Robustness of the hypoxic response: Another job for miRNAs?

Developmental Dynamics

Volumn 241, Issue 12, 2012, Pages 1842-1848

  De Lella Ezcurra, Ana Laura ^a   Bertolin, Agustina P ^a   Melani, Mariana ^a   Wappner, Pablo ^a,b  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Angiogenesis; Hypoxia; Hypoxia inducible factor; MicroRNAs; Robustness

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MICRORNA; RNA INDUCED SILENCING COMPLEX; RNA POLYMERASE II;

3' UNTRANSLATED REGION; ANGIOGENESIS; ARTICLE; BIOLOGY; DEVELOPMENT; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HYPOXIA; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; PHYSIOLOGY; POSITIVE FEEDBACK; PRIORITY JOURNAL; RNA STRUCTURE;

ANIMALS; ANOXIA; HUMANS; MICRORNAS; NEOVASCULARIZATION, PHYSIOLOGIC; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84869868714     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23865     Document Type: Article

References (85)

1. Alon U. 2007. Network motifs: theory and experimental approaches. Nat Rev Genet 8: 450-461.
2. Alvarez-Saavedra E, Horvitz HR. 2010. Many families of C. elegans microRNAs are not essential for development or viability. Curr Biol 20: 367-373.
3. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
4. Barkai N, Shilo BZ. 2007. Variability and robustness in biomolecular systems. Mol Cell 28: 755-760.
5. Becskei A, Serrano L. 2000. Engineering stability in gene networks by autoregulation. Nature 405: 590-593.
6. Bruick RK. 2003. Oxygen sensing in the hypoxic response pathway: regulation of the hypoxia-inducible transcription factor. Genes Dev 17: 2614-2623.
7. Bruning U, Cerone L, Neufeld Z, Fitzpatrick SF, Cheong A, Scholz CC, Simpson DA, Leonard MO, Tambuwala MM, Cummins EP, Taylor CT. 2011. MicroRNA-155 promotes resolution of hypoxia-inducible factor 1alpha activity during prolonged hypoxia. Mol Cell Biol 31: 4087-4096.
8. Bussolati B, Moggio A, Collino F, Aghemo G, D'Armento G, Grange C, Camussi G. 2012. Hypoxia modulates the undifferentiated phenotype of human renal inner medullary CD133+ progenitors through Oct4/miR-145 balance. Am J Physiol Renal Physiol 302: F116-128.
9. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858-864.
10. Cha ST, Chen PS, Johansson G, Chu CY, Wang MY, Jeng YM, Yu SL, Chen JS, Chang KJ, Jee SH, Tan CT, Lin MT, Kuo ML. 2010. MicroRNA-519c suppresses hypoxia-inducible factor-1alpha expression and tumor angiogenesis. Cancer Res 70: 2675-2685.
11. Chan SY, Loscalzo J. 2010. MicroRNA-210: a unique and pleiotropic hypoxamir. Cell Cycle 9: 1072-1083.
12. Chung AS, Ferrara N. 2011. Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol 27: 563-584.
13. Djuranovic S, Nahvi A, Green R. 2011. A parsimonious model for gene regulation by miRNAs. Science 331: 550-553.
14. Du R, Sun W, Xia L, Zhao A, Yu Y, Zhao L, Wang H, Huang C, Sun S. 2012. Hypoxia-induced down-regulation of microRNA-34a promotes EMT by targeting the Notch signaling pathway in tubular epithelial cells. PLoS One 7: e30771.
15. Dunwoodie SL. 2009. The role of hypoxia in development of the mammalian embryo. Dev Cell 17: 755-773.
16. Ebert MS, Sharp PA. 2012. Roles for MicroRNAs in conferring robustness to biological processes. Cell 149: 515-524.
17. Fang J, Song XW, Tian J, Chen HY, Li DF, Wang JF, Ren AJ, Yuan WJ, Lin L. 2012. Overexpression of microRNA-378 attenuates ischemia-induced apoptosis by inhibiting caspase-3 expression in cardiac myocytes. Apoptosis 17: 410-423.
18. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613.
19. Fraisl P, Mazzone M, Schmidt T, Carmeliet P. 2009. Regulation of angiogenesis by oxygen and metabolism. Dev Cell 16: 167-179.
20. Freeman M. 2000. Feedback control of intercellular signalling in development. Nature 408: 313-319.
21. Gabay L, Scholz H, Golembo M, Klaes A, Shilo BZ, Klambt C. 1996. EGF receptor signaling induces pointed P1 transcription and inactivates Yan protein in the Drosophila embryonic ventral ectoderm. Development 122: 3355-3362.
22. Gorospe M, Tominaga K, Wu X, Fahling M, Ivan M. 2011. Post-transcriptional control of the hypoxic response by RNA-binding proteins and MicroRNAs. Front Mol Neurosci 4: 7.
23. Graham TG, Tabei SM, Dinner AR, Rebay I. 2010. Modeling bistable cell-fate choices in the Drosophila eye: qualitative and quantitative perspectives. Development 137: 2265-2278.
24. Guo L, Qiu Z, Wei L, Yu X, Gao X, Jiang S, Tian H, Jiang C, Zhu D. 2012. The MicroRNA-328 regulates hypoxic pulmonary hypertension by targeting at insulin growth factor 1 receptor and L-type calcium channel-alpha1C. Hypertension 59: 1006-1013.
25. Hartman JLt, Garvik B, Hartwell L. 2001. Principles for the buffering of genetic variation. Science 291: 1001-1004.
26. Herranz H, Cohen SM. 2010. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev 24: 1339-1344.
27. Hewitson KS, McNeill LA, Riordan MV, Tian YM, Bullock AN, Welford RW, Elkins JM, Oldham NJ, Bhattacharya S, Gleadle JM, Ratcliffe PJ, Pugh CW, Schofield CJ. 2002. Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family. J Biol Chem 277: 26351-26355.
28. Hornstein E, Shomron N. 2006. Canalization of development by microRNAs. Nat Genet 38( Suppl): S20-24.
29. Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB, Zhang Y. 2006. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One 1: e116.
30. Huang LE, Gu J, Schau M, Bunn HF. 1998. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95: 7987-7992.
31. Huang X, Le QT, Giaccia AJ. 2010. MiR-210: micromanager of the hypoxia pathway. Trends Mol Med 16: 230-237.
32. Inui M, Martello G, Piccolo S. 2010. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 11: 252-263.
33. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
34. Jaubert S, Mereau A, Antoniewski C, Tagu D. 2007. MicroRNAs in Drosophila: the magic wand to enter the chamber of secrets? Biochimie 89: 1211-1220.
35. Kallio PJ, Okamoto K, O'Brien S, Carrero P, Makino Y, Tanaka H, Poellinger L. 1998. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J 17: 6573-6586.
36. Kelly BD, Hackett SF, Hirota K, Oshima Y, Cai Z, Berg-Dixon S, Rowan A, Yan Z, Campochiaro PA, Semenza GL. 2003. Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res 93: 1074-1081.
37. Kelly TJ, Souza AL, Clish CB, Puigserver P. 2011. A hypoxia-induced positive feedback loop promotes hypoxia-inducible factor 1alpha stability through miR-210 suppression of glycerol-3-phosphate dehydrogenase 1-like. Mol Cell Biol 31: 2696-2706.
38. Kim VN. 2005. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6: 376-385.
39. Kitano H. 2004. Biological robustness. Nat Rev Genet 5: 826-837.
40. Kulshreshtha R, Davuluri RV, Calin GA, Ivan M. 2008. A microRNA component of the hypoxic response. Cell Death Differ 15: 667-671.
41. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. 2002. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 16: 1466-1471.
42. Lei Z, Li B, Yang Z, Fang H, Zhang GM, Feng ZH, Huang B. 2009. Regulation of HIF-1alpha and VEGF by miR-20b tunes tumor cells to adapt to the alteration of oxygen concentration. PLoS One 4: e7629.
43. Leung AK, Sharp PA. 2010. MicroRNA functions in stress responses. Mol Cell 40: 205-215.
44. Li X, Carthew RW. 2005. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123: 1267-1277.
45. Li X, Cassidy JJ, Reinke CA, Fischboeck S, Carthew RW. 2009. A microRNA imparts robustness against environmental fluctuation during development. Cell 137: 273-282.
46. Lisy K, Peet DJ. 2008. Turn me on: regulating HIF transcriptional activity. Cell Death Differ 15: 642-649.
47. Loscalzo J. 2010. The cellular response to hypoxia: tuning the system with microRNAs. J Clin Invest 120: 3815-3817.
48. Lu X, Kang Y. 2010. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res 16: 5928-5935.
49. Majmundar AJ, Wong WJ, Simon MC. 2010. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40: 294-309.
50. Mangan S, Alon U. 2003. Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci USA 100: 11980-11985.
51. Martinez NJ, Ow MC, Barrasa MI, Hammell M, Sequerra R, Doucette-Stamm L, Roth FP, Ambros VR, Walhout AJ. 2008. A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes Dev 22: 2535-2549.
52. Maxwell PH, Pugh CW, Ratcliffe PJ. 1993. Inducible operation of the erythropoietin 3′ enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism. Proc Natl Acad Sci USA 90: 2423-2427.
53. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275.
54. Mendell JT, Olson EN. 2012. MicroRNAs in stress signaling and human disease. Cell 148: 1172-1187.
55. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U. 2002. Network motifs: simple building blocks of complex networks. Science 298: 824-827.
56. Miska EA, Alvarez-Saavedra E, Abbott AL, Lau NC, Hellman AB, McGonagle SM, Bartel DP, Ambros VR, Horvitz HR. 2007. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 3: e215.
57. O'Neill EM, Rebay I, Tjian R, Rubin GM. 1994. The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78: 137-147.
58. Osella M, Bosia C, Cora D, Caselle M. 2011. The role of incoherent microRNA-mediated feedforward loops in noise buffering. PLoS Comput Biol 7: e1001101.
59. Pelaez N, Carthew RW. 2012. Biological robustness and the role of MicroRNAs: a network perspective. Curr Top Dev Biol 99: 237-255.
60. Puissegur MP, Mazure NM, Bertero T, Pradelli L, Grosso S, Robbe-Sermesant K, Maurin T, Lebrigand K, Cardinaud B, Hofman V, Fourre S, Magnone V, Ricci JE, Pouyssegur J, Gounon P, Hofman P, Barbry P, 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.
61. Raser JM, O'Shea EK. 2005. Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013.
62. Re A, Cora D, Taverna D, Caselle M. 2009. Genome-wide survey of microRNA-transcription factor feed-forward regulatory circuits in human. Mol Biosyst 5: 854-867.
63. Rebay I, Rubin GM. 1995. Yan functions as a general inhibitor of differentiation and is negatively regulated by activation of the Ras1/MAPK pathway. Cell 81: 857-866.
64. Rey S, Semenza GL. 2010. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 86: 236-242.
65. Rohrbaugh M, Ramos E, Nguyen D, Price M, Wen Y, Lai ZC. 2002. Notch activation of yan expression is antagonized by RTK/pointed signaling in the Drosophila eye. Curr Biol 12: 576-581.
66. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
67. Semenza GL. 2007. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007: cm8.
68. Shen-Orr SS, Milo R, Mangan S, Alon U. 2002. Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31: 64-68.
69. Shi H. 2009. Hypoxia inducible factor 1 as a therapeutic target in ischemic stroke. Curr Med Chem 16: 4593-4600.
70. Silva-Rocha R, de Lorenzo V. 2010. Noise and robustness in prokaryotic regulatory networks. Annu Rev Microbiol 64: 257-275.
71. Simon MC, Keith B. 2008. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9: 285-296.
72. Staszel T, Zapala B, Polus A, Sadakierska-Chudy A, Kiec-Wilk B, Stepien E, Wybranska I, Chojnacka M, Dembinska-Kiec A. 2011. Role of microRNAs in endothelial cell pathophysiology. Pol Arch Med Wewn 121: 361-366.
73. Taguchi A, Yanagisawa K, Tanaka M, Cao K, Matsuyama Y, Goto H, Takahashi T. 2008. Identification of hypoxia-inducible factor-1 alpha as a novel target for miR-17-92 microRNA cluster. Cancer Res 68: 5540-5545.
74. Tsang J, Zhu J, van Oudenaarden A. 2007. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26: 753-767.
75. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. 2007. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316: 575-579.
76. Voellenkle C, Rooij J, Guffanti A, Brini E, Fasanaro P, Isaia E, Croft L, David M, Capogrossi MC, Moles A, Felsani A, Martelli F. 2012. Deep-sequencing of endothelial cells exposed to hypoxia reveals the complexity of known and novel microRNAs. RNA 18: 472-484.
77. Wang GL, Semenza GL. 1993. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90: 4304-4308.
78. Wang GL, Semenza GL. 1995. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270: 1230-1237.
79. Wang GL, Jiang BH, Rue EA, Semenza GL. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 92: 5510-5514.
80. Wang S, Olson EN. 2009. AngiomiRs: key regulators of angiogenesis. Curr Opin Genet Dev 19: 205-211.
81. Wu CI, Shen Y, Tang T. 2009a. Evolution under canalization and the dual roles of microRNAs: a hypothesis. Genome Res 19: 734-743.
82. Wu F, Yang Z, Li G. 2009b. Role of specific microRNAs for endothelial function and angiogenesis. Biochem Biophys Res Commun 386: 549-553.
83. Xu C, Kauffmann RC, Zhang J, Kladny S, Carthew RW. 2000. Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 103: 87-97.
84. Yamakuchi M, Lotterman CD, Bao C, Hruban RH, Karim B, Mendell JT, Huso D, Lowenstein CJ. 2010. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci USA 107: 6334-6339.
85. Yeom KH, Lee Y, Han J, Suh MR, Kim VN. 2006. Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing. Nucleic Acids Res 34: 4622-4629.