Division of Gastroenterology, Hepatology and Nutrition, Boston Children's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
Congenital Enteropathy Program, Boston Children's Hospital, Boston, Massachusetts, USA.
J Clin Invest. 2023 Oct 16;133(20):e169234. doi: 10.1172/JCI169234.
Microvillus inclusion disease (MVID), caused by loss-of-function mutations in the motor protein myosin Vb (MYO5B), is a severe infantile disease characterized by diarrhea, malabsorption, and acid/base instability, requiring intensive parenteral support for nutritional and fluid management. Human patient-derived enteroids represent a model for investigation of monogenic epithelial disorders but are a rare resource from MVID patients. We developed human enteroids with different loss-of function MYO5B variants and showed that they recapitulated the structural changes found in native MVID enterocytes. Multiplex immunofluorescence imaging of patient duodenal tissues revealed patient-specific changes in localization of brush border transporters. Functional analysis of electrolyte transport revealed profound loss of Na+/H+ exchange (NHE) activity in MVID patient enteroids with near-normal chloride secretion. The chloride channel-blocking antidiarrheal drug crofelemer dose-dependently inhibited agonist-mediated fluid secretion. MVID enteroids exhibited altered differentiation and maturation versus healthy enteroids. γ-Secretase inhibition with DAPT recovered apical brush border structure and functional Na+/H+ exchange activity in MVID enteroids. Transcriptomic analysis revealed potential pathways involved in the rescue of MVID cells including serum/glucocorticoid-regulated kinase 2 (SGK2) and NHE regulatory factor 3 (NHERF3). These results demonstrate the utility of patient-derived enteroids for developing therapeutic approaches to MVID.
微绒毛包涵体病(MVID)是一种严重的婴儿疾病,由肌球蛋白 Vb(MYO5B)的功能丧失突变引起,其特征为腹泻、吸收不良和酸碱不稳定,需要进行密集的肠外支持以进行营养和液体管理。源自人类患者的肠类器官代表了研究单基因上皮疾病的模型,但作为 MVID 患者的罕见资源。我们开发了具有不同功能丧失 MYO5B 变体的人类肠类器官,并表明它们再现了天然 MVID 肠细胞中发现的结构变化。对患者十二指肠组织的多重免疫荧光成像揭示了刷状缘转运蛋白定位的患者特异性变化。电解质转运的功能分析显示,MVID 患者肠类器官中 Na+/H+交换(NHE)活性严重丧失,而氯离子分泌接近正常。氯通道阻断性止泻药克罗非尼可剂量依赖性地抑制激动剂介导的液体分泌。与健康肠类器官相比,MVID 肠类器官表现出分化和成熟的改变。用 DAPT 抑制 γ-分泌酶可恢复 MVID 肠类器官的顶端刷状缘结构和功能性 Na+/H+交换活性。转录组分析揭示了参与 MVID 细胞拯救的潜在途径,包括血清/糖皮质激素调节激酶 2(SGK2)和 NHE 调节因子 3(NHERF3)。这些结果表明,源自患者的肠类器官可用于开发针对 MVID 的治疗方法。