Regulation of the unfolded protein response by microRNAs

• Autorzy: Bartoszewska S. , Kochan K. , Madanecki P. , Piotrowski A. , Ochocka R. , Collawn J. F. , Bartoszewski R.
• Języki publikacji: EN

Abstrakty

EN

The unfolded protein response (UPR) is an adaptive response to the stress that is caused by an accumulation of misfolded proteins in the lumen of the endoplasmic reticulum (ER). It is an important component of cellular homeostasis. During ER stress, the UPR increases the protein-folding capacity of the endoplasmic reticulum to relieve the stress. Failure to recover leads to apoptosis. Specific cellular mechanisms are required for the cellular recovery phase after UPR activation. Using bioinformatics tools, we identified a number of microRNAs that are predicted to decrease the mRNA expression levels for a number of critical components of the UPR. In this review, we discuss the potential role of microRNAs as key regulators of this pathway and describe how microRNAs may play an essential role in turning off the UPR after the stress has subsided.

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2013
• Tom: 18
• Numer: 4
• Opis fizyczny: p.555-578,fig.,ref.

Twórcy

autor

Bartoszewska S.

• Department of Inorganic Chemistry, Medical University of Gdansk, Gdansk, Poland

autor

Kochan K.

• Department of Biology and Pharmaceutical Botany, Medical University of Gdansk, Gdansk, Poland

autor

Madanecki P.

• Department of Biology and Pharmaceutical Botany, Medical University of Gdansk, Gdansk, Poland

autor

Piotrowski A.

• Department of Biology and Pharmaceutical Botany, Medical University of Gdansk, Gdansk, Poland

autor

Ochocka R.

• Department of Biology and Pharmaceutical Botany, Medical University of Gdansk, Gdansk, Poland

autor

Collawn J. F.

• Department of Cell, Developmental and Integrative Biology, University of Alabama at Birmingham, Alabama, USA

autor

Bartoszewski R.

• Department of Biology and Pharmaceutical Botany, Medical University of Gdansk, Gdansk, Poland

Bibliografia

• 1. Ellgaard, L. and Helenius, A. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell. Biol. 4 (2003) 181-191.
• 2. Schroder, M. and Kaufman, R.J. ER stress and the unfolded protein response. Mutat. Res. 569 (2005) 29-63.
• 3. Back, S.H., Schroder, M., Lee, K., Zhang, K. and Kaufman, R.J. ER stress signaling by regulated splicing: IRE1/HAC1/XBP1. Methods 35 (2005) 395-416.
• 4. Wu, J. and Kaufman, R.J. From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ. 13 (2006) 374-384.
• 5. Ron, D. and Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell. Biol. 8 (2007) 519-529.
• 6. Rutkowski, D.T. and Kaufman, R.J. A trip to the ER: coping with stress. Trends Cell Biol. 14 (2004) 20-28.
• 7. Faitova, J., Krekac, D., Hrstka, R. and Vojtesek, B. Endoplasmic reticulum stress and apoptosis. Cell. Mol. Biol. Lett. 11 (2006) 488-505.
• 8. Fonseca, S.G., Gromada, J. and Urano, F. Endoplasmic reticulum stress and pancreatic beta-cell death. Trends Endocrinol. Metab. 7 (2011) 266-274.
• 9. Malhotra, J.D. and Kaufman, R.J. The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 18 (2007) 716-731.
• 10. Malhotra, J.D. and Kaufman, R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. 9 (2007) 2277-2293.
• 11. Haze, K., Yoshida, H., Yanagi, H., Yura, T. and Mori, K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Cell Biol. 10 (1999) 3787-3799.
• 12. Shamu, C.E. and Walter, P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 15 (1996) 3028-3039.
• 13. Schroder, M. and Kaufman, R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005) 739-789.
• 14. Bommiasamy, H., Back, S.H., Fagone, P., Lee, K., Meshinchi, S., Vink, E., Sriburi, R., Frank, M., Jackowski, S., Kaufman, R.J. and Brewer, J.W. ATF6alpha induces XBP1-independent expansion of the endoplasmic reticulum. J. Cell Sci. 122 (2009) 1626-1636.
• 15. Sriburi, R., Jackowski, S., Mori, K. and Brewer, J.W. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167 (2004) 35-41.
• 16. Hollien, J. and Weissman, J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 (2006) 104-107.
• 17. Harding, H.P., Zhang, Y., Zeng, H., Novoa, I., Lu, P.D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R., Stojdl, D.F., Bell, J.C., Hettmann, T., Leiden, J.M. and Ron, D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11 (2003) 619-633.
• 18. Han, J., Back, S.H., Hur, J., Lin, Y.H., Gildersleeve, R., Shan, J., Yuan, C.L., Krokowski, D., Wang, S., Hatzoglou, M., Kilberg, M.S., Sartor, M.A. and Kaufman, R.J. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 15 (2013) 481-490.
• 19. Jackson, R.J., Hellen, C.U.T. and Pestova, T.V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell. Biol. 11 (2010) 113-127.
• 20. Bartoszewski, R., Rab, A., Twitty, G., Stevenson, L., Fortenberry, J., Piotrowski, A., Dumanski, J.P. and Bebok, Z. The mechanism of cystic fibrosis transmembrane conductance regulator transcriptional repression during the unfolded protein response. J. Biol. Chem. 283 (2008) 12154- 12165.
• 21. Durose, J.B., Scheuner, D., Kaufman, R.J., Rothblum, L.I. and Niwa, M. Phosphorylation of eukaryotic translation initiation factor 2alpha coordinates rRNA transcription and translation inhibition during endoplasmic reticulum stress. Mol. Cell Biol. 29 (2009) 4295-4307.
• 22. Harding, H.P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M. and Ron, D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6 (2000) 1099-1108.
• 23. Hollien, J., Lin, J.H., Li, H., Stevens, N., Walter, P. and Weissman, J.S. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186 (2009) 323-331.
• 24. Oda, Y., Okada, T., Yoshida, H., Kaufman, R.J., Nagata, K. and Mori, K. Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J. Cell Biol. 172 (2006) 383-393.
• 25. Bartoszewski, R., Rab, A., Fu, L., Bartoszewska, S., Collawn, J. and Bebok, Z. CFTR expression regulation by the unfolded protein response. Methods Enzymol. 491 (2011) 3-24.
• 26. Bartel, D.P. MicroRNAs: target recognition and regulatory functions. Cell 136 (2009) 215-233.
• 27. Guo, H., Ingolia, N.T., Weissman, J.S. and Bartel, D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466 (2010) 835-840.
• 28. Lin, J.H., Li, H., Yasumura, D., Cohen, H.R., Zhang, C., Panning, B., Shokat, K.M., Lavail, M.M. and Walter, P. IRE1 signaling affects cell fate during the unfolded protein response. Science 318 (2007) 944-949.
• 29. Wang, X.Z., Lawson, B., Brewer, J.W., Zinszner, H., Sanjay, A., Mi, L.J., Boorstein, R., Kreibich, G., Hendershot, L.M. and Ron, D. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 16 (1996) 4273-4280.
• 30. Wang, X.Z. and Ron, D. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP kinase. Science 272 (1996) 1347-1349.
• 31. Putcha, G.V., Le, S., Frank, S., Besirli, C.G., Clark, K., Chu, B., Alix, S., Youle, R.J., Lamarche, A., Maroney, A.C. and Johnson, E.M., Jr. JNKmediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron 38 (2003) 899-914.
• 32. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H.P. and Ron, D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287 (2000) 664- 666.
• 33. Hitomi, J., Katayama, T., Eguchi, Y., Kudo, T., Taniguchi, M., Koyama, Y., Manabe, T., Yamagishi, S., Bando, Y., Imaizumi, K., Tsujimoto, Y. and Tohyama, M. Involvement of caspase-4 in endoplasmic reticulum stressinduced apoptosis and Abeta-induced cell death. J. Cell Biol. 165 (2004) 347-356.
• 34. Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35 (2007) 495-516.
• 35. Li, J., Lee, B. and Lee, A.S. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J. Biol. Chem. 281 (2006) 7260- 7270.
• 36. Hikisz, P. and Kilianska, Z.M. PUMA, a critical mediator of cell death-one decade on from its discovery. Cell. Mol. Biol. Lett. 17 (2012) 646-669.
• 37. Treiber, T., Treiber, N. and Meister, G. Regulation of microRNA biogenesis and function. Thromb. Haemost. 107 (2012) 605-610.
• 38. Nilsen, T.W. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet. 23 (2007) 243-249.
• 39. Filipowicz, W., Bhattacharyya, S.N. and Sonenberg, N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9 (2008) 102-114.
• 40. Djuranovic, S., Nahvi, A. and Green, R. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336 (2012) 237-240.
• 41. Bisognin, A., Sales, G., Coppe, A., Bortoluzzi, S. and Romualdi, C. MAGIA(2): from miRNA and genes expression data integrative analysis to microRNA-transcription factor mixed regulatory circuits (2012 update). Nucleic Acids Res. 40 (2012) W13-21.
• 42. Bushati, N. and Cohen, S.M. microRNA functions. Annu. Rev. Cell Dev. Biol. 23 (2007) 175-205.
• 43. Raisch, J., Darfeuille-Michaud, A. and Nguyen, H.T. Role of microRNAs in the immune system, inflammation and cancer. World J. Gastroenterol. 19 (2013) 2985-2996.
• 44. Listowski, M.A., Heger, E., Boguslawska, D.M., Machnicka, B., Kuliczkowski, K., Leluk, J. and Sikorski, A.F. microRNAs: fine tuning of erythropoiesis. Cell. Mol. Biol. Lett. 18 (2013) 34-46.
• 45. Huang, X., Ding, L., Bennewith, K.L., Tong, R.T., Welford, S.M., Ang, K.K., Story, M., Le, Q.T. and Giaccia, A.J. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol. Cell 35 (2009) 856-867.
• 46. Madanecki, P., Kapoor, N., Bebok, Z., Ochocka, R., Collawn, J.F. and Bartoszewski, R. Regulation of angiogenesis by hypoxia: the role of microRNA. Cell. Mol. Biol. Lett. 18 (2013) 47-57.
• 47. Varga, Z.V., Kupai, K., Szucs, G., Gaspar, R., Paloczi, J., Farago, N., Zvara, A., Puskas, L.G., Razga, Z., Tiszlavicz, L., Bencsik, P., Gorbe, A., Csonka, C., Ferdinandy, P. and Csont, T. MicroRNA-25-dependent upregulation of NADPH oxidase 4 (NOX4) mediates hypercholesterolemiainduced oxidative/nitrative stress and subsequent dysfunction in the heart. J. Mol. Cell Cardiol. 62 (2013) 111-121.
• 48. Xu, S., Zhang, R., Niu, J., Cui, D., Xie, B., Zhang, B., Lu, K., Yu, W., Wang, X. and Zhang, Q. Oxidative stress mediated-alterations of the microRNA expression profile in mouse hippocampal neurons. Int. J. Mol. Sci. 13 (2012) 16945-16960.
• 49. Poy, M.N., Eliasson, L., Krutzfeldt, J., Kuwajima, S., Ma, X., Macdonald, P.E., Pfeffer, S., Tuschl, T., Rajewsky, N., Rorsman, P. and Stoffel, M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432 (2004) 226-230.
• 50. Vigorito, E., Perks, K.L., Abreu-Goodger, C., Bunting, S., Xiang, Z., Kohlhaas, S., Das, P.P., Miska, E.A., Rodriguez, A., Bradley, A., Smith, K.G., Rada, C., Enright, A.J., Toellner, K.M., Maclennan, I.C. and Turner, M. microRNA-155 regulates the generation of immunoglobulin classswitched plasma cells. Immunity 27 (2007) 847-859.
• 51. Bartoszewski, R., Brewer, J.W., Rab, A., Crossman, D.K., Bartoszewska, S., Kapoor, N., Fuller, C., Collawn, J.F. and Bebok, Z. The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J. Biol. Chem. 286 (2011) 41862-41870.
• 52. Behrman, S., Acosta-Alvear, D. and Walter, P. A CHOP-regulated microRNA controls rhodopsin expression. J. Cell. Biol. 192 (2011) 919- 927.
• 53. Byrd, A.E., Aragon, I.V. and Brewer, J.W. MicroRNA-30c-2* limits expression of proadaptive factor XBP1 in the unfolded protein response. J. Cell. Biol. 196 (2012) 689-698.
• 54. Dai, B.H., Geng, L., Wang, Y., Sui, C.J., Xie, F., Shen, R.X., Shen, W.F. and Yang, J.M. microRNA-199a-5p protects hepatocytes from bile acidinduced sustained endoplasmic reticulum stress. Cell Death Dis. 4 (2013) e604.
• 55. Upton, J.P., Wang, L., Han, D., Wang, E.S., Huskey, N.E., Lim, L., Truitt, M., Mcmanus, M.T., Ruggero, D., Goga, A., Papa, F.R. and Oakes, S.A. IRE1alpha cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 338 (2012) 818-822.
• 56. Byrd, A.E. and Brewer, J.W. Micro(RNA)managing endoplasmic reticulum stress. IUBMB Life 65 (2013) 373-381.
• 57. Maurel, M. and Chevet, E. Endoplasmic reticulum stress signaling: the microRNA connection. Am. J. Physiol. Cell Physiol. 304 (2013) C1117- 1126.
• 58. Lee, A.H., Iwakoshi, N.N. and Glimcher, L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell Biol. 23 (2003) 7448-7459.
• 59. Shaffer, A.L., Shapiro-Shelef, M., Iwakoshi, N.N., Lee, A.H., Qian, S.B., Zhao, H., Yu, X., Yang, L., Tan, B.K., Rosenwald, A., Hurt, E.M., Petroulakis, E., Sonenberg, N., Yewdell, J.W., Calame, K., Glimcher, L.H. and Staudt, L.M. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21 (2004) 81-93.
• 60. Belmont, P.J., Chen, W.J., Thuerauf, D.J. and Glembotski, C.C. Regulation of microRNA expression in the heart by the ATF6 branch of the ER stress response. J. Mol. Cell Cardiol. 52 (2012) 1176-1182.
• 61. Yang, F., Zhang, L., Wang, F., Wang, Y., Huo, X.S., Yin, Y.X., Wang, Y.Q. and Sun, S.H. Modulation of the unfolded protein response is the core of microRNA-122-involved sensitivity to chemotherapy in hepatocellular carcinoma. Neoplasia 13 (2011) 590-600.
• 62. Dai, R.Y., Chen, Y., Fu, J., Dong, L.W., Ren, Y.B., Yang, G.Z., Qian, Y.W., Cao, J., Tang, S.H., Yang, S.L. and Wang, H.Y. p28GANK inhibits endoplasmic reticulum stress-induced cell death via enhancement of the endoplasmic reticulum adaptive capacity. Cell Res. 19 (2009) 1243-1257.
• 63. Chhabra, R., Dubey, R. and Saini, N. Gene expression profiling indicate role of ER stress in miR-23a~27a~24-2 cluster induced apoptosis in HEK293T cells. RNA Biol. 8 (2011) 648-664.
• 64. Chhabra, R., Dubey, R. and Saini, N. Cooperative and individualistic functions of the microRNAs in the miR-23a~27a~24-2 cluster and its implication in human diseases. Mol. Cancer 9 (2010) 232.
• 65. Chhabra, R., Adlakha, Y.K., Hariharan, M., Scaria, V. and Saini, N. Upregulation of miR-23a-27a-24-2 cluster induces caspase-dependent and - independent apoptosis in human embryonic kidney cells. PLoS One 4 (2009) e5848.
• 66. Gupta, S., Read, D.E., Deepti, A., Cawley, K., Gupta, A., Oommen, D., Verfaillie, T., Matus, S., Smith, M.A., Mott, J.L., Agostinis, P., Hetz, C. and Samali, A. Perk-dependent repression of miR-106b-25 cluster is required for ER stress-induced apoptosis. Cell Death Dis. 3 (2012) e333.
• 67. Mccullough, K.D., Martindale, J.L., Klotz, L.O., Aw, T.Y. and Holbrook, N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by downregulating Bcl2 and perturbing the cellular redox state. Mol. Cell Biol. 21 (2001) 1249-1259.
• 68. Puthalakath, H., O'reilly, L.A., Gunn, P., Lee, L., Kelly, P.N., Huntington, N.D., Hughes, P.D., Michalak, E.M., Mckimm-Breschkin, J., Motoyama, N., Gotoh, T., Akira, S., Bouillet, P. and Strasser, A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129 (2007) 1337-1349.
• 69. Chitnis, N.S., Pytel, D., Bobrovnikova-Marjon, E., Pant, D., Zheng, H., Maas, N.L., Frederick, B., Kushner, J.A., Chodosh, L.A., Koumenis, C., Fuchs, S.Y. and Diehl, J.A. miR-211 is a prosurvival microRNA that regulates chop expression in a PERK-dependent manner. Mol. Cell 48 (2012) 353-364.
• 70. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107 (2001) 881-891.
• 71. Lipson, K.L., Ghosh, R. and Urano, F. The role of IRE1alpha in the degradation of insulin mRNA in pancreatic beta-cells. PLoS One 3 (2008) e1648.
• 72. Arduino, D.M., Esteves, A.R., Domingues, A.F., Pereira, C.M., Cardoso, S.M. and Oliveira, C.R. ER-mediated stress induces mitochondrialdependent caspases activation in NT2 neuron-like cells. BMB Rep. 42 (2009) 719-724.
• 73. Lerner, A.G., Upton, J.P., Praveen, P.V., Ghosh, R., Nakagawa, Y., Igbaria, A., Shen, S., Nguyen, V., Backes, B.J., Heiman, M., Heintz, N., Greengard, P., Hui, S., Tang, Q., Trusina, A., Oakes, S.A. and Papa, F.R. IRE1alpha induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab. 16 (2012) 250-264.
• 74. Maurel, M., Dejeans, N., Taouji, S., Chevet, E. and Grosset, C.F. MicroRNA-1291-mediated silencing of IRE1alpha enhances Glypican-3 expression. RNA 19 (2013) 778-788.
• 75. Suzuki, M., Sugimoto, K., Tanaka, J., Tameda, M., Inagaki, Y., Kusagawa, S., Nojiri, K., Beppu, T., Yoneda, K., Yamamoto, N., Ito, M., Yoneda, M., Uchida, K., Takase, K. and Shiraki, K. Up-regulation of glypican-3 in human hepatocellular carcinoma. Anticancer Res. 30 (2010) 5055-5061.
• 76. Capurro, M.I., Xiang, Y.Y., Lobe, C. and Filmus, J. Glypican-3 promotes the growth of hepatocellular carcinoma by stimulating canonical Wnt signaling. Cancer Res. 65 (2005) 6245-6254.
• 77. Maurel, M., Jalvy, S., Ladeiro, Y., Combe, C., Vachet, L., Sagliocco, F., Bioulac-Sage, P., Pitard, V., Jacquemin-Sablon, H., Zucman-Rossi, J., Laloo, B. and Grosset, C.F. A functional screening identifies five microRNAs controlling glypican-3: role of miR-1271 down-regulation in hepatocellular carcinoma. Hepatology 57 (2013) 195-204.
• 78. Su, S.F., Chang, Y.W., Andreu-Vieyra, C., Fang, J.Y., Yang, Z., Han, B., Lee, A.S. and Liang, G. miR-30d, miR-181a and miR-199a-5p cooperatively suppress the endoplasmic reticulum chaperone and signaling regulator GRP78 in cancer. Oncogene (2012) DOI: 10.1038/onc.2012.483.
• 79. Luo, D., He, Y., Zhang, H., Yu, L., Chen, H., Xu, Z., Tang, S., Urano, F. and Min, W. AIP1 is critical in transducing IRE1-mediated endoplasmic reticulum stress response. J. Biol. Chem. 283 (2008) 11905-11912.
• 80. Dai, R., Li, J., Liu, Y., Yan, D., Chen, S., Duan, C., Liu, X., He, T. and Li, H. miR-221/222 suppression protects against endoplasmic reticulum stressinduced apoptosis via p27(Kip1)- and MEK/ERK-mediated cell cycle regulation. Biol. Chem. 391 (2010) 791-801.
• 81. Sgambato, A., Cittadini, A., Faraglia, B. and Weinstein, I.B. Multiple functions of p27(Kip1) and its alterations in tumor cells: a review. J. Cell Physiol. 183 (2000) 18-27.
• 82. Li, G., Luna, C., Qiu, J., Epstein, D.L. and Gonzalez, P. Alterations in microRNA expression in stress-induced cellular senescence. Mech. Ageing Dev. 130 (2009) 731-741.
• 83. Li, G., Luna, C., Qiu, J., Epstein, D.L. and Gonzalez, P. Role of miR-204 in the regulation of apoptosis, endoplasmic reticulum stress response, and inflammation in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 52 (2011) 2999-3007.
• 84. Hart, L.S., Cunningham, J.T., Datta, T., Dey, S., Tameire, F., Lehman, S.L., Qiu, B., Zhang, H., Cerniglia, G., Bi, M., Li, Y., Gao, Y., Liu, H., Li, C., Maity, A., Thomas-Tikhonenko, A., Perl, A.E., Koong, A., Fuchs, S.Y., Diehl, J.A., Mills, I.G., Ruggero, D. and Koumenis, C. ER stress-mediated autophagy promotes Myc-dependent transformation and tumor growth. J. Clin. Invest. 122 (2012) 4621-4634.
• 85. Zhang, L.Y., Liu, M., Li, X. and Tang, H. miR-490-3p modulates cell growth and epithelial to mesenchymal transition of hepatocellular carcinoma cells by targeting endoplasmic reticulum-Golgi intermediate compartment protein 3 (ERGIC3). J. Biol. Chem. 288 (2013) 4035-4047.
• 86. Afonyushkin, T., Oskolkova, O.V. and Bochkov, V.N. Permissive role of miR-663 in induction of VEGF and activation of the ATF4 branch of unfolded protein response in endothelial cells by oxidized phospholipids. Atherosclerosis 225 (2012) 50-55.
• 87. Wang, X., Guo, B., Li, Q., Peng, J., Yang, Z., Wang, A., Li, D., Hou, Z., Lv, K., Kan, G., Cao, H., Wu, H., Song, J., Pan, X., Sun, Q., Ling, S., Li, Y., Zhu, M., Zhang, P., Peng, S., Xie, X., Tang, T., Hong, A., Bian, Z., Bai, Y., Lu, A., He, F. and Zhang, G. miR-214 targets ATF4 to inhibit bone formation. Nat. Med. 19 (2013) 93-100.
• 88. Duan, Q., Wang, X., Gong, W., Ni, L., Chen, C., He, X., Chen, F., Yang, L., Wang, P. and Wang, D.W. ER stress negatively modulates the expression of the miR-199a/214 cluster to regulates tumor survival and progression in human hepatocellular cancer. PLoS One 7 (2012) e31518.
• 89. Hoozemans, J.J.M., Veerhuis, R., Haastert, E.S., Rozemuller, J.M., Baas, F., Eikelenboom, P. and Scheper, W. The unfolded protein response is activated in Alzheimer’s disease. Acta Neuropathol. 110 (2005) 165-172.
• 90. Schonrock, N., Ke, Y.D., Humphreys, D., Staufenbiel, M., Ittner, L.M., Preiss, T. and Götz, J. Neuronal MicroRNA deregulation in response to Alzheimer's disease amyloid-β. PLoS One 5 (2010) e11070.
• 91. Wang, W.X., Huang, Q., Hu, Y., Stromberg, A.J. and Nelson, P.T. Patterns of microRNA expression in normal and early Alzheimer's disease human temporal cortex: white matter versus gray matter. Acta Neuropathol. 121 (2011) 193-205.
• 92. Petrofes Chapa, R.D., Emery, M.A., Fawver, J.N. and Murray, I.V. Amyloids as Sensors and Protectors (ASAP) hypothesis. J. Alzheimers Dis. 29 (2012) 503-514.
• 93. Xiao, F., Zuo, Z., Cai, G., Kang, S., Gao, X. and Li, T. miRecords: an integrated resource for microRNA-target interactions. Nucleic Acids Res. 37 (2009) D105-110.
• 94. Maragkakis, M., Reczko, M., Simossis, V.A., Alexiou, P., Papadopoulos, G.L., Dalamagas, T., Giannopoulos, G., Goumas, G., Koukis, E., Kourtis, K., Vergoulis, T., Koziris, N., Sellis, T., Tsanakas, P. and Hatzigeorgiou, A.G. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucleic Acids Res. 37 (2009) W273-276.
• 95. Paraskevopoulou, M.D., Georgakilas, G., Kostoulas, N., Vlachos, I.S., Vergoulis, T., Reczko, M., Filippidis, C., Dalamagas, T. and Hatzigeorgiou, A.G. DIANA-microT web server v5.0: service integration into miRNA functional analysis workflows. Nucleic Acids Res. 41 (2013) W169-W173.
• 96. Davis, N., Biddlecom, N., Hecht, D. and Fogel, G.B. On the relationship between GC content and the number of predicted microRNA binding sites by MicroInspector. Comput. Biol. Chem. 32 (2008) 222-226.
• 97. Rusinov, V., Baev, V., Minkov, I.N. and Tabler, M. MicroInspector: a web tool for detection of miRNA binding sites in an RNA sequence. Nucleic Acids Res. 33 (2005) W696-700.
• 98. Betel, D., Koppal, A., Agius, P., Sander, C. and Leslie, C. Comprehensive modeling of microRNA targets predicts functional non-conserved and noncanonical sites. Genome Biol. 11 (2010) R90.
• 99. Betel, D., Wilson, M., Gabow, A., Marks, D.S. and Sander, C. The microRNA.org resource: targets and expression. Nucleic Acids Res. 36 (2008) D149-153.
• 100. Wang, X. miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 14 (2008) 1012-1017.
• 101. Kim, S.K., Nam, J.W., Rhee, J.K., Lee, W.J. and Zhang, B.T. miTarget: microRNA target gene prediction using a support vector machine. BMC Bioinformatics 7 (2006) 411.
• 102. Krek, A., Grun, D., Poy, M.N., Wolf, R., Rosenberg, L., Epstein, E.J., Macmenamin, P., Da Piedade, I., Gunsalus, K.C., Stoffel, M. and Rajewsky, N. Combinatorial microRNA target predictions. Nat. Genet. 37 (2005) 495-500.
• 103. Chen, K. and Rajewsky, N. Natural selection on human microRNA binding sites inferred from SNP data. Nat. Genet. 38 (2006) 1452-1456.
• 104. Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U. and Segal, E. The role of site accessibility in microRNA target recognition. Nat. Genet. 39 (2007) 1278-1284.
• 105. Rehmsmeier, M., Steffen, P., Hochsmann, M. and Giegerich, R. Fast and effective prediction of microRNA/target duplexes. RNA 10 (2004) 1507- 1517.
• 106. Kruger, J. and Rehmsmeier, M. RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res. 34 (2006) W451-454.
• 107. Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P. and Burge, C.B. Prediction of mammalian microRNA targets. Cell 115 (2003) 787-798.
• 108. Lewis, B.P., Burge, C.B. and Bartel, D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120 (2005) 15-20.
• 109. Bou Kheir, T., Futoma-Kazmierczak, E., Jacobsen, A., Krogh, A., Bardram, L., Hother, C., Gronbaek, K., Federspiel, B., Lund, A.H. and Friis-Hansen, L. miR-449 inhibits cell proliferation and is down-regulated in gastric cancer. Mol. Cancer 10 (2011) 29.
• 110. Lopez, J.A. and Alvarez-Salas, L.M. Differential effects of miR-34c-3p and miR-34c-5p on SiHa cells proliferation apoptosis, migration and invasion. Biochem. Biophys. Res. Commun. 409 (2011) 513-519.
• 111. He, J.H., Li, Y.M., Li, Y.G., Xie, X.Y., Wang, L., Chun, S.Y. and Cheng, W.J. hsa-miR-203 enhances the sensitivity of leukemia cells to arsenic trioxide. Exp. Ther. Med. 5 (2013) 1315-1321.
• 112. Chim, C.S., Wong, K.Y., Leung, C.Y., Chung, L.P., Hui, P.K., Chan, S.Y. and Yu, L. Epigenetic inactivation of the hsa-miR-203 in haematological malignancies. J. Cell Mol. Med. 15 (2011) 2760-2767.
• 113. Takeshita, N., Mori, M., Kano, M., Hoshino, I., Akutsu, Y., Hanari, N., Yoneyama, Y., Ikeda, N., Isozaki, Y., Maruyama, T., Akanuma, N., Miyazawa, Y. and Matsubara, H. miR-203 inhibits the migration and invasion of esophageal squamous cell carcinoma by regulating LASP1. Int. J. Oncol. 41 (2012) 1653-1661.
• 114. Wei, W., Wanjun, L., Hui, S., Dongyue, C., Xinjun, Y. and Jisheng, Z. miR-203 inhibits proliferation of HCC cells by targeting survivin. Cell. Biochem. Funct. 31 (2013) 82-85.
• 115. Viticchie, G., Lena, A.M., Latina, A., Formosa, A., Gregersen, L.H., Lund, A.H., Bernardini, S., Mauriello, A., Miano, R., Spagnoli, L.G., Knight, R.A., Candi, E. and Melino, G. MiR-203 controls proliferation, migration and invasive potential of prostate cancer cell lines. Cell Cycle 10 (2011) 1121-1131.
• 116. Li, J., Chen, Y., Zhao, J., Kong, F. and Zhang, Y. miR-203 reverses chemoresistance in p53-mutated colon cancer cells through downregulation of Akt2 expression. Cancer Lett. 304 (2011) 52-59.
• 117. Furuta, M., Kozaki, K.I., Tanaka, S., Arii, S., Imoto, I. and Inazawa, J. miR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis 31 (2010) 766- 776.
• 118. Decastro, A.J., Dunphy, K.A., Hutchinson, J., Balboni, A.L., Cherukuri, P., Jerry, D.J. and Direnzo, J. MiR203 mediates subversion of stem cell properties during mammary epithelial differentiation via repression of DeltaNP63alpha and promotes mesenchymal-to-epithelial transition. Cell Death Dis. 4 (2013) e514.
• 119. Nakashima, T., Jinnin, M., Etoh, T., Fukushima, S., Masuguchi, S., Maruo, K., Inoue, Y., Ishihara, T. and Ihn, H. Down-regulation of mir-424 contributes to the abnormal angiogenesis via MEK1 and cyclin E1 in senile hemangioma: its implications to therapy. PLoS One 5 (2010) e14334.
• 120. Zhou, R., Gong, A.Y., Chen, D., Miller, R.E., Eischeid, A.N. and Chen, X.M. Histone deacetylases and NF-kB signaling coordinate expression of CX3CL1 in epithelial cells in response to microbial challenge by suppressing miR-424 and miR-503. PLoS One 8 (2013) e65153.
• 121. Zhao, Y., Liu, H., Li, Y., Wu, J., Greenlee, A.R., Yang, C. and Jiang, Y. The role of miR-506 in transformed 16HBE cells induced by antibenzo[a]pyrene-trans-7,8-dihydrodiol-9,10-epoxide. Toxicol. Lett. 205 (2011) 320-326.
• 122. Arora, H., Qureshi, R. and Park, W.Y. miR-506 regulates epithelial mesenchymal transition in breast cancer cell lines. PLoS One 8 (2013) e64273.
• 123. Papagiannakopoulos, T. and Kosik, K.S. MicroRNA-124: micromanager of neurogenesis. Cell Stem Cell. 4 (2009) 375-376.
• 124. Liu, K., Liu, Y., Mo, W., Qiu, R., Wang, X., Wu, J.Y. and He, R. MiR-124 regulates early neurogenesis in the optic vesicle and forebrain, targeting NeuroD1. Nucleic Acids Res. 39 (2011) 2869-2879.
• 125. Schumacher, S. and Franke, K. miR-124-regulated RhoG: A conductor of neuronal process complexity. Small GTPases 4 (2013) 42-46.
• 126. Lang, Q. and Ling, C. MiR-124 suppresses cell proliferation in hepatocellular carcinoma by targeting PIK3CA. Biochem. Biophys. Res. Commun. 426 (2012) 247-252.
• 127. Xia, J., Wu, Z., Yu, C., He, W., Zheng, H., He, Y., Jian, W., Chen, L., Zhang, L. and Li, W. miR-124 inhibits cell proliferation in gastric cancer through down-regulation of SPHK1. J. Pathol. 227 (2012) 470-480.
• 128. Feng, B. and Chakrabarti, S. miR-320 regulates glucose-induced gene expression in diabetes. ISRN Endocrinol. 2012 (2012) 549875.
• 129. Bronisz, A., Godlewski, J., Wallace, J.A., Merchant, A.S., Nowicki, M.O., Mathsyaraja, H., Srinivasan, R., Trimboli, A.J., Martin, C.K., Li, F., Yu, L., Fernandez, S.A., Pecot, T., Rosol, T.J., Cory, S., Hallett, M., Park, M., Piper, M.G., Marsh, C.B., Yee, L.D., Jimenez, R.E., Nuovo, G., Lawler, S.E., Chiocca, E.A., Leone, G. and Ostrowski, M.C. Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat. Cell Biol. 14 (2012) 159-167.
• 130. Hwang-Verslues, W.W., Chang, P.H., Wei, P.C., Yang, C.Y., Huang, C.K., Kuo, W.H., Shew, J.Y., Chang, K.J., Lee, E.Y. and Lee, W.H. miR-495 is upregulated by E12/E47 in breast cancer stem cells, and promotes oncogenesis and hypoxia resistance via downregulation of E-cadherin and REDD1. Oncogene 30 (2011) 2463-2474.
• 131. Jiang, X., Huang, H., Li, Z., He, C., Li, Y., Chen, P., Gurbuxani, S., Arnovitz, S., Hong, G.M., Price, C., Ren, H., Kunjamma, R.B., Neilly, M.B., Salat, J., Wunderlich, M., Slany, R.K., Zhang, Y., Larson, R.A., Le Beau, M.M., Mulloy, J.C., Rowley, J.D. and Chen, J. MiR-495 is a tumorsuppressor microRNA down-regulated in MLL-rearranged leukemia. Proc. Natl. Acad. Sci. USA 109 (2012) 19397-19402.
• 132. Li, Z., Cao, Y., Jie, Z., Liu, Y., Li, Y., Li, J., Zhu, G., Liu, Z., Tu, Y., Peng, G., Lee, D.W. and Park, S.S. miR-495 and miR-551a inhibit the migration and invasion of human gastric cancer cells by directly interacting with PRL3. Cancer Lett. 323 (2012) 41-47.
• 133. Noren Hooten, N., Abdelmohsen, K., Gorospe, M., Ejiogu, N., Zonderman, A.B. and Evans, M.K. microRNA expression patterns reveal differential expression of target genes with age. PLoS One 5 (2010) e10724.
• 134. Ritchie, W., Rajasekhar, M., Flamant, S. and Rasko, J.E. Conserved expression patterns predict microRNA targets. PLoS Comput. Biol. 5 (2009) e1000513.

Uwagi

rekord w opracowaniu