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Biol Open. 2021 Nov 15;10(11). doi: 10.1242/bio.058982. Epub 2021 Nov 02.

Interaction between Discs large and Pins/LGN/GPSM2: a comparison across species.

Biology open

Emily A Schiller, Dan T Bergstralh

Affiliations

  1. Department of Biology, University of Rochester, Rochester NY, 14627, USA.

PMID: 34596678 PMCID: PMC8576264 DOI: 10.1242/bio.058982

Abstract

The orientation of the mitotic spindle determines the direction of cell division, and therefore contributes to tissue shape and cell fate. Interaction between the multifunctional scaffolding protein Discs large (Dlg) and the canonical spindle orienting factor GPSM2 (called Pins in Drosophila and LGN in vertebrates) has been established in bilaterian models, but its function remains unclear. We used a phylogenetic approach to test whether the interaction is obligate in animals, and in particular whether Pins/LGN/GPSM2 evolved in multicellular organisms as a Dlg-binding protein. We show that Dlg diverged in C. elegans and the syncytial sponge Opsacas minuta and propose that this divergence may correspond with differences in spindle orientation requirements between these organisms and the canonical pathways described in bilaterians. We also demonstrate that Pins/LGN/GPSM2 is present in basal animals, but the established Dlg-interaction site cannot be found in either Placozoa or Porifera. Our results suggest that the interaction between Pins/LGN/GPSM2 and Dlg appeared in Cnidaria, and we therefore speculate that it may have evolved to promote accurate division orientation in the nervous system. This work reveals the evolutionary history of the Pins/LGN/GPSM2-Dlg interaction and suggests new possibilities for its importance in spindle orientation during epithelial and neural tissue development.

© 2021. Published by The Company of Biologists Ltd.

Keywords: Discs large; GPSM2; LGN; Pins; Spindle orientation

Conflict of interest statement

Competing interests The authors declare no competing or financial interests.

References

  1. Dev Biol. 2020 Sep 15;465(2):89-99 - PubMed
  2. Science. 2003 Jun 20;300(5627):1957-61 - PubMed
  3. Curr Biol. 2017 Nov 6;27(21):3350-3358.e3 - PubMed
  4. Development. 2002 Oct;129(19):4469-81 - PubMed
  5. Nature. 2014 Jun 5;510(7503):109-14 - PubMed
  6. Curr Biol. 2019 Mar 4;29(5):856-864.e3 - PubMed
  7. Curr Biol. 2010 Oct 26;20(20):1809-18 - PubMed
  8. Cell. 2005 Dec 29;123(7):1323-35 - PubMed
  9. Q Rev Biol. 1970 Dec;45(4):319-32 - PubMed
  10. BMC Evol Biol. 2007 Aug 02;7:129 - PubMed
  11. Dev Cell. 2006 Jun;10(6):731-42 - PubMed
  12. Cell Physiol Biochem. 2018;47(4):1509-1532 - PubMed
  13. Science. 2013 Dec 13;342(6164):1242592 - PubMed
  14. Structure. 2016 Nov 1;24(11):1876-1885 - PubMed
  15. Dev Cell. 2013 Aug 26;26(4):369-80 - PubMed
  16. Proc Natl Acad Sci U S A. 2011 Nov 1;108(44):E973-8 - PubMed
  17. Nat Cell Biol. 2009 Apr;11(4):365-74 - PubMed
  18. Curr Biol. 2020 Dec 21;30(24):5049-5057.e3 - PubMed
  19. Nat Cell Biol. 2000 Aug;2(8):531-9 - PubMed
  20. Int Rev Cytol. 1980;63:97-140 - PubMed
  21. Dev Biol. 1994 Feb;161(2):321-37 - PubMed
  22. Princess Takamatsu Symp. 1994;24:1-13 - PubMed
  23. Nature. 1999 Dec 2;402(6761):548-51 - PubMed
  24. J Mol Biol. 2000 Sep 8;302(1):205-17 - PubMed
  25. Genes Dev. 2003 May 15;17(10):1225-39 - PubMed
  26. EMBO J. 2011 Nov 25;30(24):4986-97 - PubMed
  27. J Cell Biol. 1996 Sep;134(6):1469-82 - PubMed
  28. Nat Struct Mol Biol. 2016 Feb;23(2):155-63 - PubMed
  29. Annu Rev Biochem. 2004;73:925-51 - PubMed
  30. Biochem J. 2005 Aug 15;390(Pt 1):293-302 - PubMed
  31. Am J Hum Genet. 2012 Jun 8;90(6):1088-93 - PubMed
  32. J Cell Biol. 2014 Sep 15;206(6):707-17 - PubMed
  33. Mol Cell. 2011 Aug 5;43(3):418-31 - PubMed
  34. Mol Cell Neurosci. 2007 Mar;34(3):431-44 - PubMed
  35. Biosystems. 2004 Aug-Oct;76(1-3):75-87 - PubMed
  36. EMBO Rep. 2017 Sep;18(9):1509-1520 - PubMed
  37. Proc Natl Acad Sci U S A. 2020 Jan 21;117(3):1496-1503 - PubMed
  38. J Mol Biol. 1999 Dec 17;294(5):1351-62 - PubMed
  39. J Biol Chem. 2000 May 5;275(18):13759-70 - PubMed
  40. Cell. 2009 Sep 18;138(6):1150-63 - PubMed
  41. Nat Commun. 2017 Jan 03;8:13996 - PubMed
  42. Development. 2016 Jul 15;143(14):2573-81 - PubMed
  43. Proc Natl Acad Sci U S A. 2011 Nov 29;108(48):19210-5 - PubMed
  44. PLoS One. 2015 Sep 23;10(9):e0138763 - PubMed
  45. Curr Biol. 2013 Sep 9;23(17):1707-12 - PubMed
  46. Trends Biochem Sci. 1998 Oct;23(10):403-5 - PubMed
  47. Nat Commun. 2021 Feb 26;12(1):1340 - PubMed
  48. Nat Cell Biol. 2005 Nov;7(11):1083-90 - PubMed
  49. PLoS One. 2012;7(4):e36014 - PubMed
  50. Cell. 2000 Feb 18;100(4):399-409 - PubMed
  51. J Cell Biol. 2010 May 3;189(3):481-95 - PubMed
  52. Nature. 2016 Feb 25;530(7591):495-8 - PubMed
  53. Mamm Genome. 2016 Feb;27(1-2):29-46 - PubMed
  54. Curr Biol. 2003 Jun 17;13(12):1029-37 - PubMed
  55. Bioinformatics. 2009 May 1;25(9):1189-91 - PubMed
  56. Cell Biochem Biophys. 2006;46(1):65-77 - PubMed
  57. Nature. 2013 Aug 15;500(7462):359-62 - PubMed
  58. Elife. 2016 Jan 07;5:e10147 - PubMed
  59. Nucleic Acids Res. 2019 Jul 2;47(W1):W636-W641 - PubMed
  60. Neuron. 2010 Aug 12;67(3):392-406 - PubMed
  61. Cell. 2001 Aug 10;106(3):355-66 - PubMed
  62. Int J Biochem Cell Biol. 2011 Jun;43(6):852-6 - PubMed
  63. J Cell Sci. 2016 Aug 15;129(16):3067-76 - PubMed
  64. Nat Cell Biol. 2007 Nov;9(11):1294-302 - PubMed
  65. Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 - PubMed
  66. Bioinformatics. 2007 May 1;23(9):1073-9 - PubMed
  67. J Cell Biol. 2012 Dec 24;199(7):1025-35 - PubMed
  68. Cell. 1993 Mar 26;72(6):971-83 - PubMed
  69. BMC Evol Biol. 2010 Apr 01;10:93 - PubMed
  70. BMC Cell Biol. 2010 Nov 02;11:85 - PubMed
  71. Science. 2020 Aug 14;369(6505):787-793 - PubMed
  72. Nucleic Acids Res. 2021 Jan 8;49(D1):D92-D96 - PubMed
  73. J Cell Biol. 2008 Jan 28;180(2):267-72 - PubMed

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