CD38-expressing myeloid-derived suppressor cells promote tumor growth in a murine model of esophageal cancer

Cancer Research

Volumn 75, Issue 19, 2015, Pages 4074-4085

  Karakasheva, Tatiana A ^a,b   Waldron, Todd J ^a,b   Eruslanov, Evgeniy ^c   Kim, Sang Bae ^d   Lee, Ju Seog ^d   O'Brien, Shaun ^c   Hicks, Philip D ^a,b   Basu, Devraj ^a,e   Singhal, Sunil ^c,e   Malavasi, Fabio ^f   Rustgi, Anil K ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF TEXAS   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; CD38 ANTIGEN; CXCL16 CHEMOKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; SOMATOMEDIN BINDING PROTEIN 3; ARGINASE; CD38 PROTEIN, HUMAN; CD38 PROTEIN, MOUSE; CYTOKINE; MEMBRANE PROTEIN; NOS2 PROTEIN, MOUSE; TUMOR PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL ISOLATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMOTAXIS; COLONY FORMATION; CONTROLLED STUDY; ESOPHAGUS CANCER; EX VIVO STUDY; HYDROLYSIS; IMMUNOSTIMULATION; MORPHOLOGY; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NEUTROPHIL; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; T LYMPHOCYTE; TUMOR GROWTH; ANIMAL; BIOSYNTHESIS; BLOOD; C57BL MOUSE; CHEMISTRY; DISEASE MODEL; ESOPHAGUS TUMOR; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; MYELOPOIESIS; PATHOLOGY; PHYSIOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; TUMOR ESCAPE; TUMOR STEM CELL ASSAY;

ANIMALS; ANTIGENS, CD38; ARGINASE; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CYTOKINES; DISEASE MODELS, ANIMAL; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; MYELOPOIESIS; NEOPLASM PROTEINS; NITRIC OXIDE SYNTHASE TYPE II; T-LYMPHOCYTES; TUMOR ESCAPE; TUMOR STEM CELL ASSAY;

EID: 84945534119     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3639     Document Type: Article

References (49)

1. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011; 331:1565-70.
2. Waldron T J, Quatromoni G J, Karakasheva T A, Singhal S, Rustgi AK. Myeloid derived suppressor cells: targets for therapy. Oncoimmunology 2013;2:e24117.
3. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
4. Pak AS, Wright MA, Matthews JP, Collins SL, Petruzzelli GJ, Young MR. Mechanisms of immune suppression in patients with head and neck cancer: presence of CD34(+) cells which suppress immune functions within cancers that secrete granulocyte-macrophage colony-stimulating factor. Clin Cancer Res 1995;1:95-103.
5. Gabitass RF, Annels NE, Stocken DD, Pandha HA, Middleton GW. Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the Th2 cytokine interleukin-13. Cancer Immunol Immunother 2011;60:1419-30.
6. Schmielau J, Finn OJ. 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.
7. + T lymphocytes in patients with advanced-stage non-small cell lung cancer. J Cancer Res Clin Oncol 2010;136:35-45.
8. Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 2005; 65:3044-8.
9. Filipazzi P, Valenti R, Huber V, Pilla L, Canese P, Iero M, et al. 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.
10. low/- monocytes in prostate cancer. Prostate 2010;70:443-55.
11. Greten TF, Manns MP, Korangy F. Myeloid derived suppressor cells in human diseases. Int Immunopharmacol 2011;11:802-7.
12. Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells throughmembrane-bound TGFbeta 1. J Immunol 2009;182:240-9.
13. + immature myeloid suppressor cells mediate the development of tumorinduced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 2006;66:1123-31.
14. Rodriguez PC, Zea AH, DeSalvo J, Culotta KS, Zabaleta J, Quiceno DG, et al. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol 2003;171:1232-9.
15. Bingisser RM, Tilbrook PA, Holt PG, Kees UR. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J Immunol 1998;160:5729-34.
16. Harari O, Liao JK. Inhibition of MHC II gene transcription by nitric oxide and antioxidants. Curr Pharm Des 2004;10:893-8.
17. Rivoltini L, Carrabba M, Huber V, Castelli C, Novellino L, Dalerba P, et al. Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol Rev 2002;188:97-113.
18. Patton DT, Wilson MD, Rowan WC, Soond DR, Okkenhaug K. The PI3K p110d regulates expression of CD38 on regulatory T cells. PLoS ONE 2011;6:e17359.
19. + T cells with IFNγ-mediated suppressor activities. PLoS ONE 2012;7:e45234.
20. Blair PA, Noreña LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010;32:129-40.
21. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, Ortolan E, et al. Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev 2008;88:841-86.
22. Lee HC. Cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate (NAADP) as messengers for calcium mobilization. J Biol Chem 2012;287:31633-40.
23. Todisco E, Suzuki T, Srivannaboon K, Coustan-Smith E, Raimondi SC, Behm FG, et al. CD38 ligation inhibits normal and leukemicmyelopoiesis. Blood 2000;95:535-42.
24. Stairs DB, Bayne LJ, Rhoades B, Vega ME, Waldron TJ, Kalabis J, et al. Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell 2011;19:470-83.
25. Opitz O, Harada H, Suliman Y, Rhoades B, Sharpless NE, Kent R, et al. A mouse model of human oral-esophageal cancer. J Clin Invest 2002; 110:761-9.
26. Takaoka M, Harada H, Deramaudt TB, Oyama K, Andl CD, Johnstone CN, et al. Ha-Ras(G12V) induces senescence in primary and immortalized human esophageal keratinocytes with p53 dysfunction. Oncogene 2004; 23:6760-8.
27. Youn J-I, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloidderived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791-802.
28. Partida-Sánchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B, et al. Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat Med 2001;7:1209-16.
29. Partida-Sanchez S, Iribarren P, Moreno-Garcia ME, Gao J-L, Murphy PM, Oppenheimer N, et al. Chemotaxis and calcium responses of phagocytes to formyl peptide receptor ligands is differentially regulated by cyclic ADP ribose. J Immunol 2004;172:1896-906.
30. Malavasi F, Deaglio S, Damle R, Cutrona G, Ferrarini M, Chiorazzi N. CD38 and chronic lymphocytic leukemia: a decade later. Blood 2011;118: 3470-8.
31. Quante M, Bhagat G, Abrams J a, Marache F, Good P, Lee MD, et al. Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell 2012;21:36-51.
32. Aktan F. iNOS-mediated nitric oxide production and its regulation. Life Sci 2004;75:639-53.
33. + glycohydrolase by arabino analogues of beta-NAD. J Biol Chem 1992;267:9606-11.
34. Mayo L, Jacob-Hirsch J, Amariglio N, Rechavi G, Moutin M-J, Lund FE, et al. Dual role of CD38 in microglial activation and activation-induced cell death. J Immunol 2008;181:92-103.
35. Levy A, Blacher E, Vaknine H, Lund FE, Stein R, Mayo L. CD38 deficiency in the tumor microenvironment attenuates glioma progression and modulates features of tumor-associated microglia/macrophages. Neuro Oncol 2012;14:1037-49.
36. Kaku H, Horikawa K, Obata Y, Kato I, Okamoto H, Sakaguchi N, et al. NFkappaB is required for CD38-mediated induction of C(gamma)1 germline transcripts in murine B lymphocytes. Int Immunol 2002;14:1055-64.
37. Xie QW, Kashiwabara Y, Nathan C. Role of transcription factorNF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem 1994;269:4705-8.
38. Sade-Feldman M, Kanterman J, Ish-Shalom E, Elnekave M, Horwitz E, Baniyash M. Tumor necrosis factor-α blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity 2013;38:541-54.
39. Abel S, Hundhausen C, Mentlein R, Schulte A, Berkhout TA, Broadway N, et al. The transmembrane CXC-chemokine ligand 16 is induced by IFN-gamma and TNF-alpha and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J Immunol 2004; 172:6362-72.
40. Seurin D, Lombet A, Babajko S, Godeau F, Ricort J-M. Insulin-like growth factor binding proteins increase intracellular calcium levels in two different cell lines. PLoS One 2013;8:e59323.
41. Sochorová K, Budinský V, Rozková D, Tobiasová Z, Dusilová-Sulková S, Spísek R, et al. Paricalcitol (19-nor-1,25-dihydroxyvitamin D2) and calcitriol (1,25-dihydroxyvitamin D3) exert potent immunomodulatory effects on dendritic cells and inhibit induction of antigen-specific T cells. Clin Immunol 2009;133:69-77.
42. Vukcevic M, Zorzato F, Spagnoli G, Treves S. Frequent calcium oscillations lead to NFAT activation in human immature dendritic cells. J Biol Chem 2010;285:16003-11.
43. Kortylewski M, Kujawski M, Wang T, Wei S, Zhang S, Pilon-Thomas S, et al. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat Med 2005;11:1314-21.
44. Sinha P, Okoro C, Foell D, Freeze HH, Ostrand-Rosenberg S, Srikrishna G. Proinflammatory S100 proteins regulate the accumulation of myeloidderived suppressor cells. J Immunol 2008;181:4666-75.
45. De Weers M, Tai Y-T, van der Veer MS, Bakker JM, Vink T, Jacobs DCH, et al. Daratumumab, a novel therapeutic human CD38 monoclonal antibody, induces killing of multiple myeloma and other hematological tumors. J Immunol 2011;186:1840-8.
46. Stevenson GT. CD38 as a therapeutic target. Mol Med 2006;12:345-6.
47. Laubach JP, Tai Y-T, Richardson PG, Anderson KC. Daratumumab granted breakthrough drug status. Expert Opin Investig Drugs 2014;23:445-52.
48. Marigo I, Dolcetti L, Serafini P, Zanovello P, Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 2008;222:162-79.
49. Chillemi A, Zaccarello G, Quarona V, Ferracin M, Ghimenti C, Massaia M, et al. Anti-CD38 antibody therapy: windows of opportunity yielded by the functional characteristics of the target molecule. Mol Med 2013;19: 99-108.