: PMC3794896.

46. Chen X, Guo X, Zhang H, Xiang Y, Chen J, Yin Y, et al. Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene. 2009;28(10):1385–92. doi: 10.1038/onc.2008.474 19137007.

47. Chivukula RR, Shi G, Acharya A, Mills EW, Zeitels LR, Anandam JL, et al. An essential mesenchymal function for miR-143/145 in intestinal epithelial regeneration. Cell. 2014;157(5):1104–16. doi: 10.1016/j.cell.2014.03.055 24855947; PubMed Central PMCID: PMC4175516.

48. Wu J, He Y, Luo Y, Zhang L, Lin H, Liu X, et al. MiR-145-5p inhibits proliferation and inflammatory responses of RMC through regulating AKT/GSK pathway by targeting CXCL16. J Cell Physiol. 2018;233(4):3648–59. doi: 10.1002/jcp.26228 29030988.

49. Yuan M, Zhang L, You F, Zhou J, Ma Y, Yang F, et al. MiR-145-5p regulates hypoxia-induced inflammatory response and apoptosis in cardiomyocytes by targeting CD40. Mol Cell Biochem. 2017;431(1–2):123–31. doi: 10.1007/s11010-017-2982-4 28281187.

50. Deiuliis JA. MicroRNAs as regulators of metabolic disease: pathophysiologic significance and emerging role as biomarkers and therapeutics. Int J Obes (Lond). 2016;40(1):88–101. doi: 10.1038/ijo.2015.170 26311337; PubMed Central PMCID: PMC4722234.

51. Keller A, Leidinger P, Lange J, Borries A, Schroers H, Scheffler M, et al. Multiple sclerosis: microRNA expression profiles accurately differentiate patients with relapsing-remitting disease from healthy controls. PLoS One. 2009;4(10):e7440. doi: 10.1371/journal.pone.0007440 19823682; PubMed Central PMCID: PMC2757919.

52. Ma X, Zhou J, Zhong Y, Jiang L, Mu P, Li Y, et al. Expression, regulation and function of microRNAs in multiple sclerosis. Int J Med Sci. 2014;11(8):810–8. doi: 10.7150/ijms.8647 24936144; PubMed Central PMCID: PMC4057480.

53. Gandhi R, Healy B, Gholipour T, Egorova S, Musallam A, Hussain MS, et al. Circulating microRNAs as biomarkers for disease staging in multiple sclerosis. Ann Neurol. 2013;73(6):729–40. doi: 10.1002/ana.23880 23494648.

54. Chen JQ, Papp G, Poliska S, Szabo K, Tarr T, Balint BL, et al. MicroRNA expression profiles identify disease-specific alterations in systemic lupus erythematosus and primary Sjogren's syndrome. PLoS One. 2017;12(3):e0174585. doi: 10.1371/journal.pone.0174585 28339495; PubMed Central PMCID: PMC5365120.

55. Concepcion CP, Bonetti C, Ventura A. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J. 2012;18(3):262–7. doi: 10.1097/PPO.0b013e318258b60a 22647363; PubMed Central PMCID: PMC3592780.

56. Paladini L, Fabris L, Bottai G, Raschioni C, Calin GA, Santarpia L. Targeting microRNAs as key modulators of tumor immune response. J Exp Clin Cancer Res. 2016;35:103. doi: 10.1186/s13046-016-0375-2 27349385; PubMed Central PMCID: PMC4924278.

57. Liu SQ, Jiang S, Li C, Zhang B, Li QJ. miR-17-92 cluster targets phosphatase and tensin homology and Ikaros Family Zinc Finger 4 to promote TH17-mediated inflammation. J Biol Chem. 2014;289(18):12446–56. doi: 10.1074/jbc.M114.550723 24644282; PubMed Central PMCID: PMC4007439.

58. Puccetti A, Saverino D, Opri R, Gabrielli O, Zanoni G, Pelosi A, et al. Immune Response to Rotavirus and Gluten Sensitivity. J Immunol Res. 2018;2018:9419204. doi: 10.1155/2018/9419204 29736406; PubMed Central PMCID: PMC5875030.

59. Zahm AM, Thayu M, Hand NJ, Horner A, Leonard MB, Friedman JR. Circulating microRNA is a biomarker of pediatric Crohn disease. J Pediatr Gastroenterol Nutr. 2011;53(1):26–33. doi: 10.1097/MPG.0b013e31822200cc 21546856; PubMed Central PMCID: PMC3807879.

60. Kim BS, Jung JY, Jeon JY, Kim HA, Suh CH. Circulating hsa-miR-30e-5p, hsa-miR-92a-3p, and hsa-miR-223-3p may be novel biomarkers in systemic lupus erythematosus. Hla. 2016;88(4):187–93. doi: 10.1111/tan.12874 27596248.

61. Weaver CT, Elson CO, Fouser LA, Kolls JK. The Th17 pathway and inflammatory diseases of the intestines, lungs, and skin. Annu Rev Pathol. 2013;8:477–512. doi: 10.1146/annurev-pathol-011110-130318 23157335; PubMed Central PMCID: PMC3965671.


Článok vyšiel v časopise

PLOS One


2019 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#