Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin

TY - JOUR

T1 - Bacterial intermediate filaments

T2 - in vivo assembly, organization, and dynamics of crescentin

AU - Charbon, Godefroid

AU - Cabeen, Matthew T

AU - Jacobs-Wagner, Christine

PY - 2009/5/1

Y1 - 2009/5/1

N2 - Crescentin, which is the founding member of a rapidly growing family of bacterial cytoskeletal proteins, was previously proposed to resemble eukaryotic intermediate filament (IF) proteins based on structural prediction and in vitro polymerization properties. Here, we demonstrate that crescentin also shares in vivo properties of assembly and dynamics with IF proteins by forming stable filamentous structures that continuously incorporate subunits along their length and that grow in a nonpolar fashion. De novo assembly of crescentin is biphasic and involves a cell size-dependent mechanism that controls the length of the structure by favoring lateral insertion of crescentin subunits over bipolar longitudinal extension when the structure ends reach the cell poles. The crescentin structure is stably anchored to the cell envelope, and this cellular organization requires MreB function, identifying a new function for MreB and providing a parallel to the role of actin in IF assembly and organization in metazoan cells. Additionally, analysis of an MreB localization mutant suggests that cell wall insertion during cell elongation normally occurs along two helices of opposite handedness, each counterbalancing the other's torque.

AB - Crescentin, which is the founding member of a rapidly growing family of bacterial cytoskeletal proteins, was previously proposed to resemble eukaryotic intermediate filament (IF) proteins based on structural prediction and in vitro polymerization properties. Here, we demonstrate that crescentin also shares in vivo properties of assembly and dynamics with IF proteins by forming stable filamentous structures that continuously incorporate subunits along their length and that grow in a nonpolar fashion. De novo assembly of crescentin is biphasic and involves a cell size-dependent mechanism that controls the length of the structure by favoring lateral insertion of crescentin subunits over bipolar longitudinal extension when the structure ends reach the cell poles. The crescentin structure is stably anchored to the cell envelope, and this cellular organization requires MreB function, identifying a new function for MreB and providing a parallel to the role of actin in IF assembly and organization in metazoan cells. Additionally, analysis of an MreB localization mutant suggests that cell wall insertion during cell elongation normally occurs along two helices of opposite handedness, each counterbalancing the other's torque.

KW - Bacterial Proteins/chemistry

KW - Caulobacter crescentus/cytology

KW - Cell Cycle/physiology

KW - Chloramphenicol/pharmacology

KW - Cytoskeletal Proteins/chemistry

KW - Escherichia coli/genetics

KW - Escherichia coli Proteins/genetics

KW - Gene Expression Regulation, Bacterial/drug effects

KW - Intermediate Filaments/metabolism

KW - Mutation

KW - Protein Multimerization/drug effects

KW - Protein Synthesis Inhibitors/pharmacology

U2 - 10.1101/gad.1795509

DO - 10.1101/gad.1795509

M3 - Journal article

C2 - 19417107

SN - 0890-9369

VL - 23

SP - 1131

EP - 1144

JO - Genes & Development

JF - Genes & Development

IS - 9

ER -