A high-content, high-throughput siRNA screen identifies cyclin D2 as a potent regulator of muscle progenitor cell fusion and a target to enhance muscle regeneration

Human Molecular Genetics

Volumn 22, Issue 16, 2013, Pages 3283-3295

  Khanjyan, Michael V ^a   Yang, Jonathan ^a   Kayali, Refik ^a   Caldwell, Thomas ^a   Bertoni, Carmen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D2; CYCLIN DEPENDENT KINASE 4; DESMIN; DYSTROPHIN; MYOGENIN; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE IDENTIFICATION; GENE TARGETING; GENETIC LINKAGE; HIGH THROUGHPUT SCREENING; MOLECULAR INTERACTION; MOUSE; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SKELETAL MUSCLE; STEM CELL; STEM CELL TRANSPLANTATION;

ANIMALS; CELL FUSION; CELLS, CULTURED; CYCLIN D2; CYCLIN-DEPENDENT KINASE 4; MICE; MICE, TRANSGENIC; MUSCLE DEVELOPMENT; MUSCULAR DYSTROPHY, DUCHENNE; MYOBLASTS, SKELETAL; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; MYOGENIN; PROTEIN INTERACTION MAPPING; REGENERATION; RETINOBLASTOMA PROTEIN; RNA, SMALL INTERFERING;

EID: 84881262553     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt184     Document Type: Article

References (51)

1. Monaco, A.P., Neve, R.L., Colletti-Feener, C., Bertelson, C.J., Kurnit, D.M. and Kunkel, L.M. (1986) Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature, 323, 646-650.
2. Wehling-Henricks, M., Lee, J.J. and Tidball, J.G. (2004) Prednisolone decreases cellular adhesion molecules required for inflammatory cell infiltration in dystrophin-deficient skeletal muscle. Neuromuscul. Disord., 14, 483-490.
3. Shavlakadze, T., White, J., Hoh, J.F., Rosenthal, N. and Grounds, M.D. (2004) Targeted expression of insulin-like growth factor-I reduces early myofiber necrosis in dystrophic mdx mice. Mol. Ther., 10, 829-843.
4. Quinlan, J.G., Wong, B.L., Niemeier, R.T., McCullough, A.S., Levin, L. and Emanuele, M. (2006) Poloxamer 188 failed to prevent exercise-induced membrane breakdown in mdx skeletal muscle fibers. Neuromuscul. Disord., 16, 855-864.
5. Bogdanovich, S., Krag, T.O., Barton, E.R., Morris, L.D., Whittemore, L.A., Ahima, R.S. and Khurana, T.S. (2002) Functional improvement of dystrophic muscle by myostatin blockade. Nature, 420, 418-421.
6. Yasuda, S., Townsend, D., Michele, D.E., Favre, E.G., Day, S.M. and Metzger, J.M. (2005) Dystrophic heart failure blocked by membrane sealant poloxamer. Nature, 436, 1025-1029.
7. Ng, R., Metzger, J.M., Claflin, D.R. and Faulkner, J.A. (2008) Poloxamer 188 reduces the contraction-induced force decline in lumbrical muscles from mdx mice. Am. J. Physiol. Cell Physiol., 295, C146-C150.
8. Granchelli, J.A., Pollina, C. and Hudecki, M.S. (2000) Pre-clinical screening of drugs using the mdx mouse. Neuromuscul. Disord., 10, 235-239.
9. Rolland, J.F., De, L.A., Burdi, R., Andreetta, F., Confalonieri, P. and Conte, C.D. (2006) Overactivity of exercise-sensitive cation channels and their impaired modulation by IGF-1 in mdx native muscle fibers: beneficial effect of pentoxifylline. Neurobiol. Dis., 24, 466-474.
10. Gosselin, L.E. and Williams, J.E. (2006) Pentoxifylline fails to attenuate fibrosis in dystrophic (mdx) diaphragm muscle. Muscle Nerve, 33, 820-823.
11. Hawke, T.J. and Garry, D.J. (2001) Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol., 91, 534-551.
12. Conboy, M.J., Karasov, A.O. and Rando, T.A. (2007) High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS. Biol., 5, e102.
13. Charge, S.B. and Rudnicki, M.A. (2004) Cellular and molecular regulation of muscle regeneration. Physiol. Rev., 84, 209-238.
14. Gopinath, S.D. and Rando, T.A. (2008) Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell, 7, 590-598.
15. Dhawan, J. and Rando, T.A. (2005) Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol., 15, 666-673.
16. Moisset, P.A., Skuk, D., Asselin, I., Goulet, M., Roy, B., Karpati, G. and Tremblay, J.P. (1998) Successful transplantation of genetically corrected DMD myoblasts following ex vivo transduction with the dystrophin minigene. Biochem. Biophys. Res. Commun., 247, 94-99.
17. Gussoni, E., Blau, H.M. and Kunkel, L.M. (1997) The fate of individual myoblasts after transplantation into muscles of DMDpatients. Nat. Med., 3, 970-977.
18. Miller, R.G., Sharma, K.R., Pavlath, G.K., Gussoni, E., Mynhier, M., Lanctot, A.M., Greco, C.M., Steinman, L. and Blau, H.M. (1997) Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study. Muscle Nerve, 20, 469-478.
19. Wagner, K.R., McPherron, A.C., Winik, N. and Lee, S.J. (2002) Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann. Neurol., 52, 832-836.
20. McPherron, A.C. and Lee, S.J. (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl Acad. Sci. USA, 94, 12457-12461.
21. Schuelke, M., Wagner, K.R., Stolz, L.E., Hubner, C., Riebel, T., Komen, W., Braun, T., Tobin, J.F. and Lee, S.J. (2004) Myostatin mutation associated with gross muscle hypertrophy in a child. N. Engl. J. Med., 350, 2682-2688.
22. Benabdallah, B.F., Bouchentouf, M. and Tremblay, J.P. (2005) Improved success of myoblast transplantation in mdx mice by blocking the myostatin signal. Transplantation, 79, 1696-1702.
23. Magee, T.R., Artaza, J.N., Ferrini, M.G., Vernet, D., Zuniga, F.I., Cantini, L., Reisz-Porszasz, S., Rajfer, J. and Gonzalez-Cadavid, N.F. (2006) Myostatin short interfering hairpin RNA gene transfer increases skeletal muscle mass. J. Gene Med., 8, 1171-1181.
24. Dennis, G., Sherman, B., Hosack, D., Yang, J., Gao, W., Lane, H.C. and Lempicki, R. (2003) DAVID: database for annotation, visualization, and integrated discovery. Genome Biol., 4, 3.
25. Huang, D.W., Sherman, B.T. and Lempicki, R.A. (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
26. Rao, S.S. and Kohtz, D.S. (1995) Positive and negative regulation of D-type cyclin expression in skeletal myoblasts by basic fibroblast growth factor and transforming growth factor. J. Biol. Chem., 270, 4093-4100.
27. Rao, S.S., Chu, C. and Kohtz, D.S. (1994) Ectopic expression of cyclin D1 prevents activation of gene transcription by myogenic basic helix-loop- helix regulators. Mol. Cell. Biol., 14, 5259-5267.
28. Skapek, S.X., Rhee, J., Kim, P.S., Novitch, B.G. and Lassar, A.B. (1996) Cyclin-mediated inhibition of muscle gene expression via a mechanism that is independent of pRB hyperphosphorylation. Mol. Cell Biol., 16, 7043-7053.
29. Skapek, S.X., Rhee, J., Spicer, D.B. and Lassar, A.B. (1995) Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science, 267, 1022-1024.
30. Maley, M.A., Davies, M.J. and Grounds, M.D. (1995) Extracellular matrix, growth factors, genetics: their influence on cell proliferation and myotube formation in primary cultures of adult mouse skeletal muscle. Exp. Cell Res., 219, 169-179.
31. Puri, P.L. and Sartorelli, V. (2000) Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J. Cell Physiol., 185, 155-173.
32. Gu, W., Schneider, J.W., Condorelli, G., Kaushal, S., Mahdavi, V. and Nadal-Ginard, B. (1993) Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell, 72, 309-324.
33. Zacksenhaus, E., Jiang, Z., Chung, D., Marth, J.D., Phillips, R.A. and Gallie, B.L. (1996) pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev., 10, 3051-3064.
34. Puri, P.L., Iezzi, S., Stiegler, P., Chen, T.T., Schiltz, R.L., Muscat, G.E., Giordano, A., Kedes, L., Wang, J.Y. and Sartorelli, V. (2001) Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol. Cell, 8, 885-897.
35. Blais, A., van Oevelen, C.J., Margueron, R., Acosta-Alvear, D. and Dynlacht, B.D. (2007) Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit. J. Cell Biol., 179, 1399-1412.
36. Huh, M.S., Parker, M.H., Scime, A., Parks, R. and Rudnicki, M.A. (2004) Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation. J. Cell Biol., 166, 865-876.
37. Morgan, J.E., Hoffman, E.P. and Partridge, T.A. (1990) Normal myogenic cells from newborn mice restore normal histology to degenerating muscles of the mdx mouse. J. Cell Biol., 111, 2437-2449.
38. Bertoni, C., Morris, G.E. and Rando, T.A. (2005) Strand bias in oligonucleotide-mediated dystrophin gene editing. Hum. Mol. Genet., 14, 221-233.
39. Partridge, T.A., Morgan, J.E., Coulton, G.R., Hoffman, E.P. and Kunkel, L.M. (1989) Conversion of mdx myofibres from dystrophin-negative to - positive by injection of normal myoblasts. Nature, 337, 176-179.
40. Huard, J., Tremblay, G., Verreault, S., Labrecque, C. and Tremblay, J.P. (1993) Utilization of an antibody specific for human dystrophin to follow myoblast transplantation in nude mice. Cell Transplant., 2, 113-118.
41. Karpati, G., Pouliot, Y., Zubrzycka-Gaarn, E., Carpenter, S., Ray, P.N., Worton, R.G. and Holland, P. (1989) Dystrophin is expressed inmdxskeletal muscle fibers after normal myoblast implantation. Am. J. Pathol., 135, 27-32.
42. Gross, J.G., Bou-Gharios, G. and Morgan, J.E. (1999) Potentiation of myoblast transplantation by host muscle irradiation is dependent on the rate of radiation delivery. Cell Tissue Res., 298, 371-375.
43. Harris, J.B., Johnson, M.A. and Karlsson, E. (1974) Proceedings: histological and histochemical aspects of the effect of notexin on rat skeletal muscle. Br. J. Pharmacol., 52, 152P.
44. Huard, J., Acsadi, G., Jani, A., Massie, B. and Karpati, G. (1994) Gene transfer into skeletal muscles by isogenic myoblasts. Hum. Gene Ther., 5, 949-958.
45. Satoh, A., Huard, J., Labrecque, C. and Tremblay, J.P. (1993) Use of fluorescent latex microspheres (FLMs) to follow the fate of transplanted myoblasts. J. Histochem. Cytochem., 41, 1579-1582.
46. Bertoni, C., Rustagi, A. and Rando, T.A. (2009) Enhanced gene repair mediated by methyl-CpG-modified single-stranded oligonucleotides. Nucleic Acids Res., 37, 7468-7482.
47. Sacco, A., Siepi, F. and Crescenzi, M. (2003) HPV E7 expression in skeletal muscle cells distinguishes initiation of the postmitotic state from its maintenance. Oncogene, 22, 4027-4034.
48. Pfaffl, M.W. (2001) Anew mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, e45.
49. Bertoni, C. and Rando, T.A. (2002) Dystrophin gene repair in mdx muscle precursor cells in vitro and in vivo mediated by RNA-DNA chimeric oligonucleotides. Hum. Gene Ther., 13, 707-718.
50. Kayali, R., Bury, F., Ballard, M. and Bertoni, C. (2010) Site directed gene repair of the dystrophin gene mediated by PNA-ssODNs. Hum. Mol. Genet., 19, 3266-3281.
51. Briguet, A., Courdier-Fruh, I., Foster, M., Meier, T. and Magyar, J.P. (2004) Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromuscul. Disord., 14, 675-682.