Borneol, a novel agent that improves central nervous system drug delivery by enhancing blood–brain barrier permeability

References

• Abbott NJ, Friedman A. (2012). Overview and introduction: the blood-brain barrier in health and disease. Epilepsia 53:1–6.
   PubMed Web of Science ®Google Scholar
• Abbruscato TJ, Lopez SP, Mark KS, et al. (2002). Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. J Pharm Sci 91:2525–38.
   PubMed Web of Science ®Google Scholar
• Ambudkar SV, Dey S, Hrycyna CA, et al. (1999). Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol 39:361–98.
   PubMed Web of Science ®Google Scholar
• Banks WA. (2009). Characteristics of compounds that cross the blood-brain barrier. BMC Neurol 9:S3.
   PubMed Web of Science ®Google Scholar
• Cai Z, Hou S, Li Y, et al. (2008). Effect of borneol on the distribution of gastrodin to the brain in mice via oral administration. J Drug Target 16:178–84.
   PubMed Web of Science ®Google Scholar
• Cai Z, Lei XL, Lin ZF, et al. (2014). Preparation and evaluation of sustained-release solid dispersions co-loading gastrodin with borneol as an oral brain-targeted enhancer. Acta Pharm Sin B 4:86–93.
   PubMed Web of Science ®Google Scholar
• Chen XH, Lin ZZ, Liu AM, et al. (2010). The orally combined neuroprotective effects of sodium ferulate and borneol against transient global ischaemia in C57 BL/6J mice. J Pharm Pharmacol 62:915–23.
   PubMed Web of Science ®Google Scholar
• Chen YM, Wang NS. (2004). Effect of borneol on the intercellular tight junction and pinocytosis vesicles in vitro blood-brain barrier model. Chin J Integr Tradit Western Med 24:632–4.
   Google Scholar
• Chen ZZ, Du SY, Lu Y, et al. (2014a). Mechanism research of aromatics borneol and muscone (Chinese). Zhong Yao Cai 37:460–4.
   PubMedGoogle Scholar
• Chen ZZ, Gong X, Lu Y, et al. (2014b). Enhancing effect of borneol and muscone on geniposide transport across the human nasal epithelial cell monolayer. PLoS One 9:e101414.
   PubMed Web of Science ®Google Scholar
• Chen ZZ, Lu Y, Du SY, et al. (2013). Influence of borneol and muscone on geniposide transport through MDCK and MDCK-MDR1 cells as blood-brain barrier in vitro model. Int J Pharm 456:73–9.
   PubMed Web of Science ®Google Scholar
• Cheng C, Liu XW, Du FF, et al. (2013). Sensitive assay for measurement of volatile borneol, isoborneol, and the metabolite camphor in rat pharmacokinetic study of Borneolum (Bingpian) and Borneolum syntheticum (synthetic Bingpian). Acta Pharmacol Sin 34:1337–48.
   PubMed Web of Science ®Google Scholar
• Cherneva E, Pavlovic V, Smelcerovic A, et al. (2012). The effect of camphor and borneol on rat thymocyte viability and oxidative stress. Molecules 17:10258–66.
   PubMed Web of Science ®Google Scholar
• Cohen Z, Bonvento G, Lacombe P, et al. (1996). Serotonin in the regulation of brain microcirculation. Prog Neurobiol 50:335–62.
   PubMed Web of Science ®Google Scholar
• Dai JP, Chen J, Bei YF, et al. (2009). Influence of borneol on primary mice oral fibroblasts: a penetration enhancer may be used in oral submucous fibrosis. J Oral Pathol Med 38:276–81.
   PubMed Web of Science ®Google Scholar
• Denora N, Trapani A, Laquintana V, et al. (2009). Recent advances in medicinal chemistry and pharmaceutical technology-strategies for drug delivery to the brain. Curr Top Med Chem 9:182–96.
   PubMed Web of Science ®Google Scholar
• Dong XP, Ruan M, Yu B, et al. (2012). Effects of borneol at different doses on concentration of geniposide in rat brains. Chin Tradi Herb Drugs 43:1366–70.
   Google Scholar
• Fan X, Chai LJ, Zhang H, et al. (2015). Borneol depresses P-glycoprotein function by a NF-kappa B signaling mediated mechanism in a blood brain barrier in vitro model. Int J Mol Sci 16:27576–88.
   PubMed Web of Science ®Google Scholar
• Fu BM. (2012). Experimental methods and transport models for drug delivery across the blood-brain barrier. Curr Pharm Biotech 13:1346–59.
   PubMed Web of Science ®Google Scholar
• Gao C, Li X, Li Y, et al. (2010). Pharmacokinetic interaction between puerarin and edaravone, and effect of borneol on the brain distribution kinetics of puerarin in rats. J Pharm Pharmacol 62:360–7.
   PubMed Web of Science ®Google Scholar
• Granger RE, Campbell EL, Johnston GA. (2005). (+)- And (−)-borneol: efficacious positive modulators of GABA action at human recombinant alpha1beta2gamma2L GABA(A) receptors. Biochem Pharmacol 69:1101–11.
   PubMed Web of Science ®Google Scholar
• Horváthová E, Slameňová D, Maršálková L, et al. (2009). Effects of borneol on the level of DNA damage induced in primary rat hepatocytes and testicular cells by hydrogen peroxide. Food Chem Toxicol 47:1318–23.
   PubMed Web of Science ®Google Scholar
• Hu L, Chen DY. (2009). Application of headspace solid phase microextraction for study of noncovalent interaction of borneol with human serum albumin. Acta Pharmacol Sin 30:1573–6.
   PubMed Web of Science ®Google Scholar
• Huang P, Jiang XF, Zou JL, et al. (2009). A novel GC–MS bioanalytical method for natural borneol and its application in investigating natural borneol distribution in mice mode. Tradit Chin Med Mater Med 11:821–7.
   Google Scholar
• Jiang XF, Zou JL, Yuan YM, et al. (2008). Preliminary study: biotransformation of borneol to camphor in mice, rats, and rabbits. Mode Tradit Chin Med Mater Med 10:27–36.
   Google Scholar
• Jin D, Wang F, Qu L, et al. (2011). The distribution and expression of claudin-5 and occludin at the rat blood-optic nerve barrier after borneol treatment. Mol Biol Rep 38:913–20.
   PubMed Web of Science ®Google Scholar
• Kröncke KD, Fehsel K, Kolb-Bachofen V. (1998). Inducible nitric oxide synthase in human diseases. Clin Exp Immunol 113:147–56.
   PubMed Web of Science ®Google Scholar
• Li WR, Chen RW, Yang L, et al. (2012). Pharmacokinetics of natural borneol after oral administration in mice brain and its effect on excitation ratio. Eur J Drug Metab Pharmacokinet 37:39–44.
   PubMed Web of Science ®Google Scholar
• Li WR, Yao LM, Mi SQ, et al. (2004). The effect of borneol on level of histamine and 5-hydroxytryptamine in rat's hypothalamus. J Chin Med Mater 27:937–9.
   Google Scholar
• Li WR, Yao LM, Mi SQ, et al. (2006). Relation of openness of blood-brain barrier by borneol with histamine and 5-hydroxytryptamine. J Clin Rehab Tissue Eng Res 10:167–9.
   Google Scholar
• Liang MR, Liu QD, Huang TL, et al. (1993). The pharmacokinetic characteristics of borneol in serum and brain tissue of rats (Chinese). Tradit Chin Drug Res Clin Pharmacol 4:38–41.
   Google Scholar
• Liu YD, Sun HJ, Li R, et al. (2008). Influence of borneol on nasal absorption of Ligustrazine (Chinese). Chin J Chin Mater Med 33:259–61.
   Google Scholar
• Löscher W, Potschka H. (2005). Blood-brain barrier active efflux transporters: ATP-binding cassette gene family. NeuroRx 2:86–98.
   PubMedGoogle Scholar
• Lu Y, Du SY, Bai J, et al. (2012). Bioavailability and brain-targeting of geniposide in gardenia-borneol co-compound by different administration routes in mice. Int J Mol Sci 13:14127–35.
   PubMed Web of Science ®Google Scholar
• Meng W, Tobin JR, Busija DW. (1995). Glutamate-induced cerebral vasodilation is mediated by nitric oxide through N-methyl-D-aspartate receptors. Stroke 26:857–62.
   PubMed Web of Science ®Google Scholar
• Neuhaus W, Freidl M, Szkokan P, et al. (2011). Effects of NMDA receptor modulators on a blood-brain barrier in vitro model. Brain Res 1394:49–61.
   PubMed Web of Science ®Google Scholar
• Ni CX, Zeng N, Xu FH, et al. (2011). Effects of aromatic resuscitation drugs on blood brain barrier in cerebral ischemia-reperfusion injury model rats (Chinese). Chin J Chin Mater Med 36:2562–6.
   Google Scholar
• Pardridge WM. (2005). The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2:3–14.
   PubMedGoogle Scholar
• Paris L, Tonutti L, Vannini C, et al. (2008). Structural organization of the tight junctions. Biochim Biophys Acta 1778:646–59.
   PubMed Web of Science ®Google Scholar
• Park TJ, Park YS, Lee TG, et al. (2003). Inhibition of acetylcholine-mediated effects by borneol. Biochem Pharmacol 65:83–90.
   PubMed Web of Science ®Google Scholar
• Perloff MD, Störmer E, von Moltke LL, et al. (2003). Rapid assessment of P-glycoprotein inhibition and induction in vitro. Pharm Res 20:1177–83.
   PubMed Web of Science ®Google Scholar
• Ren JG, Zou MJ, Gao P, et al. (2013). Tissue distribution of borneol-modified ganciclovir-loaded solid lipid nanoparticles in mice after intravenous administration. Eur J Pharm Biopharm 83:141–8.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Boulan E, Kreitzer G, Müsch A. (2005). Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6:233–47.
   PubMed Web of Science ®Google Scholar
• Sarker MH, Easton AS, Fraser PA. (1998). Regulation of cerebral microvascular permeability by histamine in the anaesthetized rat. J Physiol 507:909–18.
   PubMed Web of Science ®Google Scholar
• Saunders NR, Dziegielewska KM, Møllgård K, et al. (2015). Markers for blood-brain barrier integrity: how appropriate is Evans blue in the twenty-first century and what are the alternatives? Front Neurosci 9:385.
   PubMed Web of Science ®Google Scholar
• Shi L, Zeng M, Fu BM. (2014a). Temporal effects of vascular endothelial growth factor and 3,5-cyclic monophosphate on blood-brain barrier permeability in vivo. J Neurosci Res 92:1678–89.
   PubMed Web of Science ®Google Scholar
• Shi L, Palacio-Mancheno P, Badami J, et al. (2014b). Quantification of transient increase of the blood-brain barrier permeability to macromolecules by optimized focused ultrasound combined with microbubbles. Int J Nanomed 9:4437–48.
   PubMed Web of Science ®Google Scholar
• Slameňová D, Horváthová E, Maršálková L, et al. (2009). Investigation of anti-oxidative, cytotoxic, DNA-damaging and DNA-protective effects of plant volatiles eugenol and borneol in human-derived HepG2, Caco-2 and VH10 cell lines. Mutat Res 677:46–52.
   PubMed Web of Science ®Google Scholar
• Song X, Lu Y, Wen R, et al. (2012). In situ and in vivo study of nasal absorption of borneol in rats. Pharmazie 67:848–51.
   PubMed Web of Science ®Google Scholar
• State Pharmacopoeia Committee. (2015). The Pharmacopoeia of People's Republic of China. Beijing: China Medical Science Press.
   Google Scholar
• Tang B, Fang GH, Gao Y, et al. (2015). Co-encapsulation of borneol and paclitaxel by liprosomes improved anti-tumor effect in a xenografted glioma model. RSC Adv 5:106613–20.
   Web of Science ®Google Scholar
• Wang LP, Feng JF, Hu KL. (2014). Progress in regulation effect of aromatic refreshing traditional Chinese medicine on BBB permeability and its mechanism (in Chinese). Zhongguo Zhong Yao Za Zhi 39:949–54.
   PubMedGoogle Scholar
• Wang NS, Xie D, Liang MR, et al. (1992). A dynamic computed tomographic (CT) study on effects of borneol on the blood-brain barrier in rabbits (Chinese). Tradit Chin Drug Res Clin Pharmacol 3:28–31.
   Google Scholar
• Wang YH, Tian HY, Wang AM, et al. (2014). A green and solvent-free process for preparation of high-purity (–)-borneol from leaves of Blumea balsamifera (L.) DC. Trop J Pharm Res 13:41–6.
   Web of Science ®Google Scholar
• Wu C, Liao Q, Yao M, et al. (2014). Effect of natural borneol on the pharmacokinetics and distribution of nimodipine in mice. Eur J Drug Metab Pharmacokinet 39:17–24.
   PubMed Web of Science ®Google Scholar
• Wu SR, Cheng G, He YX, et al. (2004). Studies on the effects of borneol on the distribution of rifampicin in mice (Chinese). Chin Pharm J 39:289–91.
   Google Scholar
• Xian JW, Chan CW, Leung WN, et al. (2013). Borneol enhanced permeability of levodopa across blood-brain barrier _ Potential to lower levodopa dosage for Parkinson’s disease treatment. The 11th International Conference on Alzheimer’s and Parkinson’s Diseases and Related Neurological Disorders (AD/PDTM 2013), 2013, 288 p.
   Google Scholar
• Xiao YY, Ping QN, Chen ZP. (2007). The enhancing effect of synthetic borneol on the absorption of tetramethylpyrazine phosphate in mouse. Int J Pharm 337:74–9.
   PubMed Web of Science ®Google Scholar
• Xiao YY, Ping QN, Chen ZP. (2008). A simple gas chromatographic method for the simultaneous determination and pharmacokinetic study of tetramethylpyrazine phosphate and borneol in mouse plasma and brain tissue after oral Administration of the fufang tetramethylpyrazine phosphate tablets. J Chromatogr Sci 46:395–400.
   PubMed Web of Science ®Google Scholar
• Xin HL, He XR, Li W, et al. (2014). The effect of borneol on the concentration of meropenem in rat brain and blood. J Asian Nat Prod Res 16:648–57.
   PubMed Web of Science ®Google Scholar
• Xiong ZY, Xiao FM, Xu X, et al. (2013). Studies on pharmacological activity of borneol (Chinese). Zhongguo Zhong Yao Za Zhi 38:786–90.
   PubMedGoogle Scholar
• Xu XL, Li JJ, Han SP, et al. (2016). A novel doxorubicin loaded folic acid conjugated PAMAM modified with borneol, a nature dual-functional product of reducing PAMAM toxicity and boosting BBB penetration. Eur J Pharmaceutical Sci 88:178–90.
   PubMed Web of Science ®Google Scholar
• Yang H, Xun Y, Li Z, et al. (2009). Influence of borneol on in vitro corneal permeability and on in vivo and in vitro corneal toxicity. J Int Med Res 37:791–802.
   PubMed Web of Science ®Google Scholar
• Yu B, Lu GH, Sun Y, et al. (2011a). Effect of electroacupuncture combined with intragastric administration of borneol on the permeability of blood-brain barrier in the mouse. Zhen Ci Yan Jiu 36:335–40.
   PubMedGoogle Scholar
• Yu B, Ruan M, Sun Y, et al. (2011b). Effect of borneol and electroacupuncture on the distribution of hyperforin in the rat brain. Neural Regen Res 6:1876–82.
   Web of Science ®Google Scholar
• Yu B, Ruan M, Cui XB, et al. (2013a). Effects of borneol on the pharmacokinetics of geniposide in cortex, hippocampus, hypothalamus and striatum of conscious rat by simultaneous brain microdialysis coupled with UPLC–MS. J Pharm Biomed Anal 77:128–32.
   PubMed Web of Science ®Google Scholar
• Yu B, Ruan M, Dong XP, et al. (2012). The influence of borneol treatment interval on the concentration of geniposide in rat brains. Chin Pharmacol Bull 28:862–6.
   Google Scholar
• Yu B, Ruan M, Dong XP, et al. (2013b). The mechanism of the opening of the blood–brain barrier by borneol: a pharmacodynamics and pharmacokinetics combination study. J Ethnopharmacol 150:1096–108.
   PubMed Web of Science ®Google Scholar
• Yu B, Ruan M, Zhang ZN, et al. (2016). Synergic effect of borneol and igustrazine on the neuroprotection in global cerebral ischemia/reperfusion injury: a Region-Specificity Study. Evid Based Complement Alternat Med 2016:4072809.
   PubMed Web of Science ®Google Scholar
• Zeng CQ, He GF. (2004). Analysis of ten batches of borneol on market by GC-MS. J Chin Med Mater 27:347.
   Google Scholar
• Zhai ZH, Shen Q. (2010). Progress in research on the effects of borneol on drug absorption (Chinese). Chin Med J Res Prac 24:86–8.
   Google Scholar
• Zhang CY, Zhao P, Shi Z, et al. (2011). Effects of herbal aromatics on the permeability of MDCK-MDR1 monolayers. J Chin Pharm Sci 20:584–9.
   Google Scholar
• Zhang L, Han L, Qin J, et al. (2013). The use of borneol as an enhancer for targeting aprotinin-conjugated PEG-PLGA nanoparticles to the brain. Pharm Res 30:2560–72.
   PubMed Web of Science ®Google Scholar
• Zhang N, Liu P, He XR. (2012). Effect of borneol, moschus, storax, and acorus tatarinowii on expression levels of four amino acid neurotransmitters in the rat corpus striatum. Neural Regen Res 7:440–4.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Wu D, Wu J, et al. (2015). Improved blood-brain barrier distribution: effect of borneol on the brain pharmacokinetics of kaempferol in rats by in vivo microdialysis sampling. J Ethnopharmacol 162:270–7.
   PubMed Web of Science ®Google Scholar
• Zhao BS, Liu QD. (2002). Comparison between borneol-induced opening of blood-brain barrier and its pathological opening. Tradit Chin Drug Res Clin Pharmacol 13:287–8.
   Google Scholar
• Zhao JY, Lu Y, Du SY, et al. (2012). Comparative pharmacokinetic studies of borneol in mouse plasma and brain by different administrations. J Zhejiang Univ Sci B 13:990–6.
   PubMed Web of Science ®Google Scholar