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Cell-of-Origin Patterns Dominate the Molecular Classification of 10,000 Tumors from 33 Types of Cancer
Open accessAbstract
We conducted comprehensive integrative molecular analyses of the complete set of tumors in The Cancer Genome Atlas (TCGA), consisting of approximately 10,000 specimens and representing 33 types of cancer. We performed molecular clustering using data on chromosome-arm-level aneuploidy, DNA hypermethylation, mRNA, and miRNA expression levels and reverse-phase protein arrays, of which all, except for aneuploidy, revealed clustering primarily organized by histology, tissue type, or anatomic origin. The influence of cell type was evident in DNA-methylation-based clustering, even after excluding sites with known preexisting tissue-type-specific methylation. Integrative clustering further emphasized the dominant role of cell-of-origin patterns. Molecular similarities among histologically or anatomically related cancer types provide a basis for focused pan-cancer analyses, such as pan-gastrointestinal, pan-gynecological, pan-kidney, and pan-squamous cancers, and those related by stemness features, which in turn may inform strategies for future therapeutic development.
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“The nature of these mutations differs for each cancer [90] and in each individual [90,91,92].”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [92]
Experimental — accuracy not yet measuredIn the citing paper
“First, although tumors are readily recognized through gene expression signatures, they retain transcriptomic features of the parental tissue so that tumors arising in the same organ are more similar to each other than tumors arising in different organs.”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [3]
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“A study that classified thousands of human tumors found that tissue of origin was a major factor defining DNA methylation and gene expression patterns (3).”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [3]
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Self-citationLeveraging big data of immune checkpoint blockade response identifies novel potential targets
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“While pan-cancer classification and prediction using transcriptomic data have been successfully applied for identification of biomarkers and of cancer subtypes as well as for prediction of disease progression [66 – 68], clinical cancer treatment options are often in part guided by oncomutations.”
BackgroundPredicting master transcription factors from pan-cancer expression data
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Self-citationThe Project Baseline Health Study: a step towards a broader mission to map human health
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A multimodal graph neural network framework for cancer molecular subtype classification
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“The first is cancer molecular subtype classification on the TCGA Pan-cancer dataset and the second is breast cancer subtype classification on the TCGA breast invasive carcinoma (BRCA) dataset [15, 30].”
BackgroundMethodA census of pathway maps in cancer systems biology
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Self-citationDetection and relevance of epigenetic markers on ctDNA: recent advances and future outlook
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Cell-type heterogeneity: Why we should adjust for it in epigenome and biomarker studies
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Metadata
- Authors
- Hoadley, K. A., Yau, C., Hinoue, T., Wolf, D. M., Lazar, A. J., Drill, E., Shen, R., Taylor, A. M., Cherniack, A. D., Thorsson, V., Akbani, R., Bowlby, R., Wong, C. K., Wiznerowicz, M., Sanchez-Vega, F., Robertson, A. G., Schneider, B. G., Lawrence, M. S., Noushmehr, H., Malta, T. M., Caesar-Johnson, S. J., Demchok, J. A., Felau, I., Kasapi, M., Ferguson, M. L., Hutter, C. M., Sofia, H. J., Tarnuzzer, R., Wang, Z., Yang, L., Zenklusen, J. C., Zhang, J. (., Chudamani, S., Liu, J., Lolla, L., Naresh, R., Pihl, T., Sun, Q., Wan, Y., Wu, Y., Cho, J., DeFreitas, T., Frazer, S., Gehlenborg, N., Getz, G., Heiman, D. I., Kim, J., Lawrence, M. S., Lin, P., Meier, S., Noble, M. S., Saksena, G., Voet, D., Zhang, H., Bernard, B., Chambwe, N., Dhankani, V., Knijnenburg, T., Kramer, R., Leinonen, K., Liu, Y., Miller, M., Reynolds, S., Shmulevich, I., Thorsson, V., Zhang, W., Akbani, R., Broom, B. M., Hegde, A. M., Ju, Z., Kanchi, R. S., Korkut, A., Li, J., Liang, H., Ling, S., Liu, W., Lu, Y., Mills, G. B., Ng, K.-S., Rao, A., Ryan, M., Wang, J., Weinstein, J. N., Zhang, J., Abeshouse, A., Armenia, J., Chakravarty, D., Chatila, W. K., de Bruijn, I., Gao, J., Gross, B. E., Heins, Z. J., Kundra, R., La, K., Ladanyi, M., Luna, A., Nissan, M. G., Ochoa, A., Phillips, S. M., Reznik, E., Sanchez-Vega, F., Sander, C., Schultz, N., Sheridan, R., Sumer, S. O., Sun, Y., Taylor, B. S., Wang, J., Zhang, H., Anur, P., Peto, M., Spellman, P., Benz, C., Stuart, J. M., Wong, C. K., Yau, C., Hayes, D. N., Parker, J. S., Wilkerson, M. D., Ally, A., Balasundaram, M., Bowlby, R., Brooks, D., Carlsen, R., Chuah, E., Dhalla, N., Holt, R., Jones, S. J. M., Kasaian, K., Lee, D., Ma, Y., Marra, M. A., Mayo, M., Moore, R. A., Mungall, A. J., Mungall, K., Robertson, A. G., Sadeghi, S., Schein, J. E., Sipahimalani, P., Tam, A., Thiessen, N., Tse, K., Wong, T., Berger, A. C., Beroukhim, R., Cherniack, A. D., Cibulskis, C., Gabriel, S. B., Gao, G. F., Ha, G., Meyerson, M., Schumacher, S. E., Shih, J., Kucherlapati, M. H., Kucherlapati, R. S., Baylin, S., Cope, L., Danilova, L., Bootwalla, M. S., Lai, P. H., Maglinte, D. T., Van Den Berg, D. J., Weisenberger, D. J., Auman, J. T., Balu, S., Bodenheimer, T., Fan, C., Hoadley, K. A., Hoyle, A. P., Jefferys, S. R., Jones, C. D., Meng, S., Mieczkowski, P. A., Mose, L. E., Perou, A. H., Perou, C. M., Roach, J., Shi, Y., Simons, J. V., Skelly, T., Soloway, M. G., Tan, D., Veluvolu, U., Fan, H., Hinoue, T., Laird, P. W., Shen, H., Zhou, W., Bellair, M., Chang, K., Covington, K., Creighton, C. J., Dinh, H., Doddapaneni, H., Donehower, L. A., Drummond, J., Gibbs, R. A., Glenn, R., Hale, W., Han, Y., Hu, J., Korchina, V., Lee, S., Lewis, L., Li, W., Liu, X., Morgan, M., Morton, D., Muzny, D., Santibanez, J., Sheth, M., Shinbrot, E., Wang, L., Wang, M., Wheeler, D. A., Xi, L., Zhao, F., Hess, J., Appelbaum, E. L., Bailey, M., Cordes, M. G., Ding, L., Fronick, C. C., Fulton, L. 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V., Broudy, T., Mirsaidi, C., Nair, P., Drwiega, P., Miller, J., Smith, J., Zaren, H., Park, J.-W., Hung, N. P., Kebebew, E., Linehan, W. M., Metwalli, A. R., Pacak, K., Pinto, P. A., Schiffman, M., Schmidt, L. S., Vocke, C. D., Wentzensen, N., Worrell, R., Yang, H., Moncrieff, M., Goparaju, C., Melamed, J., Pass, H., Botnariuc, N., Caraman, I., Cernat, M., Chemencedji, I., Clipca, A., Doruc, S., Gorincioi, G., Mura, S., Pirtac, M., Stancul, I., Tcaciuc, D., Albert, M., Alexopoulou, I., Arnaout, A., Bartlett, J., Engel, J., Gilbert, S., Parfitt, J., Sekhon, H., Thomas, G., Rassl, D. M., Rintoul, R. C., Bifulco, C., Tamakawa, R., Urba, W., Hayward, N., Timmers, H., Antenucci, A., Facciolo, F., Grazi, G., Marino, M., Merola, R., de Krijger, R., Gimenez-Roqueplo, A.-P., Piché, A., Chevalier, S., McKercher, G., Birsoy, K., Barnett, G., Brewer, C., Farver, C., Naska, T., Pennell, N. A., Raymond, D., Schilero, C., Smolenski, K., Williams, F., Morrison, C., Borgia, J. A., Liptay, M. 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- Affiliations
- University of California, San Francisco (US)
- Memorial Sloan Kettering Cancer Center (US)
- Broad Institute (US)
- Vanderbilt University Medical Center (US)
- Henry Ford Health (US)
- Buck Institute for Research on Aging (US)
- Van Andel Institute (US)
- BC Cancer Agency (CA)
- Institute for Systems Biology (US)
- The University of Texas MD Anderson Cancer Center (US)
- University of California, Santa Cruz (US)
- University of North Carolina at Chapel Hill (US)
- Poznan University of Medical Sciences (PL)
- Corresponding author
- Felau, Ina
- Nissan, Moriah G.
- Weisenberger, Daniel J.
- Jones, Corbin D.
- Bellair, Michelle
- Mallery, David
- Oosterhuis, Wolter
- Kefford, Richard
- Vocke, Cathy D.
- Zuna, Rosemary
- Rubin, Mark A.
- Aredes, Natália D.
- ORCID
- Wolf, Denise M.
- Drill, Esther
- Shen, Ronglai
- Taylor, Alison M.
- Schneider, Barbara G.
- Malta, Tathiane M.
- Felau, Ina
- Kasapi, Melpomeni
- Ferguson, Martin L.
- Sofia, Heidi J.
- Tarnuzzer, Roy
- Yang, Liming
- Zenklusen, Jean C.
- Zhang, Jiashan (Julia)
- Liu, Jia
- Pihl, Todd
- Sun, Qiang
- Wu, Ye
- Gehlenborg, Nils
- Getz, Gad
- Heiman, David I.
- Kim, Jaegil
- Lin, Pei
- Noble, Michael S.
- Saksena, Gordon
- Zhang, Hailei
- Bernard, Brady
- Chambwe, Nyasha
- Knijnenburg, Theo
- Liu, Yuexin
- Miller, Michael
- Shmulevich, Ilya
- Zhang, Wei
- Broom, Bradley M.
- Hegde, Apurva M.
- Ju, Zhenlin
- Korkut, Anil
- Li, Jun
- Liang, Han
- Lu, Yiling
- Mills, Gordon B.
- Wang, Jing
- Weinstein, John N.
- Zhang, Jiexin
- Armenia, Joshua
- Chakravarty, Debyani
- Chatila, Walid K.
- Gross, Benjamin E.
- Heins, Zachary J.
- Kundra, Ritika
- Ladanyi, Marc
- Luna, Augustin
- Ochoa, Angelica
- Phillips, Sarah M.
- Reznik, Ed
- Sander, Chris
- Schultz, Nikolaus
- Sun, Yichao
- Taylor, Barry S.
- Zhang, Hongxin
- Spellman, Paul
- Hayes, D. Neil
- Parker, Joel S.
- Wilkerson, Matthew D.
- Holt, Robert
- Jones, Steven J.M.
- Marra, Marco A.
- Moore, Richard A.
- Mungall, Andrew J.
- Sadeghi, Sara
- Tam, Angela
- Wong, Tina
- Berger, Ashton C.
- Beroukhim, Rameen
- Cibulskis, Carrie
- Gabriel, Stacey B.
- Ha, Gavin
- Meyerson, Matthew
- Schumacher, Steven E.
- Shih, Juliann
- Kucherlapati, Melanie H.
- Kucherlapati, Raju S.
- Baylin, Stephen
- Cope, Leslie
- Danilova, Ludmila
- Maglinte, Dennis T.
- Weisenberger, Daniel J.
- Auman, J. Todd
- Hoyle, Alan P.
- Jones, Corbin D.
- Mieczkowski, Piotr A.
- Perou, Charles M.
- Roach, Jeffrey
- Shi, Yan
- Fan, Huihui
- Shen, Hui
- Zhou, Wanding
- Chang, Kyle
- Covington, Kyle
- Creighton, Chad J.
- Dinh, Huyen
- Doddapaneni, HarshaVardhan
- Gibbs, Richard A.
- Han, Yi
- Korchina, Viktoriya
- Liu, Xiuping
- Morgan, Margaret
- Muzny, Donna
- Sheth, Margi
- Shinbrot, Eve
- Wang, Linghua
- Wang, Min
- Wheeler, David A.
- Zhao, Fengmei
- Hess, Julian
- Bailey, Matthew
- Ding, Li
- Fronick, Catrina C.
- Fulton, Robert S.
- Kandoth, Cyriac
- Mardis, Elaine R.
- McLellan, Michael D.
- Miller, Christopher A.
- Wilson, Richard K.
- Sherman, Mark
- Bowen, Jay
- Leraas, Kristen M.
- Lichtenberg, Tara M.
- Ramirez, Nilsa C.
- Zmuda, Erik
- Corcoran, Niall
- Hovens, Christopher
- Fregnani, José H.
- Reis, Rui M.
- Silveira, Henrique C.S.
- Vidal, Daniel O.
- Anderson, Matthew L.
- Ittmann, Michael
- Huntsman, David
- Kohl, Bernard
- Andry, Chris
- Duffy, Elizabeth R.
- Lyadov, Vladimir
- Paklina, Oxana
- Setdikova, Galiya
- Tavobilov, Mikhail
- Warnick, Ronald
- Berkowitz, Ross
- Feltmate, Colleen
- Horowitz, Neil
- Kibel, Adam
- Raut, Chandrajit P.
- Ostrom, Quinn T.
- Sloan, Andrew E.
- Giuliante, Felice
- Goodman, Marc
- Karlan, Beth Y.
- Somiari, Stella
- Bennett, Joseph
- Iacocca, Mary
- Lacombe, Louis
- Têtu, Bernard
- Bergeron, Alain
- McGraw, Mary
- Hibshoosh, Hanina
- Sepulveda, Antonia
- Wang, Timothy
- Potapova, Olga
- Voronina, Olga
- Desjardins, Laurence
- Mariani, Odette
- Stern, Marc-Henri
- Cheng, Feixiong
- Signoretti, Sabina
- Berchuck, Andrew
- Bigner, Darell
- Lipp, Eric
- McCall, Shannon
- McLendon, Roger
- Secord, Angeles
- Behera, Madhusmita
- Brat, Daniel J.
- Chen, Amy
- Delman, Keith
- Force, Seth
- Khuri, Fadlo
- Magliocca, Kelly
- Maithel, Shishir
- Olson, Jeffrey J.
- Owonikoko, Taofeek
- Ramalingam, Suresh
- Shin, Dong M.
- Sica, Gabriel
- Zhang, Hongzheng
- Looijenga, Leendert
- Oosterhuis, Wolter
- Zwarthoff, Ellen C.
- Calatozzolo, Chiara
- Cuzzubbo, Stefania
- DiMeco, Francesco
- Finocchiaro, Gaetano
- Mattei, Luca
- Perin, Alessandro
- Pollo, Bianca
- Taubert, Helge
- Wach, Sven
- Wullich, Bernd
- Kycler, Witold
- Murawa, Dawid
- Martin, Julie
- Bubley, Glenn
- Bueno, Raphael
- Richards, William G.
- Kalkanis, Steven
- Mikkelsen, Tom
- Scarpace, Lisa
- Girard, Nicolas
- Aymerich, Marta
- Giné, Eva
- Tang, Yufang
- Colman, Howard
- Evason, Kimberley
- Gabra, Hani
- Juhl, Hartmut
- Hoon, Dave
- Kang, Koo Jeong
- Beuschlein, Felix
- Breggia, Anne
- Birrer, Michael
- Borad, Mitesh
- Bryce, Alan H.
- Chandan, Vishal
- Cheville, John
- Copland, John A.
- Flotte, Thomas
- Ho, Thai
- Kendrick, Michael
- Kocher, Jean-Pierre
- Nagorney, David
- O’Brien, Daniel
- O’Neill, Brian Patrick
- Patel, Tushar
- Rivera, Michael
- Roberts, Lewis
- Smyrk, Thomas
- Torbenson, Michael
- Yang, Ju Dong
- Zhang, Lizhi
- Brimo, Fadi
- Ajani, Jaffer A.
- Behrens, Carmen
- Broaddus, Russell
- Czerniak, Bogdan
- Esmaeli, Bita
- Fujimoto, Junya
- Guo, Charles
- Logothetis, Christopher
- Ramondetta, Lois
- Sood, Anil
- Troncoso, Patricia
- Tsao, Anne
- Wistuba, Ignacio
- Carter, Candace
- Haydu, Lauren
- Jakrot, Valerie
- Kakavand, Hojabr
- Kefford, Richard
- Lee, Kenneth
- Long, Georgina
- Mann, Graham
- Quinn, Michael
- Saw, Robyn
- Scolyer, Richard
- Shannon, Kerwin
- Spillane, Andrew
- Stretch, Jonathan
- Thompson, John
- Wilmott, James
- Chan, Timothy A.
- Ghossein, Ronald
- Gopalan, Anuradha
- Levine, Douglas A.
- Singer, Samuel
- Singh, Bhuvanesh
- Broudy, Thomas
- Nair, Praveen
- Zaren, Howard
- Park, Joong-Won
- Kebebew, Electron
- Linehan, W. Marston
- Metwalli, Adam R.
- Pinto, Peter A.
- Schiffman, Mark
- Schmidt, Laura S.
- Vocke, Cathy D.
- Wentzensen, Nicolas
- Yang, Hannah
- Moncrieff, Marc
- Goparaju, Chandra
- Melamed, Jonathan
- Pass, Harvey
- Cernat, Mircea
- Arnaout, Angel
- Bartlett, John
- Thomas, George
- Rassl, Doris M.
- Rintoul, Robert C.
- Bifulco, Carlo
- Urba, Walter
- Hayward, Nicholas
- Timmers, Henri
- Facciolo, Francesco
- Marino, Mirella
- Piché, Alain
- Chevalier, Simone
- McKercher, Ginette
- Barnett, Gene
- Farver, Carol
- Pennell, Nathan A.
- Borgia, Jeffrey A.
- Seder, Christopher W.
- Junker, Kerstin
- Omberg, Larsson
- Manikhas, George
- Alvaro, Domenico
- Bragazzi, Maria Consiglia
- Cardinale, Vincenzo
- Carpino, Guido
- Gaudio, Eugenio
- Dubina, Michael
- Moiseenko, Fedor
- Dhanasekaran, Renumathy
- Becker, Karl-Friedrich
- Janssen, Klaus-Peter
- Cebulla, Colleen M.
- Elder, J. Bradley
- Lehman, Norman L.
- Nguyen, Phuong
- Pilarski, Robert
- Rai, Karan
- Schoenfield, Lynn
- Wakely, Paul
- Lechan, Ronald
- Tischler, Arthur
- Grizzle, William E.
- Henderson, Joel
- Porten, Sima
- Fassnacht, Martin
- Asa, Sylvia L.
- Schadendorf, Dirk
- Couce, Marta
- Graefen, Markus
- Huland, Hartwig
- Sauter, Guido
- Schlomm, Thorsten
- Simon, Ronald
- Tennstedt, Pierre
- Nelson, Mark
- Bathe, Oliver
- Carroll, Peter R.
- Chan, June M.
- Kelley, Robin K.
- Landen, Charles N.
- Prados, Michael
- VandenBerg, Scott
- Roggin, Kevin
- Kendler, Ady
- Steele, Ruth
- Jimeno, Antonio
- Forgie, Ian
- Mannelli, Massimo
- Carney, Michael
- Campos, Benito
- Unterberg, Andreas
- Bossler, Aaron
- Ma, Deqin
- Milhem, Mohammed
- Godwin, Andrew K.
- Madan, Rashna
- Adebamowo, Clement
- Adebamowo, Sally N.
- Boussioutas, Alex
- Beer, David
- Giordano, Thomas
- Bocklage, Therese
- Landrum, Lisa
- Moore, Kathleen
- Moxley, Katherine
- Zuna, Rosemary
- Feldman, Michael
- Luketich, James
- Carlotti, Carlos Gilberto
- Kemp, Rafael
- Tirapelli, Daniela
- Catto, James
- Swisher, Elizabeth
- Creaney, Jenette
- Robinson, Bruce
- Shelley, Carl Simon
- Bradford, Carol
- Carey, Thomas
- Prince, Mark
- Rozek, Laura
- Wolf, Gregory
- Fong, Kwun M.
- Yang, Ian
- Rathmell, W. Kimryn
- Kovatich, Albert J.
- Shriver, Craig D.
- DiPersio, John
- Drake, Bettina
- Govindan, Ramaswamy
- Heath, Sharon
- Ley, Timothy
- Rubin, Mark A.
- Lee, Jung Il
- Aredes, Natália D.
- Mariamidze, Armaz
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-04
- Volume
- 173
- Issue
- 2
- Pages
- 291-304.e6
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC5957518
- OpenAlex
- W2796153844
- Cited by
- 2,546
- References
- 58
- Citations by year
- 2026: 284 · 2025: 294 · 2024: 296 · 2023: 355 · 2022: 375 · 2021: 374 · 2020: 330 · 2019: 178 · 2018: 56
- FWCI
- 71.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by-nc-nd)
- UWA Profiles and Research Repository (UWA) (submittedVersion, cc-by)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by-nc-nd)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- eScholarship (California Digital Library) (submittedVersion)
- Florence Research (University of Florence) (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, cc-by-nc-nd)
- mediaTUM (Technical University of Munich) (submittedVersion, other-oa)
- Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion, cc-by-nc-nd)
- Spiral (Imperial College London) (submittedVersion, cc-by-nc-nd)
- Funders
- National Human Genome Research Institute
- National Cancer Institute
- National Institutes of Health (U24 CA143866, U24 CA143843, P30 CA016672, U24 CA143867, U24 CA143840, U24 CA143882, U24 CA143858, U24 CA143835, U54 HG003273, U24 CA143883, U24 CA143848, U24 CA144025, U24 CA143845, U54 HG003079, U24 CA143799, U54 HG003067)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene expression and cancer classification
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- cell of origin, molecular classification of cancer, pan-cancer analysis, TCGA, aneuploidy, DNA methylation, mRNA expression, microRNA expression, reverse phase protein array, histological subtypes, tissue type, stemness, molecular clustering
- MeSH terms
- Aneuploidy, Chromosomes, Humans, Mutation, Neoplasm Proteins, Neoplasms, RNA, Messenger, Cluster Analysis, Databases, Factual, CpG Islands, DNA Methylation, MicroRNAs
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