Metabolic reprogramming: A new relevant pathway in adult adrenocortical tumors

Oncotarget

Volumn 6, Issue 42, 2015, Pages 44403-44421

  Pinheiro, Céline ^a,b,c,d   Granja, Sara ^a,b   Longatto Filho, Adhemar ^a,b,d,e   Faria, André M ^e   Fragoso, Maria C B V ^e   Lovisolo, Silvana M ^e   Lerário, Antonio M ^e   Almeida, Madson Q ^e   Baltazar, Fátima ^a,b   Zerbini, Maria C N ^e  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

^c Barretos School of Health Sciences Dr Paulo Prata FACISB   (Brazil)

^d BARRETOS CANCER HOSPITAL   (Brazil)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Adrenocortical tumors; Metabolic reprogramming; Monocarboxylate transporter; Warburg effect

Indexed keywords

CARBONATE DEHYDRATASE IX; CD147 ANTIGEN; GLUCOSE TRANSPORTER 1; HERMES ANTIGEN; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 2; MONOCARBOXYLATE TRANSPORTER 4; BSG PROTEIN, HUMAN; CA9 PROTEIN, HUMAN; CARBONATE DEHYDRATASE; CD44 PROTEIN, HUMAN; COTRANSPORTER; MONOCARBOXYLATE TRANSPORT PROTEIN 1; MONOCARBOXYLATE TRANSPORTER; MUSCLE PROTEIN; SLC16A4 PROTEIN, HUMAN; SLC16A7 PROTEIN, HUMAN; SLC2A1 PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR MARKER;

ADRENAL CORTEX ADENOMA; ADRENAL CORTEX CARCINOMA; ADRENAL CORTEX TUMOR; ADULT; ARTICLE; CANCER GRADING; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CONTROLLED STUDY; DISEASE FREE SURVIVAL; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; METABOLIC REPROGRAMMING; METABOLISM; MITOSIS INDEX; OVERALL SURVIVAL; PROTEIN EXPRESSION; SURVIVAL PREDICTION; SURVIVAL TIME; ADOLESCENT; ADRENAL CORTEX NEOPLASMS; ADRENOCORTICAL ADENOMA; ADRENOCORTICAL CARCINOMA; AGED; CHEMISTRY; COMPARATIVE STUDY; ENERGY METABOLISM; KAPLAN MEIER METHOD; MIDDLE AGED; MORTALITY; PATHOLOGY; PROPORTIONAL HAZARDS MODEL; TIME FACTOR; TREATMENT OUTCOME; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADRENAL CORTEX NEOPLASMS; ADRENOCORTICAL ADENOMA; ADRENOCORTICAL CARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD147; ANTIGENS, CD44; ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CARBONIC ANHYDRASE IX; CARBONIC ANHYDRASES; DISEASE-FREE SURVIVAL; ENERGY METABOLISM; FEMALE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; MITOTIC INDEX; MONOCARBOXYLIC ACID TRANSPORTERS; MUSCLE PROTEINS; NEOPLASM GRADING; NEOPLASM STAGING; PROPORTIONAL HAZARDS MODELS; SYMPORTERS; TIME FACTORS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84953410803     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5623     Document Type: Article

References (42)

1. Fassnacht M, Libe R, Kroiss M, Allolio B. Adrenocortical carcinoma: a clinician's update. Nat Rev Endocrinol. 2011; 7:323-335.
2. Fassnacht M, Kroiss M, Allolio B. Update in adrenocortical carcinoma. J Clin Endocrinol Metab. 2013; 98:4551-4564.
3. Else T, Kim AC, Sabolch A, Raymond VM, Kandathil A, Caoili EM, Jolly S, Miller BS, Giordano TJ, Hammer GD. Adrenocortical carcinoma. Endocr Rev. 2014; 35:282-326.
4. Fassnacht M, Terzolo M, Allolio B, Baudin E, Haak H, Berruti A,Welin S, Schade-Brittinger C, Lacroix A, Jarzab B, Sorbye H,Torpy DJ, Stepan V, Schteingart DE, Arlt W, Kroiss M, et al. Combination chemotherapy in advanced adrenocortical carcinoma. N Engl J Med. 2012; 366:2189-2197.
5. Berruti A, Baudin E, Gelderblom H, Haak HR, Porpiglia F,Fassnacht M, Pentheroudakis G, Group EGW. Adrenal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2012; 23:vii131-138.
6. Faria AM, Almeida MQ. Differences in the molecular mechanisms of adrenocortical tumorigenesis between children and adults. Mol Cell Endocrinol. 2012; 351:52-57.
7. Lucon AM, Pereira MA, Mendonca BB, Zerbini MC, Saldanha LB, Arap S. Adrenocortical tumors: results of treatment and study of Weiss's score as a prognostic factor. Rev Hosp Clin Fac Med Sao Paulo. 2002; 57:251-256.
8. Duregon E, Volante M, Giorcelli J, Terzolo M, Lalli E, Papotti M. Diagnostic and prognostic role of steroidogenic factor 1 in adrenocortical carcinoma: a validation study focusing on clinical and pathologic correlates. Hum Pathol. 2013; 44:822-828.
9. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 2004; 4:891-899.
10. Tennant DA, Duran RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer. 2010; 10:267-277.
11. Chiche J, Brahimi-Horn MC, Pouyssegur J. Tumour hypoxia induces a metabolic shift causing acidosis: a common feature in cancer. J Cell Mol Med. 2010; 14:771-794.
12. Pinheiro C, Longatto-Filho A, Azevedo-Silva J, Casal M, Schmitt FC, Baltazar F. Role of monocarboxylate transporters in human cancers: state of the art. J Bioenerg Biomembr. 2012; 44:127-139.
13. de Oliveira AT, Pinheiro C, Longatto-Filho A, Brito MJ, Martinho O, Matos D, Carvalho AL, Vazquez VL, Silva TB,Scapulatempo C, Saad SS, Reis RM, Baltazar F. Co-expression of monocarboxylate transporter 1 (MCT1) and its chaperone (CD147) is associated with low survival in patients with gastrointestinal stromal tumors (GISTs). J Bioenerg Biomembr. 2012; 44:171-178.
14. Miranda-Goncalves V, Honavar M, Pinheiro C, Martinho O,Pires MM, Pinheiro C, Cordeiro M, Bebiano G, Costa P, Palmeirim I, Reis RM, Baltazar F. Monocarboxylate transporters (MCTs) in gliomas: expression and exploitation as therapeutic targets. Neuro Oncol. 2013; 15:172-188.
15. Pinheiro C, Penna V, Morais-Santos F, Abrahao-Machado LF,Ribeiro G, Curcelli EC, Olivieri MV, Morini S, Valenca I, Ribeiro D, Schmitt FC, Reis RM, Baltazar F. Characterization of monocarboxylate transporters (MCTs) expression in soft tissue sarcomas: distinct prognostic impact of MCT1 sub-cellular localization. J Transl Med. 2014; 12:118.
16. Halestrap AP. The monocarboxylate transporter family-Structure and functional characterization. IUBMB Life. 2012; 64:1-9.
17. Kirk P, Wilson MC, Heddle C, Brown MH, Barclay AN, Halestrap AP. CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J. 2000; 19:3896-3904.
18. Wilson MC, Meredith D, Fox JE, Manoharan C, Davies AJ, Halestrap AP. Basigin (CD147) is the target for organomercurial inhibition of monocarboxylate transporter isoforms 1 and 4: the ancillary protein for the insensitive MCT2 is EMBIGIN (gp70). J Biol Chem. 2005; 280:27213-27221.
19. Slomiany MG, Grass GD, Robertson AD, Yang XY, Maria BL,Beeson C, Toole BP. Hyaluronan, CD44, and emmprin regulate lactate efflux and membrane localization of monocarboxylate transporters in human breast carcinoma cells. Cancer Res. 2009; 69:1293-1301.
20. Pinheiro C, Reis RM, Ricardo S, Longatto-Filho A, Schmitt F, Baltazar F. Expression of monocarboxylate transporters 1, 2, and 4 in human tumours and their association with CD147 and CD44. J Biomed Biotechnol. 2010; 2010:427694.
21. Fenske W, Volker HU, Adam P, Hahner S, Johanssen S, Wortmann S, Schmidt M, Morcos M, Muller-Hermelink HK,Allolio B, Fassnacht M. Glucose transporter GLUT1 expression is an stage-independent predictor of clinical outcome in adrenocortical carcinoma. Endocr Relat Cancer. 2009; 16:919-928.
22. Nunes ML, Rault A, Teynie J, Valli N, Guyot M, Gaye D, Belleannee G, Tabarin A. 18F-FDG PET for the identification of adrenocortical carcinomas among indeterminate adrenal tumors at computed tomography scanning. World J Surg. 2010; 34:1506-1510.
23. Deandreis D, Leboulleux S, Caramella C, Schlumberger M,Baudin E. FDG PET in the management of patients with adrenal masses and adrenocortical carcinoma. Horm Cancer. 2011; 2:354-362.
24. Takeuchi S, Balachandran A, Habra MA, Phan AT, Bassett RL, Jr., Macapinlac HA, Chuang HH. Impact of (1)(8)F-FDG PET/CT on the management of adrenocortical carcinoma: analysis of 106 patients. Eur J Nucl Med Mol Imaging. 2014; 41:2066-2073.
25. Bourdeau I, MacKenzie-Feder J, Lacroix A. Recent advances in adrenocortical carcinoma in adults. Curr Opin Endocrinol Diabetes Obes. 2013; 20:192-197.
26. Ribeiro RC, Sandrini F, Figueiredo B, Zambetti GP, Michalkiewicz E, Lafferty AR, DeLacerda L, Rabin M, Cadwell C, Sampaio G, Cat I, Stratakis CA, Sandrini R. An inherited p53 mutation that contributes in a tissue-specific manner to pediatric adrenal cortical carcinoma. Proc Natl Acad Sci U S A. 2001; 98:9330-9335.
27. Latronico AC, Pinto EM, Domenice S, Fragoso MC, Martin RM, Zerbini MC, Lucon AM, Mendonca BB. An inherited mutation outside the highly conserved DNA-binding domain of the p53 tumor suppressor protein in children and adults with sporadic adrenocortical tumors. J Clin Endocrinol Metab. 2001; 86:4970-4973.
28. Parks SK, Chiche J, Pouyssegur J. Disrupting proton dynamics and energy metabolism for cancer therapy. Nat Rev Cancer. 2013; 13:611-623.
29. Ganapathy V, Thangaraju M, Prasad PD. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther. 2009; 121:29-40.
30. Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, Gottfried E, Schwarz S, Rothe G, Hoves S, Renner K,Timischl B, Mackensen A, Kunz-Schughart L, Andreesen R, Krause SW, et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood. 2007; 109:3812-3819.
31. Walenta S, Schroeder T, Mueller-Klieser W. Metabolic mapping with bioluminescence: basic and clinical relevance. Biomol Eng. 2002; 18:249-262.
32. Hunt TK, Aslam RS, Beckert S, Wagner S, Ghani QP, Hussain MZ, Roy S, Sen CK. Aerobically derived lactate stimulates revascularization and tissue repair via redox mechanisms. Antioxid Redox Signal. 2007; 9:1115-1124.
33. Stern R, Shuster S, Neudecker BA, Formby B. Lactate stimulates fibroblast expression of hyaluronan and CD44: the Warburg effect revisited. Exp Cell Res. 2002; 276:24-31.
34. Sonveaux P, Vegran F, Schroeder T, Wergin MC, Verrax J,Rabbani ZN, De Saedeleer CJ, Kennedy KM, Diepart C,Jordan BF, Kelley MJ, Gallez B, Wahl ML, Feron O, Dewhirst MW. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest. 2008; 118:3930-3942.
35. Smallbone K, Gavaghan DJ, Gatenby RA, Maini PK. The role of acidity in solid tumour growth and invasion. J Theor Biol. 2005; 235:476-484.
36. Faria AM, Sbiera S, Ribeiro TC, Soares IC, Mariani BM,Freire DS, de Sousa GR, Lerario AM, Ronchi CL, Deutschbein T, Wakamatsu A, Alves VA, Zerbini MC,Mendonca BB, Fragoso MC, Latronico AC, et al. Expression of LIN28 and its regulatory microRNAs in adult adrenocortical cancer. Clin Endocrinol (Oxf). 2015; 82:481-488.
37. Weiss LM. Comparative histologic study of 43 metastasizing and nonmetastasizing adrenocortical tumors. Am J Surg Pathol. 1984; 8:163-169.
38. Fassnacht M, Johanssen S, Quinkler M, Bucsky P, Willenberg HS, Beuschlein F, Terzolo M, Mueller HH, Hahner S, Allolio B, German Adrenocortical Carcinoma Registry G, European Network for the Study of Adrenal T. Limited prognostic value of the 2004 International Union Against Cancer staging classification for adrenocortical carcinoma: proposal for a Revised TNM Classification. Cancer. 2009; 115:243-250.
39. Pinheiro C, Longatto-Filho A, Scapulatempo C, Ferreira L, Martins S, Pellerin L, Rodrigues M, Alves VA, Schmitt F, Baltazar F. Increased expression of monocarboxylate transporters 1, 2, and 4 in colorectal carcinomas. Virchows Arch. 2008; 452:139-146.
40. Pinheiro C, Sousa B, Albergaria A, Paredes J, Dufloth R,Vieira D, Schmitt F, Baltazar F. GLUT1 and CAIX expression profiles in breast cancer correlate with adverse prognostic factors and MCT1 overexpression. Histol Histopathol. 2011; 26:1279-1286.
41. Queiros O, Preto A, Pacheco A, Pinheiro C, Azevedo-Silva J,Moreira R, Pedro M, Ko YH, Pedersen PL, Baltazar F, Casal M. Butyrate activates the monocarboxylate transporter MCT4 expression in breast cancer cells and enhances the antitumor activity of 3-bromopyruvate. J Bioenerg Biomembr. 2012; 44:141-153.
42. Granja S, Morais-Santos F, Miranda-Goncalves V, Viana-Ferreira M, Nogueira R, Nogueira-Silva C, Correia-Pinto J,Baltazar F. The monocarboxylate transporter inhibitor alpha-cyano-4-hydroxycinnamic acid disrupts rat lung branching. Cell Physiol Biochem. 2013; 32:1845-1856.