Distinct roles of 1α and 1β heavy chains of the inner arm dynein I1 of Chlamydomonas flagella

Shiori Toba, Laura A. Fox, Hitoshi Sakakibara, Mary E. Porter, Kazuhiro Oiwa, Winfield S. Sale

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

The Chlamydomonas I1 dynein is a two-headed inner dynein arm important for the regulation of flagellar bending. Here we took advantage of mutant strains lacking either the 1α or 1β motor domain to distinguish the functional role of each motor domain. Single-particle electronic microscopic analysis confirmed that both the I1α and I1β complexes are single headed with similar ringlike, motor domain structures. Despite similarity in structure, however, the I1β complex has severalfold higher ATPase activity and microtubule gliding motility compared to the I1α complex. Moreover, in vivo measurement of microtubule sliding in axonemes revealed that the loss of the 1β motor results in a more severe impairment in motility and failure in regulation of microtubule sliding by the I1 dynein phosphoregulatory mechanism. The data indicate that each I1 motor domain is distinct in function: The I1β motor domain is an effective motor required for wild-type microtubule sliding, whereas the I1α motor domain may be responsible for local restraint of microtubule sliding.

Original languageEnglish (US)
Pages (from-to)342-353
Number of pages12
JournalMolecular biology of the cell
Volume22
Issue number3
DOIs
StatePublished - Feb 1 2011

Fingerprint

Chlamydomonas
Dyneins
Flagella
Microtubules
Axoneme
Adenosine Triphosphatases

Cite this

Distinct roles of 1α and 1β heavy chains of the inner arm dynein I1 of Chlamydomonas flagella. / Toba, Shiori; Fox, Laura A.; Sakakibara, Hitoshi; Porter, Mary E.; Oiwa, Kazuhiro; Sale, Winfield S.

In: Molecular biology of the cell, Vol. 22, No. 3, 01.02.2011, p. 342-353.

Research output: Contribution to journalArticle

Toba, Shiori ; Fox, Laura A. ; Sakakibara, Hitoshi ; Porter, Mary E. ; Oiwa, Kazuhiro ; Sale, Winfield S. / Distinct roles of 1α and 1β heavy chains of the inner arm dynein I1 of Chlamydomonas flagella. In: Molecular biology of the cell. 2011 ; Vol. 22, No. 3. pp. 342-353.
@article{43c0d28e5dee4442936a8ac6e3fd70cf,
title = "Distinct roles of 1α and 1β heavy chains of the inner arm dynein I1 of Chlamydomonas flagella",
abstract = "The Chlamydomonas I1 dynein is a two-headed inner dynein arm important for the regulation of flagellar bending. Here we took advantage of mutant strains lacking either the 1α or 1β motor domain to distinguish the functional role of each motor domain. Single-particle electronic microscopic analysis confirmed that both the I1α and I1β complexes are single headed with similar ringlike, motor domain structures. Despite similarity in structure, however, the I1β complex has severalfold higher ATPase activity and microtubule gliding motility compared to the I1α complex. Moreover, in vivo measurement of microtubule sliding in axonemes revealed that the loss of the 1β motor results in a more severe impairment in motility and failure in regulation of microtubule sliding by the I1 dynein phosphoregulatory mechanism. The data indicate that each I1 motor domain is distinct in function: The I1β motor domain is an effective motor required for wild-type microtubule sliding, whereas the I1α motor domain may be responsible for local restraint of microtubule sliding.",
author = "Shiori Toba and Fox, {Laura A.} and Hitoshi Sakakibara and Porter, {Mary E.} and Kazuhiro Oiwa and Sale, {Winfield S.}",
year = "2011",
month = "2",
day = "1",
doi = "10.1091/mbc.E10-10-0806",
language = "English (US)",
volume = "22",
pages = "342--353",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "3",

}

TY - JOUR

T1 - Distinct roles of 1α and 1β heavy chains of the inner arm dynein I1 of Chlamydomonas flagella

AU - Toba, Shiori

AU - Fox, Laura A.

AU - Sakakibara, Hitoshi

AU - Porter, Mary E.

AU - Oiwa, Kazuhiro

AU - Sale, Winfield S.

PY - 2011/2/1

Y1 - 2011/2/1

N2 - The Chlamydomonas I1 dynein is a two-headed inner dynein arm important for the regulation of flagellar bending. Here we took advantage of mutant strains lacking either the 1α or 1β motor domain to distinguish the functional role of each motor domain. Single-particle electronic microscopic analysis confirmed that both the I1α and I1β complexes are single headed with similar ringlike, motor domain structures. Despite similarity in structure, however, the I1β complex has severalfold higher ATPase activity and microtubule gliding motility compared to the I1α complex. Moreover, in vivo measurement of microtubule sliding in axonemes revealed that the loss of the 1β motor results in a more severe impairment in motility and failure in regulation of microtubule sliding by the I1 dynein phosphoregulatory mechanism. The data indicate that each I1 motor domain is distinct in function: The I1β motor domain is an effective motor required for wild-type microtubule sliding, whereas the I1α motor domain may be responsible for local restraint of microtubule sliding.

AB - The Chlamydomonas I1 dynein is a two-headed inner dynein arm important for the regulation of flagellar bending. Here we took advantage of mutant strains lacking either the 1α or 1β motor domain to distinguish the functional role of each motor domain. Single-particle electronic microscopic analysis confirmed that both the I1α and I1β complexes are single headed with similar ringlike, motor domain structures. Despite similarity in structure, however, the I1β complex has severalfold higher ATPase activity and microtubule gliding motility compared to the I1α complex. Moreover, in vivo measurement of microtubule sliding in axonemes revealed that the loss of the 1β motor results in a more severe impairment in motility and failure in regulation of microtubule sliding by the I1 dynein phosphoregulatory mechanism. The data indicate that each I1 motor domain is distinct in function: The I1β motor domain is an effective motor required for wild-type microtubule sliding, whereas the I1α motor domain may be responsible for local restraint of microtubule sliding.

UR - http://www.scopus.com/inward/record.url?scp=79551677928&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79551677928&partnerID=8YFLogxK

U2 - 10.1091/mbc.E10-10-0806

DO - 10.1091/mbc.E10-10-0806

M3 - Article

C2 - 21148301

AN - SCOPUS:79551677928

VL - 22

SP - 342

EP - 353

JO - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 3

ER -