RABL4/IFT27 in a nucleotide‐independent manner promotes phospholipase D ciliary retrieval via facilitating BBSome reassembly at the ciliary tip

Yan‐Xia Liu; Rui‐Kai Zhang; Zhen-Chuan Fan

doi:10.1002/jcp.30945

journal article Feb 28, 2023

RABL4/IFT27 in a nucleotide‐independent manner promotes phospholipase D ciliary retrieval via facilitating BBSome reassembly at the ciliary tip

Yan‐Xia Liu Rui‐Kai Zhang Zhen-Chuan Fan

Journal of Cellular Physiology Vol. 238 No. 3 pp. 549-565 · Wiley

View at Publisher Save 10.1002/jcp.30945

Abstract

AbstractCertain ciliary transmembrane and membrane‐associated signaling proteins export from cilia as intraflagellar transport (IFT) cargoes in a BBSome‐dependent manner. Upon reaching the ciliary tip via anterograde IFT, the BBSome disassembles before being reassembled to form an intact entity for cargo phospholipase D (PLD) coupling. During this BBSome remodeling process, Chlamydomonas Rab‐like 4 GTPase IFT27, by binding its partner IFT25 to form the heterodimeric IFT25/27, is indispensable for BBSome reassembly. Here, we show that IFT27 binds IFT25 in an IFT27 nucleotide‐independent manner. IFT25/27 and the IFT subcomplexes IFT‐A and ‐B are irrelevant for maintaining the stability of one another. GTP‐loading onto IFT27 enhances the IFT25/27 affinity for binding to the IFT‐B subcomplex core IFT‐B1 entity in cytoplasm, while GDP‐bound IFT27 does not prevent IFT25/27 from entering and cycling through cilia by integrating into IFT‐B1. Upon at the ciliary tip, IFT25/27 cycles on and off IFT‐B1 and this process is irrelevant with the nucleotide state of IFT27. During BBSome remodeling at the ciliary tip, IFT25/27 promotes BBSome reassembly independent of IFT27 nucleotide state, making postremodeled BBSomes available for PLD to interact with. Thus, IFT25/27 facilitates BBSome‐dependent PLD export from cilia via controlling availability of intact BBSomes at the ciliary tip, while IFT27 nucleotide state does not participate in this regulatory event.

Topics

No keywords indexed for this article. Browse by subject →

References

53

[1]

10.1093/hmg/ddu044

[2]

10.1038/emboj.2011.110

[3]

10.1016/s0960-9822(01)00485-7

[4]

10.1086/423903

[5]

10.1083/jcb.141.4.993

[6]

Dong B. "Chlamydomonas IFT25 is dispensable for flagellar assembly but required to export the BBSome from flagella" Biology Open (2017)

[7]

10.1007/s00253-017-8177-9

[8]

Rabl2 GTP hydrolysis licenses BBSome‐mediated export to fine‐tune ciliary signaling

Shichao Duan, Hao Li, Yirong Zhang et al.

The EMBO Journal 10.15252/embj.2020105499

[9]

10.1016/j.devcel.2014.09.011

[10]

10.1091/mbc.e10-03-0191

[11]

10.1038/nrm2278

[12]

10.1002/cm.20346

[13]

10.1083/jcb.200608041

[14]

10.7554/elife.02419

[15]

Ishikawa H. "TTC26/DYF13 is an intraflagellar transport protein required for transport of motility‐related proteins into flagella" eLife (2014) 10.7554/elife.01566

[16]

10.1016/j.cell.2010.05.015

[17]

10.1016/j.devcel.2012.04.009

[18]

10.1093/emboj/cdg518

[19]

10.1073/pnas.90.12.5519

[20]

10.1083/jcb.201207139

[21]

10.1083/jcb.200909183

[22]

10.1002/cm.20369

[23]

10.1016/j.devcel.2014.09.004

[24]

10.1093/biolre/iox029

[25]

10.1073/pnas.1713226115

[26]

10.1083/jcb.202111076

[27]

10.7554/elife.59119

[28]

10.1016/j.devcel.2008.11.001

[29]

10.1074/jbc.m505062200

[30]

10.1016/j.cell.2007.03.053

[31]

10.18388/abp.2001_3850

[32]

10.1038/nature04847

[33]

10.1083/jcb.151.3.709

[34]

10.1083/jcb.141.4.979

[35]

10.1016/j.cub.2006.12.040

[36]

Intraflagellar transport

Joel L. Rosenbaum, George B. Witman

Nature Reviews Molecular Cell Biology 10.1038/nrm952

[37]

10.3389/fgene.2019.00021

[38]

10.1136/jmedgenet-2013-101785

[39]

10.1371/journal.pgen.1002358

[40]

10.1073/pnas.2101590118

[41]

10.1242/bio.033241

[42]

Crystal structures of IFT70/52 and IFT52/46 provide insight into intraflagellar transport B core complex assembly

Michael Taschner, Fruzsina Kotsis, Philipp Braeuer et al.

The Journal of cell biology 10.1083/jcb.201408002

[43]

10.15252/embj.201593164

[44]

10.15252/embj.2018101251

[45]

10.1371/journal.pone.0005384

[46]

10.1042/ebc20180030

[47]

10.1042/bj1270597

[48]

10.1073/pnas.1901665117

[49]

10.1111/febs.16232

[50]

10.1073/pnas.1113220108

Showing 50 of 53 references

Metrics

8

Citations

53

References

Details

Published: Feb 28, 2023
Vol/Issue: 238(3)
Pages: 549-565
License: View

Authors

Y

Yan‐Xia Liu

State Key Laboratory of Food Nutrition and Safety, Institute of Health Biotechnology Tianjin University of Science and Technology Tianjin China

R

Rui‐Kai Zhang

State Key Laboratory of Food Nutrition and Safety, Institute of Health Biotechnology Tianjin University of Science and Technology Tianjin China

Z

Zhen-Chuan Fan

State Key Laboratory of Food Nutrition and Safety, Institute of Health Biotechnology Tianjin University of Science and Technology Tianjin China

Funding

National Natural Science Foundation of China

China Postdoctoral Science Foundation

Cite This Article

Yan‐Xia Liu, Rui‐Kai Zhang, Zhen-Chuan Fan (2023). RABL4/IFT27 in a nucleotide‐independent manner promotes phospholipase D ciliary retrieval via facilitating BBSome reassembly at the ciliary tip. Journal of Cellular Physiology, 238(3), 549-565. https://doi.org/10.1002/jcp.30945

RABL4/IFT27 in a nucleotide‐independent manner promotes phospholipase D ciliary retrieval via facilitating BBSome reassembly at the ciliary tip

You May Also Like