Cell-state dynamics and therapeutic resistance in melanoma from the perspective of MITF and IFNγ pathways

Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities limits the percentage of patients with long-lasting responses. Accumulating evidence indicates that a persisting subpopulation of melanoma cells...

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Vydáno v:Nature reviews. Clinical oncology Ročník 16; číslo 9; s. 549 - 562
Hlavní autoři: Bai, Xue, Fisher, David E., Flaherty, Keith T.
Médium: Journal Article
Jazyk:angličtina
Vydáno: London Nature Publishing Group UK 01.09.2019
Nature Publishing Group
Témata:
631/67/1059/2325
631/67/1059/2326
631/67/1059/602
631/67/1813/1634
Apoptosis
Cell death
Cell survival
Drug Resistance, Neoplasm - physiology
Environmental conditions
Homeostasis
Humans
Hypoxia
Immunotherapy
Interferon-gamma - metabolism
Medical prognosis
Medicine
Medicine & Public Health
Melanoma
Melanoma - metabolism
Melanoma - pathology
Metastases
Microphthalmia-associated transcription factor
Microphthalmia-Associated Transcription Factor - metabolism
Models, Biological
Nutrients
Oncology
Proteins
Review Article
Senescence
Signal transduction
Signal Transduction - physiology
Spatial heterogeneity
Tumors
γ-Interferon
ISSN:1759-4774, 1759-4782, 1759-4782
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Abstract Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities limits the percentage of patients with long-lasting responses. Accumulating evidence indicates that a persisting subpopulation of melanoma cells contributes to resistance to targeted therapy or immunotherapy, even in patients who initially have a therapeutic response; however, the root mechanism of resistance remains elusive. To address this problem, we propose a new model, in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the whole process of therapeutic resistance development. Conceptually, we focused on two different pivotal signalling pathways (mediated by microphthalmia-associated transcription factor (MITF) and IFNγ) to construct the evolving trajectories of melanoma and described each of the cell states. Accordingly, the development of therapeutic resistance could be divided into three main phases: early survival of cell populations, reversal of senescence, and the establishment of new homeostatic states and development of irreversible resistance. On the basis of existing data, we propose future directions in both translational research and the design of therapeutic strategies that incorporate this emerging understanding of resistance. The authors of this Review propose a new model in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the process of therapeutic resistance development in patients with melanoma. Key points In any particular cell, the expression of a given protein fluctuates dynamically around a pre-set homeostatic level, contributing to temporal heterogeneity. At the cell-population level, the expression of a given protein fits a log-normal distribution, contributing to spatial heterogeneity. Cell state is mostly determined by the expression levels of different proteins, which is a continuous quantitative variable and can be perturbed by extrinsic stress, such as drug exposure. The development of resistance to targeted therapy and immunotherapy can be divided into three phases, namely, early survival (including persister cells and innate resistant cells), reversal of senescence and new homeostasis; along these phases, resistance gradually changes from reversible to irreversible. The persister cell subpopulation is programmed to tolerate cell death and capable of surviving harsh environmental conditions, such as hypoxia, lack of nutrients and exposure to targeted therapy and/or immunotherapy. Future therapeutic developments should take into account the highly dynamic heterogeneity and the existence of distinct homeostatic states of tumour cells.
AbstractList Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities limits the percentage of patients with long-lasting responses. Accumulating evidence indicates that a persisting subpopulation of melanoma cells contributes to resistance to targeted therapy or immunotherapy, even in patients who initially have a therapeutic response; however, the root mechanism of resistance remains elusive. To address this problem, we propose a new model, in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the whole process of therapeutic resistance development. Conceptually, we focused on two different pivotal signalling pathways (mediated by microphthalmia-associated transcription factor (MITF) and IFNγ) to construct the evolving trajectories of melanoma and described each of the cell states. Accordingly, the development of therapeutic resistance could be divided into three main phases: early survival of cell populations, reversal of senescence, and the establishment of new homeostatic states and development of irreversible resistance. On the basis of existing data, we propose future directions in both translational research and the design of therapeutic strategies that incorporate this emerging understanding of resistance. The authors of this Review propose a new model in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the process of therapeutic resistance development in patients with melanoma. Key points In any particular cell, the expression of a given protein fluctuates dynamically around a pre-set homeostatic level, contributing to temporal heterogeneity. At the cell-population level, the expression of a given protein fits a log-normal distribution, contributing to spatial heterogeneity. Cell state is mostly determined by the expression levels of different proteins, which is a continuous quantitative variable and can be perturbed by extrinsic stress, such as drug exposure. The development of resistance to targeted therapy and immunotherapy can be divided into three phases, namely, early survival (including persister cells and innate resistant cells), reversal of senescence and new homeostasis; along these phases, resistance gradually changes from reversible to irreversible. The persister cell subpopulation is programmed to tolerate cell death and capable of surviving harsh environmental conditions, such as hypoxia, lack of nutrients and exposure to targeted therapy and/or immunotherapy. Future therapeutic developments should take into account the highly dynamic heterogeneity and the existence of distinct homeostatic states of tumour cells.
Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities limits the percentage of patients with long-lasting responses. Accumulating evidence indicates that a persisting subpopulation of melanoma cells contributes to resistance to targeted therapy or immunotherapy, even in patients who initially have a therapeutic response; however, the root mechanism of resistance remains elusive. To address this problem, we propose a new model, in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the whole process of therapeutic resistance development. Conceptually, we focused on two different pivotal signalling pathways (mediated by microphthalmia-associated transcription factor (MITF) and IFNγ) to construct the evolving trajectories of melanoma and described each of the cell states. Accordingly, the development of therapeutic resistance could be divided into three main phases: early survival of cell populations, reversal of senescence, and the establishment of new homeostatic states and development of irreversible resistance. On the basis of existing data, we propose future directions in both translational research and the design of therapeutic strategies that incorporate this emerging understanding of resistance.
Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities limits the percentage of patients with long-lasting responses. Accumulating evidence indicates that a persisting subpopulation of melanoma cells contributes to resistance to targeted therapy or immunotherapy, even in patients who initially have a therapeutic response; however, the root mechanism of resistance remains elusive. To address this problem, we propose a new model, in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the whole process of therapeutic resistance development. Conceptually, we focused on two different pivotal signalling pathways (mediated by microphthalmia-associated transcription factor (MITF) and IFNγ) to construct the evolving trajectories of melanoma and described each of the cell states. Accordingly, the development of therapeutic resistance could be divided into three main phases: early survival of cell populations, reversal of senescence, and the establishment of new homeostatic states and development of irreversible resistance. On the basis of existing data, we propose future directions in both translational research and the design of therapeutic strategies that incorporate this emerging understanding of resistance.The authors of this Review propose a new model in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the process of therapeutic resistance development in patients with melanoma.
Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities limits the percentage of patients with long-lasting responses. Accumulating evidence indicates that a persisting subpopulation of melanoma cells contributes to resistance to targeted therapy or immunotherapy, even in patients who initially have a therapeutic response; however, the root mechanism of resistance remains elusive. To address this problem, we propose a new model, in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the whole process of therapeutic resistance development. Conceptually, we focused on two different pivotal signalling pathways (mediated by microphthalmia-associated transcription factor (MITF) and IFNγ) to construct the evolving trajectories of melanoma and described each of the cell states. Accordingly, the development of therapeutic resistance could be divided into three main phases: early survival of cell populations, reversal of senescence, and the establishment of new homeostatic states and development of irreversible resistance. On the basis of existing data, we propose future directions in both translational research and the design of therapeutic strategies that incorporate this emerging understanding of resistance.Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities limits the percentage of patients with long-lasting responses. Accumulating evidence indicates that a persisting subpopulation of melanoma cells contributes to resistance to targeted therapy or immunotherapy, even in patients who initially have a therapeutic response; however, the root mechanism of resistance remains elusive. To address this problem, we propose a new model, in which dynamic fluctuations of protein expression at the single-cell level and longitudinal reshaping of the cellular state at the cell-population level explain the whole process of therapeutic resistance development. Conceptually, we focused on two different pivotal signalling pathways (mediated by microphthalmia-associated transcription factor (MITF) and IFNγ) to construct the evolving trajectories of melanoma and described each of the cell states. Accordingly, the development of therapeutic resistance could be divided into three main phases: early survival of cell populations, reversal of senescence, and the establishment of new homeostatic states and development of irreversible resistance. On the basis of existing data, we propose future directions in both translational research and the design of therapeutic strategies that incorporate this emerging understanding of resistance.
Author Bai, Xue
Fisher, David E.
Flaherty, Keith T.
AuthorAffiliation 3 Dermatology and Cutaneous Biology Research Center, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA
1 Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA, USA
2 Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education, Beijing), Department of Renal Cancer and Melanoma, Peking University Cancer Hospital and Institute, Beijing, China
AuthorAffiliation_xml – name: 3 Dermatology and Cutaneous Biology Research Center, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA
– name: 1 Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA, USA
– name: 2 Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education, Beijing), Department of Renal Cancer and Melanoma, Peking University Cancer Hospital and Institute, Beijing, China
Author_xml – sequence: 1
  givenname: Xue
  surname: Bai
  fullname: Bai, Xue
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education, Beijing), Department of Renal Cancer and Melanoma, Peking University Cancer Hospital and Institute
– sequence: 2
  givenname: David E.
  surname: Fisher
  fullname: Fisher, David E.
  organization: Dermatology and Cutaneous Biology Research Center, Massachusetts General Hospital, Harvard Medical School
– sequence: 3
  givenname: Keith T.
  orcidid: 0000-0002-3402-0478
  surname: Flaherty
  fullname: Flaherty, Keith T.
  email: kflaherty@mgh.harvard.edu
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30967646$$D View this record in MEDLINE/PubMed
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Springer Nature Limited 2019.
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Snippet Targeted therapy and immunotherapy have greatly improved the prognosis of patients with metastatic melanoma, but resistance to these therapeutic modalities...
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SubjectTerms 631/67/1059/2325
631/67/1059/2326
631/67/1059/602
631/67/1813/1634
Apoptosis
Cell death
Cell survival
Drug Resistance, Neoplasm - physiology
Environmental conditions
Homeostasis
Humans
Hypoxia
Immunotherapy
Interferon-gamma - metabolism
Medical prognosis
Medicine
Medicine & Public Health
Melanoma
Melanoma - metabolism
Melanoma - pathology
Metastases
Microphthalmia-associated transcription factor
Microphthalmia-Associated Transcription Factor - metabolism
Models, Biological
Nutrients
Oncology
Proteins
Review Article
Senescence
Signal transduction
Signal Transduction - physiology
Spatial heterogeneity
Tumors
γ-Interferon
Title Cell-state dynamics and therapeutic resistance in melanoma from the perspective of MITF and IFNγ pathways
URI https://link.springer.com/article/10.1038/s41571-019-0204-6
https://www.ncbi.nlm.nih.gov/pubmed/30967646
https://www.proquest.com/docview/2277418941
https://www.proquest.com/docview/2207159159
https://pubmed.ncbi.nlm.nih.gov/PMC7185899
Volume 16
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