The role of osteopontin (OPN/SPP1) haplotypes in the susceptibility to crohn's disease

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Glas, Jürgen ^a,b,c   Seiderer, Julia ^a   Bayrle, Corinna ^b   Wetzke, Martin ^d   Fries, Christoph ^a,b   Tillack, Cornelia ^a   Olszak, Torsten ^a,e   Beigel, Florian ^a   Steib, Christian ^a   Friedrich, Matthias ^a,b   Diegelmann, Julia ^a,b   Czamara, Darina ^f   Brand, Stephan ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; INTERLEUKIN 22; IL23R PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE; INTERLEUKIN RECEPTOR; INTERLEUKIN-22; OSTEOPONTIN;

ADOLESCENT; ADULT; AGED; ARTICLE; CAUCASIAN; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE RELEASE; DISEASE PREDISPOSITION; FEMALE; GENE; GENETIC ASSOCIATION; GENETIC EPISTASIS; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HETEROZYGOTE; HUMAN; IL23R GENE; INTERLEUKIN 22 BLOOD LEVEL; MAJOR CLINICAL STUDY; MALE; OSTEOPONTIN GENE; PROTEIN BLOOD LEVEL; SCHOOL CHILD; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; ULCERATIVE COLITIS; BLOOD; CASE CONTROL STUDY; DEMOGRAPHY; GENE FREQUENCY; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; SEXUAL DEVELOPMENT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; CHILD; COLITIS, ULCERATIVE; CROHN DISEASE; DEMOGRAPHY; EPISTASIS, GENETIC; FEMALE; GENE FREQUENCY; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; INTERLEUKINS; MALE; MIDDLE AGED; OSTEOPONTIN; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, INTERLEUKIN; SEX CHARACTERISTICS; YOUNG ADULT;

EID: 84855292706     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029309     Document Type: Article

References (76)

1. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, et al. (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603.
2. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, et al. (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603-606.
3. Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, et al. (2006) A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314: 1461-1463.
4. Glas J, Seiderer J, Wetzke M, Konrad A, Torok HP, et al. (2007) rs1004819 is the main disease-associated IL23R variant in German Crohn's disease patients: combined analysis of IL23R, CARD15, and OCTN1/2 variants. PLoS ONE 2: e819.
5. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, et al. (2007) A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 39: 207-211.
6. Glas J, Konrad A, Schmechel S, Dambacher J, Seiderer J, et al. (2008) The ATG16L1 gene variants rs2241879 and rs2241880 (T300A) are strongly associated with susceptibility to Crohn's disease in the German population. Am J Gastroenterol 103: 682-691.
7. Libioulle C, Louis E, Hansoul S, Sandor C, Farnir F, et al. (2007) Novel Crohn disease locus identified by genome-wide association maps to a gene desert on 5p13.1 and modulates expression of PTGER4. PLoS Genet 3: e58.
8. Brand S, (2009) Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 58: 1152-1167.
9. Kawamura K, Iyonaga K, Ichiyasu H, Nagano J, Suga M, et al. (2005) Differentiation, maturation, and survival of dendritic cells by osteopontin regulation. Clin Diagn Lab Immunol 12: 206-212.
10. O'Regan A, Berman JS, (2000) Osteopontin: a key cytokine in cell-mediated and granulomatous inflammation. Int J Exp Pathol 81: 373-390.
11. Giachelli CM, Steitz S, (2000) Osteopontin: a versatile regulator of inflammation and biomineralization. Matrix Biol 19: 615-622.
12. Mori R, Shaw TJ, Martin P, (2008) Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring. J Exp Med 205: 43-51.
13. Uede T, (2011) Osteopontin, intrinsic tissue regulator of intractable inflammatory diseases. Pathol Int 61: 265-280.
14. Lund SA, Giachelli CM, Scatena M, (2009) The role of osteopontin in inflammatory processes. J Cell Commun Signal 3: 311-322.
15. Renkl AC, Wussler J, Ahrens T, Thoma K, Kon S, et al. (2005) Osteopontin functionally activates dendritic cells and induces their differentiation toward a Th1-polarizing phenotype. Blood 106: 946-955.
16. Ohshima S, Yamaguchi N, Nishioka K, Mima T, Ishii T, et al. (2002) Enhanced local production of osteopontin in rheumatoid joints. J Rheumatol 29: 2061-2067.
17. Bazzichi L, Ghiadoni L, Rossi A, Bernardini M, Lanza M, et al. (2009) Osteopontin is associated with increased arterial stiffness in rheumatoid arthritis. Mol Med 15: 402-406.
18. Sennels H, Sorensen S, Ostergaard M, Knudsen L, Hansen M, et al. (2008) Circulating levels of osteopontin, osteoprotegerin, total soluble receptor activator of nuclear factor-kappa B ligand, and high-sensitivity C-reactive protein in patients with active rheumatoid arthritis randomized to etanercept alone or in combination with methotrexate. Scand J Rheumatol 37: 241-247.
19. Buommino E, Tufano MA, Balato N, Canozo N, Donnarumma M, et al. (2009) Osteopontin: a new emerging role in psoriasis. Arch Dermatol Res 301: 397-404.
20. Vogt MH, Ten Kate J, Drent RJ, Polman CH, Hupperts R, (2010) Increased osteopontin plasma levels in multiple sclerosis patients correlate with bone-specific markers. Mult Scler 16: 443-449.
21. Murugaiyan G, Mittal A, Weiner HL, (2008) Increased osteopontin expression in dendritic cells amplifies IL-17 production by CD4+ T cells in experimental autoimmune encephalomyelitis and in multiple sclerosis. J Immunol 181: 7480-7488.
22. Braitch M, Nunan R, Niepel G, Edwards LJ, Constantinescu CS, (2008) Increased osteopontin levels in the cerebrospinal fluid of patients with multiple sclerosis. Arch Neurol 65: 633-635.
23. Niino M, Kikuchi S, Fukazawa T, Yabe I, Tashiro K, (2003) Genetic polymorphisms of osteopontin in association with multiple sclerosis in Japanese patients. J Neuroimmunol 136: 125-129.
24. Standal T, Borset M, Sundan A, (2004) Role of osteopontin in adhesion, migration, cell survival and bone remodeling. Exp Oncol 26: 179-184.
25. Zohar R, Cheifetz S, McCulloch CA, Sodek J, (1998) Analysis of intracellular osteopontin as a marker of osteoblastic cell differentiation and mesenchymal cell migration. Eur J Oral Sci 106 (Suppl 1): 401-407.
26. Begum MD, Umemura M, Kon S, Yahagi A, Hamada S, et al. (2007) Suppression of the bacterial antigen-specific T cell response and the dendritic cell migration to the lymph nodes by osteopontin. Microbiol Immunol 51: 135-147.
27. O'Regan AW, Hayden JM, Berman JS, (2000) Osteopontin augments CD3-mediated interferon-gamma and CD40 ligand expression by T cells, which results in IL-12 production from peripheral blood mononuclear cells. J Leukoc Biol 68: 495-502.
28. Koguchi Y, Kawakami K, Kon S, Segawa T, Maeda M, et al. (2002) Penicillium marneffei causes osteopontin-mediated production of interleukin-12 by peripheral blood mononuclear cells. Infect Immun 70: 1042-1048.
29. Koguchi Y, Kawakami K, Uezu K, Fukushima K, Kon S, et al. (2003) High plasma osteopontin level and its relationship with interleukin-12-mediated type 1 T helper cell response in tuberculosis. Am J Respir Crit Care Med 167: 1355-1359.
30. Gassler N, Autschbach F, Gauer S, Bohn J, Sido B, et al. (2002) Expression of osteopontin (Eta-1) in Crohn disease of the terminal ileum. Scand J Gastroenterol 37: 1286-1295.
31. Agnholt J, Kelsen J, Schack L, Hvas CL, Dahlerup JF, et al. (2007) Osteopontin, a protein with cytokine-like properties, is associated with inflammation in Crohn's disease. Scand J Immunol 65: 453-460.
32. Gordon JN, MacDonald TT, (2005) Osteopontin: a new addition to the constellation of cytokines which drive T helper cell type 1 responses in Crohn's disease. Gut 54: 1213-1215.
33. Sato T, Nakai T, Tamura N, Okamoto S, Matsuoka K, et al. (2005) Osteopontin/Eta-1 upregulated in Crohn's disease regulates the Th1 immune response. Gut 54: 1254-1262.
34. Mishima R, Takeshima F, Sawai T, Ohba K, Ohnita K, et al. (2007) High plasma osteopontin levels in patients with inflammatory bowel disease. J Clin Gastroenterol 41: 167-172.
35. Masuda H, Takahashi Y, Asai S, Hemmi A, Takayama T, (2005) Osteopontin expression in ulcerative colitis is distinctly different from that in Crohn's disease and diverticulitis. J Gastroenterol 40: 409-413.
36. Masuda H, Takahashi Y, Asai S, Takayama T, (2003) Distinct gene expression of osteopontin in patients with ulcerative colitis. J Surg Res 111: 85-90.
37. da Silva AP, Ellen RP, Sorensen ES, Goldberg HA, Zohar R, et al. (2009) Osteopontin attenuation of dextran sulfate sodium-induced colitis in mice. Lab Invest 89: 1169-1181.
38. Zhong J, Eckhardt ER, Oz HS, Bruemmer D, de Villiers WJ, (2006) Osteopontin deficiency protects mice from Dextran sodium sulfate-induced colitis. Inflamm Bowel Dis 12: 790-796.
39. Heilmann K, Hoffmann U, Witte E, Loddenkemper C, Sina C, et al. (2008) Osteopontin as two-sided mediator of intestinal inflammation. J Cell Mol Med 13: 1162-1174.
40. Barizzone N, Marchini M, Cappiello F, Chiocchetti A, Orilieri E, et al. (2011) Association of osteopontin regulatory polymorphisms with systemic sclerosis. Hum Immunol 72: 930-934.
41. Chiocchetti A, Orilieri E, Cappellano G, Barizzone N, et al. (2010) The osteopontin gene +1239A/C single nucleotide polymorphism is associated with type 1 diabetes mellitus in the Italian population. Int J Immunopathol Pharmacol 23: 263-269.
42. Schmidt-Petersen K, Brand E, Telgmann R, Nicaud V, Hagedorn C, et al. (2009) Osteopontin gene variation and cardio/cerebrovascular disease phenotypes. Atherosclerosis 206: 209-215.
43. Marciano R, D'Annunzio G, Minuto N, Pasquali L, Santamaria A, et al. (2009) Association of alleles at polymorphic sites in the Osteopontin encoding gene in young type 1 diabetic patients. Clin Immunol 131: 84-91.
44. Silverberg MS, Satsangi J, Ahmad T, Arnott ID, Bernstein CN, et al. (2005) Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: Report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol 19 (Suppl A): 5-36.
45. Glas J, Seiderer J, Nagy M, Fries C, Beigel F, et al. (2010) Evidence for STAT4 as a common autoimmune gene: rs7574865 is associated with colonic Crohn's disease and early disease onset. PLoS ONE 5: e10373.
46. Glas J, Seiderer J, Fries C, Tillack C, Pfennig S, et al. (2011) CEACAM6 gene variants in inflammatory bowel disease. PLoS ONE 6: e19319.
47. Glas J, Seiderer J, Tillack C, Pfennig S, Beigel F, et al. (2010) The NOD2 single nucleotide polymorphisms rs2066843 and rs2076756 are novel and common Crohn's disease susceptibility gene variants. PLoS ONE 5: e14466.
48. Glas J, Stallhofer J, Ripke S, Wetzke M, Pfennig S, et al. (2009) Novel genetic risk markers for ulcerative colitis in the IL2/IL21 region are in epistasis with IL23R and suggest a common genetic background for ulcerative colitis and celiac disease. Am J Gastroenterol 104: 1737-1744.
49. Chiocchetti A, Comi C, Indelicato M, Castelli L, Mesturini R, et al. (2005) Osteopontin gene haplotypes correlate with multiple sclerosis development and progression. J Neuroimmunol 163: 172-178.
50. Han S, Guthridge JM, Harley IT, Sestak AL, Kim-Howard X, et al. (2008) Osteopontin and systemic lupus erythematosus association: a probable gene-gender interaction. PLoS One 3: e0001757.
51. Maver A, Medica I, Salobir B, Tercelj M, Peterlin B, (2009) Genetic variation in osteopontin gene is associated with susceptibility to sarcoidosis in Slovenian population. Dis Markers 27: 295-302.
52. Kariuki SN, Moore JG, Kirou KA, Crow MK, Utset TO, et al. (2009) Age- and gender-specific modulation of serum osteopontin and interferon-alpha by osteopontin genotype in systemic lupus erythematosus. Genes Immun 10: 487-494.
53. Forton AC, Petri MA, Goldman D, Sullivan KE, (2002) An osteopontin (SPP1) polymorphism is associated with systemic lupus erythematosus. Hum Mutat 19: 459.
54. Seiderer J, Elben I, Diegelmann J, Glas J, Stallhofer J, et al. (2007) Role of the novel Th17 cytokine IL-17F in inflammatory bowel disease (IBD): Upregulated colonic IL-17F expression in active crohn's disease and analysis of the IL17F p.His161Arg polymorphism in IBD. Inflamm Bowel Dis 14: 437-445.
55. Schmechel S, Konrad A, Diegelmann J, Glas J, Wetzke M, et al. (2008) Linking genetic susceptibility to Crohn's disease with Th17 cell function: IL-22 serum levels are increased in Crohn's disease and correlate with disease activity and IL23R genotype status. Inflamm Bowel Dis 14: 204-212.
56. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, et al. (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 42: 1118-1125.
57. Anderson CA, Boucher G, Lees CW, Franke A, D'Amato M, et al. (2011) Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 43: 246-252.
58. Glas J, Seiderer J, Fischer D, Tengler B, Pfennig S, et al. (2011) Pregnane X receptor (PXR/NR1I2) gene haplotypes modulate susceptibility to inflammatory bowel disease. Inflamm Bowel Dis 17: 1917-1924.
59. D'Alfonso S, Barizzone N, Giordano M, Chiocchetti A, Magnani C, et al. (2005) Two single-nucleotide polymorphisms in the 5′ and 3′ ends of the osteopontin gene contribute to susceptibility to systemic lupus erythematosus. Arthritis Rheum 52: 539-547.
60. Xu AP, Bai J, Lu J, Liang YY, Li JG, et al. (2007) Osteopontin gene polymorphism in association with systemic lupus erythematosus in Chinese patients. Chin Med J (Engl) 120: 2124-2128.
61. Marciano R, Giacopelli F, Divizia MT, Gattorno M, Felici E, et al. (2006) A polymorphic variant inside the osteopontin gene shows association with disease course in oligoarticular juvenile idiopathic arthritis. Ann Rheum Dis 65: 662-665.
62. Hensiek AE, Roxburgh R, Meranian M, Seaman S, Yeo T, et al. (2003) Osteopontin gene and clinical severity of multiple sclerosis. J Neurol 250: 943-947.
63. Mas A, Martinez A, de las Heras V, Bartolome M, de la Concha EG, et al. (2007) The 795CT polymorphism in osteopontin gene is not associated with multiple sclerosis in a Spanish population. Mult Scler 13: 250-252.
64. Urcelay E, Martinez A, Mas-Fontao A, Peris-Pertusa A, Pascual-Salcedo D, et al. (2005) Osteopontin gene polymorphisms in Spanish patients with rheumatoid arthritis. J Rheumatol 32: 405-409.
65. Brand S, Beigel F, Olszak T, Zitzmann K, Eichhorst ST, et al. (2006) IL-22 is increased in active Crohn's disease and promotes proinflammatory gene expression and intestinal epithelial cell migration. Am J Physiol Gastrointest Liver Physiol 290: G827-838.
66. Sugimoto K, Ogawa A, Mizoguchi E, Shimomura Y, Andoh A, et al. (2008) IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 118: 534-544.
67. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, et al. (2008) Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 29: 947-957.
68. Brand S, Dambacher J, Beigel F, Zitzmann K, Heeg MH, et al. (2007) IL-22-mediated liver cell regeneration is abrogated by SOCS-1/3 overexpression in vitro. Am J Physiol Gastrointest Liver Physiol 292: G1019-1028.
69. Aujla SJ, Chan YR, Zheng M, Fei M, Askew DJ, et al. (2008) IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 14: 275-281.
70. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, et al. (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14: 282-289.
71. Liaw L, Birk DE, Ballas CB, Whitsitt JS, Davidson JM, et al. (1998) Altered wound healing in mice lacking a functional osteopontin gene (spp1). J Clin Invest 101: 1468-1478.
72. Chen G, Zhang X, Li R, Fang L, Niu X, et al. (2010) Role of osteopontin in synovial Th17 differentiation in rheumatoid arthritis. Arthritis Rheum 62: 2900-2908.
73. Shinohara ML, Kim JH, Garcia VA, Cantor H, (2008) Engagement of the type I interferon receptor on dendritic cells inhibits T helper 17 cell development: role of intracellular osteopontin. Immunity 29: 68-78.
74. Murugaiyan G, Mittal A, Weiner HL, (2010) Identification of an IL-27/osteopontin axis in dendritic cells and its modulation by IFN-gamma limits IL-17-mediated autoimmune inflammation. Proc Natl Acad Sci U S A 107: 11495-11500.
75. Murugaiyan G, Mittal A, Lopez-Diego R, Maier LM, Anderson DE, et al. (2009) IL-27 is a key regulator of IL-10 and IL-17 production by human CD4+ T cells. J Immunol 183: 2435-2443.
76. Diegelmann J, Olszak T, Göke B, Blumberg RS, Brand S, (2011) A novel role for IL-27 as mediator of intestinal epithelial barrier protection mediated via differential STAT signaling and induction of antibacterial and anti-inflammatory proteins. J Biol Chem Nov 8. [Epub ahead of print].