Integrative action of receptor mosaics: Relevance of receptor topology and allosteric modulators

Journal of Receptors and Signal Transduction

Volumn 28, Issue 6, 2008, Pages 543-565

  Francesco, Agnati Luigi ^a   Diego, Guidolin ^b   Susanna, Genedani ^a   Giuseppina, Leo ^a   Amina, Woods S ^c   Sergi, Ferrè ^c   Rafael, Franco ^d   Kjell, Fuxe ^e  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Allosteric modulators; Homocysteine; Receptor mosaics; Receptor topology

Indexed keywords

ADENOSINE A2A RECEPTOR; DOPAMINE 2 RECEPTOR; HETERODIMER; HOMOCYSTEINE;

ALLOSTERISM; ARTICLE; CELL MEMBRANE; MENTAL DISEASE; MICROENVIRONMENT; NEUROLOGIC DISEASE; NEUROPSYCHIATRY; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ALLOSTERIC REGULATION; ANIMALS; CELL MEMBRANE; HUMANS; MEMBRANE MICRODOMAINS; MODELS, THEORETICAL; RECEPTOR CROSS-TALK; RECEPTORS, CELL SURFACE;

EID: 58149085559     PISSN: 10799893     EISSN: 15324281     Source Type: Journal    
DOI: 10.1080/10799890802590420     Document Type: Article

References (77)

1. Fuxe K, Agnati LF. Receptor-Receptor Interactions. A New Intramembrane Integrative Mechanism. London, MacMillan, 1987.
2. Agnati LF, Ferré S, Lluis C, Franco R, Fuxe K. Molecular mechanisms and therapeutical implications of intramembrane receptor / receptor interactions among heptahelical receptors with examples from the striopallidal GABA neurons. Pharm Rev 2003, 55, 509-550.
3. Fuxe K, Agnati LF, Härfstrand A, Janson AM, Neumeyer A, Andersson K, Ruggeri M, Zoli M, Goldstein M. Morphofunctional studies on the neuropeptide Y/adrenaline costoring terminal systems in the dorsal cardiovascular region of the medulla oblongata. Focus on receptor-receptor interactions in cotransmission. Prog Brain Res 1986, 68, 303-320.
4. Agnati LF, Fuxe K, Giardino L, Calza L, Zoli M, Battistini N, Benfenati F, Vanderhaeghen JJ, Guidolin D, Ruggeri M. Evidence for cholecystokinin- dopamine receptor interactions in the central nervous system of the adult and old rat. Studies on their functional meaning. Ann N Y Acad Sci 1985, 448, 315-333.
5. Fuxe K, Agnati LF, Härfstrand A, Martire M, Goldstein M, Grimaldi R, Bernardi P, Zini I, Tatemoto K, Mutt V. Evidence for a modulation by neuropeptide Y of the alpha-2 adrenergic transmission line in central adrenaline synapses. New possibilities for treatment of hypertensive disorders. Clin Exp Hypertens A 1984, 6, 1951-1956.
6. Fuxe K, Agnati LF, Härfstrand A, Zini I, Tatemoto K, Pich EM, Hökfelt T, Mutt V, Terenius L. Central administration of neuropeptide Y induces hypotension bradypnea and EEG synchronization in the rat. Acta Physiol Scand 1983, 118, 189-192.
7. Agnati LF, Fuxe K, Benfenati F, Battistini N, Härfstrand A, Hökfelt T, Cavicchioli L, Tatemoto K, Mutt V. Failure of neuropeptide Y in vitro to increase the number of alpha 2-adrenergic binding sites inmembranes of medulla oblongata of the spontaneous hypertensive rat. Acta Physiol Scand 1983, 119, 3009-3012.
8. Fuxe K, Agnati LF, 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, 18, 165-179.
9. Agnati LF, Fuxe K, Benfenati F, Battistini N. Neurotensin in vitro markedly reduces the affinity in subcortical limbic 3H-N-propylnorapomorphine binding sites. Acta Physiol Scand 1983, 119, 459-461.
10. Fuxe K, Agnati LF, Benfenati F, Cimmino M, Algeri S, Hökfelt T, Mutt V. Modulation by cholecystokinins of 3H-spiroperidol binding in rat striatum: Evidence for increased affinity and reduction in the number of binding sites. Acta Physiol Scand 1981, 113, 567-569.
11. Agnati LF, Fuxe K, Zini I, Lenzi P, Hökfelt T. Aspects on receptor regulation and isoreceptor identification. Med Biol 1980, 58, 182-187.
12. Agnati LF, Fuxe K, Zoli M, Rondanini C, Ögren S-O. New vistas on synaptic plasticity: The receptor mosaic hypothesis of the engram. Med Biol 1982, 60, 183-190.
13. Agnati LF, Franzen O, Ferrë S, Leo G, Franco R, Fuxe K. Possibile role of intramembrane receptor-receptor interactions in memory and learning via formation of long-lived heteromeric complexes: Focus on motor learning in the basal ganglia. J Neural Transm 2003, 65, 195-222.
14. Agnati LF, Ferrë S, Leo G, Lluis C, Canela EI, Franco R, Fuxe K. On the molecular basis of the receptor mosaic hypothesis of the engram. J Mol Cell Neurobiol 2004, 24, 501-516.
15. Fuxe K, Canals M, Torvinen M, Marcellino D, Terasmaa A, Genedani S, Leo G, Guidolin D, Diaz-Cabiale Z, Rivera A, Lundstrom L, Langel U, Narvaez J, Tanganelli S, Lluis C, Ferrë S, Woods A, Franco R, Agnati LF. Intramembrane receptor-receptor interactions: A novel principle in molecular medicine. J Neural Transm 2007, 114, 49-75.
16. Zoli M, Guidolin D, Fuxe K, Agnati LF. The receptor mosaic hypothesis of the engram: Possible relevance of boolean network modeling. Int J Neur Syst 1996, 7, 363-368.
17. Agnati LF, Fuxe K, Ferre S. How receptor mosaics decode transmitter signals. Possible relevance of cooperativity. Trends Biochem Sci 2005, 30, 188-193.
18. Agnati LF, Guidolin D, Genedani S, Ferrë S, Bigiani A, Woods A, Fuxe K. How proteins come together in the plasma membrane and function in macromolecular assemblies: Focus on receptor mosaics. J Mol Neurosci 2005, 26, 133-154.
19. Guidolin D, Fuxe K, Neri G, Nussdorfer GG, Agnati LF. On the role of receptorreceptor interactions and volume transmission in learning and memory. Brain Res Rev 2007, 119-133.
20. Canals M, Marcellino D, Fanelli F, Ciruela F, de Benedetti P, Goldberg SR, Neve K, Fuxe K, Agnati LF, Woods AS, Ferrë 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, 278, 46741-46749.
21. Canals M, Burgueño J, Marcellino D, Cabello N, Canela EI, Mallol J, Agnati L, Ferré S, Bouvier M, Fuxe K, Ciruela F, Lluis C, Franco R. Homodimerization of adenosine A2A receptors: Qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer. J Neurochem 2004, 88, 726-734.
22. Gozes I. Receptor-receptor interctions among heptaspanning membrane receptors: From structure to function. J Mol Neurosci 2005, 26(2-3).
23. Franco R, Lluis C, Canela EI, 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, 114, 93-104.
24. Woods AS. The mighty arginine, the stable quaternary amines, the powerful aromatics and the aggressive phosphate: Their role in the noncovalent minuet. J Proteome Res 2004, 3, 478-484.
25. Woods AS, Ferre S. The amazing stability of the arginine-phosphate electrostatic interaction. J Proteome Res 2005, 4, 1397-1402.
26. Woods AS, Ciruela F, Fuxe K, Agnati LF, Lluis C, Franco R, Ferré S. The role of electrostatic interaction in receptor-receptor heteromerization. J Mol Neurosci 2005, 26, 125-132.
27. Ciruela F, Burgueño J, Casadó V, Canals M, Marcellino D, Goldberg SR, Bader M, Fuxe K, Agnati LF, Lluis C, Franco R, Ferré S, Woods AS. Combining mass spectrometry and pull-down techniques for the study of receptor heteromerization. Direct epitope-epitope electrostatic interactions between adenosine A2A and dopamine D2 receptors. Anal Chem 2004, 76, 5354-5363.
28. Carriba P, Navarro G, Ciruela F, Ferré S, Casadó V, Agnati L, Cortés A, Mallol J, Fuxe K, Canela EI, Lluís C, Franco R. Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat Methods 2008, 5, 727-733.
29. Agnati LF, Zoli M, Merlo Pich E, Benfenati F, Fuxe K. Aspects of neural plasticity in the central nervous system. VII. Theoretical aspects of brain communication and computation. Neurochem Int 1990, 16, 479-500.
30. Agnati LF, Santarossa L, Benfenati F, Ferri M, Morpurgo A, Apolloni B, Fuxe K. Molecular basis of learning and memory: modelling based on receptor mosaics. In: Apolloni B, Kurfes F, Eds. From Synapses to Rules. New York, Academic/Plenum Publishers, 2002, 165-196.
31. Simons K, Vaz WL. Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 2004, 33, 269-295.
32. Okamoto T, Schlegel A, Scherer PE, Lisanti MP. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem1998, 273, 5419-5422.
33. Milligan G, Smith NJ. Allosteric modulation of heterodimeric G-protein-coupled receptors. Trends Pharmacol Sci 2007, 28, 615-620.
34. Marshall FH. Is the GABA B heterodimer a good drug target? J Mol Neurosci 2005, 26, 169-176.
35. Agnati LF, Santarossa L, Genedani S, Canela EI, Leo G, Franco R, Woods A, Lluis C, Ferrè S, Fuxe K. On the nested hierarchical organization of CNS: Basic characteristics of neuronal molecular networks. In: Erdi P, Esposito A, Marinaro M, Scarpetta S, Eds. Computational Neuroscience: Cortical Dynamycs, Lecture Notes in Computer Sciences. Berlin Heidelberg New York, Springer, 2004, 24-54.
36. Agnati LF, Tarakanov AO, Ferrè S, Fuxe K. Receptor-receptor interactions, receptor mosaics and basic principles of molecular network organization: Possibile implications for drug development. J Mol Neurosci 2005, 26, 193-208.
37. Agnati LF, Guidolin D, Leo G, Fuxe K. A boolean network modelling of receptor mosaics relevance of topology and cooperativity. J Neural Transm 2007, 114, 77-92.
38. Gil T, Ipsen JH, Mouritsen OG, Sabra MC, Sperotto MM, Zuckermann MJ. Theoretical analysis of protein organization in lipid membranes. Biochim Biophys Acta 1998, 1376, 245-266.
39. Sakman E, Bruisma R. Cell adhesion and wetting transition? In: Flyvbjerg H, Jülicher F, Ormos P, David F, eds. Physics of Bio-Molecules and Cells, Berlin: Springer, 2002, 285-309.
40. Levoye A, Dam J, Ayoub MA, Guillaume JL, Couturier C, Delagrange P, Jockers R. The orphan GPR50 receptor specifically inhibits MT1 melatonin receptor function through heterodimerization. EMBO J 2006, 25, 3012-3023.
41. Rozenfeld R, Abul-Husn NS, Gomes I, Devi LA. An emerging role for the delta opioid receptor in the regulation of mu opioid receptor function. NIDA. Special Issue on Frontiers in Addiction Research. The Scientific World Journal 2007, 7(S2), 64-73.
42. Agnati LF, Ferre S, Burioni R, Woods A, Genedani S, Franco R, Fuxe K. Existence and theoretical aspects of homomeric and heteromeric dopamine receptor complexes and their relevance for neurological diseases. Neuromol Med 2005, 7, 61-78.
43. Agnati LF, Leo G, Genedani S, Andreoli N, Marcellino D, Woods A, Piron L, Guidolin D, Fuxe K. Structural plasticity in G-protein coupled receptors as demonstrated by the allosteric actions of homocysteine and computer-assisted analysis of disordered domains. Brain Res Rev 2008, 58, 459-474.
44. Fuxe K, Marcellino D, Rivera A, Diaz-Cabiale Z, Filip M, Gago B, Roberts DC, Langel U, Genedani S, Ferraro L, de la Calle A, Narvaez J, Tanganelli S, Woods A, Agnati LF. Receptor-receptor interactions within receptor mosaics. Impact on neuropsychopharmacology. Brain Res Rev 2008, 58, 415-452.
45. Bray D. Molecular networks: The top-down view. Science 2003, 301, 1864-1865.
46. Kitano H. Computational systems biology. Nature 2002, 420, 206-210.
47. Agnati LF, Ferré S, Genedani S, Leo G, Guidolin D, Filaferro M, Carriba P, Casadó V, Lluis C, Franco R, Woods AS, Fuxe K. Allosteric modulation of dopamine D2 receptors by homocysteine. J Proteome Res 2006, 5, 3077-3083.
48. Yablonskiy DA, Ackerman JJ, Raichle ME. Coupling between changes in human brain temperature and oxidative metabolism during prolonged visual stimulation. Proc Natl Acad Sci U S A 2000, 97, 7603-7608.
49. Agnati LF, Vergoni AV, Leo G, Genedani S, Franco R, Bertolini A, Fuxe K. Energy gradients for VT-signal migration in the CNS: studies on melanocortin receptors, mitochondrial uncoupling proteins and food intake. J Endocrinol Invest 2004, 27, 63-34.
50. Rivera A, Agnati LF, Horvath TL, Valderrama JJ, de La Calle A, Fuxe K. Uncoupling protein 2/3 immunoreactivity and the ascending dopaminergic and noradrenergic neuronal systems: Relevance for volume transmission. Neuroscience 2006, 137, 1447-1461.
51. Allen JA, Halverson-Tamboli RA, Rasenick MM. Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 2007, 8, 128-140.
52. Patel HH, Murray F, Insel PA. G-protein-coupled receptor-signaling components in membrane raft and caveolae microdomains. Handb Exp Pharmacol 2008, 186, 167-184.
53. Echarri A, Muriel O, Del Pozo MA. Intracellular trafficking of raft/caveolae domains: Insights from integrin signaling. Semin Cell Dev Biol 2007, 18, 627-637.
54. Gimpl G, Gehrig-Burger I. Cholesterol reporter molecules. Biosci Rep 2007, 27, 335-358.
55. Maxfield FR. Plasma membrane microdomains. Curr Opin Cell Biol 2002, 14, 483-487.
56. Martens JR, O'Connell K, Tamkun M. Targeting of ion channels to membrane microdomains: localization of KV channels to lipid rafts. Trends Pharmacol Sci 2004, 25, 16-21.
57. Wang XQ, Paller AS. Lipid rafts: Membrane triage centers. J Invest Dermatol 2006, 126, 951-953.
58. Oh P, Schnitzer JE. Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol Biol Cell 2001, 12, 685-698.
59. Ostrom RS, Insel PA. The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 2004, 143, 235-345.
60. Kenakin T. Inverse, protean, and ligand-selective agonism: Matters of receptor conformation. FASEB J 2001, 15, 598-611.
61. Kenakin T. Ligand-selective receptor conformations revisited: the promise and the problem. Trends Pharmacol Sci 2003, 24, 346-354.
62. Insel PA, Head BP, Patel HH, Roth DM, Bundey RA, Swaney JS. Compartmentation of G-protein-coupled receptors and their signalling components in lipid rafts and caveolae. Biochem Soc Trans 2005, 33, 1131-1134.
63. Fastenberg ME, Shogomori H, Xu X, Brown DA, London E. Exclusion of a transmembrane-type peptide from ordered-lipid domains (rafts) detected by fluorescence quenching: Extension of quenching analysis to account for the effects of domain size and domain boundaries. Biochemistry 2003, 42, 12376-1290.
64. Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A, Palczewski K. Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 2003, 421, 127-128.
65. Gouldson PR, Higgs C, Smith RE, Dean MK, Gkoutos GV, Reynolds CA. Dimerization and domain swapping in G-protein-coupled receptors: A computational study. Neuropsychopharmacology 2000, 23, S60-S77.
66. Barequet G, Moffie M. On the complexity of Jensen's algorithm for counting fixed polyominoes. J Discr Algor 2007, 5, 348-355.
67. Vöge M, Guttmann A. On the number of hexagonal polyominoes. Theor Comp Sci 2003, 307, 433-453.
68. Kitaev S. On multi-avoidance of right angled numbered polyomino patterns. Integers 2004, 4, A21.
69. Franco R, Canals M, Marcellino D, Ferre S, Agnati L, Mallol J, Casado V, Ciruela F, Fuxe K, Lluis C, Canela EI. Regulation of heptaspanning membrane receptor function by dimerization and clustering. Trends Biochem Sci 2003, 28, 238-243.
70. Agnati LF, Leo G, Genedani S, Guidolin D, Andreoli N, Fuxe K. Possible relevance of receptor-receptor interactions between viral- and host-coded receptors for viral-induced diseases. ScientificWorldJournal 2007, 7, 1073-1081.
71. Lipton SA, Kim WK, Choi YB, Kumar S, D'Emilia DM, Rayudu PV, Arnelle DR, Stamler JS. Neurotoxicity associated with dual actions of homocysteine at the N-methyl-D-aspartate receptor. Proc Natl Acad Sci U S A 1997, 94, 5923-5928.
72. Nakata H, Yoshioka K, Kamiya T, Tsuga H, Oyanagi K. Functions of heteromeric association between adenosine and P2Y receptors. J Mol Neurosci 2005, 26, 233-238.
73. Rashid AJ, So CH, Kong MM, Furtak T, El-Ghundi M, Cheng R, O'Dowd BF, George SR. D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci U S A 2007, 104, 654-659.
74. Ferré S, Ciruela F, Woods AS, Lluis C, Franco R. Functional relevance of neurotransmitter receptor heteromers in the central nervous system. Trend Neurosci 2007, 30, 440-446.
75. Ferré S, Ciruela F, Quiroz C, Luján R, Popoli P, Cunha RA, Agnati LF, Fuxe K, Woods AS, Lluis C, Franco R. Adenosine receptor heteromers and their integrative role in striatal function. The Scientific World Journal 2007, 7, 74-85.
76. Raddatz R, Schaffhauser H, Marino MJ. Allosteric approaches to the targeting of G-protein-coupled receptors for novel drug discovery: A critical assessment. Biochem Pharmacol 2007, 74, 383-391.
77. Gunasekaran K, Ma B, Nussinov R. Is allostery an intrinsic property of all dynamic proteins? Proteins 2004, 57, 433-443.