Differential expression of gastric MUC5AC in colonic epithelial cells: TFF3-wired IL1β/Akt crosstalk-induced mucosal immune response against Shigella dysenteriae infection

Journal of Cell Science

Volumn 125, Issue 3, 2012, Pages 703-713

  Raja, Subramaniya Bharathi ^a   Murali, Malliga Raman ^a   Devaraj, Halagowder ^a   Devaraj, Sivasithamparam Niranjali ^a  

^a UNIVERSITY OF MADRAS   (India)

Author keywords

IL1 Akt crosstalk; MUC2; MUC5AC; Mucosal immunity; Shigella dysenteriae; TFF3

Indexed keywords

BETA CATENIN; CYCLIN D1; CYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; INTERLEUKIN 1BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUCIN 2; MUCIN 5AC; PEPTIDE; PROTEIN KINASE B; TREFOIL FACTOR FAMILY PEPTIDE 1; TREFOIL FACTOR FAMILY PEPTIDE 3; UNCLASSIFIED DRUG; UVOMORULIN; VASCULOTROPIN RECEPTOR;

APOPTOSIS; ARTICLE; BACTERIUM ADHERENCE; CELL ADHESION; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; COLON MUCOSA; CONTROLLED STUDY; CYTOSOL; DOWN REGULATION; EPITHELIUM CELL; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE RESPONSE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SHIGELLA DYSENTERIAE; SHIGELLOSIS; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

APOPROTEINS; BACTERIAL ADHESION; BETA CATENIN; CADHERINS; CELL PROLIFERATION; CHROMONES; DYSENTERY, BACILLARY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE KNOCKDOWN TECHNIQUES; GLYCOGEN SYNTHASE KINASE 3; HT29 CELLS; HUMANS; IMMUNITY, MUCOSAL; INTERLEUKIN-1BETA; INTESTINAL MUCOSA; MODELS, BIOLOGICAL; MORPHOLINES; MUCIN 5AC; MUCIN-2; PEPTIDES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SHIGELLA DYSENTERIAE; UP-REGULATION;

BACTERIA (MICROORGANISMS); LOTUS; SHIGELLA DYSENTERIAE;

EID: 84858121091     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.092148     Document Type: Article

References (49)

1. Alt, J. R., Cleveland, J. L., Hannink, M. and Diehl, J. A. (2000). Phosphorylationdependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev. 14, 3102-3114.
2. Alwan, A., Deignan, T., O'Sullivan, M., Kelly, J. and O'Farrelly, C. (1998). Quantitative assay of Salmonella adherence to intestinal epithelial cells: a new method for assessing novel intervention products. J. Microbiol. Methods 33, 163-170.
3. Barbash, O., Zamfirova, P., Lin, D., Chen, X., Yang, K., Lu, F., Rustgi, A. K. and Diehl, J A. (2008). Mutations in Fbx4 inhibit phosphorylation-ependent dimerization of the SCFF bx4 ligase and contribute to cyclin D1 overexpression in human cancer. Cancer Cell 14, 68-78.
4. Bartman, A. E., Sanderson, S. J., Ewing, S. L., Niehans, G. A., Wiehr, C. L., Evans, M. K. and Ho, S. B. (1999). Aberrant expression of MUC5AC and MUC6 gastric mucin genes in colorectal polyps. Int. J. Cancer 80, 210-218.
5. Basbaum, C., Lemjabbar, H., Longphre, M., Li, D., Gencsch, E. and Mcnamara, N. (1999). Control of mucin transcription by diverse injury-induced signaling pathways. Am. J. Respir. Crit. Care Med. 160, S44-S48.
6. Dabbagh, K., Takeyama, K., Lee, H. M., Ueki, I. F., Lausier, J. A. and Nadel, J. A. (1999). IL-4 induces mucin gene expression and goblet cell metaplasia in vitro and in vivo. J. Immunol. 162, 6233-6237.
7. Damera, G., Xia, B. and Sachdev, G. P. (2006). IL-4 induced MUC4 enhancement in respiratory epithelial cells in vitro is mediated through JAK-3 selective signaling. Respir. Res. 7, 39.
8. Devaraj, S., Sheyknazari, M., Warren, W. S. and Bhavanandan, V. P. (1994). Differential binding of Pseudomonas aeruginosa to normal and cystic fibrosis tracheobronchial mucins. Glycobiology 4, 307-316.
9. Dignass, A. K., Lynch-Devaney, H., Kindon, L., Thim, L. and Podolsky, D. K. (1994). Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway. J. Clin. Invest. 94, 376-383.
10. Dinarello, C. A. (2007). A signal for the caspase-1 inflammasome free of TLR. Immunity 26, 383-385.
11. Dohrman, A., Miyata, S., Gallup, M., Li, J. D., Chapelin, C., Coste, A., Escudier, E., Nadel, J. A. and Basbaum, C. (1998). Mucin gene (MUC2 and MUC5AC) upregulation by Gram-positive and Gram-negative bacteria. Biochim. Biophys. Acta 1406, 251-259.
12. Donnenberg, M. S., Donohue-Rolfe, A. and Keusch, G. T. (1989). Epithelial cell invasion: an overlooked property of enteropathogenic Escherichia coli (EPEC) associated with the EPEC adherence factor. J. Infect. Dis. 160, 452-459.
13. Guzman, K., Randell, S. H. and Nettesheim, P. (1995). Epidermal growth factor regulates expression of the mucous phenotype of rat tracheal epithelial cells. Biochem. Biophys. Res. Commun. 217, 412-418.
14. Hollingsworth, M. A. and Swanson, B. J. (2004). Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer 4, 45-60.
15. Iwashita, J., Sato, Y., Sugaya, H., Takahashi, N., Sasaki, H. and Abe, T. (2003). mRNA of MUC2 is stimulated by IL-4. IL-13 or TNF-alpha through a mitogenactivated protein kinase pathway in human colon cancer cells. Immunol. Cell Biol. 81, 275-282.
16. Kim, K. C., Nassiri, J. and Brody, J. S. (1989). Mechanisms of airway goblet cell mucin release: studies with cultured tracheal surface epithelial cells. Am. J. Respir. Cell Mol. Biol. 1, 137-143.
17. Kim, Y. D., Kwon, E. J., Kwon, T. K., Baek, S. H., Song, S. Y. and Suh, J. S. (2000). Regulation of IL-1beta-mediated MUC2 gene in NCI-H292 human airway epithelial cells. Biochem. Biophys. Res. Commun. 274, 112-116.
18. Kim, Y. D., Jeon, J. Y., Woo, H. J., Lee, J. C., Chung, J. H., Song, S. Y., Yoon, S. K. and Baek, S. H. (2002). Interleukin-1beta induces MUC2 gene expression and mucin secretion via activation of PKC-MEK/ERK and PI3K in human airway epithelial cells. J. Korean Med. Sci. 17, 765-771.
19. Kindon, H., Pothoulakis, C., Thim, L., Lynch-Devaney, K. and Podolsky, D. K. (1995). Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein Gastroenterology 109, 516-523.
20. Koga, T., Kuwahara, I., Lillehoj, E. P., Lu, W., Miyata, T., Isohama, Y. and Kim, K. C. (2007). TNF-alpha induces MUC1 gene transcription in lung epithelial cells: its signaling pathway and biological implication. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L693-L701.
21. Lesuffleur, T., Porchet, N., Aubert, J. P., Swallow, D., Gum, J. R., Kim, Y. S., Real, F. X. and Zweibau, A. (1993). Differential expression of the human mucin genes MUC1 to MUC5 in relation to growth and differentiation of different mucus-secreting HT-29 cell subpopulations. J. Cell Sci. 106, 771-783.
22. Lesuffleur, T., Roche, F., Hill, A. S., Lacasa, M., Fox, M., Swallow, D. M., Zweibaum, A. and Real, F. X. (1995). Characterization of a mucin cDNA clone isolated from HT-29 mucus-secreting cells. The 39 end of MUC5AC? J. Biol. Chem. 270, 13665-13673.
23. Leteurtre, E., Gouyer, V., Rousseau, K., Moreau, O., Barbat, A., Swallow, D., Huet, G. and Lesuffleur, T. (2004). Differential mucin expression in colon carcinoma HT-29 clones with variable resistance to 5-fluorouracil and methotrexate. Biol. Cell 96, 145-151.
24. Levine, S. J., Larivee, P., Logun, C., Angus, C. W., Ognibene, F. P. and Shelhamer, J. H. (1995). TNF-a induces mucin hypersecretion and MUC-2 gene expression by human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 12, 196-204.
25. Li, D., Gallup, M., Fan, N., Szymkowski, D. E. and Basbaum, C. B. (1998). Cloning of the amino-terminal and 59-flanking region of the human MUC5AC mucin gene and transcriptional up-regulation by bacterial exoproducts. J. Biol. Chem. 273, 6812-6820.
26. Longman, R. J., Douthwaite, J., Sylvester, P. A., Poulsom, R., Corfield, A. P., Thomas, M. G. and Wright, N. A. (2000). Coordinated localization of mucins and trefoil peptides in the ulcer associated cell lineage and the gastrointestinal mucosa. Gut. 47, 792-800.
27. Perdomo, O. J., Cavaillon, J. M., Huerre, M., Ohayon, H., Gounon, P. and Sansonetti, P. J. (1994). Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J. Exp. Med. 180, 1307-1319.
28. Perrais, M., Pigny, P., Copin, M. C., Aubert, J. P. and Van Seuningen, I. (2002). Induction of MUC2 and MUC5AC mucin by factors of the epidermal growth factor family is mediated by EGF-R/Ras/Raf/MAPK signaling cascade and Sp1. J. Biol. Chem. 19, 19.
29. Radhakrishnan, P., Halagowder, D. and Devaraj, S. N. (2007). Altered expression of MUC2 and MUC5AC in response to Shigella infection, an in vivo study. Biochim. Biophys. Acta 70, 884-889.
30. Rajkumar, R., Devaraj, H. and Niranjali, S. (1998). Binding of Shigella to rat and human intestinal mucin. Mol. Cell. Biochem. 178, 261-268.
31. Raqib, R., Wretlind, B., Andersson, J. and Lindberg, A. A. (1995). Cytokine secretion in acute shigellosis is correlated to disease activity and directed more to stool than to plasma. J. Infect. Dis. 171, 376-384.
32. Raven, J. F., Baltzis, D., Wang, S., Mounir, Z., Papadakis, A. I., Gao, H. Q. and Koromilas, A. E. (2008). PKR and PKR-like endoplasmic reticulum kinase induce the proteasome-dependent degradation of cyclin D1 via a mechanism requiring eukaryotic initiation factor 2alpha phosphorylation. J. Biol. Chem. 283, 3097-3108.
33. Skeen, J. E., Bhaskar, P. T., Chen, C. C., Chen, W. S., Peng, X. D., Nogueira, V., Hahn-Windgassen, A., Kiyokawa, H. and Hay, N. (2006). Akt deficiency impairs normal cell proliferation and suppresses oncogenesis in a p53-independent and mTORC1-dependent manner. Cancer Cell 10, 269-280.
34. Smirnova, M. G., Kiselev, S. L., Birchall, J. P. and Pearson, J. P. (2000). TNF-alpha in the regulation of MUC5AC secretion: some aspects of cytokine-induced mucin hypersecretion on the in vitro model. Cytokine 2, 1732-1736.
35. Smirnova, M. G., Kiselev, S. L., Birchall, J. P. and Pearson, J. P. (2001). Upregulation of mucin secretion in HT29-MTX cells by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin-6. Eur. Cytokine Netw. 12, 119-125.
36. Song, J. S., Kang, C. M, Yoo, M. B., Kim, S. J., Yoon, H. K., Kim, Y. K., Kim, K. H., Moon, H. S. and Park, S. H. (2007). Nitric oxide induces MUC5AC mucin in respiratory epithelial cells through PKC and ERK dependent pathways. Respir. Res. 8, 28.
37. Song, K. S., Lee, W. J., Chung, K. C., Koo, J. S., Yang, E. J., Choi, J. Y. and Yoon, J. H. (2003). Interleukin-1 beta and tumor necrosis factor-alpha induce MUC5AC overexpression through a mechanism involving ERK/p38 mitogen-activated protein kinases-MSK1-CREB activation in human airway epithelial cells. J. Biol. Chem. 278, 23243-23250.
38. Sudha, P. S., Devaraj, H. and Devaraj, N. (2001). Adherence of Shigella dysenteriae 1 to human colonic mucin. Curr. Microbiol. 42, 381-387.
39. Takeyama, K., Dabbagh, K., Jeong Shim, J., Dao-Pick, T., Ueki, I. F. and Nadel, J. A. (2000). Oxidative stress causes mucin synthesis via transactivation of epidermal growth factor receptor: role of neutrophils. J. Immunol. 164, 1546-1552.
40. Temann, U. A., Prasad, B., Gallu, M. W., Basbaum, C., Ho, S. B., Flavell, R. A. and Rankin, J. A. (1997). A novel role for murine IL-4 in vivo: induction of MUC5ac gene expression and mucin hypersecretion. Am. J. Respir. Cell Mol. Biol. 16, 471-478.
41. Thirumala-Devi, K., Lamkanfi, M. and Núñ ez, G. (2007). Intracellular NOD-like Receptors in Host Defense and Disease. Immunity. 27, 549-559.
42. Udhayakumar, G., Jayanthi, V., Devaraj, S. N. and Devaraj, H. (2007). Interaction of MUC1 with beta-catenin modulates the Wnt target gene cyclinD1 in H. pyloriinduced gastric cancer. Mol. Carcinog. 46, 807-817.
43. Weiss, A. A., Babyatsky, M. W., Ogata, S., Chen, A. and Itzkowitz, S. H. (1996). Expression of MUC2 and MUC3 mRNA in human normal, malignant and inflammatory intestinal tissues. J. Histochem. Cytochem. 44, 1161-1166.
44. Wright, N. A., Hoffmann, W., Otto, W. R., Rio, M. C. and Thim, L. (1997). Rolling in the clover: trefoil factor family (TFF)-domain peptides, cell migration and cancer. FEBS Lett. 408, 121-123.
45. Yasunori, O., Fayyaz, S. and Sutterwala, R. A. F. (2006). The inflammasome: first line of the immune response to cell stress. Cell 126, 659-662.
46. Zaretsky, J. Z., Sarid, R., Aylon, Y., Mittelman, L. A., Wreschner, D. H. and Keydar, I. (1999). Analysis of the promoter of the MUC1 gene overexpressed in breast cancer. FEBS Lett. 46, 189-195.
47. Zen, Y., Harada, K., Sasaki, M., Tsuneyama, K., Katayanagi, K., Yamamoto, Y. and Nakanuma, Y. (2002). Lipopolysaccharide induces overexpression of MUC2 and MUC5AC in cultured biliary epithelial cells: possible key phenomenon of hepatolithiasis. Am. J. Pathol. 161, 1475-1484.
48. Zweibaum, A., Pinto, M., Chevalier, G., Dussaulx, E., Triadou, N., Lacroix, B., Haffen, K., Brun, J. L. and Rousset, M. (1985). Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose. J. Cell Physiol. 22, 21-29.
49. Zychlinsky, A., Fitting, C., Cavaillon, J. M. and Sansonetti, P. J. (1994). Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri. J. Clin. Invest. 94, 1328-1332.