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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 3160360, 10 pages
https://doi.org/10.1155/2017/3160360
Research Article

HIV-1 Transactivator Protein Induces ZO-1 and Neprilysin Dysfunction in Brain Endothelial Cells via the Ras Signaling Pathway

1Department of Neurology, First Affiliated Hospital, Guangxi Medical University, Nanning 530021, China
2Nanxishan Hospital of Guangxi Zhuang Autonomous Region, Guilin 541000, China

Correspondence should be addressed to Wen Huang; moc.361@9221newh

Received 29 November 2016; Revised 9 February 2017; Accepted 1 March 2017; Published 2 May 2017

Academic Editor: Anna M. Giudetti

Copyright © 2017 Wenlin Jiang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. I. E. Adrás and M. Toborek, “HIV-1 stimulates nuclear entry of amyloid beta via dynamin dependent EEA1 and TGF-beta/Smad signaling,” Experimental Cell Research, vol. 323, no. 1, pp. 66–76, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Valcour, C. Shikuma, B. Shiramizu et al., “Higher frequency of dementia in older HIV-1 individuals: the Hawaii Aging with HIV-1 Cohort,” Neurology, vol. 63, no. 5, pp. 822–827, 2004. View at Publisher · View at Google Scholar
  3. I. E. András, S. Y. Eum, and M. Toborek, “Lipid rafts and functional caveolae regulate HIV-induced amyloid beta accumulation in brain endothelial cells,” Biochemical and Biophysical Research Communications, vol. 421, no. 2, pp. 177–183, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. C. L. Achim, A. Adame, W. Dumaop, I. P. Everall, E. Masliah, and Neurobehavioral Research Center, “Increased accumulation of intraneuronal amyloid beta in HIV-infected patients,” Journal of Neuroimmune Pharmacology, vol. 4, no. 2, pp. 190–199, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Y. Aksenov, M. V. Aksenova, C. F. Mactutus, and R. M. Booze, “HIV-1 protein-mediated amyloidogenesis in rat hippocampal cell cultures,” Neuroscience Letters, vol. 475, no. 3, pp. 174–178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Zhang, J. Liu, B. Katafiasz, H. Fox, and H. Xiong, “HIV-1 gp120-induced axonal injury detected by accumulation of beta-amyloid precursor protein in adult rat corpus callosum,” Journal of Neuroimmune Pharmacology, vol. 6, no. 4, pp. 650–657, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. H. C. Rempel and L. Pulliam, “HIV-1 Tat inhibits neprilysin and elevates amyloid beta,” Aids, vol. 19, no. 2, pp. 127–135, 2005. View at Publisher · View at Google Scholar
  8. I. E. András, S. Y. Eum, W. Huang, Y. Zhong, B. Hennig, and M. Toborek, “HIV-1-induced amyloid beta accumulation in brain endothelial cells is attenuated by simvastatin,” Molecular and Cellular Neurosciences, vol. 43, no. 2, pp. 232–243, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. W. Huang, S. Y. Eum, I. E. András, B. Hennig, and M. Toborek, “PPARalpha and PPARgamma attenuate HIV-induced dysregulation of tight junction proteins by modulations of matrix metalloproteinase and proteasome activities,” The FASEB Journal, vol. 23, no. 5, pp. 1596–1606, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. S. M. Woollard, B. Bhargavan, F. Yu, and G. D. Kanmogne, “Differential effects of Tat proteins derived from HIV-1 subtypes B and recombinant CRF02_AG on human brain microvascular endothelial cells: implications for blood-brain barrier dysfunction,” Journal of Cerebral Blood Flow and Metabolism, vol. 34, no. 6, pp. 1047–1059, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. I. E. András and M. Toborek, “Amyloid beta accumulation in HIV-1-infected brain: the role of the blood brain barrier,” IUBMB Life, vol. 65, no. 1, pp. 43–49, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Banerjee, X. Zhang, K. R. Manda, W. A. Banks, and N. Ercal, “HIV proteins (gp120 and Tat) and methamphetamine in oxidative stress-induced damage in the brain: potential role of the thiol antioxidant N-acetylcysteine amide,” Free Radical Biology & Medicine, vol. 48, no. 10, pp. 1388–1398, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. P. Dalvi, K. Wang, J. Mermis et al., “HIV-1/cocaine induced oxidative stress disrupts tight junction protein-1 in human pulmonary microvascular endothelial cells: role of Ras/ERK1/2 pathway,” PloS One, vol. 9, no. 1, article e85246, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Alluri, R. L. Wilson, C. Anasooya Shaji et al., “Melatonin preserves blood-brain barrier integrity and permeability via matrix metalloproteinase-9 inhibition,” PloS One, vol. 11, no. 5, article e0154427, 2016. View at Publisher · View at Google Scholar · View at Scopus
  15. I. E. András, G. Rha, W. Huang et al., “Simvastatin protects against amyloid beta and HIV-1 Tat-induced promoter activities of inflammatory genes in brain endothelial cells,” Molecular Pharmacology, vol. 73, no. 5, pp. 1424–1433, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Kim, J. H. Yoon, and Y. S. Kim, “HIV-1 Tat interacts with and regulates the localization and processing of amyloid precursor protein,” PloS One, vol. 8, no. 11, article e77972, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Ito, K. Matsumiya, S. Ohtsuki, J. Kamiie, and T. Terasaki, “Contributions of degradation and brain-to-blood elimination across the blood-brain barrier to cerebral clearance of human amyloid-beta peptide (1-40) in mouse brain,” Journal of Cerebral Blood Flow and Metabolism, vol. 33, no. 11, pp. 1770–1777, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Schmukler, E. Grinboim, S. Schokoroy et al., “Ras inhibition enhances autophagy, which partially protects cells from death,” Oncotarget, vol. 4, no. 1, pp. 142–152, 2013. View at Publisher · View at Google Scholar
  19. Y. Zhong, B. Hennig, and M. Toborek, “Intact lipid rafts regulate HIV-1 Tat protein-induced activation of the Rho signaling and upregulation of P-glycoprotein in brain endothelial cells,” Journal of Cerebral Blood Flow and Metabolism, vol. 30, no. 3, pp. 522–533, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. D. A. Mayes, T. A. Rizvi, H. Titus-Mitchell et al., “Nf1 loss and Ras hyperactivation in oligodendrocytes induce NOS-driven defects in myelin and vasculature,” Cell Reports, vol. 4, no. 6, pp. 1197–1212, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Schmukler, E. Wolfson, R. Haklai, G. Elad-Sfadia, Y. Kloog, and R. Pinkas-Kramarski, “Chloroquine synergizes with FTS to enhance cell growth inhibition and cell death,” Oncotarget, vol. 5, no. 1, pp. 173–184, 2014. View at Publisher · View at Google Scholar
  22. E. Bustinza-Linares, R. Kurzrock, and A. M. Tsimberidou, “Salirasib in the treatment of pancreatic cancer,” Future Oncology, vol. 6, no. 6, pp. 885–891, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. E. Aizman, E. Blacher, O. Ben-Moshe, T. Kogan, Y. Kloog, and A. Mor, “Therapeutic effect of farnesylthiosalicylic acid on adjuvant-induced arthritis through suppressed release of inflammatory cytokines,” Clinical and Experimental Immunology, vol. 175, no. 3, pp. 458–467, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Poggi, R. Carosio, D. Fenoglio et al., “Migration of V delta 1 and V delta 2 T cells in response to CXCR3 and CXCR4 ligands in healthy donors and HIV-1-infected patients: competition by HIV-1 Tat,” Blood, vol. 103, no. 6, pp. 2205–2213, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Zhong, E. J. Smart, B. Weksler, P. O. Couraud, B. Hennig, and M. Toborek, “Caveolin-1 regulates human immunodeficiency virus-1 Tat-induced alterations of tight junction protein expression via modulation of the Ras signaling,” The Journal of Neuroscience, vol. 28, no. 31, pp. 7788–7796, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Agrawal, J. P. Louboutin, B. A. Reyes, E. J. Van Bockstaele, and D. S. Strayer, “HIV-1 Tat neurotoxicity: a model of acute and chronic exposure, and neuroprotection by gene delivery of antioxidant enzymes,” Neurobiology of Disease, vol. 45, no. 2, pp. 657–670, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Buscemi, D. Ramonet, and J. D. Geiger, “Human immunodeficiency virus type-1 protein Tat induces tumor necrosis factor-alpha-mediated neurotoxicity,” Neurobiology of Disease, vol. 26, no. 3, pp. 661–670, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. J. E. King, E. A. Eugenin, C. M. Buckner, and J. W. Berman, “HIV tat and neurotoxicity,” Microbes and Infection / Institut Pasteur, vol. 8, no. 5, pp. 1347–1357, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. X. Chen, L. Hui, N. H. Geiger, N. J. Haughey, and J. D. Geiger, “Endolysosome involvement in HIV-1 transactivator protein-induced neuronal amyloid beta production,” Neurobiology of Aging, vol. 34, no. 10, pp. 2370–2378, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Niu, H. Yao, W. Zhang, R. L. Sutliff, and S. Buch, “Tat 101-mediated enhancement of brain pericyte migration involves platelet-derived growth factor subunit B homodimer: implications for human immunodeficiency virus-associated neurocognitive disorders,” The Journal of Neuroscience, vol. 34, no. 35, pp. 11812–11825, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Matzen, A. E. Dirkx, M. G. Oude Egbrink et al., “HIV-1 Tat increases the adhesion of monocytes and T-cells to the endothelium in vitro and in vivo: implications for AIDS-associated vasculopathy,” Virus Research, vol. 104, no. 2, pp. 145–155, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Toborek, Y. W. Lee, H. Pu et al., “HIV-Tat protein induces oxidative and inflammatory pathways in brain endothelium,” Journal of Neurochemistry, vol. 84, no. 1, pp. 169–179, 2003. View at Google Scholar
  33. Y. Chen, W. Huang, W. Jiang, X. Wu, B. Ye, and X. Zhou, “HIV-1 Tat regulates occludin and Abeta transfer receptor expression in brain endothelial cells via Rho/ROCK signaling pathway,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 4196572, p. 9, 2016. View at Publisher · View at Google Scholar
  34. R. F. Wu, Z. Ma, D. P. Myers, and L. S. Terada, “HIV-1 Tat activates dual Nox pathways leading to independent activation of ERK and JNK MAP kinases,” The Journal of Biological Chemistry, vol. 282, no. 52, pp. 37412–37419, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. W. Huang, L. Chen, B. Zhang, M. Park, and M. Toborek, “PPAR agonist-mediated protection against HIV Tat-induced cerebrovascular toxicity is enhanced in MMP-9-deficient mice,” Journal of Cerebral Blood Flow and Metabolism, vol. 34, no. 4, pp. 646–653, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Strazza, V. Pirrone, B. Wigdahl, and M. R. Nonnemacher, “Breaking down the barrier: the effects of HIV-1 on the blood-brain barrier,” Brain Research, vol. 1399, pp. 96–115, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. S. C. Wassmer, V. Combes, F. J. Candal, I. Juhan-Vague, and G. E. Grau, “Platelets potentiate brain endothelial alterations induced by plasmodium falciparum,” Infection and Immunity, vol. 74, no. 1, pp. 645–653, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Mishra and S. K. Singh, “HIV-1 Tat C phosphorylates VE-cadherin complex and increases human brain microvascular endothelial cell permeability,” BMC Neuroscience, vol. 15, no. 80, p. 12, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Spencer, R. A. Marr, R. Gindi et al., “Peripheral delivery of a CNS targeted, metalo-protease reduces Ab toxicity in a mouse model of Alzheimer’s disease,” PloS One, vol. 6, no. 1, article e16575, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Iwata, S. Tsubuki, Y. Takaki et al., “Metabolic regulation of brain Abeta by neprilysin,” Science, vol. 292, no. 5521, pp. 1550–1552, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Kakiya, T. Saito, P. Nilsson et al., “Cell surface expression of the major amyloid-beta peptide (Abeta)-degrading enzyme, neprilysin, depends on phosphorylation by mitogen-activated protein kinase/extracellular signal-regulated kinase kinase (MEK) and dephosphorylation by protein phosphatase 1a,” The Journal of Biological Chemistry, vol. 287, no. 35, pp. 29362–29372, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. P. A. Fitzpatrick, A. F. Guinan, T. G. Walsh et al., “Down-regulation of neprilysin (EC3.4.24.11) expression in vascular endothelial cells by laminar shear stress involves NADPH oxidase-dependent ROS production,” The International Journal of Biochemistry & Cell Biology, vol. 41, no. 11, pp. 2287–2294, 2009. View at Publisher · View at Google Scholar · View at Scopus