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Molecular Imaging Branch

Recent Publications (2012-2017)

2012

J. Hirvonen, W.C. Kreisl, M. Fujita, I. Dustin, S. Miranda, Y. Zhang, C. Morse, V.W. Pike, R.B. Innis, and W.H. Theodore. Increased in vivo expression of an inflammatory marker in temporal lobe epilepsy. J. Nucl. Med. 53: 234-240, 2012.

T.G. Lohith, S.S. Zoghbi, C.L. Morse, M.F. Araneta, V.N. Barth, N.A. Goebl, J.A. Tauscher, V.W. Pike, R.B. Innis, and M. Fujita. Brain and whole-body imaging of nociceptin/orphanin FQ peptide (NOP) receptors in humans using a novel PET ligand 11C-NOP-1A. J. Nucl. Med. 53: 385-392, 2012.

Y. Kimura, F.G. Simeon, S.S. Zoghbi, Y. Zhang, J. Hatazawa, V.W. Pike, R.B. Innis, and M. Fujita. Quantification of metabotropic glutamate subtype 5 receptors in brain by an equilibrium method using 18F-SP203. NeuroImage. 59: 2124–2130, 2012.

S.S. Zoghbi, K.B. Anderson, K.J. Jenko, D.A. Luckenbaugh, R.B. Innis, and V.W. Pike. On quantitative relationships between PET radiotracer lipophilicity and plasma free fraction in monkey and human. J. Pharmaceutical Sci. 101: 1028-1039, 2012.

X. Bao, S. Lu, J.-S. Liow, S.S. Zoghbi, K.J. Jenko, D.T. Clark, C.L. Morse, R.L. Gladding, R.B. Innis, and V.W. Pike. Radiosynthesis and evaluation of an 18F-labeled non-imidazole 2-aminoethylbenzofuran-based histamine receptor subtype-3 PET radioligand. J. Med. Chem. 55: 2406 – 2415, 2012.

P. Zanotti Fregonara and R.B. Innis. Suggested pathway to assess radiation safety of 11C-labeled PET tracers for first-in-human studies. Eur. J. Nucl. Med. Mol. Biol. 39: 396-398, 2012.

S. Li, Y. Zhang, M. Ferraris Araneta, Y. Xiang, C. Johnson, R. B. Innis, and J. Shen. In vivo detection of 13C isotopomer turnover in the human brain by sequential infusion of 13C labeled substrates. J. Magnetic Resonance. 218: 16-21, 2012.

X. Bao, S. Lu, J.-S. Liow, C.L. Morse, K.B. Anderson, S.S. Zoghbi, R.B. Innis, and V.W. Pike. [11C]Rhodamine-123: synthesis and biodistribution in rodents. Nucl. Med. Biol. 39: 1128-1136, 2012.

P. Zanotti-Fregonara, J.-S. Liow, C. Comtat, S.S. Zoghbi, Y. Zhang, V.W. Pike, M. Fujita, and R.B. Innis. Image-derived input function in PET brain studies: blood-based methods are resistant to motion artifacts. Nucl. Med. Comm. 33(9): 982-989, 2012.

M. Fujita, C.S. Hines, S.S. Zoghbi, A.G. Mallinger, L.P. Dickstein, J.-S. Liow, Y. Zhang, V.W. Pike, W.C. Drevets, R.B. Innis, and C.A. Zarate Jr. Downregulation of brain phosphodiesterase type IV measured with 11C-(R)-rolipram positron emission tomography in major depressive disorder. Biol. Psych. 72: 548-554, 2012.

J. Tam, R. Cinar, J. Liu, G. Godlewski, D. Wesley, T. Jourdan, G. Szanda, B. Mukhopadhyay, L. Chedester, J.-S. Liow, R.B. Innis, K. Cheng, K.C. Rice, J.R. Deschamps, R.J. Chorvat, J.F. McElroy, and G. Kunos. Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metabolism 16: 167-179, 2012.

P. Zanotti-Fregonara, C.S. Hines, S.S. Zoghbi, J.-S. Liow, Y. Zhang, V.W. Pike, W.C. Drevets, A.G. Mallinger, C.A. Zarate Jr., M. Fujita, and R.B. Innis. Population-based input function and image-derived input function for [11C](R)-rolipram PET imaging: methodology, validation and application to the study of major depressive disorder. NeuroImage. 63: 1532-1541, 2012.

F.G. Simeon, J.-S. Liow, Y. Zhang, J. Hong, R.L. Gladding, S.S. Zoghbi, R.B. Innis, and V.W. Pike. Synthesis and characterization in monkey of [11C]SP203 as a radioligand for imaging brain metabotropic glutamate 5 receptors. Eur. J. Nucl. Med. Mol. Imaging. 39: 1949-1958, 2012.

K.J. Jenko, J. Hirvonen, I.D. Henter, K.B. Anderson, S.S. Zoghbi, T.M. Hyde, A. Deep-Soboslay, R.B. Innis, and J.E. Kleinman. Binding of a tritiated inverse agonist to cannabinoid CB1 receptors is increased in patients with schizophrenia. Schizophrenia Research. 141: 185-188, 2012.

2013

J. Hirvonen, P. Zanotti Fregonara, J.C. Umhau, D.T. George, D. Rallis-Frutos, C.H. Lyoo, C.-T. Li, C.S. Hines, H. Sun, G.E. Terry, C. Morse, S.S. Zoghbi, V.W. Pike, R.B. Innis, and M. Heilig. Reduced cannabinoid CB1 receptor binding in alcohol dependence measured with positron emission tomography. Mol. Psychiatry 18: 916-921, 2013.

W.C. Kreisl, K.J. Jenko, C.S. Hines, C.H. Lyoo, W. Corona, C.L. Morse, S.S. Zoghbi, T. Hyde, J.E. Kleinman, V.W. Pike, F.J. McMahon, and R.B. Innis. A genetic polymorphism for translocator protein 18 kDa affects both in vitro and in vivo radioligand binding in human brain to this putative biomarker of neuroinflammation. J. Cereb. Blood Flow Metab. 33: 53-58, 2013.

P. Zanotti-Fregonara, V. Barth, J.-S. Liow, S.S. Zoghbi, D. Clark, E. Rhoads, E. Siuda, B.A. Heinz, E. Nisenbaum, B. Dressman, E. Joshi, D. Luffer-Atlas, M.J. Fisher, J. Master, N. Goebl, S. Kuklish, C. Morse, J. Tauscher, V.W. Pike, and R.B. Innis. Evaluation in vitro and in animals of a new 11C-labeled PET radioligand for the metabotropic glutamate receptor 1 in brain. Eur. J. Nucl. Med. Mol. Imaging. 40: 245-253, 2013.

C.S. Hines, M. Fujita, S.S. Zoghbi, J.S. Kim, Z. Quezado, N. Miao, M.D. Ferraris Araneta, C. Morse, P. Herscovitch, V.W. Pike, J. Labovsky, and R.B. Innis. Propofol decreases in vivo binding of [11C]PBR28 to translocator protein (18kDa) in the human brain. J. Nucl. Med. 54: 64-69, 2013.

T.G. Lohith, E.K. Osterweil, M. Fujita, K.J. Jenko, M.F. Bear, and R.B. Innis. Is metabotropic glutamate receptor 5 upregulated in prefrontal cortex in fragile X syndrome? Molecular Autism. 4:15, 2013.

P. Kannan, V.W. Pike, C. Halldin, O. Langer, M.M. Gottesman, R.B. Innis, and M.D. Hall. Factors that limit positron emission tomography imaging of P-glycoprotein density at the blood-brain barrier. Mol. Pharmaceutics. 10: 2222-2229, 2013.

P. Zanotti-Fregonara, J. Hirvonen, C.H. Lyoo, S.S. Zoghbi, D. Rallis-Frutos, M.A. Huestis, C. Morse, V.W. Pike, and R.B. Innis. Population-based input function modeling for [18F]FMPEP-d2, an inverse agonist radioligand for cannabinoid CB1 receptors: validation in clinical studies. PLOS ONE, 8(4): 360231. Doi:10.1371/journal.pone.0060231, 2013.

W.C. Kreisl, C.H. Lyoo, M. McGwier, J. Snow, K.J. Jenko, N. Kimura, W. Corona, C.L. Morse, S.S. Zoghbi, V.W. Pike, F.J. McMahon, R.S. Turner, R.B. Innis, and the Biomarkers Consortium PET Radioligand Project Team. In vivo radioligand binding to translocator protein correlates with severity of Alzheimer’s disease. Brain, 136: 2228-2238, 2013.

W.M. Bosker, E.L. Karschner, D. Lee, R.S. Goodwin, J. Hirvonen, R.B. Innis, E.L. Theunissen, K.P.C. Kuypers, M.A. Huestis, and J.G. Ramaekers. Psychomotor function in chronic daily cannabis smokers during sustained abstinence. PLOS ONE, 8(1): e53127, 2013.

P. Zanotti-Fregonara, V.N. Barth, S.S. Zoghbi, J.-S. Liow, E. Nisenbaum, E.Siuda, R.L. Gladding, D. Rallis-Frutos, C. Morse, J. Tauscher, V.W. Pike, and R.B. Innis. 11C-LY2428703, a positron emission tomographic radioligand for the metabotropic glutamate receptor 1, is unsuitable for imaging in monkey and human brain. Eur. J. Nucl. Med. Mol. Imaging Res. 3:47, 2013.

P. Zanotti-Fregonara, A.A. Lammertsma, and R.B. Innis. Suggested pathway to assess radiation safety of 18F-labeled PET tracers for first-in-human studies. Eur. J. Nucl. Med. Mol. Imaging. 40: 1781-1783, 2013.

M. Fujita, S. Mahanty, S.S. Zoghbi, M.D.F. Araneta, J. Hong, V.W. Pike, R.B. Innis, and T.E. Nash. PET reveals inflammation around calcified taenia solium granulomas with perilesional edema. PLOS ONE, 8(9): e74052, 2013.

R. Xu, P. Zanotti-Fregonara, S.S. Zoghbi, R.L. Gladding, A.E. Woock, R.B. Innis and V.W. Pike. Synthesis and evaluation in monkey of [18F]4-Fluoro-N-methyl-N-(4-(6-(methylamino)pyrimidin-4-yl)thiazol-2-yl)benzamide ([18F]FIMX): a promising radioligand for PET imaging of brain metabotropic glutamate receptor 1 (mGluR1). J Med. Chem. 56: 9146-9155, 2013.

2014

S. Shrestha, E.E. Nelson, J.-S. Liow, R. Gladding, C.H. Lyoo, P.L. Noble, C. Morse, I.D. Henter, J. Kruger, B. Zhang, S.J. Suomi, P. Svenningsson, V.W. Pike, J.T. Winslow, E. Leibenluft, D.S. Pine, and R.B Innis. Fluoxetine administered to juvenile monkeys: effects on the serotonin transporter and behavior. Am. J. Psychiatry. 171: 323-331, 2014.

S. Shrestha, J.-S. Liow, S. Lu, K. Jenko, R.L. Gladding, P. Svenningsson, C.L. Morse, S.S. Zoghbi, V.W. Pike, and R.B. Innis. [11C]CUMI-101, a positron emission tomographic radioligand, behaves as a serotonin 1A receptor antagonist and also binds to α1-adrenoceptors in brain. J. Nucl. Med. 55: 141-146, 2014.

T.G. Lohith, S.S. Zoghbi, C.L. Morse, M.F. Araneta, V.N. Barth, N.A. Goebl, J.A. Tauscher, V.W. Pike, R.B. Innis, and M. Fujita. Retest imaging of [11C]NOP-1A binding to nociceptin/orphanin FQ peptide (NOP) receptors in the brain of healthy humans. NeuroImage 87: 89-95, 2014.

T. Tsujikawa, S.S. Zoghbi, J. Hong, S.R. Donohue, K.J. Jenko, Robert L. Gladding, C. Halldin, V.W. Pike, R.B. Innis and M. Fujita. In vitro and in vivo evaluation of 11C-SD5024, a novel PET radioligand for human brain imaging of cannabinoid CB1 receptors. NeuroImage 84: 733-741, 2014.

S.S. Shrestha, D.S. Pine, D.A. Luckenbaugh, K. Varnas, I.D. Henter, R.B. Innis, A.A. Mathe, and P. Svenningsson. Antidepressant effects on serotonin 1A/1B receptors in the rat brain using a gene x environment model. Neurosci Letts. 559: 163-168, 2014.

C.H. Lyoo, P. Zanotti-Fregonara, S.S. Zoghbi, J.-S. Liow, R. Xu, V.W. Pike, C.A. Zarate, Jr., M. Fujita, and R.B. Innis. Image-derived input function derived from a supervised clustering algorithm: methodology and validation in a clinical protocol using [11C](R)-rolipram. PLOS ONE, 9(2): e89101, 2014.

N.J. Lodge, Y.-W. Li, F.T. Chin, D.D. Dischino, S.S. Zoghbi, J.A. Deskus, R.J. Mattson, M. Imaizumi, R. Pieschl, T.F. Molski, M. Fujita, H. Dulac, R. Zaczek, J.J. Bronson, J.E. Macor, R.B. Innis, V.W. Pike. Synthesis and evaluation of candidate PET radioligands for corticotrophin-releasing factor type-1 receptors. Nucl. Med. Biol. 41: 524-535, 2014.

C. Brouwer, K. Jenko, S.S. Zoghbi, R.B. Innis, and V.W. Pike. Development of N-methyl-(2-arylquinolin-4-yl)oxypropanamides as leads to PET radioligands for translocator protein (18 kDa). J. Med. Chem. 57: 6240-4251, 2014.

P. Zanotti-Fregonara, C.H. Lyoo, A. Bar-Hen, J.-S. Liow, S.S. Zoghbi, M. Fujita, R.B. Innis. Application of calibrated image derived input function to a clinical protocol. Nucl. Med. Comm., 35: 1188-1190, 2014.

P. Zanotti-Fregonara, Y. Zhang, K.J. Jenko, R.L. Gladding, S.S. Zoghbi, M. Fujita, G. Sbardella, S. Castellano, S. Taliani, C. Martini, R.B. Innis, F. Da Settimo, and V.W. Pike. Synthesis and evaluation of translocator 18 kDa protein (TSPO) positron emission tomography (PET) radioligands with low binding sensitivity to human single nucleotide polymorphism rs6971. ACS Chemical Neuroscience, 10: 963-971, 2014.

T.G. Lohith, R. Xu, T. Tsujikawa, C.L. Morse, K.B. Anderson, R.L. Gladding, S.S. Zoghbi, M. Fujita, R.B. Innis, and V.W. Pike. Evaluation in monkey of two candidate PET radioligands, [11C]RX-1 and [18F]RX-2, for imaging brain 5-HT4 receptors. Synapse, 68: 613-623, 2014.

2015

W.C. Kreisl, R. Bhatia, C.L. Morse, A.E. Woock, S.S. Zoghbi, H.U. Shetty, V.W. Pike, and R.B. Innis. Increased permeability-glycoprotein inhibition at the human blood-brain barrier can be safely achieved by performing PET during peak plasma concentrations of tariquidar. J. Nucl Med. 56: 82-87, 2015.

L.D. Gershen, P. Zanotti-Fregonara, I.H. Dustin, J.-S. Liow, J. Hirvonen, W.C. Kreisl, K.J. Jenko, S.K. Inati, M. Fujita, C.L. Morse, C. Brouwer, J.S. Hong, V.W. Pike, S.S. Zoghbi, R.B. Innis, and W.H. Theodore. Neuroinflammation in temporal lobe epilepsy measured using positron emission tomographic imaging of translocator protein. JAMA Neurology, 72: 882-888, 2015.

C.H. Lyoo, M. Ikawa, J.-S. Liow, S.S. Zoghbi, C.L. Morse, V.W. Pike, M. Fujita, R.B. Innis, and W.C. Kreisl. Cerebellum can serve as a pseudo-reference region in Alzheimer’s disease to detect neuroinflammation measured with PET radioligand binding to translocator protein. J Nucl. Med. 56: 701-706, 2015.

L.D. Weidner, S.S. Zoghbi, S. Lu, S. Shukla, S.V. Ambudkar, V.W. Pike, J. Mulder, M.M. Gottesman, R.B. Innis, and M.D. Hall. The inhibitor Ko143 is not specific for ABCG2. J. Pharmacol. Exp. Therap., 354: 384-93, 2015.

J. Hong, S. Lu, R. Xu, J.-S. Liow, A.E. Woock, K.J. Jenko, R.L. Gladding, S.S. Zoghbi, R.B. Innis, and V.W. Pike.  [carbonyl-11C]4-Fluoro-N-methyl-N-(4-(6-(methylamino)pyrimidin-4-yl)thiazol-2-yl)benzamide ([11C]FIMX) is an effective radioligand for PET imaging of metabotropic glutamate receptor 1 (mGluR1) in monkey brain. Nucl. Med. Biol., 42: 967-974, 2015.

G.R. Naumiec, K.J. Jenko, S.S. Zoghbi, R.B. Innis, L. Cai, V.W. Pike. N’-3-(Trifluoromethyl)phenyl derivatives of N-aryl –N’-methylguanidines as prospective PET radioligands for the open channel of the N-Methyl-D-asparate (NMDA) receptor: synthesis and structure-affinity relationships. J. Med. Chem., 58: 9722-9730, 2015.

2016

P. Zanotti-Fregonara, R. Xu, S.S. Zoghbi, J.-S. Liow, M. Fujita, M. Veronese, R.L. Gladding, D. Rallis-Frutos, J. Hong, V.W. Pike, and R.B. Innis. The PET radioligand 18F-FIMX images and quantifies metabotropic glutamate receptor 1 in proportion to the regional density of its gene transcript in human brain. J. Nucl. Med., 57: 242-247, 2016.

L.D. Weidner, K.-L. Fung, P. Kannan, J. Moen, J. Kumar, J. Mulder, R.B. Innis, M.M. Gottesman, and M.D. Hall. Tariquidar is an inhibitor and not a substrate of human and mouse P-gp. Drug Metab. Dispos., 44: 275-282, 2016.

M. Veronese, P. Zanotti-Fregonara, G. Rizzo, A. Bertoldo, R.B. Innis, and F.E. Turkheimer. Measuring specific receptor binding of a PET radioligand in human brain without pharmacological blockade: the genomic plot. NeuroImage, 130: 1-12, 2016.

W.C. Kreisl, C.H. Lyoo, J.-S. Liow, M. Wei, J. Snow, E. Page, K.J. Jenko, C.L. Morse, S.S. Zoghbi, V.W. Pike, R.S. Turner, and R.B. Innis. 11C-PBR28 binding to translocator protein increases with progression of Alzheimer’s disease. Neurobiology of Aging, 44: 53-61, 2016.

R. Cinar, M.R. Iyer, Z. Liu, Z. Cao, T. Jourdan, K. Erdelyi, G. Godlewski, G. Szanda, J. Liu, J.K. Park, B. Mukhopadhyay, A.Z. Rosenberg, J.-S. Liow, R.G. Lorenz, P. Pacher, R.B. Innis, and G. Kunos. Hybrid inhibitor of peripheral cannabinoid-1 receptors and inducible nitric oxide synthase mitigates liver fibrosis. JCI Insight 1, pii: e87336, 2016.

S.S. Shrestha, J.-S. Liow, K. Jenko, M. Ikawa, S.S. Zoghbi, and R.B. Innis. The 5-HT1A receptor PET radioligand 11C-CUMI-101 has significant binding to α1-adrenoceptors in human cerebellum, limiting its use as a reference region. J. Nucl. Med., 57:1945-1948, 2016.

J.-S. Liow, S.S. Zoghbi, S. Hu, M.D. Hall, C.S. Hines, H.U. Shetty, M.D. Araneta, E.M. Page, V.W. Pike, W.C. Kreisl, P. Hersocovitch, M.M. Gottesman, W.H. Theodore, and R.B. Innis. 18F-FCWAY, a serotonin 1A receptor radioligand, is a substrate for efflux transport at the human blood-brain barrier. NeuroImage 138: 134-140, 2016.

C. Brouwer, K.J. Jenko, S.S. Zoghbi, C.L. Morse, R.B. Innis, and V.W. Pike. Translocator protein ligands based on N-methyl-(quinolin-4-yl)oxypropanamides with properties suitable for PET radioligand development. Eur. J. Med. Chem. 124: 677-688, 2016.

2017

M. Fujita, E.M. Richards, M. Niciu, S.S. Zoghbi, J. Hong, S. Telu, C.S. Hines, V.W. Pike, C.A. Zarate Jr, and R.B. Innis. cAMP signaling in brain is decreased in unmedicated depressed patients and increased by treatment with a selective serotonin reuptake inhibitor. Mol. Psychiatry, 22: 754-759, 2017.

T.G. Lohith, T. Tsujikawa, F.G. Simeon, M. Veronese, S.S. Zoghbi, C.H. Lyoo, Y. Kimura, C.L., Morse, V.W. Pike, M. Fujita, and R.B. Innis. Comparison of two PET radioligands, [11C]FPEB and [11C]SP203, for quantification of metabotropic glutamate receptor 5 (mGluR5) in human brain. J. Cereb. Blood Flow Metab. 37: 2458-2470, 2017.

M. Ikawa, T.G. Lohith, S. Shrestha, S. Telu, S.S. Zoghbi, S. Castellano, S. Taliani, F. Da Settimo, M. Fujita, V.W. Pike R.B. Innis, and the Biomarkers Consortium PET Radioligand Project Team. 11C-ER176, a radioligand for 18-kDa translocator protein, has adequate sensitivity to robustly image all three affinity genotypes in human brain. J. Nucl. Med.  58:320-325, 2017.

W.C. Kreisl, C.H. Lyoo, J.-S. Liow, J. Snow, E. Page, K.J. Jenko, C.L. Morse, S.S. Zoghbi, V.W. Pike, R.S. Turner, R.B. Innis. Distinct pattern of radioligand binding to translocator protein 18 kDa in posterior cortical atrophy. Neurobiology of Aging 51: 132-140, 2017.

P. Kannan, M. Schain, W. Kretzschmar, L. Deuitch, N. Mitsios, B. Gulyas, H. Blom, M. Gottesman, R.B. Innis, M.D. Hall, and J. Mulder. An automated method measures variability in P-glycoprotein and ABCG2 densities across brain regions and brain matter. J. Cereb. Blood Flow Metab, 37:2062-2075, 2017.

W.C. Kreisl, R. Lawrence, E. Page, A.F. Teich, D.S. Subramaniam, R.B. Innis, and R.S. Turner. 11C-PBR28 PET detects translocator protein in a patient with astrocytoma and Alzheimer disease. Neurology, 88: 1001-1004, 2017.

F.A. Schroeder, T.M. Gilbert, N. Feng, B.D. Taillon, N.D. Volkow, R.B. Innis, J.M. Hooker, and B.K. Lipska. Expression of HDAC2 but not HDAC1 transcript is reduced in dorsolateral prefrontal cortex of patients with schizophrenia. ACS Chem Neurosci, 8:662-668, 2017.

M. Kobayashi, T. Jiang, S. Telu, S.S. Zoghbi, R.N. Gunn, E.A. Rabiner, D.R. Owen, Q. Guo, V.W. Pike, R.B. Innis, and M. Fujita. 11C-DPA-713 has much greater specific binding to translocator protein 18 kDa (TSPO) in human brain than 11C-(R)-PK11195.  J. Cereb. Blood Flow Metab, 2017. doi: 10.1177/0271678X17699223