A mechanism for ParB-dependent waves of ParA, a protein related to DNA segregation during cell division in prokaryotes

TY - JOUR

T1 - A mechanism for ParB-dependent waves of ParA, a protein related to DNA segregation during cell division in prokaryotes

AU - Hunding, Axel

AU - Gerdes, Kenn

AU - Charbon, Gitte Ebersbach

PY - 2003

Y1 - 2003

N2 - Prokaryotic plasmids encode partitioning (par) loci involved in segregation of DNA to daughter cells at cell division. A functional fusion protein consisting of Walker-type ParA ATPase and green fluorescent protein (Gfp) oscillates back and forth within nucleoid regions with a wave period of about 20 minutes. A model is discussed which is based on cooperative non-specific binding of ParA to the nucleoid, and local ParB initiated generation of ParA oligomer degradation products, which act autocatalytically on the degradation reaction. The model yields self-initiated spontaneous pattern formation, based on Turing's mechanism, and these patterns are destroyed by the degradation products, only to initiate a new pattern at the opposite nucleoid region. A recurrent wave thus emerges. This may be a particular example of a more general class of pattern forming mechanisms, based on protein oligomerization upon a template (membranes, DNA a.o.) with resulting enhanced NTPase function in the oligomer state, which may bring the oligomer into an unstable internal state. An effector initializes destabilization of the oligomer to yield degradation products, which act as seeds for further degradation in an autocatalytic process. We discuss this mechanism in relation to recent models for MinDE oscillations in E.coli and to microtubule degradation in mitosis. The study points to an ancestral role for the presented pattern types in generating bipolarity in prokaryotes and eukaryotes.

AB - Prokaryotic plasmids encode partitioning (par) loci involved in segregation of DNA to daughter cells at cell division. A functional fusion protein consisting of Walker-type ParA ATPase and green fluorescent protein (Gfp) oscillates back and forth within nucleoid regions with a wave period of about 20 minutes. A model is discussed which is based on cooperative non-specific binding of ParA to the nucleoid, and local ParB initiated generation of ParA oligomer degradation products, which act autocatalytically on the degradation reaction. The model yields self-initiated spontaneous pattern formation, based on Turing's mechanism, and these patterns are destroyed by the degradation products, only to initiate a new pattern at the opposite nucleoid region. A recurrent wave thus emerges. This may be a particular example of a more general class of pattern forming mechanisms, based on protein oligomerization upon a template (membranes, DNA a.o.) with resulting enhanced NTPase function in the oligomer state, which may bring the oligomer into an unstable internal state. An effector initializes destabilization of the oligomer to yield degradation products, which act as seeds for further degradation in an autocatalytic process. We discuss this mechanism in relation to recent models for MinDE oscillations in E.coli and to microtubule degradation in mitosis. The study points to an ancestral role for the presented pattern types in generating bipolarity in prokaryotes and eukaryotes.

KW - Adenosine Triphosphatases

KW - Adenosine Triphosphate

KW - Bacterial Proteins

KW - Binding Sites

KW - Cell Division

KW - Chromosome Segregation

KW - DNA, Bacterial

KW - Escherichia coli

KW - Gene Expression Regulation, Bacterial

KW - Green Fluorescent Proteins

KW - Guanosine Triphosphate

KW - Luminescent Proteins

KW - Microtubules

KW - Mitosis

KW - Models, Molecular

KW - Operator Regions, Genetic

KW - Plasmids

KW - Prokaryotic Cells

KW - Repressor Proteins

KW - Tubulin

M3 - Journal article

C2 - 12742016

SN - 0022-2836

VL - 329

SP - 35

EP - 43

JO - Journal of Molecular Biology

JF - Journal of Molecular Biology

IS - 1

ER -