Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence

Nature Nanotechnology

Volumn 12, Issue 7, 2017, Pages 692-700

  Xue, Jingwei ^a   Zhao, Zekai ^a   Zhang, Lei ^a   Xue, Lingjing ^a   Shen, Shiyang ^a   Wen, Yajing ^a   Wei, Zhuoyuan ^a   Wang, Lu ^a   Kong, Lingyi ^a   Sun, Hongbin ^a   Ping, Qineng ^a   Mo, Ran ^a   Zhang, Can ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOSOMES; MAMMALS; TARGETED DRUG DELIVERY; TUMORS;

ANTI-CANCER DRUG DELIVERY; BRAIN TUMOURS; DRUG DELIVERY SYSTEM; IMMUNE CELLS; MALIGNANT GLIOMA; PACLITAXEL; SURVIVAL RATE; TUMOUR CELLS;

CONTROLLED DRUG DELIVERY;

CXCL1 CHEMOKINE; INTERLEUKIN 10; LIPOSOME; PACLITAXEL; TUMOR NECROSIS FACTOR; ANTINEOPLASTIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; ARTICLE; CANCER INHIBITION; CANCER RECURRENCE; CANCER SURVIVAL; CELL INFILTRATION; CELL ISOLATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG FORMULATION; DRUG PENETRATION; DRUG RELEASE; DRUG SYNTHESIS; DRUG TARGETING; ENCAPSULATION; ENCEPHALITIS; GLIOBLASTOMA; HISTOLOGY; HUMAN; HUMAN CELL; MALE; MOUSE; NEUTROPHIL; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SURVIVAL RATE; TUMOR CELL; TUMOR INVASION; ANIMAL; BAGG ALBINO MOUSE; BRAIN TUMOR; CHEMISTRY; DRUG SCREENING; GLIOMA; METABOLISM; NUDE MOUSE; PATHOLOGY; PREVENTION AND CONTROL; PROCEDURES; TUMOR CELL LINE; TUMOR RECURRENCE;

ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; GLIOMA; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM RECURRENCE, LOCAL; NEUTROPHILS; PACLITAXEL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85022324338     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2017.54     Document Type: Article

References (54)

1. Gladson, C. L., Prayson, R. A. & Liu, W. M. The pathobiology of glioma tumors. Annu. Rev. Pathol. 5, 33-50 (2010).
2. Agrawal, N. S. et al. Current studies of immunotherapy on glioblastoma. J. Neurol. Neurosurg. 1, 1000104 (2014).
3. Huse, J. T. & Holland, E. C. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat. Rev. Cancer 10, 319-331 (2010).
4. Park, J. K. et al. Scale to predict survival after surgery for recurrent glioblastoma multiforme. J. Clin. Oncol. 28, 3838-3843 (2010).
5. Lacroix, M. et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J. Neurosurg. 95, 190-198 (2001).
6. Ballabh, P., Braun, A. & Nedergaard, M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 16, 1-13 (2004).
7. Stern, J. I. & Raizer, J. J. Chemotherapy in the treatment of malignant gliomas. Expert Rev. Anticancer Ther. 6, 755-767 (2006).
8. Peer, D. et al. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotech. 2, 751-760 (2007).
9. Mo, R. & Gu, Z. Tumor microenvironment and intracellular signal-activated nanomaterials for anticancer drug delivery. Mater. Today 19, 274-283 (2016).
10. Lu, Y., Aimetti, A. A., Langer, R. & Gu, Z. Bioresponsive materials. Nat. Mater. Rev. 1, 16075 (2016).
11. Mangraviti, A., Gullotti, D., Tyler, B. & Brem, H. Nanobiotechnology-based delivery strategies: new frontiers in brain tumor targeted therapies. J. Control. Release 240, 443-453 (2016).
12. Jain, R. K. & Stylianopoulos, T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7, 653-664 (2010).
13. Huynh, G. H., Deen, D. F. & Szoka, F. C. Barriers to carrier mediated drug and gene delivery to brain tumors. J. Control. Release 110, 236-259 (2006).
14. Pierige, F., Serafini, S., Rossi, L. & Magnani, M. Cell-based drug delivery. Adv. Drug Deliv. Rev. 60, 286-295 (2008).
15. Batrakova, E. V., Gendelman, H. E. & Kabanov, A. V. Cell-mediated drug delivery. Expert Opin. Drug Deliv. 8, 415-433 (2011).
16. Gu, L. & Mooney, D. J. Biomaterials and emerging anticancer therapeutics: engineering the microenvironment. Nat. Rev. Cancer. 16, 56-66 (2016).
17. Bernardes-Silva, M., Anthony, D. C., Issekutz, A. C. & Perry, V. H. Recruitment of neutrophils across the blood-brain barrier: the role of E- and P-selectins. J. Cereb. Blood Flow Metab. 21, 1115-1124 (2001).
18. Joice, S. L. et al. Modulation of blood-brain barrier permeability by neutrophils: in vitro and in vivo studies. Brain Res. 1298, 13-23 (2009).
19. Fossati, G. et al. Neutrophil infiltration into human gliomas. Acta Neuropathol. 98, 349-354 (1999).
20. Qin, J. et al. Surface modification of RGD-liposomes for selective drug delivery to monocytes/neutrophils in brain. Chem. Pharm. Bull. 55, 1192-1197 (2007).
21. Mishalian, I. et al. Tumor-associated neutrophils (TAN) develop pro-tumorigenic properties during tumor progression. Cancer Immunol. Immunother. 62, 1745-1756 (2013).
22. Gregory, A. D. & Houghton, A. M. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res. 71, 2411-2416 (2011).
23. Salmaggi, A. et al. Intracavitary vEGF, bFGF, IL-8, IL-12 levels in primary and recurrent malignant glioma. J. Neurooncol. 62, 297-303 (2003).
24. Brat, D. J., Bellail, A. C. & Van Meir, E. G. The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neuro. Oncol. 7, 122-133 (2005).
25. Ryuto, M. et al. Induction of vascular endothelial growth factor by tumor necrosis factor α in human glioma cells. Possible roles of SP-1. J. Biol. Chem. 271, 28220-28228 (1996).
26. Nabors, L. B. et al. Tumor necrosis factor α induces angiogenic factor up-regulation in malignant glioma cells: a role for RNA stabilization and HuR. Cancer Res. 63, 4181-4187 (2003).
27. Kolaczkowska, E. & Kubes, P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159-175 (2013).
28. Postma, T. J. et al. A phase II study of paclitaxel in chemonaïve patients with recurrent high-grade glioma. Ann. Oncol. 11, 409-413 (2000).
29. Lidar, Z. et al. Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: a phase I/II clinical study. J. Neurosurg. 100, 472-479 (2004).
30. Ley, K., Laudanna, C., Cybulsky, M. I. & Nourshargh, S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689 (2007).
31. Brinkmann, V. et al. Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535 (2004).
32. Keshari, R. S. et al. Cytokines induced neutrophil extracellular traps formation: implication for the inflammatory disease condition. PLoS ONE 7, e48111 (2012).
33. Boxio, R., Bossenmeyer-Pourié, C., Steinckwich, N., Dournon, C. & Nüsse, O. Mouse bone marrow contains large numbers of functionally competent neutrophils. J. Leukoc. Biol. 75, 604-611 (2004).
34. Anderson, D. C., Miller, L. J., Schmalstieg, F. C., Rothlein, R. & Springer, T. A. Contributions of the Mac-I glycoprotein family to adherence-dependent granulocyte functions: structure-function assessments employing subunitspecific monoclonal antibodies. J. Immunol. 137, 15-27 (1986).
35. Diamond, M. S. & Springer, T. A. A subpopulation of Mac-1 (CD11b/CD18) molecules mediates neutrophil adhesion to ICAM-1 and fibrinogen. J. Cell Biol. 120, 545-556 (1993).
36. Marasco, W. et al. Purification and identification of formyl-methionyl-leucylphenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J. Biol. Chem. 259, 5430-5439 (1984).
37. Heit, B., Liu, L., Colarusso, P., Puri, K. D. & Kubes, P. Pi3k accelerates, but is not required for, neutrophil chemotaxis to fMLP. J. Cell Sci. 121, 205-214 (2008).
38. Paulsson, J. M., Jacobson, S. H. & Lundahl, J. Neutrophil activation during transmigration in vivo and in vitro: a translational study using the skin chamber model. J. Immunol. Methods 361, 82-88 (2010).
39. Akahoshi, T. et al. Rapid induction of neutrophil apoptosis by sulfasalazine: implications of reactive oxygen species in the apoptotic process. J. Leukoc. Biol. 62, 817-826 (1997).
40. Fuchs, T. A. et al. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241 (2007).
41. Li, G. et al. Permeability of endothelial and astrocyte cocultures: in vitro blood-brain barrier models for drug delivery studies. Ann. Biomed. Eng. 38, 2499-2511 (2010).
42. Brown, R. C., Morris, A. P. & O'Neil, R. G. Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells. Brain Res. 1130, 17-30 (2007).
43. Ju, C. et al. Sequential intra-intercellular nanoparticle delivery system for deep tumor penetration. Angew. Chem. Int. Ed. 53, 6253-6258 (2014).
44. Hol, J., Wilhelmsen, L. & Haraldsen, G. The murine IL-8 homologues KC, MIP-2, and LIX are found in endothelial cytoplasmic granules but not in Weibel-Palade bodies. J. Leukoc. Biol. 87, 501-508 (2010).
45. Chauffier, K. et al. Induction of the chemokine IL-8/Kc by the articular cartilage: possible influence on osteoarthritis. Joint Bone Spine 79, 604-609 (2012).
46. Bello, L. et al. Suppression of malignant glioma recurrence in a newly developed animal model by endogenous inhibitors. Clin. Cancer Res. 8, 3539-3548 (2002).
47. Allen, M., Bjerke, M., Edlund, H., Nelander, S. & Westermark, B. Origin of the U87MG glioma cell line: good news and bad news. Sci. Transl. Med. 8, 354re3 (2016).
48. Summers, C. et al. Neutrophil kinetics in health and disease. Trends Immunol. 31, 318-324 (2010).
49. Thurston, G. et al. Cationic liposomes target angiogenic endothelial cells in tumors and chronic inflammation in mice. J. Clin. Invest. 101, 1401-1413 (1998).
50. Partida-Sánchez, S. et al. Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat. Med. 7, 1209-1216 (2001).
51. Iyer, A. K., Khaled, G., Fang, J. & Maeda, H. Exploiting the enhanced permeability and retention effect for tumor targeting. Drug Discov. Today 11, 812-818 (2006).
52. Bertrand, N., Wu, J., Xu, X., Kamaly, N. & Farokhzad, O. C. Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology. Adv. Drug Deliv. Rev. 66, 2-25 (2014).
53. De Filippo, K. et al. Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood 121, 4930-4937 (2013).
54. Mantovani, A., Cassatella, M. A., Costantini, C. & Jaillon, S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531 (2011).