Chemoprotective effect of Spirulina (Arthrospira) against cyclophosphamide-induced mutagenicity in mice

Food and Chemical Toxicology

Volumn 46, Issue 2, 2008, Pages 567-574

  Chamorro Cevallos, G ^a   Garduno Siciliano L ^a   Barron B L ^a   Madrigal Bujaidar, E ^a   Cruz Vega, D E ^b   Pages, N ^c  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^c Faculty of Pharmacy   (France)

Author keywords

Antigenotoxicity; Cyclophosphamide; Dominant lethal mutation; Spirulina

Indexed keywords

ANTIMUTAGENIC AGENT; CYCLOPHOSPHAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREEDING; CONTROLLED STUDY; DOMINANT LETHAL MUTANT; DOMINANT LETHAL TEST; DRUG DOSE REGIMEN; FEMALE; GENETIC DAMAGE; GERM CELL; INHIBITION KINETICS; MALE; MOUSE; MUTAGENICITY; MUTATION; NIDATION; NONHUMAN; QUALITY CONTROL; SEX RATIO; SPIRULINA;

ANIMALS; ANTIMUTAGENIC AGENTS; CYCLOPHOSPHAMIDE; FEMALE; GENES, DOMINANT; MALE; MICE; MUTAGENS; PREGNANCY; SPERMATOZOA; SPIRULINA;

ANIMALIA; ARTHROSPIRA; MUS; SPIRULINA;

EID: 37449019325     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fct.2007.08.039     Document Type: Article

References (67)

1. Albert M., and Roussel C. Changes from puberty to adulthood in the concentration, motility and morphology of mouse epididymal spermatozoa. Int. J. Androl. 6 5 (1984) 446-460
2. Anderson D., Bishop J.B., Colin Garner R., Ostrosky-Wegman P., and Selby P.B. Cyclophosphamide: review of its mutagenicity for an assessment of potential germ cell risks. Mutat. Res. 330 1-2 (1995) 115-181
3. Anderson D., McGregor D.B., Purchase I.F.H., Hodge M.C.E., and Cuthbert J.A. Dominant-lethal test results with known mutagens in two laboratories. Mutation Res. 43 (1977) 231-246
4. Badary O.A., Abd-Ellah M.F., El-Mahdy M.A., Salama S.S., and Hamada F.H. Anticlastogenic activity of thymoquinone against benzo(a)pyrene in mice. Food Chem. Toxicol. 2007 (2007) 88-92
5. Belay A. Current knowledge on potential health benefits of Spirulina. J. Appl. Phycol. 5 (1993) 235-241
6. Belay A., Otta Y., Miyakawa K., and Shimamatsu H. The potential application of Spirulina (Arthrospira) as a nutritional and therapeutic supplement in health management. J.A.N.A. 5 2 (2002) 27-48
7. Benedetti S., Benvenuti F., Pagliarini S., Francogli S., Scoglio S., and Canestrati F. Antioxidant properties of a novel phycocyanin extract from the blue-green alga Aphanizomenon flos-aquae. Life Sci. 75 1-9 (2004) 2353-2362
8. Campanella L., Crescentini G., and Avino P. Chemical composition and nutritional evaluation of some natural and commercial food products based on Spirulina. Analusis 27 (1999) 533-540
9. Chamorro G., Pérez-Albiter M., Serrano-García N., Mares-Sámano J.J., and Rojas P. Spirulina maxima partially protects against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity. Nutr. Neurosci. 9 5-6 (2006) 207-212
10. Chamorro G., and Salazar M. Dominant lethal study of Spirulina maxima in male and female rats after short-term feeding. Phytother. Res. 10 (1996) 28-32
11. Chamorro G., Salazar M., Favila L., and Bourges H. Farmacología y Toxicología del alga Spirulina. Rev. Invest. Clín. 48 5 (1996) 389-399
12. Chamorro G., Salazar M., Gómez de Lima Araujo K., Pereira dos Santos C., Ceballos G., and Fabila-Castillo L. Actualización en la farmacología de Spirulina (Arthrospira), un alimento no convencional. Arch. Latinoam. Nutr. 52 3 (2002) 232-239
13. Chamorro G., Salazar M., Izquierdo E., Salazar S., and Ulloa G. Multi-generation study on reproduction and lactation in rats fed with Spirulina. Arch. Hydrobiol. Beih. 20 (1985) 165-171
14. Chamorro G.A., and Salazar M. Dominant lethal assay of Spirulina maxima in male CD-1 mice after short-term and prolonged-term feeding. J. Food Protect. 52 2 (1989) 125-127
15. Ciferri O. Spirulina, the edible microorganism. Microbiol. Rev. 47 4 (1983) 551-578
16. Dillon J.C., Phuc A.P., and Dubacq J.P. Nutritional value of the alga Spirulina. World Rev. Nutr. Diet. 77 (1995) 32-46
17. Ehling U., and Neuhäuser-Klaus A. Induction of specific-locus and dominant-lethal mutations by cyclophosphamide and combined cyclophosphamide-radiation treatments. Mutation Res. 199 (1988) 21-30
18. Ferguson L.R. Antimutagens as cancer chemoprotective agents in the diet. Mutat. Res. 307 1 (1994) 395-410
19. Flora S.D. Mechanisms of inhibitors of mutagenesis and carcinogens. Mutat. Res. 402 1-2 (1998) 151-158
20. Generoso W.M., Katoh M., Cain K.T., Hughes L.A., Foxworth L.B., Mitchell T.J., and Bishop J.A. Chromosome malsegregation and embryonic lethality induced by treatment of normally ovulated mouse oocytes with nocodazole. Mutat. Res. 210 2 (1989) 313-322
21. Gey K.F. Vitamins E plus C and interacting conutrients required for optimal health. A critical and constructive review of epidemiology and supplementation data regarding cardiovascular disease and cancer. Biofactors 7 1-2 (1998) 113-174
22. Green S., Auletta A., and Fabricant J. Current status of bioassays in genetic toxicology: dominant lethal assay. A report of the US EPA Gene-Tox Program. Mutat. Res. 154 (1985) 49-67
23. Green S., Lavappa K.S., Manandhar M., Sheu C., Whorton E., and Springer J.A. Guide for mutagenicity testing using the dominant lethal assay. Mutat. Res. 189 (1987) 167-176
24. Haque S.E., and Gilani K.M. Effect of ambroxol, Spirulina and vitamin-E in naphtalene induced cataract in female rats. Indian J. Physiol. Pharmacol. 49 1 (2005) 57-64
25. Hernández-Corona A., Meckes M., Chamorro G., and Barron M.L. Antiviral activity of Spirulina maxima against herpes simplex virus type 2. Antivir. Res. 56 3 (2002) 279-285
26. Higuchi H., Nakaoka M., Kawamura S., Kamita Y., Coda A., and Seki T. Application of computer-assisted sperm analysis system to elucidate lack of effects of cyclophosphamide on rat epididymal sperm motion. J. Toxicol. Sci. 26 2 (2001) 75-83
27. Hsiao G., Chou P.H., Shen M.Y., Chou D.S., Lin Ch., and Cheu J.R. C-Phycocyanin, a very potent and novel platelet aggregation inhibitor from Spirulina platensis. J. Agric. Food Chem. 53 20 (2005) 7734-7740 Abstract only
28. Hu Q. Industrial production of microalgal cell-mass and secondary products-major industrial species. In: Richmond A. (Ed). Handbook of microalgal culture: biotechnology and applied phycology (2004), Blackwell Science, Oxford, England 264-272
29. James D.A., and Smith D.M. Analysis of results from a collaborative study of the dominant lethal assay. Mutat. Res. 97 (1982) 303-314
30. Jeyaprakash K., and Chinnaswamy P. Effect of Spirulina and Liv-52 on cadmium induced toxicity in albino rats. Indian J. Exp. Biol. 43 (2005) 773-781
31. Khan M., Shobha J.C., Mohan I.K., Naidu M.U., Sundaram C., Singh S., Kuppusamy P., and Kutala B.K. Effect of Spirulina against doxorubicin-reduced cardiotoxicity. Phytother. Res. 19 12 (2005) 1030-1037
32. Khan M., Shobha J.C., Mohan I.K., Rao Naidu M.U., Prayag A., and Kutala V.K. Spirulina attenuates cyclosporine-induced nephrotoxicity in rats. J. Appl. Toxicol. 26 5 (2006) 444-451
33. Khan M., Varadhara S., Gansesa L.P., Shobha J.C., Naidu M.U., Parmandi N.L., Tridadapani S., Kutala B.J., and Kuppusamy P. C-phycocyanin protects against ischemia-reperfusion injury of heart through involvement of p38 and ERK signaling. Am. J. Physiol. Heart Circ. Physiol. 290 5 (2005) H2136-H2145
34. Krishna G., Petrere J., Anderson J., and Theis J. Use of cyclophosphamide as a positive control in dominant lethal and micronucleous assays. Mutat. Res. 335 3 (1995) 331-337
35. Kusamran W.R., Tepsuwan A., and Kupradeinun P. Antimutagenic and anticarcinogenic potentials of some Thai vegetables. Mutat. Res. 402 1-2 (1998) 247-258
36. Lu H.K., Hsieh C., Hsu J.J., Yang Y.K., and Chou H.N. Preventive effects of Spirulina platensis on skeletal muscle damage under exercise-induced oxidative stress. Eur. J. Appl. Physiol. 98 2 (2006) 220-226
37. Machemer L., and Lorke D. Experiences with the dominant lethal test in female mice: effects of alkylating agents and artificial sweeteners on pre-ovulatory oocyte stages. Mutat. Res. 29 (1975) 209-214
38. Mao K., Van de Water J., and Gershwin M.E. Effects of Spirulina-based dietary supplement on cytokine production from allergic rhinitis patients. J. Med. Food 8 1 (2005) 27-30
39. Mascher D., Paredes-Carvajal M.C., Torres-Durán P.V., Zamora-González J., Díaz-Zagoya J.C., and Juárez-Oropeza M.A. Ethanolic extract of Spirulina maxima alters the vasomotor reactivity of aortic rings form obese rats. Arch. Med. Res. 37 1 (2005) 50-57
40. Mathew B., Sankaranarayanan R., Fair P., Varhese C., Somanathan T., Amma P., and Nair M. Evaluation of the chemoprevention of oral cancer with Spirulina fusiformis. Nutr. Cancer 24 2 (1995) 197-202
41. Mendes R.L., Nobre B.P., Cardoso M.T., Pereira A., and Palavra A.F. Supercritical carbon dioxide extraction of compounds with pharmaceutical importance from microalgae. Inorganica. Chim. Acta 356 (2003) 328-334
42. Miranda M.S., Cintra R.G., Barros S.B.M., and Mancini-Filho J. Antioxidant activity of the microalga Spirulina maxima. Braz. J. Med. Res. 31 8 (1998) 1075-1079
43. Mohan I.K., Khan M., Shobha J.C., Naidu M.U., Prayag A., Kuppusamy P., and Kutala V.K. Protection against cisplatin-induced nephrotoxicity by Spirulina in rats. Cancer Chemother. Pharmacol. 58 6 (2006) 802-808 (Only abstract)
44. Nagaoka S., Shimizu K., Kaneko H., Shibayama F., Morikawa K., Kanamaru Y., Otsuka A., Hirahashi T., and Kato T. A novel protein C-phycocyanin plays a crucial role in the hypocholesterolemic action of Spirulina platensis concentrate in rats. J. Nutr. 135 10 (2005) 2425-2430
45. Ozdemir G., Karabay N.U., Dalay M., and Pazarbasi B. Anti-bacterial activity of volatile component and various extracts of Spirulina platensis. Phytother. Res. 18 9 (2004) 754-757
46. Patel A., Mishra S., and Glosh P.K. Antioxidant potential of C-phycocyanin isolated from cyanobacterial species Lyngbya, Phormidium and Spirulina sp. Indian J. Biochem. Biophys. 43 1 (2006) 25-31
47. Piñero-Estrada J.E., Bermejo-Bescós P., and Villar del Fresno A.M. Antioxidant activity of different fractions of Spirulina platensis protean extract II. Farmaco 56 5-7 (2001) 497-500
48. Premkumar K., Abraham S.K., Santhiya S.T., and Ramesh A. Protective effect of Spirulina fusiformis on chemical-induced genotoxicity in mice. Fitoterapia 75 1 (2003) 24-31
49. Premkumar K., Pachiappan A., Abraham S.K., Santhiya S.T., Gopinath P.M., and Ramesh A. Effect of Spirulina fusiformis on cyclophosphamide and mitomycin-C induced genotoxicity and oxidative stress in mice. Fitoterapia 72 8 (2001) 906-911
50. Preston R.J., Fennell T.R., Leber P., Sielken Jr. R.L., and Swenberg J.A. Recommendation of the genetic risk assessment for ethylene oxide exposures. J. Environ. Mol. Mutagen. 26 3 (1995) 189-202
51. Qishen P., Baojiang G., and Kolman A. Radioprotective effect of extract form Spirulina platensis in mouse bone marrow cell studied by using the micronucleus test. Toxicol. Lett. 48 (1989) 165-169
52. Remirez D., Fernandez V., Tapia G., González R., and Videla L.A. Influence of C-phycocyanin on hepatocellular parameters related to liver oxidative stress and Kupffer cell functioning. Inflamm. Res. 51 7 (2002) 351-356
53. Romay C., Armesto J., Remirez D., González R., Ledon N., and Garcia I. Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae. Inflamm Res. 47 1 (1998) 36-41
54. Romay C., Ledón N., and González R. Further studies on anti-inflammatory activity of phycocyanin in some animal models of inflammation. Inflamm. Res. 47 8 (1998) 334-338
55. Ruiz-Flores L.E., Madrigal-Bujaidar E., Salazar M., and Chamorro G. Anticlastogenic effect of Spirulina maxima extract on the micronuclei induced by maleic hydrazide in Tradescantia. Life Sci. 72 12 (2003) 1345-1351
56. Saha S.K., Misbahuddin M., Khatu R., and Mammum I.R. Effect of hexane extract of Spirulina in the removal of arsenic form isolated liver tissues of rat. Mymensingh. Med. J. 14 2 (2005) 191-195
57. Salazar M., and Chamorro G. Study of lethal dominant of Spirulina maxima in male rats. Sci. Aliments 10 (1990) 713-718
58. Salazar M., Chamorro G., Salazar S., and Steele C.E. Effect of Spirulina maxima consumption on reproduction and peri- and postnatal development in rats. Food Chem. Toxicol. 34 4 (1996) 353-359
59. Schwartz J., and Shklar G. Regression of experimental hamster cancer by betacarotene and alga extract. J. Oral Maxillofac. Surg. 45 (1987) 510-515
60. Schwartz J., Shklar G., Reid S., and Trickler D. Prevention of experimental oral cancer by extracts or Spirulina-Dunaliela algae. Nutr. Cancer 11 (1988) 127-134
61. Selvakumar E., Prahalatan C., Sudharsan P.T., and Varalakshmi P. Chemoprotective effect of lipoic acid against cyclophosphamide-induced changes in the rat sperm. Toxicology 217 1-2 (2006) 71-78
62. Shiraki M., Hara Y., Osawa T., Kuman H., Nakayama T., and Wawakishi S. Antioxidative and antimutagenic effects of the theaflavins from black tea. Mutat. Res. 323 1-2 (1994) 29-39
63. Upasani C.D., and Balaraman R. Protective effect of Spirulina on lead induced deleterious changes in the lipid peroxidation and endogenous antioxidants in rats. Phytother. Res. 17 4 (2003) 330-334
64. Vadiraja B.B., Gaikward N.W., and Madyastha K.M. Hepatoprotective effect of C-phycocyanin: protection for carbon tetrachloride and r-(+)-pulgeone-mediated hepatotoxicity in rats. Biochem. Biophys. Res. Commun. 249 2 (1998) 428-431
65. Vadiraja B.B., and Madyastha K.M. C-phycocyanin: a potent peroxyl radical scavenger. Biochem. Biophys. Res. Commun. 275 (2000) 20-25
66. Wang Y., Chang C., Chou J., Chen H.L., Deng X., Harvey B.K., Caded J.L., and Bickford P.C. Dietary supplementation with blueberries, spinach, or Spirulina reduces ischemic brain damage. Exp. Neurol. 193 (2005) 75-84
67. Wu L.C., Ho J.A., Shieh M.C., and Lu I.W. Antioxidant and antiproliferative activities of Spirulina and Chlorella water extracts. J. Agric. Food Chem. 53 (2005) 4207-4212