A polymeric nanoparticle formulation of curcumin (NanoCurc) ameliorates CCl 4-induced hepatic injury and fibrosis through reduction of pro-inflammatory cytokines and stellate cell activation

Laboratory Investigation

Volumn 91, Issue 9, 2011, Pages 1383-1395

  Bisht, Savita ^a   Khan, Mehtab A ^a   Bekhit, Mena ^a   Bai, Haibo ^a   Cornish, Toby ^a   Mizuma, Masamichi ^a   Rudek, Michelle A ^a   Zhao, Ming ^a   Maitra, Amarnath ^b   Ray, Balmiki ^c   Lahiri, Debomoy ^c   Maitra, Anirban ^a   Anders, Robert A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VISVA BHARATI UNIVERSITY   (India)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

carbon tetrachloride; cirrhosis; curcumin; cytokines; liver fibrosis; myofibroblasts; NanoCurct; polymeric nanoparticle

Indexed keywords

CARBON TETRACHLORIDE; CURCUMIN; CYTOKINE; NANCURC; NANOPARTICLE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG BIOAVAILABILITY; DRUG FORMULATION; IN VITRO STUDY; LIVER CELL; LIVER FIBROSIS; LIVER INJURY; MALE; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; RAT; SINGLE DRUG DOSE; STELLATE CELL;

ANIMALS; BIOLOGICAL AVAILABILITY; CARBON TETRACHLORIDE POISONING; CELL LINE, TRANSFORMED; CURCUMIN; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; NANOPARTICLES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 80052279738     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.86     Document Type: Article

References (68)

1. Brenner DA. Molecular pathogenesis of liver fibrosis. Trans Am Clin Climatol Assoc 2009;120:361-368.
2. Hellerbrand C, Stefanovic B, Giordano F, et al. The role of TGFbeta1 in initiating hepatic stellate cell activation in vivo. J Hepatol 1999;30: 77-87. (Pubitemid 29023655)
3. Sinha R, Anderson DE, McDonald SS, et al. Cancer risk and diet in India. J Postgrad Med 2003;49:222-228. (Pubitemid 37493414)
4. Huang MT, Smart RC, Wong CQ, et al. Inhibitory effect of curcumin, chlorogenic acid, caffeic acid, and ferulic acid on tumor promotion in mouse skin by 12-O-tetradecanoylphorbol-13-acetate. Cancer Res 1988;48:5941-5946. (Pubitemid 18266780)
5. Sharma OP. Antioxidant activity of curcumin and related compounds. Biochem Pharmacol 1976;25:1811-1812.
6. Rao TS, Basu N, Siddiqui HH. Anti-inflammatory activity of curcumin analogues. Indian J Med Res 1982;75:574-578. (Pubitemid 13226183)
7. Brouet I, Ohshima H. Curcumin, an anti-tumour promoter and antiinflammatory agent, inhibits induction of nitric oxide synthase in activated macrophages. Biochem Biophys Res Commun 1995;206: 533-540.
8. Kulkarni SK, Bhutani MK, Bishnoi M. Antidepressant activity of curcumin: involvement of serotonin and dopamine system. Psychopharmacology (Berl) 2008;201:435-442.
9. Xu Y, Ku BS, Yao HY, et al. The effects of curcumin on depressive-like behaviors in mice. Eur J Pharmacol 2005;518:40-46. (Pubitemid 40968146)
10. Fu Y, Zheng S, Lin J, et al. Curcumin protects the rat liver from CCl4-caused injury and fibrogenesis by attenuating oxidative stress and suppressing inflammation. Mol Pharmacol 2008;73:399-409 (Pubitemid 351159210)
11. Park EJ, Jeon CH, Ko G, et al. Protective effect of curcumin in rat liver injury induced by carbon tetrachloride. J Pharm Pharmacol 2000;52: 437-440. (Pubitemid 30223687)
12. Donatus IA, Sardjoko, Vermeulen NP. Cytotoxic and cytoprotective activities of curcumin. Effects on paracetamol-induced cytotoxicity, lipid peroxidation and glutathione depletion in rat hepatocytes. Biochem Pharmacol 1990;39:1869-1875. (Pubitemid 20187320)
13. Kiso Y, Suzuki Y, Watanabe N, et al. Antihepatotoxic principles of Curcuma longa rhizomes. Planta Med 1983;49:185-187. (Pubitemid 14220766)
14. Xu J, Fu Y, Chen A. Activation of peroxisome proliferator-activated receptor-gamma contributes to the inhibitory effects of curcumin on rat hepatic stellate cell growth. Am J Physiol Gastrointest Liver Physiol 2003;285:G20-G30. (Pubitemid 36736384)
15. Zheng S, Chen A. Activation of PPARgamma is required for curcumin to induce apoptosis and to inhibit the expression of extracellular matrix genes in hepatic stellate cells in vitro. Biochem J 2004; 384(Part 1):149-157. (Pubitemid 39564171)
16. Kidd PM. Bioavailability and activity of phytosome complexes from botanical polyphenols: the silymarin, curcumin, green tea, and grape seed extracts. Altern Med Rev 2009;14:226-246.
17. Marczylo TH, Verschoyle RD, Cooke DN, et al. Comparison of systemic availability of curcumin with that of curcumin formulated with phosphatidylcholine. Cancer Chemother Pharmacol 2007;60:171-177. (Pubitemid 46742531)
18. Pan MH, Huang TM, Lin JK. Biotransformation of curcumin through reduction and glucuronidation in mice. Drug Metab Dispos 1999;27: 486-494.
19. Sharma RA, Steward WP, Gescher AJ. Pharmacokinetics and pharmacodynamics of curcumin. Adv Exp Med Biol 2007;595:453-470.
20. Anand P, Kunnumakkara AB, Newman RA, et al. Bioavailability of curcumin: problems and promises. Mol Pharm 2007;4:807-818.
21. Garcea G, Berry DP, Jones DJ, et al. Consumption of the putative chemopreventive agent curcumin by cancer patients: assessment of curcumin levels in the colorectum and their pharmacodynamic consequences. Cancer Epidemiol Biomarkers Prev 2005;14:120-125. (Pubitemid 40165291)
22. Bisht S, Mizuma M, Feldmann G, et al. Systemic administration of polymeric nanoparticle-encapsulated curcumin (NanoCurc) blocks tumor growth and metastases in preclinical models of pancreatic cancer. Mol Cancer Ther 2010;9:2255-2264.
23. Garcea G, Jones DJ, Singh R, et al. Detection of curcumin and its metabolites in hepatic tissue and portal blood of patients following oral administration. Br J Cancer 2004;90:1011-1015. (Pubitemid 38499692)
24. Dhillon N, Aggarwal BB, Newman RA, et al. Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin Cancer Res 2008;14: 4491-4499.
25. Bisht S, Feldmann G, Koorstra JB, et al. In vivo characterization of a polymeric nanoparticle platform with potential oral drug delivery capabilities. Mol Cancer Ther 2008;7:3878-3888.
26. Bisht S, Feldmann G, Soni S, et al. Polymeric nanoparticle-encapsulated curcumin ('nanocurcumin'): a novel strategy for human cancer therapy. J Nanobiotechnology 2007;5:3.
27. Anders RA, Subudhi SK, Wang J, et al. Contribution of the lymphotoxin beta receptor to liver regeneration. J Immunol 2005;175:1295-1300. (Pubitemid 41095019)
28. Vogel S, Piantedosi R, Frank J, et al. An immortalized rat liver stellate cell line (HSC-T6): a new cell model for the study of retinoid metabolism in vitro. J Lipid Res 2000;41:882-893. (Pubitemid 30434319)
29. Aggarwal BB, Sundaram C, Malani N, et al. Curcumin: the Indian solid gold. Adv Exp Med Biol 2007;595:1-75.
30. Bisht S, Maitra A. Systemic delivery of curcumin: 21st century solutions for an ancient conundrum. Curr Drug Discov Technol 2009;6:192-199.
31. Sudo K, Yamada Y, Moriwaki H, et al. Lack of tumor necrosis factor receptor type 1 inhibits liver fibrosis induced by carbon tetrachloride in mice. Cytokine 2005;29:236-244. (Pubitemid 40326610)
32. Adams DH, Ju C, Ramaiah SK, et al. Mechanisms of immune-mediated liver injury. Toxicol Sci 2010;115:307-321.
33. Li Z, Diehl AM. Innate immunity in the liver. Curr Opin Gastroenterol 2003;19:565-571. (Pubitemid 37330476)
34. Szabo G, Mandrekar P, Dolganiuc A. Innate immune response and hepatic inflammation. Semin Liver Dis 2007;27:339-350. (Pubitemid 350071835)
35. Marra F, Aleffi S, Galastri S, et al. Mononuclear cells in liver fibrosis. Semin Immunopathol 2009;31:345-358.
36. Ginsburg I, Koren E, Horani A, et al. Amelioration of hepatic fibrosis via Padma Hepaten is associated with altered natural killer T lymphocytes. Clin Exp Immunol 2009;157:155-164.
37. Ishikawa S, Ikejima K, Yamagata H, et al. CD1d-restricted natural killer T cells contribute to hepatic inflammation and fibrogenesis in mice. J Hepatol 2010.
38. Park O, Jeong WI, Wang L, et al. Diverse roles of invariant natural killer T cells in liver injury and fibrosis induced by carbon tetrachloride. Hepatology 2009;49:1683-1694.
39. Safadi R, Zigmond E, Pappo O, et al. Amelioration of hepatic fibrosis via beta-glucosylceramide-mediated immune modulation is associated with altered CD8 and NKT lymphocyte distribution. Int Immunol 2007;19:1021-1029. (Pubitemid 47386927)
40. Melhem A, Muhanna N, Bishara A, et al. Anti-fibrotic activity of NK cells in experimental liver injury through killing of activated HSC. J Hepatol 2006;45:60-71. (Pubitemid 43850614)
41. Radaeva S, Sun R, Jaruga B, et al. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosis-inducing ligand-dependent manners. Gastroenterology 2006;130:435-452. (Pubitemid 43202042)
42. Daley JM, Thomay AA, Connolly MD, et al. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukocyte Biol 2008;83:64-70.
43. Karlmark KR, Weiskirchen R, Zimmermann HW, et al. Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 2009;50:261-274.
44. Weiler-Normann C, Herkel J, Lohse AW. Mouse models of liver fibrosis. Z Gastroenterol 2007;45:43-50. (Pubitemid 46202720)
45. Burk RF, Lane JM, Patel K. Relationship of oxygen and glutathione in protection against carbon tetrachloride-induced hepatic microsomal lipid peroxidation and covalent binding in the rat. Rationale for the use of hyperbaric oxygen to treat carbon tetrachloride ingestion. J Clin Invest 1984;74:1996-2001. (Pubitemid 15197341)
46. Burk RF, Patel K, Lane JM. Reduced glutathione protection against rat liver microsomal injury by carbon tetrachloride. Dependence on O2. Biochem J 1983;215:441-445. (Pubitemid 14238655)
47. Zheng S, Yumei F, Chen A. De novo synthesis of glutathione is a prerequisite for curcumin to inhibit hepatic stellate cell (HSC) activation. Free Radic Biol Med 2007;43:444-453. (Pubitemid 46977625)
48. Friedman SL. Molecular mechanisms of hepatic fibrosis and principles of therapy. J Gastroenterol 1997;32:424-430. (Pubitemid 27254815)
49. Friedman SL, Roll FJ, Boyles J, et al. Hepatic lipocytes: the principal collagen-producing cells of normal rat liver. Proc Natl Acad Sci USA 1985;82:8681-8685. (Pubitemid 16101107)
50. Kawase T, Shiratori Y, Sugimoto T. Collagen production by rat liver fat-storing cells in primary culture. Exp Cell Biol 1986;54:183-192. (Pubitemid 16030568)
51. Ramadori G, Knittel T, Odenthal M, et al. Synthesis of cellular fibronectin by rat liver fat-storing (Ito) cells: regulation by cytokines. Gastroenterology 1992;103:1313-1321.
52. Neubauer K, Knittel T, Armbrust T, et al. Accumulation and cellular localization of fibrinogen/fibrin during short-term and long-term rat liver injury. Gastroenterology 1995;108:1124-1135.
53. Garcia-Trevijano ER, Iraburu MJ, Fontana L, et al. Transforming growth factor beta1 induces the expression of alpha1(I) procollagen mRNA by a hydrogen peroxide-C/EBPbeta-dependent mechanism in rat hepatic stellate cells. Hepatology 1999;29:960-970. (Pubitemid 29109616)
54. Gressner AM. Transdifferentiation of hepatic stellate cells (Ito cells) to myofibroblasts: a key event in hepatic fibrogenesis. Kidney Int Suppl 1996;54:S39-S45. (Pubitemid 26155479)
55. Galli A, Crabb D, Price D, et al. Peroxisome proliferator-activated receptor gamma transcriptional regulation is involved in plateletderived growth factor-induced proliferation of human hepatic stellate cells. Hepatology 2000;31:101-108. (Pubitemid 30033695)
56. Marra F, Efsen E, Romanelli RG, et al. Ligands of peroxisome proliferator-activated receptor gamma modulate profibrogenic and proinflammatory actions in hepatic stellate cells. Gastroenterology 2000;119:466-478. (Pubitemid 30621997)
57. Miyahara T, Schrum L, Rippe R, et al. Peroxisome proliferator-activated receptors and hepatic stellate cell activation. J Biol Chem 2000;275: 35715-35722.
58. Lin J, Zheng S, Chen A. Curcumin attenuates the effects of insulin on stimulating hepatic stellate cell activation by interrupting insulin signaling and attenuating oxidative stress. Lab Invest 2009;89: 1397-1409.
59. Jiao J, Friedman SL, Aloman C. Hepatic fibrosis. Curr Opin Gastroenterol 2009;25:223-229.
60. Everhart J. The Burden of Digestive Diseases in the United States, Vol. No. 09-6443 US Government: Washington, DC, 2008.
61. van Vlerken LE, Amiji MM. Multi-functional polymeric nanoparticles for tumour-targeted drug delivery. Expert Opin Drug Deliv 2006;3:205-216. (Pubitemid 43338092)
62. Vicent MJ, Duncan R. Polymer conjugates: nanosized medicines for treating cancer. Trends Biotechnol 2006;24:39-47. (Pubitemid 43017749)
63. Vasir JK, Labhasetwar V. Targeted drug delivery in cancer therapy. Technol Cancer Res Treat 2005;4:363-374. (Pubitemid 41242611)
64. Ganta S, Devalapally H, Amiji M. Curcumin enhances oral bioavailability and anti-tumor therapeutic efficacy of paclitaxel upon administration in nanoemulsion formulation. J Pharm Sci 2010;99:4630-4641.
65. Appiah-Opong R, de Esch I, Commandeur JN, et al. Structureactivity relationships for the inhibition of recombinant human cytochromes P450 by curcumin analogues. Eur J Med Chem 2008; 43:1621-1631.
66. Volak LP, Ghirmai S, Cashman JR, et al. Curcuminoids inhibit multiple human cytochromes P450, UDP-glucuronosyltransferase, and sulfotransferase enzymes, whereas piperine is a relatively selective CYP3A4 inhibitor. Drug Metab Dispos 2008;36: 1594-1605.
67. Lin J, Chen A. Activation of peroxisome proliferator-activated receptorgamma by curcumin blocks the signaling pathways for PDGF and EGF in hepatic stellate cells. Lab Invest 2008;88:529-540. (Pubitemid 351581455)
68. Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury: Present concepts. J Gastroenterol Hepatol 2011; 26(Suppl 1):173-179.