Triarylphosphonium compounds as effective vectors for mitochondria-targeted delivery systems: decoration strategies and prospects for clinical application

Cover Page

Cite item

Full Text

Abstract

Mitochondrial dysfunctions lead to the emergence and development of a large number of diseases. The present review gives the first systematic survey of various aspects of studies of mitochondria-targeted nanosystems containing triphenylphosphonium vector groups providing targeted delivery of drug substances to these organelles. Approaches to the design of both the initial triphenylphosphonium components and various nanoparticles bearing these groups are summarized and analyzed. The relationship between the key parameters of triphenylphosphonium nanoparticles (chemical composition, size, shape, ζ-potential, drug loading, drug encapsulation efficiency, etc.) and the biological action is discussed; in some cases, the mechanism of mitochondria targeting is presented. The design principles and preparation methods for mitochondria-targeted triphenylphosphonium delivery nanosystems are of interest to researchers specializing in the field of nanomaterials, nanotechnology, molecular biology, biotechnology and pharmaceutical chemistry. Bibliography — 243 references.

About the authors

Tatiana Nikandrovna Pashirova

A. E. Arbuzov Institute of Organic and Physical Chemistry of Kazan Scientific Center of Russian Academy of Sciences

ORCID iD: 0000-0002-2001-1570

Andrey Vladimirovich Nemtarev

A. E. Arbuzov Institute of Organic and Physical Chemistry of Kazan Scientific Center of Russian Academy of Sciences

ORCID iD: 0000-0001-8478-2705

E. B. Souto

University of Porto

ORCID iD: 0000-0002-9737-6017

Vladimir Fedorovich Mironov

A. E. Arbuzov Institute of Organic and Physical Chemistry of Kazan Scientific Center of Russian Academy of Sciences

Email: mironov@iopc.ru
ORCID iD: 0000-0002-4198-3774
Doctor of chemical sciences, Professor

References

  1. W.G.Bottje. In Sturkie's Avian Physiology. (7th Edn). (Eds C.G.Scanes, S.Dridi). (New York: Academic Press, 2022). P. 65
  2. R.Keshet, P.Szlosarek, A.Carracedo, A.Erez. Nat. Rev. Cancer, 18, 634 (2018)
  3. S.Matsumoto, J.Häberle, J.Kido, H.Mitsubuchi, F.Endo, K.Nakamura. J. Hum. Genet., 64, 83 (2019)
  4. I.B.Zavodnik. Biomed. Khim., 62, 311 (2016)
  5. J.F.Garbincius, J.W.Elrod. Physiol. Rev., 102, 893 (2022)
  6. M.B.Rone, J.Fan, V.Papadopoulos. Biochim. Biophys. Acta, 1791, 646 (2009)
  7. V.Papadopoulos, W.L.Miller. Best Pr. Res. Clin. Endocrinol. Metab ., 26, 771 (2012)
  8. W.L.Miller. Mol. Cell. Endocrinol., 379, 62 (2013)
  9. G.Bassi, S.K.Sidhu, S.Mishra. Cells, 10, 1851 (2021)
  10. L.Wang. Nucleosides Nucleotides Nucleic Acids, 35, 578 (2016)
  11. M.Löffler, E.A.Carrey, W.Knecht. Nucleosides Nucleotides Nucleic Acids, 39, 1281 (2020)
  12. H.Vakifahmetoglu-Norberg, A.T.Ouchida, E.Norberg. Biochem. Biophys. Res. Commun., 482, 426 (2017)
  13. F.J. Bock, S.W.G.Tait. Nat. Rev. Mol. Cell Biol., 21, 85 (2020)
  14. M.Abate, A.Festa, M.Falco, A.Lombardi, A.Luce, A.Grimaldi, S.Zappavigna, P.Sperlongano, C.Irace, M.Caraglia, G.Misso. Semin. Cell Dev. Biol., 98, 139 (2020)
  15. S.Dadsena, L.E.King, A.J.García-Sáez. Biochim. Biophys. Acta — Biomembranes, 1863, 183716 (2021)
  16. S.Javadov. Curr. Opin. Physiol., 25, 100483 (2022)
  17. J.B.Spinelli, M.C.Haigis. Nat. Cell Biol., 20, 74 (2018)
  18. C.-H.Wang, Y.-H.Wei. Int. J. Mol. Sci., 21, 5266 (2020)
  19. L.A.Videla, A.Marimán, B.Ramos, M.José Silva, A.del Campo. Mitochondrion, 63, 9 (2022)
  20. L.R.Rodríguez, T.Lapeña-Luzón, N.Benetó, V.Beltran-Beltran, F.V.Pallardó, P.Gonzalez-Cabo, J.A.Navarro. Antioxidants, 11, 165 (2022)
  21. M.Verma, B.N.Lizama, C.T.Chu. Transl. Neurodegener., 11, 3 (2022)
  22. E.Trushina, S.Trushin, M.F.Hasan. Acta Pharm. Sin. B, 12, 483 (2022)
  23. S.Ozgen, J.Krigman, R.Zhang, N.Sun. Neural Regen. Res., 17, 741 (2022)
  24. K.Zambrano, D.Barba, K.Castillo, P.Robayo, D.Argueta-Zamora, S.Sanon, E.Arizaga, A.Caicedo, A.W.D.Gavilanes. Mitochondrion, 64, 125 (2022)
  25. I.V.Shemarova, S.M.Korotkov, V.P.Nesterov. J. Evol. Biochem. Physiol., 56, 304 (2020)
  26. R.K.Sharma, A.Chafik, G.Bertolin. Am. J. Physiol. Physiol., 322, 311 (2022)
  27. H.Tian, X.Chen, J.Liao, T.Yang, S.Cheng, Z.Mei, J.Ge. J. Cell. Mol. Med., 26, 1000 (2022)
  28. A.Ludhiadch, R.Sharma, A.Muriki, A.Munshi. CNS Neurol. Disord. Drug Targets, 21, 52 (2022)
  29. S.A.Dabravolski, V.A.Khotina, V.N.Sukhorukov, V.A.Kalmykov, L.M.Mikhaleva, A.N.Orekhov. Int. J. Mol. Sci., 23, 952 (2022)
  30. J.A. Amorim, G.Coppotelli, A.P.Rolo, C.M.Palmeira, J.M.Ross, D.A.Sinclair. Nat. Rev. Endocrinol., 18, 243 (2022)
  31. A.Ravindranath, M.SenSarma. World J. Hepatol., 14, 180 (2022)
  32. Y.Yoon, C.A.Galloway, B.S.Jhun, T.Yu. Antioxid. Redox Signal., 14, 439 (2011)
  33. J.Gollmer, A.Zirlik, H.Bugger. Diabetes Metab. J., 44, 33 (2020)
  34. S.Demir, P.P.Nawroth, S.Herzig, B.E.Üstünel. Adv. Sci., 8, e2100275 (2021)
  35. L.Yao, X.Liang, Y.Qiao, B.Chen, P.Wang, Z.Liu. Metabolism, 131, 155195 (2022)
  36. W.Dai, H.Lu, Y.Chen, D.Yang, L.Sun, L.He. Front. Cell Dev. Biol., 9, 706832 (2021)
  37. M.Ito, M.Z.Gurumani, S.Merscher, A.Fornoni. Biomolecules, 12, 351 (2022)
  38. S.Mani, G.Swargiary, S.J.Ralph. Mitochondrion, 62, 50 (2022)
  39. P.J.Burke. Trends Cancer, 3, 857 (2017)
  40. B.A.Carneiro, W.S.El-Deiry. Nat. Rev. Clin. Oncol., 17, 395 (2020)
  41. C.Garcia-Ruiz, L.Conde de la Rosa, V.Ribas, J.C.Fernandez-Checa. Semin. Cancer Biol., 73, 76 (2021)
  42. E.Hajaj, M.Sciacovelli, C.Frezza, A.Erez. Mol. Cell, 81, 3749 (2021)
  43. S.Vyas, E.Zaganjor, M.C.Haigis. Cell, 166, 555 (2016)
  44. D.Grasso, L.X.Zampieri, T.Capelôa, J.A.VandeVelde, P.Sonveaux. Cell Stress, 4, 114 (2020)
  45. M.van der Merwe, G.van Niekerk, C.Fourie, M.du Plessis, A.-M.Engelbrecht. Cell. Oncol. 44, 983 (2021)
  46. X.Guo, N.Yang, W.Ji, H.Zhang, X.Dong, Z.Zhou, L.Li, H.Shen, S.Q.Yao, W.Huang. Adv. Mater., 33, е2007778 (2021)
  47. J.Patel, B.A.Baptiste, E.Kim, M.Hussain, D.L.Croteau, V.A.Bohr. Carcinogenesis, 41, 1625 (2020)
  48. E.E.Newton, L.E.Mueller, S.M.Treadwell, C.A.Morris, H.L.Machado. Cancers (Basel), 14, 482 (2022)
  49. N.M.Almansour. Front. Mol. Biosci., 9, 836417 (2022)
  50. J.W.Smithy, E.M.O’Reilly. J. Surg. Oncol., 123, 1475 (2021)
  51. J.Xu, J.G.Shamul, E.A.Kwizera, X.He. Nanomaterials, 12, 743 (2022)
  52. T.A.Tabish, M.R.Hamblin. Biomater. Biosyst., 3, 100023 (2021)
  53. Z.He, Y.Zhang, A.R.Khan, J.Ji, A.Yu, G.Zhai. J. Drug Target., 29, 12 (2021)
  54. S.Mani, G.Swargiary, S.Tyagi, M.Singh, N.K.Jha, K.K.Singh. Life Sci., 281, 119773 (2021)
  55. J.Qin, N.Gong, Z.Liao, S.Zhang, P.Timashev, S.Huo, X.-J.Liang. Nanoscale, 13, 7108 (2021)
  56. D.Choudhary, H.Goykar, T.Karanwad, S.Kannaujia, V.Gadekar, M.Misra. Asian J. Pharm. Sci., 16, 397 (2021)
  57. L.Huang, Z.Sun, Q.Shen, Z.Huang, S.Wang, N.Yang, G.Li, Q.Wu, W.Wang, L.Li, C.Yu. Chin. Chem. Lett., 33, 4146 (2022)
  58. T.I.Rokitskaya, E.V.Aleksandrova, G.A.Korshunova, L.S.Khailova, V.N.Tashlitsky, V.B.Luzhkov, Y.N.Antonenko. J. Phys. Chem. B, 126, 412 (2022)
  59. X.Fu, Y.Shi, T.Qi, S.Qiu, Y.Huang, X.Zhao, Q.Sun, G.Lin. Signal Transduct. Target. Ther., 5, 262 (2020)
  60. C.A.Kulkarni, B.D.Fink, B.E.Gibbs, P.R.Chheda, M.Wu, W.I.Sivitz, R.J.Kerns. J. Med. Chem., 64, 662 (2021)
  61. V.F.Mironov, A.V.Nemtarev, O.V.Tsepaeva, M.N.Dimukhametov, I.A.Litvinov, A.D.Voloshina, T.N.Pashirova, E.A.Titov, A.P.Lyubina, S.K.Amerhanova, A.T.Gubaidullin, D.R. Islamov. Molecules, 26, 6350 (2021)
  62. R.John, B.Dalal, A.Shankarkumar, P.V.Devarajan. Int. J. Pharm., 600, 120511 (2021)
  63. O.V.Tsepaeva, A.V.Nemtarev, T.I.Salikhova, T.I.Abdullin, L.R.Grigor`eva, S.A.Khozyainova, V.F.Mironov. Anticancer. Agents Med. Chem., 20, 286 (2020)
  64. O.V.Tsepaeva, T.I.Salikhova, L.R.Grigor’eva, D.V.Ponomaryov, T.Dang, R.A.Ishkaeva, T.I.Abdullin, A.V.Nemtarev, V.F. Mironov. Med. Chem. Res., 30, 925 (2021)
  65. G.Xu, X.Xu, J.Liu, Q.Jia, C.Ke, H.Zhang, C.Xu, E.Ou, W.Tan, Y.Zhao. ChemMedChem, 17, e202100659 (2022)
  66. L.Wang, M.Yao, Y.Hu, C.Chen, L.Jin, X.Ma, H.Yang. ACS Med. Chem. Lett., 13, 786 (2022)
  67. D.V.Tsyganov, A.V.Samet, E.A.Silyanova, V.I.Ushkarov, A.E.Varakutin, N.B.Chernysheva, R.N.Chuprov-Netochin, A.A.Khomutov, A.S.Volkova, S.V.Leonov, M.N.Semenova, V.V. Semenov. ACS Omega, 7, 3369 (2022)
  68. J.S.Armstrong. Br. J. Pharmacol., 151, 1154 (2007)
  69. M.Edeas, V.Weissig. Mitochondrion, 13, 389 (2013)
  70. L.Milane, S.Dolare, T.Jahan, M.Amiji. Nanomed.: Nanotechnol. Biol. Med., 37, 102422 (2021)
  71. Organelle-Specific Pharmaceutical Nanotechnology. (Eds V.Weissig, G.G.M.D’Souza). (Hoboken: Wiley, 2010)
  72. R.W.Horobin, S.Trapp, V.Weissig. J. Control. Release, 121, 125 (2007)
  73. M.J.Rossman, J.R.Santos-Parker, C.A.C.Steward, N.Z.Bispham, L.M.Cuevas, H.L.Rosenberg, K.A.Woodward, M.Chonchol, R.A.Gioscia-Ryan, M.P.Murphy, D.R.Seals. Hypertension, 71, 1056 (2018)
  74. S.-Y.Park, E.J.Pekas, R.J.Headid, W.-M.Son, T.K.Wooden, J.Song, G.Layec, S.K.Yadav, P.K.Mishra, I.I.Pipinos. Am. J. Physiol. Circ. Physiol., 319, H456 (2020)
  75. V.Weissig, S.V.Boddapati, S.-M.Cheng, G.G.M.D’Souza. J. Liposome Res., 16, 249 (2006)
  76. A.T.Hoye, J.E.Davoren, P.Wipf, M.P.Fink, V.E.Kagan. Acc. Chem. Res., 41, 87 (2008)
  77. C.M. Paleos, D.Tsiourvas, Z.Sideratou. Mol. Pharm., 13, 2233 (2016)
  78. S.S.Liew, X.Qin, J.Zhou, L.Li, W.Huang, S.Q.Yao. Angew. Chem., Int. Ed., 60, 2232 (2021)
  79. K.S.Allemailem, A.Almatroudi, M.A.Alsahli, A.Aljaghwani, A.MEl-Kady, A.H.Rahmani, A.A.Khan. Int. J. Nanomed., 16, 3907 (2021)
  80. Y.Yamada, Satrialdi, M.Hibino, D.Sasaki, J.Abe, H.Harashima. Adv. Drug Deliv. Rev., 154–155, 187 (2020)
  81. C.Wang, F.Li, T.Zhang, M.Yu, Y.Sun. Drug Deliv., 29, 1684 (2022)
  82. S.Buchke, M.Sharma, A.Bora, M.Relekar, P.Bhanu, J.Kumar. Life, 12, 657 (2022)
  83. P.Mi, H.Cabral, K.Kataoka. Adv. Mater., 32, 1902604 (2020)
  84. S.Tran, P.J.De Giovanni, B.Piel, P.Rai. Clin. Transl. Med., 6, 44 (2017)
  85. A.A.Khan, K.S.Allemailem, A.Almatroudi, S.A.Almatroodi, M.A.Alsahli, A.H.Rahmani. J. Drug Deliv. Sci. Technol., 61, 102315 (2021)
  86. J.Zielonka, J.Joseph, A.Sikora, M.Hardy, O.Ouari, J.Vasquez-Vivar, G.Cheng, M.Lopez, B.Kalyanaraman. Chem. Rev., 117, 10043 (2017)
  87. N.R.Khasiyatullina, V.F.Mironov, S.K.Gumerova, A.D.Voloshina, A.S.Sapunova. Mendeleev Commun., 29, 435 (2019)
  88. N.R.Khasiyatullina, V.F.Mironov, A.D.Voloshina, A.S.Sapunova. Chem. Biodiv., 16, e1900039 (2019)
  89. M.E.Shemakhina, A.V.Nemtarev, R.R.Fayzullin, N.R.Khasiyatullina, L.R.Grigor’eva, V.F.Mironov. Mendeleev Commun., 30, 700 (2020)
  90. C.Larpent, H.Patin. Tetrahedron, 44, 6107 (1988)
  91. C.Lim. Adv. Drug Deliv. Rev., 59, 697 (2007)
  92. Y.Shi, Z.Luo, J.You. WIREs Nanomed. Nanobiotechnol., 14, e1803 (2022)
  93. S.V.Boddapati, P.Tongcharoensirikul, R.N.Hanson, G.G.M.D’Souza, V.P.Torchilin, V.Weissig. J. Liposome Res., 15, 49 (2005)
  94. S.V.Boddapati, G.G.M.D’Souza, S.Erdogan, V.P.Torchilin, V.Weissig. Nano Lett., 8, 2559 (2008)
  95. N.R.Patel, S.Hatziantoniou, A.Georgopoulos, C.Demetzos, V.P.Torchilin, V.Weissig, G.G.M.D’Souza. J. Liposome Res., 20, 244 (2010)
  96. M.A.Solomon, A.A.Shah, G.G.M.D’Souza. Mitochondrion, 13, 464 (2013)
  97. J.Alizadeh, S.C.da Silva Rosa, X.Weng, J.Jacobs, S.Lorzadeh, A.Ravandi, R.Vitorino, S.Pecic, A.Zivkovic, H.Stark, S.Shojaei, S.Ghavami. Eur. J. Cell Biol., 102, 151337 (2023)
  98. D.A.Kuznetsova, G.A.Gaynanova, L.A.Vasileva, G.V.Sibgatullina, D.V.Samigullin, A.S.Sapunova, A.D.Voloshina, I.V.Galkina, K.A.Petrov, L.Y.Zakharova. J. Mater. Chem. B, 7, 7351 (2019)
  99. D.A.Kuznetsova, L.A.Vasileva, G.A.Gaynanova, R.V.Pavlov, A.S.Sapunova, A.D.Voloshina, G.V.Sibgatullina, D.V.Samigullin, K.A.Petrov, L.Y.Zakharova, O.G.Sinyashin. J. Mol. Liq., 330, 115703 (2021)
  100. V.P. Torchilin. Nat. Rev. Drug Discov., 13, 813 (2014)
  101. S.Shah, M.Ouellette, G.G.M.D’Souza. 4open, 5, 6 (2022)
  102. J.Di Gregorio, S.Petricca, R.Iorio, E.Toniato, V.Flati. Eur. J. Cell Biol., 101, 151225 (2022)
  103. P.Benein, M.A.Almuteri, A S.Mehanna, G.G.M.D’Souza. In Mitochondrial Medicine. Manipulating Mitochondrial Function. Vol. II. (Eds V.Weissig, M.Edeas). (New York: Springer Humana, 2015). P. 51
  104. P.Benien, M.A.Solomon, P.Nguyen, E.M.Sheehan, A.S.Mehanna, G.G.M.D’Souza. J. Liposome Res., 26, 21 (2016)
  105. L.Jiang, S.Zhou, X.Zhang, C.Li, S.Ji, H.Mao, X.Jiang. Nat. Commun., 12, 2390 (2021)
  106. J.Pendhari, H.Savla, D.Bethala, S.Vaidya, U.Shinde, M.Menon. J. Drug Deliv. Sci. Technol., 76, 103795 (2022)
  107. S.Xiao, S.Huang, X.Yang, Y.Lei, M.Chang, J.Hu, Y.Meng, G.Zheng, X.Chen. Drug Deliv., 30, 2162156 (2023)
  108. P.-W.Shueng, L.-Y.Yu, H.-H.Hou, H.-C.Chiu, C.-L. Lo. Int. J. Mol. Sci., 23, 3080 (2022)
  109. S.Biswas, N.S.Dodwadkar, P.P.Deshpande, V.P.Torchilin. J. Control. Release, 159, 393 (2012)
  110. J.H.Kang, Y.T.Ko. Pharmaceutics, 11, 423 (2019)
  111. C.Yue, Y.Yang, J.Song, G.Alfranca, C.Zhang, Q.Zhang, T.Yin, F.Pan, J.M.de la Fuente, D.Cui. Nanoscale, 9, 11103 (2017)
  112. J.He, D.Liu, L.Zhao, D.Zhou, J.Rong, L.Zhang, Z.Xia. Exp. Ther. Med., 23, 430 (2022)
  113. F.Li, Y.Wang, W.Li, J.Wu, S.Li, X.Hu, T.Tang, X.Liu. J. Liposome Res., 33, 1 (2023). https://doi.org/10.1080/08982104.2023.2193845
  114. L.Kennedy, J.K.Sandhu, M.E.Harper, M. Cuperlovic-Culf. Biomolecules, 10, 1429 (2020)
  115. Y.Peng, J.Lu, R.Li, Y.Zhao, L.Hai, L.Guo, Y.Wu. ACS Appl. Mater. Interfaces, 13, 26682 (2021)
  116. B.Kapoor, R.Gupta, S.K.Singh, M.Gulati, S.Singh. Adv. Colloid Interface Sci., 253, 35 (2018)
  117. H.M.Cochemé, G.F.Kelso, A.M.James, M.F.Ross, J.Trnka, T.Mahendiran, J.AsinCayuela, F.H.Blaikie, A.R.B.Manas, C.M.Porteous, V.J.Adlam, R.A.J.Smith, M.P.Murphy. Mitochondrion, 7, 94 (2007)
  118. R.A.J.Smith, M.P.Murphy. Ann. N.Y. Acad. Sci., 1201, 96 (2010)
  119. K.J.Botting, K.L.Skeffington, Y.Niu, B.J.Allison, K.L.Brain, N.Itani, C.Beck, A.Logan, A.J.Murray, M.P.Murphy, D.A.Giussani. Sci. Adv., 6, eabb1929 (2020)
  120. R.J.Perry, T.Kim, X.-M.Zhang, H.-Y.Lee, D.Pesta, V.B.Popov, D.Zhang, Y.Rahimi, M.J.Jurczak, G.W.Cline, D.A.Spiegel, G.I.Shulman. Cell Metab., 18, 740 (2013)
  121. M.Wu, L.Liao, L.Jiang, C.Zhang, H.Gao, L.Qiao, S.Liu, D. Shi. Biomaterials, 222, 119457 (2019)
  122. J.Zhou, W.-Y.Zhao, X.Ma, R.-J.Ju, X.-Y.Li, N.Li, M.-G.Sun, J.-F.Shi, C.-X.Zhang, W.-L.Lu. Biomaterials, 34, 3626 (2013)
  123. J.Zhang, C.Yang, S.Pan, M.Shi, J.Li, H.Hu, M.Qiao, D.Chen, X.Zhao. Drug Deliv., 25, 723 (2018)
  124. S.Wang, Z.Zhou, R.Hu, M.Dong, X.Zhou, S.Ren, Y.Zhang, C.Chen, R.Huang, M.Zhu, W.Xie, L.Han, J.Shen, C.Xie. Adv. Sci., 10, 2207608 (2023)
  125. X.Wang, H.Cai, X.Huang, Z.Lu, L.Zhang, J.Hu, D.Tian, J.Fu, G.Zhang, Y.Meng, G.Zheng, C.Chang. J. Biomater. Sci., Polym. Ed., (2023) (in the press)
  126. Y.Han, C.Gao, H.Wang, J.Sun, M.Liang, Y.Feng, Q.Liu, S.Fu, L.Cui, C.Gao, Y.Li, Y.Yang, B.Sun. Bioact. Mater., 6, 529 (2021)
  127. P.Karunanidhi, N.Verma, D.N.Kumar, A.K.Agrawal, S.Singh. AAPS PharmSciTech, 22, 158 (2021)
  128. X.Zhang, X.Zhao, S.Tie, H.Wang, M.Tan, J. Agric. Food Chem., 69, 2719 (2021)
  129. Y.Sun, Q.Yang, X.Xia, X.Li, W.Ruan, M.Zheng, Y.Zou, B.Shi. Front. Bioeng. Biotechnol., 9. 755727 (2021)
  130. P.Laskar, C.Dufès. Nanoscale Adv., 3, 6007 (2021)
  131. S.Biswas, N.S.Dodwadkar, A.Piroyan, V.P.Torchilin. Biomaterials, 33, 4773 (2012)
  132. E.R.Bielski, Q.Zhong, M.Brown, S.R.P.daRocha. Mol. Pharm., 12, 3043 (2015)
  133. A.Sharma, K.Liaw, R.Sharma, Z.Zhang, S.Kannan, R.M.Kannan. Theranostics, 8, 5529 (2018)
  134. A.H.Hunter. Adv. Drug Deliv. Rev., 58, 1523 (2006)
  135. K.Osada, H.Oshima, D.Kobayashi, M.Doi, M.Enoki, Y.Yamasaki, K.Kataoka. J. Am. Chem. Soc., 132, 12343 (2010)
  136. T.A.Theodossiou, Z.Sideratou, D.Tsiourvas, C.M.Paleos. Mitochondrion, 11, 982 (2011)
  137. X.-H.Wang, H.-S.Peng, L.Yang, F.-T.You, F.Teng, A.-W.Tang, F.-J.Zhang, X.-H.Li. J. Mater. Chem. B, 1, 5143 (2013)
  138. T.A.Theodossiou, Z.Sideratou, M.E.Katsarou, D.Tsiourvas. Pharm. Res., 30, 2832 (2013)
  139. K.Panagiotaki, Z.Sideratou, S.Vlahopoulos, M.Paravatou-Petsotas, M.Zachariadis, N.Khoury, V.Zoumpourlis, D.Tsiourvas. Pharmaceuticals, 10, 91 (2017)
  140. V.Stagni, A.Kaminari, Z.Sideratou, E.Sakellis, S.A.Vlahopoulos, D.Tsiourvas. Int. J. Pharm., 585, 119465 (2020)
  141. K.Stakyte, M.Rotheneder, K.Lammens, J.D.Bartho, U.Grädler, T.Fuchß, U.Pehl, A.Alt, E. van de Logt, K.P.Hopfner. Nat. Struct. Mol. Biol., 28, 789 (2021)
  142. V.Stagni, A.Kaminari, C.Contadini, D.Barilà, R.L.Sessa, Z.Sideratou, S.A.Vlahopoulos, D.Tsiourvas. Cancers (Basel), 15, 1474 (2023)
  143. D.Y.Cho, H.Cho, K.Kwon, M.Yu, E.Lee, K.M.Huh, D.H.Lee, H.C. Kang. Adv. Funct. Mater., 25, 5479 (2015)
  144. A.Sharma, G.M.Soliman, N.Al-Hajaj, R.Sharma, D.Maysinger, A.Kakkar. Biomacromolecules, 13, 239 (2012)
  145. Y.Xu, S.Wang, H.F.Chan, Y.Liu, H.Li, C.He, Z.Li, M.Chen. Int. J. Pharm., 522, 21 (2017)
  146. N.Kumar, R.S.Langer, A.J.Domb. Adv. Drug Deliv. Rev., 54, 889 (2002)
  147. D.Katti, S.Lakshmi, R.Langer, C.Laurencin. Adv. Drug Deliv. Rev., 54, 933 (2002)
  148. B.W.Schlichtmann, B.Kalyanaraman, R.L.Schlichtmann, M.G.Panthani, V.Anantharam, A.G.Kanthasamy, S.K.Mallapragada, B.Narasimhan. J. Biomed. Mater. Res., Part B: Appl. Biomater., 110, 450 (2022)
  149. A.Ghosh, M.R.Langley, D.S.Harischandra, M.L.Neal, H.Jin, V.Anantharam, J.Joseph, T.Brenza, B.Narasimhan, A.Kanthasamy, B.Kalyanaraman, A.G.Kanthasamy. J. Neuroimmune Pharmacol., 11, 259 (2016)
  150. T.M. Brenza, S.Ghaisas, J.E.V.Ramirez, D.Harischandra, V.Anantharam, B.Kalyanaraman, A.G.Kanthasamy, B.Narasimhan. Nanomed.: Nanotechnol. Biol. Med., 13, 809 (2017)
  151. Y.Liu, K.Ai, L.Lu. Chem. Rev., 114, 5057 (2014)
  152. X.Zhong, K.Yang, Z.Dong, X.Yi, Y.Wang, C.Ge, Y.Zhao, Z.Liu. Adv. Funct. Mater., 25, 7327 (2015)
  153. W.-Q.Li, Z.Wang, S.Hao, H.He, Y.Wan, C.Zhu, L.-P.Sun, G.Cheng, S.-Y.Zheng. ACS Appl. Mater. Interfaces, 9, 16793 (2017)
  154. F.Liu, X.He, J.Zhang, H.Chen, H.Zhang, Z.Wang. J. Mater. Chem. B, 3, 6731 (2015)
  155. Z.Meng, B.Wang, Y.Liu, Y.Wan, Q.Liu, H.Xu, R.Liang, Y.Shi, P.Tu, H.Wu, C.Xu. Regen. Biomater., 9, rbac051 (2022)
  156. Y.Lu, D.Cheng, B.Niu, X.Wang, X.Wu, A.Wang. Pharmaceuticals, 16, 454 (2023)
  157. A.Narmani, R.Jahedi, E.Bakhshian-Dehkordi, S.Ganji, M.Nemati, R.Ghahramani-Asl, K.Moloudi, S.M.Hosseini, H.Bagheri, P.Kesharwani, A.Khani, B.Farhood, A.Sahebkar. Expert Opin. Drug Deliv., 20, 937 (2023)
  158. S.Marrache, S.Dhar. Proc. Natl. Acad. Sci. USA, 109, 16288 (2012)
  159. S.Marrache, S.Tundup, D.A.Harn, S.Dhar. ACS Nano, 7, 7392 (2013)
  160. M.Velichkovska, B.Surnar, M.Nair, S.Dhar, M.Toborek. Mol. Pharm., 16, 724 (2019)
  161. W.Zhou, H.Yu, L.-J.Zhang, B.Wu, C.-X.Wang, Q.Wang, K.Deng, R.-X.Zhuo, S.-W.Huang. Nanoscale, 9, 17044 (2017)
  162. L.Zhang, J.M.Chan, F.X.Gu, J.-W.Rhee, A.Z.Wang, A.F.Radovic-Moreno, F.Alexis, R.Langer, O.C.Farokhzad. ACS Nano, 2, 1696 (2008)
  163. Y.Song, D.Liu, Y.Cheng, Z.Teng, H.Cui, M.Liu, B.Zhang, Q.Mei, S.Zhou. Mol. Pharm., 15, 1296 (2018)
  164. H.Li, W.Ye, M.Huan, Y.Cheng, D.Liu, H.Cui, M.Liu, B.Zhang, Q.Mei, S.Zhou. Nanomedicine (London), 14, 1011 (2019)
  165. Y.Qin, Z.Wang, X.Wang, T.Zhang, Y.Hu, D.Wang, H.Sun, L.Zhang, Y.Zhu. Mater. Today Adv., 17, 100328 (2023)
  166. R.Jha, R. A.Mayanovic. Nanomaterials, 13, 1302 (2023)
  167. H.Huang, H.Wu, Y.Huang, S.Zhang, Y.Lam, N.Ao. J. Mater. Res., 33, 2586 (2018)
  168. K.K.Arafa, M.A.Hamzawy, S.A.Mousa, I.M.El-Sherbiny. RSC Adv., 12, 21690 (2022)
  169. K.K.Arafa, H.D.C.Smyth, I.M.El-Sherbiny. Int. J. Pharm., 606, 120936 (2021)
  170. H.Liu, N.Guo, W.Guo, M.Huang-Fu, M.R.Vakili, J.Chen, W.Xu, Q.Wei, M.Han, A.Lavasanifar, J.Gao. Acta Pharmacol. Sin., 39, 1681 (2018)
  171. H.-N.Liu, N.-N.Guo, T.-T.Wang, W.-W.Guo, M.-T.Lin, M.-Y.Huang-Fu, M.R.Vakili, W.-H.Xu, J.-J.Chen, Q.-C.Wei, M.Han, A.Lavasanifar, J.-Q.Gao. Mol. Pharm., 15, 882 (2018)
  172. S.Y.Lee, H.-J.Cho. Biomacromolecules, 20, 835 (2019)
  173. K.Wang, M.Qi, C.Guo, Y.Yu, B.Wang, L.Fang, M.Liu, Z.Wang, X.Fan, D.Chen. Nanoscale Res. Lett., 13, 32 (2018)
  174. A.V.Kabanov, V.Y.Alakhov. Crit. Rev. Ther. Drug Carrier Syst., 19, 1 (2002)
  175. R.Savić, L.Luo, A.Eisenberg, D.Maysinger. Science, 300, 615 (2003)
  176. Q.Zhang, M.R.Vakili, X.-F.Li, A.Lavasanifar, X.C.Le. Biomaterials, 35, 7088 (2014)
  177. J.-M.Noy, F.Chen, M.Stenzel. Beilstein J. Org. Chem., 17, 2302 (2021)
  178. F.Ceccacci, S.Sennato, E.Rossi, R.Proroga, S.Sarti, M.Diociaiuti, S.Casciardi, V.Mussi, A.Ciogli, F.Bordi, G.Mancini, C.Bombelli. In Mitochondrial Medicine. Vol. 1. (New York: Springer, 2021). P. 27
  179. F.Ceccacci, S.Sennato, E.Rossi, R.Proroga, S.Sarti, M.Diociaiuti, S.Casciardi, V.Mussi, A.Ciogli, F.Bordi, G.Mancini, C.Bombelli. J. Colloid Interface Sci., 531, 451 (2018)
  180. K.Y.Kim, H.Jin, J.Park, S.H.Jung, J.H.Lee, H.Park, S.K.Kim, J.Bae, J.H.Jung. Nano Res., 11, 1082 (2018)
  181. G.Battogtokh, O.Gotov, J. H.Kang, J.Cho, T.H.Jeong, G.Chimed, Y.T.Ko. Nanomedicine, 13, 325 (2018)
  182. Y.Liu, D.Wang, H.Liu, L.Liu, S.Li, Z.Zhou, L.Lu, X.Liu, L.He, D.He, C.-Y.Yu, H.Wei. J. Med. Chem., 66, 4045 (2023)
  183. Y.Zhang, C.Zhang, J.Chen, L.Liu, M.Hu, J.Li, H.Bi. ACS Appl. Mater. Interfaces, 9, 25152 (2017)
  184. Y.Tan, X.Yang, S.Dai, K.Lian, L.Wen, Y.Zhu, T.Meng, X.Liu, H.Yuan, F.Hu. Polym. Chem., 10, 512 (2019)
  185. H.Wang, F.Zhang, H.Wen, W.Shi, Q.Huang, Y.Huang, J.Xie, P.Li, J.Chen, L.Qin, Y.Zhou. J. Nanobiotechnol., 18, 98 (2020)
  186. H.Wang, W.Shi, D.Zeng, Q.Huang, J.Xie, H.Wen, J.Li, X.Yu, L.Qin, Y.Zhou. J. Nanobiotechnol., 19, 152 (2021)
  187. X.Shi, G.Lv, X.Sun, D.Cao, G.Wang, Y.Chang. RSC Adv., 7, 25694 (2017)
  188. W.Li, J.Wu, D.Xiang, S.Luo, X.Hu, T.Tang, T.Sun, X.Liu. Int. J. Nanomed., 14, 8345 (2019)
  189. P.Yang, D.Sheng, Q.Guo, P.Wang, S.Xu, K.Qian, Y.Li, Y.Cheng, L.Wang, W.Lu, Q.Zhang. Biomaterials, 238, 119844 (2020)
  190. K.Damrongrak, K.Kloysawat, S.Bunsupa, K.Sakchasri, A.Wongrakpanich, V.Taresco, V.CuzzucoliCrucitti, M.C.Garnett, J.Suksiriworapong. Int. J. Pharm., 618, 121636 (2022)
  191. B.-Y.Liu, W.-X.Wu, Y.-H.Liu, C.Jia, X.-L.Yang, J.Li, N.Wang, X.-Q.Yu. Polym. Chem., 8, 5982 (2017)
  192. B.-Y.Liu, X.-L.Yang, X.Xing, J.Li, Y.-H.Liu, N.Wang, X.-Q.Yu. ACS Macro Lett., 8, 719 (2019)
  193. S.Marrache, R.K.Pathak, S.Dhar. Proc. Natl. Acad. Sci. USA, 111, 10444 (2014)
  194. R.Palao-Suay, M.R.Aguilar, F.J.Parra-Ruiz, S.Martín-Saldaña, N.A.Rohner, S.N.Thomas, J. San Román. J. Mater. Sci. Mater. Med., 28, 152 (2017)
  195. H.Yabu. Bull. Chem. Soc. Jpn., 85, 265 (2012)
  196. A.Mallick, P.More, M.M.K.Syed, S.Basu. ACS Appl. Mater. Interfaces, 8, 13218 (2016)
  197. K.Zhang, J.Fu, X.Liu, Y.Guo, M.Han, M.Liu, X.Wang. Pharmaceutics, 15, 388 (2023)
  198. Z.Xu, X.Chen, Z.Sun, C.Li, B.Jiang. Mater. Today Chem., 12, 240 (2019)
  199. X.Li, Q.He, J.Shi. ACS Nano, 8, 1309 (2014)
  200. J.Zhang, Z.-F.Yuan, Y.Wang, W.-H.Chen, G.-F.Luo, S.-X.Cheng, R.-X.Zhuo, X.-Z.Zhang. J. Am. Chem. Soc., 135, 5068 (2013)
  201. B.Yang, Y.Chen, J.Shi. Mater. Sci. Eng. R Rep., 137, 66 (2019)
  202. P.Yuan, X.Mao, X.Wu, S.S.Liew, L.Li, S.Q.Yao. Angew. Chem., Int. Ed., 58, 7657 (2019)
  203. Q.Qu, X.Ma, Y.Zhao. Nanoscale, 7, 16677 (2015)
  204. A.R.Ibragimova, D.R.Gabdrakhmanov, F.G.Valeeva, L.A.Vasileva, A.S.Sapunova, A.D.Voloshina, A.F.Saifina, A.T.Gubaidullin, M.P.Danilaev, S.R.Egorova, A.A.Tyryshkina, A.A.Lamberov, A.R.Khamatgalimov, G.V.Sibgatullina, D.V.Samigullin, K.A.Petrov, L.Y.Zakharova, O.G.Sinyashin. Int. J. Pharm., 604, 120776 (2021)
  205. Q.Cai, W.-Y.Lin, F.-S.Xiao, W.-Q.Pang, X.-H.Chen, B.-S.Zou. Microporous Mesoporous Mater., 32, 1 (1999)
  206. J.Du, N.Xu, J.Fan, W.Sun, X.Peng. Small, 15, 1805087 (2019)
  207. Y.Zhang, Y.Shen, X.Teng, M.Yan, H.Bi, P.C.Morais. ACS Appl. Mater. Interfaces, 7, 10201 (2015)
  208. X.Liang, X.Wang, J.Zhuang, Y.Chen, D.Wang, Y.Li. Adv. Funct. Mater., 16, 1805 (2006)
  209. Y.Ju.-Nam, N.Bricklebank, D.W.Allen, P.H.E.Gardiner, M.E.Light, M.B.Hursthouse. Org. Biomol. Chem., 4, 4345 (2006)
  210. Y.Ju.-Nam, D.W.Allen, P.H.E.Gardiner, N.Bricklebank. J. Organomet. Chem., 693, 3504 (2008)
  211. Y.Ju.-Nam, Y.S.Chen, J.J.Ojeda, D.W.Allen, N.A.Cross, P.H.Gardiner, N.Bricklebank. RSC Adv., 2, 10345 (2012)
  212. S.Marrache, S.Dhar. Chem. Sci., 6, 1832 (2015)
  213. S.Chakrabortty, M.Sison, Y.Wu, A.Ladenburger, G.Pramanik, J.Biskupek, J.Extermann, U.Kaiser, T.Lasser, T.Weil. Biomater. Sci., 5, 966 (2017)
  214. N.M.Vinita, U.Devan, S.Durgadevi, S.Anitha, D.Prabhu, S.Rajamanikandan, M.Govarthanan, A.Yuvaraj, M.Biruntha, A.A.J.Velanganni, J.Jeyakanthan, P.A.Prakash, M.S.M.Jaabir, P.Kumar. Sci. Rep., 13, 2230 (2023)
  215. S.Qin, C.Liu, Y.Chen, M.Yao, S.Liao, W.Xin, S.Gong, X.Guan, Y.Li, J.Xiong, J.Chen, Y.Shen, Y.Liu, J.Zhao, Y.Huang. Kidney Int., 103, 903 (2023)
  216. X.-Y.Zhang, P.-Y.Zhang. Oncol. Lett., 12, 4887 (2016)
  217. X.Wu, S.Sun, Y.Wang, J.Zhu, K.Jiang, Y.Leng, Q.Shu, H. Lin. Biosens. Bioelectron., 90, 501 (2017)
  218. K.Jiang, S.Sun, L.Zhang, Y.Lu, A.Wu, C.Cai, H.Lin. Angew. Chem., Int. Ed., 54, 5360 (2015)
  219. A.Kaminari, E.Nikoli, A.Athanasopoulos, E.Sakellis, Z.Sideratou, D.Tsiourvas. Pharmaceuticals, 14, 932 (2021)
  220. Y.Zou, M.Nishikawa, H.G.Kang, G.Cheng, W.Wang, Y.Wang, N.Komatsu. Mol. Pharm., 18, 2823 (2021)
  221. C.Ren, D.Li, Q.Zhou, X.Hu. Biomaterials, 232, 119752 (2020)
  222. A.Chakraborty, N.R.Jana. J. Phys. Chem. C, 119, 2888 (2015)
  223. Y.Ye, K.Ren, Y.Dong, L.Yang, D.Zhang, Z.Yuan, N.Ma, Y.Song, X.Huang, H.Qiao. ACS Appl. Mater. Interfaces, 15, 26285 (2023)
  224. Z.Hua, X.Zhang, Y.Chen, R.Liu, Y.Li, J.Li, D.Liu, M.Tan. Food Chem., 424, 136439 (2023)
  225. Y.Wu, G.Pramanik, K.Eisele, T.Weil. Biomacromolecules, 13, 1890 (2012)
  226. K.Katagiri, K.Ariga, J.Kikuchi. Chem. Lett., 28, 661 (1999)
  227. Y.Wang, B.Wang, H.Liao, X.Song, H.Wu, H.Wang, H.Shen, X.Ma, M.Tan. J. Mater. Chem. B, 3, 7291 (2015)
  228. D.-H.Kim, E.A.Rozhkova, I.V.Ulasov, S.D.Bader, T.Rajh, M.S.Lesniak, V.Novosad. Nat. Mater., 9, 165 (2010)
  229. Y.Cheng, M.E.Muroski, D.C.M.C.Petit, R.Mansell, T.Vemulkar, R.A.Morshed, Y.Han, I.V.Balyasnikova, C.M.Horbinski, X.Huang, L.Zhang, R.P.Cowburn, M.S.Lesniak. J. Control. Release, 223, 75 (2016)
  230. E.Zhang, M.F.Kircher, M.Koch, L.Eliasson, S.N.Goldberg, E.Renström. ACS Nano, 8, 3192 (2014)
  231. M.Chen, J.Wu, P.Ning, J.Wang, Z.Ma, L.Huang, G.R.Plaza, Y.Shen, C.Xu, Y.Han, M.S.Lesniak, Z.Liu, Y.Cheng. Small, 16, 1905424 (2020)
  232. X.Hu, J.Hu, J.Tian, Z.Ge, G.Zhang, K.Luo, S.Liu. J. Am. Chem. Soc., 135, 17617 (2013)
  233. W.Zhang, X.Hu, Q.Shen, D.Xing. Nat. Commun., 10, 1704 (2019)
  234. W.Zhuang, L.He, K.Wang, B.Ma, L.Ge, Z.Wang, H.Ying. ACS Omega, 3, 2396 (2018)
  235. C.Yang, H.Zhang, Z.Wang, X.Wu, Y.Jin. J. Porphyrins Phthalocyanines, 23, 1028 (2019)
  236. S.Wang, F.Guo, Y.Ji, M.Yu, J.Wang, N.Li. Mol. Pharm., 15, 3318 (2018)
  237. M.Sun, D.Yang, C.Wang, H.Bi, Y.Zhou, X.Wang, J.Xu, F.He, S.Gai, P.Yang. Biomater. Sci., 7, 4769 (2019)
  238. Y.Huang, W.Mo, X.Ding, Y.Ding. Med. Oncol., 40, 177 (2023)
  239. Y.Pan, S.Zhou, C.Liu, X.Ma, J.Xing, B.Parshad, W.Li, A.Wu, R.Haag. Adv. Healthc. Mater., 11 (8), e2102272 (2022)
  240. X.Li, H.Xiao, W.Xiu, K.Yang, Y.Zhang, L.Yuwen, D.Yang, L.Weng, L.Wang. ACS Appl. Mater. Interfaces, 13, 55928 (2021)
  241. J.Lv, S.Wang, D.Qiao, Y.Lin, S.Hu, M.Li. J. Nanobiotechnol., 20, 42 (2022); https://jnanobiotechnology.biomedcentral.com/articles/10.1186/s12951-022-01244-9
  242. C.Liu, L.Chen, Y.Ma, K.Hu, P.Wu, L.Pan, H.Chen, L.Li, H.Hu, J.Zhang. Theranostics, 11, 8550 (2021)
  243. X.Gu, T.Shu, W.Deng, C.Shen, Y.Wu. J. Mater. Chem. B, 11, 4539 (2023)

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies