Home LiteratureArticle Details
PMID: 12847082 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.

A subunit of the dynein regulatory complex in Chlamydomonas is a homologue of a growth arrest-specific gene product.

The Journal of cell biology ·Vol. 162 ·No. 1 ·2003-07-07 ·Pages 47-57

Rupp G, Porter ME

Abstract

The dynein regulatory complex (DRC) is an important intermediate in the pathway that regulates flagellar motility. To identify subunits of the DRC, we characterized a Chlamydomonas motility mutant obtained by insertional mutagenesis. The pf2-4 mutant displays an altered waveform that results in slow swimming cells. EM analysis reveals defects in DRC structure that can be rescued by reintroduction of the wild-type PF2 gene. Immunolocalization studies show that the PF2 protein is distributed along the length of the axoneme, where it is part of a discrete complex of polypeptides. PF2 is a coiled-coil protein that shares significant homology with a mammalian growth arrest-specific gene product (Gas11/Gas8) and a trypanosome protein known as trypanin. PF2 and its homologues appear to be universal components of motile axonemes that are required for DRC assembly and the regulation of flagellar motility. The expression of Gas8/Gas11 transcripts in a wide range of tissues may also indicate a potential role for PF2-related proteins in other microtubule-based structures.

MeSH Terms
Animals Cell Movement/genetics Chlamydomonas/genetics,metabolism,ultrastructure Cytoskeletal Proteins DNA, Complementary/analysis,genetics Dyneins/metabolism Flagella/genetics,metabolism,ultrastructure Macromolecular Substances Molecular Sequence Data Mutation/genetics Neoplasm Proteins/genetics,isolation & purification Paralysis/genetics Protein Structure, Quaternary/genetics Proteins/genetics,isolation & purification Protozoan Proteins/genetics,isolation & purification,metabolism Sequence Homology, Amino Acid Sequence Homology, Nucleic Acid
Chemicals
Cytoskeletal Proteins DNA, Complementary GAS8 protein, human Gas8 protein, mouse Macromolecular Substances Neoplasm Proteins Proteins Protozoan Proteins T lymphocyte triggering factor, Trypanosoma brucei Dyneins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Rupp Gerald
Department of Genetics, Cell Biology, and Development, University of Minnesota Medical School, 6-160 Jackson Hall, 321 Church Street SE, Minneapolis, MN 55455, USA.
Porter Mary E
References (59)
59 references, click to expand
  1. Studies on the eel sperm flagellum. I. The structure of the inner dynein arm complex.
    J Cell Sci. 1997 Jan;110 ( Pt 1):85-94 PMID: 9010787
  2. The gene for a T lymphocyte triggering factor from African trypanosomes.
    J Exp Med. 1997 Aug 4;186(3):433-8 PMID: 9236195
  3. Characterization and screening for mutations of the growth arrest-specific 11 (GAS11) and C16orf3 genes at 16q24.3 in breast cancer.
    Genomics. 1998 Sep 15;52(3):325-31 PMID: 9790751
  4. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein.
    Cell. 1998 Dec 11;95(6):829-37 PMID: 9865700
  5. Rotation of the central pair microtubules in eukaryotic flagella.
    Mol Biol Cell. 1999 Jan;10(1):1-4 PMID: 9880321
  6. A novel protein targeting domain directs proteins to the anterior cytoplasmic face of the flagellar pocket in African trypanosomes.
    J Cell Sci. 1999 Sep;112 Pt 18:3091-101 PMID: 10462525
  7. Protein phosphatases PP1 and PP2A are located in distinct positions in the Chlamydomonas flagellar axoneme.
    J Cell Sci. 2000 Jan;113 ( Pt 1):91-102 PMID: 10591628
  8. Molecular motors: the driving force behind mammalian left-right development.
    Trends Cell Biol. 2000 Feb;10(2):41-5 PMID: 10652513
  9. Casein kinase I is anchored on axonemal doublet microtubules and regulates flagellar dynein phosphorylation and activity.
    J Biol Chem. 2000 Jun 23;275(25):18905-12 PMID: 10858448
  10. The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility.
    J Cell Biol. 2000 Nov 27;151(5):F37-42 PMID: 11086017
  11. T lymphocyte-triggering factor of african trypanosomes is associated with the flagellar fraction of the cytoskeleton and represents a new family of proteins that are present in several divergent eukaryotes.
    J Biol Chem. 2000 Dec 15;275(50):39369-78 PMID: 10969087
  12. The Chlamydomonas PF6 locus encodes a large alanine/proline-rich polypeptide that is required for assembly of a central pair projection and regulates flagellar motility.
    Mol Biol Cell. 2001 Mar;12(3):739-51 PMID: 11251084
  13. Flagellar radial spoke protein 3 is an A-kinase anchoring protein (AKAP).
    J Cell Biol. 2001 Apr 16;153(2):443-8 PMID: 11309423
  14. Isolation and properties of Gas8, a growth arrest-specific gene regulated during male gametogenesis to produce a protein associated with the sperm motility apparatus.
    J Biol Chem. 2002 Feb 22;277(8):6311-7 PMID: 11751847
  15. Trypanin is a cytoskeletal linker protein and is required for cell motility in African trypanosomes.
    J Cell Biol. 2002 Mar 4;156(5):867-77 PMID: 11864997
  16. Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6.
    Mol Cell Biol. 2002 Sep;22(17):6298-305 PMID: 12167721
  17. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants.
    Int Rev Cytol. 2002;219:115-55 PMID: 12211628
  18. Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase.
    Mol Biol Cell. 2002 Sep;13(9):3303-13 PMID: 12221134
  19. Intraflagellar transport and cilia-dependent diseases.
    Trends Cell Biol. 2002 Dec;12(12):551-5 PMID: 12495842
  20. The vertebrate primary cilium is a sensory organelle.
    Curr Opin Cell Biol. 2003 Feb;15(1):105-10 PMID: 12517711
  21. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells.
    Nat Genet. 2003 Feb;33(2):129-37 PMID: 12514735
  22. A novel dynein light intermediate chain colocalizes with the retrograde motor for intraflagellar transport at sites of axoneme assembly in chlamydomonas and Mammalian cells.
    Mol Biol Cell. 2003 May;14(5):2041-56 PMID: 12802074
  23. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  24. Direction of active sliding of microtubules in Tetrahymena cilia.
    Proc Natl Acad Sci U S A. 1977 May;74(5):2045-9 PMID: 266725
  25. Chlamydomonas flagellar mutants lacking radial spokes and central tubules. Structure, composition, and function of specific axonemal components.
    J Cell Biol. 1978 Mar;76(3):729-47 PMID: 632325
  26. The pair of central tubules rotates during ciliary beat in Paramecium.
    Nature. 1979 Jun 7;279(5713):532-4 PMID: 450097
  27. Centriole deciliation associated with the early response of 3T3 cells to growth factors but not to SV40.
    Cell. 1979 Dec;18(4):1065-72 PMID: 229969
  28. Radial spokes of Chlamydomonas flagella: polypeptide composition and phosphorylation of stalk components.
    J Cell Biol. 1981 Jan;88(1):73-9 PMID: 6451632
  29. Suppressor mutations in Chlamydomonas reveal a regulatory mechanism for Flagellar function.
    Cell. 1982 Jan;28(1):115-24 PMID: 6461414
  30. Regulation of the synthesis and assembly of ciliary and flagellar proteins during regeneration.
    Annu Rev Cell Biol. 1986;2:517-46 PMID: 3548775
  31. Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function.
    Cell Motil Cytoskeleton. 1987;8(1):68-75 PMID: 2958145
  32. Direction of force generated by the inner row of dynein arms on flagellar microtubules.
    J Cell Biol. 1987 Oct;105(4):1781-7 PMID: 2959667
  33. Analysis of mammalian cell genetic regulation in situ by using retrovirus-derived "portable exons" carrying the Escherichia coli lacZ gene.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5517-21 PMID: 2501787
  34. Isolation and characterization of the nitrate reductase structural gene of Chlamydomonas reinhardtii.
    Proc Natl Acad Sci U S A. 1989 Sep;86(17):6449-53 PMID: 2475871
  35. The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus.
    EMBO J. 1989 Oct;8(10):2803-9 PMID: 2583083
  36. The Mr 78,000 intermediate chain of Chlamydomonas outer arm dynein interacts with alpha-tubulin in situ.
    J Biol Chem. 1991 May 5;266(13):8401-7 PMID: 1827120
  37. cAMP-stimulated phosphorylation of an axonemal polypeptide that copurifies with the 22S dynein arm regulates microtubule translocation velocity and swimming speed in Paramecium.
    Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):7918-22 PMID: 1654550
  38. The inner dynein arm complex: compatible images from freeze-etch and thin section methods of microscopy.
    J Cell Sci. 1991 Oct;100 ( Pt 2):319-28 PMID: 1836791
  39. Arrangement of inner dynein arms in wild-type and mutant flagella of Chlamydomonas.
    J Cell Biol. 1992 Sep;118(5):1145-62 PMID: 1387403
  40. Extragenic suppressors of paralyzed flagellar mutations in Chlamydomonas reinhardtii identify loci that alter the inner dynein arms.
    J Cell Biol. 1992 Sep;118(5):1163-76 PMID: 1387404
  41. The inner dynein arms I2 interact with a "dynein regulatory complex" in Chlamydomonas flagella.
    J Cell Biol. 1992 Sep;118(6):1455-63 PMID: 1387875
  42. Regulation of dynein-driven microtubule sliding by the radial spokes in flagella.
    Science. 1992 Sep 11;257(5076):1557-9 PMID: 1387971
  43. Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging.
    Genetics. 1993 Jul;134(3):737-47 PMID: 8394263
  44. Cloning of flagellar genes in Chlamydomonas reinhardtii by DNA insertional mutagenesis.
    Genetics. 1993 Oct;135(2):375-84 PMID: 8244002
  45. Mutations in the "dynein regulatory complex" alter the ATP-insensitive binding sites for inner arm dyneins in Chlamydomonas axonemes.
    J Cell Biol. 1994 Jun;125(5):1109-17 PMID: 8195292
  46. The CRY1 gene in Chlamydomonas reinhardtii: structure and use as a dominant selectable marker for nuclear transformation.
    Mol Cell Biol. 1994 Jun;14(6):4011-9 PMID: 8196640
  47. Role of cAMP in the reactivation of demembranated ram spermatozoa.
    Cell Motil Cytoskeleton. 1994;27(3):206-18 PMID: 8020107
  48. Mutations in the SUP-PF-1 locus of Chlamydomonas reinhardtii identify a regulatory domain in the beta-dynein heavy chain.
    J Cell Biol. 1994 Sep;126(6):1495-507 PMID: 8089181
  49. Components of a "dynein regulatory complex" are located at the junction between the radial spokes and the dynein arms in Chlamydomonas flagella.
    J Cell Biol. 1994 Dec;127(5):1311-25 PMID: 7962092
  50. Immunofluorescence microscopy of cilia and flagella.
    Methods Cell Biol. 1995;47:163-9 PMID: 7476482
  51. Computer-assisted analysis of flagellar structure.
    Methods Cell Biol. 1995;47:183-91 PMID: 7476486
  52. Role of cilia in human health.
    Cell Motil Cytoskeleton. 1995;32(2):95-7 PMID: 8681401
  53. The platelet-derived growth factor alpha-receptor is encoded by a growth-arrest-specific (gas) gene.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4617-22 PMID: 8643452
  54. The dynein gene family in Chlamydomonas reinhardtii.
    Genetics. 1996 Oct;144(2):569-85 PMID: 8889521
  55. Expression of primary cilia in mammalian cells.
    Cell Biol Int. 1996 Jan;20(1):73-81 PMID: 8936410
  56. The sup-pf-2 mutations of Chlamydomonas alter the activity of the outer dynein arms by modification of the gamma-dynein heavy chain.
    J Cell Biol. 1996 Dec;135(6 Pt 2):1853-65 PMID: 8991096
  57. Regulation of flagellar dynein by phosphorylation of a 138-kD inner arm dynein intermediate chain.
    J Cell Biol. 1997 Jan 13;136(1):167-76 PMID: 9008711
  58. Phosphoregulation of an inner dynein arm complex in Chlamydomonas reinhardtii is altered in phototactic mutant strains.
    J Cell Biol. 1997 Jan 13;136(1):177-91 PMID: 9008712
  59. Linkage maps in Chlamydomonas reinhardi.
    Genetics. 1962 May;47:531-43 PMID: 13889019
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.200303019
Published
2003-07-07
Pages
47-57
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2172716
Subset
IM
Grants
NIGMS NIH HHS · F32 GM017901 · United States
NCRR NIH HHS · RR 00592 · United States
NIGMS NIH HHS · GM 55667 · United States
NIGMS NIH HHS · R01 GM055667 · United States
NCRR NIH HHS · P41 RR000592 · United States
NIGMS NIH HHS · F32 GM 17901 · United States
NIGMS NIH HHS · R37 GM055667 · United States
External Links
PubMed source DOI: 10.1083/jcb.200303019 PMC Full Text View journal details
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: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2