More than Maintenance? A
Role for IFT Genes in Planar
Cell Polarity
Kimberly M. Jaffe and Rebecca D. Burdine
Department of Molecular Biology, Princeton University, Princeton,
New Jersey
J Am Soc Nephrol 21: 1240–1241, 2010.
doi: 10.1681/ASN.2010060665
Once thought to be vestigial organelles, cilia are now recog-
nized as important signaling and sensory centers within some
cells.
1–3
The process of intraflagellar transport (IFT) controls
cilia formation and the targeting of proteins within the cilium.
IFT depends on three key components: (1) An anterograde
complex that traffics from the base of the cilium to the tip and
consists of the kinesin 2 motor and the IFTB protein complex;
(2) the retrograde complex that brings cargo from the ciliary
tip to the base and consists of the cytoplasmic dynein motor
and the IFTA protein complex; and (3) IFTA and B complexes
that associate with motors are thought to act as docking sites
for IFT cargo.
4
In most organisms, loss of the IFTB complex blocks forma-
tion of cilia. In zebrafish, however, zygotic mutants in B com-
plex members IFT57, IFT88, and IFT172 still assemble cilia,
which degenerate over time, suggesting these IFT proteins are
not required for cilia formation. This has led one group to
propose that IFT in zebrafish is not required to assemble cilia
but rather acts to maintain cilia once they assemble.
5
In this issue of JASN, Cao et al.
6
more carefully examine the
maternal deposition of IFT57 and IFT72 at the mRNA and pro-
tein level. The authors show these proteins are maternally sup-
plied, which likely explains why these mutants can form cilia early
in development. This is in agreement with other studies suggest-
ing maternal IFT proteins allow cilia to form in zygotic ift mu-
tants.
7,8
In fact, this was tested most rigorously by creation of ma-
ternal and zygotic ift88 mutants (MZift88; generated by germline
replacement) that lack cilia in all examined tissues.
7
The more intriguing findings in the article by Cao et al.
6
involve a possible involvement for IFT genes in planar cell
polarity (PCP).
9,10
The PCP pathway was first identified in
Drosophila as an important organizer of epithelial cell polarity
during such processes as achieving proper hair and bristle ori-
entation along the body.
11
In vertebrate embryos, PCP is in-
volved in a variety of phenotypes linked to polarization of ep-
ithelia, including oriented cell divisions, neural tube closure,
orientation of stereocilia bundles in the ear, cyst formation in
the kidney, and convergent extension movements during gas-
trulation and organ formation.
3,12
While examining the multiciliated cells of the zebrafish em-
bryonic kidney (the pronephros), Cao et al
6
. found that basal
bodies were disorganized in ift mutants but still localized api-
cally. This defect, as well as the presence of kidney cysts in these
mutants, is reminiscent of a PCP defect. In fact, the authors
find antisense knockdown of the core PCP gene prickle leads to
similar phenotypes in cyst formation and basal body orienta-
tion in the pronephros in addition to convergent extension
defects. Although MZift88 mutants are not reported to have
convergent extension phenotypes even though cilia are ab-
sent,
7
Cao et al.
6
show that suboptimal knockdown of the ift
genes, including ift88, strongly synergizes with suboptimal
knockdown of prickle in convergent extension. Taken together,
these findings suggest IFT57, IFT88, and IFT172 function co-
ordinately with Prickle to regulate PCP. These findings nicely
agree with recently published work showing that zebrafish ma-
ternal zygotic mutants in the core PCP gene, vangl2, lead to
pronephric tubule distension and misorientation of basal bod-
ies in the neural tube and other tissues.
13
The looming question, though, is how would mutations in ift
genes act to affect PCP? One possibility is that knockdown of the
ift genes and prickle synergize at the level of cilia formation with
loss of cilia leading to a PCP-like phenotype. Indeed, PCP is im-
plicated in cilia formation, because mutations in some PCP genes
including inturned, fuzzy, and dishevelled affect ciliogenesis. In ad-
dition, it is clear that mutations affecting cilia can lead to PCP-like
phenotypes.
3,12
It would be interesting to know whether knock-
down of the ift genes and prickle synergize to affect cilia formation,
but this was not examined by Cao et al.
6
It has also been argued that the PCP proteins that affect
ciliogenesis are not core PCP proteins or function in additional
signaling pathways.
13
In fact, loss of the core PCP gene, Vangl2,
does not display a defect in ciliogenesis.
13
Likewise, the protein
Seahorse/Lrrc6 displays cilia-related phenotypes and interacts
with PCP components, but cilia formation and length are un-
affected.
14,15
These findings and others suggest that PCP may
function downstream of or parallel to cilia.
In fact, PCP acts in the orientation of cilia or basal body
location and orientation.
3,12
Loss of this orientation can have
functional consequences for embryos such as disruption of
fluid flow leading to laterality defects in zebrafish or loss of
orientation in hair cells in the mouse ear.
13,16
In the latter
study, mutations in Ift88 synergized with Vangl2 in orientation
of the hair cells.
16
Intriguingly, in both of those studies, al-
though cilia location was altered, asymmetric localization of
PCP components was not affected in those cells.
13,16
This sug-
gests PCP is properly established in these cells but the informa-
tion cannot be used properly. Perhaps the IFT genes cooperate
with core PCP genes to help interpret PCP information and
orient the cilium and or basal body.
Alternatively, some IFT genes might not be solely involved
with ciliogenesis.
17
For example, IFT20 associates with the
Published online ahead of print. Publication date available at www.jasn.org.
Correspondence: Dr. Rebecca D. Burdine, Department of Molecular Biology,
Princeton University, Washington Road Mof 433, Princeton, NJ 08544. Phone:
609-258-7515; Fax: 609-258-6730; E-mail: rburdine@princeton.edu
Copyright © 2010 by the American Society of Nephrology
EDITORIALS www.jasn.org
1240 Journal of the American Society of Nephrology J Am Soc Nephrol 21: 1238 –1246, 2010