5,394
Views
315
CrossRef citations to date
0
Altmetric
Report

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

, , , , , , , , , , , , , , & show all
Pages 3276-3296 | Published online: 15 Aug 2010

References

  • Koleske AJ, Baltimore D, Lisanti MP. Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci USA 1995; 92:1381 - 1385
  • Lee SW, Reimer CL, Oh P, Campbell DB, Schnitzer JE. Tumor cell growth inhibition by caveolin reexpression in human breast cancer cells. Oncogene 1998; 16:1391 - 1397
  • Park DS, Razani B, Lasorella A, Schreiber-Agus N, Pestell RG, Iavarone A, et al. Evidence that Myc isoforms transcriptionally repress caveolin-1 gene expression via an INR-dependent mechanism. Biochemistry 2001; 40:3354 - 3362
  • Galbiati F, Volonte D, Engelman JA, Watanabe G, Burk R, Pestell RG, et al. Targeted downregulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J 1998; 17:6633 - 6648
  • Liu J, Lee P, Galbiati F, Kitsis RN, Lisanti MP. Caveolin-1 expression sensitizes fibroblastic and epithelial cells to apoptotic stimulation. Am J Physiol Cell Physiol 2001; 280:823 - 835
  • Engelman JA, Wykoff CC, Yasuhara S, Song KS, Okamoto T, Lisanti MP. Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 1997; 272:16374 - 16381
  • Witkiewicz AK, Dasgupta A, Sotgia F, Mercier I, Pestell RG, Sabel M, et al. An absence of stromal caveolin-1 expression predicts early tumor recurrence and poor clinical outcome in human breast cancers. Am J Pathol 2009; 174:2023 - 2034
  • Sloan EK, Ciocca DR, Pouliot N, Natoli A, Restall C, Henderson MA, et al. Stromal cell expression of caveolin-1 predicts outcome in breast cancer. Am J Pathol 2009; 174:2035 - 2043
  • Witkiewicz AK, Dasgupta A, Nguyen KH, Liu C, Kovatich AJ, Schwartz GF, et al. Stromal caveolin-1 levels predict early DCIS progression to invasive breast cancer. Cancer Biol Ther 2009; 8:1071 - 1079
  • Witkiewicz AK, Dasgupta A, Sammons S, Er O, Potoczek MB, Guiles F, et al. Loss of stromal caveolin-1 expression predicts poor clinical outcome in triple negative and basal-like breast cancers. Cancer Biol Ther 2010; 10:135 - 143
  • Di Vizio D, Morello M, Sotgia F, Pestell RG, Freeman MR, Lisanti MP. An absence of stromal caveolin-1 is associated with advanced prostate cancer, metastatic disease and epithelial Akt activation. Cell Cycle 2009; 8:2420 - 2424
  • Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006; 6:392 - 401
  • Mercier I, Casimiro MC, Wang C, Rosenberg AL, Quong J, Minkeu A, et al. Human breast cancer-associated fibroblasts (CAFs) show caveolin-1 downregulation and RB tumor suppressor functional inactivation: Implications for the response to hormonal therapy. Cancer Biol Ther 2008; 7:1212 - 1225
  • 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 - 761
  • 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 - 2433
  • Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, et al. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 1997; 272:25437 - 25440
  • Shi Y, Pritchard KA Jr, Holman P, Rafiee P, Griffith OW, Kalyanaraman B, et al. Chronic myocardial hypoxia increases nitric oxide synthase and decreases caveolin-3. Free Radic Biol Med 2000; 29:695 - 703
  • Goligorsky MS, Li H, Brodsky S, Chen J. Relationships between caveolae and eNOS: everything in proximity and the proximity of everything. Am J Physiol Renal Physiol 2002; 283:1 - 10
  • Vakkala M, Kahlos K, Lakari E, Paakko P, Kinnula V, Soini Y. Inducible nitric oxide synthase expression, apoptosis and angiogenesis in in situ and invasive breast carcinomas. Clin Cancer Res 2000; 6:2408 - 2416
  • Haynes CM, Titus EA, Cooper AA. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol Cell 2004; 15:767 - 776
  • Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants and aging. Cell 2005; 120:483 - 495
  • Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 2000; 279:1005 - 1028
  • Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 1998; 95:11715 - 11720
  • Sandau KB, Fandrey J, Brune B. Accumulation of HIF-1alpha under the influence of nitric oxide. Blood 2001; 97:1009 - 1015
  • Palmer LA, Gaston B, Johns RA. Normoxic stabilization of hypoxia-inducible factor-1 expression and activity: redox-dependent effect of nitrogen oxides. Mol Pharmacol 2000; 58:1197 - 1203
  • Berridge MV, Tan AS. Effects of mitochondrial gene deletion on tumorigenicity of metastatic melanoma: Reassessing the Warburg effect. Rejuvenation Res 2010; 13:139 - 141
  • Pavlides S, Tsirigos A, Vera I, Flomenberg N, Frank PG, Casimiro MC, et al. Transcriptional evidence for the “Reverse Warburg Effect” in human breast cancer tumor stroma and metastasis: Similarities with oxidative stress, inflammation, Alzheimer's disease and “Neuron-Glia Metabolic Coupling”. Aging (Albany NY) 2010; 2:185 - 199
  • 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
  • Batandier C, Guigas B, Detaille D, El-Mir MY, Fontaine E, Rigoulet M, et al. The ROS production induced by a reverse-electron flux at respiratory-chain complex 1 is hampered by metformin. J Bioenerg Biomembr 2006; 38:33 - 42
  • Morales AI, Detaille D, Prieto M, Puente A, Briones E, Arevalo M, et al. Metformin prevents experimental gentamicin-induced nephropathy by a mitochondria-dependent pathway. Kidney Int 2010; 77:861 - 869
  • Wang X, Allen TD, May RJ, Lightfoot S, Houchen CW, Huycke MM. Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer Res 2008; 68:9909 - 9917
  • Bae JY, Ahn SJ, Han W, Noh DY. Peroxiredoxin I and II inhibit H2O2-induced cell death in MCF-7 cell lines. J Cell Biochem 2007; 101:1038 - 1045
  • Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008; 452:230 - 233
  • Morris ME, Felmlee MA. Overview of the proton-coupled MCT (SLC16A) family of transporters: Characterization, function and role in the transport of the drug of abuse gamma-hydroxybutyric acid. Aaps J 2008; 10:311 - 321
  • Garcia-Cardena G, Fan R, Stern DF, Liu J, Sessa WC. Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem 1996; 271:27237 - 27240
  • Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, et al. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 2001; 276:38121 - 38138
  • Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE, Chumakov PM. The antioxidant function of the p53 tumor suppressor. Nat Med 2005; 11:1306 - 1313
  • Gao P, Zhang H, Dinavahi R, Li F, Xiang Y, Raman V, et al. HIF-dependent antitumorigenic effect of antioxidants in vivo. Cancer Cell 2007; 12:230 - 238
  • Hirsch HA, Iliopoulos D, Tsichlis PN, Struhl K. Metformin selectively targets cancer stem cells, and acts together with chemotherapy to block tumor growth and prolong remission. Cancer Res 2009; 69:7507 - 7511
  • Zakikhani M, Dowling R, Fantus IG, Sonenberg N, Pollak M. Metformin is an AMP kinase-dependent growth inhibitor for breast cancer cells. Cancer Res 2006; 66:10269 - 10273
  • Bodmer M, Meier C, Krahenbuhl S, Jick SS, Meier CR, Meier CR. Long-term metformin use is associated with decreased risk of breast cancer. Diabetes Care 2010; 33:1304 - 1308
  • Dakhova O, Ozen M, Creighton CJ, Li R, Ayala G, Rowley D, Ittmann M. Global gene expression analysis of reactive stroma in prostate cancer. Clin Cancer Res 2009; 15:3979 - 3989
  • Pavlides S, Tsirigos A, Vera I, Flomenberg N, Frank PG, Casimiro MC, et al. Loss of stromal Caveolin-1 leads to oxidative stress, mimics hypoxia and drives inflammation in the tumor microenvironment, conferring the “Reverse Warburg Effect”: A transcriptional informatics analysis with validation. Cell Cycle 2010; 9:2201 - 2219
  • Ottesen GL. Carcinoma in situ of the female breast: A clinico-pathological, immunohistological and DNA ploidy study. APMIS 2003; 1 - 67
  • Gnant MF, Blijham GH, Reiner A, Schemper M, Reynders M, Schutte B, et al. Aneuploidy fraction but not DNA index is important for the prognosis of patients with stage I and II breast cancer—10-year results. Ann Oncol 1993; 4:643 - 650
  • Frezza C, Gottlieb E. Mitochondria in cancer: not just innocent bystanders. Semin Cancer Biol 2009; 19:4 - 11
  • Benard G, Rossignol R. Ultrastructure of the mitochondrion and its bearing on function and bioenergetics. Antioxid Redox Signal 2008; 10:1313 - 1342
  • Melov S, Schneider JA, Day BJ, Hinerfeld D, Coskun P, Mirra SS, et al. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet 1998; 18:159 - 163
  • Ugalde C, Janssen RJ, van den Heuvel LP, Smeitink JA, Nijtmans LG. Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. Hum Mol Genet 2004; 13:659 - 667
  • Pitkanen S, Robinson BH. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J Clin Invest 1996; 98:345 - 351
  • Chen ZX, Velaithan R, Pervaiz S. mitoEnergetics and cancer cell fate. Biochim Biophys Acta 2009; 1787:462 - 467
  • Bogaert YE, Rosenthal RE, Fiskum G. Postischemic inhibition of cerebral cortex pyruvate dehydrogenase. Free Radic Biol Med 1994; 16:811 - 820
  • Wang J, Ying G, Wang J, Jung Y, Lu J, Zhu J, et al. Characterization of phosphoglycerate kinase-1 expression of stromal cells derived from tumor microenvironment in prostate cancer progression. Cancer Res 2010; 70:471 - 480
  • Sonveaux P, Vegran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 2008; 118:3930 - 3942
  • Gstraunthaler G, Seppi T, Pfaller W. Impact of culture conditions, culture media volumes and glucose content on metabolic properties of renal epithelial cell cultures: Are renal cells in tissue culture hypoxic?. Cell Physiol Biochem 1999; 9:150 - 172
  • Seemayer TA, Lagace R, Schurch W, Tremblay G. Myofibroblasts in the stroma of invasive and metastatic carcinoma: A possible host response to neoplasia. Am J Surg Pathol 1979; 3:525 - 533
  • Ozzello L. Ultrastructure of the human mammary gland. Pathol Annu 1971; 6:1 - 59
  • Ge L, Meng W, Zhou H, Bhowmick N. Could stroma contribute to field cancerization?. Med Hypotheses 2010; 75:26 - 31
  • Nonn L, Ananthanarayanan V, Gann PH. Evidence for field cancerization of the prostate. Prostate 2009; 69:1470 - 1479
  • Heaphy CM, Bisoffi M, Fordyce CA, Haaland CM, Hines WC, Joste NE, et al. Telomere DNA content and allelic imbalance demonstrate field cancerization in histologically normal tissue adjacent to breast tumors. Int J Cancer 2006; 119:108 - 116
  • Hockel M, Dornhofer N. The hydra phenomenon of cancer: Why tumors recur locally after microscopically complete resection. Cancer Res 2005; 65:2997 - 3002
  • Izawa T, Obara T, Tanno S, Mizukami Y, Yanagawa N, Kohgo Y. Clonality and field cancerization in intraductal papillary-mucinous tumors of the pancreas. Cancer 2001; 92:1807 - 1817
  • Hong CC, Ambrosone CB, Ahn J, Choi JY, McCullough ML, Stevens VL, et al. Genetic variability in iron-related oxidative stress pathways (Nrf2, NQ01, NOS3 and HO-1), iron intake and risk of postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev 2007; 16:1784 - 1794
  • Yang J, Ambrosone CB, Hong CC, Ahn J, Rodriguez C, Thun MJ, et al. Relationships between polymorphisms in NOS3 and MPO genes, cigarette smoking and risk of post-menopausal breast cancer. Carcinogenesis 2007; 28:1247 - 1253
  • Karihtala P, Winqvist R, Syvaoja JE, Kinnula VL, Soini Y. Increasing oxidative damage and loss of mismatch repair enzymes during breast carcinogenesis. Eur J Cancer 2006; 42:2653 - 2659
  • Nakamura Y, Yasuoka H, Tsujimoto M, Yoshidome K, Nakahara M, Nakao K, et al. Nitric oxide in breast cancer: Induction of vascular endothelial growth factor-C and correlation with metastasis and poor prognosis. Clin Cancer Res 2006; 12:1201 - 1207
  • Karihtala P, Kinnula VL, Soini Y. Antioxidative response for nitric oxide production in breast carcinoma. Oncol Rep 2004; 12:755 - 759
  • Samoszu M, Brennan ML, To V, Leonor L, Zheng L, Fu X, et al. Association between nitrotyrosine levels and microvascular density in human breast cancer. Breast Cancer Res Treat 2002; 74:271 - 278
  • Reliene R, Schiestl RH. Antioxidant N-acetyl cysteine reduces incidence and multiplicity of lymphoma in Atm deficient mice. DNA Repair (Amst) 2006; 5:852 - 859
  • Reliene R, Schiestl RH. Antioxidants suppress lymphoma and increase longevity in Atm-deficient mice. J Nutr 2007; 137:229 - 232
  • Reliene R, Fischer E, Schiestl RH. Effect of N-acetyl cysteine on oxidative DNA damage and the frequency of DNA deletions in atm-deficient mice. Cancer Res 2004; 64:5148 - 5153
  • Reliene R, Schiestl RH. Glutathione depletion by buthionine sulfoximine induces DNA deletions in mice. Carcinogenesis 2006; 27:240 - 244
  • Martin KR, Saulnier MJ, Kari FW, Barrett JC, French JE. Timing of supplementation with the antioxidant N-acetyl-L-cysteine reduces tumor multiplicity in novel, cancer-prone p53 haploinsufficient Tg.AC (v-Ha-ras) transgenic mice but has no impact on malignant progression. Nutr Cancer 2002; 43:59 - 66
  • Andrade SP, Hart IR, Piper PJ. Inhibitors of nitric oxide synthase selectively reduce flow in tumor-associated neovasculature. Br J Pharmacol 1992; 107:1092 - 1095
  • Orucevic A, Lala PK. NG-nitro-L-arginine methyl ester, an inhibitor of nitric oxide synthesis, ameliorates interleukin 2-induced capillary leakage and reduces tumour growth in adenocarcinoma-bearing mice. Br J Cancer 1996; 73:189 - 196
  • Yamamoto T, Terada N, Nishizawa Y, Tanaka H, Akedo H, Seiyama A, et al. Effects of NG-nitro-L-arginine and/or L-arginine on experimental pulmonary metastasis in mice. Cancer Lett 1994; 87:115 - 120
  • Iwasaki T, Higashiyama M, Kuriyama K, Sasaki A, Mukai M, Shinkai K, et al. NG-nitro-L-arginine methyl ester inhibits bone metastasis after modified intracardiac injection of human breast cancer cells in a nude mouse model. Jpn J Cancer Res 1997; 88:861 - 866
  • Gallo O, Masini E, Morbidelli L, Franchi A, Fini-Storchi I, Vergari WA, et al. Role of nitric oxide in angiogenesis and tumor progression in head and neck cancer. J Natl Cancer Inst 1998; 90:587 - 596
  • Wang R, Ghahary A, Shen YJ, Scott PG, Tredget EE. Human dermal fibroblasts produce nitric oxide and express both constitutive and inducible nitric oxide synthase isoforms. J Invest Dermatol 1996; 106:419 - 427
  • Schaffer MR, Efron PA, Thornton FJ, Klingel K, Gross SS, Barbul A. Nitric oxide, an autocrine regulator of wound fibroblast synthetic function. J Immunol 1997; 158:2375 - 2381
  • Cobbold CA. The role of nitric oxide in the formation of keloid and hypertrophic lesions. Med Hypotheses 2001; 57:497 - 502
  • Cobbold CA, Sherratt JA. Mathematical modelling of nitric oxide activity in wound healing can explain keloid and hypertrophic scarring. J Theor Biol 2000; 204:257 - 288
  • Frank S, Kampfer H, Wetzler C, Pfeilschifter J. Nitric oxide drives skin repair: Novel functions of an established mediator. Kidney Int 2002; 61:882 - 888
  • Zhao R, Guan DW, Lu B. [Immunohistochemical study on expression of iNOS and eNOS during skin incised wound healing in mice ]. Fa Yi Xue Za Zhi 2005; 21:161 - 164
  • Ushio-Fukai M, Zafari AM, Fukui T, Ishizaka N, Griendling KK. p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem 1996; 271:23317 - 23321
  • Knudsen ES, Buckmaster C, Chen TT, Feramisco JR, Wang JY. Inhibition of DNA synthesis by RB: Effects on G1/S transition and S-phase progression. Genes Dev 1998; 12:2278 - 2292