Curcumin promotes exosomes/microvesicles secretion that attenuates lysosomal cholesterol traffic impairment

Molecular Nutrition and Food Research

Volumn 58, Issue 4, 2014, Pages 687-697

  Canfrán Duque, Alberto ^a   Pastor, Óscar ^a   Quintana Portillo, Rocío ^a   Lerma, Milagros ^a   de la Peña, Gema ^a   Martín Hidalgo, Antonia ^a,b   Fernández Hernando, Carlos ^c   Lasunción, Miguel A ^a,b   Busto, Rebeca ^a,b  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cationic amphiphilic drugs; Cholesterol; Curcumin; Exosomes; Intracellular lipid traffic; U18666A

Indexed keywords

3-BETA-(2-(DIETHYLAMINO)ETHOXY)ANDROST-5-EN-17-ONE; ANDROSTANE DERIVATIVE; CD63 ANTIGEN; CD63 PROTEIN, HUMAN; CHOLESTEROL; CURCUMIN; HYPOCHOLESTEROLEMIC AGENT; LOW DENSITY LIPOPROTEIN CHOLESTEROL;

DRUG EFFECTS; EXOSOME; HEPG2 CELL LINE; HUMAN; LYSOSOME; METABOLISM; MONOCYTE; SECRETION (PROCESS); TRANSPORT AT THE CELLULAR LEVEL;

ANDROSTENES; ANTICHOLESTEREMIC AGENTS; ANTIGENS, CD63; BIOLOGICAL TRANSPORT; CHOLESTEROL; CHOLESTEROL, LDL; CURCUMIN; EXOSOMES; HEP G2 CELLS; HUMANS; LYSOSOMES; MONOCYTES;

EID: 84897433771     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300350     Document Type: Article

References (59)

1. Goldstein, J. L., DeBose-Boyd, R. A., Brown, M. S, Protein sensors for membrane sterols. Cell 2006, 124, 35-46.
2. Ikonen, E., Mechanisms for cellular cholesterol transport: defects and human disease. Physiol. Rev. 2006, 86, 1237-1261.
3. Ikonen, E., Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell. Biol. 2008, 9, 125-138.
4. Maxfield, F. R., van Meer, G., Cholesterol, the central lipid of mammalian cells. Curr. Opin. Cell. Biol. 2010, 22, 422-429.
5. Liscum, L., Faust, J. R., The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. J. Biol. Chem. 1989, 264, 11796-11806.
6. Cenedella, R. J., Cholesterol synthesis inhibitor U18666A and the role of sterol metabolism and trafficking in numerous pathophysiological processes. Lipids 2009, 44, 477-487.
7. Lange, Y., Steck, T. L., Cholesterol homeostasis. Modulation by amphiphiles. J. Biol. Chem. 1994, 269, 29371-29374.
8. Suarez, Y., Fernandez, C., Gomez-Coronado, D., Ferruelo, A. J. et al., Synergistic upregulation of low-density lipoprotein receptor activity by tamoxifen and lovastatin. Cardiovasc. Res. 2004, 64, 346-355.
9. Sanchez-Wandelmer, J., Davalos, A., de la Pena, G., Cano, S. et al., Haloperidol disrupts lipid rafts and impairs insulin signaling in SH-SY5Y cells. Neuroscience 2010, 167, 143-153.
10. Canfran-Duque, A., Casado, M. E., Pastor, O., Sanchez-Wandelmer, J. et al., Atypical antipsychotics alter cholesterol and fatty acid metabolism in vitro. J. Lipid Res. 2013, 54, 310-324.
11. Ludwig, A. K., Giebel, B., Exosomes: small vesicles participating in intercellular communication. Int. J. Biochem. Cell. Biol. 2012, 44, 11-15.
12. Record, M., Subra, C., Silvente-Poirot, S., Poirot, M., Exosomes as intercellular signalosomes and pharmacological effectors. Biochem. Pharmacol. 2011, 81, 1171-1182.
13. Klein, D., Bussow, H., Fewou, S. N., Gieselmann, V., Exocytosis of storage material in a lysosomal disorder. Biochem. Biophys. Res. Commun. 2005, 327, 663-667.
14. Strauss, K., Goebel, C., Runz, H., Mobius, W. et al., Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease. J. Biol. Chem. 2010, 285, 26279-26288.
15. Subra, C., Grand, D., Laulagnier, K., Stella, A. et al., Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J. Lipid Res. 2010, 51, 2105-2120.
16. Aggarwal, B. B., Sung, B., Pharmacological basis for the role of curcumin in chronic diseases: an age-old spice with modern targets. Trends. Pharmacol. Sci. 2009, 30, 85-94.
17. Peschel, D., Koerting, R., Nass, N., Curcumin induces changes in expression of genes involved in cholesterol homeostasis. J. Nutr. Biochem. 2007, 18, 113-119.
18. Dou, X., Fan, C., Wo, L., Yan, J. et al., Curcumin up-regulates LDL receptor expression via the sterol regulatory element pathway in HepG2 cells. Planta Med. 2008, 74, 1374-1379.
19. Kang, Q., Chen, A., Curcumin suppresses expression of low-density lipoprotein (LDL) receptor, leading to the inhibition of LDL-induced activation of hepatic stellate cells. Br. J. Pharmacol. 2009, 157, 1354-1367.
20. Dong, S. Z., Zhao, S. P., Wu, Z. H., Yang, J. et al., Curcumin promotes cholesterol efflux from adipocytes related to PPARgamma-LXRalpha-ABCA1 passway. Mol. Cell. Biochem. 2011, 358, 281-285.
21. Zhao, J. F., Ching, L. C., Huang, Y. C., Chen, C. Y. et al., Molecular mechanism of curcumin on the suppression of cholesterol accumulation in macrophage foam cells and atherosclerosis. Mol. Nutr. Food. Res. 2012, 56, 691-701.
22. Lloyd-Evans, E., Morgan, A. J., He, X., Smith, D. A. et al., Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 2008, 14, 1247-1255.
23. Daigneault, M., Preston, J. A., Marriott, H. M., Whyte, M. K., Dockrell, D. H., The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 2010, 5, e8668.
24. Martinez-Botas, J., Ferruelo, A. J., Suarez, Y., Fernandez, C. et al., Dose-dependent effects of lovastatin on cell cycle progression. Distinct requirement of cholesterol and non-sterol mevalonate derivatives. Biochim. Biophys. Acta 2001, 1532, 185-194.
25. Calvo, D., Gomez-Coronado, D., Suarez, Y., Lasuncion, M. A., Vega, M. A., Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL. J. Lipid Res. 1998, 39, 777-788.
26. Xu, Q., Jurgens, G., Huber, L. A., Bock, G. et al., Lipid utilization by human lymphocytes is correlated with high-density-lipoprotein binding site activity. Biochem. J. 1992, 285, 105-112.
27. Thery, C., Amigorena, S., Raposo, G., Clayton, A., Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell. Biol. 2006, Chapter 3: Unit 3.22.
28. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M. et al., Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell. Biol. 2007, 9, 654-659.
29. Savina, A., Furlan, M., Vidal, M., Colombo, M. I., Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem. 2003, 278, 20083-20090.
30. Chen, F. W., Li, C., Ioannou, Y. A., Cyclodextrin induces calcium-dependent lysosomal exocytosis. PLoS One 2010, 5, e15054.
31. Ben Trivedi, A., Kitabatake, N., Doi, E., Toxicity of dimethyl sulfoxide as a solvent in bioassay system with HeLa cells evaluated colorimetrically with 3-(4, 5-dimethylthiazol-2-yl)-2, 5-diphenyl-tetrazolium bromide. Agric. Biol. Chem. 1990, 54, 2961-2966.
32. Griffiths, G., Matteoni, R., Back, R., Hoflack, B., Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J. Cell. Sci. 1990, 95, 441-461.
33. Conde-Vancells, J., Rodriguez-Suarez, E., Embade, N., Gil, D. et al., Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J. Proteome Res. 2008, 7, 5157-5166.
34. Mathivanan, S., Fahner, C. J., Reid, G. E., Simpson, R. J., ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 2012, 40, D1241-1244.
35. Rodriguez, A., Webster, P., Ortego, J., Andrews, N. W., Lysosomes behave as Ca2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell. Biol. 1997, 137, 93-104.
36. Brini, M., Carafoli, E., Calcium pumps in health and disease. Physiol. Rev. 2009, 89, 1341-1378.
37. Bilmen, J. G., Khan, S. Z., Javed, M. H., Michelangeli, F., Inhibition of the SERCA Ca2+ pumps by curcumin. Curcumin putatively stabilizes the interaction between the nucleotide-binding and phosphorylation domains in the absence of ATP. Eur. J. Biochem. 2001, 268, 6318-6327.
38. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L. et al., Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319, 1244-1247
39. Laulagnier, K., Grand, D., Dujardin, A., Hamdi, S. et al., PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett. 2004, 572, 11-14.
40. Couzin, J., Cell biology: the ins and outs of exosomes. Science 2005, 308, 1862-1863.
41. van Niel, G., Raposo, G., Candalh, C., Boussac, M. et al., Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001, 121, 337-349.
42. Fevrier, B., Vilette, D., Archer, F., Loew, D. et al., Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. USA 2004, 101, 9683-9688.
43. Calzolari, A., Raggi, C., Deaglio, S., Sposi, N. M. et al., TfR2 localizes in lipid raft domains and is released in exosomes to activate signal transduction along the MAPK pathway. J. Cell. Sci. 2006, 119, 4486-4498.
44. O'Neill, H. C., Quah, B. J., Exosomes secreted by bacterially infected macrophages are proinflammatory. Sci. Signal. 2008, 1, pe8.
45. Yang, M., Chen, J., Su, F., Yu, B. et al., Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol. Cancer 2011, 10, 117.
46. Masyuk, A. I., Masyuk, T. V., Larusso, N. F., Exosomes in the pathogenesis, diagnostics and therapeutics of liver diseases. J. Hepatol. 2013, 59, 621-625.
47. Gupta, S. C., Patchva, S., Koh, W., Aggarwal, B. B., Discovery of curcumin, a component of golden spice, and its miraculous biological activities. Clin. Exp. Pharmacol. Physiol. 2012, 39, 283-299.
48. Ramirez-Tortosa, M. C., Mesa, M. D., Aguilera, M. C., Quiles, J. L. et al., Oral administration of a turmeric extract inhibits LDL oxidation and has hypocholesterolemic effects in rabbits with experimental atherosclerosis. Atherosclerosis 1999, 147, 371-378.
49. Borbon, I. A., Hillman, Z., Duran, E., Jr., Kiela, P. R. et al., Lack of efficacy of curcumin on neurodegeneration in the mouse model of Niemann-Pick C1. Pharmacol. Biochem. Behav. 2012, 101, 125-131.
50. Bishnoi, M., Chopra, K., Kulkarni, S. K., Protective effect of Curcumin, the active principle of turmeric (Curcuma longa) in haloperidol-induced orofacial dyskinesia and associated behavioural, biochemical and neurochemical changes in rat brain. Pharmacol. Biochem. Behav. 2008, 88, 511-522.
51. El-Beshbishy, H. A., Mohamadin, A. M., Nagy, A. A., Abdel-Naim, A. B., Amelioration of tamoxifen-induced liver injury in rats by grape seed extract, black seed extract and curcumin. Indian J. Exp. Biol. 2010, 48, 280-288.
52. Sookram, C., Tan, M., Daya, R., Heffernan, S., Mishra, R. K., Curcumin prevents haloperidol-induced development of abnormal oro-facial movements: possible implications of Bcl-XL in its mechanism of action. Synapse 2011, 65, 788-794.
53. Bala, K., Tripathy, B. C., Sharma, D., Neuroprotective and anti-ageing effects of curcumin in aged rat brain regions. Biogerontology 2006, 7, 81-89.
54. Khurana, S., Jain, S., Mediratta, P. K., Banerjee, B. D., Sharma, K. K., Protective role of curcumin on colchicine-induced cognitive dysfunction and oxidative stress in rats. Hum. Exp. Toxicol. 2012, 31, 686-697.
55. Singla, N., Dhawan, D. K., N-methyl N-nitrosourea induced functional and structural alterations in mice brain-role of curcumin. Neurotox. Res. 2012, 22, 115-126.
56. Natarajan, C., Bright, J. J., Curcumin inhibits experimental allergic encephalomyelitis by blocking IL-12 signaling through Janus kinase-STAT pathway in T lymphocytes. J. Immunol. 2002, 168, 6506-6513.
57. Frautschy, S. A., Hu, W., Kim, P., Miller, S. A. et al., Phenolic anti-inflammatory antioxidant reversal of Abeta-induced cognitive deficits and neuropathology. Neurobiol. Aging 2001, 22, 993-1005.
58. Sun, C. Y., Qi, S. S., Zhou, P., Cui, H. R. et al., Neurobiological and pharmacological validity of curcumin in ameliorating memory performance of senescence-accelerated mice. Pharmacol. Biochem. Behav. 2013, 105C, 76-82.
59. Aulinskas, T. H., Oram, J. F., Bierman, E. L., Coetzee, G. A. et al., Retro-endocytosis of low density lipoprotein by cultured human skin fibroblasts. Arteriosclerosis 1985, 5, 45-54.