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PMID: 6538572 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Purification and characterization of oocyte cytoplasmic tubulin and meiotic spindle tubulin of the surf clam Spisula solidissima.

The Journal of cell biology ·Vol. 98 ·No. 1 ·1984-01-00 ·Pages 253-66

Suprenant KA, Rebhun LI

Abstract

Assembly-competent tubulin was purified from the cytoplasm of unfertilized and parthogenetically activated oocytes, and from isolated meiotic spindles of the surf clam, Spisula solidissima. At 22 degrees C or 37 degrees C, Spisula tubulin assembled into 48-51-nm macrotubules during the first cycle of polymerization and 25-nm microtubules during the third and subsequent cycles of assembly. Macrotubules were formed from sheets of 26-27 protofilaments helically arranged at a 36 degree angle relative to the long axis of the polymer and were composed of alpha and beta tubulins and several other proteins ranging in molecular weight from 30,000 to 270,000. Third cycle microtubules contained 14-15 protofilaments in cross-section and were composed of greater than 95% alpha and beta tubulins. After three cycles of polymerization at 37 degrees C, unfertilized and activated oocyte tubulin self-assembled into microtubules at a critical concentration (Ccr) of 0.09 mg/ml. At the physiological temperature of 22 degrees C, unfertilized oocyte tubulin assembled into microtubules at a Ccr of 0.36 mg/ml, activated oocyte tubulin assembled at a Ccr of 0.42 mg/ml, and isolated meiotic spindle tubulin assembled at a Ccr of 0.33 mg/ml. The isoelectric points of tubulin from both unfertilized oocytes and isolated meiotic spindles were 5.8 for alpha tubulin and 5.6 for beta tubulin. In addition, one dimensional peptide maps of oocyte and spindle alpha and beta tubulins were very similar, if not identical. These results indicate that unfertilized oocyte tubulin and tubulin isolated from the first meiotic spindle are indistinguishable on the basis of assembly properties, isoelectric focusing, and one dimensional peptide mapping. These results suggest that the transition of tubulin from the quiescent oocyte state to that competent to form spindle microtubules in vivo does not require special modification of tubulin but may involve changes in the availability of microtubule organizing centers or assembly-promoting microtubule-associated proteins.

MeSH Terms
Animals Bivalvia Cytoplasm/analysis Female Isoelectric Point Meiosis Microscopy, Electron Microtubule-Associated Proteins Microtubules/ultrastructure Molecular Weight Oocytes/analysis Peptide Fragments/analysis Protein Binding Proteins/analysis Spindle Apparatus/analysis Tubulin/isolation & purification
Chemicals
Microtubule-Associated Proteins Peptide Fragments Proteins Tubulin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Suprenant K A
Rebhun L I
References (57)
57 references, click to expand
  1. Studies on the microtubules in heliozoa. V. Factors controlling the organization of microtubules in the Axonemal pattern in Echinosphaerium (Actinosphaerium) nucleofilum.
    J Cell Biol. 1969 Oct;43(1):148-65 PMID: 5824062
  2. Augmentation and dispersion of the in vivo mitotic apparatus of living marine eggs.
    Protoplasma. 1969;68(1):1-22 PMID: 5346998
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane.
    Biochemistry. 1971 Jun 22;10(13):2606-17 PMID: 4326772
  5. Changes in the organization of tubulin during meiosis in the eggs of the surf clam, Spisula solidissima.
    J Cell Biol. 1972 Aug;54(2):266-78 PMID: 4557309
  6. Delineation by lanthanum staining of filamentous elements associated with the surfaces of axonal microtubules.
    J Cell Sci. 1973 Mar;12(2):567-83 PMID: 4122255
  7. Microtubule assembly in the absence of added nucleotides.
    Proc Natl Acad Sci U S A. 1973 Mar;70(3):765-8 PMID: 4514990
  8. Vinblastine-induced paracrystals and unusually large microtubules (macrotubules) in rat renal cells.
    Z Zellforsch Mikrosk Anat. 1973 Aug 14;141(4):443-58 PMID: 4355873
  9. Tubulin determination by an isotope dilution-vinblastine precipitation method. The tubulin content of Spisula eggs and embryos.
    J Cell Biol. 1973 Dec;59(3):755-62 PMID: 4586678
  10. Microtubule surface lattice and subunit structure and observations on reassembly.
    J Cell Biol. 1974 Jan;60(1):153-67 PMID: 4855592
  11. Microtubule biogenesis and cell shape in Ochromonas. 3. Effects of herbicidal mitotic inhibitor isopropyl N-phenylcarbamate on shape and flagellum regeneration.
    J Cell Biol. 1974 May;61(2):514-36 PMID: 4827911
  12. Arrangement of subunits in flagellar microtubules.
    J Cell Sci. 1974 May;14(3):523-49 PMID: 4830832
  13. In vitro polymerization of microtubules into asters and spindles in homogenates of surf clam eggs.
    J Cell Biol. 1975 Jan;64(1):146-58 PMID: 45844
  14. Microtubules with 15 subunits in cockroach epidermal cells.
    J Cell Biol. 1975 Jan;64(1):242-5 PMID: 1109233
  15. Turbidimetric studies of the in vitro assembly and disassembly of porcine neurotubules.
    J Mol Biol. 1974 Nov 15;89(4):737-55 PMID: 4475698
  16. Microtubules: evidence for 13 protofilaments.
    J Cell Biol. 1973 Nov;59(2 Pt 1):267-75 PMID: 4805001
  17. High resolution two-dimensional electrophoresis of proteins.
    J Biol Chem. 1975 May 25;250(10):4007-21 PMID: 236308
  18. Tannic acid-stained microtubules with 12, 13, and 15 protofilaments.
    J Cell Biol. 1975 Apr;65(1):227-33 PMID: 47861
  19. Ultrastructural localization of the high molecular weight proteins associated with in vitro-assembled brain microtubules.
    J Cell Biol. 1975 Apr;65(1):237-41 PMID: 1127013
  20. Ionic and nucleotide requirements for microtubule polymerization in vitro.
    Biochemistry. 1975 Jul;14(13):2996-3005 PMID: 238580
  21. On macrotubule structure.
    J Mol Biol. 1975 Mar 25;93(1):117-20 PMID: 1152046
  22. A protein factor essential for microtubule assembly.
    Proc Natl Acad Sci U S A. 1975 May;72(5):1858-62 PMID: 1057175
  23. Association of high-molecular-weight proteins with microtubules and their role in microtubule assembly in vitro.
    Proc Natl Acad Sci U S A. 1975 Jul;72(7):2696-700 PMID: 1058484
  24. Inhibition of tubulin assembly by RNA and other polyanions: evidence for a required protein.
    Proc Natl Acad Sci U S A. 1975 Sep;72(9):3570-4 PMID: 1059144
  25. The equilibrium assembly of microtubules in vitro.
    Soc Gen Physiol Ser. 1975;30:119-41 PMID: 242078
  26. Assay of proteins in the presence of interfering materials.
    Anal Biochem. 1976 Jan;70(1):241-50 PMID: 1259145
  27. Induction of a sheet polymer of tubulin by Zn2+.
    Exp Cell Res. 1976 Jun;100(1):104-10 PMID: 945172
  28. Microtubule-macrotubule transformations induced by volatile anesthetics. Mechanism of macrotubule assembly.
    J Ultrastruct Res. 1976 Dec;57(3):237-50 PMID: 63568
  29. Effects of RNase and RNA on in vitro aster assembly.
    J Supramol Struct. 1976;5(4):577(429)589(441) PMID: 1027923
  30. In vitro polymerization of marine egg tubulin into microtubules.
    J Biochem. 1977 Apr;81(4):1115-25 PMID: 195935
  31. Zinc ion-induced assembly of tubulin.
    J Biol Chem. 1977 Oct 10;252(19):6918-24 PMID: 893451
  32. Alterations in number of protofilaments in microtubules assembled in vitro.
    J Cell Biol. 1978 Jan;76(1):223-8 PMID: 618894
  33. In vitro assembly of dogfish brain tubulin and the induction of coiled ribbon polymers by calcium.
    Exp Cell Res. 1978 Jan;111(1):139-51 PMID: 563794
  34. Nucleation of microtubules in vitro by isolated spindle pole bodies of the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1978 Aug;78(2):401-14 PMID: 357437
  35. Macrotubules induced by halothane: in vitro assembly.
    J Cell Sci. 1978 Aug;32:99-108 PMID: 701408
  36. The in vitro assembly of flagellar outer doublet tubulin.
    J Cell Biol. 1978 Nov;79(2 Pt 1):500-15 PMID: 569158
  37. The visualization of actin filament polarity in thin sections. Evidence for the uniform polarity of membrane-associated filaments.
    J Cell Biol. 1978 Dec;79(3):846-52 PMID: 569662
  38. Separation of tubulin from microtubule-associated proteins on phosphocellulose. Accompanying alterations in concentrations of buffer components.
    Biochemistry. 1979 Jun 12;18(12):2499-503 PMID: 444471
  39. The periodic association of MAP2 with brain microtubules in vitro.
    J Cell Biol. 1979 Feb;80(2):266-76 PMID: 457745
  40. Cell cycle-dependent, in vitro assembly of microtubules onto pericentriolar material of HeLa cells.
    J Cell Biol. 1979 Jun;81(3):484-97 PMID: 457772
  41. Interaction of microtubule proteins with phospholipid vesicles.
    J Cell Biol. 1979 Jun;81(3):665-71 PMID: 457778
  42. Microtubule initiation at kinetochores and centrosomes in lysed mitotic cells. Inhibition of site-specific nucleation by tubulin antibody.
    J Cell Biol. 1979 Aug;82(2):585-91 PMID: 479317
  43. Identification of microtubule-associated proteins in the meiotic spindle of surf clam oocytes.
    J Cell Biol. 1980 Feb;84(2):235-45 PMID: 7189754
  44. Structure and phosphorylation of microtubule-associated protein 2 (MAP 2).
    Proc Natl Acad Sci U S A. 1980 Jun;77(6):3206-10 PMID: 6251448
  45. Arrangement of subunits in microtubules with 14 profilaments.
    J Cell Biol. 1980 NOV;87(2 Pt 1):521-6 PMID: 7430256
  46. Ultrasensitive stain for proteins in polyacrylamide gels shows regional variation in cerebrospinal fluid proteins.
    Science. 1981 Mar 27;211(4489):1437-8 PMID: 6162199
  47. Analysis of microtubule polymerization inhibitors in sea urchin egg extracts: evidence for a protease.
    Arch Biochem Biophys. 1981 Mar;207(1):75-80 PMID: 7016037
  48. Interaction of tubulin with phospholipid vesicles. I. Association with vesicles at the phase transition.
    J Biol Chem. 1981 Jun 10;256(11):5879-85 PMID: 6894593
  49. Purification of yeast tubulin by self-assembly in vitro.
    Biochemistry. 1981 Jun 9;20(12):3629-33 PMID: 7020758
  50. Chemical differences distinguish ciliary membrane and axonemal tubulins.
    Biochemistry. 1981 Aug 4;20(16):4716-23 PMID: 7295643
  51. Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans.
    J Cell Biol. 1982 Apr;93(1):15-23 PMID: 7068753
  52. Control of the structural fidelity of microtubules by initiation sites.
    J Mol Biol. 1982 Jan 25;154(3):485-500 PMID: 7077667
  53. Strongylocentrotus purpuratus spindle tubulin. I. Characteristics of its polymerization and depolymerization in vitro.
    J Cell Biol. 1982 Jun;93(3):788-96 PMID: 7119002
  54. Strongylocentrotus purpuratus spindle tubulin. II. Characteristics of its sensitivity to Ca++ and the effects of calmodulin isolated from bovine brain and S. purpuratus eggs.
    J Cell Biol. 1982 Jun;93(3):797-803 PMID: 7119003
  55. Assembly of unfertilized sea urchin egg tubulin at physiological temperatures.
    J Biol Chem. 1983 Apr 10;258(7):4518-25 PMID: 6833265
  56. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  57. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY.
    J Cell Biol. 1965 May;25:407-8 PMID: 14287192
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1984-01-00
Pages
253-66
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2113012
Subset
IM
Grants
NIGMS NIH HHS · 1R01 GM 26784 · United States
NHLBI NIH HHS · 5-32HB07192 · United States
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