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Cancer Immunology, Immunotherapy

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03.03.2016 | Original Article

MHC class I chain-related molecule A and B expression is upregulated by cisplatin and associated with good prognosis in patients with non-small cell lung cancer

verfasst von: Riki Okita, Takuro Yukawa, Yuji Nojima, Ai Maeda, Shinsuke Saisho, Katsuhiko Shimizu, Masao Nakata

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 5/2016

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Abstract

MHC class I chain-related molecule A and B (MICA/B) are NK group 2 member D (NKG2D) ligands, which are broadly expressed in transformed cells. Both DNA damage-induced ataxia-telangiectasia-mutated (ATM)- and ATM and Rad3-related protein kinases (ATM–ATR) signaling and oncogene-induced PI3K–AKT signaling regulate the expression of NKG2D ligands, which promote NK cell-mediated cytotoxicity via NKG2D–NKG2D ligand interactions. NKG2D ligand overexpression was recently reported to be correlated with good prognosis in several types of cancer. However, the prognostic significance of NKG2D ligands in non-small cell lung cancer (NSCLC) remains unclear. Here, MICA/B expression was evaluated based on immunohistochemistry of 91 NSCLC samples from patients following radical surgery. In addition, expression of MICA/B was assessed in NSCLC cell lines treated with cisplatin in order to evaluate the regulatory mechanisms of MICA/B expression. Overall, 28 out of 91 (30.8 %) specimens showed high expression level of MICA/B, which was associated with low ¹⁸F-fluorodeoxyglucose uptake and manifestation of adenocarcinoma. After a median follow-up of 48.2 months, high MICA/B expression was associated with good recurrence-free survival (p = 0.037). In vitro assays using cell lines revealed that MICA/B expression was upregulated by cisplatin via ATM–ATR signaling, resulting in enhanced NK cell-mediated cytotoxicity. Upregulated MICA/B expressions in patients with radically resected NSCLC are predictive of good disease prognosis. Cisplatin-induced MICA/B upregulation is possibly an indirect mechanism by which the innate immune system eliminates tumor cells. NKG2D–NKG2D ligand-targeting therapy is a promising avenue for future immune-chemotherapy development.

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Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59(4):225–249CrossRefPubMed

Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, Postmus PE, Rusch V, Sobin L, International Association for the Study of Lung Cancer International Staging C, Participating I (2007) The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol 2(8):706–714CrossRefPubMed

Okada M, Nakayama H, Okumura S, Daisaki H, Adachi S, Yoshimura M, Miyata Y (2011) Multicenter analysis of high-resolution computed tomography and positron emission tomography/computed tomography findings to choose therapeutic strategies for clinical stage IA lung adenocarcinoma. J Thorac Cardiovasc Surg 141(6):1384–1391CrossRefPubMed

Rigau V, Molina TJ, Chaffaud C, Huchon G, Audouin J, Chevret S, Brechot JM (2002) Blood vessel invasion in resected non small cell lung carcinomas is predictive of metastatic occurrence. Lung Cancer 38(2):169–176CrossRefPubMed

Tsuchiya T, Akamine S, Muraoka M, Kamohara R, Tsuji K, Urabe S, Honda S, Yamasaki N (2007) Stage IA non-small cell lung cancer: vessel invasion is a poor prognostic factor and a new target of adjuvant chemotherapy. Lung Cancer 56(3):341–348CrossRefPubMed

Okada M, Nishio W, Sakamoto T, Uchino K, Yuki T, Nakagawa A, Tsubota N (2004) Prognostic significance of perioperative serum carcinoembryonic antigen in non-small cell lung cancer: analysis of 1,000 consecutive resections for clinical stage I disease. Ann Thorac Surg 78(1):216–221CrossRefPubMed

Lim E, Clough R, Goldstraw P, Edmonds L, Aokage K, Yoshida J, Nagai K, Shintani Y, Ohta M, Okumura M, Iwasaki T, Yasumitsu T, Okada M, Mimura T, Tsubota N, Nakagawa T, Okumura N, Satoh Y, Okumura S, Nakagawa K, Higashiyama M, Kodama K, Riquet M, Vicidomini G, Santini M, Kotoulas C, Hsu JY, Chen CY, International Pleural Lavage Cytology C (2010) Impact of positive pleural lavage cytology on survival in patients having lung resection for non-small-cell lung cancer: an international individual patient data meta-analysis. J Thorac Cardiovasc Surg 139(6):1441–1446CrossRefPubMed

Lanier LL (2001) A renaissance for the tumor immunosurveillance hypothesis. Nat Med 7(11):1178–1180CrossRefPubMed

Rimawi MF, Aleixo SB, Rozas AA, de Matos Nunes, Neto J, Caleffi M, Figueira AC, Souza SC, Reiriz AB, Gutierrez C, Arantes H, Uttenreuther-Fischer MM, Solca F, Osborne CK (2015) A neoadjuvant, randomized, open-label phase II trial of afatinib versus trastuzumab versus lapatinib in patients with locally advanced HER2-positive breast cancer. Clin Breast Cancer 15(2):101–109CrossRefPubMed

10.

Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285(5428):727–729CrossRefPubMed

11.

de Kruijf EM, Sajet A, van Nes JG, Putter H, Smit VT, Eagle RA, Jafferji I, Trowsdale J, Liefers GJ, van de Velde CJ, Kuppen PJ (2012) NKG2D ligand tumor expression and association with clinical outcome in early breast cancer patients: an observational study. BMC Cancer 12:24CrossRefPubMedPubMedCentral

12.

Cho H, Chung JY, Kim S, Braunschweig T, Kang TH, Kim J, Chung EJ, Hewitt SM, Kim JH (2014) MICA/B and ULBP1 NKG2D ligands are independent predictors of good prognosis in cervical cancer. BMC Cancer 14:957CrossRefPubMedPubMedCentral

13.

Kamimura H, Yamagiwa S, Tsuchiya A, Takamura M, Matsuda Y, Ohkoshi S, Inoue M, Wakai T, Shirai Y, Nomoto M, Aoyagi Y (2012) Reduced NKG2D ligand expression in hepatocellular carcinoma correlates with early recurrence. J Hepatol 56(2):381–388CrossRefPubMed

14.

Fang L, Gong J, Wang Y, Liu R, Li Z, Wang Z, Zhang Y, Zhang C, Song C, Yang A, Ting JP, Jin B, Chen L (2014) MICA/B expression is inhibited by unfolded protein response and associated with poor prognosis in human hepatocellular carcinoma. J Exp Clin Cancer Res 33(1):76CrossRefPubMedPubMedCentral

15.

Yamaguchi K, Chikumi H, Shimizu A, Takata M, Kinoshita N, Hashimoto K, Nakamoto M, Matsunaga S, Kurai J, Miyake N, Matsumoto S, Watanabe M, Yamasaki A, Igishi T, Burioka N, Shimizu E (2012) Diagnostic and prognostic impact of serum-soluble UL16-binding protein 2 in lung cancer patients. Cancer Sci 103(8):1405–1413CrossRefPubMed

16.

Douillard JY, Rosell R, De Lena M, Carpagnano F, Ramlau R, Gonzales-Larriba JL, Grodzki T, Pereira JR, Le Groumellec A, Lorusso V, Clary C, Torres AJ, Dahabreh J, Souquet PJ, Astudillo J, Fournel P, Artal-Cortes A, Jassem J, Koubkova L, His P, Riggi M, Hurteloup P (2006) Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB-IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol 7(9):719–727CrossRefPubMed

17.

Travis WD, Brambilla E, Müller-Hermelink HK, Harris CC (2004) Tumours of the lung, pleura, thymus and heart. Pathology & genetics. IARC Press, Lyon

18.

Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, Beer DG, Powell CA, Riely GJ, Van Schil PE, Garg K, Austin JH, Asamura H, Rusch VW, Hirsch FR, Scagliotti G, Mitsudomi T, Huber RM, Ishikawa Y, Jett J, Sanchez-Cespedes M, Sculier JP, Takahashi T, Tsuboi M, Vansteenkiste J, Wistuba I, Yang PC, Aberle D, Brambilla C, Flieder D, Franklin W, Gazdar A, Gould M, Hasleton P, Henderson D, Johnson B, Johnson D, Kerr K, Kuriyama K, Lee JS, Miller VA, Petersen I, Roggli V, Rosell R, Saijo N, Thunnissen E, Tsao M, Yankelewitz D (2011) International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 6(2):244–285CrossRefPubMedPubMedCentral

19.

Okita R, Mougiakakos D, Ando T, Mao Y, Sarhan D, Wennerberg E, Seliger B, Lundqvist A, Mimura K, Kiessling R (2012) HER2/HER3 signaling regulates NK cell-mediated cytotoxicity via MHC class I chain-related molecule A and B expression in human breast cancer cell lines. J Immunol 188(5):2136–2145CrossRefPubMed

20.

Okita R, Wolf D, Yasuda K, Maeda A, Yukawa T, Saisho S, Shimizu K, Yamaguchi Y, Oka M, Nakayama E, Lundqvist A, Kiessling R, Seliger B, Nakata M (2015) Contrasting effects of the cytotoxic anticancer drug gemcitabine and the EGFR tyrosine kinase inhibitor gefitinib on NK cell-mediated cytotoxicity via regulation of NKG2D ligand in non-small-cell lung cancer cells. PLoS One 10(10):e0139809CrossRefPubMedPubMedCentral

21.

Boissel N, Rea D, Tieng V, Dulphy N, Brun M, Cayuela JM, Rousselot P, Tamouza R, Le Bouteiller P, Mahon FX, Steinle A, Charron D, Dombret H, Toubert A (2006) BCR/ABL oncogene directly controls MHC class I chain-related molecule A expression in chronic myelogenous leukemia. J Immunol 176(8):5108–5116CrossRefPubMed

22.

Gasser S, Orsulic S, Brown EJ, Raulet DH (2005) The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436(7054):1186–1190CrossRefPubMedPubMedCentral

23.

Watanabe K, Nomori H, Ohtsuka T, Naruke T, Ebihara A, Orikasa H, Yamazaki K, Uno K, Kobayashi T, Goya T (2006) [F-18]Fluorodeoxyglucose positron emission tomography can predict pathological tumor stage and proliferative activity determined by Ki-67 in clinical stage IA lung adenocarcinomas. Jpn J Clin Oncol 36(7):403–409CrossRefPubMed

24.

Cerfolio RJ, Bryant AS, Ohja B, Bartolucci AA (2005) The maximum standardized uptake values on positron emission tomography of a non-small cell lung cancer predict stage, recurrence, and survival. J Thorac Cardiovasc Surg 130(1):151–159CrossRefPubMed

25.

Higashi K, Ueda Y, Sakurai A, Mingwang X, Xu L, Murakami M, Seki H, Oguchi M, Taki S, Nambu Y, Tonami H, Katsuda S, Yamamoto I (2000) Correlation of Glut-1 glucose transporter expression with [(18)F]FDG uptake in non-small cell lung cancer. Eur J Nucl Med 27(12):1778–1785CrossRef

26.

Kaira K, Oriuchi N, Shimizu K, Tominaga H, Yanagitani N, Sunaga N, Ishizuka T, Kanai Y, Mori M, Endo K (2009) 18F-FMT uptake seen within primary cancer on PET helps predict outcome of non-small cell lung cancer. J Nucl Med 50(11):1770–1776CrossRefPubMed

27.

Taylor MD, Smith PW, Brix WK, Wick MR, Theodosakis N, Swenson BR, Kozower BD, Lau CL, Jones DR (2009) Fluorodeoxyglucose positron emission tomography and tumor marker expression in non-small cell lung cancer. J Thorac Cardiovasc Surg 137(1):43–48CrossRefPubMedPubMedCentral

28.

Nakamura H, Hirata T, Kitamura H, Nishikawa J (2009) Correlation of the standardized uptake value in FDG-PET with the expression level of cell-cycle-related molecular biomarkers in resected non-small cell lung cancers. Ann Thorac Cardiovasc Surg 15(5):304–310PubMed

29.

Shimizu K, Hirami Y, Saisho S, Yukawa T, Maeda A, Yasuda K, Nakata M (2012) Maximal standardized uptake value on FDG-PET is correlated with cyclooxygenase-2 expression in patients with lung adenocarcinoma. Ann Thorac Surg 93(2):398–403CrossRefPubMed

30.

Vantourout P, Willcox C, Turner A, Swanson CM, Haque Y, Sobolev O, Grigoriadis A, Tutt A, Hayday A (2014) Immunological visibility: posttranscriptional regulation of human NKG2D ligands by the EGF receptor pathway. Sci Transl Med 6(231):231ra249

31.

Izar B, Sequist L, Lee M, Muzikansky A, Heist R, Iafrate J, Dias-Santagata D, Mathisen D, Lanuti M (2013) The impact of EGFR mutation status on outcomes in patients with resected stage I non-small cell lung cancers. Ann Thorac Surg 96(3):962–968CrossRefPubMed

32.

Sourisseau T, Hassan KA, Wistuba I, Penault-Llorca F, Adam J, Deutsch E, Soria JC (2014) Lung cancer stem cell: fancy conceptual model of tumor biology or cornerstone of a forthcoming therapeutic breakthrough? J Thorac Oncol 9(1):7–17CrossRefPubMed

33.

Pao W, Girard N (2011) New driver mutations in non-small-cell lung cancer. Lancet Oncol 12(2):175–180CrossRefPubMed

34.

Steinbacher J, Baltz-Ghahremanpour K, Schmiedel BJ, Steinle A, Jung G, Kubler A, Andre MC, Grosse-Hovest L, Salih HR (2015) An Fc-optimized NKG2D-immunoglobulin G fusion protein for induction of natural killer cell reactivity against leukemia. Int J Cancer 136(5):1073–1084CrossRefPubMed

Titel: MHC class I chain-related molecule A and B expression is upregulated by cisplatin and associated with good prognosis in patients with non-small cell lung cancer
verfasst von: Riki Okita
Takuro Yukawa
Yuji Nojima
Ai Maeda
Shinsuke Saisho
Katsuhiko Shimizu
Masao Nakata
Publikationsdatum: 03.03.2016
Verlag: Springer Berlin Heidelberg
Erschienen in: Cancer Immunology, Immunotherapy / Ausgabe 5/2016
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI: https://doi.org/10.1007/s00262-016-1814-9

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