Synthesis of radiometal-labeled and fluorescent cell-permeating peptide-PNA conjugates for targeting the bcl-2 proto-oncogene

Bioconjug Chem. 2003 Nov-Dec;14(6):1083-95. doi: 10.1021/bc034084n.

Abstract

The B-cell lymphoma/leukemia-2 (bcl-2) proto-oncogene has been associated with the transformation of benign lesions to malignancy, disease progression, poor prognosis, reduced survival, and development of resistance to radiation and chemotherapy in many types of cancer. The objective of this work was to synthesize an antisense peptide nucleic acid (PNA) complementary to the first six codons of the bcl-2 open reading frame, conjugated to a membrane-permeating peptide for intracellular delivery, and modified with a bifunctional chelating agent for targeting imaging and therapeutic radiometals to tumors overexpressing bcl-2. Four peptide-PNA constructs were synthesized by a combination of manual and automated stepwise elongation techniques, including bcl-2 antisense conjugates and nonsense conjugates with no complementarity to any known mammalian gene or DNA sequence. The PNA sequences were synthesized manually by solid-phase 9-fluorenylmethoxycarbonyl (Fmoc) techniques. Then a fully protected lysine monomer, modified with 1,4,7,10-tetraazacyclododecane-N,N',N'',N'"-tetraacetic acid (DOTA) for radiometal chelation, was coupled manually to each PNA sequence. Synthesis of the DOTA-PNA conjugates was followed by automated elongation with a peptide sequence (PTD-4-glycine, PTD-4-G), known to mediate cellular internalization of impermeable effector molecules, or its retro-inverso analogue (ri-PTD-4-G). Preparation of the four conjugates required an innovative synthetic strategy, using mild acid conditions to generate hydrophobic, partially deprotected intermediates. These intermediates were purified by semipreparative reversed-phase HPLC and completely deprotected to yield pure peptide-PNA conjugates in 6% to 9% overall yield. Using modifications of this synthetic strategy, the ri-PTD-4-G conjugate of bcl-2 antisense PNA was prepared using a lysine derivative of tetramethylrhodamine (TMR) for fluorescence microscopy. Plasma stability studies showed that (111)In-DOTA-labeled ri-PTD-4-G-anti-bcl-2 PNA was stable for 168 h at 37 degrees C, unlike the conjugate containing the parent peptide sequence. Scanning confocal fluorescence microscopy of TMR-labeled ri-PTD-4-G-anti-bcl-2 PNA in Raji lymphoma cells demonstrated that the retro-inverso peptide was active in membrane permeation and mediated cellular internalization of the antisense PNA into the cytoplasm, where high concentrations of bcl-2 mRNA are expected to be present.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Antineoplastic Agents / chemical synthesis*
  • Antineoplastic Agents / pharmacology
  • Cell Line, Tumor
  • Chromatography, High Pressure Liquid
  • Drug Delivery Systems
  • Fluorescent Dyes
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genes, bcl-2* / drug effects
  • Heterocyclic Compounds, 1-Ring / chemistry
  • Humans
  • Indium Radioisotopes
  • Lymphoma, B-Cell / genetics*
  • Microscopy, Confocal
  • Molecular Structure
  • Peptide Nucleic Acids / chemical synthesis*
  • Peptide Nucleic Acids / pharmacology
  • Peptides / chemical synthesis*
  • Peptides / pharmacology
  • Proto-Oncogene Mas
  • RNA, Messenger / drug effects
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Rhodamines / chemistry
  • Spectrometry, Fluorescence

Substances

  • Antineoplastic Agents
  • Fluorescent Dyes
  • Heterocyclic Compounds, 1-Ring
  • Indium Radioisotopes
  • MAS1 protein, human
  • Peptide Nucleic Acids
  • Peptides
  • Proto-Oncogene Mas
  • RNA, Messenger
  • Rhodamines
  • 1,4,7,10-tetraazacyclododecane- 1,4,7,10-tetraacetic acid