Gene therapy targeting leiomyoma: adenovirus-mediated delivery of dominant-negative estrogen receptor gene shrinks uterine tumors in Eker rat model

Fertility and Sterility

Volumn 93, Issue 1, 2010, Pages 239-250

  Hassan, Memy H ^a,b   Salama, Salama A ^a   Zhang, Dong ^c,d   Arafa, Hossam M M ^b   Hamada, Farid M A ^b   Fouad, Hala ^a   Walker, Cheryl C ^c   Al Hendy, Ayman ^a,d  

^a University of Texas Medical Branch School of Medicine   (United States)

^b Al Azhar University   (Egypt)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

dominant negative estrogen receptor; gene therapy; Uterine leiomyoma

Indexed keywords

BETA GALACTOSIDASE; CASPASE 3; DOMINANT NEGATIVE ESTROGEN RECEPTOR; ESTROGEN RECEPTOR; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CLINICAL ASSESSMENT; CONSERVATIVE TREATMENT; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; GENE TARGETING; GENE THERAPY; INOCULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SAFETY; SERUM; TRANSGENE; TUMOR VOLUME; UTERUS MYOMA; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CELL CYCLE PROTEINS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ESTROGEN RECEPTOR ALPHA; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE THERAPY; GENETIC VECTORS; IMMUNITY, HUMORAL; LEIOMYOMA; MAGNETIC RESONANCE IMAGING; MUTATION; RATS; RATS, MUTANT STRAINS; TIME FACTORS; TRANSFECTION; TUMOR BURDEN; TUMOR SUPPRESSOR PROTEINS; UTERINE NEOPLASMS;

EID: 72749106400     PISSN: 00150282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2008.09.086     Document Type: Article

References (93)

1. Maruo T., Matsuo H., Samoto T., Shimomura Y., Kurachi O., Gao Z., et al. Effects of progesterone on uterine leiomyoma growth and apoptosis. Steroids 65 (2000) 585-592
2. Walker C.L., Burroughs K.D., Davis B., Sowell K., Everitt J.I., and Fuchs-Young R. Preclinical evidence for therapeutic efficacy of selective estrogen receptor modulators for uterine leiomyoma. J Soc Gynecol Invest 7 (2000) 249-256
3. Stewart E.A. Uterine fibroids. Lancet 357 9252 (2001) 293-298
4. Farhi J., Ashkenazi J., Feldberg D., Dicker D., Orvieto R., and Ben Rafael Z. Effect of uterine leiomyomata on the results of in-vitro fertilization treatment. Hum Reprod 10 (1995) 2576-2578
5. Eldar-Geva T., Meagher S., Healy D.L., MacLachlan V., Breheny S., Wood C., et al. Effect of intramural, subserosal, and submucosal uterine fibroids on the outcome of assisted reproductive technology treatment. Fertil Steril 70 (1998) 687-691
6. Surrey E.S., Lietz A.K., and Schoolcraft W.B. Impact of intramural leiomyomata in patients with a normal endometrial cavity on in vitro fertilization-embryo transfer cycle outcome. Fertil Steril 75 (2001) 405-410
7. Hart R., Khalaf Y., Yeong C.T., Seed P., Taylor A., and Braude P. A prospective controlled study of the effect of intramural uterine fibroids on the outcome of assisted conception. Hum Reprod 16 (2001) 2411-2417
8. Rein M.S., Barbieri R.L., and Friedman A.J. Progesterone: a critical role in the pathogenesis of uterine myomas. Am J Obstet Gynecol 172 (1995) 14-18
9. Coddington C.C., Collins R.L., Shawker T., Anderson R., Loriaux D.L., and Winkel C.A. Long-acting gonadotropin hormone-releasing hormone analog used to treat uteri. Fertil Steril 45 (1986) 624-629
10. Kawaguchi K., Fujii S., Konishi I., Nanbu Y., Nonogaki H., and Mori T. Mitotic activity in uterine leiomyomas during the menstrual cycle. Am J Obstetric Gynecology 160 (1989) 637-641
11. Stewart E.A., and Nowak R.A. Leiomyoma-related bleeding: a classic hypothesis updated for the molecular era. Hum Reprod Update 4 (1996) 295-296
12. Chegini N., Verala J., Luo X., Xu J., and Williams R.S. Gene expression profile of leiomyoma and myometrium and the effect of gonadotropin releasing hormone analogue therapy. J Soc Gynecol Investig 10 (2003) 161-171
13. Sozen I., and Arici A. Interactions of cytokines, growth factors, and the extracellular matrix in the cellular biology of uterine leiomyomata. Fertil Steril 78 (2002) 1-12
14. Al-Hendy A., Lee E.J., Wang H.Q., and Copland J.A. Gene therapy of uterine leiomyomas: adenovirus-mediated expression of dominant negative estrogen receptor inhibits tumor growth in nude mice. Am J Obstet Gynecol 191 (2004) 1621-1631
15. Parazzini F., Negri E., La Vecchia C., Chatenoud L., Ricci E., and Guarnerio P. Reproductive factors and risk of uterine fibroids. Epidemiology 7 (1996) 440-442
16. Ross R.K., Pike M.C., Vessey M.P., Bull D., Yeates D., and Casagrande J.T. Risk factors for uterine fibroids: reduced risk associated with oral contraceptives. BMJ 293 (1986) 359-362
17. Benassayag C., Leroy M.J., Rigourd V., Robert B., Honore J.C., Mignot T.M., et al. Estrogen receptors (ERalpha/ERbeta) in normal and pathological growth of the human myometrium: pregnancy and leiomyoma. Am J Physiol 276 (1999) E1112-E1118
18. Wang Y. Down-regulation of proliferation and up-regulation of apoptosis by gonadotropin-releasing hormone agonist in cultured uterine leiomyoma cells. Eur J Endocrinol 146 (2002) 447-456
19. Al-Hendy A., and Salama S.A. Ethnic distribution of estrogen receptor-alpha polymorphism is associated with a higher prevalence of uterine leiomyomas in black Americans. Fertil Steril 86 (2006) 686-693
20. Brandon D.D., Bethea C.L., Strawn E.Y., Novy M.J., Burry K.A., Harrington M.S., et al. Progesterone receptor messenger ribonucleic acid and protein are over expressed in human uterine leiomyomas. Am J Obstet Gynecol 169 (1993) 78-85
21. Brandon D.D., Erickson T.E., Keenan E.J., Strawn E.Y., Novy M.J., Burry K.A., et al. Estrogen receptor gene expression in human uterine leiomyomata. J Clin Endocrinol Metab 80 (1995) 1876-1881
22. Thorp J.M., and Katz V.L. Submucous myomas treated with gonadotropin releasing hormone agonist and resulting in vaginal hemorrhage. A case report. J Reprod Med 36 (1991) 625-626
23. Vilos G.A. Treatment options for uterine fibroids. [abstract]. Can J Diag 17 (2000) 55-59
24. Walker C.L., and Stewart E.A. Uterine fibroids: the elephant in the room. Science 308 (2005) 1589-1592
25. Bachmann G. Expanding treatment options for women with symptomatic uterine leiomyomas: timely medical breakthroughs. Fertil Steril 85 (2006) 46-47
26. Lefebvre G., Allaire C., Jeffrey J., Vilos G.A., Arneja J., Birch C., et al., Society of Obstetricians and Gynecologists of Canada [SOGC]. Clinical Practice Gynecology Committee and Executive Committee and Council. SOGC clinical guidelines. Hysterectomy. J Obstet Gynecol Can 24 (2002) 37-76
27. VeKaut B.S. Changing trends in treatment of leiomyomata uteri. [abstract]. Curr Opin Obstet Gynecol 5 (1993) 301
28. Al Hendy A., and Salama A. Gene therapy and uterine leiomyoma: a review. Hum Reprod Update 16 (2006) 385-400
29. Vercellini P., Maddalena S., De Giorgi O., Aimi G., and Crosignani P.G. Abdominal myomectomy for infertility: a comprehensive review. Hum Reprod 13 (1998) 873-879
30. Vilos G.A., Daly L.J., and Tse B.M. Pregnancy outcome after laparoscopic electromyolysis. J Am Assoc Gynecol Laparosc 5 (1998) 289-292
31. Payne J.F., and Haney A.F. Serious complications of uterine artery embolization for conservative treatment of fibroids. Fertil Steril 79 (2003) 128-131
32. Andrei J.L., Marshall L.A., Domestic D.A., and Jaffe R.B. Therapeutic uses of gonadotropin-releasing hormone analogs. Obstet Gynecol Surv 42 (1987) 1-21
33. Eisinger S.H., Meldrum S., Fiscella K., Le Roux H.D., and Guzick D.S. Low-dose mifepristone for uterine leiomyomata. Obstet Gynecol 101 (2003) 243-250
34. Ince B.A., Zhuang Y Wrenn C.K., Shapiro D.J., and Katzenellenbogen B.S. Powerful dominant negative mutants of the human estrogen receptor. J Biol Chem 268 (1993) 14026-14032
35. Houston K.D., Hunter D.S., Hodges L.C., and Walker C.L. Uterine leiomyomas: mechanisms of tumorigenesis. Toxicol Pathol 29 (2001) 100-104
36. Cook J.D., and Walker C.L. The Eker rat: establishing a genetic paradigm linking renal cell carcinoma and uterine leiomyoma. Curr Mol Med 4 (2004) 813-824
37. Everitt J.I., Wolf D.C., Howe S.R., Goldsworthy T.L., and Walker C.L. Rodent model of reproductive tract leiomyomata. Clinical and pathological features. Am J Pathol 146 (1995) 1556-1567
38. Lee E.J., Duan W.R., Jakacka M., Gehm B.D., and Jameson J.L. Dominant negative ER induces apoptosis in GH (4) pituitary lactotrope cells and inhibits tumor growth in nude mice. Endocrinol 142 (2001) 3756-3763
39. Al-Hendy A., Magliocco A.M., Al Tweigeri T., Braileanu G., Crellin N., Li H., et al. Ovarian cancer gene therapy: repeated treatment with thymidine kinase in an adenovirus vector and ganciclovir improves survival in a novel immunocompetent murine model. Am J Obstet Gynecol 182 (2000) 553-559
40. Boyd W. A text book of pathology, structure and function in disease (1979), Lea and Febiger, Philadelphia
41. Yamada I., Tsunoda A., Noguchi Y., Komatsuzaki A., and Shibuya H. Tumor volume measurements of acoustic neuromas with three-dimensional constructive interference in steady state and conventional spin-echo MR imaging. Magn Reson Imag 12 (2000) 826-832
42. Quast M.J., Neumeister H., Ezell E.L., and Budelmann B.U. MR microscopy of cobalt-labeled nerve cells and pathways in an invertebrate brain (Sepia officinalis, Cephalopoda). Magn Reson Med 45 (2001) 575-579
43. Willis W.D., Al Chaer E.D., Quast M.J., and Westlund K.N. A visceral pain pathway in the dorsal column of the spinal cord. Proc Natl Acad Sci U S A 96 (1999) 7675-7679
44. Al-Hendy A., and Auersperg N. Applying the herpes simplex virus thymidine kinase/ganciclovir approach to ovarian cancer: an effective in vitro drug-sensitization system. Gynecol Obstet Invest 43 (1997) 268-275
45. Colgan T.J., Pendergast S., and Leblanc M. The histopathology of uterine leiomyomas following treatment with gonadotropin-releasing hormone analogs. Hum Pathol 24 (1994) 1073-1077
46. Salama S., Kamel M., Christman G., Wang H., and Al-Hendy A. Gene therapy of uterine fibroids: adenovirus-mediated herpes simplex virus thymidine kinase/ganciclovir treatment inhibits growth of human and rat leiomyoma cells. Gynecol Obstet Invest 63 (2007) 61-70
47. Burroughs K.D., Fuchs-Young R., Davis B., and Walker C.L. Altered hormonal responsiveness of proliferation and apoptosis during myometrial maturation and the development of uterine leiomyomas in the rat. Biol Reprod 63 (2000) 1322-1330
48. Hassan M.H., Salama S.A., Arafa H.M., Hamada F.M., and Al-Hendy A. Adenovirus-mediated delivery of a dominant negative estrogen receptor gene in uterine leiomyoma cells abrogates estrogen- and progesterone-regulated gene expression. J Clin Endocrinol Metab 92 (2007) 3949-3957
49. Salama S.A., Jamaluddin M., Kumar R., Hassan M.H., and Al-Hendy A. Progesterone regulates catechol-O-methyl transferase gene expression in breast cancer cells: distinct effect of progesterone receptor isoforms. J Steroid Biochem Mol Biol 107 (2007) 253-261
50. Pfaffl M.W. A new mathematical model for relative quantifications in real-time RT-PCR. Nucleic Acids Res 29 (2001) e45
51. Othman E.R., Salama S.A., Ismail N., and Al-Hendy A. Gene therapy of endometriosis: adenovirus mediated expression of dominant negative estrogen receptor induces apoptosis in human endometriotic cells. Fertil Steril 88 (2007) 462-471
52. Sbrana E., Mateo R.I., Xiao S.Y., Popov V.L., Newman P.C., and Tesh R.B. Clinical laboratory, virologic, and pathologic changes in hamsters experimentally infected with pirital virus (Arenaviridae): a rodent model of Lassa fever. Am J Trop Med Hyg 74 (2006) 1096-1102
53. Alvarez R.D., Barnes M.N., Gomez-Navarro J., Wang M., Strong T.V., Arafat W.R., et al. A cancer gene therapy approach utilizing an antierbB-2 single-chain antibody-encoding adenovirus (AD21): a phase I trial. Clin Cancer Res 6 (2000) 3081-3087
54. Schulick A.H., Vassalli G., Dunn P.F., Dong G., Rade J.J., Zamarron C., et al. Established immunity precludes adenovirus-mediated gene transfer in rat carotid arteries: potential for immunosuppression and vector engineering to overcome barriers of immunity. J Clin Invest 99 (1997) 209-219
55. Smith T.A.G., Mehaffey M.G., Kayda D.B., Saunders J.M., Yei S., Trapnell B.C., et al. Adenovirus-mediated expression of therapeutic plasma levels of human factor-IX in mice. Nat Genet 5 (1993) 397-02
56. Harvey B.G., Hackett N.R., El-Sawy T., Rosengart T.K., Hirschowitz E.A., Lieberman M.D., et al. Variability of human systemic humoral immune responses to adenovirus gene transfer vectors administered to different organs. J Virol 73 (1999) 6729-6742
57. Murphy L.J., and Ghahary A. Uterine insulin-like growth factor-1: regulation of expression and its role in estrogen-induced uterine proliferation. Endocr Rev 11 (1990) 443-453
58. Chegini N., Verala J., X. Luo X., Xu J., and Williams R.S. Gene expression profile of leiomyoma and myometrium and the effect of gonadotropin releasing hormone analogue therapy. J Soc Gynecol Invest 10 (2003) 161-171
59. Lazennec G., Alcorn J.L., and Katzenellenbogen B.S. Adenovirus-mediated delivery of a dominant negative estrogen receptor gene abrogates estrogen-stimulated gene expression and breast cancer cell proliferation. Mol Endocrinol 13 (1999) 969-980
60. Dixon D., Flake G.P., Moore A.B., He H., Haseman J.K., Risinger J.I., Lancaster J.M., et al. Cell proliferation and apoptosis in human uterine leiomyomas and myometria. Virchows Arch 441 (2002) 53-62
61. Gao Z., Matsuo H., Satoshi N., Kurachi O., and Maruo T. p53 tumor suppressor protein content in human uterine leiomyomas and its down-regulation by 17B-estradiol. J Clin Endocrinol Metab 87 (2002) 3915-3920
62. Imai A., Takagi A., Horibe S., Takagi H., and Tamaya T. Evidence for tight coupling of gonadotropin-releasing hormone receptor to stimulated fas ligand expression in reproductive tract tumors: possible mechanism for hormonal control of apoptotic cell death. J Clin Endocrinol Metab 83 (1998) 427-431
63. Bargonetti J., and Manfredi J.J. Multiple roles of the tumor suppressor p53. Curr Opin Oncol 14 (2002) 86-91
64. Haupt S., Berger M., Goldberg Z., and Haupt Y. Apoptosis-the p53 network. J Cell Sci 116 (2003) 4077-4085
65. Lane D.P. Cancer-p53, guardian of the genome. Nature 358 6381 (1992) 15-16
66. Nagata S. Apoptosis by death factor. Cell 88 (1997) 355-365
67. Krammer P.H. CD95's deadly mission in the immune system. Nature 407 6805 (2000) 789-795
68. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275 5303 (1997) 1129-1132
69. Slee E.A., Harte M.T., Kluck R.M., Wolf B.B., Casiano C.A., Newmeyer D.D., et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144 (1999) 281-292
70. Van der Meer I.M., Oei H.H., Hofman A., Pols H.A., de Jong F.H., and Witteman J.C. Soluble Fas, a mediator of apoptosis, C-reactive protein, and coronary and extracoronary atherosclerosis-the Rotterdam Coronary Calcification Study. Atherosclerosis 189 (2006) 464-469
71. Chang H.Y., Nishitoh H., Yang X., Ichijo H., and Baltimore D. Activation of apoptosis signal regulating kinase 1 (Ask1) by the adapter protein Daxx. Science 281 5384 (1998) 1860-1863
72. Cecconi F. Apaf1 and the apoptotic machinery. Cell Death Diff 6 (1999) 1087-1098
73. Matsuda K., Yoshida K., Taya Y., Nakamura K., Nakamura Y., and Arakawa H. p53AIP1 regulates the mitochondrial apoptotic pathway. Cancer Res 62 (2002) 2883-2889
74. Chiou S.K., Rao L., and White E. Bcl-2 blocks p53-dependent apoptosis. Mol Cell Biol 14 (1994) 2556-2563
75. Reed J.C., Jurgensmeier J.M., and Matsuyama S. Bcl-2 family proteins and mitochondria. Biochim Biophys Acta 1366 (1998) 127-137
76. Nomura M., Shimizu S., Ito T., Narita M., Matsuda H., and Tsujimoto Y. Apoptotic cytosol facilitates Bax translocation to mitochondria that involves cytosolic factor regulated by Bcl-2. Cancer Res 59 (1999) 5542-5548
77. Wu, Blanck A., Olovsson M., Henriksen R., and Lindblom B. Expression of Bcl-2, Bcl-x, Mcl-1, Bax and Bak in human uterine leiomyomas and myometrium during the menstrual cycle and after menopause. J Steroid Biochem Mol Biol 80 (2002) 77-83
78. Khurana K.K., Singh S.B., Tatum A.H., Schulz V., and Badawy S.Z. Maintenance of increased Bcl-2 expression in uterine leiomyomas after GnRH agonist therapy. J Reprod Med 44 (1999) 487-492
79. Loy C.J., Evelyn S., Lim F.K., Liu M.H., and Yong E.L. Growth dynamics of human leiomyoma cells and inhibitory effects of the peroxisome proliferator-activated receptor-gamma ligand, pioglitazone. Mol Hum Reprod 11 (2005) 561-566
80. Kurki P., Vanderlaan M., Dolbeare F., Gray J., and Tan E.M. Expression of proliferating cell nuclear antigen (PCNA)/cyclin during the cell cycle. Exp Cell Res 166 (1986) 209-219
81. Baldin V., Lukas J., Marcote M.J., Pagano M., and Draetta G. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7 (1993) 812-821
82. Ingman W.V., and Robertson S.A. Defining the actions of transforming growth factor beta in reproduction. Bioessays 24 (2002) 904-1429
83. Ignotz R.A., and Massague J. Transforming growth-factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular-matrix. J Biol Chem 261 (1986) 4337-4529
84. Ignotz R.A., Endo T., and Massague J. Regulation of fibronectin and type-I collagen messenger-RNA levels by transforming growth-factor-beta. J Biol Chem 262 (1987) 6443-6629
85. Hallenbeck P.L., and Stevenson S.C. Targetable gene delivery vectors. Adv Exp Med Biol 465 (2000) 37-46
86. Worgall S., Wolff G., Falck-Pedersen E., and Crystal R.G. Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum Gene Ther 8 (1997) 37-44
87. Roth D.A., McKirnan M.D., Canestrelli I., Gao M.H., Dalton N., Lai N.C., et al. Intracoronary delivery of an adenovirus encoding fibroblast growth factor-4 in myocardial ischemia: effect of serum antibodies and previous exposure to adenovirus. Hum Gene Ther 17 (2006) 230-238
88. Yang Y., Li Q., Ertl H.C., and Wilson J.M. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol 69 (1995) 2004-2015
89. Harvey B.G., Hackett N.R., Ely S., and Crystal R.G. Host responses and persistence of vector genome following intrabronchial administration of an E1 (-) E3 (-) adenovirus gene transfer vector to normal individuals. Mol Ther 3 (2001) 206-215
90. Blake R.E. Leiomyomata uteri: hormonal and molecular determinants of growth. J Natl Med Assoc 99 (2007) 1170-1184
91. Rocconi R.P., Zhu Z.B., Stoff-Khalili M., Rivera A.A., Lu B., Wang M., et al. Treatment of ovarian cancer with a novel dual targeted conditionally replicative adenovirus (CRAd)1. Gynecol Oncol 105 (2007) 113-121
92. Sullivan D.M., Jensen T.G., Taichman L.B., and Csaky K.G. Ornithine-delta-aminotransferase expression and ornithine metabolism in cultured epidermal keratinocytes: toward metabolic sink therapy for gyrate atrophy1. Gene Ther 4 (1997) 1036-1044
93. Hassan M.H., Khatoon N., Curiel D.T., Hamada F.M., Arafa H.M., and Al-Hendy A. Toward gene therapy of uterine fibroids: targeting modified adenovirus to human leiomyoma cells. Hum Reprod 23 (2008) 514-524