Skip to main content
SpringerLink
Log in

The Role of Inflammation in Inflammatory Breast Cancer

  • Chapter
  • First Online:
Inflammation and Cancer

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 816))

Abstract

Inflammatory breast cancer (IBC) is the most aggressive form of breast cancer. Despite extensive study, whether inflammation contributes to the tumorigenicity or aggressiveness of IBC remains largely unknown. In this chapter, we will review the potential role played by inflammation in IBC based on the results of in vitro, in vivo, and patient studies. Current evidence suggests that several major inflammatory signaling pathways are constitutively active in IBC and breast cancer. Among them, the NF-κB, COX-2, and JAK/STAT signaling systems seem to play a major role in the tumorigenesis of IBC. Inflammatory molecules such as interleukin-6, tumor necrosis factor alpha (TNF-α), and gamma interferon have been shown to contribute to malignant transformation in preclinical studies of IBC, while transforming growth factor-β, interleukins 8 and 1β, as well as TNF-α appear to play a role in proliferation, survival, epithelial–mesenchymal transition, invasion, and metastasis. In this chapter, we also describe work thus far involving inhibitors of inflammation in the development of prevention and treatment strategies for IBC.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abrahamsson A, Morad V, Saarinen NM, Dabrosin C (2012) Estradiol, tamoxifen, and flaxseed alter IL-1beta and IL-1Ra levels in normal human breast tissue in vivo. J Clin Endocrinol Metab 97(11):E2044–E2054

    CAS  PubMed  Google Scholar 

  • ACS (2014) Cancer facts and figures 2014. American Cancer Society, Atlanta, GA. Accessed 25 Mar 2014

    Google Scholar 

  • Agrawal A, Fentiman IS (2008) NSAIDs and breast cancer: a possible prevention and treatment strategy. Int J Clin Pract 62(3):444–449

    CAS  PubMed  Google Scholar 

  • Ahern TP, Pedersen L, Tarp M et al (2011) Statin prescriptions and breast cancer recurrence risk: a Danish nationwide prospective cohort study. J Natl Cancer Inst 103(19):1461–1468

    CAS  PubMed Central  PubMed  Google Scholar 

  • Allin KH, Bojesen SE, Nordestgaard BG (2009) Baseline C-reactive protein is associated with incident cancer and survival in patients with cancer. J Clin Oncol: Off J Am Soc Clin Oncol 27(13):2217–2224

    CAS  Google Scholar 

  • Allin KH, Nordestgaard BG, Flyger H, Bojesen SE (2011) Elevated pre-treatment levels of plasma C-reactive protein are associated with poor prognosis after breast cancer: a cohort study. Breast Cancer Res 13(3):R55

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anderson WF, Schairer C, Chen BE, Hance KW, Levine PH (2005) Epidemiology of inflammatory breast cancer (IBC). Breast Dis 22:9–23

    PubMed Central  PubMed  Google Scholar 

  • Apte RN, Krelin Y, Song X et al (2006) Effects of micro-environment- and malignant cell-derived interleukin-1 in carcinogenesis, tumour invasiveness and tumour-host interactions. Eur J Cancer 42(6):751–759

    CAS  PubMed  Google Scholar 

  • Araki S, Eitel JA, Batuello CN et al (2010) TGF-beta1-induced expression of human Mdm2 correlates with late-stage metastatic breast cancer. J Clin Investig 120(1):290–302

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ashcroft GS (1999) Bidirectional regulation of macrophage function by TGF-beta. Microbes Infect/Ins Pasteur 1(15):1275–1282

    CAS  Google Scholar 

  • Barbieri I, Pensa S, Pannellini T et al (2010) Constitutively active Stat3 enhances neu-mediated migration and metastasis in mammary tumors via upregulation of cten. Cancer Res 70(6):2558–2567

    CAS  PubMed  Google Scholar 

  • Bichsel VE, Liotta LA, Petricoin EF 3rd (2001) Cancer proteomics: from biomarker discovery to signal pathway profiling. Cancer J 7(1):69–78

    CAS  PubMed  Google Scholar 

  • Biswas DK, Shi Q, Baily S et al (2004) NF-kappa B activation in human breast cancer specimens and its role in cell proliferation and apoptosis. Proc Natl Acad Sci USA 101(27):10137–10142

    CAS  PubMed Central  PubMed  Google Scholar 

  • Biswas S, Guix M, Rinehart C et al (2007) Inhibition of TGF-beta with neutralizing antibodies prevents radiation-induced acceleration of metastatic cancer progression. J Clin Investig 117(5):1305–1313

    CAS  PubMed Central  PubMed  Google Scholar 

  • Black S, Kushner I, Samols D (2004) C-reactive Protein. J Biol Chem 279(47):48487–48490

    CAS  PubMed  Google Scholar 

  • Bozcuk H, Uslu G, Samur M et al (2004) Tumour necrosis factor-alpha, interleukin-6, and fasting serum insulin correlate with clinical outcome in metastatic breast cancer patients treated with chemotherapy. Cytokine 27(2–3):58–65

    CAS  PubMed  Google Scholar 

  • Brewer TM, Masuda H, Iwamoto T et al (2012) Statin use and improved survival outcome in primary inflammatory breast cancer: retrospective cohort study. Paper presented at: CTRC-AACR: san antonio breast cancer symposium, 4–8 Dec 2012, San Antonio, TX

    Google Scholar 

  • Bristol IJ, Woodward WA, Strom EA et al (2008) Locoregional treatment outcomes after multimodality management of inflammatory breast cancer. Int J Radiat Oncol Biol Phys 72(2):474–484

    PubMed Central  PubMed  Google Scholar 

  • Brown JR, DuBois RN (2005) COX-2: a molecular target for colorectal cancer prevention. J Clin Oncol: Official J Am Soc Clin Oncol 23(12):2840–2855

    CAS  Google Scholar 

  • Cabioglu N, Gong Y, Islam R et al (2007) Expression of growth factor and chemokine receptors: new insights in the biology of inflammatory breast cancer. Ann Oncol: Off J Eur Soc Med Oncol/ESMO 18(6):1021–1029

    CAS  Google Scholar 

  • Casas JP, Shah T, Hingorani AD, Danesh J, Pepys MB (2008) C-reactive protein and coronary heart disease: a critical review. J Intern Med 264(4):295–314

    CAS  PubMed  Google Scholar 

  • Chakrabarti R, Subramaniam V, Abdalla S, Jothy S, Prud’homme GJ (2009) Tranilast inhibits the growth and metastasis of mammary carcinoma. Anti-Cancer Drugs 20(5):334–345

    CAS  PubMed  Google Scholar 

  • Charafe-Jauffret E, Ginestier C, Iovino F et al (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69(4):1302–1313

    CAS  PubMed Central  PubMed  Google Scholar 

  • Charafe-Jauffret E, Ginestier C, Iovino F et al (2010) Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res: Off J Am Assoc Cancer Res 16(1):45–55

    CAS  Google Scholar 

  • Chen G, Gharib TG, Huang CC et al (2002) Discordant protein and mRNA expression in lung adenocarcinomas. Mol Cell Proteomics 1(4):304–313

    CAS  PubMed  Google Scholar 

  • Cheshire JL, Baldwin AS Jr (1997) Synergistic activation of NF-kappaB by tumor necrosis factor alpha and gamma interferon via enhanced I kappaB alpha degradation and de novo I kappaB beta degradation. Mol Cell Biol 17(11):6746–6754

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clezardin P (2011) Therapeutic targets for bone metastases in breast cancer. Breast Cancer Res: BCR 13(2):207

    CAS  PubMed Central  PubMed  Google Scholar 

  • Criswell TL, Dumont N, Barnett JV, Arteaga CL (2008) Knockdown of the transforming growth factor-beta type III receptor impairs motility and invasion of metastatic cancer cells. Cancer Res 68(18):7304–7312

    CAS  PubMed  Google Scholar 

  • D’Anello L, Sansone P, Storci G et al (2010) Epigenetic control of the basal-like gene expression profile via Interleukin-6 in breast cancer cells. Mol Cancer 9:300

    PubMed Central  PubMed  Google Scholar 

  • Dawood S, Merajver SD, Viens P et al (2011) International expert panel on inflammatory breast cancer: consensus statement for standardized diagnosis and treatment. Ann Oncol: Official J Eur Soc Med Oncol/ESMO 22(3):515–523

    CAS  Google Scholar 

  • de Jong JS, van Diest PJ, van der Valk P, Baak JP (1998) Expression of growth factors, growth-inhibiting factors, and their receptors in invasive breast cancer. II: Correlations with proliferation and angiogenesis. J Pathol 184(1):53–57

    PubMed  Google Scholar 

  • Derynck R, Akhurst RJ, Balmain A (2001) TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 29(2):117–129

    CAS  PubMed  Google Scholar 

  • Diaz N, Minton S, Cox C et al (2006) Activation of stat3 in primary tumors from high-risk breast cancer patients is associated with elevated levels of activated SRC and survivin expression. Clin Cancer Res: Off J Am Assoc Cancer Res 12(1):20–28

    CAS  Google Scholar 

  • Docherty NG, O’Sullivan OE, Healy DA et al (2006) TGF-beta1-induced EMT can occur independently of its proapoptotic effects and is aided by EGF receptor activation. Am J Physiol: Ren Physiol 290(5):F1202–F1212

    CAS  Google Scholar 

  • Duda DG, Kozin SV, Kirkpatrick ND, Xu L, Fukumura D, Jain RK (2011) CXCL12 (SDF1alpha)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies? Clin Cancer Res: Off J Am Assoc Cancer Res 17(8):2074–2080

    CAS  Google Scholar 

  • Dunning AM, Ellis PD, McBride S et al (2003) A transforming growth factorbeta1 signal peptide variant increases secretion in vitro and is associated with increased incidence of invasive breast cancer. Cancer Res 63(10):2610–2615

    CAS  PubMed  Google Scholar 

  • El-Shinawi M, Mohamed HT, El-Ghonaimy EA et al (2013) Human cytomegalovirus infection enhances NF-kappaB/p65 signaling in inflammatory breast cancer patients. PLoS ONE 8(2):e55755

    CAS  PubMed Central  PubMed  Google Scholar 

  • Franco-Barraza J, Valdivia-Silva JE, Zamudio-Meza H et al (2010) Actin cytoskeleton participation in the onset of IL-1beta induction of an invasive mesenchymal-like phenotype in epithelial MCF-7 cells. Arch Med Res 41(3):170–181

    CAS  PubMed  Google Scholar 

  • Freund A, Chauveau C, Brouillet JP et al (2003) IL-8 expression and its possible relationship with estrogen-receptor-negative status of breast cancer cells. Oncogene 22(2):256–265

    CAS  PubMed Central  PubMed  Google Scholar 

  • Freund A, Jolivel V, Durand S et al (2004) Mechanisms underlying differential expression of interleukin-8 in breast cancer cells. Oncogene 23(36):6105–6114

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gabay C, Kushner I (1999) Acute-phase proteins and other systemic responses to inflammation. New Engl J Med 340(6):448–454

    CAS  PubMed  Google Scholar 

  • Garcia R, Yu CL, Hudnall A et al (1997) Constitutive activation of Stat3 in fibroblasts transformed by diverse oncoproteins and in breast carcinoma cells. Cell Growth Differ: Mol Biol J Am Assoc Cancer Res 8(12):1267–1276

    CAS  Google Scholar 

  • Garcia-Tunon I, Ricote M, Ruiz A, Fraile B, Paniagua R, Royuela M (2005) IL-6, its receptors and its relationship with bcl-2 and bax proteins in infiltrating and in situ human breast carcinoma. Histopathology 47(1):82–89

    CAS  PubMed  Google Scholar 

  • Ginestier C, Liu S, Diebel ME et al (2010) CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Investig 120(2):485–497

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gloire G, Dejardin E, Piette J (2006) Extending the nuclear roles of IkappaB kinase subunits. Biochem Pharmacol 72(9):1081–1089

    CAS  PubMed  Google Scholar 

  • Goel A, Aggarwal BB (2010) Curcumin, the golden spice from Indian saffron, is a chemosensitizer and radiosensitizer for tumors and chemoprotector and radioprotector for normal organs. Nutr Cancer 62(7):919–930

    CAS  PubMed  Google Scholar 

  • Goldberg JE, Schwertfeger KL (2010) Proinflammatory cytokines in breast cancer: mechanisms of action and potential targets for therapeutics. Curr Drug Targets 11(9):1133–1146

    CAS  PubMed  Google Scholar 

  • Graham DJ, Campen D, Hui R et al (2005) Risk of acute myocardial infarction and sudden cardiac death in patients treated with cyclo-oxygenase 2 selective and non-selective non-steroidal anti-inflammatory drugs: nested case-control study. Lancet 365(9458):475–481

    CAS  PubMed  Google Scholar 

  • Greenfield JP, Cobb WS, Lyden D (2010) Resisting arrest: a switch from angiogenesis to vasculogenesis in recurrent malignant gliomas. J Clin Investig 120(3):663–667

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guerin M, Gabillot M, Mathieu MC et al (1989) Structure and expression of c-erbB-2 and EGF receptor genes in inflammatory and non-inflammatory breast cancer: prognostic significance. Int J Cancer: J Int du Cancer 43(2):201–208

    CAS  Google Scholar 

  • Haagensen C (1971) Diseases of the breast, 2nd edn. Saunders, Philadelphia

    Google Scholar 

  • Hagedorn HG, Bachmeier BE, Nerlich AG (2001) Synthesis and degradation of basement membranes and extracellular matrix and their regulation by TGF-beta in invasive carcinomas (review). Int J Oncol 18(4):669–681

    CAS  PubMed  Google Scholar 

  • Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57–70

    CAS  PubMed  Google Scholar 

  • Hance KW, Anderson WF, Devesa SS, Young HA, Levine PH (2005) Trends in inflammatory breast carcinoma incidence and survival: the surveillance, epidemiology, and end results program at the National Cancer Institute. J Natl Cancer Inst 97(13):966–975

    PubMed Central  PubMed  Google Scholar 

  • Hartman ZC, Yang XY, Glass O et al (2011) HER2 overexpression elicits a proinflammatory IL-6 autocrine signaling loop that is critical for tumorigenesis. Cancer Res 71(13):4380–4391

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132(3):344–362

    CAS  PubMed  Google Scholar 

  • Health NIo (2001) APRiCOT-B: Study to Evaluate Apricoxib in Combination With Lapatinib and Capecitabine in the Treatment of HER2/Neu+ Breast Cancer (TP2001-202). http://clinicaltrials.gov/show/NCT00657137. Accessed on 4 Apr 2013

  • Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374(Pt 1):1–20

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hinohara K, Gotoh N (2010) Inflammatory signaling pathways in self-renewing breast cancer stem cells. Curr Opin Pharmacol 10(6):650–654

    CAS  PubMed  Google Scholar 

  • Hirschfield GM, Pepys MB (2003) C-reactive protein and cardiovascular disease: new insights from an old molecule. QJM: Monthly J Assoc Phys 96(11):793–807

    CAS  Google Scholar 

  • Hodge DR, Peng B, Cherry JC et al (2005) Interleukin 6 supports the maintenance of p53 tumor suppressor gene promoter methylation. Cancer Res 65(11):4673–4682

    CAS  PubMed  Google Scholar 

  • Howe LR (2007) Inflammation and breast cancer, cyclooxygenase/prostaglandin signaling and breast cancer. Breast Cancer Res: BCR 9(4):210

    PubMed Central  PubMed  Google Scholar 

  • Howe LR, Subbaramaiah K, Brown AM, Dannenberg AJ (2001) Cyclooxygenase-2: a target for the prevention and treatment of breast cancer. Endocr Relat Cancer 8(2):97–114

    CAS  PubMed  Google Scholar 

  • Howe LR, Subbaramaiah K, Patel J et al (2002) Celecoxib, a selective cyclooxygenase 2 inhibitor, protects against human epidermal growth factor receptor 2 (HER-2)/neu-induced breast cancer. Cancer Res 62(19):5405–5407

    CAS  PubMed  Google Scholar 

  • Howe LR, Chang SH, Tolle KC et al (2005) HER2/neu-induced mammary tumorigenesis and angiogenesis are reduced in cyclooxygenase-2 knockout mice. Cancer Res 65(21):10113–10119

    CAS  PubMed  Google Scholar 

  • Iliopoulos D, Hirsch HA, Struhl K (2009) An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 139(4):693–706

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K (2010) STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 39(4):493–506

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iliopoulos D, Hirsch HA, Wang G, Struhl K (2011) Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci USA 108(4):1397–1402

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ivanovic V, Dedovic-Tanic N, Milovanovic Z et al (2009) Quantification of transforming growth factor beta 1 levels in metastatic axillary lymph node tissue extracts from breast cancer patients: a new specimen source. Anal Quant Cytol Histol/Int Acad Cytol Am Soc Cytol 31(5):288–295

    Google Scholar 

  • Jablonska E, Kiluk M, Markiewicz W, Piotrowski L, Grabowska Z, Jablonski J (2001) TNF-alpha, IL-6 and their soluble receptor serum levels and secretion by neutrophils in cancer patients. Arch Immunologiae et Ther Exp 49(1):63–69

    CAS  Google Scholar 

  • Jain MK, Ridker PM (2005) Anti-inflammatory effects of statins: clinical evidence and basic mechanisms Nature reviews. Drug Discov 4(12):977–987

    CAS  Google Scholar 

  • Jaiyesimi IA, Buzdar AU, Hortobagyi G (1992) Inflammatory breast cancer: a review. J Clin Oncol: Off J Am Soc Clin Oncol 10(6):1014–1024

    CAS  Google Scholar 

  • Jiang XP, Yang DC, Elliott RL, Head JF (2000) Reduction in serum IL-6 after vacination of breast cancer patients with tumour-associated antigens is related to estrogen receptor status. Cytokine 12(5):458–465

    CAS  PubMed  Google Scholar 

  • Jones RL, Giembycz MA, Woodward DF (2009) Prostanoid receptor antagonists: development strategies and therapeutic applications. Br J Pharmacol 158(1):104–145

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ma LZ, Walgren B, Clayton RA, Burkholder JR (2011) T.P. LY2784544, a small molecule JAK2 inhibitor, induces apoptosis in inflammatory breast cancer spheres through targeting IL-6-JAK-STAT3 pathway. Paper presented at: Proceedings of the annual meeting of the American Association for Cancer Research; 2–6 Apr 2011, Orlando

    Google Scholar 

  • Kaklamani VG, Hou N, Bian Y et al (2003) TGFBR1*6A and cancer risk: a meta-analysis of seven case-control studies. J Clin Oncol: Off J Am Soc Clin Oncol 21(17):3236–3243

    CAS  Google Scholar 

  • Kalaitzidis D, Gilmore TD (2005) Transcription factor cross-talk: the estrogen receptor and NF-kappaB. Trends Endocrinology and Metabolism: TEM 16(2):46–52

    CAS  Google Scholar 

  • Kallioniemi OP, Holli K, Visakorpi T, Koivula T, Helin HH, Isola JJ (1991) Association of c-erbB-2 protein over-expression with high rate of cell proliferation, increased risk of visceral metastasis and poor long-term survival in breast cancer. I J Cancer: J Int du Cancer 49(5):650–655

    CAS  Google Scholar 

  • Kan CY, Iacopetta BJ, Lawson JS, Whitaker NJ (2005) Identification of human papillomavirus DNA gene sequences in human breast cancer. Br J Cancer 93(8):946–948

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kendellen MF, Bradford JW, Lawrence CL, Clark KS, Baldwin AS (2013) Canonical and non-canonical NF-kappaB signaling promotes breast cancer tumor-initiating cells. Oncogene, 11 Mar 2013

    Google Scholar 

  • Kesson EM, Allardice GM, George WD, Burns HJ, Morrison DS (2012) Effects of multidisciplinary team working on breast cancer survival: retrospective, comparative, interventional cohort study of 13,722 women. BMJ 344:e2718

    PubMed Central  PubMed  Google Scholar 

  • Kozlowski L, Zakrzewska I, Tokajuk P, Wojtukiewicz MZ (2003) Concentration of interleukin-6 (IL-6), interleukin-8 (IL-8) and interleukin-10 (IL-10) in blood serum of breast cancer patients. Rocz Akad Med Bialymst 48:82–84

    CAS  PubMed  Google Scholar 

  • Kunigal S, Lakka SS, Sodadasu PK, Estes N, Rao JS (2009) Stat3-siRNA induces Fas-mediated apoptosis in vitro and in vivo in breast cancer. Int J Oncol 34(5):1209–1220

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lanza-Jacoby S, Miller S, Flynn J et al (2003) The cyclooxygenase-2 inhibitor, celecoxib, prevents the development of mammary tumors in Her-2/neu mice. Cancer Epidemiol Biomarkers Prev 12(12):1486–1491

    CAS  PubMed  Google Scholar 

  • Lei X, Bandyopadhyay A, Le T, Sun L (2002) Autocrine TGFbeta supports growth and survival of human breast cancer MDA-MB-231 cells. Oncogene 21(49):7514–7523

    CAS  PubMed  Google Scholar 

  • Lerebours F, Vacher S, Andrieu C et al (2008) NF-kappa B genes have a major role in inflammatory breast cancer. BMC Cancer 8:41

    PubMed Central  PubMed  Google Scholar 

  • Li J, Gonzalez-Angulo AM, Allen PK et al (2011) Triple-negative subtype predicts poor overall survival and high locoregional relapse in inflammatory breast cancer. Oncologist 16(12):1675–1683

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin Y, Huang R, Chen L et al (2004) Identification of interleukin-8 as estrogen receptor-regulated factor involved in breast cancer invasion and angiogenesis by protein arrays. Int J Cancer. J Int du Cancer 109(4):507–515

    CAS  Google Scholar 

  • Liu CH, Chang SH, Narko K et al (2001) Overexpression of cyclooxygenase-2 is sufficient to induce tumorigenesis in transgenic mice. J Biol Chem 276(21):18563–18569

    CAS  PubMed  Google Scholar 

  • Liu Y, Wang L, Lin XY et al (2012) Anti-apoptotic effect of claudin-1 on TNF-alpha-induced apoptosis in human breast cancer MCF-7 cells. Tumour Biol 33(6):2307–2315

    CAS  PubMed  Google Scholar 

  • Lyons TR, O’Brien J, Borges VF et al (2011) Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat Med 17(9):1109–1115

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martin OA, Redon CE, Dickey JS, Nakamura AJ, Bonner WM (2011) Para-inflammation mediates systemic DNA damage in response to tumor growth. Communicative Integr Biol 4(1):78–81

    CAS  Google Scholar 

  • Matsumoto G, Namekawa J, Muta M et al (2005) Targeting of nuclear factor kappaB Pathways by dehydroxymethylepoxyquinomicin, a novel inhibitor of breast carcinomas: antitumor and antiangiogenic potential in vivo. Clin Cancer Res 11(3):1287–1293

    CAS  PubMed  Google Scholar 

  • Matthews JR, Watson SM, Tevendale MC, Watson CJ, Clarke AR (2007) Caspase-dependent proteolytic cleavage of STAT3alpha in ES cells, in mammary glands undergoing forced involution and in breast cancer cell lines. BMC Cancer 7:29

    PubMed Central  PubMed  Google Scholar 

  • Menter DG, Schilsky RL, DuBois RN (2010) Cyclooxygenase-2 and cancer treatment: understanding the risk should be worth the reward. Clinical Cancer Res 16(5):1384–1390

    CAS  Google Scholar 

  • Moody CA, Laimins LA (2009) Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog 5(10):e1000605

    PubMed Central  PubMed  Google Scholar 

  • Moustakas A, Heldin CH (2007) Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 98(10):1512–1520

    CAS  PubMed  Google Scholar 

  • Muraoka-Cook RS, Kurokawa H, Koh Y et al (2004) Conditional overexpression of active transforming growth factor beta1 in vivo accelerates metastases of transgenic mammary tumors. Cancer Res 64(24):9002–9011

    CAS  PubMed  Google Scholar 

  • Murohashi M, Hinohara K, Kuroda M et al (2010) Gene set enrichment analysis provides insight into novel signalling pathways in breast cancer stem cells. Br J Cancer 102(1):206–212

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ Jr, Sledge GW Jr (1997) Constitutive activation of NF-kappaB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 17(7):3629–3639

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nielsen SF, Nordestgaard BG, Bojesen SE (2012) Statin use and reduced cancer-related mortality. New Engl J Med 367(19):1792–1802

    CAS  PubMed  Google Scholar 

  • Nishimura R, Nagao K, Miyayama H et al (2000) An analysis of serum interleukin-6 levels to predict benefits of medroxyprogesterone acetate in advanced or recurrent breast cancer. Oncology 59(2):166–173

    CAS  PubMed  Google Scholar 

  • Oshima M, Dinchuk JE, Kargman SL et al (1996) Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87(5):803–809

    CAS  PubMed  Google Scholar 

  • Pan Q, Kleer CG, van Golen KL et al (2002) Copper deficiency induced by tetrathiomolybdate suppresses tumor growth and angiogenesis. Cancer Res 62(17):4854–4859

    CAS  PubMed  Google Scholar 

  • Pan Q, Bao LW, Merajver SD (2003) Tetrathiomolybdate inhibits angiogenesis and metastasis through suppression of the NFkappaB signaling cascade. Mol Cancer Res 1(10):701–706

    CAS  PubMed  Google Scholar 

  • Pasche B, Kaklamani V, Hou N et al (2004) TGFBR1*6A and cancer: a meta-analysis of 12 case-control studies. J Clin Oncol 22(4):756–758

    PubMed  Google Scholar 

  • Pierga JY, Delaloge S, Espie M et al (2010) A multicenter randomized phase II study of sequential epirubicin/cyclophosphamide followed by docetaxel with or without celecoxib or trastuzumab according to HER2 status, as primary chemotherapy for localized invasive breast cancer patients. Breast Cancer Res Treat 122(2):429–437

    CAS  PubMed  Google Scholar 

  • Prasad S, Ravindran J, Aggarwal BB (2010) NF-kappaB and cancer: how intimate is this relationship. Mol Cell Biochem 336(1–2):25–37

    CAS  PubMed Central  PubMed  Google Scholar 

  • Psaty BM, Furberg CD (2005) COX-2 inhibitors–lessons in drug safety. New Engl J Med 352(11):1133–1135

    CAS  PubMed  Google Scholar 

  • Rawlings JS, Rosler KM, Harrison DA (2004) The JAK/STAT signaling pathway. J Cell Sci 117(Pt 8):1281–1283

    CAS  PubMed  Google Scholar 

  • Ristimaki A, Sivula A, Lundin J et al (2002) Prognostic significance of elevated cyclooxygenase-2 expression in breast cancer. Cancer Res 62(3):632–635

    CAS  PubMed  Google Scholar 

  • Rivas MA, Carnevale RP, Proietti CJ et al (2008) TNF alpha acting on TNFR1 promotes breast cancer growth via p42/P44 MAPK, JNK, Akt and NF-kappa B-dependent pathways. Exp Cell Res 314(3):509–529

    CAS  PubMed  Google Scholar 

  • Robbins GF, Shah J, Rosen P, Chu F, Taylor J (1974) Inflammatory carcinoma of the breast. Surg Clin North Am 54(4):801–810

    CAS  PubMed  Google Scholar 

  • Robertson FM, Simeone AM, Mazumdar A et al (2008) Molecular and pharmacological blockade of the EP4 receptor selectively inhibits both proliferation and invasion of human inflammatory breast cancer cells. J Exp Ther Oncol 7(4):299–312

    CAS  PubMed  Google Scholar 

  • Robertson FM, Simeone AM, Lucci A, McMurray JS, Ghosh S, Cristofanilli M (2010) Differential regulation of the aggressive phenotype of inflammatory breast cancer cells by prostanoid receptors EP3 and EP4. Cancer 116(11):2806–2814

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rubio MF, Werbajh S, Cafferata EG et al (2006) TNF-alpha enhances estrogen-induced cell proliferation of estrogen-dependent breast tumor cells through a complex containing nuclear factor-kappa B. Oncogene 25(9):1367–1377

    CAS  PubMed  Google Scholar 

  • Salgado R, Junius S, Benoy I et al (2003) Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer: J Int du Cancer 103(5):642–646

    CAS  Google Scholar 

  • Sansone P, Storci G, Tavolari S et al (2007) IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Investig 117(12):3988–4002

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sasser AK, Sullivan NJ, Studebaker AW, Hendey LF, Axel AE, Hall BM (2007) Interleukin-6 is a potent growth factor for ER-alpha-positive human breast cancer. FASEB J: Off Publ Fed Am Soc Exp Biol 21(13):3763–3770

    CAS  Google Scholar 

  • Sheen-Chen SM, Chen WJ, Eng HL, Chou FF (1997) Serum concentration of tumor necrosis factor in patients with breast cancer. Breast Cancer Res Treat 43(3):211–215

    CAS  PubMed  Google Scholar 

  • Shostak K, Chariot A (2011) NF-kappaB, stem cells and breast cancer: the links get stronger. Breast Cancer Res: BCR 13(4):214

    PubMed Central  PubMed  Google Scholar 

  • Simstein R, Burow M, Parker A, Weldon C, Beckman B (2003) Apoptosis, chemoresistance, and breast cancer: insights from the MCF-7 cell model system. Exp Biol Med 228(9):995–1003

    CAS  Google Scholar 

  • Singh B, Cook KR, Martin C et al (2010) Evaluation of a CXCR4 antagonist in a xenograft mouse model of inflammatory breast cancer. Clin Exp Metastasis 27(4):233–240

    CAS  PubMed  Google Scholar 

  • Soliman AS, Kleer CG, Mrad K et al (2011) Inflammatory breast cancer in North Africa: comparison of clinical and molecular epidemiologic characteristics of patients from Egypt, Tunisia, and Morocco. Breast Dis 33(4):159–169

    CAS  PubMed  Google Scholar 

  • Speirs V, Kerin MJ, Newton CJ et al (1999) Evidence for transcriptional activation of ERalpha by IL-1beta in breast cancer cells. Int J Oncol 15(6):1251–1254

    CAS  PubMed  Google Scholar 

  • Studebaker AW, Storci G, Werbeck JL et al (2008) Fibroblasts isolated from common sites of breast cancer metastasis enhance cancer cell growth rates and invasiveness in an interleukin-6-dependent manner. Cancer Res 68(21):9087–9095

    CAS  PubMed  Google Scholar 

  • Subbaramaiah K, Norton L, Gerald W, Dannenberg AJ et al (2002) Cyclooxygenase-2 is overexpressed in HER-2/neu-positive breast cancer: evidence for involvement of AP-1 and PEA3. J Biol Chem 277(21):18649–18657

    CAS  PubMed  Google Scholar 

  • Subramaniam V, Chakrabarti R, Prud’homme GJ, Jothy S (2010) Tranilast inhibits cell proliferation and migration and promotes apoptosis in murine breast cancer. Anti-Cancer Drugs 21(4):351–361

    CAS  PubMed  Google Scholar 

  • Subramaniam V, Ace O, Prud’homme GJ, Jothy S (2011) Tranilast treatment decreases cell growth, migration and inhibits colony formation of human breast cancer cells. Exp Mol Pathol 90(1):116–122

    CAS  PubMed  Google Scholar 

  • Sullivan NJ, Sasser AK, Axel AE et al (2009) Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 28(33):2940–2947

    CAS  PubMed  Google Scholar 

  • Tawara K, Oxford JT, Jorcyk CL (2011) Clinical significance of interleukin (IL)-6 in cancer metastasis to bone: potential of anti-IL-6 therapies. Cancer Manag Res 3:177–189

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2(6):442–454

    CAS  PubMed  Google Scholar 

  • Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139(5):871–890

    CAS  PubMed  Google Scholar 

  • Ueno NT, Buzdar AU, Singletary SE et al (1997) Combined-modality treatment of inflammatory breast carcinoma: twenty years of experience at M. D. Anderson Cancer Center. Cancer Chemother Pharmacol 40(4):321–329

    CAS  PubMed  Google Scholar 

  • van Golen KL, Wu ZF, Qiao XT, Bao L, Merajver SD (2000) RhoC GTPase overexpression modulates induction of angiogenic factors in breast cells. Neoplasia 2(5):418–425

    PubMed Central  PubMed  Google Scholar 

  • Van Laere S, Van der Auwera I, Van den Eynden GG et al (2005) Distinct molecular signature of inflammatory breast cancer by cDNA microarray analysis. Breast Cancer Res Treat 93(3):237–246

    CAS  PubMed  Google Scholar 

  • Van Laere SJ, Van der Auwera I, Van den Eynden GG et al (2007) NF-kappaB activation in inflammatory breast cancer is associated with oestrogen receptor downregulation, secondary to EGFR and/or ErbB2 overexpression and MAPK hyperactivation. Br J Cancer 97(5):659–669

    PubMed Central  PubMed  Google Scholar 

  • Van Laere S, Limame R, Van Marck EA, Vermeulen PB, Dirix LY (2010) Is there a role for mammary stem cells in inflammatory breast carcinoma?: a review of evidence from cell line, animal model, and human tissue sample experiments. Cancer 116(11 Suppl):2794–2805

    PubMed  Google Scholar 

  • Walter M, Liang S, Ghosh S, Hornsby PJ, Li R (2009) Interleukin 6 secreted from adipose stromal cells promotes migration and invasion of breast cancer cells. Oncogene 28(30):2745–2755

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang D, Dubois RN (2004) Cyclooxygenase-2: a potential target in breast cancer. Semin Oncol 31(1 Suppl 3):64–73

    CAS  PubMed  Google Scholar 

  • Wang FM, Liu HQ, Liu SR, Tang SP, Yang L, Feng GS (2005) SHP-2 promoting migration and metastasis of MCF-7 with loss of E-cadherin, dephosphorylation of FAK and secretion of MMP-9 induced by IL-1beta in vivo and in vitro. Breast Cancer Res Treat 89(1):5–14

    CAS  PubMed  Google Scholar 

  • Weaver KL, Ivester P, Seeds M, Case LD, Arm JP, Chilton FH (2009) Effect of dietary fatty acids on inflammatory gene expression in healthy humans. J Biol Chem 284(23):15400–15407

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wendel M, Heller AR (2009) Anticancer actions of omega-3 fatty acids–current state and future perspectives. Anti-Cancer Agents Med Chem 9(4):457–470

    CAS  Google Scholar 

  • Williams CS, Mann M, DuBois RN (1999) The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18(55):7908–7916

    CAS  PubMed  Google Scholar 

  • Xiao Y, Ye Y, Yearsley K, Jones S, Barsky SH (2008) The lymphovascular embolus of inflammatory breast cancer expresses a stem cell-like phenotype. Am J Pathol 173(2):561–574

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu J, Lamouille S, Derynck R (2009) TGF-beta-induced epithelial to mesenchymal transition. Cell Res 19(2):156–172

    CAS  PubMed  Google Scholar 

  • Yang EY, Moses HL (1990) Transforming growth factor beta 1-induced changes in cell migration, proliferation, and angiogenesis in the chicken chorioallantoic membrane. J Cell Biol 111(2):731–741

    CAS  PubMed  Google Scholar 

  • Yang Y, Pan X, Lei W, Wang J, Song J (2006) Transforming growth factor-beta1 induces epithelial-to-mesenchymal transition and apoptosis via a cell cycle-dependent mechanism. Oncogene 25(55):7235–7244

    CAS  PubMed  Google Scholar 

  • Yang WT, Le-Petross HT, Macapinlac H et al (2008) Inflammatory breast cancer: PET/CT, MRI, mammography, and sonography findings. Breast Cancer Res Treat 109(3):417–426

    CAS  PubMed  Google Scholar 

  • Yao C, Lin Y, Chua MS et al (2007) Interleukin-8 modulates growth and invasiveness of estrogen receptor-negative breast cancer cells. Int J Cancer: J Int du Cancer 121(9):1949–1957

    CAS  Google Scholar 

  • Yin Y, Chen X, Shu Y (2009) Gene expression of the invasive phenotype of TNF-alpha-treated MCF-7 cells. Biomed Pharmacotherapie 63(6):421–428

    CAS  Google Scholar 

  • Yoshimura N, Sano H, Okamoto M et al (2003) Expression of cyclooxygenase-1 and -2 in human breast cancer. Surg Today 33(11):805–811

    CAS  PubMed  Google Scholar 

  • Yu Y, Wang Y, Ren X et al (2010) Context-dependent bidirectional regulation of the MutS homolog 2 by transforming growth factor beta contributes to chemoresistance in breast cancer cells. Mol Cancer Res 8(12):1633–1642

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang GJ, Adachi I (1999) Serum interleukin-6 levels correlate to tumor progression and prognosis in metastatic breast carcinoma. Anti-Cancer Res 19(2B):1427–1432

    CAS  Google Scholar 

  • Zhang F, Lundin M, Ristimaki A et al (2003) Ski-related novel protein N (SnoN), a negative controller of transforming growth factor-beta signaling, is a prognostic marker in estrogen receptor-positive breast carcinomas. Cancer Res 63(16):5005–5010

    CAS  PubMed  Google Scholar 

  • Zhang SM, Lin J, Cook NR et al (2007) C-reactive protein and risk of breast cancer. J Natl Cancer Inst 99(11):890–894

    CAS  PubMed  Google Scholar 

  • Zhang D, LaFortune TA, Krishnamurthy S et al (2009) Epidermal growth factor receptor tyrosine kinase inhibitor reverses mesenchymal to epithelial phenotype and inhibits metastasis in inflammatory breast cancer. Clin Cancer Res: Off J Am Assoc Cancer Res 15(21):6639–6648

    CAS  Google Scholar 

  • Zhou BP, Hu MC, Miller SA et al (2000) HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/NF-kappaB pathway. J Biol Chem 275(11):8027–8031

    CAS  PubMed  Google Scholar 

  • Zhou J, Zhang H, Gu P, Bai J, Margolick JB, Zhang Y (2008) NF-kappaB pathway inhibitors preferentially inhibit breast cancer stem-like cells. Breast Cancer Res Treat 111(3):419–427

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

Grant Support: State of Texas Rare and Aggressive Breast Cancer Research Program Grant.

Author information

Authors and Affiliations

  1. Department of Breast Medical Oncology, Morgan Welch Inflammatory Breast Cancer Research Program and Clinic, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd., Unit 1354, Houston, TX, 77030, USA

    Tamer M. Fouad, Takahiro Kogawa & Naoto T. Ueno

  2. Department of Hematopathology, Morgan Welch Inflammatory Breast Cancer Research Program and Clinic, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    James M. Reuben

  3. Department of Medical Oncology, The National Cancer Institute, Cairo University, Cairo, Egypt

    Tamer M. Fouad

Authors
  1. Tamer M. Fouad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takahiro Kogawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James M. Reuben
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naoto T. Ueno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naoto T. Ueno .

Editor information

Editors and Affiliations

  1. Dept of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA

    Bharat B. Aggarwal

  2. Dept of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA

    Bokyung Sung

  3. Dep Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA

    Subash Chandra Gupta

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Basel

About this chapter

Cite this chapter

Fouad, T.M., Kogawa, T., Reuben, J.M., Ueno, N.T. (2014). The Role of Inflammation in Inflammatory Breast Cancer. In: Aggarwal, B., Sung, B., Gupta, S. (eds) Inflammation and Cancer. Advances in Experimental Medicine and Biology, vol 816. Springer, Basel. https://doi.org/10.1007/978-3-0348-0837-8_3

Download citation

Publish with us

Policies and ethics

Search

Navigation