Home LiteratureArticle Details
PMID: 20479129 Published · ppublish English Journal Article Research Support, N.I.H., Intramural

Ric-8A and Gi alpha recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle.

Molecular and cellular biology ·Vol. 30 ·No. 14 ·2010-07-00 ·Pages 3519-30

Woodard GE, Huang NN, Cho H, Miki T, Tall GG, Kehrl JH

Abstract

In model organisms, resistance to inhibitors of cholinesterase 8 (Ric-8), a G protein alpha (G alpha) subunit guanine nucleotide exchange factor (GEF), functions to orient mitotic spindles during asymmetric cell divisions; however, whether Ric-8A has any role in mammalian cell division is unknown. We show here that Ric-8A and G alpha(i) function to orient the metaphase mitotic spindle of mammalian adherent cells. During mitosis, Ric-8A localized at the cell cortex, spindle poles, centromeres, central spindle, and midbody. Pertussis toxin proved to be a useful tool in these studies since it blocked the binding of Ric-8A to G alpha(i), thus preventing its GEF activity for G alpha(i). Linking Ric-8A signaling to mammalian cell division, treatment of cells with pertussis toxin, reduction of Ric-8A expression, or decreased G alpha(i) expression similarly affected metaphase cells. Each treatment impaired the localization of LGN (GSPM2), NuMA (microtubule binding nuclear mitotic apparatus protein), and dynein at the metaphase cell cortex and disturbed integrin-dependent mitotic spindle orientation. Live cell imaging of HeLa cells expressing green fluorescent protein-tubulin also revealed that reduced Ric-8A expression prolonged mitosis, caused occasional mitotic arrest, and decreased mitotic spindle movements. These data indicate that Ric-8A signaling leads to assembly of a cortical signaling complex that functions to orient the mitotic spindle.

MeSH Terms
Animals Antigens, Nuclear/metabolism Base Sequence Cell Cycle Proteins Cell Division/physiology Cell Line Dogs Dyneins/metabolism GTP-Binding Protein alpha Subunits, Gi-Go/antagonists & inhibitors,genetics,metabolism Guanine Nucleotide Exchange Factors/antagonists & inhibitors,genetics,metabolism HeLa Cells Humans Interphase/physiology Intracellular Signaling Peptides and Proteins/metabolism Metaphase/physiology Nuclear Matrix-Associated Proteins/metabolism Pertussis Toxin/pharmacology Protein Binding/drug effects RNA, Small Interfering/genetics Signal Transduction Spindle Apparatus/drug effects,metabolism
Chemicals
Antigens, Nuclear Cell Cycle Proteins GPSM2 protein, human Guanine Nucleotide Exchange Factors Intracellular Signaling Peptides and Proteins NUMA1 protein, human Nuclear Matrix-Associated Proteins RNA, Small Interfering Pertussis Toxin Dyneins GTP-Binding Protein alpha Subunits, Gi-Go
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Woodard Geoffrey E
B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Disease, 10 Center Drive, MSC 1888, Bethesda, MD 20892-1752, USA.
Huang Ning-Na
Cho Hyeseon
Miki Toru
Tall Gregory G
Kehrl John H
References (39)
39 references, click to expand
  1. Spindle orientation during asymmetric cell division.
    Nat Cell Biol. 2009 Apr;11(4):365-74 PMID: 19337318
  2. Resistance to inhibitors of cholinesterase 8A catalyzes release of Galphai-GTP and nuclear mitotic apparatus protein (NuMA) from NuMA/LGN/Galphai-GDP complexes.
    Proc Natl Acad Sci U S A. 2005 Nov 15;102(46):16584-9 PMID: 16275912
  3. G proteins.
    Trends Biochem Sci. 1992 Oct;17(10):383-7 PMID: 1455506
  4. Dynamic microtubules lead the way for spindle positioning.
    Nat Rev Mol Cell Biol. 2004 Jun;5(6):481-92 PMID: 15173827
  5. A yeast actin-related protein homologous to that in vertebrate dynactin complex is important for spindle orientation and nuclear migration.
    Cell. 1994 Aug 26;78(4):669-79 PMID: 8069915
  6. Heterotrimeric G proteins: organizers of transmembrane signals.
    Cell. 1995 Jan 27;80(2):249-57 PMID: 7834744
  7. Integrin-mediated adhesion orients the spindle parallel to the substratum in an EB1- and myosin X-dependent manner.
    EMBO J. 2007 Mar 21;26(6):1487-98 PMID: 17318179
  8. Ric-8A catalyzes guanine nucleotide exchange on G alphai1 bound to the GPR/GoLoco exchange inhibitor AGS3.
    J Biol Chem. 2008 Aug 22;283(34):23150-60 PMID: 18541531
  9. LIM kinase-mediated cofilin phosphorylation during mitosis is required for precise spindle positioning.
    J Biol Chem. 2008 Feb 22;283(8):4983-92 PMID: 18079118
  10. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly.
    Cell. 1996 Nov 1;87(3):447-58 PMID: 8898198
  11. The GTP-binding protein G(ialpha) translocates to kinetochores and regulates the M-G(1) cell cycle transition of Swiss 3T3 cells.
    Cell Signal. 2000 Mar;12(3):153-63 PMID: 10704822
  12. A mammalian Partner of inscuteable binds NuMA and regulates mitotic spindle organization.
    Nat Cell Biol. 2001 Dec;3(12):1069-75 PMID: 11781568
  13. Control of embryonic spindle positioning and Galpha activity by C. elegans RIC-8.
    Curr Biol. 2004 Oct 26;14(20):1871-6 PMID: 15498497
  14. Special delivery: dynamic targeting via cortical capture of microtubules.
    Dev Cell. 2007 Mar;12(3):320-2 PMID: 17336896
  15. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division.
    Cell. 2008 Feb 8;132(3):474-86 PMID: 18267077
  16. Chromosomal passengers: conducting cell division.
    Nat Rev Mol Cell Biol. 2007 Oct;8(10):798-812 PMID: 17848966
  17. Mammalian Ric-8A (synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor.
    J Biol Chem. 2003 Mar 7;278(10):8356-62 PMID: 12509430
  18. Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells.
    Curr Biol. 1998 Apr 23;8(9):541-4 PMID: 9560347
  19. Dual role of Cdc42 in spindle orientation control of adherent cells.
    Mol Cell Biol. 2009 May;29(10):2816-27 PMID: 19273597
  20. Motor- and tail-dependent targeting of dynein to microtubule plus ends and the cell cortex.
    Curr Biol. 2009 Feb 10;19(3):196-205 PMID: 19185494
  21. PtdIns(3,4,5)P3 regulates spindle orientation in adherent cells.
    Dev Cell. 2007 Dec;13(6):796-811 PMID: 18061563
  22. Identification of a novel mitotic phosphorylation motif associated with protein localization to the mitotic apparatus.
    J Cell Sci. 2007 Nov 15;120(Pt 22):4060-70 PMID: 17971412
  23. RIC-8 is required for GPR-1/2-dependent Galpha function during asymmetric division of C. elegans embryos.
    Cell. 2004 Oct 15;119(2):219-30 PMID: 15479639
  24. Drosophila Ric-8 regulates Galphai cortical localization to promote Galphai-dependent planar orientation of the mitotic spindle during asymmetric cell division.
    Nat Cell Biol. 2005 Nov;7(11):1083-90 PMID: 16228010
  25. Ric-8 controls Drosophila neural progenitor asymmetric division by regulating heterotrimeric G proteins.
    Nat Cell Biol. 2005 Nov;7(11):1091-8 PMID: 16228012
  26. Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells.
    J Cell Biol. 1994 Sep;126(6):1509-26 PMID: 8089182
  27. Heterotrimeric G-proteins interact directly with cytoskeletal components to modify microtubule-dependent cellular processes.
    Neurosignals. 2009;17(1):100-8 PMID: 19212143
  28. The G-protein regulatory (GPR) motif-containing Leu-Gly-Asn-enriched protein (LGN) and Gialpha3 influence cortical positioning of the mitotic spindle poles at metaphase in symmetrically dividing mammalian cells.
    Eur J Cell Biol. 2006 Dec;85(12):1233-40 PMID: 17000024
  29. Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins.
    Cell. 2004 Nov 12;119(4):503-16 PMID: 15537540
  30. G protein betagamma subunits and AGS3 control spindle orientation and asymmetric cell fate of cerebral cortical progenitors.
    Cell. 2005 Jul 15;122(1):119-31 PMID: 16009138
  31. Drosophila Ric-8 is essential for plasma-membrane localization of heterotrimeric G proteins.
    Nat Cell Biol. 2005 Nov;7(11):1099-105 PMID: 16228011
  32. New roles for Galpha and RGS proteins: communication continues despite pulling sisters apart.
    Curr Biol. 2005 Oct 25;15(20):R843-54 PMID: 16243026
  33. Experimental and theoretical study of mitotic spindle orientation.
    Nature. 2007 May 24;447(7143):493-6 PMID: 17495931
  34. Coupling of cortical dynein and G alpha proteins mediates spindle positioning in Caenorhabditis elegans.
    Nat Cell Biol. 2007 Nov;9(11):1294-302 PMID: 17922003
  35. Cortical localization of the Galpha protein GPA-16 requires RIC-8 function during C. elegans asymmetric cell division.
    Development. 2005 Oct;132(20):4449-59 PMID: 16162648
  36. Targeted knockdown of G protein subunits selectively prevents receptor-mediated modulation of effectors and reveals complex changes in non-targeted signaling proteins.
    J Biol Chem. 2006 Apr 14;281(15):10250-62 PMID: 16446365
  37. Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts.
    Cell. 2005 Dec 29;123(7):1323-35 PMID: 16377571
  38. Lis1/dynactin regulates metaphase spindle orientation in Drosophila neuroblasts.
    Dev Biol. 2008 Jul 1;319(1):1-9 PMID: 18485341
  39. Galphai generates multiple Pins activation states to link cortical polarity and spindle orientation in Drosophila neuroblasts.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14306-11 PMID: 17726110
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
1098-5549
Published
2010-07-00
Epub
2010-00-17
Pages
3519-30
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC2897540
Subset
IM
Grants
NIGMS NIH HHS · R01 GM088242 · United States
Intramural NIH HHS · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com