Hasumi Hisashi, Hasumi Yukiko, Baba Masaya, Nishi Hafumi, Furuya Mitsuko, Vocke Cathy D, Lang Martin, Irie Nobuko, Esumi Chiharu, Merino Maria J, Kawahara Takashi, Isono Yasuhiro, Makiyama Kazuhide, Warner Andrew C, Haines Diana C, Wei Ming-Hui, Zbar Berton, Hagenau Herbert, Feigenbaum Lionel, Kondo Keiichi, Nakaigawa Noboru, Yao Masahiro, Metwalli Adam R, Marston Linehan W, Schmidt Laura S
Urologic Oncology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Department of Urology and Molecular Genetics, Yokohama City University, Yokohama, Japan.
Hum Mol Genet. 2017 Jan 15;26(2):354-366. doi: 10.1093/hmg/ddw392.
Germline H255Y and K508R missense mutations in the folliculin (FLCN) gene have been identified in patients with bilateral multifocal (BMF) kidney tumours and clinical manifestations of Birt-Hogg-Dubé (BHD) syndrome, or with BMF kidney tumours as the only manifestation; however, their impact on FLCN function remains to be determined. In order to determine if FLCN H255Y and K508R missense mutations promote aberrant kidney cell proliferation leading to pathogenicity, we generated mouse models expressing these mutants using BAC recombineering technology and investigated their ability to rescue the multi-cystic phenotype of Flcn-deficient mouse kidneys. Flcn H255Y mutant transgene expression in kidney-targeted Flcn knockout mice did not rescue the multi-cystic kidney phenotype. However, expression of the Flcn K508R mutant transgene partially, but not completely, abrogated the phenotype. Notably, expression of the Flcn K508R mutant transgene in heterozygous Flcn knockout mice resulted in development of multi-cystic kidneys and cardiac hypertrophy in some mice. These results demonstrate that both FLCN H255Y and K508R missense mutations promote aberrant kidney cell proliferation, but to different degrees. Based on the phenotypes of our preclinical models, the FLCN H255Y mutant protein has lost it tumour suppressive function leading to the clinical manifestations of BHD, whereas the FLCN K508R mutant protein may have a dominant negative effect on the function of wild-type FLCN in regulating kidney cell proliferation and, therefore, act as an oncoprotein. These findings may provide mechanistic insight into the role of FLCN in regulating kidney cell proliferation and facilitate the development of novel therapeutics for FLCN-deficient kidney cancer.
在患有双侧多灶性(BMF)肾肿瘤且有Birt-Hogg-Dubé(BHD)综合征临床表现的患者中,或仅以BMF肾肿瘤为唯一表现的患者中,已鉴定出卵泡抑素(FLCN)基因的种系H255Y和K508R错义突变;然而,它们对FLCN功能的影响仍有待确定。为了确定FLCN H255Y和K508R错义突变是否会促进肾细胞异常增殖从而导致致病性,我们使用BAC重组技术生成了表达这些突变体的小鼠模型,并研究了它们挽救Flcn缺陷型小鼠肾脏多囊表型的能力。肾靶向Flcn基因敲除小鼠中Flcn H255Y突变转基因的表达未能挽救多囊肾表型。然而,Flcn K508R突变转基因的表达部分但未完全消除该表型。值得注意的是,Flcn K508R突变转基因在杂合Flcn基因敲除小鼠中的表达导致一些小鼠出现多囊肾和心脏肥大。这些结果表明,FLCN H255Y和K508R错义突变均会促进肾细胞异常增殖,但程度不同。基于我们临床前模型的表型,FLCN H255Y突变蛋白已丧失其肿瘤抑制功能,导致BHD的临床表现,而FLCN K508R突变蛋白可能对野生型FLCN调节肾细胞增殖的功能具有显性负效应,因此充当癌蛋白。这些发现可能为FLCN在调节肾细胞增殖中的作用提供机制性见解,并促进针对Flcn缺陷型肾癌的新型疗法的开发。