Cortagine infused into the medial prefrontal cortex attenuates predator-induced defensive behaviors and Fos protein production in selective nuclei of the amygdala in male CD1 mice

Hormones and Behavior

Volumn 64, Issue 3, 2013, Pages 519-526

  Pentkowski, Nathan S ^a,b   Tovote, Philip ^a,c   Zavala, Arturo R ^d   Litvin, Yoav ^a,b   Blanchard, D Caroline ^a,b,c   Spiess, Joachim ^a,c,e   Blanchard, Robert J ^a,b  

^a UNIVERSITY OF HAWAII   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c UNIVERSITY OF HAWAII   (United States)

^d CALIFORNIA STATE UNIVERSITY   (United States)

^e BURNHAM INSTITUTE   (United States)

Author keywords

Anxiety; Corticotropin releasing factor; CRF; Defense; Emotion; Fear; PFC

Indexed keywords

ASTRESSIN; CORTAGINE; CORTICOTROPIN RELEASING FACTOR DERIVATIVE; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; PROTEIN FOS; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; ELECTROENCEPHALOGRAM; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SYNTHESIS; MALE; MOUSE; NERVE STIMULATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANXIETY; CORTICOTROPIN-RELEASING FACTOR; CRF; DEFENSE; EMOTION; FEAR; PFC;

AMYGDALA; ANIMALS; BEHAVIOR, ANIMAL; CELL NUCLEUS; CORTICOTROPIN-RELEASING HORMONE; DOMINANCE-SUBORDINATION; ESCAPE REACTION; FOOD CHAIN; INFUSIONS, INTRAVENTRICULAR; MALE; MICE; ONCOGENE PROTEINS V-FOS; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; RECOMBINANT FUSION PROTEINS;

EID: 84884167298     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.06.008     Document Type: Article

References (68)

1. Bale T.L. Sensitivity to stress: dysregulation of CRF pathways and disease development. Horm. Behav. 2005, 48:1-10.
2. Bale T.L., Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 2004, 44:525-557.
3. Bale T.L., Contarino A., Smith G.W., Chan R., Gold L.H., Sawchenko P.E., Koob G.F., Vale W.W., Lee K.F. Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nat. Genet. 2000, 24:410-414.
4. Bi L.L., Wang J., Luo Z.Y., Chen S.P., Geng F., Chen Y.H., Li S.J., Yuan C.H., Lin S., Gao T.M. Enhanced excitability in the infralimbic cortex produces anxiety-like behaviors. Neuropharmacology 2013, 72C:148-156.
5. Blanchard D.C., Blanchard R.J., Tom P., Rodgers R.J. Diazepam changes risk assessment in an anxiety/defense test battery. Psychopharmacology (Berl) 1990, 101:511-518.
6. Blanchard D.C., Canteras N.S., Markham C.M., Pentkowski N.S., Blanchard R.J. Lesions of structures showing FOS expression to cat presentation: effects on responsivity to a cat, cat odor, and nonpredator threat. Neurosci. Biobehav. Rev. 2005, 29:1243-1253.
7. Blanchard D.C., Blanchard R.J., Griebel G. Defensive responses to predator threat in the rat and mouse. Curr. Protoc. Neurosci. 2005, 1-20. (Chapter 8, Unit 8 19).
8. Campbell B.M., Morrison J.L., Walker E.L., Merchant K.M. Differential regulation of behavioral, genomic, and neuroendocrine responses by CRF infusions in rats. Pharmacol. Biochem. Behav. 2004, 77:447-455.
9. Canteras N.S. The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol. Biochem. Behav. 2002, 71:481-491.
10. Carrasco G.A., Van de Kar L.D. Neuroendocrine pharmacology of stress. Eur. J. Pharmacol. 2003, 463:235-272.
11. Chalmers D.T., Lovenberg T.W., 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. 1995, 15:6340-6350.
12. Ciocchi S., Herry C., Grenier F., Wolff S.B., Letzkus J.J., Vlachos I., Ehrlich I., Sprengel R., Deisseroth K., Stadler M.B., Muller C., Luthi A. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 2010, 468:277-282.
13. Davidson R.J. Darwin and the neural bases of emotion and affective style. Ann. N. Y. Acad. Sci. 2003, 1000:316-336.
14. Deacon R.M., Penny C., Rawlins J.N. Effects of medial prefrontal cortex cytotoxic lesions in mice. Behav. Brain Res 2003, 139:139-155.
15. Dielenberg R.A., Hunt G.E., McGregor I.S. "When a rat smells a cat": the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 2001, 104:1085-1097.
16. Eckart K., Jahn O., Radulovic J., Tezval H., van Werven L., Spiess J. A single amino acid serves as an affinity switch between the receptor and the binding protein of corticotropin-releasing factor: implications for the design of agonists and antagonists. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:11142-11147.
17. Eckart K., Jahn O., Radulovic J., Radulovic M., Blank T., Stiedl O., Brauns O., Tezval H., Zeyda T., Spiess J. Pharmacology and biology of corticotropin-releasing factor (CRF) receptors. Receptors Channels 2002, 8:163-177.
18. Farrokhi C.B., Tovote P., Blanchard R.J., Blanchard D.C., Litvin Y., Spiess J. Cortagine: behavioral and autonomic function of the selective CRF receptor subtype 1 agonist. CNS Drug Rev. 2007, 13:423-443.
19. Franklin K.B., Paxinos G. The Mouse Brain: In Stereotaxic Coordinates 2007, Academic Press, New York. 2nd. ed.
20. Gonzalez L.E., Rujano M., Tucci S., Paredes D., Silva E., Alba G., Hernandez L. Medial prefrontal transection enhances social interaction. I: behavioral studies. Brain Res. 2000, 887:7-15.
21. Hauger R.L., Grigoriadis D.E., Dallman M.F., Plotsky P.M., Vale W.W., Dautzenberg F.M. International Union of Pharmacology. XXXVI. Current status of the nomenclature for receptors for corticotropin-releasing factor and their ligands. Pharmacol. Rev. 2003, 55:21-26.
22. Heinrichs S.C., Joppa M. Dissociation of arousal-like from anxiogenic-like actions of brain corticotropin-releasing factor receptor ligands in rats. Behav. Brain Res. 2001, 122:43-50.
23. Heinrichs S.C., Lapsansky J., Lovenberg T.W., De Souza E.B., Chalmers D.T. Corticotropin-releasing factor CRF1, but not CRF2, receptors mediate anxiogenic-like behavior. Regul. Pept. 1997, 71:15-21.
24. Hillhouse E.W., Grammatopoulos D.K. The molecular mechanisms underlying the regulation of the biological activity of corticotropin-releasing hormone receptors: implications for physiology and pathophysiology. Endocr. Rev. 2006, 27:260-286.
25. Jaferi A., Bhatnagar S. Corticotropin-releasing hormone receptors in the medial prefrontal cortex regulate hypothalamic-pituitary-adrenal activity and anxiety-related behavior regardless of prior stress experience. Brain Res. 2007, 1186:212-223.
26. Jinks A.L., McGregor I.S. Modulation of anxiety-related behaviours following lesions of the prelimbic or infralimbic cortex in the rat. Brain Res. 1997, 772:181-190.
27. Kishimoto T., Radulovic J., Radulovic M., Lin C.R., Schrick C., Hooshmand F., Hermanson O., Rosenfeld M.G., Spiess J. Deletion of crhr2 reveals an anxiolytic role for corticotropin-releasing hormone receptor-2. Nat. Genet. 2000, 24:415-419.
28. Korte S.M., Koolhaas J.M., Wingfield J.C., McEwen B.S. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci. Biobehav. Rev. 2005, 29:3-38.
29. Lacroix L., Broersen L.M., Weiner I., Feldon J. The effects of excitotoxic lesion of the medial prefrontal cortex on latent inhibition, prepulse inhibition, food hoarding, elevated plus maze, active avoidance and locomotor activity in the rat. Neuroscience 1998, 84:431-442.
30. Lacroix L., Spinelli S., Heidbreder C.A., Feldon J. Differential role of the medial and lateral prefrontal cortices in fear and anxiety. Behav. Neurosci. 2000, 114:1119-1130.
31. Li C.I., Maglinao T.L., Takahashi L.K. Medial amygdala modulation of predator odor-induced unconditioned fear in the rat. Behav. Neurosci. 2004, 118:324-332.
32. Liebsch G., Landgraf R., Gerstberger R., Probst J.C., Wotjak C.T., Engelmann M., Holsboer F., 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. 1995, 59:229-239.
33. Likhtik E., Pelletier J.G., Paz R., Pare D. Prefrontal control of the amygdala. J. Neurosci. 2005, 25:7429-7437.
34. Litvin Y., Pentkowski N.S., Blanchard D.C., Blanchard R.J. CRF type 1 receptors in the dorsal periaqueductal gray modulate anxiety-induced defensive behaviors. Horm. Behav. 2007, 52:244-251.
35. Lowry C.A., Moore F.L. Regulation of behavioral responses by corticotropin-releasing factor. Gen. Comp. Endocrinol. 2006, 146:19-27.
36. Martinez R.C., Carvalho-Netto E.F., Amaral V.C., Nunes-de-Souza R.L., Canteras N.S. Investigation of the hypothalamic defensive system in the mouse. Behav. Brain Res. 2008, 192:185-190.
37. Morgane P.J., Galler J.R., Mokler D.J. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog. Neurobiol. 2005, 75:143-160.
38. Moscarello J.M., LeDoux J.E. Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J. Neurosci. 2013, 33:3815-3823.
39. National Research Council Guide for the Care and Use of Laboratory Animals 1996, National Academy Press, Washington, DC.
40. Nemeroff C.B., Widerlov E., Bissette G., Walleus H., Karlsson I., Eklund K., Kilts C.D., Loosen P.T., Vale W. Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science 1984, 226:1342-1344.
41. Ohata H., Shibasaki T. Microinjection of different doses of corticotropin-releasing factor into the medial prefrontal cortex produces effects opposing anxiety-related behavior in rats. J. Nippon Med. Sch. 2011, 78:286-292.
42. Pentkowski N.S., Litvin Y., Blanchard D.C., Vasconcellos A., King L.B., Blanchard R.J. Effects of acidic-astressin and ovine-CRF microinfusions into the ventral hippocampus on defensive behaviors in rats. Horm. Behav. 2009, 56:35-43.
43. Quirk G.J., Beer J.S. Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr. Opin. Neurobiol. 2006, 16:723-727.
44. Radulovic J., Ruhmann A., Liepold T., Spiess J. Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J. Neurosci. 1999, 19:5016-5025.
45. Refojo D., Schweizer M., Kuehne C., Ehrenberg S., Thoeringer C., Vogl A.M., Dedic N., Schumacher M., von Wolff G., Avrabos C., Touma C., Engblom D., Schutz G., Nave K.A., Eder M., Wotjak C.T., Sillaber I., Holsboer F., Wurst W., Deussing J.M. Glutamatergic and dopaminergic neurons mediate anxiogenic and anxiolytic effects of CRHR1. Science 2011, 333:1903-1907.
46. Risbrough V.B., Hauger R.L., Roberts A.L., Vale W.W., Geyer M.A. Corticotropin-releasing factor receptors CRF1 and CRF2 exert both additive and opposing influences on defensive startle behavior. J. Neurosci. 2004, 24:6545-6552.
47. Shah A.A., Treit D. Excitotoxic lesions of the medial prefrontal cortex attenuate fear responses in the elevated-plus maze, social interaction and shock probe burying tests. Brain Res. 2003, 969:183-194.
48. Shah A.A., Treit D. Infusions of midazolam into the medial prefrontal cortex produce anxiolytic effects in the elevated plus-maze and shock-probe burying tests. Brain Res. 2004, 996:31-40.
49. Shah A.A., Sjovold T., Treit D. Inactivation of the medial prefrontal cortex with the GABAA receptor agonist muscimol increases open-arm activity in the elevated plus-maze and attenuates shock-probe burying in rats. Brain Res. 2004, 1028:112-115.
50. Skutella T., Probst J.C., Renner U., Holsboer F., Behl C. Corticotropin-releasing hormone receptor (type I) antisense targeting reduces anxiety. Neuroscience 1998, 85:795-805.
51. 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., Lee K.F. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 1998, 20:1093-1102.
52. Spiess J., Rivier J., Rivier C., Vale W. Primary structure of corticotropin-releasing factor from ovine hypothalamus. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:6517-6521.
53. Sullivan R.M., Gratton A. Behavioral effects of excitotoxic lesions of ventral medial prefrontal cortex in the rat are hemisphere-dependent. Brain Res. 2002, 927:69-79.
54. Sztainberg Y., Kuperman Y., Justice N., Chen A. An anxiolytic role for CRF receptor type 1 in the globus pallidus. J. Neurosci. 2011, 31:17416-17424.
55. Takahashi L.K., Nakashima B.R., Hong H., Watanabe K. The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neurosci. Biobehav. Rev. 2005, 29:1157-1167.
56. Tan H., Zhong P., Yan Z. Corticotropin-releasing factor and acute stress prolongs serotonergic regulation of GABA transmission in prefrontal cortical pyramidal neurons. J. Neurosci. 2004, 24:5000-5008.
57. Tezval H., Jahn O., Todorovic C., Sasse A., Eckart K., Spiess J. Cortagine, a specific agonist of corticotropin-releasing factor receptor subtype 1, is anxiogenic and antidepressive in the mouse model. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9468-9473.
58. Timpl P., Spanagel R., Sillaber I., Kresse A., Reul J.M., Stalla G.K., Blanquet V., Steckler T., Holsboer F., Wurst W. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat. Genet. 1998, 19:162-166.
59. Todorovic C., Jahn O., Tezval H., Hippel C., Spiess J. The role of CRF receptors in anxiety and depression: implications of the novel CRF1 agonist cortagine. Neurosci. Biobehav. Rev. 2005, 29:1323-1333.
60. Tovote P. The Rate Exposure Test: A Semi-Natural Model for Anxiety-like Behavior in the Mouse 2006, Society for Neuroscience, Atlanta, GA.
61. Tovote P., Farrokhi C.B., Gonzales R.M., Schnitzbauer U., Blanchard D.C., Blanchard R.J., Spiess J. Activation of central CRF receptor 1 by cortagine results in enhanced passive coping with a naturalistic threat in mice. Psychoneuroendocrinology 2010, 35:887-895.
62. Vale W., Spiess J., Rivier C., Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213:1394-1397.
63. Van Pett K., Viau V., Bittencourt J.C., Chan R.K., Li H.Y., Arias C., Prins G.S., Perrin M., Vale W., Sawchenko P.E. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 2000, 428:191-212.
64. Vertes R.P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 2004, 51:32-58.
65. Wall P.M., Blanchard R.J., Yang M., Blanchard D.C. Differential effects of infralimbic vs. ventromedial orbital PFC lidocaine infusions in CD-1 mice on defensive responding in the mouse defense test battery and rat exposure test. Brain Res. 2004, 1020:73-85.
66. Yang M., Augustsson H., Markham C.M., Hubbard D.T., Webster D., Wall P.M., Blanchard R.J., Blanchard D.C. The rat exposure test: a model of mouse defensive behaviors. Physiol. Behav. 2004, 81:465-473.
67. Zhou Y., Proudnikov D., Yuferov V., Kreek M.J. Drug-induced and genetic alterations in stress-responsive systems: Implications for specific addictive diseases. Brain Res. 2010, 1314:235-252.
68. Zieba B., Grzegorzewska M., Branski P., Domin H., Wieronska J.M., Hess G., Smialowska M. The behavioural and electrophysiological effects of CRF in rat frontal cortex. Neuropeptides 2008, 42:513-523.