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Dana-Farber Research Publication 04.01.2024

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April 01, 2024

This twice-monthly newsletter highlights the research endeavors at Dana-Farber Cancer Institute, noting recently published papers available from PubMed where Dana-Farber faculty are listed as first or senior authors. If you are a Dana-Farber faculty member and you think your paper is missing from Research News, please let us know at: Michael_buller@dfci.harvard.edu.

 

Blood

Differentiation of BCMA-Specific Induced Pluripotent Stem Cells into Rejuvenated CD8??+ T Cells Targeting Multiple Myeloma

Bae J, Kitayama S, Herbert Z, Daheron L, Kurata K, Keskin DB, Livak K, Li S, Tarannum M, Romee R, Samur M, Munshi NC, Ritz J, Anderson KC

A major hurdle in adoptive T-cell therapy is cell exhaustion and failure to maintain antitumor responses. Here, we introduce an induced pluripotent stem cell (iPSC) strategy for reprogramming and revitalizing precursor exhausted B-cell maturation antigen (BCMA)-specific T cells to effectively target multiple myeloma (MM). Heteroclitic BCMA72-80 (YLMFLLRKI)-specific CD8+ memory cytotoxic T lymphocytes (CTL) were epigenetically reprogrammed to a pluripotent state, developed into hematopoietic progenitor cells (CD34+ CD43+/CD14- CD235a-), differentiated into the T-cell lineage and evaluated for their polyfunctional activities against MM. The final T-cell products demonstrated (1) mature CD8??+ memory phenotype, (2) high expression of activation or costimulatory molecules (CD38, CD28, and 41BB), (3) no expression of immune checkpoint and senescence markers (CTLA4, PD1, LAG3, and TIM3; CD57), and (4) robust proliferation and polyfunctional immune responses to MM. The BCMA-specific iPSC-T cells possessed a single T-cell receptor clonotype with cognate BCMA peptide recognition and specificity for targeting MM. RNA sequencing analyses revealed distinct genome-wide shifts and a distinctive transcriptional profile in selected iPSC clones, which can develop CD8??+ memory T cells. This includes a repertoire of gene regulators promoting T-cell lineage development, memory CTL activation, and immune response regulation (LCK, IL7R, 4-1BB, TRAIL, GZMB, FOXF1, and ITGA1). This study highlights the potential application of iPSC technology to an adaptive T-cell therapy protocol and identifies specific transcriptional patterns that could serve as a biomarker for selection of suitable iPSC clones for the successful development of antigen-specific CD8??+ memory T cells to improve the outcome in patients with MM.


 

Blood

Low-Frequency Inherited Complement Receptor Variants are Associated with Purpura Fulminans

Bendapudi PK, Nazeen S, Ryu J, Söylemez O, Robbins A, Rouaisnel B, O'Neil JK, Pokhriyal R, Yang M, Colling M, Bouzinier M, Tomczak L, Collier L, Barrios D, Toth-Petroczy A, Krier J, Fieg E, Dzik WH, Pozdnyakova O, Nardi V, Maas R, Sunyaev S, Losman JA

Extreme disease phenotypes can provide key insights into the pathophysiology of common conditions, but studying such cases is challenging due to their rarity and the limited statistical power of existing methods. Herein, we used a novel approach to pathway-based mutational burden testing, the rare variant trend test (RVTT), to investigate genetic risk factors for an extreme form of sepsis-induced coagulopathy, infectious purpura fulminans (PF). In addition to prospective patient sample collection, we electronically screened over 10.4 million medical records from 4 large hospital systems and identified historical cases of PF for which archived specimens were available to perform germline whole-exome sequencing. We found a significantly increased burden of low-frequency, putatively function-altering variants in the complement system in patients with PF compared with unselected patients with sepsis (P = .01). A multivariable logistic regression analysis found that the number of complement system variants per patient was independently associated with PF after controlling for age, sex, and disease acuity (P = .01). Functional characterization of PF-associated variants in the immunomodulatory complement receptors CR3 and CR4 revealed that they result in partial or complete loss of anti-inflammatory CR3 function and/or gain of proinflammatory CR4 function. Taken together, these findings suggest that inherited defects in CR3 and CR4 predispose to the maladaptive hyperinflammation that characterizes severe sepsis with coagulopathy.


 

Cancer Cell

Revisiting TNM Staging for EBV-Related Nasopharyngeal Carcinoma

Dennis M, Haddad R

Advances in imaging and novel treatment approaches might have outpaced the prognostic capabilities of the current AJCC/UICC TNM 8th edition for staging nasopharyngeal carcinoma (NPC). In this issue of Cancer Cell, Du et al. propose a new TNM-9 classification that incorporates these updates.


 

Cancer Discovery

Integrative Analyses of Tumor and Peripheral Biomarkers in the Treatment of Advanced Renal Cell Carcinoma

Choueiri TK, Braun DA

The phase III JAVELIN Renal 101 trial demonstrated prolonged progression-free survival (PFS) in patients (N = 886) with advanced renal cell carcinoma treated with first-line avelumab + axitinib (A+Ax) versus sunitinib. We report novel findings from integrated analyses of longitudinal blood samples and baseline tumor tissue. PFS was associated with elevated lymphocyte levels in the sunitinib arm and an abundance of innate immune subsets in the A+Ax arm. Treatment with A+Ax led to greater T-cell repertoire modulation and less change in T-cell numbers versus sunitinib. In the A+Ax arm, patients with tumors harboring mutations in ?2 of 10 previously identified PFS-associated genes (double mutants) had distinct circulating and tumor-infiltrating immunologic profiles versus those with wild-type or single-mutant tumors, suggesting a role for non-T-cell-mediated and non-natural killer cell-mediated mechanisms in double-mutant tumors. We provide evidence for different immunomodulatory mechanisms based on treatment (A+Ax vs. sunitinib) and tumor molecular subtypes.

SIGNIFICANCE: Our findings provide novel insights into the different immunomodulatory mechanisms governing responses in patients treated with avelumab (PD-L1 inhibitor) + axitinib or sunitinib (both VEGF inhibitors), highlighting the contribution of tumor biology to the complexity of the roles and interactions of infiltrating immune cells in response to these treatment regimens. This article is featured in Selected Articles from This Issue, p. 384.


 

Cancer Discovery

Noninvasive Detection of Neuroendocrine Prostate Cancer through Targeted Cell-free DNA Methylation

Mizuno K, Ku SY, Rothmann E, Freeman D, Beltran H

Castration-resistant prostate cancer (CRPC) is a heterogeneous disease associated with phenotypic subtypes that drive therapy response and outcome differences. Histologic transformation to castration-resistant neuroendocrine prostate cancer (CRPC-NE) is associated with distinct epigenetic alterations, including changes in DNA methylation. The current diagnosis of CRPC-NE is challenging and relies on metastatic biopsy. We developed a targeted DNA methylation assay to detect CRPC-NE using plasma cell-free DNA (cfDNA). The assay quantifies tumor content and provides a phenotype evidence score that captures diverse CRPC phenotypes, leveraging regions to inform transcriptional state. We tested the design in independent clinical cohorts (n = 222 plasma samples) and qualified it achieving an AUC > 0.93 for detecting pathology-confirmed CRPC-NE (n = 136). Methylation-defined cfDNA tumor content was associated with clinical outcomes in two prospective phase II clinical trials geared towards aggressive variant CRPC and CRPC-NE. These data support the application of targeted DNA methylation for CRPC-NE detection and patient stratification.

SIGNIFICANCE: Neuroendocrine prostate cancer is an aggressive subtype of treatment-resistant prostate cancer. Early detection is important, but the diagnosis currently relies on metastatic biopsy. We describe the development and validation of a plasma cell-free DNA targeted methylation panel that can quantify tumor fraction and identify patients with neuroendocrine prostate cancer noninvasively. This article is featured in Selected Articles from This Issue, p. 384.


 

Journal of Clinical Oncology

Cannabis and Cannabinoids in Adults with Cancer: ASCO Guideline

Braun IM, Chai PR

PURPOSE: To guide clinicians, adults with cancer, caregivers, researchers, and oncology institutions on the medical use of cannabis and cannabinoids, including synthetic cannabinoids and herbal cannabis derivatives; single, purified cannabinoids; combinations of cannabis ingredients; and full-spectrum cannabis.

METHODS: A systematic literature review identified systematic reviews, randomized controlled trials (RCTs), and cohort studies on the efficacy and safety of cannabis and cannabinoids when used by adults with cancer. Outcomes of interest included antineoplastic effects, cancer treatment toxicity, symptoms, and quality of life. PubMed and the Cochrane Library were searched from database inception to January 27, 2023. ASCO convened an Expert Panel to review the evidence and formulate recommendations.

RESULTS: The evidence base consisted of 13 systematic reviews and five additional primary studies (four RCTs and one cohort study). The certainty of evidence for most outcomes was low or very low.

RECOMMENDATIONS: Cannabis and/or cannabinoid access and use by adults with cancer has outpaced the science supporting their clinical use. This guideline provides strategies for open, nonjudgmental communication between clinicians and adults with cancer about the use of cannabis and/or cannabinoids. Clinicians should recommend against using cannabis or cannabinoids as a cancer-directed treatment unless within the context of a clinical trial. Cannabis and/or cannabinoids may improve refractory, chemotherapy-induced nausea and vomiting when added to guideline-concordant antiemetic regimens. Whether cannabis and/or cannabinoids can improve other supportive care outcomes remains uncertain. This guideline also highlights the critical need for more cannabis and/or cannabinoid research. Additional information is available at www.asco.org/supportive-care-guidelines.


 

Journal of Clinical Oncology

CNS Efficacy of Osimertinib with or without Chemotherapy in Epidermal Growth Factor Receptor-Mutated Advanced Non-Small-Cell Lung Cancer

Jänne PA

PURPOSE: We report CNS efficacy of first-line osimertinib plus chemotherapy versus osimertinib monotherapy in patients with epidermal growth factor receptor (EGFR)-mutated advanced non-small-cell lung cancer (NSCLC) from the phase III FLAURA2 study according to baseline CNS metastasis status.

METHODS: Patients were randomly assigned to osimertinib plus platinum-pemetrexed (combination) or osimertinib monotherapy until disease progression or discontinuation. Brain scans were performed in all patients at baseline and progression and at scheduled assessments until progression for patients with baseline CNS metastases; scans were assessed by neuroradiologist CNS blinded independent central review (BICR).

RESULTS: On the basis of baseline CNS BICR, 118 of 279 (combination) and 104 of 278 (monotherapy) randomly assigned patients had ?one measurable and/or nonmeasurable CNS lesion and were included in the CNS full analysis set (cFAS); 40 of 118 and 38 of 104 had ?one measurable target CNS lesion and were included in the post hoc CNS evaluable-for-response set (cEFR). In the cFAS, the hazard ratio (HR) for CNS progression or death was 0.58 (95% CI, 0.33 to 1.01). In patients without baseline CNS metastases, the HR for CNS progression or death was 0.67 (95% CI, 0.43 to 1.04). In the cFAS, CNS objective response rates (ORRs; 95% CI) were 73% (combination; 64 to 81) versus 69% (monotherapy; 59 to 78); 59% versus 43% had CNS complete response (CR). In the cEFR, CNS ORRs (95% CI) were 88% (73 to 96) versus 87% (72 to 96); 48% versus 16% had CNS CR.

CONCLUSION: Osimertinib plus platinum-pemetrexed demonstrated improved CNS efficacy compared with osimertinib monotherapy, including delaying CNS progression, irrespective of baseline CNS metastasis status. These data support this combination as a new first-line treatment for patients with EGFR-mutated advanced NSCLC, including those with CNS metastases.


 

Journal of Clinical Oncology

Endocrine and Targeted Therapy for Hormone Receptor-Positive, Human Epidermal Growth Factor Receptor 2-Negative Metastatic Breast Cancer-Capivasertib-Fulvestrant: ASCO Rapid Recommendation Update

Burstein HJ

ASCO Rapid Recommendation Updates highlight revisions to select ASCO guideline recommendations as a response to the emergence of new and practice-changing data. The rapid updates are supported by an evidence review and follow the guideline development processes outlined in the ASCO Guideline Methodology Manual. The goal of these articles is to disseminate updated recommendations, in a timely manner, to better inform health practitioners and the public on the best available cancer care options. Guidelines and updates are not intended to substitute for independent professional judgment of the treating provider and do not account for individual variation among patients. See appendix for disclaimers and other important information (Appendix 1 and Appendix 2, online only).


 

Journal of Clinical Oncology

Phase II Trial of nab-Sirolimus in Patients with Advanced Malignant Perivascular Epithelioid Cell Tumors (AMPECT): Long-Term Efficacy and Safety Update

Wagner AJ, Hornick JL, Du H, Kwiatkowski DJ

Clinical trials frequently include multiple end points that mature at different times. The initial report, typically based on the primary end point, may be published when key planned co-primary or secondary analyses are not yet available. Clinical Trial Updates provide an opportunity to disseminate additional results from studies, published in JCO or elsewhere, for which the primary end point has already been reported.nab-Sirolimus is approved in the United States for the treatment of metastatic or locally advanced malignant perivascular epithelioid cell tumor (PEComa) on the basis of the primary analysis results of the phase II Advanced Malignant Perivascular Epithelioid Cell Tumors (AMPECT) trial (ClinicalTrials.gov identifier: NCT02494570). Results from the primary analysis were previously published; however, the median duration of response (mDOR) had not been reached at that time. Here, 3 years after the primary analysis, we report final efficacy and safety data (data cutoff: April 29, 2022). At study completion, the confirmed overall response rate (by independent radiologist review using RECIST v1.1) was 38.7% (95% CI, 21.8 to 57.8), with an additional converted confirmed complete response (n = 2). Median progression-free survival remained the same at 10.6 months (95% CI, 5.5 to 41.2). The mDOR was reached at 39.7 months (95% CI, 6.5 to not reached [NR]), and the median overall survival at completion was 53.1 months (95% CI, 22.2 to NR). The most common treatment-related adverse events (TRAEs) were stomatitis (82.4%) and fatigue and rash (each 61.8%). No new or unexpected adverse events occurred, and no grade ?4 TRAEs were reported. These results highlight the long-term clinical benefit of nab-sirolimus in patients with advanced malignant PEComa, with a DOR of >3 years.


 

Journal of the National Cancer Institute

Effects of a Change in Recall Period on Reporting Severe Symptoms: An Analysis of a Pragmatic Multisite Trial

Paudel R, Enzinger AC, Uno H, Cronin C, Hassett MJ

BACKGROUND: Optimal methods for deploying electronic patient-reported outcomes (ePROs) to manage symptoms in routine oncologic practice remain uncertain. The eSyM symptom management program asks chemotherapy and surgery patients to self-report 12 symptoms regularly. Feedback from nurses and patients led to changing the recall period from the past 7?days to the past 24?hours.

METHODS: Using questionnaires submitted during the 16-weeks surrounding the recall period change, we assessed the likelihood of reporting a severe, or a moderate-severe, symptom across all 12 symptoms and separately for the 5 most prevalent symptoms. Interrupted time series analyses modeled the effects of the change using generalized linear mixed-effects models. Surgery and chemotherapy cohorts were analyzed separately. Study-wide effects were estimated using a meta-analysis method.

RESULTS: In total, 1,692 patients from 6 institutions submitted 7,823 eSyM assessments during the 16-weeks surrounding the recall period change. Shortening the recall period was associated with lower odds of severe symptom reporting in the surgery cohort (OR 0.65; 95% CI 0.46 to 0.93; p?=?.02) and lower odds of moderate-severe symptom reporting in the chemotherapy cohort (OR 0.83, 95% CI 0.71 to 0.97; p?=?.02). Among the most prevalent symptoms, 24-hour recall was associated with lower rate of reporting post-operative constipation, but no differences in reporting rates for other symptoms.

CONCLUSION: A shorter recall period was associated with a reduction in the proportion of patients reporting moderate-severe symptoms. The optimal recall period may vary depending on whether ePROs are collected for active symptom management, as a clinical trial endpoint, or another purpose. (Clinicaltrails.gov (NCT03850912).


 

Journal of the National Cancer Institute

Low Physical Function Post-Cancer Diagnosis is Associated with Higher Mortality Risk in Postmenopausal Women

Gonzalo-Encabo P, Dieli-Conwright CM

BACKGROUND: Postmenopausal women with cancer experience an accelerated physical dysfunction beyond that expected through aging alone due to cancer and its treatments. The aim of this study is to determine whether declines in physical function after cancer diagnosis are associated with all-cause mortality and cancer-specific mortality.

METHODS: This prospective cohort study included 8,068 postmenopausal women enrolled in the Women's Health Initiative (WHI) who were diagnosed with cancer and had physical function assessed within 1-year of cancer diagnosis. Self-reported physical function was measured using the 10-item physical function subscale of the RAND 36-Item Health Survey. Cause of death was determined by medical record review with central adjudication and linkage to the National Death Index. Death was adjudicated through February 2022.

RESULTS: Over a median follow-up of 7.7?years from cancer diagnosis 3,316 (41.1%) women died. Our results showed that for every 10% decline in the physical function score after cancer diagnosis, all-cause mortality and cancer-specific mortality were significantly reduced by 12% (HR, 0.88; 95% CI, 0.87 to 0.89) and (HR, 0.88; 95%CI, 0.86 to 0.91), respectively. Further categorical analyses showed a significant dose-response relationship between post-diagnosis physical function categories and mortality outcomes (trend test P?

 

JAMA Oncology

Advancing Truth in Oncology by Complementing Clinical Trials with Evidence from Clinical Practice

Sharon E

Despite the increasing complexity of cancer clinical trials, the most successful trials often answer simple questions of efficacy for populations of patients with the most generalizable characteristics and adequate organ function. Unfortunately, as a result, specific populations of patients, such as older adults, who may be frail or have other comorbid conditions, can often be overlooked. In this issue of JAMA Oncology, the case series by Tsukita et al presented the results of an analysis from an impressive network of Japanese oncology sites, collating data that answer an important clinical question of relevance to patients with non–small cell lung cancer who are older than 75 years of age. These types of efforts are needed by both patients and clinicians and are often sorely lacking in oncology.


 

Lancet Oncology

Activity and Safety of Enobosarm, a Novel, Oral, Selective Androgen Receptor Modulator, in Androgen Receptor-Positive, Oestrogen Receptor-Positive, and HER2-Negative Advanced Breast Cancer (Study G200802): A Randomised, Open-Label, Multicentre, Multinational, Parallel Design, Phase 2 Trial

Overmoyer B

BACKGROUND: The androgen receptor is a tumour suppressor in oestrogen receptor-positive breast cancer. The activity and safety of enobosarm, an oral selective androgen receptor modulator, was evaluated in women with oestrogen receptor (ER)-positive, HER2-negative, and androgen receptor (AR)-positive disease.

METHODS: Women who were postmenopausal (aged ?18 years) with previously treated ER-positive, HER2-negative, locally advanced or metastatic breast cancer with an Eastern Cooperative Oncology Group performance status of 0-2 were enrolled in a randomised, open-label, multicentre, multinational, parallel design, phase 2 trial done at 35 cancer treatment centres in nine countries. Participants were stratified on the setting of immediately preceding endocrine therapy and the presence of bone-only metastasis and randomly assigned (1:1) to 9 mg or 18 mg oral enobosarm daily using an interactive web response system. The primary endpoint was clinical benefit rate at 24 weeks in those with centrally confirmed AR-positive disease (ie, the evaluable population). This trial is registered with ClinicalTrials.gov (NCT02463032).

FINDINGS: Between Sept 10, 2015, and Nov 28, 2017, 136 (79%) of 172 patients deemed eligible were randomly assigned to 9 mg (n=72) or 18 mg (n=64) oral enobosarm daily. Of these 136 patients, 102 (75%) patients formed the evaluable population (9 mg, n=50; 18 mg, n=52). The median age was 60·5 years (IQR 52·3-69·3) in the 9 mg group and 62·5 years (54·0-69·3) in the 18 mg group. The median follow-up was 7·5 months (IQR 2·9-14·1). At 24 weeks, 16 (32%, 95% CI 20-47) of 50 in the 9 mg group and 15 (29%, 17-43) of 52 in the 18 mg group had clinical benefit. Six (8%) of 75 patients who received 9 mg and ten (16%) of 61 patients who received 18 mg had grade 3 or grade 4 drug-related adverse events, most frequently increased hepatic transaminases (three [4%] of 75 in the 9 mg group and two [3%] of 61 in the 18 mg group), hypercalcaemia (two [3%] and two [3%]), and fatigue (one [1%] and two [3%]). Four deaths (one in the 9 mg group and three in the 18 mg group) were deemed unrelated to the study drug.

INTERPRETATION: Enobosarm has anti-tumour activity in patients with ER-positive, HER2-negative advanced breast cancer, showing that AR activation can result in clinical benefit, supporting further clinical investigation of selective AR activation strategies for the treatment of AR-positive, ER-positive, HER2-negative advanced breast cancer.

FUNDING: GTx.


 

Lancet Oncology

Tabelecleucel for Allogeneic Haematopoietic Stem-Cell or Solid Organ Transplant Recipients with Epstein-Barr Virus-Positive Post-Transplant Lymphoproliferative Disease After Failure of Rituximab or Rituximab and Chemotherapy (ALLELE): A Phase 3, Multicentre, Open-Label Trial

Nikiforow S, Prockop S

BACKGROUND: Survival in Epstein-Barr virus (EBV)-positive post-transplant lymphoproliferative disease following haematopoietic stem-cell transplant (HSCT) or solid organ transplant (SOT) is poor after failure of initial therapy, indicating an urgent need for therapies for this ultra-rare disease. With recent EU marketing authorisation, tabelecleucel is the first off-the-shelf, allogeneic, EBV-specific T-cell immunotherapy to receive approval for treatment of relapsed or refractory EBV-positive post-transplant lymphoproliferative disease. We aimed to determine the clinical benefit of tabelecleucel in patients with relapsed or refractory EBV-positive post-transplant lymphoproliferative disease following HSCT or SOT.

METHODS: In this global, multicentre, open-label, phase 3 trial, eligible patients (of any age) had biopsy-proven EBV-positive post-transplant lymphoproliferative disease, disease that was relapsed or refractory to rituximab after HSCT and rituximab with or without chemotherapy after SOT, and partially HLA-matched and appropriately HLA-restricted tabelecleucel available. Patients received tabelecleucel administered intravenously at 2?×?106 cells per kg on days 1, 8, and 15 in 35-day cycles and are assessed for up to 5 years for survival post-treatment initiation. The primary endpoint was objective response rate. All patients who received at least one dose of tabelecleucel were included in safety and efficacy analyses. This trial is registered with ClinicalTrials.gov, NCT03394365, and is ongoing.

FINDINGS: From June 27, 2018, to Nov 5, 2021, 63 patients were enrolled, of whom 43 (24 [56%] male and 19 [44%] female) were included, 14 had prior HSCT, 29 had SOT. Seven (50%, 95% CI 23-77) of 14 participants in the HSCT group and 15 (52%, 33-71) of 29 participants in the SOT group had an objective response, with a median follow-up of 14·1 months (IQR 5·7-23·9) and 6·0 months (1·8-18·4), respectively. The most common grade 3 or 4 treatment-emergent adverse events were disease progression (in four [29%] of 14 in HSCT and eight [28%] of 29 in SOT) and decreased neutrophil count (in four [29%] of 14 in HSCT and four [14%] of 29 in SOT). Treatment-emergent serious adverse events were reported in 23 (53%) of 43 patients and fatal treatment-emergent adverse events in five (12%); no fatal treatment-emergent adverse event was treatment-related. There were no reports of tumour flare reaction, cytokine release syndrome, immune effector cell-associated neurotoxicity syndrome, transmission of infectious diseases, marrow rejection, or infusion reactions. No events of graft-versus-host disease or SOT rejection were reported as related to tabelecleucel.

INTERPRETATION: Tabelecleucel provides clinical benefit in patients with relapsed or refractory EBV-positive post-transplant lymphoproliferative disease, for whom there are no other approved therapies, without evidence of safety concerns seen with other adoptive T-cell therapies. These data represent a potentially transformative and accessible treatment advance for patients with relapsed or refractory disease with few treatment options.

FUNDING: Atara Biotherapeutics.


 

Nature

Deciphering Cell States and Genealogies of Human Haematopoiesis

Weng C, Yu F, Poeschla M, Liggett LA, Wahlster L, Caulier A, Martin-Rufino JD, Hammond A, Ssozi D, Bueno R, Mallidi H, Kreso A, Escabi J, Hormoz S, van Galen P, Weissman JS, Sankaran VG

The human blood system is maintained through the differentiation and massive amplification of a limited number of long-lived haematopoietic stem cells (HSCs)1. Perturbations to this process underlie diverse diseases, but the clonal contributions to human haematopoiesis and how this changes with age remain incompletely understood. Although recent insights have emerged from barcoding studies in model systems2-5, simultaneous detection of cell states and phylogenies from natural barcodes in humans remains challenging. Here we introduce an improved, single-cell lineage-tracing system based on deep detection of naturally occurring mitochondrial DNA mutations with simultaneous readout of transcriptional states and chromatin accessibility. We use this system to define the clonal architecture of HSCs and map the physiological state and output of clones. We uncover functional heterogeneity in HSC clones, which is stable over months and manifests as both differences in total HSC output and biases towards the production of different mature cell types. We also find that the diversity of HSC clones decreases markedly with age, leading to an oligoclonal structure with multiple distinct clonal expansions. Our study thus provides a clonally resolved and cell-state-aware atlas of human haematopoiesis at single-cell resolution, showing an unappreciated functional diversity of human HSC clones and, more broadly, paving the way for refined studies of clonal dynamics across a range of tissues in human health and disease.


 

Abdominal Radiology

MRI, Clinical, and Radiomic Models for Differentiation of Uterine Leiomyosarcoma and Leiomyoma

Roller LA, Wan Q, Qin L, Burk KS, Guo Y, Shinagare AB


 

Annals of Surgical Oncology

Long-Term Patient-Reported Arm Symptoms in Breast Cancer Survivors

Laws A, Grossmith S, Hughes M, Lin NU, Mittendorf EA, Eliassen AH, King TA, Dominici LS


 

Arthritis Care and Research

Barriers, Facilitators, and Preferences for Mental Health Services Among Patients with Systemic Lupus Erythematosus: A Qualitative Study

Goldschen L, Peng CS, Mufson MJ, Feldman CH, Case SM, Costenbader KH, Amonoo HL


 

Arthritis and Rheumatology

Association of Somatic TET2 Mutations with Giant Cell Arteritis

Robinette ML, Weeks LD, Kramer RJ, Agrawal M, Gibson CJ, Yu Z, Sekar A, Mehta A, Niroula A, Brown JT, McDermott GC, Reshef ER, Lu JE, Liou VD, Chiou CA, Natarajan P, Freitag SK, Rao DA, Ebert BL


 

Blood Cancer Discovery

Acquired Multidrug Resistance in AML Is Caused by Low Apoptotic Priming in Relapsed Myeloblasts

Olesinski EA, Pioso MS, Yilma B, Bohl S, Ryan JA, Malani D, Luskin MR, Adamia S, Weinstock DM, Garcia JS, Letai A


 

Blood Cancer Discovery

Round Table Discussion on Optimal Clinical Trial Design in Precursor Multiple Myeloma

Ghobrial IM, Getz G, Nadeem O, O'Donnell E, Sklavenitis-Pistofidis R, Sperling AS, Munshi NC, Anderson KC


 

Blood Cancer Discovery

The Siren Song of Synergy

Bhola PD, Letai A


 

BMC Medical Informatics and Decision Making

A Qualitative Analysis of Algorithm-Based Decision Support Usability Testing for Symptom Management Across the Trajectory of Cancer Care: One Size Does Not Fit All

Halpenny B, Abrahm JL, Ligibel J, Enzinger A, Cooley ME


 

Breast Cancer Research Treatment

Survival Analysis of Patients with Brain Metastases at Initial Breast Cancer Diagnosis Over the Last Decade

Lin NU, Leone JP


 

Cancer

Alliance A151945: Accrual and Characteristics of Adolescent and Young Adult Patients in Alliance Trials from 2000 to 2017

Meyerhardt J, Ng K, Partridge AH, George S


 

Cancer

Prognostic Impact of Lymph Node Involvement and Loss of Heterozygosity of 1p or 16q in Stage III Favorable Histology Wilms Tumor: A Report from Children's Oncology Group Studies AREN03B2 and AREN0532

Mullen EA


 

Cancer

Secondary Analysis of Late Major Gastrointestinal and Genitourinary Toxicities in Unfavorable-Risk Prostate Cancer Patients Receiving Docetaxel: Insights from a Randomized Trial

Walburn T, Loffredo M, McMahon E, Orio PF, Nguyen PL, D'Amico AV, Sayan M


 

Cancer

Treatment of Children with Favorable Histology Wilms Tumor with Extrapulmonary Metastases: A Report from the COG Studies AREN0533 and AREN03B2 and NWTSG Study NWTS-5

Mullen EA


 

Cancer Research

A Benzarone Derivative Inhibits EYA to Suppress Tumor Growth in SHH Medulloblastoma

Hwang GH, Pazyra-Murphy MF, Seo HS, Dhe-Paganon S, Stopka SA, DiPiazza M, Sutter N, Gero TW, Volkert A, Ombelets L, Dittemore G, Rees MG, Ronan MM, Roth JA, Agar NYR, Scott DA, Segal RA


 

Cells

Building a Better Defense: Expanding and Improving Natural Killer Cells for Adoptive Cell Therapy

Maia A, Tarannum M, Piccinelli S, Romee R


 

Clinical Cancer Research

Phase 1/2 Study of Combined BCL-xL and MEK Inhibition with Navitoclax and Trametinib in KRAS or NRAS Mutant Advanced Solid Tumors

Corcoran RB, Do KT, Cleary JM, Parikh AR, Yeku OO, Xiong N, Weekes CD, Ahronian LG, Tian J, Norden BL, Michel AG, Van Seventer EE, Siravegna G, Camphausen K, Chi G, Fetter IJ, Brugge JS, Penson RT, Juric D, Flaherty KT, Sullivan RJ, Clark JW, Heist RS, Matulonis UA, Liu JF, Shapiro GI


 

Clinical Lymphoma, Myeloma, and Leukemia

SOHO State of the Art Updates and Next Questions | Approach to Older Adults with Philadelphia-Chromosome Negative Acute Lymphoblastic Leukemia

Shimony S, Luskin MR


 

Communications Medicine

Deep Learning Analysis of Epicardial Adipose Tissue to Predict Cardiovascular Risk in Heavy Smokers

Foldyna B, Hadzic I, Zeleznik R, Langenbach MC, Raghu VK, Mayrhofer T, Lu MT, Aerts HJWL


 

Current Opinion in Hematology

The Future of HOXA- Expressing Leukemias: Menin Inhibitor Response and Resistance

Wenge DV, Armstrong SA


 

Current Opinion in Nephrology and Hypertension

Onconephrology: Mitigation of Renal Injury in Chemotherapy Administration

Selamet U


 

EClinicalMedicine

The RELIVE Consortium for Relapsed or Refractory Pediatric Hepatoblastoma and Hepatocellular Carcinoma: A Scoping Review of the Problem and a Proposed Solution

O'Neill AF


 

European Journal of Cancer

Long-Term Patient-Reported Outcomes from MonarchE: Abemaciclib Plus Endocrine Therapy as Adjuvant Therapy for HR+, HER2-, Node-Positive, High-Risk, Early Breast Cancer

Tolaney SM


 

European Urology Open Science

Integrative Analysis of Germline Rare Variants in Clear and Non-clear Cell Renal Cell Carcinoma

Han SH, Camp SY, Chu H, Collins R, Gillani R, Park J, Bakouny Z, Ricker CA, Reardon B, Labaki C, Choueiri TK, AlDubayan SH, Van Allen EM


 

Frontier Oncology

Corrigendum: Phase 3 CLEAR Study in Patients with Advanced Renal Cell Carcinoma: Outcomes in Subgroups for the Lenvatinib-Plus-Pembrolizumab and Sunitinib Arms

Choueiri TK


 

Gut

Protein Biomarkers and Alternatively Methylated Cell-Free DNA Detect Early Stage Pancreatic Cancer

Wang QL, Zhang J, Supplee JG, Brais LK, Nowak J, Yuan C, Loftus M, Babic A, Boos N, Jajoo K, Lee L, Clancy TE, Rubinson DA, Ng K, Aguirre AJ, Jänne PA, Bardeesy N, Bullock AJ, Paweletz CP, Wolpin BM


 

Journal of the American College of Surgeons

Axillary Nodal Response to Neoadjuvant T-DM1 Combined with Pertuzumab in a Prospective Phase II Multi-Institution Clinical Trial

Jin Q, Waks AG, Spring LM, Wrabel E, Tayob N, King TA, Metzger-Filho O


 

Journal of the American College of Surgeons

Race and Ethnic Group Enrollment and Outcomes for Wilms Tumor: Analysis of the Current Era Children's Oncology Group Study, AREN03B2

Mullen EA


 

Journal of Cell Biology

PC4: A New Regulator of Cyclin D1 Transcript Levels

Sicinski P


 

Journal of the European Academy of Dermatology and Venereology

Patterns of Initial Distant Metastases in 151 Patients Undergoing Surveillance for Treated Merkel Cell Carcinoma

Kim EY, Liu M, Giobbie-Hurder A, Bahar F, Khaddour K, Silk AW, Thakuria M


 

Journal of Nuclear Medicine

The Current and Future Roles of Precision Oncology in Advanced Breast Cancer

Jacene H


 

Journal of Thoracic Oncology

MUC1-C Is a Common Driver of Acquired Osimertinib Resistance in NSCLC

Haratake N, Ozawa H, Morimoto Y, Yamashita N, Daimon T, Bhattacharya A, Wang K, Nakashoji A, Isozaki H, Hata AN, Kufe D


 

Journal of Women’s Health

Women's Information Needs and Educational Preferences Regarding Lung Cancer Screening

Warner ET, Revette A, Restrepo E, Lathan CS


 

JCO Oncology Practice

Cannabis and Cannabinoids in Adults with Cancer: ASCO Guideline Q&A

Braun IMlopis P, Agudo J


 

JCO Oncology Practice

Digital Health to Patient-Facing Artificial Intelligence: Ethical Implications and Threats to Dignity for Patients with Cancer

Kelkar AH, Hantel A, Koranteng E, Cutler CS, Hammer MJ, Abel GA


 

JCO Precision Oncology

Biomarker Inference and the Timing of Next-Generation Sequencing in a Multi-Institutional, Cross-Cancer Clinicogenomic Data Set

Kehl KL, Newcomb A


 

JMIR Human Factors

The Temperature Feature of ChatGPT: Modifying Creativity for Clinical Research

Davis J, Durieux BN, Lindvall Cgudo J


 

JMIR Research Protocol

Design and Rationale of Prolonged Nightly Fasting for Multiple Myeloma Prevention (PROFAST): Protocol for a Randomized Controlled Pilot Trial

Lee DJ, O'Donnell EK, Raje N, Panaroni C, Redd R, Ligibel J, Nadeem O, Ghobrial IM, Marinac CR


 

Leukemia

Inherent Genome Instability Underlies Trisomy 21-Associated Myeloid Malignancies

Chen CC, Perry JA, Khalid D, Pikman Y, Rowe RG


 

Leukemia

The UBE2J2/UBE2K-MARCH5 Ubiquitination Machinery Regulates Apoptosis in Response to Venetoclax in Acute Myeloid Leukemia

Lin S, Schneider C, Su AH, Alexe G, Root DE, Stegmaier K


 

Leukemia

Treatment Completion, Asparaginase Completion, and Oncologic Outcomes Among Children, Adolescents and Young Adults with Acute Lymphoblastic Leukemia Treated with DFCI Consortium Protocols

Flamand Y, Shimony S, Place AE, Silverman LB, Vrooman LM, Brunner AM, Sallan SE, Wadleigh M, Stone RM, DeAngelo DJ, Luskin MR


 

Medical Physics

MV-Based Relative Electron Density Estimation (iMREDe) for MR-LINAC Dose Calculation

Myronakis M, Hu YH, Jacobson MW, Williams CL, Berbeco RI


 

Molecular Therapy

An Empowered, Clinically Viable Hematopoietic Stem Cell Gene Therapy for the Treatment of Multisystemic Mucopolysaccharidosis Type II

Das S, Montepeloso A, Patel J, Cavalca E, Ferro F


 

NAR Cancer

The ORFIUS Complex Regulates ORC2 Localization at Replication Origins

Yang Z, Mogre S, He R, Berdan EL, Ho Sui SJ, Hill SJ


 

Nature Methods

scPerturb: Harmonized Single-Cell Perturbation Data

Green TD, Shen C, Min J, Yuan B, Marks DS, Luna A, Sander C


 

Nature Nanotechnology

Fine Tuning of CpG Spatial Distribution with DNA Origami for Improved Cancer Vaccination

Zeng YC, Young OJ, Wintersinger CM, Anastassacos FM, MacDonald JI, Isinelli G, Dellacherie MO, Sobral M, Bai H, Graveline AR, Vernet A, Sanchez M, Mulligan K, Ferrante TC, Keskin DB, Fell GG, Neuberg D, Wu CJ, Mooney DJ, Kwon IC, Ryu JH, Shih WM


 

Nature Reviews Cancer

Approaching Cancer During Pregnancy

Varella L, Partridge AH


 

Oncogene

HJURP is Recruited to Double-Strand Break Sites and Facilitates DNA Repair by Promoting Chromatin Reorganization

Serafim RB, Qi H, Parasuram R, Price BD


 

Open Forum Infectious Diseases

Neuroinvasive Bacillus cereus Infection in Immunocompromised Hosts: Epidemiologic Investigation of 5 Patients with Acute Myeloid Leukemia

Little JS, Coughlin C, Hsieh C, Lanza M, Huang WY, Kumar A, Dandawate T, Tucker R, Winkler ML, Pecora N, Kubiak DW, Pearson JC, Luskin MR, Sherman AC, Woolley AE, Bunnell C, Gross A, Platt D, Desai S, Fiumara K, Issa NC, Baden LR, Rhee C, Klompas M, Baker MA


 

Pediatric Blood and Cancer

A Nursing Perspective on Inpatient Sleep and Circadian Disruptions for Pediatric Stem Cell Transplant Patients

Zhou ES, Revette A, Waitt J, Lehmann LE, Diller LR, Emmons KM, Valenzuela AF, Redline S


 

Practical Radiation Oncology

Prospective Evaluation of the Clinical Benefits of a Novel Tattoo-less Workflow for Nonspine Bone Stereotactic Body Radiation Therapy: Integrating Surface-Guidance with Triggered Imaging Reduces Treatment Time and Eliminates the Need for Tattoos

Zhou AZ, Conway L, Bartlett S, Marques A, Physic M, Czerminska M, Spektor A, Killoran JH, Friesen S, Bredfeldt J, Huynh MA


 

Prostate

Adjuvant and Salvage Radiotherapy After Neoadjuvant Therapy and Radical Prostatectomy for High-Risk Localized Prostate Cancer

Ravi P, Kwak L, Xie W, Chipidza F, Yang X, Bubley G, Kaplan I, Kibel AS, Nguyen P, Taplin ME


 

Radiology: Artificial Intelligence

Noninvasive Molecular Subtyping of Pediatric Low-Grade Glioma with Self-Supervised Transfer Learning

Tak D, Ye Z, Zapaischykova A, Zha Y, Boyd A, Vajapeyam S, Chopra R, Hayat H, Prabhu S, Liu KX, Elhalawani H, Aerts HJWL, Bandopadhayay P, Ligon K, Haas-Kogan D, Poussaint T, Kann BH


 

Research Square

Lineage-Specific Canonical and Non-Canonical Activity of EZH2 in Advanced Prostate Cancer Subtypes

Venkadakrishnan VB, Presser AG, Booker MA, Traphagen NA, Weng K, Voss NC, Mahadevan NR, Mizuno K, Idahor O, Ku SY, Bakht MK, Borah AA, Herbert ZT, Tolstorukov MY, Barbie DA, Brown M, Beltran H


 

Stem Cells Translational Medicine

Genetic Manipulation Approaches to Enhance the Clinical Application of NK Cell-Based Immunotherapy

Maia A, Tarannum M, Romee R