Sodium-glucose cotransporters: new targets of cancer therapy?

1. Vrhovac I, Breljak D, Sabolić I. Glucose transporters in the mammalian blood cells. Period Biol 2014;116:131-8.Search in Google Scholar

2. Mueckler M, Thorens B. The SLC2 (GLUT) family of membrane transporters. Mol Aspects Med 2013;34:121-38. doi: 10.1016/j.mam.2012.07.00123506862Search in Google Scholar

3. Wright E. Glucose transport families SLC5 and SLC50. Mol Aspects Med 2013;34:183-96. doi: 10.1016/j.mam.2012.11.00223506865Search in Google Scholar

4. Wright E, Loo D, Hirayama B. Biology of human sodium glucose transporters. Physiol Rev 2011;91:733-94. doi: 10.1152/physrev.00055.200921527736Search in Google Scholar

5. Hediger M, Rhoads D. Molecular physiology of sodiumglucose cotransporters. Physiol Rev 1994;74:993-1026. doi: 10.1152/physrev.1994.74.4.993Search in Google Scholar

6. Wright EM, Ghezzi C, Loo DDF. Novel and unexpected functions of SGLTs. Physiology 2017;32:435-43. doi: 10.1152/physiol.00021.2017Search in Google Scholar

7. Thorens B, Mueckler M. Glucose transporters in the 21st Century. Am J Physiol-Endoc M 2010;298:E141-5. doi: 10.1152/ajpendo.00712.2009Search in Google Scholar

8. Wright EM, Loo DD, Panayotova-Heiermann M, Lostao MP, Hirayama BH, Mackenzie B, Boorer K, Zampighi G. “Active” sugar transport in eukaryotes. J Exp Biol 1994;196:197-212. PMID: 782302210.1242/jeb.196.1.1977823022Search in Google Scholar

9. Otto W. On the origin of cancer cells. Science 1956;123:309-14. doi: 10.1126/science.123.3191.309Search in Google Scholar

10. Vander Heiden M, Cantley L, Thompson C. Understanding the Warburg effect: the metabolic requiremetns of cell proliferation. Science 2009;324:1029-33. doi: 10.1126/ science.1160809Search in Google Scholar

11. Yu L, Chen X, Wang L, Chen S. The sweet trap in tumors: aerobic glycolysis and potential targets for therapy. Oncotarget 2016;7:38908-26. doi: 10.18632/oncotarget.7676Search in Google Scholar

12. Herrmann K, Benz MR, Krause BJ, Pomykala KL, Buck AK, Czernin J. (18)F-FDG-PET/CT in evaluating response to therapy in solid tumors: where we are and where we can go. Q J Nucl Med Mol Im 2011;55:620-32. PMID: 22231582Search in Google Scholar

13. Ganapathy V, Thangaraju M, Prasad PD. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Therapeut 2009;121:29-40. doi: 10.1016/j. pharmthera.2008.09.005Search in Google Scholar

14. Szablewski L. Expression of glucose transporters in cancers. Biochim Biophys Acta 2013;1835:164-9. doi: 10.1016/j.bbcan.2012.12.004Search in Google Scholar

15. Ouiddir A, Planès C, Fernandes I, VanHesse A, Clerici C. Hypoxia upregulates activity and expression of the glucose transporter GLUT1 in alveolar epithelial cells. Am J Resp Cell Mol 1999;21:710-8. doi: 10.1165/ajrcmb.21.6.3751Search in Google Scholar

16. Zhang J-Z, Behrooz A, Ismail-Beigi F. Regulation of glucose transport by hypoxia. Am J Kidney Dis 1999;34:189-202. doi: 10.1016/S0272-6386(99)70131-9Search in Google Scholar

17. Baumann MU, Zamudio S, Ilsley N. Hypoxic upregulation of glucose transporters in BeWo choriocarcinoma cells is mediated by hypoxia-inducible factor-1. Am J Physiol-Cell Ph 2007;293:C477-85. doi: 10.1152/ajpcell.00075.2007Search in Google Scholar

18. Gorboulev V, Schürmann A, Vallon V, Kipp H, Jaschke A, Klessen D, Friedrich A, Scherneck S, Rieg T, Cunard R, Veyhl-Wichmann M, Srinivasan A, Balen D, Breljak D, Rexhepaj R, Parker HE, Gribble FM, Reimann F, Lang F, Wiese S, Sabolić I, Sendtner M, Koepsell H. Na+-D-glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes 2012;61:187-96. doi: 10.2337/db11-1029Search in Google Scholar

19. Wright EM, Turk E. The sodium/glucose cotransport family SLC5. Pflügers Arch 2004;447:510-8. doi: 10.1007/s00424-003-1063-6Search in Google Scholar

20. Vallon V. Molecular determinants of renal glucose reabsorption. Focus on “Glucose transport by human renal Na+/D-glucose cotransporters SGLT1 and SGLT2”. Am J Physiol-Cell Ph 2011;300:C6-8. doi: 10.1152/ ajpcell.00444.2010Search in Google Scholar

21. Loo DDF, Wright EM, Zeuthen T. Water pumps. J Physiol 2002;542:53-60. doi: 10.1113/jphysiol.2002.018713Search in Google Scholar

22. Sabolić I, Vrhovac I, Balen Eror D, Gerasimova M, Rose M, Breljak D, Ljubojević M, Brzica H, Sebastiani A, Thal SC, Sauvant C, Kipp H, Vallon V, Koepsell H. Expression of Na+-D-glucose cotransporter SGLT2 in rodents is kidneyspecific and exhibits sex and species differences. Am J Physiol-Cell Ph 2012;302:C1174-88. doi: 10.1152/ajpcell.00450.2011Search in Google Scholar

23. Vrhovac I, Balen Eror D, Klessen D, Burger C, Breljak D, Kraus O, Radović N, Jadrijević S, Aleksić I, Walles T, Sauvant C, Sabolić I, Koepsell H. Localizations of Na+-Dglucose cotransporters SGLT1 and SGLT2 in human kidney and of SGLT1 in human small intestine, liver, lung, and heart. Pflügers Arch 2015;467:1881-98. doi: 10.1007/s00424-014-1619-7Search in Google Scholar

24. Vrhovac Madunić I, Breljak D, Karaica D, Koepsell H, Sabolić I. Expression profiling and immunolocalization of Na+-D-glucose-cotransporter 1 in mice employing knockout mice as specificity control indicate novel locations and differences between mice and rats. Pflügers Arch 2017;469:1545-65. doi: 10.1007/s00424-017-2056-1Search in Google Scholar

25. Chen J, Williams S, Ho S, Loraine H, Hagan D, Whaley JM, Feder JN. Quantitative PCR tissue expression profiling of the human SGLT2 gene and related family members. Diabetes Ther 2010;1:57-92. doi: 10.1007/s13300-010-0006-4Search in Google Scholar

26. Kashiwagi Y, Nagoshi T, Yoshino T, Tanaka TD, Ito K, Harada T, Takahashi H, Ikegami M, Anzawa R, Yoshimura M. Expression of SGLT1 in human hearts and impairment of cardiac glucose uptake by phlorizin during ischemiareperfusion injury in mice. PloS One 2015;10:e0130605. doi: 10.1371/journal.pone.0130605Search in Google Scholar

27. Sharma P, Khairnar V, Vrhovac Madunić I, Singh Y, Pandyra A, Salker MS, Koepsell H, Sabolić I, Lang F, Lang PA, Lang KS. SGLT1 Deficiency turns Listeria infection into a lethal disease in mice. Cell Physiol Biochem 2017:1358-65. doi: 10.1159/000479197Search in Google Scholar

28. Kepe V, Scafoglio C, Liu J, Yong WH, Bergsneider M, Huang SC, Barrio JR, Wright EM. Positron emission tomography of sodium glucose cotransport activity in high grade astrocytomas. J Neuro-Oncol 2018:138:557-69. doi: 10.1007/s11060-018-2823-7Search in Google Scholar

29. Scafoglio C, Hirayama BA, Kepe V, Liu J, Ghezzi C, Satyamurthy N, Moatamed NA, Huang J, Koepsell H, Barrio JR, Wright EM. Functional expression of sodium-glucose transporters in cancer. P Natl Acad Sci USA 2015;112:E4111-9. doi: 10.1073/pnas.1511698112Search in Google Scholar

30. Ishikawa N, Oguri T, Isobe T, Fujitaka K, Kohno N. SGLT gene expression in primary lung cancers and their metastatic lesions. Jpn J Cancer Res 2001;92:874-9. doi: 10.1111/j.1349-7006.2001.tb01175.xSearch in Google Scholar

31. Guo GF, Cai YC, Zhang B, Xu RH, Qiu HJ, Xia LP, Jiang WQ, Hu PL, Chen XX, Zhou FF, Wang F. Overexpression of SGLT1 and EGFR in colorectal cancer showing a correlation with the prognosis. Med Oncol 2011;28(Suppl 1):S197-203. doi: 10.1007/s12032-010-9696-8Search in Google Scholar

32. Blais A. Expression of Na(+)-coupled sugar transport in HT-29 cells: modulation by glucose. Am J Physiol-Cell Ph 1991;260:C1245-52. doi: 10.1152/ajpcell.1991.260.6.C1245Search in Google Scholar

33. Delezay O, Verrier B, Mabrouk K, van Rietschoten J, Fantini J, Mauchamp J, Gerard C. Characterization of an electrogenic sodium/glucose cotransporter in a human colon epithelial cell line. J Cell Physiol 1995;163:120-8. doi: 10.1002/jcp.1041630114Search in Google Scholar

34. Bissonnette P, Gagne H, Coady MJ, Benabdallah K, Lapointe JY, Berteloot A. Kinetic separation and characterization of three sugar transport modes in Caco-2 cells. Am J Physiol 1996;270:G833-43. doi: 10.1152/ajpgi.1996.270.5.G833Search in Google Scholar

35. Weihua Z, Tsan R, Huang WC, Wu Q, Chiu CH, Fidler IJ, Hung MC. Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer Cell 2008;13:385-93. doi: 10.1016/j.ccr.2008.03.01518455122Search in Google Scholar

36. Casneuf VF, Fonteyne P, Van Damme N, Demetter P, Pauwels P, de Hemptinne B, De Vos M, Van de Wiele C, Peeters M. Expression of SGLT1, Bcl-2 and p53 in primary pancreatic cancer related to survival. Cancer Invest 2008;26:852-9. doi: 10.1080/07357900801956363Search in Google Scholar

37. Hanabata Y, Nakajima Y, Morita K, Kayamori K, Omura K. Coexpression of SGLT1 and EGFR is associated with tumor differentiation in oral squamous cell carcinoma. Odontology 2012;100:156-63. doi: 10.1007/s10266-011-0033-2Search in Google Scholar

38. Helmke BM, Reisser C, Idzkoe M, Dyckhoff G, Herold- Mende C. Expression of SGLT-1 in preneoplastic and neoplastic lesions of the head and neck. Oral Oncol 2004;40:28-35. doi: 10.1016/S1368-8375(03)00129-5Search in Google Scholar

39. Blessing A, Xu L, Gao G, Bollu LR, Ren J, Li H, Wu X, Su F, Huang W-C, Hung M-C, Huo L, Palapattu GS, Weihua Z. Sodium/glucose co-transporter 1 expression increases in human diseased prostate. J Cancer Sci Ther 2012;4:306-12. doi: 10.4172/1948-5956.1000159Search in Google Scholar

40. Lin H-W, Tseng C-H. A Review on the relationship between SGLT2 inhibitors and cancer. Int J Endocrinol 2014;2014:719578. doi: 10.1155/2014/719578Search in Google Scholar

41. Hummel CS, Lu C, Liu J, Ghezzi C, Hirayama BA, Loo DDF, Kepe V, Barrio JR, Wright EM. Structural selectivity of human SGLT inhibitors. Am J Physiol-Cell Ph 2012;302:C373-82. doi: 10.1152/ajpcell.00328.2011Search in Google Scholar

42. Vallon V. The mechanisms and therapeutic potential of SGLT2 inhibitors in diabetes mellitus. Annu Rev Med 2015;66:255-70. doi: 10.1146/annurev-med-051013-110046Search in Google Scholar

43. Balen D, Ljubojević M, Breljak D, Brzica H, Žlender V, Koepsell H, Sabolić I. Revised immunolocalization of the Na+-D-glucose cotransporter SGLT1 in rat organs with an improved antibody. Am J Physiol-Cell Ph 2008;295:C475-89. doi: 10.1152/ajpcell.00180.2008Search in Google Scholar

44. World Health Organization (WHO). [displayed 22 November 2018]. Available at: http://www.who.int/en/news-room/factsheets/detail/cancerSearch in Google Scholar

45. RS B, Leung J, Kison P, Zasadny K, Flint A, Wahl R. Glucose transporters and FDG uptake in untreated primary human non-small cell lung cancer. J Nucl Med 1999;40:556-65. PMID: 1021021310210213Search in Google Scholar

46. Kurata T, Oguri T, Isobe T. Differential expression of facilitative glucose transporter (GLUT) genes in primary lung cancers and their liver metastases. Jpn J Cancer Res 1999;90:1238-43. doi: 10.1111/j.1349-7006.1999.tb00702.x10622535Search in Google Scholar

47. Yu M, Yongzhi H, Chen S, Luo X, Lin Y, Zhou Y, Jin H, Hou B, Deng Y, Tu L, Jian Z. The prognostic value of GLUT1 in cancers: a systematic review and meta-analysis. Oncotarget 2015;8:43356-67. doi: 10.18632/oncotarget.17445Search in Google Scholar

48. Kamisawa T, Wood LD, Itoi T, Takaori K. Pancreatic cancer. Lancet 2016;388:73-85. doi: 10.1016/S0140-6736(16)00141-0Search in Google Scholar

49. Ozaki T, Nakagawara A. Role of p53 in cell death and human cancers. Cancers 2011;3:994-1013. doi: 10.3390/cancers3010994Search in Google Scholar

50. Ghezzi C, Wright EM. Regulation of the human Na+- dependent glucose cotransporter hSGLT2. Am J Physiol-Cell Ph 2012;303:C348-54. doi: 10.1152/ajpcell.00115.2012Search in Google Scholar

51. Siegel RL, Miller KD, Jemal A. Cancer Statistics. CA Cancer J Clin 2017;67:7-30. doi: 10.3322/caac.21387Search in Google Scholar

52. Vaz CV, Marques R, Alves MG, Oliveira PF, Cavaco JE, Maia CJ, Socorro S. Androgens enhance the glycolytic metabolism and lactate export in prostate cancer cells by modulating the expression of GLUT1, GLUT3, PFK, LDH and MCT4 genes. J Cancer Res Clin Oncol 2016;142:5-16. doi: 10.1007/s00432-015-1992-4Search in Google Scholar

53. Lai B, Xiao Y, Pu H, Cao Q, Jing H, Liu X. Overexpression of SGLT1 is correlated with tumor development and poor prognosis of ovarian carcinoma. Arch Gynecol Obstet 2012;285:1455-61. doi: 10.1007/s00404-011-2166-5Search in Google Scholar

54. Salker MS, Singh Y, Zeng N, Chen H, Zhang S, Umbach AT, Fakhri H, Kohlhofer U, Quintanilla-Martinez L, Durairaj RRP, Barros FSV, Vrljicak P, Ott S, Brucker SY, Wallwiener D, Vrhovac Madunić I, Breljak D, Sabolić I, Koepsell H, Bronsen JJ, Lang F. Loss of endometrial sodium glucose cotransporter SGLT1 is detrimental to embryo survival and fetal growth in pregnancy. Sci Rep 2017;7:12612. doi: 10.1038/s41598-017-11674-3Search in Google Scholar

55. Yu AS, Hirayama BA, Timbol G, Liu J, Basarah E, Kepe V, Satyamurthy N, Huang S, Wright EM, Barrio JR. Functional expression of SGLTs in rat brain. Am J Physiol-Cell Ph 2010;1751:C1277-84. doi: 10.1152/ajpcell.00296.2010Search in Google Scholar

56. Yu AS, Hirayama BA, Timbol G, Liu J, Diez-Sampedro A, Kepe V, Satyamurthy N, Huang S-C, Wright EM, Barrio JR. Regional distribution of SGLT activity in rat brain in vivo. Am J Physiol-Cell Ph 2013;304:C240-7. doi: 10.1152/ajpcell.00317.2012Search in Google Scholar

57. Madunić J, Vrhovac Madunić I, Gajski G, Popić J, Garaj- Vrhovac V. Apigenin: A dietary flavonoid with diverse anticancer properties. Cancer Lett 2018;413:11-22. doi: 10.1016/j.canlet.2017.10.041Search in Google Scholar

58. Koepsell H. The Na+ -D-glucose cotransporters SGLT1 and SGLT2 are targets for the treatment of diabetes and cancer. Pharmacol Ther 2017;170:148-65. doi:10.1016/j.pharmthera.2016.10.017Search in Google Scholar

59. Yamazaki Y, Harada S, Tokuyama S. Sodium-glucose transporter as a novel therapeutic target in disease. Eur J of Pharmacol 2018;822:25-31. doi: 10.1016/j.ejphar.2018.01.003.Search in Google Scholar