β-Caryophyllene protects in vitro neurovascular unit against oxygen-glucose deprivation and re-oxygenation-induced injury

Journal of Neurochemistry

Volumn 139, Issue 5, 2016, Pages 757-768

  Tian, Xiaocui ^a   Peng, Jianhua ^b   Zhong, Jianjun ^c   Yang, Mei ^a   Pang, Jinwei ^b   Lou, Jie ^a   Li, Minghang ^a   An, Ruidi ^a   Zhang, Qian ^a   Xu, Lu ^a   Dong, Zhi ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b THE AFFILIATED HOSPITAL OF SOUTHWEST MEDICAL UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Blood brain barrier; neuronal apoptosis; neurovascular unit; oxygen glucose deprivation and re oxygenation; caryophyllene

Indexed keywords

CARYOPHYLLENE; CLAUDIN 5; GELATINASE B; NEUROMODULIN; OCCLUDIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN ZO1; GLUCOSE; NEUROPROTECTIVE AGENT; NONSTEROID ANTIINFLAMMATORY AGENT; OXYGEN; SESQUITERPENE;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN MICROVASCULAR ENDOTHELIAL CELL; CAPILLARY ENDOTHELIAL CELL; COCULTURE; CYTOKINE RELEASE; DOWN REGULATION; DRUG ACTIVITY; ENZYME ACTIVITY; HYPOGLYCEMIA; HYPOXIA; IN VITRO STUDY; MODEL; NERVE CELL; NERVE CELL CULTURE; NERVOUS SYSTEM PARAMETERS; NEUROPROTECTION; NEUROVASCULAR UNIT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; UPREGULATION; ANIMAL; CELL CULTURE; CELL HYPOXIA; DEFICIENCY; DRUG EFFECTS; METABOLISM; MICROVASCULATURE; NEWBORN; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULAR ENDOTHELIUM;

ANIMALS; ANIMALS, NEWBORN; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL HYPOXIA; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; GLUCOSE; MICROVESSELS; NEURONS; NEUROPROTECTIVE AGENTS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; SESQUITERPENES;

EID: 84988420211     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13833     Document Type: Article

References (54)

1. Amenta P. S., Jallo J. I., Tuma R. F. and Elliott M. B. (2012) A cannabinoid type 2 receptor agonist attenuates blood-brain barrier damage and neurodegeneration in a murine model of traumatic brain injury. J. Neurosci. Res. 90, 2293–2305.
2. Asahi M., Wang X., Mori T., Sumii T., Jung J. C., Moskowitz M. A., Fini M. E. and Lo E. H. (2001) Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 21, 7724–7732.
3. Bastide M., Ouk T., Plaisier F., Petrault O., Stolc S. and Bordet R. (2007) Neurogliovascular unit after cerebral ischemia: is the vascular wall a pharmacological target. Psychoneuroendocrinology 32(Suppl 1), S36–S39.
4. Bedirli N., Bagriacik E. U., Emmez H., Yilmaz G., Unal Y. and Ozkose Z. (2012) Sevoflurane and isoflurane preconditioning provides neuroprotection by inhibition of apoptosis-related mRNA expression in a rat model of focal cerebral ischemia. J. Neurosurg. Anesthesiol. 24, 336–344.
5. Bento A. F., Marcon R., Dutra R. C., Claudino R. F., Cola M., Leite D. F. and Calixto J. B. (2011) beta-Caryophyllene inhibits dextran sulfate sodium-induced colitis in mice through CB2 receptor activation and PPARgamma pathway. Am. J. Pathol. 178, 1153–1166.
6. Calabria A. R. and Shusta E. V. (2008) A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. J. Cereb. Blood Flow Metab. 28, 135–148.
7. Calleja M. A., Vieites J. M., Montero-Melendez T., Torres M. I., Faus M. J., Gil A. and Suarez A. (2013) The antioxidant effect of beta-caryophyllene protects rat liver from carbon tetrachloride-induced fibrosis by inhibiting hepatic stellate cell activation. Br. J. Nutr. 109, 394–401.
8. Chang H. J., Kim H. J. and Chun H. S. (2007) Quantitative structure-activity relationship (QSAR) for neuroprotective activity of terpenoids. Life Sci. 80, 835–841.
9. Chen F., Ohashi N., Li W., Eckman C. and Nguyen J. H. (2009) Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure. Hepatology 50, 1914–1923.
10. Choi I. Y., Ju C., Anthony Jalin A. M., da Lee I., Prather P. L. and Kim W. K. (2013) Activation of cannabinoid CB2 receptor-mediated AMPK/CREB pathway reduces cerebral ischemic injury. Am. J. Pathol. 182, 928–939.
11. Clark A. W., Krekoski C. A., Bou S. S., Chapman K. R. and Edwards D. R. (1997) Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci. Lett. 238, 53–56.
12. Deli M. A., Ábrahám C. S., Kataoka Y. and Niwa M. (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell. Mol. Neurobiol. 25, 59–127.
13. Denny J. B. (2006) Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr. Neuropharmacol. 4, 293–304.
14. Fujii M., Sherchan P., Soejima Y., Hasegawa Y., Flores J., Doycheva D. and Zhang J. H. (2014) Cannabinoid receptor type 2 agonist attenuates apoptosis by activation of phosphorylated CREB-Bcl-2 pathway after subarachnoid hemorrhage in rats. Exp. Neurol. 261, 396–403.
15. Gertsch J., Leonti M., Raduner S., Racz I., Chen J.-Z., Xie X.-Q., Altmann K.-H., Karsak M. and Zimmer A. (2008) Beta-caryophyllene is a dietary cannabinoid. Proc. Natl Acad. Sci. 105, 9099–9104.
16. Girouard H. and Iadecola C. (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J. Appl. Physiol. 100, 328–335.
17. Haseloff R. F., Blasig I. E., Bauer H. C. and Bauer H. (2005) In search of the astrocytic factor(s) modulating blood-brain barrier functions in brain capillary endothelial cells in vitro. Cell. Mol. Neurobiol. 25, 25–39.
18. Hausenloy D. J. and Yellon D. M. (2016) Ischaemic conditioning and reperfusion injury. Nat. Rev. Cardiol. 13, 193–209.
19. Hawkins B. T. and Davis T. P. (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 57, 173–185.
20. Heo J. H., Lucero J., Abumiya T., Koziol J. A., Copeland B. R. and del Zoppo G. J. (1999) Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J. Cereb. Blood Flow Metab. 19, 624–633.
21. Jauch E. C., Saver J. L., Adams H. P., Jr et al. (2013) Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 44, 870–947.
22. Kidambi S., Lee I. and Chan C. (2008) Primary neuron/astrocyte co-culture on polyelectrolyte multilayer films: a template for studying astrocyte-mediated oxidative stress in neurons. Adv. Funct. Mater. 18, 294–301.
23. Kim C., Cho S. K., Kim K. D. et al. (2014) Beta-caryophyllene oxide potentiates TNFalpha-induced apoptosis and inhibits invasion through down-modulation of NF-kappaB-regulated gene products. Apoptosis 19, 708–718.
24. Kimura-Ohba S. and Yang Y. (2016) Oxidative DNA damage mediated by intranuclear MMP activity is associated with neuronal apoptosis in ischemic stroke. Oxid. Med. Cell. Longev. 2016, 6927328.
25. Li S. and Carmichael S. T. (2006) Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke. Neurobiol. Dis. 23, 362–373.
26. Lippmann E. S., Weidenfeller C., Svendsen C. N. and Shusta E. V. (2011) Blood-brain barrier modeling with co-cultured neural progenitor cell-derived astrocytes and neurons. J. Neurochem. 119, 507–520.
27. Liu H., Yang G., Tang Y., Cao D., Qi T., Qi Y. and Fan G. (2013) Physicochemical characterization and pharmacokinetics evaluation of beta-caryophyllene/beta-cyclodextrin inclusion complex. Int. J. Pharm. 450, 304–310.
28. Lou J., Cao G., Li R., Liu J., Dong Z. and Xu L. (2016) Beta-caryophyllene attenuates focal cerebral ischemia-reperfusion injury by Nrf2/HO-1 pathway in rats. Neurochem. Res. 41, 1291–1304.
29. Luissint A. C., Artus C., Glacial F., Ganeshamoorthy K. and Couraud P. O. (2012) Tight junctions at the blood brain barrier: physiological architecture and disease-associated dysregulation. Fluids Barriers CNS 9, 23.
30. Mattson M. P., Duan W., Pedersen W. A. and Culmsee C. (2001) Neurodegenerative disorders and ischemic brain diseases. Apoptosis 6, 69–81.
31. Meiri K. F., Pfenninger K. H. and Willard M. B. (1986) Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc. Natl Acad. Sci. USA 83, 3537–3541.
32. Murata K., Matsumura S., Yoshioka Y., Ueno Y. and Matsuda H. (2015) Screening of beta-secretase and acetylcholinesterase inhibitors from plant resources. J. Nat. Med. 69, 123–129.
33. Murikinati S., Juttler E., Keinert T. et al. (2010) Activation of cannabinoid 2 receptors protects against cerebral ischemia by inhibiting neutrophil recruitment. FASEB J. 24, 788–798.
34. Nakagawa S., Deli M. A., Nakao S., Honda M., Hayashi K., Nakaoke R., Kataoka Y. and Niwa M. (2007) Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell. Mol. Neurobiol. 27, 687–694.
35. Nakagawa S., Deli M. A., Kawaguchi H., Shimizudani T., Shimono T., Kittel A., Tanaka K. and Niwa M. (2009) A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem. Int. 54, 253–263.
36. Obermeier B., Daneman R. and Ransohoff R. M. (2013) Development, maintenance and disruption of the blood-brain barrier. Nat. Med. 19, 1584–1596.
37. O'Donnell L. A., Henkins K. M., Kulkarni A., Matullo C. M., Balachandran S., Pattisapu A. K. and Rall G. F. (2015) Interferon gamma induces protective non-canonical signaling pathways in primary neurons. J. Neurochem. 135, 309–322.
38. Ruck T., Bittner S., Epping L., Herrmann A. M. and Meuth S. G. (2014) Isolation of primary murine brain microvascular endothelial cells. J. Vis. Exp. 14, e52204.
39. Schiera G. and Sala S. (2005) Permeability properties of a three-cell type in vitro model of blood-brain barrier. J. Cell Mol. Med. 9, 373–379.
40. Shan H., Bian Y., Shu Z., Zhang L., Zhu J., Ding J., Lu M., Xiao M. and Hu G. (2016) Fluoxetine protects against IL-1beta-induced neuronal apoptosis via downregulation of p53. Neuropharmacology 107, 68–78.
41. Shimbo D., Abumiya T., Shichinohe H., Nakayama N., Kazumata K. and Houkin K. (2014) Post-ischemic intra-arterial infusion of liposome-encapsulated hemoglobin can reduce ischemia reperfusion injury. Brain Res. 1554, 59–66.
42. Simon M. J. and Iliff J. J. (2016) Regulation of cerebrospinal fluid (CSF) flow in neurodegenerative, neurovascular and neuroinflammatory disease. Biochim. Biophys. Acta 1862, 442–451.
43. Soejima Y., Hu Q., Krafft P. R., Fujii M., Tang J. and Zhang J. H. (2013) Hyperbaric oxygen preconditioning attenuates hyperglycemia-enhanced hemorrhagic transformation by inhibiting matrix metalloproteinases in focal cerebral ischemia in rats. Exp. Neurol. 247, 737–743.
44. Turner R. J. and Sharp F. R. (2016) Implications of MMP9 for blood brain barrier disruption and hemorrhagic transformation following ischemic stroke. Front. Cell. Neurosci. 10, 56.
45. Vangilder R. L., Rosen C. L., Barr T. L. and Huber J. D. (2011) Targeting the neurovascular unit for treatment of neurological disorders. Pharmacol. Ther. 130, 239–247.
46. Wang C. P., Shi Y. W., Tang M., Zhang X. C., Gu Y., Liang X. M., Wang Z. W. and Ding F. (2016) Isoquercetin ameliorates cerebral impairment in focal ischemia through anti-oxidative, anti-inflammatory, and anti-apoptotic effects in primary culture of rat hippocampal neurons and hippocampal CA1 region of rats. Mol. Neurobiol. DOI: 10.1007/s12035-016-9806-5.
47. Xue Q., Liu Y., Qi H., Ma Q., Xu L., Chen W., Chen G. and Xu X. (2013) A novel brain neurovascular unit model with neurons, astrocytes and microvascular endothelial cells of rat. Int. J. Biol. Sci. 9, 174–189.
48. Xue Q., Liu Y., He R., Yang S., Tong J., Li X., Chen Y. and Xu X. (2016) Lyophilized powder of catalpol and puerarin protects neurovascular unit from stroke. Int. J. Biol. Sci. 12, 367–380.
49. Yang C. M., Hsieh H. L., Yu P. H., Lin C. C. and Liu S. W. (2015) IL-1beta induces MMP-9-dependent brain astrocytic migration via transactivation of PDGF receptor/NADPH oxidase 2-derived reactive oxygen species signals. Mol. Neurobiol. 52, 303–317.
50. Young A. R., Ali C., Duretete A. and Vivien D. (2007) Neuroprotection and stroke: time for a compromise. J. Neurochem. 103, 1302–1309.
51. Zhang J. H., Badaut J., Tang J., Obenaus A., Hartman R. and Pearce W. J. (2012) The vascular neural network–a new paradigm in stroke pathophysiology. Nat. Rev. Neurol. 8, 711–716.
52. Zhu L., Han M. B., Gao Y., Wang H., Dai L., Wen Y. and Na L. X. (2015) Curcumin triggers apoptosis via upregulation of Bax/Bcl-2 ratio and caspase activation in SW872 human adipocytes. Mol. Med. Rep. 12, 1151–1156.
53. Zlokovic B. V. (2011) Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 12, 723–738.
54. Zonta M., Angulo M. C., Gobbo S., Rosengarten B., Hossmann K. A., Pozzan T. and Carmignoto G. (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci. 6, 43–50.