Wang Ying, Gupta Mihir, Poonawala Tasneem, Farooqui Mariya, Li Yunfang, Peng Fei, Rao Sheldon, Ansonoff Michael, Pintar John E, Gupta Kalpna
Vascular Biology Center, Division of Hematology/Oncology/Transplantation, Department of Medicine, University of Minnesota, Minneapolis, Minn.
Department of Neurosurgery, University of California San Diego, La Jolla, Calif.
Transl Res. 2017 Jul;185:13-23. doi: 10.1016/j.trsl.2017.05.003. Epub 2017 May 18.
We have previously shown that topical opioids including morphine and its congeners promote healing of full thickness ischemic wounds in rats. We examined the contribution of mu opioid receptor (MOPr)-mediated healing of full thickness ischemic wounds using MOPr and delta or kappa opioid receptor knockout (KO) mice. Wound closure in the early (day 5) as well as later phases was delayed in topical morphine or PBS-treated MOPr-KO mice compared with reciprocal treatments of wounds in wild-type (WT) mice. MOPr expression was significantly upregulated at 30 min in the wound margins and colocalized with wound margins and vasculature in the epidermal and dermal layers of the skin. We next examined whether neuropeptide expression was involved in the mechanism of MOPr-mediated wound closure. Substance P (SP) and calcitonin gene-related peptide immunoreactivity (ir) was significantly increased in the skin of MOPr-KO mice as compared with WT mice. Neuropeptide-ir was increased significantly in PBS-treated wounds of MOPr and WT mice, but morphine treatment reduced neuropeptide immunoreactivity in both as compared with PBS. Wounding of keratinocytes led to the release of opioid peptide beta-endorphin (β-END) in conditioned medium, which stimulated the proliferation of endothelial cells. MOPr-selective (D-Phe-Cys-Tyr-D-Trp-Orn-Thr-Pen-Thr-NH2, CTOP) and nonselective OPr antagonist naloxone-inhibited endothelial proliferation induced by wounded keratinocyte-conditioned medium. In addition, accelerated wound area closure in vitro by morphine was suppressed by methylnaltrexone, a nonselective OPr antagonist with high affinity for MOPr. Morphine and its congeners stimulated the proliferation of endothelial cells from WT mice but not those from MOPr-KO mice. Furthermore, morphine-induced mitogen-activated protein kinase/extracellular signal-regulated kinase phosphorylation in endothelial cells was significantly decreased in MOPr-KO mice as compared with WT mice. Collectively, these data suggest that MOPr plays a critical role in the proliferation phase with the formation of granulation tissue during wound healing.
我们之前已经表明,包括吗啡及其同系物在内的局部阿片类药物可促进大鼠全层缺血性伤口的愈合。我们使用μ阿片受体(MOPr)以及δ或κ阿片受体基因敲除(KO)小鼠,研究了MOPr介导的全层缺血性伤口愈合的作用。与野生型(WT)小鼠伤口的相应处理相比,局部应用吗啡或PBS处理的MOPr-KO小鼠在早期(第5天)以及后期的伤口闭合均延迟。MOPr表达在伤口边缘30分钟时显著上调,并与皮肤表皮和真皮层的伤口边缘及脉管系统共定位。接下来,我们研究了神经肽表达是否参与MOPr介导的伤口闭合机制。与WT小鼠相比,MOPr-KO小鼠皮肤中P物质(SP)和降钙素基因相关肽免疫反应性(ir)显著增加。在MOPr和WT小鼠的PBS处理伤口中,神经肽ir显著增加,但与PBS相比,吗啡处理均降低了两者的神经肽免疫反应性。角质形成细胞损伤导致条件培养基中阿片肽β-内啡肽(β-END)释放,其刺激内皮细胞增殖。MOPr选择性(D-苯丙氨酸-半胱氨酸-酪氨酸-D-色氨酸-鸟氨酸-苏氨酸-青霉胺-苏氨酸-酰胺,CTOP)和非选择性阿片受体拮抗剂纳洛酮抑制了损伤角质形成细胞条件培养基诱导的内皮细胞增殖。此外,吗啡在体外加速伤口面积闭合的作用被甲基纳曲酮抑制,甲基纳曲酮是一种对MOPr具有高亲和力的非选择性阿片受体拮抗剂。吗啡及其同系物刺激WT小鼠的内皮细胞增殖,但不刺激MOPr-KO小鼠的内皮细胞增殖。此外,与WT小鼠相比,MOPr-KO小鼠中吗啡诱导的内皮细胞丝裂原活化蛋白激酶/细胞外信号调节激酶磷酸化显著降低。总体而言,这些数据表明MOPr在伤口愈合过程中肉芽组织形成的增殖阶段起关键作用。