Molecular imaging of breast tumors using a near-infrared fluorescently labeled clusterin binding peptide

International Journal of Cancer

Volumn 131, Issue 5, 2012, Pages

  Filfil, Rana ^a,b   Paul Roc, Béatrice ^a   Cantin, Christiane ^a   Iqbal, Umar ^a   Tolkatchev, Dmitri ^a   Vinogradova, Anna ^a   Xu, Ping ^a   Ni, Feng ^a   O'Connor McCourt, Maureen D ^a   Lenferink, Anne E G ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b HEALTH CANADA   (Canada)

Author keywords

4T1; Binding peptide; Breast cancer; Secreted clusterin; Time domain near infrared fluorescence imaging

Indexed keywords

ALEXA FLUOR 680 LABELED PEPTIDE P3378; ALEXA FLUOR 680 LABELED PEPTIDE P3378R; BINDING PROTEIN; CLUSTERIN; CLUSTERIN BINDING PEPTIDE; DYLIGHT 680 LABELED PEPTIDE P3378; DYLIGHT 680 LABELED PEPTIDE P3378R; DYLIGHT 800 LABELED PEPTIDE P3378; DYLIGHT 800 LABELED PEPTIDE P3378R; FLUORESCENT DYE; NEAR INFRARED FLUOROPHORE; PEPTIDE; SECRETED CLUSTERIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BREAST TUMOR; CONTROLLED STUDY; DIFFERENTIAL RESONANCE PERTURBATION NUCLEAR MAGNETIC RESONANCE; EX VIVO STUDY; FEMALE; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR IMAGING; MOUSE; NEAR INFRARED FLUORESCENCE IMAGING; NEAR INFRARED SPECTROSCOPY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TISSUE SPECIFICITY; TUMOR LOCALIZATION; VALIDATION PROCESS;

ANIMALS; BLOTTING, WESTERN; CLUSTERIN; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MOLECULAR IMAGING; MOLECULAR PROBES; PEPTIDE FRAGMENTS; PEPTIDE LIBRARY; SPECTROSCOPY, NEAR-INFRARED; TUMOR CELLS, CULTURED;

EID: 84863187435     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27368     Document Type: Article

References (49)

1. Fritz IB, Burdzy K, Setchell B, Blaschuk O. Ram rete testis fluid contains a protein (clusterin) which influences cell-cell interactions in vitro. Biol Reprod 1983;28:1173-88. (Pubitemid 13037974)
2. de Silva HV, Stuart WD, Park YB, Mao SJ, Gil CM, Wetterau JR, Busch SJ, Harmony JA. Purification and characterization of apolipoprotein J. J Biol Chem 1990;265:14292-7.
3. Choi NH, Mazda T, Tomita M. A serum protein SP40,40 modulates the formation of membrane attack complex of complement on erythrocytes. Mol Immunol 1989;26:835-40. (Pubitemid 19249460)
4. James RW, Hochstrasser AC, Borghini I, Martin B, Pometta D, Hochstrasser D. Characterization of a human high density lipoprotein-associated protein, NA1/NA2. Identity with SP-40,40, an inhibitor of complement-mediated cytolysis. Arterioscler Thromb 1991;11:645-52.
5. Shannan B, Seifert M, Leskov K, Willis J, Boothman D, Tilgen W, Reichrath J. Challenge and promise: roles for clusterin in pathogenesis, progression and therapy of cancer. Cell Death Differ 2006;13:12-9.
6. Trougakos IP, Gonos ES. Clusterin/apolipoprotein J in human aging and cancer. Int J Biochem Cell Biol 2002;34:1430-48. (Pubitemid 35245400)
7. Schepeler T, Mansilla F, Christensen LL, Orntoft TF, Andersen CL. Clusterin expression can be modulated by changes in TCF1-mediated Wnt signaling. J Mol Signal 2007;2:6.
8. Andersen CL, Schepeler T, Thorsen K, Birkenkamp-Demtroder K, Mansilla F, Aaltonen LA, Laurberg S, Orntoft TF. Clusterin expression in normal mucosa and colorectal cancer. Mol Cell Proteomics 2007;6:1039-48. (Pubitemid 47019405)
9. Leskov KS, Klokov DY, Li J, Kinsella TJ, Boothman DA. Synthesis and functional analyses of nuclear clusterin, a cell death protein. J Biol Chem 2003;278:11590-600. (Pubitemid 36792721)
10. Bettuzzi S, Rizzi F. Chapter 5: nuclear CLU (nCLU) and the fate of the cell. Adv Cancer Res 2009;104:59-88.
11. Djeu JY, Wei S. Clusterin and chemoresistance. Adv Cancer Res 2009;105:77-92.
12. Wei L, Xue T, Wang J, Chen B, Lei Y, Huang Y, Wang H, Xin X. Roles of clusterin in progression, chemoresistance and metastasis of human ovarian cancer. Int J Cancer 2009;125:791-806.
13. Redondo M, Tellez T, Roldan MJ. The role of clusterin (CLU) in malignant transformation and drug resistance in breast carcinomas. Adv Cancer Res 2009;105:21-43.
14. Chia S, Dent S, Ellard S, Ellis PM, Vandenberg T, Gelmon K, Powers J, Walsh W, Seymour L, Eisenhauer EA. Phase II trial of OGX-011 in combination with docetaxel in metastatic breast cancer. Clin Cancer Res 2009;15:708-13.
15. Muramaki M, So A, Hayashi N, Sowery R, Miyake H, Fujisawa M, Gleave ME. Chemosensitization of gemcitabine-resistant human bladder cancer cell line both in vitro and in vivo using antisense oligonucleotide targeting the anti-apoptotic gene, clusterin. BJU Int 2009;103:384-90.
16. Chi KN, Siu LL, Hirte H, Hotte SJ, Knox J, Kollmansberger C, Gleave M, Guns E, Powers J, Walsh W, Tu D, Eisenhauer E. A phase I study of OGX-011, a 20-methoxyethyl phosphorothioate antisense to clusterin, in combination with docetaxel in patients with advanced cancer. Clin Cancer Res 2008;14:833-9. (Pubitemid 351231167)
17. Kuk C, Kulasingam V, Gunawardana CG, Smith CR, Batruch I, Diamandis EP. Mining the ovarian cancer ascites proteome for potential ovarian cancer biomarkers. Mol Cell Proteomics 2009;8:661-9.
18. Bijian K, Mlynarek AM, Balys RL, Jie S, Xu Y, Hier MP, Black MJ, Di Falco MR, LaBoissiere S, Alaoui-Jamali MA. Serum proteomic approach for the identification of serum biomarkers contributed by oral squamous cell carcinoma and host tissue microenvironment. J Proteome Res 2009;8:2173-85.
19. Doustjalali SR, Yusof R, Yip CH, Looi LM, Pillay B, Hashim OH. Aberrant expression of acute-phase reactant proteins in sera and breast lesions of patients with malignant and benign breast tumors. Electrophoresis 2004;25:2392-401. (Pubitemid 39136360)
20. Bi J, Guo AL, Lai YR, Li B, Zhong JM, Wu HQ, Xie Z, He YL, Lv ZL, Lau SH, Wang Q, Huang XH, et al. Overexpression of clusterin correlates with tumor progression, metastasis in gastric cancer: a study on tissue microarrays. Neoplasma 2010;57:191-7.
21. Lenferink AE, Cantin C, Nantel A, Wang E, Durocher Y, Banville M, Paul-Roc B, Marcil A, Wilson MR, O'Connor-McCourt MD. Transcriptome profiling of a TGF-beta-induced epithelial-to-mesenchymal transition reveals extracellular clusterin as a target for therapeutic antibodies. Oncogene 2010;29:831-44.
22. Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED, Thompson EW. Epithelial-mesenchymal and mesenchymalepithelial transitions in carcinoma progression. J Cell Physiol 2007;213:374-83. (Pubitemid 47509716)
23. Iqbal U, Albaghdadi H, Luo Y, Arbabi M, Desvaux C, Veres T, Stanimirovic D, Abulrob A. Molecular imaging of glioblastoma multiforme using anti-insulin-like growth factor-binding protein-7 single-domain antibodies. Br J Cancer 2010;103:1606-16.
24. Bell A, Wang ZJ, Arbabi-Ghahroudi M, Chang TA, Durocher Y, Trojahn U, Baardsnes J, Jaramillo ML, Li S, Baral TN, O'Connor-McCourt M, Mackenzie R, et al. Differential tumor-targeting abilities of three single-domain antibody formats. Cancer Lett 2010;289:81-90.
25. Kossodo S, Pickarski M, Lin SA, Gleason A, Gaspar R, Buono C, Ho G, Blusztajn A, Cuneo G, Zhang J, Jensen J, Hargreaves R, et al. Dual In Vivo Quantification of Integrin-targeted and Protease-activated Agents in Cancer Using Fluorescence Molecular Tomography (FMT). Mol Imaging Biol 2010;12:488-99.
26. Wang K, Li W, Huang T, Li R, Wang D, Shen B, Chen X. Characterizing Breast Cancer Xenograft Epidermal Growth Factor Receptor Expression by Using Near-Infrared Optical Imaging. Acta Radiol 2009;50:1095-103.
27. Schmidt MM, Wittrup KD. A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol Cancer Ther 2009;8:2861-71.
28. Becker A, Hessenius C, Licha K, Ebert B, Sukowski U, Semmler W, Wiedenmann B, Grotzinger C. Receptor-targeted optical imaging of tumors with near-infrared fluorescent ligands. Nat Biotechnol 2001;19:327-31. (Pubitemid 32275340)
29. Mahmood U, Tung CH, Bogdanov A, Jr., Weissleder R. Near-infrared optical imaging of protease activity for tumor detection. Radiology 1999;213:866-70.
30. Peng L, Liu R, Andrei M, Xiao W, Lam KS. In vivo optical imaging of human lymphoma xenograft using a library-derived peptidomimetic against alpha4beta1 integrin. Mol Cancer Ther 2008;7:432-7. (Pubitemid 351302537)
31. Weissleder R, Tung CH, Mahmood U, Bogdanov A, Jr. In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nat Biotechnol 1999;17:375-8. (Pubitemid 29166041)
32. Xiao W, Yao N, Peng L, Liu R, Lam KS. Near-infrared optical imaging in glioblastoma xenograft with ligand-targeting alpha 3 integrin. Eur J Nucl Med Mol Imaging 2009;36:94-103.
33. Cheng Z, Wu Y, Xiong Z, Gambhir SS, Chen X. Near-infrared fluorescent RGD peptides for optical imaging of integrin alphavbeta3 expression in living mice. Bioconjug Chem 2005;16:1433-41. (Pubitemid 41681509)
34. Willmann JK, van Bruggen N, Dinkelborg LM, Gambhir SS. Molecular imaging in drug development. Nat Rev Drug Discov 2008;7:591-607. (Pubitemid 351927724)
35. Bloch S, Lesage F, McIntosh L, Gandjbakhche A, Liang K, Achilefu S. Whole-body fluorescence lifetime imaging of a tumor-targeted near-infrared molecular probe in mice. J Biomed Opt 2005;10:054003.
36. Napp J, Mathejczyk JE, Alves F. Optical imaging in vivo with a focus on paediatric disease: technical progress, current preclinical and clinical applications and future perspectives. Pediatr Radiol 2011;41:161-75.
37. Napp J, Dullin C, Muller F, Uhland K, Petri JB, van de Locht A, Steinmetzer T, Alves F. Timedomain in vivo near infrared fluorescence imaging for evaluation of matriptase as a potential target for the development of novel, inhibitor-based tumor therapies. Int J Cancer 2010;127:1958-74.
38. Keren S, Gheysens O, Levin CS, Gambhir SS. A comparison between a time domain and continuous wave small animal optical imaging system. IEEE Trans Med Imaging 2008;27:58-63.
39. McCormack E, Micklem DR, Pindard LE, Silden E, Gallant P, Belenkov A, Lorens JB, Gjertsen BT. In vivo optical imaging of acute myeloid leukemia by green fluorescent protein: timedomain autofluorescence decoupling, fluorophore quantification, and localization. Mol Imaging 2007;6:193-204. (Pubitemid 47152706)
40. Durocher Y, Perret S, Kamen A. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res 2002;30:E9.
41. Su Z, Vinogradova A, Koutychenko A, Tolkatchev D, Ni F. Rational design and selection of bivalent peptide ligands of thrombin incorporating P4-P1 tetrapeptide sequences: from good substrates to potent inhibitors. Protein Eng Des Sel 2004;17:647-57. (Pubitemid 39665401)
42. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 2003;31:3784-8. (Pubitemid 37442246)
43. Feher VA, Zapf JW, Hoch JA, Dahlquist FW, Whiteley JM, Cavanagh J. 1H, 15N, and 13C backbone chemical shift assignments, secondary structure, and magnesium-binding characteristics of the Bacillus subtilis response regulator, Spo0F, determined by heteronuclear high-resolution NMR. Protein Sci 1995;4:1801-14.
44. Weissleder R, Ntziachristos V. Shedding light onto live molecular targets. Nat Med 2003;9:123-8. (Pubitemid 36098273)
45. Gordon MS, Mendelson DS, Kato G. Tumor angiogenesis and novel antiangiogenic strategies. Int J Cancer 2010;126:1777-87.
46. Ribatti D, Nico B, Crivellato E, Vacca A. The structure of the vascular network of tumors. Cancer Lett 2007;248:18-23.
47. Ma G, Gallant P, McIntosh L. Sensitivity characterization of a time-domain fluorescence imager: eXplore Optix. Appl Opt 2007;46:1650-7. (Pubitemid 46659531)
48. Hochgrebe TT, Humphreys D, Wilson MR, Easterbrook-Smith SB. A reexamination of the role of clusterin as a complement regulator. Exp Cell Res 1999;249:13-21. (Pubitemid 29394020)
49. Cardone RA, Casavola V, Reshkin SJ. The role of disturbed pH dynamics and the Na+/H+exchanger in metastasis. Nat Rev Cancer 2005;5:786-95. (Pubitemid 41400778)