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Hot Water Extract of Wheat Bran Attenuates White Matter Injury in a Rat Model of Vascular Dementia

  • Lim, Sun Ha (Department of Biochemistry, Catholic University of Daegu School of Medicine) ;
  • Lee, Jongwon (Department of Biochemistry, Catholic University of Daegu School of Medicine)
  • Received : 2014.07.02
  • Accepted : 2014.09.16
  • Published : 2014.09.30

Abstract

Vascular dementia is characterized by white matter lesions involving the demyelination and activation of astrocytes and microglia. In a previous study, we showed that the supernatant of a laboratory-scale, hot water extract of ground whole wheat (TALE) attenuated white matter injury and astrocytic activation in a rat model of bilateral common carotid artery occlusion (BCCAO). In the present study, we made several modifications to the hot water extraction process to remove starch and enable large-scale production. We used wheat bran (WB), which contains less starch, instead of ground whole wheat. In addition, we removed starch granules with a decanter before hot water extraction. The final product, wheat bran extract (WBE), contained 2.42% arabinose, a surrogate marker of arabinoxylan, which is an active constituent of WBE. Supplementation of the rat model of BCCAO with WBE (400 mg/kg/day) for 33 days attenuated white matter injury, which was assessed by Luxol Fast Blue staining, in the corpus callosum (cc) and optic tract (opt) regions. Attenuation of white matter injury in the opt region was accompanied by improvement of the pupillary light reflex. Immunochemical staining revealed that supplementation with WBE reduced astrocytic activation in the cc and opt regions and reduced microglial activation in the opt region. These findings indicate that supplementation with WBE is effective at attenuating white matter injury accompanied by the inhibition of astrocytic and microglial activation. Therefore, extracts from WB, a cheap by-product of wheat milling, can be developed as a nutraceutical to prevent vascular dementia, a disease for which there is no approved pharmaceutical treatment.

Keywords

References

  1. Jellinger KA. 2013. Pathology and pathogenesis of vascular cognitive impairment-a critical update. Front Aging Neurosci 5: 17.
  2. Kalaria RN, Maestre GE, Arizaga R, Friedland RP, Galasko D, Hall K, Luchsinger JA, Ogunniyi A, Perry EK, Potocnik F, Prince M, Stewart R, Wimo A, Zhang ZX, Antuono P. 2008. Alzheimer's disease and vascular dementia in developing countries: prevalence, management, and risk factors. Lancet Neurol 7: 812-826. https://doi.org/10.1016/S1474-4422(08)70169-8
  3. Tomimoto H. 2011. Subcortical vascular dementia. Neurosci Res 71: 193-199. https://doi.org/10.1016/j.neures.2011.07.1820
  4. Roman GC, Erkinjuntti T, Wallin A, Pantoni L, Chui HC. 2002. Sucortical ischaemic vascular dementia. Lancet Neurol 1: 426-436. https://doi.org/10.1016/S1474-4422(02)00190-4
  5. Black S, Gao FQ, Bilbao J. 2009. Understanding white matter disease: imaging-pathological correlations in vascular cognitive impairment. Stroke 40: S48-S52. https://doi.org/10.1161/STROKEAHA.108.537704
  6. Thal DR, Grinberg LT, Attems J. 2012. Vascular dementia: different forms of vessel disorders contribute to the development of dementia in the elderly brain. Exp Gerontol 47: 816-824. https://doi.org/10.1016/j.exger.2012.05.023
  7. Baskys A, Cheng JX. 2012. Pharmacological prevention and treatment of vascular dementia: approaches and perspectives. Exp Gerontol 47: 887-891. https://doi.org/10.1016/j.exger.2012.07.002
  8. Jiwa NS, Garrard P, Hainsworth AH. 2010. Experimental models of vascular dementia and vascular cognitive impairment: a systematic review. J Neurochem 115: 814-828. https://doi.org/10.1111/j.1471-4159.2010.06958.x
  9. Kitamura A, Fujita Y, Oishi N, Kalaria RN, Washida K, Maki T, Okamoto Y, Hase Y, Yamada M, Takahashi J, Ito H, Tomimoto H, Fukuyama H, Takahashi R, Ihara M. 2012. Selective white matter abnormalities in a novel rat model of vascular dementia. Neurobiol Aging 33: 1012.e25-1012.e35. https://doi.org/10.1016/j.neurobiolaging.2011.10.033
  10. Farkas E, Luiten PGM, Bari F. 2007. Permanent, bilateral common carotid artery occlusion in the rat: A model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res Rev 54: 162-180. https://doi.org/10.1016/j.brainresrev.2007.01.003
  11. Hainsworth AH, Markus HS. 2008. Do in vivo experimental models reflect human cerebral small vessel disease? a systematic review. J Cereb Blood Flow Metab 28: 1877-1891. https://doi.org/10.1038/jcbfm.2008.91
  12. Dexter JE, Wood PJ. 1996. Recent applications of debranning of wheat before milling. Trends Food Sci Technol 7: 35-41. https://doi.org/10.1016/0924-2244(96)81326-4
  13. Shewry PR, Hawkesford MJ, Piironen V, Lampi AM, Gebruers K, Boros D, Andersson AAM, Aman P, Rakszegi M, Bedo Z, Ward JL. 2013. Natural variation in grain composition of wheat and related cereals. J Agric Food Chem 61: 8295-8303. https://doi.org/10.1021/jf3054092
  14. Guillon F, Tranquet O, Quillien L, Utille JP, Ortiz JJO, Saulnier L. 2004. Generation of polyclonal and monoclonal antibodies against arabinoxylans and their use for immunocytochemical location of arabinoxylans in cell walls of endosperm of wheat. J Cereal Sci 40: 167-182. https://doi.org/10.1016/j.jcs.2004.06.004
  15. Rosenfelder P, Eklund M, Mosenthin R. 2013. Nutritive value of wheat and wheat by-products in pig nutrition: A review. Animal Feed Sci Technol 185: 107-125. https://doi.org/10.1016/j.anifeedsci.2013.07.011
  16. Gebruers K, Dornez E, Bedo Z, Rakszegi M, Fras A, Boros D, Courtin CM, Delcour JA. 2010. Environment and genotype effects on the content of dietary fiber and its components in wheat in the HEALTHGRAIN diversity screen. J Agric Food Chem 58: 9353-9361. https://doi.org/10.1021/jf100447g
  17. Han HS, Jang JH, Jang JH, Choi JS, Kim YJ, Lee C, Lim SH, Lee HK, Lee JW. 2010. Water extract of Triticum aestivum L. and its components demonstrate protective effect in a model of vascular dementia. J Med Food 13: 572-578. https://doi.org/10.1089/jmf.2009.1242
  18. Goesaert H, Brijs K, Veraverbeke WS, Courtin CM, Gebruers K, Delcour JA. 2005. Wheat flour constituents: how they impact bread quality, and how to impact their functionality. Trends Food Sci Technol 16: 12-30. https://doi.org/10.1016/j.tifs.2004.02.011
  19. Sayaslan A. 2004. Wet-milling of wheat flour: industrial processes and small-scale test methods. LWT-Food Sci Technol 37: 499-515. https://doi.org/10.1016/j.lwt.2004.01.009
  20. KFDA. 2008. Korea Food Standards Codex. Korea Food and Drug Administration, Chungbuk, Korea.
  21. Melton LD, Smith BG. 2001. Determination of neutral sugars by gas chromatography of their alditol acetates. Current Protocols in Food Analytical Chemistry E3.2.1-E3.2.13.
  22. Stevens WD, Fortin T, Pappas BA. 2002. Retinal and optic degeneration after chronic carotid ligation: Time course and role of light exposure. Stroke 33: 1107-1112. https://doi.org/10.1161/01.STR.0000014204.05597.0C
  23. Paxinos G, Watson C. 1998. The Rat Brain in Stereotaxic Coordinates. 4th ed. Academic Press Inc, Orland, FL, USA. Figure 31.
  24. Pistorio AL, Hendry SH, Wang X. 2006. A modified technique for high-resolution staining of myelin. J Neurosci Methods 153: 135-146. https://doi.org/10.1016/j.jneumeth.2005.10.014
  25. Cho KO, La HO, Cho YJ, Sung KW, Kim SY. 2006. Minocycline attenuates white matter damage in a rat model of chronic cerebral hypoperfusion. J Neurosci Res 83: 285-291. https://doi.org/10.1002/jnr.20727
  26. Wakita H, Tomimoto H, Akiguchi I, Kimura J. 1994. Glial activation and white matter changes in the rat brain induced by chronic cerebral hypoperfusion: an immunohistochemistry. Acta Neuropathol 87: 484-492. https://doi.org/10.1007/BF00294175
  27. Milledge JJ, Heaven S. 2013. A review of the harvesting of micro-algae for biofuel production. Rev Environ Sci Biotechnol 12: 165-178. https://doi.org/10.1007/s11157-012-9301-z
  28. Pekny M, Wilhelmsson U, Pekna M. 2014. The dual role of astrocyte activation and reactive gliosis. Neurosci Lett 565: 30-38. https://doi.org/10.1016/j.neulet.2013.12.071
  29. Zhang D, Hu X, Qian L, O'Callaghan JP, Hong JS. 2010. Astrogliosis in CNS pathologies: is there a role for microglia? Mol Neurobiol 41: 232-241. https://doi.org/10.1007/s12035-010-8098-4
  30. Eng LF, Ghirnikar RS, Lee YL. 2000. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 25: 1439-1451. https://doi.org/10.1023/A:1007677003387
  31. Zielasek J, Hartung HP. 1996. Molecular mechanisms of microglial activation. Adv Neuroimmunol 6: 191-222. https://doi.org/10.1016/0960-5428(96)00017-4
  32. Imai Y, Kohsaka S. 2002. Intracellular signaling in M-CSFinduced microglia activation: role of Iba1. Glia 40: 164-174. https://doi.org/10.1002/glia.10149
  33. Ziebell JM, Adelson PD, Lifshitz J. 2014. Microglia: dismantling and rebuilding circuits after acute neurological injury. Metab Brain Dis DOI: 10.1007/s11011-014-9539-y.
  34. Sutherland K. 2009. Filtration and separation technology: what's new with centrifuges? Filtr Sep 46: 30-32.
  35. Swennen K, Courtin CM, Lindemans GCJE, Delcour JA. 2006. Large-scale production and characterization of wheat bran arabinoxylooligosaccharides. J Sci Food Agric 86: 1722-1731. https://doi.org/10.1002/jsfa.2470
  36. Zhou S, Liu X, Guo Y, Wang Q, Peng D, Cao L. 2010. Comparison of the immunological activities of arabinoxylans from wheat bran with alkali and xylanase-aided extraction. Carbohydr Polym 81: 784-789. https://doi.org/10.1016/j.carbpol.2010.03.040
  37. Davidson CM, Pappas BA, Stevens WD, Fortin T, Bennett SA. 2000. Chronic cerebral hypoperfusion: loss of pupillary reflex, visual impairment and retinal neurodegeneration. Brain Res 859: 96-103. https://doi.org/10.1016/S0006-8993(00)01937-5
  38. Minhas G, Morishita R, Anand A. 2012. Preclinical models to investigate retinal ischemia: advances and drawbacks. Front Neurol 3: 75.
  39. Weinstein JR, Koerner IP, Moller T. 2010. Microglia in ischemic brain injury. Future Neurol 5: 227-246. https://doi.org/10.2217/fnl.10.1
  40. Perry VH, Nicoll JAR, Holmes C. 2010. Microglia in neurodegenerative disease. Nat Rev Neurol 6: 193-201. https://doi.org/10.1038/nrneurol.2010.17
  41. Block ML, Zecca L, Hong JS. 2007. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8: 57-69. https://doi.org/10.1038/nrn2038
  42. Kawabori M, Yenari MA. 2014. The role of the microglia in acute CNS injury. Metab Brain Dis DOI: 10.1007/s11011-014-9531-6.
  43. Kim KK, Tsao R, Yang R, Cui SW. 2006. Phenolic acid profiles and antioxidant activities of wheat bran extracts and the effect of hydrolysis conditions. Food Chem 95: 466-473. https://doi.org/10.1016/j.foodchem.2005.01.032
  44. Xu Y, Zhang JJ, Xiong L, Zhang L, Sun D, Liu H. 2010. Green tea polyphenols inhibit impairment induced by chronic cerebral hypoperfusion via modulating oxidative stress. J Nutr Biochem 21: 741-748. https://doi.org/10.1016/j.jnutbio.2009.05.002
  45. Mota FL, Queimada AJ, Pinho SP, Macedo EA. 2008. Aqueous solubility of some natural phenolic compounds. Ind Eng Chem Res 47: 5182-5189. https://doi.org/10.1021/ie071452o

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