The aims of this short tutorial are fourfold: 1) to introduce readers unfamiliar with the field to major concepts in the field; 2) to inform the reader of major unresolved questions; 3) to inform readers of a few major sources of relevant literature; and 4) to place the subject in relation to its relevance to other areas of science and practical application

Curtis, A.S.G.

English

Enlighten

      Curtis, A.S.G. (2004) Tutorial on the biology of nanotopography. IEEE Transactions on NanoBioscience 3(4):pp. 293-295.        http://eprints.gla.ac.uk/3888/  Deposited on: 11 February 2008   Glasgow ePrints Service http://eprints.gla.ac.uk IEEE TRANSACTIONS ON NANOBIOSCIENCE, VOL. 3, NO. 4, DECEMBER 2004 293Tutorial on the Biology of NanotopographyAdam CurtisTutorial PaperAbstract—The aims of this short tutorial are fourfold: 1) to in-troduce readers unfamiliar with the field to major concepts in thefield; 2) to inform the reader of major unresolved questions; 3) toinform readers of a few major sources of relevant literature; and4) to place the subject in relation to its relevance to other areas ofscience and practical application.Index Terms—Adhesion, biological reactions, cell surface, nan-otopography, order, physical form of nanotopography, symmetry.I. NANOFEATURES: THEIR OCCURRENCE INBIOLOGICAL SYSTEMSREFERENCE TO any good textbook of cell biology [1]will show that the organelles of cells are usually on thenanoscale. Even the surfaces of cells often carry fine processes(microspikes, filopodia, fimbriae, etc.) protruding from thecell on this nanoscale. The surface of cells and the internalorganelles is covered with a mosaic of molecules of many dif-ferent sorts, which may be arranged into more segregated areassuch as domains or rafts, also on the nanoscale. Much of thematerial between cells in multicellular organisms is organizedinto fibrils, etc., on the nanoscale. Both nanotopography andnanopatterned chemistry are encountered by cells, and they ofcourse in turn present their own features of these two types toother cells. These interactions are mainly, and certainly initially,between the two surfaces, namely, that of the cell and that ofthe nanofeatured material.If the nanofeatured material is mechanically weak or ispresent as nano- or microparticles, such material may be takeninto the cell later by the processes of endocytosis (phago-cytosis); see [1] for definitions. This initial surface–surfaceinteraction determines the further progress of any reactionbecause if adhesion fails to take place, there are no subsequentevents. Adhesion which is sufficient to elicit a reaction maybe, however, transitory, and we do not know in most cases howshort an interaction has to be to produce no effect.The nonliving surfaces that cells encounter, such as prostheticdevices in the body or parts of process plants, usually bearnanotopographic features if only because of their methods ofmanufacture. Molecularly smooth surface are very difficult tomake.The prime question is whether these nanofeatures are ofimportance in the lives of the cells and whether they could beManuscript received September 10, 2004; revised September 17, 2004.The author is with the Centre for Cell Engineering, University of Glasgow,Glasgow G12 8QQ, U.K. (e-mail: A.Curtis@bio.gla.ac.uk).Digital Object Identifier 10.1109/TNB.2004.837898manipulated to yield results valuable in the treatment of diseaseor injury or in improving biotechnology. I am not providinganswers to this because this is what current research is trying toelucidate.A. Are There Nanoscale Interactions in Biological Systems?This almost seems like an unnecessary question, because inprinciple there must be; but the next level of question is verynecessary. Just what nanoscale interactions are involved in anyparticular system?One simple way to classify such interactions are those thatrely on repeated structures extending over a few to manymolecules where the repetition and order contribute to the inter-action and those that depend upon the properties of individualmolecules where the relationship of one molecule to anotherplays little or no role. This distinction may mark the boundarybetween nanoscience and molecular biology for some people.For example, I and my colleagues [2] have suggested thatthe adhesion of cells to nanotopography may be controlled toa considerable extent by the regularity and type of order aswell as scale of nanofeatures the cells encounter. On the otherhand [3], specific molecules apparently in a random or chaoticarrangement such as fibronectin may stimulate cell adhesion.The importance of topography has also been emphasized byothers working in this field [4]–[6]. One interpretation of thistype of reaction to nanotopography occurs because there aresmall differences in chemistry between one part of the topog-raphy and another, An opposite view is that even when smalllocal differences in chemistry are made by techniques such asnanoprinting, there is also a small difference in topography.Printing or coating a surface minimally leaves a step of theheight of a monolayer of the material, and in practice there isoften edge accumulation of the added material so that a step ofseveral nanometers may develop.B. Features of Initial Interactions of CellsWith NanotopographyThe first interactions are the formation of adhesions or thefailure of adhesion on contact between cell and nanofeaturesin situations where both surfaces could form adhesions if theywere flat or of different topography [2]. Regularly spaced pitsor pillars of appropriate dimensions tend to reduce adhesion;steps and grooves of nanometric height or depth and extendedlength may raise adhesion [7]. The step effect often leads to cellsaccumulating and aligning along the steps.1536-1241/04$20.00 © 2004 IEEE294 IEEE TRANSACTIONS ON NANOBIOSCIENCE, VOL. 3, NO. 4, DECEMBER 2004C. Size and Shape Features of NanotopographyThough much research remains to be done and many possiblefeatures have not been examined, the following appears to betrue.1) Responses both quantitatively and qualitatively vary fromcell type to cell type for any one nanofeatures, Statementsthat some particular topography has no effect cannot bemade with confidence until a very wide range of differentdimensions has been examined. For example, epitenoncells do not react to 30-nm-wide pits, but blood plateletsdo, while epitenon cells react to 40- and 80-nm-deep pits.2) Shape of the nanofeatures is important; see [8].3) Order and symmetry. There is evidence that order andsymmetry of any nanotopography can affect cell reactions[2], [7], [9].4) Area of features. Little work has been done on this, butthere are suggestions that nanotopographic features mustbe continued linearly over at least 2000 nm to have effects.5) Further work in this area should be of value both forobtaining a better understanding of the underlying mech-anisms and for discovering commercial potentials ofnanotopography.D. How Can We Decide Between Chemical Effects andPhysical Effects of Topography?Until nanoscale mapping of individual molecules becomespossible, we can only make somewhat indirect attempts atanswering this question. If the same type of nanotopographicfeature made in a variety of different materials has the samebiological effects this makes chemical explanations unlikely,since it is improbable that surface chemistry of different mate-rials with different surface chemistry and differing adsorptionof extraneous molecules would be the same. In addition, similarresults are obtained for the same type of structure in a variety ofmedia. Nanopitted surfaces derivatized with the carbovyl-richsurface of polyacrylic acid have low adhesion for a varietyof cell types of similar value to those obtained in the controlpolycarbonate surfaces. Derivatization with polylysine, whichprovides a basic amine-rich surface, does raise adhesion, buteffects of nanofeatures are still detectable.E. Cell Functions Believed to Be Affected byExternal NanofeatureThese include:• adhesion [2];• cell morphology [10];• cytoskeletal arrangement [11];• surface antigen display [12];• gene display [12];• proliferation [13].F. FabricationIt is very important to appreciate how any nanodevice is madeand to what accuracy when biological uses and investigationsare planned. The reason for this is that cells are very sensitive tonanofeatures. For example, [14] it was found that neurons wouldreact to a 5-nm-deep groove. Randomly displayed nanotopog-raphy has little or no effect on cells [2] with results comparablewith very smooth surfaces. But polished surfaces usually havelinear nanotopography up to 100 nm deep, and the exact methodof surface treatment may have a large effect. Bright polishedmetals are usually nanoscratched.Many different methods of nanofabrication are available, butelectron beam lithography followed by dry etching and replica-tion, colloidal lithography, and nanoprinting are all appropriatemethods for making materials for this area of nanotechnology(see, e.g., [15] and [16]). Polymer demixing has also been usedto produce nanofeatured surfaces [7].G. Mechanisms of Response—Speculation and HypothesisThis subject is so young that little has been established withany certainty. However, this also means that there is much op-portunity for research.The results on shape, size, and type of packing of nanotopog-raphy on cell interactions suggest that the cells may be able tomeasure distances or at least relative distances on such surfaces.This would account for the different results with hexagonaland with orthogonal packing [2]. Possible mechanisms for thiscould be: 1) stretch receptors in the plasmalemma, in partic-ular, the three state receptors described for chloride channels[17]) which might allow axis comparisons; 2) effects onthe cell nucleus and chromosome packing [18]; 3) differencesand gradients in surface energy (hydrophobicity/hydrophilicity)resulting from the topography; and 4) differences in proteinadsorption due to differences and gradients in surface energy.H. ApplicationsThe literature (see above) shows that many cell processes canbe affected by the precise nanotopography of the local environ-ment of the cell in ways specific to the order, shape, and scaleof the nanofeatures. All these effects seem to result from theinitial adhesion (or not) of the cells. Materials—in particular,polymers—can be used to make surfaces that can be broughtinto contact with cells to produce desired biological effects. Forexample, low-adhesion surfaces could be put on stents for vas-cular use or on biodegradable membranes designed to preventunwanted tissue adhesion.REFERENCES[1] B. Alberts, Molecular Biology of the Cell. New York: Garland, 2002.[2] A. S. G. Curtis, N. Gadegaard, M. J. Dalby, M. O. Riehle, C. D. W.Wilkinson, and G. Aitchison, “Cells react to nanoscale order and sym-metry in their surroundings,” IEEE Trans. Nanobiosci., vol. 3, pp. 61–65,Mar. 2004.[3] W. D. Norris, J. G. Steele, G. Johnson, and P. A. Underwood, “Serumenhancement of human endothelial cell attachment to and spreading oncollagens I and IV does not require serum fibronectin or vitronectin,” J.Cell Sci., vol. 95, pp. 255–262, 1990.[4] R. G. Flemming, C. J. Murphy, G. A. Abrams, S. L. Goodman, and P.F. Nealey, “Effects of synthetic micro- and nano-structured surfaces oncell behavior,” Biomaterials, vol. 20, pp. 573–5688, 1999.[5] A. I. Teixeira, G. A. Abrams, P. J. Bertics, C. J. Murphy, and P. F. Nealey,“Epithelial contact guidance on well-defined micro- and nanostructuredsubstrates,” J. Cell Sci., vol. 116, pp. 1881–1892, 2003.[6] S. Turner, L. Kam, M. Isaacson, H. G. Craighead, W. Shain, and J.Turner, “Cell attachment on silicon nanostructure,” J. Vac. Sci. Technol.B, vol. 15, pp. 2848–2854, 1997.CURTIS: TUTORIAL ON THE BIOLOGY OF NANOTOPOGRAPHY 295[7] A. S. G. Curtis, B. Casey, J. D. Gallagher, D. Pasqui, M. A. W. Wood,and C. D. W. Wilkinson, “Substratum nanotopography and the adhesionof biological cells. Are symmetry or regularity of nanotopography im-portant?,” Biophys. Chem., vol. 94, pp. 275–283, 2001.[8] A.-S. Andersson, F. Blasckhed, A. von Euler, A. Richter-Dahlfors, D.Sutherland, and B. Kasemo, “Nanoscale features influence epithelialcell morphology and cytokine production,” Biomaterials, vol. 24, pp.3427–3436, 2000.[9] J. O. Gallagher, K. F. McGhee, C. D. W. Wilkinson, and M. O. Riehle,“Interaction of animal cells with ordered nanotopography,” IEEE Trans.Nanobiosci., vol. 1, pp. 24–28, Mar. 2003.[10] M. J. Dalby, M. O. Riehle, H. Johnstone, S. Affrossman, and A. S. G.Curtis, “In vitro reaction of endothelial cells to polymer demixed nan-otopography,” Biomaterials, vol. 23, pp. 2945–2954, 2002.[11] M. J. Dalby, S. Childs, M. O. Riehle, and H. J. H. Johnstone, “Fibroblastreaction to island topography: Changes in cytoskeleton and morphologywith time,” Biomaterials, vol. 24, pp. 927–935, 2002.[12] M. J. Dalby, S. J. Yarwood, H. H. Johnstone, S. Affrossman, and M.Riehle, “Fibroblast signaling events in response to nanotopography: Agene array study,” IEEE Trans Nanobiosci., vol. 1, pp. 12–17, Mar. 2002.[13] M. J. Dalby, M. O. Riehle, H. J. H. Johnstone, S. Affrossman, and A.S. G. Curtis, “Polymer-demixed nanotopography: Control of fibroblastspreading and proliferation,” Tissue Eng., vol. 8, pp. 1099–1107, 2002.[14] A. M. Rajnicek, S. Britland, and C. D. McCaig, “Contact guidance ofCNS neurites on grooved quartz: Influence of groove dimensions, neu-ronal age and cell type,” J. Cell Sci., vol. 110, pp. 2905–2913, 1997.[15] C. D. W. Wilkinson and A. S. G. Curtis, “Nanofabrication and its appli-cations in medicine and biology,” Dev. Nanotechnol., vol. 3, pp. 19–31,1996.[16] P. Hanarp, D. Sutherland, J. Gold, and B. Kasemo, “Nanostructuredmodel biomaterial surfaces prepared by colloidal lithography,” Nanos-truct. Mater., vol. 12, pp. 429–432, 1999.[17] U. Ludewig, M. Pusch, and T. J. Jentsch, “Two physically distinct poresin the dimeric CIC-O chloride channel,” Nature, vol. 383, pp. 340–343,1996.[18] A. R. Leitch, T. Schwarzacher, W. Mosgoller, M. D. Bennett, and J.S. Heslop-Harrison, “Parental genomes are separated throughout thecell-cycle in a plant hybrid,” Chromosoma, vol. 101, pp. 206–213,1991.[19] M. J. Dalby, M. O. Riehle, D. S. Sutherland, H. Agheli, and A. S. G.Curtis, “Use of nanotopography to study mechanotransduction in fi-broblasts—Methods and perspectives,” Eur. J. Cell Biol., vol. 83, pp.159–169, 2004.Adam Curtis, photograph and biography not available at the time ofpublication.

Cell attachment on silicon nanostructure,”

Cells react to nanoscale order and symmetryintheirsurroundings,”IEEETrans.Nanobiosci.,vol.3,pp.61–65,

Contact guidance of CNS neurites on grooved quartz: Inﬂuence of groove dimensions, neuronal age and cell type,”

Effects of synthetic micro- and nano-structured surfaces on cell behavior,”

Epithelial contact guidance on well-deﬁned micro- and nanostructured substrates,”

Fibroblast reaction to island topography: Changes in cytoskeleton and morphology with time,”

Fibroblast signaling events in response to nanotopography: A genearraystudy,”IEEETransNanobiosci.,vol.1,pp.12–17,Mar.2002.

In vitro reaction of endothelial cells to polymer demixed nanotopography,”

Interaction of animal cells with ordered nanotopography,”

Molecular Biology of the Cell.

Nanofabrication and its applications in medicine and biology,”

Nanoscale features inﬂuence epithelial cell morphology and cytokine production,”

Nanostructured model biomaterial surfaces prepared by colloidal lithography,”

Parental genomes are separated throughout the cell-cycle in a plant hybrid,”

Polymer-demixed nanotopography: Control of ﬁbroblast spreading and proliferation,”

Serum enhancement of human endothelial cell attachment to and spreading on collagens I and IV does not require serum ﬁbronectin or vitronectin,”

Substratum nanotopography and the adhesion of biological cells. Are symmetry or regularity of nanotopography important?,”

Two physically distinct pores in the dimeric CIC-O chloride channel,”

Use of nanotopography to study mechanotransduction in ﬁ-broblasts—Methods and perspectives,”

Tutorial on the biology of nanotopography

Enlighten: Publications

 
 
 
 
 
 
Curtis, A.S.G. (2004) Tutorial on the biology of nanotopography. IEEE 
Transactions on NanoBioscience 3(4):pp. 293-295. 
 
 
 
 
 
 
 
http://eprints.gla.ac.uk/3888/ 
 
Deposited on: 11 February 2008 
 
 
Glasgow ePrints Service 
http://eprints.gla.ac.uk 
IEEE TRANSACTIONS ON NANOBIOSCIENCE, VOL. 3, NO. 4, DECEMBER 2004 293
Tutorial on the Biology of Nanotopography
Adam Curtis
Tutorial Paper
Abstract—The aims of this short tutorial are fourfold: 1) to in-
troduce readers unfamiliar with the field to major concepts in the
field; 2) to inform the reader of major unresolved questions; 3) to
inform readers of a few major sources of relevant literature; and
4) to place the subject in relation to its relevance to other areas of
science and practical application.
Index Terms—Adhesion, biological reactions, cell surface, nan-
otopography, order, physical form of nanotopography, symmetry.
I. NANOFEATURES: THEIR OCCURRENCE IN
BIOLOGICAL SYSTEMS
REFERENCE TO any good textbook of cell biology [1]will show that the organelles of cells are usually on the
nanoscale. Even the surfaces of cells often carry fine processes
(microspikes, filopodia, fimbriae, etc.) protruding from the
cell on this nanoscale. The surface of cells and the internal
organelles is covered with a mosaic of molecules of many dif-
ferent sorts, which may be arranged into more segregated areas
such as domains or rafts, also on the nanoscale. Much of the
material between cells in multicellular organisms is organized
into fibrils, etc., on the nanoscale. Both nanotopography and
nanopatterned chemistry are encountered by cells, and they of
course in turn present their own features of these two types to
other cells. These interactions are mainly, and certainly initially,
between the two surfaces, namely, that of the cell and that of
the nanofeatured material.
If the nanofeatured material is mechanically weak or is
present as nano- or microparticles, such material may be taken
into the cell later by the processes of endocytosis (phago-
cytosis); see [1] for definitions. This initial surface–surface
interaction determines the further progress of any reaction
because if adhesion fails to take place, there are no subsequent
events. Adhesion which is sufficient to elicit a reaction may
be, however, transitory, and we do not know in most cases how
short an interaction has to be to produce no effect.
The nonliving surfaces that cells encounter, such as prosthetic
devices in the body or parts of process plants, usually bear
nanotopographic features if only because of their methods of
manufacture. Molecularly smooth surface are very difficult to
make.
The prime question is whether these nanofeatures are of
importance in the lives of the cells and whether they could be
Manuscript received September 10, 2004; revised September 17, 2004.
The author is with the Centre for Cell Engineering, University of Glasgow,
Glasgow G12 8QQ, U.K. (e-mail: A.Curtis@bio.gla.ac.uk).
Digital Object Identifier 10.1109/TNB.2004.837898
manipulated to yield results valuable in the treatment of disease
or injury or in improving biotechnology. I am not providing
answers to this because this is what current research is trying to
elucidate.
A. Are There Nanoscale Interactions in Biological Systems?
This almost seems like an unnecessary question, because in
principle there must be; but the next level of question is very
necessary. Just what nanoscale interactions are involved in any
particular system?
One simple way to classify such interactions are those that
rely on repeated structures extending over a few to many
molecules where the repetition and order contribute to the inter-
action and those that depend upon the properties of individual
molecules where the relationship of one molecule to another
plays little or no role. This distinction may mark the boundary
between nanoscience and molecular biology for some people.
For example, I and my colleagues [2] have suggested that
the adhesion of cells to nanotopography may be controlled to
a considerable extent by the regularity and type of order as
well as scale of nanofeatures the cells encounter. On the other
hand [3], specific molecules apparently in a random or chaotic
arrangement such as fibronectin may stimulate cell adhesion.
The importance of topography has also been emphasized by
others working in this field [4]–[6]. One interpretation of this
type of reaction to nanotopography occurs because there are
small differences in chemistry between one part of the topog-
raphy and another, An opposite view is that even when small
local differences in chemistry are made by techniques such as
nanoprinting, there is also a small difference in topography.
Printing or coating a surface minimally leaves a step of the
height of a monolayer of the material, and in practice there is
often edge accumulation of the added material so that a step of
several nanometers may develop.
B. Features of Initial Interactions of Cells
With Nanotopography
The first interactions are the formation of adhesions or the
failure of adhesion on contact between cell and nanofeatures
in situations where both surfaces could form adhesions if they
were flat or of different topography [2]. Regularly spaced pits
or pillars of appropriate dimensions tend to reduce adhesion;
steps and grooves of nanometric height or depth and extended
length may raise adhesion [7]. The step effect often leads to cells
accumulating and aligning along the steps.
1536-1241/04$20.00 © 2004 IEEE
294 IEEE TRANSACTIONS ON NANOBIOSCIENCE, VOL. 3, NO. 4, DECEMBER 2004
C. Size and Shape Features of Nanotopography
Though much research remains to be done and many possible
features have not been examined, the following appears to be
true.
1) Responses both quantitatively and qualitatively vary from
cell type to cell type for any one nanofeatures, Statements
that some particular topography has no effect cannot be
made with confidence until a very wide range of different
dimensions has been examined. For example, epitenon
cells do not react to 30-nm-wide pits, but blood platelets
do, while epitenon cells react to 40- and 80-nm-deep pits.
2) Shape of the nanofeatures is important; see [8].
3) Order and symmetry. There is evidence that order and
symmetry of any nanotopography can affect cell reactions
[2], [7], [9].
4) Area of features. Little work has been done on this, but
there are suggestions that nanotopographic features must
be continued linearly over at least 2000 nm to have effects.
5) Further work in this area should be of value both for
obtaining a better understanding of the underlying mech-
anisms and for discovering commercial potentials of
nanotopography.
D. How Can We Decide Between Chemical Effects and
Physical Effects of Topography?
Until nanoscale mapping of individual molecules becomes
possible, we can only make somewhat indirect attempts at
answering this question. If the same type of nanotopographic
feature made in a variety of different materials has the same
biological effects this makes chemical explanations unlikely,
since it is improbable that surface chemistry of different mate-
rials with different surface chemistry and differing adsorption
of extraneous molecules would be the same. In addition, similar
results are obtained for the same type of structure in a variety of
media. Nanopitted surfaces derivatized with the carbovyl-rich
surface of polyacrylic acid have low adhesion for a variety
of cell types of similar value to those obtained in the control
polycarbonate surfaces. Derivatization with polylysine, which
provides a basic amine-rich surface, does raise adhesion, but
effects of nanofeatures are still detectable.
E. Cell Functions Believed to Be Affected by
External Nanofeature
These include:
• adhesion [2];
• cell morphology [10];
• cytoskeletal arrangement [11];
• surface antigen display [12];
• gene display [12];
• proliferation [13].
F. Fabrication
It is very important to appreciate how any nanodevice is made
and to what accuracy when biological uses and investigations
are planned. The reason for this is that cells are very sensitive to
nanofeatures. For example, [14] it was found that neurons would
react to a 5-nm-deep groove. Randomly displayed nanotopog-
raphy has little or no effect on cells [2] with results comparable
with very smooth surfaces. But polished surfaces usually have
linear nanotopography up to 100 nm deep, and the exact method
of surface treatment may have a large effect. Bright polished
metals are usually nanoscratched.
Many different methods of nanofabrication are available, but
electron beam lithography followed by dry etching and replica-
tion, colloidal lithography, and nanoprinting are all appropriate
methods for making materials for this area of nanotechnology
(see, e.g., [15] and [16]). Polymer demixing has also been used
to produce nanofeatured surfaces [7].
G. Mechanisms of Response—Speculation and Hypothesis
This subject is so young that little has been established with
any certainty. However, this also means that there is much op-
portunity for research.
The results on shape, size, and type of packing of nanotopog-
raphy on cell interactions suggest that the cells may be able to
measure distances or at least relative distances on such surfaces.
This would account for the different results with hexagonal
and with orthogonal packing [2]. Possible mechanisms for this
could be: 1) stretch receptors in the plasmalemma, in partic-
ular, the three state receptors described for chloride channels
[17]) which might allow axis comparisons; 2) effects on
the cell nucleus and chromosome packing [18]; 3) differences
and gradients in surface energy (hydrophobicity/hydrophilicity)
resulting from the topography; and 4) differences in protein
adsorption due to differences and gradients in surface energy.
H. Applications
The literature (see above) shows that many cell processes can
be affected by the precise nanotopography of the local environ-
ment of the cell in ways specific to the order, shape, and scale
of the nanofeatures. All these effects seem to result from the
initial adhesion (or not) of the cells. Materials—in particular,
polymers—can be used to make surfaces that can be brought
into contact with cells to produce desired biological effects. For
example, low-adhesion surfaces could be put on stents for vas-
cular use or on biodegradable membranes designed to prevent
unwanted tissue adhesion.
REFERENCES
[1] B. Alberts, Molecular Biology of the Cell. New York: Garland, 2002.
[2] A. S. G. Curtis, N. Gadegaard, M. J. Dalby, M. O. Riehle, C. D. W.
Wilkinson, and G. Aitchison, “Cells react to nanoscale order and sym-
metry in their surroundings,” IEEE Trans. Nanobiosci., vol. 3, pp. 61–65,
Mar. 2004.
[3] W. D. Norris, J. G. Steele, G. Johnson, and P. A. Underwood, “Serum
enhancement of human endothelial cell attachment to and spreading on
collagens I and IV does not require serum fibronectin or vitronectin,” J.
Cell Sci., vol. 95, pp. 255–262, 1990.
[4] R. G. Flemming, C. J. Murphy, G. A. Abrams, S. L. Goodman, and P.
F. Nealey, “Effects of synthetic micro- and nano-structured surfaces on
cell behavior,” Biomaterials, vol. 20, pp. 573–5688, 1999.
[5] A. I. Teixeira, G. A. Abrams, P. J. Bertics, C. J. Murphy, and P. F. Nealey,
“Epithelial contact guidance on well-defined micro- and nanostructured
substrates,” J. Cell Sci., vol. 116, pp. 1881–1892, 2003.
[6] S. Turner, L. Kam, M. Isaacson, H. G. Craighead, W. Shain, and J.
Turner, “Cell attachment on silicon nanostructure,” J. Vac. Sci. Technol.
B, vol. 15, pp. 2848–2854, 1997.
CURTIS: TUTORIAL ON THE BIOLOGY OF NANOTOPOGRAPHY 295
[7] A. S. G. Curtis, B. Casey, J. D. Gallagher, D. Pasqui, M. A. W. Wood,
and C. D. W. Wilkinson, “Substratum nanotopography and the adhesion
of biological cells. Are symmetry or regularity of nanotopography im-
portant?,” Biophys. Chem., vol. 94, pp. 275–283, 2001.
[8] A.-S. Andersson, F. Blasckhed, A. von Euler, A. Richter-Dahlfors, D.
Sutherland, and B. Kasemo, “Nanoscale features influence epithelial
cell morphology and cytokine production,” Biomaterials, vol. 24, pp.
3427–3436, 2000.
[9] J. O. Gallagher, K. F. McGhee, C. D. W. Wilkinson, and M. O. Riehle,
“Interaction of animal cells with ordered nanotopography,” IEEE Trans.
Nanobiosci., vol. 1, pp. 24–28, Mar. 2003.
[10] M. J. Dalby, M. O. Riehle, H. Johnstone, S. Affrossman, and A. S. G.
Curtis, “In vitro reaction of endothelial cells to polymer demixed nan-
otopography,” Biomaterials, vol. 23, pp. 2945–2954, 2002.
[11] M. J. Dalby, S. Childs, M. O. Riehle, and H. J. H. Johnstone, “Fibroblast
reaction to island topography: Changes in cytoskeleton and morphology
with time,” Biomaterials, vol. 24, pp. 927–935, 2002.
[12] M. J. Dalby, S. J. Yarwood, H. H. Johnstone, S. Affrossman, and M.
Riehle, “Fibroblast signaling events in response to nanotopography: A
gene array study,” IEEE Trans Nanobiosci., vol. 1, pp. 12–17, Mar. 2002.
[13] M. J. Dalby, M. O. Riehle, H. J. H. Johnstone, S. Affrossman, and A.
S. G. Curtis, “Polymer-demixed nanotopography: Control of fibroblast
spreading and proliferation,” Tissue Eng., vol. 8, pp. 1099–1107, 2002.
[14] A. M. Rajnicek, S. Britland, and C. D. McCaig, “Contact guidance of
CNS neurites on grooved quartz: Influence of groove dimensions, neu-
ronal age and cell type,” J. Cell Sci., vol. 110, pp. 2905–2913, 1997.
[15] C. D. W. Wilkinson and A. S. G. Curtis, “Nanofabrication and its appli-
cations in medicine and biology,” Dev. Nanotechnol., vol. 3, pp. 19–31,
1996.
[16] P. Hanarp, D. Sutherland, J. Gold, and B. Kasemo, “Nanostructured
model biomaterial surfaces prepared by colloidal lithography,” Nanos-
truct. Mater., vol. 12, pp. 429–432, 1999.
[17] U. Ludewig, M. Pusch, and T. J. Jentsch, “Two physically distinct pores
in the dimeric CIC-O chloride channel,” Nature, vol. 383, pp. 340–343,
1996.
[18] A. R. Leitch, T. Schwarzacher, W. Mosgoller, M. D. Bennett, and J.
S. Heslop-Harrison, “Parental genomes are separated throughout the
cell-cycle in a plant hybrid,” Chromosoma, vol. 101, pp. 206–213,
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