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In-depth LC-MS/MS analysis of the chicken ovarian cancer proteome reveals conserved and novel differentially regulated proteins in humans

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Abstract

Ovarian cancer (OVC) remains the most lethal gynecological malignancy in the world due to the combined lack of early-stage diagnostics and effective therapeutic strategies. The development and application of advanced proteomics technology and new experimental models has created unique opportunities for translational studies. In this study, we investigated the ovarian cancer proteome of the chicken, an emerging experimental model of OVC that develops ovarian tumors spontaneously. Matched plasma, ovary, and oviduct tissue biospecimens derived from healthy, early-stage OVC, and late-stage OVC birds were quantitatively characterized by label-free proteomics. Over 2600 proteins were identified in this study, 348 of which were differentially expressed by more than twofold (p ≤ 0.05) in early- and late-stage ovarian tumor tissue specimens relative to healthy ovarian tissues. Several of the 348 proteins are known to be differentially regulated in human cancers including B2M, CLDN3, EPCAM, PIGR, S100A6, S100A9, S100A11, and TPD52. Of particular interest was ovostatin 2 (OVOS2), a novel 165-kDa protease inhibitor found to be strongly upregulated in chicken ovarian tumors (p = 0.0005) and matched plasma (p = 0.003). Indeed, RT-quantitative PCR and Western blot analysis demonstrated that OVOS2 mRNA and protein were also upregulated in multiple human OVC cell lines compared to normal ovarian epithelia (NOE) cells and immunohistochemical staining confirmed overexpression of OVOS2 in primary human ovarian cancers relative to non-cancerous tissues. Collectively, these data provide the first evidence for involvement of OVOS2 in the pathogenesis of both chicken and human ovarian cancer.

Translational workflow for the LC-MS/MS identification of novel differentially expressed proteins such as ovostatin 2 (OVOS2) in the chicken followed by targeted analysis in humans

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Acknowledgments

This work was financially supported by NIH-NCI through award K25CA128666 and VCU (AMH) and R01GM087964 (D.C.M. and A.I.N for tissue proteomics). H.S and X.F were supported, in part, by NIH-NCI R21CA161478. Human ovarian cancer tissues were provided by the VCU Tissue and Data Acquisition and Analysis Core (TDAAC) Facility, supported, in part, with the funding from NIH-NCI Cancer Center Core Support Grant P30 CA016059, as well as through the Dept. of Pathology, School of Medicine, and Massey Cancer Center of Virginia Commonwealth University.

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Authors and Affiliations

  1. W.M. Keck FTMS Laboratory for Human Health Research, Department of Chemistry, North Carolina State University, 2620 Yarbrough Dr., Box 8204, Raleigh, NC, 27695, USA

    Angelito I. Nepomuceno & David C. Muddiman

  2. Prestage Department of Poultry Science, North Carolina State University, 2711 Founders Drive, Raleigh, NC, 27695, USA

    James N. Petitte

  3. Department of Biochemistry and Molecular Biology, Virginia Commonwealth University, 1101 E. Marshall Street, Richmond, VA, 23298, USA

    Huanjie Shao, Kai Jing, Yibao Ma & Xianjun Fang

  4. Department of Pathology, Virginia Commonwealth University, 1101 E. Marshall Street, Richmond, VA, 23298, USA

    Michael O. Idowu

  5. Department of Pharmaceutics, Virginia Commonwealth University, 410 North 12th Street Smith Building, Richmond, VA, 23298, USA

    Adam M. Hawkridge

  6. Department of Pharmacotherapy & Outcomes Science, Virginia Commonwealth University, 410 North 12th Street Smith Building, Richmond, VA, 23298, USA

    Adam M. Hawkridge

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  1. Angelito I. Nepomuceno
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Nepomuceno, A.I., Shao, H., Jing, K. et al. In-depth LC-MS/MS analysis of the chicken ovarian cancer proteome reveals conserved and novel differentially regulated proteins in humans. Anal Bioanal Chem 407, 6851–6863 (2015). https://doi.org/10.1007/s00216-015-8862-4

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