Jackson Carolyn C, Best Lucy, Lorenzo Lazaro, Casanova Jean-Laurent, Wacker Jochen, Bertz Simone, Agaimy Abbas, Harrer Thomas
St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA.
Department of Pediatrics, The Memorial Sloan Kettering Cancer Center, New York, NY, USA.
J Clin Immunol. 2016 Jan;36(1):19-27. doi: 10.1007/s10875-015-0225-6. Epub 2015 Dec 19.
Collagen and calcium-binding EGF domain-containing protein 1 (CCBE1) bi-allelic mutations have been associated with syndromes of widespread congenital lymphatic dysplasia, including Hennekam Syndrome (HS). HS is characterized by lymphedema, lymphangiectasia, and intellectual disability. CCBE1 encodes a putative extracellular matrix protein but the HS-causing mutations have not been studied biochemically. We report two HS siblings, born to consanguineous parents of Turkish ancestry, whose clinical phenotype also includes protein losing enteropathy, painful relapsing chylous ascites, and hypogammaglobulinemia. We identified by whole exome and Sanger sequencing the homozygous CCBE1 C174Y mutation in both siblings. This mutation had been previously reported in another HS kindred from the Netherlands. In over-expression studies, we found increased intracellular expression of all forms (monomers, dimers, trimers) of the CCBE1 C174Y mutant protein, by Western blot, despite mutant mRNA levels similar to wild-type (WT). In addition, we detected increased secretion of the mutant CCBE1 protein by ELISA. We further found the mutant and WT proteins to be evenly distributed in the cytoplasm, by immunofluorescence and confocal microscopy. Finally, we found a strong decrease of lymphatic vessels, with a corresponding diminished expression of CCBE1, by immunohistochemistry of the patients' intestinal biopsies. In contrast, mucosal blood vessels and muscularis mucosae showed normal CCBE1 staining. Our findings show that the mutant CCBE1 C174Y protein is not loss-of-function by loss-of-expression.
胶原蛋白和含钙结合表皮生长因子结构域蛋白1(CCBE1)双等位基因突变与广泛的先天性淋巴发育异常综合征有关,包括亨内坎综合征(HS)。HS的特征为淋巴水肿、淋巴管扩张和智力残疾。CCBE1编码一种假定的细胞外基质蛋白,但尚未对导致HS的突变进行生化研究。我们报告了两名HS患者,其父母为有土耳其血统的近亲,他们的临床表型还包括蛋白丢失性肠病、疼痛性复发性乳糜腹水和低丙种球蛋白血症。我们通过全外显子组测序和桑格测序在两名患者中均鉴定出纯合的CCBE1 C174Y突变。该突变先前在来自荷兰的另一个HS家族中也有报道。在过表达研究中,我们通过蛋白质印迹法发现,尽管CCBE1 C174Y突变体mRNA水平与野生型(WT)相似,但该突变体蛋白的所有形式(单体、二聚体、三聚体)在细胞内的表达均增加。此外,我们通过酶联免疫吸附测定法检测到突变型CCBE1蛋白的分泌增加。通过免疫荧光和共聚焦显微镜检查,我们进一步发现突变体和WT蛋白在细胞质中均匀分布。最后,通过对患者肠道活检组织进行免疫组织化学检查,我们发现淋巴管明显减少,同时CCBE1的表达相应降低。相比之下,黏膜血管和黏膜肌层的CCBE1染色显示正常。我们的研究结果表明,突变型CCBE1 C174Y蛋白并非因表达缺失而功能丧失。