2,069
Views
14
CrossRef citations to date
0
Altmetric
Research Article

Curcumin-loaded nanoliposomes linked to homing peptides for integrin targeting and neuropilin-1-mediated internalization

, , , &
Pages 277-285 | Received 22 Jul 2015, Accepted 07 Nov 2016, Published online: 10 Dec 2016

References

  • Aggarwal BB, Harikumar KB. 2009. Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neurodegenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplastic diseases. Int J Biochem Cell Biol. 41:40–59.
  • Ahmad S, Ahmad A, Schneider BK, et al. 2006. Cholesterol interferes with the MTT assay in human epithelial-like (A549) and endothelial (HLMVE and HCAE) Cells. Int J Toxicol. 25:17–23.
  • Ak T, Gülçin I. 2008. Antioxidant and radical scavenging properties of curcumin. Chem Biol Interact. 174:27–37.
  • Anand P, Kunnumakkara AB, Newman RA, et al. 2007. Bioavailability of curcumin: Problems and promises. Mol Pharm. 4:807–818.
  • Anand P, Sundaram C, Jhurani S, et al. 2008. Curcumin and cancer: an “old-age” disease with an “age-old” solution. Cancer Lett. 267:133–164.
  • Androutsopoulos VP, Ruparelia K, Arroo RRJ, et al. 2009. CYP1-mediated antiproliferative activity of dietary flavonoids in MDA-MB-468 breast cancer cells. Toxicology. 264:162–170.
  • Andrushchenko VV, Vogel HJ, Prenner EJ. 2007. Optimization of the hydrochloric acid concentration used for trifluoroacetate removal from synthetic peptides. J Pept Sci. 13:37–43.
  • Angius F, Floris A. 2015. Liposomes and MTT cell viability assay: an incompatible affair. Toxicol in Vitro. 29:314–319.
  • Avraamides CJ, Garmy-Susini B, Varner JA. 2008. Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer. 8:604–617.
  • Banfi L, Basso A, Damonte G, et al. 2007. Synthesis and biological evaluation of new conformationally biased integrin ligands based on a tetrahydroazoninone scaffold. Bioorg. Med Chem Lett. 17:1341–1345.
  • Barry J, Fritz M, Brender JR, et al. 2009. Determining the effects of lipophilic drugs on membrane structure by solid-state NMR spectroscopy: the case of the antioxidant curcumin. J Am Chem Soc. 131:4490–4498.
  • Basu A, Kumar GS. 2014. Elucidating the energetics of the interaction of non-toxic dietary pigment curcumin with human serum albumin: a calorimetric study. J Chem Thermodyn. 70:176–181.
  • Baum L, Ng A. 2004. Curcumin interaction with copper and iron suggests one possible mechanism of action in Alzheimer's disease animal models. J Alzheimers Dis. 6:367–377.
  • Belvisi L, Bernardi A, Colombo M, et al. 2006. Targeting integrins: insights into structure and activity of cyclic RGD pentapeptide mimics containing azabicycloalkane amino acids. Bioorgan Med Chem. 14:169–180.
  • Bernabé-Pineda M, Ramı´rez-Silva MT, Romero-Romo M, et al. 2004. Determination of acidity constants of curcumin in aqueous solutions and apparent rate constant of its decomposition. Spectrochim Acta a. 60:1091–1097.
  • Bush JA, Cheung KJ Jr, Li G. 2001. Curcumin induces apoptosis in human melanoma cells through a Fas receptor/caspase-8 pathway independent of p53. Exp Cell Res. 271:305–314.
  • Chan KS, Koh CG, Li HY. 2012. Mitosis-targeted anti-cancer therapies: where they stand. Cell Death Dis. 3:e411
  • Chen B, Zhang Y, Wang Y, et al. 2014. Curcumin inhibits proliferation of breast cancer cells through Nrf2-mediated down-regulation of Fen1 expression. J Steroid Biochem. 143:11–18.
  • Chen QY, Lu GH, Wu YQ, et al. 2010. Curcumin induces mitochondria pathway mediated cell apoptosis in A549 lung adenocarcinoma cells. Oncol Rep. 23:1285–1292.
  • Choudhuri T, Pal S, Das T, et al. 2005. Curcumin selectively induces apoptosis in deregulated cyclin D1-expressed cells at G2 phase of cell cycle in a p53-dependent manner. J Biol Chem. 280:20059–20068.
  • Colombo G, Curnis F, De Mori GMS, et al. 2002. Structure-activity relationships of linear and cyclic peptides containing the NGR tumor-homing motif. J Biol Chem. 277:47891–47897.
  • Cos S, Sinchez-Barcelb EJ. 1995. Melatonin inhibition of MCF-7 human breast-cancer cells growth: Influence of cell proliferation rate. Cancer Lett. 93:207–212.
  • Creighton CJ, Du Y, Santulli RJ, et al. 2006. Synthesis and biological evaluation of type VI beta-turn templated RGD peptidomimetics . Bioorg Med Chem Lett. 16:3971–3974.
  • Curnis F, Longhi R, Crippa L, et al. 2006. Spontaneous formation of l-isoaspartate and gain of function in fibronectin. J Biol Chem. 281:36466–36476.
  • Egan ME, Pearson M, Weiner SA, et al. 2004. Curcumin, a major constituent of turmeric, corrects cystic fibrosis defects. Science. 304:600–602.
  • El-Sayed A, Futaki S, Harashima H. 2009. Delivery of macromolecules using arginine-rich cell-penetrating peptides: Ways to overcome endosomal entrapment. AAPS J. 11:13–22.
  • El-Sayed MEH, Hoffman AS, Stayton PS. 2005. Rational design of composition and activity correlations for pH-sensitive and glutathione-reactive polymer therapeutics. J Control Release. 101:47–58.
  • Gandhy SU, Kim KH, Larsen L, et al. 2012. Curcumin and synthetic analogs induce reactive oxygen species and decreases specificity protein (Sp) transcription factors by targeting microRNAs. BMC Cancer. 12:564.
  • Gentilucci L, Cardillo G, Squassabia F, et al. 2007. Inhibition of cancer cell adhesion by heterochiral Pro-containing RGD mimetics. Bioorg Med Chem Lett. 17:2329–2333.
  • Gubernator J. 2011. Active methods of drug loading into liposomes: Recent strategies for stable drug entrapment and increased in vivo activity. Expert Opin Drug Deliv. 8:565–580.
  • Haspel N, Zanuy D, Nussinov R, et al. 2011. Binding of a C-end rule peptide to the neuropilin-1 receptor: a molecular modeling approach. Biochemistry. 50:1755–1762.
  • Henrotin Y, Gharbi M, Dierckxsens Y, et al. 2014. Decrease of a specific biomarker of collagen degradation in osteoarthritis, Coll2-1, by treatment with highly bioavailable curcumin during an exploratory clinical trial. BMC Complement Altern Med. 14:159
  • Holliday DL, Speirs V. 2011. Choosing the right cell line for breast cancer research. Breast Cancer Res. 13:215
  • Huang HW. 2009. Free energies of molecular bound states in lipid bilayers: Lethal concentrations of antimicrobial peptides. Biophys J. 96:3263–3272.
  • Hung WC, Chen FY, Lee CC, et al. 2008. Membrane-thinning effect of curcumin. Biophys J. 94:4331–4338.
  • Jiang M, Huang O, Zhang X, et al. 2013. Curcumin induces cell death and restores Tamoxifen sensitivity in the antiestrogen-resistant breast cancer cell lines MCF-7/LCC2 and MCF-7/LCC9. Molecules. 18:701–720.
  • Kang N, Wang MM, Wang YH, et al. 2014. Tetrahydrocurcumin induces G2/M cell cycle arrest and apoptosis involving p38 MAPK activation in human breast cancer cells. Food Chem Toxicol. 67:193–200.
  • Karewicz A, Bielska D, Gzyl-Malcher B, et al. 2011. Interaction of curcumin with lipid monolayers and liposomal bilayers. Colloids Surf B Biointerfaces. 88:231–239.
  • Khanna D, Sethi G, Seok Ahn K, et al. 2007. Natural products as a gold mine for arthritis treatment. Curr Opin Pharmacol. 7:344–351.
  • Kichler A, Leborgne C, März J, et al. 2003. Histidine-rich amphipathic peptide antibiotics promote efficient delivery of DNA into mammalian cells. Proc Natl Acad Sci USA. 100:1564–1568.
  • Kumar SSD, Mahesh A, Mahadevan S, et al. 2014. Synthesis and characterization of curcumin loaded polymer/lipid based nanoparticles and evaluation of their antitumor effects on MCF-7 cells. Biochim Biophys Acta. 1840:1913–1922.
  • Kunwar A, Barik A, Pandey R, et al. 2006. Transport of liposomal and albumin loaded curcumin to living cells: An absorption and fluorescence spectroscopic study. Biochim Biophys Acta. 1760:1513–1520.
  • Leung MHM, Colangelo H, Kee TW. 2008. Encapsulation of curcumin in cationic micelles suppresses alkaline hydrolysis. Langmuir. 24:5672–5675.
  • Li HL, Liu C, de Couto G, et al. 2008. Curcumin prevents and reverses murine cardiac hypertrophy. J Clin Invest. 118:879–893.
  • Li Q, Chen J, Luo S, et al. 2015. Synthesis and assessment of the antioxidant and antitumor properties of asymmetric curcumin analogues. Eur J Med Chem. 93:461–469.
  • Li Y, Zheng X, Sun Y, et al. 2014. RGD-fatty alcohol-modified docetaxel liposomes improve tumor selectivity in-vivo. Int J Pharm. 468:133–141.
  • Lin L, Hutzen B, Ball S, et al. 2009. New curcumin analogues exhibit enhanced growth-suppressive activity and inhibit AKT and signal transducer and activator of transcription 3 phosphorylation in breast and prostate cancer cells. Cancer Sci. 100:1719–1727.
  • Loyer P, Bedhouche W, Wei Huang Z, et al. 2013. Degradable and biocompatible nanoparticles decorated with cyclic RGD peptide for efficient drug delivery to hepatoma cells in vitro. Int J Pharm. 454:727–737.
  • Marchand-Brynaert J, Detrait E, Noiset O, et al. 1999. Biological evaluation of RGD peptidomimetics, designed for the covalent derivatization of cell culture substrata, as potential promotors of cellular adhesion. Biomaterials. 20:1773–1782.
  • Marchini M, Mingozzi M, Colombo R, et al. 2012. Cyclic RGD peptidomimetics containing bifunctional diketopiperazine scaffolds as new potent integrin ligands. Chemistry. 18:6195–6207.
  • McNally SJ, Harrison EM, Ross JA, et al. 2007. Curcumin induces hemeoxygenase 1 through generation of reactive oxygen species, p38 activation and phosphatase inhibition. Int J Mol Med. 19:165–172.
  • Mehta K, Pantazis P, McQueen T, et al. 1997. Antiproliferative effect of curcumin (diferuloylmethane) against human breast tumor cell lines. Anticancer Drugs. 8:470–481.
  • Midoux P, Pichon C, Yaouanc JJ, et al. 2009. Chemical vectors for gene delivery: a current review on polymers, peptides and lipids containing histidine or imidazole as nucleic acids carriers. Br J Pharmacol. 157:166–178.
  • Mohankumar K, Pajaniradje S, Sridharan S, et al. 2014. Mechanism of apoptotic induction in human breast cancer cell, MCF-7, by an analog of curcumin in comparison with curcumin-an in vitro and in silico approach. Chem Biol Interact. 210:51–63.
  • Muller A, Schumann F, Koksch M, et al. 1997. Synthesis of cyclic RGD-peptides containing G-amino acids. Lett Pept Sci. 4:275–281.
  • Naik S, Patel D, Chuttani K, et al. 2012. In-vitro mechanistic study of cell death and in-vivo performance evaluation of RGD grafted PEGylated docetaxel liposomes in breast cancer. Nanomed Nanotechnol. 8:951–962.
  • Nava G, Piñón E, Mendoza L, et al. 2011. Formulation and in vitro, ex vivo and in vivo evaluation of elastic liposomes for transdermal delivery of ketorolac tromethamine. Pharmaceutics. 3:954–970.
  • Ogunsola OA, Kraeling ME, Zhong S, et al. 2012. Structural analysis of ‘‘flexible’’ liposome formulations: new insights into the skin-penetrating ability of soft nanostructures. Commun Soft Matter. 8:10226.
  • Palange AL, Di Mascolo D, Singh J, et al. 2012. Modulating the vascular behavior of metastatic breast cancer cells by curcumin treatment. Front Oncol. 2: (art 161), doi: 10.3389/fonc.2012.00161.
  • Particle sciences, drug development services; technical brief, 2012, Vol. 2. An overview of the zeta potential, [cited 2016 Jan 21]. Available from: http://www.particlesciences.com/news/technical-briefs/2012/overview-of-zeta-potential.html.
  • Patel PR, Conrad Kiser R, Lu YY, et al. 2012. Synthesis and cell adhesive properties of linear and cyclic RGD functionalized polynorbornene thin films. Biomacromolecules. 13:2546–2553.
  • Patel R, Singh SK, Singh S, et al. 2009. Development and characterization of curcumin loaded transfersome for transdermal delivery. J Pharm Sci Res. 1:71–80.
  • Patil YP, Jadhav S. 2014. Novel methods for liposome preparation. Chem Phys Lipids. 177:8–18.
  • Prasada CP, Ratha G, Mathurc S, et al. 2009. Potent growth suppressive activity of curcumin in human breast cancer cells: Modulation of Wnt/beta-catenin signaling. Chem Biol Interact. 181:263–271.
  • Qin H, Liu J, Zhang Z, et al. 2014. In situ electrochemical assessment of cytotoxicity of chlorophenols in MCF-7 and HeLa cells. Anal Biochem. 462:60–66.
  • Ramachandran C, Rodriguez S, Ramachandran R, et al. 2005. Expression profiles of apoptotic genes induced by curcumin in human breast cancer and mammary epithelial cell lines. Anticancer Res. 25:3293–3302.
  • Ramachandran C, You W. 1999. Differential sensitivity of human mammary epithelial and breast carcinoma cell lines to curcumin. Breast Cancer Res Treat. 54:269–278.
  • Ranjan AP, Mukerjee A, Helson L, et al. 2013. Efficacy of liposomal curcumin in a human pancreatic tumor xenograft model: inhibition of tumor growth and angiogenesis. Anticancer Res. 33:3603–3610.
  • Ravindran J, Prasad S, Aggarwal BB. 2009. Curcumin and cancer cells: How many ways can curry kill tumor cells selectively?. AAPS J. 11:495–510.
  • Roxin A, Zheng G. 2012. Flexible or fixed: a comparative review of linear and cyclic cancer-targeting peptides. Future Med Chem. 4:1601–1618.
  • Ruoslahti E, Bhatia SN, Sailor MJ. 2010. Targeting of drugs and nanoparticles to tumors. J Cell Biol. 188:759–768.
  • Ruoslahti E, Teesalu T, Sugahara K. inventors. 2009. Burnham Institute for Medical Research, assignee. Methods and compositions related to peptides and proteins with C-terminal elements. United States patent US 20090226372 A1. Sep 10.
  • Sahebkar A, Chew GT, Watts GF. 2014. Recent advances in pharmacotherapy for hypertriglyceridemia. Prog Lipid Res. 56:47–66.
  • Sanmukhani J, Satodia V, Trivedi J, et al. 2014. Efficacy and safety of curcumin in major depressive disorder: a randomized controlled trial. Phytother Res. 28:579–585.
  • Santo RD, Costi R, Artico M, et al. 2003. HIV-1 integrase inhibitors that block HIV-1 replication in infected cells. Planning synthetic derivatives from natural products. Pure Appl Chem. 75:195–206.
  • Sharma PK, Varadan VV, Varadan VK. 2002. Effect of Tween-80 on the control of particle size and shrinkage properties of nanoscale α-alumina synthesized by sol-gel processing. J Am Ceram Soc. 85:2584–2586.
  • Stephenson JM, Banerjee S, Saxena NK, et al. 2002. Neuropilin-1 is differentially expressed in myoepithelial cells and vascular smooth muscle cells in preneoplastic and neoplastic human breast: a possible marker for the progression of breast cancer. Int J Cancer. 101:409–414.
  • Sun SH, Huang HC, Huang C, et al. 2012. Cycle arrest and apoptosis in MDA-MB-231/Her2 cells induced by curcumin. Eur J Pharmacol. 690:22–30.
  • Sutherland RL, Hall RE, Taylor IW. 1983. Cell proliferation kinetics of MCF-7 human mammary carcinoma cells in culture and effects of tamoxifen on exponentially growing and plateau-phase cells. Cancer Res. 43:3998–4006.
  • Taylor RA, Leonard MC. 2011. Curcumin for inflammatory bowel disease: a review of human studies. Altern Med Rev. 16:152–156.
  • Teesalu T, Sugahara KN, Ramana Kotamraju V, et al. 2009. C-End rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci USA. 106:16157–16162.
  • Thompson EW, Paik S, Brünner N, et al. 1992. Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines. J Cell Physiol. 150:534–544.
  • Thulasiraman P, McAndrews DJ, Mohiudddin IQ. 2014. Curcumin restores sensitivity to retinoic acid in triple negative breast cancer cells. BMC Cancer. 14:724
  • Tong D, Czerwenka K, Sedlak J, et al. 1999. Association of in-vitro invasiveness and gene expression of estrogen receptor, progesterone receptor, pS2 and plasminogen activator inhibitor-1 in human breast cancer cell lines. Breast Cancer Res Tr. 56:91–97.
  • Tønnesen HH. 2006. Solubility and stability of curcumin in solutions containing alginate and other viscosity modifying macromolecules. Studies of curcumin and curcuminoids. XXX. Pharmazie. 61:696–700.
  • Tu YF, Kaipparettu BA, Ma Y, et al. 2011. Mitochondria of highly metastatic breast cancer cell line MDA-MB-231 exhibits increased autophagic properties. Biochim Biophys Acta. 1807:1125–1132.
  • Updike MS, Davis ME, Wang LS, et al. 2005. Decreased MCF-7 breast cancer cell proliferation by serum from a selected line of beef cattle. Anticancer Res. 25:871–874.
  • Vander Kooi CW, Jusino MA, Perman B, et al. 2007. Structural basis for ligand and heparin binding to neuropilin B domains. Proc Natl Acad Sci USA. 104:6152–6157.
  • Varkouhi AK, Scholte M, Storm G, et al. 2010. Endosomal escape pathways for delivery of biologicals. J Control Release. 151:220–228.
  • von Wronski MA, Raju N, Pillai R, et al. 2006. Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor. J Biol Chem. 281:5702–5710.
  • Voss MJ, Möller MF, Powe DG, et al. 2011. Luminal and basal-like breast cancer cells show increased migration induced by hypoxia, mediated by an autocrine mechanism. BMC Cancer. 11:158.
  • Wang F, Chen L, Zhang R, et al. 2014. RGD peptide conjugated liposomal drug delivery system for enhance therapeutic efficacy in treating bone metastasis from prostate cancer. J Control Release. 196:222–233.
  • Wang YJ, Pan MH, Cheng AL, et al. 1997. Stability of curcumin in buffer solutions and characterization of its degradation products. J Pharm Biomed Anal. 15:1867–1876.
  • Watanabe N, Okochi E, Mochizuki M, et al. 2001. The presence of single nucleotide instability in human breast cancer cell lines. Cancer Res. 61:7739–7742.
  • Xiong XB, Huang Y, Lu WL, et al. 2005. Enhanced intracellular delivery and improved antitumor efficacy of doxorubicin by sterically stabilized liposomes modified with a synthetic RGD mimetic. J Control Release. 107:262–275.
  • Yadav B, Taurin S, Rosengren RJ, et al. 2010. Synthesis and cytotoxic potential of heterocyclic cyclohexanone analogues of curcumin. Bioorg Med Chem. 18:6701–6707.
  • Zaidi D, Singh N, Zareen Ahmad I, et al. 2011. Antiproliferative effects of curcumin plus centchroman in MCF-7 and MDA-MB-231 cells. Int J Pharm Pharm Sci. 3:212–216.
  • Zhang DW, Fu M, Gao SH, et al. 2013. Curcumin and diabetes: a systematic review. Evid Based Complement Alternat Med. doi: 10.1155/2013/636053.
  • Zhou H, Yang Q, Wang X. 2014. Spectrometric study on the binding of curcumin with AOT: effect of micelle-to-vesicle transition. Food Chem. 161:136–141.