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Research ArticleDrug Discovery and Translational Medicine

Parallel Buprenorphine phMRI Responses in Conscious Rodents and Healthy Human Subjects

Lino Becerra, Jaymin Upadhyay, Pei-Ching Chang, James Bishop, Julie Anderson, Richard Baumgartner, Adam J. Schwarz, Alexandre Coimbra, Diana Wallin, Lauren Nutile, Edward George, Gary Maier, Soujanya Sunkaraneni, Smriti Iyengar, Jeffrey L. Evelhoch, David Bleakman, Richard Hargreaves and David Borsook
Journal of Pharmacology and Experimental Therapeutics April 2013, 345 (1) 41-51; DOI: https://doi.org/10.1124/jpet.112.201145
Lino Becerra
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Jaymin Upadhyay
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Pei-Ching Chang
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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James Bishop
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Julie Anderson
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Richard Baumgartner
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Adam J. Schwarz
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Alexandre Coimbra
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Diana Wallin
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Lauren Nutile
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Edward George
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Gary Maier
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Soujanya Sunkaraneni
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Smriti Iyengar
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Jeffrey L. Evelhoch
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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David Bleakman
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Richard Hargreaves
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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David Borsook
Imaging Consortium for Drug Development (L.B., J.U., P.-C.C., J.B., J.A., R.B., A.J.S., A.C., D.W., L.N., E.G., G.M., S.S., S.I., J.L.E., D.B., R.H., D.B.), P.A.I.N. Group, Children’s Hospital of Boston, Waltham, Massachusetts (L.B., J.U., P.-C.C., J.B., J.A., D.W., L.N., E.G., D.B.); Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts (L.B., D.B.); Merck Research Laboratories, Merck and Company, West Point, Pennsylvania (R.B., A.C., J.L.E., R.H.); Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana (A.J.S., S.I., D.B.); and Sunovion Inc., Marlborough, Massachusetts (S.S., G.M.)
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Abstract

Pharmacological magnetic resonance imaging (phMRI) is one method by which a drug’s pharmacodynamic effects in the brain can be assessed. Although phMRI has been frequently used in preclinical and clinical settings, the extent to which a phMRI signature for a compound translates between rodents and humans has not been systematically examined. In the current investigation, we aimed to build on recent clinical work in which the functional response to 0.1 and 0.2 mg/70 kg i.v. buprenorphine (partial µ-opioid receptor agonist) was measured in healthy humans. Here, we measured the phMRI response to 0.04 and 0.1 mg/kg i.v. buprenorphine in conscious, naive rats to establish the parallelism of the phMRI signature of buprenorphine across species. PhMRI of 0.04 and 0.1 mg/kg i.v. buprenorphine yielded dose-dependent activation in a brain network composed of the somatosensory cortex, cingulate, insula, striatum, thalamus, periaqueductal gray, and cerebellum. Similar dose-dependent phMRI activation was observed in the human phMRI studies. These observations indicate an overall preservation of pharmacodynamic responses to buprenorphine between conscious, naive rodents and healthy human subjects, particularly in brain regions implicated in pain and analgesia. This investigation further demonstrates the usefulness of phMRI as a translational tool in neuroscience research that can provide mechanistic insight and guide dose selection in drug development.

Footnotes

    • Received October 24, 2012.
    • Accepted January 30, 2013.
  • L.B. and J.U. contributed equally to this work.

  • This work was supported by the Imaging Consortium for Drug Development (to D.B. and L.B.).

  • dx.doi.org/10.1124/jpet.112.201145.

  • ↵Embedded ImageThis article has supplemental material available at jpet.aspetjournals.org.

  • Copyright © 2013 by The American Society for Pharmacology and Experimental Therapeutics
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Journal of Pharmacology and Experimental Therapeutics: 345 (1)
Journal of Pharmacology and Experimental Therapeutics
Vol. 345, Issue 1
1 Apr 2013
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Research ArticleDrug Discovery and Translational Medicine

Translation of the Buprenorphine PhMRI Response

Lino Becerra, Jaymin Upadhyay, Pei-Ching Chang, James Bishop, Julie Anderson, Richard Baumgartner, Adam J. Schwarz, Alexandre Coimbra, Diana Wallin, Lauren Nutile, Edward George, Gary Maier, Soujanya Sunkaraneni, Smriti Iyengar, Jeffrey L. Evelhoch, David Bleakman, Richard Hargreaves and David Borsook
Journal of Pharmacology and Experimental Therapeutics April 1, 2013, 345 (1) 41-51; DOI: https://doi.org/10.1124/jpet.112.201145

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Research ArticleDrug Discovery and Translational Medicine

Translation of the Buprenorphine PhMRI Response

Lino Becerra, Jaymin Upadhyay, Pei-Ching Chang, James Bishop, Julie Anderson, Richard Baumgartner, Adam J. Schwarz, Alexandre Coimbra, Diana Wallin, Lauren Nutile, Edward George, Gary Maier, Soujanya Sunkaraneni, Smriti Iyengar, Jeffrey L. Evelhoch, David Bleakman, Richard Hargreaves and David Borsook
Journal of Pharmacology and Experimental Therapeutics April 1, 2013, 345 (1) 41-51; DOI: https://doi.org/10.1124/jpet.112.201145
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