Dg-Dys-Syn1 signaling in Drosophila regulates the microRNA profile

BMC Cell Biology

Volumn 13, Issue , 2012, Pages

  Marrone, April K ^a   Edeleva, Evgeniia V ^a   Kucherenko, Mariya M ^a   Hsiao, Nai Hua ^a   Shcherbata, Halyna R ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Dystroglycan; Dystrophin; microRNAs; Neuromuscular disorders; Syntrophin

Indexed keywords

DYSTROGLYCAN; DYSTROPHIN; MICRORNA; MICRORNA 252; MICRORNA 956; MICRORNA 980; SYNTROPHIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; DYSTROGLYCAN DYSTROPHIN SYNTROPHIN SIGNALING PATHWAY; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; HOMEOSTASIS; MALE; MICROARRAY ANALYSIS; MUSCULAR DYSTROPHY; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TEMPERATURE SENSITIVITY; WELFARE;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; DYSTROGLYCANS; DYSTROPHIN; DYSTROPHIN-ASSOCIATED PROTEINS; MICRORNAS; MUSCULAR DYSTROPHIES; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA;

EID: 84867896834     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-13-26     Document Type: Article

References (64)

1. Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, Cohn RD, Ross-Barta SE, Westra S, Williamson RA, et al. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 2002, 418(6896):422-425. 10.1038/nature00838, 12140559.
2. Matsumura K, Campbell KP. Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 1994, 17(1):2-15. 10.1002/mus.880170103, 8264699.
3. Cohn RD, Campbell KP. Molecular basis of muscular dystrophies. Muscle Nerve 2000, 23(10):1456-1471. 10.1002/1097-4598(200010)23:10<1456::AID-MUS2>3.0.CO;2-T, 11003781.
4. Campbell KP. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 1995, 80(5):675-679. 10.1016/0092-8674(95)90344-5, 7889563.
5. Constantin B, Sebille S, Cognard C. New insights in the regulation of calcium transfers by muscle dystrophin-based cytoskeleton: implications in DMD. JMuscle ResCell Motil 2006, 27(5-7):375-386.
6. Wallace GQ, McNally EM. Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 2009, 71:37-57. 10.1146/annurev.physiol.010908.163216, 18808326.
7. Vercherat C, Chung TK, Yalcin S, Gulbagci N, Gopinadhan S, Ghaffari S, Taneja R. Stra13 regulates oxidative stress mediated skeletal muscle degeneration. Hum Mol Genet 2009, 18(22):4304-4316. 10.1093/hmg/ddp383, 19679564.
8. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 1992, 355(6362):696-702. 10.1038/355696a0, 1741056.
9. Xiong Y, Zhou Y, Jarrett HW. Dystrophin glycoprotein complex-associated Gbetagamma subunits activate phosphatidylinositol-3-kinase/Akt signaling in skeletal muscle in a laminin-dependent manner. J Cell Physiol 2009, 219(2):402-414. 10.1002/jcp.21684, 2820875, 19117013.
10. Zhou YW, Thomason DB, Gullberg D, Jarrett HW. Binding of laminin alpha1-chain LG4-5 domain to alpha-dystroglycan causes tyrosine phosphorylation of syntrophin to initiate Rac1 signaling. Biochemistry 2006, 45(7):2042-2052. 10.1021/bi0519957, 16475793.
11. Marrone AK, Shcherbata HR. Dystrophin orchestrates the epigenetic profile of muscle cells via miRNAs. Frontiers in Genetics 2011, 2:64. 3268617, 22303359.
12. Cacchiarelli D, Martone J, Girardi E, Cesana M, Incitti T, Morlando M, Nicoletti C, Santini T, Sthandier O, Barberi L, et al. MicroRNAs involved in molecular circuitries relevant for the Duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway. Cell Metab 2010, 12(4):341-351. 10.1016/j.cmet.2010.07.008, 20727829.
13. Eisenberg I, Eran A, Nishino I, Moggio M, Lamperti C, Amato AA, Lidov HG, Kang PB, North KN, Mitrani-Rosenbaum S, et al. Distinctive patterns of microRNA expression in primary muscular disorders. Proc Natl Acad Sci U S A 2007, 104(43):17016-17021. 10.1073/pnas.0708115104, 2040449, 17942673.
14. Licursi V, Caiello I, Lombardi L, De Stefano ME, Negri R, Paggi P. Lack of dystrophin in mdx mice modulates the expression of genes involved in neuron survival and differentiation. Eur J Neurosci 2012, 35(5):691-701. 10.1111/j.1460-9568.2011.07984.x, 22309284.
15. Greener MJ, Roberts RG. Conservation of components of the dystrophin complex in Drosophila. FEBS Lett 2000, 482(1-2):13-18.
16. Dekkers LC, van der Plas MC, van Loenen PB, den Dunnen JT, van Ommen GJ, Fradkin LG, Noordermeer JN. Embryonic expression patterns of the Drosophila dystrophin-associated glycoprotein complex orthologs. Gene Expr Patterns 2004, 4(2):153-159. 10.1016/j.modgep.2003.09.004, 15161095.
17. Shcherbata HR, Yatsenko AS, Patterson L, Sood VD, Nudel U, Yaffe D, Baker D, Ruohola-Baker H. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J 2007, 26(2):481-493. 10.1038/sj.emboj.7601503, 1783456, 17215867.
18. Kucherenko MM, Marrone AK, Rishko VM, Magliarelli Hde F, Shcherbata HR. Stress and muscular dystrophy: a genetic screen for dystroglycan and dystrophin interactors in Drosophila identifies cellular stress response components. Dev Biol 2011, 352(2):228-242. 10.1016/j.ydbio.2011.01.013, 21256839.
19. Marrone AK, Kucherenko MM, Rishko VM, Shcherbata HR. New Dystrophin/Dystroglycan interactors control neuron behavior in Drosophila eye. BMC Neurosci 2011, 12:93. 10.1186/1471-2202-12-93, 3217851, 21943192.
20. Saleh AD, Savage JE, Cao L, Soule BP, Ly D, DeGraff W, Harris CC, Mitchell JB, Simone NL. Cellular stress induced alterations in microRNA let-7a and let-7b expression are dependent on p53. PLoS One 2011, 6(10):e24429. 10.1371/journal.pone.0024429, 3191136, 22022355.
21. Zhang X, Zabinsky R, Teng Y, Cui M, Han M. microRNAs play critical roles in the survival and recovery of Caenorhabditis elegans from starvation-induced L1 diapause. Proc Natl Acad Sci U S A 2011, 108(44):17997-18002. 10.1073/pnas.1105982108, 3207661, 22011579.
22. Greco S, De Simone M, Colussi C, Zaccagnini G, Fasanaro P, Pescatori M, Cardani R, Perbellini R, Isaia E, Sale P, et al. Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J 2009, 23(10):3335-3346. 10.1096/fj.08-128579, 19528256.
23. Marrone AK, Kucherenko MM, Wiek R, Gopfert MC, Shcherbata HR. Hyperthermic seizures and aberrant cellular homeostasis in Drosophila dystrophic muscles. Sci Rep 2011, 1:47. 3216534, 22355566.
24. Griffiths-Jones S. The microRNA Registry. Nucleic Acids Res 2004, 32(Database issue):109-111.
25. Mestdagh P, Feys T, Bernard N, Guenther S, Chen C, Speleman F, Vandesompele J. High-throughput stem-loop RT-qPCR miRNA expression profiling using minute amounts of input RNA. Nucleic Acids Res 2008, 36(21):e143. 10.1093/nar/gkn725, 2588502, 18940866.
26. Chen Y, Gelfond JA, McManus LM, Shireman PK. Reproducibility of quantitative RT-PCR array in miRNA expression profiling and comparison with microarray analysis. BMC Genomics 2009, 10:407. 10.1186/1471-2164-10-407, 2753550, 19715577.
27. Alessi A, Bragg AD, Percival JM, Yoo J, Albrecht DE, Froehner SC, Adams ME. gamma-Syntrophin scaffolding is spatially and functionally distinct from that of the alpha/beta syntrophins. 3095 2006, 312(16):3084.
28. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403(6772):901-906. 10.1038/35002607, 10706289.
29. Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75(5):855-862. 10.1016/0092-8674(93)90530-4, 8252622.
30. Ha I, Wightman B, Ruvkun G. A bulged lin-4/lin-14 RNA duplex is sufficient for Caenorhabditis elegans lin-14 temporal gradient formation. Genes Dev 1996, 10(23):3041-3050. 10.1101/gad.10.23.3041, 8957004.
31. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75(5):843-854. 10.1016/0092-8674(93)90529-Y, 8252621.
32. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 2007, 17(12):1850-1864. 10.1101/gr.6597907, 2099593, 17989254.
33. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008, 36(Database issue):149-153.
34. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G. GO:TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 2004, 20(18):3710-3715. 10.1093/bioinformatics/bth456, 3037731, 15297299.
35. Kucherenko MM, Pantoja M, Yatsenko AS, Shcherbata HR, Fischer KA, Maksymiv DV, Chernyk YI, Ruohola-Baker H. Genetic modifier screens reveal new components that interact with the Drosophila dystroglycan-dystrophin complex. PLoS One 2008, 3(6):e2418. 10.1371/journal.pone.0002418, 2398783, 18545683.
36. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116(2):281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
37. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008, 455(7209):64-71. 10.1038/nature07242, 2745094, 18668037.
38. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455(7209):58-63. 10.1038/nature07228, 18668040.
39. Dickson BJ, Gilestro GF. Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu Rev Cell Dev Biol 2006, 22:651-675. 10.1146/annurev.cellbio.21.090704.151234, 17029581.
40. Tayler TD, Robichaux MB, Garrity PA. Compartmentalization of visual centers in the Drosophila brain requires Slit and Robo proteins. Development 2004, 131(23):5935-5945. 10.1242/dev.01465, 1201521, 15525663.
41. Lo PC, Frasch M. bagpipe-Dependent expression of vimar, a novel Armadillo-repeats gene, in Drosophila visceral mesoderm. Mech Dev 1998, 72(1-2):65-75.
42. Chen J, Shi X, Padmanabhan R, Wang Q, Wu Z, Stevenson SC, Hild M, Garza D, Li H. Identification of novel modulators of mitochondrial function by a genome-wide RNAi screen in Drosophila melanogaster. Genome Res 2008, 18(1):123-136. 2134776, 18042644.
43. Biggar KK, Storey KB. The emerging roles of microRNAs in the molecular responses of metabolic rate depression. J Mol Cell Biol 2011, 3(3):167-175. 10.1093/jmcb/mjq045, 21177365.
44. Mirouse V, Christoforou CP, Fritsch C, St Johnston D, Ray RP. Dystroglycan and perlecan provide a basal cue required for epithelial polarity during energetic stress. Dev Cell 2009, 16(1):83-92. 10.1016/j.devcel.2008.11.006, 2789236, 19154720.
45. Xu XL, Li Y, Wang F, Gao FB. The steady-state level of the nervous-system-specific microRNA-124a is regulated by dFMR1 in Drosophila. J Neurosci 2008, 28(46):11883-11889. 10.1523/JNEUROSCI.4114-08.2008, 2605156, 19005053.
46. Ronshaugen M, Biemar F, Piel J, Levine M, Lai EC. The Drosophila microRNA iab-4 causes a dominant homeotic transformation of halteres to wings. Genes Dev 2005, 19(24):2947-2952. 10.1101/gad.1372505, 1315399, 16357215.
47. Ghahramani Seno MM, Trollet C, Athanasopoulos T, Graham IR, Hu P, Dickson G. Transcriptomic analysis of dystrophin RNAi knockdown reveals a central role for dystrophin in muscle differentiation and contractile apparatus organization. BMC Genomics 2010, 11:345. 10.1186/1471-2164-11-345, 2890566, 20515474.
48. Cherbas L, Lee K, Cherbas P. Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev 1991, 5(1):120-131. 10.1101/gad.5.1.120, 1899227.
49. Dobens L, Rudolph K, Berger EM. Ecdysterone regulatory elements function as both transcriptional activators and repressors. Mol Cell Biol 1991, 11(4):1846-1853. 359858, 2005885.
50. Nagai R, Hashimoto R, Yamaguchi M. Drosophila Syntrophins are involved in locomotion and regulation of synaptic morphology. Exp Cell Res 2010, 316(14):2313-2321. 10.1016/j.yexcr.2010.05.016, 20632467.
51. Jobgen WS, Fried SK, Fu WJ, Meininger CJ, Wu G. Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem 2006, 17(9):571-588. 10.1016/j.jnutbio.2005.12.001, 16524713.
52. Gao Y. The multiple actions of NO. Pflugers Arch 2010, 459(6):829-839. 10.1007/s00424-009-0773-9, 20024580.
53. Erusalimsky JD, Moncada S. Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 2007, 27(12):2524-2531. 10.1161/ATVBAHA.107.151167, 17885213.
54. Kuzin B, Roberts I, Peunova N, Enikolopov G. Nitric oxide regulates cell proliferation during Drosophila development. Cell 1996, 87(4):639-649. 10.1016/S0092-8674(00)81384-7, 8929533.
55. Regulski M, Tully T. Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase. Proc Natl Acad Sci U S A 1995, 92(20):9072-9076. 10.1073/pnas.92.20.9072, 40926, 7568075.
56. Cote PD, Moukhles H, Carbonetto S. Dystroglycan is not required for localization of dystrophin, syntrophin, and neuronal nitric-oxide synthase at the sarcolemma but regulates integrin alpha 7B expression and caveolin-3 distribution. J Biol Chem 2002, 277(7):4672-4679. 10.1074/jbc.M106879200, 11741881.
57. De Arcangelis V, Serra F, Cogoni C, Vivarelli E, Monaco L, Naro F. beta1-syntrophin modulation by miR-222 in mdx mice. PLoS One 2010, 5(8):12098.
58. Cacchiarelli D, Incitti T, Martone J, Cesana M, Cazzella V, Santini T, Sthandier O, Bozzoni I. miR-31 modulates dystrophin expression: new implications for Duchenne muscular dystrophy therapy. EMBO Rep 2011, 12(2):136-141. 10.1038/embor.2010.208, 3049433, 21212803.
59. Fuentes-Mera L, Rodriguez-Munoz R, Gonzalez-Ramirez R, Garcia-Sierra F, Gonzalez E, Mornet D, Cisneros B. Characterization of a novel Dp71 dystrophin-associated protein complex (DAPC) present in the nucleus of HeLa cells: members of the nuclear DAPC associate with the nuclear matrix. Exp Cell Res 2006, 312(16):3023-3035. 10.1016/j.yexcr.2006.06.002, 16824516.
60. Gonzalez-Ramirez R, Morales-Lazaro SL, Tapia-Ramirez V, Mornet D, Cisneros B. Nuclear and nuclear envelope localization of dystrophin Dp71 and dystrophin-associated proteins (DAPs) in the C2C12 muscle cells: DAPs nuclear localization is modulated during myogenesis. J Cell Biochem 2008, 105(3):735-745. 10.1002/jcb.21870, 18680104.
61. Christoforou CP, Greer CE, Challoner BR, Charizanos D, Ray RP. The detached locus encodes Drosophila Dystrophin, which acts with other components of the Dystrophin Associated Protein Complex to influence intercellular signalling in developing wing veins. Dev Biol 2008, 313(2):519-532. 10.1016/j.ydbio.2007.09.044, 18093579.
62. Fradkin LG, Baines RA, van der Plas MC, Noordermeer JN. The dystrophin Dp186 isoform regulates neurotransmitter release at a central synapse in Drosophila. J Neurosci 2008, 28(19):5105-5114. 10.1523/JNEUROSCI.4950-07.2008, 2408742, 18463264.
63. Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 2011, 6(7):e21800. 10.1371/journal.pone.0021800, 3138752, 21789182.
64. Kucherenko MM, Marrone AK, Rishko VM, Yatsenko AS, Klepzig A, Shcherbata HR. Paraffin-embedded and frozen sections of Drosophila adult muscles. J Vis Exp 2010, (46). pii: 2438..