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Journal of Applied Phycology

, Volume 31, Issue 1, pp 281–299 | Cite as

Approaches for the sustainable production of fucoxanthin, a xanthophyll with potential health benefits

  • Amirreza Zarekarizi
  • Linn Hoffmann
  • David BurrittEmail author
Article

Abstract

Fucoxanthin is a xanthophyll and one of the main marine carotenoids. It is present in macro- and micro-algae as a component of photosynthetic light-harvesting complexes. Fucoxanthin has been shown to be bioactive in a variety of model systems, having antioxidant, anti-cancer, anti-diabetic, anti-obesity, anti-aging, anti-angiogenic, and anti-metastatic effects in animals. Fucoxanthin has been proven to be safe for consumption by animals, including humans, and hence has the potential to be used as a bioactive molecule for the prevention and/or treatment of diseases in humans. In this review, we provide an overview of the main fucoxanthin-containing algae and the fucoxanthin biosynthetic pathway in algae, and discuss the potential health benefits of fucoxanthin for humans. We summarize the various methods that can be used to extract fucoxanthin from algae and evaluate the potential of biotechnological approaches, such as cell culture and the genetic engineering, for sustainable fucoxanthin production.

Keywords

Fucoxanthin Xanthophylls Carotenoids Bioactivity Cell culture Genetic engineering 

References

  1. Abidov M, Ramazanov Z, Seifulla R, Grachev S (2010) The effects of Xanthigen™ in the weight management of obese premenopausal women with non-alcoholic fatty liver disease and normal liver fat. Diabetes Obes Metab 12:72–81PubMedGoogle Scholar
  2. Afolayan AF, Bolton JJ, Lategan CA, Smith PJ, Beukes DR (2008) Fucoxanthin, tetraprenylated toluquinone and toluhydroquinone metabolites from Sargassum heterophyllum inhibit the in vitro growth of the malaria parasite Plasmodium falciparum. Z Naturforsch C 63:848PubMedGoogle Scholar
  3. Airanthi MK, Hosokawa M, Miyashita K (2011) Comparative antioxidant activity of edible Japanese brown seaweeds. J Food Sci 76:C104–C111PubMedGoogle Scholar
  4. Baweja P, Sahoo D, García-Jiménez P, Robaina RR (2009) Review: seaweed tissue culture as applied to biotechnology: problems, achievements and prospects. Phycol Res 57:45–58Google Scholar
  5. Beppu F, Niwano Y, Tsukui T, Hosokawa M, Miyashita K (2009) Single and repeated oral dose toxicity study of fucoxanthin (FX), a marine carotenoid, in mice. J Toxicol Sci 34:501–510PubMedGoogle Scholar
  6. Boderskov T, Schmedes PS, Bruhn A, Rasmussen MB, Nielsen MM, Pedersen MF (2016) The effect of light and nutrient availability on growth, nitrogen, and pigment contents of Saccharina latissima (Phaeophyceae) grown in outdoor tanks, under natural variation of sunlight and temperature, during autumn and early winter in Denmark. J Appl Phycol 28:1153–1165Google Scholar
  7. Borowitzka MA, Vonshak A (2017) Scaling up microalgal cultures to commercial scale. Eur J Phycol 52:407–418Google Scholar
  8. Burgess JG, Iwamoto K, Miura Y, Takano H, Matsunaga T (1993) An optical fibre photobioreactor for enhanced production of the marine unicellular alga Isochrysis aff. galbana T-Iso (UTEX LB 2307) rich in docosahexaenoic acid. Appl Microbiol Biotechnol 39:456–459Google Scholar
  9. Chen S-J, Lee C-J, Lin T-B, Liu H-J, Huang S-Y, Chen J-Z, Tseng K-W (2016) Inhibition of ultraviolet B-induced expression of the proinflammatory cytokines TNF-α and VEGF in the cornea by fucoxanthin treatment in a rat model. Mar Drugs 14(1):13PubMedPubMedCentralGoogle Scholar
  10. Conde E, Moure A, Domínguez H (2015) Supercritical CO2 extraction of fatty acids, phenolics and fucoxanthin from freeze-dried Sargassum muticum. J Appl Phycol 27:957–964Google Scholar
  11. D’Orazio N, Gemello E, Gammone MA, de Girolamo M, Ficoneri C, Riccioni G (2012) Fucoxantin: a treasure from the sea. Mar Drugs 10:604–616PubMedPubMedCentralGoogle Scholar
  12. Dambek M, Eilers U, Breitenbach J, Steiger S, Büchel C, Sandmann G (2012) Biosynthesis of fucoxanthin and diadinoxanthin and function of initial pathway genes in Phaeodactylum tricornutum. J Exp Bot 63:5607–5612PubMedPubMedCentralGoogle Scholar
  13. Das SK, Ren R, Hashimoto T, Kanazawa K (2010) Fucoxanthin induces apoptosis in osteoclast-like cells differentiated from RAW264.7 cells. J Agric Food Chem 58:6090–6095PubMedGoogle Scholar
  14. Del Campo JA, García-González M, Guerrero MG (2007) Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 74:1163–1174PubMedGoogle Scholar
  15. Egeland ES (2016) Carotenoids. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 507–563Google Scholar
  16. Eilers U, Bikoulis A, Breitenbach J, Büchel C, Sandmann G (2016) Limitations in the biosynthesis of fucoxanthin as targets for genetic engineering in Phaeodactylum tricornutum. J Appl Phycol 28:123–129Google Scholar
  17. Fariman GA, Shastan SJ, Zahedi MM (2016) Seasonal variation of total lipid, fatty acids, fucoxanthin content, and antioxidant properties of two tropical brown algae (Nizamuddinia zanardinii and Cystoseira indica) from Iran. J Appl Phycol 28:1323–1331Google Scholar
  18. Fernandes F, Barbosa M, Oliveira AP, Azevedo IC, Sousa-Pinto I, Valentão P, Andrade PB (2016) The pigments of kelps (Ochrophyta) as part of the flexible response to highly variable marine environments. J Appl Phycol 28:3689–3696Google Scholar
  19. Foo SC, Yusoff FM, Ismail M, Basri M, Chan KW, Khong NMH, Yau SK (2015a) Production of fucoxanthin-rich fraction (FxRF) from a diatom, Chaetoceros calcitrans (Paulsen) Takano 1968. Algal Res 12:26–32Google Scholar
  20. Foo SC, Yusoff FM, Ismail M, Basri M, Khong NMH, Chan KW, Yau SK (2015b) Efficient solvent extraction of antioxidant-rich extract from a tropical diatom, Chaetoceros calcitrans (Paulsen) Takano 1968. Asian Pac J Trop Biomed 5(10):834–840Google Scholar
  21. Fuller RW, JHn C, Kato Y, Brinen LS, Clardy J, Snader KM, Boyd MR (1992) A pentahalogenated monoterpene from the red alga Portieria hornemannii produces a novel cytotoxicity profile against a diverse panel of human tumor cell lines. J Med Chem 35:3007–3011PubMedGoogle Scholar
  22. Fung A, Hamid N, Lu J (2013) Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem 136:1055–1062PubMedGoogle Scholar
  23. Gammone MA, D'Orazio N (2015) Anti-obesity activity of the marine carotenoid fucoxanthin. Mar Drugs 13:2196–2214PubMedPubMedCentralGoogle Scholar
  24. Gómez-Loredo A, Benavides J, Rito-Palomares M (2016) Growth kinetics and fucoxanthin production of Phaeodactylum tricornutum and Isochrysis galbana cultures at different light and agitation conditions. J Appl Phycol 28:849–860Google Scholar
  25. Gómez-Loredo A, González-Valdez J, Rito-Palomares M (2015) Insights on the downstream purification of fucoxanthin, a microalgal carotenoid, from an aqueous two-phase system stream exploiting ultrafiltration. J Appl Phycol 27:1517–1523Google Scholar
  26. Guiry MD (2012) How many species of algae are there? J Phycol 48:1057–1063PubMedGoogle Scholar
  27. Guo B, Liu B, Yang B, Sun P, Lu X, Liu J, Chen F (2016) Screening of diatom strains and characterization of Cyclotella cryptica as a potential fucoxanthin producer. Mar Drugs 14(7):125PubMedCentralGoogle Scholar
  28. Ha AW, Kim WK (2013) The effect of fucoxanthin rich power on the lipid metabolism in rats with a high fat diet. Nutr Res Pract 7:287–293PubMedPubMedCentralGoogle Scholar
  29. Ha AW, Na SJ, Kim WK (2013) Antioxidant effects of fucoxanthin rich powder in rats fed with high fat diet. Nutr Res Pract 7:475–480PubMedPubMedCentralGoogle Scholar
  30. Heo S-J, Jeon Y-J (2009) Protective effect of fucoxanthin isolated from Sargassum siliquastrum on UV-B induced cell damage. J Photochem Photobiol B 95:101–107PubMedGoogle Scholar
  31. Heo S-J, Yoon W-J, Kim K-N, Ahn G-N, Kang S-M, Kang D-H, Affan A, Oh C, Jung W-K, Jeon Y-J (2010) Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide-stimulated RAW 264.7 macrophages. Food Chem Toxicol 48:2045–2051PubMedGoogle Scholar
  32. Heo S-J, Yoon W-J, Kim K-N, Oh C, Choi Y-U, Yoon K-T, Kang D-H, Qian Z-J, Choi I-W, Jung W-K (2012) Anti-inflammatory effect of fucoxanthin derivatives isolated from Sargassum siliquastrum in lipopolysaccharide-stimulated RAW 264.7 macrophage. Food Chem Toxicol 50:3336–3342PubMedGoogle Scholar
  33. Hosokawa M, Miyashita T, Nishikawa S, Emi S, Tsukui T, Beppu F, Okada T, Miyashita K (2010) Fucoxanthin regulates adipocytokine mRNA expression in white adipose tissue of diabetic/obese KK-Ay mice. Arch Biochem Biophys 504:17–25PubMedGoogle Scholar
  34. Hosokawa M, Wanezaki S, Miyauchi K, Kurihara H, Kohno H, Kawabata J, Odashima S, Takahashi K (1999) Apoptosis-inducing effect of fucoxanthin on human leukemia cell line HL-60. Food Sci Technol Res 5:243–246Google Scholar
  35. Hu X, Li Y, Li C, Fu Y, Cai F, Chen Q, Li D (2012) Combination of fucoxanthin and conjugated linoleic acid attenuates body weight gain and improves lipid metabolism in high-fat diet-induced obese rats. Arch Biochem Biophys 519:59–65PubMedGoogle Scholar
  36. Hwang EK, Kim CH, Sohn CH (1994) Callus-like formation and differentiation in Hizikia fusiformis (Harvey) Okamura. Algae 9:77–84Google Scholar
  37. Iio K, Okada Y, Ishikura M (2011) Single and 13-week oral toxicity study of fucoxanthin oil from microalgae in rats. Food Hyg Saf Sci (Shokuhin Eiseigaku Zasshi) 52(3):183–189Google Scholar
  38. Ikeda K, Kitamura A, Machida H, Watanabe M, Negishi H, Hiraoka J, Nakano T (2003) Effect of Undaria pinnatifida (Wakame) on the development of cerebrovascular diseases in stroke-prone spontaneously hypertensive rats. Clin Exp Pharmacol Physiol 30:44–48PubMedGoogle Scholar
  39. Irvani N, Solouki M, Omidi M, Zare AR, Shahnazi S (2010) Callus induction and plant regeneration in Dorem ammoniacum D., an endangered medicinal plant. Plant Cell Tissue Organ Cult 100:293–299Google Scholar
  40. Ishikawa C, Tafuku S, Kadekaru T, Sawada S, Tomita M, Okudaira T, Nakazato T, Toda T, Uchihara J-N, Taira N, Ohshiro K, Yasumoto T, Ohta T, Mori N (2008) Antiadult T-cell leukemia effects of brown algae fucoxanthin and its deacetylated product, fucoxanthinol. Int J Cancer 123:2702–2712PubMedGoogle Scholar
  41. Jaswir I, Noviendri D, Salleh HM, Miyashita K (2012) Fucoxanthin extractions of brown seaweeds and analysis of their lipid fraction in methanol. Food Sci Technol Res 18:251–257Google Scholar
  42. Jaswir I, Noviendri D, Salleh HM, Taher M, Miyashita K, Ramli N (2013) Analysis of fucoxanthin content and purification of all-trans-fucoxanthin from Turbinaria turbinata and Sargassum plagyophyllum by SiO2 open column chromatography and reversed phase-HPLC. J Liq Chromatogr Rel Technol 36:1340–1354Google Scholar
  43. Jeon S-M, Kim H-J, Woo M-N, Lee M-K, Shin YC, Park YB, Choi M-S (2010) Fucoxanthin-rich seaweed extract suppresses body weight gain and improves lipid metabolism in high-fat-fed C57BL/6J mice. Biotechnol J 5:961–969PubMedGoogle Scholar
  44. Jin E-S, Polle JEW, Lee H-K, Hyun S-M, Chang M (2003) Xanthophylls in microalgae: from biosynthesis to biotechnological mass production and application. J Microbiol Biotechnol 13:165–174Google Scholar
  45. Jin HJ, Seo GM, Cho YC, Hwang EK, Sohn CH, Hong Y-K (1997) Gelling agents for tissue culture of the seaweed Hizikia fusiformis. J Appl Phycol 9:489–501Google Scholar
  46. Jung HA, Islam MN, Lee CM, Jeong HO, CH Y, Woo HC, Choi JS (2012) Promising antidiabetic potential of fucoxanthin isolated from the edible brown algae Eisenia bicyclis and Undaria pinnatifida. Fish Sci 78:1321–1329Google Scholar
  47. Kadekaru T, Toyama H, Yasumoto T (2008) Safety evaluation of fucoxanthin purified from Undaria pinnatifida. J Jpn Soc Food Sci 55:304–308Google Scholar
  48. Kanazawa K, Ozaki Y, Hashimoto T, Das SK, Matsushita S, Hirano M, Okada T, Komoto A, Mori N, Nakatsuka M (2008) Commercial-scale preparation of biofunctional fucoxanthin from waste parts of brown sea algae Laminaria japonica. Food Sci Technol Res 14:573–573Google Scholar
  49. Kanda H, Kamo Y, Machmudah S, Wahyudiono GM (2014) Extraction of fucoxanthin from raw macroalgae excluding drying and cell wall disruption by liquefied dimethyl ether. Mar Drugs 12:2383–2396PubMedPubMedCentralGoogle Scholar
  50. Kang S-I, Ko H-C, Shin H-S, Kim H-M, Hong Y-S, Lee N-H, Kim S-J (2011) Fucoxanthin exerts differing effects on 3T3-L1 cells according to differentiation stage and inhibits glucose uptake in mature adipocytes. Biochem Biophys Res Commun 409:769–774PubMedGoogle Scholar
  51. Kang S-I, Shin H-S, Kim H-M, Yoon S-A, Kang S-W, Kim J-H, Ko H-C, Kim S-J (2012) Petalonia binghamiae extract and its constituent fucoxanthin ameliorate high-fat diet-induced obesity by activating AMP-activated protein kinase. J Agric Food Chem 60:3389–3395PubMedGoogle Scholar
  52. Kawashima Y, Tokuda H (1993) Regeneration from callus of Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta). Hydrobiologia 260:385–389Google Scholar
  53. Kawee-ai A, Kuntiya A, Kim SM (2013) Anticholinesterase and antioxidant activities of fucoxanthin purified from the microalga Phaeodactylum tricornutum. Nat Prod Commun 8:1381–1386PubMedGoogle Scholar
  54. Kim J-C (2014) Solvent extraction of fucoxanthin from Phaeodactylum tricornutum. Sep Sci Technol 49:410–415Google Scholar
  55. Kim K-N, Ahn G, Heo S-J, Kang S-M, Kang M-C, Yang H-M, Kim D, Roh SW, Kim S-K, Jeon B-T, Park P-J, Jung W-K, Jeon Y-J (2013) Inhibition of tumor growth in vitro and in vivo by fucoxanthin against melanoma B16F10 cells. Environ Toxicol Pharmacol 35:39–46PubMedGoogle Scholar
  56. Kim K-N, Heo S-J, Kang S-M, Ahn G, Jeon Y-J (2010a) Fucoxanthin induces apoptosis in human leukemia HL-60 cells through a ROS-mediated Bcl-xL pathway. Toxicol in Vitro 24:1648–1654PubMedGoogle Scholar
  57. Kim K-N, Heo S-J, Yoon W-J, Kang S-M, Ahn G, Yi T-H, Jeon Y-J (2010b) Fucoxanthin inhibits the inflammatory response by suppressing the activation of NF-κB and MAPKs in lipopolysaccharide-induced RAW 264.7 macrophages. Eur J Pharmacol 649:369–375PubMedGoogle Scholar
  58. Kim SJ, Kim HJ, Moon JS, Kim JM, Kang SG, Jung ST (2004) Characteristic and extraction of fucoxanthin pigment in Undaria pinnatifida. J Korean Soc Food Sci Nutr 33:847–851Google Scholar
  59. Kim SM, Jung YJ, Kwon ON, Cha KH, Um BH, Chung D, Pan CH (2012a) A potential commercial source of fucoxanthin extracted from the microalga Phaeodactylum tricornutum. Appl Biochem Biotechnol 166:1843–1855PubMedGoogle Scholar
  60. Kim SM, Kang S-W, Kwon ON, Chung D, Pan C-H (2012b) Fucoxanthin as a major carotenoid in Isochrysis aff. galbana: characterization of extraction for commercial application. J Korean Soc Appl Biol Chem 55:477–483Google Scholar
  61. Kok JM-L, Jee J-M, Chew L-Y, Wong C-L (2016) The potential of the brown seaweed Sargassum polycystum against acne vulgaris. J Appl Phycol 28:3127–3133Google Scholar
  62. Koller M, Muhr A, Braunegg G (2014) Microalgae as versatile cellular factories for valued products. Algal Res 6:52–63Google Scholar
  63. Kotake-Nara E, Asai A, Nagao A (2005a) Neoxanthin and fucoxanthin induce apoptosis in PC-3 human prostate cancer cells. Cancer Lett 220:75–84PubMedGoogle Scholar
  64. Kotake-Nara E, Terasaki M, Nagao A (2005b) Characterization of apoptosis induced by fucoxanthin in human promyelocytic leukemia cells. Biosci Biotechnol Biochem 69:224–227PubMedGoogle Scholar
  65. Kumar SR, Hosokawa M, Miyashita K (2013) Fucoxanthin: a marine carotenoid exerting anti-cancer effects by affecting multiple mechanisms. Mar Drugs 11:5130–5147PubMedPubMedCentralGoogle Scholar
  66. Lawlor HJ, Borowitzka MA, McComb JA (1991) A rapid and inexpensive method for surface sterilization of Ecklonia radiata (Phaeophyta) for tissue culture. Bot Mar 34:261–264Google Scholar
  67. Lawlor HJ, McComb JA, Borowitzka MA (1989) Tissue culture of Ecklonia radiata (Phaeophyceae, Laminariales): effects on growth of light, organic carbon source and vitamins. J Appl Phycol 1:105–112Google Scholar
  68. Leu S, Boussiba S (2014) Advances in the production of high-value products by microalgae. Ind Biotechnol 10:169–183Google Scholar
  69. Liu C-L, Liang A-L, Hu M-L (2011) Protective effects of fucoxanthin against ferric nitrilotriacetate-induced oxidative stress in murine hepatic BNL CL.2 cells. Toxicol in Vitro 25:1314–1319PubMedGoogle Scholar
  70. Liu Y, Liu M, Zhang X, Chen Q, Chen H, Sun L, Liu G (2016) Protective effect of fucoxanthin isolated from Laminaria japonica against visible light-induced retinal damage both in vitro and in vivo. J Agric Food Chem 64:416–424PubMedGoogle Scholar
  71. Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K (2005) Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem Biophys Res Commun 332:392–397PubMedGoogle Scholar
  72. Maeda H, Hosokawa M, Sashima T, Miyashita K (2007) Dietary combination of fucoxanthin and fish oil attenuates the weight gain of white adipose tissue and decreases blood glucose in obese/diabetic KK-ay mice. J Agric Food Chem 55:7701–7706PubMedGoogle Scholar
  73. Maeda H, Hosokawa M, Sashima T, Murakami-Funayama K, Miyashita K (2009) Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol Med Report 2:897–902Google Scholar
  74. Maeda H, Hosokawa M, Sashima T, Takahashi N, Kawada T, Miyashita K (2006) Fucoxanthin and its metabolite, fucoxanthinol, suppress adipocyte differentiation in 3T3-L1 cells. Int J Mol Med 8:147–152Google Scholar
  75. Martin LJ (2015) Fucoxanthin and its metabolite fucoxanthinol in cancer prevention and treatment. Mar Drugs 13:4784–4798PubMedPubMedCentralGoogle Scholar
  76. Matsui M, Tanaka K, Higashiguchi N, Okawa H, Yamada Y, Tanaka K, Taira S, Aoyama T, Takanishi M, Natsume C, Takakura Y, Fujita N, Hashimoto T, Fujita T (2016) Protective and therapeutic effects of fucoxanthin against sunburn caused by UV irradiation. J Pharmacol Sci 132:55–64PubMedGoogle Scholar
  77. McClure DD, Luiz A, Gerber B, Barton GW, Kavanagh JM (2018) An investigation into the effect of culture conditions on fucoxanthin production using the marine microalgae Phaeodactylum tricornutum. Algal Res 29:41–48Google Scholar
  78. Mikami K, Hosokawa M (2013) Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int J Mol Sci 14:13763–13781PubMedPubMedCentralGoogle Scholar
  79. Moreau D, Tomasoni C, Jacquot C, Kaas R, Le Guedes R, Cadoret J-P, Muller-Feuga A, Kontiza I, Vagias C, Roussis V, Roussakis C (2006) Cultivated microalgae and the carotenoid fucoxanthin from Odontella aurita as potent anti-proliferative agents in bronchopulmonary and epithelial cell lines. Environ Toxicol Pharmacol 22:97–103PubMedGoogle Scholar
  80. Mori K, Ooi T, Hiraoka M, Oka N, Hamada H, Tamura M, Kusumi T (2004) Fucoxanthin and its metabolites in edible brown algae cultivated in deep seawater. Mar Drugs 2:63–72PubMedCentralGoogle Scholar
  81. Mulders KJM, Lamers PP, Martens DE, Wijffels RH (2014) Phototrophic pigment production with microalgae: biological constraints and opportunities. J Phycol 50:229–242PubMedGoogle Scholar
  82. Muller-Feuga A (2000) The role of microalgae in aquaculture: situation and trends. J Appl Phycol 12:527–534Google Scholar
  83. Muradian K, Vaiserman A, Min KJ, Fraifeld VE (2015) Fucoxanthin and lipid metabolism: a minireview. Nutr Metab Cardiovasc Dis 25:891–897PubMedGoogle Scholar
  84. Mussio I, Rusig A (2009) Morphogenetic responses from protoplasts and tissue culture of Laminaria digitata (Linnaeus) J. V. Lamouroux (Laminariales, Phaeophyta): callus and thalloid-like structures regeneration. J Appl Phycol 21:255–264Google Scholar
  85. Nomura M, Kamogawa H, Susanto E, Kawagoe C, Yasui H, Saga N, Hosokawa M, Miyashita K (2013) Seasonal variations of total lipids, fatty acid composition, and fucoxanthin contents of Sargassum horneri (Turner) and Cystoseira hakodatensis (Yendo) from the northern seashore of Japan. J Appl Phycol 25:1159–1169Google Scholar
  86. Nomura T, Kikuchi M, Kubodera A, Kawakami Y (1997) Proton-donative antioxidant activity of fucoxanthin with 1,1-diphenyl-2-picrylhydrazyl (DPPH). Biochem Mol Biol Int 42:361–370PubMedGoogle Scholar
  87. Okuzumi J, Nishino H, Murakoshi M, Iwashima A, Tanaka Y, Yamane T, Fujita Y, Takahashi T (1990) Inhibitory effects of fucoxanthin, a natural carotenoid, on N-myc expression and cell cycle progression in human malignant tumor cells. Cancer Lett 55:75–81PubMedGoogle Scholar
  88. Okuzumi J, Takahashi T, Yamane T, Kitao Y, Inagake M, Ohya K, Nishino H, Tanaka Y (1993) Inhibitory effects of fucoxanthin, a natural carotenoid, on N-ethyl-N′-nitro-N-nitrosoguanidine-induced mouse duodenal carcinogenesis. Cancer Lett 68:159–168PubMedGoogle Scholar
  89. Orosa M, Torres E, Fidalgo P, Abalde J (2000) Production and analysis of secondary carotenoids in green algae. J Appl Phycol 12:553–556Google Scholar
  90. Pádua D, Rocha E, Gargiulo D, Ramos AA (2015) Bioactive compounds from brown seaweeds: Phloroglucinol, fucoxanthin and fucoidan as promising therapeutic agents against breast cancer. Phytochem Lett 14:91–98Google Scholar
  91. Park HJ, Lee MK, Park YB, Shin YC, Choi MS (2011) Beneficial effects of Undaria pinnatifida ethanol extract on diet-induced-insulin resistance in C57BL/6J mice. Food Chem Toxicol 49:727–733PubMedGoogle Scholar
  92. Pasquet V, Chérouvrier J-R, Farhat F, Thiéry V, Piot J-M, Bérard J-B, Kaas R, Serive B, Patrice T, Cadoret J-P, Picot L (2011) Study on the microalgal pigments extraction process: performance of microwave assisted extraction. Process Biochem 46:59–67Google Scholar
  93. Peng J, Yuan J-P, Wu C-F, Wang J-H (2011) Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: metabolism and bioactivities relevant to human health. Mar Drugs 9:1806–1828PubMedPubMedCentralGoogle Scholar
  94. Petrushkina M, Gusev E, Sorokin B, Zotko N, Mamaeva A, Filimonova A, Kulikovskiy M, Maltsev Y, Yampolsky I, Guglya E, Vinokurov V, Namsaraev Z, Kuzmin D (2017) Fucoxanthin production by heterokont microalgae. Algal Res 24:387–393Google Scholar
  95. Piovan A, Seraglia R, Bresin B, Caniato R, Filippini R (2013) Fucoxanthin from Undaria pinnatifida: Photostability and coextractive effects. Molecules 18:6298–6310PubMedPubMedCentralGoogle Scholar
  96. Qin S, Lin H, Jiang P (2012) Advances in genetic engineering of marine algae. Biotechnol Adv 30:1602–1613PubMedGoogle Scholar
  97. Radakovits R, Jinkerson RE, Darzins A, Posewitz MC (2010) Genetic engineering of algae for enhanced biofuel production. Eukaryot Cell 9:486–501PubMedPubMedCentralGoogle Scholar
  98. Reddy CRK, Jha B, Fujita Y, Ohno M (2008) Seaweed micropropagation techniques and their potentials: an overview. J Appl Phycol 20:609–617Google Scholar
  99. Rorrer GL, Cheney D (2004) Bioprocess engineering of cell and tissue cultures for marine seaweeds. Aquac Eng 32:11–14Google Scholar
  100. Rorrer GL, Modrell J, Zhi C, Yoo H-D, Nagle DN, Gerwick WH (1995) Bioreactor seaweed cell culture for production of bioactive oxylipins. J Appl Phycol 7:187–198Google Scholar
  101. Sachindra NM, Sato E, Maeda H, Hosokawa M, Niwano Y, Kohno M, Miyashita K (2007) Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J Agric Food Chem 55:8516–8522PubMedGoogle Scholar
  102. Sakai S, Sugawara T, Matsubara K, Hirata T (2009) Inhibitory effect of carotenoids on the degranulation of mast cells via suppression of antigen-induced aggregation of high affinity IgE receptors. J Biol Chem 284:28172–28179PubMedPubMedCentralGoogle Scholar
  103. Saravana PS, Getachew AT, Cho Y-J, Choi JH, Park YB, Woo HC, Chun BS (2017) Influence of co-solvents on fucoxanthin and phlorotannin recovery from brown seaweed using supercritical CO2. J Supercrit Fluids 120:295–303Google Scholar
  104. Satomi Y (2017) Antitumor and cancer-preventative function of fucoxanthin: a marine carotenoid. Anticancer Res 37:1557–1562PubMedGoogle Scholar
  105. Seely GR, Duncan MJ, Vidaver WE (1972) Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide. Mar Biol 12:184–188Google Scholar
  106. Shannon E, Abu-Ghannam N (2017) Optimisation of fucoxanthin extraction from Irish seaweeds by response surface methodology. J Appl Phycol 29:1027–1036Google Scholar
  107. Shimoda H, Tanaka J, Shan S-J, Maoka T (2010) Anti-pigmentary activity of fucoxanthin and its influence on skin mRNA expression of melanogenic molecules. J Pharm Pharmacol 62:1137–1145PubMedGoogle Scholar
  108. Shiratori K, Ohgami K, Ilieva I, Jin X-H, Koyama Y, Miyashita K, Yoshida K, Kase S, Ohno S (2005) Effects of fucoxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Exp Eye Res 81:422–428PubMedGoogle Scholar
  109. Sugawara T, Matsubara K, Akagi R, Mori M, Hirata T (2006) Antiangiogenic activity of brown algae fucoxanthin and its deacetylated product, fucoxanthinol. J Agric Food Chem 54:9805–9810PubMedGoogle Scholar
  110. Teas J, Irhimeh MR (2017) Melanoma and brown seaweed: an integrative hypothesis. J Appl Phycol 29:941–948PubMedGoogle Scholar
  111. Urikura I, Sugawara T, Hirata T (2011) Protective effect of fucoxanthin against UVB-induced skin photoaging in hairless mice. Biosci Biotechnol Biochem 75:757–760PubMedGoogle Scholar
  112. Wang J, Chen S, Xu S, Yu X, Ma D, Hu X, Cao X (2012) In vivo induction of apoptosis by fucoxanthin, a marine carotenoid, associated with down-Rregulating STAT3/EGFR signaling in sarcoma 180 (S180) xenografts-bearing mice. Mar Drugs 10:2055–2068PubMedPubMedCentralGoogle Scholar
  113. Woo M-N, Jeon S-M, Kim H-J, Lee M-K, Shin S-K, Shin YC, Park Y-B, Choi M-S (2010) Fucoxanthin supplementation improves plasma and hepatic lipid metabolism and blood glucose concentration in high-fat fed C57BL/6N mice. Chem Biol Interact 186:316–322PubMedGoogle Scholar
  114. Woo M-N, Jeon S-M, Shin YC, Lee M-K, Kang MA, Choi M-S (2009) Anti-obese property of fucoxanthin is partly mediated by altering lipid-regulating enzymes and uncoupling proteins of visceral adipose tissue in mice. Mol Nutr Food Res 53:1603–1611PubMedGoogle Scholar
  115. Wu H, Li T, Wang G, Dai S, He H, Xiang W (2016a) A comparative analysis of fatty acid composition and fucoxanthin content in six Phaeodactylum tricornutum strains from different origins. Chin J Oceanol Limnol 34:391–398Google Scholar
  116. Wu S, Xie X, Huan L, Zheng Z, Zhao P, Kuang J, Liu X, Wang G (2016b) Selection of optimal flocculant for effective harvesting of the fucoxanthin-rich marine microalga Isochrysis galbana. J Appl Phycol 28:1579–1588Google Scholar
  117. Xi-hua W, Song Q, Xin-ping L, Peng J, Cheng-kui Z, Mei Q (1998) High efficiency induction of callus and regeneration of sporophytes of Laminaria japonica (Phaeophyta). Chin J Oceanol Limnol 16:67–78Google Scholar
  118. Xia S, Wang K, Wan L, Li A, Hu Q, Zhang C (2013) Production, characterization, and antioxidant activity of fucoxanthin from the marine diatom Odontella aurita. Mar Drugs 11:2667–2681PubMedPubMedCentralGoogle Scholar
  119. Xiao X, Si X, Yuan Z, Xu X, Li G (2012) Isolation of fucoxanthin from edible brown algae by microwave-assisted extraction coupled with high-speed countercurrent chromatography. J Sep Sci 35:2313–2317PubMedGoogle Scholar
  120. Xuewu L, Kloareg B (1992) Explant exenisation for tissue culture in marine macroalgae. Chin J Oceanol Limnol 10:268–275Google Scholar
  121. Yamamoto K, Ishikawa C, Katano H, Yasumoto T, Mori N (2011) Fucoxanthin and its deacetylated product, fucoxanthinol, induce apoptosis of primary effusion lymphomas. Cancer Lett 300:225–234PubMedGoogle Scholar
  122. Yan X, Chuda Y, Suzuki M, Nagata T (1999) Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed. Biosci Biotechnol Biochem 63:605–607PubMedGoogle Scholar
  123. Ye G, Lu Q, Zhao W, Du D, Jin L, Liu Y (2014) Fucoxanthin induces apoptosis in human cervical cancer cell line HeLa via PI3K/Akt pathway. Tumor Biol 35:11261–11267Google Scholar
  124. Yeoman MM, Yeoman CL (1996) Manipulating secondary metabolism in cultured plant cells. New Phytol 134:553–569Google Scholar
  125. Yoshiko S, Hoyoku N (2007) Fucoxanthin, a natural carotenoid, induces G1 arrest and GADD45 gene expression in human cancer cells. In Vivo 21:305–309PubMedGoogle Scholar
  126. Yu R-X, Hu X-M, Xu S-Q, Jiang Z-J, Yang W (2011) Effects of fucoxanthin on proliferation and apoptosis in human gastric adenocarcinoma MGC-803 cells via JAK/STAT signal pathway. Eur J Pharmacol 657:10–19PubMedGoogle Scholar
  127. Zaragozá MC, López D, P. Sáiz M, Poquet M, Pérez J, Puig-Parellada P, Màrmol F, Simonetti P, Gardana C, Lerat Y, Burtin P, Inisan C, Rousseau I, Besnard M, Mitjavila MT (2008) Toxicity and antioxidant activity in vitro and in vivo of two Fucus vesiculosus extracts. J Agric Food Chem 567:7773–7780Google Scholar
  128. Zare AR, Solouki M, Omidi M, Irvani N, Nezad NM, Rezazadeh S (2010) Callus induction and plant regeneration in Ferula assafoetida L. (Asafetida), an endangered medicinal plant. Trakia J Sci 8:11–18Google Scholar
  129. Zhang Z, Zhang P, Hamada M, Takahashi S, Xing G, Liu J, Sugiura N (2008) Potential chemoprevention effect of dietary fucoxanthin on urinary bladder cancer EJ-1 cell line. Oncol Rep 20:1099–1103PubMedGoogle Scholar
  130. Zuo-Mei Y (1984) Studies on tissue culture of Laminaria japonica and Undaria pinnatifida. In: Bird CJ, Ragan MA (eds) Eleventh International Seaweed Symposium. Developments in Hydrobiology, vol 22. . Springer, Dordrecht, pp 314–316Google Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Institue of Medicinal PlantThe Academic Center for Education, Culture and Research (ACECR)KarajIran
  2. 2.Department of BotanyUniversity of OtagoDunedinNew Zealand

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