Display options
Cite
Turkel N, Portela M, Poon C, et al. Cooperation of the BTB-Zinc finger protein, Abrupt, with cytoskeletal regulators in Drosophila epithelial tumorigenesis. Biol Open. 2015;4(8):1024-39doi: 10.1242/bio.012815.
Turkel, N., Portela, M., Poon, C., Li, J., Brumby, A. M., & Richardson, H. E. (2015). Cooperation of the BTB-Zinc finger protein, Abrupt, with cytoskeletal regulators in Drosophila epithelial tumorigenesis. Biology open, 4(8), 1024-39. https://doi.org/10.1242/bio.012815
Turkel, Nezaket, et al. "Cooperation of the BTB-Zinc finger protein, Abrupt, with cytoskeletal regulators in Drosophila epithelial tumorigenesis." Biology open vol. 4,8 (2015): 1024-39. doi: https://doi.org/10.1242/bio.012815
Turkel N, Portela M, Poon C, Li J, Brumby AM, Richardson HE. Cooperation of the BTB-Zinc finger protein, Abrupt, with cytoskeletal regulators in Drosophila epithelial tumorigenesis. Biol Open. 2015 Jul 17;4(8):1024-39. doi: 10.1242/bio.012815. PMID: 26187947; PMCID: PMC4542289.
Copy Download .nbib Format: NLM
Share it on

Biol Open. 2015 Jul 17;4(8):1024-39. doi: 10.1242/bio.012815.

Cooperation of the BTB-Zinc finger protein, Abrupt, with cytoskeletal regulators in Drosophila epithelial tumorigenesis.

Biology open

Nezaket Turkel, Marta Portela, Carole Poon, Jason Li, Anthony M Brumby, Helena E Richardson

Affiliations

  1. Cell Cycle and Development Laboratory, Peter MacCallum Cancer Centre, Melbourne, Victoria 3002, Australia.
  2. Bioinformatics Core Facility, Peter MacCallum Cancer Centre, Melbourne, Victoria 3002, Australia.
  3. Cell Cycle and Development Laboratory, Peter MacCallum Cancer Centre, Melbourne, Victoria 3002, Australia Sir Peter MacCallum Department of Oncology, Department of Anatomy and Neuroscience, Department of Biochemistry and Molecular Biology, University of Melbourne, Melbourne, Victoria 3010, Australia School of Molecular Sciences, La Trobe University, Melbourne, Victoria 3086, Australia [email protected].

PMID: 26187947 PMCID: PMC4542289 DOI: 10.1242/bio.012815

Abstract

The deregulation of cell polarity or cytoskeletal regulators is a common occurrence in human epithelial cancers. Moreover, there is accumulating evidence in human epithelial cancer that BTB-ZF genes, such as Bcl6 and ZBTB7A, are oncogenic. From our previous studies in the vinegar fly, Drosophila melanogaster, we have identified a cooperative interaction between a mutation in the apico-basal cell polarity regulator Scribble (Scrib) and overexpression of the BTB-ZF protein Abrupt (Ab). Herein, we show that co-expression of ab with actin cytoskeletal regulators, RhoGEF2 or Src64B, in the developing eye-antennal epithelial tissue results in the formation of overgrown amorphous tumours, whereas ab and DRac1 co-expression leads to non-cell autonomous overgrowth. Together with ab, these genes affect the expression of differentiation genes, resulting in tumours locked in a progenitor cell fate. Finally, we show that the expression of two mammalian genes related to ab, Bcl6 and ZBTB7A, which are oncogenes in mammalian epithelial cancers, significantly correlate with the upregulation of cytoskeletal genes or downregulation of apico-basal cell polarity neoplastic tumour suppressor genes in colorectal, lung and other human epithelial cancers. Altogether, this analysis has revealed that upregulation of cytoskeletal regulators cooperate with Abrupt in Drosophila epithelial tumorigenesis, and that high expression of human BTB-ZF genes, Bcl6 and ZBTB7A, shows significant correlations with cytoskeletal and cell polarity gene expression in specific epithelial tumour types. This highlights the need for further investigation of the cooperation between these genes in mammalian systems.

© 2015. Published by The Company of Biologists Ltd.

Keywords: Abrupt; Actin cytoskeletal regulators; Apico-basal cell polarity; BTB-ZF; Drosophila; Eye-antennal disc; Rac1; RhoGEF2; Scribble; Src

References

  1. EMBO J. 2014 Jul 1;33(13):1474-91 - PubMed
  2. Front Oral Biol. 2010;14:32-47 - PubMed
  3. J Clin Invest. 2011 Nov;121(11):4257-67 - PubMed
  4. BMC Dev Biol. 2011 Sep 29;11:57 - PubMed
  5. Nat Rev Cancer. 2013 Mar;13(3):172-83 - PubMed
  6. J Oncol. 2012;2012:752860 - PubMed
  7. Nat Rev Mol Cell Biol. 2012 Sep;13(9):591-600 - PubMed
  8. Genes Dev. 2014 Sep 1;28(17):1917-28 - PubMed
  9. Int J Cancer. 2008 Mar 15;122(6):1324-32 - PubMed
  10. Proc Natl Acad Sci U S A. 2012 Jan 10;109(2):484-9 - PubMed
  11. Am J Pathol. 2010 Jun;176(6):3007-14 - PubMed
  12. Nat Cell Biol. 2009 May;11(5):569-79 - PubMed
  13. Genes Dev. 1994 Aug 1;8(15):1787-802 - PubMed
  14. PLoS Genet. 2013;9(7):e1003627 - PubMed
  15. Acta Biochim Pol. 2009;56(2):225-34 - PubMed
  16. Breast Cancer Res. 2009;11(1):R7 - PubMed
  17. Genesis. 2011 Dec;49(12):912-8 - PubMed
  18. Asian Pac J Cancer Prev. 2013;14(9):4999-5005 - PubMed
  19. Curr Biol. 2006 Jun 6;16(11):1139-46 - PubMed
  20. Cancer Genet Cytogenet. 2004 Oct 1;154(1):27-35 - PubMed
  21. Oncogene. 2014 Apr 17;33(16):2027-39 - PubMed
  22. Oncogene. 2008 Nov 24;27(55):6888-907 - PubMed
  23. Mol Cell. 1998 May;1(6):831-40 - PubMed
  24. Dis Model Mech. 2013 May;6(3):661-78 - PubMed
  25. BMC Biol. 2009 Sep 24;7:62 - PubMed
  26. Development. 1998 Aug;125(15):2883-92 - PubMed
  27. EMBO J. 2011 May 10;30(12):2325-35 - PubMed
  28. Lung Cancer. 2008 Oct;62(1):113-9 - PubMed
  29. Mol Cell. 1998 May;1(6):819-29 - PubMed
  30. Biochem Biophys Res Commun. 2014 Jan 24;443(4):1226-31 - PubMed
  31. J Cell Biol. 2002 Feb 18;156(4):703-13 - PubMed
  32. Genes Dev. 1997 Sep 15;11(18):2295-322 - PubMed
  33. EMBO J. 2006 Nov 15;25(22):5294-304 - PubMed
  34. Genetics. 2011 May;188(1):105-25 - PubMed
  35. EMBO J. 2003 Nov 3;22(21):5769-79 - PubMed
  36. Nat Med. 2011 Apr;17 (4):500-3 - PubMed
  37. Am J Pathol. 2008 May;172(5):1363-80 - PubMed
  38. Mol Biol Cell. 2008 May;19(5):1883-92 - PubMed
  39. J Transl Med. 2008 Nov 07;6:69 - PubMed
  40. Curr Biol. 2004 Oct 26;14(20):1822-6 - PubMed
  41. Genes Dev. 1998 Jan 15;12(2):274-84 - PubMed
  42. PLoS Genet. 2014 May 22;10(5):e1004323 - PubMed
  43. Nature. 2012 Oct 25;490(7421):547-51 - PubMed
  44. Cancer Res. 2005 Oct 1;65(19):8575-8 - PubMed
  45. Oncogene. 2013 Sep 19;32(38):4471-9 - PubMed
  46. Cell. 1997 Dec 26;91(7):893-903 - PubMed
  47. Development. 1995 Mar;121(3):903-14 - PubMed
  48. Cell. 2011 Mar 4;144(5):646-74 - PubMed
  49. Genes Dev. 1995 Dec 1;9(23):2936-48 - PubMed
  50. Essays Biochem. 2012;53:141-68 - PubMed
  51. Genetics. 2007 Apr;175(4):1707-18 - PubMed
  52. PLoS One. 2013 Jul 17;8(7):e68981 - PubMed
  53. Development. 2013 Apr;140(7):1507-16 - PubMed
  54. Oncol Rep. 2014 Jan;31(1):103-10 - PubMed
  55. Oncogene. 2014 Nov 27;33(48):5523-33 - PubMed
  56. Development. 2006 Jul;133(14):2627-38 - PubMed
  57. Cancer Res. 2007 Nov 1;67(21):10163-72 - PubMed
  58. Annu Rev Cell Dev Biol. 1997;13:513-609 - PubMed
  59. Cell. 2014 Jul 3;158(1):143-56 - PubMed
  60. Int J Mol Sci. 2012;13(5):5818-31 - PubMed
  61. BMC Cancer. 2014 Jun 10;14:418 - PubMed
  62. Oncogene. 2004 Jun 10;23(27):4754-62 - PubMed
  63. Neuron. 1999 Mar;22(3):451-61 - PubMed
  64. Mol Cell Biol. 2004 Aug;24(15):6676-89 - PubMed
  65. Int J Dev Biol. 2009;53(8-10):1341-7 - PubMed
  66. Elife. 2015 Feb 26;4:null - PubMed
  67. Development. 1997 Jan;124(1):45-52 - PubMed
  68. Dev Growth Differ. 2011 Feb;53(2):168-76 - PubMed
  69. Cancer Cell. 2004 Jun;5(6):607-16 - PubMed
  70. PLoS One. 2010 Oct 01;5(10):null - PubMed
  71. Genes Dev. 1996 Jul 1;10(13):1645-56 - PubMed
  72. EMBO Rep. 2013 Jan;14(1):65-72 - PubMed
  73. Trends Cell Biol. 2006 Nov;16(11):578-87 - PubMed
  74. Cell Death Dis. 2013 Oct 17;4:e864 - PubMed
  75. Genes Dev. 1998 May 1;12(9):1290-303 - PubMed
  76. Proc Natl Acad Sci U S A. 2005 Sep 13;102(37):13123-8 - PubMed
  77. Oncogene. 2015 Feb 26;34(9):1073-82 - PubMed
  78. Dev Biol. 2006 Feb 15;290(2):435-46 - PubMed
  79. Neoplasia. 2004 Sep-Oct;6(5):611-22 - PubMed
  80. Cell. 1997 Dec 26;91(7):905-15 - PubMed
  81. Nature. 2000 Feb 10;403(6770):676-80 - PubMed
  82. Cancer Invest. 2010 Jul;28(6):672-8 - PubMed
  83. Dis Model Mech. 2013 Mar;6(2):521-9 - PubMed
  84. Cold Spring Harb Perspect Biol. 2012 Aug 01;4(8):a008797 - PubMed
  85. J Cell Sci. 2004 Mar 1;117(Pt 7):989-98 - PubMed
  86. Development. 2001 May;128(9):1519-29 - PubMed
  87. Nat Genet. 2007 Jan;39(1):41-51 - PubMed
  88. Nat Rev Cancer. 2005 Aug;5(8):626-39 - PubMed
  89. Dev Biol. 2007 Nov 1;311(1):106-23 - PubMed
  90. Brief Funct Genomic Proteomic. 2007 Mar;6(1):8-18 - PubMed
  91. J Biol Chem. 2008 Nov 28;283(48):33199-210 - PubMed
  92. Curr Biol. 2010 Apr 13;20(7):573-81 - PubMed
  93. Development. 2004 May;131(9):2113-24 - PubMed
  94. Dev Cell. 2013 Dec 9;27(5):530-44 - PubMed
  95. Exp Mol Pathol. 2010 Oct;89(2):140-8 - PubMed
  96. J Genet Genomics. 2011 Oct 20;38(10):431-8 - PubMed
  97. Trends Mol Med. 2014 Jun;20(6):343-52 - PubMed
  98. Cancer Res. 2007 Nov 1;67(21):10278-85 - PubMed
  99. Oncogene. 2015 Apr 30;34(18):2371-84 - PubMed
  100. Oncogene. 2008 Oct 9;27(46):5988-6001 - PubMed
  101. Development. 2009 Apr;136(7):1169-77 - PubMed
  102. J Cell Sci. 2013 Feb 15;126(Pt 4):927-38 - PubMed
  103. Development. 2011 Jun;138(11):2337-46 - PubMed
  104. Prog Mol Subcell Biol. 1999;22:201-29 - PubMed
  105. Annu Rev Cell Dev Biol. 2005;21:247-69 - PubMed
  106. Curr Biol. 2004 Oct 26;14(20):1827-33 - PubMed
  107. Dev Dyn. 2012 Jan;241(1):107-18 - PubMed
  108. Dev Dyn. 2005 Mar;232(3):673-84 - PubMed
  109. Exp Mol Pathol. 2011 Apr;90(2):226-30 - PubMed
  110. Genes Dev. 2002 Jul 1;16(13):1587-609 - PubMed
  111. J Cell Biol. 2005 Feb 14;168(4):575-85 - PubMed
  112. Dev Cell. 2006 Jan;10(1):33-44 - PubMed

Publication Types