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20.07.2016 | Original Article

Resistance to cytotoxicity and sustained release of interleukin-6 and interleukin-8 in the presence of decreased interferon-γ after differentiation of glioblastoma by human natural killer cells

verfasst von: Anna K. Kozlowska, Han-Ching Tseng, Kawaljit Kaur, Paytsar Topchyan, Akihito Inagaki, Vickie T. Bui, Noriyuki Kasahara, Nicholas Cacalano, Anahid Jewett

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 9/2016

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Abstract

Natural killer (NK) cells are functionally suppressed in the glioblastoma multiforme (GBM) tumor microenvironment. We have recently shown that survival and differentiation of cancer stem-like cells (CSCs)/poorly differentiated tumors are controlled through two distinct phenotypes of cytotoxic and non-cytotoxic/split anergized NK cells, respectively. In this paper, we studied the function of NK cells against brain CSCs/poorly differentiated GBM and their NK cell-differentiated counterparts. Brain CSCs/poorly differentiated GBM, differentiated by split anergized NK supernatants (supernatants from NK cells treated with IL-2 + anti-CD16mAb) expressed higher levels of CD54, B7H1 and MHC-I and were killed less by the NK cells, whereas their CSCs/poorly differentiated counterparts were highly susceptible to NK cell lysis. Resistance to NK cells and differentiation of brain CSCs/poorly differentiated GBM by split anergized NK cells were mediated by interferon (IFN)-γ and tumor necrosis factor (TNF)-α. Brain CSCs/poorly differentiated GBM expressed low levels of TNFRs and IFN-γRs, and when differentiated and cultured with IL-2-treated NK cells, they induced increased secretion of pro-inflammatory cytokine interleukin (IL)-6 and chemokine IL-8 in the presence of decreased IFN-γ secretion. NK-induced differentiation of brain CSCs/poorly differentiated GBM cells was independent of the function of IL-6 and/or IL-8. The inability of NK cells to lyse GBM tumors and the presence of a sustained release of pro-inflammatory cytokines IL-6 and chemokine IL-8 in the presence of a decreased IFN-γ secretion may lead to the inadequacy of NK cells to differentiate GBM CSCs/poorly differentiated tumors, thus failing to control tumor growth.

Nur mit Berechtigung zugänglich

Safari M, Khoshnevisan A (2015) Cancer stem cells and chemoresistance in glioblastoma multiform: a review article. J Stem Cells 10(4):271–285

Ropolo M, Daga A, Griffero F, Foresta M, Casartelli G, Zunino A, Poggi A, Cappelli E, Zona G, Spaziante R, Corte G, Frosina G (2009) Comparative analysis of DNA repair in stem and nonstem glioma cell cultures. Mol Cancer Res 7(3):383–392. doi:10.1158/1541-7786.MCR-08-0409 CrossRefPubMed

Shan Y, He X, Song W, Han D, Niu J, Wang J (2015) Role of IL-6 in the invasiveness and prognosis of glioma. Int J Clin Exp Med 8(6):9114–9120PubMedPubMedCentral

Xie K (2001) Interleukin-8 and human cancer biology. Cytokine Growth Factor Rev 12(4):375–391CrossRefPubMed

Sasaki A, Ishiuchi S, Kanda T, Hasegawa M, Nakazato Y (2001) Analysis of interleukin-6 gene expression in primary human gliomas, glioblastoma xenografts, and glioblastoma cell lines. Brain Tumor Pathol 18(1):13–21CrossRefPubMed

Desbaillets I, Diserens AC, de Tribolet N, Hamou MF, Van Meir EG (1999) Regulation of interleukin-8 expression by reduced oxygen pressure in human glioblastoma. Oncogene 18(7):1447–1456. doi:10.1038/sj.onc.1202424 CrossRefPubMed

Desbaillets I, Diserens AC, Tribolet N, Hamou MF, Van Meir EG (1997) Upregulation of interleukin 8 by oxygen-deprived cells in glioblastoma suggests a role in leukocyte activation, chemotaxis, and angiogenesis. J Exp Med 186(8):1201–1212CrossRefPubMedPubMedCentral

Tada M, Suzuki K, Yamakawa Y, Sawamura Y, Sakuma S, Abe H, van Meir E, de Tribolet N (1993) Human glioblastoma cells produce 77 amino acid interleukin-8 (IL-8(77)). J Neurooncol 16(1):25–34CrossRefPubMed

Van Meir E, Ceska M, Effenberger F, Walz A, Grouzmann E, Desbaillets I, Frei K, Fontana A, de Tribolet N (1992) Interleukin-8 is produced in neoplastic and infectious diseases of the human central nervous system. Cancer Res 52(16):4297–4305PubMed

10.

Tseng HC, Bui V, Man YG, Cacalano N, Jewett A (2014) Induction of split anergy conditions natural killer cells to promote differentiation of stem cells through cell–cell contact and secreted factors. Front Immunol 5:269. doi:10.3389/fimmu.2014.00269 PubMedPubMedCentral

11.

Nakazawa T, Nakamura M, Park YS, Motoyama Y, Hironaka Y, Nishimura F, Nakagawa I, Yamada S, Matsuda R, Tamura K, Sugimoto T, Takeshima Y, Marutani A, Tsujimura T, Ouji N, Ouji Y, Yoshikawa M, Nakase H (2014) Cytotoxic human peripheral blood-derived gammadelta T cells kill glioblastoma cell lines: implications for cell-based immunotherapy for patients with glioblastoma. J Neurooncol 116(1):31–39. doi:10.1007/s11060-013-1258-4 CrossRefPubMed

12.

Finocchiaro G, Pellegatta S (2014) Perspectives for immunotherapy in glioblastoma treatment. Curr Opin Oncol 26(6):608–614. doi:10.1097/CCO.0000000000000135 CrossRefPubMed

13.

Chanvillard C, Jacolik RF, Infante-Duarte C, Nayak RC (2013) The role of natural killer cells in multiple sclerosis and their therapeutic implications. Front Immunol 4:63. doi:10.3389/fimmu.2013.00063 CrossRefPubMedPubMedCentral

14.

Kaur G, Trowsdale J, Fugger L (2013) Natural killer cells and their receptors in multiple sclerosis. Brain 136(Pt 9):2657–2676. doi:10.1093/brain/aws159 CrossRefPubMed

15.

Poli A, Kmiecik J, Domingues O, Hentges F, Blery M, Chekenya M, Boucraut J, Zimmer J (2013) NK cells in central nervous system disorders. J Immunol 190(11):5355–5362. doi:10.4049/jimmunol.1203401 CrossRefPubMed

16.

Poli A, Wang J, Domingues O, Planaguma J, Yan T, Rygh CB, Skaftnesmo KO, Thorsen F, McCormack E, Hentges F, Pedersen PH, Zimmer J, Enger PO, Chekenya M (2013) Targeting glioblastoma with NK cells and mAb against NG2/CSPG4 prolongs animal survival. Oncotarget 4(9):1527–1546CrossRefPubMedPubMedCentral

17.

Tsuboi I, Tanaka H, Nakao M, Shichijo S, Itoh K (1995) Nonsteroidal anti-inflammatory drugs differentially regulate cytokine production in human lymphocytes: up-regulation of TNF, IFN-gamma and IL-2, in contrast to down-regulation of IL-6 production. Cytokine 7(4):372–379CrossRefPubMed

18.

Miescher S, Stoeck M, Qiao L, Barras C, Barrelet L, von Fliedner V (1988) Preferential clonogenic deficit of CD8-positive T-lymphocytes infiltrating human solid tumors. Cancer Res 48(24 Pt 1):6992–6998PubMed

19.

Qin J, Han B, Pang J (1997) The relationship between TIL from human primary hepatic carcinoma and prognosis. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 77(3):167–170 (Article in Chinese)

20.

Han X, Papadopoulos AJ, Ruparelia V, Devaja O, Raju KS (1997) Tumor lymphocytes in patients with advanced ovarian cancer: changes during in vitro culture and implications for immunotherapy. Gynecol Oncol 65(3):391–398CrossRefPubMed

21.

Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9(5):391–403. doi:10.1016/j.ccr.2006.03.030 CrossRefPubMed

22.

Castriconi R, Daga A, Dondero A, Zona G, Poliani PL, Melotti A, Griffero F, Marubbi D, Spaziante R, Bellora F, Moretta L, Moretta A, Corte G, Bottino C (2009) NK cells recognize and kill human glioblastoma cells with stem cell-like properties. J Immunol 182(6):3530–3539. doi:10.4049/jimmunol.0802845 CrossRefPubMed

23.

Jewett A, Gan XH, Lebow LT, Bonavida B (1996) Differential secretion of TNF-alpha and IFN-gamma by human peripheral blood-derived NK subsets and association with functional maturation. J Clin Immunol 16(1):46–54CrossRefPubMed

24.

Jewett A, Cavalcanti M, Bonavida B (1997) Pivotal role of endogenous TNF-alpha in the induction of functional inactivation and apoptosis in NK cells. J Immunol 159(10):4815–4822PubMed

25.

Jewett A, Bonavida B (1996) Target-induced inactivation and cell death by apoptosis in a subset of human NK cells. J Immunol 156(3):907–915PubMed

26.

Jewett A, Bonavida B (1995) Target-induced anergy of natural killer cytotoxic function is restricted to the NK-target conjugate subset. Cell Immunol 160(1):91–97CrossRefPubMed

27.

Jewett A, Bonavida B (2000) MHC-Class I antigens regulate both the function and the survival of human peripheral blood NK cells: role of endogenously secreted TNF-alpha. Clin Immunol 96(1):19–28CrossRefPubMed

28.

Jewett A, Cacalano NA, Head C, Teruel A (2006) Coengagement of CD16 and CD94 receptors mediates secretion of chemokines and induces apoptotic death of naive natural killer cells. Clin Cancer Res 12(7 Pt 1):1994–2003CrossRefPubMed

29.

Jewett A, Teruel A, Romero M, Head C, Cacalano N (2008) Rapid and potent induction of cell death and loss of NK cell cytotoxicity against oral tumors by F(ab’)2 fragment of anti-CD16 antibody. Cancer Immunol Immunother 57(7):1053–1066CrossRefPubMed

30.

Lai P, Rabinowich H, Crowley-Nowick PA, Bell MC, Mantovani G, Whiteside TL (1996) Alterations in expression and function of signal-transducing proteins in tumor-associated T and natural killer cells in patients with ovarian carcinoma. Clin Cancer Res 2(1):161–173PubMed

31.

Kuss I, Saito T, Johnson JT, Whiteside TL (1999) Clinical significance of decreased zeta chain expression in peripheral blood lymphocytes of patients with head and neck cancer. Clin Cancer Res 5(2):329–334PubMed

32.

Tseng HC, Arasteh A, Paranjpe A, Teruel A, Yang W, Behel A, Alva JA, Walter G, Head C, Ishikawa TO, Herschman HR, Cacalano N, Pyle AD, Park NH, Jewett A (2010) Increased lysis of stem cells but not their differentiated cells by natural killer cells; de-differentiation or reprogramming activates NK cells. PLoS One 5(7):e11590. doi:10.1371/journal.pone.0011590 CrossRefPubMedPubMedCentral

33.

Oka N, Soeda A, Inagaki A, Onodera M, Maruyama H, Hara A, Kunisada T, Mori H, Iwama T (2007) VEGF promotes tumorigenesis and angiogenesis of human glioblastoma stem cells. Biochem Biophys Res Commun 360(3):553–559. doi:10.1016/j.bbrc.2007.06.094 CrossRefPubMed

34.

Soeda A, Inagaki A, Oka N, Ikegame Y, Aoki H, Yoshimura S, Nakashima S, Kunisada T, Iwama T (2008) Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells. J Biol Chem 283(16):10958–10966. doi:10.1074/jbc.M704205200 CrossRefPubMed

35.

Tseng HC, Inagaki A, Bui VT, Cacalano N, Kasahara N, Man YG, Jewett A (2015) Differential targeting of stem cells and differentiated glioblastomas by NK cells. J Cancer 6(9):866–876CrossRefPubMedPubMedCentral

36.

Jewett A, Bonavida B (1995) Interferon-alpha activates cytotoxic function but inhibits interleukin-2-mediated proliferation and tumor necrosis factor-alpha secretion by immature human natural killer cells. J Clin Immunol 15(1):35–44CrossRefPubMed

37.

Jewett A, Wang MY, Teruel A, Poupak Z, Bostanian Z, Park NH (2003) Cytokine dependent inverse regulation of CD54 (ICAM1) and major histocompatibility complex class I antigens by nuclear factor kappaB in HEp2 tumor cell line: effect on the function of natural killer cells. Hum Immunol 64(5):505–520CrossRefPubMed

38.

Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD, Engh J, Iwama T, Kunisada T, Kassam AB, Pollack IF, Park DM (2009) Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 28(45):3949–3959. doi:10.1038/onc.2009.252 CrossRefPubMed

39.

Inagaki A, Soeda A, Oka N, Kitajima H, Nakagawa J, Motohashi T, Kunisada T, Iwama T (2007) Long-term maintenance of brain tumor stem cell properties under at non-adherent and adherent culture conditions. Biochem Biophys Res Commun 361(3):586–592CrossRefPubMed

40.

Hong X, Chedid K, Kalkanis SN (2012) Glioblastoma cell line-derived spheres in serumcontaining medium versus serum-free medium: a comparison of cancer stem cell properties. Int J Oncol 41(5):1693–1700. doi:10.3892/ijo.2012.1592 PubMed

41.

Jewett A, Tseng HC (2013) Tumor microenvironment may shape the function and phenotype of NK cells through the induction of split anergy and generation of regulatory NK cells. In: Shurin M, Umansky V, Malyguine A (eds) The tumor immunoenvironment. Springer, Dordrecht, pp 361–384CrossRef

42.

Jewett A, Arasteh A, Tseng HC, Behel A, Arasteh H, Yang W, Cacalano NA, Paranjpe A (2010) Strategies to rescue mesenchymal stem cells (MSCs) and dental pulp stem cells (DPSCs) from NK cell mediated cytotoxicity. PLoS One 5(3):e9874. doi:10.1371/journal.pone.0009874 CrossRefPubMedPubMedCentral

43.

Jewett A, Man YG, Tseng HC (2013) Dual functions of natural killer cells in selection and differentiation of stem cells; role in regulation of inflammation and regeneration of tissues. J Cancer 4(1):12–24. doi:10.7150/jca.5519 CrossRefPubMed

44.

Jewett A, Tseng HC (2012) Potential rescue, survival and differentiation of cancer stem cells and primary non-transformed stem cells by monocyte-induced split anergy in natural killer cells. Cancer Immunol Immunother 61(2):265–274. doi:10.1007/s00262-011-1163-7 CrossRefPubMed

45.

Jewett A, Tseng HC, Arasteh A, Saadat S, Christensen RE, Cacalano NA (2012) Natural killer cells preferentially target cancer stem cells; role of monocytes in protection against NK cell mediated lysis of cancer stem cells. Curr Drug Deliv 9(1):5–16CrossRefPubMed

46.

Jewett A, Man YG, Cacalano N, Kos J, Tseng HC (2014) Natural killer cells as effectors of selection and differentiation of stem cells: role in resolution of inflammation. J Immunotoxicol 11(4):297–307. doi:10.3109/1547691X.2013.877104 CrossRefPubMed

47.

Wang H, Lathia JD, Wu Q, Wang J, Li Z, Heddleston JM, Eyler CE, Elderbroom J, Gallagher J, Schuschu J, MacSwords J, Cao Y, McLendon RE, Wang XF, Hjelmeland AB, Rich JN (2009) Targeting interleukin 6 signaling suppresses glioma stem cell survival and tumor growth. Stem Cells 27(10):2393–2404. doi:10.1002/stem.188 CrossRefPubMedPubMedCentral

48.

Black KL, Chen K, Becker DP, Merrill JE (1992) Inflammatory leukocytes associated with increased immunosuppression by glioblastoma. J Neurosurg 77(1):120–126. doi:10.3171/jns.1992.77.1.0120 CrossRef

49.

Chiorean R, Berindan-Neagoe I, Braicu C, Florian IS, Leucuta D, Crisan D, Cernea V (2014) Quantitative expression of serum biomarkers involved in angiogenesis and inflammation, in patients with glioblastoma multiforme: correlations with clinical data. Cancer Biomark 14(2–3):185–194. doi:10.3233/CBM-130310 PubMed

50.

Reynes G, Vila V, Martin M, Parada A, Fleitas T, Reganon E, Martinez-Sales V (2011) Circulating markers of angiogenesis, inflammation, and coagulation in patients with glioblastoma. J Neurooncol 102(1):35–41. doi:10.1007/s11060-010-0290-x CrossRefPubMed

51.

Rygh CB, Wang J, Thuen M, Gras Navarro A, Huuse EM, Thorsen F, Poli A, Zimmer J, Haraldseth O, Lie SA, Enger PO, Chekenya M (2014) Dynamic contrast enhanced MRI detects early response to adoptive NK cellular immunotherapy targeting the NG2 proteoglycan in a rat model of glioblastoma. PLoS One 9(9):e108414. doi:10.1371/journal.pone.0108414 CrossRefPubMedPubMedCentral

52.

Gras Navarro A, Kmiecik J, Leiss L, Zelkowski M, Engelsen A, Bruserud O, Zimmer J, Enger PO, Chekenya M (2014) NK cells with KIR2DS2 immunogenotype have a functional activation advantage to efficiently kill glioblastoma and prolong animal survival. J Immunol 193(12):6192–6206. doi:10.4049/jimmunol.1400859 CrossRefPubMedPubMedCentral

Titel: Resistance to cytotoxicity and sustained release of interleukin-6 and interleukin-8 in the presence of decreased interferon-γ after differentiation of glioblastoma by human natural killer cells
verfasst von: Anna K. Kozlowska
Han-Ching Tseng
Kawaljit Kaur
Paytsar Topchyan
Akihito Inagaki
Vickie T. Bui
Noriyuki Kasahara
Nicholas Cacalano
Anahid Jewett
Publikationsdatum: 20.07.2016
Verlag: Springer Berlin Heidelberg
Erschienen in: Cancer Immunology, Immunotherapy / Ausgabe 9/2016
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI: https://doi.org/10.1007/s00262-016-1866-x

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Resistance to cytotoxicity and sustained release of interleukin-6 and interleukin-8 in the presence of decreased interferon-γ after differentiation of glioblastoma by human natural killer cells

Abstract

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