Il-6 signaling between ductal carcinoma in situ cells and carcinoma-associated fibroblasts mediates tumor cell growth and migration

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Osuala, Kingsley O ^a   Sameni, Mansoureh ^a   Shah, Seema ^a,b   Aggarwal, Neha ^a   Simonait, Michelle L ^a   Franco, Omar E ^c   Hong, Yan ^d   Hayward, Simon W ^c   Behbod, Fariba ^d   Mattingly, Raymond R ^a   Sloane, Bonnie F ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^d UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

3D cell culture; Breast cancer; Carcinoma associated fibroblasts (CAFs); Ductal carcinoma in situ (DCIS); Interleukin 6 (IL 6)

Indexed keywords

CATHEPSIN B; INTERLEUKIN 6; IL6 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; AUTOCRINE EFFECT; BREAST CARCINOGENESIS; CANCER CELL; CANCER GROWTH; CARCINOMA ASSOCIATED FIBROBLAST; CELL GROWTH; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRADUCTAL CARCINOMA; PARACRINE SIGNALING; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; BREAST TUMOR; METABOLISM; PAGET NIPPLE DISEASE; PATHOLOGY; TUMOR CELL LINE; TUMOR INVASION;

BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL LINE, TUMOR; FEMALE; FIBROBLASTS; HUMANS; INTERLEUKIN-6; NEOPLASM INVASIVENESS;

EID: 84938919353     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1576-3     Document Type: Article

References (90)

1. Virnig BA, Tuttle TM, Shamliyan T, Kane RL. Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes. J Natl Cancer Inst. 2010;102(3):170-8.
2. Society AC. Cancer Facts & Figures 2014. American Cancer Society. Cancer.org. 2014;8-10.
3. Sanders ME, Schuyler PA, Dupont WD, Page DL. The natural history of low-grade ductal carcinoma in situ of the breast in women treated by biopsy only revealed over 30 years of long-term follow-up. Cancer. 2005;103(12):2481-4.
4. Page DL, Dupont WD, Rogers LW, Jensen RA, Schuyler PA. Continued local recurrence of carcinoma 15-25 years after a diagnosis of low grade ductal carcinoma in situ of the breast treated only by biopsy. Cancer. 1995;76(7):1197-200.
5. Network NCC. Stage 0 Breast Cancer. NCCN Guidlines for Patients. 2014;1(2014):17-28.
6. Bissell MJ, Radisky DC, Rizki A, Weaver VM, Petersen OW. The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation. 2002;70(9-10):537-46.
7. Lee GY, Kenny PA, Lee EH, Bissell MJ. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods. 2007;4(4):359-65.
8. Ma XJ, Dahiya S, Richardson E, Erlander M, Sgroi DC. Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res. 2009;11(1):R7.
9. Hu M, Yao J, Cai L, Bachman KE, van den Brule F, Velculescu V, et al. Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet. 2005;37(8):899-905.
10. Sung KE, Yang N, Pehlke C, Keely PJ, Eliceiri KW, Friedl A, et al. Transition to invasion in breast cancer: a microfluidic in vitro model enables examination of spatial and temporal effects. Integr Biol. 2011;3(4):439-50.
11. Madar S, Goldstein I, Rotter V. Cancer associated fibroblasts'--more than meets the eye. Trends Mol Med. 2013;19(8):447-53.
12. Campbell I, Polyak K, Haviv I. Clonal mutations in the cancer-associated fibroblasts: the case against genetic coevolution. Cancer Res. 2009;69(17):6765-8. discussion 6769.
13. Qiu W, Hu M, Sridhar A, Opeskin K, Fox S, Shipitsin M, et al. No evidence of clonal somatic genetic alterations in cancer-associated fibroblasts from human breast and ovarian carcinomas. Nat Genet. 2008;40(5):650-5.
14. Augsten M. Cancer-associated fibroblasts as another polarized cell type of the tumor microenvironment. Front Oncol. 2014;4:62.
15. Tamm I, Cardinale I, Murphy JS. Decreased adherence of interleukin 6-treated breast carcinoma cells can lead to separation from neighbors after mitosis. Proc Natl Acad Sci U S A. 1991;88(10):4414-8.
16. Tamm I, Cardinale I, Kikuchi T, Krueger JG. E-cadherin distribution in interleukin 6-induced cell-cell separation of ductal breast carcinoma cells. Proc Natl Acad Sci U S A. 1994;91(10):4338-42.
17. Krueger J, Ray A, Tamm I, Sehgal PB. Expression and function of interleukin-6 in epithelial cells. J Cell Biochem. 1991;45(4):327-34.
18. Cheng GZ, Zhang WZ, Sun M, Wang Q, Coppola D, Mansour M, et al. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem. 2008;283(21):14665-73.
19. Sullivan NJ, Sasser AK, Axel AE, Vesuna F, Raman V, Ramirez N, et al. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene. 2009;28(33):2940-7.
20. Rose-John S, Heinrich PC. Soluble receptors for cytokines and growth factors: generation and biological function. Biochem J. 1994;300(Pt 2):281-90.
21. Mohamed MM, Cavallo-Medved D, Rudy D, Anbalagan A, Moin K, Sloane BF. Interleukin-6 increases expression and secretion of cathepsin B by breast tumor-associated monocytes. Cell Physiol Biochem. 2010;25(2-3):315-24.
22. Bengsch F, Buck A, Gunther SC, Seiz JR, Tacke M, Pfeifer D, et al. Cell type-dependent pathogenic functions of overexpressed human cathepsin B in murine breast cancer progression. Oncogene. 2013.
23. Hobisch A, Rogatsch H, Hittmair A, Fuchs D, Bartsch Jr G, Klocker H, et al. Immunohistochemical localization of interleukin-6 and its receptor in benign, premalignant and malignant prostate tissue. J Pathol. 2000;191(3):239-44.
24. Kinoshita T, Ito H, Miki C. Serum interleukin-6 level reflects the tumor proliferative activity in patients with colorectal carcinoma. Cancer. 1999;85(12):2526-31.
25. Guo Y, Xu F, Lu T, Duan Z, Zhang Z. Interleukin-6 signaling pathway in targeted therapy for cancer. Cancer Treat Rev. 2012;38(7):904-10.
26. Hartman ZC, Poage GM, den Hollander P, Tsimelzon A, Hill J, Panupinthu N, et al. Growth of triple-negative breast cancer cells relies upon coordinate autocrine expression of the proinflammatory cytokines IL-6 and IL-8. Cancer Res. 2013;73(11):3470-80.
27. Jiang XP, Yang DC, Elliott RL, Head JF. Down-regulation of expression of interleukin-6 and its receptor results in growth inhibition of MCF-7 breast cancer cells. Anticancer Res. 2011;31(9):2899-906.
28. Leslie K, Gao SP, Berishaj M, Podsypanina K, Ho H, Ivashkiv L, et al. Differential interleukin-6/Stat3 signaling as a function of cellular context mediates Ras-induced transformation. Breast Cancer Res. 2010;12(5):R80.
29. Lovitt CJ, Shelper TB, Avery VM. Evaluation of chemotherapeutics in a three-dimensional breast cancer model. J Cancer Res Clin Oncol. 2015;141(5):951-9.
30. Dawson PJ, Wolman SR, Tait L, Heppner GH, Miller FR. MCF10AT: a model for the evolution of cancer from proliferative breast disease. Am J Pathol. 1996;148(1):313-9.
31. Jedeszko C, Victor BC, Podgorski I, Sloane BF. Fibroblast hepatocyte growth factor promotes invasion of human mammary ductal carcinoma in situ. Cancer Res. 2009;69(23):9148-55.
32. Sameni M, Anbalagan A, Olive MB, Moin K, Mattingly RR, Sloane BF. MAME models for 4D live-cell imaging of tumor: microenvironment interactions that impact malignant progression. J Vis Exp. 2012;(60). doi: 10.3791/3661.
33. Cavallo-Medved D, Rudy D, Blum G, Bogyo M, Caglic D, Sloane BF. Live-cell imaging demonstrates extracellular matrix degradation in association with active cathepsin B in caveolae of endothelial cells during tube formation. Exp Cell Res. 2009;315(7):1234-46.
34. Sloane BF, Moin K, Sameni M, Tait LR, Rozhin J, Ziegler G. Membrane association of cathepsin B can be induced by transfection of human breast epithelial cells with c-Ha-ras oncogene. J Cell Sci. 1994;107(Pt 2):373-84.
35. Mullins SR, Sameni M, Blum G, Bogyo M, Sloane BF, Moin K. Three-dimensional cultures modeling premalignant progression of human breast epithelial cells: role of cysteine cathepsins. Biol Chem. 2012;393(12):1405-16.
36. Dethlefsen C, Hojfeldt G, Hojman P. The role of intratumoral and systemic IL-6 in breast cancer. Breast Cancer Res Treat. 2013;138(3):657-64.
37. Bachelot T, Ray-Coquard I, Menetrier-Caux C, Rastkha M, Duc A, Blay JY. Prognostic value of serum levels of interleukin 6 and of serum and plasma levels of vascular endothelial growth factor in hormone-refractory metastatic breast cancer patients. Br J Cancer. 2003;88(11):1721-6.
38. Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, Van Marck E, et al. Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer. 2003;103(5):642-6.
39. Yang L, Han S, Sun Y. An IL6-STAT3 loop mediates resistance to PI3K inhibitors by inducing epithelial-mesenchymal transition and cancer stem cell expansion in human breast cancer cells. Biochem Biophys Res Commun. 2014;453(3):582-7.
40. Hung SY, Shih YP, Chen M, Lo SH. Up-regulated cten by FGF2 contributes to FGF2-mediated cell migration. Mol Carcinog. 2014;53(10):787-92.
41. Patel NA, Patel PS, Vora HH. Role of PRL-3, Snail, Cytokeratin and Vimentin expression in epithelial mesenchymal transition in breast carcinoma. Breast Dis. 2014;35(2):113-127.
42. D'Angelo RC, Liu XW, Najy AJ, Jung YS, Won J, Chai KX, et al. TIMP-1 via TWIST1 induces EMT phenotypes in human breast epithelial cells. Mol Cancer Res. 2014;12(9):1324-33.
43. Ibrahim SA, Hassan H, Vilardo L, Kumar SK, Kumar AV, Kelsch R, et al. Syndecan-1 (CD138) modulates triple-negative breast cancer stem cell properties via regulation of LRP-6 and IL-6-mediated STAT3 signaling. PLoS One. 2013;8(12), e85737.
44. Guzman JR, Koo JS, Goldsmith JR, Muhlbauer M, Narula A, Jobin C. Oxymatrine prevents NF-kappaB nuclear translocation and ameliorates acute intestinal inflammation. Sci Rep. 2013;3:1629.
45. Cirri P, Chiarugi P. Cancer associated fibroblasts: the dark side of the coin. Am J Cancer Res. 2011;1(4):482-97.
46. Orimo A, Weinberg RA. Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle. 2006;5(15):1597-601.
47. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 1999;59(19):5002-11.
48. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A. 2002;99(20):12877-82.
49. Rowe RG, Keena D, Sabeh F, Willis AL, Weiss SJ. Pulmonary fibroblasts mobilize the membrane-tethered matrix metalloprotease, MT1-MMP, to destructively remodel and invade interstitial type I collagen barriers. Am J Physiol Lung Cell Mol Physiol. 2011;301(5):L683-92.
50. Holliday DL, Hughes S, Shaw JA, Walker RA, Jones JL. Intrinsic genetic characteristics determine tumor-modifying capacity of fibroblasts: matrix metalloproteinase-3 5A/5A genotype enhances breast cancer cell invasion. Breast Cancer Res. 2007;9(5):R67.
51. Casey T, Bond J, Tighe S, Hunter T, Lintault L, Patel O, et al. Molecular signatures suggest a major role for stromal cells in development of invasive breast cancer. Breast Cancer Res Treat. 2009;114(1):47-62.
52. Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell. 2011;147(5):992-1009.
53. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002;2(3):161-74.
54. O'Brien P, O'Connor BF. Seprase: an overview of an important matrix serine protease. Biochim Biophys Acta. 2008;1784(9):1130-45.
55. Linebaugh BE, Sameni M, Day NA, Sloane BF, Keppler D. Exocytosis of active cathepsin B enzyme activity at pH 7.0, inhibition and molecular mass. Eur J Biochem. 1999;264(1):100-9.
56. Nielsen BS, Rank F, Lopez JM, Balbin M, Vizoso F, Lund LR, et al. Collagenase-3 expression in breast myofibroblasts as a molecular marker of transition of ductal carcinoma in situ lesions to invasive ductal carcinomas. Cancer Res. 2001;61(19):7091-100.
57. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141(1):52-67.
58. Peters M, Muller AM, Rose-John S. Interleukin-6 and soluble interleukin-6 receptor: direct stimulation of gp130 and hematopoiesis. Blood. 1998;92(10):3495-504.
59. Ao M, Franco OE, Park D, Raman D, Williams K, Hayward SW. Cross-talk between paracrine-acting cytokine and chemokine pathways promotes malignancy in benign human prostatic epithelium. Cancer Res. 2007;67(9):4244-53.
60. Franco OE, Jiang M, Strand DW, Peacock J, Fernandez S, Jackson 2nd RS, et al. Altered TGF-beta signaling in a subpopulation of human stromal cells promotes prostatic carcinogenesis. Cancer Res. 2011;71(4):1272-81.
61. Hendrayani SF, Al-Khalaf HH, Aboussekhra A. The Cytokine IL-6 Reactivates Breast Stromal Fibroblasts through Transcription Factor STAT3-dependent Up-regulation of the RNA Binding Protein AUF1. J Biol Chem. 2014.
62. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121(3):335-48.
63. Cho YA, Sung MK, Yeon JY, Ro J, Kim J. Prognostic role of interleukin-6, interleukin-8, and leptin levels according to breast cancer subtype. Cancer Res Treat. 2013;45(3):210-9.
64. Narita D, Seclaman E, Ursoniu S, Ilina R, Cireap N, Anghel A. Expression of CCL18 and interleukin-6 in the plasma of breast cancer patients as compared with benign tumor patients and healthy controls. Rom J Morphol Embryol. 2011;52(4):1261-7.
65. Ravishankaran P, Karunanithi R. Clinical significance of preoperative serum interleukin-6 and C-reactive protein level in breast cancer patients. World J Surg Oncol. 2011;9:18.
66. Franco OE, Shaw AK, Strand DW, Hayward SW. Cancer associated fibroblasts in cancer pathogenesis. Semin Cell Dev Biol. 2010;21(1):33-9.
67. Laoui D, Movahedi K, Van Overmeire E, Van den Bossche J, Schouppe E, Mommer C, et al. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int J Dev Biol. 2011;55(7-9):861-7.
68. Medrek C, Ponten F, Jirstrom K, Leandersson K. The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients. BMC Cancer. 2012;12:306.
69. Rudnick JA, Kuperwasser C. Stromal biomarkers in breast cancer development and progression. Clin Exp Metastasis. 2012;29(7):663-72.
70. Palucka K, Coussens LM, O'Shaughnessy J. Dendritic cells, inflammation, and breast cancer. Cancer J. 2013;19(6):511-6.
71. Kees T, Egeblad M. Innate immune cells in breast cancer--from villains to heroes? J Mammary Gland Biol Neoplasia. 2011;16(3):189-203.
72. Fridman WH, Galon J, Pages F, Tartour E, Sautes-Fridman C, Kroemer G. Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res. 2011;71(17):5601-5.
73. DeNardo DG, Coussens LM. Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res. 2007;9(4):212.
74. Wilson KS, Roberts H, Leek R, Harris AL, Geradts J. Differential gene expression patterns in HER2/neu-positive and -negative breast cancer cell lines and tissues. Am J Pathol. 2002;161(4):1171-85.
75. Kim G, Ouzounova M, Quraishi AA, Davis A, Tawakkol N, Clouthier SG, et al. SOCS3-mediated regulation of inflammatory cytokines in PTEN and p53 inactivated triple negative breast cancer model. Oncogene. 2015;34(6):671-80.
76. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol. 2007;9(12):1392-400.
77. Sung KE, Su X, Berthier E, Pehlke C, Friedl A, Beebe DJ. Understanding the impact of 2D and 3D fibroblast cultures on in vitro breast cancer models. PLoS One. 2013;8(10), e76373.
78. To Y, Dohi M, Matsumoto K, Tanaka R, Sato A, Nakagome K, et al. A two-way interaction between hepatocyte growth factor and interleukin-6 in tissue invasion of lung cancer cell line. Am J Respir Cell Mol Biol. 2002;27(2):220-6.
79. Krishnamurthy S, Warner KA, Dong Z, Imai A, Nor C, Ward BB, et al. Endothelial interleukin-6 defines the tumorigenic potential of primary human cancer stem cells. Stem Cells. 2014;32(11):2845-57.
80. Yu Y, Xiao CH, Tan LD, Wang QS, Li XQ, Feng YM. Cancer-associated fibroblasts induce epithelial-mesenchymal transition of breast cancer cells through paracrine TGF-beta signalling. Br J Cancer. 2014;110(3):724-32.
81. Zhang XL, Topley N, Ito T, Phillips A. Interleukin-6 regulation of transforming growth factor (TGF)-beta receptor compartmentalization and turnover enhances TGF-beta1 signaling. J Biol Chem. 2005;280(13):12239-45.
82. Nishimoto N, Terao K, Mima T, Nakahara H, Takagi N, Kakehi T. Mechanisms and pathologic significances in increase in serum interleukin-6 (IL-6) and soluble IL-6 receptor after administration of an anti-IL-6 receptor antibody, tocilizumab, in patients with rheumatoid arthritis and Castleman disease. Blood. 2008;112(10):3959-64.
83. Voorhees PM, Manges RF, Sonneveld P, Jagannath S, Somlo G, Krishnan A, et al. A phase 2 multicentre study of siltuximab, an anti-interleukin-6 monoclonal antibody, in patients with relapsed or refractory multiple myeloma. Br J Haematol. 2013;161(3):357-66.
84. Rossi JF, Negrier S, James ND, Kocak I, Hawkins R, Davis H, et al. A phase I/II study of siltuximab (CNTO 328), an anti-interleukin-6 monoclonal antibody, in metastatic renal cell cancer. Br J Cancer. 2010;103(8):1154-62.
85. Hunsucker SA, Magarotto V, Kuhn DJ, Kornblau SM, Wang M, Weber DM, et al. Blockade of interleukin-6 signalling with siltuximab enhances melphalan cytotoxicity in preclinical models of multiple myeloma. Br J Haematol. 2011;152(5):579-92.
86. Dorff TB, Goldman B, Pinski JK, Mack PC, Lara Jr PN, Van Veldhuizen Jr PJ, et al. Clinical and correlative results of SWOG S0354: a phase II trial of CNTO328 (siltuximab), a monoclonal antibody against interleukin-6, in chemotherapy-pretreated patients with castration-resistant prostate cancer. Clin Cancer Re. 2010;16(11):3028-34.
87. Johnson and Johnson (Janssen Biotech I. SYLVANT™ (siltuximab) Receives FDA Approval to Treat Multicentric Castleman's Disease (MCD). www.jnj.com/news/all/sylvant . 2014.
88. Song L, Smith MA, Doshi P, Sasser K, Fulp W, Altiok S, et al. Antitumor efficacy of the anti-interleukin-6 (IL-6) antibody siltuximab in mouse xenograft models of lung cancer. J Thorac Oncol. 2014;9(7):974-82.
89. Coward J, Kulbe H, Chakravarty P, Leader D, Vassileva V, Leinster DA, et al. Interleukin-6 as a therapeutic target in human ovarian cancer. Clin Cancer Res. 2011;17(18):6083-96.
90. Axel A, Casneuf T, King P, Alvarez J, Hall B, Sasser K. Abstract 3530: The role of IL-6 in ER + breast cancer and potential use for Siltuximab, an anti-IL-6 antibody, in ER + breast cancer treatment. Cancer Res. 2013;73(8 Supplement):3530-0.