Functional role of dimer (heteromer) receptors in the CNS of mammalians
- Authors: Bukinich A.A.1, Shabanov P.D.1
-
Affiliations:
- Institute of Experimental Medicine
- Issue: Vol 13, No 1 (2015)
- Pages: 25-31
- Section: Articles
- URL: https://journals.eco-vector.com/RCF/article/view/729
- DOI: https://doi.org/10.17816/RCF13125-31
Cite item
Full Text
Abstract
A review of modern look at functional role of dimer (heteromer) receptors in the CNS of mammalians is presented in the article. According to original papers and publications analysis concerning dimer (heteromer) structure of G-coupled receptors in the CNS of mammalians was shown that functional role of dimer (heteromer) receptors formation is dual-code of information coding.
About the authors
Anna Alexandrovna Bukinich
Institute of Experimental Medicine
Email: abukinich@yahoo.com
PhD (Physiology), scientific researcher, Dept. of NeuroPharmacology
Petr Dmitriyevich Shabanov
Institute of Experimental Medicine
Email: pdshabanov@mail.ru
Doct. of Med. Sci. (Pharmacology), Professor and Head, Dept. of Pharmacology
References
- Bouvier M. Oligomerization of G-protein-coupled transmitter receptors // Nat. Rev. Neurosci. - 2001. - Vol. 2. - P. 274-286.
- Devi L. A. Heterodimerization of G-protein-coupled receptors: pharmacology, signaling and trafficking // Trends Pharmacol. Sci. - 2001. - Vol. 22, N. 10. - P. 532-537.
- Marshall F. H. Heterodimerization of G-protein-coupled receptors in the CNS // Curr. Opin. Pharmacol. - 2001. - Vol. 1. - P. 40-44.
- Angers S., Salahpour A., Bouvier M. Dimerization: an emerging concept for G protein-coupled receptor ontogeny and function // Ann. Rev. Pharmacol. Toxicol. - 2002. - Vol. 42. - P. 409-435.
- George S. R., O'Dowd B. F., Lee S. P. G-protein-coupled receptor oligomerizaton and its potential for drug discovery // Nat. Rev. Drug Discov. - 2002. - Vol. 1. - P. 808-820.
- Gazi L., Lopez-Gimenez J. F., Strange P. G. Formation of oligomers by G protein-coupled receptors // Curr. Opin. Drug Discov. Devel. - 2002. - Vol. 5. - P. 756-763.
- Agnati L. F., Ferre S., Lluis C., Franco R., Fuxe K. Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons // Pharmacol. Rev. 2003. - Vol. 55. - P. 509-550.
- Franco R., Canals M., Marcellino D., Ferre S., Agnati L., Mallol J., Casado V., Ciruela F., Fuxe K., Lluis C., Canela E. I. Regulation of heptaspanning-membrane-receptor function by dimerization and clustering // Trends Biochem. Sci. - 2003. - Vol. 28. - P. 238-243.
- Franco R., Casado V., Cortes A., Mallol J., Ciruela F., Ferre S., Lluis C., Canela E. I. G-protein-coupled receptor heteromers: function and ligand pharmacology // Brit. J.of Pharm. - 2008. - Vol. 153. - P. S90-S98.
- Terrilon D., Bouvier M. Role of G-protein-coupled receptor dimerization // EMBO. - 2004. - Vol. 5. - P. 30-34.
- Bulenger S., Marullo S., Bouvier M. Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation // Trends Pharmacol. Sci. - 2005. - Vol. 26, N 3. - P. 131-137.
- Prinster S. C., Hague C., Hall R. A. Heterodimerization of g protein-coupled receptors: specificity and functional significance // Pharmacol. Rev. - 2005. - Vol. 57. - P. 289-298.
- Rios C., Gomes I., Devi L. A. mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis // Br. J. Pharmacol. - 2006. - Vol. 148, N 4. - P. 387-395.
- Milligan G. G-protein-coupled receptor heterodimers: pharmacology, function and relevance to drug discovery // Drug Discov. Today. - 2006. - Vol. 11. N 11-12. - P. 541-549.
- Milligan G. G protein-coupled receptor dimerisation: molecular basis and relevance to function // Biochim. Biophys. Acta. - 2007. - Vol. 1768, N 4. - P. 825-35.
- Milligan G. G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function // Br. J. Pharmacol. - 2009. - Vol. 158, N 1. - P. 5-14.
- Milligan G., Kostenis E. Heterotrimeric G-proteins: a short history // Br. J. Pharmac. - 2006, 147 (Suppl. 1). - P. S46-55.
- Herrick-Davis K., Grinde E, Weaver B. A. Serotonin 5-HT (2C) receptor homodimerization is not regulated by agonist or inverse agonist treatment // Eur. J. Pharmacol. - 2007. - Vol. 568, N 1-3. - P. 45-53.
- Pin J., Neubig R., Bouvier M., Devi L., Filizola M., Javitch J. A. International union of basic and clinical pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers // Pharmacol. Rev. - 2007. - Vol. 59. - P. 5-13.
- Casadó V., Ferrada C., Bonaventura J., Gracia E., Mallol J., Canela E. I., Lluís C., Cortés A., Franco R. Useful pharmacological parameters for G-protein-coupled receptor homodimers obtained from competition experiments. Agonist-antagonist binding modulation // Biochem. Pharmacol. - 2009. - Vol. 78, N 12. - P. 1456-63.
- Franco R., Casadó V., Mallol J., Ferrada C., Ferré S., Fuxe K., Cortés A., Ciruela F., Lluis C., Canela E. I. The two-state dimer receptor model: a general model for receptor dimers // Mol. Pharmacol. - 2006. - Vol. 69, N 6. - P. 1905-1912.
- Fuxe K., Agnati L. F., Benfenati F., Celani M., Zini I., Zoli M., Mutt V. Evidence for the existence of receptor-receptor interactions in the central nervous system. Studies on the regulation of monoamine receptors by neuropeptides // J. Neural. Transm. Suppl. 1983. - Vol. 18. - P. 165-179.
- Avissar S., Amitai G., Sokolovsky M. Oligomeric structure of muscarinic receptors is shown by photoaffinity labeling: subunit assembly may explain high- and low-affinity agonist states // Proc. Natl. Acad. Sci. USA. 1983. - Vol. 80. - P. 156-159.
- Ng G. Y., George S. R. Dopamine receptor agonist reduces ethanol self-administration in the ethanol-preferring C57BL/6J inbred mouse // Eur. J. Pharmacol. 1994. - Vol. 15. - P. 365-374.
- Ciruela F., Casadó V., Mallol J., Canela E. I., Lluis C., Franco R. Immunological identification of A1 adenosine receptors in brain cortex // J. Neurosci. Res. 1995. - Vol. 42. - P. 818-828.
- George S. R., Fan T., Xie Z., Tse R., Tam V., Varghese G., O'Dowd B. F. Oligomerization of mu- and delta-opioid receptors. Generation of novel functional properties // J. Biol. Chem. - 2000. - Vol. 275. - P. 26128-26135.
- Milligan G., White J. H. Protein-protein interactions at G-protein-coupled receptors // Trends. Pharmacol. Sci. - 2001. - Vol. 22. - P. 513-518.
- Levac B. A., O'Dowd B. F., George S. R. Oligomerization of opioid receptors: generation of novel signaling units // Curr. Opin. Pharmacol. - 2002. - Vol. 2. - P. 76-81.
- Bai M. Dimerization of G-protein-coupled receptors: roles in signal transduction // Cell. Signal. - 2004. - Vol. 16. - P. 175-186.
- Lee F. J., Liu F. Direct interactions between NMDA and D1 receptors: a tale of tails // Biochem So. Trans. - 2004. - Vol. 32, N 6. - P. 1032-1036.
- Urizar E., Montanelli L., Loy T., Bonomi M., Swillens S., Gales C., Bouvier M., Smits G., Vassart G., Costagliola S. Glycoprotein hormone receptors: link between receptor homodimerization and negative cooperativity // EMBO (Eur. Mol. Biol. Organ.) J. - 2005. - Vol. 24, N 11. - P. 1954-1964.
- Ciruela F., Casadó V., Rodrigues R. J., Luján R., Burgueño J., Canals M., Borycz J., Rebola N., Goldberg S. R., Mallol J., Cortés A., Canela E. I., López-Giménez J. F., Milligan G., Lluis C., Cunha R. A., Ferré S., Franco R. Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromers // J. Neurosci. - 2006. - Vol. 26, N 7. - P. 2080-2087.
- Rashid A. J., So C. H., Kong M. M., Furtak T., El-Ghundi M., Cheng R., O'Dowd B. F., George S. R. D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum // Proc. Natl. Acad. Sci. USA. - 2007. - Vol. 104. - P. 654-659.
- Ferré S., Ciruela F., Quiroz C., Luján R., Popoli P., Cunha R. A., Agnati L.F, Fuxe K., Woods A. S., Lluis C., Franco R. Adenosine receptor heteromers and their integrative role in striatal function // Scientific. World. Journal. - 2007. - Vol. 7. - P. 74-85.
- Rozenfeld R., Devi L. A. Receptor heteromerization leads to a switch in signaling: β-arrestin2-mediated ERK activation by µ-δ opioid receptor heterodimers // FASEB J. - 2007. - Vol. 21, N 10. - P. 2455-2465.
- Marcellino D., Ferré S., Casadó V., Cortés A., Le Foll B., Mazzola C., Drago F., Saur O., Stark H., Soriano A., Barnes C., Goldberg S. R., Lluis C., Fuxe K., Franco R. Identification of dopamine D1-D3 receptor heteromers. Indications for a role of synergistic D1-D3 receptor interactions in the striatum // J. Biol. Chem. - 2008. - Vol. 283, N 38. - P. 26016-26025.
- Agnati L. F., Fuxe K., Ferre S. How receptor mosaics decode transmitter signals. Possible relevance of cooperativity // Trends Bichem. Sci. - 2005. - Vol. 30. - P. 188-193.
- De Meyts P., Roth J., Neville D. M., Gavin J. R., Lesniak M. A. Insulin interactions with its receptors: experimental evidence for negative cooperativity // Biochem. Biophys. Res. Commun. 1973. - Vol. 55. - P. 154-161.
- Limbird L. E., Meyts P. D., Lefkowitz R. J. Beta-adrenergic receptors: evidence for negative cooperativity // Biochem. Biophys. Res. Com. 1973. - Vol. 64. - P. 1160-1168.
- Casadó V., Cortés A., Ciruela F., Mallol J., Ferré S., Lluis C., Canela E. I., Franco R. Old and new ways to calculate the affinity of agonists and antagonists interacting with G-protein-coupled monomeric and dimeric receptors: the receptor-dimer cooperativity index // Pharmacol. Ther. - 2007. - Vol. 116, N 3. - P. 343-354.
- Franco R., Casado V., Cortes A., Mallol J., Ciruela F., Ferre S., Lluis C., Canela E. I. G-protein-coupled receptor heteromers: function and ligand pharmacology // Brit. J.of Pharm. - 2008. - Vol. 153. - P. S90-S98.
- Angers S. et al. Detection of beta 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET) // Proc. Natl. Acad. Sci. USA. - 2000. - Vol. 97. - P. 3684-3689.
- Mercier J. F., Salahpour A., Angers S., Breit A., Bouvier M. Quantitative assessment of beta 1-and beta 2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer // J. Biol. Chem. - 2002. - Vol. 277. - P. 44925-44931.
- Canals M., Marcellino D., Fanelli F., Ciruela F., de Benedetti P., Goldberg S. R., Neve K., Fuxe K., Agnati L. F., Woods A. S., Ferré S., Lluis C., Bouvier M., Franco R. Adenosine A2A-dopamine D2 receptor-receptor heteromerization: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer // J. Biol. Chem. - 2003. - Vol. 278, N 47. - P. 46741-46749.
- Fotiadis D. et al. Atomic-force microscopy: rhodopsin dimmers in native disc membranes // Nature. - 2003. - Vol. 421. - P. 127-128.
- Milliggan G., Bouvier M. Methods to monitor the quaternary structure of G protein-coupled receptors // FEBS J. - 2005. - Vol. 272. - P. 2914-2925.
- Pfleger K. D., Einde K. A. Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET) // Nat. Metods. - 2006. - Vol. 3. - P. 165-174.
- Dorsch S., Klotz K. N., Engelhardt S., Lohse M. J., Bunemann M. Analysis of receptor oligomeriszation by FRAP microscopy // Nature Methods. - 2009. - Vol. 6, N 3. - P. 225-230.
- Agnati L. F., Fuxe K., Zini I., Lenzi P., Hökfelt T. Aspects on receptor regulation and isoreceptor identification // Med. Biol. - 1980. - Vol. 58, N 4. - P. 182-187.
- Ferre S., von Euler G., Johansson B., Fredholm B. B., Fuxe K. Stimulation of high-affinity adenosine A2 receptors decreases the affinity of dopamine D2 receptors in rat striatal membranes // Proc. Natl. Acad. Sci. USA. - 1991. - Vol. 88, N 16. - P. 7238-7241.
- Ginés S., Hillion J., Torvinen M., Le Crom S., Casadó V., Canela E. I., Rondin S., Lew J. Y., Watson S., Zoli M., Agnati L. F., Verniera P., Lluis C., Ferré S., Fuxe K., Franco R. Dopamine D1 and adenosine A1 receptors form functionally interacting heteromeric complexes // Proc. Natl. Acad. Sci. USA. - 2000. - Vol. 7, N 15. - P. 8606-8611.
- Ferré S., Ciruela F., Canals M., Marcellino D., Burgueno J., Casadó V., Hillion J., Torvinen M., Fanelli F., Benedetti Pd. P., Goldberg S. R., Bouvier M., Fuxe K., Agnati L. F., Lluis C., Franco R., Woods A. Adenosine A2A-dopamine D2 receptor-receptor heteromers. Targets for neuro-psychiatric disorders // Parkinsonism Relat. Disord. - 2004. - Vol. 10, N 5. - P. 265-271.
- Soriano A., Ventura R., Molero A., Hoen R., Casado V., Cortés A., Fanelli F., Albericio F., Lluis C., Franco R., Royo M. Adenosine A (2A) Receptor-Antagonist/Dopamine D (2) Receptor-Agonist Bivalent Ligands as Pharmacological Tools to Detect A (2A)-D (2) Receptor Heteromers // J. Med. Chem. - 2009. Aug 27. [Epub. ahead of print].
- Franco R., Ferre S., Agnati L., Torvinen M., Gines S., Hillion J., Casado V., Lledo P., Zoli M., Lluis C., Fuxe K. Evidence for adenosine/dopamine receptor interactions: indication for heteromerization // Neuropsychopharmacology. - 2000. - Vol. 23. - P. S50-S59.
- Franco R., Lluis C., Canela E. I., Mallol J., Agnati L., Casadó V., Ciruela F., Ferré S., Fuxe K. Receptor-receptor interactions involving adenosine A1 or dopamine D1 receptors and accessory proteins // J. Neural. Transm. - 2007. - Vol. 114, N 1. - P. 93-104.
- Fuxe K., Ferré S., Canals M., Torvinen M., Terasma A., Marcellino D., Goldberg S. R., Staines W., Jacobsen K. X., Lluis C., Woods A. S., Agnati L. F., Franco R. Adenosine A2A and dopamine D2 heteromeric receptor complexes and their function // J. Mol. Neurosci. - 2005. - Vol. 26, N 2-3. - P. 209-220.
- Navarro G., Aymerich M. S., Marcellino D., Cortes A., Casado V., Mallol J., Canela E. I., Agnati L. F., Woods A. S., Fuxe K., Lluis C., Lanciego J. L., Ferre S., Franco R. Interactions between calmodulin, adenosine A2A and dopamine D2 receptors // J. Biol. Chem. - 2009, Jul 24 [Epub. ahead of print].
- Azdad K., Gall D., Woods A. S., Ledent C., Ferré S., Schiffmann S. N. Dopamine D2 and adenosine A2A receptors regulate NMDA-mediated excitation in accumbens neurons through A2A-D2 receptor heteromerization // Neuropsychopharmacology. - 2009. - Vol. 34, N 4. - P. 972-986.
- Fuxe K., Von Euler G., Agnati L. F., Pich E. M., O'Connor W. T., Tanganelli S., Li X. M., Tinner B., Cintra A., Carani C., Berfenati F. Intramembrane interactions between neurotensin receptors and dopamine D2 receptors as a major mechanism for the neuroleptic-like action of neurotensin // Ann. N. Y. Acad. Sci. 1992. - Vol. 668. - P. 186-204.
- Liu F., Wan Q., Pristupa Z. B., Yu X. M., Wang Y. T., Niznik H. B. Direct protein-protein coupling enables cross-talk between dopamine D5 and gamma-aminobutyric acid A receptors // Nature. - 2000. - Vol. 403, N 6767. - P. 274-280.
- Lee F. J., Wang Y. T., Liu F. Direct receptor cross-talk can mediate the modulation of excitatory and inhibitory neurotransmission by dopamine // J. Mol. Neurosci. - 2005. - Vol. 26, N 2-3. - P. 245-252.
- Zou S., Li L., Pei L., Vukusic B., Van Tol H. H., Lee F. J., Wan Q., Liu F. Protein-protein coupling/uncoupling enables dopamine D2 receptor regulation of AMPA receptor-mediated excitotoxicity // J. Neurosci. - 2005. - Vol. 25, N 17. - P. 4385-4395.
- Cabello N., Gandía J., Bertarelli D. C., Watanabe M., Lluís C., Franco R., Ferré S., Luján R., Ciruela F. Metabotropic glutamate type 5, dopamine D2 and adenosine A2a-receptors form higher-order oligomers in living cells // J. Neurochem. - 2009. - Vol. 109, N 5. - P. 1497-1507.
- Lee F. J., Xue S., Pei L., Vukusic B., Chéry N., Wang Y., Wang Y. T., Niznik H. B., Yu X. M., Liu F. Dual regulation of NMDA-receptor functions by direct protein-protein interactions with the dopamine D1 receptor // Cell. - 2002. - Vol. 111, N 2. - P. 219-230.
- Lee F. J., Liu F. Direct interactions between NMDA and D1 receptors: a tale of tails // Biochem So. Trans. - 2004. - Vol. 32, N 6. - P. 1032-1036.
- Salter M. W. D1 and NMDA receptors hook up: expanding on an emerging theme // Trends Neurosci. - 2003. - Vol. 26. - P. 235-237.
- Pei L., Lee F. J., Moszczynska A., Vukusic B., Liu F. Regulation of dopamine D1 receptor function by physical interaction with the NMDA receptors // J. Neurosci. - 2004. - Vol. 24, N 5. - P. 1149-1158.
- Liu X. Y., Chu X. P., Mao L. M. Modulation of D2R-NR2B interaction in response to cocaine // Neuron. - 2006. - Vol. 52. - P. 897-909.
- Missale C., Fiorentini C., Busi C., Collo G., Spano P. F. The NMDA/D1 receptor complex as new target in drug development // Curr. Top. Med. Chem. - 2006. - Vol. 6, N 8. - P. 801-808.
- Agnati L. F., Ferre S., Lluis C., Franco R., Fuxe K. Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons // Pharmacol. Rev. - 2003. - Vol. 55. - P. 509-550.
- Ferré S., Ciruela F., Quiroz C., Luján R., Popoli P., Cunha R. A., Agnati L.F, Fuxe K., Woods A. S., Lluis C., Franco R. Adenosine receptor heteromers and their integrative role in striatal function // Scientific. World. Journal. - 2007. - Vol. 7. - P. 74-85.
- Jordan B. A., Devi L. A. G-protein-coupled receptor heterodimerization modulates receptor function // Nature. 1999. - Vol. 399. - P. 697-700.
- George S. T., Fan T., Xie Z., Tse R., Tam V., Varghese G., O'Dowd B. F. Oligomerization of mu- and delta-opioid receptors. Generation of novel signaling units // J. Biol. Chem. - 2000. - Vol. 275. - P. 26128-26135.
- Levac B. A., O'Dowd B. F., George S. T. Oligomerization of opioid receptors: generation of novel signaling units // Curr. Opin. Pharmacol. - 2002. - Vol. 2. - P. 76-81.
- Gomes I., Gupta A., Filipovska J., Szeto H. H., Pintar J. E., Devi L. A. A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia // Proc. Natl. Acad. Sci. USA. - 2004. - Vol. 101. - P. 5135-5239.
- Gupta A., Decaillot F. M., Devi L. A. Targeting opioid receptor heterodimers: strategies for screening and drug development // AAPS J. - 2006. - Vol. 8. - P. E153-159.
- Vendrell M., Angulo E., Casadó V., Lluís C., Franco R., Albericio F. Novel ergopeptides as dual ligands for adenosine and dopamine receptors // J. Med. Chem. - 2007. - Vol. 50. - P. 3062-3069.
- Vendrell M., Soriano A., Casadó V., Díaz J. L., Lavilla R., Canela E. I., Lluís C., Franco R., Albericio F., Royo M. Indoloquinolizidine-peptide hybrids as multiple agonists for D1 and D2 dopamine receptors // J. Med. Chem. - 2009. - Vol. 4, N 9. - P. 1514-22.
- Waldhoer F., Fong J., Jones R. M., Lunzer M. M., Sharma S. K., Kostenis E., Portoghese P. S., Whistler J. L. A heterodimer-selective agonist shows in vivo relevance of G protein-coupled receptor dimers // Proc. Natl. Acad. Sci. U. S.A. - 2005. - Vol. 102. - P. 9050-9055.
- Franco R., Ferre S., Agnati L., Torvinen M., Gines S., Hillion J., Casado V., Lledo P., Zoli M., Lluis C., Fuxe K. Evidence for adenosine/dopamine receptor interactions: indication for heteromerization // Neuropsychopharmacology. - 2000. - Vol. 23. - P. S50-S59.
- Franco R., Casado V., Cortes A., Mallol J., Ciruela F., Ferre S., Lluis C., Canela E. I. G-protein-coupled receptor heteromers: function and ligand pharmacology // Brit. J.of Pharm. - 2008. - Vol. 153. - P. S90-S98.
- Yang C. R., Chen L. Targeting prefrontal cortical dopamine D1 and N-methyl-D-aspartate receptor interactions in schizophrenia treatment // Neuroscientist. - 2005. - Vol. 11, N 5. - P. 452-70.
- Букинич А. А., Шабанов П. Д. Новый подход к лечению наркологических и психических расстройств на основе принятия концепции прямого рецептор-рецепторного взаимодействия // Обз. по клин. фармакол. и лек. терапии. - 2013, Спецвыпуск. - Т. 11. - C. 26-28.
- Букинич А. А., Шабанов П. Д. Прямое рецептор-рецепторное взаимодействие - физиологическая основа психических и наркологических заболеваний // Экспериментальная и клиническая фармакология: научные чтения. Всерос. науч. конф. Рязань, 2013. - C. 33-39.
- Bukinich A. A., Shabanov P. D. A monomer/dimmer model of dopamine membrane receptors for pharmacological investigations // 26th ECNP Congr. Barcelona, Spain, 2013. Abstract CG13P-0127.
- Barreiro-Iglesias A., Villar-Cerviño V., Anadón R., et al. Descending brain-spinal cord projections in a primitive vertebrate, the lamprey: cerebrospinal fluid-contacting and dopaminergic neurons // J. Comp. Neurol. - 2008. - Vol. 511, N 6. - P. 711-723.
- Букинич А. А., Шабанов П. Д. (-)-Сульпирид - маркер выявления димерных рецепторов на мембранах нейронов ЦНС позвоночных // Экспериментальная и клиническая фармакология: научные чтения. Всерос. науч. конф. Рязань, 2013. - С. 39-42.
- Букинич А. А., Цветков Е. А., Веселкин Н. П. Особенности дофаминовых рецепторов на мембране мультиполярных нейронов спинного мозга пескоройки // Журнал эволюц. биохимии и физиологии. - 2007. - Т. 43, № 1. - С. 39-45.
- Букинич А. А., Шабанов П. Д. Новый маркер для выявления димерных рецепторов в нейронах ЦНС позвоночных // Обозр. психиатр. и мед. психол. им. В. М. Бехтерева. - 2014, прил. - С. 32-33.
- Franco, R., Casado, V., Cortes, A., Mallol, J., Ciruela, F., Ferre, S., Lluis, C., Canela, E. I. G-protein-coupled receptor heteromers: function and ligand pharmacology // Brit. J. Pharmacol. - 2008. - Vol. 153. - P. S90-S98.
- Casadó, V., Ferrada, C., Bonaventura, J., Gracia, E., Mallol, J., Canela, E. I., Lluís, C., Cortés, A., Franco, R. Useful pharmacological parameters for G-protein-coupled receptor homodimers obtained from competition experiments. Agonist-antagonist binding modulation // Biochem. Pharmacol. - 2009. - Vol. 78, N 12. - P. 1456-1463.
- Букинич А. А., Шабанов П. Д. Возможность образования гетеромерного комплекса между дофаминовыми и глютаматными рецепторами на мембранах ЦНС позвоночных // Экспериментальная и клиническая фармакология: научные чтения. Всерос. науч. конф. Рязань, 2013. - С. 43-44.
- Букинич А. А., Шабанов П. Д. Головной мозг человека работает в системе двоичного кода (гипотеза) // Обз. по клин. фармакол. и лек. терапии. - 2013. - Т. 11, № 2. - C. 52-56.
- Lanau, F., Zenner, M. T., Civelli, O., Hartman, D. S. Epinephrine and norepinephrine act as potent agonists at the recombinant human dopamine D4 receptor // J. Neurochem. - 1997. - Vol. 68, № 2. - P. 804-812.
- Bukinich A. A., Shabanov P. D. Dual code as a basis of the CNS activity // Eur. Neuropsychopharmacol. - 2014. Vol. - 24, Suppl. 2. - P. S215-216.

by Luis Hefner (12.09.2017)
by Alvina Amanda (24.10.2017)
by alice brant (26.10.2017)
by Wei Wang (26.10.2017)
by Dina Haines (03.11.2017)
by Steven Martin (08.11.2017)
by Lisa Amanda (15.11.2017)
by Billy Gun (06.12.2017)
by marsha kaplan (06.12.2017)
by Rob Schneider (07.12.2017)
by Robert Jack (08.12.2017)
by James Louis (08.12.2017)
by James Clarke (08.12.2017)
by Elizabeth David (21.12.2017)
by Elizabeth David (21.12.2017)
by Adam Milne (23.12.2017)
by maria denial (28.12.2017)
by Florence Eliza (28.12.2017)
by Amanda Leon (29.12.2017)
by Euricana Ciara (29.12.2017)
by Cristina aarora (29.12.2017)
by laura martin (01.01.2018)
by jonny blaze (01.01.2018)
by jhon smith (01.01.2018)
by Gracie Flora (01.01.2018)
by Deanna Williams (01.01.2018)
by Sharlyn Harville (02.01.2018)
by Jacob Arch (04.01.2018)
by Sara Canaday (10.01.2018)
by Anastasia Amanda (22.01.2018)
by Ainsley Alexavier (22.01.2018)
by Edward Peter (22.01.2018)
by Stephen Hawking (23.01.2018)
by Essay Avenue (23.01.2018)
by Stephen merchant (23.01.2018)
by Roy J. Fischer (24.01.2018)
by judee elliot (07.02.2018)
by Cerys Perry (01.03.2018)
by Emma Granger (12.03.2018)
by Edward Mark (12.03.2018)
by Edward Mark (13.03.2018)
by Amelia Hadlock (14.03.2018)
by Camila Lucas (21.03.2018)
by Bud Gerace (26.03.2018)
"Winchester Rokowich Winchester, Rokki" (06.04.2018)
"Winchester Rokowich Winchester, Rokki" (06.04.2018)
"Winchester Rokowich Winchester, Rokki" (06.04.2018)
"Winchester Rokowich Winchester, Rokki" (06.04.2018)
"Winchester Rokowich Winchester, Rokki" (06.04.2018)
by alma hernandez (14.04.2018)
by Glenn J. Davis (26.04.2018)
by Angela Ruther (03.05.2018)
by Lloyd Garvin (08.05.2018)
by judee elliot (08.05.2018)
by Rachelle Marie (18.05.2018)
by jason morgan (21.06.2018)
by hazal kaya (21.06.2018)
by Bo Cooley (02.07.2018)
by julia john (03.07.2018)
by cruz john (03.07.2018)
by Bo Cooley (03.07.2018)
by Bo Cooley (04.07.2018)
by Bo Cooley (04.07.2018)
by Robert Haney (06.07.2018)
by jose mabeaq (17.07.2018)
by John Hozy (24.07.2018)
by Evelyn Warner (05.09.2018)
by kathleen swafford (13.09.2018)
by roger flopple (13.09.2018)
by Emma Alex (13.09.2018)
by Levy Jeramiah (15.09.2018)
by Levy Jeramiah (15.09.2018)
by Levy Jeramiah (15.09.2018)
by kathleen swafford (19.09.2018)
by Britt Rogers (19.09.2018)
by Emma Alex (19.09.2018)
by Emma Alex (20.09.2018)
by Emma Alex (20.09.2018)
by Amber x Amber Byrne (10.10.2018)
by Rose Jacob (18.10.2018)
by alberd john (20.10.2018)
by Bo Cooley (27.11.2018)
by thomas jessica (27.12.2018)
by Amelia Stone (12.01.2019)
by Alexender Smith (08.02.2019)
by Daniel Lee (11.02.2019)
by thomas jessica (02.03.2019)
by Amanda Orleander (17.03.2019)
by gordon voren blue (24.03.2019)
"Bratbyt Bratbyt" (25.03.2019)
"dawntruetesas dawntruetesas" (04.04.2019)
by James Brown (16.04.2019)
by jack willaim (25.04.2019)
by Jill Cosner (29.04.2019)
by Kate Brouwn (03.05.2019)
"dawntruetesas dawntruetesas" (10.05.2019)
by Alexander Porkhun (30.05.2019)
by Lilia Ramsey (13.06.2019)
by angela jones (17.06.2019)
by angela jones (17.06.2019)
", DonavanDonavan Donavan" (19.06.2019)
by ABRAHAM KIMLEY (02.07.2019)
by ABRAHAM KIMLEY (02.07.2019)
by Francis Thomas (05.07.2019)
by Mehak Ali (10.07.2019)
by Komal Zain (10.07.2019)
by Alfred Allen (16.07.2019)
by Martin Joe (17.07.2019)
by alex Stanford (20.07.2019)
by alex Stanford (20.07.2019)
by alex Stanford (20.07.2019)
by Rosie Howard (06.08.2019)
by Jason Voorhees (29.08.2019)
by Denise Adams (03.09.2019)
by Victoria James (04.09.2019)
by alex Stanford (08.09.2019)
by Denice Phillips (08.09.2019)
by Lynn Raymundo (13.09.2019)
by Phil Danny (15.09.2019)
by Jason Voorhees (16.09.2019)
by Johnson Tom Rivers (24.09.2019)
by Johnson Tom Rivers (24.09.2019)
by erica fernandes (26.09.2019)
by Aliza Davis (30.09.2019)
by Jason Voorhees (20.10.2019)
by Amanda Orleander (09.11.2019)
by Jason Boo (21.11.2019)
by tara rubena (09.12.2019)
by Susan Webb (17.12.2019)
by Susan Webb (17.12.2019)
by Forever Fiances (20.12.2019)
by malan johnson (23.12.2019)
by apps twisty (23.12.2019)
by mitchel johnson (23.12.2019)
by Lena Smith (06.01.2020)
by Trista Manners (09.01.2020)
by Lara Harris (12.01.2020)
by Aisha perween (13.01.2020)
by pop achat (15.01.2020)
by Oliver Saanti (23.01.2020)
by Ethan Wood (24.01.2020)
by Emma Flores (02.02.2020)
by Export Hub (03.02.2020)
by Dennis Smith (06.02.2020)
by Mason Dillon (10.02.2020)
by Tony Logan (13.02.2020)
by Linda Ween (17.02.2020)
by Emma Din Sin (17.02.2020)
by Emma Din Sin (17.02.2020)
by blogger jaan (26.02.2020)
by leah melda (26.02.2020)
by Mikki Grow (06.03.2020)
by Jamie anderson (20.03.2020)
by berenice aldway (18.04.2020)
by Emma Velson (10.05.2020)
by kevin bear (19.05.2020)
by Kevin Peterson (21.05.2020)
by Kevin Peterson (21.05.2020)
by Tami mayer (22.05.2020)
by waheed murad sheikh (23.05.2020)
by waheed murad sheikh (23.05.2020)
by waheed murad sheikh (23.05.2020)
by Allan Pross (25.05.2020)
by Fred Meadors (29.05.2020)
by mitchel johnson (01.06.2020)
by Monika Jacob (03.06.2020)
by Stevin Cod (03.06.2020)
by Kevin Dot (03.06.2020)
by Kevin Cod (05.06.2020)
by Kevin Peterson (06.06.2020)
by Tami mayer (09.06.2020)
by Tami mayer (09.06.2020)
by james evers (13.06.2020)
by Tony Logan (15.06.2020)
by Erika Rewlon (16.06.2020)
by Wayne Dietz (23.06.2020)
by Linda Ween (15.07.2020)
by OkeJoker Situs Bandar Judi Slot Online Deposit Pulsa Terpercaya (20.07.2020)
by Serenity Reid (23.07.2020)
by Andrew John Snow (31.07.2020)
by Andrew John Snow (31.07.2020)
by Harry Oliver (12.08.2020)
by mina yang (17.08.2020)
by shaun alan (17.08.2020)
by Manoj Patel (20.08.2020)
by Peter Blakes (25.08.2020)
by Colin Boven (02.09.2020)
by Colin Boven (02.09.2020)
by Colin Boven (02.09.2020)
by Fred Wells (02.09.2020)
by Fred Wells (02.09.2020)
by Fred Wells (02.09.2020)
by Simon James (03.09.2020)
by Jonny Steve (08.09.2020)
by Tim Woods (08.09.2020)
by Jack Henry (10.09.2020)
by Jonny Steve (15.09.2020)
by sheikh uddin (18.09.2020)
by joly kormath (19.09.2020)
by James Cooper (21.09.2020)
by Jack Black (23.09.2020)
by James Vince (24.09.2020)
"haven haven" (28.09.2020)
by Susan Penson (01.10.2020)
by coinprice iq (08.10.2020)
by Emma Moore (09.10.2020)
by Deepak Sood (15.10.2020)
by Karen Hill (16.10.2020)
by Karen Hill (16.10.2020)
by Andrew Mark (19.10.2020)
by james oliver (31.10.2020)
by james oliver (31.10.2020)
by Justin Lake (31.10.2020)
by Millie Palmer (06.11.2020)
by Victor Bradford (07.11.2020)
by Hassaan khan (10.11.2020)
by Hassaan khan (10.11.2020)
by bean ter8 (12.11.2020)
by Brenda John (12.11.2020)
by Robert Cooper (13.11.2020)
by Bryon Thomas (13.11.2020)
"Dattong Dattong" (18.11.2020)
by Logan Smith (19.11.2020)
by Junaid Khan (19.11.2020)
by Phill Wagner (24.11.2020)
by Trisha Pitt (25.11.2020)
by James Polson (02.12.2020)
by James K Stiller (03.12.2020)
by James K Stiller (03.12.2020)
by James K Stiller (03.12.2020)
by Dorothy Nicholson (07.12.2020)
by Christie Brown (07.12.2020)
by jazz 2204 2204 (09.12.2020)
by jazz 2204 2204 (09.12.2020)
by jazz 2204 2204 (09.12.2020)
by Jack Stephens (10.12.2020)
by kevin bear (11.12.2020)
by Malena Morgan (11.12.2020)
by Nic Picalato (12.12.2020)
by Linda Ween (15.12.2020)
by Ian Rowe (17.12.2020)
by James K Stiller (24.12.2020)
by James K Stiller (24.12.2020)
by Emilia Cod (24.12.2020)
by Kelly Rise (24.12.2020)
"adessive adessive" (27.12.2020)
by Angelica Gill (27.12.2020)
by Social Media Marketing Services (30.12.2020)
by Brayden LIN (30.12.2020)
by Christie Brown (04.01.2021)
by Ada Hall (05.01.2021)
by Albert B Bova (09.01.2021)
by Theo Smith (12.01.2021)
by Jack Stephens (14.01.2021)
by John Fazio (22.01.2021)
by Eshley Durst (23.01.2021)
by James William (25.01.2021)
by Bebas B Bnana (26.01.2021)
by Jack Stephens (28.01.2021)
by canon printer (30.01.2021)
by Helen D Matteo (31.01.2021)
by Bebas Bnana (07.02.2021)
by Jaylee Keck (17.02.2021)
by Atif Ivacy (17.02.2021)
by Albert Bova (20.02.2021)
by Stive Morris (23.02.2021)
by Lola Nickson (01.03.2021)
by Lovely Alberto (02.03.2021)
by Anna Moore (02.03.2021)
by Martin Banett (10.03.2021)
by Patricia Lambert (10.03.2021)
by mark movie222 (14.03.2021)
by Stive Morris (15.03.2021)
by David Wong (15.03.2021)
by Robert Cooper (23.03.2021)
by Games 4U (26.03.2021)
by Klais Last (06.04.2021)
by kerry cooper (13.04.2021)
by jazz 2204 2204 (14.04.2021)
by jazz 2204 2204 (17.04.2021)
by John Writer (21.04.2021)
by Christie Brown (23.04.2021)
by Sarah James (23.04.2021)
by Baldu King Bai (28.04.2021)
by Emilia Cod (30.04.2021)
by Vivienne Norton (05.05.2021)
by Christie Brown (19.05.2021)
by James Nick (19.05.2021)
by Malena Morgan (19.05.2021)
by Gregor Brown (21.05.2021)
by Hasten Cleanse (24.05.2021)
by laura howard (24.05.2021)
by Dustin Hunt (27.05.2021)
by Stephanie Anna (29.05.2021)
by Lola Nickson (01.06.2021)
by Devid Miller (09.06.2021)
by cricn score1 (09.06.2021)
by Izhar Korejo (10.06.2021)
by Ryan Harvey (14.06.2021)
by sara tores (18.06.2021)
by Alex jason (22.06.2021)
by Anna Luss (29.06.2021)
by Mary Ross (30.06.2021)
by Mildred D. Brown (03.07.2021)
by Fannie Davis (05.07.2021)
by Fannie Davis (05.07.2021)
by Fannie Davis (05.07.2021)
by Fannie Davis (05.07.2021)
by jang dong (09.07.2021)
by James Nick (14.07.2021)
by Disability Dream Date (15.07.2021)
by creative hatti (19.07.2021)
by Valeriy Brumov (27.07.2021)
by Sarah James (11.08.2021)
by Hanna Cooper (17.08.2021)
by Get reviews buzz (25.08.2021)
by Lily Johnson (25.08.2021)
by Manoj Bhatt (04.09.2021)
by Get Reviews Buzz (07.09.2021)
by Local Seo Buzz (09.09.2021)
by Craig Andersen (09.09.2021)
by Kate Backer (10.09.2021)
by stream line myrei (13.09.2021)
by stream line myrei (13.09.2021)
by stream line myrei (13.09.2021)
by Lauren Walker (16.09.2021)
by lucille mcmahan (17.09.2021)
by elizabet roos (21.09.2021)
by deni charlotte (21.09.2021)
by deni charlotte (21.09.2021)
by Arianna Palmer (23.09.2021)
by Mona Sharma (28.09.2021)
by Mona Sharma (28.09.2021)
by ibrahim ira (05.10.2021)
by ruth riordan (13.10.2021)
by Marina Petrenko (15.10.2021)
by stand sm mixer (20.10.2021)
by sajjad sajjad ali (21.10.2021)
by stand sm mixer (22.10.2021)
by coaching in kenya (23.10.2021)
by sajjad sajjad ali (23.10.2021)
by stand sm mixer (23.10.2021)
by Jay Richie (28.10.2021)
by umar farooq (01.11.2021)
by William Smith (03.11.2021)
by military drummer jacket (13.11.2021)
by Mona kell (19.11.2021)
by Cierra Fox (25.11.2021)
by color man (26.11.2021)
by thisis kate winslet (29.11.2021)
by thisis kate winslet (29.11.2021)
by thisis kate winslet (29.11.2021)
by candy candymika mika (29.11.2021)
by Olivia James (01.12.2021)
by sajjad sajjad ali (03.12.2021)
by stand sm mixer (05.12.2021)
by Connie Zapata (06.12.2021)
by stevie martin (08.12.2021)
by Fay Anabelle (08.12.2021)
by Frederick Carter (09.12.2021)
by Mark Andy (09.12.2021)
by olivila jhon (24.12.2021)
by jasmine wiltor (27.12.2021)
by jasmine wiltor (27.12.2021)
by james pattinson (27.12.2021)
by james pattinson (27.12.2021)
by Fay Anabelle (16.01.2022)
by Roger Adams (18.01.2022)
by Jake Lambe (24.01.2022)
by Seha Garden (02.02.2022)
by Vlone Hub (08.02.2022)
by Vlone Hub (08.02.2022)
by stand sm mixer (19.02.2022)
by Charles Mc McCarthy (26.02.2022)
by steve davis (01.03.2022)
by Maxus Maxus van van (02.03.2022)
by James Dutchson (03.03.2022)
by Kimberly Scott (03.03.2022)
by sajjad sajjad ali (03.03.2022)
by android development android development ireland ireland (05.03.2022)
by sajjad sajjad ali (08.03.2022)
by sajjad sajjad ali (16.03.2022)
by Dean Warren (18.03.2022)
by sajjad sajjad ali (21.03.2022)
by Salena Jack (30.03.2022)
by Salena Jack (30.03.2022)
by Roger Adams (31.03.2022)
by Megan Fox (02.04.2022)
by David Marco (06.04.2022)
by olivila jhon (06.04.2022)
by Daniel Scott (18.04.2022)
by Daniel Scott (02.05.2022)
by Daniel Scott (02.05.2022)
by Daniel Scott (02.05.2022)
by Ruth Adam (03.05.2022)
by Austin Frank (03.05.2022)
by Mario Shaw (03.05.2022)
by Dona Brown (03.05.2022)
by hilary cory (12.05.2022)
by Thomas Rhett (13.05.2022)
by Lara Logan (14.05.2022)
by mccarty torres (16.05.2022)
by charles trevino (16.05.2022)
by Mike James (06.06.2022)
by Kevin hawks (06.06.2022)
by David Hug (06.06.2022)
by Mo Martin (08.06.2022)
by Mo Martin (08.06.2022)
by Daniel Scott (08.06.2022)
by Discover Mongolian Altai (26.06.2022)
by James William (30.06.2022)
by John Michael (04.07.2022)
by Philip Collin (05.07.2022)
by remorquage auto auto (05.07.2022)
by Elvia Shan (21.07.2022)
by Joe Wilson (21.07.2022)
by Holly Dorey (23.07.2022)
by Vlone Hub (27.07.2022)
by Vlone Hub (27.07.2022)
by Bhpesh kumar (31.07.2022)
by Jennifer Parker (04.08.2022)
by EMMO oliva oli (19.08.2022)
by Daniel Scott (29.08.2022)
by Explendid videos (01.09.2022)
by App Maestros (01.09.2022)
by Dionne Jenner (05.09.2022)
by Capstar Fx (05.09.2022)
by Capstar Fx (05.09.2022)
by David Rose (11.10.2022)
by Andrew Lopez Lopez (12.10.2022)
by Bailey Patterson Bailey (14.10.2022)
by Bailey Patterson Bailey (14.10.2022)
by British Dissertation Help (28.10.2022)
by Alisha Kihn (31.10.2022)
by james swanson (31.10.2022)
by James Harden (02.11.2022)
by jiho uni (10.11.2022)
by justinfowler fowler fowler (19.11.2022)
by Skyman Mentalist (21.11.2022)
by chan vova (28.11.2022)
by Kathryn Haney (29.11.2022)
by Kathryn Haney (29.11.2022)
by alexander 1357 (10.12.2022)
by Made Made line line (28.12.2022)
by Tudor Sebastian (10.01.2023)
by Nekopoi APK (12.01.2023)
by Lora Jhon (13.01.2023)
by Lora Jhon (13.01.2023)
by Santos Bogisich (19.01.2023)
by Lora Jhon (28.01.2023)