Elevated endoplasmic reticulum stress reinforced immunosuppression in the tumor microenvironment via myeloid-derived suppressor cells

Oncotarget

Volumn 5, Issue 23, 2014, Pages 12331-12345

  Lee, Bo Ra ^a   Chang, Sun Young ^b   Hong, Eun Hye ^a   Kwon, Bo Eun ^a   Kim, Hong Min ^c   Kim, Yeon Jeong ^d   Lee, Jongkook ^a   Cho, Hyun Jong ^a   Cheon, Jae Hee ^e   Ko, Hyun Jeong ^a  

^a Kangwon National University   (South Korea)

^b Ajou University   (South Korea)

^c Yonsei University Wonju   (South Korea)

^d Inje University   (South Korea)

^e Yonsei University College of Medicine   (South Korea)

Author keywords

Arginase 1; Cancer; ER stress; Immunosuppression; MDSC

Indexed keywords

4 PHENYLBUTYRIC ACID; ARGINASE 1; CD11B ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; 4-PHENYLBUTYRIC ACID; ANTINEOPLASTIC AGENT; ARYLBUTYRIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER LOCALIZATION; CELL DEATH; CELL POPULATION; CELL VIABILITY; COLON CANCER; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTIC INFILTRATION; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PROTEIN EXPRESSION; SPLEEN CELL; SUPPRESSOR CELL; TRANSCRIPTION INITIATION; TUMOR MICROENVIRONMENT; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; C57BL MOUSE; DRUG EFFECTS; EXPERIMENTAL NEOPLASM; IMMUNOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM STRESS; HETEROGRAFTS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID CELLS; NEOPLASMS, EXPERIMENTAL; PHENYLBUTYRATES; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT;

EID: 84919969162     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2589     Document Type: Article

References (51)

1. Peters LR, Raghavan M. Endoplasmic reticulum calcium depletion impacts chaperone secretion, innate immunity, and phagocytic uptake of cells. J Immunol. 2011; 187:919-931.
2. Jackisch C, Hahm HA, Tombal B, McCloskey D, Butash K, Davidson NE, Denmeade SR. Delayed micromolar elevation in intracellular calcium precedes induction of apoptosis in thapsigargin-treated breast cancer cells. Clin Cancer Res. 2000; 6:2844-2850.
3. Dubois C, Vanden Abeele F, Sehgal P, Olesen C, Junker S, Christensen SB, Prevarskaya N, Moller JV. Differential effects of thapsigargin analogues on apoptosis of prostate cancer cells: complex regulation by intracellular calcium. FEBS J. 2013; 280:5430-5440.
4. Ko HJ, Kim YJ, Kim YS, Chang WS, Ko SY, Chang SY, Sakaguchi S, Kang CY. A combination of chemoimmunotherapies can efficiently break self-tolerance and induce antitumor immunity in a tolerogenic murine tumor model. Cancer Res. 2007; 67:7477-7486.
5. Ko HJ, Lee JM, Kim YJ, Kim YS, Lee KA, Kang CY. Immunosuppressive myeloid-derived suppressor cells can be converted into immunogenic APCs with the help of activated NKT cells: an alternative cell-based antitumor vaccine. J Immunol. 2009; 182:1818-1828.
6. Hong EH, Chang SY, Lee BR, Kim YS, Lee JM, Kang CY, Kweon MN, Ko HJ. Blockade of Myd88 signaling induces antitumor effects by skewing the immunosuppressive function of myeloid-derived suppressor cells. Int J Cancer. 2013; 132:2839-2848.
7. Chen CJ, Kono H, Golenbock D, Reed G, Akira S, Rock KL. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med. 2007; 13:851-856.
8. Malo A, Kruger B, Goke B, Kubisch CH. 4-Phenylbutyric acid reduces endoplasmic reticulum stress, trypsin activation, and acinar cell apoptosis while increasing secretion in rat pancreatic acini. Pancreas. 2013; 42:92-101.
9. Pyrko P, Kardosh A, Liu Y-T, Soriano N, Xiong W, Chow RH, Uddin J, Petasis NA, Mircheff AK, Farley RA, Louie SG, Chen TC, Schönthal AH. Calcium-activated endoplasmic reticulum stress as a major component of tumor cell death induced by 2,5-dimethyl-celecoxib, a non-coxib analogue of celecoxib. Mol. Cancer Ther. 2007; 6:1262-1275.
10. Thastrup O, Cullen PJ, Drobak BK, Hanley MR, Dawson AP. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. P Natl Acad Sci USA. 1990; 87:2466-2470.
11. Denmeade SR, Jakobsen CM, Janssen S, Khan SR, Garrett ES, Lilja H, Christensen SB, Isaacs JT. Prostate-Specific Antigen-Activated Thapsigargin Prodrug as Targeted Therapy for Prostate Cancer. J Natl Cancer Inst. 2003; 95:990-1000.
12. Iwawaki T, Akai R, Kohno K, Miura M. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med. 2004; 10:98-102.
13. Kaiser AD, Gadiot J, Guislain A, Blank CU. Mimicking homeostatic proliferation in vitro generates T cells with high anti-tumor function in non-lymphopenic hosts. Cancer Immunol Immun. 2013; 62:503-515.
14. Mahadevan NR, Zanetti M. Tumor stress inside out: cellextrinsic effects of the unfolded protein response in tumor cells modulate the immunological landscape of the tumor microenvironment. J Immunol. 2011; 187:4403-4409.
15. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009; 9:162-174.
16. Bayne LJ, Vonderheide RH. A myeloid-derived suppressor cell-mediated T-cell suppression assay for functional evaluation of immune cells in tumor-bearing mice. Cold Spring Harb Protoc. 2013; 2013:849-853.
17. Lee J, Ryu H, Ferrante RJ, Morris SM, Jr., Ratan RR. Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox. P Natl Acad Sci USA. 2003; 100:4843-4848.
18. Corzo CA, Cotter MJ, Cheng P, Cheng F, Kusmartsev S, Sotomayor E, Padhya T, McCaffrey TV, McCaffrey JC, Gabrilovich DI. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol. 2009; 182:5693-5701.
19. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, Harding H, Novoa I, Varia M, Raleigh J, Scheuner D, Kaufman RJ, Bell J, Ron D, Wouters BG, Koumenis C. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 2005; 24:3470-3481.
20. Werno C, Zhou J, Brüne B. A23187, ionomycin and thapsigargin upregulate mRNA of HIF-1a via endoplasmic reticulum stress rather than a rise in intracellular calcium. J Cell Physiol. 2008; 215:708-714.
21. Bunt SK, Yang L, Sinha P, Clements VK, Leips J, Ostrand-Rosenberg S. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloidderived suppressor cells and limits tumor progression. Cancer Res. 2007; 67:10019-10026.
22. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, Cho HI, Celis E, Quiceno DG, Padhya T, McCaffrey TV, McCaffrey JC, Gabrilovich DI. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med. 2010; 207:2439-2453.
23. Fu ZQ, Yang Y, Song J, Jiang Q, Lin ZC, Wang Q, Zhu LQ, Wang JZ, Tian Q. LiCl attenuates thapsigargin-induced tau hyperphosphorylation by inhibiting GSK-3beta in vivo and in vitro. J Alzheimers Dis. 2010; 21:1107-1117.
24. Li D. GSK-3beta as a driving force in ovarian cancer. Cell Res. 2006; 16:609.
25. Shakoori A, Ougolkov A, Yu ZW, Zhang B, Modarressi MH, Billadeau DD, Mai M, Takahashi Y, Minamoto T. Deregulated GSK3beta activity in colorectal cancer: its association with tumor cell survival and proliferation. Biochem Biophys Res Commun. 2005; 334:1365-1373.
26. Rodriguez PC, Hernandez CP, Quiceno D, Dubinett SM, Zabaleta J, Ochoa JB, Gilbert J, Ochoa AC. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med. 2005; 202:931-939.
27. Schmid MC, Varner JA. Myeloid cells in the tumor microenvironment: modulation of tumor angiogenesis and tumor inflammation. J Oncol. 2010; 2010:201026.
28. Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, Beschin A, De Baetselier P, Van Ginderachter JA. Identification of discrete tumorinduced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood. 2008; 111:4233-4244.
29. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol. 2008; 181:5791-5802.
30. Zitvogel L, Kepp O, Senovilla L, Menger L, Chaput N, Kroemer G. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway. Clin Cancer Res. 2010; 16:3100-3104.
31. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature. 2011; 469:323-335.
32. Coe H, Jung J, Groenendyk J, Prins D, Michalak M. ERp57 modulates STAT3 signaling from the lumen of the endoplasmic reticulum. J Biol Chem. 2010; 285: 6725-6738.
33. Chao TS, Abe M, Hershenson MB, Gomes I, Rosner MR. Src tyrosine kinase mediates stimulation of Raf-1 and mitogen-activated protein kinase by the tumor promoter thapsigargin. Cancer Res. 1997; 57:3168-3173.
34. Huber M, Hughes MR, Krystal G. Thapsigargin-induced degranulation of mast cells is dependent on transient activation of phosphatidylinositol-3 kinase. J Immunol. 2000; 165:124-133.
35. Brusilow SW, Maestri NE. Urea cycle disorders: diagnosis, pathophysiology, and therapy. Adv Pediatr. 1996; 43:127-170.
36. Li LZ, Deng HX, Lou WZ, Sun XY, Song MW, Tao J, Xiao BX, Guo JM. Growth inhibitory effect of 4-phenyl butyric acid on human gastric cancer cells is associated with cell cycle arrest. World J Gastroentero. 2012; 18:79-83.
37. Kim DS, Li B, Rhew KY, Oh HW, Lim HD, Lee W, Chae HJ, Kim HR. The regulatory mechanism of 4-phenylbutyric acid against ER stress-induced autophagy in human gingival fibroblasts. Arch Pharm Res. 2012; 35:1269-1278.
38. Wiley JC, Meabon JS, Frankowski H, Smith EA, Schecterson LC, Bothwell M, Ladiges WC. Phenylbutyric acid rescues endoplasmic reticulum stress-induced suppression of APP proteolysis and prevents apoptosis in neuronal cells. PloS one. 2010; 5:e9135.
39. Petri S, Kiaei M, Kipiani K, Chen J, Calingasan NY, Crow JP, Beal MF. Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis. 2006; 22:40-49.
40. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006; 313:1137-1140.
41. Cao SS, Zimmermann EM, Chuang BM, Song B, Nwokoye A, Wilkinson JE, Eaton KA, Kaufman RJ. The unfolded protein response and chemical chaperones reduce protein misfolding and colitis in mice. Gastroenterology. 2013; 144:989-1000.e1006.
42. West AC, Mattarollo SR, Shortt J, Cluse LA, Christiansen AJ, Smyth MJ, Johnstone RW. An intact immune system is required for the anticancer activities of histone deacetylase inhibitors. Cancer Res. 2013; 73:7265-7276.
43. Kubota K, Niinuma Y, Kaneko M, Okuma Y, Sugai M, Omura T, Uesugi M, Uehara T, Hosoi T, Nomura Y. Suppressive effects of 4-phenylbutyrate on the aggregation of Pael receptors and endoplasmic reticulum stress. J Neurochem. 2006; 97:1259-1268.
44. Goedegebuure P, Mitchem JB, Porembka MR, Tan MC, Belt BA, Wang-Gillam A, Gillanders WE, Hawkins WG, Linehan DC. Myeloid-derived suppressor cells: general characteristics and relevance to clinical management of pancreatic cancer. Curr Cancer Drug Tar. 2011; 11:734-751.
45. Kim SJ, Hong EH, Lee BR, Park MH, Kim JW, Pyun AR, Kim YJ, Chang SY, Chin YW, Ko HJ. alpha-Mangostin Reduced ER Stress-mediated Tumor Growth through Autophagy Activation. Immune netw. 2012; 12:253-260.
46. Bachar-Wikstrom E, Wikstrom JD, Ariav Y, Tirosh B, Kaiser N, Cerasi E, Leibowitz G. Stimulation of autophagy improves endoplasmic reticulum stress-induced diabetes. Diabetes. 2013; 62:1227-1237.
47. Rabinowitz JD, White E. Autophagy and metabolism. Science. 2010; 330:1344-1348.
48. Salazar M, Carracedo A, Salanueva IJ, Hernandez-Tiedra S, Lorente M, Egia A, Vazquez P, Blazquez C, Torres S, Garcia S, Nowak J, Fimia GM, Piacentini M, Cecconi F, Pandolfi PP, Gonzalez-Feria L, et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Invest. 2009; 119:1359-1372.
49. Ciechomska IA, Kaminska B. ER stress and autophagy contribute to CsA-induced death of malignant glioma cells. Autophagy. 2012; 8:1526-1528.
50. Chang SY, Lee KC, Ko SY, Ko HJ, Kang CY. Enhanced efficacy of DNA vaccination against Her-2/neu tumor antigen by genetic adjuvants. Int J Cancer. 2004; 111:86-95.
51. Kim YS, Kim YJ, Lee JM, Han SH, Ko HJ, Park HJ, Pereboev A, Nguyen HH, Kang CY. CD40-targeted recombinant adenovirus significantly enhances the efficacy of antitumor vaccines based on dendritic cells and B cells. Hum Gene Ther. 2010; 21:1697-1706.