ITPK1 mediates the lipid-independent synthesis of inositol phosphates controlled by metabolism

Proc Natl Acad Sci U S A. 2019 Dec 3;116(49):24551-24561. doi: 10.1073/pnas.1911431116. Epub 2019 Nov 21.

Abstract

Inositol phosphates (IPs) comprise a network of phosphorylated molecules that play multiple signaling roles in eukaryotes. IPs synthesis is believed to originate with IP3 generated from PIP2 by phospholipase C (PLC). Here, we report that in mammalian cells PLC-generated IPs are rapidly recycled to inositol, and uncover the enzymology behind an alternative "soluble" route to synthesis of IPs. Inositol tetrakisphosphate 1-kinase 1 (ITPK1)-found in Asgard archaea, social amoeba, plants, and animals-phosphorylates I(3)P1 originating from glucose-6-phosphate, and I(1)P1 generated from sphingolipids, to enable synthesis of IP6 We also found using PAGE mass assay that metabolic blockage by phosphate starvation surprisingly increased IP6 levels in a ITPK1-dependent manner, establishing a route to IP6 controlled by cellular metabolic status, that is not detectable by traditional [3H]-inositol labeling. The presence of ITPK1 in archaeal clades thought to define eukaryogenesis indicates that IPs had functional roles before the appearance of the eukaryote.

Keywords: glucose; inositol phosphate; metabolism; phosphate; phospholipase C.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Archaeal Proteins / metabolism
  • Conserved Sequence
  • HCT116 Cells
  • Humans
  • Hydrolysis
  • Inositol / metabolism
  • Inositol Phosphates / biosynthesis*
  • Inositol Phosphates / metabolism
  • Phosphorylation
  • Phosphotransferases (Alcohol Group Acceptor) / chemistry
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism*
  • Saccharomyces cerevisiae / metabolism
  • Sphingolipids / metabolism
  • Type C Phospholipases / metabolism

Substances

  • Archaeal Proteins
  • Inositol Phosphates
  • Sphingolipids
  • Inositol
  • Phosphotransferases (Alcohol Group Acceptor)
  • inositol-tetrakisphosphate 1-kinase
  • ITPK1 protein, human
  • Type C Phospholipases