Journal of fish pathology (한국어병학회지)

The Korean Society of Fish Pathology (한국어병학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of hypoxia on the concentration of circulating miR-210 in serum and the expression of HIF-1α and HSP90α in tissues of olive flounder (Paralichthys olivaceus)

  • Abdellaoui, Najib (Department of Life Science, School of Medical-biosystematics, Soongsil University) ;
  • Kwak, Jun Soung (Department of Aquatic Life Medicine, Pukyong National University) ;
  • Kim, Ki Hong (Department of Aquatic Life Medicine, Pukyong National University)
  • Received : 2020.04.21
  • Accepted : 2020.05.26
  • Published : 2020.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Hypoxia is a serious problem in the marine ecosystem causing a decline in aquatic resources. MicroRNAs (miRNAs) regulate the expression of genes through binding to the corresponding sequences of their target mRNAs. Especially, miRNAs in the cytoplasm can be secreted into body fluids, which called circulating miRNAs, and the availability of circulating miRNAs as biomarkers for hypoxia has been demonstrated in mammals. However, there has been no report on the hypoxia-mediated changes in the circulating miRNAs in fish. miR-210 is known as the representative hypoxia-responsive circulating miRNA in mammals. To know whether fish miR-210 also respond to hypoxia, we analyzed the change of circulating miR-210 quantity in the serum of olive flounder (Paralichthys olivaceus) in response to hypoxia. The expression of hypoxia related genes, hypoxia inducible factor 1α (HIF-1α) and the heat shock protein 90α (HSP90α) was also analyzed. Similar to the reports from mammals, miR-210-5p and miR-210-3p were significantly increased in the serum of olive flounder in response to hypoxia, suggesting that circulating miR-210 levels in the serum can be used as a noninvasive prognostic biomarker for fish suffered hypoxia. The target genes of miR-210 were related to various biological processes, which explains the major regulatory role of miR-210 in response to hypoxia. The expression of HIF-1α and HSP90α in the tissues was also up-regulated by hypoxia. Considering the critical role of HIF-1α in miR-210 expression and HSP90 in miRNAs function, the present up-regulation of HIF-1α and HSP90α might be related to the increase of circulatory miR-210, and the interaction mechanism among HIF-1α, HSP90α, and hypoxia-responsive microRNAs in fish should be further studied.

Keywords

References

  1. Bandara, V., Michael, M. and Gleadle, J.: Hypoxia represses microRNA biogenesis proteins in breast cancer cells. BMC Cancer, 14: 533, 2014. https://doi.org/10.1186/1471-2407-14-533
  2. Bartel, D.P.: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116: 281-297, 2004. https://doi.org/10.1016/S0092-8674(04)00045-5
  3. Bye, A., Rosjo, H., Aspenes, S.T., Condorelli, G., Omland, T. and Wisloff, U.: Circulating microRNAs and aerobic fitness? The HUNT-Study. PLoS One, 8: e57496, 2013. https://doi.org/10.1371/journal.pone.0057496
  4. Chan, S.Y. and Loscalzo, J.: MicroRNA-210: A unique and pleiotropic hypoxamir. Cell Cycle, 9: 1072-1083, 2010. https://doi.org/10.4161/cc.9.6.11006
  5. Chan, S.Y., Zhang, Y.-Y., Hemann, C., Mahoney, C.E., Zweier, J.L. and Loscalzo, J.: MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metabolism, 10: 273-284, 2009. https://doi.org/10.1016/j.cmet.2009.08.015
  6. Cicchillitti, L., Di Stefano, V., Isaia, E., Crimaldi, L., Fasanaro, P., Ambrosino, V., Antonini, A., Capogrossi, M.C., Gaetano, C., Piaggio, G. and Martelli, F.: Hypoxia-inducible factor 1-alpha induces miR-210 in normoxic differentiating myoblasts. J. Biol. Chem., 287: 44761-44771, 2012. https://doi.org/10.1074/jbc.M112.421255
  7. Enright, A.J., John, B., Gaul, U., Tuschl, T., Sander, C. and Marks, D.S.: MicroRNA targets in Drosophila. Genome Biol., 5: 1-14, 2003.
  8. Gibbings, D.J., Ciaudo, C., Erhardt, M. and Voinnet, O.: Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol., 11: 1143-1149, 2009. https://doi.org/10.1038/ncb1929
  9. Granchi, C., Fancelli, D. and Minutolo, F.: An update on therapeutic opportunities offered by cancer glycolytic metabolism. Bioorg. Med. Chem. Lett., 24: 4915-4925, 2014. https://doi.org/10.1016/j.bmcl.2014.09.041
  10. Guimbellot, J.S., Erickson, S.W., Mehta, T., Wen, H., Page, G.P., Sorscher, E.J. and Hong, J.S.: Correlation of microRNA levels during hypoxia with predicted target mRNAs through genome-wide microarray analysis. BMC Med. Genomics, 2: 1-17, 2009. https://doi.org/10.1186/1755-8794-2-1
  11. Ho, A.S., Huang, X., Cao, H., Christman-Skieller, C., Bennewith, K., Le, Q.-T. and Koong, A.C.: Circulating miR-210 as a novel hypoxia marker in pancreatic cancer. Transl. Oncol., 3: 109-113, 2010. https://doi.org/10.1593/tlo.09256
  12. Hua, Z., Lv, Q., Ye, W., Wong, C.-K.A., Cai, G., Gu, D., Ji, Y., Zhao, C., Wang, J., Yang, B.B. and Zhang, Y.: MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One, 1: e116, 2006. https://doi.org/10.1371/journal.pone.0000116
  13. 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: 856-867, 2009. https://doi.org/10.1016/j.molcel.2009.09.006
  14. Huang, X., Le, Q.-T. and Giaccia, A.J.: MiR-210 - micromanager of the hypoxia pathway. Trends Mol. Med., 16: 230-237, 2010. https://doi.org/10.1016/j.molmed.2010.03.004
  15. Hutvagner, G. and Zamore, P.D.: A microRNA in a multiple-turnover RNAi enzyme complex. Science, 297: 2056-2060, 2002. https://doi.org/10.1126/science.1073827
  16. Ivan, M., Harris, A.L., Martelli, F. and Kulshreshtha, R.: Hypoxia response and microRNAs: no longer two separate worlds. J. Cell. Mol. Med., 12: 1426-1431, 2008. https://doi.org/10.1111/j.1582-4934.2008.00398.x
  17. Iwasaki, S., Kobayashi, M., Yoda, M., Sakaguchi, Y., Katsuma, S., Suzuki, T. and Tomari, Y.: Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell, 39: 292-299, 2010. https://doi.org/10.1016/j.molcel.2010.05.015
  18. John, B., Enright, A.J., Aravin, A., Tuschl, T., Sander, C. and Marks, D.S.: Human microRNA targets. PLoS Biol., 2: e363, 2004. https://doi.org/10.1371/journal.pbio.0020363
  19. Kallio, P.J., Pongratz, I., Gradin, K., McGuire, J. and Poellinger, L.: Activation of hypoxia-inducible factor $1{\alpha}$: Posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proceedings of the National Academy of Sciences, 94: 5667-5672, 1997. https://doi.org/10.1073/pnas.94.11.5667
  20. Katakowski, M., Buller, B., Wang, X., Rogers, T. and Chopp, M.: Functional microRNA is transferred between glioma cells. Cancer Res., 70: 8259-8263, 2010. https://doi.org/10.1158/0008-5472.CAN-10-0604
  21. Kharaziha, P., Ceder, S., Li, Q. and Panaretakis, T.: Tumor cell-derived exosomes: A message in a bottle. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, 1826: 103-111, 2012. https://doi.org/10.1016/j.bbcan.2012.03.006
  22. Kulshreshtha, R., Ferracin, M., Wojcik, S.E., Garzon, R., Alder, H., Agosto-Perez, F.J., Davuluri, R., Liu, C.-G., Croce, C.M., Negrini, M., Calin, G.A. and Ivan, M.: A microRNA signature of hypoxia. Mol. Cell. Biol., 27: 1859-1867, 2007. https://doi.org/10.1128/MCB.01395-06
  23. Lai, K.P., Li, J.-W., Tse, A.C.-K., Chan, T.-F. and Wu, R.S.S.: Hypoxia alters steroidogenesis in female marine medaka through miRNAs regulation. Aquat. Toxicol., 172: 1-8, 2016. https://doi.org/10.1016/j.aquatox.2015.12.012
  24. Lau, K., Lai, K.P., Bao, J.Y.J., Zhang, N., Tse, A., Tong, A., Li, J.W., Lok, S., Kong, R.Y.C., Lui, W.Y., Wong, A. and Wu, R.S.S.: Identification and expression profiling of microRNAs in the brain, liver and gonads of marine medaka (Oryzias melastigma) and in response to hypoxia. PLoS One, 9: e110698, 2014. https://doi.org/10.1371/journal.pone.0110698
  25. Lays, N., Iversen, M.M.T., Frantzen, M. and Jorgensen, E.H.: Physiological stress responses in spotted wolffish (Anarhichas minor) subjected to acute disturbance and progressive hypoxia. Aquaculture, 295: 126-133, 2009. https://doi.org/10.1016/j.aquaculture.2009.06.039
  26. Minet, E., Mottet, D., Michel, G., Roland, I., Raes, M., Remacle, J. and Michiels, C.: Hypoxia-induced activation of HIF-1: role of HIF-$1{\alpha}$-Hsp90 interaction. FEBS Lett., 460: 251-256, 1999. https://doi.org/10.1016/S0014-5793(99)01359-9
  27. Mitchell, P.S., Parkin, R.K., Kroh, E.M., Fritz, B.R., Wyman, S.K., Pogosova-Agadjanyan, E.L., Peterson, A., Noteboom, J., O'Briant, K.C., Allen, A., Lin, D.W., Urban, N., Drescher, C.W., Knudsen, B.S., Stirewalt, D.L., Gentleman, R., Vessella, R.L., Nelson, P.S., Martin, D.B. and Tewari, M.: Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences, 105: 10513-10518, 2008. https://doi.org/10.1073/pnas.0804549105
  28. Ohh, M., Park, C.W., Ivan, M., Hoffman, M.A., Kim, T.-Y., Huang, L.E., Pavletich, N., Chau, V. and Kaelin, W.G.: Ubiquitination of hypoxia-inducible factor requires direct binding to the [bgr]-domain of the von Hippel-Lindau protein. Nat. Cell Biol., 2: 423-427, 2000. https://doi.org/10.1038/35017054
  29. Park, M.H., Bae, S.S., Choi, K.-Y. and Min, D.S.: Phospholipase D2 promotes degradation of hypoxia-inducible factor-$1{\alpha}$ independent of lipase activity. Exp. Mol. Med., 47: e196, 2015. https://doi.org/10.1038/emm.2015.87
  30. Poellinger, L. and Johnson, R.S.: HIF-1 and hypoxic response: the plot thickens. Curr. Opin. Genet. Dev., 14: 81-85, 2004. https://doi.org/10.1016/j.gde.2003.12.006
  31. Rabalais, N.N., Diaz, R.J., Levin, L.A., Turner, R.E., Gilbert, D. and Zhang, J.: Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences, 7: 585-619, 2010. https://doi.org/10.5194/bg-7-585-2010
  32. Richards, J.G.: Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J. Exp. Biol., 214: 191-199, 2011. https://doi.org/10.1242/jeb.047951
  33. Rosjo, H., Dahl, M.B., Bye, A., Andreassen, J., Jorgensen, M., Wisloff, U., Christensen, G., Edvardsen, T. and Omland, T.: Prognostic value of circulating microRNA-210 levels in patients with moderate to severe aortic stenosis. PLoS One, 9: e91812, 2014. https://doi.org/10.1371/journal.pone.0091812
  34. Rueda, A., Barturen, G., Lebron, R., Gomez-Martin, C., Alganza, A., Oliver, J.L. and Hackenberg, M.: sRN Atoolbox: an integrated collection of small RNA research tools. Nucleic Acids Res., 43: W467-W473, 2015. https://doi.org/10.1093/nar/gkv555
  35. Semenza, G.L.: Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology, 24: 97-106, 2009. https://doi.org/10.1152/physiol.00045.2008
  36. Soitamo, A.J., Rabergh, C.M.I., Gassmann, M., Sistonen, L. and Nikinmaa, M.: Characterization of a Hypoxia-inducible Factor (HIF-$1{\alpha}$) from Rainbow Trout: Accumulation of protein occurs at normal venous oxygen tension. J. Biol. Chem., 276: 19699-19705, 2001. https://doi.org/10.1074/jbc.M009057200
  37. Stroka, D.M., Burkhardt, T., Desbaillets, I., Wenger, R. H., Neil, D.A.H., Bauer, C., Gassmann, M. and Candinas, D.: HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J., 15: 2445-2453, 2001. https://doi.org/10.1096/fj.01-0125com
  38. Sturm, M., Hackenberg, M., Langenberger, D. and Frishman, D.: TargetSpy: a supervised machine learning approach for microRNA target prediction. BMC Bioinformatics, 11: 1-17, 2010. https://doi.org/10.1186/1471-2105-11-1
  39. Tse, A.C.-K., Li, J.-W., Chan, T.-F., Wu, R.S.-S. and Lai, K.-P.: Hypoxia induces miR-210, leading to anti-apoptosis in ovarian follicular cells of marine medaka Oryzias melastigma. Aquat. Toxicol., 165: 189-196, 2015. https://doi.org/10.1016/j.aquatox.2015.06.002
  40. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J.J. and Lotvall, J.O.: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 9: 654-659, 2007. https://doi.org/10.1038/ncb1596
  41. Ye, J., Fang, L., Zheng, H., Zhang, Y., Chen, J., Zhang, Z., Wang, J., Li, S., Li, R., Bolund, L. and Wang, J.: WEGO: a web tool for plotting GO annotations. Nucleic Acids Res., 34: W293-W297, 2006. https://doi.org/10.1093/nar/gkl031
  42. Zhang, C., Wang, C., Chen, X., Yang, C., Li, K., Wang, J., Dai, J., Hu, Z., Zhou, X., Chen, L., Zhang, Y., Li, Y., Qiu, H., Xing, J., Liang, Z., Ren, B., Yang, C., Zen, K. and Zhang, C.-Y.: Expression profile of microRNAs in serum: A fingerprint for esophageal squamous cell carcinoma. Clin. Chem., 56: 1871-1879, 2010. https://doi.org/10.1373/clinchem.2010.147553