Selective in vivo imaging of syngeneic, spontaneous, and xenograft tumors using a novel tumor cell-specific hsp70 peptide-based probe

Cancer Research

Volumn 74, Issue 23, 2014, Pages 6903-6912

  Stangl, Stefan ^a   Varga, Julia ^b   Freysoldt, Bianca ^a   Trajkovic Arsic, Marija ^c   Siveke, Jens T ^c   Greten, Florian R ^b   Ntziachristos, Vasilis ^a   Multhoff, Gabriele ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Institute for Tumor Biology and Experimental Therapy Georg Speyer Haus   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PENETRATING PEPTIDE; HEAT SHOCK PROTEIN 70; FLUORESCENT DYE; VITRONECTIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CELL SPECIFICITY; COLON ADENOCARCINOMA; COLON TUMOR; CONTROLLED STUDY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR PROBE; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PROTEIN METABOLISM; RELIABILITY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR DIFFERENTIATION; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; CARCINOGENESIS; DIAGNOSTIC IMAGING; HCT116 CELL LINE; HELA CELL LINE; MCF 7 CELL LINE; METABOLISM; MULTIMODAL IMAGING; PHYSIOLOGY; PROCEDURES; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CARCINOGENESIS; CELL LINE, TUMOR; CELL-PENETRATING PEPTIDES; DIAGNOSTIC IMAGING; FEMALE; FLUORESCENT DYES; HCT116 CELLS; HELA CELLS; HETEROGRAFTS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; INTEGRIN ALPHAVBETA3; MCF-7 CELLS; MICE; MICE, INBRED BALB C; MULTIMODAL IMAGING; TUMOR MICROENVIRONMENT;

EID: 84917690627     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0413     Document Type: Article

References (37)

1. Snyder EL, Dowdy SF. Cell penetrating peptides in drug delivery. Pharm Res 2004;21:389-93.
2. Kondo E, Saito K, Tashiro Y, Kamide K, Uno S, Furuya T, et al. Tumour lineage-homing cell-penetrating peptides as anticancer molecular delivery systems. Nat Commun 2012;3:951.
3. El-Andaloussi S, Holm T, Langel U. Cell-penetrating peptides: mechanisms and applications. Curr Pharm Des 2005;11: 3597-611.
4. Farkas B, Hantschel M, Magyarlaki M, Becker B, Scherer K, Landthaler M, et al. Heat shock protein 70 membrane expression and melanoma- associated marker phenotype in primary and metastatic melanoma. Melanoma Res 2003;13:147-52.
5. Hantschel M, Pfister K, Jordan A, Scholz R, Andreesen R, Schmitz G, et al. Hsp70 plasma membrane expression on primary tumor biopsy material and bone marrow of leukemic patients. Cell Stress Chaperones 2000;5:438-42.
6. Sakamoto M, Effendi K, Masugi Y. Molecular diagnosis of multistage hepatocarcinogenesis. Japanese J Clin Oncol 2010;40:891-6.
7. Sherman M, Multhoff G. Heat shock proteins in cancer. Ann N Y Acad Sci 2007;1113:192-201.
8. Kurahashi T, Miyake H, Hara I, Fujisawa M. Expression of major heat shock proteins in prostate cancer: correlation with clinicopathological outcomes in patients undergoing radical prostatectomy. J Urol 2007;177:757-61.
9. Multhoff G, Botzler C, Jennen L, Schmidt J, Ellwart J, Issels R. Heat shock protein 72 on tumor cells: a recognition structure for natural killer cells. J Immunol 1997;158:4341-50.
10. Radons J, Multhoff G. Immunostimulatory functions of membranebound and exported heat shock protein 70. Exerc Immunol Rev 2005;11:17-33.
11. Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, Hoyer-Hansen M, et al. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med 2004;200:425-35.
12. Steiner K, Graf M, Hecht K, Reif S, Rossbacher L, Pfister K, et al. High HSP70-membrane expression on leukemic cells from patients with acute myeloid leukemia is associated with a worse prognosis. Leukemia 2006;20:2076-9.
13. Thanner F, Sutterlin MW, Kapp M, Rieger L, Kristen P, Dietl J, et al. Heat-shock protein 70 as a prognostic marker in node-negative breast cancer. Anticancer Res 2003;23:1057-62.
14. Pfister K, Radons J, Busch R, Tidball JG, Pfeifer M, Freitag L, et al. Patient survival by Hsp70 membrane phenotype: association with different routes of metastasis. Cancer 2007;110:926-35.
15. Li H, Sui C, Kong F, Zhang H, Liu J, Dong M. Expression of HSP70 and JNK-related proteins in human liver cancer: potential effects on clinical outcome. Dig Liver Dis 2007;39:663-70.
16. Stangl S, Gehrmann M, Dressel R, Alves F, Dullin C, Themelis G, et al. In vivo imaging of CT26 mouse tumours by using cmHsp70.1monoclonal antibody. J Cell Mol Med 2011;15:874-87.
17. Stangl S, Gehrmann M, Riegger J, Kuhs K, Riederer I, Sievert W, et al. Targeting membrane heat-shock protein 70 (Hsp70) on tumors by cmHsp70.1 antibody. Proc Natl Acad Sci U S A 2011;108:733-8.
18. Gehrmann M, Foulds GA, Breuninger S, Stangl S, Pockley AG, Multhoff G. Tumor imaging and targeting potential of an Hsp70-derived 14-mer peptide. PLoS ONE 2014;28:9e105344.
19. Mahalka AK, Kirkegaard T, Jukolal, J€a€attel €a M, Kinnunen PHJ. Human heat shock protein 70 (Hsp70) as a peripheral membrane protein. Biochim Biophys Acta 2014;1838:1344-61.
20. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004;118:285-96.
21. Ardito CM, Gruner BM, Takeuchi KK, Lubeseder-Martellato C, Teichmann N, Mazur PK, et al. EGF receptor is required for KRAS-induced pancreatic tumorigenesis. Can Cell 2012;22:304-17.
22. Themelis G, Harlaar NJ, Kelder W, Bart J, Sarantopoulos A, van Dam GM, et al. Enhancing surgical vision by using real-time imaging of alphaVbeta3-integrin targeted near-infrared fluorescent agent. Ann Surg Oncol 2011;18:3506-13.
23. Hosotani R, Kawaguchi M, Masui T, Koshiba T, Ida J, Fujimoto K, et al. Expression of integrin alphaVbeta3 in pancreatic carcinoma: relation to MMP-2 activation and lymph node metastasis. Pancreas 2002;25: e30-5.
24. Cardoso F, Saghatchian M, Thompson A, Rutgers ECommittee TCS. Inconsistent criteria used in American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol 2008;26:2058-9.
25. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM, et al. REporting recommendations for tumor MARKer prognostic studies (REMARK). Nat Clin Pract Oncol 2005;2:416-22.
26. Schilsky RL, Taube SE. Tumor markers as clinical cancer tests - are we there yet? Semin Oncol 2002;29:211-2.
27. Barrott JJ, Hughes PF, Osda T, Yang XY, Hartman ZC, Loiselle DR, et al. Optical and radioiodinated tethered Hsp90 inhibitors reveal selective internalization of ectotpic Hsp90 in malignant breast tumor cells. Chem Biol 2013;20:1187-97.
28. He T, Xue Z, Lu K, Valdivia Y, Alvarado M, Wong KK, et al. A minimally invasive multimodality image-guided (MIMG) system for peripheral lung cancer intervention and diagnosis. Comput Med Imaging Graph 2012;36:345-55.
29. Valvidia Y, Alvarado M, Wong K, He TC, Xue Z, Wong ST. Imageguided fiberoptic molecular imaging in a VX2 rabbit lung tumor model. J Vasc Interv Radiol 2011;22:1758-64.
30. Trajkovic-Arsic M, Mohajerani P, Sarantopoulos A, Kalideris E, Steiger K, Esposito I, et al.Multimodal molecular imaging of integrin avb3 for in vivo detection of pancreatic cancer. J Nucl Med 2014; 55:446-51.
31. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010; 10:9-22.
32. Brooks PC, Clark RA, Cheresh DA. Requirement of vascular integrin alphaVbeta3 for angiogenesis. Science 1994;264:569-71.
33. Ruegg C, Yilmaz A, Bieler G, Bamat J, Chaubert P, Lejeune FJ. Evidence for the involvement of endothelial cell integrin alphaVbeta3 in the disruption of the tumor vasculature induced by TNF and IFNgamma. Nat Med 1998;4:408-14.
34. Gehrmann M, Stangl S, Kirschner A, Foulds GA, Sievert W, Doss BT, et al. Immunotherapeutic targeting of membrane Hsp70-expressing tumors using recombinant human granzyme B. PLoS ONE 2012;7: e41341.
35. Burger M, Glodek A, Hartmann T, Schmitt-Graff A, Silberstein LE, Fujii N, et al. Functional expression of CXCR4 (CD184) on small-cell lung cancer cells mediates migration, integrin activation, and adhesion to stromal cells. Oncogene 2003;22:8093-101.
36. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006;107: 1761-67.
37. Liles WC, Broxmeyer HE, Rodger E, Wood B, Hubel K, Cooper S, et al. Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 2003;102:2728-30.