Abstract
Identification of small-molecule targets remains an important challenge for chemical genetics. We report an approach for target identification and protein discovery based on functional suppression of chemical inhibition in vitro. We discovered pirl1, an inhibitor of actin assembly, in a screen conducted with cytoplasmic extracts. Pirl1 was used to partially inhibit actin assembly in the same assay, and concentrated biochemical fractions of cytoplasmic extracts were added to find activities that suppressed pirl1 inhibition. Two activities were detected, separately purified, and identified as Arp2/3 complex and Cdc42/RhoGDI complex, both known regulators of actin assembly. We show that pirl1 directly inhibits activation of Cdc42/RhoGDI, but that Arp2/3 complex represents a downstream suppressor. This work introduces a general method for using low-micromolar chemical inhibitors to identify both inhibitor targets and other components of a signaling pathway.
MeSH Terms
Actin-Related Protein 2-3 Complex/antagonists & inhibitors
Actins/metabolism
Animals
Cell Surface Extensions/drug effects
Drug Evaluation, Preclinical/methods
Female
Guanine Nucleotide Dissociation Inhibitors/antagonists & inhibitors
In Vitro Techniques
Oocytes/drug effects,metabolism
Phosphatidylinositol 4,5-Diphosphate/metabolism
Signal Transduction/drug effects
Tetradecanoylphorbol Acetate/pharmacology
Xenopus laevis
cdc42 GTP-Binding Protein/antagonists & inhibitors
rho-Specific Guanine Nucleotide Dissociation Inhibitors
Chemicals
Actin-Related Protein 2-3 Complex
Actins
Guanine Nucleotide Dissociation Inhibitors
Phosphatidylinositol 4,5-Diphosphate
rho-Specific Guanine Nucleotide Dissociation Inhibitors
cdc42 GTP-Binding Protein
Tetradecanoylphorbol Acetate
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Peterson Jeffrey R
Division of Basic Sciences, Fox Chase Cancer Center, 333 Cottman Avenue, Philadelphia, Pennsylvania 19111, USA. jeffrey.peterson@fccc.edu
Lebensohn Andres M
Pelish Henry E
Kirschner Marc W
References (25)
25 references, click to expand
-
Ubistatins inhibit proteasome-dependent degradation by binding the ubiquitin chain.
Science. 2004 Oct 1;306(5693):117-20
PMID: 15459393
-
Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration.
Mol Biol Cell. 2000 Sep;11(9):2999-3012
PMID: 10982396
-
Identification of a novel protein regulating microtubule stability through a chemical approach.
Chem Biol. 2004 Jan;11(1):135-46
PMID: 15113003
-
Small molecules, big impact: a history of chemical inhibitors and the cytoskeleton.
Chem Biol. 2002 Dec;9(12):1275-85
PMID: 12498880
-
Requirements for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes.
J Exp Med. 1997 Nov 3;186(9):1487-94
PMID: 9348306
-
Target identification in chemical genetics: the (often) missing link.
Chem Biol. 2004 May;11(5):593-7
PMID: 15157870
-
Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases.
J Biol Chem. 1999 May 7;274(19):13198-204
PMID: 10224076
-
Multicopy suppressors for novel antibacterial compounds reveal targets and drug efflux susceptibility.
Chem Biol. 2004 Oct;11(10):1423-30
PMID: 15489169
-
Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex.
Cell. 2004 Jul 23;118(2):203-16
PMID: 15260990
-
The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro.
Methods Cell Biol. 1999;61:385-412
PMID: 9891325
-
Secramine inhibits Cdc42-dependent functions in cells and Cdc42 activation in vitro.
Nat Chem Biol. 2006 Jan;2(1):39-46
PMID: 16408091
-
A chemical inhibitor of N-WASP reveals a new mechanism for targeting protein interactions.
Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10624-9
PMID: 11553809
-
Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport.
Proc Natl Acad Sci U S A. 1988 Nov;85(21):7852-6
PMID: 3186695
-
The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly.
Cell. 1999 Apr 16;97(2):221-31
PMID: 10219243
-
Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex.
Biochem J. 2004 May 15;380(Pt 1):1-17
PMID: 15040784
-
Corequirement of specific phosphoinositides and small GTP-binding protein Cdc42 in inducing actin assembly in Xenopus egg extracts.
J Cell Biol. 1998 Mar 9;140(5):1125-36
PMID: 9490725
-
The role of Mg2+ cofactor in the guanine nucleotide exchange and GTP hydrolysis reactions of Rho family GTP-binding proteins.
J Biol Chem. 2000 Aug 18;275(33):25299-307
PMID: 10843989
-
Chemical genetics: ligand-based discovery of gene function.
Nat Rev Genet. 2000 Nov;1(2):116-25
PMID: 11253651
-
The small GTP-binding protein rac regulates growth factor-induced membrane ruffling.
Cell. 1992 Aug 7;70(3):401-10
PMID: 1643658
-
A genome-wide overexpression screen in yeast for small-molecule target identification.
Chem Biol. 2005 Jan;12(1):55-63
PMID: 15664515
-
GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors.
Nat Rev Mol Cell Biol. 2005 Feb;6(2):167-80
PMID: 15688002
-
Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI.
Cell. 2000 Feb 4;100(3):345-56
PMID: 10676816
-
Target identification strategies in chemical genetics.
Comb Chem High Throughput Screen. 2004 Nov;7(7):677-88
PMID: 15578930
-
Chemical inhibition of N-WASP by stabilization of a native autoinhibited conformation.
Nat Struct Mol Biol. 2004 Aug;11(8):747-55
PMID: 15235593
-
A crystallographic view of interactions between Dbs and Cdc42: PH domain-assisted guanine nucleotide exchange.
EMBO J. 2002 Mar 15;21(6):1315-26
PMID: 11889037