A role for central spindle proteins in cilia structure and function.
Cytokinesis and ciliogenesis are fundamental cellular processes that require strict coordination of microtubule organization and directed membrane trafficking. These processes have been intensely studied, but there has been little indication that regulatory machinery might be extensively shared between them. Here, we show that several central spindle/midbody proteins (PRC1, MKLP-1, INCENP, centriolin) also localize in specific patterns at the basal body complex in vertebrate ciliated epithelial cells. Moreover, bioinformatic comparisons of midbody and cilia proteomes reveal a highly significant degree of overlap. Finally, we used temperature-sensitive alleles of PRC1/spd-1 and MKLP-1/zen-4 in C. elegans to assess ciliary functions while bypassing these proteins' early role in cell division. These mutants displayed defects in both cilia function and cilia morphology. Together, these data suggest the conserved reuse of a surprisingly large number of proteins in the cytokinetic apparatus and in cilia.
Section of Molecular Cell and Developmental Biology, University of Texas at Austin, Austin, Texas, USA.
Katherine R
KR
Smith
Esther K
EK
Kieserman
Peggy I
PI
Wang
Sander G
SG
Basten
Rachel H
RH
Giles
Edward M
EM
Marcotte
John B
JB
Wallingford
D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002923:Cilia / Q000235:genetics / Q000378:metabolism*; D007814:Larva; D008869:Microtubule-Associated Proteins / Q000235:genetics / Q000378:metabolism*; D009154:Mutation; D029867:Xenopus Proteins / Q000235:genetics / Q000378:metabolism*; D014982:Xenopus laevis
D029742:Caenorhabditis elegans Proteins; D008869:Microtubule-Associated Proteins; D029867:Xenopus Proteins
EMBO J. 2007 Jun 20;26(12):2966-80
17510633
Nat Cell Biol. 2009 Nov;11(11):1332-9
19855387
Nat Cell Biol. 2007 Apr;9(4):436-44
17351640
Science. 2005 Mar 18;307(5716):1735-9
15774750
Cell. 2007 Aug 24;130(4):678-90
17719545
Dev Cell. 2008 May;14(5):762-74
18477458
Nat Cell Biol. 2009 Oct;11(10):1225-32
19767740
Exp Cell Res. 2005 Oct 1;309(2):379-89
16018997
Mol Biol Cell. 2009 May;20(10):2522-9
19297529
J Cell Sci. 1968 Jun;3(2):207-30
5661997
Nature. 2007 May 3;447(7140):97-101
17450123
Mol Cell. 1998 Dec;2(6):877-85
9885575
Cell. 1997 Oct 17;91(2):161-9
9346234
Nature. 2010 Apr 15;464(7291):1048-51
20393563
Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3380-5
18299575
Cell. 2004 May 14;117(4):527-39
15137945
Curr Biol. 2003 Jul 1;13(13):1145-9
12842015
Mol Biol Cell. 2004 Nov;15(11):5172-86
15371535
Curr Biol. 2008 Jan 22;18(2):116-23
18207743
J Mol Biol. 2005 Feb 25;346(3):677-87
15713455
Cell. 2007 Jun 15;129(6):1201-13
17574030
Methods Mol Biol. 2006;322:69-86
16739717
J Cell Sci. 2007 Jun 1;120(Pt 11):1868-76
17488776
Trends Genet. 2006 Sep;22(9):491-500
16860433
PLoS Biol. 2009 Oct;7(10):e1000213
19806183
Curr Biol. 2007 Feb 6;17(3):193-202
17276912
Dev Biol. 1985 Sep;111(1):158-70
3928418
Mol Cell. 2000 Mar;5(3):411-21
10882127
Nat Genet. 2006 Sep;38(9):961-2
16940995
Nucleic Acids Res. 2010 Jan;38(Database issue):D155-60
19783819
Mol Cell Proteomics. 2007 Aug;6(8):1299-317
17494944
Am J Respir Cell Mol Biol. 2005 Jul;33(1):41-7
15845866
Nat Genet. 2008 Feb;40(2):181-8
18223650
Cell. 2005 Oct 7;123(1):75-87
16213214
Nature. 2006 Apr 13;440(7086):954-8
16612388
Am J Anat. 1968 Jan;122(1):19-55
5654501
CSH Protoc. 2008 Feb 01;2008:pdb.prot4957
21356778
EMBO J. 2004 Aug 18;23(16):3237-48
15297875
Nature. 2003 Dec 4;426(6966):570-4
14654843
Dev Biol. 1986 Oct;117(2):456-87
2428682
Anat Rec. 1968 Oct;162(2):221-32
5726142
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7157-62
17420466
Nat Rev Mol Cell Biol. 2009 Jan;10(1):9-20
19197328
J Cell Biol. 2008 Jan 14;180(1):17-21
18180369
Nucleic Acids Res. 2009 Jan;37(Database issue):D690-7
19033362
J Comp Neurol. 1997 Oct 13;387(1):148-56
9331178
Curr Top Dev Biol. 2008;85:371-427
19147012
Dev Biol. 2007 Dec 1;312(1):115-30
17961536
Nat Genet. 2006 Mar;38(3):303-11
16493421
Science. 2004 Jul 2;305(5680):61-6
15166316
J Cell Biol. 2008 Jun 2;181(5):777-90
18504302
Nature. 2009 Apr 2;458(7238):651-4
19242413
Curr Biol. 2005 Jun 21;15(12):1090-8
15964273
Genetics. 1998 Jul;149(3):1303-21
9649522
J Cell Sci. 2005 Mar 1;118(Pt 5):1007-20
15731008
Nat Genet. 2008 Jul;40(7):871-9
18552847
Curr Opin Cell Biol. 2010 Feb;22(1):75-80
19962875
Genome Biol. 2008;9 Suppl 1:S4
18613948
Curr Biol. 2004 Oct 5;14(19):1755-60
15458647
Cell. 2004 May 14;117(4):541-52
15137946