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Journal of Applied Phycology

, Volume 30, Issue 6, pp 3253–3260 | Cite as

Neuritogenic and in vitro antioxidant activities of Malaysian Gracilaria manilaensis Yamamoto & Trono

  • Jun-Rui Pang
  • Veronica Ming-Jun Goh
  • Cheng-Yau Tan
  • Siew-Moi Phang
  • Kah-Hui Wong
  • Yoon-Yen YowEmail author
8th Asian Pacific Phycological Forum

Abstract

Numerous marine-based compounds have been identified as having diverse biological activities. Gracilaria manilaensis Yamamoto & Trono is a red agarophyte endemic to the Malaysia coastal area. It is used as a gelling and thickening agent for food industries. In this study, the rat pheochromocytoma cell line (PC-12Adh) was employed as in vitro model to investigate the neuritogenic activities in hot aqueous, methanol, and ethanol extracts of G. manilaensis. Phytochemical contents and in vitro antioxidant activities of the extracts were also determined. All G. manilaensis extracts were found to increase the percentage of neurite-bearing cells and upregulated the neuronal cytoskeleton of PC-12Adh cells with no inhibition across the tested concentration range (0–0.15 mg mL−1). The methanol and ethanol extracts had higher phenolic and flavonoid contents than the hot aqueous extract. They also showed higher antioxidant activities against 2,2-diphenyl-1-pircryhydrazyl (DPPH) and 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) free radicals and higher reducing power compared to the hot aqueous extract. It is believed that G. manilaensis may possess potent bioactive compounds that mimic the neuroactivity of the nerve growth factor (NGF) for neuronal survival, development, and differentiation. It has been suggested that agar producer G. manilaensis might be a promising dietary supplement for cognitive health in the prevention of neurological disorders.

Keywords

Gracilaria manilaensis PC-12Adh Neuritogenesis Antioxidant Phytochemicals 

Notes

Funding information

This research was funded by Sunway Internal Research Grants (project no.: INT-FST-DBS-2016-1 & INTS-2017-SST-DBS-01) from Sunway University and Jeffery Cheah foundation Scholarship. We are thankful to the Mushroom Research Centre, University of Malaya, for providing the PC-12Adh cell line. Special thanks to Ms. Chai-Chee Ng for her technical supports.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdullah NS (2013) Fatty acids profiles of red seaweed, Gracilaria manilaensis. Experiment 11:726–732Google Scholar
  2. Abdullah NS, Muhamad S, Omar IC, Abdullah H (2013) Determination of antioxidant and cytotoxic activities of red seaweed, (Gracilaria manilaensis) against different cancer cell lines. J Food Sci Eng 3:616–624Google Scholar
  3. Ahamad ZH, Shuhanija SN (2013) Physiological and biochemical responses of a Malaysian red alga, Gracilaria manilaensis treated with copper, lead and mercury. J Environ Res Dev 7:1246–1253Google Scholar
  4. Ahmad R, Surif M, Ramli N, Yahya N, Nor ARM, Bekbayeva L (2011) A preliminary study on the agar content and agar gel strength of Gracilaria manilaensis using different agar extraction processes. World Appl Sci J 15:184–188Google Scholar
  5. Alghazwi M, Kan YQ, Zhang W, Gai WP, Garson MJ, Smid S (2016) Neuroprotective activities of natural products from marine macroalgae during 1999–2015. J Appl Phycol 28:3599–3616CrossRefGoogle Scholar
  6. Andriani Y, Syamsumir D, Yee T, Harisson F, Herng G, Oroscoa S, Orosco C, AM A, Latip J, Kikuzaki H, Mohamad H (2016) Biological activities of isolated compounds from three edible Malaysian red seaweeds, Gracilaria changii, G. manilaensis and Gracilaria sp. Nat Prod Commun 11:1117–1120Google Scholar
  7. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 30:25–30CrossRefGoogle Scholar
  8. Chan PT, Matanjun P, Yasir SM, Tan TS (2015) Antioxidant activities and polyphenolics of various solvent extracts of red seaweed, Gracilaria changii. J Appl Phycol 27:2377–2386CrossRefGoogle Scholar
  9. de Almeida CLF, Falcão H de S, Lima GR de M, Montenegro C de A, Lira NS, de Athayde-Filho PF, Rodrigues LC, de Souza MFV, Barbosa-Filho JM, Batista LM (2011) Bioactivities from marine algae of the genus Gracilaria. Int J Mol Sci 12:4550–4573CrossRefGoogle Scholar
  10. Farasat M, Khavari-Nejad RA, Nabavi SMB, Namjooyan F (2014) Antioxidant activity, total phenolics and flavonoid contents of some edible green seaweeds from northern coasts of the Persian Gulf. Iran J Pharm Res 13:163–170PubMedPubMedCentralGoogle Scholar
  11. Ferreira ICFR, Baptista P, Vilas-boas M, Barros L (2007) Free-radical scavenging capacity and reducing power of wild edible mushrooms from northeast Portugal: individual cap and stipe activity. Food Chem 100:1511–1516CrossRefGoogle Scholar
  12. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci 73:2424–2428CrossRefGoogle Scholar
  13. Gupta S, Abu-Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweed. Trends Food Sci Technol 22:315–326CrossRefGoogle Scholar
  14. Hannan A, Mohibbullah M, Hong Y-K (2014) Gelidium amansii promotes dendritic spine morphology and synaptogenesis, and modulates NMDA receptor-mediated postsynaptic current. In Vitro Cell Dev Biol Anim 50:445–452CrossRefGoogle Scholar
  15. Heo S-J, Cha S-H, Lee K-W, Jeon Y-J (2006) Antioxidant activities of red algae from Jeju Island. Algae 21:149–156CrossRefGoogle Scholar
  16. Hu N, Yu J-T, Tan L, Wang Y-L, Sun L, Tan L (2013) Nutrition and the risk of Alzheimer’s disease. Biomed Res Int 2013:524820PubMedPubMedCentralGoogle Scholar
  17. Hurtado AQ, Joe M, Sanares RC, Fan D, Prithiviraj B, Critchley AT (2012) Investigation of the application of Acadian marine plant extract powder (AMPEP) to enhance the growth, phenolic content, free radical scavenging, and iron chelating activities of Kappaphycus Doty (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 24:601–611CrossRefGoogle Scholar
  18. Ina A, Hayashi KI, Nozaki H, Kamei Y (2007) Pheophytin a, a low molecular weight compound found in the marine brown alga Sargassum fulvellum, promotes the differentiation of PC12 cells. Int J Dev Neurosci 25:63–68CrossRefGoogle Scholar
  19. Kamei Y, Tsang CK (2003) Sargaquinoic acid promotes neurite outgrowth via protein kinase A and MAP kinases-mediated signaling pathways in PC12D cells. Int J Dev Neurosci 21:255–262CrossRefGoogle Scholar
  20. Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A (1993) A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci 84:407–412CrossRefGoogle Scholar
  21. Mohibbullah M, Bhuiyan MMH, Hannan MA, Getachew P, Hong YK, Choi JS, Choi IS, Moon IS (2016a) The edible red alga Porphyra yezoensis promotes neuronal survival and cytoarchitecture in primary hippocampal neurons. Cell Mol Neurobiol 36:669–682CrossRefGoogle Scholar
  22. Mohibbullah M, Hannan A, Park I, Moon IS, Hong Y-K (2016b) The edible red seaweed Gracilariopsis chorda promotes axodendritic architectural complexity in hippocampal neurons. J Med Food 19:638–644CrossRefGoogle Scholar
  23. Oroian M, Escriche I (2015) Antioxidants: characterization, natural sources, extraction and analysis. Food Res Int 74:10–36CrossRefGoogle Scholar
  24. Oyaizu M (1986) Studies on product of browning reaction prepared from glucose amine. Jpn J Nutr 44:307–315CrossRefGoogle Scholar
  25. Ozawa M, Ninomiya T, Ohara T, Doi Y, Uchida K, Shirota T, Yonemoto K, Kitazono T, Kiyohara Y (2013) Dietary patterns and risk of dementia in an elderly Japanese population: the Hisayama study. Am J Clin Nutr 97:1076–1082CrossRefGoogle Scholar
  26. Pangestuti R, Kim SK (2011) Neuroprotective effects of marine algae. Mar Drugs 9:803–818CrossRefGoogle Scholar
  27. Pękal A, Pyrzynska K (2014) Evaluation of aluminium complexation reaction for flavonoid content assay. Food Anal Methods 7:1776–1782CrossRefGoogle Scholar
  28. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237CrossRefGoogle Scholar
  29. Santos SAO, Vilela C, Freire CSR, Abreu MH, Rocha SM, Silvestre AJD (2015) Chlorophyta and Rhodophyta macroalgae: a source of health promoting phytochemicals. Food Chem 183:122–128CrossRefGoogle Scholar
  30. Seow SL-S, Eik L, Naidu M, David P, Wong K-H, Sabaratnam V (2015) Lignosus rhinocerotis (Cooke) Ryvarden mimics the neuritogenic activity of nerve growth factor via MEK/ERK1/2 signaling pathway in PC-12 cells. Sci Rep 5:1–13CrossRefGoogle Scholar
  31. Seow SL-S, Naidu M, David P, Wong K-H, Sabaratnam V (2013) Potentiation of neuritogenic activity of medicinal mushrooms in rat pheochromocytoma cells. BMC Complement Altern Med 13:157CrossRefGoogle Scholar
  32. Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol 299:152–178CrossRefGoogle Scholar
  33. Smalheiser NR, Schwartz NB (1987) Kinetic analysis of ‘rapid onset’ neurite formation in NG108-15 cells reveals a dual role for substratum-bound laminin. Brain Res 431:111–121CrossRefGoogle Scholar
  34. Snyder LR, Kirkland JJ (1979) Solvents. In: Snyder LR, Kirkland JJ (eds) Introduction to modern liquid chromatography, 2nd edn. John Wiley & Sons, Inc., New York, pp 248–250Google Scholar
  35. Tirtawijaya G, Mohibbullah M, Meinita MDN, Moon IS, Hong YK (2016) The ethanol extract of the rhodophyte Kappaphycus alvarezii promotes neurite outgrowth in hippocampal neurons. J Appl Phycol 28:2515–2522CrossRefGoogle Scholar
  36. Tsang CK, Ina A, Goto T, Kamei Y (2005) Sargachromenol, a novel nerve growth factor-potentiating substance isolated from Sargassum macrocarpum, promotes neurite outgrowth and survival via distinct signaling pathways in PC12D cells. Neuroscience 132:633–643CrossRefGoogle Scholar
  37. Tsang CK, Kamei Y (2004) Sargaquinoic acid supports the survival of neuronal PC12D cells in a nerve growth factor-independent manner. Eur J Pharmacol 488:11–18CrossRefGoogle Scholar
  38. United Nations (2011) Globally harmonized system of classification and labelling of chemicals (GHS), Fourth rev. United Nations, New York and GenevaGoogle Scholar
  39. Wang W, Dai R, Yan H, Han C, Liu L (2015) Current situation of PC12 cell use in neuronal injury study. Int J Biotechnol Wellness Ind 4:61–66CrossRefGoogle Scholar
  40. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982CrossRefGoogle Scholar
  41. Wong K-H, Sabaratnam V, Abdullah N, Naidu M, Keynes R (2007) Activity of aqueous extract of lion’s mane mushroom Hericium erinaceus (Bull.: Fr.) Pers. (Aphyllophoromycetidae) on the neural cell line NG108-15. Int J Med Mushr 9:57–65CrossRefGoogle Scholar
  42. Yildiz G, Vatan Ö, Çelikler S, Dere Ş (2011) Determination of the phenolic compounds and antioxidative capacity in red algae Gracilaria bursa-pastoris. Int J Food Prop 14:496–502CrossRefGoogle Scholar
  43. Zhang A, Fang Y, Wang H, Li H, Zhang Z (2011) Free-radical scavenging properties and reducing power of grape cane extracts from 11 selected grape cultivars widely grown in China. Molecules 16:10104–10122CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Jun-Rui Pang
    • 1
  • Veronica Ming-Jun Goh
    • 1
  • Cheng-Yau Tan
    • 2
  • Siew-Moi Phang
    • 2
  • Kah-Hui Wong
    • 3
  • Yoon-Yen Yow
    • 1
    Email author
  1. 1.Department of Biological Sciences, School of Science & TechnologySunway UniversityBandar SunwayMalaysia
  2. 2.Institute of Ocean and Earth SciencesUniversity of MalayaKuala LumpurMalaysia
  3. 3.Department of Anatomy, Faculty of MedicineUniversity of MalayaKuala LumpurMalaysia

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