Disruption of Spermatogenesis and Infertility in Ataxia with Oculomotor Apraxia Type 2 (AOA2)

Cerebellum. 2019 Jun;18(3):448-456. doi: 10.1007/s12311-019-01012-w.

Abstract

Ataxia with oculomotor apraxia type 2 (AOA2) is a rare autosomal recessive cerebellar ataxia characterized by onset between 10 and 20 years of age and a range of neurological features that include progressive cerebellar atrophy, axonal sensorimotor neuropathy, oculomotor apraxia in a majority of patients, and elevated serum alpha-fetoprotein (AFP). AOA2 is caused by mutation of the SETX gene which encodes senataxin, a DNA/RNA helicase involved in transcription regulation, RNA processing, and DNA maintenance. Disruption of senataxin in rodents led to defective spermatogenesis and sterility in males uncovering a key role for senataxin in male germ cell survival. Here, we report the first clinical and cellular evidence of impaired spermatogenesis in AOA2 patients. We assessed sperm production in three AOA2 patients and testicular pathology in one patient and compared the findings to those of Setx-knockout mice. Sperm production was impaired in all patients assessed (3/3, 100%). Analyses of testicular biopsies from an AOA2 patient recapitulate features of the histology seen in Setx-knockout mice, strongly suggesting an underlying mechanism centering on DNA-damage-mediated germ cell apoptosis. These findings support a role for senataxin in human reproductive function and highlight a novel clinical feature of AOA2 that extends the extra-neurological roles of senataxin. This raises an important reproductive counseling issue for clinicians, and fertility specialists should be aware of SETX mutations as a possible diagnosis in young male patients presenting with oligospermia or azoospermia since infertility may presage the later onset of neurological manifestations in some individuals.

Keywords: Cerebellum; Fertility; Gait disorders/ataxia; Genetics; Sperm.

Publication types

  • Case Reports

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • DNA Helicases
  • Humans
  • Infertility / genetics*
  • Infertility / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Multifunctional Enzymes
  • Mutation
  • RNA Helicases / genetics
  • Spermatogenesis / genetics*
  • Spinocerebellar Ataxias / complications
  • Spinocerebellar Ataxias / congenital*
  • Spinocerebellar Ataxias / genetics

Substances

  • Multifunctional Enzymes
  • SETX protein, human
  • DNA Helicases
  • RNA Helicases

Supplementary concepts

  • Spinocerebellar ataxia, autosomal recessive 1