Review

Tumor-specific Peptide Probes and the Applications in Bioimaging

  • Bo Wang ,
  • Xiangdong Cai ,
  • Jianxi Xiao
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  • a College of Chemistry and Chemical Engineering, Lanzhou University, Lanzhou 730000, China
    b Gansu Engineering Research Center of Medical Collagen, Lanzhou 730000, China

Received date: 2023-10-13

  Online published: 2024-02-02

Supported by

National Natural Science Foundation of China(22074057); Natural Science Foundation of Gansu Province(20YF3FA025); Natural Science Foundation of Gansu Province(23JRRA1096); China Postdoctoral Science Foundation(2022M711449)

Abstract

The tumor is a complex system composed of various elements, encompassing cells, extracellular matrix, and the tumor microenvironment. Each of these distinct factors plays a pivotal role in the development and progression of tumors. The specific analysis of tumor-associated cells, extracellular matrix, and tumor microenvironment is of paramount importance for precise diagnosis and targeted therapy of tumors. Peptide probes have gained substantial prominence in investigations focused on tumor-specific imaging, primarily attributed to their notable attributes, including high specificity, biocompatibility, tissue-penetrating capabilities, and straightforward preparation processes. This review comprehensively summarizes the peptide probes for specific imaging of tumor-associated cells. The specific recognition of cells was by binding various cellular markers, such as the epidermal growth factor receptor (EGFR), vascular endothelial growth factor receptor (VEGFR), and folate receptor (FRα) for tumor cells. Additionally, the biomarkers include CD206, neurokinin-1 receptor (NK-1R), and CD11c for immune cells, along with nucleolin and integrins for tumor vascular endothelial cells. Furthermore, this comprehensive review encapsulates peptide probes designed for the specific targeting of extracellular matrix proteins and their applications in tumor-specific imaging. The focal points among these protein targets encompass pathological collagen, matrix metalloproteinases, and fibronectin. Of particular significance is the potential of pathological collagen as a highly promising extracellular matrix target for achieving tumor-specific imaging. The review comprehensively outlines tumor-specific peptide probes responsive to various factors within the tumor microenvironment. Commonly encountered responsive factors in the tumor microenvironment include mild acidity (pH), heightened enzyme activity, such as matrix metalloproteinases and cathepsin, and elevated levels of oxidative stress. It further explores their versatile applications in bioimaging. Lastly, this review discusses the clinical applications of tumor-specific peptide probes in diagnostic practices. It explores the current challenges and prospects of these peptide probes, elucidating their potential contributions to precision diagnosis and personalized treatment of tumors, including precise surgical navigation and their synergistic use with immunotherapy.

Cite this article

Bo Wang , Xiangdong Cai , Jianxi Xiao . Tumor-specific Peptide Probes and the Applications in Bioimaging[J]. Acta Chimica Sinica, 2024 , 82(3) : 367 -376 . DOI: 10.6023/A23100448

References

[1]
Henke, E.; Nandigama, R.; Ergün, S. Front. Mol. Biosci. 2019, 6, 160.
[2]
Bejarano, L.; Jordāo, M. J. C.; Joyce, J. A. Cancer Discov. 2021, 11, 933.
[3]
Sa, P.; Sahoo, S. K.; Dilnawaz, F. Curr. Med. Chem. 2023, 30, 3335.
[4]
Monteiro, A. C.; Lepique, A. P.; Bonamino, M.; Fuertes, M. B. Front. Immunol. 2023, 14, 1141084.
[5]
Peng, S. J.; Xiao, F. F.; Chen, M. W.; Gao, H. L. Adv. Sci. 2022, 9, 2103836.
[6]
Wang, Q.; Shao, X.; Zhang, Y.; Zhu, M.; Wang, F. X. C.; Mu, J.; Li, J.; Yao, H.; Chen, K. Cancer Med. 2023, 12, 11149.
[7]
Binnewies, M.; Roberts, E. W.; Krummel, M. F. Nat. Med. 2018, 24, 541.
[8]
de Visser, K. E.; Joyce, J. A. Cancer Cell 2023, 41, 374.
[9]
Junttila, M. R.; de Sauvage, F. J. Nature 2013, 501, 346.
[10]
Kashyap, B. K.; Singh, V. V.; Solanki, M. K.; Kumar, A.; Ruokolainen, J.; Kesari, K. K. ACS Omega 2023, 8, 14290.
[11]
Nirmala, M. J.; Kizhuveetil, U.; Johnson, A.; Balaji, G.; Nagarajan, R.; Muthuvijayan, V. RSC Adv. 2023, 13, 8606.
[12]
Kondo, E.; Iioka, H.; Saito, K. Cancer Sci. 2021, 112, 2118.
[13]
Shim, H. Biomolecules 2020, 10, 360.
[14]
Yan, J.; Gao, T.; Lu, Z.; Yin, J.; Zhang, Y.; Pei, R. ACS Appl. Mater. Interfaces 2021, 13, 27749.
[15]
Mo, T.; Liu, X.; Luo, Y.; Zhong, L.; Zhang, Z.; Li, T.; Gan, L.; Liu, X.; Li, L.; Wang, H.; Sun, X.; Fan, D.; Qian, Z.; Wu, P.; Chen, X. Cancer Sci. 2022, 113, 7.
[16]
Ma, T.; Hou, Y.; Zeng, J.; Liu, C.; Zhang, P.; Jing, L.; Shangguan, D.; Gao, M. J. Am. Chem. Soc. 2018, 140, 211.
[17]
Lin, Y.; Wang, S.; Zhang, Y.; Gao, J.; Hong, L.; Wang, X.; Wu, W.; Jiang, X. J. Mater. Chem. B 2015, 3, 5702.
[18]
Davis, K. M.; Ryan, J. L.; Aaron, V. D.; Sims, J. B. Semin. Ultrasound CT MR 2020, 41, 521.
[19]
Lu, Z. R.; Laney, V.; Li, Y. Acc. Chem. Res. 2022, 55, 2833.
[20]
Nicolescu, C.; Schilb, A.; Kim, J.; Sun, D.; Hall, R.; Gao, S.; Gilmore, H.; Schiemann, W. P.; Lu, Z. R. Chem. Biomed. Eng. 2023, 1, 461.
[21]
Zhu, S.; Tian, R.; Antaris, A. L.; Chen, X.; Dai, H. Adv. Mater. 2019, 31, 1900321.
[22]
Zhao, D.; Cao, J.; Zhang, L.; Zhang, S.; Wu, S. Biosensors (Basel) 2022, 12, 342.
[23]
Merkes, J. M.; Kiessling, F.; Banala, S. Curr. Med. Chem. 2022, 29, 6008.
[24]
Santis, E. D.; Ryadnov, M. G. Chem. Soc. Rev. 2015, 44, 8288.
[25]
Lu, L.; Zhang, Q.; Wang, Z.; Gao, L.; Shen, J. Curr. Med. Chem. 2021, 28, 6411.
[26]
Zhang, C.; Wu, W.; Li, R. Q.; Qiu, W. X.; Zhuang, Z. N.; Cheng, S. X.; Zhang, X. Z. Adv. Funct. Mater. 2018, 28, 1804492.
[27]
Shadidi, M.; Sioud, M. FASEB J. 2023, 17, 256.
[28]
Xing, L.; Xu, Y.; Sun, K.; Wang, H.; Zhang, F.; Zhou, Z.; Zhang, J.; Zhang, F.; Caliskan, B.; Qiu, Z.; Wang, M. Sci. Rep. 2018, 8, 8426.
[29]
Qin, X.; Wan, Y.; Li, M.; Xue, X. C.; Wu, S. Z.; Zhang, C.; You, Y. J.; Wang, W. H.; Jiang, C. L.; Liu, Y.; Zhu, W. H.; Ran, Y. G.; Zhang, Z.; Han, W.; Zhang, Y. Q. J. Biochem. 2007, 142, 79.
[30]
Goldbloom-Helzner, L.; Hao, D.; Wang, A. Int. J. Mol. Sci. 2019, 20, 4072.
[31]
Gong, F.; Yang, N.; Wang, X.; Zhao, Q.; Chen, Q.; Liu, Z.; Cheng, L. Nano Today 2020, 32, 100851.
[32]
Trac, N. T.; Chung, E. J. Bioact. Mater. 2020, 5, 92.
[33]
David, A. Adv. Drug Deliver. Rev. 2017, 119, 120.
[34]
Chen, Y.; Liu, G.; Guo, L.; Wang, H.; Fu, Y.; Luo, Y. Int. J. Cancer 2015, 136, 182.
[35]
Ries, J.; Vairaktaris, E.; Agaimy, A.; Bechtold, M.; Gorecki, P.; Neukam, F. W.; Nkenke, E. Oncol. Rep. 2013, 30, 1149.
[36]
Voron, T.; Colussi, O.; Marcheteau, E.; Pernot, S.; Nizard, M.; Pointet, A. L.; Latreche, S.; Bergaya, S.; Benhamouda, N.; Tanchot, C.; Stockmann, C.; Combe, P.; Berger, A.; Zinzindohoue, F.; Yagita, H.; Tartour, E.; Taieb, J.; Terme, M. J. Exp. Med. 2015, 212, 139.
[37]
Ellis, L. M.; Hicklin, D. J. Nat. Rev. Cancer 2008, 8, 579.
[38]
Jordan, N. V.; Bardia, A.; Wittner, B. S.; Benes, C.; Ligorio, M.; Zheng, Y.; Yu, M.; Sundaresan, T. K.; Licausi, J. A.; Desai, R.; O’Keefe, R. M.; Ebright, R. Y.; Boukhali, M.; Sil, S.; Onozato, M. L.; Iafrate, A. J.; Kapur, R.; Sgroi, D.; Ting, D. T.; Toner, M.; Ramaswamy, S.; Haas, W.; Maheswaran, S.; Haber, D. A. Nature 2016, 537, 102.
[39]
Cao, R.; Li, R.; Shi, H.; Liu, H.; Cheng, Z. Mol. Pharmaceutics 2023, 20, 1394.
[40]
Huang, W.; He, Z.; Cai, X.; Zhang, J.; Li, W.; Wang, K.; Zhang, S. Biosensors 2022, 12, 729.
[41]
Fiacco, S. V.; Kelderhouse, L. E.; Hardy, A.; Peleg, Y.; Hu, B.; Ornelas, A.; Yang, P.; Gammon, S. T.; Howell, S. M.; Wang, P.; Takahashi, T. T.; Millward, S. W.; Roberts, R. W. ChemBioChem 2016, 17, 1643.
[42]
Li, Z.; Zhao, R.; Wu, X.; Sun, Y.; Yao, M.; Li, J.; Xu, Y.; Gu, J. FASEB J. 2005, 19, 1978.
[43]
Huang, W.; Wang, L.; Zhang, H.; Han, Z.; Gu, Y. Sensor. Actuat. B-Chem. 2023, 393, 134102.
[44]
Xu, Y.; Zhao, Y.; Zhang, Y. J.; Cui, Z. F.; Wang, L. H.; Fan, C. H.; Gao, J. M.; Sun, Y. H. Acta Chim. Sinica 2018, 76, 393 (in Chinese).
[44]
(徐毅, 赵彦, 张叶俊, 崔之芬, 王丽华, 樊春海, 高基民, 孙艳红, 化学学报, 2018, 76, 393.)
[45]
Hao, Y.; Luo, J.; Wang, Y.; Li, Z.; Wang, X.; Yan, F. Biomaterials 2023, 293, 121974.
[46]
Xie, W.; Yang, P.; Zeng, X.; Wang, H.; Cai, H.; Cai, J. Chin. Sci. Bull. 2010, 55, 2390.
[47]
Staquicini, F. I.; Ozawa, M. G.; Moya, C. A.; Driessen, W. H. P.; Barbu, E. M.; Nishimori, H.; Soghomonyan, S.; Flores, L. G.; Liang, X.; Paolillo, V.; Alauddin, M. M.; Basilion, J. P.; Furnari, F. B.; Bogler, O.; Lang, F. F.; Aldape, K. D.; Fuller, G. N.; H??k, M.; Gelovani, J. G.; Sidman, R. L.; Cavenee, W. K.; Pasqualini, R.; Arap, W. J. Clin. Invest. 2011, 121, 161.
[48]
Su, C. Y.; Huang, G. C.; Chang, Y. C.; Chen, Y. J.; Fang, H. W. In Vivo 2021, 35, 1545.
[49]
Hou, Y.; Zou, Q.; Ge, R.; Shen, F.; Wang, Y. Cell Res. 2012, 22, 259.
[50]
Zhang, D.; Jia, H.; Wang, Y.; Li, W. M.; Hou, Y. C.; Yin, S. W.; Wang, T. D.; He, S. X.; Lu, S. Y. Biotechnol. Lett. 2015, 37, 2311.
[51]
Wang, Z.; Zhao, C.; Li, Y.; Wang, J.; Hou, D.; Wang, L.; Wang, Y.; Wang, X.; Liu, X.; Wang, H.; Xu, W. Adv. Mater. 2023, 35, 2210732.
[52]
Sun, J.; Zhang, C.; Liu, G.; Liu, H.; Zhou, C.; Lu, Y.; Zhou, C.; Yuan, L.; Li, X. Clin. Exp. Metastasis 2012, 29, 185.
[53]
Wang, Y.; Yan, K.; Wang, J.; Lin, J.; Bi, J. Front. Oncol. 2021, 11, 609334.
[54]
Cieslewicz, M.; Tang, J.; Yu, J. L.; Cao, H.; Zavaljevski, M.; Motoyama, K.; Lieber, A.; Raines, E. W.; Pun, S. H. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 15919.
[55]
Huang, M.; Wang, R.; Li, M.; Cai, H.; Tian, R. Pharmaceutics 2022, 14, 2511.
[56]
Scodeller, P.; Simón-Gracia, L.; Kopanchuk, S.; Tobi, A.; Kilk, K.; S??lik, P.; Kurm, K.; Squadrito, M. L.; Kotamraju, V. R.; Rinken, A.; De Palma, M.; Ruoslahti, E.; Teesalu, T. Sci. Rep. 2017, 7, 14655.
[57]
Ou, W.; Thapa, R. K.; Jiang, L.; Soe, Z. C.; Gautam, M.; Chang, J. H.; Jeong, J. H.; Ku, S. K.; Choi, H. G.; Yong, C. S.; Kim, J. O. J. Control. Release 2018, 281, 84.
[58]
Curiel, T. J.; Morris, C.; Brumlik, M.; Landry, S. J.; Finstad, K.; Nelson, A.; Joshi, V.; Hawkins, C.; Alarez, X.; Lackner, A.; Mohamadzadeh, M. J. Immunol. 2004, 172, 7425.
[59]
Ihanus, E.; Uotila, L. M.; Toivanen, A.; Varis, M.; Gahmberg, C. G. Blood 2007, 109, 802.
[60]
McDonald, D. M.; Baluk, P. Cancer Res. 2002, 62, 5381.
[61]
Maishi, N.; Hida, K. Cancer Sci. 2017, 108, 1921.
[62]
Christian, S.; Pilch, J.; Akerman, M. E.; Porkka, K.; Laakkonen, P.; Ruoslahti, E. J. Cell Biol. 2003, 163, 871.
[63]
Zheng, Y.; Gao, S.; Ying, J. Y. Adv. Mater. 2007, 19, 376.
[64]
Pasqualini, R.; Koivunen, E.; Ruoslahti, E. Nat. Biotechnol. 1997, 15, 542.
[65]
Zhu, H.; Li, N.; Lin, X.; Hong, Y.; Yang, Z. Acta Chim. Sinica 2014, 72, 427 (in Chinese).
[65]
(朱华, 李囡, 林新峰, 洪业, 杨志, 化学学报, 2014, 72, 427.)
[66]
Liu, X.; Wang, F.; Liu, L.; Li, T.; Zhong, X.; Lin, H.; Zhang, Y.; Xue, W. Biosens. Bioelectron. 2023, 222, 114995.
[67]
Xiao, W.; Wang, Y.; Lau, E. Y.; Luo, J.; Yao, N.; Shi, C.; Meza, L.; Tseng, H.; Maeda, Y.; Kumaresan, P.; Liu, R.; Lightstone, F. C.; Takada, Y.; Lam, K. S. Mol. Cancer Ther. 2010, 9, 2714.
[68]
Wang, Q.; Yan, H.; Jin, Y.; Wang, Z.; Huang, W.; Qiu, J.; Kang, F.; Wang, K.; Zhao, X.; Tian, J. Biomaterials 2018, 183, 173.
[69]
Liu, W.; Ma, H.; Li, F.; Cai, H.; Liang, R.; Chen, X.; Lan, T.; Yang, J.; Liao, J.; Yang, Y.; Liu, N. Bioorg. Med. Chem. 2022, 59, 116677.
[70]
Nissen, N. I.; Karsdal, M.; Willumsen, N. J. Exp. Clin. Cancer Res. 2019, 38, 115.
[71]
Xu, S.; Xu, H.; Wang, W.; Li, S.; Li, H.; Li, T.; Zhang, W.; Yu, X.; Liu, L. J. Transl. Med. 2019, 17, 309.
[72]
Lepp?nen, J.; Lindholm, V.; Isohookana, J.; Haapasaari, K. M.; Karihtala, P.; Lehenkari, P. P.; Saarnio, J.; Kauppila, J. H.; Karttunen, T. J.; Helminen, O.; Huhta, H. Pancreas 2019, 48, 43.
[73]
Van Obberghen-Schilling, E.; Tucker, R. P.; Saupe, F.; Gasser, I.; Cseh, B.; Orend, G. Int. J. Dev. Biol. 2011, 55, 511.
[74]
Qiao, P.; Lu, Z. R. Adv. Exp. Med. Biol. 2020, 1245, 85.
[75]
Costantini, V.; Zacharski, L. R. Cancer Metastasis Rev. 1992, 11, 283.
[76]
Wang, A. Y.; Mo, X.; Chen, C. S.; Yu, S. M. J. Am. Chem. Soc. 2005, 127, 4130.
[77]
Bennink, L. L.; Li, Y.; Kim, B.; Shin, I. J.; San, B. H.; Zangari, M.; Yoon, D.; Yu, S. M. Biomaterials 2018, 183, 67.
[78]
Li, Y.; Foss, C. A.; Summerfield, D. D.; Doyle, J. J.; Torok, C. M.; Dietz, H. C.; Pomper, M. G.; Yu, S. M. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 14767.
[79]
Cai, X.; Wei, W.; Liu, Z.; Bai, Z; Lei, J.; Xiao, J. ACS Appl. Bio Mater. 2020, 3, 7492.
[80]
Wei, W.; Li, D.; Cai, X.; Liu, Z.; Bai, Z.; Xiao, J. J. Mater. Chem. B 2020, 8, 10093.
[81]
Cai, X.; Wei, W.; Bi, Y.; Liu, Z.; Bai, Z.; Lei, J.; Xiao, J. Adv. Funct. Mater. 2020, 30, 2004532.
[82]
Kuhnast, B.; Bodenstein, C.; Haubner, R.; Wester, H. J.; Senekowitsch-Schmidtke, R.; Schwaiger, M.; Weber, W. A. Nucl. Med. Biol. 2004, 31, 337.
[83]
Sprague, J. E.; Li, W. P.; Liang, K.; Achilefu, S.; Anderson, C. J. Nucl. Med. Biol. 2006, 33, 227.
[84]
Zhu, L.; Wang, H.; Wang, L.; Wang, Y.; Jiang, K.; Li, C.; Ma, Q.; Gao, S.; Wang, L.; Li, W.; Cai, M.; Wang, H.; Niu, G.; Lee, S.; Yang, W.; Fang, X.; Chen, X. J. Control. Release 2011, 150, 248.
[85]
Li, X.; Ma, Z.; Wang, H.; Ren, L.; Zhang, D.; Liang, W.; Zhang, G.; Zhang, J.; Yu, D.; Fang, X. Bioconjug. Chem. 2019, 30, 1507.
[86]
Ren, L.; Li, Q.; Ma, Z.; Wang, Y.; Li, H.; Shen, L.; Yu, J.; Fang, X. J. Mater. Chem. B 2018, 6, 7719.
[87]
Starmans, L. W. E.; van Mourik, T.; Rossin, R.; Verel, I.; Nicolay, K.; Grüll, H. Mol. Pharm. 2015, 12, 1921.
[88]
Kim, M. Y.; Kim, O. R.; Choi, Y. S.; Lee, H.; Park, K.; Lee, C. T.; Kang, K. W.; Jeong, S. Mol. Cells 2012, 33, 71.
[89]
Han, Z.; Zhou, Z.; Shi, X.; Wang, J.; Wu, X.; Sun, D.; Chen, Y.; Zhu, H.; Magi-Galluzzi, C.; Lu, Z. R. Bioconjug. Chem. 2015, 26, 830.
[90]
Zhou, Z.; Qutaish, M.; Han, Z.; Schur, R. M.; Liu, Y.; Wilson, D. L.; Lu, Z. R. Nat. Commun. 2015, 6, 7984.
[91]
Zhou, Z.; Wu, X.; Kresak, A.; Griswold, M.; Lu, Z. R. Biomaterials 2013, 34, 7683.
[92]
Zhou, Z.; Lu, Z. R. Adv. Drug Deliver. Rev. 2017, 113, 24.
[93]
Gao, C.; Tang, F.; Gong, G.; Zhang, J.; Hoi, M. P. M.; Lee, S. M. Y.; Wang, R. Nanoscale 2017, 9, 12533.
[94]
Dharmaratne, N. U.; Kaplan, A. R.; Glazer, P. M. Cells 2021, 10, 541.
[95]
Reshetnyak, Y. K.; Yao, L.; Zheng, S.; Kuznetsov, S.; Engelman, D. M.; Andreev, O. A. Mol. Imaging Biol. 2011, 13, 1146.
[96]
Andreev, O. A.; Dupuy, A. D.; Segala, M.; Sandugu, S.; Serra, D. A.; Chichester, C. O.; Engelman, D. M.; Reshetnyak, Y. K. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 7893.
[97]
Demoin, D. W.; Wyatt, L. C.; Edwards, K. J.; Abdel-Atti, D.; Sarparanta, M.; Pourat, J.; Longo, V. A.; Carlin, S. D.; Engelman, D. M.; Andreev, O. A.; Reshetnyak, Y. K.; Viola-Villegas, N.; Lewis, J. S. Bioconjug. Chem. 2016, 27, 2014.
[98]
Crawford, T.; Moshnikova, A.; Roles, S.; Weerakkody, D.; DuPont, M.; Carter, L. M.; Shen, J.; Engelman, D. M.; Lewis, J. S.; Andreev, O. A.; Reshetnyak, Y. K. Sci. Rep. 2020, 10, 18356.
[99]
Moyer, T. J.; Finbloom, J. A.; Chen, F.; Toft, D. J.; Cryns, V. L.; Stupp, S. I. J. Am. Chem. Soc. 2014, 136, 14746.
[100]
Myochin, T.; Hanaoka, K.; Komatsu, T.; Terai, T.; Nagano, T. J. Am. Chem. Soc. 2012, 134, 13730.
[101]
Liu, Y.; Zhang, D.; Qiao, Z. Y.; Qi, G. B.; Liang, X. J.; Chen, X. G.; Wang, H. Adv. Mater. 2015, 27, 5034.
[102]
Sun, L.; Xie, S.; Qi, J.; Liu, E.; Liu, D.; Liu, Q.; Chen, S.; He, H.; Yang, V. C. ACS Appl. Mater. Interfaces 2017, 9, 39209.
[103]
Ma, P.; Chen, J.; Bi, X.; Li, Z.; Gao, X.; Li, H.; Zhu, H.; Huang, Y.; Qi, J.; Zhang, Y. ACS Appl. Mater. Interfaces 2018, 10, 12351.
[104]
Kasten, B. B.; Jiang, K.; Cole, D.; Jani, A.; Udayakumar, N.; Gillespie, G. Y.; Lu, G.; Dai, T.; Rosenthal, E. L.; Markert, J. M.; Rao, J.; Warram, J. M. Eur. J. Nucl. Med. Mol. Imaging 2020, 47, 1412.
[105]
Chen, X.; Lee, D.; Yu, S.; Kim, G.; Lee, S.; Cho, Y.; Jeong, H.; Nam, K. T.; Yoon, J. Biomaterials 2017, 122, 130.
[106]
Kisin-Finfer, E.; Ferber, S.; Blau, R.; Satchi-Fainaro, R.; Shabat, D. Bioorg. Med. Chem. Lett. 2014, 24, 2453.
[107]
Shi, W.; Ogbomo, S. M.; Wagh, N. K.; Zhou, Z.; Jia, Y.; Brusnahan, S. K.; Garrison, J. C. Biomaterials 2014, 35, 5760.
[108]
Kim, J.; Won, Y.; Goh, S. H.; Choi, Y. J. Mater. Chem. B 2016, 4, 6787.
[109]
Cai, Z.; Wang, A.; Wang, Y.; Qiu, Z.; Li, Y.; Yan, H.; Fu, M.; Liu, M.; Yu, Y.; Gao, F. Anal. Chem. 2022, 94, 9715.
[110]
Wang, X.; Xia, Y.; Liu, Y.; Qi, W.; Sun, Q.; Zhao, Q.; Tang, B. Chemistry 2012, 18, 7189.
[111]
Huang, S.; Shao, K.; Liu, Y.; Kuang, Y.; Li, J.; An, S.; Guo, Y.; Ma, H.; Jiang, C. ACS Nano 2013, 7, 2860.
[112]
Qiao, Z. Y.; Zhao, W. J.; Gao, Y. J.; Cong, Y.; Zhao, L.; Hu, Z.; Wang, H. ACS Appl. Mater. Interfaces 2017, 9, 30426.
[113]
Mohtavinejad, N.; Shafiee Ardestani, M.; Khalaj, A.; Pormohammad, A.; Najafi, R.; Bitarafan-Rajabi, A.; Hajiramezanali, M.; Amanlou, M. Life Sci. 2020, 258, 118206.
[114]
Khalily, M. P.; Soydan, M. Chem. Biol. Drug Des. 2023, 101, 772.
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