Seminars in Oncology
Volume 35, Issue 1 , Pages 41-50 , February 2008

Defining the Molecular Biology of Inflammatory Breast Cancer

  • Emmanuelle Charafe-Jauffret

      Affiliations

    • Département d’Oncologie Moléculaire, Institut Paoli-Calmettes and UMR599 Inserm, IFR137, Marseille, France.
    • Département de Biopathologie, Institut Paoli-Calmettes and UMR599 Inserm, IFR137, Marseille, France.
    • Faculté de Médecine, Université de la Méditerranée, Marseille, France.
    • ,
  • Carole Tarpin

      Affiliations

    • Département d’Oncologie Médicale, Institut Paoli-Calmettes and UMR599 Inserm, IFR137, Marseille, France
    • ,
  • Patrice Viens

      Affiliations

    • Faculté de Médecine, Université de la Méditerranée, Marseille, France.
    • Département d’Oncologie Médicale, Institut Paoli-Calmettes and UMR599 Inserm, IFR137, Marseille, France
    • ,
  • François Bertucci

      Affiliations

    • Département d’Oncologie Moléculaire, Institut Paoli-Calmettes and UMR599 Inserm, IFR137, Marseille, France.
    • Faculté de Médecine, Université de la Méditerranée, Marseille, France.
    • Département d’Oncologie Médicale, Institut Paoli-Calmettes and UMR599 Inserm, IFR137, Marseille, France
    • Corresponding Author InformationAddress correspondence to François Bertucci, MD, PhD, Département d’Oncologie Médicale, Institut Paoli-Calmettes, UMR599 Inserm, 232, Bd Sainte-Marguerite, 13273 Marseille Cedex 09, France.

References 

  1. Chang S, Parker SL, Pham T, et al. Inflammatory breast carcinoma incidence and survival: the Surveillance, Epidemiology, and End Results program of the National Cancer Institute, 1975-1992. Cancer. 1998;82:2366–2372
  2. Gonzalez-Angulo AM, Hortobagyi GN, Esteva FJ. Adjuvant therapy with trastuzumab for HER-2/neu-positive breast cancer. Oncologist. 2006;11:857–867
  3. Jaiyesimi IA, Buzdar AU, Hortobagyi G. Inflammatory breast cancer: a review. J Clin Oncol. 1992;10:1014–1024
  4. Kerlikowske K, Miglioretti DL, Buist DS, et al. Declines in invasive breast cancer and use of postmenopausal hormone therapy in a screening mammography population. J Natl Cancer Inst. 2007;99:1335–1339
  5. Ravdin PM, Cronin KA, Howlader N, et al. The decrease in breast-cancer incidence in 2003 in the United States. N Engl J Med. 2007;356:1670–1674
  6. Hance KW, Anderson WF, Devesa SS, et al. Trends in inflammatory breast carcinoma incidence and survival: the Surveillance, Epidemiology, and End Results program at the National Cancer Institute. J Natl Cancer Inst. 2005;97:966–975
  7. Ueno NT, Buzdar AU, Singletary SE, et al. Combined-modality treatment of inflammatory breast carcinoma: twenty years of experience at M.D. Anderson Cancer Center. Cancer Chemother Pharmacol. 1997;40:321–329
  8. Chevallier B, Asselain B, Kunlin A, et al. Inflammatory breast cancer (Determination of prognostic factors by univariate and multivariate analysis). Cancer. 1987;60:897–902
  9. Cristofanilli M, Buzdar AU, Sneige N, et al. Paclitaxel in the multimodality treatment for inflammatory breast carcinoma. Cancer. 2001;92:1775–1782
  10. Feldman LD, Hortobagyi GN, Buzdar AU, et al. Pathological assessment of response to induction chemotherapy in breast cancer. Cancer Res. 1986;46:2578–2581
  11. Palangie T, Mosseri V, Mihura J, et al. Prognostic factors in inflammatory breast cancer and therapeutic implications. Eur J Cancer. 1994;30A:921–927
  12. Sataloff DM, Mason BA, Prestipino AJ, et al. Pathologic response to induction chemotherapy in locally advanced carcinoma of the breast: a determinant of outcome. J Am Coll Surg. 1995;180:297–306
  13. Cristofanilli M, Gonzalez-Angulo AM, Buzdar AU, et al. Paclitaxel improves the prognosis in estrogen receptor negative inflammatory breast cancer: the M.D. Anderson Cancer Center experience. Clin Breast Cancer. 2004;4:415–419
  14. Vincent-Salomon A, Carton M, Freneaux P, et al. ERBB2 overexpression in breast carcinomas: no positive correlation with complete pathological response to preoperative high-dose anthracycline-based chemotherapy. Eur J Cancer. 2000;36:586–591
  15. Cristofanilli M, Buzdar AU, Hortobagyi GN. Update on the management of inflammatory breast cancer. Oncologist. 2003;8:141–148
  16. Kleer CG, van Golen KL, Merajver SD. Molecular biology of breast cancer metastasis (Inflammatory breast cancer: clinical syndrome and molecular determinants). Breast Cancer Res. 2000;2:423–429
  17. Paradiso A, Tommasi S, Brandi M, et al. Cell kinetics and hormonal receptor status in inflammatory breast carcinoma (Comparison with locally advanced disease). Cancer. 1989;64:1922–1927
  18. Charafe-Jauffret E, Tarpin C, Bardou VJ, et al. Immunophenotypic analysis of inflammatory breast cancers: identification of an ‘inflammatory signature’. J Pathol. 2004;202:265–273
  19. Van den Eynden GG, Van der Auwera I, Van Laere S, et al. Validation of a tissue microarray to study differential protein expression in inflammatory and non-inflammatory breast cancer. Breast Cancer Res Treat. 2004;85:13–22
  20. Somlo G, Frankel P, Chow W, et al. Prognostic indicators and survival in patients with stage IIIB inflammatory breast carcinoma after dose-intense chemotherapy. J Clin Oncol. 2004;22:1839–1848
  21. Guerin M, Gabillot M, Mathieu MC, et al. Structure and expression of c-erbB-2 and EGF receptor genes in inflammatory and non-inflammatory breast cancer: prognostic significance. Int J Cancer. 1989;43:201–208
  22. Lerebours F, Bertheau P, Bieche I, et al. Evidence of chromosome regions and gene involvement in inflammatory breast cancer. Int J Cancer. 2002;102:618–622
  23. Charpin C, Bonnier P, Khouzami A, et al. Inflammatory breast carcinoma: an immunohistochemical study using monoclonal anti-pHER-2/neu, pS2, cathepsin, ER and PR. Anticancer Res. 1992;12:591–597
  24. Sawaki M, Ito Y, Akiyama F, et al. High prevalence of HER-2/neu and p53 overexpression in inflammatory breast cancer. Breast Cancer. 2006;13:172–178
  25. Charafe-Jauffret E, Mrad K, Intidhar LS, et al. Inflammatory breast cancers in Tunisia and France show similar immunophenotypes. Breast. 2007;16:352–358
  26. Parton M, Dowsett M, Ashley S, et al. High incidence of HER-2 positivity in inflammatory breast cancer. Breast. 2004;13:97–103
  27. Prost S, Le MG, Douc-Rasy S, et al. Association of c-erbB2-gene amplification with poor prognosis in non-inflammatory breast carcinomas but not in carcinomas of the inflammatory type. Int J Cancer. 1994;58:763–768
  28. Van Pelt AE, Mohsin S, Elledge RM, et al. Neoadjuvant trastuzumab and docetaxel in breast cancer: preliminary results. Clin. Breast Cancer. 2003;4:348–353
  29. Nieto Y, Nawaz S, Shpall EJ, et al. Long-term analysis and prospective validation of a prognostic model for patients with high-risk primary breast cancer receiving high-dose chemotherapy. Clin Cancer Res. 2004;10:2609–2617
  30. Hurley J, Doliny P, Reis I, et al. Docetaxel, cisplatin, and trastuzumab as primary systemic therapy for human epidermal growth factor receptor 2-positive locally advanced breast cancer. J Clin Oncol. 2006;24:1831–1838
  31. Limentani SA, Brufsky AM, Erban JK, et al. Phase II study of neoadjuvant docetaxel, vinorelbine, and trastuzumab followed by surgery and adjuvant doxorubicin plus cyclophosphamide in women with human epidermal growth factor receptor 2-overexpressing locally advanced breast cancer. J Clin Oncol. 2007;25:1232–1238
  32. Dawood S, Gonzalez-Angulo AM, Peintinger F, et al. Efficacy and safety of neoadjuvant trastuzumab combined with paclitaxel and epirubicin: a retrospective review of the M.D. Anderson experience. Cancer. 2007;110:1195–1200
  33. Le MG, Arriagada R, Bahi J, et al. Are risk factors for breast cancer similar in women with inflammatory breast cancer and in those with non-inflammatory breast cancer?. Breast. 2006;15:355–362
  34. Nieto Y, Nawaz F, Jones RB, et al. Prognostic significance of overexpression and phosphorylation of epidermal growth factor receptor (EGFR) and the presence of truncated EGFRvIII in locoregionally advanced breast cancer. J Clin Oncol. 2007;25:4405–4413
  35. Dawood S, Cristofanilli M. What progress have we made in managing inflammatory breast cancer?. Oncology (Williston Park). 2007;21:673–679
  36. Nigro JM, Baker SJ, Preisinger AC, et al. Mutations in the p53 gene occur in diverse human tumour types. Nature. 1989;342:705–708
  37. Davidoff AM, Humphrey PA, Iglehart JD, et al. Genetic basis for p53 overexpression in human breast cancer. Proc Natl Acad Sci U S A. 1991;88:5006–5010
  38. Faille A, De Cremoux P, Extra JM, et al. p53 mutations and overexpression in locally advanced breast cancers. Br J Cancer. 1994;69:1145–1150
  39. Moll UM, Riou G, Levine AJ. Two distinct mechanisms alter p53 in breast cancer: mutation and nuclear exclusion. Proc Natl Acad Sci U S A. 1992;89:7262–7266
  40. Riou G, Le MG, Travagli JP, et al. Poor prognosis of p53 gene mutation and nuclear overexpression of p53 protein in inflammatory breast carcinoma. J Natl Cancer Inst. 1993;85:1765–1767
  41. Resetkova E, Gonzalez-Angulo AM, Sneige N, et al. Prognostic value of P53, MDM-2, and MUC-1 for patients with inflammatory breast carcinoma. Cancer. 2004;101:913–917
  42. Yang CH, Cristofanilli M. The role of p53 mutations as a prognostic factor and therapeutic target in inflammatory breast cancer. Future Oncol. 2006;2:247–255
  43. McCarthy NJ, Yang X, Linnoila IR, et al. Microvessel density, expression of estrogen receptor alpha, MIB-1, p53, and c-erbB-2 in inflammatory breast cancer. Clin Cancer Res. 2002;8:3857–3862
  44. Colpaert CG, Vermeulen PB, Fox SB, et al. The presence of a fibrotic focus in invasive breast carcinoma correlates with the expression of carbonic anhydrase IX and is a marker of hypoxia and poor prognosis. Breast Cancer Res Treat. 2003;81:137–147
  45. Van der Auwera I, Van Laere SJ, Van den Eynden GG, et al. Increased angiogenesis and lymphangiogenesis in inflammatory versus noninflammatory breast cancer by real-time reverse transcriptase-PCR gene expression quantification. Clin Cancer Res. 2004;10:7965–7971
  46. Shirakawa K, Furuhata S, Watanabe I, et al. Induction of vasculogenesis in breast cancer models. Br J Cancer. 2002;87:1454–1461
  47. Wedam SB, Low JA, Yang SX, et al. Antiangiogenic and antitumor effects of bevacizumab in patients with inflammatory and locally advanced breast cancer. J Clin Oncol. 2006;24:769–777
  48. Kleer CG, van Golen KL, Braun T, et al. Persistent E-cadherin expression in inflammatory breast cancer. Mod Pathol. 2001;14:458–464
  49. Oka H, Shiozaki H, Kobayashi K, et al. Expression of E-cadherin cell adhesion molecules in human breast cancer tissues and its relationship to metastasis. Cancer Res. 1993;53:1696–1701
  50. Hoffmeyer MR, Wall KM, Dharmawardhane SF. In vitro analysis of the invasive phenotype of SUM 149, an inflammatory breast cancer cell line. Cancer Cell Int. 2005;5:11
  51. Tomlinson JS, Alpaugh ML, Barsky SH. An intact overexpressed E-cadherin/alpha, beta-catenin axis characterizes the lymphovascular emboli of inflammatory breast carcinoma. Cancer Res. 2001;61:5231–5241
  52. Alpaugh ML, Tomlinson JS, Kasraeian S, et al. Cooperative role of E-cadherin and sialyl-Lewis X/A-deficient MUC1 in the passive dissemination of tumor emboli in inflammatory breast carcinoma. Oncogene. 2002;21:3631–3643
  53. Alpaugh ML, Tomlinson JS, Ye Y, et al. Relationship of sialyl-Lewis(x/a) underexpression and E-cadherin overexpression in the lymphovascular embolus of inflammatory breast carcinoma. Am J Pathol. 2002;161:619–628
  54. Cabioglu N, Gong Y, Islam R, et al. Expression of growth factor and chemokine receptors: new insights in the biology of inflammatory breast cancer. Ann Oncol. 2007;18:1021–1029
  55. Andre F, Cabioglu N, Assi H, et al. Expression of chemokine receptors predicts the site of metastatic relapse in patients with axillary node positive primary breast cancer. Ann Oncol. 2006;17:945–951
  56. Cabioglu N, Sahin A, Doucet M, et al. Chemokine receptor CXCR4 expression in breast cancer as a potential predictive marker of isolated tumor cells in bone marrow. Clin Exp Metast. 2005;22:39–46
  57. Minn AJ, Gupta GP, Padua D, et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci U S A. 2007;104:6740–6745
  58. Smith MC, Luker KE, Garbow JR, et al. CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res. 2004;64:8604–8612
  59. Forozan F, Veldman R, Ammerman CA, et al. Molecular cytogenetic analysis of 11 new breast cancer cell lines. Br J Cancer. 1999;81:1328–1334
  60. Alpaugh ML, Tomlinson JS, Shao ZM, et al. A novel human xenograft model of inflammatory breast cancer. Cancer Res. 1999;59:5079–5084
  61. Shirakawa K, Tsuda H, Heike Y, et al. Absence of endothelial cells, central necrosis, and fibrosis are associated with aggressive inflammatory breast cancer. Cancer Res. 2001;61:445–451
  62. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000;406:747–752
  63. Sorlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001;98:10869–10874
  64. Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A. 2003;100:8418–8423
  65. Shirakawa K, Kobayashi H, Sobajima J, et al. Inflammatory breast cancer: vasculogenic mimicry and its hemodynamics of an inflammatory breast cancer xenograft model. Breast Cancer Res. 2003;5:136–139
  66. Maniotis AJ, Folberg R, Hess A, et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999;155:739–752
  67. van Golen KL, Davies S, Wu ZF, et al. A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin Cancer Res. 1999;5:2511–2519
  68. Sahai E, Marshall CJ. RHO-GTPases and cancer. Nat Rev Cancer. 2002;2:133–142
  69. van Golen KL, Wu ZF, Qiao XT, et al. RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype. Cancer Res. 2000;60:5832–5838
  70. van Golen KL, Wu ZF, Qiao XT, et al. RhoC GTPase overexpression modulates induction of angiogenic factors in breast cells. Neoplasia. 2000;2:418–425
  71. Wu M, Wu ZF, Kumar-Sinha C, et al. RhoC induces differential expression of genes involved in invasion and metastasis in MCF10A breast cells. Breast Cancer Res Treat. 2004;84:3–12
  72. van Golen KL, Bao LW, Pan Q, et al. Mitogen activated protein kinase pathway is involved in RhoC GTPase induced motility, invasion and angiogenesis in inflammatory breast cancer. Clin Exp Metast. 2002;19:301–311
  73. Kleer CG, van Golen KL, Zhang Y, et al. Characterization of RhoC expression in benign and malignant breast disease: a potential new marker for small breast carcinomas with metastatic ability. Am J Pathol. 2002;160:579–584
  74. Kleer CG, Griffith KA, Sabel MS, et al. RhoC-GTPase is a novel tissue biomarker associated with biologically aggressive carcinomas of the breast. Breast Cancer Res Treat. 2005;93:101–110
  75. van Golen KL, Bao L, DiVito MM, et al. Reversion of RhoC GTPase-induced inflammatory breast cancer phenotype by treatment with a farnesyl transferase inhibitor. Mol Cancer Ther. 2002;1:575–583
  76. Kleer CG, Zhang Y, Pan Q, et al. WISP3 is a novel tumor suppressor gene of inflammatory breast cancer. Oncogene. 2002;21:3172–3180
  77. Kleer CG, Zhang Y, Pan Q, et al. WISP3 (CCN6) is a secreted tumor-suppressor protein that modulates IGF signaling in inflammatory breast cancer. Neoplasia. 2004;6:179–185
  78. Kleer CG, Zhang Y, Pan Q, et al. WISP3 and RhoC guanosine triphosphatase cooperate in the development of inflammatory breast cancer. Breast Cancer Res. 2004;6:R110–R115
  79. Bertucci F, Finetti P, Rougemont J, et al. Gene expression profiling for molecular characterization of inflammatory breast cancer and prediction of response to chemotherapy. Cancer Res. 2004;64:8558–8565
  80. Bertucci F, Finetti P, Rougemont J, et al. Gene expression profiling identifies molecular subtypes of inflammatory breast cancer. Cancer Res. 2005;65:2170–2178
  81. Rouzier R, Perou CM, Symmans WF, et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res. 2005;11:5678–5685
  82. Garcia S, Dales JP, Jacquemier J, et al. c-Met overexpression in inflammatory breast carcinomas: automated quantification on tissue microarrays. Br J Cancer. 2007;96:329–335
  83. Van Laere S, Van der Auwera I, Van den Eynden GG, et al. Distinct molecular signature of inflammatory breast cancer by cDNA microarray analysis. Breast Cancer Res Treat. 2005;93:237–246
  84. Van Laere SJ, Van der Auwera I, Van den Eynden GG, et al. Nuclear factor-kappaB signature of inflammatory breast cancer by cDNA microarray validated by quantitative real-time reverse transcription-PCR, immunohistochemistry, and nuclear factor-kappaB DNA-binding. Clin Cancer Res. 2006;12:3249–3256
  85. Van Laere S, Van der Auwera I, Van den Eynden G, et al. 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. 2007;97:659–669
  86. Van Laere S, Van der Auwera I, Van den Eynden G, et al. Distinct molecular phenotype of inflammatory breast cancer compared to non-inflammatory breast cancer using Affymetrix-based genome-wide gene-expression analysis. Br J Cancer. 2007;97:165–174
  87. Van den Eynden GG, Van Laere SJ, Van der Auwera I, et al. Overexpression of caveolin-1 and -2 in cell lines and in human samples of inflammatory breast cancer. Breast Cancer Res Treat. 2006;95:219–228
  88. Bieche I, Lerebours F, Tozlu S, et al. Molecular profiling of inflammatory breast cancer: identification of a poor-prognosis gene expression signature. Clin Cancer Res. 2004;10:6789–6795
  89. Dressman HK, Hans C, Bild A, et al. Gene expression profiles of multiple breast cancer phenotypes and response to neoadjuvant chemotherapy. Clin Cancer Res. 2006;12:819–826
  90. Nguyen DM, Sam K, Tsimelzon A, et al. Molecular heterogeneity of inflammatory breast cancer: a hyperproliferative phenotype. Clin Cancer Res. 2006;12:5047–5054
  91. Lee B, Tannenbaum N. Inflammatory carcinoma of the breast: a report of twenty-eight cases from the Breast Clinic of Memorial Hospital. Surg Gynecol Obstet. 1924;39:580–595
  92. Stingl J, Caldas C. Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis. Nat Rev Cancer. 2007;7:791–799

PII: S0093-7754(07)00240-0

doi: 10.1053/j.seminoncol.2007.11.015

Seminars in Oncology
Volume 35, Issue 1 , Pages 41-50 , February 2008

Article Tools