Genomics of ovarian cancer progression reveals diverse metastatic trajectories including intraepithelial metastasis to the fallopian tube

Cancer Discovery

Volumn 6, Issue 12, 2016, Pages 1342-1351

  Eckert, Mark A ^a   Pan, Shawn ^a   Hernandez, Kyle M ^a   Loth, Rachel M ^a   Andrade, Jorge ^a   Volchenboum, Samuel L ^a   Faber, Pieter ^a   Montag, Anthony ^a   Lastra, Ricardo ^a   Peter, Marcus E ^b   Yamada, S Diane ^a   Lengyel, Ernst ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOCARCINOMA CELL LINE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL ADHESION; CELL ADHESION ASSAY; CLINICAL ARTICLE; DNA EXTRACTION; DNA ISOLATION; GENE; GENE AMPLIFICATION; GENE SEQUENCE; GENOMICS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; METASTASIS; OVARY CANCER; OVARY TUMOR; PHYLOGENY; SOMATIC MUTATION; TP53 GENE; TUMOR SUPPRESSOR GENE; UTERINE TUBE CARCINOMA; WHOLE EXOME SEQUENCING; CYSTADENOCARCINOMA, SEROUS; DISEASE COURSE; DNA SEQUENCE; FALLOPIAN TUBE NEOPLASMS; FEMALE; GENETICS; GENOMIC INSTABILITY; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; PROCEDURES; TUMOR CELL CULTURE;

CYSTADENOCARCINOMA, SEROUS; DISEASE PROGRESSION; FALLOPIAN TUBE NEOPLASMS; FEMALE; GENOMIC INSTABILITY; GENOMICS; HUMANS; NEOPLASM METASTASIS; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; TUMOR CELLS, CULTURED;

EID: 85007358573     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-16-0607     Document Type: Article

References (51)

1. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol 2010; 177: 1053-64.
2. Norquist BM, Harrell MI, Brady MF, Walsh T, Lee MK, Gulsuner S, et al. Inherited mutations in women with ovarian carcinoma. JAMA Oncol 2015: 1-9.
3. Patch AM, Christie EL, Etemadmoghadam D, Garsed DW, George J, Fereday S, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature 2015; 521: 489-94.
4. 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: 451-6.
5. Kuhn E, Kurman RJ, Vang R, Sehdev AS, Han G, Soslow R, et al. TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma-evidence supporting the clonal relationship of the two lesions. J Pathol 2012; 226: 421-6.
6. 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: 26-35.
7. Perets R, Wyant GA, Muto KW, Bijron JG, Poole BB, Chin KT, 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: 751-65.
8. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759-67.
9. The Cancer Genome Atlas N. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474: 609-15.
10. Ciriello G, Miller ML, Aksoy BA, Senbabaoglu Y, Schultz N, Sander C. Emerging landscape of oncogenic signatures across human cancers. Nat Genet 2013; 45: 1127-33.
11. Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010; 467: 1114-7.
12. McDaniel AS, Stall JN, Hovelson DH, Cani AK, Liu CJ, Tomlins SA, et al. Next-generation sequencing of tubal intraepithelial carcinomas. JAMA Oncol 2015; 1: 1128-32.
13. Schwarz RF, Ng CK, Cooke SL, Newman S, Temple J, Piskorz A M, et al. Spatial and temporal heterogeneity in high-grade serous ovarian cancer: A phylogenetic analysis. PLoS Med 2015; 12: e1001789.
14. McPherson A, Roth A, Laks E, Masud T, Bashashati A, Zhang AW, et al. Divergent modes of clonal spread and intraperitoneal mixing in high-grade serous ovarian cancer. Nat Genet 2016; 48: 758-67.
15. Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, et al. Mutational landscape and signifi cance across 12 major cancer types. Nature 2013; 502: 333-9.
16. Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013; 499: 214-8.
17. George J, Alsop K, Etemadmoghadam D, Hondow H, Mikeska T, Dobrovic A, et al. Nonequivalent gene expression and copy number alterations in high-grade serous ovarian cancers with BRCA1 and BRCA2 mutations. Clin Cancer Res 2013; 19: 3474-84.
18. Mermel CH, Schumacher SE, Hill B, Meyerson ML, Beroukhim R, Getz G. GISTIC2.0 facilitates sensitive and confi dent localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol 2011; 12: R41.
19. Stewart CJ, Leung YC, Whitehouse A. Fallopian tube metastases of non-gynaecological origin: A series of 20 cases emphasizing patterns of involvement including intra-epithelial spread. Histopathology 2012; 60: E106-14.
20. Rabban JT, Vohra P, Zaloudek CJ. Nongynecologic metastases to fallopian tube mucosa: A potential mimic of tubal high-grade serous carcinoma and benign tubal mucinous metaplasia or nonmucinous hyperplasia. Am J Surg Pathol 2015; 39: 35-51.
21. Bijron JG, Seldenrijk CA, Zweemer RP, Lange JG, Verheijen RH, van Diest PJ. Fallopian tube intraluminal tumor spread from noninvasive precursor lesions: A novel metastatic route in early pelvic carcinogenesis. Am J Surg Pathol 2013; 37: 1123-30.
22. Karst AM, Drapkin R. Primary culture and immortalization of human fallopian tube secretory epithelial cells. Nat Protoc 2012; 7: 1755-64.
23. Karst AM, Levanon K, Duraisamy S, Liu JF, Hirsch MS, Hecht JL, et al. Stathmin 1, a marker of PI3K pathway activation and regulator of microtubule dynamics, is expressed in early pelvic serous carcinomas. Gynecol Oncol 2011; 123: 5-12.
24. Ahmet 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. Journal of Pathology 2010; 221: 49-56. 2
25. K iryu T, H oshi H, M atsui E, I wata H, K okubo M, S himokawa K, et al. Endotracheal/endobronchial metastases: Clinicopathologic study with special reference to developmental modes. Chest 2001; 119: 768-75.
26. Nik NN, Vang R, Shih IE M, Kurman RJ. Origin and pathogenesis of pelvic (ovarian, tubal, and primary peritoneal) serous carcinoma. Annu Rev Pathol 2014; 9: 27-45.
27. Kenny HA, Kaur S, Coussens LM, Lengyel E. The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fi bronectin. J Clin Invest 2008; 118: 1367-79.
28. Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R, Zillhardt M, et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat Med 2011; 17: 1498-503.
29. Zinsser KR, Wheeler JE. Endosalpingiosis in the omentum: A study of autopsy and surgical material. Am J Surg Pathol 1982; 6: 109-17.
30. Prentice L, Stewart A, Mohiuddin S, Johnson NP. What is endosalpingiosis? Fertil Steril 2012; 98: 942-7.
31. McCoubrey A, Houghton O, McCallion K, McCluggage WG. Serous adenocarcinoma of the sigmoid mesentery arising in cystic endosalpingiosis. J Clin Pathol 2005; 58: 1221-3.
32. Perets R, Drapkin R. It’s totally tubular…riding the new wave of ovarian cancer research. Cancer Res 2016; 76: 10-7.
33. Falconer H, Yin L, Gronberg H, Altman D. Ovarian cancer risk after salpingectomy: a nationwide population-based study. J Natl Cancer Inst 2015; 107.
34. Daly MB, Dresher CW, Yates MS, Jeter JM, Karlan BY, Alberts DS, et al. Salpingectomy as a means to reduce ovarian cancer risk. Cancer Prev Res (Phila) 2015; 8: 342-8.
35. Przybycin CG, Kurman RJ, Ronnett BM, Shih Ie M, Vang R. Are all pelvic (nonuterine) serous carcinomas of tubal origin? Am J Surg Pathol 2010; 34: 1407-16.
36. Colon E, Carlson JW. Evaluation of the fallopian tubes after neoadjuvant chemotherapy: Persistence of serous tubal intraepithelial carcinoma. Int J Gynecol Pathol 2014;33:463-9.
37. Tarasov A, Vilella AJ, Cuppen E, Nijman IJ, Prins P. Sambamba: Fast processing of NGS alignment formats. Bioinformatics 2015; 31: 2032-4.
38. Van der Auwera GA, Carneiro MO, Hartl C, Poplin R, Del Angel G, Levy-Moonshine A, et al. From FastQ data to high confi dence variant calls: The genome analysis toolkit best practices pipeline. Curr Protoc Bioinformatics 2013; 43: 1101-33.
39. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20: 1297-303.
40. Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, Sougnez C, et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol 2013; 31: 213-9.
41. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, et al. VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 2012; 22: 568-76.
42. Kim S, Jeong K, Bhutani K, Lee J, Patel A, Scott E, e t al. Virmid: Accurate detection of somatic mutations with sample impurity inference. Genome Biol 2013; 14: R90.
43. Bao R, Hernandez K, Huang L, Kang W, Bartom E, Onel K, et al. ExScalibur: A high-performance cloud-enabled suite for whole exome germline and somatic mutation identifi cation. PLoS One 2015; 10: e0135800.
44. Wang K, Li M, Hakonarson H. ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 2010; 38: e164.
45. Ramos AH, Lichtenstein L, Gupta M, Lawrence MS, Pugh TJ, Saksena G, et al. Oncotator: cancer variant annotation tool. Hum Mutat 2015; 36: E2423-9.
46. Lonigro RJ, Grasso CS, Robinson DR, Jing X, Wu YM, Cao X, et al. Detection of somatic copy number alterations in cancer using targeted exome capture sequencing. Neoplasia 2011; 13: 1019-25.
47. Nilsen G, Liestol K, Van Loo P, Moen Vollan HK, Eide MB, Rueda OM, et al. Copynumber: Effi cient algorithms for single-and multitrack copy number segmentation. BMC Genomics 2012; 13: 591.
48. Garcia-Vallve S, Palau J, Romeu A. Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis. Mol Biol Evol 1999; 16: 1125-34.
49. Sokal RR, Rohlf FJ. The comparison of dendrograms by objective methods. Taxon 1962; 11: 33-40.
50. Letunic I, Bork P. Interactive Tree Of Life (iTOL): An online tool for phylogenetic tree display and annotation. Bioinformatics 2007; 23: 127-8.
51. Iwanicki M, Davidowitz RA, Ng MR, Besser A, Muranen T, Merritt M, et al. Ovarian cancer spheroids use myosin-generated force to clear the mesothelium. Cancer Discov 2011; 1: 144-57.