Targeted gene silencing of TLR4 using liposomal nanoparticles for preventing liver ischemia reperfusion injury

American Journal of Transplantation

Volumn 11, Issue 9, 2011, Pages 1835-1844

  Jiang, N ^a,b,c   Zhang, X ^a,b   Zheng, X ^a,b   Chen, D ^b   Zhang, Y ^b   Siu, L K S ^b   Xin, H B ^d   Li, R ^d   Zhao, H ^e   Riordan, N ^f   Ichim, T E ^f   Quan, D ^a,b   Jevnikar, A M ^a   Chen, G ^c   Min, W ^a,b,c  

^a LONDON HEALTH SCIENCES CENTRE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c SUN YAT SEN UNIVERSITY   (China)

^d NANCHANG UNIVERSITY   (China)

^e PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^f Medistem Panama City of Knowledge   (Panama)

Author keywords

Gene silencing; ischemia reperfusion injury; liposomes; liver; siRNA; TLR4

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GALACTOSE; INTERLEUKIN 1; LIPOSOME; MALONALDEHYDE; MYELOPEROXIDASE; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; GENE SILENCING; HISTOPATHOLOGY; IN VIVO STUDY; LIVER CELL; LIVER ISCHEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; TREATMENT RESPONSE;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; GENE SILENCING; IMMUNOHISTOCHEMISTRY; LIPOSOMES; LIVER; MICE; NANOPARTICLES; POLYMERASE CHAIN REACTION; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; TOLL-LIKE RECEPTOR 4;

EID: 80052264101     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2011.03660.x     Document Type: Article

References (56)

1. Fondevila C, Busuttil RW, Kupiec-Weglinski JW,. Hepatic ischemia/reperfusion injury-a fresh look. Exp Mol Pathol 2003; 74: 86-93. (Pubitemid 36438656)
2. Laskowski I, Pratschke J, Wilhelm MJ, Gasser M, Tilney NL,. Molecular and cellular events associated with ischemia/reperfusion injury. Ann Transplant 2000; 5: 29-35.
3. Mencin A, Kluwe J, Schwabe RF,. Toll-like receptors as targets in chronic liver diseases. Gut 2009; 58: 704-720.
4. Paterson HM, Murphy TJ, Purcell EJ, et al,. Injury primes the innate immune system for enhanced Toll-like receptor reactivity. J Immunol 2003; 171: 1473-1483. (Pubitemid 36900082)
5. Zhai Y, Qiao B, Shen XD, et al,. Evidence for the pivotal role of endogenous toll-like receptor 4 ligands in liver ischemia and reperfusion injury. Transplantation 2008; 85: 1016-1022. (Pubitemid 351543166)
6. Ellett JD, Evans ZP, Atkinson C, Schmidt MG, Schnellmann RG, Chavin KD,. Toll-like receptor 4 is a key mediator of murine steatotic liver warm ischemia/reperfusion injury. Liver Transpl 2009; 15: 1101-1109.
7. Hui W, Jinxiang Z, Heshui W, Zhuoya L, Qichang Z,. Bone marrow and non-bone marrow TLR4 regulates hepatic ischemia/reperfusion injury. Biochem Biophys Res Commun 2009; 389: 328-332.
8. Ichim TE, Li M, Qian H, et al,. RNA interference: a potent tool for gene-specific therapeutics. Am J Transplant 2004; 4: 1227-1236. (Pubitemid 39013568)
9. Zheng X, Zhang X, Feng B, et al,. Gene silencing of complement C5a receptor using siRNA for preventing ischemia/reperfusion injury. Am J Pathol 2008; 173: 973-980.
10. Zheng X, Feng B, Chen G, et al,. Preventing renal ischemia-reperfusion injury using small interfering RNA by targeting complement 3 gene. Am J Transplant 2006; 6: 2099-2108. (Pubitemid 44199544)
11. Zhang ZX, Beduhn ME, Zheng X, Min WP, Jevnikar AM,. Preventing tissue injury using siRNA. Methods Mol Biol 2010; 623: 341-355.
12. Zhang X, Zheng X, Sun H, et al,. Prevention of renal ischemic injury by silencing the expression of renal caspase 3 and caspase 8. Transplantation 2006; 82: 1728-1732. (Pubitemid 46035659)
13. Zheng X, Zhang X, Sun H, et al,. Protection of renal ischemia injury using combination gene silencing of complement 3 and caspase 3 genes. Transplantation 2006; 82: 1781-1786. (Pubitemid 46035667)
14. Feng B, Chen G, Zheng X, et al,. Small interfering RNA targeting RelB protects against renal ischemia-reperfusion injury. Transplantation 2009; 87: 1283-1289.
15. Zheng X, Lian D, Wong A, et al,. Novel small interfering RNA-containing solution protecting donor organs in heart transplantation. Circulation 2009; 120: 1099-1107, 1091 (p following 1107).
16. Scherr M, Battmer K, Dallmann I, Ganser A, Eder M,. Inhibition of GM-CSF receptor function by stable RNA interference in a NOD/SCID mouse hematopoietic stem cell transplantation model. Oligonucleotides 2003; 13: 353-363. (Pubitemid 38404820)
17. Song E, Lee SK, Wang J, et al,. RNA interference targeting Fas protects mice from fulminant hepatitis. Nat Med 2003; 9: 347-351. (Pubitemid 36362792)
18. Yano J, Hirabayashi K, Nakagawa S, et al,. Antitumor activity of small interfering RNA/cationic liposome complex in mouse models of cancer. Clin Cancer Res 2004; 10: 7721-7726. (Pubitemid 39557537)
19. Zhang G, Gao X, Song YK, et al,. Hydroporation as the mechanism of hydrodynamic delivery. Gene Ther 2004; 11: 675-682. (Pubitemid 38519275)
20. Wu SY, McMillan NA,. Lipidic systems for in vivo siRNA delivery. AAPS J 2009; 11: 639-652.
21. Wagner E,. Application of membrane-active peptides for nonviral gene delivery. Adv Drug Deliv Rev 1999; 38: 279-289. (Pubitemid 29376578)
22. West MA, Billiar TR, Curran RD, Hyland BJ, Simmons RL,. Evidence that rat Kupffer cells stimulate and inhibit hepatocyte protein synthesis in vitro by different mechanisms. Gastroenterology 1989; 96: 1572-1582. (Pubitemid 19138703)
23. Gabizon A, Horowitz AT, Goren D, et al,. Targeting folate receptor with folate linked to extremities of poly(ethylene glycol)-grafted liposomes: In vitro studies. Bioconjug Chem 1999; 10: 289-298. (Pubitemid 29147733)
24. Li SD, Chono S, Huang L,. Efficient gene silencing in metastatic tumor by siRNA formulated in surface-modified nanoparticles. J Control Release 2008; 126: 77-84.
25. Abe Y, Hines IN, Zibari G, et al,. Mouse model of liver ischemia and reperfusion injury: method for studying reactive oxygen and nitrogen metabolites in vivo. Free Radic Biol Med 2009; 46: 1-7.
26. Suzuki S, Toledo-Pereyra LH, Rodriguez FJ, Cejalvo D,. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation 1993; 55: 1265-1272. (Pubitemid 23183235)
27. Tsuchihashi S, Livhits M, Zhai Y, Busuttil RW, Araujo JA, Kupiec-Weglinski JW,. Basal rather than induced heme oxygenase-1 levels are crucial in the antioxidant cytoprotection. J Immunol 2006; 177: 4749-4757. (Pubitemid 44469809)
28. Kaya H, Sezik M, Ozkaya O, Dittrich R, Siebzehnrubl E, Wildt L,. Lipid peroxidation at various estradiol concentrations in human circulation during ovarian stimulation with exogenous gonadotropins. Horm Metab Res 2004; 36: 693-695. (Pubitemid 39486969)
29. Wang H, Joseph JA,. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 1999; 27: 612-616. (Pubitemid 29408648)
30. Dhillon N, Walsh L, Kruger B, et al,. A single nucleotide polymorphism of Toll-like receptor 4 identifies the risk of developing graft failure after liver transplantation. J Hepatol; 53: 67-72.
31. Li SD, Huang L,. Targeted delivery of antisense oligodeoxynucleotide and small interference RNA into lung cancer cells. Mol Pharm 2006; 3: 579-588. (Pubitemid 44639135)
32. Nomura T, Nakajima S, Kawabata K, Yamashita F, Takakura Y, Hashida M,. Intratumoral pharmacokinetics and in vivo gene expression of naked plasmid DNA and its cationic liposome complexes after direct gene transfer. Cancer Res 1997; 57: 2681-2686. (Pubitemid 27283780)
33. Schroeder A, Levins CG, Cortez C, Langer R, Anderson DG,. Lipid-based nanotherapeutics for siRNA delivery. J Intern Med 2010; 267: 9-21.
34. Ke B, Shen XD, Gao F, et al,. Small interfering RNA targeting heme oxygenase-1 (HO-1) reinforces liver apoptosis induced by ischemia-reperfusion injury in mice: HO-1 is necessary for cytoprotection. Hum Gene Ther 2009; 20: 1133-1142.
35. Tsung A, Klune JR, Zhang X, et al,. HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med 2007; 204: 2913-2923. (Pubitemid 350179560)
36. Lentsch AB, Kato A, Yoshidome H, McMasters KM, Edwards MJ,. Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury. Hepatology 2000; 32: 169-173. (Pubitemid 30614647)
37. Hashida M, Nishikawa M, Yamashita F, Takakura Y,. Cell-specific delivery of genes with glycosylated carriers. Adv Drug Deliv Rev 2001; 52: 187-196. (Pubitemid 33097545)
38. Mukthavaram R, Marepally S, Venkata MY, Vegi GN, Sistla R, Chaudhuri A,. Cationic glycolipids with cyclic and open galactose head groups for the selective targeting of genes to mouse liver. Biomaterials 2009; 30: 2369-2384.
39. Ni HM, Chen X, Ding WX, Schuchmann M, Yin XM,. Differential roles of JNK in ConA/GalN and ConA-induced liver injury in mice. Am J Pathol 2008; 173: 962-972.
40. Takeda K, Kaisho T, Akira S,. Toll-like receptors. Annu Rev Immunol 2003; 21: 335-376. (Pubitemid 37174535)
41. Jiang H, Meng F, Li W, Tong L, Qiao H, Sun X,. Splenectomy ameliorates acute multiple organ damage induced by liver warm ischemia reperfusion in rats. Surgery 2007; 141: 32-40. (Pubitemid 44918074)
42. Dybdahl B, Wahba A, Lien E, et al,. Inflammatory response after open heart surgery: Release of heat-shock protein 70 and signaling through toll-like receptor-4. Circulation 2002; 105: 685-690. (Pubitemid 34157370)
43. Beg AA,. Endogenous ligands of Toll-like receptors: Implications for regulating inflammatory and immune responses. Trends Immunol 2002; 23: 509-512. (Pubitemid 35223541)
44. Liu S, Gallo DJ, Green AM, et al,. Role of toll-like receptors in changes in gene expression and NF-kappa B activation in mouse hepatocytes stimulated with lipopolysaccharide. Infect Immun 2002; 70: 3433-3442. (Pubitemid 34665980)
45. Isogawa M, Robek MD, Furuichi Y, Chisari FV,. Toll-like receptor signaling inhibits hepatitis B virus replication in vivo. J Virol 2005; 79: 7269-7272. (Pubitemid 40677357)
46. Seki E, De Minicis S, Osterreicher CH, et al,. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 2007; 13: 1324-1332. (Pubitemid 350073596)
47. Volpes R, van den Oord JJ, Desmet VJ,. Can hepatocytes serve as 'activated' immunomodulating cells in the immune response? J Hepatol 1992; 16: 228-240. (Pubitemid 23013204)
48. Vodovotz Y, Liu S, McCloskey C, Shapiro R, Green A, Billiar TR,. The hepatocyte as a microbial product-responsive cell. J Endotoxin Res 2001; 7: 365-373. (Pubitemid 34048537)
49. Yamamoto M, Sato S, Hemmi H, et al,. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 2002; 420: 324-329. (Pubitemid 35398188)
50. Yamamoto M, Sato S, Hemmi H, et al,. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 2003; 4: 1144-1150. (Pubitemid 37428043)
51. Akira S, Uematsu S, Takeuchi O,. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801. (Pubitemid 43261452)
52. Tazi KA, Quioc JJ, Saada V, Bezeaud A, Lebrec D, Moreau R,. Upregulation of TNF-alpha production signaling pathways in monocytes from patients with advanced cirrhosis: possible role of Akt and IRAK-M. J Hepatol 2006; 45: 280-289. (Pubitemid 44026567)
53. Adachi O, Kawai T, Takeda K, et al,. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998; 9: 143-150. (Pubitemid 28361303)
54. Zhai Y, Shen XD, O'Connell R, et al,. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway. J Immunol 2004; 173: 7115-7119. (Pubitemid 39628144)
55. Hensler T, Sauerland S, Bouillon B, et al,. Association between injury pattern of patients with multiple injuries and circulating levels of soluble tumor necrosis factor receptors, interleukin-6 and interleukin-10, and polymorphonuclear neutrophil elastase. J Trauma 2002; 52: 962-970. (Pubitemid 34534485)
56. Shen XD, Ke B, Zhai Y, Gao F, et al,. Absence of toll-like receptor 4 (TLR4) signaling in the donor organ reduces ischemia and reperfusion injury in a murine liver transplantation model. Liver Transpl 2007; 13: 1435-1443. (Pubitemid 47629578)