Curcumin modulates pancreatic adenocarcinoma cell-derived exosomal function

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Osterman, Carlos J Diaz ^a   Lynch, James C ^a   Leaf, Patrick ^a   Gonda, Amber ^a   Bennit, Heather R Ferguson ^a   Griffiths, Duncan ^b   Wall, Nathan R ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Malvern Instruments Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CURCUMIN; ANTINEOPLASTIC AGENT;

ADENOCARCINOMA CELL LINE; ARTICLE; CELL FUNCTION; CELL ISOLATION; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; EXOSOME; HUMAN; HUMAN CELL; IN VITRO STUDY; MIA PACA 2 CELL LINE; PANC 1 CELL LINE; PANCREAS ADENOCARCINOMA; PANCREATIC CANCER CELL LINE; CARCINOMA, PANCREATIC DUCTAL; CELL SHAPE; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; METABOLISM; PANCREATIC NEOPLASMS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL SHAPE; CELL SURVIVAL; CURCUMIN; DRUG SCREENING ASSAYS, ANTITUMOR; EXOSOMES; HUMANS; PANCREATIC NEOPLASMS;

EID: 84941338355     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132845     Document Type: Article

References (60)

1. American Cancer Society. Cancer Facts & Figures 2013. Atlanta: American Cancer Society; 2013.
2. American Cancer Society. Cancer Facts & Figures 2015. Atlanta: American Cancer Society; 2015.
3. Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. The New England journal of medicine. 2014; 371(22):2140-1.
4. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians. 2014; 64 (1):9-29.
5. Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA. The pancreas cancer microenvironment. Clinical cancer research: an official journal of the American Association for Cancer Research. 2012; 18(16):4266-76.
6. Taylor DD, Lyons KS, Gercel-Taylor C. Shed membrane fragment-Associated markers for endometrial and ovarian cancers. Gynecologic oncology. 2002; 84(3):443-8. PMID: 11855885
7. Taylor DD, Black PH. Shedding of plasma membrane fragments. Neoplastic and developmental importance. Developmental biology (New York, NY: 1985). 1986; 3:33-57.
8. Atay S, Godwin AK. Tumor-derived exosomes: A message delivery system for tumor progression. Communicative & integrative biology. 2014; 7(1):e28231.
9. Kharaziha P, Ceder S, Li Q, Panaretakis T. Tumor cell-derived exosomes: a message in a bottle. Biochimica et biophysica acta. 2012; 1826(1):103-11. doi: 10.1016/j.bbcan.2012.03.006 PMID: 22503823
10. Gupta SC, Sung B, Kim JH, Prasad S, Li S, Aggarwal BB. Multitargeting by turmeric, the golden spice: From kitchen to clinic. Molecular nutrition & food research. 2013; 57(9):1510-28.
11. Ferrucci LM, Daniel CR, Kapur K, Chadha P, Shetty H, Graubard BI, et al. Measurement of spices and seasonings in India: opportunities for cancer epidemiology and prevention. Asian Pacific journal of cancer prevention: APJCP. 2010; 11(6):1621-9. PMID: 21338207
12. Shehzad A, Lee J, Lee YS. Curcumin in various cancers. BioFactors (Oxford, England). 2013; 39 (1):56-68.
13. Li L, Aggarwal BB, Shishodia S, Abbruzzese J, Kurzrock R. Nuclear factor-kappaB and IkappaB kinase are constitutively active in human pancreatic cells, and their down-regulation by curcumin (diferuloylmethane) is associated with the suppression of proliferation and the induction of apoptosis. Cancer. 2004; 101(10):2351-62. PMID: 15476283
14. Lin YG, Kunnumakkara AB, Nair A, Merritt WM, Han LY, Armaiz-Pena GN, et al. Curcumin inhibits tumor growth and angiogenesis in ovarian carcinoma by targeting the nuclear factor-kappaB pathway. Clinical cancer research: an official journal of the American Association for Cancer Research. 2007; 13 (11):3423-30.
15. Glienke W, Maute L, Wicht J, Bergmann L. Curcumin inhibits constitutive STAT3 phosphorylation in human pancreatic cancer cell lines and downregulation of survivin/BIRC5 gene expression. Cancer investigation. 2010; 28(2):166-71. doi: 10.3109/07357900903287006 PMID: 20121547
16. Yang CL, Liu YY, Ma YG, Xue YX, Liu DG, Ren Y, et al. Curcumin blocks small cell lung cancer cells migration, invasion, angiogenesis, cell cycle and neoplasia through Janus kinase-STAT3 signalling pathway. PloS one. 2012; 7(5):e37960. doi: 10.1371/journal.pone.0037960 PMID: 22662257
17. Youns M, Fathy GM. Upregulation of extrinsic apoptotic pathway in curcumin-mediated antiproliferative effect on human pancreatic carcinogenesis. Journal of cellular biochemistry. 2013; 114(12):2654-65. doi: 10.1002/jcb.24612 PMID: 23794119
18. Jutooru I, Chadalapaka G, Lei P, Safe S. Inhibition of NFkappaB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein down-regulation. The Journal of biological chemistry. 2010; 285(33):25332-44. doi: 10.1074/jbc.M109.095240 PMID: 20538607
19. Lev-Ari S, Vexler A, Starr A, Ashkenazy-Voghera M, Greif J, Aderka D, et al. Curcumin augments gemcitabine cytotoxic effect on pancreatic adenocarcinoma cell lines. Cancer investigation. 2007; 25 (6):411-8. PMID: 17882652
20. Bimonte S, Barbieri A, Palma G, Luciano A, Rea D, Arra C. Curcumin inhibits tumor growth and angiogenesis in an orthotopic mouse model of human pancreatic cancer. BioMed research international. 2013; 2013:810423. doi: 10.1155/2013/810423 PMID: 24324975
21. Ramachandran C, Resek AP, Escalon E, Aviram A, Melnick SJ. Potentiation of gemcitabine by Turmeric Force in pancreatic cancer cell lines. Oncology reports. 2010; 23(6):1529-35. PMID: 20428806
22. Gupta SC, Patchva S, Aggarwal BB. Therapeutic roles of curcumin: lessons learned from clinical trials. The AAPS journal. 2013; 15(1):195-218. doi: 10.1208/s12248-012-9432-8 PMID: 23143785
23. Shehzad A, Wahid F, Lee YS. Curcumin in cancer chemoprevention: molecular targets, pharmacokinetics, bioavailability, and clinical trials. Archiv der Pharmazie. 2010; 343(9):489-99. doi: 10.1002/ardp.200900319 PMID: 20726007
24. Dhillon N, Aggarwal BB, Newman RA, Wolff RA, Kunnumakkara AB, Abbruzzese JL, et al. Phase II trial of curcumin in patients with advanced pancreatic cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2008; 14(14):4491-9.
25. Epelbaum R, Schaffer M, Vizel B, Badmaev V, Bar-Sela G. Curcumin and gemcitabine in patients with advanced pancreatic cancer. Nutrition and cancer. 2010; 62(8):1137-41. doi: 10.1080/01635581.2010. 513802 PMID: 21058202
26. Kanai M, Otsuka Y, Otsuka K, Sato M, Nishimura T, Mori Y, et al. A phase I study investigating the safety and pharmacokinetics of highly bioavailable curcumin (Theracurmin) in cancer patients. Cancer chemotherapy and pharmacology. 2013; 71(6):1521-30. doi: 10.1007/s00280-013-2151-8 PMID: 23543271
27. Kanai M, Yoshimura K, Asada M, Imaizumi A, Suzuki C, Matsumoto S, et al. A phase I/II study of gemcitabine-based chemotherapy plus curcumin for patients with gemcitabine-resistant pancreatic cancer. Cancer chemotherapy and pharmacology. 2011; 68(1):157-64. doi: 10.1007/s00280-010-1470-2 PMID: 20859741
28. Li L, Braiteh FS, Kurzrock R. Liposome-encapsulated curcumin: in vitro and in vivo effects on proliferation, apoptosis, signaling, and angiogenesis. Cancer. 2005; 104(6):1322-31. PMID: 16092118
29. Sahu A, Bora U, Kasoju N, Goswami P. Synthesis of novel biodegradable and self-Assembling methoxy poly(ethylene glycol)-palmitate nanocarrier for curcumin delivery to cancer cells. Acta biomaterialia. 2008; 4(6):1752-61. doi: 10.1016/j.actbio.2008.04.021 PMID: 18524701
30. Gupta V, Aseh A, Rios CN, Aggarwal BB, Mathur AB. Fabrication and characterization of silk fibroinderived curcumin nanoparticles for cancer therapy. International journal of nanomedicine. 2009; 4:115-22 PMID: 19516890
31. Shaikh J, Ankola DD, Beniwal V, Singh D, Kumar MN. Nanoparticle encapsulation improves oral bioavailability of curcumin by at least 9-fold when compared to curcumin administered with piperine as absorption enhancer. European journal of pharmaceutical sciences: official journal of the European Federation for Pharmaceutical Sciences. 2009; 37(3-4):223-30.
32. Sasaki H, Sunagawa Y, Takahashi K, Imaizumi A, Fukuda H, Hashimoto T, et al. Innovative preparation of curcumin for improved oral bioavailability. Biological & pharmaceutical bulletin. 2011; 34(5):660-5.
33. Yallapu MM, Ebeling MC, Khan S, Sundram V, Chauhan N, Gupta BK, et al. Novel curcumin-loaded magnetic nanoparticles for pancreatic cancer treatment. Molecular cancer therapeutics. 2013; 12 (8):1471-80. doi: 10.1158/1535-7163.MCT-12-1227 PMID: 23704793
34. Kanai M, Imaizumi A, Otsuka Y, Sasaki H, Hashiguchi M, Tsujiko K, et al. Dose-escalation and pharmacokinetic study of nanoparticle curcumin, a potential anticancer agent with improved bioavailability, in healthy human volunteers. Cancer chemotherapy and pharmacology. 2012; 69(1):65-70. doi: 10.1007/s00280-011-1673-1 PMID: 21603867
35. Shi HS, Gao X, Li D, Zhang QW, Wang YS, Zheng Y, et al. A systemic administration of liposomal curcumin inhibits radiation pneumonitis and sensitizes lung carcinoma to radiation. International journal of nanomedicine. 2012; 7:2601-11. doi: 10.2147/IJN.S31439 PMID: 22679371
36. Matabudul D, Pucaj K, Bolger G, Vcelar B, Majeed M, Helson L. Tissue distribution of (Lipocurc) liposomal curcumin and tetrahydrocurcumin following two-And eight-hour infusions in Beagle dogs. Anticancer research. 2012; 32(10):4359-64. PMID: 23060559
37. Ghalandarlaki N, Alizadeh AM. Nanotechnology-Applied curcumin for different diseases therapy. 2014; 2014:394264. doi: 10.1155/2014/394264 PMID: 24995293
38. Ranjan AP, Mukerjee A, Helson L, Gupta R, Vishwanatha JK. Efficacy of liposomal curcumin in a human pancreatic tumor xenograft model: inhibition of tumor growth and angiogenesis. Anticancer research. 2013; 33(9):3603-9. PMID: 24023285
39. Kanai M. Therapeutic applications of curcumin for patients with pancreatic cancer. World journal of gastroenterology: WJG. 2014; 20(28):9384-91. doi: 10.3748/wjg.v20.i28.9384 PMID: 25071333
40. Sun D, Zhuang X, Xiang X, Liu Y, Zhang S, Liu C, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Molecular therapy: the journal of the American Society of Gene Therapy. 2010; 18(9):1606-14.
41. Savina A, Furlan M, Vidal M, Colombo MI. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. The Journal of biological chemistry. 2003; 278(22):20083-90. PMID: 12639953
42. Rieu S, Geminard C, Rabesandratana H, Sainte-Marie J, Vidal M. Exosomes released during reticulocyte maturation bind to fibronectin via integrin alpha4beta1. European journal of biochemistry/FEBS. 2000; 267(2):583-90. PMID: 10632729
43. Lancaster GI, Febbraio MA. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. The Journal of biological chemistry. 2005; 280(24):23349-55. PMID: 15826944
44. Kunwar A, Barik A, Mishra B, Rathinasamy K, Pandey R, Priyadarsini KI. Quantitative cellular uptake, localization and cytotoxicity of curcumin in normal and tumor cells. Biochimica et biophysica acta. 2008; 1780(4):673-9. doi: 10.1016/j.bbagen.2007.11.016 PMID: 18178166
45. Kunwar A, Barik A, Pandey R, Priyadarsini KI. Transport of liposomal and albumin loaded curcumin to living cells: an absorption and fluorescence spectroscopic study. Biochimica et biophysica acta. 2006; 1760(10):1513-20. PMID: 16904830
46. Nardo L, Andreoni A, Masson M, Haukvik T, Tonnesen HH. Studies on curcumin and curcuminoids. XXXIX. Photophysical properties of bisdemethoxycurcumin. Journal of fluorescence. 2011; 21(2):627-35 doi: 10.1007/s10895-010-0750-x PMID: 20953820
47. Franzen CA, Simms PE, Van Huis AF, Foreman KE, Kuo PC, Gupta GN. Characterization of uptake and internalization of exosomes by bladder cancer cells. BioMed research international. 2014; 2014:619829. doi: 10.1155/2014/619829 PMID: 24575409
48. Christianson HC, Svensson KJ, van Kuppevelt TH, Li JP, Belting M. Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(43):17380-5. doi: 10. 1073/pnas.1304266110 PMID: 24101524
49. Atai NA, Balaj L, van Veen H, Breakefield XO, Jarzyna PA, Van Noorden CJ, et al. Heparin blocks transfer of extracellular vesicles between donor and recipient cells. Journal of neuro-oncology. 2013; 115(3):343-51. doi: 10.1007/s11060-013-1235-y PMID: 24002181
50. van der Meel R, Fens MH, Vader P, van Solinge WW, Eniola-Adefeso O, Schiffelers RM. Extracellular vesicles as drug delivery systems: lessons from the liposome field. Journal of controlled release: official journal of the Controlled Release Society. 2014; 195:72-85.
51. Khan S, Aspe JR, Asumen MG, Almaguel F, Odumosu O, Acevedo-Martinez S, et al. Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential. British journal of cancer. 2009; 100(7):1073-86. doi: 10.1038/sj.bjc.6604978 PMID: 19293795
52. Khan S, Jutzy JM, Aspe JR, McGregor DW, Neidigh JW, Wall NR. Survivin is released from cancer cells via exosomes. Apoptosis: an international journal on programmed cell death. 2011; 16(1):1-12.
53. Neoptolemos JP. Adjuvant treatment of pancreatic cancer. European Journal of Cancer. 2011; 47: S378-S80. doi: 10.1016/S0959-8049(11)70210-6 PMID: 21944022
54. Demory Beckler M, Higginbotham JN, Franklin JL, Ham AJ, Halvey PJ, Imasuen IE, et al. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Molecular & cellular proteomics: MCP. 2013; 12(2):343-55.
55. Martinez-Lorenzo MJ, Anel A, Alava MA, Pineiro A, Naval J, Lasierra P, et al. The human melanoma cell line MelJuSo secretes bioactive FasL and APO2L/TRAIL on the surface of microvesicles. Possible contribution to tumor counterattack. Experimental cell research. 2004; 295(2):315-29. PMID: 15093732
56. Rana S, Malinowska K, Zoller M. Exosomal tumor microRNA modulates premetastatic organ cells. Neoplasia (New York, NY). 2013; 15(3):281-95.
57. Jung T, Castellana D, Klingbeil P, Cuesta Hernandez I, Vitacolonna M, Orlicky DJ, et al. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia (New York, NY). 2009; 11 (10):1093-105.
58. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB. Bioavailability of curcumin: problems and promises. Molecular pharmaceutics. 2007; 4(6):807-18. PMID: 17999464
59. Kunnumakkara AB, Guha S, Krishnan S, Diagaradjane P, Gelovani J, Aggarwal BB. Curcumin potentiates antitumor activity of gemcitabine in an orthotopic model of pancreatic cancer through suppression of proliferation, angiogenesis, and inhibition of nuclear factor-kappaB-regulated gene products. Cancer research. 2007; 67(8):3853-61. PMID: 17440100
60. Diaz Osterman CJ, Gonda A, Stiff TR, Sigaran U, Asuncion Valenzuela MM, Ferguson Bennit HR, et al. Curcumin induces pancreatic adenocarcinoma cell death via reduction of the inhibitors of apoptosis. Pancreas, In Press. 2015.