Paraoxonase 2 Facilitates Pancreatic Cancer Growth and Metastasis by Stimulating GLUT1-Mediated Glucose Transport

Molecular Cell

Volumn 67, Issue 4, 2017, Pages 685-701.e6

  Nagarajan, Arvindhan ^a   Dogra, Shaillay Kumar ^b   Sun, Lisha ^a   Gandotra, Neeru ^a   Ho, Thuy ^a   Cai, Guoping ^a   Cline, Gary ^a   Kumar, Priti ^a   Cowles, Robert A ^a   Wajapeyee, Narendra ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AGENCY FOR SCIENCE   (Singapore)

Author keywords

anoikis; glucose; GLUT1; metabolism; pancreatic cancer; PON2

Indexed keywords

ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; ARYLDIALKYLPHOSPHATASE; BBC3 PROTEIN, HUMAN; FOXO3 PROTEIN, HUMAN; GLUCOSE; GLUCOSE TRANSPORTER 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; KRAS PROTEIN, HUMAN; ONCOPROTEIN; PON2 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; PROTEIN P21; PROTEIN P53; SLC2A1 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL; CARCINOMA, PANCREATIC DUCTAL; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; ENERGY METABOLISM; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HUMAN; LIVER NEOPLASMS; LUNG NEOPLASMS; MALE; METABOLISM; MUTATION; NUDE MOUSE; PANCREATIC NEOPLASMS; PATHOLOGY; RNA INTERFERENCE; SECONDARY; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR CELL LINE; TUMOR VOLUME;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; ARYLDIALKYLPHOSPHATASE; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ENERGY METABOLISM; FEMALE; FORKHEAD BOX PROTEIN O3; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; LIVER NEOPLASMS; LUNG NEOPLASMS; MALE; MICE, NUDE; MUTATION; PANCREATIC NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS P21(RAS); RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TUMOR BURDEN; TUMOR SUPPRESSOR PROTEIN P53; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85027570435     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2017.07.014     Document Type: Article

References (60)

1. Adekola, K., Rosen, S.T., Shanmugam, M., Glucose transporters in cancer metabolism. Curr. Opin. Oncol. 24 (2012), 650–654.
2. Altenhöfer, S., Witte, I., Teiber, J.F., Wilgenbus, P., Pautz, A., Li, H., Daiber, A., Witan, H., Clement, A.M., Förstermann, U., Horke, S., One enzyme, two functions: PON2 prevents mitochondrial superoxide formation and apoptosis independent from its lactonase activity. J. Biol. Chem. 285 (2010), 24398–24403.
3. Badea, L., Herlea, V., Dima, S.O., Dumitrascu, T., Popescu, I., Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology 55 (2008), 2016–2027.
4. Bardeesy, N., DePinho, R.A., Pancreatic cancer biology and genetics. Nat. Rev. Cancer 2 (2002), 897–909.
5. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A.A., Kim, S., Wilson, C.J., Lehár, J., Kryukov, G.V., Sonkin, D., et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483 (2012), 603–607.
6. Bensaad, K., Tsuruta, A., Selak, M.A., Vidal, M.N., Nakano, K., Bartrons, R., Gottlieb, E., Vousden, K.H., TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126 (2006), 107–120.
7. Birsoy, K., Possemato, R., Lorbeer, F.K., Bayraktar, E.C., Thiru, P., Yucel, B., Wang, T., Chen, W.W., Clish, C.B., Sabatini, D.M., Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides. Nature 508 (2014), 108–112.
8. Boado, R.J., Black, K.L., Pardridge, W.M., Gene expression of GLUT3 and GLUT1 glucose transporters in human brain tumors. Brain Res. Mol. Brain Res. 27 (1994), 51–57.
9. Bryant, K.L., Mancias, J.D., Kimmelman, A.C., Der, C.J., KRAS: feeding pancreatic cancer proliferation. Trends Biochem. Sci. 39 (2014), 91–100.
10. Campbell, P.M., Groehler, A.L., Lee, K.M., Ouellette, M.M., Khazak, V., Der, C.J., K-Ras promotes growth transformation and invasion of immortalized human pancreatic cells by Raf and phosphatidylinositol 3-kinase signaling. Cancer Res. 67 (2007), 2098–2106.
11. Cantor, J.R., Sabatini, D.M., Cancer cell metabolism: one hallmark, many faces. Cancer Discov. 2 (2012), 881–898.
12. Chelur, D.S., Ernstrom, G.G., Goodman, M.B., Yao, C.A., Chen, L., O’ Hagan, R., Chalfie, M., The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel. Nature 420 (2002), 669–673.
13. Chen, J., Zhao, S., Nakada, K., Kuge, Y., Tamaki, N., Okada, F., Wang, J., Shindo, M., Higashino, F., Takeda, K., et al. Dominant-negative hypoxia-inducible factor-1 alpha reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism. Am. J. Pathol. 162 (2003), 1283–1291.
14. Collins, M.A., Bednar, F., Zhang, Y., Brisset, J.C., Galbán, S., Galbán, C.J., Rakshit, S., Flannagan, K.S., Adsay, N.V., Pasca di Magliano, M., Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J. Clin. Invest. 122 (2012), 639–653.
15. Corton, J.M., Gillespie, J.G., Hawley, S.A., Hardie, D.G., 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells?. Eur. J. Biochem. 229 (1995), 558–565.
16. Ding, S., Wu, X., Li, G., Han, M., Zhuang, Y., Xu, T., Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122 (2005), 473–483.
17. Egan, D.F., Shackelford, D.B., Mihaylova, M.M., Gelino, S., Kohnz, R.A., Mair, W., Vasquez, D.S., Joshi, A., Gwinn, D.M., Taylor, R., et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331 (2011), 456–461.
18. Faubert, B., Boily, G., Izreig, S., Griss, T., Samborska, B., Dong, Z., Dupuy, F., Chambers, C., Fuerth, B.J., Viollet, B., et al. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell Metab. 17 (2013), 113–124.
19. Forloni, M., Dogra, S.K., Dong, Y., Conte, D. Jr., Ou, J., Zhu, L.J., Deng, A., Mahalingam, M., Green, M.R., Wajapeyee, N., miR-146a promotes the initiation and progression of melanoma by activating Notch signaling. eLife, 3, 2014, e01460.
20. Ginsberg, D., Mechta, F., Yaniv, M., Oren, M., Wild-type p53 can down-modulate the activity of various promoters. Proc. Natl. Acad. Sci. USA 88 (1991), 9979–9983.
21. Greer, E.L., Oskoui, P.R., Banko, M.R., Maniar, J.M., Gygi, M.P., Gygi, S.P., Brunet, A., The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem. 282 (2007), 30107–30119.
22. Grützmann, R., Pilarsky, C., Ammerpohl, O., Lüttges, J., Böhme, A., Sipos, B., Foerder, M., Alldinger, I., Jahnke, B., Schackert, H.K., et al. Gene expression profiling of microdissected pancreatic ductal carcinomas using high-density DNA microarrays. Neoplasia 6 (2004), 611–622.
23. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
24. Hardie, D.G., Ross, F.A., Hawley, S.A., AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13 (2012), 251–262.
25. Havugimana, P.C., Hart, G.T., Nepusz, T., Yang, H., Turinsky, A.L., Li, Z., Wang, P.I., Boutz, D.R., Fong, V., Phanse, S., et al. A census of human soluble protein complexes. Cell 150 (2012), 1068–1081.
26. He, T.L., Zhang, Y.J., Jiang, H., Li, X.H., Zhu, H., Zheng, K.L., The c-Myc-LDHA axis positively regulates aerobic glycolysis and promotes tumor progression in pancreatic cancer. Med. Oncol., 32, 2015, 187.
27. Hidalgo, M., Pancreatic cancer. N. Engl. J. Med. 362 (2010), 1605–1617.
28. Hishinuma, S., Ogata, Y., Tomikawa, M., Ozawa, I., Hirabayashi, K., Igarashi, S., Patterns of recurrence after curative resection of pancreatic cancer, based on autopsy findings. J. Gastrointest. Surg. 10 (2006), 511–518.
29. Horke, S., Xiao, J., Schütz, E.M., Kramer, G.L., Wilgenbus, P., Witte, I., Selbach, M., Teiber, J.F., Novel Paraoxonase 2-dependent mechanism mediating the biological effects of the Pseudomonas aeruginosa quorum-sensing molecule N-(3-Oxo-Dodecanoyl)-L-homoserine lactone. Infect. Immun. 83 (2015), 3369–3380.
30. Ishikawa, M., Yoshida, K., Yamashita, Y., Ota, J., Takada, S., Kisanuki, H., Koinuma, K., Choi, Y.L., Kaneda, R., Iwao, T., et al. Experimental trial for diagnosis of pancreatic ductal carcinoma based on gene expression profiles of pancreatic ductal cells. Cancer Sci. 96 (2005), 387–393.
31. Jones, R.G., Plas, D.R., Kubek, S., Buzzai, M., Mu, J., Xu, Y., Birnbaum, M.J., Thompson, C.B., AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 18 (2005), 283–293.
32. Jones, S., Zhang, X., Parsons, D.W., Lin, J.C., Leary, R.J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A., et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321 (2008), 1801–1806.
33. Kondoh, H., Lleonart, M.E., Gil, J., Wang, J., Degan, P., Peters, G., Martinez, D., Carnero, A., Beach, D., Glycolytic enzymes can modulate cellular life span. Cancer Res. 65 (2005), 177–185.
34. Lapatsina, L., Brand, J., Poole, K., Daumke, O., Lewin, G.R., Stomatin-domain proteins. Eur. J. Cell Biol. 91 (2012), 240–245.
35. Matoba, S., Kang, J.G., Patino, W.D., Wragg, A., Boehm, M., Gavrilova, O., Hurley, P.J., Bunz, F., Hwang, P.M., p53 regulates mitochondrial respiration. Science 312 (2006), 1650–1653.
36. Mitsuishi, Y., Taguchi, K., Kawatani, Y., Shibata, T., Nukiwa, T., Aburatani, H., Yamamoto, M., Motohashi, H., Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 22 (2012), 66–79.
37. Mohammad, G.H., Olde Damink, S.W., Malago, M., Dhar, D.K., Pereira, S.P., Pyruvate kinase M2 and lactate dehydrogenase A are overexpressed in pancreatic cancer and correlate with poor outcome. PLoS ONE, 11, 2016, e0151635.
38. Montel-Hagen, A., Kinet, S., Manel, N., Mongellaz, C., Prohaska, R., Battini, J.L., Delaunay, J., Sitbon, M., Taylor, N., Erythrocyte Glut1 triggers dehydroascorbic acid uptake in mammals unable to synthesize vitamin C. Cell 132 (2008), 1039–1048.
39. Morton, J.P., Timpson, P., Karim, S.A., Ridgway, R.A., Athineos, D., Doyle, B., Jamieson, N.B., Oien, K.A., Lowy, A.M., Brunton, V.G., et al. Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc. Natl. Acad. Sci. USA 107 (2010), 246–251.
40. Nakano, K., Vousden, K.H., PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 7 (2001), 683–694.
41. Ogawa, H., Nagano, H., Konno, M., Eguchi, H., Koseki, J., Kawamoto, K., Nishida, N., Colvin, H., Tomokuni, A., Tomimaru, Y., et al. The combination of the expression of hexokinase 2 and pyruvate kinase M2 is a prognostic marker in patients with pancreatic cancer. Mol. Clin. Oncol. 3 (2015), 563–571.
42. Paoli, P., Giannoni, E., Chiarugi, P., Anoikis molecular pathways and its role in cancer progression. Biochim. Biophys. Acta 1833 (2013), 3481–3498.
43. Pei, H., Li, L., Fridley, B.L., Jenkins, G.D., Kalari, K.R., Lingle, W., Petersen, G., Lou, Z., Wang, L., FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 16 (2009), 259–266.
44. Possemato, R., Marks, K.M., Shaul, Y.D., Pacold, M.E., Kim, D., Birsoy, K., Sethumadhavan, S., Woo, H.K., Jang, H.G., Jha, A.K., et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 476 (2011), 346–350.
45. Santra, M.K., Wajapeyee, N., Green, M.R., F-box protein FBXO31 mediates cyclin D1 degradation to induce G1 arrest after DNA damage. Nature 459 (2009), 722–725.
46. Scarpa, A., Capelli, P., Mukai, K., Zamboni, G., Oda, T., Iacono, C., Hirohashi, S., Pancreatic adenocarcinomas frequently show p53 gene mutations. Am. J. Pathol. 142 (1993), 1534–1543.
47. Schwartzenberg-Bar-Yoseph, F., Armoni, M., Karnieli, E., The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression. Cancer Res. 64 (2004), 2627–2633.
48. Shats, I., Milyavsky, M., Tang, X., Stambolsky, P., Erez, N., Brosh, R., Kogan, I., Braunstein, I., Tzukerman, M., Ginsberg, D., Rotter, V., p53-dependent down-regulation of telomerase is mediated by p21waf1. J. Biol. Chem. 279 (2004), 50976–50985.
49. Son, J., Lyssiotis, C.A., Ying, H., Wang, X., Hua, S., Ligorio, M., Perera, R.M., Ferrone, C.R., Mullarky, E., Shyh-Chang, N., et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature 496 (2013), 101–105.
50. Takanaga, H., Chaudhuri, B., Frommer, W.B., GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim. Biophys. Acta 1778 (2008), 1091–1099.
51. Teo, M., Crotty, G.F., O'Súilleabháin, C., Ridgway, P.F., Conlon, K.C., Power, D.G., McDermott, R.S., Identification of distinct phenotypes of locally advanced pancreatic adenocarcinoma. J. Gastrointest. Cancer 44 (2013), 73–78.
52. Wajapeyee, N., Serra, R.W., Zhu, X., Mahalingam, M., Green, M.R., Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132 (2008), 363–374.
53. Weissmueller, S., Manchado, E., Saborowski, M., Morris, J.P. 4th, Wagenblast, E., Davis, C.A., Moon, S.H., Pfister, N.T., Tschaharganeh, D.F., Kitzing, T., et al. Mutant p53 drives pancreatic cancer metastasis through cell-autonomous PDGF receptor β signaling. Cell 157 (2014), 382–394.
54. Witte, I., Altenhöfer, S., Wilgenbus, P., Amort, J., Clement, A.M., Pautz, A., Li, H., Förstermann, U., Horke, S., Beyond reduction of atherosclerosis: PON2 provides apoptosis resistance and stabilizes tumor cells. Cell Death Dis., 2, 2011, e112.
55. Yamamoto, T., Seino, Y., Fukumoto, H., Koh, G., Yano, H., Inagaki, N., Yamada, Y., Inoue, K., Manabe, T., Imura, H., Over-expression of facilitative glucose transporter genes in human cancer. Biochem. Biophys. Res. Commun. 170 (1990), 223–230.
56. Ying, H., Kimmelman, A.C., Lyssiotis, C.A., Hua, S., Chu, G.C., Fletcher-Sananikone, E., Locasale, J.W., Son, J., Zhang, H., Coloff, J.L., et al. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell 149 (2012), 656–670.
57. You, H., Pellegrini, M., Tsuchihara, K., Yamamoto, K., Hacker, G., Erlacher, M., Villunger, A., Mak, T.W., FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J. Exp. Med. 203 (2006), 1657–1663.
58. Yu, M., Zhou, Q., Zhou, Y., Fu, Z., Tan, L., Ye, X., Zeng, B., Gao, W., Zhou, J., Liu, Y., et al. Metabolic phenotypes in pancreatic cancer. PLoS ONE, 10, 2015, e0115153.
59. Zhang, J.Z., Abbud, W., Prohaska, R., Ismail-Beigi, F., Overexpression of stomatin depresses GLUT-1 glucose transporter activity. Am. J. Physiol. Cell Physiol. 280 (2001), C1277–C1283.
60. Zhang, Y., Xing, Y., Zhang, L., Mei, Y., Yamamoto, K., Mak, T.W., You, H., Regulation of cell cycle progression by forkhead transcription factor FOXO3 through its binding partner DNA replication factor Cdt1. Proc. Natl. Acad. Sci. USA 109 (2012), 5717–5722.