Silencing microRNA-143 protects the integrity of the blood-brain barrier: Implications for methamphetamine abuse

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Bai, Ying ^a   Zhang, Yuan ^b   Hua, Jun ^c   Yang, Xiangyu ^a   Zhang, Xiaotian ^d   Duan, Ming ^a   Zhu, Xinjian ^e   Huang, Wenhui ^a   Chao, Jie ^f   Zhou, Rongbin ^b   Hu, Gang ^a,c   Yao, Honghong ^a  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

^c SOUTHEAST UNIVERSITY   (China)

^d BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^e SAARLAND UNIVERSITY   (Germany)

^f UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; BBC3 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHAMPHETAMINE; MICRORNA; MIRN143 MICRORNA, HUMAN; MIRN143 MICRORNA, MOUSE; ONCOPROTEIN; PROTEIN P53; PUMA PROTEIN, MOUSE; TIGHT JUNCTION PROTEIN; TP53 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

AMPHETAMINE DEPENDENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD BRAIN BARRIER; C57BL MOUSE; CELL CULTURE; DEFICIENCY; DRUG EFFECTS; ENDOTHELIUM CELL; GENE SILENCING; GENETICS; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AMPHETAMINE-RELATED DISORDERS; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BLOOD-BRAIN BARRIER; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE SILENCING; HUMANS; MALE; METHAMPHETAMINE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TIGHT JUNCTION PROTEINS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84992398719     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35642     Document Type: Article

References (59)

1. Abbott, N. J., Ronnback, L. & Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53 (2006).
2. Abumiya, T. et al. Activated microvessels express vascular endothelial growth factor and integrin alpha(v)beta3 during focal cerebral ischemia. J. Cereb. Blood Flow Metab. 19, 1038-1050 (1999).
3. Argaw, A. T. et al. Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J. Clin. Invest. 122, 2454-2468 (2012).
4. Yao, Y., Chen, Z. L., Norris, E. H. & Strickland, S. Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat. Commun. 5, 3413 (2014).
5. Persidsky, Y., Ramirez, S. H., Haorah, J. & Kanmogne, G. D. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J. Neuroimmune Pharmacol. 1, 223-236 (2006).
6. Dore-Duffy, P., Katychev, A., Wang, X. & Van Buren, E. CNS microvascular pericytes exhibit multipotential stem cell activity. J. Cereb. Blood Flow Metab. 26, 613-624 (2006).
7. Zipser, B. D. et al. Microvascular injury and blood-brain barrier leakage in Alzheimers disease. Neurobiol. Aging. 28, 977-986 (2007).
8. van Vliet, E. A. et al. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain. 130, 521-534 (2007).
9. Wardlaw, J. M. et al. Lacunar stroke is associated with diffuse blood-brain barrier dysfunction. Ann. Neurol. 65, 194-202 (2009).
10. Schepers, R. J. et al. Methamphetamine and amphetamine pharmacokinetics in oral fluid and plasma after controlled oral methamphetamine administration to human volunteers. Clin. Chem. 49, 121-132 (2003).
11. Kaushal, N. & Matsumoto, R. R. Role of sigma receptors in methamphetamine-induced neurotoxicity. Curr. Neuropharmacol. 9, 54-57 (2011).
12. Bowyer, J. F. & Ali, S. High doses of methamphetamine that cause disruption of the blood-brain barrier in limbic regions produce extensive neuronal degeneration in mouse hippocampus. Synapse. 60, 521-532 (2006).
13. Martins, T. et al. Methamphetamine-induced nitric oxide promotes vesicular transport in blood-brain barrier endothelial cells. Neuropharmacology. 65, 74-82 (2013).
14. Sharma, H. S. & Kiyatkin, E. A. Rapid morphological brain abnormalities during acute methamphetamine intoxication in the rat: An experimental study using light and electron microscopy. J. Chem. Neuroanat. 37, 18-32 (2009).
15. Urrutia, A. et al. A study on the effect of JNK inhibitor, SP600125, on the disruption of blood-brain barrier induced by methamphetamine. Neurobiol. Dis. 50, 49-58 (2013).
16. Melgar, M. A., Rafols, J., Gloss, D. & Diaz, F. G. Postischemic reperfusion: ultrastructural blood-brain barrier and hemodynamic correlative changes in an awake model of transient forebrain ischemia. Neurosurgery. 56, 571-581 (2005).
17. Kalani, A. et al. Role of microRNA29b in blood-brain barrier dysfunction during hyperhomocysteinemia: An epigenetic mechanism. J. Cereb. Blood Flow Metab. 34, 1212-1222 (2014).
18. Reijerkerk, A. et al. MicroRNAs regulate human brain endothelial cell-barrier function in inflammation: implications for multiple sclerosis. J. Neurosci. 33, 6857-6863 (2013).
19. Li, H. et al. Effects of microRNA-143 in the differentiation and proliferation of bovine intramuscular preadipocytes. Mol. Biol. Rep. 38, 4273-4280 (2011).
20. Li, R. et al. MicroRNA-143 targets Syndecan-1 to repress cell growth in melanoma. PLoS One. 9, e94855 (2014).
21. Borralho, P. M. et al. miR-143 overexpression impairs growth of human colon carcinoma xenografts in mice with induction of apoptosis and inhibition of proliferation. PLoS One. 6, e23787 (2011).
22. Jordan, S. D. et al. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat. Cell Biol. 13, 434-446 (2011).
23. Chipuk, J. E. & Green, D. R. PUMA cooperates with direct activator proteins to promote mitochondrial outer membrane permeabilization and apoptosis. Cell Cycle. 8, 2692-2696 (2009).
24. Thakur, V. S. et al. p53-Dependent p21-mediated growth arrest pre-empts and protects HCT116 cells from PUMA-mediated apoptosis induced by EGCG. Cancer Lett. 296, 225-232 (2010).
25. Yu, J., Zhang, L., Hwang, P. M., Kinzler, K. W. & Vogelstein, B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell. 7, 673-682 (2001).
26. Nakano, K. & Vousden, K. H. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell. 7, 683-694 (2001).
27. Sharma, A., Hu, X. T., Napier, T. C. & Al-Harthi, L. Methamphetamine and HIV-1 Tat down regulate beta-catenin signaling: implications for methampetamine abuse and HIV-1 co-morbidity. J. Neuroimmune Pharmacol. 6, 597-607 (2011).
28. Talloczy, Z. et al. Methamphetamine inhibits antigen processing, presentation, and phagocytosis. PLoS Pathog. 4, e28 (2008).
29. Takahashi, S., Miwa, T. & Horikomi, K. Involvement of sigma 1 receptors in methamphetamine-induced behavioral sensitization in rats. Neurosci. Lett. 289, 21-24 (2000).
30. Robson, M. J. et al. SN79, a sigma receptor antagonist, attenuates methamphetamine-induced astrogliosis through a blockade of OSMR/gp130 signaling and STAT3 phosphorylation. Exp. Neurol. 254, 180-189 (2014).
31. Chen, X. et al. Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene. 28, 1385-1392 (2009).
32. Kohlstedt, K. et al. AMP-Activated protein kinase regulates endothelial cell angiotensin-converting enzyme expression via p53 and the post-Transcriptional regulation of microRNA-143/145. Circ. Res. 112, 1150-1158 (2013).
33. Climent, M. et al. TGFbeta triggers miR-143/145 transfer from smooth muscle cells to endothelial cells, thereby modulating vessel stabilization. Circ. Res. 116, 1753-1764 (2015).
34. Hergenreider, E. et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol. 14, 249-256 (2012).
35. Boettger, T. et al. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J. Clin. Invest. 119, 2634-2647 (2009).
36. Cordes, K. R. et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature. 460, 705-710 (2009).
37. Elia, L. et al. The knockout of miR-143 and-145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ. 16, 1590-1598 (2009).
38. Quintavalle, M., Elia, L., Condorelli, G. & Courtneidge, S. A. MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J. Cell Biol. 189, 13-22 (2010).
39. Xin, M. et al. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev. 23, 2166-2178 (2009).
40. Tu, J. B. et al. Pingyangmycin stimulates apoptosis in human hemangioma-derived endothelial cells through activation of the p53 pathway. Mol. Med. Rep. 10, 301-305 (2014).
41. Weng, C. Y. et al. Arsenic trioxide induces unfolded protein response in vascular endothelial cells. Arch. Toxicol. 88, 213-226 (2014).
42. Zhang, F. et al. Proliferative and survival effects of PUMA promote angiogenesis. Cell Rep. 2, 1272-1285 (2012).
43. Yan, J. et al. Blood-brain barrier disruption following subarchnoid hemorrhage may be faciliated through PUMA induction of endothelial cell apoptosis from the endoplasmic reticulum. Exp. Neurol. 230, 240-247 (2011).
44. Miao, Y. S. et al. MiR-18a increased the permeability of BTB via RUNX1 mediated down-regulation of ZO-1, occludin and claudin-5. Cell. Signal. 27, 156-167 (2015).
45. Zhang, Y. G. et al. Tight junction CLDN2 gene is a direct target of the vitamin D receptor. Sci. Rep. 5, 10642 (2015).
46. Na, W., Lee, J. Y., Kim, W. S., Yune, T. Y. & Ju, B. G. 17beta-estradiol ameliorates tight junction disruption via repression of MMP transcription. Mol. Endocrinol. 29, 1347-1361 (2015).
47. ElKeeb, A. M., Collier, M. E., Maraveyas, A. & Ettelaie, C. Accumulation of tissue factor in endothelial cells induces cell apoptosis, mediated through p38 and p53 activation. Thromb. Haemost. 114, 364-378 (2015).
48. Yin, J. et al. Pyrrolidine dithiocarbamate inhibits NF-KappaB activation and upregulates the expression of Gpx1, Gpx4, occludin, and ZO-1 in DSS-induced colitis. Appl. Biochem. Biotechnol. 177, 1716-1728 (2015).
49. Lee, H. Y. et al. Sphingosylphosphorylcholine stimulates CCL2 production from human umbilical vein endothelial cells. J. Immunol. 186, 4347-4353 (2011).
50. Jiang, S. et al. A novel miR-155/miR-143 cascade controls glycolysis by regulating hexokinase 2 in breast cancer cells. EMBO J. 31, 1985-1998 (2012).
51. Yao, H., Duan, M. & Buch, S. Cocaine-mediated induction of platelet-derived growth factor: implication for increased vascular permeability. Blood. 117, 2538-2547 (2011).
52. Yao, H., Duan, M., Hu, G. & Buch, S. Platelet-derived growth factor B chain is a novel target gene of cocaine-mediated Notch1 signaling: implications for HIV-Associated neurological disorders. J. Neurosci. 31, 12449-12454 (2011).
53. Ramirez, S. H. et al. Methamphetamine disrupts blood-brain barrier function by induction of oxidative stress in brain endothelial cells. J. Cereb. Blood Flow Metab. 29, 1933-1945 (2009).
54. Schmidt, C. J., Ritter, J. K., Sonsalla, P. K., Hanson, G. R. & Gibb, J. W. Role of dopamine in the neurotoxic effects of methamphetamine. J. Pharmacol. Exp. Ther. 233, 539-544 (1985).
55. Yao, H. et al. Molecular mechanisms involving sigma receptor-mediated induction of MCP-1: implication for increased monocyte transmigration. Blood. 115, 4951-4962 (2010).
56. Wang, H. et al. P2RX7 sensitizes Mac-1/ICAM-1-dependent leukocyte-endothelial adhesion and promotes neurovascular injury during septic encephalopathy. Cell Res. 25, 674-690 (2015).
57. Hill, R. A., Patel, K. D., Goncalves, C. M., Grutzendler, J. & Nishiyama, A. Modulation of oligodendrocyte generation during a critical temporal window after NG2 cell division. Nat. Neurosci. 17, 1518-1527 (2014).
58. Yao, H. et al. Cocaine hijacks sigma1 receptor to initiate induction of activated leukocyte cell adhesion molecule: implication for increased monocyte adhesion and migration in the CNS. J. Neurosci. 31, 5942-5955 (2011).
59. Yao, H. et al. MiR-9 promotes microglial activation by targeting MCPIP1. Nat. Commun. 5, 4386 (2014).