·
REVIEW
·

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

Shuqin Cao1 Quan Yuan1*
Show Less
1 State Key Laboratory of Oral Diseases, National Clinical Research Centre for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan Province, China
Submitted: 24 January 2022 | Revised: 6 March 2022 | Accepted: 10 March 2022 | Published: 28 March 2022
Copyright © 2022 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution–NonCommercial–ShareAlike 4.0 License.
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.

Keywords
biomaterials
mechanotransduction
nanotopographical surfaces
stem cell
tissue regeneration
References

Below is the content of the Citations in the paper which has been de-formatted, however, the content stays consistent with the original.

感谢您提供的文献列表。以下是您所列的文献引用:

1. Bianco, P.; Robey, P. G. Stem cells in tissue engineering. *Nature*. 2001, 414, 118-121.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.

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.

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.

21. Ripamonti, U. Functionalized surface geometries induce: “bone: formation by autoinduction”. *Front Physiol*. 2017, 8, 1084.

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.

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.

25. Xia, Y.; Whitesides, G. M. Soft lithography. *Annu Rev Mater Sci*. 1998, 28, 153-184.

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.

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.

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.

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.

30. Basnar, B.; Willner, I. Dip-pen-nanolithographic patterning of metallic, semiconductor, and metal oxide nanostructures on surfaces. *Small*. 2009, 5, 28-44.

31. Norman, J. J.; Desai, T. A. Methods for fabrication of nanoscale topography for tissue engineering scaffolds. *Ann Biomed Eng*. 2006, 34, 89-101.

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.

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.

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.

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.

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.

39. Kim, H. J. Regulation of neural stem cell fate by natural products. *Biomol Ther (Seoul)*. 2019, 27, 15-24.

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.

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.

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.

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.

45. Leclech, C.; Villard, C. Cellular and subcellular contact guidance on microfabricated substrates. *Front Bioeng Biotechnol*. 2020, 8, 551505.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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*. 2009, 106, 2130-2135.

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.

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.

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.

以下是您提供的文献引用的完整列表:

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

81. Salsmann, A.; Schaffner-Reckinger, E.; Kieffer, N. RGD, the Rho’d to cell spreading. *Eur J Cell Biol*. 2006, 85, 249-254.

82. Berrier, A. L.; Yamada, K. M. Cell-matrix adhesion. *J Cell Physiol*. 2007, 213, 565-573.93. 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. 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.

83. Wehrle-Haller, B. Structure and function of focal adhesions. *Curr Opin Cell Biol*. 2012, 24, 116-124.

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.

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.

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.

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.

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.

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.

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.

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.

Conflict of interest
The authors declare they have no competing interests.
Share
Back to top