Research ArticleNeuropharmacology
Chronic Morphine-Induced Changes in Signaling at the A3 Adenosine Receptor Contribute to Morphine-Induced Hyperalgesia, Tolerance, and Withdrawal
Timothy M. Doyle, Tally M. Largent-Milnes, Zhoumou Chen, Vasiliki Staikopoulos, Emanuela Esposito, Rebecca Dalgarno, Churmy Fan, Dilip K. Tosh, Salvatore Cuzzocrea, Kenneth A. Jacobson, Tuan Trang, Mark R. Hutchinson, Gary J. Bennett, Todd W. Vanderah and Daniela Salvemini
Journal of Pharmacology and Experimental Therapeutics August 2020, 374 (2) 331-341; DOI: https://doi.org/10.1124/jpet.120.000004
Timothy M. Doyle
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Tally M. Largent-Milnes
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Zhoumou Chen
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Vasiliki Staikopoulos
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Emanuela Esposito
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Rebecca Dalgarno
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Churmy Fan
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Dilip K. Tosh
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Salvatore Cuzzocrea
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Kenneth A. Jacobson
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Tuan Trang
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Mark R. Hutchinson
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Gary J. Bennett
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Todd W. Vanderah
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Daniela Salvemini
Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
Article Information
vol. 374 no. 2 331-341
PubMed
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History
- Received March 11, 2020
- Accepted April 27, 2020
- Published online July 19, 2020.
Article Versions
- Earlier version (May 20, 2020 - 05:46).
- You are viewing the most recent version of this article.
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Author Information
- Timothy M. Doyle,
- Tally M. Largent-Milnes,
- Zhoumou Chen,
- Vasiliki Staikopoulos,
- Emanuela Esposito,
- Rebecca Dalgarno,
- Churmy Fan,
- Dilip K. Tosh,
- Salvatore Cuzzocrea,
- Kenneth A. Jacobson,
- Tuan Trang,
- Mark R. Hutchinson,
- Gary J. Bennett,
- Todd W. Vanderah, and
- Daniela Salvemini
- Department of Pharmacology and Physiology and Henry and Amelia Nasrallah Center for Neuroscience, Saint Louis University School of Medicine, St. Louis, Missouri (T.M.D., Z.C., D.S.); Department of Pharmacology, University of Arizona College of Medicine, Tucson, Arizona (T.M.L.-M., T.W.V.); Discipline of Physiology, Institute for Photonics and Advanced Sensing, ARC Centre of Excellence for Nanoscale BioPhotonics, University of Adelaide, Adelaide, Australia (V.S., M.R.H.); Department of Clinical and Experimental Medicine and Pharmacology, University of Messina, Messina, Italy (E.E., S.C.); Departments of Comparative Biology and Experimental Medicine and Physiology and Pharmacology, Hotchkiss Brain Institute, University of Calgary, Calgary, Canada (R.D., C.F., T.T.); Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland (D.K.T., K.A.J.); and Department of Anesthesiology, University of California San Diego, La Jolla, California (G.J.B.)
- Address correspondence to:
Daniela Salvemini, St. Louis University, 1402 South Grand Blvd., St. Louis, MO 63104. E-mail: daniela.salvemini{at}health.slu.edu
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Research ArticleNeuropharmacology
A3 Adenosine Receptor and Morphine-Induced Adverse Effects
Timothy M. Doyle, Tally M. Largent-Milnes, Zhoumou Chen, Vasiliki Staikopoulos, Emanuela Esposito, Rebecca Dalgarno, Churmy Fan, Dilip K. Tosh, Salvatore Cuzzocrea, Kenneth A. Jacobson, Tuan Trang, Mark R. Hutchinson, Gary J. Bennett, Todd W. Vanderah and Daniela Salvemini
Journal of Pharmacology and Experimental Therapeutics August 1, 2020, 374 (2) 331-341; DOI: https://doi.org/10.1124/jpet.120.000004
Research ArticleNeuropharmacology
A3 Adenosine Receptor and Morphine-Induced Adverse Effects
Timothy M. Doyle, Tally M. Largent-Milnes, Zhoumou Chen, Vasiliki Staikopoulos, Emanuela Esposito, Rebecca Dalgarno, Churmy Fan, Dilip K. Tosh, Salvatore Cuzzocrea, Kenneth A. Jacobson, Tuan Trang, Mark R. Hutchinson, Gary J. Bennett, Todd W. Vanderah and Daniela Salvemini
Journal of Pharmacology and Experimental Therapeutics August 1, 2020, 374 (2) 331-341; DOI: https://doi.org/10.1124/jpet.120.000004
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