Functional TRAIL receptors in monocytes and tumor-associated macrophages: A possible targeting pathway in the tumor microenvironment

Oncotarget

Volumn 7, Issue 27, 2016, Pages 41662-41676

  Liguori, Manuela ^a   Buracchi, Chiara ^a   Pasqualini, Fabio ^a   Bergomas, Francesca ^a   Pesce, Samantha ^a   Sironi, Marina ^a   Grizzi, Fabio ^a   Mantovani, Alberto ^a,b   Belgiovine, Cristina ^a   Allavena, Paola ^a,b  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b HUMANITAS UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

APIGENIN; CASPASE 8; GLUCOCORTICOID; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; PALMITIC ACID; QUERCETIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE; LYMPHOCYTE; MACROPHAGE; METASTASIS; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTE; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASM; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELLS, CULTURED; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MOLECULAR TARGETED THERAPY; MONOCYTES; NEOPLASMS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR MICROENVIRONMENT;

EID: 85011400108     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9340     Document Type: Article

References (64)

1. Coussens LM, Zitvogel L, Palucka AK. Neutralizing tumorpromoting chronic inflammation: a magic bullet? Science. 2013; 339:286-291.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
3. Mantovani A, Allavena P, Sica A, Balkwill F. Cancerrelated inflammation. Nature. 2008; 454:436-444.
4. Chittezhath M, Dhillon MK, Lim JY, Laoui D, Shalova IN, Teo YL, Chen J, Kamaraj R, Raman L, Lum J, Thamboo TP, Chiong E, Zolezzi F, Yang H, Van Ginderachter JA, Poidinger M, et al. Molecular profiling reveals a tumorpromoting phenotype of monocytes and macrophages in human cancer progression. Immunity. 2014; 41:815-829.
5. Li H, Yang B, Huang J, Lin Y, Xiang T, Wan J, Chouaib S, Ren G. Cyclooxygenase-2 in tumor-associated macrophages promotes breast cancer cell survival by triggering a positive-feedback loop between macrophages and cancer cells. Oncotarget. 2015; 6:29637-29650. doi: 10.18632/oncotarget.4936.
6. Lin L, Chen YS, Yao YD, Chen JQ, Chen JN, Huang SY, Zeng YJ, Yao HR, Zeng SH, Fu YS, Song EW. CCL18 from tumor-associated macrophages promotes angiogenesis in breast cancer. Oncotarget. 2015; 6:34758-34773. doi: 10.18632/oncotarget.5325.
7. Mantovani A, Allavena P. The interaction of anticancer therapies with tumor-associated macrophages. J Exp Med. 2015; 212:435-445.
8. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity. 2014; 41:49-61.
9. Brana I, Calles A, LoRusso PM, Yee LK, Puchalski TA, Seetharam S, Zhong B, de Boer CJ, Tabernero J, Calvo E. Carlumab, an anti-C-C chemokine ligand 2 monoclonal antibody, in combination with four chemotherapy regimens for the treatment of patients with solid tumors: an openlabel, multicenter phase 1b study. Target Oncol. 2015; 10:111-123.
10. Sandhu SK, Papadopoulos K, Fong PC, Patnaik A, Messiou C, Olmos D, Wang G, Tromp BJ, Puchalski TA, Balkwill F, Berns B, Seetharam S, de Bono JS, Tolcher AW. A firstin- human, first-in-class, phase I study of carlumab (CNTO 888), a human monoclonal antibody against CC-chemokine ligand 2 in patients with solid tumors. Cancer Chemother Pharmacol. 2013; 71:1041-1050.
11. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA, Rugo HS, Hwang ES, Jirstrom K, West BL, Coussens LM. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 2011; 1:54-67.
12. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V, Setty M, Leslie CS, Oei Y, Pedraza A, Zhang J, Brennan CW, et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med. 2013; 19:1264-1272.
13. Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, Rey-Giraud F, Pradel LP, Feuerhake F, Klaman I, Jones T, Jucknischke U, Scheiblich S, Kaluza K, Gorr IH, Walz A, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell. 2014; 25:846-859.
14. Germano G, Frapolli R, Belgiovine C, Anselmo A, Pesce S, Liguori M, Erba E, Uboldi S, Zucchetti M, Pasqualini F, Nebuloni M, van Rooijen N, Mortarini R, Beltrame L, Marchini S, Fuso Nerini I, et al. Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell. 2013; 23:249-262.
15. Vincent M, Sayre NL, Graham MJ, Crooke RM, Shealy DJ, Liscum L. Evaluation of an anti-tumor necrosis factor therapeutic in a mouse model of Niemann-Pick C liver disease. PLoS One. 2010; 5:e12941.
16. Chen W, Ma T, Shen XN, Xia XF, Xu GD, Bai XL, Liang TB. Macrophage-induced tumor angiogenesis is regulated by the TSC2-mTOR pathway. Cancer Res. 2012; 72:1363-1372.
17. Mercalli A, Calavita I, Dugnani E, Citro A, Cantarelli E, Nano R, Melzi R, MaffiP, Secchi A, Sordi V, Piemonti L. Rapamycin unbalances the polarization of human macrophages to M1. Immunology. 2013; 140:179-190.
18. Mercier I, Camacho J, Titchen K, Gonzales DM, Quann K, Bryant KG, Molchansky A, Milliman JN, Whitaker- Menezes D, Sotgia F, Jasmin JF, Schwarting R, Pestell RG, Blagosklonny MV, Lisanti MP. Caveolin-1 and accelerated host aging in the breast tumor microenvironment: chemoprevention with rapamycin, an mTOR inhibitor and anti-aging drug. Am J Pathol. 2012; 181:278-293.
19. Klug F, Prakash H, Huber PE, Seibel T, Bender N, Halama N, Pfirschke C, Voss RH, Timke C, Umansky L, Klapproth K, Schakel K, Garbi N, Jager D, Weitz J, Schmitz- Winnenthal H, et al. Low-dose irradiation programs macrophage differentiation to an iNOS(+)/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell. 2013; 24:589-602.
20. Zhao Y, Wang D, Xu T, Liu P, Cao Y, Wang Y, Yang X, Xu X, Wang X, Niu H. Bladder cancer cells re-educate TAMs through lactate shuttling in the microfluidic cancer microenvironment. Oncotarget. 2015; 6:39196-39210. doi: 10.18632/oncotarget.5538.
21. Almasan A, Ashkenazi A. Apo2L/TRAIL: apoptosis signaling, biology, and potential for cancer therapy. Cytokine Growth Factor Rev. 2003; 14:337-348.
22. Degli-Esposti MA, Smolak PJ, Walczak H, Waugh J, Huang CP, DuBose RF, Goodwin RG, Smith CA. Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor family. J Exp Med. 1997; 186:1165-1170.
23. Lee HW, Lee SH, Ryu YW, Kwon MH, Kim YS. Homomeric and heteromeric interactions of the extracellular domains of death receptors and death decoy receptors. Biochemical and biophysical research communications. 2005; 330:1205-1212.
24. Aggarwal BB, Gupta SC, Kim JH. Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey. Blood. 2012; 119:651-665.
25. Ashkenazi A. Targeting the extrinsic apoptosis pathway in cancer. Cytokine Growth Factor Rev. 2008; 19:325-331.
26. Ashkenazi A. Targeting the extrinsic apoptotic pathway in cancer: lessons learned and future directions. J Clin Invest. 2015; 125:487-489.
27. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer. 2008; 8:782-798.
28. Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, Sutherland GR, Smith TD, Rauch C, Smith CA, et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity. 1995; 3:673-682.
29. Benedict CA, Ware CF. TRAIL: not just for tumors anymore? J Exp Med. 2012; 209:1903-1906.
30. Daniels RA, Turley H, Kimberley FC, Liu XS, Mongkolsapaya J, Ch'En P, Xu XN, Jin BQ, Pezzella F, Screaton GR. Expression of TRAIL and TRAIL receptors in normal and malignant tissues. Cell research. 2005; 15:430-438.
31. Steinwede K, Henken S, Bohling J, Maus R, Ueberberg B, Brumshagen C, Brincks EL, Griffith TS, Welte T, Maus UA. TNF-related apoptosis-inducing ligand (TRAIL) exerts therapeutic efficacy for the treatment of pneumococcal pneumonia in mice. J Exp Med. 2012; 209:1937-1952.
32. Cazanave SC, Mott JL, Bronk SF, Werneburg NW, Fingas CD, Meng XW, Finnberg N, El-Deiry WS, Kaufmann SH, Gores GJ. Death receptor 5 signaling promotes hepatocyte lipoapoptosis. J Biol Chem. 2011; 286:39336-39348.
33. Prasad S, Kim JH, Gupta SC, Aggarwal BB. Targeting death receptors for TRAIL by agents designed by Mother Nature. Trends in pharmacological sciences. 2014; 35:520-536.
34. Wu GS, Burns TF, Zhan Y, Alnemri ES, El-Deiry WS. Molecular cloning and functional analysis of the mouse homologue of the KILLER/DR5 tumor necrosis factorrelated apoptosis-inducing ligand (TRAIL) death receptor. Cancer Res. 1999; 59:2770-2775.
35. Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol. 2013; 35:585-600.
36. Ehrlich S, Infante-Duarte C, Seeger B, Zipp F. Regulation of soluble and surface-bound TRAIL in human T cells, B cells, and monocytes. Cytokine. 2003; 24:244-253.
37. Lamhamedi-Cherradi SE, Zheng SJ, Maguschak KA, Peschon J, Chen YH. Defective thymocyte apoptosis and accelerated autoimmune diseases in TRAIL-/- mice. Nature immunology. 2003; 4:255-260.
38. Song K, Chen Y, Goke R, Wilmen A, Seidel C, Goke A, Hilliard B. Tumor necrosis factor-related apoptosisinducing ligand (TRAIL) is an inhibitor of autoimmune inflammation and cell cycle progression. J Exp Med. 2000; 191:1095-1104.
39. Cretney E, Uldrich AP, Berzins SP, Strasser A, Godfrey DI, Smyth MJ. Normal thymocyte negative selection in TRAILdeficient mice. J Exp Med. 2003; 198:491-496.
40. Sedger LM, Katewa A, Pettersen AK, Osvath SR, Farrell GC, Stewart GJ, Bendall LJ, Alexander SI. Extreme lymphoproliferative disease and fatal autoimmune thrombocytopenia in FasL and TRAIL double-deficient mice. Blood. 2010; 115:3258-3268.
41. Diehl GE, Yue HH, Hsieh K, Kuang AA, Ho M, Morici LA, Lenz LL, Cado D, Riley LW, Winoto A. TRAIL-R as a negative regulator of innate immune cell responses. Immunity. 2004; 21:877-889.
42. Cullen SP, Martin SJ. Fas and TRAIL 'death receptors' as initiators of inflammation: Implications for cancer. Seminars in cell & developmental biology. 2015; 39:26-34.
43. Bossi F, Bernardi S, Zauli G, Secchiero P, Fabris B. TRAIL modulates the immune system and protects against the development of diabetes. Journal of immunology research. 2015; 2015:680749.
44. Zauli G, Sancilio S, Cataldi A, Sabatini N, Bosco D, Di Pietro R. PI-3K/Akt and NF-kappaB/IkappaBalpha pathways are activated in Jurkat T cells in response to TRAIL treatment. Journal of cellular physiology. 2005; 202:900-911.
45. Idrissova L, Malhi H, Werneburg NW, LeBrasseur NK, Bronk SF, Fingas C, Tchkonia T, Pirtskhalava T, White TA, Stout MB, Hirsova P, Krishnan A, Liedtke C, Trautwein C, Finnberg N, El-Deiry WS, et al. TRAIL receptor deletion in mice suppresses the inflammation of nutrient excess. Journal of hepatology. 2015; 62:1156-1163.
46. Lunemann JD, Waiczies S, Ehrlich S, Wendling U, Seeger B, Kamradt T, Zipp F. Death ligand TRAIL induces no apoptosis but inhibits activation of human (auto)antigenspecific T cells. J Immunol. 2002; 168:4881-4888.
47. Secchiero P, Corallini F, di Iasio MG, Gonelli A, Barbarotto E, Zauli G. TRAIL counteracts the proadhesive activity of inflammatory cytokines in endothelial cells by downmodulating CCL8 and CXCL10 chemokine expression and release. Blood. 2005; 105:3413-3419.
48. Secchiero P, Gonelli A, Mirandola P, Melloni E, Zamai L, Celeghini C, Milani D, Zauli G. Tumor necrosis factorrelated apoptosis-inducing ligand induces monocytic maturation of leukemic and normal myeloid precursors through a caspase-dependent pathway. Blood. 2002; 100:2421-2429.
49. Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature. 2013; 496:445-455.
50. Condamine T, Kumar V, Ramachandran IR, Youn JI, Celis E, Finnberg N, El-Deiry WS, Winograd R, Vonderheide RH, English NR, Knight SC, Yagita H, McCaffrey JC, Antonia S, Hockstein N, Witt R, et al. ER stress regulates myeloid-derived suppressor cell fate through TRAIL-Rmediated apoptosis. J Clin Invest. 2014; 124:2626-2639.
51. Wilson NS, Yang A, Yang B, Couto S, Stern H, Gogineni A, Pitti R, Marsters S, Weimer RM, Singh M, Ashkenazi A. Proapoptotic activation of death receptor 5 on tumor endothelial cells disrupts the vasculature and reduces tumor growth. Cancer Cell. 2012; 22:80-90.
52. Klemm F, Joyce JA. Microenvironmental regulation of therapeutic response in cancer. Trends in cell biology. 2015; 25:198-213.
53. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, Huhn RD, Song W, Li D, Sharp LL, Torigian DA, O'Dwyer PJ, Vonderheide RH. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science. 2011; 331:1612-1616.
54. Golden EB, Demaria S, SchiffPB, Chachoua A, Formenti SC. An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer. Cancer Immunol Res. 2013; 1:365-372.
55. Van Overmeire E, Stijlemans B, Heymann F, Keirsse J, Morias Y, Elkrim Y, Brys L, Abels C, Lahmar Q, Ergen C, Vereecke L, Tacke F, De Baetselier P, Van Ginderachter JA, Laoui D. M-CSF and GM-CSF Receptor Signaling Differentially Regulate Monocyte Maturation and Macrophage Polarization in the Tumor Microenvironment. Cancer Res. 2016; 76:35-42.
56. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010; 141:39-51.
57. Fulda S. Targeting apoptosis for anticancer therapy. Seminars in cancer biology. 2015; 31:84-88.
58. Lemke J, von Karstedt S, Zinngrebe J, Walczak H. Getting TRAIL back on track for cancer therapy. Cell death and differentiation. 2014; 21:1350-1364.
59. Secchiero P, Gonelli A, Celeghini C, Mirandola P, Guidotti L, Visani G, Capitani S, Zauli G. Activation of the nitric oxide synthase pathway represents a key component of tumor necrosis factor-related apoptosis-inducing ligandmediated cytotoxicity on hematologic malignancies. Blood. 2001; 98:2220-2228.
60. Amm HM, Oliver PG, Lee CH, Li Y, Buchsbaum DJ. Combined modality therapy with TRAIL or agonistic death receptor antibodies. Cancer biology & therapy. 2011; 11:431-449.
61. Dai X, Zhang J, Arfuso F, Chinnathambi A, Zayed ME, Alharbi SA, Kumar AP, Ahn KS, Sethi G. Targeting TNF-related apoptosis-inducing ligand (TRAIL) receptor by natural products as a potential therapeutic approach for cancer therapy. Exp Biol Med (Maywood). 2015; 240:760-773.
62. Clancy L, Mruk K, Archer K, Woelfel M, Mongkolsapaya J, Screaton G, Lenardo MJ, Chan FK. Preligand assembly domain-mediated ligand-independent association between TRAIL receptor 4 (TR4) and TR2 regulates TRAILinduced apoptosis. Proc Natl Acad Sci U S A. 2005; 102:18099-18104.
63. Lim SC, Duong HQ, Choi JE, Lee TB, Kang JH, Oh SH, Han SI. Lipid raft-dependent death receptor 5 (DR5) expression and activation are critical for ursodeoxycholic acid-induced apoptosis in gastric cancer cells. Carcinogenesis. 2011; 32:723-731.
64. Allavena P, Signorelli M, Chieppa M, Erba E, Bianchi G, Marchesi F, Olimpio CO, Bonardi C, Garbi A, Lissoni A, de Braud F, Jimeno J, D'Incalci M. Anti-inflammatory properties of the novel antitumor agent yondelis (trabectedin): inhibition of macrophage differentiation and cytokine production. Cancer Res. 2005; 65:2964-2971.