Spermidine stimulates T cell protein-tyrosine phosphatasemediated protection of intestinal epithelial barrier function

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32651-32662

  Penrose, Harrison M ^b   Marchelletta, Ronald R ^b   Krishnan, Moorthy ^a   McCole, Declan F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIAL PERMEABILITY; INFLAMMATORY BOWEL DISEASE; INFLAMMATORY SIGNALING; INTESTINAL EPITHELIAL CELLS; PROINFLAMMATORY CYTOKINES; PROTEIN-TYROSINE PHOSPHATASE; SIGNAL TRANSDUCERS AND ACTIVATORS OF TRANSCRIPTIONS; TRANSEPITHELIAL ELECTRICAL RESISTANCES;

AMINO ACIDS; CHEMICAL ACTIVATION; GENE ENCODING; GENE EXPRESSION; GENE EXPRESSION REGULATION; PATHOLOGY; PHOSPHATASES; PROTEINS; SIGNALING;

CELL SIGNALING;

GAMMA INTERFERON; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE (NADP); NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 2; SPERMIDINE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENTERITIS; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PTPN2 GENE; SIGNAL TRANSDUCTION;

EPITHELIAL CELL; INTERFERON; PERMEABILITY; STAT TRANSCRIPTION FACTOR; TIGHT JUNCTIONS;

CELL LINE; EPITHELIAL CELLS; HUMANS; INTERFERON-GAMMA; INTESTINAL MUCOSA; PERMEABILITY; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 2; SIGNAL TRANSDUCTION; SPERMIDINE;

EID: 84887433975     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.475962     Document Type: Article

References (40)

1. Fuss, I. J., Neurath, M., Boirivant, M., Klein, J. S., de la Motte, C., Strong, S. A., Fiocchi, C., and Strober, W. (1996) Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-γ, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J. Immunol. 157, 1261-1270
2. Turner, J. R. (2009) Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809
3. Madara, J. L., and Stafford, J. (1989) Interferon-γ directly affects barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest. 83, 724-727
4. Youakim, A., and Ahdieh, M. (1999) Interferon-γ decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am. J. Physiol. 276, G1279-1288
5. Tonks, N. K., and Neel, B. G. (2001) Combinatorial control of the specificity of protein tyrosine phosphatases. Curr. Opin. Cell Biol. 13, 182-195
6. Mattila, E., Pellinen, T., Nevo, J., Vuoriluoto, K., Arjonen, A., and Ivaska, J. (2005) Negative regulation of EGFR signalling through integrin-α1β1- mediated activation of protein tyrosine phosphatase TCPTP. Nat. Cell Biol. 7, 78-85
7. Galic, S., Klingler-Hoffmann, M., Fodero-Tavoletti, M. T., Puryer, M. A., Meng, T. C., Tonks, N. K., and Tiganis, T. (2003) Regulation of insulin receptor signaling by the protein tyrosine phosphatase TCPTP. Mol. Cell Biol. 23, 2096-2108
8. ten Hoeve, J., de Jesus Ibarra-Sanchez, M., Fu, Y., Zhu, W., Tremblay, M., David, M., and Shuai, K. (2002) Identification of a nuclear Stat1 protein tyrosine phosphatase. Mol. Cell Biol. 22, 5662-5668
9. Yamamoto, T., Sekine, Y., Kashima, K., Kubota, A., Sato, N., Aoki, N., and Matsuda, T. (2002) The nuclear isoform of protein-tyrosine phosphatase TC-PTP regulates interleukin-6-mediated signaling pathway through STAT3 dephosphorylation. Biochem. Biophys. Res. Commun. 297, 811-817
10. Franke, A., McGovern, D. P., Barrett, J. C., Wang, K., Radford-Smith, G. L., Ahmad, T., Lees, C. W., Balschun, T., Lee, J., Roberts, R., Anderson, C. A., Bis, J. C., Bumpstead, S., Ellinghaus, D., Festen, E. M., Georges, M., Green, T., Haritunians, T., Jostins, L., Latiano, A., Mathew, C. G., Montgomery, G. W., Prescott, N. J., Raychaudhuri, S., Rotter, J. I., Schumm, P., Sharma, Y., Simms, L. A., Taylor, K. D., Whiteman, D., Wijmenga, C., Baldassano, R. N., Barclay, M., Bayless, T. M., Brand, S., Buning, C., Cohen, A., Colombel, J. F., Cottone, M., Stronati, L., Denson, T., De Vos, M., D'Inca, R., Dubinsky, M., Edwards, C., Florin, T., Franchimont, D., Gearry, R., Glas, J., Van Gossum, A., Guthery, S. L., Halfvarson, J., Verspaget, H. W., Hugot, J. P., Karban, A., Laukens, D., Lawrance, I., Lemann, M., Levine, A., Libioulle, C., Louis, E., Mowat, C., Newman, W., Panes, J., Phillips, A., Proctor, D. D., Regueiro, M., Russell, R., Rutgeerts, P., Sanderson, J., Sans, M., Seibold, F., Steinhart, A. H., Stokkers, P. C., Torkvist, L., Kullak-Ublick, G., Wilson, D., Walters, T., Targan, S. R., Brant, S. R., Rioux, J. D., D'Amato, M., Weersma, R. K., Kugathasan, S., Griffiths, A. M., Mansfield, J. C., Vermeire, S., Duerr, R. H., Silverberg, M. S., Satsangi, J., Schreiber, S., Cho, J. H., Annese, V., Hakonarson, H., Daly, M. J., and Parkes, M. (2010) Genome- wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat. Genet. 42, 1118-1125
11. Parkes, M., Barrett, J. C., Prescott, N. J., Tremelling, M., Anderson, C. A., Fisher, S. A., Roberts, R. G., Nimmo, E. R., Cummings, F. R., Soars, D., Drummond, H., Lees, C. W., Khawaja, S. A., Bagnall, R., Burke, D. A., Todhunter, C. E., Ahmad, T., Onnie, C. M., McArdle, W., Strachan, D., Bethel, G., Bryan, C., Lewis, C. M., Deloukas, P., Forbes, A., Sanderson, J., Jewell, D. P., Satsangi, J., Mansfield, J. C., Wellcome Trust Case Control Consortium, Cardon, L., and Mathew, C. G. (2007) Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat. Genet. 39, 830-832
12. Scharl, M., Paul, G., Weber, A., Jung, B. C., Docherty, M. J., Hausmann, M., Rogler, G., Barrett, K. E., and McCole, D. F. (2009) Protection of epithelial barrier function by the Crohn's disease associated gene protein tyrosine phosphatase n2. Gastroenterology 137, 2030-2040
13. Scharl, M., Hruz, P., and McCole, D. F. (2010) Protein tyrosine phosphatase non-receptor Type 2 regulates IFN-γ-induced cytokine signaling in THP-1 monocytes. Inflamm. Bowel Dis. 16, 2055-2064
14. Mattila, E., Marttila, H., Sahlberg, N., Kohonen, P., Tähtinen, S., Halonen, P., Perälä, M., and Ivaska, J. (2010) Inhibition of receptor tyrosine kinase signalling by small molecule agonist of T-cell protein tyrosine phosphatase. BMC Cancer 10, 7
15. Dharmsathaphorn, K., McRoberts, J. A., Mandel, K. G., Tisdale, L. D., and Masui, H. (1984) A human colonic tumor cell line that maintains vectorial electrolyte transport. Am. J. Physiol. 246, G204-208
16. Augeron, C., and Laboisse, C. L. (1984) Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res. 44, 2961-3969
17. Cafferata, E. G., González-Guerrico, A. M., Giordano, L., Pivetta, O. H., and Santa-Coloma, T. A. (2000) Interleukin-1β regulates CFTR expression in human intestinal T84 cells. Biochim. Biophys. Acta 1500, 241-248
18. McKay, D. M., Watson, J. L., Wang, A., Caldwell, J., Prescott, D., Ceponis, P. M., Di Leo, V., and Lu, J. (2007) Phosphatidylinositol 3'-kinase is a critical mediator of interferon-γ-induced increases in enteric epithelial permeability. J. Pharmacol. Exp. Ther. 320, 1013-1022
19. Boivin, M. A., Roy, P. K., Bradley, A., Kennedy, J. C., Rihani, T., and Ma, T. Y. (2009) Mechanism of interferon-γ-induced increase in T84 intestinal epithelial tight junction. J. Interferon Cytokine Res. 29, 45-54
20. Moinard, C., Cynober, L., and de Bandt, J. P. (2005) Polyamines. Metabolism and implications in human diseases. Clin. Nutr. 24, 184-197
21. Fanning, A. S., Jameson, B. J., Jesaitis, L. A., and Anderson, J. M. (1998) The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 273, 29745-29753
22. Heinonen, K. M., Nestel, F. P., Newell, E. W., Charette, G., Seemayer, T. A., Tremblay, M. L., and Lapp, W. S. (2004) T-cell protein tyrosine phosphatase deletion results in progressive systemic inflammatory disease. Blood 103, 3457-3464
23. Seiler, N., Delcros, J. G., and Moulinoux, J. P. (1996) Polyamine transport in mammalian cells. An update. Int. J. Biochem. Cell Biol. 28, 843-861
24. Hoet, P. H., and Nemery, B. (2000) Polyamines in the lung. Polyamine uptake and polyamine-linked pathological or toxicological conditions. Am. J. Physiol. Lung Cell Mol. Physiol. 278, L417-433
25. Johnson, L. R., and McCormack, S. A. (1999) Healing of gastrointestinal mucosa. Involvement of polyamines. News Physiol. Sci. 14, 12-17
26. Hao, L., Tiganis, T., Tonks, N. K., and Charbonneau, H., (1997) The noncatalytic C-terminal segment of the T cell protein tyrosine phosphatase regulates activity via an intramolecular mechanism. J. Biol. Chem. 272, 29322-29329
27. Otsuka, H. (1971) The toxic effect of spermidine on normal and transformed cells. J. Cell Sci. 9, 71-84
28. Watson, C. J., Hoare, C. J., Garrod, D. R., Carlson, G. L., and Warhurst, G. (2005) Interferon-γ selectively increases epithelial permeability to large molecules by activating different populations of paracellular pores. J. Cell Sci. 118, 5221-5230
29. Utech, M., Ivanov, A. I., Samarin, S. N., Bruewer, M., Turner, J. R., Mrsny, R. J., Parkos, C. A., and Nusrat, A. (2005) Mechanism of IFN-γ-induced endocytosis of tight junction proteins. Myosin II-dependent vacuolarization of the apical plasma membrane. Mol. Biol. Cell 16, 5040-5052
30. Festen, E. A., Goyette, P., Green, T., Boucher, G., Beauchamp, C., Trynka, G., Dubois, P. C., Lagacé, C., Stokkers, P. C., Hommes, D. W., Barisani, D., Palmieri, O., Annese, V., van Heel, D. A., Weersma, R. K., Daly, M. J., Wijmenga, C., and Rioux, J. D. (2011) A meta-analysis of genome-wide association scans identifies IL18RAP, PTPN2, TAGAP, and PUS10 as shared risk loci for Crohn's disease and celiac disease. PLoS Genet. 7, e1001283
31. Bruewer, M., Utech, M., Ivanov, A. I., Hopkins, A. M., Parkos, C. A., and Nusrat, A. (2005) Interferon-γ induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J. 19, 923-933
32. Wang, F., Graham, W. V., Wang, Y., Witkowski, E. D., Schwarz, B. T., and Turner, J. R. (2005) Interferon-γ and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am. J. Pathol. 166, 409-419
33. Beaurepaire, C., Smyth, D., and McKay, D. M. (2009) Interferon-γ regulation of intestinal epithelial permeability. J. Interferon Cytokine Res. 29, 133-144
34. Adams, R. B., Planchon, S. M., and Roche, J. K. (1993) IFN-γ modulation of epithelial barrier function. Time course, reversibility, and site of cytokine binding. J. Immunol. 150, 2356-2363
35. Scharl, M., Paul, G., Barrett, K. E., and McCole, D. F. (2009) AMP-activated protein kinase mediates the interferon-γ-induced decrease in intestinal epithelial barrier function. J. Biol. Chem. 284, 27952-27963
36. Ma, T. Y., Nguyen, D., Bui, V., Nguyen, H., and Hoa, N. (1999) Ethanol modulation of intestinal epithelial tight junction barrier. Am. J. Physiol. Gastrointest. Liver Physiol. 276, G965-G974
37. Tiganis, T., Kemp, B. E., and Tonks, N. K. (1999) The protein-tyrosine phosphatase TCPTP regulates epidermal growth factor receptor-mediated and phosphatidylinositol 3-kinase-dependent signaling. J. Biol. Chem. 274, 27768-27775
38. Guo, X., Rao, J. N., Liu, L., Zou, T. T., Turner, D. J., Bass, B. L., and Wang, J. Y. (2003) Regulation of adherens junctions and epithelial paracellular permeability. A novel function for polyamines. Am. J. Physiol. Cell Physiol. 285, C1174-C1187
39. Guo, X., Rao, J. N., Liu, L., Zou, T., Keledjian, K. M., Boneva, D., Marasa, B. S., and Wang, J. Y. (2005) Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G1159-1169
40. Todd, J. A., Walker, N. M., Cooper, J. D., Smyth, D. J., Downes, K., Plagnol, V., Bailey, R., Nejentsev, S., Field, S. F., Payne, F., Lowe, C. E., Szeszko, J. S., Hafler, J. P., Zeitels, L., Yang, J. H., Vella, A., Nutland, S., Stevens, H. E., Schuilenburg, H., Coleman, G., Maisuria, M., Meadows, W., Smink, L. J., Healy, B., Burren, O. S., Lam, A. A., Ovington, N. R., Allen, J., Adlem, E., Leung, H. T., Wallace, C., Howson, J. M., Guja, C., Ionescu-Tîrgovite, C., Genetics of Type 1 Diabetes in Finland, Simmonds, M. J., Heward, J. M., Gough, S. C., Wellcome Trust Case Control Consortium, Dunger, D. B., Wicker, L. S., and Clayton, D. G. (2007) Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes. Nat. Genet. 39, 857-864