Copper chlorophyllin: A food colorant with bioactive properties?

Food Research International

Volumn 46, Issue 2, 2012, Pages 451-459

  Tumolo, Tathyana ^a   Lanfer Marquez, Ursula Maria ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Bioavailability; Biological activity; Copper chlorins; Copper chlorophyllin

Indexed keywords

ANTIMUTAGENIC; ANTIOXIDANT ACTIVITIES; BIOACTIVE PRODUCTS; BIOACTIVE PROPERTIES; BIOAVAILABILITY; CHLORINS; CHLOROPHYLLIN; COMPLEX MIXTURE; FOOD COLORANTS; HEALTH BENEFITS; HUMAN HEALTH; SCIENTIFIC RESEARCHES;

BIOACTIVITY; CHLOROPHYLL; COPPER; FOOD ADDITIVES; HEALTH; PORPHYRINS;

COPPER COMPOUNDS;

EID: 84858006700     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2011.10.031     Document Type: Article

References (89)

1. Abraham S.K., Sarma L., Kesavan P.C. Role of chlorophyllin as an in vivo anticlastogen: Protection against gamma-radiation and chemical clastogens. Mutation Research 1994, 322:209-212.
2. Ames B.N., McCann J., Yamasaki E. Methods for detecting carcinogens and mutagens with the Salmonella/mammalian-microsome mutagenicity test. Mutation Research 1975, 31:347-364.
3. ANVS Regulamento Técnico sobre atribuição de aditivos e seus limites máximos para alimentos 2008, Agência Nacional de Vigilância Sanitária - Brasil, Resolução RDC 64 de 16 de setembro de 2008.
4. Arimoto S., Fukuoka S., Itome C., Nakano H., Rai H., Hayatsu H. Binding of polycyclic planar mutagens to chlorophyllin resulting in inhibition of the mutagenic activity. Mutation Research 1993, 287:293-305.
5. Arimoto S., Kan-yama K., Rai H., Hayatsu H. Inhibitory effect of hemin, chlorophyllin and related pyrrole pigments on the mutagenicity of benzo[a]pyrene and its metabolites. Mutation Research 1995, 345:127-135.
6. Baxter J.H. Absorption of chlorophyll phytol in normal man and in patients with Refsum's disease. Journal of Lipid Research 1968, 9:636-641.
7. Bez G.C., Jordao B.Q., Vincentini V.E.P., Mantovani M.S. Investigation of genotoxic and antigenotoxic activities of chlorophylls and chlorophyllin in cultured V79 cells. Mutation Research 2001, 497:139-145.
8. Blum C.A., Xu M., Orner G.A., Díaz G.D., Li Q., Dashwood W.M., et al. Promotion versus suppression of rat colon carcinogenesis by chlorophyllin and chlorophyll: Modulation of apoptosis, cell proliferation, and β-catenin/Tcf signaling. Mutation Research 2003, 523-524:217-223.
9. Boloor K.K., Kamat J.P., Devasagayam T.P.A. Chlorophyllin as a protector of mitochondrial membranes against γ-radiation and photosensitization. Toxicology 2000, 155:63-71.
10. 1 bath treatment: An evaluation of reduced bioavailability vs. target organ protective mechanisms. Toxicology and Applied Pharmacology 1999, 158:141-151.
11. Breinholt V., Hendricks J., Pereira C., Arbogast D., Bailey G. Dietary chlorophyllin is a potent inhibitor of aflatoxin B, hepatocarcinogenesis in rainbow trout. Cancer Research 1995, 55:57-62.
12. 1: Complex formation with the carcinogen. Chemical Research in Toxicology 1995, 8(4):506-514.
13. Chernomorsky S., Rancourt R., Sahai D., Poretz R. Evaluation of commercial chlorophyllin copper complex preparations by liquid chromatography with photodiode array detection. Journal of AOAC International 1997, 80:433-435.
14. Chernomorsky S., Rancourt R., Virdi K., Segelman A., Poretz R.D. Antimutagenicity, cytotoxicity and composition of chlorophyllin copper complex. Cancer Letters 1997, 120:141-147.
15. Chimploy K., Díaz G.D., Li Q., Carter O., Dashwood W.-M., Mathews C.K., et al. E2F4 and ribonucleotide reductase mediate S-phase arrest in colon cancer cells treated with chlorophyllin. International Journal of Cancer 2009, 125:2086-2094.
16. Chung W.-Y., Lee J.-M., Lee W.-Y., Surh W.-J., Park K.-K. Protective effects of hemin and tetrakis(4-benzoic acid)porphyrin on bacterial mutagenesis and mouse skin carcinogenesis induced by 7,12-dimethylbenz[a]anthracene. Mutation Research, Genetic Toxicology and Environmental Mutagenesis 2000, 472:139-145.
17. 3) in somatic cells of Drosophila. Mutation Research 2003, 536:139-144.
18. Cruces M.P., Pimentel E., Zimmering S. Evidence that low concentrations of chlorophyllin (CHLN) increase the genetic damage induced by gamma rays in somatic cells of Drosophila. Mutation Research 2009, 679:84-86.
19. Dashwood R.H. The importance of using pure chemicals in (anti)mutagenicity studies: Chlorophyllin as a case in point. Mutation Research 1997, 381:283-286.
20. 1 and two heterocyclic amines in the Salmonella mutagenicity assay. Carcinogenesis 1991, 12:939-942.
21. Dashwood R., Liew C. Chlorophyllin-enhanced excretion of urinary and fecal mutagens in rats given 2-amino-3-methylimidazo[4, 5-f]quinoline. Environmental and Molecular Mutagenesis 1992, 20:199-205.
22. Dashwood R., Negishi T., Hayatsu H., Breinholt V., Hendricks J., Bailey G. Chemopreventive properties of chlorophylls towards aflatoxin B1: A review of the antimutagenicity and anticarcinogenicity data in rainbow trout. Carcinogenesis 1999, 20:1919-1926.
23. Dashwood R., Yamane S., Larsen R. Study of the forces stabilizing complexes between chlorophylls and heterocyclic amine mutagens. Environmental and Molecular Mutagenesis 1996, 27:211-218.
24. EC Commission Directive 94/36/EC. Official Journal of the European Communities 1994, L237:13-29.
25. Egner P.A., Muñoz A., Kensler T.W. Chemoprevention with chlorophyllin in individuals exposed to dietary aflatoxin. Mutation Research 2003, 523-524:209-216.
26. Egner P.A., Stansbury K.H., Snyder E.P., Rogers M.E., Hintz P.A., Kensler T.W. Identification and characterization of chlorin e4 ethyl ester in sera of individuals participating in the chlorophyllin chemoprevention trial. Chemical Research in Toxicology 2000, 13:900-906.
27. Egner P.A., Wang J.B., Zhu Y.R., Zhang B.C., Wu Y., Zhang Q.N., et al. Chlorophyllin intervention reduces aflatoxin-DNA adducts in individuals at high risk for liver cancer. Proceedings of the National Academy of Sciences 2001, 98:14601-14606.
28. Fahey J.D., Stephenson K.K., Dinkova-Kostova A.T., Egner P.A., Kensler T.W., Talalay P. Chlorophyll, chlorophyllin and related tetrapyrroles are significant inducers of mammalian phase 2 cytoprotective genes. Carcinogenesis 2005, 26:1247-1255.
29. FDA Listing of color additives exempt from certification: Sodium copper chlorophyllin 2002, US Food and Drug Administration, Department of Health and Human Services, Federal Register 67FR49567/67FR35429.
30. Fernandes T.M., Gomes B.B., Lanfer-Marquez U.M. Apparent absorption of chlorophyll from spinach in an assay with dogs. Innovative Food Science and Emerging Technologies 2007, 8:426-432.
31. Ferruzzi M.G., Blakeslee J. Digestion, absorption and cancer preventative activity of dietary chlorophyll derivatives. Nutrition Research 2007, 27:1-12.
32. Ferruzzi M.G., Failla M.L., Schwartz S.J. Assessment of degradation and intestinal cell uptake of carotenoids and chlorophyll derivatives from spinach puree using an in vitro digestion and Caco-2 human cell model. Journal of Agricultural and Food Chemistry 2001, 49:2082-2089.
33. Ferruzzi M.G., Failla M.L., Schwartz S.J. Sodium copper chlorophyllin: In vitro digestive stability and accumulation by Caco-2 human intestinal cells. Journal of Agricultural and Food Chemistry 2002, 50(7):2173-2179.
34. Gomes B.B., Barros S.B.M., Andrade-Wartha E.R.S., Silva A.M.O., Silva V.V., Lanfer-Marquez U.M. Bioavailability of dietary sodium copper chlorophyllin and its effect on antioxidant defence parameters of Wistar rats. Journal of the Science of Food and Agriculture 2009, 89(12):2003-2010.
35. Harrison J.W.E., Levin S.E., Trabin B. The safety and fate of potassium sodium copper chlorophyllin and other copper compounds. Journal of the American Pharmaceutical Association 1954, 43:722-737.
36. Hendry G.A.F. Chlorophylls. Natural food colorants - Science and technology 2000, 227-236. Marcel Dekker, Inc, New York. G.J. Lauro, F.J. Francis (Eds.).
37. Hernaez J., Xu M., Dashwood R. Effects of tea and chlorophyllin on the mutagenicity of N-hydroxy-IQ: Studies of enzyme inhibition, molecular complex formation, and degradation/scavenging of the active metabolites. Environmental and Molecular Mutagenesis 1997, 30:468-474.
38. Hughes J.H., Latner A.L. Chlorophyll and haemoglobin regeneration after haemorrhage. The Journal of Physiology 1936, 86:388-395.
39. Humphrey A.M. Chlorophyll. Food Chemistry 1980, 5:57-67.
40. Inoue H., Yamashita H., Furuya K., Nonomura Y., Yoshioka N., Li S. Determination of copper(II) chlorophyllin by reversed-phase high-performance liquid chromatography. Journal of Chromatography A 1994, 679:99-104.
41. John K., Keshava C., Richardson D.L., Weston A., Nath J. Transcriptional profiles of benzo(a)pyrene exposure in normal human mammary epithelial cells in the absence or presence of chlorophyllin. Mutation Research 2008, 640:145-152.
42. Jubert C., Mata J., Bench G., Dashwood R., Pereira C., Tracewell W., et al. Effects of chlorophyll and chlorophyllin on low-dose aflatoxin B(1) pharmacokinetics in human volunteers. Cancer Prevention Research (Philadelphia, Pa.) 2009, 2:1015-1022.
43. Kamat J.P., Boloor K.K., Devasagayam T.P.A. Chorophyllin as an effective antioxidant against membrane damage in vitro and ex vivo. Biochimica et Biophysica Acta 2000, 1487:113-127.
44. Kephart J.C. Chlorophyll derivatives: Their chemistry, commercial preparation and uses. Economic Botany 1955, 9:3-38.
45. Keshava C., Divi R.L., Einem T.L., Richardson D.L., Leonard S.L., Keshava N., et al. Chlorophyllin significantly reduces benzo[a]pyrene-DNA adduct formation and alters cytochrome P450 1A1 and 1B1expression and EROD activity in normal human mammary epithelial cells. Environmental and Molecular Mutagenesis 2009, 50:134-144.
46. Kumar S.S., Chaubey R.C., Devasagayam T.P.A., Priyadarsini K.I., Chauhan P.S. Inhibition of radiation-induced DNA damage in plasmid pBR322 by chlorophyllin and possible mechanism(s) of action. Mutation Research 1999, 425:71-79.
47. Kumar S.S., Devasagayam T.P.A., Bhushan B., Verma N.C. Scavenging of reactive oxygen species by chlorophyllin: An ESR study. Free Radical Research 2001, 35(5):563-574.
48. Kumar S.S., Shankar B., Sainis K.B. Effect of chlorophyllin against oxidative stress in splenic lymphocytes in vitro and in vivo. Biochimica et Biophysica Acta 2004, 1672:100-111.
49. Lai C.N., Butler M.A., Matney T.S. Antimutagenic activities of common vegetables and their chlorophyll content. Mutation Research 1980, 77:245-250.
50. Lanfer-Marquez U.M. The role of chlorophyll in human feeding: A review. Brazilian Journal of Pharmaceutical Science 2003, 39:227-242.
51. Lanfer-Marquez U.M., Barros R.M.C., Sinnecker P. Antioxidant activity of chlorophylls and their derivatives. Food Research International 2005, 38:885-891.
52. Maron D.M., Ames B.N. Revised methods for the Salmonella mutagenicity test. Mutation Research 1983, 113:173-215.
53. Marques A.C., Valente T.B., Rosa C.V. Toxin formation during food processing and possible consequences to the human body. Brazilian Journal of Nutrition 2009, 22(2):283-293.
54. Marty R., Ouameur A.A., Neault J.F., Tajmir-Riahi H.A. RNA adducts with chlorophyll and chlorophyllin: Stability and structural features. Journal of Biomolecular Structure and Dynamics 2004, 22(1):45-50.
55. 1 across Caco-2 cell monolayers. Toxicology 2004, 196:117-125.
56. Mortensen A., Geppel A. HPLC-MS analysis of the green food colorant sodium copper chlorophyllin. Innovative Food Science and Emerging Technologies 2007, 8:419-425.
57. Negraes P.D., Jordão B.Q., Vicentini V.E.P., Mantovani M.S. Anticlastogenicity of chlorophyllin in the different cell cycle phases in cultured mammalian cells. Mutation Research 2004, 557:177-182.
58. Negraes P.D., Jordão B.Q., Vicentini V.E.P., Mantovani M.S. The mutagenic potentiator effect of chlorophyllin by the HGPRT assay. Toxicology in Vitro 2004, 18:147-149.
59. Nelson R.L. Chlorophyllin, an antimutagen, acts as a tumor promoter in the rat-dimethylhydrazine colon carcinogenesis model. Anticancer Research 1992, 12(3):737-739.
60. Okai Y., Higashi-Okai K., Yano Y., Otani S. Suppressive effects of chlorophyllin on mutagen-induced umu C gene expression in Salmonella typhimurium (TA 1535/pSK 1002) and tumor promoter-dependent ornithine decarboxylase induction in BALB/c 3T3 fibroblast cells. Mutation Research 1996, 370:11-17.
61. Olvera O., Arceo C., Zimmering S. Chlorophyllin [CHLN] and the mutagenicity of monofunctional alkylating agents in Drosophila: The action of CHLN need not include an influence on metabolic activation. Mutation Research 2000, 467:113-117.
62. Ong T.-M., Whong W.-Z., Stewart J., Brockman H.E. Chlorophyllin: A potent antimutagen against environmental and dietary complex mixtures. Mutation Research 1986, 173:111-115.
63. Ong T.-M., Whong W.-Z., Stewart J.D., Brockman H.D. Comparative antimutagenicity of 5 compounds against 5 mutagenic complex mixtures in Salmonella typhimurium strain TA98. Mutation Research 1989, 222:19-25.
64. Park K.-K., Surh Y.-J., Miller J.A. Chemoprotective properties of chlorophyllin against vinyl carbamate, p-nitrophenyl vinyl ether and their electrophilic epoxides. Cancer Letters 1995, 94:33-40.
65. Patek A.J. Chlorophyll and regeneration of the blood: Effect of administration of chlorophyll derivatives to patients with chronic hypochromic anemia. Archives of Internal Medicine 1936, 57:73-84.
66. Pietrzak M., Halicka H.D., Wieczorek Z., Wieczorek J., Darzynkiewicz Z. Attenuation of acridine mutagen ICR-191 - DNA interactions and DNA damage by the mutagen interceptor chlorophyllin. Biophysical Chemistry 2008, 135:69-75.
67. Pietrzak M., Wieczorek Z., Stachelska A., Darzynkiewicz Z. Interactions of chlorophyllin with acridine orange, quinacrine mustard and doxorubicin analyzed by light absorption and fluorescence spectroscopy. Biophysical Chemistry 2003, 104:305-313.
68. Pietrzak M., Wieczorek Z., Wieczorek J., Darzynkiewicz J. The "interceptor" properties of chlorophyllin measured within the three-component system: Intercalator-DNA-chlorophyllin. Biophysical Chemistry 2006, 123:11-19.
69. Pimentel E., Cruces M.P., Zimmering S. On the persistence of the radioprotective effect of chlorophyllin (CHLN) in somatic cells of Drosophila. Mutation Research 1999, 446:189-192.
70. Pimentel E., Cruces M.P., Zimmering S. Evidence that chlorophyllin (CHLN) may behave as an inhibitor or a promoter of radiation-induced genetic damage in somatic cells of Drosophila. Mutation Research 2000, 472:71-74.
71. Pratt M.M., Reddy A.P., Hendricks J.D., Pereira C., Kensler T.W., Bailey G.S. The importance of carcinogen dose in chemoprevention studies: Quantitative interrelationships between, dibenzo[a, l]pyrene dose, chlorophyllin dose, target organ DNA adduct biomarkers and final tumor outcome. Carcinogenesis 2007, 28:611-624.
72. Reddy A.P., Harttig U., Barth M.C., Baird W.M., Schimerlik M., Hendricks J.D., et al. Inhibition of dibenzo[a, l]pyrene-induced multi-organ carcinogenesis by dietary chlorophyllin in rainbow trout. Carcinogenesis 1999, 20:1919-1926.
73. Redmond R.W., Gamlin J.N. A compilation of singlet oxygen yields from biologically relevant molecules. Photochemistry and Photobiology 1999, 70(4):391-475.
74. Robey R.W., Steadman K., Polgar O., Bates S.E. ABCG2-mediated transport of photosensitizers: Potential impact on photodynamic therapy. Cancer Biology & Therapy 2005, 4:187-194.
75. Romert L., Curvall M., Jenssen D. Chlorophyllin is both a positive and negative modifier of mutagenicity. Mutagenesis 1992, 7:349-355.
76. Sarkar D., Sharma A., Talukder G. Chlorophyll and chlorophyllin as modifiers of genotoxic effects. Mutation Research 1994, 318:239-247.
77. Sato M., Fujimoto I., Sakai T., Aimoto T., Kimura R., Murata T. Effect of sodium copper chlorophyllin on lipid peroxidation. IX. On the antioxidative components in commercial preparations of sodium copper chlorophyllin. Chemical & Pharmaceutical Bulletin 1986, 34:2428-2434.
78. Sato M., Fujimoto I., Sakai T., Kimura R., Murata T. An antioxidative component in the commercial preparations of sodium copper chlorophyllin. Yakugaku Zasshi 1979, 99:1055-1057.
79. Sato M., Imai K., Kimura R., Murata T. Effect of sodium copper chlorophyllin on lipid peroxidation. VI. Effect of its administration on mitochondrial and microsomal lipid peroxidation in rat liver. Chemical & Pharmaceutical Bulletin 1984, 32:716-722.
80. Sharma D., Kumar S.S., Sainis K.B. Antiapoptotic and immunomodulatory effects of chlorophyllin. Molecular Immunology 2007, 44:347-359.
81. Simonich M.T., McQuistan T., Jubert C., Pereira C., Hendricks J.D., Schimerlik M., et al. Low-dose dietary chlorophyll inhibits multi-organ carcinogenesis in the rainbow trout. Food and Chemical Toxicology 2008, 46:1014-1024.
82. Tachino N., Guo D., Dashwood W.M., Yamane S., Larsen R., Dashwood R. Mechanisms of the in vitro antimutagenic action of chlorophyllin against benzo[a]pyrene: Studies of enzyme inhibition, molecular complex formation and degradation of the ultimate carcinogen. Mutation Research 1994, 308:191-203.
83. Tajmir-Riahi H.A., Neault J.F., Diamantoglou S. DNA adducts with chlorophyll and chlorophyllin as antimutagenic agents: Synthesis, stability, and structural features. Methods in Molecular Biology 2004, 274:159-171.
84. Tanaka R., Tanaka A. Tetrapyrrole biosynthesis in higher plants. Annual Review of Plant Biology 2007, 58:321-346.
85. Woo G.-H., Shibutani M., Kuroiwa K., Lee K.-Y., Takahashi M., Inoue K., et al. Lack of preventive effects of dietary fibers or chlorophyllin against acrylamide toxicity in rats. Food and Chemical Toxicology 2007, 45:1507-1515.
86. Xu M., Orner G.A., Bailey G.S., Stoner G.D., Horio D.T., Dashwood R.H. Post-initiation effects of chlorophyllin and indole-3-carbinol in rats given 1,2-dimethylhydrazine or 2-amino-3-methyl-imidazo[4,5, f]quinoline. Carcinogenesis 2001, 22:309-314.
87. Yamazaki H., Fujieda M., Togashi M., Saito T., Preti G., Cashman J.R., et al. Effects of the dietary supplements, activated charcoal and copper chlorophyllin, on urinary excretion of trimethylamine in Japanese trimethylaminuria patients. Life Sciences 2004, 74:2739-2747.
88. Yun C.-H., Jeon Y.J., Yang Y., Ju H.R., Han S.H. Chlorophyllin suppresses interleukin-1 beta expression in lipopolysaccharide-activated RAW 264.7 cells. International Immunopharmacology 2006, 6:252-259.
89. Yun C.-H., Jeong H.G., Jhoun J.W., Guengerich F.P. Non-specific inhibition of cytochrome P450 activities by chlorophyllin in human and rat liver microsomes. Carcinogenesis 1995, 16:1437-1440.