Leukemia-associated RhoGEF (LARG) is a novel RhoGEF in cytokinesis and required for the proper completion of abscission

Molecular Biology of the Cell

Volumn 24, Issue 18, 2013, Pages 2785-2794

  Martz, Matthew K ^a   Grabocka, Elda ^a,c   Beeharry, Neil ^b   Yen, Timothy J ^b   Wedegaertner, Philip B ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; AURORA B KINASE; LEUKEMIA ASSOCIATED RHOGEF; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL JUNCTION; CONTROLLED STUDY; CYTOKINESIS; HUMAN; HUMAN CELL; MICROTUBULE; PRIORITY JOURNAL; SPINDLE POLE BODY;

APOPTOSIS; AURORA KINASE B; CYTOKINESIS; HELA CELLS; HUMANS; KINETICS; MITOSIS; MUTATION; PROTEIN BINDING; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; STRUCTURE-ACTIVITY RELATIONSHIP; TYROSINE;

EID: 84884496386     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-07-0533     Document Type: Article

References (62)

1. Aittaleb M, Gao G, Evelyn CR, Neubig RR, Tesmer JJ (2009). A conserved hydrophobic surface of the LARG pleckstrin homology domain is critical for RhoA activation in cells. Cell Signal 21, 1569-1578.
2. Asiedu M, Wu D, Matsumura F, Wei Q (2009). Centrosome/spindle pole-associated protein regulates cytokinesis via promoting the recruitment of MyoGEF to the central spindle. Mol Biol Cell 20, 1428-1440.
3. Aurandt J, Vikis HG, Gutkind JS, Ahn N, Guan KL (2002). The semaphorin receptor plexin-B1 signals through a direct interaction with the Rho-specific nucleotide exchange factor, LARG. Proc Natl Acad Sci USA 99, 12085-12090.
4. Becknell B, Shen T, Maghraby E, Taya S, Kaibuchi K, Caligiuri MA, Marcucci G (2003). Characterization of leukemia-associated Rho guanine nucleotide exchange factor (LARG) expression during murine development. Cell Tissue Res 314, 361-366. (Pubitemid 37518636)
5. Bement WM, Benink HA, von Dassow G (2005). A microtubule-dependent zone of active RhoA during cleavage plane specification. J Cell Biol 170, 91-101. (Pubitemid 40994099)
6. Birkenfeld J (2007). GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev Cell 12, 699-712. (Pubitemid 46671149)
7. Birkenfeld J, Nalbant P, Bohl BP, Pertz O, Hahn KM, Bokoch GM (2007). GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev Cell 12, 699-712. (Pubitemid 46671149)
8. Chang YC, Nalbant P, Birkenfeld J, Chang ZF, Bokoch GM (2008). GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell 19, 2147-2153.
9. Dambournet D, Machicoane M, Chesneau L, Sachse M, Rocancourt M, El Marjou A, Formstecher E, Salomon R, Goud B, Echard A (2011). Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat Cell Biol 13, 981-988.
10. Di Leonardo A, Khan SH, Linke SP, Greco V, Seidita G, Wahl GM (1997). DNA rereplication in the presence of mitotic spindle inhibitors in human and mouse fibroblasts lacking either p53 or pRb function. Cancer Res 57, 1013-1019. (Pubitemid 27138591)
11. Dubash AD, Wennerberg K, Garcia-Mata R, Menold MM, Arthur WT, Burridge K (2007). A novel role for Lsc/p115 RhoGEF and LARG in regulating RhoA activity downstream of adhesion to fibronectin. J Cell Sci 120, 3989-3998. (Pubitemid 350269404)
12. Eggert US, Mitchison TJ, Field CM (2006). Animal cytokinesis: from parts list to mechanisms. Annu Rev Biochem 75, 543-566. (Pubitemid 44118043)
13. Elia N, Sougrat R, Spurlin TA, Hurley JH, Lippincott-Schwartz J (2011). Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci USA 108, 4846-4851.
14. Estey MP, Di Ciano-Oliveira C, Froese CD, Bejide MT, Trimble WS (2010). Distinct roles of septins in cytokinesis: SEPT9 mediates midbody abscission. J Cell Biol 191, 741-749.
15. Evelyn CR, Ferng T, Rojas RJ, Larsen MJ, Sondek J, Neubig RR (2009). High-throughput screening for small-molecule inhibitors of LARG-stimulated RhoA nucleotide binding via a novel fluorescence polarization assay. J Biomol Screen 14, 161-172.
16. Fededa JP, Gerlich DW (2012). Molecular control of animal cell cytokinesis. Nat Cell Biol 14, 440-447.
17. Fujishiro SH, Tanimura S, Mure S, Kashimoto Y, Watanabe K, Kohno M (2008). ERK1/2 phosphorylate GEF-H1 to enhance its guanine nucleotide exchange activity toward RhoA. Biochem Biophys Res Commun 368, 162-167.
18. Fujiwara T (2005). Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043-1047. (Pubitemid 41486987)
19. Fukuhara S, Chikumi H, Gutkind JS (2000). Leukemia-associated Rho guanine nucleotide exchange factor (LARG) links heterotrimeric G proteins of the G(12) family to Rho. FEBS Lett 485, 183-188.
20. Gai M, Camera P, Dema A, Bianchi F, Berto G, Scarpa E, Germena G, Di Cunto F (2011). Citron kinase controls abscission through RhoA and anillin. Mol Biol Cell 22, 3768-3778.
21. Garcia-Mata R, Wennerberg K, Arthur WT, Noren NK, Ellerbroek SM, Burridge K (2006). Analysis of activated GAPs and GEFs in cell lysates. Methods Enzymol 406, 425-437. (Pubitemid 43207456)
22. Goulimari P, Knieling H, Engel U, Grosse R (2008). LARG and mDia1 link Galpha12/13 to cell polarity and microtubule dynamics. Mol Biol Cell 19, 30-40. (Pubitemid 351186130)
23. Grabocka E, Wedegaertner PB (2007). Disruption of oligomerization induces nucleocytoplasmic shuttling of leukemia-associated Rho guanine-nucleotide exchange factor. Mol Pharmacol 72, 993-1002. (Pubitemid 47481422)
24. Gromley A (2005). Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123, 75-87. (Pubitemid 41414530)
25. Guilluy C, Swaminathan V, Garcia-Mata R, O'Brien ET, Superfine R, Burridge K (2011). The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat Cell Biol 13, 722-727.
26. Huang H-C, Shi J, Orth JD, Mitchison TJ (2009). Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly. Cancer Cell 16, 347-358.
27. Kanda T, Sullivan KF, Wahl GM (1998). Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr Biol 8, 377-385. (Pubitemid 28173996)
28. Kerr JF, Wyllie AH, Currie AR (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26, 239-257.
29. Kitzing TM, Sahadevan AS, Brandt DT, Knieling H, Hannemann S, Fackler OT, Grosshans J, Grosse R (2007). Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Genes Dev 21, 1478-1483. (Pubitemid 46955720)
30. Krendel M, Zenke FT, Bokoch GM (2002). Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 4, 294-301. (Pubitemid 34308855)
31. Kristelly R, Earnest BT, Krishnamoorthy L, Tesmer JJG (2003). Preliminary structure analysis of the DH/PH domains of leukemia-associated RhoGEF. Acta Crystallogr D 59, 1859-1862. (Pubitemid 37245152)
32. Loria A, Longhini KM, Glotzer M (2012). The RhoGAP domain of CYK-4 has an essential role in RhoA activation. Curr Biol 22, 213-219.
33. Mackay DR, Makise M, Ullman KS (2010). Defects in nuclear pore assembly lead to activation of an Aurora B-mediated abscission checkpoint. J Cell Biol 191, 923-931.
34. Matuliene J, Kuriyama R (2002). Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells. Mol Biol Cell 13, 1832-1845. (Pubitemid 34651475)
35. Medlin MD, Staus DP, Dubash AD, Taylor JM, Mack CP (2010). Sphingosine 1-phosphate receptor 2 signals through leukemia-associated RhoGEF (LARG), to promote smooth muscle cell differentiation. Arterioscler Thromb Vasc Biol 30, 1779-1786.
36. Mishima M, Kaitna S, Glotzer M (2002). Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2, 41-54. (Pubitemid 34065905)
37. Mullins J, Biesele J (1977). Terminal phase of cytokinesis in D-98S cells. J Cell Biol 73, 672-684. (Pubitemid 8115201)
38. Neto H, Gould GW (2011). The regulation of abscission by multi-protein complexes. J Cell Sci 124, 3199-3207.
39. Nishimura Y, Yonemura S (2006). Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J Cell Sci 119, 104-114. (Pubitemid 43169303)
40. Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, Barral Y (2006). The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 125, 85-98.
41. Perrot V, Vazquez-Prado J, Gutkind JS (2002). Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J Biol Chem 277, 43115-43120. (Pubitemid 35285695)
42. Petronczki M, Glotzer M, Kraut N, Peters JM (2007). Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. Dev Cell 12, 713-725. (Pubitemid 46667747)
43. Pfreimer M, Vatter P, Langer T, Wieland T, Gierschik P, Moepps B (2012). LARG links histamine-H1-receptor-activated Gq to Rho-GTPase-dependent signaling pathways. Cell Signal 24, 652-663.
44. Pohl C, Jentsch S (2008). Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 132, 832-845. (Pubitemid 351312799)
45. Rieder CL, Palazzo RE (1992). Colcemid and the mitotic cycle. J Cell Sci 102, (Pt 3), 387-392.
46. Shi Y, Zhang J, Mullin M, Dong B, Alberts AS, Siminovitch KA (2009). The mDial formin is required for neutrophil polarization, migration, and activation of the LARG/RhoA/ROCK signaling axis during chemotaxis. J Immunol 182, 3837-3845.
47. Slee EA, Adrain C, Martin SJ (2001). Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem 276, 7320-7326.
48. Steigemann P (2009). Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-484.
49. Steigemann P, Gerlich DW (2009). Cytokinetic abscission: cellular dynamics at the midbody. Trends Cell Biol 19, 606-616.
50. Steigemann P, Wurzenberger C, Schmitz MH, Held M, Guizetti J, Maar S, Gerlich DW (2009). Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-484.
51. Su K-C, Takaki T, Petronczki M (2011a). Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev Cell 21, 1104-1115.
52. Su KC, Takaki T, Petronczki M (2011b). Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev Cell 21, 1104-1115.
53. Suzuki N, Tokita R, Minami S (2007). Involvement of IGF-1/LARG signaling in the differentiation of neural stem cells into oligodendrocytes. J Nippon Med Sch 47, 3-2.
54. Swiercz JM, Kuner R, Behrens J, Offermanns S (2002). Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35, 51-63. (Pubitemid 34804322)
55. Tao W, South VJ, Zhang Y, Davide JP, Farrell L, Kohl NE, Sepp-Lorenzino L, Lobell RB (2005). Induction of apoptosis by an inhibitor of the mitotic kinesin KSP requires both activation of the spindle assembly checkpoint and mitotic slippage. Cancer Cell 8, 49-59. (Pubitemid 40991814)
56. Tatsumoto T, Xie X, Blumenthal R, Okamoto I, Miki T (1999). Human Ect2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J Cell Biol 147, 921-928.
57. Tomas A (2004). Annexin 11 is required for midbody formation and completion of the terminal phase of cytokinesis. J Cell Biol 165, 813-822. (Pubitemid 38821972)
58. Wolfe BA, Takaki T, Petronczki M, Glotzer M (2009). Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol 7, e1000110.
59. Wu D, Asiedu M, Adelstein RS, Wei Q (2006). A novel guanine nucleotide exchange factor MyoGEF is required for cytokinesis. Cell Cycle 5, 1234-1239. (Pubitemid 43845385)
60. Yang D (2008). Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat Struct Mol Biol 15, 1278-1286.
61. Yonemura S, Hirao-Minakuchi K, Nishimura Y (2004). Rho localization in cells and tissues. Exp Cell Res 295, 300-314. (Pubitemid 38490487)
62. Yüce O, Piekny A, Glotzer M (2005). An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 170, 571-582. (Pubitemid 41186932)