Empty liposomes induce antitumoral effects associated with macrophage responses distinct from those of the TLR1/2 agonist Pam3CSK 4 (BLP)

Cancer Immunology, Immunotherapy

Volumn 62, Issue 10, 2013, Pages 1587-1597

  König, Simone ^a   Regen, Tommy ^a,c   Dittmann, Kai ^a   Engelke, Michael ^a   Wienands, Jürgen ^a   Schwendener, Reto ^b   Hanisch, Uwe Karsten ^a   Pukrop, Tobias ^a   Hahn, Heidi ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Antitumor effects; Bacterial lipoprotein; Liposomes; Macrophages; TAM

Indexed keywords

ANTINEOPLASTIC AGENT; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPROTEIN; PHOSPHATIDYLCHOLINE LIPOSOME; PROTEIN PAM3CSK4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARG1 GENE; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; CXCL10 GENE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; IN VITRO STUDY; INOS GENE; MACROPHAGE; MACROPHAGE FUNCTION; MACROPHAGE MIGRATION INHIBITION; MARKER GENE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN TUMOR; TREM2 GENE; TUMOR MICROENVIRONMENT;

ANIMALS; CARCINOMA, BASAL CELL; GENE EXPRESSION; LIPOPEPTIDES; LIPOSOMES; MACROPHAGES; MICE; RANDOM ALLOCATION; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2;

EID: 84885847692     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1444-4     Document Type: Article

References (50)

1. Immordino ML, Dosio F, Cattel L (2006) Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int J Nanomedicine 1:297-315
2. Riaz M (1995) Review article: stability and uses of liposomes. Pak J Pharm Sci 8:69-79
3. Schwendener RA (2007) Liposomes in biology and medicine. Adv Exp Med Biol 620:117-128
4. Alipour M, Smith MG, Pucaj K, Suntres ZE (2012) Acute toxicity study of liposomal antioxidant formulations containing Nacetylcysteine, alpha-tocopherol, and gamma-tocopherol in rats. J Liposome Res 22(2):158-167
5. Papahadjopoulos D, Allen TM, Gabizon A, Mayhew E, Matthay K et al (1991) Sterically stabilized liposomes: improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc Natl Acad Sci USA 88:11460-11464
6. van Rooijen N, van Nieuwmegen R (1980) Liposomes in immunology: multilamellar phosphatidylcholine liposomes as a simple, biodegradable and harmless adjuvant without any immunogenic activity of its own. Immunol Commun 9:243-256
7. Takano S, Aramaki Y, Tsuchiya S (2003) Physicochemical properties of liposomes affecting apoptosis induced by cationic liposomes in macrophages. Pharm Res 20:962-968
8. Ma HM, Wu Z, Nakanishi H (2011) Phosphatidylserine-containing liposomes suppress inflammatory bone loss by ameliorating the cytokine imbalance provoked by infiltrated macrophages. Lab Invest 91:921-931
9. Zhang J, Fujii S, Wu Z, Hashioka S, Tanaka Y et al (2006) Involvement of COX-1 and up-regulated prostaglandin E synthases in phosphatidylserine liposome-induced prostaglandin E2 production by microglia. J Neuroimmunol 172:112-120
10. Graeser R, Bornmann C, Esser N, Ziroli V, Jantscheff P et al (2009) Antimetastatic effects of liposomal gemcitabine and empty liposomes in an orthotopic mouse model of pancreatic cancer. Pancreas 38:330-337
11. Gordon S, Taylor PR (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5:953-964
12. Lewis CE, Pollard JW (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res 66:605-612
13. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A et al (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677-686
14. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958-969
15. Biswas SK, Mantovani A (2010) Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 11:889-896
16. Ydens E, Cauwels A, Asselbergh B, Goethals S, Peeraer L et al (2012) Acute injury in the peripheral nervous system triggers an alternative macrophage response. J Neuroinflammation 9:176
17. Liew FY, Patel M, Xu D (2005) Toll-like receptor 2 signalling and inflammation. Ann Rheum Dis 64(Suppl 4):iv104-iv105
18. Zhang Y, Luo F, Cai Y, Liu N, Wang L et al (2011) TLR1/TLR2 agonist induces tumor regression by reciprocal modulation of effector and regulatory T cells. J Immunol 186:1963-1969
19. Zeisberger SM, Odermatt B, Marty C, Zehnder-Fjallman AH, Ballmer-Hofer K et al (2006) Clodronate-liposome-mediated depletion of tumour-associated macrophages: a new and highly effective antiangiogenic therapy approach. Br J Cancer 95:272-281
20. Zibat A, Uhmann A, Nitzki F, Wijgerde M, Frommhold A et al (2009) Time-point and dosage of gene inactivation determine the tumor spectrum in conditional Ptch knockouts. Carcinogenesis 30:918-926
21. So PL, Langston AW, Daniallinia N, Hebert JL, Fujimoto MA et al (2006) Long-term establishment, characterization and manipulation of cell lines from mouse basal cell carcinoma tumors. Exp Dermatol 15:742-750
22. Francke A, Herold J, Weinert S, Strasser RH, Braun-Dullaeus RC (2011) Generation of mature murine monocytes from heterogeneous bone marrow and description of their properties. J Histochem Cytochem 59:813-825
23. Liu J, Buckley JM, Redmond HP, Wang JH (2010) ST2 negatively regulates TLR2 signaling, but is not required for bacterial lipoprotein-induced tolerance. J Immunol 184:5802-5808
24. Scheffel J, Regen T, Van Rossum D, Seifert S, Ribes S et al (2012) Toll-like receptor activation reveals developmental reorganization and unmasks responder subsets of microglia. Glia 60:1930-1943
25. Rasmussen JW, Cello J, Gil H, Forestal CA, Furie MB et al (2006) Mac-1 ? cells are the predominant subset in the early hepatic lesions of mice infected with Francisella tularensis. Infect Immun 74:6590-6598
26. Ferron M, Vacher J (2005) Targeted expression of cre recombinase in macrophages and osteoclasts in transgenic mice. Genesis 41:138-145
27. D'Ambrosio D, Panina-Bordignon P, Sinigaglia F (2003) Chemokine receptors in inflammation: an overview. J Immunol Methods 273:3-13
28. Zhao Q (2010) Dual targeting of CCR2 and CCR5: therapeutic potential for immunologic and cardiovascular diseases. J Leukoc Biol 88:41-55
29. Salaun B, Coste I, Rissoan MC, Lebecque SJ, Renno T (2006) TLR3 can directly trigger apoptosis in human cancer cells. J Immunol 176:4894-4901
30. Geutskens SB, Nikolic T, Dardenne M, Leenen PJ, Savino W (2004) Defective up-regulation of CD49d in final maturation of NOD mouse macrophages. Eur J Imun 34:3465-3476
31. Aliprantis AO, Yang RB, Weiss DS, Godowski P, Zychlinsky A (2000) The apoptotic signaling pathway activated by Toll-like receptor-2. EMBO J 19:3325-3336
32. Luster AD (2002) The role of chemokines in linking innate and adaptive immunity. Curr Opin Immunol 14:129-135
33. Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29:313-326
34. Murata M (2008) Activation of Toll-like receptor 2 by a novel preparation of cell wall skeleton from mycobacterium bovis BCG Tokyo (SMP-105) sufficiently enhances immune responses against tumors. Cancer Sci 99:1435-1440
35. Cheng N, Xia T, Han Y, He QJ, Zhao R et al (2011) Synergistic antitumor effects of liposomal honokiol combined with cisplatin in colon cancer models. Oncol Lett 2:957-962
36. SakakimaY, HayakawaA, Nagasaka T, Nakao A(2007) Prevention of hepatocarcinogenesis with phosphatidylcholine and menaquinone-4: in vitro and in vivo experiments. J Hepatol 47:83-92
37. Fukunaga K, Hossain Z, Takahashi K (2008) Marine phosphatidylcholine suppresses 1,2-dimethylhydrazine-induced colon carcinogenesis in rats by inducing apoptosis. Nutr Res 28:635-640
38. Cheng Y, Zhao Q, Liu X, Araki S, Zhang S et al (2006) Phosphatidylcholine-specific phospholipase C, p53 and ROS in the association of apoptosis and senescence in vascular endothelial cells. FEBS Lett 580:4911-4915
39. Li H, Lee JH, Kim SY, Yun HY, Baek KJ et al (2011) Phosphatidylcholine induces apoptosis of 3T3-L1 adipocytes. J Biomed Sci 18:91
40. Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS et al (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472:57-63
41. Harokopakis E, Hajishengallis G, Michalek SM (1998) Effectiveness of liposomes possessing surface-linked recombinant B subunit of cholera toxin as an oral antigen delivery system. Infect Immun 66:4299-4304
42. Richards RL, Rao M, Wassef NM, Glenn GM, Rothwell SW et al (1998) Liposomes containing lipid A serve as an adjuvant for induction of antibody and cytotoxic T-cell responses against RTS, S malaria antigen. Infect Immun 66:2859-2865
43. Faisal SM, Chen JW, McDonough SP, Chang CF, Teng CH et al (2011) Immunostimulatory and antigen delivery properties of liposomes made up of total polar lipids from non-pathogenic bacteria leads to efficient induction of both innate and adaptive immune responses. Vaccine 29:2381-2391
44. Laverman P, Dams ET, Storm G, Hafmans TG, Croes HJ et al (2001) Microscopic localization of PEG-liposomes in a rat model of focal infection. J Controlled Release 75:347-355
45. De Palma M, Lewis CE (2013) Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 23:277-286
46. Sonoki T, Nagasaki A, Gotoh T, Takiguchi M, Takeya M et al (1997) Coinduction of nitric-oxide synthase and arginase I in cultured rat peritoneal macrophages and rat tissues in vivo by lipopolysaccharide. J Biol Chem 272:3689-3693
47. Turnbull IR, Gilfillan S, Cella M, Aoshi T, Miller M et al (2006) Cutting edge: TREM-2 attenuates macrophage activation. J Immunol 177:3520-3524
48. Gordon S, Martinez FO (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32:593-604
49. Carr MW, Roth SJ, Luther E, Rose SS, Springer TA (1994) Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc Natl Acad Sci U S A 91:3652-3656
50. Flaishon L, Becker-Herman S, Hart G, Levo Y, Kuziel WA et al (2004) Expression of the chemokine receptor CCR2 on immature B cells negatively regulates their cytoskeletal rearrangement and migration. Blood 104:933-941