DOI: 10.1242/jcs.94.2.333. Enolase exists in the fluid phase of cytoplasm in 3T3 cells

Enolase exists in the fluid phase of cytoplasm in 3T3 cells

10.1242/jcs.94.2.333

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

ABSTRACT We have investigated the intracellular distribution and mobility of the glycolytic enzyme enolase, using functional fluorescent analogs labeled with the succinimidyl esters of carboxyfluorescein (Flenolase) and carboxytetramethylrhodamirie (Rh-enolase). In contrast to aldolase, neither native enolase nor labeled enolase gelled filamentous actin (F-actin), as measured by falling-ball viscometry, indicating a lack of interaction between enolase and F-actin. Fluorescence redistribution after photobleaching (FRAP) measurements of the dflfusion coefficient (D) of Fl-enolase in aqueous solutions gave a value of D337,aq = 6·08×10−7cm2s-1, and no immobile fraction, consistent with a native molecular weight of 90 000. These values were not significantly dHferent with Rh-enolase, or in the presence of F-actin, 2-ρhosρhoglycerate or F-actin–aldolase gels, demonstrating that neither Fl-enolase nor Rh-enolase binds to F-actin or aldolase in vitro. FRAP measurements of Fl- and Rh-enolase microinjected into living Swiss 3T3 cells revealed spatial differences in the diffusion coefficient, but not the mobile fraction. In the perinuclear cytoplasm, we measured an apparent diffusion coefficient of l·1×10−7cm2s-1, compared to 7·1×10−8cm2s-1 in the peripheral cytoplasm, with ≈ 100% mobility of Fl- or Rh-enolase in both regions. Imaging of cells co-injected with Rh-enolase and size-fractionated FITC–dextran (FD-90) revealed that Rh-enolase entered the nucleus, while FD-90 was excluded. Ratio imaging showed a relatively high nuclear ratio of Rh-enolase/FD-90, and a uniform cytoplasmic ratio, with no indication of increased concentration of enolase around stress fibers. These data demonstrate that Rh- and Fl-enolase do not bind to F-actin in vitro, and are 100% mobile in vivo. Together with our recent finding that a significant fraction of aldolase binds to F-actin in vivo and is immobile in vivo, these data suggest a correlation between actin-binding activity and cytoplasmic mobility of glycolytic enzymes.

Bibliography

Pagliaro, L., Kerr, K., & taylor, D. L. (1989). Enolase exists in the fluid phase of cytoplasm in 3T3 cells. Journal of Cell Science, 94(2), 333â342.

Authors 3

Len Pagliaro (first)
Karen Kerr (additional)
D. Lansing taylor (additional)

References 63 Referenced 15

10.1111/j.1432-1033.1971.tb01522.x / Eur.J. Biochem / Quantitative comparison of the binding of various glycolytic enzymes to F-actin and the interaction of aldolase with G-actin by Arnold (1971)
10.1111/j.1432-1033.1970.tb01016.x / Eur.J. Biochem / Binding of aldolase and triosephoβphate dehydrogenase to F-actin and modification of catalytic properties of aldolase by Arnold (1970)
10.1016/S0006-3495(76)85755-4 / Biophvs. J / Mobility measurement by analysis of fluorescence photobleaching recovery kinetics by Axelrod (1976)
10.1016/0076-6879(75)42137-1 / Meth. Enzym / Enolase fron human muscle by Baranowski (1975)
10.1016/0303-2647(85)90066-8 / B10systems / Is the “soluble” phase of cells structured? by Bhargava (1985)
10.1021/ma00136a011 / Macromolecules / Hindered diffusion of dextran and ficoll in microporous membranes by Bohrer (1984)
10.1016/0092-8674(81)90147-1 / Cell / Nerve-specific enolase and creatine phosphokinase in axonal transport: soluble proteins and the axoplasmic matrix by Brady (1981)
10.1083/jcb.104.4.1019 / J. Cell Biol / Fluorescence ratio imaging microscopy: temporal and spatial measurements of cytoplasmic pH by Bright (1987)
{'key': '2023071213551425300_JOCES_94_2_333C9', 'first-page': '157', 'article-title': 'Fluorescence ratio imaging microscopy', 'author': 'Bright', 'year': '1989', 'journal-title': 'In Methods in Cell Biology. Fluorescence Microscopy of Living Cells in Culture'} / In Methods in Cell Biology. Fluorescence Microscopy of Living Cells in Culture / Fluorescence ratio imaging microscopy by Bright (1989)
10.1139/o81-069 / Can. J. Biochem / Interaction of muscle glycolytic enzymes with thin filament proteins by Bronstein (1981)
{'key': '2023071213551425300_JOCES_94_2_333C11', 'first-page': '359', 'article-title': 'Interactions between muscle proteins and glycolytic enzymes, hit', 'volume': '7', 'author': 'Clarke', 'year': '1976', 'journal-title': 'J. Biochem'} / J. Biochem / Interactions between muscle proteins and glycolytic enzymes, hit by Clarke (1976)
{'key': '2023071213551425300_JOCES_94_2_333C12', 'first-page': '235', 'article-title': 'The functional duality of glycolytic enzymes: potential integrators of cytoplasmic structure and function', 'volume-title': 'In Cell Motility: Mechanism and Regulation (10th Yamada Conference)', 'author': 'Clarke', 'year': '1985'} / In Cell Motility: Mechanism and Regulation (10th Yamada Conference) / The functional duality of glycolytic enzymes: potential integrators of cytoplasmic structure and function by Clarke (1985)
{'key': '2023071213551425300_JOCES_94_2_333C13', 'first-page': 'R133', 'article-title': 'Properties and metabolism of the aqueous cytoplasm and its boundaries', 'volume': '246', 'author': 'Clegg', 'year': '1984', 'journal-title': 'Am. J. Physiol'} / Am. J. Physiol / Properties and metabolism of the aqueous cytoplasm and its boundaries by Clegg (1984)
10.1083/jcb.99.1.167s / J. Cell Biol / Intracellular water and the cytomatrix: some methods of study and current views by Clegg (1984)
10.1083/jcb.105.4.1613 / Cell Biol / Five-parameter fluorescence imaging: wound healing of living Swiss 3T3 cells. J by DeBiasio (1987)
10.1016/B978-0-08-016874-6.50085-0 / In Structure and Function of Oxidation–Reduction Enzymes / Is there a glycolytic particle? by DE Duve (1972)
10.1083/jcb.96.5.1486 / J. Cell Biol / Evidence for mediated protein uptake by amphibian oocyte nuclei by Feldherr (1983)
10.1016/0005-2744(76)90077-2 / Biochim. biophys. Acta / Enolase isozymes. III. Chromatographic and immunological characteristics of rat brain enolase by Fletcher (1976)
10.1002/jcb.1982.240180305 / J. Cell Biochem / In vitro rEconstitution of chromaffin granule-cytoskeleton interactions: ionic factors influencing the association of F-actin with purified chromaffin granule membranes by Fowler (1982)
10.1042/bst0150973 / Biochem. Soc. Trans / An overview of supramolecular enzyme organization by Friedrich (1987)
10.1073/pnas.82.15.5030 / Proc. natn. Acad. Sci. U.SA / The cytoplasmic matrix: its volume and surface area and the diffusion of molecules through it by Gershon (1985)
10.1083/jcb.102.3.853 / J. Cell Biol / Chemical factors that influence nucleocytoplasmic transport: a fluorescence photobleaching study by Jiang (1986)
10.1083/jcb.106.1.13 / J. Cell Biol / Nuclear transport in 3T3 fibroblasts: effects of growth factors, transformation, and cell shape by Jiang (1988)
10.1016/B978-1-4832-3161-7.50034-3 / In Control of Energy Metabolism / On the direction of pyridine nucleotide oxidation-reduction reactions in gluconeogenesis and hpogenesi3 by Lardy (1965)
{'key': '2023071213551425300_JOCES_94_2_333C25', 'volume-title': 'Biochemistry: The Molecular Basis of Cell Structure and Function, p. 1104', 'author': 'Lehninger', 'year': '1975'} / Biochemistry: The Molecular Basis of Cell Structure and Function, p. 1104 by Lehninger (1975)
10.1016/S0006-3495(83)84314-8 / B10phys. J / Rotational diffusion of tempone in the cytoplasm of Chinese hamster lung cells by Lepock (1983)
10.1073/pnas.84.14.4910 / Proc. natn. Acad. Sci. U.SA / Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells by Luby-Phelps (1987)
10.1083/jcb.101.4.1245 / J. Cell Biol / Behavior of a fluorescent analogue of calmodulin in living 3T3 cells by Luby-Phelps (1985)
10.1146/annurev.bb.17.060188.002101 / Rev. Biophys. biophys. Chern / The submicroscopic properties of cytoplasm as a determinant of cellular function. A by Luby-Phelps (1988)
10.1083/jcb.102.6.2015 / J. Cell Biol / Probing the structure of cytoplasm by Luby-Phelps (1986)
10.1083/jcb.85.2.414 / J. Cell Biol / Viscometric analysis of the gelation of Acanthamoeba extracts and purification of two gelation factors by MacLean-FletchĒr (1980)
10.1083/jcb.99.1.222s / J. Cell Biol / Interactions between glycolytic enzymes and components of the cytomatrix by Masters (1984)
10.1073/pnas.81.11.3414 / Proc. natn. Acad. Sci. U.SA / Diffusion of a small molecule in the cytoplasm of mammalian cells by Mastro (1984)
10.1111/j.1432-1033.1988.tb14465.x / Eur. J. Biochem / Complete amino acid sequence of the neurone-specific gamma isozyme of enolase (NSE) from human brain and comparison with the non-neuronal a form (NNE) by McAleese (1988)
10.1016/0014-5793(89)80515-0 / FEBS Lett / cDNA cloning and nucleotide sequence of rat muscle-specific enolase (ßß enolase) by Ohshima (1989)
{'key': '2023071213551425300_JOCES_94_2_333C36', 'first-page': '107', 'article-title': 'The role of compartmentation in the control of glycolysis', 'volume-title': 'In Curr. Top. Cell. Regul', 'author': 'Ottaway', 'year': '1977'} / In Curr. Top. Cell. Regul / The role of compartmentation in the control of glycolysis by Ottaway (1977)
10.1083/jcb.107.3.981 / J. Cell Biol / Aldolase exists in both the fluid and solid phases of cytoplasm by Pagliaro (1988)
10.1016/B978-0-12-289504-3.50013-9 / In Cell Biology. A Comprehensive Treatise / The movement of material between nucleus and cytoplasm by Paine (1980)
10.1038/254109a0 / Nature, Land / Nuclear envelope permeability by Paine (1975)
10.1083/jcb.99.1.3s / J. Cell Biol / The cytomatrix: a short history of its study by Porter (1984)
10.1016/0005-2795(74)90273-6 / Biochim. biophys. Aeta / Enolase isozymes in rat tissues. Electrophoretic, chromatographic, immunological and kinetic properties by Rider (1974)
10.1016/0006-291X(75)90582-3 / Biochem. biophvs. Res. Commun / Evidence for a new form of enolase in rat brain by Rider (1975)
10.1002/cyto.990100402 / Cytometry / Evaluation of algorithms for ratio imaging in fluorescence microscopy by Rogowska (1989)
10.1042/bj2360115 / Biochem. J / The complete amino acid sequence of chicken skeletal-muscle enolase by Russell (1986)
10.1021/ac60214a047 / Analyt. Chern / Smoothing and differentiation of data by simplified least squares procedures by Savγrzky (1964)
10.1016/0003-2697(73)90523-X / Analyt. Biochem / A simplified method for the quantitative assay of small amounts of protein in biological material by Schacterle (1973)
10.1083/jcb.102.3.859 / Cell Biol / Nuclear actin and myosin as control elements in nucleocytoplasmic transport. J by Schindler (1986)
10.1002/cm.970110107 / Cell Motil. Cytoskel / The molecular mobility of a-actinin and actin in a rEconstituted model of gelation by Simon (1988)
10.1016/0076-6879(86)34115-6 / Meth. Enzym / Preparation of a fluorescent analog: acetamidofluoresceinyl-labeled Dictyostelium discoideum a- actinin by Simon (1986)
10.1016/S0021-9258(18)62016-2 / Biol. Chern / The regulation of rabbit skeletal muscle contraction by Spudich (1971)
10.1146/annurev.bi.56.070187.000513 / Rev. Biochem / Complexes of sequential metabolic enzymes. In A by Srere (1987)
10.1016/B978-0-12-152828-7.50003-2 / Curr. Top. Cell. Regul / Enzyme-enzyme interactions and the regulation of metabolic reaction pathways by Srivastava (1986)
10.1126/science.3775377 / Science / Metabolite transfer via enzyme-enzyme complexes by Srivastava (19866)
{'key': '2023071213551425300_JOCES_94_2_333C54', 'first-page': '175', 'article-title': 'Biophysical chemistry of metabolic reaction sequences in concentrated enzyme solution and in the cell. A', 'volume': '16', 'author': 'Srivastava', 'year': '1987', 'journal-title': 'Rev. Biophvs. biophvs. Chern'} / Rev. Biophvs. biophvs. Chern / Biophysical chemistry of metabolic reaction sequences in concentrated enzyme solution and in the cell. A by Srivastava (1987)
10.1083/jcb.100.6.1968 / J. Cell Biol / The small subunit of ribonucleotide reductase is encoded by one of the most abundant translationally regulated maternal RNAs in clam and sea urchin eggs by Standart (1985)
10.1093/oxfordjournals.jbchem.a132901 / J. Biochem. (Japan / Rat brain enolase isozymes: purification of 3 forms of enolase by Suzuki (1980)
10.1083/jcb.98.2.717 / J. Cell Biol / Microspectrofluorometry by digital image processing: measurement of cytoplasmic pH by Tanasugarn (1984)
10.1073/pnas.75.2.857 / Proc, natn. Acad. Sci. U.S.A / Molecular cytochemistry: incorporation of fluorescently labeled actin into living cells by Taylor (1978)
10.1016/0167-4838(88)90104-5 / Biochim. biophys. Acta / Heteromerous interactions among glycolytic enzymes and of glycolytic enzymes with F-actin: effects of polyethylene glycol by Walsh (1988)
10.1042/bj1650165 / Biochem. 7 / Modification of the kinetic parameters of aldolase on binding to the actin-containing filaments of skeletal muscle by Walsh (1977)
10.1073/pnas.79.15.4660 / Proc. natn. Acad. Sci. U.SA / Mobility of cytoplasmic and membrane-associated actin in living cells by Wang (1982)
10.1016/0079-6107(78)90019-6 / Prog. Biophvs. molec. Biol / On the role of organized multienzyme systems in cellular metabolism: a general synthesis by Welch (1977)
10.1016/S0006-3495(82)84459-7 / Biophvs. J / Lateral mobility in membranes as detected by fluorescence recovery after photobleaching by Yguerabide (1982)

Dates

Type	When
Created	4 years, 4 months ago (April 26, 2021, 5:28 p.m.)
Deposited	2 years, 1 month ago (July 12, 2023, 9:56 a.m.)
Indexed	4 months, 1 week ago (April 25, 2025, 8:29 a.m.)
Issued	35 years, 11 months ago (Oct. 1, 1989)
Published	35 years, 11 months ago (Oct. 1, 1989)
Published Online	35 years, 11 months ago (Oct. 1, 1989)
Published Print	35 years, 11 months ago (Oct. 1, 1989)

Funders 0

None

BibTeX

@article{Pagliaro_1989, title={Enolase exists in the fluid phase of cytoplasm in 3T3 cells}, volume={94}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.94.2.333}, DOI={10.1242/jcs.94.2.333}, number={2}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Pagliaro, Len and Kerr, Karen and taylor, D. Lansing}, year={1989}, month=oct, pages={333–342} }

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  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>We have investigated the intracellular distribution and mobility of the glycolytic enzyme enolase, using functional fluorescent analogs labeled with the succinimidyl esters of carboxyfluorescein (Flenolase) and carboxytetramethylrhodamirie (Rh-enolase). In contrast to aldolase, neither native enolase nor labeled enolase gelled filamentous actin (F-actin), as measured by falling-ball viscometry, indicating a lack of interaction between enolase and F-actin. Fluorescence redistribution after photobleaching (FRAP) measurements of the dflfusion coefficient (D) of Fl-enolase in aqueous solutions gave a value of D337,aq = 6\u00b708\u00d710\u22127cm2s-1, and no immobile fraction, consistent with a native molecular weight of 90 000. These values were not significantly dHferent with Rh-enolase, or in the presence of F-actin, 2-\u03c1hos\u03c1hoglycerate or F-actin\u2013aldolase gels, demonstrating that neither Fl-enolase nor Rh-enolase binds to F-actin or aldolase in vitro. FRAP measurements of Fl- and Rh-enolase microinjected into living Swiss 3T3 cells revealed spatial differences in the diffusion coefficient, but not the mobile fraction. In the perinuclear cytoplasm, we measured an apparent diffusion coefficient of l\u00b71\u00d710\u22127cm2s-1, compared to 7\u00b71\u00d710\u22128cm2s-1 in the peripheral cytoplasm, with \u2248 100% mobility of Fl- or Rh-enolase in both regions. Imaging of cells co-injected with Rh-enolase and size-fractionated FITC\u2013dextran (FD-90) revealed that Rh-enolase entered the nucleus, while FD-90 was excluded. Ratio imaging showed a relatively high nuclear ratio of Rh-enolase/FD-90, and a uniform cytoplasmic ratio, with no indication of increased concentration of enolase around stress fibers. These data demonstrate that Rh- and Fl-enolase do not bind to F-actin in vitro, and are 100% mobile in vivo. Together with our recent finding that a significant fraction of aldolase binds to F-actin in vivo and is immobile in vivo, these data suggest a correlation between actin-binding activity and cytoplasmic mobility of glycolytic enzymes.</jats:p>",
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      "volume": "16",
      "author": "Axelrod",
      "year": "1976",
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      "author": "Baranowski",
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      "author": "DE Duve",
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    {
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      "first-page": "1486",
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      "article-title": "Evidence for mediated protein uptake by amphibian oocyte nuclei",
      "volume": "96",
      "author": "Feldherr",
      "year": "1983",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C18",
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      "first-page": "245",
      "DOI": "10.1016/0005-2744(76)90077-2",
      "article-title": "Enolase isozymes. III. Chromatographic and immunological characteristics of rat brain enolase",
      "volume": "452",
      "author": "Fletcher",
      "year": "1976",
      "journal-title": "Biochim. biophys. Acta"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C19",
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      "first-page": "295",
      "DOI": "10.1002/jcb.1982.240180305",
      "article-title": "In vitro rEconstitution of chromaffin granule-cytoskeleton interactions: ionic factors influencing the association of F-actin with purified chromaffin granule membranes",
      "volume": "18",
      "author": "Fowler",
      "year": "1982",
      "journal-title": "J. Cell Biochem"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C20",
      "doi-asserted-by": "crossref",
      "first-page": "973",
      "DOI": "10.1042/bst0150973",
      "article-title": "An overview of supramolecular enzyme organization",
      "volume": "15",
      "author": "Friedrich",
      "year": "1987",
      "journal-title": "Biochem. Soc. Trans"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C21",
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      "first-page": "5030",
      "DOI": "10.1073/pnas.82.15.5030",
      "article-title": "The cytoplasmic matrix: its volume and surface area and the diffusion of molecules through it",
      "volume": "82",
      "author": "Gershon",
      "year": "1985",
      "journal-title": "Proc. natn. Acad. Sci. U.SA"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C22",
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      "first-page": "853",
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      "article-title": "Chemical factors that influence nucleocytoplasmic transport: a fluorescence photobleaching study",
      "volume": "102",
      "author": "Jiang",
      "year": "1986",
      "journal-title": "J. Cell Biol"
    },
    {
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      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1083/jcb.106.1.13",
      "article-title": "Nuclear transport in 3T3 fibroblasts: effects of growth factors, transformation, and cell shape",
      "volume": "106",
      "author": "Jiang",
      "year": "1988",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C24",
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      "first-page": "245",
      "DOI": "10.1016/B978-1-4832-3161-7.50034-3",
      "article-title": "On the direction of pyridine nucleotide oxidation-reduction reactions in gluconeogenesis and hpogenesi3",
      "volume-title": "In Control of Energy Metabolism",
      "author": "Lardy",
      "year": "1965"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C25",
      "volume-title": "Biochemistry: The Molecular Basis of Cell Structure and Function, p. 1104",
      "author": "Lehninger",
      "year": "1975"
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      "first-page": "405",
      "DOI": "10.1016/S0006-3495(83)84314-8",
      "article-title": "Rotational diffusion of tempone in the cytoplasm of Chinese hamster lung cells",
      "volume": "44",
      "author": "Lepock",
      "year": "1983",
      "journal-title": "B10phys. J"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C27",
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      "first-page": "4910",
      "DOI": "10.1073/pnas.84.14.4910",
      "article-title": "Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells",
      "volume": "84",
      "author": "Luby-Phelps",
      "year": "1987",
      "journal-title": "Proc. natn. Acad. Sci. U.SA"
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      "first-page": "1245",
      "DOI": "10.1083/jcb.101.4.1245",
      "article-title": "Behavior of a fluorescent analogue of calmodulin in living 3T3 cells",
      "volume": "101",
      "author": "Luby-Phelps",
      "year": "1985",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C29",
      "doi-asserted-by": "crossref",
      "first-page": "369",
      "DOI": "10.1146/annurev.bb.17.060188.002101",
      "article-title": "The submicroscopic properties of cytoplasm as a determinant of cellular function. A",
      "volume": "17",
      "author": "Luby-Phelps",
      "year": "1988",
      "journal-title": "Rev. Biophys. biophys. Chern"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C30",
      "doi-asserted-by": "crossref",
      "first-page": "2015",
      "DOI": "10.1083/jcb.102.6.2015",
      "article-title": "Probing the structure of cytoplasm",
      "volume": "102",
      "author": "Luby-Phelps",
      "year": "1986",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C31",
      "doi-asserted-by": "crossref",
      "first-page": "414",
      "DOI": "10.1083/jcb.85.2.414",
      "article-title": "Viscometric analysis of the gelation of Acanthamoeba extracts and purification of two gelation factors",
      "volume": "85",
      "author": "MacLean-Fletch\u0112r",
      "year": "1980",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C32",
      "doi-asserted-by": "crossref",
      "first-page": "222s",
      "DOI": "10.1083/jcb.99.1.222s",
      "article-title": "Interactions between glycolytic enzymes and components of the cytomatrix",
      "volume": "99",
      "author": "Masters",
      "year": "1984",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C33",
      "doi-asserted-by": "crossref",
      "first-page": "3414",
      "DOI": "10.1073/pnas.81.11.3414",
      "article-title": "Diffusion of a small molecule in the cytoplasm of mammalian cells",
      "volume": "81",
      "author": "Mastro",
      "year": "1984",
      "journal-title": "Proc. natn. Acad. Sci. U.SA"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C34",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1111/j.1432-1033.1988.tb14465.x",
      "article-title": "Complete amino acid sequence of the neurone-specific gamma isozyme of enolase (NSE) from human brain and comparison with the non-neuronal a form (NNE)",
      "volume": "178",
      "author": "McAleese",
      "year": "1988",
      "journal-title": "Eur. J. Biochem"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C35",
      "doi-asserted-by": "crossref",
      "first-page": "425",
      "DOI": "10.1016/0014-5793(89)80515-0",
      "article-title": "cDNA cloning and nucleotide sequence of rat muscle-specific enolase (\u00df\u00df enolase)",
      "volume": "242",
      "author": "Ohshima",
      "year": "1989",
      "journal-title": "FEBS Lett"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C36",
      "first-page": "107",
      "article-title": "The role of compartmentation in the control of glycolysis",
      "volume-title": "In Curr. Top. Cell. Regul",
      "author": "Ottaway",
      "year": "1977"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C37",
      "doi-asserted-by": "crossref",
      "first-page": "981",
      "DOI": "10.1083/jcb.107.3.981",
      "article-title": "Aldolase exists in both the fluid and solid phases of cytoplasm",
      "volume": "107",
      "author": "Pagliaro",
      "year": "1988",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C38",
      "doi-asserted-by": "crossref",
      "first-page": "299",
      "DOI": "10.1016/B978-0-12-289504-3.50013-9",
      "article-title": "The movement of material between nucleus and cytoplasm",
      "volume-title": "In Cell Biology. A Comprehensive Treatise",
      "author": "Paine",
      "year": "1980"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C39",
      "doi-asserted-by": "crossref",
      "first-page": "109",
      "DOI": "10.1038/254109a0",
      "article-title": "Nuclear envelope permeability",
      "volume": "254",
      "author": "Paine",
      "year": "1975",
      "journal-title": "Nature, Land"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C40",
      "doi-asserted-by": "crossref",
      "first-page": "3s",
      "DOI": "10.1083/jcb.99.1.3s",
      "article-title": "The cytomatrix: a short history of its study",
      "volume": "99",
      "author": "Porter",
      "year": "1984",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C41",
      "doi-asserted-by": "crossref",
      "first-page": "285",
      "DOI": "10.1016/0005-2795(74)90273-6",
      "article-title": "Enolase isozymes in rat tissues. Electrophoretic, chromatographic, immunological and kinetic properties",
      "volume": "365",
      "author": "Rider",
      "year": "1974",
      "journal-title": "Biochim. biophys. Aeta"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C42",
      "doi-asserted-by": "crossref",
      "first-page": "814",
      "DOI": "10.1016/0006-291X(75)90582-3",
      "article-title": "Evidence for a new form of enolase in rat brain",
      "volume": "66",
      "author": "Rider",
      "year": "1975",
      "journal-title": "Biochem. biophvs. Res. Commun"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C43",
      "doi-asserted-by": "crossref",
      "first-page": "357",
      "DOI": "10.1002/cyto.990100402",
      "article-title": "Evaluation of algorithms for ratio imaging in fluorescence microscopy",
      "volume": "10",
      "author": "Rogowska",
      "year": "1989",
      "journal-title": "Cytometry"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C44",
      "doi-asserted-by": "crossref",
      "first-page": "115",
      "DOI": "10.1042/bj2360115",
      "article-title": "The complete amino acid sequence of chicken skeletal-muscle enolase",
      "volume": "236",
      "author": "Russell",
      "year": "1986",
      "journal-title": "Biochem. J"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C45",
      "doi-asserted-by": "crossref",
      "first-page": "1627",
      "DOI": "10.1021/ac60214a047",
      "article-title": "Smoothing and differentiation of data by simplified least squares procedures",
      "volume": "36",
      "author": "Sav\u03b3rzky",
      "year": "1964",
      "journal-title": "Analyt. Chern"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C46",
      "doi-asserted-by": "crossref",
      "first-page": "654",
      "DOI": "10.1016/0003-2697(73)90523-X",
      "article-title": "A simplified method for the quantitative assay of small amounts of protein in biological material",
      "volume": "51",
      "author": "Schacterle",
      "year": "1973",
      "journal-title": "Analyt. Biochem"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C47",
      "doi-asserted-by": "crossref",
      "first-page": "859",
      "DOI": "10.1083/jcb.102.3.859",
      "article-title": "Nuclear actin and myosin as control elements in nucleocytoplasmic transport. J",
      "volume": "102",
      "author": "Schindler",
      "year": "1986",
      "journal-title": "Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C48",
      "doi-asserted-by": "crossref",
      "first-page": "64",
      "DOI": "10.1002/cm.970110107",
      "article-title": "The molecular mobility of a-actinin and actin in a rEconstituted model of gelation",
      "volume": "11",
      "author": "Simon",
      "year": "1988",
      "journal-title": "Cell Motil. Cytoskel"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C49",
      "doi-asserted-by": "crossref",
      "first-page": "487",
      "DOI": "10.1016/0076-6879(86)34115-6",
      "article-title": "Preparation of a fluorescent analog: acetamidofluoresceinyl-labeled Dictyostelium discoideum a- actinin",
      "volume": "134",
      "author": "Simon",
      "year": "1986",
      "journal-title": "Meth. Enzym"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C50",
      "doi-asserted-by": "crossref",
      "first-page": "4866",
      "DOI": "10.1016/S0021-9258(18)62016-2",
      "article-title": "The regulation of rabbit skeletal muscle contraction",
      "volume": "246",
      "author": "Spudich",
      "year": "1971",
      "journal-title": "Biol. Chern"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C51",
      "doi-asserted-by": "crossref",
      "first-page": "89",
      "DOI": "10.1146/annurev.bi.56.070187.000513",
      "article-title": "Complexes of sequential metabolic enzymes. In A",
      "author": "Srere",
      "year": "1987",
      "journal-title": "Rev. Biochem"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C52",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/B978-0-12-152828-7.50003-2",
      "article-title": "Enzyme-enzyme interactions and the regulation of metabolic reaction pathways",
      "volume": "28",
      "author": "Srivastava",
      "year": "1986",
      "journal-title": "Curr. Top. Cell. Regul"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C53",
      "doi-asserted-by": "crossref",
      "first-page": "1081",
      "DOI": "10.1126/science.3775377",
      "article-title": "Metabolite transfer via enzyme-enzyme complexes",
      "volume": "234",
      "author": "Srivastava",
      "year": "19866",
      "journal-title": "Science"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C54",
      "first-page": "175",
      "article-title": "Biophysical chemistry of metabolic reaction sequences in concentrated enzyme solution and in the cell. A",
      "volume": "16",
      "author": "Srivastava",
      "year": "1987",
      "journal-title": "Rev. Biophvs. biophvs. Chern"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C55",
      "doi-asserted-by": "crossref",
      "first-page": "1968",
      "DOI": "10.1083/jcb.100.6.1968",
      "article-title": "The small subunit of ribonucleotide reductase is encoded by one of the most abundant translationally regulated maternal RNAs in clam and sea urchin eggs",
      "volume": "100",
      "author": "Standart",
      "year": "1985",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C56",
      "doi-asserted-by": "crossref",
      "first-page": "1587",
      "DOI": "10.1093/oxfordjournals.jbchem.a132901",
      "article-title": "Rat brain enolase isozymes: purification of 3 forms of enolase",
      "volume": "87",
      "author": "Suzuki",
      "year": "1980",
      "journal-title": "J. Biochem. (Japan"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C57",
      "doi-asserted-by": "crossref",
      "first-page": "717",
      "DOI": "10.1083/jcb.98.2.717",
      "article-title": "Microspectrofluorometry by digital image processing: measurement of cytoplasmic pH",
      "volume": "98",
      "author": "Tanasugarn",
      "year": "1984",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023071213551425300_JOCES_94_2_333C58",
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      "first-page": "857",
      "DOI": "10.1073/pnas.75.2.857",
      "article-title": "Molecular cytochemistry: incorporation of fluorescently labeled actin into living cells",
      "volume": "75",
      "author": "Taylor",
      "year": "1978",
      "journal-title": "Proc, natn. Acad. Sci. U.S.A"
    },
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      "first-page": "83",
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      "article-title": "Heteromerous interactions among glycolytic enzymes and of glycolytic enzymes with F-actin: effects of polyethylene glycol",
      "volume": "952",
      "author": "Walsh",
      "year": "1988",
      "journal-title": "Biochim. biophys. Acta"
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      "DOI": "10.1042/bj1650165",
      "article-title": "Modification of the kinetic parameters of aldolase on binding to the actin-containing filaments of skeletal muscle",
      "volume": "165",
      "author": "Walsh",
      "year": "1977",
      "journal-title": "Biochem. 7"
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      "DOI": "10.1073/pnas.79.15.4660",
      "article-title": "Mobility of cytoplasmic and membrane-associated actin in living cells",
      "volume": "79",
      "author": "Wang",
      "year": "1982",
      "journal-title": "Proc. natn. Acad. Sci. U.SA"
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      "first-page": "103",
      "DOI": "10.1016/0079-6107(78)90019-6",
      "article-title": "On the role of organized multienzyme systems in cellular metabolism: a general synthesis",
      "volume": "32",
      "author": "Welch",
      "year": "1977",
      "journal-title": "Prog. Biophvs. molec. Biol"
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      "DOI": "10.1016/S0006-3495(82)84459-7",
      "article-title": "Lateral mobility in membranes as detected by fluorescence recovery after photobleaching",
      "volume": "39",
      "author": "Yguerabide",
      "year": "1982",
      "journal-title": "Biophvs. J"
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