Salmonella-mediated tumor regression involves targeting of tumor myeloid suppressor cells causing a shift to M1-like phenotype and reduction in suppressive capacity

Cancer Immunology, Immunotherapy

Volumn 63, Issue 6, 2014, Pages 587-599

  Kaimala, Suneesh ^a   Mohamed, Yassir A ^a   Nader, Nancy ^a   Issac, Jincy ^a   Elkord, Eyad ^a   Chouaib, Salem ^b   Fernandez Cabezudo, Maria J ^a   Al Ramadi, Basel K ^a  

^a UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

^b INSERM   (France)

Author keywords

Macrophages; Myeloid suppressor cells; Salmonella; Tumor immunity

Indexed keywords

ARGINASE 1; ATAXIN 1; CALGRANULIN B; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 4; MYELOID DIFFERENTIATION FACTOR 88; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL STRAIN; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CELL MATURATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; IMMUNE RESPONSE; MACROPHAGE ACTIVATION; MELANOMA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA TYPHIMURIUM; SPLEEN CELL; SUPPRESSOR CELL; SURVIVAL; T LYMPHOCYTE; TUMOR GROWTH; TUMOR REGRESSION; TUMOR VOLUME; UPREGULATION;

ANIMALS; ANTIGENS, CD11B; ARGINASE; BLOTTING, WESTERN; FEMALE; INTERLEUKIN-4; MACROPHAGES; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, NUDE; MYELOID CELLS; NITRIC OXIDE SYNTHASE TYPE II; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SALMONELLA TYPHIMURIUM; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; VACCINES, ATTENUATED;

EID: 84901635201     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-014-1543-x     Document Type: Article

References (50)

1. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V (2012) Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 12(4):253-268
2. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23(11):549-555
3. Poschke I, Kiessling R (2012) On the armament and appearances of human myeloid-derived suppressor cells. Clin Immunol 144(3):250-268
4. Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141(1):39-51
5. Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496(7446):445-455
6. Steidl C, Lee T, Shah SP, Farinha P, Han G, Nayar T, Delaney A, Jones SJ, Iqbal J, Weisenburger DD, Bast MA, Rosenwald A, Muller-Hermelink HK, Rimsza LM, Campo E, Delabie J, Braziel RM, Cook JR, Tubbs RR, Jaffe ES, Lenz G, Connors JM, Staudt LM, Chan WC, Gascoyne RD (2010) Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med 362(10):875-885
7. Zabuawala T, Taffany DA, Sharma SM, Merchant A, Adair B, Srinivasan R, Rosol TJ, Fernandez S, Huang K, Leone G, Ostrowski MC (2010) An ets2-driven transcriptional program in tumor-associated macrophages promotes tumor metastasis. Cancer Res 70(4):1323-1333
8. al-Ramadi BK, Brodkin MA, Mosser DM, Eisenstein TK (1991) Immunosuppression induced by attenuated Salmonella. Evidence for mediation by macrophage precursors. J Immunol 146(8):2737-2746
9. al-Ramadi BK, Chen YW, Meissler JJ Jr, Eisenstein TK (1991) Immunosuppression induced by attenuated Salmonella. Reversal by IL-4. J Immunol 147(6):1954-1961
10. Sander LE, Sackett SD, Dierssen U, Beraza N, Linke RP, Muller M, Blander JM, Tacke F, Trautwein C (2010) Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J Exp Med 207(7):1453-1464
11. Van Ginderachter JA, Beschin A, De Baetselier P, Raes G (2010) Myeloid-derived suppressor cells in parasitic infections. Eur J Immunol 40(11):2976-2985
12. Balkwill F, Charles KA, Mantovani A (2005) Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7(3):211-217
13. Saccani A, Schioppa T, Porta C, Biswas SK, Nebuloni M, Vago L, Bottazzi B, Colombo MP, Mantovani A, Sica A (2006) p50 nuclear factor-kappaB overexpression in tumor-associated macrophages inhibits M1 inflammatory responses and antitumor resistance. Cancer Res 66(23):11432-11440
14. Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, Politi LS, Gentner B, Brown JL, Naldini L, De Palma M (2011) Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 19(4):512-526
15. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, Song H, Vandenberg S, Johnson RS, Werb Z, Bergers G (2008) HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13(3):206-220
16. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, Cho HI, Celis E, Quiceno DG, Padhya T, McCaffrey TV, McCaffrey JC, Gabrilovich DI (2010) HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 207(11):2439-2453
17. Hix LM, Karavitis J, Khan MW, Shi YH, Khazaie K, Zhang M (2013) Tumor STAT1 transcription factor activity enhances breast tumor growth and immune suppression mediated by myeloid-derived suppressor cells. J Biol Chem 288(17):11676-11688
18. Sonda N, Simonato F, Peranzoni E, Cali B, Bortoluzzi S, Bisognin A, Wang E, Marincola FM, Naldini L, Gentner B, Trautwein C, Sackett SD, Zanovello P, Molon B, Bronte V (2013) miR-142-3p prevents macrophage differentiation during cancer-induced myelopoiesis. Immunity 38(6):1236-1249
19. Forbes NS (2010) Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer 10(11):785-794
20. Lee CH (2012) Engineering bacteria toward tumor targeting for cancer treatment: current state and perspectives. Appl Microbiol Biotechnol 93(2):517-523
21. Eisenstein TK, Bushnell B, Meissler JJ Jr, Dalal N, Schafer R, Havas HF (1995) Immunotherapy of a plasmacytoma with attenuated Salmonella. Med Oncol 12(2):103-108
22. Pawelek JM, Low KB, Bermudes D (1997) Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res 57:4537-4544
23. al-Ramadi BK, Fernandez-Cabezudo MJ, El-Hasasna H, Al-Salam S, Bashir G, Chouaib S (2009) Potent anti-tumor activity of systemically-administered IL2-expressing Salmonella correlates with decreased angiogenesis and enhanced tumor apoptosis. Clin Immunol 130(1):89-97
24. al-Ramadi BK, Fernandez-Cabezudo MJ, El-Hasasna H, Al-Salam S, Attoub S, Xu D, Chouaib S (2008) Attenuated bacteria as effectors in cancer immunotherapy. Ann N Y Acad Sci 1138:351-357
25. Richter-Dahlfors A, Buchan AMJ, Finlay BB (1997) Murine Salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186:569-580
26. al-Ramadi BK, Adeghate E, Mustafa N, Ponery AS, Fernandez-Cabezudo MJ (2002) Cytokine expression by attenuated intracellular bacteria regulates the immune response to infection: the Salmonella model. Mol Immunol 38(12-13):931-940
27. Fernandez-Cabezudo MJ, El-Kharrag R, Torab F, Bashir G, George JA, El-Taji H, al-Ramadi BK (2013) Intravenous administration of manuka honey inhibits tumor growth and improves host survival when used in combination with chemotherapy in a melanoma mouse model. PLoS One 8(2):e55993
28. al-Ramadi BK, Bashir G, Rizvi TA, Fernandez-Cabezudo MJ (2004) Poor survival but high immunogenicity of IL-2-expressing Salmonella typhimurium in inherently resistant mice. Microbes Infect 6(4):350-359
29. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9(1):143-150
30. Xu J, Foy TM, Laman JD, Elliott EA, Dunn JJ, Waldschmidt TJ, Elsemore J, Noelle RJ, Flavell RA (1994) Mice deficient for the CD40 ligand. Immunity 1:423-431
31. Issac JM, Sarawathiamma D, Al-Ketbi MI, Azimullah S, Al-Ojali SM, Mohamed YA, Flavell RA, Fernandez-Cabezudo MJ, al-Ramadi BK (2013) Differential outcome of infection with attenuated Salmonella in MyD88-deficient mice is dependent on the route of administration. Immunobiology 218(1):52-63
32. al-Ramadi BK, Fernandez-Cabezudo MJ, Ullah A, El-Hasasna H, Flavell RA (2006) CD154 is essential for protective immunity in experimental salmonella infection: evidence for a dual role in innate and adaptive immune responses. J Immunol 176(1):496-506
33. Fernandez-Cabezudo MJ, Mechkarska M, Azimullah S, al-Ramadi BK (2009) Modulation of macrophage proinflammatory functions by cytokine-expressing Salmonella vectors. Clin Immunol 130(1):51-60
34. Dolcetti L, Peranzoni E, Ugel S, Marigo I, Fernandez Gomez A, Mesa C, Geilich M, Winkels G, Traggiai E, Casati A, Grassi F, Bronte V (2010) Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 40(1):22-35
35. Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J (2009) The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leukoc Biol 86(3):557-566
36. al-Ramadi BK, Greene JM, Meissler JJ Jr, Eisenstein TK (1992) Immunosuppression induced by attenuated Salmonella: effect of LPS responsiveness on development of suppression. Microb Pathog 12(4):267-278
37. al-Ramadi BK, Meissler JJ Jr, Huang D, Eisenstein TK (1992) Immunosuppression induced by nitric oxide and its inhibition by interleukin-4. Eur J Immunol 22(9):2249-2254
38. Low KB, Ittensohn M, Le T, Platt J, Sodi S, Amoss M, Ash O, Carmichael E, Chakraborty A, Fischer J, Lin SL, Luo X, Miller SI, Zheng L, King I, Pawelek JM, Bermudes D (1999) Lipid A mutant Salmonella with suppressed virulence and TNFalpha induction retain tumor-targeting in vivo. Nat Biotechnol 17(1):37-41
39. Kasinskas RW, Forbes NS (2007) Salmonella typhimurium lacking ribose chemoreceptors localize in tumor quiescence and induce apoptosis. Cancer Res 67(7):3201-3209
40. Leschner S, Westphal K, Dietrich N, Viegas N, Jablonska J, Lyszkiewicz M, Lienenklaus S, Falk W, Gekara N, Loessner H, Weiss S (2009) Tumor invasion of Salmonella enterica serovar Typhimurium is accompanied by strong hemorrhage promoted by TNF-alpha. PLoS One 4(8):e6692
41. Ganai S, Arenas RB, Sauer JP, Bentley B, Forbes NS (2011) In tumors Salmonella migrate away from vasculature toward the transition zone and induce apoptosis. Cancer Gene Ther 18(7):457-466
42. Lee CH, Wu CL, Shiau AL (2008) Toll-like receptor 4 mediates an antitumor host response induced by Salmonella choleraesuis. Clin Cancer Res 14(6):1905-1912
43. Saccheri F, Pozzi C, Avogadri F, Barozzi S, Faretta M, Fusi P, Rescigno M (2010) Bacteria-induced gap junctions in tumors favor antigen cross-presentation and antitumor immunity. Sci Transl Med 2(44):44ra57
44. al-Ramadi BK, Al-Dhaheri MH, Mustafa N, Abouhaidar M, Xu D, Liew FY, Lukic ML, Fernandez-Cabezudo MJ (2001) Influence of vector-encoded cytokines on anti-Salmonella immunity: divergent effects of interleukin-2 and tumor necrosis factor alpha. Infect Immun 69(6):3980-3988
45. Dougan G, John V, Palmer S, Mastroeni P (2011) Immunity to salmonellosis. Immunol Rev 240(1):196-210
46. Bronte V, Zanovello P (2005) Regulation of immune responses by l-arginine metabolism. Nat Rev Immunol 5(8):641-654
47. Gallina G, Dolcetti L, Serafini P, De Santo C, Marigo I, Colombo MP, Basso G, Brombacher F, Borrello I, Zanovello P, Bicciato S, Bronte V (2006) Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 116(10):2777-2790
48. Hong EH, Chang SY, Lee BR, Pyun AR, Kim JW, Kweon MN, Ko HJ (2013) Intratumoral injection of attenuated Salmonella vaccine can induce tumor microenvironmental shift from immune suppressive to immunogenic. Vaccine 31(10):1377-1384
49. Angiolillo AL, Sgadari C, Taub DD, Liao F, Farber JM, Maheshwari S, Kleinman HK, Reaman GH, Tosato G (1995) Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J Exp Med 182(1):155-162
50. Sgadari C, Farber JM, Angiolillo AL, Liao F, Teruya-Feldstein J, Burd PR, Yao L, Gupta G, Kanegane C, Tosato G (1997) Mig, the monokine induced by interferon-gamma, promotes tumor necrosis in vivo. Blood 89(8):2635-2643