The Src kinase Fyn is protective in acute chemical-induced colitis and promotes recovery from disease

Journal of Leukocyte Biology

Volumn 97, Issue 6, 2015, Pages 1089-1099

  Lopes, Fernando ^a   Wang, Arthur ^a   Smyth, David ^a   Reyes, Jose Luis ^a   Doering, Axinia ^a   Patrick Schenck, L ^a,b   Beck, Paul ^a,b   Waterhouse, Christopher ^b   McKay, Derek M ^a  

^a Gastrointestinal Research Group and Inflammation Research Network Department of Physiology and Pharmacology   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Dextran sodium sulfate; Foxp3; Inflammatory bowel disease; Regulatory T cell

Indexed keywords

DEXTRAN SULFATE; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; MESSENGER RNA; PROTEIN KINASE FYN; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; FYN PROTEIN, MOUSE; IL10 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOODY DIARRHEA; CD4+ T LYMPHOCYTE; COLITIS; COLON FLORA; COLON HEMORRHAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY SCORE; ENZYME INHIBITION; FLOW CYTOMETRY; HEMATOPOIETIC CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; INTESTINE MUCOSA PERMEABILITY; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGULATORY T LYMPHOCYTE; SPLEEN CELL; STROMA CELL; ANIMAL; CHEMICALLY INDUCED; COLON; DEFICIENCY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; PERMEABILITY; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; COLITIS; COLON; DEXTRAN SULFATE; EPITHELIAL CELLS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; INTERLEUKIN-10; INTERLEUKIN-17; MALE; MICE; MICE, KNOCKOUT; PERMEABILITY; PROTO-ONCOGENE PROTEINS C-FYN; SIGNAL TRANSDUCTION;

EID: 84930260925     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0814-405RR     Document Type: Article

References (50)

1. Kostic, A. D., Xavier, R. J., Gevers, D. (2014) The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146, 1489–1499.
2. Cader, M. Z., Kaser, A. (2013) Recent advances in inflammatory bowel disease: mucosal immune cells in intestinal inflammation. Gut 62, 1653–1664.
3. Szalmás, A., Gyöngyösi, E., Ferenczi, A., Lászl ó, B., Karosi, T., Csomor, P., Gergely, L., Veress, G., Kónya, J. (2013) Activation of Src, Fyn and Yes non-receptor tyrosine kinases in keratinocytes expressing human papillomavirus (HPV) type 16 E7 oncoprotein. Virol. J. 10, 79.
4. Hermiston, M. L., Zikherman, J., Zhu, J. W. (2009) CD45, CD148, and Lyp/Pep: critical phosphatases regulating Src family kinase signaling networks in immune cells. Immunol. Rev. 228, 288–311.
5. Smyth, D., Phan, V., Wang, A., McKay, D. M. (2011) Interferon-g-induced increases in intestinal epithelial macromolecular permeability requires the Src kinase Fyn. Lab. Invest. 91, 764–777.
6. Chen, R. J., Chang, W. W., Lin, Y. C., Cheng, P. L., Chen, Y. R. (2013) Alzheimer’s amyloid-b oligomers rescue cellular prion protein induced tau reduction via the Fyn pathway. ACS Chem. Neurosci. 4, 1287–1296.
7. Imbert, V., Farahifar, D., Auberger, P., Mary, D., Rossi, B., Peyron, J. F. (1996) Stimulation of the T-cell antigen receptor-CD3 complex signaling pathway by the tyrosine phosphatase inhibitor pervanadate is mediated by inhibition of CD45: evidence for two interconnected Lck/Fyn- or zap- 70-dependent signaling pathways. J. Inflamm. 46, 65–77.
8. Rajasekaran, K., Kumar, P., Schuldt, K. M., Peterson, E. J., Vanhaesebroeck, B., Dixit, V., Thakar, M. S., Malarkannan, S. (2013) Signaling by Fyn-ADAP via the Carma1-Bcl-10-MAP3K7 signalosome exclusively regulates inflammatory cytokine production in NK cells. Nat. Immunol. 14, 1127–1136.
9. Zhong, M. C., Veillette, A. (2013) The adaptor molecule signaling lymphocytic activation molecule (SLAM)-associated protein (SAP) is essential in mechanisms involving the Fyn tyrosine kinase for induction and progression of collagen-induced arthritis. J. Biol. Chem. 288, 31423–31436.
10. De Wispelaere, M., LaCroix, A. J., Yang, P. L. (2013) The small molecules AZD0530 and dasatinib inhibit dengue virus RNA replication via Fyn kinase. J. Virol. 87, 7367–7381.
11. Melgar, S., Karlsson, A., Michäelsson, E. (2005) Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G1328–G1338.
12. Vu, J. P., Million, M., Larauche, M., Luong, L., Norris, J., Waschek, J. A., Pothoulakis, C., Pisegna, J. R., Germano, P. M. (2014) Inhibition of vasoactive intestinal polypeptide (VIP) induces resistance to dextran sodium sulfate (DSS)-induced colitis in mice. J. Mol. Neurosci. 52, 37–47.
13. Diaz-Granados, N., Howe, K., Lu, J., McKay, D. M. (2000) Dextran sulfate sodium-induced colonic histopathology, but not altered epithelial ion transport, is reduced by inhibition of phosphodiesterase activity. Am. J. Pathol. 156, 2169–2177.
14. Schmidt, D., Amrani, A., Verdaguer, J., Bou, S., Santamaria, P. (1999) Autoantigen-independent deletion of diabetogenic CD4+ thymocytes by protective MHC class II molecules. J. Immunol. 162, 4627–4636.
15. Johnston, M. J., Wang, A., Catarino, M. E., Ball, L., Phan, V. C., MacDonald, J. A., McKay, D. M. (2010) Extracts of the rat tapeworm, Hymenolepis diminuta, suppress macrophage activation in vitro and alleviate chemically induced colitis in mice. Infect. Immun. 78, 1364–1375.
16. Feito, M. J., Vila, M., Matesanz, M. C., Linares, J., Gonçalves, G., Marques, P. A., Vallet-Regí, M., Rojo, J. M., Portolés, M. T. (2014) In vitro evaluation of graphene oxide nanosheets on immune function. J. Colloid Interface Sci. 432, 221–228.
17. Song, B., Huang, G., Tong, C., Li, G., Wang, Z., Xiong, Y., Zhang, S., Lu, J., Guan, S. (2013) Gossypol suppresses mouse T lymphocytes via inhibition of NFkB, NFAT and AP-1 pathways. Immunopharmacol. Immunotoxicol. 35, 615–621.
18. Prescott, D., McKay, D. M. (2011) Aspirin-triggered lipoxin enhances macrophage phagocytosis of bacteria while inhibiting inflammatory cytokine production. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G487–G497.
19. Schmittgen, T. D., Livak, K. J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
20. Hahn, J. N., Falck, V. G., Jirik, F. R. (2011) Smad4 deficiency in T cells leads to the Th17-associated development of premalignant gastroduodenal lesions in mice. J. Clin. Invest. 121, 4030–4042.
21. Wallace, J. L., MacNaughton, W. K., Morris, G. P., Beck, P. L. (1989) Inhibition of leukotriene synthesis markedly accelerates healing in a rat model of inflammatory bowel disease. Gastroenterology 96, 29–36.
22. Chen, X., Katchar, K., Goldsmith, J. D., Nanthakumar, N., Cheknis, A., Gerding, D. N., Kelly, C. P. (2008) A mouse model of Clostridium difficileassociated disease. Gastroenterology 135, 1984–1992.
23. Naito, Y., Takagi, T., Handa, O., Ishikawa, T., Nakagawa, S., Yamaguchi, T., Yoshida, N., Minami, M., Kita, M., Imanishi, J., Yoshikawa, T. (2003) Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-a deficient mice. J. Gastroenterol. Hepatol. 18, 560–569.
24. McDermott, A. J., Higdon, K. E., Muraglia, R., Erb-Downward, J. R., Falkowski, N. R., McDonald, R. A., Young, V. B., Huffnagle, G. B. (2015) The Role of Gr-1 cells and TNFa signaling during Clostridium difficile colitis in Mice. Immunology. 144,704–716.
25. Kinnebrew, M. A., Pamer, E. G. (2012) Innate immune signaling in defense against intestinal microbes. Immunol. Rev. 245, 113–131.
26. Abraham, C., Medzhitov, R. (2011) Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 140, 1729–1737.
27. Koboziev, I., Reinoso Webb, C., Furr, K. L., Grisham, M. B. (2014) Role of the enteric microbiota in intestinal homeostasis and inflammation. Free Radic. Biol. Med. 68, 122–133.
28. Cooke, M. P., Abraham, K. M., Forbush, K. A., Perlmutter, R. M. (1991) Regulation of T cell receptor signaling by a src family protein-tyrosine kinase (p59fyn). Cell 65, 281–291.
29. Parravicini, V., Gadina, M., Kovarova, M., Odom, S., Gonzalez-Espinosa, C., Furumoto, Y., Saitoh, S., Samelson, L. E., O’Shea, J. J., Rivera, J. (2002) Fyn kinase initiates complementary signals required for IgEdependent mast cell degranulation. Nat. Immunol. 3, 741–748.
30. Zamoyska, R., Basson, A., Filby, A., Legname, G., Lovatt, M., Seddon, B. (2003) The influence of the src-family kinases, Lck and Fyn, on T cell differentiation, survival and activation. Immunol. Rev. 191, 107–118.
31. Lee, S. K., Shaw, A., Maher, S. E., Bothwell, A. L. (1994) p59fyn tyrosine kinase regulates p56lck tyrosine kinase activity and early TCR-mediated signaling. Int. Immunol. 6, 1621–1627.
32. Eberl, G., Lowin-Kropf, B., MacDonald, H. R. (1999) Cutting edge: NKT cell development is selectively impaired in Fyn-deficient mice. J. Immunol. 163, 4091–4094.
33. Chan, B., Lanyi, A., Song, H. K., Griesbach, J., Simarro-Grande, M., Poy, F., Howie, D., Sumegi, J., Terhorst, C., Eck, M. J. (2003) SAP couples Fyn to SLAM immune receptors. Nat. Cell Biol. 5, 155–160.
34. Latour, S., Roncagalli, R., Chen, R., Bakinowski, M., Shi, X., Schwartzberg, P. L., Davidson, D., Veillette, A. (2003) Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation. Nat. Cell Biol. 5, 149–154.
35. Mamchak, A. A., Sullivan, B. M., Hou, B., Lee, L. M., Gilden, J. K., Krummel, M. F., Locksley, R. M., DeFranco, A. L. (2008) Normal development and activation but altered cytokine production of Fyndeficient CD4+ T cells. J. Immunol. 181, 5374–5385.
36. Filby, A., Seddon, B., Kleczkowska, J., Salmond, R., Tomlinson, P., Smida, M., Lindquist, J. A., Schraven, B., Zamoyska, R. (2007) Fyn regulates the duration of TCR engagement needed for commitment to effector function. J. Immunol. 179, 4635–4644.
37. Karrasch, T., Jobin, C. (2008) NF-kappaB and the intestine: friend or foe? Inflamm. Bowel Dis. 14, 114–124.
38. Chisti, M. M., Khachani, A., Brahmanday, G. R., Klamerus, J. (2013) Dasatinib-induced haemorrhagic colitis in chronic myeloid leukaemia (CML) in blast crisis. BMJ Case Rep. doi: 10.1136/bcr-2013-200610 [Epub ahead of print].
39. Jellbauer, S., Raffatellu, M. (2014) An intestinal arsonist: pathobiont ignites IBD and flees the scene. Gut 63, 1034–1035.
40. Yang, X., Yang, Y., Wang, Y., Zhan, B., Gu, Y., Cheng, Y., Zhu, X. (2014) Excretory/secretory products from Trichinella spiralis adult worms ameliorate DSS-induced colitis in mice. PLoS ONE 9, e96454.
41. Bhuyan, Z. A., Arimochi, H., Nishida, J., Kataoka, K., Kurihara, T., Ishifune, C., Tsumura, H., Ito, M., Ito, Y., Kitamura, A., Yasutomo, K. (2014) CD98hc regulates the development of experimental colitis by controlling effector and regulatory CD4(+) T cells. Biochem. Biophys. Res. Commun. 444, 628–633.
42. Furusawa, Y., Obata, Y., Fukuda, S., Endo, T. A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K., Kato, T., Takahashi, M., Fukuda, N. N., Murakami, S., Miyauchi, E., Hino, S., Atarashi, K., Onawa, S., Fujimura, Y., Lockett, T., Clarke, J. M., Topping, D. L., Tomita, M., Hori, S., Ohara, O., Morita, T., Koseki, H., Kikuchi, J., Honda, K., Hase, K., Ohno, H. (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446–450.
43. Huang, Y. J., Haist, V., Baumgärtner, W., Föhse, L., Prinz, I., Suerbaum, S., Floess, S., Huehn, J. (2014) Induced and thymus-derived Foxp3+ regulatory T cells share a common niche. Eur. J. Immunol. 44, 460–468.
44. Mamchak, A. A., Thien, C. B., Dagger, S. A., Lyandres, J., Jiang, S., Langdon, W. Y., DeFranco, A. L. (2010) Unaltered negative selection and Treg development of self-reactive thymocytes in TCR transgenic Fyndeficient mice. Eur. J. Immunol. 40, 539–547.
45. Reardon, C., Wang, A., McKay, D. M. (2008) Transient local depletion of Foxp3+ regulatory T cells during recovery from colitis via Fas/Fas ligandinduced death. J. Immunol. 180, 8316–8326.
46. Davidson, D., Chow, L. M., Fournel, M., Veillette, A. (1992) Differential regulation of T cell antigen responsiveness by isoforms of the src-related tyrosine protein kinase p59fyn. J. Exp. Med. 175, 1483–1492.
47. Ueda, A., Zhou, L., Stein, P. L. (2012) Fyn promotes Th17 differentiation by regulating the kinetics of RORgt and Foxp3 expression. J. Immunol. 188, 5247–5256.
48. Fallarino, F., Grohmann, U., Puccetti, P. (2012) Indoleamine 2,3- dioxygenase: from catalyst to signaling function. Eur. J. Immunol. 42, 1932–1937.
49. Pallotta, M. T., Orabona, C., Volpi, C., Vacca, C., Belladonna, M. L., Bianchi, R., Servillo, G., Brunacci, C., Calvitti, M., Bicciato, S., Mazza, E. M., Boon, L., Grassi, F., Fioretti, M. C., Fallarino, F., Puccetti, P., Grohmann, U. (2011) Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat. Immunol. 12, 870–878.
50. Matteoli, G., Mazzini, E., Iliev, I. D., Mileti, E., Fallarino, F., Puccetti, P., Chieppa, M., Rescigno, M. (2010) Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction. Gut 59, 595–604.