Immunosuppressive activity enhances central carbon metabolism and bioenergetics in myeloid-derived suppressor cells in vitro models

BMC Cell Biology

Volumn 13, Issue , 2012, Pages

  Hammami, Ines ^a   Chen, Jingkui ^a   Murschel, Frederic ^a   Bronte, Vincenzo ^b   De Crescenzo, Gregory ^a   Jolicoeur, Mario ^a  

^a ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

^b UNIVERSITY OF VERONA   (Italy)

Author keywords

Bioenergetics; Central carbon metabolism; GM CSF; IL 6; MSC 1 cells; Myeloid derived suppressor cells

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ARGINASE 1; ARGININE; GLUCOSE; GLUTAMINE; GRANULOCYTE COLONY STIMULATING FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INDUCIBLE NITRIC OXIDE SYNTHASE;

AMINO ACID SYNTHESIS; ANAEROBIC GLYCOLYSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOACCUMULATION; BIOENERGY; BIOLOGICAL MONITORING; BONE MARROW CELL; CARBON METABOLISM; CELL FUNCTION; CELL IMMORTALIZATION; CELL MATURATION; CELL METABOLISM; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IMMUNE DEFICIENCY; IMMUNOPATHOGENESIS; IN VITRO STUDY; MALE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; NUTRIENT UPTAKE; PROTEIN FUNCTION; UPREGULATION;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ARGININE; BONE MARROW CELLS; CELLS, CULTURED; ENERGY METABOLISM; GLUCOSE; GLUTAMINE; GLYCOLYSIS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNOSUPPRESSION; INTERLEUKIN-6; MYELOID CELLS;

EID: 84863224448     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-13-18     Document Type: Article

References (48)

1. Obermueller E, Vosseler S, Fusenig NE, Mueller MM. Cooperative autocrine and paracrine functions of granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor in the progression of skin carcinoma cells. Cancer Res 2004, 64(21):7801-7812.
2. Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S, Schreiber H. The terminology issue for myeloid-derived suppressor cells. Cancer Res 2007, 67(1):425. author reply 426.
3. Serafini, Borrello I, Bronte V. Myeloid suppressor cells in cancer: Recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol 2006, 16(1):53-65.
4. Buttgereit F, Burmester GR, Brand MD. Bioenergetics of immune functions: fundamental and therapeutic aspects. Immunol Today 2000, 21(4):192-199.
5. Marigo I, Bosio E, Solito S, Mesa C, Fernandez A, Dolcetti L, Ugel S, Sonda N, Bicciato S, Falisi E, et al. Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 2010, 32(6):790-802.
6. Dolcetti L, Peranzoni E, Ugel S, Marigo I, Fernandez Gomez A, Mesa C, Geilich M, Winkels G, Traggiai E, Casati A, et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 2010, 40(1):22-35.
7. Hammami I, Chen J, Bronte V, De Crescenzo G, Jolicoeur M. Myeloid-derived suppressor cells exhibit two bioenergetic steady-states in vitro. J Biotechnol 2011, 152(1-2):43-48.
8. Apolloni E, Bronte V, Mazzoni A, Serafini P, Cabrelle A, Segal DM, Young HA, zanovello P. Immortalized myeloid suppressor cells trigger apoptosis in antigen-activated T lymphocytes. J Immunol 2000, 165:6723-6730.
9. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, Knowles RG. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 1997, 272(8):4959-4963.
10. Berkowitz DE, White R, Li D, Minhas KM, Cernetich A, Kim S, Burke S, Shoukas AA, Nyhan D, Champion HC, et al. Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels. Circulation 2003, 108(16):2000-2006.
11. Kim N, Cox J, Baggio R, Emig F, Mistry S, Harper S, Speicher D, Morris SJ, Ash D, Traish A, et al. Probing erectile function: S-(2-bronoethyl)-L-cysteine binds to arginase as a transition state analogue and enhances smooth muscle relaxation in human penile corpus cavernosum. Biochemistry 2001, 40(9):2678-2688.
12. Farley KS, Wang LF, Law C, Mehta S. Alveolar macrophage inducible nitric oxide synthase-dependent pulmonary microvascular endothelial cell septic barrier dysfunction. Microvasc Res 2008, 76(3):208-216.
13. Cavicchi M, Whittle BJ. Potentiation of cytokine induced iNOS expression in the human intestinal epithelial cell line, DLD-1, by cyclic AMP. Gut 1999, 45(3):367-374.
14. Toque HA, Tostes RC, Yao L, Xu Z, Webb RC, Caldwell RB, Caldwell RW. Arginase II Deletion Increases Corpora Cavernosa Relaxation in Diabetic Mice. J Sex Med 2010, 8:3335-3344.
15. Colleluori DM, Ash DE. Classical and slow-binding inhibitors of human type II arginase. Biochemistry 2001, 40(31):9356-9362.
16. Atkinson DE. Cellular Energy Metabolism and its Regulation 1977, USA: Proceedings of the National Academy of Science.
17. McMurray-Beaulieu V, Hisiger S, Durand C, Perrier M, Jolicoeur M. Na-butyrate sustains energetic states of metabolism and t-PA productivity of CHO cells. J Biosci Bioeng 2009, 108(2):160-167.
18. Reich JG, Sel'Kov EE. Energy metabolism of the cell - a theoritical treatise 1981, London: Academic.
19. Cidad P, Almeida A, Bolanos JP. Inhibition of mitochondrial respiration by nitric oxide rapidly stimulates cytoprotective GLUT3-mediated glucose uptake through 5'-AMP-activated protein kinase. Biochem J 2004, 384(Pt 3):629-636.
20. Zhu Z, Fu C, Li X, Song Y, Li C, Zou M, Guan Y, Zhu Y. Prostaglandin E2 Promotes Endothelial Differentiation from Bone Marrow-Derived Cells through AMPK Activation. PLoS One 2011, 6(8):e23554.
21. Li X, Han Y, Pang W, Li C, Xie X, Shyy JY, Zhu Y. AMP-activated protein kinase promotes the differentiation of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2008, 28(10):1789-1795.
22. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 2007, 67(9):4507-4513.
23. Murphy C, Newsholme P. Importance of glutamine metabolism in murine macrophages and human monocytes to L-arginine biosynthesis and rates of nitrite or urea production. Clin Sci (Lond) 1998, 95(4):397-407.
24. Costa Rosa LF, Curi R, Murphy C, Newsholme P. Effect of adrenaline and phorbol myristate acetate or bacterial lipopolysaccharide on stimulation of pathways of macrophage glucose, glutamine and O2 metabolism. Evidence for cyclic AMP-dependent protein kinase mediated inhibition of glucose-6-phosphate dehydrogenase and activation of NADP+-dependent 'malic' enzyme. Biochem J 1995, 310(Pt 2):709-714.
25. Fleetwood AJ, Cook AD, Hamilton JA. Functions of granulocyte-macrophage colony-stimulating factor. Crit Rev Immunol 2005, 25(5):405-428.
26. Ando M, Uehara I, Kogure K, Asano Y, Nakajima W, Abe Y, Kawauchi K, Tanaka N. Interleukin 6 enhances glycolysis through expression of the glycolytic enzymes hexokinase 2 and 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3. J Nippon Med Sch 2010, 77(2):97-105.
27. Dhar-Mascareno M, Chen J, Zhang RH, Carcamo JM, Golde DW. Granulocyte-macrophage colony-stimulating factor signals for increased glucose transport via phosphatidylinositol 3-kinase- and hydrogen peroxide-dependent mechanisms. J Biol Chem 2003, 278(13):11107-11114.
28. Ahmed N, Berridge MV. Ceramides that mediate apoptosis reduce glucose uptake and transporter affinity for glucose in human leukaemic cell lines but not in neutrophils. Pharmacol Toxicol 2000, 86(3):114-121.
29. Fernandes LC, Mattozo CA, Machado UF, Rosa LF, Curi R. Insulin treatment can abolish changes in glucose and glutamine metabolism of lymphocytes and macrophages caused by the implantation of the Walker 256 tumour. Cell Biochem Funct 1996, 14(3):187-192.
30. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis?. Nat Rev Cancer 2004, 4(11):891-899.
31. Koivunen P, Hirsila M, Remes AM, Hassinen IE, Kivirikko KI, Myllyharju J. Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem 2007, 282(7):4524-4532.
32. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, Cho HI, Celis E, Quiceno DG, Padhya T, et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 2010, 207(11):2439-2453.
33. Wada HG, Indelicato SR, Meyer L, Kitamura T, Miyajima A, Kirk G, Muir VC, Parce JW. GM-CSF triggers a rapid, glucose dependent extracellular acidification by TF-1 cells: evidence for sodium/proton antiporter and PKC mediated activation of acid production. J Cell Physiol 1993, 154(1):129-138.
34. Albina JE, Mastrofrancesco B. Modulation of glucose metabolism in macrophages by products of nitric oxide synthase. Am J Physiol 1993, 264(6 Pt 1):C1594-C1599.
35. Irace C, Esposito G, Maffettone C, Rossi A, Festa M, Iuvone T, Santamaria R, Sautebin L, Carnuccio R, Colonna A. Oxalomalate affects the inducible nitric oxide synthase expression and activity. Life Sci 2007, 80(14):1282-1291.
36. Hardie DG. AMP-activated protein kinase: a cellular energy sensor with a key role in metabolic disorders and in cancer. Biochem Soc Trans 2011, 39(1):1-13.
37. Kelly M, Gauthier MS, Saha AK, Ruderman NB. Activation of AMP-activated protein kinase by interleukin-6 in rat skeletal muscle: association with changes in cAMP, energy state, and endogenous fuel mobilization. Diabetes 2009, 58(9):1953-1960.
38. Wegrzyn J, Potla R, Chwae YJ, Sepuri NB, Zhang Q, Koeck T, Derecka M, Szczepanek K, Szelag M, Gornicka A, et al. Function of mitochondrial Stat3 in cellular respiration. Science 2009, 323(5915):793-797.
39. Wang W, Guan KL. AMP-activated protein kinase and cancer. Acta Physiol (Oxf) 2009, 196(1):55-63.
40. Jin J, Mullen TD, Hou Q, Bielawski J, Bielawska A, Zhang X, Obeid LM, Hannun YA, Hsu YT. AMPK inhibitor Compound C stimulates ceramide production and promotes Bax redistribution and apoptosis in MCF7 breast carcinoma cells. J Lipid Res 2009, 50(12):2389-2397.
41. Hammami I, Chen J, Bronte V, Decrescenzo G, Jolicoeur M. Immunosuppression mediated by myeloid-derived suppressor cells is energetically costly. Submitted Paper 2012, 12:253-268.
42. Jeong HW, Hsu KC, Lee JW, Ham M, Huh JY, Shin HJ, Kim WS, Kim JB. Berberine suppresses proinflammatory responses through AMPK activation in macrophages. Am J Physiol Endocrinol Metab 2009, 296(4):E955-E964.
43. Chang MY, Ho FM, Wang JS, Kang HC, Chang Y, Ye ZX, Lin WW. AICAR induces cyclooxygenase-2 expression through AMP-activated protein kinase-transforming growth factor-beta-activated kinase 1-p38 mitogen-activated protein kinase signaling pathway. Biochem Pharmacol 2010, 80(8):1210-1220.
44. Fujita M, Kohanbash G, Fellows-Mayle W, Hamilton RL, Komohara Y, Decker SA, Ohlfest JR, Okada H. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res 2011, 71(7):2664-2674.
45. Görgens JF, Van Zyl WH, Knoetze JH. Reliability of methods for the determination of specific substrate consumption rates in batch culture. Biochem Eng J 2005, 25(2):109-112.
46. Munder M, Eichmann K, Moran JM, Centeno F, Soler G, Modolell M. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J Immunol 1999, 163(7):3771-3777.
47. Lamboursain L, St-Onge F, Jolicoeur M. A lab-respirometer forplant and animal cell culture. Biotechnol Progr 2002, 18:1377-1386.
48. Kimball E, Rabinowitz JD. Identifying decomposition products in extracts of cellular metabolites. Anal Biochem 2006, 358(2):273-280.