Skip to main content

Advertisement

SpringerLink
Log in

Breast cancers from black women exhibit higher numbers of immunosuppressive macrophages with proliferative activity and of crown-like structures associated with lower survival compared to non-black Latinas and Caucasians

  • Epidemiology
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

Racial disparities in breast cancer incidence and outcome are a major health care challenge. Patients in the black race group more likely present with an early onset and more aggressive disease. The occurrence of high numbers of macrophages is associated with tumor progression and poor prognosis in solid malignancies. Macrophages are observed in adipose tissues surrounding dead adipocytes in “crown-like structures” (CLS). Here we investigated whether the numbers of CD163+ tumor-associated macrophages (TAMs) and/or CD163+ CLS are associated with patient survival and whether there are significant differences across blacks, non-black Latinas, and Caucasians. Our findings confirm that race is statistically significantly associated with the numbers of TAMs and CLS in breast cancer, and demonstrate that the highest numbers of CD163+ TAM/CLS are found in black breast cancer patients. Our results reveal that the density of CD206 (M2) macrophages is a significant predictor of progression-free survival univariately and is also significant after adjusting for race and for HER2, respectively. We examined whether the high numbers of TAMs detected in tumors from black women were associated with macrophage proliferation, using the Ki-67 nuclear proliferation marker. Our results reveal that TAMs actively divide when in contact with tumor cells. There is a higher ratio of proliferating macrophages in tumors from black patients. These findings suggest that interventions based on targeting TAMs may not only benefit breast cancer patients in general but also serve as an approach to remedy racial disparity resulting in better prognosis patients from minority racial groups.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Cancer Facts and Figures 2014 (2014) American Cancer Society, Atlanta

  2. Porter PL, Lund MJ, Lin MG, Yuan X, Liff JM, Flagg EW, Coates RJ, Eley JW (2004) Racial differences in the expression of cell cycle-regulatory proteins in breast carcinoma. Cancer 100(12):2533–2542. doi:10.1002/cncr.20279

    Article  PubMed  Google Scholar 

  3. Henderson BE, Lee NH, Seewaldt V, Shen H (2012) The influence of race and ethnicity on the biology of cancer. Nat Rev Cancer 12(9):648–653. doi:10.1038/nrc3341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kolonel LN, Altshuler D, Henderson BE (2004) The multiethnic cohort study: exploring genes, lifestyle and cancer risk. Nat Rev Cancer 4(7):519–527. doi:10.1038/nrc1389

    Article  CAS  PubMed  Google Scholar 

  5. Amend K, Hicks D, Ambrosone CB (2006) Breast cancer in African-American women: differences in tumor biology from European-American women. Cancer Res 66(17):8327–8330. doi:10.1158/0008-5472.CAN-06-1927

    Article  CAS  PubMed  Google Scholar 

  6. Furberg H, Millikan R, Dressler L, Newman B, Geradts J (2001) Tumor characteristics in African American and white women. Breast Cancer Res Treat 68(1):33–43. doi:10.1023/A:1017994726207

    Article  CAS  PubMed  Google Scholar 

  7. Martin DN, Boersma BJ, Yi M, Reimers M, Howe TM, Yfantis HG, Tsai YC, Williams EH, Lee DH, Stephens RM, Weissman AM, Ambs S (2009) Differences in the Tumor Microenvironment between African-American and European-American Breast Cancer Patients. PLoS One 4(2):e4531. doi:10.1371/journal.pone.0004531

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jatoi I, Becher H, Leake CR (2003) Widening disparity in survival between white and African-American patients with breast carcinoma treated in the U. S. Department of Defense Healthcare system. Cancer 98(5):894–899. doi:10.1002/cncr.11604

    Article  PubMed  Google Scholar 

  9. Newman LA, Griffith KA, Jatoi I, Simon MS, Crowe JP, Colditz GA (2006) Meta-analysis of survival in African American and white American patients with breast cancer: ethnicity compared with socioeconomic status. J Clin Oncol Off J Am Soc Clin Oncol 24(9):1342–1349. doi:10.1200/JCO.2005.03.3472

    Article  Google Scholar 

  10. Elledge RM, Clark GM, Chamness GC, Osborne CK (1994) Tumor biologic factors and breast cancer prognosis among white, Hispanic, and black women in the United States. J Natl Cancer Inst 86(9):705–712. doi:10.1158/0008-5472.CAN-06-1927

    Article  CAS  PubMed  Google Scholar 

  11. Chlebowski RT, Chen Z, Anderson GL, Rohan T, Aragaki A, Lane D, Dolan NC, Paskett ED, McTiernan A, Hubbell FA, Adams-Campbell LL, Prentice R (2005) Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 97(6):439–448. doi:10.1093/jnci/dji064

    Article  PubMed  Google Scholar 

  12. Churpek JE, Walsh T, Zheng Y, Moton Z, Thornton AM, Lee MK, Casadei S, Watts A, Neistadt B, Churpek MM, Huo D, Zvosec C, Liu F, Niu Q, Marquez R, Zhang J, Fackenthal J, King MC, Olopade OI (2015) Inherited predisposition to breast cancer among African American women. Breast Cancer Res Treat 149(1):31–39. doi:10.1007/s10549-014-3195-0

    Article  CAS  PubMed  Google Scholar 

  13. Mahmoud SM, Lee AH, Paish EC, Macmillan RD, Ellis IO, Green AR (2012) Tumour-infiltrating macrophages and clinical outcome in breast cancer. J Clin Pathol 65(2):159–163. doi:10.1136/jclinpath-2011-200355

    Article  CAS  PubMed  Google Scholar 

  14. Bingle L, Brown NJ, Lewis CE (2002) The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 196(3):254–265. doi:10.1002/path.1027

    Article  CAS  PubMed  Google Scholar 

  15. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, Huhn RD, Song W, Li D, Sharp LL, Torigian DA, O’Dwyer PJ, Vonderheide RH (2011) CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331(6024):1612–1616. doi:10.1126/science.1198443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kondo T, Tsunematsu T, Yamada A, Arakaki R, Saito M, Otsuka K, Kujiraoka S, Ushio A, Kurosawa M, Kudo Y, Ishimaru N (2016) Acceleration of tumor growth due to dysfunction in M1 macrophages and enhanced angiogenesis in an animal model of autoimmune disease. Lab Investig J Tech Methods Pathol 96(4):468–480. doi:10.1038/labinvest.2015.166

    Article  CAS  Google Scholar 

  17. Balkwill F, Charles KA, Mantovani A (2005) Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7(3):211–217. doi:10.1016/j.ccr.2005.02.013

    Article  CAS  PubMed  Google Scholar 

  18. Grivennikov SI, Greten FR, Karin M (2010) Immunity, inflammation, and cancer. Cell 140(6):883–899. doi:10.1016/j.cell.2010.01.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23(11):549–555. doi:10.1016/S1471-4906(02)02302-5

    Article  CAS  PubMed  Google Scholar 

  20. Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4(1):71–78. doi:10.1038/nrc1256

    Article  CAS  PubMed  Google Scholar 

  21. Noy R, Pollard JW (2014) Tumor-associated macrophages: from mechanisms to therapy. Immunity 41(1):49–61. doi:10.1016/j.immuni.2014.06.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Torroella-Kouri M, Ma X, Perry G, Ivanova M, Cejas PJ, Owen JL, Iragavarapu-Charyulu V, Lopez DM (2005) Diminished expression of transcription factors nuclear factor kappaB and CCAAT/enhancer binding protein underlies a novel tumor evasion mechanism affecting macrophages of mammary tumor-bearing mice. Cancer Res 65(22):10578–10584. doi:10.1158/0008-5472.CAN-05-0365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Torroella-Kouri M, Silvera R, Rodriguez D, Caso R, Shatry A, Opiela S, Ilkovitch D, Schwendener RA, Iragavarapu-Charyulu V, Cardentey Y, Strbo N, Lopez DM (2009) Identification of a subpopulation of macrophages in mammary tumor-bearing mice that are neither M1 nor M2 and are less differentiated. Cancer Res 69(11):4800–4809. doi:10.1158/0008-5472.CAN-08-3427

    Article  CAS  PubMed  Google Scholar 

  24. Rodriguez D, Silvera R, Carrio R, Nadji M, Caso R, Rodriguez G, Iragavarapu-Charyulu V, Torroella-Kouri M (2013) Tumor microenvironment profoundly modifies functional status of macrophages: peritoneal and tumor-associated macrophages are two very different subpopulations. Cell Immunol 283(1–2):51–60. doi:10.1016/j.cellimm.2013.06.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Torroella-Kouri M, Rodriguez D, Caso R (2013) Alterations in macrophages and monocytes from tumor-bearing mice: evidence of local and systemic immune impairment. Immunol Res 57(1–3):86–98. doi:10.1007/s12026-013-8438-3

    Article  CAS  PubMed  Google Scholar 

  26. Yuan A, Hsiao YJ, Chen HY, Chen HW, Ho CC, Chen YY, Liu YC, Hong TH, Yu SL, Chen JJ, Yang PC (2015) Opposite effects of M1 and M2 macrophage subtypes on lung cancer progression. Sci Rep 5:14273. doi:10.1038/srep14273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Investig 117(1):175–184. doi:10.1172/JCI29881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, Wang S, Fortier M, Greenberg AS, Obin MS (2005) Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 46(11):2347–2355. doi:10.1194/jlr.M500294-JLR200

    Article  CAS  PubMed  Google Scholar 

  29. Morris PG, Hudis CA, Giri D, Morrow M, Falcone DJ, Zhou XK, Du B, Brogi E, Crawford CB, Kopelovich L, Subbaramaiah K, Dannenberg AJ (2011) Inflammation and increased aromatase expression occur in the breast tissue of obese women with breast cancer. Cancer Prev Res (Phila) 4(7):1021–1029. doi:10.1158/1940-6207.CAPR-11-0110

    Article  CAS  Google Scholar 

  30. Subbaramaiah K, Howe LR, Bhardwaj P, Du B, Gravaghi C, Yantiss RK, Zhou XK, Blaho VA, Hla T, Yang P, Kopelovich L, Hudis CA, Dannenberg AJ (2011) Obesity is associated with inflammation and elevated aromatase expression in the mouse mammary gland. Cancer Prev Res (Phila) 4(3):329–346. doi:10.1158/1940-6207.CAPR-10-0381

    Article  CAS  Google Scholar 

  31. Santander AM, Lopez-Ocejo O, Casas O, Agostini T, Sanchez L, Lamas-Basulto E, Carrio R, Cleary MP, Gonzalez-Perez RR, Torroella-Kouri M (2015) Paracrine interactions between adipocytes and tumor cells recruit and modify macrophages to the mammary tumor microenvironment: the role of obesity and inflammation in breast adipose tissue. Cancers 7(1):143–178. doi:10.3390/cancers7010143

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nelson LR, Bulun SE (2001) Estrogen production and action. J Am Acad Dermatol 45(3 Suppl):S116–S124. doi:10.1067/mjd.2001.117432

    Article  CAS  PubMed  Google Scholar 

  33. Fanelli MA, Vargas-Roig LM, Gago FE, Tello O, Lucero De Angelis R, Ciocca DR (1996) Estrogen receptors, progesterone receptors, and cell proliferation in human breast cancer. Breast Cancer Res Treat 37(3):217–228. doi:10.1007/BF01806503

    Article  CAS  PubMed  Google Scholar 

  34. Tan H, Zhong Y, Pan Z (2009) Autocrine regulation of cell proliferation by estrogen receptor-alpha in estrogen receptor-alpha-positive breast cancer cell lines. BMC Cancer 9:31. doi:10.1186/1471-2407-9-31

    Article  PubMed  PubMed Central  Google Scholar 

  35. Liao XH, Lu DL, Wang N, Liu LY, Wang Y, Li YQ, Yan TB, Sun XG, Hu P, Zhang TC (2014) Estrogen receptor alpha mediates proliferation of breast cancer MCF-7 cells via a p21/PCNA/E2F1-dependent pathway. FEBS J 281(3):927–942. doi:10.1111/febs.12658

    Article  CAS  PubMed  Google Scholar 

  36. Carrio R, Koru-Sengul T, Miao F, Gluck S, Lopez O, Selman Y, Alvarez C, Milikowski C, Gomez C, Jorda M, Nadji M, Torroella-Kouri M (2013) Macrophages as independent prognostic factors in small T1 breast cancers. Oncol Rep 29(1):141–148. doi:10.3892/or.2012.2088

    PubMed  Google Scholar 

  37. Pettersen JS, Fuentes-Duculan J, Suarez-Farinas M, Pierson KC, Pitts-Kiefer A, Fan L, Belkin DA, Wang CQ, Bhuvanendran S, Johnson-Huang LM, Bluth MJ, Krueger JG, Lowes MA, Carucci JA (2011) Tumor-associated macrophages in the cutaneous SCC microenvironment are heterogeneously activated. J Invest Dermatol 131(6):1322–1330. doi:10.103/jid.2011.9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Shabo I, Stal O, Olsson H, Dore S, Svanvik J (2008) Breast cancer expression of CD163, a macrophage scavenger receptor, is related to early distant recurrence and reduced patient survival. Int J Cancer J Int du Cancer 123(4):780–786. doi:10.1002/ijc.23527

    Article  CAS  Google Scholar 

  39. Lau SK, Chu PG, Weiss LM (2004) CD163: a specific marker of macrophages in paraffin-embedded tissue samples. Am J Clin Pathol 122(5):794–801. doi:10.1309/QHD6-YFN8-1KQX-UUH6

    Article  PubMed  Google Scholar 

  40. Lahmar Q, Keirsse J, Laoui D, Movahedi K, Van Overmeire E, Van Ginderachter JA (2016) Tissue-resident versus monocyte-derived macrophages in the tumor microenvironment. Biochim Biophys Acta 1865 1:23–34. doi:10.1016/j.bbcan.2015.06.009

    Google Scholar 

  41. Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182(3):311–322. doi:10.1002/(SICI)1097-4652(200003)182:3<311:AID-JCP1>3.0.CO;2-9

    Article  CAS  PubMed  Google Scholar 

  42. Zhang Y, Cheng S, Zhang M, Zhen L, Pang D, Zhang Q, Li Z (2013) High-infiltration of tumor-associated macrophages predicts unfavorable clinical outcome for node-negative breast cancer. PLoS One 8(9):e76147. doi:10.1371/journal.pone.0076147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Medrek C, Ponten F, Jirstrom K, Leandersson K (2012) The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients. BMC Cancer 12:306. doi:10.1186/1471-2407-12-306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Qian BZ, Zhang H, Li J, He T, Yeo EJ, Soong DY, Carragher NO, Munro A, Chang A, Bresnick AR, Lang RA, Pollard JW (2015) FLT1 signaling in metastasis-associated macrophages activates an inflammatory signature that promotes breast cancer metastasis. J Exp Med 212(9):1433–1448. doi:10.1084/jem.20141555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Pollard JW (2008) Macrophages define the invasive microenvironment in breast cancer. J Leukoc Biol 84(3):623–630. doi:10.1189/jlb.1107762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Mantovani A, Locati M (2013) Tumor-associated macrophages as a paradigm of macrophage plasticity, diversity, and polarization: lessons and open questions. Arterioscler Thromb Vasc Biol 33(7):1478–1483. doi:10.1161/ATVBAHA.113.300168

    Article  CAS  PubMed  Google Scholar 

  47. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, Becker CD, See P, Price J, Lucas D, Greter M, Mortha A, Boyer SW, Forsberg EC, Tanaka M, van Rooijen N, Garcia-Sastre A, Stanley ER, Ginhoux F, Frenette PS, Merad M (2013) Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38(4):792–804. doi:10.1016/j.immuni.2013.04.004

    Article  CAS  PubMed  Google Scholar 

  48. Gordon S, Pluddemann A, Martinez Estrada F (2014) Macrophage heterogeneity in tissues: phenotypic diversity and functions. Immunol Rev 262(1):36–55. doi:10.1111/imr.12223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Zheng C, Yang Q, Cao J, Xie N, Liu K, Shou P, Qian F, Wang Y, Shi Y (2016) Local proliferation initiates macrophage accumulation in adipose tissue during obesity. Cell Death Dis 7:e2167. doi:10.1038/cddis.2016.54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lindau A, Hardtner C, Hergeth SP, Blanz KD, Dufner B, Hoppe N, Anto-Michel N, Kornemann J, Zou J, Gerhardt LM, Heidt T, Willecke F, Geis S, Stachon P, Wolf D, Libby P, Swirski FK, Robbins CS, McPheat W, Hawley S, Braddock M, Gilsbach R, Hein L, von Zur Muhlen C, Bode C, Zirlik A, Hilgendorf I (2016) Atheroprotection through SYK inhibition fails in established disease when local macrophage proliferation dominates lesion progression. Basic Res Cardiol 111(2):20. doi:10.1007/s00395-016-0535-8

    Article  PubMed  PubMed Central  Google Scholar 

  51. Zhang W, He KF, Yang JG, Ren JG, Sun YF, Zhao JH, Zhao YF (2016) Infiltration of M2-polarized macrophages in infected lymphatic malformations: possible role in disease progression. Br J Dermatol. doi:10.1111/bjd.14471

    Google Scholar 

  52. Campbell MJ, Tonlaar NY, Garwood ER, Huo D, Moore DH, Khramtsov AI, Au A, Baehner F, Chen Y, Malaka DO, Lin A, Adeyanju OO, Li S, Gong C, McGrath M, Olopade OI, Esserman LJ (2011) Proliferating macrophages associated with high grade, hormone receptor negative breast cancer and poor clinical outcome. Breast Cancer Res Treat 128(3):703–711. doi:10.1007/s10549-010-1154-y

    Article  PubMed  Google Scholar 

  53. Campbell MJ, Wolf D, Mukhtar RA, Tandon V, Yau C, Au A, Baehner F, van’t Veer L, Berry D, Esserman LJ (2013) The prognostic implications of macrophages expressing proliferating cell nuclear antigen in breast cancer depend on immune context. PLoS One 8(10):e79114. doi:10.1371/journal.pone.0079114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Mukhtar RA, Moore AP, Tandon VJ, Nseyo O, Twomey P, Adisa CA, Eleweke N, Au A, Baehner FL, Moore DH, McGrath MS, Olopade OI, Gray JW, Campbell MJ, Esserman LJ (2012) Elevated levels of proliferating and recently migrated tumor-associated macrophages confer increased aggressiveness and worse outcomes in breast cancer. Ann Surg Oncol 19(12):3979–3986. doi:10.1245/s10434-012-2415-2

    Article  PubMed  Google Scholar 

  55. Pal T, Bonner D, Kim J, Monteiro AN, Kessler L, Royer R, Narod SA, Vadaparampil ST (2013) Early onset breast cancer in a registry-based sample of African-american women: BRCA mutation prevalence, and other personal and system-level clinical characteristics. Breast J 19(2):189–192. doi:10.1111/tbj.12083

    Article  CAS  PubMed  Google Scholar 

  56. Kong F, Gao F, Li H, Liu H, Zhang Y, Zheng R, Chen J, Li X, Liu G, Jia Y (2016) CD47: a potential immunotherapy target for eliminating cancer cells. Clin Transl Oncol Off Publ Fed Spanish Oncol Soc Natl Cancer Inst Mexico. doi:10.1007/s12094-016-1489-x

    Google Scholar 

Download references

Acknowledgments

We would like to extend our thanks to the University of Miami Sylvester Comprehensive Cancer Center’s Tissue Bank Core Facility and the Tumor Registry, and particularly to Drs. Consuelo Alvarez and Clara Milikowski without whom this investigation would not have been carried out. This study was funded by the Braman Family Breast Cancer Institute Development Grant from Sylvester Comprehensive Cancer Center at University of Miami Miller School of Medicine and also in part by the NCI/NIH R21CA176055 both to MTK. Research for this article was supported in part by funding to T.A.I from Breast Cancer Research Foundation and Play for P.I.N.K., NIEHS R01-ES024991, Women’s Cancer Association of UM and Sylvester Comprehensive Cancer Center; to L.G.S from a supplement to R21CA176055, to ZC from R21CA178675; to MLP from R01CA181115 and to M.P.C. from R01CA157012.

Author information

Author notes

  1. Stefan Glück

    Present address: Celgene Corporation, Summit, NJ, USA

Authors and Affiliations

  1. Department of Public Health Sciences, University of Miami Miller School of Medicine, Miami, FL, USA

    Tulay Koru-Sengul & Marta Torroella-Kouri

  2. Department of Microbiology and Immunology, University of Miami Miller School of Medicine, 1600 NW 10th Avenue Rosenstiel Medical School Building Suite 3123A, P.O. Box 016960 (R-138), Miami, FL, 33101, USA

    Ana M. Santander, Lidia G. Sanchez, Zhibin Chen & Marta Torroella-Kouri

  3. Department of Pathology, University of Miami Miller School of Medicine, Miami, FL, USA

    Merce Jorda, Tan A. Ince & Mehrad Nadji

  4. Department of Medicine, University of Miami Miller School of Medicine, Miami, FL, USA

    Stefan Glück

  5. Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL, USA

    Tulay Koru-Sengul, Feng Miao, Merce Jorda, Stefan Glück, Tan A. Ince, Mehrad Nadji, Zhibin Chen & Marta Torroella-Kouri

  6. Division of Surgical Oncology, Department of Surgery, UCLA, Los Angeles, CA, USA

    Manuel L Penichet

  7. Department of Microbiology, Immunology, and Molecular Genetics, David Geffen School of Medicine at UCLA, UCLA, Los Angeles, CA, USA

    Manuel L Penichet

  8. Jonsson Comprehensive Cancer Center, UCLA, Los Angeles, CA, USA

    Manuel L Penichet

  9. UCLA AIDS Institute, UCLA, Los Angeles, CA, USA

    Manuel L Penichet

  10. The Molecular Biology Institute, UCLA, Los Angeles, CA, USA

    Manuel L Penichet

  11. Hormel Institute, University of Minnesota, Austin, MN, 55912, USA

    Margot P. Cleary

Authors
  1. Tulay Koru-Sengul
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana M. Santander
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Feng Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lidia G. Sanchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Merce Jorda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stefan Glück
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tan A. Ince
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mehrad Nadji
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhibin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Manuel L Penichet
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Margot P. Cleary
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Marta Torroella-Kouri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marta Torroella-Kouri.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Tulay Koru-Sengul, Ana M. Santander share first authorship.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 384 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koru-Sengul, T., Santander, A.M., Miao, F. et al. Breast cancers from black women exhibit higher numbers of immunosuppressive macrophages with proliferative activity and of crown-like structures associated with lower survival compared to non-black Latinas and Caucasians. Breast Cancer Res Treat 158, 113–126 (2016). https://doi.org/10.1007/s10549-016-3847-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-016-3847-3

Keywords

Search

Navigation