A Novel ¹¹¹In-Labeled Anti-Prostate-Specific Membrane Antigen Nanobody for Targeted SPECT/CT Imaging of Prostate Cancer

J Nucl Med. 2015 Jul;56(7):1094-9. doi: 10.2967/jnumed.115.156729. Epub 2015 May 14.

Abstract

Prostate-specific membrane antigen (PSMA) is overexpressed in prostate cancer (PCa) and a promising target for molecular imaging and therapy. Nanobodies (single-domain antibodies, VHH) are the smallest antibody-based fragments possessing ideal molecular imaging properties, such as high target specificity and rapid background clearance. We developed a novel anti-PSMA Nanobody (JVZ-007) for targeted imaging and therapy of PCa. Here, we report on the application of the (111)In-radiolabeled Nanobody for SPECT/CT imaging of PCa.

Methods: A Nanobody library was generated by immunization of a llama with 4 human PCa cell lines. Anti-PSMA Nanobodies were captured by biopanning on PSMA-overexpressing cells. JVZ-007 was selected for evaluation as an imaging probe. JVZ-007 was initially produced with a c-myc-hexahistidine (his) tag allowing purification and detection. The c-myc-his tag was subsequently replaced by a single cysteine at the C terminus, allowing site-specific conjugation of chelates for radiolabeling. JVZ-007-c-myc-his was conjugated to 2-(4-isothiocyanatobenzyl)-diethylenetriaminepentaacetic acid (p-SCN-DTPA) via the lysines, whereas JVZ-007-cys was conjugated to maleimide-DTPA via the C-terminal cysteine. PSMA targeting was analyzed in vitro by cell-binding experiments using flow cytometry, autoradiography, and internalization assays with various PCa cell lines and patient-derived xenografts (PDXs). The targeting properties of radiolabeled Nanobodies were evaluated in vivo in biodistribution and SPECT/CT imaging experiments, using nude mice bearing PSMA-positive PC-310 and PSMA-negative PC-3 tumors.

Results: JVZ-007 was successfully conjugated to DTPA for radiolabeling with (111)In at room temperature. (111)In-JVZ007-c-myc-his and (111)In-JVZ007-cys internalized in LNCaP cells and bound to PSMA-expressing PDXs and, importantly, not to PSMA-negative PDXs and human kidneys. Good tumor targeting and fast blood clearance were observed for (111)In-JVZ-007-c-myc-his and (111)In-JVZ-007-cys. Renal uptake of (111)In-JVZ-007-c-myc-his was initially high but was efficiently reduced by coinjection of gelofusine and lysine. The replacement of the c-myc-his tag by the cysteine contributed to a further reduction of renal uptake without loss of targeting. PC-310 tumors were clearly visualized by SPECT/CT with both tracers, with low renal uptake (<4 percentage injected dose per gram) for (111)In-JVZ-007-cys already at 3 h after injection.

Conclusion: We developed an (111)In-radiolabeled anti-PSMA Nanobody, showing good tumor targeting, low uptake in nontarget tissues, and low renal retention, allowing excellent SPECT/CT imaging of PCa within a few hours after injection.

Keywords: 111In; Nanobody; PSMA; SPECT; prostate cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Surface / chemistry*
  • Autoradiography
  • Cell Line, Tumor
  • Cysteine / chemistry
  • Flow Cytometry
  • Glutamate Carboxypeptidase II / chemistry*
  • Histidine / chemistry
  • Humans
  • Kidney / diagnostic imaging
  • Male
  • Mice
  • Multimodal Imaging*
  • Nanomedicine
  • Neoplasm Transplantation
  • Oligopeptides / chemistry
  • Peptide Library
  • Prostatic Neoplasms / diagnosis
  • Prostatic Neoplasms / diagnostic imaging*
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins c-myc / chemistry
  • Single-Domain Antibodies / chemistry*
  • Tomography, Emission-Computed, Single-Photon*
  • Tomography, X-Ray Computed*

Substances

  • Antigens, Surface
  • His-His-His-His-His-His
  • Oligopeptides
  • Peptide Library
  • Proto-Oncogene Proteins c-myc
  • Single-Domain Antibodies
  • Histidine
  • FOLH1 protein, human
  • Glutamate Carboxypeptidase II
  • Cysteine