Defective Intestinal Mucin-Type O-Glycosylation Causes Spontaneous Colitis-Associated Cancer in Mice

Gastroenterology

Volumn 151, Issue 1, 2016, Pages 152-164.e11

  Bergstrom, Kirk ^a   Liu, Xiaowei ^b   Zhao, Yiming ^a,c   Gao, Nan ^a,c   Wu, Qian ^a,d   Song, Kai ^a   Cui, Yi ^a   Li, Yun ^a,c   McDaniel, J Michael ^a   McGee, Samuel ^a   Chen, Weichang ^c   Huycke, Mark M ^e,f   Houchen, Courtney W ^f   Zenewicz, Lauren A ^f   West, Christopher M ^f   Chen, Hong ^a   Braun, Jonathan ^g   Fu, Jianxin ^a,c   Xia, Lijun ^a,c,f  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^d FUDAN UNIVERSITY   (China)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mouse Model; Mucin Type O Glycans; Mucus Barrier; Ulcerative Colitis

Indexed keywords

ANTIBIOTIC AGENT; CASPASE 11; GLYCAN; INTERLEUKIN 1BETA CONVERTING ENZYME; MUCIN; TN ANTIGEN; POLYSACCHARIDE; TUMOR ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DIAGNOSTIC IMAGING; ENZYME LINKED IMMUNOSORBENT ASSAY; HYPERPLASIA; IMMUNOBLOTTING; INFLAMMATORY INFILTRATE; INTESTINAL TISSUE; INTESTINE EPITHELIUM; INTESTINE FLORA; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; QUANTITATIVE ANALYSIS; ULCERATIVE COLITIS; ANIMAL; CHEMICALLY INDUCED; COLITIS; COLORECTAL NEOPLASMS; COMPLICATION; GLYCOSYLATION; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; COLITIS; COLORECTAL NEOPLASMS; GASTROINTESTINAL MICROBIOME; GLYCOSYLATION; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; MUCINS; POLYSACCHARIDES;

EID: 84990053233     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2016.03.039     Document Type: Article

References (48)

1. 1 Fearon, E.R., Vogelstein, B., A genetic model for colorectal tumorigenesis. Cell 61 (1990), 759–767.
2. 2 Ullman, T.A., Itzkowitz, S.H., Intestinal inflammation and cancer. Gastroenterology 140 (2011), 1807–1816.e1.
3. 3 Saleh, M., Trinchieri, G., Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat Rev Immunol 11 (2011), 9–20.
4. 4 Garrett, W.S., Punit, S., Gallini, C.A., et al. Colitis-associated colorectal cancer driven by T-bet deficiency in dendritic cells. Cancer Cell 16 (2009), 208–219.
5. 5 Van der Sluis, M., De Koning, B.A., De Bruijn, A.C., et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131 (2006), 117–129.
6. 6 Johansson, M.E., Phillipson, M., Petersson, J., et al. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105 (2008), 15064–15069.
7. 7 An, G., Wei, B., Xia, B., et al. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med 204 (2007), 1417–1429.
8. 8 Fu, J., Wei, B., Wen, T., et al. Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice. J Clin Invest 121 (2011), 1657–1666.
9. 9 Ju, T., Cummings, R.D., A unique molecular chaperone Cosmc required for activity of the mammalian core 1 beta 3-galactosyltransferase. Proc Natl Acad Sci U S A 2013 99 (2002), 16613–16618.
10. 10 Larsson, J.M.H., Karlsson, H., Crespo, J.G., et al. Altered O-glycosylation profile of MUC2 mucin occurs in active ulcerative colitis and is associated with increased inflammation. Inflamm Bowel Dis 17 (2011), 2299–2307.
11. 11 Itzkowitz, S.H., Young, E., Dubois, D., et al. Sialosyl-Tn antigen is prevalent and precedes dysplasia in ulcerative colitis: a retrospective case-control study. Gastroenterology 110 (1996), 694–704.
12. 12 Springer, G.F., T and Tn, general carcinoma autoantigens. Science 224 (1984), 1198–1206.
13. 13 Monteleone, G., Trapasso, F., Parrello, T., et al. Bioactive IL-18 expression is up-regulated in Crohn's disease. J Immunol 163 (1999), 143–147.
14. 14 Liu, J.J., Davis, E.M., Wine, E., et al. Epithelial cell extrusion leads to breaches in the intestinal epithelium. Inflamm Bowel Dis 19 (2013), 912–921.
15. 15 Zaki, M.H., Lamkanfi, M., Kanneganti, T.-D., Inflammasomes and intestinal tumorigenesis. Drug Discov Today Dis Mech 8 (2011), e71–e78.
16. 16 Lamkanfi, M., Dixit, V.M., Mechanisms and functions of inflammasomes. Cell 157 (2014), 1013–1022.
17. 17 Kayagaki, N., Warming, S., Lamkanfi, M., et al. Non-canonical inflammasome activation targets caspase-11. Nature 479 (2011), 117–121.
18. 18 Demon, D., Kuchmiy, A., Fossoul, A., et al. Caspase-11 is expressed in the colonic mucosa and protects against dextran sodium sulfate-induced colitis. Mucosal Immunol 7 (2014), 1480–1491.
19. 19 Dupaul-Chicoine, J., Yeretssian, G., Doiron, K., et al. Control of intestinal homeostasis, colitis, and colitis-associated colorectal cancer by the inflammatory caspases. Immunity 32 (2010), 367–378.
20. 20 Gill, D.J., Min, K., Chia, J., et al. Initiation of GalNAc-type O-glycosylation in the endoplasmic reticulum promotes cancer cell invasiveness. Proc Natl Acad Sci U S A 110 (2013), E3152–E3161.
21. 21 Radhakrishnan, P., Dabelsteen, S., Madsen, F.B., et al. Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proc Natl Acad Sci U S A 111 (2014), E4066–E4075.
22. 22 Jamieson, T., Clarke, M., Steele, C.W., et al. Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J Clin Invest 122 (2012), 3127–3144.
23. 23 Shaked, H., Hofseth, L.J., Chumanevich, A., et al. Chronic epithelial NF-κβ activation accelerates APC loss and intestinal tumor initiation through iNOS up-regulation. Proc Natl Acad Sci U S A 109 (2012), 14007–14012.
24. 24 Arthur, J.C., Perez-Chanona, E., Mühlbauer, M., et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338 (2012), 120–123.
25. 25 Man, S.M., Zhu, Q., Zhu, L., Liu, Z., et al. Critical role for the DNA sensor AIM2 in stem cell proliferation and cancer. Cell 162 (2015), 45–58.
26. 26 Wlodarska, M., Thaiss, C.A., Nowarski, R., et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 156 (2014), 1045–1059.
27. 27 Leach, S.T., Messina, I., Lemberg, D.A., et al. Local and systemic interleukin-18 and interleukin-18-binding protein in children with inflammatory bowel disease. Inflamm Bowel Dis 14 (2008), 68–74.
28. 28 Andus, T., Daig, R., Vogl, D., et al. Imbalance of the interleukin 1 system in colonic mucosa–association with intestinal inflammation and interleukin 1 receptor antagonist [corrected] genotype 2. Gut 41 (1997), 651–657.
29. 29 Iwai, T., Kudo, T., Kawamoto, R., et al. Core 3 synthase is down-regulated in colon carcinoma and profoundly suppresses the metastatic potential of carcinoma cells. Proc Natl Acad Sci U S A 102 (2005), 4572–4577.
30. 30 Itzkowitz, S.H., Marshall, A., Kornbluth, A., et al. Sialosyl-Tn antigen: initial report of a new marker of malignant progression in long-standing ulcerative colitis. Gastroenterology 109 (1995), 490–497.
31. 31 Zaki, M.H., Boyd, K.L., Vogel, P., et al. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32 (2010), 379–391.
32. 32 Hu, B., Elinav, E., Huber, S., et al. Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4. Proc Natl Acad Sci U S A 107 (2010), 21635–21640.
33. 33 Aguilera, M., Darby, T., Melgar, S., The complex role of inflammasomes in the pathogenesis of inflammatory bowel diseases - lessons learned from experimental models. Cytokine Growth Factor Rev 25 (2014), 715–730.
34. 34 Siegmund, B., Lehr, H.A., Fantuzzi, G., et al. IL-1 beta-converting enzyme (caspase-1) in intestinal inflammation. Proc Natl Acad Sci U S A 98 (2001), 13249–13254.
35. 35 Zhang, J., Fu, S., Sun, S., et al. Inflammasome activation has an important role in the development of spontaneous colitis. Mucosal Immunol 7 (2014), 1139–1150.
36. 36 Coccia, M., Harrison, O.J., Schiering, C., et al. IL-1beta mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J Exp Med 209 (2012), 1595–1609.
37. 37 Ikuta, T., Kobayashi, Y., Kitazawa, M., et al. ASC-associated inflammation promotes cecal tumorigenesis in aryl hydrocarbon receptor-deficient mice. Carcinogenesis 34 (2013), 1620–1627.
38. 38 Huber, S., Gagliani, N., Zenewicz, L.A., et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491 (2012), 259–263.
39. 39 Berg, D.J., Davidson, N., Kuhn, R., et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest 98 (1996), 1010–1020.
40. 40 Rudolph, U., Finegold, M.J., Rich, S.S., et al. Ulcerative colitis and adenocarcinoma of the colon in G alpha i2-deficient mice. Nat Genet 10 (1995), 143–150.
41. 41 Erdman, S.E., Rao, V.P., Poutahidis, T., et al. Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc Natl Acad Sci U S A 106 (2009), 1027–1032.
42. 42 Neufert, C., Becker, C., Neurath, M.F., An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protoc 2 (2007), 1998–2004.
43. 1 Fu, J., Wei, B., Wen, T., et al. Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice. J Clin Invest 121 (2011), 1657–1666.
44. 2 Heazlewood, C.K., Cook, M.C., Eri, R., et al. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med, 5, 2008, e54.
45. 3 Fu, J., Gerhardt, H., McDaniel, J.M., et al. Endothelial cell O-glycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice. J Clin Invest 118 (2008), 3725–3737.
46. 4 Huang, Y., Mechref, Y., Novotny, M.V., Microscale nonreductive release of O-linked glycans for subsequent analysis through MALDI mass spectrometry and capillary electrophoresis. Anal Chem 73 (2001), 6063–6069.
47. 5 Bigge, J.C., Patel, T.P., Bruce, J.A., et al. Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid. Anal Biochem 230 (1995), 229–238.
48. 6 Kang, P., Mechref, Y., Klouckova, I., et al. Solid-phase permethylation of glycans for mass spectrometric analysis. Rapid Commun Mass Spectrom 19 (2005), 3421–3428.