MicroRNA-31 targets FIH-1 to positively regulate corneal epithelial glycogen metabolism

FASEB Journal

Volumn 26, Issue 8, 2012, Pages 3140-3147

  Peng, Han ^a   Hamanaka, Robert B ^a   Katsnelson, Julia ^b   Hao, Liang Liang ^a   Yang, Wending ^a   Chandel, Navdeep S ^a   Lavker, Robert M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b RUSH MEDICAL COLLEGE   (United States)

Author keywords

Akt signaling; Energy metabolism; Keratinocytes

Indexed keywords

ANTAGOMIR; FACTOR INHIBITING HYPOXIA INDUCIBLE FACTOR 1; GLYCOGEN SYNTHASE KINASE 3BETA; HYPOXIA INDUCIBLE FACTOR 1; MICRORNA 31; OXYGENASE; PROTEIN KINASE B; REGULATOR PROTEIN; RETROVIRUS VECTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA EPITHELIUM; ENERGY METABOLISM; ENZYME INACTIVATION; FEMALE; GENE MUTATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC TRANSDUCTION; GLYCOGEN METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MOUSE; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; EPITHELIUM, CORNEAL; FEMALE; GLYCOGEN; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KERATINOCYTES; MICE; MICRORNAS; MIXED FUNCTION OXYGENASES; OLIGORIBONUCLEOTIDES; PROTO-ONCOGENE PROTEINS C-AKT; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84864773117     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-198515     Document Type: Article

References (43)

1. Piatigorsky, J. (2008) Lens and cornea: the "refracton hypothesis". Semin. Cell Dev. Biol. 19, 69-70
2. Sun, L., Sun, T.-T., and Lavker, R. M. (1999) Identification of a cytosolic NADP+-dependent isocitrate dehydrogenase that is preferentially expressed in bovine corneal epithelium: a corneal epithelial crystallin. J. Biol. Chem. 274, 17334-17341
3. Cursiefen, C., Chen, L., Saint-Geniez, M., Hamrah, P., Jin, Y., Rashid, S., Pytowski, B., Persaud, K., Wu, Y., Streilein, J. W., and Dana, R. (2006) Nonvascular VEGF receptor 3 expression by corneal epithelium maintains avascularity and vision. Proc. Natl. Acad. Sci. U. S. A. 103, 11405-11410 (Pubitemid 44156530)
4. Thoft, R. A., and Friend, J. (1975) Biochmical aspects of contact lens wear. Am. J. Ophthalmol. 80, 139-145
5. Thoft, R. A., and Friend, J. (1977) Biochemical transformation of regenerating ocular surface epithelium. Invest. Ophthalmol. Vis. Sci. 16, 14-20 (Pubitemid 8040402)
6. Kimura, K., Teranishi, S., Kawamoto, K., and Nishida, T. (2010) Protection of human corneal epithelial cells from hypoxia-induced disruption of barrier function by hepatocyte growth factor. Exp. Eye Res. 90, 337-343
7. Yamamoto, N., Jester, J. V., Petroll, W. M., and Cavanagh, H. D. (2006) Prolonged hypoxia induces lipid raft formation and increases Pseudomonas internalization in vivo after contact lens wear and lid closure. Eye Contact Lens 32, 114-120 (Pubitemid 44510035)
8. Kaji, Y. (2005) Prevention of diabetic keratopathy. Br. J. Ophthalmol. 89, 254-255
9. Xu, K., and Yu, F. S. (2011) Impaired epithelial wound healing and EGFR signaling pathways in the corneas of diabetic rats. Invest. Ophthalmol. Vis. Sci. 52, 3301-3308
10. Xu, K. P., Li, Y., Ljubimov, A. V., and Yu, F. S. (2009) High glucose suppresses epidermal growth factor receptor/phosphatidylinositol 3-kinase/Akt signaling pathway and attenuates corneal epithelial wound healing. Diabetes 58, 1077-1085
11. Semenza, G. L. (2001) HIF-1, O2, and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107, 1-3
12. Gunton, J. E., Kulkarni, R. N., Yim, S., Okada, T., Hawthorne, W. J., Tseng, Y. H., Roberson, R. S., Ricordi, C., O'Connell, P. J., Gonzalez, F. J., and Kahn, C. R. (2005) Loss of ARNT/HIF1beta mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 122, 337-349 (Pubitemid 41127137)
13. Ohh, M., Park, C. W., Ivan, M., Hoffman, M. A., Kim, T. Y., Huang, L. E., Pavletich, N., Chau, V., and Kaelin, W. G. (2000) Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat. Cell Biol. 2, 423-427
14. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275 (Pubitemid 29246458)
15. 2-regulated prolyl hydroxylation. Science 292, 468-472
16. Masson, N., Willam, C., Maxwell, P. H., Pugh, C. W., and Ratcliffe, P. J. (2001) Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 20, 5197-5206 (Pubitemid 32910914)
17. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., Mukherji, M., Metzen, E., Wilson, M. I., Dhanda, A., Tian, Y. M., Masson, N., Hamilton, D. L., Jaakkola, P., Barstead, R., Hodgkin, J., Maxwell, P. H., Pugh, C. W., Schofield, C. J., and Ratcliffe, P. J. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54 (Pubitemid 32972036)
18. Bruick, R. K., and McKnight, S. L. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340 (Pubitemid 33063099)
19. Lando, D., Peet, D. J., Gorman, J. J., Whelan, D. A., Whitelaw, M. L., and Bruick, R. K. (2002) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia- inducible factor. Genes Dev. 16, 1466-1471 (Pubitemid 34686328)
20. Mahon, P. C., Hirota, K., and Semenza, G. L. (2001) FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15, 2675-2686 (Pubitemid 32988878)
21. Cockman, M. E., Webb, J. D., and Ratcliffe, P. J. (2009) FIH-dependent asparaginyl hydroxylation of ankyrin repeat domain-containing proteins. Ann. N. Y. Acad. Sci. 1177, 9-18
22. Coleman, M. L., McDonough, M. A., Hewitson, K. S., Coles, C., Mecinovic, J., Edelmann, M., Cook, K. M., Cockman, M. E., Lancaster, D. E., Kessler, B. M., Oldham, N. J., Ratcliffe, P. J., and Schofield, C. J. (2007) Asparaginyl hydroxylation of the Notch ankyrin repeat domain by factor inhibiting hypoxia-inducible factor. J. Biol. Chem. 282, 24027-24038 (Pubitemid 47328043)
23. Liu, C. J., Tsai, M. M., Hung, P. S., Kao, S. Y., Liu, T. Y., Wu, K. J., Chiou, S. H., Lin, S. C., and Chang, K. W. (2010) miR-31 ablates expression of the HIF regulatory factor FIH to activate the HIF pathway in head and neck carcinoma. Cancer Res. 70, 1635-1644
24. Zhou, M., Li, X. M., and Lavker, R. M. (2006) Transcriptional profiling of enriched populations of stem cells versus transient amplifying cells. A comparison of limbal and corneal epithelial basal cells. J. Biol. Chem. 281, 19600-19609 (Pubitemid 44035463)
25. Yu, J., Peng, H., Ruan, Q., Fatima, A., Getsios, S., and Lavker, R. M. (2010) MicroRNA-205 promotes keratinocyte migration via the lipid phosphatase SHIP2. FASEB J. 24, 3950-3959
26. Weinberg, F., Hamanaka, R., Wheaton, W. W., Weinberg, S., Joseph, J., Lopez, M., Kalyanaraman, B., Mutlu, G. M., Budinger, G. R., and Chandel, N. S. (2010) Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc. Natl. Acad. Sci. U. S. A. 107, 8788-8793
27. Getsios, S., Simpson, C. L., Kojima, S., Harmon, R., Sheu, L. J., Dusek, R. L., Cornwell, M., and Green, K. J. (2009) Desmoglein 1-dependent suppression of EGFR signaling promotes epidermal differentiation and morphogenesis. J. Cell Biol. 185, 1243-1258
28. Wei, Z. G., Sun, T. T., and Lavker, R. M. (1996) Rabbit conjunctival and corneal epithelial cells belong to two separate lineages. Invest. Ophthalmol. Vis. Sci. 37, 523-533
29. Ryan, D. G., Oliveira-Fernandes, M., and Lavker, R. M. (2006) MicroRNAs of the mammalian eye display distinct and overlapping tissue specificity. Mol. Vis. 12, 1175-1184
30. Yu, J., Ryan, D. G., Getsios, S., Oliveira-Fernandes, M., Fatima, A., and Lavker, R. M. (2008) MicroRNA-184 antagonizes microRNA- 205 to maintain SHIP2 levels in epithelia. Proc. Natl.Acad. Sci. U. S. A. 105, 19300-19305
31. Barad, O., Meiri, E., Avniel, A., Aharonov, R., Barzilai, A., Bentwich, I., Einav, U., Gilad, S., Hurban, P., Karov, Y., Lobenhofer, E. K., Sharon, E., Shiboleth, Y. M., Shtutman, M., Bentwich, Z., and Einat, P. (2004) MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res. 14, 2486-2494 (Pubitemid 40012232)
32. Weidemann, A., and Johnson, R. S. (2008) Biology of HIF-1α. Cell Death Differ. 15, 621-627
33. Bartrons, R., and Caro, J. (2007) Hypoxia, glucose metabolism and the Warburg's effect. J. Bioenerg. Biomembr. 39, 223-229 (Pubitemid 47619374)
34. Rayasam, G. V., Tulasi, V. K., Sodhi, R., Davis, J. A., and Ray, A. (2009) Glycogen synthase kinase 3: more than a namesake. Br. J. Pharmacol. 156, 885-898
35. Rebuffe-Scrive, M., Surwit, R., Feinglos, M., Kuhn, C., and Rodin, J. (1993) Regional fat distribution and metabolism in a new mouse model (C57BL/6J) of non-insulin-dependent diabetes mellitus. Metabolism 42, 1405-1409 (Pubitemid 23335871)
36. Surwit, R. S., Kuhn, C. M., Cochrane, C., McCubbin, J. A., and Feinglos, M. N. (1988) Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37, 1163-1167 (Pubitemid 19035045)
37. Buchanan, J., Mazumder, P. K., Hu, P., Chakrabarti, G., Roberts, M. W., Yun, U. J., Cooksey, R. C., Litwin, S. E., and Abel, E. D. (2005) Reduced cardiac efficiency and altered substrate metabolism precedes the onset of hyperglycemia and contractile dysfunction in two mouse models of insulin resistance and obesity. Endocrinology 146, 5341-5349 (Pubitemid 41653047)
38. Koivunen, P., Hirsila, M., Gunzler, V., Kivirikko, K. I., and Myllyharju, J. (2004) Catalytic properties of the asparaginyl hydroxylase (FIH) in the oxygen sensing pathway are distinct from those of its prolyl 4-hydroxylases. J. Biol. Chem. 279, 9899-9904 (Pubitemid 38372589)
39. Stolze, I. P., Tian, Y. M., Appelhoff, R. J., Turley, H., Wykoff, C. C., Gleadle, J. M., and Ratcliffe, P. J. (2004) Genetic analysis of the role of the asparaginyl hydroxylase factor inhibiting hypoxia-inducible factor (HIF) in regulating HIF transcriptional target genes. J. Biol. Chem. 279, 42719-42725 (Pubitemid 39372158)
40. Zhang, N., Fu, Z., Linke, S., Chicher, J., Gorman, J. J., Visk, D., Haddad, G. G., Poellinger, L., Peet, D. J., Powell, F., and Johnson, R. S. (2010) The asparaginyl hydroxylase factor inhibiting HIF-1alpha is an essential regulator of metabolism. Cell Metab. 11, 364-378
41. Lu, L., Reinach, P. S., and Kao, W. W. (2001) Corneal epithelial wound healing. Exp. Biol. Med. (Maywood) 226, 653-664 (Pubitemid 32619604)
42. Kinoshita, S., Kiorpes, T. C., Friend, J., and Thoft, R. A. (1982) Limbal epithelium in ocular surface wound healing. Invest. Ophthalmol. Vis. Sci. 23, 73-80 (Pubitemid 12089684)
43. Sridharan, V., Guichard, J., Bailey, R. M., Kasiganesan, H., Beeson, C., and Wright, G. L. (2007) The prolyl hydroxylase oxygen-sensing pathway is cytoprotective and allows maintenance of mitochondrial membrane potential during metabolic inhibition. Am. J. Physiol. Cell Physiol. 292, C719-C728