TNF Counterbalances the Emergence of M2 Tumor Macrophages

Cell Reports

Volumn 12, Issue 11, 2015, Pages 1902-1914

  Kratochvill, Franz ^a   Neale, Geoffrey ^a   Haverkamp, Jessica M ^a   Van de Velde, Lee Ann ^a   Smith, Amber M ^a   Kawauchi, Daisuke ^a   McEvoy, Justina ^a,b   Roussel, Martine F ^a   Dyer, Michael A ^a   Qualls, Joseph E ^a,c   Murray, Peter J ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; MESSENGER RNA; STAT6 PROTEIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CELL POLARITY; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; MONOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; TUMOR NECROSIS FACTOR GENE; ANIMAL; C57BL MOUSE; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; NEOPLASM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84942833116     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.033     Document Type: Article

References (65)

1. Ahn G.O., Tseng D., Liao C.H., Dorie M.J., Czechowicz A., Brown J.M. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc. Natl. Acad. Sci. USA 2010, 107:8363-8368.
2. Alsina L., Israelsson E., Altman M.C., Dang K.K., Ghandil P., Israel L., von Bernuth H., Baldwin N., Qin H., Jin Z., et al. A narrow repertoire of transcriptional modules responsive to pyogenic bacteria is impaired in patients carrying loss-of-function mutations in MYD88 or IRAK4. Nat. Immunol. 2014, 15:1134-1142.
3. Bain C.C., Mowat A.M. Macrophages in intestinal homeostasis and inflammation. Immunol. Rev. 2014, 260:102-117.
4. Bain C.C., Scott C.L., Uronen-Hansson H., Gudjonsson S., Jansson O., Grip O., Guilliams M., Malissen B., Agace W.W., Mowat A.M. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol. 2013, 6:498-510.
5. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 2011, 17:320-329.
6. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
7. Biswas S.K., Gangi L., Paul S., Schioppa T., Saccani A., Sironi M., Bottazzi B., Doni A., Vincenzo B., Pasqualini F., et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood 2006, 107:2112-2122.
8. Bonapace L., Coissieux M.M., Wyckoff J., Mertz K.D., Varga Z., Junt T., Bentires-Alj M. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature 2014, 515:130-133.
9. Carretero R., Sektioglu I.M., Garbi N., Salgado O.C., Beckhove P., Hämmerling G.J. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nat. Immunol. 2015, 16:609-617.
10. Chen F., Wu W., Millman A., Craft J.F., Chen E., Patel N., Boucher J.L., Urban J.F., Kim C.C., Gause W.C. Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat. Immunol. 2014, 15:938-946.
11. Chittezhath M., Dhillon M.K., Lim J.Y., Laoui D., Shalova I.N., Teo Y.L., Chen J., Kamaraj R., Raman L., Lum J., et al. Molecular profiling reveals a tumor-promoting phenotype of monocytes and macrophages in human cancer progression. Immunity 2014, 41:815-829.
12. Colegio O.R., Chu N.Q., Szabo A.L., Chu T., Rhebergen A.M., Jairam V., Cyrus N., Brokowski C.E., Eisenbarth S.C., Phillips G.M., et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 2014, 513:559-563.
13. Cortez-Retamozo V., Etzrodt M., Newton A., Rauch P.J., Chudnovskiy A., Berger C., Ryan R.J., Iwamoto Y., Marinelli B., Gorbatov R., et al. Origins of tumor-associated macrophages and neutrophils. Proc. Natl. Acad. Sci. USA 2012, 109:2491-2496.
14. Dannenmann S.R., Thielicke J., Stöckli M., Matter C., von Boehmer L., Cecconi V., Hermanns T., Hefermehl L., Schraml P., Moch H., et al. Tumor-associated macrophages subvert T-cell function and correlate with reduced survival in clear cell renal cell carcinoma. OncoImmunology 2013, 2:e23562.
15. De Palma M., Lewis C.E. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 2013, 23:277-286.
16. Dvorak H.F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 1986, 315:1650-1659.
17. El Kasmi K.C., Qualls J.E., Pesce J.T., Smith A.M., Thompson R.W., Henao-Tamayo M., Basaraba R.J., König T., Schleicher U., Koo M.S., et al. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol. 2008, 9:1399-1406.
18. El Kasmi K.C., Pugliese S.C., Riddle S.R., Poth J.M., Anderson A.L., Frid M.G., Li M., Pullamsetti S.S., Savai R., Nagel M.A., et al. Adventitial fibroblasts induce a distinct proinflammatory/profibrotic macrophage phenotype in pulmonary hypertension. J. Immunol. 2014, 193:597-609.
19. Elpek K.G., Cremasco V., Shen H., Harvey C.J., Wucherpfennig K.W., Goldstein D.R., Monach P.A., Turley S.J. The tumor microenvironment shapes lineage, transcriptional, and functional diversity of infiltrating myeloid cells. Cancer Immunol. Res. 2014, 2:655-667.
20. Epelman S., Lavine K.J., Randolph G.J. Origin and functions of tissue macrophages. Immunity 2014, 41:21-35.
21. Farlik M., Reutterer B., Schindler C., Greten F., Vogl C., Müller M., Decker T. Nonconventional initiation complex assembly by STAT and NF-kappaB transcription factors regulates nitric oxide synthase expression. Immunity 2010, 33:25-34.
22. Flynn J.L., Goldstein M.M., Chan J., Triebold K.J., Pfeffer K., Lowenstein C.J., Schreiber R., Mak T.W., Bloom B.R. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 1995, 2:561-572.
23. Franklin R.A., Liao W., Sarkar A., Kim M.V., Bivona M.R., Liu K., Pamer E.G., Li M.O. The cellular and molecular origin of tumor-associated macrophages. Science 2014, 344:921-925.
24. Fridman W.H., Pagès F., Sautès-Fridman C., Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat. Rev. Cancer 2012, 12:298-306.
25. Gajewski T.F., Schreiber H., Fu Y.X. Innate and adaptive immune cells in the tumor microenvironment. Nat. Immunol. 2013, 14:1014-1022.
26. Galon J., Angell H.K., Bedognetti D., Marincola F.M. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013, 39:11-26.
27. Hagemann T., Lawrence T., McNeish I., Charles K.A., Kulbe H., Thompson R.G., Robinson S.C., Balkwill F.R. "Re-educating" tumor-associated macrophages by targeting NF-kappaB. J. Exp. Med. 2008, 205:1261-1268.
28. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
29. Haverkamp J.M., Smith A.M., Weinlich R., Dillon C.P., Qualls J.E., Neale G., Koss B., Kim Y., Bronte V., Herold M.J., et al. Myeloid-derived suppressor activity is mediated by monocytic lineages maintained by continuous inhibition of extrinsic and intrinsic death pathways. Immunity 2014, 41:947-959.
30. Huber S., Hoffmann R., Muskens F., Voehringer D. Alternatively activated macrophages inhibit T-cell proliferation by Stat6-dependent expression of PD-L2. Blood 2010, 116:3311-3320.
31. Kawauchi D., Robinson G., Uziel T., Gibson P., Rehg J., Gao C., Finkelstein D., Qu C., Pounds S., Ellison D.W., et al. A mouse model of the most aggressive subgroup of human medulloblastoma. Cancer Cell 2012, 21:168-180.
32. +/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 2013, 24:589-602.
33. Kratochvill F., Gratz N., Qualls J.E., Van De Velde L.A., Chi H., Kovarik P., Murray P.J. Tristetraprolin limits inflammatory cytokine production in tumor-associated macrophages in an mRNA decay-independent manner. Cancer Res. 2015, 75:3054-3064.
34. Lee J.J., Jacobsen E.A., Ochkur S.I., McGarry M.P., Condjella R.M., Doyle A.D., Luo H., Zellner K.R., Protheroe C.A., Willetts L., et al. Human versus mouse eosinophils: "that which we call an eosinophil, by any other name would stain as red". J. Allergy Clin. Immunol. 2012, 130:572-584.
35. Liang H.E., Reinhardt R.L., Bando J.K., Sullivan B.M., Ho I.C., Locksley R.M. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat. Immunol. 2012, 13:58-66.
36. Lumeng C.N., Bodzin J.L., Saltiel A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117:175-184.
37. Ma Y., Adjemian S., Mattarollo S.R., Yamazaki T., Aymeric L., Yang H., Portela Catani J.P., Hannani D., Duret H., Steegh K., et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013, 38:729-741.
38. Movahedi K., Laoui D., Gysemans C., Baeten M., Stangé G., Van den Bossche J., Mack M., Pipeleers D., In't Veld P., De Baetselier P., Van Ginderachter J.A. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010, 70:5728-5739.
39. Murray P.J., Wynn T.A. Obstacles and opportunities for understanding macrophage polarization. J. Leukoc. Biol. 2011, 89:557-563.
40. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11:723-737.
41. Murray P.J., Allen J.E., Biswas S.K., Fisher E.A., Gilroy D.W., Goerdt S., Gordon S., Hamilton J.A., Ivashkiv L.B., Lawrence T., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014, 41:14-20.
42. Nakasone E.S., Askautrud H.A., Kees T., Park J.H., Plaks V., Ewald A.J., Fein M., Rasch M.G., Tan Y.X., Qiu J., et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 2012, 21:488-503.
43. Nathan C., Ding A. Nonresolving inflammation. Cell 2010, 140:871-882.
44. O'Sullivan T., Saddawi-Konefka R., Vermi W., Koebel C.M., Arthur C., White J.M., Uppaluri R., Andrews D.M., Ngiow S.F., Teng M.W., et al. Cancer immunoediting by the innate immune system in the absence of adaptive immunity. J. Exp. Med. 2012, 209:1869-1882.
45. Orr J.S., Puglisi M.J., Ellacott K.L., Lumeng C.N., Wasserman D.H., Hasty A.H. Toll-like receptor 4 deficiency promotes the alternative activation of adipose tissue macrophages. Diabetes 2012, 61:2718-2727.
46. Potian J.A., Rafi W., Bhatt K., McBride A., Gause W.C., Salgame P. Preexisting helminth infection induces inhibition of innate pulmonary anti-tuberculosis defense by engaging the IL-4 receptor pathway. J. Exp. Med. 2011, 208:1863-1874.
47. Predina J., Eruslanov E., Judy B., Kapoor V., Cheng G., Wang L.C., Sun J., Moon E.K., Fridlender Z.G., Albelda S., Singhal S. Changes in the local tumor microenvironment in recurrent cancers may explain the failure of vaccines after surgery. Proc. Natl. Acad. Sci. USA 2013, 110:E415-E424.
48. Pyonteck S.M., Akkari L., Schuhmacher A.J., Bowman R.L., Sevenich L., Quail D.F., Olson O.C., Quick M.L., Huse J.T., Teijeiro V., et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat. Med. 2013, 19:1264-1272.
49. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
50. Qiu Y., Nguyen K.D., Odegaard J.I., Cui X., Tian X., Locksley R.M., Palmiter R.D., Chawla A. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 2014, 157:1292-1308.
51. Ries C.H., Cannarile M.A., Hoves S., Benz J., Wartha K., Runza V., Rey-Giraud F., Pradel L.P., Feuerhake F., Klaman I., et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 2014, 25:846-859.
52. Ruffell B., Affara N.I., Coussens L.M. Differential macrophage programming in the tumor microenvironment. Trends Immunol. 2012, 33:119-126.
53. Sanjabi S., Hoffmann A., Liou H.C., Baltimore D., Smale S.T. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc. Natl. Acad. Sci. USA 2000, 97:12705-12710.
54. Sen R., Smale S.T. Selectivity of the NF-κB response. Cold Spring Harb. Perspect. Biol. 2010, 2:a000257.
55. Shand F.H., Ueha S., Otsuji M., Koid S.S., Shichino S., Tsukui T., Kosugi-Kanaya M., Abe J., Tomura M., Ziogas J., Matsushima K. Tracking of intertissue migration reveals the origins of tumor-infiltrating monocytes. Proc. Natl. Acad. Sci. USA 2014, 111:7771-7776.
56. Tundup S., Srivastava L., Nagy T., Harn D. CD14 influences host immune responses and alternative activation of macrophages during Schistosoma mansoni infection. Infect. Immun. 2014, 82:3240-3251.
57. Vos A.C., Wildenberg M.E., Duijvestein M., Verhaar A.P., van den Brink G.R., Hommes D.W. Anti-tumor necrosis factor-α antibodies induce regulatory macrophages in an Fc region-dependent manner. Gastroenterology 2011, 140:221-230.
58. Vos A.C., Wildenberg M.E., Arijs I., Duijvestein M., Verhaar A.P., de Hertogh G., Vermeire S., Rutgeerts P., van den Brink G.R., Hommes D.W. Regulatory macrophages induced by infliximab are involved in healing in vivo and in vitro. Inflamm. Bowel Dis. 2012, 18:401-408.
59. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112:1796-1808.
60. Weiss W.A., Aldape K., Mohapatra G., Feuerstein B.G., Bishop J.M. Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J. 1997, 16:2985-2995.
61. Wynn T.A., Chawla A., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496:445-455.
62. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., Sole J., Nichols A., Ross J.S., Tartaglia L.A., Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 2003, 112:1821-1830.
63. Yu M., Zhou H., Zhao J., Xiao N., Roychowdhury S., Schmitt D., Hu B., Ransohoff R.M., Harding C.V., Hise A.G., et al. MyD88-dependent interplay between myeloid and endothelial cells in the initiation and progression of obesity-associated inflammatory diseases. J. Exp. Med. 2014, 211:887-907.
64. Zhang Q.W., Liu L., Gong C.Y., Shi H.S., Zeng Y.H., Wang X.Z., Zhao Y.W., Wei Y.Q. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS ONE 2012, 7:e50946.
65. Zhou L., Nazarian A.A., Smale S.T. Interleukin-10 inhibits interleukin-12 p40 gene transcription by targeting a late event in the activation pathway. Mol. Cell. Biol. 2004, 24:2385-2396.