bims-tucedo Biomed News
on Tumor cell dormancy
Issue of 2020‒05‒31
28 papers selected by
Isabel Puig Borreil
Vall d’Hebron Institute of Oncology


  1. PLoS Genet. 2020 May 28. 16(5): e1008743
      Metastasis remains the principle cause of mortality for breast cancer and presents a critical challenge because secondary lesions are often refractory to conventional treatments. While specific genetic alterations are tightly linked to primary tumor development and progression, the role of genetic alteration in the metastatic process is not well-understood. The theory of tumor evolution postulated by Peter Nowell in 1976 has yet to be proven in the context of metastasis. Therefore, in order to investigate how somatic evolution contributes to breast cancer metastasis, we performed exome, whole genome, and RNA sequencing of matched metastatic and primary tumors from pre-clinical mouse models of breast cancer. Here we show that in a treatment-naïve setting, recurrent single nucleotide variants and copy number variation, but not gene fusion events, play key metastasis-driving roles in breast cancer. For instance, we identified recurrent mutations in Kras, a known driver of colorectal and lung tumorigenesis that has not been previously implicated in breast cancer metastasis. However, in a set of in vivo proof-of-concept experiments we show that the Kras G12D mutation is sufficient to significantly promote metastasis using three syngeneic allograft models. The work herein confirms the existence of metastasis-driving mutations and presents a novel framework to identify actionable metastasis-targeted therapies.
    DOI:  https://doi.org/10.1371/journal.pgen.1008743
  2. Leukemia. 2020 May 23.
      Resistance of acute myeloid leukemia (AML) to therapeutic agents is frequent. Consequently, the mechanisms leading to this resistance must be understood and addressed. In this paper, we demonstrate that inhibition of deubiquitinylase USP7 significantly reduces cell proliferation in vitro and in vivo, blocks DNA replication progression and increases cell death in AML. Transcriptomic dataset analyses reveal that a USP7 gene signature is highly enriched in cells from AML patients at relapse, as well as in residual blasts from patient-derived xenograft (PDX) models treated with clinically relevant doses of cytarabine, which indicates a relationship between USP7 expression and resistance to therapy. Accordingly, single-cell analysis of AML patient samples at relapse versus at diagnosis showed that a gene signature of the pre-existing subpopulation responsible for relapse is enriched in transcriptomes of patients with a high USP7 level. Furthermore, we found that USP7 interacts and modulates CHK1 protein levels and functions in AML. Finally, we demonstrated that USP7 inhibition acts in synergy with cytarabine to kill AML cell lines and primary cells of patients with high USP7 levels. Altogether, these data demonstrate that USP7 is both a marker of resistance to chemotherapy and a potential therapeutic target in overcoming resistance to treatment.
    DOI:  https://doi.org/10.1038/s41375-020-0878-x
  3. Oncogene. 2020 May 30.
      Estrogen receptor (ER) positive breast cancer is frequently sensitive to endocrine therapy. Multiple mechanisms of endocrine therapy resistance have been identified, including cancer stem-like cell (CSC) activity. Here we investigate SFX-01, a stabilised formulation of sulforaphane (SFN), for its effects on breast CSC activity in ER+ preclinical models. SFX-01 reduced mammosphere formation efficiency (MFE) of ER+ primary and metastatic patient samples. Both tamoxifen and fulvestrant increased MFE and aldehyde dehydrogenase (ALDH) activity of patient-derived xenograft (PDX) tumors, which was reversed by combination with SFX-01. SFX-01 significantly reduced tumor-initiating cell frequency in secondary transplants and reduced the formation of spontaneous lung micrometastases by PDX tumors in mice. Mechanistically, we establish that both tamoxifen and fulvestrant induce STAT3 phosphorylation. SFX-01 suppressed phospho-STAT3 and SFN directly bound STAT3 in patient and PDX samples. Analysis of ALDH+ cells from endocrine-resistant patient samples revealed activation of STAT3 target genes MUC1 and OSMR, which were inhibited by SFX-01 in patient samples. Increased expression of these genes after 3 months' endocrine treatment of ER+ patients (n = 68) predicted poor prognosis. Our data establish the importance of STAT3 signaling in CSC-mediated resistance to endocrine therapy and the potential of SFX-01 for improving clinical outcomes in ER+ breast cancer.
    DOI:  https://doi.org/10.1038/s41388-020-1335-z
  4. Neuro Oncol. 2020 May 27. pii: noaa128. [Epub ahead of print]
      BACKGROUND: Residual disease of glioblastoma (GBM) causes recurrence. However, targeting residual cells have failed due to their inaccessibility and our lack of understanding their survival mechanisms to radiation therapy. Here we deciphered residual cell specific survival mechanism essential for GBM relapse.METHODS: Therapy Resistant Residual (RR) cells were captured from primary patient samples and cell line models mimicking clinical scenario of radiation resistance. Molecular signaling of resistance in RR cells was identified using RNA sequencing, genetic and pharmacological perturbations, overexpression systems, molecular and biochemical assays. Findings were validated in patient samples and orthotopic mouse model.
    RESULTS: RR cells form more aggressive tumors than the parental cells in orthotopic mouse model. Upon radiation-induced damage, RR cells preferentially activated non homologous end joining (NHEJ) repair pathway, up-regulating Ku80 and Artemis while down-regulating of Mre11 at protein but not RNA levels. Mechanistically, RR cells upregulate SETMAR, mediating high levels of H3K36me2 and global euchromatization. High H3K36me2 leads to efficiently recruiting NHEJ proteins. Conditional knockdown of SETMAR in RR cells induced irreversible senescence partly mediated by reduced H3K36me2. RR cells expressing mutant H3K36A could not retain Ku80 at DSBs thus, compromising NHEJ repair leading to apoptosis and abrogation of tumorigenicity in vitro and in vivo. Pharmacological inhibition of NHEJ pathway phenocopied H3K36 mutation effect, confirming dependency of RR cells on NHEJ pathway for their survival.
    CONCLUSIONS: We demonstrate that SETMAR- NHEJ regulatory axis is essential for the survival of clinically relevant radiation resistant residual cells, abrogation of which prevents recurrence in GBM.
    Keywords:  Glioblastoma; NHEJ; SETMAR; radiation-resistance; residual disease
    DOI:  https://doi.org/10.1093/neuonc/noaa128
  5. Trends Cancer. 2020 Jun;pii: S2405-8033(20)30081-9. [Epub ahead of print]6(6): 489-505
      Chemoresistance is a major factor driving tumour relapse and the high rates of cancer-related deaths. Understanding how cancer cells overcome chemotherapy-induced cell death is critical in promoting patient survival. One emerging mechanism of chemoresistance is the tumour cell secretome (TCS), an array of protumorigenic factors released by tumour cells. Chemotherapy exposure can also alter the composition of the TCS, known as therapy-induced TCS, and can promote tumour relapse and the formation of an immunosuppressive tumour microenvironment (TME). Here, we outline how the TCS can protect cancer cells from chemotherapy-induced cell death. We also highlight recent evidence describing how therapy-induced TCS can impact cancer stem cell (CSC) expansion and tumour-associated immune cells to enable tumour regrowth and antitumour immunity.
    Keywords:  cancer stem cells (CSCs); chemoresistance; immune escape, tumour cell secretome (TCS); tumour microenvironment (TME); tumour relapse
    DOI:  https://doi.org/10.1016/j.trecan.2020.02.020
  6. Proc Natl Acad Sci U S A. 2020 May 29. pii: 201918307. [Epub ahead of print]
      Acute myeloid leukemia (AML) is a deadly hematologic malignancy with poor prognosis, particularly in the elderly. Even among individuals with favorable-risk disease, approximately half will relapse with conventional therapy. In this clinical circumstance, the determinants of relapse are unclear, and there are no therapeutic interventions that can prevent recurrent disease. Mutations in the transcription factor CEBPA are associated with favorable risk in AML. However, mutations in the growth factor receptor CSF3R are commonly co-occurrent in CEBPA mutant AML and are associated with an increased risk of relapse. To develop therapeutic strategies for this disease subset, we performed medium-throughput drug screening on CEBPA/CSF3R mutant leukemia cells and identified sensitivity to inhibitors of lysine-specific demethylase 1 (LSD1). Treatment of CSF3R/CEBPA mutant leukemia cells with LSD1 inhibitors reactivates differentiation-associated enhancers driving immunophenotypic and morphologic differentiation. LSD1 inhibition is ineffective as monotherapy but demonstrates synergy with inhibitors of JAK/STAT signaling, doubling median survival in vivo. These results demonstrate that combined inhibition of JAK/STAT signaling and LSD1 is a promising therapeutic strategy for CEBPA/CSF3R mutant AML.
    Keywords:  CSF3R; LSD1; acute myeloid leukemia; epigenetics; targeted
    DOI:  https://doi.org/10.1073/pnas.1918307117
  7. Mol Cancer Res. 2020 May 27. pii: molcanres.1245.2019. [Epub ahead of print]
      The increased treatment of metastatic castration resistant prostate cancer (mCRPC) with second-generation anti-androgen therapies (ADT) has coincided with a greater incidence of lethal, aggressive variant prostate cancer (AVPC) tumors that have lost dependence on androgen receptor (AR) signaling. These AR independent tumors may also transdifferentiate to express neuroendocrine lineage markers and are termed neuroendocrine prostate cancer (NEPC). Recent evidence suggests kinase signaling may be an important driver of NEPC. To identify targetable kinases in NEPC, we performed global phosphoproteomics comparing several AR independent to AR dependent prostate cancer cell lines and identified multiple altered signaling pathways, including enrichment of RET kinase activity in the AR independent cell lines. Clinical NEPC patient samples and NEPC patient derived xenografts displayed upregulated RET transcript and RET pathway activity. Genetic knockdown or pharmacological inhibition of RET kinase in multiple mouse and human models of NEPC dramatically reduced tumor growth and decreased cell viability. Our results suggest that targeting RET in NEPC tumors with high RET expression could be an effective treatment option. Currently, there are limited treatment options for patients with aggressive neuroendocrine prostate cancer and none are curative. Implications: Identification of aberrantly expressed RET kinase as a driver of tumor growth in multiple models of NEPC provides a significant rationale for testing the clinical application of RET inhibitors in AVPC patients.
    DOI:  https://doi.org/10.1158/1541-7786.MCR-19-1245
  8. Sci Transl Med. 2020 May 27. pii: eaaz5387. [Epub ahead of print]12(545):
      The functions of immune cells in brain metastases are unclear because the brain has traditionally been considered "immune privileged." However, we found that a subgroup of immunosuppressive neutrophils is recruited into the brain, enabling brain metastasis development. In brain metastatic cells, enhancer of zeste homolog 2 (EZH2) is highly expressed and phosphorylated at tyrosine-696 (pY696)-EZH2 by nuclear-localized Src tyrosine kinase. Phosphorylation of EZH2 at Y696 changes its binding preference from histone H3 to RNA polymerase II, which consequently switches EZH2's function from a methyltransferase to a transcription factor that increases c-JUN expression. c-Jun up-regulates protumorigenic inflammatory cytokines, including granulocyte colony-stimulating factor (G-CSF), which recruits Arg1+- and PD-L1+ immunosuppressive neutrophils into the brain to drive metastasis outgrowth. G-CSF-blocking antibodies or immune checkpoint blockade therapies combined with Src inhibitors impeded brain metastasis in multiple mouse models. These findings indicate that pY696-EZH2 can function as a methyltransferase-independent transcription factor to facilitate the brain infiltration of immunosuppressive neutrophils, which could be clinically targeted for brain metastasis treatment.
    DOI:  https://doi.org/10.1126/scitranslmed.aaz5387
  9. Nat Commun. 2020 May 26. 11(1): 2641
      Acquired resistance to PARP inhibitors (PARPi) is a major challenge for the clinical management of high grade serous ovarian cancer (HGSOC). Here, we demonstrate CX-5461, the first-in-class inhibitor of RNA polymerase I transcription of ribosomal RNA genes (rDNA), induces replication stress and activates the DNA damage response. CX-5461 co-operates with PARPi in exacerbating replication stress and enhances therapeutic efficacy against homologous recombination (HR) DNA repair-deficient HGSOC-patient-derived xenograft (PDX) in vivo. We demonstrate CX-5461 has a different sensitivity spectrum to PARPi involving MRE11-dependent degradation of replication forks. Importantly, CX-5461 exhibits in vivo single agent efficacy in a HGSOC-PDX with reduced sensitivity to PARPi by overcoming replication fork protection. Further, we identify CX-5461-sensitivity gene expression signatures in primary and relapsed HGSOC. We propose CX-5461 is a promising therapy in combination with PARPi in HR-deficient HGSOC and also as a single agent for the treatment of relapsed disease.
    DOI:  https://doi.org/10.1038/s41467-020-16393-4
  10. Autophagy. 2020 May 27. 1-2
      Major histocompatibility complex class I (MHC-I) is a key molecule in anti-tumor adaptive immunity. MHC-I is essential for endogenous antigen presentation by cancer cells and subsequent recognition and clearance by CD8+ T cells. Defects in MHC-I expression occur frequently in several cancers, leading to impaired antigen presentation, immune evasion and/or resistance to immune checkpoint blockade (ICB) therapy. Pancreatic ductal adenocarcinoma (PDAC), a deadly malignancy with dismal patient prognosis, is resistant to ICB and shows frequent downregulation of MHC-I independent of genetic mutations abrogating MHC-I expression. Previously, we showed that PDAC cells exhibit elevated levels of autophagy and lysosomal biogenesis, which together support the survival and growth of PDAC tumors via both cell-autonomous and non-cell-autonomous mechanisms. In our recent study, we have identified NBR1-mediated selective macroautophagy/autophagy of MHC-I as a novel mechanism that facilitates immune evasion by PDAC cells. Importantly, autophagy or lysosome inhibition restores MHC-I expression, leading to enhanced anti-tumor T cell immunity and improved response to ICB in transplanted tumor models in syngeneic host mice. Our results highlight a previously unknown function of autophagy and the lysosome in regulation of immunogenicity in PDAC, and provide a novel therapeutic strategy for targeting this deadly disease.
    Keywords:  MHC-I; Pancreatic cancer; anti-tumor immunity; autophagy; immune checkpoint blockade; lysosome
    DOI:  https://doi.org/10.1080/15548627.2020.1769973
  11. Trends Cancer. 2020 May 21. pii: S2405-8033(20)30156-4. [Epub ahead of print]
      Tumor metastases, that is, the development of secondary tumors in organs distant from the primary tumor, and their treatment remain a serious problem in cancer therapy. The unique challenges for tracking and treating tumor metastases lie in the small size, high heterogeneity, and wide dispersion to distant organs of metastases. Recently, nanomedicines, with the capacity to precisely deliver therapeutic agents to both primary and secondary tumors, have demonstrated many potential benefits for metastatic cancer theranostics. Given the remarkable progression in emerging nanotherapeutics for antimetastatic treatment, it is timely to summarize the latest advances in this field. This review highlights the rationale, advantages, and challenges for integrating biomedical nanotechnology with cancer biology to develop antimetastatic nanotherapeutics.
    Keywords:  circulating tumor cells; combination therapy; microenvironment; nanotherapeutics; tumor metastasis
    DOI:  https://doi.org/10.1016/j.trecan.2020.05.001
  12. Gastroenterology. 2020 May 21. pii: S0016-5085(20)34705-3. [Epub ahead of print]
      BACKGROUND & AIMS: Pancreatic tumor cells release extracellular vesicles (sEVs, exosomes) that contain lipids and proteins, RNA, and DNA molecules might promote formation of metastases. It is not clear what cargo these vesicles contain and how they are released. Protein kinase D1 (PRKD1) inhibits cell motility and is believed to be dysregulated in pancreatic ductal adenocarcinomas (PDACs). We investigated whether it regulates production of sEVs in pancreatic cancer cells and their ability to form pre-metastatic niches for pancreatic cancer cells in mice.METHODS: We analyzed data from UALCAN and human pancreatic tissue microarrays to compare levels of PRKD1 between tumor and non-tumor tissues. We studied mice with pancreas-specific disruption of Prkd1 (PRKD1KO mice), mice that express oncogenic KRAS (KC mice), and KC mice with disruption of Prkd1 (PRKD1KO-KC mice). Subcutaneous xenograft tumors were grown in NSG mice from Panc1 cells; some mice were then given injections of sEVs. Pancreata and lung tissues from mice were analyzed by histology, immunohistochemistry, and/or quantitative PCR; we performed nanoparticle tracking analysis of plasma sEVs. The Prkd1 gene was disrupted in Panc1 cells using CRISPR-Cas9 or knocked down with small hairpin RNAs, or PRKD1 activity was inhibited with the selective inhibitor CRT0066101. Pancreatic cancer cell lines were analyzed by gene-expression microarray, quantitative PCR, immunoblot, and immunofluorescence analyses. sEVs secreted by Panc1 cell lines were analyzed by flow cytometry, transmission electron microscopy, and mass spectrometry.
    RESULTS: Levels of PRKD1 were reduced in human PDAC tissues compared with non-tumor tissues. PRKD1KO-KC mice developed more pancreatic intraepithelial neoplasia, at a faster rate, than KC mice, and had more lung metastases and significantly shorter average survival time. Serum from PRKD1KO-KC mice had increased levels of sEVs, compared with KC mice. Pancreatic cancer cells with loss or inhibition of PRKD1 increased secretion of sEVs; loss of PRKD1 reduced phosphorylation of its substrate, cortactin, resulting in increased F-actin levels at the plasma membrane. sEVs from cells with loss or reduced expression of PRKD1 had altered content, and injection of these sEVs into mice increased metastasis of xenograft tumors to lung, compared with sEVs from pancreatic cells that expressed PRKD1. PRKD1-deficient pancreatic cancer cells showed increased loading of integrin α6β4 into sEVs-a process that required CD82.
    CONCLUSIONS: Human PDAC have reduced levels of PRKD1 compared with non-tumor pancreatic tissues. Loss of PRKD1 results in reduced phosphorylation of cortactin in pancreatic cancer cell lines, resulting in increased in F-actin at the plasma membrane and increased release of sEVs, with altered content. These sEVs promote metastasis of xenograft and pancreatic tumors to lung in mice.
    Keywords:  cytoskeletal organization; cytoskeleton; invasion; multivesicular bodies (MVBs)
    DOI:  https://doi.org/10.1053/j.gastro.2020.05.052
  13. Nat Med. 2020 May 29.
      PD-1 blockade has transformed the management of advanced clear cell renal cell carcinoma (ccRCC), but the drivers and resistors of the PD-1 response remain incompletely elucidated. Here, we analyzed 592 tumors from patients with advanced ccRCC enrolled in prospective clinical trials of treatment with PD-1 blockade by whole-exome and RNA sequencing, integrated with immunofluorescence analysis, to uncover the immunogenomic determinants of the therapeutic response. Although conventional genomic markers (such as tumor mutation burden and neoantigen load) and the degree of CD8+ T cell infiltration were not associated with clinical response, we discovered numerous chromosomal alterations associated with response or resistance to PD-1 blockade. These advanced ccRCC tumors were highly CD8+ T cell infiltrated, with only 27% having a non-infiltrated phenotype. Our analysis revealed that infiltrated tumors are depleted of favorable PBRM1 mutations and enriched for unfavorable chromosomal losses of 9p21.3, as compared with non-infiltrated tumors, demonstrating how the potential interplay of immunophenotypes with somatic alterations impacts therapeutic efficacy.
    DOI:  https://doi.org/10.1038/s41591-020-0839-y
  14. Trends Cancer. 2020 Jun;pii: S2405-8033(20)30077-7. [Epub ahead of print]6(6): 454-461
      Intratumor heterogeneity is a key hallmark of cancer that contributes to progression and therapeutic resistance. Phenotypic heterogeneity is in part caused by Darwinian selection of subclones that arise by random (epi)genetic aberrations. In addition, cancer cells are endowed with increased cellular plasticity compared with their normal counterparts, further adding to their heterogeneous behavior. However, the molecular mechanisms underpinning cancer cell plasticity are incompletely understood. Here, I outline the hypothesis that cancer-associated perturbations collectively disrupt normal gene regulatory networks (GRNs) by increasing their entropy. Importantly, in this model both somatic driver and passenger alterations contribute to 'perturbation-driven entropy', thereby increasing phenotypic heterogeneity and evolvability. This additional layer of heterogeneity may contribute to our understanding of cancer evolution and therapeutic resistance.
    Keywords:  cancer heterogeneity; entropy; gene regulatory networks; therapeutic resistance
    DOI:  https://doi.org/10.1016/j.trecan.2020.02.016
  15. Cancer Discov. 2020 May 29.
      Whether metastases were seeded mono- or polyclonally depended on cancer site and treatment.
    DOI:  https://doi.org/10.1158/2159-8290.CD-RW2020-082
  16. Nat Commun. 2020 May 29. 11(1): 2682
      Pancreatic cancer stem cells (PaCSCs) drive pancreatic cancer tumorigenesis, chemoresistance and metastasis. While eliminating this subpopulation of cells would theoretically result in tumor eradication, PaCSCs are extremely plastic and can successfully adapt to targeted therapies. In this study, we demonstrate that PaCSCs increase expression of interferon-stimulated gene 15 (ISG15) and protein ISGylation, which are essential for maintaining their metabolic plasticity. CRISPR-mediated ISG15 genomic editing reduces overall ISGylation, impairing PaCSCs self-renewal and their in vivo tumorigenic capacity. At the molecular level, ISG15 loss results in decreased mitochondrial ISGylation concomitant with increased accumulation of dysfunctional mitochondria, reduced oxidative phosphorylation (OXPHOS) and impaired mitophagy. Importantly, disruption in mitochondrial metabolism affects PaCSC metabolic plasticity, making them susceptible to prolonged inhibition with metformin in vivo. Thus, ISGylation is critical for optimal and efficient OXPHOS by ensuring the recycling of dysfunctional mitochondria, and when absent, a dysregulation in mitophagy occurs that negatively impacts PaCSC stemness.
    DOI:  https://doi.org/10.1038/s41467-020-16395-2
  17. Mol Cancer. 2020 May 27. 19(1): 96
      Gastric cancer is a deadly disease and remains the third leading cause of cancer-related death worldwide. The 5-year overall survival rate of patients with early-stage localized gastric cancer is more than 60%, whereas that of patients with distant metastasis is less than 5%. Surgical resection is the best option for early-stage gastric cancer, while chemotherapy is mainly used in the middle and advanced stages of this disease, despite the frequently reported treatment failure due to chemotherapy resistance. Therefore, there is an unmet medical need for identifying new biomarkers for the early diagnosis and proper management of patients, to achieve the best response to treatment. Long non-coding RNAs (lncRNAs) in body fluids have attracted widespread attention as biomarkers for early screening, diagnosis, treatment, prognosis, and responses to drugs due to the high specificity and sensitivity. In the present review, we focus on the clinical potential of lncRNAs as biomarkers in liquid biopsies in the diagnosis and prognosis of gastric cancer. We also comprehensively discuss the roles of lncRNAs and their molecular mechanisms in gastric cancer chemoresistance as well as their potential as therapeutic targets for gastric cancer precision medicine.
    Keywords:  Cancer treatment; Chemoresistance; Early diagnosis; Gastric cancer; LncRNA; Precision medicine
    DOI:  https://doi.org/10.1186/s12943-020-01219-0
  18. Cancer Discov. 2020 May 28. pii: CD-19-1409. [Epub ahead of print]
      Mechanism-based strategies to overcome resistance to programmed cell death-1 (PD-1) blockade therapy are urgently needed. We developed genetic acquired resistant models of JAK1, JAK2 and B2M loss of function mutations by gene knockout in human and murine cell lines. Human melanoma cell lines with JAK1/2 knockout became insensitive to interferon (IFN)-induced antitumor effects, while B2M knockout were no longer recognized by antigen-specific T cells and hence resistant to cytotoxicity. All of these mutations led to resistance to anti-PD-1 therapy in vivo. JAK1/2 knockout resistance could be overcome with the activation of innate and adaptive immunity by intratumoral Toll-like receptor 9 (TLR9) agonist administration together with anti-PD-1, mediated by natural killer (NK) and CD8 T cells. B2M knockout resistance could be overcome by NK and CD4 T cell activation using the CD122 preferential interleukin 2 (IL-2) agonist bempegaldesleukin. Therefore, mechanistically-designed combination therapies can overcome genetic resistance to PD-1 blockade therapy.
    DOI:  https://doi.org/10.1158/2159-8290.CD-19-1409
  19. Nat Cell Biol. 2020 May 25.
      It is well accepted that cancers co-opt the microenvironment for their growth. However, the molecular mechanisms that underlie cancer-microenvironment interactions are still poorly defined. Here, we show that Rho-associated kinase (ROCK) in the mammary tumour epithelium selectively actuates protein-kinase-R-like endoplasmic reticulum kinase (PERK), causing the recruitment and persistent education of tumour-promoting cancer-associated fibroblasts (CAFs), which are part of the cancer microenvironment. An analysis of tumours from patients and mice reveals that cysteine-rich with EGF-like domains 2 (CRELD2) is the paracrine factor that underlies PERK-mediated CAF education downstream of ROCK. We find that CRELD2 is regulated by PERK-regulated ATF4, and depleting CRELD2 suppressed tumour progression, demonstrating that the paracrine ROCK-PERK-ATF4-CRELD2 axis promotes the progression of breast cancer, with implications for cancer therapy.
    DOI:  https://doi.org/10.1038/s41556-020-0523-y
  20. Nat Genet. 2020 May 25.
      Genetic diversity among metastases is poorly understood but contains important information about disease evolution at secondary sites. Here we investigate inter- and intra-lesion heterogeneity for two types of metastases that associate with different clinical outcomes: lymph node and distant organ metastases in human colorectal cancer. We develop a rigorous mathematical framework for quantifying metastatic phylogenetic diversity. Distant metastases are typically monophyletic and genetically similar to each other. Lymph node metastases, in contrast, display high levels of inter-lesion diversity. We validate these findings by analyzing 317 multi-region biopsies from an independent cohort of 20 patients. We further demonstrate higher levels of intra-lesion heterogeneity in lymph node than in distant metastases. Our results show that fewer primary tumor lineages seed distant metastases than lymph node metastases, indicating that the two sites are subject to different levels of selection. Thus, lymph node and distant metastases develop through fundamentally different evolutionary mechanisms.
    DOI:  https://doi.org/10.1038/s41588-020-0633-2
  21. Cancer Discov. 2020 May 28.
      Circulating tumor DNA (ctDNA) may be a useful biomarker for minimal residual disease (MRD) in patients with early-stage non-small cell lung cancer-and MRD may be a good predictor of relapse. In the TRACERx study, a ctDNA assay confirmed MRD negativity in more than 99% of patients-and detected MRD in patients who relapsed before their disease was picked up by standard imaging.
    DOI:  https://doi.org/10.1158/2159-8290.CD-ND2020-010
  22. Trends Cancer. 2020 May 26. pii: S2405-8033(20)30155-2. [Epub ahead of print]
      Tunneling nanotubes (TNTs) are thin membrane tubes connecting remote cells and allowing the transfer of cellular content. TNTs have been reported in several cancer in vitro, ex vivo, and in vivo models. Cancer cells exploit TNT-like connections to exchange material between themselves or with the tumoral microenvironment. Cells acquire new abilities (e.g., enhanced metabolic plasticity, migratory phenotypes, angiogenic ability, and therapy resistance) via these exchanges, contributing to cancer aggressiveness. Here, we review the morphological and functional features of TNT-like structures and their impact on cancer progression and resistance to therapies. Finally, we discuss the case of glioblastoma (GBM), in which a functional and resistant network between cancer cells in an in vivo model has been described for the first time.
    Keywords:  cancer; cell-to-cell communication; glioblastoma; tunneling nanotubes
    DOI:  https://doi.org/10.1016/j.trecan.2020.04.012
  23. Cell Death Differ. 2020 May 26.
      TP53 wild-type breast tumors rarely undergo a complete pathological response after chemotherapy treatment. These patients have an extremely poor survival rate and studies show these tumors preferentially undergo senescence instead of apoptosis. These senescent cells persist after chemotherapy and secrete cytokines and chemokines comprising the senescence associated secretory phenotype, which promotes survival, proliferation, and metastasis. We hypothesized that eliminating senescent tumor cells would improve chemotherapy response and extend survival. Previous studies have shown "senolytic" agents selectively kill senescent normal cells, but their efficacy in killing chemotherapy-induced senescent cancer cells is unknown. We show that ABT-263, a BH3 mimetic that targets antiapoptotic proteins BCL2/BCL-XL/BCL-W, had no effect on proliferating cells, but rapidly and selectively induced apoptosis in a subset of chemotherapy-treated cancer cells, though sensitivity required days to develop. Low NOXA expression conferred resistance to ABT-263 in some cells, necessitating additional MCL1 inhibition. Gene editing confirmed breast cancer cells relied on BCL-XL or BCL-XL/MCL1 for survival in senescence. In a mouse model of breast cancer, ABT-263 treatment following chemotherapy led to apoptosis, greater tumor regression, and longer survival. Our results reveal cancer cells that have survived chemotherapy by entering senescence can be eliminated using BH3 mimetic drugs that target BCL-XL or BCL-XL/MCL1. These drugs could help minimize residual disease and extend survival in breast cancer patients that otherwise have a poor prognosis and are most in need of improved therapies.
    DOI:  https://doi.org/10.1038/s41418-020-0564-6
  24. Cancer Cell. 2020 May 25. pii: S1535-6108(20)30259-2. [Epub ahead of print]
      In a recent Nature paper, Yamamoto et al. demonstrate that, in the particular context of pancreatic carcinoma, autophagy causes the continuous destruction of major histocompatibility complex class I (MHC-I) proteins. Suppression of autophagy favors MHC-I re-appearance on the surface of malignant cells, facilitating their clearance by cytotoxic T lymphocytes.
    DOI:  https://doi.org/10.1016/j.ccell.2020.05.009
  25. Cancers (Basel). 2020 May 22. pii: E1323. [Epub ahead of print]12(5):
      Treatments of metastatic melanoma underwent an impressive development over the past few years, with the emergence of small molecule inhibitors targeting mutated proteins, such as BRAF, NRAS, or cKIT. However, since a significant proportion of patients acquire resistance to these therapies, new strategies are currently being considered to overcome this issue. For this purpose, melanoma cell lines with mutant BRAF, NRAS, or cKIT and with acquired resistances to BRAF, MEK, or cKIT inhibitors, respectively, were investigated using both 1H-NMR-based metabonomic and protein microarrays. The 1H-NMR profiles highlighted a similar go and return pattern in the metabolism of the BRAF, NRAS, and cKIT mutated cell lines. Indeed, melanoma cells exposed to mutation-specific inhibitors underwent metabolic disruptions following acute exposure but partially recovered their basal metabolism in long-term exposure, most likely acquiring resistance skills. The protein microarrays inquired about the potential cellular mechanisms used by the resistant cells to escape drug treatment, by showing decreased levels of proteins linked to the drug efficacy, especially in the downstream part of the MAPK signaling pathway. Integrating metabonomic and proteomic findings revealed some metabolic pathways (i.e., glutaminolysis, choline metabolism, glutathione production, glycolysis, oxidative phosphorylation) and key proteins (i.e., EPHA2, DUSP4, and HIF-1A) as potential targets to discard drug resistance.
    Keywords:  cancer metabolic reprogramming; metabolic switch; metabonomics; metastatic melanoma; proteomics; resistance to drugs; targeted therapies
    DOI:  https://doi.org/10.3390/cancers12051323
  26. Cancer Discov. 2020 May 29.
      Olaparib has solidified its place as a standard maintenance therapy for patients with platinum-sensitive relapsed ovarian cancer who have BRCA mutations. In the phase III SOLO 2 trial, the drug extended overall survival by more than a year in these patients compared with a placebo.
    DOI:  https://doi.org/10.1158/2159-8290.CD-NB2020-048
  27. Nat Commun. 2020 May 27. 11(1): 2661
      RNA G-quadruplexes (RG4s) are four-stranded structures known to control mRNA translation of cancer relevant genes. RG4 formation is pervasive in vitro but not in cellulo, indicating the existence of poorly characterized molecular machinery that remodels RG4s and maintains them unfolded. Here, we performed a quantitative proteomic screen to identify cytosolic proteins that interact with a canonical RG4 in its folded and unfolded conformation. Our results identified hnRNP H/F as important components of the cytoplasmic machinery modulating the structural integrity of RG4s, revealed their function in RG4-mediated translation and uncovered the underlying molecular mechanism impacting the cellular stress response linked to the outcome of glioblastoma.
    DOI:  https://doi.org/10.1038/s41467-020-16168-x
  28. Cell. 2020 May 22. pii: S0092-8674(20)30561-4. [Epub ahead of print]
      Brain malignancies can either originate from within the CNS (gliomas) or invade from other locations in the body (metastases). A highly immunosuppressive tumor microenvironment (TME) influences brain tumor outgrowth. Whether the TME is predominantly shaped by the CNS micromilieu or by the malignancy itself is unknown, as is the diversity, origin, and function of CNS tumor-associated macrophages (TAMs). Here, we have mapped the leukocyte landscape of brain tumors using high-dimensional single-cell profiling (CyTOF). The heterogeneous composition of tissue-resident and invading immune cells within the TME alone permitted a clear distinction between gliomas and brain metastases (BrM). The glioma TME presented predominantly with tissue-resident, reactive microglia, whereas tissue-invading leukocytes accumulated in BrM. Tissue-invading TAMs showed a distinctive signature trajectory, revealing tumor-driven instruction along with contrasting lymphocyte activation and exhaustion. Defining the specific immunological signature of brain tumors can facilitate the rational design of targeted immunotherapy strategies.
    Keywords:  T cells; Tregs; brain metastases; exhaustion; glioma; macrophages; mass cytometry; microglia; monocytes; tumor microenvironment
    DOI:  https://doi.org/10.1016/j.cell.2020.04.055