Metagenomics reveals dysbiosis and a potentially pathogenic N. flavescens strain in duodenum of adult celiac patients

American Journal of Gastroenterology

Volumn 111, Issue 6, 2016, Pages 879-890

  D'Argenio, Valeria ^a,b   Casaburi, Giorgio ^a,k   Precone, Vincenza ^a,b   Pagliuca, Chiara ^a,b   Colicchio, Roberta ^b   Sarnataro, Daniela ^a,b   Discepolo, Valentina ^a,b   Kim, Sangman M ^c   Russo, Ilaria ^d   Del Vecchio Blanco, Giovanna ^e   Horner, David S ^f   Chiara, Matteo ^f   Pesole, Graziano ^g,h   Salvatore, Paola ^a,b   Monteleone, Giovanni ^e   Ciacci, Carolina ^d   Caporaso, Gregory J ⁱ   Jabrì, Bana ^c   Salvatore, Francesco ^a,b,j   Sacchetti, Lucia ^a  

^a CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c University of Chicago Medicine   (United States)

^d UNIVERSITY OF SALERNO   (Italy)

^e UNIVERSITY OF ROME TOR VERGATA   (Italy)

^f UNIVERSITY OF MILAN   (Italy)

^g CNR   (Italy)

^h UNIVERSITY OF BARI   (Italy)

ⁱ NORTHERN ARIZONA UNIVERSITY   (United States)

^j IRCCS SDN   (Italy)

^k UNIVERSITY OF FLORIDA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; GLYCOPROTEIN P 15095; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HAPTOGLOBIN; HEMOGLOBIN; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; IRON; RNA 16S; TRANSFERRIN; TUMOR NECROSIS FACTOR ALPHA;

ACTINOBACTERIA; ADULT; ARTICLE; BACTERIAL GENOME; BONE MARROW DERIVED DENDRITIC CELL; CAUCASIAN; CELIAC DISEASE; CHRONIC GASTRITIS; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DIARRHEA; DNA SEQUENCE; DUODENUM; DUODENUM BIOPSY; DYSBIOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FEMALE; FIRMICUTES; GASTROESOPHAGEAL REFLUX; GENETIC VARIABILITY; GLUTEN FREE DIET; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; LACTOBACILLUS; MALE; MASS SPECTROMETRY; MONOCYTE; NEISSERIA; NEISSERIA FLAVESCENS; NONHUMAN; PRIORITY JOURNAL; WEIGHT REDUCTION; BIOPSY; CACO-2 CELL LINE; CLASSIFICATION; FLUORESCENT ANTIBODY TECHNIQUE; ISOLATION AND PURIFICATION; ITALY; METAGENOMICS; MICROBIOLOGY; MICROFLORA; PROTEOBACTERIA;

ACTINOBACTERIA; ADULT; BIOPSY; CACO-2 CELLS; CELIAC DISEASE; DIET, GLUTEN-FREE; DUODENUM; DYSBIOSIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; ITALY; MALE; METAGENOMICS; MICROBIOTA; NEISSERIA; PROTEOBACTERIA;

EID: 84962708324     PISSN: 00029270     EISSN: 15720241     Source Type: Journal    
DOI: 10.1038/ajg.2016.95     Document Type: Article

References (56)

1. Green PH, Cellier C. Celiac disease. N Engl J Med 2007; 357: 1731-43.
2. Schuppan D, Junker Y, Barisani D. Celiac disease: from pathogenesis to novel therapies. Gastroenterology 2009; 137: 1912-33.
3. Sollid LM. Coeliac disease: dissecting a complex infl ammatory disorder. Nat Rev Immunol 2002; 2: 647-55.
4. Stene LC, Honeyman MC, Hoffenberg EJ, et al. Rotavirus infection frequency and risk of celiac disease autoimmunity in early childhood: a longitudinal study. Am J Gastroenterol 2006; 101: 2333-40.
5. Akobeng AK, Ramanan AV, Buchan I, et al. Eff ect of breast feeding on risk of coeliac disease: a systematic review and meta-Analysis of observational studies. Arch Dis Child 2006; 91: 39-43.
6. Vivas S, Ruiz de Morales JM, Fernandez M, et al. Age-related clinical, serological, and histopathological features of celiac disease. Am J Gastroenterol 2008; 103: 2360-5.
7. Lohi S, Mustalahti K, Kaukinen K, et al. Increasing prevalence of coeliac disease over time. Aliment Pharmacol Ther 2007; 26: 1217-25.
8. Sanz Y, Sanchez E, Marzotto M, et al. Diff erences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol 2007; 51: 562-8.
9. Collado MC, Calabuig M, Sanz Y. Diff erences between the fecal microbiota of celiac infants and healthy controls. Curr Issues Intest Microbiol 2007; 8: 9-14.
10. Conte MP, Schippa S, Zamboni I, et al. Gut-Associated bacterial microbiota in paediatric patients with infl ammatory bowel disease. Gut 2006; 55: 1760-7.
11. Maynard CL, Elson CO, Hatton RD, et al. Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012; 489: 231-41.
12. Becker S, Oelschlaeger TA, Wullaert A, et al. Bacteria regulate intestinal epithelial cell diff erentiation factors both in vitro and in vivo. PLoS One 2013; 8: e55620.
13. Capuano M, Iaffaldano L, Tinto N, et al. MicroRNA-449a overexpression, reduced NOTCH1 signals and scarce goblet cells characterize the small intestine of celiac patients. PLoS One 2011; 6: e29094.
14. McAuley JL, Linden SK, Png CW, et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007; 117: 2313-34.
15. De Palma G, Nadal I, Medina M, et al. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol 2010; 10: 63.
16. Nistal E, Caminero A, Vivas S, et al. Diff erences in faecal bacteria populations and faecal bacteria metabolism in healthy adults and celiac disease patients. Biochimie 2012; 94: 1724-9.
17. Sellitto M, Bai G, Serena G, et al. Proof of concept of microbiome-metabolome analysis and delayed gluten exposure on celiac disease autoimmunity in genetically at-risk infants. PLoS One 2012; 7: e33387.
18. Nadal I, Donat E, Ribes-Koninckx C, et al. Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J Med Microbiol 2007; 56: 1669-74.
19. Collado MC, Donat E, Ribes-Koninckx C, et al. Specifi c duodenal and faecal bacterial groups associated with paediatric coeliac disease. J Clin Pathol 2009; 62: 264-9.
20. Ou G, Hedberg M, Horstedt P, et al. Proximal small intestinal microbiota and identifi cation of rod-shaped bacteria associated with childhood celiac disease. Am J Gastroenterol 2009; 104: 3058-67.
21. Di Cagno R, De Angelis M, De Pasquale I, et al. Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol 2011; 11: 219.
22. Nistal E, Caminero A, Herran AR, et al. Diff erences of small intestinal bacteria populations in adults and children with/without celiac disease: eff ect of age, gluten diet, and disease. Infl amm Bowel Dis 2012; 18: 649-56.
23. Wacklin P, Kaukinen K, Tuovinen E, et al. The duodenal microbiota composition of adult celiac disease patients is associated with the clinical manifestation of the disease. Infl amm Bowel Dis 2013; 19: 934-41.
24. Cheng J, Kalliomaki M, Heilig HG, et al. Duodenal microbiota composition and mucosal homeostasis in pediatric celiac disease. BMC Gastroenterol 2013; 13: 113.
25. Sanchez E, Donat E, Ribes-Koninckx C, et al. Duodenal-mucosal bacteria associated with celiac disease in children. Appl Environ Microbiol 2013; 79: 5472-9.
26. Saulnier DM, Riehle K, Mistretta TA, et al. Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology 2011; 141: 1782-91.
27. Koren O, Knights D, Gonzalez A, et al. A guide to enterotypes across the human body: meta-Analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol 2013; 9: e1002863.
28. Huebinger RM, Liu MM, Dowd SE, et al. Examination with next-generation sequencing technology of the bacterial microbiota in bronchoalveolar lavage samples aft er traumatic injury. Surg Infect 2013; 14: 275-82.
29. Schwarzberg K, Le R, Bharti B, et al. The personal human oral microbiome obscures the eff ects of treatment on periodontal disease. PLoS One 2014; 9: e86708.
30. D'Argenio V, Precone V, Casaburi G, et al. An altered gut microbiome profi le in a child aff ected by Crohn's disease normalized aft er nutritional therapy. Am J Gastroenterol 2013; 108: 851-2.
31. Hill P, Austin A, Forsyth J, et al. British Society of Gastroenterology guidelines on the diagnosis and management of coeliac disease. Gut 2015; 64 ( 4 ): 691-2.
32. Baker GC, Smith JJ, Cowan DA. Review and re-Analysis of domain-specifi c 16S primers. J Microbiol Methods 2003; 55: 541-55.
33. Margulies M, Egholm M, Altman WE, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005; 437: 376-80.
34. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-Throughput community sequencing data. Nat Methods 2010; 7: 335-6.
35. Bucci C, Lavitola A, Salvatore P, et al. Hypermutation in pathogenic bacteria: frequent phase variation in meningococci is a phenotypic trait of a specialized mutator biotype. Mol Cell 1999; 3: 435-45.
36. D'Argenio V, Petrillo M, Cantiello P, et al. De novo sequencing and assembly of the whole genome of Novosphingobium sp. strain PP1Y. J Bacteriol 2011; 193: 4296.
37. Bankevich A, Nurk S, Antipov D, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19: 455-77.
38. Aziz RK, Bartels D, Best AA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9: 75.
39. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5: 113.
40. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17: 540-52.
41. Stamatakis A, Ludwig T, Meier H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. B ioinformatics 2005; 21: 456-63.
42. Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001; 18: 691-9.
43. Ardavin C, Martinez del Hoyo G, Martin P, et al. Origin and diff erentiation of dendritic cells. Trends Immunol 2001; 22: 691-700.
44. Devkota S, Wang Y, Musch MW, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 2012; 487: 104-8.
45. Spinosa MR, Progida C, Tala A, et al. The Neisseria meningitidis capsule is important for intracellular survival in human cells. Infect Immun 2007; 75: 3594-603.
46. Tala A, De Stefano M, Bucci C, et al. Reverse transcriptase-PCR diff erential display analysis of meningococcal transcripts during infection of human cells: Up-regulation of priA and its role in intracellular replication. BMC Microbiol 2008; 8: 131.
47. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol 2001; 26: 32-46.
48. Evans NJ, Harrison OB, Clow K, et al. Variation and molecular evolution of HmbR, the Neisseria meningitidis haemoglobin receptor. Microbiology 2010; 156: 1384-93.
49. Tauseef I, Harrison OB, Wooldridge KG, et al. Influence of the combination and phase variation status of the haemoglobin receptors HmbR and HpuAB on meningococcal virulence. Microbiology 2011; 157: 1446-56.
50. Harrison OB, Bennett JS. Derrick JP, et al. Distribution and diversity of the haemoglobin-haptoglobin iron-Acquisition systems in pathogenic and non-pathogenic Neisseria. Microbiology 2013; 159: 1920-30.
51. Mahlen SD. Serratia Infections: from military experiments to current practice. In: Clin Microbiol Rev 2011; 24: 755-91.
52. Wacklin P, Laurikka P, Lindfors K, et al. Altered duodenal microbiota composition in celiac disease patients suff ering from persistent symptoms on a long-Term gluten-free diet. Am J Gastroenterol 2014; 109: 1933-41.
53. Caminero A, Nistal E, Herran AR, et al. Diff erences in gluten metabolism among healthy volunteers, coeliac disease patients and fi rst-degree relatives. Br J Nutr 2015; 114: 1157-67.
54. Caminero A, Herran AR, Nistal E, et al. Diversity of the cultivable human gut microbiome involved in gluten metabolism: isolation of microorganisms with potential interest for coeliac disease. FEMS Microbiol Ecol 2014; 88: 309-19.
55. Fernandez-Feo M, Wei G, Blumenkranz G, et al. The cultivable human oral gluten-degrading microbiome and its potential implications in coeliac disease and gluten sensitivity. Clin Microbiol Infect 2013; 19: E386-E394.
56. Barone MV, Zanzi D, Maglio M, et al. Gliadin-mediated proliferation and innate immune activation in celiac disease are due to alterations in vesicular traffi cking. PLoS One 2011; 6: e17039.