Citrus limon-derived nanovesicles inhibit cancer cell proliferation and suppress CML xenograft growth by inducing TRAIL-mediated cell death

Oncotarget

Volumn 6, Issue 23, 2015, Pages 19514-19527

  Raimondo, Stefania ^a   Naselli, Flores ^a   Fontana, Simona ^a   Monteleone, Francesca ^a   Lo Dico, Alessia ^a   Saieva, Laura ^a   Zito, Giovanni ^b   Flugy, Anna ^a   Manno, Mauro ^c   Di Bella, Maria Antonietta ^a   De Leo, Giacomo ^a   Alessandro, Riccardo ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^c CNR   (Italy)

Author keywords

Cancer; Citrus limon L.; Exosome like nanovesicles; TRAIL mediated cell death

Indexed keywords

ANTINEOPLASTIC AGENT; NANOVESICLE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; NANOPARTICLE; PLANT EXTRACT; PLANT PROTEIN; TNFSF10 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL PROLIFERATION; CELL VIABILITY; CHRONIC MYELOID LEUKEMIA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG DISTRIBUTION; DRUG ISOLATION; DRUG MECHANISM; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; LEMON JUICE; MALE; MOUSE; NONHUMAN; TUMOR XENOGRAFT; ULTRACENTRIFUGATION; ANIMAL; CELL SURVIVAL; CHEMISTRY; CITRUS; DRUG EFFECTS; DRUG SCREENING; EXOSOME; FRUIT AND VEGETABLE JUICE; ISOLATION AND PURIFICATION; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MEDICINAL PLANT; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYTOTHERAPY; PROCEDURES; PROTEOMICS; SCID MOUSE; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR CELL LINE; TUMOR VOLUME; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CITRUS; EXOSOMES; FRUIT AND VEGETABLE JUICES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MALE; MICE, INBRED NOD; MICE, SCID; NANOPARTICLES; PHYTOTHERAPY; PLANT EXTRACTS; PLANT PROTEINS; PLANTS, MEDICINAL; PROTEOMICS; SIGNAL TRANSDUCTION; TIME FACTORS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84939250467     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4004     Document Type: Article

References (32)

1. Corrado C, Raimondo S, Chiesi A, Ciccia F, De Leo G, Alessandro R. Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications. Int J Mol Sci. 2013; 14:5338-5366.
2. Lakkaraju A, Rodriguez-Boulan E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol. 2008; 18:199-209.
3. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, Garcia-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012; 18:883-891.
4. Saman S, Kim W, Raya M, Visnick Y, Miro S, Jackson B, McKee AC, Alvarez VE, Lee NC, Hall GF. Exosomeassociated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J Biol Chem. 2012; 287:3842-3849.
5. Lin J, Li J, Huang B, Liu J, Chen X, Chen XM, Xu YM, Huang LF, Wang XZ. Exosomes: Novel Biomarkers for Clinical Diagnosis. ScientificWorldJournal. 2015; 2015:657086.
6. Regente M, Corti-Monzon G, Maldonado AM, Pinedo M, Jorrin J, de la Canal L. Vesicular fractions of sunflower apoplastic fluids are associated with potential exosome marker proteins. FEBS Lett. 2009; 583:3363-3366.
7. Wang B, Zhuang X, Deng ZB, Jiang H, Mu J, Wang Q, Xiang X, Guo H, Zhang L, Dryden G, Yan J, Miller D, Zhang HG. Targeted drug delivery to intestinal macrophages by bioactive nanovesicles released from grapefruit. Mol Ther. 2014; 22:522-534.
8. Ju S, Mu J, Dokland T, Zhuang X, Wang Q, Jiang H, Xiang X, Deng ZB, Wang B, Zhang L, Roth M, Welti R, Mobley J, Jun Y, Miller D, Zhang HG. Grape exosome-like nanoparticles induce intestinal stem cells and protect mice from DSS-induced colitis. Mol Ther. 2013; 21:1345-1357.
9. Wang L, Wang J, Fang L, Zheng Z, Zhi D, Wang S, Li S, Ho CT, Zhao H. Anticancer activities of citrus peel polyme-thoxyflavones related to angiogenesis and others. Biomed Res Int. 2014; 2014:453972.
10. Manthey JA, Grohmann K, Guthrie N. Biological properties of citrus flavonoids pertaining to cancer and inflammation. Curr Med Chem. 2001; 8:135-153.
11. Benavente-Garcia O, Castillo J. Update on uses and properties of citrus flavonoids: new findings in anticancer, cardiovascular, and anti-inflammatory activity. J Agric Food Chem. 2008; 56:6185-6205.
12. Blagosklonny MV. Overcoming limitations of natural anti-cancer drugs by combining with artificial agents. Trends Pharmacol Sci. 2005; 26:77-81.
13. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer. 2008; 8:782-798.
14. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest. 1999; 104:155-162.
15. Nesterov A, Nikrad M, Johnson T, Kraft AS. Oncogenic Ras sensitizes normal human cells to tumor necrosis factor-alpha-related apoptosis-inducing ligand-induced apoptosis. Cancer Res. 2004; 64:3922-3927.
16. Falschlehner C, Emmerich CH, Gerlach B, Walczak H. TRAIL signalling: decisions between life and death. Int J Biochem Cell Biol. 2007; 39:1462-1475.
17. Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010; 73:1907-1920.
18. Ishibashi M, Ohtsuki T. Studies on search for bioactive natural products targeting TRAIL signaling leading to tumor cell apoptosis. Med Res Rev. 2008; 28:688-714.
19. Ouyang L, Luo Y, Tian M, Zhang SY, Lu R, Wang JH, Kasimu R, Li X. Plant natural products: from traditional compounds to new emerging drugs in cancer therapy. Cell Prolif. 2014; 47:506-515.
20. Alshatwi AA, Shafi G, Hasan TN, Al-Hazzani AA, Alsaif MA, Alfawaz MA, Lei KY, Munshi A. Apoptosis-mediated inhibition of human breast cancer cell proliferation by lemon citrus extract. Asian Pac J Cancer Prev. 2011; 12:1555-1559.
21. Luo G, Guan X, Zhou L. Apoptotic effect of citrus fruit extract nobiletin on lung cancer cell line A549 in vitro and in vivo. Cancer Biol Ther. 2008; 7:966-973.
22. Tse AK, Chow KY, Cao HH, Cheng CY, Kwan HY, Yu H, Zhu GY, Wu YC, Fong WF, Yu ZL. The herbal compound cryptotanshinone restores sensitivity in cancer cells that are resistant to the tumor necrosis factor-related apoptosis-inducing ligand. J Biol Chem. 2013; 288:29923-29933.
23. Beranova L, Pombinho AR, Spegarova J, Koc M, Klanova M, Molinsky J, Klener P, Bartunek P, Andera L. The plant alkaloid and anti-leukemia drug homoharringtonine sensitizes resistant human colorectal carcinoma cells to TRAIL-induced apoptosis via multiple mechanisms. Apoptosis. 2013; 18:739-750.
24. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem. 1996; 271:12687-12690.
25. Blagosklonny MV. Prospective strategies to enforce selectively cell death in cancer cells. Oncogene. 2004; 23:2967-2975.
26. Zhang Y, Zhang B. TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol Cancer Res. 2008; 6:1861-1871.
27. Corrado C, Raimondo S, Saieva L, Flugy AM, De Leo G, Alessandro R. Exosome-mediated crosstalk between chronic myelogenous leukemia cells and human bone marrow stromal cells triggers an interleukin 8-dependent survival of leukemia cells. Cancer Lett. 2014; 348:71-76.
28. Noto R, Santangelo MG, Ricagno S, Mangione MR, Levantino M, Pezzullo M, Martorana V, Cupane A, Bolognesi M, Manno M. The tempered polymerization of human neuroserpin. PLoS One. 2012; 7:e32444.
29. Raimondo S, Saieva L, Corrado C, Fontana S, Flugy A, Rizzo A, De Leo G, Alessandro R. Chronic myeloid leukemia-derived exosomes promote tumor growth through an autocrine mechanism. Cell Commun Signal. 2015; 13:8.
30. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem. 1996; 68:850-858.
31. Simpson RJ, Kalra H, Mathivanan S. ExoCarta as a resource for exosomal research. J Extracell Vesicles. 2012; 1.
32. Corrado C, Raimondo S, Flugy AM, Fontana S, Santoro A, Stassi G, Marfia A, Iovino F, Arlinghaus R, Kohn EC, Leo GD, Alessandro R. Carboxyamidotriazole inhibits cell growth of imatinib-resistant chronic myeloid leukaemia cells including T315I Bcr-Abl mutant by a redox-mediated mechanism. Cancer Lett. 2011; 300:205-214.