Nuclear factor of activated T-cells 5 increases intestinal goblet cell differentiation through an mTOR/Notch signaling pathway

Molecular Biology of the Cell

Volumn 25, Issue 18, 2014, Pages 2882-2890

  Zhou, Yuning ^a   Wang, Qingding ^a,b   Weiss, Heidi L ^a   Evers, B Mark ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DAMAGE RESPONSE 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MUCIN 2; NOTCH RECEPTOR; SMALL INTERFERING RNA; SODIUM CHLORIDE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT5; UNCLASSIFIED DRUG; DDIT4 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; MUC2 PROTEIN, HUMAN; NFAT5 PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR;

ARTICLE; CATION TRANSPORT; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME REPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GOBLET CELL; HUMAN; HUMAN CELL; INTESTINE MUCOSA; NONHUMAN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING; CACO 2 CELL LINE; HCT116 CELL LINE; HT 29 CELL LINE; METABOLISM; PHYSIOLOGY;

CACO-2 CELLS; CELL DIFFERENTIATION; GOBLET CELLS; HCT116 CELLS; HT29 CELLS; HUMANS; MUCIN-2; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84907221167     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-05-0998     Document Type: Article

References (59)

1. Aramburu J, Drews-Elger K, Estrada-Gelonch A, Minguillon J, Morancho B, Santiago V, Lopez-Rodriguez C (2006). Regulation of the hypertonic stress response and other cellular functions by the Rel-like transcription factor NFAT5. Biochem Pharmacol 72, 1597-1604.
2. Barros R, da Costa LT, Pinto-de-Sousa J, Duluc I, Freund JN, David L, Almeida R (2011). CDX2 autoregulation in human intestinal metaplasia of the stomach: impact on the stability of the phenotype. Gut 60, 290-298.
3. Berga-Bolanos R, Drews-Elger K, Aramburu J, Lopez-Rodriguez C (2010). NFAT5 regulates T lymphocyte homeostasis and CD24-dependent T cell expansion under pathologic hypernatremia. J Immunol 185, 6624-6635.
4. Chen M, Sastry SK, O'Connor KL (2011). Src kinase pathway is involved in NFAT5-mediated S100A4 induction by hyperosmotic stress in colon cancer cells. Am J Physiol Cell Physiol 300, C1155-C1163.
5. Cheng H, Leblond CP (1974). Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian theory of the origin of the four epithelial cell types. Am J Anat 141, 537-561.
6. Clark JA, Doelle SM, Halpern MD, Saunders TA, Holubec H, Dvorak K, Boitano SA, Dvorak B (2006). Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. Am J Physiol Gastrointest Liver Physiol 291, G938-G949.
7. Corradetti MN, Inoki K, Guan KL (2005). The stress-inducted proteins RTP801 and RTP801L are negative regulators of the mammalian target of rapamycin pathway. J Biol Chem 280, 9769-9772.
8. Deng L, Zhou JF, Sellers RS, Li JF, Nguyen AV, Wang Y, Orlofsky A, Liu Q, Hume DA, Pollard JW, et al. (2010). A novel mouse model of inflammatory bowel disease links mammalian target of rapamycin-dependent hyperproliferation of colonic epithelium to inflammation-associated tumorigenesis. Am J Pathol 176, 952-967.
9. DeYoung MP, Horak P, Sofer A, Sgroi D, Ellisen LW (2008). Hypoxia regulates TSC1/2-mTOR signaling and tumor suppression through REDD1-mediated 14-3-3 shuttling. Genes Dev 22, 239-251.
10. Einerhand AW, Renes IB, Makkink MK, van der Sluis M, Buller HA, Dekker J (2002). Role of mucins in inflammatory bowel disease: important lessons from experimental models. Eur J Gastroenterol Hepatol 14, 757-765.
11. Fawcett TW, Martindale JL, Guyton KZ, Hai T, Holbrook NJ (1999). Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem J 339, 135-141.
12. Feng Q, Zou X, Lu L, Li Y, Liu Y, Zhou J, Duan C (2012). The stress-response gene redd1 regulates dorsoventral patterning by antagonizing Wnt/β-catenin activity in zebrafish. PLoS One 7, e52674.
13. Francipane MG, Lagasse E (2013). Selective targeting of human colon cancer stem-like cells by the mTOR inhibitor Torin-1. Oncotarget 4, 1948-1962.
14. Garcia-Maurino S, Alcaide A, Dominguez C (2012). Pharmacological control of autophagy: therapeutic perspectives in inflammatory bowel disease and colorectal cancer. Curr Pharm Des 18, 3853-3873.
15. Garg P, Ravi A, Patel NR, Roman J, Gewirtz AT, Merlin D, Sitaraman SV (2007). Matrix metalloproteinase-9 regulates MUC-2 expression through its effect on goblet cell differentiation. Gastroenterology 132, 1877-1889.
16. Gersemann M, Wehkamp J, Stange EF (2012). Innate immune dysfunction in inflammatory bowel disease. J Intern Med 271, 421-428.
17. Gingras AC, Raught B, Sonenberg N (2001). Regulation of translation initiation by FRAP/mTOR. Genes Dev 15, 807-826.
18. Gobbi G, Marcantonio DD, Micheloni C, Carubbi C, Galli D, Vaccarezza M, Bucci G, Vitale M, Mirandola P (2012). TRAIL up-regulation must be accompanied by a reciprocal PKC? down-regulation during differentiation of colonic epithelial cell: implications for colorectal cancer cell differentiation. J Cell Physiol 227, 630-638.
19. Guertin DA, Sabatini DM (2007). Defining the role of mTOR in cancer. Cancer Cell 12, 9-22.
20. Heuberger J, Kosel F, Qi J, Grossmann KS, Rajewsky K, Birchmeier W (2014). Shp2/MAPK signaling controls goblet/Paneth cell fate decisions in the intestine. Proc Natl Acad Sci USA 111, 3472-3477.
21. Huang T, Xie Z, Wang J, Li M, Jing N, Li L (2011). Nuclear factor of activated T cells (NFAT) proteins repress canonical Wnt signaling via its interaction with Dishevelled (Dvl) protein and participate in regulating neural progenitor cell proliferation and differentiation. J Biol Chem 286, 37399-37405.
22. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, et al. (2006). TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126, 955-968.
23. Jin HO, Seo SK, Kim YS, Woo SH, Lee KH, Yi JY, Lee SJ, Choe TB, Lee JH, An S, et al. (2011). TXNIP potentiates Redd1-induced mTOR suppression through stabilization of Redd1. Oncogene 30, 3792-3801.
24. Kao SC, Wu H, Xie J, Chang CP, Ranish JA, Graef IA, Crabtree GR (2009). Calcineurin/NFAT signaling is required for neuregulin-regulated Schwann cell differentiation. Science 323, 651-654.
25. Kim JH, Yoon MS, Chen J (2009). Signal transducer and activator of transcription 3 (STAT3) mediates amino acid inhibition of insulin signaling through serine 727 phosphorylation. J Biol Chem 284, 35425-35432.
26. Kim S, Domon-Dell C, Kang J, Chung DH, Freund JN, Evers BM (2004). Down-regulation of the tumor suppressor PTEN by the tumor necrosis factor-α/nuclear factor-κB (NF-κB)-inducing kinase/NF-κB pathway is linked to a default IκB-α autoregulatory loop. J Biol Chem 279, 4285-4291.
27. Li H, Lee J, He C, Zou MH, Xie Z (2014). Suppression of the mTORC1/STAT3/Notch1 pathway by activated AMPK prevents hepatic insulin resistance induced by excess amino acids. Am J Physiol Endocrinol Metab 306, E197-E209.
28. Lopez-Rodriguez C, Antos CL, Shelton JM, Richardson JA, Lin F, Novobrantseva TI, Bronson RT, Igarashi P, Rao A, Olson EN (2004). Loss of NFAT5 results in renal atrophy and lack of tonicity-responsive gene expression. Proc Natl Acad Sci USA 101, 2392-2397.
29. Lopez-Rodriguez C, Aramburu J, Jin L, Rakeman AS, Michino M, Rao A (2001). Bridging the NFAT and NF-κB families: NFAT5 dimerization regulates cytokine gene transcription in response to osmotic stress. Immunity 15, 47-58.
30. Lopez-Rodriguez C, Aramburu J, Rakeman AS, Rao A (1999). NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc Natl Acad Sci USA 96, 7214-7219.
31. Lu P, Sodhi CP, Hackam DJ (2014). Toll-like receptor regulation of intestinal development and inflammation in the pathogenesis of necrotizing enterocolitis. Pathophysiology 21, 81-93.
32. Luo ML, Shen XM, Zhang Y, Wei F, Xu X, Cai Y, Zhang X, Sun YT, Zhan QM, Wu M, et al. (2006). Amplification and overexpression of CTTN (EMS1) contribute to the metastasis of esophageal squamous cell carcinoma by promoting cell migration and anoikis resistance. Cancer Res 66, 11690-11699.
33. Ma J, Meng Y, Kwiatkowski DJ, Chen X, Peng H, Sun Q, Zha X, Wang F, Wang Y, Jing Y, et al. (2010). Mammalian target of rapamycin regulates murine and human cell differentiation through STAT3/p63/Jagged/Notch cascade. J Clin Invest 120, 103-114.
34. Mair M, Zollner G, Schneller D, Musteanu M, Fickert P, Gumhold J, Schuster C, Fuchsbichler A, Bilban M, Tauber S, et al. (2010). Signal transducer and activator of transcription 3 protects from liver injury and fibrosis in a mouse model of sclerosing cholangitis. Gastroenterology 138, 2499-2508.
35. Mak AB, Nixon AM, Kittanakom S, Stewart JM, Chen GI, Curak J, Gingras AC, Mazitschek R, Neel BG, Stagljar I, et al. (2012). Regulation of CD133 by HDAC6 promotes β-catenin signaling to suppress cancer cell differentiation. Cell Rep 2, 951-963.
36. Makky K, Tekiela J, Mayer AN (2007). Target of rapamycin (TOR) signaling controls epithelial morphogenesis in the vertebrate intestine. Dev Biol 303, 501-513.
37. Mungrue IN, Pagnon J, Kohannim O, Gargalovic PS, Lusis AJ (2009). CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J Immunol 182, 466-476.
38. Neuhofer W (2010). Role of NFAT5 in inflammatory disorders associated with osmotic stress. Curr Genomics 11, 584-590.
39. O'Connor RS, Mills ST, Jones KA, Ho SN, Pavlath GK (2007). A combinatorial role for NFAT5 in both myoblast migration and differentiation during skeletal muscle myogenesis. J Cell Sci 120, 149-159.
40. Pear WS (2010). New roles for Notch in tuberous sclerosis. J Clin Invest 120, 84-87.
41. Puglisi RN, Strande L, Santos M, Schulte G, Hewitt CW, Whalen TV (1996). Beneficial effects of cyclosporine and rapamycin in small bowel ischemic injury. J Surg Res 65, 115-118.
42. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall WS, Khvorova A (2004). Rational siRNA design for RNA interference. Nat Biotech 22, 326-330.
43. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, Batlle E, Simon-Assmann P, Clevers H, Nathke IS, et al. (2004). Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18, 1385-1390.
44. Santini MP, Talora C, Seki T, Bolgan L, Dotto GP (2001). Cross talk among calcineurin, Sp1/Sp3, and NFAT in control of p21(WAF1/CIP1) expression in keratinocyte differentiation. Proc Natl Acad Sci USA 98, 9575-9580.
45. Shirazi T, Longman RJ, Corfield AP, Probert CS (2000). Mucins and inflammatory bowel disease. Postgrad Med J 76, 473-478.
46. Sikandar SS, Pate KT, Anderson S, Dizon D, Edwards RA, Waterman ML, Lipkin SM (2010). NOTCH signaling is required for formation and self-renewal of tumor-initiating cells and for repression of secretory cell differentiation in colon cancer. Cancer Res 70, 1469-1478.
47. Sodhi CP, Neal MD, Siggers R, Sho S, Ma C, Branca MF, Prindle T Jr, Russo AM, Afrazi A, Good M, et al. (2012). Intestinal epithelial Toll-like receptor 4 regulates goblet cell development and is required for necrotizing enterocolitis in mice. Gastroenterology 143, 708-718.
48. Tytgat KM, Bovelander FJ, Opdam FJ, Einerhand AW, Buller HA, Dekker J (1995). Biosynthesis of rat MUC2 in colon and its analogy with human MUC2. Biochem J 309, 221-229.
49. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, et al. (2002). The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250.
50. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, et al. (2005). Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435, 959-963.
51. Vooijs M, Liu Z, Kopan R (2011). Notch: architect, landscaper, and guardian of the intestine. Gastroenterology 141, 448-459.
52. Wang Q, Wang X, Evers BM (2003). Induction of cIAP-2 in human colon cancer cells through PKC delta/NF-κ B. J Biol Chem 278, 51091-51099.
53. Wang Q, Wang X, Hernandez A, Kim S, Evers BM (2001). Inhibition of the phosphatidylinositol 3-kinase pathway contributes to HT29 and Caco-2 intestinal cell differentiation. Gastroenterology 120, 1381-1392.
54. Wang Q, Zhou Y, Jackson LN, Johnson SM, Chow CW, Evers BM (2011). Nuclear factor of activated T cells (NFAT) signaling regulates PTEN expression and intestinal cell differentiation. Mol Biol Cell 22, 412-420.
55. Wang Q, Zhou Y, Rychahou P, Liu C, Weiss HL, Evers BM (2013). NFAT5 represses canonical Wnt signaling via inhibition of β-catenin acetylation and participates in regulating intestinal cell differentiation. Cell Death Dis 4, e671.
56. Wang Q, Zhou Y, Wang X, Evers BM (2006). Glycogen synthase kinase-3 is a negative regulator of extracellular signal-regulated kinase. Oncogene 25, 43-50.
57. Wang S, Evers BM (1999). Caco-2 cell differentiation is associated with a decrease in stat protein levels and binding. J Gastrointest Surg 3, 200-207.
58. Yeung TM, Chia LA, Kosinski CM, Kuo CJ (2011). Regulation of self-renewal and differentiation by the intestinal stem cell niche. Cell Mol Life Sci 68, 2513-2523.
59. Zhou Y, Wang Q, Guo Z, Weiss HL, Evers BM (2012). Nuclear factor of activated T-cell c3 inhibition of mammalian target of rapamycin signaling through induction of regulated in development and DNA damage response 1 in human intestinal cells. Mol Biol Cell 23, 2963-2972.