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Original Research

Protective Role of mPGES-1 (Microsomal Prostaglandin E Synthase-1)–Derived PGE2 (Prostaglandin E2) and the Endothelial EP4 (Prostaglandin E Receptor) in Vascular Responses to Injury

Huifeng Hao, Sheng Hu, Qing Wan, Chuansheng Xu, Hong Chen, Liyuan Zhu, Zhenyu Xu, Jian Meng, Richard M. Breyer, Nailin Li, De-Pei Liu, Garret A. FitzGerald, Miao Wang
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https://doi.org/10.1161/ATVBAHA.118.310713
Arteriosclerosis, Thrombosis, and Vascular Biology. 2018;ATVBAHA.118.310713
Originally published March 29, 2018
Huifeng Hao
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Sheng Hu
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Qing Wan
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Chuansheng Xu
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Hong Chen
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Liyuan Zhu
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Zhenyu Xu
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Jian Meng
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Richard M. Breyer
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Nailin Li
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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De-Pei Liu
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Garret A. FitzGerald
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Miao Wang
From the State Key Laboratory of Cardiovascular Disease (H.H., S.H., Q.W., C.X., H.C., L.Z., Z.X., J.M., M.W.) and Clinical Pharmacology Center (M.W.), Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing; Vanderbilt University, Nashville, TN (R.M.B.); Department of Medicine, Karolinska Institutet, Stockholm, Sweden (N.L.); Clinical Pharmacology, Karolinska University Hospital, Stockholm, Sweden (N.L.); Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing (D.-P.L.); and Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia (G.A.F.).
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Abstract

Objective—Deletion of mPGES-1 (microsomal prostaglandin E synthase-1)—an anti-inflammatory target alternative to COX (cyclooxygenase)-2—attenuates injury-induced neointima formation in mice. This is attributable to the augmented levels of PGI2 (prostacyclin)—a known restraint of the vascular response to injury, acting via IP (I prostanoid receptor). To examine the role of mPGES-1–derived PGE2 (prostaglandin E2) in vascular remodeling without the IP.

Approach and Results—Mice deficient in both IP and mPGES-1 (DKO [double knockout] and littermate controls [IP KO (knockout)]) were subjected to angioplasty wire injury. Compared with the deletion of IP alone, coincident deletion of IP and mPGES-1 increased neointima formation, without affecting media area. Early pathological changes include impaired reendothelialization and increased leukocyte invasion in neointima. Endothelial cells (ECs), but not vascular smooth muscle cells, isolated from DKOs exhibited impaired cell proliferation. Activation of EP (prostaglandin E receptor) 4 (and EP2, to a lesser extent), but not of EP1 or EP3, promoted EC proliferation. EP4 antagonism inhibited proliferation of mPGES-1–competent ECs, but not of mPGES-1–deficient ECs, which showed suppressed PGE2 production. EP4 activation inhibited leukocyte adhesion to ECs in vitro, promoted reendothelialization, and limited neointima formation post-injury in the mouse. Endothelium-restricted deletion of EP4 in mice suppressed reendothelialization, increased neointimal leukocytes, and exacerbated neointimal formation.

Conclusions—Removal of the IP receptors unmasks a protective role of mPGES-1–derived PGE2 in limiting injury-induced vascular hyperplasia. EP4, in the endothelial compartment, is essential to promote reendothelialization and restrain neointimal formation after injury. Activating EP4 bears therapeutic potential to prevent restenosis after percutaneous coronary intervention (Graphic Abstract).

  • dinoprostone
  • endothelium
  • mice
  • prostaglandin E synthases
  • vascular remodeling
  • Received December 8, 2017.
  • Accepted March 12, 2018.
  • © 2018 American Heart Association, Inc.

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    Protective Role of mPGES-1 (Microsomal Prostaglandin E Synthase-1)–Derived PGE2 (Prostaglandin E2) and the Endothelial EP4 (Prostaglandin E Receptor) in Vascular Responses to Injury
    Huifeng Hao, Sheng Hu, Qing Wan, Chuansheng Xu, Hong Chen, Liyuan Zhu, Zhenyu Xu, Jian Meng, Richard M. Breyer, Nailin Li, De-Pei Liu, Garret A. FitzGerald and Miao Wang
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2018;ATVBAHA.118.310713, originally published March 29, 2018
    https://doi.org/10.1161/ATVBAHA.118.310713

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    Protective Role of mPGES-1 (Microsomal Prostaglandin E Synthase-1)–Derived PGE2 (Prostaglandin E2) and the Endothelial EP4 (Prostaglandin E Receptor) in Vascular Responses to Injury
    Huifeng Hao, Sheng Hu, Qing Wan, Chuansheng Xu, Hong Chen, Liyuan Zhu, Zhenyu Xu, Jian Meng, Richard M. Breyer, Nailin Li, De-Pei Liu, Garret A. FitzGerald and Miao Wang
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2018;ATVBAHA.118.310713, originally published March 29, 2018
    https://doi.org/10.1161/ATVBAHA.118.310713
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