Curcumin-loaded embryonic stem cell exosomes restored neurovascular unit following ischemia-reperfusion injury

International Journal of Biochemistry and Cell Biology

Volumn 79, Issue , 2016, Pages 360-369

  Kalani, Anuradha ^a   Chaturvedi, Pankaj ^a   Kamat, Pradip K ^a   Maldonado, Claudio ^a   Bauer, Philip ^a   Joshua, Irving G ^a   Tyagi, Suresh C ^a   Tyagi, Neetu ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Curcumin; Exosomes; Neurons; Stroke

Indexed keywords

CLAUDIN 5; CURCUMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; INTERCELLULAR ADHESION MOLECULE 1; MALONALDEHYDE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEURON SPECIFIC NUCLEAR PROTEIN; OCCLUDIN; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; VASCULAR ENDOTHELIAL CADHERIN; CELL ADHESION MOLECULE; NEUROPROTECTIVE AGENT; TIGHT JUNCTION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN WATER; CONTROLLED STUDY; EXOSOME; GENE EXPRESSION; MALE; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; PROTEIN BLOOD LEVEL; REPERFUSION INJURY; THERAPY EFFECT; ANIMAL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; DRUG FORMULATION; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; METABOLISM; NERVE CELL; PATHOLOGY;

ANIMALS; ASTROCYTES; CELL ADHESION MOLECULES; CURCUMIN; DRUG COMPOUNDING; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; EXOSOMES; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED C57BL; NEURONS; NEUROPROTECTIVE AGENTS; REPERFUSION INJURY; TIGHT JUNCTION PROTEINS;

EID: 84986325551     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2016.09.002     Document Type: Article

References (50)

1. Anand, P., Kunnumakkara, A.B., Newman, R.A., Aggarwal, B.B., Bioavailability of curcumin: problems and promises. Mol. Pharm. 4:6 (2007), 807–818.
2. Belayev, L., Alonso, O.F., Busto, R., Zhao, W., Ginsberg, M.D., Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke 27:9 (1996), 1616–1622 discussion 1623.
3. Chang, Y.C., Kim, H.W., Rapoport, S.I., Rao, J.S., Chronic NMDA administration increases neuroinflammatory markers in rat frontal cortex: cross-talk between excitotoxicity and neuroinflammation. Neurochem. Res. 33:11 (2008), 2318–2323.
4. Chopp, M., Zhang, Z.G., Emerging potential of exosomes and noncoding microRNAs for the treatment of neurological injury/diseases. Expert Opin. Emerg. Drugs 20:4 (2015), 523–526.
5. Corti, R., Hutter, R., Badimon, J.J., Fuster, V., Evolving concepts in the triad of atherosclerosis, inflammation and thrombosis. J. Thromb. Thrombolysis 17:1 (2004), 35–44.
6. Dai, L.Y., Cheng, B.H., Li, J., [Effect of curcumin on cerebral ischemia-reperfusion injury in rats]. Zhong Yao Cai 38:2 (2015), 344–349.
7. Doeppner, T.R., Herz, J., Gorgens, A., Schlechter, J., Ludwig, A.K., Radtke, S., de Miroschedji, K., Horn, P.A., Giebel, B., Hermann, D.M., Extracellular vesicles improve post-stroke neuroregeneration and prevent postischemic immunosuppression. Stem Cells Transl. Med. 4:10 (2015), 1131–1143.
8. Fan, X., Jiang, Y., Yu, Z., Yuan, J., Sun, X., Xiang, S., Lo, E.H., Wang, X., Combination approaches to attenuate hemorrhagic transformation after tPA thrombolytic therapy in patients with poststroke hyperglycemia/diabetes. Adv. Pharmacol. 71 (2014), 391–410.
9. Gangoda, L., Boukouris, S., Liem, M., Kalra, H., Mathivanan, S., Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic?. Proteomics 15:2–3 (2015), 260–271.
10. Gordon, G.R., Mulligan, S.J., MacVicar, B.A., Astrocyte control of the cerebrovasculature. Glia 55:12 (2007), 1214–1221.
11. Haney, M.J., Klyachko, N.L., Zhao, Y., Gupta, R., Plotnikova, E.G., He, Z., Patel, T., Piroyan, A., Sokolsky, M., Kabanov, A.V., Batrakova, E.V., Exosomes as drug delivery vehicles for Parkinson's disease therapy. J. Control. Release 207 (2015), 18–30.
12. Huber, J.D., Campos, C.R., Mark, K.S., Davis, T.P., Alterations in blood-brain barrier ICAM-1 expression and brain microglial activation after lambda-carrageenan-induced inflammatory pain. Am. J. Physiol. Heart Circ. Physiol. 290:2 (2006), H732–740.
13. Ji, B., Han, Y., Liu, Q., Liu, X., Yang, F., Zhou, R., Lian, Q., Cao, H., Li, J., [Curcumin improves the impaired working memory in cerebral ischemia-reperfusion rats by inhibiting proinflammatory cytokines]. Zhonghua Yi Xue Za Zhi 94:13 (2014), 1029–1033.
14. Kalani, A., Tyagi, N., Exosomes in neurological disease, neuroprotection, repair and therapeutics: problems and perspectives. Neural Regen. Res. 10:10 (2015), 1565–1567.
15. Kalani, A., Kamat, P.K., Chaturvedi, P., Tyagi, S.C., Tyagi, N., Curcumin-primed exosomes mitigate endothelial cell dysfunction during hyperhomocysteinemia. Life Sci. 107:1–2 (2014), 1–7.
16. Kalani, A., Kamat, P.K., Givvimani, S., Brown, K., Metreveli, N., Tyagi, S.C., Tyagi, N., Nutri-epigenetics ameliorates blood-brain barrier damage and neurodegeneration in hyperhomocysteinemia: role of folic acid. J. Mol. Neurosci. 52:2 (2014), 202–215.
17. Kalani, A., Kamat, P.K., Kalani, K., Tyagi, N., Epigenetic impact of curcumin on stroke prevention. Metab. Brain Dis., 2014.
18. Kalani, A., Tyagi, A., Tyagi, N., Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol. Neurobiol. 49:1 (2014), 590–600.
19. Kalani, A., Kamat, P.K., Tyagi, N., Diabetic stroke severity: epigenetic remodeling and neuronal, glial, and vascular dysfunction. Diabetes 64:12 (2015), 4260–4271.
20. Khan, M., Nickoloff, E., Abramova, T., Johnson, J., Verma, S.K., Krishnamurthy, P., Mackie, A.R., Vaughan, E., Garikipati, V.N., Benedict, C., Ramirez, V., Lambers, E., Ito, A., Gao, E., Misener, S., Luongo, T., Elrod, J., Qin, G., Houser, S.R., Koch, W.J., Kishore, R., Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ. Res. 117:1 (2015), 52–64.
21. Kochanek, K.D., Murphy, S.L., Xu, J., Arias, E., Mortality in the United States, 2013. NCHS Data Brief 178 (2014), 1–8.
22. Lai, R.C., Tan, S.S., Teh, B.J., Sze, S.K., Arslan, F., de Kleijn, D.P., Choo, A., Lim, S.K., Proteolytic potential of the MSC exosome proteome: implications for an exosome-mediated delivery of therapeutic proteasome. Int. J. Proteomics, 2012, 2012, 971907.
23. Lakhan, S.E., Kirchgessner, A., Hofer, M., Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J. Transl. Med., 7, 2009, 97.
24. Lau, L.T., Yu, A.C., Astrocytes produce and release interleukin-1, interleukin-6, tumor necrosis factor alpha and interferon-gamma following traumatic and metabolic injury. J. Neurotrauma 18:3 (2001), 351–359.
25. Li, Y., Liu, Z., Xin, H., Chopp, M., The role of astrocytes in mediating exogenous cell-based restorative therapy for stroke. Glia 62:1 (2014), 1–16.
26. Li, W., Suwanwela, N.C., Patumraj, S., Curcumin by down regulating NF-kB and elevating Nrf2, reduces brain edema and neurological dysfunction after cerebral I/R. Microvasc. Res., 2015.
27. Mishra, S., Palanivelu, K., The effect of curcumin (turmeric) on Alzheimer's disease: an overview. Ann. Indian Acad. Neurol. 11:1 (2008), 13–19.
28. M Mouslmani, J.M.R., Prabhakar, Neeraj, Peurla, Markus, Baydound, Elias, Patra, Digambara, Curcumin associated poly(allylamine hydrochloride)-phosphate self-assembled hierarchically ordered nanocapsules: size dependent investigation on release and DPPH scavenging activity of curcumin. RSC Adv. 5 (2015), 18740–18750.
29. Mozaffarian, D., Benjamin, E.J., Go, A.S., Arnett, D.K., Blaha, M.J., Cushman, M., de Ferranti, S., Despres, J.P., Fullerton, H.J., Howard, V.J., Huffman, M.D., Judd, S.E., Kissela, B.M., Lackland, D.T., Lichtman, J.H., Lisabeth, L.D., Liu, S., Mackey, R.H., Matchar, D.B., McGuire, D.K., Mohler, E.R. 3rd., Moy, C.S., Muntner, P., Mussolino, M.E., Nasir, K., Neumar, R.W., Nichol, G., Palaniappan, L., Pandey, D.K., Reeves, M.J., Rodriguez, C.J., Sorlie, P.D., Stein, J., Towfighi, A., Turan, T.N., Virani, S.S., Willey, J.Z., Woo, D., Yeh, R.W., Turner, M.B., American Heart Association Statistics, C., Stroke Statistics, S., Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation 131:4 (2015), e29–e322.
30. Munagala, R., Aqil, F., Jeyabalan, J., Gupta, R.C., Bovine milk-derived exosomes for drug delivery. Cancer Lett., 2015.
31. Ovbiagele, B., Potential role of curcumin in stroke prevention. Expert Rev. Neurother. 8:8 (2008), 1175–1176.
32. Pardridge, W.M., Drug transport across the blood-brain barrier. J. Cereb. Blood Flow Metab. 32:11 (2012), 1959–1972.
33. Patra, D., Sleem, F., A new method for pH triggered curcumin release by applying poly(L-lysine) mediated nanoparticle-congregation. Anal. Chim. Acta 795 (2013), 60–68.
34. Perry, E., Howes, M.J., Medicinal plants and dementia therapy: herbal hopes for brain aging?. CNS Neurosci. Ther. 17:6 (2011), 683–698.
35. Rai, S., Kamat, P.K., Nath, C., Shukla, R., A study on neuroinflammation and NMDA receptor function in STZ (ICV) induced memory impaired rats. J. Neuroimmunol. 254:1–2 (2013), 1–9.
36. Schipke, C.G., Ohlemeyer, C., Matyash, M., Nolte, C., Kettenmann, H., Kirchhoff, F., Astrocytes of the mouse neocortex express functional N-methyl-D-aspartate receptors. FASEB J. 15:7 (2001), 1270–1272.
37. Sokolova, V., Ludwig, A.K., Hornung, S., Rotan, O., Horn, P.A., Epple, M., Giebel, B., Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf. B Biointerfaces 87:1 (2011), 146–150.
38. Soni, K.B., Kuttan, R., Effect of oral curcumin administration on serum peroxides and cholesterol levels in human volunteers. Indian J. Physiol. Pharmacol. 36:4 (1992), 273–275.
39. Strimpakos, A.S., Sharma, R.A., Curcumin: preventive and therapeutic properties in laboratory studies and clinical trials. Antioxid. Redox Signal. 10:3 (2008), 511–545.
40. Sun, D., Zhuang, X., Xiang, X., Liu, Y., Zhang, S., Liu, C., Barnes, S., Grizzle, W., Miller, D., Zhang, H.G., A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol. Ther. 18:9 (2010), 1606–1614.
41. Thiyagarajan, M., Sharma, S.S., Neuroprotective effect of curcumin in middle cerebral artery occlusion induced focal cerebral ischemia in rats. Life Sci. 74:8 (2004), 969–985.
42. Tota, S., Kamat, P.K., Saxena, G., Hanif, K., Najmi, A.K., Nath, C., Central angiotensin converting enzyme facilitates memory impairment in intracerebroventricular streptozotocin treated rats. Behav. Brain Res. 226:1 (2012), 317–330.
43. Wang, S., Chen, P., Zhang, L., Yang, C., Zhai, G., Formulation and evaluation of microemulsion-based in situ ion-sensitive gelling systems for intranasal administration of curcumin. J. Drug Target. 20:10 (2012), 831–840.
44. Wang, H., Li, Y., Jiang, N., Chen, X., Zhang, Y., Zhang, K., Wang, T., Hao, Y., Ma, L., Zhao, C., Wang, Y., Sun, T., Yu, J., Protective effect of oxysophoridine on cerebral ischemia/reperfusion injury in mice. Neural Regen. Res. 8:15 (2013), 1349–1359.
45. Wong, R., NMDA receptors expressed in oligodendrocytes. Bioessays 28:5 (2006), 460–464.
46. Xin, H., Li, Y., Buller, B., Katakowski, M., Zhang, Y., Wang, X., Shang, X., Zhang, Z.G., Chopp, M., Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 30:7 (2012), 1556–1564.
47. Xin, H., Li, Y., Cui, Y., Yang, J.J., Zhang, Z.G., Chopp, M., Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J. Cereb. Blood Flow Metab. 33:11 (2013), 1711–1715.
48. Zhang, H.G., Grizzle, W.E., Exosomes: a novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am. J. Pathol. 184:1 (2014), 28–41.
49. Zhou, Y., Li, H.L., Zhao, R., Yang, L.T., Dong, Y., Yue, X., Ma, Y.Y., Wang, Z., Chen, J., Cui, C.L., Yu, A.C., Astrocytes express N-methyl-D-aspartate receptor subunits in development, ischemia and post-ischemia. Neurochem. Res. 35:12 (2010), 2124–2134.
50. Zhuang, X., Xiang, X., Grizzle, W., Sun, D., Zhang, S., Axtell, R.C., Ju, S., Mu, J., Zhang, L., Steinman, L., Miller, D., Zhang, H.G., Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol. Ther. 19:10 (2011), 1769–1779.