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The inhibitory effects of butein on cell proliferation and TNF-α-induced CCL2 release in racially different triple negative breast cancer cells


Autoři: Patricia Mendonca aff001;  Ainsley Horton aff001;  David Bauer aff001;  Samia Messeha aff001;  Karam F. A. Soliman aff001
Působiště autorů: College of Pharmacy and Pharmaceutical Sciences, Florida A&M University, Tallahassee, Florida, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0215269

Souhrn

Drug resistance is the leading cause of breast cancer-related mortality in women, and triple negative breast cancer (TNBC) is the most aggressive subtype, affecting African American women more aggressively compared to Caucasians women. Of all cancer-related deaths, 15 to 20% are associated with inflammation, where proinflammatory cytokines have been implicated in the tumorigenesis process. The current study investigated the effects of the polyphenolic compound butein (2′,3,4,4′-tetrahydroxychalcone) on cell proliferation and survival, as well as its modulatory effect on the release of proinflammatory cytokines in MDA-MB-231 (Caucasian) and MDA-MB-468 (African American) TNBC cell. The results obtained showed that butein decreased cell viability in a time and dose-dependent manner, and after 72-h of treatment, the cell proliferation rate was reduced in both cell lines. In addition, butein was found to have higher potency in MDA-MB-468, exhibiting anti-proliferative effects in lower concentrations. Apoptosis assays demonstrated that butein (50 μM) increased apoptotic cells in MDA MB-468, showing 60% of the analyzed cells in the apoptotic phase, compared to 20% in MDA-MB-231 cells. Additionally, butein downregulated both protein and mRNA expression of the proinflammatory cytokine, CCL2, and IKBKE in TNFα-activated Caucasian cells, but not in African Americans. This study demonstrates butein potential in cancer cell suppression showing a higher cytotoxic, anti-proliferative, and apoptotic effects in African Americans, compared to Caucasians TNBC cells. It also reveals the butein inhibitory effect on CCL2 expression with a possible association with IKBKE downregulation in MDA-MB-231 cells only, indicating that Caucasians and African Americans TNBC cells respond differently to butein treatment. The obtained findings may provide an explanation regarding the poor therapeutic response in African American patients with advanced TNBC.

Klíčová slova:

African American people – Apoptosis – Breast cancer – Cancer treatment – Cell proliferation – Cytokines – Enzyme-linked immunoassays – Protein expression


Zdroje

1. Kim JH, Jung CH, Jang BH, Go HY, Park JH, Choi YK, et al. (2009) Selective cytotoxic effects on human cancer cell lines of phenolic-rich ethyl-acetate fraction from Rhus verniciflua Stokes. Am J Chin Med 37: 609–620. doi: 10.1142/S0192415X09007090 19606519

2. Siegel RL, Miller KD, Jemal A (2018) Cancer statistics 2018 CA Cancer J Clin 68(1): pp. 7–30.

3. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, Gandhi J, et al. (2009) Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 4: e6146. doi: 10.1371/journal.pone.0006146 19582160

4. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, et al. (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 121: 2750–2767. doi: 10.1172/JCI45014 21633166

5. Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO. (2007) Prognostic markers in triple-negative breast cancer. Cancer 109: 25–32. doi: 10.1002/cncr.22381 17146782

6. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V (2007) Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer Registry. Cancer 109: 1721–1728. doi: 10.1002/cncr.22618 17387718

7. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, et al. (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. Jama 295: 2492–2502. doi: 10.1001/jama.295.21.2492 16757721

8. Dietze EC, Sistrunk C, Miranda-Carboni G, O’Regan R, Seewaldt VL (2015) Triple-negative breast cancer in African-American women: disparities versus biology. Nat Rev Cancer 15: 248–254. doi: 10.1038/nrc3896 25673085

9. DeSantis C, Siegel R, Jemal, A (2016) Breast Cancer Facts & Figures 2015–2016.

10. Mitra S (2017) MicroRNA Therapeutics in Triple Negative Breast Cancer. Arch Pathol Clin Res 1: 009–017.

11. Lakshmi P, Bhanu PK, Venkata SK, Josthna P (2015) Herbal and Medicinal Plants Molecules Towards Treatment of Cancer: A Mini Review. American Journal of Ethnomedicine Vol. 2, No. 2

12. Balunas MJ, Kinghorn AD (2005) Drug discovery from medicinal plants. Life Sci 78: 431–441. doi: 10.1016/j.lfs.2005.09.012 16198377

13. Cragg GM, Newman DJ (2005) Plants as a source of anti-cancer agents. J Ethnopharmacol 100: 72–79. doi: 10.1016/j.jep.2005.05.011 16009521

14. Desai AG, Qazi GN, Ganju RK, El-Tamer M, Singh J, Saxena AK, et al. (2008) Medicinal plants and cancer chemoprevention. Curr Drug Metab 9: 581–591. 18781909

15. Burns J, Yokota T, Ashihara H, Lean ME, Crozier A (2002) Plant foods and herbal sources of resveratrol. J Agric Food Chem 50: 3337–3340. doi: 10.1021/jf0112973 12010007

16. Mans DR, da Rocha AB, Schwartsmann G (2000) Anti-cancer drug discovery and development in Brazil: targeted plant collection as a rational strategy to acquire candidate anti-cancer compounds. Oncologist 5: 185–198. doi: 10.1634/theoncologist.5-3-185 10884497

17. Lee JC, Lee KY, Kim J, Na CS, Jung NC, Chung GH, et al. (2004) Extract from Rhus verniciflua Stokes is capable of inhibiting the growth of human lymphoma cells. Food Chem Toxicol 42: 1383–1388. doi: 10.1016/j.fct.2004.03.012 15234068

18. Semwal RB, Semwal DK, Combrinck S, Viljoen A (2015) Butein: From ancient traditional remedy to modern nutraceutical. Phytochemistry Letters 11: 188–201.

19. Jung CH, Jun CY, Lee S, Park CH, Cho K, Ko SG. (2006) Rhus verniciflua stokes extract: radical scavenging activities and protective effects on H2O2-induced cytotoxicity in macrophage RAW 264.7 cell lines. Biol Pharm Bull 29: 1603–1607. doi: 10.1248/bpb.29.1603 16880612

20. Jung CH, Kim JH, Hong MH, Seog HM, Oh SH, Lee PJ, et al. (2007) Phenolic-rich fraction from Rhus verniciflua Stokes (RVS) suppress inflammatory response via NF-kappaB and JNK pathway in lipopolysaccharide-induced RAW 264.7 macrophages. J Ethnopharmacol 110: 490–497. doi: 10.1016/j.jep.2006.10.013 17112694

21. Wang Y, Chan FL, Chen S, Leung LK (2005) The plant polyphenol butein inhibits testosterone-induced proliferation in breast cancer cells expressing aromatase. Life Sci 77: 39–51. doi: 10.1016/j.lfs.2004.12.014 15848217

22. Chua AW, Hay HS, Rajendran P, Shanmugam MK, Li F, Bist P, et al. (2010) Butein downregulates chemokine receptor CXCR4 expression and function through suppression of NF-kappaB activation in breast and pancreatic tumor cells. Biochem Pharmacol 80: 1553–1562. doi: 10.1016/j.bcp.2010.07.045 20699088

23. Yang LH, Ho YJ, Lin JF, Yeh CW, Kao SH, Hsu LS (2012) Butein inhibits the proliferation of breast cancer cells through generation of reactive oxygen species and modulation of ERK and p38 activities. Mol Med Rep 6: 1126–1132. doi: 10.3892/mmr.2012.1023 22895548

24. Orlikova B, Tasdemir D, Golais F, Dicato M, Diederich M (2011) Dietary chalcones with chemopreventive and chemotherapeutic potential. Genes Nutr 6: 125–147. doi: 10.1007/s12263-011-0210-5 21484163

25. Kuper H, Adami HO, Trichopoulos D (2000) Infections as a major preventable cause of human cancer. J Intern Med 248: 171–183. doi: 10.1046/j.1365-2796.2000.00742.x 10971784

26. Trimboli AJ, Cantemir-Stone CZ, Li F, Wallace JA, Merchant A, Creasap N, et al. (2009) Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 461: 1084–1091. doi: 10.1038/nature08486 19847259

27. Al-Rakan MA, Colak D, Hendrayani SF, Al-Bakheet A, Al-Mohanna FH, Kaya N, et al. (2013) Breast stromal fibroblasts from histologically normal surgical margins are pro-carcinogenic. J Pathol 231: 457–465. doi: 10.1002/path.4256 24009142

28. Yashiro M, Ikeda K, Tendo M, Ishikawa T, Hirakawa K (2005) Effect of organ-specific fibroblasts on proliferation and differentiation of breast cancer cells. Breast Cancer Res Treat 90: 307–313. doi: 10.1007/s10549-004-5364-z 15830145

29. Hembruff SL, Jokar I, Yang L, Cheng N (2010) Loss of transforming growth factor-beta signaling in mammary fibroblasts enhances CCL2 secretion to promote mammary tumor progression through macrophage-dependent and -independent mechanisms. Neoplasia 12: 425–433. doi: 10.1593/neo.10200 20454514

30. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A (2009) Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30: 1073–1081. doi: 10.1093/carcin/bgp127 19468060

31. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, et al. (2011) CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475: 222–225. doi: 10.1038/nature10138 21654748

32. Sica A, Porta C, Morlacchi S, Banfi S, Strauss L, Rimoldi M, et al. (2012) Origin and Functions of Tumor-Associated Myeloid Cells (TAMCs). Cancer Microenviron 5: 133–149. doi: 10.1007/s12307-011-0091-6 21948460

33. Grivennikov SI, Greten FR, Karin M (2010) Immunity, inflammation, and cancer. Cell 140: 883–899. doi: 10.1016/j.cell.2010.01.025 20303878

34. Balkwill F (2006) TNF-alpha in promotion and progression of cancer. Cancer Metastasis Rev 25.

35. Bertazza L, Mocellin S (2010) The dual role of tumor necrosis factor (TNF) in cancer biology. Curr Med Chem 17: 3337–3352. doi: 10.2174/092986710793176339 20712570

36. Ben-Baruch A (2006) The multifaceted roles of chemokines in malignancy. Cancer Metastasis Rev 25.

37. Apte RN, Krelin Y, Song X, Dotan S, Recih E, Elkabets M, et al. (2006) Effects of micro-environment- and malignant cell-derived interleukin-1 in carcinogenesis, tumour invasiveness and tumour-host interactions. Eur J Cancer 42.

38. Dinarello CA (2010) Why not treat human cancer with interleukin-1 blockade? Cancer Metastasis Rev 29: 317–329. doi: 10.1007/s10555-010-9229-0 20422276

39. Lewis AM, Varghese S, Xu H, Alexander HR (2006) Interleukin-1 and cancer progression: the emerging role of interleukin-1 receptor antagonist as a novel therapeutic agent in cancer treatment. J Transl Med 4.

40. Apte RN, Dotan S, Elkabets M, White MR, Reich E, Carmi Y, et al. (2006) The involvement of IL-1 in tumorigenesis, tumor invasiveness, metastasis and tumor-host interactions. Cancer Metastasis Rev 25: 387–408. doi: 10.1007/s10555-006-9004-4 17043764

41. Schmid MC, Avraamides CJ, Foubert P, Shaked Y, Kang SW, Kerbel RS, et al. (2011) Combined blockade of integrin-alpha4beta1 plus cytokines SDF-1alpha or IL-1beta potently inhibits tumor inflammation and growth. Cancer Res 71: 6965–6975. doi: 10.1158/0008-5472.CAN-11-0588 21948958

42. Zhou W, Guo S, Gonzalez-Perez RR (2003) Leptin pro-angiogenic signature in breast cancer is linked to IL-1 signalling. British journal of cancer 177: 128–137.

43. Palmieri C, Roberts-Clark D, Assadi-Sabet A, Coope RC, O’Hare M, Sunters A, et al. (2003) Fibroblast growth factor 7, secreted by breast fibroblasts, is an interleukin-1beta-induced paracrine growth factor for human breast cells. J Endocrinol 177.

44. Naldini A, Filippi I, Miglietta D, Moschetta M, Giavazzi R, Carraro F (2010) Interleukin-1beta regulates the migratory potential of MDAMB231 breast cancer cells through the hypoxia-inducible factor-1alpha. Eur J Cancer 46: 3400–3408. doi: 10.1016/j.ejca.2010.07.044 20801015

45. Argiles JM, Busquets S, Lopez-Soriano FJ (2011) Anti-inflammatory therapies in cancer cachexia. Eur J Pharmacol 668 Suppl 1: S81–86.

46. Balkwill FR, Mantovani A (2012) Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol 22: 33–40. doi: 10.1016/j.semcancer.2011.12.005 22210179

47. Balkwill F, Mantovani A (2010) Cancer and inflammation: implications for pharmacology and therapeutics. Clin Pharmacol Ther 87: 401–406. doi: 10.1038/clpt.2009.312 20200512

48. Liu D, Wang X, Chen Z (2016) Tumor Necrosis Factor-alpha, a Regulator and Therapeutic Agent on Breast Cancer. Curr Pharm Biotechnol 17: 486–494. doi: 10.2174/1389201017666160301102713 26927216

49. Katanov C, Lerrer S, Liubomirski Y, Leider-Trejo L, Meshel T, Bar J, et al. (2015) Regulation of the inflammatory profile of stromal cells in human breast cancer: prominent roles for TNF-alpha and the NF-kappaB pathway. Stem Cell Res Ther 6: 87. doi: 10.1186/s13287-015-0080-7 25928089

50. Trivanovic D, Jaukovic A, Krstic J, Nikolic S, Okic Djordjevic I, Kukolj T, et al. (2016) Inflammatory cytokines prime adipose tissue mesenchymal stem cells to enhance malignancy of MCF-7 breast cancer cells via transforming growth factor-beta1. IUBMB Life 68: 190–200. doi: 10.1002/iub.1473 26805406

51. Soria G, Ofri-Shahak M, Haas I, Yaal-Hahoshen N, Leider-Trejo L, Leibovich-Rivkin T, et al. (2011) Inflammatory mediators in breast cancer: Coordinated expression of TNFα & IL-1β with CCL2 & CCL5 and effects on epithelial-to-mesenchymal transition. BMC Cancer 11: 130. doi: 10.1186/1471-2407-11-130 21486440

52. Steiner JL, Murphy EA (2012) Importance of chemokine (CC-motif) ligand 2 in breast cancer. Int J Biol Markers 27: e179–185. doi: 10.5301/JBM.2012.9345 22865298

53. Vrakas CN, O’Sullivan RM, Evans SE, Ingram DA, Jones CB, Phuong T, et al. (2015) The Measure of DAMPs and a role for S100A8 in recruiting suppressor cells in breast cancer lung metastasis. Immunol Invest 44: 174–188. doi: 10.3109/08820139.2014.952818 25255046

54. Tabariès S, Ouellet V, Hsu BE, Annis MG, Rose AAN, Meunier L, et al. (2015) Granulocytic immune infiltrates are essential for the efficient formation of breast cancer liver metastases. Breast cancer research: BCR 17: 45–45. doi: 10.1186/s13058-015-0558-3 25882816

55. Ibrahim T, Mercatali L, Amadori D (2013) A new emergency in oncology: bone metastases in breast cancer patients (review). Oncol Lett 6.

56. Kindlund B, Sjoling A, Yakkala C, Adamsson J, Janzon A, Hansson LE, et al. (2017) CD4(+) regulatory T cells in gastric cancer mucosa are proliferating and express high levels of IL-10 but little TGF-beta. 20: 116–125.

57. Mishra P, Banerjee D, Ben-Baruch A (2011) Chemokines at the crossroads of tumor-fibroblast interactions that promote malignancy. J Leukoc Biol 89: 31–39. doi: 10.1189/jlb.0310182 20628066

58. Papi A, Storci G, Guarnieri T, De Carolis S, Bertoni S, Avenia N, et al. (2013) Peroxisome proliferator activated receptor-alpha/hypoxia inducible factor-1alpha interplay sustains carbonic anhydrase IX and apoliprotein E expression in breast cancer stem cells. PLoS One 8: e54968. doi: 10.1371/journal.pone.0054968 23372804

59. Ueno T, Toi M, Saji H, Muta M, Bando H, Kuroi K, et al. (2000) Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res 6: 3282–3289. 10955814

60. Chun E, Lavoie S, Michaud M, Gallini CA, Kim J, Soucy G, et al. (2015) CCL2 Promotes Colorectal Carcinogenesis by Enhancing Polymorphonuclear Myeloid-Derived Suppressor Cell Population and Function. Cell Rep 12: 244–257. doi: 10.1016/j.celrep.2015.06.024 26146082

61. McClellan JL, Davis JM, Steiner JL, Enos RT, Jung SH, Carson JA, et al. (2012) Linking tumor-associated macrophages, inflammation, and intestinal tumorigenesis: role of MCP-1. Am J Physiol Gastrointest Liver Physiol 303: G1087–1095. doi: 10.1152/ajpgi.00252.2012 23019193

62. Cho SG, Woo SM, Ko SG (2014) Butein suppresses breast cancer growth by reducing a production of intracellular reactive oxygen species. J Exp Clin Cancer Res 33: 51. doi: 10.1186/1756-9966-33-51 24919544

63. Barkett M, Gilmore TD (1999) Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18: 6910–6924. doi: 10.1038/sj.onc.1203238 10602466

64. Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221–227. doi: 10.1038/ni0302-221 11875461

65. Biswas DK, Martin KJ, McAlister C, Cruz AP, Graner E, Dai SC, et al. (2003) Apoptosis caused by chemotherapeutic inhibition of nuclear factor-kappaB activation. Cancer Res 63: 290–295. 12543776

66. Nakshatri H, Goulet RJ Jr. (2002) NF-kappaB and breast cancer. Curr Probl Cancer 26: 282–309. 12429950

67. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100: 57–70. doi: 10.1016/s0092-8674(00)81683-9 10647931

68. Dvorak HF (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315: 1650–1659. doi: 10.1056/NEJM198612253152606 3537791

69. Hussain SP, Hofseth LJ, Harris CC (2003) Radical causes of cancer. Nat Rev Cancer 3: 276–285. doi: 10.1038/nrc1046 12671666

70. Ernst CA, Zhang YJ, Hancock PR, Rutledge BJ, Corless CL, Rollins BJ (1994) Biochemical and biologic characterization of murine monocyte chemoattractant protein-1. Identification of two functional domains. J Immunol 152: 3541–3549. 8144933

71. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM (2001) Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193: 713–726. doi: 10.1084/jem.193.6.713 11257138

72. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ (2000) CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp Med 192: 899–905. doi: 10.1084/jem.192.6.899 10993920

73. Chavey C, Bibeau F, Gourgou-Bourgade S, Burlinchon S, Boissiere F, Laune D, et al. (2007) Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast Cancer Res 9: R15. doi: 10.1186/bcr1648 17261184

74. Fujimoto H, Sangai T, Ishii G, Ikehara A, Nagashima T, Miyazaki M, et al. (2009) Stromal MCP-1 in mammary tumors induces tumor-associated macrophage infiltration and contributes to tumor progression. Int J Cancer 125: 1276–1284. doi: 10.1002/ijc.24378 19479998

75. Lu X, Kang Y (2009) Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J Biol Chem 284: 29087–29096. doi: 10.1074/jbc.M109.035899 19720836

76. Yamashiro S, Takeya M, Nishi T, Kuratsu J, Yoshimura T, Yshio Y, et al. (1994) Tumor-derived monocyte chemoattractant protein-1 induces intratumoral infiltration of monocyte-derived macrophage subpopulation in transplanted rat tumors. Am J Pathol 145: 856–867. 7943176

77. Hoshino Y, Hatake K, Kasahara T, Takahashi Y, Ikeda M, Tomizuka H, et al. (1995) Monocyte chemoattractant protein-1 stimulates tumor necrosis and recruitment of macrophages into tumors in tumor-bearing nude mice: increased granulocyte and macrophage progenitors in murine bone marrow. Exp Hematol 23: 1035–1039. 7635182

78. Fang WB, Jokar I, Zou A, Lambert D, Dendukuri P, Cheng N (2012) CCL2/CCR2 chemokine signaling coordinates survival and motility of breast cancer cells through Smad3 protein- and p42/44 mitogen-activated protein kinase (MAPK)-dependent mechanisms. J Biol Chem 287: 36593–36608. doi: 10.1074/jbc.M112.365999 22927430

79. Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9: 239–252. doi: 10.1038/nrc2618 19279573

80. Kopfstein L, Christofori G (2006) Metastasis: cell-autonomous mechanisms versus contributions by the tumor microenvironment. Cell Mol Life Sci 63: 449–468. doi: 10.1007/s00018-005-5296-8 16416030

81. Boehm JS, Zhao JJ, Yao J, Kim SY, Firestein R, Dunn IF, et al. (2007) Integrative genomic approaches identify IKBKE as a breast cancer oncogene. Cell 129: 1065–1079. doi: 10.1016/j.cell.2007.03.052 17574021

82. Shen RR, Zhou AY, Kim E, Lim E, Habelhah H, Hahn WC. (2012) IkappaB kinase epsilon phosphorylates TRAF2 to promote mammary epithelial cell transformation. Mol Cell Biol 32: 4756–4768. doi: 10.1128/MCB.00468-12 23007157

83. Barbie TU, Alexe G, Aref AR, Li S, Zhu Z, Zhang X, et al. (2014) Targeting an IKBKE cytokine network impairs triple-negative breast cancer growth. J Clin Invest 124: 5411–5423. doi: 10.1172/JCI75661 25365225

84. Hutti JE, Shen RR, Abbott DW, Zhou AY, Sprott KM, Asara JM, et al. (2009) Phosphorylation of the tumor suppressor CYLD by the breast cancer oncogene IKKepsilon promotes cell transformation. Mol Cell 34: 461–472. doi: 10.1016/j.molcel.2009.04.031 19481526

85. Bauer D, Redmon N, Mazzio E, Soliman KF (2017) Apigenin inhibits TNFalpha/IL-1alpha-induced CCL2 release through IKBK-epsilon signaling in MDA-MB-231 human breast cancer cells. PLoS One 12: e0175558. doi: 10.1371/journal.pone.0175558 28441391

86. Messeha SS, Zarmouh NO, Mendonca P, Alwagdani H, Kolta MG, Soliman KFA (2018) The inhibitory effects of plumbagin on the NF-B pathway and CCL2 release in racially different triple-negative breast cancer cells. 13: e0201116.


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