Nutrition Research and Practice

  • 제14권3호
  • /
  • Pages.188-202
  • /
  • 2020
  • /
  • 1976-1457(pISSN)
  • /
  • 2005-6168(eISSN)
한국영양학회 (The Korean Nutrition Society)
권호 표지
DOI QR코드

DOI QR Code

L-histidine and L-carnosine exert anti-brain aging effects in D-galactose-induced aged neuronal cells

  • Kim, Yerin (Department of Nutritional Science and Food Management, Ewha Womans University) ;
  • Kim, Yuri (Department of Nutritional Science and Food Management, Ewha Womans University)
  • 투고 : 2019.09.06
  • 심사 : 2019.11.06
  • 발행 : 2020.06.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

BACKGROUND/OBJECTIVES: Brain aging is a major risk factor for severe neurodegenerative diseases. Conversely, L-histidine and L-carnosine are known to exhibit neuroprotective effects. The aim of this study was to examine the potential for L-histidine, L-carnosine, and their combination to mediate anti-brain aging effects in neuronal cells subjected to D-galactose-induced aging. MATERIALS/METHODS: The neuroprotective potential of L-histidine, L-carnosine, and their combination was examined in a retinoic acid-induced neuronal differentiated SH-SY5Y cell line exposed to D-galactose (200 mM) for 48 h. Neuronal cell proliferation, differentiation, and expression of anti-oxidant enzymes and apoptosis markers were subsequently evaluated. RESULTS: Treatment with L-histidine (1 mM), L-carnosine (10 mM), or both for 48 h efficiently improved the proliferation, neurogenesis, and senescence of D-galactose-treated SH-SY5Y cells. In addition, protein expression levels of both neuronal markers (β tubulin-III and neurofilament heavy protein) and anti-oxidant enzymes, glutathione peroxidase-1 and superoxide dismutase-1 were up-regulated. Conversely, protein expression levels of amyloid β (1-42) and cleaved caspase-3 were down-regulated. Levels of mRNA for the pro-inflammatory cytokines, interleukin (IL)-8, IL-1β, and tumor necrosis factor-α were also down-regulated. CONCLUSIONS: To the best of our knowledge, we provide the first evidence that L-histidine, L-carnosine, and their combination mediate anti-aging effects in a neuronal cell line subjected to D-galactose-induced aging. These results suggest the potential benefits of L-histidine and L-carnosine as anti-brain aging agents and they support further research of these amino acid molecules.

키워드

참고문헌

  1. Gandhi S, Abramov AY. Mechanism of oxidative stress in neurodegeneration. Oxid Med Cell Longev 2012;2012:428010. https://doi.org/10.1155/2012/428010
  2. Mattson MP, Magnus T. Ageing and neuronal vulnerability. Nat Rev Neurosci 2006;7:278-94. https://doi.org/10.1038/nrn1886
  3. Ohnuma S, Harris WA. Neurogenesis and the cell cycle. Neuron 2003;40:199-208. https://doi.org/10.1016/S0896-6273(03)00632-9
  4. Khodosevich K, Monyer H. Signaling involved in neurite outgrowth of postnatally born subventricular zone neurons in vitro. BMC Neurosci 2010;11:18. https://doi.org/10.1186/1471-2202-11-18
  5. Park MH, Son DJ, Nam KT, Kim SY, Oh SY, Song MJ, Chun HO, Lee TH, Hong JT. PRDX6 inhibits neurogenesis of neural precursor cells through downregulation of wdfy1 mediated TLR4 signal. bioRxivorg. Forthcoming 2016.
  6. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000;408:239-47. https://doi.org/10.1038/35041687
  7. Zhang YW, Thompson R, Zhang H, Xu H. APP processing in Alzheimer's disease. Mol Brain 2011;4:3. https://doi.org/10.1186/1756-6606-4-3
  8. Yin F, Sancheti H, Patil I, Cadenas E. Energy metabolism and inflammation in brain aging and Alzheimer's disease. Free Radic Biol Med 2016;100:108-22. https://doi.org/10.1016/j.freeradbiomed.2016.04.200
  9. Tha KK, Okuma Y, Miyazaki H, Murayama T, Uehara T, Hatakeyama R, Hayashi Y, Nomura Y. Changes in expressions of proinflammatory cytokines IL-1beta, TNF-alpha and IL-6 in the brain of senescence accelerated mouse (SAM) P8. Brain Res 2000;885:25-31. https://doi.org/10.1016/S0006-8993(00)02883-3
  10. McLarnon JG. Chemokine interleukin-8 (IL-8) in Alzheimer's and other neurodegenerative diseases. J Alzheimers Dis Parkinsonism 2016;6:273. https://doi.org/10.4172/2161-0460.1000273
  11. Song X, Bao M, Li D, Li YM. Advanced glycation in D-galactose induced mouse aging model. Mech Ageing Dev 1999;108:239-51. https://doi.org/10.1016/S0047-6374(99)00022-6
  12. Lu J, Zheng YL, Luo L, Wu DM, Sun DX, Feng YJ. Quercetin reverses D-galactose induced neurotoxicity in mouse brain. Behav Brain Res 2006;171:251-60. https://doi.org/10.1016/j.bbr.2006.03.043
  13. Shwe T, Pratchayasakul W, Chattipakorn N, Chattipakorn SC. Role of D-galactose-induced brain aging and its potential used for therapeutic interventions. Exp Gerontol 2018;101:13-36. https://doi.org/10.1016/j.exger.2017.10.029
  14. Shen Y, Gao H, Shi X, Wang N, Ai D, Li J, Ouyang L, Yang J, Tian Y, Lu J. Glutamine synthetase plays a role in D-galactose-induced astrocyte aging in vitro and in vivo. Exp Gerontol 2014;58:166-73. https://doi.org/10.1016/j.exger.2014.08.006
  15. Hsieh HM, Wu WM, Hu ML. Genistein attenuates D-galactose-induced oxidative damage through decreased reactive oxygen species and $NF-{\kappa}B$ binding activity in neuronal PC12 cells. Life Sci 2011;88:82-8. https://doi.org/10.1016/j.lfs.2010.10.021
  16. Liu YY, Nagpure BV, Wong PT, Bian JS. Hydrogen sulfide protects SH-SY5Y neuronal cells against d-galactose induced cell injury by suppression of advanced glycation end products formation and oxidative stress. Neurochem Int 2013;62:603-9. https://doi.org/10.1016/j.neuint.2012.12.010
  17. Heidari S, Mehri S, Shariaty V, Hosseinzadeh H. Preventive effects of crocin on neuronal damages induced by D-galactose through AGEs and oxidative stress in human neuroblastoma cells (SH-SY5Y). J Pharmacopuncture 2018;21:18-25. https://doi.org/10.3831/KPI.2018.21.003
  18. Rassin DK. Essential and non-essential amino acids in neonatal nutrition. Nestle Nutr Workshop Ser 1994;33:183-95.
  19. Cai Q, Takemura G, Ashraf M. Antioxidative properties of histidine and its effect on myocardial injury during ischemia/reperfusion in isolated rat heart. J Cardiovasc Pharmacol 1995;25:147-55. https://doi.org/10.1097/00005344-199501000-00023
  20. Matheson IB, Lee J. Chemical reaction rates of amino acids with singlet oxygen. Photochem Photobiol 1979;29:879-81. https://doi.org/10.1111/j.1751-1097.1979.tb07786.x
  21. Edwards C, Canfield J, Copes N, Brito A, Rehan M, Lipps D, Brunquell J, Westerheide SD, Bradshaw PC. Mechanisms of amino acid-mediated lifespan extension in Caenorhabditis elegans. BMC Genet 2015;16:8. https://doi.org/10.1186/s12863-015-0167-2
  22. Adachi N, Liu K, Arai T. Prevention of brain infarction by postischemic administration of histidine in rats. Brain Res 2005;1039:220-3. https://doi.org/10.1016/j.brainres.2005.01.061
  23. Liao RJ, Jiang L, Wang RR, Zhao HW, Chen Y, Li Y, Wang L, Jie LY, Zhou YD, Zhang XN, Chen Z, Hu WW. Histidine provides long-term neuroprotection after cerebral ischemia through promoting astrocyte migration. Sci Rep 2015;5:15356. https://doi.org/10.1038/srep15356
  24. Rama Rao KV, Reddy PV, Tong X, Norenberg MD. Brain edema in acute liver failure: inhibition by L-histidine. Am J Pathol 2010;176:1400-8. https://doi.org/10.2353/ajpath.2010.090756
  25. Farshid AA, Tamaddonfard E, Najafi S. Effects of histidine and n-acetylcysteine on experimental lesions induced by doxorubicin in sciatic nerve of rats. Drug Chem Toxicol 2015;38:436-41. https://doi.org/10.3109/01480545.2014.981753
  26. Ruszkiewicz J, Albrecht J. Changes of the thioredoxin system, glutathione peroxidase activity and total antioxidant capacity in rat brain cortex during acute liver failure: modulation by L-histidine. Neurochem Res 2015;40:293-300. https://doi.org/10.1007/s11064-014-1417-9
  27. Pichili VB, Rao KV, Jayakumar AR, Norenberg MD. Inhibition of glutamine transport into mitochondria protects astrocytes from ammonia toxicity. Glia 2007;55:801-9. https://doi.org/10.1002/glia.20499
  28. Kohen R, Yamamoto Y, Cundy KC, Ames BN. Antioxidant activity of carnosine, homocarnosine, and anserine present in muscle and brain. Proc Natl Acad Sci U S A 1988;85:3175-9. https://doi.org/10.1073/pnas.85.9.3175
  29. Yuneva AO, Kramarenko GG, Vetreshchak TV, Gallant S, Boldyrev AA. Effect of carnosine on Drosophila melanogaster lifespan. Bull Exp Biol Med 2002;133:559-61. https://doi.org/10.1023/a:1020273506970
  30. Gallant S, Semyonova M, Yuneva M. Carnosine as a potential anti-senescence drug. Biochemistry (Mosc) 2000;65:866-8.
  31. Shen Y, Hu WW, Fan YY, Dai HB, Fu QL, Wei EQ, Luo JH, Chen Z. Carnosine protects against NMDAinduced neurotoxicity in differentiated rat PC12 cells through carnosine-histidine-histamine pathway and H(1)/H(3) receptors. Biochem Pharmacol 2007;73:709-17. https://doi.org/10.1016/j.bcp.2006.11.007
  32. Mizuno D, Konoha-Mizuno K, Mori M, Sadakane Y, Koyama H, Ohkawara S, Kawahara M. Protective activity of carnosine and anserine against zinc-induced neurotoxicity: a possible treatment for vascular dementia. Metallomics 2015;7:1233-9. https://doi.org/10.1039/c5mt00049a
  33. Zhang L, Yao K, Fan Y, He P, Wang X, Hu W, Chen Z. Carnosine protects brain microvascular endothelial cells against rotenone-induced oxidative stress injury through histamine $H_{1}$ and $H_{2}$ receptors in vitro. Clin Exp Pharmacol Physiol 2012;39:1019-25. https://doi.org/10.1111/1440-1681.12019
  34. Preston JE, Hipkiss AR, Himsworth DT, Romero IA, Abbott JN. Toxic effects of beta-amyloid(25-35) on immortalised rat brain endothelial cell: protection by carnosine, homocarnosine and beta-alanine. Neurosci Lett 1998;242:105-8. https://doi.org/10.1016/S0304-3940(98)00058-5
  35. Zhang ZY, Sun BL, Yang MF, Li DW, Fang J, Zhang S. Carnosine attenuates early brain injury through its antioxidative and anti-apoptotic effects in a rat experimental subarachnoid hemorrhage model. Cell Mol Neurobiol 2015;35:147-57. https://doi.org/10.1007/s10571-014-0106-1
  36. Herculano B, Tamura M, Ohba A, Shimatani M, Kutsuna N, Hisatsune T. ${\beta}$-alanyl-L-histidine rescues cognitive deficits caused by feeding a high fat diet in a transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 2013;33:983-97. https://doi.org/10.3233/JAD-2012-121324
  37. Flancbaum L, Fitzpatrick JC, Brotman DN, Marcoux AM, Kasziba E, Fisher H. The presence and significance of carnosine in histamine-containing tissues of several mammalian species. Agents Actions 1990;31:190-6. https://doi.org/10.1007/bf01997607
  38. Park S, Kim J, Kim Y. Mulberry leaf extract inhibits cancer cell stemness in neuroblastoma. Nutr Cancer 2012;64:889-98. https://doi.org/10.1080/01635581.2012.707280
  39. Teunissen CE, Khalil M. Neurofilaments as biomarkers in multiple sclerosis. Mult Scler 2012;18:552-6. https://doi.org/10.1177/1352458512443092
  40. Draberova E, Del Valle L, Gordon J, Markova V, Smejkalova B, Bertrand L, de Chadarevian JP, Agamanolis DP, Legido A, Khalili K, Draber P, Katsetos CD. Class III ${\beta}$-tubulin is constitutively coexpressed with glial fibrillary acidic protein and nestin in midgestational human fetal astrocytes: implications for phenotypic identity. J Neuropathol Exp Neurol 2008;67:341-54. https://doi.org/10.1097/NEN.0b013e31816a686d
  41. Cho S, Hwang ES. Fluorescence-based detection and quantification of features of cellular senescence. Methods Cell Biol 2011;103:149-88. https://doi.org/10.1016/B978-0-12-385493-3.00007-3
  42. Mattson MP, Arumugam TV. Hallmarks of brain aging: adaptive and pathological modification by metabolic states. Cell Metab 2018;27:1176-99. https://doi.org/10.1016/j.cmet.2018.05.011
  43. Godbout JP, Johnson RW. Age and neuroinflammation: a lifetime of psychoneuroimmune consequences. Immunol Allergy Clin North Am 2009;29:321-37. https://doi.org/10.1016/j.iac.2009.02.007
  44. Rea IM, Gibson DS, McGilligan V, McNerlan SE, Alexander HD, Ross OA. Age and age-related diseases: role of inflammation triggers and cytokines. Front Immunol 2018;9:586. https://doi.org/10.3389/fimmu.2018.00586
  45. Pardridge WM. Blood-brain barrier transport of nutrients. Nutr Rev 1986;44 Suppl:15-25. https://doi.org/10.1111/j.1753-4887.1986.tb07674.x
  46. Ohtsuki S, Terasaki T. Contribution of carrier-mediated transport systems to the blood-brain barrier as a supporting and protecting interface for the brain; importance for CNS drug discovery and development. Pharm Res 2007;24:1745-58. https://doi.org/10.1007/s11095-007-9374-5
  47. Keep RF, Smith DE. Chapter 198-oligopeptide transport at the blood-brain and blood-CSF barriers. In: Kastin AJ, editor. Handbook of Biologically Active Peptides. Amsterdam; Academic Press; 2006. p.1423-28.
  48. Zlokovic BV. Cerebrovascular permeability to peptides: manipulations of transport systems at the bloodbrain barrier. Pharm Res 1995;12:1395-406. https://doi.org/10.1023/A:1016254514167
  49. Sasahara I, Fujimura N, Nozawa Y, Furuhata Y, Sato H. The effect of histidine on mental fatigue and cognitive performance in subjects with high fatigue and sleep disruption scores. Physiol Behav 2015;147:238-44. https://doi.org/10.1016/j.physbeh.2015.04.042
  50. Yoshikawa T, Nakamura T, Shibakusa T, Sugita M, Naganuma F, Iida T, Miura Y, Mohsen A, Harada R, Yanai K. Insufficient intake of L-histidine reduces brain histamine and causes anxiety-like behaviors in male mice. J Nutr 2014;144:1637-41. https://doi.org/10.3945/jn.114.196105
  51. Aydin AF, Coban J, Dogan-Ekici I, Betul-Kalaz E, Dogru-Abbasoglu S, Uysal M. Carnosine and taurine treatments diminished brain oxidative stress and apoptosis in D-galactose aging model. Metab Brain Dis 2016;31:337-45. https://doi.org/10.1007/s11011-015-9755-0
  52. Banerjee S, Poddar MK. Carnosine: effect on aging-induced increase in brain regional monoamine oxidase-A activity. Neurosci Res 2015;92:62-70. https://doi.org/10.1016/j.neures.2014.09.009
  53. Davinelli S, Di Marco R, Bracale R, Quattrone A, Zella D, Scapagnini G. Synergistic effect of L-Carnosine and EGCG in the prevention of physiological brain aging. Curr Pharm Des 2013;19:2722-7. https://doi.org/10.2174/1381612811319150007
  54. Boldyrev AA, Aldini G, Derave W. Physiology and pathophysiology of carnosine. Physiol Rev 2013;93:1803-45. https://doi.org/10.1152/physrev.00039.2012
  55. Decker EA, Livisay SA, Zhou S. A re-evaluation of the antioxidant activity of purified carnosine. Biochemistry (Mosc) 2000;65:766-70.
  56. Babizhayev MA, Seguin MC, Gueyne J, Evstigneeva RP, Ageyeva EA, Zheltukhina GA. L-carnosine (betaalanyl-L-histidine) and carcinine (beta-alanylhistamine) act as natural antioxidants with hydroxyl-radicalscavenging and lipid-peroxidase activities. Biochem J 1994;304:509-16. https://doi.org/10.1042/bj3040509
  57. Canonaco M, Madeo M, Alo R, Giusi G, Granata T, Carelli A, Canonaco A, Facciolo RM. The histaminergic signaling system exerts a neuroprotective role against neurodegenerative-induced processes in the hamster. J Pharmacol Exp Ther 2005;315:188-95. https://doi.org/10.1124/jpet.105.088153
  58. Hiraga N, Adachi N, Liu K, Nagaro T, Arai T. Suppression of inflammatory cell recruitment by histamine receptor stimulation in ischemic rat brains. Eur J Pharmacol 2007;557:236-44. https://doi.org/10.1016/j.ejphar.2006.11.020
  59. Fu Q, Dai H, Hu W, Fan Y, Shen Y, Zhang W, Chen Z. Carnosine protects against Abeta42-induced neurotoxicity in differentiated rat PC12 cells. Cell Mol Neurobiol 2008;28:307-16. https://doi.org/10.1007/s10571-007-9235-0
  60. Bae ON, Majid A. Role of histidine/histamine in carnosine-induced neuroprotection during ischemic brain damage. Brain Res 2013;1527:246-54. https://doi.org/10.1016/j.brainres.2013.07.004
  61. Attanasio F, Convertino M, Magno A, Caflisch A, Corazza A, Haridas H, Esposito G, Cataldo S, Pignataro B, Milardi D, Rizzarelli E. Carnosine inhibits $A{\beta}$(42) aggregation by perturbing the H-bond network in and around the central hydrophobic cluster. ChemBioChem 2013;14:583-92. https://doi.org/10.1002/cbic.201200704
  62. Thinakaran G, Koo EH. Amyloid precursor protein trafficking, processing, and function. J Biol Chem 2008;283:29615-9. https://doi.org/10.1074/jbc.R800019200
  63. Gralle M, Botelho MG, Wouters FS. Neuroprotective secreted amyloid precursor protein acts by disrupting amyloid precursor protein dimers. J Biol Chem 2009;284:15016-25. https://doi.org/10.1074/jbc.M808755200
  64. Yang WN, Han H, Hu XD, Feng GF, Qian YH. The effects of perindopril on cognitive impairment induced by d-galactose and aluminum trichloride via inhibition of acetylcholinesterase activity and oxidative stress. Pharmacol Biochem Behav 2013;114-115:31-6. https://doi.org/10.1016/j.pbb.2013.10.027
  65. Li JJ, Zhu Q, Lu YP, Zhao P, Feng ZB, Qian ZM, Zhu L. Ligustilide prevents cognitive impairment and attenuates neurotoxicity in D-galactose induced aging mice brain. Brain Res 2015;1595:19-28. https://doi.org/10.1016/j.brainres.2014.10.012
  66. Wade AM, Tucker HN. Antioxidant characteristics of L-histidine. J Nutr Biochem 1998;9:308-15. https://doi.org/10.1016/S0955-2863(98)00022-9
  67. Ruszkiewicz J, Fresko I, Hilgier W, Albrecht J. Decrease of glutathione content in the prefrontal cortical mitochondria of rats with acute hepatic encephalopathy: prevention by histidine. Metab Brain Dis 2013;28:11-4. https://doi.org/10.1007/s11011-012-9342-6
  68. Han CH, Lin YS, Lee TL, Liang HJ, Hou WC. Asn-Trp dipeptides improve the oxidative stress and learning dysfunctions in D-galactose-induced BALB/c mice. Food Funct 2014;5:2228-36. https://doi.org/10.1039/c4fo00205a
  69. Hawkins RA, O'Kane RL, Simpson IA, Vina JR. Structure of the blood-brain barrier and its role in the transport of amino acids. J Nutr 2006;136:218S-226S.
  70. Margolis FL. Carnosine in the primary olfactory pathway. Science 1974;184:909-11. https://doi.org/10.1126/science.184.4139.909
  71. Margolis FL, Grillo M. Axoplasmic transport of carnosine (${\beta}$-alanyl-L-histidine) in the mouse olfactory pathway. Neurochem Res 1977;2:507-19. https://doi.org/10.1007/BF00966011
  72. Berezhnoy DS, Stvolinsky SL, Lopachev AV, Devyatov AA, Lopacheva OM, Kulikova OI, Abaimov DA, Fedorova TN. Carnosine as an effective neuroprotector in brain pathology and potential neuromodulator in normal conditions. Amino Acids 2019;51:139-50. https://doi.org/10.1007/s00726-018-2667-7

피인용 문헌

  1. Physicochemical Characteristics of Protein Isolated from Thraustochytrid Oilcake vol.9, pp.6, 2020, https://doi.org/10.3390/foods9060779
  2. Zinc enhances carnosine inhibitory effect against structural and functional age-related protein alterations in an albumin glycoxidation model vol.33, pp.6, 2020, https://doi.org/10.1007/s10534-020-00254-0
  3. Human iPSC-Derived Neurons as A Platform for Deciphering the Mechanisms behind Brain Aging vol.9, pp.11, 2020, https://doi.org/10.3390/biomedicines9111635