Lignosus rhinocerotis (Cooke) Ryvarden mimics the neuritogenic activity of nerve growth factor via MEK/ERK1/2 signaling pathway in PC-12 cells

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Seow, Syntyche Ling Sing ^a,b   Eik, Lee Fang ^a,b   Naidu, Murali ^a   David, Pamela ^a   Wong, Kah Hui ^a   Sabaratnam, Vikineswary ^a,b  

^a UNIVERSITY OF MALAYA   (Malaysia)

^b UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL; CHEMISTRY; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; NEURITE; PC12 CELL LINE; PHOSPHORYLATION; POLYPORACEAE; RAT; SIGNAL TRANSDUCTION;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; MAP KINASE SIGNALING SYSTEM; NERVE GROWTH FACTOR; NEURITES; PC12 CELLS; PHOSPHORYLATION; POLYPORACEAE; RATS; SIGNAL TRANSDUCTION;

EID: 84946730878     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep16349     Document Type: Article

References (60)

1. Wasser, S. P., Weis, A. L. Therapeutic effects of substance occurring in higher basidiomycetes mushrooms: A modern perspective. Critical Reviews in Immunology. 19(1), 65-96 (1999).
2. Phan, C. W., Wong, W. L., David, P., Naidu, M., Sabaratnam, V. Therapeutic potential of culinary-medicinal mushrooms for the management of neurodegenerative diseases: diversity, metabolite, and mechanism. Critical Reviews in Biotechnology. 1-14 (2014), doi: 10.3109/07388551.2014.887649.
3. Tan, C. S., Ng, S. T., Yap, Y. H. Y., Lee, S. S., Lee, M. L. et al. Breathing new life to a Malaysia lost national treasure-the tiger's milk mushroom (Lignosus rhinocerotis) in Mushroom Science XVIII: Proceedings of the18th Congress of the International Society for Mushroom Science (eds Zhang, J. et al.) 66-71 (Beijing, China, 2012).
4. Lee, S. S., Chang, Y. S., Noraswati, M. N. R. Utilization of macrofungi by some indigenous communities for food and medicine in Peninsular Malaysia. Forest Ecology and Management. 257, 2062-2065 (2009).
5. Burkill, I. H., Birtwistle, W., Foxworthy, F. W., Scrivenor, J. B., Watson, J. B. A Dictionary of the Economic Products of the Malay Peninsula, volume I & II. Kuala Lumpur: Governments of Malaysia and Singapore by the Ministry of Agriculture and Cooperatives. (Malaysia, 1966).
6. Chang, Y. S., Lee, S. S. Utilisation of macrofungi species in Malaysia. Fungal Diversity. 15, 15-22 (2004).
7. Huang, N. L. Identification of the scientific name of Hurulingzhi. Acta Edulis Fungi. 6, 30-32 (1999).
8. Da Silva, J. S., Dotti, C. G. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nature Reviews Neuroscience. 3, 694-704 (2002).
9. Kromer, L. F. Nerve growth factor treatment after brain injury prevents neuronal death. Science. 235, 214-216 (1987).
10. Thoenen, H. Neurotrophins and neuronal plasticity. Science. 270, 593-598 (1995).
11. Koliatsos, V. E., Clatterbuck, R. E., Nauta, W. H. J., Knusel, B., Burton, L. E. et al. Recombinant human nerve growth factor prevents degeneration of basal forebrain cholinergic neurons in primates. Annals of Neurology. 30, 831-840 (1991).
12. Hefti, F., Weiner, W. J. Nerve growth factor and Alzheimer's disease. Annals of Neurology. 20, 275-281 (1986).
13. Capsoni, S., Ugolini, G., Comparini, A., Ruberti, F., Berardi, N. et al. Alzheimer-like neurodegeneration in aged anti-nerve growth factor transgenic mice. Proceedings of the National Academy of Sciences of the United States of America. 97, 6826-6831 (2000).
14. Granholm, A. C., Sanders, L. A., Reyland, M. E., Hoernig, G. R., Shen, L. et al. Transplantation of fetal tissues from trophic factor knockout mice to wildtype and heterozygous siblings. In: Abstract American Society for Neural Transplantation. (Clearwater, FL, 1998).
15. Williams, B., Dwyer, D. S. Structure-based discovery of low molecular weight compounds that stimulate neurite outgrowth and substitute for nerve growth factor. Journal of Neurochemistry. 110(6), 1876-1884 (2009).
16. Kao, S. C., Jaiswal, R. K., Kolch, W., Landreth, G. E. Identification of the mechanisms regulating the differential activation of the MAPK cascade by epidermal growth factor and nerve growth factor in PC12 cells. The Journal of Biological Chemistry. 276(21), 18169-18177 (2001).
17. Roskoski, R. ERK1/2 MAP kinases: structure, function, and regulation. Pharmacological Research. 66, 105-143 (2012).
18. Vaudry, D., Stork, P. J. S., Lazarovici, P., Eiden, L. E. Signaling pathways for PC-12 cell differentiation: making the right connections. Science. 296(5573), 1648-1649 (2002).
19. Naidu, M., David, P., Asher, R., Fawcett, J. Expression of Akt and MAPK in the normal and regenerating peripheral nerve and their dorsal root ganglia. Malaysian Journal of Biochemistry and Molecular Biology. 17, 16-19 (2009).
20. Wong, K. H., Naidu, M., David, P., Bakar, R., Sabaratnam, V. Neuroregenerative potential of lion's mane mushroom, Hericium erinaceus (Bull.: Fr.) Pers. (Higher Basidiomycetes), in the treatment of peripheral nerve injury (Review). International Journal of Medicinal Mushrooms. 14, 427-446 (2012).
21. Parmar, P. K., Coates, L. C., Pearson, J. F., Hill, R. M., Birch, N. P. Neuroserpin regulates neurite outgrowth in nerve growth factor-treated PC12 cells. Journal of Neurochemistry. 82, 1406-1415 (2002).
22. Teng, K. K., Angelastro, J. M., Cunningham, M. E., Greene, L. A. Cultured PC12 cells: A model for neuronal function, differentiation, and survival in Cell Biology: A Laboratory Handbook. 3rd ed. (ed. Colin, J. E.) 171-176 (USA: Elsevier Science, 2006).
23. Greene, L. A., Tischler, A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proceedings of the National Academy of Sciences. 73, 2424-2428 (1976).
24. Cheung, W. M. W., Hui, W. S., Chu, P. W. K., Chiu, S. W., Ip, N. Y. I. Ganoderma extract activates MAP kinases and induces the neuronal differentiation of rat pheochromocytoma PC12 cells. FEBS Letters. 486, 291-296 (2000).
25. Phan, C. W., Wong, W. L., David, P., Naidu, M., Sabaratnam, V. Pleurotus giganteus (Berk.) Karunarathna & K. D. Hyde: nutritional value and in vitro neurite outgrowth activity in rat pheochromocytoma cells. BMC Complementary and Alternative Medicine. 12, 102 (2012), doi: 10.1186/1472-6882-12-102.
26. Seow, S. L. S., Naidu, M., David, P., Wong, K. H., Sabaratnam, V. Potentiation of neuritogenic activity of medicinal mushrooms in rat pheochromocytoma cells. BMC Complementary and Alternative Medicine. 13, 157 (2013), doi: 10.1186/1472-6882-13-157.
27. Lai, C. K. M., Wong, K. H., Cheung, P. C. K. Antiproliferative effects of sclerotial polysaccharides from Polyporus rhinocerus Cooke (Aphyllophoromycetideae) on different kinds of leukemic cells. International Journal of Medicinal Mushrooms. 10, 255-264 (2008).
28. Lee, M. L., Tan, N. H., Fung, S. Y., Tan, C. S., Ng, S. T. The antiproliferative activity of sclerotia of Lignosus rhinocerus (Tiger Milk Mushroom). Evidence-based complementary and alternative medicine. eCAM, 697603 (2012), doi: 10.1155/2012/697603.
29. Lau, B. F., Abdullah, N., Aminudin, N., Lee, H. B. Chemical composition and cellular toxicity of ethnobotanical-based hot and cold aqueous preparations of the tiger's milk mushroom (Lignosus rhinocerotis). Journal of Ethnopharmacology. 150, 252-262 (2013).
30. Wong, K. H., Lai, C. K. M., Cheung, P. C. K. Stimulation of human innate immune cells by medicinal mushroom sclerotial polysaccharides. International Journal of Medicinal Mushrooms. 11, 215-223 (2009).
31. Wong, K. H., Lai, C. K. M., Cheung, P. C. K. Immunomodulatory activities of mushroom sclerotial polysaccharides. Food Hydrocolloids 25(2), 150-158 (2011).
32. Guo, C., Wong, K. H., Cheung, P. C. Hot water extract of the sclerotium of Polyporus rhinocerus Cooke enhances the immune functions of murine macrophages. International Journal of Medicinal Mushrooms. 13(3), 237-44 (2011).
33. Yap, Y. H. Y., Tan, N., Fung, S., Aziz, A. A., Tan, C. et al. Nutrient composition, antioxidant properties, and anti-proliferative activity of Lignosus rhinocerus Cooke sclerotium. Journal of the Science of Food and Agriculture. 93, 2945-2952 (2013).
34. Eik, L. F., Naidu, M., David, P., Wong, K. H., Tan, Y. S. et al. Lignosus rhinocerus (Cooke) Ryvarden: a medicinal mushroom that stimulates neurite outgrowth in PC-12 cells. Evidence-based Complementary and Alternative Medicine. eCAM, 320308 (2012), doi: 10.1155/2012/320308.
35. Lee, S. S., Tan, N. H., Fung, S. Y., Pailoor, J., Sim, S. Evaluation of the sub-acute toxicity of the sclerotium of Lignosus rhinocerus (Cooke), the Tiger Milk mushroom. Journal of Ethnopharmacology. 138, 192-200 (2011).
36. Lee, S. S., Enchang, F. K., Tan, N. H., Fung, S. Y., Pailoor, J. Preclinical toxicological evaluations of the sclerotium of Lignosus rhinocerus (Cooke), the tiger milk mushroom. Journal of Ethnopharmacology. 147, 157-163 (2013).
37. John, P. A., Wong, K. H., Naidu, M., Sabaratnam, V., David, P. Combination effects of curcumin and aqueous extract of Lignosus rhinocerotis mycelium on neurite outgrowth stimulation activity in PC-12 cells. Natural Product Communications. 8, 711-714 (2013).
38. Mizuno, T. The extraction and development of antitumour-active polysaccharides from medicinal mushrooms in Japan. International Journal of Medicinal Mushrooms. 1, 9-29 (1999).
39. Vannucci, L., Krizan, J., Sima, P., Stakheev, D., Caja, F. et al. Immunostimulatory properties and antitumor activities of glucans (Review). International Journal of Oncology. 43, 357-364 (2013).
40. Kawagishi, H., Ando, M., Sakamoto, H., Yoshida, S., Ojima, F. et al. Hericenones C, D and E, stimulators of nerve growth factor (NGF)-synthesis, from the mushroom Hericium erinaceum. Tetrahedron Letters. 32, 4561-4564 (1991).
41. Kawagishi, H., Shimada, A., Shirai, R., Okamoto, K., Ojima, F. et al. Erinacines A, B and C, strong stimulators of nerve growth factor (NGF)-synthesis, from the mycelia of Hericium erinaceum. Tetrahedron Letters. 35, 1569-1572 (1994).
42. Obara, Y., Nakahata, N., Kita, T., Takaya, Y., Kobayashi, H. et al. Stimulation of neurotrophic factor secretion from 1321N1 human astrocytoma cells by novel diterpenoids, scabronines A and G. European Journal of Pharmacology. 370, 79-84 (1999).
43. Qi, J., Ojika, M., Sakagami, Y. Termitomycesphins A-D, novel neuritogenic cerebrosides from the edible Chinese mushroom Termitomyces albuminosus. Tetrahedron. 56, 5835-5841 (2000).
44. Marcotullio, M. C., Pagiotti, R., Maltese, F., Mwankie, G. N. O., Hoshino, T. et al. Cyathane diterpenes from Sarcodon cyrneus and evaluation of their activities of neuritegenesis and nerve growth factor production. Bioorganic and Medicinal Chemistry. 15, 2878-2882 (2007).
45. Lee, M. K., Xu, Z., Wong, P. C., Cleveland, D. W. Neurofilaments are obligate heteropolymers in vivo. J. Cell Biol. 122, 1337-1350 (1993).
46. Liem, R. K. H., Yen, S. H., Salomon G. B., Shelanski M. L. Intermediate filaments in nervous tissue. J. Cell Biol. 79, 637-645 (1978).
47. Phan, C. W., Lee, G. S., Hong, S. L., Wong, Y. T., Brklja?a, R. et al. Hericium erinaceus (Bull.:Fr) Pers. cultivated in tropical conditions: Isolation of hericenones and demonstration of NGF-mediated neurite outgrowth in PC12 cells via MEK/ERK and PI3K-Akt signaling pathways. Food & Function. 00, 1-3 (2014).
48. Lai, P. L., Naidu, M., Sabaratnam, V., Wong, K. H., David, R. S. et al. Neurotrophic Properties of the Lion's Mane Medicinal Mushroom, Hericium erinaceus (Higher Basidiomycetes) from Malaysia. International Journal of Medicinal Mushrooms. 15, 539-554 (2013).
49. Frade, J. M., Barde, Y. A. Nerve growth factor: two receptors, multiple functions. Bioessays. 20, 137-145 (1998).
50. Limpert, A. S., Karlo, J. C., Landreth, G. E. Nerve growth factor stimulates the concentration of TrkA within lipid rafts and extracellular signal-regulated kinase activation through c-Cbl-associated protein. Molecular and Cellular Biology. 27, 5686-5698 (2007).
51. Egea, J., Espinet, C., Soler, R. M., Peiro, S., Rocamora, N. et al. Growth factor activation of the extracellular signal-regulated kinase pathway is modulated by Ca2+ and calmodulin. Molecular and Cellular Biology. 20, 1931-1946 (2000).
52. Koizumi, S., Contreras, M. L., Matsuda, Y., Hama, T., Lazarovici, P. et al. K-252a: A specific inhibitor of the action of nerve growth factor on PC 12 cells. The journal of Neuroscience. 8(2), 715-721 (1988).
53. Favata, M. F., Horiuchi, K. Y., Manos, E. J., Daulerio, A. J., Stradley, D. A. et al. Identification of a novel inhibitor of mitogenactivated protein kinase kinase. The Journal of Biological Chemistry. 273(29), 18623-18632 (1998).
54. Kawamata, T., Yamaguchi, T., Shin-ya, K., Hori, T. Divergence in signaling pathways involved in promotion of cell viability mediated by bFGF, NGF, and EGF in PC12 cells. Neurochemical Research. 28(8), 1221-1225 (2003).
55. Nishina, A., Kimura, H., Sekiguchi, A., Fukumoto, R., Nakajima, S. et al. Lysophosphatidylethanolamine in Grifola frondosa as a neurotrophic activator via activation of MAPK. Journal of Lipid Research. 47, 1434-1443 (2006).
56. Vikineswary, S., Chang, S. T. Edible and medicinal mushrooms for sub-health intervention and prevention of lifestyle diseases. Technology Trends, Tech Monitor. Jul-Sept, 33-43 (2013).
57. Tan, C. S., Ng, S. T., Vikineswary, S., Lo, E. P., Tee, C. S. Genetic markers for identification of a Malaysian medicinal mushroom Lignosus rhinocerus (Cendawan susu rimau). Acta Hort (ISHS). 859, 161-167 (2010).
58. Smalheiser, N. R., Schwartz, N. B. Kinetic analysis of 'rapid onset' neurite formation in NG108-15 cells reveals a dual role for substratum-bound laminin. Brain Res. 431(1), 111-121 (1987).
59. Ojha, A. K., Chandra, K., Ghosh, K., Islam, S. S. Glucans from the alkaline extract of an edible mushroom, Pleurotus florida, cv Assam Florida: isolation, purification, and characterization. Carbohydrate Research. 345, 2157-2163 (2010).
60. Schimmelpfeng, J., Weibezahn, K. F., Dertinger, H. Quantification of NGF-dependent neuronal differentiation of PC-12 cells by means of neurofilament-L mRNA expression and neuronal outgrowth. Journal of Neuroscience Methods. 139(2), 299-306 (2004).