Effect of myonuclear number and mitochondrial fusion on Drosophila indirect flight muscle organization and size

Experimental Cell Research

Volumn 319, Issue 17, 2013, Pages 2566-2577

  Rai, Mamta ^a   Nongthomba, Upendra ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Drosophila; Indirect flight muscles; Mitochondrial fusion; Muscle organization; Myoblast; Myonuclear number

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL FUSION; CONTROLLED STUDY; DROSOPHILA; FLIGHT MUSCLE; MITOCHONDRION; MUSCLE CELL; MUSCLE CHARACTERISTICS AND FUNCTIONS; MUSCLE DEVELOPMENT; MUSCLE FIBRIL; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE;

EID: 84885386551     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.06.021     Document Type: Article

References (63)

1. Pavlath G.K., Rich K., Webster S.G., Blau H.M. Localization of muscle gene products in nuclear domains. Nature 1989, 337:570-573.
2. Cheek D.B. The control of cell mass and replication. The DNA unit-a personal 20-year study. Early Hum. Dev. 1985, 12:211-239.
3. Hall Z.W., Ralston E. Nuclear domains in muscle cells. Cell 1989, 59:771-772.
4. Allen D.L., Roy R.R., Edgerton V.R. Myonuclear domains in muscle adaptation and disease. Muscle Nerve 1999, 22:1350-1360.
5. Patel K., Christ B., Stockdale F.E. Control of muscle size during embryonic, fetal and adult life. Vertebrate Myogenesis 2002, vol. 38:163-186. Springer-Verlag, Berlin Heidelberg.
6. Yan X., Zhu M.J., Dodson M.V., Du M. Developmental programming of fetal skeletal muscle and adipose tissue development. J. Genomics 2012, 1:29-38.
7. White R.B., Bierinx A.S., Gnocchi V.F., Zammit P.S. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev. Biol. 2010, 10:21.
8. Tajbakhsh S. Skeletal muscle stem cells in developmental versus regenerative myogenesis. J. Int. Med. 2009, 266:372-389.
9. Wigmore P.M., Evans D.J. Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis. Int. Rev. Cytol. 2002, 216:175-232.
10. Teixeira C., Duarte J. Myonuclear domain in skeletal muscle fibers. A critical review. Arch. Exercise Health Dis. 2011, 2:92-101.
11. Relaix F., Zammit P.S. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 2012, 139:2845-2856.
12. Dutta D., VijayRaghavan K. Metamorphosis and the formation of the adult musculature. Muscle Development in Drosophila 2006, 125-142. Landes Bioscience, USA. H. Sink (Ed.).
13. Vigoreaux J.O. Molecular basis of muscle structure. Muscle Development in Drosophila 2006, 143-156. Landes Bioscience, USA. H. Sink (Ed.).
14. Sink H. Muscle Development in Drosophila 2006, Landes Bioscience, USA.
15. Taylor M.V. Comparison of muscle development in Drosophila and vertebrates. Muscle Development in Drosophila 2006, 169-203. Landes Bioscience, USA. H. Sink (Ed.).
16. Fernandes J., Bate M., Vijayraghavan K. Development of the indirect flight muscles of Drosophila. Development 1991, 113:67-77.
17. Nongthomba U., Clark S., Cummins M., Ansari M., Stark M., Sparrow J.C. Troponin I is required for myofibrillogenesis and sarcomere formation in Drosophila flight muscle. J. Cell Sci. 2004, 117:1795-1805.
18. Reedy M.C., Beall C. Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Dev. Biol. 1993, 160:443-465.
19. Kelly D.P., Scarpulla R.C. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 2004, 18:357-368.
20. Scarpulla R.C. Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann. N.Y. Acad. Sci. 2008, 1147:321-334.
21. Virbasius J.V., Scarpulla R.C. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc. Nat. Acad. Sci. U.S.A. 1994, 91:1309-1313.
22. Chen H., Chan D.C. Physiological functions of mitochondrial fusion. Ann. N.Y. Acad. Sci. 2010, 1201:21-25.
23. Chen H., Vermulst M., Wang Y.E., Chomyn A., Prolla T.A., McCaffery J.M., Chan D.C. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010, 141:280-289.
24. Detmer S.A., Chan D.C. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 2007, 8:870-879.
25. Chan D.C. Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 2012, 46:265-287.
26. Hiona A., Sanz A., Kujoth G.C., Pamplona R., Seo A.Y., Hofer T., Someya S., Miyakawa T., Nakayama C., Samhan-Arias A.K., Servais S., Barger J.L., Portero-Otin M., Tanokura M., Prolla T.A., Leeuwenburgh C. Mitochondrial DNA mutations induce mitochondrial dysfunction, apoptosis and sarcopenia in skeletal muscle of mitochondrial DNA mutator mice. PLoS One 2010, 5:e11468.
27. Wagatsuma A., Sakuma K. Molecular mechanisms for age-associated mitochondrial deficiency in skeletal muscle. J. Aging Res. 2012, (2012):768304.
28. Wagatsuma A., Kotake N., Mabuchi K., Yamada S. Expression of nuclear-encoded genes involved in mitochondrial biogenesis and dynamics in experimentally denervated muscle. J. Physiol. Biochem. 2011, 67:359-370.
29. Sohal R.S. Aging changes in insect flight muscle. Gerontology 1976, 22:317-333.
30. Deng H., Dodson M.W., Huang H., Guo M. The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:14503-14508.
31. Anant S., Roy S., VijayRaghavan K. Twist and Notch negatively regulate adult muscle differentiation in Drosophila. Development 1998, 125:1361-1369.
32. Schnorrer F., Schonbauer C., Langer C.C., Dietzl G., Novatchkova M., Schernhuber K., Fellner M., Azaryan A., Radolf M., Stark A., Keleman K., Dickson B.J. Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 2010, 464:287-291.
33. Ranganayakulu G., Schulz R.A., Olson E.N. Wingless signaling induces nautilus expression in the ventral mesoderm of the Drosophila embryo. Dev. Biol. 1996, 176:143-148.
34. Luo L., Liao Y.J., Jan L.Y., Jan Y.N. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 1994, 8:1787-1802.
35. Pilling A.D., Horiuchi D., Lively C.M., Saxton W.M. Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol. Biol. Cell 2006, 17:2057-2068.
36. DeSimone S.M., White K. The Drosophila erect wing gene, which is important for both neuronal and muscle development, encodes a protein which is similar to the sea urchin P3A2 DNA binding protein. Mol. Cell Biol. 1993, 13:3641-3649.
37. Haussmann I.U., White K., Soller M. Erect wing regulates synaptic growth in Drosophila by integration of multiple signaling pathways. Genome Biol. 2008, 9:R73.
38. Drummond D.R., Hennessey E.S., Sparrow J.C. Characterisation of missense mutations in the Act88F gene of Drosophila melanogaster. Mol. Gen. Genet. 1991, 226:70-80.
39. Nongthomba U., Ramachandra N.B. A direct screen identifies new flight muscle mutants on the Drosophila second chromosome. Genetics 1999, 153:261-274.
40. Kronert W.A., O'Donnell P.T., Fieck A., Lawn A., Vigoreaux J.O., Sparrow J.C., Bernstein S.I. Defects in the Drosophila myosin rod permit sarcomere assembly but cause flight muscle degeneration. J. Mol. Biol. 1995, 249:111-125.
41. Clyne P.J., Brotman J.S., Sweeney S.T., Davis G. Green fluorescent protein tagging Drosophila proteins at their native genomic loci with small P elements. Genetics 2003, 165:1433-1441.
42. Orfanos Z., Sparrow J.C. Myosin isoform switching during assembly of the Drosophila flight muscle thick filament lattice. J. Cell Sci. 2012, 126:139-148.
43. Martini F.H., Timmons M.J., Tallitsch R.B. Human Anatomy 2008, 251-252. Benjamin Cummings.
44. DeSimone S., Coelho C., Roy S., VijayRaghavan K., White K., WING ERECT the Drosophila member of a family of DNA binding proteins is required in imaginal myoblasts for flight muscle development. Development 1996, 122:31-39.
45. Heller H., Gredinger E., Bengal E. Rac1 inhibits myogenic differentiation by preventing the complete withdrawal of myoblasts from the cell cycle. J. Biol. Chem. 2001, 276:37307-37316.
46. Fernandes J.J., Atreya K.B., Desai K.M., Hall R.E., Patel M.D., Desai A.A., Benham A.E., Mable J.L., Straessle J.L. A dominant negative form of Rac1 affects myogenesis of adult thoracic muscles in Drosophila. Dev. Biol. 2005, 285:11-27.
47. Roy S., VijayRaghavan K. Patterning muscles using organizers: larval muscle templates and adult myoblasts actively interact to pattern the dorsal longitudinal flight muscles of Drosophila. J. Cell Biol. 1998, 141:1135-1145.
48. Bate M. The embryonic development of larval muscles in Drosophila. Development 1990, 110:791-804.
49. Rushton E., Drysdale R., Abmayr S.M., Michelson A.M., Bate M. Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 1995, 121:1979-1988.
50. Dohrmann C., Azpiazu N., Frasch M. A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev. 1990, 4:2098-2111.
51. Bataille L., Delon I., Da Ponte J.P., Brown N.H., Jagla K. Downstream of identity genes: muscle-type-specific regulation of the fusion process. Dev. Cell 2010, 19:317-328.
52. Belu M., Mizutani C.M. Variation in mesoderm specification across Drosophilids is compensated by different rates of myoblast fusion during body wall musculature development. PLoS One 2011, 6:e28970.
53. McPherron A.C., Lee S.J. Double muscling in cattle due to mutations in the myostatin gene. Proc. Nat. Acad. Sci. U.S.A. 1997, 94:12457-12461.
54. Thomas M., Langley B., Berry C., Sharma M., Kirk S., Bass J., Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem. 2000, 275:40235-40243.
55. Joulia D., Bernardi H., Garandel V., Rabenoelina F., Vernus B., Cabello G. Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp. Cell Res. 2003, 286:263-275.
56. Nishi M., Yasue A., Nishimatu S., Nohno T., Yamaoka T., Itakura M., Moriyama K., Ohuchi H., Noji S. A missense mutant myostatin causes hyperplasia without hypertrophy in the mouse muscle. Biochem. Biophys. Res. Commun. 2002, 293:247-251.
57. Jaramillo M.S., Lovato C.V., Baca E.M., Cripps R.M. Crossveinless and the TGFbeta pathway regulate fiber number in the Drosophila adult jump muscle. Development 2009, 136:1105-1113.
58. Flanagan-Steet H., Hannon K., McAvoy M.J., Hullinger R., Olwin B.B. Loss of FGF receptor 1 signaling reduces skeletal muscle mass and disrupts myofiber organization in the developing limb. Dev. Biol. 2000, 218:21-37.
59. Horsley V., Friday B.B., Matteson S., Kegley K.M., Gephart J., Pavlath G.K. Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J. Cell Biol. 2001, 153:329-338.
60. Otto A., Macharia R., Matsakas A., Valasek P., Mankoo B.S., Patel K. A hypoplastic model of skeletal muscle development displaying reduced foetal myoblast cell numbers, increased oxidative myofibres and improved specific tension capacity. Dev. Biol. 2010, 343:51-62.
61. Amthor H., Macharia R., Navarrete R., Schuelke M., Brown S.C., Otto A., Voit T., Muntoni F., Vrbova G., Partridge T., Zammit P., Bunger L., Patel K. Lack of myostatin results in excessive muscle growth but impaired force generation. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:1835-1840.
62. Mendias C.L., Marcin J.E., Calerdon D.R., Faulkner J.A. Contractile properties of EDL and soleus muscles of myostatin-deficient mice. J. Appl. Physiol. 2006, 101:898-905.
63. De Palma C., Falcone S., Pisoni S., Cipolat S., Panzeri C., Pambianco S., Pisconti A., Allevi R., Bassi M.T., Cossu G., Pozzan T., Moncada S., Scorrano L., Brunelli S., Clementi E. Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation. Cell Death Differ. 2010, 17:1684-1696.