Pan-cancer Alterations of the MYC Oncogene and Its Proximal Network across the Cancer Genome Atlas

Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors, and co-regulatory proteins, forming the proximal MYC network (PMN), across human cancers is lacking. Using computational approaches, we define genomic and proteomic...

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Published inCell systems Vol. 6; no. 3; pp. 282 - 300.e2
Main Authors Berger, Ashton C., Hurlin, Peter J., Eisenman, Robert N., Felau, Ina, Zhang, Jiashan (Julia), Kim, Jaegil, Kramer, Roger, Reynolds, Sheila, Shmulevich, Ilya, Thorsson, Vesteinn, Liang, Han, Lu, Yiling, Ng, Kwok-Shing, Gao, Jianjiong, Heins, Zachary J., La, Konnor, Schultz, Nikolaus, Taylor, Barry S., Bowlby, Reanne, Lee, Darlene, Mungall, Karen, Schein, Jacqueline E., Schumacher, Steven E., Hoyle, Alan P., Perou, Amy H., Skelly, Tara, Chang, Kyle, Shinbrot, Eve, Wang, Min, Xi, Liu, Schmidt, Heather K., Curley, Erin, Gardner, Johanna, Morris, Scott, Paulauskis, Joseph, Longatto-Filho, Adhemar, Kibel, Adam, Devine, Karen, Ostrom, Quinn T., Shimmel, Kristen, Harr, Jodi, Zach, Leigh Anne, Kvecher, Leonid, Latour, Mathieu, Têtu, Bernard, McGraw, Mary, Chen, Amy, Sica, Gabriel, Van Meir, Erwin G., Calatozzolo, Chiara, Mattei, Luca, Pollo, Bianca, Houck, John, Bueno, Raphael, Girard, Nicolas, Aymerich, Marta, Stepa, Serghei, Hoon, Dave, Beuschlein, Felix, Chandan, Vishal, Moser, Catherine, O’Brien, Daniel, Thompson, R. Houston, Torbenson, Michael, Behrens, Carmen, Tsao, Anne, Jakrot, Valerie, Lee, Kenneth, Spillane, Andrew, Chan, Timothy A., Park, Joong-Won, Kebebew, Electron, Thomas, George, Facciolo, Francesco, Piché, Alain, Pennell, Nathan A., Morrison, Carl, Seder, Christopher W., Bragazzi, Maria Consiglia, Gaudio, Eugenio, Becker, Karl-Friedrich, Bell, Sue, Hilty, Joe, Grizzle, William E., Porten, Sima, Asa, Sylvia L., Sauter, Guido, Schlomm, Thorsten, Bathe, Oliver, Phillips, Joanna, Prados, Michael, Sifri, Suzanne, Forgie, Ian, Mannelli, Massimo, Herold-Mende, Christel, Landrum, Lisa, Kemp, Rafael, Rathmell, W. Kimryn, Fantacone-Campbell, J. Leigh, Mariamidze, Armaz
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 28.03.2018
Subjects
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - genetics
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - metabolism
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Biomarkers, Tumor - genetics
Carcinogenesis - genetics
Chromatin
Computational Biology - methods
Genes, myc - genetics
Genes, myc - physiology
Genomics
Humans
MAX
MNT
MYC genomic alterations
Neoplasms - genetics
Neoplasms - physiopathology
Oncogenes
Proteomics
Proto-Oncogene Proteins c-myc - genetics
Proto-Oncogene Proteins c-myc - physiology
Repressor Proteins - genetics
Repressor Proteins - metabolism
Signal Transduction - genetics
TCGA
The Cancer Genome Atlas
Transcription Factors - genetics
MNT
MAX
MYC genomic alterations
TCGA
The Cancer Genome Atlas
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Abstract Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors, and co-regulatory proteins, forming the proximal MYC network (PMN), across human cancers is lacking. Using computational approaches, we define genomic and proteomic features associated with MYC and the PMN across the 33 cancers of The Cancer Genome Atlas. Pan-cancer, 28% of all samples had at least one of the MYC paralogs amplified. In contrast, the MYC antagonists MGA and MNT were the most frequently mutated or deleted members, proposing a role as tumor suppressors. MYC alterations were mutually exclusive with PIK3CA, PTEN, APC, or BRAF alterations, suggesting that MYC is a distinct oncogenic driver. Expression analysis revealed MYC-associated pathways in tumor subtypes, such as immune response and growth factor signaling; chromatin, translation, and DNA replication/repair were conserved pan-cancer. This analysis reveals insights into MYC biology and is a reference for biomarkers and therapeutics for cancers with alterations of MYC or the PMN. [Display omitted] •MYC paralogs are significantly amplified (28% of all samples)•MYC antagonists are mutated (MGA, 4% of samples) or deleted (MNT, 10% of samples)•MYC alterations are mutually exclusive with PIK3CA, PTEN, APC, or BRAF alterations•Expression analysis reveals pan-cancer and tumor-specific MYC-associated pathways We present a computational study determining the frequency and extent of alterations of the MYC network across the 33 human cancers of TCGA. These data, together with MYC, positively correlated pathways as well as mutually exclusive cancer genes, will be a resource for understanding MYC-driven cancers and designing of therapeutics.
AbstractList Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors and coregulatory proteins, forming the Proximal MYC Network (PMN), across human cancers is lacking. Using computational approaches, we define genomic and proteomic features associated with MYC and the PMN across the 33 cancers of The Cancer Genome Atlas. Pan-cancer, 28% of all samples had at least one of the MYC paralogs amplified. In contrast, the MYC antagonists MGA and MNT were the most frequently mutated or deleted members, proposing a role as tumor suppressors. MYC alterations were mutually exclusive with PIK3CA , PTEN , APC , or BRAF alterations, suggesting MYC is a distinct oncogenic driver. Expression analysis revealed MYC-associated pathways in tumor subtypes, such as immune response and growth factor signaling; chromatin, translation and DNA replication/repair were conserved pan-cancer. This analysis reveals insights into MYC biology and is a reference for biomarkers and therapeutics for cancers with alterations of MYC or the PMN. We present a computational study determining the frequency and extent of alterations of the MYC network across the 33 human cancers of TCGA. This data, together with MYC positively correlated pathways as well as mutually exclusive cancer genes, will be a resource for understanding MYC-driven cancers and designing of therapeutics.
Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors, and co-regulatory proteins, forming the proximal MYC network (PMN), across human cancers is lacking. Using computational approaches, we define genomic and proteomic features associated with MYC and the PMN across the 33 cancers of The Cancer Genome Atlas. Pan-cancer, 28% of all samples had at least one of the MYC paralogs amplified. In contrast, the MYC antagonists MGA and MNT were the most frequently mutated or deleted members, proposing a role as tumor suppressors. MYC alterations were mutually exclusive with PIK3CA, PTEN, APC, or BRAF alterations, suggesting that MYC is a distinct oncogenic driver. Expression analysis revealed MYC-associated pathways in tumor subtypes, such as immune response and growth factor signaling; chromatin, translation, and DNA replication/repair were conserved pan-cancer. This analysis reveals insights into MYC biology and is a reference for biomarkers and therapeutics for cancers with alterations of MYC or the PMN. [Display omitted] •MYC paralogs are significantly amplified (28% of all samples)•MYC antagonists are mutated (MGA, 4% of samples) or deleted (MNT, 10% of samples)•MYC alterations are mutually exclusive with PIK3CA, PTEN, APC, or BRAF alterations•Expression analysis reveals pan-cancer and tumor-specific MYC-associated pathways We present a computational study determining the frequency and extent of alterations of the MYC network across the 33 human cancers of TCGA. These data, together with MYC, positively correlated pathways as well as mutually exclusive cancer genes, will be a resource for understanding MYC-driven cancers and designing of therapeutics.
Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors, and co-regulatory proteins, forming the proximal MYC network (PMN), across human cancers is lacking. Using computational approaches, we define genomic and proteomic features associated with MYC and the PMN across the 33 cancers of The Cancer Genome Atlas. Pan-cancer, 28% of all samples had at least one of the MYC paralogs amplified. In contrast, the MYC antagonists MGA and MNT were the most frequently mutated or deleted members, proposing a role as tumor suppressors. MYC alterations were mutually exclusive with PIK3CA, PTEN, APC, or BRAF alterations, suggesting that MYC is a distinct oncogenic driver. Expression analysis revealed MYC-associated pathways in tumor subtypes, such as immune response and growth factor signaling; chromatin, translation, and DNA replication/repair were conserved pan-cancer. This analysis reveals insights into MYC biology and is a reference for biomarkers and therapeutics for cancers with alterations of MYC or the PMN.
Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors, and co-regulatory proteins, forming the proximal MYC network (PMN), across human cancers is lacking. Using computational approaches, we define genomic and proteomic features associated with MYC and the PMN across the 33 cancers of The Cancer Genome Atlas. Pan-cancer, 28% of all samples had at least one of the MYC paralogs amplified. In contrast, the MYC antagonists MGA and MNT were the most frequently mutated or deleted members, proposing a role as tumor suppressors. MYC alterations were mutually exclusive with PIK3CA, PTEN, APC, or BRAF alterations, suggesting that MYC is a distinct oncogenic driver. Expression analysis revealed MYC-associated pathways in tumor subtypes, such as immune response and growth factor signaling; chromatin, translation, and DNA replication/repair were conserved pan-cancer. This analysis reveals insights into MYC biology and is a reference for biomarkers and therapeutics for cancers with alterations of MYC or the PMN.Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors, and co-regulatory proteins, forming the proximal MYC network (PMN), across human cancers is lacking. Using computational approaches, we define genomic and proteomic features associated with MYC and the PMN across the 33 cancers of The Cancer Genome Atlas. Pan-cancer, 28% of all samples had at least one of the MYC paralogs amplified. In contrast, the MYC antagonists MGA and MNT were the most frequently mutated or deleted members, proposing a role as tumor suppressors. MYC alterations were mutually exclusive with PIK3CA, PTEN, APC, or BRAF alterations, suggesting that MYC is a distinct oncogenic driver. Expression analysis revealed MYC-associated pathways in tumor subtypes, such as immune response and growth factor signaling; chromatin, translation, and DNA replication/repair were conserved pan-cancer. This analysis reveals insights into MYC biology and is a reference for biomarkers and therapeutics for cancers with alterations of MYC or the PMN.
Author Desjardins, Laurence
Aredes, Natália D.
Liu, Yuexin
Bossler, Aaron
Khuri, Fadlo
Deyarmin, Brenda
Bondaruk, Jolanta
Copland, John A.
Duffy, Elizabeth R.
Marino, Mirella
Smyrk, Thomas
Carey, Francis
Facciolo, Francesco
Weinstein, John N.
Nagorney, David
Kovatich, Albert J.
De Rienzo, Assunta
Knudson, Michael
Sadeghi, Sara
Baylin, Stephen
Fan, Cheng
Oosterhuis, Wolter
Heath, Sharon
Longatto-Filho, Adhemar
Mann, Graham
Cebulla, Colleen M.
Balu, Saianand
Wilson, Richard K.
Breggia, Anne
Warnick, Ronald
Lu, Yiling
Mayo, Michael
Stoop, Hans
Wang, Linghua
Wentzensen, Nicolas
de Bruijn, Ino
Zenklusen, Jean C.
Quinn, Michael
Reynolds, Sheila
Bifulco, Carlo
Graefen, Markus
Eisenman, Robert N.
Zhang, Hailei
Kefford, Richard
Muto, Michael
Horowitz, Neil
Voet, Doug
Costello, Tony
Brimo, Fadi
Robinson, Bruce
Gao, Galen F.
Liu, Wenbin
Richards, William G.
Huntsman, David
McPherson, Christopher
Sigmund, Rita
Long, Georgina
Schlomm, Thorsten
Thorp, Richard
Giuliante, Felice
Couce, Marta
Broom, Bradley M.
Lin, Pei
Hess, Julian
Hoadley, Katherine A.
Czerniak, Bogdan
Lew
AuthorAffiliation 6 Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA
1 Cure First, Seattle, WA, USA
5 Dana-Farber Cancer Institute, the Broad Institute of Harvard and MIT, and Harvard Medical School, Boston, MA, USA
2 SEngine Precision Medicine, Seattle, WA, USA
7 Department of Oncological Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA
10 Institute for Systems Biology, Seattle, Washington, Providence Health and Services, Portland, OR, USA
3 The Eli and Edythe L. Broad Institute of Massachusetts Institute of Technology and Harvard University, Cambridge, MA, USA
4 Department of Systems Biology, University of Texas MD Anderson Cancer Center, Houston, TX USA
8 Shriners Hospitals for Children Research Center, Department of Cell, Developmental and Cancer Biology, Oregon Health & Science University, Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA
9 Division of Basic Sciences, Fred Hutchinson Cancer Research Ce
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29596783$$D View this record in MEDLINE/PubMed
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Liu, Yuexin
Armenia, Joshua
Stuart, Joshua M
DeFreitas, Timothy
Dhankani, Varsha
Zenklusen, Jean C
Liu, Jia
Leinonen, Kalle
Weinstein, John N
Noble, Michael S
Abeshouse, Adam
Wilkerson, Matthew D
Meier, Sam
Hegde, Apurva M
Zhang, Jiashan Julia
Wong, Christopher K
Lu, Yiling
Broom, Bradley M
Frazer, Scott
Reznik, Ed
de Bruijn, Ino
Cho, Juok
Reynolds, Sheila
Bernard, Brady
Zhang, Hailei
Demchok, John A
Voet, Doug
Kundra, Ritika
Rao, Arvind
Pihl, Todd
Tarnuzzer, Roy
Liu, Wenbin
Sun, Yichao
Heiman, David I
Ng, Kwok-Shing
Chudamani, Sudha
Lin, Pei
Phillips, Sarah M
Nissan, Moriah G
Chatila, Walid K
Taylor, Barry S
Miller, Michael
Hayes, D Neil
Yang, Liming
Gross, Benjamin E
Wu, Ye
Ferguson, Martin L
Sanchez-Vega, Francisco
Chakravarty, Debyani
Lawrence, Michael S
Yau, Christina
Felau, Ina
Heins, Zachary J
Wang, Jioajiao
Korkut, Anil
Ju, Zhenlin
Mills, Gordon B
Gao, Jianjiong
Kanchi, Rupa S
Kasapi, Melpomeni
Schultz, Nikolaus
Shmulevich, Ilya
Zhang, Jiexin
Spellman, Paul
Parker, Joel S
Sumer, S Onur
Benz, Christopher
Kramer, Roger
Zhang, Hongxin
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  surname: Lin
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– sequence: 30
  givenname: Sam
  surname: Meier
  fullname: Meier, Sam
– sequence: 31
  givenname: Michael S
  surname: Noble
  fullname: Noble, Michael S
– sequence: 32
  givenname: Gordon
  surname: Saksena
  fullname: Saksena, Gordon
– sequence: 33
  givenname: Doug
  surname: Voet
  fullname: Voet, Doug
– sequence: 34
  givenname: Hailei
  surname: Zhang
  fullname: Zhang, Hailei
– sequence: 35
  givenname: Brady
  surname: Bernard
  fullname: Bernard, Brady
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  givenname: Nyasha
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  givenname: Varsha
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  givenname: Theo
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  givenname: Roger
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  givenname: Kalle
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  givenname: Yuexin
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– sequence: 42
  givenname: Michael
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– sequence: 43
  givenname: Sheila
  surname: Reynolds
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– sequence: 44
  givenname: Ilya
  surname: Shmulevich
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– sequence: 45
  givenname: Vesteinn
  surname: Thorsson
  fullname: Thorsson, Vesteinn
– sequence: 46
  givenname: Wei
  surname: Zhang
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  givenname: Rehan
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– sequence: 48
  givenname: Bradley M
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  givenname: Apurva M
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  givenname: Zhenlin
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  fullname: Ju, Zhenlin
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  givenname: Rupa S
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– sequence: 52
  givenname: Anil
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– sequence: 53
  givenname: Jun
  surname: Li
  fullname: Li, Jun
– sequence: 54
  givenname: Han
  surname: Liang
  fullname: Liang, Han
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  givenname: Shiyun
  surname: Ling
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  givenname: Wenbin
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  fullname: Liu, Wenbin
– sequence: 57
  givenname: Yiling
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  givenname: Gordon B
  surname: Mills
  fullname: Mills, Gordon B
– sequence: 59
  givenname: Kwok-Shing
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– sequence: 60
  givenname: Arvind
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– sequence: 61
  givenname: Michael
  surname: Ryan
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– sequence: 62
  givenname: Jing
  surname: Wang
  fullname: Wang, Jing
– sequence: 63
  givenname: John N
  surname: Weinstein
  fullname: Weinstein, John N
– sequence: 64
  givenname: Jiexin
  surname: Zhang
  fullname: Zhang, Jiexin
– sequence: 65
  givenname: Adam
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– sequence: 67
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– sequence: 68
  givenname: Walid K
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– sequence: 69
  givenname: Ino
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  fullname: Gao, Jianjiong
– sequence: 71
  givenname: Benjamin E
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– sequence: 72
  givenname: Zachary J
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– sequence: 73
  givenname: Ritika
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  fullname: Kundra, Ritika
– sequence: 74
  givenname: Konnor
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  fullname: La, Konnor
– sequence: 75
  givenname: Marc
  surname: Ladanyi
  fullname: Ladanyi, Marc
– sequence: 76
  givenname: Augustin
  surname: Luna
  fullname: Luna, Augustin
– sequence: 77
  givenname: Moriah G
  surname: Nissan
  fullname: Nissan, Moriah G
– sequence: 78
  givenname: Angelica
  surname: Ochoa
  fullname: Ochoa, Angelica
– sequence: 79
  givenname: Sarah M
  surname: Phillips
  fullname: Phillips, Sarah M
– sequence: 80
  givenname: Ed
  surname: Reznik
  fullname: Reznik, Ed
– sequence: 81
  givenname: Francisco
  surname: Sanchez-Vega
  fullname: Sanchez-Vega, Francisco
– sequence: 82
  givenname: Chris
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– sequence: 83
  givenname: Nikolaus
  surname: Schultz
  fullname: Schultz, Nikolaus
– sequence: 84
  givenname: Robert
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  fullname: Sheridan, Robert
– sequence: 85
  givenname: S Onur
  surname: Sumer
  fullname: Sumer, S Onur
– sequence: 86
  givenname: Yichao
  surname: Sun
  fullname: Sun, Yichao
– sequence: 87
  givenname: Barry S
  surname: Taylor
  fullname: Taylor, Barry S
– sequence: 88
  givenname: Jioajiao
  surname: Wang
  fullname: Wang, Jioajiao
– sequence: 89
  givenname: Hongxin
  surname: Zhang
  fullname: Zhang, Hongxin
– sequence: 90
  givenname: Pavana
  surname: Anur
  fullname: Anur, Pavana
– sequence: 91
  givenname: Myron
  surname: Peto
  fullname: Peto, Myron
– sequence: 92
  givenname: Paul
  surname: Spellman
  fullname: Spellman, Paul
– sequence: 93
  givenname: Christopher
  surname: Benz
  fullname: Benz, Christopher
– sequence: 94
  givenname: Joshua M
  surname: Stuart
  fullname: Stuart, Joshua M
– sequence: 95
  givenname: Christopher K
  surname: Wong
  fullname: Wong, Christopher K
– sequence: 96
  givenname: Christina
  surname: Yau
  fullname: Yau, Christina
– sequence: 97
  givenname: D Neil
  surname: Hayes
  fullname: Hayes, D Neil
– sequence: 98
  givenname: Joel S
  surname: Parker
  fullname: Parker, Joel S
– sequence: 99
  givenname: Matthew D
  surname: Wilkerson
  fullname: Wilkerson, Matthew D
– sequence: 100
  givenname: Adrian
  surname: Ally
  fullname: Ally, Adrian
Copyright 2018 The Authors
Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.
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– notice: Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.
CorporateAuthor The Cancer Genome Atlas Network
Cancer Genome Atlas Network
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Issue 3
Keywords MNT
MAX
MYC genomic alterations
TCGA
The Cancer Genome Atlas
Language English
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Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.
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Snippet Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors, and co-regulatory...
Although the MYC oncogene has been implicated in cancer, a systematic assessment of alterations of MYC, related transcription factors and coregulatory...
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SubjectTerms Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - genetics
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors - metabolism
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Biomarkers, Tumor - genetics
Carcinogenesis - genetics
Chromatin
Computational Biology - methods
Genes, myc - genetics
Genes, myc - physiology
Genomics
Humans
MAX
MNT
MYC genomic alterations
Neoplasms - genetics
Neoplasms - physiopathology
Oncogenes
Proteomics
Proto-Oncogene Proteins c-myc - genetics
Proto-Oncogene Proteins c-myc - physiology
Repressor Proteins - genetics
Repressor Proteins - metabolism
Signal Transduction - genetics
TCGA
The Cancer Genome Atlas
Transcription Factors - genetics
Title Pan-cancer Alterations of the MYC Oncogene and Its Proximal Network across the Cancer Genome Atlas
URI https://dx.doi.org/10.1016/j.cels.2018.03.003
https://www.ncbi.nlm.nih.gov/pubmed/29596783
https://www.proquest.com/docview/2020480126
https://pubmed.ncbi.nlm.nih.gov/PMC5892207
Volume 6
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