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Research ArticleGastrointestinal, Hepatic, Pulmonary, and Renal

Specific Activin Receptor–Like Kinase 3 Inhibitors Enhance Liver Regeneration

Daisuke Tsugawa, Yuki Oya, Ryota Masuzaki, Kevin Ray, Darren W. Engers, Martin Dib, Nhue Do, Kaori Kuramitsu, Karen Ho, Audrey Frist, Paul B. Yu, Kenneth D. Bloch, Craig W. Lindsley, Corey R. Hopkins, Charles C. Hong and Seth J. Karp
Journal of Pharmacology and Experimental Therapeutics December 2014, 351 (3) 549-558; DOI: https://doi.org/10.1124/jpet.114.216903
Daisuke Tsugawa
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Yuki Oya
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Ryota Masuzaki
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Kevin Ray
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Darren W. Engers
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Martin Dib
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Nhue Do
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Kaori Kuramitsu
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Karen Ho
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Audrey Frist
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Paul B. Yu
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Kenneth D. Bloch
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Craig W. Lindsley
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Corey R. Hopkins
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Charles C. Hong
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Seth J. Karp
The Transplant Center and Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee (D.T., Y.O., R.M., K.R., S.J.K.); Department of Pharmacology, Vanderbilt Center for Neuroscience Drug Discovery, Nashville, Tennessee (D.W.E., C.W.L., C.R.H.); Department of Surgery, Beth Israel Deaconess Medical Center, Boston, Massachusetts (M.D., N.D.); Department of Surgery, Kobe University, Kobe, Japan (K.K.); Department of Surgery (K.H.), and Division of Cardiology, Department of Medicine (P.B.Y.), Brigham and Women’s Hospital, Boston, Massachusetts; Anesthesia Center for Critical Care Research, Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts (K.D.B.); Department of Chemistry, Vanderbilt University, Nashville, Tennessee (C.W.L.); and Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, Tennessee (A.F., C.C.H.)
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Abstract

Pharmacologic agents to enhance liver regeneration after injury would have wide therapeutic application. Based on previous work suggesting inhibition of bone morphogenetic protein (BMP) signaling stimulates liver regeneration, we tested known and novel BMP inhibitors for their ability to accelerate regeneration in a partial hepatectomy (PH) model. Compounds were produced based on the 3,6-disubstituted pyrazolo[1,5-a] pyrimidine core of the BMP antagonist dorsomorphin and evaluated for their ability to inhibit BMP signaling and enhance liver regeneration. Antagonists of the BMP receptor activin receptor–like kinase 3 (ALK3), including LDN-193189 (LDN; 4-[6-[4-(1-piperazinyl)phenyl]pyrazolo[1,5-a]pyrimidin-3-yl]-quinoline), DMH2 (4-(2-(4-(3-(quinolin-4-yl)pyrazolo[1,5-a]pyrimidin-6-yl)phenoxy)ethyl)morpholine; VU0364849), and the novel compound VU0465350 (7-(4-isopropoxyphenyl)-3-(1H-pyrazol-4-yl)imidazo[1,2-a]pyridine; VU5350), blocked SMAD phosphorylation in vitro and in vivo, and enhanced liver regeneration after PH. In contrast, an antagonist of the BMP receptor ALK2, VU0469381 (5-(6-(4-methoxyphenyl)pyrazolo[1,5-a]pyrimidin-3-yl)quinolone; 1LWY), did not affect liver regeneration. LDN did not affect liver synthetic or metabolic function. Mechanistically, LDN increased serum interleukin-6 levels and signal transducer and activator of transcription 3 phosphorylation in the liver, and modulated other factors known to be important for liver regeneration, including suppressor of cytokine signaling 3 and p53. These findings suggest that inhibition of ALK3 may be part of a therapeutic strategy for treating human liver disease.

Footnotes

    • Received May 27, 2014.
    • Accepted September 25, 2014.
  • This work was supported by the National Institutes of Health National Institute of Diabetes and Digestive and Kidney Diseases [Grants 7R01-DK081387 and R01-DK0829710]; Vanderbilt University Medical Center; and the Foundation LeDucq.

  • Kenneth D. Bloch died during the preparation of this manuscript.

  • dx.doi.org/10.1124/jpet.114.216903.

  • Copyright © 2014 by The American Society for Pharmacology and Experimental Therapeutics
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Journal of Pharmacology and Experimental Therapeutics: 351 (3)
Journal of Pharmacology and Experimental Therapeutics
Vol. 351, Issue 3
1 Dec 2014
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Research ArticleGastrointestinal, Hepatic, Pulmonary, and Renal

ALK3 in Liver Regeneration

Daisuke Tsugawa, Yuki Oya, Ryota Masuzaki, Kevin Ray, Darren W. Engers, Martin Dib, Nhue Do, Kaori Kuramitsu, Karen Ho, Audrey Frist, Paul B. Yu, Kenneth D. Bloch, Craig W. Lindsley, Corey R. Hopkins, Charles C. Hong and Seth J. Karp
Journal of Pharmacology and Experimental Therapeutics December 1, 2014, 351 (3) 549-558; DOI: https://doi.org/10.1124/jpet.114.216903

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Research ArticleGastrointestinal, Hepatic, Pulmonary, and Renal

ALK3 in Liver Regeneration

Daisuke Tsugawa, Yuki Oya, Ryota Masuzaki, Kevin Ray, Darren W. Engers, Martin Dib, Nhue Do, Kaori Kuramitsu, Karen Ho, Audrey Frist, Paul B. Yu, Kenneth D. Bloch, Craig W. Lindsley, Corey R. Hopkins, Charles C. Hong and Seth J. Karp
Journal of Pharmacology and Experimental Therapeutics December 1, 2014, 351 (3) 549-558; DOI: https://doi.org/10.1124/jpet.114.216903
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