Hypoxia-inducible factor 1-α induces miR-210 in normoxic differentiating myoblasts

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44761-44771

  Cicchillitti, Lucia ^a   Di Stefano, Valeria ^a,b   Isaia, Eleonora ^a   Crimaldi, Luca ^a,e   Fasanaro, Pasquale ^b   Ambrosino, Valeria ^c   Antonini, Annalisa ^b   Capogrossi, Maurizio C ^b   Gaetano, Carlo ^d   Piaggio, Giulia ^c   Martelli, Fabio ^a  

^a IRCCS POLICLINICO SAN DONATO   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^e EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIO-VASCULAR DISEASE; CHROMATIN IMMUNOPRECIPITATION; FUNCTIONAL RELEVANCE; HYPOXIA-INDUCIBLE FACTOR 1; IN-VITRO; LOCKED NUCLEIC ACID; LUCIFERASE REPORTER ASSAYS; MITOCHONDRIAL DYSFUNCTION; MYOBLAST CELLS; MYOBLASTS; MYOFIBERS; MYOTUBES; SKELETAL MUSCLE;

CELL CULTURE; CHEMICAL COMPOUNDS; OLIGONUCLEOTIDES;

DISEASES;

CARDIOTOXIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LUCIFERASE; MICRORNA 210; OLIGONUCLEOTIDE;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL LINE; CELL PROTECTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA METHYLATION; ENZYME ASSAY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUSCLE INJURY; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; RNA TRANSCRIPTION; SKELETAL MUSCLE; STRUCTURE ANALYSIS;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; MYOBLASTS; OXYGEN; PROMOTER REGIONS, GENETIC;

EID: 84871746640     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421255     Document Type: Article

References (53)

1. Devlin, C., Greco, S., Martelli, F., and Ivan, M. (2011) miR-210. More than a silent player in hypoxia. IUBMB Life 63, 94-100
2. Huang, X., Le, Q. T., and Giaccia, A. J. (2010) MiR-210-micromanager of the hypoxia pathway. Trends Mol. Med. 16, 230-237
3. Voellenkle, C., van Rooij, J., Guffanti, A., Brini, E., Fasanaro, P., Isaia, E., Croft, L., David, M., Capogrossi, M. C., Moles, A., Felsani, A., and Martelli, F. (2012) Deep-sequencing of endothelial cells exposed to hypoxia reveals the complexity of known and novel microRNAs. RNA 18, 472-484
4. Ivan, M., Harris, A. L., Martelli, F., and Kulshreshtha, R. (2008) Hypoxia response and microRNAs. No longer two separate worlds. J. Cell Mol. Med. 12, 1426-1431
5. 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. (2009) Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol. Cell 35, 856-867
6. Camps, C., Buffa, F. M., Colella, S., Moore, J., Sotiriou, C., Sheldon, H., Harris, A. L., Gleadle, J. M., and Ragoussis, J. (2008) HSA-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin. Cancer Res. 14, 1340-1348 (Pubitemid 351413913)
7. Fasanaro, P., D'Alessandra, Y., Di Stefano, V., Melchionna, R., Romani, S., Pompilio, G., Capogrossi, M. C., and Martelli, F. (2008) MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J. Biol. Chem. 283, 15878-15883
8. Favaro, E., Ramachandran, A., McCormick, R., Gee, H., Blancher, C., Crosby, M., Devlin, C., Blick, C., Buffa, F., Li, J. L., Vojnovic, B., Pires das Neves, R., Glazer, P., Iborra, F., Ivan, M., Ragoussis, J., and Harris, A. L. (2010) MicroRNA-210 regulates mitochondrial free radical response to hypoxia and Krebs cycle in cancer cells by targeting iron sulfur cluster protein ISCU. PLoS ONE 5, e10345
9. Puisségur, M. P., Mazure, N. M., Bertero, T., Pradelli, L., Grosso, S., Robbe- Sermesant, K., Maurin, T., Lebrigand, K., Cardinaud, B., Hofman, V., Fourre, S., Magnone, V., Ricci, J. E., Pouysségur, J., Gounon, P., Hofman, P., Barbry, P., and Mari, B. (2011) miR-210 is overexpressed in late stages of lung cancer and mediates mitochondrial alterations associated with modulation of HIF-1 activity. Cell Death Differ. 18, 465-478
10. Zhang, Z., Sun, H., Dai, H., Walsh, R. M., Imakura, M., Schelter, J., Burchard, J., Dai, X., Chang, A. N., Diaz, R. L., Marszalek, J. R., Bartz, S. R., Carleton, M., Cleary, M. A., Linsley, P. S., and Grandori, C. (2009) MicroRNA miR-210 modulates cellular response to hypoxia through the MYC antagonist MNT. Cell Cycle 8, 2756-2768
11. Chan, Y. C., Banerjee, J., Choi, S. Y., and Sen, C. K. (2011) miR-210. The master hypoxamir. Microcirculation 19, 215-223
12. Fasanaro, P., Greco, S., Lorenzi, M., Pescatori, M., Brioschi, M., Kulshreshtha, R., Banfi, C., Stubbs, A., Calin, G. A., Ivan, M., Capogrossi, M. C., and Martelli, F. (2009) An integrated approach for experimental target identification of hypoxia-induced miR-210. J. Biol. Chem. 284, 35134-35143
13. Kosaka, N., Sugiura, K., Yamamoto, Y., Yoshioka, Y., Miyazaki, H., Komatsu, N., Ochiya, T., and Kato, T. (2008) Identification of erythropoietin-induced microRNAs in haematopoietic cells during erythroid differentiation. Br. J. Haematol. 142, 293-300 (Pubitemid 351987314)
14. Yang, W., Sun, T., Cao, J., Liu, F., Tian, Y., and Zhu, W. (2012) Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp. Cell Res. 318, 944-954
15. Gou, D., Ramchandran, R., Peng, X., Yao, L., Kang, K., Sarkar, J., Wang, Z., Zhou, G., and Raj, J. U. (2012) miR-210 has an anti-apoptotic effect in pulmonary artery smooth muscle cells during hypoxia. Am. J. Physiol. Lung Cell Mol. Physiol., L682-L691
16. Quero, L., Dubois, L., Lieuwes, N. G., Hennequin, C., and Lambin, P. (2011) miR-210 as a marker of chronic hypoxia, but not a therapeutic target in prostate cancer. Radiother. Oncol. 101, 203-208
17. Kim, H. W., Haider, H. K., Jiang, S., and Ashraf, M. (2009) Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J. Biol. Chem. 284, 33161-33168
18. Hu, S., Huang, M., Li, Z., Jia, F., Ghosh, Z., Lijkwan, M. A., Fasanaro, P., Sun, N., Wang, X., Martelli, F., Robbins, R. C., and Wu, J. C. (2010) MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 122, S124-131
19. Mutharasan, R. K., Nagpal, V., Ichikawa, Y., and Ardehali, H. (2011) microRNA-210 is upregulated in hypoxic cardiomyocytes through Akt- and p53-dependent pathways and exerts cytoprotective effects. Am. J. Physiol. Heart Circ. Physiol. 301, H1519-1530
20. Chan, S. Y., Zhang, Y. Y., Hemann, C., Mahoney, C. E., Zweier, J. L., and Loscalzo, J. (2009) MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab. 10, 273-284
21. Yoshioka, Y., Kosaka, N., Ochiya, T., and Kato, T. (2012) Micromanaging iron homeostasis. Hypoxia-inducible miR-210 suppresses iron homeostasis-related proteins. J. Biol. Chem. 287, 34110-34119
22. Chen, Z., Li, Y., Zhang, H., Huang, P., and Luthra, R. (2010) Hypoxia-regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression. Oncogene 29, 4362-4368
23. Liu, F., Lou, Y. L., Wu, J., Ruan, Q. F., Xie, A., Guo, F., Cui, S. P., Deng, Z. F., and Wang, Y. (2012) Upregulation of MicroRNA-210 regulates renal angiogenesis mediated by activation of VEGF signaling pathway under ischemia/perfusion injury in vivo and in vitro. Kidney Blood Press. Res. 35, 182-191
24. Lou, Y. L., Guo, F., Liu, F., Gao, F. L., Zhang, P. Q., Niu, X., Guo, S. C., Yin, J. H., Wang, Y., and Deng, Z. F. (2012) miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol. Cell Biochem. 370, 45-51
25. Alaiti, M. A., Ishikawa, M., Masuda, H., Simon, D. I., Jain, M. K., Asahara, T., and Costa, M. A. (2012) Up-regulation of miR-210 by vascular endothelial growth factor in ex vivo expanded CD34+ cells enhances cell-mediated angiogenesis. J. Cell Mol. Med. 16, 2413-2421
26. Bianchi, N., Zuccato, C., Lampronti, I., Borgatti, M., and Gambari, R. (2009) Expression of miR-210 during erythroid differentiation and induction of γ-globin gene expression. BMB Rep. 42, 493-499
27. Mizuno, Y., Tokuzawa, Y., Ninomiya, Y., Yagi, K., Yatsuka-Kanesaki, Y., Suda, T., Fukuda, T., Katagiri, T., Kondoh, Y., Amemiya, T., Tashiro, H., and Okazaki, Y. (2009) miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett. 583, 2263-2268
28. Qin, L., Chen, Y., Niu, Y., Chen, W., Wang, Q., Xiao, S., Li, A., Xie, Y., Li, J., Zhao, X., He, Z., and Mo, D. (2010) A deep investigation into the adipogenesis mechanism. Profile of microRNAs regulating adipogenesis by modulating the canonical Wnt/β-catenin signaling pathway. BMC Genomics 11, 320
29. Greco, S., Fasanaro, P., Castelvecchio, S., D'Alessandra, Y., Arcelli, D., Di Donato, M., Malavazos, A., Capogrossi, M. C., Menicanti, L., and Martelli, F. (2012) MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes 61, 1633-1641
30. Martelli, F., Cenciarelli, C., Santarelli, G., Polikar, B., Felsani, A., and Caruso, M. (1994) MyoD induces retinoblastoma gene expression during myogenic differentiation. Oncogene 9, 3579-3590 (Pubitemid 24359396)
31. Cardinali, B., Castellani, L., Fasanaro, P., Basso, A., Alemà, S., Martelli, F., and Falcone, G. (2009) Microrna-221 and microrna-222 modulate differentiation and maturation of skeletal muscle cells. PLoS ONE 4, e7607
32. Zaccagnini, G., Martelli, F., Magenta, A., Cencioni, C., Fasanaro, P., Nicoletti, C., Biglioli, P., Pelicci, P. G., and Capogrossi, M. C. (2007) p66(ShcA) and oxidative stress modulate myogenic differentiation and skeletal muscle regeneration after hind limb ischemia. J. Biol. Chem. 282, 31453-31459 (Pubitemid 350044897)
33. Travaglione, S., Messina, G., Fabbri, A., Falzano, L., Giammarioli, A. M., Grossi, M., Rufini, S., and Fiorentini, C. (2005) Cytotoxic necrotizing factor 1 hinders skeletal muscle differentiation in vitro by perturbing the activation/deactivation balance of Rho GTPases. Cell Death Differ. 12, 78-86 (Pubitemid 40090030)
34. Fasanaro, P., Romani, S., Voellenkle, C., Maimone, B., Capogrossi, M. C., and Martelli, F. (2012) ROD1 is a seedless target gene of hypoxia-induced miR-210. PLoS ONE 7, e44651
35. Gurtner, C., Tu, E., Jamshidi, N., Haigis, R. W., Onofrey, T. J., Edman, C. F., Sosnowski, R., Wallace, B., and Heller, M. J. (2002) Microelectronic array devices and techniques for electric field enhanced DNA hybridization in low-conductance buffers. Electrophoresis 23, 1543-1550 (Pubitemid 34649586)
36. Musarò, A., Giacinti, C., Borsellino, G., Dobrowolny, G., Pelosi, L., Cairns, L., Ottolenghi, S., Cossu, G., Bernardi, G., Battistini, L., Molinaro, M., and Rosenthal, N. (2004) Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc. Natl. Acad. Sci. U.S.A. 101, 1206-1210 (Pubitemid 38182667)
37. Ono, Y., Sensui, H., Sakamoto, Y., and Nagatomi, R. (2006) Knockdown of hypoxia-inducible factor-1α by siRNA inhibits C2C12 myoblast differentiation. J. Cell. Biochem. 98, 642-649 (Pubitemid 43727181)
38. Mason, S. D., Howlett, R. A., Kim, M. J., Olfert, I. M., Hogan, M. C., McNulty, W., Hickey, R. P., Wagner, P. D., Kahn, C. R., Giordano, F. J., and Johnson, R. S. (2004) Loss of skeletal muscle HIF-1α results in altered exercise endurance. PLoS Biol. 2, e288
39. Pisani, D. F., and Dechesne, C. A. (2005) Skeletal muscle HIF-1α expression is dependent on muscle fiber type. J. Gen. Physiol. 126, 173-178 (Pubitemid 41124193)
40. Stroka, D. M., Burkhardt, T., Desbaillets, I., Wenger, R. H., Neil, D. A., Bauer, C., Gassmann, M., and Candinas, D. (2001) HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J. 15, 2445-2453 (Pubitemid 33063172)
41. Du, Y., Liu, Z., Gu, L., Zhou, J., Zhu, B. D., Ji, J., and Deng, D. (2012) Characterization of human gastric carcinoma-related methylation of 9 miR CpG islands and repression of their expressions in vitro and in vivo. BMC Cancer 12, 249
42. Scatena, R. (2012) Mitochondria and drugs. Adv. Exp. Med. Biol. 942, 329-346
43. Guzy, R. D., and Schumacker, P. T. (2006) Oxygen sensing by mitochondria at complex III. The paradox of increased reactive oxygen species during hypoxia. Exp. Physiol. 91, 807-819 (Pubitemid 44266577)
44. d'Albis, A., Couteaux, R., Janmot, C., Roulet, A., and Mira, J. C. (1988) Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals. Myosin isoform analysis. Eur. J. Biochem. 174, 103-110
45. Tsuchiya, S., Oku, M., Imanaka, Y., Kunimoto, R., Okuno, Y., Terasawa, K., Sato, F., Tsujimoto, G., and Shimizu, K. (2009) MicroRNA-338-3p and microRNA-451 contribute to the formation of basolateral polarity in epithelial cells. Nucleic Acids Res. 37, 3821-3827
46. Hildebrand, J., Rütze, M., Walz, N., Gallinat, S., Wenck, H., Deppert, W., Grundhoff, A., and Knott, A. (2011) A comprehensive analysis of microRNA expression during human keratinocyte differentiation in vitro and in vivo. J. Invest Dermatol. 131, 20-29
47. Kane, N. M., Meloni, M., Spencer, H. L., Craig, M. A., Strehl, R., Milligan, G., Houslay, M. D., Mountford, J. C., Emanueli, C., and Baker, A. H. (2010) Derivation of endothelial cells from human embryonic stem cells by directed differentiation. Analysis of microRNA and angiogenesis in vitro and in vivo. Arterioscler. Thromb. Vasc. Biol. 30, 1389-1397
48. Zhang, Y., Fei, M., Xue, G., Zhou, Q., Jia, Y., Li, L., Xin, H., and Sun, S. (2012) Elevated levels of hypoxia-inducible microRNA-210 in pre-eclampsia. New insights into molecular mechanisms for the disease. J. Cell Mol. Med. 16, 249-259
49. Guttridge, D. C., Albanese, C., Reuther, J. Y., Pestell, R. G., and Baldwin, A. S., Jr. (1999) NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell. Biol. 19, 5785-5799 (Pubitemid 29339933)
50. Milkiewicz, M., Pugh, C. W., and Egginton, S. (2004) Inhibition of endogenous HIF inactivation induces angiogenesis in ischaemic skeletal muscles of mice. J. Physiol. 560, 21-26 (Pubitemid 39406013)
51. Bloomer, R. J., and Goldfarb, A. H. (2004) Anaerobic exercise and oxidative stress. A review. Can J. Appl. Physiol. 29, 245-263 (Pubitemid 38834582)
52. Musarò, A., Fulle, S., and Fanò, G. (2010) Oxidative stress and muscle homeostasis. Curr. Opin Clin. Nutr. Metab. Care 13, 236-242
53. Kon, M., Tanabe, K., Lee, H., Kimura, F., Akimoto, T., and Kono, I. (2007) Eccentric muscle contractions induce greater oxidative stress than concentric contractions in skeletal muscle. Appl Physiol. Nutr. Metab. 32, 273-281