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Differential expression of genes that encode glycolysis enzymes in kidney and lung cancer in humans

  • Molecular Genetics
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Abstract

Glycolysis is a main catabolic pathway of glucose metabolism, accompanied by ATP synthesis. More than 30 enzymes are involved in glycolysis, and genes that encode them can be considered housekeeping genes due to the high conservatism and evolutionary antiquity of the process. We studied the expression of these genes in kidney papillary cancer and planocellular lung cancer via the bioinformatic analysis of transcriptome database and method of quantitative real time PCR. Quantitative analysis of mRNA level demonstrated that only a part of genes that encode glycolysis enzymes maintain relatively stable mRNA level, including the HK1, ADPGK, GPI, PGK1, and PKM2 genes in kidney papillary cancer and the ADPGK, ALDOA, GAPDH, PGK1, BPGM, ENO1, and PKM2 genes in planocellular lung cancer. The frequent increase in the mRNA expression of PFKP, ALDOA, and GAPDH genes in kidney cancer, as well as the GPI gene in lung cancer, were detected for the first time by real time PCR. For other genes, their differential expression was demonstrated; the cases of both a decrease and increase in the mRNA level were detected. Thus, several genes that can be used as control genes in transcriptome analysis by real time PCR in kidney and lung cancer, as well as a number of differentially expressed genes that can be potential oncomarkers, were identified.

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References

  1. Shen, Y., Li, Y., Ye, F., et al., Identification of suitable reference genes for measurement of gene expression in human cervical tissues, Anal. Biochem., 2010, vol. 405, no. 2, pp. 224–229.

    Article  PubMed  CAS  Google Scholar 

  2. Stamova, B.S., Apperson, M., Walker, W.L., et al., Identification and validation of suitable endogenous reference genes for gene expression studies in human peripheral blood, BMC Med. Genomics, 2009, vol. 2, pp. 49–61.

    Article  PubMed  Google Scholar 

  3. Zainuddin, A., Chua, K.H., Abdul Rahim, N., et al., Effect of experimental treatment on GAPDH mRNA expression as a housekeeping gene in human diploid fibroblasts, BMC Mol. Biol., 2010, vol. 11, pp. 59–65.

    Article  PubMed  Google Scholar 

  4. Cheng, C., Long, X., Li, X., et al., The expressions of alpha-enolase in the nasopharyngeal cancer tissue, Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi, 2011, vol. 25, no. 12, pp. 554–556.

    PubMed  CAS  Google Scholar 

  5. Jahns, F., Wilhelm, A., Greulich, K.O., et al., Impact of butyrate on PKM2 and HSP90beta expression in human colon tissues of different transformation stages: A comparison of gene and protein data, Genes Nutr., 2012, vol. 7, no. 2, pp. 235–246.

    Article  PubMed  CAS  Google Scholar 

  6. Soh, M.A., Garrett, S.H., Somji, S., et al., Arsenic, cadmium and neuron specific enolase (ENO2, gammaenolase) expression in breast cancer, Cancer Cell Int., 2011, vol. 11, no. 1, pp. 41–52.

    Article  PubMed  CAS  Google Scholar 

  7. Jemal, A., Bray, F., Center, M.M., et al., Global cancer statistics, CA Cancer J. Clin., 2011, vol. 61, no. 2, pp. 69–90.

    Article  PubMed  Google Scholar 

  8. Thoenes, W., Storkel, S., Rumpelt, H.J., et al., Renal cell carcinoma-a classification based on cytomorphological criteria, Zentralbl. Allg. Pathol. Anat., 1986, vol. 132, no. 56, pp. 503–513.

    CAS  Google Scholar 

  9. dbEST. http://www.ncbi.nlm.nih.gov/sites/entrez?db=nucest

  10. GeneHub GEPIS. http://research-public.gene.com/Research/genentech/genehub-gepis/index.html

  11. Jung, M., Ramankulov, A., Roigas, J., et al., In search of suitable reference genes for gene expression studies of human renal cell carcinoma by real-time PCR, BMC Mol. Biol., 2007, vol. 8, pp. 47–59.

    Article  PubMed  Google Scholar 

  12. Krasnov, G.S., Oparina, N.Yu., Dmitriev, A.A., et al., RPN1, a new reference gene for quantitative data normalization in lung and kidney cancer, Mol. Biol. (Moscow), 2011, vol. 45, no. 2, pp. 211–220.

    Article  CAS  Google Scholar 

  13. UCSC. http://genome.ucsc.edu

  14. Oncomine. http://www.oncomine.org

  15. Senchenko, V.N., Krasnov, G.S., Dmitriev, A.A., et al., Differential expression of CHL1 gene during development of major human cancers, PLoS One, 2011, vol. 6, no. 3, p. e15612

    Article  PubMed  CAS  Google Scholar 

  16. Fothergill-Gilmore, L.A. and Michels, P.A., Evolution of glycolysis, Prog. Biophys. Mol. Biol., 1993, vol. 59, no. 2, pp. 105–235.

    Article  PubMed  CAS  Google Scholar 

  17. Heinrich, R., Melendez-Hevia, E., Montero, F., et al., The structural design of glycolysis: An evolutionary approach, Biochem. Soc. Trans., 1999, vol. 27, no. 2, pp. 294–298.

    PubMed  CAS  Google Scholar 

  18. Karantanis, D., Allen-Auerbach, M., and Czernin, J., Relationship among glycolytic phenotype, grade, and histological subtype in ovarian carcinoma, Clin. Nucl. Med., 2012, vol. 37, no. 1, pp. 49–53.

    Article  PubMed  Google Scholar 

  19. Moreno-Sanchez, R., Rodriguez-Enriquez, S., Saavedra, E., et al., The bioenergetics of cancer: Is glycolysis the main ATP supplier in all tumor cells?, Biofactors, 2009, vol. 35, no. 2, pp. 209–225.

    Article  PubMed  CAS  Google Scholar 

  20. Gatenby, R.A. and Gillies, R.J., Glycolysis in cancer: A potential target for therapy, Int. J. Biochem. Cell Biol., 2007, vol. 39, nos. 7–8, pp. 1358–1366.

    Article  PubMed  CAS  Google Scholar 

  21. Kurtoglu, M. and Lampidis, T.J., From delocalized lipophilic cations to hypoxia: Blocking tumor cell mitochondrial function leads to therapeutic gain with glycolytic inhibitors, Mol. Nutr. Food Res., 2009, vol. 53, no. 1, pp. 68–75.

    Article  PubMed  CAS  Google Scholar 

  22. Bujalowska, B., Contribution from the Wielkopolska territories to the history of medicine and studies in the field of history of medicine in the Nowiny Lekarskie, Arch. Hist. Med., 1975, vol. 38, no. 1, pp. 23–31.

    CAS  Google Scholar 

  23. Niinaka, Y., Paku, S., Haga, A., et al., Expression and secretion of neuroleukin/phosphohexose isomerase/maturation factor as autocrine motility factor by tumor cells, Cancer Res., 1998, vol. 58, no. 12, pp. 2667–2674.

    PubMed  CAS  Google Scholar 

  24. Hofer, M.D., Browne, T.J., He, L., et al., Identification of two molecular groups of seminomas by using expression and tissue microarrays, Clin. Cancer Res., 2005, vol. 11, no. 16, pp. 5722–5729.

    Article  PubMed  CAS  Google Scholar 

  25. Lin, C.C., Chen, L.C., Tseng, V.S., et al., Malignant pleural effusion cells show aberrant glucose metabolism gene expression, Eur. Respir. J., 2011, vol. 37, no. 6, pp. 1453–1465.

    Article  PubMed  Google Scholar 

  26. Suzuki A., Iizuka A., Komiyama M. et al. Identification of melanoma antigens using a serological proteome approach (SERPA), Cancer Genomics Proteomics, 2010, vol. 7, no. 1, pp. 17–23.

    PubMed  CAS  Google Scholar 

  27. Rho, J.H., Roehrl, M.H., and Wang, J.Y., Glycoproteomic analysis of human lung adenocarcinomas using glycoarrays and tandem mass spectrometry: differential expression and glycosylation patterns of vimentin and fetuin A isoforms, Protein J., 2009, vol. 28, nos. 3–4, pp. 148–160.

    Article  PubMed  CAS  Google Scholar 

  28. Vila, M.R., Nicolas, A., Morote, J., et al., Increased glyceraldehyde-3-phosphate dehydrogenase expression in renal cell carcinoma identified by RNA-based, arbitrarily primed polymerase chain reaction, Cancer, 2000, vol. 89, no. 1, pp. 152–164.

    Article  PubMed  CAS  Google Scholar 

  29. Lay, A.J., Jiang, X.M., Kisker, O., et al., Phosphoglycerate kinase acts in tumor angiogenesis as a disulphide reductase, Nature, 2000, vol. 408, no. 6814, pp. 869–873.

    Article  PubMed  CAS  Google Scholar 

  30. Vander Heiden, M.G., Locasale, J.W., Swanson, K.D., et al., Evidence for an alternative glycolytic pathway in rapidly proliferating cells, Science, 2010, vol. 329, no. 5998, pp. 1492–1499.

    Article  Google Scholar 

  31. Lei, Y., Huang, K., Gao, C., et al., Proteomics identification of ITGB3 as a key regulator in reactive oxygen species-induced migration and invasion of colorectal cancer cells, Mol. Cell Proteomics, 2011, vol. 10, no. 10, p. M110 005397.

    PubMed  Google Scholar 

  32. Ren, F., Wu, H., Lei, Y., et al., Quantitative proteomics identification of phosphoglycerate mutase 1 as a novel therapeutic target in hepatocellular carcinoma, Mol. Cancer, 2010, vol. 9, pp. 81–98.

    Article  PubMed  Google Scholar 

  33. Yan, G.R., Xu, S.H., Tan, Z.L., et al., Proteomics characterization of gastrokine 1-induced growth inhibition of gastric cancer cells, Proteomics, 2011, vol. 11, no. 18, pp. 3657–3664.

    Article  PubMed  CAS  Google Scholar 

  34. Bai, Z., Ye, Y., Liang, B., et al., Proteomics-based identification of a group of apoptosis-related proteins and biomarkers in gastric cancer, Int. J. Oncol., 2011, vol. 38, no. 2, pp. 375–383.

    PubMed  CAS  Google Scholar 

  35. Zhang, Y., Li, M., Liu, Y., et al., ENO1 protein levels in the tumor tissues and circulating plasma samples of non-small cell lung cancer patients, Zhongguo Fei Ai Za Zhi, 2010, vol. 13, no. 12, pp. 1089–1093.

    PubMed  CAS  Google Scholar 

  36. Tu, S.H., Chang, C.C., Chen, C.S., et al., Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells, Breast Cancer Res. Tret., 2010, vol. 121, no. 3, pp. 539–553.

    Article  CAS  Google Scholar 

  37. Chang, G.C., Liu, K.J., Hsieh, C.L., et al., Identification of alpha-enolase as an autoantigen in lung cancer: Its overexpression is associated with clinical outcomes, Clin. Cancer Res., 2006, vol. 12, no. 19, pp. 5746–5754.

    Article  PubMed  CAS  Google Scholar 

  38. Christofk, H.R., Vander Heiden, M.G., Harris, M.H., et al., The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumor growth, Nature, 2008, vol. 452, no. 7184, pp. 230–233.

    Article  PubMed  CAS  Google Scholar 

  39. David, C.J., Chen, M., Assanah, M., et al., HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer, Nature, 2010, vol. 463, no. 7279, pp. 364–368.

    Article  PubMed  CAS  Google Scholar 

  40. Kitagawa, S., Obata, T., Hasumura, S., et al., A cellular 3,3’,5-triiodo-L-thyronine binding protein from a human carcinoma cell line: Purification and characterization, Biol. Chem., 1987, vol. 262, no. 8, pp. 3903–3908.

    CAS  Google Scholar 

  41. Tani, K., Yoshida, M.C., Satoh, H., et al., Human M2-type pyruvate kinase: cDNA cloning, chromosomal assignment and expression in hepatoma, Gene, 1988, vol. 73, no. 2, pp. 509–516.

    Article  PubMed  CAS  Google Scholar 

  42. GeneCards. http://www.genecards.org/

  43. NCBI Pubmed. http://www.ncbi.nlm.nih.gov/pubmed/

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Correspondence to N. Yu. Oparina.

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Original Russian Text © N.Yu. Oparina, A.V. Snezhkina, A.F. Sadritdinova, V.A. Veselovskii, A.A. Dmitriev, V.N. Senchenko, N.V. Mel’nikova, A.S. Speranskaya, M.V. Darii, O.A. Stepanov, I.M. Barkhatov, A.V. Kudryavtseva, 2013, published in Genetika, 2013, Vol. 49, No. 7, pp. 814–823.

The authors contributed equally to this work.

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Oparina, N.Y., Snezhkina, A.V., Sadritdinova, A.F. et al. Differential expression of genes that encode glycolysis enzymes in kidney and lung cancer in humans. Russ J Genet 49, 707–716 (2013). https://doi.org/10.1134/S1022795413050104

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