Evaluation and validation of a robust single cell RNA-amplification protocol through transcriptional profiling of enriched lung cancer initiating cells

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Rothwell, Dominic G ^a   Li, Yaoyong ^a   Ayub, Mahmood ^a   Tate, Catriona ^a   Newton, Gillian ^a   Hey, Yvonne ^a   Carter, Louise ^a   Faulkner, Suzanne ^a   Moro, Massimo ^b   Pepper, Stuart ^a   Miller, Crispin ^a   Blackhall, Fiona ^c   Bertolini, Giulia ^b   Roz, Luca ^b   Dive, Caroline ^a   Brady, Ged ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b NATIONAL CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cancer initiating cell; Microarray; RNA Amplification; RNA Seq; Single cell; Transcriptional profiling

Indexed keywords

COMPLEMENTARY DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER INITIATING CELL; CANCER STEM CELL; CELL LINE; CELL SUBPOPULATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIAGNOSTIC KIT; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FEMALE; GENE AMPLIFICATION; HUMAN; HUMAN CELL; INTERMETHOD COMPARISON; MCF 7 CELL LINE; MCF10A CELL LINE; METASTASIS; MICROARRAY ANALYSIS; MOUSE; NEXT GENERATION SEQUENCING; NON SMALL CELL LUNG CANCER; NONHUMAN; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SINGLE CELL ANALYSIS; SINGLE CELL RNA AMPLIFICATION; TRANSCRIPTOMICS; TUMOR XENOGRAFT; DNA MICROARRAY; EVALUATION STUDY; GENE EXPRESSION PROFILING; LUNG; METABOLISM; NUCLEIC ACID AMPLIFICATION; PATHOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; SEQUENCE ANALYSIS; TUMOR CELL LINE; VALIDATION STUDY;

CELL LINE, TUMOR; GENE EXPRESSION PROFILING; HUMANS; LUNG; NEOPLASTIC STEM CELLS; NUCLEIC ACID AMPLIFICATION TECHNIQUES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS;

EID: 84924283950     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1129     Document Type: Article

References (54)

1. Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, Xu N, Wang X, Bodeau J, Tuch BB, Siddiqui A, Lao K, Surani MA: mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 2009,6(5):377-382. 10.1038/nmeth.1315
2. Picelli S, Bjorklund AK, Faridani OR, Sagasser S, Winberg G, Sandberg R: Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat Methods 2013,10(11):1096-1098. 10.1038/nmeth.2639
3. Hartmann CH, Klein CA: Gene expression profiling of single cells on large-scale oligonucleotide arrays. Nucleic Acids Res 2006, 34:e143. 10.1093/nar/gkl740
4. Klein CA, Seidl S, Petat-Dutter K, Offner S, Geigl JB, Schmidt-Kittler O, Wendler N, Passlick B, Huber RM, Schlimok G, Baeuerle PA, Riethmüller G: Combined transcriptome and genome analysis of single micrometastatic cells. Nat Biotechnol 2002, 20:387-392. 10.1038/nbt0402-387
5. Brady G, Barbara M, Iscove NN: Representative in vitro amplification from individual hemopoietic cells and colonies. Methods Mol Cell Biol 1990, 2:17-25.
6. Ali MM, Li F, Zhang Z, Zhang K, Kang DK, Ankrum JA, Le XC, Zhao W: Rolling circle amplification: a versatile tool for chemical biology, materials science and medicine. Chem Soc Rev 2014,43(10):3324-3341. 10.1039/c3cs60439j
7. Ramskold D, Luo S, Wang YC, Li R, Deng Q, Faridani OR, Daniels GA, Khrebtukova I, Loring JF, Laurent LC, Schroth GP, Sandberg R: Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat Biotechnol 2012,30(8):777-782. 10.1038/nbt.2282
8. Kawasaki ES: Microarrays and the gene expression profile of a single cell. Ann N Y Acad Sci 2004, 1020:2-100.
9. Schena M, Shalon D, Davis RW, Brown PO: Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 1995,270(5235):467-470. 10.1126/science.270.5235.467
10. DeRisi J, Penland L, Brown PO, Bittner ML, Meltzer PS, Ray M, Chen Y, Su YA, Trent JM: Use of a cDNA microarray to analyse gene expression patterns in human cancer. Nat Genet 1996,14(4):457-460.
11. Wang Z, Gerstein M, Snyder M: RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009,10(1):57-63. 10.1038/nrg2484
12. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008,5(7):621-628. 10.1038/nmeth.1226
13. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010,28(5):511-515. 10.1038/nbt.1621
14. Murphy J, Bustin SA: Reliability of real-time reverse-transcription PCR in clinical diagnostics: gold standard or substandard? Expert Rev Mol Diagn 2009, 9:187-197. 10.1586/14737159.9.2.187
15. Krebs MG, Hou JM, Ward TH, Blackhall FH, Dive C: Circulating tumour cells: their utility in cancer management and predicting outcomes. Ther Adv Med Oncol 2010,2(6):351-365. 10.1177/1758834010378414
16. Visvader JE, Lindeman GJ: Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008, 8:755-768. 10.1038/nrc2499
17. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM: Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006, 66:9339-9344. 10.1158/0008-5472.CAN-06-3126
18. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T: Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer 2005, 5:744-749. 10.1038/nrc1694
19. Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, Tinelli S, Roz E, Caserini R, Lo Vullo S, Camerini T, Mariani L, Delia D, Calabrò E, Pastorino U, Sozzi G: Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci U S A 2009, 106:16281-16286. 10.1073/pnas.0905653106
20. Bertolini G, Moro M, Tortoreto M, Caserini R, Pastorino U, Roz L, Sozzi G: The subset of CD133+/CXCR4+/EpCAM- cancer initiating cells is responsible for lung tumor metastatic spreading [abstract]. Eur J Cancer 2012,48(Supplement: 5):S90-S90. 372
21. Loboda A, Nebozhyn MV, Watters JW, Buser CA, Shaw PM, Huang PS, Van't VL, Tollenaar RA, Jackson DB, Agrawal D, Dai H, Yeatman TJ: EMT is the dominant program in human colon cancer. BMC Med Genomics 2011, 4:9. 10.1186/1755-8794-4-9
22. Blick T, Hugo H, Widodo E, Waltham M, Pinto C, Mani SA, Weinberg RA, Neve RM, Lenburg ME, Thompson EW: Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia 2010, 15:235-252. 10.1007/s10911-010-9175-z
23. Bitton DA, Okoniewski MJ, Connolly Y, Miller CJ: Exon level integration of proteomics and microarray data. BMC Bioinformatics 2008, 9:118. 10.1186/1471-2105-9-118
24. Jiao X, Sherman BT, da Huang W, Stephens R, Baseler MW, Lane HC, Lempicki RA: DAVID-WS: a stateful web service to facilitate gene/protein list analysis. Bioinformatics 2012,28(13):1805-1806. 10.1093/bioinformatics/bts251
25. Culhane AC, Schroder MS, Sultana R, Picard SC, Martinelli EN, Kelly C, Haibe-Kains B, Kapushesky M, St Pierre AA, Flahive W, Picard KC, Gusenleitner D, Papenhausen G, O'Connor N, Correll M, Quackenbush J: GeneSigDB: a manually curated database and resource for analysis of gene expression signatures. Nucleic Acids Res 2012, 40:D1060-D1066. 10.1093/nar/gkr901
26. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J: Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80
27. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, Hartwell K, Onder TT, Gupta PB, Evans KW, Hollier BG, Ram PT, Lander ES, Rosen JM, Weinberg RA, Mani SA: Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci U S A 2010, 107:15449-15454. 10.1073/pnas.1004900107
28. Belyavsky A, Vinogradova T, Rajewsky K: PCR-based cDNA library construction: general cDNA libraries at the level of a few cells. Nucleic Acids Res 1989, 17:2919-2932. 10.1093/nar/17.8.2919
29. Eberwine J, Yeh H, Miyashiro K, Cao Y, Nair S, Finnell R, Zettel M, Coleman P: Analysis of gene expression in single live neurons. Proc Natl Acad Sci U S A 1992, 89:3010-3014. 10.1073/pnas.89.7.3010
30. Cumano A, Paige CJ, Iscove NN, Brady G: Bipotential precursors of B cells and macrophages in murine fetal liver. Nature 1992, 356:612-615. 10.1038/356612a0
31. Dulac C, Axel R: A novel family of genes encoding putative pheromone receptors in mammals. Cell 1995, 83:195-206. 10.1016/0092-8674(95)90161-2
32. Tang F, Lao K, Surani MA: Development and applications of single-cell transcriptome analysis. Nat Methods 2011, 8:S6-S11. 10.1038/nchembio.740
33. Alix-Panabieres C, Pantel K: Circulating tumor cells: liquid biopsy of cancer. Clin Chem 2013, 59:110-118. 10.1373/clinchem.2012.194258
34. Pantel K, Brakenhoff RH, Brandt B: Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 2008, 8:329-340. 10.1038/nrc2375
35. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA: The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027
36. Polyak K, Weinberg RA: Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9:265-273. 10.1038/nrc2620
37. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S: Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 2009, 11:R46. 10.1186/bcr2333
38. Balic M, Lin H, Young L, Hawes D, Giuliano A, McNamara G, Datar RH, Cote RJ: Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 2006, 12:5615-5621. 10.1158/1078-0432.CCR-06-0169
39. Baccelli I, Schneeweiss A, Riethdorf S, Stenzinger A, Schillert A, Vogel V, Klein C, Saini M, Bauerle T, Wallwiener M, Holland-Letz T, Höfner T, Sprick M, Scharpff M, Marmé F, Sinn HP, Pantel K, Weichert W, Trumpp A: Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat Biotechnol 2013, 31:539-544. 10.1038/nbt.2576
40. Zhang L, Ridgway LD, Wetzel MD, Ngo J, Yin W, Kumar D, Goodman JC, Groves MD, Marchetti D: The identification and characterization of breast cancer CTCs competent for brain metastasis. Sci Transl Med 2013, 5:180ra48.
41. Sekine I, Minna JD, Nishio K, Tamura T, Saijo N: A literature review of molecular markers predictive of clinical response to cytotoxic chemotherapy in patients with lung cancer. J Thorac Oncol 2006, 1:31-37. 10.1097/01243894-200601000-00008
42. Nakanishi Y, Kawasaki M, Bai F, Takayama K, Pei XH, Takano K, Inoue K, Osaki S, Hara N, Kiyohara C: Expression of p53 and glutathione S-transferase-pi relates to clinical drug resistance in non-small cell lung cancer. Oncology 1999, 57:318-323. 10.1159/000012068
43. Smalley MJ, Reis-Filho JS, Ashworth A: BRCA1 and stem cells: tumour typecasting. Nat Cell Biol 2008, 10:377-379. 10.1038/ncb0408-377
44. Buckley NE, Mullan PB: BRCA1-conductor of the breast stem cell orchestra: the role of BRCA1 in mammary gland development and identification of cell of origin of BRCA1 mutant breast cancer. Stem Cell Rev 2012, 8:982-993. 10.1007/s12015-012-9354-y
45. Sotiropoulou PA, Karambelas AE, Debaugnies M, Candi A, Bouwman P, Moers V, Revenco T, Rocha AS, Sekiguchi K, Jonkers J, Blanpain C: BRCA1 deficiency in skin epidermis leads to selective loss of hair follicle stem cells and their progeny. Genes Dev 2013, 27:39-51. 10.1101/gad.206573.112
46. Moro M, Bertolini G, Tortoreto M, Pastorino U, Sozzi G, Roz L: Patient-derived xenografts of non-small cell lung cancer: resurgence of an old model for investigation of modern concepts of tailored therapy and cancer stem cells. J Biomed Biotechnol 2012, 2012:1-11.
47. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistisc 2003, 4:249-264. 10.1093/biostatistics/4.2.249
48. Yates T, Okoniewski MJ, Miller CJ: X:Map: annotation and visualization of genome structure for Affymetrix exon array analysis. Nucleic Acids Res 2008, 36:D780-D786.
49. Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article 3.
50. Smyth GK: LIMMA: Linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor. Edited by: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W. New York: Springer; 2005:397-420.
51. Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Bio 2009, 10:R25. 10.1186/gb-2009-10-3-r25
52. David M, Dzamba M, Lister D, Ilie L, Brudno M: SHRiMP2: sensitive yet practical SHort Read Mapping. Bioinformatics 2011, 27:1011-1012. 10.1093/bioinformatics/btr046
53. Robinson MD, McCarthy DJ, Smyth GK: edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140. 10.1093/bioinformatics/btp616
54. Robinson MD, Smyth GK: Moderated statistical tests for assessing differences in tag abundance. Bioinformatics 2007, 23:2881-2887. 10.1093/bioinformatics/btm453