Functional role of dimer (heteromer) receptors in the CNS of mammalians

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

  1. Bouvier M. Oligomerization of G-protein-coupled transmitter receptors // Nat. Rev. Neurosci. - 2001. - Vol. 2. - P. 274-286.
  2. Devi L. A. Heterodimerization of G-protein-coupled receptors: pharmacology, signaling and trafficking // Trends Pharmacol. Sci. - 2001. - Vol. 22, N. 10. - P. 532-537.
  3. Marshall F. H. Heterodimerization of G-protein-coupled receptors in the CNS // Curr. Opin. Pharmacol. - 2001. - Vol. 1. - P. 40-44.
  4. 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.
  5. 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.
  6. 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.
  7. 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.
  8. 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.
  9. 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.
  10. Terrilon D., Bouvier M. Role of G-protein-coupled receptor dimerization // EMBO. - 2004. - Vol. 5. - P. 30-34.
  11. 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.
  12. 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.
  13. 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.
  14. 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.
  15. Milligan G. G protein-coupled receptor dimerisation: molecular basis and relevance to function // Biochim. Biophys. Acta. - 2007. - Vol. 1768, N 4. - P. 825-35.
  16. Milligan G. G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function // Br. J. Pharmacol. - 2009. - Vol. 158, N 1. - P. 5-14.
  17. Milligan G., Kostenis E. Heterotrimeric G-proteins: a short history // Br. J. Pharmac. - 2006, 147 (Suppl. 1). - P. S46-55.
  18. 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.
  19. 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.
  20. 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.
  21. 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.
  22. 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.
  23. 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.
  24. 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.
  25. 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.
  26. 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.
  27. Milligan G., White J. H. Protein-protein interactions at G-protein-coupled receptors // Trends. Pharmacol. Sci. - 2001. - Vol. 22. - P. 513-518.
  28. 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.
  29. Bai M. Dimerization of G-protein-coupled receptors: roles in signal transduction // Cell. Signal. - 2004. - Vol. 16. - P. 175-186.
  30. 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.
  31. 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.
  32. 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.
  33. 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.
  34. 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.
  35. 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.
  36. 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.
  37. 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.
  38. 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.
  39. 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.
  40. 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.
  41. 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.
  42. 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.
  43. 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.
  44. 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.
  45. Fotiadis D. et al. Atomic-force microscopy: rhodopsin dimmers in native disc membranes // Nature. - 2003. - Vol. 421. - P. 127-128.
  46. Milliggan G., Bouvier M. Methods to monitor the quaternary structure of G protein-coupled receptors // FEBS J. - 2005. - Vol. 272. - P. 2914-2925.
  47. 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.
  48. 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.
  49. 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.
  50. 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.
  51. 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.
  52. 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.
  53. 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].
  54. 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.
  55. 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.
  56. 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.
  57. 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].
  58. 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.
  59. 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.
  60. 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.
  61. 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.
  62. 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.
  63. 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.
  64. 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.
  65. 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.
  66. Salter M. W. D1 and NMDA receptors hook up: expanding on an emerging theme // Trends Neurosci. - 2003. - Vol. 26. - P. 235-237.
  67. 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.
  68. 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.
  69. 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.
  70. 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.
  71. 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.
  72. Jordan B. A., Devi L. A. G-protein-coupled receptor heterodimerization modulates receptor function // Nature. 1999. - Vol. 399. - P. 697-700.
  73. 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.
  74. 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.
  75. 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.
  76. 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.
  77. 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.
  78. 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.
  79. 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.
  80. 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.
  81. 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.
  82. 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.
  83. 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.
  84. 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.
  85. 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.
  86. 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.
  87. 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.
  88. 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.
  89. 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.
  90. 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.
  91. 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.
  92. 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.
  93. 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.
  94. 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.
  95. 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.

Statistics

Views

Abstract - 1148

PDF (Russian) - 330

Cited-By


Article Metrics

Metrics Loading ...

PlumX

Dimensions

Comments on this article

Comments on this article

View all comments

Copyright (c) 2015 Bukinich A.A., Shabanov P.D.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies