Regulation of the pentose phosphate pathway by an androgen receptor-mTOR-mediated mechanism and its role in prostate cancer cell growth

Oncogenesis

Volumn 3, Issue 5, 2014, Pages

  Tsouko, E ^a   Khan, A S ^a   White, M A ^a   Han, J J ^a   Shi, Y ^a   Merchant, F A ^b   Sharpe, M A ^c   Xin, L ^d,e   Frigo, D E ^a,c  

^a University of Houston   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e Dan L Duncan Cancer Center   (United States)

Author keywords

androgen receptor; G6PD; mTOR; pentose phosphate pathway; prostate cancer; PTEN

Indexed keywords

6 AMINONICOTINAMIDE; ANDROGEN RECEPTOR; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RAPAMYCIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RIBOSE; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CARBOHYDRATE SYNTHESIS; CASTRATION RESISTANT PROSTATE CANCER; CELL GROWTH; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; GLEASON SCORE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LNCAP CELL LINE; MALE; MOUSE; NONHUMAN; NUCLEIC ACID SYNTHESIS; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA ISOLATION; UPREGULATION; WESTERN BLOTTING;

MAMMALIA;

EID: 84906894979     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2014.18     Document Type: Article

References (70)

1. Attar RM, Takimoto CH, Gottardis MM. Castration-resistant prostate cancer: locking up the molecular escape routes. Clin Cancer Res 2009; 15: 3251-3255.
2. Warburg O. On the origin of cancer cells. Science 1956; 123: 309-314.
3. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012; 21: 297-308.
4. Wittig R, Coy JF. The role of glucose metabolism and glucose-Associated signalling in cancer. Perspect Medicin Chem 2008; 1: 64-82.
5. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell 2008; 134: 703-707.
6. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer 2011; 11: 325-337.
7. Ros S, Santos CR, Moco S, Baenke F, Kelly G, Howell M et al. Functional metabolic screen identifies 6-phosphofructo-2-kinase/fructose-2,6-biphosphatase 4 as an important regulator of prostate cancer cell survival. Cancer Discov 2012; 2: 328-343.
8. Yi W, Clark PM, Mason DE, Keenan MC, Hill C, Goddard 3rd WA et al. Phosphofructokinase glycosylation regulates cell growth and metabolism. Science 2012; 337: 975-980.
9. Zhou CF, Li XB, Sun H, Zhang B, Han YS, Jiang Y et al. Pyruvate kinase type M2 is upregulated in colorectal cancer and promotes proliferation and migration of colon cancer cells. IUBMB Life 2012; 64: 775-782.
10. Roigas J, Deger S, Schroeder J, Wille A, Turk I, Brux B et al. Tumor type M2 pyruvate kinase expression in metastatic renal cell carcinoma. Urol Res 2003; 31: 358-362.
11. Schneider J, Neu K, Grimm H, Velcovsky HG, Weisse G, Eigenbrodt E. Tumor M2-pyruvate kinase in lung cancer patients: immunohistochemical detection and disease monitoring. Anticancer Res 2002; 22: 311-318.
12. Wong N, Ojo D, Yan J, Tang D. PKM2 contributes to cancer metabolism. Cancer Lett. (e-pub ahead of print 4 February 2014; doi:10.1016/j.canlet.2014.01.031).
13. Anastasiou D, Poulogiannis G, Asara JM, Boxer MB, Jiang JK, Shen M et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011; 334: 1278-1283.
14. Gruning NM, Rinnerthaler M, Bluemlein K, Mulleder M, Wamelink MM, Lehrach H et al. Pyruvate kinase triggers a metabolic feedback loop that controls redox metabolism in respiring cells. Cell Metab 2011; 14: 415-427.
15. Mazurek S, Zwerschke W, Jansen-Durr P, Eigenbrodt E. Metabolic cooperation between different oncogenes during cell transformation: interaction between activated ras and HPV-16 E7. Oncogene 2001; 20: 6891-6898.
16. Chaneton B, Gottlieb E. Rocking cell metabolism: revised functions of the key glycolytic regulator PKM2 in cancer. Trends Biochem Sci 2012; 37: 309-316.
17. Eggleston LV, Krebs HA. Regulation of the pentose phosphate cycle. Biochem J 1974; 138: 425-435.
18. Kruger NJ, von Schaewen A. The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 2003; 6: 236-246.
19. Riganti C, Gazzano E, Polimeni M, Aldieri E, Ghigo D. The pentose phosphate pathway: an antioxidant defense and a crossroad in tumor cell fate. Free Radic Biol Med 2012; 53: 421-436.
20. Boros LG, Brandes JL, Yusuf FI, Cascante M, Williams RD, Schirmer WJ. Inhibition of the oxidative and nonoxidative pentose phosphate pathways by somatostatin: a possible mechanism of antitumor action. Med Hypotheses 1998; 50: 501-506.
21. Frederiks WM, Bosch KS, Hoeben KA, van Marle J, Langbein S. Renal cell carcinoma and oxidative stress: the lack of peroxisomes. Acta Histochem 2010; 112: 364-371.
22. Du W, Jiang P, Mancuso A, Stonestrom A, Brewer MD, Minn AJ et al. TAp73 enhances the pentose phosphate pathway and supports cell proliferation. Nat Cell Biol 2013; 15: 991-1000.
23. Wang J, Yuan W, Chen Z, Wu S, Chen J, Ge J et al. Overexpression of G6PD is associated with poor clinical outcome in gastric cancer. Tumour Biol 2012; 33: 95-101.
24. Jiang P, Du W, Wang X, Mancuso A, Gao X, Wu M et al. p53 regulates biosynthesis through direct inactivation of glucose-6-phosphate dehydrogenase. Nat Cell Biol 2011; 13: 310-316.
25. Zampella EJ, Bradley Jr. EL, Pretlow 2nd TG. Glucose-6-phosphate dehydrogenase: a possible clinical indicator for prostatic carcinoma. Cancer 1982; 49: 384-387.
26. Pretlow 2nd TG, Harris BE, Bradley Jr. EL, Bueschen AJ, Lloyd KL, Pretlow TP. Enzyme activities in prostatic carcinoma related to Gleason grades. Cancer Res 1985; 45: 442-446.
27. Kaushik AK, Vareed SK, Basu S, Putluri V, Putluri N, Panzitt K et al. Metabolomic profiling identifies biochemical pathways associated with castration-resistant prostate cancer. J Proteome Res 2013; 13: 1088-1100.
28. Nna E, Tothill IE, Ludeman L, Bailey T. Endogenous control genes in prostate cells: evaluation of gene expression using 'real-time' quantitative polymerase chain reaction. Med Princ Pract 2010; 19: 433-439.
29. Stanton RC. Glucose-6-phosphate dehydrogenase, NADPH, and cell survival. IUBMB Life 2012; 64: 362-369.
30. Li D, Zhu Y, Tang Q, Lu H, Li H, Yang Y et al. A new G6PD knockdown tumor-cell line with reduced proliferation and increased susceptibility to oxidative stress. Cancer Biother Radiopharm 2009; 24: 81-90.
31. Pandolfi PP, Sonati F, Rivi R, Mason P, Grosveld F, Luzzatto L. Targeted disruption of the housekeeping gene encoding glucose 6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. EMBO J 1995; 14: 5209-5215.
32. Kuo W, Lin J, Tang TK. Human glucose-6-phosphate dehydrogenase (G6PD) gene transforms NIH 3T3 cells and induces tumors in nude mice. Int J Cancer 2000; 85: 857-864.
33. Koutcher JA, Alfieri AA, Matei C, Meyer KL, Street JC, Martin DS. Effect of 6-Aminonicotinamide on the pentose phosphate pathway: 31P NMR and tumor growth delay studies. Magn Reson Med 1996; 36: 887-892.
34. Shi Y, Han JJ, Tennakoon JB, Mehta FF, Merchant FA, Burns AR et al. Androgens promote prostate cancer cell growth through induction of autophagy. Mol Endocrinol 2013; 27: 280-295.
35. Lin H, Lu JP, Laflamme P, Qiao S, Shayegan B, Bryskin I et al. Inter-related in vitro effects of androgens, fatty acids and oxidative stress in prostate cancer: a mechanistic model supporting prevention strategies. Int J Oncol 2010; 37: 761-766.
36. Huang WC, Li X, Liu J, Lin J, Chung LW. Activation of androgen receptor, lipogenesis, and oxidative stress converged by SREBP-1 is responsible for regulating growth and progression of prostate cancer cells. Mol Cancer Res 2012; 10: 133-142.
37. Veeramani S, Chou YW, Lin FC, Muniyan S, Lin FF, Kumar S et al. Reactive oxygen species induced by p66Shc longevity protein mediate nongenomic androgen action via tyrosine phosphorylation signaling to enhance tumorigenicity of prostate cancer cells. Free Radic Biol Med 2012; 53: 95-108.
38. Tennakoon JB, Shi Y, Han JJ, Tsouko E, White MA, Burns AR et al. Androgens regulate prostate cancer cell growth via an AMPK-PGC-1alpha-mediated metabolic switch. Oncogene advance online publication 14 November 2013; doi:10.1038/ONC.2013.463.
39. Dehm SM, Schmidt LJ, Heemers HV, Vessella RL, Tindall DJ. Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance. Cancer Res 2008; 68: 5469-5477.
40. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149: 274-293.
41. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 2010; 39: 171-183.
42. Wu Y, Chhipa RR, Cheng J, Zhang H, Mohler JL, Ip C. Androgen receptor-mTOR crosstalk is regulated by testosterone availability: implication for prostate cancer cell survival. Anticancer Res 2010; 30: 3895-3901.
43. Xu Y, Chen SY, Ross KN, Balk SP. Androgens induce prostate cancer cell proliferation through mammalian target of rapamycin activation and posttranscriptional increases in cyclin D proteins. Cancer Res 2006; 66: 7783-7792.
44. Sircar K, Yoshimoto M, Monzon FA, Koumakpayi IH, Katz RL, Khanna A et al. PTEN genomic deletion is associated with p-Akt and AR signalling in poorer outcome, hormone refractory prostate cancer. J Pathol 2009; 218: 505-513.
45. Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, Jiao J et al. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 2003; 4: 209-221.
46. Choi N, Zhang B, Zhang L, Ittmann M, Xin L. Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation. Cancer Cell 2012; 21: 253-265.
47. Zhang L, Zhang B, Han SJ, Shore AN, Rosen JM, Demayo FJ et al. Targeting CreER(T2) expression to keratin 8-expressing murine simple epithelia using bacterial artificial chromosome transgenesis. Transgenic Res 2012; 21: 1117-1123.
48. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
49. Lu SC. Regulation of glutathione synthesis. Mol Aspects Med 2009; 30: 42-59.
50. Beaconsfield P, Ginsburg J, Jeacock MK. Glucose metabolism via the pentose phosphate pathway relative to nucleic acid and protein synthesis in the human placenta. Dev Med Child Neurol 1964; 6: 469-474.
51. Sukhatme VP, Chan B. Glycolytic cancer cells lacking 6-phosphogluconate dehydrogenase metabolize glucose to induce senescence. FEBS Lett 2012; 586: 2389-2395.
52. Wang C, Guo K, Gao D, Kang X, Jiang K, Li Y et al. Identification of transaldolase as a novel serum biomarker for hepatocellular carcinoma metastasis using xenografted mouse model and clinic samples. Cancer Lett 2011; 313: 154-166.
53. Foldi M, Stickeler E, Bau L, Kretz O, Watermann D, Gitsch G et al. Transketolase protein TKTL1 overexpression: A potential biomarker and therapeutic target in breast cancer. Oncol Rep 2007; 17: 841-845.
54. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S et al. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 2008; 8: 224-236.
55. Swinnen JV, Verhoeven G. Androgens and the control of lipid metabolism in human prostate cancer cells. J Steroid Biochem Mol Biol 1998; 65: 191-198.
56. Heemers H, Verrijdt G, Organe S, Claessens F, Heyns W, Verhoeven G et al. Identification of an androgen response element in intron 8 of the sterol regulatory element-binding protein cleavage-Activating protein gene allowing direct regulation by the androgen receptor. J Biol Chem 2004; 279: 30880-30887.
57. Ettinger SL, Sobel R, Whitmore TG, Akbari M, Bradley DR, Gleave ME et al. Dysregulation of sterol response element-binding proteins and downstream effectors in prostate cancer during progression to androgen independence. Cancer Res 2004; 64: 2212-2221.
58. Dufner A, Thomas G. Ribosomal S6 kinase signaling and the control of translation. Exp Cell Res 1999; 253: 100-109.
59. Wang X, Proud CG. The mTOR pathway in the control of protein synthesis. Physiology (Bethesda) 2006; 21: 362-369.
60. Kimball SR. Interaction between the AMP-Activated protein kinase and mTOR signaling pathways. Med Sci Sports Exerc 2006; 38: 1958-1964.
61. Ortega-Molina A, Serrano M. PTEN in cancer, metabolism, and aging. Trends Endocrinol Metab 2013; 24: 184-189.
62. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997; 275: 1943-1947.
63. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010; 18: 11-22.
64. Morgan TM, Koreckij TD, Corey E. Targeted therapy for advanced prostate cancer: inhibition of the PI3K/Akt/mTOR pathway. Curr Cancer Drug Targets 2009; 9: 237-249.
65. Rai JS, Henley MJ, Ratan HL. Mammalian target of rapamycin: a new target in prostate cancer. Urol Oncol 2010; 28: 134-138.
66. Bitting RL, Armstrong AJ. Targeting the PI3K/Akt/mTOR pathway in castrationresistant prostate cancer. Endocr Relat Cancer 2013; 20: R83-R99.
67. Frigo DE, McDonnell DP. Differential effects of prostate cancer therapeutics on neuroendocrine transdifferentiation. Mol Cancer Ther 2008; 7: 659-669.
68. Culig Z, Hoffmann J, Erdel M, Eder IE, Hobisch A, Hittmair A et al. Switch from antagonist to agonist of the androgen receptor bicalutamide is associated with prostate tumour progression in a new model system. Br J Cancer 1999; 81: 242-251.
69. Frigo DE, Howe MK, Wittmann BM, Brunner AM, Cushman I, Wang Q et al. CaM kinase kinase beta-mediated activation of the growth regulatory kinase AMPK is required for androgen-dependent migration of prostate cancer cells. Cancer Res 2011; 71: 528-537.
70. Zhang B, Chen H, Zhang L, Dakhova O, Zhang Y, Lewis MT et al. A dosagedependent pleiotropic role of Dicer in prostate cancer growth and metastasis. Oncogene advance online publication 15 July 2013; doi:10.1038/ONC.2013.281.