Home LiteratureArticle Details
PMID: 8089180 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte.

The Journal of cell biology ·Vol. 126 ·No. 6 ·1994-09-00 ·Pages 1475-94

Li M, McGrail M, Serr M, Hays TS

Abstract

The unidirectional movements of the microtubule-associated motors, dyneins, and kinesins, provide an important mechanism for the positioning of cellular organelles and molecules. An intriguing possibility is that this mechanism may underlie the directed transport and asymmetric positioning of morphogens that influence the development of multicellular embryos. In this report, we characterize the Drosophila gene, Dhc64C, that encodes a cytoplasmic dynein heavy chain polypeptide. The primary structure of the Drosophila cytoplasmic dynein heavy chain polypeptide has been determined by the isolation and sequence analysis of overlapping cDNA clones. Drosophila cytoplasmic dynein is highly similar in sequence and structure to cytoplasmic dynein isoforms reported for other organisms. The Dhc64C dynein transcript is differentially expressed during development with the highest levels being detected in the ovaries of adult females. Within the developing egg chambers of the ovary, the dynein gene is predominantly transcribed in the nurse cell complex. In contrast, the encoded dynein motor protein displays a striking accumulation in the single cell that will develop as the oocyte. The temporal and spatial pattern of dynein accumulation in the oocyte is remarkably similar to that of several maternal effect gene products that are essential for oocyte differentiation and axis specification. This distribution and its disruption by specific maternal effect mutations lends support to recent models suggesting that microtubule motors participate in the transport of these morphogens from the nurse cell cytoplasm to the oocyte.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Cloning, Molecular Cytoplasm/metabolism DNA, Complementary/isolation & purification Drosophila/metabolism Dyneins/chemistry,genetics,metabolism,physiology Female Molecular Sequence Data Mutation Oocytes/metabolism RNA, Messenger/analysis Sequence Homology, Amino Acid Tissue Distribution
Chemicals
DNA, Complementary RNA, Messenger Dyneins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Li M
Department of Genetics and Cell Biology, University of Minnesota, St. Paul 55108-1095.
McGrail M
Serr M
Hays T S
References (94)
94 references, click to expand
  1. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase.
    Gene. 1988 Jul 15;67(1):31-40 PMID: 3047011
  2. Tropomyosin coiled-coil interactions: evidence for an unstaggered structure.
    J Mol Biol. 1975 Oct 25;98(2):293-304 PMID: 1195389
  3. The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo.
    EMBO J. 1988 Jun;7(6):1749-56 PMID: 2901954
  4. A cytoplasmic dynein heavy chain in sea urchin embryos.
    Biol Cell. 1992;76(3):303-9 PMID: 1305477
  5. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates.
    Nucleic Acids Res. 1987 Feb 25;15(4):1353-61 PMID: 3822832
  6. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  7. Structure, function and regulation of cytoplasmic dynein.
    Curr Opin Cell Biol. 1994 Feb;6(1):69-73 PMID: 8167028
  8. Bicaudal-D, a Drosophila gene involved in developmental asymmetry: localized transcript accumulation in ovaries and sequence similarity to myosin heavy chain tail domains.
    Genes Dev. 1989 Dec;3(12A):1957-68 PMID: 2576013
  9. The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing.
    EMBO J. 1988 Feb;7(2):473-83 PMID: 3284745
  10. An investigation of microtubule organization and functions in living Drosophila embryos by injection of a fluorescently labeled antibody against tyrosinated alpha-tubulin.
    J Cell Biol. 1987 Oct;105(4):1721-30 PMID: 3117804
  11. Progression of the cell cycle through mitosis leads to abortion of nascent transcripts.
    Cell. 1991 Oct 18;67(2):303-10 PMID: 1680567
  12. The Drosophila cytoskeleton.
    Annu Rev Cell Biol. 1990;6:559-96 PMID: 2275822
  13. Multiple nucleotide-binding sites in the sequence of dynein beta heavy chain.
    Nature. 1991 Aug 15;352(6336):640-3 PMID: 1830927
  14. Vectors for Drosophila P-element-mediated transformation and tissue culture transfection.
    Gene. 1988 Dec 30;74(2):445-56 PMID: 3246353
  15. Cytoplasmic dynein is required for normal nuclear segregation in yeast.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11172-6 PMID: 8248224
  16. A central role for microtubules in the differentiation of Drosophila oocytes.
    Development. 1993 Aug;118(4):1169-80 PMID: 8269846
  17. Intercellular migration of centrioles in the germarium of Drosophila melanogaster. An electron microscopic study.
    J Cell Biol. 1970 May;45(2):306-20 PMID: 4327572
  18. Cellular roles of kinesin and related proteins.
    Curr Opin Cell Biol. 1994 Feb;6(1):63-8 PMID: 8167027
  19. Genetic analysis of the brahma gene of Drosophila melanogaster and polytene chromosome subdivisions 72AB.
    Genetics. 1994 Jul;137(3):803-13 PMID: 7916308
  20. Motor proteins for cytoplasmic microtubules.
    Curr Opin Cell Biol. 1992 Feb;4(1):66-73 PMID: 1532721
  21. A family of dynein genes in Drosophila melanogaster.
    Mol Biol Cell. 1994 Jan;5(1):45-55 PMID: 8186464
  22. Motor proteins of cytoplasmic microtubules.
    Annu Rev Biochem. 1990;59:909-32 PMID: 2142876
  23. The origin of pattern and polarity in the Drosophila embryo.
    Cell. 1992 Jan 24;68(2):201-19 PMID: 1733499
  24. The arflike gene encodes an essential GTP-binding protein in Drosophila.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3120-4 PMID: 1901655
  25. RNA on the move: the mRNA localization pathway.
    J Cell Biol. 1993 Oct;123(2):269-74 PMID: 8408211
  26. Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology.
    Genetics. 1991 Dec;129(4):1119-36 PMID: 1783295
  27. Isolation and mapping of a cloned ribosomal protein gene of Drosophila melanogaster.
    Nature. 1980 Jun 26;285(5767):674-6 PMID: 6771656
  28. The involvement of the Notch locus in Drosophila oogenesis.
    Development. 1992 Aug;115(4):913-22 PMID: 1451667
  29. Molecular analysis of the microtubule motor dynein.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8769-72 PMID: 8415604
  30. The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos.
    Development. 1992 May;115(1):75-88 PMID: 1638994
  31. Cytoplasmic microtubule-associated motors.
    Annu Rev Biochem. 1993;62:429-51 PMID: 8352594
  32. oskar mRNA is localized to the posterior pole of the Drosophila oocyte.
    Cell. 1991 Jul 12;66(1):23-35 PMID: 2070416
  33. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos.
    Cell. 1991 Jul 12;66(1):37-50 PMID: 2070417
  34. Molecular cloning and nucleotide sequence of the gene for Escherichia coli leucyl-tRNA synthetase.
    Nucleic Acids Res. 1987 Dec 23;15(24):10199-210 PMID: 3320963
  35. chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis.
    Cell. 1992 Apr 3;69(1):173-84 PMID: 1339308
  36. Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2100-4 PMID: 8134356
  37. Molecular analysis of the gamma heavy chain of Chlamydomonas flagellar outer-arm dynein.
    J Cell Sci. 1994 Mar;107 ( Pt 3):497-506 PMID: 7516341
  38. Properties of Commelina yellow mottle virus's complete DNA sequence, genomic discontinuities and transcript suggest that it is a pararetrovirus.
    Nucleic Acids Res. 1990 Sep 25;18(18):5505-13 PMID: 1699203
  39. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  40. Functional cDNA libraries from Drosophila embryos.
    J Mol Biol. 1988 Sep 20;203(2):425-37 PMID: 3199441
  41. Characterization of the ATP-sensitive binding of Tetrahymena 30 S dynein to bovine brain microtubules.
    J Biol Chem. 1983 May 25;258(10):6575-81 PMID: 6222046
  42. Enzymes for microtubule-dependent motility.
    J Biol Chem. 1989 Apr 15;264(11):6001-4 PMID: 2522925
  43. Organization of the cytoskeleton in early Drosophila embryos.
    J Cell Biol. 1986 Apr;102(4):1494-509 PMID: 3514634
  44. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins.
    J Mol Biol. 1978 Mar 25;120(1):97-120 PMID: 642007
  45. Expression and function of Drosophila cyclin A during embryonic cell cycle progression.
    Cell. 1989 Mar 24;56(6):957-68 PMID: 2564316
  46. A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses.
    Cell. 1989 Mar 10;56(5):879-89 PMID: 2522352
  47. The primary structure of rat brain (cytoplasmic) dynein heavy chain, a cytoplasmic motor enzyme.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7928-32 PMID: 7690137
  48. A Chlamydomonas outer arm dynein mutant with a truncated beta heavy chain.
    J Cell Biol. 1993 Aug;122(3):653-61 PMID: 8335691
  49. The role of gene cassettes in axis formation during Drosophila oogenesis.
    Trends Genet. 1994 Mar;10(3):89-94 PMID: 8178370
  50. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter.
    Nucleic Acids Res. 1984 Sep 25;12(18):7035-56 PMID: 6091052
  51. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  52. A map of photolytic and tryptic cleavage sites on the beta heavy chain of dynein ATPase from sea urchin sperm flagella.
    J Cell Biol. 1988 May;106(5):1607-14 PMID: 2453517
  53. Evidence for a highly selective RNA transport system and its role in establishing the dorsoventral axis of the Drosophila egg.
    Development. 1992 Mar;114(3):653-61 PMID: 1377623
  54. How RNA polymerase II terminates transcription in higher eukaryotes.
    Trends Biochem Sci. 1989 Mar;14(3):105-10 PMID: 2658217
  55. Null alleles reveal novel requirements for Bic-D during Drosophila oogenesis and zygotic development.
    Development. 1994 May;120(5):1233-42 PMID: 8026332
  56. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport.
    Development. 1992 Aug;115(4):923-36 PMID: 1451668
  57. Identification of microtubule-associated proteins in the centrosome, spindle, and kinetochore of the early Drosophila embryo.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2977-91 PMID: 2574177
  58. Cytoplasmic dynein plays a role in mammalian mitotic spindle formation.
    J Cell Biol. 1993 Nov;123(4):849-58 PMID: 8227145
  59. Periodic features in the amino acid sequence of nematode myosin rod.
    J Mol Biol. 1983 Mar 15;164(4):605-26 PMID: 6341606
  60. Cytoplasmic microtubule-based motor proteins.
    Curr Opin Cell Biol. 1993 Feb;5(1):95-104 PMID: 8448036
  61. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis.
    J Cell Sci. 1983 May;61:31-70 PMID: 6411748
  62. Structure of the alpha and beta heavy chains of the outer arm dynein from Chlamydomonas flagella. Masses of chains and sites of ultraviolet-induced vanadate-dependent cleavage.
    J Biol Chem. 1987 Dec 25;262(36):17596-604 PMID: 2961738
  63. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2.
    Cell. 1992 Feb 7;68(3):561-72 PMID: 1346755
  64. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte.
    Curr Biol. 1994 Apr 1;4(4):289-300 PMID: 7922338
  65. A spring-loaded mechanism for the conformational change of influenza hemagglutinin.
    Cell. 1993 May 21;73(4):823-32 PMID: 8500173
  66. Dynein from Dictyostelium: primary structure comparisons between a cytoplasmic motor enzyme and flagellar dynein.
    J Cell Biol. 1992 Dec;119(6):1597-604 PMID: 1469051
  67. Sequence analysis of the Chlamydomonas alpha and beta dynein heavy chain genes.
    J Cell Sci. 1994 Mar;107 ( Pt 3):635-44 PMID: 8006077
  68. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  69. Localized RNAs and their functions.
    Bioessays. 1993 Oct;15(10):651-8 PMID: 7506023
  70. Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples.
    J Biol Chem. 1981 Dec 10;256(23):11955-7 PMID: 7028745
  71. Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila.
    Cell. 1991 Aug 9;66(3):433-49 PMID: 1907889
  72. Multiple effects of colchicine on oogenesis in Drosophila: induced sterility and switch of potential oocyte to nurse-cell developmental pathway.
    Cell Tissue Res. 1983;228(1):21-32 PMID: 6403242
  73. Nuclear elongation and cytokinesis in Drosophila montana.
    Dev Biol. 1971 Dec;26(4):560-77 PMID: 5167431
  74. With apologies to scheherazade: tails of 1001 kinesin motors.
    Annu Rev Genet. 1993;27:319-51 PMID: 8122906
  75. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998-9002 PMID: 2461560
  76. Scanning electron microscopy of Drosophila embryogenesis. 1. The structure of the egg envelopes and the formation of the cellular blastoderm.
    Dev Biol. 1976 May;50(1):95-108 PMID: 817949
  77. Molecular cloning of the retrograde transport motor cytoplasmic dynein (MAP 1C).
    Neuron. 1993 May;10(5):787-96 PMID: 7684232
  78. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback.
    Chromosoma. 1989 Aug;98(2):81-5 PMID: 2476281
  79. Structure of the alpha and beta heavy chains of the outer arm dynein from Chlamydomonas flagella. Location of epitopes and protease-sensitive sites.
    J Biol Chem. 1988 Jul 5;263(19):9244-55 PMID: 2454234
  80. Dynamic changes in microtubule configuration correlate with nuclear migration in the preblastoderm Drosophila embryo.
    J Cell Biol. 1993 Jul;122(1):113-21 PMID: 8314839
  81. A cytoplasmic dynein motor in Drosophila: identification and localization during embryogenesis.
    J Cell Sci. 1994 Jun;107 ( Pt 6):1557-69 PMID: 7962198
  82. Nuclear gene for mitochondrial leucyl-tRNA synthetase of Neurospora crassa: isolation, sequence, chromosomal mapping, and evidence that the leu-5 locus specifies structural information.
    Mol Cell Biol. 1989 Nov;9(11):4631-44 PMID: 2574823
  83. Disruption of mitotic spindle orientation in a yeast dynein mutant.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10096-100 PMID: 8234262
  84. The kinesin superfamily: tails of functional redundancy.
    Trends Cell Biol. 1991 Oct;1(4):93-8 PMID: 14731795
  85. Molecular movements in oocyte patterning and pole cell differentiation.
    Bioessays. 1992 Aug;14(8):507-12 PMID: 1365903
  86. Sequence identification of 2,375 human brain genes.
    Nature. 1992 Feb 13;355(6361):632-4 PMID: 1538749
  87. Unidirectional digestion with exonuclease III in DNA sequence analysis.
    Methods Enzymol. 1987;155:156-65 PMID: 3323819
  88. cappuccino and spire: two unique maternal-effect loci required for both the anteroposterior and dorsoventral patterns of the Drosophila embryo.
    Genes Dev. 1989 Sep;3(9):1437-52 PMID: 2514120
  89. Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis.
    Development. 1991 Sep;113(1):55-66 PMID: 1684934
  90. Staufen, a gene required to localize maternal RNAs in the Drosophila egg.
    Cell. 1991 Jul 12;66(1):51-63 PMID: 1712672
  91. Preparative and analytical purification of DNA from agarose.
    Proc Natl Acad Sci U S A. 1979 Feb;76(2):615-9 PMID: 284385
  92. Structure of the tubulin dimer.
    J Biol Chem. 1977 Oct 25;252(20):7006-14 PMID: 561780
  93. Predicting coiled coils from protein sequences.
    Science. 1991 May 24;252(5009):1162-4 PMID: 2031185
  94. Complementary DNA sequencing: expressed sequence tags and human genome project.
    Science. 1991 Jun 21;252(5013):1651-6 PMID: 2047873
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-09-00
Pages
1475-94
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2290959
Subset
IM
Grants
NIGMS NIH HHS · GM-44757 · United States
Databases
GENBANK
L23195
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com