Bombesin receptor regulation of emotional memory

Reviews in the Neurosciences

Volumn 23, Issue 5-6, 2012, Pages 571-586

  Roesler, Rafael ^a,b,c   Kent, Pamela ^d   Schroder, Nadja ^c,e   Schwartsmann, Gilberto ^b,c   Merali, Zul ^d,f  

^a Instituto de Ciencias Biologicas e da Saude Pontifical Catholic University of Minas Gerais   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^c National Institute for Translational Medicine   (Brazil)

^d UNIVERSITY OF OTTAWA   (Canada)

^e PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^f CARLETON UNIVERSITY   (Canada)

Author keywords

BB1 receptor; BB2 receptor; Gastrin releasing peptide receptor; Memory modulation; Neuromedin B receptor

Indexed keywords

BIM 23127; BOMBESIN; BOMBESIN RECEPTOR; BRS 3 RECEPTOR; G PROTEIN COUPLED RECEPTOR; GASTRIN RELEASING PEPTIDE; GROWTH FACTOR; HORMONE; NEUROMEDIN B RECEPTOR; NEUROTRANSMITTER; PROTEIN KINASE; RC 3095; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANXIETY DISORDER; BASOLATERAL AMYGDALA; BRAIN CORTEX; DORSAL HIPPOCAMPUS; EMOTION; HIPPOCAMPUS; HUMAN; MEMORY; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS;

ANIMALS; EMOTIONS; HUMANS; MEMORY; MODELS, MOLECULAR; RECEPTORS, BOMBESIN; SIGNAL TRANSDUCTION;

EID: 84869390943     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/revneuro-2012-0046     Document Type: Review

References (132)

1. Anastasi, A., Erspamer, V., and Bucci, M. (1972). Isolation and amino acid sequences of alytesin and bombesin, two analogous active tetradecapeptides from the skin of European discoglossid frogs. Arch. Biochem. Biophys. 148, 443-446.
2. Battey, J. and Wada, E. (1991). Two distinct receptor subtypes for mammalian bombesin-like peptides. Trends Neurosci. 14, 524-528.
3. Battey, J.F., Way, J.M., Corjay, M.H., Shapira, H., Kusano, K., Harkins, R., Wu, J.M., Slattery, T., Mann, E., and Feldman, R.I. (1991). Molecular cloning of the bombesin/gastrin-releasing peptide receptor from Swiss 3T3 cells. Proc. Natl. Acad. Sci. USA 88, 395-399.
4. B e dard, T., Mountney, C., Kent, P., Anisman, H., and Merali, Z. (2007). Role of gastrin-releasing peptide and neuromedin B in anxiety and fear-related behavior. Behav. Brain Res. 179, 133-140.
5. Benya, R.V., Kusui, T., Pradhan, T.K., Battey, J.F., and Jensen, R.T. (1995). Expression and characterization of cloned human bombesin receptors. Mol. Pharmacol. 47, 10-20.
6. Brown, M., Rivier, J., and Vale, W. (1977a). Bombesin: potent effects on thermoregulation in the rat. Science 196, 998-1000.
7. Brown, M.R., Rivier, J., and Vale W.W. (1977b). Bombesin affects the central nervous system to produce hyperglycemia in rats. Life Sci. 21, 1729-1734.
8. Chan, A.S. and Wong, Y.H. (2005). Gq-mediated activation of c-Jun N-terminal kinase by the gastrin-releasing peptidepreferring bombesin receptor is inhibited upon costimulation of the Gs-coupled dopamine D1 receptor in COS-7 cells. Mol. Pharmacol. 68, 1354-1364.
9. Chaperon, F., Fendt, M., Kelly, P.H., Lingenhoehl, K., Mosbacher, J., Olpe, H.R., Schmid, P., Sturchler, C., McAllister, K.H., van der Putten, P.H., et al. (2012). Gastrin-releasing peptide signalling plays a limited and subtle role in amygdala physiology and aversive memory. PLoS ONE 7, e34963.
10. Chatzistamou, I., Schally, A.V., Sun, B., Armatis, P., and Szepeshazi, K. (2000). Inhibition of growth of OV-1063 human epithelial ovarian cancers and c-jun and c-fos oncogene expression by bombesin antagonists. Br. J. Cancer 83, 906-913.
11. Chen, P.W. and Kroog, G.S. (2004). Alterations in receptor expression or agonist concentration change the pathways gastrin-releasing peptide receptor uses to regulate extracellular signal-regulated kinase. Mol. Pharmacol. 66, 1625-1634.
12. Chronwall, B.M., Pisano, J.J., Bishop, J.F., Moody, T.W., and O'Donohue, T.L. (1985). Biochemical and histochemical characterization of ranatensin immunoreactive peptides in rat brain: lack of coexistence with bombesin/GRP. Brain Res. 338, 97-113.
13. Corjay, M.H., Dobrzanski, D.J., Way, J.M., Viallet, J., Shapira, H., Worland, P., Sausville, E.A., and Battey, J.F. (1991). Two distinct bombesin receptor subtypes are expressed and functional in human lung carcinoma cells. J. Biol. Chem. 266, 18771-18779.
14. Czepielewski, R.S., Porto, B.N., Rizzo, L.B., Roesler, R., Abujamra, A.L., Pinto, L.G., Schwartsmann, G., Cunha, F.Q., and Bonorino, C. (2012). Gastrin-releasing peptide receptor (GRPR) mediates chemotaxis in neutrophils. Proc. Natl. Acad. Sci. USA 109, 547-552.
15. Dantas, A.S., Luft, T., Henriques, J.A., Schwartsmann, G., and Roesler, R. (2006). Opposite effects of low and high doses of the gastrin-releasing peptide receptor antagonist RC-3095 on memory consolidation in the hippocampus: possible involvement of the GABAergic system. Peptides 27, 2307-2312.
16. De Castiglione, R. and Gozzini, L. (1996). Bombesin receptor antagonists. Crit. Rev. Oncol. Hematol. 24, 117-151.
17. de Farias, C.B., Lima, R.C., Lima, L.O., Flores, D.G., Meurer, L., Brunetto, A.L., Schwartsmann, G., and Roesler, R. (2008). Stimulation of proliferation of U138-MG glioblastoma cells by gastrin-releasing peptide in combination with agents that enhance cAMP signaling. Oncology 75, 27-31.
18. de Farias, C.B., Rosemberg, D.B., Heinen, T.E., Koehler-Santos, P., Abujamra, A.L., Kapczinski, F., Brunetto, A.L., Ashton-Prolla, P., Meurer, L., Bogo, M.R., et al. (2010). BDNF/TrkB content and interaction with gastrin-releasing peptide receptor blockade in colorectal cancer. Oncology 79, 430-439.
19. de Wied, D. (1997). Neuropeptides in learning and memory processes. Behav. Brain Res. 83, 83-90.
20. Del Rio, M. and De la Fuente, M. (1994). Chemoattractant capacity of bombesin, gastrin-releasing peptide and neuromedin C is mediated through PKC activation in murine peritoneal leukocytes. Regul. Pept. 49, 185-193.
21. Dobrzanski, D., Sharoni, Y., Wada, E., Battey, J., and Sausville, E. (1993). Neuromedin-B receptor transfected BALB/3T3 cells: signal transduction and effects of ectopic receptor expression on cell growth. Regul. Pept. 45, 341-352.
22. Engelmann, M., Wotjak, C.T., Neumann, I., Ludwig, M., and Landgraf, R. (1996). Behavioral consequences of intracerebral vasopressin and oxytocin: focus on learning and memory. Neurosci. Biobehav. Rev. 20, 341-58.
23. Erspamer, V., Erpamer, G.F., and Inselvini, M. (1970). Some pharmacological actions of alytesin and bombesin. J. Pharm. Pharmacol. 22, 875-876.
24. Fathi, Z., Corjay, M.H., Shapira, H., Wada, E., Benya, R., Jensen, R., Viallet, J., Sausville, E.A., and Battey, J.F. (1993). BRS-3: novel bombesin receptor subtype selectively expressed in testis and lung carcinoma cells. J. Biol. Chem. 268, 5979-5984.
25. Feany, M.B. (1996). Neuropeptide modulation of learning and memory processes. Rev. Neurosci. 7, 151-164.
26. Fehm, H.L., Perras, B., Smolnik, R., Kern, W., and Born, J. (2000). Manipulating neuropeptidergic pathways in humans: a novel approach to neuropharmacology? Eur. J. Pharmacol. 405, 43-54.
27. Flood, J.F. and Morley, J.E. (1988). Effects of bombesin and gastrinreleasing peptide on memory processing. Brain Res. 460, 314-322.
28. Flood, J.F. and Morley, J.E. (1989). Cholecystokinin receptors mediate enhanced memory retention produced by feeding and gastrointestinal peptides. Peptides 10, 809-813.
29. Flores, D.G., de Farias, C.B., Leites, J., de Oliveira, M.S., Lima, R.C., Tamajusuku, A.S., Di Leone, L.P., Meurer, L., Brunetto, A.L., Schwartsmann, G., et al. (2008). Gastrin-releasing peptide receptors regulate proliferation of C6 glioma cells through a phosphatidylinositol 3-kinase-dependent mechanism. Curr. Neurovasc. Res. 5, 99-105.
30. Garcia, V.A., Dornelles, A.S., Presti-Torres, J., Alcalde, L.A., Halmenschlager, L.H., Schwartsmann, G., Roesler, R., Lucion, A.B., and Schr o der, N. (2010). Neonatal gastrin-releasing peptide receptor blockade reduces maternal odor preference in rats. Behav. Brain Res. 214, 456-459.
31. Gibson, G.E., Vestling, M., Zhang, H., Szolosi, S., Alkon, D., Lannfelt, L., Gandy, S., and Cowburn, R.F. (1997). Abnormalities in Alzheimer's disease fibroblasts bearing the APP670/671 mutation. Neurobiol. Aging 18, 573-580.
32. Gonzalez, N., Moody, T.W., Igarashi, H., Ito, T., and Jensen, R.T. (2008). Bombesin-related peptides and their receptors: recent advances in their role in physiology and disease states. Curr. Opin. Endocrinol. Diabetes Obes. 15, 58-64.
33. Gorbulev, V., Akhundova, A., Buchner, H., and Fahrenholz, F. (1992). Molecular cloning of a new bombesin receptor subtype expressed in uterus during pregnancy. Eur. J. Biochem. 208, 405-410.
34. Gutzwiller, J.P., Drewe, J., Hildebrand, P., Rossi, L., Lauper, J.Z., and Beglinger, C. (1994). Effect of intravenous human gastrinreleasing peptide on food intake in humans. Gastroenterology 106, 1168-1173.
35. Hellmich, M.R., Ives, K.L., Udupi, V., Soloff, M.S., Greeley, G.H. Jr., Christensen, B.N., and Townsend, C.M. Jr. (1999). Multiple protein kinase pathways are involved in gastrin-releasing peptide receptor-regulated secretion. J. Biol. Chem. 274, 23901-23909.
36. Hodges, L.M., Weissman, M.M., Haghighi, F., Costa, R., Bravo, O., Evgrafov, O., Knowles, J.A., Fyer, A.J., and Hamilton, S.P. (2009). Association and linkage analysis of candidate genes GRP, GRPR, CRHR1, and TACR1 in panic disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B, 65-73.
37. Hohla, F., Schally, A.V., Kanashiro, C.A., Buchholz, S., Baker, B., Kannadka, C., Moder, A., Aigner, E., Datz, C., and Halmos, G. (2007). Growth inhibition of non-small-cell lung carcinoma by BN/GRP antagonist is linked with suppression of K-Ras, COX-2, and pAkt. Proc. Natl. Acad. Sci. USA 104, 18671-18676.
38. Hou, W., Tsuda, T., and Jensen, R.T. (1998). Neuromedin B activates phospholipase D through both PKC-dependent and PKC-independent mechanisms. Biochim. Biophys. Acta 1391, 337-350.
39. Ishikawa-Brush, Y., Powell, J.F., Bolton, P., Miller, A.P., Francis, F., Willard, H.F., Lehrach, H., and Monaco, A.P. (1997). Autism and multiple exostoses associated with an X;8 translocation occurring within the GRPR gene and 3' to the SDC2 gene. Hum. Mol. Genet. 6, 1241-1250.
40. Ishola, T.A., Kang, J., Qiao, J., Evers, B.M., and Chung, D.H. (2007). Phosphatidylinositol 3-kinase regulation of gastrin-releasing peptide-induced cell cycle progression in neuroblastoma cells. Biochim. Biophys. Acta 1770, 927-932.
41. Ito, E., Oka, K., Etcheberrigaray, R., Nelson, T.J., McPhie, D.L., Tofel-Grehl, B., Gibson, G.E., and Alkon, D.L. (1994). Internal Ca 2+ mobilization is altered in fibroblasts from patients with Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 534-538.
42. Iwabuchi, M., Ui-Tei, K., Yamada, K., Matsuda, Y., Sakai, Y., Tanaka, K., and Ohki-Hamazaki, H. (2003). Molecular cloning and characterization of avian bombesin-like peptide receptors: new tools for investigating molecular basis for ligand selectivity. Br. J. Pharmacol. 139, 555-566.
43. Izquierdo, I. and Medina, J.H. (1997). Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68, 285-316.
44. Jensen, R.T. and Gardner, J.D. (1981). Identification and characterization of receptors for secretagogues on pancreatic acinar cells. Fed. Proc. 40, 2486-2496.
45. Jensen, R.T., Battey, J.F., Spindel, E.R., and Benya, R.V. (2008). International Union of Pharmacology. LXVIII. Mammalian bombesin receptors: nomenclature, distribution, pharmacology, signaling, and functions in normal and disease states. Pharmacol. Rev. 60, 1-42.
46. Jensen, R.T., Battey, J.F., and Benya, R.V. (2012). Spindel ER. Bombesin receptors. IUPHAR database (IUPHAR-DB). http://www.iuphar-db.org/DATABASE/ FamilyMenuForward?family = 9. Accessed on May 11, 2012.
47. Kamichi, S., Wada, E., Aoki, S., Sekiguchi, M., Kimura, I., and Wada, K. (2005). Immunohistochemical localization of gastrinreleasing peptide receptor in the mouse brain. Brain Res. 1032, 162-170.
48. Kilgore, W.R., Mantyh, P.W., Mantyh, C.R., McVey, D.C., and Vigna, S.R. (1993). Bombesin/GRP-preferring and neuromedin B-preferring receptors in the rat urogenital system. Neuropeptides 24, 43-52.
49. Krane, I.M., Naylor, S.L., Helin-Davis, D., Chin, W.W., and Spindel, E.R. (1988). Molecular cloning of cDNAs encoding the human bombesin-like peptide neuromedin B. Chromosomal localization and comparison to cDNAs encoding its amphibian homolog ranatensin. J. Biol. Chem. 263, 13317-13323.
50. Ladenheim, E.E., Jensen, R.T., Mantey, S.A., McHugh, P.R., and Moran, T.H. (1990). Receptor heterogeneity for bombesin-like peptides in the rat central nervous system. Brain Res. 537, 233-240.
51. Ladenheim, E.E., Jensen, R.T., Mantey, S.A., McHugh, P.R., and Moran, T.H. (1992). Distinct distributions of bombesin receptor subtypes in the rat central nervous system. Brain Res. 593, 168-178.
52. Lebacq-Verheyden, A.M., Krystal, G., Sartor, O., Way, J., and Battey, J.F. (1988). The rat prepro gastrin releasing peptide gene is transcribed from two initiation sites in the brain. Mol. Endocrinol. 2, 556-563.
53. Liu, J., Lao, Z.J., Zhang, J., Schaeffer, M.T., Jiang, M.M., Guan, X.M., Van der Ploeg, L.H., and Fong, T.M. (2002). Molecular basis of the pharmacological difference between rat and human bombesin receptor subtype-3 (BRS-3). Biochemistry 41, 8954-8960.
54. Liu, X., Carlisle, D.L., Swick, M.C., Gaither-Davis, A., Grandis, J.R., and Siegfried, J.M. (2007). Gastrin-releasing peptide activates Akt through the epidermal growth factor receptor pathway and abrogates the effect of gefitinib. Exp. Cell Res. 313, 1361-1372.
55. Luft, T., Flores, D.G., Vianna, M.R., Schwartsmann, G., Roesler, R., and Izquierdo, I. (2006). A role for hippocampal gastrinreleasing peptide receptors in extinction of aversive memory. Neuroreport 17, 935-939.
56. Luft, T., Amaral, O.B., Schwartsmann, G., and Roesler, R. (2008). Transient disruption of fear-related memory by post-retrieval inactivation of gastrin-releasing peptide or N-methyl-Daspartate receptors in the hippocampus. Curr. Neurovasc. Res. 5, 21-27.
57. Martel, G., Hevi, C., Wong, A., Zushida, K., Uchida, S., and Shumyatsky, G.P. (2012). Murine GRPR and stathmin control in opposite directions both cued fear extinction and neural activities of the amygdala and prefrontal cortex. PLoS ONE 7, e30942.
58. Marui, T., Hashimoto, O., Nanba, E., Kato, C., Tochigi, M., Umekage, T., Kato, N., and Sasaki, T. (2004). Gastrin-releasing peptide receptor (GRPR) locus in Japanese subjects with autism. Brain Dev. 26, 5-7.
59. McDonald, T.J., Jornvall, H., Nilsson, G., Vagne, M., Ghatei, M., Bloom, S.R., and Mutt, V. (1979). Characterization of a gastrinreleasing peptide from porcine non-antral gastric tissue. Biochem. Biophys. Res. Commun. 90, 227-233.
60. McGaugh, J.L. (1989). Dissociating learning and performance: drug and hormone enhancement of memory storage. Brain Res. Bull. 23, 339-345.
61. McGaugh, J.L. (2000). Memory: a century of consolidation. Science 287, 248-251.
62. McGaugh, J.L. (2002). Memory consolidation and the amygdala: a systems perspective. Trends Neurosci. 25, 456-461.
63. McGaugh, J.L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1-28.
64. Merali, Z., Kent, P., and Anisman, H. (2002). Role of bombesinrelated peptides in the mediation or integration of the stress response. Cell. Mol. Life Sci. 59, 272-287.
65. Merali, Z., B e dard, T., Andrews, N., Davis, B., McKnight, A.T., Gonzalez, M.I., Pritchard, M., Kent, P., and Anisman, H. (2006a). Bombesin receptors as a novel anti-anxiety therapeutic target: BB1 receptor actions on anxiety through alterations of serotonin activity. J. Neurosci. 26, 10387-10396.
66. Merali, Z., Kent, P., Du, L., Hrdina, P., Palkovits, M., Faludi, G., Poulter, M.O., B e dard, T., and Anisman, H. (2006b). Corticotropin-releasing hormone, arginine vasopressin, gastrin-releasing peptide, and neuromedin B alterations in stress-relevant brain regions of suicides and control subjects. Biol. Psychiatry 59, 594-602.
67. Merali, Z., Mountney, C., Kent, P., and Anisman, H. (2011). Effects of intracerebral ventricular administration of gastrin-releasing peptide and its receptor antagonist RC-3095 on learned fear responses in the rat. Behav. Brain Res. 216, 519-524.
68. Milusheva, E.A., Kortezova, N.I., Mizhorkova, Z.N., Papasova, M., Coy, D.H., Balint, A., Vizi, E.S., and Varga, G. (1998). Role of different bombesin receptor subtypes mediating contractile activity in cat upper gastrointestinal tract. Peptides 19, 549-556.
69. Minamino, N., Kangawa, K., and Matsuo, H. (1983). Neuromedin B: a novel bombesin-like peptide identified in porcine spinal cord. Biochem. Biophys Res. Commun. 114, 541-548.
70. Minamino, N., Kangawa, K., and Matsuo, H. (1984). Neuromedin C: a bombesin-like peptide identified in porcine spinal cord. Biochem. Biophys. Res. Commun. 119, 14-20.
71. Moody, T.W. and Pert, C.B. (1979). Bombesin-like peptides in rat brain: quantitation and biochemical characterization. Biochem. Biophys. Res. Commun. 90, 7-14.
72. Moody, T.W. and Merali, Z. (2004). Bombesin-like peptides and associated receptors within the brain: distribution and behavioral implications. Peptides 25, 511-520.
73. Moody, T.W., Pert, C.B., Rivier, J., and Brown, M.R. (1978). Bombesin: specific binding to rat brain membranes. Proc. Natl. Acad. Sci. USA 75, 5372-5376.
74. Moody, T.W., O'Donohue, T.L., and Jacobowitz, D.M. (1981). Biochemical localization and characterization of bombesin-like peptides in discrete regions of rat brain. Peptides 2, 75-79.
75. Moody, T.W., Getz, R., O'Donohue, T.L., and Rosenstein, J.M. (1988). Localization of receptors for bombesin-like peptides in the rat brain. Ann. N. Y. Acad. Sci. 547, 114-130.
76. Moody, T.W., Staley, J., Zia, F., Coy, D.H., and Jensen, R.T. (1992). Neuromedin B binds with high affinity, elevates cytosolic calcium and stimulates the growth of small cell lung cancer cell lines. J. Pharmacol. Exp. Ther. 263, 311-317.
77. Moody, T.W., Fagarasan, M., and Zia, F. (1995). Neuromedin B stimulates arachidonic acid release, c-fos gene expression, and the growth of C6 glioma cells. Peptides 16, 1133-1140.
78. Mountney, C., Sillberg, V., Kent, P., Anisman, H., and Merali, Z. (2006). The role of gastrin-releasing peptide on conditioned fear: differential cortical and amygdaloid responses in the rat. Psychopharmacology (Berl) 189, 287-296.
79. Mountney, C., Anisman, H., and Merali, Z. (2008). Effects of gastrinreleasing peptide agonist and antagonist administered to the basolateral nucleus of the amygdala on conditioned fear in the rat. Psychopharmacology (Berl) 200, 51-58.
80. Mountney, C., Anisman, H., and Merali, Z. (2011). In vivo levels of corticotropin-releasing hormone and gastrin-releasing peptide at the basolateral amygdala and medial prefrontal cortex in response to conditioned fear in the rat. Neuropharmacology 60, 410-417.
81. Nagalla, S.R., Barry, B.J., Creswick, K.C., Eden, P., Taylor, J.T., and Spindel, E.R. (1995). Cloning of a receptor for amphibian [Phe13]bombesin distinct from the receptor for gastrinreleasing peptide: identification of a fourth bombesin receptor subtype (BB4). Proc. Natl. Acad. Sci. USA 92, 6205-6209.
82. Niebergall-Roth, E. and Singer, M.V. (2001). Central and peripheral neural control of pancreatic exocrine secretion. J. Physiol. Pharmacol. 52, 523-538.
83. Ohki-Hamazaki, H., Wada, E., Matsui, K., and Wada, K. (1997). Cloning and expression of the neuromedin b receptor and the third subtype of bombesin receptor genes in the mouse. Brain Res. 762, 165-172.
84. Ohki-Hamazaki, H., Sakai, Y., Kamata, K., Ogura, H., Okuyama, S., Watase, K., Yamada, K., and Wada, K. (1999). Functional properties of two bombesin-like peptide receptors revealed by the analysis of mice lacking neuromedin B receptor. J. Neurosci. 19, 948-954.
85. Ohki-Hamazaki, H., Iwabuchi, M., and Maekawa, F. (2005). Development and function of bombesin-like peptides and their receptors. Int. J. Dev. Biol. 49, 293-300.
86. Parkman, H.P., Vozzelli, M.A., Pagano, A.P., and Cowan, A. (1994). Pharmacological analysis of receptors for bombesin-related peptides on guinea pig gallbladder smooth muscle. Regul. Pept. 52, 173-180.
87. Preissler, T., Luft, T., Kapczinski, F., Quevedo, J., Schwartsmann, G., and Roesler, R. (2007). Basic fibroblast growth factor prevents the memory impairment induced by gastrin-releasing peptide receptor antagonism in area CA1 of the rat hippocampus. Neurochem. Res. 32, 1381-1386.
88. Presti-Torres, J., de Lima, M.N., Scalco, F.S., Caldana, F., Garcia, V.A., Guimar a es, M.R., Schwartsmann, G., Roesler, R., and Schr o der, N. (2007). Impairments of social behavior and memory after neonatal gastrin-releasing peptide receptor blockade in rats: Implications for an animal model of neurodevelopmental disorders. Neuropharmacology 52, 724-732.
89. Presti-Torres, J., Garcia, V.A., Dornelles, A., Halmenschlager, L.H., Alcalde, L.A., Vedana, G., Rico, E.P., Bogo, M.R., Schwartsmann, G., Roesler, R., et al. (2012). Rescue of social behavior impairment by clozapine and alterations in the expression of neuronal receptors in a rat model of neurodevelopmental impairment induced by GRPR blockade. J. Neural Transm. 119, 319-327.
90. Qin, Y., Ertl, T., Cai, R.Z., Horvath, J.E., Groot, K., and Schally, A.V. (1995). Antagonists of bombesin/gastrin-releasing peptide inhibit growth of SW-1990 human pancreatic adenocarcinoma and production of cyclic AMP. Int. J. Cancer 63, 257-262.
91. Rashidy-Pour, A. and Razvani, M.E. (1998). Unilateral reversible inactivations of the nucleus tractus solitarius and amygdala attenuate the effects of bombesin on memory storage. Brain Res. 814, 127-132.
92. Rettori, V., Pazos-Moura, C.C., Moura, E.G., Polak, J., and McCann, S.M. (1992). Role of neuromedin B in control of the release of thyrotropin in hypothyroid and hyperthyroid rats. Proc. Natl. Acad. Sci. USA 89, 3035-3039.
93. Roesler, R. and Schr o der, N. (2011). Cognitive enhancers: focus on modulatory signaling influencing memory consolidation. Pharmacol. Biochem. Behav. 99, 155-163.
94. Roesler, R., Meller, C.A., Kopschina, M.I., Souza, D.O., Henriques, J.A., and Schwartsmann, G. (2003). Intrahippocampal infusion of the bombesin/gastrin-releasing peptide antagonist RC-3095 impairs inhibitory avoidance retention. Peptides 24, 1069-1074.
95. Roesler, R., Henriques, J.A., and Schwartsmann, G. (2004a). Neuropeptides and anxiety disorders: bombesin receptors as novel therapeutic targets. Trends Pharmacol. Sci. 25, 241-242.
96. Roesler, R., Kopschina, M.I., Rosa, R.M., Henriques, J.A., Souza, D.O., and Schwartsmann, G. (2004b). RC-3095, a bombesin/gastrin-releasing peptide receptor antagonist, impairs aversive but not recognition memory in rats. Eur. J. Pharmacol. 486, 35-41.
97. Roesler, R., Lessa, D., Venturella, R., Vianna, M.R., Luft, T., Henriques, J.A., Izquierdo, I., and Schwartsmann, G. (2004c). Bombesin/gastrin-releasing peptide receptors in the basolateral amygdala regulate memory consolidation. Eur. J. Neurosci. 19, 1041-1045.
98. Roesler, R., Henriques, J.A., and Schwartsmann, G. (2006a). Gastrin-releasing peptide receptor as a molecular target for psychiatric and neurological disorders. CNS Neurol. Disord. Drug Targets 5, 197-204.
99. Roesler, R., Luft, T., Oliveira, S.H., Farias, C.B., Almeida, V.R., Quevedo, J., Dal Pizzol, F., Schr o der, N., Izquierdo, I., and Schwartsmann, G. (2006b). Molecular mechanisms mediating gastrin-releasing peptide receptor modulation of memory consolidation in the hippocampus. Neuropharmacology 51, 350-357.
100. Roesler, R., Kapczinski, F., Quevedo, J., Dal Pizzol, F., and Schwartsmann, G. (2007). The gastrin-releasing peptide receptor as a therapeutic target in central nervous system disorders. Recent Pat. CNS Drug Discov. 2, 125-129.
101. Roesler, R., Valvassori, S.S., Castro, A.A., Luft, T., Schwartsmann, G., and Quevedo, J. (2009). Phosphoinositide 3-kinase is required for bombesin-induced enhancement of fear memory consolidation in the hippocampus. Peptides 30, 1192-1196.
102. Ruff, M., Schiffmann, E., Terranova, V., and Pert, C.B. (1985). Neuropeptides are chemoattractants for human tumor cells and monocytes: a possible mechanism for metastasis. Clin. Immunol. Immunopathol. 37, 387-396.
103. Ryan, R.R., Weber, H.C., Mantey, S.A., Hou, W., Hilburger, M.E., Pradhan, T.K., Coy, D.H., and Jensen, R.T. (1998). Pharmacology and intracellular signaling mechanisms of the native human orphan receptor BRS-3 in lung cancer cells. J. Pharmacol. Exp. Ther. 287, 366-380.
104. Sano, H., Feighner, S.D., Hreniuk, D.L., Iwaasa, H., Sailer, A.W., Pan, J., Reitman, M.L., Kanatani, A., Howard, A.D., and Tan, C.P. (2004). Characterization of the bombesin-like peptide receptor family in primates. Genomics 84, 139-146.
105. Santo-Yamada, Y., Yamada, K., Wada, E., Goto, Y., and Wada, K. (2003). Blockade of bombesin-like peptide receptors impairs inhibitory avoidance learning in mice. Neurosci. Lett. 340, 65-68.
106. Sausville, E.A., Lebacq-Verheyden, A.-M., Spindel, E.R., Cuttitta, F., Gazdar, A.F., and Battey, J.F. (1986). Expression of the gastrinreleasing peptide gene in human small cell lung cancer: evidence for alternative processing resulting in three distinct mRNAs. J. Biol. Chem. 261, 2451-2457.
107. Schubert, M.L., Hightower, J., Coy, D.H., and Makhlouf, G.M. (1991). Regulation of acid secretion by bombesin/GRP neurons of the gastric fundus. Am. J. Physiol. 260, G156 - G160.
108. Schwartsmann, G., DiLeone, L.P., Horowitz, M., Schunemann, D., Cancella, A., Pereira, A.S., Richter, M., Souza, F., da Rocha, A.B., Souza, F.H., et al. (2006). A phase I trial of the bombesin/gastrin-releasing peptide (BN/GRP) antagonist RC3095 in patients with advanced solid malignancies. Invest. New Drugs 24, 403-412.
109. Seidita, G., Mirisola, M., D' Anna, R.P., Gallo, A., Jensen, R.T., Mantey, S.A., Gonzalez, N., Falco, M., Zingale, M., Elia, M., et al. (2008). Analysis of the gastrin-releasing peptide receptor gene in Italian patients with autism spectrum disorders. Am. J. Med. Genet. B Neuropsychiatr. Genet. 147B, 807-813.
110. Severi, C., Jensen, R.T., Erspamer, V., D' Arpino, L., Coy, D.H., Torsoli, A., and Delle Fave, G. (1991). Different receptors mediate the action of bombesin-related peptides on gastric smooth muscle cells. Am. J. Physiol. 260, G683 - G690.
111. Shumyatsky, G.P., Tsvetkov, E., Malleret, G., Vronskaya, S., Hatton, M., Hampton, L., Battey, J.F., Dulac, C., Kandel, E.R., and Bolshakov, V.Y. (2002). Identification of a signaling network in lateral nucleus of amygdala important for inhibiting memory specifically related to learned fear. Cell 111, 905-918.
112. Spindel, E.R., Chin, W.W., Price, J., Rees, L.H., Besser, G.M., and Habener, J.F. (1984). Cloning and characterization of cDNAs encoding human gastrin-releasing peptide. Proc. Natl. Acad. Sci. USA 81, 5699-5703.
113. Spindel, E.R., Zilberberg, M.D., Habener, J.F., and Chin W.W. (1986). Two prohormones for gastrin-releasing peptide are encoded by two mRNAs differing by 19 nucleotides. Proc. Natl. Acad. Sci. USA 83, 19-23.
114. Spindel, E.R., Giladi, E., Brehm, P., Goodman, R.H., and Segerson, T.P. (1990). Cloning and functional characterization of a complementary DNA encoding the murine fibroblast bombesin/gastrin-releasing peptide receptor. Mol. Endocrinol. 4, 1956-1963.
115. Stangelberger, A., Schally, A.V., Varga, J.L., Zarandi, M., Cai, R.Z., Baker, B., Hammann, B.D., Armatis, P., and Kanashiro, C.A. (2005). Inhibition of human androgen-independent PC-3 and DU-145 prostate cancers by antagonists of bombesin and growth hormone releasing hormone is linked to PKC, MAPK and c-jun intracellular signalling. Eur. J. Cancer 41, 2735-2344.
116. Szepeshazi, K., Schally, A.V., Halmos, G., Lamharzi, N., Groot, K., and Horvath, J.E. (1997). A single in vivo administration of bombesin antagonist RC-3095 reduces the levels and mRNA expression of epidermal growth factor receptors in MXT mouse mammary cancers. Proc. Natl. Acad. Sci. USA 94, 10913-10918.
117. Thomas, S.M., Grandis, J.R., Wentzel, A.L., Gooding, W.E., Lui, V.W., and Siegfried, J.M. (2005). Gastrin-releasing peptide receptor mediates activation of the epidermal growth factor receptor in lung cancer cells. Neoplasia 7, 426-431.
118. Venturella, R., Lessa, D., Luft, T., Roozendaal, B., Schwartsmann, G., and Roesler, R. (2005). Dexamethasone reverses the memory impairment induced by antagonism of hippocampal gastrinreleasing peptide receptors. Peptides 26, 821-825.
119. von Schrenck, T., Heinz-Erian, P., Moran, T., Mantey, S.A., Gardner, J.D., and Jensen, R.T. (1989). Neuromedin B receptor in esophagus: evidence for subtypes of bombesin receptors. Am. J. Physiol. 256, G747 - G758.
120. von Schrenck, T., Wang, L.H., Coy, D.H., Villanueva, M.L., Mantey, S., and Jensen, R.T. (1990). Potent bombesin receptor antagonists distinguish receptor subtypes. Am. J. Physiol. 259, G468 - G473.
121. Wada, E., Way, J., Lebacq-Verheyden, A.M., and Battey, J.F. (1990). Neuromedin B and gastrin-releasing peptide mRNAs are differentially distributed in the rat nervous system. J. Neurosci. 10, 2917-2930.
122. Wada, E., Way, J., Shapira, H., Kusano, K., Lebacq-Verheyden, A.M., Coy, D., Jensen, R., and Battey, J. (1991). cDNA cloning, characterization, and brain region-specific expression of a neuromedin B-preferring bombesin receptor. Neuron 6, 421-430.
123. Wada, E., Watase, K., Yamada, K., Ogura, H., Yamano, M., Inomata, Y., Eguchi, J., Yamamoto, K., Sunday, M.E., Maeno, H., et al. (1997). Generation and characterization of mice lacking gastrin-releasing peptide receptor. Biochem. Biophys. Res. Commun. 239, 28-33.
124. Wang, L.H., Battey, J.F., Wada, E., Lin, J.T., Mantey, S., Coy, D.H., and Jensen, R.T. (1992). Activation of neuromedin B-preferring bombesin receptors on rat glioblastoma c-6 cells increases cellular Ca 2+ and phosphoinositides. Biochem. J. 286, 641-648.
125. Weber, H.C., Walters, J., Leyton, J., Casibang, M., Purdom, S., Jensen, R.T., Coy, D.H., Ellis, C., Clark, G., and Moody, T.W. (2001). A bombesin receptor subtype-3 peptide increases nuclear oncogene expression in a MEK-1 dependent manner in human lung cancer cells. Eur. J. Pharmacol. 412, 13-20.
126. Whitley, J.C., Moore, C., Giraud, A.S., and Shulkes, A. (1999). Molecular cloning, genomic organization and selective expression of bombesin receptor subtype 3 in the sheep hypothalamus and pituitary. J. Mol. Endocrinol. 23, 107-116.
127. Williams, C.L. and McGaugh, J.L. (1994). Enhancement of memory processing in an inhibitory avoidance and radial maze task by post-training infusion of bombesin into the nucleus tractus solitarius. Brain Res. 654, 251-256.
128. Wolf, S.S. and Moody, T.W. (1985). Receptors for GRP/bombesin-like peptides in the rat forebrain. Peptides 6, 111-114.
129. Wolf, S.S., Moody, T.W., O'Donohue, T.L., Zarbin, M.A., and Kuhar, M.J. (1983). Autoradiographic visualization of rat brain binding sites for bombesin-like peptides. Eur. J. Pharmacol. 87, 163-164.
130. Wong, S.T., Athos, J., Figueroa, X.A., Pineda, V.V., Schaefer, M.L., Chavkin, C.C., Muglia, L.J., and Storm, D.R. (1999). Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23, 787-798.
131. Yamada, K., Santo-Yamada, Y., and Wada, K. (2003). Stressinduced impairment of inhibitory avoidance learning in female neuromedin B receptor-deficient mice. Physiol. Behav. 78, 303-309.
132. Zarbin, M.A., Kuhar, M.J., O'Donohue, T.L., Wolf, S.S., and Moody, T.W. (1985). Autoradiographic localization of (125 I-Tyr4) bombesin-binding sites in rat brain. J. Neurosci. 5, 429-437.