Novel applications of nanobodies for in vivo bio-imaging of inflamed tissues in inflammatory diseases and cancer

Immunobiology

Volumn 217, Issue 12, 2012, Pages 1266-1272

  Schoonooghe, Steve ^a,b   Laoui, Damya ^a,b   Van Ginderachter, Jo A ^a,b   Devoogdt, Nick ^a   Lahoutte, Tony ^a,c   De Baetselier, Patrick ^a,b   Raes, Geert ^a,b  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

Cancer; Inflammation; Macrophage; Molecular imaging; Myeloid cell; Nanobody; SPECT

Indexed keywords

ANTIBODY; BIOLOGICAL MARKER; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FLUORINE 18; GALLIUM 68; MANNOSE RECEPTOR; NANOBODY; TECHNETIUM 99M; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; BONE MARROW CELL; BREAST CARCINOMA; CELL INFILTRATION; COLITIS; CYTOLOGY; ENDOTHELIUM; HUMAN; IN VIVO STUDY; INFECTION; INFLAMMATION; MACROPHAGE; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR BIOLOGY; MOLECULAR IMAGING; MOLECULAR PROBE; NON INVASIVE MEASUREMENT; NONHUMAN; PARASITOSIS; PATIENT MONITORING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TREATMENT RESPONSE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR VOLUME;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; INFLAMMATION; MOLECULAR IMAGING; MYELOID CELLS; NEOPLASMS; SINGLE-DOMAIN ANTIBODIES;

EID: 84869079676     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.07.009     Document Type: Article

References (56)

1. Aparici C.M., Carlson D., Nguyen N., Hawkins R.A., Seo Y. Combined SPECT and multidetector CT for prostate cancer evaluations. Am. J. Nucl. Med. Mol. Imaging 2012, 2:48-54.
2. Baral T.N., Magez S., Stijlemans B., Conrath K., Vanhollebeke B., Pays E., Muyldermans S., De Baetselier P. Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nat. Med. 2006, 12:580-584.
3. Bentzen S.M. Theragnostic imaging for radiation oncology: dose-painting by numbers. Lancet Oncol. 2005, 6:112-117.
4. Broisat A., Hernot S., Toczek J., De Vos J., Riou L.M., Martin S., Ahmadi M., Thielens N., Wernery U., Caveliers V., Muyldermans S., Lahoutte T., Fagret D., Ghezzi C., Devoogdt N. Nanobodies targeting mouse/human VCAM1 for the nuclear imaging of atherosclerotic lesions. Circ. Res. 2012, 110:927-937.
5. Chapman P.T., Jamar F., Keelan E.T., Peters A.M., Haskard D.O. Use of a radiolabeled monoclonal antibody against E-selectin for imaging of endothelial activation in rheumatoid arthritis. Arthritis Rheum. 1996, 39:1371-1375.
6. Coenen H.H., Elsinga P.H., Iwata R., Kilbourn M.R., Pillai M.R., Rajan M.G., Wagner H.N., Zaknun J.J. Fluorine-18 radiopharmaceuticals beyond [18F]FDG for use in oncology and neurosciences. Nucl. Med. Biol. 2010, 37:727-740.
7. Cortez-Retamozo V., Lauwereys M., Hassanzadeh Gh.G., Gobert M., Conrath K., Muyldermans S., De Baetselier P., Revets H. Efficient tumor targeting by single-domain antibody fragments of camels. Int. J. Cancer 2002, 98:456-462.
8. Cortez-Retamozo V., Backmann N., Senter P.D., Wernery U., De Baetselier P., Muyldermans S., Revets H. Efficient cancer therapy with a nanobody-based conjugate. Cancer Res. 2004, 64:2853-2857.
9. D'Huyvetter M., Aerts A., Xavier C., Vaneycken I., Devoogdt N., Gijs M., Impens N., Baatout S., Ponsard B., Muyldermans S., Caveliers V., Lahoutte T. Development of (177) Lu-nanobodies for radioimmunotherapy of HER2-positive breast cancer: evaluation of different bifunctional chelators. Contrast Media Mol. Imaging 2012, 7:254-264.
10. De Genst E., Silence K., Decanniere K., Conrath K., Loris R., Kinne J., Muyldermans S., Wyns L. Molecular basis for the preferential cleft recognition by dromedary heavy-chain antibodies. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4586-4591.
11. De Groeve K., Deschacht N., De Koninck C., Caveliers V., Lahoutte T., Devoogdt N., Muyldermans S., De Baetselier P., Raes G. Nanobodies as tools for in vivo imaging of specific immune cell types. J. Nucl. Med. 2010, 51:782-789.
12. De Rycke L., Baeten D., Foell D., Kruithof E., Veys E.M., Roth J., De Keyser F. Differential expression and response to anti-TNFalpha treatment of infiltrating versus resident tissue macrophage subsets in autoimmune arthritis. J. Pathol. 2005, 206:17-27.
13. Dijkers E.C., Oude Munnink T.H., Kosterink J.G., Brouwers A.H., Jager P.L., de Jong J.R., van Dongen G.A., Schroder C.P., Lub-de Hooge M.N., de Vries E.G. Biodistribution of 89Zr-trastuzumab and PET imaging of HER2-positive lesions in patients with metastatic breast cancer. Clin. Pharmacol. Ther. 2010, 87:586-592.
14. Dijkgraaf I., Boerman O.C. Radionuclide imaging of tumor angiogenesis. Cancer Biother. Radiopharm. 2009, 24:637-647.
15. Elsadek B., Kratz F. Impact of albumin on drug delivery-new applications on the horizon. J. Control. Release 2012, 157:4-28.
16. Fu W., Wojtkiewicz G., Weissleder R., Benoist C., Mathis D. Early window of diabetes determinism in NOD mice, dependent on the complement receptor CRIg, identified by noninvasive imaging. Nat. Immunol. 2012, 13:361-368.
17. Fuster V., Moreno P.R., Fayad Z.A., Corti R., Badimon J.J. Atherothrombosis and high-risk plaque. Part I. Evolving concepts. J. Am. Coll. Cardiol. 2005, 46:937-954.
18. Gainkam L.O., Caveliers V., Devoogdt N., Vanhove C., Xavier C., Boerman O., Muyldermans S., Bossuyt A., Lahoutte T. Localization, mechanism and reduction of renal retention of technetium-99m labeled epidermal growth factor receptor-specific nanobody in mice. Contrast Media Mol. Imaging 2011, 6:85-92.
19. Gainkam L.O., Keyaerts M., Caveliers V., Devoogdt N., Vanhove C., Van Grunsven L., Muyldermans S., Lahoutte T. Correlation between epidermal growth factor receptor-specific nanobody uptake and tumor burden: a tool for noninvasive monitoring of tumor response to therapy. Mol. Imaging Biol. 2011, 13:940-948.
20. Ghahroudi M.A., Desmyter A., Wyns L., Hamers R., Muyldermans S. Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett. 1997, 414:521-526.
21. Ghassabeh G.H., De Baetselier P., Brys L., Noel W., Van Ginderachter J.A., Meerschaut S., Beschin A., Brombacher F., Raes G. Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions. Blood 2006, 108:575-583.
22. Goyvaerts, C., De Groeve, K., Dingemans, J., Van Lint, S., Robays, L., Heirman, C., Reiser, J., Zhang, X.Y., Thielemans, K., De Baetselier, P., Raes, G., Breckpot, K. Development of the nanobody display technology to target lentiviral vectors to antigen-presenting cells. Gene Ther., , in press. doi:10.1038/gt.2011.206.
23. Hamers-Casterman C., Atarhouch T., Muyldermans S., Robinson G., Hamers C., Songa E.B., Bendahman N., Hamers R. Naturally occurring antibodies devoid of light chains. Nature 1993, 363:446-448.
24. Hernot S., Unnikrishnan S., Du Z., Shevchenko T., Cosyns B., Broisat A., Toczek J., Caveliers V., Muyldermans S., Lahoutte T., Klibanov A.L., Devoogdt N. Nanobody-coupled microbubbles as novel molecular tracer. J. Control. Release 2012, 158:346-353.
25. Hong H., Sun J., Cai W. Radionuclide-based cancer imaging targeting the carcinoembryonic antigen. Biomark Insights 2008, 3:435-451.
26. Huang L., Gainkam L.O., Caveliers V., Vanhove C., Keyaerts M., De Baetselier P., Bossuyt A., Revets H., Lahoutte T. SPECT imaging with 99mTc-labeled EGFR-specific nanobody for in vivo monitoring of EGFR expression. Mol. Imaging Biol. 2008, 10:167-175.
27. Hughes O.D., Bishop M.C., Perkins A.C., Wastie M.L., Denton G., Price M.R., Frier M., Denley H., Rutherford R., Schubiger P.A. Targeting superficial bladder cancer by the intravesical administration of copper-67-labeled anti-MUC1 mucin monoclonal antibody C595. J. Clin. Oncol. 2000, 18:363-370.
28. Kaur S., Venktaraman G., Jain M., Senapati S., Garg P.K., Batra S.K. Recent trends in antibody-based oncologic imaging. Cancer Lett. 2012, 315:97-111.
29. Keelan E.T., Harrison A.A., Chapman P.T., Binns R.M., Peters A.M., Haskard D.O. Imaging vascular endothelial activation: an approach using radiolabeled monoclonal antibodies against the endothelial cell adhesion molecule E-selectin. J. Nucl. Med. 1994, 35:276-281.
30. Kim R., Osaki A., Kojima J., Toge T. Significance of lymphoscintigraphic mapping with Tc-99m human serum albumin and tin colloid in sentinel lymph node biopsy in breast cancer. Int. J. Oncol. 2001, 19:991-996.
31. Kinne R.W., Becker W., Schwab J., Horneff G., Schwarz A., Kalden J.R., Emmrich F., Burmester G.R., Wolf F. Comparison of 99Tcm-labelled specific murine anti-CD4 monoclonal antibodies and nonspecific human immunoglobulin for imaging inflamed joints in rheumatoid arthritis. Nucl. Med. Commun. 1993, 14:667-675.
32. Laoui D., Movahedi K., Van Overmeire E., Van den Bossche J., Schouppe E., Mommer C., Nikolaou A., Morias Y., De Baetselier P., Van Ginderachter J.A. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int. J. Dev. Biol. 2011, 55:861-867.
33. Laoui D., Van Overmeire E., Movahedi K., Van den Bossche J., Schouppe E., Mommer C., Nikolaou A., Morias Y., De Baetselier P., Van Ginderachter J.A. Mononuclear phagocyte heterogeneity in cancer: different subsets and activation states reaching out at the tumor site. Immunobiology 2011, 216:1192-1202.
34. Locher J.T., Seybold K., Andres R.Y., Schubiger P.A., Mach J.P., Buchegger F. Imaging of inflammatory and infectious lesions after injection of radioiodinated monoclonal anti-granulocytes antibodies. Nucl. Med. Commun. 1986, 7:659-670.
35. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25:677-686.
36. Marcus C., Thakur M.L., Huynh T.V., Louie J.S., Leibling M., Minami C., Diggles L. Imaging rheumatic joint diseases with anti-T lymphocyte antibody OKT-3. Nucl. Med. Commun. 1994, 15:824-830.
37. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
38. Movahedi K., Laoui D., Gysemans C., Baeten M., Stange G., Van den Bossche J., Mack M., Pipeleers D., In't Veld P., De Baetselier P., Van Ginderachter J.A. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010, 70:5728-5739.
39. Movahedi, K., Schoonooghe, S., Laoui, D., Houbracken, I., Waelput, W., Breckpot, K., Bouwens, L., Lahoutte, T., De Baetselier, P., Raes, G., Devoogdt, N., Van Ginderachter, J.A., 2012. Nanobody-based targeting of the macrophage mannose receptor for effective in vivo imaging of tumor-associated macrophages. Cancer Res., , in press. doi:10.1158/0008-5472.CAN-11-2994.
40. Muyldermans S., Atarhouch T., Saldanha J., Barbosa J.A., Hamers R. Sequence and structure of VH domain from naturally occurring camel heavy chain immunoglobulins lacking light chains. Protein Eng. 1994, 7:1129-1135.
41. Oliveira S., van Dongen G.A., Stigter-van Walsum M., Roovers R.C., Stam J.C., Mali W., van Diest P.J., van Bergen En Henegouwen P.M. Rapid visulization of human tumor xenografts through optical imaging with a near-infrared fluorescent anti-epidermal growth factor receptor nanobody. Mol. Imaging 2012, 11:33-46.
42. Pysz M.A., Gambhir S.S., Willmann J.K. Molecular imaging: current status and emerging strategies. Clin. Radiol. 2010, 65:500-516.
43. Raes G., Brys L., Dahal B.K., Brandt J., Grooten J., Brombacher F., Vanham G., Noel W., Bogaert P., Boonefaes T., Kindt A., Van den Bergh R., Leenen P.J., De Baetselier P., Ghassabeh G.H. Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J. Leukoc. Biol. 2005, 77:321-327.
44. Raes G., Beschin A., Ghassabeh G.H., De Baetselier P. Alternatively activated macrophages in protozoan infections. Curr. Opin. Immunol. 2007, 19:454-459.
45. Sharkey R.M., Press O.W., Goldenberg D.M. A re-examination of radioimmunotherapy in the treatment of non-Hodgkin lymphoma: prospects for dual-targeted antibody/radioantibody therapy. Blood 2009, 113:3891-3895.
46. Signore A., Mather S.J., Piaggio G., Malviya G., Dierckx R.A. Molecular imaging of inflammation/infection: nuclear medicine and optical imaging agents and methods. Chem. Rev. 2010, 110:3112-3145.
47. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 1992, 176:287-292.
48. Stijlemans B., Conrath K., Cortez-Retamozo V., Van Xong H., Wyns L., Senter P., Revets H., De Baetselier P., Muyldermans S., Magez S. Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies, African trypanosomes as paradigm. J. Biol. Chem. 2004, 279:1256-1261.
49. Stijlemans B., Caljon G., Natesan S.K., Saerens D., Conrath K., Perez-Morga D., Skepper J.N., Nikolaou A., Brys L., Pays E., Magez S., Field M.C., De Baetselier P., Muyldermans S. High affinity nanobodies against the Trypanosome brucei VSG are potent trypanolytic agents that block endocytosis. PLoS Pathog. 2011, 7:e1002072.
50. Van den Bossche J., Bogaert P., van Hengel J., Guerin C.J., Berx G., Movahedi K., Van den Bergh R., Pereira-Fernandes A., Geuns J.M., Pircher H., Dorny P., Grooten J., De Baetselier P., Van Ginderachter J.A. Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/catenin complexes. Blood 2009, 114:4664-4674.
51. Vandenbroucke K., de Haard H., Beirnaert E., Dreier T., Lauwereys M., Huyck L., Van Huysse J., Demetter P., Steidler L., Remaut E., Cuvelier C., Rottiers P. Orally administered L. lactis secreting an anti-TNF nanobody demonstrate efficacy in chronic colitis. Mucosal Immunol. 2010, 3:49-56.
52. Vaneycken I., Govaert J., Vincke C., Caveliers V., Lahoutte T., De Baetselier P., Raes G., Bossuyt A., Muyldermans S., Devoogdt N. In vitro analysis and in vivo tumor targeting of a humanized, grafted nanobody in mice using pinhole SPECT/micro-CT. J. Nucl. Med. 2010, 51:1099-1106.
53. Vaneycken I., D'Huyvetter M., Hernot S., De Vos J., Xavier C., Devoogdt N., Caveliers V., Lahoutte T. Immuno-imaging using nanobodies. Curr. Opin. Biotechnol. 2011, 22:877-881.
54. Vaneycken I., Devoogdt N., Van Gassen N., Vincke C., Xavier C., Wernery U., Muyldermans S., Lahoutte T., Caveliers V. Preclinical screening of anti-HER2 nanobodies for molecular imaging of breast cancer. FASEB J. 2011, 25:2433-2446.
55. Vincke C., Loris R., Saerens D., Martinez-Rodriguez S., Muyldermans S., Conrath K. General strategy to humanize a camelid single-domain antibody and identification of a universal humanized nanobody scaffold. J. Biol. Chem. 2009, 284:3273-3284.
56. Vu K.B., Ghahroudi M.A., Wyns L., Muyldermans S. Comparison of llama VH sequences from conventional and heavy chain antibodies. Mol. Immunol. 1997, 34:1121-1131.