Autotaxin inhibition reduces cardiac inflammation and mitigates adverse cardiac remodeling after myocardial infarction

J Mol Cell Cardiol. 2020 Dec:149:95-114. doi: 10.1016/j.yjmcc.2020.09.011. Epub 2020 Oct 2.

Abstract

Objective: Acute myocardial infarction (AMI) initiates pathological inflammation which aggravates tissue damage and causes heart failure. Lysophosphatidic acid (LPA), produced by autotaxin (ATX), promotes inflammation and the development of atherosclerosis. The role of ATX/LPA signaling nexus in cardiac inflammation and resulting adverse cardiac remodeling is poorly understood.

Approach and results: We assessed autotaxin activity and LPA levels in relation to cardiac and systemic inflammation in AMI patients and C57BL/6 (WT) mice. Human and murine peripheral blood and cardiac tissue samples showed elevated levels of ATX activity, LPA, and inflammatory cells following AMI and there was strong correlation between LPA levels and circulating inflammatory cells. In a gain of function model, lipid phosphate phosphatase-3 (LPP3) specific inducible knock out (Mx1-Plpp3Δ) showed higher systemic and cardiac inflammation after AMI compared to littermate controls (Mx1-Plpp3fl/fl); and a corresponding increase in bone marrow progenitor cell count and proliferation. Moreover, in Mx1- Plpp3Δ mice, cardiac functional recovery was reduced with corresponding increases in adverse cardiac remodeling and scar size (as assessed by echocardiography and Masson's Trichrome staining). To examine the effect of ATX/LPA nexus inhibition, we treated WT mice with the specific pharmacological inhibitor, PF8380, twice a day for 7 days post AMI. Inhibition of the ATX/LPA signaling nexus resulted in significant reduction in post-AMI inflammatory response, leading to favorable cardiac functional recovery, reduced scar size and enhanced angiogenesis.

Conclusion: ATX/LPA signaling nexus plays an important role in modulating inflammation after AMI and targeting this mechanism represents a novel therapeutic target for patients presenting with acute myocardial injury.

Keywords: Autotaxin; Heart failure; Inflammation; Lysophosphatidic acid; Myocardial infarction.

Publication types

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

MeSH terms

  • Animals
  • Benzoxazoles / pharmacology
  • Cell Count
  • Cell Movement / drug effects
  • Female
  • Gene Deletion
  • Humans
  • Inflammation / genetics
  • Inflammation / pathology*
  • Interferon-alpha / metabolism
  • Interferon-beta / metabolism
  • Lysophospholipids / metabolism
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Male
  • Mice, Inbred C57BL
  • Middle Aged
  • Myelopoiesis
  • Myocardial Infarction / diagnostic imaging
  • Myocardial Infarction / enzymology*
  • Myocardial Infarction / genetics
  • Myocardial Infarction / physiopathology*
  • Myocardium / enzymology*
  • Myocardium / pathology
  • Phosphatidate Phosphatase / metabolism
  • Phosphoric Diester Hydrolases / metabolism*
  • Piperazines / pharmacology
  • Recovery of Function / drug effects
  • Up-Regulation / genetics
  • Vascular Remodeling*
  • Wound Healing

Substances

  • 6-(3-(piperazin-1-yl)propanoyl)benzo(d)oxazol-2(3H)-one
  • Benzoxazoles
  • Interferon-alpha
  • Lysophospholipids
  • Piperazines
  • Interferon-beta
  • lipid phosphate phosphatase
  • Phosphatidate Phosphatase
  • Phosphoric Diester Hydrolases
  • alkylglycerophosphoethanolamine phosphodiesterase
  • lysophosphatidic acid