Ovarian Cancer Animal Models for Preclinical Studies and Development of Ovarian Cancer Drugs
Abstract
Treatment for ovarian carcinoma is still far from optimal, animal models are still needed to study human epithelial ovarian cancer. Animal models of ovarian cancer are very important for understanding the pathogenesis of the disease and for testing new treatment strategies. Ovarian carcinogenesis models in mice have been modified and repaired to produce preneoplastic lesions and neoplastic ovaries that are pathogens resembling human ovarian cancer. Although spontaneous ovarian tumors in mice have been reported, some of the shortcomings of existing studies preclude their use as animal models of ovarian cancer. Because of this, many efforts have been made to develop animal models that are relevant for ovarian cancer. Experimental animal models are developed accurately to represent cellular and molecular changes associated with the initiation and development of human ovarian cancer. Accurate experimental models have significant potential in facilitating the development of better methods for early detection and treatment of ovarian cancer. Several animal models of ovarian cancer have been reported, including manipulation of various reproductive factors or exposure to carcinogens. The latest advance in ovarian cancer modeling is using genetically engineered mice.
References
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22. Schumacher U, Adam E, Horny HP, Dietl J. Transplantation of a human ovarian cystadenocarcinoma into severe combined immunodeficient (SCID) mice—formation of metastases without significant alteration of the tumour cell phenotype. International journal of experimental pathology. 1996;77(5):219-227.
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27. Cannistra SA, Matulonis UA, Penson RT, et al. Phase II study of bevacizumab in patients with platinum-resistant ovarian cancer or peritoneal serous cancer. Journal of Clinical Oncology. 2007;25(33):5180-5186.
28. Hu L, Hofmann J, Zaloudek C, Ferrara N, Hamilton T, Jaffe RB. Vascular endothelial growth factor immunoneutralization plus Paclitaxel markedly reduces tumor burden and ascites in athymic mouse model of ovarian cancer. The American journal of pathology. 2002;161(5):1917-1924.
29. Weroha SJ, Becker MA, Enderica-Gonzalez S, et al. Tumorgrafts as in vivo surrogates for women with ovarian cancer. Clinical Cancer Research. 2014;20(5):1288-1297.
30. Dobbin ZC, Katre AA, Steg AD, et al. Using heterogeneity of the patient-derived xenograft model to identify the chemoresistant population in ovarian cancer. Oncotarget. 2014;5(18):8750.
31. Ricci F, Bizzaro F, Cesca M, et al. Patient-derived ovarian tumor xenografts recapitulate human clinicopathology and genetic alterations. Cancer research. 2014;74(23):6980-6990.
32. Elkas JC, Baldwin RL, Pegram M, Tseng Y, Slamon D, Karlan BY. A human ovarian carcinoma murine xenograft model useful for preclinical trials. Gynecologic oncology. 2002;87(2):200-206.
33. Khabele D, Fadare O, Liu AY, et al. An orthotopic model of platinum-sensitive high grade serous fallopian tube carcinoma. International journal of clinical and experimental pathology. 2012;5(1):37.
34. Hidalgo M, Bruckheimer E, Rajeshkumar N, et al. A pilot clinical study of treatment guided by personalized tumorgrafts in patients with advanced cancer. Molecular cancer therapeutics. 2011;10(8):1311-1316.
35. Scott CL, Mackay HJ, Haluska Jr P. Patient-derived xenograft models in gynecological malignancies. Paper presented at: American Society of Clinical Oncology educational book/ASCO. American Society of Clinical Oncology. Meeting2014.
36. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nature medicine. 2004;10(9):942.
37. Ito R, Takahashi T, Katano I, Ito M. Current advances in humanized mouse models. Cellular & molecular immunology. 2012;9(3):208.
38. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565-1570.
39. Cooper TK, Gabrielson KL. Spontaneous lesions in the reproductive tract and mammary gland of female non‐human primates. Birth Defects Research Part B: Developmental and Reproductive Toxicology. 2007;80(2):149-170.
40. Barua A, Bitterman P, Abramowicz JS, et al. Histopathology of ovarian tumors in laying hens: a preclinical model of human ovarian cancer. International Journal of Gynecologic Cancer. 2009;19(4):531-539-531-539.
41. Tillmann T, Kamino K, Mohr U. Incidence and spectrum of spontaneous neoplasms in male and female CBA/J mice. Experimental and Toxicologic Pathology. 2000;52(3):221-225.
42. Walsh KM, Poteracki J. Spontaneous neoplasms in control Wistar rats. Fundamental and applied toxicology. 1994;22(1):65-72.
43. Gregson R, Lewis D, Abbott D. Spontaneous ovarian neoplasms of the laboratory rat. Veterinary pathology. 1984;21(3):292-299.
44. Krarup T. Oocyte destruction and ovarian tumorigenesis after direct application of a chemical carcinogen (9: 10‐dimethyl‐1: 2‐benzanthrene) to the mouse ovary. International journal of cancer. 1969;4(1):61-75.
45. Stewart SL, Querec TD, Ochman AR, et al. Characterization of a carcinogenesis rat model of ovarian preneoplasia and neoplasia. Cancer research. 2004;64(22):8177-8183.
46. Gertig DM, Hunter DJ, Cramer DW, et al. Prospective study of talc use and ovarian cancer. Journal of the National Cancer Institute. 2000;92(3):249-252.
47. Sims DE, Singh A, Donald A, Jarrell J, Villeneuve DC. Alteration of primate ovary surface epithelium by exposure to hexachlorobenzene: a quantitative study. Histology and histopathology. 1991;6(4):525-529.
48. Maronpot RR. Ovarian toxicity and carcinogenicity in eight recent National Toxicology Program studies. Environmental health perspectives. 1987;73:125-130.
49. Nishida T, Sugiyama T, Kataoka A, Ushijima K, Yakushiji M. Histologic characterization of rat ovarian carcinoma induced by intraovarian insertion of a 7, 12‐dimethylbenz [a] anthracene‐coated suture: Common epithelial tumors of the ovary in rats? Cancer: Interdisciplinary International Journal of the American Cancer Society. 1998;83(5):965-970.
50. Tanaka T, Kohno H, Suzuki R, Sugie S. Lack of modifying effects of an estrogenic compound atrazine on 7, 12-dimethylbenz (a) anthracene-induced ovarian carcinogenesis in rats. Cancer letters. 2004;210(2):129-137.
51. Hoyer PB, Davis J, Bedrnicek J, et al. Ovarian neoplasm development by 7, 12-dimethylbenz [a] anthracene (DMBA) in a chemically-induced rat model of ovarian failure. Gynecologic oncology. 2009;112(3):610-615.
52. Crist KA, Zhang Z, You M, et al. Characterization of rat ovarian adenocarcinomas developed in response to direct instillation of 7, 12-dimethylbenz [a] anthracene (DMBA) coated suture. Carcinogenesis. 2005;26(5):951-957.
53. Tanaka T, Kohno H, Tanino M, Yanaida Y. Inhibitory effects of estrogenic compounds, 4-nonylphenol and genistein, on 7, 12-dimethylbenz [a] anthracene-induced ovarian carcinogenesis in rats. Ecotoxicology and environmental safety. 2002;52(1):38-45.
54. Tunca JC, Ertürk E, Ertürk E, Bryan GT. Chemical induction of ovarian tumors in rats. Gynecologic oncology. 1985;21(1):54-64.
55. Hilfrich J. Comparative morphological studies on the carcinogenic effect of 7, 12-dimethylbenz (A) anthracene (DMBA) in normal or intrasplenic ovarian tissue of C3H mice. British journal of cancer. 1975;32(5):588.
56. Huang Y, Jiang W, Wang Y, Zheng Y, Cong Q, Xu C. Enhanced efficacy and specificity of epithelial ovarian carcinogenesis by embedding a DMBA-coated cloth strip in the ovary of rat. Journal of ovarian research. 2012;5(1):21.
57. McDermott S, Ranheim E, Leatherberry V, Khwaja S, Klos K, Alexander C. Juvenile syndecan-1 null mice are protected from carcinogen-induced tumor development. Oncogene. 2007;26(10):1407.
58. Wang Y, Zhang Z, Lu Y, et al. Enhanced susceptibility to chemical induction of ovarian tumors in mice with a germ line p53 mutation. Molecular Cancer Research. 2008;6(1):99-109.
59. Chien JR, Aletti G, Bell DA, Keeney GL, Shridhar V, Hartmann LC. Molecular pathogenesis and therapeutic targets in epithelial ovarian cancer. Journal of cellular biochemistry. 2007;102(5):1117-1129.
60. Ness RB, Cottreau C. Possible role of ovarian epithelial inflammation in ovarian cancer. Journal of the National Cancer Institute. 1999;91(17):1459-1467.
61. Tsuta K, Shikata N, Kominami S, Tsubura A. Mechanisms of Adrenal Damage Induced by 7, 12-Dimethylbenz (α) anthrancene in Female Sprague-Dawley Rats. Experimental and molecular pathology. 2001;70(2):162-172.
62. Enomoto T, Weghorst C, Inoue M, Tanizawa O, Rice J. K-ras activation occurs frequently in mucinous adenocarcinomas and rarely in other common epithelial tumors of the human ovary. The American journal of pathology. 1991;139(4):777.
2. Rescigno P, Cerillo I, Ruocco R, Condello C, De Placido S, Pensabene M. New hypothesis on pathogenesis of ovarian cancer lead to future tailored approaches. BioMed research international. 2013;2013.
3. Piek JM, Van Diest PJ, Verheijen RH. Ovarian carcinogenesis: an alternative hypothesis. In: Ovarian Cancer. Springer; 2008:79-87.
4. Yang-Hartwich Y, Gurrea-Soteras M, Sumi N, et al. Ovulation and extra-ovarian origin of ovarian cancer. Scientific reports. 2014;4:6116.
5. Bowtell DD. The genesis and evolution of high-grade serous ovarian cancer. Nature Reviews Cancer. 2010;10(11):803.
6. Koshiyama M, Matsumura N, Konishi I. Recent concepts of ovarian carcinogenesis: type I and type II. BioMed research international. 2014;2014.
7. Ahmed N, Stenvers K. Getting to know ovarian cancer ascites: opportunities for targeted therapy-based translational research. Frontiers in oncology. 2013;3:256.
8. Puls LE, Duniho T, Hunter IV JE, Kryscio R, Blackhurst D, Gallion H. The prognostic implication of ascites in advanced-stage ovarian cancer. Gynecologic oncology. 1996;61(1):109-112.
9. Lengyel E. Ovarian cancer development and metastasis. The American journal of pathology. 2010;177(3):1053-1064.
10. Connolly DC. Animal models of ovarian cancer. In: Ovarian Cancer. Springer; 2009:353-391.
11. Ruggeri BA, Camp F, Miknyoczki S. Animal models of disease: pre-clinical animal models of cancer and their applications and utility in drug discovery. Biochemical pharmacology. 2014;87(1):150-161.
12. Vanderhyden BC, Shaw TJ, Ethier J-F. Animal models of ovarian cancer. Reproductive Biology and Endocrinology. 2003;1(1):67.
13. Perets R, Wyant GA, Muto KW, et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca; Tp53; Pten models. Cancer cell. 2013;24(6):751-765.
14. Sherman‐Baust CA, Kuhn E, Valle BL, et al. A genetically engineered ovarian cancer mouse model based on fallopian tube transformation mimics human high‐grade serous carcinoma development. The Journal of pathology. 2014;233(3):228-237.
15. Kim J, Coffey DM, Creighton CJ, Yu Z, Hawkins SM, Matzuk MM. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proceedings of the National Academy of Sciences. 2012;109(10):3921-3926.
16. Kuhn E, Tisato V, Rimondi E, Secchiero P. Current preclinical models of ovarian cancer. J Carcinog Mutagen.
2015;6(2):220.
17. Shaw TJ, Senterman MK, Dawson K, Crane CA, Vanderhyden BC. Characterization of intraperitoneal, orthotopic, and metastatic xenograft models of human ovarian cancer. Molecular therapy. 2004;10(6):1032-1042.
18. Connolly DC, Hensley HH. Xenograft and Transgenic Mouse Models of Epithelial Ovarian Cancer and Non‐Invasive Imaging Modalities to Monitor Ovarian Tumor Growth In Situ: Applications in Evaluating Novel Therapeutic Agents. Current protocols in pharmacology. 2009;45(1):14.12. 11-14.12. 26.
19. Kiguchi K, Kubota T, Aoki D, et al. A patient-like orthotopic implantation nude mouse model of highly metastatic human ovarian cancer. Clinical & experimental metastasis. 1998;16(8):751-756.
20. XINYU F, Robert M. Human ovarian carcinoma metastatic models constructed in nude mice by orthotopic transplantation of histologically-intact patient specimens. Anticancer research. 1993;3:283-286.
21. Verschraegen CF, Hu W, Du Y, et al. Establishment and characterization of cancer cell cultures and xenografts derived from primary or metastatic Mullerian cancers. Clinical cancer research. 2003;9(2):845-852.
22. Schumacher U, Adam E, Horny HP, Dietl J. Transplantation of a human ovarian cystadenocarcinoma into severe combined immunodeficient (SCID) mice—formation of metastases without significant alteration of the tumour cell phenotype. International journal of experimental pathology. 1996;77(5):219-227.
23. Domcke S, Sinha R, Levine DA, Sander C, Schultz N. Evaluating cell lines as tumour models by comparison of genomic profiles. Nature communications. 2013;4:2126.
24. Sabbatini P, Harter P, Scambia G, et al. Abagovomab as maintenance therapy in patients with epithelial ovarian cancer: a phase III trial of the AGO OVAR, COGI, GINECO, and GEICO—the MIMOSA study. Journal of clinical oncology. 2013;31(12):1554.
25. Hu L, Hofmann J, Holash J, Yancopoulos GD, Sood AK, Jaffe RB. Vascular endothelial growth factor trap combined with paclitaxel strikingly inhibits tumor and ascites, prolonging survival in a human ovarian cancer model. Clinical Cancer Research. 2005;11(19):6966-6971.
26. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434(7035):917.
27. Cannistra SA, Matulonis UA, Penson RT, et al. Phase II study of bevacizumab in patients with platinum-resistant ovarian cancer or peritoneal serous cancer. Journal of Clinical Oncology. 2007;25(33):5180-5186.
28. Hu L, Hofmann J, Zaloudek C, Ferrara N, Hamilton T, Jaffe RB. Vascular endothelial growth factor immunoneutralization plus Paclitaxel markedly reduces tumor burden and ascites in athymic mouse model of ovarian cancer. The American journal of pathology. 2002;161(5):1917-1924.
29. Weroha SJ, Becker MA, Enderica-Gonzalez S, et al. Tumorgrafts as in vivo surrogates for women with ovarian cancer. Clinical Cancer Research. 2014;20(5):1288-1297.
30. Dobbin ZC, Katre AA, Steg AD, et al. Using heterogeneity of the patient-derived xenograft model to identify the chemoresistant population in ovarian cancer. Oncotarget. 2014;5(18):8750.
31. Ricci F, Bizzaro F, Cesca M, et al. Patient-derived ovarian tumor xenografts recapitulate human clinicopathology and genetic alterations. Cancer research. 2014;74(23):6980-6990.
32. Elkas JC, Baldwin RL, Pegram M, Tseng Y, Slamon D, Karlan BY. A human ovarian carcinoma murine xenograft model useful for preclinical trials. Gynecologic oncology. 2002;87(2):200-206.
33. Khabele D, Fadare O, Liu AY, et al. An orthotopic model of platinum-sensitive high grade serous fallopian tube carcinoma. International journal of clinical and experimental pathology. 2012;5(1):37.
34. Hidalgo M, Bruckheimer E, Rajeshkumar N, et al. A pilot clinical study of treatment guided by personalized tumorgrafts in patients with advanced cancer. Molecular cancer therapeutics. 2011;10(8):1311-1316.
35. Scott CL, Mackay HJ, Haluska Jr P. Patient-derived xenograft models in gynecological malignancies. Paper presented at: American Society of Clinical Oncology educational book/ASCO. American Society of Clinical Oncology. Meeting2014.
36. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nature medicine. 2004;10(9):942.
37. Ito R, Takahashi T, Katano I, Ito M. Current advances in humanized mouse models. Cellular & molecular immunology. 2012;9(3):208.
38. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565-1570.
39. Cooper TK, Gabrielson KL. Spontaneous lesions in the reproductive tract and mammary gland of female non‐human primates. Birth Defects Research Part B: Developmental and Reproductive Toxicology. 2007;80(2):149-170.
40. Barua A, Bitterman P, Abramowicz JS, et al. Histopathology of ovarian tumors in laying hens: a preclinical model of human ovarian cancer. International Journal of Gynecologic Cancer. 2009;19(4):531-539-531-539.
41. Tillmann T, Kamino K, Mohr U. Incidence and spectrum of spontaneous neoplasms in male and female CBA/J mice. Experimental and Toxicologic Pathology. 2000;52(3):221-225.
42. Walsh KM, Poteracki J. Spontaneous neoplasms in control Wistar rats. Fundamental and applied toxicology. 1994;22(1):65-72.
43. Gregson R, Lewis D, Abbott D. Spontaneous ovarian neoplasms of the laboratory rat. Veterinary pathology. 1984;21(3):292-299.
44. Krarup T. Oocyte destruction and ovarian tumorigenesis after direct application of a chemical carcinogen (9: 10‐dimethyl‐1: 2‐benzanthrene) to the mouse ovary. International journal of cancer. 1969;4(1):61-75.
45. Stewart SL, Querec TD, Ochman AR, et al. Characterization of a carcinogenesis rat model of ovarian preneoplasia and neoplasia. Cancer research. 2004;64(22):8177-8183.
46. Gertig DM, Hunter DJ, Cramer DW, et al. Prospective study of talc use and ovarian cancer. Journal of the National Cancer Institute. 2000;92(3):249-252.
47. Sims DE, Singh A, Donald A, Jarrell J, Villeneuve DC. Alteration of primate ovary surface epithelium by exposure to hexachlorobenzene: a quantitative study. Histology and histopathology. 1991;6(4):525-529.
48. Maronpot RR. Ovarian toxicity and carcinogenicity in eight recent National Toxicology Program studies. Environmental health perspectives. 1987;73:125-130.
49. Nishida T, Sugiyama T, Kataoka A, Ushijima K, Yakushiji M. Histologic characterization of rat ovarian carcinoma induced by intraovarian insertion of a 7, 12‐dimethylbenz [a] anthracene‐coated suture: Common epithelial tumors of the ovary in rats? Cancer: Interdisciplinary International Journal of the American Cancer Society. 1998;83(5):965-970.
50. Tanaka T, Kohno H, Suzuki R, Sugie S. Lack of modifying effects of an estrogenic compound atrazine on 7, 12-dimethylbenz (a) anthracene-induced ovarian carcinogenesis in rats. Cancer letters. 2004;210(2):129-137.
51. Hoyer PB, Davis J, Bedrnicek J, et al. Ovarian neoplasm development by 7, 12-dimethylbenz [a] anthracene (DMBA) in a chemically-induced rat model of ovarian failure. Gynecologic oncology. 2009;112(3):610-615.
52. Crist KA, Zhang Z, You M, et al. Characterization of rat ovarian adenocarcinomas developed in response to direct instillation of 7, 12-dimethylbenz [a] anthracene (DMBA) coated suture. Carcinogenesis. 2005;26(5):951-957.
53. Tanaka T, Kohno H, Tanino M, Yanaida Y. Inhibitory effects of estrogenic compounds, 4-nonylphenol and genistein, on 7, 12-dimethylbenz [a] anthracene-induced ovarian carcinogenesis in rats. Ecotoxicology and environmental safety. 2002;52(1):38-45.
54. Tunca JC, Ertürk E, Ertürk E, Bryan GT. Chemical induction of ovarian tumors in rats. Gynecologic oncology. 1985;21(1):54-64.
55. Hilfrich J. Comparative morphological studies on the carcinogenic effect of 7, 12-dimethylbenz (A) anthracene (DMBA) in normal or intrasplenic ovarian tissue of C3H mice. British journal of cancer. 1975;32(5):588.
56. Huang Y, Jiang W, Wang Y, Zheng Y, Cong Q, Xu C. Enhanced efficacy and specificity of epithelial ovarian carcinogenesis by embedding a DMBA-coated cloth strip in the ovary of rat. Journal of ovarian research. 2012;5(1):21.
57. McDermott S, Ranheim E, Leatherberry V, Khwaja S, Klos K, Alexander C. Juvenile syndecan-1 null mice are protected from carcinogen-induced tumor development. Oncogene. 2007;26(10):1407.
58. Wang Y, Zhang Z, Lu Y, et al. Enhanced susceptibility to chemical induction of ovarian tumors in mice with a germ line p53 mutation. Molecular Cancer Research. 2008;6(1):99-109.
59. Chien JR, Aletti G, Bell DA, Keeney GL, Shridhar V, Hartmann LC. Molecular pathogenesis and therapeutic targets in epithelial ovarian cancer. Journal of cellular biochemistry. 2007;102(5):1117-1129.
60. Ness RB, Cottreau C. Possible role of ovarian epithelial inflammation in ovarian cancer. Journal of the National Cancer Institute. 1999;91(17):1459-1467.
61. Tsuta K, Shikata N, Kominami S, Tsubura A. Mechanisms of Adrenal Damage Induced by 7, 12-Dimethylbenz (α) anthrancene in Female Sprague-Dawley Rats. Experimental and molecular pathology. 2001;70(2):162-172.
62. Enomoto T, Weghorst C, Inoue M, Tanizawa O, Rice J. K-ras activation occurs frequently in mucinous adenocarcinomas and rarely in other common epithelial tumors of the human ovary. The American journal of pathology. 1991;139(4):777.
Published
2019-10-29
How to Cite
DWI SANDHIUTAMI, Ni Made et al.
Ovarian Cancer Animal Models for Preclinical Studies and Development of Ovarian Cancer Drugs.
JURNAL ILMU KEFARMASIAN INDONESIA, [S.l.], v. 17, n. 2, p. 139-149, oct. 2019.
ISSN 2614-6495.
Available at: <http://jifi.farmasi.univpancasila.ac.id/index.php/jifi/article/view/734>. Date accessed: 23 dec. 2024.
doi: https://doi.org/10.35814/jifi.v17i2.734.
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