Circulating tumor cells (CTCs) are associated with abnormalities in peripheral blood dendritic cells in patients with inflammatory breast cancer

Oncotarget

Volumn 8, Issue 22, 2017, Pages 35656-35668

  Mego, Michal ^a,b   Gao, Hui ^a   Cohen, Evan N ^a   Anfossi, Simone ^a   Giordano, Antonio ^a,g   Tin, Sanda ^a   Fouad, Tamer M ^a,c   Giorgi, Ugo De ^a,d   Giuliano, Mario ^a,e   Woodward, Wendy A ^a   Alvarez, Ricardo H ^a   Valero, Vicente ^a   Ueno, Naoto T ^a   Hortobagyi, Gabriel N ^a   Cristofanilli, Massimo ^a,f   Reuben, James M ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Faculty of Natural Sciences   (Slovakia)

^c CAIRO UNIVERSITY   (Egypt)

^d DEPARTMENT OF MEDICAL ONCOLOGY   (Italy)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^f NORTHWESTERN UNIVERSITY   (United States)

^g MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Adaptive immunity; Circulating tumors cells; Dendritic cells; Inflammatory breast cancer; Innate immunity

Indexed keywords

CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; INTERLEUKIN 12; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; CHEMOKINE RECEPTOR; CYTOKINE;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CIRCULATING TUMOR CELL; CLINICAL OUTCOME; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; INFLAMMATORY BREAST CANCER; MAJOR CLINICAL STUDY; OVERALL SURVIVAL; PERIPHERAL BLOOD DENDRITIC CELL; PROTEIN EXPRESSION; ADAPTIVE IMMUNITY; CANCER STAGING; CELL COUNT; DENDRITIC CELL; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; METASTASIS; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; SURVIVAL ANALYSIS; TUMOR EMBOLISM;

ADAPTIVE IMMUNITY; ADULT; AGED; CELL COUNT; CYTOKINES; DENDRITIC CELLS; FEMALE; HUMANS; IMMUNITY, INNATE; INFLAMMATORY BREAST NEOPLASMS; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASM STAGING; NEOPLASTIC CELLS, CIRCULATING; PROGNOSIS; RECEPTORS, CHEMOKINE; SURVIVAL ANALYSIS;

EID: 85020039992     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10290     Document Type: Article

References (57)

1. Anderson WF, Schairer C, Chen BE, Hance KW, Levine PH. Epidemiology of inflammatory breast cancer (IBC). Breast Dis 2005; 22:9-23.
2. Hance KW, Anderson WF, Devesa SS, Young HA, Levine PH. 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: 966-75.
3. Walshe J, Swain S. Clinical aspects of inflammatory breast cancer. Breast Dis 2005-2006; 22: 35-44.
4. Ueno NT, Buzdar AU, Singletary SE, Ames FC, McNeese MD, Holmes FA, Theriault RL, Strom EA, Wasaff BJ, Asmar L, Frye D, Hortobagyi GN. Combined-modality treatment of inflammatory breast carcinoma: twenty years of experience at M.D. Anderson Cancer Center. Cancer Chemother Pharmacol 1997, 40: 321-29.
5. Masuda H, Brewer TM, Liu DD, Iwamoto T, Shen Y, Hsu L, Willey JS, Gonzalez-Angulo AM, Chavez-MacGregor M, Fouad TM, Woodward WA, Reuben JM, Valero V, Alvarez RH, Hortobagyi GN, Ueno NT. Long-term treatment efficacy in primary inflammatory breast cancer by hormonal receptor-and HER2-defined subtypes. Ann Oncol. 2014, 25: 384-91.
6. Fouad TM, Kogawa T, Liu DD, Shen Y, Masuda H, El-Zein R, Woodward WA, Chavez-MacGregor M, Alvarez RH, Arun B, Lucci A, Krishnamurthy S, Babiera G, Buchholz TA, Valero V, Ueno NT. Overall survival differences between patients with inflammatory and noninflammatory breast cancer presenting with distant metastasis at diagnosis. Breast Cancer Res Treat 2015; 152: 407-16.
7. Cristofanilli M, Buzdar AU, Hortobagyi GN. Update on the management of inflammatory breast cancer. Oncologist 2003; 8: 141-48.
8. Cristofanilli M, Valero V, Buzdar AU, Kau SW, Broglio KR, Gonzalez-Angulo AM, Sneige N, Islam R, Ueno NT, Buchholz TA, Singletary SE, Hortobagyi GN. Inflammatory breast cancer (IBC) and patterns of recurrence-understanding the biology of a unique disease. Cancer 2007, 110: 1436-44.
9. Robertson FM, Bondy M, Yang W, Yamauchi H, Wiggins S, Kamrudin S, Krishnamurthy S, Le-Petross H, Bidaut L, Player AN, Barsky SH, Woodward WA, Buchholz T, Lucci A, Ueno NT, Cristofanilli M. Inflammatory breast cancer: the disease, the biology, the treatment. CA Cancer J Clin 2010, 60: 351-75.
10. Mego M, Giordano A, De Giorgi U, Masuda H, Hsu L, Giuliano M, Fouad TM, Dawood S, Ueno NT, Valero V, Andreopoulou E, Alvarez RH, Woodward WA, Hortobagyi GN, Cristofanilli M, Reuben JM. Circulating tumor cells in newly diagnosed inflammatory breast cancer. Breast Cancer Res. 2015, 17:2.
11. Lucci A, Hall CS, Lodhi AK, Bhattacharyya A, Anderson AE, Xiao L, Bedrosian I, Kuerer HM, Krishnamurthy S. Circulating tumour cells in non-metastatic breast cancer: a prospective study. Lancet Oncol 2012, 13: 688-95.
12. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW, Hayes DF. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 2004; 351, 781-91.
13. Zhan, M., Zhao, H. & Han, Z. C. Signaling mechanisms of anoikis. Histol. Histopathol. 2004; 19, 973-83.
14. Mego M, Mani SA, Cristofanilli M. Molecular mechanisms of metastasis in breast cancer-clinical applications. Nat Rev Clin Oncol. 2010; 7:693-701.
15. Baccelli I, Schneeweiss A, Riethdorf S, Stenzinger A, Schillert A, Vogel V, Klein C, Saini M, Bäuerle T, Wallwiener M, Holland-Letz T, Höfner T, Sprick M, Scharpff M, Marmé F, Sinn HP, Pantel K, Weichert W, Trumpp A. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat Biotechnol. 2013; 31:539-44.
16. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-74.
17. Lehner M, Morhart P, Stilper A, Petermann D, Weller P, Stachel D, Holter W. Efficient chemokine-dependent migration and primary and secondary IL-12 secretion by human dendritic cells stimulated through Toll-like receptors. J Immunother. 2007;30: 312-22.
18. Stary G, Bangert C, Tauber M, Strohal R, Kopp T, Stingl G. Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J Exp Med. 2007;204:1441-51.
19. Riol-Blanco L, Sánchez-Sánchez N, Torres A, Tejedor A, Narumiya S, Corbí AL, Sánchez-Mateos P, Rodríguez-Fernández JL. The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. Journal of Immunology 2005, 174: 4070-80.
20. Sisirak V, Faget J, Gobert M, Goutagny N, Vey N, Treilleux I, Renaudineau S, Poyet G, Labidi-Galy SI, Goddard-Leon S, Durand I, Le Mercier I, Bajard A, Bachelot T, Puisieux A, Puisieux I, Blay JY, Ménétrier-Caux C, Caux C, Bendriss-Vermare N. Impaired IFN-á production by plasmacytoid dendritic cells favors regulatory T-cell expansion that may contribute to breast cancer progression. Cancer Res. 2012, 72: 5188-97.
21. Matta BM, Castellaneta A, Thomson AW. Tolerogenic plasmacytoid DC. Eur J Immunol. 2010, 40: 2667-76.
22. Oh JZ, Kurche JS, Burchill MA, Kedl RM. TLR7 enables cross-presentation by multiple dendritic cell subsets through a type I IFN-dependent pathway. Blood. 2011, 118: 3028-38.
23. Liu YJ. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol. 2005; 23: 275-230.
24. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, Lee H, Arthur CD, White JM, Kalinke U, Murphy KM, Schreiber RD. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med. 2011, 208:1989-2003.
25. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM, Murphy KM, Gajewski TF. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8 (alpha)+ dendritic cells. J Exp Med. 2011, 208: 2005-2016.
26. Green TL, Cruse JM, Lewis RE, Craft BS. Circulating tumor cells (CTCs) from metastatic breast cancer patients linked to decreased immune function and response to treatment. Exp Mol Pathol. 2013; 95:174-79.
27. Green TL, Santos MF, Ejaeidi AA, Craft BS, Lewis RE, Cruse JM. Toll-like receptor (TLR) expression of immune system cells from metastatic breast cancer patients with circulating tumor cells. Exp Mol Pathol. 2014; 97: 44-48.
28. Mego M, Gao H, Cohen EN, Anfossi S, Giordano A, Sanda T, Fouad TM, De Giorgi U, Giuliano M, Woodward WA, Alvarez RH, Valero V, Ueno NT, Hortobagyi GN, Cristofanilli M, Reuben JM. Circulating tumor cells (CTC) are associated with defects in adaptive immunity in patients with inflammatory breast cancer. J of Cancer, 2015 (In press).
29. Greene FL, Page DL, Fleming ID et al. AJCC Cancer Staging Handbook, 6th edition. New York, NY: Springer 2002.
30. Dawood S, Merajver SD, Viens P, Vermeulen PB, Swain SM, Buchholz TA, Dirix LY, Levine PH, Lucci A, Krishnamurthy S, Robertson FM, Woodward WA, Yang WT, Ueno NT, Cristofanilli M. International expert panel on inflammatory breast cancer: consensus statement for standardized diagnosis and treatment. Ann Oncol 2011; 22: 515-23.
31. Singletary SE, Allred C, Ashley P, Bassett LW, Berry D, Bland KI, Borgen PI, Clark GM, Edge SB, Hayes DF, Hughes LL, Hutter RV, Morrow M, Page DL, Recht A, Theriault RL, Thor A, Weaver DL, Wieand HS, Greene FL. Staging system for breast cancer: revisions for the 6th edition of the AJCC Cancer Staging Manual. Surg Clin North Am 2003, 83: 803-19.
32. Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, Rao C, Tibbe AG, Uhr JW, Terstappen LW. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res. 2004;10:6897-6904.
33. Lee BN, Follen M, Rodriquez G, Shen DY, Malpica A, Shearer WT, Reuben JM. Deficiencies in myeloid antigen-presenting cells in women with cervical squamous intraepithelial lesions. Cancer. 2006, 107: 999-1007
34. Ida JA, Shrestha N, Desai S, Pahwa S, Hanekom WA, Haslett PA. A whole blood assay to assess peripheral blood dendritic cell function in response to Toll-like receptor stimulation. J Immunol Methods. 2006;310:86-99
35. Naing A, Reuben JM, Camacho LH, Gao H, Lee BN, Cohen EN, Verschraegen C, Stephen S, Aaron J, Hong D, Wheler J, Kurzrock R. Phase I Dose Escalation Study of Sodium Stibogluconate (SSG), a Protein Tyrosine Phosphatase Inhibitor, Combined with Interferon Alpha for Patients with Solid Tumors. J Cancer. 2011, 2:81-89.
36. Butchi NB, Pourciau S, Du M, Morgan TW, Peterson KE. Analysis of the neuroinflammatory response to TLR7 stimulation in the brain: comparison of multiple TLR7 and/ or TLR8 agonists. J Immunol. 2008;180:7604-12.
37. Salio M, Speak AO, Shepherd D, Polzella P, Illarionov PA, Veerapen N, Besra GS, Platt FM, Cerundolo V. Modulation of human natural killer T cell ligands on TLR-mediated antigen-presenting cell activation. Proc Natl Acad Sci U S A. 2007; 104: 20490-95.
38. Bidard FC, Mathiot C, Delaloge S, Brain E, Giachetti S, de Cremoux P, Marty M, Pierga JY. Single circulating tumor cell detection and overall survival in nonmetastatic breast cancer. Ann Oncol 2010, 21: 729-733.
39. Lang JE, Mosalpuria K, Cristofanilli M, Krishnamurthy S, Reuben J, Singh B, Bedrosian I, Meric-Bernstam F, Lucci A. HER2 status predicts the presence of circulating tumor cells in patients with operable breast cancer. Breast Cancer Res Treat 2009, 113: 501-517.
40. Rack B, Schindlbeck C, Jückstock J, Andergassen U, Hepp P, Zwingers T, Friedl TW, Lorenz R, Tesch H, Fasching PA, Fehm T, Schneeweiss A, Lichtenegger W, Beckmann MW, Friese K, Pantel K, Janni W; SUCCESS Study Group. Circulating tumor cells predict survival in early average-tohigh risk breast cancer patients. J Natl Cancer Inst. 2014,106 pii: dju066.
41. Mego M, De Giorgi U, Hsu L, Ueno NT, Valero V, Jackson S, Andreopoulou E, Kau SW, Reuben JM, Cristofanilli M. Circulating tumor cells in metastatic inflammatory breast cancer. Ann Oncol 2009, 20: 1824-28.
42. Li Z, Pang Y, Gara SK, Achyut BR, Heger C, Goldsmith PK, Lonning S, Yang L. Gr-1+CD11b+ cells are responsible for tumor promoting effect of TGF-â in breast cancer progression. Int J Cancer. 2012, 131:2584-95.
43. Beury DW, Parker KH, Nyandjo M, Sinha P, Carter KA, Ostrand-Rosenberg S. Cross-talk among myeloid-derived suppressor cells, macrophages, and tumor cells impacts the inflammatory milieu of solid tumors. J Leukoc Biol. 2014, 96:1109-18.
44. Filipazzi P, Huber V, Rivoltini L. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients. Cancer Immunol Immunother. 2012, 61:255-63.
45. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K. Immunobiology of dendritic cell. Annu Rev Immunol. 2000;18: 767-811.
46. Lutz MB, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 2002, 23:445-9.
47. Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, Ravoet M, Le Buanec H, Sibille C, Manfouo-Foutsop G, Veys I, Haibe-Kains B, Singhal SK, Michiels S, Rothé F, Salgado R, Duvillier H, Ignatiadis M, Desmedt C, Bron D, Larsimont D, Piccart M, Sotiriou C, Willard-Gallo K. CD4+ follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123: 2873-92.
48. Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, Kellokumpu-Lehtinen PL, Bono P, Kataja V, Desmedt C, Piccart MJ, Loibl S, Denkert C, Smyth MJ, Joensuu H, Sotiriou C. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol. 2014; 25:1544-50.
49. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JP, Hitre E, de Azambuja E, Quinaux E, Di Leo A, Michiels S, Piccart MJ, Sotiriou C. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicinbased chemotherapy: BIG 02-98. J Clin Oncol. 2013; 31: 860-7.
50. Treilleux I, Blay JY, Bendriss-Vermare N, Ray-Coquard I, Bachelot T, Guastalla JP, Bremond A, Goddard S, Pin JJ, Barthelemy-Dubois C, Lebecque S. Dendritic cell infiltration and prognosis of early stage breast cancer. Clin Cancer Res. 2004, 10:7466-74.
51. Guiducci C, Ott G, Chan JH, Damon E, Calacsan C, Matray T, Lee KD, Coffman RL, Barrat FJ. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J Exp Med. 2006, 203:1999-2008.
52. Sisirak V, Faget J, Vey N, Blay JY, Ménétrier-Caux C, Caux C, Bendriss-Vermare N. Plasmacytoid dendritic cells deficient in IFNá production promote the amplification of FOXP3(+) regulatory T cells and are associated with poor prognosis in breast cancer patients. Oncoimmunology. 2013; 2: e22338.
53. Cohen EN, Gao H, Anfossi S, Mego M, Reddy NG, Debeb B, Giordano A, Tin S, Wu Q, Garza RJ, Cristofanilli M, Mani SA, Croix DA, Ueno NT, Woodward WA, Luthra R, Krishnamurthy S, Reuben JM. Inflammation Mediated Metastasis: Immune Induced Epithelial-To-Mesenchymal Transition in Inflammatory Breast Cancer Cells. PLoS One. 2015, 10:e0132710.
54. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, Concannon KF, Donaldson MC, Sequist LV, Brachtel E, Sgroi D, Baselga J, Ramaswamy S, Toner M, Haber DA, Maheswaran S. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013; 339: 580-4.
55. Mego M, Mani SA, Lee BN, Li C, Evans KW, Cohen EN, Gao H, Jackson SA, Giordano A, Hortobagyi GN, Cristofanilli M, Lucci A, Reuben JM. Expression of epithelial-mesenchymal transition-inducing transcription factors in primary breast cancer: the effect of neoadjuvant therapy. Int J Cancer 2012; 130: 808-16.
56. Giordano A, Gao H, Anfossi S, Cohen E, Mego M, Lee BN, Tin S, De Laurentiis M, Parker CA, Alvarez RH, Valero V, Ueno NT, De Placido S, Mani SA, Esteva FJ, Cristofanilli M, Reuben JM. Epithelial-mesenchymal transition and stem cell markers in patients with HER2-positive metastatic breast cancer. Mol Cancer Ther. 2012; 11:2526-34.
57. Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell. 2009; 15:195-206.