Myc Cooperates with Ras by Programming Inflammation and Immune Suppression

Cell

Volumn 171, Issue 6, 2017, Pages 1301-1315.e14

  Kortlever, Roderik M ^a,b   Sodir, Nicole M ^a,b   Wilson, Catherine H ^a   Burkhart, Deborah L ^a   Pellegrinet, Luca ^a   Brown Swigart, Lamorna ^b   Littlewood, Trevor D ^a   Evan, Gerard I ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CCL9; IL 23; immune suppression; inflammation; lung cancer; Myc; NK cells; oncogene cooperation; Ras; tumor microenvironment

Indexed keywords

CHEMOKINE; CHEMOKINE CCL9; INTERLEUKIN 23; PROGRAMMED DEATH 1 LIGAND 1; UNCLASSIFIED DRUG; BETA CHEMOKINE; CCL9 PROTEIN, MOUSE; KRAS2 PROTEIN, MOUSE; MACROPHAGE INFLAMMATORY PROTEIN; MYC PROTEIN; MYC PROTEIN, MOUSE; PROTEIN P21;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; INFLAMMATION; LUNG ADENOCARCINOMA; LUNG CARCINOGENESIS; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; ONCOGENE K RAS; ONCOGENE MYC; ONCOGENE RAS; PRIORITY JOURNAL; STROMA; T LYMPHOCYTE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ADENOCARCINOMA; ADENOMA; ANIMAL; CARCINOGENESIS; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; LUNG TUMOR; MALE; METABOLISM; PATHOLOGY;

ADENOCARCINOMA; ADENOMA; ANIMALS; CARCINOGENESIS; CHEMOKINES, CC; DISEASE MODELS, ANIMAL; FEMALE; INFLAMMATION; INTERLEUKIN-23; LUNG NEOPLASMS; MACROPHAGE INFLAMMATORY PROTEINS; MACROPHAGES; MALE; MICE; PROTO-ONCOGENE PROTEINS C-MYC; PROTO-ONCOGENE PROTEINS P21(RAS); TUMOR MICROENVIRONMENT;

EID: 85036636976     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.11.013     Document Type: Article

References (80)

1. Aggarwal, N.R., King, L.S., D'Alessio, F.R., Diverse macrophage populations mediate acute lung inflammation and resolution. Am. J. Physiol. Lung Cell. Mol. Physiol. 306 (2014), L709–L725.
2. Alexander, W.S., Adams, J.M., Cory, S., Oncogene cooperation in lymphocyte transformation: malignant conversion of E mu-myc transgenic pre-B cells in vitro is enhanced by v-H-ras or v-raf but not v-abl. Mol. Cell. Biol. 9 (1989), 67–73.
3. Ancrile, B.B., O'Hayer, K.M., Counter, C.M., Oncogenic ras-induced expression of cytokines: a new target of anti-cancer therapeutics. Mol. Interv. 8 (2008), 22–27.
4. Andres, A.C., van der Valk, M.A., Schönenberger, C.A., Flückiger, F., LeMeur, M., Gerlinger, P., Groner, B., Ha-ras and c-myc oncogene expression interferes with morphological and functional differentiation of mammary epithelial cells in single and double transgenic mice. Genes Dev. 2 (1988), 1486–1495.
5. Bailey, S.R., Nelson, M.H., Himes, R.A., Li, Z., Mehrotra, S., Paulos, C.M., Th17 cells in cancer: the ultimate identity crisis. Front. Immunol., 5, 2014, 276.
6. Baird, A.-M., Leonard, J., Naicker, K.M., Kilmartin, L., O'Byrne, K.J., Gray, S.G., IL-23 is pro-proliferative, epigenetically regulated and modulated by chemotherapy in non-small cell lung cancer. Lung Cancer 79 (2013), 83–90.
7. Born, T.L., Frost, J.A., Schönthal, A., Prendergast, G.C., Feramisco, J.R., c-Myc cooperates with activated Ras to induce the cdc2 promoter. Mol. Cell. Biol. 14 (1994), 5710–5718.
8. Boxer, R.B., Jang, J.W., Sintasath, L., Chodosh, L.A., Lack of sustained regression of c-MYC-induced mammary adenocarcinomas following brief or prolonged MYC inactivation. Cancer Cell 6 (2004), 577–586.
9. Brekken, R.A., Huang, X., King, S.W., Thorpe, P.E., Vascular endothelial growth factor as a marker of tumor endothelium. Cancer Res. 58 (1998), 1952–1959.
10. Campbell, P.M., Der, C.J., Oncogenic Ras and its role in tumor cell invasion and metastasis. Semin. Cancer Biol. 14 (2004), 105–114.
11. Casey, S.C., Tong, L., Li, Y., Do, R., Walz, S., Fitzgerald, K.N., Gouw, A.M., Baylot, V., Gütgemann, I., Eilers, M., Felsher, D.W., MYC regulates the antitumor immune response through CD47 and PD-L1. Science 352 (2016), 227–231.
12. Chang, S.H., Tumorigenic Th17 cells in oncogenic Kras-driven and inflammation-accelerated lung cancer. OncoImmunology, 4, 2015, e955704.
13. Chang, S.H., Mirabolfathinejad, S.G., Katta, H., Cumpian, A.M., Gong, L., Caetano, M.S., Moghaddam, S.J., Dong, C., T helper 17 cells play a critical pathogenic role in lung cancer. Proc. Natl. Acad. Sci. USA 111 (2014), 5664–5669.
14. Chanmee, T., Ontong, P., Konno, K., Itano, N., Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel) 6 (2014), 1670–1690.
15. Christophorou, M.A., Martin-Zanca, D., Soucek, L., Lawlor, E.R., Brown-Swigart, L., Verschuren, E.W., Evan, G.I., Temporal dissection of p53 function in vitro and in vivo. Nat. Genet. 37 (2005), 718–726.
16. Compere, S.J., Baldacci, P., Sharpe, A.H., Thompson, T., Land, H., Jaenisch, R., The ras and myc oncogenes cooperate in tumor induction in many tissues when introduced into midgestation mouse embryos by retroviral vectors. Proc. Natl. Acad. Sci. USA 86 (1989), 2224–2228.
17. Cox, A.D., Der, C.J., The dark side of Ras: regulation of apoptosis. Oncogene 22 (2003), 8999–9006.
18. D'Alessio, F.R., Tsushima, K., Aggarwal, N.R., West, E.E., Willett, M.H., Britos, M.F., Pipeling, M.R., Brower, R.G., Tuder, R.M., McDyer, J.F., King, L.S., CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J. Clin. Invest. 119 (2009), 2898–2913.
19. Dang, C.V., MYC, metabolism, cell growth, and tumorigenesis. Cold Spring Harb. Perspect. Med., 3, 2013.
20. Dong, J., Sutor, S., Jiang, G., Cao, Y., Asmann, Y.W., Wigle, D.A., c-Myc regulates self-renewal in bronchoalveolar stem cells. PLoS ONE, 6, 2011, e23707.
21. Evan, G., Littlewood, T., A matter of life and cell death. Science 281 (1998), 1317–1322.
22. Fasbender, A., Lee, J.H., Walters, R.W., Moninger, T.O., Zabner, J., Welsh, M.J., Incorporation of adenovirus in calcium phosphate precipitates enhances gene transfer to airway epithelia in vitro and in vivo. J. Clin. Invest. 102 (1998), 184–193.
23. Fridman, W.H., Pagès, F., Sautès-Fridman, C., Galon, J., The immune contexture in human tumours: impact on clinical outcome. Nat. Rev. Cancer 12 (2012), 298–306.
24. Gaffen, S.L., Jain, R., Garg, A.V., Cua, D.J., The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat. Rev. Immunol. 14 (2014), 585–600.
25. Goc, J., Fridman, W.H., Sautès-Fridman, C., Dieu-Nosjean, M.-C., Characteristics of tertiary lymphoid structures in primary cancers. OncoImmunology, 2, 2013, e26836.
26. Graziano, S.L., Gamble, G.P., Newman, N.B., Abbott, L.Z., Rooney, M., Mookherjee, S., Lamb, M.L., Kohman, L.J., Poiesz, B.J., Prognostic significance of K-ras codon 12 mutations in patients with resected stage I and II non-small-cell lung cancer. J. Clin. Oncol. 17 (1999), 668–675.
27. Igarashi, T., Teramoto, K., Ishida, M., Hanaoka, J., Daigo, Y., Scoring of PD-L1 expression intensity on pulmonary adenocarcinomas and the correlations with clinicopathological factors. ESMO Open, 1, 2016, e000083.
28. Ischenko, I., Zhi, J., Moll, U.M., Nemajerova, A., Petrenko, O., Direct reprogramming by oncogenic Ras and Myc. Proc. Natl. Acad. Sci. USA 110 (2013), 3937–3942.
29. Iwakawa, R., Kohno, T., Kato, M., Shiraishi, K., Tsuta, K., Noguchi, M., Ogawa, S., Yokota, J., MYC amplification as a prognostic marker of early-stage lung adenocarcinoma identified by whole genome copy number analysis. Clin. Cancer Res. 17 (2011), 1481–1489.
30. Jackson, E.L., Willis, N., Mercer, K., Bronson, R.T., Crowley, D., Montoya, R., Jacks, T., Tuveson, D.A., Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15 (2001), 3243–3248.
31. Ji, H., Houghton, A.M., Mariani, T.J., Perera, S., Kim, C.B., Padera, R., Tonon, G., McNamara, K., Marconcini, L.A., Hezel, A., et al. K-ras activation generates an inflammatory response in lung tumors. Oncogene 25 (2006), 2105–2112.
32. Joshi, N.S., Akama-Garren, E.H., Lu, Y., Lee, D.-Y., Chang, G.P., Li, A., DuPage, M., Tammela, T., Kerper, N.R., Farago, A.F., et al. Regulatory T Cells in Tumor-Associated Tertiary Lymphoid Structures Suppress Anti-tumor T Cell Responses. Immunity 43 (2015), 579–590.
33. Karin, M., Inflammation and cancer: the long reach of Ras. Nat. Med. 11 (2005), 20–21.
34. Kauffmann-Zeh, A., Rodriguez-Viciana, P., Ulrich, E., Gilbert, C., Coffer, P., Downward, J., Evan, G., Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 385 (1997), 544–548.
35. Kimmelman, A.C., Metabolic Dependencies in RAS-Driven Cancers. Clin. Cancer Res. 21 (2015), 1828–1834.
36. Kitamura, T., Kometani, K., Hashida, H., Matsunaga, A., Miyoshi, H., Hosogi, H., Aoki, M., Oshima, M., Hattori, M., Takabayashi, A., et al. SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion. Nat. Genet. 39 (2007), 467–475.
37. Kitamura, T., Qian, B.-Z., Soong, D., Cassetta, L., Noy, R., Sugano, G., Kato, Y., Li, J., Pollard, J.W., CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J. Exp. Med. 212 (2015), 1043–1059.
38. Koizumi, K., Hojo, S., Akashi, T., Yasumoto, K., Saiki, I., Chemokine receptors in cancer metastasis and cancer cell-derived chemokines in host immune response. Cancer Sci. 98 (2007), 1652–1658.
39. Kranenburg, O., Gebbink, M.F.B.G., Voest, E.E., Stimulation of angiogenesis by Ras proteins. Biochim. Biophys. Acta 1654 (2004), 23–37.
40. Land, H., Parada, L.F., Weinberg, R.A., Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304 (1983), 596–602.
41. Langowski, J.L., Zhang, X., Wu, L., Mattson, J.D., Chen, T., Smith, K., Basham, B., McClanahan, T., Kastelein, R.A., Oft, M., IL-23 promotes tumour incidence and growth. Nature 442 (2006), 461–465.
42. Leone, G., DeGregori, J., Sears, R., Jakoi, L., Nevins, J.R., Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature 387 (1997), 422–426.
43. Littlewood, T.D., Hancock, D.C., Danielian, P.S., Parker, M.G., Evan, G.I., A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23 (1995), 1686–1690.
44. Martinez, F.O., Gordon, S., The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep., 6, 2014, 13.
45. Morvan, M.G., Lanier, L.L., NK cells and cancer: you can teach innate cells new tricks. Nat. Rev. Cancer 16 (2016), 7–19.
46. Murphy, D.J., Junttila, M.R., Pouyet, L., Karnezis, A., Shchors, K., Bui, D.A., Brown-Swigart, L., Johnson, L., Evan, G.I., Distinct thresholds govern Myc's biological output in vivo. Cancer Cell 14 (2008), 447–457.
47. Ngiow, S.F., Teng, M.W.L., Smyth, M.J., A balance of interleukin-12 and -23 in cancer. Trends Immunol. 34 (2013), 548–555.
48. Pelengaris, S., Khan, M., Evan, G.I., Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 109 (2002), 321–334.
49. Podsypanina, K., Politi, K., Beverly, L.J., Varmus, H.E., Oncogene cooperation in tumor maintenance and tumor recurrence in mouse mammary tumors induced by Myc and mutant Kras. Proc. Natl. Acad. Sci. USA 105 (2008), 5242–5247.
50. Pollard, J.W., Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4 (2004), 71–78.
51. Rapp, U.R., Korn, C., Ceteci, F., Karreman, C., Luetkenhaus, K., Serafin, V., Zanucco, E., Castro, I., Potapenko, T., MYC is a metastasis gene for non-small-cell lung cancer. PLoS ONE, 4, 2009, e6029.
52. Restifo, N.P., Can antitumor immunity help to explain “oncogene addiction”?. Cancer Cell 18 (2010), 403–405.
53. Riabov, V., Gudima, A., Wang, N., Mickley, A., Orekhov, A., Kzhyshkowska, J., Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis. Front. Physiol., 5, 2014, 75.
54. Richardson, G.E., Johnson, B.E., The biology of lung cancer. Semin. Oncol. 20 (1993), 105–127.
55. Rodenhuis, S., Slebos, R.J., Boot, A.J., Evers, S.G., Mooi, W.J., Wagenaar, S.S., van Bodegom, P.C., Bos, J.L., Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res. 48 (1988), 5738–5741.
56. Rőszer, T., Understanding the Mysterious M2 Macrophage through Activation Markers and Effector Mechanisms. Mediators Inflamm., 2015, 2015, 816460.
57. Sears, R., Nuckolls, F., Haura, E., Taya, Y., Tamai, K., Nevins, J.R., Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev. 14 (2000), 2501–2514.
58. Seo, A.N., Yang, J.M., Kim, H., Jheon, S., Kim, K., Lee, C.T., Jin, Y., Yun, S., Chung, J.H., Paik, J.H., Clinicopathologic and prognostic significance of c-MYC copy number gain in lung adenocarcinomas. Br. J. Cancer 110 (2014), 2688–2699.
59. Sharma, S.V., Gajowniczek, P., Way, I.P., Lee, D.Y., Jiang, J., Yuza, Y., Classon, M., Haber, D.A., Settleman, J., A common signaling cascade may underlie “addiction” to the Src, BCR-ABL, and EGF receptor oncogenes. Cancer Cell 10 (2006), 425–435.
60. Shchors, K., Shchors, E., Rostker, F., Lawlor, E.R., Brown-Swigart, L., Evan, G.I., The Myc-dependent angiogenic switch in tumors is mediated by interleukin 1beta. Genes Dev. 20 (2006), 2527–2538.
61. Sodir, N.M., Swigart, L.B., Karnezis, A.N., Hanahan, D., Evan, G.I., Soucek, L., Endogenous Myc maintains the tumor microenvironment. Genes Dev. 25 (2011), 907–916.
62. Soucek, L., Whitfield, J., Martins, C.P., Finch, A.J., Murphy, D.J., Sodir, N.M., Karnezis, A.N., Swigart, L.B., Nasi, S., Evan, G.I., Modelling Myc inhibition as a cancer therapy. Nature 455 (2008), 679–683.
63. Soucek, L., Whitfield, J.R., Sodir, N.M., Massó-Vallés, D., Serrano, E., Karnezis, A.N., Swigart, L.B., Evan, G.I., Inhibition of Myc family proteins eradicates KRas-driven lung cancer in mice. Genes Dev. 27 (2013), 504–513.
64. Sparmann, A., Bar-Sagi, D., Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 6 (2004), 447–458.
65. Stenhouse, G., Fyfe, N., King, G., Chapman, A., Kerr, K.M., Thyroid transcription factor 1 in pulmonary adenocarcinoma. J. Clin. Pathol. 57 (2004), 383–387.
66. Sunaga, N., Imai, H., Shimizu, K., Shames, D.S., Kakegawa, S., Girard, L., Sato, M., Kaira, K., Ishizuka, T., Gazdar, A.F., et al. Oncogenic KRAS-induced interleukin-8 overexpression promotes cell growth and migration and contributes to aggressive phenotypes of non-small cell lung cancer. Int. J. Cancer 130 (2012), 1733–1744.
67. Teng, M.W.L., Andrews, D.M., McLaughlin, N., von Scheidt, B., Ngiow, S.F., Möller, A., Hill, G.R., Iwakura, Y., Oft, M., Smyth, M.J., IL-23 suppresses innate immune response independently of IL-17A during carcinogenesis and metastasis. Proc. Natl. Acad. Sci. USA 107 (2010), 8328–8333.
68. Teng, M.W.L., Vesely, M.D., Duret, H., McLaughlin, N., Towne, J.E., Schreiber, R.D., Smyth, M.J., Opposing roles for IL-23 and IL-12 in maintaining occult cancer in an equilibrium state. Cancer Res. 72 (2012), 3987–3996.
69. Töpfer, K., Kempe, S., Müller, N., Schmitz, M., Bachmann, M., Cartellieri, M., Schackert, G., Temme, A., Tumor evasion from T cell surveillance. J. Biomed. Biotechnol., 2011, 2011, 918471.
70. Tran, P.T., Fan, A.C., Bendapudi, P.K., Koh, S., Komatsubara, K., Chen, J., Horng, G., Bellovin, D.I., Giuriato, S., Wang, C.S., et al. Combined Inactivation of MYC and K-Ras oncogenes reverses tumorigenesis in lung adenocarcinomas and lymphomas. PLoS ONE, 3, 2008, e2125.
71. Tran, P.T., Bendapudi, P.K., Lin, H.J., Choi, P., Koh, S., Chen, J., Horng, G., Hughes, N.P., Schwartz, L.H., Miller, V.A., et al. Survival and death signals can predict tumor response to therapy after oncogene inactivation. Sci. Transl. Med., 3, 2011, 103ra199.
72. Tsuneoka, M., Mekada, E., Ras/MEK signaling suppresses Myc-dependent apoptosis in cells transformed by c-myc and activated ras. Oncogene 19 (2000), 115–123.
73. Vaqué J.P., Navascues, J., Shiio, Y., Laiho, M., Ajenjo, N., Mauleon, I., Matallanas, D., Crespo, P., León, J., Myc antagonizes Ras-mediated growth arrest in leukemia cells through the inhibition of the Ras-ERK-p21Cip1 pathway. J. Biol. Chem. 280 (2005), 1112–1122.
74. Wang, C., Lisanti, M.P., Liao, D.J., Reviewing once more the c-myc and Ras collaboration: converging at the cyclin D1-CDK4 complex and challenging basic concepts of cancer biology. Cell Cycle 10 (2011), 57–67.
75. White, G.E., Iqbal, A.J., Greaves, D.R., CC chemokine receptors and chronic inflammation–therapeutic opportunities and pharmacological challenges. Pharmacol. Rev. 65 (2013), 47–89.
76. Wilson, C.H., Gamper, I., Perfetto, A., Auw, J., Littlewood, T.D., Evan, G.I., The kinetics of ER fusion protein activation in vivo. Oncogene 33 (2014), 4877–4880.
77. Wolfer, A., Wittner, B.S., Irimia, D., Flavin, R.J., Lupien, M., Gunawardane, R.N., Meyer, C.A., Lightcap, E.S., Tamayo, P., Mesirov, J.P., et al. MYC regulation of a “poor-prognosis” metastatic cancer cell state. Proc. Natl. Acad. Sci. USA 107 (2010), 3698–3703.
78. Wu, Q., Gardiner, G.J., Berry, E., Wagner, S.R., Lu, T., Clay, B.S., Moore, T.V., Ferreira, C.M., Williams, J.W., Luster, A.D., et al. ICOS-expressing lymphocytes promote resolution of CD8-mediated lung injury in a mouse model of lung rejection. PLoS ONE, 8, 2013, e72955.
79. Wynn, T.A., Vannella, K.M., Macrophages in Tissue Repair, Regeneration, and Fibrosis. Immunity 44 (2016), 450–462.
80. Yaari, S., Jacob-Hirsch, J., Amariglio, N., Haklai, R., Rechavi, G., Kloog, Y., Disruption of cooperation between Ras and MycN in human neuroblastoma cells promotes growth arrest. Clin. Cancer Res. 11 (2005), 4321–4330.