Ranitidine modifies myeloid cell populations and inhibits breast tumor development and spread in mice

OncoImmunology

Volumn 5, Issue 7, 2016, Pages

  Vila Leahey, Ava ^a   Oldford, Sharon A ^a   Marignani, Paola A ^a   Wang, Jun ^a,b,c   Haidl, Ian D ^a   Marshall, Jean S ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c IWK HEALTH CENTRE   (Canada)

Author keywords

H2 antagonist; histamine; metastasis; monocytes; myeloid cells; myeloid derived suppressor cells; tumor immunology

Indexed keywords

CD11B ANTIGEN; CETIRIZINE; CIMETIDINE; FAMOTIDINE; GEMCITABINE; MEPYRAMINE; RANITIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BREAST CANCER; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; LUNG METASTASIS; MONOCYTE; MOUSE; NONHUMAN; SPLEEN CELL; SUPPRESSOR CELL; TUMOR VOLUME;

EID: 84976582964     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1151591     Document Type: Article

References (85)

1. J.R.Lam, J.L.Schneider, W.Zhao, D.A.Corley. Proton pump inhibitor and histamine 2 receptor antagonist use and vitamin B12 deficiency. Jama 2013; 310:2435-42; PMID:24327038; http://dx.doi.org/10.1001/jama.2013.280490.
2. R.MacLaren, P.M.Reynolds, R.R.Allen. Histamine-2 receptor antagonists vs proton pump inhibitors on gastrointestinal tract hemorrhage and infectious complications in the intensive care unit. JAMA Intern Med 2014; 174:564-74; PMID:24535015; http://dx.doi.org/10.1001/jamainternmed.2013.14673.
3. E.D.Agura, E.Vila, F.B.Petersen, A.F.Shields, E.D.Thomas. The use of ranitidine in bone marrow transplantation. A review of 223 cases. Transplantation 1988; 46:53-6; PMID:3293286; http://dx.doi.org/10.1097/00007890-198807000-00008.
4. A.F.List, D.H.Beaird, T.Kummet. Ranitidine-induced granulocytopenia:recurrence with cimetidine administration. Ann Intern Med 1988; 108:566-7; PMID:3348565; http://dx.doi.org/10.7326/0003-4819-108-4-566.
5. G.P.Cricco, N.A.Mohamad, L.A.Sambuco, F.Genre, M.Croci, A.S.Gutierrez, V.A.Medina, R.M.Bergoc, E.S.Rivera, G.A.Martin. Histamine regulates pancreatic carcinoma cell growth through H3 and H4 receptors. Inflamm Res 2008; 57 Suppl 1:S23-4; PMID:18345506; http://dx.doi.org/10.1007/s00011-007-0611-5.
6. K.Boer, E.Helinger, A.Helinger, P.Pocza, Z.Pos, P.Demeter, Z.Baranyai, K.Dede, Z.Darvas, A.Falus. Decreased expression of histamine H1 and H4 receptors suggests disturbance of local regulation in human colorectal tumours by histamine. Eur J Cell Biol 2008; 87:227-36; PMID:18258331; http://dx.doi.org/10.1016/j.ejcb.2007.12.003.
7. H.Francis, S.DeMorrow, J.Venter, P.Onori, M.White, E.Gaudio, T.Francis, J.F.Greene, Jr, S.Tran, C.J.Meininger et al. Inhibition of histidine decarboxylase ablates the autocrine tumorigenic effects of histamine in human cholangiocarcinoma. Gut 2012; 61:753-64; PMID:21873469; http://dx.doi.org/10.1136/gutjnl-2011-300007.
8. V.A.Medina, E.S.Rivera. Histamine receptors and cancer pharmacology. Br J Pharmacol 2010; 161:755-67; PMID:20636392; http://dx.doi.org/10.1111/j.1476-5381.2010.00961.x.
9. M.Jutel, K.Blaser, C.A.Akdis. Histamine receptors in immune regulation and allergen-specific immunotherapy. Immunol Allergy Clin North Am 2006; 26:245-59, vii; PMID:16701143; http://dx.doi.org/10.1016/j.iac.2006.02.006.
10. J.C.Porretti, N.A.Mohamad, G.A.Martin, G.P.Cricco. Fibroblasts induce epithelial to mesenchymal transition in breast tumor cells which is prevented by fibroblasts treatment with histamine in high concentration. Int J Biochem Cell Biol 2014; 51:29-38; PMID:24685678; http://dx.doi.org/10.1016/j.biocel.2014.03.016.
11. G.P.Cricco, C.A.Davio, G.Martin, N.Engel, C.P.Fitzsimons, R.M.Bergoc, E.S.Rivera. Histamine as an autocrine growth factor in experimental mammary carcinomas. Agents Actions 1994; 43:17-20; PMID:7741034; http://dx.doi.org/10.1007/BF02005757.
12. V.Medina, G.Cricco, M.Nunez, G.Martin, N.Mohamad, F.Correa-Fiz, F.Sanchez-Jimenez, R.Bergoc, E.S.Rivera. Histamine-mediated signaling processes in human malignant mammary cells. Cancer Biol Ther 2006; 5:1462-71; PMID:17012845; http://dx.doi.org/10.4161/cbt.5.11.3273.
13. H.Tonnesen, U.Knigge, S.Bulow, P.Damm, K.Fischerman, P.Hesselfeldt, A.Hjortrup, I.K.Pedersen, V.M.Pedersen, O.J.Siemssen et al. Effect of cimetidine on survival after gastric cancer. Lancet 1988; 2:990-2; PMID:2902494; http://dx.doi.org/10.1016/S0140-6736(88)90743-X.
14. C.Burtin, C.Noirot, P.Scheinmann, L.Galoppin, D.Sabolovic, P.Bernard. Clinical improvement in advanced cancer disease after treatment combining histamine and H2-antihistaminics (ranitidine or cimetidine). Eur J Cancer Clin Oncol 1988; 24:161-7; PMID:3356203; http://dx.doi.org/10.1016/0277-5379(88)90247-7.
15. E.Bolton, J.King, D.L.Morris. H2-antagonists in the treatment of colon and breast cancer. Semin Cancer Biol 2000; 10:3-10; PMID:10888265; http://dx.doi.org/10.1006/scbi.2000.0301.
16. K.Kim, A.D.Skora, Z.Li, Q.Liu, A.J.Tam, R.L.Blosser, L.A.Diaz, Jr., N.Papadopoulos, K.W.Kinzler, B.Vogelstein et al. Eradication of metastatic mouse cancers resistant to immune checkpoint blockade by suppression of myeloid-derived cells. Proc Natl Acad Sci U S A 2014; 111:11774-9; PMID:25071169; http://dx.doi.org/10.1073/pnas.1410626111.
17. P.Sinha, V.K.Clements, S.Ostrand-Rosenberg. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J Immunol 2005; 174:636-45; http://dx.doi.org/10.4049/jimmunol.174.2.636.
18. H.Li, Y.Han, Q.Guo, M.Zhang, X.Cao. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-β 1. J Immunol 2009; 182:240-9; PMID:19109155; http://dx.doi.org/10.4049/jimmunol.182.1.240.
19. B.Hoechst, T.Voigtlaender, L.Ormandy, J.Gamrekelashvili, F.Zhao, H.Wedemeyer, F.Lehner, M.P.Manns, T.F.Greten, F.Korangy. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009; 50:799-807; PMID:19551844; http://dx.doi.org/10.1002/hep.23054.
20. I.Poschke, Y.Mao, L.Adamson, F.Salazar-Onfray, G.Masucci, R.Kiessling. Myeloid-derived suppressor cells impair the quality of dendritic cell vaccines. Cancer Immunol Immunother 2012; 61:827-38; PMID:22080405; http://dx.doi.org/10.1007/s00262-011-1143-y.
21. S.Watanabe, K.Deguchi, R.Zheng, H.Tamai, L.X.Wang, P.A.Cohen, S.Shu. Tumor-induced CD11b+Gr-1+ myeloid cells suppress T cell sensitization in tumor-draining lymph nodes. J Immunol 2008; 181:3291-300; PMID:18714001; http://dx.doi.org/10.4049/jimmunol.181.5.3291.
22. K.Movahedi, M.Guilliams, J.Van den Bossche, R.Van den Bergh, C.Gysemans, A.Beschin, P.De Baetselier, J.A.Van Ginderachter. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008; 111:4233-44; PMID:18272812; http://dx.doi.org/10.1182/blood-2007-07-099226.
23. B.Huang, P.Y.Pan, Q.Li, A.I.Sato, D.E.Levy, J.Bromberg, C.M.Divino, S.H.Chen. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 2006; 66:1123-31; PMID:16424049; http://dx.doi.org/10.1158/0008-5472.CAN-05-1299.
24. E.Suzuki, V.Kapoor, A.S.Jassar, L.R.Kaiser, S.M.Albelda. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res 2005; 11:6713-21; PMID:16166452; http://dx.doi.org/10.1158/1078-0432.CCR-05-0883.
25. M.Tongu, N.Harashima, H.Monma, T.Inao, T.Yamada, H.Kawauchi, M.Harada. Metronomic chemotherapy with low-dose cyclophosphamide plus gemcitabine can induce anti-tumor T cell immunity in vivo. Cancer Immunol Immunother 2013; 62:383-91; PMID:22926062; http://dx.doi.org/10.1007/s00262-012-1343-0.
26. J.Vincent, G.Mignot, F.Chalmin, S.Ladoire, M.Bruchard, A.Chevriaux, F.Martin, L.Apetoh, C.Rebe, F.Ghiringhelli. Five-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 2010; 70:3052-61; PMID:20388795; http://dx.doi.org/10.1158/0008-5472.CAN-09-3690.
27. R.Wesolowski, J.Markowitz, W.E.Carson, 3rd. Myeloid derived suppressor cells - a new therapeutic target in the treatment of cancer. J Immunother Cancer 2013; 1:10; PMID:24829747; http://dx.doi.org/10.1186/2051-1426-1-10.
28. S.Ostrand-Rosenberg, P.Sinha. Myeloid-derived suppressor cells:linking inflammation and cancer. J Immunol 2009; 182:4499-506; PMID:19342621; http://dx.doi.org/10.4049/jimmunol.0802740.
29. A.Mazzoni, H.A.Young, J.H.Spitzer, A.Visintin, D.M.Segal. Histamine regulates cytokine production in maturing dendritic cells, resulting in altered T cell polarization. J Clin Invest 2001; 108:1865-73; PMID:11748270; http://dx.doi.org/10.1172/JCI200113930.
30. T.C.van der Pouw Kraan, A.Snijders, L.C.Boeije, E.R.de Groot, A.E.Alewijnse, R.Leurs, L.A.Aarden. Histamine inhibits the production of interleukin-12 through interaction with H2 receptors. J Clin Invest 1998; 102:1866-73; PMID:9819373; http://dx.doi.org/10.1172/JCI3692.
31. J.Zhang, H.K.Takahashi, K.Liu, H.Wake, R.Liu, H.Sadamori, H.Matsuda, T.Yagi, T.Yoshino, S.Mori et al. Histamine inhibits adhesion molecule expression in human monocytes, induced by advanced glycation end products, during the mixed lymphocyte reaction. Br J Pharmacol 2010; 160:1378-86; PMID:20590628; http://dx.doi.org/10.1111/j.1476-5381.2010.00800.x.
32. W.Dawicki, D.W.Jawdat, N.Xu, J.S.Marshall. Mast cells, histamine, and IL-6 regulate the selective influx of dendritic cell subsets into an inflamed lymph node. J Immunol 2010; 184:2116-23; PMID:20083654; http://dx.doi.org/10.4049/jimmunol.0803894.
33. A.Asea, S.Hermodsson, K.Hellstrand. Histaminergic regulation of natural killer cell-mediated clearance of tumour cells in mice. Scand J Immunol 1996; 43:9-15; PMID:8560202; http://dx.doi.org/10.1046/j.1365-3083.1996.d01-14.x.
34. K.Hellstrand, A.Asea, S.Hermodsson. Role of histamine in natural killer cell-mediated resistance against tumor cells. J Immunol 1990; 145:4365-70; PMID:2147942
35. M.Jutel, T.Watanabe, S.Klunker, M.Akdis, O.A.Thomet, J.Malolepszy, T.Zak-Nejmark, R.Koga, T.Kobayashi, K.Blaser et al. Histamine regulates T-cell and antibody responses by differential expression of H1 and H2 receptors. Nature 2001; 413:420-5; PMID:11574888; http://dx.doi.org/10.1038/35096564.
36. N.Osna, K.Elliott, M.M.Khan. Regulation of interleukin-10 secretion by histamine in TH2 cells and splenocytes. Int Immunopharmacol 2001; 1:85-96; PMID:11367520; http://dx.doi.org/10.1016/S0162-3109(00)00268-X.
37. N.Osna, K.Elliott, M.M.Khan. The effects of histamine on interferon gamma production are dependent on the stimulatory signals. Int Immunopharmacol 2001; 1:135-45; PMID:11367511; http://dx.doi.org/10.1016/S1567-5769(00)00005-9.
38. M.M.Khan, K.M.Keaney, K.L.Melmon, C.Clayberger, A.M.Krensky. Histamine regulates the generation of human cytolytic T lymphocytes. Cell Immunol 1989; 121:60-73; PMID:2541932; http://dx.doi.org/10.1016/0008-8749(89)90005-1.
39. X.D.Yang, W.Ai, S.Asfaha, G.Bhagat, R.A.Friedman, G.Jin, H.Park, B.Shykind, T.G.Diacovo, A.Falus et al. Histamine deficiency promotes inflammation-associated carcinogenesis through reduced myeloid maturation and accumulation of CD11b+Ly6G+ immature myeloid cells. Nat Med 2011; 17:87-95; PMID:21170045; http://dx.doi.org/10.1038/nm.2278.
40. Y.Zheng, M.Xu, X.Li, J.Jia, K.Fan, G.Lai. Cimetidine suppresses lung tumor growth in mice through proapoptosis of myeloid-derived suppressor cells. Mol Immunol 2013; 54:74-83; PMID:23220070; http://dx.doi.org/10.1016/j.molimm.2012.10.035.
41. R.K.Martin, S.J.Saleem, L.Folgosa, H.B.Zellner, S.R.Damle, G.K.Nguyen, J.J.Ryan, H.D.Bear, A.M.Irani, D.H.Conrad. Mast cell histamine promotes the immunoregulatory activity of myeloid-derived suppressor cells. J Leukoc Biol 2014; 96:151-9; PMID:24610880; http://dx.doi.org/10.1189/jlb.5A1213-644R.
42. H.K.Le, L.Graham, E.Cha, J.K.Morales, M.H.Manjili, H.D.Bear. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int Immunopharmacol 2009; 9:900-9; PMID:19336265; http://dx.doi.org/10.1016/j.intimp.2009.03.015.
43. B.Lemos, C.Davio, H.Gass, P.Gonzalez, G.Cricco, G.Martin, R.Bergoc, E.Rivera. Histamine receptors in human mammary gland, different benign lesions and mammary carcinomas. Inflamm Res 1995; 44 Suppl 1:S68-9; PMID:8521007; http://dx.doi.org/10.1007/BF01674400.
44. V.Bronte, P.Serafini, C.De Santo, I.Marigo, V.Tosello, A.Mazzoni, D.M.Segal, C.Staib, M.Lowel, G.Sutter et al. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J Immunol 2003; 170:270-8; PMID:12496409; http://dx.doi.org/10.4049/jimmunol.170.1.270.
45. P.Sinha, V.K.Clements, A.M.Fulton, S.Ostrand-Rosenberg. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 2007; 67:4507-13; PMID:17483367; http://dx.doi.org/10.1158/0008-5472.CAN-06-4174.
46. S.A.Gujar, D.Clements, R.Dielschneider, E.Helson, P.Marcato, P.W.Lee. Gemcitabine enhances the efficacy of reovirus-based oncotherapy through anti-tumour immunological mechanisms. Br J Cancer 2014; 110:83-93; PMID:24281006; http://dx.doi.org/10.1038/bjc.2013.695.
47. R.Andrade-Vieira, Z.Xu, P.Colp, P.A.Marignani. Loss of LKB1 expression reduces the latency of ErbB2-mediated mammary gland tumorigenesis, promoting changes in metabolic pathways. PloS One 2013; 8:e56567; PMID:23451056; http://dx.doi.org/10.1371/journal.pone.00-56567.
48. K.Hellstrand, A.Asea, C.Dahlgren, S.Hermodsson. Histaminergic regulation of NK cells. Role of monocyte-derived reactive oxygen metabolites. J Immunol 1994; 153:4940-7; PMID:7963557
49. M.Hansson, S.Hermodsson, M.Brune, U.H.Mellqvist, P.Naredi, A.Betten, K.R.Gehlsen, K.Hellstrand. Histamine protects T cells and natural killer cells against oxidative stress. J Interferon Cytokine Res 1999; 19:1135-44; PMID:10547153; http://dx.doi.org/10.1089/107999099313073.
50. S.S.Agarwala, J.Glaspy, S.J.O'Day, M.Mitchell, J.Gutheil, E.Whitman, R.Gonzalez, E.Hersh, L.Feun, R.Belt et al. Results from a randomized phase III study comparing combined treatment with histamine dihydrochloride plus interleukin-2 versus interleukin-2 alone in patients with metastatic melanoma. J Clin Oncol 2002; 20:125-33; PMID:11773161; http://dx.doi.org/10.1200/JCO.20.1.125.
51. P.F.Bowrey, J.King, C.Magarey, P.Schwartz, P.Marr, E.Bolton, D.L.Morris. Histamine, mast cells and tumour cell proliferation in breast cancer:does preoperative cimetidine administration have an effect? Br J Cancer 2000; 82:167-70; PMID:10638985; http://dx.doi.org/10.1054/bjoc.1999.0895.
52. C.L.Hsu, C.H.Chang, J.W.Lin, L.C.Wu, L.M.Chuang, M.S.Lai. Histamine-2 receptor antagonists and risk of lung cancer in diabetic patients - an exploratory analysis. Pharmacoepidemiol Drug Saf 2013; 22:632-40; PMID:23576472; http://dx.doi.org/10.1002/pds.3441.
53. C.T.Seto, P.Jeraldo, R.Orenstein, N.Chia, J.K.DiBaise. Prolonged use of a proton pump inhibitor reduces microbial diversity:implications for Clostridium difficile susceptibility. Microbiome 2014; 2:42; PMID:25426290; http://dx.doi.org/10.1186/2049-2618-2-42.
54. N.Arpaia, C.Campbell, X.Fan, S.Dikiy, J.van der Veeken, P.deRoos, H.Liu, J.R.Cross, K.Pfeffer, P.J.Coffer et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013; 504:451-5; PMID:24226773; http://dx.doi.org/10.1038/nature12726.
55. H.J.Wu, I.I.Ivanov, J.Darce, K.Hattori, T.Shima, Y.Umesaki, D.R.Littman, C.Benoist, D.Mathis. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010; 32:815-27; PMID:20620945; http://dx.doi.org/10.1016/j.immuni.2010.06.001.
56. J.R.Lakritz, T.Poutahidis, S.Mirabal, B.J.Varian, T.Levkovich, Y.M.Ibrahim, J.M.Ward, E.C.Teng, B.Fisher, N.Parry et al. Gut bacteria require neutrophils to promote mammary tumorigenesis. Oncotarget 2015; 6:9387-96; PMID:25831236; http://dx.doi.org/10.18632/oncotarget.3328.
57. W.Goh, I.Sleptsova-Freidrich, N.Petrovic. Use of proton pump inhibitors as adjunct treatment for triple-negative breast cancers. An introductory study. J Pharm Pharm Sci 2014; 17:439-46; PMID:25224353.
58. U.H.Jin, S.O.Lee, C.Pfent, S.Safe. The aryl hydrocarbon receptor ligand omeprazole inhibits breast cancer cell invasion and metastasis. BMC Cancer 2014; 14:498; PMID:25011475; http://dx.doi.org/10.1186/1471-2407-14-498.
59. R.Z.Panni, D.C.Linehan, D.G.DeNardo. Targeting tumor-infiltrating macrophages to combat cancer. Immunotherapy 2013; 5:1075-87; PMID:24088077; http://dx.doi.org/10.2217/imt.13.102.
60. R.Ward, A.H.Sims, A.Lee, C.Lo, L.Wynne, H.Yusuf, H.Gregson, M.P.Lisanti, F.Sotgia, G.Landberg et al. Monocytes and macrophages, implications for breast cancer migration and stem cell-like activity and treatment. Oncotarget 2015; 6:14687-99.
61. S.K.Sharma, N.K.Chintala, S.K.Vadrevu, J.Patel, M.Karbowniczek, M.M.Markiewski. Pulmonary alveolar macrophages contribute to the premetastatic niche by suppressing antitumor T cell responses in the lungs. J Immunol 2015; 194:5529-38; http://dx.doi.org/10.4049/jimmunol.1403215; PMID:26008983; http://dx.doi.org/10.18632/oncotarget.4189
62. L.A.Haile, J.Gamrekelashvili, M.P.Manns, F.Korangy, T.F.Greten. CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice. J Immunol 2010; 185:203-10; PMID:20525890; http://dx.doi.org/10.4049/jimmunol.0903573.
63. K.Oh, O.Y.Lee, S.Y.Shon, O.Nam, P.M.Ryu, M.W.Seo, D.S.Lee. A mutual activation loop between breast cancer cells and myeloid-derived suppressor cells facilitates spontaneous metastasis through IL-6 trans-signaling in a murine model. Breast Cancer Res 2013; 15:R79; PMID:24021059; http://dx.doi.org/10.1186/bcr3473.
64. L.Y.OuYang, X.J.Wu, S.B.Ye, R.X.Zhang, Z.L.Li, W.Liao, Z.Z.Pan, L.M.Zheng, X.S.Zhang, Z.Wang et al. Tumor-induced myeloid-derived suppressor cells promote tumor progression through oxidative metabolism in human colorectal cancer. J Transl Med 2015; 13:47; PMID:25638150; http://dx.doi.org/10.1186/s12967-015-0410-7.
65. C.Bergenfelz, A.M.Larsson, K.von Stedingk, S.Gruvberger-Saal, K.Aaltonen, S.Jansson, H.Jernstrom, H.Janols, M.Wullt, A.Bredberg et al. Systemic Monocytic-MDSCs Are Generated from Monocytes and Correlate with Disease Progression in Breast Cancer Patients. PloS One 2015; 10:e0127028; PMID:25992611; http://dx.doi.org/10.1371/journal.pone.0127028.
66. S.J.Saleem, R.K.Martin, J.K.Morales, J.L.Sturgill, D.R.Gibb, L.Graham, H.D.Bear, M.H.Manjili, J.J.Ryan, D.H.Conrad. Cutting edge:mast cells critically augment myeloid-derived suppressor cell activity. J Immunol 2012; 189:511-5; PMID:22706087; http://dx.doi.org/10.4049/jimmunol.1200647.
67. C.A.Corzo, M.J.Cotter, P.Cheng, F.Cheng, S.Kusmartsev, E.Sotomayor, T.Padhya, T.V.McCaffrey, J.C.McCaffrey, D.I.Gabrilovich. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 2009; 182:5693-701; PMID:19380816; http://dx.doi.org/10.4049/jimmunol.0900092.
68. J.Schmielau, O.J.Finn. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res 2001; 61:4756-60; PMID:11406548.
69. J.Zhu, X.Huang, Y.Yang. Myeloid-derived suppressor cells regulate natural killer cell response to adenovirus-mediated gene transfer. J Virol 2012; 86:13689-96; PMID:23055553; http://dx.doi.org/10.1128/JVI.01595-12.
70. S.Nagaraj, K.Gupta, V.Pisarev, L.Kinarsky, S.Sherman, L.Kang, D.L.Herber, J.Schneck, D.I.Gabrilovich. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med 2007; 13:828-35; PMID:17603493; http://dx.doi.org/10.1038/nm1609.
71. M.Terabe, S.Matsui, J.M.Park, M.Mamura, N.Noben-Trauth, D.D.Donaldson, W.Chen, S.M.Wahl, S.Ledbetter, B.Pratt et al. Transforming growth factor-β production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance:abrogation prevents tumor recurrence. J Exp Med 2003; 198:1741-52; PMID:14657224; http://dx.doi.org/10.1084/jem.20022227.
72. S.Fichtner-Feigl, M.Terabe, A.Kitani, C.A.Young, I.Fuss, E.K.Geissler, H.J.Schlitt, J.A.Berzofsky, W.Strober. Restoration of tumor immunosurveillance via targeting of interleukin-13 receptor-α 2. Cancer Res 2008; 68:3467-75; PMID:18451175; http://dx.doi.org/10.1158/0008-5472.CAN-07-5301.
73. P.Filipazzi, R.Valenti, V.Huber, L.Pilla, P.Canese, M.Iero, C.Castelli, L.Mariani, G.Parmiani, L.Rivoltini. Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J Clin Oncol 2007; 25:2546-53; PMID:17577033; http://dx.doi.org/10.1200/JCO.2006.08.5829.
74. N.Weizman, Y.Krelin, A.Shabtay-Orbach, M.Amit, Y.Binenbaum, R.J.Wong, Z.Gil. Macrophages mediate gemcitabine resistance of pancreatic adenocarcinoma by upregulating cytidine deaminase. Oncogene 2014; 33:3812-9; PMID:23995783; http://dx.doi.org/10.1038/onc.2013.357.
75. A.Perez-Diez, N.T.Joncker, K.Choi, W.F.Chan, C.C.Anderson, O.Lantz, P.Matzinger. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 2007; 109:5346-54; PMID:17327412; http://dx.doi.org/10.1182/blood-2006-10-051318.
76. H.Tsukamoto, R.Nishikata, S.Senju, Y.Nishimura. Myeloid-derived suppressor cells attenuate TH1 development through IL-6 production to promote tumor progression. Cancer Immunol Res 2013; 1:64-76; PMID:24777249; http://dx.doi.org/10.1158/2326-6066.CIR-13-0030.
77. K.R.Crook, M.Jin, M.F.Weeks, R.R.Rampersad, R.M.Baldi, A.S.Glekas, Y.Shen, D.A.Esserman, P.Little, T.A.Schwartz et al. Myeloid-derived suppressor cells regulate T cell and B cell responses during autoimmune disease. J Leukoc Biol 2015; 97:573-82; PMID:25583578; http://dx.doi.org/10.1189/jlb.4A0314-139R.
78. B.Hoechst, L.A.Ormandy, M.Ballmaier, F.Lehner, C.Kruger, M.P.Manns, T.F.Greten, F.Korangy. A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 2008; 135:234-43; PMID:18485901; http://dx.doi.org/10.1053/j.gastro.2008.03.020.
79. H.Watanabe, K.Numata, T.Ito, K.Takagi, A.Matsukawa. Innate immune response in Th1- and Th2-dominant mouse strains. Shock 2004; 22:460-6; PMID:15489639; http://dx.doi.org/10.1097/01.shk.0000142249.08135.e9.
80. X.Chen, J.J.Oppenheim, O.M.Howard. BALB/c mice have more CD4+CD25+ T regulatory cells and show greater susceptibility to suppression of their CD4+CD25- responder T cells than C57BL/6 mice. J Leukoc Biol 2005; 78:114-21; PMID:15845645; http://dx.doi.org/10.1189/jlb.0604341.
81. B.A.Pulaski, S.Ostrand-Rosenberg. Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7.1 cell-based tumor vaccines. Cancer Res 1998; 58:1486-93; PMID:9537252.
82. B.Z.Qian, J.Li, H.Zhang, T.Kitamura, J.Zhang, L.R.Campion, E.A.Kaiser, L.A.Snyder, J.W.Pollard. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011; 475:222-5; PMID:21654748; http://dx.doi.org/10.1038/nature10138.
83. M.Vehabovic, S.Hadzovic, F.Stambolic, A.Hadzic, E.Vranjes, E.Haracic. Stability of ranitidine in injectable solutions. Int J Pharm 2003; 256:109-15; PMID:12695016; http://dx.doi.org/10.1016/S0378-5173(03)00067-X.
84. L.S.Bullock, J.F.Fitzgerald, H.I.Mazur. Stability of intravenous famotidine stored in polyvinyl chloride syringes. DICP 1989; 23:588-90; PMID:2763581.
85. B.A.Pulaski, S.Ostrand-Rosenberg. Mouse 4T1 breast tumor model. Curr Protoc Immunol 2001; Chapter 20:Unit 20 2; PMID:18432775; http://dx.doi.org/10.1002/0471142735.im2002s39