Understanding how topographical cues can control cell behavior is a major fundamental question which is of particular interest for implant design. Recent findings show that cell-scale curvature, as well as nanoscale topography, can affect different aspects of cell migration. However, the correlation between specific curvature radii and cell behavior, as well as the combinatorial effect of nanoscale topography and cell-scale curvature, has not yet been investigated. Herein, the authors employ a new femtosecond laser ablation method to generate multiscale topographical patterns directly on titanium surfaces. The process allows us to produce microgrooves of specific curvature imprinted with oriented nanotopographical features called Laser-Induced Periodic Surface Structures (LIPSS). The authors show that curved grooves stimulate the stem cell migration speed in comparison to flat or linear grooves. The fastest velocities are observed on 75 μm curvature radius, whereas cells migrating on 125 μm curvatures exhibit a lower speed similar to the ones migrating on straight lines. Double replicas of these grooves allow us to mask the LIPSS while keeping identical the cell-scale pattern, therefore permitting to uncouple the effect of nanoscale and microscale topographies. The authors found that the presence of nanoscale topographies improves the reading of microgrooves curvature by cells. Altogether, this work shows that the combination of specific curvatures together with nanopatterning can control the velocity of migrating stem cells and promote the use of femtosecond laser ablation in the context of surface implant design.

1.
M.
Bigerelle
,
K.
Anselme
,
B.
Noël
,
I.
Ruderman
,
P.
Hardouin
, and
A.
Iost
,
Biomaterials
23
,
1563
(
2002
).
2.
O.
Zinger
,
K.
Anselme
,
A.
Denzer
,
P.
Habersetzer
,
M.
Wieland
,
J.
Jeanfils
,
P.
Hardouin
, and
D.
Landolt
,
Biomaterials
25
,
2695
(
2004
).
3.
S.
Giljean
,
M.
Bigerelle
, and
K.
Anselme
,
Proc. Inst. Mech. Eng. B J. Eng. Manuf.
221
,
1407
(
2007
).
4.
M.
Bigerelle
,
S.
Giljean
, and
K.
Anselme
,
Acta Biomater.
7
,
3302
(
2011
).
5.
B.
Dusser
,
Z.
Sagan
,
H.
Soder
,
N.
Faure
,
J. P.
Colombier
,
M.
Jourlin
, and
E.
Audouard
,
Opt. Express
18
,
2913
(
2010
).
6.
P.
Bizi-Bandoki
,
S.
Benayoun
,
S.
Valette
,
B.
Beaugiraud
, and
E.
Audouard
,
Appl. Surf. Sci.
257
,
5213
(
2011
).
7.
K. M. T.
Ahmmed
,
C.
Grambow
, and
A. M.
Kietzig
,
Micromachines
5
,
1219
(
2014
).
8.
J. L.
Calvo-Guirado
 et al,
J. Osseointegr.
5
,
39
(
2013
).
9.
V.
Dumas
,
A.
Rattner
,
L.
Vico
,
E.
Audouard
,
J. C.
Dumas
,
P.
Naisson
, and
P.
Bertrand
,
J. Biomed. Mater. Res. A
100
,
3108
(
2012
).
10.
V.
Dumas
 et al,
Biomed. Mater.
10
,
055002
(
2015
).
11.
O.
Raimbault
,
S.
Benayoun
,
K.
Anselme
,
C.
Mauclair
,
T.
Bourgade
,
A. M.
Kietzig
,
P. L.
Girard-Lauriault
,
S.
Valette
, and
C.
Donnet
,
Mater. Sci. Eng. C Mater. Biol. Appl.
69
,
311
(
2016
).
12.
A. I.
Teixeira
,
G. A.
Abrams
,
P. J.
Bertics
,
C. J.
Murphy
, and
P. F.
Nealey
,
J. Cell Sci.
116
,
1881
(
2003
).
13.
S. H.
Yoon
,
Y. K.
Kim
,
E. D.
Han
,
Y. H.
Seo
,
B. H.
Kim
, and
M. R.
Mofrad
,
Lab Chip
12
,
2391
(
2012
).
14.
X.
Sun
,
M. K.
Driscoll
,
C.
Guven
,
S.
Das
,
C. A.
Parent
,
J. T.
Fourkas
, and
W.
Losert
,
Proc. Natl. Acad. Sci. U.S.A.
112
,
12557
(
2015
).
15.
Q.
Zhou
,
P. T.
Kuhn
,
T.
Huisman
,
E.
Nieboer
,
Z. C.
van
,
T. G.
van Kooten
, and
R. P.
van
,
Sci. Rep.
5
,
16240
(
2015
).
16.
W. G.
Bae
,
J.
Kim
,
Y. H.
Choung
,
Y.
Chung
,
K. Y.
Suh
,
C.
Pang
,
J. H.
Chung
, and
H. E.
Jeong
,
Biomaterials
69
,
158
(
2015
).
17.
F.
Pouthas
,
P.
Girard
,
V.
Lecaudey
,
T. B.
Ly
,
D.
Gilmour
,
C.
Boulin
,
R.
Pepperkok
, and
E. G.
Reynaud
,
J. Cell Sci.
121
,
2406
(
2008
).
18.
A. D.
Doyle
,
F. W.
Wang
,
K.
Matsumoto
, and
K. M.
Yamada
,
J. Cell Biol.
184
,
481
(
2009
).
19.
P.
Maiuri
 et al,
Curr. Biol.
22
,
R673
(
2012
).
20.
G.
Kumar
,
C. C.
Ho
, and
C. C.
Co
,
Adv. Mater.
19
,
1084
(
2007
).
21.
G.
Mahmud
,
C. J.
Campbell
,
K. J. M.
Bishop
,
Y. A.
Komarova
,
O.
Chaga
,
S.
Soh
,
S.
Huda
,
K.
Kandere-Grzybowska
, and
B. A.
Grzybowski
,
Nat. Phys.
5
,
606
(
2009
).
22.
K.
Kushiro
and
A. R.
Asthagiri
,
Langmuir
28
,
4357
(
2012
).
23.
D.
Caballero
,
J.
Comelles
,
M.
Piel
,
R.
Voituriez
, and
D.
Riveline
,
Trends Cell Biol.
25
,
815
(
2015
).
24.
D. H.
Kim
,
K.
Han
,
K.
Gupta
,
K. W.
Kwon
,
K. Y.
Suh
, and
A.
Levchenko
,
Biomaterials
30
,
5433
(
2009
).
25.
D. H.
Kim
,
C. H.
Seo
,
K.
Han
,
K. W.
Kwon
,
A.
Levchenko
, and
K. Y.
Suh
,
Adv. Funct. Mater.
19
,
1579
(
2009
).
26.
Y. G.
Ko
,
C. C.
Co
, and
C. C.
Ho
,
Soft Matter
9
,
2467
(
2013
).
27.
Y. G.
Ko
,
C. C.
Co
, and
C. C.
Ho
,
Biomaterials
34
,
353
(
2013
).
28.
Y. A.
Rovensky
and
V. I.
Samoilov
,
J. Cell Sci.
107
,
1255
(
1994
).
29.
S.
Meehan
and
A. S.
Nain
,
Biophys. J.
107
,
2604
(
2014
).
30.
J. Y.
Park
,
D. H.
Lee
,
E. J.
Lee
, and
S. H.
Lee
,
Lab Chip
9
,
2043
(
2009
).
31.
M.
Werner
,
S. B.
Blanquer
,
S. P.
Haimi
,
G.
Korus
,
J. W.
Dunlop
,
G. N.
Duda
,
D. W.
Grijpma
, and
A.
Petersen
,
Adv. Sci.
4
,
1600347
(
2017
).
32.
M. C.
Kim
,
C.
Kim
,
L.
Wood
,
D.
Neal
,
R. D.
Kamm
, and
H. H.
Asada
,
Integr. Biol.
4
,
1386
(
2012
).
33.
X.
He
and
Y.
Jiang
,
Phys. Biol.
14
,
035006
(
2017
).
34.
L.
Pieuchot
 et al,
Nat. Commun.
9
,
3995
(
2018
).
35.
P.
Bajaj
,
B.
Reddy
, Jr.
,
L.
Millet
,
C.
Wei
,
P.
Zorlutuna
,
G.
Bao
, and
R.
Bashir
,
Integr. Biol.
3
,
897
(
2011
).
36.
L. Q.
Wan
,
K.
Ronaldson
,
M.
Park
,
G.
Taylor
,
Y.
Zhang
,
J. M.
Gimble
, and
G.
Vunjak-Novakovic
,
Proc. Natl. Acad. Sci. U.S.A.
108
,
12295
(
2011
).
37.
C. G.
Rolli
,
H.
Nakayama
,
K.
Yamaguchi
,
J. P.
Spatz
,
R.
Kemkemer
, and
J.
Nakanishi
,
Biomaterials
33
,
2409
(
2012
).
38.
C.
Schreiber
,
F. J.
Segerer
,
E.
Wagner
,
A.
Roidl
, and
J. O.
Radler
,
Sci. Rep.
6
,
26858
(
2016
).
39.
J.
Xu
 et al,
Biochem. Biophys. Res. Commun.
415
,
591
(
2011
).
40.
K.
Wang
,
L.
Cai
,
L.
Zhang
,
J. Y.
Dong
, and
S. F.
Wang
,
Adv. Health Mater.
1
,
292
(
2012
).
41.
W.
Du
,
J.
Chen
,
H.
Li
,
G.
Zhao
,
G.
Liu
,
W.
Zhu
,
D.
Wu
, and
J.
Chu
,
J. Mater. Chem. B
4
,
3398
(
2016
).
42.
A.
Tropmann
,
L.
Tanguy
,
P.
Koltay
,
R.
Zengerle
, and
L.
Riegger
,
Langmuir
28
,
8292
(
2012
).
43.
M. E.
Ngandu
,
M.
Cantini
,
P. M.
Reynolds
,
N.
Gadegaard
,
M. J.
Dalby
, and
M.
Salmeron-Sanchez
,
ACS Nano
10
,
6638
(
2016
).
44.
J.
Schindelin
 et al,
Nat. Methods
9
,
676
(
2012
).
45.
B.
Efron
and
R.
Tibshirani
, An Introduction to the Bootstrap (
Chapman and Hall
,
New York
,
1993
).
46.
D.
Najjar
,
M.
Bigerelle
, and
A.
Iost
,
Wear
254
,
450
(
2003
).
47.
K.
Anselme
and
M.
Bigerelle
,
Biomaterials
27
,
1187
(
2006
).
48.
P.
Bizi-Bandoki
,
S.
Valette
,
E.
Audouard
, and
S.
Benayoun
,
Appl. Surf. Sci.
270
,
197
(
2013
).
49.
H. M.
van Driel
,
J. E.
Sipe
, and
J. F.
Young
,
Phys. Rev. Lett.
49
,
1955
(
1982
).
50.
Q. Y.
Tang
,
W. X.
Qian
,
Y. H.
Xu
,
S.
Gopalakrishnan
,
J. Q.
Wang
,
Y. W.
Lam
, and
S. W.
Pang
,
J. Biomed. Mater. Res. A
103
,
2383
(
2015
).
51.
See supplementary material at https://doi.org/10.1116/1.5042747E-BJIOBN-13-331806for the topographical analysis of nanotextures and microtextures on Ti6Al4V substrates (Fig. S1) and PDMS replicates (Fig. S2).

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