We use cookies to improve your experience. By continuing to browse this site, you accept our cookie policy.×
Skip main navigation
Aging Health
Bioelectronics in Medicine
Biomarkers in Medicine
Breast Cancer Management
CNS Oncology
Colorectal Cancer
Concussion
Epigenomics
Future Cardiology
Future Medicine AI
Future Microbiology
Future Neurology
Future Oncology
Future Rare Diseases
Future Virology
Hepatic Oncology
HIV Therapy
Immunotherapy
International Journal of Endocrine Oncology
International Journal of Hematologic Oncology
Journal of 3D Printing in Medicine
Lung Cancer Management
Melanoma Management
Nanomedicine
Neurodegenerative Disease Management
Pain Management
Pediatric Health
Personalized Medicine
Pharmacogenomics
Regenerative Medicine

Recent progress in therapeutic strategies and biomimetic nanomedicines based on neutrophils for inflammation treatment

    Yan Liu‡

    Department of Pharmaceutical Sciences, School of Pharmacy, Southwest Medical University, Luzhou, Sichuan, 646000, China

    ‡These authors contributed equally to this work

    Search for more papers by this author

    ,
    Yang Yu‡

    Department of cardiology, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, 646000, China

    Nucleic Acid Medicine of Luzhou Key Laboratory, Southwest Medical University, Luzhou, Sichuan, 646000, China

    ‡These authors contributed equally to this work

    Search for more papers by this author

    ,
    Minrui Wang‡

    Nucleic Acid Medicine of Luzhou Key Laboratory, Southwest Medical University, Luzhou, Sichuan, 646000, China

    The Key Laboratory of Medical Electrophysiology of the Ministry of Education, Southwest Medical University, Luzhou, Sichuan, 646000, China

    ‡These authors contributed equally to this work

    Search for more papers by this author

    ,
    Chunxiang Zhang

    *Author for correspondence:

    E-mail Address: zhangchx999@163.com

    Nucleic Acid Medicine of Luzhou Key Laboratory, Southwest Medical University, Luzhou, Sichuan, 646000, China

    The Key Laboratory of Medical Electrophysiology of the Ministry of Education, Southwest Medical University, Luzhou, Sichuan, 646000, China

    &
    Chunhong Li

    **Author for correspondence:

    E-mail Address: lispringhong@126.com

    Department of Pharmaceutical Sciences, School of Pharmacy, Southwest Medical University, Luzhou, Sichuan, 646000, China

    Nucleic Acid Medicine of Luzhou Key Laboratory, Southwest Medical University, Luzhou, Sichuan, 646000, China

    Published Online:https://doi.org/10.2217/nnm-2022-0211

    Inflammation is a defensive response that helps repair and restore damaged tissue by activating immune and nonimmune cells against pathogens. However, inflammation may cause chronic disease if it persists for a long time. Neutrophils recruit immediately to the lesion site and regulate the inflammatory process when inflammation occurs. Therefore, neutrophil-mediated therapy has been considered as a promising strategy for inflammatory diseases and has been extensively studied. In this review, we summarize the recent research progress of neutrophil-based personalized treatment strategies for inflammation. We also review the research progress of various neutrophil-mediated drug-delivery systems in combination with the inflammatory microenvironment.

    Plain language summary

    Introduction: Neutrophils are the most abundant white blood cells in humans. When inflammation occurs, neutrophils bind to ligands on endothelial cells through a variety of specific receptors on their surfaces and migrate from the bone marrow to the site of inflammation across endothelial cells, meaning that they are able to recruit to the lesion site at the first opportunity and regulate the inflammatory process. Neutrophil-based therapeutic strategies and drug-delivery systems have been extensively studied in inflammatory diseases, as specific protein receptors are retained on the neutrophil membrane, which is considered a promising approach for inflammatory therapy. Areas covered: This work focuses on the various mechanisms of neutrophil-based therapeutic strategies and reviews the current types and advantages of neutrophil-mediated drug-delivery systems for the treatment of inflammatory disorders. Summary: Neutrophil-mediated drug-delivery systems have a wider range of disease applications, and neutrophil-based therapeutic strategies can be used to treat inflammation through different pathways. Our review of the literature suggests that neutrophil-targeted nanoparticles are one of the most promising strategies for the treatment of inflammation, as they promote drug accumulation at the site of inflammation and limit adverse events, while prolonging drug circulation in the blood and improving drug stability.

    Tweetable abstract

    In this review, we summarize the recent research progress of neutrophil-based treatment strategies for inflammation and review the research progress of various neutrophil-mediated drug-delivery systems developed in recent years.

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

    References

    • 1. He Y, Yue Y, Zheng X et al. Curcumin, inflammation, and chronic diseases: how are they linked? Molecules 20(5), 9183–9213 (2015).
    • 2. Zhang G, Ma L, Bai L et al. Inflammatory microenvironment-targeted nanotherapies. J. Control. Rel. 334, 114–126 (2021).
    • 3. Schraufstätter I, Hyslop PA, Jackson JH, Cochrane CG. Oxidant-induced DNA damage of target cells. J. Clin. Invest. 82(3), 1040–1050 (1988).
    • 4. Couzin-Frankel J. Inflammation bares a dark side. Science. 330(6011), 1621 (2010).
    • 5. Nasef NA, Mehta S, Ferguson LR. Susceptibility to chronic inflammation: an update. Arch. Toxicol. 91(3), 1131–1141 (2017).
    • 6. Straub RH. The brain and immune system prompt energy shortage in chronic inflammation and ageing. Nat. Rev. Rheumatol. 13(12), 743–751 (2017).
    • 7. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 140(6), 883–899 (2010).
    • 8. Haley RM, Von Recum HA. Localized and targeted delivery of NSAIDs for treatment of inflammation: a review. Exp. Biol. Med. 244(6), 433–444 (2019).
    • 9. George MD, Baker JF, Winthrop K et al. Risk for serious infection with low-dose glucocorticoids in patients with rheumatoid arthritis: a cohort study. Ann. Intern. Med. 173(11), 870–878 (2020).
    • 10. Sargazi S, Arshad R, Ghamari R et al. siRNA-based nanotherapeutics as emerging modalities for immune-mediated diseases: a preliminary review. Cell Biol. Int. 46(9), 1320–1344 (2022).
    • 11. Nooreen R, Nene S, Jain H et al. Polymer nanotherapeutics: a versatile platform for effective rheumatoid arthritis therapy. J. Control. Rel. 348, 397–419 (2022).
    • 12. Badri W, Miladi K, Nazari QA et al. Encapsulation of NSAIDs for inflammation management: overview, progress, challenges and prospects. Int. J. Pharm. 515(1-2), 757–773 (2016).
    • 13. Wang Q, Qin X, Fang J, Sun X. Nanomedicines for the treatment of rheumatoid arthritis: state of art and potential therapeutic strategies. Acta Pharm. Sinica. B 11(5), 1158–1174 (2021).
    • 14. Simadibrata M. Gastrointestinal tract disorder as a side effect of non-steroidal anti inflammatory drugs (NSAIDs). Acta Med. Indonesiana 36(4), 195–196 (2004).
    • 15. Li C, Zheng X, Hu M et al. Recent progress in therapeutic strategies and biomimetic nanomedicines for rheumatoid arthritis treatment. Expert Opin. Drug Deliv. 19(8), 883–898 (2022).
    • 16. Emerich DF. Nanomedicine–prospective therapeutic and diagnostic applications. Expert Opin. Biol. Ther. 5(1), 1–5 (2005).
    • 17. Grazú V. Nanocarriers as nanomedicines. Front. of Nanosci. 4, 337–440 (2012).
    • 18. Kreuter J. Nanoparticles – a historical perspective. Int. J. Pharm. 331(1), 1–10 (2007).
    • 19. Jin K, Luo Z, Zhang B, Pang Z. Biomimetic nanoparticles for inflammation targeting. Acta Pharm. Sinica. B 8(1), 23–33 (2018).
    • 20. Ejigah V, Owoseni O, Bataille-Backer P et al. Approaches to improve macromolecule and nanoparticle accumulation in the tumor microenvironment by the enhanced permeability and retention effect. Polymers 14(13), 2601(2022).
    • 21. Wang H, Liu Y, He R et al. Cell membrane biomimetic nanoparticles for inflammation and cancer targeting in drug delivery. Biomater. Sci. 8(2), 552–568 (2020).
    • 22. Wang H, Zang J, Zhao Z et al. The advances of neutrophil-derived effective drug delivery systems: a key review of managing tumors and inflammation. Int. J. Nanomed. 16, 7663–7681 (2021).
    • 23. Nemeth T, Sperandio M, Mocsai A. Neutrophils as emerging therapeutic targets. Nat. Rev. Drug Discov. 19(4), 253–275 (2020).
    • 24. Chu D, Dong X, Shi X et al. Neutrophil-based drug delivery systems. Adv. Mater. 30(22), e1706245 (2018).
    • 25. Rosales C. Neutrophils at the crossroads of innate and adaptive immunity. J. Leukoc. Biol. 108(1), 377–396 (2020).
    • 26. Wang W, Zhang Z, Liu Y et al. Nano-integrated cascade antioxidases opsonized by albumin bypass the blood-brain barrier for treatment of ischemia-reperfusion injury. Biomater. Sci. 10(24), 7103–7116 (2022). •• The ability of neutrophils to cross the blood–brain barrier was used to deliver albumin drug-carrying nanoparticles via neutrophils to the disease site.
    • 27. Carnevale S, Ghasemi S, Rigatelli A, Jaillon S. The complexity of neutrophils in health and disease: focus on cancer. Semin. Immunol. 48, 101409 (2020).
    • 28. Smith JA. Neutrophils, host defense, and inflammation: a double-edged sword. J. Leuk. Biol. 56(6), 672–686 (1994).
    • 29. Laudanna C, Alon R. Right on the spot. Chemokine triggering of integrin-mediated arrest of rolling leukocytes. Thromb. Haemostas. 95(1), 5–11 (2006).
    • 30. Phillipson M, Heit B, Colarusso P et al. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 203(12), 2569–2575 (2006).
    • 31. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7(9), 678–689 (2007).
    • 32. Liew PX, Kubes P. The neutrophil's role during health and disease. Physiol. Rev. 99(2), 1223–1248 (2019).
    • 33. Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol. 5(4), 354–366 (2012).
    • 34. Tecchio C, Micheletti A, Cassatella MA. Neutrophil-derived cytokines: facts beyond expression. Front. Immunol. 5, 508 (2014).
    • 35. Huang SU, O'Sullivan KM. The expanding role of extracellular traps in inflammation and autoimmunity: the new players in casting dark webs. Int. J. Mol. Sci. 23(7), 3793 (2022).
    • 36. Campbell EL, Kao DJ, Colgan SP. Neutrophils and the inflammatory tissue microenvironment in the mucosa. Immunol. Rev. 273(1), 112–120 (2016).
    • 37. Delgado-Rizo V, Martínez-Guzmán MA, Iñiguez-Gutierrez L et al. Neutrophil extracellular traps and its implications in inflammation: an overview. Front. Immunol. 8, 81 (2017).
    • 38. Thiam HR, Wong SL, Wagner DD, Waterman CM. Cellular mechanisms of NETosis. Annu. Rev. Cell Dev. Biol. 36, 191–218 (2020).
    • 39. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191(3), 677–691 (2010).
    • 40. Sollberger G, Tilley DO, Zychlinsky A. Neutrophil extracellular traps: the biology of chromatin externalization. Dev. Cell 44(5), 542–553 (2018).
    • 41. Fidan K, Koçak S, Söylemezoğlu O, Atak Yücel A. A well-intentioned enemy in autoimmune and autoinflammatory diseases: NETosis. Turk Arch. Pediatr. 58(1), 10–19 (2023). • This review details the role of NETosis in autoimmune and autoinflammatory diseases.
    • 42. Castanheira FVS, Kubes P. Neutrophils and NETs in modulating acute and chronic inflammation. Blood 133(20), 2178–2185 (2019).
    • 43. Bissenova S, Ellis D, Mathieu C, Gysemans C. Neutrophils in autoimmunity: when the hero becomes the villain. Clin. Exp. Immunol. 210(2), 128–140 (2022).
    • 44. Zhao Z, Pan Z, Zhang S et al. Neutrophil extracellular traps: a novel target for the treatment of stroke. Pharmacol. Ther. 241, 108328 (2023).
    • 45. Tembhre MK, Sriwastva MK, Hote MP et al. Interleukin-33 induces neutrophil extracellular trap (NET) formation and macrophage necroptosis via enhancing oxidative stress and secretion of proatherogenic factors in advanced atherosclerosis. Antioxidants (Basel) 11(12), 2343 (2022).
    • 46. Cacciotto C, Alberti A. Eating the enemy: mycoplasma strategies to evade neutrophil extracellular traps (NETs) promoting bacterial nucleotides uptake and inflammatory damage. Int. J. Mol. Sci. 23(23), 15030 (2022).
    • 47. Pan W, Xin Q, Xu J et al. IgD enhances the release of neutrophil extracellular traps (NETs) via FcδR in rheumatoid arthritis patients. Int. Immunopharmacol. 114, 109484 (2023).
    • 48. Albrengues J, Shields MA, Ng D et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science 361(6409), eaao4227 (2018).
    • 49. Aikawa N, Kawasaki Y. Clinical utility of the neutrophil elastase inhibitor sivelestat for the treatment of acute respiratory distress syndrome. Ther. Clin. Risk Manage. 10, 621–629 (2014).
    • 50. Zeiher BG, Artigas A, Vincent JL et al. Neutrophil elastase inhibition in acute lung injury: results of the STRIVE study. Crit. Care Med. 32(8), 1695–1702 (2004).
    • 51. Sahebnasagh A, Saghafi F, Safdari M et al. Neutrophil elastase inhibitor (sivelestat) may be a promising therapeutic option for management of acute lung injury/acute respiratory distress syndrome or disseminated intravascular coagulation in COVID-19. J. Clin. Pharm. Ther. 45(6), 1515–1519 (2020).
    • 52. Okeke EB, Louttit C, Fry C et al. Inhibition of neutrophil elastase prevents neutrophil extracellular trap formation and rescues mice from endotoxic shock. Biomaterials 238, 119836 (2020).
    • 53. Dong W, Liu D, Zhang T et al. Oral delivery of staphylococcal nuclease ameliorates DSS induced ulcerative colitis in mice via degrading intestinal neutrophil extracellular traps. Ecotoxicol. Environ. Safety 215, 112161 (2021).
    • 54. Kim JY, Stevens P, Karpurapu M et al. Targeting ETosis by miR-155 inhibition mitigates mixed granulocytic asthmatic lung inflammation. Front. Immunol. 13, 943554 (2022). • The production of ETosis was inhibited by lowering the expression of miR-155, thus alleviating pneumonia.
    • 55. Özcan A, Boyman O. Mechanisms regulating neutrophil responses in immunity, allergy, and autoimmunity. Allergy 77(12), 3567–3583 (2022).
    • 56. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13(3), 159–175 (2013).
    • 57. Van Der Linden M, Meyaard L. Fine-tuning neutrophil activation: strategies and consequences. Immunol. Lett. 178, 3–9 (2016).
    • 58. Bayless RL, Sheats MK, Jones SL. Withaferin A inhibits neutrophil adhesion, migration, and respiratory burst and promotes timely neutrophil apoptosis. Front. Vet. Sci. 9, 900453 (2022).
    • 59. Basu S, Hodgson G, Katz M, Dunn AR. Evaluation of role of G-CSF in the production, survival, and release of neutrophils from bone marrow into circulation. Blood 100(3), 854–861 (2002).
    • 60. Kobayashi SD, Voyich JM, Whitney AR, Deleo FR. Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage-colony stimulating factor. J. Leukocyte Biol. 78(6), 1408–1418 (2005).
    • 61. Ioannou M, Hoving D, Aramburu IV et al. Microbe capture by splenic macrophages triggers sepsis via T cell-death-dependent neutrophil lifespan shortening. Nat. Commun. 13(1), 4658 (2022).
    • 62. Hou M, Wu X, Zhao Z et al. Endothelial cell-targeting, ROS-ultrasensitive drug/siRNA co-delivery nanocomplexes mitigate early-stage neutrophil recruitment for the anti-inflammatory treatment of myocardial ischemia reperfusion injury. Acta Biomater. 143, 344–355 (2022).
    • 63. Kobayashi SD, Voyich JM, Braughton KR, Deleo FR. Down-regulation of proinflammatory capacity during apoptosis in human polymorphonuclear leukocytes. J. Immunol. 170(6), 3357–3368 (2003).
    • 64. Barone A, D'avanzo N, Cristiano MC et al. Macrophage-derived extracellular vesicles: a promising tool for personalized cancer therapy. Biomedicines 10(6), 1252 (2022).
    • 65. Zhang CY, Dong X, Gao J et al. Nanoparticle-induced neutrophil apoptosis increases survival in sepsis and alleviates neurological damage in stroke. Sci. Adv. 5(11), eaax7964 (2019).
    • 66. Kala SG, Chinni S. Development and characterization of venetoclax nanocrystals for oral bioavailability enhancement. AAPS PharmSciTech 22(3), 92 (2021).
    • 67. Su R, Wang H, Xiao C et al. Venetoclax nanomedicine alleviates acute lung injury via increasing neutrophil apoptosis. Biomater. Sci. 9(13), 4746–4754 (2021). • Venetoclax nanodrug was used to reduce acute lung injury by increasing neutrophil apoptosis.
    • 68. Shi J, Li J. Neutrophil-targeted engineered prodrug nanoparticles for anti-inflammation. FASEB J 34(8), 9828–9831 (2020).
    • 69. Eyles JL, Hickey MJ, Norman MU et al. A key role for G-CSF-induced neutrophil production and trafficking during inflammatory arthritis. Blood 112(13), 5193–5201 (2008).
    • 70. Kruger P, Saffarzadeh M, Weber AN et al. Neutrophils: between host defence, immune modulation, and tissue injury. PLOS Pathogens 11(3), e1004651 (2015).
    • 71. Brennan FM, Zachariae CO, Chantry D et al. Detection of interleukin 8 biological activity in synovial fluids from patients with rheumatoid arthritis and production of interleukin 8 mRNA by isolated synovial cells. Eur. J. Immunol. 20(9), 2141–2144 (1990).
    • 72. Emmi G, Becatti M, Bettiol A et al. Behcet's syndrome as a model of thrombo-inflammation: the role of neutrophils. Front. Immunol. 10, 1085 (2019).
    • 73. O'Neil LJ, Kaplan MJ. Neutrophils in rheumatoid arthritis: breaking immune tolerance and fueling disease. Trends Mol. Med. 25(3), 215–227 (2019).
    • 74. Gajbhiye KR, Gajbhiye V, Siddiqui IA, Gajbhiye JM. cRGD functionalised nanocarriers for targeted delivery of bioactives. J. Drug Target. 27(2), 111–124 (2019).
    • 75. Sadik CD, Kim ND, Iwakura Y, Luster AD. Neutrophils orchestrate their own recruitment in murine arthritis through C5aR and FcγR signaling. Proc. Natl. Acad. Sci. USA 109(46), E3177–E3185 (2012).
    • 76. Wang Z, Li J, Cho J, Malik AB. Prevention of vascular inflammation by nanoparticle targeting of adherent neutrophils. Nat. Nanotechnol. 9(3), 204–210 (2014).
    • 77. Chu D, Gao J, Wang Z. Neutrophil-mediated delivery of therapeutic nanoparticles across blood vessel barrier for treatment of inflammation and infection. ACS Nano 9(12), 11800–11811 (2015).
    • 78. Lyu J, Wang L, Bai X et al. Treatment of rheumatoid arthritis by serum albumin nanoparticles coated with mannose to target neutrophils. ACS Appl. Mater. Interfaces 13(1), 266–276 (2021).
    • 79. Fan C, Li C, Lu S et al. Polysialic acid self-assembled nanocomplexes for neutrophil-based immunotherapy to suppress lung metastasis of breast cancer. AAPS PharmSciTech 23(4), 109 (2022).
    • 80. Raffler NA, Rivera-Nieves J, Ley K. L-selectin in inflammation, infection and immunity. Drug Discov. Today Ther. Strat. 2(3), 213–220 (2005).
    • 81. Hu L, Luo X, Zhou S et al. Neutrophil-mediated delivery of dexamethasone palmitate-loaded liposomes decorated with a sialic acid conjugate for rheumatoid arthritis treatment. Pharm. Res. 36(7), 97 (2019).
    • 82. Haroon HB, Hunter AC, Farhangrazi ZS, Moghimi SM. A brief history of long circulating nanoparticles. Adv. Drug Deliv. Rev. 188, 114396 (2022).
    • 83. Luk BT, Zhang L. Cell membrane-camouflaged nanoparticles for drug delivery. J. Control. Rel. 220(Pt B), 600–607 (2015).
    • 84. Yurkin ST, Wang Z. Cell membrane-derived nanoparticles: emerging clinical opportunities for targeted drug delivery. Nanomedicine 12(16), 2007–2019 (2017).
    • 85. Rampado R, Biccari A, D'Angelo E et al. Optimization of biomimetic, leukocyte-mimicking nanovesicles for drug delivery against colorectal cancer using a design of experiment approach. Front. Bioeng. Biotechnol. 10, 883034 (2022).
    • 86. Matsuzaka Y, Yashiro R. Therapeutic strategy of mesenchymal-stem-cell-derived extracellular vesicles as regenerative medicine. Int. J. Mol. Sci. 23(12), 6480(2022).
    • 87. Dostalova S, Vasickova K, Hynek D et al. Apoferritin as an ubiquitous nanocarrier with excellent shelf life. Int. J. Nanomed. 12, 2265–2278 (2017).
    • 88. Veroniaina H, Pan X, Wu Z, Qi X. Apoferritin: a potential nanocarrier for cancer imaging and drug delivery. Expert Rev. Anticancer Ther. 21(8), 901–913 (2021).
    • 89. Xue J, Zhao Z, Zhang L et al. Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence. Nat. Nanotechnol. 12(7), 692–700 (2017).
    • 90. Wu M, Zhang H, Tie C et al. MR imaging tracking of inflammation-activatable engineered neutrophils for targeted therapy of surgically treated glioma. Nat. Commun. 9(1), 4777 (2018).
    • 91. Ju C, Wen Y, Zhang L et al. Neoadjuvant chemotherapy based on abraxane/human neutrophils cytopharmaceuticals with radiotherapy for gastric cancer. Small 15(5), e1804191 (2019).
    • 92. Ye B, Zhao B, Wang K et al. Neutrophils mediated multistage nanoparticle delivery for prompting tumor photothermal therapy. J. Nanobiotechnol. 18(1), 138 (2020).
    • 93. Sun R, Wang X, Nie Y et al. Targeted trapping of endogenous endothelial progenitor cells for myocardial ischemic injury repair through neutrophil-mediated SPIO nanoparticle-conjugated CD34 antibody delivery and imaging. Acta Biomater. 146, 421–433 (2022).
    • 94. Kang T, Zhu Q, Wei D et al. Nanoparticles coated with neutrophil membranes can effectively treat cancer metastasis. ACS Nano 11(2), 1397–1411 (2017).
    • 95. Zhang Q, Dehaini D, Zhang Y et al. Neutrophil membrane-coated nanoparticles inhibit synovial inflammation and alleviate joint damage in inflammatory arthritis. Nat. Nanotechnol. 13(12), 1182–1190 (2018).
    • 96. Zhou X, Cao X, Tu H et al. Inflammation-targeted delivery of celastrol via neutrophil membrane-coated nanoparticles in the management of acute pancreatitis. Mol. Pharm. 16(3), 1397–1405 (2019).
    • 97. Liu Z, Liu X, Yang Q et al. Neutrophil membrane-enveloped nanoparticles for the amelioration of renal ischemia-reperfusion injury in mice. Acta Biomater. 104, 158–166 (2020).
    • 98. Zhang Z, Li D, Cao Y et al. Biodegradable hypocrellin B nanoparticles coated with neutrophil membranes for hepatocellular carcinoma photodynamics therapy effectively via JUNB/ROS signaling. Int. Immunopharmacol. 99, 107624 (2021).
    • 99. Hassanzadeh P, Arbabi E, Rostami F. Coating of ferulic acid-loaded silk fibroin nanoparticles with neutrophil membranes: a promising strategy against the acute pancreatitis. Life Sci. 270, 119128 (2021).
    • 100. Xie W, Liu P, Gao F et al. Platelet-neutrophil hybrid membrane-coated gelatin nanoparticles for enhanced targeting ability and intelligent release in the treatment of non-alcoholic steatohepatitis. Nanomed. Nanotechnol. Biol. Med. 42, 102538 (2022). •• The authors used a platelet–neutrophil mixed membrane coated with gelatin nanoparticles to enhance hepatitis targeting and intelligent release function.
    • 101. Gao J, Chu D, Wang Z. Cell membrane-formed nanovesicles for disease-targeted delivery. J. Control. Rel. 224, 208–216 (2016).
    • 102. Gao J, Wang S, Wang Z. High yield, scalable and remotely drug-loaded neutrophil-derived extracellular vesicles (EVs) for anti-inflammation therapy. Biomaterials 135, 62–73 (2017).
    • 103. Dong X, Gao J, Zhang CY et al. Neutrophil membrane-derived nanovesicles alleviate inflammation to protect mouse brain injury from ischemic stroke. ACS Nano 13(2), 1272–1283 (2019).
    • 104. Gao J, Dong X, Su Y, Wang Z. Human neutrophil membrane-derived nanovesicles as a drug delivery platform for improved therapy of infectious diseases. Acta Biomaterialia 123, 354–363 (2021).
    • 105. Wang J, Tang W, Yang M et al. Inflammatory tumor microenvironment responsive neutrophil exosomes-based drug delivery system for targeted glioma therapy. Biomaterials 273, 120784 (2021).
    • 106. Zhang J, Ji C, Zhang H et al. Engineered neutrophil-derived exosome-like vesicles for targeted cancer therapy. Sci. Adv. 8(2), eabj8207 (2022).
    • 107. Zhang L, Qin Z, Sun H et al. Nanoenzyme engineered neutrophil-derived exosomes attenuate joint injury in advanced rheumatoid arthritis via regulating inflammatory environment. Bioact. Mater. 18, 1–14 (2022). •• The authors used the inflammatory chemotaxis and anti-inflammatory capabilities of neutrophil-derived EVs to prepare drug-loaded nanoparticles.
    • 108. Ishida T, Atobe K, Wang X, Kiwada H. Accelerated blood clearance of PEGylated liposomes upon repeated injections: effect of doxorubicin-encapsulation and high-dose first injection. J. Control. Rel. 115(3), 251–258 (2006).
    • 109. Ishida T, Ichihara M, Wang X et al. Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. J. Control. Rel. 112(1), 15–25 (2006).
    • 110. Wang D, Wang S, Zhou Z et al. White blood cell membrane-coated nanoparticles: recent development and medical applications. Adv. Healthc. Mater. 11(7), e2101349 (2022).
    • 111. Larsen C, Ostergaard J, Larsen SW et al. Intra-articular depot formulation principles: role in the management of postoperative pain and arthritic disorders. J. Pharm. Sci. 97(11), 4622–4654 (2008).
    • 112. Simón-Vázquez R, Tsapis N, Lorscheider M et al. Improving dexamethasone drug loading and efficacy in treating arthritis through a lipophilic prodrug entrapped into PLGA-PEG nanoparticles. Drug Deliv. Transl. Res. 12(5), 1270–1284 (2022).
    • 113. Chen Y, Wu Q, Zhang Z et al. Preparation of curcumin-loaded liposomes and evaluation of their skin permeation and pharmacodynamics. Molecules 17(5), 5972–5987 (2012).
    • 114. Liu X, Zhang L, Jiang W et al. In vitro and in vivo evaluation of liposomes modified with polypeptides and red cell membrane as a novel drug delivery system for myocardium targeting. Drug Deliv. 27(1), 599–606 (2020).
    • 115. Liu P, Gu L, Ren L et al. Intra-articular injection of etoricoxib-loaded PLGA-PEG-PLGA triblock copolymeric nanoparticles attenuates osteoarthritis progression. Am. J. Transl. Res. 11(11), 6775–6789 (2019).
    • 116. Dong J, Jiang D, Wang Z et al. Intra-articular delivery of liposomal celecoxib-hyaluronate combination for the treatment of osteoarthritis in rabbit model. Int. J. Pharm. 441(1-2), 285–290 (2013).
    • 117. Casares D, Escribá PV, Rosselló CA. Membrane lipid composition: effect on membrane and organelle structure, function and compartmentalization and therapeutic avenues. Int. J. Mol. Sci. 20(9), (2019).
    • 118. Liang T, Zhang R, Liu X et al. Recent advances in macrophage-mediated drug delivery systems. Int. J. Nanomed. 16, 2703–2714 (2021).
    • 119. Rauchhaus U, Schwaiger FW, Panzner S. Separating therapeutic efficacy from glucocorticoid side-effects in rodent arthritis using novel, liposomal delivery of dexamethasone phosphate: long-term suppression of arthritis facilitates interval treatment. Arthritis Res. Ther. 11(6), R190 (2009).
    • 120. Song G, Petschauer JS, Madden AJ, Zamboni WC. Nanoparticles and the mononuclear phagocyte system: pharmacokinetics and applications for inflammatory diseases. Curr. Rheumatol. Rev. 10(1), 22–34 (2014).
    • 121. Li SD, Huang L. Pharmacokinetics and biodistribution of nanoparticles. Mol. Pharm. 5(4), 496–504 (2008).
    • 122. Mirkasymov AB, Zelepukin IV, Nikitin PI et al. In vivo blockade of mononuclear phagocyte system with solid nanoparticles: efficiency and affecting factors. J. Control. Rel. 330, 111–118 (2021).
    • 123. Wang K, Lei Y, Xia D et al. Neutrophil membranes coated, antibiotic agent loaded nanoparticles targeting to the lung inflammation. Colloids and Surfaces. B Biointerfaces 188, 110755 (2020).
    • 124. Li W, Su Z, Hao M, Ju C, Zhang C. Cytopharmaceuticals: an emerging paradigm for drug delivery. J. Control. Rel. 328, 313–324 (2020).
    • 125. Neog MK, Rasool M. Targeted delivery of p-coumaric acid encapsulated mannosylated liposomes to the synovial macrophages inhibits osteoclast formation and bone resorption in the rheumatoid arthritis animal model. Eur. J. Pharm. Biopharm. 133, 162–175 (2018).
    • 126. Vijayan V, Uthaman S, Park IK. Cell membrane coated nanoparticles: an emerging biomimetic nanoplatform for targeted bioimaging and therapy. Adv. Exp. Med. Biol. 1064, 45–59 (2018).
    • 127. Godfrin Y, Horand F, Franco R et al. International seminar on the red blood cells as vehicles for drugs. Exp. Opin. Biol. Ther. 12(1), 127–133 (2012).
    • 128. Xu P, Zuo H, Zhou R et al. Doxorubicin-loaded platelets conjugated with anti-CD22 mAbs: a novel targeted delivery system for lymphoma treatment with cardiopulmonary avoidance. Oncotarget 8(35), 58322–58337 (2017).
    • 129. Stuckey DW, Shah K. Stem cell-based therapies for cancer treatment: separating hope from hype. Nat. Rev. Cancer 14(10), 683–691 (2014).
    • 130. Li Z, Huang H, Tang S et al. Small gold nanorods laden macrophages for enhanced tumor coverage in photothermal therapy. Biomaterials 74, 144–154 (2016).
    • 131. Ma Q, Cao J, Gao Y et al. Microfluidic-mediated nano-drug delivery systems: from fundamentals to fabrication for advanced therapeutic applications. Nanoscale 12(29), 15512–15527 (2020).
    • 132. Su Y, Xie Z, Kim GB et al. Design strategies and applications of circulating cell-mediated drug delivery systems. ACS Biomater. Sci. Eng. 1(4), 201–217 (2015).
    • 133. Yu H, Yang Z, Li F et al. Cell-mediated targeting drugs delivery systems. Drug Deliv. 27(1), 1425–1437 (2020).
    • 134. Kaltenmeier C, Yazdani HO, Handu S et al. The role of neutrophils as a driver in hepatic ischemia-reperfusion injury and cancer growth. Front. Immunol. 13, 887565 (2022).
    • 135. Gao J, Hu X, Xu C et al. Neutrophil-mediated delivery of the combination of colistin and azithromycin for the treatment of bacterial infection. iScience 25(9), 105035 (2022).
    • 136. Salvermoser M, Begandt D, Alon R, Walzog B. Nuclear deformation during neutrophil migration at sites of inflammation. Front. Immunol. 9, 2680 (2018).
    • 137. Pick R, Brechtefeld D, Walzog B. Intraluminal crawling versus interstitial neutrophil migration during inflammation. Mol. Immunol. 55(1), 70–75 (2013).
    • 138. Yuan H, Li J, Bao G, Zhang S. Variable nanoparticle-cell adhesion strength regulates cellular uptake. Phys. Rev. Lett. 105(13), 138101 (2010).
    • 139. Pillay J, Den Braber I, Vrisekoop N et al. In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116(4), 625–627 (2010).
    • 140. Chen J, Song Y, Wang Q et al. Targeted neutrophil-mimetic liposomes promote cardiac repair by adsorbing proinflammatory cytokines and regulating the immune microenvironment. J. Nanobiotechnol. 20(1), 218 (2022).
    • 141. Liu S, Xu J, Liu Y et al. Neutrophil-biomimetic ‘nanobuffer’ for remodeling the microenvironment in the infarct core and protecting neurons in the penumbra via neutralization of detrimental factors to treat ischemic stroke. ACS Appl. Mater. Interfaces 14(24), 27743–27761 (2022).
    • 142. Yang Y, Wang K, Pan Y et al. Engineered cell membrane-derived nanoparticles in immune modulation. Adv. Sci. 8(24), e2102330 (2021).
    • 143. Wu Z, Zhang H, Yan J et al. Engineered biomembrane-derived nanoparticles for nanoscale theranostics. Theranostics 13(1), 20–39 (2023).
    • 144. Chen T, Li Y, Sun R et al. Receptor-mediated NETosis on neutrophils. Front. Immunol. 12, 775267 (2021).
    • 145. Nie M, Yang L, Bi X et al. Neutrophil extracellular traps induced by IL8 promote diffuse large b-cell lymphoma progression via the TLR9 signaling. Clin. Cancer Res. 25(6), 1867–1879 (2019).
    • 146. Yáñez-Mó M, Siljander PR, Andreu Z et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles 4, 27066 (2015).
    • 147. Lu M, Xing H, Yang Z et al. Recent advances on extracellular vesicles in therapeutic delivery: challenges, solutions, and opportunities. Eur. J. Pharm. Biopharm. 119, 381–395 (2017).
    • 148. Lu S, Wang R, Fu W, Si Y. Applications of extracellular vesicles in abdominal aortic aneurysm. Front. Cardiovasc. Med. 9, 927542 (2022).
    • 149. Pfister H. Neutrophil extracellular traps and neutrophil-derived extracellular vesicles: common players in neutrophil effector functions. Diagnostics 12(7), 1715 (2022).
    • 150. Bie N, Yong T, Wei Z et al. Extracellular vesicles for improved tumor accumulation and penetration. Adv. Drug Deliv. Rev. 188, 114450 (2022).
    • 151. Rezaie J, Nejati V, Mahmoodi M, Ahmadi M. Mesenchymal stem cells derived extracellular vesicles: a promising nanomedicine for drug delivery system. Biochem. Pharmacol. 203, 115167 (2022).