mir-1 microRNA precursor family

miR-1
mIR-1 microRNA precursor family
Identifiers
Symbol mir-1
Rfam RF00103
miRBase MI0000651
miRBase family MIPF0000038
Entrez 406904
HUGO HGNC:31499
OMIM 609326
Other data
RNA type Gene; miRNA;
Domain(s) Metazoa
GO 0035195
SO 0001244
Locus Chr. 20 q13.33

The miR-1 microRNA precursor is a small micro RNA that regulates its target protein's expression in the cell. microRNAs are transcribed as ~70 nucleotide precursors and subsequently processed by the Dicer enzyme to give a ~22 nucleotide products. In this case the mature sequence comes from the 3' arm of the precursor. The mature products are thought to have regulatory roles through complementarity to mRNA. In humans there are two distinct microRNAs that share an identical mature sequence, these are called miR-1-1 and miR-1-2.

These micro RNAs have pivotal roles in development and physiology of muscle tissues including the heart.[1][2] MiR-1 is known to be involved in important role in heart diseases such as hypertrophy, myocardial infarction, and arrhythmias.[3][4][5] Studies have shown that MiR-1 is an important regulator of heart adaption after ischemia or ischaemic stress and it is upregulated in the remote myocardium of patients with myocardial infarction.[6] Also MiR-1 is downregulated in myocardial infarcted tissue compared to healthy heart tissue.[7] Plasma levels of MiR-1 can be used as a sensitive biomarker for myocardial infarction.[8]

Targets of miR-1

The heat shock protein, HSP60 is also known to be a target for post-transcriptional regulation by miR-1 and miR-206. HSP60 is a component of the defence mechanism against diabetic myocardial injury and its level is reduced in the diabetic myocardium. In both in vivo and in vitro experiments increased levels of glucose in myocardiomyctes led to significant upregulation of miR-1 and miR-206 with resulting modulation of HSP60 leading to accelerated glucose-mediated apoptosis in cardiomyocetes.[9] The level of HSP70 is also a target for post-transcriptional repression by MiR-1.[10]

MiR-1 has key roles in the development and differentiation of smooth and skeletal muscles.[11][12][13] For example in the lineage-specific differention of smooth muscle cells from embroyonic stem cell derived cultures, MiR-1 is required; as its loss of function resulted in a reduction in smooth muscle cell biomarkers and a reduction in the derived smooth muscle cell population. There is evidence that the control of smooth muscle cell differentiation by MiR-1 may be mediated by the down regulation of Kruppel-like factor 4 (KLF4), since a MiR-1 recognition site is predicted in the 3' UTR of KLF4 and inhibition of MiR-1 results in reversed down-regulation of KLF4 and an inhibition of smooth muscle cell differentiation.[14] A mutation in the 3' UTR of the myostatin gene in Texel sheep creates a miR-1 and miR-206 target site. This is likely to cause the muscular phenotype of this breed of sheep.[15]

Clinical relevance of miR-1

Mir-1 plays an important role in some cancers. Rhabdomyosarcoma is the most common soft tissue sarcoma in children. Since the tumor results from undifferentiated cells, agents that promote differentiation hold promise as possible therapies. A study showed that levels of mir-1 and mir-133a were drastically reduced in tumourous cell lines whilst their targets were up-regulated.[16]

Introduction of miR-1 and miR-133a into an embryonal rhabdomyosarcoma-derived cell line is cytostatic, which suggested a strong tumour-suppressive role for these microRNAs. Expression of miR-1 but not miR-133a gave transcriptional profiles that were consistent with a strong promyogenic influence on the cells, again demonstrating the role of miR-1 in muscle differentiation from precursor stem cells. The authors propose that miR-1 and miR-133a act to repress isoforms of genes that are not normally expressed in muscle cells. All of these observations suggest that mis-regulation of miR-1 and miR-133a can result in tumorogenesis via abolition of the suppressive effect they have on certain gene targets and of the removal of the promotion of differentiation of the cells exerted my miR-1.[16]

The involvement of miR-1 in cancer is not limited to cancers of muscle and muscle tissues. MiR-1 may have a tumour-suppressive effect in bladder cancer by regulation of LIM and SH3 protein 1 (LASP1) .[17] In lung cancer there is evidence for the down-regulation of miR-1.[18]

There is evidence for the role of miR-1-2 as a modulator in acute myeloid leukemia via its transcription by the zinc-finger transcription factor, EVI1, ectopic virus expression site 1. ChIP assays have shown that EVI1 binds strongly to the promoters of miR-1-2 and miR-133-a-1, and expression of EVI1 is significantly correlated with the expression of miR-1-2 and miR-133-a-1 in established cell lines and in patient samples. However, only miR-1-2 was involved in abnormal proliferation in EVI1 expressing cell lines.[19]

miR-1 and related microRNA miR-499 are proposed to be involved in the regulation of hepatocellular carcinoma (HCC) pathogenisis.[20] These two microRNAs have been shown to downregulate the expression of the ets1 proto-oncogene in cell lines HepG2 by targeting the 3'UTR of ets1. ets1 is involved in extracellular matrix (ECM) degradation which is an important process required for tumor cell invasion and migration.

References

  1. ↑ Mishima Y, Stahlhut C, Giraldez AJ (2007). "miR-1-2 gets to the heart of the matter". Cell 129 (2): 247–9. doi:10.1016/j.cell.2007.04.008. PMID 17448987.
  2. ↑ Zhao Y, Ransom JF, Li A et al. (2007). "Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2". Cell 129 (2): 303–17. doi:10.1016/j.cell.2007.03.030. PMID 17397913.
  3. ↑ Cai B, Pan Z, Lu Y (2010). "The roles of microRNAs in heart diseases: a novel important regulator.". Curr Med Chem 17 (5): 407–11. doi:10.2174/092986710790226129. PMID 20015039.
  4. ↑ Silvestri P, Di Russo C, Rigattieri S, Fedele S, Todaro D, Ferraiuolo G et al. (2009). "MicroRNAs and ischemic heart disease: towards a better comprehension of pathogenesis, new diagnostic tools and new therapeutic targets.". Recent Pat Cardiovasc Drug Discov 4 (2): 109–18. doi:10.2174/157489009788452977. PMID 19519553.
  5. ↑ Zorio E, Medina P, Rueda J, Millán JM, Arnau MA, Beneyto M et al. (2009). "Insights into the role of microRNAs in cardiac diseases: from biological signalling to therapeutic targets.". Cardiovasc Hematol Agents Med Chem 7 (1): 82–90. doi:10.2174/187152509787047676. PMID 19149547.
  6. ↑ Bostjancic E, Zidar N, Stajner D, Glavac D (2010). "MicroRNA miR-1 is up-regulated in remote myocardium in patients with myocardial infarction.". Folia Biol (Praha) 56 (1): 27–31. PMID 20163779.
  7. ↑ Bostjancic E, Zidar N, Stajer D, Glavac D (2010). "MicroRNAs miR-1, miR-133a, miR-133b and miR-208 are dysregulated in human myocardial infarction.". Cardiology 115 (3): 163–9. doi:10.1159/000268088. PMID 20029200.
  8. ↑ D'Alessandra Y, Devanna P, Limana F, Straino S, Di Carlo A, Brambilla PG et al. (2010). "Circulating microRNAs are new and sensitive biomarkers of myocardial infarction.". Eur Heart J 31 (22): 2765–73. doi:10.1093/eurheartj/ehq167. PMC 2980809. PMID 20534597.
  9. ↑ Shan ZX, Lin QX, Deng CY, Zhu JN, Mai LP, Liu JL et al. (2010). "miR-1/miR-206 regulate Hsp60 expression contributing to glucose-mediated apoptosis in cardiomyocytes". FEBS Lett 584 (16): 3592–600. doi:10.1016/j.febslet.2010.07.027. PMID 20655308.
  10. ↑ Xu C, Lu Y, Pan Z, Chu W, Luo X, Lin H et al. (2007). "The muscle-specific microRNAs miR-1 and miR-133 produce opposing effects on apoptosis by targeting HSP60, HSP70 and caspase-9 in cardiomyocytes.". J Cell Sci 120 (Pt 17): 3045–52. doi:10.1242/jcs.010728. PMID 17715156. (Retracted. If this is intentional, please replace {{Retracted}} with {{Retracted|intentional=yes}}.)
  11. ↑ Chen Y, Gelfond J, McManus LM, Shireman PK (2010). "Temporal MicroRNA Expression during in vitro Myogenic Progenitor Cell Proliferation and Differentiation: Regulation of Proliferation by miR-682.". Physiol Genomics 43: 621–630. doi:10.1152/physiolgenomics.00136.2010. PMID 20841498.
  12. ↑ Chen JF, Tao Y, Li J, Deng Z, Yan Z, Xiao X et al. (2010). "microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7.". J Cell Biol 190 (5): 867–79. doi:10.1083/jcb.200911036. PMC 2935565. PMID 20819939.
  13. ↑ Townley-Tilson WH, Callis TE, Wang D (2010). "MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease.". Int J Biochem Cell Biol 42 (8): 1252–5. doi:10.1016/j.biocel.2009.03.002. PMC 2904322. PMID 20619221.
  14. ↑ Xie C, Huang H, Sun X, Guo Y, Hamblin M, Ritchie RP et al. (2010). "MicroRNA-1 Regulates Smooth Muscle Cell Differentiation by Repressing KLF4.". Stem Cells Dev 20 (2): 205–210. doi:10.1089/scd.2010.0283. PMID 20799856.
  15. ↑ Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibé B, Bouix J, Caiment F, Elsen JM, Eychenne F, Larzul C, Laville E, Meish F, Milenkovic D, Tobin J, Charlier C, Georges M (2006). "A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep.". Nat Genet 38 (7): 813–8. doi:10.1038/ng1810. PMID 16751773.
  16. ↑ 16.0 16.1 Rao PK, Missiaglia E, Shields L, Hyde G, Yuan B, Shepherd CJ et al. (2010). "Distinct roles for miR-1 and miR-133a in the proliferation and differentiation of rhabdomyosarcoma cells.". FASEB J 24 (9): 3427–37. doi:10.1096/fj.09-150698. PMC 3231107. PMID 20466878.
  17. ↑ Chiyomaru T, Enokida H, Kawakami K, Tatarano S, Uchida Y, Kawahara K et al. (2010). "Functional role of LASP1 in cell viability and its regulation by microRNAs in bladder cancer.". Urol Oncol 30: 434–443. doi:10.1016/j.urolonc.2010.05.008. PMID 20843712.
  18. ↑ Nasser MW, Datta J, Nuovo G, Kutay H, Motiwala T, Majumder S et al. (2008). "Down-regulation of micro-RNA-1 (miR-1) in lung cancer Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1.". J Biol Chem 283 (48): 33394–405. doi:10.1074/jbc.M804788200. PMC 2586284. PMID 18818206.
  19. ↑ Gómez-Benito M, Conchillo A, García MA, Vázquez I, Maicas M, Vicente C et al. (2010). "EVI1 controls proliferation in acute myeloid leukaemia through modulation of miR-1-2.". Br J Cancer 103 (8): 1292–6. doi:10.1038/sj.bjc.6605874. PMC 2967053. PMID 20842122.
  20. ↑ Wu, Y.; Hu, Z.; Fu, H.; Tie, Y.; Zhang, H.; Wu, Y.; Zheng, X. (2012). "MicroRNA-1 and microRNA-499 downregulate the expression of the ets1 proto-oncogene in HepG2 cells". Oncology Reports 28 (2): 701–706. doi:10.3892/or.2012.1850. PMID 22664953.

Further reading

  1. ↑ Chen J, Yin H, Jiang Y, Radhakrishnan SK, Huang ZP, Li J, Shi Z, Catharina EP, Gui Y, Wang DZ, Zheng XL (2010). "Induction of MicroRNA-1 by Myocardin in Smooth Muscle Cells Inhibits Cell Proliferation.". Arterioscler Thromb Vasc Biol 31 (2): 368–375. doi:10.1161/ATVBAHA.110.218149. PMID 21051663.
  2. ↑ Sumiyoshi K, Kubota S, Ohgawara T, Kawata K, Nishida T, Shimo T, Yamashiro T, Takigawa M (2010). "Identification of miR-1 as a micro RNA that supports late-stage differentiation of growth cartilage cells.". Biochem Biophys Res Commun 402 (2): 286–90. doi:10.1016/j.bbrc.2010.10.016. PMID 20937250.
  3. ↑ Xie C, Huang H, Sun X, Guo Y, Hamblin M, Ritchie RP, Garcia-Barrio MT, Zhang J, Chen YE (2010). "MicroRNA-1 Regulates Smooth Muscle Cell Differentiation by Repressing Kruppel-Like Factor 4.". Stem Cells Dev 20 (2): 205–210. doi:10.1089/scd.2010.0283. PMID 20799856.
  4. ↑ Li Q, Song XW, Zou J, Wang GK, Kremneva E, Li XQ, Zhu N, Sun T, Lappalainen P, Yuan WJ, Qin YW, Jing Q (2010). "Attenuation of microRNA-1 derepresses the cytoskeleton regulatory protein twinfilin-1 to provoke cardiac hypertrophy.". J Cell Sci 123 (Pt 14): 2444–52. doi:10.1242/jcs.067165. PMID 20571053.
  5. ↑ Jiang Y, Yin H, Zheng XL (2010). "MicroRNA-1 inhibits myocardin-induced contractility of human vascular smooth muscle cells.". J Cell Physiol 225 (2): 506–11. doi:10.1002/jcp.22230. PMID 20458751.
  6. ↑ Cheng Y, Tan N, Yang J, Liu X, Cao X, He P, Dong X, Qin S, Zhang C (2010). "A translational study of circulating cell-free microRNA-1 in acute myocardial infarction.". Clin Sci (Lond) 119 (2): 87–95. doi:10.1042/CS20090645. PMID 20218970.
  7. ↑ Sluijter JP, van Mil A, van Vliet P, Metz CH, Liu J, Doevendans PA, Goumans MJ (2010). "MicroRNA-1 and -499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells.". Arterioscler Thromb Vasc Biol 30 (4): 859–68. doi:10.1161/ATVBAHA.109.197434. PMID 20081117.
  8. ↑ Divakaran VG (2010). "MicroRNAs miR-1, -133 and -208: same faces, new roles.". Cardiology 115 (3): 172–3. doi:10.1159/000272540. PMID 20068301.
  9. ↑ Girmatsion Z, Biliczki P, Bonauer A, Wimmer-Greinecker G, Scherer M, Moritz A, Bukowska A, Goette A, Nattel S, Hohnloser SH, Ehrlich JR (2009). "Changes in microRNA-1 expression and IK1 up-regulation in human atrial fibrillation.". Heart Rhythm 6 (12): 1802–9. doi:10.1016/j.hrthm.2009.08.035. PMID 19959133.
  10. ↑ Elia L, Contu R, Quintavalle M, Varrone F, Chimenti C, Russo MA, Cimino V, De Marinis L, Frustaci A, Catalucci D, Condorelli G (2009). "Reciprocal regulation of microRNA-1 and insulin-like growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions.". Circulation 120 (23): 2377–85. doi:10.1161/CIRCULATIONAHA.109.879429. PMC 2825656. PMID 19933931.
  11. ↑ Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, Li K, Yu B, Li Z, Wang R, Wang L, Li Q, Wang N, Shan H, Li Z, Yang B (2010). "Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction.". Biochem Biophys Res Commun 391 (1): 73–7. doi:10.1016/j.bbrc.2009.11.005. PMID 19896465.
  12. ↑ Lin WC, Huang KY, Chen SC, Huang TY, Chen SJ, Huang PJ, Tang P (2009). "Malate dehydrogenase is negatively regulated by miR-1 in Trichomonas vaginalis.". Parasitol Res 105 (6): 1683–9. doi:10.1007/s00436-009-1616-5. PMID 19777264.
  13. ↑ Shan H, Li X, Pan Z, Zhang L, Cai B, Zhang Y, Xu C, Chu W, Qiao G, Li B, Lu Y, Yang B (2009). "Tanshinone IIA protects against sudden cardiac death induced by lethal arrhythmias via repression of microRNA-1.". Br J Pharmacol 158 (5): 1227–35. doi:10.1111/j.1476-5381.2009.00377.x. PMC 2782332. PMID 19775284.
  14. ↑ Yan D, Dong Xda E, Chen X, Wang L, Lu C, Wang J, Qu J, Tu L (2009). "MicroRNA-1/206 targets c-Met and inhibits rhabdomyosarcoma development.". J Biol Chem 284 (43): 29596–604. doi:10.1074/jbc.M109.020511. PMC 2785592. PMID 19710019.
  15. ↑ Lu Y, Zhang Y, Shan H, Pan Z, Li X, Li B, Xu C, Zhang B, Zhang F, Dong D, Song W, Qiao G, Yang B (2009). "MicroRNA-1 downregulation by propranolol in a rat model of myocardial infarction: a new mechanism for ischaemic cardioprotection.". Cardiovasc Res 84 (3): 434–41. doi:10.1093/cvr/cvp232. PMID 19581315.
  16. ↑ Takaya T, Ono K, Kawamura T, Takanabe R, Kaichi S, Morimoto T, Wada H, Kita T, Shimatsu A, Hasegawa K (2009). "MicroRNA-1 and MicroRNA-133 in spontaneous myocardial differentiation of mouse embryonic stem cells.". Circ J 73 (8): 1492–7. doi:10.1253/circj.CJ-08-1032. PMID 19521018.
  17. ↑ Tang Y, Zheng J, Sun Y, Wu Z, Liu Z, Huang G (2009). "MicroRNA-1 regulates cardiomyocyte apoptosis by targeting Bcl-2.". Int Heart J 50 (3): 377–87. doi:10.1536/ihj.50.377. PMID 19506341.
  18. ↑ Shan ZX, Lin QX, Fu YH, Deng CY, Zhou ZL, Zhu JN, Liu XY, Zhang YY, Li Y, Lin SG, Yu XY (2009). "Upregulated expression of miR-1/miR-206 in a rat model of myocardial infarction.". Biochem Biophys Res Commun 381 (4): 597–601. doi:10.1016/j.bbrc.2009.02.097. PMID 19245789.
  19. ↑ Mishima Y, Abreu-Goodger C, Staton AA, Stahlhut C, Shou C, Cheng C, Gerstein M, Enright AJ, Giraldez AJ (2009). "Zebrafish miR-1 and miR-133 shape muscle gene expression and regulate sarcomeric actin organization.". Genes Dev 23 (5): 619–32. doi:10.1101/gad.1760209. PMC 2658521. PMID 19240126.
  20. ↑ Ikeda S, He A, Kong SW, Lu J, Bejar R, Bodyak N, Lee KH, Ma Q, Kang PM, Golub TR, Pu WT (2009). "MicroRNA-1 negatively regulates expression of the hypertrophy-associated calmodulin and Mef2a genes.". Mol Cell Biol 29 (8): 2193–204. doi:10.1128/MCB.01222-08. PMC 2663304. PMID 19188439.
  21. ↑ Terentyev D, Belevych AE, Terentyeva R, Martin MM, Malana GE, Kuhn DE, Abdellatif M, Feldman DS, Elton TS, Györke S (2009). "miR-1 overexpression enhances Ca(2+) release and promotes cardiac arrhythmogenesis by targeting PP2A regulatory subunit B56alpha and causing CaMKII-dependent hyperphosphorylation of RyR2.". Circ Res 104 (4): 514–21. doi:10.1161/CIRCRESAHA.108.181651. PMID 19131648.
  22. ↑ Yu XY, Song YH, Geng YJ, Lin QX, Shan ZX, Lin SG, Li Y (2008). "Glucose induces apoptosis of cardiomyocytes via microRNA-1 and IGF-1.". Biochem Biophys Res Commun 376 (3): 548–52. doi:10.1016/j.bbrc.2008.09.025. PMID 18801338.
  23. ↑ Sweetman D, Goljanek K, Rathjen T, Oustanina S, Braun T, Dalmay T, Münsterberg A (2008). "Specific requirements of MRFs for the expression of muscle specific microRNAs, miR-1, miR-206 and miR-133.". Dev Biol 321 (2): 491–9. doi:10.1016/j.ydbio.2008.06.019. PMID 18619954.
  24. ↑ Datta J, Kutay H, Nasser MW, Nuovo GJ, Wang B, Majumder S, Liu CG, Volinia S, Croce CM, Schmittgen TD, Ghoshal K, Jacob ST (2008). "Methylation mediated silencing of MicroRNA-1 gene and its role in hepatocellular carcinogenesis.". Cancer Res 68 (13): 5049–58. doi:10.1158/0008-5472.CAN-07-6655. PMC 2562630. PMID 18593903.
  25. ↑ Simon DJ, Madison JM, Conery AL, Thompson-Peer KL, Soskis M, Ruvkun GB, Kaplan JM, Kim JK (2008). "The microRNA miR-1 regulates a MEF-2-dependent retrograde signal at neuromuscular junctions.". Cell 133 (5): 903–15. doi:10.1016/j.cell.2008.04.035. PMC 2553566. PMID 18510933.
  26. ↑ Luo X, Lin H, Pan Z, Xiao J, Zhang Y, Lu Y, Yang B, Wang Z (2008). "Down-regulation of miR-1/miR-133 contributes to re-expression of pacemaker channel genes HCN2 and HCN4 in hypertrophic heart.". J Biol Chem 283 (29): 20045–52. doi:10.1074/jbc.M801035200. PMID 18458081.
  27. ↑ Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, Zhang Y, Xu C, Bai Y, Wang H, Chen G, Wang Z (2007). "The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2.". Nat Med 13 (4): 486–91. doi:10.1038/nm1569. PMID 17401374.
  28. ↑ Mishima T, Mizuguchi Y, Kawahigashi Y, Takizawa T, Takizawa T (2007). "RT-PCR-based analysis of microRNA (miR-1 and -124) expression in mouse CNS.". Brain Res 1131 (1): 37–43. doi:10.1016/j.brainres.2006.11.035. PMID 17182009.
  29. ↑ Nakajima N, Takahashi T, Kitamura R, Isodono K, Asada S, Ueyama T, Matsubara H, Oh H (2006). "MicroRNA-1 facilitates skeletal myogenic differentiation without affecting osteoblastic and adipogenic differentiation.". Biochem Biophys Res Commun 350 (4): 1006–12. doi:10.1016/j.bbrc.2006.09.153. PMID 17045567.
  30. ↑ McCarthy JJ, Esser KA (2007). "MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy.". J Appl Physiol 102 (1): 306–13. doi:10.1152/japplphysiol.00932.2006. PMID 17008435.
  31. ↑ Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ (2006). "The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation.". Nat Genet 38 (2): 228–33. doi:10.1038/ng1725. PMC 2538576. PMID 16380711.
  32. ↑ Kwon C, Han Z, Olson EN, Srivastava D (2005). "MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling.". Proc Natl Acad Sci U S A 102 (52): 18986–91. doi:10.1073/pnas.0509535102. PMC 1315275. PMID 16357195.
  33. ↑ Sokol NS, Ambros V (2005). "Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth.". Genes Dev 19 (19): 2343–54. doi:10.1101/gad.1356105. PMC 1240043. PMID 16166373.
  34. ↑ Jacoby GA, Tran J (1999). "Sequence of the MIR-1 beta-lactamase gene.". Antimicrob Agents Chemother 43 (7): 1759–60. PMC 89358. PMID 10390237.
  35. ↑ Bingham GE, Salisbury FB, Campbell WF, Carman JG, Bubenheim DL, Yendler B, Sytchev VN, Berkovitch YuA , Levinskikh MA, Podolsky IG (1996). "The Spacelab-Mir-1 "Greenhouse-2" experiment.". Adv Space Res 18 (4–5): 225–32. doi:10.1016/0273-1177(95)00881-E. PMID 11538801.
  36. ↑ Papanicolaou GA, Medeiros AA, Jacoby GA (1990). "Novel plasmid-mediated beta-lactamase (MIR-1) conferring resistance to oxyimino- and alpha-methoxy beta-lactams in clinical isolates of Klebsiella pneumoniae". Antimicrob Agents Chemother 34 (11): 2200–9. doi:10.1128/aac.34.11.2200. PMC 172023. PMID 1963529.
  37. ↑ Lee, RC; Ambros V (2001). "An extensive class of small RNAs in Caenorhabditis elegans". Science 294 (5543): 862–864. doi:10.1126/science.1065329. PMID 11679672.
  38. ↑ Ambros, V (2001). "microRNAs: tiny regulators with great potential". Cell 107 (7): 823–826. doi:10.1016/S0092-8674(01)00616-X. PMID 11779458.

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