ArticleNature communications2023
Integrated molecular and multiparametric MRI mapping of high-grade glioma identifies regional biologic signatures.
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Article in Nature communications, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 40 papers.
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40citing papers in PubMed
12.1field-weighted citation impact, top 1% of its field
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Who cites it
40 citing papers in PubMed, 42 citations in OpenAlex.
- The Next Frontier in Quantitative Co-Clinical Imaging to Advance Functional Precision Oncology.Clinical cancer research : an official journal of the American Association for Cancer Research · 2026Article
- Spatial Omics in High-Grade Gliomas: Mapping Immune-Tumor Niches for Precision Therapy.Cancer medicine · 2026Review
- Multi-sampling allows intra-tumoral heterogeneity querying and vulnerability profiling in glioblastoma.Neuro-oncology · 2026Article
- The Invasive Margin of Glioblastoma as a Molecular Ecosystem: Spatial Heterogeneity, Tumor-Host Interactions, and Therapeutic Opportunities.International journal of molecular sciences · 2026Review
- Exploring the landscape of targetable alterations in patients with glioblastoma.Nature reviews. Clinical oncology · 2026Review
- Clinical fluorescent probes: mechanisms, advantages and inspirations.Chemical science · 2026Review
- Attract to kill: Exploring the potential of motility trapping as a novel treatment strategy for high-grade gliomas.Neuro-oncology · 2026Review
- PF-CMNet: Progressive Frequency-Aware Cross-Modal Network with Missing-Modality Distillation for 3D Brain Tumor Segmentation.Brain sciences · 2026Article
- mRNA-based MRI contrast agent for precise diagnosis of glioma and pseudoprogression.Cell biomaterials · 2026Article
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- Multimodal fusion of pathology and radiology foundation models for WHO 2021 glioma subtyping.NPJ precision oncology · 2026Article
- AI-powered radiogenomics: imaging-driven diagnosis and discovery of cancer's molecular and cellular landscape.Molecular genetics and genomics : MGG · 2026Review
- Review
- Spatial tumour characteristics as an indirect marker of metabolic dysregulation: evaluation for non-invasive IDH-genotyping of glioma using hybrid [18 F]FET-PET/MRI.European journal of nuclear medicine and molecular imaging · 2026Article
- FA-DeepMSM: a few-shot adapted interpretable multimodal survival model for improved prognostic prediction in glioblastoma.Scientific reports · 2026Article
- Progress in the study of molecular markers in the prognosis assessment and recurrence patterns of glioblastoma.Cancer biology & therapy · 2025Review
- Intratumoral preservation of the stem-like malignant cell proportion in glioblastoma, prognostic impact, and its radiomethylomic signatures.Neuro-oncology · 2025Article
- Glioblastoma resistance to EGFR antibody-drug conjugate is driven by transcriptional reprogramming and TEK-induced EGFR suppression.Journal of translational medicine · 2025Article
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Authors and funding
60 authors at 17 institutions in 3 countries.
Leland S Hu *Department of Radiology, Mayo Clinic Arizona, Phoenix, AZ, USA. hu.leland@mayo.edu.ORCID http://orcid.org/0000-0001-9282-7619
Fulvio D'Angelo *Department of Neurological Surgery, Sylvester Comprehensive Cancer Center, Miller School of Medicine, University of Miami, Miami, FL, USA. fxd317@med.miami.edu.ORCID http://orcid.org/0000-0002-4940-4693
Taylor M Weiskittel *Mayo Clinic Alix School of Medicine Minnesota, Rochester, MN, USA.
Francesca P Caruso *Department of Electrical Engineering and Information Technologies, University of Naples, "Federico II", I-80128, Naples, Italy.ORCID http://orcid.org/0000-0002-2206-1459
Shannon P Fortin Ensign *Department of Cancer Biology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Mylan R Blomquist *Department of Cancer Biology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Matthew J FlickDepartment of Radiology, Mayo Clinic Arizona, Phoenix, AZ, USA.ORCID http://orcid.org/0000-0001-7939-4871
Lujia WangH. Milton Stewart School of Industrial and Systems Engineering, Georgia Institute of Technology, Atlanta, GA, USA.
Christopher P SeredukDepartment of Cancer Biology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Kevin Meng-LinDepartment of Molecular Pharmacology and Experimental Therapeutics, Mayo Clinic, Rochester, MN, USA.
Gustavo De LeonDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Ashley NespodzanyDepartment of Neuroimaging Research, Barrow Neurological Institute, Dignity Health, Phoenix, AZ, USA.
Javier C UrcuyoDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.ORCID http://orcid.org/0000-0003-4017-7284
Ashlyn C GonzalesDepartment of Neuroimaging Research, Barrow Neurological Institute, Dignity Health, Phoenix, AZ, USA.
Lee CurtinDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.ORCID http://orcid.org/0000-0002-4083-3803
Erika M LewisSchool of Biological and Health Systems Engineering, Arizona State University, Tempe, AZ, USA.
Kyle W SingletonDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.ORCID http://orcid.org/0000-0002-9969-8474
Timothy DondlingerImaging Biometrics, LLC, Elm Grove, Milwaukee, USA.ORCID http://orcid.org/0000-0003-0851-1940
Aliya AnilDepartment of Neuroimaging Research, Barrow Neurological Institute, Dignity Health, Phoenix, AZ, USA.
Natenael B SemminehDepartment of Cancer Systems Imaging, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Teresa NovielloDepartment of Electrical Engineering and Information Technologies, University of Naples, "Federico II", I-80128, Naples, Italy.ORCID http://orcid.org/0000-0002-3411-6752
Reyna A PatelDepartment of Radiology, Mayo Clinic Arizona, Phoenix, AZ, USA.
Panwen WangQuantitative Health Sciences, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Junwen WangDivision of Applied Oral Sciences & Community Dental Care, The University of Hong Kong, Hong Kong SAR, China.ORCID http://orcid.org/0000-0002-4432-4707
Jennifer M EschbacherDepartment of Neuropathology, Barrow Neurological Institute, Dignity Health, Phoenix, AZ, USA.
Andrea Hawkins-DaarudDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Pamela R JacksonDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Itamar S GrunfeldDepartment of Psychology, Hunter College, The City University of New York, New York, NY, USA.ORCID http://orcid.org/0000-0001-7237-136X
Christian ElrodAvinger Incorporated, Redwood City, CA, USA.
Gina L MazzaQuantitative Health Sciences, Mayo Clinic Arizona, Scottsdale, AZ, USA.ORCID http://orcid.org/0000-0002-5305-6193
Sam C McGeeDepartment of Speech and Hearing Science, Arizona State University, Tempe, AZ, USA.
Lisa PaulsonDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Kamala Clark-SwansonDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Yvette Lassiter-MorrisDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Kris A SmithDepartment of Neurosurgery, Barrow Neurological Institute, Dignity Health, Phoenix, AZ, USA.
Peter NakajiDepartment of Neurosurgery, Banner University Medical Center, University of Arizona, Phoenix, AZ, USA.
Bernard R BendokDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Richard S ZimmermanDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Chandan KrishnaDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Devi P PatraDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Naresh P PatelDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Mark LyonsDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.ORCID http://orcid.org/0000-0001-8133-0295
Matthew NealDepartment of Neurological Surgery, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Kliment DonevDepartment of Pathology, Mayo Clinic Arizona, Phoenix, AZ, USA.
Maciej M MrugalaDepartment of Neurology, Mayo Clinic Arizona, Phoenix, AZ, USA.
Alyx B PorterDepartment of Neurology, Mayo Clinic Arizona, Phoenix, AZ, USA.
Scott C BeemanSchool of Biological and Health Systems Engineering, Arizona State University, Tempe, AZ, USA.
Todd R JensenJensen Informatics LLC, Shorewood, WI, USA.ORCID http://orcid.org/0000-0001-5908-5537
Kathleen M SchmaindaDepartments of Biophysics and Radiology, Medical College of Wisconsin, Milwaukee, WI, USA.
Yuxiang ZhouDepartment of Radiology, Mayo Clinic Arizona, Phoenix, AZ, USA.
Leslie C BaxterDepartment of Radiology, Mayo Clinic Arizona, Phoenix, AZ, USA.
Christopher L PlaisierSchool of Biological and Health Systems Engineering, Arizona State University, Tempe, AZ, USA.ORCID http://orcid.org/0000-0003-3273-5717
Jing LiH. Milton Stewart School of Industrial and Systems Engineering, Georgia Institute of Technology, Atlanta, GA, USA.
Hu LiDepartment of Molecular Pharmacology and Experimental Therapeutics, Mayo Clinic, Rochester, MN, USA.ORCID http://orcid.org/0000-0001-5957-5472
Anna LasorellaDepartment of Biochemistry and Molecular Biology, Sylvester Comprehensive Cancer Center, Miller School of Medicine, University of Miami, Miami, FL, USA.
C Chad QuarlesDepartment of Cancer Systems Imaging, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Kristin R SwansonDepartment of Cancer Biology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Michele CeccarelliDepartment of Public Health Sciences, Sylvester Comprehensive Cancer Center, Miller School of Medicine, University of Miami, Miami, FL, USA. mxc2982@miami.edu.
Antonio IavaroneDepartment of Neurological Surgery, Sylvester Comprehensive Cancer Center, Miller School of Medicine, University of Miami, Miami, FL, USA. axi435@med.miami.edu.
Nhan L TranDepartment of Cancer Biology, Mayo Clinic Arizona, Scottsdale, AZ, USA. Tran.Nhan@mayo.edu.ORCID http://orcid.org/0000-0003-0908-9964
WinnMed · USMayo Clinic in Arizona · USBarrow Neurological Institute · USMayo Clinic Hospital · USArizona State University · USMayo Clinic · USUniversity of Miami · USBiogem · ITGeorgia Institute of Technology · USThe University of Texas MD Anderson Cancer Center · USAvinger (United States) · USBanner - University Medical Center Tucson · USImaging Biometrics (United States) · USJensen Hughes (United States) · USMedical College of Wisconsin · USThe Graduate Center, CUNY · USUniversity of Hong Kong · HK
Funding
TRAINING GRANT IN CLINICAL PHARMACOLOGYT32GM008685 · NIGMS · MAYO CLINIC ROCHESTER · PI Liewei Wang · 1998 to 2026
$8.2MMedical Scientist Traning Program at Mayo ClinicT32GM065841 · NIGMS · MAYO CLINIC ROCHESTER · PI KAUFMANN, SCOTT H, SCHIMMENTI, LISA A · 2003 to 2022
$5.8MMSTP at Mayo Clinic RochesterT32GM145408 · NIGMS · MAYO CLINIC ROCHESTER · PI SCOTT H KAUFMANN, LISA A SCHIMMENTI · 2023 to 2026
$4.7MQuantifying Multiscale Competitive Landscapes of Clonal Diversity in GlioblastomaU01CA220378 · NCI · MAYO CLINIC ARIZONA · PI HU, LELAND, SWANSON, KRISTIN R · 2017 to 2021
$4.3MLangworthy Diversity Supplement: Image-based models of tumor-immune dynamics in glioblastomaU01CA250481 · NCI · MAYO CLINIC ARIZONA · PI CANOLL, PETER, HU, LELAND · 2021 to 2025
$3.8MEstablishing the clinical utility of a consensus DSC-MRI ProtocolR01CA264992 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI Jerrold L Boxerman, Leland Hu · 2022 to 2026
$2.4MMulti-site Validation and Application of a Consensus DSC MRI ProtocolR01CA221938 · NCI · ST. JOSEPH'S HOSPITAL AND MEDICAL CENTER · PI BOXERMAN, JERROLD L, HU, LELAND · 2018 to 2020
$738kMRI-based mapping of regional genomic diversity in GlioblastomaR21NS082609 · NINDS · MAYO CLINIC ARIZONA · PI HU, LELAND · 2013 to 2014
$525kNCI NIH HHS R01 CA221938NCI NIH HHS R01 CA264992NCI NIH HHS U01 CA220378NCI NIH HHS U01 CA250481NIGMS NIH HHS T32 GM008685NIGMS NIH HHS T32 GM065841NIGMS NIH HHS T32 GM145408NINDS NIH HHS R21 NS082609
Abstract
Sampling restrictions have hindered the comprehensive study of invasive non-enhancing (NE) high-grade glioma (HGG) cell populations driving tumor progression. Here, we present an integrated multi-omic analysis of spatially matched molecular and multi-parametric magnetic resonance imaging (MRI) profiling across 313 multi-regional tumor biopsies, including 111 from the NE, across 68 HGG patients. Whole exome and RNA sequencing uncover unique genomic alterations to unresectable invasive NE tumor, including subclonal events, which inform genomic models predictive of geographic evolution. Infiltrative NE tumor is alternatively enriched with tumor cells exhibiting neuronal or glycolytic/plurimetabolic cellular states, two principal transcriptomic pathway-based glioma subtypes, which respectively demonstrate abundant private mutations or enrichment in immune cell signatures. These NE phenotypes are non-invasively identified through normalized K2 imaging signatures, which discern cell size heterogeneity on dynamic susceptibility contrast (DSC)-MRI. NE tumor populations predicted to display increased cellular proliferation by mean diffusivity (MD) MRI metrics are uniquely associated with EGFR amplification and CDKN2A homozygous deletion. The biophysical mapping of infiltrative HGG potentially enables the clinical recognition of tumor subpopulations with aggressive molecular signatures driving tumor progression, thereby informing precision medicine targeting.
Indexed as
Biological ProductsBrain NeoplasmsGliomaMultiparametric Magnetic Resonance ImagingHomozygoteHumansMagnetic Resonance ImagingSequence DeletionBiological Products
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