WH2 and proline-rich domains of WASP-family proteins collaborate to accelerate actin filament elongation

Bieling, Peter; Hansen, Scott D.; Akin, Orkun; Li, Tai‐De; Hayden, Carl C.; Fletcher, Daniel A.; Mullins, R. Dyche

doi:10.15252/embj.201797039

Title: WH2 and proline-rich domains of WASP-family proteins collaborate to accelerate actin filament elongation

Journal Article · Thu Sep 28 00:00:00 EDT 2017 · EMBO Journal

DOI:https://doi.org/10.15252/embj.201797039· OSTI ID:1627930

^[1]; Hansen, Scott D. ^[2]; Akin, Orkun ^[2]; Li, Tai‐De ^[3]; Hayden, Carl C. ^[4];

^[3];

^[2]

Department of Cellular and Molecular Pharmacology and Howard Hughes Medical Institute University of California San Francisco CA USA; Department of Bioengineering &, Biophysics Program University of California Berkeley CA USA; Chan Zuckerberg Biohub San Francisco CA USA
Department of Cellular and Molecular Pharmacology and Howard Hughes Medical Institute University of California San Francisco CA USA
Department of Bioengineering &, Biophysics Program University of California Berkeley CA USA; Chan Zuckerberg Biohub San Francisco CA USA; Biological Systems &, Engineering Division Lawrence Berkeley National Laboratory Berkeley CA USA
Sandia National Laboratories Livermore CA USA

WASP-family proteins are known to promote assembly of branched actin networks by stimulating the filament-nucleating activity of the Arp2/3 complex. Here, we show that WASP-family proteins also function as polymerases that accelerate elongation of uncapped actin filaments. When clustered on a surface, WASP-family proteins can drive branched actin networks to grow much faster than they could by direct incorporation of soluble monomers. This polymerase activity arises from the coordinated action of two regulatory sequences: (i) a WASP homology 2 (WH2) domain that binds actin, and (ii) a proline-rich sequence that binds profilin–actin complexes. In the absence of profilin, WH2 domains are sufficient to accelerate filament elongation, but in the presence of profilin, proline-rich sequences are required to support polymerase activity by (i) bringing polymerization-competent actin monomers in proximity to growing filament ends, and (ii) promoting shuttling of actin monomers from profilin–actin complexes onto nearby WH2 domains. Unoccupied WH2 domains transiently associate with free filament ends, preventing their growth and dynamically tethering the branched actin network to the WASP-family proteins that create it. Collaboration between WH2 and proline-rich sequences thus strikes a balance between filament growth and tethering. Our work expands the number of critical roles that WASP-family proteins play in the assembly of branched actin networks to at least three: (i) promoting dendritic nucleation; (ii) linking actin networks to membranes; and (iii) accelerating filament elongation.

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Research Organization:: Lawrence Berkeley National Lab (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH); Howard Hughes Medical Institute; Human Frontier Science Program (HFSP); Taiwan National Science Council

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627930

Journal Information:: EMBO Journal, Vol. 37, Issue 1; ISSN 0261-4189

Publisher:: EMBO PressCopyright Statement

Country of Publication:: United States

Language:: English

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