Requirement of NPHP5 in the Hierarchical Assembly of Basal Feet Associated with Basal Bodies of Primary Cilia

Overview

Journal Cell Mol Life Sci

Publisher Springer

Specialty Biology

Date 2019 Jun 10

PMID 31177295

Citations 4

Authors

Delowar Hossain

Marine Barbelanne

William Y Tsang

Affiliations

Soon will be listed here.

Abstract

During ciliogenesis, the mother centriole transforms into a basal body competent to nucleate a cilium. The mother centriole and basal body possess sub-distal appendages (SDAs) and basal feet (BF), respectively. SDAs and BF are thought to be equivalent structures. In contrast to SDA assembly, little is known about the players involved in BF assembly and its assembly order. Furthermore, the contribution of BF to ciliogenesis is not understood. Here, we found that SDAs are distinguishable from BF and that the protein NPHP5 is a novel SDA and BF component. Remarkably, NPHP5 is specifically required for BF assembly in cells able to form basal bodies but is dispensable for SDA assembly. Determination of the hierarchical assembly reveals that NPHP5 cooperates with a subset of SDA/BF proteins to organize BF. The assembly pathway of BF is similar but not identical to that of SDA. Loss of NPHP5 or a BF protein simultaneously inhibits BF assembly and primary ciliogenesis, and these phenotypes could be rescued by manipulating the expression of certain components in the BF assembly pathway. These findings define a novel role for NPHP5 in specifically regulating BF assembly, a process which is tightly coupled to primary ciliogenesis.

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References

Inaba H, Goto H, Kasahara K, Kumamoto K, Yonemura S, Inoko A . Ndel1 suppresses ciliogenesis in proliferating cells by regulating the trichoplein-Aurora A pathway. J Cell Biol. 2016; 212(4):409-23. PMC: 4754717. DOI: 10.1083/jcb.201507046. View

Das A, Qian J, Tsang W . USP9X counteracts differential ubiquitination of NPHP5 by MARCH7 and BBS11 to regulate ciliogenesis. PLoS Genet. 2017; 13(5):e1006791. PMC: 5446187. DOI: 10.1371/journal.pgen.1006791. View

Delgehyr N, Sillibourne J, Bornens M . Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J Cell Sci. 2005; 118(Pt 8):1565-75. DOI: 10.1242/jcs.02302. View

Mazo G, Soplop N, Wang W, Uryu K, Tsou M . Spatial Control of Primary Ciliogenesis by Subdistal Appendages Alters Sensation-Associated Properties of Cilia. Dev Cell. 2016; 39(4):424-437. PMC: 5125554. DOI: 10.1016/j.devcel.2016.10.006. View

Vorobjev I, Chentsov YuS . Centrioles in the cell cycle. I. Epithelial cells. J Cell Biol. 1982; 93(3):938-49. PMC: 2112136. DOI: 10.1083/jcb.93.3.938. View

Graser S, Stierhof Y, Lavoie S, Gassner O, Lamla S, Le Clech M . Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol. 2007; 179(2):321-30. PMC: 2064767. DOI: 10.1083/jcb.200707181. View

Gordon R . Three-dimensional organization of microtubules and microfilaments of the basal body apparatus of ciliated respiratory epithelium. Cell Motil. 1982; 2(4):385-91. DOI: 10.1002/cm.970020407. View

Pugacheva E, Jablonski S, Hartman T, Henske E, Golemis E . HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell. 2007; 129(7):1351-63. PMC: 2504417. DOI: 10.1016/j.cell.2007.04.035. View

Ibi M, Zou P, Inoko A, Shiromizu T, Matsuyama M, Hayashi Y . Trichoplein controls microtubule anchoring at the centrosome by binding to Odf2 and ninein. J Cell Sci. 2011; 124(Pt 6):857-64. DOI: 10.1242/jcs.075705. View

10.

Ishikawa H, Kubo A, Tsukita S, Tsukita S . Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat Cell Biol. 2005; 7(5):517-24. DOI: 10.1038/ncb1251. View

11.

Inoko A, Matsuyama M, Goto H, Ohmuro-Matsuyama Y, Hayashi Y, Enomoto M . Trichoplein and Aurora A block aberrant primary cilia assembly in proliferating cells. J Cell Biol. 2012; 197(3):391-405. PMC: 3341160. DOI: 10.1083/jcb.201106101. View

12.

Kobayashi T, Dynlacht B . Regulating the transition from centriole to basal body. J Cell Biol. 2011; 193(3):435-44. PMC: 3087006. DOI: 10.1083/jcb.201101005. View

13.

Nigg E, Stearns T . The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries. Nat Cell Biol. 2011; 13(10):1154-60. PMC: 3947860. DOI: 10.1038/ncb2345. View

14.

Hehnly H, Chen C, Powers C, Liu H, Doxsey S . The centrosome regulates the Rab11- dependent recycling endosome pathway at appendages of the mother centriole. Curr Biol. 2012; 22(20):1944-50. PMC: 3917512. DOI: 10.1016/j.cub.2012.08.022. View

15.

Sonnen K, Schermelleh L, Leonhardt H, Nigg E . 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol Open. 2012; 1(10):965-76. PMC: 3507176. DOI: 10.1242/bio.20122337. View

16.

Sang L, Miller J, Corbit K, Giles R, Brauer M, Otto E . Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell. 2011; 145(4):513-28. PMC: 3383065. DOI: 10.1016/j.cell.2011.04.019. View

17.

ODOR D, BLANDAU R . Observations on the solitary cilium of rabbit oviductal epithelium: its motility and ultrastructure. Am J Anat. 1985; 174(4):437-53. DOI: 10.1002/aja.1001740407. View

18.

Mogensen M, Malik A, Piel M, Bornens M . Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J Cell Sci. 2000; 113 ( Pt 17):3013-23. DOI: 10.1242/jcs.113.17.3013. View

19.

Gromley A, Jurczyk A, Sillibourne J, Halilovic E, Mogensen M, Groisman I . A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase. J Cell Biol. 2003; 161(3):535-45. PMC: 2172935. DOI: 10.1083/jcb.200301105. View

20.

Takeda S, Yonekawa Y, Tanaka Y, Okada Y, Nonaka S, Hirokawa N . Left-right asymmetry and kinesin superfamily protein KIF3A: new insights in determination of laterality and mesoderm induction by kif3A-/- mice analysis. J Cell Biol. 1999; 145(4):825-36. PMC: 2133177. DOI: 10.1083/jcb.145.4.825. View