Molecular pathways: Trafficking of metabolic resources in the tumor microenvironment

Clinical Cancer Research

Volumn 21, Issue 4, 2015, Pages 680-686

  Romero, Iris L ^a   Mukherjee, Abir ^a   Kenny, Hilary A ^a   Litchfield, Lacey M ^a   Lengyel, Ernst ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; 4 PHENYLBUTYRIC ACID; ANTINEOPLASTIC AGENT; ARGININE; ASPARAGINASE; AZD 3965; CHLOROQUINE; CYSTINE; CYTOKINE; DICHLOROACETIC ACID; FATTY ACID; FATTY ACID BINDING PROTEIN 4 INHIBITOR; GLUTAMINE; GLUTATHIONE; LACTATE DEHYDROGENASE; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; METFORMIN; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 4; PIOGLITAZONE; PROTEIN P62; PROTEIN TYROSINE KINASE INHIBITOR; PROTEINASE; SORAFENIB; SUNITINIB; TETRAHYDROLIPSTATIN; TROGLITAZONE; TRYPTOPHAN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADIPOCYTE; AMINO ACID METABOLISM; ANAEROBIC GLYCOLYSIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BLADDER CANCER; CACHEXIA; CANCER ADJUVANT THERAPY; CANCER RESISTANCE; CARDIOVASCULAR DISEASE; CELL DEDIFFERENTIATION; CELL INVASION; CELL PROTECTION; CHRONIC LYMPHATIC LEUKEMIA; CITRIC ACID CYCLE; COLORECTAL CANCER; CYTOKINE RELEASE; DRUG EFFICACY; DRUG SAFETY; DRUG TARGETING; ENDOTHELIUM CELL; ENERGY TRANSFER; ENERGY YIELD; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; LIPOSARCOMA; MESOTHELIUM CELL; METASTASIS; MOLECULAR INTERACTION; MULTIDRUG RESISTANCE; NEOPLASM; NONHUMAN; NUCLEOTIDE METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SOLID TUMOR; STROMA CELL; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; UNSPECIFIED SIDE EFFECT; BIOLOGICAL MODEL; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84923164098     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-2198     Document Type: Article

References (52)

1. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol 2010;177:1053-64.
2. Orimo A, Gupta P, Sgroi D, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL 12 secretion. Cell 2005;121:335-48.
3. Karnoub A, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007;449:557-63.
4. Kenny HA, Chiang CY, White EA, Schryver EM, Habis M, Romero IL, et al. Mesothelial cells promote early ovarian cancer metastasis through fibronectin secretion. J Clin Invest 2014;124:4614-28.
5. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-7.
6. White EA, Kenny HA, Lengyel E. Three-dimensional modeling of ovarian cancer. Adv Drug Deliv Rev 2014;79-80C:184-92.
7. Kenny HA, Kaur S, Coussens LM, Lengyel E. The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin. J Clin Invest 2008;118:1367-79.
8. De-Berardinis RJ, Sayed N, Ditsworth D, Thompson CB. Brick by brick: metabolismand tumor cell growth. Curr Opin Genet Dev 2008;18:54-61.
9. Wakil SJ, Abu-Elheiga LA. Fatty acid metabolism: target for metabolic syndrome. J Lipid Res 2009;50:S138-S43.
10. Brooks GA. Cell-cell and intracellular lactate shuttles. J Physiol 2009;587: 5591-600.
11. Sonveaux P, Schroeder VF, Wergin MC, Verrax J, Rabbani ZN, De-Saedeleer CJ, et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 2008;118:3930-42.
12. Brooks GA. Anaerobic threshold: review of the concept and directions for future research. Med Sci Sports Exerc 1985;17:22-34.
13. Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E. Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role of tumor-associated stroma. Cancer Res 2006;66:632-7.
14. Martinez-Outschoorn UE, Whitaker-Menezes D, Pavlides S, Chiavarina B, Bonuccelli G, Trimmer C, et al. The autophagic tumor stroma model of cancer or "battery-operated tumor growth" a simple solution to the autophagy paradox. Cell Cycle 2010;9:4297-306.
15. Martinez-Outschoorn UE, Balliet RM, Rivadeneira DB, Chiavarina B, Pavlides S, Wang C, et al. 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;9:3256-76.
16. Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, et al. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle 2009;8: 3984-4001.
17. Sotgia F, Del-Galdo F, Casimiro MC, Bonuccelli G, Mercier I, Whitaker- Menezes D, et al. Caveolin-1-/- null mammary stromal fibroblasts share characteristics with human breast cancer-associated fibroblasts. Am J Pathol 2009;174:746-61.
18. Chen D, Che G. Value of caveolin-1 in cancer progression and prognosis: emphasis on cancer-associated fibroblasts, human cancer cells and mechanism of caveolin-1 expression (review). Oncol Lett 2014; 8:1409-21.
19. Witkiewicz AK, Whitaker-Menezes D, Dasgupta A, Philp NJ, Lin Z, Gandara R, et al. Using the "reverse Warburg effect" to identify high-risk breast cancer patients: stromal MCT4 predicts poor clinical outcome in triple-negative breast cancers. Cell Cycle 2012;11:1108-17.
20. Wise DR, Thompson CB. Glutamine addiction: a new therapeutic target in cancer. Trends Biochem Sci 2010;35:427-33.
21. Terunuma A, Putluri N, Mishra P, Mathe EA, Dorsey TH, Yi M, et al. MYCdriven accumulation of 2-hydroxyglutarate is associated with breast cancer prognosis. J Clin Invest 2014;124:398-412.
22. Li B, Simon MC. Molecular pathways: targeting MYC-induced metabolic reprogramming and oncogenic stress in cancer. Clin Cancer Res 2013;19: 5835-41.
23. Pavlides S, Tsirigos A, Migneco G, Whitaker-Menezes D, Chiavarina B, Flomenberg N, et al. The autophagic tumor stroma model of cancer: role of oxidative stress and ketone production in fueling tumor cell metabolism. Cell Cycle 2010;9:3485-505.
24. Ko YH, Lin Z, Flomenberg N, Pestell RG, Howell A, Sotgia F, et al. Glutamine fuels a vicious cycle of autophagy in the tumor stroma and oxidative mitochondrial metabolism in epithelial cancer cells: implications for preventing chemotherapy resistance. Cancer Biol Ther 2011;12: 1085-97.
25. Gottfried E, Kreutz M, Mackensen A. Tumor metabolism as modulator of immune response and tumor progression. Semin Cancer Biol 2012;22: 335-41.
26. Ino Y, Yamazaki-Itoh R, Oguro S, Shimada K, Kosuge T, Zavada J, et al. Arginase II expressed in cancer-associated fibroblasts indicates tissue hypoxia and predicts poor outcome in patients with pancreatic cancer. PLoS ONE 2013;8:e55146.
27. Chen JY, Li CF, Kuo CC, Tsai KK, Hou MF, Hung WC. Cancer/stroma interplay via cyclooxygenase-2 and indoleamine 2, 3-dioxygenase promotes breast cancer progression. Breast Cancer Res 2014;16:410.
28. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, et al. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 2011;478:197-203.
29. Valencia T, Kim JY, Abu-Baker S, Moscat-Pardos J, Ahn CS, Reina-Campos M, et al. Metabolic reprogramming of stromal fibroblasts through p62- mTORC1 signaling promotes inflammation and tumorigenesis. Cancer Cell 2014;26:121-35.
30. Zhang W, Trachootham D, Liu J, Chen G, Pelicano H, Garcia-Prieto C, et al. Stromal control of cystine metabolism promotes cancer cell survival in chronic lymphocytic leukaemia. Nat Cell Biol 2012;14: 276-86.
31. Dirat B, Bochet L, Dabek M, Daviaud D, Dauviller S, Majad B, et al. Cancerassociated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res 2011;71:2455-65.
32. Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R, Zillhardt M, et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat Med 2011;17:1498-503.
33. Andarawewa KL, Montrescu ER, Chenard MP, Gansmuller A, Stoll I, Tomasetto C, et al. Stromelysin-3 is a potent negative regulator of adipogenesis participating to cancer cell-adipocyte interaction/crosstalk at the tumor invasive front. Cancer Res 2005;65:10862-71.
34. Gazi E, Gardner P, Lockyer NP, Hart CA, Brown MD, Clarke NW. Direct evidence of lipid translocation between adipocytes and prostate cancer cells with imaging FTIR microspectroscopy. J Lipid Res 2007; 48:1846.
35. Liu Y. Fatty acid oxidation is a dominant bioenergetic pathway in prostate cancer. Prostate Cancer Prostatic Dis 2006;9:230-4.
36. Takahashi N, Inoue T, Lee J, Yamaguchi T, Shizukuishi K. The roles of PET and PET/CT in the diagnosis and management of prostate cancer. Oncology 2007;72:226-33.
37. Nieman KM, Romero IL, Van-Houten B, Lengyel E. Adipocyte tissue and adipocytes support tumorigenesis and metastasis. Biochim Biophys Acta 2013;1831:1533-41.
38. Das S, Eder S, Schauer S, Diwoky C, Temmel H, Guertl B, et al. Adipose triglyceride lipase contributes to cancer-associated cachexia. Science 2011; 333:233-8.
39. Martinez-Outschoorn UE, Pavlides S, Whitaker-Menezes D, Daumer KM, Milliman JN, Chiavarina B, et al. Tumor cells induce the cancer associated fibroblast phenotype via caveolin-1 degradation: implications for breast cancer and DCIS therapy with autophagy inhibitors. Cell Cycle 2010;9:2423-33.
40. Kimura T, Takabatake Y, Takahashi A, Isaka Y. Chloroquine in cancer therapy: a double-edged sword of autophagy. Cancer Res 2013;73:3-7.
41. Tontonoz P, Hu E, Spiegelman BM. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 1994;79:1147-56.
42. Demetri GD, Fletcher CD, Mueller E, Sarraf P, Naujoks R, Campbell N, et al. Induction of solid tumor differentiation by the peroxisome proliferatoractivated receptor-gamma ligand troglitazone in patients with liposarcoma. Proc Natl Acad Sci U S A 1999;96:3951-6.
43. Avramis VI, Panosyan EH. Pharmacokinetic/pharmacodynamic relationships of asparaginase formulations: the past, the present and recommendations for the future. Clin Pharmacokinet 2005;44:367-93.
44. Gilbert J, Baker SD, Bowling MK, Grochow L, Figg WD, Zabelina Y, et al. A phase I dose escalation and bioavailability study of oral sodium phenylbutyrate in patients with refractory solid tumor malignancies. Clin Cancer Res 2001;7:2292-300.
45. Carducci MA, Gilbert J, Bowling MK, Noe D, Eisenberger MA, Sinibaldi V, et al. A Phase I clinical and pharmacological evaluation of sodium phenylbutyrate on an 120-h infusion schedule. Clin Cancer Res 2001;7: 3047-55.
46. Doherty JR, Cleveland JL. Targeting lactate metabolism for cancer therapeutics. J Clin Invest 2013;123:3685-92.
47. Michelakis ED, Webster L, Mackey JR. Dichloroacetate (DCA) as a potential metabolic-targeting therapy for cancer. Br J Cancer 2008;99:989-94.
48. Decensi A, Puntoni M, Goodwin P, Cazzaniga M, Gennari A, Bonanni B, et al. Metformin and cancer risk in diabetic patients: a systematic review and meta-analysis. Cancer Prev Res 2010;3:1451-61.
49. Tebbe C, Chhina J, Dar SA, Sarigiannis K, Giri S, Munkarah AR, et al. Metformin limits the adipocyte tumor-promoting effect on ovarian cancer. Oncotarget 2014;5:4123-41.
50. Sounni NE, Cimino J, Blacher S, Primac I, Truong A, Mazzucchelli G, et al. Blocking lipid synthesis overcomes tumor regrowth and metastasis after antiangiogenic therapy withdrawal. Cell Metab 2014;20:280-94.
51. Liu X, Ser Z, Locasale JW. Development and quantitative evaluation of a high-resolution metabolomics technology. Anal Chem 2014;86: 2175-84.
52. Members MSIB, Sansone SA, Fan T, Goodacre R, Griffin JL, Hardy NW, et al. The metabolomics standards initiative. Nat Biotechnol 2007;25:846-8.