Crossref journal-article
American Association for the Advancement of Science (AAAS)
Science (221)
Abstract

The healing of an adult skin wound is a complex process requiring the collaborative efforts of many different tissues and cell lineages. The behavior of each of the contributing cell types during the phases of proliferation, migration, matrix synthesis, and contraction, as well as the growth factor and matrix signals present at a wound site, are now roughly understood. Details of how these signals control wound cell activities are beginning to emerge, and studies of healing in embryos have begun to show how the normal adult repair process might be readjusted to make it less like patching up and more like regeneration.

Bibliography

Martin, P. (1997). Wound Healing--Aiming for Perfect Skin Regeneration. Science, 276(5309), 75–81.

Authors 1
  1. Paul Martin (first)
References 130 Referenced 3,855
  1. Clark R. A. F. in (1) pp. 3–50.
  2. Riches D. W. H. in (1) pp. 95–141.
  3. 10.1016/0092-8674(94)90337-9
  4. Mayadas T. N., et al., ibid.74, 541 (1993). / ibid. by Mayadas T. N. (1993)
  5. Hubner G., et al., Cytokine8, 548 (1996). (10.1006/cyto.1996.0074) / Cytokine by Hubner G. (1996)
  6. Leibovich S. J., Ross R., Am. J. Pathol.78, 71 (1975). / Am. J. Pathol. by Leibovich S. J. (1975)
  7. Cavani A., et al., J. Invest. Dermatol.101, 600 (1993); (10.1111/1523-1747.ep12366057) / J. Invest. Dermatol. by Cavani A. (1993)
  8. Breuss J. M., et al., J. Cell Sci.108, 2241 (1995); (10.1242/jcs.108.6.2241) / J. Cell Sci. by Breuss J. M. (1995)
  9. Yamada K. M. Clark R. A. F. in (1) pp. 51–93;
  10. Haapasalmi K., et al., J. Invest. Dermatol.106, 42 (1996). (10.1111/1523-1747.ep12327199) / J. Invest. Dermatol. by Haapasalmi K. (1996)
  11. Mitcheson T. J., Cramer L. P., Cell84, 371 (1996). (10.1016/S0092-8674(00)81281-7) / Cell by Mitcheson T. J. (1996)
  12. Grinnell F., J. Cell. Sci.101, 1 (1992). (10.1242/jcs.101.1.1) / J. Cell. Sci. by Grinnell F. (1992)
  13. Garlick J. A., Taichman L. B., Lab. Invest.70, 916 (1994) / Lab. Invest. by Garlick J. A. (1994)
  14. Hertle M. D., Kubler M.-D., Leigh I. M., Watt F. M., J. Clin. Invest.89, 1892 (1992). (10.1172/JCI115794) / J. Clin. Invest. by Hertle M. D. (1992)
  15. Matoltsy A. G., Viziam C. B., J. Invest. Dermatol.55, 20 (1970); (10.1111/1523-1747.ep12290488) / J. Invest. Dermatol. by Matoltsy A. G. (1970)
  16. Krawczyk W. S., J. Cell Biol.49, 247 (1971). (10.1083/jcb.49.2.247) / J. Cell Biol. by Krawczyk W. S. (1971)
  17. Compton C. C., et al., Lab. Invest.60, 600 (1989). / Lab. Invest. by Compton C. C. (1989)
  18. Rochat A., Kobayashi K., Barrandon Y., Cell76, 1063 (1994). (10.1016/0092-8674(94)90383-2) / Cell by Rochat A. (1994)
  19. Jones P. H., Watt F. M., ibid.73, 713 (1993); / ibid. by Jones P. H. (1993)
  20. Jones P. H., Harper S., Watt F. M., ibid.80, 83 (1995). / ibid. by Jones P. H. (1995)
  21. Grondahl-Hansen J., et al., J. Invest. Dermatol.90, 790 (1988); (10.1111/1523-1747.ep12461511) / J. Invest. Dermatol. by Grondahl-Hansen J. (1988)
  22. Romer J., et al., ibid97, 803 (1991); / 97 / ibid by Romer J. (1991)
  23. Romer J., et al., ibid.102, 519 (1994). / ibid. by Romer J. (1994)
  24. Romer J., et al., Nature Med.2, 287 (1996). (10.1038/nm0396-287) / Nature Med. by Romer J. (1996)
  25. Salo T., et al., Lab. Invest.70, 176. (1994). / Lab. Invest. by Salo T. (1994)
  26. Saarialho-Kere U. K., Chang E. S., Welgus H. G., Parks W. C., J. Clin. Invest.90, 1952 (1992). (10.1172/JCI116073) / J. Clin. Invest. by Saarialho-Kere U. K. (1992)
  27. Saarialho-Kere U. K., et al., ibid.94, 79 (1994). / ibid. by Saarialho-Kere U. K. (1994)
  28. Grinnell F., Ho C.-H., Wysocki A., J. Invest. Dermatol.98, 410 (1992); (10.1111/1523-1747.ep12499839) / J. Invest. Dermatol. by Grinnell F. (1992)
  29. Tarnuzzer R.W., Schultz G. S., Wound Repair Regen.4,321 (1996); (10.1046/j.1524-475X.1996.40307.x) / Wound Repair Regen. by Tarnuzzer R.W. (1996)
  30. Mast B. A., Schultz G. S., ibid., p. 411. / ibid. by Mast B. A.
  31. Gipson I. K., Spurr-Michaud S. J., Tisdale A. S., Dev. Biol.126, 253 (1988); (10.1016/0012-1606(88)90136-4) / Dev. Biol. by Gipson I. K. (1988)
  32. Uitto J. Mauviel A. McGrath J. in (1) pp. 513–560.
  33. Brown G. L., et al., J. Exp. Med.163, 1319 (1986); (10.1084/jem.163.5.1319) / J. Exp. Med. by Brown G. L. (1986)
  34. Schultz G. S., et al., Science235, 350 (1987). (10.1126/science.3492044) / Science by Schultz G. S. (1987)
  35. Barrandon Y., Green H., Cell50, 1131 (1987). (10.1016/0092-8674(87)90179-6) / Cell by Barrandon Y. (1987)
  36. Ridley A. J., Hall A., ibid.70, 389 (1992); / ibid. by Ridley A. J. (1992)
  37. Ridley A. J., Comoglio P. M., Hall A., Mol. Cell. Biol.15, 1110 (1995); (10.1128/MCB.15.2.1110) / Mol. Cell. Biol. by Ridley A. J. (1995)
  38. 10.1016/0092-8674(95)90370-4
  39. Werner S., et al., Proc. Natl. Acad. Sci. U.S.A.89, 6896 (1992). (10.1073/pnas.89.15.6896) / Proc. Natl. Acad. Sci. U.S.A. by Werner S. (1992)
  40. Brauchle M., Fassler R., Werner S., J. Invest. Dermatol.105, 579 (1995). (10.1111/1523-1747.ep12323521) / J. Invest. Dermatol. by Brauchle M. (1995)
  41. Guo L., Degenstein L., Fuchs E., Genes Dev.10, 165 (1996). (10.1101/gad.10.2.165) / Genes Dev. by Guo L. (1996)
  42. Werner S., et al., Science266, 819 (1994). (10.1126/science.7973639) / Science by Werner S. (1994)
  43. Staiano-Coico L., et al., J. Exp. Med.178, 865 (1993); (10.1084/jem.178.3.865) / J. Exp. Med. by Staiano-Coico L. (1993)
  44. Pierce G. F., et al., ibid.179, 831 (1994). / ibid. by Pierce G. F. (1994)
  45. Tsuboi R., et al., J. Invest. Dermatol.101, 49 (1993); (10.1111/1523-1747.ep12358892) / J. Invest. Dermatol. by Tsuboi R. (1993)
  46. Madlener M., et al., Biochem. J.320, 659 (1996). (10.1042/bj3200659) / Biochem. J. by Madlener M. (1996)
  47. Gailet J., Welch M. P., Clark R. A. F., J. Invest. Dermatol.103, 221 (1994); (10.1111/1523-1747.ep12393176) / J. Invest. Dermatol. by Gailet J. (1994)
  48. Hertle M. D., et al., ibid.104, 260 (1995). / ibid. by Hertle M. D. (1995)
  49. Martin P., Lewis J., Nature360, 179 (1992); (10.1038/360179a0) / Nature by Martin P. (1992)
  50. McCluskey J., Martin P., Dev. Biol.170, 102 (1995). (10.1006/dbio.1995.1199) / Dev. Biol. by McCluskey J. (1995)
  51. Brock J., Midwinter K., Lewis J., Martin P., J. Cell Biol.135, 1097 (1996). (10.1083/jcb.135.4.1097) / J. Cell Biol. by Brock J. (1996)
  52. Bement W. M., Forscher P., Mooseker M. S., ibid.121, 565 (1993); / ibid. by Bement W. M. (1993)
  53. Heath J. P., Cell Biol. Int.20, 139 (1996). (10.1006/cbir.1996.0018) / Cell Biol. Int. by Heath J. P. (1996)
  54. Guo L., et al., Cell81, 233 (1995). (10.1016/0092-8674(95)90333-X) / Cell by Guo L. (1995)
  55. Paladini R. D., Takahashi K., Bravo N. S., Coulombe P. A., J. Cell Biol.132, 381 (1996). (10.1083/jcb.132.3.381) / J. Cell Biol. by Paladini R. D. (1996)
  56. Brock J., McCluskey J., Baribault H., Martin P., Cell Motil. Cytoskel.35, 358 (1996). (10.1002/(SICI)1097-0169(1996)35:4<358::AID-CM7>3.0.CO;2-2) / Cell Motil. Cytoskel. by Brock J. (1996)
  57. Sengel P., in Biology of the Integument, , Bereiter-Hahn J., Matolsty A. G., Richards K. S., Eds. (Springer-Verlag, Berlin, 1986). / in Biology of the Integument by Sengel P. (1986)
  58. Zhou P., Byrne C., Jacobs J., Fuchs E., Genes Dev.9, 570 (1995); / Genes Dev. by Zhou P. (1995)
  59. Nohno T., et al., Biochem. Biophys. Res. Commun.206, 33 (1995); (10.1006/bbrc.1995.1005) / Biochem. Biophys. Res. Commun. by Nohno T. (1995)
  60. Stenn R. S., et al.Dermatol. Clin.14, 543 (1996)] have a table of all genes expressed in developing hair bud. / Dermatol. Clin. by Stenn R. S.
  61. Luetteke N. C., et al., Cell73, 263 (1993); (10.1016/0092-8674(93)90228-I) / Cell by Luetteke N. C. (1993)
  62. Mann G. B., et al., ibid., p. 249; / ibid. by Mann G. B.
  63. Hebert J. M., et al., ibid.78, 1017 (1994). / ibid. by Hebert J. M. (1994)
  64. Jahoda C. A. B., Development115, 1103 (1992). (10.1242/dev.115.4.1103) / Development by Jahoda C. A. B. (1992)
  65. Eckes B. Aumailley M. Krieg T. in (1) pp. 493-512.
  66. McClain S. A., et al., Am. J. Pathol.149, 1257 (1996). / Am. J. Pathol. by McClain S. A. (1996)
  67. Eriksson A., et al., EMBO J.11, 543 (1992); (10.1002/j.1460-2075.1992.tb05085.x) / EMBO J. by Eriksson A. (1992)
  68. Heldin C.-H. Westermark B. in (1) pp. 249–273.
  69. Roberts A. B. Sporn M. B. in (1) pp. 275–308;
  70. Frank S., Madlener M., Werner S., J. Biol. Chem.271, 10188 (1996). (10.1074/jbc.271.17.10188) / J. Biol. Chem. by Frank S. (1996)
  71. Hubner G., Hu Q., Smola H., Werner S., Dev. Biol.173, 490 (1996). (10.1006/dbio.1996.0042) / Dev. Biol. by Hubner G. (1996)
  72. Igarashi A., Okochi H., Bradham D. M., Grotendorst G. R., Mol. Biol. Cell4, 637 (1993); (10.1091/mbc.4.6.637) / Mol. Biol. Cell by Igarashi A. (1993)
  73. Mason E. D., Conrad K. D., Webb C. D., Marsh J. L., Genes Dev.8, 1489 (1994); (10.1101/gad.8.13.1489) / Genes Dev. by Mason E. D. (1994)
  74. Grotendorst G. R., Okochi H., Hayashi N., Cell Growth Differ. 7, 469 (1996); / Cell Growth Differ. by Grotendorst G. R.
  75. Kothapalli D., et al., ibid.8, 61 (1997). / ibid. by Kothapalli D. (1997)
  76. Xu J., Clark R. A. F., J. Cell Biol.132, 239 (1996). (10.1083/jcb.132.1.239) / J. Cell Biol. by Xu J. (1996)
  77. Greiling D., Clark R. A. F., J. Cell Sci., in press. / J. Cell Sci. by Greiling D.
  78. Ffrench-Constant C., van de Water L., Dvorak H. F., Hynes R. O., J. Cell Biol.109, 903 (1989); (10.1083/jcb.109.2.903) / J. Cell Biol. by Ffrench-Constant C. (1989)
  79. Brown L. F., et al., Am. J. Pathol.142, 793 (1993). / Am. J. Pathol. by Brown L. F. (1993)
  80. Witke W., et al., Cell81, 41 (1995); see S. O'Kane et al. [Mol. Biol. Cell (suppl. 7), 543a (1996)] for preliminary in vivo wound healing report. (10.1016/0092-8674(95)90369-0) / Cell by Witke W. (1995)
  81. Hartwig J. H. H., et al., Cell82, 643 (1995). (10.1016/0092-8674(95)90036-5) / Cell by Hartwig J. H. H. (1995)
  82. Desmouliere A. Gabbiani G. in (1) pp. 391–423.
  83. Desmouliere A., Geinoz A., Gabbiani F., Gabbiani G., J. Cell Biol.122, 103 (1993). (10.1083/jcb.122.1.103) / J. Cell Biol. by Desmouliere A. (1993)
  84. Grinnell F., ibid.124, 401 (1994). / ibid. by Grinnell F. (1994)
  85. Montesano R., Orci L., Proc. Natl. Acad. Sci. U.S.A.85, 4894 (1988); (10.1073/pnas.85.13.4894) / Proc. Natl. Acad. Sci. U.S.A. by Montesano R. (1988)
  86. Clark R. A. F., et al., J. Clin. Invest.84, 1036 (1989). (10.1172/JCI114227) / J. Clin. Invest. by Clark R. A. F. (1989)
  87. He Y., Grinnell F., J. Cell Biol.126, 457 (1994); ibid.130, 1197 (1995). / ibid. / J. Cell Biol. by He Y. (1994)
  88. Lin Y.-C., Grinnell F., ibid.122, 663 (1993). / ibid. by Lin Y.-C. (1993)
  89. Desmouliere A., Redard M., Darby I., Gabbiani G., Am. J. Pathol.146, 56 (1995). / Am. J. Pathol. by Desmouliere A. (1995)
  90. Abraham J. A. Klagsbrun M. in (1) pp. 195–248.
  91. Broadley K. N., et al., Lab. Invest.61, 571 (1989). / Lab. Invest. by Broadley K. N. (1989)
  92. Brown L. F., et al., J. Exp. Med.176, 1375 (1992); (10.1084/jem.176.5.1375) / J. Exp. Med. by Brown L. F. (1992)
  93. Berse B., et al., Mol. Biol. Cell3, 211 (1992). (10.1091/mbc.3.2.211) / Mol. Biol. Cell by Berse B. (1992)
  94. Frank S., et al., J. Biol. Chem.270, 12607 (1995). (10.1074/jbc.270.21.12607) / J. Biol. Chem. by Frank S. (1995)
  95. 10.1126/science.7512751
  96. Clark R. A. F., Tonnesen M. G., Gailit J., Cheresh D. A., Am. J. Pathol.148, 1407 (1996). / Am. J. Pathol. by Clark R. A. F. (1996)
  97. Fisher C., et al., Dev. Biol.162, 499 (1994). (10.1006/dbio.1994.1104) / Dev. Biol. by Fisher C. (1994)
  98. Reynolds M. L., Fitzgerald M., J. Comp. Neurol.358, 487 (1995). (10.1002/cne.903580403) / J. Comp. Neurol. by Reynolds M. L. (1995)
  99. 10.1097/00001756-199411000-00019
  100. Buchman V. L., Sporn M., Davies A. M., Development120, 1621 (1994). (10.1242/dev.120.6.1621) / Development by Buchman V. L. (1994)
  101. Mullen L. M., et al., ibid.122, 3487 (1996). / ibid. by Mullen L. M. (1996)
  102. Nilsson J., von Euler A., Dalsgaard C.-J., Nature315, 61 (1985). (10.1038/315061a0) / Nature by Nilsson J. (1985)
  103. 10.1016/0092-8674(92)90286-L
  104. Estes J. M., et al., Differentiation56, 173 (1994). (10.1046/j.1432-0436.1994.5630173.x) / Differentiation by Estes J. M. (1994)
  105. See chapters in N. S. Adzick and M. T. Longaker Eds. Fetal Wound Healing (Elsevier New York 1992);
  106. McCallion R. L. Ferguson M. W. J. in (1) pp. 561–600;
  107. Martin P., Curr. Top. Dev. Biol.32, 175 (1996); (10.1016/S0070-2153(08)60428-7) / Curr. Top. Dev. Biol. by Martin P. (1996)
  108. Nodder S., Martin P., Anat. Embryol.195, 215 (1997). (10.1007/s004290050041) / Anat. Embryol. by Nodder S. (1997)
  109. Longaker M. T., et al., Surg. Forum41, 639 (1990). / Surg. Forum by Longaker M. T. (1990)
  110. Armstrong J. R., Ferguson M. W. J., Dev. Biol.169, 242 (1995). (10.1006/dbio.1995.1141) / Dev. Biol. by Armstrong J. R. (1995)
  111. Adzick N. S., et al., J. Pediatr. Surg.20, 315 (1985); (10.1016/S0022-3468(85)80210-4) / J. Pediatr. Surg. by Adzick N. S. (1985)
  112. Whitby D. J., Ferguson M. W. J., Development112, 651 (1991); (10.1242/dev.112.2.651) / Development by Whitby D. J. (1991)
  113. Hopkinson-Woolley J., Hughes D., Gordon S., Martin P., J. Cell Sci.107, 1159 (1994). (10.1242/jcs.107.5.1159) / J. Cell Sci. by Hopkinson-Woolley J. (1994)
  114. Whitby D. J., Ferguson M. W. J., Dev. Biol.147, 207 (1991); (10.1016/S0012-1606(05)80018-1) / Dev. Biol. by Whitby D. J. (1991)
  115. Martin P., Dickson M. C., Millan F. A., Akhurst R. J., Dev. Genet.14, 225 (1993). (10.1002/dvg.1020140309) / Dev. Genet. by Martin P. (1993)
  116. Noble W. A., Noble N. A., N. Engl. J. Med.331, 1286 (1994). (10.1056/NEJM199411103311907) / N. Engl. J. Med. by Noble W. A. (1994)
  117. Shah M., Foreman D. M., Ferguson M. W. J., Lancet339, 213 (1992); J. Cell Sci.107, 1137 (1994). / J. Cell Sci. / Lancet by Shah M. (1992)
  118. Shah M., Foreman D. M., J. Cell Sci.108, 985 (1995). (10.1242/jcs.108.3.985) / J. Cell Sci. by Shah M. (1995)
  119. McCallion R. L., Wood J. M., Foreman D. M., Ferguson M. W. J., Lancet, in press. / Lancet by McCallion R. L.
  120. Verrier B., Muller D., Bravo R., Muller R., EMBO. J.5, 913 (1986); (10.1002/j.1460-2075.1986.tb04303.x) / EMBO. J. by Verrier B. (1986)
  121. Martin P., Nobes C. D., Mech. Dev.38, 209 (1992); (10.1016/0925-4773(92)90054-N) / Mech. Dev. by Martin P. (1992)
  122. Pawar S., Kartha S., Toback F. G., J. Cell. Physiol.165, 556 (1995). (10.1002/jcp.1041650314) / J. Cell. Physiol. by Pawar S. (1995)
  123. Goliger J. A., Paul D. L., Mol. Biol. Cell6, 1491 (1995). (10.1091/mbc.6.11.1491) / Mol. Biol. Cell by Goliger J. A. (1995)
  124. Burgess L. P. A., et al., Arch. Otolaryngol. Head Neck Surg.116, 798 (1990). (10.1001/archotol.1990.01870070046008) / Arch. Otolaryngol. Head Neck Surg. by Burgess L. P. A. (1990)
  125. Frank S., Munz B., Werner S., Oncogene, in press. / Oncogene by Frank S.
  126. Nanney L. B. King L. E. in (1) pp. 171–194.
  127. 10.1126/science.3041594
  128. Marikovsky M., et al., Proc. Natl. Acad. Sci. U.S.A.90, 3889 (1993). (10.1073/pnas.90.9.3889) / Proc. Natl. Acad. Sci. U.S.A. by Marikovsky M. (1993)
  129. Mueller R. V., Hunt T. K., Tokunaga A., Spencer E. M., Arch. Surg.129, 262 (1994). (10.1001/archsurg.1994.01420270038008) / Arch. Surg. by Mueller R. V. (1994)
  130. Forsberg E., et al., Proc. Natl. Acad. Sci. U.S.A.93, 6594 (1996). (10.1073/pnas.93.13.6594) / Proc. Natl. Acad. Sci. U.S.A. by Forsberg E. (1996)
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 5:50 a.m.)
Deposited 1 year, 7 months ago (Jan. 12, 2024, 10:47 p.m.)
Indexed 6 hours, 21 minutes ago (Aug. 27, 2025, 12:39 p.m.)
Issued 28 years, 4 months ago (April 4, 1997)
Published 28 years, 4 months ago (April 4, 1997)
Published Print 28 years, 4 months ago (April 4, 1997)
Funders 0

None

@article{Martin_1997, title={Wound Healing--Aiming for Perfect Skin Regeneration}, volume={276}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.276.5309.75}, DOI={10.1126/science.276.5309.75}, number={5309}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Martin, Paul}, year={1997}, month=apr, pages={75–81} }