Visualizing corticotropin-releasing hormone receptor type 1 expression and neuronal connectivities in the mouse using a novel multifunctional allele

Journal of Comparative Neurology

Volumn 520, Issue 14, 2012, Pages 3150-3180

  Kühne, Claudia ^a   Puk, Oliver ^b   Graw, Jochen ^b   Hrabě de Angelis, Martin ^b,c   Schütz, Günther ^d   Wurst, Wolfgang ^b,c,e   Deussing, Jan M ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Anxiety; Axonal projection; Conditional mouse model; Corticotropin releasing hormone receptor type 1; Depression; Tau lacZ reporter

Indexed keywords

BETA GALACTOSIDASE; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CRE RECOMBINASE; MESSENGER RNA; TAU PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BETA GALACTOSIDASE GENE; BRAIN STEM; CELL COMPARTMENTALIZATION; CELL LABELING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS STRIATUM; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1 GENE; DENDRITE; DOPAMINERGIC NERVE CELL; EMBRYO; ENZYME ACTIVITY; GABAERGIC TRANSMISSION; GENE CASSETTE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENE LOCUS; GENETIC ANALYSIS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS NUCLEUS; MALE; MICROTUBULE ASSEMBLY; MOUSE; NEOCORTEX; NERVE PROJECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; REPORTER GENE; SENSORY CORTEX; SENSORY NERVE CONDUCTION; TAU GENE; THALAMUS;

ADRENOCORTICOTROPIC HORMONE; ALLELES; ANIMALS; ANTIBODY SPECIFICITY; AXONS; CENTRAL NERVOUS SYSTEM; ELECTRORETINOGRAPHY; EMBRYONIC STEM CELLS; GENE KNOCK-IN TECHNIQUES; LAC OPERON; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, ANIMAL; NEURAL PATHWAYS; PROTEIN KINASE C; RECEPTOR, TRKC; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RNA, MESSENGER; TAU PROTEINS; TYROSINE 3-MONOOXYGENASE; VISCERA;

EID: 84865089294     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23082     Document Type: Article

References (85)

1. Adams N, Gale N. 2006. High resolution gene expression analysis in mice using genetically inserted reporter genes. In: Pease S, Lois C, editors. Mammalian and avian transgenesis - new approaches. Berlin, Heidelberg: Springer. p 131-172.
2. Alon T, Zhou L, Perez CA, Garfield AS, Friedman JM, Heisler LK. 2009. Transgenic mice expressing green fluorescent protein under the control of the corticotropin-releasing hormone promoter. Endocrinology 150: 5626-5632.
3. Ambroggi F, Turiault M, Milet A, Roche-Gamonet V, Parnaudeau S, Balado E, Barik J, van der Veen R, Maroteaux G, Lemberger T, Schutz G, Lazar M, Marinelli M, Piazza PV, Tronche F. 2009. Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nat Neurosci 12: 247-249.
4. Arborelius L, Owens MJ, Plotsky PM, Nemeroff CB. 1999. The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol 160: 1-12.
5. Awatramani R, Soriano P, Rodriguez C, Mai JJ, Dymecki SM. 2003. Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat Genet 35: 70-75.
6. Barrow JR, Capecchi MR. 1996. Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122: 3817-3828.
7. Belteki G, Gertsenstein M, Ow DW, Nagy A. 2003. Site-specific cassette exchange and germline transmission with mouse ES cells expressing phiC31 integrase. Nat Biotechnol 21: 321-324.
8. Bolam JP, Hanley JJ, Booth PA, Bevan MD. 2000. Synaptic organisation of the basal ganglia. J Anat 196( Pt 4): 527-542.
9. Branda CS, Dymecki SM. 2004. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev Cell 6: 7-28.
10. Callahan CA, Yoshikawa S, Thomas JB. 1998. Tracing axons. Curr Opin Neurobiol 8: 582-586.
11. Cardell M, Landsend AS, Eidet J, Wieloch T, Blackstad TW, Ottersen OP. 1998. High resolution immunogold analysis reveals distinct subcellular compartmentation of protein kinase C gamma and delta in rat Purkinje cells. Neuroscience 82: 709-725.
12. Chen Y, Brunson KL, Muller MB, Cariaga W, Baram TZ. 2000. Immunocytochemical distribution of corticotropin-releasing hormone receptor type-1 (CRF(1))-like immunoreactivity in the mouse brain: light microscopy analysis using an antibody directed against the C-terminus. J Comp Neurol 420: 305-323.
13. Dalke C, Loster J, Fuchs H, Gailus-Durner V, Soewarto D, Favor J, Neuhauser-Klaus A, Pretsch W, Gekeler F, Shinoda K, Zrenner E, Meitinger T, Hrabe de AM, Graw J. 2004. Electroretinography as a screening method for mutations causing retinal dysfunction in mice. Invest Ophthalmol Vis Sci 45: 601-609.
14. de Felipe P. 2004. Skipping the co-expression problem: the new 2A "CHYSEL" technology. Genet Vaccines Ther 2: 13.
15. de Felipe P, Ryan MD. 2004. Targeting of proteins derived from self-processing polyproteins containing multiple signal sequences. Traffic 5: 616-626.
16. de Felipe P, Hughes LE, Ryan MD, Brown JD. 2003. Co-translational, intraribosomal cleavage of polypeptides by the foot-and-mouth disease virus 2A peptide. J Biol Chem 278: 11441-11448.
17. de Felipe P, Luke GA, Hughes LE, Gani D, Halpin C, Ryan MD. 2006. E unum pluribus: multiple proteins from a self-processing polyprotein. Trends Biotechnol 24: 68-75.
18. de Kloet ER, Joels M, Holsboer F. 2005. Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6: 463-475.
19. Deussing JM, Kuhne C, Putz B, Panhuysen M, Breu J, Stenzel-Poore MP, Holsboer F, Wurst W. 2007. Expression profiling identifies the CRH/CRH-R1 system as a modulator of neurovascular gene activity. J Cereb Blood Flow Metab 27: 1476-1495.
20. Deussing JM, Breu J, Kuhne C, Kallnik M, Bunck M, Glasl L, Yen YC, Schmidt MV, Zurmuhlen R, Vogl AM, Gailus-Durner V, Fuchs H, Holter SM, Wotjak CT, Landgraf R, de Angelis MH, Holsboer F, Wurst W. 2010. Urocortin 3 modulates social discrimination abilities via corticotropin-releasing hormone receptor type 2. J Neurosci 30: 9103-9116.
21. Donelan J, Marchand JE, Kempuraj D, Papadopoulou N, Papaliodis D, Theoharides TC. 2006. Perifollicular and perivascular mouse skin mast cells express corticotropin-releasing hormone receptor. J Invest Dermatol 126: 929-932.
22. Dunn AJ, Berridge CW. 1990. Physiological and behavioral responses to corticotropin-releasing factor administration: is CRF a mediator of anxiety or stress responses? Brain Res Brain Res Rev 15: 71-100.
23. Dymecki SM, Kim JC. 2007. Molecular neuroanatomy's "Three Gs": a primer. Neuron 54: 17-34.
24. Engblom D, Bilbao A, Sanchis-Segura C, Dahan L, Perreau-Lenz S, Balland B, Parkitna JR, Lujan R, Halbout B, Mameli M, Parlato R, Sprengel R, Luscher C, Schutz G, Spanagel R. 2008. Glutamate receptors on dopamine neurons control the persistence of cocaine seeking. Neuron 59: 497-508.
25. Enjin A, Rabe N, Nakanishi ST, Vallstedt A, Gezelius H, Memic F, Lind M, Hjalt T, Tourtellotte WG, Bruder C, Eichele G, Whelan PJ, Kullander K. 2010. Identification of novel spinal cholinergic genetic subtypes disclose Chodl and Pitx2 as markers for fast motor neurons and partition cells. J Comp Neurol 518: 2284-2304.
26. Gailus-Durner V, Fuchs H, Becker L, Bolle I, Brielmeier M, Calzada-Wack J, Elvert R, Ehrhardt N, Dalke C, Franz TJ, Grundner-Culemann E, Hammelbacher S, Holter SM, Holzlwimmer G, Horsch M, Javaheri A, Kalaydjiev SV, Klempt M, Kling E, Kunder S, Lengger C, Lisse T, Mijalski T, Naton B, Pedersen V, Prehn C, Przemeck G, Racz I, Reinhard C, Reitmeir P, Schneider I, Schrewe A, Steinkamp R, Zybill C, Adamski J, Beckers J, Behrendt H, Favor J, Graw J, Heldmaier G, Hofler H, Ivandic B, Katus H, Kirchhof P, Klingenspor M, Klopstock T, Lengeling A, Muller W, Ohl F, Ollert M, Quintanilla-Martinez L, Schmidt J, Schulz H, Wolf E, Wurst W, Zimmer A, Busch DH, de Angelis MH. 2005. Introducing the German Mouse Clinic: open access platform for standardized phenotyping. Nat Methods 2: 403-404.
27. Gallagher JP, Orozco-Cabal LF, Liu J, Shinnick-Gallagher P. 2008. Synaptic physiology of central CRH system. Eur J Pharmacol 583: 215-225.
28. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15: 133-139.
29. Gerfen CR, Surmeier DJ. 2011. Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34: 441-466.
30. Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA. 2006. Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44: 611-621.
31. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925.
32. Harrison SJ, Parrish M, Monaghan AP. 2008. Sall3 is required for the terminal maturation of olfactory glomerular interneurons. J Comp Neurol 507: 1780-1794.
33. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM. 2006. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497: 326-349.
34. Hillhouse EW, Grammatopoulos DK. 2006. The molecular mechanisms underlying the regulation of the biological activity of corticotropin-releasing hormone receptors: implications for physiology and pathophysiology. Endocr Rev 27: 260-286.
35. Holsboer F. 1999. The rationale for corticotropin-releasing hormone receptor (CRH-R) antagonists to treat depression and anxiety. J Psychiatr Res 33: 181-214.
36. Holsboer F, Ising M. 2008. Central CRH system in depression and anxiety-evidence from clinical studies with CRH1 receptor antagonists. Eur J Pharmacol 583: 350-357.
37. Huising MO, van der MT, Vaughan JM, Matsumoto M, Donaldson CJ, Park H, Billestrup N, Vale WW. 2010. CRFR1 is expressed on pancreatic beta cells, promotes beta cell proliferation, and potentiates insulin secretion in a glucose-dependent manner. Proc Natl Acad Sci U S A 107: 912-917.
38. Hunter NL, Awatramani RB, Farley FW, Dymecki SM. 2005. Ligand-activated Flpe for temporally regulated gene modifications. Genesis 41: 99-109.
39. Inada A, Nienaber C, Bonner-Weir S. 2006. Endogenous beta-galactosidase expression in murine pancreatic islets. Diabetologia 49: 1120-1122.
40. Ito N, Ito T, Kromminga A, Bettermann A, Takigawa M, Kees F, Straub RH, Paus R. 2005. Human hair follicles display a functional equivalent of the hypothalamic-pituitary-adrenal axis and synthesize cortisol. FASEB J 19: 1332-1334.
41. Justice NJ, Yuan ZF, Sawchenko PE, Vale W. 2008. Type 1 corticotropin-releasing factor receptor expression reported in BAC transgenic mice: implications for reconciling ligand-receptor mismatch in the central corticotropin-releasing factor system. J Comp Neurol 511: 479-496.
42. Klein R, Silos-Santiago I, Smeyne RJ, Lira SA, Brambilla R, Bryant S, Zhang L, Snider WD, Barbacid M. 1994. Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature 368: 249-251.
43. Komori T, Gyobu H, Ueno H, Kitamura T, Senba E, Morikawa Y. 2008. Expression of kin of irregular chiasm-like 3/mKirre in proprioceptive neurons of the dorsal root ganglia and its interaction with nephrin in muscle spindles. J Comp Neurol 511: 92-108.
44. Korosi A, Kozicz T, Richter J, Veening JG, Olivier B, Roubos EW. 2007. Corticotropin-releasing factor, urocortin 1, and their receptors in the mouse spinal cord. J Comp Neurol 502: 973-989.
45. Lariviere WR, Melzack R. 2000. The role of corticotropin-releasing factor in pain and analgesia. Pain 84: 1-12.
46. Lemberger T, Parlato R, Dassesse D, Westphal M, Casanova E, Turiault M, Tronche F, Schiffmann SN, Schutz G. 2007. Expression of Cre recombinase in dopaminoceptive neurons. BMC Neurosci 8: 4.
47. Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R, Bernstein Y, Goldenberg D, Xiao C, Fliegauf M, Kremer E, Otto F, Brenner O, Lev-Tov A, Groner Y. 2002. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 21: 3454-3463.
48. Luo L, Callaway EM, Svoboda K. 2008. Genetic dissection of neural circuits. Neuron 57: 634-660.
49. Luo X, Kiss A, Makara G, Lolait SJ, Aguilera G. 1994. Stress-specific regulation of corticotropin releasing hormone receptor expression in the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Neuroendocrinol 6: 689-696.
50. Mannen H, Sugiura Y. 1976. Reconstruction of neurons of dorsal horn proper using Golgi-stained serial sections. J Comp Neurol 168: 303-312.
51. Marmigere F, Ernfors P. 2007. Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 8: 114-127.
52. Maxwell DJ, Belle MD, Cheunsuang O, Stewart A, Morris R. 2007. Morphology of inhibitory and excitatory interneurons in superficial laminae of the rat dorsal horn. J Physiol 584: 521-533.
53. McMahon SB, Armanini MP, Ling LH, Phillips HS. 1994. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12: 1161-1171.
54. Merchenthaler I, Hynes MA, Vigh S, Shally AV, Petrusz P. 1983. Immunocytochemical localization of corticotropin releasing factor (CRF) in the rat spinal cord. Brain Res 275: 373-377.
55. Millan MJ. 2002. Descending control of pain. Prog Neurobiol 66: 355-474.
56. Minichiello L, Korte M, Wolfer D, Kuhn R, Unsicker K, Cestari V, Rossi-Arnaud C, Lipp HP, Bonhoeffer T, Klein R. 1999. Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24: 401-414.
57. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G. 2010. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30: 1582-1594.
58. Mombaerts P. 2006. Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22: 713-737.
59. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87: 675-686.
60. Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wolfel B, Dodt HU, Zieglgansberger W, Wotjak CT, Mackie K, Elphick MR, Marsicano G, Lutz B. 2006. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51: 455-466.
61. Moqrich A, Earley TJ, Watson J, Andahazy M, Backus C, Martin-Zanca D, Wright DE, Reichardt LF, Patapoutian A. 2004. Expressing TrkC from the TrkA locus causes a subset of dorsal root ganglia neurons to switch fate. Nat Neurosci 7: 812-818.
62. Mori M, Kose A, Tsujino T, Tanaka C. 1990. Immunocytochemical localization of protein kinase C subspecies in the rat spinal cord: light and electron microscopic study. J Comp Neurol 299: 167-177.
63. Muller MB, Preil J, Renner U, Zimmermann S, Kresse AE, Stalla GK, Keck ME, Holsboer F, Wurst W. 2001. Expression of CRHR1 and CRHR2 in mouse pituitary and adrenal gland: implications for HPA system regulation. Endocrinology 142: 4150-4153.
64. Muller MB, Zimmermann S, Sillaber I, Hagemeyer TP, Deussing JM, Timpl P, Kormann MS, Droste SK, Kuhn R, Reul JM, Holsboer F, Wurst W. 2003. Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nat Neurosci 6: 1100-1107.
65. Prusky GT, Alam NM, Beekman S, Douglas RM. 2004. Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45: 4611-4616.
66. Refojo D, Schweizer M, Kuehne C, Ehrenberg S, Thoeringer C, Vogl AM, Dedic N, Schumacher M, von WG, Avrabos C, Touma C, Engblom D, Schutz G, Nave KA, Eder M, Wotjak CT, Sillaber I, Holsboer F, Wurst W, Deussing JM. 2011. Glutamatergic and dopaminergic neurons mediate anxiogenic and anxiolytic effects of CRHR1. Science 333: 1903-1907.
67. Ren K, Ruda MA. 1994. A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord. Brain Res Brain Res Rev 19: 163-179.
68. Rivest S, Laflamme N, Nappi RE. 1995. Immune challenge and immobilization stress induce transcription of the gene encoding the CRF receptor in selective nuclei of the rat hypothalamus. J Neurosci 15: 2680-2695.
69. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM. 2000. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 25: 139-140.
70. Roloff B, Fechner K, Slominski A, Furkert J, Botchkarev VA, Bulfone-Paus S, Zipper J, Krause E, Paus R. 1998. Hair cycle-dependent expression of corticotropin-releasing factor (CRF) and CRF receptors in murine skin. FASEB J 12: 287-297.
71. Schwartz CM, Cheng A, Mughal MR, Mattson MP, Yao PJ. 2010. Clathrin assembly proteins AP180 and CALM in the embryonic rat brain. J Comp Neurol 518: 3803-3818.
72. Slominski A, Pisarchik A, Tobin DJ, Mazurkiewicz JE, Wortsman J. 2004. Differential expression of a cutaneous corticotropin-releasing hormone system. Endocrinology 145: 941-950.
73. Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian LM, Gold LH, Chen R, Marchuk Y, Hauser C, Bentley CA, Sawchenko PE, Koob GF, Vale W, Lee KF. 1998. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20: 1093-1102.
74. Song ZH, Takemori AE. 1991. Antagonism of morphine antinociception by intrathecally administered corticotropin-releasing factor in mice. J Pharmacol Exp Ther 256: 909-912.
75. Steckler T, Holsboer F. 1999. Corticotropin-releasing hormone receptor subtypes and emotion. Biol Psychiatry 46: 1480-1508.
76. Sun W, Li N, He S. 2002. Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol 451: 115-126.
77. Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JM, Stalla GK, Blanquet V, Steckler T, Holsboer F, Wurst W. 1998. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat Genet 19: 162-166.
78. Vale W, Spiess J, Rivier C, Rivier J. 1981. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 213: 1394-1397.
79. Valentino RJ, Van Bockstaele E. 2008. Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583: 194-203.
80. Valjent E, Bertran-Gonzalez J, Herve D, Fisone G, Girault JA. 2009. Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice. Trends Neurosci 32: 538-547.
81. Van den Heuvel DM, Pasterkamp RJ. 2008. Getting connected in the dopamine system. Prog Neurobiol 85: 75-93.
82. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE. 2000. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428: 191-212.
83. Xu Q, Tam M, Anderson SA. 2008. Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J Comp Neurol 506: 16-29.
84. Yeh HH, Olschowka JA. 1989. A system of corticotropin releasing factor-containing amacrine cells in the rat retina. Neuroscience 33: 229-240.
85. Zmijewski MA, Sharma RK, Slominski AT. 2007. Expression of molecular equivalent of hypothalamic-pituitary-adrenal axis in adult retinal pigment epithelium. J Endocrinol 193: 157-169.