Neuroblastoma arginase activity creates an immunosuppressive microenvironment that impairs autologous and engineered immunity

Cancer Research

Volumn 75, Issue 15, 2015, Pages 3043-3053

  Mussai, Francis ^a   Egan, Sharon ^b   Hunter, Stuart ^a   Webber, Hannah ^c   Fisher, Jonathan ^d   Wheat, Rachel ^a   McConville, Carmel ^a   Sbirkov, Yordan ^c   Wheeler, Kate ^e   Bendle, Gavin ^a   Petrie, Kevin ^c   Anderson, John ^d   Chesler, Louis ^c   De Santo, Carmela ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; ARGINASE II; CD34 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; GANGLIOSIDE GD2; NY ESO 1 ANTIGEN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; ARGINASE II, HUMAN; ARGININE; CTAG1B PROTEIN, HUMAN; GANGLIOSIDE; GANGLIOSIDE, GD2; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; TUMOR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CONTROLLED STUDY; ENGINEERED IMMUNITY; ENZYME ACTIVITY; ENZYME ANALYSIS; GROWTH INHIBITION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNITY; IMMUNOSURVEILLANCE; LYMPHOCYTE PROLIFERATION; LYMPHOCYTOTOXICITY; MOUSE; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TUMOR MICROENVIRONMENT; ANIMAL; CELL PROLIFERATION; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MORTALITY; PATHOLOGY;

ANIMALS; ANTIGENS, NEOPLASM; ARGINASE; ARGININE; CELL PROLIFERATION; GANGLIOSIDES; HUMANS; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; MICE; NEOPLASMS, EXPERIMENTAL; NEUROBLASTOMA; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT PROTEINS; TUMOR MICROENVIRONMENT;

EID: 84942884570     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3443     Document Type: Article

References (50)

1. Maris J. The biologic basis for neuroblastoma heterogeneity and risk stratification. Curr Opin Pediat 2005; 17: 7-13.
2. Rudnick E, Khakoo Y, Antunes N., Seeger R, Brodeur G, Shimada H., et al. Opsoclonus-myoclonus-ataxia syndrome in neuroblastoma: clinical outcome and anti-neuronal antibodies-a report from the Children's Cancer Group Study. Med Pediatr Oncol 2001; 36: 612-22.
3. Hero B, Simon T, Spitz R., Ernestus K, Gnekow A, Scheel-Walter H, et al. Localized infant neuroblastomas often show spontaneous regression: results of the prospective trials NB95-S and NB97. J Clin Oncol 2008; 26:1504-10.
4. Mujoo K, Kipps T, Yang H., Cheresh D, Wargalla U, Sander D., et al. Functional properties and effect on growth suppression of human neuro-blastoma tumours by isotype switch variants of monoclonal antiganglioside GD2 antibody 14.18. Cancer Res 1989; 49: 2857-61.
5. Pule M, Savoldo B, Myers G., Rossig C, Russell H, Doti G., et al. Virus-specific T cells engineered to coexpress tumour-specific receptors: persistence and anti-tumour activity in individuals with neuroblastoma. Nat Med 2008; 14:1264-70.
6. Simon T, Hero B, Faldum A., Handgretinger R, Schrappe M, Nierthammer D., et al. Consolidation treatment with chimeric anti-GD2-antibody ch1.18 in children older than 1 year with metastatic neuroblastoma. J Clin Oncol 2004; 22: 3549-57.
7. Yu AL, Gilman AL, Ozkaynak M.F., London WB, Kreissman SG, Chen HX, et al Anti-GD2 antibody with GM-CSF, interlukin-2, and isotretinoin for neuroblastoma. N Engl J Med 2010; 363: 1324-34.
8. Pistoia V, Morandi F, Bianchi G., Bezzolo A, Prigione I, Raffaghello L. Immunosuppressive microenvironment in neuroblastoma. Front Oncol 2013; 3: 167.
9. Chen X, Doffek K, Sugg S.L., Shilyansky J. Neuroblastoma cells inhibit the immunostimulatory function of dendritic cells. J Pediatric Surg 2003; 38: 901-5.
10. Mussai F, De Santo C, Abu-Dayyeh I, Booth S., Quek L, McEwen-Smith RM, et al. Acute Myeloid leukaemia creates an arginase dependent immunosuppressive microenvironment. Blood 2013; 122: 749-58.
11. Grody W, Argyle C, Kern R.M., Dizikes GJ, Spector EB, Strickland AD, et al Differential expression of the two human arginase genes in hyperargininemia. J Clin Invest 1989; 83: 602-9.
12. Serafini P, Meckel K, Kelso M., Noonan K, Califano J, Koch W., et al. Phosphodiesterase-5-inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J Exp Med 2006; 27: 2691-02.
13. Gotoh T, Araki M, Mori M. Chromosomal localization of the human arginase II gene and tissue distribution of its mRNA. Biochem Biophys Res Commun 1997; 233: 487-91
14. Quinn JJ, Altman A. The multiple hematologic manifestations of neuroblastoma. Am J Pediatr Hematol Oncol 1979; 1: 201-5.
15. Scott JP, Morgan E. Coagulopathy of disseminated neuroblastoma. J Pediat 1983; 103: 219-222.
16. Terrile M, Bryan K, Vaughan L., Hallsworth A, Webber H, Chesler L., et al. miRNA expression profiling of the murine TH-MYCN neuroblastoma model reveals similarities with human tumors and identifies novel candidate miRNAs. PLoS One 2011; 6: e28356.
17. Zhang Y, Xiang L, Hassan R., Pastan I. Immunotoxin and Taxol synergy results from a decrease in shed mesothelin levels in the extracellular space of tumours. Proc Natl Acad Sci USA 2007; 104: 17099-104.
18. Song L, Asgharzadeh S, Salo J., Engell K, Hong-wei W, Sposto Ret al. Va24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J Clin Inv 2009; 119: 1524-36.
19. Liu D, Song, Wei J, Courney A, Gao X, Marinova E, et al. IL-15 protects NKT cells from inhibition by tumor-associated macrophages and enhances antimetastatic activity. J Clin Invest 2012; 12: 2221-33.
20. Asgharzadeh S, Salo JA, Oberthuer A, Fischer M., Bethold F, Hadjidaniel M, et al Clinical significance of tumor-associated inflammatory cells in metastatic neuroblastoma. J Clin Oncol 2012; 30: 3525-32.
21. Grupp S, Prak EL, Boyer J, McDonald K., Shusterman S, Thompson E, et al Adoptive transfer of autologous T cells improves T-cell repertoire diversity and long-term B cell function in pediatric patients with neuroblastoma. Clin Cancer Res 2012; 18: 6732-41.
22. Rodolfo M, Luksh R, Stockert E., Chen YT, Collini P, Ranzani T, et al Antigen-specific immunity in neuroblastoma patients: antibody and T-cell recognition of NY-ESO-1 tumor antigen. Cancer Res 2003; 63: 6948-55.
23. Jenkinson C, Grody W, Cederbaum S. Comparative properties of arginases. Comp Biochem Physiol B Biochem Mol Biol 1996; 114: 107-32.
24. Morris SM Jr. Recent advances inarginine metabolism: roles and regulation of the arginases. Br J Pharm 2009; 15: 922-30.
25. Huber K. The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Dev Biol 2006; 298: 335-43.
26. De Preter K., Vandesompele J, Heiann P., Yigit N, Beckman S, Schramm A., et al. Human fetal neuroblast and neuroblastoma transcriptome analysis confirms neuroblast origin and highlights neuroblastoma candidate genes. Genome Biol 2006; 7: R84.
27. Braissant O, Gotoh T, Loup M., Mori M, Backmann C. L-arginine uptake, the citrulline-NO cycle and arginase II in the rat brain: an in situ hybridisation study. Brain Res Mol Brain Res 1999; 70: 231-41.
28. Wiesinger H. Arginine metabolism and the synthesis of nitric oxide in the nervous system. Prog Neurobiol 2001; 64: 365-91.
29. R2: microarray analysis and visualization platform'. Available from: http://r2.amc.nl.
30. Mussai F, De Santo C, Cerundolo V. Interaction between iNKT cells and MDSCs in cancer patients: Evidence and Therapeutic Opportunities. J Immunother 2012; 35: 449-59.
31. Ino Y, Yamazaki-Itoh R, Oguro S., Shimada K, Kosuge T, Zavada J., et al. Arginase II expressed in cancer-associated fibroblasts indicates tissue hypoxia and predicts poor outcome in patients with pancreatic cancer. PLoS One 2013; 8: e55146.
32. Rotondo R, Mastracci L, Piazza T., Barisione G, Fabbi M, Cassanello M., et al. Arginase 2 is expressed by human lung cancer, but it neither induces immune suppression, nor affects disease progression. Int J Cancer 2008; 123:1108-16.
33. Bron L, Jandus C, Andrejevic-Blant S, Speiser D.E., Monnier P., Romero P. Rivals JP. Prognostic value of arginase-II expression and regulatory T-cell infiltration in head and neck squamous cell carcinoma. Int J Cancer 2013; 132:E85-93.
34. Borsheim E, Kobayashi H, Traber D.L., Wolfe RR. Compartmental distribution of amino acids during hemodialysis-induced hypoaminoacidemeina. Am J Physiology Endocrinol Metab 2006; 290: e643-E652.
35. Lofberg E, Essen P, McNurlan M., Wernerman J, Garlick P, Anderstam B., et al. Effect of hemodialysis on protein synthesis. Clin Nephrol 2000; 54: 284-94.
36. Green GJ, Weitzmann SS, Pencharz PB Resting energy expenditure in children newly diagnosed with stage IV neuroblastoma. Pediatr Res 2008; 63:332-36.
37. Buijs N, Luttikhold J, Houdijk A.P., van Leeuwen PA. The role of a disturbed arginine/NO metabolism in the onset of cancer cachexia: a working hypothesis. Curr Med Chem 2012; 19: 5278-86.
38. Hasim A, Aili A, Maimaiti A., Mamtimin B, Abudula A, Upur H. Plasma-free amino acid profiling of cervical cancer and cervical intraepithelial neoplasia patients and its application for early detection. Mol Biol Rep. 2013; 40: 5853-59.
39. Rodriguez P, Ernstoff M, Hernandez C., Atkins M, Zabaleta J, Sierra R., et al. Arginase I-producing myeloid derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res 2009; 69:1553-60.
40. Lin SE, Wu Fl, Wei M.F., Shen LJ. Depletion of arginine by recombinant arginine deiminase induces nNOS-activated neurotoxicity in neuroblastoma cells. Biomed Res Int 2014; 2014: 589424.
41. Morris SM Jr. Arginine metabolism: boundaries of our knowledge. J Nutr 2007; 137: 1602S-1609S.
42. Rodriguez PC, Quiceno DG, Ochoa AC L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood 2007; 109: 1568-73.
43. Zea AH, Rodriguez PC, Culotta K.S., Hernandez CP, DeSalvo J, Ochoa JB, et al L-arginine modulates CD3zeta expression and T cell function in activated human T lymphocytes. Cell Immunol. 2004; 232: 21-31.
44. Apps JR, Hasan F, Campus O., Behjati S, Jacques TS, Sebire N, et al The immune environment of paediatric and solid malignancies: evidence from an immunohistochemical study of clinical cases. Fetal Pediatr Pathol 2013; 32: 298-07.
45. Santilli G, Piotrowska I, Cantilena S.A., Chayka O., D'Alicarnasso M, Morgenstern DA, et al Polyphenon E enhances the antitumor immune response in neuroblastoma by inactivating myeloid suppressor cells. Clin Cancer Res 2013; 19: 1116-25.
46. Barr KM, Jing W, Hallett W.H., Gershan JA, Johnson BD. Examining T cells at vaccine sites of tumor-bearing hosts provides insights to dysfunctional T-cell immunity. J Immunother 2013; 36: 41-51.
47. Bowman L, Grossmann M, Rill D., Brown M, Zhong WY, Alexander B, et al IL-2 adenovector transduced autologous tumor cells induce antitumor immune responses in patients with neuroblastoma. Blood 1998; 92: 1941-49.
48. Rodolfo M, Luksch R, Stockert E., Chen YT, Collini P, Ranzani T, et al Antigen-specific immunity in neuroblastoma patients: antibody and T-cell recognition of NY-ESO-1 tumour antigen. Cancer Res 2003; 63: 6948-55.
49. Sun J, Dotti G, Huye L.E., Foster AE, Savoldo B, Gramatges MM, et al T cells expressing constitutively active Akt resist multiple tumor-associated inhibitory mechanisms. Mol Ther 2010; 18: 2006-17.
50. Lieberman M, Nishioka K, Redmond H., Daly J. Enhancement of interlukin-2 immunotherapy with L-arginine. Ann Surg 1992; 215: 157-65.