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Francisco Ciruela

Education

Ph.D. in Biological Sciences, University of Barcelona, Spain, 1995

Current position

Associate Professor in Pharmacology, Pharmacology Unit, Department of Pathology and Experimental Therapeutics, School of Medicine, University of Barcelona, Spain (12/2007-ongoing)
Visiting Professor, Department of Physiology (WE15), Faculty of Sciences University of Ghent, Belgium (01/2013-ongoing)

Publications (since 2010)

  1. Constantino, L. C., Pamplona, F. A., Matheus, F. C., Ludka, F. K., Gómez-Soler, M., Ciruela, F., Boeck, C. R., Prediger, R. D. S and Tasca, C. I. (2014). Adenosine A1 receptor activation modulates N-methyl-D-aspartate preconditioning phenotype in the brain. Neuroscience (In press)
  2. Fuxe, K., Borroto-Escuela, D. O., Romero-Fernandez, W., Palkovits, M., Tarakanov, A. O., Ciruela, F. and Agnati, L. F. (2014). Moonlighting proteins and protein-protein interactions as neurotherapeutic targets in the g protein-coupled receptor field. Neuropsychopharmacology 39(1): 131-155.
  3. Gomez-Soler, M., Fernandez-Duenas, V., Portillo-Salido, E., Perez, P., Zamanillo, D., Vela, J. M., Burgueno, J. and Ciruela, F. (2014). Predicting the antinociceptive efficacy of sigma(1) receptor ligands by a novel receptor fluorescence resonance energy transfer (FRET) based biosensor. J Med Chem 57(1): 238-242.
  4. Borroto-Escuela, D. O., Romero-Fernández, W., Garriga, P., Ciruela, F., Narváez, M., Tarakanov, A. O., Palkovits, M., Agnati, L. F. and Fuxe, K. (2013). Chapter Fifteen – G Protein–Coupled Receptor Heterodimerization in the Brain. Methods in Enzymology 521: 281-294.
  5. Balana, B., Bahima, L., Bodhinathan, K., Taura, J. J., Taylor, N. M., Nettleton, M. Y., Ciruela, F. and Slesinger, P. A. (2013). Ras-association domain of sorting Nexin 27 is critical for regulating expression of GIRK potassium channels. PLoS ONE 8(3): e59800.
  6. Gandia, J., Fernandez-Duenas, V., Morato, X., Caltabiano, G., Gonzalez-Muniz, R., Pardo, L., Stagljar, I. and Ciruela, F. (2013). The Parkinson's disease-associated GPR37 receptor-mediated cytotoxicity is controlled by its intracellular cysteine-rich domain. J Neurochem 125(3): 362-372.
  7. Agnati, L. F., Guidolin, D., Woods, A. S., Ciruela, F., Carone, C., Vallelunga, A., Escuela, D. O., Genedani, S. and Fuxe, K. (2013). A new interpretative paradigm for Conformational Protein Diseases. Curr Protein Pept Sci 14(2): 141-160.
  8. Giraldo, J. and Ciruela, F. (2013). Oligomerization in Health and Disease. Progress In Molecular Biology and Translational Science 117, xix- xxii.
  9. Fernandez-Duenas, V., Gomez-Soler, M., Morato, X., Nunez, F., Das, A., Kumar, T. S., Jauma, S., Jacobson, K. A. and Ciruela, F. (2013). Dopamine D(2) receptor-mediated modulation of adenosine A(2A) receptor agonist binding within the A(2A)R/D(2)R oligomer framework. Neurochem Int 63(1): 42-46.
  10. Incontro, S., Ciruela, F., Ziff, E., Hofmann, F., Sanchez-Prieto, J. and Torres, M. (2013). The type II cGMP dependent protein kinase regulates GluA1 levels at the plasma membrane of developing cerebellar granule cells. Biochim Biophys Acta 1833(8): 1820-1831.
  11. Ciruela, F. (2013). Guanosine behind the scene. J Neurochem 126(4): 425-427.
  12. Ferrero, J. J., Alvarez, A. M., Ramirez-Franco, J., Godino, M. C., Bartolome-Martin, D., Aguado, C., Torres, M., Lujan, R., Ciruela, F. and Sanchez-Prieto, J. (2013). beta-Adrenergic receptors activate exchange protein directly activated by cAMP (Epac), translocate Munc13-1, and enhance the Rab3A-RIM1alpha interaction to potentiate glutamate release at cerebrocortical nerve terminals. J Biol Chem 288(43): 31370-31385.
  13. Vallano, A., Fernandez-Duenas, V., Garcia-Negredo, G., Quijada, M. A., Simon, C. P., Cuffi, M. L., Carbonell, L., Sanchez, S., Arnau, J. M. and Ciruela, F. (2013). Targeting striatal metabotropic glutamate receptor type 5 in Parkinson's disease: bridging molecular studies and clinical trials. CNS Neurol Disord Drug Targets 12(8): 1128-1142.
  14. Ciruela, F. (2012). G protein-coupled receptors interacting proteins: towards the druggable interactome. Curr Drug Targets 13(1): 1-2.
  15. Borroto-Escuela, D. O., Agnati, L. F., Fuxe, K. and Ciruela, F. (2012). Muscarinic acetylcholine receptor-interacting proteins (mAChRIPs): targeting the receptorsome. Curr Drug Targets 13(1): 53-71.
  16. Lujan, R. and Ciruela, F. (2012). GABAB receptors-associated proteins: potential drug targets in neurological disorders? Curr Drug Targets 13(1): 129-144.
  17. Borroto-Escuela, D. O., Romero-Fernandez, W., Mudo, G., Perez-Alea, M., Ciruela, F., Tarakanov, A. O., Narvaez, M., Di Liberto, V., Agnati, L. F., Belluardo, N. and Fuxe, K. (2012). Fibroblast growth factor receptor 1- 5-hydroxytryptamine 1A heteroreceptor complexes and their enhancement of hippocampal plasticity. Biol Psychiatry 71(1): 84-91.
  18. Guescini, M., Leo, G., Genedani, S., Carone, C., Pederzoli, F., Ciruela, F., Guidolin, D., Stocchi, V., Mantuano, M., Borroto-Escuela, D. O., Fuxe, K. and Agnati, L. F. (2012). Microvesicle and tunneling nanotube mediated intercellular transfer of g-protein coupled receptors in cell cultures. Exp Cell Res 318(5): 603-613.
  19. Fuxe, K., Borroto-Escuela, D. O., Marcellino, D., Romero-Fernandez, W., Frankowska, M., Guidolin, D., Filip, M., Ferraro, L., Woods, A. S., Tarakanov, A., Ciruela, F., Agnati, L. F. and Tanganelli, S. (2012). GPCR heteromers and their allosteric receptor-receptor interactions. Curr Med Chem 19(3): 356-363.
  20. Fernandez-Duenas, V., Poveda, R., Sanchez, S. and Ciruela, F. (2012). Synergistic interaction between fentanyl and a tramadol: paracetamol combination on the inhibition of nociception in mice. J Pharmacol Sci 118(2): 299-302.
  21. Capdevila-Nortes, X., López-Hernández, T., Ciruela, F. and Estévez, R. (2012). A modification of the split-tobacco etch virus method for monitoring interactions between membrane proteins in mammalian cells. Analytical Biochemistry 423 (1): 109-118.
  22. Borroto-Escuela, D. O., Romero-Fernandez, W., Perez-Alea, M., Narvaez, M., Tarakanov, A. O., Mudo, G., Agnati, L. F., Ciruela, F., Belluardo, N. and Fuxe, K. (2012). The existence of FGFR1-5-HT1A receptor heterocomplexes in midbrain 5-HT neurons of the rat: relevance for neuroplasticity. J Neurosci 32(18): 6295-6303.
  23. Gonzalez, S., Rangel-Barajas, C., Peper, M., Lorenzo, R., Moreno, E., Ciruela, F., Borycz, J., Ortiz, J., Lluis, C., Franco, R., McCormick, P. J., Volkow, N. D., Rubinstein, M., Floran, B. and Ferre, S. (2012). Dopamine D4 receptor, but not the ADHD-associated D4.7 variant, forms functional heteromers with the dopamine D2S receptor in the brain. Mol Psychiatry 17(6): 650-662.
  24. Fuxe, K., Borroto-Escuela, D., Romero-Fernández, W., Diaz-Cabiale, Z., Rivera, A., Ferraro, L., Tanganelli, S., Tarakonov, A. O., Garriga, P., Narváez, J. A., Ciruela, F., Guescini, M. and Agnati, L. F. (2012). Extrasynaptic neurotransmission in the modulation of brain function. Focus on the striatal neuronal-glialnetworks. Frontiers in Physiology (3) 136.
  25. Canela, L., Selga, E., Garcia-Martinez, J. M., Amaral, O. B., Fernandez-Duenas, V., Alberch, J., Canela, E. I., Franco, R., Noe, V., Lluis, C., Ciudad, C. J. and Ciruela, F. (2012). Transcriptional profiling of striatal neurons in response to single or concurrent activation of dopamine D2, adenosine A(2A) and metabotropic glutamate type 5 receptors: focus on beta-synuclein expression. Gene 508(2): 199-205.
  26. Fernandez-Duenas, V., Llorente, J., Gandia, J., Borroto-Escuela, D. O., Agnati, L. F., Tasca, C. I., Fuxe, K. and Ciruela, F. (2012). Fluorescence resonance energy transfer-based technologies in the study of protein-protein interactions at the cell surface. Methods 57(4): 467-472.
  27. Ciruela, F., Fernandez-Duenas, V., Llorente, J., Borroto-Escuela, D., Cuffi, M. L., Carbonell, L., Sanchez, S., Agnati, L. F., Fuxe, K. and Tasca, C. I. (2012). G protein-coupled receptor oligomerization and brain integration: focus on adenosinergic transmission. Brain Res 1476: 86-95.
  28. Fuxe, K., Borroto-Escuela, D. O., Romero-Fernandez, W., Ciruela, F., Manger, P., Leo, G., Diaz-Cabiale, Z. and Agnati, L. F. (2012). On the role of volume transmission and receptor-receptor interactions in social behaviour: focus on central catecholamine and oxytocin neurons. Brain Res 1476: 119-131.
  29. Fernandez-Duenas, V., Gomez-Soler, M., Jacobson, K. A., Kumar, S. T., Fuxe, K., Borroto-Escuela, D. O. and Ciruela, F. (2012). Molecular determinants of A2AR-D2R allosterism: role of the intracellular loop 3 of the D2R. J Neurochem 123(3): 373-384.
  30. Fuxe, K., Borroto-Escuela, D. O., Romero-Fernandez, W., Tarakanov, A. O., Calvo, F., Garriga, P., Tena, M., Narvaez, M., Millon, C., Parrado, C., Ciruela, F., Agnati, L. F., Narvaez, J. A. and Diaz-Cabiale, Z. (2012). On the existence and function of galanin receptor heteromers in the central nervous system. Front Endocrinol (Lausanne) 3: 127.
  31. Borroto-Escuela, D. O., Correia, P. A., Romero-Fernandez, W., Narvaez, M., Fuxe, K., Ciruela, F. and Garriga, P. (2011). Muscarinic receptor family interacting proteins: role in receptor function. J Neurosci Methods 195(2): 161-169.
  32. Borroto-Escuela, D. O., Romero-Fernandez, W., Tarakanov, A. O., Ciruela, F., Agnati, L. F. and Fuxe, K. (2011). On the existence of a possible A2A-D2-beta-Arrestin2 complex: A2A agonist modulation of D2 agonist-induced beta-arrestin2 recruitment. J Mol Biol 406(5): 687-699.
  33. Fernandez-Duenas, V., Poveda, R., Fernandez, A., Sanchez, S., Planas, E. and Ciruela, F. (2011). Fentanyl-trazodone-paracetamol triple drug combination: multimodal analgesia in a mouse model of visceral pain. Pharmacol Biochem Behav 98(3): 331-336.
  34. Llach, A., Molina, C. E., Prat-Vidal, C., Fernandes, J., Casado, V., Ciruela, F., Lluis, C., Franco, R., Cinca, J. and Hove-Madsen, L. (2011). Abnormal calcium handling in atrial fibrillation is linked to up-regulation of adenosine A2A receptors. Eur Heart J 32(6): 721-729.
  35. Ciruela, F. (2011). Adenosine receptors. Biochim Biophys Acta 1808(5): 1231-1232.
  36. Ciruela, F., Gomez-Soler, M., Guidolin, D., Borroto-Escuela, D. O., Agnati, L. F., Fuxe, K. and Fernandez-Duenas, V. (2011). Adenosine receptor containing oligomers: their role in the control of dopamine and glutamate neurotransmission in the brain. Biochim Biophys Acta 1808(5): 1245-1255.
  37. Guidolin, D., Ciruela, F., Genedani, S., Guescini, M., Tortorella, C., Albertin, G., Fuxe, K. and Agnati, L. F. (2011). Bioinformatics and mathematical modelling in the study of receptor-receptor interactions and receptor oligomerization: focus on adenosine receptors. Biochim Biophys Acta 1808(5): 1267-1283.
  38. Van Craenenbroeck, K., Borroto-Escuela, D. O., Romero-Fernandez, W., Skieterska, K., Rondou, P., Lintermans, B., Vanhoenacker, P., Fuxe, K., Ciruela, F. and Haegeman, G. (2011). Dopamine D4 receptor oligomerization--contribution to receptor biogenesis. FEBS J 278(8): 1333-1344.
  39. Caballero, M., Nunez, F., Ahern, S., Cuffi, M. L., Carbonell, L., Sanchez, S., Fernandez-Duenas, V. and Ciruela, F. (2011). Caffeine improves attention deficit in neonatal 6-OHDA lesioned rats, an animal model of attention deficit hyperactivity disorder (ADHD). Neurosci Lett 494(1): 44-48.
  40. Gómez-Soler, M., Ahern, S., Fernández-Dueñas, V. and Ciruela, F. (2011). On the Role of G Protein-Coupled Receptors Oligomerization. The Open Biology Journal 4 (1), 47-53.
  41. Romero-Fernandez, W., Borroto-Escuela, D. O., Tarakanov, A. O., Mudo, G., Narvaez, M., Perez-Alea, M., Agnati, L. F., Ciruela, F., Belluardo, N. and Fuxe, K. (2011). Agonist-induced formation of FGFR1 homodimers and signaling differ among members of the FGF family. Biochem Biophys Res Commun 409(4): 764-768.
  42. Borroto-Escuela, D. O., Tarakanov, A. O., Guidolin, D., Ciruela, F., Agnati, L. F. and Fuxe, K. (2011). Moonlighting characteristics of G protein-coupled receptors: focus on receptor heteromers and relevance for neurodegeneration. IUBMB Life 63(7): 463-472.
  43. Lopez-Hernandez, T., Sirisi, S., Capdevila-Nortes, X., Montolio, M., Fernandez-Duenas, V., Scheper, G. C., van der Knaap, M. S., Casquero, P., Ciruela, F., Ferrer, I., Nunes, V. and Estevez, R. (2011). Molecular mechanisms of MLC1 and GLIALCAM mutations in megalencephalic leukoencephalopathy with subcortical cysts. Hum Mol Genet 20(16): 3266-3277.
  44. Ciruela, F. and Fernández-Dueñas, V. (2011). G protein-coupled receptors oligomerization: Insights from fluorescence/luminescence-based methods. In: Giraldo, J., and Pin, J-P. (eds). The Royal Society of Chemistry, 90-110.
  45. Sahlholm, K., Barchad-Avitzur, O., Marcellino, D., Gomez-Soler, M., Fuxe, K., Ciruela, F. and Arhem, P. (2011). Agonist-specific voltage sensitivity at the dopamine D2S receptor--molecular determinants and relevance to therapeutic ligands. Neuropharmacology 61(5-6): 937-949.
  46. Vallano, A., Fernandez-Duenas, V., Pedros, C., Arnau, J. M. and Ciruela, F. (2011). An update on adenosine A2A receptors as drug target in Parkinson's disease. CNS Neurol Disord Drug Targets 10(6): 659-669.
  47. Agnati, L. F., Guidolin, D., Leo, G., Guescini, M., Pizzi, M., Stocchi, V., Spano, P. F., Ghidoni, R., Ciruela, F., Genedani, S. and Fuxe, K. (2011). Possible new targets for GPCR modulation: allosteric interactions, plasma membrane domains, intercellular transfer and epigenetic mechanisms. J Recept Signal Transduct Res 31(5): 315-331.
  48. Barrachina, M., Martín, M., Ciruela, F. and Ferrer, I. (2011). Epigenetic modulation of adenosine A2A receptor: A putative therapeutical tool for Parkinson’s disease treatment. In: David I. Finkelstein (ed). InTech Open Access Publisher, 295-312.
  49. Borroto-Escuela, D. O., Romero-Fernandez, W., Garcia-Negredo, G., Correia, P. A., Garriga, P., Fuxe, K. and Ciruela, F. (2011). Dissecting the conserved NPxxY motif of the M3 muscarinic acetylcholine receptor: critical role of Asp-7.49 for receptor signaling and multiprotein complex formation. Cell Physiol Biochem 28(5): 1009-1022.
  50. Ciruela, F., Albergaria, C., Soriano, A., Cuffi, L., Carbonell, L., Sanchez, S., Gandia, J. and Fernandez-Duenas, V. (2010). Adenosine receptors interacting proteins (ARIPs): Behind the biology of adenosine signaling. Biochim Biophys Acta 1798(1): 9-20.
  51. Borroto-Escuela, D. O., Marcellino, D., Narvaez, M., Flajolet, M., Heintz, N., Agnati, L., Ciruela, F. and Fuxe, K. (2010). A serine point mutation in the adenosine A2AR C-terminal tail reduces receptor heteromerization and allosteric modulation of the dopamine D2R. Biochem Biophys Res Commun 394(1): 222-227.
  52. Borroto-Escuela, D. O., Correia, P. A., Perez Alea, M., Narvaez, M., Garriga, P., Fuxe, K. and Ciruela, F. (2010). Impaired M(3) muscarinic acetylcholine receptor signal transduction through blockade of binding of multiple proteins to its third intracellular loop. Cell Physiol Biochem 25(4-5): 397-408.
  53. Fuxe, K., Marcellino, D., Borroto-Escuela, D. O., Guescini, M., Fernandez-Duenas, V., Tanganelli, S., Rivera, A., Ciruela, F. and Agnati, L. F. (2010). Adenosine-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci Ther 16(3): e18-42.
  54. Martin, R., Durroux, T., Ciruela, F., Torres, M., Pin, J. P. and Sanchez-Prieto, J. (2010). The metabotropic glutamate receptor mGlu7 activates phospholipase C, translocates munc-13-1 protein, and potentiates glutamate release at cerebrocortical nerve terminals. J Biol Chem 285(23): 17907-17917.
  55. Borroto-Escuela, D. O., Garcia-Negredo, G., Garriga, P., Fuxe, K. and Ciruela, F. (2010). The M(5) muscarinic acetylcholine receptor third intracellular loop regulates receptor function and oligomerization. Biochim Biophys Acta 1803(7): 813-825.
  56. Fernandez-Duenas, V., Ciruela, F., Gandia, J., Sanchez, S., Planas, E. and Poveda, R. (2010). Histamine H3 receptor activation potentiates peripheral opioid-mediated antinociception: substance P role in peripheral inflammation in mice. Eur J Pharmacol 638(1-3): 72-77.
  57. Ciruela, F., Vilardaga, J. P. and Fernandez-Duenas, V. (2010). Lighting up multiprotein complexes: lessons from GPCR oligomerization. Trends Biotechnol 28(8): 407-415.
  58. Fuxe, K., Marcellino, D., Borroto-Escuela, D. O., Frankowska, M., Ferraro, L., Guidolin, D., Ciruela, F. and Agnati, L. F. (2010). The changing world of G protein-coupled receptors: from monomers to dimers and receptor mosaics with allosteric receptor-receptor interactions. J Recept Signal Transduct Res 30(5): 272-283.
  59. Agnati, L. F., Guidolin, D., Vilardaga, J. P., Ciruela, F. and Fuxe, K. (2010). On the expanding terminology in the GPCR field: the meaning of receptor mosaics and receptor heteromers. J Recept Signal Transduct Res 30(5): 287-303.
  60. Ciruela, F., Vallano, A., Arnau, J. M., Sanchez, S., Borroto-Escuela, D. O., Agnati, L. F., Fuxe, K. and Fernandez-Duenas, V. (2010). G protein-coupled receptor oligomerization for what? J Recept Signal Transduct Res 30(5): 322-330.
  61. Agnati, L. F., Guidolin, D., Albertin, G., Trivello, E., Ciruela, F., Genedani, S., Tarakanov, A. and Fuxe, K. (2010). An integrated view on the role of receptor mosaics at perisynaptic level: focus on adenosine A(2A), dopamine D(2), cannabinoid CB(1), and metabotropic glutamate mGlu(5) receptors. J Recept Signal Transduct Res 30(5): 355-369.
  62. Ciruela, F., Fernandez-Duenas, V., Sahlholm, K., Fernandez-Alacid, L., Nicolau, J. C., Watanabe, M. and Lujan, R. (2010). Evidence for oligomerization between GABAB receptors and GIRK channels containing the GIRK1 and GIRK3 subunits. Eur J Neurosci 32(8): 1265-1277.
  63. Borroto-Escuela, D. O., Romero-Fernandez, W., Tarakanov, A. O., Marcellino, D., Ciruela, F., Agnati, L. F. and Fuxe, K. (2010). Dopamine D2 and 5-hydroxytryptamine 5-HT((2)A) receptors assemble into functionally interacting heteromers. Biochem Biophys Res Commun 401(4): 605-610.
  64. Borroto-Escuela, D. O., Romero-Fernandez, W., Tarakanov, A. O., Gomez-Soler, M., Corrales, F., Marcellino, D., Narvaez, M., Frankowska, M., Flajolet, M., Heintz, N., Agnati, L. F., Ciruela, F. and Fuxe, K. (2010). Characterization of the A2AR-D2R interface: focus on the role of the C-terminal tail and the transmembrane helices. Biochem Biophys Res Commun 402(4): 801-807.
  65. Vilardaga, J. P., Agnati, L. F., Fuxe, K. and Ciruela, F. (2010). G-protein-coupled receptor heteromer dynamics. J Cell Sci 123(Pt 24): 4215-4220.
  66. Cuffi, M. L., Artells, R., Navarro, A., Ciruela, F. and Carbonell, L. (2010). Regulation of alpha(2)-adrenoceptor gene expression by chronic lithium treatment in rat brain. Methods Find Exp Clin Pharmacol 32(10): 721-725.
Protocols by Francisco Ciruela
  1. Synthesis of the Adenosine A2A Receptor Fluorescent Agonist MRS5424
  2. Adenosine A2A Receptor Ligand Binding Experiments by Using Real-time Single-cell FRET