Altered emotional behaviors in the diabetes mellitus OLETF type 1 congenic rat

Brain Research

Volumn 1178, Issue 1, 2007, Pages 114-124

  Watanabe, Akihito ^a,b   Okuno, Shiro ^b   Okano, Mai ^b   Jordan, Shaun ^c   Aihara, Koutoku ^b   Watanabe, Takeshi K ^b   Yamasaki, Yuki ^b   Kitagawa, Hisashi ^b   Sugawara, Kiyoshi ^a   Kato, Satoru ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b OTSUKA PHARMACEUTICAL CO LTD   (Japan)

^c OTSUKA PHARMACEUTICAL DEVELOPMENT AND COMMERCIALIZATION INC   (United States)

Author keywords

Diabetes mellitus OLETF type 1 (Dmo1); G protein coupled receptor 10 (GPR10); Less anxious behavior; Otsuka Long Evans Tokushima Fatty (OLETF) rat; Prolactin releasing peptide

Indexed keywords

G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 10; PROTEIN C FOS; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONGENIC STRAIN; CONTROLLED STUDY; DIABETES MELLITUS; EMOTION; FEMALE; IMMUNOREACTIVITY; MALE; MAZE TEST; NONHUMAN; OPEN FIELD BEHAVIOR; OTSUKA LONG EVANS TOKUSHIMA FATTY RAT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RAT; STATISTICAL SIGNIFICANCE; THALAMUS MIDLINE NUCLEUS;

AGGRESSION; ALLELES; ANIMALS; ANIMALS, CONGENIC; ANXIETY; AUTORADIOGRAPHY; BEHAVIOR, ANIMAL; BODY WEIGHT; CIRCADIAN RHYTHM; DIABETES MELLITUS, TYPE 1; EMOTIONS; FEMALE; GENES, FOS; GENETIC MARKERS; INJECTIONS, INTRAVENTRICULAR; LIGANDS; MOTOR ACTIVITY; NEURONS; RATS; RATS, INBRED OLETF; SIGNAL TRANSDUCTION;

RATTUS;

EID: 35448932683     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.07.075     Document Type: Article

References (77)

1. Ballaz S., Barber A., Fortuno A., Del Rio J., Martin-Martinez M., Gomez-Monterrey I., Herranz R., Gonzalez-Muniz R., and Garcia-Lopez M.T. Pharmacological evaluation of IQM-95,333, a highly selective CCKA receptor antagonist with anxiolytic-like activity in animal models. Br. J. Pharmacol. 121 (1997) 759-767
2. Bechtold D.A., and Luckman S.M. Prolactin-releasing peptide mediates cholecystokinin-induced satiety in mice. Endocrinology 147 (2006) 4723-4729
3. Bickerdike M.J., Marsden C.A., Dourish C.T., and Fletcher A. The influence of 5-hydroxytryptamine re-uptake blockade on CCK receptor antagonist effects in the rat elevated zero-maze. Eur. J. Pharmacol. 271 (1994) 403-411
4. Bonini J.A., Jones K.A., Adham N., Forray C., Artymyshyn R., Durkin M.M., Smith K.E., Tamm J.A., Boteju L.W., Lakhlani P.P., Raddatz R., Yao W.J., Ogozalek K.L., Boyle N., Kouranova E.V., Quan Y., Vaysse P.J., Wetzel J.M., Branchek T.A., Gerald C., and Borowsky B. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J. Biol. Chem. 275 (2000) 39324-39331
5. Bruhwyler J., Chleide E., Liegeois J.F., Delarge J., and Mercier M. Anxiolytic potential of sulpiride, clozapine and derivatives in the open-field test. Pharmacol. Biochem. Behav. 36 (1990) 57-61
6. Chalmers D.T., Lovenberg T.W., and De Souza E.B. Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression. J. Neurosci. 15 (1995) 6340-6350
7. Covenas R., de Leon M., Cintra A., Bjelke B., Gustafsson J.A., and Fuxe K. Coexistence of c-Fos and glucocorticoid receptor immunoreactivities in the CRF immunoreactive neurons of the paraventricular hypothalamic nucleus of the rat after acute immobilization stress. Neurosci. Lett. 149 (1993) 149-152
8. Crawley J.N. Cholecystokinin-dopamine interactions. Trends Pharmacol. Sci. 12 (1991) 232-236
9. de Kloet E.R., Joels M., and Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev., Neurosci. 6 (2005) 463-475
10. De Souza E.B. Corticotropin-releasing factor receptors: physiology, pharmacology, biochemistry and role in central nervous system and immune disorders. Psychoneuroendocrinology 20 (1995) 789-819
11. Ellacott K.L., Donald E.L., Clarkson P., Morten J., Masters D., Brennand J., and Luckman S.M. Characterization of a naturally-occurring polymorphism in the UHR-1 gene encoding the putative rat prolactin-releasing peptide receptor. Peptides 26 (2005) 675-681
12. Engstrom M., Brandt A., Wurster S., Savola J.M., and Panula P. Prolactin releasing peptide has high affinity and efficacy at neuropeptide FF2 receptors. J. Pharmacol. Exp. Ther. 305 (2003) 825-832
13. Fujii R., Fukusumi S., Hosoya M., Kawamata Y., Habata Y., Hinuma S., Sekiguchi M., Kitada C., Kurokawa T., Nishimura O., Onda H., Sumino Y., and Fujino M. Tissue distribution of prolactin-releasing peptide (PrRP) and its receptor. Regul. Pept. 83 (1999) 1-10
14. Griebel G., Perrault G., and Sanger D.J. Characterization of the behavioral profile of the non-peptide CRF receptor antagonist CP-154,526 in anxiety models in rodents. Comparison with diazepam and buspirone. Psychopharmacology (Berl) 138 (1998) 55-66
15. Gu W., Geddes B.J., Zhang C., Foley K.P., and Stricker-Krongrad A. The prolactin-releasing peptide receptor (GPR10) regulates body weight homeostasis in mice. J. Mol. Neurosci. 22 (2004) 93-103
16. Heinrichs S.C., Lapsansky J., Lovenberg T.W., De Souza E.B., and Chalmers D.T. Corticotropin-releasing factor CRF1, but not CRF2, receptors mediate anxiogenic-like behavior. Regul. Pept. 71 (1997) 15-21
17. Hendrie C.A., Neill J.C., Shepherd J.K., and Dourish C.T. The effects of CCKA and CCKB antagonists on activity in the black/white exploration model of anxiety in mice. Physiol. Behav. 54 (1993) 689-693
18. Hill D.R., Campbell N.J., Shaw T.M., and Woodruff G.N. Autoradiographic localization and biochemical characterization of peripheral type CCK receptors in rat CNS using highly selective nonpeptide CCK antagonists. J. Neurosci. 7 (1987) 2967-2976
19. Hinuma S., Habata Y., Fujii R., Kawamata Y., Hosoya M., Fukusumi S., Kitada C., Masuo Y., Asano T., Matsumoto H., Sekiguchi M., Kurokawa T., Nishimura O., Onda H., and Fujino M. A prolactin-releasing peptide in the brain. Nature 393 (1998) 272-276
20. Honda T., Wada E., Battey J.F., and Wank S.A. Differential gene expression of CCKA and CCKB receptors in the rat brain. Mol. Cell. Neurosci. 4 (1993) 143-154
21. Hsu D.T., Chen F.L., Takahashi L.K., and Kalin N.H. Rapid stress-induced elevations in corticotropin-releasing hormone mRNA in rat central amygdala nucleus and hypothalamic paraventricular nucleus: an in situ hybridization analysis. Brain Res. 788 (1998) 305-310
22. Imaki T., Shibasaki T., Hotta M., and Demura H. Early induction of c-fos precedes increased expression of corticotropin-releasing factor messenger ribonucleic acid in the paraventricular nucleus after immobilization stress. Endocrinology 131 (1992) 240-246
23. Imaki T., Shibasaki T., Hotta M., and Demura H. Intracerebroventricular administration of corticotropin-releasing factor induces c-fos mRNA expression in brain regions related to stress responses: comparison with pattern of c-fos mRNA induction after stress. Brain Res. 616 (1993) 114-125
24. Jhamandas J.H., and MacTavish D. Central administration of neuropeptide FF causes activation of oxytocin paraventricular hypothalamic neurones that project to the brainstem. J. Neuroendocrinol. 15 (2003) 24-32
25. Kalin N.H., Takahashi L.K., and Chen F.L. Restraint stress increases corticotropin-releasing hormone mRNA content in the amygdala and paraventricular nucleus. Brain Res. 656 (1994) 182-186
26. Kamilaris T.C., Johnson E.O., Calogero A.E., Kalogeras K.T., Bernardini R., Chrousos G.P., and Gold P.W. Cholecystokinin-octapeptide stimulates hypothalamic-pituitary-adrenal function in rats: role of corticotropin-releasing hormone. Endocrinology 130 (1992) 1764-1774
27. Kanemoto N., Hishigaki H., Miyakita A., Oga K., Okuno S., Tsuji A., Takagi T., Takahashi E., Nakamura Y., and Watanabe T.K. Genetic dissection of "OLETF", a rat model for non-insulin-dependent diabetes mellitus. Mamm. Genome 9 (1998) 419-425
28. Kato S., Ishita S., Sugawara K., and Mawatari K. Cystine/glutamate antiporter expression in retinal Muller glial cells: implications for dl-alpha-aminoadipate toxicity. Neuroscience 57 (1993) 473-482
29. Katsuura G., Ibii N., and Matsushita A. Activation of CCK-A receptors induces elevation of plasma corticosterone in rats. Peptides 13 (1992) 203-205
30. Kawano K., Hirashima T., Mori S., Saitoh Y., Kurosumi M., and Natori T. Spontaneous long-term hyperglycemic rat with diabetic complications. Otsuka Long-Evans Tokushima Fatty (OLETF) strain. Diabetes 41 (1992) 1422-1428
31. Keck M.E., and Holsboer F. Hyperactivity of CRH neuronal circuits as a target for therapeutic interventions in affective disorders. Peptides 22 (2001) 835-844
32. Keck M.E., Welt T., Wigger A., Renner U., Engelmann M., Holsboer F., and Landgraf R. The anxiolytic effect of the CRH(1) receptor antagonist R121919 depends on innate emotionality in rats. Eur. J. Neurosci. 13 (2001) 373-380
33. Laurent P., Becker J.A., Valverde O., Ledent C., de Kerchove d'Exaerde A., Schiffmann S.N., Maldonado R., Vassart G., and Parmentier M. The prolactin-releasing peptide antagonizes the opioid system through its receptor GPR10. Nat. Neurosci. 8 (2005) 1735-1741
34. Lawrence C.B., Celsi F., Brennand J., and Luckman S.M. Alternative role for prolactin-releasing peptide in the regulation of food intake. Nat. Neurosci. 3 (2000) 645-646
35. Lawrence C.B., Ellacott K.L., and Luckman S.M. PRL-releasing peptide reduces food intake and may mediate satiety signaling. Endocrinology 143 (2002) 360-367
36. Li X.L., Aou S., Hori T., and Oomura Y. Spatial memory deficit and emotional abnormality in OLETF rats. Physiol. Behav. 75 (2002) 15-23
37. Liebsch G., Landgraf R., Gerstberger R., Probst J.C., Wotjak C.T., Engelmann M., Holsboer F., and Montkowski A. Chronic infusion of a CRH1 receptor antisense oligodeoxynucleotide into the central nucleus of the amygdala reduced anxiety-related behavior in socially defeated rats. Regul. Pept. 59 (1995) 229-239
38. Liebsch G., Landgraf R., Engelmann M., Lorscher P., and Holsboer F. Differential behavioural effects of chronic infusion of CRH 1 and CRH 2 receptor antisense oligonucleotides into the rat brain. J. Psychiatr. Res. 33 (1999) 153-163
39. Lin S.H., Leslie F.M., and Civelli O. Neurochemical properties of the prolactin releasing peptide (PrRP) receptor expressing neurons: evidence for a role of PrRP as a regulator of stress and nociception. Brain Res. 952 (2002) 15-30
40. Lin S.H., and Civelli O. Orphan G protein-coupled receptors: targets for new therapeutic interventions. Ann. Med. 36 (2004) 204-214
41. Marchese A., Heiber M., Nguyen T., Heng H.H., Saldivia V.R., Cheng R., Murphy P.M., Tsui L.C., Shi X., Gregor P., et al. Cloning and chromosomal mapping of three novel genes, GPR9, GPR10, and GPR14, encoding receptors related to interleukin 8, neuropeptide Y, and somatostatin receptors. Genomics 29 (1995) 335-344
42. Maruyama M., Matsumoto H., Fujiwara K., Kitada C., Hinuma S., Onda H., Fujino M., and Inoue K. Immunocytochemical localization of prolactin-releasing peptide in the rat brain. Endocrinology 140 (1999) 2326-2333
43. Maruyama M., Matsumoto H., Fujiwara K., Noguchi J., Kitada C., Hinuma S., Onda H., Nishimura O., Fujino M., Higuchi T., and Inoue K. Central administration of prolactin-releasing peptide stimulates oxytocin release in rats. Neurosci. Lett. 276 (1999) 193-196
44. Maruyama M., Matsumoto H., Fujiwara K., Noguchi J., Kitada C., Fujino M., and Inoue K. Prolactin-releasing peptide as a novel stress mediator in the central nervous system. Endocrinology 142 (2001) 2032-2038
45. Matsumoto H., Maruyama M., Noguchi J., Horikoshi Y., Fujiwara K., Kitada C., Hinuma S., Onda H., Nishimura O., Inoue K., and Fujino M. Stimulation of corticotropin-releasing hormone-mediated adrenocorticotropin secretion by central administration of prolactin-releasing peptide in rats. Neurosci. Lett. 285 (2000) 234-238
46. Mera T., Fujihara H., Kawasaki M., Hashimoto H., Saito T., Shibata M., Saito J., Oka T., Tsuji S., Onaka T., and Ueta Y. Prolactin-releasing peptide is a potent mediator of stress responses in the brain through the hypothalamic paraventricular nucleus. Neuroscience 141 (2006) 1069-1086
47. Okuno S., Watanabe T.K., Ono T., Yamasaki Y., Goto Y., Miyao H., Asai T., Kanemoto N., Oga K., Mizoguchi-Miyakita A., Takagi T., Takahashi E., Nakamura Y., and Tanigami A. Genetic determinants of plasma triglyceride levels in (OLETF × BN) × OLETF backcross rats. Genomics 62 (1999) 350-355
48. Okuno S., Watanabe T.K., Ono T., Oga K., Mizoguchi-Miyakita A., Yamasaki Y., Goto Y., Shinomiya H., Momota H., Miyao H., Hayashi I., Asai T., Suzuki M., Harada Y., Hishigaki H., Wakitani S., Takagi T., Nakamura Y., and Tanigami A. Effects of Dmo1 on obesity, dyslipidaemia and hyperglycaemia in the Otsuka Long Evans Tokushima Fatty strain. Genet. Res. 77 (2001) 183-190
49. Okuno S., Kondo M., Yamasaki Y., Miyao H., Ono T., Iwanaga T., Omori K., Okano M., Suzuki M., Momota H., Hishigaki H., Hayashi I., Goto Y., Shinomiya H., Harada Y., Hirashima T., Kanemoto N., Asai T., Wakitani S., Takagi T., Nakamura Y., Tanigami A., and Watanabe T.K. Substitution of Dmo1 with normal alleles results in decreased manifestation of diabetes in OLETF rats. Diabetes Obes. Metab. 4 (2002) 309-318
50. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, New York
51. Pellow S., and File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol. Biochem. Behav. 24 (1986) 525-529
52. Pezzone M.A., Lee W.S., Hoffman G.E., and Rabin B.S. Induction of c-Fos immunoreactivity in the rat forebrain by conditioned and unconditioned aversive stimuli. Brain Res. 597 (1992) 41-50
53. Preil J., Muller M.B., Gesing A., Reul J.M., Sillaber I., van Gaalen M.M., Landgrebe J., Holsboer F., Stenzel-Poore M., and Wurst W. Regulation of the hypothalamic-pituitary-adrenocortical system in mice deficient for CRH receptors 1 and 2. Endocrinology 142 (2001) 4946-4955
54. Rodgers R.J., Cao B.J., Dalvi A., and Holmes A. Animal models of anxiety: an ethological perspective. Braz. J. Med. Biol. Res. 30 (1997) 289-304
55. Roland B.L., Sutton S.W., Wilson S.J., Luo L., Pyati J., Huvar R., Erlander M.G., and Lovenberg T.W. Anatomical distribution of prolactin-releasing peptide and its receptor suggests additional functions in the central nervous system and periphery. Endocrinology 140 (1999) 5736-5745
56. Samson W.K., Keown C., Samson C.K., Samson H.W., Lane B., Baker J.R., and Taylor M.M. Prolactin-releasing peptide and its homolog RFRP-1 act in hypothalamus but not in anterior pituitary gland to stimulate stress hormone secretion. Endocrine 20 (2003) 59-66
57. Saunders J., and Williams J. Antagonists of the corticotropin releasing factor receptor. Prog. Med. Chem. 41 (2003) 195-247
58. Seal L.J., Small C.J., Dhillo W.S., Kennedy A.R., Ghatei M.A., and Bloom S.R. Prolactin-releasing peptide releases corticotropin-releasing hormone and increases plasma adrenocorticotropin via the paraventricular nucleus of the hypothalamus. Neuroendocrinology 76 (2002) 70-78
59. Shibasaki T., Imaki T., Hotta M., Ling N., and Demura H. Psychological stress increases arousal through brain corticotropin-releasing hormone without significant increase in adrenocorticotropin and catecholamine secretion. Brain Res. 618 (1993) 71-75
60. Skutella T., Probst J.C., Renner U., Holsboer F., and Behl C. Corticotropin-releasing hormone receptor (type I) antisense targeting reduces anxiety. Neuroscience 85 (1998) 795-805
61. Smith G.W., Aubry J.M., Dellu F., Contarino A., Bilezikjian L.M., Gold L.H., Chen R., Marchuk Y., Hauser C., Bentley C.A., Sawchenko P.E., Koob G.F., Vale W., and Lee K.F. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20 (1998) 1093-1102
62. Steckler T., and Holsboer F. Corticotropin-releasing hormone receptor subtypes and emotion. Biol. Psychiatry 46 (1999) 1480-1508
63. Takahashi L.K., Kalin N.H., Vanden Burgt J.A., and Sherman J.E. Corticotropin-releasing factor modulates defensive-withdrawal and exploratory behavior in rats. Behav. Neurosci. 103 (1989) 648-654
64. Takiguchi S., Takata Y., Funakoshi A., Miyasaka K., Kataoka K., Fujimura Y., Goto T., and Kono A. Disrupted cholecystokinin type-A receptor (CCKAR) gene in OLETF rats. Gene 197 (1997) 169-175
65. Takiguchi S., Takata Y., Takahashi N., Kataoka K., Hirashima T., Kawano K., Miyasaka K., Funakoshi A., and Kono A. A disrupted cholecystokinin A receptor gene induces diabetes in obese rats synergistically with ODB1 gene. Am. J. Physiol. 274 (1998) E265-E270
66. Timpl P., Spanagel R., Sillaber I., Kresse A., Reul J.M., Stalla G.K., Blanquet V., Steckler T., Holsboer F., and Wurst W. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat. Genet. 19 (1998) 162-166
67. Tobe I., Ishida Y., Tanaka M., Endoh H., Fujioka T., and Nakamura S. Effects of repeated maternal stress on FOS expression in the hypothalamic paraventricular nucleus of fetal rats. Neuroscience 134 (2005) 387-395
68. Van Pett K., Viau V., Bittencourt J.C., Chan R.K., Li H.Y., Arias C., Prins G.S., Perrin M., Vale W., and Sawchenko P.E. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 428 (2000) 191-212
69. Wang L., Martinez V., Barrachina M.D., and Tache Y. Fos expression in the brain induced by peripheral injection of CCK or leptin plus CCK in fasted lean mice. Brain Res. 791 (1998) 157-166
70. Watanabe T.K., Okuno S., Oga K., Mizoguchi-Miyakita A., Tsuji A., Yamasaki Y., Hishigaki H., Kanemoto N., Takagi T., Takahashi E., Irie Y., Nakamura Y., and Tanigami A. Genetic dissection of "OLETF", a rat model for non-insulin-dependent diabetes mellitus: quantitative trait locus analysis of (OLETF × BN) × OLETF. Genomics 58 (1999) 233-239
71. Watanabe T.K., Ono T., Okuno S., Mizoguchi-Miyakita A., Yamasaki Y., Kanemoto N., Hishigaki H., Oga K., Takahashi E., Irie Y., Bihoreau M.T., James M.R., Lathrop G.M., Takagi T., Nakamura Y., and Tanigami A. Characterization of newly developed SSLP markers for the rat. Mamm. Genome 11 (2000) 300-305
72. Watanabe T.K., Okuno S., Ono T., Yamasaki Y., Oga K., Mizoguchi-Miyakita A., Miyao H., Suzuki M., Momota H., Goto Y., Shinomiya H., Hishigaki H., Hayashi I., Asai T., Wakitani S., Takagi T., Nakamura Y., and Tanigami A. Single-allele correction of the Dmo1 locus in congenic animals substantially attenuates obesity, dyslipidaemia and diabetes phenotypes of the OLETF rat. Clin. Exp. Pharmacol. Physiol. 28 (2001) 28-42
73. Watanabe T.K., Suzuki M., Yamasaki Y., Okuno S., Hishigaki H., Ono T., Oga K., Mizoguchi-Miyakita A., Tsuji A., Kanemoto N., Wakitani S., Takagi T., Nakamura Y., and Tanigami A. Mutated G-protein-coupled receptor GPR10 is responsible for the hyperphagia/dyslipidaemia/obesity locus of Dmo1 in the OLETF rat. Clin. Exp. Pharmacol. Physiol. 32 (2005) 355-366
74. Yamamoto Y., Akiyoshi J., Kiyota A., Katsuragi S., Tsutsumi T., Isogawa K., and Nagayama H. Increased anxiety behavior in OLETF rats without cholecystokinin-A receptor. Brain Res. Bull. 53 (2000) 789-792
75. Yamasaki Y., Watanabe T.K., Okuno S., Ono T., Oga K., Mizoguchi-Miyakita A., Goto Y., Shinomiya H., Momota H., Miyao H., Hayashi I., Asai T., Suzuki M., Harada Y., Hishigaki H., Wakitani S., Takagi T., Nakamura Y., and Tanigami A. Quantitative trait loci for lipid metabolism in the study of OLETF × (OLETF × Fischer 344) backcross rats. Clin. Exp. Pharmacol. Physiol. 27 (2000) 881-886
76. Zhang S.Q., Kimura M., and Inoue S. Effects of prolactin-releasing peptide (PrRP) on sleep regulation in rats. Psychiatry Clin. Neurosci. 54 (2000) 262-264
77. Zorrilla E.P., and Koob G.F. The therapeutic potential of CRF1 antagonists for anxiety. Expert Opin. Investig. Drugs 13 (2004) 799-828