Generation of destabilized herpes simplex virus type 1 thymidine kinase as transcription reporter for PET reporter systems in molecular genetic imaging

J Nucl Med. 2008 Jan;49(1):142-50. doi: 10.2967/jnumed.106.038943. Epub 2007 Dec 12.

Abstract

Herpes simplex virus type 1 thymidine kinase (HSV1-TK) is a widely used reporter for in vivo noninvasive monitoring of therapeutic gene expression, immune cell trafficking, and protein-protein interactions in various animal systems. However, the stability of HSV1-TK limits its application in studies that require rapid turnover of the reporter. The purpose of this study was to create a destabilized HSV1-TK as a transcription reporter that allows for dynamic studies of short-time-scale gene expression events.

Methods: A destabilized HSV1-TK was created by targeting inactivating mutations in the nuclear localization signal of HSV1-TK and fusing the degradation domain of mouse ornithine decarboxylase to the C-terminal end. The protein or enzyme stability was determined by Western blot analysis and HSV1-TK enzyme activity assay, respectively. The proteasome inhibition assay was used to test whether the rapid turnover of the destabilized HSV1-TK was processed in a 26S proteasome-dependent manner. The suitability of destabilized HSV1-TK as a transcription reporter was tested by linking it to a tetracycline-turnoff-expressing system. The dynamic transcriptional events mediating a series of doxycycline inductions were monitored by destabilized HSV1-TK or by native HSV1-TK and were determined by an in vitro HSV1-TK enzyme activity assay and in vivo small-animal PET imaging.

Results: The destabilized HSV1-TK, unlike wild-type HSV1-TK, was unstable in the presence of cycloheximide and had a short half-life of protein and enzyme activity. The rapid turnover of the destabilized HSV1-TK was processed in a 26S proteasome-dependent manner. Furthermore, the destabilized HSV1-TK had low cytotoxicity when it was highly expressed in living cells. The results of dynamic gene expression studies in vitro and in vivo showed that the destabilized HSV1-TK is an optimal reporter for monitoring short-time-scale dynamic transcriptional events mediating a series of doxycycline inductions, whereas the wild-type HSV1-TK is not optimal to achieve this purpose.

Conclusion: The use of destabilized HSV1-TK as a transcription reporter together with a molecular probe, which has a short physical and biologic half-life, allows more direct monitoring of transcription induction and easier monitoring of its coincidence with other biochemical changes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cycloheximide / pharmacology
  • Doxycycline / pharmacology
  • Enzyme Stability
  • Female
  • Genes, Reporter*
  • Herpesvirus 1, Human / enzymology*
  • Humans
  • Mice
  • Mutation
  • Nuclear Localization Signals / genetics
  • Nuclear Localization Signals / metabolism
  • Ornithine Decarboxylase / genetics
  • Ornithine Decarboxylase / metabolism
  • Positron-Emission Tomography
  • Proteasome Endopeptidase Complex / metabolism
  • Thymidine Kinase / genetics*
  • Thymidine Kinase / metabolism
  • Transcription, Genetic*
  • Xenograft Model Antitumor Assays

Substances

  • Nuclear Localization Signals
  • Cycloheximide
  • Thymidine Kinase
  • Proteasome Endopeptidase Complex
  • ATP dependent 26S protease
  • Ornithine Decarboxylase
  • Doxycycline