Loss of SUN1 function in spermatocytes disrupts the attachment of telomeres to the nuclear envelope and contributes to non-obstructive azoospermia in humans

Hum Genet. 2023 Apr;142(4):531-541. doi: 10.1007/s00439-022-02515-z. Epub 2023 Mar 18.

Abstract

One of the most severe forms of infertility in humans, caused by gametogenic failure, is non-obstructive azoospermia (NOA). Approximately, 20-30% of men with NOA may have single-gene mutations or other genetic variables that cause this disease. While a range of single-gene mutations associated with infertility has been identified in prior whole-exome sequencing (WES) studies, current insight into the precise genetic etiology of impaired human gametogenesis remains limited. In this paper, we described a proband with NOA who experienced hereditary infertility. WES analyses identified a homozygous variant in the SUN1 (Sad1 and UNC84 domain containing 1) gene [c. 663C > A: p.Tyr221X] that segregated with infertility. SUN1 encodes a LINC complex component essential for telomeric attachment and chromosomal movement. Spermatocytes with the observed mutations were incapable of repairing double-strand DNA breaks or undergoing meiosis. This loss of SUN1 functionality contributes to significant reductions in KASH5 levels within impaired chromosomal telomere attachment to the inner nuclear membrane. Overall, our results identify a potential genetic driver of NOA pathogenesis and provide fresh insight into the role of the SUN1 protein as a regulator of prophase I progression in the context of human meiosis.

MeSH terms

  • Azoospermia* / pathology
  • Humans
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Microtubule-Associated Proteins / genetics
  • Nuclear Envelope* / genetics
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Spermatocytes / metabolism
  • Spermatocytes / pathology
  • Telomere / pathology

Substances

  • Microtubule-Associated Proteins
  • SUN1 protein, human
  • Membrane Proteins
  • Nuclear Proteins

Supplementary concepts

  • Azoospermia, Nonobstructive