Receptor usage of Syncytin-1: ASCT2, but not ASCT1, is a functional receptor and effector of cell fusion in the human placenta

Proc Natl Acad Sci U S A. 2024 Oct 29;121(44):e2407519121. doi: 10.1073/pnas.2407519121. Epub 2024 Oct 21.

Abstract

Syncytin-1, a human fusogenic protein of retroviral origin, is crucial for placental syncytiotrophoblast formation. To mediate cell-to-cell fusion, Syncytin-1 requires specific interaction with its cognate receptor. Two trimeric transmembrane proteins, Alanine, Serine, Cysteine Transporters 1 and 2 (ASCT1 and ASCT2), were suggested and widely accepted as Syncytin-1 cellular receptors. To quantitatively assess the individual contributions of human ASCT1 and ASCT2 to the fusogenic activity of Syncytin-1, we developed a model system where the ASCT1 and ASCT2 double knockout was rescued by ectopic expression of either ASCT1 or ASCT2. We demonstrated that ASCT2 was required for Syncytin-1 binding, cellular entry, and cell-to-cell fusion, while ASCT1 was not involved in this receptor interaction. We experimentally validated the ASCT1-ASCT2 heterotrimers as a possible explanation for the previous misidentification of ASCT1 as a receptor for Syncytin-1. This redefinition of receptor specificity is important for proper understanding of Syncytin-1 function in normal and pathological pregnancy.

Keywords: Syncytin-1; cell-to-cell fusion; endogenous retrovirus; placenta; viral receptor.

MeSH terms

  • Amino Acid Transport System ASC* / genetics
  • Amino Acid Transport System ASC* / metabolism
  • Amino Acid Transport Systems, Neutral / genetics
  • Amino Acid Transport Systems, Neutral / metabolism
  • Cell Fusion*
  • Female
  • Fusion Regulatory Protein 1, Heavy Chain
  • Gene Products, env* / genetics
  • Gene Products, env* / metabolism
  • Humans
  • Minor Histocompatibility Antigens / genetics
  • Minor Histocompatibility Antigens / metabolism
  • Placenta* / metabolism
  • Pregnancy
  • Pregnancy Proteins* / genetics
  • Pregnancy Proteins* / metabolism
  • Trophoblasts / cytology
  • Trophoblasts / metabolism

Substances

  • Amino Acid Transport System ASC
  • syncytin
  • Pregnancy Proteins
  • Gene Products, env
  • SLC1A5 protein, human
  • Amino Acid Transport Systems, Neutral
  • Minor Histocompatibility Antigens
  • SLC3A2 protein, human
  • Fusion Regulatory Protein 1, Heavy Chain