Universal and Unique Features of Kinesin Motors: Insights from a Comparison of Fungal and Animal Conventional Kinesins

Abstract Kinesins are microtubule motors that use the energy derived from the hydrolysis of ATP to move unidirectionally along microtubules. The founding member of this still growing superfamily is conventional kinesin, a dimeric motor that moves processively towards the plus end of microtubules. Within the family of conventional kinesins, two groups can be distinguished to date, one derived from animal species, and one originating from filamentous fungi. So far no conventional kinesin has been reported from plant cells. Fungal and animal conventional kinesins differ in several respects, both in terms of their primary sequence and their physiological properties. Thus all fungal conventional kinesins move at velocities that are 4–5 times higher than those of animal conventional kinesins, and all of them appear to lack associated light chains. Both groups of motors are characterized by a number of group-specific sequence features which are considered here with respect to their functional importance. Animal and fungal conventional kinesins also share a number of sequence characteristics which point to common principles of motor function. The overall domain organization is remarkably similar. A C-terminal sequence motif common to all kinesins, which constitutes the only region of high homology outside the motor domain, suggests common principles of cargo association in both groups of motors. Consideration of the differences of, and similarities between, fungal and animal kinesins offers novel possibilities for experimentation (e. g., by constructing chimeras) that can be expected to contribute to our understanding of motor function.

[1]  T. Mitchison,et al.  The Bipolar Kinesin, KLP61F, Cross-links Microtubules within Interpolar Microtubule Bundles of Drosophila Embryonic Mitotic Spindles , 1999, The Journal of cell biology.

[2]  Timothy J. Mitchison,et al.  Kin I Kinesins Are Microtubule-Destabilizing Enzymes , 1999, Cell.

[3]  T. Rapoport,et al.  Light Chain– dependent Regulation of Kinesin's Interaction with Microtubules , 1998, Journal of Cell Biology.

[4]  J. Mackay,et al.  The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. , 1998, Biochemistry.

[5]  M. Schleicher,et al.  Importance of a flexible hinge near the motor domain in kinesin‐driven motility , 1998, The EMBO journal.

[6]  L. Goldstein,et al.  Chromosomal localization reveals three kinesin heavy chain genes in mouse. , 1998, Genomics.

[7]  S. Endow,et al.  Determinants of kinesin motor polarity. , 1998, Science.

[8]  V. Allan,et al.  Microtubule-based membrane movement. , 1998, Biochimica et biophysica acta.

[9]  N. Hirokawa,et al.  Targeted Disruption of Mouse Conventional Kinesin Heavy Chain kif5B, Results in Abnormal Perinuclear Clustering of Mitochondria , 1998, Cell.

[10]  Steinberg.  Organelle transport and molecular motors in fungi , 1998, Fungal genetics and biology : FG & B.

[11]  Ronald D. Vale,et al.  Role of the Kinesin Neck Region in Processive Microtubule-based Motility , 1998, The Journal of cell biology.

[12]  J Vandekerckhove,et al.  Proteolytic mapping of kinesin/ncd‐microtubule interface: nucleotide‐dependent conformational changes in the loops L8 and L12 , 1998, The EMBO journal.

[13]  I. Rayment,et al.  X-ray crystal structure of the yeast Kar3 motor domain complexed with Mg.ADP to 2.3 A resolution. , 1998, Biochemistry.

[14]  N. Hirokawa,et al.  Kinesin and dynein superfamily proteins and the mechanism of organelle transport. , 1998, Science.

[15]  B. Turgeon,et al.  A fungal kinesin required for organelle motility, hyphal growth, and morphogenesis. , 1998, Molecular biology of the cell.

[16]  E. Mandelkow,et al.  The Crystal Structure of Dimeric Kinesin and Implications for Microtubule-Dependent Motility , 1997, Cell.

[17]  E. Mandelkow,et al.  X-ray structure of motor and neck domains from rat brain kinesin. , 1997, Biochemistry.

[18]  Ronald D Vale,et al.  The Directional Preference of Kinesin Motors Is Specified by an Element outside of the Motor Catalytic Domain , 1997, Cell.

[19]  M. Schliwa,et al.  Reversal in the direction of movement of a molecular motor , 1997, Nature.

[20]  N. Hirokawa,et al.  Identification and classification of 16 new kinesin superfamily (KIF) proteins in mouse genome. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Andreas Hoenger,et al.  A Model for the Microtubule-Ncd Motor Protein Complex Obtained by Cryo-Electron Microscopy and Image Analysis , 1997, Cell.

[22]  Ronald D Vale,et al.  Microtubule Interaction Site of the Kinesin Motor , 1997, Cell.

[23]  M. Bölker,et al.  Identification of a motor protein required for filamentous growth in Ustilago maydis , 1997, The EMBO journal.

[24]  S. Seiler,et al.  Kinesin is essential for cell morphogenesis and polarized secretion in Neurospora crassa , 1997, The EMBO journal.

[25]  Hanry Yu,et al.  Molecular Requirements for Bi-directional Movement of Phagosomes Along Microtubules , 1997, The Journal of cell biology.

[26]  R. Hodges,et al.  Demonstration of Coiled-Coil Interactions within the Kinesin Neck Region Using Synthetic Peptides , 1997, The Journal of Biological Chemistry.

[27]  H. Morii,et al.  Identification of kinesin neck region as a stable alpha-helical coiled coil and its thermodynamic characterization. , 1997, Biochemistry.

[28]  R J Fletterick,et al.  The design plan of kinesin motors. , 1997, Annual review of cell and developmental biology.

[29]  W. Saxton,et al.  Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. , 1996, Genetics.

[30]  R. Vale,et al.  Switches, latches, and amplifiers: common themes of G proteins and molecular motors , 1996, The Journal of cell biology.

[31]  Ronald D. Vale,et al.  Crystal structure of the kinesin motor domain reveals a structural similarity to myosin , 1996, Nature.

[32]  Roger Cooke,et al.  Crystal structure of the motor domain of the kinesin-related motor ncd , 1996, Nature.

[33]  J. Burkhardt.  In search of membrane receptors for microtubule-based motors - is kinectin a kinesin receptor? , 1996, Trends in cell biology.

[34]  M. Sheetz.  Microtubule motor complexes moving membranous organelles. , 1996, Cell structure and function.

[35]  M. Sheetz,et al.  Kinectin, an essential anchor for kinesin-driven vesicle motility. , 1995, Science.

[36]  M. Sheetz,et al.  Characterization of kinectin, a kinesin-binding protein: primary sequence and N-terminal topogenic signal analysis. , 1995, Molecular biology of the cell.

[37]  C. Burd,et al.  Conserved structures and diversity of functions of RNA-binding proteins. , 1994, Science.

[38]  G. Bloom,et al.  Motor proteins. 1: kinesins. , 1994, Protein profile.

[39]  D. Thierry-Mieg,et al.  Cloning by insertional mutagenesis of a cDNA encoding Caenorhabditis elegans kinesin heavy chain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Gho,et al.  Effects of kinesin mutations on neuronal functions. , 1992, Science.

[41]  T. Reese,et al.  Kinesin is bound with high affinity to squid axon organelles that move to the plus-end of microtubules , 1992, The Journal of cell biology.

[42]  D. Hackney,et al.  Kinesin undergoes a 9 S to 6 S conformational transition. , 1992, The Journal of biological chemistry.

[43]  A. Lupas,et al.  Predicting coiled coils from protein sequences , 1991, Science.

[44]  E. Raff,et al.  Kinesin heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis , 1991, Cell.

[45]  E. Raff,et al.  Evidence that the head of kinesin is sufficient for force generation and motility in vitro. , 1990, Science.

[46]  G. Bloom,et al.  Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration , 1989, Cell.

[47]  M. Sheetz,et al.  The role of kinesin and other soluble factors in organelle movement along microtubules , 1988, The Journal of cell biology.

[48]  J. McIntosh,et al.  Identification of kinesin in sea urchin eggs, and evidence for its localization in the mitotic spindle , 1985, Nature.

[49]  Michael P. Sheetz,et al.  Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility , 1985, Cell.

[50]  Scott T. Brady,et al.  A novel brain ATPase with properties expected for the fast axonal transport motor , 1985, Nature.