Information de reference pour ce titreAccession Number: | 00009274-200827090-00023.
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Author: | Jedema, Hank P. 1,2; Gold, Stephen J. 3; Gonzalez-Burgos, Guillermo 2,4; Sved, Alan F. 1,2,4; Tobe, Ben J. 5; Wensel, Theodore G. 5; Grace, Anthony A. 1,2,4,6
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Institution: | Departments of (1)Neuroscience (4)Psychiatry (6)Psychology (2)Center for Neuroscience at the University of Pittsburgh (CNUP), University of Pittsburgh, Pittsburgh, PA 15261, USA (3)Department of Psychiatry, UTSW, Dallas, TX, USA (5)Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX, USA
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Title: | |
Source: | European Journal of Neuroscience. 27(9):2433-2443, May 2008.
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Abstract: | Chronic stress exposure alters the central noradrenergic neurons originating from the locus coeruleus (LC). Previously, we demonstrated that evoked increases in the firing rate of LC neurons and their release of norepinephrine are enhanced following chronic cold exposure. In the present studies, we tested the hypothesis that reduced feedback inhibition of LC neurons might underlie these alterations in LC activity by examining the effect of [alpha]2-autoreceptor stimulation on LC activity in chronically stressed rats using in vivo and in vitro single unit recordings. Given that regulators of G-protein signaling (RGS) proteins can impact the coupling of [alpha]2-autoreceptors to downstream signaling cascades, we also explored the expression of several RGS proteins following chronic stress exposure. We observed that the [alpha]2-autoreceptor-evoked inhibition of LC neurons was reduced and that the expression of RGS7 was increased following chronic stress exposure. Finally, we demonstrated that intracellular administration of RGS7 via patch clamp electrodes mimicked the stress-induced decrease in clonidine-evoked autoreceptor-mediated inhibition. These novel data provide a mechanism to explain how chronic stress-induced alterations in receptor coupling can result in changes in [alpha]2-autoreceptor control of noradrenergic function throughout the central nervous system, potentially leading to alterations in anxiety-related behaviors, and may suggest novel therapeutic targets for the treatment of mood and anxiety disorders.
Copyright (C) 2008 Blackwell Publishing Ltd.
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Author Keywords: | [alpha]2-adrenergic receptor; chronic stress; clonidine; norepinephrine; rat; RGS protein.
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References: | Abercrombie, E.D. & Jacobs, B.L. (1987) Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli. J. Neurosci., 7, 2837-2843.
Abercrombie, E.D., Nisenbaum, L.K. & Zigmond, M.J. (1992) Impact of acute and chronic stress on the release and synthesis of norepinephrine in brain: microdialysis studies in behaving animals. In: Kvetnansky, R., McCarty, R. & Axelrod, J. (Eds), Stress: Neuroendocrine and Molecular Approaches. Gordon and Breach Science Publishers, New York, pp. 29-42.
Acosta, G.B., Otero Losada, M.E. & Rubio, M.C. (1993) Area-dependent changes in GABAergic function after acute and chronic cold stress. Neuroscience Lett., 154, 175-178.
Adell, A., Garcia-Marquez, C., Armario, A. & Gelpi, E. (1988) Chronic stress increases serotonin and noradrenaline in rat brain and sensitizes their responses to a further acute stress. J. Neurochem., 50, 1678-1681.
Aghajanian, G.K. & VanderMaelen, C.P. (1982) alpha 2-adrenoceptor-mediated hyperpolarization of locus coeruleus neurons: intracellular studies in vivo. Science, 215, 1394-1396.
Aghajanian, G.K. & Wang, Y.Y. (1986) Pertussis toxin blocks the outward currents evoked by opiate and alpha 2-agonists in locus coeruleus neurons. Brain Res., 371, 390-394.
Andrade, R. & Aghajanian, G.K. (1984) Intrinsic regulation of locus coeruleus neurons: electrophysiological evidence indicating a predominant role for autoinhibition. Brain Res., 310, 401-406.
Anisman, H. & Zacharko, R.M. (1990) Multiple neurochemical and behavioral consequences of stressors: implications for depression. Pharm. Ther., 46, 119-136.
Aston-Jones, G., Rajkowski, J. & Cohen, J. (2000) Locus coeruleus and regulation of behavioral flexibility and attention. Prog. Brain Res., 126, 165-182.
Aston-Jones, G., Shipley, M.T. & Grzanna, R. (1995) The locus coeruleus, A5 and A7 noradrenergic cell groups. In: Paxinos, G. (Ed.), The Rat Nervous System. Academic Press, New York, pp. 183-213.
Baffi, J.S. & Palkovits, M. (2000) Fine topography of brain areas activated by cold stress. A fos immunohistochemical study in rats. Neuroendocrinology, 72, 102-113.
Bahia, D.S., Sartania, N., Ward, R.J., Cavalli, A., Jones, T.L.Z., Druey, K.M. & Milligan, G. (2003) Concerted stimulation and deactivation of pertussis toxin-sensitive G proteins by chimeric G protein-coupled receptor-regulator of G protein signaling 4 fusion proteins: analysis of the contribution of palmitoylated cysteine residues to the GAP activity of RGS4. J. Neurochem., 85, 1289-1298.
Benzing, T., Brandes, R., Sellin, L., Schermer, B., Lecker, S., Walz, G. & Kim, E. (1999) Upregulation of RGS7 may contribute to tumor necrosis factor-induced changes in central nervous function. Nat. Med., 5, 913-918.
Bremner, J.D., Innis, R.B., Ng, C.K., Staib, L.H., Salomon, R.M., Bronen, R.A., Duncan, J., Southwick, S.M., Krystal, J.H., Rich, D., Zubal, G., Dey, H., Soufer, R. & Charney, D.S. (1997) Positron emission tomography measurement of cerebral metabolic correlates of yohimbine administration in combat-related posttraumatic stress disorder. Arch. Gen. Psychiatry, 54, 246-254.
Bunemann, M., Bucheler, M.M., Philipp, M., Lohse, M.J. & Hein, L. (2001) Activation and deactivation kinetics of alpha 2A- and alpha 2C-adrenergic receptor-activated G protein-activated inwardly rectifying K+ channel currents. J. Biol. Chem., 276, 47512-47517.
Cabrera-Vera, T.M., Hernandez, S., Earls, L.R., Medkova, M., Sundgren-Andersson, A.K., Surmeier, D.J. & Hamm, H.E. (2004) RGS9-2 modulates D2 dopamine receptor-mediated Ca2+ channel inhibition in rat striatal cholinergic interneurons. Proc. Natl Acad. Sci. USA, 101, 16339-16344.
Cavalli, A., Druey, K.M. & Milligan, G. (2000) The regulator of G protein signaling RGS4 selectively enhances alpha 2A-adreoreceptor stimulation of the GTPase activity of Go1alpha and Gi2alpha. J. Biol. Chem., 275, 23693-23699.
Curtis, A.L., Lechner, S.M., Pavcovich, L.A. & Valentino, R.J. (1997) Activation of the locus coeruleus noradrenergic system by intracoerulear microinfusion of corticotropin-releasing factor: effects on discharge rate, cortical norepinephrine levels and cortical electroencephalographic activity. J. Pharm. Exp. Ther., 281, 163-172.
Drenan, R.M., Doupnik, C.A., Boyle, M.P., Muglia, L.J., Huettner, J.E., Linder, M.E. & Blumer, K.J. (2005) Palmitoylation regulates plasma membrane-nuclear shuttling of R7 BP, a novel membrane anchor for the RGS7 family. J. Cell Biol., 169, 623-633.
Drenan, R.M., Doupnik, C.A., Jayaraman, M., Buchwalter, A.L., Kaltenbronn, K.M., Huettner, J.E., Linder, M.E. & Blumer, K.J. (2006) R7 BP augments the function of RGS7*Gbeta5 complexes by a plasma membrane-targeting mechanism. J. Biol. Chem., 281, 28222-28231.
Elsworth, J.D., Morrow, B.A., Nguyen, V.T., Mitra, J., Picciotto, M.R. & Roth, R.H. (2007) Prenatal cocaine exposure enhances responsivity of locus coeruleus norepinephrine neurons: role of autoreceptors. Neuroscience, 147, 419-427.
Featherby, T. & Lawrence, A.J. (2004) Chronic cold stress regulates ascending noradrenergic pathways. Neuroscience, 127, 949-960.
Finlay, J.M., Jedema, H.P., Rabinovic, A.D., Mana, M.J., Zigmond, M.J. & Sved, A.F. (1997) Impact of corticotropin-releasing hormone on extracellular norepinephrine in prefrontal cortex after chronic cold stress. J. Neurochem., 69, 144-150.
Flugge, G. (1996) Alterations in the central nervous alpha 2-adrenoceptor system under chronic psychosocial stress. Neuroscience., 75, 187-196.
Fluharty, S.J., Snyder, G.L., Stricker, E.M. & Zigmond, M.J. (1983) Short- and long-term changes in adrenal tyrosine hydroxylase activity during insulin-induced hypoglycemia and cold stress. Brain Res., 267, 384-387.
Folk, G.E. Jr (1974) Textbook of Environmental Physiology. Lea & Febiger, Philadelphia.
Foote, S.L., Bloom, F.E. & Aston-Jones, G. (1983) Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. Physiol. Rev., 63, 844-914.
Ghavami, A., Hunt, R.A., Olsen, M.A., Zhang, J., Smith, D.L., Kalgaonkar, S., Rahman, Z. & Young, K.H. (2004) Differential effects of regulator of G protein signaling (RGS) proteins on serotonin 5-HT1A, 5-HT2A, and dopamine D2 receptor-mediated signaling and adenylyl cyclase activity. Cell Signal, 16, 711-721.
Gold, S.J., Han, M.H., Herman, A.E., Ni, Y.G., Pudiak, C.M., Aghajanian, G.K., Liu, R.J., Potts, B.W., Mumby, S.M. & Nestler, E.J. (2003) Regulation of RGS proteins by chronic morphine in rat locus coeruleus. Eur. J. Neurosci., 17, 971-980.
Gold, S.J., Ni, Y.G., Dohlman, H.G. & Nestler, E.J. (1997) Regulators of G-protein signaling (RGS) proteins: region-specific expression of nine subtypes in rat brain. J. Neurosci., 17, 8024-8037.
Grace, A.A. & Bunney, B.S. (1984) The control of firing pattern in nigral dopamine neurons: burst firing. J. Neurosci., 4, 2877-2890.
Grant, S.J. & Redmond, D.E. Jr (1984) Neuronal activity of the locus ceruleus in awake Macaca arctoides. Exp. Neurol., 84, 701-708.
Gresch, P.J., Sved, A.F., Zigmond, M.J. & Finlay, J.M. (1994) Stress-induced sensitization of dopamine and norepinephrine efflux in medial prefrontal cortex of the rat. J. Neurochem., 63, 575-583.
Harlow, E. & Lane, D. (1988) Immunoblotting. In: Harlow, E. & Lane, D. (Eds), Antibodies: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 471-501.
He, W., Lu, L., Zhang, X., El-Hodiri, H.M., Chen, C.K., Slep, K.C., Simon, M.I., Jamrich, M. & Wensel, T.G. (2000) Modules in the photoreceptor RGS9-1.Gbeta 5L GTPase-accelerating protein complex control effector coupling, GTPase acceleration, protein folding, and stability. J. Biol. Chem., 275, 37093-37100.
Hepler, J.R. (2005) R7 BP: a surprising new link between G proteins, RGS proteins, and nuclear signaling in the brain. Sci. STKE, 2005, 294, pe38.
Heximer, S.P., Srinivasa, S.P., Bernstein, L.S., Bernard, J.L., Linder, M.E., Hepler, J.R. & Blumer, K.J. (1999) G protein selectivity is a determinant of RGS2 function. J. Biol. Chem., 274, 34253-34259.
Hollinger, S. & Hepler, J.R. (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol. Rev., 54, 527-559.
Hooks, S.B., Waldo, G.L., Corbitt, J., Bodor, E.T., Krumins, A.M. & Harden, T.K. (2003) RGS6, RGS7, RGS9, and RGS11 stimulate GTPase activity of Gi family G-proteins with differential selectivity and maximal activity. J. Biol. Chem., 278, 10087-10093.
Huang, H.P., Wang, S.R., Yao, W., Zhang, C., Zhou, Y., Chen, X.W., Zhang, B., Xiong, W., Wang, L.Y., Zheng, L.H., Landry, M., Hokfelt, T., Xu, Z.Q.D. & Zhou, Z. (2007) Long latency of evoked quantal transmitter release from somata of locus coeruleus neurons in rat pontine slices. Proc. Natl Acad. Sci. USA, 104, 1401-1406.
Jedema, H.P., Finlay, J.M., Sved, A.F. & Grace, A.A. (2001) Chronic cold exposure potentiates CRH-evoked increases in electrophysiologic activity of locus coeruleus neurons. Biol. Psychiatry, 49, 351-359.
Jedema, H.P. & Grace, A.A. (2003) Chronic exposure to cold stress alters electrophysiological properties of locus coeruleus neurons recorded in vitro. Neuropsychopharmacology, 28, 63-72.
Jedema, H.P., Sved, A.F., Zigmond, M.J. & Finlay, J.M. (1999) Sensitization of norepinephrine release in medial prefrontal cortex: effect of different chronic stress protocols. Brain Res., 830, 211-217.
Krumins, A.M., Barker, S.A., Huang, C. & Sunahara, R.K., Yu, K., Wilkie, T.M., Gold, S.J. & Mumby, S.M. (2004) Differentially regulated expression of endogenous RGS4 and RGS7. J. Biol. Chem., 279, 2593-2599.
Lacroix, D., Blier, P., Curet, O. & de Montigny, C. (1991) Effects of long-term desipramine administration on noradrenergic neurotransmission: electrophysiological studies in the rat brain. J. Pharm. Exp. Ther., 257, 1081-1090.
Linder, M.E., Middleton, P., Hepler, J.R., Taussig, R., Gilman, A.G. & Mumby, S.M. (1993) Lipid modifications of G proteins: alpha subunits are palmitoylated. Proc. Natl Acad. Sci. USA, 90, 3675-3679.
Mana, M.J. & Grace, A.A. (1997) Chronic cold stress alters the basal and evoked electrophysiological activity of rat locus coeruleus neurons. Neuroscience, 81, 1055-1064.
Meyer, H., Palchaudhuri, M., Scheinin, M. & Flugge, G. (2000) Regulation of alpha (2A) -adrenoceptor expression by chronic stress in neurons of the brain stem. Brain Res., 880, 147-158.
Miner, L.A.H., Jedema, H.P., Moore, F.W., Blakely, R.D., Grace, A.A. & sesack, S.R. (2006) Chronic stress increases the plasmalemmal distribution of the norepinephrine transporter and the coexpression of tyrosine hydroxylase in norepinephrine axons in the prefrontal cortex. J. Neuroscience (Online), 26, 1571-1578.
Mirnics, K., Middleton, F.A., Stanwood, G.D., Lewis, D.A. & Levitt, P. (2001) Disease-specific changes in regulator of G-protein signaling 4 (RGS4) expression in schizophrenia. Mol Psychiatry, 6, 293-301.
Moore, H., Rose, H.J. & Grace, A.A. (2001) Chronic cold stress reduces the spontaneous activity of ventral tegmental dopamine neurons. Neuropsychopharmacology, 24, 410-419.
Morilak, D.A., Barrera, G., Echevarria, D.J., Garcia, A.S., Hernandez, A., Ma, S. & Petre, C.O. (2005) Role of brain norepinephrine in the behavioral response to stress. Prog. Neuro-Psychopharmacol. Biol. Psychiatry, 29, 1214-1224.
Ni, Y.G., Gold, S.J., Iredale, P.A., Terwilliger, R.Z., Duman, R.S. & Nestler, E.J. (1999) Region-specific regulation of RGS4 (Regulator of G-protein-signaling protein type 4) in brain by stress and glucocorticoids: in vivo and in vitro studies. J. Neurosci., 19, 3674-3680.
Nisenbaum, L.K. & Abercrombie, E.D. (1992) Enhanced tyrosine hydroxylation in hippocampus of chronically stressed rats upon exposure to a novel stressor. J. Neurochem., 58, 276-281.
Nisenbaum, L.K. & Abercrombie, E.D. (1993) Presynaptic alterations associated with enhancement of evoked release and synthesis of norepinephrine in hippocampus of chronically cold-stressed rats. Brain Res., 608, 280-287.
Nisenbaum, L.K., Zigmond, M.J., Sved, A.F. & Abercrombie, E.D. (1991) Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor. J. Neurosci., 11, 1478-1484.
Oliveira-dos-Santos, A.J., Matsumoto, G., Snow, B.E., Bai, D., Houston, F.P., Whishaw, I.Q., Mariathasan, S., Sasaki, T., Wakeham, A., Ohashi, P.S., Roder, J.C., Barnes, C.A., Siderovski, D.P. & Penninger, J.M. (2000) Regulation of T cell activation, anxiety, and male aggression by RGS2. Proc. Natl Acad. Sci. USA., 97, 12272-12277.
Pardon, M.-C., Ma, S. & Morilak, D.A. (2003) Chronic cold stress sensitizes brain noradrenergic reactivity and noradrenergic facilitation of the HPA stress response in Wistar Kyoto rats. Brain Res., 971, 55-65.
Pavcovich, L.A., Cancela, L.M., Volosin, M., Molina, V.A. & Ramirez, O.A. (1990) Chronic stress-induced changes in locus coeruleus neuronal activity. Brain Res. Bull., 24, 293-296.
Pineda, J., Ruiz-Ortega, J.A. & Ugedo, L. (1997) Receptor reserve and turnover of alpha-2 adrenoceptors that mediate the clonidine-induced inhibition of rat locus coeruleus neurons in vivo. J. Pharm. Exp. Ther., 281, 690-698.
Prieto, M.N., Gamez, F.M. & Teresa Giralt, M. (2003) Effects of acute, repeated and chronic variable stress on in vivo tyrosine hydroxylase activity and on alpha (2)-adrenoceptor sensitivity in the rat brain. Stress, 6, 281-287.
Ross, E.M. & Wilkie, T.M. (2000) GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu. Rev. Biochem., 69, 795-827.
Seiple, S.D., Jedema, H.P., Sved, A.F., Zigmond, M.J., Austin, M.C. & Finlay, J.M. (1997) Chronic stress: effects on behavior and tyrosine hydroxylase mRNA in the locus coeruleus. Soc. Neurosci. Abstract, 23, 1078.
Simson, P.E. & Weiss, J.M. (1987) Alpha-2 receptor blockade increases responsiveness of locus coeruleus neurons to excitatory stimulation. J. Neurosci., 7, 1732-1740.
Simson, P.E. & Weiss, J.M. (1988) Altered activity of the locus coeruleus in an animal model of depression. Neuropsychopharmacology, 1, 287-295.
Southwick, S.M., 3rd, C.A.M., Bremner, A.D., Grillon, C.G., Krystal, J.H., Nagy, L.M. & Charney, D.S. (1997) Noradrenergic alterations in posttraumatic stress disorder. Ann. NY Acad. Sci., 821, 125-141.
Stanford, S.C. (1995) Central noradrenergic neurones and stress. Pharm. Ther., 68, 297-242.
Taymans, J.M., Wintmolders, C., Te Riele, P., Jurzak, M., Groenewegen, H.J., Leysen, J.E. & Langlois, X. (2002) Detailed localization of regulator of G protein signaling 2 messenger ribonucleic acid and protein in the rat brain. Neuroscience, 114, 39-53.
Thierry, A.M., Javoy, F., Glowinski, J. & Kety, S.S. (1968) Effects of stress on the metabolism of norepinephrine, dopamine and serotonin in the central nervous system of the rat. I. Modifications of norepinephrine turnover. J. Pharm. Exp. Ther., 163, 163-171.
Valentino, R.J. & Foote, S.L. (1988) Corticotropin-releasing hormone increases tonic but not sensory-evoked activity of noradrenergic locus coeruleus neurons in unanesthetized rats. J. Neurosci., 8, 1016-1025.
Vernikos, J., Dallman, M.F., Bonner, C., Katzen, A. & Shinsako, J. (1982) Pituitary-adrenal function in rats chronically exposed to cold. Endocrinology, 110, 413-420.
Williams, J.T., Henderson, G. & North, R.A. (1985) Characterization of alpha 2-adrenoceptors which increase potassium conductance in rat locus coeruleus neurones. Neuroscience, 14, 95-101.
Williams, J.T., North, R.A., Shefner, S.A., Nishi, S. & Egan, T.M. (1984) Membrane properties of rat locus coeruleus neurones. Neuroscience, 13, 137-156.
Witherow, D.S., Tovey, S.C., Wang, Q., Willars, G.B. & Slepak, V.Z. (2003) G beta 5.RGS7 inhibits G alpha q-mediated signaling via a direct protein-protein interaction. J. Biol. Chem., 278, 21307-21313.
Wong, M.L., Kling, M.A., Munson, P.J., Listwak, S., Licinio, J., Prolo, P., Karp, B., McCutcheon, I.E., Geracioti, T.D. Jr, DeBellis, M.D., Rice, K.C., Goldstein, D.S., Veldhuis, J.D., Chrousos, G.P., Oldfield, E.H., McCann, S.M. & Gold, P.W. (2000) Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: relation to hypercortisolism and corticotropin-releasing hormone. Proc. Natl Acad. Sci. USA, 97, 325-330.
Xie, G.-X. & Palmer, P.P. (2005) RGS proteins: new players in the field of opioid signaling and tolerance mechanisms. Anesth. Analg., 100, 1034-1042.
Xie, G.-X. & Palmer, P.P. (2007) How regulators of G protein signaling achieve selective regulation. J. Mol. Biol., 366, 349-365.
Xu, X., Zeng, W., Popov, S., Berman, D.M. & Davignon, I., Yu, K., Yowe, D., Offermanns, S., Muallem, S. & Wilkie, T.M. (1999) RGS proteins determine signaling specificity of Gq-coupled receptors. J. Biol. Chem., 274, 3549-3556.
Yalcin, B., Willis-Owen, S.A.G., Fullerton, J., Meesaq, A., Deacon, R.M., Rawlins, J.N.P., Copley, R.R., Morris, A.P., Flint, J. & Mott, R. (2004) Genetic dissection of a behavioral quantitative trait locus shows that Rgs2 modulates anxiety in mice.[see comment]. Nature Genet., 36, 1197-1202.
Zhang, S., Coso, O.A., Lee, C., Gutkind, J.S. & Simonds, W.F. (1996) Selective activation of effector pathways by brain-specific G protein beta5. J. Biol. Chem., 271, 33575-33579.
Zigmond, M.J., Finlay, J.M. & Sved, A.F. (1995) Neurochemical studies of central noradrenergic responses to acute and chronic stress. In: Friedman, M.J., Charney, D.S. & Deutsch, A.Y. (Eds), Neurobiological and Clinical Consequences of Stress: from Normal Adaptation to PTSD. Lippincott-Raven Publishers, Philadelpia, pp. 45-60.
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Language: | English.
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Document Type: | Research Report.
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Journal Subset: | Life Sciences.
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ISSN: | 0953-816X
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NLM Journal Code: | byg, 8918110
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