Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamide in mice germ cells

Toxicology

Volumn 248, Issue 2-3, 2008, Pages 96-103

  Tripathi, D N ^a   Jena, G B ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

Author keywords

Astaxanthin; Cyclophosphamide; Sperm comet; Testis; TUNEL assay

Indexed keywords

ASTAXANTHIN; CYCLOPHOSPHAMIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DRUG ACTIVITY; EVALUATION; GERM CELL; HISTOLOGY; MALE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; SPERMATOZOON; SPERMATOZOON COUNT; TESTIS; TESTIS INJURY; TESTIS WEIGHT; TREATMENT DURATION;

ANIMALS; ANTIMUTAGENIC AGENTS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; BODY WEIGHT; COMET ASSAY; CYCLOPHOSPHAMIDE; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ANTAGONISM; EPIDIDYMIS; IN SITU NICK-END LABELING; INJECTIONS, INTRAPERITONEAL; MALE; MICE; ORGAN SIZE; SPERM COUNT; SPERM HEAD; TESTIS; XANTHOPHYLLS;

ANIMALIA; MUS;

EID: 43849092492     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2008.03.015     Document Type: Article

References (71)

1. Adams Jr. J.D., and Klaidman L.K. Acrolein-induced oxygen radical formation. Free. Radic. Biol. Med. 15 (1993) 187-193
2. Aguilar-Mahecha A., Hales B.F., and Robaire B. Chronic cyclophosphamide treatment alters the expression of stress response genes in rat male germ cells. Biol. Reprod. 66 (2002) 1024-1032
3. Aitken R.J., Gordon E., Harkiss D., Twigg J.P., Milne P., Jennings Z., and Irvine D.S. Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol. Reprod. 59 (1998) 1037-1046
4. Anderson D., Bishop J.B., Garner R.C., Ostrosky-Wegman P., and Selby P.B. Cyclophosphamide: review of its mutagenicity for an assessment of potential germ cell risks. Mutat. Res. 330 (1995) 115-181
5. Auroux M., Dulioust E., Selva J., and Rince P. Cyclophosphamide in the F0 male rat: physical and behavioral changes in three successive adult generations. Mutat. Res. 229 (1990) 189-200
6. Barton T.S., Robaire B., and Hales B.F. Epigenetic programming in the preimplantation rat embryo is disrupted by chronic paternal cyclophosphamide exposure. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 7865-7870
7. Baume P., Vincent P.C., Fenton B., and Nicholls A. Effect of nitrogen mustard on gastric secretion in the rat. Am. J. Dig. Dis. 8 (1963) 330-336
8. Bennedsen M., Wang X., Willen R., Wadstrom T., and Andersen L.P. Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunol. Lett. 70 (1999) 185-189
9. Bianchi L., Tateo F., Pizzala R., Stivala L.A., Grazia Verri M., Melli R., and Santamaria L. Carotenoids reduce the chromosomal damage induced by bleomycin in human cultured lymphocytes. Anticancer Res. 13 (1993) 1007-1010
10. Borgmann A., Zinn C., Hartmann R., Herold R., Kaatsch P., Escherich G., Moricke A., Henze G., and von Stackelberg A. Secondary malignant neoplasms after intensive treatment of relapsed acute lymphoblastic leukaemia in childhood. Eur. J. Cancer 44 (2007) 257-268
11. Brown C.D., Forman C.L., McEuen S.F., and Miller M.G. Metabolism and testicular toxicity of 1,3-dinitrobenzene in rats of different ages. Fundam. Appl. Toxicol. 23 (1994) 439-446
12. Burruel V.R., Yanagimachi R., and Whitten W.K. Normal mice develop from oocytes injected with spermatozoa with grossly misshapen heads. Biol. Reprod. 55 (1996) 709-714
13. Cai L., Hales B.F., and Robaire B. Induction of apoptosis in the germ cells of adult male rats after exposure to cyclophosphamide. Biol. Reprod. 56 (1997) 1490-1497
14. Charak B.S., Gupta R., Mandrekar P., Sheth N.A., Banavali S.D., Saikia T.K., Gopal R., Dinshaw K.A., and Advani S.H. Testicular dysfunction after cyclophosphamide-vincristine-procarbazine-prednisolone chemotherapy for advanced Hodgkin's disease. A long-term follow-up study. Cancer 65 (1990) 1903-1906
15. Chew B.P., Park J.S., Wong M.W., and Wong T.S. A comparison of the anticancer activities of dietary beta-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res. 19 (1999) 1849-1853
16. Codrington A.M., Hales B.F., and Robaire B. Exposure of male rats to cyclophosphamide alters the chromatin structure and basic proteome in spermatozoa. Hum. Reprod. 22 (2007) 1431-1442
17. Comhaire F.H., and Mahmoud A. The role of food supplements in the treatment of the infertile man. Reprod. Biomed. Online 7 (2003) 385-391
18. Crook T.R., Souhami R.L., and McLean A.E. Cytotoxicity, DNA cross-linking, and single strand breaks induced by activated cyclophosphamide and acrolein in human leukemia cells. Cancer Res. 46 (1986) 5029-5034
19. Das U.B., Mallick M., Debnath J.M., and Ghosh D. Protective effect of ascorbic acid on cyclophosphamide-induced testicular gametogenic and androgenic disorders in male rats. Asian J. Androl. 4 (2002) 201-207
20. Daubrawa F., Sies H., and Stahl W. Astaxanthin diminishes gap junctional intercellular communication in primary human fibroblasts. J. Nutr. 135 (2005) 2507-2511
21. de Jong W.K., Groen H.J., Koolen M.G., Biesma B., Willems L.N., Kwa H.B., van Bochove A., van Tinteren H., and Smit E.F. Phase III study of cyclophosphamide, doxorubicin, and etoposide compared with carboplatin and paclitaxel in patients with extensive disease small-cell lung cancer. Eur. J. Cancer 43 (2007) 2345-2350
22. de la Mora G.I., Arredondo-Figueroa J.L., Barriga-Sosa Ide L., Bazan-Arias J., and Vernon-Carter J. Effects of the dietary incorporation of carotenoid pigments on gonad development and oocyte maturity in females of rainbow trout (Oncorhynchus mykiss, Walbaum, 1972). Arch. Latinoam. Nutr. 54 (2004) 235-240
23. Di Mascio P., Devasagayam T.P., Kaiser S., and Sies H. Carotenoids, tocopherols and thiols as biological singlet molecular oxygen quenchers. Biochem. Soc. Trans. 18 (1990) 1054-1056
24. Elangovan N., Chiou T.J., Tzeng W.F., and Chu S.T. Cyclophosphamide treatment causes impairment of sperm and its fertilizing ability in mice. Toxicology 222 (2006) 60-70
25. Fahey J.W., Stephenson K.K., Dinkova-Kostova A.T., Egner P.A., Kensler T.W., and Talalay P. Chlorophyll, chlorophyllin and related tetrapyrroles are significant inducers of mammalian phase 2 cytoprotective genes. Carcinogenesis 26 (2005) 1247-1255
26. Fraiser L.H., Kanekal S., and Kehrer J.P. Cyclophosphamide toxicity characterizing and avoiding the problem. Drugs 42 (1991) 81-95
27. Ghosh D., Das U.B., Ghosh S., Mallick M., and Debnath J. Testicular gametogenic and steroidogenic activities in cyclophosphamide treated rat: a correlative study with testicular oxidative stress. Drug Chem. Toxicol. 25 (2002) 281-292
28. Goto S., Kogure K., Abe K., Kimata Y., Kitahama K., Yamashita E., and Terada H. Efficient radical trapping at the surface and inside the phospholipid membrane is responsible for highly potent antiperoxidative activity of the carotenoid astaxanthin. Biochim. Biophys. Acta 1512 (2001) 251-258
29. Griveau J.F., Dumont E., Renard P., Callegari J.P., and Le Lannou D. Reactive oxygen species, lipid peroxidation and enzymatic defence systems in human spermatozoa. J. Reprod. Fertil. 103 (1995) 17-26
30. Guerin M., Huntley M.E., and Olaizola M. Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol. 21 (2003) 210-216
31. Haines G.A., Hendry J.H., Daniel C.P., and Morris I.D. Germ cell and dose-dependent DNA damage measured by the comet assay in murine spermatozoaa after testicular X-irradiation. Biol. Reprod. 67 (2002) 854-861
32. Hemminki K., and Kallama S. Reactions of nitrogen mustards with DNA. IARC Sci. Publ. 78 (1986) 55-70
33. Higuchi H., Nakaoka M., Katsuda Y., Kawamura S., Kato T., and Matsuo M. Collaborative assessment of optimal administration period and parameters to detect effects on male fertility in the rat: effects of cyclophosphamide on the male reproductive system. J. Toxicol. Sci. 20 (1995) 239-249
34. Hix L.M., Frey D.A., McLaws M.D., Osterlie M., Lockwood S.F., and Bertram J.S. Inhibition of chemically-induced neoplastic transformation by a novel tetrasodium diphosphate astaxanthin derivative. Carcinogenesis 26 (2005) 1634-1641
35. Hix L.M., Lockwood S.F., and Bertram J.S. Bioactive carotenoids: potent antioxidants and regulators of gene expression. Redox. Rep. 9 (2004) 181-191
36. Hoorweg-Nijman J.J., Delemarre-van de Waal H.A., de Waal F.C., and Behrendt H. Cyclophosphamide-induced disturbance of gonadotropin secretion manifesting testicular damage. Acta Endocrinol. (Copenh) 126 (1992) 143-148
37. Hussein G., Goto H., Oda S., Sankawa U., Matsumoto K., and Watanabe H. Antihypertensive potential and mechanism of action of astaxanthin: III. Antioxidant and histopathological effects in spontaneously hypertensive rats. Biol. Pharm. Bull. 29 (2006) 684-688
38. Hussein G., Nakagawa T., Goto H., Shimada Y., Matsumoto K., Sankawa U., and Watanabe H. Astaxanthin ameliorates features of metabolic syndrome in SHR/NDmcr-cp. Life Sci. 80 (2007) 522-529
39. Ichikawa T., Oeda T., Ohmori H., and Schill W.B. Reactive oxygen species influence the acrosome reaction but not acrosin activity in human spermatozoa. Int. J. Androl. 22 (1999) 37-42
40. Ikeuchi M., Koyama T., Takahashi J., and Yazawa K. Effects of astaxanthin supplementation on exercise-induced fatigue in mice. Biol. Pharm. Bull. 29 (2006) 2106-2110
41. Ikeuchi M., Koyama T., Takahashi J., and Yazawa K. Effects of astaxanthin in obese mice fed a high-fat diet. Biosci. Biotechnol. Biochem. 71 (2007) 893-899
42. Katoh C., Kitajima S., Saga Y., Kanno J., Horii I., and Inoue T. Assessment of quantitative dual-parameter flow cytometric analysis for the evaluation of testicular toxicity using cyclophosphamide- and ethinylestradiol-treated rats. J. Toxicol. Sci. 27 (2002) 87-96
43. Kenney L.B., Laufer M.R., Grant F.D., Grier H., and Diller L. High risk of infertility and long term gonadal damage in males treated with high dose cyclophosphamide for sarcoma during childhood. Cancer 91 (2001) 613-621
44. Kim J.H., Kim Y.S., Song G.G., Park J.J., and Chang H.I. Protective effect of astaxanthin on naproxen-induced gastric antral ulceration in rats. Eur. J. Pharmacol. 514 (2005) 53-59
45. Kishikawa H., Tateno H., and Yanagimachi R. Chromosome analysis of BALB/c mouse spermatozoa with normal and abnormal head morphology. Biol. Reprod. 61 (1999) 809-812
46. Konca K., Lankoff A., Banasik A., Lisowska H., Kuszewski T., Gozdz S., Koza Z., and Wojcik A. A cross-platform public domain PC image-analysis program for the comet assay. Mutat. Res. 534 (2003) 15-20
47. Kurihara H., Koda H., Asami S., Kiso Y., and Tanaka T. Contribution of the antioxidative property of astaxanthin to its protective effect on the promotion of cancer metastasis in mice treated with restraint stress. Life Sci. 70 (2002) 2509-2520
48. Lai J.P., Jiang Y., He X.W., Huang J.C., and Chen F. Separation and determination of astaxanthin from microalgal and yeast samples by molecularly imprinted microspheres. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 804 (2004) 25-30
49. Li D.J., Xu Z.S., Zhang Z.H., and Huang Q.Y. Antagonistic effects of vitamin E on the testicular injury by cyclophosphamide in mice. Zhonghua Nan Ke Xue 12 (2006) 318-322
50. Matsui H., Mitsumori K., Yasuhara K., Onodera H., Shimo T., and Takahashi M. Morphological evaluation of cyclophosphamide testicular toxicity in rats using quantitative morphometry of spermatogenic cycle stages. J. Toxicol. Sci. 20 (1995) 407-414
51. McLachlan R.I., O'Donnell L., Meachem S.J., Stanton P.G., de Kretser D.M., Pratis K., and Robertson D.M. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog. Horm. Res. 57 (2002)
52. McNulty H.P., Byun J., Lockwood S.F., Jacob R.F., and Mason R.P. Differential effects of carotenoids on lipid peroxidation due to membrane interactions: X-ray diffraction analysis. Biochim. Biophys. Acta 1768 (2007) 167-174
53. Miki W. Biological functions and activities of animal carotenoids. Pure Appl. Chem. 63 (1991) 141-146
54. Miniati I., and Matucci Cerinic M. Pulmonary fibrosis in systemic sclerosis: is treatment with cyclophosphamide more effective than placebo?. Nat. Clin. Pract. Rheumatol. 3 (2007) 372-373
55. Naito Y., Uchiyama K., Aoi W., Hasegawa G., Nakamura N., Yoshida N., Maoka T., Takahashi J., and Yoshikawa T. Prevention of diabetic nephropathy by treatment with astaxanthin in diabetic db/db mice. Biofactors 20 (2004) 49-59
56. Olive P.L. DNA damage and repair in individual cells: applications of the comet assay in radiobiology. Int. J. Radiat. Biol. 75 (1999) 395-405
57. Perini P., Calabrese M., Rinaldi L., and Gallo P. The safety profile of cyclophosphamide in multiple sclerosis therapy. Expert Opin. Drug Saf. 6 (2007) 183-190
58. Rekhadevi P.V., Sailaja N., Chandrasekhar M., Mahboob M., Rahman M.F., and Grover P. Genotoxicity assessment in oncology nurses handling anti-neoplastic drugs. Mutagenesis 22 (2007) 395-401
59. Schimenti K.J., Hanneman W.H., and Schimenti J.C. Evidence for cyclophosphamide-induced gene conversion and mutation in mouse germ cells. Toxicol. Appl. Pharmacol. 147 (1997) 343-350
60. Selvakumar E., Prahalathan C., Sudharsan P.T., and Varalakshmi P. Chemoprotective effect of lipoic acid against cyclophosphamide-induced changes in the rat sperm. Toxicology 217 (2006) 71-78
61. Sikka S.C. Relative impact of oxidative stress on male reproductive function. Curr. Med. Chem. 8 (2001) 851-862
62. Sikka S.C. Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J. Androl. 25 (2004) 5-18
63. Singh N.P., Muller C.H., and Berger R.E. Effects of age on DNA double-strand breaks and apoptosis in human sperm. Fertil. Steril. 80 (2003) 1420-1430
64. Starzl T.E., Putnam C.W., Halgrimson C.G., Schroter G.T., Martineau G., Launois B., Corman J.L., Penn I., Booth Jr. A.S., Groth C.G., and Porter K.A. Cyclophosphamide and whole organ transplantation in human beings. Surg. Gynecol. Obstet. 133 (1971) 981-991
65. Sulkowska M., Sulkowski S., Skrzydlewska E., and Farbiszewski R. Cyclophosphamide-induced generation of reactive oxygen species. Comparison with morphological changes in type II alveolar epithelial cells and lung capillaries. Exp. Toxicol. Pathol. 50 (1998) 209-220
66. Trasler J.M., Hales B.F., and Robaire B. Chronic low dose cyclophosphamide treatment of adult male rats: effect on fertility, pregnancy outcome and progeny. Biol. Reprod. 34 (1986) 275-283
67. Uber W.E., Self S.E., Van Bakel A.B., and Pereira N.L. Acute antibody-mediated rejection following heart transplantation. Am. J. Transplant. 7 (2007) 2064-2074
68. Vikram A., Tripathi D.N., Ramarao P., and Jena G.B. Evaluation of streptozotocin genotoxicity in rats from different ages using the micronucleus assay. Regul. Toxicol. Pharmacol. 49 (2007) 238-244
69. Vikram A., Tripathi D.N., Ramarao P., and Jena G.B. Intervention of d-glucose ameliorates the toxicity of streptozotocin in accessory sex organs of rat. Toxicol. Appl. Pharmacol. 226 (2008) 84-93
70. Zhang Q.H., Wu C.F., Duan L., and Yang J.Y. Protective effects of ginsenoside Rg(3) against cyclophosphamide-induced DNA damage and cell apoptosis in mice. Arch. Toxicol. 82 (2007) 117-123
71. Zhang X., Pan L., Wei X., Gao H., and Liu J. Impact of astaxanthin-enriched algal powder of Haematococcus pluvialis on memory improvement in BALB/c mice. Environ. Geochem. Health 29 (2007) 483-489