Stalling interkinetic nuclear migration in curved pseudostratified epithelium of developing cochlea

1.

2.

3.

Hirashima T. 2014 Pattern formation of

an epithelial tubule by mechanical

instability during epididymal development. Cell

Rep. 9, 866–873. (doi:10.1016/j.celrep.2014.09.

041)

Savin T, Kurpios NA, Shyer AE, Florescu P, Liang

H, Mahadevan L, Tabin CJ. 2011 On the growth

and form of the gut. Nature 476, 57–62.

(doi:10.1038/nature10277)

Varner VD, Nelson CM. 2014 Cellular and

physical mechanisms of branching

4.

5.

6.

morphogenesis. Development 141, 2750–2759.

(doi:10.1242/dev.104794)

Taber LA. 2014 Morphomechanics: transforming

tubes into organs. Curr. Opin. Genet. Dev. 27,

7–13. (doi:10.1016/j.gde.2014.03.004)

Johnson AB, Fogel NS, Lambert JD. 2019 Growth

and morphogenesis of the gastropod shell. Proc.

Natl Acad. Sci. USA 116, 6878–6883. (doi:10.

1073/pnas.1816089116)

Smyth DR. 2016 Helical growth in plant

organs: mechanisms and significance.

7.

8.

9.

Development 143, 3272–3282. (doi:10.1242/

dev.134064)

Žádníková P et al. 2016 A model of differential

growth-guided apical hook formation in plants.

Plant Cell 28, 2464–2477. (doi:10.1105/tpc.15.

00569)

Eskandari M, Kuhl E. 2015 Systems biology and

mechanics of growth. Wiley Interdiscip. Rev. Syst.

Biol. Med. 7, 401–412. (doi:10.1002/wsbm.1312)

Cantos R, Cole LK, Acampora D, Simeone A, Wu

DK. 2000 Patterning of the mammalian cochlea.

R. Soc. Open Sci. 8: 211024

4.3.3. Detailed setting in virtual experiments for cell cycle arrest

12

royalsocietypublishing.org/journal/rsos

from obtained images. We set the value of γ because the nuclei fully returned to the basal side according

to the cell cycle length in the simulation, which occurred only in the uncurved region of the MEL. Other

parameters were first chosen empirically and the plausibility for the numerical simulation was tested by

fitting with the experimental data on the MEL curvature. We demonstrated the similarity of the

simulated results to the experimental ones by introducing the root-mean-square error (RMSE), to

measure the differences in datasets between simulations and experiments. The RMSE at the standard

parameter set showed a minimal value and small variance. Note that relative values rather than

absolute ones are critical for the dynamics.

In the simulations, the edges of the cells at the tissue boundary were set to be free within the finite

window size, which was determined as a practical condition for the quantitative investigation. By

contrast, under experimental conditions, the boundary cells were constrained by other cells outside

the corresponding window. We were concerned that these different boundary conditions caused the

quantitative difference in the curves between experiments and simulations.

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

11.

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

24.

25.

26.

27.

28.

29.

30.

31.

32.

33.

34.

35.

36.

37.

38.

39.

40.

41.

42.

43.

44.

45.

46.

47.

48.

49.

50.

51.

EMBO J. 30, 1690–1704. (doi:10.1038/emboj.

2011.81)

Sauer FC. 1935 Mitosis in the neural tube.

J. Comp. Neurol. 62, 377–405. (doi:10.1002/cne.

900620207)

Norden C. 2017 Pseudostratified epithelia – cell

biology, diversity and roles in organ formation

at a glance. J. Cell Sci. 130, 1859–1863. (doi:10.

1242/jcs.192997)

Smith J, Schoenwolf G. 1988 Role of cell-cycle

in regulating neuroepithelial cell shape during

bending of the chick neural plate. Cell Tissue

Res. 252, 491–500. (doi:10.1007/BF00216636)

Yanakieva I, Erzberger A, Matejčić M, Modes CD,

Norden C. 2019 Cell and tissue morphology

determine actin-dependent nuclear migration

mechanisms in neuroepithelia. J. Cell Biol. 218,

3272–3289. (doi:10.1083/jcb.201901077)

Sidhaye J, Norden C. 2017 Concerted action of

neuroepithelial basal shrinkage and active

epithelial migration ensures efficient optic cup

morphogenesis. Elife 6, e22689. (doi:10.7554/

eLife.22689)

Okamoto M et al. 2013 TAG-1-assisted

progenitor elongation streamlines nuclear

migration to optimize subapical crowding. Nat.

Neurosci. 16, 1556–1566. (doi:10.1038/nn.

3525)

Wittmann T, Dema A, van Haren J. 2020 Lights,

cytoskeleton, action: optogenetic control of cell

dynamics. Curr. Opin. Cell Biol. 66, 1–10.

(doi:10.1016/j.ceb.2020.03.003)

Hüll K, Morstein J, Trauner D. 2018 In vivo

photopharmacology. Chem. Rev. 118, 10

710–10 747. (doi:10.1021/acs.chemrev.

8b00037)

Nair RV, Zhao S, Terriac E, Lautenschläger F,

Hetmanski JHR, Caswell PT, del Campo A. 2020

Possibilities and limitations of photoactivatable

cytochalasin d for the spatiotemporal regulation

of actin dynamics. ChemRxiv. (doi:10.26434/

chemrxiv.12609545.v1)

Borowiak M et al. 2015 Photoswitchable

inhibitors of microtubule dynamics optically

control mitosis and cell death. Cell 162,

403–411. (doi:10.1016/j.cell.2015.06.049)

Mumford TR, Roth L, Bugaj LJ. 2020 Reverse

and forward engineering multicellular structures

with optogenetics. Curr. Opin. Biomed. Eng. 16,

61–71. (doi:10.1016/j.cobme.2020.100250)

Cohen R, Sprinzak D. 2021 Mechanical forces

shaping the development of the inner ear.

Biophys. J. 120, 4142–4148. (doi:10.1016/j.bpj.

2021.06.036)

Riedl J et al. 2010 Lifeact mice for studying

F-actin dynamics. Nat. Methods 7, 168–169.

(doi:10.1038/nmeth0310-168)

Abe T, Kiyonari H, Shioi G, Inoue KI, Nakao K,

Aizawa S, Fujimori T. 2011 Establishment of

conditional reporter mouse lines at ROSA26

locus for live cell imaging. Genesis 49,

579–590. (doi:10.1002/dvg.20753)

Hirashima T, Adachi T. 2015 Procedures for the

quantification of whole-tissue

immunofluorescence images obtained

at single-cell resolution during murine

tubular organ development. PLoS ONE

10, e0135343. (doi:10.1371/journal.pone.

0135343)

13

R. Soc. Open Sci. 8: 211024

Downloaded from https://royalsocietypublishing.org/ on 10 October 2022

12.

23.

cystic kidney disease. Nat. Genet. 40,

1010–1015. (doi:10.1038/ng.179)

Montcouquiol M, Kelley MW. 2020 Development

and patterning of the cochlea: from convergent

extension to planar polarity. Cold Spring Harb.

Perspect. Med. 10, a033266. (doi:10.1101/

cshperspect.a033266)

Chen P, Johnson JE, Zoghbi HY, Segil N. 2002

The role of Math1 in inner ear development:

uncoupling the establishment of the sensory

primordium from hair cell fate determination.

Development 129, 2495–2505.

Yamamoto N, Okano T, Ma X, Adelstein RS,

Kelley MW. 2009 Myosin II regulates extension,

growth and patterning in the mammalian

cochlear duct. Development 136, 1977–1986.

(doi:10.1242/dev.030718)

Driver EC, Northrop A, Kelley MW. 2017 Cell

migration, intercalation and growth regulate

mammalian cochlear extension. Development

144, 3766–3776. (doi:10.1242/dev.151761)

Cohen R et al. 2020 Mechanical forces drive

ordered patterning of hair cells in the

mammalian inner ear. Nat. Commun. 11, 5137.

(doi:10.1038/s41467-020-18894-8)

Sato K, Hiraiwa T, Maekawa E, Isomura A,

Shibata T, Kuranaga E. 2015 Left-right

asymmetric cell intercalation drives directional

collective cell movement in epithelial

morphogenesis. Nat. Commun. 6, 1. (doi:10.

1038/ncomms10074)

Taniguchi K et al. 2011 Chirality in planar cell

shape contributes to left-right asymmetric

epithelial morphogenesis. Science 333,

339–341. (doi:10.1126/science.1200940)

Ishii M, Tateya T, Matsuda M, Hirashima T. 2021

Retrograde ERK activation waves drive base-toapex multicellular flow in murine cochlear duct

morphogenesis. Elife 10, e61092. (doi:10.7554/

eLife.61092)

Hino N, Rossetti L, Marín-Llauradó A, Aoki K,

Trepat X, Matsuda M, Hirashima T. 2020 ERKmediated mechanochemical waves direct

collective cell polarization. Dev. Cell 53,

646–660.e8. (doi:10.1016/j.devcel.2020.05.011)

Boocock D, Hino N, Ruzickova N, Hirashima T,

Hannezo E. 2021 Theory of mechanochemical

patterning and optimal migration in cell

monolayers. Nat. Phys. 17, 267–274. (doi:10.

1038/s41567-020-01037-7)

Meyer EJ, Ikmi A, Gibson MC. 2011 Interkinetic

nuclear migration is a broadly conserved feature of

cell division in pseudostratified epithelia. Curr. Biol.

21, 485–491. (doi:10.1016/j.cub.2011.02.002)

Grosse AS, Pressprich MF, Curley LB, Hamilton

KL, Margolis B, Hildebrand JD, Gumucio DL.

2011 Cell dynamics in fetal intestinal

epithelium: implications for intestinal growth

and morphogenesis. Development 138,

4423–4432. (doi:10.1242/dev.065789)

Norden C, Young S, Link BA, Harris WA. 2009

Actomyosin is the main driver of interkinetic

nuclear migration in the retina. Cell 138,

1195–1208. (doi:10.1016/j.cell.2009.06.032)

Kosodo Y, Suetsugu T, Suda M, Mimori-Kiyosue

Y, Toida K, Baba SA, Kimura A, Matsuzaki F.

2011 Regulation of interkinetic nuclear

migration by cell cycle-coupled active and

passive mechanisms in the developing brain.

royalsocietypublishing.org/journal/rsos

10.

Proc. Natl Acad. Sci. USA 97, 11 707–11 713.

(doi:10.1073/pnas.97.22.11707)

Bok J, Chang W, Wu DK. 2007 Patterning and

morphogenesis of the vertebrate inner ear.

Int. J. Dev. Biol. 51, 521–533. (doi:10.1387/ijdb.

072381jb)

Davis RL. 2003 Gradients of neurotrophins, ion

channels, and tuning in the cochlea.

Neuroscientist 9, 311–316. (doi:10.1177/

1073858403251986)

Bok J, Zenczak C, Hwang CH, Wu DK. 2013

Auditory ganglion source of Sonic hedgehog

regulates timing of cell cycle exit and

differentiation of mammalian cochlear hair cells.

Proc. Natl Acad. Sci. USA 110, 13 869–13 874.

(doi:10.1073/pnas.1222341110)

Liu Z, Owen T, Zhang L, Zuo J. 2010 Dynamic

expression pattern of Sonic hedgehog in

developing cochlear spiral ganglion neurons.

Dev. Dyn. 239, 1674–1683. (doi:10.1002/dvdy.

22302)

Tateya T, Imayoshi I, Tateya I, Hamaguchi K,

Torii H, Ito J, Kageyama R. 2013 Hedgehog

signaling regulates prosensory cell properties

during the basal-to-apical wave of hair cell

differentiation in the mammalian cochlea.

Development 140, 3848–3857. (doi:10.1242/

dev.095398)

Urness LD, Wang X, Doan H, Shumway N, Noyes

CA, Gutierrez-Magana E, Lu R, Mansour SL.

2018 Spatial and temporal inhibition of FGFR2b

ligands reveals continuous requirements and

novel targets in mouse inner ear

morphogenesis. Development 145, dev170142.

(doi:10.1242/dev.170142)

Urness LD, Wang X, Shibata S, Ohyama T,

Mansour SL. 2015 Fgf10 is required for

specification of non-sensory regions of the

cochlear epithelium. Dev. Biol. 400, 59–71.

(doi:10.1016/j.ydbio.2015.01.015)

Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel

K, Fritzsch B. 2003 Expression and function of

FGF10 in mammalian inner ear development.

Dev. Dyn. 227, 203–215. (doi:10.1002/dvdy.

10297)

Pirvola U, Spencer-Dene B, Xing-Qun L,

Kettunen P, Thesleff I, Fritzsch B, Dickson C,

Ylikoski J. 2000 FGF/FGFR-2(IIIb) signaling is

essential for inner ear morphogenesis.

J. Neurosci. 20, 6125–6134. (doi:10.1523/

JNEUROSCI.20-16-06125.2000)

Wang J et al. 2005 Regulation of polarized

extension and planar cell polarity in the cochlea

by the vertebrate PCP pathway. Nat. Genet. 37,

980–985. (doi:10.1038/ng1622)

Mao Y, Mulvaney J, Zakaria S, Yu T, Morgan KM,

Allen S, Basson MA, Francis-West P, Irvine KD.

2011 Characterization of a Dchs1 mutant

mouse reveals requirements for Dchs1-Fat4

signaling during mammalian development.

Development 138, 947–957. (doi:10.1242/dev.

057166)

Qian D, Jones C, Rzadzinska A, Mark S, Zhang X,

Steel KP, Dai X, Chen P. 2007 Wnt5a functions

in planar cell polarity regulation in mice. Dev.

Biol. 306, 121–133. (doi:10.1016/j.ydbio.2007.

03.011)

Saburi S et al. 2008 Loss of Fat4 disrupts PCP

signaling and oriented cell division and leads to

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

52.

56.

57.

58.

viscosity-dependent deformation during

tissue morphogenesis. Biomech. Model.

Mechanobiol. 14, 413–425. (doi:10.1007/

s10237-014-0613-5)

Hirashima T. 2021 Model for developing

cochlear duct. (doi:10.5281/zenodo.5636659)

Ishii M, Tateya T, Matsuda M, Hirashima T. 2021

Stalling interkinetic nuclear migration in curved

pseudostratified epithelium of developing

cochlea. Figshare.

14

R. Soc. Open Sci. 8: 211024

Downloaded from https://royalsocietypublishing.org/ on 10 October 2022

54.

55.

radial size in developing epithelial tubes.

Development 146, dev181206. (doi:10.1242/dev.

181206)

Mao Y, Tournier AL, Hoppe A, Kester L, Thompson

BJ, Tapon N. 2013 Differential proliferation rates

generate patterns of mechanical tension that

orient tissue growth. EMBO J. 32, 2790–2803.

(doi:10.1038/emboj.2013.197)

Okuda S, Inoue Y, Eiraku M, Adachi T, Sasai Y.

2014 Vertex dynamics simulations of

royalsocietypublishing.org/journal/rsos

53.

Fletcher AG, Osterfield M, Baker RE, Shvartsman

SY. 2014 Vertex models of epithelial

morphogenesis. Biophys. J. 106, 2291–2304.

(doi:10.1016/j.bpj.2013.11.4498)

Nagai T, Honda H. 2001 A dynamic cell model

for the formation of epithelial tissues. Phil. Mag.

B 81, 699–719. (doi:10.1080/1364281010

8205772)

Hirashima T, Adachi T. 2019 Polarized cellular

mechano-response system for maintaining

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