Topographic Cues Guiding Cell Polarization via Distinct Cellular Mechanosensing Pathways
Wei Liu
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorQian Sun
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorZi-Li Zheng
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorYa-Ting Gao
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorGuan-Yin Zhu
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, 610041 China
Search for more papers by this authorCorresponding Author
Qiang Wei
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
College of Biomedical Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Jia-Zhuang Xu
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorZhong-Ming Li
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorChang-Sheng Zhao
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
College of Biomedical Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorWei Liu
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorQian Sun
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorZi-Li Zheng
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorYa-Ting Gao
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorGuan-Yin Zhu
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, 610041 China
Search for more papers by this authorCorresponding Author
Qiang Wei
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
College of Biomedical Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Jia-Zhuang Xu
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorZhong-Ming Li
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorChang-Sheng Zhao
State Key Laboratory of Polymer Materials and Engineering, College of Polymer Science and Engineering, Sichuan University, Chengdu, 610065 China
College of Biomedical Engineering, Sichuan University, Chengdu, 610065 China
Search for more papers by this authorAbstract
Cell polarization exists in a variety of tissues to regulate cell behaviors and functions. Space constraint (spatially limiting cell extension) and adhesion induction (guiding adhesome growth) are two main ways to induce cell polarization according to the microenvironment topographies. However, the mechanism of cell polarization induced by these two ways and the downstream effects on cell functions are yet to be understood. Here, space constraint and adhesion induction guiding cell polarization are achieved by substrate groove arrays in micro and nano size, respectively. Although the morphology of polarized cells is similar on both structures, the signaling pathways to induce the cell polarization and the downstream functions are distinctly different. The adhesion induction (nano-groove) leads to the formation of focal adhesions and activates the RhoA/ROCK pathway to enhance the myosin-based intracellular force, while the space constraint (micro-groove) only activates the formation of pseudopodia. The enhanced intracellular force caused by adhesion induction inhibits the chromatin condensation, which promotes the osteogenic differentiation of stem cells. This study presents an overview of cell polarization and mechanosensing at biointerface to aid in the design of novel biomaterials.
Conflict of Interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
Research data are not shared.
Supporting Information
| Filename | Description |
|---|---|
| smll202104328-sup-0001-SuppMat.pdf1.1 MB | Supporting Information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1E. Karzbrun, A. Kshirsagar, S. R. Cohen, J. H. Hanna, O. Reiner, Nat. Phys. 2018, 14, 515.
- 2Z. G. Zhao, R. C. Fang, Q. F. Rong, M. J. Liu, Adv. Mater. 2017, 29, 16.
- 3M. A. Pickett, V. F. Naturale, J. L. Feldman, in Annual Review of Cell and Developmental Biology, Vol. 35 (Ed: R. Lehmann), Annual Reviews, Palo Alto 2019, p. 285.
- 4I. Yanakieva, A. Erzberger, M. Matejcic, C. D. Modes, C. Norden, J. Cell Biol. 2019, 218, 3272.
- 5T. Fujimori, A. Nakajima, N. Shimada, S. Sawai, Proc. Natl. Acad. Sci. U. S. A. 2019, 116, 4291.
- 6H. Aubin, J. W. Nichol, C. B. Hutson, H. Bae, A. L. Sieminski, D. M. Cropek, P. Akhyari, A. Khademhosseini, Biomaterials 2010, 31, 6941.
- 7D. H. Kim, A. J. Ewald, J. Park, Kshitiz, M. Kwak, R. S. Gray, C. Y. Su, J. Seo, S. S. An, A. Levchenko, Sci. Rep. 2018, 8, 10.
- 8D. Docheva, S. A. Müller, M. Majewski, C. H. Evans, Adv. Drug Deliv. Rev. 2015, 84, 222.
- 9D. Park, E. Wershof, S. Boeing, A. Labernadie, R. P. Jenkins, S. George, X. Trepat, P. A. Bates, E. Sahai, Nat. Mater. 2020, 19, 227.
- 10M. Nebuloni, L. Albarello, A. Andolfo, C. Magagnotti, L. Genovese, I. Locatelli, G. Tonon, E. Longhi, P. Zerbi, R. Allevi, A. Podestà, L. Puricelli, P. Milani, A. Soldarini, A. Salonia, M. Alfano, Sci. Rep. 2016, 6, 22522.
- 11Y. H. Li, G. Y. Huang, X. H. Zhang, L. Wang, Y. A. Du, T. J. Lu, F. Xu, Biotechnol. Adv. 2014, 32, 347.
- 12H. Kang, S. H. D. Wong, Q. Pan, G. Li, L. Bian, Nano Lett. 2019, 19, 1963.
- 13X. Yao, R. Peng, J. Ding, Adv. Mater. 2013, 25, 5257.
- 14A. Ray, O. Lee, Z. Win, R. M. Edwards, P. W. Alford, D. H. Kim, P. P. Provenzano, Nat. Commun. 2017, 8, 17.
- 15S. Qiu, J. Ji, W. Sun, J. Pei, J. He, Y. Li, J. J. Li, G. Wang, Smart Mater. Med. 2021, 2, 65.
10.1016/j.smaim.2020.12.002 Google Scholar
- 16M. Ding, H. Andersson, S. Martinsson, A. Sabirsh, A. Jonebring, Q.-D. Wang, A. T. Plowright, L. Drowley, Sci. Rep. 2020, 10, 13575.
- 17M. A. Bucaro, Y. Vasquez, B. D. Hatton, J. Aizenberg, ACS Nano 2012, 6, 6222.
- 18F. Greco, T. Fujie, L. Ricotti, S. Taccola, B. Mazzolai, V. Mattoli, ACS Appl. Mater. Interfaces 2013, 5, 573.
- 19A. F. Adler, A. T. Speidel, N. Christoforou, K. Kolind, M. Foss, K. W. Leong, Biomaterials 2011, 32, 3611.
- 20M. Wang, B. Cheng, Y. W. Yang, H. Liu, G. Y. Huang, L. C. Han, F. Li, F. Xu, Nano Lett. 2019, 19, 5949.
- 21J. Zou, S. Q. Wu, J. Chen, X. J. Lei, Q. H. Li, H. Yu, S. Tang, D. D. Ye, Adv. Mater. 2019, 31, 8.
- 22A. M. Y. Shum, H. Che, A. O. T. Wong, C. Z. Zhang, H. K. Wu, C. W. Y. Chan, K. Costa, M. Khine, C. W. Kong, R. A. Li, Adv. Mater. 2017, 29, 1602448.
- 23J. M. Dang, K. W. Leong, Adv. Mater. 2007, 19, 2775.
- 24J. Ren, Q. F. Xu, X. M. Chen, W. Li, K. Guo, Y. Zhao, Q. Wang, Z. T. Zhang, H. S. Peng, Y. G. Li, Adv. Mater. 2017, 29, 8.
- 25Z. Zhang, Y. Fu, W. Yu, X. Y. Qin, Z. J. Xue, Y. Liu, D. Luo, C. Yan, X. H. Sun, T. Wang, Adv. Mater. 2016, 28, 9589.
- 26K. H. Vining, D. J. Mooney, Nat. Rev. Mol. Cell Biol. 2017, 18, 728.
- 27L. He, G. Si, J. H. Huang, A. D. T. Samuel, N. Perrimon, Nature 2018, 555, 103.
- 28V. Vogel, M. Sheetz, Nat. Rev. Mol. Cell Biol. 2006, 7, 265.
- 29H. Kang, B. Yang, K. Zhang, Q. Pan, W. Yuan, G. Li, L. Bian, Nat. Commun. 2019, 10, 1696.
- 30M. Zhang, C. Li, S. Yang, J. Hirte, W. Zhao, Q. Wei, Z. Diao, J. P. Spatz, C. Zhao, Smart Mater. Med. 2021, 2, 38.
10.1016/j.smaim.2020.10.001 Google Scholar
- 31Q. Wei, A. Holle, J. Li, F. Posa, F. Biagioni, O. Croci, A. S. Benk, J. Young, F. Noureddine, J. Deng, M. Zhang, G. J. Inman, J. P. Spatz, S. Campaner, E. A. Cavalcanti-Adam, Adv. Sci. 2020, 7, 15.
- 32H. Kang, K. Zhang, H. J. Jung, B. Yang, X. Chen, Q. Pan, R. Li, X. Xu, G. Li, V. P. Dravid, L. Bian, Adv. Mater. 2018, 30, 1803591.
- 33Q. Sun, Q. Wei, C. S. Zhao, Chin. Sci. Bull. 2021, 66, 2303.
- 34E. Rebollar, I. Frischauf, M. Olbrich, T. Peterbauer, S. Hering, J. Preiner, P. Hinterdorfer, C. Romanin, J. Heitz, Biomaterials 2008, 29, 1796.
- 35K. A. Kilian, B. Bugarija, B. T. Lahn, M. Mrksich, Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 4872.
- 36W. Liu, H. M. Yin, A. Shi, W. J. Sun, D. W. Wu, S. S. Huang, B. S. Zhao, J. Z. Xu, Z. M. Li, Macromolecules 2020, 53, 1736.
- 37J. Deng, C. S. Zhao, J. P. Spatz, Q. Wei, ACS Nano 2017, 11, 8282.
- 38R. Changede, H. Cai, S. J. Wind, M. P. Sheetz, Nat. Mater. 2019, 18, 1366.
- 39J. H. Wen, L. G. Vincent, A. Fuhrmann, Y. S. Choi, K. C. Hribar, H. Taylor-Weiner, S. Chen, A. J. Engler, Nat. Mater. 2014, 13, 979.
- 40Q. Wei, T. Becherer, S. Angioletti-Uberti, J. Dzubiella, C. Wischke, A. T. Neffe, A. Lendlein, M. Ballauff, R. Haag, Angew. Chem., Int. Ed. 2014, 53, 8004.
- 41W. Qiang, R. Haag, Mater. Horiz. 2015, 2, 567.
- 42K. Riento, A. J. Ridley, Nat. Rev. Mol. Cell Biol. 2003, 4, 446.
- 43L. X. Yu, Y. Hou, W. Y. Xie, J. L. C. Camacho, C. Cheng, A. Holle, J. Young, B. Trappmann, W. F. Zhao, M. F. Melzig, E. A. Cavalcanti-Adam, C. S. Zhao, J. P. Spatz, Q. Wei, R. Haag, Adv. Mater. 2020, 32, 12.
- 44N. O. Alieva, A. K. Efremov, S. Hu, D. Oh, Z. Chen, M. Natarajan, H. T. Ong, A. Jegou, G. Romet-Lemonne, J. T. Groves, M. P. Sheetz, J. Yan, A. D. Bershadsky, Nat. Commun. 2019, 10, 14.
- 45B. Geiger, J. P. Spatz, A. D. Bershadsky, Nat. Rev. Mol. Cell Biol. 2009, 10, 21.
- 46T. G. Kapp, F. Rechenmacher, S. Neubauer, O. V. Maltsev, E. A. Cavalcanti-Adam, R. Zarka, U. Reuning, J. Notni, H. J. Wester, C. Mas-Moruno, J. Spatz, B. Geiger, H. Kessler, Sci. Rep. 2017, 7, 13.
- 47J. Swift, I. L. Ivanovska, A. Buxboim, T. Harada, P. Dingal, J. Pinter, J. D. Pajerowski, K. R. Spinler, J. W. Shin, M. Tewari, F. Rehfeldt, D. W. Speicher, D. E. Discher, Science 2013, 341, 1240104.
- 48S.-J. Heo, T. P. Driscoll, S. D. Thorpe, N. L. Nerurkar, B. M. Baker, M. T. Yang, C. S. Chen, D. A. Lee, R. L. Mauck, Elife 2016, 5, e18207.
- 49Y. Hou, W. Y. Xie, L. X. Yu, L. C. Camacho, C. X. Nie, M. Zhang, R. Haag, Q. Wei, Small 2020, 16, 10.
- 50M. D. Cabezas, B. Meckes, C. A. Mirkin, M. Mrksich, ACS Nano 2019, 13, 11144.
- 51A. Elosegui-Artola, X. Trepat, P. Roca-Cusachs, Trends Cell Biol. 2018, 28, 356.
- 52Z. Q. Sun, M. Costell, R. Fassler, Nat. Cell Biol. 2019, 21, 25.
- 53S. Huveneers, E. H. J. Danen, J. Cell Sci. 2009, 122, 1059.
- 54Y. Hou, L. Yu, W. Xie, L. C. Camacho, M. Zhang, Z. Chu, Q. Wei, R. Haag, Nano Lett. 2020, 20, 748.
- 55H. Wolfenson, B. Yang, M. P. Sheetz, in Annual Review of Physiology, Vol. 81 (Eds: M. T. Nelson, K. Walsh), Annual Reviews, Palo Alto 2019, p. 585.
- 56S. H. D. Wong, B. Yin, B. Yang, S. Lin, R. Li, Q. Feng, H. Yang, L. Zhang, Z. Yang, G. Li, C. H. J. Choi, L. Bian, Adv. Funct. Mater. 2019, 29, 1806822.
- 57J.-K. Kim, A. Louhghalam, G. Lee, B. W. Schafer, D. Wirtz, D.-H. Kim, Nat. Commun. 2017, 8, 2123.
- 58A. R. Killaars, C. J. Walker, K. S. Anseth, Proc. Natl. Acad. Sci. U. S. A. 2020, 117, 21258.
- 59A. J. Engler, S. Sen, H. L. Sweeney, D. E. Discher, Cell 2006, 126, 677.
- 60N. Huebsch, P. R. Arany, A. S. Mao, D. Shvartsman, O. A. Ali, S. A. Bencherif, J. Rivera-Feliciano, D. J. Mooney, Nat. Mater. 2010, 9, 518.
