The dynamic and structural properties of axonemal tubulins support the high length stability of cilia

Ron Orbach; Jonathon Howard

doi:10.1038/s41467-019-09779-6

The dynamic and structural properties of axonemal tubulins support the high length stability of cilia

Ron Orbach, Jonathon Howard

Yale University

Research output: Contribution to journal › Article › peer-review

39 Scopus citations

Abstract

Cilia and flagella play essential roles in cell motility, sensing and development. These organelles have tightly controlled lengths, and the axoneme, which forms the core structure, has exceptionally high stability. This is despite being composed of microtubules that are often characterized as highly dynamic. To understand how ciliary tubulin contribute to stability, we develop a procedure to differentially extract tubulins from different components of axonemes purified from Chlamydomonas reinhardtii, and characterize their properties. We find that the microtubules support length stability by two distinct mechanisms: low dynamicity, and unusual stability of the protofilaments. The high stability of the protofilaments manifests itself in the formation of curved tip structures, up to a few microns long. These structures likely reflect intrinsic curvature of GTP or GDP·Pi tubulin and provide structural insights into the GTP-cap. Together, our study provides insights into growth, stability and the role of post-translational modifications of axonemal microtubules.

Original language	English
Article number	1838
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-09779-6
State	Published - 23 Apr 2019
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2019, The Author(s).

Funding

We thank Dr. Xinran Liu from the core center for cellular and molecular imaging at Yale for sample processing, sectioning and image acquisition, and Dr. Joel Nott from the protein facility at Iowa State University for the mass-spectrometry analysis. Special thanks to Dr. Sabyasachi Sutradhar for the great help with MATLAB and all The Howard lab members for fruitful discussion. Research reported in this publication was supported by a Cross-Disciplinary Fellowship from Human Frontier Science Program (LT000919/ 2015-C) and European Molecular Biology Organization long-term fellowship (ALTF 1424-2014) to RO, and National Institute of General Medicine Sciences of the National Institutes of Health under award number R01GM110386 to JH.

Funders	Funder number
National Institute of General Medicine Sciences
National Institutes of Health
National Institute of General Medical Sciences	R01GM110386
European Molecular Biology Organization	ALTF 1424-2014
Human Frontier Science Program	LT000919/ 2015-C

Access to Document

10.1038/s41467-019-09779-6

Cite this

@article{bace797920ba4f26990e6363eea92c37,

title = "The dynamic and structural properties of axonemal tubulins support the high length stability of cilia",

abstract = "Cilia and flagella play essential roles in cell motility, sensing and development. These organelles have tightly controlled lengths, and the axoneme, which forms the core structure, has exceptionally high stability. This is despite being composed of microtubules that are often characterized as highly dynamic. To understand how ciliary tubulin contribute to stability, we develop a procedure to differentially extract tubulins from different components of axonemes purified from Chlamydomonas reinhardtii, and characterize their properties. We find that the microtubules support length stability by two distinct mechanisms: low dynamicity, and unusual stability of the protofilaments. The high stability of the protofilaments manifests itself in the formation of curved tip structures, up to a few microns long. These structures likely reflect intrinsic curvature of GTP or GDP·Pi tubulin and provide structural insights into the GTP-cap. Together, our study provides insights into growth, stability and the role of post-translational modifications of axonemal microtubules.",

author = "Ron Orbach and Jonathon Howard",

note = "Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = apr,

day = "23",

doi = "10.1038/s41467-019-09779-6",

language = "אנגלית",

volume = "10",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

}

TY - JOUR

T1 - The dynamic and structural properties of axonemal tubulins support the high length stability of cilia

AU - Orbach, Ron

AU - Howard, Jonathon

PY - 2019/4/23

Y1 - 2019/4/23

N2 - Cilia and flagella play essential roles in cell motility, sensing and development. These organelles have tightly controlled lengths, and the axoneme, which forms the core structure, has exceptionally high stability. This is despite being composed of microtubules that are often characterized as highly dynamic. To understand how ciliary tubulin contribute to stability, we develop a procedure to differentially extract tubulins from different components of axonemes purified from Chlamydomonas reinhardtii, and characterize their properties. We find that the microtubules support length stability by two distinct mechanisms: low dynamicity, and unusual stability of the protofilaments. The high stability of the protofilaments manifests itself in the formation of curved tip structures, up to a few microns long. These structures likely reflect intrinsic curvature of GTP or GDP·Pi tubulin and provide structural insights into the GTP-cap. Together, our study provides insights into growth, stability and the role of post-translational modifications of axonemal microtubules.

AB - Cilia and flagella play essential roles in cell motility, sensing and development. These organelles have tightly controlled lengths, and the axoneme, which forms the core structure, has exceptionally high stability. This is despite being composed of microtubules that are often characterized as highly dynamic. To understand how ciliary tubulin contribute to stability, we develop a procedure to differentially extract tubulins from different components of axonemes purified from Chlamydomonas reinhardtii, and characterize their properties. We find that the microtubules support length stability by two distinct mechanisms: low dynamicity, and unusual stability of the protofilaments. The high stability of the protofilaments manifests itself in the formation of curved tip structures, up to a few microns long. These structures likely reflect intrinsic curvature of GTP or GDP·Pi tubulin and provide structural insights into the GTP-cap. Together, our study provides insights into growth, stability and the role of post-translational modifications of axonemal microtubules.

UR - http://www.scopus.com/inward/record.url?scp=85064913187&partnerID=8YFLogxK

U2 - 10.1038/s41467-019-09779-6

DO - 10.1038/s41467-019-09779-6

M3 - ???researchoutput.researchoutputtypes.contributiontojournal.article???

C2 - 31015426

AN - SCOPUS:85064913187

SN - 2041-1723

VL - 10

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1838

ER -

The dynamic and structural properties of axonemal tubulins support the high length stability of cilia

Abstract

Bibliographical note

Funding

Access to Document

Other files and links

Fingerprint

Cite this