Glycoprotein A33 deficiency: A new mouse model of impaired intestinal epithelial barrier function and inflammatory disease

DMM Disease Models and Mechanisms

Volumn 8, Issue 8, 2015, Pages 805-815

  Williams, Benjamin B ^a,b,c   Tebbutt, Niall C ^c,f,g   Buchert, Michael ^a,b,c,f,g   Putoczki, Tracy L ^a,b,c   Doggett, Karen ^a,b   Bao, Shisan ^d   Johnstone, Cameron N ^c,e   Masson, Frederick ^a,b,f,g   Hollande, Frederic ^b   Burgess, Antony W ^a,b,c   Scott, Andrew M ^c,f,g   Ernst, Matthias ^a,b,c,f,g   Heath, Joan K ^a,b,c  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e PETER MACCALLUM CANCER CENTRE   (Australia)

^f OLIVIA NEWTON JOHN CANCER RESEARCH INSTITUTE   (Australia)

^g LA TROBE UNIVERSITY   (Australia)

Author keywords

Colitis; Colorectal cancer; GPA33; Intestinal permeability; Oral tolerance

Indexed keywords

GLYCOPROTEIN; GLYCOPROTEIN A33; UNCLASSIFIED DRUG; ANTIGEN; DEXTRAN SULFATE; GPA33 PROTEIN, MOUSE; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SUSCEPTIBILITY; CARCINOGENESIS; COLITIS; COLITIS ASSOCIATED CANCER; FOOD ALLERGY; IMMUNOSURVEILLANCE; INTESTINE EPITHELIUM; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLORECTAL NEOPLASMS; COMPLICATION; DEFICIENCY; DISEASE MODEL; DISEASE PREDISPOSITION; FOOD; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASE; INTESTINE MUCOSA; METABOLISM; PATHOLOGY;

MUS;

ANIMALS; ANTIGENS; COLITIS; COLORECTAL NEOPLASMS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FOOD; IMMUNE TOLERANCE; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL;

EID: 84939528417     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.019935     Document Type: Article

References (56)

1. Ackerman, M. E. , Chalouni, C. , Schmidt, M. M. , Raman, V. V. , Ritter, G. , Old, L. J. , Mellman, I. and Wittrup, K. D. (2008). A33 antigen displays persistent surface expression. Cancer Immunol. Immunother. 57, 1017-1027.
2. Becker, C. , Dornhoff, H. , Neufert, C. , Fantini, M. C. , Wirtz, S. , Huebner, S. , Nikolaev, A. , Lehr, H.-A. , Murphy, A. J. , Valenzuela, D. M. et al. (2006). Cutting edge: IL-23 cross-regulates IL-12 production in T cell-dependent experimental colitis. J. Immunol. 177, 2760-2764.
3. Brandl, K. , Rutschmann, S. , Li, X. , Du, X. , Xiao, N. , Schnabl, B. , Brenner, D. A. and Beutler, B. (2009). Enhanced sensitivity to DSS colitis caused by a hypomorphic Mbtps1 mutation disrupting the ATF6-driven unfolded protein response. Proc. Natl. Acad. Sci. USA 106, 3300-3305.
4. Chrétien, I. , Marcuz, A. , Courtet, M. , Katevuo, K. , Vainio, O. , Heath, J. K. , White, S. J. and Du Pasquier, L. (1998). CTX, a Xenopus thymocyte receptor, defines a molecular family conserved throughout vertebrates. Eur. J. Immunol. 28, 4094-4104.
5. Ciprotti, M. , Chong, G. , Gan, H. K. , Chan, A. , Murone, C. , MacGregor, D. , Lee, F.-T. , Johns, T. G. , Heath, J. K. , Ernst, M. et al. (2014). Quantitative intratumoural microdistribution and kinetics of (131)I-huA33 antibody in patients with colorectal carcinoma. EJNMMI Res. 4, 22.
6. Eaden, J. A. , Abrams, K. R. and Mayberry, J. F. (2001). The risk of colorectal cancer in ulcerative colitis: A meta-analysis. Gut 48, 526-535.
7. Ernst, M. , Preaudet, A. and Putoczki, T. (2015). Non-invasive assessment of the efficacy of new therapeutics for intestinal pathologies using serial endoscopic imaging of live mice. J. Vis. Exp. , e52383.
8. Ewert, P. , Aguilera, S. , Alliende, C. , Kwon, Y.-J. , Albornoz, A. , Molina, C. , Urzúa, U. , Quest, A. F. G. , Olea, N. , Pérez, P. et al. (2010). Disruption of tight junction structure in salivary glands from Sjögren's syndrome patients is linked to proinflammatory cytokine exposure. Arthritis Rheum. 62, 1280-1289.
9. Fries, W. , Belvedere, A. and Vetrano, S. (2013). Sealing the broken barrier in IBD: Intestinal permeability, epithelial cells and junctions. Curr. Drug Targets 14, 1460-1470.
10. Garinchesa, P. , Sakamoto, J. , Welt, S. , Real, F. , Rettig, W. and Old, L. (1996). Organ-specific expression of the colon cancer antigen A33, a cell surface target for antibody-based therapy. Int. J. Oncol. 9, 465-471.
11. Heath, J. K. , White, S. J. , Johnstone, C. N. , Catimel, B. , Simpson, R. J. , Moritz, R. L. , Tu, G.-F. , Ji, H. , Whitehead, R. H. , Groenen, L. C. et al. (1997). The human A33 antigen is a transmembrane glycoprotein and a novel member of the immunoglobulin superfamily. Proc. Natl. Acad. Sci. USA 94, 469-474.
12. Heller, F. , Florian, P. , Bojarski, C. , Richter, J. , Christ, M. , Hillenbrand, B. , Mankertz, J. , Gitter, A. H. , Bürgel, N. , Fromm, M. et al. (2005). Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129, 550-564.
13. Hermiston, M. L. and Gordon, J. I. (1995). Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270, 1203-1207.
14. Infante, J. R. , Bendell, J. C. , Goff, L. W. , Jones, S. F. , Chan, E. , Sudo, T. , Burris, H. A. and Berlin, J. D. (2013). Safety, pharmacokinetics and pharmacodynamics of the anti-A33 fully-human monoclonal antibody, KRN330, in patients with advanced colorectal cancer. Eur. J. Cancer 49, 1169-1175.
15. Itzkowitz, S. H. and Yio, X. (2004). Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: The role of inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G7-G17.
16. Johansson, M. E. V. , Gustafsson, J. K. , Sjöberg, K. E. , Petersson, J. , Holm, L. , Sjövall, H. and Hansson, G. C. (2010). Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS ONE 5, e12238.
17. Johnstone, C. N. , Tebbutt, N. C. , Abud, H. E. , White, S. J. , Stenvers, K. L. , Hall, N. E. , Cody, S. H. , Whitehead, R. H. , Catimel, B. , Nice, E. C. et al. (2000). Characterization of mouse A33 antigen, a definitive marker for basolateral surfaces of intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G500-G510.
18. Johnstone, C. N. , White, S. J. , Tebbutt, N. C. , Clay, F. J. , Ernst, M. , Biggs, W. H. , Viars, C. S. , Czekay, S. , Arden, K. C. and Heath, J. K. (2002). Analysis of the regulation of the A33 antigen gene reveals intestine-specific mechanisms of gene expression. J. Biol. Chem. 277, 34531-34539.
19. Kim, E. R. and Chang, D. K. (2014). Colorectal cancer in inflammatory bowel disease: The risk, pathogenesis, prevention and diagnosis. World J. Gastroenterol. 20, 9872-9881.
20. Kim, E. R. and Kim, Y.-H. (2014). Clinical application of genetics in management of colorectal cancer. Intest. Res. 12, 184-193.
21. Kitajima, S. , Takuma, S. and Morimoto, M. (1999). Changes in colonic mucosal permeability in mouse colitis induced with dextran sulfate sodium. Exp. Anim. 48, 137-143.
22. Kraus, T. A. , Toy, L. , Chan, L. , Childs, J. and Mayer, L. (2004). Failure to induce oral tolerance to a soluble protein in patients with inflammatory bowel disease. Gastroenterology 126, 1771-1778.
23. Laukoetter, M. G. , Nava, P. , Lee, W. Y. , Severson, E. A. , Capaldo, C. T. , Babbin, B. A. , Williams, I. R. , Koval, M. , Peatman, E. , Campbell, J. A. et al. (2007). JAMA regulates permeability and inflammation in the intestine in vivo. J. Exp. Med. 204, 3067-3076.
24. Mallegol, J. , van Niel, G. and Heyman, M. (2005). Phenotypic and functional characterization of intestinal epithelial exosomes. Blood Cells Mol. Dis. 35, 11-16.
25. Mallegol, J. , Van Niel, G. , Lebreton, C. , Lepelletier, Y. , Candalh, C. , Dugave, C. , Heath, J. K. , Raposo, G. , Cerf-Bensussan, N. and Heyman, M. (2007). T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells. Gastroenterology 132, 1866-1876.
26. Mao, Z. , Song, S. , Zhu, Y. , Yi, X. , Zhang, H. , Shang, Y. and Tong, T. (2003). Transcriptional regulation of A33 antigen expression by gut-enriched Krüppel-like factor. Oncogene 22, 4434-4443.
27. Morton, P. E. , Hicks, A. , Nastos, T. , Santis, G. and Parsons, M. (2013). CAR regulates epithelial cell junction stability through control of E-cadherin trafficking. Sci. Rep. 3, 2889.
28. Nasdala, I. , Wolburg-Buchholz, K. , Wolburg, H. , Kuhn, A. , Ebnet, K. , Brachtendorf, G. , Samulowitz, U. , Kuster, B. , Engelhardt, B. , Vestweber, D. et al. (2002). A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J. Biol. Chem. 277, 16294-16303.
29. Neufert, C. , Becker, C. and Neurath, M. F. (2007). An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat. Protoc. 2, 1998-2004.
30. Nguyen, C. Q. , Cornelius, J. G. , Cooper, L. , Neff, J. , Tao, J. , Lee, B. H. and Peck, A. B. (2008). Identification of possible candidate genes regulating Sjögren's syndrome-associated autoimmunity: A potential role for TNFSF4 in autoimmune exocrinopathy. Arthritis Res. Ther. 10, R137.
31. Noble, C. L. , Abbas, A. R. , Cornelius, J. , Lees, C. W. , Ho, G.-T. , Toy, K. , Modrusan, Z. , Pal, N. , Zhong, F. , Chalasani, S. et al. (2008). Regional variation in gene expression in the healthy colon is dysregulated in ulcerative colitis. Gut 57, 1398-1405.
32. Olsen, J. , Gerds, T. A. , Seidelin, J. B. , Csillag, C. , Bjerrum, J. T. , Troelsen, J. T. and Nielsen, O. H. (2009). Diagnosis of ulcerative colitis before onset of inflammation by multivariate modeling of genome-wide gene expression data. Inflamm. Bowel Dis. 15, 1032-1038.
33. Pastorelli, L. , De Salvo, C. , Mercado, J. R. , Vecchi, M. and Pizarro, T. T. (2013). Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: Lessons learned from animal models and human genetics. Front. Immunol. 4, 280.
34. Pazirandeh, A. , Sultana, T. , Mirza, M. , Rozell, B. , Hultenby, K. , Wallis, K. , Vennström, B. , Davis, B. , Arner, A. , Heuchel, R. et al. (2011). Multiple phenotypes in adult mice following inactivation of the Coxsackievirus and Adenovirus Receptor (Car) gene. PLoS ONE 6, e20203.
35. Pereira-Fantini, P. M. , Judd, L. M. , Kalantzis, A. , Peterson, A. , Ernst, M. , Heath, J. K. and Giraud, A. S. (2010). A33 antigen-deficient mice have defective colonic mucosal repair. Inflamm. Bowel Dis. 16, 604-612.
36. Raschperger, E. , Thyberg, J. , Pettersson, S. , Philipson, L. , Fuxe, J. and Pettersson, R. F. (2006). The coxsackie-and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostasis. Exp. Cell Res. 312, 1566-1580.
37. Rudolph, U. , Finegold, M. J. , Rich, S. S. , Harriman, G. R. , Srinivasan, Y. , Brabet, P. , Bradley, A. and Birnbaumer, L. (1995). Gi2 alpha protein deficiency: A model for inflammatory bowel disease. J. Clin. Immunol. 15, S101-S105.
38. Saitou, M. , Furuse, M. , Sasaki, H. , Schulzke, J.-D. , Fromm, M. , Takano, H. , Noda, T. and Tsukita, S. (2000). Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol. Biol. Cell 11, 4131-4142.
39. Sakamoto, J. , Kojima, H. , Kato, J. , Hamashima, H. and Suzuki, H. (2000). Organspecific expression of the intestinal epithelium-related antigen A33, a cell surface target for antibody-based imaging and treatment in gastrointestinal cancer. Cancer Chemother. Pharmacol. 46 Suppl. , S27-S32.
40. Scott, A. M. , Lee, F.-T. , Jones, R. , Hopkins, W. , MacGregor, D. , Cebon, J. S. , Hannah, A. , Chong, G. , U, P. , Papenfuss, A. et al. (2005). A phase I trial of humanized monoclonal antibody A33 in patients with colorectal carcinoma: Biodistribution, pharmacokinetics, and quantitative tumor uptake. Clin. Cancer Res. 11, 4810-4817.
41. Scott, C. L. , Aumeunier, A. M. and Mowat, A. M. (2011). Intestinal CD103+ dendritic cells: Master regulators of tolerance? Trends Immunol. 32, 412-419.
42. Smalley-Freed, W. G. , Efimov, A. , Burnett, P. E. , Short, S. P. , Davis, M. A. , Gumucio, D. L. , Washington, M. K. , Coffey, R. J. and Reynolds, A. B. (2010). p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J. Clin. Invest. 120, 1824-1835.
43. Turner, J. R. (2009). Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809.
44. Van Niel, G. , Mallegol, J. , Bevilacqua, C. , Candalh, C. , Brugière, S. , Tomaskovic-Crook, E. , Heath, J. K. , Cerf-Bensussan, N. and Heyman, M. (2003). Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice. Gut 52, 1690-1697.
45. Ventura, M. T. , Polimeno, L. , Amoruso, A. C. , Gatti, F. , Annoscia, E. , Marinaro, M. , Di Leo, E. , Matino, M. G. , Buquicchio, R. , Bonini, S. et al. (2006). Intestinal permeability in patients with adverse reactions to food. Dig. Liver Dis. 38, 732-736.
46. Vetrano, S. and Danese, S. (2009). The role of JAM-A in inflammatory bowel disease: Unrevealing the ties that bind. Ann. N. Y. Acad. Sci. 1165, 308-313.
47. Vetrano, S. , Rescigno, M. , Cera, M. R. , Correale, C. , Rumio, C. , Doni, A. , Fantini, M. , Sturm, A. , Borroni, E. , Repici, A. et al. (2008). Unique role of junctional adhesion molecule-A in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology 135, 173-184.
48. Wang, Y. , Mei, Y. , Bao, S. and Xu, L. (2007). Vasoactive intestinal polypeptide enhances oral tolerance by regulating both cellular and humoral immune responses. Clin. Exp. Immunol. 148, 178-187.
49. Welt, S. , Divgi, C. R. , Real, F. X. , Yeh, S. D. , Garin-Chesa, P. , Finstad, C. L. , Sakamoto, J. , Cohen, A. , Sigurdson, E. R. , Kemeny, N. et al. (1990). Quantitative analysis of antibody localization in human metastatic colon cancer: A phase I study of monoclonal antibody A33. J. Clin. Oncol. 8, 1894-1906.
50. Welt, S. , Divgi, C. R. , Kemeny, N. , Finn, R. D. , Scott, A. M. , Graham, M. , Germain, J. S. , Richards, E. C. , Larson, S. M. , Oettgen, H. F. et al. (1994). Phase I/II study of iodine 131-labeled monoclonal antibody A33 in patients with advanced colon cancer. J. Clin. Oncol. 12, 1561-1571.
51. Welt, S. , Scott, A. M. , Divgi, C. R. , Kemeny, N. E. , Finn, R. D. , Daghighian, F. , Germain, J. S. , Richards, E. C. , Larson, S. M. and Old, L. J. (1996). Phase I/II study of iodine 125-labeled monoclonal antibody A33 in patients with advanced colon cancer. J. Clin. Oncol. 14, 1787-1797.
52. Welt, S. , Ritter, G. , Williams, C. , Jr, Cohen, L. S. , Jungbluth, A. , Richards, E. A. , Old, L. J. and Kemeny, N. E. (2003). Preliminary report of a phase I study of combination chemotherapy and humanized A33 antibody immunotherapy in patients with advanced colorectal cancer. Clin. Cancer Res. 9, 1347-1353.
53. Whitehead, R. H. , Brown, A. and Bhathal, P. S. (1987). A method for the isolation and culture of human colonic crypts in collagen gels. In Vitro Cell Dev. Biol. 23, 436-442.
54. Wirtz, S. and Neurath, M. F. (2007). Mouse models of inflammatory bowel disease. Adv. Drug Deliv. Rev. 59, 1073-1083.
55. Wirtz, S. , Neufert, C. , Weigmann, B. and Neurath, M. F. (2007). Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2, 541-546.
56. Zeissig, S. , Burgel, N. , Gunzel, D. , Richter, J. , Mankertz, J. , Wahnschaffe, U. , Kroesen, A. J. , Zeitz, M. , Fromm, M. and Schulzke, J.-D. (2007). Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 56, 61-72.