DOI: 10.1152/jappl.2001.91.2.534. Myogenic satellite cells: physiology to molecular biology

Myogenic satellite cells: physiology to molecular biology

10.1152/jappl.2001.91.2.534

Crossref journal-article

American Physiological Society

Journal of Applied Physiology (24)

Abstract

Adult skeletal muscle has a remarkable ability to regenerate following myotrauma. Because adult myofibers are terminally differentiated, the regeneration of skeletal muscle is largely dependent on a small population of resident cells termed satellite cells. Although this population of cells was identified 40 years ago, little is known regarding the molecular phenotype or regulation of the satellite cell. The use of cell culture techniques and transgenic animal models has improved our understanding of this unique cell population; however, the capacity and potential of these cells remain ill-defined. This review will highlight the origin and unique markers of the satellite cell population, the regulation by growth factors, and the response to physiological and pathological stimuli. We conclude by highlighting the potential therapeutic uses of satellite cells and identifying future research goals for the study of satellite cell biology.

Bibliography

Hawke, T. J., & Garry, D. J. (2001). Myogenic satellite cells: physiology to molecular biology. Journal of Applied Physiology, 91(2), 534â551.

Authors 2

Thomas J. Hawke (first)
Daniel J. Garry (additional)

References 203 Referenced 1,207

10.1152/jappl.1999.87.5.1705
10.1159/000145438
10.1002/jcp.1041380213
10.1002/jcp.1041650211
10.1002/(SICI)1520-6408(1996)18:3<254::AID-DVG6>3.0.CO;2-8
10.1091/mbc.11.5.1859
10.1016/0022-510X(91)90045-9
10.1073/pnas.95.26.15603
10.1083/jcb.151.6.1221
10.1016/0022-510X(68)90058-0
10.1242/dev.126.22.4965 / Development by Bendall AJ (1999)
10.1002/(SICI)1097-0177(199704)208:4<505::AID-AJA6>3.0.CO;2-M
10.1038/376768a0
10.1002/(SICI)1097-4598(199802)21:2<173::AID-MUS4>3.0.CO;2-8
10.1242/dev.126.8.1665 / Development by Borycki AG (1999)
10.1242/dev.127.2.437 / Development by Brohmann H (2000)
{'key': 'B18', 'first-page': '91', 'volume': '183', 'author': 'Brown SC', 'year': '1993', 'journal-title': 'J Anat'} / J Anat by Brown SC (1993)
10.1016/0168-9525(92)90373-C
10.1038/328434a0
10.2527/jas1981.5251014x
{'key': 'B22', 'first-page': '485', 'volume': '6', 'author': 'Cantini M', 'year': '1996', 'journal-title': 'Basic Appl Myol'} / Basic Appl Myol by Cantini M (1996)
10.1152/ajpcell.1989.256.6.C1262
10.1093/gerona/51A.1.B43
10.1074/jbc.M005832200
10.1152/jappl.2000.89.4.1365
10.1007/BF01919688
10.1126/science.288.5471.1660
10.1242/jcs.106.1.121 / J Cell Sci by Clarke MS (1993)
10.1083/jcb.105.2.949
{'key': 'B31', 'first-page': 'B71', 'volume': '47', 'author': 'Coggan AR', 'year': '1992', 'journal-title': 'J Gerontol B Psychol Sci Soc Sci'} / J Gerontol B Psychol Sci Soc Sci by Coggan AR (1992)
10.1074/jbc.272.10.6653
10.1006/dbio.1997.8721
{'key': 'B34', 'first-page': '755', 'volume': '12', 'author': 'Cossu G.', 'year': '1997', 'journal-title': 'Histol Histopathol'} / Histol Histopathol by Cossu G. (1997)
10.1016/0012-1606(87)90425-8
10.1172/JCI10376
10.1016/S0070-2153(08)60625-0
10.1016/0168-9525(96)10025-1
10.1083/jcb.102.3.716
10.1006/excr.1998.4100
10.1128/MCB.11.10.4854
10.1111/j.1432-1033.1988.tb14068.x
10.1073/pnas.86.6.2018
10.1152/jappl.1989.67.5.1827
10.1083/jcb.147.4.869
10.1016/S0960-8966(99)00093-0
10.1089/hum.1996.7.11-1347
10.1089/hum.1997.8.12-1429
10.1016/S0092-8674(00)80532-2
{'key': 'B50', 'first-page': '601', 'volume': '45', 'author': 'Dietrich S', 'year': '1999', 'journal-title': 'Cell Mol Biol (Oxf)'} / Cell Mol Biol (Oxf) by Dietrich S (1999)
10.1016/0012-1606(91)90340-9
10.1016/0047-6374(87)90003-0
{'key': 'B53', 'first-page': '288', 'volume': '118', 'author': 'Doroshow JH', 'year': '1985', 'journal-title': 'Am J Pathol'} / Am J Pathol by Doroshow JH (1985)
10.1002/jcp.1041570216
10.1016/0012-1606(92)90107-R
10.1006/bbrc.2000.2703
{'key': 'B58', 'first-page': '544', 'volume': '23', 'author': 'Fischel A.', 'year': '1895', 'journal-title': 'Morphol Jb'} / Morphol Jb by Fischel A. (1895)
10.1101/gad.11.16.2040
10.1007/BF00171747
10.1016/S0092-8674(00)81691-8
10.1016/S0167-4889(97)00124-9
10.1073/pnas.100501197
10.1006/dbio.1997.8657
10.1002/ar.1092020305
10.1002/mus.880060807
10.1084/jem.183.4.1797
10.1038/nm1297-1337
10.1083/jcb.136.4.871
10.2527/1991.691146x
10.1242/dev.127.2.413 / Development by Gross MK (2000)
10.1111/j.1749-6632.1998.tb09894.x
10.1097/00019052-199910000-00007
10.1007/BF00318695
10.1002/mus.880150508
10.1038/nm0997-970
10.1038/43919
10.1038/364501a0
10.2527/1995.7371972x
10.1242/jcs.113.12.2299 / J Cell Sci by Heslop L (2000)
10.1007/BF00202068
10.1126/science.3659917
10.1007/s004410051365
10.1016/S0925-4773(96)00631-4
10.1242/dev.118.4.1137 / Development by Hughes SM (1993)
10.1249/00005768-199202000-00007
10.1002/aja.1001990407
10.1073/pnas.96.25.14482
10.1083/jcb.140.5.1265
10.1002/jcp.1041540106
10.1006/excr.1995.1251
10.1002/1097-4652(200101)186:1<104::AID-JCP1015>3.0.CO;2-0
10.1006/dbio.1995.1144
10.1007/s004180050012
10.1016/0012-1606(74)90181-X
10.1002/(SICI)1097-4598(199806)21:6<819::AID-MUS20>3.0.CO;2-M
10.1006/excr.1996.3432
10.1098/rstb.1961.0001
10.1002/1097-4652(200101)186:1<146::AID-JCP1014>3.0.CO;2-Q
10.1002/aja.1002020304
10.1002/(SICI)1097-4598(199707)20:7<815::AID-MUS5>3.0.CO;2-A
10.1177/002215549904701104
10.1016/0092-8674(91)90620-E
10.1046/j.1469-7580.1998.19220161.x
{'key': 'B105', 'first-page': '1543', 'volume': '269', 'author': 'Le Douarin N', 'year': '1969', 'journal-title': 'CR Acad Sci Hebd Seances Acad Sci D'} / CR Acad Sci Hebd Seances Acad Sci D by Le Douarin N (1969)
10.1083/jcb.150.5.1085
10.1016/0960-8966(95)00012-C
10.1073/pnas.96.25.14193
10.1159/000109323
10.1016/S0960-8966(98)00111-4
10.1002/(SICI)1097-0185(199707)248:3<355::AID-AR8>3.0.CO;2-O
10.1016/S0092-8674(00)81372-0
10.1016/S0092-8674(00)80190-7
10.1002/mus.880120703
10.1016/S0021-9258(19)49859-1 / J Biol Chem by Martin JF (1992)
10.1093/jb/118.5.959
10.1083/jcb.9.2.493
10.1007/BF00261848
10.1101/gad.10.10.1173
10.1002/1097-4652(200010)185:1<143::AID-JCP14>3.0.CO;2-U
10.1002/(SICI)1097-4598(199906)22:6<724::AID-MUS9>3.0.CO;2-O
10.1002/hep.1840150125
10.1016/S0070-2153(08)60382-8
10.1152/ajpcell.2000.278.1.C174
10.3109/08977199609034565
10.1016/S0959-437X(96)80066-9
10.1038/323646a0
10.1002/ar.1091700405
10.1152/jappl.2000.88.1.158
{'key': 'B130', 'first-page': '435', 'volume': '99', 'author': 'Muir AR', 'year': '1965', 'journal-title': 'J Anat'} / J Anat by Muir AR (1965)
10.1242/dev.121.3.651 / Development by Munsterberg AE (1995)
10.1038/84839
10.1172/JCI112815
10.1002/(SICI)1097-0177(199609)207:1<100::AID-AJA9>3.0.CO;2-M
10.1016/S0047-6374(99)00076-7
10.1016/S0092-8674(00)00212-9
10.1101/gad.4.9.1454
10.1111/j.1749-6632.1996.tb56248.x
10.1083/jcb.147.4.695
10.1242/dev.114.2.339 / Development by Ordahl CP (1992)
10.1016/S0070-2153(08)60761-9
10.1242/dev.121.10.3347 / Development by Patapoutian A (1995)
10.1074/jbc.270.18.10915
10.1006/dbio.2000.9784
10.1152/jappl.1999.86.1.40
10.1006/dbio.1995.0004
10.1242/dev.125.13.2349 / Development by Rawls A (1998)
10.1016/S0070-2153(08)60724-3
10.1054/ghir.2000.0143
10.1016/S0531-5565(00)00151-0
10.1006/excr.1993.1199
10.1002/ar.1092430405
10.1152/jappl.1992.73.6.2538
10.1007/BF00374404
10.1002/mus.880170607
10.1016/0092-8674(93)90621-V
10.1016/0022-510X(85)90051-6
10.1007/PL00007422
10.1006/excr.1999.4506
10.1002/ar.1091890204
10.1073/pnas.86.1.307
10.1006/dbio.1996.0097
10.1007/BF01753657
10.1002/mus.880080307
10.1016/0047-6374(82)90105-1
10.1007/BFb0030904
10.1006/dbio.1999.9565
10.1016/S0092-8674(00)00066-0
10.1038/23054
10.1152/ajpcell.2001.280.2.C408
10.1667/0033-7587(2001)155[0188:TATIFC]2.0.CO;2
10.1002/(SICI)1097-4652(199912)181:3<499::AID-JCP14>3.0.CO;2-1
10.1002/(SICI)1097-4598(200002)23:2<239::AID-MUS15>3.0.CO;2-U
10.1242/dev.117.3.1125 / Development by Smith TH (1993)
10.1007/BF00220299
10.1126/science.2898810
10.1016/S0021-9258(18)67682-3 / J Biol Chem by Spizz G (1986)
10.1083/jcb.139.2.375
10.1016/S0092-8674(00)80189-0
10.1006/dbio.1997.8803
10.1111/j.1748-1716.1990.tb09029.x
10.1128/MCB.9.8.3576
10.1006/dbio.2000.9621
10.1006/cbir.2000.0499
10.1002/(SICI)1097-0185(199707)248:3<346::AID-AR7>3.0.CO;2-N
10.1002/(SICI)1097-0185(20000201)258:2<176::AID-AR7>3.0.CO;2-Y
10.1006/dbio.1995.1087
10.1002/ar.1092220103
10.1007/BF00309688
10.1016/0092-8674(93)90610-3
10.1073/pnas.86.14.5434
10.1016/S0092-8674(00)81692-X
10.1126/science.287.5457.1442
10.1101/gad.12.16.2445
10.1002/ar.1092320306
10.1002/ar.1092230209
10.1016/0092-8674(89)90583-7
10.1006/dbio.1994.1226
10.1152/jappl.1993.74.1.410
10.1128/MCB.17.9.5236
10.1042/bj3450335
10.1242/dev.122.7.2163 / Development by Yang XM (1996)
10.1128/MCB.17.3.1626
10.1016/S0955-0674(96)80091-3
10.1073/pnas.89.11.5176

Dates

Type	When
Created	7 years, 8 months ago (Dec. 22, 2017, 4:19 p.m.)
Deposited	3 years ago (Aug. 10, 2022, 11:08 p.m.)
Indexed	22 hours, 49 minutes ago (Aug. 29, 2025, 6:01 a.m.)
Issued	24 years ago (Aug. 1, 2001)
Published	24 years ago (Aug. 1, 2001)
Published Print	24 years ago (Aug. 1, 2001)

Funders 0

None

BibTeX

@article{Hawke_2001, title={Myogenic satellite cells: physiology to molecular biology}, volume={91}, ISSN={1522-1601}, url={http://dx.doi.org/10.1152/jappl.2001.91.2.534}, DOI={10.1152/jappl.2001.91.2.534}, number={2}, journal={Journal of Applied Physiology}, publisher={American Physiological Society}, author={Hawke, Thomas J. and Garry, Daniel J.}, year={2001}, month=aug, pages={534–551} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        29
      ]
    ],
    "date-time": "2025-08-29T10:01:07Z",
    "timestamp": 1756461667142
  },
  "reference-count": 203,
  "publisher": "American Physiological Society",
  "issue": "2",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        8,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Adult skeletal muscle has a remarkable ability to regenerate following myotrauma. Because adult myofibers are terminally differentiated, the regeneration of skeletal muscle is largely dependent on a small population of resident cells termed satellite cells. Although this population of cells was identified 40 years ago, little is known regarding the molecular phenotype or regulation of the satellite cell. The use of cell culture techniques and transgenic animal models has improved our understanding of this unique cell population; however, the capacity and potential of these cells remain ill-defined. This review will highlight the origin and unique markers of the satellite cell population, the regulation by growth factors, and the response to physiological and pathological stimuli. We conclude by highlighting the potential therapeutic uses of satellite cells and identifying future research goals for the study of satellite cell biology.</jats:p>",
  "DOI": "10.1152/jappl.2001.91.2.534",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2017,
        12,
        22
      ]
    ],
    "date-time": "2017-12-22T21:19:41Z",
    "timestamp": 1513977581000
  },
  "page": "534-551",
  "source": "Crossref",
  "is-referenced-by-count": 1207,
  "title": "Myogenic satellite cells: physiology to molecular biology",
  "prefix": "10.1152",
  "volume": "91",
  "author": [
    {
      "given": "Thomas J.",
      "family": "Hawke",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Internal Medicine and"
        }
      ]
    },
    {
      "given": "Daniel J.",
      "family": "Garry",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Internal Medicine and"
        },
        {
          "name": "Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390"
        }
      ]
    }
  ],
  "member": "24",
  "reference": [
    {
      "key": "B1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jappl.1999.87.5.1705"
    },
    {
      "key": "B2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000145438"
    },
    {
      "key": "B3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.1041380213"
    },
    {
      "key": "B4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.1041650211"
    },
    {
      "key": "B5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1520-6408(1996)18:3<254::AID-DVG6>3.0.CO;2-8"
    },
    {
      "key": "B6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.11.5.1859"
    },
    {
      "key": "B7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-510X(91)90045-9"
    },
    {
      "key": "B8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.95.26.15603"
    },
    {
      "key": "B9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.151.6.1221"
    },
    {
      "key": "B10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-510X(68)90058-0"
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "4965",
      "DOI": "10.1242/dev.126.22.4965",
      "volume": "126",
      "author": "Bendall AJ",
      "year": "1999",
      "journal-title": "Development"
    },
    {
      "key": "B13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0177(199704)208:4<505::AID-AJA6>3.0.CO;2-M"
    },
    {
      "key": "B14",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/376768a0"
    },
    {
      "key": "B15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-4598(199802)21:2<173::AID-MUS4>3.0.CO;2-8"
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "1665",
      "DOI": "10.1242/dev.126.8.1665",
      "volume": "126",
      "author": "Borycki AG",
      "year": "1999",
      "journal-title": "Development"
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "437",
      "DOI": "10.1242/dev.127.2.437",
      "volume": "127",
      "author": "Brohmann H",
      "year": "2000",
      "journal-title": "Development"
    },
    {
      "key": "B18",
      "first-page": "91",
      "volume": "183",
      "author": "Brown SC",
      "year": "1993",
      "journal-title": "J Anat"
    },
    {
      "key": "B19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-9525(92)90373-C"
    },
    {
      "key": "B20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/328434a0"
    },
    {
      "key": "B21",
      "doi-asserted-by": "publisher",
      "DOI": "10.2527/jas1981.5251014x"
    },
    {
      "key": "B22",
      "first-page": "485",
      "volume": "6",
      "author": "Cantini M",
      "year": "1996",
      "journal-title": "Basic Appl Myol"
    },
    {
      "key": "B23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.1989.256.6.C1262"
    },
    {
      "key": "B24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/gerona/51A.1.B43"
    },
    {
      "key": "B25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M005832200"
    },
    {
      "key": "B26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jappl.2000.89.4.1365"
    },
    {
      "key": "B27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01919688"
    },
    {
      "key": "B28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.288.5471.1660"
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "121",
      "DOI": "10.1242/jcs.106.1.121",
      "volume": "106",
      "author": "Clarke MS",
      "year": "1993",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "B30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.105.2.949"
    },
    {
      "key": "B31",
      "first-page": "B71",
      "volume": "47",
      "author": "Coggan AR",
      "year": "1992",
      "journal-title": "J Gerontol B Psychol Sci Soc Sci"
    },
    {
      "key": "B32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.10.6653"
    },
    {
      "key": "B33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1997.8721"
    },
    {
      "key": "B34",
      "first-page": "755",
      "volume": "12",
      "author": "Cossu G.",
      "year": "1997",
      "journal-title": "Histol Histopathol"
    },
    {
      "key": "B35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(87)90425-8"
    },
    {
      "key": "B36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI10376"
    },
    {
      "key": "B37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0070-2153(08)60625-0"
    },
    {
      "key": "B38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-9525(96)10025-1"
    },
    {
      "key": "B39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.102.3.716"
    },
    {
      "key": "B40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/excr.1998.4100"
    },
    {
      "key": "B41",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.11.10.4854"
    },
    {
      "key": "B42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1988.tb14068.x"
    },
    {
      "key": "B43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.6.2018"
    },
    {
      "key": "B44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jappl.1989.67.5.1827"
    },
    {
      "key": "B45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.147.4.869"
    },
    {
      "key": "B46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-8966(99)00093-0"
    },
    {
      "key": "B47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/hum.1996.7.11-1347"
    },
    {
      "key": "B48",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/hum.1997.8.12-1429"
    },
    {
      "key": "B49",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)80532-2"
    },
    {
      "key": "B50",
      "first-page": "601",
      "volume": "45",
      "author": "Dietrich S",
      "year": "1999",
      "journal-title": "Cell Mol Biol (Oxf)"
    },
    {
      "key": "B51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(91)90340-9"
    },
    {
      "key": "B52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0047-6374(87)90003-0"
    },
    {
      "key": "B53",
      "first-page": "288",
      "volume": "118",
      "author": "Doroshow JH",
      "year": "1985",
      "journal-title": "Am J Pathol"
    },
    {
      "key": "B54",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.1041570216"
    },
    {
      "key": "B56",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(92)90107-R"
    },
    {
      "key": "B57",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.2000.2703"
    },
    {
      "key": "B58",
      "first-page": "544",
      "volume": "23",
      "author": "Fischel A.",
      "year": "1895",
      "journal-title": "Morphol Jb"
    },
    {
      "key": "B59",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.11.16.2040"
    },
    {
      "key": "B60",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00171747"
    },
    {
      "key": "B61",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81691-8"
    },
    {
      "key": "B62",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0167-4889(97)00124-9"
    },
    {
      "key": "B63",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.100501197"
    },
    {
      "key": "B64",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1997.8657"
    },
    {
      "key": "B65",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1092020305"
    },
    {
      "key": "B66",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/mus.880060807"
    },
    {
      "key": "B67",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.183.4.1797"
    },
    {
      "key": "B68",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nm1297-1337"
    },
    {
      "key": "B69",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.136.4.871"
    },
    {
      "key": "B70",
      "doi-asserted-by": "publisher",
      "DOI": "10.2527/1991.691146x"
    },
    {
      "key": "B71",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1242/dev.127.2.413",
      "volume": "127",
      "author": "Gross MK",
      "year": "2000",
      "journal-title": "Development"
    },
    {
      "key": "B72",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1749-6632.1998.tb09894.x"
    },
    {
      "key": "B73",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00019052-199910000-00007"
    },
    {
      "key": "B74",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00318695"
    },
    {
      "key": "B75",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/mus.880150508"
    },
    {
      "key": "B76",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nm0997-970"
    },
    {
      "key": "B77",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/43919"
    },
    {
      "key": "B78",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/364501a0"
    },
    {
      "key": "B79",
      "doi-asserted-by": "publisher",
      "DOI": "10.2527/1995.7371972x"
    },
    {
      "key": "B80",
      "doi-asserted-by": "crossref",
      "first-page": "2299",
      "DOI": "10.1242/jcs.113.12.2299",
      "volume": "113",
      "author": "Heslop L",
      "year": "2000",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "B81",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00202068"
    },
    {
      "key": "B82",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3659917"
    },
    {
      "key": "B83",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s004410051365"
    },
    {
      "key": "B84",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0925-4773(96)00631-4"
    },
    {
      "key": "B85",
      "doi-asserted-by": "crossref",
      "first-page": "1137",
      "DOI": "10.1242/dev.118.4.1137",
      "volume": "118",
      "author": "Hughes SM",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "B86",
      "doi-asserted-by": "publisher",
      "DOI": "10.1249/00005768-199202000-00007"
    },
    {
      "key": "B87",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/aja.1001990407"
    },
    {
      "key": "B88",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.25.14482"
    },
    {
      "key": "B89",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.140.5.1265"
    },
    {
      "key": "B90",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.1041540106"
    },
    {
      "key": "B91",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/excr.1995.1251"
    },
    {
      "key": "B92",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/1097-4652(200101)186:1<104::AID-JCP1015>3.0.CO;2-0"
    },
    {
      "key": "B93",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1995.1144"
    },
    {
      "key": "B94",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s004180050012"
    },
    {
      "key": "B95",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(74)90181-X"
    },
    {
      "key": "B96",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-4598(199806)21:6<819::AID-MUS20>3.0.CO;2-M"
    },
    {
      "key": "B97",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/excr.1996.3432"
    },
    {
      "key": "B98",
      "doi-asserted-by": "publisher",
      "DOI": "10.1098/rstb.1961.0001"
    },
    {
      "key": "B99",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/1097-4652(200101)186:1<146::AID-JCP1014>3.0.CO;2-Q"
    },
    {
      "key": "B100",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/aja.1002020304"
    },
    {
      "key": "B101",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-4598(199707)20:7<815::AID-MUS5>3.0.CO;2-A"
    },
    {
      "key": "B102",
      "doi-asserted-by": "publisher",
      "DOI": "10.1177/002215549904701104"
    },
    {
      "key": "B103",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90620-E"
    },
    {
      "key": "B104",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1469-7580.1998.19220161.x"
    },
    {
      "key": "B105",
      "first-page": "1543",
      "volume": "269",
      "author": "Le Douarin N",
      "year": "1969",
      "journal-title": "CR Acad Sci Hebd Seances Acad Sci D"
    },
    {
      "key": "B106",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.150.5.1085"
    },
    {
      "key": "B107",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0960-8966(95)00012-C"
    },
    {
      "key": "B108",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.25.14193"
    },
    {
      "key": "B109",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000109323"
    },
    {
      "key": "B110",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-8966(98)00111-4"
    },
    {
      "key": "B111",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0185(199707)248:3<355::AID-AR8>3.0.CO;2-O"
    },
    {
      "key": "B112",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81372-0"
    },
    {
      "key": "B113",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)80190-7"
    },
    {
      "key": "B114",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/mus.880120703"
    },
    {
      "key": "B115",
      "doi-asserted-by": "crossref",
      "first-page": "10956",
      "DOI": "10.1016/S0021-9258(19)49859-1",
      "volume": "267",
      "author": "Martin JF",
      "year": "1992",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "B116",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/jb/118.5.959"
    },
    {
      "key": "B117",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.9.2.493"
    },
    {
      "key": "B118",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00261848"
    },
    {
      "key": "B119",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.10.10.1173"
    },
    {
      "key": "B120",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/1097-4652(200010)185:1<143::AID-JCP14>3.0.CO;2-U"
    },
    {
      "key": "B121",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-4598(199906)22:6<724::AID-MUS9>3.0.CO;2-O"
    },
    {
      "key": "B122",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/hep.1840150125"
    },
    {
      "key": "B123",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0070-2153(08)60382-8"
    },
    {
      "key": "B124",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.2000.278.1.C174"
    },
    {
      "key": "B125",
      "doi-asserted-by": "publisher",
      "DOI": "10.3109/08977199609034565"
    },
    {
      "key": "B126",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0959-437X(96)80066-9"
    },
    {
      "key": "B127",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/323646a0"
    },
    {
      "key": "B128",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1091700405"
    },
    {
      "key": "B129",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jappl.2000.88.1.158"
    },
    {
      "key": "B130",
      "first-page": "435",
      "volume": "99",
      "author": "Muir AR",
      "year": "1965",
      "journal-title": "J Anat"
    },
    {
      "key": "B131",
      "doi-asserted-by": "crossref",
      "first-page": "651",
      "DOI": "10.1242/dev.121.3.651",
      "volume": "121",
      "author": "Munsterberg AE",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "B132",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/84839"
    },
    {
      "key": "B133",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI112815"
    },
    {
      "key": "B134",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0177(199609)207:1<100::AID-AJA9>3.0.CO;2-M"
    },
    {
      "key": "B135",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0047-6374(99)00076-7"
    },
    {
      "key": "B136",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)00212-9"
    },
    {
      "key": "B137",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.4.9.1454"
    },
    {
      "key": "B138",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1749-6632.1996.tb56248.x"
    },
    {
      "key": "B139",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.147.4.695"
    },
    {
      "key": "B140",
      "doi-asserted-by": "crossref",
      "first-page": "339",
      "DOI": "10.1242/dev.114.2.339",
      "volume": "114",
      "author": "Ordahl CP",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "B141",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0070-2153(08)60761-9"
    },
    {
      "key": "B142",
      "doi-asserted-by": "crossref",
      "first-page": "3347",
      "DOI": "10.1242/dev.121.10.3347",
      "volume": "121",
      "author": "Patapoutian A",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "B144",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.18.10915"
    },
    {
      "key": "B145",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.2000.9784"
    },
    {
      "key": "B146",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jappl.1999.86.1.40"
    },
    {
      "key": "B147",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1995.0004"
    },
    {
      "key": "B148",
      "doi-asserted-by": "crossref",
      "first-page": "2349",
      "DOI": "10.1242/dev.125.13.2349",
      "volume": "125",
      "author": "Rawls A",
      "year": "1998",
      "journal-title": "Development"
    },
    {
      "key": "B149",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0070-2153(08)60724-3"
    },
    {
      "key": "B150",
      "doi-asserted-by": "publisher",
      "DOI": "10.1054/ghir.2000.0143"
    },
    {
      "key": "B151",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0531-5565(00)00151-0"
    },
    {
      "key": "B152",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/excr.1993.1199"
    },
    {
      "key": "B153",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1092430405"
    },
    {
      "key": "B154",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jappl.1992.73.6.2538"
    },
    {
      "key": "B155",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00374404"
    },
    {
      "key": "B156",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/mus.880170607"
    },
    {
      "key": "B157",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90621-V"
    },
    {
      "key": "B158",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-510X(85)90051-6"
    },
    {
      "key": "B159",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/PL00007422"
    },
    {
      "key": "B160",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/excr.1999.4506"
    },
    {
      "key": "B161",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1091890204"
    },
    {
      "key": "B162",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.1.307"
    },
    {
      "key": "B163",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1996.0097"
    },
    {
      "key": "B164",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01753657"
    },
    {
      "key": "B165",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/mus.880080307"
    },
    {
      "key": "B166",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0047-6374(82)90105-1"
    },
    {
      "key": "B167",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BFb0030904"
    },
    {
      "key": "B168",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1999.9565"
    },
    {
      "key": "B169",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)00066-0"
    },
    {
      "key": "B170",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/23054"
    },
    {
      "key": "B171",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.2001.280.2.C408"
    },
    {
      "key": "B172",
      "doi-asserted-by": "publisher",
      "DOI": "10.1667/0033-7587(2001)155[0188:TATIFC]2.0.CO;2"
    },
    {
      "key": "B173",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-4652(199912)181:3<499::AID-JCP14>3.0.CO;2-1"
    },
    {
      "key": "B174",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-4598(200002)23:2<239::AID-MUS15>3.0.CO;2-U"
    },
    {
      "key": "B175",
      "doi-asserted-by": "crossref",
      "first-page": "1125",
      "DOI": "10.1242/dev.117.3.1125",
      "volume": "117",
      "author": "Smith TH",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "B176",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00220299"
    },
    {
      "key": "B177",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2898810"
    },
    {
      "key": "B178",
      "doi-asserted-by": "crossref",
      "first-page": "9483",
      "DOI": "10.1016/S0021-9258(18)67682-3",
      "volume": "261",
      "author": "Spizz G",
      "year": "1986",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "B179",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.139.2.375"
    },
    {
      "key": "B181",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)80189-0"
    },
    {
      "key": "B182",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1997.8803"
    },
    {
      "key": "B183",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1748-1716.1990.tb09029.x"
    },
    {
      "key": "B184",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.9.8.3576"
    },
    {
      "key": "B185",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.2000.9621"
    },
    {
      "key": "B186",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/cbir.2000.0499"
    },
    {
      "key": "B187",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0185(199707)248:3<346::AID-AR7>3.0.CO;2-N"
    },
    {
      "key": "B188",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0185(20000201)258:2<176::AID-AR7>3.0.CO;2-Y"
    },
    {
      "key": "B189",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1995.1087"
    },
    {
      "key": "B190",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1092220103"
    },
    {
      "key": "B191",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00309688"
    },
    {
      "key": "B192",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90610-3"
    },
    {
      "key": "B193",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.14.5434"
    },
    {
      "key": "B194",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81692-X"
    },
    {
      "key": "B195",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.287.5457.1442"
    },
    {
      "key": "B196",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.12.16.2445"
    },
    {
      "key": "B198",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1092320306"
    },
    {
      "key": "B199",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/ar.1092230209"
    },
    {
      "key": "B200",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90583-7"
    },
    {
      "key": "B201",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1994.1226"
    },
    {
      "key": "B202",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jappl.1993.74.1.410"
    },
    {
      "key": "B203",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.17.9.5236"
    },
    {
      "key": "B204",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj3450335"
    },
    {
      "key": "B205",
      "doi-asserted-by": "crossref",
      "first-page": "2163",
      "DOI": "10.1242/dev.122.7.2163",
      "volume": "122",
      "author": "Yang XM",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "B206",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.17.3.1626"
    },
    {
      "key": "B207",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0955-0674(96)80091-3"
    },
    {
      "key": "B208",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.11.5176"
    }
  ],
  "container-title": "Journal of Applied Physiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.physiology.org/doi/pdf/10.1152/jappl.2001.91.2.534",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        8,
        11
      ]
    ],
    "date-time": "2022-08-11T03:08:24Z",
    "timestamp": 1660187304000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.physiology.org/doi/10.1152/jappl.2001.91.2.534"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        8,
        1
      ]
    ]
  },
  "references-count": 203,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          2001,
          8,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1152/jappl.2001.91.2.534"
  ],
  "URL": "http://dx.doi.org/10.1152/jappl.2001.91.2.534",
  "relation": {},
  "ISSN": [
    "8750-7587",
    "1522-1601"
  ],
  "subject": [],
  "container-title-short": "Journal of Applied Physiology",
  "published": {
    "date-parts": [
      [
        2001,
        8,
        1
      ]
    ]
  }
}