217
Views
9
CrossRef citations to date
0
Altmetric
ORIGINAL ARTICLE

Loss of p53 in stromal fibroblasts enhances tumor cell proliferation through nitric-oxide-mediated cyclooxygenase 2 activation

, , , , , , & show all
Pages 269-278 | Received 05 Sep 2014, Accepted 07 Dec 2014, Published online: 09 Feb 2015

References

  • Gupta RA, Dubois RN. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat Rev Cancer 2001;1:11–21.
  • Singh S, Gupta AK. Nitric oxide: role in tumour biology and iNOS/NO-based anticancer therapies. Cancer Chemother Pharmacol 2011;67:1211–1224.
  • Lowe SW, Cepero E, Evan G. Intrinsic tumour suppression. Nature 2004;432:307–315.
  • Murata M, Thanan R, Ma N, Kawanishi S. Role of nitrative and oxidative DNA damage in inflammation-related carcinogenesis. J Biomed Biotechnol 2012;2012:623019.
  • Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012;2012:948098.
  • Meek DW. Tumour suppression by p53: a role for the DNA damage response? Nat Rev Cancer 2009;9:714–723.
  • Levine AJ, Momand J, Finlay CA. The p53 tumour suppressor gene. Nature 1991;351:453–456.
  • Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991;253:49–53.
  • Munro AJ, Lain S, Lane DP. P53 abnormalities and outcomes in colorectal cancer: a systematic review. Br J Cancer 2005; 92:434–444.
  • Adegboyega PA, Ololade O, Saada J, Mifflin R, Di Mari JF, Powell DW. Subepithelial myofibroblasts express cyclooxygenase-2 in colorectal tubular adenomas. Clin Cancer Res 2004; 10:5870–5879.
  • Liu Q, Chan STF, Mahendran R. Nitric oxide induces cyclooxygenase expression and inhibits cell growth in colon cancer cell lines. Carcinogenesis 2003;24:637–642.
  • Davel L, D’Agostino A, Espanol A, Jasnis MA, Lauria de Cidre L, de Lustig ES, Sales ME. Nitric oxide synthase-cyclooxygenase interactions are involved in tumor cell angiogenesis and migration. J Biol Regul Homeost Agents 2002; 16:181–189.
  • Kisley LR, Barrett BS, Bauer AK, Dwyer-Nield LD, Barthel B, Meyer AM, et al. Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res 2002;62:6850–6856.
  • Connelly L, Palacios-Callender M, Ameixa C, Moncada S, Hobbs AJ. Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 2001;166:3873–3881.
  • Duarte ML, de Moraes E, Pontes E, Schluckebier L, de Moraes JL, Hainaut P, Ferreira CG. Role of p53 in the induction of cyclooxygenase-2 by cisplatin or paclitaxel in non-small cell lung cancer cell lines. Cancer Lett 2009;279:57–64.
  • Han JA, Kim JI, Ongusaha PP, Hwang DH, Ballou LR, Mahale A, et al. P53-mediated induction of Cox-2 counteracts p53- or genotoxic stress-induced apoptosis. EMBO J 2002; 21:5635–5644.
  • Subbaramaiah K, Altorki N, Chung WJ, Mestre JR, Sampat A, Dannenberg AJ. Inhibition of cyclooxygenase-2 gene expression by p53. J Biol Chem 1999;274:10911–10915.
  • Kawabe A, Shimada Y, Uchida S, Maeda M, Sato F, Itami A, Imamura M. Expression of cyclooxygenase-2 is associated with carcinogenesis of the lower part of thoracic esophageal squamous cell carcinoma and p53 expression. Oncology 2002; 62:46–54.
  • Ristimaki A, Sivula A, Lundin J, Lundin M, Salminen T, Haglund C, et al. Prognostic significance of elevated cyclooxygenase-2 expression in breast cancer. Cancer Res 2002;62: 632–635.
  • Goulart Filho JA, Nonaka CF, da Costa Miguel MC, de Almeida Freitas R, Galvao HC. Immunoexpression of cyclooxygenase-2 and p53 in oral squamous cell carcinoma. Am J Otolaryngol 2009;30:89–94.
  • Lim SC, Lee TB, Choi CH, Ryu SY, Kim KJ, Min YD. Expression of cyclooxygenase-2 and its relationship to p53 accumulation in colorectal cancers. Yonsei Med J 2007;48: 495–501.
  • Niki T, Kohno T, Iba S, Moriya Y, Takahashi Y, Saito M, et al. Frequent co-localization of Cox-2 and laminin-5 gamma2 chain at the invasive front of early-stage lung adenocarcinomas. Am J Pathol 2002;160:1129–1141.
  • Forrester K, Ambs S, Lupold SE, Kapust RB, Spillare EA, Weinberg WC, et al. Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53. Proc Natl Acad Sci U S A 1996;93: 2442–2447.
  • Schneiderhan N, Budde A, Zhang Y, Brune B. Nitric oxide induces phosphorylation of p53 and impairs nuclear export. Oncogene 2003;22:2857–2868.
  • Cook T, Wang Z, Alber S, Liu K, Watkins SC, Vodovotz Y, et al. Nitric oxide and ionizing radiation synergistically promote apoptosis and growth inhibition of cancer by activating p53. Cancer Res 2004;64:8015–8021.
  • Goodman JE, Hofseth LJ, Hussain SP, Harris CC. Nitric oxide and p53 in cancer-prone chronic inflammation and oxyradical overload disease. Environ Mol Mutagen 2004;44:3–9.
  • Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6:392–401.
  • Ko SC, Chapple KS, Hawcroft G, Coletta PL, Markham AF, Hull MA. Paracrine cyclooxygenase-2-mediated signalling by macrophages promotes tumorigenic progression of intestinal epithelial cells. Oncogene 2002;21:7175–7186.
  • Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA, et al. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 1997;91:649–659.
  • Tatemichi M, Tazawa H, Masuda M, Saleem M, Wada S, Donehower LA, et al. Suppression of thymic lymphomas and increased nonthymic lymphomagenesis in Trp53-deficient mice lacking inducible nitric oxide synthase gene. Int J Cancer 2004;111:819–828.
  • Tatemichi M, Hata H, Tazawa H, Nakadate T. Lipopolysaccharide induces aberrant hypermethylation of Hic-1 in mouse embryonic fibroblasts lacking p53 gene. Anticancer Res 2008; 28:2101–2108.
  • Tazawa H, Tatemichi M, Sawa T, Gilibert I, Ma N, Hiraku Y, et al. Oxidative and nitrative stress caused by subcutaneous implantation of a foreign body accelerates sarcoma development in Trp53+/− mice. Carcinogenesis 2007;28:191–198.
  • Wang D, Dubois RN. Eicosanoids and cancer. Nat Rev Cancer 2010;10:181–193.
  • Wang D, Wang H, Shi Q, Katkuri S, Walhi W, Desvergne B, et al. Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator- activated receptor delta. Cancer Cell 2004;6:285–295.
  • Shao J, Sheng H, Inoue H, Morrow JD, DuBois RN. Regulation of constitutive cyclooxygenase-2 expression in colon carcinoma cells. J Biol Chem 2000;275:33951–33956.
  • Mbonye UR, Wada M, Rieke CJ, Tang HY, Dewitt DL, Smith WL. The 19-amino acid cassette of cyclooxygenase-2 mediates entry of the protein into the endoplasmic reticulum-associated degradation system. J Biol Chem 2006;281: 35770–35778.
  • Kibbe MR, Nie S, Seol DW, Kovesdi I, Lizonova A, Makaroun M, et al. Nitric oxide prevents p21 degradation with the ubiquitin-proteasome pathway in vascular smooth muscle cells. J Vasc Surg 2000;31:364–374.
  • Eliopoulos AG, Dumitru CD, Wang CC, Cho J, Tsichlis PN. Induction of COX-2 by LPS in macrophages is regulated by Tpl2-dependent CREB activation signals. EMBO J 2002; 21:4831–4840.
  • Moon Y, Pestka JJ. Vomitoxin-induced cyclooxygenase-2 gene expression in macrophages mediated by activation of ERK and p38 but not JNK mitogen-activated protein kinases. Toxicol Sci 2002;69:373–382.
  • Paterson RF, Ulbright TM, MacLennan GT, Zhang S, Pan CX, Sweeney CJ, et al. Molecular genetic alterations in the laser-capture-microdissected stroma adjacent to bladder carcinoma. Cancer 2003;98:1830–1836.
  • Fukino K, Shen L, Patocs A, Mutter GL, Eng C. Genomic instability within tumor stroma and clinicopathological characteristics of sporadic primary invasive breast carcinoma. JAMA 2007;297:2103–2111.
  • Wernert N, Locherbach C, Wellmann A, Behrens P, Hugel A. Presence of genetic alterations in microdissected stroma of human colon and breast cancers. Anticancer Res 2001;21: 2259–2264.
  • Kiaris H, Chatzistamou I, Trimis G, Frangou-Plemmenou M, Pafiti-Kondi A, Kalofoutis A. Evidence for nonautonomous effect of p53 tumor suppressor in carcinogenesis. Cancer Res 2005;65:1627–1630.
  • Addadi Y, Moskovits N, Granot D, Lozano G, Carmi Y, Apte RN, et al. p53 status in stromal fibroblasts modulates tumor growth in an SDF1-dependent manner. Cancer Res 2010;70:9650–9658.
  • Tsatsanis C, Androulidaki A, Venihaki M, Margioris AN. Signalling networks regulating cyclooxygenase-2. Int J Biochem Cell Biol 2006;38:1654–1661.
  • Cressey R, Pimpa S, Tontrong W, Watananupong O, Leartprasertsuke N. Expression of cyclooxygenase-2 in colorectal adenocarcinoma is associated with p53 accumulation and hdm2 overexpression. Cancer Lett 2006;233:232–239.
  • Asting AG, Caren H, Andersson M, Lonnroth C, Lagerstedt K, Lundholm K. COX-2 gene expression in colon cancer tissue related to regulating factors and promoter methylation status. BMC Cancer 2011;11:238.
  • Tetsuka T, Daphna-Iken D, Srivastava SK, Baier LD, DuMaine J, Morrison AR. Cross-talk between cyclooxygenase and nitric oxide pathways: prostaglandin E2 negatively modulates induction of nitric oxide synthase by interleukin 1. Proc Natl Acad Sci U S A 1994;91:12168–12172.
  • MacKenzie KF, Van Den Bosch MW, Naqvi S, Elcombe SE, McGuire VA, Reith AD, et al. MSK1 and MSK2 inhibit lipopolysaccharide-induced prostaglandin production via an interleukin-10 feedback loop. Mol Cell Biol 2013;33: 1456–1467.
  • Zaric J, Ruegg C. Integrin-mediated adhesion and soluble ligand binding stabilize COX-2 protein levels in endothelial cells by inducing expression and preventing degradation. J Biol Chem 2005;280:1077–1085.
  • Bogdan C. Nitric oxide and the regulation of gene expression. Trends Cell Biol 2001;11:66–75.
  • Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010;40:280–293.
  • Shin IY, Sung NY, Lee YS, Kwon TS, Si Y, Lee YS, et al. The expression of multiple proteins as prognostic factors in colorectal cancer: cathepsin D, p53, COX-2, epidermal growth factor receptor, C-erbB2, and Ki-27. Gut Liver 2014;8: 13–23.
  • Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, DuBois RN. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 1998;93:705–716.
  • Iniguez MA, Rodriguez A, Volpert OV, Fresno M, Redondo JM. Cyclooxygenase-2: a therapeutic target in angiogenesis. Trends Mol Med 2003;9:73–78.
  • Williams CS, Tsujii M, Reese J, Dey SK, DuBois RN. Host cyclooxygenase-2 modulates carcinoma growth. J Clin Invest 2000;105:1589–1594.
  • Yang L, Pei Z. Bacteria, inflammation, and colon cancer. World J Gastroenterol 2006;12:6741–6746.
  • Hope ME, Hold GL, Kain R, El-Omar EM. Sporadic colorectal cancer–role of the commensal microbiota. FEMS Microbiol Lett 2005;244:1–7.
  • Irrazabal T, Belcheva A, Girardin SE, Martin A, Philpott DJ. The multifaceted role of the intestinal microbiota in colon cancer. Mol Cell 2014;54:309–320.
  • Mira-Pascual L, Cabrera-Rubio R, Ocon S, Costales P, Parra A, Suarez A, et al. Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal biomarkers. J Gastroenterol 2014. Epub ahead of print.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.