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Mechanism of Ultra-Fast Actin-Myosin Sliding Producing Cytoplasmic Streaming in Giant Algal Cell, Studied Using the Centrifuge Microscope

Abstract

Shigeru Chaen and Haruo Sugi

In giant intermodal cells of green algae Chara collaria, cytoplasmic streaming is produced by ATP-dependent sliding between myosin heads extending from amorphous cytoplasmic organelles and actin filament arrays (actin cables) fixed on chloroplast rows. The velocity of cytoplasmic streaming is many times faster than the maximum myofilament sliding in skeletal muscle. In this article, we compared steady-state force-velocity (P-V) relations between cytoplasmic myosin and skeletal and cardiac muscle myosins using the centrifuge microscope, in which myosincoated latex beads were made to slide along the actin cables under various centrifugal forces. In contrast with the hyperbolic P-V relation of actin-myosin sliding in skeletal and cardiac myosins, the P-V relation of cytoplasmic myosin versus actin cable sliding was a straight line, indicating a very large duty ratio and a very small rate of chemomechanical energy conversion. Possible mechanisms of the ultra-fast actin-myosin sliding are discussed.
Highlights
• The velocity of cytoplasmic streaming, caused by ATP-dependent sliding between cytoplasmic myosin and actin cables in giant algal cells is many times faster than ATP-dependent actin-myosin sliding in skeletal and cardiac muscles.
• The mechanism of ultra-fast actin-myosin sliding was studied using the centrifuge microscope, in which beads coated with cytoplasmic myosin were made to slide along actin cables under various centrifugal forces serving as loads against cytoplasmic myosin versus actin cable sliding.
• Unlike the hyperbolic force-velocity (P-V) relation of skeletal and cardiac muscle actin-myosin sliding, the P-V relation of cytoplasmic actin myosin sliding was a straight line irrespective of the force generated by cytoplasmic myosin.
• These results indicate a very large duty ratio and a very small efficiency of chemo-mechanical energy conversion in cytoplasmic actin-myosin sliding.

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