Use of in vivo bioluminescence and MRI to determine hyperthermia-induced changes in luciferase activity under the control of an hsp70 promoter

NMR in Biomedicine

Volumn 25, Issue 12, 2012, Pages 1378-1391

  Hundt, Walter ^a,b   Schink, Christian ^b   Steinbach, Silke ^b   O'Connell Rodwell, Caitlin E ^c   Mayer, Dirk ^a   Burbelko, Mykhaylo ^b   Kießling, Andreas ^b   Guccione, Samira ^a  

^a STANFORD UNIVERSITY   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bioluminescence imaging; Heat; HSP70; Luciferase; Magnetic resonance imaging

Indexed keywords

ACQUISITION MODES; APPARENT DIFFUSION COEFFICIENT; BIOCHEMICAL CHANGES; BIOLUMINESCENCE IMAGING; CELL LINES; CONTRAST MEDIUM; CORRELATION COEFFICIENT; DYNAMIC CONTRAST ENHANCED MRI; FAST SPIN ECHOS; GENERAL ELECTRICS; HEAT; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HSP70; IMMUNOBLOT ANALYSIS; IMMUNOBLOTTING; IN-VIVO; LUCIFERASE; LUCIFERASE ACTIVITIES; MRI SCAN; MRI SCANNERS; OPTICAL IMAGING; PROMOTER FRAGMENTS; PROTEIN PRODUCTION; REPORTER GENE; SET TIME; SPIN ECHO; TISSUE TYPES; TUMOR CELL LINES; TUMOR TISSUES; WATER BATHS;

BIOLUMINESCENCE; CELL CULTURE; CONTRAST MEDIA; DIFFUSION; ENZYME ACTIVITY; GENES; MAGNETIC RESONANCE IMAGING; PHOSPHORESCENCE; PLANTS (BOTANY); PROTEINS; SPIN POLARIZATION; TUMORS;

TRANSCRIPTION;

HEAT SHOCK PROTEIN 70; LUCIFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; CANCER CELL CULTURE; COMPUTER PROGRAM; CONTRAST ENHANCEMENT; CONTROLLED STUDY; CORRELATION COEFFICIENT; DIFFUSION COEFFICIENT; DIFFUSION WEIGHTED IMAGING; ENZYME ACTIVITY; ENZYME REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYPERTHERMIA; IMAGE ANALYSIS; IMMUNOBLOTTING; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REPORTER GENE; TEMPERATURE SENSITIVITY; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE, TUMOR; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYPERTHERMIA, INDUCED; IMMUNOBLOTTING; KINETICS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MAGNETIC RESONANCE IMAGING; MICE; NIH 3T3 CELLS; PROMOTER REGIONS, GENETIC; SIGNAL-TO-NOISE RATIO; TEMPERATURE; TIME FACTORS; TRANSFECTION;

MUS;

EID: 84868152705     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2811     Document Type: Article

References (61)

1. Rome C, Couillaud F, Moonen C. Spatial and temporal control of expression of therapeutic genes using heat shock protein promoters. Methods 2005; 35: 188-198.
2. Arispe N, DeMaio A. ATP and ADP modulate a cation channel formed by Hsp70 in acidic phospholipid membranes. J. Biol. Chem. 2000; 275: 30 839-30 843.
3. Hendrick JP, Hartl FU. Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 1993; 62: 349-384.
4. DeNagel DC, Pierce SK. A case for chaperones in antigen processing. Immunol. Today 1992; 3: 86-89.
5. Hartl FU. Molecular chaperones in protein folding. Nature 1996; 381: 571-580.
6. Kiang JG, Tsokos GC. Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol. Ther. 1998; 80: 183-201.
7. Siddiqui F, Avery PR, Li CY, Zhang X, LaRue SM, Dewhirst MW, Ullrich RL. Induction of the human heat shock promoter HSP70B by nutritional stress: implications for cancer gene therapy. Cancer Invest. 2008; 26(6): 553-561.
8. Marschall S, Rothschild MA, Bohnert M. Expression of heat-shock protein 70 (Hsp70) in the respiratory tract and lungs of fire victims. Int. J. Legal Med. 2006; 120(6): 355-359.
9. Fujitomi Y, Kashima K, Ueda S, Yamada Y, Mori H, Uchida Y. Histopathological features of liver damage induced by laser ablation in rabbits. Lasers Surg. Med. 1999; 24: 14-23.
10. Contag CH, Bachmann MH. Advances in in vivo bioluminescence imaging of gene expression. Annu. Rev. Biomed. Eng. 2002; 4: 235-260.
11. Huber P, Jenne J, Rastert R, Simiantonakis I, Sinn HP, Strittmatter HJ, Fournier D, Wannenmacher M, Debus J. A new noninvasive approach in breast cancer therapy using magnetic resonance imaging-guided focused ultrasound surgery. Cancer Res. 2001; 61: 8441-8447.
12. Kogure T, Kogure K. Molecular and biochemical events within the brain subjected to cerebral ischemia (targets for therapeutical intervention). Clin. Neurosci. 1997; 4: 179-183.
13. Choyke PL, Dwyer AJ, Knopp MV. Functional tumor imaging with dynamic contrast-enhanced magnetic resonance imaging. J. Magn. Reson. Imaging 2003; 17: 509-520.
14. Reischauer C, Staempfli P, Jaermann T, Boesiger P. Construction of a temperature-controlled diffusion phantom for quality control of diffusion measurements. J. Magn. Reson. Imaging 2009; 29(3): 692-698.
15. Lüdemann L, Wlodarczyk W, Nadobny J, Weihrauch M, Gellermann J, Wust P. Non-invasive magnetic resonance thermography during regional hyperthermia. Int. J. Hyperthermia 2010; 26(3): 273-282.
16. Baur A, Stabler A, Wendtner CM, Arbogast S, Rahman SA, Santl M, Issels R, Reiser M. MR-imaging changes of musculoskeletal soft-tissue sarcomas associated with neoadjuvant chemotherapy and hyperthermia. Int. J. Hyperthermia 2003; 19: 391-401.
17. Pahernik S, Peller M, Dellian M, Loeffler R, Issels R, Reiser M, Messmer K, Goetz A. Validation of MR thermometry technology: a small animal model for hyperthermic treatment of tumours. Res. Exp. Med. (Berlin) 1999: 199: 59-71.
18. Rehemtulla A, Stegman LD, Cardozo SJ, Gupta S, Hall DE, Contag CH, Ross BD. Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2000; 2: 491-495.
19. Hoffmann U, Brix G, Knopp MV, Hess T, Lorenz WJ. Pharmacokinetic mapping of the breast: a new method for dynamic MR mammography. Magn. Reson. Med. 1995; 33: 506-514.
20. Brix G, Semmler W, Port R, Schad LR, Layer G, Lorenz WJ. Pharmacokinetic parameters in CNS Gd-DTPA enhanced MR imaging. J. Comput. Assist. Tomogr. 1991; 15: 621-628.
21. Pelham HRB. Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J. 1984; 3: 3095-3100.
22. Li GC, Li L, Liu YK, Mak JY, Chen L, Lee WMF. Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc. Natl. Acad. Sci. USA 1991; 88: 1681-1685.
23. Angelidis CE, Nova C, Lazaridis I, Kontoyiannis D, Kollias G, Pagoulatos GN. Overexpression of HSP70 in transgenic mice results in increased cell thermotolerance. Transgenics 1996; 2: 111-117.
24. Hundt W, O'Connell-Rodwell CE, Bednarski MD, Steinbach S, Guccione S. In vitro effect of focused ultrasound or thermal stress on HSP70 expression and cell viability in three tumor cell lines. Acad. Radiol. 2007; 14: 859-870.
25. Hundt W, Steinbach S, Burbelko M, Kiessling A, Rominger M, O'Connell-Rodwell CE, Mayer D, Bednarski MD, Guccione S. Induction of luciferase activity under the control of an hsp70 promoter using high-intensity focused ultrasound: combination of bioluminescence and MRI imaging in three different tumour models. Technol. Cancer Res. Treat. 2011; 10(2): 197-210.
26. Ménoret A, Chaillot D, Callahan M, Jacquin C. Hsp70, an immunological actor playing with the intracellular self under oxidative stress. Int. J. Hyperthermia 2002; 18(6): 490-505.
27. Gething MJ, Sambrook J. Protein folding in the cell. Nature 1992; 355(6355): 33-45.
28. Henle KJ, Nagle WA. Inhibition of heat shock protein synthesis and protein glycosylation by stepdown heating. Exp. Cell Res. 1991; 196(2): 184-191.
29. Henle KJ, Kaushal GP, Nagle WA, Nolen GT. Prompt protein glycosylation during acute heat stress. Exp. Cell Res. 1993; 207(2): 245-251.
30. Henle K, Jethmalani S, Li L, Li GC. Protein glycosylation in a heat-resistant rat fibroblast cell model expressing human HSP70. Biochem. Biophys. Res. Commun. 1997; 232: 26-32.
31. Jethmalani SM, Henle KJ. Partial homology of stress glycoprotein GP62 with HSP70. Exp. Cell Res. 1997; 232(1): 8-16.
32. Vekris A, Maurange C, Moonen C, Mazurier F, De Verneuil H, Canioni P, Voisin P. Control of transgene expression using local hyperthermia in combination with a heat-sensitive promoter. J. Gene Med. 2000; 2: 89-96.
33. Beuth J. Evidence-based complementary oncology: innovative approaches to optimise standard therapy strategies. Anticancer Res. 2010; 30(5): 1767-1771.
34. 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. Spatial and temporal control of transgene expression in vivo using a heat-sensitive promoter and MRI-guided focused ultrasound. J. Gene Med. 2003; 5: 333-342.
35. Blackburn RV, Galoforo SS, Corry PM, Lee YJ. Adenoviral-mediated transfer of a heat-inducible double suicide gene into prostate carcinoma cells. Cancer Res. 1998; 58: 1358-1362.
36. Deckers R, Quesson B, Arsaut J, Eimer S, Couillaud F, Moonen CT. Image-guided, non-invasive spatiotemporal control of gene expression. Proc. Natl. Acad. Sci. USA 2009; 106: 1175-1180.
37. O'Connell-Rodwell CE, Mackanos MA, Simanovskii D, Cao YA, Bachmann MH, Schwettman HA, Contag CH. In vivo analysis of heat shock-protein-70 induction following pulsed laser irradiation in a transgenic reporter mouse. J. Biomed. Opt. 2008; 13: 030501.
38. Hundt W, Steinbach S, O'Connell-Rodwell CE, Bednarski MD, Guccione S. The effect of high intensity focused ultrasound on luciferase activity on two tumor cell lines in vitro, under the control of a CMV promoter. Ultrasonic 2009; 49: 312-318.
39. Wilmink GJ, Opalenik SR, Beckham JT, Davidson JM, Jansen ED. Assessing laser-tissue damage with bioluminescent imaging. J. Biomed. Opt. 2006; 11(4)L: 041114.
40. Liotta LA, Kleinerman J, Saidel G. Quantitative relationships of intravascular tumor cells, tumor vessels and pulmonary metastases following tumor implantation. Cancer Res. 1974; 34: 997-1004.
41. Weidner N. Tumor angiogenesis: review of current applications in tumor prognostication. Semin. Diagn. Pathol. 1993; 10: 302-313.
42. Tofts PS. Modeling tracer kinetics in dynamic GdDTPA MR imaging. J. Magn. Reson. Imaging 1997; 7: 91-101.
43. Tofts PS, Kermode AG. Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging: 1. Fundamental concepts. Magn. Reson. Med. 1991; 17: 357-367.
44. Weinmann HJ, Brasch RC, Press WR, Wesby GE. Characteristics of gadolinium DTPA complex: a potential NMR contrast agent. Am. J. Roentgenol. 1984; 142: 619-624.
45. Tyninnen O, Aronen HJ, Ruhala M, Paetau A, von Boguslawski K, Salonen O, Jaaskelainen J, Paavonen T. MRI enhancement and microvascular density in gliomas. Correlation with tumor cell proliferation. Invest. Radiol. 1999; 34: 427-434.
46. Buckley DL, Drew PJ, Mussurakis S, Monson JR, Horsman A. Microvessel density of invasive breast cancer assessed by dynamic Gd-DTPA enhanced MRI. J. Magn. Reson. Imaging 1997; 7: 461-464.
47. Pham CD, Roberts TP, van Bruggen N, Melnyk O, Mann J, Ferrara N, Cohen RL, Brasch RC. Magnetic resonance imaging detects suppression of tumor vascular permeability after administration of antibody to vascular endothelial growth factor. Cancer Invest. 1998; 16: 225-230.
48. Gullino PM. Considerations of blood supply and fluid exchange in tumors. In: Gautherie M, Albert E (eds). Biomedical Thermology. Alan R. Liss: New York; 1982, pp. 1-20.
49. 1H NMR relaxation times and water compartmentalization in experimental tumor models. Magn. Reson. Imaging 1986; 4: 335-342.
50. Gore JC, Brown MS. Pathophysiological significance of relaxation. In: Par-tam CL, Price RR, Patton JA, Kulkarni MV, James AE (eds). Magnetic Resonance Imaging. Saunders: Philadelphia, PA; 1988, pp. 1070-1074.
51. Hawighorst H, Knapstein PG, Knopp MV, Weikel W, Brix G, Zuna I, Schönberg SO, Essig M, Vaupel P, van Kaick G. Uterine cervical carcinoma: comparison of standard and pharmacokinetic analysis of time-intensity curves for assessment of tumor angiogenesis and patient survival. Cancer Res. 1998; 58: 3598-3602.
52. Contag CH, Spilman SD, Contag PR, Oshiro M, Eames B. Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem. Photobiol. 1997; 66: 523-531.
53. Egmont-Petersen M, Hogendoorn PC, van der Geest RJ, Vrooman HA, van der Woude H, Janssen JP, Bloem JL, Reiber JH. Detection of areas with viable remnant tumor in postchemotherapy patients with Ewing's sarcoma by dynamic contrast-enhanced MRI using pharmacokinetic modeling. Magn. Reson. Imaging 2000; 18(5): 525-535.
54. Kiessling F, Farhan N, Lichy MP, Vosseler S, Heilmann M, Krix M, Bohlen P, Miller DW, Mueller MM, Semmler W, Fusenig NE, Delorme S. Dynamic contrast-enhanced magnetic resonance imaging rapidly indicates vessel regression in human squamous cell carcinomas grown in nude mice caused by VEGF receptor 2 blockade with DC101. Neoplasia 2004; 6(3): 213-223.
55. Gaustad JV, Brurberg KG, Simonsen TG, Mollatt CS, Rofstad EK. Tumor vascularity assessed by magnetic resonance imaging and intravital microscopy imaging. Neoplasia 2008; 10(4): 354-362.
56. Lyng H, Haraldseth O, Rofstad EK. Measurement of cell density and necrotic fraction in human melanoma xenografts by diffusion weighted magnetic resonance imaging. Magn. Reson. Med. 2000; 43: 823-836.
57. Benveniste H, Hedlund LW, Johnson GA. Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 1992; 23: 746-754.
58. Jain RK. Vascular and interstitial barriers to delivery of therapeutic agents in tumors. Cancer Metastasis Rev. 1990; 9: 253-266.
59. Mannelli L, Kim S, Hajdu CH, Babb JS, Clark TW, Taouli B. Assessment of tumor necrosis of hepatocellular carcinoma after chemoembolization: diffusion-weighted and contrast-enhanced MRI with histopathologic correlation of the explanted liver. Am. J. Roentgenol. 2009; 193(4): 1044-1052.
60. Leeds NE, Kumar AJ, Zhou XJ, McKinnon GC. Magnetic resonance imaging of benign spinal lesions simulating metastasis: role of diffusion-weighted imaging. Top. Magn. Reson. Imaging 2000; 11: 224-234.
61. Spuentrup E, Buecker A, Adam G, van Vaals JJ, Guenther RW. Diffusion-weighted MR imaging for differentiation of benign fracture edema and tumor infiltration of the vertebral body. Am. J. Roentgenol. 2001; 176: 351-358.