DOI: 10.1242/jcs.96.4.571. The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy

The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy

10.1242/jcs.96.4.571

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

ABSTRACT Microtubules (MTs) are dynamic polymers that can exist in phases of elongation and rapid-shortening at steady-state. These phases have been observed in vitro and in living cells, and this property of MTs has been termed ‘dynamic instability’. The purpose of this study was to use negative-stain electron microscopy (EM) to test if there are structural differences between the ends of MTs in the elongation and shortening phases, which could provide insight into the mechanisms of dynamic instability. MTs in the elongation phase were obtained by seeding either highly purified porcine brain tubulin (PC-tubulin) or tubulin containing microtubule-associated proteins (MTP), from isolated Tetrahymena axonemes. The results are that, in addition to intact cylindrical MTs, a significant fraction of the tubulin polymer in the elongation phase occurred as sheets of parallel protofilaments, as found in previous investigations with setf-assembled MTs. Therefore, sheet formation is an intrinsic property of MT assembly that does not depend on the tubulin purity or the method of nucleation. Also, since sheets lack helical symmetry, at least a fraction of tubulin polymers seeded from axonemes did not assemble by helical addition of tubulin dimers to the ends, an assumption often made in mathematical models of dynamic instability. Sheets and intact MTs that were seeded from isolated axonemes, emanated both from the intact MT wall of the axoneme A-subfiber and from the incomplete wall of the B-subfiber. Therefore, axoneme seeds do not provide a homogeneous nucleation site for tubulin growth, or produce a homogeneous population of tubulin polymers under our conditions. Previous evidence has indicated that MT disassembly can occur by a segmental release of tubulin oligomers from the ends and at sites along the length of MTs. However, these studies were performed with MTP, and disassembly was induced by cold depolymerization. We examined MT shortening under conditions that closely represent shortening via dynamic instability, namely isothermal dilution at 37 °C of selfassembled MTs. This was compared with the morphology of cold-disassembled MTs. The cold-depolymerization of MTs composed of MTP showed rings and protofilament curls as previously observed using similar methods. Surprisingly, cold-depolymerization of MTs assembled from PC-tubulin induced not only shortening, but also the opening of a large fraction of MTs into sheets, suggesting that the MT lattice contains a cold-labile seam. Under conditions that mimic stochastic shortening, MTs were intact, closed cylinders with ends that were approximately blunt. Therefore, rapid shortening occurs at the ends of the MT, without a long-range disruption of the MT wall. In conclusion, MTs in the elongation phase can have highly irregular ends and need not elongate by a helical assembly process. Conversely, MTs in the shortening phase can have relatively blunt, even ends and can depolymerize in a relatively uniform fashion.

Bibliography

Simon, J. R., & Salmon, E. D. (1990). The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy. Journal of Cell Science, 96(4), 571â582.

Authors 2

John R. Simon (first)
Edward D. Salmon (additional)

References 54 Referenced 77

10.1242/jcs.14.3.523 / J. Cell Sci / Arrangement of subunits in flagellar microtubules by Amos (1974)
10.1242/jcs.93.2.241 / J. Cell Sci / A simple formulation of microtubule dynamics: Quantitative implications of the dynamic instability of microtubule populations in vivo and in vitro by Bayley (1989)
10.1242/jcs.95.1.33 / J. Cell Sci / Microtubule dynamic instability: numberical simulation of microtubule transition properties using a lateral cap model by Bayler (1990)
10.1073/pnas.72.3.1122 / Proc. natn. Acad. Sci. U.S.A / Assembly of chick brain tubulin onto flagellar microtubules from Chlamydomonas and sea urchin sperm by Binder (1975)
10.1016/S0021-9258(18)38061-X / J. biol. Chem / Kinetics and mechanism of MT length changes by dynamic instability by Caplow (1988)
10.1021/bi00388a036 / Biochemistry / MT elongation and guanosine 5′-triphosphate hydrolysis. Role of guanine nucleotides in MT dynamics by Carlier (1987)
10.1083/jcb.107.6.2223 / J. Cell Biol / Real-time observations of microtubule dynamic instability in living cells by Cassimeris (1988)
10.1073/pnas.82.4.1131 / Proc. natn. Acad. Sci. U.S.A / Monte Carlo study of the GTP cap in a five-start helix model of a microtubule by Chen (1985)
10.1073/pnas.75.10.5006 / Proc. natn. Acad. Sci. U.S.A / Differences in a and ß polypeptide chains of tubulin resolved by electron microscopy with image reconstruction by Crepeau (1978)
10.1083/jcb.74.3.747 / J. Cell Biol / Flagellar elongation and shortening in Chlamydomonas III. Structures attached to the tips of flagellar MTs and their relationship to the directionality of flagellar MT assembly by Dentler (1977)
{'key': '2024062901262395000_JOCES_96_4_571C11', 'article-title': 'Mechanism of assembly of sea urchin egg tubulin', 'volume-title': 'Ann, N.Y. Acad. Sci', 'author': 'Detrich', 'year': '1986'} / Ann, N.Y. Acad. Sci / Mechanism of assembly of sea urchin egg tubulin by Detrich (1986)
10.1016/S0021-9258(17)39390-0 / J. biol. Chem / Mechanism of microtubule assembly by Detrich (1985)
{'key': '2024062901262395000_JOCES_96_4_571C13', 'article-title': 'Microtubules. Berlin, Heidelberg', 'author': 'Dustin', 'year': '1984'} / Microtubules. Berlin, Heidelberg by Dustin (1984)
10.1083/jcb.60.1.153 / J. Cell Biol / Microtubule surface lattice and subunit structure and observations on reassembly by Erickson (1974)
10.1002/jss.400020228 / supramolec. Struct / Assembly of microtubules from preformed, ringshaped protofilaments and 6-S tubulin.J by Erickson (1974)
10.1111/j.1749-6632.1986.tb38432.x / Ann. N.Y. Acad. Sci / Nucleation of MT assembly by Erickson (1986)
{'key': '2024062901262395000_JOCES_96_4_571C17', 'first-page': '1186', 'article-title': 'Influence of the centrosome on the structure of nucleated MTs', 'volume': '100', 'author': 'Evans', 'year': '1986', 'journal-title': 'J. Cell Biol'} / J. Cell Biol / Influence of the centrosome on the structure of nucleated MTs by Evans (1986)
10.1016/S0006-291X(88)81306-8 / Biochem. biophyβ. Res. Commun / Fast disassembly of MTs induced by Mg*+ or Ca2+ by Gal (1988)
10.1038/286517a0 / Nature / Visualization of the structural polarity of microtubules by Heidemann (1980)
10.1016/0309-1651(82)90139-4 / Cell Biol. Int. Rep / The effects of glutaraldehyde on the bound nucleotide ∞ntent and morphology of MTs in vitro by Himes (1982)
10.1038/321605a0 / Nature / Visualization of the dynamic instability of individual microtubules by dark-field microscopy by Horio (1986)
10.1016/0022-2836(77)90020-1 / J. molec. Biol / Kinetic analysis of microtubule self-assembly in vitro by Johnson (1977)
10.1242/jcs.94.3.479 / J. Cell Sci / Polymorphism of tubulin assembly in vitro by Karecla (1989)
10.1016/S0074-7696(08)60164-3 / Int. Rev. Cytol / MT assembly and nucleation by Kirschner (1978)
10.1016/S0022-2836(75)80144-6 / J. molec. Biol / Quantitative electron microscopy of MT assembly in vitro by Kirschner (1976)
10.1038/324621a0 / Nature / MT dynamics by Kirschner (1986)
10.1002/jss.400020229 / J. supramolec. Struct / The mechanism of MT assembly in vitro by Kirschner (1974)
10.1073/pnas.71.4.1159 / Proc. natn. Acad. Sci. U.S.A / MTs from mammalian brain: Some properties of their depolymerization products and a proposed mechanism of assembly and disassembly by Kirschner (1974)
10.1083/jcb.89.2.323 / J. Cell Biol / Reassembly of flagellar B(al3) tubulin into singlet microtubules: Consequences for cytoplasmic microtubule structure and assembly by Linck (1981)
10.1083/jcb.89.2.309 / J. Cell Biol / Arrangement of tubulin subunits and microtubule-associated proteins in the centralpair microtubule apparatus of squid (Loligo pealei) sperm flagella by Linck (1981)
{'key': '2024062901262395000_JOCES_96_4_571C31', 'first-page': '23', 'article-title': 'Tubulin, microtubules, and oligomers: Molecular structure and implications for assembly', 'volume-title': 'Cell Movement, vol. 2: Kinesin, Dynein, and Microtubules Dynamics (ed. F. D. Warner and J. R. McIntosh)', 'author': 'Mandelkow', 'year': '1989'} / Cell Movement, vol. 2: Kinesin, Dynein, and Microtubules Dynamics (ed. F. D. Warner and J. R. McIntosh) / Tubulin, microtubules, and oligomers: Molecular structure and implications for assembly by Mandelkow (1989)
10.1016/0022-2836(85)90330-4 / J. molec. Biol / Unstained MTs studied by cryo-electron microscopy substructure, βupertwist and disassembly by Mandelkow (1985)
{'key': '2024062901262395000_JOCES_96_4_571C33', 'first-page': '51', 'article-title': 'Cryo-electron microscopy and freeze fracture studies of microtubules', 'volume-title': 'Microtubules and Microtubule Inhibitors', 'author': 'Mandelkow', 'year': '1986'} / Microtubules and Microtubule Inhibitors / Cryo-electron microscopy and freeze fracture studies of microtubules by Mandelkow (1986)
10.1083/jcb.102.3.1067 / J. Cell Biol / On the surface lattice of MTs: Helix starts, protofilament number, seam, and handedness by Mandelkow (1986)
10.1016/0022-2836(80)90300-9 / J. molec. Biol / Evidence for a mixed lattice in microtubules reassembled in vitro by McEwen (1980)
10.1021/bi00449a028 / Biochemistry / Cold depolymerization of microtubules to double rings: Geometric stabilization of assemblies by Melki (1989)
10.1038/312237a0 / Nature / Dynamic instability of MT growth by Mitchison (1984)
10.1021/bi00480a014 / Biochemistry (in press) / Effects of magnesium on the dynamic instability of individual microtubules by O’brien (1990)
10.1021/bi00387a061 / Biochemistry / GTP hydrolysis during MT assembly by O’ribn (1987)
{'key': '2024062901262395000_JOCES_96_4_571C40', 'article-title': 'Microtubule-associated proteins modulate microtubule dynamic instability in vitro: Real-time observations using video microscopy', 'volume-title': 'J. Cell Biol, (in press)', 'author': 'Phyer', 'year': '1990'} / J. Cell Biol, (in press) / Microtubule-associated proteins modulate microtubule dynamic instability in vitro: Real-time observations using video microscopy by Phyer (1990)
10.1038/332724a0 / Nature / Direct observation of microtubule dynamics in living cells by Sammak (1988)
10.1016/S0022-2836(82)80008-9 / J. molec. Biol / Control of the structural fidelity of MTs by initiation sites by Scheele (1982)
{'key': '2024062901262395000_JOCES_96_4_571C43', 'first-page': '356', 'article-title': 'New features of microtubule behavior observed in vivo. Nature', 'volume': '334', 'author': 'Schulze', 'year': '1988'} / New features of microtubule behavior observed in vivo. Nature by Schulze (1988)
10.1073/pnas.70.3.765 / Proc. natn. Acad. Sci. U.S.A / MT assembly in the absence of added nucleotides by Shelanski (1973)
10.1083/jcb.109.1.341 / J. Cell Biol / The structure of microtubule ends during the elongation and shortening phases of dynamic instability observed by negative-stain electron microscopy by Simon (1989)
{'key': '2024062901262395000_JOCES_96_4_571C46', 'first-page': '4497', 'article-title': 'MT associated proteins and the stimulation of tubulin assembly in vitro. Biochemistry', 'volume': '15', 'author': 'Sloboda', 'year': '1976'} / MT associated proteins and the stimulation of tubulin assembly in vitro. Biochemistry by Sloboda (1976)
10.1083/jcb.61.1.253 / J. Cell Biol / Nonlethal deciliation of Tetrahymena by a local anesthetic and its utility as a tool for studying cilia regeneration by Thompson (1974)
10.1016/S0021-9258(18)90982-8 / J. BLOL Chern / The kinetics of MT assembly by Voter (1984)
10.1111/j.1768-322X.1989.tb00768.x / Biol. Cell / Monotonic versus oscillating MT assembly: a cryo-electron microscope study by Wade (1989)
10.1083/jcb.107.4.1437 / J. Cell Biol / Dynamic instability of individual MTs analyxed by video light microscopy: Rate constants and transition frequencies by Walker (1988)
{'key': '2024062901262395000_JOCES_96_4_571C51', 'first-page': '342a', 'article-title': 'Dilution of individual microtubules observed in real time in vitro. Determination of the delay preceding the onset of rapid shortening', 'volume': '109', 'author': 'Walker', 'year': '1989', 'journal-title': 'J. Cell BioL'} / J. Cell BioL / Dilution of individual microtubules observed in real time in vitro. Determination of the delay preceding the onset of rapid shortening by Walker (1989)
10.1002/jss.400020231 / J. supramolec. Struct / The role of ring aggregates and other structures in the assembly of MTs by Weibbnberg (1974)
10.1083/jcb.76.3.729 / J. Cell Biol / Chlamydomonas flagellar mutants lacking radial spokes and central tubules by Witman (1978)
10.1021/bi00563a022 / Biochemistry / Exchange of tubulin dimer into rings in MT assembly-disassembly by Zeeberg (1980)

Dates

Type	When
Created	4 years, 4 months ago (April 26, 2021, 5:23 p.m.)
Deposited	1 year, 2 months ago (June 28, 2024, 9:26 p.m.)
Indexed	1 month ago (July 27, 2025, 3:54 a.m.)
Issued	35 years ago (Aug. 1, 1990)
Published	35 years ago (Aug. 1, 1990)
Published Online	35 years ago (Aug. 1, 1990)
Published Print	35 years ago (Aug. 1, 1990)

Funders 0

None

BibTeX

@article{Simon_1990, title={The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy}, volume={96}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.96.4.571}, DOI={10.1242/jcs.96.4.571}, number={4}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Simon, John R. and Salmon, Edward D.}, year={1990}, month=aug, pages={571–582} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        27
      ]
    ],
    "date-time": "2025-07-27T07:54:28Z",
    "timestamp": 1753602868078
  },
  "reference-count": 54,
  "publisher": "The Company of Biologists",
  "issue": "4",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1990,
            8,
            1
          ]
        ],
        "date-time": "1990-08-01T00:00:00Z",
        "timestamp": 649468800000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://www.biologists.com/user-licence-1-1/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1990,
        8,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>Microtubules (MTs) are dynamic polymers that can exist in phases of elongation and rapid-shortening at steady-state. These phases have been observed in vitro and in living cells, and this property of MTs has been termed \u2018dynamic instability\u2019. The purpose of this study was to use negative-stain electron microscopy (EM) to test if there are structural differences between the ends of MTs in the elongation and shortening phases, which could provide insight into the mechanisms of dynamic instability. MTs in the elongation phase were obtained by seeding either highly purified porcine brain tubulin (PC-tubulin) or tubulin containing microtubule-associated proteins (MTP), from isolated Tetrahymena axonemes. The results are that, in addition to intact cylindrical MTs, a significant fraction of the tubulin polymer in the elongation phase occurred as sheets of parallel protofilaments, as found in previous investigations with setf-assembled MTs. Therefore, sheet formation is an intrinsic property of MT assembly that does not depend on the tubulin purity or the method of nucleation. Also, since sheets lack helical symmetry, at least a fraction of tubulin polymers seeded from axonemes did not assemble by helical addition of tubulin dimers to the ends, an assumption often made in mathematical models of dynamic instability. Sheets and intact MTs that were seeded from isolated axonemes, emanated both from the intact MT wall of the axoneme A-subfiber and from the incomplete wall of the B-subfiber. Therefore, axoneme seeds do not provide a homogeneous nucleation site for tubulin growth, or produce a homogeneous population of tubulin polymers under our conditions.</jats:p>\n               <jats:p>Previous evidence has indicated that MT disassembly can occur by a segmental release of tubulin oligomers from the ends and at sites along the length of MTs. However, these studies were performed with MTP, and disassembly was induced by cold depolymerization. We examined MT shortening under conditions that closely represent shortening via dynamic instability, namely isothermal dilution at 37 \u00b0C of selfassembled MTs. This was compared with the morphology of cold-disassembled MTs. The cold-depolymerization of MTs composed of MTP showed rings and protofilament curls as previously observed using similar methods. Surprisingly, cold-depolymerization of MTs assembled from PC-tubulin induced not only shortening, but also the opening of a large fraction of MTs into sheets, suggesting that the MT lattice contains a cold-labile seam. Under conditions that mimic stochastic shortening, MTs were intact, closed cylinders with ends that were approximately blunt. Therefore, rapid shortening occurs at the ends of the MT, without a long-range disruption of the MT wall. In conclusion, MTs in the elongation phase can have highly irregular ends and need not elongate by a helical assembly process. Conversely, MTs in the shortening phase can have relatively blunt, even ends and can depolymerize in a relatively uniform fashion.</jats:p>",
  "DOI": "10.1242/jcs.96.4.571",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T21:23:32Z",
    "timestamp": 1619472212000
  },
  "page": "571-582",
  "source": "Crossref",
  "is-referenced-by-count": 77,
  "title": "The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy",
  "prefix": "10.1242",
  "volume": "96",
  "author": [
    {
      "given": "John R.",
      "family": "Simon",
      "sequence": "first",
      "affiliation": [
        {
          "name": "University of North Carolina Department of Biology, 433 Wilson Hall , , Chapel Hill, NC 27599-3280, USA"
        }
      ]
    },
    {
      "given": "Edward D.",
      "family": "Salmon",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "University of North Carolina Department of Biology, 433 Wilson Hall , , Chapel Hill, NC 27599-3280, USA"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1990,
        8,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2024062901262395000_JOCES_96_4_571C1",
      "doi-asserted-by": "publisher",
      "first-page": "523",
      "DOI": "10.1242/jcs.14.3.523",
      "article-title": "Arrangement of subunits in flagellar microtubules",
      "volume": "14",
      "author": "Amos",
      "year": "1974",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C2",
      "doi-asserted-by": "publisher",
      "first-page": "241",
      "DOI": "10.1242/jcs.93.2.241",
      "article-title": "A simple formulation of microtubule dynamics: Quantitative implications of the dynamic instability of microtubule populations in vivo and in vitro",
      "volume": "93",
      "author": "Bayley",
      "year": "1989",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C3",
      "doi-asserted-by": "publisher",
      "first-page": "33",
      "DOI": "10.1242/jcs.95.1.33",
      "article-title": "Microtubule dynamic instability: numberical simulation of microtubule transition properties using a lateral cap model",
      "volume": "95",
      "author": "Bayler",
      "year": "1990",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C4",
      "doi-asserted-by": "publisher",
      "first-page": "1122",
      "DOI": "10.1073/pnas.72.3.1122",
      "article-title": "Assembly of chick brain tubulin onto flagellar microtubules from Chlamydomonas and sea urchin sperm",
      "volume": "72",
      "author": "Binder",
      "year": "1975",
      "journal-title": "Proc. natn. Acad. Sci. U.S.A"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C5",
      "doi-asserted-by": "publisher",
      "first-page": "10 943",
      "DOI": "10.1016/S0021-9258(18)38061-X",
      "article-title": "Kinetics and mechanism of MT length changes by dynamic instability",
      "volume": "263",
      "author": "Caplow",
      "year": "1988",
      "journal-title": "J. biol. Chem"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C6",
      "doi-asserted-by": "publisher",
      "first-page": "4428",
      "DOI": "10.1021/bi00388a036",
      "article-title": "MT elongation and guanosine 5\u2032-triphosphate hydrolysis. Role of guanine nucleotides in MT dynamics",
      "volume": "26",
      "author": "Carlier",
      "year": "1987",
      "journal-title": "Biochemistry"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C7",
      "doi-asserted-by": "publisher",
      "first-page": "2223",
      "DOI": "10.1083/jcb.107.6.2223",
      "article-title": "Real-time observations of microtubule dynamic instability in living cells",
      "volume": "107",
      "author": "Cassimeris",
      "year": "1988",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C8",
      "doi-asserted-by": "publisher",
      "first-page": "1131",
      "DOI": "10.1073/pnas.82.4.1131",
      "article-title": "Monte Carlo study of the GTP cap in a five-start helix model of a microtubule",
      "volume": "82",
      "author": "Chen",
      "year": "1985",
      "journal-title": "Proc. natn. Acad. Sci. U.S.A"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C9",
      "doi-asserted-by": "publisher",
      "first-page": "5006",
      "DOI": "10.1073/pnas.75.10.5006",
      "article-title": "Differences in a and \u00df polypeptide chains of tubulin resolved by electron microscopy with image reconstruction",
      "volume": "75",
      "author": "Crepeau",
      "year": "1978",
      "journal-title": "Proc. natn. Acad. Sci. U.S.A"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C10",
      "doi-asserted-by": "publisher",
      "first-page": "747",
      "DOI": "10.1083/jcb.74.3.747",
      "article-title": "Flagellar elongation and shortening in Chlamydomonas III. Structures attached to the tips of flagellar MTs and their relationship to the directionality of flagellar MT assembly",
      "volume": "74",
      "author": "Dentler",
      "year": "1977",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C11",
      "article-title": "Mechanism of assembly of sea urchin egg tubulin",
      "volume-title": "Ann, N.Y. Acad. Sci",
      "author": "Detrich",
      "year": "1986"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C12",
      "doi-asserted-by": "publisher",
      "first-page": "9479",
      "DOI": "10.1016/S0021-9258(17)39390-0",
      "article-title": "Mechanism of microtubule assembly",
      "volume": "260",
      "author": "Detrich",
      "year": "1985",
      "journal-title": "J. biol. Chem"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C13",
      "article-title": "Microtubules. Berlin, Heidelberg",
      "author": "Dustin",
      "year": "1984"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C14",
      "doi-asserted-by": "publisher",
      "first-page": "153",
      "DOI": "10.1083/jcb.60.1.153",
      "article-title": "Microtubule surface lattice and subunit structure and observations on reassembly",
      "volume": "60",
      "author": "Erickson",
      "year": "1974",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C15",
      "doi-asserted-by": "publisher",
      "first-page": "393",
      "DOI": "10.1002/jss.400020228",
      "article-title": "Assembly of microtubules from preformed, ringshaped protofilaments and 6-S tubulin.J",
      "volume": "2",
      "author": "Erickson",
      "year": "1974",
      "journal-title": "supramolec. Struct"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C16",
      "doi-asserted-by": "publisher",
      "first-page": "552",
      "DOI": "10.1111/j.1749-6632.1986.tb38432.x",
      "article-title": "Nucleation of MT assembly",
      "volume": "466",
      "author": "Erickson",
      "year": "1986",
      "journal-title": "Ann. N.Y. Acad. Sci"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C17",
      "first-page": "1186",
      "article-title": "Influence of the centrosome on the structure of nucleated MTs",
      "volume": "100",
      "author": "Evans",
      "year": "1986",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C18",
      "doi-asserted-by": "publisher",
      "first-page": "1464",
      "DOI": "10.1016/S0006-291X(88)81306-8",
      "article-title": "Fast disassembly of MTs induced by Mg*+ or Ca2+",
      "volume": "55",
      "author": "Gal",
      "year": "1988",
      "journal-title": "Biochem. biophy\u03b2. Res. Commun"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C19",
      "doi-asserted-by": "publisher",
      "first-page": "517",
      "DOI": "10.1038/286517a0",
      "article-title": "Visualization of the structural polarity of microtubules",
      "volume": "286",
      "author": "Heidemann",
      "year": "1980",
      "journal-title": "Nature"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C20",
      "doi-asserted-by": "publisher",
      "first-page": "697",
      "DOI": "10.1016/0309-1651(82)90139-4",
      "article-title": "The effects of glutaraldehyde on the bound nucleotide \u221entent and morphology of MTs in vitro",
      "volume": "6",
      "author": "Himes",
      "year": "1982",
      "journal-title": "Cell Biol. Int. Rep"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C21",
      "doi-asserted-by": "publisher",
      "first-page": "606",
      "DOI": "10.1038/321605a0",
      "article-title": "Visualization of the dynamic instability of individual microtubules by dark-field microscopy",
      "volume": "321",
      "author": "Horio",
      "year": "1986",
      "journal-title": "Nature"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C22",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1016/0022-2836(77)90020-1",
      "article-title": "Kinetic analysis of microtubule self-assembly in vitro",
      "volume": "117",
      "author": "Johnson",
      "year": "1977",
      "journal-title": "J. molec. Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C23",
      "doi-asserted-by": "publisher",
      "first-page": "479",
      "DOI": "10.1242/jcs.94.3.479",
      "article-title": "Polymorphism of tubulin assembly in vitro",
      "volume": "94",
      "author": "Karecla",
      "year": "1989",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C24",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1016/S0074-7696(08)60164-3",
      "article-title": "MT assembly and nucleation",
      "volume": "54",
      "author": "Kirschner",
      "year": "1978",
      "journal-title": "Int. Rev. Cytol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C25",
      "doi-asserted-by": "publisher",
      "first-page": "263",
      "DOI": "10.1016/S0022-2836(75)80144-6",
      "article-title": "Quantitative electron microscopy of MT assembly in vitro",
      "volume": "99",
      "author": "Kirschner",
      "year": "1976",
      "journal-title": "J. molec. Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C26",
      "doi-asserted-by": "publisher",
      "first-page": "621",
      "DOI": "10.1038/324621a0",
      "article-title": "MT dynamics",
      "volume": "324",
      "author": "Kirschner",
      "year": "1986",
      "journal-title": "Nature"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C27",
      "doi-asserted-by": "publisher",
      "first-page": "412",
      "DOI": "10.1002/jss.400020229",
      "article-title": "The mechanism of MT assembly in vitro",
      "volume": "2",
      "author": "Kirschner",
      "year": "1974",
      "journal-title": "J. supramolec. Struct"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C28",
      "doi-asserted-by": "publisher",
      "first-page": "1159",
      "DOI": "10.1073/pnas.71.4.1159",
      "article-title": "MTs from mammalian brain: Some properties of their depolymerization products and a proposed mechanism of assembly and disassembly",
      "volume": "71",
      "author": "Kirschner",
      "year": "1974",
      "journal-title": "Proc. natn. Acad. Sci. U.S.A"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C29",
      "doi-asserted-by": "publisher",
      "first-page": "323",
      "DOI": "10.1083/jcb.89.2.323",
      "article-title": "Reassembly of flagellar B(al3) tubulin into singlet microtubules: Consequences for cytoplasmic microtubule structure and assembly",
      "volume": "89",
      "author": "Linck",
      "year": "1981",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C30",
      "doi-asserted-by": "publisher",
      "first-page": "309",
      "DOI": "10.1083/jcb.89.2.309",
      "article-title": "Arrangement of tubulin subunits and microtubule-associated proteins in the centralpair microtubule apparatus of squid (Loligo pealei) sperm flagella",
      "volume": "89",
      "author": "Linck",
      "year": "1981",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C31",
      "first-page": "23",
      "article-title": "Tubulin, microtubules, and oligomers: Molecular structure and implications for assembly",
      "volume-title": "Cell Movement, vol. 2: Kinesin, Dynein, and Microtubules Dynamics (ed. F. D. Warner and J. R. McIntosh)",
      "author": "Mandelkow",
      "year": "1989"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C32",
      "doi-asserted-by": "publisher",
      "first-page": "123",
      "DOI": "10.1016/0022-2836(85)90330-4",
      "article-title": "Unstained MTs studied by cryo-electron microscopy substructure, \u03b2upertwist and disassembly",
      "volume": "181",
      "author": "Mandelkow",
      "year": "1985",
      "journal-title": "J. molec. Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C33",
      "first-page": "51",
      "article-title": "Cryo-electron microscopy and freeze fracture studies of microtubules",
      "volume-title": "Microtubules and Microtubule Inhibitors",
      "author": "Mandelkow",
      "year": "1986"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C34",
      "doi-asserted-by": "publisher",
      "first-page": "1067",
      "DOI": "10.1083/jcb.102.3.1067",
      "article-title": "On the surface lattice of MTs: Helix starts, protofilament number, seam, and handedness",
      "volume": "102",
      "author": "Mandelkow",
      "year": "1986",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C35",
      "doi-asserted-by": "publisher",
      "first-page": "123",
      "DOI": "10.1016/0022-2836(80)90300-9",
      "article-title": "Evidence for a mixed lattice in microtubules reassembled in vitro",
      "volume": "139",
      "author": "McEwen",
      "year": "1980",
      "journal-title": "J. molec. Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C36",
      "doi-asserted-by": "publisher",
      "first-page": "9143",
      "DOI": "10.1021/bi00449a028",
      "article-title": "Cold depolymerization of microtubules to double rings: Geometric stabilization of assemblies",
      "volume": "28",
      "author": "Melki",
      "year": "1989",
      "journal-title": "Biochemistry"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C37",
      "doi-asserted-by": "publisher",
      "first-page": "237",
      "DOI": "10.1038/312237a0",
      "article-title": "Dynamic instability of MT growth",
      "volume": "312",
      "author": "Mitchison",
      "year": "1984",
      "journal-title": "Nature"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C38",
      "doi-asserted-by": "crossref",
      "DOI": "10.1021/bi00480a014",
      "article-title": "Effects of magnesium on the dynamic instability of individual microtubules",
      "volume-title": "Biochemistry (in press)",
      "author": "O\u2019brien",
      "year": "1990"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C39",
      "doi-asserted-by": "publisher",
      "first-page": "4148",
      "DOI": "10.1021/bi00387a061",
      "article-title": "GTP hydrolysis during MT assembly",
      "volume": "26",
      "author": "O\u2019ribn",
      "year": "1987",
      "journal-title": "Biochemistry"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C40",
      "article-title": "Microtubule-associated proteins modulate microtubule dynamic instability in vitro: Real-time observations using video microscopy",
      "volume-title": "J. Cell Biol, (in press)",
      "author": "Phyer",
      "year": "1990"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C41",
      "doi-asserted-by": "publisher",
      "first-page": "724",
      "DOI": "10.1038/332724a0",
      "article-title": "Direct observation of microtubule dynamics in living cells",
      "volume": "332",
      "author": "Sammak",
      "year": "1988",
      "journal-title": "Nature"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C42",
      "doi-asserted-by": "publisher",
      "first-page": "486",
      "DOI": "10.1016/S0022-2836(82)80008-9",
      "article-title": "Control of the structural fidelity of MTs by initiation sites",
      "volume": "154",
      "author": "Scheele",
      "year": "1982",
      "journal-title": "J. molec. Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C43",
      "first-page": "356",
      "article-title": "New features of microtubule behavior observed in vivo. Nature",
      "volume": "334",
      "author": "Schulze",
      "year": "1988"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C44",
      "doi-asserted-by": "publisher",
      "first-page": "765",
      "DOI": "10.1073/pnas.70.3.765",
      "article-title": "MT assembly in the absence of added nucleotides",
      "volume": "70",
      "author": "Shelanski",
      "year": "1973",
      "journal-title": "Proc. natn. Acad. Sci. U.S.A"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C45",
      "doi-asserted-by": "publisher",
      "first-page": "341a",
      "DOI": "10.1083/jcb.109.1.341",
      "article-title": "The structure of microtubule ends during the elongation and shortening phases of dynamic instability observed by negative-stain electron microscopy",
      "volume": "109",
      "author": "Simon",
      "year": "1989",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C46",
      "first-page": "4497",
      "article-title": "MT associated proteins and the stimulation of tubulin assembly in vitro. Biochemistry",
      "volume": "15",
      "author": "Sloboda",
      "year": "1976"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C47",
      "doi-asserted-by": "publisher",
      "first-page": "253",
      "DOI": "10.1083/jcb.61.1.253",
      "article-title": "Nonlethal deciliation of Tetrahymena by a local anesthetic and its utility as a tool for studying cilia regeneration",
      "volume": "61",
      "author": "Thompson",
      "year": "1974",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C48",
      "doi-asserted-by": "publisher",
      "first-page": "10 430",
      "DOI": "10.1016/S0021-9258(18)90982-8",
      "article-title": "The kinetics of MT assembly",
      "volume": "259",
      "author": "Voter",
      "year": "1984",
      "journal-title": "J. BLOL Chern"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C49",
      "doi-asserted-by": "publisher",
      "first-page": "37",
      "DOI": "10.1111/j.1768-322X.1989.tb00768.x",
      "article-title": "Monotonic versus oscillating MT assembly: a cryo-electron microscope study",
      "volume": "65",
      "author": "Wade",
      "year": "1989",
      "journal-title": "Biol. Cell"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C50",
      "doi-asserted-by": "publisher",
      "first-page": "1437",
      "DOI": "10.1083/jcb.107.4.1437",
      "article-title": "Dynamic instability of individual MTs analyxed by video light microscopy: Rate constants and transition frequencies",
      "volume": "107",
      "author": "Walker",
      "year": "1988",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C51",
      "first-page": "342a",
      "article-title": "Dilution of individual microtubules observed in real time in vitro. Determination of the delay preceding the onset of rapid shortening",
      "volume": "109",
      "author": "Walker",
      "year": "1989",
      "journal-title": "J. Cell BioL"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C52",
      "doi-asserted-by": "publisher",
      "first-page": "451",
      "DOI": "10.1002/jss.400020231",
      "article-title": "The role of ring aggregates and other structures in the assembly of MTs",
      "volume": "2",
      "author": "Weibbnberg",
      "year": "1974",
      "journal-title": "J. supramolec. Struct"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C53",
      "doi-asserted-by": "publisher",
      "first-page": "729",
      "DOI": "10.1083/jcb.76.3.729",
      "article-title": "Chlamydomonas flagellar mutants lacking radial spokes and central tubules",
      "volume": "76",
      "author": "Witman",
      "year": "1978",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2024062901262395000_JOCES_96_4_571C54",
      "doi-asserted-by": "publisher",
      "first-page": "6078",
      "DOI": "10.1021/bi00563a022",
      "article-title": "Exchange of tubulin dimer into rings in MT assembly-disassembly",
      "volume": "19",
      "author": "Zeeberg",
      "year": "1980",
      "journal-title": "Biochemistry"
    }
  ],
  "container-title": "Journal of Cell Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/jcs/article-pdf/96/4/571/3534804/joces_96_4_571.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/jcs/article-pdf/96/4/571/3534804/joces_96_4_571.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        6,
        29
      ]
    ],
    "date-time": "2024-06-29T01:26:33Z",
    "timestamp": 1719624393000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/jcs/article/96/4/571/60898/The-structure-of-microtubule-ends-during-the"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1990,
        8,
        1
      ]
    ]
  },
  "references-count": 54,
  "journal-issue": {
    "issue": "4",
    "published-print": {
      "date-parts": [
        [
          1990,
          8,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/jcs.96.4.571",
  "relation": {},
  "ISSN": [
    "0021-9533",
    "1477-9137"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1990,
        8,
        1
      ]
    ]
  }
}