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    Andrew R Tapper PhD

    TitleProfessor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentPsychiatry
    AddressUniversity of Massachusetts Medical School
    303 Belmont Street
    Worcester MA 01605
    Phone508-856-8164
      Other Positions
      InstitutionUMMS - School of Medicine
      DepartmentPsychiatry

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentBiochemistry and Molecular Pharmacology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentInterdisciplinary Graduate Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentMD/PhD Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentNeuroscience

      InstitutionUMMS - Programs, Centers and Institutes
      DepartmentBrudnick Neuropsychiatric Research Institute

        Overview 
        Narrative

        Academic Background:

        B.S. Universityof California, Riverside 1995
        M.S. University of California, Riverside 1996
        Ph.D. Vanderbilt University2001

        Postdoctoral Scholar 2002-2006
        Department of Biology
        California Institute of Technology

        Assistant Professor 2006-present
        Department of Psychiatry
        University of MassachusettsMedical School

        Neuronal nicotinic acetylcholine receptors in addiction and neurological disease.

        Nicotine addiction elicited by smoking tobacco is responsible for over 3 million deaths annually making it the largest cause of preventable mortality in the world. Nicotine is a naturally occurring alkaloid found in tobacco and is the primary addictive component of cigarette smoke. Vaporized nicotine is rapidly absorbed through the lungs where it enters the blood stream. Within seconds of inhaling, nicotine base readily crosses the blood-brain barrier where it gains access to neuronal nicotinic acetylcholine receptors (nAChRs) expressed throughout the central nervous system (CNS). In its protonated form, nicotine mimics the endogenous neurotransmitter, acetylcholine, and can activate nAChRs, utilizing the cholinergic system which, under normal conditions, plays an important role in reward, anxiety, cognition, attention, and many other physiological processes. This ability of nicotine to “hijack” nAChRs is thought to underlie the molecular basis of nicotine addiction.

        What are nicotinic acetylcholine receptors?

        Neuronal nAChRs are ligand gated cation-selective ion channels that, when activated, can depolarize and activate neurons, as well as modulate neurotransmitter release. Currently, 12 neuronal nicotinic acetylcholine receptor subunits have been identified (a2-10 andb 2-4). The majority of subunits form functional heteromeric pentamers while a subset may form homomeric receptors. Thus, a myriad of nAChR subtypes exist.

        Neuronal nAChRs in nicotine addiction.

        It is becoming increasingly clear that nicotine dependence begins with activation of nAChRs. However, which nAChR subtypes are involved in the addictive properties of nicotine? Recent work has highlighted the idea that different subtypes may mediate different dependence-related behaviors. For example, activation of one particular nAChR subtype may be responsible for the rewarding properties of nicotine whereas chronic activation of a separate subtype may be responsible for withdrawal symptoms upon nicotine cessation. A primary goal of our lab is to identify specific nAChR subtypes critical for behaviors associated with addiction including reward, tolerance, sensitization, and withdrawal.

        Acute nicotine exposure elicits many physiological effects including reward, hypothermia, and, at high enough concentrations, seizures. However, smokers expose themselves to nicotine chronically. It is this chronic exposure that produces long term physiological and behavioral changes associated with dependence. A second goal of our lab is to identify circuits and gene products that undergo adaptations because of chronic nAChR activation (or desensitization) and trigger a nicotine dependent state.

        Neuronal nAChRs in the regulation of dopamine neurotransmission.

        Parkinson’s disease (PD) is a devastating movement disorder that affects approximately one percent of the population over the age of 60. The disease is characterized by slowness of movement (bradykinesia), rigidity, and resting tremor. PD is caused by the disruption of dopamine release in basal ganglia due to the progressive death of dopaminergic neurons in substantia nigra. The reason for this neuronal loss is unknown. To date, the predominant PD treatment is L-dopa, an isomer to the precursor of dopamine (DA) that is used to boost remaining DA release in surviving DAergic neurons. Because of L-dopa’s fading efficacy over time, more recent research has focused on identifying neuroprotective agents that promote midbrain DAergic neuron survival. Remarkably, strong epidemiological data indicates PD is less prevalent in smokers. In addition, animal studies have found that nicotine, the addictive component of tobacco smoke, protects DAergic neurons from chemical insult. Thus, nicotine has emerged as a potential neuroprotective agent in PD. An additional goal of the lab is to understand how nicotinic receptors regulate dopamine neurotransmission in brain regions implicated in Parkinson’s disease.

         



        Rotation Projects

        Rotation Projects:

        1. Identify the role of specific nicotinic receptor subtypes in nicotine withdrawal. This project combines novel rodent models of nicotine dependence and incorporates behavior, pharmacology, and neurophysiology to understand withdrawal.

        2. There is mounting evidence that nicotinic acetylcholine receptors are involved in other forms of drug addiction besides nicotine. A second project involves determining the role of nAChRs in mediating the addictive properties of alcohol, cocaine, and heroin.

        Because of their wide distribution in the CNS, neuronal nAChRs have been linked to a variety of neurological diseases ranging from Parkinson’s disease to depression to epilepsy. Additional rotation projects are available to elucidate the function of nicotinic receptors in these neurological conditions.



        Bibliographic 
        selected publications
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        1. Guildford MJ, Sacino AV, Tapper AR. Modulation of ethanol reward sensitivity by nicotinic acetylcholine receptors containing the a6 subunit. Alcohol. 2016 Oct 8.
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        2. Pang X, Liu L, Ngolab J, Zhao-Shea R, McIntosh JM, Gardner PD, Tapper AR. Habenula cholinergic neurons regulate anxiety during nicotine withdrawal via nicotinic acetylcholine receptors. Neuropharmacology. 2016 Aug; 107:294-304.
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        3. Slater CA, Jackson A, Muldoon PP, Dawson A, O'Brien M, Soll LG, Abdullah R, Carroll FI, Tapper AR, Miles MF, Banks ML, Bettinger JC, Damaj IM. Nicotine Enhances the Hypnotic and Hypothermic Effects of Alcohol in the Mouse. Alcohol Clin Exp Res. 2016 Jan; 40(1):62-72.
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        4. Shea JM, Serra RW, Carone BR, Shulha HP, Kucukural A, Ziller MJ, Vallaster MP, Gu H, Tapper AR, Gardner PD, Meissner A, Garber M, Rando OJ. Genetic and Epigenetic Variation, but Not Diet, Shape the Sperm Methylome. Dev Cell. 2015 Dec 21; 35(6):750-8.
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        5. You IJ, Wright SR, Garcia-Garcia AL, Tapper AR, Gardner PD, Koob GF, David Leonardo E, Bohn LM, Wee S. 5-HT1A Autoreceptors in the Dorsal Raphe Nucleus Convey Vulnerability to Compulsive Cocaine Seeking. Neuropsychopharmacology. 2016 Apr; 41(5):1210-22.
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        6. Zhao-Shea R, DeGroot SR, Liu L, Vallaster M, Pang X, Su Q, Gao G, Rando OJ, Martin GE, George O, Gardner PD, Tapper AR. Corrigendum: Increased CRF signalling in a ventral tegmental area-interpeduncular nucleus-medial habenula circuit induces anxiety during nicotine withdrawal. Nat Commun. 2015; 6:7625.
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        7. Ngolab J, Liu L, Zhao-Shea R, Gao G, Gardner PD, Tapper AR. Functional Upregulation of a4* Nicotinic Acetylcholine Receptors in VTA GABAergic Neurons Increases Sensitivity to Nicotine Reward. J Neurosci. 2015 Jun 3; 35(22):8570-8.
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        8. Aad G, Abbott B, Abdallah J, Abdinov O, Aben R, Abolins M, AbouZeid OS, Abramowicz H, Abreu H, Abreu R, Abulaiti Y, Acharya BS, Adamczyk L, Adams DL, Adelman J, Adomeit S, Adye T, Affolder AA, Agatonovic-Jovin T, Aguilar-Saavedra JA, Ahlen SP, Ahmadov F, Aielli G, Akerstedt H, Åkesson TP, Akimoto G, Akimov AV, Alberghi GL, Albert J, Albrand S, Alconada Verzini MJ, Aleksa M, Aleksandrov IN, Alexa C, Alexander G, Alexopoulos T, Alhroob M, Alimonti G, Alio L, Alison J, Alkire SP, Allbrooke BM, Allport PP, Aloisio A, Alonso A, Alonso F, Alpigiani C, Altheimer A, Alvarez Gonzalez B, Álvarez Piqueras D, Alviggi MG, Amadio BT, Amako K, Amaral Coutinho Y, Amelung C, Amidei D, Amor Dos Santos SP, Amorim A, Amoroso S, Amram N, Amundsen G, Anastopoulos C, Ancu LS, Andari N, Andeen T, Anders CF, Anders G, Anders JK, Anderson KJ, Andreazza A, Andrei V, Angelidakis S, Angelozzi I, Anger P, Angerami A, Anghinolfi F, Anisenkov AV, Anjos N, Annovi A, Antonelli M, Antonov A, Antos J, Anulli F, Aoki M, Aperio Bella L, Arabidze G, Arai Y, Araque JP, Arce AT, Arduh FA, Arguin JF, Argyropoulos S, Arik M, Armbruster AJ, Arnaez O, Arnal V, Arnold H, Arratia M, Arslan O, Artamonov A, Artoni G, Asai S, Asbah N, Ashkenazi A, Åsman B, Asquith L, Assamagan K, Astalos R, Atkinson M, Atlay NB, Auerbach B, Augsten K, Aurousseau M, Avolio G, Axen B, Ayoub MK, Azuelos G, Baak MA, Baas AE, Bacci C, Bachacou H, Bachas K, Backes M, Backhaus M, Badescu E, Bagiacchi P, Bagnaia P, Bai Y, Bain T, Baines JT, Baker OK, Balek P, Balestri T, Balli F, Banas E, Banerjee S, Bannoura AA, Bansil HS, Barak L, Baranov SP, Barberio EL, Barberis D, Barbero M, Barillari T, Barisonzi M, Barklow T, Barlow N, Barnes SL, Barnett BM, Barnett RM, Barnovska Z, Baroncelli A, Barone G, Barr AJ, Barreiro F, Barreiro Guimarães da Costa J, Bartoldus R, Barton AE, Bartos P, Bassalat A, Basye A, Bates RL, Batista SJ, Batley JR, Battaglia M, Bauce M, Bauer F, Bawa HS, Beacham JB, Beattie MD, Beau T, Beauchemin PH, Beccherle R, Bechtle P, Beck HP, Becker K, Becker M, Becker S, Beckingham M, Becot C, Beddall AJ, Beddall A, Bednyakov VA, Bee CP, Beemster LJ, Beermann TA, Begel M, Behr JK, Belanger-Champagne C, Bell WH, Bella G, Bellagamba L, Bellerive A, Bellomo M, Belotskiy K, Beltramello O, Benary O, Benchekroun D, Bender M, Bendtz K, Benekos N, Benhammou Y, Benhar Noccioli E, Benitez Garcia JA, Benjamin DP, Bensinger JR, Bentvelsen S, Beresford L, Beretta M, Berge D, Bergeaas Kuutmann E, Berger N, Berghaus F, Beringer J, Bernard C, Bernard NR, Bernius C, Bernlochner FU, Berry T, Berta P, Bertella C, Bertoli G, Bertolucci F, Bertsche C, Bertsche D, Besana MI, Besjes GJ, Bessidskaia Bylund O, Bessner M, Besson N, Betancourt C, Bethke S, Bevan AJ, Bhimji W, Bianchi RM, Bianchini L, Bianco M, Biebel O, Bieniek SP, Biglietti M, Bilbao De Mendizabal J, Bilokon H, Bindi M, Binet S, Bingul A, Bini C, Black CW, Black JE, Black KM, Blackburn D, Blair RE, Blanchard JB, Blanco JE, Blazek T, Bloch I, Blocker C, Blum W, Blumenschein U, Bobbink GJ, Bobrovnikov VS, Bocchetta SS, Bocci A, Bock C, Boehler M, Bogaerts JA, Bogdanchikov AG, Bohm C, Boisvert V, Bold T, Boldea V, Boldyrev AS, Bomben M, Bona M, Boonekamp M, Borisov A, Borissov G, Borroni S, Bortfeldt J, Bortolotto V, Bos K, Boscherini D, Bosman M, Boudreau J, Bouffard J, Bouhova-Thacker EV, Boumediene D, Bourdarios C, Bousson N, Boveia A, Boyd J, Boyko IR, Bozic I, Bracinik J, Brandt A, Brandt G, Brandt O, Bratzler U, Brau B, Brau JE, Braun HM, Brazzale SF, Brendlinger K, Brennan AJ, Brenner L, Brenner R, Bressler S, Bristow K, Bristow TM, Britton D, Britzger D, Brochu FM, Brock I, Brock R, Bronner J, Brooijmans G, Brooks T, Brooks WK, Brosamer J, Brost E, Brown J, Bruckman de Renstrom PA, Bruncko D, Bruneliere R, Bruni A, Bruni G, Bruschi M, Bryngemark L, Buanes T, Buat Q, Buchholz P, Buckley AG, Buda SI, Budagov IA, Buehrer F, Bugge L, Bugge MK, Bulekov O, Bullock D, Burckhart H, Burdin S, Burghgrave B, Burke S, Burmeister I, Busato E, et al. Combined Measurement of the Higgs Boson Mass in pp Collisions at sqrt[s]=7 and 8 TeV with the ATLAS and CMS Experiments. Phys Rev Lett. 2015 May 15; 114(19):191803.
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        9. Zhao-Shea R, DeGroot SR, Liu L, Vallaster M, Pang X, Su Q, Gao G, Rando OJ, Martin GE, George O, Gardner PD, Tapper AR. Increased CRF signalling in a ventral tegmental area-interpeduncular nucleus-medial habenula circuit induces anxiety during nicotine withdrawal. Nat Commun. 2015 Apr 21; 6:6770.
          View in: PubMed
        10. Grieder TE, Herman MA, Contet C, Tan LA, Vargas-Perez H, Cohen A, Chwalek M, Maal-Bared G, Freiling J, Schlosburg JE, Clarke L, Crawford E, Koebel P, Repunte-Canonigo V, Sanna PP, Tapper AR, Roberto M, Kieffer BL, Sawchenko PE, Koob GF, van der Kooy D, George O. VTA CRF neurons mediate the aversive effects of nicotine withdrawal and promote intake escalation. Nat Neurosci. 2014 Dec; 17(12):1751-8.
          View in: PubMed
        11. Hogan EM, Casserly AP, Scofield MD, Mou Z, Zhao-Shea R, Johnson CW, Tapper AR, Gardner PD. miRNAome analysis of the mammalian neuronal nicotinic acetylcholine receptor gene family. RNA. 2014 Dec; 20(12):1890-9.
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        12. Zhao-Shea R, Liu L, Pang X, Gardner PD, Tapper AR. Activation of GABAergic neurons in the interpeduncular nucleus triggers physical nicotine withdrawal symptoms. Curr Biol. 2013 Dec 2; 23(23):2327-35.
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        13. Pang X, Hogan EM, Casserly A, Gao G, Gardner PD, Tapper AR. Dicer expression is essential for adult midbrain dopaminergic neuron maintenance and survival. Mol Cell Neurosci. 2014 Jan; 58:22-8.
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        14. Improgo MR, Soll LG, Tapper AR, Gardner PD. Nicotinic acetylcholine receptors mediate lung cancer growth. Front Physiol. 2013; 4:251.
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        15. Almeida S, Gascon E, Tran H, Chou HJ, Gendron TF, Degroot S, Tapper AR, Sellier C, Charlet-Berguerand N, Karydas A, Seeley WW, Boxer AL, Petrucelli L, Miller BL, Gao FB. Modeling key pathological features of frontotemporal dementia with C9ORF72 repeat expansion in iPSC-derived human neurons. Acta Neuropathol. 2013 Sep; 126(3):385-99.
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        16. Liu L, Zhao-Shea R, McIntosh JM, Tapper AR. Nicotinic acetylcholine receptors containing the a6 subunit contribute to ethanol activation of ventral tegmental area dopaminergic neurons. Biochem Pharmacol. 2013 Oct 15; 86(8):1194-200.
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        17. Soll LG, Grady SR, Salminen O, Marks MJ, Tapper AR. A role for a4(non-a6)* nicotinic acetylcholine receptors in motor behavior. Neuropharmacology. 2013 Oct; 73:19-30.
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        18. Hendrickson LM, Guildford MJ, Tapper AR. Neuronal nicotinic acetylcholine receptors: common molecular substrates of nicotine and alcohol dependence. Front Psychiatry. 2013; 4:29.
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        19. Liu L, Hendrickson LM, Guildford MJ, Zhao-Shea R, Gardner PD, Tapper AR. Nicotinic acetylcholine receptors containing the a4 subunit modulate alcohol reward. Biol Psychiatry. 2013 Apr 15; 73(8):738-46.
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        20. Liu L, Zhao-Shea R, McIntosh JM, Gardner PD, Tapper AR. Nicotine persistently activates ventral tegmental area dopaminergic neurons via nicotinic acetylcholine receptors containing a4 and a6 subunits. Mol Pharmacol. 2012 Apr; 81(4):541-8.
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        21. Armata HL, Shroff P, Garlick DE, Penta K, Tapper AR, Sluss HK. Loss of p53 Ser18 and Atm results in embryonic lethality without cooperation in tumorigenesis. PLoS One. 2011; 6(9):e24813.
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        22. Improgo MR, Johnson CW, Tapper AR, Gardner PD. Bioluminescence-based high-throughput screen identifies pharmacological agents that target neurotransmitter signaling in small cell lung carcinoma. PLoS One. 2011; 6(9):e24132.
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        23. Improgo MR, Tapper AR, Gardner PD. Nicotinic acetylcholine receptor-mediated mechanisms in lung cancer. Biochem Pharmacol. 2011 Oct 15; 82(8):1015-21.
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        24. Hendrickson LM, Gardner P, Tapper AR. Nicotinic acetylcholine receptors containing the a4 subunit are critical for the nicotine-induced reduction of acute voluntary ethanol consumption. Channels (Austin). 2011 Mar-Apr; 5(2):124-7.
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        25. Zhao-Shea R, Liu L, Soll LG, Improgo MR, Meyers EE, McIntosh JM, Grady SR, Marks MJ, Gardner PD, Tapper AR. Nicotine-mediated activation of dopaminergic neurons in distinct regions of the ventral tegmental area. Neuropsychopharmacology. 2011 Apr; 36(5):1021-32.
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        26. Scofield MD, Tapper AR, Gardner PD. A transcriptional regulatory element critical for CHRNB4 promoter activity in vivo. Neuroscience. 2010 Nov 10; 170(4):1056-64.
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        27. Hendrickson LM, Zhao-Shea R, Pang X, Gardner PD, Tapper AR. Activation of alpha4* nAChRs is necessary and sufficient for varenicline-induced reduction of alcohol consumption. J Neurosci. 2010 Jul 28; 30(30):10169-76.
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        28. Improgo MR, Scofield MD, Tapper AR, Gardner PD. From smoking to lung cancer: the CHRNA5/A3/B4 connection. Oncogene. 2010 Sep 2; 29(35):4874-84.
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        29. Improgo MR, Scofield MD, Tapper AR, Gardner PD. The nicotinic acetylcholine receptor CHRNA5/A3/B4 gene cluster: dual role in nicotine addiction and lung cancer. Prog Neurobiol. 2010 Oct; 92(2):212-26.
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        30. Improgo MR, Schlichting NA, Cortes RY, Zhao-Shea R, Tapper AR, Gardner PD. ASCL1 regulates the expression of the CHRNA5/A3/B4 lung cancer susceptibility locus. Mol Cancer Res. 2010 Feb; 8(2):194-203.
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        31. Zhao-Shea R, Cohen BN, Just H, McClure-Begley T, Whiteaker P, Grady SR, Salminen O, Gardner PD, Lester HA, Tapper AR. Dopamine D2-receptor activation elicits akinesia, rigidity, catalepsy, and tremor in mice expressing hypersensitive {alpha}4 nicotinic receptors via a cholinergic-dependent mechanism. FASEB J. 2010 Jan; 24(1):49-57.
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        32. Vanoye CG, Welch RC, Daniels MA, Manderfield LJ, Tapper AR, Sanders CR, George AL. Distinct subdomains of the KCNQ1 S6 segment determine channel modulation by different KCNE subunits. J Gen Physiol. 2009 Sep; 134(3):207-17.
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        33. Mou Z, Tapper AR, Gardner PD. The armadillo repeat-containing protein, ARMCX3, physically and functionally interacts with the developmental regulatory factor Sox10. J Biol Chem. 2009 May 15; 284(20):13629-40.
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        34. Hendrickson LM, Zhao-Shea R, Tapper AR. Modulation of ethanol drinking-in-the-dark by mecamylamine and nicotinic acetylcholine receptor agonists in C57BL/6J mice. Psychopharmacology (Berl). 2009 Jul; 204(4):563-72.
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        35. Martin GE, Hendrickson LM, Penta KL, Friesen RM, Pietrzykowski AZ, Tapper AR, Treistman SN. Identification of a BK channel auxiliary protein controlling molecular and behavioral tolerance to alcohol. Proc Natl Acad Sci U S A. 2008 Nov 11; 105(45):17543-8.
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        36. Schroeder FA, Penta KL, Matevossian A, Jones SR, Konradi C, Tapper AR, Akbarian S. Drug-induced activation of dopamine D(1) receptor signaling and inhibition of class I/II histone deacetylase induce chromatin remodeling in reward circuitry and modulate cocaine-related behaviors. Neuropsychopharmacology. 2008 Nov; 33(12):2981-92.
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        37. Tapper AR, McKinney SL, Marks MJ, Lester HA. Nicotine responses in hypersensitive and knockout alpha 4 mice account for tolerance to both hypothermia and locomotor suppression in wild-type mice. Physiol Genomics. 2007 Nov 14; 31(3):422-8.
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        38. Tapper AR, McKinney SL, Nashmi R, Schwarz J, Deshpande P, Labarca C, Whiteaker P, Marks MJ, Collins AC, Lester HA. Nicotine activation of alpha4* receptors: sufficient for reward, tolerance, and sensitization. Science. 2004 Nov 5; 306(5698):1029-32.
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        39. Lester HA, Fonck C, Tapper AR, McKinney S, Damaj MI, Balogh S, Owens J, Wehner JM, Collins AC, Labarca C. Hypersensitive knockin mouse strains identify receptors and pathways for nicotine action. Curr Opin Drug Discov Devel. 2003 Sep; 6(5):633-9.
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        40. Tapper AR, George AL. Heterologous expression of ion channels. Methods Mol Biol. 2003; 217:285-94.
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        41. Andelfinger G, Tapper AR, Welch RC, Vanoye CG, George AL, Benson DW. KCNJ2 mutation results in Andersen syndrome with sex-specific cardiac and skeletal muscle phenotypes. Am J Hum Genet. 2002 Sep; 71(3):663-8.
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        42. Tapper AR, George AL. Location and orientation of minK within the I(Ks) potassium channel complex. J Biol Chem. 2001 Oct 12; 276(41):38249-54.
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        43. Tapper AR, George AL. MinK subdomains that mediate modulation of and association with KvLQT1. J Gen Physiol. 2000 Sep; 116(3):379-90.
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        44. Morrow JD, Tapper AR, Zackert WE, Yang J, Sanchez SC, Montine TJ, Roberts LJ. Formation of novel isoprostane-like compounds from docosahexaenoic acid. Adv Exp Med Biol. 1999; 469:343-7.
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        45. Roberts LJ, Montine TJ, Markesbery WR, Tapper AR, Hardy P, Chemtob S, Dettbarn WD, Morrow JD. Formation of isoprostane-like compounds (neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem. 1998 May 29; 273(22):13605-12.
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