Essential role of the cancer stem/progenitor cell marker nucleostemin for indole-3-carbinol anti-proliferative responsiveness in human breast cancer cells

BMC Biology

Volumn 12, Issue 1, 2014, Pages

  Tin, Antony S ^a   Park, Anna H ^a   Sundar, Shyam N ^a   Firestone, Gary L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anti proliferative response in breast cancer cell; Cancer stem progenitor cell marker; Elastase signaling; Indole 3 carbinol; Nucleostemin; Nucleostemin MDM2 interaction; Tumor xenograft; Tumorsphere

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; GNL3 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; INDOLE DERIVATIVE; INDOLE-3-CARBINOL; NUCLEAR PROTEIN;

ANIMAL; APOPTOSIS; BREAST NEOPLASMS; CANCER STEM CELL; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; METABOLISM; MOUSE; TUMOR CELL LINE;

ANIMALS; ANTICARCINOGENIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GTP-BINDING PROTEINS; HUMANS; INDOLES; MICE; NEOPLASTIC STEM CELLS; NUCLEAR PROTEINS; RECEPTOR, ERBB-2;

EID: 84908123753     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-014-0072-6     Document Type: Article

References (86)

1. Al-Hajj M. Cancer stem cells and oncology therapeutics. Curr Opin Oncol 2007, 19:61-64. 17133114.
2. Charafe-Jauffret E, Ginestier C, Birnbaum D. Breast cancer stem cells: tools and models to rely on. BMC Cancer 2009, 9:202. 10.1186/1471-2407-9-202, 19555472.
3. Lawson JC, Blatch GL, Edkins AL. Cancer stem cells in breast cancer and metastasis. Breast Cancer Res Treat 2009, 118:241-254. 10.1007/s10549-009-0524-9, 19731012.
4. Marsden CG, Wright MJ, Pochampally R, Rowan BG. Breast tumor-initiating cells isolated from patient core biopsies for study of hormone action. Methods Mol Biol 2009, 590:363-375. 10.1007/978-1-60327-378-7_23, 19763516.
5. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111. 10.1038/35102167, 11689955.
6. Stingl J, Caldas C. Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis. Nat Rev Cancer 2007, 7:791-799. 10.1038/nrc2212, 17851544.
7. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov 2009, 8:806-823. 10.1038/nrd2137, 19794444.
8. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006, 8:1777-1785. 10.1093/jnci/djj495.
9. O'Brien CS, Howell SJ, Farnie G, Clarke RB. Resistance to endocrine therapy: are breast cancer stem cells the culprits?. J Mammary Gland Biol Neoplasia 2009, 14:45-54. 10.1007/s10911-009-9115-y, 19252972.
10. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003, 17:1253-1270. 10.1101/gad.1061803, 12756227.
11. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005, 65:5506-5511. 10.1158/0008-5472.CAN-05-0626, 15994920.
12. Nakanishi T, Chumsri S, Khakpour N, Brodie AH, Leyland-Jones B, Hamburger AW, Ross DD, Burger AM. Side-population cells in luminal-type breast cancer have tumour-initiating cell properties, and are regulated by HER2 expression and signalling. Br J Canc 2010, 102:815-826. 10.1038/sj.bjc.6605553.
13. Korkaya H, Paulson A, Iovino F, Wicha MS. HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 2008, 27:6120-6130. 10.1038/onc.2008.207, 18591932.
14. Freudenberg JA, Wang Q, Katsumata M, Drebin J, Nagatomo I, Greene MI. The role of HER2 in early breast cancer metastasis and the origins of resistance to HER2-targeted therapies. Exp Mol Pathol 2009, 87:1-11. 10.1016/j.yexmp.2009.05.001, 19450579.
15. Zhang Y, Opresko L, Shankaran H, Chrisler WB, Wiley HS, Resat H. HER/ErbB receptor interactions and signaling patterns in human mammary epithelial cells. BMC Cell Biol 2009, 10:78. 10.1186/1471-2121-10-78, 19878579.
16. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987, 235:177-182. 10.1126/science.3798106, 3798106.
17. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang JC. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679. 10.1093/jnci/djn123, 18445819.
18. Heppner GH, Wolman SR. MCF-10AT: a model for human breast cancer development. Breast J 1999, 5:122-129. 10.1046/j.1524-4741.1999.00136.x, 11348271.
19. Miller FR. Xenograft models of premalignant breast disease. J Mammary Gland Biol Neoplasia 2001, 5:2000.
20. Worsham MJ, Pals G, Schouten JP, Miller F, Tiwari N, Spaendonk RV, Wolman SR. High-resolution mapping of molecular events associated with immortalization, transformation, and progression to breast cancer in the MCF10 model. Breast Cancer Res Treat 2006, 96:177-186. 10.1007/s10549-005-9077-8, 16319984.
21. Lin T, Meng L, Li Y, Tsai RY. Tumor-initiating function of nucleostemin-enriched mammary tumor cells. Cancer Res 2010, 70:9444-9452. 10.1158/0008-5472.CAN-10-2159, 21045149.
22. Woodward WA, Sulman EP. Cancer stem cells: markers or biomarkers?. Cancer Metastasis Rev 2008, 27:459-470. 10.1007/s10555-008-9130-2, 18437295.
23. Kai K, Arima Y, Kamiya T, Saya H. Breast cancer stem cells. Breast Cancer 2010, 17:80-85. 10.1007/s12282-009-0176-y, 19806428.
24. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567. 10.1016/j.stem.2007.08.014, 18371393.
25. Aggarwal BB, Ichikawa H. Molecular targets and anticancer potential of indole-3- carbinol and its derivatives. Cell Cycle 2005, 4:1201-1215. 10.4161/cc.4.9.1993, 16082211.
26. Weng JR, Tsai CH, Kulp SK, Chen CS. Indole-3-carbinol as a chemopreventive and anti-cancer agent. Cancer Letts 2008, 262:153-163. 10.1016/j.canlet.2008.01.033.
27. Ahmad A, Sakr WA, Rahman KM. Anticancer properties of indole compounds: mechanism of apoptosis induction and role in chemotherapy. Curr Drug Targets 2010, 11:652-666. 10.2174/138945010791170923, 20298156.
28. Safe S, Papineni S, Chintharlapalli S. Cancer chemotherapy with indole-3-carbinol, bis(3'-indolyl)methane and synthetic analogs. Cancer Letts 2008, 269:326-338. 10.1016/j.canlet.2008.04.021.
29. Sarkar FH, Li Y. Harnessing the fruits of nature for the development of multi- targeted cancer therapeutics. Cancer Treat Rev 2009, 35:597-607. 10.1016/j.ctrv.2009.07.001, 19660870.
30. Firestone GL, Sundar SN. Minireview: modulation of hormone receptor signaling by dietary anticancer indoles. Mol Endocrinol 2009, 23:1940-1947. 10.1210/me.2009-0149, 19837944.
31. Firestone GL, Bjeldanes LF. Indole-3-carbinol and 3-3'-diindolylmethane antiproliferative signaling pathways control cell-cycle gene transcription in human breast cancer cells by regulating promoter-Sp1 transcription factor interactions. J Nutr 2003, 133:2448S-2455S. 12840223.
32. Brew CT, Aronchik I, Hsu JC, Sheen JH, Dickson RB, Bjeldanes LF, Firestone GL. Indole-3-carbinol activates the ATM signaling pathway independent of DNA damage to stabilize p53 and induce G1 arrest of human mammary epithelial cells. Int J Cancer 2006, 118:857-868. 10.1002/ijc.21445, 16152627.
33. Nguyen HH, Aronchik I, Brar GA, Nguyen DH, Bjeldanes LF, Firestone GL. The dietary phytochemical indole-3-carbinol is a natural elastase enzymatic inhibitor that disrupts cyclin E protein processing. Proc Natl Acad Sci USA 2008, 105:19750-19755. 10.1073/pnas.0806581105, 19064917.
34. Aronchik I, Bjeldanes LF, Firestone GL. Direct inhibition of elastase activity by indole-3-carbinol triggers a CD40-TRAF regulatory cascade that disrupts NF-κB transcriptional activity in human breast cancer cells. Cancer Res 2010, 70:4961-4971. 10.1158/0008-5472.CAN-09-3349, 20530686.
35. Meng Q, Goldberg ID, Rosen EM, Fan S. Inhibitory effects of indole-3-carbinol on invasion and migration in human breast cancer cells. Breast Cancer Res Treat 2000, 63:147-152. 10.1023/A:1006495824158, 11097090.
36. Rahman KM, Aranha O, Glazyrin A, Chinni SR, Sarkar FH. Translocation of Bax to mitochondria induces apoptotic cell death in indole-3-carbinol (I3C) treated breast cancer cells. Oncogene 2000, 19:5764-5771. 10.1038/sj.onc.1203959, 11126363.
37. Moiseeva EP, Heukers R, Manson MM. EGFR and Src are involved in indole-3- carbinol-induced death and cell cycle arrest of human breast cancer cells. Carcinogenesis 2007, 28:435-445. 10.1093/carcin/bgl171, 16956907.
38. Marconett CN, Sundar SN, Poindexter KM, Stueve TR, Bjeldanes LF, Firestone GL. Indole-3-carbinol triggers aryl hydrocarbon receptor-dependent estrogen receptor (ER)α protein degradation in breast cancer cells disrupting an ERα-GATA3 transcriptional cross-regulatory loop. Mol Biol Cell 2010, 21:1166-1177. 10.1091/mbc.E09-08-0689, 20130088.
39. Marconett CN, Singhal AK, Sundar SN, Firestone GL. Indole-3-carbinol disrupts estrogen receptor-alpha dependent expression of insulin-like growth factor-1 receptor and insulin receptor substrate-1 and proliferation of human breast cancer cells. Mol Cell Endocrinol 2012, 363:74-84. 10.1016/j.mce.2012.07.008, 22835548.
40. Marconett CN, Sundar SN, Tseng M, Tin AS, Tran KQ, Mahuron KM, Bjeldanes LF, Firestone GL. Indole-3-carbinol downregulation of telomerase gene expression requires the inhibition of estrogen receptor-alpha and Sp1 transcription factor interactions within the hTERT promoter and mediates the G1 cell cycle arrest of human breast cancer cells. Carcinogenesis 2011, 32:1315-1323. 10.1093/carcin/bgr116, 21693539.
41. Brew CT, Aronchik I, Kosco K, McCammon J, Bjeldanes LF, Firestone GL. Indole-3- carbinol inhibits MDA-MB-231 breast cancer cell motility and induces stress fibers and focal adhesion formation by activation of Rho kinase activity. Int J Cancer 2009, 124:2294-2302. 10.1002/ijc.24210, 19173291.
42. McAlindon TE, Gulin J, Chen T, Klug T, Lahita R, Nuite M. Indole-3-carbinol in women with SLE: effect on estrogen metabolism and disease activity. Lupus 2001, 10:779-783. 10.1177/096120330101001104, 11789487.
43. Agrawal RC, Mehrotra N. Assessment of mutagenic potential of propoxur and its modulation by indole-3-carbinol. Food Chem Toxicol 1997, 35:1081-1084. 10.1016/S0278-6915(97)87275-4, 9463542.
44. Agrawal RC, Kumar S. Prevention of cyclophosphamide-induced micronucleus formation in mouse bone marrow by indole-3-carbinol. Food Chem Toxicol 1998, 36:975-977. 10.1016/S0278-6915(98)00032-5, 9771561.
45. Reed GA, Peterson KS, Smith HJ, Gray JC, Sullivan DK, Mayo MS, Crowell JA, Hurwitz A. A phase I study of indole-3-carbinol in women: tolerability and effects. Cancer Epidemiol Biomarkers Prev 2005, 14:1953-1960. 10.1158/1055-9965.EPI-05-0121, 16103443.
46. Staub RE, Feng C, Onisko B, Bailey GS, Firestone GL, Bjeldanes LF. Fate of indole-3- carbinol in cultured human breast tumor cells. Chem Res Toxicol 2002, 15:101-109. 10.1021/tx010056m, 11849035.
47. Nguyen HH, Lavrenov SN, Sundar SN, Nguyen DH, Tseng M, Marconett CN, Kung J, Staub RE, Preobrazhenskaya MN, Bjeldanes LF, Firestone GL. 1-benzyl-indole-3-carbinol is a novel indole-3-carbinol derivative with significantly enhanced potency of anti- proliferative and anti-estrogenic properties in human breast cancer cells. Chemico- biological interactions 2010, 186:255-266. 10.1016/j.cbi.2010.05.015, 20570586.
48. Aronchik I, Chen T, Durkin KA, Horwitz MS, Preobrazhenskaya MN, Bjeldanes LF, Firestone GL. Target protein interactions of indole-3-carbinol and the highly potent derivative 1-benzyl-I3C with the C-terminal domain of human elastase uncouples cell cycle arrest from apoptotic signaling. Mol Carcinog 2012, 51:881-894. 10.1002/mc.20857, 22012859.
49. Akizuki M, Fukutomi T, Takasugi M, Takahashi S, Sato T, Harao M, Mizumoto T, Yamashita J. Prognostic significance of immunoreactive neutrophil elastase in human breast cancer: long-term follow-up results in 313 patients. Neoplasia 2007, 9:260-264. 10.1593/neo.06808, 17401466.
50. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe JP, Tong F, Speed T, Spellman PT, DeVries S, Lapuk A, Wang NJ, Kuo WL, Stilwell JL, Pinkel D, Albertson DG, Waldman FM, McCormick F, Dickson RB, Johnson MD, Lippman M, Ethier S, Gazdar A, Gray JW. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006, 10:515-527. 10.1016/j.ccr.2006.10.008, 17157791.
51. Tin AS, Sundar SN, Tran KQ, Park AH, Poindexter KM, Firestone GL. Antiproliferative effects of artemisinin on human breast cancer cells requires the downregulated expression of the E2F1 transcription factor and loss of E2F1-target cell cycle genes. Anticancer Drugs 2012, 23:370-379. 10.1097/CAD.0b013e32834f6ea8, 22185819.
52. Peut VM, Rice AM. A Nod/SCID model of primary human breast cancer. Open Transplant J 2008, 2:1-8. 10.2174/1874418400802010001.
53. Ishiyama M, Tominaga H, Shiga M, Sasamoto K, Ohkura Y, Ueno K. A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Biol Pharm Bull 1996, 19:1518-1520. 10.1248/bpb.19.1518, 8951178.
54. Walsh JG, Cullen SP, Sheridan C, Luthi AU, Gerner C, Martin SJ. Executioner caspase-3 and caspase-7 are functionally distinct proteases. Proc Natl Acad Sci USA 2008, 105:12815-12819. 10.1073/pnas.0707715105, 18723680.
55. Zilfou JT, Lowe SW. Tumor suppressive functions of p53. Cold Spring Harb Perspect Biol 2009, 1:a001883. 10.1101/cshperspect.a001883, 20066118.
56. Moll UM, Petrenko O. The MDM2-p53 interaction. Mol Cancer Res 2003, 1:1001-1008. 14707283.
57. Lo D, Lu H. Nucleostemin: another nucleolar "twister" of the p53-MDM2 loop. Cell Cycle 2010, 9:3227-3232. 10.4161/cc.9.16.12605, 20703089.
58. Meng L, Lin T, Pen G, Hsu JK, Lee S, Lin SY, Tsai RYL. Nucleostemin deletion reveals an essential mechanism that maintains the enomic stability of stem and progenitor cells. Proc Natl Acad Sci USA 2013, 110:11415-11420. 10.1073/pnas.1301672110, 23798389.
59. Okamoto N, Yasukawa M, Nguyen C, Kasim V, Maida Y, Possemato R, Shibata T, Ligon KL, Fukami K, Hahn WC, Masutomi K. Maintenance of tumor initiating cells of defined genetic composition by nucleostemin. Proc Natl Acad Sci USA 2011, 108:20388-20393. 10.1073/pnas.1015171108, 21730156.
60. Dai MS, Sun XX, Lu H. Aberrant expression of nucleostemin activates p53 and induces cell cycle arrest via inhibition of MDM2. Mol Cell Biol 2008, 28:4365-4376. 10.1128/MCB.01662-07, 18426907.
61. Meng L, Hsu JK, Tsai RY. GNL3L depletion destabilizes MDM2 and induces p53- dependent G2/M arrest. Oncogene 2011, 30:1716-1726. 10.1038/onc.2010.550, 21132010.
62. Yang WL, Wang J, Chan CH, Lee SW, Campos AD, Lamothe B, Hur L, Grabiner BC, Lin X, Darnay BG, Lin HK. The E3 ligase TRAF6 regulates Akt ubiquitination and activation. Science 2009, 325:1134-1138. 10.1126/science.1175065, 19713527.
63. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988. 10.1073/pnas.0530291100, 12629218.
64. de Beca FF, Caetano P, Gerhard R, Alvarenga CA, Gomes M, Paredes J, Schmitt F. Cancer stem cells markers CD44, CD24 and ALDH1 in breast cancer special histological types. J Clin Pathol 2013, 66:187-191. 10.1136/jclinpath-2012-201169, 23112116.
65. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet R, Badve S, Nakshatri H. CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 2006, 8:R59. 10.1186/bcr1610, 17062128.
66. Lin Y, Zhong Y, Guan H, Zhang X, Sun Q. CD44+/CD24- phenotype contributes to malignant relapse following surgical resection and chemotherapy in patients with invasive ductal carcinoma. J Exp Clin Cancer Res 2012, 31:59. 10.1186/1756-9966-31-59, 22762532.
67. Economopoulou P, Kaklamani VG, Siziopikou K. The role of cancer stem cells in breast cancer initiation and progression: potential cancer stem cell-directed therapies. The Oncologist 2012, 17:1394-1401. 10.1634/theoncologist.2012-0163, 22941971.
68. Ucar D, Cogle CR, Zucali JR, Ostmark B, Scott EW, Zori R, Gray BA, Moreb JS. Aldehyde dehydrogenase activity as a functional marker for lung cancer. Chemico- Biological Interactions 2009, 178:48-55. 10.1016/j.cbi.2008.09.029, 18952074.
69. Douville J, Beaulieu R, Balicki D. ALDH1 as a functional marker of cancer stem and progenitor cells. Stem Cell Dev 2009, 18:17-25. 10.1089/scd.2008.0055.
70. Stingl J, Raouf A, Emerman JT, Eaves CJ. Epithelial progenitors in the normal human mammary gland. J Mammary Gland Biol Neoplasia 2005, 10:49-59. 10.1007/s10911-005-2540-7, 15886886.
71. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, Lander ES. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644. 10.1016/j.cell.2011.07.026, 21854987.
72. Hill RP. Identifying cancer stem cells in solid tumors: case not proven. Cancer Res 2006, 66:1891-1895. discussion 1890, 10.1158/0008-5472.CAN-05-3450, 16488984.
73. Korkaya H, Wicha MS. HER-2, notch, and breast cancer stem cells: targeting an axis of evil. Clin Cancer Res 2009, 15:1845-1847. 10.1158/1078-0432.CCR-08-3087, 19276254.
74. Liu JC, Deng T, Lehal RS, Kim J, Zacksenhaus E. Identification of tumorsphere- and tumor-initiating cells in HER2/Neu-induced mammary tumors. Cancer Res 2007, 67:8671-8681. 10.1158/0008-5472.CAN-07-1486, 17875707.
75. Kang L, Guo Y, Zhang X, Meng J, Wang ZY. A positive cross-regulation of HER2 and ER-α36 controls ALDH1 positive breast cancer cells. J Steroid Biochem Mol Biol 2011, 127:262-268. 10.1016/j.jsbmb.2011.08.011, 21907803.
76. Gasparini P, Bertolini G, Binda M, Magnifico A, Albano L, Tortoreto M, Pratesi G, Facchinetti F, Abolafio G, Roz L, Tagliabue E, Daidone MG, Sozzi G. Molecular cytogenetic characterization of stem-like cancer cells isolated from established cell lines. Canc Lett 2010, 296:206-215. 10.1016/j.canlet.2010.04.009.
77. Mayo LD, Donner DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA 2001, 98:11598-11603. 10.1073/pnas.181181198, 11504915.
78. Cheng X, Xia W, Yang JY, Hsu JL, Lang JY, Chou CK, Du Y, Sun HL, Wyszomierski SL, Mills GB, Muller WJ, Yu D, Hung MC. Activation of murine double minute 2 by Akt in mammary epithelium delays mammary involution and accelerates mammary tumorigenesis. Cancer Res 2010, 70:7684-7689. 10.1158/0008-5472.CAN-09-3231, 20841468.
79. Eliopoulos AG, Davies C, Knox PG, Gallagher NJ, Afford SC, Adams DH, Young LS. CD40 induces apoptosis in carcinoma cells through activation of cytotoxic ligands of the tumor necrosis factor superfamily. Mol Cell Biol 2000, 20:5503-5515. 10.1128/MCB.20.15.5503-5515.2000, 10891490.
80. Benson RJ, Hostager BS, Bishop GA. Rapid CD40-mediated rescue from CD95- induced apoptosis requires TNFR-associated factor-6 and PI3K. Eur J Immunol 2006, 36:2535-2543. 10.1002/eji.200535483, 16897814.
81. Nawa M, Osada S, Morimitsu K, Nonaka K, Futamura M, Kawaguchi Y, Yoshida K. Growth effect of neutrophil elastase on breast cancer: favorable action of sivelestat and application to anti-HER2 therapy. Anticancer Res 2012, 32:13-19. 22213283.
82. Mittendorf EA, Alatrash G, Qiao N, Wu Y, Sukhumalchandra P, St John LS, Philips AV, Xiao H, Zhang M, Ruisaard K, Clise-Dwyer K, Lu S, Molldrem JJ. Breast cancer cell uptake of the inflammatory mediator neutrophil elastase triggers an anticancer adaptive immune response. Cancer Res 2012, 72:3153-3162. 10.1158/0008-5472.CAN-11-4135, 22564522.
83. ATCC website. http://www.atcc.org/en/STR_Database.aspx
84. Romano P, Manniello A, Aresu O, Armento M, Cesaro M, Parodi B. Cell Line Data Base: structure and recent improvements towards molecular authentication of human cell lines. Nucleic Acids Res 2009, 37:D925-D932. 10.1093/nar/gkn730, 18927105.
85. Failor KL, Desyatnikov Y, Finger LA, Firestone GL. Glucocorticoid-induced degradation of glycogen synthase kinase-3 protein is triggered by serum- and glucocorticoid-induced protein kinase and Akt signaling and controls beta-catenin dynamics and tight junction formation in mammary epithelial tumor cells. Mol Endocrinol 2007, 21:2403-2415. 10.1210/me.2007-0143, 17595317.
86. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989, 24:148-154. 10.1007/BF00300234, 2544306.