Review
Recent Advances in DNA-Templated Protein Patterning
Qinglin Xia,
Mo Zhou,
Kai Jiao,
Bin Li,
Linjie Guo,
Lihua Wang,
Jiang Li,
Qinglin Xia
Division of Physical Biology, CAS Key Laboratory of Interfacial Physics and Technology, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, 201800 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Search for more papers by this authorMo Zhou
Division of Physical Biology, CAS Key Laboratory of Interfacial Physics and Technology, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, 201800 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Zhangjiang Laboratory, 100 Haike Road, Shanghai, 201210 China
Search for more papers by this authorKai Jiao
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
Search for more papers by this authorBin Li
Division of Physical Biology, CAS Key Laboratory of Interfacial Physics and Technology, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, 201800 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Search for more papers by this authorCorresponding Author
Linjie Guo
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorLihua Wang
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
Search for more papers by this authorCorresponding Author
Jiang Li
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorQinglin Xia,
Mo Zhou,
Kai Jiao,
Bin Li,
Linjie Guo,
Lihua Wang,
Jiang Li,
Qinglin Xia
Division of Physical Biology, CAS Key Laboratory of Interfacial Physics and Technology, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, 201800 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Search for more papers by this authorMo Zhou
Division of Physical Biology, CAS Key Laboratory of Interfacial Physics and Technology, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, 201800 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Zhangjiang Laboratory, 100 Haike Road, Shanghai, 201210 China
Search for more papers by this authorKai Jiao
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
Search for more papers by this authorBin Li
Division of Physical Biology, CAS Key Laboratory of Interfacial Physics and Technology, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, 201800 China
University of Chinese Academy of Sciences, Beijing, 100049 China
Search for more papers by this authorCorresponding Author
Linjie Guo
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorLihua Wang
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
Search for more papers by this authorCorresponding Author
Jiang Li
Institute of Materiobiology, College of Sciences, Shanghai University, Shanghai, 200444 China
E-mail: [email protected]; [email protected]
Search for more papers by this authorAbstract
In recent decades, the advancement of DNA nanotechnology enables precise nanoscale organization of diverse functional materials with DNA templates. Particularly, a variety of DNA-templated protein patterns are constructed as powerful tools for programming biomimetic protein complexes. In this review, recent progress in DNA-templated protein patterning, including cutting-edge methods for arranging proteins with DNA templates, and protein patterns across varying dimensions are briefly summarized. Representative applications in biological analysis and biomedicine are discussed. DNA-protein patterns with programmable dynamics, which hold promise in precision diagnosis and therapeutics are highlighted. Finally, current challenges and opportunities in the fabrication and application of DNA-templated protein pattering are discussed.
Conflict of Interest
The authors declare no conflict of interest.
References
- 1P. Zhu, J. Liu, J. Bess, E. Chertova, J. D. Lifson, H. Grisé, G. A. Ofek, K. A. Taylor, K. H. Roux, Nature 2006, 441, 847.
- 2H. Yao, Y. Song, Y. Chen, N. Wu, J. Xu, C. Sun, J. Zhang, T. Weng, Z. Zhang, Z. Wu, L. Cheng, D. Shi, X. Lu, J. Lei, M. Crispin, Y. Shi, L. Li, S. Li, Cell 2020, 183, 730.
- 3Q. Wang, T. Wang, L. Cao, A. Mu, S. Fu, P. Wang, Y. Gao, W. Ji, Z. Liu, Z. Du, L. W. Guddat, W. Zhang, S. Li, X. Li, Z. Lou, X. Wang, Z. Hu, Z. Rao, Science 2024, 385, 1217.
- 4M. I. Rosenbaum, L. S. Clemmensen, D. S. Bredt, B. Bettler, K. Strømgaard, Nat. Rev. Drug Discovery 2020, 19, 884.
- 5J. C. Kagan, V. G. Magupalli, H. Wu, Nat. Rev. Immunol. 2014, 14, 821.
- 6N. E. Chayen, E. Saridakis, Nat. Methods 2008, 5, 147.
- 7Y. Bai, Q. Luo, J. Liu, Chem. Soc. Rev. 2016, 45, 2756.
- 8B. J. G. E. Pieters, M. B. Van Eldijk, R. J. M. Nolte, J. Mecinović, Chem. Soc. Rev. 2016, 45, 24.
- 9F. L. Sendker, Y. K. Lo, T. Heimerl, S. Bohn, L. J. Persson, C. N. Mais, W. Sadowska, N. Paczia, E. Nussbaum, M. D. S. Olmos, K. Forchhammer, D. Schindler, T. J. Erb, J. L. P. Benesch, E. G. Marklund, G. Bange, J. M. Schuller, G. K. A. Hochberg, Nature 2024, 628, 894.
- 10S. Gonen, F. Dimaio, T. Gonen, D. Baker, Science 2015, 348, 1365.
- 11J. B. Bale, S. Gonen, Y. Liu, W. Sheffler, D. Ellis, C. Thomas, D. Cascio, T. O. Yeates, T. Gonen, N. P. King, D. Baker, Science 2016, 353, 389.
- 12P.-S. Huang, S. E. Boyken, D. Baker, Nature 2016, 537, 320.
- 13W. D. Liu, Y. F. Li, B. Yang, Sci. China Chem. 2013, 56, 1087.
- 14E. Menard, M. A. Meitl, Y. G. Sun, J. U. Park, D. J. L. Shir, Y. S. Nam, S. Jeon, J. A. Rogers, Chem. Rev. 2007, 107, 1117.
- 15A. del Campo, E. Arzt, Chem. Rev. 2008, 108, 911.
- 16M. J. Mitchell, M. M. Billingsley, R. M. Haley, M. E. Wechsler, N. A. Peppas, R. Langer, Nat. Rev. Drug Discovery 2021, 20, 101.
- 17E. R. Brannon, M. V. Guevara, N. J. Pacifici, J. K. Lee, J. S. Lewis, O. Eniola-Adefeso, Nat. Rev. Mater. 2022, 7, 796.
- 18M. M. Rahman, J. Wang, G. S. Wang, Z. P. Su, Y. Z. Li, Y. D. Chen, J. G. Meng, Y. Yao, L. F. Wang, S. Wilkens, J. F. Tan, J. T. Luo, T. Zhang, C. D. Zhu, S. H. Cho, L. X. Wang, L. P. Lee, Y. Wan, Nat. Nanotechnol. 2024, 19, 818.
- 19G. Georgiou, C. Stathopoulos, P. S. Daugherty, A. R. Nayak, B. L. Iverson, R. Curtiss 3rd, Nat. Biotechnol. 1997, 15, 29.
- 20S. J. Draper, J. L. Heeney, Nat. Rev. Microbiol. 2010, 8, 62.
- 21C. McMahon, A. S. Baier, R. Pascolutti, M. Wegrecki, S. Zheng, J. X. Ong, S. C. Erlandson, D. Hilger, S. G. F. Rasmussen, A. M. Ring, A. Manglik, A. C. Kruse, Nat. Struct. Mol. Biol. 2018, 25, 289.
- 22S. Dey, C. Fan, K. V. Gothelf, J. Li, C. Lin, L. Liu, N. Liu, M. A. D. Nijenhuis, B. Saccà, F. C. Simmel, H. Yan, P. Zhan, Nat. Rev. Methods Primers 2021, 1, 13.
- 23Y. R. Yang, Y. Liu, H. Yan, Bioconjugate Chem. 2015, 26, 1381.
- 24N. Stephanopoulos, Chem 2020, 6, 364.
- 25G. Z. Kong, M. Y. Xiong, L. Liu, L. Hu, H. M. Meng, G. L. Ke, X. B. Zhang, W. H. Tan, Chem. Soc. Rev. 2021, 50, 1846.
- 26G. A. Knappe, E. C. Wamhoff, M. Bathe, Nat. Rev. Mater. 2023, 8, 123.
- 27N. C. Seeman, J. Theor. Biol. 1982, 99, 237.
- 28A. Heuer-Jungemann, T. Liedl, Trends Chem. 2019, 1, 799.
- 29P. W. K. Rothemund, Nature 2006, 440, 297.
- 30F. Hong, F. Zhang, Y. Liu, H. Yan, Chem. Rev. 2017, 117, 12584.
- 31B. Wei, M. J. Dai, P. Yin, Nature 2012, 485, 623.
- 32N. C. Seeman, H. F. Sleiman, Nat. Rev. Mater. 2018, 3, 17068.
- 33S. M. Douglas, H. Dietz, T. Liedl, B. Högberg, F. Graf, W. M. Shih, Nature 2009, 459, 414.
- 34Y. G. Ke, L. L. Ong, W. M. Shih, P. Yin, Science 2012, 338, 1177.
- 35P. K. Lo, P. Karam, F. A. Aldaye, C. K. McLaughlin, G. D. Hamblin, G. Cosa, H. F. Sleiman, Nat. Chem. 2010, 2, 319.
- 36S. M. Douglas, I. Bachelet, G. M. Church, Science 2012, 335, 831.
- 37H. Yan, S. H. Park, G. Finkelstein, J. H. Reif, T. H. LaBean, Science 2003, 301, 1882.
- 38L. Li, J. Yin, W. Ma, L. G. Tang, J. H. Zou, L. Z. Yang, T. Du, Y. Zhao, L. H. Wang, Z. Yang, C. H. Fan, J. Chao, X. Y. Chen, Nat. Mater. 2024, 23, 993.
- 39J. Yin, S. Y. Wang, J. H. Wang, Y. W. Zhang, C. H. Fan, J. Chao, Y. Gao, L. H. Wang, Nat. Mater. 2024, 23, 854.
- 40G. A. Knappe, E. C. Wamhoff, B. J. Read, D. J. Irvine, M. Bathe, ACS Nano 2021, 15, 14316.
- 41Y. Wang, I. Baars, F. Fordos, B. Hogberg, ACS Nano 2021, 15, 9614.
- 42E.-C. Wamhoff, L. Ronsard, J. Feldman, G. A. Knappe, B. M. Hauser, A. Romanov, J. B. Case, S. Sanapala, E. C. Lam, K. J. S. Denis, J. Boucau, A. K. Barczak, A. B. Balazs, M. S. Diamond, A. G. Schmidt, D. Lingwood, M. Bathe, Nat. Commun. 2024, 15, 795.
- 43B. J. H. M. Rosier, A. J. Markvoort, B. Gumí Audenis, J. A. L. Roodhuizen, A. Den Hamer, L. Brunsveld, T. F. A. De Greef, Nat. Catal. 2020, 3, 295.
- 44N. Stephanopoulos, M. H. Liu, G. J. Tong, Z. Li, Y. Liu, H. Yan, M. B. Francis, Nano Lett. 2010, 10, 2714.
- 45Q. Shen, T. Tian, Q. Xiong, P. D. Ellis Fisher, Y. Xiong, T. J. Melia, C. P. Lusk, C. Lin, J. Am. Chem. Soc. 2021, 143, 12294.
- 46Q. Shen, Q. Feng, C. Wu, Q. Xiong, T. Tian, S. Yuan, J. Shi, G. J. Bedwell, R. Yang, C. Aiken, A. N. Engelman, C. P. Lusk, C. Lin, Y. Xiong, Nat. Struct. Mol. Biol. 2023, 30, 425.
- 47B. Sacca, R. Meyer, M. Erkelenz, K. Kiko, A. Arndt, H. Schroeder, K. S. Rabe, C. M. Niemeyer, Angew. Chem., Int. Ed. 2010, 49, 9378.
- 48N. D. Derr, B. S. Goodman, R. Jungmann, A. E. Leschziner, W. M. Shih, S. L. Reck-Peterson, Science 2012, 338, 662.
- 49R. Veneziano, T. J. Moyer, M. B. Stone, E.-C. Wamhoff, B. J. Read, S. Mukherjee, T. R. Shepherd, J. Das, W. R. Schief, D. J. Irvine, M. Bathe, Nat. Nanotechnol. 2020, 15, 716.
- 50J. Hellmeier, R. Platzer, V. Muhlgrabner, M. C. Schneider, E. Kurz, G. J. Schutz, J. B. Huppa, E. Sevcsik, ACS Nano 2021, 15, 15057.
- 51H. J. Liu, T. Torring, M. D. Dong, C. B. Rosen, F. Besenbacher, K. V. Gothelf, J. Am. Chem. Soc. 2010, 132, 18054.
- 52N. V. Voigt, T. Torring, A. Rotaru, M. F. Jacobsen, J. B. Ravnsbaek, R. Subramani, W. Mamdouh, J. Kjems, A. Mokhir, F. Besenbacher, K. V. Gothelf, Nat. Nanotechnol. 2010, 5, 200.
- 53Y. Zhang, F. Wang, J. Chao, M. Xie, H. Liu, M. Pan, E. Kopperger, X. Liu, Q. Li, J. Shi, L. Wang, J. Hu, L. Wang, F. C. Simmel, C. Fan, Nat. Commun. 2019, 10, 5469.
- 54P. Zhang, X. Liu, P. Liu, F. Wang, H. Ariyama, T. Ando, J. Lin, L. Wang, J. Hu, B. Li, C. Fan, Nat. Commun. 2020, 11, 3114.
- 55L. Abendstein, W. E. M. Noteborn, L. S. Veenman, D. J. Dijkstra, F. S. van de Bovenkamp, L. A. Trouw, T. H. Sharp, J. Am. Chem. Soc. 2024, 146, 13455.
- 56A. Shaw, I. T. Hoffecker, I. Smyrlaki, J. Rosa, A. Grevys, D. Bratlie, I. Sandlie, T. E. Michaelsen, J. T. Andersen, B. Hogberg, Nat. Nanotechnol. 2019, 14, 184.
- 57S. Zhao, R. Tian, J. Wu, S. Liu, Y. Wang, M. Wen, Y. Shang, Q. Liu, Y. Li, Y. Guo, Z. Wang, T. Wang, Y. Zhao, H. Zhao, H. Cao, Y. Su, J. Sun, Q. Jiang, B. Ding, Nat. Commun. 2021, 12, 358.
- 58A. A. Rafat, S. Sagredo, M. Thalhammer, F. C. Simmel, Nat. Chem. 2020, 12, 852.
- 59E. Nakata, F. F. Liew, C. Uwatoko, S. Kiyonaka, Y. Mori, Y. Katsuda, M. Endo, H. Sugiyama, T. Morii, Angew. Chem., Int. Ed. 2012, 51, 2421.
- 60F. Praetorius, H. Dietz, Science 2017, 355, 8.
- 61F. Wang, Y. Y. Hao, Q. Li, J. Li, H. L. Zhang, X. L. Zhang, L. H. Wang, C. Bustamante, C. H. Fan, Sci. Adv. 2020, 6, eaay9948.
- 62I. Seitz, S. Saarinen, E.-P. Kumpula, D. McNeale, E. Anaya-Plaza, V. Lampinen, V. P. Hytönen, F. Sainsbury, J. J. L. M. Cornelissen, V. Linko, J. T. Huiskonen, M. A. Kostiainen, Nat. Nanotechnol. 2023, 18, 1205.
- 63K. L. Wark, P. J. Hudson, Adv. Drug Delivery Rev. 2006, 58, 657.
- 64K. L. Mpye, S. Gildenhuys, S. Mosebi, AIMS Biophys. 2020, 7, 236.
- 65M. R. Dunn, R. M. Jimenez, J. C. Chaput, Nat. Rev. Chem. 2017, 1, 0076.
- 66Y. Liu, C. X. Lin, H. Y. Li, H. Yan, Angew. Chem., Int. Ed. 2005, 44, 4333.
- 67Y. Fu, D. Zeng, J. Chao, Y. Jin, Z. Zhang, H. Liu, D. Li, H. Ma, Q. Huang, K. V. Gothelf, C. Fan, J. Am. Chem. Soc. 2013, 135, 696.
- 68L. Sun, Y. Gao, Y. Xu, J. Chao, H. Liu, L. Wang, D. Li, C. Fan, J. Am. Chem. Soc. 2017, 139, 17525.
- 69Y. Suzuki, M. Endo, H. Sugiyama, Nat. Commun. 2015, 6, 8052.
- 70R. Chhabra, J. Sharma, Y. G. Ke, Y. Liu, S. Rinker, S. Lindsay, H. Yan, J. Am. Chem. Soc. 2007, 129, 10304.
- 71R. F. Hariadi, R. F. Sommese, A. S. Adhikari, R. E. Taylor, S. Sutton, J. A. Spudich, S. Sivaramakrishnan, Nat. Nanotechnol. 2015, 10, 696.
- 72I. Smyrlaki, F. Fördős, I. Rocamonde-Lago, Y. Wang, B. Shen, A. Lentini, V. C. Luca, B. Reinius, A. I. Teixeira, B. Högberg, Nat. Commun. 2024, 15, 465.
- 73M. N. Rushdi, V. Pan, K. Li, H.-K. Choi, S. Travaglino, J. Hong, F. Griffitts, P. Agnihotri, R. A. Mariuzza, Y. Ke, C. Zhu, Nat. Commun. 2022, 13, 7055.
- 74S. H. Park, P. Yin, Y. Liu, J. H. Reif, T. H. LaBean, H. Yan, Nano Lett. 2005, 5, 729.
- 75B. A. R. Williams, K. Lund, Y. Liu, H. Yan, J. C. Chaput, Angew. Chem., Int. Ed. 2007, 46, 3051.
- 76J. D. Cohen, J. P. Sadowski, P. B. Dervan, J. Am. Chem. Soc. 2008, 130, 402.
- 77W. Li, C. Wang, H. Lv, Z. Wang, M. Zhao, S. Liu, L. Gou, Y. Zhou, J. Li, J. Zhang, L. Li, Y. Wang, P. Lou, L. Wu, L. Zhou, Y. Chen, Y. Lu, J. Cheng, Y.-P. Han, Q. Cao, W. Huang, N. Tong, X. Fu, J. Liu, X. Zheng, P.-O. Berggren, ACS Nano 2021, 15, 18237.
- 78L. Schneider, K. S. Rabe, C. M. Domínguez, C. M. Niemeyer, ACS Nano 2023, 17, 6719.
- 79R. F. Hariadi, M. Cale, S. Sivaramakrishnan, Proc. Natl. Acad. Sci. 2014, 111, 4091.
- 80M. García-Chamé, P. Wadhwani, J. Pfeifer, U. Schepers, C. M. Niemeyer, C. M. Domínguez, Angew. Chem., Int. Ed. 2024, 63, 202318805.
- 81L. Yu, Y. Xu, M. Al-Amin, S. Jiang, M. Sample, A. Prasad, N. Stephanopoulos, P. Sulc, H. Yan, J. Am. Chem. Soc. 2023, 145, 27336.
- 82Y. Y. Sun, L. Yan, J. J. Sun, M. S. Xiao, W. Lai, G. Q. Song, L. Li, C. H. Fan, H. Pei, Nat. Commun. 2022, 13, 3916.
- 83Y. Sun, J. Sun, M. Xiao, W. Lai, L. Li, C. Fan, H. Pei, Sci. Adv. 2022, 8, eadd1106.
- 84Y. X. Ma, Q. Wang, S. Y. Du, J. W. Luo, X. L. Sun, B. Jia, J. R. Ge, J. Dong, S. X. Jiang, Z. Li, ACS Nano 2024, 18, 5418.
- 85Y. C. Zeng, O. J. Young, C. M. Wintersinger, F. M. Anastassacos, J. I. Macdonald, G. Isinelli, M. O. Dellacherie, M. Sobral, H. Bai, A. R. Graveline, A. Vernet, M. Sanchez, K. Mulligan, Y. Choi, T. C. Ferrante, D. B. Keskin, G. G. Fell, D. Neuberg, C. J. Wu, D. J. Mooney, I. C. Kwon, J. H. Ryu, W. M. Shih, Nat. Nanotechnol. 2024, 19, 1055.
- 86C. Geary, G. Grossi, E. K. S. McRae, P. W. K. Rothemund, E. S. Andersen, Nat. Chem. 2021, 13, 549.
- 87M. T. A. Nguyen, G. Pothoulakis, E. S. Andersen, ACS Synth. Biol. 2022, 11, 1710.
- 88T. B. Nielsen, R. P. Thomsen, M. R. Mortensen, J. Kjems, P. F. Nielsen, T. E. Nielsen, A. L. B. Kodal, E. Cló, K. V. Gothelf, Angew. Chem., Int. Ed. 2019, 58, 9068.
- 89F. Y. Shen, Z. J. Xiong, Y. M. Wu, R. Peng, Y. Wang, L. L. Sun, C. H. Fan, Z. Liu, Angew. Chem., Int. Ed. 2023, 62, 202301147.
- 90P. Ketterer, A. N. Ananth, D. S. L. Trip, A. Mishra, E. Bertosin, M. Ganji, J. van der Torre, P. Onck, H. Dietz, C. Dekker, Nat. Commun. 2018, 9, 902.
- 91M. W. Grome, Z. Zhang, F. Pincet, C. X. Lin, Angew. Chem., Int. Ed. 2018, 57, 5330.
- 92J. Zhang, Y. Xu, M. Chen, Y. Huang, T. Song, C. Yang, Y. Yang, Y. Song, J. Am. Chem. Soc. 2022, 144, 21295.
- 93W. Luo, V. Demidov, Q. Shen, H. Girão, M. Chakraborty, A. Maiorov, F. I. Ataullakhanov, C. Lin, H. Maiato, E. L. Grishchuk, Sci. Adv. 2023, 9, eabq5404.
- 94Y. Wang, I. Baars, I. Berzina, I. Rocamonde-Lago, B. Shen, Y. Yang, M. Lolaico, J. Waldvogel, I. Smyrlaki, K. Zhu, R. A. Harris, B. Hogberg, Nat. Nanotechnol. 2024, 19, 1366.
- 95K. Zhou, Y. Ke, Q. Wang, J. Am. Chem. Soc. 2018, 140, 8074.
- 96X. Mao, K. Li, M. Liu, X. Wang, T. Zhao, B. An, M. Cui, Y. Li, J. Pu, J. Li, L. Wang, T. K. Lu, C. Fan, C. Zhong, Nat. Commun. 2019, 10, 1395.
- 97A. Udomprasert, M. N. Bongiovanni, R. J. Sha, W. B. Sherman, T. Wang, P. S. Arora, J. W. Canary, S. L. Gras, N. C. Seeman, Nat. Nanotechnol. 2014, 9, 537.
- 98T. Jiang, T. A. Meyer, C. Modlin, X. B. Zuo, V. P. Conticello, Y. G. Ke, J. Am. Chem. Soc. 2017, 139, 14025.
- 99W. Engelen, C. Sigl, K. Kadletz, E. M. Willner, H. Dietz, J. Am. Chem. Soc. 2021, 143, 21630.
- 100M. Schliwa, G. Woehlke, Nature 2003, 422, 759.
- 101K. Fujita, M. Ohmachi, K. Ikezaki, T. Yanagida, M. Iwaki, Commun. Biol. 2019, 2, 437.
- 102C. Strambio-De-Castillia, M. Niepel, M. P. Rout, Nat. Rev. Mol. Cell. Biol. 2010, 11, 490.
- 103Q. Shen, S. Kumari, C. Xu, S. Jang, J. Shi, R. C. Burdick, L. Levintov, Q. Xiong, C. Wu, S. C. Devarkar, T. Tian, T. N. Tripler, Y. Hu, S. Yuan, J. Temple, Q. Feng, C. P. Lusk, C. Aiken, A. N. Engelman, J. R. Perilla, V. K. Pathak, C. Lin, Y. Xiong, Proc. Natl. Acad. Sci. U. S. A. 2023, 120, 2202815120.
- 104A. I. Benítez-Mateos, D. Roura Padrosa, F. Paradisi, Nat. Chem. 2022, 14, 489.
- 105M. Vázquez-González, C. Wang, I. Willner, Nat. Catal. 2020, 3, 256.
- 106S. Kröll, T. Burgahn, K. S. Rabe, M. Franzreb, C. M. Niemeyer, Small 2024, 20, 2304578.
- 107J. S. Kahn, Y. Xiong, J. Huang, O. Gang, JACS Au 2022, 2, 357.
- 108P. Lin, H. Dinh, Y. Morita, E. Nakata, T. Morii, Adv. Funct. Mater. 2023, 33, 2215023.
- 109J. Huang, A. Jaekel, J. van den Boom, D. Podlesainski, M. Elnaggar, A. Heuer-Jungemann, M. Kaiser, H. Meyer, B. Saccà, Nat. Nanotechnol. 2024, 19, 1521.
- 110M. J. Thompson, J. E. Baenziger, Nat. Chem. Biol. 2020, 16, 1331.
- 111S. Pang, J. Liu, T. Li, K. Ye, Z. Yan, L. Zhao, C. Bao, J. Am. Chem. Soc. 2023, 145, 20761.
- 112I. Mayer, T. Karimian, K. Gordiyenko, A. Angelin, R. Kumar, M. Hirtz, R. Mikut, M. Reischl, J. Stegmaier, L. Zhou, R. Ma, G. U. Nienhaus, K. S. Rabe, P. Lanzerstorfer, C. M. Dominguez, C. M. Niemeyer, Nano Lett. 2024, 24, 1611.
- 113R. M. L. Berger, J. M. Weck, S. M. Kempe, O. Hill, T. Liedl, J. O. Radler, C. Monzel, A. Heuer-Jungemann, Small 2021, 17, 2101678.
- 114N. Ma, K. Cheng, Q. Feng, G. Liu, J. Liang, X. Ma, Z. Chen, Y. Lu, X. Wang, W. He, H. Xu, S. Wu, J. Zou, Q. Shi, G. Nie, X. Zhao, Small 2023, 19, 2206160.
- 115J. Spratt, J. M. Dias, C. Kolonelou, G. Kiriako, E. Engstrom, E. Petrova, C. Karampelias, I. Cervenka, N. Papanicolaou, A. Lentini, B. Reinius, O. Andersson, E. Ambrosetti, J. L. Ruas, A. I. Teixeira, Nat. Nanotechnol. 2024, 19, 237.
- 116K. F. Wagenbauer, N. Pham, A. Gottschlich, B. Kick, V. Kozina, C. Frank, D. Trninic, P. Stommer, R. Grunmeier, E. Carlini, C. A. Tsiverioti, S. Kobold, J. J. Funke, H. Dietz, Nat. Nanotechnol. 2023, 18, 1319.
- 117A. Engelman, P. Cherepanov, Nat. Rev. Microbiol. 2012, 10, 279.
- 118H. Yang, Z. Rao, Nat. Rev. Microbiol. 2021, 19, 685.
- 119Y. Yang, J. Zhang, Y. Xu, M. Chen, S. Wang, G. Lin, Y. Huang, C. Yang, Y. Song, Angew. Chem., Int. Ed. 2024, 63, 202412294.
- 120C. Sigl, E. M. Willner, W. Engelen, J. A. Kretzmann, K. Sachenbacher, A. Liedl, F. Kolbe, F. Wilsch, S. A. Aghvami, U. Protzer, M. F. Hagan, S. Fraden, H. Dietz, Nat. Mater. 2021, 20, 1281.
- 121J. Hellmeier, R. Platzer, A. S. Eklund, T. Schlichthaerle, A. Karner, V. Motsch, M. C. Schneider, E. Kurz, V. Bamieh, M. Brameshuber, J. Preiner, R. Jungmann, H. Stockinger, G. J. Schutz, J. B. Huppa, E. Sevcsik, Proc. Natl. Acad. Sci. U. S. A. 2021, 118, 2016857118.
- 122L. Sun, F. Shen, Z. Xiong, Y. Chao, C. Fan, Z. Liu, CCS Chem. 2024, 6, 719.
- 123T. Fang, J. Alvelid, J. Spratt, E. Ambrosetti, I. Testa, A. I. Teixeira, ACS Nano 2021, 15, 3441.
- 124C. L. Ji, J. Y. Wei, L. Zhang, X. R. Hou, J. Tan, Q. Yuan, W. H. Tan, Chem. Rev. 2023, 123, 12471.
- 125Q. Y. Yang, R. Y. Wang, K. Wu, D. Li, Chin. J. Chem. 2023, 41, 2269.
- 126N. Chauhan, Y. Xiong, S. Ren, A. Dwivedy, N. Magazine, L. Zhou, X. Jin, T. Zhang, B. T. Cunningham, S. Yao, W. Huang, X. Wang, J. Am. Chem. Soc. 2023, 145, 20214.
- 127Y. H. Chen, G. L. Ke, Y. L. Ma, Z. Zhu, M. H. Liu, Y. Liu, H. Yan, C. J. Yang, J. Am. Chem. Soc. 2018, 140, 8990.
- 128S. Kröll, K. S. Rabe, C. M. Niemeyer, Small 2021, 17, 2105095.
- 129N. Cao, R. Guo, P. Song, S. Wang, G. Liu, J. Shi, L. Wang, M. Li, X. Zuo, X. Yang, C. Fan, M. Li, Y. Zhang, Nano Lett. 2024, 24, 4682.
- 130P. Song, J. Shen, D. Ye, B. Dong, F. Wang, H. Pei, J. Wang, J. Shi, L. Wang, W. Xue, Y. Huang, G. Huang, X. Zuo, C. Fan, Nat. Commun. 2020, 11, 838.
- 131Y. Ke, T. Meyer, W. M. Shih, G. Bellot, Nat. Commun. 2016, 7, 10935.
- 132X. Chang, Q. Yang, J. Y. Lee, D. Perumal, F. Zhang, J. Am. Chem. Soc. 2024, 146, 26131.
- 133M. Cui, D. Zhang, X. Zheng, H. Zhai, M. Xie, Q. Fan, L. Wang, C. Fan, J. Chao, J. Am. Chem. Soc. 2024, 146, 29609.
- 134S. Liu, Q. Jiang, X. Zhao, R. Zhao, Y. Wang, Y. Wang, J. Liu, Y. Shang, S. Zhao, T. Wu, Y. Zhang, G. Nie, B. Ding, Nat. Mater. 2021, 20, 421.
- 135P. Kosuri, B. D. Altheimer, M. Dai, P. Yin, X. Zhuang, Nature 2019, 572, 136.
- 136D. Jiang, Z. Ge, H.-J. Im, C. G. England, D. Ni, J. Hou, L. Zhang, C. J. Kutyreff, Y. Yan, Y. Liu, S. Y. Cho, J. W. Engle, J. Shi, P. Huang, C. Fan, H. Yan, W. Cai, Nat. Biomed. Eng. 2018, 2, 865.
- 137X. Liu, B. Shi, Y. Gao, S. Zhu, Q. Yan, X. Liu, J. Shi, Q. Li, L. Wang, J. Li, C. Zhao, H. Tian, I. Willner, Y. Zhu, C. Fan, Nat. Photonics 2024, 19, 79.
- 138Y. Xu, Q. Zhang, R. Chen, H. Cao, J. Tang, Y. Wu, X. Lu, B. Chu, B. Song, H. Wang, Y. He, J. Am. Chem. Soc. 2022, 144, 23522.
- 139Q. Lu, Y. Xu, E. Poppleton, K. Zhou, P. Sulc, N. Stephanopoulos, Y. Ke, Nano Lett. 2024, 24, 1703.
- 140K. Dai, Y. Xu, Y. Yang, J. Shen, X. Liu, X. Tu, L. Yu, X. Qi, J. Li, L. Wang, X. Zuo, Y. Liu, H. Yan, C. Fan, G. Yao, J. Am. Chem. Soc. 2023, 145, 17112.
- 141Y. Zhao, J. Hou, L. Guo, S. Zhu, X. Hou, S. Cao, M. Zhou, J. Shi, J. Li, K. Liu, H. Zhang, L. Wang, C. Fan, Y. Zhu, J. Am. Chem. Soc. 2024, 146, 25253.
