Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73104, United States.
Department of Ophthalmology/Optometry, Research Program for Experimental Ophthalmology and Glaucoma Research, Paracelsus Medical University/SALK, Salzburg, Austria; Department of Anatomy and Cell Biology, Paracelsus Medical University, Salzburg, Austria.
Exp Eye Res. 2020 Dec;201:108252. doi: 10.1016/j.exer.2020.108252. Epub 2020 Sep 19.
Choroidal all- trans -retinoic acid (atRA) may play a key role in the control of postnatal eye growth in a variety of vertebrates through modulation of scleral extracellular matrix synthesis and may therefore play a crucial role in the development of myopia. In the chick eye, choroidal atRA synthesis is exclusively regulated by its synthesizing enzyme, retinaldehyde dehydrogenase 2 (RALDH2). In chicks and humans, RALDH2 has been detected in a population of hitherto uncharacterized choroidal cells.Therefore, the aim of this study was to identify the RALDH2+ cell type(s) in the choroid and determine how these cells modulate atRA concentrations during periods of visually guided eye growth. Chicks wore translucent goggles on one eye for 10 days and choroids were analyzed for RALDH activity and RALDH2 protein expression at days 0, 1, 4, 7, 15 following removal of the goggle ("recovery"); choroids from contralateral eyes served as controls. The presence of RALDH2+ cells was assessed in chick choroid wholemounts using multiphoton microscopy. RALDH2 protein expression was measured by western blot and RALDH2 activity was assessed via HPLC quantification of atRA. Cell proliferation was assessed by BrdU-labelling in combination with RALDH2-immunohistochemistry. For characterization of RALDH2+ cells, immunohistochemistry for various tissue specific markers was applied in chicken (Ia antigen, CD5, Col1-propeptide, desmin, IgY, L-Cam, Cadherin1, MHC-II; Tcr-γδ, vimentin) and human donor tissue (α-smooth-muscle-actin, CD's 31/34/68/146, desmin, IBA1, LYVE-1, PGP9.5, vimentin) followed by confocal microscopy. In the chick and human choroid, RALDH2+ cells with variable morphology were present in the stroma and adjacent to choroidal blood vessels. In chick wholemounts, RALDH2+ cells were concentrated toward the choriocapillaris, and their number increased nearly linearly between 1 and 7 days of recovery and plateaued between 7 and 15 days compared to corresponding controls. A significant increase in choroidal RALDH2 protein concentration and atRA synthetic activity was observed by four days of recovery (↑107% and ↑120%) by western blot and HPLC, respectively. A 3-fold increase in RALDH2+/BrDU+ cells was observed following 4 days of recovery compared to controls (12.43 ± 0.73% of all RALDH2+ cells in recovering eyes as compared with 4.46 ± 0.63% in control eyes, p < 0.001). In chick choroids, the vast majority of RALDH2+ cells co-expressed Col1-propetide, but did not co-label with any other antibodies tested. In human choroid, some, but not all RALDH2+ cells colocalized with vimentin, but were negative for all other antibodies tested. RALDH2+ cells represent a novel cell type in the chick and human choroid. Our findings that some human RALDH2+ cells were positive for vimentin and all chick RALDH2+ cells were positive for Col1, suggest that RALDH2+ cells most closely resemble perivascular and stromal fibroblasts. The increased number of RALDH2+/BRDU+ cells following 4 days of recovery suggests that choroidal atRA concentrations are partially controlled by proliferation of RALDH2+ cells. The identification of this choroidal cell type will provide a broader understanding of the cellular events responsible for the regulation of postnatal ocular growth, and may provide new avenues for specifically targeted strategies for the treatment of myopia.
脉络膜全反式视黄酸(atRA)可能通过调节巩膜细胞外基质的合成,在多种脊椎动物中对出生后眼球生长的控制起关键作用,因此可能在近视的发展中起关键作用。在鸡眼中,脉络膜 atRA 的合成仅受其合成酶视黄醛脱氢酶 2(RALDH2)的调节。在鸡和人中,已经在一群尚未明确特征的脉络膜细胞中检测到 RALDH2。因此,本研究的目的是鉴定脉络膜中的 RALDH2+细胞类型,并确定这些细胞在视觉引导的眼球生长过程中如何调节 atRA 浓度。小鸡在一只眼睛上戴半透明的护目镜 10 天,在去除护目镜后第 0、1、4、7、15 天分析脉络膜的 RALDH 活性和 RALDH2 蛋白表达(“恢复”);对侧眼的脉络膜作为对照。使用多光子显微镜在鸡脉络膜整体标本中评估 RALDH2+细胞的存在。通过 Western blot 测量 RALDH2 蛋白表达,通过 HPLC 定量分析 atRA 评估 RALDH2 活性。通过 BrdU 标记与 RALDH2 免疫组织化学相结合评估细胞增殖。为了鉴定 RALDH2+细胞,在鸡(Ia 抗原、CD5、Col1-前肽、结蛋白、IgY、L-Cam、钙粘蛋白 1、MHC-II;Tcr-γδ、波形蛋白)和人供体组织(α-平滑肌-肌动蛋白、CD's 31/34/68/146、结蛋白、IBA1、LYVE-1、PGP9.5、波形蛋白)中应用免疫组织化学进行各种组织特异性标志物的检测,然后进行共聚焦显微镜分析。在鸡和人脉络膜中,在基质中和脉络膜血管附近存在形态各异的 RALDH2+细胞。在鸡整体标本中,RALDH2+细胞集中在脉络膜毛细血管附近,与相应的对照相比,在恢复的第 1 天至第 7 天之间,它们的数量几乎呈线性增加,在第 7 天至第 15 天之间达到平台期。Western blot 和 HPLC 分别显示,在恢复的第 4 天观察到脉络膜 RALDH2 蛋白浓度和 atRA 合成活性显著增加(↑107%和↑120%)。与对照组相比,在恢复的第 4 天观察到 RALDH2+/BrDU+细胞增加了 3 倍(恢复眼中所有 RALDH2+细胞中有 12.43±0.73%为 RALDH2+/BrDU+细胞,而对照眼中为 4.46±0.63%,p<0.001)。在鸡脉络膜中,绝大多数 RALDH2+细胞共表达 Col1-前肽,但与测试的任何其他抗体均不共标记。在人脉络膜中,一些但不是所有的 RALDH2+细胞与波形蛋白共定位,但与测试的所有其他抗体均为阴性。RALDH2+细胞是鸡和人脉络膜中的一种新的细胞类型。我们的研究结果表明,一些人 RALDH2+细胞对波形蛋白呈阳性,而所有鸡 RALDH2+细胞对 Col1 呈阳性,表明 RALDH2+细胞最类似于血管周和基质成纤维细胞。在恢复的第 4 天观察到 RALDH2+/BRDU+细胞数量增加表明,脉络膜 atRA 浓度部分受到 RALDH2+细胞增殖的控制。鉴定这种脉络膜细胞类型将更全面地了解调节出生后眼球生长的细胞事件,并可能为近视的治疗提供新的靶向策略。