DOI: 10.1126/science.2658062. The Neuronal Growth-Associated Protein GAP-43 Induces Filopodia in Non-Neuronal Cells

The Neuronal Growth-Associated Protein GAP-43 Induces Filopodia in Non-Neuronal Cells

10.1126/science.2658062

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The neuron-specific protein GAP-43 is associated with the membrane of the nerve growth cone and thus may be important to the activity of this distinctive neuronal structure. Transient transfection of COS and NIH 3T3 cells with appropriate vectors resulted in expression of GAP-43 in these non-neuronal cells; as in neurons, transfected GAP-43 associated with the membrane. In addition, many long fine filopodial processes extended from the periphery of such transfected cells. Stable CHO cell lines expressing GAP-43 also exhibited processes that were more numerous, far longer, and more complex than those of CHO cell lines not transfected or transfected with control plasmids. Thus GAP-43 may directly contribute to growth cone activity by regulating cell membrane structure and enhancing extension of filopodial processes.

Bibliography

Zuber, M. X., Goodman, D. W., Karns, L. R., & Fishman, M. C. (1989). The Neuronal Growth-Associated Protein GAP-43 Induces Filopodia in Non-Neuronal Cells. Science, 244(4909), 1193â1195.

Authors 4

Mauricio X. Zuber (first)
Daniel W. Goodman (additional)
Larry R. Karns (additional)
Mark C. Fishman (additional)

References 33 Referenced 181

AKERS, R.F., CALCIUM-PROMOTED TRANSLOCATION OF PROTEIN-KINASE-C TO SYNAPTIC-MEMBRANES - RELATION TO THE PHOSPHORYLATION OF AN ENDOGENOUS SUBSTRATE (PROTEIN-F1) INVOLVED IN SYNAPTIC PLASTICITY, JOURNAL OF NEUROSCIENCE 7: 3976 (1987). (10.1523/JNEUROSCI.07-12-03976.1987) / JOURNAL OF NEUROSCIENCE (1987)
ALEXANDER, K.A., IDENTIFICATION AND CHARACTERIZATION OF THE CALMODULIN-BINDING DOMAIN OF NEUROMODULIN, A NEUROSPECIFIC CALMODULIN-BINDING PROTEIN, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 7544 (1988). (10.1016/S0021-9258(18)68533-3) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
Allred, L. E., Surfaces of Normal and Malignant Cells: 21 (1979). / Surfaces of Normal and Malignant Cells (1979)
ANDREASEN, T.J., PURIFICATION OF A NOVEL CALMODULIN BINDING-PROTEIN FROM BOVINE CEREBRAL-CORTEX MEMBRANES, BIOCHEMISTRY 22: 4615 (1983). (10.1021/bi00289a001) / BIOCHEMISTRY (1983)
Ausubel, F. M., Current Protocols in Molecular Biology 1: 9.0.1 (1987). / Current Protocols in Molecular Biology (1987)
BENOWITZ, L.I., SPECIFIC CHANGES IN RAPIDLY TRANSPORTED PROTEINS DURING REGENERATION OF THE GOLDFISH OPTIC-NERVE, JOURNAL OF NEUROSCIENCE 1: 300 (1981). (10.1523/JNEUROSCI.01-03-00300.1981) / JOURNAL OF NEUROSCIENCE (1981)
BENOWITZ, L.I., ANATOMICAL DISTRIBUTION OF THE GROWTH-ASSOCIATED PROTEIN GAP-43/B-50 IN THE ADULT-RAT BRAIN, JOURNAL OF NEUROSCIENCE 8: 339 (1988). (10.1523/JNEUROSCI.08-01-00339.1988) / JOURNAL OF NEUROSCIENCE (1988)
BENOWITZ, L.I., A MEMBRANE PHOSPHOPROTEIN ASSOCIATED WITH NEURAL DEVELOPMENT, AXONAL REGENERATION, PHOSPHOLIPID-METABOLISM, AND SYNAPTIC PLASTICITY, TRENDS IN NEUROSCIENCES 10: 527 (1987). (10.1016/0166-2236(87)90135-4) / TRENDS IN NEUROSCIENCES (1987)
10.1126/science.3277283
DEGRAAN, PNE, PHOSPHOPROTEIN B-50 IN NERVE GROWTH CONES FROM FETAL-RAT BRAIN, NEUROSCIENCE LETTERS 61: 235 (1985). (10.1016/0304-3940(85)90470-7) / NEUROSCIENCE LETTERS (1985)
de la Monte, S. M., Developmental Brain Research 46: 161 (1989). (10.1016/0165-3806(89)90279-4) / Developmental Brain Research (1989)
DELLAVALLE, G, CELL-TRANSFORMATION MEDIATED BY CHROMOSOMAL DEOXYRIBONUCLEIC-ACID OF POLYOMA VIRUS-TRANSFORMED CELLS, MOLECULAR AND CELLULAR BIOLOGY 1: 418 (1981). / MOLECULAR AND CELLULAR BIOLOGY (1981)
FEDEROFF, H.J., DUAL REGULATION OF GAP-43 GENE-EXPRESSION BY NERVE GROWTH-FACTOR AND GLUCOCORTICOIDS, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 19290 (1988). (10.1016/S0021-9258(19)77633-9) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
Fishman M. C. Assembly of the Nervous System (1989).
GLUZMAN, Y, SV40-TRANSFORMED SIMIAN CELLS SUPPORT THE REPLICATION OF EARLY SV40 MUTANTS, CELL 23: 175 (1981). (10.1016/0092-8674(81)90282-8) / CELL (1981)
10.1126/science.2437653
KATZ, F, NERVE GROWTH CONES ISOLATED FROM FETAL-RAT BRAIN .3. CALCIUM-DEPENDENT PROTEIN-PHOSPHORYLATION, JOURNAL OF NEUROSCIENCE 5: 1402 (1985). (10.1523/JNEUROSCI.05-06-01402.1985) / JOURNAL OF NEUROSCIENCE (1985)
MEIRI, K.F., DISTRIBUTION AND PHOSPHORYLATION OF THE GROWTH-ASSOCIATED PROTEIN GAP-43 IN REGENERATING SYMPATHETIC NEURONS IN CULTURE, JOURNAL OF NEUROSCIENCE 8: 2571 (1988). (10.1523/JNEUROSCI.08-07-02571.1988) / JOURNAL OF NEUROSCIENCE (1988)
MEIRI, K.F., GROWTH-ASSOCIATED PROTEIN, GAP-43, A POLYPEPTIDE THAT IS INDUCED WHEN NEURONS EXTEND AXONS, IS A COMPONENT OF GROWTH CONES AND CORRESPONDS TO PP46, A MAJOR POLYPEPTIDE OF A SUBCELLULAR FRACTION ENRICHED IN GROWTH CONES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 3537 (1986). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1986)
NEVE, R.L., GROWTH-ASSOCIATED PROTEIN GAP-43 IS EXPRESSED SELECTIVELY IN ASSOCIATIVE REGIONS OF THE ADULT HUMAN-BRAIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 3638 (1988). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1988)
NG, S.C., CLONING OF HUMAN GAP-43 - GROWTH ASSOCIATION AND ISCHEMIC RESURGENCE, NEURON 1: 133 (1988). (10.1016/0896-6273(88)90197-3) / NEURON (1988)
ROSENTHAL, A, PRIMARY STRUCTURE AND MESSENGER-RNA LOCALIZATION OF PROTEIN-F1, A GROWTH-RELATED PROTEIN-KINASE-C SUBSTRATE ASSOCIATED WITH SYNAPTIC PLASTICITY, EMBO JOURNAL 6: 3641 (1987). (10.1002/j.1460-2075.1987.tb02696.x) / EMBO JOURNAL (1987)
SEED B COMMUNICATION.
10.1038/329840a0
SEED, B, MOLECULAR-CLONING OF THE CD2 ANTIGEN, THE T-CELL ERYTHROCYTE RECEPTOR, BY A RAPID IMMUNOSELECTION PROCEDURE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 84: 3365 (1987). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1987)
SKENE, JHP, CHANGES IN AXONALLY TRANSPORTED PROTEINS DURING AXON REGENERATION IN TOAD RETINAL GANGLION-CELLS, JOURNAL OF CELL BIOLOGY 89: 86 (1981). (10.1083/jcb.89.1.86) / JOURNAL OF CELL BIOLOGY (1981)
SKENE, JHP, AXONALLY TRANSPORTED PROTEINS ASSOCIATED WITH AXON GROWTH IN RABBIT CENTRAL AND PERIPHERAL NERVOUS SYSTEMS, JOURNAL OF CELL BIOLOGY 89: 96 (1981). (10.1083/jcb.89.1.96) / JOURNAL OF CELL BIOLOGY (1981)
10.1126/science.3738509
10.1126/science.3055292
Trinkuns, J. P., Biology of the Nerve Growth Cone: 1 (1988). / Biology of the Nerve Growth Cone (1988)
Van Doren, K., Journal of Virology 50: 606 (1984). (10.1128/jvi.50.2.606-614.1984) / Journal of Virology (1984)
VANHOOFF, COM, B-50 PHOSPHORYLATION AND POLYPHOSPHOINOSITIDE METABOLISM IN NERVE GROWTH CONE MEMBRANES, JOURNAL OF NEUROSCIENCE 8: 1789 (1988). (10.1523/JNEUROSCI.08-05-01789.1988) / JOURNAL OF NEUROSCIENCE (1988)
10.1126/science.3535074

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 5:21 p.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 5:37 p.m.)
Indexed	1 year, 1 month ago (July 10, 2024, 4:31 p.m.)
Issued	36 years, 2 months ago (June 9, 1989)
Published	36 years, 2 months ago (June 9, 1989)
Published Print	36 years, 2 months ago (June 9, 1989)

Funders 0

None

BibTeX

@article{Zuber_1989, title={The Neuronal Growth-Associated Protein GAP-43 Induces Filopodia in Non-Neuronal Cells}, volume={244}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2658062}, DOI={10.1126/science.2658062}, number={4909}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Zuber, Mauricio X. and Goodman, Daniel W. and Karns, Larry R. and Fishman, Mark C.}, year={1989}, month=jun, pages={1193–1195} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        7,
        10
      ]
    ],
    "date-time": "2024-07-10T20:31:47Z",
    "timestamp": 1720643507074
  },
  "reference-count": 33,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "4909",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1989,
        6,
        9
      ]
    ]
  },
  "abstract": "<jats:p>The neuron-specific protein GAP-43 is associated with the membrane of the nerve growth cone and thus may be important to the activity of this distinctive neuronal structure. Transient transfection of COS and NIH 3T3 cells with appropriate vectors resulted in expression of GAP-43 in these non-neuronal cells; as in neurons, transfected GAP-43 associated with the membrane. In addition, many long fine filopodial processes extended from the periphery of such transfected cells. Stable CHO cell lines expressing GAP-43 also exhibited processes that were more numerous, far longer, and more complex than those of CHO cell lines not transfected or transfected with control plasmids. Thus GAP-43 may directly contribute to growth cone activity by regulating cell membrane structure and enhancing extension of filopodial processes.</jats:p>",
  "DOI": "10.1126/science.2658062",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T21:21:28Z",
    "timestamp": 1160083288000
  },
  "page": "1193-1195",
  "source": "Crossref",
  "is-referenced-by-count": 181,
  "title": "The Neuronal Growth-Associated Protein GAP-43 Induces Filopodia in Non-Neuronal Cells",
  "prefix": "10.1126",
  "volume": "244",
  "author": [
    {
      "given": "Mauricio X.",
      "family": "Zuber",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Developmental Biology Laboratory, Massachusetts General Hospital Cancer Center, and the Howard Hughes Medical Institute, Massachusetts General Hospital, Boston, MA 02114, and Harvard Medical School, Boston, MA 02115."
        }
      ]
    },
    {
      "given": "Daniel W.",
      "family": "Goodman",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Developmental Biology Laboratory, Massachusetts General Hospital Cancer Center, and the Howard Hughes Medical Institute, Massachusetts General Hospital, Boston, MA 02114, and Harvard Medical School, Boston, MA 02115."
        }
      ]
    },
    {
      "given": "Larry R.",
      "family": "Karns",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Developmental Biology Laboratory, Massachusetts General Hospital Cancer Center, and the Howard Hughes Medical Institute, Massachusetts General Hospital, Boston, MA 02114, and Harvard Medical School, Boston, MA 02115."
        }
      ]
    },
    {
      "given": "Mark C.",
      "family": "Fishman",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Developmental Biology Laboratory, Massachusetts General Hospital Cancer Center, and the Howard Hughes Medical Institute, Massachusetts General Hospital, Boston, MA 02114, and Harvard Medical School, Boston, MA 02115."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "3976",
      "DOI": "10.1523/JNEUROSCI.07-12-03976.1987",
      "volume": "7",
      "year": "1987",
      "unstructured": "AKERS, R.F., CALCIUM-PROMOTED TRANSLOCATION OF PROTEIN-KINASE-C TO SYNAPTIC-MEMBRANES - RELATION TO THE PHOSPHORYLATION OF AN ENDOGENOUS SUBSTRATE (PROTEIN-F1) INVOLVED IN SYNAPTIC PLASTICITY, JOURNAL OF NEUROSCIENCE 7: 3976 (1987).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "7544",
      "DOI": "10.1016/S0021-9258(18)68533-3",
      "volume": "263",
      "year": "1988",
      "unstructured": "ALEXANDER, K.A., IDENTIFICATION AND CHARACTERIZATION OF THE CALMODULIN-BINDING DOMAIN OF NEUROMODULIN, A NEUROSPECIFIC CALMODULIN-BINDING PROTEIN, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 7544 (1988).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_3_1",
      "first-page": "21",
      "year": "1979",
      "unstructured": "Allred, L. E., Surfaces of Normal and Malignant Cells: 21 (1979).",
      "journal-title": "Surfaces of Normal and Malignant Cells"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "4615",
      "DOI": "10.1021/bi00289a001",
      "volume": "22",
      "year": "1983",
      "unstructured": "ANDREASEN, T.J., PURIFICATION OF A NOVEL CALMODULIN BINDING-PROTEIN FROM BOVINE CEREBRAL-CORTEX MEMBRANES, BIOCHEMISTRY 22: 4615 (1983).",
      "journal-title": "BIOCHEMISTRY"
    },
    {
      "key": "e_1_2_1_5_1",
      "first-page": "9.0.1",
      "volume": "1",
      "year": "1987",
      "unstructured": "Ausubel, F. M., Current Protocols in Molecular Biology 1: 9.0.1 (1987).",
      "journal-title": "Current Protocols in Molecular Biology"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "300",
      "DOI": "10.1523/JNEUROSCI.01-03-00300.1981",
      "volume": "1",
      "year": "1981",
      "unstructured": "BENOWITZ, L.I., SPECIFIC CHANGES IN RAPIDLY TRANSPORTED PROTEINS DURING REGENERATION OF THE GOLDFISH OPTIC-NERVE, JOURNAL OF NEUROSCIENCE 1: 300 (1981).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "339",
      "DOI": "10.1523/JNEUROSCI.08-01-00339.1988",
      "volume": "8",
      "year": "1988",
      "unstructured": "BENOWITZ, L.I., ANATOMICAL DISTRIBUTION OF THE GROWTH-ASSOCIATED PROTEIN GAP-43/B-50 IN THE ADULT-RAT BRAIN, JOURNAL OF NEUROSCIENCE 8: 339 (1988).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "527",
      "DOI": "10.1016/0166-2236(87)90135-4",
      "volume": "10",
      "year": "1987",
      "unstructured": "BENOWITZ, L.I., A MEMBRANE PHOSPHOPROTEIN ASSOCIATED WITH NEURAL DEVELOPMENT, AXONAL REGENERATION, PHOSPHOLIPID-METABOLISM, AND SYNAPTIC PLASTICITY, TRENDS IN NEUROSCIENCES 10: 527 (1987).",
      "journal-title": "TRENDS IN NEUROSCIENCES"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3277283"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "235",
      "DOI": "10.1016/0304-3940(85)90470-7",
      "volume": "61",
      "year": "1985",
      "unstructured": "DEGRAAN, PNE, PHOSPHOPROTEIN B-50 IN NERVE GROWTH CONES FROM FETAL-RAT BRAIN, NEUROSCIENCE LETTERS 61: 235 (1985).",
      "journal-title": "NEUROSCIENCE LETTERS"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "crossref",
      "first-page": "161",
      "DOI": "10.1016/0165-3806(89)90279-4",
      "volume": "46",
      "year": "1989",
      "unstructured": "de la Monte, S. M., Developmental Brain Research 46: 161 (1989).",
      "journal-title": "Developmental Brain Research"
    },
    {
      "key": "e_1_2_1_12_1",
      "first-page": "418",
      "volume": "1",
      "year": "1981",
      "unstructured": "DELLAVALLE, G, CELL-TRANSFORMATION MEDIATED BY CHROMOSOMAL DEOXYRIBONUCLEIC-ACID OF POLYOMA VIRUS-TRANSFORMED CELLS, MOLECULAR AND CELLULAR BIOLOGY 1: 418 (1981).",
      "journal-title": "MOLECULAR AND CELLULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "19290",
      "DOI": "10.1016/S0021-9258(19)77633-9",
      "volume": "263",
      "year": "1988",
      "unstructured": "FEDEROFF, H.J., DUAL REGULATION OF GAP-43 GENE-EXPRESSION BY NERVE GROWTH-FACTOR AND GLUCOCORTICOIDS, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 19290 (1988).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_14_1",
      "unstructured": "Fishman M. C. Assembly of the Nervous System (1989)."
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "175",
      "DOI": "10.1016/0092-8674(81)90282-8",
      "volume": "23",
      "year": "1981",
      "unstructured": "GLUZMAN, Y, SV40-TRANSFORMED SIMIAN CELLS SUPPORT THE REPLICATION OF EARLY SV40 MUTANTS, CELL 23: 175 (1981).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2437653"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "crossref",
      "first-page": "1402",
      "DOI": "10.1523/JNEUROSCI.05-06-01402.1985",
      "volume": "5",
      "year": "1985",
      "unstructured": "KATZ, F, NERVE GROWTH CONES ISOLATED FROM FETAL-RAT BRAIN .3. CALCIUM-DEPENDENT PROTEIN-PHOSPHORYLATION, JOURNAL OF NEUROSCIENCE 5: 1402 (1985).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "crossref",
      "first-page": "2571",
      "DOI": "10.1523/JNEUROSCI.08-07-02571.1988",
      "volume": "8",
      "year": "1988",
      "unstructured": "MEIRI, K.F., DISTRIBUTION AND PHOSPHORYLATION OF THE GROWTH-ASSOCIATED PROTEIN GAP-43 IN REGENERATING SYMPATHETIC NEURONS IN CULTURE, JOURNAL OF NEUROSCIENCE 8: 2571 (1988).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_19_1",
      "first-page": "3537",
      "volume": "83",
      "year": "1986",
      "unstructured": "MEIRI, K.F., GROWTH-ASSOCIATED PROTEIN, GAP-43, A POLYPEPTIDE THAT IS INDUCED WHEN NEURONS EXTEND AXONS, IS A COMPONENT OF GROWTH CONES AND CORRESPONDS TO PP46, A MAJOR POLYPEPTIDE OF A SUBCELLULAR FRACTION ENRICHED IN GROWTH CONES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 3537 (1986).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_20_1",
      "first-page": "3638",
      "volume": "85",
      "year": "1988",
      "unstructured": "NEVE, R.L., GROWTH-ASSOCIATED PROTEIN GAP-43 IS EXPRESSED SELECTIVELY IN ASSOCIATIVE REGIONS OF THE ADULT HUMAN-BRAIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 3638 (1988).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "133",
      "DOI": "10.1016/0896-6273(88)90197-3",
      "volume": "1",
      "year": "1988",
      "unstructured": "NG, S.C., CLONING OF HUMAN GAP-43 - GROWTH ASSOCIATION AND ISCHEMIC RESURGENCE, NEURON 1: 133 (1988).",
      "journal-title": "NEURON"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "3641",
      "DOI": "10.1002/j.1460-2075.1987.tb02696.x",
      "volume": "6",
      "year": "1987",
      "unstructured": "ROSENTHAL, A, PRIMARY STRUCTURE AND MESSENGER-RNA LOCALIZATION OF PROTEIN-F1, A GROWTH-RELATED PROTEIN-KINASE-C SUBSTRATE ASSOCIATED WITH SYNAPTIC PLASTICITY, EMBO JOURNAL 6: 3641 (1987).",
      "journal-title": "EMBO JOURNAL"
    },
    {
      "key": "e_1_2_1_23_1",
      "unstructured": "SEED B COMMUNICATION."
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/329840a0"
    },
    {
      "key": "e_1_2_1_25_1",
      "first-page": "3365",
      "volume": "84",
      "year": "1987",
      "unstructured": "SEED, B, MOLECULAR-CLONING OF THE CD2 ANTIGEN, THE T-CELL ERYTHROCYTE RECEPTOR, BY A RAPID IMMUNOSELECTION PROCEDURE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 84: 3365 (1987).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "86",
      "DOI": "10.1083/jcb.89.1.86",
      "volume": "89",
      "year": "1981",
      "unstructured": "SKENE, JHP, CHANGES IN AXONALLY TRANSPORTED PROTEINS DURING AXON REGENERATION IN TOAD RETINAL GANGLION-CELLS, JOURNAL OF CELL BIOLOGY 89: 86 (1981).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "96",
      "DOI": "10.1083/jcb.89.1.96",
      "volume": "89",
      "year": "1981",
      "unstructured": "SKENE, JHP, AXONALLY TRANSPORTED PROTEINS ASSOCIATED WITH AXON GROWTH IN RABBIT CENTRAL AND PERIPHERAL NERVOUS SYSTEMS, JOURNAL OF CELL BIOLOGY 89: 96 (1981).",
      "journal-title": "JOURNAL OF CELL BIOLOGY"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3738509"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3055292"
    },
    {
      "key": "e_1_2_1_30_1",
      "first-page": "1",
      "year": "1988",
      "unstructured": "Trinkuns, J. P., Biology of the Nerve Growth Cone: 1 (1988).",
      "journal-title": "Biology of the Nerve Growth Cone"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "crossref",
      "first-page": "606",
      "DOI": "10.1128/jvi.50.2.606-614.1984",
      "volume": "50",
      "year": "1984",
      "unstructured": "Van Doren, K., Journal of Virology 50: 606 (1984).",
      "journal-title": "Journal of Virology"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "crossref",
      "first-page": "1789",
      "DOI": "10.1523/JNEUROSCI.08-05-01789.1988",
      "volume": "8",
      "year": "1988",
      "unstructured": "VANHOOFF, COM, B-50 PHOSPHORYLATION AND POLYPHOSPHOINOSITIDE METABOLISM IN NERVE GROWTH CONE MEMBRANES, JOURNAL OF NEUROSCIENCE 8: 1789 (1988).",
      "journal-title": "JOURNAL OF NEUROSCIENCE"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3535074"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.2658062",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        12
      ]
    ],
    "date-time": "2024-01-12T22:37:49Z",
    "timestamp": 1705099069000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.2658062"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1989,
        6,
        9
      ]
    ]
  },
  "references-count": 33,
  "journal-issue": {
    "issue": "4909",
    "published-print": {
      "date-parts": [
        [
          1989,
          6,
          9
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.2658062"
  ],
  "URL": "http://dx.doi.org/10.1126/science.2658062",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1989,
        6,
        9
      ]
    ]
  }
}