Recka Nicole, Simons Andrean, Cornell Robert A, Van Otterloo Eric
Department of Anatomy and Cell Biology, Carver College of Medicine, University of Iowa, Iowa City, Iowa, USA; Iowa Institute of Oral Health Research, College of Dentistry & Dental Clinics, University of Iowa, Iowa City, Iowa, USA; Interdisciplinary Graduate Program in Genetics, University of Iowa, Iowa City, Iowa, USA.
Department of Radiation Oncology, Carver College of Medicine, University of Iowa, Iowa City, Iowa, USA.
J Invest Dermatol. 2025 May 7. doi: 10.1016/j.jid.2025.04.008.
During skin development, ectoderm-derived cells undergo precisely coordinated proliferation, differentiation, and adhesion to yield stratified epidermis. Disruptions in these processes can result in congenital anomalies, including ectodermal dysplasia and harlequin ichthyosis. PRMT5-an enzyme responsible for methylating arginine residues in histones and other proteins-maintains progenitor status in germ and limb bud cells. Similarly, in vitro evidence suggests that PRMT5 prevents differentiation of basal keratinocytes, leading us to hypothesize that PRMT5 preserves the stem-cell phenotype of keratinocytes in vivo. To test this possibility, we generated conditional knockout mice lacking Prmt5 in early ectoderm (embryonic day 7.5), impacting the entire epidermis. Prmt5 conditional knockouts exhibited gross skin defects, compromised skin barrier function, and reduced postnatal viability. Histological analyses revealed significant defects in epidermal stratification, without alterations in apoptosis or proliferation. Single-cell RNA sequencing and Assay for Transposase-Accessible Chromatin with high-throughput sequencing analysis identified an atypical population of basal keratinocyte-like cells in Prmt5 conditional knockouts that exhibited a senescence-like program, characterized by increased Cdkn1a (p21), elevated senescence-associated secretory phenotype molecules (Igfbp2), and decreased developmental transcription factor (Trp63) expression. Our findings suggest that PRMT5 prevents basal keratinocyte senescence by repressing Cdkn1a, shedding light on the epigenetic regulation of basal keratinocyte maintenance and senescence in congenital skin disorders.
在皮肤发育过程中,外胚层来源的细胞经历精确协调的增殖、分化和黏附,以产生分层的表皮。这些过程的破坏可导致先天性异常,包括外胚层发育不良和丑角鱼鳞病。PRMT5是一种负责组蛋白和其他蛋白质中精氨酸残基甲基化的酶,在生殖细胞和肢芽细胞中维持祖细胞状态。同样,体外证据表明PRMT5可防止基底角质形成细胞分化,这使我们推测PRMT5在体内维持角质形成细胞的干细胞表型。为了验证这种可能性,我们构建了在早期外胚层(胚胎第7.5天)缺乏Prmt5的条件性敲除小鼠,这会影响整个表皮。Prmt5条件性敲除小鼠表现出明显的皮肤缺陷、受损的皮肤屏障功能和出生后存活率降低。组织学分析显示表皮分层存在显著缺陷,而细胞凋亡或增殖无改变。单细胞RNA测序和转座酶可及染色质高通量测序分析确定,Prmt5条件性敲除小鼠中有一群非典型的基底角质形成细胞样细胞,其表现出类似衰老的程序,特征为Cdkn1a(p21)增加、衰老相关分泌表型分子(Igfbp2)升高以及发育转录因子(Trp63)表达降低。我们的研究结果表明,PRMT5通过抑制Cdkn1a来防止基底角质形成细胞衰老,这为先天性皮肤疾病中基底角质形成细胞维持和衰老的表观遗传调控提供了线索。