In vivo modeling of metastatic human high-grade serous ovarian cancer in mice


Autoři: Olga Kim aff001;  Eun Young Park aff001;  David L. Klinkebiel aff002;  Svetlana D. Pack aff003;  Yong-Hyun Shin aff001;  Zied Abdullaev aff003;  Robert E. Emerson aff004;  Donna M. Coffey aff005;  Sun Young Kwon aff006;  Chad J. Creighton aff007;  Sanghoon Kwon aff008;  Edmund C. Chang aff009;  Theodore Chiang aff009;  Alexander N. Yatsenko aff010;  Jeremy Chien aff011;  Dong-Joo Cheon aff012;  Yang Yang-Hartwich aff013;  Harikrishna Nakshatri aff014;  Kenneth P. Nephew aff015;  Richard R. Behringer aff016;  Facundo M. Fernández aff017;  Chi-Heum Cho aff018;  Barbara Vanderhyden aff019;  Ronny Drapkin aff020;  Robert C. Bast, Jr aff021;  Kathy D. Miller aff022;  Adam R. Karpf aff023;  Jaeyeon Kim aff001
Působiště autorů: Department of Biochemistry and Molecular Biology, Indiana University Melvin and Bren Simon Comprehensive Cancer Center, Indiana University School of Medicine, Indianapolis, Indiana, United States of America aff001;  Department of Biochemistry and Molecular Biology, Fred & Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, Nebraska, United States of America aff002;  Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America aff003;  Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, Indiana, United States of America aff004;  Department of Pathology and Genomic Medicine, Houston Methodist and Weill Cornell Medical College, Houston, Texas, United States of America aff005;  Department of Pathology, School of Medicine, Keimyung University, Daegu, Republic of Korea aff006;  Department of Medicine, Baylor College of Medicine, Houston, Texas, United States of America aff007;  Research and Development Center, Bioway Inc, Seoul, Republic of Korea aff008;  Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas, United States of America aff009;  Department of Obstetrics, Gynecology & Reproductive Sciences, Magee-Womens Research Institute, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America aff010;  Department of Biochemistry and Molecular Medicine, University of California, Davis, Sacramento, California, United States of America aff011;  Department of Regenerative and Cancer Cell Biology, Albany Medical College, Albany, NY, United States of America aff012;  Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, Connecticut, United States of America aff013;  Department of Surgery, Indiana University Melvin and Bren Simon Comprehensive Cancer Center, Indiana University School of Medicine, Indianapolis, Indiana, United States of America aff014;  Medical Sciences Program, Indiana University Melvin and Bren Simon Comprehensive Cancer Center, Indiana University School of Medicine, Bloomington, Indiana, United States of America aff015;  Departments of Genetics, University of Texas MD Anderson Cancer Center, Houston, Texas, United States of America aff016;  School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, Georgia, United States of America aff017;  Department of Obstetrics and Gynecology, School of Medicine, Keimyung University, Daegu, Republic of Korea aff018;  Department of Cellular and Molecular Medicine, University of Ottawa, and Ottawa Hospital Research Institute, Ottawa, Ontario, Canada aff019;  Penn Ovarian Cancer Research Center, Department of Obstetrics and Gynecology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America aff020;  Department of Experimental Therapeutics, University of Texas MD Anderson Cancer Center, Houston, Texas, United States of America aff021;  Department of Medicine, Indiana University Melvin and Bren Simon Comprehensive Cancer Center, Indiana University School of Medicine Indianapolis, Indiana, United States of America aff022;  Eppley Institute for Cancer Research, Fred & Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, Nebraska, United States of America aff023
Vyšlo v časopise: In vivo modeling of metastatic human high-grade serous ovarian cancer in mice. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008808
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008808

Souhrn

Metastasis is responsible for 90% of human cancer mortality, yet it remains a challenge to model human cancer metastasis in vivo. Here we describe mouse models of high-grade serous ovarian cancer, also known as high-grade serous carcinoma (HGSC), the most common and deadliest human ovarian cancer type. Mice genetically engineered to harbor Dicer1 and Pten inactivation and mutant p53 robustly replicate the peritoneal metastases of human HGSC with complete penetrance. Arising from the fallopian tube, tumors spread to the ovary and metastasize throughout the pelvic and peritoneal cavities, invariably inducing hemorrhagic ascites. Widespread and abundant peritoneal metastases ultimately cause mouse deaths (100%). Besides the phenotypic and histopathological similarities, mouse HGSCs also display marked chromosomal instability, impaired DNA repair, and chemosensitivity. Faithfully recapitulating the clinical metastases as well as molecular and genomic features of human HGSC, this murine model will be valuable for elucidating the mechanisms underlying the development and progression of metastatic ovarian cancer and also for evaluating potential therapies.

Klíčová slova:

Animal models of disease – Chromosomes – Mammalian genomics – Metastasis – Metastatic tumors – Mouse models – Ovarian cancer – Fallopian tubes


Zdroje

1. Bast RC Jr., Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation. Nature reviews Cancer. 2009;9(6):415–28. doi: 10.1038/nrc2644 19461667.

2. Cho KR, Shih Ie M. Ovarian cancer. Annu Rev Pathol. 2009;4:287–313. doi: 10.1146/annurev.pathol.4.110807.092246 18842102.

3. Bowtell DD, Bohm S, Ahmed AA, Aspuria PJ, Bast RC Jr., Beral V, et al. Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer. Nature reviews Cancer. 2015;15(11):668–79. doi: 10.1038/nrc4019 26493647; PubMed Central PMCID: PMC4892184.

4. Gurung A, Hung T, Morin J, Gilks CB. Molecular abnormalities in ovarian carcinoma: clinical, morphological and therapeutic correlates. Histopathology. 2013;62(1):59–70. doi: 10.1111/his.12033 23240670.

5. Seidman JD, Horkayne-Szakaly I, Haiba M, Boice CR, Kurman RJ, Ronnett BM. The histologic type and stage distribution of ovarian carcinomas of surface epithelial origin. Int J Gynecol Pathol. 2004;23(1):41–4. doi: 10.1097/01.pgp.0000101080.35393.16 14668549.

6. Peres LC, Cushing-Haugen KL, Kobel M, Harris HR, Berchuck A, Rossing MA, et al. Invasive Epithelial Ovarian Cancer Survival by Histotype and Disease Stage. Journal of the National Cancer Institute. 2019;111(1):60–8. Epub 2018/05/03. doi: 10.1093/jnci/djy071 29718305; PubMed Central PMCID: PMC6335112.

7. Kim J, Park EY, Kim O, Schilder JM, Coffey DM, Cho CH, et al. Cell Origins of High-Grade Serous Ovarian Cancer. Cancers. 2018;10(11). Epub 2018/11/15. doi: 10.3390/cancers10110433 30424539; PubMed Central PMCID: PMC6267333.

8. Torre LA, Trabert B, DeSantis CE, Miller KD, Samimi G, Runowicz CD, et al. Ovarian cancer statistics, 2018. CA: a cancer journal for clinicians. 2018. Epub 2018/05/29. doi: 10.3322/caac.21456 29809280.

9. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol. 2010;177(3):1053–64. doi: 10.2353/ajpath.2010.100105 20651229.

10. Yap TA, Carden CP, Kaye SB. Beyond chemotherapy: targeted therapies in ovarian cancer. Nature reviews Cancer. 2009;9(3):167–81. doi: 10.1038/nrc2583 19238149.

11. Seidman JD, Zhao P, Yemelyanova A. "Primary peritoneal" high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer. Gynecologic oncology. 2011;120(3):470–3. doi: 10.1016/j.ygyno.2010.11.020 21159368.

12. Stuckelberger S, Drapkin R. Precious GEMMs: emergence of faithful models for ovarian cancer research. J Pathol. 2018;245(2):129–31. Epub 2018/03/02. doi: 10.1002/path.5065 29493783.

13. 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 of the United States of America. 2012;109(10):3921–6. doi: 10.1073/pnas.1117135109 22331912.

14. TCGA. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474(7353):609–15. doi: 10.1038/nature10166 21720365.

15. Ahmed AA, Etemadmoghadam D, Temple J, Lynch AG, Riad M, Sharma R, et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol. 2010;221(1):49–56. doi: 10.1002/path.2696 20229506.

16. Brachova P, Thiel KW, Leslie KK. The consequence of oncomorphic TP53 mutations in ovarian cancer. International journal of molecular sciences. 2013;14(9):19257–75. Epub 2013/09/26. doi: 10.3390/ijms140919257 24065105; PubMed Central PMCID: PMC3794832.

17. Levine AJ, Oren M. The first 30 years of p53: growing ever more complex. Nature reviews Cancer. 2009;9(10):749–58. Epub 2009/09/25. doi: 10.1038/nrc2723 19776744; PubMed Central PMCID: PMC2771725.

18. Freed-Pastor WA, Prives C. Mutant p53: one name, many proteins. Genes Dev. 2012;26(12):1268–86. Epub 2012/06/21. doi: 10.1101/gad.190678.112 22713868; PubMed Central PMCID: PMC3387655.

19. Rivlin N, Brosh R, Oren M, Rotter V. Mutations in the p53 Tumor Suppressor Gene: Important Milestones at the Various Steps of Tumorigenesis. Genes & cancer. 2011;2(4):466–74. Epub 2011/07/23. doi: 10.1177/1947601911408889 21779514; PubMed Central PMCID: PMC3135636.

20. Bowtell DD. The genesis and evolution of high-grade serous ovarian cancer. Nature reviews Cancer. 2010;10(11):803–8. Epub 2010/10/15. doi: 10.1038/nrc2946 20944665.

21. Crum CP, Drapkin R, Miron A, Ince TA, Muto M, Kindelberger DW, et al. The distal fallopian tube: a new model for pelvic serous carcinogenesis. Curr Opin Obstet Gynecol. 2007;19(1):3–9. doi: 10.1097/GCO.0b013e328011a21f 17218844.

22. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, Saleemuddin A, et al. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol. 2007;211(1):26–35. doi: 10.1002/path.2091 17117391.

23. Kurman RJ, Shih Ie M. The Dualistic Model of Ovarian Carcinogenesis: Revisited, Revised, and Expanded. Am J Pathol. 2016;186(4):733–47. Epub 2016/03/26. doi: 10.1016/j.ajpath.2015.11.011 27012190; PubMed Central PMCID: PMC5808151.

24. Varley JM. Germline TP53 mutations and Li-Fraumeni syndrome. Hum Mutat. 2003;21(3):313–20. doi: 10.1002/humu.10185 12619118.

25. Nichols KE, Malkin D, Garber JE, Fraumeni JF Jr., Li FP. Germ-line p53 mutations predispose to a wide spectrum of early-onset cancers. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2001;10(2):83–7. 11219776.

26. Birch JM, Alston RD, McNally RJ, Evans DG, Kelsey AM, Harris M, et al. Relative frequency and morphology of cancers in carriers of germline TP53 mutations. Oncogene. 2001;20(34):4621–8. doi: 10.1038/sj.onc.1204621 11498785.

27. Buller RE, Skilling JS, Kaliszewski S, Niemann T, Anderson B. Absence of significant germ line p53 mutations in ovarian cancer patients. Gynecologic oncology. 1995;58(3):368–74. doi: 10.1006/gyno.1995.1244 7672703.

28. Donehower LA. The p53-deficient mouse: a model for basic and applied cancer studies. Semin Cancer Biol. 1996;7(5):269–78. doi: 10.1006/scbi.1996.0035 9110404.

29. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT, et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell. 2004;119(6):847–60. doi: 10.1016/j.cell.2004.11.004 15607980.

30. Clark-Knowles KV, Senterman MK, Collins O, Vanderhyden BC. Conditional inactivation of Brca1, p53 and Rb in mouse ovaries results in the development of leiomyosarcomas. PloS one. 2009;4(12):e8534. doi: 10.1371/journal.pone.0008534 20046869.

31. Kim J, Coffey DM, Ma L, Matzuk MM. The ovary is an alternative site of origin for high-grade serous ovarian cancer in mice. Endocrinology. 2015;156(6):1975–81. doi: 10.1210/en.2014-1977 25815421.

32. Pradeep S, Kim SW, Wu SY, Nishimura M, Chaluvally-Raghavan P, Miyake T, et al. Hematogenous metastasis of ovarian cancer: rethinking mode of spread. Cancer cell. 2014;26(1):77–91. Epub 2014/07/16. doi: 10.1016/j.ccr.2014.05.002 25026212; PubMed Central PMCID: PMC4100212.

33. Monk BJ, Minion LE, Coleman RL. Anti-angiogenic agents in ovarian cancer: past, present, and future. Annals of oncology: official journal of the European Society for Medical Oncology. 2016;27 Suppl 1:i33–i9. Epub 2016/05/04. doi: 10.1093/annonc/mdw093 27141068; PubMed Central PMCID: PMC6283356.

34. Merritt WM, Lin YG, Han LY, Kamat AA, Spannuth WA, Schmandt R, et al. Dicer, Drosha, and outcomes in patients with ovarian cancer. The New England journal of medicine. 2008;359(25):2641–50. doi: 10.1056/NEJMoa0803785 19092150.

35. Ravi A, Gurtan AM, Kumar MS, Bhutkar A, Chin C, Lu V, et al. Proliferation and tumorigenesis of a murine sarcoma cell line in the absence of DICER1. Cancer cell. 2012;21(6):848–55. doi: 10.1016/j.ccr.2012.04.037 22698408.

36. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74. Epub 2011/03/08. doi: 10.1016/j.cell.2011.02.013 21376230.

37. Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nature genetics. 2006;38(9):1043–8. Epub 2006/08/22. doi: 10.1038/ng1861 16921376.

38. Albertson DG, Collins C, McCormick F, Gray JW. Chromosome aberrations in solid tumors. Nature genetics. 2003;34(4):369–76. Epub 2003/08/19. doi: 10.1038/ng1215 12923544.

39. Frohling S, Dohner H. Chromosomal abnormalities in cancer. The New England journal of medicine. 2008;359(7):722–34. Epub 2008/08/16. doi: 10.1056/NEJMra0803109 18703475.

40. Kobayashi Y, Mizuhara H, Ohara T, Kondo H, Sato S, Kiguchi K, et al. Establishment and characterization of a cell line derived from a human serous surface papillary carcinoma of the ovary. Hum Cell. 2006;19(4):133–7. doi: 10.1111/j.1749-0774.2006.00021.x 17257376.

41. Oostra AB, Nieuwint AW, Joenje H, de Winter JP. Diagnosis of fanconi anemia: chromosomal breakage analysis. Anemia. 2012;2012:238731. Epub 2012/06/14. doi: 10.1155/2012/238731 22693659; PubMed Central PMCID: PMC3368163.

42. King SM, Quartuccio SM, Vanderhyden BC, Burdette JE. Early transformative changes in normal ovarian surface epithelium induced by oxidative stress require Akt upregulation, DNA damage and epithelial-stromal interaction. Carcinogenesis. 2013;34(5):1125–33. Epub 2013/01/10. doi: 10.1093/carcin/bgt003 23299406.

43. Elias KM, Emori MM, Westerling T, Long H, Budina-Kolomets A, Li F, et al. Epigenetic remodeling regulates transcriptional changes between ovarian cancer and benign precursors. JCI insight. 2016;1(13). Epub 2016/09/13. doi: 10.1172/jci.insight.87988 27617304; PubMed Central PMCID: PMC5017158.

44. Karst AM, Drapkin R. Primary culture and immortalization of human fallopian tube secretory epithelial cells. Nature protocols. 2012;7(9):1755–64. Epub 2012/09/01. doi: 10.1038/nprot.2012.097 22936217.

45. Kajstura M, Halicka HD, Pryjma J, Darzynkiewicz Z. Discontinuous fragmentation of nuclear DNA during apoptosis revealed by discrete "sub-G1" peaks on DNA content histograms. Cytometry Part A: the journal of the International Society for Analytical Cytology. 2007;71(3):125–31. Epub 2007/01/26. doi: 10.1002/cyto.a.20357 17252584.

46. Liu G, McDonnell TJ, Montes de Oca Luna R, Kapoor M, Mims B, El-Naggar AK, et al. High metastatic potential in mice inheriting a targeted p53 missense mutation. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(8):4174–9. doi: 10.1073/pnas.97.8.4174 10760284.

47. Goh HS, Yao J, Smith DR. p53 point mutation and survival in colorectal cancer patients. Cancer research. 1995;55(22):5217–21. Epub 1995/11/15. 7585578.

48. Muller PA, Vousden KH. p53 mutations in cancer. Nature cell biology. 2013;15(1):2–8. Epub 2012/12/25. doi: 10.1038/ncb2641 23263379.

49. Brosh R, Rotter V. When mutants gain new powers: news from the mutant p53 field. Nature reviews Cancer. 2009;9(10):701–13. Epub 2009/08/21. doi: 10.1038/nrc2693 19693097.

50. Vogelstein B, Kinzler KW. The Path to Cancer—Three Strikes and You're Out. The New England journal of medicine. 2015;373(20):1895–8. Epub 2015/11/13. doi: 10.1056/NEJMp1508811 26559569.

51. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr., Kinzler KW. Cancer genome landscapes. Science (New York, NY). 2013;339(6127):1546–58. doi: 10.1126/science.1235122 23539594.

52. Quinn JE, James CR, Stewart GE, Mulligan JM, White P, Chang GK, et al. BRCA1 mRNA expression levels predict for overall survival in ovarian cancer after chemotherapy. Clinical cancer research: an official journal of the American Association for Cancer Research. 2007;13(24):7413–20. Epub 2007/12/21. doi: 10.1158/1078-0432.Ccr-07-1083 18094425.

53. Tsibulak I, Wieser V, Degasper C, Shivalingaiah G, Wenzel S, Sprung S, et al. BRCA1 and BRCA2 mRNA-expression prove to be of clinical impact in ovarian cancer. British journal of cancer. 2018;119(6):683–92. Epub 2018/08/17. doi: 10.1038/s41416-018-0217-4 30111871.

54. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell. 2006;127(4):679–95. doi: 10.1016/j.cell.2006.11.001 17110329.

55. Mehlen P, Puisieux A. Metastasis: a question of life or death. Nature reviews Cancer. 2006;6(6):449–58. doi: 10.1038/nrc1886 16723991.

56. Gomez-Cuadrado L, Tracey N, Ma R, Qian B, Brunton VG. Mouse models of metastasis: progress and prospects. Disease models & mechanisms. 2017;10(9):1061–74. Epub 2017/09/09. doi: 10.1242/dmm.030403 28883015; PubMed Central PMCID: PMC5611969.

57. Lloyd SM, Arnold J, Sreekumar A. Metabolomic profiling of hormone-dependent cancers: a bird's eye view. Trends in endocrinology and metabolism: TEM. 2015;26(9):477–85. Epub 2015/08/06. doi: 10.1016/j.tem.2015.07.001 26242817; PubMed Central PMCID: PMC4560106.

58. Gaul DA, Mezencev R, Long TQ, Jones CM, Benigno BB, Gray A, et al. Highly-accurate metabolomic detection of early-stage ovarian cancer. Scientific reports. 2015;5:16351. doi: 10.1038/srep16351 26573008; PubMed Central PMCID: PMC4647115.

59. Huang D, Gaul DA, Nan H, Kim J, Fernandez FM. Deep Metabolomics of a High-Grade Serous Ovarian Cancer Triple-Knockout Mouse Model. Journal of proteome research. 2019;18(8):3184–94. Epub 2019/07/11. doi: 10.1021/acs.jproteome.9b00263 31290664.

60. Collisson EA, Cho RJ, Gray JW. What are we learning from the cancer genome? Nature reviews Clinical oncology. 2012;9(11):621–30. Epub 2012/09/12. doi: 10.1038/nrclinonc.2012.159 22965149; PubMed Central PMCID: PMC4169265.

61. Li SC, Tachiki LM, Kabeer MH, Dethlefs BA, Anthony MJ, Loudon WG. Cancer genomic research at the crossroads: realizing the changing genetic landscape as intratumoral spatial and temporal heterogeneity becomes a confounding factor. Cancer cell international. 2014;14(1):115. Epub 2014/11/21. doi: 10.1186/s12935-014-0115-7 25411563; PubMed Central PMCID: PMC4236490.

62. Ciriello G, Miller ML, Aksoy BA, Senbabaoglu Y, Schultz N, Sander C. Emerging landscape of oncogenic signatures across human cancers. Nature genetics. 2013;45(10):1127–33. Epub 2013/09/28. doi: 10.1038/ng.2762 24071851; PubMed Central PMCID: PMC4320046.

63. Macintyre G, Goranova TE, De Silva D, Ennis D, Piskorz AM, Eldridge M, et al. Copy number signatures and mutational processes in ovarian carcinoma. Nature genetics. 2018;50(9):1262–70. Epub 2018/08/15. doi: 10.1038/s41588-018-0179-8 30104763; PubMed Central PMCID: PMC6130818.

64. Patch AM, Christie EL, Etemadmoghadam D, Garsed DW, George J, Fereday S, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature. 2015;521(7553):489–94. Epub 2015/05/29. doi: 10.1038/nature14410 26017449.

65. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nature medicine. 2004;10(8):789–99. doi: 10.1038/nm1087 15286780.

66. Barger CJ, Branick C, Chee L, Karpf AR. Pan-Cancer Analyses Reveal Genomic Features of FOXM1 Overexpression in Cancer. Cancers. 2019;11(2). Epub 2019/02/24. doi: 10.3390/cancers11020251 30795624; PubMed Central PMCID: PMC6406812.

67. Hanel W, Moll UM. Links between mutant p53 and genomic instability. J Cell Biochem. 2012;113(2):433–9. Epub 2011/10/19. doi: 10.1002/jcb.23400 22006292; PubMed Central PMCID: PMC4407809.

68. Arango NA, Kobayashi A, Wang Y, Jamin SP, Lee HH, Orvis GD, et al. A mesenchymal perspective of Mullerian duct differentiation and regression in Amhr2-lacZ mice. Mol Reprod Dev. 2008;75(7):1154–62. doi: 10.1002/mrd.20858 18213646.

69. Huang CC, Orvis GD, Wang Y, Behringer RR. Stromal-to-Epithelial Transition during Postpartum Endometrial Regeneration. PloS one. 2012;7(8):e44285. doi: 10.1371/journal.pone.0044285 22970108.

70. Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, Menko FH, et al. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol. 2001;195(4):451–6. doi: 10.1002/path.1000 11745677.

71. Piek JM, Verheijen RH, Kenemans P, Massuger LF, Bulten H, van Diest PJ. BRCA1/2-related ovarian cancers are of tubal origin: a hypothesis. Gynecologic oncology. 2003;90(2):491. Epub 2003/08/02. doi: 10.1016/s0090-8258(03)00365-2 12893227.

72. Kurman RJ, Shih Ie M. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. The American journal of surgical pathology. 2010;34(3):433–43. doi: 10.1097/PAS.0b013e3181cf3d79 20154587.

73. Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, et al. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship. The American journal of surgical pathology. 2007;31(2):161–9. doi: 10.1097/01.pas.0000213335.40358.47 17255760.

74. Przybycin CG, Kurman RJ, Ronnett BM, Shih Ie M, Vang R. Are all pelvic (nonuterine) serous carcinomas of tubal origin? The American journal of surgical pathology. 2010;34(10):1407–16. doi: 10.1097/PAS.0b013e3181ef7b16 20861711.

75. Labidi-Galy SI, Papp E, Hallberg D, Niknafs N, Adleff V, Noe M, et al. High grade serous ovarian carcinomas originate in the fallopian tube. Nat Commun. 2017;8(1):1093. Epub 2017/10/25. doi: 10.1038/s41467-017-00962-1 29061967; PubMed Central PMCID: PMC5653668.

76. Tone AA, Salvador S, Finlayson SJ, Tinker AV, Kwon JS, Lee CH, et al. The role of the fallopian tube in ovarian cancer. Clin Adv Hematol Oncol. 2012;10(5):296–306. 22706539.

77. Dietl J, Wischhusen J, Hausler SF. The post-reproductive Fallopian tube: better removed? Human reproduction (Oxford, England). 2011;26(11):2918–24. doi: 10.1093/humrep/der274 21849300.

78. Klotz DM, Wimberger P. Cells of origin of ovarian cancer: ovarian surface epithelium or fallopian tube? Arch Gynecol Obstet. 2017;296(6):1055–62. Epub 2017/09/25. doi: 10.1007/s00404-017-4529-z 28940023.

79. Quartuccio SM, Lantvit DD, Bosland MC, Burdette JE. Conditional inactivation of p53 in mouse ovarian surface epithelium does not alter MIS driven Smad2-dominant negative epithelium-lined inclusion cysts or teratomas. PloS one. 2013;8(5):e65067. Epub 2013/06/07. doi: 10.1371/journal.pone.0065067 23741457; PubMed Central PMCID: PMC3669126.

80. Yaginuma Y, Westphal H. Abnormal structure and expression of the p53 gene in human ovarian carcinoma cell lines. Cancer research. 1992;52(15):4196–9. Epub 1992/08/01. 1638534.

81. Whitfield ML, Zheng LX, Baldwin A, Ohta T, Hurt MM, Marzluff WF. Stem-loop binding protein, the protein that binds the 3' end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Molecular and cellular biology. 2000;20(12):4188–98. Epub 2000/05/29. doi: 10.1128/mcb.20.12.4188-4198.2000 10825184; PubMed Central PMCID: PMC85788.

82. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics (Oxford, England). 2013;29(1):15–21. Epub 2012/10/30. doi: 10.1093/bioinformatics/bts635 23104886; PubMed Central PMCID: PMC3530905.

83. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics (Oxford, England). 2014;30(7):923–30. Epub 2013/11/15. doi: 10.1093/bioinformatics/btt656 24227677.

84. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biology. 2014;15(12):550. Epub 2014/12/18. doi: 10.1186/s13059-014-0550-8 25516281; PubMed Central PMCID: PMC4302049.

85. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer discovery. 2012;2(5):401–4. Epub 2012/05/17. doi: 10.1158/2159-8290.CD-12-0095 22588877; PubMed Central PMCID: PMC3956037.


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 6

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se