Kinetic mechanism of Nicotiana tabacum myosin-11 defines a new type of a processive motor

Ralph P. Diensthuber, Motoki Tominaga, Matthias Preller, Falk K. Hartmann, Hidefumi Orii, Igor Chizhov, Kazuhiro Oiwa, Georgios Tsiavaliaris

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

The 175-kDa myosin-11 from Nicotiana tabacum (Nt(175kDa)myosin-11) is exceptional in its mechanical activity as it is the fastest known processive actin-based motor, moving 10 times faster than the structurally related class 5 myosins. Although this ability might be essential for long-range organelle transport within larger plant cells, the kinetic features underlying the fast processive movement of Nt(175kDa)myosin-11 still remain unexplored. To address this, we generated a single-headed motor domain construct and carried out a detailed kinetic analysis. The data demonstrate that Nt(175kDa)myosin-11 is a high duty ratio motor, which remains associated with actin most of its enzymatic cycle. However, different from other processive myosins that establish a high duty ratio on the basis of a rate-limiting ADP-release step, Nt(175kDa)myosin-11 achieves a high duty ratio by a prolonged duration of the ATP-induced isomerization of the actin-bound states and ADP release kinetics, both of which in terms of the corresponding time constants approach the total ATPase cycle time. Molecular modeling predicts that variations in the charge distribution of the actin binding interface might contribute to the thermodynamic fine-tuning of the kinetics of this myosin. Our study unravels a new type of a high duty ratio motor and provides important insights into the molecular mechanism of processive movement of higher plant myosins.

Original languageEnglish
Pages (from-to)81-94
Number of pages14
JournalFASEB Journal
Volume29
Issue number1
DOIs
Publication statusPublished - 2015 Jan 1
Externally publishedYes

Fingerprint

Myosins
Tobacco
Kinetics
Actins
Adenosine Diphosphate
Molecular modeling
Charge distribution
Plant Cells
Isomerization
Thermodynamics
Organelles
Adenosine Triphosphatases
Tuning
Adenosine Triphosphate

Keywords

  • homology modeling
  • molecular mechanics
  • plant
  • processivity

ASJC Scopus subject areas

  • Medicine(all)

Cite this

Diensthuber, R. P., Tominaga, M., Preller, M., Hartmann, F. K., Orii, H., Chizhov, I., ... Tsiavaliaris, G. (2015). Kinetic mechanism of Nicotiana tabacum myosin-11 defines a new type of a processive motor. FASEB Journal, 29(1), 81-94. https://doi.org/10.1096/fj.14-254763

Kinetic mechanism of Nicotiana tabacum myosin-11 defines a new type of a processive motor. / Diensthuber, Ralph P.; Tominaga, Motoki; Preller, Matthias; Hartmann, Falk K.; Orii, Hidefumi; Chizhov, Igor; Oiwa, Kazuhiro; Tsiavaliaris, Georgios.

In: FASEB Journal, Vol. 29, No. 1, 01.01.2015, p. 81-94.

Research output: Contribution to journalArticle

Diensthuber, RP, Tominaga, M, Preller, M, Hartmann, FK, Orii, H, Chizhov, I, Oiwa, K & Tsiavaliaris, G 2015, 'Kinetic mechanism of Nicotiana tabacum myosin-11 defines a new type of a processive motor', FASEB Journal, vol. 29, no. 1, pp. 81-94. https://doi.org/10.1096/fj.14-254763
Diensthuber, Ralph P. ; Tominaga, Motoki ; Preller, Matthias ; Hartmann, Falk K. ; Orii, Hidefumi ; Chizhov, Igor ; Oiwa, Kazuhiro ; Tsiavaliaris, Georgios. / Kinetic mechanism of Nicotiana tabacum myosin-11 defines a new type of a processive motor. In: FASEB Journal. 2015 ; Vol. 29, No. 1. pp. 81-94.
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