Single cell profiling of Circulating tumor cells: Transcriptional heterogeneity and diversity from breast cancer cell lines

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Powell, Ashley A ^a   Talasaz, AmirAli H ^a,b,g   Zhang, Haiyu ^a   Coram, Marc A ^a   Reddy, Anupama ^c,h   Deng, Glenn ^a,i   Telli, Melinda L ^a   Advani, Ranjana H ^a   Carlson, Robert W ^a   Mollick, Joseph A ^a   Sheth, Shruti ^a   Kurian, Allison W ^a   Ford, James M ^a   Stockdale, Frank E ^a   Quake, Stephen R ^b   Pease, R Fabian ^b   Mindrinos, Michael N ^a   Bhanot, Gyan ^c,d,e   Dairkee, Shanaz H ^a,f   Davis, Ronald W ^a   Jeffrey, Stefanie S ^a   more..

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Stanford University   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^e INSTITUTE FOR ADVANCED STUDY   (United States)

^f CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^g ILLUMINA INC   (United States)

^h NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

ⁱ HUBEI UNIVERSITY OF ARTS AND SCIENCE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL AGGREGATION; CELL DIFFERENTIATION; CIRCULATING TUMOR CELL; CONTROLLED STUDY; CXCR4 GENE; EPITHELIAL MESENCHYMAL TRANSITION; FOXC1 GENE; GENE; GENE EXPRESSION PROFILING; GENETIC HETEROGENEITY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; METASTASIS; MICROFLUIDICS; NPTN GENE; S100A4 GENE; S100A9 GENE; SINGLE CELL ANALYSIS; TGF BETA1 GENE; VIM GENE; ZEB2 GENE; BLOOD; BREAST TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; INSTRUMENTATION; LYMPHOMA; METABOLISM; METHODOLOGY; MICROARRAY ANALYSIS; MICROFLUIDIC ANALYSIS; TUMOR CELL LINE; TUMOR EMBOLISM;

BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHOMA; MICROARRAY ANALYSIS; MICROFLUIDIC ANALYTICAL TECHNIQUES; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; SINGLE-CELL ANALYSIS;

EID: 84860601923     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033788     Document Type: Article

References (62)

1. Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, et al. (2009) Tumor self-seeding by circulating cancer cells. Cell 139: 1315-1326.
2. Comen E, Norton L, Massague J, (2011) Clinical implications of cancer self-seeding. Nat Rev Clin Oncol 8: 369-377.
3. Niikura N, Liu J, Hayashi N, Mittendorf EA, Gong Y, et al. (2011) Loss of Human Epidermal Growth Factor Receptor 2 (HER2) Expression in Metastatic Sites of HER2-Overexpressing Primary Breast Tumors. J Clin Oncol. DOI 10.1200/JCO.2010.33.8889 [Epub ahead of print].
4. Dupont Jensen J, Laenkholm AV, Knoop A, Ewertz M, Bandaru R, et al. (2011) PIK3CA mutations may be discordant between primary and corresponding metastatic disease in breast cancer. Clinical Cancer Research 17: 667-677.
5. Pantel K, Brakenhoff RH, Brandt B, (2008) Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 8: 329-340.
6. Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, et al. (2004) Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res 10: 6897-6904.
7. van de Stolpe A, Pantel K, Sleijfer S, Terstappen LW, den Toonder JM, (2011) Circulating tumor cell isolation and diagnostics: toward routine clinical use. Cancer Res 71: 5955-5960.
8. Charbonneau H, Tonks NK, Walsh KA, Fischer EH, (1988) The leukocyte common antigen (CD45): a putative receptor-linked protein tyrosine phosphatase. Proc Natl Acad Sci U S A. 85: 7182-7186.
9. Nagrath S, Sequist LV, Maheswaran S, Bell DW, Irimia D, et al. (2007) Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature. 450: 1235-1239.
10. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, et al. (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351: 781-791.
11. Moreno JG, Miller MC, Gross S, Allard WJ, Gomella LG, et al. (2005) Circulating tumor cells predict survival in patients with metastatic prostate cancer. Urology 65: 713-718.
12. Cohen SJ, Punt CJ, Iannotti N, Saidman BH, Sabbath KD, et al. (2009) Prognostic significance of circulating tumor cells in patients with metastatic colorectal cancer. Ann Oncol 20: 1223-1229.
13. Krebs MG, Sloane R, Priest L, Lancashire L, Hou JM, et al. (2011) Evaluation and prognostic significance of circulating tumor cells in patients with non-small-cell lung cancer. J Clin Oncol 29: 1556-1563.
14. Smirnov DA, Zweitzig DR, Foulk BW, Miller MC, Doyle GV, et al. (2005) Global gene expression profiling of circulating tumor cells. Cancer Research 65: 4993-4997.
15. Sieuwerts AM, Kraan J, Bolt-de Vries J, van der Spoel P, Mostert B, et al. (2009) Molecular characterization of circulating tumor cells in large quantities of contaminating leukocytes by a multiplex real-time PCR. Breast Cancer Res Treat 118: 455-468.
16. Talasaz AH, Powell AA, Huber DE, Berbee JG, Roh KH, et al. (2009) Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proc Natl Acad Sci U S A 106: 3970-3975.
17. Ameri K, Luong R, Zhang H, Powell AA, Montgomery KD, et al. (2010) Circulating tumour cells demonstrate an altered response to hypoxia and an aggressive phenotype. Br J Cancer 102: 561-569.
18. Gupta GP, Minn AJ, Kang Y, Siegel PM, Serganova I, et al. (2005) Identifying site-specific metastasis genes and functions. Cold Spring Harb Symp Quant Biol 70: 149-158.
19. Dairkee SH, Nicolau M, Sayeed A, Champion S, Ji Y, et al. (2007) Oxidative stress pathways highlighted in tumor cell immortalization: association with breast cancer outcome. Oncogene 26: 6269-6279.
20. Dairkee SH, Sayeed A, Luciani G, Champion S, Meng Z, et al. (2009) Immutable functional attributes of histologic grade revealed by context-independent gene expression in primary breast cancer cells. Cancer Research 69: 7826-7834.
21. Luciani MG, Seok J, Sayeed A, Champion S, Goodson WH, et al. (2011) Distinctive responsiveness to stromal signaling accompanies histologic grade programming of cancer cells. PLoS One 6: e20016.
22. Dairkee SH, Ji Y, Ben Y, Moore DH, Meng Z, et al. (2004) A molecular 'signature' of primary breast cancer cultures; patterns resembling tumor tissue. BMC Genomics 5: 47.
23. Liu J, Hansen C, Quake SR, (2003) Solving the "world-to-chip" interface problem with a microfluidic matrix. Anal Chem 75: 4718-4723.
24. Spurgeon SL, Jones RC, Ramakrishnan R, (2008) High throughput gene expression measurement with real time PCR in a microfluidic dynamic array. PLoS One 3: e1662.
25. Popovici V, Goldstein DR, Antonov J, Jaggi R, Delorenzi M, et al. (2009) Selecting control genes for RT-QPCR using public microarray data. BMC Bioinformatics 10: 42.
26. Jeffrey SS, Lonning PE, Hillner BE, (2005) Genomics-based prognosis and therapeutic prediction in breast cancer. J Natl Compr Canc Netw 3: 291-300.
27. Lurje G, Lenz HJ, (2009) EGFR signaling and drug discovery. Oncology 77: 400-410.
28. Fischer EH, Charbonneau H, Tonks NK, (1991) Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes. Science 253: 401-406.
29. Kalisky T, Quake SR, (2011) Single-cell genomics. Nat Methods 8: 311-314.
30. Ignatiadis M, Georgoulias V, Mavroudis D, (2008) Micrometastatic disease in breast cancer: clinical implications. Eur J Cancer 44: 2726-2736.
31. Dairkee SH, Mayall BH, Smith HS, Hackett AJ, (1987) Monoclonal marker that predicts early recurrence of breast cancer. Lancet 1: 514.
32. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, et al. (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98: 10869-10874.
33. Watson MA, Ylagan LR, Trinkaus KM, Gillanders WE, Naughton MJ, et al. (2007) Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients. Clin Cancer Res 13: 5001-5009.
34. He H, Yang X, Davidson AJ, Wu D, Marshall FF, et al. (2010) Progressive epithelial to mesenchymal transitions in ARCaP E prostate cancer cells during xenograft tumor formation and metastasis. Prostate 70: 518-528.
35. Willipinski-Stapelfeldt B, Riethdorf S, Assmann V, Woelfle U, Rau T, et al. (2005) Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells. Clin Cancer Res 11: 8006-8014.
36. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, et al. (2009) Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 11: R46.
37. Wang D, Bodovitz S, (2010) Single cell analysis: the new frontier in 'omics'. Trends Biotechnol 28: 281-290.
38. Bosch A, Eroles P, Zaragoza R, Vina JR, Lluch A, (2010) Triple-negative breast cancer: Molecular features, pathogenesis, treatment and current lines of research. Cancer Treat Rev. 36: 206-215.
39. Korsching E, Jeffrey SS, Meinerz W, Decker T, Boecker W, et al. (2008) Basal carcinoma of the breast revisited: an old entity with new interpretations. J Clin Pathol 61: 553-560.
40. Meng S, Tripathy D, Shete S, Ashfaq R, Saboorian H, et al. (2006) uPAR and HER-2 gene status in individual breast cancer cells from blood and tissues. Proc Natl Acad Sci U S A 103: 17361-17365.
41. Wülfing P, Borchard J, Buerger H, Heidl S, Zänker KS, et al. (2006) HER2-positive circulating tumor cells indicate poor clinical outcome in stage I to III breast cancer patients. Clin Cancer Res 12: 1715-1720.
42. Fehm T, Becker S, Duerr-Stoerzer S, Sotlar K, Mueller V, et al. (2007) Determination of HER2 status using both serum HER2 levels and circulating tumor cells in patients with recurrent breast cancer whose primary tumor was HER2 negative or of unknown HER2 status. Breast Cancer Res 9: R74.
43. Pestrin M, Bessi S, Galardi F, Truglia M, Biggeri A, et al. (2009) Correlation of HER2 status between primary tumors and corresponding circulating tumor cells in advanced breast cancer patients. Breast Cancer Res Treat 118: 523-530.
44. Fehm T, Müller V, Aktas B, Janni W, Schneeweiss A, et al. (2010) HER2 status of circulating tumor cells in patients with metastatic breast cancer: a prospective, multicenter trial. Breast Cancer Res Treat 124: 403-412.
45. Aktas B, Müller V, Tewes M, Zeitz J, Kasimir-Bauer S, et al. (2011) Comparison of estrogen and progesterone receptor status of circulating tumor cells and the primary tumor in metastatic breast cancer patients. Gynecol Oncol 122: 356-360.
46. Strati A, Markou A, Parisi C, Politaki E, Mavroudis D, et al. (2011) Gene expression profile of circulating tumor cells in breast cancer by RT-qPCR. BMC Cancer 11: 422.
47. Patel AS, Allen JE, Dicker DT, Peters KL, Sheehan JM, et al. (2011) Identification and enumeration of circulating tumor cells in the cerebrospinal fluid of breast cancer patients with central nervous system metastases. Oncotarget 2: 752-760.
48. Giordano A, Giuliano M, De Laurentiis M, Arpino G, Jackson S, et al. (2011) Circulating tumor cells in immunohistochemical subtypes of metastatic breast cancer: lack of prediction in HER2-positive disease treated with targeted therapy. Ann Oncol DOI 10.1093/annonc/mdr434 [Epub ahead of print].
49. Kalluri R, Weinberg RA, (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428.
50. Polyak K, Weinberg RA, (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273.
51. Chua HL, Bhat-Nakshatri P, Clare SE, Morimiya A, Badve S, et al. (2007) NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 26: 711-724.
52. Bertran E, Caja L, Navarro E, Sancho P, Mainez J, et al. (2009) Role of CXCR4/SDF-1 alpha in the migratory phenotype of hepatoma cells that have undergone epithelial-mesenchymal transition in response to the transforming growth factor-beta. Cell Signal 21: 1595-1606.
53. Padua D, Massague J, (2009) Roles of TGFbeta in metastasis. Cell Res 19: 89-102.
54. Barcellos-Hoff MH, Akhurst RJ, (2009) Transforming growth factor-beta in breast cancer: too much, too late. Breast Cancer Res 11: 202.
55. Rodriguez-Pinto D, Sparkowski J, Keough MP, Phoenix KN, Vumbaca F, et al. (2009) Identification of novel tumor antigens with patient-derived immune-selected antibodies. Cancer Immunol Immunother 58: 221-234.
56. Boye K, Maelandsmo GM, (2010) S100A4 and metastasis: a small actor playing many roles. Am J Pathol 176: 528-535.
57. Thiery JP, (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
58. Chow JY, Dong H, Quach KT, Van Nguyen PN, Chen K, et al. (2008) TGF-beta mediates PTEN suppression and cell motility through calcium-dependent PKC-alpha activation in pancreatic cancer cells. Am J Physiol Gastrointest Liver Physiol 294: G899-905.
59. Chow JY, Quach KT, Cabrera BL, Cabral JA, Beck SE, et al. (2007) RAS/ERK modulates TGFbeta-regulated PTEN expression in human pancreatic adenocarcinoma cells. Carcinogenesis 28: 2321-2327.
60. Habib AA, Chatterjee S, Park SK, Ratan RR, Lefebvre S, et al. (2001) The epidermal growth factor receptor engages receptor interacting protein and nuclear factor-kappa B (NF-kappa B)-inducing kinase to activate NF-kappa B. Identification of a novel receptor-tyrosine kinase signalosome. J Biol Chem 276: 8865-8874.
61. Arai K, Takano S, Teratani T, Ito Y, Yamada T, et al. (2008) S100A8 and S100A9 overexpression is associated with poor pathological parameters in invasive ductal carcinoma of the breast. Curr Cancer Drug Targets 8: 243-252.
62. Courtney KD, Corcoran RB, Engelman JA, (2010) The PI3K pathway as drug target in human cancer. J Clin Oncol 28: 1075-1083.