DOI: 10.1083/jcb.200304023. A mutant heterodimeric myosin with one inactive head generates maximal displacement

A mutant heterodimeric myosin with one inactive head generates maximal displacement

10.1083/jcb.200304023

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Each of the heads of the motor protein myosin II is capable of supporting motion. A previous report showed that double-headed myosin generates twice the displacement of single-headed myosin (Tyska, M.J., D.E. Dupuis, W.H. Guilford, J.B. Patlak, G.S. Waller, K.M. Trybus, D.M. Warshaw, and S. Lowey. 1999. Proc. Natl. Acad. Sci. USA. 96:4402–4407). To determine the role of the second head, we expressed a smooth muscle heterodimeric heavy meromyosin (HMM) with one wild-type head, and the other locked in a weak actin-binding state by introducing a point mutation in switch II (E470A). Homodimeric E470A HMM did not support in vitro motility, and only slowly hydrolyzed MgATP. Optical trap measurements revealed that the heterodimer generated unitary displacements of 10.4 nm, strikingly similar to wild-type HMM (10.2 nm) and approximately twice that of single-headed subfragment-1 (4.4 nm). These data show that a double-headed molecule can achieve a working stroke of ∼10 nm with only one active head and an inactive weak-binding partner. We propose that the second head optimizes the orientation and/or stabilizes the structure of the motion-generating head, thereby resulting in maximum displacement.

Bibliography

Kad, N. M., Rovner, A. S., Fagnant, P. M., Joel, P. B., Kennedy, G. G., Patlak, J. B., Warshaw, D. M., & Trybus, K. M. (2003). A mutant heterodimeric myosin with one inactive head generates maximal displacement. The Journal of Cell Biology, 162(3), 481â488.

Authors 8

Neil M. Kad (first)
Arthur S. Rovner (additional)
Patricia M. Fagnant (additional)
Peteranne B. Joel (additional)
Guy G. Kennedy (additional)
Joseph B. Patlak (additional)
David M. Warshaw (additional)
Kathleen M. Trybus (additional)

References 68 Referenced 43

10.1002/j.1460-2075.1996.tb00995.x / EMBO J. (1996)
10.1073/pnas.95.6.2944 / Proc. Natl. Acad. Sci. USA. (1998)
10.1016/S0006-3495(98)77581-2 / Biophys. J. (1998)
10.1016/0022-2836(78)90424-2 / J. Mol. Biol. (1978)
10.1038/22704 / Nature (1999)
10.1074/jbc.270.5.2171 / J. Biol. Chem. (1995)
10.1042/bj2320343 / Biochem. J. (1985)
10.1016/S0092-8674(00)81598-6 / Cell. (1998)
10.1023/A:1018672631256 / J. Muscle Res. Cell Motil. (1997)
10.1038/368113a0 / Nature. (1994)
{'key': '2023072908344823900_BIB11', 'first-page': '194S', 'volume': '68', 'year': '1995', 'journal-title': 'Biophys. J.'} / Biophys. J. (1995)
10.1016/S0006-3495(97)78753-8 / Biophys. J. (1997)
10.1038/326805a0 / Nature. (1987)
10.1007/BF00123828 / J. Muscle Res. Cell Motil. (1994)
10.1073/pnas.200376897 / Proc. Natl. Acad. Sci. USA. (2000)
10.1007/BF00713057 / J. Muscle Res. Cell Motil. (1985)
10.1016/S0006-3495(99)77262-0 / Biophys. J. (1999)
10.1074/jbc.M006930200 / J. Biol. Chem. (2001)
{'key': '2023072908344823900_BIB19'}
10.1006/jmbi.1998.1715 / J. Mol. Biol. (1998)
10.1083/jcb.134.3.675 / J. Cell Biol. (1996)
10.1021/bi990081f / Biochemistry. (1999)
10.1023/A:1005489501357 / J. Muscle Res. Cell Motil. (1998)
10.1016/S0006-3495(01)76159-0 / Biophys. J. (2001)
{'key': '2023072908344823900_BIB25', 'volume': 'In press', 'year': '2003', 'journal-title': 'J. Biol. Chem.'} / J. Biol. Chem. (2003)
10.1073/pnas.232161999 / Proc. Natl. Acad. Sci. USA. (2002)
10.1083/jcb.113.2.303 / J. Cell Biol. (1991)
10.1016/0022-2836(73)90376-8 / J. Mol. Biol. (1973)
10.1021/bi00618a017 / Biochemistry. (1978)
10.1016/0022-2836(80)90050-9 / J. Mol. Biol. (1980)
10.1126/science.279.5350.527 / Science. (1998)
10.1038/378209a0 / Nature. (1995)
10.1016/0022-2836(92)90114-Y / J. Mol. Biol. (1992)
10.1006/bbrc.2001.6142 / Biochem. Biophys. Res. Commun. (2002)
10.1016/S0006-3495(00)76350-8 / Biophys. J. (2000)
10.1021/bi00430a070 / Biochemistry. (1989)
10.1073/pnas.95.12.6653 / Proc. Natl. Acad. Sci. USA. (1998)
10.1007/978-1-4684-6039-1_12 / Adv. Exp. Med. Biol. (1998)
10.1016/S0006-3495(93)81041-5 / Biophys. J. (1993)
10.1042/bj1190031 / Biochem. J. (1970)
10.1073/pnas.182539599 / Proc. Natl. Acad. Sci. USA. (2002)
10.1126/science.8316857 / Science. (1993)
10.1073/pnas.191512398 / Proc. Natl. Acad. Sci. USA. (2001)
10.1074/jbc.270.51.30260 / J. Biol. Chem. (1995)
10.1023/A:1018689102122 / J. Muscle Res. Cell Motil. (1997)
{'key': '2023072908344823900_BIB46'}
10.1038/84962 / Nat. Struct. Biol. (2001)
10.1074/jbc.273.32.20334 / J. Biol. Chem. (1998)
{'key': '2023072908344823900_BIB49', 'first-page': '159', 'volume': '8', 'year': '1991', 'journal-title': 'Mol. Biol. Med.'} / Mol. Biol. Med. (1991)
10.1126/science.2377894 / Science. (1990)
10.1074/jbc.M010887200 / J. Biol. Chem. (2001)
10.1038/24640 / Nature. (1998)
10.1016/S0006-3495(98)77629-5 / Biophys. J. (1998)
10.1038/328536a0 / Nature. (1987)
10.1038/341154a0 / Nature. (1989)
10.1006/meth.2000.1085 / Methods. (2000)
10.1083/jcb.109.6.2879 / J. Cell Biol. (1989)
10.1073/pnas.96.8.4402 / Proc. Natl. Acad. Sci. USA. (1999)
10.1161/01.RES.86.7.737 / Circ. Res. (2000)
10.1073/pnas.93.9.4459 / Proc. Natl. Acad. Sci. USA. (1996)
10.1016/S0006-3495(98)74061-5 / Biophys. J. (1998)
10.1038/ncb732 / Nat. Cell Biol. (2002)
10.1083/jcb.111.2.453 / J. Cell Biol. (1990)
10.1083/jcb.147.7.1385 / J. Cell Biol. (1999)
10.1073/pnas.071051098 / Proc. Natl. Acad. Sci. USA. (2001)
10.1007/BF00154058 / J. Muscle Res. Cell Motil. (1996)
10.1016/S0006-3495(93)81388-2 / Biophys. J. (1993)
10.1016/0022-2836(87)90302-0 / J. Mol. Biol. (1987)

Dates

Type	When
Created	22 years, 1 month ago (Aug. 4, 2003, 3:54 p.m.)
Deposited	2 years, 1 month ago (July 29, 2023, 4:35 a.m.)
Indexed	1 month, 4 weeks ago (July 8, 2025, 7:30 a.m.)
Issued	22 years, 1 month ago (Aug. 4, 2003)
Published	22 years, 1 month ago (Aug. 4, 2003)
Published Online	22 years, 1 month ago (Aug. 4, 2003)
Published Print	22 years, 1 month ago (Aug. 4, 2003)

Funders 0

None

BibTeX

@article{Kad_2003, title={A mutant heterodimeric myosin with one inactive head generates maximal displacement}, volume={162}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200304023}, DOI={10.1083/jcb.200304023}, number={3}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Kad, Neil M. and Rovner, Arthur S. and Fagnant, Patricia M. and Joel, Peteranne B. and Kennedy, Guy G. and Patlak, Joseph B. and Warshaw, David M. and Trybus, Kathleen M.}, year={2003}, month=aug, pages={481–488} }

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  "abstract": "<jats:p>Each of the heads of the motor protein myosin II is capable of supporting motion. A previous report showed that double-headed myosin generates twice the displacement of single-headed myosin (Tyska, M.J., D.E. Dupuis, W.H. Guilford, J.B. Patlak, G.S. Waller, K.M. Trybus, D.M. Warshaw, and S. Lowey. 1999. Proc. Natl. Acad. Sci. USA. 96:4402\u20134407). To determine the role of the second head, we expressed a smooth muscle heterodimeric heavy meromyosin (HMM) with one wild-type head, and the other locked in a weak actin-binding state by introducing a point mutation in switch II (E470A). Homodimeric E470A HMM did not support in vitro motility, and only slowly hydrolyzed MgATP. Optical trap measurements revealed that the heterodimer generated unitary displacements of 10.4 nm, strikingly similar to wild-type HMM (10.2 nm) and approximately twice that of single-headed subfragment-1 (4.4 nm). These data show that a double-headed molecule can achieve a working stroke of \u223c10 nm with only one active head and an inactive weak-binding partner. We propose that the second head optimizes the orientation and/or stabilizes the structure of the motion-generating head, thereby resulting in maximum displacement.</jats:p>",
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    {
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      "first-page": "2944",
      "DOI": "10.1073/pnas.95.6.2944",
      "volume": "95",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB3",
      "doi-asserted-by": "crossref",
      "first-page": "926",
      "DOI": "10.1016/S0006-3495(98)77581-2",
      "volume": "75",
      "year": "1998",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB4",
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      "first-page": "361",
      "DOI": "10.1016/0022-2836(78)90424-2",
      "volume": "120",
      "year": "1978",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072908344823900_BIB5",
      "doi-asserted-by": "crossref",
      "first-page": "425",
      "DOI": "10.1038/22704",
      "volume": "400",
      "year": "1999",
      "journal-title": "Nature"
    },
    {
      "key": "2023072908344823900_BIB6",
      "doi-asserted-by": "crossref",
      "first-page": "2171",
      "DOI": "10.1074/jbc.270.5.2171",
      "volume": "270",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072908344823900_BIB7",
      "doi-asserted-by": "crossref",
      "first-page": "343",
      "DOI": "10.1042/bj2320343",
      "volume": "232",
      "year": "1985",
      "journal-title": "Biochem. J."
    },
    {
      "key": "2023072908344823900_BIB8",
      "doi-asserted-by": "crossref",
      "first-page": "559",
      "DOI": "10.1016/S0092-8674(00)81598-6",
      "volume": "94",
      "year": "1998",
      "journal-title": "Cell."
    },
    {
      "key": "2023072908344823900_BIB9",
      "doi-asserted-by": "crossref",
      "first-page": "17",
      "DOI": "10.1023/A:1018672631256",
      "volume": "18",
      "year": "1997",
      "journal-title": "J. Muscle Res. Cell Motil."
    },
    {
      "key": "2023072908344823900_BIB10",
      "doi-asserted-by": "crossref",
      "first-page": "113",
      "DOI": "10.1038/368113a0",
      "volume": "368",
      "year": "1994",
      "journal-title": "Nature."
    },
    {
      "key": "2023072908344823900_BIB11",
      "first-page": "194S",
      "volume": "68",
      "year": "1995",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB12",
      "doi-asserted-by": "crossref",
      "first-page": "1006",
      "DOI": "10.1016/S0006-3495(97)78753-8",
      "volume": "72",
      "year": "1997",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB13",
      "doi-asserted-by": "crossref",
      "first-page": "805",
      "DOI": "10.1038/326805a0",
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      "year": "1987",
      "journal-title": "Nature."
    },
    {
      "key": "2023072908344823900_BIB14",
      "doi-asserted-by": "crossref",
      "first-page": "11",
      "DOI": "10.1007/BF00123828",
      "volume": "15",
      "year": "1994",
      "journal-title": "J. Muscle Res. Cell Motil."
    },
    {
      "key": "2023072908344823900_BIB15",
      "doi-asserted-by": "crossref",
      "first-page": "11238",
      "DOI": "10.1073/pnas.200376897",
      "volume": "97",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB16",
      "doi-asserted-by": "crossref",
      "first-page": "153",
      "DOI": "10.1007/BF00713057",
      "volume": "6",
      "year": "1985",
      "journal-title": "J. Muscle Res. Cell Motil."
    },
    {
      "key": "2023072908344823900_BIB17",
      "doi-asserted-by": "crossref",
      "first-page": "985",
      "DOI": "10.1016/S0006-3495(99)77262-0",
      "volume": "76",
      "year": "1999",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB18",
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      "first-page": "2998",
      "DOI": "10.1074/jbc.M006930200",
      "volume": "276",
      "year": "2001",
      "journal-title": "J. Biol. Chem."
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      "key": "2023072908344823900_BIB20",
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      "DOI": "10.1006/jmbi.1998.1715",
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      "year": "1998",
      "journal-title": "J. Mol. Biol."
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      "first-page": "675",
      "DOI": "10.1083/jcb.134.3.675",
      "volume": "134",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072908344823900_BIB22",
      "doi-asserted-by": "crossref",
      "first-page": "11670",
      "DOI": "10.1021/bi990081f",
      "volume": "38",
      "year": "1999",
      "journal-title": "Biochemistry."
    },
    {
      "key": "2023072908344823900_BIB23",
      "doi-asserted-by": "crossref",
      "first-page": "825",
      "DOI": "10.1023/A:1005489501357",
      "volume": "19",
      "year": "1998",
      "journal-title": "J. Muscle Res. Cell Motil."
    },
    {
      "key": "2023072908344823900_BIB24",
      "doi-asserted-by": "crossref",
      "first-page": "1900",
      "DOI": "10.1016/S0006-3495(01)76159-0",
      "volume": "80",
      "year": "2001",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB25",
      "volume": "In press",
      "year": "2003",
      "journal-title": "J. Biol. Chem."
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    {
      "key": "2023072908344823900_BIB26",
      "doi-asserted-by": "crossref",
      "first-page": "14801",
      "DOI": "10.1073/pnas.232161999",
      "volume": "99",
      "year": "2002",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB27",
      "doi-asserted-by": "crossref",
      "first-page": "303",
      "DOI": "10.1083/jcb.113.2.303",
      "volume": "113",
      "year": "1991",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072908344823900_BIB28",
      "doi-asserted-by": "crossref",
      "first-page": "313",
      "DOI": "10.1016/0022-2836(73)90376-8",
      "volume": "74",
      "year": "1973",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072908344823900_BIB29",
      "doi-asserted-by": "crossref",
      "first-page": "5431",
      "DOI": "10.1021/bi00618a017",
      "volume": "17",
      "year": "1978",
      "journal-title": "Biochemistry."
    },
    {
      "key": "2023072908344823900_BIB30",
      "doi-asserted-by": "crossref",
      "first-page": "573",
      "DOI": "10.1016/0022-2836(80)90050-9",
      "volume": "139",
      "year": "1980",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072908344823900_BIB31",
      "doi-asserted-by": "crossref",
      "first-page": "527",
      "DOI": "10.1126/science.279.5350.527",
      "volume": "279",
      "year": "1998",
      "journal-title": "Science."
    },
    {
      "key": "2023072908344823900_BIB32",
      "doi-asserted-by": "crossref",
      "first-page": "209",
      "DOI": "10.1038/378209a0",
      "volume": "378",
      "year": "1995",
      "journal-title": "Nature."
    },
    {
      "key": "2023072908344823900_BIB33",
      "doi-asserted-by": "crossref",
      "first-page": "1143",
      "DOI": "10.1016/0022-2836(92)90114-Y",
      "volume": "225",
      "year": "1992",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072908344823900_BIB34",
      "doi-asserted-by": "crossref",
      "first-page": "311",
      "DOI": "10.1006/bbrc.2001.6142",
      "volume": "290",
      "year": "2002",
      "journal-title": "Biochem. Biophys. Res. Commun."
    },
    {
      "key": "2023072908344823900_BIB35",
      "doi-asserted-by": "crossref",
      "first-page": "962",
      "DOI": "10.1016/S0006-3495(00)76350-8",
      "volume": "79",
      "year": "2000",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB36",
      "doi-asserted-by": "crossref",
      "first-page": "1898",
      "DOI": "10.1021/bi00430a070",
      "volume": "28",
      "year": "1989",
      "journal-title": "Biochemistry."
    },
    {
      "key": "2023072908344823900_BIB37",
      "doi-asserted-by": "crossref",
      "first-page": "6653",
      "DOI": "10.1073/pnas.95.12.6653",
      "volume": "95",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB38",
      "doi-asserted-by": "crossref",
      "first-page": "99",
      "DOI": "10.1007/978-1-4684-6039-1_12",
      "volume": "453",
      "year": "1998",
      "journal-title": "Adv. Exp. Med. Biol."
    },
    {
      "key": "2023072908344823900_BIB39",
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      "first-page": "29",
      "DOI": "10.1016/S0006-3495(93)81041-5",
      "volume": "65",
      "year": "1993",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB40",
      "doi-asserted-by": "crossref",
      "first-page": "31",
      "DOI": "10.1042/bj1190031",
      "volume": "119",
      "year": "1970",
      "journal-title": "Biochem. J."
    },
    {
      "key": "2023072908344823900_BIB41",
      "doi-asserted-by": "crossref",
      "first-page": "14159",
      "DOI": "10.1073/pnas.182539599",
      "volume": "99",
      "year": "2002",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB42",
      "doi-asserted-by": "crossref",
      "first-page": "50",
      "DOI": "10.1126/science.8316857",
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      "year": "1993",
      "journal-title": "Science."
    },
    {
      "key": "2023072908344823900_BIB43",
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      "first-page": "13655",
      "DOI": "10.1073/pnas.191512398",
      "volume": "98",
      "year": "2001",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB44",
      "doi-asserted-by": "crossref",
      "first-page": "30260",
      "DOI": "10.1074/jbc.270.51.30260",
      "volume": "270",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072908344823900_BIB45",
      "doi-asserted-by": "crossref",
      "first-page": "103",
      "DOI": "10.1023/A:1018689102122",
      "volume": "18",
      "year": "1997",
      "journal-title": "J. Muscle Res. Cell Motil."
    },
    {
      "key": "2023072908344823900_BIB46"
    },
    {
      "key": "2023072908344823900_BIB47",
      "doi-asserted-by": "crossref",
      "first-page": "226",
      "DOI": "10.1038/84962",
      "volume": "8",
      "year": "2001",
      "journal-title": "Nat. Struct. Biol."
    },
    {
      "key": "2023072908344823900_BIB48",
      "doi-asserted-by": "crossref",
      "first-page": "20334",
      "DOI": "10.1074/jbc.273.32.20334",
      "volume": "273",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072908344823900_BIB49",
      "first-page": "159",
      "volume": "8",
      "year": "1991",
      "journal-title": "Mol. Biol. Med."
    },
    {
      "key": "2023072908344823900_BIB50",
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      "first-page": "406",
      "DOI": "10.1126/science.2377894",
      "volume": "249",
      "year": "1990",
      "journal-title": "Science."
    },
    {
      "key": "2023072908344823900_BIB51",
      "doi-asserted-by": "crossref",
      "first-page": "19491",
      "DOI": "10.1074/jbc.M010887200",
      "volume": "276",
      "year": "2001",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072908344823900_BIB52",
      "doi-asserted-by": "crossref",
      "first-page": "380",
      "DOI": "10.1038/24640",
      "volume": "396",
      "year": "1998",
      "journal-title": "Nature."
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    {
      "key": "2023072908344823900_BIB53",
      "doi-asserted-by": "crossref",
      "first-page": "1886",
      "DOI": "10.1016/S0006-3495(98)77629-5",
      "volume": "75",
      "year": "1998",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB54",
      "doi-asserted-by": "crossref",
      "first-page": "536",
      "DOI": "10.1038/328536a0",
      "volume": "328",
      "year": "1987",
      "journal-title": "Nature."
    },
    {
      "key": "2023072908344823900_BIB55",
      "doi-asserted-by": "crossref",
      "first-page": "154",
      "DOI": "10.1038/341154a0",
      "volume": "341",
      "year": "1989",
      "journal-title": "Nature."
    },
    {
      "key": "2023072908344823900_BIB56",
      "doi-asserted-by": "crossref",
      "first-page": "327",
      "DOI": "10.1006/meth.2000.1085",
      "volume": "22",
      "year": "2000",
      "journal-title": "Methods."
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    {
      "key": "2023072908344823900_BIB57",
      "doi-asserted-by": "crossref",
      "first-page": "2879",
      "DOI": "10.1083/jcb.109.6.2879",
      "volume": "109",
      "year": "1989",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072908344823900_BIB58",
      "doi-asserted-by": "crossref",
      "first-page": "4402",
      "DOI": "10.1073/pnas.96.8.4402",
      "volume": "96",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB59",
      "doi-asserted-by": "crossref",
      "first-page": "737",
      "DOI": "10.1161/01.RES.86.7.737",
      "volume": "86",
      "year": "2000",
      "journal-title": "Circ. Res."
    },
    {
      "key": "2023072908344823900_BIB60",
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      "first-page": "4459",
      "DOI": "10.1073/pnas.93.9.4459",
      "volume": "93",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072908344823900_BIB61",
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      "first-page": "1424",
      "DOI": "10.1016/S0006-3495(98)74061-5",
      "volume": "75",
      "year": "1998",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072908344823900_BIB62",
      "doi-asserted-by": "crossref",
      "first-page": "59",
      "DOI": "10.1038/ncb732",
      "volume": "4",
      "year": "2002",
      "journal-title": "Nat. Cell Biol."
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    {
      "key": "2023072908344823900_BIB63",
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      "first-page": "453",
      "DOI": "10.1083/jcb.111.2.453",
      "volume": "111",
      "year": "1990",
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      "first-page": "1385",
      "DOI": "10.1083/jcb.147.7.1385",
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      "first-page": "4361",
      "DOI": "10.1073/pnas.071051098",
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      "DOI": "10.1007/BF00154058",
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      "DOI": "10.1016/S0006-3495(93)81388-2",
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      "first-page": "143",
      "DOI": "10.1016/0022-2836(87)90302-0",
      "volume": "198",
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