Nanobody-based cancer therapy of solid tumors

Nanomedicine

Volumn 10, Issue 1, 2015, Pages 161-174

  Kijanka, Marta ^a   Dorresteijn, Bram ^a   Oliveira, Sabrina ^a   Van Bergen En Henegouwen, Paul M P ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

cancer; delivery; nanobody; single domain antibody; therapy; VHH

Indexed keywords

MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; NANOPARTICLE; NANOBODY;

ANTIGEN BINDING; CANCER THERAPY; CELL PROLIFERATION; CIRCULATION TIME; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG TARGETING; EXTRAVASATION; HUMAN; IN VITRO STUDY; KIDNEY CLEARANCE; LIGHT CHAIN; LIVER CLEARANCE; MOLECULARLY TARGETED THERAPY; PHAGE DISPLAY; PRIORITY JOURNAL; RETICULOENDOTHELIAL SYSTEM; REVIEW; SOLID TUMOR; SURFACE PROPERTY; SYSTEMIC CIRCULATION; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASMS;

ANTIBODIES, MONOCLONAL; HUMANS; IMMUNOTHERAPY; MOLECULAR TARGETED THERAPY; NEOPLASMS; SINGLE-DOMAIN ANTIBODIES;

EID: 84921509883     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.14.178     Document Type: Review

References (97)

1. Oldham RK, Dillman RO. Monoclonal antibodies in cancer therapy: 25 years of progress. J. Clin. Oncol. 26(11), 1774-1777 (2008).
2. Oliveira S, Heukers R, Sornkom J, Kok RJ, van Bergen en Henegouwen PM. Targeting tumors with nanobodies for cancer imaging and therapy. J. Control. Release 172(3), 607-617 (2013).
3. Senter PD. Potent antibody drug conjugates for cancer therapy. Curr. Opin. Chem. Biol. 13(3), 235-244 (2009).
4. Sarma VR, Silverton EW, Davies DR, Terry WD. The three-dimensional structure at 6 A resolution of a human gamma Gl immunoglobulin molecule. J. Biol. Chem. 246(11), 3753-3759 (1971).
5. Siontorou CG. Nanobodies as novel agents for disease diagnosis and therapy. Int. J. Nanomedicine 8, 4215-4227 (2013).
6. Baker JH, Lindquist KE, Huxham LA, Kyle AH, Sy JT, Minchinton AI. Direct visualization of heterogeneous extravascular distribution of trastuzumab in human epidermal growth factor receptor type 2 overexpressing xenografts. Clin. Cancer Res. 14(7), 2171-2179 (2008).
7. Rudnick SI, Adams GP. Affinity and avidity in antibody-based tumor targeting. Cancer Biother. Radiopharm. 24(2), 155-161 (2009).
8. Bell A, Wang ZJ, Arbabi-Ghahroudi M et al. Differential tumor-targeting abilities of three single-domain antibody formats. Cancer Lett. 289(1), 81-90 (2010).
9. Hamers-Casterman C, Atarhouch T, Muyldermans S et al. Naturally occurring antibodies devoid of light chains. Nature 363(6428), 446-448 (1993).
10. Padlan EA. Anatomy of the antibody molecule. Mol. Immunol. 31(3), 169-217 (1994).
11. Muyldermans S. Nanobodies: natural single-domain antibodies. Annu. Rev. Biochem. 82, 775-797 (2013).
12. Oliveira S, van Dongen GA, Stigter-van Walsum M et al. Rapid visualization of human tumor xenografts through optical imaging with a near-infrared fluorescent anti-epidermal growth factor receptor Nanobody. Mol. Imaging 11(1), 33-46 (2012).
13. Dumoulin M, Conrath K, Van Meirhaeghe A et al. Single-domain antibody fragments with high conformational stability. Protein Sci. 11(3), 500-515 (2002).
14. van der Linden RH, Frenken LG, de Geus B et al. Comparison of physical chemical properties of llama VHH antibody fragments and mouse monoclonal antibodies. Biochim. Biophys. Acta 1431(1), 37-46 (1999).
15. Muyldermans S, Atarhouch T, Saldanha J, Barbosa JA, Hamers R. Sequence and structure of VH domain from naturally occurring camel heavy chain immunoglobulins lacking light chains. Protein Eng. 7(9), 1129-1135 (1994).
16. Ablynx homepage. www.ablynx.com
17. 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. 284(5), 3273-3284 (2009).
18. Kijanka M, Warnders FJ, El Khattabi M et al. Rapid optical imaging of human breast tumour xenografts using anti-HER2 VHHs site-directly conjugated to IRDye 800CW for image-guided surgery. Eur. J. Nucl. Med. Mol. Imaging 40(11), 1718-1729 (2013).
19. Vosjan MJ, Vercammen J, Kolkman JA, Stigter-van Walsum M, Revets H, van Dongen GA. Nanobodies targeting the hepatocyte growth factor: potential new drugs for molecular cancer therapy. Mol. Cancer Ther. 11(4), 1017-1025 (2012).
20. Roovers RC, Laeremans T, Huang L et al. Efficient inhibition of EGFR signaling and of tumour growth by antagonistic anti-EFGR nanobodies. Cancer Immunol. Immunother. 56(3), 303-317 (2007).
21. Pardon E, Laeremans T, Triest S et al. A general protocol for the generation of nanobodies for structural biology. Nat. Protoc. 9(3), 674-693 (2014).
22. Vaneycken I, Devoogdt N, Van Gassen N et al. Preclinical screening of anti-HER2 nanobodies for molecular imaging of breast cancer. FASEB J. 25(7), 2433-2446 (2011).
23. Van de Broek B, Devoogdt N, D'Hollander A et al. Specific cell targeting with Nanobody conjugated branched gold nanoparticles for photothermal therapy. ACS Nano 5(6), 4319-4328 (2011).
24. Holmes K, Roberts OL, Thomas AM, Cross MJ. Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell. Signal. 19(10), 2003-2012 (2007).
25. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling-in control of vascular function. Nat. Rev. Mol. Cell Biol. 7(5), 359-371 (2006).
26. Behdani M, Zeinali S, Khanahmad H et al. Generation and characterization of a functional Nanobody against the vascular endothelial growth factor receptor-2; angiogenesis cell receptor. Mol. Immunol. 50(1-2), 35-41 (2012).
27. Bottaro DP, Rubin JS, Faletto DL et al. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 251(4995), 802-804 (1991).
28. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat. Rev. Cancer 12(2), 89-103 (2012).
29. Schmidt Slordahl T, Denayer T, Helen Moen S et al. Anti-c-MET Nanobody® - a new potential drug in multiple myeloma treatment. Eur. J. Haematol. 91(5), 399-410 (2013).
30. Heukers R, Altintas I, Raghoenath S et al. Targeting hepatocyte growth factor receptor (Met) positive tumor cells using internalizing nanobody-decorated albumin nanoparticles. Biomaterials 35(1), 601-610 (2014).
31. Rajagopal S, Kim J, Ahn S et al. Beta-arrestin-but not G protein-mediated signaling by the 'decoy' receptor CXCR7. Proc. Natl Acad. Sci. USA 107(2), 628-632 (2010).
32. Miao Z, Luker KE, Summers BC et al. CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc. Natl Acad. Sci. USA 104(40), 15735-15740 (2007).
33. Sadeqzadeh E, Rahbarizadeh F, Ahmadvand D, Rasaee MJ, Parhamifar L, Moghimi SM. Combined MUC1-specific nanobody-tagged PEG-polyethylenimine polyplex targeting and transcriptional targeting of tBid transgene for directed killing of MUC1 over-expressing tumour cells. J. Control. Release 156(1), 85-91 (2011).
34. Cortez-Retamozo V, Backmann N, Senter PD et al. Efficient cancer therapy with a nanobody-based conjugate. Cancer Res. 64(8), 2853-2857 (2004).
35. Blanchetot C, Verzijl D, Mujic-Delic A et al. Neutralizing nanobodies targeting diverse chemokines effectively inhibit chemokine function. J. Biol. Chem. 288(35), 25173-25182 (2013).
36. Roovers RC, Vosjan MJ, Laeremans T et al. A biparatopic anti-EGFR nanobody efficiently inhibits solid tumour growth. Int. J. Cancer 129(8), 2013-2024 (2011).
37. Omidfar K, Amjad Zanjani FS, Hagh AG, Azizi MD, Rasouli SJ, Kashanian S. Efficient growth inhibition of EGFR over-expressing tumor cells by an anti-EGFR nanobody. Mol. Biol. Rep. 40(12), 6737-6745 (2013).
38. Talelli M, Rijcken CJ, Oliveira S et al. Nanobody-shell functionalized thermosensitive core-crosslinked polymeric micelles for active drug targeting. J. Control. Release 151(2), 183-192 (2011).
39. Oliveira S, Schiffelers RM, van der Veeken J et al. Downregulation of EGFR by a novel multivalent nanobody-liposome platform. J. Control. Release 145(2), 165-175 (2010).
40. van der Meel R, Oliveira S, Altintas I et al. Tumor-targeted Nanobullets: anti-EGFR nanobody-liposomes loaded with anti-IGF-1R kinase inhibitor for cancer treatment. J. Control. Release 159(2), 281-289 (2012).
41. Heukers R, van Bergen en Henegouwen PM, Oliveira S. Nanobody-photosensitizer conjugates for targeted photodynamic therapy. Nanomedicine 10(7), 1441-1451 (2014).
42. van der Meel R, Oliveira S, Altintas I et al. Inhibition of tumor growth by targeted anti-EGFR/IGF-1R nanobullets depends on efficient blocking of cell survival pathways. Mol. Pharm. 10(10), 3717-3727 (2013).
43. Talelli M, Oliveira S, Rijcken CJ et al. Intrinsically active nanobody-modified polymeric micelles for tumor-targeted combination therapy. Biomaterials 34(4), 1255-1260 (2013).
44. Altintas I, Heukers R, van der Meel R et al. Nanobody-albumin nanoparticles (NANAPs) for the delivery of a multikinase inhibitor 17864 to EGFR overexpressing tumor cells. J. Control. Release 165(2), 110-118 (2013).
45. D'Huyvetter M, Vincke C, Xavier C et al. Targeted radionuclide therapy with a 177Lu-labeled anti-HER2 nanobody. Theranostics 4(7), 708-720 (2014).
46. Behdani M, Zeinali S, Karimipour M et al. Development of VEGFR2-specific Nanobody Pseudomonas exotoxin A conjugated to provide efficient inhibition of tumor cell growth. N. Biotechnol. 30(2), 205-209 (2013).
47. Maussang D, Mujic-Delic A, Descamps FJ et al. Llama-derived single variable domains (nanobodies) directed against chemokine receptor CXCR7 reduce head and neck cancer cell growth in vivo. J. Biol. Chem. 288(41), 29562-29572 (2013).
48. Araste F, Ebrahimizadeh W, Rasooli I, Rajabibazl M, Mousavi Gargari SL. A novel VHH nanobody against the active site (the CA domain) of tumor-associated, carbonic anhydrase isoform IX and its usefulness for cancer diagnosis. Biotechnol. Lett. 36(1), 21-28 (2014).
49. Altintas I, Heukers R, van der Meel R et al. Nanobody-albumin nanoparticles (NANAPs) for the delivery of a multikinase inhibitor 17864 to EGFR overexpressing tumor cells. J. Control. Release 165(2), 110-118 (2013).
50. Bannas P, Well L, Lenz A et al. In vivo near-infrared fluorescence targeting of T cells: comparison of nanobodies and conventional monoclonal antibodies. Contrast Media Mol. Imaging 9(2), 135-142 (2014).
51. Heukers R, Vermeulen JF, Fereidouni F et al. Endocytosis of EGFR requires its kinase activity and N-terminal transmembrane dimerization motif. J. Cell. Sci. 126(Pt 21), 4900-4912 (2013).
52. Sapra P, Allen TM. Ligand-targeted liposomal anticancer drugs. Prog. Lipid Res. 42(5), 439-462 (2003).
53. Nichols JW, Bae YH. Odyssey of a cancer nanoparticle: from injection site to site of action. Nano Today 7(6), 606-618 (2012).
54. Hussack G, Hirama T, Ding W, Mackenzie R, Tanha J. Engineered single-domain antibodies with high protease resistance and thermal stability. PLoS ONE 6(11), e28218 (2011).
55. Longmire M, Choyke PL, Kobayashi H. Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. Nanomedicine (Lond.) 3(5), 703-717 (2008).
56. Vaneycken I, Govaert J, Vincke C et al. In vitro analysis and in vivo tumor targeting of a humanized, grafted nanobody in mice using pinhole SPECT/micro-CT. J. Nucl. Med. 51(7), 1099-1106 (2010).
57. Vegt E, Melis M, Eek A et al. Renal uptake of different radiolabelled peptides is mediated by megalin: SPECT and biodistribution studies in megalin-deficient mice. Eur. J. Nucl. Med. Mol. Imaging 38(4), 623-632 (2011).
58. Kobayashi H, Le N, Kim IS et al. The pharmacokinetic characteristics of glycolated humanized anti-Tac Fabs are determined by their isoelectric points. Cancer Res. 59(2), 422-430 (1999).
59. Choi HS, Liu W, Misra P et al. Renal clearance of quantum dots. Nat. Biotechnol. 25(10), 1165-1170 (2007).
60. Li T, Bourgeois JP, Celli S et al. Cell-penetrating anti-GFAP VHH and corresponding fluorescent fusion protein VHH-GFP spontaneously cross the blood-brain barrier and specifically recognize astrocytes: application to brain imaging. FASEB J. 26(10), 3969-3979 (2012).
61. Muyldermans S, Baral TN, Retamozzo VC et al. Camelid immunoglobulins and nanobody technology. Vet. Immunol. Immunopathol. 128(1-3), 178-183 (2009).
62. Cortez-Retamozo V, Lauwereys M, Hassanzadeh Gh G et al. Efficient tumor targeting by single-domain antibody fragments of camels. Int. J. Cancer 98(3), 456-462 (2002).
63. Gunther R, Chelstrom LM, Wendorf HR et al. Toxicity profile of the investigational new biotherapeutic agent, B43 (anti-CD19)-pokeweed antiviral protein immunotoxin. Leuk. Lymphoma 22(1-2), 61-70, follow.186, color plate II-V (1996).
64. Uckun FM, Yanishevski Y, Tumer N et al. Pharmacokinetic features, immunogenicity, and toxicity of B43(anti-CD19)-pokeweed antiviral protein immunotoxin in cynomolgus monkeys. Clin. Cancer Res. 3(3), 325-337 (1997).
65. Gainkam LO, Caveliers V, Devoogdt N et al. Localization, mechanism and reduction of renal retention of technetium-99m labeled epidermal growth factor receptor-specific nanobody in mice. Contrast Media Mol. Imaging 6(2), 85-92 (2011).
66. Huang L, Gainkam LO, Caveliers V et al. SPECT imaging with 99mTc-labeled EGFR-specific nanobody for in vivo monitoring of EGFR expression. Mol. Imaging Biol. 10(3), 167-175 (2008).
67. Gainkam LO, Huang L, Caveliers V et al. Comparison of the biodistribution and tumor targeting of two 99mTc-labeled anti-EGFR nanobodies in mice, using pinhole SPECT/micro-CT. J. Nucl. Med. 49(5), 788-795 (2008).
68. Tijink BM, Laeremans T, Budde M et al. Improved tumor targeting of anti-epidermal growth factor receptor Nanobodies through albumin binding: taking advantage of modular Nanobody technology. Mol. Cancer Ther. 7(8), 2288-2297 (2008).
69. Newkirk MM, Novick J, Stevenson MM, Fournier MJ, Apostolakos P. Differential clearance of glycoforms of IgG in normal and autoimmune-prone mice. Clin. Exp. Immunol. 106(2), 259-264 (1996).
70. Chapman AP, Antoniw P, Spitali M, West S, Stephens S, King DJ. Therapeutic antibody fragments with prolonged in vivo half-lives. Nat. Biotechnol. 17(8), 780-783 (1999).
71. Kuntz E. Hepatology: Principles and Practice; History, Morphology, Biochemistry, Diagnostics, Clinic, Therapy. Springer, Germany (2006).
72. Xie H, Svenmarker P, Axelsson J et al. Pharmacokinetic and biodistribution study following systemic administration of Fospeg® - a Pegylated liposomal mTHPC formulation in a murine model. J. Biophotonics doi:10.1002/jbio.201300133 (2013) (Epub ahead of print).
73. Gabizon A, Horowitz AT, Goren D, Tzemach D, Shmeeda H, Zalipsky S. In vivo fate of folate-targeted polyethylene-glycol liposomes in tumor-bearing mice. Clin. Cancer Res. 9(17), 6551-6559 (2003).
74. Lewanski CR, Stewart S. Pegylated liposomal adriamycin: a review of current and future applications. Pharm. Sci. Technol. Today 2(12), 473-477 (1999).
75. Mamot C, Drummond DC, Noble CO et al. Epidermal growth factor receptor-targeted immunoliposomes significantly enhance the efficacy of multiple anticancer drugs in vivo. Cancer Res. 65(24), 11631-11638 (2005).
76. Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7(11), 653-664 (2010).
77. Fujimori K, Covell DG, Fletcher JE, Weinstein JN. A modeling analysis of monoclonal antibody percolation through tumors: a binding-site barrier. J. Nucl. Med. 31(7), 1191-1198 (1990).
78. Li Y, Wang J, Wientjes MG, Au JL. Delivery of nanomedicines to extracellular and intracellular compartments of a solid tumor. Adv. Drug Deliv. Rev. 64(1), 29-39 (2012).
79. Sexton K, Tichauer K, Samkoe KS, Gunn J, Hoopes PJ, Pogue BW. Fluorescent affibody peptide penetration in glioma margin is superior to full antibody. PLoS ONE 8(4), e60390 (2013).
80. Matsumura Y, Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 46(12 Pt 1), 6387-6392 (1986).
81. Koh WW, Steffensen S, Gonzalez-Pajuelo M et al. Generation of a family-specific phage library of llama single chain antibody fragments that neutralize HIV-1. J. Biol. Chem. 285(25), 19116-19124 (2010).
82. Sukhanova A, Even-Desrumeaux K, Kisserli A et al. Oriented conjugates of single-domain antibodies and quantum dots: toward a new generation of ultrasmall diagnostic nanoprobes. Nanomedicine 8(4), 516-525 (2012).
83. Massa S, Xavier C, De Vos J et al. Site-specific labeling of cysteine-tagged camelid single-domain antibody-fragments for use in molecular imaging. Bioconjug. Chem. 25(5), 979-988 (2014).
84. Wood DW, Camarero JA. Intein applications: from protein purification and labeling to metabolic control methods. J. Biol. Chem. 289(21), 14512-14519 (2014).
85. Popp MW, Antos JM, Ploegh HL. Site-specific protein labeling via sortase-mediated transpeptidation. Curr. Protoc. Protein Sci. Chapter 15, Unit 15.3 (2009).
86. Mao H, Hart SA, Schink A, Pollok BA. Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc. 126(9), 2670-2671 (2004).
87. Proft T. Sortase-mediated protein ligation: an emerging biotechnology tool for protein modification and immobilisation. Biotechnol. Lett. 32(1), 1-10 (2010).
88. Moses JE, Moorhouse AD. The growing applications of click chemistry. Chem. Soc. Rev. 36(8), 1249-1262 (2007).
89. Spangler JB, Neil JR, Abramovitch S et al. Combination antibody treatment down-regulates epidermal growth factor receptor by inhibiting endosomal recycling. Proc. Natl Acad. Sci. USA 107(30), 13252-13257 (2010).
90. Mamot C, Drummond DC, Greiser U et al. Epidermal growth factor receptor (EGFR)-targeted immunoliposomes mediate specific and efficient drug delivery to EGFR-and EGFRvIII-overexpressing tumor cells. Cancer Res. 63(12), 3154-3161 (2003).
91. Mamot C, Ritschard R, Kung W, Park JW, Herrmann R, Rochlitz CF. EGFR-targeted immunoliposomes derived from the monoclonal antibody EMD72000 mediate specific and efficient drug delivery to a variety of colorectal cancer cells. J. Drug Target. 14(4), 215-223 (2006).
92. Prat M, Crepaldi T, Pennacchietti S, Bussolino F, Comoglio PM. Agonistic monoclonal antibodies against the Met receptor dissect the biological responses to HGF. J. Cell. Sci. 111(Pt 2), 237-247 (1998).
93. Defize LH, Moolenaar WH, van der Saag PT, de Laat SW. Dissociation of cellular responses to epidermal growth factor using anti-receptor monoclonal antibodies. EMBO J. 5(6), 1187-1192 (1986).
94. Talelli M, Iman M, Varkouhi AK et al. Core-crosslinked polymeric micelles with controlled release of covalently entrapped doxorubicin. Biomaterials 31(30), 7797-7804 (2010).
95. Lim EK, Jang E, Lee K, Haam S, Huh YM. Delivery of cancer therapeutics using nanotechnology. Pharmaceutics 5(2), 294-317 (2013).
96. van de Water JA, Bagci-Onder T, Agarwal AS et al. Therapeutic stem cells expressing variants of EGFR-specific nanobodies have antitumor effects. Proc. Natl Acad. Sci. USA 109(41), 16642-16647 (2012).
97. Hofman EG, Ruonala MO, Bader AN et al. EGF induces coalescence of different lipid rafts. J. Cell. Sci. 121(Pt 15), 2519-2528 (2008).