Ferguson Mark W J, O'Kane Sharon
UK Centre for Tissue Engineering, School of Biological Sciences, University of Manchester, 3.239 Stopford Building, Oxford Road, Manchester M13 9PT, UK.
Philos Trans R Soc Lond B Biol Sci. 2004 May 29;359(1445):839-50. doi: 10.1098/rstb.2004.1475.
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.
在人类和家畜中,创伤、手术、烧伤或运动损伤后皮肤产生瘢痕是一个重大医学问题,常常导致不良美观、功能丧失、组织活动和/或生长受限以及不良心理影响。目前的治疗方法是经验性的、不可靠且不可预测的:尚无用于预防或治疗皮肤瘢痕形成的处方药。早期哺乳动物胚胎的皮肤伤口能完美愈合且不留瘢痕,而成体哺乳动物的伤口则会形成瘢痕。我们研究了胚胎伤口无瘢痕愈合与成体伤口瘢痕形成愈合之间的细胞和分子差异。重要差异包括炎症反应,胚胎伤口中的炎症反应由数量较少、分化程度较低的炎症细胞组成。这一点,再加上参与皮肤生长和形态发生的高水平形态发生分子,意味着愈合中的胚胎伤口的生长因子谱与成体伤口的截然不同。因此,无瘢痕愈合的胚胎伤口中转化生长因子β1(TGFβ1)和转化生长因子β2(TGFβ2)水平较低,血小板衍生生长因子水平较低,而转化生长因子β3(TGFβ3)水平较高。我们已通过实验对小鼠、大鼠和猪的成体伤口愈合进行调控,以模拟无瘢痕的胚胎状态,例如中和血小板衍生生长因子、中和TGFβ1和TGFβ2或添加外源性TGFβ3。这些实验使成体伤口实现了无瘢痕愈合。此类实验已确定了治疗靶点,我们据此研发了新型药物分子,这些分子能显著改善或完全预防实验动物成体伤口愈合过程中的瘢痕形成。其中一些新药已成功完成安全性及其他研究,从而在获得相关监管机构批准后进入人体临床试验。初步试验采用双盲随机设计,将药物或安慰剂应用于人类志愿者手臂下的实验切口伤口或打孔活检伤口。基于此类人体志愿者研究的鼓舞人心的结果,先导药物现已进入以人类患者为对象的试验,例如在皮肤移植供区。我们考虑了伤口愈合、瘢痕形成和再生的进化背景。我们推测,进化压力作用于中等大小、广泛存在、有相当组织损伤的脏伤口,例如咬伤、擦伤和挫伤。由尖锐物体造成且在清洁或无菌环境中、组织紧密对合情况下愈合的现代伤口(如因创伤或手术导致)是新出现的情况,在自然界中以前未曾遇到过,进化选择的伤口愈合反应对此有些不适用。我们还证明,瘢痕修复和再生在同一动物(包括人类)体内,甚至在同一组织内都可能发生,这表明它们具有相似的机制和调节因子。因此,通过巧妙改变成体伤口愈合过程中存在的生长因子比例,我们能够诱导成体伤口完美愈合且不留瘢痕,实现加速愈合且无不良影响,例如对伤口强度或伤口感染率无不良影响。这意味着瘢痕形成可能不再是现代损伤或手术的必然结果,现在有可能采用全新的药物方法来预防人类瘢痕形成。除皮肤外,许多组织在损伤后都会出现瘢痕形成。因此,改善瘢痕的药物可能具有广泛益处,并能预防多个组织中的并发症,例如预防眼外伤后瘢痕形成导致的失明,通过消除胶质瘢痕促进中枢和外周神经系统中的神经元重新连接,通过预防胃肠道或生殖系统损伤后的狭窄和粘连恢复正常肠道和生殖功能,以及通过预防肌腱和韧带中的瘢痕形成恢复运动功能。