In-depth tissue profiling using multiplexed immunohistochemical consecutive staining on single slide

Science Immunology

Volumn 1, Issue 1, 2016, Pages

  Remark, Romain ^a   Merghoub, Taha ^b   Grabe, Niels ^c   Litjens, Geert ^c   Damotte, Diane ^d,e   Wolchok, Jedd D ^b   Merad, Miriam ^a   Gnjatic, Sacha ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d CENTRE DE RECHERCHE DES CORDELIERS   (France)

^e AP HP ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85007330121     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aaf6925     Document Type: Article

References (34)

1. M. E. De Obaldia, A. Bhandoola, Transcriptional regulation of innate and adaptive lymphocyte lineages. Annu. Rev. Immunol. 33, 607–642 (2015).
2. H. Spits, T. Cupedo, Innate lymphoid cells: Emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 30, 647–675 (2012).
3. S. A. van de Pavert, R. E. Mebius, New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 10, 664–674 (2010).
4. W. H. Fridman, F. Pagès, C. Sautès-Fridman, J. Galon, The immune contexture in human tumours: Impact on clinical outcome. Nat. Rev. Cancer 12, 298–306 (2012).
5. S. Shalapour, M. Karin, Immunity, inflammation, and cancer: An eternal fight between good and evil. J. Clin. Invest. 125, 3347–3355 (2015).
6. J. Galon, A. Costes, F. Sanchez-Cabo, A. Kirilovsky, B. Mlecnik, C. Lagorce-Pagès, M. Tosolini, M. Camus, A. Berger, P. Wind, F. Zinzindohoué, P. Bruneval, P.-H. Cugnenc, Z. Trajanoski, W.-H. Fridman, F. Pagès, Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960–1964 (2006).
7. W. H. Fridman, R. Remark, J. Goc, N. A. Giraldo, E. Becht, S. A. Hammond, D. Damotte, M.-C. Dieu-Nosjean, C. Sautès-Fridman, The immune microenvironment: A major player in human cancers. Int. Arch. Allergy Immunol. 164, 13–26 (2014).
8. J. Galon, H. K. Angell, D. Bedognetti, F. M. Marincola, The continuum of cancer immunosurveillance: Prognostic, predictive, and mechanistic signatures. Immunity 39, 11–26 (2013).
9. J. Galon, F. Pagès, F. M. Marincola, H. K. Angell, M. Thurin, A. Lugli, I. Zlobec, A. Berger, C. Bifulco, G. Botti, F. Tatangelo, C. M. Britten, S. Kreiter, L. Chouchane, P. Delrio, H. Arndt, M. Asslaber, M. Maio, G. V. Masucci, M. Mihm, F. Vidal-Vanaclocha, J. P. Allison, S. Gnjatic, L. Hakansson, C. Huber, H. Singh-Jasuja, C. Ottensmeier, H. Zwierzina, L. Laghi, F. Grizzi, P. S. Ohashi, P. A. Shaw, B. A. Clarke, B. G. Wouters, Y. Kawakami, S. Hazama, K. Okuno, E. Wang, J. O’Donnell-Tormey, C. Lagorce, G. Pawelec, M. I. Nishimura, R. Hawkins, R. Lapointe, A. Lundqvist, S. N. Khleif, S. Ogino, P. Gibbs, P. Waring, N. Sato, T. Torigoe, K. Itoh, P. S. Patel, S. N. Shukla, R. Palmqvist, I. D. Nagtegaal, Y. Wang, C. D’Arrigo, S. Kopetz, F. A. Sinicrope, G. Trinchieri, T. F. Gajewski, P. A. Ascierto, B. A. Fox, Cancer classification using the Immunoscore: A worldwide task force. J. Transl. Med. 10, 205 (2012).
10. + T cells. Cancer Res. 74, 705–715 (2014).
11. R. Remark, M. Alifano, I. Cremer, A. Lupo, M.-C. Dieu-Nosjean, M. Riquet, L. Crozet, H. Ouakrim, J. Goc, A. Cazes, J.-F. Fléjou, L. Gibault, V. Verkarre, J.-F. Régnard, O.-N. Pagès, S. Oudard, B. Mlecnik, C. Sautès-Fridman, W.-H. Fridman, D. Damotte, Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: Influence of tumor origin. Clin. Cancer Res. 19, 4079–4091 (2013).
12. R. Remark, C. Becker, J. E. Gomez, D. Damotte, M.-C. Dieu-Nosjean, C. Sautès-Fridman, W.-H. Fridman, C. A. Powell, N. K. Altorki, M. Merad, S. Gnjatic, The non-small cell lung cancer immune contexture. A major determinant of tumor characteristics and patient outcome. Am. J. Respir. Crit. Care Med. 191, 377–390 (2015).
13. D. M. Pardoll, The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12, 252–264 (2012).
14. D. B. Page, M. A. Postow, M. K. Callahan, J. P. Allison, J. D. Wolchok, Immune modulation in cancer with antibodies. Annu. Rev. Med. 65, 185–202 (2014).
15. R. S. Herbst, J.-C. Soria, M. Kowanetz, G. D. Fine, O. Hamid, M. S. Gordon, J. A. Sosman, D. F. McDermott, J. D. Powderly, S. N. Gettinger, H. E. K. Kohrt, L. Horn, D. P. Lawrence, S. Rost, M. Leabman, Y. Xiao, A. Mokatrin, H. Koeppen, P. S. Hegde, I. Mellman, D. S. Chen, F. S. Hodi, Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515, 563–567 (2014).
16. P. C. Tumeh, C. L. Harview, J. H. Yearley, I. P. Shintaku, E. J. M. Taylor, L. Robert, B. Chmielowski, M. Spasic, G. Henry, V. Ciobanu, A. N. West, M. Carmona, C. Kivork, E. Seja, G. Cherry, A. J. Gutierrez, T. R. Grogan, C. Mateus, G. Tomasic, J. A. Glaspy, R. O. Emerson, H. Robins, R. H. Pierce, D. A. Elashoff, C. Robert, A. Ribas, PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515, 568–571 (2014).
17. J. D. Wolchok, T. A. Chan, Cancer: Antitumour immunity gets a boost. Nature 515, 496–498 (2014).
18. D. Robertson, K. Savage, J. S. Reis-Filho, C. M. Isacke, Multiple immunofluorescence labelling of formalin-fixed paraffin-embedded (FFPE) tissue. BMC Cell Biol. 9, 13 (2008).
19. C. Giesen, H. A. O. Wang, D. Schapiro, N. Zivanovic, A. Jacobs, B. Hattendorf, P. J. Schüffler, D. Grolimund, J. M. Buhmann, S. Brandt, Z. Varga, P. J. Wild, D. Günther, B. Bodenmiller, Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat. Methods 11, 417–422 (2014).
20. M. J. Gerdes, C. J. Sevinsky, A. Sood, S. Adak, M. O. Bello, A. Bordwell, A. Can, A. Corwin, S. Dinn, R. J. Filkins, D. Hollman, V. Kamath, S. Kaanumalle, K. Kenny, M. Larsen, M. Lazare, Q. Li, C. Lowes, C. C. McCulloch, E. McDonough, M. C. Montalto, Z. Pang, J. Rittscher, A. Santamaria-Pang, B. D. Sarachan, M. L. Seel, A. Seppo, K. Shaikh, Y. Sui, J. Zhang, F. Ginty, Highly multiplexed single-cell analysis of formalin-fixed, paraffin-embedded cancer tissue. Proc. Natl. Acad. Sci. U.S.A. 110, 11982–11987 (2013).
21. E. C. Stack, C. Wang, K. A. Roman, C. C. Hoyt, Multiplexed immunohistochemistry, imaging, and quantitation: A review, with an assessment of Tyramide signal amplification, multispectral imaging and multiplex analysis. Methods 70, 46–58 (2014).
22. M. Angelo, S. C. Bendall, R. Finck, M. B. Hale, C. Hitzman, A. D. Borowsky, R. M. Levenson, J. B. Lowe, S. D. Liu, S. Zhao, Y. Natkunam, G. P. Nolan, Multiplexed ion beam imaging of human breast tumors. Nat. Med. 20, 436–442 (2014).
23. A. M. Lesokhin, M. K. Callahan, M. A. Postow, J. D. Wolchok, On being less tolerant: Enhanced cancer immunosurveillance enabled by targeting checkpoints and agonists of T cell activation. Sci. Transl. Med. 7, 280sr1 (2015).
24. M. A. Postow, J. Chesney, A. C. Pavlick, C. Robert, K. Grossmann, D. McDermott, G. P. Linette, N. Meyer, J. K. Giguere, S. S. Agarwala, M. Shaheen, M. S. Ernstoff, D. Minor, A. K. Salama, M. Taylor, P. A. Ott, L. M. Rollin, C. Horak, P. Gagnier, J. D. Wolchok, F. S. Hodi, Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N. Engl. J. Med. 372, 2006–2017 (2015).
25. P. Sharma, J. P. Allison, The future of immune checkpoint therapy. Science 348, 56–61 (2015).
26. L. M. McShane, D. G. Altman, W. Sauerbrei, S. E. Taube, M. Gion, G. M. Clark; Statistics Subcommittee of the NCI-EORTC Working Group on Cancer Diagnostics, Reporting recommendations for tumor marker prognostic studies. J. Clin. Oncol. 23, 9067–9072 (2005).
27. M.-G. Anitei, G. Zeitoun, B. Mlecnik, F. Marliot, N. Haicheur, A.-M. Todosi, A. Kirilovsky, C. Lagorce, G. Bindea, D. Ferariu, M. Danciu, P. Bruneval, V. Scripcariu, J.-M. Chevallier, F. Zinzindohoué, A. Berger, J. Galon, F. Pagès, Prognostic and predictive values of the immunoscore in patients with rectal cancer. Clin. Cancer Res. 20, 1891–1899 (2014).
28. T. R. Jones, I. H. Kang, D. B. Wheeler, R. A. Lindquist, A. Papallo, D. M. Sabatini, P. Golland, A. E. Carpenter, CellProfiler Analyst: Data exploration and analysis software for complex image-based screens. BMC Bioinformatics 9, 482 (2008).
29. S. Klein, M. Staring, K. Murphy, M. A. Viergever, J. P. W. Pluim, elastix: A toolbox for intensity-based medical image registration. IEEE Trans. Med. Imaging 29, 196–205 (2010).
30. D. Mueller, D. Vossen, B. Hulsken, Real-time deformable registration of multi-modal whole slides for digital pathology. Comput. Med. Imaging Graph. 35, 542–556 (2011).
31. Y. LeCun, Y. Bengio, G. Hinton, Deep learning. Nature 521, 436–444 (2015).
32. D. C. Cireşan, A. Giusti, L. M. Gambardella, J. Schmidhuber, Mitosis detection in breast cancer histology images with deep neural networks. Med. Image Comput. Comput. Assist. Interv. 16, 411–418 (2013).
33. G. Loy, A. Zelinsky, Fast radial symmetry for detecting points of interest. IEEE Trans. Pattern Anal. Mach. Intell. 25, 959–973 (2003).
34. D. A. Schoenfeld, Sample-size formula for the proportional-hazards regression model. Biometrics 39, 499–503 (1983).