Breast Cancer Research and Treatment

, Volume 158, Issue 1, pp 113–126 | Cite as

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

  • Tulay Koru-Sengul
  • Ana M. Santander
  • Feng Miao
  • Lidia G. Sanchez
  • Merce Jorda
  • Stefan Glück
  • Tan A. Ince
  • Mehrad Nadji
  • Zhibin Chen
  • Manuel L Penichet
  • Margot P. Cleary
  • Marta Torroella-KouriEmail author


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.


Breast cancer Race/ethnicities Macrophages Crown-like structures Inflammation 



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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10549_2016_3847_MOESM1_ESM.pdf (384 kb)
Supplementary material 1 (PDF 384 kb)


  1. 1.
    Cancer Facts and Figures 2014 (2014) American Cancer Society, AtlantaGoogle Scholar
  2. 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 CrossRefPubMedGoogle Scholar
  3. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 CrossRefPubMedGoogle Scholar
  5. 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 CrossRefPubMedGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefPubMedGoogle Scholar
  11. 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 CrossRefPubMedGoogle Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. 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 CrossRefPubMedGoogle Scholar
  14. 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 CrossRefPubMedGoogle Scholar
  15. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefPubMedGoogle Scholar
  18. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. 20.
    Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4(1):71–78. doi: 10.1038/nrc1256 CrossRefPubMedGoogle Scholar
  21. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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 CrossRefPubMedGoogle Scholar
  24. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 CrossRefPubMedGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 CrossRefPubMedGoogle Scholar
  36. 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 PubMedGoogle Scholar
  37. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefPubMedGoogle Scholar
  40. 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. 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 CrossRefPubMedGoogle Scholar
  42. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Pollard JW (2008) Macrophages define the invasive microenvironment in breast cancer. J Leukoc Biol 84(3):623–630. doi: 10.1189/jlb.1107762 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. 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 CrossRefPubMedGoogle Scholar
  48. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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. 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 CrossRefPubMedGoogle Scholar
  53. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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 CrossRefPubMedGoogle Scholar
  55. 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 CrossRefPubMedGoogle Scholar
  56. 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

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Tulay Koru-Sengul
    • 1
    • 5
  • Ana M. Santander
    • 2
  • Feng Miao
    • 5
  • Lidia G. Sanchez
    • 2
  • Merce Jorda
    • 3
    • 5
  • Stefan Glück
    • 4
    • 5
    • 12
  • Tan A. Ince
    • 3
    • 5
  • Mehrad Nadji
    • 3
    • 5
  • Zhibin Chen
    • 2
    • 5
  • Manuel L Penichet
    • 6
    • 7
    • 8
    • 9
    • 10
  • Margot P. Cleary
    • 11
  • Marta Torroella-Kouri
    • 2
    • 1
    • 5
    Email author
  1. 1.Department of Public Health SciencesUniversity of Miami Miller School of MedicineMiamiUSA
  2. 2.Department of Microbiology and ImmunologyUniversity of Miami Miller School of MedicineMiamiUSA
  3. 3.Department of PathologyUniversity of Miami Miller School of MedicineMiamiUSA
  4. 4.Department of MedicineUniversity of Miami Miller School of MedicineMiamiUSA
  5. 5.Sylvester Comprehensive Cancer CenterUniversity of Miami Miller School of MedicineMiamiUSA
  6. 6.Division of Surgical Oncology, Department of SurgeryUCLALos AngelesUSA
  7. 7.Department of Microbiology, Immunology, and Molecular GeneticsDavid Geffen School of Medicine at UCLA, UCLALos AngelesUSA
  8. 8.Jonsson Comprehensive Cancer Center, UCLALos AngelesUSA
  9. 9.UCLA AIDS Institute, UCLALos AngelesUSA
  10. 10.The Molecular Biology Institute, UCLALos AngelesUSA
  11. 11.Hormel Institute, University of MinnesotaAustinUSA
  12. 12.Celgene CorporationSummitUSA

Personalised recommendations