Basic biology and mechanisms of neural ciliogenesis and the B9 family

Molecular Neurobiology

Volumn 45, Issue 3, 2012, Pages 564-570

  Gate, David ^a   Danielpour, Moise ^a   Levy, Rachelle ^a   Breunig, Joshua J ^a   Town, Terrence ^a,b  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

B9 C2 family; Ciliary signaling; Neural ciliogenesis; Neural ciliopathy; Primary cilia; Progenitor; Stem cell

Indexed keywords

MEMBRANE PROTEIN;

ANIMAL; BRAIN TUMOR; EUKARYOTIC FLAGELLUM; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; NERVE CELL; NERVOUS SYSTEM; ORGANOGENESIS; PATHOLOGY; REVIEW;

ANIMALS; BRAIN NEOPLASMS; CILIA; HUMANS; MEMBRANE PROTEINS; NERVOUS SYSTEM; NEURONS; ORGANOGENESIS;

EID: 84867437340     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8276-7     Document Type: Article

References (75)

1. Dobell C, van Leeuwenhoek A (1958) Antony van Leeuwenhoek and his "Little animals": being some account of the father of protozoology and bacteriology and his multifarious discoveries in these disciplines. Russell & Russell, New York
2. Haimo LT, Rosenbaum JL (1981) Cilia, flagella, and microtubules. J Cell Biol 91(3 Pt 2):125s-130s
3. Satir P (1995) Landmarks in cilia research from Leeuwenhoek to us. Cell Motil Cytoskeleton 32(2):90-94
4. Zimmerman KW (1898) Beitrage zur kenntniss einiger drusen und epithelien. Archiv for Mikrosk Anat 52:552-706
5. Dellinger OP (1909) The cilium as a key to the structure of contractile protoplasm. J Morphol 20:171-209
6. Grave C, Schmitt FO (1924) A Mechanism for the coordination and regulation of the movement of cilia of epithelia. Science 60 (1550):246-248
7. Jakus MA, Hall CE (1946) Electron microscope observations of the trichocysts and cilia of Paramecium. Biol Bull 91(02):141-144
8. Dahl HA (1963) Fine structure of cilia in rat cerebral cortex. Z Zellforsch Mikrosk Anat 60:369-386
9. Karlsson U (1966) Three-dimensional studies of neurons in the lateral geniculate nucleus of the rat. I. Organelle organization in the perikaryon and its proximal branches. J Ultrastruct Res 16(5):429-481
10. Louvi A, Grove EA (2011) Cilia in the CNS: the quiet organelle claims center stage. Neuron 69(6):1046-1060
11. Kozminski KG, Johnson KA et al (1993) A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90(12):5519-5523
12. Kozminski KG, Beech PL et al (1995) The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J Cell Biol 131(6 Pt 1):1517-1527
13. Perkins LA, Hedgecock EM et al (1986) Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117(2):456-487
14. Cole DG, Diener DR et al (1998) Chlamydomonas kinesin-IIdependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 141(4):993-1008
15. Collet J, Spike CA et al (1998) Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans. Genetics 148(1):187-200
16. Signor D,Wedaman KP et al (1999) Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J Cell Biol 147(3):519-530
17. Rosenbaum JL, Witman GB (2002) Intraflagellar transport. Nat Rev Mol Cell Biol 3(11):813-825
18. Pazour GJ, Dickert BL et al (2000) Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151(3):709-718
19. Rohatgi R, Milenkovic L et al (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science 317(5836):372-376
20. Milenkovic L, Scott MP et al (2009) Lateral transport of smoothened from the plasma membrane to the membrane of the cilium. J Cell Biol 187(3):365-374
21. Huangfu D, Liu A et al (2003) Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426(6962):83-87
22. Huangfu D, Anderson KV (2005) Cilia and hedgehog responsiveness in the mouse. Proc Natl Acad Sci USA 102(32):11325-11330
23. May SR, Ashique AM et al (2005) Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli. Dev Biol 287 (2):378-389
24. Tuson M, He M et al (2011) Protein kinase A acts at the basal body of the primary cilium to prevent Gli2 activation and ventralization of the mouse neural tube. Development 138(22):4921-4930
25. Delattre M, Briand S et al (1999) The suppressor of fused gene, involved in Hedgehog signal transduction in Drosophila, is conserved in mammals. Dev Genes Evol 209(5):294-300
26. Ding Q, Fukami S et al (1999) Mouse suppressor of fused is a negative regulator of sonic hedgehog signaling and alters the subcellular distribution of Gli1. Curr Biol 9(19):1119-1122
27. Kogerman P, Grimm T et al (1999) Mammalian suppressor-offused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat Cell Biol 1(5):312-319
28. Pearse RV 2nd, Collier LS et al (1999) Vertebrate homologs of Drosophila suppressor of fused interact with the gli family of transcriptional regulators. Dev Biol 212(2):323-336
29. Stone DM, Murone M et al (1999) Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli. J Cell Sci 112(Pt 23):4437-4448
30. Cooper AF, Yu KP et al (2005) Cardiac and CNS defects in a mouse with targeted disruption of suppressor of fused. Development 132(19):4407-4417
31. Svard J, Heby-Henricson K et al (2006) Genetic elimination of suppressor of fused reveals an essential repressor function in the mammalian hedgehog signaling pathway. Dev Cell 10(2):187-197
32. Jia J, Kolterud A et al (2009) Suppressor of fused inhibits mammalian hedgehog signaling in the absence of cilia. Dev Biol 330 (2):452-460
33. Haycraft CJ, Banizs B et al (2005) Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet 1(4):e53
34. Tukachinsky H, Lopez LVet al (2010) A mechanism for vertebrate hedgehog signaling: recruitment to cilia and dissociation of SuFu-Gli protein complexes. J Cell Biol 191(2):415-428
35. Zeng H, Jia J et al (2010) Coordinated translocation of mammalian Gli proteins and suppressor of fused to the primary cilium. PLoS One 5(12):e15900
36. Chen MH, Wilson CWet al (2009) Cilium-independent regulation of Gli protein function by Sufu in Hedgehog signaling is evolutionarily conserved. Genes Dev 23(16):1910-1928
37. Humke EW, Dorn KVet al (2010) The output of hedgehog signaling is controlled by the dynamic association between suppressor of fused and the Gli proteins. Genes Dev 24(7):670-682
38. Hu Q, Milenkovic L et al (2010) A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329(5990):436-439
39. Seeley ES, Nachury MV (2010) The perennial organelle: assembly and disassembly of the primary cilium. J Cell Sci 123(Pt 4):511-518
40. Hu Q, Nelson WJ (2011) Ciliary diffusion barrier: the gatekeeper for the primary cilium compartment. Cytoskeleton (Hoboken) 68 (6):313-324
41. Town T, Breunig JJ et al (2008) The stumpy gene is required for mammalian ciliogenesis. Proc Natl Acad Sci USA 105(8):2853-2858
42. Garcia-Gonzalo FR, Corbit KC et al (2011) A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 43(8):776-784
43. Williams CL, Li C et al (2011) MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J Cell Biol 192(6):1023-1041
44. Chih B, Liu P et al (2012) A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat Cell Biol 14(1):61-72
45. Zhang D, Aravind L (2010) Identification of novel families and classification of the C2 domain superfamily elucidate the origin and evolution of membrane targeting activities in eukaryotes. Gene 469(1-2):18-30
46. Williams CL,Winkelbauer ME et al (2008) Functional redundancy of the B9 proteins and nephrocystins in Caenorhabditis elegans ciliogenesis. Mol Biol Cell 19(5):2154-2168
47. Dowdle WE, Robinson JF et al (2011) Disruption of a ciliary B9 protein complex causes Meckel syndrome. Am J Hum Genet 89 (1):94-110
48. Breunig JJ, Sarkisian MR et al (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci USA 105(35):13127-13132
49. Chizhikov VV, Davenport J et al (2007) Cilia proteins control cerebellar morphogenesis by promoting expansion of the granule progenitor pool. J Neurosci 27(36):9780-9789
50. Spassky N, Han YG et al (2008) Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev Biol 317(1):246-259
51. Gherman A, Davis EE et al (2006) The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat Genet 38(9):961-962
52. Kyttala M, Tallila J et al (2006) MKS1, encoding a component of the flagellar apparatus basal body proteome, is mutated in Meckel syndrome. Nat Genet 38(2):155-157
53. Weatherbee SD, Niswander LA et al (2009) A mouse model for Meckel syndrome reveals Mks1 is required for ciliogenesis and hedgehog signaling. Hum Mol Genet 18(23):4565-4575
54. Breunig JJ, Haydar TF et al (2011) Neural stem cells: historical perspective and future prospects. Neuron 70(4):614-625
55. Guillemot F (2007) Cell fate specification in the mammalian telencephalon. Prog Neurobiol 83(1):37-52
56. Han YG, Spassky N et al (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11(3):277-284
57. Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301(3):365-381
58. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250
59. Kumamoto N, Gu Y et al (2012) A role for primary cilia in glutamatergic synaptic integration of adult-born neurons. Nat Neurosci 15:399-405
60. Badano JL, Mitsuma N et al (2006) The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7:125-148
61. Adams M, Smith UM et al (2008) Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J Med Genet 45(5):257-267
62. Gerdes JM, Davis EE et al (2009) The vertebrate primary cilium in development, homeostasis, and disease. Cell 137(1):32-45
63. Fliegauf M, Benzing T et al (2007) When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8(11):880-893
64. Budny B, Chen Wet al (2006) A novel X-linked recessive mental retardation syndrome comprising macrocephaly and ciliary dysfunction is allelic to oral-facial-digital type I syndrome. Hum Genet 120(2):171-178
65. Martinez-Campos M, Basto R et al (2004) The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J Cell Biol 165(5):673-683
66. Rauch A, Thiel CT et al (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319 (5864):816-819
67. Bishop GA, Berbari NF et al (2007) Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J Comp Neurol 505(5):562-571
68. Arellano JI, Guadiana SM et al (2012) Development and distribution of neuronal cilia in mouse neocortex. J Comp Neurol 520 (4):848-873
69. Wallace FM (2008) Chapter 1 basal bodies: platforms for building cilia. In: Bradley KY (ed) Current topics in developmental biology, vol 85. Academic, Burlington, pp 1-22
70. Pan J, SnellW (2007) The primary cilium: keeper of the key to cell division. Cell 129(7):1255-1257
71. Wang X, Tsai JW et al (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461 (7266):947-955
72. Han YG, Kim HJ et al (2009) Dual and opposing roles of primary cilia in medulloblastoma development. Nat Med 15(9):1062-1065
73. Pietsch T, Waha A et al (1997) Medulloblastomas of the desmoplastic variant carry mutations of the human homologue of Drosophila patched. Cancer Res 57(11):2085-2088
74. Raffel C, Jenkins RB et al (1997) Sporadic medulloblastomas contain PTCH mutations. Cancer Res 57(5):842-845
75. Gilbertson RJ, Ellison DW (2008) The origins of medulloblastoma subtypes. Annu Rev Pathol 3:341-365