Hypoxia induced upregulation and function of the thiamine transporter, SLC19A3 in a breast cancer cell line

Cancer Biology and Therapy

Volumn 10, Issue 11, 2010, Pages 1101-1111

  Sweet, Rebecca ^a   Paul, Amber ^a   Zastre, Jason ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Breast cancer; HIF; Hypoxia; Microenvironment; Transporter

Indexed keywords

CARRIER PROTEIN; DEFEROXAMINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; PROTEIN SLC19A2; PROTEIN SLC19A3; THIAMINE; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HYPOXIA; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

BIOLOGICAL TRANSPORT; BREAST NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION PROFILING; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MEMBRANE TRANSPORT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 78649859188     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.10.11.13444     Document Type: Article

References (59)

1. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply and metabolic microenvironment of human tumors: A review. Cancer Res 1989; 49:6449-65.
2. Vaupel P, Mayer A, Briest S, Hockel M. Hypoxia in breast cancer: role of blood flow, oxygen diffusion distances and anemia in the development of oxygen depletion. Adv Exp Med Biol 2005; 566:333-42.
3. Harris AL. Hypoxia - a key regulatory factor in tumor growth. Nat Rev Cancer 2002; 2:38-47.
4. Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 2006; 70:1469-80.
5. Gruber G, Greiner RH, Hlushchuk R, Aebersold DM, Altermatt HJ, Berclaz G, et al. Hypoxia-inducible factor 1alpha in high-risk breast cancer: an independent prognostic parameter? Breast Cancer Res 2004; 6:191-8.
6. Generali D, Berruti A, Brizzi MP, Campo L, Bonardi S, Wigfield S, et al. Hypoxia-inducible factor-1alpha expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin Cancer Res 2006; 12:4562-8. (Pubitemid 44297805)
7. Moeller BJ, Dewhirst MW. HIF-1 and tumour radiosensitivity. Br J Cancer 2006; 95:1-5.
8. Liao D, Corle C, Seagroves TN, Johnson RS. Hypoxia-inducible factor-1alpha is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res 2007; 67:563-72. (Pubitemid 46192193)
9. Dales JP, Garcia S, Meunier-Carpentier S, Andrac-Meyer L, Haddad O, Lavaut MN, et al. Overexpression of hypoxia-inducible factor HIF-1alpha predicts early relapse in breast cancer: Retrospective study in a series of 745 patients. Int J Cancer 2005; 116:734-9. (Pubitemid 41099705)
10. Schindl M, Schoppmann SF, Samonigg H, Hausmaninger H, Kwasny W, Gnant M, et al. Overexpression of hypoxia-inducible factor 1alpha is associated with an unfavorable prognosis in lymph node-positive breast cancer. Clin Cancer Res 2002; 8:1831-7.
11. Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 2003; 55:3-29.
12. Huang Y, Anderle P, Bussey KJ, Barbacioru C, Shankavaram U, Dai Z, et al. Membrane Transporters and Channels: Role of the Transportome in Cancer Chemosensitivity and Chemoresistance. Cancer Res 2004; 64:4294-301. (Pubitemid 38802436)
13. He L, Vasiliou K, Nebert DW. Analysis and update of the human solute carrier (SLC) gene superfamily. Hum Genomics 2009; 3:195-206.
14. Gupta N, Prasad PD, Ghamande S, Moore-Martin P, Herdman AV, Martindale RG, et al. Upregulation of the amino acid transporter ATB0, +(SLC6A14) in carcinoma of the cervix. Gynecol Oncol 2006; 100:8-13.
15. Wlcek K, Svoboda M, Thalhammer T, Sellner F, Krupitza G, Jaeger W. Altered expression of organic anion transporter polypeptide (OATP) genes in human breast carcinoma. Cancer Biol Ther 2008; 7:1450-5.
16. Whitman SP, Hackanson B, Liyanarachchi S, Liu S, Rush LJ, Maharry K, et al. DNA hypermethylation and epigenetic silencing of the tumor suppressor gene, SLC5A8, in acute myeloid leukemia with the MLL partial tandem duplication. Blood 2008; 112:2013-6.
17. Kaira K, Oriuchi N, Imai H, Shimizu K, Yanagitani N, Sunaga N, et al. Prognostic significance of L-type amino acid transporter 1 expression in resectable stage I-III nonsmall cell lung cancer. Br J Cancer 2008; 98:742-8. (Pubitemid 351272621)
18. Lee W, Belkhiri A, Lockhart AC, Merchant N, Glaeser H, Harris EI, et al. Overexpression of OATP1B3 confers apoptotic resistance in colon cancer. Cancer Res 2008; 68:10315-23.
19. Thangaraju M, Gopal E, Martin PM, Ananth S, Smith SB, Prasad PD, et al. SLC5A8 Triggers Tumor Cell Apoptosis through Pyruvate-Dependent Inhibition of Histone Deacetylases. Cancer Res 2006; 66:11560-4.
20. Santini D, Vincenzi B, Fratto ME, Perrone G, Lai R, Catalano V, et al. Prognostic role of human equilibrative transporter 1 (hENT1) in patients with resected gastric cancer. J Cell Physiol 2010; 223:384-8.
21. Muto M, Onogawa T, Suzuki T, Ishida T, Rikiyama T, Katayose Y, et al. Human liver-specific organic anion transporter-2 is a potent prognostic factor for human breast carcinoma. Cancer Sci 2007; 98:1570-6.
22. Gupta N, Martin PM, Prasad PD, Ganapathy V. SLC5A8 (SMCT1)-mediated transport of butyrate forms the basis for the tumor suppressive function of the transporter. Life Sci 2006; 78:2419-25.
23. Lockhart AC, Harris E, LaFleur BJ, Merchant NB, Washington MK, Resnick MB, et al. Organic anion transporting polypeptide IB3 (OATPIB3) is overexpressed in colorectal tumors and is a predictor of clinical outcome. Clin Exp Gastroenterol 2008; 1:1-7.
24. Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A. Regulation of glut1 mRNA by hypoxia-inducible factor- 1: interaction between H-ras and hypoxia. J Biol Chem 2001; 276:9519-25.
25. Macheda ML, Rogers S, Best JD. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 2004; 202:654-62.
26. Ullah MS, Davies AJ, Halestrap AP. The Plasma Membrane Lactate Transporter MCT4, but Not MCT1, Is Upregulated by Hypoxia through a HIF-1alpha-dependent Mechanism. J Biol Chem 2006; 281:9030-7.
27. Casanello P, Torres A, Sanhueza F, Gonzalez M, Farias M, Gallardo V, et al. Equilibrative nucleoside transporter 1 expression is downregulated by hypoxia in human umbilical vein endothelium. Circ Res 2005; 97:16-24.
28. Eltzschig HK, Abdulla P, Hoffman E, Hamilton KE, Daniels D, Schoenfeld C, et al. HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J Exp Med 2005; 202:1493-505.
29. Chaudary N, Naydenova Z, Shuralyova I, Coe IR. Hypoxia regulates the adenosine transporter, mENT1, in the murine cardiomyocyte cell line, HL-1. Cardiovasc Res 2004; 61:780-8.
30. Warburg O. On the origin of cancer cells. Science 1956; 123:309-14.
31. Isidoro A, Casado E, Redondo A, Acebo P, Espinosa E, Alonso AM, et al. Breast carcinomas fulfill the Warburg hypothesis and provide metabolic markers of cancer prognosis. Carcinogenesis 2005; 26:2095-104.
32. Schmidt M, Voelker HU, Kapp M, Krockenberger M, Dietl J, Kammerer U. Glycolytic phenotype in breast cancer: activation of Akt, upregulation of GLUT1, TKTL1 and downregulation of M2PK. J Cancer Res Clin Oncol 2010; 136:219-25.
33. Kim J, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006; 3:177-85.
34. Lacroix M, Leclercq G. Relevance of Breast Cancer Cell Lines as Models for Breast Tumours: An Update. Breast Cancer Res Treat 2004; 83:249-89.
35. Oguri T, Achiwa H, Muramatsu H, Ozasa H, Sato S, Shimizu S, et al. The absence of human equilibrative nucleoside transporter 1 expression predicts nonresponse to gemcitabine-containing chemotherapy in non-small cell lung cancer. Cancer Lett 2007; 256:112-9.
36. Holzer AK, Samimi G, Katano K, Naerdemann W, Lin X, Safaei R, et al. The copper influx transporter human copper transport protein 1 regulates the uptake of cisplatin in human ovarian carcinoma cells. Mol Pharmacol 2004; 66:817-23.
37. Worm J, Kirkin AF, Dzhandzhugazyan KN, Guldberg P. Methylation-dependent silencing of the reduced folate carrier gene in inherently methotrexate- resistant human breast cancer cells. J Biol Chem 2001; 276:39990-40000.
38. Ganapathy V, Smith SB, Prasad PD. SLC19: the folate/ thiamine transporter family. Pfluegers Arch 2004; 447:641-6.
39. Dutta B, Huang W, Molero M, Kekuda R, Leibach FH, Devoe LD, et al. Cloning of the human thiamine transporter, a member of the folate transporter family. J Biol Chem 1999; 274:31925-9.
40. Said HM, Balamurugan K, Subramanian VS, Marchant JS. Expression and functional contribution of hTHTR-2 in thiamin absorption in human intestine. Am J Physiol 2004; 286:491-8.
41. Yuan Y, Hilliard G, Ferguson T, Millhorn DE. Cobalt Inhibits the Interaction between Hypoxia-inducible Factor-alpha and von Hippel-Lindau Protein by Direct Binding to Hypoxia-inducible Factor-alpha. J Biol Chem 2003; 278:15911-6.
42. Liu S, Huang H, Lu X, Golinski M, Comesse S, Watt D, et al. Downregulation of thiamine transporter THTR2 gene expression in breast cancer and is association with resistance to apoptosis. Mol Cancer Res 2003; 1:665-73.
43. Liu X, Lam EKY, Wang X, Zhang JB, Cheng YY, Lam YW, et al. Promoter Hypermethylation Mediates Downregulation of Thiamine Receptor SLC19A3 in Gastric Cancer. Tumor Biol 2009; 30:242-8.
44. Boros LG, Lee PWN, Brandes JL, Cascante M, Muscarella P, Schirmer WJ, et al. Nonoxidative pentose phosphate pathways and their direct role in ribose synthesis in tumors: is cancer a disease of cellular glucose metabolism? Med Hypotheses 1998; 50:55-9.
45. Foeldi 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; 17:841-5.
46. Langbein S, Zerilli M, zur Hausen A, Staiger W, Rensch-Boschert K, Lukan N, et al. Expression of transketolase TKTL1 predicts colon and urothelial cancer patient survival: Warburg effect reinterpreted. Br J Cancer 2006; 94:578-85.
47. Schultz H, Kaehler D, Branscheid D, Vollmer E, Zabel P, Goldmann T. TKTL1 is overexpressed in a large portion of non-small cell lung cancer specimens. Diagn Pathol 2008; 3:35.
48. Boros LG, Puigjaner J, Cascante M, Lee WNP, Brandes JL, Bassilian S, et al. Oxythiamine and dehydroepiandrosterone inhibit the nonoxidative synthesis of ribose and tumor cell proliferation. Cancer Res 1997; 57:4242-8.
49. Hu LH, Yang JH, Zhang DT, Zhang S, Wang L, Cai PC, et al. The TKTL1 gene influences total transketolase activity and cell proliferation in human colon cancer LoVo cells. Anticancer Drugs 2007; 18:427-33.
50. Xu X, zur Hausen A, Coy JF, Lochelt M. Transketolase-like protein 1 (TKTL1) is required for rapid cell growth and full viability of human tumor cells. Int J Cancer 2009; 124:1330-7.
51. Comin-Anduix B, Boren J, Martinez S, Moro C, Centelles JJ, Trebukhina R, et al. The effect of thiamine supplementation on tumour proliferation. A metabolic control analysis study. Eur J Biochem 2001; 268:4177-82. (Pubitemid 32862878)
52. Boros LG, Brandes JL, Lee WNP, Cascante M, Puigjaner J, Revesz E, et al. Thiamine supplementation to cancer patients: a double-edged sword. Anticancer Res 1998; 18:595-602. (Pubitemid 28174878)
53. Basu TK, Dickerson JWT. The thiamin status of early cancer patients with particular reference to those with breast and bronchial carcinomas. Oncology 1976; 33:250-2.
54. Ashokkumar B, Vaziri ND, Said HM. Thiamin uptake by the human-derived renal epithelial (HEK-293) cells: cellular and molecular mechanisms. Am J Physiol 2006; 291:796-805.
55. Nabokina SM, Said HM. Characterization of the 5′-regulatory region of the human thiamin transporter SLC19A3: In vitro and in vivo studies. Am J Physiol 2004; 287:822-9.
56. Discher DJ, Bishopric NH, Wu X, Peterson CA, Webster KA. Hypoxia regulates beta-enolase and pyruvate kinase-M promoters by modulating Sp1/Sp3 binding to a conserved GC element. J Biol Chem 1998; 273:26087-93. (Pubitemid 28475843)
57. Szalad A, Katakowski M, Zheng X, Jiang F, Chopp M. Transcription factor Sp1 induces ADAM17 and contributes to tumor cell invasiveness under hypoxia. J Exp Clin Cancer Res 2009; 28:129.
58. Xu Q, Ji YS, Schmedtje JFJ. Sp1 increases expression of cyclooxygenase-2 in hypoxic vascular endothelium. Implications for the mechanisms of aortic aneurysm and heart failure. J Biol Chem 2000; 275:24583-9.
59. Shahrzad S, Bertrand K, Minhas K, Coomber BL. Induction of DNA hypomethylation by tumor hypoxia. Epigenetics 2007; 2:119-25. (Pubitemid 351682006)