Estimating the population abundance of tissue-infiltrating immune and stromal cell populations using gene expression

Genome Biology

Volumn 17, Issue 1, 2016, Pages

  Becht, Etienne ^a,b,c,d   Giraldo, Nicolas A ^a,b,c   Lacroix, Laetitia ^a,b,c   Buttard, Bénédicte ^a,b,c   Elarouci, Nabila ^d   Petitprez, Florent ^a,b,c,d   Selves, Janick ^e,f   Laurent Puig, Pierre ^g   Sautès Fridman, Catherine ^a,b,c   Fridman, Wolf H ^a,b,c   de Reyniès, Aurélien ^d  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d Programme Cartes d'Identite des Tumeurs   (France)

^e CANCER RESEARCH CENTER OF TOULOUSE   (France)

^f TOULOUSE UNIVERSITY HOSPITAL   (France)

^g INSERM   (France)

Author keywords

Deconvolution; Gene signatures; Transcriptomic markers; Tumor microenvironment

Indexed keywords

MESSENGER RNA; TRANSCRIPTOME; TUMOR MARKER;

ALGORITHM; ARTICLE; BREAST CANCER; CANCER SURVIVAL; CELL COUNT; CELL INFILTRATION; COLORECTAL CANCER; COMPUTER ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; EX VIVO STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTERMETHOD COMPARISON; LUNG ADENOCARCINOMA; QUANTITATIVE ANALYSIS; STROMA CELL; TRANSCRIPTOMICS; TUMOR MICROENVIRONMENT; VALIDITY; ADENOCARCINOMA; BIOLOGY; BIOSYNTHESIS; BREAST TUMOR; CELL TRACKING; COLORECTAL TUMOR; FEMALE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; LUNG TUMOR; PATHOLOGY; PROCEDURES;

ADENOCARCINOMA; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CELL TRACKING; COLORECTAL NEOPLASMS; COMPUTATIONAL BIOLOGY; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LUNG NEOPLASMS; RNA, MESSENGER; STROMAL CELLS; TRANSCRIPTOME; TUMOR MICROENVIRONMENT;

EID: 84992053166     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-016-1070-5     Document Type: Article

References (27)

1. Becht E, Giraldo NA, Germain C, de Reyniès A, Laurent-Puig P, Zucman-Rossi J, Dieu-Nosjean M, Sautès-Fridman C, Fridman WH. Immune contexture, immunoscore, and malignant cell molecular subgroups for prognostic and theranostic classifications of cancers. Adv Immunol. 2016;130:95-190.
2. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc P, Trajanoski Z, Fridman W, Galon J. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med. 2005;353:2654-66.
3. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoué F, Bruneval P, Cugnenc P, Trajanoski Z, Fridman W, Pagès F. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313:1960-4.
4. Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12:298-306.
5. Giraldo NA, Becht E, Pagès F, Skliris G, Verkarre V, Vano Y, Mejean A, Saint-Aubert N, Lacroix L, Natario I, Lupo A, Alifano M, Damotte D, Cazes A, Triebel F, Freeman GJ, Dieu-Nosjean M, Oudard S, Fridman WH, Sautès-Fridman C. Orchestration and prognostic significance of immune checkpoints in the microenvironment of primary and metastatic renal cell cancer. Clin Cancer Res. 2015;21:3031-40.
6. Isella C, Terrasi A, Bellomo SE, Petti C, Galatola G, Muratore A, Mellano A, Senetta R, Cassenti A, Sonetto C, Inghirami G, Trusolino L, Fekete Z, De Ridder M, Cassoni P, Storme G, Bertotti A, Medico E. Stromal contribution to the colorectal cancer transcriptome. Nat Genet. 2015;47:312-9.
7. Calon A, Lonardo E, Berenguer-Llergo A, Espinet E, Hernando-Momblona X, Iglesias M, Sevillano M, Palomo-Ponce S, Tauriello DVF, Byrom D, Cortina C, Morral C, Barceló C, Tosi S, Riera A, Attolini CS, Rossell D, Sancho E, Batlle E. Stromal gene expression defines poor-prognosis subtypes in colorectal cancer. Nat Genet. 2015;47:320-9.
8. Shen-Orr SS, Gaujoux R. Computational deconvolution: extracting cell type-specific information from heterogeneous samples. Curr Opin Immunol. 2013;25:571-8.
9. Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12:453-7.
10. Gong T, Szustakowski JD. DeconRNASeq: a statistical framework for deconvolution of heterogeneous tissue samples based on mRNA-Seq data. Bioinformatics. 2013;29:1083-5.
11. Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, Angell H, Fredriksen T, Lafontaine L, Berger A, Bruneval P, Fridman WH, Becker C, Pagès F, Speicher MR, Trajanoski Z, Galon J. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity. 2013;39:782-95.
12. Yoshihara K, Shahmoradgoli M, Martínez E, Vegesna R, Kim H, Torres-Garcia W, Treviño V, Shen H, Laird PW, Levine DA, Carter SL, Getz G, Stemke-Hale K, Mills GB, Verhaak RGW. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat Commun. 2013;4:2612.
13. McCall MN, Bolstad BM, Irizarry RA. Frozen robust multiarray analysis (fRMA). Biostatistics. 2010;11:242-53.
14. Lukk M, Kapushesky M, Nikkilä J, Parkinson H, Goncalves A, Huber W, Ukkonen E, Brazma A. A global map of human gene expression. Nat Biotechnol. 2010;28:322-4.
15. Fehrmann RSN, de Jonge HJM, Ter Elst A, de Vries A, Crijns AGP, Weidenaar AC, Gerbens F, de Jong S, van der Zee AGJ, de Vries EGE, Kamps WA, Hofstra RMW, Te Meerman GJ, de Bont ESJM. A new perspective on transcriptional system regulation (TSR): towards TSR profiling. PLoS One. 2008;3:e1656.
16. Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, Goc J, Lepelley A, Becht E, Katsahian S, Bizouard G, Validire P, Damotte D, Alifano M, Magdeleinat P, Cremer I, Teillaud J, Fridman W, Sautès-Fridman C, Dieu-Nosjean M. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am J Respir Crit Care Med. 2014;189:832-44.
17. Goc J, Germain C, Vo-Bourgais TKD, Lupo A, Klein C, Knockaert S, de Chaisemartin L, Ouakrim H, Becht E, Alifano M, Validire P, Remark R, Hammond SA, Cremer I, Damotte D, Fridman W, Sautès-Fridman C, Dieu-Nosjean M. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8+ T cells. Cancer Res. 2014;74:705-15.
18. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA, Rugo HS, Hwang ES, Jirström K, West BL, Coussens LM. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 2011;1:54-67.
19. Venet D, Pecasse F, Maenhaut C, Bersini H. Separation of samples into their constituents using gene expression data. Bioinformatics. 2001;17 Suppl 1:S279-87.
20. Li B, Li T, Pignon J, Wang B, Wang J, Shukla SA, Dou R, Chen Q, Hodi FS, Choueiri TK, Wu C, Hacohen N, Signoretti S, Liu JS, Liu XS. Landscape of tumor-infiltrating T cell repertoire of human cancers. Nat Genet. 2016;48:725-32.
21. Iglesia MD, Parker JS, Hoadley KA, Serody JS, Perou CM, Vincent BG. Genomic analysis of immune cell infiltrates across 11 tumor types. J Natl Cancer Inst. 2016;108.
22. Brown SD, Raeburn LA, Holt RA. Profiling tissue-resident T cell repertoires by RNA sequencing. Genome Med. 2015;7:125.
23. Sims D, Sudbery I, Ilott NE, Heger A, Ponting CP. Sequencing depth and coverage: key considerations in genomic analyses. Nat Rev Genet. 2014;15:121-32.
24. Andre F, Dieci MV, Dubsky P, Sotiriou C, Curigliano G, Denkert C, Loi S. Molecular pathways: involvement of immune pathways in the therapeutic response and outcome in breast cancer. Clin Cancer Res. 2013;19:28-33.
25. Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, Chen L, Pardoll DM, Topalian SL, Anders RA. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res. 2014;20:5064-74.
26. Dalman MR, Deeter A, Nimishakavi G, Duan Z. Fold change and p-value cutoffs significantly alter microarray interpretations. BMC Bioinf. 2012;13 Suppl 2:S11.
27. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest. 1973;52:2745-56.