Cationic nanocarriers induce cell necrosis through impairment of Na+/K+-ATPase and cause subsequent inflammatory response

Cell Research

Volumn 25, Issue 2, 2015, Pages 237-253

  Wei, Xiawei ^a   Shao, Bin ^a   He, Zhiyao ^a   Ye, Tinghong ^a   Luo, Min ^a   Sang, Yaxiong ^a   Liang, Xiao ^a   Wang, Wei ^a   Luo, Shuntao ^a   Yang, Shengyong ^a   Zhang, Shuang ^a   Gong, Changyang ^a   Gou, Maling ^a   Deng, Hongxing ^a   Zhao, Yinglan ^a   Yang, Hanshuo ^a   Deng, Senyi ^a   Zhao, Chengjian ^a   Yang, Li ^a   Qian, Zhiyong ^a   Li, Jiong ^a   Sun, Xun ^a   Han, Jiahuai ^b   Jiang, Chengyu ^c   Wu, Min ^d   Zhang, Zhirong ^a   more..

^a SICHUAN UNIVERSITY   (China)

^b XIAMEN UNIVERSITY   (China)

^c PEKING UNION MEDICAL COLLEGE   (China)

^d UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

cationic nanocarriers; damage associated molecular patterns; inflammation; Na+ K+ ATPase; necrosis

Indexed keywords

MUS; STROPHANTHUS GRATUS;

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CATION; CHITOSAN; DRUG CARRIER; LIPOSOME; MITOCHONDRIAL DNA; MYELOID DIFFERENTIATION FACTOR 88; NANOMATERIAL; OUABAIN; POLYETHYLENEIMINE; TLR9 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 9;

ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; MOUSE; NECROSIS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CATIONS; CELL LINE, TUMOR; CHITOSAN; DNA, MITOCHONDRIAL; DRUG CARRIERS; HUMANS; INFLAMMATION; LIPOSOMES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MYELOID DIFFERENTIATION FACTOR 88; NANOSTRUCTURES; NECROSIS; OUABAIN; POLYETHYLENEIMINE; SIGNAL TRANSDUCTION; SODIUM-POTASSIUM-EXCHANGING ATPASE; TOLL-LIKE RECEPTOR 9;

EID: 84961288748     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2015.9     Document Type: Article

References (56)

1. Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at the nano level. Science 2006; 311:622-627
2. Davis ME, Chen ZG, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 2008; 7:771-782
3. Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science 2004; 303:1818-1822
4. Singh R, Lillard JW Jr. Nanoparticle-based targeted drug delivery. Exp Mol Pathol 2009; 86:215-223
5. Fortier C, Durocher Y, De Crescenzo G. Surface modification of nonviral nanocarriers for enhanced gene delivery. Nanomedicine 2014; 9:135-151
6. Wang B, Zhang L, Bae SC, Granick S. Nanoparticle-induced surface reconstruction of phospholipid membranes. Proc Natl Acad Sci USA 2008; 105:18171-18175
7. Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov 2005; 4:145-160
8. Luo D, Saltzman WM. Synthetic DNA delivery systems. Nat Biotechnol 2000; 18:33-37
9. Sunshine JC, Bishop CJ, Green JJ. Advances in polymeric and inorganic vectors for nonviral nucleic acid delivery. Ther Deliv 2011; 2:493-521
10. Wright J. Nanotechnology: Deliver on a promise. Nature 2014; 509:S58-S59
11. Lv H, Zhang S, Wang B, Cui S, Yan J. Toxicity of cationic lipids and cationic polymers in gene delivery. J Control Release 2006; 114:100-109
12. Sharma A, Madhunapantula SV, Robertson GP. Toxicological considerations when creating nanoparticle-based drugs and drug delivery systems. Expert Opin Drug Metab Toxicol 2012; 8:47-69
13. Ilinskaya AN, Dobrovolskaia MA. Nanoparticles and the blood coagulation system. Part II: safety concerns. Nanomedicine 2013; 8:969-981
14. Dobrovolskaia MA, Aggarwal P, Hall JB, McNeil SE. Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. Mol Pharm 2008; 5:487-495
15. Xue HY, Liu S, Wong HL. Nanotoxicity: a key obstacle to clinical translation of siRNA-based nanomedicine. Nanomedicine 2014; 9:295-312
16. Hortobagyi GN, Ueno NT, Xia W, et al. Cationic liposome-mediated E1A gene transfer to human breast and ovarian cancer cells and its biologic effects: a phase I clinical trial. J Clin Oncol 2001; 19:3422-3433
17. Zhang JS, Liu F, Huang L. Implications of pharmacokinetic behavior of lipoplex for its inflammatory toxicity. Adv Drug Deliv Rev 2005; 57:689-698
18. Dass CR. Lipoplex-mediated delivery of nucleic acids: factors affecting in vivo transfection. J Mol Med (Berl) 2004; 82:579-591
19. Tousignant JD, Gates AL, Ingram LA, et al. Comprehensive analysis of the acute toxicities induced by systemic administration of cationic lipid:plasmid DNA complexes in mice. Hum Gene Ther 2000; 11:2493-2513
20. Goula D, Becker N, Lemkine GF, et al. Rapid crossing of the pulmonary endothelial barrier by polyethylenimine/DNA complexes. Gene Ther 2000; 7:499-504
21. Sakurai F, Nishioka T, Yamashita F, et al. Effects of erythrocytes and serum proteins on lung accumulation of lipoplexes containing cholesterol or DOPE as a helper lipid in the single-pass rat lung perfusion system. Eur J Pharm Biopharm 2001; 52:165-172
22. Bragonzi A, Boletta A, Biffi A, et al. Comparison between cationic polymers and lipids in mediating systemic gene delivery to the lungs. Gene Ther 1999; 6:1995-2004
23. Beyerle A, Braun A, Banerjee A, et al. Inflammatory responses to pulmonary application of PEI-based siRNA nanocarriers in mice. Biomaterials 2011; 32:8694-8701
24. Scheule RK, St George JA, Bagley RG, et al. Basis of pul monary toxicity associated with cationic lipid-mediated gene transfer to the mammalian lung. Hum Gene Ther 1997; 8:689-707
25. Sydlik U, Gallitz I, Albrecht C, et al. The compatible solute ectoine protects against nanoparticle-induced neutrophilic lung inflammation. Am J Respir Crit Care Med 2009; 180:29-35
26. Yew NS, Wang KX, Przybylska M, et al. Contribution of plasmid DNA to inflammation in the lung after administration of cationic lipid:pDNA complexes. Hum Gene Ther 1999; 10:223-234
27. Edinger AL, Thompson CB. Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004; 16:663-669
28. Green DR, Ferguson T, Zitvogel L, et al. Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009; 9:353-363
29. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995; 146:3-15
30. Han J, Zhong CQ, Zhang DW. Programmed necrosis: backup to and competitor with apoptosis in the immune system. Nat Immunol 2011; 12:1143-1149
31. Wang H, Sun L, Su L, et al. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell 2014; 54:133-146
32. Cai Z, Jitkaew S, Zhao J, et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 2014; 16:55-65
33. Wu J, Huang Z, Ren J, et al. Mlkl knockout mice demonstrate the indispensable role of Mlkl in necroptosis. Cell Res 2013; 23:994-1006
34. Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol 2008; 8:279-289
35. Rubartelli A, Lotze MT. Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol 2007; 28:429-436
36. Lang BF, Burger G, OKelly CJ, et al. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 1997; 387:493-497
37. Zhang Q, Raoof M, Chen Y, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010; 464:104-107
38. Krysko DV, Agostinis P, Krysko O, et al. Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol 2011; 32:157-164
39. Manfredi AA, Rovere-Querini P. The mitochondrion-a Trojan horse that kicks off inflammation?. N Engl J Med 2010; 362:2132-2134
40. Heller LC, Cruz YL, Ferraro B, Yang H, Heller R. Plasmid injection and application of electric pulses alter endogenous mRNA and protein expression in B16.F10 mouse melanomas. Cancer Gene Ther 2010; 17:864-871
41. Iwaoka S, Nakamura T, Takano S, et al. Cationic liposomes induce apoptosis through p38 MAP kinase-caspase-8-Bid pathway in macrophage-like RAW264.7 cells. J Leukoc Biol 2006; 79:184-191
42. Hasegawa M, Yagi K, Iwakawa S, et al. Chitosan induces apoptosis via caspase-3 activation in bladder tumor cells. Jpn J Cancer Res 2001; 92:459-466
43. Chen X, Li W, Ren J, et al. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res 2014; 24:105-121
44. Palasis M, Kuntzweiler TA, Arguello JM, et al. Ouabain interactions with the H5-H6 hairpin of the Na,K-ATPase reveal a possible inhibition mechanism via the cation binding domain. J Biol Chem 1996; 271:14176-14182
45. Zheng Y, Gardner SE, Clarke MC. Cell death, damage-associated molecular patterns, and sterile inflammation in cardiovascular disease. Arterioscler Thromb Vasc Biol 2011; 31:2781-2786
46. Bundschuh DS, Uhlig S, Wendel A. Isolation of rat primary lung cells: characterization of an improved method. Exp Toxicol Pathol 1996; 48:512-514
47. Saito M, Korsmeyer SJ, Schlesinger PH. BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat Cell Biol 2000; 2:553-555
48. Li XY, Li X, Kong XY, et al. Preparation of N-trimethyl chitosan-protein nanoparticles intended for vaccine delivery. J Nanosci Nanotechnol 2010; 10:4850-4858
49. DHulst A I, Maes T, Bracke KR, et al. Cigarette smoke-induced pulmonary emphysema in scid-mice. Is the acquired immune system required?. Respir Res 2005; 6:147
50. Mello de Queiroz F, Ponte CG, Bonomo A, et al. Study of membrane potential in T lymphocytes subpopulations using flow cytometry. BMC Immunol 2008; 9:63
51. Murphy AJ, Hoover JC. Inhibition of the Na,K-ATPase by fluoride. Parallels with its inhibition of the sarcoplasmic reticulum CaATPase. J Biol Chem 1992; 267:16995-16700
52. Unal-Cevik I, Kilinc M, Can A, et al. Apoptotic and necrotic death mechanisms are concomitantly activated in the same cell after cerebral ischemia. Stroke 2004; 35:2189-2194
53. Krajewski S, Tanaka S, Takayama S, et al. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res 1993; 53:4701-4714
54. Masuyama M, Iida R, Takatsuka H, et al. Quantitative change in mitochondrial DNA content in various mouse tissues during aging. Biochim Biophys Acta 2005; 1723:302-308
55. Bixel MG, Petri B, Khandoga AG, et al. A CD99-related antigen on endothelial cells mediates neutrophil but not lymphocyte extravasation in vivo. Blood 2007; 109:5327-5336
56. Lee HY, Kim MK, Park KS, et al. Group IB secretory phospholipase A2 stimulates leukotriene B4 production by a unique mechanism in human neutrophils. Biochem Biophys Res Commun 2005; 334:500-508