Loss of dystrophin and the microtubule-binding protein ELP-1 causes progressive paralysis and death of adult C. elegans

Developmental Dynamics

Volumn 238, Issue 8, 2008, Pages 1878-1886

  Hueston, Jennifer L ^a   Suprenant, Kathy A ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Cell adhesion; Cholinergic agents; Cytoskeleton; Muscle physiology; Muscular dystrophy

Indexed keywords

BINDING PROTEIN; DYSTROPHIN; DYTROPHIN LIKE PROTEIN 1; ENDOTHELIAL MONOCYTE ACTIVATING POLYPEPTIDE LIKE PROTEIN; RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE INTERACTION; MUSCLE CONTRACTION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

ACETYLCHOLINE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DYSTROPHIN; GENES, HELMINTH; GENES, LETHAL; MICROTUBULE-ASSOCIATED PROTEINS; MUSCLE CONTRACTION; MUSCULAR DYSTROPHY, ANIMAL; PHENOTYPE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TEMPERATURE;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 67650805460     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22007     Document Type: Article

References (56)

1. Anderson JL, Head SI, Rae C, Morley JW. 2002. Brain function in Duchenne muscular dystrophy. Brain 125:4-13.
2. Bessou C, Giugia JB, Franks CJ, Holden-Dye L, Segalat L. 1998. Mutations in the Caenorhabditis elegans dystrophin-like gene dys-1 lead to hyperactivity and suggest a link with cholinergic transmission. Neurogenetics 2:61-72.
3. Blake DJ, Kroger S. 2000. The neurobiology of duchenne muscular dystrophy: learning lessons from muscle? Trends Neurosci 23:92-99.
4. Bosher JM, Hahn BS, Legouis R, Sookhareea S, Weimer RM, Gansmuller A, Chisholm AD, Rose AM, Bessereau JL, Labouesse M. 2003. The Caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces. J Cell Biol 161:757-768.
5. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
6. Campbell KP. 1995. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80:675-679.
7. Carre-Pierrat M, Grisoni K, Gieseler K, Mariol MC, Martin E, Jospin M, Allard B, Segalat L. 2006. The SLO-1 BK channel of Caenorhabditis elegans is critical for muscle function and is involved in dystrophin-dependent muscle dystrophy. J Mol Biol 358:387-395.
8. Cerecedo D, Cisneros B, Suarez-Sanchez R, Hernandez-Gonzalez E, Galvan I. 2008. beta-Dystroglycan modulates the interplay between actin and microtubules in human-adhered platelets. Br J Haematol 141:517-528.
9. Ceron J, Rual JF, Chandra A, Dupuy D, Vidal M, van den Heuvel S. 2007. Largescale RNAi screens identify novel genes that interact with the C. elegans retinoblastoma pathway as well as splicingrelated components with synMuv B activity. BMC Dev Biol 7:30.
10. Chamberlain JS, Benian GM. 2000. Muscular dystrophy: the worm turns to genetic disease. Curr Biol 10:R795-797.
11. Costa M, Draper BW, Priess JR. 1997. The role of actin filaments in patterning the Caenorhabditis elegans cuticle. Dev Biol 184:373-384.
12. Cox EA, Hardin J. 2004. Sticky worms: adhesion complexes in C. elegans. J Cell Sci 117:1885-1897.
13. Culetto E, Baylis HA, Richmond JE, Jones AK, Fleming JT, Squire MD, Lewis JA, Sattelle DB. 2004. The Caenorhabditis elegans unc-63 gene encodes a levamisole-sensitive nicotinic acetylcholine receptor alpha subunit. J Biol Chem 279: 42476-42483.
14. De Keersmaecker K, Graux C, Odero MD, Mentens N, Somers R, Maertens J, Wlodarska I, Vandenberghe P, Hagemeijer A, Marynen P, Cools J. 2005. Fusion of EML1 to ABL1 in T-cell acute lymphoblastic leukemia with cryptic t(9;14)(q34; q32). Blood 105:4849-4852.
15. Duchenne D. 1868. Recherches sur la paralysie musculaire pseudo-hypertrophique, ou paralysie myosclerosique. Arch Gen Med 11:5-25.
16. Dupuy D, Bertin N, Hidalgo CA, Venkatesan K, Tu D, Lee D, Rosenberg J, Svrzikapa N, Blanc A, Carnec A, Carvunis AR, Pulak R, Shingles J, Reece-Hoyes J, Hunt-Newbury R, Viveiros R, Mohler WA, Tasan M, Roth FP, Le Peuch C, Hope IA, Johnsen R, Moerman DG, Barabasi AL, Baillie D, Vidal M. 2007. Genome-scale analysis of in vivo spatiotemporal promoter activity in Caenorhabditis elegans. Nat Biotechnol 25: 663-668.
17. Ehmsen J, Poon E, Davies K. 2002. The dystrophin-associated protein complex. J Cell Sci 115:2801-2803.
18. Eichenmuller B, Ahrens DP, Li Q, Suprenant KA. 2001. Saturable binding of the echinoderm microtubule-associated protein (EMAP) on microtubules, but not filamentous actin or vimentin filaments. Cell Motil Cytoskeleton 50:161-172.
19. Eichenmuller B, Everley P, Palange J, Lepley D, Suprenant KA. 2002. The human EMAP-like protein-70 (ELP70) is a microtubule destabilizer that localizes to the mitotic apparatus. J Biol Chem 277: 1301-1309.
20. Eudy JD, Ma-Edmonds M, Yao SF, Talmadge CB, Kelley PM, Weston MD, Kimberling WJ, Sumegi J. 1997. Isolation of a novel human homologue of the gene coding for echinoderm microtubule-associated protein (EMAP) from the Usher syndrome type 1a locus at 14q32. Genomics 43:104-106.
21. Fleming JT, Squire MD, Barnes TM, Tornoe C, Matsuda K, Ahnn J, Fire A, Sulston JE, Barnard EA, Sattelle DB, Lewis JA. 1997. Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J Neurosci 17:5843-5857.
22. Francis MM, Evans SP, Jensen M, Madsen DM, Mancuso J, Norman KR, Maricq AV. 2005. The Ror receptor tyrosine kinase CAM-1 is required for ACR-16-mediated synaptic transmission at the C. elegans neuromuscular junction. Neuron 46:581-594.
23. Gerber S, Bonneau D, Gilbert B, Munnich A, Dufier JL, Rozet JM, Kaplan J. 2006. USH1A: chronicle of a slow death. Am J Hum Genet 78:357-359.
24. Gieseler K, Bessou C, Segalat L. 1999. Dystrobrevin-and dystrophin-like mutants display similar phenotypes in the nematode Caenorhabditis elegans. Neurogenetics 2:87-90.
25. Gieseler K, Mariol MC, Bessou C, Migaud M, Franks CJ, Holden-Dye L, Segalat L. 2001. Molecular, genetic and physiological characterisation of dystrobrevin-like (dyb-1) mutants of Caenorhabditis elegans. J Mol Biol 307:107-117.
26. Gotta M, Ahringer J. 2001. Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat Cell Biol 3:297-300.
27. Gregory SL, Brown NH. 1998. kakapo, a gene required for adhesion between and within cell layers in Drosophila, encodes a large cytoskeletal linker protein related to plectin and dystrophin. J Cell Biol 143:1271-1282.
28. Grisoni K, Martin E, Gieseler K, Mariol MC, Segalat L. 2002. Genetic evidence for a dystrophin-glycoprotein complex (DGC) in Caenorhabditis elegans. Gene 294:77-86.
29. Grisoni K, Gieseler K, Mariol MC, Martin E, Carre-Pierrat M, Moulder G, Barstead R, Segalat L. 2003. The stn-1 syntrophin gene of C. elegans is functionally related to dystrophin and dystrobrevin. J Mol Biol 332:1037-1046.
30. Heidebrecht HJ, Buck F, Pollmann M, Siebert R, Parwaresch R. 2000. Cloning and localization of C2orf2(ropp120), a previously unknown WD repeat protein. Genomics 68:348-350.
31. Heydemann A, Doherty KR, McNally EM. 2007. Genetic modifiers of muscular dystrophy: implications for therapy. Biochim Biophys Acta 1772:216-228.
32. Huang C, Xiong C, Kornfeld K. 2004. Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans. Proc Natl Acad Sci USA 101:8084-8089.
33. Hueston JL, Purinton Herren G, Cueva JG, Buechner M, Lundquist EA, Goodman MB, Suprenant KA. 2008. The C. elegans EMAP-like protein, ELP-1 is required for normal touch sensation and associates with microtubules and adhesion complexes. BMC Dev Biol 8:110.
34. Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, Fang L, Halfnight E, Lee D, Lin J, Lorch A, McKay S, Okada HM, Pan J, Schulz AK, Tu D, Wong K, Zhao Z, Alexeyenko A, Burglin T, Sonnhammer E, Schnabel R, Jones SJ, Marra MA, Baillie DL, Moerman DG. 2007. High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 5:e237.
35. Johnson RP, Kang SH, Kramer JM. 2006. C. elegans dystroglycan DGN-1 functions in epithelia and neurons, but not muscle, and independently of dystrophin. Development 133:1911-1921.
36. Kim H, Rogers MJ, Richmond JE, McIntire SL. 2004. SNF-6 is an acetylcholine transporter interacting with the dystrophin complex in Caenorhabditis elegans. Nature 430:891-896.
37. Lecroisey C, Martin E, Mariol MC, Granger L, Schwab Y, Labouesse M, Segalat L, Gieseler K. 2008. DYC-1, a protein functionally linked to dystrophin in Caenorhabditis elegans is associated with the dense body, where it interacts with the muscle LIM domain protein ZYX-1. Mol Biol Cell 19:785-796.
38. Leung CL, Sun D, Zheng M, Knowles DR, Liem RK. 1999. Microtubule actin crosslinking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol 147:1275-1286.
39. Leung CL, Zheng M, Prater SM, Liem RK. 2001. The BPAG1 locus: Alternative splicing produces multiple isoforms with distinct cytoskeletal linker domains, including predominant isoforms in neurons and muscles. J Cell Biol 154:691-697.
40. Lewis JA, Wu CH, Berg H, Levine JH. 1980. The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 95:905-928.
41. Mariol MC, Segalat L. 2001. Muscular degeneration in the absence of dystrophin is a calcium-dependent process. Curr Biol 11:1691-1694.
42. Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, Rand JB. 1996. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA 93:12593-12598.
43. Paradis S, Ruvkun G. 1998. Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev 12:2488-2498.
44. Plenefisch JD, Zhu X, Hedgecock EM. 2000. Fragile skeletal muscle attachments in dystrophic mutants of Caenorhabditis elegans: isolation and characterization of the mua genes. Development 127:1197-1207.
45. Rand JB. 2007. Acetylcholine (January 30, 2007), WormBook, ed. The C. elegans Research Community, WormBook. [DOI: 10.1895/wormbook.1.131.1] http://www.wormbook.org.
46. Richmond JE, Jorgensen EM. 1999. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat Neurosci 2:791-797.
47. Robatzek M, Thomas JH. 2000. Calcium/calmodulin-dependent protein kinase II regulates Caenorhabditis elegans locomotion in concert with a G(o)/G(q) signaling network. Genetics 156:1069-1082.
48. Samuelson AV, Carr CE, Ruvkun G. 2007. Gene activities that mediate increased life span of C. elegans insulin-like signaling mutants. Genes Dev 21:2976-2994.
49. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S, Watanabe H, Kurashina K, Hatanaka H, Bando M, Ohno S, Ishikawa Y, Aburatani H, Niki T, Sohara Y, Sugiyama Y, Mano H. 2007. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 448:561-566.
50. Soda M, Takada S, Takeuchi K, Choi YL, Enomoto M, Ueno T, Haruta H, Hamada T, Yamashita Y, Ishikawa Y, Sugiyama Y, Mano H. 2008. A mouse model for EML4-ALK-positive lung cancer. Proc Natl Acad Sci USA 105:19893-19897.
51. Sonnenberg A, Liem RK. 2007. Plakins in development and disease. Exp Cell Res 313:2189-2203.
52. Suprenant KA, Dean K, McKee J, Hake S. 1993. EMAP, an echinoderm microtubule-associated protein found in microtubule-ribosome complexes. J Cell Sci 104:445-450.
53. Suprenant KA, Tuxhorn JA, Daggett MA, Ahrens DP, Hostetler A, Palange JM, VanWinkle CE, Livingston BT. 2000. Conservation of the WD-repeat, microtubule-binding protein, EMAP, in sea urchins, humans, and the nematode C. elegans. Dev Genes Evol 210:2-10.
54. Tegha-Dunghu J, Neumann B, Reber S, Krause R, Erfle H, Walter T, Held M, Rogers P, Hupfeld K, Ruppert T, Ellenberg J, Gruss OJ. 2008. EML3 is a nuclear microtubule-binding protein required for the correct alignment of chromosomes in metaphase. J Cell Sci 121:1718-1726.
55. Timmons L, Court DL, Fire A. 2001. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263:103-112.
56. Touroutine D, Fox RM, Von Stetina SE, Burdina A, Miller DM, 3rd, Richmond JE. 2005. acr-16 encodes an essential subunit of the levamisole-resistant nicotinic receptor at the Caenorhabditis elegans neuromuscular junction. J Biol Chem 280:27013-27021.