Somatostatin signaling in neuronal cilia is critical for object recognition memory

Journal of Neuroscience

Volumn 30, Issue 12, 2010, Pages 4306-4314

  Einstein, Emily B ^a   Patterson, Carlyn A ^a   Hon, Beverly J ^a   Regan, Kathleen A ^a   Reddi, Jyoti ^a   Melnikoff, David E ^a   Mateer, Marcus J ^a   Schulz, Stefan ^b   Johnson, Brian N ^a   Tallent, Melanie K ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; FORSKOLIN; SOMATOSTATIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; FEMALE; HIPPOCAMPUS; KNOCKOUT MOUSE; MEMORY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; RECOGNITION; WILD TYPE;

1-METHYL-3-ISOBUTYLXANTHINE; ACTION POTENTIALS; ADENYLATE CYCLASE; AMIDES; ANIMALS; BEHAVIOR, ANIMAL; BICUCULLINE; BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; CILIA; CYCLIC AMP; DISCRIMINATION (PSYCHOLOGY); ELECTRIC STIMULATION; FEMALE; FORSKOLIN; GABA ANTAGONISTS; ISOQUINOLINES; LOCOMOTION; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; NEUROPSYCHOLOGICAL TESTS; NITROBENZENES; PHOSPHODIESTERASE INHIBITORS; RECEPTORS, SOMATOSTATIN; RECOGNITION (PSYCHOLOGY); SIGNAL TRANSDUCTION; SOMATOSTATIN;

EID: 77949816722     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5295-09.2010     Document Type: Article

References (48)

1. Adams NA, Awadein A, Toma HS (2007) The retinal ciliopathies. Ophthalmic Genet 28:113-125.
2. Banizs B, Pike MM, Millican CL, Ferguson WB, Komlosi P, Sheetz J, Bell PD, Schwiebert EM, Yoder BK (2005) Dysfunctional cilia lead to altered ependyma and choroid plexus function, and result in the formation of hydrocephalus. Development 132:5329-5339.
3. Bänziger M, Cercus J, Hirt H, Laumen K, Malan C, Spindler F, Struber F, Troxler T (2003) The development of a practical synthesis of the potent and selective somatostatin sst3 receptor antagonist [4-(3,4-difluorophenyl)- piperazine-1-yl]-{(4S,4aS,8aR)-2[(S)-3-(6-methoxy-pyridin-3-yl)-2-methyl-propyl] -decahydroisoquinoline-4-yl}-methanone (NVP-ACQ090). Tetrahedron Asymmetry 14:3469-3477.
4. Baraban SC, Tallent MK (2004) Interneuron diversity series: interneuronal neuropeptides - endogenous regulators of neuronal excitability. Trends Neurosci 27:135-142.
5. Baratta MV, Lamp T, Tallent MK (2002) Somatostatin depresses long-term potentiation and Ca2+ signaling in mouse dentate gyrus. J Neurophysiol 88:3078-3086.
6. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K (2008a) Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc Natl Acad SciU S A 105:4242-4246.
7. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K (2008b) Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Mol Biol Cell 19:1540-1547.
8. Bishop GA, Berbari NF, Lewis J, Mykytyn K (2007) Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J Comp Neurol 505:562-571.
9. Breunig JJ, Sarkisian MR, Arellano JI, Morozov YM, Ayoub AE, Sojitra S, Wang B, Flavell RA, Rakic P, Town T (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci U S A 105:13127-13132.
10. Burgos-Ramos E, Hervás-Aguilar A, Aguado-Llera D, Puebla-Jiménez L, Hernández-Pinto AM, Barrios V, Arilla-Ferreiro E (2008) Somatostatin and Alzheimer's disease. Mol Cell Endocrinol 286:104-111.
11. Davenport JR, Watts AJ, Roper VC, Croyle MJ, van Groen T, Wyss JM, Nagy TR, Kesterson RA, Yoder BK (2007) Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr Biol 17:1586-1594.
12. Dere E, Huston JP, De Souza Silva MA (2007) The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 31:673-704.
13. Eley L, Yates LM, Goodship JA (2005) Cilia and disease. Curr Opin Genet Dev 15:308-314.
14. Fanselow EE, Richardson KA, Connors BW (2008) Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100:2640-2652.
15. Fuchs JL, Schwark HD (2004) Neuronal primary cilia: a review. Cell Biol Int 28:111-118.
16. Garelick MG, Chan GC, DiRocco DP, Storm DR (2009) Overexpression of type I adenylyl cyclase in the forebrain impairs spatial memory in aged but not young mice. J Neurosci 29:10835-10842.
17. Gelinas JN, Nguyen PV (2005) Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J Neurosci 25:3294-3303.
18. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11:277-284.
19. Händel M, Schulz S, Stanarius A, Schreff M, Erdtmann-Vourliotis M, Schmidt H, Wolf G, Höllt V (1999) Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89:909-926.
20. Hervieu G, Emson PC (1998) Visualisation of non-glycosylated somatostatin receptor two (ngsst2) immunoreactivity in the rat central nervous system. Brain Res Mol Brain Res 58:138-155.
21. Ibañez-Tallon I, Pagenstecher A, Fliegauf M, Olbrich H, Kispert A, Ketelsen UP, North A, Heintz N, Omran H (2004) Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation. Hum Mol Genet 13:2133-2141.
22. Lalonde R, Qian S (2007) Exploratory activity, motor coordination, and spatial learning in Mchr1 knockout mice. Behav Brain Res 178:293-304.
23. Masyuk AI, Masyuk TV, Splinter PL, Huang BQ, Stroope AJ, LaRusso NF (2006) Cholangiocyte cilia detect changes in luminal fluid flow and transmit them into intracellular Ca2+ and cAMP signaling. Gastroenterology 131:911-920.
24. Monzon ME, de Souza MM, Izquierdo LA, Izquierdo I, Barros DM, de Barioglio SR (1999) Melanin-concentrating hormone (MCH) modifies memory retention in rats. Peptides 20:1517-1519.
25. Nguyen PV, Woo NH (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71:401-437.
26. Nitz D, McNaughton B (2004) Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J Neurophysiol 91:863-872.
27. Pan J, Wang Q, Snell WJ (2005) Cilium-generated signaling and cilia-related disorders. Lab Invest 85:452-463.
28. Pazour GJ, Witman GB (2003) The vertebrate primary cilium is a sensory organelle. Curr Opin Cell Biol 15:105-110.
29. Pineda VV, Athos JI, Wang H, Celver J, Ippolito D, Boulay G, Birnbaumer L, Storm DR (2004) Removal of G(ialpha1) constraints on adenylyl cyclase in the hippocampus enhances LTP and impairs memory formation. Neuron 41:153-163.
30. Pissios P, Trombly DJ, Tzameli I, Maratos-Flier E (2003) Melanin-concentrating hormone receptor 1 activates extracellular signal-regulated kinase and synergizes with G(s)-coupled pathways. Endocrinology 144:3514-3523.
31. Qiu C, Zeyda T, Johnson B, Hochgeschwender U, de Lecea L, Tallent MK (2008) Somatostatin receptor subtype 4 couples to the M-current to regulate seizures. J Neurosci 28:3567-3576.
32. Ramírez JL, Mouchantaf R, Kumar U, Otero Corchon V, Rubinstein M, Low MJ, Patel YC (2002) Brain somatostatin receptors are up-regulated in somatostatin-deficient mice. Mol Endocrinol 16:1951-1963.
33. Restrepo D, Teeter JH, Schild D (1996) Second messenger signaling in olfactory transduction. J Neurobiol 30:37-48.
34. Saito Y, Cheng M, Leslie FM, Civelli O (2001) Expression of the melanin-concentrating hormone (MCH) receptor mRNA in the rat brain. J Comp Neurol 435:26-40.
35. Schmid A, Sutto Z, Nlend MC, Horvath G, Schmid N, Buck J, Levin LR, Conner GE, Fregien N, Salathe M (2007) Soluble adenylyl cyclase is localized to cilia and contributes to ciliary beat frequency regulation via production of cAMP. J Gen Physiol 130:99-109.
36. Smith LA, Bukanov NO, Husson H, Russo RJ, Barry TC, Taylor AL, Beier DR, Ibraghimov-Beskrovnaya O (2006) Development of polycystic kidney disease in juvenile cystic kidney mice: insights into pathogenesis, ciliary abnormalities, and common features with human disease. J Am Soc Nephrol 17:2821-2831.
37. Spassky N, Han YG, Aguilar A, Strehl L, Besse L, Laclef C, Ros MR, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev Biol 317:246-259.
38. Stanić D, Malmgren H, He H, Scott L, Aperia A, Hökfelt T (2009) Developmental changes in frequency of the ciliary somatostatin receptor 3 protein. Brain Res 1249:101-112.
39. Takeuchi H, Kurahashi T (2008) Distribution, amplification, and summation of cyclic nucleotide sensitivities within single olfactory sensory cilia. J Neurosci 28:766-775.
40. Town T, Breunig JJ, Sarkisian MR, Spilianakis C, Ayoub AE, Liu X, Ferrandino AF, Gallagher AR, Li MO, Rakic P, Flavell RA (2008) The stumpy gene is required for mammalian ciliogenesis. Proc Natl Acad Sci U S A 105:2853-2858.
41. Verlaet M, Adamantidis A, Coumans B, Chanas G, Zorzi W, Heinen E, Grisar T, Lakaye B (2002) Human immune cells express ppMCH mRNA and functional MCHR1 receptor. FEBS Lett 527:205-210.
42. Wang H, Storm DR (2003) Calmodulin-regulated adenylyl cyclases: crosstalk and plasticity in the central nervous system. Mol Pharmacol 63:463-468.
43. Wang Z, Li V, Chan GC, Phan T, Nudelman AS, Xia Z, Storm DR (2009) Adult type 3 adenylyl cyclase-deficient mice are obese. PLoS One 4:e6979.
44. Wei J, Wayman G, StormDR (1996) Phosphorylation and inhibition of type III adenylyl cyclase by calmodulin-dependent protein kinase II in vivo. J Biol Chem 271:24231-24235.
45. Yasuda K, Rens-Domiano S, Breder CD, Law SF, Saper CB, Reisine T, Bell GI (1992) Cloning of a novel somatostatin receptor, SSTR3, coupled to adenylycyclase. J Biol Chem 267:20422-20428.
46. Zhang M, Moon C, Chan GC, Yang L, Zheng F, Conti AC, Muglia L, Muglia LJ, Storm DR, Wang H (2008) Ca-stimulated type 8 adenylyl cyclase is required for rapid acquisition of novel spatial information and for working/episodic-like memory. J Neurosci 28:4736-4744.
47. Zheng H, Bailey A, Jiang MH, Honda K, Chen HY, Trumbauer ME, Van der Ploeg LH, Schaeffer JM, Leng G, Smith RG (1997) Somatostatin receptor subtype 2 knockout mice are refractory to growth hormone-negative feedback on arcuate neurons x. Mol Endocrinol 11:1709-1717.
48. Zufall F, Leinders-Zufall T, Greer CA (2000) Amplification of odor-induced Ca(2+) transients by store-operated Ca(2+) release and its role in olfactory signal transduction. J Neurophysiol 83:501-512.