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Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles

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Abstract

Sulforaphane (SFN), an isothiocyanate found in cruciferous vegetables, is a potent inhibitor of experimental mammary carcinogenesis and may be an effective, safe chemopreventive agent for use in humans. SFN acts in part on the Keap1/Nrf2 pathway to regulate a battery of cytoprotective genes. In this study, transcriptomic and proteomic changes in the estrogen receptor negative, non-tumorigenic human breast epithelial MCF10A cell line were analyzed following SFN treatment or KEAP1 knockdown with siRNA using microarray and stable isotopic labeling with amino acids in culture (SILAC), respectively. Changes in selected transcripts and proteins were confirmed by PCR and Western blot in MCF10A and MCF12A cells. There was strong correlation between the transcriptomic and proteomic responses in both the SFN treatment (R = 0.679, P < 0.05) and KEAP1 knockdown (R = 0.853, P < 0.05) experiments. Common pathways for SFN treatment and KEAP1 knockdown were xenobiotic metabolism and antioxidants, glutathione metabolism, carbohydrate metabolism, and NADH/NADPH regeneration. Moreover, these pathways were most prominent in both the transcriptomic and the proteomic analyses. The aldo–keto reductase family members, AKR1B10, AKR1C1, AKR1C2 and AKR1C3, as well as NQO1 and ALDH3A1, were highly upregulated at both the transcriptomic and the proteomic levels. Collectively, these studies served to identify potential biomarkers that can be used in clinical trials to investigate the initial pharmacodynamic action of SFN in the breast.

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Abbreviations

SFN:

Sulforaphane

SILAC:

Stable isotopic labeling with amino acids in culture

ER:

Estrogen receptor

Nrf2:

Nuclear factor-E2-related factor 2

Keap1:

Kelch-like ECH-associated protein 1

ARE:

Antioxidant response element

siRNA:

Small interfering ribonucleic acid

AKR:

Aldo–keto reductase

HSD:

Hydroxysteroid dehydrogenase

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Acknowledgments

The authors would like to thank Harrys K. C. Jacob for his help with the microarray array data analysis and Santosh Renuse and Praveen Kumar for their help with the SILAC data analysis. This study was supported by the Johns Hopkins Breast Cancer Specialized Programs of Research Excellence P50 CA088843, CA94076, Department of Defense Breast Cancer Research Program Predoctoral Traineeship Award W81XWH-08-1-0176, Department of Defense Breast Cancer Research Program Era of Hope Award W81XWH-06-1-0428, Johns Hopkins Bloomberg School of Public Health Sommer Scholars Program and NIH Technology Centers for Networks and Pathways grant U54 RR020839.

Conflicts of interest

No potential conflicts of interest were disclosed.

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA

    Abena S. Agyeman, Patrick G. Shaw & Thomas W. Kensler

  2. Department of Environmental Health Science, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA

    Patrick G. Shaw & Thomas W. Kensler

  3. Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA

    Kala Visvanathan

  4. Departments of Biological Chemistry, Oncology and Pathology, McKusick-Nathans Institute for Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA

    Raghothama Chaerkady & Akhilesh Pandey

  5. Department of Environmental Health Science, Johns Hopkins Bloomberg School of Public Health, Room E7030, 615 N. Wolfe St., Baltimore, MD, 21205, USA

    Thomas W. Kensler

  6. Institute of Bioinformatics, International Technology Park, Bangalore, 560066, Karnataka, India

    Raghothama Chaerkady & Akhilesh Pandey

  7. Department of Pharmacology & Chemical Biology, University of Pittsburgh, Pittsburgh, PA, 15232, USA

    Nancy E. Davidson & Thomas W. Kensler

  8. University of Pittsburgh Cancer Institute, University of Pittsburgh, Pittsburgh, PA, 15232, USA

    Nancy E. Davidson & Thomas W. Kensler

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  1. Abena S. Agyeman
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Agyeman, A.S., Chaerkady, R., Shaw, P.G. et al. Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles. Breast Cancer Res Treat 132, 175–187 (2012). https://doi.org/10.1007/s10549-011-1536-9

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