Decoding norovirus infection in crohn's disease

Inflammatory Bowel Diseases

Volumn 20, Issue 4, 2014, Pages 767-770

  Chamaillard, Mathias ^a,b   Cesaro, Annabelle ^a,b   Lober, Pierre Emmanuel ^c   Hober, Didier ^c  

^a INSERM U1019   (France)

^b UNIV LILLE   (France)

^c University Lille   (France)

Author keywords

Crohn's ileitis; Dysbiosis; Fecal transplantation; Norovirus; Vitamin B12 deficiency

Indexed keywords

CROHN DISEASE; DISEASE PREDISPOSITION; DYSBIOSIS; FECES MICROFLORA; HOST RESISTANCE; HUMAN; ILEITIS; NONHUMAN; NOROVIRUS INFECTION; PRIORITY JOURNAL; REVIEW; VIRUS RESISTANCE; ASYMPTOMATIC INFECTION; CALICIVIRUS INFECTION; COMPLICATION; GENETIC PREDISPOSITION; GENETICS; NOROVIRUS; VIROLOGY;

ALCOHOL DEHYDROGENASE; ATG16L1 PROTEIN, HUMAN; CARRIER PROTEIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; FUCOSYLTRANSFERASE; GALACTOSIDE 2-ALPHA-L-FUCOSYLTRANSFERASE; LACTATE-MALATE TRANSHYDROGENASE; NOD2 PROTEIN, HUMAN;

ALCOHOL OXIDOREDUCTASES; ASYMPTOMATIC INFECTIONS; CALICIVIRIDAE INFECTIONS; CARRIER PROTEINS; CROHN DISEASE; DYSBIOSIS; FUCOSYLTRANSFERASES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; ILEITIS; NOD2 SIGNALING ADAPTOR PROTEIN; NOROVIRUS;

EID: 84898750790     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/01.MIB.0000440613.83703.4a     Document Type: Review

References (68)

1. Fankhauser RL, Noel JS, Monroe SS, et al. Molecular epidemiology of "Norwalk-like viruses" in outbreaks of gastroenteritis in the United States. J Infect Dis. 1998;178:1571-1578.
2. Hutson AM, Atmar RL, Estes MK. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 2004;12: 279-287.
3. Lopman BA, Brown DW, Koopmans M. Human caliciviruses in Europe. J Clin Virol. 2002;24:137-160.
4. Kirkwood CD, Streitberg R. Calicivirus shedding in children after recovery from diarrhoeal disease. J Clin Virol. 2008;43:346-348.
5. Zintz C, Bok K, Parada E, et al. Prevalence and genetic characterization of caliciviruses among children hospitalized for acute gastroenteritis in the United States. Infect Genet Evol. 2005;5:281-290.
6. Hutson AM, Atmar RL, Marcus DM, et al. Norwalk virus-like particle hemagglutination by binding to h histo-blood group antigens. J Virol. 2003;77:405-415.
7. Harrington PR, Vinje J, Moe CL, et al. Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions. J Virol. 2004;78: 3035-3045.
8. Lindesmith L, Moe C, Marionneau S, et al. Human susceptibility and resistance to Norwalk virus infection. Nat Med. 2003;9:548-553.
9. Kelly RJ, Rouquier S, Giorgi D, et al. Sequence and expression of a candidate for the human Secretor blood group alpha(1,2)fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J Biol Chem. 1995;270:4640-4649.
10. Kaneko M, Nishihara S, Shinya N, et al. Wide variety of point mutations in the H gene of Bombay and para-Bombay individuals that inactivate H enzyme. Blood. 1997;90:839-849.
11. Thorven M, Grahn A, Hedlund KO, et al. A homozygous nonsense mutation (428G-.A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. J Virol. 2005; 79:15351-15355.
12. Larsson MM, Rydell GE, Grahn A, et al. Antibody prevalence and titer to norovirus (genogroup II) correlate with secretor (FUT2) but not with ABO phenotype or Lewis (FUT3) genotype. J Infect Dis. 2006;194:1422-1427.
13. Soejima M, Koda Y. Molecular mechanisms of Lewis antigen expression. Leg Med (Tokyo). 2005;7:266-269.
14. Kudo T, Iwasaki H, Nishihara S, et al. Molecular genetic analysis of the human Lewis histo-blood group system. II. Secretor gene inactivation by a novel single missense mutation A385T in Japanese nonsecretor individuals. J Biol Chem. 1996;271:9830-9837.
15. Ferrer-Admetlla A, Sikora M, Laayouni H, et al. A natural history of FUT2 polymorphism in humans. Mol Biol Evol. 2009;26:1993-2003.
16. Koda Y, Tachida H, Soejima M, et al. Ancient origin of the null allele se (428) of the human ABO-secretor locus (FUT2). J Mol Evol. 2000;50: 243-248.
17. Wobus CE, Karst SM, Thackray LB, et al. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2004;2:e432.
18. Elftman MD, Gonzalez-Hernandez MB, Kamada N, et al. Multiple effects of dendritic cell depletion on murine norovirus infection. J Gen Virol. 2013;94:1761-1768.
19. Fang H, Tan M, Xia M, et al. Norovirus P particle efficiently elicits innate, humoral and cellular immunity. PLoS One. 2013;8:e63269.
20. McCartney SA, Thackray LB, Gitlin L, et al. MDA-5 recognition of a murine norovirus. PLoS Pathog. 2008;4:e1000108.
21. Sabbah A, Chang TH, Harnack R, et al. Activation of innate immune antiviral responses by Nod2. Nat Immunol. 2009;10:1073-1080.
22. Karst SM, Wobus CE, Lay M, et al. STAT1-dependent innate immunity to a Norwalk-like virus. Science. 2003;299:1575-1578.
23. Mumphrey SM, Changotra H, Moore TN, et al. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J Virol. 2007;81:3251-3263.
24. Thackray LB, Duan E, Lazear HM, et al. Critical role for interferon regulatory factor 3 (IRF-3) and IRF-7 in type I interferon-mediated control of murine norovirus replication. J Virol. 2012;86:13515-13523.
25. Changotra H, Jia Y, Moore TN, et al. Type I and type II interferons inhibit the translation of murine norovirus proteins. J Virol. 2009;83:5683-5692.
26. Jounai N, Takeshita F, Kobiyama K, et al. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci U S A. 2007;104:14050-14055.
27. Hwang S, Maloney NS, Bruinsma MW, et al. Nondegradative role of Atg5-Atg12/Atg16L1 autophagy protein complex in antiviral activity of interferon gamma. Cell Host Microbe. 2012;11:397-409.
28. Zhu S, Regev D, Watanabe M, et al. Identification of immune and viral correlates of norovirus protective immunity through comparative study of intra-cluster norovirus strains. PLoS Pathog. 2013;9:e1003592.
29. Chachu KA, LoBue AD, Strong DW, et al. Immune mechanisms responsible for vaccination against and clearance of mucosal and lymphatic norovirus infection. PLoS Pathog. 2008;4:e1000236.
30. Chachu KA, Strong DW, LoBue AD, et al. Antibody is critical for the clearance of murine norovirus infection. J Virol. 2008;82:6610-6617.
31. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology. 2004; 126:1504-1517.
32. McGovern DP, Jones MR, Taylor KD, et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet. 2010;19:3468-3476.
33. Franke A, McGovern DP, Barrett JC, et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet. 2010;42:1118-1125.
34. Miyoshi J, Yajima T, Okamoto S, et al. Ectopic expression of blood type antigens in inflamed mucosa with higher incidence of FUT2 secretor status in colonic Crohn's disease. J Gastroenterol. 2011;46:1056-1063.
35. Gebhard RL, Greenberg HB, Singh N, et al. Acute viral enteritis and exacerbations of inflammatory bowel disease. Gastroenterology. 1982; 83:1207-1209.
36. Van Kruiningen HJ, Mayo DR, Vanopdenbosch E, et al. Virus serology in familial Crohn disease. Scand J Gastroenterol. 2000;35:403-407.
37. Gump D, Caul E, Eade O, et al. Lymphocytotoxic and microbial antibodies in Crohn's disease and matched controls. Antonie Van Leeuwenhoek. 1981;47:455-464.
38. Kolho KL, Klemola P, Simonen-Tikka ML, et al. Enteric viral pathogens in children with inflammatory bowel disease. J Med Virol. 2012;84: 345-347.
39. Tanaka T, Scheet P, Giusti B, et al. Genome-wide association study of vitamin B6, vitamin B12, folate, and homocysteine blood concentrations. Am J Hum Genet. 2009;84:477-482.
40. Hazra A, Kraft P, Selhub J, et al. Common variants of FUT2 are associated with plasma vitamin B12 levels. Nat Genet. 2008;40:1160-1162.
41. Peyrin-Biroulet L, Rodriguez-Gueant RM, Chamaillard M, et al. Vascular and cellular stress in inflammatory bowel disease: revisiting the role of homocysteine. Am J Gastroenterol. 2007;102:1108-1115.
42. Adolph TE, Tomczak MF, Niederreiter L, et al. Paneth cells as a site of origin for intestinal inflammation. Nature. 2013;503:272-276.
43. Chu H, Pazgier M, Jung G, et al. Human alpha-defensin 6 promotes mucosal innate immunity through self-assembled peptide nanonets. Science. 2012;337:477-481.
44. Salzman NH, Ghosh D, Huttner KM, et al. Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature. 2003;422:522-526.
45. Bressenot A, Pooya S, Bossenmeyer-Pourie C, et al. Methyl donor deficiency affects small-intestinal differentiation and barrier function in rats. Br J Nutr. 2012;1-11.
46. Cadwell K, Patel KK, Maloney NS, et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell. 2010;141:1135-1145.
47. Chamaillard M, Dessein R. Defensins couple dysbiosis to primary immunodeficiency in Crohn's disease. World J Gastroenterol. 2011; 17:567-571.
48. Murakami K, Kurihara C, Oka T, et al. Norovirus binding to intestinal epithelial cells is independent of histo-blood group antigens. PLoS One. 2013;8:e66534.
49. Parmar AS, Alakulppi N, Paavola-Sakki P, et al. Association study of FUT2 (rs601338) with celiac disease and inflammatory bowel disease in the Finnish population. Tissue Antigens. 2012;80:488-493.
50. Bry L, Falk PG, Midtvedt T, et al. A model of host-microbial interactions in an open mammalian ecosystem. Science. 1996;273:1380-1383.
51. Lin B, Hayashi Y, Saito M, et al. GDP-fucose: beta-galactoside alpha1,2- fucosyltransferase, MFUT-II, and not MFUT-I or -III, is induced in a restricted region of the digestive tract of germ-free mice by hostmicrobe interactions and cycloheximide. Biochim Biophys Acta. 2000; 1487:275-285.
52. Meng D, Newburg DS, Young C, et al. Bacterial symbionts induce a FUT2-dependent fucosylated niche on colonic epithelium via ERK and JNK signaling. Am J Physiol Gastrointest Liver Physiol. 2007;293: G780-G787.
53. Nelson AM, Walk ST, Taube S, et al. Disruption of the human gut microbiota following Norovirus infection. PLoS One. 2012;7:e48224.
54. Frank DN, Robertson CE, Hamm CM, et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17:179-184.
55. Rausch P, Rehman A, Kunzel S, et al. Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc Natl Acad Sci U S A. 2011;108:19030-19035.
56. Folseraas T, Melum E, Rausch P, et al. Extended analysis of a genomewide association study in primary sclerosing cholangitis detects multiple novel risk loci. J Hepatol. 2012;57:366-375.
57. Rehman A, Sina C, Gavrilova O, et al. Nod2 is essential for temporal development of intestinal microbial communities. Gut. 2011;60:1354-1362.
58. Mondot S, Barreau F, Al Nabhani Z, et al. Altered gut microbiota composition in immune-impaired Nod2(-/-) mice. Gut. 2012;61:634-635.
59. Petnicki-Ocwieja T, Hrncir T, Liu YJ, et al. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A. 2009;106:15813-15818.
60. Couturier-Maillard A, Secher T, Rehman A, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest. 2013;123:700-711.
61. Cave DR, Mitchell DN, Brooke BN. Experimental animal studies of the etiology and pathogenesis of Crohn's disease Gastroenterology. 1975;69: 618-624.
62. Mitchell DN, Rees RJ. Further observations on the transmissibility of Crohn's disease. Ann N Y Acad Sci. 1976;278:546-559.
63. Das KM, Valenzuela I, Williams SE, et al. Studies of the etiology of Crohn's disease using athymic nude mice. Gastroenterology. 1983;84: 364-374.
64. Hober D, Sauter P. Pathogenesis of type 1 diabetes mellitus: interplay between enterovirus and host. Nat Rev Endocrinol. 2010;6:279-289.
65. Lidar M, Langevitz P, Shoenfeld Y. The role of infection in inflammatory bowel disease: initiation, exacerbation and protection. Isr Med Assoc J. 2009;11:558-563.
66. Hubbard VM, Cadwell K. Viruses, autophagy genes, and Crohn's disease. Viruses. 2011;3:1281-1311.
67. Foxman EF, Iwasaki A. Genome-virome interactions: examining the role of common viral infections in complex disease. Nat Rev Microbiol. 2011; 9:254-264.
68. Schwartz M, Gluck M, Koon S. Norovirus gastroenteritis after fecal microbiota transplantation for treatment of Clostridium difficile infection despite asymptomatic donors and lack of sick contacts. Am J Gastroenterol. 2013;108:1367.