Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 2480375, 10 pages
https://doi.org/10.1155/2017/2480375
Review Article

An Examination of the Role of Transcriptional and Posttranscriptional Regulation in Rhabdomyosarcoma

1Stem Cell Institute, University of Minnesota Medical School, Minneapolis, MN 55455, USA
2Paul and Sheila Wellstone Muscular Dystrophy Center, University of Minnesota Medical School, Minneapolis, MN 55455, USA
3Department of Neurology, University of Minnesota Medical School, Minneapolis, MN 55455, USA

Correspondence should be addressed to Atsushi Asakura; ude.nmu@arukasa

Received 12 January 2017; Revised 1 April 2017; Accepted 18 April 2017; Published 30 May 2017

Academic Editor: Ninghui Cheng

Copyright © 2017 Alexander Hron and Atsushi Asakura. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. M. Wood, S. Etemad, M. Yamamoto, and D. J. Goldhamer, “MyoD-expressing progenitors are essential for skeletal myogenesis and satellite cell development,” Developmental Biology, vol. 384, no. 1, pp. 114–127, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Bernasconi, A. Remppis, W. J. Fredericks, F. J. Rauscher 3rd, and B. W. Schafer, “Induction of apoptosis in rhabdomyosarcoma cells through down-regulation of PAX proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 23, pp. 13164–13169, 1996. View at Google Scholar
  3. G. Merlino and L. J. Helman, “Rhabdomyosarcoma—working out the pathways,” Oncogene, vol. 18, no. 38, pp. 5340–5348, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. L. P. Lim, N. C. Lau, P. Garrett-Engele et al., “Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs,” Nature, vol. 433, no. 7027, pp. 769–773, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Wachtel and B. W. Schafer, “Unpeaceful roles of mutant PAX proteins in cancer,” Seminars in Cell & Developmental Biology, vol. 44, pp. 126–134, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Missiaglia, C. J. Shepherd, E. Aladowicz et al., “MicroRNA and gene co-expression networks characterize biological and clinical behavior of rhabdomyosarcomas,” Cancer Letters, vol. 385, pp. 251–260, 2016. View at Publisher · View at Google Scholar
  7. G. Haas, S. Cetin, M. Messmer et al., “Identification of factors involved in target RNA-directed microRNA degradation,” Nucleic Acids Research, vol. 44, no. 6, pp. 2873–2887, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. D. M. Loeb, K. Thornton, and O. Shokek, “Pediatric soft tissue sarcomas,” The Surgical Clinics of North America, vol. 88, no. 3, pp. 615–627, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. M. S. Merchant, D. Bernstein, M. Amoako et al., “Adjuvant immunotherapy to improve outcome in high-risk pediatric sarcomas,” Clinical Cancer Research, vol. 22, no. 13, pp. 3182–3191, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. E. C. Douglass, M. Valentine, E. Etcubanas et al., “A specific chromosomal abnormality in rhabdomyosarcoma,” Cytogenetics and Cell Genetics, vol. 45, no. 3-4, pp. 148–155, 1987. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Galili, R. J. Davis, W. J. Fredericks et al., “Fusion of a fork head domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma,” Nature Genetics, vol. 5, no. 3, pp. 230–235, 1993. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Dasgupta, J. Fuchs, and D. Rodeberg, “Rhabdomyosarcoma,” Seminars in Pediatric Surgery, vol. 25, no. 5, pp. 276–283, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Rohrbeck, J. N. Gong, E. F. Lee et al., “Hepatocyte growth factor renders BRAF mutant human melanoma cell lines resistant to PLX4032 by downregulating the pro-apoptotic BH3-only proteins PUMA and BIM,” Cell Death and Differentiation, vol. 23, no. 12, pp. 2054–2062, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Arnold and F. G. Barr, “Molecular diagnostics in the management of rhabdomyosarcoma,” Expert Review of Molecular Diagnostics, vol. 17, no. 2, pp. 189–194, 2017. View at Publisher · View at Google Scholar
  15. M. Buckingham, “Skeletal muscle formation in vertebrates,” Current Opinion in Genetics & Development, vol. 11, no. 4, pp. 440–448, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Hirai, M. Verma, S. Watanabe, C. Tastad, Y. Asakura, and A. Asakura, “MyoD regulates apoptosis of myoblasts through microRNA-mediated down-regulation of Pax3,” The Journal of Cell Biology, vol. 191, no. 2, pp. 347–365, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Seale, L. A. Sabourin, A. Girgis-Gabardo, A. Mansouri, P. Gruss, and M. A. Rudnicki, “Pax7 is required for the specification of myogenic satellite cells,” Cell, vol. 102, no. 6, pp. 777–786, 2000. View at Publisher · View at Google Scholar
  18. N. A. Dumont and M. A. Rudnicki, “Characterizing satellite cells and myogenic progenitors during skeletal muscle regeneration,” Methods in Molecular Biology, vol. 1560, pp. 179–188, 2017. View at Publisher · View at Google Scholar
  19. J. Khan, M. L. Bittner, L. H. Saal et al., “cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 23, pp. 13264–13269, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. J. M. Loupe, P. J. Miller, B. P. Bonner et al., “Comparative transcriptomic analysis reveals the oncogenic fusion protein PAX3-FOXO1 globally alters mRNA and miRNA to enhance myoblast invasion,” Oncogene, vol. 5, no. 7, p. e246, 2016. View at Publisher · View at Google Scholar
  21. M. E. Massari and C. Murre, “Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms,” Molecular and Cellular Biology, vol. 20, no. 2, pp. 429–440, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Murre, G. Bain, M. A. van Dijk et al., “Structure and function of helix-loop-helix proteins,” Biochimica et Biophysica Acta, vol. 1218, no. 2, pp. 129–135, 1994. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Gordân, N. Shen, I. Dror et al., “Genomic regions flanking E-box binding sites influence DNA binding specificity of bHLH transcription factors through DNA shape,” Cell Reports, vol. 3, no. 4, pp. 1093–1104, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Q. KL, Z. Yao, A. P. Fong et al., “Comparison of genome-wide binding of MyoD in normal human myogenic cells and rhabdomyosarcomas identifies regional and local suppression of promyogenic transcription factors,” Molecular and Cellular Biology, vol. 33, no. 4, pp. 773–784, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. Z. Yang, M. Q. KL, E. Analau et al., “MyoD and E-protein heterodimers switch rhabdomyosarcoma cells from an arrested myoblast phase to a differentiated state,” Genes & Development, vol. 23, no. 6, pp. 694–707, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. K. L. Macquarrie, Z. Yao, A. P. Fong, and S. J. Tapscott, “Genome-wide binding of the basic helix-loop-helix myogenic inhibitor musculin has substantial overlap with MyoD: implications for buffering activity,” Skeletal Muscle, vol. 3, no. 1, p. 26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. R. C. Lee, R. L. Feinbaum, and V. Ambros, “The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14,” Cell, vol. 75, no. 5, pp. 843–854, 1993. View at Publisher · View at Google Scholar · View at Scopus
  28. S. M. Elbashir, J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl, “Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells,” Nature, vol. 411, no. 6836, pp. 494–498, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. E. J. Kaufman and E. A. Miska, “The microRNAs of Caenorhabditis elegans,” Seminars in Cell & Developmental Biology, vol. 21, no. 7, pp. 728–737, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Lee, C. Ahn, J. Han et al., “The nuclear RNase III Drosha initiates microRNA processing,” Nature, vol. 425, no. 6956, pp. 415–419, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Sharma and D. Mohanty, “Sequence- and structure-based analysis of proteins involved in miRNA biogenesis,” Journal of Biomolecular Structure & Dynamics, pp. 1–13, 2017. View at Publisher · View at Google Scholar
  32. E. Lund and J. E. Dahlberg, “Substrate selectivity of exportin 5 and Dicer in the biogenesis of microRNAs,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 71, pp. 59–66, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. G. X. Zheng, B. T. Do, D. E. Webster, P. A. Khavari, and H. Y. Chang, “Dicer-microRNA-Myc circuit promotes transcription of hundreds of long noncoding RNAs,” Nature Structural & Molecular Biology, vol. 21, no. 7, pp. 585–590, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. A. J. Pratt and I. J. MacRae, “The RNA-induced silencing complex: a versatile gene-silencing machine,” The Journal of Biological Chemistry, vol. 284, no. 27, pp. 17897–17901, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Yan, X. D. Dong, X. Chen et al., “MicroRNA-1/206 targets c-Met and inhibits rhabdomyosarcoma development,” The Journal of Biological Chemistry, vol. 284, no. 43, pp. 29596–29604, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Rota, R. Ciarapica, A. Giordano, L. Miele, and F. Locatelli, “MicroRNAs in rhabdomyosarcoma: pathogenetic implications and translational potentiality,” Molecular Cancer, vol. 10, p. 120, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. C. F. Wong and R. L. Tellam, “MicroRNA-26a targets the histone methyltransferase enhancer of zeste homolog 2 during myogenesis,” The Journal of Biological Chemistry, vol. 283, no. 15, pp. 9836–9843, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. A. H. Juan, R. M. Kumar, J. G. Marx, R. A. Young, and V. Sartorelli, “Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells,” Molecular Cell, vol. 36, no. 1, pp. 61–74, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Caretti, M. Di Padova, B. Micales, G. E. Lyons, and V. Sartorelli, “The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation,” Genes & Development, vol. 18, no. 21, pp. 2627–2638, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. I. Marchesi, A. Giordano, and L. Bagella, “Roles of enhancer of zeste homolog 2: from skeletal muscle differentiation to rhabdomyosarcoma carcinogenesis,” Cell Cycle, vol. 13, no. 4, pp. 516–527, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Wang, R. Garzon, H. Sun et al., “NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma,” Cancer Cell, vol. 14, no. 5, pp. 369–381, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. I. Naguibneva, M. Ameyar-Zazoua, A. Polesskaya et al., “The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation,” Nature Cell Biology, vol. 8, no. 3, pp. 278–284, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Diao, X. Guo, L. Jiang et al., “miR-203, a tumor suppressor frequently down-regulated by promoter hypermethylation in rhabdomyosarcoma,” The Journal of Biological Chemistry, vol. 289, no. 1, pp. 529–539, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. H. J. Huang, J. Liu, H. Hua et al., “MiR-214 and N-ras regulatory loop suppresses rhabdomyosarcoma cell growth and xenograft tumorigenesis,” Oncotarget, vol. 5, no. 8, pp. 2161–2175, 2014. View at Publisher · View at Google Scholar
  45. F. Megiorni, S. Cialfi, M. D. HP et al., “Deep sequencing the microRNA profile in rhabdomyosarcoma reveals down-regulation of miR-378 family members,” BMC Cancer, vol. 14, p. 880, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. S. C. Boutet, M. H. Disatnik, L. S. Chan, K. Iori, and T. A. Rando, “Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors,” Cell, vol. 130, no. 2, pp. 349–362, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Gong, Y. K. Kim, C. F. Woeller, Y. Tang, and L. E. Maquat, “SMD and NMD are competitive pathways that contribute to myogenesis: effects on PAX3 and myogenin mRNAs,” Genes & Development, vol. 23, no. 1, pp. 54–66, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. C. G. Crist, D. Montarras, G. Pallafacchina et al., “Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 32, pp. 13383–13387, 2009. View at Google Scholar
  49. A. G. Borycki, J. Li, F. Jin, C. P. Emerson, and J. A. Epstein, “Pax3 functions in cell survival and in pax7 regulation,” Development, vol. 126, no. 8, pp. 1665–1674, 1999. View at Google Scholar
  50. L. Pani, M. Horal, and M. R. Loeken, “Rescue of neural tube defects in Pax-3-deficient embryos by p53 loss of function: implications for Pax-3-dependent development and tumorigenesis,” Genes & Development, vol. 16, no. 6, pp. 676–680, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. K. R. Degenhardt, R. C. Milewski, A. Padmanabhan et al., “Distinct enhancers at the Pax3 locus can function redundantly to regulate neural tube and neural crest expressions,” Developmental Biology, vol. 339, no. 2, pp. 519–527, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. C. M. Margue, M. Bernasconi, F. G. Barr, and B. W. Schafer, “Transcriptional modulation of the anti-apoptotic protein BCL-XL by the paired box transcription factors PAX3 and PAX3/FKHR,” Oncogene, vol. 19, no. 25, pp. 2921–2929, 2000. View at Publisher · View at Google Scholar
  53. H. G. Li, Q. Wang, H. M. Li et al., “PAX3 and PAX3-FKHR promote rhabdomyosarcoma cell survival through downregulation of PTEN,” Cancer Letters, vol. 253, no. 2, pp. 215–223, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Blake and M. R. Ziman, “Aberrant PAX3 and PAX7 expression. A link to the metastatic potential of embryonal rhabdomyosarcoma and cutaneous malignant melanoma?” Histology and Histopathology, vol. 18, no. 2, pp. 529–539, 2003. View at Publisher · View at Google Scholar
  55. E. J. Robson, S. J. He, and M. R. Eccles, “A PANorama of PAX genes in cancer and development,” Nature Reviews. Cancer, vol. 6, no. 1, pp. 52–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. Q. Wang, W. H. Fang, J. Krupinski, S. Kumar, M. Slevin, and P. Kumar, “Pax genes in embryogenesis and oncogenesis,” Journal of Cellular and Molecular Medicine, vol. 12, no. 6a, pp. 2281–2294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. S. J. He, G. Stevens, A. W. Braithwaite, and M. R. Eccles, “Transfection of melanoma cells with antisense PAX3 oligonucleotides additively complements cisplatin-induced cytotoxicity,” Molecular Cancer Therapeutics, vol. 4, no. 6, pp. 996–1003, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. W. H. Fang, Q. Wang, H. M. Li, M. Ahmed, P. Kumar, and S. Kumar, “PAX3 in neuroblastoma: oncogenic potential, chemosensitivity and signalling pathways,” Journal of Cellular and Molecular Medicine, vol. 18, no. 1, pp. 38–48, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. S. B. Charge and M. A. Rudnicki, “Cellular and molecular regulation of muscle regeneration,” Physiological Reviews, vol. 84, no. 1, pp. 209–238, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Asakura, M. Komaki, and M. Rudnicki, “Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation,” Differentiation, vol. 68, no. 4-5, pp. 245–253, 2001. View at Publisher · View at Google Scholar
  61. C. A. Collins, “Satellite cell self-renewal,” Current Opinion in Pharmacology, vol. 6, no. 3, pp. 301–306, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Sreenivasan, T. Braun, and J. Kim, “Systematic identification of genes regulating muscle stem cell self-renewal and differentiation,” Methods in Molecular Biology, vol. 1556, pp. 343–353, 2017. View at Publisher · View at Google Scholar
  63. A. Asakura, P. Seale, A. Girgis-Gabardo, and M. A. Rudnicki, “Myogenic specification of side population cells in skeletal muscle,” The Journal of Cell Biology, vol. 159, no. 1, pp. 123–134, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Montarras, J. Morgan, C. Collins et al., “Direct isolation of satellite cells for skeletal muscle regeneration,” Science, vol. 309, no. 5743, pp. 2064–2067, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Asakura, H. Hirai, B. Kablar et al., “Increased survival of muscle stem cells lacking the MyoD gene after transplantation into regenerating skeletal muscle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 42, pp. 16552–16557, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. Q. Yang, J. Yu, B. Yu et al., “PAX3+ skeletal muscle satellite cells retain long-term self-renewal and proliferation,” Muscle & Nerve, vol. 54, no. 5, pp. 943–951, 2016. View at Publisher · View at Google Scholar · View at Scopus
  67. S. C. Boutet, T. H. Cheung, N. L. Quach et al., “Alternative polyadenylation mediates microRNA regulation of muscle stem cell function,” Cell Stem Cell, vol. 10, no. 3, pp. 327–336, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. T. D. Barber, M. C. Barber, T. E. Cloutier, and T. B. Friedman, “PAX3 gene structure, alternative splicing and evolution,” Gene, vol. 237, no. 2, pp. 311–319, 1999. View at Publisher · View at Google Scholar · View at Scopus
  69. K. Goljanek-Whysall, D. Sweetman, M. Abu-Elmagd et al., “MicroRNA regulation of the paired-box transcription factor Pax3 confers robustness to developmental timing of myogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 29, pp. 11936–11941, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. L. Li, A. L. Sarver, S. Alamgir, and S. Subramanian, “Downregulation of microRNAs miR-1, -206 and -29 stabilizes PAX3 and CCND2 expression in rhabdomyosarcoma,” Laboratory Investigation, vol. 92, no. 4, pp. 571–583, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. F. B. Ruymann and A. C. Grovas, “Progress in the diagnosis and treatment of rhabdomyosarcoma and related soft tissue sarcomas,” Cancer Investigation, vol. 18, no. 3, pp. 223–241, 2000. View at Google Scholar
  72. D. Walterhouse and A. Watson, “Optimal management strategies for rhabdomyosarcoma in children,” Paediatric Drugs, vol. 9, no. 6, pp. 391–400, 2007. View at Google Scholar
  73. D. El Demellawy, J. McGowan-Jordan, J. de Nanassy, E. Chernetsova, and A. Nasr, “Update on molecular findings in rhabdomyosarcoma,” Pathology, vol. 49, no. 3, pp. 238–246, 2017. View at Publisher · View at Google Scholar
  74. A. S. Pappo, D. N. Shapiro, W. M. Crist, and H. M. Maurer, “Biology and therapy of pediatric rhabdomyosarcoma,” Journal of Clinical Oncology, vol. 13, no. 8, pp. 2123–2139, 1995. View at Publisher · View at Google Scholar
  75. R. Taulli, F. Bersani, V. Foglizzo et al., “The muscle-specific microRNA miR-206 blocks human rhabdomyosarcoma growth in xenotransplanted mice by promoting myogenic differentiation,” The Journal of Clinical Investigation, vol. 119, no. 8, pp. 2366–2378, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. R. Ciarapica, G. Russo, F. Verginelli et al., “Deregulated expression of miR-26a and Ezh2 in rhabdomyosarcoma,” Cell Cycle, vol. 8, no. 1, pp. 172–175, 2009. View at Publisher · View at Google Scholar
  77. M. Kozakowska, M. Ciesla, A. Stefanska et al., “Heme oxygenase-1 inhibits myoblast differentiation by targeting myomirs,” Antioxidants & Redox Signaling, vol. 16, no. 2, pp. 113–127, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. M. M. Sun, J. F. Li, L. L. Guo et al., “TGF-beta1 suppression of microRNA-450b-5p expression: a novel mechanism for blocking myogenic differentiation of rhabdomyosarcoma,” Oncogene, vol. 33, no. 16, pp. 2075–2086, 2014. View at Publisher · View at Google Scholar · View at Scopus
  79. C. F. Chen, X. He, A. D. Arslan et al., “Novel regulation of nuclear factor-YB by miR-485-3p affects the expression of DNA topoisomerase IIα and drug responsiveness,” Molecular Pharmacology, vol. 79, no. 4, pp. 735–741, 2011. View at Publisher · View at Google Scholar · View at Scopus