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European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 5, May 2004
Abstract.
Two genetic reporter systems were developedfor multimodality reporter gene imaging of differentmolecular-genetic processes using fluorescence, biolumi-nescence (BLI), and nuclear imaging techniques. TheeGFP cDNA was fused at the N-terminus with HSV1-tk cDNA bearing a nuclear export signal from MAPKK(NES-HSV1-tk) or with truncation at the N-terminus of the first 45 amino acids (
45HSV1-tk) and with fireflyluciferase at the C-terminus. A single fusion protein withthree functional subunits is formed following transcrip-tion and translation from a single open reading frame.The NES-TGL (NES-TGL) or
45HSV1-tk/GFP/lucifer-ase (
45-TGL) triple-fusion gene cDNAs were clonedinto a MoMLV-based retrovirus, which was used fortransduction of U87 human glioma cells. The integrity,fluorescence, bioluminescence, and enzymatic activityof the TGL reporter proteins were assessed in vitro.The predicted molecular weight of the fusion proteins(~130kDa) was confirmed by western blot. The U87-NES-TGL and U87-
45-TGL cells had cytoplasmicgreen fluorescence. The in vitro BLI was 7- and 13-foldhigher in U87-NES-TGL and U87-
45-TGL cellscompared to nontransduced control cells. The Ki of 
14
C-FIAU was 0.49±0.02, 0.51±0.03, and 0.003±0.001ml/min/g in U87-NES-TGL, U87-
45-TGL, andwild-type U87 cells, respectively. Multimodality in vivoimaging studies were performed in
nu
 / 
nu
mice bearingmultiple s.c. xenografts established from U87-NES-TGL, U87-
45-TGL, and wild-type U87 cells. BLI wasperformed after administration of 
D
-luciferin (150mg/kgi.v.). Gamma camera or PET imaging was conducted at2h after i.v. administration of [
131
I]FIAU (7.4MBq/ animal) or [
124
I]FIAU (7.4MBq/animal), respectively.Whole-body fluorescence imaging was performed inparallel with the BLI and radiotracer imaging studies. Invivo BLI and gamma camera imaging showed specificlocalization of luminescence and radioactivity to theTGL transduced xenografts with background levels of activity in the wild-type xenografts. Tissue samplingyielded values of 0.47%±0.08%, 0.86%±0.06%, and0.03%±0.01%dose/g [
131
I]FIAU in U87-NES-TGL,U87-
45-TGL, and U87 xenografts, respectively. TheTGL triple-fusion reporter gene preserves the functionalactivity of its subunits and is very effective for multi-modality imaging. It provides for the seamless transitionfrom fluorescence microscopy and FACS to whole-body bioluminescence imaging, to nuclear (PET, SPET,gamma camera) imaging, and back to in situ fluores-cence image analysis.
Keywords:
Molecular imaging – Multimodality imaging –Herpes virus type one – Thymidine kinase – Green fluo-rescent protein – Luciferase – FIAU
Eur J Nucl Med Mol Imaging (2004) 31:740–751
DOI 10.1007/s00259-003-1441-5
Introduction
The past decade has witnessed a remarkable increasein our knowledge and understanding of the geneticsand molecular biology of human diseases. Significantprogress in the understanding of the molecular-geneticmechanisms of many diseases has been achieved with theadvent of the modern molecular-biological assays (e.g.,western and northern blots, PCR, RT-PCR, ELISA, etc.).
JuriGelovaniTjuvajev (
)MDAndersonCancerCenter, 1515HolcombeRoad, Box0057,Houston, TX77030,USAe-mail:jgelovani@mdanderson.orgTel.:+1-713-5633343
Molecular imaging 
A novel triple-modality reporter gene for whole-body fluorescent,bioluminescent, and nuclear noninvasive imaging
VladimirPonomarev
1
, MichaelDoubrovin
2
, InnaSerganova
2
, JelenaVider
1
, AleksanderShavrin
1
, TatianaBeresten
2
,AnnaIvanova
2
, LudmilaAgeyeva
1
, ViliaTourkova
1
, JuliusBalatoni
3
, WilliamBornmann
4
, RonaldBlasberg
2
,JuriGelovani Tjuvajev
1, 5
1
Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, USA
2
Department of Neurology, Memorial Sloan-Kettering Cancer Center, New York, USA
3
Radiochemistry/Cyclotron Core Facility, Memorial Sloan-Kettering Cancer Center, New York, USA
4
Organic Chemistry Synthesis Core Facility, Memorial Sloan-Kettering Cancer Center, New York, USA
5
MD Anderson Cancer Center, Houston, USAPublished online: 11 March 2004 ©Springer-Verlag 2004
 
The development of transgenic animal models of humandiseases, where the molecular basis of the disease can bestudied in a living organism, has provided new insightsinto disease development, progression, and treatment. Inparallel with the developments in genetics and molecularbiology, the imaging sciences have also made remarkableadvances in technology for visualizing tissue structureand function. These include new instruments for imagingsmall animals (e.g., microPET, microCT, high-fieldstrength magnets, novel optical and ultrasound imagingsystems). This convergence and interaction between the“molecular” and the “imaging” sciences has spawned thenew field of “molecular-genetic imaging” [1, 2, 3].This convergence of molecular biology and noninva-sive imaging was timely and addresses several experi-mental objectives. For example, ex vivo molecular assaysin animal models of disease and in transgenic animalsrequire invasive sampling procedures. Tissue samplingmay not always adequately represent the biochemical orpathological process under investigation owing to tissueheterogeneity, which is especially characteristic of cancer.Furthermore, temporal studies that employ molecular-biological assays require large numbers of animals thatare sacrificed at specific time points in order to achieve astatistically significant temporal profile. Noninvasive im-aging of molecular-genetic and cellular processes usingvarious reporter genes complements existing ex vivo mo-lecular-biological assays, and adds both spatial and tem-poral dimensions to the understanding of different molec-ular-biological processes. For example, several studiesdescribing successful monitoring of various signal trans-duction pathways have recently been reported, including:p53 signaling activity [4], NFAT-mediated T cell activa-tion [5], PSA activity [6], p53 and SV40 protein interac-tions [7], and TGF-
β
[8]. Noninvasive reporter gene im-aging has been successfully applied to monitoring varioustypes of gene therapy, including gene delivery and ex-pression mediated by retroviral [9, 10], adenoviral [11],herpes viral vectors [1], and oncolytic herpes viral [12]vectors. Reporter gene imaging has found a wide applica-tion in the development and monitoring of different adop-tive cell therapies [13, 14].In these studies, different types of imaging modalitieshave been utilized with corresponding modality-specificreporter genes, including: (a) for radiotracer imagingmodalities (gamma camera, SPET, PET)—herpes virus 1thymidine kinase (HSV1-tk) [11, 15, 16, 17] and its mu-tants [18], xanthine phosphoribosyl transferase (XPRT)[19], uracil phosphoribosyl transferase (UPRT) [20], hu-man truncated mitochondrial thymidine kinase type two(
hTK2) [21], dopamine receptor type 2 (D2R) [22],somatostatin receptor (SSTr2) [23], and sodium iodidesymporter (NIS) [24]; (b) for MRI or NMR spectrosco-py—cytosine deaminase (CD) [25, 26] and UPRT [20];(c) for whole-body fluorescence imaging—
 Aequoreavictoria
green fluorescent protein (GFP) and differentspectral shifted GFP variants [27, 28, 29, 30], humanizedversion (hrGFP) [31, 32], and red fluorescent proteins(Red1 and Red2) [33, 34]; and (d) for whole-body bio-luminescence imaging—
 Renilla
and firefly luciferaseenzymes in combination with their substrates coelenter-azine and
D
-luciferin, respectively [35, 36].Multimodality imaging approaches allow for differentimaging technologies to be combined during the course of the same study and harness the best features and utilitiesof each modality. The best clinical example of multi-modality imaging is combined PET/CT imaging, whichprovides functional (metabolic) information (PET compo-nent) overlaid/fused with the anatomical landmarks (CTcomponent) [37]. The advantages of hybrid reporter genesthat allow for multimodality imaging in vivo have beenrecognized as well. Initially, the advantages of multi-modality imaging using HSV1-tk (for nuclear imaging)and GFP (for optical fluorescent imaging) were demon-strated by our group [5, 38]. The HSV1-tk/GFP fusiongene allows for the optical microscopic and whole-bodyfluorescence imaging as well as PET imaging. Further im-provements were made by cytoplasmic retargeting of HSV1-tk/GFP fusion reporter protein using site-specificmutagenesis [18]. The fusion of 
 Renilla
luciferase (RLuc)and eGFP has also been reported [39]. GFP facilitates flu-orescence-based selection of transduced cell populationswhile the RLuc component allows for planar whole-bodybioluminescence imaging (BLI) of the transduced cell dis-tribution. In another study, the advantages of sr39HSV1-tk fused to RLuc, to yield the sr39HSV1-tk/ RLuc fusiongene, have also been demonstrated for dual-modality im-aging with microPET and bioluminescence imaging in liv-ing mice bearing transduced tumor xenografts [40].Following our initial HSV1-tk/GFP-based studies andthe reports from other groups using RLuc/GFP andsr39HSV1-tk/RLuc, we have developed an HSV1-tk/ GFP/firefly luciferase (TGL) triple reporter construct[41]. In this paper we describe the construction and vali-dation of the TGL triple-fusion reporter gene.
Materials and methods
 Expression vectors.
The schematic structures of the retroviral vec-tors used in this study are shown in Fig.1. PmlI-NheI fragmentwith blunted ends from the SGF-NES-HSV1-tk/GFP vector (de-scribed by us previously [18]) containing NES-HSV1-tk/GFP fu-sion gene was subcloned into pLNCX retroviral vector (Clontech,Palo Alto, CA) between blunt-ended
 Eco
RI-
 Bam
HI sites, replacingNeo resistance gene (vector pLNES-HSV1-tk/GFPCX). Then, fire-fly luciferase cDNA was amplified from the plasmid pEGFPLuc(Clontech, Palo Alto, CA) using primers 5
-AGTCAAGCTTATG-GAAGACGCCAAAAAC-3
and 5
-AGTCATCGATTACACGGC-GATCTTTC-3
, treated with
 Hin
dIII and
Cla
I restriction enzymesand subcloned downstream of the internal CMV promoter betweencorresponding sites of the pLNES-HSV1-tk/GFPCX vector, result-ing in pLNES-HSV1-tk/GFP-cmvFLuc vector. The cDNA of thefusion gene consisting of 
 Aequorea victoria
eGFP and firefly luci-ferase (eGFP/FLuc) was obtained from the plasmid pEGFPLuc(Clontech, Palo Alto, CA). The pEGFPLuc plasmid was treated741European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 5, May 2004
 
742European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 5, May 2004with
 Nco
I and
 Xba
I restriction enzymes (NEB, NH) and the
 Xba
Isite was blunt ended. Then, the eGFP/FLuc cDNA was subclonedinto the retroviral vector SFG-Ntp [42] (kindly provided by Dr.Sadelain, MSKCC, NY), replacing Ntp cDNA between
 Nco
I andblunt-ended
 Bam
HI restriction sites. The resultant vector wasnamed SFG-GL. Then, the SFG-NES-HSV1-tk/GFP vector wastreated with
 Nco
I restriction enzyme and the fragment containingNES-HSV1-tk lacking the stop codon was subcloned into the
 Nco
Isite of the SFG-GL vector upstream and in frame with theeGFP/FLuc gene, resulting in SFG-NES-HSV1-tk/eGFP/FLuc(SFG-NES-TGL) vector. In a similar way, the truncated form of theHSV1-tk,
45HSV1-tk, lacking the first 45 amino acids describedby us previously [18], was subcloned into the
 Nco
I site of the SFG-GL vector upstream and in frame with the eGFP/FLuc gene, result-ing in SFG-
45-HSV1-tk/eGFP/FLuc (SFG-45TGL) vector.For the production of the retroviral vectors for transduction of tumor cells, 10
µ
g of DNA of each vector-encoding plasmid wastransfected into the GPG29 packaging cell line using the calciumphosphate method as previously described [42]. The VSV-G-pseu-dotyped retroviral particles were used as cell-free viral stocks fortransduction.
Transduction of tumor cells.
The U87 human glioma cell line wasobtained from ATCC (Rockville, MD). U87 cells were grown asmonolayers in MEM supplemented with 10% FCS at 37°C in ahumidified atmosphere with 5% CO
2
. The in vitro transduction of U87 cells with the retroviral vectors was accomplished by expos-ing the cell monolayers to a filtered (0.45
µ
m) culture mediumobtained from the vector producer cells for 8h in the presence of polybrene (8
µ
g/ml, Sigma, MO).
Flow cytometry and fluorescent microscopy.
Retrovirally trans-duced U87 cells were grown as bulk cultures for 48h and sub-sequently sorted for positive GFP expression using FACS(FACSVantage, Becton Dickinson, CA); the 488-nm excitationbeam and 510-nm emission filters were used. Subcellular localiza-tion of the NES-HSV1-tk/GFP, eGFP/FLuc, NES-TGL and
45-TGL proteins in transduced tumor cells was visualized by fluores-cence microscopy (Nikon, Osaka, Japan) using similar excitationand emission parameters.
 Assessment of the integrity of different reporter proteins.
The in-tegrity of the different reporter proteins was assessed by westernblot analysis. Total protein was extracted from transduced tumorcells using the Mammalian Protein Extraction Reagent (Pierce,Rockford, IL) and a complete protease inhibitor cocktail (RocheDiagnostics GmbH, Mannheim, Germany). The lysates were cen-trifuged at 4°C for 10min at 14,000rpm/min, and protein concen-tration in the supernatants was measured with a BCA Protein As-say Kit (Pierce, Rockford, IL) using Tecan Safire (Tecan,Salzburg, Austria) at 562nm. The proteins were separated by elec-trophoresis in NuPAGE 4%–12% Bis-Tris Gel (Invitrogen, Carls-bad, CA) and transferred to the Invitrolon PVDF membrane (Invi-trogen, Carlsbad, CA) using a semi-dry XCell II Blot Module (In-vitrogen, Carlsbad, CA). Immunoblotted proteins were analyzedusing a monoclonal anti-GFP antibody (cat # 8362; Clontech, PaloAlto, CA) at a 1:1,000 dilution, anti-HSV1-TK monoclonal anti-body (kindly provided by Dr. Summers, Yale University) at 1:200dilution, or anti-luciferase monoclonal antibody (FL-Y, SerotecLtd., Kidlington, Oxford, UK). Secondary anti-mouse HRP conju-gated antibody (cat # 65-6420, Zymed, San-Francisco, CA) wasused at 1:4,000 dilution. Restore Western Blot Stripping Bufferwas used to strip the membrane. Detection was performed usingan ECL Western blot detection kit (cat # RPN 2106, AmershamPharmacia Biotech, Piscataway, NJ).
 In vitro bioluminescence assay.
Cells were seeded at a concentra-tion 0.5
×
10
6
cells/well in six-well tissue culture plates.
D
-Lucife-rin (Xenogen, Stanford, CA) at a concentration of 0.5m
 M 
wasadded immediately prior to assay. Bioluminescence was measuredusing Luminoscan Ascent and analyzed by Ascent Software (Lab-Systems, Finland).
 In vivo fluorescent imaging.
Whole-body imaging of GFP fluores-cence in mice was performed using a home-built digital opticalfluorescence imaging (OFI) system consisting of: a 150-W halo-gen light source LT-9500 (Lightools Research, Encinitas, CA)equipped with an excitation filter (480–490nm), two fiberopticguides with linear illuminators (each positioned at 45°), and anemission filter plate (505nm cut-off filter; 6
×
12cm). The GFPfluorescence was readily observed with the naked eye and the im-
Fig. 1A–E.
Schematic struc-tures of retroviral vectors formammalian expression of different reporter genes:
A
SFG-NES-HSV1-tk/GFP;
B
pLNES-HSV1-tk/GFP withfirefly luciferase expressedfrom internal CMV promoter;
C
SFG-GFP/firefly luciferase;
D
SFG-NES-TGL;
E
SFG-
45-TGL with truncation of N-terminal sequence encodingthe first 45 amino acids of thenative protein
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