Loss of Drosophila A-type lamin C initially causes tendon abnormality including disintegration of cytoskeleton and nuclear lamina in muscular defects

Developmental Biology

Volumn 373, Issue 1, 2013, Pages 216-227

  Uchino, Ryo ^a   Nonaka, Yu Ki ^a   Horigome, Tuneyoshi ^a   Sugiyama, Shin ^b   Furukawa, Kazuhiro ^a  

^a NIIGATA UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

A type lamin; Cytoskeleton; Muscular dystrophy; Nuclear lamina; Tendon cells

Indexed keywords

CYTOSKELETON PROTEIN; LAMIN C; SHORTSTOP PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CYTOSKELETON; DROSOPHILA; EMERY DREIFUSS MUSCULAR DYSTROPHY; GENE LOSS; LETHALITY; METAMORPHOSIS; MUSCLE CELL; MUSCLE DISEASE; MUTANT; NONHUMAN; NUCLEAR LAMINA; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PUPA (LIFE CYCLE STAGE); SKELETAL MUSCLE; TENDON CELL; TENDON LESION;

EID: 84870058421     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.08.001     Document Type: Article

References (58)

1. Alves-Silva J., Hahn I., Huber O., Mende M., Reissaus A., Prokop A. Prominent actin fiber arrays in Drosophila tendon cells represent architectural elements different from stress fibers. Mol. Biol. Cell. 2008, 19:4287-4297.
2. Banos C.C., Thomas A.H., Kuo C.K. Collagen fibrillogenesis in tendon development: current models and regulation of fibril assembly. Birth Defects Res. C Embryo Today 2008, 84:228-244.
3. Bate M. The mesoderm and it derivatives. The Development of Drosophila melanogaster 1993, vol. II:1013-1090. CSHL Press, New York.
4. Bottenberg W., Sanchez-Soriano N., Alves-Silva.J., Hahn I., Mende M., Prokop A. Context-specific requirements of functional domains of the Spectraplakin Short stop in vivo. Mech. Dev. 2009, 126:489-502.
5. Boyer J.G., Bernstein M.A., Boudreau-Larivière C. Plakins in striated muscle. Muscle Nerve 2010, 41:299-308.
6. Dechat T., Adam S.A., Taimen P., Shimi T., Goldman R.D. Nuclear lamins. Cold Spring Harbor Perspect. Biol. 2010, 2:a000547.
7. Delon I., Brown N.H. Integrins and the actin cytoskeleton. Curr. Opin. Cell Biol. 2007, 19:43-50.
8. Dialynas G., Speese S., Budnik V., Geyer P.K., Wallrath L.L. The role of Drosophila Lamin C in muscle function and gene expression. Development 2010, 137:3067-3077.
9. Emery A.E.H. Emery-Dreifuss muscular dystrophy-a 40 year retrospective. Neuromuscular Disord. 2000, 10:228-232.
10. Fristrom J.W. Development of the morphological mutant cryptocephal of Drosophila melanogaster. Genetics 1965, 52:297-318.
11. Frommer G., Vorbrüggen G., Pasca G., Jäckle H., Volk T. Epidermal egr-like zinc finger protein of Drosophila participates in myotube guidance. EMBO J. 1996, 15:1642-1649.
12. Gurudatta B.V., Shashidhara L.S., Parnaik V.K. Lamin C and chromatin organization in Drosophila. J. Genet. 2010, 89:37-49.
13. Gnocchi V.F., Scharner J., Huang Z., Brady K., Lee J.S., White R.B., Morgan J.E., Sun Y.B., Ellis J.A., Zammit P.S. Uncoordinated transcription and compromised muscle function in the lmna-null mouse model of Emery-Dreifuss muscular dystrophy. PLoS One 2011, 6:e16651.
14. Grevengoed E.E., Peifer M. Cytoskeletal connections: building strong cells in new ways. Curr. Biol. 2003, 13:R568-R570.
15. Gruenbaum Y., Goldman R.D., Meyuhas R., Mills E., Margalit A., Fridkin A., Dayani Y., Prokocimer M., Enosh A. The nuclear lamina and its functions in the nucleus. Int. Rev. Cytol. 2003, 226:1-62.
16. Houben F., Ramaekers F.C., Snoeckx L.H., Broers J.L. Role of nuclear lamina-cytoskeleton interactions in the maintenance of cellular strength. Biochim. Biophys. Acta 2007, 1773:675-686.
17. Ippolito E., Natali P.G., Postacchini F., Accinni L., DeMartino C. Ultrastructural and immunochemical evidence of actin in the tendon cells. Clin. Orthop. Relat. Res. 1977, 126:282-284.
18. Ippolito E., Natali P.G., Postacchini F., Accinni L., DeMartino C. Morphological, immunochemical, and biochemical study of rabbit achilles tendon at various ages. J. Bone Jt. Surg. Am. 1980, 62:583-598.
19. Kannus P. Structure of the tendon connective tissue. Scand. J. Med. Sci. Sports 2000, 10:312-320.
20. Kracklauer M.P., Banks S.M., Xie X., Wu Y., Fischer J.A. Drosophila klaroid encodes a SUN domain protein required for Klarsicht localization to the nuclear envelope and nuclear migration in the eye. Fly 2007, 1:75-85.
21. Kracklauer M.P., Wiora H.M., Deery W.J., Chen X., Bolival B., Romanowicz D., Simonette R.A., Fuller M.T., Fischer J.A., Beckingham K.M. The Drosophila SUN protein Spag4 cooperates with the coiled-coil protein Yuri Gagarin to maintain association of the basal body and spermatid nucleus. J. Cell Sci. 2010, 123:2763-2772.
22. Krzemien J., Fabre C.C., Casal J., Lawrence P.A. The muscle pattern of the Drosophila abdomen depends on a subdivision of the anterior compartment of each segment. Development 2012, 139:75-83.
23. Lammerding J., Fong L.G., Ji J.Y., Reue K., Stewart C.L., Young S.G., Lee R.T. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 2006, 281:25768-25780.
24. Lee J.S., Hale C.M., Panorchan P., Khatau S.B., George J.P., Tseng Y., Stewart C.L., Hodzic D., Wirtz D. Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys. J. 2007, 93:2542-2552.
25. Maqbool T., Jagla K. Genetic control of muscle development: learning from Drosophila. J. Muscle Res. Cell Motil. 2007, 28:397-407.
26. Melcer S., Gruenbaum Y., Krohne G. Invertebrate lamins. Exp. Cell Res. 2007, 313:2157-2166.
27. Mittelbronn M., Sullivan T., Stewart C.L., Bornemann A. Myonuclear degeneration in LMNA null mice. Brain Pathol. 2008, 18:338-343.
28. Moir R.D., Spann T.P., Herrmann H., Goldman R.D. Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J. Cell Biol. 2000, 149:1179-1192.
29. Morin X., Daneman R., Zavortink M., Chia W. A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc. Natl. Acad. Sci. USA 2001, 98:15050-15055.
30. Mosley-Bishop K.L., Li Q., Patterson L., Fischer J.A. Molecular analysis of the Klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye. Curr. Biol. 1999, 9:1211-1220.
31. Postacchini F., Accinni L., Natali P.G., Ippolito E., DeMartino C. Regeneration of rabbit calcaneal tendon: a morphological and immunochemical study. Cell Tissue 1978, 195:81-97.
32. Rankin J., Ellard S. The laminopathies: a clinical review. Clin. Genet. 2006, 70:261-274.
33. Razafsky D., Hodzic D.A. Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J. Cell Biol. 2009, 186:461-472.
34. Riemer D., Stuurman N., Berrios M., Hunter C., Fisher P.A., Weber K. Expression of Drosophila lamin C is developmentally regulated: analogies with vertebrate A-type lamins. J. Cell Sci. 1995, 108:3189-3198.
35. Roux K.J., Burke B. Nuclear envelope defects in muscular dystrophy. Biochim. Biophys. Acta 2007, 1772:118-127.
36. Röper K., Gregory S.L., Brown N.H. The 'spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J. Cell Sci. 2002, 115:4215-4225.
37. Schäpe J., Prausse S., Radmacher M., Stick R. Influence of lamin A on the mechanical properties of amphibian oocyte nuclei measured by atomic force microscopy. Biophys. J. 2009, 96:4319-4325.
38. Schulze S.R., Curio-Penny B., Li Y., Imani R.A., Rydberg L., Geyer P.K., Wallrath L.L. Molecular genetic analysis of the nested Drosophila melanogaster lamin C gene. Genetics 2005, 71:185-196.
39. Schulze S.R., Curio-Penny B., Speese S., Dialynas G., Cryderman D.E., McDonough C.W., Nalbant D., Petersen M., Budnik V., Geyer P.K., Wallrath L.L. A comparative study of Drosophila and human A-type lamins. PLoS One 2009, 26:e7564.
40. Schweitzer R., Zelzer E., Volk T. Connecting muscles to tendons: tendons and musculoskeletal development in flies and vertebrates. Development 2010, 137:334-337.
41. Sonnenberg A., Liem R.K. Plakins in development and disease. Exp. Cell Res. 2007, 313:2189-2203.
42. Stuurman N., Delbecque J.P., Callaerts P., Aebi U. Ectopic overexpression of Drosophila lamin C is stage-specific lethal. Exp. Cell Res. 1999, 248:350-357.
43. Spann T.P., Moir R.D., Goldman A.E., Stick R., Goldman R.D. Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J. Cell Biol. 1997, 136:1201-1212.
44. Spann T.P., Goldman A.E., Wang C., Huang S., Goldman R.D. Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J. Cell Biol. 2002, 156:603-608.
45. Starr D.A., Han H. Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 2002, 298:406-409.
46. Strumpf D., Volk T. Kakapo, a novel cytoskeletal-associated protein is essential for the restricted localization of the neuregulin-like factor, vein, at the muscle-tendon junction site. J. Cell Biol. 1998, 143:1259-1270.
47. Subramanian A., Prokop A., Yamamoto M., Sugimura K., Uemura T., Betschinger J., Knoblich J.A., Volk T. Shortstop recruits EB1/APC1 and promotes microtubule assembly at the muscle-tendon junction. Curr. Biol. 2003, 13:1086-1095.
48. Sullivan T., Escalante-Alcalde D., Bhatt H., Anver M., Bhat N., Nagashima K., Stewart C.L., Burke B. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 1999, 147:913-920.
49. Technau M., Roth S. The Drosophila KASH domain proteins Msp-300 and Klarsicht and the SUN domain protein Klaroid have no essential function during oogenesis. Fly 2008, 2:82-91.
50. Volk T. A new member of the spectrin superfamily may participate in the formation of embryonic muscle attachments in Drosophila. Development 1992, 116:721-730.
51. Volk T. Singling out Drosophila tendon cells: a dialogue between two distinct cell types. Trends Genet. 1999, 15:448-453.
52. Wilson K.L., Foisner R. Lamin-binding proteins. Cold Spring Harbor Perspect. Biol. 2010, 2:a000554.
53. Worman H.J., Östlund C., Wang Y. Diseases of the nuclear envelope. Cold Spring Harbor Perspect. Biol. 2010, 2:a000760.
54. Xie X., Fischer J.A. On the roles of the Drosophila KASH domain proteins Msp-300 and Klarsicht. Fly 2008, 2:74-81.
55. Young K.G., Pool M., Kothary R. Bpag1 localization to actin filaments and to the nucleus is regulated by its N-terminus. J. Cell Sci. 2003, 116:4543-4555.
56. Young K.G., Kothary R. A Bpag1 isoform involved in cytoskeletal organization surrounding the nucleus. Exp. Cell Res. 2006, 312:121-134.
57. Young K.G., Kothary R. Dystonin/Bpag1 is a necessary endoplasmic reticulum/nuclear envelope protein in sensory neurons. Exp. Cell Res. 2008, 314:2750-2761.
58. Zaffran S., Astier M., Gratecos D., Sémériva 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.