STAT6 silencing up-regulates cholesterol synthesis via miR-197/FOXJ2 axis and induces ER stress-mediated apoptosis in lung cancer cells

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 1, 2015, Pages 32-43

  Dubey, Richa ^a   Saini, Neeru ^a  

^a CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

Author keywords

Apoptosis; Cholesterol; ER stress; FOXJ2; MiRNA 197; STAT6

Indexed keywords

BH3 PROTEIN; CHOLESTEROL; MICRORNA; MICRORNA 197; SMALL INTERFERING RNA; STAT6 PROTEIN; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXJ2 PROTEIN, HUMAN; MIRN197 MICRORNA, HUMAN; STAT6 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; HUMAN; HUMAN CELL; LUNG CANCER CELL LINE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; BINDING SITE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; PATHOLOGY; TUMOR CELL LINE;

APOPTOSIS; BINDING SITES; CELL LINE, TUMOR; CHOLESTEROL; ENDOPLASMIC RETICULUM STRESS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MICRORNAS; STAT6 TRANSCRIPTION FACTOR;

EID: 84912006743     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.10.002     Document Type: Article

References (55)

1. Le T.D., Liu L., Liu B., Tsykin A., Goodall G.J., Satou K., Li J. Inferring microRNA and transcription factor regulatory networks in heterogeneous data. BMC Bioinforma. 2013, 14:92.
2. Nazarov P.V., Reinsbach S.E., Muller A., Nicot N., Philippidou D., Vallar L., Kreis S. Interplay of microRNAs, transcription factors and target genes: linking dynamic expression changes to function. Nucleic Acids Res. 2013, 41:2817.
3. Poos K., Smida J., Nathrath M., Maugg D., Baumhoer D., Korsching E. How microRNA and transcription factor co-regulatory networks affect osteosarcoma cell proliferation. PLoS Comput. Biol. 2013, 9:e1003210.
4. Bromberg J. Stat proteins and oncogenesis. J. Clin. Invest. 2002, 109:1139.
5. Haura E.B., Turkson J., Jove R. Mechanisms of disease: insights into the emerging role of signal transducers and activators of transcription in cancer. Nat. Clin. Pract. Oncol. 2005, 2:315.
6. Turkson J., Jove R. STAT proteins: novel molecular targets for cancer drug discovery. Oncogene 2000, 19:6613.
7. Hebenstreit D., Wirnsberger G., Horejs-Hoeck J., Duschl A. Signaling mechanisms, interaction partners, and target genes of STAT6. Cytokine Growth Factor Rev. 2006, 17:173.
8. Kaplan M.H., Schindler U., Smiley S.T., Grusby M.J. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 1996, 4:313.
9. Kuperman D.A., Schleimer R.P. Interleukin-4, interleukin-13, signal transducer and activator of transcription factor 6, and allergic asthma. Curr. Mol. Med. 2008, 8:384.
10. Wu D., Ahrens R., Osterfeld H., Noah T.K., Groschwitz K., Foster P.S., Steinbrecher K.A., Rothenberg M.E., Shroyer N.F., Matthaei K.I., Finkelman F.D., Hogan S.P. Interleukin-13 (IL-13)/IL-13 receptor alpha1 (IL-13Ralpha1) signaling regulates intestinal epithelial cystic fibrosis transmembrane conductance regulator channel-dependent Cl- secretion. J. Biol. Chem. 2011, 286(15):13357-13369.
11. Jaruga B., Hong F., Sun R., Radaeva S., Gao B. Crucial role of IL-4/STAT6 in T cell-mediated hepatitis: up-regulating eotaxins and IL-5 and recruiting leukocytes. J. Immunol. 2003, 171:3233.
12. Olsan E.E., Mukherjee S., Wulkersdorfer B., Shillingford J.M., Giovannone A.J., Todorov G., Song X., Pei Y., Weimbs T. Signal transducer and activator of transcription-6 (STAT6) inhibition suppresses renal cyst growth in polycystic kidney disease. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18067.
13. Bruns H.A., Kaplan M.H. The role of constitutively active Stat6 in leukemia and lymphoma. Crit. Rev. Oncol. Hematol. 2006, 57:245.
14. Das S., Roth C.P., Wasson L.M., Vishwanatha J.K. Signal transducer and activator of transcription-6 (STAT6) is a constitutively expressed survival factor in human prostate cancer. Prostate 2007, 67:1550.
15. Li B.H., Xu S.B., Li F., Zou X.G., Saimaiti A., Simayi D., Wang Y.H., Zhang Y., Yuan J., Zhang W.J. Stat6 activity-related Th2 cytokine profile and tumor growth advantage of human colorectal cancer cells in vitro and in vivo. Cell. Signal. 2012, 24:718.
16. Merk B.C., Owens J.L., Lopes M.B., Silva C.M., Hussaini I.M. STAT6 expression in glioblastoma promotes invasive growth. BMC Cancer 2011, 11:184.
17. Jacobs R.J., Voorneveld P.W., Kodach L.L., Hardwick J.C. Cholesterol metabolism and colorectal cancers. Curr. Opin. Pharmacol. 2012, 12:690.
18. Tania M., Khan M.A., Song Y. Association of lipid metabolism with ovarian cancer. Curr. Oncol. 2010, 17:6.
19. Zhang F., Du G. Dysregulated lipid metabolism in cancer. World J. Biol. Chem. 2012, 3:167.
20. Li Y.C., Park M.J., Ye S.K., Kim C.W., Kim Y.N. Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents. Am. J. Pathol. 2006, 168:1107.
21. Lim S.C., Parajuli K.R., Duong H.Q., Choi J.E., Han S.I. Cholesterol induces autophagic and apoptotic death in gastric carcinoma cells. Int. J. Oncol. 2014, 44:805.
22. Oh H.Y., Lee E.J., Yoon S., Chung B.H., Cho K.S., Hong S.J. Cholesterol level of lipid raft microdomains regulates apoptotic cell death in prostate cancer cells through EGFR-mediated Akt and ERK signal transduction. Prostate 2007, 67:1061.
23. Dubey R., Chhabra R., Saini N. Small interfering RNA against transcription factor STAT6 leads to increased cholesterol synthesis in lung cancer cell lines. PLoS ONE 2011, 6:e28509.
24. Ritchie M.E., Silver J., Oshlack A., Holmes M., Diyagama D., Holloway A., Smyth G.K. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007, 23:2700.
25. Xi Y., Shalgi R., Fodstad O., Pilpel Y., Ju J. Differentially regulated micro-RNAs and actively translated messenger RNA transcripts by tumor suppressor p53 in colon cancer. Clin. Cancer Res. 2006, 12:2014.
26. Singh R., Saini N. Downregulation of BCL2 by miRNAs augments drug-induced apoptosis-a combined computational and experimental approach. J. Cell Sci. 2012, 125:1568.
27. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
28. Chhabra R., Adlakha Y.K., Hariharan M., Scaria V., Saini N. Upregulation of miR-23a-27a-24-2 cluster induces caspase-dependent and -independent apoptosis in human embryonic kidney cells. PLoS ONE 2009, 4:e5848.
29. Yadav V., Sultana S., Yadav J., Saini N. Gatifloxacin induces S and G2-phase cell cycle arrest in pancreatic cancer cells via p21/p27/p53. PLoS ONE 2012, 7:e47796.
30. Adlakha Y.K., Saini N. miR-128 exerts pro-apoptotic effect in a p53 transcription-dependent and -independent manner via PUMA-Bak axis. Cell Death Dis. 2013, 4:e542.
31. Goel A., Prasad A.K., Parmar V.S., Ghosh B., Saini N. Apoptogenic effect of 7,8-diacetoxy-4-methylcoumarin and 7,8-diacetoxy-4-methylthiocoumarin in human lung adenocarcinoma cell line: role of NF-kappaB, Akt, ROS and MAP kinase pathway. Chem. Biol. Interact. 2009, 179:363.
32. Goel A., Prasad A.K., Parmar V.S., Ghosh B., Saini N. 7,8-Dihydroxy-4-methylcoumarin induces apoptosis of human lung adenocarcinoma cells by ROS-independent mitochondrial pathway through partial inhibition of ERK/MAPK signaling. FEBS Lett. 2007, 581:2447.
33. Norman A.W., Demel R.A., de Kruyff B., van Deenen L.L. Studies on the biological properties of polyene antibiotics. Evidence for the direct interaction of filipin with cholesterol. J. Biol. Chem. 1972, 247:1918.
34. Scull C.M., Tabas I. Mechanisms of ER stress-induced apoptosis in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2792.
35. Devries-Seimon T.1., Li Y., Yao P.M., Stone E., Wang Y., Davis R.J., Flavell R., Tabas I. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J. Cell Biol. 2005, 171:61.
36. Malhotra J.D., Kaufman R.J. ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb. Perspect. Biol. 2011, 3:a004424.
37. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006, 7:880.
38. Basseri S., Austin R.C. Endoplasmic reticulum stress and lipid metabolism: mechanisms and therapeutic potential. Biochem. Res. Int. 2012, 2012:841362.
39. Ricardo-Gonzalez R.R., Red E.A., Odegaard J.I., Jouihan H., Morel C.R., Heredia J.E., Mukundan L., Wu D., Locksley R.M., Chawla A. IL-4/STAT6 immune axis regulates peripheral nutrient metabolism and insulin sensitivity. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:22617.
40. Iff J., Wang W., Sajic T., Oudry N., Gueneau E., Hopfgartner G., Varesio E., Szanto I. Differential proteomic analysis of STAT6 knockout mice reveals new regulatory function in liver lipid homeostasis. J. Proteome Res. 2009, 8:4511.
41. Jeon T.I., Esquejo R.M., Roqueta-Rivera M., Phelan P.E., Moon Y.A., Govindarajan S.S., Esau C.C., Osborne T.F. An SREBP-responsive microRNA operon contributes to a regulatory loop for intracellular lipid homeostasis. Cell Metab. 2013, 18:51.
42. Kohanbash G., Okada H. MicroRNAs and STAT interplay. Semin. Cancer Biol. 2012, 22:70.
43. Sasaki K., Kohanbash G., Hoji A., Ueda R., McDonald H.A., Reinhart T.A., Martinson J., Lotze M.T., Marincola F.M., Wang E., Fujita M., Okada H. miR-17-92 expression in differentiated T cells-implications for cancer immunotherapy. J. Transl. Med. 2010, 8:17.
44. Hamada S., Satoh K., Miura S., Hirota M., Kanno A., Masamune A., Kikuta K., Kume K., Unno J., Egawa S., Motoi F., Unno M., Shimosegawa T. miR-197 induces epithelial-mesenchymal transition in pancreatic cancer cells by targeting p120 catenin. J. Cell. Physiol. 2013, 228:1255.
45. Du L., Schageman J.J., Subauste M.C., Saber B., Hammond S.M., Prudkin L., Wistuba I.I., Ji L., Roth J.A., Minna J.D., Pertsemlidis A. miR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Mol. Cancer Res. 2009, 7:1234.
46. Karolina D.S., Tavintharan S., Armugam A., Sepramaniam S., Pek S.L., Wong M.T., Lim S.C., Sum C.F., Jeyaseelan K. Circulating miRNA profiles in patients with metabolic syndrome. J. Clin. Endocrinol. Metab. 2012, 97:E2271-E2276.
47. Gomez-Ferreria M.A., Rey-Campos J. Functional domains of FOXJ2. J. Mol. Biol. 2003, 329:631.
48. Wang Y., Yang S., Ni Q., He S., Zhao Y., Yuan Q., Li C., Chen H., Zhang L., Zou L., Shen A., Cheng C. Overexpression of forkhead box J2 can decrease the migration of breast cancer cells. J. Cell. Biochem. 2012, 113:2729.
49. Marciniak S.J., Yun C.Y., Oyadomari S., Novoa I., Zhang Y., Jungreis R., Nagata K., Harding H.P., Ron D. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 2004, 18:3066.
50. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004, 11:381.
51. Puthalakath H., O'Reilly L.A., Gunn P., Lee L., Kelly P.N., Huntington N.D., Hughes P.D., Michalak E.M., Kimm-Breschkin J., Motoyama N., Gotoh T., Akira S., Bouillet P., Strasser A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337.
52. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998, 12:982.
53. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 2001, 21:1249.
54. Haupt S., Berger M., Goldberg Z., Haupt Y. Apoptosis-the p53 network. J. Cell Sci. 2003, 116:4077.
55. Li G., Mongillo M., Chin K.T., Harding H., Ron D., Marks A.R., Tabas I. Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J. Cell Biol. 2009, 186:783.