Identification and molecular evolution of new dynein-like protein sequences in rat brain
10.1242/jcs.108.5.1883
Crossref journal-article
The Company of Biologists
Journal of Cell Science (237)
Abstract

ABSTRACT RT-PCR cloning was performed to find unknown members of the dynein superfamily expressed in rat brain. Six kinds of degenerate primers designed for the dynein catalytic domain consensuses were used for extensive PCR amplifications. We have sequenced 550 plasmid clones which turned out to include 13 kinds of new dynein-like sequences (DLP1-8, 9A/B, 10-12) and cytoplasmic dynein heavy chain. In these clones, alternative splicing was detected for a 105 nt-domain containing the CFDEFNRI consensus just downstream of the most N-terminal P-loop (DLP9A and 9B). By using these obtained sequences, initial hybridization studies were performed. Genomic Southern blotting showed each sequence corresponds to a single copy of the gene, while northern blotting of adult brain presented more than one band for some subtypes. We further accomplished molecular evolutionary analysis to recognize their phylogenetic origins for the axonemal and non-axonemal (cytoplasmic) functions. Different methods (UPGMA, nJ and MP) presented well coincident phylogenetic trees from 44 partial amino acid sequences of dynein heavy chain from various eukaryotes. The trunk for all the cytoplasmic dynein heavy chain homologues diverged directly from the root of the phylogenetic tree, suggesting that the first dynein gene duplication defined two distinct functions as respective subfamilies. Of particular interest, we found a duplication event of the cytoplasmic dynein heavy chain gene giving rise to another subtype, DLP4, located between the divergence of yeast and that of Dictyostelium. Such evolutionary topology builds up an inceptive hypothesis that there are at least two non-axonemal dynein heavy chains in mammals.

Bibliography

Tanaka, Y., Zhang, Z., & Hirokawa, N. (1995). Identification and molecular evolution of new dynein-like protein sequences in rat brain. Journal of Cell Science, 108(5), 1883–1893.

Authors 3
  1. Yosuke Tanaka (first)
  2. Zhizeng Zhang (additional)
  3. Nobutaka Hirokawa (additional)
References 71 Referenced 90
  1. 10.1083/jcb.66.2.225 / J. Cell Biol / Lack of dynein arms in immotile human spermatozoa by Afzelius (1975)
  2. {'key': '2023122621440514300_JOCES_108_5_1883C2', 'first-page': '537', 'article-title': 'Choroid plexus and ependyma', 'volume-title': 'In Cytology and Cellular Pathology of the Nervous System', 'author': 'Agduhr', 'year': '1932'} / In Cytology and Cellular Pathology of the Nervous System / Choroid plexus and ependyma by Agduhr (1932)
  3. 10.1083/jcb.119.5.1287 / J. Cell Biol / Kinesin family in murine central nervous system by Aizawa (1992)
  4. 10.1016/0962-8924(93)90090-N / Trends Cell Biol / Dynein heavy chain isoforms and axonemal motility by Asai (1993)
  5. 10.1242/jcs.107.4.839 / J. Cell Sci / The dynein genes of Paramecium tetraurelia. Sequences adjacent to the catalytic P-loop identify cytoplasmic and axonemal heavy chain isoforms by Asai (1994)
  6. 10.1002/cm.970240402 / Cell Motil. Cytoskel / Phylogenetic analysis of the myosin superfamily by Cheney (1993)
  7. 10.1083/jcb.118.6.1333 / J. Cell Biol / Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex by Corthésy-Theulaz (1992)
  8. {'key': '2023122621440514300_JOCES_108_5_1883C8', 'volume-title': 'Atlas of Protein Sequence and Structure 1966', 'author': 'Eck', 'year': '1966'} / Atlas of Protein Sequence and Structure 1966 by Eck (1966)
  9. 10.1016/0092-8674(83)90170-8 / Cell / A recovered avian myelocytomatosis virus that induces lymphomas in chickens: pathogenic properties and their molecular basis by Enrietto (1983)
  10. 10.1073/pnas.90.23.11172 / Proc. Nat. Acad. Sci. USA / Cytoplasmic dynein is required for normal nuclear segregation in yeast by Eshel (1993)
  11. 10.1083/jcb.119.6.1541 / J. Cell Biol / Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains by Espreafico (1992)
  12. 10.2307/2408678 / Evolution / Confidence limits on phylogenies: an approach using the bootstrap by Felsenstein (1985)
  13. {'key': '2023122621440514300_JOCES_108_5_1883C13', 'volume-title': 'PHYLIP (Phylogeny Inference Package), version 3.5p. Distributed by the author. Department of Genetics, University of Washington, Seattle', 'author': 'Felsenstein', 'year': '1993'} / PHYLIP (Phylogeny Inference Package), version 3.5p. Distributed by the author. Department of Genetics, University of Washington, Seattle by Felsenstein (1993)
  14. 10.1091/mbc.5.1.57 / Mol. Biol. Cell / Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins by Gibbons (1994)
  15. 10.1083/jcb.91.3.107s / J. Cell Biol / Cilia and flagella of eukaryotes by Gibbons (1981)
  16. 10.1038/352640a0 / Nature / Multiple nucleotide-binding sites in the sequence of dynein β heavy chain by Gibbons (1991)
  17. 10.1083/jcb.109.5.2379 / J. Cell Biol / A squid dynein isoform promotes axoplasmic vesicle translocation by Gilbert (1989)
  18. Gilbert, D. G. (1990). TreeDraw Deck, A Hypercard implementation of Joseph Felsenstein’s phylogenetic tree drawing routines. Published electronically on the Internet, available via anonymous ftp toftp.bio.indiana.edu.
  19. 10.1146/annurev.ge.27.120193.001535 / Annu. Review Genet / With apologies to Scheherazade: tales of 1001 kinesin motors by Goldstein (1993)
  20. 10.1073/pnas.90.2.659 / Proc. Nat. Acad. Sci. USA / Molecular evolution of the myosin family: relationships derived from comparisons of amino acid sequences by Goodson (1993)
  21. 10.1242/jcs.107.7.1875 / J. Cell Sci / Molecular phylogeny of the kinesin family of microtubule motor proteins by Goodson (1994)
  22. 10.1007/BF00182185 / J. Mol. Evol / Early branchings in the evolution of eukaryotes: ancient divergence of entamoeba that lacks mitochondria revealed by protein sequence data by Hasegawa (1993)
  23. {'key': '2023122621440514300_JOCES_108_5_1883C23', 'first-page': '189', 'article-title': 'Clustal V: improved software for multiple sequence alignment', 'volume': '8', 'author': 'Higgins', 'year': '1992', 'journal-title': 'CABIOS'} / CABIOS / Clustal V: improved software for multiple sequence alignment by Higgins (1992)
  24. 10.1083/jcb.94.1.129 / J. Cell Biol / The crosslinker system between neurofilaments, microtubules and membranous organelles in frog axons revealed by quick freeze, freeze fracture, deep etching method by Hirokawa (1982)
  25. 10.1083/jcb.111.3.1027 / J. Cell Biol / Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo by Hirokawa (1990)
  26. 10.1016/0959-4388(93)90144-N / Curr. Opin. Neurobiol / Axonal transport and the cytoskeleton by Hirokawa (1993)
  27. 10.1016/0168-0102(93)90099-C / Neurosci. Res / Mechanism of axonal transport: identification of new molecular motors and regulations of transports by Hirokawa (1993)
  28. 10.1242/jcs.103.3.653 / J. Cell Sci / Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein by Kagami (1992)
  29. 10.1007/BF02141468 / Beitr. Klin. Tuberk / Zur Pathogenese der Bronchiektasien: Bronchiektasien bei Situs viscerum inversus by Kartagener (1933)
  30. 10.1083/jcb.125.5.1095 / J. Cell Biol / KIF3A is a new microtubule-based anterograde motor in the nerve axon by Kondo (1994)
  31. 10.1083/jcb.119.6.1597 / J. Cell Biol / Dynein from Dictyostelium: primary structure comparisons between a cytoplasmic motor enzyme and flagellar dynein by Koonce (1992)
  32. 10.1073/pnas.90.12.5519 / Proc. Nat. Acad. Sci. USA / A motility in the eukaryotic flagellum unrelated to flagellar beating by Kozminski (1994)
  33. 10.1073/pnas.90.21.10096 / Proc. Nat. Acad. Sci. USA / Disruption of mitotic spindle orientation in a yeast dynein mutant by Li (1993)
  34. 10.1073/pnas.87.23.9093 / Proc. Nat. Acad. Sci. USA / Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison by Loomis (1990)
  35. {'key': '2023122621440514300_JOCES_108_5_1883C35', 'first-page': '49', 'article-title': 'Dynein arm mutants of Chlamydomonas', 'volume-title': 'In Cell Movement', 'author': 'Luck', 'year': '1989'} / In Cell Movement / Dynein arm mutants of Chlamydomonas by Luck (1989)
  36. 10.1093/genetics/128.3.549 / Genetics / Genetic interactions at the FLA10 locus: suppressors and synthetic phenotypes that affect the cell cycle and flagellar function in Chlamydomonas reinhardtii by Lux (1991)
  37. 10.1016/0092-8674(87)90157-7 / Cell / Identification of a microtubule-based motor in the nematode, Caenorhabditis elegans by Lye (1987)
  38. 10.1525/9780520340510 / Microcosmos: Four Billion Years of Microbial Evolution. Summit Books, New York by Margulis (1986)
  39. 10.1016/0896-6273(93)90195-W / Neuron / Molecular cloning of the retrograde transport motor cytoplasmic dynein (MAP 1C) by Mikami (1993)
  40. 10.1242/jcs.107.3.635 / J. Cell Sci / Sequence analysis of the Chlamydomonas alpha and beta dynein heavy chain genes by Mitchell (1994)
  41. 10.1016/0092-8674(94)90012-4 / Cell / KIF1B; A new microtubule plusend directed monomeric motor for mitochondria transport by Nangaku (1994)
  42. 10.1083/jcb.107.5.1767 / J. Cell Biol / Sertoli cell processes have axoplasmic features: an ordered microtubule distribution and an abundant high molecular weight microtubule-associated protein (cytoplasmic dynein) by Neely (1988)
  43. {'key': '2023122621440514300_JOCES_108_5_1883C43', 'article-title': 'KIF2 is a new anterograde microtubule based motor which transports membranous organelles distinct from those carried by KHC or KIF3A/B', 'volume-title': 'J. Cell Biol', 'author': 'Noda', 'year': '1995'} / J. Cell Biol / KIF2 is a new anterograde microtubule based motor which transports membranous organelles distinct from those carried by KHC or KIF3A/B by Noda (1995)
  44. 10.1038/352643a0 / Nature / Four ATP-binding sites in the midregion of the β heavy chain of dynein by Ogawa (1991)
  45. 10.1016/0076-6879(87)54067-8 / Meth. Enzymol / High-efficiency cloning of full-length cDNA: Construction and screening of cDNA expression libraries from mammalian cells by Okayama (1987)
  46. 10.1146/annurev.bi.55.070186.005351 / Annu. Rev. Biochem / Splicing of messenger RNA precursors by Padgett (1986)
  47. 10.1083/jcb.105.3.1273 / J. Cell Biol / MAP1C is a microtubule-associated ATPase which translocates microtubules in vitro and has dynein-like properties by Paschal (1987)
  48. 10.1095/biolreprod12.5.541 / Biol. Reprod / Absence of arms in the axoneme of immobile human spermatozoa by Pedersen (1975)
  49. 10.1038/262494a0 / Nature / Absence of axonemal arms in nasal cilia in Kartagener’s syndrome by Pedersen (1976)
  50. 10.1038/345263a0 / Nature / Cytoplasmic dynein is localized to kinetochores during mitosis by Pfarr (1990)
  51. 10.1083/jcb.127.1.139 / J. Cell Biol / Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi by Plamann (1994)
  52. 10.1016/S0074-7696(08)62440-7 / Int. Rev. Cytol / ATPases in mitotic spindles by Pratt (1984)
  53. 10.1091/mbc.5.1.45 / Mol. Biol. Cell / A family of dynein genes in Drosophila melanogaster by Rasmusson (1994)
  54. {'key': '2023122621440514300_JOCES_108_5_1883C54', 'first-page': '406', 'article-title': 'The neighbor-joining method: a new method for reconstructing phylogenetic trees', 'volume': '4', 'author': 'Saitou', 'year': '1987', 'journal-title': 'Mol. Biol. Evol'} / Mol. Biol. Evol / The neighbor-joining method: a new method for reconstructing phylogenetic trees by Saitou (1987)
  55. {'key': '2023122621440514300_JOCES_108_5_1883C55', 'first-page': '514', 'article-title': 'Relative efficiencies of the Fitch-Margoliash, maximum-parsimony, maximum-likelihood, minimumevolution, and neighbor-joining methods of phylogenetic tree construction in obtaining the correct tree', 'volume': '6', 'author': 'Saitou', 'year': '1989', 'journal-title': 'Mol. Biol. Evol'} / Mol. Biol. Evol / Relative efficiencies of the Fitch-Margoliash, maximum-parsimony, maximum-likelihood, minimumevolution, and neighbor-joining methods of phylogenetic tree construction in obtaining the correct tree by Saitou (1989)
  56. {'key': '2023122621440514300_JOCES_108_5_1883C56', 'volume-title': 'Molecular Cloning: a Laboratory Manual', 'author': 'Sambrook', 'year': '1989'} / Molecular Cloning: a Laboratory Manual by Sambrook (1989)
  57. 10.1073/pnas.86.5.1548 / Proc. Nat. Acad. Sci. USA / Dynein is the motor for retrograde axonal transport of organelles by Schnapp (1989)
  58. 10.1016/0092-8674(89)90627-2 / Cell / Cytoplasmic dynein is a minus end-directed motor for membranous organelles by Schroer (1989)
  59. 10.1083/jcb.127.1.187 / J. Cell Biol / A novel microtubule-based motor protein (KIF4) for organelle transports whose expression is regulated developmentally by Sekine (1994)
  60. {'key': '2023122621440514300_JOCES_108_5_1883C60', 'first-page': '1409', 'article-title': 'A statistical method for evaluating systematic relationships', 'volume': '28', 'author': 'Sokal', 'year': '1958', 'journal-title': 'University of Kansas Sci. Bull'} / University of Kansas Sci. Bull / A statistical method for evaluating systematic relationships by Sokal (1958)
  61. 10.1038/345266a0 / Nature / Localization of cytoplasmic dynein to mitotic spindles and kinetochores by Steuer (1990)
  62. 10.1093/nar/22.22.4673 / Nucl. Acids Res / CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice by Thompson (1994)
  63. {'key': '2023122621440514300_JOCES_108_5_1883C63', 'first-page': '341', 'article-title': 'Ultrastructure of respiratory cilia of WIC-Hyd male rats', 'volume': '138', 'author': 'Torikata', 'year': '1991', 'journal-title': 'Am. J. Pathol'} / Am. J. Pathol / Ultrastructure of respiratory cilia of WIC-Hyd male rats by Torikata (1991)
  64. 10.1083/jcb.123.4.849 / J. Cell Biol / Cytoplasmic dynein plays a role in mammalian mitotic spindle formation by Vaisberg (1993)
  65. {'key': '2023122621440514300_JOCES_108_5_1883C65', 'first-page': '285a', 'article-title': 'Three isoforms of dynein heavy chain expressed in human cells', 'volume': '5', 'author': 'Vaisberg', 'year': '1994', 'journal-title': 'Mol. Biol. Cell (suppl'} / Mol. Biol. Cell (suppl / Three isoforms of dynein heavy chain expressed in human cells by Vaisberg (1994)
  66. 10.1073/pnas.90.19.8769 / Proc. Nat. Acad. Sci. USA / Molecular analysis of the microtubule motor dynein by Vallee (1993)
  67. 10.1083/jcb.126.1.175 / J. Cell Biol / The Chlamydomonas FLA10 gene encodes a novel kinesin-homologous protein by Walther (1994)
  68. 10.1242/jcs.107.3.497 / J. Cell Sci / Molecular analysis of the γ heavy chain of Chlamydomonas flagellar outer-arm dynein by Wilkerson (1994)
  69. 10.1016/0955-0674(92)90061-G / Curr. Opin. Cell. Biol / Axonemal dyneins by Witman (1992)
  70. 10.1073/pnas.91.6.2100 / Proc. Nat. Acad. Sci. USA / Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans by Xiang (1994)
  71. 10.1073/pnas.90.17.7928 / Proc. Nat. Acad. Sci. USA / The primary structure of rat brain (cytoplasmic) dynein heavy chain, a cytoplasmic motor enzyme by Zhang (1993)
Dates
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Created 4 years, 4 months ago (April 23, 2021, 10:35 p.m.)
Deposited 1 year, 8 months ago (Dec. 26, 2023, 4:44 p.m.)
Indexed 1 year, 1 month ago (July 26, 2024, 10:15 p.m.)
Issued 30 years, 4 months ago (May 1, 1995)
Published 30 years, 4 months ago (May 1, 1995)
Published Online 30 years, 4 months ago (May 1, 1995)
Published Print 30 years, 4 months ago (May 1, 1995)
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@article{Tanaka_1995, title={Identification and molecular evolution of new dynein-like protein sequences in rat brain}, volume={108}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.108.5.1883}, DOI={10.1242/jcs.108.5.1883}, number={5}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Tanaka, Yosuke and Zhang, Zhizeng and Hirokawa, Nobutaka}, year={1995}, month=may, pages={1883–1893} }