In vitro toxicity of microalgal and cyanobacterial strains of interest as food source

Journal of Applied Phycology

Volumn 29, Issue 1, 2017, Pages 199-209

  Niccolai, Alberto ^a   Bigagli, Elisabetta ^a   Biondi, Natascia ^a   Rodolfi, Liliana ^a   Cinci, Lorenzo ^a   Luceri, Cristina ^a   Tredici, Mario R ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Brine shrimp bioassay; Fibroblasts; Food; Microalgae; Toxicity

Indexed keywords

EID: 84983380334     PISSN: 09218971     EISSN: 15735176     Source Type: Journal    
DOI: 10.1007/s10811-016-0924-2     Document Type: Article

References (67)

1. Abbott WS (1987) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc 3:302–303
2. AECOSAN (Agencia Española de Consumo, Seguridad Alimentaria y Nutrición) (2014) Authorisation to market Tetraselmis chuii. Ministry of Health, Social Services and Equality
3. AESAN (Agencia Española de Seguridad Alimentaria y Nutrición) (2013) Report of the scientific committee of the Spanish agency for food safety and nutrition on a request for initial assessment for marketing of the marine microalgae Tetraselmis chuii under regulation (EC) No 258/97 on novel foods and novel food ingredients. Report AESAN-2013-001. Revista del Comité Científico de la AESAN 18:11–28
4. Anderson JE, Goetz CM, McLaughlin JL, Suffness M (1991) A blind comparison of simple bench-top bioassays and human tumour cell cytotoxicities as antitumor prescreens. Phytochem Anal 2:107–111
5. Arad SM, Levy-Ontman O (2010) Red microalgal cell-wall polysaccharides: biotechnological aspects. Curr Opin Biotech 21:358–364
6. Ballot A, Fastner J, Lentz M, Wiedner C (2010a) First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany. Toxicon:56:6964–56:6971
7. Ballot A, Fastner J, Wiedner C (2010b) Paralytic shellfish poisoning toxin-producing cyanobacterium Aphanizomenon gracile in Northeast Germany. Appl Environ Microb 76:1173–1180
8. Batista AP, Gouveia L, Bandarra NM, Franco JM, Raymundo A (2013) Comparison of microalgal biomass profiles as novel functional ingredient for food products. Algal Res 2:164–173
9. Bechelli J, Coppage M, Rosell K, Liesveld J (2011) Cytotoxicity of algae extracts on normal and malignant cells. Leukemia Res 2011:1–7
10. Becker EW (2007) Microalgae as a source of protein. Biotechnol Adv 25:207–210
11. Biondi N, Piccardi R, Margheri MC, Rodolfi L, Smith GD, Tredici MR (2004) Evaluation of Nostoc strain ATCC 53789 as a potential source of natural pesticides. Appl Environ Microb 70:3313–3320
12. Biondi N, Tredici MR, Taton A, Wilmotte A, Hodgson DA, Losi D, Marinelli F (2008) Cyanobacteria from benthic mats of Antarctic lakes as a source of new bioactivities. J Appl Microbiol 105:105–115
13. Bishop WM, Zubeck HM (2012) Evaluation of microalgae for use as nutraceuticals and nutritional supplements. J Nutr Food Sci 2:1–6
14. Carballo JL, Hernández-Inda ZL, Pérez P, García-Grávalos MD (2002) A comparison between two brine shrimp assays to detect in vitro cytotoxicity in marine natural products. BMC Biotechnol 2:17
15. Carmichael WW (1992) Cyanobacteria secondary metabolites—the cyanotoxins. J Appl Bacteriol 72:445–459
16. Chamorro-Cevallos G, Barron BL, Vazquez-Sanchez J (2007) Toxicologic studies and antitoxic properties of Spirulina. In: Gershwin ME, Belay A (eds) Spirulina in human nutrition and health. CRC Press, Boca Raton, pp. 27–45
17. Chini Zittelli G, Biondi N, Rodolfi L, Tredici MR (2013) Photobioreactors for mass production of microalgae. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: Applied phycology and biotechnology, 2nd edn. Wiley, Oxford, pp. 225–266
18. Commonwealth of Australia Gazette (2007) Australia New Zealand Food Standards Code, Amendment No. 95–2007. Commonwealth of Australia Gazette No. FSC 36 Thursday, 11 October 2007, p 3
19. Del Campo JA, García-González M, Guerrero MG (2007) Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biot 74:1163–1174
20. EFSA (European Food Safety Authority) (2014) Scientific opinion on the safety of astaxanthin-rich ingredients (AstaREAL A1010 and AstaREAL L10) as novel food ingredients. EFSA J 12:3757
21. European Union (1997) Regulation (EC) No 258/97 of the European Parliament and of the Council of 27 January 1997 concerning novel foods and novel food ingredients. Official Journal of the European Union, L 43/1 of 14 February 1997, pp 1–6
22. European Union (2005) Summary of notifications received by the Commission until 31 December 2004 pursuant to Article 5 of Regulation (EC) No 258/97 of the European Parliament and of the Council. Official Journal of the European Union, C 208/2, 25.8.2005
23. European Union (2010) Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Union, L 276/33 of 20 October 2010, pp 1–47
24. European Union (2015) P8_TA-PROV(2015)0380. European Parliament legislative resolution of 28 October 2015 on the proposal for a regulation of the European Parliament and of the Council on novel foods (COM(2013)0894 – C7–0487/2013–2013/0435(COD)). http://www.europarl.europa.eu/sides/getDoc.do?pubRef=-//EP//TEXT+TA+P8-TA-2015-0380+0+DOC+XML+V0//EN#ref_1_1. Accessed 25 Jan 2016
25. European Union, Novel Food catalogue http://ec.europa.eu/food/safety/novel_food/catalogue/search/public/index.cfm. Accessed 12 Feb 2016
26. Fackenthal JD, Godley LA (2008) Aberrant RNA splicing and its functional consequences in cancer cells. Dis Model Mech 1:37–42
27. FDA (2014) Guidance for industry. Considerations regarding substances added to foods, including beverages and dietary supplements. U.S. Department of Health and Human Services, Food and Drug Administration, Center for Food Safety and Applied Nutrition, January 2014
28. Federal Food, Drug, And Cosmetic Act, as amended through P.L. 113–5, enacted March 13, 2013. Chapter II—definitions, Section 201, (s)
29. Ferreira FMB, Franco Soler JM, Fidalgo ML, Fernández-Vila P (2001) PSP toxins from Aphanizomenon flos-aquae (cyanobacteria) collected in the Crestuma-lever reservoir (Douro river, northern Portugal). Toxicon 39:757–761
30. FSANZ, Proposal P1024 - Revision of the regulation of nutritive substances & novel foods Supporting document 2. Assessment of risks and safety data requirements for new foods. http://www.foodstandards.gov.au/code/proposals/pages/proposalp1024revisio5756.aspx. Accessed 29 June 2016
31. FSANZ (2016) Novel food-record of views. Record of views formed by the FSANZ. Novel Foods Reference Group or the Advisory Committee on Novel Foods, March 2016
32. Gardeva E, Toshkova R, Yossifova L, Minkova K, Gigova L (2012) Cytotoxic and apoptogenic potential of red microalgal polysaccharides. Biotechnol Biotec Eq. 26:3167–3172
33. Gilroy DJ, Kauffman KW, Hall RA, Huang X, Chu FS (2000) Assessing potential health risks from microcystin toxins in blue-green algae dietary supplements. Environ Health Persp 108:435–439
34. Giovannelli L, Innocenti M, Santamaria AR, Bigagli E, Pasqua G, Mulinacci N (2014) Antitumoural activity of viniferin-enriched extracts from Vitis vinifera L. cell cultures. Nat Prod Res 28:2006–2016
35. Goh SH, Alitheen NBM, Yusoff FM, Yap SK, Loh SP (2014) Crude ethyl acetate extract of marine microalga, Chaetoceros calcitrans, induces apoptosis in MDA-MB-231 breast cancer cells. Pharmacogn Mag 10:1–8
36. Golakoti T, Ogino J, Heltzel CE, Le Husebo T, Jensen CM, Larsen LK, Patterson GML, Moore RE, Mooberry SL (1995) Structure determination, conformational analysis, chemical stability studies, and antitumor evaluation of the cryptophycins. Isolation of 18 new analogs from Nostoc sp. strain GSV 224. J Am Chem Soc 117:12030–12049
37. Guilhermino L, Diamantino T, Silva MC, Soares AMVM (2000) Acute toxicity test with Daphnia magna: an alternative to mammals in the prescreening of chemical toxicity? Ecotox Environ Safe 46:357–362
38. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239
39. Guccione A, Biondi N, Sampietro G, Rodolfi L, Bassi N, Tredici MR (2014) Chlorella for protein and biofuels: from strain selection to outdoor cultivation in a green wall panel photobioreactor. Biotechnol Biofuels 7:84
40. Guiry MD (2012) How many species of algae are there? J Phycol 48:1057–1063
41. Han D, Zhongyang D, Lu F, Zhengyu H (2013) Biology and biotechnology of edible Nostoc. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: Applied phycology and biotechnology, 2nd edn. Wiley, Oxford, pp. 433–444
42. Heussner AH, Mazija L, Fastner J, Dietrich DR (2012) Toxin content and cytotoxicity of algal dietary supplements. Toxicol Appl Pharm 265:263–271
43. Hisem D, Hrouzek P, Tomek P, Tomsícková J, Zapomelová E, Skácelová K, Lukesová A, Kopecký J (2011) Cyanobacterial cytotoxicity versus toxicity to brine shrimp Artemia salina. Toxicon 57:76–83
44. Hrouzek P, Tomek P, Lukesová A, Urban J, Voloshko L, Pushparaj B, Lukavský J, Stys D, Kopecký J (2011) Cytotoxicity and secondary metabolites production in terrestrial Nostoc strains originating from different climatic/geographic regions and habitats: is their cytotoxicity environmentally dependent? Environ Toxicol 26:345–358
45. Hrouzek P, Kapuścik A, Vacek J, Voráčová K, Paichlová J, Kosina P, Voloshko L, Ventura S, Kopecký J (2016) Cytotoxicity evaluation of large cyanobacterial strain set using selected human and murine in vitro cell models. Ecotox Environ Safe 124:177–185
46. Ibañez E, Cifuentes A (2013) Benefits of using algae as natural sources of functional ingredients. J Sci Food Agr 93:703–709
47. Jaki B, Orjala J, Bürgi HR, Sticher O (1999) Biological screening of cyanobacteria for antimicrobial and molluscicidal activity, brine shrimp lethality, and cytotoxicity. Pharm Biol 37:138–143
48. Jallepalli PV, Lengauer C (2001) Chromosome segregation and cancer: cutting through the mystery. Nat Rev Cancer 1:109–117
49. Lagarto Parra A, Yhebra RS, Sardiñas IG, Buela LI (2001) Comparative study of the assay of Artemia salina L. and the estimate of the medium lethal dose (LD50 value) in mice, to determine oral acute toxicity of plant extracts. Phytomedicine 8:395–400
50. Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390
51. Lincoln RA, Strupinski K, Walker JM (1996) The use of Artemia nauplii (brine shrimp larvae) to detect toxic compounds from microalgal cultures. Int J Pharmacogn 34:384–389
52. Lopes VR, Schmidtke M, Fernandes MH, Martins R, Vasconcelos V (2011) Cytotoxicity in L929 fibroblasts and inhibition of herpes simplex virus type 1 Kupka by estuarine cyanobacteria extracts. Toxicol in Vitro 25:944–950
53. Matsushima R, Yoshizawa S, Watanabe MF, Harada KI, Furusawa M, Carmichael WW, Fujiki H (1990) In vitro and in vivo effects of protein phosphatase inhibitors, microcystins and nodularin, on mouse skin and fibroblasts. Biochem Bioph Res Co 171:867–874
54. Muller-Feuga A (2013) Microalgae for aquaculture: the current global situation and future trends. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: Applied phycology and biotechnology, 2nd edn. Wiley, Oxford, pp. 615–627
55. Panda D, Himes RH, Moore RE, Wilson L, Jordan MA (1997) Mechanism of action of the unusually potent microtubule inhibitor cryptophycin 1. Biochemistry 36:12948–12953
56. Papendorf O, Konig GM, Wright AD, Choris I, Oberemm A (1997) Mueggelone, a novel inhibitor of fish development from the fresh water cyanobacterium Aphanizomenon flos-aquae. J Nat Prod 60:1298–1300
57. Piccardi R, Frosini A, Tredici MR, Margheri MC (2000) Bioactivity in free-living and symbiotic cyanobacteria of the genus Nostoc. J Appl Phycol 12:543–547
58. Piccardi R, Margheri MC, Biondi N, Carotti S, Landini I, Mini E, Tredici MR (2001) Valutazione dell’attività citotossica di estratti e polisaccaridi cianobatterici in modelli cellulari in vitro. 21° Congresso Nazionale della Società Italiana di Chemioterapia, Florence, 2–5 December 2001
59. Prestegard SK, Oftedal L, Coyne RT, Nygaard G, Skjærven KH, Knutsen G, Døskeland SV, Herfindal L (2009) Marine benthic diatoms contain compounds able to induce leukemia cell death and modulate blood platelet activity. Mar Drugs 7:605–623
60. Rajasulochana P, Preethy V (2015) Glimpses on cosmetic applications using marine red algae. Int J Pharm Tech 7:9235–9242
61. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
62. Sleet RB, Brendel K (1985) Homogeneous populations of Artemia nauplii and their potential use for in vitro testing in developmental toxicology. Teratogen Carcin Mut 5:41–54
63. Solis PN, Wright CW, Anderson MM, Gupta MP, Phillipson JD (1993) A microwell cytotoxicity assay using Artemia salina (brine shrimp). Planta Med 59:250–252
64. Tredici MR, Biondi N, Ponis E, Rodolfi L, Chini Zittelli G (2009) Advances in microalgal culture for aquaculture feed and other uses. In: Burnell G, Allan G (eds) New technologies in aquaculture: improving production efficiency, quality and environmental management. Woodhead Publishing, Cambridge, pp. 610–676
65. Tredici MR, Rodolfi L, Sampietro G, Bassi N (2011) Low-cost photobioreactor for microalgae cultivation. Patent WO 2011/013104 A1
66. Vezie C, Benoufella F, Sivonen K, Bertru G, Laplanche A (1996) Detection of toxicity of cyanobacterial strains using Artemia salina and MicrotoxR assays compared with mouse bioassay results. Phycologia 35:198–202
67. Zarrouk C (1966) Contribution à l’étude d’une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et la photosynthèse de Spirulina maxima (Setch et Gardner) Geitler. Ph.D. thesis, Université de Paris, Paris