Archives of Medical Research
Volume 40, Issue 6 , Pages 449-465 , August 2009

The Role of Retinoid Deficiency and Estrogens as Cofactors in Cervical Cancer

Received 14 May 2009 ,Accepted 9 July 2009.

References 

  1. zur Hausen H. Human papillomaviruses and their possible role in squamous cell carcinomas. Curr Top Microbiol Immunol. 1977;78:1–30
  2. Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999;189:12–19
  3. Munoz N, Bosch FX, de Sanjose S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348:518–527
  4. Bosch FX, Manos MM, Munoz N, et al. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International Biological Study on Cervical Cancer (IBSCC) Study Group. J Natl Cancer Inst. 1995;87:796–802
  5. Brown DR, Schroeder JM, Bryan JT, et al. Detection of multiple human papillomavirus types in condylomata acuminata lesions from otherwise healthy and immunosuppressed patients. J Clin Microbiol. 1999;37:3316–3322
  6. Lizano M, De la Cruz-Hernandez E, Carrillo-Garcia A, et al. Distribution of HPV16 and 18 intratypic variants in normal cytology, intraepithelial lesions, and cervical cancer in a Mexican population. Gynecol Oncol. 2006;102:230–235
  7. Smith JS, Lindsay L, Hoots B, et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer. 2007;121:621–632
  8. Clifford G, Franceschi S, Diaz M, et al. Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine. 2006;24(suppl 3):S3/26–34
  9. Bernard BA, Bailly C, Lenoir MC, et al. The human papillomavirus type 18 (HPV18) E2 gene product is a repressor of the HPV18 regulatory region in human keratinocytes. J Virol. 1989;63:4317–4324
  10. Romanczuk H, Thierry F, Howley PM. Mutational analysis of cis elements involved in E2 modulation of human papillomavirus type 16 P97 and type 18 P105 promoters. J Virol. 1990;64:2849–2859
  11. Thierry F, Howley PM. Functional analysis of E2-mediated repression of the HPV18 P105 promoter. New Biol. 1991;3:90–100
  12. Guido MC, Zamorano R, Garrido-Guerrero E, et al. Early promoters of genital and cutaneous human papillomaviruses are differentially regulated by the bovine papillomavirus type 1 E2 gene product. J Gen Virol. 1992;73(Pt 6):1395–1400
  13. Butz K, Hoppe-Seyler F. Transcriptional control of human papillomavirus (HPV) oncogene expression: composition of the HPV type 18 upstream regulatory region. J Virol. 1993;67:6476–6486
  14. Chen YH, Huang LH, Chen TM. Differential effects of progestins and estrogens on long control regions of human papillomavirus types 16 and 18. Biochem Biophys Res Commun. 1996;224:651–659
  15. Bromberg-White JL, Meyers C. The upstream regulatory region of human papillomavirus type 31 is insensitive to glucocorticoid induction. J Virol. 2002;76:9702–9715
  16. McLaughlin-Drubin ME, Huh KW, Munger K. Human papillomavirus type 16 E7 oncoprotein associates with E2F6. J Virol. 2008;82:8695–8705
  17. Boyer SN, Wazer DE, Band V. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 1996;56:4620–4624
  18. Scheffner M, Werness BA, Huibregtse JM, et al. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell. 1990;63:1129–1136
  19. Band V, De Caprio JA, Delmolino L, et al. Loss of p53 protein in human papillomavirus type 16 E6-immortalized human mammary epithelial cells. J Virol. 1991;65:6671–6676
  20. Halbert CL, Demers GW, Galloway DA. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J Virol. 1991;65:473–478
  21. Narisawa-Saito M, Kiyono T. Basic mechanisms of high-risk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci. 2007;98:1505–1511
  22. Boulet G, Horvath C, Vanden Broeck D, et al. Human papillomavirus: E6 and E7 oncogenes. Int J Biochem Cell Biol. 2007;39:2006–2011
  23. Lagunas-Martinez A, Madrid-Marina V, Gariglio P. Modulation of apoptosis by early human papillomavirus proteins in cervical cancer. Biochim Biophys Acta (in press).
  24. Shai A, Brake T, Somoza C, et al. The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res. 2007;67:1626–1635
  25. Nakagawa S, Huibregtse JM. Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol Cell Biol. 2000;20:8244–8253
  26. Nguyen ML, Nguyen MM, Lee D, et al. The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6's induction of epithelial hyperplasia in vivo. J Virol. 2003;77:6957–6964
  27. Munger K, Basile JR, Duensing S, et al. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene. 2001;20:7888–7898
  28. Hwang SG, Lee D, Kim J, et al. Human papillomavirus type 16 E7 binds to E2F1 and activates E2F1-driven transcription in a retinoblastoma protein-independent manner. J Biol Chem. 2002;277:2923–2930
  29. He W, Staples D, Smith C, et al. Direct activation of cyclin-dependent kinase 2 by human papillomavirus E7. J Virol. 2003;77:10566–10574
  30. Avvakumov N, Torchia J, Mymryk JS. Interaction of the HPV E7 proteins with the pCAF acetyltransferase. Oncogene. 2003;22:3833–3841
  31. Habig M, Smola H, Dole VS, et al. E7 proteins from high- and low-risk human papillomaviruses bind to TGF-beta-regulated Smad proteins and inhibit their transcriptional activity. Arch Virol. 2006;151:1961–1972
  32. Baldwin A, Huh KW, Munger K. Human papillomavirus E7 oncoprotein dysregulates steroid receptor coactivator 1 localization and function. J Virol. 2006;80:6669–6677
  33. Severino A, Abbruzzese C, Manente L, et al. Human papillomavirus-16 E7 interacts with Siva-1 and modulates apoptosis in HaCaT human immortalized keratinocytes. J Cell Physiol. 2007;212:118–125
  34. Mammas IN, Sourvinos G, Giannoudis A, Spandidos DA. Human papilloma virus (HPV) and host cellular interactions. Pathol Oncol Res. 2008;14:345–354
  35. Rangel LM, Ramirez M, Torroella M, et al. Multistep carcinogenesis and genital papillomavirus infection. Implications for diagnosis and vaccines. Arch Med Res. 1994;25:265–272
  36. Nair HB, Luthra R, Kirma N, et al. Induction of aromatase expression in cervical carcinomas: effects of endogenous estrogen on cervical cancer cell proliferation. Cancer Res. 2005;65:11164–11173
  37. Munoz N, Castellsague X, de Gonzalez AB, et al. Chapter 1: HPV in the etiology of human cancer. Vaccine. 2006;24(suppl 3):1–10
  38. Brisson J, Morin C, Fortier M, et al. Risk factors for cervical intraepithelial neoplasia: differences between low- and high-grade lesions. Am J Epidemiol. 1994;140:700–710
  39. Castle PE, Giuliano AR. Chapter 4: Genital tract infections, cervical inflammation, and antioxidant nutrients–assessing their roles as human papillomavirus cofactors. J Natl Cancer Inst Monogr. 2003;31:29–34
  40. Liu T, Soong SJ, Wilson NP, et al. A case control study of nutritional factors and cervical dysplasia. Cancer Epidemiol Biomarkers Prev. 1993;2:525–530
  41. Hildesheim A, Herrero R, Castle PE, et al. HPV co-factors related to the development of cervical cancer: results from a population-based study in Costa Rica. Br J Cancer. 2001;84:1219–1226
  42. Castle PE, Wacholder S, Lorincz AT, et al. A prospective study of high-grade cervical neoplasia risk among human papillomavirus-infected women. J Natl Cancer Inst. 2002;94:1406–1414
  43. Zoodsma M, Nolte IM, Te Meerman GJ, et al. HLA genes and other candidate genes involved in susceptibility for (pre)neoplastic cervical disease. Int J Oncol. 2005;26:769–784
  44. Zoodsma M, Nolte IM, Schipper M, et al. Analysis of the entire HLA region in susceptibility for cervical cancer: a comprehensive study. J Med Genet. 2005;42:e49
  45. Castellsague X, Munoz N. Chapter 3: Cofactors in human papillomavirus carcinogenesis–role of parity, oral contraceptives, and tobacco smoking. J Natl Cancer Inst Monogr. 2003;31:20–28
  46. Autier P, Coibion M, Huet F, et al. Transformation zone location and intraepithelial neoplasia of the cervix uteri. Br J Cancer. 1996;74:488–490
  47. Munoz N, Franceschi S, Bosetti C, et al. Role of parity and human papillomavirus in cervical cancer: the IARC multicentric case-control study. Lancet. 2002;359:1093–1101
  48. Sethi S, Muller M, Schneider A, et al. Serologic response to the E4, E6, and E7 proteins of human papillomavirus type 16 in pregnant women. Am J Obstet Gynecol. 1998;178:360–364
  49. Tolstrup J, Munk C, Thomsen BL, et al. The role of smoking and alcohol intake in the development of high-grade squamous intraepithelial lesions among high-risk HPV-positive women. Acta Obstet Gynecol Scand. 2006;85:1114–1119
  50. Alam S, Conway MJ, Chen HS, et al. The cigarette smoke carcinogen benzo[a]pyrene enhances human papillomavirus synthesis. J Virol. 2008;82:1053–1058
  51. Hecht SS. Cigarette smoking: cancer risks, carcinogens, and mechanisms. Langenbecks Arch Surg. 2006;391:603–613
  52. Yang X, Hao Y, Pater MM, et al. Enhanced expression of anti-apoptotic proteins in human papillomavirus-immortalized and cigarette smoke condensate-transformed human endocervical cells: correlation with resistance to apoptosis induced by DNA damage. Mol Carcinog. 1998;22:95–101
  53. Syrjanen K, Shabalova I, Petrovichev N, et al. Smoking is an independent risk factor for oncogenic human papillomavirus (HPV) infections but not for high-grade CIN. Eur J Epidemiol. 2007;22:723–735
  54. Giuliano AR, Gapstur S. Can cervical dysplasia and cancer be prevented with nutrients?. Nutr Rev. 1998;56:9–16
  55. Piyathilake CJ. Update on micronutrients and cervical dysplasia. Ethn Dis. 2007;17:(2 suppl2):14–17
  56. Butterworth CE, Hatch KD, Macaluso M, et al. Folate deficiency and cervical dysplasia. JAMA. 1992;267:528–533
  57. Hernandez BY, McDuffie K, Wilkens LR, et al. Diet and premalignant lesions of the cervix: evidence of a protective role for folate, riboflavin, thiamin, and vitamin B12. Cancer Causes Control. 2003;14:859–870
  58. Sedjo RL, Fowler BM, Schneider A, et al. Folate, vitamin B12, and homocysteine status. Findings of no relation between human papillomavirus persistence and cervical dysplasia. Nutrition. 2003;19:497–502
  59. Kwanbunjan K, Saengkar P, Cheeramakara C, et al. Vitamin B12 status of Thai women with neoplasia of the cervix uteri. Southeast Asian J Trop Med Public Health. 2006;37(suppl 3):178–183
  60. Piyathilake CJ, Macaluso M, Brill I, et al. Lower red blood cell folate enhances the HPV-16-associated risk of cervical intraepithelial neoplasia. Nutrition. 2007;23:203–210
  61. Garcia-Closas R, Castellsague X, Bosch X, et al. The role of diet and nutrition in cervical carcinogenesis: a review of recent evidence. Int J Cancer. 2005;117:629–637
  62. Giuliano AR, Papenfuss M, Nour M, et al. Antioxidant nutrients: associations with persistent human papillomavirus infection. Cancer Epidemiol Biomarkers Prev. 1997;6:917–923
  63. Sedjo RL, Roe DJ, Abrahamsen M, et al. Vitamin A, carotenoids, and risk of persistent oncogenic human papillomavirus infection. Cancer Epidemiol Biomarkers Prev. 2002;11:876–884
  64. Palan PR, Chang CJ, Mikhail MS, et al. Plasma concentrations of micronutrients during a nine-month clinical trial of beta-carotene in women with precursor cervical cancer lesions. Nutr Cancer. 1998;30:46–52
  65. Khachik F, Beecher GR, Smith JC. Lutein, lycopene, and their oxidative metabolites in chemoprevention of cancer. J Cell Biochem Suppl. 1995;22:236–246
  66. Conner EM, Grisham MB. Inflammation, free radicals, and antioxidants. Nutrition. 1996;12:274–277
  67. Anderson R, Theron AJ. Physiological potential of ascorbate, beta-carotene and alpha-tocopherol individually and in combination in the prevention of tissue damage, carcinogenesis and immune dysfunction mediated by phagocyte-derived reactive oxidants. World Rev Nutr Diet. 1990;62:27–58
  68. Looi ML, Mohd Dali AZ, Md Ali SA, et al. Oxidative damage and antioxidant status in patients with cervical intraepithelial neoplasia and carcinoma of the cervix. Eur J Cancer Prev. 2008;17:555–560
  69. Peterhans E. Reactive oxygen species and nitric oxide in viral diseases. Biol Trace Elem Res. 1997;56:107–116
  70. Palmer HJ, Paulson KE. Reactive oxygen species and antioxidants in signal transduction and gene expression. Nutr Rev. 1997;55:353–361
  71. Rosl F, Schwarz E. Regulation of E6 and E7 oncogenic transcription. In:  Tommasino M editors. Papillomaviruses in Human Cancer: Role of E6 and E7 Oncoproteins. Austin, TX: Landes Bioscience and Chapman & Hall; 1997;p. 25–70
  72. Siegel EM, Craft NE, Duarte-Franco E, et al. Associations between serum carotenoids and tocopherols and type-specific HPV persistence: the Ludwig–McGill cohort study. Int J Cancer. 2007;120:672–680
  73. Giuliano AR, Siegel EM, Roe DJ, et al. Dietary intake and risk of persistent human papillomavirus (HPV) infection: the Ludwig-McGill HPV natural history study. J Infect Dis. 2003;188:1508–1516
  74. Goodman MT, Shvetsov YB, McDuffie K, et al. Hawaii cohort study of serum micronutrient concentrations and clearance of incident oncogenic human papillomavirus infection of the cervix. Cancer Res. 2007;67:5987–5996
  75. Ghosh C, Baker JA, Moysich KB, et al. Dietary intakes of selected nutrients and food groups and risk of cervical cancer. Nutr Cancer. 2008;60:331–341
  76. Higdon JV, Delage B, Williams DE, et al. Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol Res. 2007;55:224–236
  77. Hecht SS. Inhibition of carcinogenesis by isothiocyanates. Drug Metab Rev. 2000;32:395–411
  78. Hong C, Kim HA, Firestone GL, et al. 3,3′-Diindolylmethane (DIM) induces a G(1) cell cycle arrest in human breast cancer cells that is accompanied by Sp1-mediated activation of p21(WAF1/CIP1) expression. Carcinogenesis. 2002;23:1297–1305
  79. Chen D, Carter TH, Auborn KJ. Apoptosis in cervical cancer cells: implications for adjunct anti-estrogen therapy for cervical cancer. Anticancer Res. 2004;24:2649–2656
  80. Jin L, Qi M, Chen DZ, et al. Indole-3-carbinol prevents cervical cancer in human papilloma virus type 16 (HPV16) transgenic mice. Cancer Res. 1999;59:3991–3997
  81. Arbeit JM, Howley PM, Hanahan D. Chronic estrogen-induced cervical and vaginal squamous carcinogenesis in human papillomavirus type 16 transgenic mice. Proc Natl Acad Sci USA. 1996;93:2930–2935
  82. Dallenbach-Hellweg G. Structural variations of cervical cancer and its precursors under the influence of exogenous hormones. Curr Top Pathol. 1981;70:143–170
  83. Goodman LS, Gilman A, Brunton LL, et al. Goodman & Gilman's The Pharmacological Basis of Therapeutics. 11th ed. New York: McGraw-Hill; 2006;
  84. Auborn KJ, Woodworth C, DiPaolo JA, et al. The interaction between HPV infection and estrogen metabolism in cervical carcinogenesis. Int J Cancer. 1991;49:867–869
  85. Santner SJ, Pauley RJ, Tait L, et al. Aromatase activity and expression in breast cancer and benign breast tissue stromal cells. J Clin Endocrinol Metab. 1997;82:200–208
  86. Bhattacharya D, Redkar A, Mittra I, et al. Oestrogen increases S-phase fraction and oestrogen and progesterone receptors in human cervical cancer in vivo. Br J Cancer. 1997;75:554–558
  87. Salazar EL, Sojo-Aranda I, Lopez R, et al. The evidence for an etiological relationship between oral contraceptive use and dysplastic change in cervical tissue. Gynecol Endocrinol. 2001;15:23–28
  88. Newfield L, Bradlow HL, Sepkovic DW, et al. Estrogen metabolism and the malignant potential of human papillomavirus immortalized keratinocytes. Proc Soc Exp Biol Med. 1998;217:322–326
  89. Swaneck GE, Fishman J. Covalent binding of the endogenous estrogen 16 alpha-hydroxyestrone to estradiol receptor in human breast cancer cells: characterization and intranuclear localization. Proc Natl Acad Sci USA. 1988;85:7831–7835
  90. Telang NT, Suto A, Wong GY, et al. Induction by estrogen metabolite 16 alpha-hydroxyestrone of genotoxic damage and aberrant proliferation in mouse mammary epithelial cells. J Natl Cancer Inst. 1992;84:634–638
  91. de Villiers EM. Relationship between steroid hormone contraceptives and HPV, cervical intraepithelial neoplasia and cervical carcinoma. Int J Cancer. 2003;103:705–708
  92. Salazar EL, Mercado E, Sojo I, et al. Relationship between estradiol 16 alpha-hydroxylation and human papillomavirus infection in cervical cell transformation. Gynecol Endocrinol. 2001;15:335–340
  93. Wheeler WJ, Cherry LM, Downs T, et al. Mitotic inhibition and aneuploidy induction by naturally occurring and synthetic estrogens in Chinese hamster cells in vitro. Mutat Res. 1986;171:31–41
  94. Barrett JC, Hesterberg TW, Oshimura M, Tsutsui T. Role of chemically induced mutagenic events in neoplastic transformation of Syrian hamster embryo cells. Carcinog Compr Surv. 1985;9:123–137
  95. Hajek RA, King DW, Hernandez-Valero MA, et al. Detection of chromosomal aberrations by fluorescence in situ hybridization in cervicovaginal biopsies from women exposed to diethylstilbestrol in utero. Int J Gynecol Cancer. 2006;16:318–324
  96. Singer A, Jordan JA. Basic structure and function of the cervix. In:  Jordan J,  Singer A,  Jones H,  Shafi M editor. The Cervix. 2nd ed. London: Wiley-Blackwell; 1976;
  97. Birchmeier C, Meyer D, Riethmacher D. Factors controlling growth, motility, and morphogenesis of normal and malignant epithelial cells. Int Rev Cytol. 1995;160:221–266
  98. Brake T, Lambert PF. Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc Natl Acad Sci USA. 2005;102:2490–2495
  99. Woodworth CD. HPV innate immunity. Front Biosci. 2002;7:d2058–d2071
  100. Mendoza-Villanueva D, Diaz-Chavez J, Uribe-Figueroa L, et al. Gene expression profile of cervical and skin tissues from human papillomavirus type 16 E6 transgenic mice. BMC Cancer. 2008;8:347
  101. Hughes RG, Norval M, Howie SE. Expression of major histocompatibility class II antigens by Langerhans' cells in cervical intraepithelial neoplasia. J Clin Pathol. 1988;41:253–259
  102. Memar OM, Arany I, Tyring SK. Skin-associated lymphoid tissue in human immunodeficiency virus-1, human papillomavirus, and herpes simplex virus infections. J Invest Dermatol. 1995;105:99S–104S
  103. Frazer IH. Interaction of human papillomaviruses with the host immune system: a well evolved relationship. Virology. 2009;384:410–414
  104. Kaushic C, Frauendorf E, Rossoll RM, et al. Influence of the estrous cycle on the presence and distribution of immune cells in the rat reproductive tract. Am J Reprod Immunol. 1998;39:209–216
  105. Wira CR, Rossoll RM. Antigen-presenting cells in the female reproductive tract: influence of sex hormones on antigen presentation in the vagina. Immunology. 1995;84:505–508
  106. Prabhala RH, Wira CR. Sex hormone and IL-6 regulation of antigen presentation in the female reproductive tract mucosal tissues. J Immunol. 1995;155:5566–5573
  107. Gruber CJ, Tschugguel W, Schneeberger C, et al. Production and actions of estrogens. N Engl J Med. 2002;346:340–352
  108. Wang H, Eriksson H, Sahlin L. Estrogen receptors alpha and beta in the female reproductive tract of the rat during the estrous cycle. Biol Reprod. 2000;63:1331–1340
  109. Remoue F, Jacobs N, Miot V, et al. High intraepithelial expression of estrogen and progesterone receptors in the transformation zone of the uterine cervix. Am J Obstet Gynecol. 2003;189:1660–1665
  110. Shew ML, McGlennen R, Zaidi N, et al. Oestrogen receptor transcripts associated with cervical human papillomavirus infection. Sex Transm Infect. 2002;78:210–214
  111. Au WW, Abdou-Salama S, Al-Hendy A. Inhibition of growth of cervical cancer cells using a dominant negative estrogen receptor gene. Gynecol Oncol. 2007;104:276–280
  112. Heo MY, Salama SA, Khatoon N, et al. Abrogation of estrogen receptor signaling augments cytotoxicity of anticancer drugs on CaSki cervical cancer cells. Anticancer Res. 2008;28:2181–2187
  113. Chen GG, Zeng Q, Tse GM. Estrogen and its receptors in cancer. Med Res Rev. 2008;28:954–974
  114. Ricke WA, Wang Y, Cunha GR. Steroid hormones and carcinogenesis of the prostate: the role of estrogens. Differentiation. 2007;75:871–882
  115. Cho NL, Javid SH, Carothers AM, et al. Estrogen receptors alpha and beta are inhibitory modifiers of Apc-dependent tumorigenesis in the proximal colon of Min/+ mice. Cancer Res. 2007;67:2366–2372
  116. Chung SH, Wiedmeyer K, Shai A, et al. Requirement for estrogen receptor alpha in a mouse model for human papillomavirus-associated cervical cancer. Cancer Res. 2008;68:9928–9934
  117. Mitrani-Rosenbaum S, Tsvieli R, Tur-Kaspa R. Oestrogen stimulates differential transcription of human papillomavirus type 16 in SiHa cervical carcinoma cells. J Gen Virol. 1989;70(Pt 8):2227–2232
  118. Kim CJ, Um SJ, Kim TY, et al. Regulation of cell growth and HPV genes by exogenous estrogen in cervical cancer cells. Int J Gynecol Cancer. 2000;10:157–164
  119. Vogt PK, Bos TJ. jun: oncogene and transcription factor. Adv Cancer Res. 1990;55:1–35
  120. Milde-Langosch K. The Fos family of transcription factors and their role in tumourigenesis. Eur J Cancer. 2005;41:2449–2461
  121. de Wilde J, De-Castro Arce J, Snijders PJ, Meijer CJ, Rosl F, Steenbergen RD. Alterations in AP-1 and AP-1 regulatory genes during HPV-induced carcinogenesis. Cell Oncol. 2008;30:77–87
  122. Thierry F, Spyrou G, Yaniv M, et al. Two AP1 sites binding JunB are essential for human papillomavirus type 18 transcription in keratinocytes. J Virol. 1992;66:3740–3748
  123. De-Castro Arce J, Soto U, van Riggelen J, et al. Ectopic expression of nonliganded retinoic acid receptor beta abrogates AP-1 activity by selective degradation of c-Jun in cervical carcinoma cells. J Biol Chem. 2004;279:45408–45416
  124. Nurnberg W, Artuc M, Vorbrueggen G, et al. Nuclear proto-oncogene products transactivate the human papillomavirus type 16 promoter. Br J Cancer. 1995;71:1018–1024
  125. Weisz A, Rosales R. Identification of an estrogen response element upstream of the human c-fos gene that binds the estrogen receptor and the AP-1 transcription factor. Nucleic Acids Res. 1990;18:5097–5106
  126. Weisz A, Cicatiello L, Persico E, et al. Estrogen stimulates transcription of c-jun protooncogene. Mol Endocrinol. 1990;4:1041–1050
  127. Paech K, Webb P, Kuiper GG, et al. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science. 1997;277:1508–1510
  128. Wang WM, Chung MH, Huang SM. Regulation of nuclear receptor activities by two human papillomavirus type 18 oncoproteins, E6 and E7. Biochem Biophys Res Commun. 2003;303:932–939
  129. Webster K, Taylor A, Gaston K. Oestrogen and progesterone increase the levels of apoptosis induced by the human papillomavirus type 16 E2 and E7 proteins. J Gen Virol. 2001;82:201–213
  130. Webster K, Parish J, Pandya M, et al. The human papillomavirus (HPV) 16 E2 protein induces apoptosis in the absence of other HPV proteins and via a p53-dependent pathway. J Biol Chem. 2000;275:87–94
  131. Sanchez-Perez AM, Soriano S, Clarke AR, et al. Disruption of the human papillomavirus type 16 E2 gene protects cervical carcinoma cells from E2F-induced apoptosis. J Gen Virol. 1997;78(Pt 11):3009–3018
  132. Wang Q, Li X, Wang L, et al. Antiapoptotic effects of estrogen in normal and cancer human cervical epithelial cells. Endocrinology. 2004;145:5568–5579
  133. Ruutu M, Wahlroos N, Syrjanen K, et al. Effects of 17β-estradiol and progesterone on transcription of human papillomavirus 16 E6/E7 oncogenes in CaSki and SiHa cell lines. Int J Gynecol Cancer. 2006;16:1261–1268
  134. Comerford SA, Maika SD, Laimins LA, et al. E6 and E7 expression from the HPV 18 LCR: development of genital hyperplasia and neoplasia in transgenic mice. Oncogene. 1995;10:587–597
  135. Cid A, Auewarakul P, Garcia-Carranca A, et al. Cell-type-specific activity of the human papillomavirus type 18 upstream regulatory region in transgenic mice and its modulation by tetradecanoyl phorbol acetate and glucocorticoids. J Virol. 1993;67:6742–6752
  136. Michelin D, Gissmann L, Street D, et al. Regulation of human papillomavirus type 18 in vivo: effects of estrogen and progesterone in transgenic mice. Gynecol Oncol. 1997;66:202–208
  137. Park JS, Rhyu JW, Kim CJ, et al. Neoplastic change of squamo-columnar junction in uterine cervix and vaginal epithelium by exogenous estrogen in hpv-18 URR E6/E7 transgenic mice. Gynecol Oncol. 2003;89:360–368
  138. Arbeit JM, Munger K, Howley PM, et al. Progressive squamous epithelial neoplasia in K14–human papillomavirus type 16 transgenic mice. J Virol. 1994;68:4358–4368
  139. Elson DA, Riley RR, Lacey A, et al. Sensitivity of the cervical transformation zone to estrogen-induced squamous carcinogenesis. Cancer Res. 2000;60:1267–1275
  140. Shai A, Brake T, Somoza C, et al. The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res. 2007;67:1626–1635
  141. Balsitis S, Dick F, Dyson N, et al. Critical roles for non–pRb targets of human papillomavirus type 16 E7 in cervical carcinogenesis. Cancer Res. 2006;66:9393–9400
  142. Sporn MB, Dunlop NM, Newton DL, et al. Prevention of chemical carcinogenesis by vitamin A and its synthetic analogs (retinoids). Fed Proc. 1976;35:1332–1338
  143. Chambon P. The nuclear receptor superfamily: a personal retrospect on the first two decades. Mol Endocrinol. 2005;19:1418–1428
  144. Kastner P, Mark M, Chambon P. Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life?. Cell. 1995;83:859–869
  145. Niederreither K, Abu-Abed S, Schuhbaur B, et al. Genetic evidence that oxidative derivatives of retinoic acid are not involved in retinoid signaling during mouse development. Nat Genet. 2002;31:84–88
  146. Bonanni B, Lazzeroni M. Retinoids and breast cancer prevention. Recent Results Cancer Res. 2009;181:77–82
  147. Lens M, Medenica L. Systemic retinoids in chemoprevention of non-melanoma skin cancer. Expert Opin Pharmacother. 2008;9:1363–1374
  148. Brtko J. Role of retinoids and their cognate nuclear receptors in breast cancer chemoprevention. Cent Eur J Public Health. 2007;15:3–6
  149. Fields AL, Soprano DR, Soprano KJ. Retinoids in biological control and cancer. J Cell Biochem. 2007;102:886–898
  150. Okuno M, Kojima S, Matsushima-Nishiwaki R, et al. Retinoids in cancer chemoprevention. Curr Cancer Drug Targets. 2004;4:285–298
  151. Robinson-Rechavi M, Escriva Garcia H, Laudet V. The nuclear receptor superfamily. J Cell Sci. 2003;116:585–586
  152. Giguere V, Ong ES, Segui P, et al. Identification of a receptor for the morphogen retinoic acid. Nature. 1987;330:624–629
  153. Benbrook D, Lernhardt E, Pfahl M. A new retinoic acid receptor identified from a hepatocellular carcinoma. Nature. 1988;333:669–672
  154. Krust A, Kastner P, Petkovich M, et al. A third human retinoic acid receptor, hRAR-gamma. Proc Natl Acad Sci USA. 1989;86:5310–5314
  155. Mangelsdorf DJ, Borgmeyer U, Heyman RA, et al. Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev. 1992;6:329–344
  156. Heyman RA, Mangelsdorf DJ, Dyck JA, et al. 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell. 1992;68:397–406
  157. Allenby G, Bocquel MT, Saunders M, et al. Retinoic acid receptors and retinoid X receptors: interactions with endogenous retinoic acids. Proc Natl Acad Sci USA. 1993;90:30–34
  158. Mangelsdorf DJ, Evans RM. The RXR heterodimers and orphan receptors. Cell. 1995;83:841–850
  159. Kastner P, Mark M, Ghyselinck N, et al. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development. 1997;124:313–326
  160. Mark M, Ghyselinck NB, Wendling O, et al. A genetic dissection of the retinoid signalling pathway in the mouse. Proc Nutr Soc. 1999;58:609–613
  161. Zhang XK, Lehmann J, Hoffmann B, et al. Homodimer formation of retinoid X receptor induced by 9-cis retinoic acid. Nature. 1992;358:587–591
  162. Leid M, Kastner P, Chambon P. Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem Sci. 1992;17:427–433
  163. Hu X, Lazar MA. Transcriptional repression by nuclear hormone receptors. Trends Endocrinol Metab. 2000;11:6–10
  164. Aranda A, Pascual A. Nuclear hormone receptors and gene expression. Physiol Rev. 2001;81:1269–1304
  165. Privalsky ML. Regulation of SMRT and N-CoR corepressor function. Curr Top Microbiol Immunol. 2001;254:117–136
  166. McKenna NJ, O'Malley BW. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell. 2002;108:465–474
  167. Darwiche N, Celli G, De Luca LM. Specificity of retinoid receptor gene expression in mouse cervical epithelia. Endocrinology. 1994;134:2018–2025
  168. Li M, Indra AK, Warot X, et al. Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis. Nature. 2000;407:633–636
  169. Metzger D, Indra AK, Li M, et al. Targeted conditional somatic mutagenesis in the mouse: temporally-controlled knock out of retinoid receptors in epidermal keratinocytes. Methods Enzymol. 2003;364:379–408
  170. Chapellier B, Mark M, Bastien J, et al. A conditional floxed (loxP-flanked) allele for the retinoic acid receptor beta (RARbeta) gene. Genesis. 2002;32:91–94
  171. Ocadiz-Delgado R, Castaneda-Saucedo E, Indra AK, et al. Impaired cervical homeostasis upon selective ablation of RXRalpha in epithelial cells. Genesis. 2008;46:19–28
  172. Zhou Q, Stetler-Stevenson M, Steeg PS. Inhibition of cyclin D expression in human breast carcinoma cells by retinoids in vitro. Oncogene. 1997;15:107–115
  173. Seewaldt VL, Kim JH, Parker MB, et al. Dysregulated expression of cyclin D1 in normal human mammary epithelial cells inhibits all-trans-retinoic acid-mediated G0/G1-phase arrest and differentiation in vitro. Exp Cell Res. 1999;249:70–85
  174. Sah JF, Eckert RL, Chandraratna RA, et al. Retinoids suppress epidermal growth factor-associated cell proliferation by inhibiting epidermal growth factor receptor-dependent ERK1/2 activation. J Biol Chem. 2002;277:9728–9735
  175. Arany I, Ember IA, Tyring SK. All-trans-retinoic acid activates caspase-1 in a dose-dependent manner in cervical squamous carcinoma cells. Anticancer Res. 2003;23:471–473
  176. Altucci L, Gronemeyer H. The promise of retinoids to fight against cancer. Nat Rev Cancer. 2001;1:181–193
  177. Clarke N, Jimenez-Lara AM, Voltz E, et al. Tumor suppressor IRF-1 mediates retinoid and interferon anticancer signaling to death ligand TRAIL. EMBO J. 2004;23:3051–3060
  178. Niles RM. Signaling pathways in retinoid chemoprevention and treatment of cancer. Mutat Res. 2004;555:81–96
  179. Nagy L, Thomazy VA, Heyman RA, et al. Retinoid-induced apoptosis in normal and neoplastic tissues. Cell Death Differ. 1998;5:11–19
  180. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J. 1996;10:940–954
  181. Nagpal S, Zelent A, Chambon P. RAR-beta 4, a retinoic acid receptor isoform is generated from RAR-beta 2 by alternative splicing and usage of a CUG initiator codon. Proc Natl Acad Sci USA. 1992;89:2718–2722
  182. Sommer KM, Chen LI, Treuting PM, et al. Elevated retinoic acid receptor beta(4) protein in human breast tumor cells with nuclear and cytoplasmic localization. Proc Natl Acad Sci USA. 1999;96:8651–8656
  183. Gebert JF, Moghal N, Frangioni JV, et al. High frequency of retinoic acid receptor beta abnormalities in human lung cancer. Oncogene. 1991;6:1859–1868
  184. Xu XC, Ro JY, Lee JS, et al. Differential expression of nuclear retinoid receptors in normal, premalignant, and malignant head and neck tissues. Cancer Res. 1994;54:3580–3587
  185. Swisshelm K, Ryan K, Lee X. Down-regulation of retinoic acid receptor beta in mammary carcinoma cell lines and its up-regulation in senescing normal mammary epithelial cells. Cell Growth Differ. 1994;5:133–141
  186. Crowe DL, Hu L, Gudas LJ, et al. Variable expression of retinoic acid receptor (RAR beta) mRNA in human oral and epidermal keratinocytes; relation to keratin 19 expression and keratinization potential. Differentiation. 1991;48:199–208
  187. Geisen C, Denk C, Gremm B, et al. High-level expression of the retinoic acid receptor beta gene in normal cells of the uterine cervix is regulated by the retinoic acid receptor alpha and is abnormally down-regulated in cervical carcinoma cells. Cancer Res. 1997;57:1460–1467
  188. Xu XC, Mitchell MF, Silva E, et al. Decreased expression of retinoic acid receptors, transforming growth factor beta, involucrin, and cornifin in cervical intraepithelial neoplasia. Clin Cancer Res. 1999;5:1503–1508
  189. Houle B, Rochette-Egly C, Bradley WE. Tumor-suppressive effect of the retinoic acid receptor beta in human epidermoid lung cancer cells. Proc Natl Acad Sci USA. 1993;90:985–989
  190. Liu Y, Lee MO, Wang HG, et al. Retinoic acid receptor beta mediates the growth-inhibitory effect of retinoic acid by promoting apoptosis in human breast cancer cells. Mol Cell Biol. 1996;16:1138–1149
  191. Si SP, Lee X, Tsou HC, et al. RAR beta 2-mediated growth inhibition in HeLa cells. Exp Cell Res. 1996;223:102–111
  192. Berard J, Laboune F, Mukuna M, et al. Lung tumors in mice expressing an antisense RARbeta2 transgene. FASEB J. 1996;10:1091–1097
  193. Kaiser A, Herbst H, Fisher G, et al. Retinoic acid receptor beta regulates growth and differentiation in human pancreatic carcinoma cells. Gastroenterology. 1997;113:920–929
  194. Faria TN, Mendelsohn C, Chambon P, et al. The targeted disruption of both alleles of RARbeta(2) in F9 cells results in the loss of retinoic acid-associated growth arrest. J Biol Chem. 1999;274:26783–26788
  195. Lin F, Xiao D, Kolluri SK, et al. Unique anti-activator protein-1 activity of retinoic acid receptor beta. Cancer Res. 2000;60:3271–3280
  196. Toulouse A, Morin J, Dion PA, et al. RARbeta2 specificity in mediating RA inhibition of growth of lung cancer-derived cells. Lung Cancer. 2000;28:127–137
  197. Geisen C, Denk C, Kupper JH, et al. Growth inhibition of cervical cancer cells by the human retinoic acid receptor beta gene. Int J Cancer. 2000;85:289–295
  198. Ivanova T, Petrenko A, Gritsko T, et al. Methylation and silencing of the retinoic acid receptor-beta 2 gene in cervical cancer. BMC Cancer. 2002;2:4
  199. Virmani AK, Rathi A, Zochbauer-Muller S, et al. Promoter methylation and silencing of the retinoic acid receptor-beta gene in lung carcinomas. J Natl Cancer Inst. 2000;92:1303–1307
  200. Youssef EM, Lotan D, Issa JP, et al. Hypermethylation of the retinoic acid receptor-beta(2) gene in head and neck carcinogenesis. Clin Cancer Res. 2004;10:1733–1742
  201. Suh YA, Lee HY, Virmani A, et al. Loss of retinoic acid receptor beta gene expression is linked to aberrant histone H3 acetylation in lung cancer cell lines. Cancer Res. 2002;62:3945–3949
  202. Soto U, Denk C, Finzer P, et al. Genetic complementation to non-tumorigenicity in cervical-carcinoma cells correlates with alterations in AP-1 composition. Int J Cancer. 2000;86:811–817
  203. Prusty BK, Das BC. Constitutive activation of transcription factor AP-1 in cervical cancer and suppression of human papillomavirus (HPV) transcription and AP-1 activity in HeLa cells by curcumin. Int J Cancer. 2005;113:951–960
  204. Huang C, Ma WY, Dawson MI, et al. Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid. Proc Natl Acad Sci USA. 1997;94:5826–5830
  205. Yang-Yen HF, Zhang XK, Graupner G, et al. Antagonism between retinoic acid receptors and AP-1: implications for tumor promotion and inflammation. New Biol. 1991;3:1206–1219
  206. Schule R, Rangarajan P, Yang N, et al. Retinoic acid is a negative regulator of AP-1-responsive genes. Proc Natl Acad Sci USA. 1991;88:6092–6096
  207. De-Castro Arce J, Gockel-Krzikalla E, Rosl F. Retinoic acid receptor beta silences human papillomavirus-18 oncogene expression by induction of de novo methylation and heterochromatinization of the viral control region. J Biol Chem. 2007;282:28520–28529
  208. Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene. 2001;20:2390–2400
  209. Suzukawa K, Colburn NH. AP-1 transrepressing retinoic acid does not deplete coactivators or AP-1 monomers but may target specific Jun or Fos containing dimers. Oncogene. 2002;21:2181–2190
  210. Zhou XF, Shen XQ, Shemshedini L. Ligand-activated retinoic acid receptor inhibits AP-1 transactivation by disrupting c-Jun/c-Fos dimerization. Mol Endocrinol. 1999;13:276–285
  211. Kamei Y, Xu L, Heinzel T, et al. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell. 1996;85:403–414
  212. Lee HY, Walsh GL, Dawson MI, et al. All-trans-retinoic acid inhibits Jun N-terminal kinase-dependent signaling pathways. J Biol Chem. 1998;273:7066–7071

PII: S0188-4409(09)00140-4

doi: 10.1016/j.arcmed.2009.08.002

Archives of Medical Research
Volume 40, Issue 6 , Pages 449-465 , August 2009

Article Tools

* Image Usage & Resolution