Multiclonal Invasion in Breast Tumors Identified by Topographic Single Cell Sequencing

Cell

Volumn 172, Issue 1-2, 2018, Pages 205-217.e12

  Casasent, Anna K ^a,b   Schalck, Aislyn ^a,b   Gao, Ruli ^a   Sei, Emi ^a   Long, Annalyssa ^a   Pangburn, William ^a   Casasent, Tod ^a   Meric Bernstam, Funda ^a   Edgerton, Mary E ^a   Navin, Nicholas E ^a,b  

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

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

breast cancer; breast cancer progression; cancer genomics; clonal evolution; copy number evolution; ductal carcinoma in situ; genome evolution; intratumor heterogeneity; invasion; single cell sequencing

Indexed keywords

ARTICLE; BREAST CARCINOMA; BREAST TUMOR; CARCINOGENESIS; CELL LINEAGE; CELL MIGRATION; CELL SUBPOPULATION; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; COPY NUMBER VARIATION; DNA SEQUENCE; EXOME; GENE DOSAGE; GENE MUTATION; GENETIC DISTANCE; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRADUCTAL CARCINOMA; PRIORITY JOURNAL; TOPOGRAPHIC SINGEL CELL SEQUENCING; TUMOR INVASION; ADULT; AGED; CELL MOTION; CLONAL EVOLUTION; FEMALE; GENETICS; MIDDLE AGED; MUTATION; PAGET NIPPLE DISEASE; PATHOLOGY; SINGLE CELL ANALYSIS;

ADULT; AGED; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL MOVEMENT; CLONAL EVOLUTION; EXOME; FEMALE; HUMANS; MIDDLE AGED; MUTATION; NEOPLASM INVASIVENESS; SEQUENCE ANALYSIS, DNA; SINGLE-CELL ANALYSIS;

EID: 85039917429     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.12.007     Document Type: Article

References (64)

1. Aceto, N., Bardia, A., Miyamoto, D.T., Donaldson, M.C., Wittner, B.S., Spencer, J.A., Yu, M., Pely, A., Engstrom, A., Zhu, H., et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158 (2014), 1110–1122.
2. Allred, D.C., Ductal carcinoma in situ: terminology, classification, and natural history. J. Natl. Cancer Inst. Monogr. 2010 (2010), 134–138.
3. Allred, D.C., Wu, Y., Mao, S., Nagtegaal, I.D., Lee, S., Perou, C.M., Mohsin, S.K., O'Connell, P., Tsimelzon, A., Medina, D., Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin. Cancer Res. 14 (2008), 370–378.
4. Andl, C.D., Mizushima, T., Oyama, K., Bowser, M., Nakagawa, H., Rustgi, A.K., EGFR-induced cell migration is mediated predominantly by the JAK-STAT pathway in primary esophageal keratinocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 287 (2004), G1227–G1237.
5. Baslan, T., Kendall, J., Rodgers, L., Cox, H., Riggs, M., Stepansky, A., Troge, J., Ravi, K., Esposito, D., Lakshmi, B., et al. Genome-wide copy number analysis of single cells. Nat. Protoc. 7 (2012), 1024–1041.
6. Baslan, T., Kendall, J., Ward, B., Cox, H., Leotta, A., Rodgers, L., Riggs, M., D'Italia, S., Sun, G., Yong, M., et al. Optimizing sparse sequencing of single cells for highly multiplex copy number profiling. Genome Res. 25 (2015), 714–724.
7. Chin, K., de Solorzano, C.O., Knowles, D., Jones, A., Chou, W., Rodriguez, E.G., Kuo, W.L., Ljung, B.M., Chew, K., Myambo, K., et al. In situ analyses of genome instability in breast cancer. Nat. Genet. 36 (2004), 984–988.
8. Cowell, C.F., Weigelt, B., Sakr, R.A., Ng, C.K., Hicks, J., King, T.A., Reis-Filho, J.S., Progression from ductal carcinoma in situ to invasive breast cancer: revisited. Mol. Oncol. 7 (2013), 859–869.
9. Datta, S., Malhotra, L., Dickerson, R., Chaffee, S., Sen, C.K., Roy, S., Laser capture microdissection: Big data from small samples. Histol. Histopathol. 30 (2015), 1255–1269.
10. Dudik, J.M., Kurosu, A., Coyle, J.L., Sejdić E., A comparative analysis of DBSCAN, K-means, and quadratic variation algorithms for automatic identification of swallows from swallowing accelerometry signals. Comput. Biol. Med. 59 (2015), 10–18.
11. Ester, M., Kriegel, H.-P., Sander, J., Xu, X. (1996). A Density-Based Algorithm for Discovering Clusters in Large Spatial Databases with Noise. Proceedings of the 2nd International Conference on Knowledge Discovery and Data Mining.
12. Foschini, M.P., Morandi, L., Leonardi, E., Flamminio, F., Ishikawa, Y., Masetti, R., Eusebi, V., Genetic clonal mapping of in situ and invasive ductal carcinoma indicates the field cancerization phenomenon in the breast. Hum. Pathol. 44 (2013), 1310–1319.
13. Futreal, P.A., Coin, L., Marshall, M., Down, T., Hubbard, T., Wooster, R., Rahman, N., Stratton, M.R., A census of human cancer genes. Nat. Rev. Cancer 4 (2004), 177–183.
14. Galili, T., dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics 31 (2015), 3718–3720.
15. Gao, R., Davis, A., McDonald, T.O., Sei, E., Shi, X., Wang, Y., Tsai, P.C., Casasent, A., Waters, J., Zhang, H., et al. Punctuated copy number evolution and clonal stasis in triple-negative breast cancer. Nat. Genet. 48 (2016), 1119–1130.
16. Gao, R., Kim, C., Sei, E., Foukakis, T., Crosetto, N., Chan, L.K., Srinivasan, M., Zhang, H., Meric-Bernstam, F., Navin, N., Nanogrid single-nucleus RNA sequencing reveals phenotypic diversity in breast cancer. Nat. Commun., 8, 2017, 228.
17. Gerlinger, M., Horswell, S., Larkin, J., Rowan, A.J., Salm, M.P., Varela, I., Fisher, R., McGranahan, N., Matthews, N., Santos, C.R., et al. Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing. Nat. Genet. 46 (2014), 225–233.
18. Gerstung, M., Beisel, C., Rechsteiner, M., Wild, P., Schraml, P., Moch, H., Beerenwinkel, N., Reliable detection of subclonal single-nucleotide variants in tumour cell populations. Nat. Commun., 3, 2012, 811.
19. Gerstung, M., Papaemmanuil, E., Campbell, P.J., Subclonal variant calling with multiple samples and prior knowledge. Bioinformatics 30 (2014), 1198–1204.
20. Grindberg, R.V., Yee-Greenbaum, J.L., McConnell, M.J., Novotny, M., O'Shaughnessy, A.L., Lambert, G.M., Araúzo-Bravo, M.J., Lee, J., Fishman, M., Robbins, G.E., et al. RNA-sequencing from single nuclei. Proc. Natl. Acad. Sci. USA 110 (2013), 19802–19807.
21. Hernandez, L., Wilkerson, P.M., Lambros, M.B., Campion-Flora, A., Rodrigues, D.N., Gauthier, A., Cabral, C., Pawar, V., Mackay, A., A'Hern, R., et al. Genomic and mutational profiling of ductal carcinomas in situ and matched adjacent invasive breast cancers reveals intra-tumour genetic heterogeneity and clonal selection. J. Pathol. 227 (2012), 42–52.
22. Heselmeyer-Haddad, K., Berroa Garcia, L.Y., Bradley, A., Ortiz-Melendez, C., Lee, W.J., Christensen, R., Prindiville, S.A., Calzone, K.A., Soballe, P.W., Hu, Y., et al. Single-cell genetic analysis of ductal carcinoma in situ and invasive breast cancer reveals enormous tumor heterogeneity yet conserved genomic imbalances and gain of MYC during progression. Am. J. Pathol. 181 (2012), 1807–1822.
23. Hu, M., Yao, J., Carroll, D.K., Weremowicz, S., Chen, H., Carrasco, D., Richardson, A., Violette, S., Nikolskaya, T., Nikolsky, Y., et al. Regulation of in situ to invasive breast carcinoma transition. Cancer Cell 13 (2008), 394–406.
24. Johnson, C.E., Gorringe, K.L., Thompson, E.R., Opeskin, K., Boyle, S.E., Wang, Y., Hill, P., Mann, G.B., Campbell, I.G., Identification of copy number alterations associated with the progression of DCIS to invasive ductal carcinoma. Breast Cancer Res. Treat. 133 (2012), 889–898.
25. Kim, S.Y., Jung, S.H., Kim, M.S., Baek, I.P., Lee, S.H., Kim, T.M., Chung, Y.J., Lee, S.H., Genomic differences between pure ductal carcinoma in situ and synchronous ductal carcinoma in situ with invasive breast cancer. Oncotarget 6 (2015), 7597–7607.
26. Krøigård, A.B., Larsen, M.J., Lænkholm, A.V., Knoop, A.S., Jensen, J.D., Bak, M., Mollenhauer, J., Kruse, T.A., Thomassen, M., Clonal expansion and linear genome evolution through breast cancer progression from pre-invasive stages to asynchronous metastasis. Oncotarget 6 (2015), 5634–5649.
27. Leung, M.L., Wang, Y., Waters, J., Navin, N.E., SNES: single nucleus exome sequencing. Genome Biol., 16, 2015, 55.
28. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
29. Lohr, J.G., Adalsteinsson, V.A., Cibulskis, K., Choudhury, A.D., Rosenberg, M., Cruz-Gordillo, P., Francis, J.M., Zhang, C.Z., Shalek, A.K., Satija, R., et al. Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer. Nat. Biotechnol. 32 (2014), 479–484.
30. Macosko, E.Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A.R., Kamitaki, N., Martersteck, E.M., et al. Highly Parallel Genome-wide Expression Profiling of Individual Cells Using Nanoliter Droplets. Cell 161 (2015), 1202–1214.
31. Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., and Hornik, K. (2012). Cluster: Cluster Analysis Basics and Extensions.
32. Malikic, S., McPherson, A.W., Donmez, N., Sahinalp, C.S., Clonality inference in multiple tumor samples using phylogeny. Bioinformatics 31 (2015), 1349–1356.
33. Martelotto, L.G., Baslan, T., Kendall, J., Geyer, F.C., Burke, K.A., Spraggon, L., Piscuoglio, S., Chadalavada, K., Nanjangud, G., Ng, C.K., et al. Whole-genome single-cell copy number profiling from formalin-fixed paraffin-embedded samples. Nat. Med. 23 (2017), 376–385.
34. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Daly, M., et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20 (2010), 1297–1303.
35. McPherson, A., Roth, A., Laks, E., Masud, T., Bashashati, A., Zhang, A.W., Ha, G., Biele, J., Yap, D., Wan, A., et al. Divergent modes of clonal spread and intraperitoneal mixing in high-grade serous ovarian cancer. Nat. Genet. 48 (2016), 758–767.
36. Miron, A., Varadi, M., Carrasco, D., Li, H., Luongo, L., Kim, H.J., Park, S.Y., Cho, E.Y., Lewis, G., Kehoe, S., et al. PIK3CA mutations in in situ and invasive breast carcinomas. Cancer Res. 70 (2010), 5674–5678.
37. Murtagh, F., Legendre, P., Ward's Hierarchical Agglomerative Clustering Method: Which Algorithms Implement Ward's Criterion?. J. Classif. 31 (2014), 274–295.
38. Navin, N., Krasnitz, A., Rodgers, L., Cook, K., Meth, J., Kendall, J., Riggs, M., Eberling, Y., Troge, J., Grubor, V., et al. Inferring tumor progression from genomic heterogeneity. Genome Res. 20 (2010), 68–80.
39. Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., Cook, K., Stepansky, A., Levy, D., Esposito, D., et al. Tumour evolution inferred by single-cell sequencing. Nature 472 (2011), 90–94.
40. Newburger, D.E., Kashef-Haghighi, D., Weng, Z., Salari, R., Sweeney, R.T., Brunner, A.L., Zhu, S.X., Guo, X., Varma, S., Troxell, M.L., et al. Genome evolution during progression to breast cancer. Genome Res. 23 (2013), 1097–1108.
41. Patel, A.P., Tirosh, I., Trombetta, J.J., Shalek, A.K., Gillespie, S.M., Wakimoto, H., Cahill, D.P., Nahed, B.V., Curry, W.T., Martuza, R.L., et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344 (2014), 1396–1401.
42. Piekenbrock, M.H.a.M. (2017). dbscan: Density Based Clustering of Applications with Noise (DBSCAN) and Related Algorithms. (CRAN).
43. Roth, A., Khattra, J., Yap, D., Wan, A., Laks, E., Biele, J., Ha, G., Aparicio, S., Bouchard-Côté A., Shah, S.P., PyClone: statistical inference of clonal population structure in cancer. Nat. Methods 11 (2014), 396–398.
44. Sakr, R.A., Weigelt, B., Chandarlapaty, S., Andrade, V.P., Guerini-Rocco, E., Giri, D., Ng, C.K., Cowell, C.F., Rosen, N., Reis-Filho, J.S., King, T.A., PI3K pathway activation in high-grade ductal carcinoma in situ–implications for progression to invasive breast carcinoma. Clin. Cancer Res. 20 (2014), 2326–2337.
45. Sarper, M., Allen, M.D., Gomm, J., Haywood, L., Decock, J., Thirkettle, S., Ustaoglu, A., Sarker, S.J., Marshall, J., Edwards, D.R., Jones, J.L., Loss of MMP-8 in ductal carcinoma in situ (DCIS)-associated myoepithelial cells contributes to tumour promotion through altered adhesive and proteolytic function. Breast Cancer Res., 19, 2017, 33.
46. Scornavacca, C., Zickmann, F., Huson, D.H., Tanglegrams for rooted phylogenetic trees and networks. Bioinformatics 27 (2011), i248–i256.
47. Shah, S.P., Xuan, X., DeLeeuw, R.J., Khojasteh, M., Lam, W.L., Ng, R., Murphy, K.P., Integrating copy number polymorphisms into array CGH analysis using a robust HMM. Bioinformatics 22 (2006), e431–e439.
48. Shah, S.P., Roth, A., Goya, R., Oloumi, A., Ha, G., Zhao, Y., Turashvili, G., Ding, J., Tse, K., Haffari, G., et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 486 (2012), 395–399.
49. Sharma, M., Beck, A.H., Webster, J.A., Espinosa, I., Montgomery, K., Varma, S., van de Rijn, M., Jensen, K.C., West, R.B., Analysis of stromal signatures in the tumor microenvironment of ductal carcinoma in situ. Breast Cancer Res. Treat. 123 (2010), 397–404.
50. Smith, M.A., Nielsen, C.B., Chan, F.C., McPherson, A., Roth, A., Farahani, H., Machev, D., Steif, A., Shah, S.P., E-scape: interactive visualization of single-cell phylogenetics and cancer evolution. Nat. Methods 14 (2017), 549–550.
51. Song, Y., Tian, T., Shi, Y., Liu, W., Zou, Y., Khajvand, T., Wang, S., Zhu, Z., Yang, C., Enrichment and single-cell analysis of circulating tumor cells. Chem. Sci. (Camb.) 8 (2017), 1736–1751.
52. Sontag, L., Axelrod, D.E., Evaluation of pathways for progression of heterogeneous breast tumors. J. Theor. Biol. 232 (2005), 179–189.
53. Suh, S.S., Yoo, J.Y., Cui, R., Kaur, B., Huebner, K., Lee, T.K., Aqeilan, R.I., Croce, C.M., FHIT suppresses epithelial-mesenchymal transition (EMT) and metastasis in lung cancer through modulation of microRNAs. PLoS Genet., 10, 2014, e1004652.
54. Tibshirani, R., Walther, G., Hastie, T., Estimating the number of data clusters via the Gap statistic. J. Royal Stat. Soc. 63 (2001), 411–423.
55. Tirosh, I., Izar, B., Prakadan, S.M., Wadsworth, M.H. 2nd, Treacy, D., Trombetta, J.J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352 (2016), 189–196.
56. Vandewoestyne, M., Goossens, K., Burvenich, C., Van Soom, A., Peelman, L., Deforce, D., Laser capture microdissection: should an ultraviolet or infrared laser be used?. Anal. Biochem. 439 (2013), 88–98.
57. Vehviläinen, P., Hyytiäinen, M., Keski-Oja, J., Latent transforming growth factor-beta-binding protein 2 is an adhesion protein for melanoma cells. J. Biol. Chem. 278 (2003), 24705–24713.
58. Virnig, B.A., Tuttle, T.M., Shamliyan, T., Kane, R.L., Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes. J. Natl. Cancer Inst. 102 (2010), 170–178.
59. Wang, K., Li, M., Hakonarson, H., ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res., 38, 2010, e164.
60. Wang, Y., Waters, J., Leung, M.L., Unruh, A., Roh, W., Shi, X., Chen, K., Scheet, P., Vattathil, S., Liang, H., et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 512 (2014), 155–160.
61. Xu, X., Hou, Y., Yin, X., Bao, L., Tang, A., Song, L., Li, F., Tsang, S., Wu, K., Wu, H., et al. Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. Cell 148 (2012), 886–895.
62. Yates, L.R., Gerstung, M., Knappskog, S., Desmedt, C., Gundem, G., Van Loo, P., Aas, T., Alexandrov, L.B., Larsimont, D., Davies, H., et al. Subclonal diversification of primary breast cancer revealed by multiregion sequencing. Nat. Med. 21 (2015), 751–759.
63. Yue, S.H., Li, P., Guo, J.D., Zhou, S.G., Using Greedy algorithm: DBSCAN revisited II. J. Zhejiang Univ. Sci. 5 (2004), 1405–1412.
64. Zong, C., Lu, S., Chapman, A.R., Xie, X.S., Genome-wide detection of single-nucleotide and copy-number variations of a single human cell. Science 338 (2012), 1622–1626.