Cap-binding protein (eukaryotic initiation factor 4E) and 4E-inactivating protein BP-1 independently regulate cap-dependent translation

Mol Cell Biol. 1996 Oct;16(10):5450-7. doi: 10.1128/MCB.16.10.5450.

Abstract

Cap-dependent protein synthesis in animal cells is inhibited by heat shock, serum deprivation, metaphase arrest, and infection with certain viruses such as adenovirus (Ad). At a mechanistic level, translation of capped mRNAs is inhibited by dephosphorylation of eukaryotic initiation factor 4E (eIF-4E) (cap-binding protein) and its physical sequestration with the translation repressor protein BP-1 (PHAS-I). Dephosphorylation of BP-I blocks cap-dependent translation by promoting sequestration of eIF-4E. Here we show that heat shock inhibits translation of capped mRNAs by simultaneously inducing dephosphorylation of eIF-4E and BP-1, suggesting that cells might coordinately regulate translation of capped mRNAs by impairing both the activity and the availability of eIF-4E. Like heat shock, late Ad infection is shown to induce dephosphorylation of eIF-4E. However, in contrast to heat shock, Ad also induces phosphorylation of BP-1 and release of eIF-4E. BP-1 and eIF-4E can therefore act on cap-dependent translation in either a mutually antagonistic or cooperative manner. Three sets of experiments further underscore this point: (i) rapamycin is shown to block phosphorylation of BP-1 without inhibiting dephosphorylation of eIF-4E induced by heat shock or Ad infection, (ii) eIF-4E is efficiently dephosphorylated during heat shock or Ad infection regardless of whether it is in a complex with BP-1, and (iii) BP-1 is associated with eIF-4E in vivo regardless of the state of eIF-4E phosphorylation. These and other studies establish that inhibition of cap-dependent translation does not obligatorily involve sequestration of eIF-4E by BP-1. Rather, translation is independently regulated by the phosphorylation states of eIF-4E and the 4E-binding protein, BP-1. In addition, these results demonstrate that BP-1 and eIF-4E can act either in concert or in opposition to independently regulate cap-dependent translation. We suggest that independent regulation of eIF-4E and BP-1 might finely regulate the efficiency of translation initiation or possibly control cap-dependent translation for fundamentally different purposes.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Adenoviruses, Human*
  • Animals
  • CHO Cells
  • Carrier Proteins*
  • Cell Cycle Proteins
  • Cell Line, Transformed
  • Cell Transformation, Viral
  • Cricetinae
  • Eukaryotic Initiation Factor-4E
  • Gene Expression Regulation
  • Hot Temperature
  • Humans
  • Insulin / pharmacology
  • Kidney
  • Peptide Initiation Factors / isolation & purification
  • Peptide Initiation Factors / metabolism*
  • Phosphoproteins / isolation & purification
  • Phosphoproteins / metabolism*
  • Phosphorylation
  • Polyenes / pharmacology
  • Protein Biosynthesis*
  • RNA Caps / metabolism*
  • RNA, Messenger / metabolism
  • Repressor Proteins / metabolism
  • Sirolimus
  • beta-Galactosidase / biosynthesis

Substances

  • Adaptor Proteins, Signal Transducing
  • Carrier Proteins
  • Cell Cycle Proteins
  • EIF4EBP1 protein, human
  • Eukaryotic Initiation Factor-4E
  • Insulin
  • Peptide Initiation Factors
  • Phosphoproteins
  • Polyenes
  • RNA Caps
  • RNA, Messenger
  • Repressor Proteins
  • beta-Galactosidase
  • Sirolimus