A non-canonical ESCRT pathway, including histidine domain phosphotyrosine phosphatase (HD-PTP), is used for down-regulation of virally ubiquitinated MHC class I

Biochem J. 2015 Oct 1;471(1):79-88. doi: 10.1042/BJ20150336. Epub 2015 Jul 28.

Abstract

The Kaposi's sarcoma-associated herpes virus (KSHV) K3 viral gene product effectively down-regulates cell surface MHC class I. K3 is an E3 ubiquitin ligase that promotes Lys(63)-linked polyubiquitination of MHC class I, providing the signal for clathrin-mediated endocytosis. Endocytosis is followed by sorting into the intralumenal vesicles (ILVs) of multivesicular bodies (MVBs) and eventual delivery to lysosomes. The sorting of MHC class I into MVBs requires many individual proteins of the four endosomal sorting complexes required for transport (ESCRTs). In HeLa cells expressing the KSHV K3 ubiquitin ligase, the effect of RNAi-mediated depletion of individual proteins of the ESCRT-0 and ESCRT-I complexes and three ESCRT-III proteins showed that these are required to down-regulate MHC class I. However, depletion of proteins of the ESCRT-II complex or of the ESCRT-III protein, VPS20 (vacuolar protein sorting 20)/CHMP6 (charged MVB protein 6), failed to prevent the loss of MHC class I from the cell surface. Depletion of histidine domain phosphotyrosine phosphatase (HD-PTP) resulted in an increase in the cell surface concentration of MHC class I in HeLa cells expressing the KSHV K3 ubiquitin ligase. Rescue experiments with wild-type (WT) and mutant HD-PTP supported the conclusion that HD-PTP acts as an alternative to ESCRT-II and VPS20/CHMP6 as a link between the ESCRT-I and those ESCRT-III protein(s) necessary for ILV formation. Thus, the down-regulation of cell surface MHC class I, polyubiquitinated by the KSHV K3 ubiquitin ligase, does not employ the canonical ESCRT pathway, but instead utilizes an alternative pathway in which HD-PTP replaces ESCRT-II and VPS20/CHMP6.

Keywords: endocytosis; endosomal sorting complex required for transport (ESCRT); histidine domain phosphotyrosine phosphatase (HD-PTP); histidine-domain protein tyrosine phosphatase non-receptor type 23 (PTPN23); lysosome; ubiquitination (ubiquitylation).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Down-Regulation*
  • Endosomal Sorting Complexes Required for Transport / genetics
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • HeLa Cells
  • Herpesvirus 8, Human / genetics
  • Herpesvirus 8, Human / metabolism*
  • Histocompatibility Antigens Class I / biosynthesis*
  • Histocompatibility Antigens Class I / genetics
  • Humans
  • Protein Tyrosine Phosphatases, Non-Receptor / genetics
  • Protein Tyrosine Phosphatases, Non-Receptor / metabolism*
  • Ubiquitination*
  • Viral Proteins / genetics
  • Viral Proteins / metabolism*

Substances

  • Endosomal Sorting Complexes Required for Transport
  • Histocompatibility Antigens Class I
  • K3 protein, Kaposi's sarcoma-associated herpesvirus
  • Viral Proteins
  • PTPN23 protein, human
  • Protein Tyrosine Phosphatases, Non-Receptor