Tumor-stroma metabolic relationship based on lactate shuttle can sustain prostate cancer progression

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Sanità, Patrizia ^a   Capulli, Mattia ^a   Teti, Anna ^a   Galatioto, Giuseppe P ^a   Vicentini, Carlo ^a   Chiarugi, Paola ^b   Bologna, Mauro ^a   Angelucci, Adriano ^a  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Aerobic glycolysis; Cancer associated fibroblasts; Monocarboxylate transporters; Tumor stroma; Warburg effect

Indexed keywords

CYCLOOXYGENASE 1; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 4; COTRANSPORTER; LACTIC ACID DERIVATIVE; MONOCARBOXYLATE TRANSPORT PROTEIN 1; MONOCARBOXYLATE TRANSPORTER; MUSCLE PROTEIN; SLC16A4 PROTEIN, HUMAN;

ADULT; AEROBIC METABOLISM; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER MODEL; CANCER TISSUE; CARCINOGENESIS; CARCINOMA CELL; CELL METABOLISM; CELL PROLIFERATION; CELL STRAIN; CELL STRAIN WI 38; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; DIPLOIDY; ENERGY METABOLISM; ENZYME ACTIVATION; FIBROBLAST; GENE SILENCING; GLYCOLYSIS; GROWTH RATE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PROSTATE CARCINOMA; PROSTATE EPITHELIUM; PROSTATE HYPERTROPHY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STROMA CELL; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT; UPREGULATION; VERY ELDERLY; ANIMAL; DISEASE COURSE; DISEASE MODEL; GENE EXPRESSION; GENETICS; METABOLISM; PATHOLOGY; PROSTATE TUMOR; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; XENOGRAFT;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FIBROBLASTS; GENE EXPRESSION; GENE SILENCING; GLYCOLYSIS; HETEROGRAFTS; HUMANS; LACTATES; MALE; MONOCARBOXYLIC ACID TRANSPORTERS; MUSCLE PROTEINS; PROSTATIC HYPERPLASIA; PROSTATIC NEOPLASMS; STROMAL CELLS; SYMPORTERS; TUMOR MICROENVIRONMENT;

EID: 84896722500     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-154     Document Type: Article

References (32)

1. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314. 10.1126/science.123.3191.309, 13298683.
2. Moreno-Sanchez R, Rodriguez-Enriquez S, Marin-Hernandez A, Saavedra E. Energy metabolism in tumor cells. FEBS J 2007, 274:1393-1418. 10.1111/j.1742-4658.2007.05686.x, 17302740.
3. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008, 7:11-20. 10.1016/j.cmet.2007.10.002, 18177721.
4. Roberts MJ, Schirra HJ, Lavin MF, Gardiner RA. Metabolomics: a novel approach to early and noninvasive prostate cancer detection. Korean J Urol 2011, 52:79-89. 10.4111/kju.2011.52.2.79, 3045724, 21379423.
5. Garcia CK, Li X, Luna J, Francke U. cDNA cloning of the human monocarboxylate transporter 1 and chromosomal localization of the SLC16A1 locus to 1p13.2-p12. Genomics 1994, 23:500-503. 10.1006/geno.1994.1532, 7835905.
6. Bonen A. The expression of lactate transporters (MCT1 and MCT4) in heart and muscle. Eur J Appl Physiol 2001, 86:6-11. 10.1007/s004210100516, 11820324.
7. Halestrap AP, Price NT. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem J 1999, 343(Pt 2):281-299. 1220552, 10510291.
8. Cuff MA, Lambert DW, Shirazi-Beechey SP. Substrate-induced regulation of the human colonic monocarboxylate transporter, MCT1. J Physiol 2002, 539:361-371. 10.1113/jphysiol.2001.014241, 2290148, 11882670.
9. Bergersen LH. Is lactate food for neurons? Comparison of monocarboxylate transporter subtypes in brain and muscle. Neuroscience 2007, 145:11-19. 10.1016/j.neuroscience.2006.11.062, 17218064.
10. Kuchiiwa T, Nio-Kobayashi J, Takahashi-Iwanaga H, Yajima T, Iwanaga T. Cellular expression of monocarboxylate transporters in the female reproductive organ of mice: implications for the genital lactate shuttle. Histochem Cell Biol 2011, 135:351-360. 10.1007/s00418-011-0794-2, 21360229.
11. Hirschhaeuser F, Sattler UG, Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res 2011, 71:6921-6925. 10.1158/0008-5472.CAN-11-1457, 22084445.
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. 10.1007/s10863-012-9428-1, 22407107.
13. Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, Pestell RG, Martinez-Outschoorn UE, Sotgia F, Lisanti MP. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle 2009, 8:3984-4001. 10.4161/cc.8.23.10238, 19923890.
14. 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. 2582933, 19033663.
15. Costello LC, Franklin RB, Narayan P. Citrate in the diagnosis of prostate cancer. Prostate 1999, 38:237-245. 10.1002/(SICI)1097-0045(19990215)38:3<237::AID-PROS8>3.0.CO;2-O, 10068348.
16. Swanson MG, Zektzer AS, Tabatabai ZL, Simko J, Jarso S, Keshari KR, Schmitt L, Carroll PR, Shinohara K, Vigneron DB, Kurhanewicz J. Quantitative analysis of prostate metabolites using 1H HR-MAS spectroscopy. Magn Reson Med 2006, 55:1257-1264. 10.1002/mrm.20909, 16685733.
17. Movsas B, Chapman JD, Horwitz EM, Pinover WH, Greenberg RE, Hanlon AL, Iyer R, Hanks GE. Hypoxic regions exist in human prostate carcinoma. Urology 1999, 53:11-18. 10.1016/S0090-4295(98)00500-7, 9886581.
18. Remmele W, Hildebrand U, Hienz HA, Klein PJ, Vierbuchen M, Behnken LJ, Heicke B, Scheidt E. Comparative histological, histochemical, immunohistochemical and biochemical studies on oestrogen receptors, lectin receptors, and Barr bodies in human breast cancer. Virchows Arch A Pathol Anat Histopathol 1986, 409:127-147. 10.1007/BF00708323, 2424168.
19. Sieh S, Taubenberger AV, Rizzi SC, Sadowski M, Lehman ML, Rockstroh A, An J, Clements JA, Nelson CC, Hutmacher DW. Phenotypic characterization of prostate cancer LNCaP cells cultured within a bioengineered microenvironment. PLoS One 2012, 7:e40217. 10.1371/journal.pone.0040217, 3434144, 22957009.
20. Takebe K, Nio-Kobayashi J, Takahashi-Iwanaga H, Yajima T, Iwanaga T. Cellular expression of a monocarboxylate transporter (MCT1) in the mammary gland and sebaceous gland of mice. Histochem Cell Biol 2009, 131:401-409. 10.1007/s00418-008-0543-3, 19048272.
21. Takebe K, Takahashi-Iwanaga H, Iwanaga T. Intensified expressions of a monocarboxylate transporter in consistently renewing tissues of the mouse. Biomed Res 2011, 32:293-301. 10.2220/biomedres.32.293, 21878737.
22. Pertega-Gomes N, Vizcaino JR, Miranda-Goncalves V, Pinheiro C, Silva J, Pereira H, Monteiro P, Henrique RM, Reis RM, Lopes C, Baltazar F. Monocarboxylate transporter 4 (MCT4) and CD147 overexpression is associated with poor prognosis in prostate cancer. BMC Cancer 2011, 11:312. 10.1186/1471-2407-11-312, 3157459, 21787388.
23. Hao J, Chen H, Madigan MC, Cozzi PJ, Beretov J, Xiao W, Delprado WJ, Russell PJ, Li Y. Co-expression of CD147 (EMMPRIN), CD44v3-10, MDR1 and monocarboxylate transporters is associated with prostate cancer drug resistance and progression. Br J Cancer 2010, 103:1008-1018. 10.1038/sj.bjc.6605839, 2965856, 20736947.
24. Pellerin L, Magistretti PJ. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 1994, 91:10625-10629. 10.1073/pnas.91.22.10625, 45074, 7938003.
25. Johnson MT, Freeman EA, Gardner DK, Hunt PA. Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol Reprod 2007, 77:2-8. 10.1095/biolreprod.106.059899, 17314311.
26. Py G, Eydoux N, Lambert K, Chapot R, Koulmann N, Sanchez H, Bahi L, Peinnequin A, Mercier J, Bigard AX. Role of hypoxia-induced anorexia and right ventricular hypertrophy on lactate transport and MCT expression in rat muscle. Metabolism 2005, 54:634-644. 10.1016/j.metabol.2004.12.007, 15877294.
27. Ord JJ, Streeter EH, Roberts IS, Cranston D, Harris AL. Comparison of hypoxia transcriptome in vitro with in vivo gene expression in human bladder cancer. Br J Cancer 2005, 93:346-354. 10.1038/sj.bjc.6602666, 2361571, 16052224.
28. Martinez-Outschoorn UE, Balliet RM, Rivadeneira DB, Chiavarina B, Pavlides S, Wang C, Whitaker-Menezes D, Daumer KM, Lin Z, Witkiewicz AK, Flomenberg N, Howell A, Pestell RG, Knudsen ES, Sotgia F, Lisanti MP. Oxidative stress in cancer associated fibroblasts drives tumor-stroma co-evolution: a new paradigm for understanding tumor metabolism, the field effect and genomic instability in cancer cells. Cell Cycle 2010, 9:3256-3276. 3041164, 20814239.
29. Fiaschi T, Marini A, Giannoni E, Taddei ML, Gandellini P, De Donatis A, Lanciotti M, Serni S, Cirri P, Chiarugi P. Reciprocal metabolic reprogramming through lactate shuttle coordinately influences tumor-stroma interplay. Cancer Res 2012, 72:5130-5140. 10.1158/0008-5472.CAN-12-1949, 22850421.
30. Martinez-Outschoorn UE, Lin Z, Trimmer C, Flomenberg N, Wang C, Pavlides S, Pestell RG, Howell A, Sotgia F, Lisanti MP. Cancer cells metabolically " fertilize" the tumor microenvironment with hydrogen peroxide, driving the Warburg effect: implications for PET imaging of human tumors. Cell Cycle 2011, 10:2504-2520. 10.4161/cc.10.15.16585, 3180189, 21778829.
31. Kim HS, Masko EM, Poulton SL, Kennedy KM, Pizzo SV, Dewhirst MW, Freedland SJ. Carbohydrate restriction and lactate transporter inhibition in a mouse xenograft model of human prostate cancer. BJU Int 2012, 110:1062-1069. 10.1111/j.1464-410X.2012.10971.x, 3371292, 22394625.
32. Maehama T, Patzelt A, Lengert M, Hutter KJ, Kanazawa K, Hausen H, Rosl F. Selective down-regulation of human papillomavirus transcription by 2-deoxyglucose. Int J Cancer 1998, 76:639-646. 10.1002/(SICI)1097-0215(19980529)76:5<639::AID-IJC5>3.0.CO;2-R, 9610719.