European Radiology

, Volume 17, Issue 2, pp 305–319 | Cite as

Gene expression and gene therapy imaging

  • Claire Rome
  • Franck Couillaud
  • Chrit T. W. Moonen
Molecular Imaging

Abstract

The fast growing field of molecular imaging has achieved major advances in imaging gene expression, an important element of gene therapy. Gene expression imaging is based on specific probes or contrast agents that allow either direct or indirect spatio-temporal evaluation of gene expression. Direct evaluation is possible with, for example, contrast agents that bind directly to a specific target (e.g., receptor). Indirect evaluation may be achieved by using specific substrate probes for a target enzyme. The use of marker genes, also called reporter genes, is an essential element of MI approaches for gene expression in gene therapy. The marker gene may not have a therapeutic role itself, but by coupling the marker gene to a therapeutic gene, expression of the marker gene reports on the expression of the therapeutic gene. Nuclear medicine and optical approaches are highly sensitive (detection of probes in the picomolar range), whereas MRI and ultrasound imaging are less sensitive and require amplification techniques and/or accumulation of contrast agents in enlarged contrast particles. Recently developed MI techniques are particularly relevant for gene therapy. Amongst these are the possibility to track gene therapy vectors such as stem cells, and the techniques that allow spatiotemporal control of gene expression by non-invasive heating (with MRI guided focused ultrasound) and the use of temperature sensitive promoters.

Keywords

Molecular imaging Gene expression Gene therapy 

Notes

Acknowledgement

European Commission, Network of Excellence “Diagnostic Molecular Imaging”; Ligue National Contre le Cancer, Conseil Régional d’Aquitaine.

References

  1. 1.
    Cavazzana-Calvo M, Hacein-Bey S, de Saint Basile G, Gross F, Yvon E, Nusbaum P, Selz F, Hue C, Certain S, Casanova JL, Bousso P, Deist FL, Fischer A (2000) Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288:669–672PubMedCrossRefGoogle Scholar
  2. 2.
    Wunderbaldinger P, Bogdanov A, Weissleder R (2000) New approaches for imaging in gene therapy. Eur J Radiol 34:156–165PubMedCrossRefGoogle Scholar
  3. 3.
    Bogdanov AA Jr., Simonova M, Weissleder R (2000) Engineering membrane proteins for nuclear medicine: applications for gene therapy and cell tracking. Q J Nucl Med 44:224–235PubMedGoogle Scholar
  4. 4.
    Reader AJ, Zweit J (2001) Developments in whole-body molecular imaging of live subjects. Trends Pharmacol Sci 22:604–607PubMedCrossRefGoogle Scholar
  5. 5.
    Jacobs AH, Dittmar C, Winkeler A, Garlip G, Heiss WD (2002) Molecular imaging of gliomas. Mol Imaging 1:309–335PubMedCrossRefGoogle Scholar
  6. 6.
    Shah K, Jacobs A, Breakefield XO, Weissleder R (2004) Molecular imaging of gene therapy for cancer. Gene Ther 11:1175–1187PubMedCrossRefGoogle Scholar
  7. 7.
    van Roessel P, Brand AH (2002) Imaging into the future: visualizing gene expression and protein interactions with fluorescent proteins. Nat Cell Biol 4:E15–E20PubMedCrossRefGoogle Scholar
  8. 8.
    Weissleder R, Ntziachristos V (2003) Shedding light onto live molecular targets. Nat Med 9:123–128PubMedCrossRefGoogle Scholar
  9. 9.
    Contag CH, Spilman SD, Contag PR, Oshiro M, Eames B, Dennery P, Stevenson DK, Benaron DA (1997) Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem Photobiol 66:523–531PubMedGoogle Scholar
  10. 10.
    Turnbull DH, Ramsay JA, Shivji GS, Bloomfield TS, From L, Sauder DN, Foster FS (1996) Ultrasound backscatter microscope analysis of mouse melanoma progression. Ultrasound Med Biol 22:845–853PubMedCrossRefGoogle Scholar
  11. 11.
    Turnbull DH, Bloomfield TS, Baldwin HS, Foster FS, Joyner AL (1995) Ultrasound backscatter microscope analysis of early mouse embryonic brain development. Proc Natl Acad Sci U S A 92:2239–2243PubMedCrossRefGoogle Scholar
  12. 12.
    Hildebrandt IJ, Gambhir SS (2004) Molecular imaging applications for immunology. Clin Immunol 111:210–224PubMedCrossRefGoogle Scholar
  13. 13.
    Weissleder R (2002) Scaling down imaging: molecular mapping of cancer in mice. Nat Rev Cancer 2:11–18PubMedCrossRefGoogle Scholar
  14. 14.
    Liang HD, Blomley MJ (2003) The role of ultrasound in molecular imaging. Br J Radiol 76(Spec No 2):S140–S150PubMedCrossRefGoogle Scholar
  15. 15.
    Jain KK (2004) Role of pharmacoproteomics in the development of personalized medicine. Pharmacogenomics 5:331–336PubMedCrossRefGoogle Scholar
  16. 16.
    Artemov D, Mori N, Ravi R, Bhujwalla ZM (2003) Magnetic resonance molecular imaging of the HER-2/neu receptor. Cancer Res 63:2723–2727PubMedGoogle Scholar
  17. 17.
    Noble ME, Endicott JA, Johnson LN (2004) Protein kinase inhibitors: insights into drug design from structure. Science 303:1800–1805PubMedCrossRefGoogle Scholar
  18. 18.
    Waldherr C, Pless M, Maecke HR, Schumacher T, Crazzolara A, Nitzsche EU, Haldemann A, Mueller-Brand J (2002) Tumor response and clinical benefit in neuroendocrine tumors after 7.4 GBq (90)Y-DOTATOC. J Nucl Med 43:610–616PubMedGoogle Scholar
  19. 19.
    Li S, Peck-Radosavljevic M, Koller E, Koller F, Kaserer K, Kreil A, Kapiotis S, Hamwi A, Weich HA, Valent P, Angelberger P, Dudczak R, Virgolini I (2001) Characterization of (123)I-vascular endothelial growth factor-binding sites expressed on human tumour cells: possible implication for tumour scintigraphy. Int J Cancer 91:789–796PubMedCrossRefGoogle Scholar
  20. 20.
    MacLaren DC, Gambhir SS, Satyamurthy N, Barrio JR, Sharfstein S, Toyokuni T, Wu L, Berk AJ, Cherry SR, Phelps ME, Herschman HR (1999) Repetitive, non-invasive imaging of the dopamine D2 receptor as a reporter gene in living animals. Gene Ther 6:785–791PubMedCrossRefGoogle Scholar
  21. 21.
    Rogers BE, McLean SF, Kirkman RL, Della Manna D, Bright SJ, Olsen CC, Myracle AD, Mayo MS, Curiel DT, Buchsbaum DJ (1999) In vivo localization of [(111)In]-DTPA-D-Phe1-octreotide to human ovarian tumor xenografts induced to express the somatostatin receptor subtype 2 using an adenoviral vector. Clin Cancer Res 5:383–393PubMedGoogle Scholar
  22. 22.
    De Santes K, Slamon D, Anderson SK, Shepard M, Fendly B, Maneval D, Press O (1992) Radiolabeled antibody targeting of the HER-2/neu oncoprotein. Cancer Res 52:1916–1923PubMedGoogle Scholar
  23. 23.
    Schmieder AH, Winter PM, Caruthers SD, Harris TD, Williams TA, Allen JS, Lacy EK, Zhang H, Scott MJ, Hu G, Robertson JD, Wickline SA, Lanza GM (2005) Molecular MR imaging of melanoma angiogenesis with alphanubeta3-targeted paramagnetic nanoparticles. Magn Reson Med 53:621–627PubMedCrossRefGoogle Scholar
  24. 24.
    Frangioni JV (2003) In vivo near-infrared fluorescence imaging. Curr Opin Chem Biol 7:626–634PubMedCrossRefGoogle Scholar
  25. 25.
    Santra S, Xu J, Wang K, Tan W (2004) Luminescent nanoparticle probes for bioimaging. J Nanosci Nanotechnol 4:590–599PubMedCrossRefGoogle Scholar
  26. 26.
    Chung JK (2002) Sodium iodide symporter: its role in nuclear medicine. J Nucl Med 43:1188–1200PubMedGoogle Scholar
  27. 27.
    Chung JK, Kang JH (2004) Translational research using the sodium/iodide symporter in imaging and therapy. Eur J Nucl Med Mol Imaging 31:799–802PubMedCrossRefGoogle Scholar
  28. 28.
    Ichikawa T, Hogemann D, Saeki Y, Tyminski E, Terada K, Weissleder R, Chiocca EA, Basilion JP (2002) MRI of transgene expression: correlation to therapeutic gene expression. Neoplasia 4:523–530PubMedCrossRefGoogle Scholar
  29. 29.
    Hogemann-Savellano D, Bos E, Blondet C, Sato F, Abe T, Josephson L, Weissleder R, Gaudet J, Sgroi D, Peters PJ, Basilion JP (2003) The transferrin receptor: a potential molecular imaging marker for human cancer. Neoplasia 5:495–506PubMedGoogle Scholar
  30. 30.
    Weissleder R, Moore A, Mahmood U, Bhorade R, Benveniste H, Chiocca EA, Basilion JP (2000) In vivo magnetic resonance imaging of transgene expression. Nat Med 6:351–355PubMedCrossRefGoogle Scholar
  31. 31.
    Tung CH, Mahmood U, Bredow S, Weissleder R (2000) In vivo imaging of proteolytic enzyme activity using a novel molecular reporter. Cancer Res 60:4953–4958PubMedGoogle Scholar
  32. 32.
    Bremer C, Tung CH, Weissleder R (2001) In vivo molecular target assessment of matrix metalloproteinase inhibition. Nat Med 7:743–748PubMedCrossRefGoogle Scholar
  33. 33.
    Ntziachristos V, Tung CH, Bremer C, Weissleder R (2002) Fluorescence molecular tomography resolves protease activity in vivo. Nat Med 8:757–760PubMedCrossRefGoogle Scholar
  34. 34.
    Vihinen P, Kahari VM (2002) Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int J Cancer 99:157–166PubMedCrossRefGoogle Scholar
  35. 35.
    Bogdanov A, Jr., Matuszewski L, Bremer C, Petrovsky A, Weissleder R (2002) Oligomerization of paramagnetic substrates result in signal amplification and can be used for MR imaging of molecular targets. Mol Imaging 1:16–23PubMedCrossRefGoogle Scholar
  36. 36.
    Chen JW, Pham W, Weissleder R, Bogdanov A Jr (2004) Human myeloperoxidase: a potential target for molecular MR imaging in atherosclerosis. Magn Reson Med 52:1021–1028PubMedCrossRefGoogle Scholar
  37. 37.
    Yaghoubi SS, Barrio JR, Namavari M, Satyamurthy N, Phelps ME, Herschman HR, Gambhir SS (2005) Imaging progress of herpes simplex virus type 1 thymidine kinase suicide gene therapy in living subjects with positron emission tomography. Cancer Gene Ther 12:329–339PubMedCrossRefGoogle Scholar
  38. 38.
    Louie AY, Huber MM, Ahrens ET, Rothbacher U, Moats R, Jacobs RE, Fraser SE, Meade TJ (2000) In vivo visualization of gene expression using magnetic resonance imaging. Nat Biotechnol 18:321–325PubMedCrossRefGoogle Scholar
  39. 39.
    Tung CH, Zeng Q, Shah K, Kim DE, Schellingerhout D, Weissleder R (2004) In vivo imaging of beta-galactosidase activity using far red fluorescent switch. Cancer Res 64:1579–1583PubMedCrossRefGoogle Scholar
  40. 40.
    Audic Y, Hartley RS (2004) Post-transcriptional regulation in cancer. Biol Cell 96:479–498PubMedCrossRefGoogle Scholar
  41. 41.
    Wu JC, Inubushi M, Sundaresan G, Schelbert HR, Gambhir SS (2002) Optical imaging of cardiac reporter gene expression in living rats. Circulation 105:1631–1634PubMedCrossRefGoogle Scholar
  42. 42.
    de Boer J, van Blitterswijk C, Lowik C (2006) Bioluminescent imaging: emerging technology for non-invasive imaging of bone tissue engineering. Biomaterials 27:1851–1858PubMedCrossRefGoogle Scholar
  43. 43.
    Marignol L, Lawler M, Coffey M, Hollywood D (2005) Achieving hypoxia-inducible gene expression in tumors. Cancer Biol Ther 4:359–364PubMedCrossRefGoogle Scholar
  44. 44.
    Murdoch C, Lewis CE (2005) Macrophage migration and gene expression in response to tumor hypoxia. Int J Cancer 117:701–708PubMedCrossRefGoogle Scholar
  45. 45.
    Dachs GU, Patterson AV, Firth JD, Ratcliffe PJ, Townsend KM, Stratford IJ, Harris AL (1997) Targeting gene expression to hypoxic tumor cells. Nat Med 3:515–520PubMedCrossRefGoogle Scholar
  46. 46.
    Liu J, Qu R, Ogura M, Shibata T, Harada H, Hiraoka M (2005) Real-time imaging of hypoxia-inducible factor-1 activity in tumor xenografts. J Radiat Res (Tokyo) 46:93–102CrossRefGoogle Scholar
  47. 47.
    Huang D, Desbois A, Hou ST (2005) A novel adenoviral vector which mediates hypoxia-inducible gene expression selectively in neurons. Gene Ther 12:1369–1376PubMedCrossRefGoogle Scholar
  48. 48.
    Jacobs A, Dubrovin M, Hewett J, Sena-Esteves M, Tan CW, Slack M, Sadelain M, Breakefield XO, Tjuvajev JG (1999) Functional coexpression of HSV-1 thymidine kinase and green fluorescent protein: implications for noninvasive imaging of transgene expression. Neoplasia 1:154–161PubMedCrossRefGoogle Scholar
  49. 49.
    Doubrovin M, Ponomarev V, Beresten T, Balatoni J, Bornmann W, Finn R, Humm J, Larson S, Sadelain M, Blasberg R, Gelovani Tjuvajev J (2001) Imaging transcriptional regulation of p53-dependent genes with positron emission tomography in vivo. Proc Natl Acad Sci U S A 98:9300–9305PubMedCrossRefGoogle Scholar
  50. 50.
    Sato M, Johnson M, Zhang L, Zhang B, Le K, Gambhir SS, Carey M, Wu L (2003) Optimization of adenoviral vectors to direct highly amplified prostate-specific expression for imaging and gene therapy. Mol Ther 8:726–737PubMedCrossRefGoogle Scholar
  51. 51.
    Cheng WS, Kraaij R, Nilsson B, van der Weel L, de Ridder CM, Totterman TH, Essand M (2004) A novel TARP-promoter-based adenovirus against hormone-dependent and hormone-refractory prostate cancer. Mol Ther 10:355–364PubMedCrossRefGoogle Scholar
  52. 52.
    Iyer M, Salazar FB, Wu L, Carey M, Gambhir SS (2006) Bioluminescence imaging of systemic tumor targeting using a prostate-specific lentiviral vector. Hum Gene Ther 17:125–132PubMedCrossRefGoogle Scholar
  53. 53.
    Iyer M, Salazar FB, Lewis X, Zhang L, Carey M, Wu L, Gambhir SS (2004) Noninvasive imaging of enhanced prostate-specific gene expression using a two-step transcriptional amplification-based lentivirus vector. Mol Ther 10:545–552PubMedCrossRefGoogle Scholar
  54. 54.
    Adams JY, Johnson M, Sato M, Berger F, Gambhir SS, Carey M, Iruela-Arispe ML, Wu L (2002) Visualization of advanced human prostate cancer lesions in living mice by a targeted gene transfer vector and optical imaging. Nat Med 8:891–897PubMedGoogle Scholar
  55. 55.
    Herschman HR (2002) Non-invasive imaging of reporter genes. J Cell Biochem Suppl 39:36–44PubMedCrossRefGoogle Scholar
  56. 56.
    Phelps ME (2000) PET: the merging of biology and imaging into molecular imaging. J Nucl Med 41:661–681PubMedGoogle Scholar
  57. 57.
    Hemminki A, Zinn KR, Liu B, Chaudhuri TR, Desmond RA, Rogers BE, Barnes MN, Alvarez RD, Curiel DT (2002) In vivo molecular chemotherapy and noninvasive imaging with an infectivity-enhanced adenovirus. J Natl Cancer Inst 94:741–749PubMedGoogle Scholar
  58. 58.
    Altmann A, Kissel M, Zitzmann S, Kubler W, Mahmut M, Peschke P, Haberkorn U (2003) Increased MIBG uptake after transfer of the human norepinephrine transporter gene in rat hepatoma. J Nucl Med 44:973–980PubMedGoogle Scholar
  59. 59.
    Jacobs A, Voges J, Reszka R, Lercher M, Gossmann A, Kracht L, Kaestle C, Wagner R, Wienhard K, Heiss WD (2001) Positron-emission tomography of vector-mediated gene expression in gene therapy for gliomas. Lancet 358:727–729PubMedCrossRefGoogle Scholar
  60. 60.
    Reszka RC, Jacobs A, Voges J (2005) Liposome-mediated suicide gene therapy in humans. Methods Enzymol 391:200–208PubMedGoogle Scholar
  61. 61.
    Laxman B, Hall DE, Bhojani MS, Hamstra DA, Chenevert TL, Ross BD, Rehemtulla A (2002) Noninvasive real-time imaging of apoptosis. Proc Natl Acad Sci U S A 99:16551–16555PubMedCrossRefGoogle Scholar
  62. 62.
    Hackman T, Doubrovin M, Balatoni J, Beresten T, Ponomarev V, Beattie B, Finn R, Bornmann W, Blasberg R, Tjuvajev JG (2002) Imaging expression of cytosine deaminase-herpes virus thymidine kinase fusion gene (CD/TK) expression with [124I]FIAU and PET. Mol Imaging 1:36–42PubMedCrossRefGoogle Scholar
  63. 63.
    Herschman HR (2003) Molecular imaging: looking at problems, seeing solutions. Science 302:605–608PubMedCrossRefGoogle Scholar
  64. 64.
    Weissleder R, Simonova M, Bogdanova A, Bredow S, Enochs WS, Bogdanov A Jr (1997) MR imaging and scintigraphy of gene expression through melanin induction. Radiology 204:425–429PubMedGoogle Scholar
  65. 65.
    Enochs WS, Petherick P, Bogdanova A, Mohr U, Weissleder R (1997) Paramagnetic metal scavenging by melanin: MR imaging. Radiology 204:417–423PubMedGoogle Scholar
  66. 66.
    Bogdanov AA Jr, Weissleder R (2002) In vivo imaging of gene delivery and expression. Trends Biotech 20:511–518Google Scholar
  67. 67.
    Rehemtulla A, Stegman LD, Cardozo SJ, Gupta S, Hall DE, Contag CH, Ross BD (2000) Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2:491–495PubMedCrossRefGoogle Scholar
  68. 68.
    Rudin M, Rausch M, Stoeckli M (2005) Molecular imaging in drug discovery and development: potential and limitations of nonnuclear methods. Mol Imaging Biol 7:5–13PubMedCrossRefGoogle Scholar
  69. 69.
    Thorne SH, Tam BY, Kirn DH, Contag CH, Kuo CJ (2006) Selective Intratumoral Amplification of an Antiangiogenic Vector by an Oncolytic Virus Produces Enhanced Antivascular and Anti-tumor Efficacy. Mol TherGoogle Scholar
  70. 70.
    Cronin J, Zhang XY, Reiser J (2005) Altering the tropism of lentiviral vectors through pseudotyping. Curr Gene Ther 5:387–398PubMedCrossRefGoogle Scholar
  71. 71.
    Pack DW, Hoffman AS, Pun S, Stayton PS (2005) Design and development of polymers for gene delivery. Nat Rev Drug Discov 4:581–593PubMedCrossRefGoogle Scholar
  72. 72.
    Li C, Bowles DE, van Dyke T, Samulski RJ (2005) Adeno-associated virus vectors: potential applications for cancer gene therapy. Cancer Gene Ther 12:913–925PubMedCrossRefGoogle Scholar
  73. 73.
    Barzon L, Stefani AL, Pacenti M, Palu G (2005) Versatility of gene therapy vectors through viruses. Expert Opin Biol Ther 5:639–662PubMedCrossRefGoogle Scholar
  74. 74.
    Banerjee P, Reichardt W, Weissleder R, Bogdanov A Jr (2004) Novel hyperbranched dendron for gene transfer in vitro and in vivo. Bioconjug Chem 15:960–968PubMedCrossRefGoogle Scholar
  75. 75.
    Meilander-Lin NJ, Cheung PJ, Wilson DL, Bellamkonda RV (2005) Sustained in vivo gene delivery from agarose hydrogel prolongs nonviral gene expression in skin. Tissue Eng 11:546–555PubMedCrossRefGoogle Scholar
  76. 76.
    Schellingerhout D, Rainov NG, Breakefield XO, Weissleder R (2000) Quantitation of HSV mass distribution in a rodent brain tumor model. Gene Ther 7:1648–1655PubMedCrossRefGoogle Scholar
  77. 77.
    Unger EC, Hersh E, Vannan M, McCreery T (2001) Gene delivery using ultrasound contrast agents. Echocardiography 18:355–361PubMedCrossRefGoogle Scholar
  78. 78.
    Bos C, Lepetit-Coiffe M, Quesson B, Moonen CT (2005) Simultaneous monitoring of temperature and T1: methods and preliminary results of application to drug delivery using thermosensitive liposomes. Magn Reson Med 54:1020–1024PubMedCrossRefGoogle Scholar
  79. 79.
    Tarner IH, Nakajima A, Seroogy CM, Ermann J, Levicnik A, Contag CH, Fathman CG (2002) Retroviral gene therapy of collagen-induced arthritis by local delivery of IL-4. Clin Immunol 105:304–314PubMedCrossRefGoogle Scholar
  80. 80.
    Tarner IH, Slavin AJ, McBride J, Levicnik A, Smith R, Nolan GP, Contag CH, Fathman CG (2003) Treatment of autoimmune disease by adoptive cellular gene therapy. Ann N Y Acad Sci 998:512–519PubMedCrossRefGoogle Scholar
  81. 81.
    Leo BM, Li X, Balian G, Anderson DG (2004) In vivo bioluminescent imaging of virus-mediated gene transfer and transduced cell transplantation in the intervertebral disc. Spine 29:838–844PubMedCrossRefGoogle Scholar
  82. 82.
    Song Y, Morikawa S, Morita M, Inubushi T, Takada T, Torii R, Tooyama I (2006) Magnetic resonance imaging using hemagglutinating virus of Japan-envelope vector successfully detects localization of intra-cardially administered microglia in normal mouse brain. Neurosci Lett 395:42–45PubMedCrossRefGoogle Scholar
  83. 83.
    Hauger O, Delalande C, Deminiere C, Fouqueray B, Ohayon C, Garcia S, Trillaud H, Combe C, Grenier N (2000) Nephrotoxic nephritis and obstructive nephropathy: evaluation with MR imaging enhanced with ultrasmall superparamagnetic iron oxide-preliminary findings in a rat model. Radiology 217:819–826PubMedGoogle Scholar
  84. 84.
    Harisinghani MG, Barentsz J, Hahn PF, Deserno WM, Tabatabaei S, van de Kaa CH, de la Rosette J, Weissleder R (2003) Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med 348:2491–2499PubMedCrossRefGoogle Scholar
  85. 85.
    Dubey P, Su H, Adonai N, Du S, Rosato A, Braun J, Gambhir SS, Witte ON (2003) Quantitative imaging of the T cell antitumor response by positron-emission tomography. Proc Natl Acad Sci U S A 100:1232–1237PubMedCrossRefGoogle Scholar
  86. 86.
    Koehne G, Doubrovin M, Doubrovina E, Zanzonico P, Gallardo HF, Ivanova A, Balatoni J, Teruya-Feldstein J, Heller G, May C, Ponomarev V, Ruan S, Finn R, Blasberg RG, Bornmann W, Riviere I, Sadelain M, O’Reilly RJ, Larson SM, Tjuvajev JG (2003) Serial in vivo imaging of the targeted migration of human HSV-TK-transduced antigen-specific lymphocytes. Nat Biotechnol 21:405–413PubMedCrossRefGoogle Scholar
  87. 87.
    de Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC, Oyen WJ, Bonenkamp JJ, Boezeman JB, Adema GJ, Bulte JW, Scheenen TW, Punt CJ, Heerschap A, Figdor CG (2005) Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 23:1407–1413PubMedCrossRefGoogle Scholar
  88. 88.
    Daley GQ, Goodell MA, Snyder EY (2003) Realistic prospects for stem cell therapeutics. Hematology (Am Soc Hematol Educ Program):398–418Google Scholar
  89. 89.
    Frank JA, Miller BR, Arbab AS, Zywicke HA, Jordan EK, Lewis BK, Bryant LH Jr, Bulte JW (2003) Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 228:480–487PubMedCrossRefGoogle Scholar
  90. 90.
    Hoehn M, Kustermann E, Blunk J, Wiedermann D, Trapp T, Wecker S, Focking M, Arnold H, Hescheler J, Fleischmann BK, Schwindt W, Buhrle C (2002) Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci U S A 99:16267–16272PubMedCrossRefGoogle Scholar
  91. 91.
    Cao YA, Wagers AJ, Beilhack A, Dusich J, Bachmann MH, Negrin RS, Weissman IL, Contag CH (2004) Shifting foci of hematopoiesis during reconstitution from single stem cells. Proc Natl Acad Sci U S A 101:221–226PubMedCrossRefGoogle Scholar
  92. 92.
    Guilhon E, Voisin P, de Zwart JA, Quesson B, Salomir R, Maurange C, Bouchaud V, Smirnov P, de Verneuil H, Vekris A, Canioni P, Moonen CT (2003) Spatial and temporal control of transgene expression in vivo using a heat-sensitive promoter and MRI-guided focused ultrasound. J Gene Med 5:333–342PubMedCrossRefGoogle Scholar
  93. 93.
    Letavernier B, Salomir R, Delmas Y, Rome C, Couillaud F, Desmouliere A, Hauger O, Grenier N, Combe C, Ripoche J, Moonen C (2006) Spatio-temporal expression control of a heat shock promoter-driven transgene delivered in the kidney by modified mesenchymal stem cells: a feasibility study using MR guided focused ultrasound. International Society for Magnetic Resonance in Medicine 14th Scientific Meeting and Exhibition, 6–12th May 2006, Seattle, Washington, USAGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Claire Rome
    • 1
  • Franck Couillaud
    • 1
  • Chrit T. W. Moonen
    • 1
    • 2
  1. 1.Laboratory for Molecular and Functional Imaging: From Physiology to Therapy ERT CNRSUniversité Victor SegalenBordeauxFrance
  2. 2.Imagerie Moléculaire et Fonctionnelle, ERT CNRSUniversité Victor SegalenBordeauxFrance

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