Development and distribution of neuronal cilia in mouse neocortex

Journal of Comparative Neurology

Volumn 520, Issue 4, 2012, Pages 848-873

  Arellano, Jon I ^a   Guadiana, Sarah M ^b   Breunig, Joshua J ^c   Rakic, Pasko ^a   Sarkisian, Matthew R ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Axoneme; Centrioles; Ciliogenesis; Corticogenesis; Forebrain; Interneuron; Protracted maturation; Pyramidal cell

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE III; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; CELL POLARITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CENTRIOLE; CILIARY NERVE; CILIOGENESIS; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; FETUS; IMMUNOHISTOCHEMISTRY; INTERNEURON; KINETOSOME; NEOCORTEX; NERVE CELL; NEUROBLAST; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL;

ACTINS; ADENYLATE CYCLASE; ANIMALS; ANTIBODIES; ANTIGENS; AXONS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL POLARITY; CHICKENS; CILIA; ELECTROPORATION; EMBRYONIC DEVELOPMENT; FEMALE; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, ELECTRON; MICROSCOPY, IMMUNOELECTRON; NEOCORTEX; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PARVALBUMINS; PREGNANCY;

EID: 84855517436     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22793     Document Type: Article

References (88)

1. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M. 1997. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci U S A 94: 1488-1493.
2. Amador-Arjona A, Elliott J, Miller A, Ginbey A, Pazour GJ, Enikolopov G, Roberts AJ, Terskikh AV. 2011. Primary cilia regulate proliferation of amplifying progenitors in adult hippocampus: implications for learning and memory. J Neurosci 31: 9933-9944.
3. 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. (Epub 2010, Jun 4).
4. Barzi M, Berenguer J, Menendez A, Alvarez-Rodriguez R, Pons S. 2010. Sonic-hedgehog-mediated proliferation requires the localization of PKA to the cilium base. J Cell Sci 123: 62-69.
5. Bearzatto B, Servais L, Roussel C, Gall D, Baba-Aissa F, Schurmans S, de Kerchove d'Exaerde A, Cheron G, Schiffmann SN. 2006. Targeted calretinin expression in granule cells of calretinin-null mice restores normal cerebellar functions. FASEB J 20: 380-382.
6. Belgacem YH, Borodinsky LN. 2011. Sonic hedgehog signaling is decoded by calcium spike activity in the developing spinal cord. Proc Natl Acad Sci U S A 108: 4482-4487.
7. 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 (E-pub 25 April 2011).
8. Berbari NF, Bishop GA, Askwith CC, Lewis JS, Mykytyn K. 2007. Hippocampal neurons possess primary cilia in culture. J Neurosci Res 85: 1095-1100.
9. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K. 2008. 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.
10. 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.
11. 6 receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res 872: 271-275.
12. 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.
13. Celio MR, Heizmann CW. 1981. Calcium-binding protein parvalbumin as a neuronal marker. Nature 293: 300-302.
14. Celio MR, Baier W, Scharer L, Gregersen HJ, de Viragh PA, Norman AW. 1990. Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. Cell Calcium 11: 599-602.
15. 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.
16. Cho YJ, Lee JC, Kang BG, An J, Song HS, Son O, Nam DH, Cha CI, Joo KM. 2011. Immunohistochemical study on the expression of calcium binding proteins (calbindin-D28k, calretinin, and parvalbumin) in the cerebral cortex and in the hippocampal region of nNOS knock-out(-/-) mice. Anat Cell Biol 44: 106-115.
17. Cohen E, Binet S, Meininger V. 1988. Ciliogenesis and centriole formation in the mouse embryonic nervous system. An ultrastructural analysis. Biol Cell 62: 165-169.
18. Dahl HA. 1963. Fine structure of cilia in rat cerebral cortex. Z Zellforsch Mikrosk Anat 60: 369-386.
19. 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.
20. Defelipe J, Gonzalez-Albo MC, Del Rio MR, Elston GN. 1999. Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412: 515-526.
21. Domire JS, Mykytyn K. 2009. Markers for neuronal cilia. Methods Cell Biol 91: 111-121.
22. Domire JS, Green JA, Lee KG, Johnson AD, Askwith CC, Mykytyn K. 2010. Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Cell Mol Life Sci (E-pub 9 December 2010).
23. Doxsey SJ, Stein P, Evans L, Calarco PD, Kirschner M. 1994. Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76: 639-650.
24. Dredge BK, Jensen KB. 2011. NeuN/Rbfox3 Nuclear and cytoplasmic isoforms differentially regulate alternative splicing and nonsense-mediated decay of Rbfox2. PLoS ONE 6: e21585.
25. Dubreuil V, Marzesco AM, Corbeil D, Huttner WB, Wilsch-Brauninger M. 2007. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J Cell Biol 176: 483-495.
26. 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.
27. Feng L, Cooper JA. 2009. Dual functions of Dab1 during brain development. Mol Cell Biol 29: 324-332.
28. Ferland RJ, Cherry TJ, Preware PO, Morrisey EE, Walsh CA. 2003. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol 460: 266-279.
29. Fiala JC. 2005. Reconstruct: a free editor for serial section microscopy. J Microsc 218: 52-61.
30. Fuchs JL, Schwark HD. 2004. Neuronal primary cilia: a review. Cell Biol Int 28: 111-118.
31. Goetz SC, Anderson KV. 2010. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11: 331-344.
32. Green JA, Mykytyn K. 2010. Neuronal ciliary signaling in homeostasis and disease. Cell Mol Life Sci 67: 3287-3297.
33. 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.
34. Handel M, Schulz S, Stanarius A, Schreff M, Erdtmann-Vourliotis M, Schmidt H, Wolf G, Hollt V. 1999. Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89: 909-926.
35. Higginbotham HR, Gleeson JG. 2007. The centrosome in neuronal development. Trends Neurosci 30: 276-283.
36. Jurczyk A, Pino SC, O'sullivan-Murphy B, Addorio M, Lidstone EA, Diiorio P, Lipson KL, Standley C, Fogarty K, Lifshitz L, Urano F, Mordes JP, Greiner DL, Rossini AA, Bortell R. 2010. A novel role for the centrosomal protein, pericentrin, in regulation of insulin secretory vesicle docking in mouse pancreatic beta-cells. PLoS ONE 5: e11812.
37. Kao HT, Li P, Chao HM, Janoschka S, Pham K, Feng J, McEwen BS, Greengard P, Pieribone VA, Porton B. 2008. Early involvement of synapsin III in neural progenitor cell development in the adult hippocampus. J Comp Neurol 507: 1860-1870.
38. Kim J, Lee JE, Heynen-Genel S, Suyama E, Ono K, Lee K, Ideker T, Aza-Blanc P, Gleeson JG. 2010. Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464: 1048-1051.
39. Kim KK, Adelstein RS, Kawamoto S. 2009. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284: 31052-31061.
40. Lee JH, Gleeson JG. 2010. The role of primary cilia in neuronal function. Neurobiol Dis 38: 167-172.
41. LeVay S. 1973. Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations. J Comp Neurol 150: 53-85.
42. Li A, Saito M, Chuang JZ, Tseng YY, Dedesma C, Tomizawa K, Kaitsuka T, Sung CH. 2011. Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat Cell Biol 13: 402-411.
43. Lund JS, Boothe RG, Lund RD. 1977. Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): a Golgi study from fetal day 127 to postnatal maturity. J Comp Neurol 176: 149-188.
44. Lyck L, Kroigard T, Finsen B. 2007. Unbiased cell quantification reveals a continued increase in the number of neocortical neurones during early post-natal development in mice. Eur J Neurosci 26: 1749-1764.
45. Miyoshi K, Kasahara K, Miyazaki I, Asanuma M. 2009. Lithium treatment elongates primary cilia in the mouse brain and in cultured cells. Biochem Biophys Res Commun 388: 757-762.
46. Morris RL, Scholey JM. 1997. Heterotrimeric kinesin-II is required for the assembly of motile 9 + 2 ciliary axonemes on sea urchin embryos. J Cell Biol 138: 1009-1022.
47. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116: 201-211.
48. Murthy KS, Makhlouf GM. 1997. Differential coupling of muscarinic m2 and m3 receptors to adenylyl cyclases V/VI in smooth muscle. Concurrent M2-mediated inhibition via Galphai3 and m3-mediated stimulation via Gbetagammaq. J Biol Chem 272: 21317-21324.
49. Nigg EA, Raff JW. 2009. Centrioles, centrosomes, and cilia in health and disease. Cell 139: 663-678.
50. 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.
51. Paxinos G, Franklin KBJ. 2004. The mouse brain in stereotaxic coordinates. London: Academic Press.
52. Pazour GJ, Dickert BL, Vucica Y, Seeley ES, Rosenbaum JL, Witman GB, Cole DG. 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151: 709-718.
53. Pedersen LB, Rosenbaum JL. 2008. Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85: 23-61.
54. Pedersen LB, Veland IR, Schroder JM, Christensen ST. 2008. Assembly of primary cilia. Dev Dyn 237: 1993-2006.
55. Poole CA, Jensen CG, Snyder JA, Gray CG, Hermanutz VL, Wheatley DN. 1997. Confocal analysis of primary cilia structure and colocalization with the Golgi apparatus in chondrocytes and aortic smooth muscle cells. Cell Biol Int 21: 483-494.
56. Rasin MR, Gazula VR, Breunig JJ, Kwan KY, Johnson MB, Liu-Chen S, Li HS, Jan LY, Jan YN, Rakic P, Sestan N. 2007. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat Neurosci 10: 819-827.
57. Rooryck C, Pelras S, Chateil JF, Cances C, Arveiler B, Verloes A, Lacombe D, Goizet C. 2007. Bardet-Biedl syndrome and brain abnormalities. Neuropediatrics 38: 5-9.
58. Saino-Saito S, Hozumi Y, Goto K. 2011. Excitotoxicity by kainate-induced seizure causes diacylglycerol kinase zeta to shuttle from the nucleus to the cytoplasm in hippocampal neurons. Neurosci Lett 494: 185-189.
59. Sarkisian MR, Frenkel M, Li W, Oborski JA, LoTurco JJ. 2001. Altered interneuron development in the cerebral cortex of the flathead mutant. Cereb Cortex 11: 734-743.
60. 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.
61. Sfakianos J, Togawa A, Maday S, Hull M, Pypaert M, Cantley L, Toomre D, Mellman I. 2007. Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells. J Cell Biol 179: 1133-1140.
62. Sharma N, Berbari NF, Yoder BK. 2008. Ciliary dysfunction in developmental abnormalities and diseases. Curr Top Dev Biol 85: 371-427.
63. Sharma N, Kosan ZA, Stallworth JE, Berbari NF, Yoder BK. 2011. Soluble levels of cytosolic tubulin regulate ciliary length control. Mol Biol Cell 22: 808-816.
64. Sorokin S. 1962. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J Cell Biol 15: 363-377.
65. Sorokin SP. 1968. Centriole formation and ciliogenesis. Aspen Emphysema Conf 11: 213-216.
66. Sotelo JR, Trujillo-Cenoz O. 1958. Electron microscope study on the development of ciliary components of the neural epithelium of the chick embryo. Z Zellforsch Mikrosk Anat 49: 1-12.
67. 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.
68. Stanic D, Malmgren H, He H, Scott L, Aperia A, Hokfelt T. 2009. Developmental changes in frequency of the ciliary somatostatin receptor 3 protein. Brain Res 1249: 101-112.
69. Stillman AA, Krsnik Z, Sun J, Rasin MR, State MW, Sestan N, Louvi A. 2009. Developmentally regulated and evolutionarily conserved expression of SLITRK1 in brain circuits implicated in Tourette syndrome. J Comp Neurol 513: 21-37.
70. 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.
71. Tsai JW, Bremner KH, Vallee RB. 2007. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 10: 970-979.
72. Tucker RW, Pardee AB, Fujiwara K. 1979a. Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells. Cell 17: 527-535.
73. Tucker RW, Scher CD, Stiles CD. 1979b. Centriole deciliation associated with the early response of 3T3 cells to growth factors but not to SV40. Cell 18: 1065-1072.
74. Tury A, Mairet-Coello G, Dicicco-Bloom E. 2011. The cyclin-dependent kinase inhibitor p57Kip2 regulates cell cycle exit, differentiation, and migration of embryonic cerebral cortical precursors. Cereb Cortex 21: 1840-1856.
75. Van Eden CG, Uylings HB. 1985. Cytoarchitectonic development of the prefrontal cortex in the rat. J Comp Neurol 241: 253-267.
76. Waclaw RR, Ehrman LA, Pierani A, Campbell K. 2010. Developmental origin of the neuronal subtypes that comprise the amygdalar fear circuit in the mouse. J Neurosci 30: 6944-6953.
77. Wang Y, Yin X, Rosen G, Gabel L, Guadiana SM, Sarkisian MR, Galaburda AM, Loturco JJ. 2011. Dcdc2 knockout mice display exacerbated developmental disruptions following knockdown of doublecortin. Neuroscience 190: 398-408.
78. 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.
79. Wei J, Wayman G, Storm DR. 1996. Phosphorylation and inhibition of type III adenylyl cyclase by calmodulin-dependent protein kinase II in vivo. J Biol Chem 271: 24231-24235.
80. Wei J, Zhao AZ, Chan GC, Baker LP, Impey S, Beavo JA, Storm DR. 1998. Phosphorylation and inhibition of olfactory adenylyl cyclase by CaM kinase II in neurons: a mechanism for attenuation of olfactory signals. Neuron 21: 495-504.
81. Westra JW, Peterson SE, Yung YC, Mutoh T, Barral S, Chun J. 2008. Aneuploid mosaicism in the developing and adult cerebellar cortex. J Comp Neurol 507: 1944-1951.
82. White EL, Rock MP. 1980. Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections. J Neurocytol 9: 615-636.
83. Whitfield JF. 2004. The neuronal primary cilium-an extrasynaptic signaling device. Cell Signal 16: 763-767.
84. Willaredt MA, Hasenpusch-Theil K, Gardner HA, Kitanovic I, Hirschfeld-Warneken VC, Gojak CP, Gorgas K, Bradford CL, Spatz J, Wolfl S, Theil T, Tucker KL. 2008. A crucial role for primary cilia in cortical morphogenesis. J Neurosci 28: 12887-12900.
85. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat Rev Neurosci 7: 687-696.
86. Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR. 2000. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27: 487-497.
87. Xu H, He JH, Xiao ZD, Zhang QQ, Chen YQ, Zhou H, Qu LH. 2010. Liver-enriched transcription factors regulate microRNA-122 that targets CUTL1 during liver development. Hepatology 52: 1431-1442.
88. 2+-binding status and differences in antigen accessibility in colon cancer cells. Cell Calcium 31: 13-25.