Synthetic retinoid fenretinide in breast cancer chemoprevention

Expert Review of Anticancer Therapy

Volumn 7, Issue 4, 2007, Pages 423-432

  Bonanni, Bernardo ^a   Lazzeroni, Matteo ^a   Veronesi, Umberto ^a  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

Breast neoplasm; Chemoprevention; Clinical trial; Fenretinide; Retinoid

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; FENRETINIDE; HYDROGEN PEROXIDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PLACEBO; RETINOID DERIVATIVE; RETINOL; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; SUPEROXIDE; TAMOXIFEN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

APOPTOSIS; BLADDER CANCER; BREAST CANCER; BREAST CARCINOGENESIS; CHEMOPROPHYLAXIS; CLINICAL TRIAL; DARK ADAPTATION; DRUG ACCUMULATION; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG STRUCTURE; DRUG WITHDRAWAL; DRY SKIN; EYE DISEASE; FOLLOW UP; GASTROINTESTINAL SYMPTOM; GENOTOXICITY; HIGH RISK PATIENT; HUMAN; HYPERTRIGLYCERIDEMIA; INCIDENCE; LIPID BLOOD LEVEL; LIVER FUNCTION TEST; LIVER TOXICITY; LOW DRUG DOSE; META ANALYSIS; MUCOSAL DRYNESS; NIGHT BLINDNESS; NONHUMAN; OVARY CANCER; PREMENOPAUSE; PRIMARY PREVENTION; PROTEIN BLOOD LEVEL; PRURITUS; REVIEW; SIDE EFFECT; SKIN DISEASE; SYSTEMATIC REVIEW; TERATOGENICITY; URTICARIA; VISUAL DISORDER; VISUAL IMPAIRMENT;

APOPTOSIS; BREAST NEOPLASMS; FEMALE; FENRETINIDE; HUMANS; RETINOIDS;

EID: 34247559202     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/14737140.7.4.423     Document Type: Review

References (96)

1. American Cancer Society. Cancer Facts & Figures 2007. American Cancer Society, USA (2007).
2. Broet P, de la Rochefordiere A. Scholl SM et al. Contralateral breast cancer annual incidence and risk parameters. J. Clin. Oncol. 13(7), 1578-1583 (1995).
3. Cuzick J, Powles T, Veronesi U et al. Overview of the main outcomes in breast-cancer prevention trials. Lancet 361 (9354), 296-300 (2003).
4. Vogel VG, Costantino JP, Wickerham DL et al. Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: the NSABP Study of Tamoxifen And Raloxifene (STAR) P-2 trial. JAMA 295(23), 2727-2741 (2006).
5. Lippman SM, Lee JJ, Sabichi AL. Cancer chemoprevention: progress and promise. J Natl Cancer Inst. 90(20), 1514-1528 (1998).
6. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J. 10(9), 940-954 (1996).
7. Rehman F, Shan mugasundaram P, Schrey MP. Fenretinide stimulates redox-sensitive ceramide production in breast cancer cells: potential role in drug-induced cytotoxicity. Br. J Cancer 91(10), 1821-1828 (2004).
8. Dawson MI, Chao WR, Pine P et al. Correlation of retinoid binding affinity to retinoic acid receptor α with retinoid inhibition of growth of estrogen receptor-positive MCF-7 mammary carcinoma cells. Cancer Res. 55(19), 4446-4451 (1995).
9. Simeone AM, Tari AM. How retinoids regulate breast cancer cell proliferation and apoptosis. Cell Mol. Life Sci. 61(12), 1475-1484 (2004).
10. Chen TK, Smith LM, Gebhardt DK, Birrer MJ, Brown PH. Activation and inhibition of the AP-1 complex in human breast cancer cells. Mol. Carcinog. 15(3), 215-226 (1996).
11. Fanjul A, Dawson MI, Hobbs PD et al. A new class of retinoids with selective inhibition of AP-1 inhibits proliferation. Nature 372(6501), 107-111 (1994).
12. Li JJ, Dong Z, Dawson MI, Colburn NH. Inhibition of tumor promoter-induced transformation by retinoids that transrepress AP-1 without transactivating retinoic acid response element. Cancer Res. 56(3), 483-489 (1996).
13. Shah S, Pishvaian MJ, Easwaran V, Brown PH, Byers SW. The role of cadherin, β-catenin, and AP-1 in retinoid-regulated carcinoma cell differentiation and proliferation. J. Biol. Chem. 277(28), 25313-25322 (2002).
14. Zhang XK, Liu Y, Lee MO. Retinoid receptors in human lung cancer and breast cancer. Mutat. Res. 350(1), 267-277 (1996).
15. Oridate N, Lotan D, Xu XC, Hong WK, Lotan R. Differential induction of apoptosis by all-trans-retinoic acid and N-(4-hydroxyphenyl)retinamide in human head and neck squamous cell carcinoma cell lines. Clin. Cancer Res. 2(5), 855-863 (1996).
16. Zou CP, Kurie JM, Lotan D, Zou CC, Hong WK, Lotan R. Higher potency of N-(4-hydroxyphenyl)retinamide than all-trans-retinoic acid in induction of apoptosis in non-small cell lung cancer cell lines. Clin. Cancer Res. 4(5), 1345-1355 (1998).
17. Sporn MB, Dunlop NM, Newton DL, Smith JM. Prevention of chemical carcinogenesis by vitamin A and its synthetic analogs (retinoids). Fed. Proc. 35(6), 1332-1338 (1976).
18. Moon RC, Thompson HJ, Becci PJ et al. N-(4-Hydroxyphenyl)retinamide, a new retinoid for prevention of breast cancer in the rat. Cancer Res. 39(4), 1339-1346 (1979).
19. Sun SY, Li W, Yue P, Lippman SM, Hong WK, Lotan R. Mediation of N-(4-hydoxyphenyl)retinamide-induced apoptosis in human cancer cells by different mechanisms. Cancer Res. 59(10), 2493-2498 (1999).
20. Sheikh MS, Shao ZM, Li XS et al. N-(4-hydroxyphenyl)retinamide (4-HPR)-mediated biological actions involve retinoid receptor-independent pathways in human breast carcinoma. Carcinogenesis 16(10), 2477-2486 (1995).
21. Sabichi AL, Hendricks DT, Bober MA, Birrer MJ. Retinoic acid receptor β expression and growth inhibition of gynecologic cancer cells by the synthetic retinoid N-(4-hydroxyphenyl) retinamide. J. Natl Cancer Inst. 90(8), 597-605 (1998).
22. Oridate N, Suzuki S, Higuchi M, Mitchell MF, Hong WK, Lotan R. Involvement of reactive oxygen species in N-(4-hydroxyphenyl)retinamide-induced apoptosis in cervical carcinoma cells. J. Natl Cancer Inst. 89(16), 1191-1198 (1997).
23. Kelloff GJ, Crowell JA, Boone CW et al. Clinical development plan: N-(4-hydroxyphenyl)retinamide. J. Cell Biochem. Suppl. 20, 176-196 (1994).
24. Mehta RG, Moon RC, Hawthorne M, Formelli F, Costa A. Distribution of fenretinide in the mammary gland of breast cancer patients. Eur. J. Cancer 27(2), 138-141 (1991).
25. Reynolds CP, Matthay KK, Villablanca JG, Maurer BJ. Retinoid therapy of high-risk neuroblastoma. Cancer Lett. 197(1-2), 185-192 (2003).
26. Maurer BJ, Metelitsa LS, Seeger RC, Cabot MC, Reynolds CP, Increase of ceramide and induction of mixed apoptosis/necrosis by N-(4-hydroxyphenyl)-retinamide in neuroblastoma cell lines. J. Natl Cancer Inst. 91(13), 1138-1146 (1999).
27. Maurer BJ, Melton L, Billups C, Cabot MC, Reynolds CP. Synergistic cytotoxicity in solid tumor cell lines between N-(4-hydroxyphenyl)retinamide and modulators of ceramide metabolism. J. Natl Cancer Inst. 92(23), 1897-1909 (2000).
28. O'Donnell PH, Guo WX, Reynolds CP, Maurer BJ. N-(4-hydroxyphenyl)retinamide increases ceramide and is cytotoxic to acute lymphoblastic leukemia cell lines, but not to non-malignant lymphocytes. Leukemia 16(5), 902-910 (2002).
29. Batra S, Reynolds CP Maurer BJ. Fenretinide cytotoxicity for Ewine's sarcoma and primitive neuroectodermal tumor cell lines is decreased by hypoxia and synergistically enhanced by ceramide modulators. Cancer Res. 64(15), 5415-5424 (2004).
30. Reynolds CP, Maurer BJ, Kolesnick RN. Ceramide synthesis and metabolism as a target for cancer therapy. Cancer Lett. 206(2), 169-180 (2004).
31. Fanjul AN, Delia D, Pierotti MA et al. 4-Hydroxyphenyl retinamide is a highly selective activator of retinoid receptors. J. Biol. Chem. 271(37), 22441-22446 (1996).
32. Liu G, Wu M, Levi G, Ferrari N. Inhibition of cancer cell growth by all-trans retinoic acid and its analog N-(4-hydroxyphenyl) retinamide: a possible mechanism of action via regulation of retinoid receptors expression. Int. J. Cancer 78(2), 248-254 (1998).
33. Panigone S, Debernardi S, Taya Y, Fontanella E, Airoldi R, Delia D. pRb and Cdk regulation by N-(4-hydroxyphenyl)retinamide. Oncogene 19(35), 4035-4041 (2000).
34. Lotan R. Retinoids and apoptosis: implications for cancer chemoprevention and therapy. J. Natl Cancer Inst. 87(22), 1655-1657 (1995).
35. Wu JM, DiPietrantonio AM, Hsieh TC. Mechanism of fenretinide (4-HPR)-induced cell death. Apoptosis 6(5), 377-388 (2001).
36. Delia D, Aiello A, Meroni L, Nicolini M, Reed JC, Pierotti MA. Role of antioxidants and intracellular free radicals in retinamide-induced cell death. Carcinogenesis 18(5), 943-948 (1997).
37. Tosetti F, Vene R, Arena G et al. N-(4-hydroxyphenyl)retinamide inhibits retinoblastoma growth through reactive oxygen species-mediated cell death. Mol. Pharmacol. 63(3), 565-573 (2003).
38. Simeone AM, Ekmekcioglu S, Broemeling LD, Grimm EA, Tari AM. A novel mechanism by which N-(4-hydroxyphenyl)retinamide inhibits breast cancer cell growth: the production of nitric oxide. Mol. Cancer Ther. 1(12), 1009-1017 (2002).
39. Simeone AM, Broemeling LD, Rosenblum J, Tari AM. HER2/neu reduces the apoptotic effects of N-(4-hydroxyphenyl)retinamide (4-HPR) in breast cancer cells by decreasing nitric oxide production. Oncogene 22(43), 6739-6747 (2003).
40. Umansky V, Ushmorov A, Ratter F et al. Nitric oxide-mediated apoptosis in human breast cancer cells requires changes in mitochondrial functions and is independent of CD95 (APO-1/Fas). Int. J. Oncol. 16(1), 109-117 (2000).
41. Favoni RE, de Cupis A, Bruno S et al. Modulation of the insulin-like growth factor-I system by N-(4-hydroxyphenyl)-retinamide in human breast cancer cell lines. Br. J. Cancer 77(12), 2138-2147 (1998).
42. Fontana JA, Burrows-Mezu A, Clemmons DR. LeRoith D. Retinoid modulation of insulin-like growth factor-binding proteins and inhibition of breast carcinoma proliferation. Endocrinology 128(2), 1115-1122 (1991).
43. Herbert BS, Sanders BG, Kline K. N-(4-hydroxyphenyl)retinamide activation of transforming growth factor-β and induction of apoptosis in human breast cancer cells. Nutr Cancer 34(2), 121-132 (1999).
44. Bednarek A. Shilkaitis A, Green A et al. Suppression of cell proliferation and telomerase activity in 4-(hydroxyphenyl)retinamide-treated mammary tumors. Carcinogenesis 20(5), 879-883 (1999).
45. Bowman R. Clarke B, Duhig E, Larsen J, Fong K. Re: effects of N-(4-hydroxy-phenyl)retinamide on hTERT expression in the bronchial epithelium of cigarette smokers. J. Natl. Cancer Inst. 94(12), 949-950 (2002).
46. Simeone AM, Li YJ, Broemeling LD. Johnson MM, Tuna M, Tari AM. Cyclooxygenase-2 is essential for HER2/neu to suppress N-(4-hydroxyphenyl)retinamide apoptotic effects in breast cancer cells. Cancer Res. 64(4), 1224-1228 (2004).
47. Jinno H, Steiner MG, Mehta RG, Osborne MP, Telang NT. Inhibition of aberrant proliferation and induction of apoptosis in HER-2/neu oncogene transformed human mammary epithelial cells by N-(4-hydroxyphenyl)retinamide. Carrinogenesis 20(2), 229-236 (1999).
48. Rao GN, Ney E, Herbert RA. Effect of retinoid analogues on mammary cancer in transgenic mice with c-neu breast cancer oncogene. Breast Cancer Res. Treat. 48(3), 265-271 (1998).
49. Simeone AM, Deng CX, Kelloff GJ, Steele VE, Johnson MM, Tari AM. N-(4-Hydroxyphenyl)retinamide is more potent than other phenylretinamides in inhibiting the growth of BRCA1-mutated breast cancer cells. Carrinogenesis 26(5), 1000-1007 (2005).
50. Doose DR, Minn FL, Stellar S, Nayak RK. Effects of meals and meal composition on the bioavailability of fenretinide. J. Clin. Pharmacol. 32(12), 1089-1095 (1992).
51. Formelli F, Clerici M, Campa T et al. Five-year administration of fenretinide: pharmacokinetics and effects on plasma retinol concentrations. J Clin. Oncol. 11(10), 2036-2042 (1993).
52. Formelli F, Carsana R, Costa A et al. Plasma retinol level reduction by the synthetic retinoid fenretinide: a one year follow-up study of breast cancer patients. Cancer Res. 49(21), 6149-6152 (1989).
53. Peng YM, Dalton WS, Alberts DS, Xu MJ, Lim H, Meyskens FL Jr. Pharmacokinetics of N-4-hydroxyphenyl-retinamide and the effect of its oral administration on plasma retinol concentrations in cancer patients. Int. J. Cancer 43(1), 22-26 (1989).
54. Berni R, Formelli F. In vitro interaction of fenretinide with plasma retinol-binding protein and its functional consequences. FEBS Lett. 308(1), 43-45 (1992).
55. Lewis KC, Zech LA, Phang JM. Effects of chronic administration of N-(4-hydroxyphenyl)retinamide (4-HPR) in rats on vitamin A metabolism in the eye. Eur. J. Cancer 32A(10), 1803-1808 (1996).
56. Torrisi R, Parodi S, Fontana V et al. Factors affecting plasma retinol decline during long-term administration of the synthetic retinoid fenretinide in breast cancer patients. Cancer Epidemiol. Biomarkers Prev. 3(6), 507-510 (1994).
57. Costa A, Malone W, Perloff M et al. Tolerability of the synthetic retinoid Fenretinide (HPR). Eur. J Cancer Clin. Oncol. 25(5), 805-808 (1989).
58. Zujewski J, Pai L, Wakefield L et al. Tamoxifen and fenretinide in women with metastatic breast cancer. Breast Cancer Res. Treat. 57(3), 277-283 (1999).
59. Cobleigh MA, Dowlatshahi K, Deutsch TA et al. Phase I/II trial of tamoxifen with or without fenretinide, an analog of vitamin A, in women with metastatic breast cancer. J. Clin. Oncol. 11(3), 474-477 (1993).
60. Decensi A, Torrisi R, Bruno S et al. Randomized trial of fenretinide in superficial bladder cancer using DNA-flow citometry as an intermediate endpoint. Proc. Am. Soc. Clin. Oncol. (1997).
61. Camerini T, Mariani L, De Palo G et al. Safety of the synthetic retinoid fenretinide: long-term results from a controlled clinical trial for the prevention of contralateral breast cancer. J. Clin. Oncol. 19(6), 1664-1670 (2001).
62. Conley B, O'Shaughnessy J, Prindiville S et al. Pilot trial of the safety, tolerability, and retinoid levels of N-(4-hydroxyphenyl) retinamide in combination with tamoxifen in patients at high risk for developing invasive breast cancer. J. Clin. Oncol. 18(2), 275-283 (2000).
63. Mariani L, Formelli F, De Palo G et al. Chemoprevention of breast cancer with fenretinide (4-HPR): study of long-term visual and ophthalmologic tolerability. Tumori 82(5), 444-449 (1996).
64. Decensi A, Torrisi R, Polizzi A et al. Effect of the synthetic retinoid fenretinide on dark adaptation and the ocular surface. J. Natl. Cancer Inst. 86(2), 105-110 (1994).
65. Caruso RC, Zujewski J, Iwata F et al. Effects of fenretinide (4-HPR) on dark adaptation. Arch. Ophthalmol. 116(6), 759-763 (1998).
66. Veronesi U, De Palo G, Marubini E et al. Randomized trial of fenretinide to prevent second breast malignancy in women with early breast cancer. J. Natl. Cancer Inst. 91(21), 1847-1856 (1999).
67. Turton JA, Willars GB, Haselden JN, Ward SJ, Steele CE, Hicks RM. Comparative teratogenicity of nine retinoids in the rat. Int. J. Exp. Pathol. 73(5), 551-563 (1992).
68. Kenel MF, Krayer JH, Merz EA, Pritchard JF. Teratogenicity of N-(4-hydroxyphenyl)-all-trans-retinamide in rats and rabbits. Teratog. Carcinog. Mutagen. 8(1), 1-11 (1988).
69. Formelli F, De Palo G, Costa A, Veronesi U. Human transplacental passage of the retinoid fenretinide (4HPR). Eur. J. Cancer 34(3), 428-429 (1998).
70. Torrisi R, Pensa F, Orengo MA et al. The synthetic retinoid fenretinide lowers plasma insulin-like growth factor I levels in breast cancer patients. Cancer Res. 53(20), 4769-4771 (1993).
71. Torrisi R, Paxodi S, Fontana V et al. Effect of fenretinide on plasma IGF-I and IGFBP-3 in early breast cancer patients. Int. J. Cancer 76(6), 787-790 (1998).
72. Pollak M. Insulin-like growth factor physiology and cancer risk. Eur. J. Cancer 36(10), 1224-1228 (2000).
73. Yu H, Rohan T. Role of the insulin-like growth factor family in cancer development and progression. J. Natl. Cancer Inst. 92(18), 1472-1489 (2000).
74. Moschos SJ, Mantzoros CS. The role of the IGF system in cancer: from basic to clinical studies and clinical applications. Oncology 63(4), 317-332 (2002).
75. Gill ZP, Perks CM, Newcomb PV, Holly JM. Insulin-like growth factor-binding protein (IGFBP-3) predisposes breast cancer cells to programmed cell death in a non-IGF-dependent manner. J. Biol. Chem. 272(41), 25602-25607 (1997).
76. Rajah R, Valentinis B, Cohen P. Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-β1 on programmed cell death through a p53- and IGF-independent mechanism. J. Biol. Chem. 272(18), 12181-12188 (1997).
77. Chan JM, Stampfer MJ, Giovannucci E, Ma J, Pollak M. Insulin-like growth factor I (IGF-I), IGF-binding protein-3 and prostate cancer risk: epidemiological studies. Growth Horm. IGF Res. 10(Suppl. A), S32-S33 (2000).
78. Giovannucci E, Pollak MN, Platz EA et al. A prospective study of plasma insulin-like growth factor-1 and binding protein-3 and risk of colorectal neoplasia in women. Cancer Epidemiol. Biomarkers Prev. 9(4), 345-349 (2000).
79. Hankinson SE, Willett WC, Colditz GA et al. Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 351(9113), 1393-1396 (1998).
80. London SJ, Yuan JM, Travlos GS et al. Insulin-like growth factor I, IGF-binding protein 3, and lung cancer risk in a prospective study of men in China. J. Natl. Cancer Inst. 94(10), 749-754 (2002).
81. Ma J, Pollak MN, Giovannucci E et al. Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J. Natl. Cancer Inst. 91(7), 620-625 (1999).
82. Toniolo P, Bruning PF, Akhmedkhanov A et al. Serum insulin-like growth factor-I and breast cancer. Int. J. Cancer 88(5), 828-832 (2000).
83. Renehan AG, Zwahlen M, Minder C, O'Dwyer ST, Shalet SM, Egger M. Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet 363(9418), 1346-1353 (2004).
84. Clarke RB, Howell A, Anderson E. Type I insulin-like growth factor receptor gene expression in normal human breast tissue treated with oestrogen and progesterone. Br. J. Cancer 75(2), 251-257 (1997).
85. Lai A, Sarcevic B, Prall OW, Sutherland RL. Insulin/insulin-like growth factor-I and estrogen cooperate to stimulate cyclin E-Cdk2 activation and cell cycle progression in MCF-7 breast cancer cells through differential regulation of cyclin E and p21(WAF1/Cip1). J. Biol. Chem. 276(28), 25823-25833 (2001).
86. Decensi A, Johansson H, Miceli R et al. Long-term effects of fenretinide, a retinoic acid derivative, on the insulin-like growth factor system in women with early breast cancer. Cancer Epidemiol. Biomarkers Prev. 10(10), 1047-1053 (2001).
87. Decensi A, Veronesi U, Miceli R et al. Relationships between plasma insulin-like growth factor-I and insulin-like growth factor binding protein-3 and second breast cancer risk in a prevention trial of fenretinide. Clin. Cancer Res. 9(13), 4722-4729 (2003)
88. Li Z, Meredith MP, Hoseyni MS. A method to assess the proportion of treatment effect explained by a surrogate endpoint. Stat. Med. 20(21), 3175-3188 (2001).
89. Freedman LS, Graubard BI, Schatzkin A. Statistical validation of intermediate endpoints for chronic diseases. Stat. Med. 11(2), 167-178 (1992).
90. Widschwendter M, Berger J, Daxenbichler G et al. Loss of retinoic acid receptor β expression in breast cancer and morphologically normal adjacent tissue but not in the normal breast tissue distant from the cancer. Cancer Res. 57(19), 4158-4161 (1997).
91. Veronesi U, Mariani L, Decensi A et al. Fifteen-year results of a randomized Phase III trial of fenretinide to prevent second breast cancer. Ann. Oncol. 17(7), 1065-1071 (2006).
92. Formelli F, Barua AB, Olson JA. Bioactivities of N-(4-hydroxyphenyl) retinamide and retinoyl β-glucuronide. FASEB J. 10(9), 1014-1024 (1996).
93. Formelli F, Cleris L. Synthetic retinoid fenretinide is effective against a human ovarian carcinoma xenograft and potentiates cisplatin activity. Cancer Res. 53(22), 5374-5376 (1993).
94. Kaiser PC, Korner M, Kappeler A, Aebi S. Retinoid receptors in ovarian cancer: expression and prognosis. Ann. Oncol. 16(9), 1477-1487 (2005).
95. De Palo G, Veronesi U, Camerini T et al. Can fenretinide protect women against ovarian cancer? J. Natl Cancer Inst. 87(2), 146-147 (1995).
96. De Palo G, Mariani L, Camerini T et al. Effect of fenretinide on ovarian carcinoma occurrence. Gynecol. Oncol. 86(1), 24-27 (2002).