Clever-1/stabilin-1 controls cancer growth and metastasis

Clinical Cancer Research

Volumn 20, Issue 24, 2014, Pages 6452-6464

  Karikoski, Marika ^a   Marttila Ichihara, Fumiko ^a   Elima, Kati ^a,b   Rantakari, Pia ^a,c   Hollmén, Maija ^a   Kelkka, Tiina ^a   Gerke, Heidi ^a   Huovinen, Ville ^a   Irjala, Heikki ^a,d   Holmdahl, Rikard ^a   Salmi, Marko ^a,b,e   Jalkanen, Sirpa ^a,b,e  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c Institute of Biomedicine   (Finland)

^d TURKU UNIVERSITY HOSPITAL   (Finland)

^e NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COMMON LYMPHATIC ENDOTHELIAL AND VASCULAR ENDOTHELIAL RECEPTOR 1 ANTIBODY; COMMON LYMPHATIC ENDOTHELIAL AND VASCULAR ENDOTHELIAL RECEPTOR 1 PROTEIN; MONOCLONAL ANTIBODY; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; NERVE CELL ADHESION MOLECULE; OSTEONECTIN; SPARC PROTEIN, MOUSE; STAB1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CELL ADHESION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG TARGETING; HUMAN; HUMAN CELL; LYMPH NODE METASTASIS; LYMPHOMA; MELANOMA B16; METASTASIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE; TUMOR VASCULARIZATION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; AUTOIMMUNITY; CELL PROLIFERATION; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL MELANOMA; GENETICS; IMMUNITY; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; NEOPLASMS; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; RABBIT; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; TUMOR VOLUME;

ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; AUTOIMMUNITY; CELL ADHESION MOLECULES, NEURONAL; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNITY; LYMPHOCYTES, TUMOR-INFILTRATING; MACROPHAGES; MELANOMA, EXPERIMENTAL; MICE; MICE, KNOCKOUT; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OSTEONECTIN; RABBITS; TUMOR BURDEN; TUMOR MICROENVIRONMENT;

EID: 84919723781     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-1236     Document Type: Article

References (36)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
2. Wilting J, Hawighorst T, Hecht M., Christ B, Papoutsi M. Development of lymphatic vessels: tumour lymphangiogenesis and lymphatic invasion. Curr Med Chem 2005;12:3043-53.
3. Curiel TJ, Coukos G, Zou L., Alvarez X, Cheng P, Mottram P., et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10: 942-9.
4. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 2006;6:295-307.
5. Kzhyshkowska J, Gratchev A, Goerdt S. Stabilin-1, a homeostatic scavenger receptor with multiple functions. J Cell Mol Med 2006; 10:635-49.
6. Lin EY, Pollard JW. Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res 2007;67:5064-6.
7. Adachi H, Tsujimoto M. FEEL-1, a novel scavenger receptor with in vitro bacteria-binding and angiogenesis-modulating activities. J Biol Chem 2002;277:34264-70.
8. Prevo R, Banerji S, Ni J., Jackson DG. Rapid plasma membraneendosomal trafficking of the lymph node sinus and high endothelial venule scavenger receptor/homing receptor stabilin-1 (FEEL-1/CLEV-ER-1). J Biol Chem 2004;279:52580-92.
9. Kzhyshkowska J, Workman G, Cardo-Vila M, Arap W., Pasqualini R, Gratchev A, et al. Novel function of alternatively activated macrophages: stabilin-1-mediated clearance of SPARC. J Immunol 2006; 176:5825-32.
10. Kzhyshkowska J, Gratchev A, Schmuttermaier C., Brundiers H, Krusell L, Mamidi S., et al. Alternatively activated macrophages regulate extracellular levels of the hormone placental lactogen via receptor-mediated uptake and transcytosis. J Immunol 2008;180: 3028-37.
11. Kzhyshkowska J, Gratchev A, Martens J.H., Pervushina O., Mamidi S, Johansson S, et al. Stabilin-1 localizes to endosomes and the trans-Golgi network in human macrophages and interacts with GGA adaptors. J Leukoc Biol 2004;76:1151-61.
12. Goerdt S, Walsh LJ, Murphy G.F., Pober JS. Identification of a novel high molecular weight protein preferentially expressed by sinusoidal endothelial cells in normal human tissues. J Cell Biol 1991;113: 1425-37.
13. Irjala H, Elima K, Johansson E.L., Merinen M., Kontula K, Alanen K, et al. The same endothelial receptor controls lymphocyte traffic both in vascular and lymphatic vessels. Eur J Immunol 2003;33:815-24.
14. Martens JH, Kzhyshkowska J, Falkowski-Hansen M, Schledzewski K., Gratchev A, Mansmann U, et al. Differential expression of a gene signature for scavenger/lectin receptors by endothelial cells and macrophages in human lymph node sinuses, the primary sites of regional metastasis. J Pathol 2006;208:574-89.
15. Irjala H, Alanen K, Grenman R., Heikkila P, Joensuu H, Jalkanen S. 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 2003; 63:4671-6.
16. Salmi M, Koskinen K, Henttinen T., Elima K, Jalkanen S. CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood 2004;104:3849-57.
17. Karikoski M, Irjala H, Maksimow M., Miiluniemi M, Granfors K, Hernesniemi S., et al. Clever-1/Stabilin-1 regulates lymphocyte migration within lymphatics and leukocyte entrance to sites of inflammation. Eur J Immunol 2009;39:3477-87.
18. Ålgars A, Irjala H., Vaittinen S, Huhtinen H, Sundström J, Salmi M., et al. Type and location of tumor-infiltrating macrophages and lymphatic vessels predict survival of colorectal cancer patients. Int J Cancer 2012;131:864-73.
19. Holmdahl R, Malissen B. The need for littermate controls. Eur J Immunol 2012;42:45-7.
20. Lewandoski M, Meyers EN, Martin GR. Analysis of Fgf8 gene function in vertebrate development. Cold Spring Harb Symp Quant Biol 1997;62:159-68.
21. Koni PA, Joshi SK, Temann U.A., Olson D., Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med 2001; 193:741-54.
22. Clausen BE, Burkhardt C, Reith W., Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 1999;8:265-77.
23. Marttila-Ichihara F., Turja R, Miiluniemi M., Karikoski M, Maksimow M, Niemela J., et al. Macrophage mannose receptor on lymphatics controls cell trafficking. Blood 2008;112:64-72.
24. Fischer C, Jonckx B, Mazzone M., Zacchigna S, Loges S, Pattarini L., et al. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 2007;131: 463-75.
25. + macrophages in malignant tumours and wound healing tissue in vivo and in bone marrow cultures in vitro: implications for the assessment of lymphangiogenesis. J Pathol 2006;209:67-77.
26. + myeloid cells into tumors. Cancer Res 2009;69: 7875-83.
27. Jalkanen ST, Butcher EC. In vitro analysis of the homing properties of human lymphocytes: developmental regulation of functional receptors for high endothelial venules. Blood 1985;66:577-82.
28. Salmi M, Jalkanen S. Human leukocyte subpopulations from inflamed gut bind to joint vasculature using distinct sets of adhesion molecules. J Immunol 2001;166:4650-7.
29. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003;3:23-35.
30. Palani S, Maksimow M, Miiluniemi M., Auvinen K, Jalkanen S, Salmi M. Stabilin-1/CLEVER-1, a type2 macrophagemarker, isanadhesionand scavenging molecule on human placental macrophages. Eur J Immunol 2011;41:2052-63.
31. Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol 2013;35:585-600.
32. Porta C, Larghi P, Rimoldi M., Totaro MG, Allavena P, Mantovani A, et al. Cellular and molecular pathways linking inflammation and cancer. Immunobiology 2009;214:761-77.
33. Movahedi K, Laoui D, Gysemans C., Baeten M, Stange G, Van den Bossche J, et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 2010;70:5728-39.
34. +regulatoryTcells, which suppressvia membrane-bound TGFbeta-1. J Immunol 2008;181:2220-6.
35. Turk MJ, Guevara-Patino JA, Rizzuto G.A., Engelhorn ME, Sakaguchi S, Houghton AN. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J Exp Med 2004;200: 771-82.
36. Bouwhuis MG, Ten Hagen TL, Suciu S, Eggermont AM. Autoimmunity and treatment outcome in melanoma. Curr Opin Oncol 2011;23:170-6.