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CCL8 mediates crosstalk between endothelial colony forming cells and triple-negative breast cancer cells through IL-8, aggravating invasion and tumorigenicity

Oncogene volume 40, pages 3245–3259 (2021)Cite this article

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Abstract

Triple-negative breast cancer (TNBC) is an aggressive type of breast cancer with a poor prognosis for which no effective therapeutic measures are currently available. The present study aimed to investigate whether interactions with endothelial colony-forming cells (ECFCs) promote aggressive progression of TNBC cells. Herein, using an indirect co-culture system, we showed that co-culture increased the invasive and migratory phenotypes of both MDA-MB-231 TNBC cells and ECFCs. Through a cytokine antibody array and RT-PCR analysis, we revealed that co-culture markedly induced secretion of the chemokine C-C motif ligand (CCL)8 from ECFCs and that of interleukin (IL)-8 from MDA-MB-231 cells. CCL8 was crucial for ECFC-induced IL-8 secretion and invasion of MDA-MB-231 cells as well as for MDA-MB-231-enhanced MMP-2 secretion and angiogenesis of ECFCs. We suggest c-Jun as a transcription factor for CCL8-induced IL-8 expression in MDA-MB-231 cells. IL-8 was important for co-culture-induced CCL8 and MMP-2 upregulation and invasion of ECFCs. Notably, our findings reveal a positive feedback loop between CCL8 and IL-8, which contributes to the aggressive phenotypes of both ECFC and TNBC cells. Using an MDA-MB-231 cell-based xenograft model, we show that tumor growth and metastasis are increased by co-injected ECFCs in vivo. Increased expression of IL-8 was observed in tissues with bone metastases in mice injected with conditioned media from co-cultured cells. High IL-8 levels are correlated with poor recurrence-free survival in TNBC patients. Together, these results suggest that CCL8 and IL-8 mediate the crosstalk between ECFCs and TNBC, leading to aggravation of tumorigenicity in TNBC.

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Fig. 1: ECFCs increase proliferation, invasion, migration, and anchorage-independent growth in MDA-MB-231 TNBC cells.
Fig. 2: The invasive, migratory, and angiogenic properties and MMP-2 expression of ECFCs are enhanced by co-culture with MDA-MB-231 cells.
Fig. 3: Co-culture induces secretion of IL-8 from MDA-MB-231 cells and secretion of CCL8 and PDGF-BB from ECFCs.
Fig. 4: CCL8 is crucial for ECFC-induced IL-8 expression and invasion of MDA-MB-231 cells as well as MDA-MB-231-enhanced MMP-2 and angiogenesis of ECFCs.
Fig. 5: c-Jun is involved in transcription of IL-8 induced by ECFCs and CCL8.
Fig. 6: Tumor growth, metastasis, and expression of CCL8 and IL-8 are increased by ECFCs in vivo.

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References

  1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010;60:277–300.

    Article  PubMed  Google Scholar 

  2. Yin WJ, Lu JS, Di GH, Lin YP, Zhou LH, Liu GY, et al. Clinicopathological features of the triple-negative tumors in Chinese breast cancer patients. Breast Cancer Res Treat. 2009;115:325–33.

    Article  PubMed  Google Scholar 

  3. André F, Zielinski CC. Optimal strategies for the treatment of metastatic triple-negative breast cancer with currently approved agents. Ann Oncol. 2012;23:46–51.

    Article  Google Scholar 

  4. Le Bourhis X, Romon R, Hondermarck H. Role of endothelial progenitor cells in breast cancer angiogenesis: from fundamental research to clinical ramifications. Breast Cancer Res Treat. 2010;120:17–24.

    Article  PubMed  Google Scholar 

  5. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1:27–31.

    Article  CAS  PubMed  Google Scholar 

  6. Khodarev NN, Yu J, Labay E, Darga T, Brown CK, Mauceri HJ, et al. Tumour-endothelium interactions in co-culture: coordinated changes of gene expression profiles and phenotypic properties of endothelial cells. J Cell Sci. 2003;116:1013–22.

    Article  CAS  PubMed  Google Scholar 

  7. Hoffmann OI, Ilmberger C, Magosch S, Joka M, Jauch KW, Mayer B. Impact of the spheroid model complexity on drug response. J Biotechnol. 2015;205:14–23.

    Article  CAS  PubMed  Google Scholar 

  8. Zhang W, Xu J, Fang H, Tang L, Chen W, Sun Q, et al. Endothelial cells promote triple-negative breast cancer cell metastasis via PAI-1 and CCL5 signaling. FASEB J. 2018;32:276–88.

    Article  CAS  PubMed  Google Scholar 

  9. Zhao K, Yao Y, Luo X, Lin B, Huang Y, Zhou Y, et al. LYG-202 inhibits activation of endothelial cells and angiogenesis through CXCL12/CXCR7 pathway in breast cancer. Carcinogenesis. 2018;39:588–600.

    Article  CAS  PubMed  Google Scholar 

  10. Delia D, Lampugnani M, Resnati M, Dejana E, Aiello A, Fontanella E, et al. CD34 expression is regulated reciprocally with adhesion molecules in vascular endothelial cells in vitro. Blood. 1993;81:1001–8.

    Article  CAS  PubMed  Google Scholar 

  11. Melero-Martin JM, Khan ZA, Picard A, Wu X, Paruchuri S, Bischoff J. In vivo vasculogenic potential of human bloodderived endothelial progenitor cells. Blood. 2007;109:4761–8.

    Article  CAS  PubMed  Google Scholar 

  12. Arnaoutova I, Kleinman HK. In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc. 2010;5:628–35.

    Article  CAS  PubMed  Google Scholar 

  13. Kwon YH, Lee JH, Jung SY, Kim JW, Lee SH, Lee DH, et al. Phloroglucinol inhibits the in vitro differentiation potential of CD34 positive cells into endothelial progenitor cells. Biomol Ther (Seoul). 2012;20:158–64.

    Article  CAS  Google Scholar 

  14. Fadini GP, Losordo D, Dimmeler S. Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res. 2012;110:624–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104:2752–60.

    Article  CAS  PubMed  Google Scholar 

  16. Finkenzeller G, Graner S, Kirkpatrick CJ, Fuchs S, Stark GB. Impaired in vivo vasculogenic potential of endothelial progenitor cells in comparison to human umbilical vein endothelial cells in a spheroid-based implantation model. Cell Prolif. 2009;42:498–505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Smadja DM, d’Audigier C, Weiswald LB, Badoual C, Dangles-Marie V, Mauge L, et al. The Wnt antagonist Dickkopf-1 increases endothelial progenitor cell angiogenic potential. Arterioscler Thromb Vasc Biol. 2010;30:2544–52.

    Article  CAS  PubMed  Google Scholar 

  18. Liu L, Shi GP. CD31: beyond a marker for endothelial cells. Cardiovasc Res. 2012;94:3–5.

    Article  CAS  PubMed  Google Scholar 

  19. Tsutsui S, Kume M, Era S. Prognostic value of microvessel density in invasive ductal carcinoma of the breast. Breast Cancer. 2003;10:312–9.

    Article  PubMed  Google Scholar 

  20. Afshar Moghaddam N, Mahsuni P, Taheri D. Evaluation of endoglin as an angiogenesis marker in glioblastoma. Iran J Pathol. 2015;10:89–96.

    PubMed  PubMed Central  Google Scholar 

  21. Bianconi D, Herac M, Posch F, Schmeidl M, Unseld M, Kieler M, et al. Microvascular density assessed by CD31 predicts clinical benefit upon bevacizumab treatment in metastatic colorectal cancer. Ther Adv Med Oncol. 2020. https://doi.org/10.1177/1758835920928635.

  22. Miettinen M, Lindenmayer AE, Chaubal A. Endothelial cell markers CD31, CD34, and BNH9 antibody to H- and Y-antigens-evaluation of their specificity and sensitivity in the diagnosis of vascular tumors and comparison with von Willebrand factor. Mod Pathol. 1994;7:82–90.

    CAS  PubMed  Google Scholar 

  23. McKenney JK, Weiss SW, Folpe AL. CD31 expression in intratumoral macrophages: a potential diagnostic pitfall. Am J Surg Pathol. 2001;25:1167–73.

    Article  CAS  PubMed  Google Scholar 

  24. Medrek C, Pontén F, Jirström 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Connolly KM, Bogdanffy MS. Evaluation of proliferating cell nuclear antigen (PCNA) as an endogenous marker of cell proliferation in rat liver: a dual-stain comparison with 5-bromo-2’-deoxyuridine. J Histochem Cytochem. 1993;41:1–6.

    Article  CAS  PubMed  Google Scholar 

  26. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol. 2000;2:737–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zheng H, Takahashi H, Murai Y, Cui Z, Nomoto K, Niwa H, et al. Expressions of MMP-2, MMP-9 and VEGF are closely linked to growth, invasion, metastasis and angiogenesis of gastric carcinoma. Anticancer Res. 2006;26:3579–83.

    CAS  PubMed  Google Scholar 

  28. An G, Wu F, Huang S, Feng L, Bai J, Gu S, et al. Effects of CCL5 on the biological behavior of breast cancer and the mechanisms of its interaction with tumor-associated macrophages. Oncol Rep. 2019;42:2499–511.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Halvorsen EC, Hamilton MJ, Young A, Wadsworth BJ, LePard NE, Lee HN, et al. Maraviroc decreases CCL8-mediated migration of CCR5(+) regulatory T cells and reduces metastatic tumor growth. Oncoimmunology. 2016;5:e1150398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Khanjani S, Terzidou V, Johnson MR, Bennett PR. NFκB and AP-1 drive human myometrial IL8 expression. Mediators Inflamm. 2012;2012:504952.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Riedlinger T, Liefke R, Meier-Soelch J, Jurida L, Nist A, Stiewe T, et al. NF-κB p65 dimerization and DNA-binding is important for inflammatory gene expression. FASEB J. 2019;33:4188–202.

    Article  CAS  PubMed  Google Scholar 

  32. Bettelli E, Dastrange M, Oukka M. Foxp3 interacts with nuclear factor of activated T cells and NF-kappa B to repress cytokine gene expression and effector functions of T helper cells. Proc Natl Acad Sci U.S.A. 2005;102:5138–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Matthews JR, Hay RT. Regulation of the DNA binding activity of NF-kappa B. Int J Biochem Cell Biol. 1995;27:865–79.

    Article  CAS  PubMed  Google Scholar 

  34. Gómez-Cuadrado L, Tracey N, Ma R, Qian B, Brunton VG. Mouse models of metastasis: progress and prospects. Dis Model Mech. 2017;10:1061–74.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1809 patients. Breast Cancer Res Treat. 2010;123:725–31.

    Article  PubMed  CAS  Google Scholar 

  36. Uzzan B, Nicolas P, Cucherat M, Perret GY. Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res. 2004;64:2941–55.

    Article  CAS  PubMed  Google Scholar 

  37. Vasudev NS, Reynolds AR. Anti-angiogenic therapy for cancer: current progress, unresolved questions and future directions. Angiogenesis. 2014;17:471–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Neophytou C, Boutsikos P, Papageorgis P. Molecular mechanisms and emerging therapeutic targets of triple-negative breast cancer metastasis. Front Oncol. 2018;8:31.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Paschalaki KE, Randi AM. Recent advances in endothelial colony forming cellstoward their use in clinical translation. Front Med (Lausanne). 2018;5:295.

    Article  Google Scholar 

  40. Zhou J, Zheng S, Liu T, Liu Q, Chen Y, Tan D, et al. MCP2 activates NF-κB signaling pathway promoting the migration and invasion of ESCC cells. Cell Biol Int. 2018;42:365–72.

    Article  CAS  PubMed  Google Scholar 

  41. Farmaki E, Chatzistamou I, Kaza V, Kiaris H. A CCL8 gradient drives breast cancer cell dissemination. Oncogene. 2016;35:6309–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Cassetta L, Fragkogianni S, Sims AH, Swierczak A, Forrester LM, Zhang H, et al. Human tumor-associated macrophage and monocyte transcriptional landscapes reveal cancer-specific reprogramming, biomarkers, and therapeutic targets. Cancer Cell. 2019;35:588–602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Freund A, Chauveau C, Brouillet J-P, Lucas A, Lacroix M, Licznar A, et al. IL-8 expression and its possible relationship with estrogen-receptor-negative status of breast cancer cells. Oncogene. 2003;22:256–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Snoussi K, Mahfoudh W, Bouaouina N, Ahmed SB, Helal AN, Chouchane L. Genetic variation in IL-8 associated with increased risk and poor prognosis of breast carcinoma. Hum Immunol. 2006;67:13–21.

    Article  CAS  PubMed  Google Scholar 

  45. Snoussi K, Mahfoudh W, Bouaouina, Fekih M, Khairi H, Helal AN, et al. Combined effects of IL-8 and CXCR2 gene polymorphisms on breast cancer susceptibility and aggressiveness. BMC Cancer. 2010;10:283.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Kivistö KT, Kroemer HK, Eichelbaum M. The role of human cytochrome P450 enzymes in the metabolism of anticancer agents: implications for drug interactions. Br J Clin Pharm. 1995;40:523–30.

    Article  Google Scholar 

  47. Singh JK, Simões BM, Howell SJ, Farnie G, Clarke RB. Recent advances reveal IL-8 signaling as a potential key to targeting breast cancer stem cells. Breast Cancer Res. 2013;15:210.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Rody A, Karn T, Liedtke C, Pusztai L, Ruckhaeberle E, Hanker L, et al. A clinically relevant gene signature in triple negative and basal-like breast cancer. Breast Cancer Res. 2011;13:R97.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Engels K, Fox SB, Whitehouse RM, Gatter KC, Harris AL. Distinct angiogenic patterns are associated with high-grade in situ ductal carcinomas of the breast. J Pathol. 1997;181:207–12.

    Article  CAS  PubMed  Google Scholar 

  50. Sato T, Takemura T, Ouchi T, Mori S, Sakamoto M, Arai Y, et al. Monitoring of blood vessel density using contrast-enhanced high frequency ultrasound may facilitate early diagnosis of lymph node metastasis. J Cancer. 2017;8:704–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Miller LJ, Kurtzman SH, Wang Y, Anderson KH, Lindquist RR, Kreutzer DL. Expression of interleukin-8 receptors on tumor cells and vascular endothelial cells in human breast cancer tissue. Anticancer Res. 1998;18:77–81.

    CAS  PubMed  Google Scholar 

  52. Yuan A, Yu CJ, Luh KT, Kuo SH, Lee YC, Yang PC. Aberrant p53 expression correlates with expression of vascular endothelial growth factor mRNA and interleukin-8 mRNA and neoangiogenesis in non-small-cell lung cancer. J Clin Oncol. 2002;20:900–10.

    CAS  PubMed  Google Scholar 

  53. Huang S, Mills L, Mian B, Tellez C, McCarty M, Yang XD, et al. Fully humanized neutralizing antibodies to interleukin-8 (ABX-IL8) inhibit angiogenesis, tumor growth, and metastasis of human melanoma. Am J Pathol. 2002;161:125–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Weidner N, Folkman J, Pozza F, Bevilacqua P, Allred EN, Moore DH, et al. Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst. 1992;84:1875–87.

    Article  CAS  PubMed  Google Scholar 

  55. Sunaga N, Kaira K, Tomizawa Y, Shimizu K, Imai H, Takahashi G, et al. Clinicopathological and prognostic significance of interleukin-8 expression and its relationship to KRAS mutation in lung adenocarcinoma. Br J Cancer. 2014;110:2047–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lambert E, Dassé E, Haye B, Petitfrère E. TIMPs as multifacial proteins. Crit Rev Oncol Hematol. 2004;49:187–98.

    Article  PubMed  Google Scholar 

  57. Li A, Dubey S, Varney ML, Dave BJ, Singh RK. IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol. 2003;170:3369–76.

    Article  CAS  PubMed  Google Scholar 

  58. Velasco-Velazquez M, Jiao X, De La Fuente M, Pestell TG, Ertel A, Lisanti MP, et al. CCR5 antagonist blocks metastasis of basal breast cancer cells. Cancer Res. 2012;72:3839–50.

    Article  CAS  PubMed  Google Scholar 

  59. Sicoli D, Jiao X, Ju X, Velasco-Velazquez M, Ertel A, Addya S, et al. CCR5 receptor antagonists block metastasis to bone of v-Src oncogene-transformed metastatic prostate cancer cell lines. Cancer Res. 2014;74:7103–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Halama N, Zoernig I, Berthel A, Kahlert C, Klupp F, Suarez-Carmona M, et al. Tumoral immune cell exploitation in colorectal cancer metastases can be targeted effectively by Anti-CCR5 therapy in cancer patients. Cancer Cell. 2016;29:587–601.

    Article  CAS  PubMed  Google Scholar 

  61. Lee HM, Moon A. Amygdalin regulates apoptosis and adhesion in Hs578T triple-negative breast cancer cells. Biomol Ther (Seoul). 2016;24:62–6.

    Article  CAS  Google Scholar 

  62. Melero-Martin JM, De Obaldia ME, Kang SY, Khan ZA, Yuan L, Oettgen P, et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res. 2008;103:194–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lee H, Kang KT. Advanced tube formation assay using human endothelial colonyforming cells for in vitro evaluation of angiogenesis. Korean J Physiol Pharm. 2018;22:705–12.

    Article  CAS  Google Scholar 

  64. Song H, Ki SH, Kim SG, Moon A. Activating transcription factor 2 mediates matrix metalloproteinase-2 transcriptional activation induced by p38 in breast epithelial cells. Cancer Res. 2006;66:10487–96.

    Article  CAS  PubMed  Google Scholar 

  65. Fong YC, Maa MC, Tsai FJ, Chen WC, Lin JG, Jeng LB, et al. Osteoblast-derived TGF-beta1 stimulates IL-8 release through AP-1 and NF-kappaB in human cancer cells. J Bone Min Res. 2008;23:961–70.

    Article  CAS  Google Scholar 

  66. Mencarelli A, Graziosi L, Renga B, Cipriani S, D’Amore C, Francisci D, et al. CCR5 antagonism by maraviroc reduces the potential for gastric cancer cell dissemination. Transl Oncol. 2013;6:784–93.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Zhang X, Chen L, Dang W-Q, Cao M-F, Xiao JF, Lv SQ, et al. CCL8 secreted by tumor-associated macrophages promotes invasion and stemness of glioblastoma cells via ERK1/2 signaling. Lab Invest. 2020;100:619–29.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The present study was supported by the National Research Foundation of Korea (no. 2016R1A6A1A03007648 and no. 2019R1A2C1009773).

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Authors and Affiliations

  1. Duksung Innovative Drug Center, College of Pharmacy, Duksung Women’s University, Seoul, Korea

    Eun-Sook Kim, Su-Min Nam, Seungeun Lee, Kyoungmee Kim, Hyun Kyung Lim, Hyunsook Lee, Kyu-Tae Kang, Joohee Jung & Aree Moon

  2. College of Chemistry, Duksung Women’s University, Seoul, Korea

    Hye Kyung Song

  3. College of Pharmacy, Chung-Ang University, Seoul, Korea

    Yeo-Jung Kwon & Young-Jin Chun

  4. Department of Pathology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea

    So Yeon Park

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Kim, ES., Nam, SM., Song, H.K. et al. CCL8 mediates crosstalk between endothelial colony forming cells and triple-negative breast cancer cells through IL-8, aggravating invasion and tumorigenicity. Oncogene 40, 3245–3259 (2021). https://doi.org/10.1038/s41388-021-01758-w

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