Arborization of dendrites by developing neocortical neurons is dependent on primary cilia and type 3 adenylyl cyclase

Journal of Neuroscience

Volumn 33, Issue 6, 2013, Pages 2626-2638

  Guadiana, Sarah M ^a   Semple Rowland, Susan ^a   Daroszewski, Daniel ^a   Madorsky, Irina ^a   Breunig, Joshua J ^b   Mykytyn, Kirk ^c   Sarkisian, Matthew R ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENYLATE CYCLASE; ADENYLATE CYCLASE 3; G PROTEIN COUPLED RECEPTOR; PERICENTRIN; PROTEIN KIF3A; SEROTONIN 6 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL STRUCTURE; CILIARY NERVE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC ARBORIZATION; ELECTROPORATION; EMBRYO; FEMALE; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING;

ADENYLATE CYCLASE; ANIMALS; CELLS, CULTURED; CILIA; DENDRITES; FEMALE; KINESIN; MALE; MICE; NEOCORTEX; NEUROGENESIS; NEURONS; NIH 3T3 CELLS; PREGNANCY; RECEPTORS, SEROTONIN;

EID: 84873309650     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2906-12.2013     Document Type: Article

References (60)

1. Anastas SB, Mueller D, Semple-Rowland SL, Breunig JJ, Sarkisian MR (2011) Failed cytokinesis of neural progenitors in citron kinase-deficient rats leads to multiciliated neurons. Cereb Cortex 21:338-344. CrossRef Medline
2. Arellano JI, Guadiana SM, Breunig JJ, Rakic P, Sarkisian MR (2012) Development and distribution of neuronal cilia in mouse neocortex. J Comp Neurol 520:848-873. CrossRef Medline
3. Avasthi P, Marshall WF (2012) Stages of ciliogenesis and regulation of ciliary length. Differentiation 83 [Suppl]:S30-S42.
4. Avasthi P, Marley A, Lin H, Gregori-Puigjane E, Shoichet BK, von Zastrow M, Marshall WF (2012) A chemical screen identifies class a G-protein coupled receptors as regulators of cilia. ACS Chem Biol 7:911-919. CrossRef Medline
5. Bennouna-Greene V, Kremer S, Stoetzel C, Christmann D, Schuster C, Durand M, Verloes A, Sigaudy S, Holder-Espinasse M, Godet J, Brandt C, Marion V, Danion A, Dietemann JL, Dollfus H (2011) Hippocampal dysgenesis and variable neuropsychiatric phenotypes in patients with Bardet-Biedl syndrome underline complex CNS impact of primary cilia. Clin Genet 80:523-531. CrossRef Medline
6. Berbari NF, Bishop GA, Askwith CC, Lewis JS, Mykytyn K (2007) Hippocampal neurons possess primary cilia in culture. J Neurosci Res 85: 1095-1100. CrossRef Medline
7. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K (2008a) Identification of ciliary localization sequences within the third intracellular 0loop of G protein-coupled receptors. Mol Biol Cell 19:1540-1547. CrossRef Medline
8. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K (2008b) Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc Natl Acad Sci U S A 105:4242-4246. CrossRef Medline
9. 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. CrossRef Medline
10. Brailov I, Bancila M, Brisorgueil MJ, Miquel MC, Hamon M, Vergé D (2000) Localization of 5-HT(6) receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res 872:271-275. CrossRef Medline
11. 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. CrossRef Medline
12. Chakravarthy B, Gaudet C, Ménard M, Atkinson T, Chiarini A, Dal Pra I, Whitfield J (2010) The p75 neurotrophin receptor is localized to primary cilia in adult murine hippocampal dentate gyrus granule cells. Biochem Biophys Res Commun 401:458-462. CrossRef Medline
13. Chizhikov VV, Davenport J, Zhang Q, Shih EK, Cabello OA, Fuchs JL, Yoder BK, Millen KJ (2007) Cilia proteins control cerebellar morphogenesis by promoting expansion of the granule progenitor pool. J Neurosci 27: 9780-9789. CrossRef Medline
14. Dave RH, Saengsawang W, Yu JZ, Donati R, Rasenick MM (2009) Heterotrimeric G-proteins interact directly with cytoskeletal components to modify mi Crotubule-dependent cellular processes. Neurosignals 17:100-108. CrossRef Medline
15. Davé RH, Saengsawang W, Lopus M, Davé S, Wilson L, Rasenick MM (2011) A molecular and structural mechanism for G protein-mediated mi Crotubule destabilization. J Biol Chem 286:4319-4328. CrossRef Medline
16. 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. CrossRef Medline
17. Domire JS, Green JA, Lee KG, Johnson AD, Askwith CC, Mykytyn K (2011) Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Cell Mol Life Sci. 68:2951-2960. CrossRef Medline
18. Einstein EB, Patterson CA, Hon BJ, Regan KA, Reddi J, Melnikoff DE, Mateer MJ, Schulz S, Johnson BN, Tallent MK (2010) Somatostatin signaling in neuronal cilia is critical for object recognition memory. J Neurosci 30: 4306-4314. CrossRef Medline
19. Follit JA, Li L, Vucica Y, Pazour GJ (2010) The cytoplasmic tail of fibrocystin contains a ciliary targeting sequence. J Cell Biol 188:21-28. CrossRef Medline
20. Garcia-Gonzalo FR, Reiter JF (2012) Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. J Cell Biol 197:697-709. CrossRef Medline
21. Geng L, Okuhara D, Yu Z, Tian X, Cai Y, Shibazaki S, Somlo S (2006) Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J Cell Sci 119:1383-1395. CrossRef Medline
22. Goetz SC, Anderson KV (2010) The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11:331-344. CrossRef Medline
23. Green JA, Mykytyn K (2010) Neuronal ciliary signaling in homeostasis and disease. Cell Mol Life Sci 67:3287-3297. CrossRef Medline
24. Green JA, Gu C, Mykytyn K (2012) Heteromerization of ciliary G proteincoupled receptors in the mouse brain. PLoS ONE 7:e46304. CrossRef Medline
25. Grissom PM, Vaisberg EA, McIntosh JR (2002) Identification of a novel light intermediate chain (D2LIC) for mammalian cytoplasmic dynein 2. Mol Biol Cell 11:817-829. CrossRef Medline
26. Hamon M, Doucet E, Lefevre K, Miquel MC, Lanfumey L, Insausti R, Frechilla D, Del Rio J, Verge D (1999) Antibodies and antisense oligonucleotide for probing the distribution and putative functions of central 5-HT6 receptors. Neuropsychopharmacology 21 [Suppl]:68S-76S.
27. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A (2008) Hedgehog signalingand primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11:277-284. CrossRef Medline
28. 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. CrossRef Medline
29. Higginbotham H, Eom TY, Mariani LE, Bachleda A, Hirt J, Gukassyan V, Cusack CL, Lai C, Caspary T, Anton ES (2012) Arl13b in primary cilia regulates the migration and placement of interneurons in the developing cerebral cortex. Dev Cell 23:925-938.
30. Kang H, Lee WK, Choi YH, Vukoti KM, Bang WG, Yu YG (2005) Molecular analysis of the interaction between the intracellular loops of the human serotonin receptor type 6 (5-HT6) and the alpha subunit of GS protein. Biochem Biophys Res Commun 329:684-692. CrossRef Medline
31. Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL (1993) A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci U S A 90:5519-5523. CrossRef Medline
32. Kumamoto N, Gu Y, Wang J, Janoschka S, Takemaru K, Levine J, Ge S (2012) A role for primary cilia in glutamatergic synaptic integration of adultborn neurons. Nat Neurosci 15:399-405. CrossRef Medline
33. Law SF, Zaina S, Sweet R, Yasuda K, Bell GI, Stadel J, Reisine T (1994) Gi 1 selectively couples somatostatin receptor subtype 3 to adenylyl cyclase: identification of the functional domains of this _ subunit necessary for mediating the inhibition by somatostatin of cAMP formation. Mol Pharmacol 45:587-590. Medline
34. Lee JE, Gleeson JG (2011) Cilia in the nervous system: linking cilia function and neurodevelopmental disorders. Curr Opin Neurol 24:98-105.CrossRef Medline
35. Louvi A, Grove EA (2011) Cilia in the CNS: the quiet organelle claims center stage. Neuron 69:1046-1060. CrossRef Medline
36. Makokha M, Hare M, Li M, Hays T, Barbar E (2002) Interactions of cytoplasmic dynein light chains Tctex-1 and LC8 with the intermediate chain IC74. Biochemistry 41:4302-4311. CrossRef Medline
37. Marley A, von Zastrow M (2010) DISC1 regulates primary cilia that display specific dopamine receptors. PLoS ONE 5:e10902. CrossRef Medline
38. Massinen S, Hokkanen ME, Matsson H, Tammimies K, Tapia-Páez I, Dahlström-Heuser V, Kuja-Panula J, Burghoorn J, Jeppsson KE, Swoboda P, Peyrard-Janvid M, Toftgård R, Castrén E, Kere J (2011) Increased expression of the dyslexia candidate gene DCDC2 affects length and signaling of primary cilia in neurons. PLoS ONE 6:e20580. CrossRef Medline
39. Miyoshi K, Onishi K, Asanuma M, Miyazaki I, Diaz-Corrales FJ, Ogawa N (2006) Embryonic expression of pericentrin suggests universal roles in ciliogenesis. Dev Genes Evol 216:537-542. CrossRef Medline
40. Miyoshi K, Kasahara K, Miyazaki I, Asanuma M (2011) Factors that influence primary cilium length. Acta Med Okayama 65:279-285. Medline
41. Mukhopadhyay S, Wen X, Chih B, Nelson CD, Lane WS, Scales SJ, Jackson PK (2010) TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes Dev 24:2180-2193. CrossRef Medline
42. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peränen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129:1201-1213. CrossRef Medline
43. Novarino G, Akizu N, Gleeson JG (2011) Modeling human disease in humans: the ciliopathies. Cell 147:70-79. CrossRef Medline
44. Ou Y, Ruan Y, Cheng M, Moser JJ, Rattner JB, van der Hoorn FA (2009) Adenylate cyclase regulates elongation of mammalian primary cilia. Exp Cell Res 315:2802-2817. CrossRef Medline
45. Pazour GJ, Wilkerson CG, Witman GB (1998) A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J Cell Biol 141:979-992. CrossRef Medline
46. Riccio O, Potter G, Walzer C, Vallet P, Szabó G, Vutskits L, Kiss JZ, Dayer AG (2009) Excess of serotonin affects embryonic interneuron migration through activation of the serotonin receptor 6. Mol Psychiatry 14:280-290. CrossRef Medline
47. Sarkisian MR, Siebzehnrubl D (2012) Abnormal levels of Gadd45α in developing neocortex impair neurite outgrowth. PLoS ONE 7:e44207. CrossRef Medline
48. Sarkisian MR, Bartley CM, Chi H, Nakamura F, Hashimoto-Torii K, Torii M, Flavell RA, Rakic P (2006) MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 52:789-801. CrossRef Medline
49. Satir P, Pedersen LB, Christensen ST (2010) The primary cilium at a glance. J Cell Sci 123:499-503. CrossRef Medline
50. Sattar S, Gleeson JG (2011) The ciliopathies in neuronal development: a clinical approach to investigation of Joubert syndrome and Joubert syndrome-related disorders. Dev Med Child Neurol 53:793-798. CrossRef Medline
51. Sharma N, Kosan ZA, Stallworth JE, Berbari NF, Yoder BK (2011) Soluble levels of cytosolic tubulin regulate ciliary length control. Mol Biol Cell 22:806-816. CrossRef Medline
52. 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. CrossRef Medline
53. 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. CrossRef Medline
54. Tai AW, Chuang JZ, Bode C, Wolfrum U, Sung CH (1999) Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell 97:877-887. CrossRef Medline
55. Taschner M, Bhogaraju S, Lorentzen E (2012) Architecture and function of IFT complex proteins in ciliogenesis. Differentiation 83 [Suppl]:S12-S22.
56. Verrier JD, Madorsky I, Coggin WE, Geesey M, Hochman M, Walling E, Daroszewski D, Eccles KS, Ludlow R, Semple-Rowland SL (2011) Bicistronic lentiviruses containing a viral 2A cleavage sequence reliably coexpress two proteins and restore vision to an animal model of LCA1. PLoS One 6:e20553. CrossRef Medline
57. Wang Z, Phan T, Storm DR (2011) The type 3 adenylyl cyclase is required for novel object learning and extinction of contextual memory: role of cAMP signaling in primary cilia. J Neurosci 31:5557-5561. CrossRef Medline
58. Willaredt MA, Hasenpusch-Theil K, Gardner HA, Kitanovic I, Hirschfeld- Warneken VC, Gojak CP, Gorgas K, Bradford CL, Spatz J, Wölfl S, Theil T, Tucker KL (2008) A crucial role for primary cilia in cortical morphogenesis. J Neurosci 28:12887-12900. CrossRef Medline
59. Yu JZ, Dave RH, Allen JA, Sarma T, Rasenick MM (2009) CytosolicGαs acts as an intracellular messenger to increase mi Crotubule dynamics and promote neurite outgrowth. J Biol Chem 284:10462-10472. CrossRef Medline
60. Zhang J, Shen CP, Xiao JC, Lanza TJ, Lin LS, Francis BE, Fong TM, Chen RZ (2006) Effects of mutations at conserved TM II residues on ligand binding and activation of mouse 5-HT6 receptor. Eur J Pharmacol 534:77-82. CrossRef Medline