The evolutionarily conserved RNA binding protein SMOOTH is essential for maintaining normal muscle function

Fly

Volumn 3, Issue 4, 2009, Pages 235-246

  Draper, Isabelle ^a   Tabaka, Meg E ^a   Jackson, F Rob ^b   Salomon, Robert N ^a   Kopin, Alan S ^a  

^a TUFTS MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila; HnRNP; Muscle physiology; RNA processing; Smooth; TDT

Indexed keywords

MAMMALIA;

EID: 85011940601     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.9517     Document Type: Article

References (64)

1. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNAbinding proteins and the messages they carry. Nat Rev Mol Cell Biol 2002; 3:195-205.
2. Wang Z, Burge CB. Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 2008; 14:802-813
3. Charroux B, Angelats C, Fasano L, Kerridge S, Vola C. The levels of the bancal product, a Drosophila homologue of vertebrate hnRNP K protein, affect cell proliferation and apoptosis in imaginal disc cells. Mol Cell Biol 1999; 19:7846-7856
4. Hartmuth K, Urlaub H, Vornlocher HP, Will CL, Gentzel M, Wilm M, Luhrmann R. Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc Natl Acad Sci USA 2002; 99:16719-16724
5. Jain RA, Gavis ER. The Drosophila hnRNP M homolog Rumpelstiltskin regulates nanos mRNA localization. Development 2008; 135:973-982
6. Kalifa Y, Huang T, Rosen LN, Chatterjee S, Gavis ER. Glorund, a Drosophila hnRNP F/H homolog, is an ovarian repressor of nanos translation. Dev Cell 2006; 10:291-301.
7. Lasko P. The Drosophila melanogaster genome: translation factors and RNA binding proteins. J Cell Biol 2000; 150:51-56
8. Matunis EL, Kelley R, Dreyfuss G. Essential role for a heterogeneous nuclear ribonucleoprotein (hnRNP) in oogenesis: hrp40 is absent from the germ line in the dorsoventral mutant squid. Proc Natl Acad Sci USA 1994; 91:2781-2784
9. Matunis EL, Matunis MJ, Dreyfuss G. Characterization of the major hnRNP proteins from Drosophila melanogaster. J Cell Biol 1992; 116:257-269
10. Mackay TF. Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics 1985; 111:351-374
11. zur Lage P, Shrimpton AD, Flavell AJ, Mackay TF, Brown AJ. Genetic and molecular analysis of smooth, a quantitative trait locus affecting bristle number in Drosophila melanogaster. Genetics 1997; 146:607-618
12. Layalle S, Coessens E, Ghysen A, Dambly-Chaudiere C. Smooth, a hnRNP encoding gene, controls axonal navigation in Drosophila. Genes Cells 2005; 10:119-125
13. Norga KK, Gurganus MC, Dilda CL, Yamamoto A, Lyman RF, Patel PH, et al. Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development. Curr Biol 2003; 13:1388-1396
14. Fan X, Messaed C, Dion P, Laganiere J, Brais B, Karpati G, Rouleau GA. HnRNP A1 and A/B interaction with PABPN1 in oculopharyngeal muscular dystrophy. Can J Neurol Sci 2003; 30:244-251
15. Kim DH, Langlois MA, Lee KB, Riggs AD, Puymirat J, Rossi JJ. HnRNP H inhibits nuclear export of mRNA containing expanded CUG repeats and a distal branch point sequence. Nucleic Acids Res 2005; 33:3866-3874
16. Zaffran S, Astier M, Gratecos D, Semeriva M. The held out wings (how) Drosophila gene encodes a putative RNA-binding protein involved in the control of muscular and cardiac activity. Development 1997; 124:2087-2098
17. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007; 448:151-156
18. Allikian MJ, Bhabha G, Dospoy P, Heydemann A, Ryder P, Earley JU, et al. Reduced life span with heart and muscle dysfunction in Drosophila sarcoglycan mutants. Hum Mol Genet 2007; 16:2933-2943
19. Karpen GH, Spradling AC. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics 1992; 132:737-753
20. O'Kane CJ, Gehring WJ. Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci USA 1987; 84:9123-9127
21. Kelso RJ, Buszczak M, Quinones AT, Castiblanco C, Mazzalupo S, Cooley L. Flytrap, a database documenting a GFP protein-trap insertion screen in Drosophila melanogaster. Nucleic Acids Res 2004; 32:418-420
22. Quinones-Coello AT, Petrella LN, Ayers K, Melillo A, Mazzalupo S, Hudson AM, et al. Exploring strategies for protein trapping in Drosophila. Genetics 2007; 175:1089-1104
23. Demerec M, ed. Biology of Drosophila. New York: Cold Spring Harbor Laboratory Press; John Wiley and Sons, Inc 1994.
24. Beall CJ, Fyrberg E. Muscle abnormalities in Drosophila melanogaster heldup mutants are caused by missing or aberrant troponin-I isoforms. J Cell Biol 1991; 114:941-951
25. Naimi B, Harrison A, Cummins M, Nongthomba U, Clark S, Canal I, et al. A tropomyosin-2 mutation suppresses a troponin I myopathy in Drosophila. Mol Biol Cell 2001; 12:1529-1539
26. Prado A, Canal I, Barbas JA, Molloy J, Ferrus A. Functional recovery of troponin I in a Drosophila heldup mutant after a second site mutation. Mol Biol Cell 1995; 6:1433-1441
27. Taghli-Lamallem O, Akasaka T, Hogg G, Nudel U, Yaffe D, Chamberlain JS, et al. Dystrophin deficiency in Drosophila reduces lifespan and causes a dilated cardiomyopathy phenotype. Aging Cell 2008; 7:237-249
28. van der Plas MC, Pilgram GS, de Jong AW, Bansraj MR, Fradkin LG, Noordermeer JN. Drosophila Dystrophin is required for integrity of the musculature. Mech Dev 2007; 124:617-630
29. Rajendra TK, Gonsalvez GB, Walker MP, Shpargel KB, Salz HK, Matera AG. A Drosophila melanogaster model of spinal muscular atrophy reveals a function for SMN in striated muscle. J Cell Biol 2007; 176:831-841
30. Chartier A, Benoit B, Simonelig M. A Drosophila model of oculopharyngeal muscular dystrophy reveals intrinsic toxicity of PABPN1. EMBO J 2006; 25:225362.
31. Shcherbata HR, Yatsenko AS, Patterson L, Sood VD, Nudel U, Yaffe D, et al. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J 2007; 26:481-493
32. Mahaffey JW, Coutu MD, Fyrberg EA, Inwood W. The flightless Drosophila mutant raised has two distinct genetic lesions affecting accumulation of myofibrillar proteins in flight muscles. Cell 1985; 40:101-110
33. Nongthomba U, Cummins M, Clark S, Vigoreaux JO, Sparrow JC. Suppression of muscle hypercontraction by mutations in the myosin heavy chain gene of Drosophila melanogaster. Genetics 2003; 164:209-222
34. Reedy MC, Bullard B, Vigoreaux JO. Flightin is essential for thick filament assembly and sarcomere stability in Drosophila flight muscles. J Cell Biol 2000; 151:1483-1500
35. Maughan DW, Vigoreaux JO. An Integrated View of Insect Flight Muscle: Genes, Motor Molecules and Motion. News Physiol Sci 1999; 14:87-92.
36. Zumstein N, Forman O, Nongthomba U, Sparrow JC, Elliott CJ. Distance and force production during jumping in wild-type and mutant Drosophila melanogaster. J Exp Biol 2004; 207:3515-3522
37. Courchesne-Smith CL, Tobin SL. Tissue-specific expression of the 79B actin gene during Drosophila development. Dev Biol 1989; 133:313-321
38. Deak II. A histochemical study of the muscles of Drosophila melanogaster. J Morphol 1977; 153:307-316
39. Hastings GA, Emerson CP Jr. Myosin functional domains encoded by alternative exons are expressed in specific thoracic muscles of Drosophila. J Cell Biol 1991; 114:263-276
40. Karlik CC, Coutu MD, Fyrberg EA. A nonsense mutation within the act88F actin gene disrupts myofibril formation in Drosophila indirect flight muscles. Cell 1984; 38:711-719
41. O'Donnell PT, Collier VL, Mogami K, Bernstein SI. Ultrastructural and molecular analyses of homozygousviable Drosophila melanogaster muscle mutants indicate there is a complex pattern of myosin heavy-chain isoform distribution. Genes Dev 1989; 3:1233-1246
42. Peckham M, Molloy JE, Sparrow JC, White DC. Physiological properties of the dorsal longitudinal flight muscle and the tergal depressor of the trochanter muscle of Drosophila melanogaster. J Muscle Res Cell Motil 1990; 11:203-215
43. Baehrecke EH. Who encodes a KH RNA binding protein that functions in muscle development. Development 1997; 124:1323-1332
44. Fyrberg C, Becker J, Barthmaier P, Mahaffey J, Fyrberg E. A Drosophila muscle-specific gene related to the mouse quaking locus. Gene 1997; 197:315-323
45. Volohonsky G, Edenfeld G, Klambt C, Volk T. Muscledependent maturation of tendon cells is induced by post-transcriptional regulation of stripeA. Development 2007; 134:347-356
46. Chen CD, Kobayashi R, Helfman DM. Binding of hnRNP H to an exonic splicing silencer is involved in the regulation of alternative splicing of the rat betatropomyosin gene. Genes Dev 1999; 13:593-606.
47. Crawford JB, Patton JG. Activation of alpha-tropomyosin exon 2 is regulated by the SR protein 9G8 and heterogeneous nuclear ribonucleoproteins H and F. Mol Cell Biol 2006; 26:8791-8802
48. Nasim MT, Chernova TK, Chowdhury HM, Yue BG, Eperon IC. HnRNP G and Tra2beta: opposite effects on splicing matched by antagonism in RNA binding. Hum Mol Genet 2003; 12:1337-1348
49. Paul S, Dansithong W, Kim D, Rossi J, Webster NJ, Comai L, Reddy S. Interaction of muscleblind, CUGBP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. EMBO J 2006; 25:4271-4283
50. Sink H, ed. Muscle Development in Drosophila. Georgetown, Texas; New York, New York: Landes Bioscience/Eurekah.com, Springer Science + Business Media, Inc 2006.
51. Bernstein SI, O'Donnell PT, Cripps RM. Molecular genetic analysis of muscle development, structure and function in Drosophila. Int Rev Cytol 1993; 143:63-152.
52. Siviter RJ, Coast GM, Winther AM, Nachman RJ, Taylor CA, Shirras AD, et al. Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A. J Biol Chem 2000; 275:23273-23280
53. Kaminski S, Orlowski E, Berry K, Nichols R. The effects of three Drosophila melanogaster myotropins on the frequency of foregut contractions differ. J Neurogenet 2002; 16:125-134
54. Palmer GC, Tran T, Duttlinger A, Nichols R. The drosulfakinin 0 (DSK 0) peptide encoded in the conserved Dsk gene affects adult Drosophila melanogaster crop contractions. J Insect Physiol 2007; 53:1125-1133
55. Pitsouli C, Perrimon N. Developmental biology: Our fly cousins' gut. Nature 2008; 454:592-593
56. Cheli Y, Kunicki TJ. hnRNP L regulates differences in expression of mouse integrin alpha2beta1. Blood 2006; 107:4391-4398
57. Hui J, Stangl K, Lane WS, Bindereif A. HnRNP L stimulates splicing of the eNOS gene by binding to variable-length CA repeats. Nat Struct Biol 2003; 10:33-37
58. Hung LH, Heiner M, Hui J, Schreiner S, Benes V, Bindereif A. Diverse roles of hnRNP L in mammalian mRNA processing: a combined microarray and RNAi analysis. RNA 2008; 14:284-296
59. Soderberg M, Raffalli-Mathieu F, Lang MA. Inflammation modulates the interaction of heterogeneous nuclear ribonucleoprotein (hnRNP) I/polypyrimidine tract binding protein and hnRNP L with the 3'untranslated region of the murine inducible nitric-oxide synthase mRNA. Mol Pharmacol 2002; 62:423-431
60. Draper I, Kurshan PT, McBride E, Jackson FR, Kopin AS. Locomotor activity is regulated by D2-like receptors in Drosophila: an anatomic and functional analysis. Dev Neurobiol 2007; 67:378-393
61. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, et al. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 2004; 36:283-287
62. Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, Tsang G, et al. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 2004; 167:761-781
63. Young SS, Sheldon BL. Correlated response in scutellar bristles to selection for abdominal bristles in Drosophila melanogaster. Genetics 1965; 52:287-295
64. Bridges CB, Brehme KS. The mutants of Drosophila. Carnegie Inst Wash Publ 1944; 522.