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Targeting MMP-14 for dual PET and fluorescence imaging of glioma in preclinical models

  • Original Article
  • Published:
European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

There is a clinical need for agents that target glioma cells for non-invasive and intraoperative imaging to guide therapeutic intervention and improve the prognosis of glioma. Matrix metalloproteinase (MMP)-14 is overexpressed in glioma with negligible expression in normal brain, presenting MMP-14 as an attractive biomarker for imaging glioma. In this study, we designed a peptide probe containing a near-infrared fluorescence (NIRF) dye/quencher pair, a positron emission tomography (PET) radionuclide, and a moiety with high affinity to MMP-14. This novel substrate-binding peptide allows dual modality imaging of glioma only after cleavage by MMP-14 to activate the quenched NIRF signal, enhancing probe specificity and imaging contrast.

Methods

MMP-14 expression and activity in human glioma tissues and cells were measured in vitro by immunofluorescence and gel zymography. Cleavage of the novel substrate and substrate-binding peptides by glioma cells in vitro and glioma xenograft tumors in vivo was determined by NIRF imaging. Biodistribution of the radiolabeled MMP-14-binding peptide or substrate-binding peptide was determined in mice bearing orthotopic patient-derived xenograft (PDX) glioma tumors by PET imaging.

Results

Glioma cells with MMP-14 activity showed activation and retention of NIRF signal from the cleaved peptides. Resected mouse brains with PDX glioma tumors showed tumor-to-background NIRF ratios of 7.6–11.1 at 4 h after i.v. injection of the peptides. PET/CT images showed localization of activity in orthotopic PDX tumors after i.v. injection of 68Ga-binding peptide or 64Cu-substrate-binding peptide; uptake of the radiolabeled peptides in tumors was significantly reduced (p < 0.05) by blocking with the non-labeled-binding peptide. PET and NIRF signals correlated linearly in the orthotopic PDX tumors. Immunohistochemistry showed co-localization of MMP-14 expression and NIRF signal in the resected tumors.

Conclusions

The novel MMP-14 substrate-binding peptide enabled PET/NIRF imaging of glioma models in mice, warranting future image-guided resection studies with the probe in preclinical glioma models.

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Abbreviations

5-ALA :

5-aminolevulinic acid

ANOVA :

analysis of variance

BBB:

blood-brain barrier

BSA:

bovine serum albumin

CT :

computed tomography

FDA :

Food and Drug Administration

FFPE :

formalin-fixed paraffin-embedded

GBM :

glioblastoma multiforme

%ID/g :

percent injected dose per g

i.v. :

intravenous

mAb :

monoclonal antibody

MMP :

matrix metalloproteinase

NIR :

near-infrared

NIRF :

near-infrared fluorescence

NOTA :

1,4,7-triazacyclononane-1,4,7-triacetic acid

PDX :

patient-derived xenograft

PET :

positron emission tomography

p.i. :

postinjection

PpIX :

protoporphyrin IX

RIPA :

radioimmunoprecipitation assay

s.c. :

subcutaneous

SUVR :

standardized uptake value ratio

TBR :

tumor-to-background ratio

UAB :

University of Alabama at Birmingham

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Acknowledgments

Yolanda Hartman, Catherine Langford, Savannah Ferch, Kurt Zinn, Andrew Prince, Marilyn Shackelford, Sally Jordan, Lauren Radford, Charlotte Jeffers, Jennifer Burkemper, Tolulope Aweda, Adriana Massicano, Kiranya Tipirneni, Jonathan McConathy, Suzanne Lapi, Jinda Fan, Jennifer Coleman, Norio Yasui, Dattatray Devalankar, Sharon Samuel, Sheila Bright, Erika McMillian, Himani Modi, Hailey Houson and Morgan Richardson are gratefully acknowledged for their contributions. LI-COR Biosciences is gratefully acknowledged for supplying IRDye800CW-maleimide and QC-1-NHS ester to prepare the peptide probes.

Funding

Funding was provided by the NIH/NINDS T32 UAB Training Program in Brain Tumor Biology (T32 NS048039), the UAB Brain Tumor Core Facility (USPHS NCI P20CA151129), the National Center for Advancing Translational Research of the National Institutes of Health (UL1TR001417), the Department of Defense Congressionally Directed Medical Research Program (CA170769), and the Comprehensive Cancer Center at UAB (NIH P30CA013148).

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Author notes

  1. Benjamin B. Kasten and Ke Jiang contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL, 35294, USA

    Benjamin B. Kasten, G. Yancey Gillespie & James M. Markert

  2. Departments of Radiology and Chemistry, Molecular Imaging Program at Stanford, Stanford University School of Medicine, Stanford, CA, 94305, USA

    Ke Jiang, Tingting Dai & Jianghong Rao

  3. Department of Otolaryngology, University of Alabama at Birmingham, Birmingham, AL, 35294, USA

    Denzel Cole & Jason M. Warram

  4. School of Medicine, University of Alabama at Birmingham, Birmingham, AL, 35294, USA

    Aditi Jani & Neha Udayakumar

  5. Department of Otolaryngology – Head and Neck Surgery, Stanford University, Stanford, CA, 94305, USA

    Guolan Lu & Eben L. Rosenthal

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  1. Benjamin B. Kasten
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Corresponding authors

Correspondence to Jianghong Rao or Jason M. Warram.

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The authors declare that they have no conflicts of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. Animal studies were approved by the University of Alabama at Birmingham Institutional Animal Care and Use Committee (20366) and performed in compliance with guidelines from the Public Health Service Policy and Animal Welfare Act of the United States. This article does not contain any studies with human participants performed by any of the authors.

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Kasten, B.B., Jiang, K., Cole, D. et al. Targeting MMP-14 for dual PET and fluorescence imaging of glioma in preclinical models. Eur J Nucl Med Mol Imaging 47, 1412–1426 (2020). https://doi.org/10.1007/s00259-019-04607-x

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