Embracing cancer complexity: Hallmarks of systemic disease

Charles Swanton; Elsa Bernard; Chris Abbosh; Fabrice André; Johan Auwerx; Allan Balmain; Dafna Bar-Sagi; René Bernards; Susan Bullman; James DeGregori; Catherine Elliott; Ayelet Erez; Gerard Evan; Mark A. Febbraio; Andrés Hidalgo; Mariam Jamal-Hanjani; Johanna A. Joyce; Matthew Kaiser; Katja Lamia; Jason W. Locasale; Sherene Loi; Ilaria Malanchi; Miriam Merad; Kathryn Musgrave; Ketan J. Patel; Sergio Quezada; Jennifer A. Wargo; Ashani Weeraratna; Eileen White; Frank Winkler; John N. Wood; Karen H. Vousden; Douglas Hanahan

doi:10.1016/j.cell.2024.02.009

Embracing cancer complexity: Hallmarks of systemic disease

Charles Swanton^*, Elsa Bernard, Chris Abbosh, Fabrice André, Johan Auwerx, Allan Balmain, Dafna Bar-Sagi, René Bernards, Susan Bullman, James DeGregori, Catherine Elliott, Ayelet Erez, Gerard Evan, Mark A. Febbraio, Andrés Hidalgo, Mariam Jamal-Hanjani, Johanna A. Joyce, Matthew Kaiser, Katja Lamia, Jason W. LocasaleSherene Loi, Ilaria Malanchi, Miriam Merad, Kathryn Musgrave, Ketan J. Patel, Sergio Quezada, Jennifer A. Wargo, Ashani Weeraratna, Eileen White, Frank Winkler, John N. Wood, Karen H. Vousden^*, Douglas Hanahan^*

^*Corresponding author for this work

Department of Molecular Cell Biology

Research output: Contribution to journal › Review article › peer-review

42 Citations (Scopus)

Abstract

The last 50 years have witnessed extraordinary developments in understanding mechanisms of carcinogenesis, synthesized as the hallmarks of cancer. Despite this logical framework, our understanding of the molecular basis of systemic manifestations and the underlying causes of cancer-related death remains incomplete. Looking forward, elucidating how tumors interact with distant organs and how multifaceted environmental and physiological parameters impinge on tumors and their hosts will be crucial for advances in preventing and more effectively treating human cancers. In this perspective, we discuss complexities of cancer as a systemic disease, including tumor initiation and promotion, tumor micro- and immune macro-environments, aging, metabolism and obesity, cancer cachexia, circadian rhythms, nervous system interactions, tumor-related thrombosis, and the microbiome. Model systems incorporating human genetic variation will be essential to decipher the mechanistic basis of these phenomena and unravel gene-environment interactions, providing a modern synthesis of molecular oncology that is primed to prevent cancers and improve patient quality of life and cancer outcomes.

Original language	English
Pages (from-to)	1589-1616
Number of pages	28
Journal	Cell
Volume	187
Issue number	7
DOIs	https://doi.org/10.1016/j.cell.2024.02.009
Publication status	Published - 28 Mar 2024

All Science Journal Classification (ASJC) codes

General Biochemistry,Genetics and Molecular Biology

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10.1016/j.cell.2024.02.009

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Swanton, C., Bernard, E., Abbosh, C., André, F., Auwerx, J., Balmain, A., Bar-Sagi, D., Bernards, R., Bullman, S., DeGregori, J., Elliott, C., Erez, A., Evan, G., Febbraio, M. A., Hidalgo, A., Jamal-Hanjani, M., Joyce, J. A., Kaiser, M., Lamia, K., ... Hanahan, D. (2024). Embracing cancer complexity: Hallmarks of systemic disease. Cell, 187(7), 1589-1616. https://doi.org/10.1016/j.cell.2024.02.009

@article{3a4665d665454ebb8e8503f6e5dd635c,

title = "Embracing cancer complexity: Hallmarks of systemic disease",

abstract = "The last 50 years have witnessed extraordinary developments in understanding mechanisms of carcinogenesis, synthesized as the hallmarks of cancer. Despite this logical framework, our understanding of the molecular basis of systemic manifestations and the underlying causes of cancer-related death remains incomplete. Looking forward, elucidating how tumors interact with distant organs and how multifaceted environmental and physiological parameters impinge on tumors and their hosts will be crucial for advances in preventing and more effectively treating human cancers. In this perspective, we discuss complexities of cancer as a systemic disease, including tumor initiation and promotion, tumor micro- and immune macro-environments, aging, metabolism and obesity, cancer cachexia, circadian rhythms, nervous system interactions, tumor-related thrombosis, and the microbiome. Model systems incorporating human genetic variation will be essential to decipher the mechanistic basis of these phenomena and unravel gene-environment interactions, providing a modern synthesis of molecular oncology that is primed to prevent cancers and improve patient quality of life and cancer outcomes.",

author = "Charles Swanton and Elsa Bernard and Chris Abbosh and Fabrice Andr{\'e} and Johan Auwerx and Allan Balmain and Dafna Bar-Sagi and Ren{\'e} Bernards and Susan Bullman and James DeGregori and Catherine Elliott and Ayelet Erez and Gerard Evan and Febbraio, {Mark A.} and Andr{\'e}s Hidalgo and Mariam Jamal-Hanjani and Joyce, {Johanna A.} and Matthew Kaiser and Katja Lamia and Locasale, {Jason W.} and Sherene Loi and Ilaria Malanchi and Miriam Merad and Kathryn Musgrave and Patel, {Ketan J.} and Sergio Quezada and Wargo, {Jennifer A.} and Ashani Weeraratna and Eileen White and Frank Winkler and Wood, {John N.} and Vousden, {Karen H.} and Douglas Hanahan",

year = "2024",

month = mar,

day = "28",

doi = "10.1016/j.cell.2024.02.009",

language = "English",

volume = "187",

pages = "1589--1616",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

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Swanton, C, Bernard, E, Abbosh, C, André, F, Auwerx, J, Balmain, A, Bar-Sagi, D, Bernards, R, Bullman, S, DeGregori, J, Elliott, C, Erez, A, Evan, G, Febbraio, MA, Hidalgo, A, Jamal-Hanjani, M, Joyce, JA, Kaiser, M, Lamia, K, Locasale, JW, Loi, S, Malanchi, I, Merad, M, Musgrave, K, Patel, KJ, Quezada, S, Wargo, JA, Weeraratna, A, White, E, Winkler, F, Wood, JN, Vousden, KH & Hanahan, D 2024, 'Embracing cancer complexity: Hallmarks of systemic disease', Cell, vol. 187, no. 7, pp. 1589-1616. https://doi.org/10.1016/j.cell.2024.02.009

TY - JOUR

T1 - Embracing cancer complexity

T2 - Hallmarks of systemic disease

AU - Swanton, Charles

AU - Bernard, Elsa

AU - Abbosh, Chris

AU - André, Fabrice

AU - Auwerx, Johan

AU - Balmain, Allan

AU - Bar-Sagi, Dafna

AU - Bernards, René

AU - Bullman, Susan

AU - DeGregori, James

AU - Elliott, Catherine

AU - Erez, Ayelet

AU - Evan, Gerard

AU - Febbraio, Mark A.

AU - Hidalgo, Andrés

AU - Jamal-Hanjani, Mariam

AU - Joyce, Johanna A.

AU - Kaiser, Matthew

AU - Lamia, Katja

AU - Locasale, Jason W.

AU - Loi, Sherene

AU - Malanchi, Ilaria

AU - Merad, Miriam

AU - Musgrave, Kathryn

AU - Patel, Ketan J.

AU - Quezada, Sergio

AU - Wargo, Jennifer A.

AU - Weeraratna, Ashani

AU - White, Eileen

AU - Winkler, Frank

AU - Wood, John N.

AU - Vousden, Karen H.

AU - Hanahan, Douglas

PY - 2024/3/28

Y1 - 2024/3/28

N2 - The last 50 years have witnessed extraordinary developments in understanding mechanisms of carcinogenesis, synthesized as the hallmarks of cancer. Despite this logical framework, our understanding of the molecular basis of systemic manifestations and the underlying causes of cancer-related death remains incomplete. Looking forward, elucidating how tumors interact with distant organs and how multifaceted environmental and physiological parameters impinge on tumors and their hosts will be crucial for advances in preventing and more effectively treating human cancers. In this perspective, we discuss complexities of cancer as a systemic disease, including tumor initiation and promotion, tumor micro- and immune macro-environments, aging, metabolism and obesity, cancer cachexia, circadian rhythms, nervous system interactions, tumor-related thrombosis, and the microbiome. Model systems incorporating human genetic variation will be essential to decipher the mechanistic basis of these phenomena and unravel gene-environment interactions, providing a modern synthesis of molecular oncology that is primed to prevent cancers and improve patient quality of life and cancer outcomes.

AB - The last 50 years have witnessed extraordinary developments in understanding mechanisms of carcinogenesis, synthesized as the hallmarks of cancer. Despite this logical framework, our understanding of the molecular basis of systemic manifestations and the underlying causes of cancer-related death remains incomplete. Looking forward, elucidating how tumors interact with distant organs and how multifaceted environmental and physiological parameters impinge on tumors and their hosts will be crucial for advances in preventing and more effectively treating human cancers. In this perspective, we discuss complexities of cancer as a systemic disease, including tumor initiation and promotion, tumor micro- and immune macro-environments, aging, metabolism and obesity, cancer cachexia, circadian rhythms, nervous system interactions, tumor-related thrombosis, and the microbiome. Model systems incorporating human genetic variation will be essential to decipher the mechanistic basis of these phenomena and unravel gene-environment interactions, providing a modern synthesis of molecular oncology that is primed to prevent cancers and improve patient quality of life and cancer outcomes.

UR - http://www.scopus.com/inward/record.url?scp=85188424693&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2024.02.009

DO - 10.1016/j.cell.2024.02.009

M3 - Review article

AN - SCOPUS:85188424693

SN - 0092-8674

VL - 187

SP - 1589

EP - 1616

JO - Cell

JF - Cell

IS - 7

ER -

Embracing cancer complexity: Hallmarks of systemic disease

Abstract

All Science Journal Classification (ASJC) codes

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