Novel bi-allelic variants in DNAH2 cause severe asthenoteratozoospermia with multiple morphological abnormalities of the flagella

Reprod Biomed Online. 2021 May;42(5):963-972. doi: 10.1016/j.rbmo.2021.01.011. Epub 2021 Jan 22.

Abstract

Research question: Multiple morphological abnormalities of the flagella (MMAF) is characterized by excessive immotile spermatozoa with severe flagellar abnormalities in the ejaculate. Previous studies have reported a heterogeneous genetic profile associated with MMAF. What other genetic variants might explain the cause of MMAF?

Design: Whole-exome sequencing was conducted in a cohort of 90 Chinese patients with MMAF. The pathogenicity of identified mutations was assessed through electron microscopy and immunofluorescent examinations.

Results: Three unrelated men with bi-allelic DNAH2 variants were identified. Sanger sequencing verified that the six novel variants originated from every parent. All these variants were located at the conserved domains of DNAH2 and predicted to be deleterious by bioinformatic tools. Haematoxylin and eosin staining and scanning electron microscopy revealed that spermatozoa harbouring DNAH2 variants displayed severely aberrant morphology mainly with absent and short flagella (≥78%). Moreover, transmission electron microscopy revealed the obvious absence of a central pair of microtubules and inner dynein arms in the spermatozoa with mutated DNAH2. Immunofluorescence data further validated these findings, showing reduced DNAH2 protein expression in the spermatozoa with DNAH2 variants, compared with normal spermatozoa. Intracytoplasmic sperm injection using spermatozoa from the three men with mutated DNAH2 resulted in blastocyst formation in all cases. Embryo transfer was carried out in two couples, both resulting in clinical pregnancy.

Conclusions: These experimental and clinical data suggest that bi-allelic DNAH2 variants might induce MMAF-associated asthenoteratozoospermia, which can be overcome through intracytoplasmic sperm injection. These findings contribute to the knowledge of the genetic landscape of asthenoteratozoospermia and clinical counselling of male infertility.

Keywords: Asthenoteratozoospermia; Axonemal dyneins; DNAH2; Flagella; MMAF.

MeSH terms

  • Adult
  • Asthenozoospermia / genetics*
  • Asthenozoospermia / pathology
  • Axonemal Dyneins / genetics*
  • Case-Control Studies
  • Exome Sequencing
  • Female
  • Humans
  • Male
  • Pregnancy
  • Sperm Injections, Intracytoplasmic
  • Sperm Tail / ultrastructure

Substances

  • DNAH2 protein, human
  • Axonemal Dyneins