Hexokinase and phosphofructokinase activity and intracellular distribution correlate with aggressiveness and invasiveness of human breast carcinoma

Oncotarget

Volumn 6, Issue 30, 2015, Pages 29375-29387

  Coelho, Raquel G ^a   Calaça, Isadora C ^a   Celestrini, Deborah M ^a   Correia Carneiro, Ana Helena P ^a   Costa, Mauricio M ^a   Zancan, Patricia ^a   Sola Penna, Mauro ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Breast cancer; Diagnosis; Glycolysis; Prognosis; Treatment

Indexed keywords

6 PHOSPHOFRUCTOKINASE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; HEXOKINASE; KI 67 ANTIGEN; LACTIC ACID; PROGESTERONE RECEPTOR; PROTEIN P53; ERBB2 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; ARTICLE; AXILLARY LYMPH NODE; BREAST CARCINOMA; CANCER AGGRESSIVENESS; CANCER PROGNOSIS; CANCER STAGING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORRELATIONAL STUDY; ENZYME ACTIVITY; FEMALE; GLUCOSE INTAKE; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHADENOPATHY; MAJOR CLINICAL STUDY; ONCOGENESIS AND MALIGNANT TRANSFORMATION; SKIN METASTASIS; TUMOR INVASION; TUMOR VOLUME; AGED; BREAST NEOPLASMS; CARCINOMA; CELL MOTION; ENZYMOLOGY; GLYCOLYSIS; LYMPH NODE METASTASIS; MASTECTOMY; MIDDLE AGED; PATHOLOGY; SIGNAL TRANSDUCTION;

AGED; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CARCINOMA; CELL MOVEMENT; FEMALE; GLYCOLYSIS; HEXOKINASE; HUMANS; KI-67 ANTIGEN; LYMPHATIC METASTASIS; MASTECTOMY; MIDDLE AGED; NEOPLASM INVASIVENESS; PHOSPHOFRUCTOKINASES; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; TUMOR BURDEN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84945144220     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4910     Document Type: Article

References (70)

1. Pelicano H, Zhang W, Liu J, Hammoudi N, Dai J, Xu RH, Pusztai L, Huang P. Mitochondrial dysfunction in some triple-negative breast cancer cell lines: role of mTOR pathway and therapeutic potential. Breast cancer research. 2014; 16:434.
2. Son SH, Kim DH, Hong CM, Kim CY, Jeong SY, Lee SW, Lee J, Ahn BC. Prognostic implication of intratumoral metabolic heterogeneity in invasive ductal carcinoma of the breast. BMC cancer. 2014; 14:585.
3. Kim SK, Jung WH, Koo JS. Differential expression of enzymes associated with serine/glycine metabolism in different breast cancer subtypes. PLoS One. 2014; 9:e101004.
4. Di Leo A, Curigliano G, Dieras V, Malorni L, Sotiriou C, Swanton C, Thompson A, Tutt A, Piccart M. New approaches for improving outcomes in breast cancer in Europe. Breast. 2015; 24:321-330.
5. Balogun OD, Formenti SC. Locally advanced breast cancer-strategies for developing nations. Frontiers in oncology. 2015; 5:89.
6. Tavassoli FA, Devilee P International Agency for Research on Cancer. and World Health Organization. 2003 Pathology and genetics of tumours of the breast and female genital organs. (Lyon: IARC Press).
7. Guth U, Singer G, Schotzau A, Langer I, Dieterich H, Rochlitz C, Herberich L, Holzgreve W, Wight E. Scope and significance of non-uniform classification practices in breast cancer with non-inflammatory skin involvement: a clinicopathologic study and an international survey. Annals of oncology: official journal of the European Society for Medical Oncology /ESMO. 2005; 16:1618-1623.
8. Ferreira AR, Saini KS, Metzger-Filho O. Treatment of early-stage HER2+ breast cancer-an evolving field. Ecancermedicalscience. 2015; 9:523.
9. Zardavas D, Irrthum A, Swanton C, Piccart M. Clinical management of breast cancer heterogeneity. Nature reviews Clinical oncology. 2015; 12:381-394.
10. Qiu SQ, Wei XL, Huang WH, Wu MY, Qin YS, Li YK, Zhang GJ. Diagnostic and therapeutic strategy and the most efficient prognostic factors of breast malignant fibrous histiocytoma. Scientific reports. 2013; 3:2529.
11. Mustacchi G, Biganzoli L, Pronzato P, Montemurro F, Dambrosio M, Minelli M, Molteni L, Scaltriti L. HER2-positive metastatic breast cancer: A changing scenario. Critical reviews in oncology/hematology. 2015; 95:78-87.
12. Oostra DR, Macrae ER. Role of trastuzumab emtansine in the treatment of HER2-positive breast cancer. Breast cancer. 2014; 6:103-113.
13. Nazarali SA, Narod SA. Tamoxifen for women at high risk of breast cancer. Breast cancer. 2014; 6:29-36.
14. Morad SA, Cabot MC. Tamoxifen regulation of sphingolipid metabolism-therapeutic implications. Biochim Biophys Acta. 2015; 185:1134-1145.
15. Duffy MJ, Synnott NC, McGowan PM, Crown J, O'Connor D, Gallagher WM. p53 as a target for the treatment of cancer. Cancer treatment reviews. 2014; 40:1153-1160.
16. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
17. Nikitovic D, Tzardi M, Berdiaki A, Tsatsakis A, Tzanakakis GN. Cancer microenvironment and inflammation: role of hyaluronan. Frontiers in immunology. 2015; 6:169.
18. Hsu PP, Sabatini DM. Cancer Cell Metabolism: Warburg and Beyond. Cell. 2008; 134:703-707.
19. Bayley JP, Devilee P. The Warburg effect in 2012. Current opinion in oncology. 2012; 24:62-67.
20. Kim JW, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 2006; 66:8927-8930.
21. Robey IF, Stephen RM, Brown KS, Baggett BK, Gatenby RA, Gillies RJ. Regulation of the Warburg effect in early-passage breast cancer cells. Neoplasia. 2008; 10:745-756.
22. Gillies RJ, Robey I, Gatenby RA. Causes and consequences of increased glucose metabolism of cancers. J Nucl Med. 2008; 49:24S-42S.
23. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis?. NatRevCancer. 2004; 4:891-899.
24. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009; 324:1029-1033.
25. Pedersen PL. Warburg, me and Hexokinase 2: Multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the "Warburg Effect", i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr. 2007; 39:211-222.
26. Zancan P, Almeida FV, Faber-Barata J, Dellias JM, Sola-Penna M. Fructose-2,6-bisphosphate counteracts guanidinium chloride-, thermal-, and ATP-induced dissociation of skeletal muscle key glycolytic enzyme 6-phosphofructo-1-kinase: A structural mechanism for PFK allosteric regulation. ArchBiochemBiophys. 2007; 467:275-282.
27. Zancan P, Marinho-Carvalho MM, Faber-Barata J, Dellias JM, Sola-Penna M. ATP and fructose-2,6-bisphosphate regulate skeletal muscle 6-phosphofructo-1-kinase by altering its quaternary structure. IUBMBLife. 2008; 60:526-533.
28. Sola-Penna M, Da Silva D, Coelho WS, MarinhoCarvalho MM, Zancan P. Regulation of mammalian muscle type 6-phosphofructo-1-kinase and its implication for the control of the metabolism. IUBMB Life. 2010; 62:791-796.
29. Guzun R, Gonzalez-Granillo M, Karu-Varikmaa M, Grichine A, Usson Y, Kaambre T, Guerrero-Roesch K, Kuznetsov A, Schlattner U, Saks V. Regulation of respiration in muscle cells in vivo by VDAC through interaction with the cytoskeleton and MtCK within Mitochondrial Interactosome. Biochim Biophys Acta. 2012; 1818:1545-1554.
30. Furtado CM, Marcondes MC, Sola-Penna M, de Souza ML, Zancan P. Clotrimazole preferentially inhibits human breast cancer cell proliferation, viability and glycolysis. PLoS ONE. 2012; 7:e30462.
31. Coelho RG, Calaça IdC, Celestrini DdM, Correia AH, Costa MASM, Sola-Penna M. Clotrimazole disrupts glycolysis in human breast cancer without affecting non-tumoral tissues. Molecular Genetics and Metabolism. 2011; 103:394-398.
32. Zancan P, Sola-Penna M, Furtado CM, Da Silva D. Differential expression of phosphofructokinase-1 isoforms correlates with the glycolytic efficiency of breast cancer cells. Mol Genet Metab. 2010; 100:372-378.
33. Zancan P, Rosas AO, Marcondes MC, Marinho-Carvalho MM, Sola-Penna M. Clotrimazole inhibits and modulates heterologous association of the key glycolytic enzyme 6-phosphofructo-1-kinase. BiochemPharmacol. 2007; 73:1520-1527.
34. Meira DD, Marinho-Carvalho MM, Teixeira CA, Veiga VF, Da Poian AT, Holandino C, de Freitas MS, Sola-Penna M. Clotrimazole decreases human breast cancer cells viability through alterations in cytoskeleton-associated glycolytic enzymes. MolGenetMetab. 2005; 84:354-362.
35. El-Bacha T, de Freitas MS, Sola-Penna M. Cellular distribution of phosphofructokinase activity and implications to metabolic regulation in human breast cancer. MolGenetMetab. 2003; 79:294-299.
36. Penso J, Beitner R. Lithium detaches hexokinase from mitochondria and inhibits proliferation of B16 melanoma cells. MolGenetMetab. 2003; 78:74-78.
37. Penso J, Beitner R. Detachment of glycolytic enzymes from cytoskeleton of Lewis lung carcinoma and colon adenocarcinoma cells induced by clotrimazole and its correlation to cell viability and morphology. MolGenetMetab. 2002; 76:181-188.
38. Schwartz D, Beitner R. Detachment of the glycolytic enzymes, phosphofructokinase and aldolase, from cytoskeleton of melanoma cells, induced by local anesthetics. MolGenetMetab. 2000; 69:159-164.
39. Vertessy BG, Orosz F, Kovacs J, Ovadi J. Alternative binding of two sequential glycolytic enzymes to microtubules. Molecular studies in the phosphofructokinase/aldolase/microtubule system. J Biol Chem. 1997; 272:25542-25546.
40. Orosz F, Vertessy BG, Salerno C, Crifo C, Capuozzo E, Ovadi J. The interaction of a new anti-tumour drug, KAR-2 with calmodulin. BrJPharmacol. 1997; 121:955-962.
41. Marin-Hernandez A, Gallardo-Perez JC, Rodriguez-EnrÌquez S, Encalada R, Moreno-Sanchez R, Saavedra E. Modeling cancer glycolysis. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2011;. DOI: 10.1016/j.bbabio.2010.11.006.
42. Alves GG, Sola-Penna M. Epinephrine modulates cellular distribution of muscle phosphofructokinase. MolGenetMetab. 2003; 78:302-306.
43. Coelho WS, Costa KC, Sola-Penna M. Serotonin stimulates mouse skeletal muscle 6-phosphofructo-1-kinase through tyrosine-phosphorylation of the enzyme altering its intracellular localization. MolGenetMetab. 2007; 92:364-370.
44. Coelho WS, Da Silva D, Marinho-Carvalho MM, SolaPenna M. Serotonin modulates hepatic 6-phosphofructo-1-kinase in an insulin synergistic manner. Int J Biochem Cell Biol. 2012; 44:150-157.
45. Coelho WS, Sola-Penna M. Serotonin regulates 6-phosphofructo-1-kinase activity in a PLC-PKC-CaMK II-and Janus kinase-dependent signaling pathway. Mol Cell Biochem. 2013; 372:211-220.
46. Da Silva D, Ausina P, Alencar EM, Coelho WS, Zancan P, Sola-Penna M. Metformin reverses hexokinase and phosphofructokinase downregulation and intracellular distribution in the heart of diabetic mice. IUBMB Life. 2012; 64:766-774.
47. Da Silva D, Zancan P, Coelho WS, Gomez LS, Sola-Penna M. Metformin reverses hexokinase and 6-phosphofructo-1-kinase inhibition in skeletal muscle, liver and adipose tissues from streptozotocin-induced diabetic mouse. Arch Biochem Biophys. 2010; 496:53-60.
48. Gomez LS, Zancan P, Marcondes MC, Ramos-Santos L, Meyer-Fernandes JR, Sola-Penna M, Da Silva D. Resveratrol decreases breast cancer cell viability and glucose metabolism by inhibiting 6-phosphofructo-1-kinase. Biochimie. 2013; 95:1336-1343.
49. Grechi J, Marinho-Carvalho M, Zancan P, Cinelli LP, Gomes AMO, Rodrigues ML, Nimrichter L, Sola-Penna M. Glucuronoxylomannan from Cryptococcus neoformans Down-regulates the Enzyme 6-Phosphofructo-1-kinase of Macrophages. Journal of Biological Chemistry. 2011; 286:14820-14829.
50. Leite TC, Coelho RG, Silva DD, Coelho WS, MarinhoCarvalho MM, Sola-Penna M. Lactate downregulates the glycolytic enzymes hexokinase and phosphofructokinase in diverse tissues from mice. FEBS Letters. 2011; 585:92-98.
51. Leite TC, Da Silva D, Coelho RG, Zancan P, Sola-Penna M. Lactate favours the dissociation of skeletal muscle 6-phosphofructo-1-kinase tetramers down-regulating the enzyme and muscle glycolysis. BiochemJ. 2007; 408:123-130.
52. Marinho-Carvalho MM, Costa-Mattos PV, Spitz GA, Zancan P, Sola-Penna M. Calmodulin upregulates skeletal muscle 6-phosphofructo-1-kinase reversing the inhibitory effects of allosteric modulators. Biochimica et Biophysica Acta (BBA)-Proteins & Proteomics. 2009; 1794:1175-1180.
53. Real-Hohn A, Zancan P, Da Silva D, Martins ER, Salgado LT, Mermelstein CS, Gomes AM, Sola-Penna M. Filamentous actin and its associated binding proteins are the stimulatory site for 6-phosphofructo-1-kinase association within the membrane of human erythrocytes. Biochimie. 2010; 92:538-544.
54. Spitz GA, Furtado CM, Sola-Penna M, Zancan P. Acetylsalicylic acid and salicylic acid decrease tumor cell viability and glucose metabolism modulating 6-phosphofructo-1-kinase structure and activity. Biochemical Pharmacology. 2009; 77:46-53.
55. Lu CL, Qin L, Liu HC, Candas D, Fan M, Li JJ. Tumor cells switch to mitochondrial oxidative phosphorylation under radiation via mTOR-mediated hexokinase II inhibition-a Warburg-reversing effect. PLoS One. 2015; 10:e0121046.
56. Dai W, Wang F, Lu J, Xia Y, He L, Chen K, Li J, Li S, Liu T, Zheng Y, Wang J, Lu W, Zhou Y, Yin Q, Abudumijiti H, Chen R, et al. By reducing hexokinase 2, resveratrol induces apoptosis in HCC cells addicted to aerobic glycolysis and inhibits tumor growth in mice. Oncotarget. 2015.
57. Xian SL, Cao W, Zhang XD, Lu YF. 3-Bromopyruvate inhibits human gastric cancer tumor growth in nude mice via the inhibition of glycolysis. Oncology letters. 2015; 9:739-744.
58. Justus CR, Sanderlin EJ, Yang LV. Molecular Connections between Cancer Cell Metabolism and the Tumor Microenvironment. Int J Mol Sci. 2015; 16:11055-11086.
59. Engel C, Fischer C. Breast cancer risks and risk prediction models. Breast care. 2015; 10:7-12.
60. Abramson VG, Lehmann BD, Ballinger TJ, Pietenpol JA. Subtyping of triple-negative breast cancer: implications for therapy. Cancer. 2015; 121:8-16.
61. Castello A, Martin M, Ruiz A, Casas AM, Baena-Canada JM, Lope V, Antolin S, Sanchez P, Ramos M, Anton A, Munoz M, Bermejo B, De Juan-Ferre A, Jara C, Chacon JI, Jimeno MA, et al. Lower Breast Cancer Risk among Women following the World Cancer Research Fund and American Institute for Cancer Research Lifestyle Recommendations: EpiGEICAM Case-Control Study. PLoS One. 2015; 10:e0126096.
62. Al-azawi D, Leong S, Wong L, Kay E, Hill AD, Young L. HER-2 positive and p53 negative breast cancers are associated with poor prognosis. Cancer investigation. 2011; 29:365-369.
63. Wolff AC, Hammond ME, Schwartz JN, Hagerty KL, Allred DC, Cote RJ, Dowsett M, Fitzgibbons PL, Hanna WM, Langer A, McShane LM, Paik S, Pegram MD, Perez EA, Press MF, Rhodes A, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. Archives of pathology & laboratory medicine. 2007; 131:18-43.
64. Kim T, Han W, Kim MK, Lee JW, Kim J, Ahn SK, Lee HB, Moon HG, Lee KH, Kim TY, Han SW, Im SA, Park IA, Kim JY, Noh DY. Predictive Significance of p53, Ki-67, and Bcl-2 Expression for Pathologic Complete Response after Neoadjuvant Chemotherapy for Triple-Negative Breast Cancer. Journal of breast cancer. 2015; 18:16-21.
65. Maia JCC, Gomes SL, Juliani MH, Morel CM. Preparation of and [a-32 P]-nucleoside triphosphate, with high specific activity. Genes and Antigenes of Parasites: a Laboratory Manual. Rio de Janeiro, Brazil: FIOCRUZ1983; 146-157.
66. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry. 1951; 193:265-275.
67. Bacchi LM, Corpa M, Santos PP, Bacchi CE, Carvalho FM. Estrogen receptor-positive breast carcinomas in younger women are different from those of older women: a pathological and immunohistochemical study. Breast. 2010; 19:137-141.
68. Sola-Penna M, dos Santos AC, Alves GG, El-Bacha T, Faber-Barata J, Pereira MF, Serejo FC, Da Poian AT, Sorenson M. A radioassay for phosphofructokinase-1 activity in cell extracts and purified enzyme. JBiochemBiophysMethods. 2002; 50:129-140.
69. Zancan P, Sola-Penna M. Calcium influx: a possible role for insulin modulation of intracellular distribution and activity of 6-phosphofructo-1-kinase in human erythrocytes. MolGenetMetab. 2005; 86:392-400.
70. Zancan P, Sola-Penna M. Regulation of human erythrocyte metabolism by insulin: cellular distribution of 6-phosphofructo-1-kinase and its implication for red blood cell function. MolGenetMetab. 2005; 86:401-411.