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The Influence of Microgrooved Surfaces on the Behavior and Celluar Function of Osteoblasts

Qirong Li

West China School of Stomatology Sichuan University, oral implantology, Chengdu, Sichuan 610041, China

Yuchen Guo

West China School of Stomatology Sichuan University, oral implantology, Chengdu, Sichuan 610041, China

Yongyue Wang

West China School of Stomatology Sichuan University, oral implantology, Chengdu, Sichuan 610041, China

E-mail : westchinawangyy@163.com

DOI: 10.15761/DOCR.1000176

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Abstract

Since 1945 Weiss Paul described the phenomenon ‘contact guidance’ which means the cell elongates along the direction of the groove and migrates guided by the grooves. Cell could sense the surface topography where it lies and react to these surface cues. Many researches have devoted themselves to reveal the potential mechanisms. The interaction is mainly mediated by the cytoskeleton, the focal adhesions and the extracellular matrix (ECM). But how would the groove dimensions affect the cellular behavior is still obscure. Nowadays, micro fabrication techniques such as electron beam lithography have been applied to the production of micro-textured surfaces. They are relatively fast and cheap, and could fabricate microgrooves of reasonable size. Thus, they have been widely utilized to generate (micro-) nano-topographical surfaces or scaffolds for in vitro cell research. According to the report of P. CLARK, the response of cells to micro-grooved surfaces is cell type-dependent, so the focus of this review is on the osteoblast(s) reaction to micro-grooved surfaces.

Key words

osteoblast(s), nanotechnology, Surface chemistry /properties, cell biology, cell differentiation, cell-matrix interactions

Introduction

A century ago, in 1911 Harrison depicted that cells cultured on spider’s webs grew along the fibers [1]. Later on, in 1945 Weiss P initially named the phenomenon ‘contact guidance’: a tendency of cells to align, grow, or migrate along the grooves [2]. Cell can ‘sense’ the surface topography and then take reaction to these surface cues. The interaction between substrates and cells is achieved through the effort of the cytoskeleton, the extracellular matrix (ECM) [3-5] and the focal adhesions [6].

In terms of the defined (micro-) nano-topographical surface, they are usually produced by the micromachining technology: lithographic patterning (photolithography, electron beam lithography, colloidal lithography), galvanoformung abformung process LIGA, focused ion beam-chemical vapor deposition FIB-CVD and so on. Some of these techniques such as electron beam lithography (EBL) have been developed for creating well-defined patterns with feature sizes <10 nm [7]. Recent years, femtosecond laser patterning has obtained a position in the microgrooves‵ machining [8,9]. These techniques promoted the development of biomaterials and tissue engineering greatly.

As the response of cells to micro-grooved surfaces is cell type-dependent [10], the react of osteoblasts to the micro-machined surface might be different from other cell types. This review is based on the gathered information about the defined microgrooves, ranging from nanometers to microns, role on the osteoblasts, aiming at finding out the interaction between these ultrafine arrays and the bone-forming cells.

Micro/Nanofabrication technologies

A variety of methods such as Femtosecond laser microtexturing can be applied to the fabrication of microtextured surface. These nano/micro patterning techniques were early used in the semiconductor and microelectronics industries [11], later they were increasingly applied in biology, medicine, and biomedical engineering fields [12]. Researchers [13,14] use these techniques to manufacture materials, attempting to get a value that is optimal for the growth of cells. These technologies both have their adaptations as well as limitations, also they have got developments. Hence it is hard to define the best tech in this field [15].

Microgrooved surface influences cellular behavior

Cell adhesive to the grafting materials, more importantly, they are in reciprocity with them. Different surface materials and topographies may induce distinct cell morphology, proliferation, and gene expression [16]. Cells can “sense” substrate elasticity [17,18] as long as its surface patterns in the scope of 10 nm to 100 mm [19,20].

Different dimensions are thought to play varied roles in cellular behavior [10,21]. The average size of the osteoblasts is 20-30μm. When the dimensions of grooves/ridges are reduced to the sizes of the cells and less, topographic effects on cell orientation become more prominent [22]. As will be discussed below, a majority of results focused on groove width of the micro-or-nanoscaled surface, some reports show that ridge width is more important in conducting the cellular behavior, while maybe the groove depth is the leading factor inducing cellular activities.

Groove/ridge topographies are important modulators of both cellular adhesion and osteospecific function and that groove width is vital in determining cellular response [23]. Certain groove width guides the cell to align along the direction [8,9,24,25]. The change of the width affects celluar shape [26], attachment [27], cellular proliferation [28] as well as bone forming ability [25,26]. Form these opinions and Table 1 and 2, we can infer that substrates with the microgroove width of 1-5μm, particularly 2μm seems to be optical for the biological behavior of osteoblasts. On 2μm-wide-grooves the cellular adhesion [29], proliferation [28], osteogenic differentiation [28,30] as well as calcification [28]. Also,these nanophase material increased adhesions of osteoblasts compared with the conventional materials [31]. Depicted in table 2, almost all of these dimensions guide the cells to align along the long axis of micropatterns. Some nano-dimensions display an osteogenic influencing function [25,30,32].

Table 1. The influence of microscale microgrooves on osteoblasts′ function.

References

Cell and Substrate type

Groov width(µm)

Ridge width (µm)

Groove Depth (µm)

Results

Delgado‐Ruíz et al. 2015) [9]

hFOB, zirconia

30

70

LSA, density and cellular activity increase

(Matsuzaka et al. 2003)  [27]

RBM cells, polystyrene 

1, 2, 5, 10      

1, 2, 5, 10     

0.5, 1,1.5         

smooth and grooves >5 μm cells extensions close to substrates grooves〈2μm were bridged

(Puckett et al. 2008) [26]

human osteobalsts, titanium

80,48,22      

45, 35 30          

Attachment gradually decrease, cellular function increase, cellular shape change

(Biggs et al. 2009) [39]

HOB, PMMA

10,100

10,100

300 nm

10μm focal adhesions and osteospecific lineage decrease adipospecific genes increased 100μm cellular adhesion increase

(Ismail et al. 2007) [29]

MG63, silicon

2, 4, 8,10

1.5-2

cell viability 8, 10μm grooves increase

smaller groove sizes smooth one’s better cell adhesion

(Abagnale et al. 2015) [30]

MSCs, Polyimide

2,3,5,10,15

2,3,5,10,15

15 down to sub-micrometer

1 5μm ridges increased, adipogenic differentiation,2μm enhanced osteogenic differentiation

(Biggs et al. 2008) [23]

HOBs, Silicon

10, 25, 100

10, 25,100

330nm

planar adhesion more,100μm increased osteospecific function, 25μm reduction SMA increase FX formation,10μm reduced, adhesion and induced an interplay of up- a and downregulation of gene expression

(Taniguchi et al. 2015) [28]

MC3T3-E1, zirconia, polycrystal

2μm

— 

— 

proliferation was significantly greater, The Runx2 mRNA level increased time dependently, calcification and ALP activity and osteocalcin mRNA levels were higher

(Lu and Leng 2009) [21]

osteoblast, myoblast, silicon

8, 24

—         

2, 4, 10

8μm width strongly affect both osteoblasts and myoblasts 24μm strongly affect myoblasts only

(Lu and Leng 2003) [40]

osteoblast, myoblast, silicon

8, 24

2, 4, 10

8μm width strongly affect both osteoblasts and myoblasts, 24μm strongly affect myoblasts only

(Lu and Leng 2003) [40]

SaOS-2, Ti and HA

4, 8, 16, 24, 30, 38

2, 4, 10

No difference in orientation angle between HA and Ti microgrooves

(Koo et al. 2014) [41]

human primary cells, titanium

15-, 30-, 60-

3.5- ,10-

lower levels of type I collagen 1 gene expression at day 14, extremely increase in osteopontin gene expression at days 21 and 28

(Hamilton and Brunette 2007) [42]

Osteoblast cell, epoxy-resin 

 Pitch: 30-175

5-175

 

Total tyrosine phosphorylation increased Src levels decrease, but FAK and ERK1/2 phosphorylation were highest, Inhibition of Src phosphorylation with PP2 inhibited FAK and ERK 1/2 phosphorylation

(Fransiska et al. 2013) [43]

ROS, silicon

from 1 to 20

width less than 10 μm induced the alignment of osteoblasts, increase osteogenic proteins

Table 2. The influence of nanoscale microgrooves on osteoblasts′ function.

References

Cell and Substrate type

Groov width(nm)

Ridge width (nm)

Groove Depth (nm)

Results

(Lamers et al. 2010) [25]

rats bone marrow stromal cells, silicon

down to 75

down to 33

minimal align dimensions’ width:75nm nanogroove-to-ridge ratios of 1:1, 1:3 and 3:1 depth:33nm. minimal mineralization width: 50nm, depth:17nm, osteoblast- specific gene expression increased

(Yim et al. 2007) [44]

hMSCs, Poly(dimethylsiloxane)

350 ,700

350

Upregulation of neuronal

     markers— MAP2 and GFAP

 

 

 

(Yang et al. 2009) [45]

MG-63, Silicon       

90,150,250,340,500

90,150,250,340,500   

elongated and aligned along the direction, so does cell nucleiei

(Abagnale et al. 2015) [30]

MSCs, Polyimide                 

pitch of 650

200

increased differentiation towards both osteogenic and adipogenic lineages

(Azeem et al. 2015) [32]

Primary human osteoblasts polystyrene

~1860

~2220

~35, 306,2046

~306 and 2046 nm promote osteoblast alignment parallel to

underlined topography in vitro In vivo showed osteogenic ability

 

(Lenhert et al. 2005) [46]

Primary osteoblasts, polystyrene    

periodicity of 500           

50, 150              

align, elongate and migrate parallel to the grooves

(Lamers et al. 2012) [47]

old male Wistar WU rats Osteoblast-like cells, silicon

periods 1000, 300,150

32-150

Cells aligned down to 300 nm pitch In vivo 150 nm pitch grooves has the lowest

density of multinucleated cells

(Prodanov et al. 2013) [48]

MC3T3-E1, silicon

200

50

PFF(pulsatile fluid flow)did affect cellular morphology. Cells aligned on

nanotexture substrate in a direction parallel to the groove orientation

(Prodanov et al. 2010) [49]

Rat MSCs, Silicone rubber

300 (600 pitch)

1 μm(pitch 2 μm)

∼150, 500

perpendicular the substrates when parallel stretch to the nanotexture greater

than 3% applied

(Klymov et al. 2015) [33]

Rat MSCs, Silicon, polystyrene

10 – 1000 ridge to groove ratios of 1:1, 1:3 and 3:1

All sizes of squares showed strong cell-repelling capacity. 3:1 partially

showed cell attraction

Those who focused on the effect of ridge part had some limited findings. Alexey Klymov et al. designed the substrates with ridge to groove ratios of 1:1, 1:3 and 3:1. He demonstrated that nano-grooved patterns with the ridge to groove ratio of 1:3 showed cell repelling, meanwhile grooves with the ridge to groove ratio of 3:1 partially showed cell attraction during cellular selective migration [33]. Apart from that the ridge width clearly enhanced differentiation of MSCs towards specific lineages [30]. Tests on other kinds of cells, say fibroblasts, found that ridge width is the main parameter affecting cell alignment (alignment being inversely proportional to ridge width) [34].

Actually there is no defined item about the influence of groove depth on the osteoblast. From the information Azeem A reported, 306nm and 2046nm promoted osteoblasts alignment parallel to underlined topography. Besides this size showed its osteogenesis ability [32]. Kenichi Matsuzaka observed that on a 0.5μm deep and 10μm wide grooved surface, the cell descends into the groove, on a 1.5μm deep and 1μm wide grooved surface, cells attach to the ridges only. Nowhere, differences were observed between specimens with different groove depths. Instead Kenichi Matsuzaka attributed this phenomenon to the width of the ridge merely [27].

In vivo studies on effect of the surface micromachining to the osseointegration also take for the positive side. The laser micromachining technology enhances bone [24] and soft-tissue integration and controls the local microstructural geometry of attached bone [35]. The organized pattern of the microgrooved surfaces is capable of resulting in transverse collagen fiber microenvironment reaction to the load, being positive to promote and to maintain the bone remodeling; in addition, blood vessels and bone cells are able to penetrate microgrooved surfaces [36]. What’s more, micromachined implants enhances primary and secondary implant stability, preserves crestal bone levels [36,37].

Conclusions and outlook

With the acceptance of ‘contact guidance’ theory, many defined patterns were made by various micro/nano technoloies, prompting the study of different dimensions to the cellular behavior. The limited collected data in the table 1 and 2 showed that the groove width is the most influencing factor affecting the osteoblasts. On the micropatterned substrates, osteoblasts adhere and elongate along the long axis of the microgrooves. Improper width of microgrooves may lead to adhesion down growth. On certain groove width cell density, proliferation and osteogenic ability show an improvement. The differentiation also can be affected by the nanotopography. However, the reports based on the virtues of the ridge width and the depth of the array still needs further exploration. Moreover, we can do a further step research on the effect of the wettability and inclination of ridge. Soluble biochemical cues, dynamic control and regulation of topographical features, as well as cell co-culture systems, have all been declared to act in synergy with physical cues in regulating stem cell fate [38]. When we design a test, multi-factors should be taken into consideration. In conclusion, critical dimensions do play a part in regulating celluar behavior. However, it is a pity that we have not completely revealed the mystery of micro-nanotopographical on the osteoblasts. In addition, which dimension of microarrays is optimal for the adhesion, proliferation, differentiation, and osteogenisis is still under research. We can use the obtained data as a guide and reference for the study in the future. Besides, these results could be helpful in the design and fabrication of implants and biomaterials.

Acknowledgement

The authors acknowledge funding from the Chengdu science and technology huimin engineering projects. China. 0040305301462. The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

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Editorial Information

Editor-in-Chief

JON B. SUZUKI
Temple University

Article Type

Research article

Publication history

Received date: August 29, 2016
Accepted date: September 19, 2016
Published date: September 22, 2016

Copyright

© 2016 Li Q. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Citation

Li Q, Guo Y, Wang Y (2016) The influence of microgrooved surfaces on the behavior and celluar function of osteoblasts. Dent Oral Craniofac Res 2: DOI: 10.15761/DOCR.1000176.

Corresponding author

Yongyue Wang

DDS, Ph.D, Professor, Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University, #14, 3rd Section, Renmin Nan Road Chengdu, Sichuan 610041, China, Tel.:86-28-85503579; Fax: 86-28-85582167;

E-mail : westchinawangyy@163.com

Table 1. The influence of microscale microgrooves on osteoblasts′ function.

References

Cell and Substrate type

Groov width(µm)

Ridge width (µm)

Groove Depth (µm)

Results

Delgado‐Ruíz et al. 2015) [9]

hFOB, zirconia

30

70

LSA, density and cellular activity increase

(Matsuzaka et al. 2003)  [27]

RBM cells, polystyrene 

1, 2, 5, 10      

1, 2, 5, 10     

0.5, 1,1.5         

smooth and grooves >5 μm cells extensions close to substrates grooves〈2μm were bridged

(Puckett et al. 2008) [26]

human osteobalsts, titanium

80,48,22      

45, 35 30          

Attachment gradually decrease, cellular function increase, cellular shape change

(Biggs et al. 2009) [39]

HOB, PMMA

10,100

10,100

300 nm

10μm focal adhesions and osteospecific lineage decrease adipospecific genes increased 100μm cellular adhesion increase

(Ismail et al. 2007) [29]

MG63, silicon

2, 4, 8,10

1.5-2

cell viability 8, 10μm grooves increase

smaller groove sizes smooth one’s better cell adhesion

(Abagnale et al. 2015) [30]

MSCs, Polyimide

2,3,5,10,15

2,3,5,10,15

15 down to sub-micrometer

1 5μm ridges increased, adipogenic differentiation,2μm enhanced osteogenic differentiation

(Biggs et al. 2008) [23]

HOBs, Silicon

10, 25, 100

10, 25,100

330nm

planar adhesion more,100μm increased osteospecific function, 25μm reduction SMA increase FX formation,10μm reduced, adhesion and induced an interplay of up- a and downregulation of gene expression

(Taniguchi et al. 2015) [28]

MC3T3-E1, zirconia, polycrystal

2μm

— 

— 

proliferation was significantly greater, The Runx2 mRNA level increased time dependently, calcification and ALP activity and osteocalcin mRNA levels were higher

(Lu and Leng 2009) [21]

osteoblast, myoblast, silicon

8, 24

—         

2, 4, 10

8μm width strongly affect both osteoblasts and myoblasts 24μm strongly affect myoblasts only

(Lu and Leng 2003) [40]

osteoblast, myoblast, silicon

8, 24

2, 4, 10

8μm width strongly affect both osteoblasts and myoblasts, 24μm strongly affect myoblasts only

(Lu and Leng 2003) [40]

SaOS-2, Ti and HA

4, 8, 16, 24, 30, 38

2, 4, 10

No difference in orientation angle between HA and Ti microgrooves

(Koo et al. 2014) [41]

human primary cells, titanium

15-, 30-, 60-

3.5- ,10-

lower levels of type I collagen 1 gene expression at day 14, extremely increase in osteopontin gene expression at days 21 and 28

(Hamilton and Brunette 2007) [42]

Osteoblast cell, epoxy-resin 

 Pitch: 30-175

5-175

 

Total tyrosine phosphorylation increased Src levels decrease, but FAK and ERK1/2 phosphorylation were highest, Inhibition of Src phosphorylation with PP2 inhibited FAK and ERK 1/2 phosphorylation

(Fransiska et al. 2013) [43]

ROS, silicon

from 1 to 20

width less than 10 μm induced the alignment of osteoblasts, increase osteogenic proteins

Table 2. The influence of nanoscale microgrooves on osteoblasts′ function.

References

Cell and Substrate type

Groov width(nm)

Ridge width (nm)

Groove Depth (nm)

Results

(Lamers et al. 2010) [25]

rats bone marrow stromal cells, silicon

down to 75

down to 33

minimal align dimensions’ width:75nm nanogroove-to-ridge ratios of 1:1, 1:3 and 3:1 depth:33nm. minimal mineralization width: 50nm, depth:17nm, osteoblast- specific gene expression increased

(Yim et al. 2007) [44]

hMSCs, Poly(dimethylsiloxane)

350 ,700

350

Upregulation of neuronal

     markers— MAP2 and GFAP

 

 

 

(Yang et al. 2009) [45]

MG-63, Silicon       

90,150,250,340,500

90,150,250,340,500   

elongated and aligned along the direction, so does cell nucleiei

(Abagnale et al. 2015) [30]

MSCs, Polyimide                 

pitch of 650

200

increased differentiation towards both osteogenic and adipogenic lineages

(Azeem et al. 2015) [32]

Primary human osteoblasts polystyrene

~1860

~2220

~35, 306,2046

~306 and 2046 nm promote osteoblast alignment parallel to

underlined topography in vitro In vivo showed osteogenic ability

 

(Lenhert et al. 2005) [46]

Primary osteoblasts, polystyrene    

periodicity of 500           

50, 150              

align, elongate and migrate parallel to the grooves

(Lamers et al. 2012) [47]

old male Wistar WU rats Osteoblast-like cells, silicon

periods 1000, 300,150

32-150

Cells aligned down to 300 nm pitch In vivo 150 nm pitch grooves has the lowest

density of multinucleated cells

(Prodanov et al. 2013) [48]

MC3T3-E1, silicon

200

50

PFF(pulsatile fluid flow)did affect cellular morphology. Cells aligned on

nanotexture substrate in a direction parallel to the groove orientation

(Prodanov et al. 2010) [49]

Rat MSCs, Silicone rubber

300 (600 pitch)

1 μm(pitch 2 μm)

∼150, 500

perpendicular the substrates when parallel stretch to the nanotexture greater

than 3% applied

(Klymov et al. 2015) [33]

Rat MSCs, Silicon, polystyrene

10 – 1000 ridge to groove ratios of 1:1, 1:3 and 3:1

All sizes of squares showed strong cell-repelling capacity. 3:1 partially

showed cell attraction