Lipophilic modification enhances anti-colitic properties of rosmarinic acid by potentiating its HIF-prolyl hydroxylases inhibitory activity

Eur J Pharmacol. 2015 Jan 15:747:114-22. doi: 10.1016/j.ejphar.2014.11.030. Epub 2014 Dec 4.

Abstract

Inhibition of hypoxia inducible factor-prolyl hydroxylase-2 (HPH), leading to activation of hypoxia inducible factor (HIF)-1 is a potential therapeutic strategy for the treatment of colitis. Rosmarinic acid (RA), an ester of caffeic acid and 3,4-dihydroxyphenyllactic acid is a naturally occurring polyphenolic compound with two catechols, a or inhibition of HPH. To improve accessibility of highly hydrophilic RA to HPH, an intracellular target, RA was chemically modified to decrease hydrophilicity. Of the less-hydrophilic derivatives, rosmarinic acid methyl ester (RAME) most potently inhibited HPH. Accordingly, RAME prevented hydroxylation of HIF-1α and consequently stabilized HIF-1α protein in cells. RAME inhibition of HPH and induction of HIF-1α were diminished by elevated doses of the required factors of HPH, 2-ketoglutarate and ascorbate. RAME induction of HIF-1α led to activation of an ulcer healing pathway, HIF-1-vascular endothelial growth factor (VEGF), in human colon carcinoma cells. RAME administered rectally ameliorated TNBS-induced rat colitis and substantially decreased the levels of pro-inflammatory mediators in the inflamed colonic tissue. In parallel with the cellular effects of RAME, RAME up-regulated HIF-1α and VEGF in the inflamed colonic tissue. Thus, lipophilic modification of RA improves its ability to inhibit HPH, leading to activation of the HIF-1-VEGF pathway. RAME, a lipophilic RA derivative, may exert anti-colitic effects via activation of the ulcer healing pathway.

Keywords: (+)-5,6-O-Isopropylidene-l-ascorbic acid; (PubChem CID: 54691418); 2-ketoglutarate (PubChem CID: 164533); Animal model; Cycloheximide (PubChem CID: 6197); Hypoxia inducible factor; Hypoxia inducible factor-prolyl hydroxylase; Lipophilic modification; MG132 (PubChem CID: 462382); Rosmarinic acid; Rosmarinic acid (PubChem CID: 5281792); Sodium ascorbate (PubChem CID: 23667548); TNBS-induced colitis; Trinitrobenzenesulfonic acid (PubChem CID : 11045).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ascorbic Acid / pharmacology
  • Carboxylic Acids / chemistry
  • Cell Line, Tumor
  • Cinnamates / chemistry*
  • Cinnamates / pharmacology*
  • Cinnamates / therapeutic use
  • Coenzymes / physiology
  • Colitis / chemically induced
  • Colitis / drug therapy*
  • Colitis / metabolism
  • Colitis / pathology
  • Depsides / chemistry*
  • Depsides / pharmacology*
  • Depsides / therapeutic use
  • Enzyme Inhibitors / chemistry*
  • Enzyme Inhibitors / pharmacology*
  • Enzyme Inhibitors / therapeutic use
  • Esters
  • Humans
  • Hydrophobic and Hydrophilic Interactions*
  • Hydroxylation / drug effects
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Hypoxia-Inducible Factor-Proline Dioxygenases / antagonists & inhibitors*
  • Hypoxia-Inducible Factor-Proline Dioxygenases / metabolism
  • Ketoglutaric Acids / pharmacology
  • Protein Stability / drug effects
  • Rats
  • Rosmarinic Acid
  • Signal Transduction / drug effects
  • Structure-Activity Relationship
  • Trinitrobenzenesulfonic Acid / adverse effects
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Carboxylic Acids
  • Cinnamates
  • Coenzymes
  • Depsides
  • Enzyme Inhibitors
  • Esters
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Ketoglutaric Acids
  • Vascular Endothelial Growth Factor A
  • Trinitrobenzenesulfonic Acid
  • Hypoxia-Inducible Factor-Proline Dioxygenases
  • Ascorbic Acid