Intracellular NAD(H) levels control motility and invasion of glioma cells

Cellular and Molecular Life Sciences

Volumn 70, Issue 12, 2013, Pages 2175-2190

  Van Horssen, Remco ^a   Willemse, Marieke ^a   Haeger, Anna ^a   Attanasio, Francesca ^b   Güneri, Tuba ^a   Schwab, Albrecht ^c   Stock, Christian M ^c   Buccione, Roberto ^b   Fransen, Jack A M ^a   Wieringa, Bé ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Santa Maria Imbaro   (Italy)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Cancer metabolism; Invasion; Lactic acid; Migration; NAD(H)

Indexed keywords

DAPORINAD; GLUCOSE; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE ISOENZYME 5; LACTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL INVASION; CELL MOTILITY; CELL PH; CELL PROLIFERATION; CONTROLLED STUDY; GLIOMA CELL;

BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL MOVEMENT; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; HYDROGEN-ION CONCENTRATION; L-LACTATE DEHYDROGENASE; LACTIC ACID; NAD; NEOPLASM INVASIVENESS; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; TIME-LAPSE IMAGING; TUMOR CELLS, CULTURED;

EID: 84878548018     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1249-1     Document Type: Article

References (53)

1. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646-674. doi: 10.1016/j.cell.2011.02.013
2. Friedl P, Alexander S (2011) Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147(5):992-1009
3. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324(5930):1029-1033
4. Warburg O (1956) On the origin of cancer cells. Science 123(3191):309-314
5. Deberardinis RJ, Sayed N, Ditsworth D, Thompson CB (2008) Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev 18(1):54-61. doi: 10.1016/j.gde.2008.02.003
6. + metabolism. Biochem J 439(2):341-348
7. +-dependent signalling. FEBS Lett 585(11):1651-1656. doi: 10.1016/j.febslet.2011.03.045
8. de Groof AJ, Te Lindert MM, van Dommelen MM, Wu M, Willemse M, Smift AL, Winer M, Oerlemans F, Pluk H, Fransen JA, Wieringa B (2009) Increased OXPHOS activity precedes rise in glycolytic rate in H-RasV12/E1A transformed fibroblasts that develop a Warburg phenotype. Mol Cancer 8(1):54
9. Garten A, Petzold S, Korner A, Imai S, Kiess W (2009) Nampt: linking NAD biology, metabolism and cancer. Trends Endocrinol Metab 20(3):130-138
10. Nikiforov A, Dolle C, Niere M, Ziegler M (2011) Pathways and subcellular compartmentation of NAD biosynthesis in human cells: from entry of extracellular precursors to mitochondrial NAD generation. J Biol Chem 286(24):21767-21778. doi: 10.1074/jbc.M110.213298
11. Houtkooper RH, Pirinen E, Auwerx J (2012) Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13(4):225-238. doi: 10.1038/nrm3293
12. Bowlby SC, Thomas MJ, D'Agostino RB Jr, Kridel SJ (2012) Nicotinamide phosphoribosyl transferase (Nampt) is required for de novo lipogenesis in tumor cells. PLoS ONE 7(6):e40195. doi: 10.1371/journal.pone.0040195
13. Holen K, Saltz LB, Hollywood E, Burk K, Hanauske AR (2008) The pharmacokinetics, toxicities, and biologic effects of FK866, a nicotinamide adenine dinucleotide biosynthesis inhibitor. Investig New Drugs 26(1):45-51
14. Cerna D, Li H, Flaherty S, Takebe N, Coleman CN, Yoo SS (2012) Inhibition of nicotinamide phosphoribosyltransferase (NAMPT) activity by small molecule GMX1778 regulates reactive oxygen species (ROS)-mediated cytotoxicity in a p53- and nicotinic acid phosphoribosyltransferase1 (NAPRT1)-dependent manner. J Biol Chem 287(26):22408-22417. doi: 10.1074/jbc.M112.357301
15. Zhao Y, Jin J, Hu Q, Zhou HM, Yi J, Yu Z, Xu L, Wang X, Yang Y, Loscalzo J (2011) Genetically encoded fluorescent sensors for intracellular NADH detection. Cell Metab 14(4):555-566. doi: 10.1016/j.cmet.2011.09.004
16. Van Horssen R, Galjart N, Rens JA, Eggermont AM, ten Hagen TL (2006) Differential effects of matrix and growth factors on endothelial and fibroblast motility: application of a modified cell migration assay. J Cell Biochem 99(6):1536-1552
17. Murphy DA, Courtneidge SA (2011) The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 12(7):413-426. doi: 10.1038/nrm3141
18. Fantin VR, St-Pierre J, Leder P (2006) Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 9(6):425-434. doi: 10.1016/j.ccr.2006.04.023
19. Le A, Cooper CR, Gouw AM, Dinavahi R, Maitra A, Deck LM, Royer RE, Vander Jagt DL, Semenza GL, Dang CV (2010) Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proc Natl Acad Sci USA 107(5):2037-2042. doi: 10.1073/pnas.0914433107
20. Tennant DA, Duran RV, Gottlieb E (2010) Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 10(4):267-277
21. Gianni D, Diaz B, Taulet N, Fowler B, Courtneidge SA, Bokoch GM (2009) Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci Signal 2(88):ra54. doi: 10.1126/scisignal.2000370
22. Hung RJ, Pak CW, Terman JR (2011) Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334(6063):1710-1713. doi: 10.1126/science.1211956
23. Zhang Q, Wang SY, Nottke AC, Rocheleau JV, Piston DW, Goodman RH (2006) Redox sensor CtBP mediates hypoxia-induced tumor cell migration. Proc Natl Acad Sci USA 103(24):9029-9033. doi: 10.1073/pnas.0603269103
24. Terashima M, Shimoyama M, Tsuchiya M (1999) Introduction of NAD decreases fMLP-induced actin polymerization in chicken polymorphonuclear leukocytes - the role of intracellular ADP-ribosylation of actin for cytoskeletal organization. Biochem Mol Biol Int 47(4):615-620
25. +-dependent tubulin deacetylase. Mol Cell 11(2):437-444
26. Zhang Y, Zhang M, Dong H, Yong S, Li X, Olashaw N, Kruk PA, Cheng JQ, Bai W, Chen J, Nicosia SV, Zhang X (2009) Deacetylation of cortactin by SIRT1 promotes cell migration. Oncogene 28(3):445-460
27. + in muscle morphogenesis. Dev Biol 344(2):809-826. doi: 10.1016/j.ydbio.2010.05.513
28. Quistorff B, Grunnet N (2011) The isoenzyme pattern of LDH does not play a physiological role; except perhaps during fast transitions in energy metabolism. Aging (Albany NY) 3(5):457-460
29. Attanasio F, Caldieri G, Giacchetti G, van Horssen R, Wieringa B, Buccione R (2011) Novel invadopodia components revealed by differential proteomic analysis. Eur J Cell Biol 90(2-3):115-127. doi: 10.1016/j.ejcb.2010. 05.004
30. Hirschhaeuser F, Sattler UG, Mueller-Klieser W (2011) Lactate: a metabolic key player in cancer. Cancer Res 71(22):6921-6925
31. Goetze K, Walenta S, Ksiazkiewicz M, Kunz-Schughart LA, Mueller-Klieser W (2011) Lactate enhances motility of tumor cells and inhibits monocyte migration and cytokine release. Int J Oncol 39(2):453-463. doi: 10.3892/ijo.2011.1055
32. Colen CB, Shen Y, Ghoddoussi F, Yu P, Francis TB, Koch BJ, Monterey MD, Galloway MP, Sloan AE, Mathupala SP (2011) Metabolic targeting of lactate efflux by malignant glioma inhibits invasiveness and induces necrosis: an in vivo study. Neoplasia 13(7):620-632
33. Bonuccelli G, Tsirigos A, Whitaker-Menezes D, Pavlides S, Pestell RG, Chiavarina B, Frank PG, Flomenberg N, Howell A, Martinez-Outschoorn UE, Sotgia F, Lisanti MP (2010) Ketones and lactate "fuel" tumor growth and metastasis: evidence that epithelial cancer cells use oxidative mitochondrial metabolism. Cell Cycle 9(17):3506-3514
34. Stock C, Schwab A (2009) Protons make tumor cells move like clockwork. Pflugers Arch 458(5):981-992. doi: 10.1007/s00424-009-0677-8
35. Frantz C, Barreiro G, Dominguez L, Chen X, Eddy R, Condeelis J, Kelly MJ, Jacobson MP, Barber DL (2008) Cofilin is a pH sensor for actin free barbed end formation: role of phosphoinositide binding. J Cell Biol 183(5):865-879. doi: 10.1083/jcb.200804161
36. Magalhaes MA, Larson DR, Mader CC, Bravo-Cordero JJ, Gil-Henn H, Oser M, Chen X, Koleske AJ, Condeelis J (2011) Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J Cell Biol 195(5):903-920. doi: 10.1083/jcb.201103045
37. Busco G, Cardone RA, Greco MR, Bellizzi A, Colella M, Antelmi E, Mancini MT, Dell'Aquila ME, Casavola V, Paradiso A, Reshkin SJ (2010) NHE1 promotes invadopodial ECM proteolysis through acidification of the peri-invadopodial space. Faseb J 24(10):3903-3915. doi: 10.1096/fj.09-149518
38. Olson MF, Sahai E (2009) The actin cytoskeleton in cancer cell motility. Clin Exp Metastasis 26(4):273-287
39. Van Horssen R, Janssen E, Peters W, van de Pasch L, Te Lindert MM, van Dommelen MM, Linssen PC, ten Hagen TL, Fransen JA, Wieringa B (2009) Modulation of cell motility by spatial repositioning of enzymatic ATP/ADP exchange capacity. J Biol Chem 284(3):1620-1627
40. Hung YP, Albeck JG, Tantama M, Yellen G (2011) Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor. Cell Metab 14(4):545-554. doi: 10.1016/j.cmet.2011.08.012
41. Koivusalo M, Welch C, Hayashi H, Scott CC, Kim M, Alexander T, Touret N, Hahn KM, Grinstein S (2010) Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol 188(4):547-563. doi: 10.1083/jcb.200908086
42. Chiarugi A, Dolle C, Felici R, Ziegler M (2012) The NAD metabolome - a key determinant of cancer cell biology. Nat Rev Cancer 12(11):741-752. doi: 10.1038/nrc3340
43. + biosynthesis. J Cell Sci. doi: 10.1242/jcs.110262
44. Zhou M, Zhao Y, Ding Y, Liu H, Liu Z, Fodstad O, Riker AI, Kamarajugadda S, Lu J, Owen LB, Ledoux SP, Tan M (2010) Warburg effect in chemosensitivity: targeting lactate dehydrogenase-A re-sensitizes taxol-resistant cancer cells to taxol. Mol Cancer 9:33. doi: 10.1186/1476-4598-9-33
45. + biosynthesis and base excision repair. Cancer Res 71(6):2308-2317. doi: 10.1158/0008-5472.can-10-3213
46. Ho VW, Leung K, Hsu A, Luk B, Lai J, Shen SY, Minchinton AI, Waterhouse D, Bally MB, Lin W, Nelson BH, Sly LM, Krystal G (2011) A low carbohydrate, high protein diet slows tumor growth and prevents cancer initiation. Cancer Res 71(13):4484-4493. doi: 10.1158/0008-5472.can-10-3973
47. Menssen A, Hydbring P, Kapelle K, Vervoorts J, Diebold J, Luscher B, Larsson LG, Hermeking H (2012) The c-MYC oncoprotein, the NAMPT enzyme, the SIRT1-inhibitor DBC1, and the SIRT1 deacetylase form a positive feedback loop. Proc Natl Acad Sci USA 109(4):E187-E196. doi: 10.1073/pnas.1105304109
48. Wang B, Hasan MK, Alvarado E, Yuan H, Wu H, Chen WY (2011) NAMPT overexpression in prostate cancer and its contribution to tumor cell survival and stress response. Oncogene 30(8):907-921. doi: 10.1038/onc.2010.468
49. Wosikowski K, Mattern K, Schemainda I, Hasmann M, Rattel B, Loser R (2002) WK175, a novel antitumor agent, decreases the intracellular nicotinamide adenine dinucleotide concentration and induces the apoptotic cascade in human leukemia cells. Cancer Res 62(4):1057-1062
50. Dordick RS, Brierley GP, Garlid KD (1980) On the mechanism of A23187-induced potassium efflux in rat liver mitochondria. J Biol Chem 255(21):10299-10305
51. Krahling H, Mally S, Eble JA, Noel J, Schwab A, Stock C (2009) The glycocalyx maintains a cell surface pH nanoenvironment crucial for integrin-mediated migration of human melanoma cells. Pflugers Arch 458(6):1069-1083. doi: 10.1007/s00424-009-0694-7
52. Stock C, Mueller M, Kraehling H, Mally S, Noel J, Eder C, Schwab A (2007) pH nanoenvironment at the surface of single melanoma cells. Cell Physiol Biochem 20(5):679-686
53. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR (1990) New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 82(13):1107 -1112