Delivering drugs to tubular cells and organelles: the application of nanodrugs in acute kidney injury

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Abebe A, Kumela K, Belay M, Kebede B, Wobie Y. Mortality and predictors of acute kidney injury in adults: a hospital-based prospective observational study. Sci. Rep. 11(1), 15672 (2021).
  Medline CASGoogle Scholar
• 2. Kellum JA, Romagnani P, Ashuntantang G, Ronco C, Zarbock A, Anders HJ. Acute kidney injury. Nat. Rev. Dis. Primers 7(1), 52 (2021).
  MedlineGoogle Scholar
• 3. Ronco C, Bellomo R, Kellum JA. Acute kidney injury. Lancet 394(10212), 1949–1964 (2019).
  Medline CASGoogle Scholar
• 4. Hukriede NA, Soranno DE, Sander V et al. Experimental models of acute kidney injury for translational research. Nat. Rev. Nephrol. 18(5), 277–293 (2022).
  MedlineGoogle Scholar
• 5. Kuwabara S, Goggins E, Okusa MD. The pathophysiology of sepsis-associated AKI. Clin. J. Am. Soc. Nephrol. 17(7), 1050–1069 (2022).
  Medline CASGoogle Scholar
• 6. Park SJ, Li C, Chen YM. Endoplasmic reticulum calcium homeostasis in kidney disease: pathogenesis and therapeutic targets. Am. J. Pathol. 191(2), 256–265 (2021).
  Medline CASGoogle Scholar
• 7. Lankadeva YR, May CN, Bellomo R, Evans RG. Role of perioperative hypotension in postoperative acute kidney injury: a narrative review. Br. J. Anaesth. 128(6), 931–948 (2022).
  MedlineGoogle Scholar
• 8. Perazella MA, Rosner MH. Drug-induced acute kidney injury. Clin. J. Am. Soc. Nephrol. 17(8), 1220–1233 (2022).
  Medline CASGoogle Scholar
• 9. Liu BC, Tang TT, Lv LL, Lan HY. Renal tubule injury: a driving force toward chronic kidney disease. Kidney Int. 93(3), 568–579 (2018).
  Medline CASGoogle Scholar
• 10. Li Z, Liu Z, Luo M et al. The pathological role of damaged organelles in renal tubular epithelial cells in the progression of acute kidney injury. Cell Death Discov. 8(1), 239 (2022).
  Medline CASGoogle Scholar
• 11. Jourde-Chiche N, Fakhouri F, Dou L et al. Endothelium structure and function in kidney health and disease. Nat. Rev. Nephrol. 15(2), 87–108 (2019).
  MedlineGoogle Scholar
• 12. Molema G, Zijlstra JG, van Meurs M, Kamps J. Renal microvascular endothelial cell responses in sepsis-induced acute kidney injury. Nat. Rev. Nephrol. 18(2), 95–112 (2022).
  Medline CASGoogle Scholar
• 13. Zhang K, Li R, Chen X et al. Renal endothelial cell-targeted extracellular vesicles protect the kidney from ischemic injury. Adv. Sci. (Weinh.) 10(3), e2204626 (2023).
  Medline CASGoogle Scholar
• 14. Wang S, Wang Y, Lai X et al. Minimalist nanocomplex with dual regulation of endothelial function and inflammation for targeted therapy of inflammatory vascular diseases. ACS Nano 17(3), 2761–2781 (2023).
  Medline CASGoogle Scholar
• 15. Oroojalian F, Charbgoo F, Hashemi M et al. Recent advances in nanotechnology-based drug delivery systems for the kidney. J. Control. Rel. 321, 442–462 (2020).
  Medline CASGoogle Scholar
• 16. Geo HN, Murugan DD, Chik Z et al. Renal nano-drug delivery for acute kidney Injury: current status and future perspectives. J. Control. Rel. 343, 237–254 (2022).
  Medline CASGoogle Scholar
• 17. Kamaly N, He JC, Ausiello DA, Farokhzad OC. Nanomedicines for renal disease: current status and future applications. Nat. Rev. Nephrol. 12(12), 738–753 (2016).
  Medline CASGoogle Scholar
• 18. Kamada H, Tsutsumi Y, Sato-Kamada K et al. Synthesis of a poly(vinylpyrrolidone-co-dimethyl maleic anhydride) co-polymer and its application for renal drug targeting. Nat. Biotechnol. 21(4), 399–404 (2003).
  Medline CASGoogle Scholar
• 19. Wei H, Jiang D, Yu B et al. Nanostructured polyvinylpyrrolidone–curcumin conjugates allowed for kidney-targeted treatment of cisplatin induced acute kidney injury. Bioact. Mater. 19, 282–291 (2023).
  Medline CASGoogle Scholar
• 20. Zhu Z, Liu X, Li P et al. Renal clearable quantum dot–drug conjugates modulate labile iron species and scavenge free radicals for attenuating chemotherapeutic drug-induced acute kidney injury. ACS Appl. Mater. Interfaces 15(18), 21854–21865 (2023).
  Medline CASGoogle Scholar
• 21. Duan R, Li Y, Zhang R et al. Reversing acute kidney injury through coordinated interplay of anti-inflammation and iron supplementation. Adv. Mater. 35(28), e2301283 (2023). •• Fe3O4 is an excellent nanocarrier, but its use during acute kidney injury (AKI) may exacerbate iron death in renal tubular epithelial cells. This study discovered for the first time that nicotinamide mononucleotide can inhibit inflammation, eliminate the local microenvironment that can induce iron death, and utilize Fe3O4 to improve anemia and promote AKI recovery.
  Medline CASGoogle Scholar
• 22. Li Y, Wang G, Wang T et al. PEGylated gambogic acid nanoparticles enable efficient renal-targeted treatment of acute kidney injury. Nano Lett. 23(12), 5641–5656 (2023).
  Medline CASGoogle Scholar
• 23. Alidori S, Akhavein N, Thorek DL et al. Targeted fibrillar nanocarbon RNAi treatment of acute kidney injury. Sci. Transl. Med. 8(331), 331ra339 (2016).
  Google Scholar
• 24. Yan R, Cui W, Ma W, Li J, Liu Z, Lin Y. Typhaneoside–tetrahedral framework nucleic acids system: mitochondrial recovery and antioxidation for acute kidney injury treatment. ACS Nano 17(9), 8767–8781 (2023).
  Medline CASGoogle Scholar
• 25. Choi HS, Mathew AP, Uthaman S et al. Inflammation-sensing catalase-mimicking nanozymes alleviate acute kidney injury via reversing local oxidative stress. J. Nanobiotechnol. 20(1), 205 (2022).
  Medline CASGoogle Scholar
• 26. Wang S, Chen Y, Han S et al. Selenium nanoparticles alleviate ischemia reperfusion injury-induced acute kidney injury by modulating GPx-1/NLRP3/Caspase-1 pathway. Theranostics 12(8), 3882–3895 (2022).
  Medline CASGoogle Scholar
• 27. Jiang D, Ge Z, Im HJ et al. DNA origami nanostructures can exhibit preferential renal uptake and alleviate acute kidney injury. Nat. Biomed. Eng. 2(11), 865–877 (2018).
  Medline CASGoogle Scholar
• 28. Williams RM, Shah J, Mercer E et al. Kidney-targeted redox scavenger therapy prevents cisplatin-induced acute kidney injury. Front. Pharmacol. 12, 790913 (2021).
  Medline CASGoogle Scholar
• 29. Han SJ, Williams RM, D’Agati V, Jaimes EA, Heller DA, Lee HT. Selective nanoparticle-mediated targeting of renal tubular Toll-like receptor 9 attenuates ischemic acute kidney injury. Kidney Int. 98(1), 76–87 (2020).
  Medline CASGoogle Scholar
• 30. Vallorz EL, Janda J, Mansour HM, Schnellmann RG. Kidney targeting of formoterol containing polymeric nanoparticles improves recovery from ischemia reperfusion-induced acute kidney injury in mice. Kidney Int. 102(5), 1073–1089 (2022).
  Medline CASGoogle Scholar
• 31. Deng X, Zeng T, Li J et al. Kidney-targeted triptolide-encapsulated mesoscale nanoparticles for high-efficiency treatment of kidney injury. Biomater. Sci. 7(12), 5312–5323 (2019).
  Medline CASGoogle Scholar
• 32. Nurunnabi M, Khatun Z, Huh KM et al. In vivo biodistribution and toxicology of carboxylated graphene quantum dots. ACS Nano 7(8), 6858–6867 (2013).
  Medline CASGoogle Scholar
• 33. Wang H, Yu D, Fang J et al. Phenol-like group functionalized graphene quantum dots structurally mimicking natural antioxidants for highly efficient acute kidney injury treatment. Chem. Sci. 11(47), 12721–12730 (2020).
  Medline CASGoogle Scholar
• 34. Yu H, Lin T, Chen W et al. Size and temporal-dependent efficacy of oltipraz-loaded PLGA nanoparticles for treatment of acute kidney injury and fibrosis. Biomaterials 219, 119368 (2019). • After inducing ischemia–reperfusion injury (IRI) damage on one side of a mouse’s kidney while keeping the other side healthy, different sizes of PLGA-DSPE-PEG nanoparticles were injected. Nanoparticles with a size of 100 nm accumulated in the IRI-side renal tubular epithelial cells but not in the healthy-side renal tubular epithelial cells.
  Medline CASGoogle Scholar
• 35. Leeuwis JW, Nguyen TQ, Dendooven A, Kok RJ, Goldschmeding R. Targeting podocyte-associated diseases. Adv. Drug Deliv. Rev. 62(14), 1325–1336 (2010).
  Medline CASGoogle Scholar
• 36. Williams RM, Shah J, Ng BD et al. Mesoscale nanoparticles selectively target the renal proximal tubule epithelium. Nano Lett. 15(4), 2358–2364 (2015). •• It was serendipitously discovered that PLGA-PEG nanoparticles of medium size accumulated in renal tubular epithelial cells, not via the conventional brush-border absorption but by entry from the basolateral side of the renal tubules. PEG modification was indispensable for this accumulation pathway.
  Medline CASGoogle Scholar
• 37. Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ. Res. 100(2), 174–190 (2007).
  Medline CASGoogle Scholar
• 38. Brenner BM, Troy JL, Daugharty TM. On the mechanism of inhibition in fluid reabsorption by the renal proximal tubule of the volume-expanded rat. J. Clin. Invest. 50(8), 1596–1602 (1971).
  Medline CASGoogle Scholar
• 39. Williams RM, Shah J, Tian HS et al. Selective nanoparticle targeting of the renal tubules. Hypertension 71(1), 87–94 (2018).
  Medline CASGoogle Scholar
• 40. Vallorz EL, Blohm-Mangone K, Schnellmann RG, Mansour HM. Formoterol PLGA-PEG nanoparticles induce mitochondrial biogenesis in renal proximal tubules. AAPS J. 23(4), 88 (2021).
  Medline CASGoogle Scholar
• 41. Otsuka H, Nagasaki Y, Kataoka K. PEGylated nanoparticles for biological and pharmaceutical applications. Adv. Drug Deliv. Rev. 55(3), 403–419 (2003).
  Medline CASGoogle Scholar
• 42. Zhang F, Liu MR, Wan HT. Discussion about several potential drawbacks of PEGylated therapeutic proteins. Biol. Pharm. Bull. 37(3), 335–339 (2014).
  Medline CASGoogle Scholar
• 43. Christensen EI, Birn H, Storm T, Weyer K, Nielsen R. Endocytic receptors in the renal proximal tubule. Physiology 27(4), 223–236 (2012).
  CASGoogle Scholar
• 44. Qin S, Wu B, Gong T, Zhang ZR, Fu Y. Targeted delivery via albumin corona nanocomplex to renal tubules to alleviate acute kidney injury. J. Control. Rel. 349, 401–412 (2022).
  Medline CASGoogle Scholar
• 45. Pang M, Duan S, Zhao M et al. Co-delivery of celastrol and lutein with pH sensitive nano micelles for treating acute kidney injury. Toxicol. Appl. Pharmacol. 450, 116155 (2022).
  Medline CASGoogle Scholar
• 46. Matsuura S, Katsumi H, Suzuki H et al. L-serine-modified polyamidoamine dendrimer as a highly potent renal targeting drug carrier. Proc. Natl Acad. Sci. USA 115(41), 10511–10516 (2018).
  Medline CASGoogle Scholar
• 47. Knight SF, Kundu K, Joseph G et al. Folate receptor-targeted antioxidant therapy ameliorates renal ischemia–reperfusion injury. J. Am. Soc. Nephrol. 23(5), 793–800 (2012).
  Medline CASGoogle Scholar
• 48. Huang C, Zeng T, Li J et al. Folate receptor-mediated renal-targeting nanoplatform for the specific delivery of triptolide to treat renal ischemia/reperfusion injury. ACS Biomater. Sci. Eng. 5(6), 2877–2886 (2019).
  Medline CASGoogle Scholar
• 49. Du B, Zhao M, Wang Y et al. Folic acid-targeted pluronic F127 micelles improve oxidative stress and inhibit fibrosis for increasing AKI efficacy. Eur. J. Pharmacol. 930, 175131 (2022).
  Medline CASGoogle Scholar
• 50. Hu JB, Li SJ, Kang XQ et al. CD44-targeted hyaluronic acid–curcumin prodrug protects renal tubular epithelial cell survival from oxidative stress damage. Carbohydr. Polym. 193, 268–280 (2018).
  Medline CASGoogle Scholar
• 51. Huang ZW, Shi Y, Zhai YY et al. Hyaluronic acid coated bilirubin nanoparticles attenuate ischemia reperfusion-induced acute kidney injury. J. Control. Rel. 334, 275–289 (2021).
  Medline CASGoogle Scholar
• 52. Walkon LL, Strubbe-Rivera JO, Bazil JN. Calcium overload and mitochondrial metabolism. Biomolecules 12(12), 1891 (2022).
  Medline CASGoogle Scholar
• 53. Liu D, Shu G, Jin F et al. ROS-responsive chitosan-SS31 prodrug for AKI therapy via rapid distribution in the kidney and long-term retention in the renal tubule. Sci. Adv. 6(41), eabb7422 (2020). • Inspired by phospholipid serine as the substrate of KIM-1, chitosan modified with L-serine and loaded with SS31 formed nanoparticles for AKI treatment. In this system, L-serine binds to the highly expressed KIM-1 on damaged renal tubular epithelial cells, enabling targeted delivery. The reactive oxygen species environment within the cells triggers the release of SS31, which itself targets the mitochondrial inner membrane and clears mitochondrial reactive oxygen species.
  Medline CASGoogle Scholar
• 54. Li J, Duan Q, Wei X, Wu J, Yang Q. Kidney-targeted nanoparticles loaded with the natural antioxidant rosmarinic acid for acute kidney injury treatment. Small 18(48), e2204388 (2022).
  Medline CASGoogle Scholar
• 55. Tang TT, Wang B, Li ZL et al. KIM-1 targeted extracellular vesicles: a new therapeutic platform for RNAi to treat AKI. J. Am. Soc. Nephrol. 32(10), 2467–2483 (2021).
  Medline CASGoogle Scholar
• 56. Yan J, Wang Y, Zhang J, Liu X, Yu L, He Z. Rapidly blocking the calcium overload/ROS production feedback loop to alleviate acute kidney injury via microenvironment-responsive BAPTA-AM/BAC co-delivery nanosystem. Small 19(17), e2206936 (2023).
  Medline CASGoogle Scholar
• 57. Huang Z, Chun C, Li X. Kidney targeting peptide-modified biomimetic nanoplatforms for treatment of acute kidney injury. J. Control. Rel. 358, 368–381 (2023). •• The principle of ‘homologous targeting’ was first extended to areas beyond tumor-targeted delivery. Renal tubular epithelial cell membrane-coated nanoparticles exhibited better targeting effects than uncoated nanoparticles. Their targeting ability was further enhanced by modification with the renal-targeting peptide KCSAVPLC.
  Medline CASGoogle Scholar
• 58. Liu Z, Liu X, Yang Q, Yu L, Chang Y, Qu M. Neutrophil membrane-enveloped nanoparticles for the amelioration of renal ischemia–reperfusion injury in mice. Acta Biomater. 104, 158–166 (2020).
  Medline CASGoogle Scholar
• 59. Tang TT, Wang B, Wu M et al. Extracellular vesicle-encapsulated IL-10 as novel nanotherapeutics against ischemic AKI. Sci. Adv. 6(33), eaaz0748 (2020).
  Medline CASGoogle Scholar
• 60. Gatti S, Bruno S, Deregibus MC et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia–reperfusion-induced acute and chronic kidney injury. Nephrol. Dial. Transplant. 26(5), 1474–1483 (2011).
  Medline CASGoogle Scholar
• 61. Zhao M, Liu S, Wang C et al. Mesenchymal stem cell-derived extracellular vesicles attenuate mitochondrial damage and inflammation by stabilizing mitochondrial DNA. ACS Nano 15(1), 1519–1538 (2021).
  Medline CASGoogle Scholar
• 62. Cao H, Cheng Y, Gao H et al. In vivo tracking of mesenchymal stem cell-derived extracellular vesicles improving mitochondrial function in renal ischemia–reperfusion injury. ACS Nano 14(4), 4014–4026 (2020).
  Medline CASGoogle Scholar
• 63. Yuan ZX, Zhang ZR, Zhu D et al. Specific renal uptake of randomly 50% N-acetylated low molecular weight chitosan. Mol. Pharm. 6(1), 305–314 (2009).
  Medline CASGoogle Scholar
• 64. Wang DW, Li SJ, Tan XY et al. Engineering of stepwise-targeting chitosan oligosaccharide conjugate for the treatment of acute kidney injury. Carbohydr. Polym. 256, 117556 (.2021).
  Medline CASGoogle Scholar
• 65. Kaunitz JD, Cummins VP, Mishler D, Nagami GT. Inhibition of gentamicin uptake into cultured mouse proximal tubule epithelial cells by L-lysine. J. Clin. Pharmacol. 33(1), 63–69 (1993).
  Medline CASGoogle Scholar
• 66. Wischnjow A, Sarko D, Janzer M et al. Renal targeting: peptide-based drug delivery to proximal tubule cells. Bioconjug. Chem. 27(4), 1050–1057 (2016).
  Medline CASGoogle Scholar
• 67. Wang J, Poon C, Chin D et al. Design and in vivo characterization of kidney-targeting multimodal micelles for renal drug delivery. Nano Res. 11(10), 5584–5595 (2018).
  CASGoogle Scholar
• 68. Schreiber A, Theilig F, Schweda F, Hocherl K. Acute endotoxemia in mice induces downregulation of megalin and cubilin in the kidney. Kidney Int. 82(1), 53–59 (2012).
  Medline CASGoogle Scholar
• 69. Wu X, Tang S, Dai Q et al. Vitamin D–vitamin D receptor alleviates oxidative stress in ischemic acute kidney injury via upregulating glutathione peroxidase 3. FASEB J. 37(2), e22738 (2023).
  Medline CASGoogle Scholar
• 70. Wang S, Huang S, Liu X, He Y, Liu Y. Paricalcitol ameliorates acute kidney injury in mice by suppressing oxidative stress and inflammation via Nrf2/HO-1 signaling. Int. J. Mol. Sci. 24(2), 969 (2023).
  Medline CASGoogle Scholar
• 71. Du J, Jiang S, Hu Z et al. Vitamin D receptor activation protects against lipopolysaccharide-induced acute kidney injury through suppression of tubular cell apoptosis. Am. J. Physiol. Renal Physiol. 316(5), F1068–F1077 (2019).
  Medline CASGoogle Scholar
• 72. Siegelman MH, Degrendele HC, Estess P. Activation and interaction of CD44 and hyaluronan in immunological systems. J. Leukoc. Biol. 66(2), 315–321 (1999).
  Medline CASGoogle Scholar
• 73. Lewington AJ, Padanilam BJ, Martin DR, Hammerman MR. Expression of CD44 in kidney after acute ischemic injury in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278(1), R247–254 (2000).
  Medline CASGoogle Scholar
• 74. Fu Z, Fan Q, Zhou Y, Zhao Y, He Z. Elimination of intracellular calcium overload by BAPTA-AM-loaded liposomes: a promising therapeutic agent for acute liver failure. ACS Appl. Mater. Interfaces 11(43), 39574–39585 (2019).
  Medline CASGoogle Scholar
• 75. Wang Y, Pu M, Yan J et al. 1,2-Bis(2-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid acetoxymethyl ester loaded reactive oxygen species responsive hyaluronic acid–bilirubin nanoparticles for acute kidney injury therapy via alleviating calcium overload mediated endoplasmic reticulum stress. ACS Nano 17(1), 472–491 (2023).
  Medline CASGoogle Scholar
• 76. Cichy J, Pure E. The liberation of CD44. J. Cell Biol. 161(5), 839–843 (2003).
  Medline CASGoogle Scholar
• 77. Ichimura T, Bonventre JV, Bailly V et al. Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is up-regulated in renal cells after injury. J. Biol. Chem. 273(7), 4135–4142 (1998).
  Medline CASGoogle Scholar
• 78. Arai S, Kitada K, Yamazaki T et al. Apoptosis inhibitor of macrophage protein enhances intraluminal debris clearance and ameliorates acute kidney injury in mice. Nat. Med. 22(2), 183–193 (2016).
  Medline CASGoogle Scholar
• 79. Han WK, Bailly V, Abichandani R, Thadhani R, Bonventre JV. Kidney injury molecule-1 (KIM-1): a novel biomarker for human renal proximal tubule injury. Kidney Int. 62(1), 237–244 (2002).
  Medline CASGoogle Scholar
• 80. Ichimura T, Asseldonk EJPV, Humphreys BD, Gunaratnam L, Duffield JS, Bonventre JV. Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J. Clin. Invest. 118(5), 1657–1668 (2008).
  Medline CASGoogle Scholar
• 81. Freeman GJ, Casasnovas JM, Umetsu DT, Dekruyff RH. TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol. Rev. 235, 172–189 (2010).
  Medline CASGoogle Scholar
• 82. Kong L, Fan D, Zhou L, Wei S. The influence of modified molecular (D/L-serine) chirality on the theragnostics of PAMAM-based nanomedicine for acute kidney injury. J. Mater. Chem. B 9(43), 9023–9030 (2021).
  Medline CASGoogle Scholar
• 83. Luk BT, Zhang L. Cell membrane-camouflaged nanoparticles for drug delivery. J. Control. Rel. 220(Pt B), 600–607 (2015).
  Medline CASGoogle Scholar
• 84. Chen L, Hong W, Ren W, Xu T, Qian Z, He Z. Recent progress in targeted delivery vectors based on biomimetic nanoparticles. Signal Transduct. Target. Ther. 6(1), 225 (2021).
  MedlineGoogle Scholar
• 85. Jin K, Luo Z, Zhang B, Pang Z. Biomimetic nanoparticles for inflammation targeting. Acta Pharm. Sin. B 8(1), 23–33 (2018).
  MedlineGoogle Scholar
• 86. Deng J, Kohda Y, Chiao H et al. Interleukin-10 inhibits ischemic and cisplatin-induced acute renal injury. Kidney Int. 60(6), 2118–2128 (2001).
  Medline CASGoogle Scholar
• 87. Ouyang W, O’Garra A. IL-10 family cytokines IL-10 and IL-22: from basic science to clinical translation. Immunity 50(4), 871–891 (2019).
  Medline CASGoogle Scholar
• 88. Karp JM, Teol GSL. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4(3), 206–216 (2009).
  Medline CASGoogle Scholar
• 89. Bruno S, Grange C, Deregibus MC et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J. Am. Soc. Nephrol. 20(5), 1053–1067 (2009).
  Medline CASGoogle Scholar
• 90. Cheng YQ, Yue YX, Cao HM et al. Coassembly of hypoxia-sensitive macrocyclic amphiphiles and extracellular vesicles for targeted kidney injury imaging and therapy. J. Nanobiotechnol. 19(1), 451 (2021).
  Medline CASGoogle Scholar
• 91. Li Y, Wang J, Wientjes MG, Au JL. Delivery of nanomedicines to extracellular and intracellular compartments of a solid tumor. Adv. Drug Deliv. Rev. 64(1), 29–39 (2012).
  Medline CASGoogle Scholar
• 92. Tang C, Cai J, Yin XM, Weinberg JM, Venkatachalam MA, Dong Z. Mitochondrial quality control in kidney injury and repair. Nat. Rev. Nephrol. 17(5), 299–318 (2021).
  Medline CASGoogle Scholar
• 93. Liu Z, Li Y, Li C, Yu L, Chang Y, Qu M. Delivery of coenzyme Q10 with mitochondria-targeted nanocarrier attenuates renal ischemia–reperfusion injury in mice. Mater. Sci. Eng. C Mater. Biol. Appl. 131, 112536 (2021).
  Medline CASGoogle Scholar
• 94. Yu H, Jin F, Liu D et al. ROS-responsive nano-drug delivery system combining mitochondria-targeting ceria nanoparticles with atorvastatin for acute kidney injury. Theranostics 10(5), 2342–2357 (2020).
  Medline CASGoogle Scholar
• 95. Qin S, Liu C, Chen Y et al. Cobaltosic oxide–polyethylene glycol–triphenylphosphine nanoparticles ameliorate the acute-to-chronic kidney disease transition by inducing BNIP3-mediated mitophagy. Kidney Int. 103(5), 903–916 (2023).
  Medline CASGoogle Scholar
• 96. Liu D, Jin F, Shu G et al. Enhanced efficiency of mitochondria-targeted peptide SS-31 for acute kidney injury by pH-responsive and AKI-kidney targeted nanopolyplexes. Biomaterials 211, 57–67 (2019).
  Medline CASGoogle Scholar
• 97. Huang Q, Yang Y, Zhao T et al. Passively-targeted mitochondrial tungsten-based nanodots for efficient acute kidney injury treatment. Bioact. Mater. 21, 381–393 (2023).
  Medline CASGoogle Scholar
• 98. Smith RA, Porteous CM, Coulter CV, Murphy MP. Selective targeting of an antioxidant to mitochondria. Eur. J. Biochem. 263(3), 709–716 (1999).
  Medline CASGoogle Scholar
• 99. Murphy MP, Smith RA. Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Ann. Rev. Pharmacol. Toxicol. 47, 629–656 (2007).
  Medline CASGoogle Scholar
• 100. Reily C, Mitchell T, Chacko BK, Benavides GA, Murphy MP, Darley-Usmar VM. Mitochondrially targeted compounds and their impact on cellular bioenergetics. Redox Biol. 1(1), 86–93 (2013).
  Medline CASGoogle Scholar
• 101. Battogtokh G, Choi YS, Kang DS et al. Mitochondria-targeting drug conjugates for cytotoxic, anti-oxidizing and sensing purposes: current strategies and future perspectives. Acta Pharm. Sin. B 8(6), 862–880 (2018).
  MedlineGoogle Scholar
• 102. Zhao K, Zhao GM, Wu D et al. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J. Biol. Chem. 279(33), 34682–34690 (2004).
  Medline CASGoogle Scholar
• 103. Birk AV, Liu S, Soong Y et al. The mitochondrial-targeted compound SS-31 re-energizes ischemic mitochondria by interacting with cardiolipin. J. Am. Soc. Nephrol. 24(8), 1250–1261 (2013).
  Medline CASGoogle Scholar
• 104. Szeto HH. First-in-class cardiolipin-protective compound as a therapeutic agent to restore mitochondrial bioenergetics. Br. J. Pharmacol. 171(8), 2029–2050 (2014).
  Medline CASGoogle Scholar
• 105. Kumar S. Cellular and molecular pathways of renal repair after acute kidney injury. Kidney Int. 93(1), 27–40 (2018).
  Medline CASGoogle Scholar
• 106. Ruggiero A, Villa CH, Bander E et al. Paradoxical glomerular filtration of carbon nanotubes. Proc. Natl Acad. Sci. USA 107(27), 12369–12374 (2010).
  Medline CASGoogle Scholar
• 107. Ma X, Gong N, Zhong L, Sun J, Liang XJ. Future of nanotherapeutics: targeting the cellular sub-organelles. Biomaterials 97, 10–21 (2016).
  Medline CASGoogle Scholar
• 108. Ledford H. ‘Astonishing’ molecular syringe ferries proteins into human cells. Nature 616(7955), 18–19 (2023).
  Medline CASGoogle Scholar
• 109. Kreitz J, Friedrich MJ, Guru A et al. Programmable protein delivery with a bacterial contractile injection system. Nature 616(7956), 357–364 (2023). •• F Zhang’s team developed the Photorhabdus virulence cassette (PVC) bacterial injection system. Editing of the tail fiber of PVC enables it to recognize specific cells, thus achieving targeted delivery. The efficiency of the PVC delivery system is nearly 100%.
  Medline CASGoogle Scholar
• 110. Hulse M, Rosner MH. Drugs in development for acute kidney injury. Drugs 79(8), 811–821 (2019).
  Medline CASGoogle Scholar
• 111. Fouad AA, Al-Mulhim AS, Jresat I. Cannabidiol treatment ameliorates ischemia/reperfusion renal injury in rats. Life Sci. 91(7–8), 284–292 (2012).
  Medline CASGoogle Scholar
• 112. Kanlaya R, Thongboonkerd V. Protective effects of epigallocatechin-3-gallate from green tea in various kidney diseases. Adv. Nutr. 10(1), 112–121 (2019).
  MedlineGoogle Scholar
• 113. Li HD, Meng XM, Huang C, Zhang L, Lv XW, Li J. Application of herbal traditional Chinese medicine in the treatment of acute kidney injury. Front. Pharmacol. 10, 376 (2019).
  MedlineGoogle Scholar