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5 Published by Pan Stanford Publishing Pte. Ltd. Penthouse Level, Suntec Tower 3 8 Temasek Boulevard Singapore editorial@panstanford.com Web: British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library. Handbook of Dynein Copyright 2012 Pan Stanford Publishing Pte. Ltd. All rights reserved. This book, or parts thereof, may not be reproduced in any form or by any means, electronic or mechanical, including photocopying, recording or any information storage and retrieval system now known or to be invented, without written permission from the publisher. For photocopying of material in this volume, please pay a copying fee through the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, USA. In this case permission to photocopy is not required from the publisher. ISBN (Hardcover) ISBN (ebook) Printed in the USA
6 Contents 1. Dyneins: Ancient Protein Complexes Gradually Reveal their Secrets 1 Linda A. Amos and Keiko Hirose 1.1 Introduction Dynein Molecular Structure Coming into View Axonemal Arms Dynein Molecules Lighter Components of the Complexes Effect on the Heavy Chain of Vanadate and UV Motility of Dynein Evolution Where did Dyneins Come From? AAA+ Proteins Ancestors and Relatives of the Dynein Heavy Chain CD-2 Is Probably Similar to the Common Ancestor Almost All Eukaryotic Organisms Express Dynein Summary Two Decades of Cytoplasmic Dynein: From Fast to Forceful 27 Richard J. McKenney and Richard B. Vallee 2.1 Introduction Cytoplasmic Dynein Functions Compositional and Regulatory Diversity Cytoplasmic Dynein Isoforms Accessory Complexes Dynactin LIS1 and NudE/NudEL Effects of LIS1 and NudE on Dynein Activity in vitro LIS1/NudE Enhancement of Multiple Motor Transport Cytoplasmic Dynein Regulation by Dynactin vs. NudE-LIS Functional Analysis of the Dynein Motor Domain 43 Tomohiro Shima, Kazuo Sutoh, and Takahide Kon 3.1 Introduction The Dynein Motor Domain ATPase Cycles in the Head Domain Movement of the Linker 49
7 vi Contents 3.5 Microtubule Binding at the Stalk Perspectives Structural Studies on the Dynein Heavy Chain 63 Anthony J. Roberts and Stan A. Burgess 4.1 Introduction The Form and Function of the Heavy Chain The Tail Domain The Stalk Domain The Head Domain The AAA+ ring The C-terminal sequence The linker domain Conformational Changes Conclusions and Outlook Structural Analysis of Dynein Bound to Microtubules 81 Keiko Hirose 5.1 Introduction Formation of a Dynein-Microtubule Complex MT-Binding of Outer-Arm Dynein Purified from Chlamydomonas Axoneme MT-Binding of Outer-Arm Dynein Purified from Tetrahymena Axoneme MT-Binding of Outer-Arm Dynein Purified from Sea Urchin Axonemes MT-Binding of Cytoplasmic Dynein MT-Binding of Recombinant Dynein Motor Domains Analysis of the Dynein-Microtubule Complex D Structural Analysis of the Dynein-MT Complex D structural analysis of recombinant dynein stalk regions bound to MTs D structural analysis of recombinant dynein bound to MTs D structural analysis of axonemal dynein cross-bridging MTs Angles of Dynein Stalks Bound to MTs Movement of the Heads in MT-Bound Axonemal Dynein Motile Mechanism of Dynein Future Outlook 94
8 Contents vii 6. The Dynein Stalk: Atomic Structure and Roles in the Mechanism of the Dynein Motor 99 Andrew P. Carter 6.1 Introduction Structural Features of the Dynein Stalk Historical Background Microtubule-Binding Domain Stalk Coiled Coil Junction of Stalk and AAA Ring Communication Along the Dynein Stalk Models for Communication Large scale conformational changes Communication via changes in stalk binding angle Relative sliding of helices in the coiled coil Structural Changes During Communication Half-heptad movement Smaller shifts in the coiled coil Conformational changes around the kink in the stalk Role of the Stalk in the Dynein Powerstroke Models of Stalk Involvement in the Powerstroke Stalk acts as a paddle Structural change near MTBD rotates stalk (stalk lever arm model) Stalk is rigid and holds AAA ring so that conformational change is directed Stalk acts as a tether, preferentially binding toward the MT minus end The Stalk and Directionality Conclusion Motile and Enzymatic Properties of Native Dynein Molecules 123 Yoko Y. Toyoshima and Hideo Higuchi 7.1 Introduction Preparations of Native Dynein Molecules for Functional Assays Cytoplasmic Dynein from Mammalian Brain Axonemal Dyneins from Tetrahymena Cilia 126
9 viii Contents 7.3 Measurement of Dynein ATPase Activity Method for Steady-State ATPase Assaying of Dyneins ATPase Activity Properties of Native Dyneins In vitro Motility of Native Dynein Molecules In vitro Motility Assay for Dynein Motile Properties of Native Dynein Molecules In vitro Motility of Single Native Dynein Molecules Processivity of Single Dynein Molecules Processivity and Step Size as Determined with FIONA Method Step Size and Force Measurement of Single Dynein Molecules by Optical Trapping Model of Dynein Walking Vesicles Transport Driven by Dynein in Cells Step Size of Dynein During Vesicle Transport in Cells Force Generation by Dynein in Cells In vivo Mechanical Measurement of Dynein Summary Motile Properties of Cytoplasmic Dynein 145 Samara L. Reck-Peterson, Ronald D. Vale, and Arne Gennerich 8.1 Introduction Sources of Cytoplasmic Dynein Native Dynein Recombinant Dynein Cytoplasmic Dynein Motility in the Absence of Load Cytoplasmic Dynein is a Processive Motor Stepping Behavior of Cytoplasmic Dynein Under Unloaded Conditions Directionality of Cytoplasmic Dynein Response of Cytoplasmic Dynein to Load Regulation of Cytoplasmic Dynein Motility AAA+ Domains AAA AAA2, AAA AAA Dynein Cofactors Dynactin LIS1 and NudE 163
10 Contents ix 8.6 In vivo Studies of Dynein Motility Conclusions and Future Directions Motility of Inner-Arm Dyneins 173 Yuji Shitaka, Hiroaki Kojima, and Kazuhiro Oiwa 9.1 Introduction Description of Inner Arms In vitro Motility Assays Single-Molecule Measurements Solutions Protein Preparations Inner-Arm Dynein Subspecies Preparation of Microtubules and their Fluorescent Labeling In vitro Motility Assays Overview Preparation of dynein-coated beads for optical trap nanometry Preparation of a flow cell Preparation of patterned surface for bio-nano device development In vitro motility assay of inner-arm dyneins Evaluation of the processivity Optical trap nanometry Results In vitro Motility Assays Optical-Trap Nanometry Studies on Dynein Motility The Directional Control of MT Movement on Dynein-Coated Surfaces Summary and Outlook Levels of Coordination that Need to be Studied Dynein Motility in Cilia and Flagella 203 Avanti Gokhale, Maureen Wirschell, Winfield S. Sale, and David R. Mitchell 10.1 Introduction Axoneme Structural Organization and Dynein Subforms Basic Axonemal Structure, Axis of Bending and the 96 nm Repeat 205
11 x Contents Definition of the Dyneins and their Functions The outer dynein arms, beat frequency, and force The inner dynein arms and control of ciliary waveform Axonemal Structures that Regulate Dynein The Central Pair Radial Spoke Network The DRC The Dynein Arm Linkers Sliding Microtubule/Direction Switching Model The Sliding Microtubule Model A Switching Model for Forward and Reverse Bending Inherent Regulation of Microtubule Sliding Mechanical Feedback and Calcium Regulation Mechanical Feedback Mechanisms Central pair orientation Radial spoke tilting Central pair asymmetry Signaling Mechanisms in Bend Propagation Central pair as control center Control via bend-plane doublets Calcium Sensors and Control of Dynein Asymmetry in metazoan spermatozoa Waveform control in algal flagella Arm-associated calcium-binding proteins Regulation of Motility by Phosphorylation Regulation of Outer Arms by Calcium and Phosphorylation Control of beat frequency Activation of motility Regulation of Inner Dynein Arms by Phosphorylation Protein kinase inhibition IC138 mutants Inhibition of CK Role of IC Future Challenges and Opportunities 231
12 Contents xi 11. 3D Structures of Axonemes 245 Takashi Ishikawa 11.1 Introduction Single-Particle Analysis and Electron Tomography Specimen Preparation for Electron Tomography/ Microscopy Ice-embedding by plunge freezing (cryo) Freeze-fracture deep-etch replica and rotary shadowing Negative staining, cryo-negative, and positive staining Plastic embedded sections Data Acquisition and Reconstruction in Electron Tomography D Averaging from Tomogram, Classification, and Modeling In situ Structure of Dynein Arms Revealed by Electron Tomography D Structure of Outer Dynein Arms D Structure of Inner Dynein Arms Asymmetric Dynein Arrangement in Chlamydomonas Flagella Nucleotide-Induced Structural Change of Flagellar Dynein Arms Structures of Other Components in Flagella Nexin and Other Interdoublet Linkers IFT Radial Spokes and Central Pairs Future Outlook Functional Diversity of Axonemal Dyneins 267 Ritsu Kamiya 12.1 Introduction Biochemical Analyses Separation of Individual Dyneins Subunit Composition Total gene assignment of axonemal dynein heavy chains Phylogeny of axonemal dyneins 272
13 xii Contents 12.3 Functional Diversity Assessed by the Mutant Motility Available Mutants Mutant Phenotypes Mutants lacking any single type of dynein can swim slowly Outer- and inner-arm dynein Specific functions of certain types of dyneins Function of individual heavy chains In Vitro Motility Assays General Features ADP Sensitivity Functional Interactions Between Outer-Arm Heavy Chains Novel Phenomena in Inner-Arm Dyneins Microtubule bending Ratchet-like properties Conclusions and Outlook Assembly and Regulation of Dynein Light Chains 285 Afua Nyarko and Elisar Barbar 13.1 Introduction The Regulatory Subunits: Structure, Functions, and Association States Interactions Between the Intermediate and Light Chain Subunits Mapping Interactions Identifying Conformational Changes High-Resolution Complex Structures Regulation by Disorder-to-Order Transitions Disorder-to-Order Transition at the Sites of Binding Disorder-to-Order Transition Distant from Binding Regulation by Subunit Phosphorylation Poly-Bivalency in Assembled IC The Light Chains Intermediate Chain Assembled Subcomplex Regulatory Subunits of Axonemal Dynein 303 Kazuo Inaba 14.1 Introduction Chlamydomonas Outer-Arm Dynein 304
14 Contents xiii Heavy Chains Intermediate Chains Light Chains LC1: leucine-rich repeat light chain LC2: Tctex2-related light chain LC3 and LC5: thioredoxin homolog associated with dynein HCs LC4: Ca 2+ -binding light chain LC7a and LC7b: Drosophila roadblock homologs LC8, LC6, and LC10: highly conserved protein LC8 and its homologs Dynein Docking Complex Proteins Associated with Outer-Arm Dynein Outer-Arm Dynein from Sperm Flagella Heavy Chains Intermediate Chains Light Chains Proteins Associated with Outer-Arm Dynein Chlamydomonas Inner-Arm Dynein Subunits of Dynein-f/I Subunits of Other Inner-Arm Dyneins Inner-Arm Dynein from Sperm Flagella Regulatory Functions of Dynein Subunits in Ciliary and Flagellar Motility Protein Phosphorylation and Dephosphorylation Ca 2+ -Dependent Regulation Redox Poise Nucleotide Metabolism Comparison and Evolutionary Aspects of Axonemal Dynein Components The Role of Dynein in Yeast Nuclear Segregation 325 Melissa D. Stuchell-Brereton, Jeffery K. Moore, and John A. Cooper 15.1 Introduction Mechanisms that Position Nucleus and Spindle The Kar9 Pathway The Dynein Pathway 327
15 xiv Contents Discovery of dynein in yeast Dynein localizes to MT plus ends and the cell cortex in S. cerevisiae Dynein generates force at interface between cmts and the cortex Components of the Yeast Dynein Complex and Conservation Across Species Heavy Chain/DYN Intermediate Chain/PAC Light Intermediate Chain/DYN Light Chain/DYN Regulatory Components Contributing to Dynein Function Dynactin Nip100/p150 Glued Jnm1/dynamitin Yll049w/Ldb18/p Arp Arp10/Arp Bik1/CLIP-170 and the Kinesin Kip Pac1/LIS1 and Ndl1/NudE(L) Num Cell Polarity and Cell Cycle Regulators Offloading Model Methods for Studying Dynein Function in Yeast Assaying the Position of the Nucleus and Spindle as a Measure of Dynein Activity Examining nuclear segregation by DAPI-stain Examining the position of the mitotic spindle using GFP-labeled MTs 349 Index 363
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