A novel mechanism underlying phytate-mediated biological action-phytate hydrolysates induce intracellular calcium signaling by a Gαq protein-coupled receptor and phospholipase C-dependent mechanism in colorectal cancer cells

Mol Nutr Food Res. 2010 Jul;54(7):947-55. doi: 10.1002/mnfr.200900279.

Abstract

Phytate (inositol hexa-phosphate, IP6) possesses multiple biological functions including anticancer activity. IP6 is converted to inositol di-, tri-, and tetra-phosphates (IP2, IP3, and IP4) by phytase in large intestinal microbes; however, their contribution to the IP6-mediated functions has not been investigated. We have developed the preparations of IP2-4 and IP3-rich phytate hydrolysate (IP3-RPH) by IP6 digestion using microbial phytase, and examined the induction of intracellular Ca(2+) signaling in response to the preparations in colorectal cancer cells. IP2-4, but not inositol (IP0) and IP6, induced increases in intracellular Ca(2+) concentration ([Ca(2+)](i)) in Caco-2 cells with the following rank order: IP3>IP2=IP4. Inositol tri-phosphate (IP3)-RPH induced increases in [Ca(2+)](i) in both undifferentiated Caco-2 and HT-29 cells, but not in differentiated Caco-2. The IP3-RPH-induced [Ca(2+)](i) increase was resistant to extracellular Ca(2+) depletion, however, it was impaired by inhibitors of phospholipase C, inositol 1, 4, 5 tri-phosphate receptor, ryanodine receptor, and Galphaq protein. These results show that the putative G protein-coupled receptor on the plasma membrane senses the IP6 hydrolysates and activates phospholipase Cbeta, resulting in Ca(2+) mobilization through Ca(2+) channels coupled with the inositol 1, 4, 5 tri-phosphate and ryanodine receptors on the sarco-endoplasmic reticulum Ca(2+) store in colorectal cancer cells.

Publication types

  • Comparative Study

MeSH terms

  • Animals
  • Antineoplastic Agents, Phytogenic / metabolism
  • Antineoplastic Agents, Phytogenic / pharmacology*
  • Caco-2 Cells
  • Calcium Channel Blockers / pharmacology
  • Calcium Signaling / drug effects*
  • Cell Dedifferentiation
  • Cell Line
  • Colorectal Neoplasms / drug therapy*
  • Enzyme Inhibitors / pharmacology
  • GTP-Binding Protein alpha Subunits, Gq-G11 / antagonists & inhibitors
  • GTP-Binding Protein alpha Subunits, Gq-G11 / metabolism*
  • HT29 Cells
  • Humans
  • Inositol 1,4,5-Trisphosphate Receptors / antagonists & inhibitors
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism
  • Inositol Phosphates / metabolism
  • Inositol Phosphates / pharmacology*
  • Osmolar Concentration
  • Phospholipase C beta / antagonists & inhibitors
  • Phospholipase C beta / metabolism
  • Phytic Acid / metabolism
  • Phytic Acid / pharmacology
  • Phytic Acid / physiology*
  • Rats
  • Ryanodine Receptor Calcium Release Channel / metabolism
  • Type C Phospholipases / antagonists & inhibitors
  • Type C Phospholipases / metabolism*

Substances

  • Antineoplastic Agents, Phytogenic
  • Calcium Channel Blockers
  • Enzyme Inhibitors
  • Inositol 1,4,5-Trisphosphate Receptors
  • Inositol Phosphates
  • Ryanodine Receptor Calcium Release Channel
  • Phytic Acid
  • Type C Phospholipases
  • Phospholipase C beta
  • GTP-Binding Protein alpha Subunits, Gq-G11