Steroid hormones induce HMG1 overexpression and sensitize breast cancer cells to cisplatin and carboplatin

He, Qing; Liang, Cynthia H.; Lippard, Stephen J.

doi:10.1073/pnas.100108697

Cited by 192 publications

(162 citation statements)

References 49 publications

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“…Given the abundance of HMGB1 in nuclei, one copy per kb of the human genome, and its roles in various biological processes, it was hypothesized that the cellular HMGB1 level might modulate the cisplatin sensitivity of cancer cells. Consistent with this notion, hormone-induced HMGB1 up-regulation in MCF-7 breast cancer cells correlates with enhanced cisplatin sensitivity (27). Increased cisplatin sensitivity was also observed in a lung adenocarcinoma cell line transfected with a plasmid expressing HMGB2, a protein with more than 80% identity to HMGB1 (28).…”

supporting

confidence: 59%

“…There are, however, a number of scenarios that might prevent HMGB1 from interacting with cisplatin-modified DNA in the cells and modulating their responses to cisplatin. One possibility is that the HMGB1 level in the mouse embryonic fibroblasts is considerably lower than that of cells in other tissues or animals, such as MCF-7 human breast cancer cells, the subject of a previous study (27). A Western analysis for HMGB1 levels in both cell lines excluded this possibility.…”

Section: Resultsmentioning

confidence: 95%

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Cisplatin Sensitivity in Hmgb1−/− and Hmgb1+/+ Mouse Cells

Wei¹,

Burenkova

Lippard

2003

Journal of Biological Chemistry

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The study presented here investigates the effect of HMGB1 knockout on the sensitivity of mouse embryonic fibroblasts treated with the anticancer drug cisplatin. We evaluated both the growth inhibition by cisplatin and cisplatin-induced cell death in the Hmgb1 ؊/؊ cells and its wild-type counterpart. No significant differences were observed in the responses of these cells to cisplatin, indicating that HMGB1 does not play a significant role in modulating the cellular responses to cisplatin in this context. Since HMGB1 significantly enhances the cytotoxicity of cisplatin in other cells, these results illustrate the importance of cell type in determining the ability of this and probably other cisplatin-DNA-binding proteins to influence the efficacy of the drug.cis-Diamminedichloroplatinum(II) (cisplatin) 1 is one of the most widely used anticancer drugs for the treatment of a variety of human malignancies (1). Whereas cisplatin is extremely effective in treating testicular cancer, the cure rate being Ͼ90% when tumors are promptly diagnosed (2), the curative potential of the drug against other tumors, such as ovarian, breast, and lung cancers, is significantly undermined by intrinsic and acquired resistance (3). Determining the factors that influence cellular sensitivity to cisplatin is thus important for understanding the anticancer activity of cisplatin and for developing a more effective platinum-based chemotherapy.The cytotoxicity of cisplatin arises from its ability to react with DNA and form covalent DNA adducts (4). The major adducts, 1,2-intrastrand d(GpG) and d(ApG) platinum-DNA cross-links, are formed by coordination of the {Pt(NH 3 ) 2 } 2ϩ moiety to the N 7 atoms of adjacent purines in double-stranded DNA. The cisplatin modification produces distinct changes in the architecture of the DNA duplex that inhibit replication and transcription and stimulate nucleotide excision repair (1). Cisplatin damage throughout the genome leads to cell cycle arrest and apoptosis (5). Moreover, cisplatin-DNA adducts are recognized by a variety of cellular proteins, a process that may affect the fate of platinum-DNA lesions and the responsiveness of tumor cells to cisplatin treatment (6, 7). Recognition of cisplatin-modified DNA by damage recognition proteins in the nucleotide excision repair pathway leads to the removal of platinum lesions and restoration of genomic integrity. Studies have suggested that increase in the repair of platinum-DNA adducts is key to cisplatin resistance (3). Several proteins not involved in repair, including HMGB1, TATA-binding protein, and other structure-specific recognition proteins, also bind tightly to the major platinum-DNA adducts (1). The role that these proteins might play in mediating the cytotoxicity of cisplatin is a subject of much current interest. One hypothesis, which has been proposed in various studies, suggests that the binding of these proteins to platinum-DNA adducts blocks the removal of DNA lesions, thereby enhancing the sensitivity of cells to cisplatin (8 -14). This model...

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supporting

confidence: 59%

Section: Resultsmentioning

confidence: 95%

Cisplatin Sensitivity in Hmgb1−/− and Hmgb1+/+ Mouse Cells

Wei¹,

Burenkova

Lippard

2003

Journal of Biological Chemistry

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“…Cisplatin-modified DNA can divert TBP from its natural binding site, the TATA box, thus inhibiting transcription initiation (13). When binding to platinum-DNA adducts, HMGB1 can interfere with repair of the damaged DNA (11,19). HMGB1 contains two HMG box domains (HMGB1a and HMGB1b), 80-amino acid DNA-binding motifs that recognize bent DNA structures (20,21).…”

Section: Cis-ddp Cis-diamminedichloroplatinum(ii) (Cisplatin)mentioning

confidence: 99%

Effects of Spectator Ligands on the Specific Recognition of Intrastrand Platinum-DNA Cross-links by High Mobility Group Box and TATA-binding Proteins

Wei¹,

Cohen²,

Silverman

et al. 2001

Journal of Biological Chemistry

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“…He et al (42) reported an estrogen-induced increase in the transcription of HMGB1 in breast cancer cells. This observation suggested that endometrial HMGB1 expression, and possibly secretion, is steroid-dependent.…”

Section: Discussionmentioning

confidence: 99%

Association between follicular fluid levels of HMGB1 protein and outcomes in patients undergoing in vitro fertilization/intracytoplasmic sperm injection cycles

Yin

et al. 2015

Experimental and Therapeutic Medicine

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Abstract. The aim of the present study was to evaluate the association between follicular fluid (FF) levels of high-mobility group box 1 (HMGB1) protein and the reproductive outcome in patients undergoing in vitro fertilization (IVF) with intracytoplasmic sperm injection (ICSI). FF samples were collected from the ovarian follicles (≥14 mm) of 143 infertile patients that had undergone IVF/ICSI, and the HMGB1 expression levels were determined using ELISA. Spearman's correlation and receiver operating characteristic (ROC) curve analysis were applied to analyze the results. Significantly increased levels of HMGB1 protein (7.38±2.02 vs. 6.14±2.52 ng/ml; P<0.01), endometrial thickness on the day of human chorionic gonadotropin (hCG) administration (10.3±1.3 vs. 9.7±1.7 mm; P<0.01) and retrieved oocyte counts (11.68±6.51 vs. 11.00±6.34; P<0.01) were observed in the pregnant group when compared with the non-pregnant group. Conversely, the level of luteinizing hormone on the day of hCG administration was significantly reduced in the pregnant group compared with the non-pregnant group (0.92±1.78 vs. 1.78±2.03 pmol/l, P<0.01). The ROC curve indicated a significant association between the FF level of HMGB1 protein and the pregnancy rate, with an area under the ROC curve of 0.673 (0.581-0.765; P<0.01). In addition, the HMGB1 protein level was shown to have a significant positive correlation with the endometrial thickness (r=0.170; P<0.05). Therefore, the present study indicated that the FF levels of HMGB1 protein are increased in pregnant patients and are positively correlated with endometrial thickness. Thus, FF levels of HMGB1 may be a useful factor for predicting the outcome of IVF/ICSI treatments.

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Steroid hormones induce HMG1 overexpression and sensitize breast cancer cells to cisplatin and carboplatin

Cited by 192 publications

References 49 publications

Cisplatin Sensitivity in Hmgb1−/− and Hmgb1+/+ Mouse Cells

Cisplatin Sensitivity in Hmgb1−/− and Hmgb1+/+ Mouse Cells

Effects of Spectator Ligands on the Specific Recognition of Intrastrand Platinum-DNA Cross-links by High Mobility Group Box and TATA-binding Proteins

Association between follicular fluid levels of HMGB1 protein and outcomes in patients undergoing in vitro fertilization/intracytoplasmic sperm injection cycles

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