Fucosylation Deficiency in Mice Leads to Colitis and Adenocarcinoma

Gastroenterology

Volumn 152, Issue 1, 2017, Pages 193-205.e10

  Wang, Yiwei ^a   Huang, Dan ^a   Chen, Kai Yuan ^c   Cui, Min ^a   Wang, Weihuan ^a   Huang, Xiaoran ^a   Awadellah, Amad ^d   Li, Qing ^d   Friedman, Ann ^e   Xin, William W ^f   Di Martino, Luca ^d   Cominelli, Fabio ^d   Miron, Alex ^a   Chan, Ricky ^b   Fox, James G ^g   Xu, Yan ^h   Shen, Xiling ^c   Kalady, Mathew F ⁱ   Markowitz, Sanford ^a   Maillard, Ivan ^e   Lowe, John B ^j   Xin, Wei ^a,d   Zhou, Lan ^a,d   more..

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c Cornell University   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^h CLEVELAND STATE UNIVERSITY   (United States)

ⁱ LERNER RESEARCH INSTITUTE   (United States)

^j GENENTECH INC   (United States)

more..

Author keywords

Colon Cancer; Metabolism; Signal Transduction; Tumorigenesis

Indexed keywords

COLONY STIMULATING FACTOR 1; COMPLEMENT COMPONENT C5A; CYCLOOXYGENASE 2; EPIMERASE; FLUORESCEIN ISOTHIOCYANATE; GAMMA INTERFERON; GUANOSINE DIPHOSPHATE 4 KETO 6 DEOXYMANNOSE 3,5 EPIMERASE; GUANOSINE DIPHOSPHATE FUCOSE; GUANOSINE DIPHOSPHATE MANNOSE 4,6 DEHYDRATASE; HYDROLYASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MUTL PROTEIN HOMOLOG 1; NOTCH RECEPTOR; RNA 16S; TUMOR NECROSIS FACTOR; TWIST RELATED PROTEIN 1; UNCLASSIFIED DRUG; CYTOKINE; FUCOSE; HES1 PROTEIN, MOUSE; MESSENGER RNA; NOTCH1 PROTEIN, MOUSE; NOTCH1 RECEPTOR; NOTCH2 PROTEIN, MOUSE; NOTCH2 RECEPTOR; OXIDOREDUCTASE; TRANSCRIPTION FACTOR HES 1; TSTA3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CECUM; COLITIS; COLON ADENOCARCINOMA; COLON CARCINOGENESIS; COLON MUCOSA; COLON TISSUE; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DYSPLASIA; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; FECES ANALYSIS; FUCOSYLATION; GENE DELETION; GENE LOSS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECTUM ADENOMA; RNA SEQUENCE; ADENOCARCINOMA; ADULT; AGED; ANIMAL; BIOSYNTHESIS; CARCINOGENESIS; CELL PROLIFERATION; CHEMISTRY; COLON; COLONIC NEOPLASMS; DEFICIENCY; FECES; FEMALE; GENETICS; INTESTINE FLORA; INTESTINE MUCOSA; KNOCKOUT MOUSE; MALE; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PATHOLOGY; PERMEABILITY; SIGNAL TRANSDUCTION; VERY ELDERLY; YOUNG ADULT;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BONE MARROW TRANSPLANTATION; CARBOHYDRATE EPIMERASES; CARCINOGENESIS; CECUM; CELL PROLIFERATION; COLITIS; COLON; COLONIC NEOPLASMS; CYTOKINES; FECES; FEMALE; FUCOSE; GASTROINTESTINAL MICROBIOME; GUANOSINE DIPHOSPHATE FUCOSE; HUMANS; INTESTINAL MUCOSA; KETONE OXIDOREDUCTASES; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; PERMEABILITY; RECEPTOR, NOTCH1; RECEPTOR, NOTCH2; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR HES-1; YOUNG ADULT;

EID: 85006314838     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2016.09.004     Document Type: Article

References (55)

1. 1 Becker, D.J., Lowe, J.B., Fucose: biosynthesis and biological function in mammals. Glycobiology 13 (2003), 41R–53R.
2. 2 Miyoshi, E., Moriwaki, K., Nakagawa, T., Biological function of fucosylation in cancer biology. J Biochem 143 (2008), 725–729.
3. 3 Tonetti, M., Sturla, L., Bisso, A., et al. Synthesis of GDP-L-fucose by the human FX protein. J Biol Chem 271 (1996), 27274–27279.
4. 4 Ohyama, C., Smith, P.L., Angata, K., et al. Molecular cloning and expression of GDP-D-mannose-4,6-dehydratase, a key enzyme for fucose metabolism defective in Lec13 cells. J Biol Chem 273 (1998), 14582–14587.
5. 5 Larsen, R.D., Ernst, L.K., Nair, R.P., et al. Molecular cloning, sequence, and expression of a human GDP-L-fucose:beta-D-galactoside 2-alpha-L-fucosyltransferase cDNA that can form the H blood group antigen. Proc Natl Acad Sci U S A 87 (1990), 6674–6678.
6. 6 Kelly, R.J., Ernst, L.K., Larsen, R.D., et al. Molecular basis for H blood group deficiency in Bombay (Oh) and para-Bombay individuals. Proc Natl Acad Sci U S A 91 (1994), 5843–5847.
7. 7 Lowe, J.B., Selectin ligands, leukocyte trafficking, and fucosyltransferase genes. Kidney Int 51 (1997), 1418–1426.
8. 8 Hooper, L.V., Gordon, J.I., Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology 11 (2001), 1R–10R.
9. 9 Wang, Y., Shao, L., Shi, S., et al. Modification of epidermal growth factor-like repeats with O-fucose. Molecular cloning and expression of a novel GDP-fucose protein O-fucosyltransferase. J Biol Chem 276 (2001), 40338–40345.
10. 10 De Strooper, B., Annaert, W., Cupers, P., et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398 (1999), 518–522.
11. 11 Jeffries, S., Robbins, D.J., Capobianco, A.J., Characterization of a high-molecular-weight Notch complex in the nucleus of Notch(ic)-transformed RKE cells and in a human T-cell leukemia cell line. Mol Cell Biol 22 (2002), 3927–3941.
12. 12 Koch, U., Lacombe, T.A., Holland, D., et al. Subversion of the T/B lineage decision in the thymus by lunatic fringe-mediated inhibition of Notch-1. Immunity 15 (2001), 225–236.
13. 13 Visan, I., Tan, J.B., Yuan, J.S., et al. Regulation of T lymphopoiesis by Notch1 and Lunatic fringe-mediated competition for intrathymic niches. Nat Immunol 7 (2006), 634–643.
14. 14 Lu, L., Stanley, P., Roles of O-fucose glycans in notch signaling revealed by mutant mice. Methods Enzymol 417 (2006), 127–136.
15. 15 Zhou, L., Li, L.W., Yan, Q., et al. Notch-dependent control of myelopoiesis is regulated by fucosylation. Blood 112 (2008), 308–319.
16. 16 Yao, D., Huang, Y., Huang, X., et al. Protein O-fucosyltransferase 1 (Pofut1) regulates lymphoid and myeloid homeostasis through modulation of Notch receptor ligand interactions. Blood 117 (2011), 5652–5662.
17. 17 van Es, J.H., van Gijn, M.E., Riccio, O., et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435 (2005), 959–963.
18. 18 Fre, S., Huyghe, M., Mourikis, P., et al. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435 (2005), 964–968.
19. 19 Qiao, L., Wong, B.C., Role of Notch signaling in colorectal cancer. Carcinogenesis 30 (2009), 1979–1986.
20. 20 Moriwaki, K., Miyoshi, E., Fucosylation and gastrointestinal cancer. World J Hepatol 2 (2010), 151–161.
21. 21 Aoyagi, Y., Isemura, M., Suzuki, Y., et al. Fucosylated alpha-fetoprotein as marker of early hepatocellular carcinoma. Lancet 2 (1985), 1353–1354.
22. 22 Moriwaki, K., Noda, K., Furukawa, Y., et al. Deficiency of GMDS leads to escape from NK cell-mediated tumor surveillance through modulation of TRAIL signaling. Gastroenterology 137 (2009), 188–198 198 e1-2.
23. 23 Nakayama, K., Moriwaki, K., Imai, T., et al. Mutation of GDP-mannose-4,6-dehydratase in colorectal cancer metastasis. PLoS One, 8, 2013, e70298.
24. 24 Cancer Genome Atlas Network, Comprehensive molecular characterization of human colon and rectal cancer. Nature 487 (2012), 330–337.
25. 25 Smith, P.L., Myers, J.T., Rogers, C.E., et al. Conditional control of selectin ligand expression and global fucosylation events in mice with a targeted mutation at the FX locus. J Cell Biol 158 (2002), 801–815.
26. 26 Kostomitsopoulos, N., Donnelly, H., Kostavasili, I., et al. Eradication of Helicobacter bilis and H. hepaticus from infected mice by using a medicated diet. Lab Anim (NY) 36 (2007), 37–40.
27. 27 Waterhouse, C.C., Johnson, S., Phillipson, M., et al. Secretory cell hyperplasia and defects in Notch activity in a mouse model of leukocyte adhesion deficiency type II. Gastroenterology, 138, 2010 1079–1090 e1-5.
28. 28 Rex, D.K., Ahnen, D.J., Baron, J.A., et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 107 (2012), 1315–1329 quiz 1314, 1330.
29. 29 Batts, K.P., The pathology of serrated colorectal neoplasia: practical answers for common questions. Mod Pathol 28:Suppl 1 (2015), S80–S87.
30. 30 Eaden, J.A., Abrams, K.R., Mayberry, J.F., The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48 (2001), 526–535.
31. 31 Beaugerie, L., Svrcek, M., Seksik, P., et al. Risk of colorectal high-grade dysplasia and cancer in a prospective observational cohort of patients with inflammatory bowel disease. Gastroenterology 145 (2013), 166–175 e8.
32. 32 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.
33. 33 Ward, J.M., Anver, M.R., Haines, D.C., et al. Inflammatory large bowel disease in immunodeficient mice naturally infected with Helicobacter hepaticus. Lab Anim Sci 46 (1996), 15–20.
34. 34 Foltz, C.J., Fox, J.G., Cahill, R., et al. Spontaneous inflammatory bowel disease in multiple mutant mouse lines: association with colonization by Helicobacter hepaticus. Helicobacter 3 (1998), 69–78.
35. 35 Cui, M., Awadallah, A., Liu, W., et al. Loss of Hes1 differentiates sessile serrated adenoma/polyp from hyperplastic polyp. Am J Surg Pathol 40 (2016), 113–119.
36. 36 Iacucci, M., Hassan, C., Fort Gasia, M., et al. Serrated adenoma prevalence in inflammatory bowel disease surveillance colonoscopy, and characteristics revealed by chromoendoscopy and virtual chromoendoscopy. Can J Gastroenterol Hepatol 28 (2014), 589–594.
37. 37 Szylberg, L., Janiczek, M., Popiel, A., et al. Expression of COX-2, IL-1beta, TNF-alpha and IL-4 in epithelium of serrated adenoma, adenoma and hyperplastic polyp. Arch Med Sci 12 (2016), 172–178.
38. 38 Kiedrowski, M., Mroz, A., Kraszewska, E., et al. Cyclooxygenase-2 immunohistochemical expression in serrated polyps of the colon. Contemp Oncol (Pozn) 18 (2014), 409–413.
39. 39 Bongers, G., Pacer, M.E., Geraldino, T.H., et al. Interplay of host microbiota, genetic perturbations, and inflammation promotes local development of intestinal neoplasms in mice. J Exp Med 211 (2014), 457–472.
40. 40 Matkowskyj, K.A., Chen, Z.E., Rao, M.S., et al. Dysplastic lesions in inflammatory bowel disease: molecular pathogenesis to morphology. Arch Pathol Lab Med 137 (2013), 338–350.
41. 41 Jensen, J., Pedersen, E.E., Galante, P., et al. Control of endodermal endocrine development by Hes-1. Nat Genet 24 (2000), 36–44.
42. 42 Ueo, T., Imayoshi, I., Kobayashi, T., et al. The role of Hes genes in intestinal development, homeostasis and tumor formation. Development 139 (2012), 1071–1082.
43. 43 Pickard, J.M., Chervonsky, A.V., Intestinal fucose as a mediator of host-microbe symbiosis. J Immunol 194 (2015), 5588–5593.
44. 44 Goto, Y., Obata, T., Kunisawa, J., et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science, 345, 2014, 1254009.
45. 45 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 108 (2011), 19030–19035.
46. 1 Chan, E.R., Menard, D., David, P.H., et al. Whole genome sequencing of field isolates provides robust characterization of genetic diversity in Plasmodium vivax. PLoS Negl Trop Dis, 6, 2012 e1811.
47. 2 Nawrocki, E.P., Eddy, S.R., Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29 (2013), 2933–2935.
48. 3 Price, M.N., Dehal, P.S., Arkin, A.P., FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26 (2009), 1641–1650.
49. 4 Langfelder, P., Horvath, S., WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 2008, 559.
50. 5 Wang, Q., Garrity, G.M., Tiedje, J.M., et al. Native Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73 (2007), 5261–5267.
51. 6 Cole, J.R., Wang, Q., Fish, J.A., et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42 (2014), D633–642.
52. 7 Kodani, T., Rodriguez-Palacios, A., Corridoni, D., et al. Flexible colonoscopy in mice to evaluate the severity of colitis and colorectal tumors using a validated endoscopic scoring system. J Vis Exp(80), 2013, e50843 http://dx.doi.org/10.3791/50843.
53. 8 Ge, Z., White, D.A., Whary, M.T., et al. Fluorogenic PCR-based quantitative detection of a murine pathogen, Helicobacter hepaticus. J Clin Microbiol 39 (2001), 2598–2602.
54. 9 Wang, W., Yu, S., Zimmerman, G., et al. Notch receptor-ligand engagement maintains hematopoietic stem cell quiescence and niche retention. Stem Cells 33 (2015), 2280–2293.
55. 10 Grady, W.M., Rajput, A., Lutterbaugh, J.D., et al. Detection of aberrantly methylated hMLH1 promoter DNA in the serum of patients with microsatellite unstable colon cancer. Cancer Res 61 (2001), 900–902.