Activation of epidermal growth factor receptor mediates mucin production stimulated by p40, a Lactobacillus rhamnosus GG-derived protein

Journal of Biological Chemistry

Volumn 289, Issue 29, 2014, Pages 20234-20244

  Wang, Lihong ^a   Cao, Hailong ^b   Liu, Liping ^a   Wang, Bangmao ^b   Walker, W Allan ^c   Acra, Sari A ^a   Yan, Fang ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; BACILLI; BODY FLUIDS; CELL DEATH; CHEMICAL ACTIVATION; ENZYMES; GENE EXPRESSION; PROTEINS;

BARRIER FUNCTIONS; CONCENTRATION-DEPENDENT MANNERS; DOMINANT NEGATIVE; EPIDERMAL GROWTH FACTOR RECEPTORS; GASTROINTESTINAL TRACT; INTESTINAL EPITHELIAL CELLS; INTESTINAL EPITHELIUM; LACTOBACILLUS RHAMNOSUS;

MOLECULAR BIOLOGY;

MUCIN; MUCIN 2; PROTEIN KINASE B; PROTEIN P40; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL LINE; COLITIS; COLON MUCOSA; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REPRESSION; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC TRANSFECTION; GOBLET CELL; INTESTINE INJURY; LACTOBACILLUS RHAMNOSUS; MOUSE; MUC2 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; PROTEIN TARGETING;

APOPTOSIS; EPIDERMAL GROWTH FACTOR RECEPTOR (EGFR); GOBLET CELL; INTESTINE; LACTOBACILLUS RHAMNOSUS GG; MUCIN; MUCUS; PROBIOTIC; PROBIOTICS;

ANIMALS; APOPTOSIS; BACTERIAL PROTEINS; CELL LINE; COLON; HUMANS; INTESTINAL MUCOSA; LACTOBACILLUS RHAMNOSUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCIN-2; MUCINS; PROBIOTICS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, SMALL INTERFERING; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84904512621     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.553800     Document Type: Article

References (51)

1. Johansson, M. E., Sjövall, H., and Hansson, G. C. (2013) The gastrointestinal mucus system in health and disease. Nat. Rev. Gastroenterol. Hepatol. 10, 352-361
2. Kim, Y. S., and Ho, S. B. (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr. Gastroenterol. Rep. 12, 319-330
3. Rubin, B. K. (2002) Physiology of airway mucus clearance. Respir. Care 47, 761-768
4. 2+ and protein kinase C. Exp. Eye Res. 71, 619-628
5. Dharmani, P., Srivastava, V., Kissoon-Singh, V., and Chadee, K. (2009) Role of intestinal mucins in innate host defense mechanisms against pathogens. J. Innate Immun. 1, 123-135
6. Button, B., Cai, L. H., Ehre, C., Kesimer, M., Hill, D. B., Sheehan, J. K., Boucher, R. C., and Rubinstein, M. (2012)Apericiliary brush promotes the lung health by separating the mucus layer from airway epithelia. Science 337, 937-941
7. Ermund, A., Schütte, A., Johansson, M. E., Gustafsson, J. K., and Hansson, G. C. (2013) Studies of mucus in mouse stomach, small intestine, and colon: I. gastrointestinal mucus layers have different properties depending on location as well as over the Peyer's patches. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G341-G347
8. Rodríguez-Piñeiro, A. M., Bergström, J. H., Ermund, A., Gustafsson, J. K., Schütte, A., Johansson, M. E., and Hansson, G. C. (2013) Studies of mucus in mouse stomach, small intestine, and colon: II. gastrointestinal mucus proteome reveals Muc2 and Muc5ac accompanied by a set of core proteins. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G348-G356
9. Johansson, M. E., Gustafsson, J. K., Holmén-Larsson, J., Jabbar, K. S., Xia, L., Xu, H., Ghishan, F. K., Carvalho, F. A., Gewirtz, A. T., Sjövall, H., and Hansson, G. C. (2014) Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut 63, 281-291
10. McElroy, S. J., Prince, L. S., Weitkamp, J. H., Reese, J., Slaughter, J. C., and Polk, D. B. (2011) Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: a potential role in neonatal necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G656-G666
11. Van der Sluis, M., De Koning, B. A., De Bruijn, A. C., Velcich, A., Meijerink, J. P., Van Goudoever, J. B., Büller, H. A., Dekker, J., Van Seuningen, I., Renes, I. B., and Einerhand, A. W. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131, 117-129 (Pubitemid 44015753)
12. Mattar, A. F., Teitelbaum, D. H., Drongowski, R. A., Yongyi, F., Harmon, C. M., and Coran, A. G. (2002) Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr. Surg. Int. 18, 586-590 (Pubitemid 36069911)
13. Mack, D. R., Michail, S., Wei, S., McDougall, L., and Hollingsworth, M. A. (1999) Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am. J. Physiol. 276, G941-G950 (Pubitemid 29214108)
14. Yarden, Y. (2001) The EGFR family and its ligands in human cancer: signalling mechanisms and therapeutic opportunities. Eur. J. Cancer 37, (Suppl. 4) S3-S8
15. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137 (Pubitemid 33674041)
16. Nadel, J. A. (2001) Role of epidermal growth factor receptor activation in regulating mucin synthesis. Respir. Res. 2, 85-89
17. Gorbach, S. L. (1996) The discovery of Lactobacillus GG. Nutr. Today 31, 2S-4S
18. Zocco, M. A., dal Verme, L. Z., Cremonini, F., Piscaglia, A. C., Nista, E. C., Candelli, M., Novi, M., Rigante, D., Cazzato, I. A., Ojetti, V., Armuzzi, A., Gasbarrini, G., and Gasbarrini, A. (2006) Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment. Pharmacol. Ther. 23, 1567-1574 (Pubitemid 43727463)
19. Basu, S., Paul, D. K., Ganguly, S., Chatterjee, M., and Chandra, P. K. (2009) Efficacy of high-dose Lactobacillus rhamnosus GG in controlling acute watery diarrhea in Indian children: a randomized controlled trial. J. Clin. Gastroenterol. 43, 208-213
20. Szajewska, H., Wanke, M., and Patro, B. (2011) Meta-analysis: the effects of Lactobacillus rhamnosus GG supplementation for the prevention of healthcare-associated diarrhoea in children. Aliment. Pharmacol. Ther. 34, 1079-1087
21. Doron, S., Snydman, D. R., and Gorbach, S. L. (2005) Lactobacillus GG: bacteriology and clinical applications. Gastroenterol. Clin. North Am. 34, 483-498 (Pubitemid 41097279)
22. Yan, F., Cao, H., Cover, T. L., Whitehead, R., Washington, M. K., and Polk, D. B. (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132, 562-575 (Pubitemid 46274659)
23. Seth, A., Yan, F., Polk, D. B., and Rao, R. K. (2008) Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1060-G1069 (Pubitemid 351520059)
24. Yan, F., Liu, L., Dempsey, P. J., Tsai, Y. H., Raines, E. W., Wilson, C. L., Cao, H., Cao, Z., Liu, L., and Polk, D. B. (2013) A Lactobacillus rhamnosus GG-derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. J. Biol. Chem. 288, 30742-30751
25. Yan, F., Cao, H., Cover, T. L., Washington, M. K., Shi, Y., Liu, L., Chaturvedi, R., Peek, R. M., Jr., Wilson, K. T., and Polk, D. B. (2011) Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J. Clin. Invest. 121, 2242-2253
26. Lee, D., Cross, S. H., Strunk, K. E., Morgan, J. E., Bailey, C. L., Jackson, I. J., and Threadgill, D. W. (2004) Wa5 is a novel ENU-induced antimorphic allele of the epidermal growth factor receptor. Mamm. Genome 15, 525-536 (Pubitemid 38798843)
27. Whitehead, R. H., Demmler, K., Rockman, S. P., and Watson, N. K. (1999) Clonogenic growth of epithelial cells from normal colonic mucosa from both mice and humans. Gastroenterology 117, 858-865 (Pubitemid 29468228)
28. Garcia, M. A., Yang, N., and Quinton, P. M. (2009) Normal mouse intestinal mucus release requires cystic fibrosis transmembrane regulator-dependent bicarbonate secretion. J. Clin. Invest. 119, 2613-2622
29. Takeyama, K., Dabbagh, K., Lee, H. M., Agustí, C., Lausier, J. A., Ueki, I. F., Grattan, K. M., and Nadel, J. A. (1999) Epidermal growth factor system regulates mucin production in airways. Proc. Natl. Acad. Sci. U.S.A. 96, 3081-3086 (Pubitemid 29148847)
30. Liu, L., Fishman, M. L., Hicks, K. B., Kende, M., and Ruthel, G. (2006) Pectin/zein beads for potential colon-specific drug delivery: synthesis and in vitro evaluation. Drug Deliv. 13, 417-423 (Pubitemid 44470221)
31. Liu, L., Fishman, M. L., Kost, J., and Hicks, K. B. (2003) Pectin-based systems for colon-specific drug delivery via oral route. Biomaterials 24, 3333-3343 (Pubitemid 36581891)
32. Kuan, S. F., Byrd, J. C., Basbaum, C., and Kim, Y. S. (1989) Inhibition of mucin glycosylation by aryl-N-acetyl-α-galactosaminides in human colon cancer cells. J. Biol. Chem. 264, 19271-19277 (Pubitemid 19285840)
33. Truant, S., Bruyneel, E., Gouyer, V., De Wever, O., Pruvot, F. R., Mareel, M., and Huet, G. (2003) Requirement of both mucins and proteoglycans in cell-cell dissociation and invasiveness of colon carcinoma HT-29 cells. Int. J. Cancer 104, 683-694 (Pubitemid 36418504)
34. Vanderpool, C., Yan, F., and Polk, D. B. (2008) Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases. Inflamm. Bowel Dis. 14, 1585-1596
35. Mack, D. R., Ahrne, S., Hyde, L., Wei, S., and Hollingsworth, M. A. (2003) Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52, 827-833 (Pubitemid 36613489)
36. Oksvold, M. P., Thien, C. B., Widerberg, J., Chantry, A., Huitfeldt, H. S., and Langdon, W. Y. (2003) Serine mutations that abrogate ligand-induced ubiquitination and internalization of the EGF receptor do not affect c-Cbl association with the receptor. Oncogene 22, 8509-8518 (Pubitemid 37523902)
37. de Melker, A. A., van der Horst, G., and Borst, J. (2004) c-Cbl directs EGF receptors into an endocytic pathway that involves the ubiquitin-interacting motif of Eps15. J. Cell Sci. 117, 5001-5012 (Pubitemid 39517516)
38. Dikic, I., and Giordano, S. (2003) Negative receptor signalling. Curr. Opin. Cell Biol. 15, 128-135 (Pubitemid 36332186)
39. Bucci, M., Roviezzo, F., Cicala, C., Sessa, W. C., and Cirino, G. (2000) Geldanamycin, an inhibitor of heat shock protein 90 (Hsp90) mediated signal transduction has anti-inflammatory effects and interacts with glucocorticoid receptor in vivo. Br J. Pharmacol. 131, 13-16
40. de Renzis, S., Sönnichsen, B., and Zerial, M. (2002) Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat. Cell Biol. 4, 124-133 (Pubitemid 34141478)
41. Perrais, M., Pigny, P., Copin, M. C., Aubert, J. P., and Van Seuningen, I. (2002) Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J. Biol. Chem. 277, 32258-32267 (Pubitemid 34969042)
42. 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-1β 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
43. Davis, C. W., and Dickey, B. F. (2008) Regulated airway goblet cell mucin secretion. Annu. Rev. Physiol. 70, 487-512 (Pubitemid 351738189)
44. Hodges, R. R., Bair, J. A., Carozza, R. B., Li, D., Shatos, M. A., and Dartt, D. A. (2012) Signaling pathways used by EGF to stimulate conjunctival goblet cell secretion. Exp. Eye Res. 103, 99-113
45. Okamoto, R., Tsuchiya, K., Nemoto, Y., Akiyama, J., Nakamura, T., Kanai, T., and Watanabe, M. (2009) Requirement of Notch activation during regeneration of the intestinal epithelia. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G23-G35
46. Engelman, J. A., Zejnullahu, K., Mitsudomi, T., Song, Y., Hyland, C., Park, J. O., Lindeman, N., Gale, C. M., Zhao, X., Christensen, J., Kosaka, T., Holmes, A. J., Rogers, A. M., Cappuzzo, F., Mok, T., Lee, C., Johnson, B. E., Cantley, L. C., and Jänne, P. A. (2007) MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316, 1039-1043 (Pubitemid 46799492)
47. Noah, T. K., Kazanjian, A., Whitsett, J., and Shroyer, N. F. (2010) SAM pointed domain ETS factor (SPDEF) regulates terminal differentiation and maturation of intestinal goblet cells. Exp. Cell Res. 316, 452-465
48. Hansson, G. C. (2012) Role of mucus layers in gut infection and inflammation. Curr. Opin. Microbiol. 15, 57-62
49. Swidsinski, A., Loening-Baucke, V., Theissig, F., Engelhardt, H., Bengmark, S., Koch, S., Lochs, H., and Dörffel, Y. (2007) Comparative study of the intestinal mucus barrier in normal and inflamed colon. Gut 56, 343-350 (Pubitemid 46579762)
50. Fu, J., Wei, B., Wen, T., Johansson, M. E., Liu, X., Bradford, E., Thomsson, K. A., McGee, S., Mansour, L., Tong, M., McDaniel, J. M., Sferra, T. J., Turner, J. R., Chen, H., Hansson, G. C., Braun, J., and Xia, L. (2011) Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice. J. Clin. Invest. 121, 1657-1666
51. Martens, E. C., Roth, R., Heuser, J. E., and Gordon, J. I. (2009) Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J. Biol. Chem. 284, 18445-18457