Anatomical characterization of bombesin receptor subtype-3 mRNA expression in the rodent central nervous system

Journal of Comparative Neurology

Volumn 521, Issue 5, 2013, Pages 1020-1039

  Zhang, Li ^a,b   Parks, Gregory S ^a   Wang, Zhiwei ^a   Wang, Lien ^a   Lew, Michelle ^a   Civelli, Olivier ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

BRS 3; Corticotropin releasing factor; Growth hormone releasing hormone; Hypothalamus; In situ hybridization; Neurochemical

Indexed keywords

BOMBESIN RECEPTOR; BOMBESIN RECEPTOR 3; CORTICOTROPIN RELEASING FACTOR; GONADORELIN; GROWTH HORMONE RELEASING FACTOR; KISSPEPTIN; MELANIN CONCENTRATING HORMONE; MESSENGER RNA; NEUROPEPTIDE Y; OREXIN; PROOPIOMELANOCORTIN; PROTIRELIN; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DIENCEPHALON; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; EMOTION; ENERGY METABOLISM; FEMALE; GABAERGIC SYSTEM; GENE EXPRESSION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; TELENCEPHALON; TISSUE DISTRIBUTION;

ANIMALS; ARABIDOPSIS PROTEINS; CENTRAL NERVOUS SYSTEM; FEMALE; GLUTAMATE DECARBOXYLASE; IN SITU HYBRIDIZATION; INTRAMOLECULAR TRANSFERASES; MALE; MICE; MICE, INBRED C57BL; PEPTIDE HORMONES; PRO-OPIOMELANOCORTIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, BOMBESIN; TYROSINE 3-MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 84873811970     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23216     Document Type: Article

References (60)

1. Carboni L, Carletti R, Tacconi S, Corti C, Ferraguti F. 1998. Differential expression of SAPK isoforms in the rat brain. An in situ hybridization study in the adult rat brain and during post-natal development. Brain Res Mol Brain Res 60: 57-68.
2. Clark SD, Nothacker HP, Wang Z, Saito Y, Leslie FM, Civelli O. 2001. The urotensin II receptor is expressed in the cholinergic mesopontine tegmentum of the rat. Brain Res 923: 120-127.
3. Coll AP. 2010. Treating obesity? It's in the bag! Cell Metab 11: 95-96.
4. Collin M, Bäckberg M, Ovesjö ML, Fisone G, Edwards RH, Fujiyama F, Meister B. 2003. Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weight. Eur J Neurosci 18: 1265-1278.
5. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett IIFS, Frankel WN, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG. 1998. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95: 322-327.
6. Fathi Z, Corjay MH, Shapira H, Wada E, Benya R, Jensen R, Viallet J, Sausville EA, Battey JF. 1993. BRS-3: a novel bombesin receptor subtype selectively expressed in testis and lung carcinoma cells. J Biol Chem 268: 5979-5984.
7. Franklin K, Paxinos G. 2007. The mouse brain in stereotaxic coordinates. Third edition. New York: Elsevier Academic Press.
8. Gonzalez N, Moody TW, Igarashi H, Ito T, Jensen RT. 2008. Bombesin-related peptides and their receptors: recent advances in the role in physiology and disease states. Curr Opin Endocrinol Diabetes Obes 15: 58-64.
9. Gorbulev V, Akhundova A, Büchner H, Fahrenholz F. 1992. Molecular cloning of a new bombesin receptor subtype expressed in uterus during pregnancy. Eur J Biochem 208: 405-410.
10. Guan XM, Chen H, Dobbelaar PH, Dong Y, Fong TM, Gagen K, Gorski J, He S, Howard AD, Jian T, Jiang M, Kan Y, Kelly TM, Kosinski J, Lin LS, Liu J, Marsh DJ, Metzger JM, Miller R, Nargund RP, Palyha O, Shearman L, Shen Z, Stearns R, Strack AM, Stribling S, Tang YS, Wang SP, White A, Yu H, Reitman ML. 2010. Regulation of energy homeostasis by bombesin receptor subtype-3: selective receptor agonists for the treatment of obesity. Cell Metab 11: 101-112.
11. Guan XM, Metzger JM, Yang L, Raustad KA, Wang SP, Spann SK, Kosinski JA, Yu H, Shearman LP, Faidley TD, Palyha O, Kan Y, Kelly TM, Sebhat I, Lin LS, Dragovic J, Lyons KA, Craw S, Nargund RP, Marsh DJ, Strack AM, Reitman ML. 2011. Antiobesity effect of MK-5046, a novel bombesin receptor subtype-3 agonist. J Pharmacol Exp Ther 336: 356-364.
12. Harrold JA, Widdowson PS, Williams G. 1999. Altered energy balance causes selective changes in melanocortin-4 (MC4-R), but not melanocortin-3 (MC3-R), receptors in specific hypothalamic regions: further evidence that activation of MC4-R is a physiological inhibition of feeding. Diabetes 48: 267-271.
13. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C. 1991. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41: 89-125.
14. Heinrichs SC, Koob GF. 2004. Corticotropin-releasing factor in brain: a role in activation, arousal and affect regulation. J Pharmacol Exp Ther 311: 427-440.
15. Herbert H, Saper CB. 1990. Cholecystokinin-, galanin-, and corticotrophin-releasing factor-like immunoreactive projections from the nucleus of the solitary tract to the parabrachial nucleus in the rat. J Comp Neurol 293: 581-598.
16. Herkenham M, Nauta WJ. 1977. Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173: 123-146.
17. Herkenham M, Nauta WJ. 1979. Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187: 19-47.
18. Hoffman BJ, Hansson SR, Mezey E, Palkovits M. 1998. Localization and dynamic regulation of biogenic amine transporters in the mammalian central nervous system. Front Neuroendocrinol 19: 187-231.
19. Jennings CA, Harrison DC, Maycox PR, Crook B, Smart D, Hervieu GJ. 2003. The distribution of the orphan bombesin receptor subtype-3 in the rat CNS. Neuroscience 120: 309-324.
20. Jensen RT, Battey JF, Spindel ER, Benya RV. 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.
21. Kim U. 2009. Topographic commissural and descending projections of the habenula in the rat. J Comp Neurol 513: 173-187.
22. Koob GF, Heinrichs SC. 1999. A role for corticotrophin releasing factor and urocortin in behavioral responses to stressors. Brain Res 848: 141-152.
23. Krukoff TL, Harris KH, Jhamandas JH. 1993. Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Res Bull 30: 163-172.
24. Ladenheim EE, Hamilton NL, Behles RR, Bi S, Hampton LL, Battey JF, Moran TH. 2008. Factors contributing to obesity in bombesin receptor subtype-3-deficient mice. Endocrinology 149: 971-978.
25. Lauterborn JC, Isackson PJ, Montalvo R, Gall CM. 1993. In situ hybridization localization of choline acetyltransferase mRNA in adult rat brain and spinal cord. Brain Res Mol Brain Res 17: 59-69.
26. Lauterio TJ, Perez FM. 1997. Growth hormone secretion and synthesis are depressed in obesity-susceptible compared with obesity-resistant rats. Metabolism 46: 210-216.
27. Liu JY, Pan JT. 1994. Stimulatory effects of bombesin-like peptides on hypothalamic arcuate neurons in rat brain slices. Brain Res Bull 35: 241-246.
28. Liu J, Lao ZJ, Zhang J, Schaeffer MT, Jiang MM, Guan XM, Van del Ploeg LHT, Fong TM. 2002. Molecular basis of the pharmacological difference between rat and human bombesin receptor subtype-3 (BRS-3). Biochemistry 41: 8954-8960.
29. Long JA, Evans HM. 1922. The estrous cycle in the rat and its associated phenomena. Memories of University of California. 6: 1-148.
30. Maekawa F, Quah HM, Tanaka K, Ohki-Hamazaki H. 2004. Leptin resistance and enhancement of feeding facilitation by melanin-concentrating hormone in mice lacking bombesin receptor subtype-3. Diabetes 53: 570-576.
31. Majumdar ID, Weber HC. 2012. Appetite-modifying effects of bombesin receptor subtype-3 agonists. Handb Exp Pharmacol 209: 405-432.
32. Mandl AM. 1951. The phases of the oestrous cycle in the adult white rat. J Exp Biol 28: 576-584.
33. Mantey SA, Weber HC, Sainz E, Akeson M, Ryan, Pradhan TK, Searles RP, Spindel ER, Battey JF, Coy DH, Jensen RT. 1997. Discovery of a high affinity radioligand for the human orphan receptor, bombesin receptor subtype 3, which demonstrates that it has a unique pharmacology compared with other mammalian bombesin receptors. J Biol Chem 272: 26062-26071.
34. Marcondes FK, Bianchi FJ, Tanno AP. 2002. Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 62( 4A): 609-614.
35. Martin DL, Rimvall K. 1993. Regulation of gamma-aminobutyric acid synthesis in the brain. J Neurochem 60: 395-407.
36. Meister B. 2007. Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol Behav 92: 263-271.
37. Ohki-Hamazaki H, Watase K, Yamamoto K, Ogura H, Yamano M, Yamada K, Maeno H, Imaki J, Kikuyama S, Wada E, Wada K. 1997a. Mice lacking bombesin receptor subtype-3 develop metabolic defects and obesity. Nature 390: 165-169.
38. Ohki-Hamazaki H, Wada E, Matsui K, Wada K. 1997b. Cloning and expression of the neuromedin B receptor and the third subtype of bombesin receptor genes in the mouse. Brain Res 762: 165-172.
39. Paxinos G, Watson C. 2009. The rat brain in stereotaxic coordinates. Compact sixth edition. New York: Academic Press.
40. Qi Y, Namavar MR, Iqbal J, Oldfield BJ, Clarke IJ. 2009. Characterization of the projections to the hypothalamic paraventricular and periventricular nuclei in the female sheep brain, using retrograde tracing and immunohistochemistry. Neuroendocrinology 90: 31-53.
41. Qu D, Ludwig DS, Gammeltoft S, Piper M, Pelleymounter MA, Cullen MJ, Mathes WF, Przypek R, Kanarek R, Maratos-Flier E. 1996. A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380: 243-247.
42. Regard JB, Sato IT, Coughlin SR. 2008. Anatomical profiling of G protein-coupled receptor expression. Cell 135: 561-571.
43. Reilly S. 1999. The parabrachial nucleus and conditioned taste aversion. Brain Res Bull 48: 239-254.
44. Sah P, Faber ES, Lopez De Armentia M, Power J. 2003. The amygdaloid complex: anatomy and physiology. Physiol Rev 83: 803-834.
45. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M. 1998. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92: 573-585.
46. Sano H, Feighner SD, Hreniuk DL, Iwaasa H, Sailer AW, Pan J, Reitman MI, Kanatani A, Howard AD, Tan CP. 2004. Characterization of the bombesin-like peptide receptor family in primates. Genomics 84: 139-146.
47. Saper CB, Loewy AD. 1980. Efferent connections of the parabrachial nucleus in the rat. Brain Res 197: 291-317.
48. Shelton L, Becerra L, Borsook D. 2012. Unmasking the mysteries of the habenula in pain and analgesia. Prog Neurobiol 96: 208-219.
49. Silver R, Silverman AJ, Vitkovic L, Lederhendler II. 1996. Mast cells in the brain: evidence and functional significance. Trends Neurosci 19: 25-31.
50. Sugama S, Cho BP, Baker H, Joh TH, Lucero J, Conti B. 2002. Neurons of the superior nucleus of the medial habenula and ependymal cells express IL-18 in rat CNS. Brain Res 958: 1-9.
51. Tannenbaum GS, Lapointe M, Gurd W, Finkelstein JA. 1990. Mechanisms of impaired growth hormone secretion in the genetically obese Zucker rats: Role of growth hormone-releasing factor and somatostatin. Endocrinology 127: 3087-3095.
52. Toppila J, Alanko L, Asikaninen M, Tobler I, Stenberg D, Porkka-Heiskanen T. 1997. Sleep deprivation increases somatostatin and growth hormone-releasing hormone messenger RNA in the rat hypothalamus. J Sleep Res 6: 171-178.
53. Xu YL, Gall CM, Jackson VR, Civelli O, Reinscheid RK. 2007. Distribution of neuropeptide S receptor mRNA and neurochemical characteristics of neuropeptide S-expressing neurons in the rat brain. J Comp Neurol 500: 84-102.
54. Xu X, Coats JK, Yang CF, Wang A, Ahmed OM, Alvarado M, Izumi T, Shah NM. 2012. Modular genetic control of sexually dimorphic behaviors. Cell 148: 596-607.
55. Yamada K, Wada E, Imaki J, Ohki-Hamazaki H, Wada K. 1999. Hyperresponsiveness to palatable and aversive taste stimuli in genetically obese (bombesin receptor subtype-3-deficient) mice. Physiol Behav 66: 863-867.
56. Yamada K, Ohki-Hamazaki H, Wada K. 2000. Differential effects of social isolation upon body weight, food consumption, and responsiveness to novel and social environment in bombesin receptor subtype-3 (BRS-3) deficient mice. Physio Behav 68: 555-561.
57. Yamada K, Santo-Yamada Y, Wada E, Wada K. 2002. Role of bombesin (BN)-like peptides/receptors in emotional behavior by comparison of three strains of BN-like peptide receptor knockout mice. Mol Psychiatry 7: 113-117.
58. Yamamoto T, Shimura T, Sako N, Yasoshima Y, Sakai N. 1994. Neural substrates for conditioned taste aversion in the rat. Behav Brain Res 65: 123-137.
59. Zhang L, Nothacker HP, Wang Z, Bohn LM, Civelli O. 2009. Pharmacological characterization of a selective agonist for bombesin receptor subtype-3. Biochem Biophys Res Commun 387: 283-288.
60. Ziegler DR, Cullinan WE, Herman JP. 2002. Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J Comp Neurol 448: 217-229.