Scar–free healing: from embryonic mechanisms to adult therapeutic intervention
In man and domestic animals, scarring in the skin after trauma, surgery, burn or sports injury is a major medical problem, often resulting in adverse aesthetics, loss of function, restriction of tissue movement and/or growth and adverse psychological effects. Current treatments are empirical, unreli...
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| Published in | Philosophical transactions of the Royal Society of London. Series B. Biological sciences Vol. 359; no. 1445; pp. 839 - 850 |
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| Main Authors | , |
| Format | Journal Article |
| Language | English |
| Published |
England
The Royal Society
29.05.2004
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| Subjects | |
| Online Access | Get full text |
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| Abstract | In man and domestic animals, scarring in the skin after trauma, surgery, burn or sports injury is a major medical problem, often resulting in adverse aesthetics, loss of function, restriction of tissue movement and/or growth and adverse psychological effects. Current treatments are empirical, unreliable and unpredictable: there are no prescription drugs for the prevention or treatment of dermal scarring. Skin wounds on early mammalian embryos heal perfectly with no scars whereas wounds to adult mammals scar. We investigated the cellular and molecular differences between scar-free healing in embryonic wounds and scar-forming healing in adult wounds. Important differences include the inflammatory response, which in embryonic wounds consists of lower numbers of less differentiated inflammatory cells. This, together with high levels of morphogenetic molecules involved in skin growth and morphogenesis, means that the growth factor profile in a healing embryonic wound is very different from that in an adult wound. Thus, embryonic wounds that heal without a scar have low levels of TGFβ1 and TGFβ2, low levels of platelet-derived growth factor and high levels of TGFβ3. We have experimentally manipulated healing adult wounds in mice, rats and pigs to mimic the scar-free embryonic profile, e.g. neutralizing PDGF, neutralizing TGFβ1 and TGFβ2 or adding exogenous TGFβ3. These experiments result in scar-free wound healing in the adult. Such experiments have allowed the identification of therapeutic targets to which we have developed novel pharmaceutical molecules, which markedly improve or completely prevent scarring during adult wound healing in experimental animals. Some of these new drugs have successfully completed safety and other studies, such that they have entered human clinical trials with approval from the appropriate regulatory authorities. Initial trials involve application of the drug or placebo in a double-blind randomized design, to experimental incision or punch biopsy wounds under the arms of human volunteers. Based on encouraging results from such human volunteer studies, the lead drugs have now entered human patient-based trials e.g. in skin graft donor sites. We consider the evolutionary context of wound healing, scarring and regeneration. We hypothesize that evolutionary pressures have been exerted on intermediate sized, widespread, dirty wounds with considerable tissue damage e.g. bites, bruises and contusions. Modern wounds (e.g. resulting from trauma or surgery) caused by sharp objects and healing in a clean or sterile environment with close tissue apposition are new occurrences, not previously encountered in nature and to which the evolutionary selected wound healing responses are somewhat inappropriate. We also demonstrate that both repair with scarring and regeneration can occur within the same animal, including man, and indeed within the same tissue, thereby suggesting that they share similar mechanisms and regulators. Consequently, by subtly altering the ratio of growth factors present during adult wound healing, we can induce adult wounds to heal perfectly with no scars, with accelerated healing and with no adverse effects, e.g. on wound strength or wound infection rates. This means that scarring may no longer be an inevitable consequence of modern injury or surgery and that a completely new pharmaceutical approach to the prevention of human scarring is now possible. Scarring after injury occurs in many tissues in addition to the skin. Thus scar-improving drugs could have widespread benefits and prevent complications in several tissues, e.g. prevention of blindness after scarring due to eye injury, facilitation of neuronal reconnections in the central and peripheral nervous system by the elimination of glial scarring, restitution of normal gut and reproductive function by preventing strictures and adhesions after injury to the gastrointestinal or reproductive systems, and restoration of locomotor function by preventing scarring in tendons and ligaments. |
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| AbstractList | In man and domestic animals, scarring in the skin after trauma, surgery, burn or sports injury is a major medical problem, often resulting in adverse aesthetics, loss of function, restriction of tissue movement and/or growth and adverse psychological effects. Current treatments are empirical, unreliable and unpredictable: there are no prescription drugs for the prevention or treatment of dermal scarring. Skin wounds on early mammalian embryos heal perfectly with no scars whereas wounds to adult mammals scar. We investigated the cellular and molecular differences between scar-free healing in embryonic wounds and scar-forming healing in adult wounds. Important differences include the inflammatory response, which in embryonic wounds consists of lower numbers of less differentiated inflammatory cells. This, together with high levels of morphogenetic molecules involved in skin growth and morphogenesis, means that the growth factor profile in a healing embryonic wound is very different from that in an adult wound. Thus, embryonic wounds that heal without a scar have low levels of TGFbeta1 and TGFbeta2, low levels of platelet-derived growth factor and high levels of TGFbeta3. We have experimentally manipulated healing adult wounds in mice, rats and pigs to mimic the scar-free embryonic profile, e.g. neutralizing PDGF, neutralizing TGFbeta1 and TGFbeta2 or adding exogenous TGFbeta3. These experiments result in scar-free wound healing in the adult. Such experiments have allowed the identification of therapeutic targets to which we have developed novel pharmaceutical molecules, which markedly improve or completely prevent scarring during adult wound healing in experimental animals. Some of these new drugs have successfully completed safety and other studies, such that they have entered human clinical trials with approval from the appropriate regulatory authorities. Initial trials involve application of the drug or placebo in a double-blind randomized design, to experimental incision or punch biopsy wounds under the arms of human volunteers. Based on encouraging results from such human volunteer studies, the lead drugs have now entered human patient-based trials e.g. in skin graft donor sites. We consider the evolutionary context of wound healing, scarring and regeneration. We hypothesize that evolutionary pressures have been exerted on intermediate sized, widespread, dirty wounds with considerable tissue damage e.g. bites, bruises and contusions. Modem wounds (e.g. resulting from trauma or surgery) caused by sharp objects and healing in a clean or sterile environment with close tissue apposition are new occurrences, not previously encountered in nature and to which the evolutionary selected wound healing responses are somewhat inappropriate. We also demonstrate that both repair with scarring and regeneration can occur within the same animal, including man, and indeed within the same tissue, thereby suggesting that they share similar mechanisms and regulators. Consequently, by subtly altering the ratio of growth factors present during adult wound healing, we can induce adult wounds to heal perfectly with no scars, with accelerated healing and with no adverse effects, e.g. on wound strength or wound infection rates. This means that scarring may no longer be an inevitable consequence of modem injury or surgery and that a completely new pharmaceutical approach to the prevention of human scarring is now possible. Scarring after injury occurs in many tissues in addition to the skin. Thus scar-improving drugs could have widespread benefits and prevent complications in several tissues, e.g. prevention of blindness after scarring due to eye injury, facilitation of neuronal reconnections in the central and peripheral nervous system by the elimination of glial scarring, restitution of normal gut and reproductive function by preventing strictures and adhesions after injury to the gastrointestinal or reproductive systems, and restoration of locomotor function by preventing scarring in tendons and ligaments. In man and domestic animals, scarring in the skin after trauma, surgery, burn or sports injury is a major medical problem, often resulting in adverse aesthetics, loss of function, restriction of tissue movement and/or growth and adverse psychological effects. Current treatments are empirical, unreliable and unpredictable: there are no prescription drugs for the prevention or treatment of dermal scarring. Skin wounds on early mammalian embryos heal perfectly with no scars whereas wounds to adult mammals scar. We investigated the cellular and molecular differences between scar-free healing in embryonic wounds and scar-forming healing in adult wounds. Important differences include the inflammatory response, which in embryonic wounds consists of lower numbers of less differentiated inflammatory cells. This, together with high levels of morphogenetic molecules involved in skin growth and morphogenesis, means that the growth factor profile in a healing embryonic wound is very different from that in an adult wound. Thus, embryonic wounds that heal without a scar have low levels of TGFβ1 and TGFβ2, low levels of platelet-derived growth factor and high levels of TGFβ3. We have experimentally manipulated healing adult wounds in mice, rats and pigs to mimic the scar-free embryonic profile, e.g. neutralizing PDGF, neutralizing TGFβ1 and TGFβ2 or adding exogenous TGFβ3. These experiments result in scar-free wound healing in the adult. Such experiments have allowed the identification of therapeutic targets to which we have developed novel pharmaceutical molecules, which markedly improve or completely prevent scarring during adult wound healing in experimental animals. Some of these new drugs have successfully completed safety and other studies, such that they have entered human clinical trials with approval from the appropriate regulatory authorities. Initial trials involve application of the drug or placebo in a double-blind randomized design, to experimental incision or punch biopsy wounds under the arms of human volunteers. Based on encouraging results from such human volunteer studies, the lead drugs have now entered human patient-based trials e.g. in skin graft donor sites. We consider the evolutionary context of wound healing, scarring and regeneration. We hypothesize that evolutionary pressures have been exerted on intermediate sized, widespread, dirty wounds with considerable tissue damage e.g. bites, bruises and contusions. Modern wounds (e.g. resulting from trauma or surgery) caused by sharp objects and healing in a clean or sterile environment with close tissue apposition are new occurrences, not previously encountered in nature and to which the evolutionary selected wound healing responses are somewhat inappropriate. We also demonstrate that both repair with scarring and regeneration can occur within the same animal, including man, and indeed within the same tissue, thereby suggesting that they share similar mechanisms and regulators. Consequently, by subtly altering the ratio of growth factors present during adult wound healing, we can induce adult wounds to heal perfectly with no scars, with accelerated healing and with no adverse effects, e.g. on wound strength or wound infection rates. This means that scarring may no longer be an inevitable consequence of modern injury or surgery and that a completely new pharmaceutical approach to the prevention of human scarring is now possible. Scarring after injury occurs in many tissues in addition to the skin. Thus scar-improving drugs could have widespread benefits and prevent complications in several tissues, e.g. prevention of blindness after scarring due to eye injury, facilitation of neuronal reconnections in the central and peripheral nervous system by the elimination of glial scarring, restitution of normal gut and reproductive function by preventing strictures and adhesions after injury to the gastrointestinal or reproductive systems, and restoration of locomotor function by preventing scarring in tendons and ligaments. In man and domestic animals, scarring in the skin after trauma, surgery, burn or sports injury is a major medical problem, often resulting in adverse aesthetics, loss of function, restriction of tissue movement and/or growth and adverse psychological effects. Current treatments are empirical, unreliable and unpredictable: there are no prescription drugs for the prevention or treatment of dermal scarring. Skin wounds on early mammalian embryos heal perfectly with no scars whereas wounds to adult mammals scar. We investigated the cellular and molecular differences between scar–free healing in embryonic wounds and scar–forming healing in adult wounds. Important differences include the inflammatory response, which in embryonic wounds consists of lower numbers of less differentiated inflammatory cells. This, together with high levels of morphogenetic molecules involved in skin growth and morphogenesis, means that the growth factor profile in a healing embryonic wound is very different from that in an adult wound. Thus, embryonic wounds that heal without a scar have low levels of TGFβ1 and TGFβ2, low levels of platelet–derived growth factor and high levels of TGFβ3. We have experimentally manipulated healing adult wounds in mice, rats and pigs to mimic the scar–free embryonic profile, e.g. neutralizing PDGF, neutralizing TGFβ1 and TGFβ2 or adding exogenous TGFβ3. These experiments result in scar–free wound healing in the adult. Such experiments have allowed the identification of therapeutic targets to which we have developed novel pharmaceutical molecules, which markedly improve or completely prevent scarring during adult wound healing in experimental animals. Some of these new drugs have successfully completed safety and other studies, such that they have entered human clinical trials with approval from the appropriate regulatory authorities. Initial trials involve application of the drug or placebo in a double–blind randomized design, to experimental incision or punch biopsy wounds under the arms of human volunteers. Based on encouraging results from such human volunteer studies, the lead drugs have now entered human patient–based trials e.g. in skin graft donor sites. We consider the evolutionary context of wound healing, scarring and regeneration. We hypothesize that evolutionary pressures have been exerted on intermediate sized, widespread, dirty wounds with considerable tissue damage e.g. bites, bruises and contusions. Modern wounds (e.g. resulting from trauma or surgery) caused by sharp objects and healing in a clean or sterile environment with close tissue apposition are new occurrences, not previously encountered in nature and to which the evolutionary selected wound healing responses are somewhat inappropriate. We also demonstrate that both repair with scarring and regeneration can occur within the same animal, including man, and indeed within the same tissue, thereby suggesting that they share similar mechanisms and regulators. Consequently, by subtly altering the ratio of growth factors present during adult wound healing, we can induce adult wounds to heal perfectly with no scars, with accelerated healing and with no adverse effects, e.g. on wound strength or wound infection rates. This means that scarring may no longer be an inevitable consequence of modern injury or surgery and that a completely new pharmaceutical approach to the prevention of human scarring is now possible. Scarring after injury occurs in many tissues in addition to the skin. Thus scar–improving drugs could have widespread benefits and prevent complications in several tissues, e.g. prevention of blindness after scarring due to eye injury, facilitation of neuronal reconnections in the central and peripheral nervous system by the elimination of glial scarring, restitution of normal gut and reproductive function by preventing strictures and adhesions after injury to the gastrointestinal or reproductive systems, and restoration of locomotor function by preventing scarring in tendons and ligaments. |
| Author | Ferguson, Mark W. J. O'Kane, Sharon |
| AuthorAffiliation | UK Centre for Tissue Engineering, School of Biological Sciences, University of Manchester, 3.239 Stopford Building, Oxford Road, Manchester M13 9PT, UK. mark.ferguson@man.ac.uk |
| AuthorAffiliation_xml | – name: UK Centre for Tissue Engineering, School of Biological Sciences, University of Manchester, 3.239 Stopford Building, Oxford Road, Manchester M13 9PT, UK. mark.ferguson@man.ac.uk |
| Author_xml | – sequence: 3 givenname: Mark W. J. surname: Ferguson fullname: Ferguson, Mark W. J. email: mark.ferguson@man.ac.uk organization: UK Centre for Tissue Engineering, School of Biological Sciences, University of Manchester, 3.239 Stopford Building, Oxford Road, Manchester M13 9PT, UK – sequence: 4 givenname: Sharon surname: O'Kane fullname: O'Kane, Sharon organization: Renovo Limited, Manchester Incubator Building, 48 Grafton Street, Manchester M13 9XX, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/15293811$$D View this record in MEDLINE/PubMed |
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| References_xml | – ident: p_38 doi: 10.1038/35018085 – volume: 112 start-page: 651 year: 1991 ident: p_39 article-title: The extracellular matrix of lip wounds in fetal, neonatal and adult mice publication-title: Development doi: 10.1242/dev.112.2.651 contributor: fullname: Whitby D. J. – ident: p_22 doi: 10.1098/rstb.2004.1472 – volume: 107 start-page: 1137 year: 1994 ident: p_34 article-title: Neutralising antibody to TGF~1,2, reduces scarring in adult rodents publication-title: J. Cell Sci. doi: 10.1242/jcs.107.5.1137 contributor: fullname: Shah M. – volume: 108 start-page: 985 year: 1995 ident: p_35 article-title: Neutralisation of TGF~1 and TGF~2 or exogenous addition of TGF~3 to cutaneous rat wounds reduces scarring publication-title: J. Cell Sci. doi: 10.1242/jcs.108.3.985 contributor: fullname: Shah M. – ident: p_18 doi: 10.1098/rstb.2004.1468 – ident: p_2 – volume: 43 start-page: 2250 year: 2002 ident: p_31 article-title: Retinal microenvironment controls resident and infiltrating macrophage function during uveoretinitis publication-title: Invest. Ophthalmol. Visual Sci. contributor: fullname: Robertson M. J. – ident: p_37 doi: 10.1002/jez.10144 – ident: p_26 doi: 10.1016/S1357-2725(96)00120-3 – ident: p_24 doi: 10.1016/S0960-9822(02)00839-4 – ident: p_32 doi: 10.1093/oxfordjournals.molbev.a004023 – ident: p_30 doi: 10.1007/978-3-642-49295-2_8 – ident: p_28 – ident: p_20 doi: 10.1097/00000658-199401000-00011 – volume: 99 start-page: 583 year: 1991 ident: p_41 article-title: Rapid epithelialisation of fetal wounds is associated with the early deposition of tenascin publication-title: J. Cell Sci. doi: 10.1242/jcs.99.3.583 contributor: fullname: Whitby D. J. – ident: p_3 doi: 10.1038/nm1197-1209 – ident: p_19 doi: 10.1098/rstb.2004.1467 – ident: p_42 doi: 10.1073/pnas.94.4.1441 – volume: 11 start-page: 424 year: 2001 ident: p_12 article-title: Expression of TGF-~ and its receptors in murine fetal and adult dermal wounds publication-title: Eur. J. Dermatol. contributor: fullname: Cowin A. J. – ident: p_11 doi: 10.1002/(SICI)1097-0177(199807)212:3<385::AID-AJA6>3.0.CO;2-D – ident: p_4 doi: 10.1111/1523-1747.ep12289705 – ident: p_5 doi: 10.1046/j.1469-7580.1997.19030351.x – ident: p_16 – ident: p_8 doi: 10.1097/00006534-199811000-00022 – ident: p_10 – volume: 161 start-page: 1983 year: 1998 ident: p_13 article-title: Initial cytokine exposure determines function of macrophages and renders them unresponsive to other cytokines publication-title: J. Immunol. doi: 10.4049/jimmunol.161.4.1983 contributor: fullname: Erwig L.-P. – ident: p_33 doi: 10.1016/0140-6736(92)90009-R – ident: p_27 doi: 10.1038/ng1295-409 – ident: p_17 doi: 10.1097/00006534-199604000-00029 – ident: p_29 doi: 10.1002/dvdy.10242 – ident: p_6 doi: 10.1016/S0002-9440(10)65217-0 – ident: p_14 doi: 10.1097/00041552-200105000-00007 – ident: p_25 doi: 10.1007/978-3-0348-8354-2_8 – ident: p_7 doi: 10.1136/bmj.326.7380.88 – ident: p_36 doi: 10.1201/b14004-11 – ident: p_1 doi: 10.1006/dbio.1995.1141 – ident: p_40 doi: 10.1016/S0012-1606(05)80018-1 – ident: p_9 doi: 10.1172/JCI11867 – ident: p_15 doi: 10.1016/S0168-8278(00)80412-2 – ident: p_23 doi: 10.1098/rstb.2004.1470 – ident: p_21 doi: 10.1007/978-1-4899-0185-9_18 |
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| Snippet | In man and domestic animals, scarring in the skin after trauma, surgery, burn or sports injury is a major medical problem,
often resulting in adverse... In man and domestic animals, scarring in the skin after trauma, surgery, burn or sports injury is a major medical problem, often resulting in adverse... |
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| SubjectTerms | Adults Biological Evolution Cicatrix - drug therapy Cicatrix - physiopathology Embryo, Mammalian - physiology Healing Humans Medical treatment Molecules Physical trauma Platelet-Derived Growth Factor Regeneration Regeneration - physiology Regenerative Medicine Scarring Scars Skin Skin - pathology Skin Pharmaceuticals Skin Physiological Phenomena Tissue repair Transforming Growth Factor Beta Transforming Growth Factor beta - therapeutic use Transforming Growth Factor beta1 Transforming Growth Factor beta2 Transforming Growth Factor beta3 Wound Healing Wound Healing - physiology |
| Title | Scar–free healing: from embryonic mechanisms to adult therapeutic intervention |
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