γ-tilmanocept, a new radiopharmaceutical tracer for cancer sentinel lymph nodes, binds to the mannose receptor (CD206)

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 2019-2029

  Azad, Abul K ^a   Rajaram, Murugesan V S ^a   Metz, Wendy L ^b   Cope, Frederick O ^b   Blue, Michael S ^b   Vera, David R ^c   Schlesinger, Larry S ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Biomedical Research Tower ^*  (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CY 3 TILMANOCEPT TC 99M; MANNAN; MANNOSE RECEPTOR; SMALL INTERFERING RNA; TRACER; UNCLASSIFIED DRUG; CARBOCYANINE; CELL SURFACE RECEPTOR; CYANINE DYE 3; DEXTRAN; LECTIN; MANNOSE BINDING LECTIN; PENTETATE TECHNETIUM TC 99M; PROTEIN BINDING; RADIOPHARMACEUTICAL AGENT; TECHNETIUM-DIETHYLENETRIAMINEPENTAACETIC ACID-MANNOSYL-DEXTRAN;

ARTICLE; BINDING AFFINITY; CELL MEMBRANE; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; DRUG BINDING; HUMAN; HUMAN CELL; HUMAN TISSUE; ISOTOPE LABELING; LYMPH VESSEL ENDOTHELIUM; MACROPHAGE; MICROENVIRONMENT; PRIORITY JOURNAL; SENTINEL LYMPH NODE; ANALOGS AND DERIVATIVES; CELL CULTURE; CHEMICAL STRUCTURE; CHEMISTRY; FLOW CYTOMETRY; GENETICS; HEK293 CELL LINE; IMMUNOHISTOCHEMISTRY; LYMPH NODE; METABOLISM; NEOPLASMS; PROCEDURES; RNA INTERFERENCE; SENTINEL LYMPH NODE BIOPSY;

CARBOCYANINES; CELLS, CULTURED; DEXTRANS; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; LECTINS, C-TYPE; LYMPH NODES; MACROPHAGES; MANNANS; MANNOSE-BINDING LECTINS; MICROSCOPY, CONFOCAL; MOLECULAR STRUCTURE; NEOPLASMS; PROTEIN BINDING; RADIOPHARMACEUTICALS; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SENTINEL LYMPH NODE BIOPSY; TECHNETIUM TC 99M PENTETATE;

EID: 84940112134     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402005     Document Type: Article

References (74)

1. Vera, D. R., A. M. Wallace, and C. K. Hoh. 2001. [(99m)Tc]MAG(3)-mannosyldextran: a receptor-binding radiopharmaceutical for sentinel node detection. Nucl. Med. Biol. 28: 493-498.
2. Hoh, C. K., A. M. Wallace, and D. R. Vera. 2003. Preclinical studies of [(99m)Tc]DTPA-mannosyl-dextran. Nucl. Med. Biol. 30: 457-464.
3. Coughlin, A., and V. A. Resto. 2010. Oral cavity squamous cell carcinoma and the clinically n0 neck: the past, present, and future of sentinel lymph node biopsy. Curr. Oncol. Rep. 12: 129-135.
4. Vera, D. R., A. M. Wallace, C. K. Hoh, and R. F. Mattrey. 2001. A synthetic macromolecule for sentinel node detection: (99m)Tc-DTPA-mannosyl-dextran. J. Nucl. Med. 42: 951-959.
5. Méndez, J., A. M. Wallace, C. K. Hoh, and D. R. Vera. 2003. Detection of gastric and colonic sentinel nodes through endoscopic administration of 99mTc-DTPAmannosyl-dextran in pigs. J. Nucl. Med. 44: 1677-1681.
6. Wallace, A. M., S. J. Ellner, J. Méndez, C. K. Hoh, C. E. Salem, C. M. Bosch, R. C. Orahood, and D. R. Vera. 2006. Minimally invasive sentinel lymph node mapping of the pig colon with Lymphoseek. Surgery 139: 217-223.
7. Ellner, S. J., J. Méndez, D. R. Vera, C. K. Hoh, W. L. Ashburn, and A. M. Wallace. 2004. Sentinel lymph node mapping of the colon and stomach using lymphoseek in a pig model. Ann. Surg. Oncol. 11: 674-681.
8. Salem, C. E., C. K. Hoh, A. M. Wallace, and D. R. Vera. 2006. A preclinical study of prostate sentinel lymph node mapping with [99mTC]diethylenetetramine pentaacetic acid-mannosyl-dextran. J. Urol. 175: 744-748.
9. Wallace, A. M., C. K. Hoh, S. J. Ellner, D. D. Darrah, G. Schulteis, and D. R. Vera. 2007. Lymphoseek: a molecular imaging agent for melanoma sentinel lymph node mapping. Ann. Surg. Oncol. 14: 913-921.
10. Leong, S. P., J. Kim, M. Ross, M. Faries, C. R. Scoggins, W. L. Metz, F. O. Cope, and R. C. Orahood. 2011. A phase 2 study of (99m)Tc-tilmanocept in the detection of sentinel lymph nodes in melanoma and breast cancer. Ann. Surg. Oncol. 18: 961-969.
11. Ellner, S. J., C. K. Hoh, D. R. Vera, D. D. Darrah, G. Schulteis, and A. M. Wallace. 2003. Dose-dependent biodistribution of [(99m)Tc]DTPA-mannosyl-dextran for breast cancer sentinel lymph node mapping. Nucl. Med. Biol. 30: 805-810.
12. Wallace, A. M., C. K. Hoh, D. R. Vera, D. D. Darrah, and G. Schulteis. 2003. Lymphoseek: a molecular radiopharmaceutical for sentinel node detection. Ann. Surg. Oncol. 10: 531-538.
13. Wallace, A. M., C. K. Hoh, K. K. Limmer, D. D. Darrah, G. Schulteis, and D. R. Vera. 2009. Sentinel lymph node accumulation of Lymphoseek and Tc-99m-sulfur colloid using a "2-day" protocol. Nucl. Med. Biol. 36: 687-692.
14. Gordon, S. 2002. Pattern recognition receptors: doubling up for the innate immune response. Cell 111: 927-930.
15. Taylor, P. R., L. Martinez-Pomares, M. Stacey, H. H. Lin, G. D. Brown, and S. Gordon. 2005. Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23: 901-944.
16. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
17. Torrelles, J. B., A. K. Azad, L. N. Henning, T. K. Carlson, and L. S. Schlesinger. 2008. Role of C-type lectins in mycobacterial infections. Curr. Drug Targets 9: 102-112.
18. Stahl, P., P. H. Schlesinger, E. Sigardson, J. S. Rodman, and Y. C. Lee. 1980. Receptor-mediated pinocytosis of mannose glycoconjugates by macrophages: characterization and evidence for receptor recycling. Cell 19: 207-215.
19. Schlesinger, L. S. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J. Immunol. 150: 2920-2930.
20. Kang, P. B., A. K. Azad, J. B. Torrelles, T. M. Kaufman, A. Beharka, E. Tibesar, L. E. DesJardin, and L. S. Schlesinger. 2005. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J. Exp. Med. 202: 987-999.
21. Miller, J. L., B. J. de Wet, L. Martinez-Pomares, C. M. Radcliffe, R. A. Dwek, P. M. Rudd, and S. Gordon. 2008. The mannose receptor mediates dengue virus infection of macrophages. [Published erratum appears in 2008 PLoS Pathog. 4: 10.] PLoS Pathog. 4: e17.
22. Taylor, P. R., S. Gordon, and L. Martinez-Pomares. 2005. The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol. 26: 104-110.
23. Lee, S. J., S. Evers, D. Roeder, A. F. Parlow, J. Risteli, L. Risteli, Y. C. Lee, T. Feizi, H. Langen, and M. C. Nussenzweig. 2002. Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science 295: 1898-1901.
24. Mantovani, A., B. Bottazzi, F. Colotta, S. Sozzani, and L. Ruco. 1992. The origin and function of tumor-associated macrophages. Immunol. Today 13: 265-270.
25. Balkwill, F., and A. Mantovani. 2001. Inflammation and cancer: back to Virchow? Lancet 357: 539-545.
26. Luo, Y., H. Zhou, J. Krueger, C. Kaplan, S. H. Lee, C. Dolman, D. Markowitz, W. Wu, C. Liu, R. A. Reisfeld, and R. Xiang. 2006. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J. Clin. Invest. 116: 2132-2141.
27. Mantovani, A., S. Sozzani, M. Locati, P. Allavena, and A. Sica. 2002. Macro-phage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23: 549-555.
28. Mills, C. D., K. Kincaid, J. M. Alt, M. J. Heilman, and A. M. Hill. 2000. M-1/M- 2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164: 6166-6173.
29. Rajaram, M. V., M. N. Brooks, J. D. Morris, J. B. Torrelles, A. K. Azad, and L. S. Schlesinger. 2010. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor gamma linking mannose receptor recognition to regulation of immune responses. J. Immunol. 185: 929-942.
30. Rajaram, M. V., B. Ni, J. D. Morris, M. N. Brooks, T. K. Carlson, B. Bakthavachalu, D. R. Schoenberg, J. B. Torrelles, and L. S. Schlesinger. 2011. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc. Natl. Acad. Sci. USA 108: 17408-17413.
31. Shi, S. R., M. E. Key, and K. L. Kalra. 1991. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39: 741-748.
32. Henning, L. N., A. K. Azad, K. V. Parsa, J. E. Crowther, S. Tridandapani, and L. S. Schlesinger. 2008. Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J. Immunol. 180: 7847-7858.
33. Gazi, U., and L. Martinez-Pomares. 2009. Influence of the mannose receptor in host immune responses. Immunobiology 214: 554-561.
34. Puig-Kröger, A., D. Serrano-Gómez, E. Caparrós, A. Domínguez-Soto, M. Relloso, M. Colmenares, L. Martínez-Muñoz, N. Longo, N. Sánchez-Sánchez, M. Rincon, et al. 2004. Regulated expression of the pathogen receptor dendritic cell-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin in THP-1 human leukemic cells, monocytes, and macrophages. J. Biol. Chem. 279: 25680-25688.
35. Shabo, I., and J. Svanvik. 2011. Expression of macrophage antigens by tumor cells. Adv. Exp. Med. Biol. 714: 141-150.
36. Allavena, P., M. Chieppa, G. Bianchi, G. Solinas, M. Fabbri, G. Laskarin, and A. Mantovani. 2010. Engagement of the mannose receptor by tumoral mucins activates an immune suppressive phenotype in human tumor-associated macrophages. Clin. Dev. Immunol. 2010: 547179.
37. Geijtenbeek, T. B., S. J. van Vliet, A. Engering, B. A. 't Hart, and Y. van Kooyk. 2004. Self- and nonself-recognition by C-type lectins on dendritic cells. Annu. Rev. Immunol. 22: 33-54.
38. Engering, A., T. B. Geijtenbeek, S. J. van Vliet, M. Wijers, E. van Liempt, N. Demaurex, A. Lanzavecchia, J. Fransen, C. G. Figdor, V. Piguet, and Y. van Kooyk. 2002. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J. Immunol. 168: 2118-2126.
39. Irjala, H., E. L. Johansson, R. Grenman, K. Alanen, M. Salmi, and S. Jalkanen. 2001. Mannose receptor is a novel ligand for L-selectin and mediates lymphocyte binding to lymphatic endothelium. J. Exp. Med. 194: 1033-1042.
40. Irjala, H., K. Alanen, R. Grénman, P. Heikkilä, H. Joensuu, and S. Jalkanen. 2003. Mannose receptor (MR) and common lymphatic endothelial and vascular endothelial receptor (CLEVER)-1 direct the binding of cancer cells to the lymph vessel endothelium. Cancer Res. 63: 4671-4676.
41. Petrova, T. V., T. Mäkinen, T. P. Mäkelä, J. Saarela, I. Virtanen, R. E. Ferrell, D. N. Finegold, D. Kerjaschki, S. Ylä-Herttuala, and K. Alitalo. 2002. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 21: 4593-4599.
42. Podgrabinska, S., P. Braun, P. Velasco, B. Kloos, M. S. Pepper, and M. Skobe. 2002. Molecular characterization of lymphatic endothelial cells. [Published erratum appears in 2003 Proc. Natl. Acad. Sci. U S A. 100: 4970.] Proc. Natl. Acad. Sci. USA 99: 16069-16074.
43. Wild, J., D. Robinson, and B. Winchester. 1983. Isolation of mannose-binding proteins from human and rat liver. Biochem. J. 210: 167-174.
44. Wileman, T., R. L. Boshans, P. Schlesinger, and P. Stahl. 1984. Monensin inhibits recycling of macrophage mannose-glycoprotein receptors and ligand delivery to lysosomes. Biochem. J. 220: 665-675.
45. Dave, S. S., K. Fu, G. W. Wright, L. T. Lam, P. Kluin, E. J. Boerma, T. C. Greiner, D. D. Weisenburger, A. Rosenwald, G. Ott, et al; Lymphoma/ Leukemia Molecular Profiling Project. 2006. Molecular diagnosis of Burkitt's lymphoma. N. Engl. J. Med. 354: 2431-2442.
46. Law, S. K. A., K. J. Micklem, J. M. Shaw, X.-P. Zhang, Y. Dong, A. C. Willis, and D. Y. Mason. 1993. A new macrophage differentiation antigen which is a member of the scavenger receptor superfamily. Eur. J. Immunol. 23: 2320-2325.
47. Lau, S. K., P. G. Chu, and L. M. Weiss. 2004. CD163: a specific marker of macrophages in paraffin-embedded tissue samples. Am. J. Clin. Pathol. 122: 794-801.
48. Jensen, T. O., H. Schmidt, H. J. Møller, M. Høyer, M. B. Maniecki, P. Sjoegren, I. J. Christensen, and T. Steiniche. 2009. Macrophage markers in serum and tumor have prognostic impact in American Joint Committee on Cancer stage I/II melanoma. J. Clin. Oncol. 27: 3330-3337.
49. Lee, C. H., I. Espinosa, S. Vrijaldenhoven, S. Subramanian, K. D. Montgomery, S. Zhu, R. J. Marinelli, J. L. Peterse, N. Poulin, T. O. Nielsen, et al. 2008. Prognostic significance of macrophage infiltration in leiomyosarcomas. Clin. Cancer Res. 14: 1423-1430.
50. Kamper, P., K. Bendix, S. Hamilton-Dutoit, B. Honoré, J. R. Nyengaard, and F. d'Amore. 2011. Tumor-infiltrating macrophages correlate with adverse prognosis and Epstein-Barr virus status in classical Hodgkin's lymphoma. Haematologica 96: 269-276.
51. Leek, R. D., C. E. Lewis, R. Whitehouse, M. Greenall, J. Clarke, and A. L. Harris. 1996. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 56: 4625-4629.
52. Shabo, I., O. Stål, H. Olsson, S. Doré, and J. Svanvik. 2008. Breast cancer expression of CD163, a macrophage scavenger receptor, is related to early distant recurrence and reduced patient survival. Int. J. Cancer 123: 780-786.
53. Kurahara, H., H. Shinchi, Y. Mataki, K. Maemura, H. Noma, F. Kubo, M. Sakoda, S. Ueno, S. Natsugoe, and S. Takao. 2011. Significance of M2- polarized tumor-associated macrophage in pancreatic cancer. J. Surg. Res. 167: e211-e219.
54. Farinha, P., A. Al-Tourah, K. Gill, R. Klasa, J. M. Connors, and R. D. Gascoyne. 2010. The architectural pattern of FOXP3-positive T cells in follicular lymphoma is an independent predictor of survival and histologic transformation. Blood 115: 289-295.
55. Banerji, S., J. Ni, S. X. Wang, S. Clasper, J. Su, R. Tammi, M. Jones, and D. G. Jackson. 1999. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 144: 789-801.
56. Skobe, M., T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar. 2001. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat. Med. 7: 192-198.
57. Beasley, N. J., R. Prevo, S. Banerji, R. D. Leek, J. Moore, P. van Trappen, G. Cox, A. L. Harris, and D. G. Jackson. 2002. Intratumoral lymphangiogenesis and lymph node metastasis in head and neck cancer. Cancer Res. 62: 1315-1320.
58. Mattila, M. M., J. K. Ruohola, T. Karpanen, D. G. Jackson, K. Alitalo, and P. L. Härkönen. 2002. VEGF-C induced lymphangiogenesis is associated with lymph node metastasis in orthotopic MCF-7 tumors. Int. J. Cancer 98: 946-951.
59. Maula, S. M., M. Luukkaa, R. Grénman, D. Jackson, S. Jalkanen, and R. Ristamäki. 2003. Intratumoral lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region. Cancer Res. 63: 1920-1926.
60. Marttila-Ichihara, F., R. Turja, M. Miiluniemi, M. Karikoski, M. Maksimow, J. Niemelä, L. Martinez-Pomares, M. Salmi, and S. Jalkanen. 2008. Macrophage mannose receptor on lymphatics controls cell trafficking. Blood 112: 64-72.
61. Salmi, M., M. Karikoski, K. Elima, P. Rantakari, and S. Jalkanen. 2013. CD44 binds to macrophage mannose receptor on lymphatic endothelium and supports lymphocyte migration via afferent lymphatics. Circ. Res. 112: 1577-1582.
62. Choi, Y. K., B. A. Fallert Junecko, C. R. Klamar, and T. A. Reinhart. 2013. Characterization of cells expressing lymphatic marker LYVE-1 in macaque large intestine during simian immunodeficiency virus infection identifies a large population of nonvascular LYVE-1(+)/DC-SIGN(+) cells. Lymphat. Res. Biol. 11: 26-34.
63. Wilting, J., M. Papoutsi, B. Christ, K. H. Nicolaides, C. S. von Kaisenberg, J. Borges, G. B. Stark, K. Alitalo, S. I. Tomarev, C. Niemeyer, and J. Rössler. 2002. The transcription factor Prox1 is a marker for lymphatic endothelial cells in normal and diseased human tissues. FASEB J. 16: 1271-1273.
64. Park, S. M., C. E. Angel, J. D. McIntosh, C. M. Mansell, C. J. Chen, J. Cebon, and P. R. Dunbar. 2014. Mapping the distinctive populations of lymphatic endothelial cells in different zones of human lymph nodes. [Published erratum appears in 2014 PLoS ONE 9: e94781.] PLoS One 9: e94781.
65. Vera, D. R., K. A. Krohn, R. C. Stadalnik, and P. O. Scheibe. 1984. Tc-99m galactosyl-neoglycoalbumin: in vitro characterization of receptor-mediated binding. J. Nucl. Med. 25: 779-787.
66. Vera, D. R., E. S. Woodle, and R. C. Stadalnik. 1989. Kinetic sensitivity of a receptor-binding radiopharmaceutical: technetium-99m galactosyl-neoglycoalbumin. J. Nucl. Med. 30: 1519-1530.
67. Hattori, Y., S. Kawakami, Y. Lu, K. Nakamura, F. Yamashita, and M. Hashida. 2006. Enhanced DNA vaccine potency by mannosylated lipoplex after intraperitoneal administration. J. Gene Med. 8: 824-834.
68. Lu, Y., S. Kawakami, F. Yamashita, and M. Hashida. 2007. Development of an antigen-presenting cell-targeted DNA vaccine against melanoma by mannosylated liposomes. Biomaterials 28: 3255-3262.
69. Kawakami, S., A. Sato, M. Nishikawa, F. Yamashita, and M. Hashida. 2000. Mannose receptor-mediated gene transfer into macrophages using novel mannosylated cationic liposomes. Gene Ther. 7: 292-299.
70. Azad, A. K., M. V. Rajaram, and L. S. Schlesinger. 2014. Exploitation of the Macrophage Mannose Receptor (CD206) in Infectious Disease Diagnostics and Therapeutics. J. Cytol. Mol. Biol. 1: 1.
71. Yu, S. S., C. M. Lau, W. J. Barham, H. M. Onishko, C. E. Nelson, H. Li, C. A. Smith, F. E. Yull, C. L. Duvall, and T. D. Giorgio. 2013. Macrophagespecific RNA interference targeting via "click", mannosylated polymeric micelles. Mol. Pharm. 10: 975-987.
72. Movahedi, K., S. Schoonooghe, D. Laoui, I. Houbracken, W. Waelput, K. Breckpot, L. Bouwens, T. Lahoutte, P. De Baetselier, G. Raes, et al. 2012. Nanobody-based targeting of the macrophage mannose receptor for effective in vivo imaging of tumor-associated macrophages. Cancer Res. 72: 4165-4177.
73. Locke, L. W., M. W. Mayo, A. D. Yoo, M. B. Williams, and S. S. Berr. 2012. PET imaging of tumor associated macrophages using mannose coated 64Cu liposomes. Biomaterials 33: 7785-7793.
74. Tahara, N., J. Mukherjee, H. J. de Haas, A. D. Petrov, A. Tawakol, N. Haider, A. Tahara, C. C. Constantinescu, J. Zhou, H. H. Boersma, et al. 2014. 2-deoxy-2- [18F]fluoro-D-mannose positron emission tomography imaging in atherosclerosis. Nat. Med. 20: 215-219.