Elevation of MMP-9 and IDO induced by pancreatic cancer cells mediates natural killer cell dysfunction

BMC Cancer

Volumn 14, Issue 1, 2014, Pages 1-12

  Peng, Yun Peng ^a   Zhang, Jing Jing ^a,b   Liang, Wen Biao ^c   Tu, Min ^a   Lu, Zi Peng ^a   Wei, Ji Shu ^a   Jiang, Kui Rong ^a   Gao, Wen Tao ^a   Wu, Jun Li ^a   Xu, Ze Kuan ^a,b   Miao, Yi ^a,b   Zhu, Yi ^a,b  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b Jiangsu Province Academy of Clinical Medicine   (China)

^c Jiangsu Province Blood Center   (China)

Author keywords

IDO; MMP 9; Natural killer cell dysfunction; Pancreatic cancer

Indexed keywords

1 MT PROTEIN; GAMMA INTERFERON; GELATINASE B; GRANZYME B; INDOLEAMINE 2,3 DIOXYGENASE; LYMPHOCYTE RECEPTOR; MEMBRANE PROTEIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; PROTEIN DNAM 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; CYTOKINE;

APOPTOSIS; ARTICLE; BLOOD CULTURE; CANCER CELL CULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; MYELOID LEUKEMIA; NATURAL KILLER CELL; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR ESCAPE; UPREGULATION; BIOSYNTHESIS; CELL CULTURE; COCULTURE; IMMUNOLOGY; METABOLISM; PANCREAS TUMOR; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KILLER CELLS, NATURAL; MATRIX METALLOPROTEINASE 9; PANCREATIC NEOPLASMS; RECEPTORS, CELL SURFACE;

EID: 84928724945     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-738     Document Type: Article

References (50)

1. Siegel R, Naishadham D, Jemal A: Cancer statistics, 2012. CA Cancer J Clin 2012, 62:10-29.
2. Erkan M, Hausmann S, Michalski CW, Fingerle AA, Dobritz M, Kleeff J, Friess H: The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat Rev Gastroenterol Hepatol 2012, 9:454-467.
3. Tuveson DA, Neoptolemos JP: Understanding metastasis in pancreatic cancer: a call for new clinical approaches. Cell 2012, 148:21-23.
4. Tredan O, Galmarini CM, Patel K, Tannock IF: Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 2007, 99:1441-1454.
5. Mahadevan D, Von Hoff DD: Tumor-stroma interactions in pancreatic ductal adenocarcinoma. Mol Cancer Ther 2007, 6:1186-1197.
6. Esposito I, Menicagli M, Funel N, Bergmann F, Boggi U, Mosca F, Bevilacqua G, Campani D: Inflammatory cells contribute to the generation of an angiogenic phenotype in pancreatic ductal adenocarcinoma. J Clin Pathol 2004, 57:630-636.
7. Duan X, Deng L, Chen X, Lu Y, Zhang Q, Zhang K, Hu Y, Zeng J, Sun W: Clinical significance of the immunostimulatory MHC class I chain-related molecule A and NKG2D receptor on NK cells in pancreatic cancer. Med Oncol 2011, 28:466-474.
8. Kiessling R, Klein E, Wigzell H: "Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol 1975, 5:112-117.
9. Herberman RB, Nunn ME, Lavrin DH: Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer 1975, 16:216-229.
10. Storkus WJ, Howell DN, Salter RD, Dawson JR, Cresswell P: NK susceptibility varies inversely with target cell class I HLA antigen expression. J Immunol 1987, 138:1657-1659.
11. Davis M, Conlon K, Bohac GC, Barcenas J, Leslie W, Watkins L, Lamzabi I, Deng Y, Li Y, Plate JM: Effect of pemetrexed on innate immune killer cells and adaptive immune T cells in subjects with adenocarcinoma of the pancreas. J Immunother 2012, 35:629-640.
12. Saito H, Osaki T, Ikeguchi M: Decreased NKG2D expression on NK cells correlates with impaired NK cell function in patients with gastric cancer. Gastric Cancer 2012, 15:27-33.
13. Shen Y, Lu C, Tian W, Wang L, Cui B, Jiao Y, Ma C, Ju Y, Zhu L, Shao C, Liu X, Wang J, Zhang B, Lu Z: Possible association of decreased NKG2D expression levels and suppression of the activity of natural killer cells in patients with colorectal cancer. Int J Oncol 2012, 40:1285-1290.
14. Garcia-Iglesias T, Del Toro-Arreola A, Albarran-Somoza B, Del Toro-Arreola S, Sanchez-Hernandez PE, Ramirez-Duenas MG, Balderas-Pena LM, Bravo-Cuellar A, Ortiz-Lazareno PC, Daneri-Navarro A: Low NKp30, NKp46 and NKG2D expression and reduced cytotoxic activity on NK cells in cervical cancer and precursor lesions. BMC Cancer 2009, 9:186.
15. Bae S, Oh K, Kim H, Kim Y, Kim HR, Hwang YI, Lee DS, Kang JS, Lee WJ: The effect of alloferon on the enhancement of NK cell cytotoxicity against cancer via the up-regulation of perforin/granzyme B secretion. Immunobiology 2013, 218:1026-1033.
16. Li T, Yang Y, Hua X, Wang G, Liu W, Jia C, Tai Y, Zhang Q, Chen G: Hepatocellular carcinoma-associated fibroblasts trigger NK cell dysfunction via PGE2 and IDO. Cancer Lett 2012, 318:154-161.
17. Ozturk OG, Gun FD, Polat G: Killer cell immunoglobulin-like receptor genes in patients with breast cancer. Med Oncol 2012, 29:511-515.
18. Al Omar S, Middleton D, Marshall E, Porter D, Xinarianos G, Raji O, Field JK, Christmas SE: Associations between genes for killer immunoglobulin-like receptors and their ligands in patients with solid tumors. Hum Immunol 2010, 71:976-981.
19. Ding Y, Xu D, Feng G, Bushell A, Muschel RJ, Wood KJ: Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and -9. Diabetes 2009, 58:1797-1806.
20. Lee BK, Kim MJ, Jang HS, Lee HR, Ahn KM, Lee JH, Choung PH: A high concentration of MMP-2/gelatinase A and MMP-9/gelatinase B reduce NK cell-mediated cytotoxicity against an oral squamous cell carcinoma cell line. In Vivo 2008, 22:593-597.
21. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D: Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 2004, 103:4619-4621.
22. Wang D, Saga Y, Mizukami H, Sato N, Nonaka H, Fujiwara H, Takei Y, Machida S, Takikawa O, Ozawa K, Suzuki M: Indoleamine-2,3-dioxygenase, an immunosuppressive enzyme that inhibits natural killer cell function, as a useful target for ovarian cancer therapy. Int J Oncol 2012, 40:929-934.
23. Sharma S, Yang SC, Zhu L, Reckamp K, Gardner B, Baratelli F, Huang M, Batra RK, Dubinett SM: Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res 2005, 65:5211-5220.
24. Ma X, Kundu N, Rifat S, Walser T, Fulton AM: Prostaglandin E receptor EP4 antagonism inhibits breast cancer metastasis. Cancer Res 2006, 66:2923-2927.
25. Kundu N, Ma X, Holt D, Goloubeva O, Ostrand-Rosenberg S, Fulton AM: Antagonism of the prostaglandin E receptor EP4 inhibits metastasis and enhances NK function. Breast Cancer Res Treat 2009, 117:235-242.
26. Lee KM, Nguyen C, Ulrich AB, Pour PM, Ouellette MM: Immortalization with telomerase of the Nestin-positive cells of the human pancreas. Biochem Biophys Res Commun 2003, 301:1038-1044.
27. Gong JH, Maki G, Klingemann HG: Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia 1994, 8:652-658.
28. Peng YP, Zhu Y, Zhang JJ, Xu ZK, Qian ZY, Dai CC, Jiang KR, Wu JL, Gao WT, Li Q, Du Q, Miao Y: Comprehensive analysis of the percentage of surface receptors and cytotoxic granules positive natural killer cells in patients with pancreatic cancer, gastric cancer, and colorectal cancer. J Transl Med 2013, 11:262.
29. Mirjacic Martinovic K, Konjevic G, Babovic N, Inic M: The stage dependent changes in NK cell activity and the expression of activating and inhibitory NK cell receptors in melanoma patients. J Surg Res 2011, 171:637-649.
30. Arreygue-Garcia NA, Daneri-Navarro A, del Toro-Arreola A, Cid-Arregui A, Gonzalez-Ramella O, Jave-Suarez LF, Aguilar-Lemarroy A, Troyo-Sanroman R, Bravo-Cuellar A, Delgado-Rizo V, Garcia-Iglesias T, Hernandez-Flores G, Del Toro-Arreola S: Augmented serum level of major histocompatibility complex class I-related chain A (MICA) protein and reduced NKG2D expression on NK and T cells in patients with cervical cancer and precursor lesions. BMC Cancer 2008, 8:16.
31. Gasser S, Orsulic S, Brown EJ, Raulet DH: The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005, 436:1186-1190.
32. Hecht ML, Rosental B, Horlacher T, Hershkovitz O, De Paz JL, Noti C, Schauer S, Porgador A, Seeberger PH: Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J Proteome Res 2009, 8:712-720.
33. Chowdhury D, Lieberman J: Death by a thousand cuts: granzyme pathways of programmed cell death. Annu Rev Immunol 2008, 26:389-420.
34. Fauriat C, Long EO, Ljunggren HG, Bryceson YT: Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 2010, 115:2167-2176.
35. Campbell KS, Hasegawa J: Natural killer cell biology: An update and future directions. J Allergy Clin Immunol 2013, 132:536-544.
36. van den Bosch G, Preijers F, Vreugdenhil A, Hendriks J, Maas F, De Witte T: Granulocyte-macrophage colony-stimulating factor (GM-CSF) counteracts the inhibiting effect of monocytes on natural killer (NK) cells. Clin Exp Immunol 1995, 101:515-520.
37. Sun K, Alvarez M, Ames E, Barao I, Chen M, Longo DL, Redelman D, Murphy WJ: Mouse NK cell-mediated rejection of bone marrow allografts exhibits patterns consistent with Ly49 subset licensing. Blood 2012, 119:1590-1598.
38. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D: Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000, 2:737-744.
39. Coussens LM, Tinkle CL, Hanahan D, Werb Z: MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000, 103:481-490.
40. Itoh T, Tanioka M, Matsuda H, Nishimoto H, Yoshioka T, Suzuki R, Uehira M: Experimental metastasis is suppressed in MMP-9-deficient mice. Clin Exp Metastasis 1999, 17:177-181.
41. Sheu BC, Hsu SM, Ho HN, Lien HC, Huang SC, Lin RH: A novel role of metalloproteinase in cancer-mediated immunosuppression. Cancer Res 2001, 61:237-242.
42. Opdenakker G, Van den Steen PE, Van Damme J: Gelatinase B: a tuner and amplifier of immune functions. Trends Immunol 2001, 22:571-579.
43. Schroecksnadel K, Winkler C, Duftner C, Wirleitner B, Schirmer M, Fuchs D: Tryptophan degradation increases with stage in patients with rheumatoid arthritis. Clin Rheumatol 2006, 25:334-337.
44. Mellor AL, Munn DH: IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 2004, 4:762-774.
45. Sato N, Saga Y, Mizukami H, Wang D, Takahashi S, Nonaka H, Fujiwara H, Takei Y, Machida S, Takikawa O, Ozawa K, Suzuki M: Downregulation of indoleamine-2,3-dioxygenase in cervical cancer cells suppresses tumor growth by promoting natural killer cell accumulation. Oncol Rep 2012, 28:1574-1578.
46. Witkiewicz A, Williams TK, Cozzitorto J, Durkan B, Showalter SL, Yeo CJ, Brody JR: Expression of indoleamine 2,3-dioxygenase in metastatic pancreatic ductal adenocarcinoma recruits regulatory T cells to avoid immune detection. J Am Coll Surg 2008, 206:849-854. discussion 854-846.
47. Yu J, Sun J, Wang SE, Li H, Cao S, Cong Y, Liu J, Ren X: Upregulated expression of indoleamine 2, 3-dioxygenase in primary breast cancer correlates with increase of infiltrated regulatory T cells in situ and lymph node metastasis. Clin Dev Immunol 2011, 2011:469135.
48. Liang M, Li J, Wang D, Li S, Sun Y, Sun T, Zhang J, Chen X, Li Q, Sun S: T-cell infiltration and expressions of T lymphocyte co-inhibitory B7-H1 and B7-H4 molecules among colorectal cancer patients in northeast China's Heilongjiang province. Tumour Biol 2013, 35:55-60.
49. Polimeno M, Napolitano M, Costantini S, Portella L, Esposito A, Capone F, Guerriero E, Trotta A, Zanotta S, Pucci L, Longo N, Perdonà S, Pignata S, Castello G, Scala S: Regulatory T cells, interleukin (IL)-6, IL-8, Vascular endothelial growth factor (VEGF), CXCL10, CXCL11, epidermal growth factor (EGF) and hepatocyte growth factor (HGF) as surrogate markers of host immunity in patients with renal cell carcinoma. BJU Int 2013, 112:686-696.
50. Pietra G, Manzini C, Rivara S, Vitale M, Cantoni C, Petretto A, Balsamo M, Conte R, Benelli R, Minghelli S, Solari N, Gualco M, Queirolo P, Moretta L, Mingari MC: Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res 2012, 72:1407-1415.