Literature DB >> 31596235

Length regulation of multiple flagella that self-assemble from a shared pool of components.

Thomas G Fai1, Lishibanya Mohapatra2, Prathitha Kar3, Jane Kondev2, Ariel Amir3.   

Abstract

The single-celled green algae Chlamydomonas reinhardtii with its two flagella-microtubule-based structures of equal and constant lengths-is the canonical model organism for studying size control of organelles. Experiments have identified motor-driven transport of tubulin to the flagella tips as a key component of their length control. Here we consider a class of models whose key assumption is that proteins responsible for the intraflagellar transport (IFT) of tubulin are present in limiting amounts. We show that the limiting-pool assumption is insufficient to describe the results of severing experiments, in which a flagellum is regenerated after it has been severed. Next, we consider an extension of the limiting-pool model that incorporates proteins that depolymerize microtubules. We show that this 'active disassembly' model of flagellar length control explains in quantitative detail the results of severing experiments and use it to make predictions that can be tested in experiments.
© 2019, Fai et al.

Entities:  

Keywords:  chlamydomonas reinhardtii; depolymerization; diffusion; flagella; length control; molecular motors; physics of living systems

Mesh:

Substances:

Year:  2019        PMID: 31596235      PMCID: PMC6863624          DOI: 10.7554/eLife.42599

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  47 in total

1.  Activation loop phosphorylation of a protein kinase is a molecular marker of organelle size that dynamically reports flagellar length.

Authors:  Muqing Cao; Dan Meng; Liang Wang; Shuqing Bei; William J Snell; Junmin Pan
Journal:  Proc Natl Acad Sci U S A       Date:  2013-07-08       Impact factor: 11.205

2.  Length regulation of active biopolymers by molecular motors.

Authors:  Denis Johann; Christoph Erlenkämper; Karsten Kruse
Journal:  Phys Rev Lett       Date:  2012-06-22       Impact factor: 9.161

3.  Physical model for the geometry of actin-based cellular protrusions.

Authors:  G Orly; M Naoz; N S Gov
Journal:  Biophys J       Date:  2014-08-05       Impact factor: 4.033

Review 4.  Cell Geometry: How Cells Count and Measure Size.

Authors:  Wallace F Marshall
Journal:  Annu Rev Biophys       Date:  2016-04-27       Impact factor: 12.981

5.  A motility in the eukaryotic flagellum unrelated to flagellar beating.

Authors:  K G Kozminski; K A Johnson; P Forscher; J L Rosenbaum
Journal:  Proc Natl Acad Sci U S A       Date:  1993-06-15       Impact factor: 11.205

6.  The Limiting-Pool Mechanism Fails to Control the Size of Multiple Organelles.

Authors:  Lishibanya Mohapatra; Thibaut J Lagny; David Harbage; Predrag R Jelenkovic; Jane Kondev
Journal:  Cell Syst       Date:  2017-05-24       Impact factor: 10.304

7.  Anomalies in the motion dynamics of long-flagella mutants of Chlamydomonas reinhardtii.

Authors:  Dolly K Khona; Venkatramanan G Rao; Mustafa J Motiwalla; P C Sreekrishna Varma; Anisha R Kashyap; Koyel Das; Seema M Shirolikar; Lalit Borde; Jayashree A Dharmadhikari; Aditya K Dharmadhikari; Siuli Mukhopadhyay; Deepak Mathur; Jacinta S D'Souza
Journal:  J Biol Phys       Date:  2012-09-30       Impact factor: 1.365

Review 8.  The intraflagellar transport machinery of Chlamydomonas reinhardtii.

Authors:  Douglas G Cole
Journal:  Traffic       Date:  2003-07       Impact factor: 6.215

9.  Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins.

Authors:  J L Rosenbaum; J E Moulder; D L Ringo
Journal:  J Cell Biol       Date:  1969-05       Impact factor: 10.539

10.  Self-organization of waves and pulse trains by molecular motors in cellular protrusions.

Authors:  A Yochelis; S Ebrahim; B Millis; R Cui; B Kachar; M Naoz; N S Gov
Journal:  Sci Rep       Date:  2015-09-03       Impact factor: 4.379

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  9 in total

1.  Speed and Diffusion of Kinesin-2 Are Competing Limiting Factors in Flagellar Length-Control Model.

Authors:  Rui Ma; Nathan L Hendel; Wallace F Marshall; Hongmin Qin
Journal:  Biophys J       Date:  2020-04-22       Impact factor: 4.033

2.  On the unity and diversity of cilia.

Authors:  Kirsty Y Wan; Gáspár Jékely
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-12-30       Impact factor: 6.237

3.  Global asymptotic stability of the active disassembly model of flagellar length control.

Authors:  Thomas G Fai; Youngmin Park
Journal:  J Math Biol       Date:  2021-12-30       Impact factor: 2.259

4.  Size regulation of multiple organelles competing for a limiting subunit pool.

Authors:  Deb Sankar Banerjee; Shiladitya Banerjee
Journal:  PLoS Comput Biol       Date:  2022-06-17       Impact factor: 4.779

5.  Equilibrium mechanisms of self-limiting assembly.

Authors:  Michael F Hagan; Gregory M Grason
Journal:  Rev Mod Phys       Date:  2021-06-11       Impact factor: 50.485

6.  Functional exploration of heterotrimeric kinesin-II in IFT and ciliary length control in Chlamydomonas.

Authors:  Shufen Li; Kirsty Y Wan; Wei Chen; Hui Tao; Xin Liang; Junmin Pan
Journal:  Elife       Date:  2020-10-28       Impact factor: 8.140

7.  Length-dependent disassembly maintains four different flagellar lengths in Giardia.

Authors:  Shane G McInally; Jane Kondev; Scott C Dawson
Journal:  Elife       Date:  2019-12-19       Impact factor: 8.140

8.  Analysis of biological noise in the flagellar length control system.

Authors:  David Bauer; Hiroaki Ishikawa; Kimberly A Wemmer; Nathan L Hendel; Jane Kondev; Wallace F Marshall
Journal:  iScience       Date:  2021-03-23

Review 9.  Intraflagellar Transport Proteins as Regulators of Primary Cilia Length.

Authors:  Wei Wang; Brittany M Jack; Henry H Wang; Matthew A Kavanaugh; Robin L Maser; Pamela V Tran
Journal:  Front Cell Dev Biol       Date:  2021-05-19
  9 in total

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