An update of nanotopographical surfaces in modulating stem cell fate: a narrative review

doi:10.12336/biomatertransl.2022.01.006

Biomaterials Translational ›› 2022, Vol. 3 ›› Issue (1): 55-64.doi: 10.12336/biomatertransl.2022.01.006

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An update of nanotopographical surfaces in modulating stem cell fate: a narrative review

Shuqin Cao, Quan Yuan^*()

State Key Laboratory of Oral Diseases, National Clinical Research Centre for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan Province, China

Received:2022-01-24 Revised:2022-03-06 Accepted:2022-03-10 Online:2022-03-28 Published:2022-03-28
Contact: Quan Yuan E-mail:yaunquan@scu.edu.cn
About author:Quan Yuan, yaunquan@scu.edu.cn.

Abstract

Abstract:

Stem cells have been one of the ideal sources for tissue regeneration owing to their capability of self-renewal and differentiation. In vivo, the extracellular microenvironment plays a vital role in modulating stem cell fate. When developing biomaterials for regenerative medicine, incorporating biochemical and biophysical cues to mimic extracellular matrix can enhance stem cell lineage differentiation. More specifically, modulating the stem cell fate can be achieved by controlling the nanotopographic features on synthetic surfaces. Optimization of nanotopographical features leads to desirable stem cell functions, which can maximize the effectiveness of regenerative treatment. In this review, nanotopographical surfaces, including static patterned surface, dynamic patterned surface, and roughness are summarized, and their fabrication, as well as the impact on stem cell behaviour, are discussed. Later, the recent progress of applying nanotopographical featured biomaterials for altering different types of stem cells is presented, which directs the design and fabrication of functional biomaterial. Last, the perspective in fundamental research and for clinical application in this field is discussed.

Key words: biomaterials, mechanotransduction, nanotopographical surfaces, stem cell, tissue regeneration

1.	Bianco, P.; Robey, P. G. Stem cells in tissue engineering. Nature. 2001, 414, 118-121. doi: 10.1038/35102181 URL
2.	Frazier, T.; Hamel, K.; Wu, X.; Rogers, E.; Lassiter, H.; Robinson, J.; Mohiuddin, O.; Henderson, M.; Gimble, J. Adipose-derived cells: building blocks of three-dimensional microphysiological systems. Biomater Transl. 2021, 2, 301-306.
3.	Mahla, R. S. Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol. 2016, 2016, 6940283.
4.	Jones, D. L.; Wagers, A. J. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol. 2008, 9, 11-21.
5.	Morrison, S. J.; Spradling, A. C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 2008, 132, 598-611. doi: 10.1016/j.cell.2008.01.038 URL
6.	Ding, S.; Kingshott, P.; Thissen, H.; Pera, M.; Wang, P. Y. Modulation of human mesenchymal and pluripotent stem cell behavior using biophysical and biochemical cues: A review. Biotechnol Bioeng. 2017, 114, 260-280. doi: 10.1002/bit.26075 URL
7.	Li, J.; Liu, Y.; Zhang, Y.; Yao, B.; Enhejirigala; Li, Z.; Song, W.; Wang, Y.; Duan, X.; Yuan, X.; Fu, X.; Huang, S. Biophysical and biochemical cues of biomaterials guide mesenchymal stem cell behaviors. Front Cell Dev Biol. 2021, 9, 640388. doi: 10.3389/fcell.2021.640388 URL
8.	Lou, H. Y.; Zhao, W.; Li, X.; Duan, L.; Powers, A.; Akamatsu, M.; Santoro, F.; McGuire, A. F.; Cui, Y.; Drubin, D. G.; Cui, B. Membrane curvature underlies actin reorganization in response to nanoscale surface topography. Proc Natl Acad Sci U S A. 2019, 116, 23143-23151. doi: 10.1073/pnas.1910166116 URL
9.	Wan, X.; Liu, Z.; Li, L. Manipulation of stem cells fates: the master and multifaceted roles of biophysical cues of biomaterials. Adv Funct Mater. 2021, 31, 2010626. doi: 10.1002/adfm.v31.23 URL
10.	Wang, S.; Hashemi, S.; Stratton, S.; Arinzeh, T. L. The effect of physical cues of biomaterial scaffolds on stem cell behavior. Adv Healthc Mater. 2021, 10, e2001244.
11.	Hou, Y.; Xie, W.; Fan, X.; Tang, P.; Yu, L.; Haag, R. “Raspberry” hierarchical topographic features regulate human mesenchymal stem cell adhesion and differentiation via enhanced mechanosensing. ACS Appl Mater Interfaces. 2021, 13, 54840-54849. doi: 10.1021/acsami.1c18722 URL
12.	Yu, L.; Tang, P.; Nie, C.; Hou, Y.; Haag, R. Well-defined nanostructured biointerfaces: strengthened cellular interaction for circulating tumor cells isolation. Adv Healthc Mater. 2021, 10, e2002202.
13.	Zhang, M.; Sun, Q.; Liu, Y.; Chu, Z.; Yu, L.; Hou, Y.; Kang, H.; Wei, Q.; Zhao, W.; Spatz, J. P.; Zhao, C.; Cavalcanti-Adam, E. A. Controllable ligand spacing stimulates cellular mechanotransduction and promotes stem cell osteogenic differentiation on soft hydrogels. Biomaterials. 2021, 268, 120543. doi: 10.1016/j.biomaterials.2020.120543 URL
14.	Qiang, W.; Shenghao, W.; Feng, H.; Huan, W.; Weidong, Z.; Qifan, Y.; Changjiang, L.; Luguang, D.; Jiayuan, W.; Lili, Y.; Caihong, Z.; Bin, L. Cellular modulation by the mechanical cues from biomaterials for tissue engineering. Biomater Transl. 2021, 2, 323-342.
15.	Chen, W.; Shao, Y.; Li, X.; Zhao, G.; Fu, J. Nanotopographical surfaces for stem cell fate control: engineering mechanobiology from the bottom. Nano Today. 2014, 9, 759-784. doi: 10.1016/j.nantod.2014.12.002 URL
16.	Firkowska-Boden, I.; Helbing, C.; Dauben, T. J.; Pieper, M.; Jandt, K. D. How nanotopography-induced conformational changes of fibrinogen affect platelet adhesion and activation. Langmuir. 2020, 36, 11573-11580. doi: 10.1021/acs.langmuir.0c02094 URL
17.	Dalby, M. J.; Gadegaard, N.; Oreffo, R. O. Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. Nat Mater. 2014, 13, 558-569. doi: 10.1038/nmat3980 URL
18.	Kartikasari, N.; Yamada, M.; Watanabe, J.; Tiskratok, W.; He, X.; Kamano, Y.; Egusa, H. Titanium surface with nanospikes tunes macrophage polarization to produce inhibitory factors for osteoclastogenesis through nanotopographic cues. Acta Biomater. 2022, 137, 316-330. doi: 10.1016/j.actbio.2021.10.019 URL
19.	Damiati, L. A.; Tsimbouri, M. P.; Hernandez, V. L.; Jayawarna, V.; Ginty, M.; Childs, P.; Xiao, Y.; Burgess, K.; Wells, J.; Sprott, M. R.; Meek, R. M. D.; Li, P.; Oreffo, R. O. C.; Nobbs, A.; Ramage, G.; Su, B.; Salmeron-Sanchez, M.; Dalby, M. J. Materials-driven fibronectin assembly on nanoscale topography enhances mesenchymal stem cell adhesion, protecting cells from bacterial virulence factors and preventing biofilm formation. Biomaterials. 2022, 280, 121263. doi: 10.1016/j.biomaterials.2021.121263 URL
20.	Chen, Z.; Ni, S.; Han, S.; Crawford, R.; Lu, S.; Wei, F.; Chang, J.; Wu, C.; Xiao, Y. Nanoporous microstructures mediate osteogenesis by modulating the osteo-immune response of macrophages. Nanoscale. 2017, 9, 706-718. doi: 10.1039/C6NR06421C URL
21.	Ripamonti, U. Functionalized surface geometries induce: “bone: formation by autoinduction”. Front Physiol. 2017, 8, 1084. doi: 10.3389/fphys.2017.01084 URL
22.	Donnelly, H.; Dalby, M. J.; Salmeron-Sanchez, M.; Sweeten, P. E. Current approaches for modulation of the nanoscale interface in the regulation of cell behavior. Nanomedicine. 2018, 14, 2455-2464.
23.	Ankam, S.; Teo, B. K. K.; Pohan, G.; Ho, S. W. L.; Lim, C. K.; Yim, E. K. F. Temporal changes in nucleus morphology, lamin A/C and histone methylation during nanotopography-induced neuronal differentiation of stem cells. Front Bioeng Biotechnol. 2018, 6, 69. doi: 10.3389/fbioe.2018.00069 URL
24.	Jiao, A.; Moerk, C. T.; Penland, N.; Perla, M.; Kim, J.; Smith, A. S. T.; Murry, C. E.; Kim, D. H. Regulation of skeletal myotube formation and alignment by nanotopographically controlled cell-secreted extracellular matrix. J Biomed Mater Res A. 2018, 106, 1543-1551. doi: 10.1002/jbm.a.v106.6 URL
25.	Xia, Y.; Whitesides, G. M. Soft lithography. Annu Rev Mater Sci. 1998, 28, 153-184. doi: 10.1146/matsci.1998.28.issue-1 URL
26.	Griffin, M. F.; Butler, P. E.; Seifalian, A. M.; Kalaskar, D. M. Control of stem cell fate by engineering their micro and nanoenvironment. World J Stem Cells. 2015, 7, 37-50. doi: 10.4252/wjsc.v7.i1.37 URL
27.	Higuchi, A.; Ling, Q. D.; Chang, Y.; Hsu, S. T.; Umezawa, A. Physical cues of biomaterials guide stem cell differentiation fate. Chem Rev. 2013, 113, 3297-3328. doi: 10.1021/cr300426x URL
28.	Kilian, K. A.; Bugarija, B.; Lahn, B. T.; Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A. 2010, 107, 4872-4877. doi: 10.1073/pnas.0903269107 URL
29.	van Dorp, W. F.; Zhang, X.; Feringa, B. L.; Hansen, T. W.; Wagner, J. B.; De Hosson, J. T. Molecule-by-molecule writing using a focused electron beam. ACS Nano. 2012, 6, 10076-10081. doi: 10.1021/nn303793w URL
30.	Basnar, B.; Willner, I. Dip-pen-nanolithographic patterning of metallic, semiconductor, and metal oxide nanostructures on surfaces. Small. 2009, 5, 28-44. doi: 10.1002/smll.v5:1 URL
31.	Norman, J. J.; Desai, T. A. Methods for fabrication of nanoscale topography for tissue engineering scaffolds. Ann Biomed Eng. 2006, 34, 89-101. doi: 10.1007/s10439-005-9005-4 URL
32.	Higgins, S. G.; Becce, M.; Belessiotis-Richards, A.; Seong, H.; Sero, J. E.; Stevens, M. M. High-aspect-ratio nanostructured surfaces as biological metamaterials. Adv Mater. 2020, 32, e1903862.
33.	Bucaro, M. A.; Vasquez, Y.; Hatton, B. D.; Aizenberg, J. Fine-tuning the degree of stem cell polarization and alignment on ordered arrays of high-aspect-ratio nanopillars. ACS Nano. 2012, 6, 6222-6230. doi: 10.1021/nn301654e URL
34.	Kim, J. S.; Kuk, E.; Yu, K. N.; Kim, J. H.; Park, S. J.; Lee, H. J.; Kim, S. H.; Park, Y. K.; Park, Y. H.; Hwang, C. Y.; Kim, Y. K.; Lee, Y. S.; Jeong, D. H.; Cho, M. H. Antimicrobial effects of silver nanoparticles. Nanomedicine. 2007, 3, 95-101.
35.	Rasmussen, C. H.; Reynolds, P. M.; Petersen, D. R.; Hansson, M.; McMeeking, R. M.; Dufva, M.; Gadegaard, N. Enhanced differentiation of human embryonic stem cells toward definitive endoderm on ultrahigh aspect ratio nanopillars. Adv Funct Mater. 2016, 26, 815-823. doi: 10.1002/adfm.v26.6 URL
36.	Kim, J. H.; Kim, H. W.; Cha, K. J.; Han, J.; Jang, Y. J.; Kim, D. S.; Kim, J. H. Nanotopography promotes pancreatic differentiation of human embryonic stem cells and induced pluripotent stem cells. ACS Nano. 2016, 10, 3342-3355. doi: 10.1021/acsnano.5b06985 URL
37.	Karazisis, D.; Omar, O.; Petronis, S.; Thomsen, P.; Rasmusson, L. Molecular response to nanopatterned implants in the human jaw bone. ACS Biomater Sci Eng. 2021, 7, 5878-5889. doi: 10.1021/acsbiomaterials.1c00861 URL
38.	Seo, C. H.; Jeong, H.; Feng, Y.; Montagne, K.; Ushida, T.; Suzuki, Y.; Furukawa, K. S. Micropit surfaces designed for accelerating osteogenic differentiation of murine mesenchymal stem cells via enhancing focal adhesion and actin polymerization. Biomaterials. 2014, 35, 2245-2252. doi: 10.1016/j.biomaterials.2013.11.089 URL
39.	Kim, H. J Regulation of neural stem cell fate by natural products. Biomol Ther (Seoul). 2019, 27, 15-24. doi: 10.4062/biomolther.2018.184 URL
40.	Park, S.; Park, H. H.; Sun, K.; Gwon, Y.; Seong, M.; Kim, S.; Park, T. E.; Hyun, H.; Choung, Y. H.; Kim, J.; Jeong, H. E. Hydrogel nanospike patch as a flexible anti-pathogenic scaffold for regulating stem cell behavior. ACS Nano. 2019, 13, 11181-11193. doi: 10.1021/acsnano.9b04109 URL
41.	Armstrong, J. P. K.; Puetzer, J. L.; Serio, A.; Guex, A. G.; Kapnisi, M.; Breant, A.; Zong, Y.; Assal, V.; Skaalure, S. C.; King, O.; Murty, T.; Meinert, C.; Franklin, A. C.; Bassindale, P. G.; Nichols, M. K.; Terracciano, C. M.; Hutmacher, D. W.; Drinkwater, B. W.; Klein, T. J.; Perriman, A. W.; Stevens, M. M. Engineering anisotropic muscle tissue using acoustic cell patterning. Adv Mater. 2018, 30, e1802649.
42.	Kim, C. S.; Kim, J. H.; Kim, B.; Park, Y. S.; Kim, H. K.; Tran, H. T.; Kim, S. H.; Jeon, H.; Kim, S.; Sim, J. H.; Shin, H. M.; Kim, G.; Baik, Y. J.; Lee, K. J.; Kim, H. Y.; Yun, T. J.; Kim, Y. S.; Kim, H. R. A specific groove pattern can effectively induce osteoblast differentiation. Adv Funct Mater. 2017, 27, 1703569. doi: 10.1002/adfm.v27.44 URL
43.	Baek, J.; Jung, W. B.; Cho, Y.; Lee, E.; Yun, G. T.; Cho, S. Y.; Jung, H. T.; Im, S. G. Facile fabrication of high-definition hierarchical wrinkle structures for investigating the geometry-sensitive fate commitment of human neural stem cells. ACS Appl Mater Interfaces. 2019, 11, 17247-17255. doi: 10.1021/acsami.9b03479 URL
44.	Bjørge, I. M.; Choi, I. S.; Correia, C. R.; Mano, J. F. Nanogrooved microdiscs for bottom-up modulation of osteogenic differentiation. Nanoscale. 2019, 11, 16214-16221. doi: 10.1039/C9NR06267J URL
45.	Leclech, C.; Villard, C. Cellular and subcellular contact guidance on microfabricated substrates. Front Bioeng Biotechnol. 2020, 8, 551505. doi: 10.3389/fbioe.2020.551505 URL
46.	Abagnale, G.; Sechi, A.; Steger, M.; Zhou, Q.; Kuo, C. C.; Aydin, G.; Schalla, C.; Müller-Newen, G.; Zenke, M.; Costa, I. G.; van Rijn, P.; Gillner, A.; Wagner, W. Surface topography guides morphology and spatial patterning of induced pluripotent stem cell colonies. Stem Cell Reports. 2017, 9, 654-666. doi: 10.1016/j.stemcr.2017.06.016 URL
47.	Lee, M. R.; Kwon, K. W.; Jung, H.; Kim, H. N.; Suh, K. Y.; Kim, K.; Kim, K. S. Direct differentiation of human embryonic stem cells into selective neurons on nanoscale ridge/groove pattern arrays. Biomaterials. 2010, 31, 4360-4366. doi: 10.1016/j.biomaterials.2010.02.012 URL
48.	De Martino, S.; Zhang, W.; Klausen, L.; Lou, H. Y.; Li, X.; Alfonso, F. S.; Cavalli, S.; Netti, P. A.; Santoro, F.; Cui, B. Dynamic manipulation of cell membrane curvature by light-driven reshaping of azopolymer. Nano Lett. 2020, 20, 577-584. doi: 10.1021/acs.nanolett.9b04307 URL
49.	Nickmans, K.; van der Heijden, D. A. C.; Schenning, A. P. H. J. Photonic shape memory chiral nematic polymer coatings with changing surface topography and color. Adv Funct Mater. 2019, 7, 1900592.
50.	Wei, Y.; Mo, X.; Zhang, P.; Li, Y.; Liao, J.; Li, Y.; Zhang, J.; Ning, C.; Wang, S.; Deng, X.; Jiang, L. Directing stem cell differentiation via electrochemical reversible switching between nanotubes and nanotips of polypyrrole array. ACS Nano. 2017, 11, 5915-5924. doi: 10.1021/acsnano.7b01661 URL
51.	De Martino, S.; Cavalli, S.; Netti, P. A. Photoactive interfaces for spatio-temporal guidance of mesenchymal stem cell fate. Adv Healthc Mater. 2020, 9, e2000470.
52.	Shi, H.; Wu, X.; Sun, S.; Wang, C.; Vangelatos, Z.; Ash-Shakoor, A.; Grigoropoulos, C. P.; Mather, P. T.; Henderson, J. H.; Ma, Z. Profiling the responsiveness of focal adhesions of human cardiomyocytes to extracellular dynamic nano-topography. Bioact Mater. 2022, 10, 367-377.
53.	Hou, H.; Yin, J.; Jiang, X. Smart patterned surface with dynamic wrinkles. Acc Chem Res. 2019, 52, 1025-1035. doi: 10.1021/acs.accounts.8b00623 URL
54.	Zhang, S.; Ma, B.; Liu, F.; Duan, J.; Wang, S.; Qiu, J.; Li, D.; Sang, Y.; Liu, C.; Liu, D.; Liu, H. Polylactic acid nanopillar array-driven osteogenic differentiation of human adipose-derived stem cells determined by pillar diameter. Nano Lett. 2018, 18, 2243-2253. doi: 10.1021/acs.nanolett.7b04747 URL
55.	Das Ghosh, L.; Hasan, J.; Jain, A.; Sundaresan, N. R.; Chatterjee, K. A nanopillar array on black titanium prepared by reactive ion etching augments cardiomyogenic commitment of stem cells. Nanoscale. 2019, 11, 20766-20776. doi: 10.1039/C9NR03424B URL
56.	Yang, W.; Han, W.; He, W.; Li, J.; Wang, J.; Feng, H.; Qian, Y. Surface topography of hydroxyapatite promotes osteogenic differentiation of human bone marrow mesenchymal stem cells. Mater Sci Eng C Mater Biol Appl. 2016, 60, 45-53. doi: 10.1016/j.msec.2015.11.012 URL
57.	Chen, H.; Huang, X.; Zhang, M.; Damanik, F.; Baker, M. B.; Leferink, A.; Yuan, H.; Truckenmüller, R.; van Blitterswijk, C.; Moroni, L. Tailoring surface nanoroughness of electrospun scaffolds for skeletal tissue engineering. Acta Biomater. 2017, 59, 82-93. doi: 10.1016/j.actbio.2017.07.003 URL
58.	Sun, S.; Shi, H.; Moore, S.; Wang, C.; Ash-Shakoor, A.; Mather, P. T.; Henderson, J. H.; Ma, Z. Progressive myofibril reorganization of human cardiomyocytes on a dynamic nanotopographic substrate. ACS Appl Mater Interfaces. 2020, 12, 21450-21462. doi: 10.1021/acsami.0c03464 URL
59.	Hou, Y.; Yu, L.; Xie, W.; Camacho, L. C.; Zhang, M.; Chu, Z.; Wei, Q.; Haag, R. Surface roughness and substrate stiffness synergize to drive cellular mechanoresponse. Nano Lett. 2020, 20, 748-757. doi: 10.1021/acs.nanolett.9b04761 URL
60.	Park, J.; Bauer, S.; von der Mark, K.; Schmuki, P. Nanosize and vitality: TiO2 nanotube diameter directs cell fate. Nano Lett. 2007, 7, 1686-1691. doi: 10.1021/nl070678d URL
61.	Oh, S.; Brammer, K. S.; Li, Y. S.; Teng, D.; Engler, A. J.; Chien, S.; Jin, S. Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci U S A. 2007, 106, 2130-2135. doi: 10.1073/pnas.0813200106 URL
62.	Lee, M. S.; Lee, D. H.; Jeon, J.; Oh, S. H.; Yang, H. S. Topographically defined, biodegradable nanopatterned patches to regulate cell fate and acceleration of bone regeneration. ACS Appl Mater Interfaces. 2018, 10, 38780-38790. doi: 10.1021/acsami.8b14745 URL
63.	Dehghan-Baniani, D.; Mehrjou, B.; Chu, P. K.; Wu, H. A Biomimetic nano-engineered platform for functional tissue engineering of cartilage superficial zone. Adv Healthc Mater. 2021, 10, e2001018.
64.	Wu, Y.; Yang, Z.; Denslin, V.; Ren, X.; Lee, C. S.; Yap, F. L.; Lee, E. H. Repair of osteochondral defects with predifferentiated mesenchymal stem cells of distinct phenotypic character derived from a nanotopographic platform. Am J Sports Med. 2020, 48, 1735-1747. doi: 10.1177/0363546520907137 URL
65.	Yao, S.; Liu, X.; Yu, S.; Wang, X.; Zhang, S.; Wu, Q.; Sun, X.; Mao, H. Co-effects of matrix low elasticity and aligned topography on stem cell neurogenic differentiation and rapid neurite outgrowth. Nanoscale. 2016, 8, 10252-10265. doi: 10.1039/C6NR01169A URL
66.	Poudineh, M.; Wang, Z.; Labib, M.; Ahmadi, M.; Zhang, L.; Das, J.; Ahmed, S.; Angers, S.; Kelley, S. O. Three-dimensional nanostructured architectures enable efficient neural differentiation of mesenchymal stem cells via mechanotransduction. Nano Lett. 2018, 18, 7188-7193. doi: 10.1021/acs.nanolett.8b03313 URL
67.	Lim, M. S.; Ko, S. H.; Kim, M. S.; Lee, B.; Jung, H. S.; Kim, K.; Park, C. H. Hybrid nanofiber scaffold-based direct conversion of neural precursor cells/dopamine neurons. Int J Stem Cells. 2019, 12, 340-346. doi: 10.15283/ijsc18123 URL
68.	Yang, S. S.; Cha, J.; Cho, S. W.; Kim, P. Time-dependent retention of nanotopographical cues in differentiated neural stem cells. ACS Biomater Sci Eng. 2019, 5, 3802-3807. doi: 10.1021/acsbiomaterials.8b01057 URL
69.	Cho, Y. W.; Kim, D. S.; Suhito, I. R.; Han, D. K.; Lee, T.; Kim, T. H. Enhancing neurogenesis of neural stem cells using homogeneous nanohole pattern-modified conductive platform. Int J Mol Sci. 2019, 21, 191. doi: 10.3390/ijms21010191 URL
70.	Simitzi, C.; Karali, K.; Ranella, A.; Stratakis, E. Controlling the outgrowth and functions of neural stem cells: the effect of surface topography. Chemphyschem. 2018, 19, 1143-1163. doi: 10.1002/cphc.v19.10 URL
71.	Lee, J. M.; Kang, W. S.; Lee, K. G.; Cho, H. Y.; Conley, B.; Ahrberg, C. D.; Lim, J. H.; Mo, S. J.; Mun, S. G.; Kim, E. J.; Choi, J. W.; Lee, K. B.; Lee, S. J.; Chung, B. G. Combinatorial biophysical cue sensor array for controlling neural stem cell fate. Biosens Bioelectron. 2020, 156, 112125. doi: 10.1016/j.bios.2020.112125 URL
72.	Peter, W. A. Human pluripotent stem cells: tools for regenerative medicine. Biomater Transl. 2021, 2, 294-300.
73.	Tsui, J. H.; Ostrovsky-Snider, N. A.; Yama, D. M. P.; Donohue, J. D.; Choi, J. S.; Chavanachat, R.; Larson, J. D.; Murphy, A. R.; Kim, D. H. Conductive silk-polypyrrole composite scaffolds with bioinspired nanotopographic cues for cardiac tissue engineering. J Mater Chem B. 2018, 6, 7185-7196. doi: 10.1039/C8TB01116H URL
74.	Macgregor, M.; Williams, R.; Downes, J.; Bachhuka, A.; Vasilev, K. The role of controlled surface topography and chemistry on mouse embryonic stem cell attachment, growth and self-renewal. Materials (Basel). 2017, 10, 1081. doi: 10.3390/ma10091081 URL
75.	Kim, J. H.; Park, B. G.; Kim, S. K.; Lee, D. H.; Lee, G. G.; Kim, D. H.; Choi, B. O.; Lee, K. B.; Kim, J. H. Nanotopographical regulation of pancreatic islet-like cluster formation from human pluripotent stem cells using a gradient-pattern chip. Acta Biomater. 2019, 95, 337-347. doi: 10.1016/j.actbio.2018.12.011 URL
76.	Ko, J. Y.; Oh, H. J.; Lee, J.; Im, G. I. Nanotopographic influence on the in vitro behavior of induced pluripotent stem cells. Tissue Eng Part A. 2018, 24, 595-606. doi: 10.1089/ten.tea.2017.0144 URL
77.	Chen, W.; Han, S.; Qian, W.; Weng, S.; Yang, H.; Sun, Y.; Villa-Diaz, L. G.; Krebsbach, P. H.; Fu, J. Nanotopography regulates motor neuron differentiation of human pluripotent stem cells. Nanoscale. 2018, 10, 3556-3565. doi: 10.1039/C7NR05430K URL
78.	Smith, A. S. T.; Choi, E.; Gray, K.; Macadangdang, J.; Ahn, E. H.; Clark, E. C.; Laflamme, M. A.; Wu, J. C.; Murry, C. E.; Tung, L.; Kim, D. H. NanoMEA: a tool for high-throughput, electrophysiological phenotyping of patterned excitable cells. Nano Lett. 2020, 20, 1561-1570. doi: 10.1021/acs.nanolett.9b04152 URL
79.	Pennacchio, F. A.; Caliendo, F.; Iaccarino, G.; Langella, A.; Siciliano, V.; Santoro, F. Three-dimensionally patterned scaffolds modulate the biointerface at the nanoscale. Nano Lett. 2019, 19, 5118-5123. doi: 10.1021/acs.nanolett.9b01468 URL
80.	Hansel, C. S.; Crowder, S. W.; Cooper, S.; Gopal, S.; João Pardelha da Cruz, M.; de Oliveira Martins, L.; Keller, D.; Rothery, S.; Becce, M.; Cass, A. E. G.; Bakal, C.; Chiappini, C.; Stevens, M. M. Nanoneedle-mediated stimulation of cell mechanotransduction machinery. ACS Nano. 2019, 13, 2913-2926. doi: 10.1021/acsnano.8b06998 URL
81.	Salsmann, A.; Schaffner-Reckinger, E.; Kieffer, N. RGD, the Rho’d to cell spreading. Eur J Cell Biol. 2006, 85, 249-254. doi: 10.1016/j.ejcb.2005.08.003 URL
82.	Berrier, A. L.; Yamada, K. M. Cell-matrix adhesion. J Cell Physiol. 2007, 213, 565-573. doi: 10.1002/(ISSN)1097-4652 URL
83.	Wehrle-Haller, B. Structure and function of focal adhesions. Curr Opin Cell Biol. 2012, 24, 116-124. doi: 10.1016/j.ceb.2011.11.001 URL
84.	Dumbauld, D. W.; Lee, T. T.; Singh, A.; Scrimgeour, J.; Gersbach, C. A.; Zamir, E. A.; Fu, J.; Chen, C. S.; Curtis, J. E.; Craig, S. W.; García, A. J. How vinculin regulates force transmission. Proc Natl Acad Sci U S A. 2013, 110, 9788-9793. doi: 10.1073/pnas.1216209110 URL
85.	Roca-Cusachs, P.; del Rio, A.; Puklin-Faucher, E.; Gauthier, N. C.; Biais, N.; Sheetz, M. P. Integrin-dependent force transmission to the extracellular matrix by α-actinin triggers adhesion maturation. Proc Natl Acad Sci U S A. 2013, 110, E1361-1370.
86.	Lv, H.; Li, L.; Sun, M.; Zhang, Y.; Chen, L.; Rong, Y.; Li, Y. Mechanism of regulation of stem cell differentiation by matrix stiffness. Stem Cell Res Ther. 2015, 6, 103. doi: 10.1186/s13287-015-0083-4 URL
87.	Randriantsilefisoa, R.; Hou, Y.; Pan, Y.; Camacho, J. L. C.; Kulka, M. W.; Zhang, J.; Haag, R. Interaction of human mesenchymal stem cells with soft nanocomposite hydrogels based on polyethylene glycol and dendritic polyglycerol. Adv Funct Mater. 2020, 30, 1905200. doi: 10.1002/adfm.v30.1 URL
88.	Lundin, V.; Sugden, W. W.; Theodore, L. N.; Sousa, P. M.; Han, A.; Chou, S.; Wrighton, P. J.; Cox, A. G.; Ingber, D. E.; Goessling, W.; Daley, G. Q.; North, T. E. YAP regulates hematopoietic stem cell formation in response to the biomechanical forces of blood flow. Dev Cell. 2020, 52, 446-460.e5.
89.	González-García, C.; Sousa, S. R.; Moratal, D.; Rico, P.; Salmerón-Sánchez, M. Effect of nanoscale topography on fibronectin adsorption, focal adhesion size and matrix organisation. Colloids Surf B Biointerfaces. 2010, 77, 181-190. doi: 10.1016/j.colsurfb.2010.01.021 URL
90.	Ross, E. A.; Turner, L. A.; Saeed, A.; Burgess, K. V.; Blackburn, G.; Reynolds, P.; Wells, J. A.; Mountford, J.; Gadegaard, N.; Salmeron-Sanchez, M.; Oreffo, R. O.; Dalby, M. J. Nanotopography reveals metabolites that maintain the immunosuppressive phenotype of mesenchymal stem cells. bioRxiv. 2019, 603332.
91.	Ngandu Mpoyi, E.; Cantini, M.; Reynolds, P. M.; Gadegaard, N.; Dalby, M. J.; Salmerón-Sánchez, M. Protein adsorption as a key mediator in the nanotopographical control of cell behavior. ACS Nano. 2016, 10, 6638-6647. doi: 10.1021/acsnano.6b01649 URL
92.	Luo, J.; Walker, M.; Xiao, Y.; Donnelly, H.; Dalby, M. J.; Salmeron-Sanchez, M. The influence of nanotopography on cell behaviour through interactions with the extracellular matrix - a review. Bioact Mater. 2021. doi: 10.1016/j.bioactmat.2021.11.024. doi: 10.1016/j.bioactmat.2021.11.024 URL
93.	Lei, R.; Kumar, S. Getting the big picture of cell-matrix interactions: High-throughput biomaterial platforms and systems-level measurements. Curr Opin Solid State Mater Sci. 2020, 24, 100871. doi: 10.1016/j.cossms.2020.100871 URL
94.	Yang, L.; Jurczak, K. M.; Ge, L.; van Rijn, P. High-throughput screening and hierarchical topography-mediated neural differentiation of mesenchymal stem cells. Adv Healthc Mater. 2020, 9, e2000117.

Nanotopographical surfaces	Structure features	Fabrication technique	Cellular effect
Static patterned surfaces	Nanopillar^{33, 35}	Ultraviolet-lithography, injection molding	Promote cells elongation and differentiation
	Nanopits³⁷	Colloidal lithography	Provide large surface traction forces to promote cell adhesion
	Nanopore³⁶	Anodization	Prohibit cell attachment and limit cell migration
	Nanospike⁴⁰	Photolithography	Enhance stem cell differentiation, secretion of growth factors
	Grooved surfaces^{43, 44}	Argon ion plasma, molding	Promote cell adhesion and proliferation
Dynamic patterned surfaces	Electro responsive, nanotubes to nanotips⁵⁰	Electrochemical polymerization	Dynamic attachment and detachment to mesenchymal stem cells
	Ultraviolet responsive, flat to rigid⁵¹	Spin coating	Induce cyclic cellular and nuclear stretches
	Thermoresponsive, flat to wrinkle⁵²	Ultraviolet polymerization and spin coating	Dynamic response of focal adhesion
Roughness	Gradient: 0.77–1.09 µm⁵⁶	Molding	Cellular attachment, F-actin arrangement
	High: 14.3 nm, low: 71 nm⁵⁷	Electrospinning	Cell morphology, metabolic activity
	Gradient: 200 nm–1.2 μm⁵⁹	Soft lithography	Enhance cell mechanosensing and osteogenic differentiation of mesenchymal stem cells

Nanotopographical surfaces	Structure features	Fabrication technique	Cellular effect
Static patterned surfaces	Nanopillar^{33, 35}	Ultraviolet-lithography, injection molding	Promote cells elongation and differentiation
	Nanopits³⁷	Colloidal lithography	Provide large surface traction forces to promote cell adhesion
	Nanopore³⁶	Anodization	Prohibit cell attachment and limit cell migration
	Nanospike⁴⁰	Photolithography	Enhance stem cell differentiation, secretion of growth factors
	Grooved surfaces^{43, 44}	Argon ion plasma, molding	Promote cell adhesion and proliferation
Dynamic patterned surfaces	Electro responsive, nanotubes to nanotips⁵⁰	Electrochemical polymerization	Dynamic attachment and detachment to mesenchymal stem cells
	Ultraviolet responsive, flat to rigid⁵¹	Spin coating	Induce cyclic cellular and nuclear stretches
	Thermoresponsive, flat to wrinkle⁵²	Ultraviolet polymerization and spin coating	Dynamic response of focal adhesion
Roughness	Gradient: 0.77–1.09 µm⁵⁶	Molding	Cellular attachment, F-actin arrangement
	High: 14.3 nm, low: 71 nm⁵⁷	Electrospinning	Cell morphology, metabolic activity
	Gradient: 200 nm–1.2 μm⁵⁹	Soft lithography	Enhance cell mechanosensing and osteogenic differentiation of mesenchymal stem cells

Stem cell type	Scaffold	Topographical features	Application
Mesenchymal stem cell	Polyesters⁶⁴	Nanograting or nanopillars	Cartilage regenerationNeurogenic differentiation
Mesenchymal stem cell	Fibrin hydrogel⁶⁵	Hierarchical aligned	Cartilage regenerationNeurogenic differentiation
Neural stem cell	Indium tin oxide-coated glass⁶⁹	Nanopore	Neuronal differentiation
	Silicon oxide surface⁷¹	Nanopillar arrays
	Polydimethylsiloxane⁶⁸	Nanowrinkle
Induced pluripotent stem cell	Glass surface⁷⁷	Random nanoscale structures	Neuronal differentiation
	Silk fibroin substrates⁷³	Anisotropic patterned	Cardiac regeneration
	Multielectrode arrays	Nanoarrays	Preclinical analysis of excitable cell function

Stem cell type	Scaffold	Topographical features	Application
Mesenchymal stem cell	Polyesters⁶⁴	Nanograting or nanopillars	Cartilage regenerationNeurogenic differentiation
Mesenchymal stem cell	Fibrin hydrogel⁶⁵	Hierarchical aligned	Cartilage regenerationNeurogenic differentiation
Neural stem cell	Indium tin oxide-coated glass⁶⁹	Nanopore	Neuronal differentiation
	Silicon oxide surface⁷¹	Nanopillar arrays
	Polydimethylsiloxane⁶⁸	Nanowrinkle
Induced pluripotent stem cell	Glass surface⁷⁷	Random nanoscale structures	Neuronal differentiation
	Silk fibroin substrates⁷³	Anisotropic patterned	Cardiac regeneration
	Multielectrode arrays	Nanoarrays	Preclinical analysis of excitable cell function

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[2]	Deepika Arora, Pamela Gehron Robey. Recent updates on the biological basis of heterogeneity in bone marrow stromal cells/skeletal stem cells [J]. Biomaterials Translational, 2022, 3(1): 3-16.
[3]	Suzanne M. Watt. The long and winding road: homeostatic and disordered haematopoietic microenvironmental niches: a narrative review [J]. Biomaterials Translational, 2022, 3(1): 31-54.
[4]	Emma Steijvers, Armaan Ghei, Zhidao Xia. Manufacturing artificial bone allografts: a perspective [J]. Biomaterials Translational, 2022, 3(1): 65-80.
[5]	Ke Hu, Yuxuan Li, Zunxiang Ke, Hongjun Yang, Chanjun Lu, Yiqing Li, Yi Guo, Weici Wang. History, progress and future challenges of artificial blood vessels: a narrative review [J]. Biomaterials Translational, 2022, 3(1): 81-98.
[6]	Peter W. Andrews. Human pluripotent stem cells: tools for regenerative medicine [J]. Biomaterials Translational, 2021, 2(4): 294-300.
[7]	Trivia P. Frazier, Katie Hamel, Xiying Wu, Emma Rogers, Haley Lassiter, Jordan Robinson, Omair Mohiuddin, Michael Henderson, Jeffrey M. Gimble. Adipose-derived cells: building blocks of three-dimensional microphysiological systems [J]. Biomaterials Translational, 2021, 2(4): 301-306.
[8]	Arnold I. Caplan. Mesenchymal stem cells and COVID-19: the process of discovery and of translation [J]. Biomaterials Translational, 2021, 2(4): 307-311.
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[13]	Yiqing Wang, Xiangyu Chu, Bing Wang. Recombinant adeno-associated virus-based gene therapy combined with tissue engineering for musculoskeletal regenerative medicine [J]. Biomaterials Translational, 2021, 2(1): 19-29.
[14]	Isak Jatoi, Jingyu Fan. A biomaterials viewpoint for the 2020 SARS-CoV-2 vaccine development [J]. Biomaterials Translational, 2021, 2(1): 30-42.
[15]	Xing Yang, Yuanyuan Li, Xujie Liu, Wei He, Qianli Huang, Qingling Feng. Nanoparticles and their effects on differentiation of mesenchymal stem cells [J]. Biomaterials Translational, 2020, 1(1): 58-68.

An update of nanotopographical surfaces in modulating stem cell fate: a narrative review

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