Variant G6PD levels promote tumor cell proliferation or apoptosis via the STAT3/5 pathway in the human melanoma xenograft mouse model

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Hu, Tao ^a,b   Zhang, Chunhua ^a,c   Tang, Qiongling ^a,d   Su, Yanan ^e   Li, Bo ^a   Chen, Long ^a   Zhang, Zheng ^a   Cai, Tianchi ^a   Zhu, Yuechun ^a  

^a KUNMING MEDICAL UNIVERSITY   (China)

^b The Third People's Hospital of Yunnan Province   (China)

^c Yunnan Maternal and Child Health Hospital   (China)

^d Shenzhen Maternal and Child Health Hospital   (China)

^e GenProMarkers Inc   (United States)

Author keywords

Apoptosis; Glucose 6 phosphate dehydrogenase; Melanoma; Nude mice; Signal transduction and transcription activator

Indexed keywords

CALVASCULIN; CELL CYCLE PROTEIN; COMPLEMENTARY DNA; CYCLIN D1; CYCLIN E; FAS ANTIGEN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P53; STAT3 PROTEIN; STAT5 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER TISSUE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; CUTANEOUS MELANOMA; DOWN REGULATION; G6PD GENE; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; GROWTH INHIBITION; HUMAN; HUMAN CELL; MELANOCYTE; MELANOMA CELL; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; WESTERN BLOTTING; WILD TYPE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GENETIC VARIATION; GLUCOSEPHOSPHATE DEHYDROGENASE; HETEROGRAFTS; HUMANS; MELANOMA; MICE; MICE, NUDE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR;

EID: 84878005738     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-251     Document Type: Article

References (47)

1. Cappellini MD, Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet 2008, 371(9606):64-74. 10.1016/S0140-6736(08)60073-2, 18177777.
2. Beutler E. G6PD deficiency. Blood 1994, 84(11):3613-3636.
3. WHO Working Group Glucose-6-phosphate dehydrogenase deficiency. Bull World Health Organ 1989, 67(6):601-611. 67, 2491315, 2633878, WHO Working Group.
4. Minucci A, Moradkhani K, Hwang MJ, Zuppi C, Giardina B, Capoluongo E. Glucose-6-phosphate dehydrogenase (G6PD) mutations database: review of the " old" and update of the new mutations. Blood Cells Mol Dis 2012, 48(3):154-165. 10.1016/j.bcmd.2012.01.001, 22293322.
5. Zhao X, Li Z, Zhang X. G6PD-MutDB: a mutation and phenotype database of glucose-6-phosphate (G6PD) deficiency. J Bioinforma Comput Biol 2010, 8(Suppl 1):101-109.
6. Yang Y, Zhu Y, Li D, Li Z, Lu H, Wu J, Tang J, Tong S. Characterization of glucose-6-phosphate dehydrogenase deficiency and identification of a novel haplotype 487G>A/IVS5-612(G>C) in the Achang population of Southwestern China. Science in China Series C, Life sciences / Chinese Academy of Sciences 2007, 50(4):479-485. 10.1007/s11427-007-0072-7, 17653668.
7. Louicharoen C, Patin E, Paul R, Nuchprayoon I, Witoonpanich B, Peerapittayamongkol C, Casademont I, Sura T, Laird NM, Singhasivanon P. Positively selected G6PD-Mahidol mutation reduces Plasmodium vivax density in Southeast Asians. Science 2009, 326(5959):1546-1549. 10.1126/science.1178849, 20007901.
8. Panich V. Glucose-6-phosphate dehydrogenase deficiency. Part 2. Tropical Asia. Clin Haematol 1981, 10(3):800-814.
9. Hedrick PW. Population genetics of malaria resistance in humans. Heredity 2011, 107(4):283-304. 10.1038/hdy.2011.16, 3182497, 21427751.
10. Casanova JL, Abel L, Quintana-Murci L. Human TLRs and IL-1Rs in host defense: natural insights from evolutionary, epidemiological, and clinical genetics. Annu Rev Immunol 2011, 29:447-491. 10.1146/annurev-immunol-030409-101335, 21219179.
11. Batetta B, Pulisci D, Bonatesta RR, Sanna F, Piras S, Mulas MF, Spano O, Putzolu M, Broccia G, Dessi S. G6PD activity and gene expression in leukemic cells from G6PD-deficient subjects. Cancer Lett 1999, 140(1-2):53-58.
12. Wang J, Yuan W, Chen Z, Wu S, Chen J, Ge J, Hou F. Overexpression of G6PD is associated with poor clinical outcome in gastric cancer. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine 2012, 33(1):95-101.
13. Langbein S, Frederiks WM, zur Hausen A, Popa J, Lehmann J, Weiss C, Alken P, Coy JF. Metastasis is promoted by a bioenergetic switch: new targets for progressive renal cell cancer. Int J Cancer 2008, 122(11):2422-2428. 10.1002/ijc.23403, 18302154.
14. Van Driel BE, Valet GK, Lyon H, Hansen U, Song JY, Van Noorden CJ. Prognostic estimation of survival of colorectal cancer patients with the quantitative histochemical assay of G6PDH activity and the multiparameter classification program CLASSIF1. Cytometry 1999, 38(4):176-183. 10.1002/(SICI)1097-0320(19990815)38:4<176::AID-CYTO4>3.0.CO;2-#, 10440855.
15. Polat MF, Taysi S, Gul M, Cikman O, Yilmaz I, Bakan E, Erdogan F. Oxidant/antioxidant status in blood of patients with malignant breast tumour and benign breast disease. Cell Biochem Funct 2002, 20(4):327-331. 10.1002/cbf.980, 12415567.
16. Philipson KA, Elder MG, White JO. The effects of medroxyprogesterone acetate on enzyme activities in human endometrial carcinoma. J Steroid Biochem 1985, 23(6A):1059-1064.
17. 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. Medical principles and practice: international journal of the Kuwait University, Health Science Centre 2010, 19(6):433-439.
18. Rao KN, Elm MS, Kelly RH, Chandar N, Brady EP, Rao B, Shinozuka H, Eagon PK. Hepatic hyperplasia and cancer in rats: metabolic alterations associated with cell growth. Gastroenterology 1997, 113(1):238-248. 10.1016/S0016-5085(97)70101-X, 9207284.
19. Kobayashi M, Fujita I, Itagaki S, Hirano T, Iseki K. Transport mechanism for L-lactic acid in human myocytes using human prototypic embryonal rhabdomyosarcoma cell line (RD cells). Biol Pharm Bull 2005, 28(7):1197-1201. 10.1248/bpb.28.1197, 15997097.
20. Maly K, Hochleitner B, Uberall F, Loferer H, Oberhuber H, Doppler W, Grunicke H. Mechanism and biological significance of the Ha-ras-induced activation of the Na+/H(+)-antiporter. Adv Enzym Regul 1990, 30:63-74.
21. Messina JL, Yu H, Riker AI, Munster PN, Jove RL, Daud AI. Activated stat-3 in melanoma. Cancer control: journal of the Moffitt Cancer Center 2008, 15(3):196-201.
22. Mirmohammadsadegh A, Hassan M, Bardenheuer W, Marini A, Gustrau A, Nambiar S, Tannapfel A, Bojar H, Ruzicka T, Hengge UR. STAT5 phosphorylation in malignant melanoma is important for survival and is mediated through SRC and JAK1 kinases. J Investig Dermatol 2006, 126(10):2272-2280. 10.1038/sj.jid.5700385, 16741510.
23. Bromberg J. Stat proteins and oncogenesis. J Clin Investig 2002, 109(9):1139-1142. 150969, 11994401.
24. Li D, Zhu Y, Tang Q, Lu H, Li H, Yang Y, Li Z, Tong S. A new G6PD knockdown tumor-cell line with reduced proliferation and increased susceptibility to oxidative stress. Cancer Biother Radiopharm 2009, 24(1):81-90. 10.1089/cbr.2008.0494, 19243250.
25. Eisinger M, Marko O. Selective proliferation of normal human melanocytes in vitro in the presence of phorbol ester and cholera toxin. Proc Natl Acad Sci U S A 1982, 79(6):2018-2022. 10.1073/pnas.79.6.2018, 346113, 6952249.
26. Niu G, Heller R, Catlett-Falcone R, Coppola D, Jaroszeski M, Dalton W, Jove R, Yu H. Gene therapy with dominant-negative Stat3 suppresses growth of the murine melanoma B16 tumor in vivo. Cancer Res 1999, 59(20):5059-5063.
27. Raisova M, Bektas M, Wieder T, Daniel P, Eberle J, Orfanos CE, Geilen CC. Resistance to CD95/Fas-induced and ceramide-mediated apoptosis of human melanoma cells is caused by a defective mitochondrial cytochrome c release. FEBS Lett 2000, 473(1):27-32. 10.1016/S0014-5793(00)01491-5, 10802053.
28. Sauter ER, Yeo UC, von Stemm A, Zhu W, Litwin S, Tichansky DS, Pistritto G, Nesbit M, Pinkel D, Herlyn M, et al. Cyclin D1 is a candidate oncogene in cutaneous melanoma. Cancer Res 2002, 62(11):3200-3206.
29. Arooz T, Yam CH, Siu WY, Lau A, Li KK, Poon RY. On the concentrations of cyclins and cyclin-dependent kinases in extracts of cultured human cells. Biochemistry 2000, 39(31):9494-9501. 10.1021/bi0009643, 10924145.
30. Bales E, Mills L, Milam N, McGahren-Murray M, Bandyopadhyay D, Chen D, Reed JA, Timchenko N, van den Oord JJ, Bar-Eli M, et al. The low molecular weight cyclin E isoforms augment angiogenesis and metastasis of human melanoma cells in vivo. Cancer Res 2005, 65(3):692-697.
31. Bergman R, Shemer A, Levy R, Friedman-Birnbaum R, Trau H, Lichtig C. Immunohistochemical study of p53 protein expression in Spitz nevus as compared with other melanocytic lesions. Am J Dermatopathol 1995, 17(6):547-550. 10.1097/00000372-199512000-00003, 8599466.
32. Miracco C, Santopietro R, Biagioli M, Lazzi S, Nyongo A, Vatti R, Luzi P. Different patterns of cell proliferation and death and oncogene expression in cutaneous malignant melanoma. J Cutan Pathol 1998, 25(5):244-251. 10.1111/j.1600-0560.1998.tb01728.x, 9696289.
33. Murtas D, Piras F, Minerba L, Ugalde J, Floris C, Maxia C, Demurtas P, Perra MT, Sirigu P. Nuclear 8-hydroxy-2'-deoxyguanosine as survival biomarker in patients with cutaneous melanoma. Oncol Rep 2010, 23(2):329-335.
34. Jiang P, Du W, Wang X, Mancuso A, Gao X, Wu M, Yang X. p53 regulates biosynthesis through direct inactivation of glucose-6-phosphate dehydrogenase. Nat Cell Biol 2011, 13(3):310-316. 10.1038/ncb2172, 3110666, 21336310.
35. Cajone F, Sherbet GV. Stathmin is involved in S100A4-mediated regulation of cell cycle progression. Clin Exp Metastasis 1999, 17(10):865-871. 10.1023/A:1006778804532, 11089885.
36. Sherbet GV, Lakshmi MS. S100A4 (MTS1) calcium binding protein in cancer growth, invasion and metastasis. Anticancer Res 1998, 18(4A):2415-2421.
37. Bullani RR, Wehrli P, Viard-Leveugle I, Rimoldi D, Cerottini JC, Saurat JH, Tschopp J, French LE. Frequent downregulation of Fas (CD95) expression and function in melanoma. Melanoma Res 2002, 12(3):263-270. 10.1097/00008390-200206000-00010, 12140383.
38. Brunelle JK, Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J Cell Sci 2009, 122(Pt 4):437-441. 2714431, 19193868.
39. Heath-Engel HM, Chang NC, Shore GC. The endoplasmic reticulum in apoptosis and autophagy: role of the BCL-2 protein family. Oncogene 2008, 27(50):6419-6433. 10.1038/onc.2008.309, 18955970.
40. Raisova M, Hossini AM, Eberle J, Riebeling C, Wieder T, Sturm I, Daniel PT, Orfanos CE, Geilen CC. The Bax/Bcl-2 ratio determines the susceptibility of human melanoma cells to CD95/Fas-mediated apoptosis. J Investig Dermatol 2001, 117(2):333-340. 10.1046/j.0022-202x.2001.01409.x, 11511312.
41. Barton BE, Karras JG, Murphy TF, Barton A, Huang HF. Signal transducer and activator of transcription 3 (STAT3) activation in prostate cancer: Direct STAT3 inhibition induces apoptosis in prostate cancer lines. Mol Cancer Ther 2004, 3(1):11-20. 10.1186/1476-4598-3-11, 14749471.
42. Hatiboglu MA, Kong LY, Wei J, Wang Y, McEnery KA, Fuller GN, Qiao W, Davies MA, Priebe W, Heimberger AB. The tumor microenvironment expression of p-STAT3 influences the efficacy of cyclophosphamide with WP1066 in murine melanoma models. International journal of cancer Journal international du cancer 2012, 131(1):8-17. 10.1002/ijc.26307, 3319790, 21792892.
43. Manuel ER, Blache CA, Paquette R, Kaltcheva TI, Ishizaki H, Ellenhorn JD, Hensel M, Metelitsa L, Diamond DJ. Enhancement of cancer vaccine therapy by systemic delivery of a tumor-targeting Salmonella-based STAT3 shRNA suppresses the growth of established melanoma tumors. Cancer Res 2011, 71(12):4183-4191. 10.1158/0008-5472.CAN-10-4676, 3117077, 21527558.
44. Farley J, Smith LM, Darcy KM, Sobel E, O'Connor D, Henderson B, Morrison LE, Birrer MJ. Cyclin E expression is a significant predictor of survival in advanced, suboptimally debulked ovarian epithelial cancers: a Gynecologic Oncology Group study. Cancer Res 2003, 63(6):1235-1241.
45. Krasilnikov M, Ivanov VN, Dong J, Ronai Z. ERK and PI3K negatively regulate STAT-transcriptional activities in human melanoma cells: implications towards sensitization to apoptosis. Oncogene 2003, 22(26):4092-4101. 10.1038/sj.onc.1206598, 12821943.
46. Zhuang L, Lee CS, Scolyer RA, McCarthy SW, Zhang XD, Thompson JF, Hersey P. Mcl-1, Bcl-XL and Stat3 expression are associated with progression of melanoma whereas Bcl-2, AP-2 and MITF levels decrease during progression of melanoma. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 2007, 20(4):416-426.
47. Wellbrock C, Weisser C, Hassel JC, Fischer P, Becker J, Vetter CS, Behrmann I, Kortylewski M, Heinrich PC, Schartl M. STAT5 contributes to interferon resistance of melanoma cells. Curr Biol 2005, 15(18):1629-1639. 10.1016/j.cub.2005.08.036, 16169484.