Control of PD-L1 expression by oncogenic activation of the AKT-mTOR pathway in non-small cell lung cancer

Cancer Research

Volumn 76, Issue 2, 2016, Pages 227-238

  Lastwika, Kristin J ^a,b   Wilson, Willie ^c   Li, Qing Kay ^a   Norris, Jeffrey ^a   Xu, Haiying ^d   Ghazarian, Sharon R ^d   Kitagawa, Hiroshi ^a   Kawabata, Shigeru ^a   Taube, Janis M ^d   Yao, Sheng ^e   Liu, Linda N ^e   Gills, Joell J ^a   Dennis, Phillip A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e Amplimmune Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA INTERFERON; K RAS PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PROGRAMMED DEATH 1 ANTIBODY; PROGRAMMED DEATH 1 LIGAND 1; PROTEIN KINASE B; RAPAMYCIN; UNCLASSIFIED DRUG; MTOR PROTEIN, HUMAN; ONCOPROTEIN; PROGRAMMED DEATH 1 RECEPTOR; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ADENOCARCINOMA; LUNG CARCINOGENESIS; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SQUAMOUS CELL LUNG CARCINOMA; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE; ANIMAL; GENETIC TRANSFECTION; GENETICS; LUNG TUMOR; METABOLISM; PATHOLOGY;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; HUMANS; LUNG NEOPLASMS; MICE; ONCOGENE PROTEIN V-AKT; PROGRAMMED CELL DEATH 1 RECEPTOR; TOR SERINE-THREONINE KINASES; TRANSFECTION;

EID: 84958963164     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3362     Document Type: Article

References (51)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014;64:9-29.
2. Memmott RM, Mercado JR, Maier CR, Kawabata S, Fox SD, Dennis PA. Metformin prevents tobacco carcinogen-induced lung tumorigenesis. Cancer Prev Res 2010;3:1066-76.
3. Granville CA, Warfel N, Tsurutani J, Hollander MC, Robertson M, Fox SD, et al. Identification of a highly effective rapamycin schedule that markedly reduces the size, multiplicity, and phenotypic progression of tobacco carcinogen-induced murine lung tumors. Clin Cancer Res 2007;13: 2281-9.
4. Hollander MC, Maier CR, Hobbs EA, Ashmore AR, Linnoila RI, Dennis PA. Akt1 deletion prevents lung tumorigenesis by mutant K-ras. Oncogene 2011;30:1812-21.
5. Granville CA,Memmott RM, Balogh A, Mariotti J, Kawabata S, HanW, et al. A central role for Foxp3+ regulatory T cells in K-Ras-driven lung tumorigenesis. PLoS ONE 2009;4:e5061.
6. Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 1999;5:1365-9.
7. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002;8:793-800.
8. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T-cell responses. Immunity 2007;27:111-22.
9. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermottDF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
10. Brahmer JR, Tykodi SS, Chow LQM, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
11. Lipson EJ, Sharfman WH, Drake CG, Wollner I, Taube JM, Anders RA, et al. Durable cancer regression off-treatment and effective reinduction therapy with an anti-PD-1 antibody. Clin Cancer Res 2013;19: 462-8.
12. Green MR, Monti S, Rodig SJ, Juszczynski P, Currie T, O'Donnell E, et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood 2010;116:3268-77.
13. Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci U S A 2008;105:20852-7.
14. Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med 2007;13:84-8.
15. Crane CA, Panner A, Murray JC, Wilson SP, Xu H, Chen L, et al. PI(3) kinase is associated with amechanism of immunoresistance in breast and prostate cancer. Oncogene 2009;28:306-12.
16. Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, et al. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov 2013;3:1355-63.
17. Xu C, Fillmore CM, Koyama S, Wu H, Zhao Y, Chen Z, et al. Loss of Lkb1 and Pten leads to lung squamous cell carcinoma with elevated PD-L1 expression. Cancer Cell 2014;25:590-604.
18. D'Incecco A, Andreozzi M, Ludovini V, Rossi E, Capodanno A, Landi L, et al. PD-1 and PD-L1 expression in molecularly selected non-small cell lung cancer patients. Br J Cancer 2015;112:95-102.
19. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, et al. Pembrolizumab for the treatment of non-small cell lung cancer. N Engl J Med 2015;372:2018-28.
20. Jones-Bolin SE, Johansson E, Palmisano WA, Anderson MW, Wiest JS, Belinsky SA. Effect of promoter and intron 2 polymorphisms on murine lung K-ras gene expression. Carcinogenesis 1998;19:1503-8.
21. Klein-Szanto AJ, Iizasa T, Momiki S, Garcia-Palazzo I, Caamano J, Metcalf R, et al. A tobacco-specific N-nitrosamine or cigarette smoke condensate causes neoplastic transformation of xenotransplanted human bronchial epithelial cells. Proc Natl Acad Sci U S A 1992;89:6693-7.
22. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307: 1098-101.
23. Politi K, Zakowski MF, Fan PD, Schonfeld EA, Pao W, Varmus HE. Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to downregulation of the receptors. Genes Dev 2006;20:1496-510.
24. Johnson L, Mercer K, GreenbaumD, Bronson RT, Crowley D, Tuveson DA, et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 2001;410:1111-6.
25. O'Donnell A, Faivre S, BurrisHAIII, Rea D, Papadimitrakopoulou V, Shand N, et al. Phase I pharmacokinetic and pharmacodynamic study of the oral mammalian target of rapamycin inhibitor everolimus in patients with advanced solid tumors. J Clin Oncol 2008;26:1588-95.
26. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012;4:127ra37.
27. West KA, Linnoila IR, Belinsky SA, Harris CC, Dennis PA. Tobacco carcinogen-induced cellular transformation increases activation of the phosphatidylinositol 30-kinase/Akt pathway in vitro and in vivo. Cancer Res 2004;64: 446-51.
28. Lee SJ, Jang BC, Lee SW, Yang YI, Suh SI, Park YM, et al. Interferon regulatory factor-1 is prerequisite to the constitutive expression and IFN-gammainduced upregulation of B7-H1 (CD274). FEBS Lett 2006;580:755-62.
29. Wolfle SJ, Strebovsky J, Bartz H, Sahr A, Arnold C, Kaiser C, et al. PD-L1 expression on tolerogenic APCs is controlled by STAT-3. Eur J Immunol 2011;41:413-24.
30. Mu CY, Huang JA, Chen Y, Chen C, Zhang XG. High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol 2011;28:682-8.
31. Chen YB, Mu CY, Huang JA. Clinical significance of programmed death-1 ligand-1 expression in patients with non-small cell lung cancer: a 5-yearfollow-up study. Tumori 2012;98:751-5.
32. Boland JM, Kwon ED, Harrington SM, Wampfler JA, Tang H, Yang P, et al. Tumor B7-H1 and B7-H3 expression in squamous cell carcinoma of the lung. Clin Lung Cancer 2013;14:157-63.
33. Konishi J, Yamazaki K, Azuma M, Kinoshita I, Dosaka-Akita H, Nishimura M. B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clin Cancer Res 2004;10:5094-100.
34. Velcheti V, Schalper KA, Carvajal DE, Anagnostou VK, Syrigos KN, Sznol M, et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest 2014;94:107-16.
35. Jiang X, Zhou J, Giobbie-Hurder A, Wargo J, Hodi FS. The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clin Cancer Res 2013;19:598-609.
36. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB, et al. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 2007;9: 166-80.
37. Sasaki H, Suzuki A, Shitara M, Hikosaka Y, Okuda K, Moriyama S, et al. gene expression in Japanese lung cancer patients. Biomed Rep 2013;1: 93-6.
38. Loke P, Allison JP. PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc Natl Acad Sci U S A 2003;100:5336-41.
39. Kaur S, Sassano A, Dolniak B, Joshi S, Majchrzak-Kita B, Baker DP, et al. Role of the Akt pathway in mRNA translation of interferon-stimulated genes. Proc Natl Acad Sci U S A 2008;105:4808-13.
40. Muthumani K, Shedlock DJ, Choo DK, Fagone P, Kawalekar OU, Goodman J, et al. HIV-mediated phosphatidylinositol 3-kinase/serine-threonine kinase activation in APCs leads to programmed death-1 ligand upregulation and suppression of HIV-specific CD8 T cells. J Immunol 2011;187: 2932-43.
41. Braumuller H, Wieder T, Brenner E, Assmann S, HahnM, Alkhaled M, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013;494: 361-5.
42. Ye J, Huang X, Hsueh EC, Zhang Q, Ma C, Zhang Y, et al. Human regulatory T cells induce T-lymphocyte senescence. Blood 2012;120:2021-31.
43. Hidalgo M, Buckner JC, Erlichman C, Pollack MS, Boni JP, Dukart G, et al. A phase I and pharmacokinetic study of temsirolimus (CCI-779) administered intravenously daily for 5 days every 2 weeks to patients with advanced cancer. Clin Cancer Res 2006;12:5755-63.
44. Bissler JJ,McCormack FX, Young LR, Elwing JM, Chuck G, Leonard JM, et al. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N Engl J Med 2008;358:140-51.
45. Haydar AA, Denton M, West A, Rees J, Goldsmith DJ. Sirolimus-induced pneumonitis: three cases and a review of the literature. Am J Transplant 2004;4:137-9.
46. Rao RR, Li Q, Odunsi K, Shrikant PA. The mTOR kinase determines effector versus memory CD8+ T-cell fate by regulating the expression of transcription factors T-bet and Eomesodermin. Immunity 2010;32: 67-78.
47. Hahnel PS, Thaler S, Antunes E, Huber C, Theobald M, Schuler M. Targeting AKT signaling sensitizes cancer to cellular immunotherapy. Cancer Res 2008;68:3899-906.
48. Garon EB, Balmanoukian A, Hamid O, Hui R, Gandhi L, Leighl N, et al. Abstract A20: MK-3475monotherapy for previously treated non-small cell lung cancer (NSCLC): preliminary safety and clinical activity. Clin Cancer Res 2014;20(2 Suppl):A20-A.
49. Creelan BC. Update on immune checkpoint inhibitors in lung cancer. Cancer Control 2014;21:80-9.
50. Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014;515:563-7.
51. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015;348: 124-8.