Biallelic variants in MAATS1 encoding CFAP91, a calmodulin-associated and spoke-associated complex protein, cause severe astheno-teratozoospermia and male infertility

J Med Genet. 2020 Oct;57(10):708-716. doi: 10.1136/jmedgenet-2019-106775. Epub 2020 Mar 11.

Abstract

Background: Multiple morphological abnormalities of the flagella (MMAF) consistently lead to male infertility due to a reduced or absent sperm motility defined as asthenozoospermia. Despite numerous genes recently described to be recurrently associated with MMAF, more than half of the cases analysed remain unresolved, suggesting that many yet uncharacterised gene defects account for this phenotype METHODS: Exome sequencing was performed on 167 infertile men with an MMAF phenotype. Immunostaining and transmission electron microscopy (TEM) in sperm cells from affected individuals were performed to characterise the ultrastructural sperm defects. Gene inactivation using RNA interference (RNAi) was subsequently performed in Trypanosoma.

Results: We identified six unrelated affected patients carrying a homozygous deleterious variants in MAATS1, a gene encoding CFAP91, a calmodulin-associated and spoke-associated complex (CSC) protein. TEM and immunostaining experiments in sperm cells showed severe central pair complex (CPC) and radial spokes defects. Moreover, we confirmed that the WDR66 protein is a physical and functional partner of CFAP91 into the CSC. Study of Trypanosoma MAATS1's orthologue (TbCFAP91) highlighted high sequence and structural analogies with the human protein and confirmed the axonemal localisation of the protein. Knockdown of TbCFAP91 using RNAi impaired flagellar movement led to CPC defects in Trypanosoma as observed in humans.

Conclusions: We showed that CFAP91 is essential for normal sperm flagellum structure and function in human and Trypanosoma and that biallelic variants in this gene lead to severe flagellum malformations resulting in astheno-teratozoospermia and primary male infertility.

Keywords: genetics; molecular genetics; reproductive medicine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abnormalities, Multiple / genetics*
  • Abnormalities, Multiple / pathology
  • Animals
  • Asthenozoospermia / genetics*
  • Asthenozoospermia / pathology
  • Axoneme / genetics
  • Axoneme / ultrastructure
  • Calcium-Binding Proteins / genetics*
  • Carrier Proteins / genetics*
  • Exome Sequencing
  • Homozygote
  • Humans
  • Infertility, Male / genetics*
  • Infertility, Male / pathology
  • Male
  • Mutation / genetics
  • Sperm Motility / genetics
  • Sperm Tail / metabolism
  • Sperm Tail / pathology
  • Sperm Tail / ultrastructure
  • Spermatozoa / pathology
  • Spermatozoa / ultrastructure
  • Trypanosoma / genetics

Substances

  • CFAP91 protein, human
  • Calcium-Binding Proteins
  • Carrier Proteins
  • WDR66 protein, human