Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
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Panax ginseng (Korea Red Ginseng) repairs diabetic sensorineural damage through promotion of the nerve growth factor pathway in diabetic zebrafish

  • Nam, Youn Hee (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Moon, Hyo Won (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Lee, Yeong Ro (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Kim, Eun Young (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Rodriguez, Isabel (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Jeong, Seo Yule (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Castaneda, Rodrigo (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Park, Ji-Ho (Graduate School of East-West Medical Science, Kyung Hee University) ;
  • Choung, Se-Young (Department of Preventive Pharmacy and Toxicology, College of Pharmacy, Kyung Hee University) ;
  • Hong, Bin Na (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University) ;
  • Kang, Tong Ho (Department of Oriental Medicine Biotechnology, College of Life Sciences and Graduate School of Biotechnology, Kyung Hee University)
  • Received : 2017.09.05
  • Accepted : 2018.02.12
  • Published : 2019.04.15
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Abstract

Background: Diabetic sensorineural damage is a complication of the sensory neural system, resulting from long-term hyperglycemia. Red ginseng (RG) has shown efficacy for treatment of various diseases, including diabetes mellitus; however, there is little research about its benefit for treating sensorineural damage. Therefore, we aim to evaluate RG efficacy in alloxan-induced diabetic neuromast (AIDN) zebrafish. Methods: In this study, we developed and validated an AIDN zebrafish model. To assess RG effectiveness, we observed morphological changes in live neuromast zebrafish. Also, zebrafish has been observed to have an ultrastructure of hair-cell cilia under scanning electron microscopy. Thus, we recorded these physiological traits to assess hair cell function. Finally, we confirmed that RG promoted neuromast recovery via nerve growth factor signaling pathway markers. Results: First, we established an AIDN zebrafish model. Using this model, we showed via live neuromast imaging that RG fostered recovery of sensorineural damage. Damaged hair cell cilia were recovered in AIDN zebrafish. Furthermore, RG rescued damaged hair cell function through cell membrane ion balance. Conclusion: Our data suggest that RG potentially facilitates recovery in AIDN zebrafish, and its mechanism seems to be promotion of the nerve growth factor pathway through increased expression of topomyosin receptor kinase A, transient receptor potential channel vanilloid subfamily type 1, and mitogen-activated protein kinase phosphorylation.

Keywords

References

  1. Baek KS, Yi YS, Son YJ, Jeong D, Sung NY, Aravinthan A, Kim JH, Cho JY. Comparison of anticancer activities of Korean Red Ginseng-derived fractions. J Ginseng Res 2017;41(3):386-91. https://doi.org/10.1016/j.jgr.2016.11.001
  2. Kim JH, Yi YS, Kim MY, Cho JY. Role of ginsenosides, the main active components of Panax ginseng, in inflammatory responses and diseases. J Ginseng Res 2017;41:435-43. https://doi.org/10.1016/j.jgr.2016.08.004
  3. Cheon JM, Kim DI, Kim KS. Insulin sensitivity improvement of fermented Korean Red Ginseng (Panax ginseng) mediated by insulin resistance hallmarks in old-aged ob/ob mice. J Ginseng Res 2015;39(4):331-7. https://doi.org/10.1016/j.jgr.2015.03.005
  4. Park TY, Hong M, Sung H, Kim S, Suk KT. Effect of Korean Red Ginseng in chronic liver disease. J Ginseng Res 2017;41:450-5. https://doi.org/10.1016/j.jgr.2016.11.004
  5. Faucherre A, Pujol-Marti J, Kawakami K, Lopez-Schier H. Afferent neurons of the zebrafish lateral line are strict selectors of hair-cell orientation. PLoS One 2009;4(2):e4477. https://doi.org/10.1371/journal.pone.0004477
  6. Santos F, MacDonald G, Rubel EW, Raible DW. Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hear Res 2006;213(1):25-33. https://doi.org/10.1016/j.heares.2005.12.009
  7. McHenry MJ, Feitl KE, Strother JA, Van Trump WJ. Larval zebrafish rapidly sense the water flow of a predator's strike. Biol Lett 2009;5(4):477-9. https://doi.org/10.1098/rsbl.2009.0048
  8. Metcalfe WK, Kimmel CB, Schabtach E. Anatomy of the posterior lateral line system in young larvae of the zebrafish. J Comp Neurol 1985;233(3): 377-89. https://doi.org/10.1002/cne.902330307
  9. Raible DW, Kruse GJ. Organization of the lateral line system in embryonic zebrafish. J Comp Neurol 2000;421:189-98. https://doi.org/10.1002/(SICI)1096-9861(20000529)421:2<189::AID-CNE5>3.0.CO;2-K
  10. Gompel N, Cubedo N, Thisse C, Thisse B, Dambly-Chaudiere C, Ghysen A. Pattern formation in the lateral line of zebrafish. Mech Dev 2001;105:69-77. https://doi.org/10.1016/S0925-4773(01)00382-3
  11. Ghysen A, Dambly-Chaudiere C. The lateral line microcosmos. Genes Dev 2007;21:2118-30. https://doi.org/10.1101/gad.1568407
  12. Hong BN, Ji MG, Kang TH. The efficacy of red ginseng in type 1 and type 2 diabetes in animals. Evid Based Complement Alternat Med 2013;2013: 593181.
  13. Szkudelski T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 2001;50(6):537-46.
  14. Radenkovic M, Stojanovic M, Prostran M. Experimental diabetes induced by alloxan and streptozotocin: the current state of the art. J Pharmacol Toxicol Methods 2016;78:13-31. https://doi.org/10.1016/j.vascn.2015.11.004
  15. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25(4):402-8. https://doi.org/10.1006/meth.2001.1262
  16. Elo B, Villano CM, Govorko D, White LA. Larval zebrafish as a model for glucose metabolism: expression of phosphoenolpyruvate carboxykinase as a marker for exposure to anti-diabetic compounds. J Mol Endocrinol 2007;38(4):433-40. https://doi.org/10.1677/JME-06-0037
  17. Bauer CA, Brozoski TJ, Myers KS. Acoustic injury and TRPV1 expression in the cochlear spiral ganglion. Int Tinnitus J 2007;13(1):21.
  18. Patapoutian A, Reichardt LF. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 2001;11(3):272-80. https://doi.org/10.1016/S0959-4388(00)00208-7
  19. Nguyen TL, Kim CK, Cho JH, Lee KH, Ahn JY. Neuroprotection signaling pathway of nerve growth factor and brain-derived neurotrophic factor against staurosporine induced apoptosis in hippocampal H19-7 cells. Exp Mol Med 2010;42(8):583-95. https://doi.org/10.3858/emm.2010.42.8.060
  20. Kao SC, Jaiswal RK, Kolch W, Landreth GE. Identification of the mechanisms regulating the differential activation of the mapk cascade by epidermal growth factor and nerve growth factor in PC12 cells. J Biol Chem 2001;276(21):18169-77. https://doi.org/10.1074/jbc.M008870200
  21. Kim CS, Park JB, Kim KJ, Chang SJ, Ryoo SW, Jeon BH. Effect of Korea red ginseng on cerebral blood flow and superoxide production. Acta Pharmacol Sin 2002;23(12):1152-6.
  22. Quan HY, Kim DY, Chung SH. Korean red ginseng extract alleviates advanced glycation end product-mediated renal injury. J Ginseng Res 2013;37(2):187-93. https://doi.org/10.5142/jgr.2013.37.187
  23. Ou HC, Raible DW, Rubel EW. Cisplatin-induced hair cell loss in zebrafish (Danio rerio) lateral line. Hear Res 2007;233(1):46-53. https://doi.org/10.1016/j.heares.2007.07.003
  24. Shin YS, Hwang HS, Kang SU, Chang JW, Oh YT, Kim CH. Inhibition of p38 mitogen-activated protein kinase ameliorates radiation-induced ototoxicity in zebrafish and cochlea-derived cell lines. Neurotoxicology 2014;40:111-22. https://doi.org/10.1016/j.neuro.2013.12.006
  25. Van Trump WJ, McHenry MJ. The morphology and mechanical sensitivity of lateral line receptors in zebrafish larvae (Danio rerio). J Exp Biol 2008;211(13): 2105-15. https://doi.org/10.1242/jeb.016204
  26. Zhu Y, Colak T, Shenoy M, Liu L, Pai R, Li C, Mehta K, Pasricha PJ. Nerve growth factor modulates TRPV1 expression and function and mediates pain in chronic pancreatitis. Gastroenterology 2011;141(1):370-7. https://doi.org/10.1053/j.gastro.2011.03.046
  27. Nam YH, Hong BN, Rodriguez I, Ji MG, Kim K, Kim UJ, Kang TH. Synergistic potentials of coffee on injured pancreatic islets and insulin action via KATP channel blocking in zebrafish. J Agric Food Chem 2015;63(23):5612-21. https://doi.org/10.1021/acs.jafc.5b00027
  28. Nam YH, Le HT, Rodriguez I, Kim EY, Kim K, Jeong SY, Woo SH, Lee YR, Castaneda R, Hong J, et al. Enhanced antidiabetic efficacy and safety of compound K/ ${\beta}$-cyclodextrin inclusion complex in zebrafish. J Ginseng Res 2017;41(1):103-12. https://doi.org/10.1016/j.jgr.2016.08.007
  29. Shao J, Qiao L, Janssen RC, Pagliassotti M, Friedman JE. Chronic hyperglycemia enhances PEPCK gene expression and hepatocellular glucose production via elevated liver activating protein/liver inhibitory protein ratio. Diabetes 2005;54(4):976-84. https://doi.org/10.2337/diabetes.54.4.976
  30. Lauria G, Morbin M, Lombardi R, Capobianco R, Camozzi F, Pareyson D, Manconi M, Geppetti P. Expression of capsaicin receptor immunoreactivity in human peripheral nervous system and in painful neuropathies. J Peripher Nerv Syst 2006;11(3):262-71. https://doi.org/10.1111/j.1529-8027.2006.0097.x
  31. Apfel SC. Nerve growth factor for the treatment of diabetic neuropathy: what went wrong, what went right, and what does the future hold? Int Revi Neurobiol 2002;50:393-413. https://doi.org/10.1016/S0074-7742(02)50083-0
  32. Pittenger G, Vinik A. Nerve growth factor and diabetic neuropathy. Exp Diabetes Res 2003;4(4):271-85. https://doi.org/10.1155/EDR.2003.271
  33. Hirose M, Kuroda Y, Murata E. NGF/TrkA signaling as a therapeutic target for pain. Pain Pract 2016;16(2):175-82. https://doi.org/10.1111/papr.12342
  34. Khan N, Smith MT. Neurotrophins and neuropathic pain: role in pathobiology. Molecules 2015;20(6):10657-88. https://doi.org/10.3390/molecules200610657

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