Review

Advances in Detection of Epigenetic Modification—5-Hydroxymethylcytosine

  • Chen-chen Li ,
  • Hui-yan Chen ,
  • Yue-hong Dong ,
  • Xiliang Luo ,
  • Juan Hu ,
  • Chun-yang Zhang
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  • a College of Chemistry and Molecular Engineering, Qingdao University of Science and Technology, Qingdao 266042, China
    b College of Chemistry, Chemical Engineering and Materials Science, Shandong Normal University, Jinan 250014, China
    c School of Chemistry and Chemical Engineering, Southeast University, Nanjing 211189, China

Received date: 2020-12-10

  Online published: 2021-01-25

Supported by

National Natural Science Foundation of China(21735003); National Natural Science Foundation of China(21527811); Taishan Scholar Program of Shandong Province of China(ts20110829); Award for Team Leader Program of Taishan Scholars of Shandong Province, China

Abstract

Epigenetic inheritance is a heritable change in gene function independent of alterations in nucleotide sequence. 5-Hydroxymethylcytosine (5hmC), which is called “the sixth base”, is an epigenetic modification discovered after 5-methylcytosine (5mC). 5hmC is widely distributed in mammalian tissues and cells, and its abnormality is closely related to tumorigenesis, developmental diseases, and nervous system diseases. Because the structure of 5hmC is similar to that of 5mC and its abundance is much lower than that of 5mC, it is much difficult to accurately detect 5hmC by using the traditional methods. Recently, scientists have developed a series of new methods for the detection of 5hmC, including liquid chromatography tandem mass spectrometry, fluorescent method, electrochemical method, photoelectrochemical method, single base-resolution sequencing, and single-molecule detection technology. These emerging technologies have their own unique advantages and greatly promote the advance of epigenetic research. The recent advance in the detection of 5hmC is reviewed in this paper, and the challenge and trends of this area is highlighted as well.

Cite this article

Chen-chen Li , Hui-yan Chen , Yue-hong Dong , Xiliang Luo , Juan Hu , Chun-yang Zhang . Advances in Detection of Epigenetic Modification—5-Hydroxymethylcytosine[J]. Acta Chimica Sinica, 2021 , 79(5) : 614 -627 . DOI: 10.6023/A20120564

References

[1]
Wolffe, A. P.; Matzke, M. A. Science 1999, 286,481.
[2]
Jaenisch, R.; Bird, A. Nat. Genet. 2003, 33,245.
[3]
Prins, G. S.; Ye, S. H.; Birch, L.; Zhang, X.; Cheong, A.; Lin, H.; Calderon-Gierszal, E.; Groen, J.; Hu, W. Y.; Ho, S. M.; van Breemen, R. B. Environ. Health Perspect. 2017, 125,077007.
[4]
Portela, A.; Esteller, M. Nat. Biotechnol. 2010, 28,1057.
[5]
Tahara, T.; Tahara, S.; Horiguchi, N.; Kawamura, T.; Okubo, M.; Yamada, H.; Yoshida, D.; Ohmori, T.; Maeda, K.; Komura, N.; Ikuno, H.; Jodai, Y.; Kamano, T.; Nagasaka, M.; Nakagawa, Y.; Tsukamoto, T.; Urano, M.; Shibata, T.; Kuroda, M.; Ohmiya, N. Clin. Exp. Med. 2018, 18,215.
[6]
Moruzzi, S.; Guarini, P.; Udali, S.; Ruzzenente, A.; Guglielmi, A.; Conci, S.; Pattini, P.; Martinelli, N.; Olivieri, O.; Tammen, S. A.; Choi, S. W.; Friso, S. PLoS One 2017, 12,e0185792.
[7]
Iwata, A.; Nagata, K.; Hatsuta, H.; Takuma, H.; Bundo, M.; Iwamoto, K.; Tamaoka, A.; Murayama, S.; Saido, T.; Tsuji, S. Hum. Mol. Genet. 2014, 23,648.
[8]
Lee, J.; Hagerty, S.; Cormier, K. A.; Kim, J.; Kung, A. L.; Ferrante, R. J.; Ryu, H. Hum. Mol. Genet. 2008, 17,1774.
[9]
Begum, G.; Davies, A.; Stevens, A.; Oliver, M.; Jaquiery, A.; Challis, J.; Harding, J.; Bloomfield, F.; White, A. Endocrinology 2013, 154,4560.
[10]
Baserga, M.; Kaur, R.; Hale, M. A.; Bares, A.; Yu, X.; Callaway, C. W.; McKnight, R. A.; Lane, R. H. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010,299,R334.
[11]
Baserga, M.; Hale, M. A.; Wang, Z. M.; Yu, X.; Callaway, C. W.; McKnight, R. A.; Lane, R. H. Am. J. Physiol-Reg I. 2007, 292,R1943.
[12]
Masuyama, H.; Hiramatsu, Y. Endocrinology 2012, 153,2823.
[13]
Li, D.; Tian, Y. J.; Guo, J.; Sun, W. P.; Lun, Y. Z.; Guo, M.; Luo, N.; Cao, Y.; Cao, J. M.; Gong, X. J.; Zhou, S. S. Br. J. Nutr. 2013, 110,2156.
[14]
Zhao, C.; Wang, H. L. Acta Chim. Sinica 2013, 71,26. (in Chinese).
[14]
( 赵超, 汪海林, 化学学报, 2013, 71,26.)
[15]
Cheng, X.; Roberts, R. J. Nucleic Acids Res. 2001, 29,3784.
[16]
Smith, Z. D.; Meissner, A. Nat. Rev. Genet. 2013, 14,204.
[17]
Wood, R. J.; McKelvie, J. C.; Maynard-Smith, M. D.; Roach, P. L. Nucleic Acids Res. 2010, 38,e107.
[18]
Xu, H.; Jia, P.; Zhao, Z. Brief Bioinform. 2020,doi: 10.1093/bib/bbaa099.
[19]
Xiao, C. L.; Zhu, S.; He, M. H.; Chen, D.; Zhang, Q.; Chen, Y.; Yu, G. L.; Liu, J. B.; Xie, S. Q.; Luo, F.; Liang, Z.; Wang, D. P.; Bo, X. C.; Gu, X. F.; Wang, K.; Yan, G. R. Mol. Cell 2018, 71,306.
[20]
Stains, C. I.; Furman, J. L.; Segal, D. J.; Ghosh, I. J. Am. Chem. Soc. 2006, 128,9761.
[21]
Costello, J. F.; Fruhwald, M. C.; Smiraglia, D. J.; Rush, L. J.; Robertson, G. P.; Gao, X.; Wright, F. A.; Feramisco, J. D.; Peltomaki, P.; Lang, J. C.; Schuller, D. E.; Yu, L.; Bloomfield, C. D.; Caligiuri, M. A.; Yates, A.; Nishikawa, R.; Huang, H. J. S.; Petrelli, N. J.; Zhang, X. L.; O'Dorisio, M. S.; Held, W. A.; Cavenee, W. K.; Plass, C. Nat. Genet. 2000, 24,132.
[22]
Bernstein, B. E.; Meissner, A.; Lander, E. S. Cell 2007, 128,669.
[23]
Zhang, Q.; Wu, Y.; Xu, Q.; Ma, F.; Zhang, C. Y. Biosens. Bioelectron. 2021, 171,112712.
[24]
Song, C. X.; Szulwach, K. E.; Fu, Y.; Dai, Q.; Yi, C.; Li, X.; Li, Y.; Chen, C. H.; Zhang, W.; Jian, X.; Wang, J.; Zhang, L.; Looney, T. J.; Zhang, B.; Godley, L. A.; Hicks, L. M.; Lahn, B. T.; Jin, P.; He, C. Nat. Biotechnol. 2011, 29,68.
[25]
Scarano, M. I.; Strazzullo, M.; Matarazzo, M. R.; D'Esposito, M. J. Cell. Physiol. 2005, 204,21.
[26]
Robertson, K. D. Nat. Rev. Genet. 2005, 6,597.
[27]
Iwan, K.; Rahimoff, R.; Kirchner, A.; Spada, F.; Schroder, A. S.; Kosmatchev, O.; Ferizaj, S.; Steinbacher, J.; Parsa, E.; Muller, M.; Carell, T. Nat. Chem. Biol. 2018, 14,72.
[28]
Wu, S. C.; Zhang, Y. Nat. Rev. Mol. Cell Bio. 2010, 11,607.
[29]
Huang, W.; Lan, M. D.; Qi, C. B.; Zheng, S. J.; Wei, S. Z.; Yuan, B. F.; Feng, Y. Q. Chem. Sci. 2016, 7,5495.
[30]
Crawford, D. J.; Liu, M. Y.; Nabel, C. S.; Cao, X. J.; Garcia, B. A.; Kohli, R. M. J. Am. Chem. Soc. 2016, 138,730.
[31]
Chen, S.; Dou, Y.; Zhao, Z.; Li, F.; Su, J.; Fan, C.; Song, S. Anal. Chem. 2016, 88,3476.
[32]
Zhang, L.; Yu, M.; He, C. Acta Chim. Sinica 2012, 70,2123. (in Chinese).
[32]
( 张良, 于淼, 何川, 化学学报, 2012, 70,2123.)
[33]
Liutkeviciute, Z.; Kriukiene, E.; Licyte, J.; Rudyte, M.; Urbanaviciute, G.; Klimasauskas, S. J. Am. Chem. Soc. 2014, 136,5884.
[34]
Kohli, R. M.; Zhang, Y. Nature 2013, 502,472.
[35]
Kagiwada, S.; Kurimoto, K.; Hirota, T.; Yamaji, M.; Saitou, M. EMBO J. 2013, 32,340.
[36]
Ginno, P. A.; Gaidatzis, D.; Feldmann, A.; Hoerner, L.; Imanci, D.; Burger, L.; Zilbermann, F.; Peters, A. H. F. M.; Edenhofer, F.; Smallwood, S. A.; Krebs, A. R.; Schubeler, D. Nat. Commun. 2020, 11,2680.
[37]
Shukla, A.; Sehgal, M.; Singh, T. R. Gene 2015, 564,109.
[38]
Munzel, M.; Globisch, D.; Carell, T. Angew. Chem., Int. Ed. 2011, 50,6460.
[39]
Tahiliani, M.; Koh, K. P.; Shen, Y.; Pastor, W. A.; Bandukwala, H.; Brudno, Y.; Agarwal, S.; Iyer, L. M.; Liu, D. R.; Aravind, L.; Rao, A. Science 2009, 324,930.
[40]
Kriaucionis, S.; Heintz, N. Science 2009, 324,929.
[41]
Mellen, M.; Ayata, P.; Dewell, S.; Kriaucionis, S.; Heintz, N. Cell 2012, 151,1417.
[42]
Szulwach, K. E.; Li, X.; Li, Y.; Song, C. X.; Han, J. W.; Kim, S.; Namburi, S.; Hermetz, K.; Kim, J. J.; Rudd, M. K.; Yoon, Y. S.; Ren, B.; He, C.; Jin, P. PLoS Genet. 2011, 7,e1002154.
[43]
Pfeifer, G. P.; Kadam, S.; Jin, S. G. Epigenetics Chromatin 2013, 6,10.
[44]
Jin, S. G.; Jiang, Y.; Qiu, R.; Rauch, T. A.; Wang, Y.; Schackert, G.; Krex, D.; Lu, Q.; Pfeifer, G. P. Cancer Res. 2011, 71,7360.
[45]
Kato, T.; Iwamoto, K. Neuropharmacology 2014, 80,133.
[46]
Wen, L.; Tang, F. Genomics 2014, 104,341.
[47]
Yang, Y.; Yang, G.; Chen, H.; Zhang, H.; Feng, J. J.; Cai, C. Analyst 2018, 143,2051.
[48]
Jin, S. G.; Kadam, S.; Pfeifer, G. P. Nucleic Acids Res. 2010, 38,e125.
[49]
Nestor, C.; Ruzov, A.; Meehan, R. R.; Dunican, D. S. Biotechniques 2010, 48,317.
[50]
Ito, S.; D'Alessio, A. C.; Taranova, O. V.; Hong, K.; Sowers, L. C.; Zhang, Y. Nature 2010, 466,1129.
[51]
Huang, Y.; Pastor, W. A.; Shen, Y. H.; Tahiliani, M.; Liu, D. R.; Rao, A. PLoS One 2010, 5,e8888.
[52]
Flusberg, B. A.; Webster, D. R.; Lee, J. H.; Travers, K. J.; Olivares, E. C.; Clark, T. A.; Korlach, J.; Turner, S. W. Nat. Methods 2010, 7,461.
[53]
Munzel, M.; Globisch, D.; Bruckl, T.; Wagner, M.; Welzmiller, V.; Michalakis, S.; Muller, M.; Biel, M.; Carell, T. Angew. Chem., Int. Ed. 2010, 49,5375.
[54]
Yin, R. C.; Mo, J. Z.; Lu, M. L.; Wang, H. L. Anal. Chem. 2015, 87,1846.
[55]
Krais, A. M.; Park, Y. J.; Plass, C.; Schmeiser, H. H. Epigenetics 2011, 6,560.
[56]
Hong, T.; Wang, T.; Guo, P.; Xing, X.; Ding, F.; Chen, Y.; Wu, J.; Ma, J.; Wu, F.; Zhou, X. Anal. Chem. 2013, 85,10797.
[57]
Pastor, W. A.; Pape, U. J.; Huang, Y.; Henderson, H. R.; Lister, R.; Ko, M.; McLoughlin, E. M.; Brudno, Y.; Mahapatra, S.; Kapranov, P.; Tahiliani, M.; Daley, G. Q.; Liu, X. S.; Ecker, J. R.; Milos, P. M.; Agarwal, S.; Rao, A. Nature 2011, 473,394.
[58]
Ko, M.; Huang, Y.; Jankowska, A. M.; Pape, U. J.; Tahiliani, M.; Bandukwala, H. S.; An, J.; Lamperti, E. D.; Koh, K. P.; Ganetzky, R.; Liu, X. S.; Aravind, L.; Agarwal, S.; Maciejewski, J. P.; Rao, A. Nature 2010, 468,839.
[59]
Nestor, C. E.; Ottaviano, R.; Reddington, J.; Sproul, D.; Reinhardt, D.; Dunican, D.; Katz, E.; Dixon, J. M.; Harrison, D. J.; Meehan, R. R. Genome Res. 2012, 22,467.
[60]
Voigt, P.; Tee, W. W.; Reinberg, D. Genes Dev. 2013, 27,1318.
[61]
Plongthongkum, N.; Diep, D. H.; Zhang, K. Nat. Rev. Genet. 2014, 15,647.
[62]
Tang, Y.; Chu, J. M.; Huang, W.; Xiong, J.; Xing, X. W.; Zhou, X.; Feng, Y. Q.; Yuan, B. F. Anal. Chem. 2013, 85,6129.
[63]
He, Y. F.; Li, B. Z.; Li, Z.; Liu, P.; Wang, Y.; Tang, Q.; Ding, J.; Jia, Y.; Chen, Z.; Li, L.; Sun, Y.; Li, X.; Dai, Q.; Song, C. X.; Zhang, K.; He, C.; Xu, G. L. Science 2011, 333,1303.
[64]
Le, T.; Kim, K. P.; Fan, G.; Faull, K. F. Anal. Biochem. 2011, 412,203.
[65]
Liu, S.; Wang, J.; Su, Y.; Guerrero, C.; Zeng, Y.; Mitra, D.; Brooks, P. J.; Fisher, D. E.; Song, H.; Wang, Y. Nucleic Acids Res. 2013, 41,6421.
[66]
Yuan, F.; Yu, Y.; Zhou, Y. L.; Zhang, X. X. Anal. Chem. 2020, 92,1605.
[67]
Shahal, T.; Koren, O.; Shefer, G.; Stern, N.; Ebenstein, Y. Anal. Chim. Acta 2018, 1038,87.
[68]
Wang, Z. Y.; Wang, M.; Zhang, Y.; Zhang, C. Y. Chem. Commun. 2018, 54,8602.
[69]
Chen, H. Y.; Wei, J. R.; Pan, J. X.; Zhang, W.; Dang, F. Q.; Zhang, Z. Q.; Zhang, J. Biosens. Bioelectron. 2017, 91,328.
[70]
Cui, L.; Hu, J.; Wang, M.; Li, C. C.; Zhang, C. Y. Anal. Chem. 2019, 91,1232.
[71]
Wang, H.; Liu, M. Z.; Bai, W. Q.; Sun, H. P.; Li, Y.; Deng, H. Q. Sens. Actuators B 2019, 284,236.
[72]
Ma, S.; Sun, H.; Li, Y.; Qi, H.; Zheng, J. Anal. Chem. 2016, 88,9934.
[73]
Zhou, Y. L.; Yin, H. S.; Sui, C. J.; Wang, Y.; Ai, S. Y. Chem. Eng. J. 2019, 357,94.
[74]
Sui, C.; Li, F.; Wu, H.; Yin, H.; Zhang, S.; Waterhouse, G. I. N.; Wang, J.; Zhu, L.; Ai, S. Biosens. Bioelectron. 2019, 142,111516.
[75]
Wang, Y.; Zhang, X.; Wu, F.; Chen, Z.; Zhou, X. Chem. Sci. 2019, 10,447.
[76]
Hu, L.; Liu, Y.; Han, S.; Yang, L.; Cui, X.; Gao, Y.; Dai, Q.; Lu, X.; Kou, X.; Zhao, Y.; Sheng, W.; Gao, S.; He, X.; He, C. J. Am. Chem. Soc. 2019, 141,8694.
[77]
Liu, Y.; Siejka-Zielinska, P.; Velikova, G.; Bi, Y.; Yuan, F.; Tomkova, M.; Bai, C.; Chen, L.; Schuster-Bockler, B.; Song, C. X. Nat. Biotechnol. 2019, 37,424.
[78]
Song, C. X.; Clark, T. A.; Lu, X. Y.; Kislyuk, A.; Dai, Q.; Turner, S. W.; He, C.; Korlach, J. Nat. Methods 2012, 9,75.
[79]
Gilat, N.; Tabachnik, T.; Shwartz, A.; Shahal, T.; Torchinsky, D.; Michaeli, Y.; Nifker, G.; Zirkin, S.; Ebenstein, Y. Clin. Epigenetics. 2017, 9,70.
[80]
Cui, L.; Chung, T. H.; Tan, D.; Sun, X.; Jia, X. Y. Genomics 2014, 104,368.
[81]
Hofer, A.; Liu, Z. J.; Balasubramanian, S. J. Am. Chem. Soc. 2019, 141,6420.
[82]
Lichtman, J. W.; Conchello, J. A. Nat. Methods 2005, 2,910.
[83]
Hall, T. Science 1961, 134,449.
[84]
Zhang, Z.; Yan, J.; Li, Z. Chem. Commun. 2020, 56,3111.
[85]
Shahal, T.; Gilat, N.; Michaeli, Y.; Redy-Keisar, O.; Shabat, D.; Ebenstein, Y. Anal. Chem. 2014, 86,8231.
[86]
Beyer, S.; Nickels, P.; Simmel, F. C. Nano Lett. 2005, 5,719.
[87]
Baner, J.; Nilsson, M.; Mendel-Hartvig, M.; Landegren, U. Nucleic Acids Res. 1998, 26,5073.
[88]
Zhang, Z. H.; Shan, X.; Zhang, P. B.; Liu, W. L.; Yan, J. L.; Li, Z. P. Org. Biomol. Chem. 2019, 17,9849.
[89]
Yin, H. S.; Yang, Z. Q.; Wang, H. Y.; Zhou, Y. L.; Ai, S. Y. Sens. Actuators B 2017, 243,602.
[90]
Tang, Z. W.; Huang, J.; He, H. L.; Ma, C. B.; Wang, K. M. Coord. Chem. Rev. 2020, 415,213317.
[91]
Povedano, E.; Montiel, V. R.; Valverde, A.; Navarro-Villoslada, F.; Yanez-Sedeno, P.; Pedrero, M.; Montero-Calle, A.; Barderas, R.; Pelaez-Garcia, A.; Mendiola, M.; Hardisson, D.; Feliu, J.; Camps, J.; Rodriguez-Tomas, E.; Joven, J.; Arenas, M.; Campuzano, S.; Pingarron, J. M. ACS Sens. 2019, 4,227.
[92]
Povedano, E.; Ruiz-Valdepenas Montiel, V.; Gamella, M.; Pedrero, M.; Barderas, R.; Pelaez-Garcia, A.; Mendiola, M.; Hardisson, D.; Feliu, J.; Yanez-Sedeno, P.; Campuzano, S.; Pingarron, J. M. Anal. Chem. 2020, 92,5604.
[93]
Liu, C. Y.; Bard, A. J. Nat. Mater. 2008, 7,505.
[94]
Li, L. L.; Chen, Y.; Zhu, J. J. Anal. Chem. 2017, 89,358.
[95]
Xu, S. J.; Liu, Y.; Wang, T. H.; Li, J. H. Anal. Chem. 2010, 82,9566.
[96]
Tang, X.; Zhao, D.; He, J.; Li, F.; Peng, J.; Zhang, M. Anal. Chem. 2013, 85,1711.
[97]
Sun, H.; Ma, S.; Li, Y.; Qi, H.; Ning, X.; Zheng, J. Biosens. Bioelectron. 2016, 79,92.
[98]
Sun, H.; Wang, H.; Bai, W.; Bao, L.; Lin, J.; Li, Y. Talanta 2019, 191,350.
[99]
Zhao, W. W.; Xu, J. J.; Chen, H. Y. Chem. Rev. 2014, 114,7421.
[100]
Zhao, W. W.; Xu, J. J.; Chen, H. Y. Trac-Trend Anal. Chem. 2016, 82,307.
[101]
Yang, Z. Q.; Shi, Y. H.; Liao, W. R.; Yin, H. S.; Ai, S. Y. Sens. Actuators B 2016, 223,621.
[102]
Wang, M.; Yin, H.; Zhou, Y.; Sui, C.; Wang, Y.; Meng, X.; Waterhouse, G. I. N.; Ai, S. Biosens. Bioelectron. 2019, 128,137.
[103]
Zang, Y.; Lei, J.; Hao, Q.; Ju, H. Biosens. Bioelectron. 2016, 77,557.
[104]
Tan, Y.; Li, M. S.; Ye, X. X.; Wang, Z. G.; Wang, Y. Y.; Li, C. Y. Sens. Actuators B 2018, 262,982.
[105]
Lan, F.; Liang, L.; Zhang, Y.; Li, L.; Ren, N.; Yan, M.; Ge, S.; Yu, J. ACS Appl. Mater. Interfaces 2017, 9,37839.
[106]
Okoth, O. K.; Yan, K.; Liu, Y.; Zhang, J. Biosens. Bioelectron. 2016, 86,636.
[107]
Li, L.; Wang, T.; Zhang, Y.; Xu, C.; Zhang, L.; Cheng, X.; Liu, H.; Chen, X.; Yu, J. ACS Appl. Mater. Interfaces 2018, 10,14594.
[108]
Sui, C.; Wang, T.; Zhou, Y.; Yin, H.; Meng, X.; Zhang, S.; Waterhouse, G. I. N.; Xu, Q.; Zhuge, Y.; Ai, S. Biosens. Bioelectron. 2019, 127,38.
[109]
Pastor, W. A.; Huang, Y.; Henderson, H. R.; Agarwal, S.; Rao, A. Nat. Protoc. 2012, 7,1909.
[110]
Huang, Y.; Pastor, W. A.; Zepeda-Martinez, J. A.; Rao, A. Nat. Protoc. 2012, 7,1897.
[111]
Tan, L.; Xiong, L.; Xu, W.; Wu, F.; Huang, N.; Xu, Y.; Kong, L.; Zheng, L.; Schwartz, L.; Shi, Y.; Shi, Y. G. Nucleic Acids Res. 2013, 41,e84.
[112]
Casanello, P.; Krause, B. J.; Castro-Rodriguez, J. A.; Uauy, R. Rev. Chil. Pediatr. 2016, 87,335.
[113]
Booth, M. J.; Marsico, G.; Bachman, M.; Beraldi, D.; Balasubramanian, S. Nat. Chem. 2014, 6,435.
[114]
Raiber, E. A.; Hardisty, R.; van Delft, P.; Balasubramanian, S. Nat. Rev. Chem. 2017, 1,0069.
[115]
Yu, M.; Hon, G. C.; Szulwach, K. E.; Song, C. X.; Zhang, L.; Kim, A.; Li, X.; Dai, Q.; Shen, Y.; Park, B.; Min, J. H.; Jin, P.; Ren, B.; He, C. Cell 2012, 149,1368.
[116]
Booth, M. J.; Branco, M. R.; Ficz, G.; Oxley, D.; Krueger, F.; Reik, W.; Balasubramanian, S. Science 2012, 336,934.
[117]
Tanaka, K.; Okamoto, A. Bioorg. Med. Chem. Lett. 2007, 17,1912.
[118]
Zeng, H.; He, B.; Xia, B.; Bai, D.; Lu, X.; Cai, J.; Chen, L.; Zhou, A.; Zhu, C.; Meng, H.; Gao, Y.; Guo, H.; He, C.; Dai, Q.; Yi, C. J. Am. Chem. Soc. 2018, 140,13190.
[119]
Sun, Z.; Dai, N.; Borgaro, J. G.; Quimby, A.; Sun, D.; Correa, I. R. Jr.; Zheng, Y.; Zhu, Z.; Guan, S. Mol. Cell. 2015, 57,750.
[120]
Fang, K.; Zhang, K. X.; Wang, J.; Fu, Z. M.; Zhao, X. H. Yi Chuan 2016, 38,206. (in Chinese).
[120]
( 方科, 张凯翔, 王建, 付志猛, 赵湘辉, 遗传, 2016, 38,206.)
[121]
Li, C. C.; Liu, W. X.; Hu, J.; Zhang, C. Y. Chem. Sci. 2019, 10,8675.
[122]
Ma, F.; Li, Y.; Tang, B.; Zhang, C. Y. Acc. Chem. Res. 2016, 49,1722.
[123]
Eid, J.; Fehr, A.; Gray, J.; Luong, K.; Lyle, J.; Otto, G.; Peluso, P.; Rank, D.; Baybayan, P.; Bettman, B.; Bibillo, A.; Bjornson, K.; Chaudhuri, B.; Christians, F.; Cicero, R.; Clark, S.; Dalal, R.; Dewinter, A.; Dixon, J.; Foquet, M.; Gaertner, A.; Hardenbol, P.; Heiner, C.; Hester, K.; Holden, D.; Kearns, G.; Kong, X.; Kuse, R.; Lacroix, Y.; Lin, S.; Lundquist, P.; Ma, C.; Marks, P.; Maxham, M.; Murphy, D.; Park, I.; Pham, T.; Phillips, M.; Roy, J.; Sebra, R.; Shen, G.; Sorenson, J.; Tomaney, A.; Travers, K.; Trulson, M.; Vieceli, J.; Wegener, J.; Wu, D.; Yang, A.; Zaccarin, D.; Zhao, P.; Zhong, F.; Korlach, J.; Turner, S. Science 2009, 323,133.
[124]
Kasianowicz, J. J.; Brandin, E.; Branton, D.; Deamer, D. W. Proc. Natl. Acad. Sci. U. S. A. 1996,93,13770.
[125]
Clarke, J.; Wu, H. C.; Jayasinghe, L.; Patel, A.; Reid, S.; Bayley, H. Nat. Nanotechnol. 2009, 4,265.
[126]
Cherf, G. M.; Lieberman, K. R.; Rashid, H.; Lam, C. E.; Karplus, K.; Akeson, M. Nat. Biotechnol. 2012, 30,344.
[127]
Manrao, E. A.; Derrington, I. M.; Laszlo, A. H.; Langford, K. W.; Hopper, M. K.; Gillgren, N.; Pavlenok, M.; Niederweis, M.; Gundlach, J. H. Nat. Biotechnol. 2012, 30,349.
[128]
Wendell, D.; Jing, P.; Geng, J.; Subramaniam, V.; Lee, T. J.; Montemagno, C.; Guo, P. Nat. Nanotechnol. 2009, 4,765.
[129]
Howorka, S.; Siwy, Z. Chem. Soc. Rev. 2009, 38,2360.
[130]
Venkatesan, B. M.; Bashir, R. Nat. Nanotechnol. 2011, 6,615.
[131]
Haque, F.; Li, J.; Wu, H. C.; Liang, X. J.; Guo, P. Nano Today 2013, 8,56.
[132]
Wanunu, M.; Cohen-Karni, D.; Johnson, R. R.; Fields, L.; Benner, J.; Peterman, N.; Zheng, Y.; Klein, M. L.; Drndic, M. J. Am. Chem. Soc. 2011, 133,486.
[133]
Li, W. W.; Gong, L. Z.; Bayley, H. Angew. Chem., Int. Ed. 2013, 52,4350.
[134]
Zeng, T.; Liu, L.; Li, T.; Li, Y.; Gao, J.; Zhao, Y.; Wu, H. C. Chem. Sci. 2015, 6,5628.
[135]
Gabrieli, T.; Sharim, H.; Nifker, G.; Jeffet, J.; Shahal, T.; Arielly, R.; Levi-Sakin, M.; Hoch, L.; Arbib, N.; Michaeli, Y.; Ebenstein, Y. ACS Nano 2018, 12,7148.
[136]
Chen, F.; Xue, J.; Zhang, J.; Bai, M.; Yu, X.; Fan, C.; Zhao, Y. J. Am. Chem. Soc. 2020, 142,2889.
[137]
Song, C. X.; Diao, J.; Brunger, A. T.; Quake, S. R. Proc. Natl. Acad. Sci. U. S. A. 2016,113,4338.
[138]
Szulwach, K. E.; Li, X.; Li, Y.; Song, C. X.; Wu, H.; Dai, Q.; Irier, H.; Upadhyay, A. K.; Gearing, M.; Levey, A. I.; Vasanthakumar, A.; Godley, L. A.; Chang, Q.; Cheng, X.; He, C.; Jin, P. Nat. Neurosci. 2011, 14,1607.
[139]
Li, C. C.; Dong, Y. H.; Zou, X.; Luo, X.; Shen, D.; Hu, J.; Zhang, C. Y. Anal. Chem. 2021, 93,1939.
[140]
Walker, G. T.; Fraiser, M. S.; Schram, J. L.; Little, M. C.; Nadeau, J. G.; Malinowski, D. P. Nucleic Acids Res. 1992, 20,1691.
[141]
Ma, F.; Yang, Y.; Zhang, C. Y. Anal. Chem. 2014, 86,6006.
[142]
Zhao, W.; Ali, M. M.; Brook, M. A.; Li, Y. Angew. Chem., Int. Ed. 2008, 47,6330.
[143]
Ma, F.; Liu, M.; Zhang, C. Y. Chem. Commun. 2019, 55,8963.
[144]
Barany, F. Proc. Natl. Acad. Sci. U. S. A. 1991,88,189.
[145]
Ma, F.; Liu, H.; Li, C. C.; Zhang, C. Y. Chem. Commun. 2018, 54,12638.
[146]
Yin, B. C.; Liu, Y. Q.; Ye, B. C. J. Am. Chem. Soc. 2012, 134,5064.
[147]
Ma, F.; Liu, W. J.; Zhang, Q.; Zhang, C. Y. Chem. Commun. 2017, 53,10596.
[148]
Zhang, Y.; Li, C. C.; Tang, B.; Zhang, C. Y. Anal. Chem. 2017, 89,7684.
[149]
Li, C. C.; Zhang, Y.; Tang, B.; Zhang, C. Y. Chem. Commun. 2018, 54,5839.
[150]
Bi, S.; Yue, S.; Zhang, S. Chem. Soc. Rev. 2017, 46,4281.
[151]
Jiang, Y. S.; Li, B.; Milligan, J. N.; Bhadra, S.; Ellington, A. D. J. Am. Chem. Soc. 2013, 135,7430.
[152]
Ma, F.; Wei, S. H.; Zhang, C. Y. Anal. Chem. 2019, 91,7505.
[153]
Lu, X.; Song, C. X.; Szulwach, K.; Wang, Z.; Weidenbacher, P.; Jin, P.; He, C. J. Am. Chem. Soc. 2013, 135,9315.
[154]
Xia, B.; Han, D. L.; Lu, X. Y.; Sun, Z. Z.; Zhou, A. K.; Yin, Q. Z.; Zeng, H.; Liu, M. H.; Jiang, X.; Xie, W.; He, C.; Yi, C. Q. Nat. Methods 2015, 12,1047.
[155]
Ma, F.; Liu, M.; Wang, Z. Y.; Zhang, C. Y. Chem. Commun. 2016, 52,1218.
[156]
Zhang, H. D.; Huang, X. D.; Liu, J. W.; Liu, B. H. Chem. Sci. 2020, 11,3812.
[157]
Miyata, K.; Naito, M.; Miyata, T.; Mokuda, S.; Asahara, H. Methods Mol. Biol. 2017, 1668,3.
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