Lycopene-derived bioactive retinoic acid receptors/retinoid-X receptors-activating metabolites may be relevant for lycopene's anti-cancer potential

Molecular Nutrition and Food Research

Volumn 57, Issue 5, 2013, Pages 739-747

  Aydemir, Gamze ^a   Kasiri, Yasamin ^a   Birta, Eszter ^a   Béke, Gabriella ^a   Garcia, Ada L ^c   Bartók, Emoke Márta ^a   Rühl, Ralph ^a,b,d  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b Apoptosis and Genomics Research Group of the Hungarian Academy of Science   (Hungary)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d Paprika Bioanalytics Bt   (Hungary)

Author keywords

Carotenoid; Lycopene; Nuclear hormone receptor; Retinoic acid; Tomato

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIOXIDANT; BETA CAROTENE 15,15' MONOOXYGENASE; CAROTENOID; LYCOPENE; RETINOID; RETINOID X RECEPTOR;

ANIMAL; ANIMAL MODEL; CHEMISTRY; DIET; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY; REVIEW; SIGNAL TRANSDUCTION; TOMATO;

ANIMALS; ANTICARCINOGENIC AGENTS; ANTIOXIDANTS; BETA-CAROTENE 15,15'-MONOOXYGENASE; CAROTENOIDS; DIET; HUMANS; LYCOPERSICON ESCULENTUM; MODELS, ANIMAL; NEOPLASMS; RETINOID X RECEPTORS; RETINOIDS; SIGNAL TRANSDUCTION;

LYCOPERSICON ESCULENTUM;

EID: 84876435852     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200548     Document Type: Review

References (68)

1. Wiseman, M., The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc. Nutr. Soc. 2008, 67, 253-256.
2. Davison, A., Rousseau, E., Dunn, B., Putative anticarcinogenic actions of carotenoids: nutritional implications. Can. J. Physiol. Pharmacol. 1993, 71, 732-745.
3. Cohen, L. A., A review of animal model studies of tomato carotenoids, lycopene, and cancer chemoprevention. Exp. Biol. Med. 2002, 227, 864-868.
4. Gullett, N. P., Ruhul Amin, A. R., Bayraktar, S., Pezzuto, J. M. et al., Cancer prevention with natural compounds. Semin. Oncol. 2010, 37, 258-281.
5. Khachik, F., Carvalho, L., Bernstein, P. S., Muir, G. J. et al., Chemistry, distribution, and metabolism of tomato carotenoids and their impact on human health. Exp. Biol. Med. 2002, 227, 845-851.
6. Mangels, A. R., Holden, J. M., Beecher, G. R., Forman, M. R. et al., Carotenoid content of fruits and vegetables: an evaluation of analytic data. J. Am. Diet. Assoc. 1993, 93, 284-296.
7. Rao, A. V., Processed tomato products as a source of dietary lycopene: bioavailability and antioxidant properties. Can. J. Diet. Pract. Res. 2004, 65, 161-165.
8. Stahl, W., Sies, H., Lycopene: a biologically important carotenoid for humans? Arch. Biochem. Biophys. 1996, 336, 1-9.
9. Aune, D., Chan, D. S., Vieira, A. R., Rosenblatt, D. A. et al., Fruits, vegetables and breast cancer risk: a systematic review and meta-analysis of prospective studies. Breast Cancer. Res. Treat. 134, 479-493.
10. Edefonti, V., Hashibe, M., Ambrogi, F., Parpinel, M. et al., Nutrient-based dietary patterns and the risk of head and neck cancer: a pooled analysis in the International Head and Neck Cancer Epidemiology consortium. Ann. Oncol. 2012, 23, 1869-1880.
11. Campbell, J. K., Canene-Adams, K., Lindshield, B. L., Boileau, T. W. et al., Tomato phytochemicals and prostate cancer risk. J. Nutr. 2004, 134, 3486S-3492S.
12. Haseen, F., Cantwell, M. M., O'Sullivan, J. M., Murray, L. J., Is there a benefit from lycopene supplementation in men with prostate cancer? A systematic review. Prostate Cancer Prostatic Dis. 2009, 12, 325-332.
13. Basu, A., Imrhan, V., Tomatoes versus lycopene in oxidative stress and carcinogenesis: conclusions from clinical trials. Eur. J. Clin. Nutr. 2007, 61, 295-303.
14. Etminan, M., Takkouche, B., Caamano-Isorna, F., The role of tomato products and lycopene in the prevention of prostate cancer: a meta-analysis of observational studies. Cancer Epidemiol. Biomarkers Prev. 2004, 13, 340-345.
15. Ilic, D., Forbes, K. M., Hassed, C., Lycopene for the prevention of prostate cancer. Cochrane Database Syst. Rev. 2011, CD008007.
16. Ilic, D., Misso, M., Lycopene for the prevention and treatment of benign prostatic hyperplasia and prostate cancer: a systematic review. Maturitas 2012, 72, 269-276.
17. Wei, M. Y., Giovannucci, E. L., Lycopene, tomato products, and prostate cancer incidence: a review and reassessment in the PSA screening era. J. Oncol. 2012, 2012, 271063.
18. Giovannucci, E., A review of epidemiologic studies of tomatoes, lycopene, and prostate cancer. Exp. Biol. Med. (Maywood) 2002, 227, 852-859.
19. Giovannucci, E., Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. J. Natl. Cancer Inst. 1999, 91, 317-331.
20. Kucuk, O., Sarkar, F. H., Djuric, Z., Sakr, W. et al., Effects of lycopene supplementation in patients with localized prostate cancer. Exp. Biol. Med. 2002, 227, 881-885.
21. Erdman, J. W., Jr., Ford, N. A., Lindshield, B. L., Are the health attributes of lycopene related to its antioxidant function? Arch. Biochem. Biophys. 2009, 483, 229-235.
22. Agarwal, S., Rao, A. V., Tomato lycopene and its role in human health and chronic diseases. Cmaj. 2000, 163, 739-744.
23. Stahl, W., von Laar, J., Martin, H. D., Emmerich, T. et al., Stimulation of gap junctional communication: comparison of acyclo-retinoic acid and lycopene. Arch. Biochem. Biophys. 2000, 373, 271-274.
24. Zhang, L. X., Cooney, R. V., Bertram, J. S., Carotenoids up-regulate connexin43 gene expression independent of their provitamin A or antioxidant properties. Cancer Res. 1992, 52, 5707-5712.
25. Nahum, A., Zeller, L., Danilenko, M., Prall, O. W. et al., Lycopene inhibition of IGF-induced cancer cell growth depends on the level of cyclin D1. Eur. J. Nutr. 2006, 45, 275-282.
26. Riso, P., Brusamolino, A., Martinetti, A., Porrini, M., Effect of a tomato drink intervention on insulin-like growth factor (IGF)-1 serum levels in healthy subjects. Nutr. Cancer. 2006, 55, 157-162.
27. Wang, S., DeGroff, V. L., Clinton, S. K., Tomato and soy polyphenols reduce insulin-like growth factor-I-stimulated rat prostate cancer cell proliferation and apoptotic resistance in vitro via inhibition of intracellular signaling pathways involving tyrosine kinase. J. Nutr. 2003, 133, 2367-2376.
28. Khandwala, H. M., McCutcheon, I. E., Flyvbjerg, A., Friend, K. E., The effects of insulin-like growth factors on tumorigenesis and neoplastic growth. Endocr. Rev. 2000, 21, 215-244.
29. Levy, J., Bosin, E., Feldman, B., Giat, Y. et al., Lycopene is a more potent inhibitor of human cancer cell proliferation than either alpha-carotene or beta-carotene. Nutr. Cancer. 1995, 24, 257-266.
30. Renehan, A. G., Zwahlen, M., Minder, C., O'Dwyer, S. T. et al., Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet 2004, 363, 1346-1353.
31. Mantzoros, C. S., Tzonou, A., Signorello, L. B., Stampfer, M. et al., Insulin-like growth factor 1 in relation to prostate cancer and benign prostatic hyperplasia. Br. J. Cancer 1997, 76, 1115-1118.
32. Hankinson, S. E., Willett, W. C., Colditz, G. A., Hunter, D. J. et al., Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 1998, 351, 1393-1396.
33. Lukanova, A., Lundin, E., Toniolo, P., Micheli, A. et al., Circulating levels of insulin-like growth factor-I and risk of ovarian cancer. Int. J. Cancer 2002, 101, 549-554.
34. Kanagaraj, P., Vijayababu, M. R., Ravisankar, B., Anbalagan, J. et al., Effect of lycopene on insulin-like growth factor-I, IGF binding protein-3 and IGF type-I receptor in prostate cancer cells. J. Cancer Res. Clin. Oncol. 2007, 133, 351-359.
35. Karas, M., Amir, H., Fishman, D., Danilenko, M. et al., Lycopene interferes with cell cycle progression and insulin-like growth factor I signaling in mammary cancer cells. Nutr. Cancer 2000, 36, 101-111.
36. Drop, S. L., Schuller, A. G., Lindenbergh-Kortleve, D. J., Groffen, C. et al., Structural aspects of the IGFBP family. Growth Reg. 1992, 2, 69-79.
37. Ben-Dor, A., Nahum, A., Danilenko, M., Giat, Y. et al., Effects of acyclo-retinoic acid and lycopene on activation of the retinoic acid receptor and proliferation of mammary cancer cells. Arch. Biochem. Biophys. 2001, 391, 295-302.
38. Lindshield, B. L., Canene-Adams, K., Erdman, J. W., Jr., Lycopenoids: are lycopene metabolites bioactive? Arch. Biochem. Biophys. 2007, 458, 136-140.
39. Aydemir, G., Carlsen, H., Blomhoff, R., Rühl, R., Lycopene induces retinoic acid receptor transcriptional activation in mice. Mol. Nutr. Food Res. 2012, 56, 702-712.
40. Darwiche, N., Celli, G., De Luca, L. M., Specificity of retinoid receptor gene expression in mouse cervical epithelia. Endocrinology 1994, 134, 2018-2025.
41. Dogra, S. C., Khanduja, K. L., Gupta, M. P., The effect of vitamin A deficiency on the initiation and postinitiation phases of benzo(a)pyrene-induced lung tumourigenesis in rats. Br. J. Cancer 1985, 52, 931-935.
42. Altucci, L., Leibowitz, M. D., Ogilvie, K. M., de Lera, A. R. et al., RAR and RXR modulation in cancer and metabolic disease. Nat. Rev. Drug. Discov. 2007, 6, 793-810.
43. Seren, S., Lieberman, R., Bayraktar, U. D., Heath, E. et al., Lycopene in cancer prevention and treatment. Am. J. Ther. 2008, 15, 66-81.
44. Balmer, J. E., Blomhoff, R., Gene expression regulation by retinoic acid. J. Lipid. Res. 2002, 43, 1773-1808.
45. Bogan, A. A., Cohen, F. E., Scanlan, T. S., Natural ligands of nuclear receptors have conserved volumes. Nat. Struct. Biol. 1998, 5, 679-681.
46. Khachik, F., Spangler, C. J., Smith, J. C., Jr., Canfield, L. M. et al., Identification, quantification, and relative concentrations of carotenoids and their metabolites in human milk and serum. Anal. Chem. 1997, 69, 1873-1881.
47. Khachik, F., Pfander, H., Traber, B., Proposed mechanism for teh formation of synthetic and naturally occurring metabolites of lycopene in tomato products, and human serum. J. Agric. Food Chem. 1998, 46, 4885-4890.
48. Khachik, F., Steck, A., Niggli, U. A., Pfander, H., Partial synthesis and structural elucidation of the oxidative metabolites of lycopene identified in tomato paste, tomato juice and human serum. J. Agric. Food Chem. 1998, 46, 4874-4884.
49. Boileau, T. W., Boileau, A. C., Erdman, J. W., Jr., Bioavailability of all-trans and cis-isomers of lycopene. Exp. Biol. Med. (Maywood) 2002, 227, 914-919.
50. Boileau, T. W., Clinton, S. K., Erdman, J. W., Jr., Tissue lycopene concentrations and isomer patterns are affected by androgen status and dietary lycopene concentration in male F344 rats. J. Nutr. 2000, 130, 1613-1618.
51. Nguyen, M. L., Schwartz, S. J., Lycopene stability during food processing. Proc. Soc. Exp. Biol. Med. 1998, 218, 101-105.
52. Erdman, J. W., Jr., How do nutritional and hormonal status modify the bioavailability, uptake, and distribution of different isomers of lycopene? J. Nutr. 2005, 135, 2046S-2047S.
53. Lindshield, B. L., King, J. L., Wyss, A., Goralczyk, R. et al., Lycopene biodistribution is altered in 15, 15'-carotenoid monooxygenase knockout mice. J. Nutr. 2008, 138, 2367-2371.
54. Clinton, S. K., Emenhiser, C., Schwartz, S. J., Bostwick, D. G. et al., cis-trans lycopene isomers, carotenoids, and retinol in the human prostate. Cancer Epidemiol. Biomarkers Prev. 1996, 5, 823-833.
55. Sicilia, T., Bub, A., Rechkemmer, G., Kraemer, K. et al., Novel lycopene metabolites are detectable in plasma of preruminant calves after lycopene supplementation. J. Nutr. 2005, 135, 2616-2621.
56. Caris-Veyrat, C., Schmid, A., Carail, M., Bohm, V., Cleavage products of lycopene produced by in vitro oxidations: characterization and mechanisms of formation. J. Agric. Food Chem. 2003, 51, 7318-7325.
57. Gajic, M., Zaripheh, S., Sun, F., Erdman, J. W., Jr., Apo-8'-lycopenal and apo-12'-lycopenal are metabolic products of lycopene in rat liver. J. Nutr. 2006, 136, 1552-1557.
58. Ferreira, A. L., Yeum, K. J., Russell, R. M., Krinsky, N. I. et al., Enzymatic and oxidative metabolites of lycopene. J. Nutr. Biochem. 2003, 14, 531-540.
59. Hu, K. Q., Liu, C., Ernst, H., Krinsky, N. I. et al., The biochemical characterization of ferret carotene-9', 10'-monooxygenase catalyzing cleavage of carotenoids in vitro and in vivo. J. Biol. Chem. 2006, 281, 19327-19338.
60. Kopec, R. E., Riedl, K. M., Harrison, E. H., Curley, R. W., Jr. et al., Identification and quantification of apo-lycopenals in fruits, vegetables, and human plasma. J. Agric. Food Chem. 2010, 58, 3290-3296.
61. Kiefer, C., Hessel, S., Lampert, J. M., Vogt, K. et al., Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J. Biol. Chem. 2001, 276, 14110-14116.
62. Gouranton, E., Aydemir, G., Reynaud, E., Marcotorchino, J. et al., Apo-10'-lycopenoic acid impacts adipose tissue biology via the retinoic acid receptors. Biochim. Biophys. Acta. 2011, 1811, 1105-1114.
63. Araki, H., Shidoji, Y., Yamada, Y., Moriwaki, H. et al., Retinoid agonist activities of synthetic geranyl geranoic acid derivatives. Biochem. Biophys. Res. Commun. 1995, 209, 66-72.
64. Nakamura, N., Shidoji, Y., Moriwaki, H., Muto, Y., Apoptosis in human hepatoma cell line induced by 4, 5-didehydro geranylgeranoic acid (acyclic retinoid) via down-regulation of transforming growth factor-alpha. Biochem. Biophys. Res. Commun. 1996, 219, 100-104.
65. Okusaka, T., Ueno, H., Ikeda, M., Morizane, C., Phase I and pharmacokinetic clinical trial of oral administration of the acyclic retinoid NIK-333. Hepatol. Res. 2011, 41, 542-552.
66. von Lintig, J., Vogt, K., Filling the gap in vitamin A research. Molecular identification of an enzyme cleaving beta-carotene to retinal. J. Biol. Chem. 2000, 275, 11915-11920.
67. Redmond, T. M., Gentleman, S., Duncan, T., Yu, S. et al., Identification, expression, and substrate specificity of a mammalian beta-carotene 15, 15'-dioxygenase. J. Biol. Chem. 2001, 276, 6560-6565.
68. von Lintig, J., Wyss, A., Molecular analysis of vitamin A formation: cloning and characterization of beta-carotene 15, 15'-dioxygenases. Arch. Biochem. Biophys. 2001, 385, 47-452.