Unveiling the role of cellular dormancy in cancer progression and recurrence.


Journal

Current opinion in oncology
ISSN: 1531-703X
Titre abrégé: Curr Opin Oncol
Pays: United States
ID NLM: 9007265

Informations de publication

Date de publication:
03 Jan 2024
Historique:
medline: 9 1 2024
pubmed: 9 1 2024
entrez: 9 1 2024
Statut: aheadofprint

Résumé

Cellular dormancy is a major contributor to cancer progression and recurrence. This review explores recent findings on the molecular mechanisms implicated in cancer dormancy and investigates potential strategies to improve therapeutic interventions. Research on cancer dormancy reveals a complex and multifaceted phenomenon. Providing a latent reservoir of tumor cells with reduced proliferation and enhanced drug-tolerance, dormant cancer cells emerge from a clonally diverse population after therapy or at metastatic sites. These cells exhibit distinct transcriptional and epigenetic profiles, involving the downregulation of Myc and mechanistic target of rapamycin (mTOR) pathways, and the induction of autophagy. Senescence traits, under the control of factors such as p53, also contribute significantly. The tumor microenvironment can either promote or prevent dormancy establishment, notably through the involvement of T and NK cells within the dormant tumor niche. Strategies to combat dormancy-related relapse include direct elimination of dormant tumor cells, sustaining dormancy to prolong survival, or awakening dormant cells to re-sensitize them to antiproliferative drugs. Improving our understanding of cancer dormancy at primary and secondary sites provides valuable insights into patient care and relapse prevention.

Identifiants

pubmed: 38193374
doi: 10.1097/CCO.0000000000001013
pii: 00001622-990000000-00140
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 The Author(s). Published by Wolters Kluwer Health, Inc.

Références

Pilleron S, Alqurini N, Ferlay J, et al. International trends in cancer incidence in middle-aged and older adults in 44 countries. J Geriatr Oncol 2022; 13:346–355.
Sharma SV, Lee DY, Li B, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010; 141:69–80.
Gerstberger S, Jiang Q, Ganesh K. Metastasis. Cell 2023; 186:1564–1579.
Giancotti FG. Mechanisms governing metastatic dormancy and reactivation. Cell 2013; 155:750.
Echeverria GV, Ge Z, Seth S, et al. Resistance to neoadjuvant chemotherapy in triple-negative breast cancer mediated by a reversible drug-tolerant state. Sci Transl Med 2019; 11:936.
Liu Y, Azizian NG, Sullivan DK, Li Y. mTOR inhibition attenuates chemosensitivity through the induction of chemotherapy resistant persisters. Nat Commun 2022; 13:7047.
Min H-Y, Lee H-Y. Cellular dormancy in cancer – mechanisms and potential targeting strategies. Cancer Res Treat 2023; 55:720–736.
Gelman IH. The genomic regulation of metastatic dormancy. Cancer Metastasis Rev 2023; 42:255–276.
Truskowski K, Amend SR, Pienta KJ. Dormant cancer cells: programmed quiescence, senescence, or both? Cancer Metastasis Rev 2023; 42:37–47.
Bulut-Karslioglu A, Biechele S, Jin H, et al. Inhibition of mTOR induces a paused pluripotent state. Nature 2016; 540:119–123.
Rehman SK, Haynes J, Collignon E, et al. Colorectal cancer cells enter a diapause-like DTP state to survive chemotherapy. Cell 2021; 184:226–242. e21.
Tau S, Miller TW. The role of cancer cell bioenergetics in dormancy and drug resistance. Cancer Metastasis Rev 2023; 42:87–98.
Li Y, Chen H, Lu D, et al. Mitophagy is a novel protective mechanism for drug-tolerant persister (DTP) cancer cells. Autophagy 2023; 19:2618–2619.
Hadfield G. The dormant cancer cell. Br Med J 1954; 2:607–610.
Elkholi IE, Lalonde A, Park M, Côté JF. Breast cancer metastatic dormancy and relapse: an enigma of microenvironment(s). Cancer Res 2022; 82:4497–4510.
Mirza S, Sharma G, Pandya P, Ralhan R. Demethylating agent 5-aza-2-deoxycytidine enhances susceptibility of breast cancer cells to anticancer agents. Mol Cell Biochem 2010; 342:101–109.
Guler GD, Tindell CA, Pitti R, et al. Repression of stress-induced LINE-1 expression protects cancer cell subpopulations from lethal drug exposure. Cancer Cell 2017; 32:221–237. e13.
Liau BB, Sievers C, Donohue LK, et al. Adaptive chromatin remodeling drives glioblastoma stem cell plasticity and drug tolerance. Cell Stem Cell 2017; 20:233–246. e7.
Dhimolea E, de Matos Simoes R, Kansara D, et al. An embryonic diapause-like adaptation with suppressed myc activity enables tumor treatment persistence. Cancer Cell 2021; 39:240–256. e11.
Marsolier J, Prompsy P, Durand A, et al. H3K27me3 conditions chemotolerance in triple-negative breast cancer. Nat Genet 2022; 54:459–468.
Kalkavan H, Chen MJ, Crawford JC, et al. Sublethal cytochrome c release generates drug-tolerant persister cells. Cell 2022; 185:3356–3374. e22.
Kurppa KJ, Liu Y, To C, et al. Treatment-induced tumor dormancy through YAP-mediated transcriptional reprogramming of the apoptotic pathway. Cancer Cell 2020; 37:104–122. e12.
Moghal N, Li Q, Stewart EL, et al. Single-cell analysis reveals transcriptomic features of drug-tolerant persisters and stromal adaptation in a patient-derived EGFR-mutated lung adenocarcinoma xenograft model. J Thorac Oncol 2023; 18:499–515.
Chang CA, Jen J, Jiang S, et al. Ontogeny and vulnerabilities of drug-tolerant persisters in HER2+ breast cancer. Cancer Discov 2022; 12:1022–1045.
Oren Y, Tsabar M, Cuoco MS, et al. Cycling cancer persister cells arise from lineages with distinct programs. Nature 2021; 596:576–582.
Russo M, Pompei S, Sogari A, et al. A modified fluctuation-test framework characterizes the population dynamics and mutation rate of colorectal cancer persister cells. Nat Genet 2022; 54:976–984.
Maeshiro M, Shinriki S, Liu R, et al. Colonization of distant organs by tumor cells generating circulating homotypic clusters adaptive to fluid shear stress. Sci Rep 2021; 11:6150.
Hanahan D. Hallmarks of cancer: new dimensions. Cancer Discov 2022; 12:31–46.
Tu SM, Estecio MR, Lin SH, Zacharias NM. Stem cell theory of cancer: rude awakening or bad dream from cancer dormancy? Cancers (Basel) 2022; 14:655.
Tomasin R, Bruni-Cardoso A. The role of cellular quiescence in cancer – beyond a quiet passenger. J Cell Sci 2022; 135:jcs259676.
Fenelon JC, Renfree MB. The history of the discovery of embryonic diapause in mammals. Biol Reprod 2018; 99:242–251.
Hussein AM, Balachandar N, Mathieu J, Ruohola-Baker H. Molecular regulators of embryonic diapause and cancer diapause-like state. Cells 2022; 11:2929.
Garcia-Ojalvo J, Bulut-Karslioglu A. On time: developmental timing within and across species. Development 2023; 150:dev201045.
Duy C, Li M, Teater M, et al. Chemotherapy induces senescence-like resilient cells capable of initiating AML recurrence. Cancer Discov 2021; 11:1542.
Manoir S Du, Delpech H, Orsetti B, et al. In high grade ovarian carcinoma, platinum-sensitive tumor recurrence and acquired-resistance derive from quiescent residual cancer cells that overexpress CRYAB, CEACAM6 and SOX2. J Path 2022; 257:367–378.
Tau S, Miller TW. The role of cancer cell bioenergetics in dormancy and drug resistance. Cancer Metastasis Rev 2023; 42:87–98.
You B, Xia T, Gu M, et al. AMPK-mTOR-mediated activation of autophagy promotes formation of dormant polyploid giant cancer cells. Cancer Res 2022; 82:846–858.
Tian X, He Y, Qi L, et al. Autophagy inhibition contributes to apoptosis of PLK4 downregulation-induced dormant cells in colorectal cancer. Int J Biol Sci 2023; 19:2817–2834.
Álvarez-Varela A, Novellasdemunt L, Barriga FM, et al. Mex3a marks drug-tolerant persister colorectal cancer cells that mediate relapse after chemotherapy. Nat Cancer 2022; 3:1052–1070.
Lavado A, Park JY, Paré J, et al. The hippo pathway prevents YAP/TAZ-driven hypertranscription and controls neural progenitor number. Dev Cell 2018; 47:576–591.e8.
Homann L, Rentschler M, Brenner E, et al. IFN-γ and TNF induce senescence and a distinct senescence-associated secretory phenotype in melanoma. Cells 2022; 11:1514.
Saleh T, Gewirtz DA. Considering therapy-induced senescence as a mechanism of tumour dormancy contributing to disease recurrence. Br J Cancer 2022; 126:1363–1365.
Dörr JR, Yu Y, Milanovic M, et al. Synthetic lethal metabolic targeting of cellular senescence in cancer therapy. Nature 2013; 501:421–425.
Kunimasa K, Nagano T, Shimono Y, et al. Glucose metabolism-targeted therapy and withaferin A are effective for epidermal growth factor receptor tyrosine kinase inhibitor-induced drug-tolerant persisters. Cancer Sci 2017; 108:1368–1377.
Bui T, Gu Y, Ancot F, et al. Emergence of β1 integrin-deficient breast tumours from dormancy involves both inactivation of p53 and generation of a permissive tumour microenvironment. Oncogene 2022; 41:527–537.
Scognamiglio R, Cabezas-Wallscheid N, Thier MC, et al. Myc depletion induces a pluripotent dormant state mimicking diapause. Cell 2016; 164:668–680.
Collignon E, Cho B, Furlan G, et al. m6A RNA methylation orchestrates transcriptional dormancy during paused pluripotency. Nat Cell Biol 2023; 25:1279–1289.
Borriello L, Coste A, Traub B, et al. Primary tumor associated macrophages activate programs of invasion and dormancy in disseminating tumor cells. Nat Commun 2022; 13:626.
Sosa MS, Parikh F, Maia AG, et al. NR2F1 controls tumour cell dormancy via SOX9- and RARβ-driven quiescence programmes. Nat Commun 2015; 6:6170.
Wu R, Roy AM, Tokumaru Y, et al. NR2F1, a tumor dormancy marker, is expressed predominantly in cancer-associated fibroblasts and is associated with suppressed breast cancer cell proliferation. Cancers (Basel) 2022; 14:2962.
Evertts AG, Manning AL, Wang X, et al. H4K20 methylation regulates quiescence and chromatin compaction. Mol Biol Cell 2013; 24:3025–3037.
Clements ME, Holtslander L, Edwards C, et al. HDAC inhibitors induce LIFR expression and promote a dormancy phenotype in breast cancer. Oncogene 2021; 40:5314–5326.
Singh DK, Carcamo S, Farias EF, et al. 5-Azacytidine- and retinoic-acid-induced reprogramming of DCCs into dormancy suppresses metastasis via restored TGF-β-SMAD4 signaling. Cell Rep 2023; 42:112560.
Mukherjee A, Bravo-Cordero JJ. Regulation of dormancy during tumor dissemination: the role of the ECM. Cancer Metastasis Rev 2023; 42:99–112.
Fane ME, Chhabra Y, Alicea GM, et al. Stromal changes in the aged lung induce an emergence from melanoma dormancy. Nature 2022; 606:396–405.
Aouad P, Zhang Y, De Martino F, et al. Epithelial-mesenchymal plasticity determines estrogen receptor positive breast cancer dormancy and epithelial reconversion drives recurrence. Nat Commun 2022; 13:4975.
Nobre AR, Dalla E, Yang J, et al. ZFP281 drives a mesenchymal-like dormancy program in early disseminated breast cancer cells that prevents metastatic outgrowth in the lung. Nat Cancer 2022; 3:1165–1180.
Di Martino JS, Nobre AR, Mondal C, et al. A tumor-derived type III collagen-rich ECM niche regulates tumor cell dormancy. Nat Cancer 2022; 3:90–107.
Correia AL, Guimaraes JC, Auf der Maur P, et al. Hepatic stellate cells suppress NK cell-sustained breast cancer dormancy. Nature 2021; 594:566–571.
Tallón de Lara P, Castañón H, Vermeer M, et al. CD39+PD-1+CD8+ T cells mediate metastatic dormancy in breast cancer. Nat Commun 2021; 12:769.
Nobre AR, Risson E, Singh DK, et al. Bone marrow NG2+/Nestin+ mesenchymal stem cells drive DTC dormancy via TGFβ2. Nat Cancer 2021; 2:327–339.
Kim HS, Kim Y, Lim MJ, et al. The p38-activated ER stress-ATF6α axis mediates cellular senescence. FASEB J 2019; 33:2422–2434.
Li B, Huang Y, Ming H, et al. Redox control of the dormant cancer cell life cycle. Cells 2021; 10:2707.
Radnaa E, Richardson L, Goldman B, et al. Stress signaler p38 mitogen-activated kinase activation: a cause for concern? Clin Sci (Lond) 2022; 136:1591–1614.
Kma L, Baruah TJ. The interplay of ROS and the PI3K/Akt pathway in autophagy regulation. Biotechnol Appl Biochem 2022; 69:248–264.
Yuan R, Fan Q, Liang X, et al. Cucurbitacin B inhibits TGF-β1-induced epithelial-mesenchymal transition (EMT) in NSCLC through regulating ROS and PI3K/Akt/mTOR pathways. Chin Med 2022; 17:24.
Gu Y, Bui T, Muller WJ. Exploiting mouse models to recapitulate clinical tumor dormancy and recurrence in breast cancer. Endocrinology 2022; 163:bqac055.
Recasens A, Munoz L. Targeting cancer cell dormancy. Trends Pharmacol Sci 2019; 40:128–141.
Board NL, Moskovljevic M, Wu F, et al. Engaging innate immunity in HIV-1 cure strategies. Nat Rev Immunol 2022; 22:499–512.
Carlson P, Dasgupta A, Grzelak CA, et al. Targeting the perivascular niche sensitizes disseminated tumour cells to chemotherapy. Nat Cell Biol 2019; 21:238–250.
Oliveira G, Wu CJ. Dynamics and specificities of T cells in cancer immunotherapy. Nat Rev Cancer 2023; 23:295–316.
Baldominos P, Barbera-Mourelle A, Barreiro O, et al. Quiescent cancer cells resist T cell attack by forming an immunosuppressive niche. Cell 2022; 185:1694–1708. e19.
Hu J, Sánchez-Rivera FJ, Wang Z, et al. STING inhibits the reactivation of dormant metastasis in lung adenocarcinoma. Nature 2023; 616:806–813.

Auteurs

Evelyne Collignon (E)

Laboratory of Cancer Epigenetics, Faculty of Medicine, ULB-Cancer Research Centre (U-CRC) and Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.

Classifications MeSH