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Identification of TGFβ-induced proteins in non-endocrine mouse pituitary cell line TtT/GF by SILAC-assisted quantitative mass spectrometry

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Abstract

TtT/GF is a mouse cell line derived from a thyrotropic pituitary tumor and has been used as a model of folliculostellate cells. Our previous microarray data indicate that TtT/GF possesses some properties of endothelial cells, pericytes and stem/progenitor cells, along with folliculostellate cells, suggesting its plasticity. We also found that transforming growth factor beta (TGFβ) alters cell motility, increases pericyte marker transcripts and attenuates endothelial cell and stem/progenitor cell markers in TtT/GF cells. The present study explores the wide-range effect of TGFβ on TtT/GF cells at the protein level and characterizes TGFβ-induced proteins and their partnerships using stable isotope labeling of amino acids in cell culture (SILAC)-assisted quantitative mass spectrometry. Comparison between quantified proteins from TGFβ-treated cells and those from SB431542 (a selective TGFβ receptor I inhibitor)-treated cells revealed 51 upregulated and 112 downregulated proteins (|log2| > 0.6). Gene ontology and STRING analyses revealed that these are related to the actin cytoskeleton, cell adhesion, extracellular matrix and DNA replication. Consistently, TGFβ-treated cells showed a distinct actin filament pattern and reduced proliferation compared to vehicle-treated cells; SB431542 blocked the effect of TGFβ. Upregulation of many pericyte markers (CSPG4, NES, ACTA, TAGLN, COL1A1, THBS1, TIMP3 and FLNA) supports our previous hypothesis that TGFβ reinforces pericyte properties. We also found downregulation of CTSB, EZR and LGALS3, which are induced in several pituitary adenomas. These data provide valuable information about pericyte differentiation as well as the pathological processes in pituitary adenomas.

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Acknowledgments

We would like to thank Tom Kouki (Jichi Medical University) for his support in transmission electron microscopy and Editage (www.editage.jp) for English language editing.

Funding

This work was partially supported by the Japan Society for the Promotion of Science KAKENHI Grants (Numbers 16K18818 to SY, 26460281 to KF, 16K08475 to KH, 26292166 to YK and 15K07771 to TK), the MEXT-supported Program for the Strategic Research Foundation at Private Universities (2014–2018), the Meiji University International Institute for BioResource Research (MUIIR) and start-up funds to TT from the Faculty of Science Department at Toho University.

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  1. Takehiro Tsukada, Yukinobu Isowa and Keiji Kito contributed equally to this work.

Authors and Affiliations

  1. Department of Biomolecular Science, Faculty of Science, Toho University, 2-2-1 Miyama, Funabashi, Chiba, 274-8510, Japan

    Takehiro Tsukada & Seina Toneri

  2. Organization for the Strategic Coordination of Research and Intellectual Properties, Meiji University, Kawasaki, Kanagawa, Japan

    Yukinobu Isowa, Saishu Yoshida & Takako Kato

  3. Institute for Endocrinology, Meiji University, Kawasaki, Kanagawa, Japan

    Keiji Kito, Saishu Yoshida, Takako Kato & Yukio Kato

  4. Department of Life Sciences, School of Agriculture, Meiji University, Kawasaki, Kanagawa, Japan

    Keiji Kito & Yukio Kato

  5. Laboratory of Anatomy and Cell Biology, Department of Health Sciences, Kyorin University, Mitaka, Tokyo, Japan

    Kotaro Horiguchi

  6. Division of Histology and Cell Biology, Department of Anatomy, Jichi Medical University School of Medicine, Shimotsuke, Tochigi, Japan

    Ken Fujiwara & Takashi Yashiro

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  1. Takehiro Tsukada
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  2. Yukinobu Isowa
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Electronic Supplementary Material Fig. 1

Heavy medium containing 13C6-labeled lysine and arginine have no effect on TGFβ-induced Smad2 nuclear translocation. After a 3-day culture in light (top) or heavy medium (bottom), TtT/GF cells were treated with vehicle, TGFβ (10 ng/mL), or TGFβ (10 ng/mL) and selective TGFβ receptor inhibitor (SB431542, 10 μM) for 30 min. Treated cells were stained for Smad2 (green) and DAPI (blue) (for staining protocol see Tsukada et al. 2018). Diffuse cytoplasmic staining for Smad2 was observed with vehicle treatment (a, a′); however, intense nuclear staining was observed with 10 ng/mL TGFβ (b, b′). The TGFβ-induced Smad2 nuclear translocation was completely blocked by 10 μM SB431542 (c, c′). No significant difference was observed between light and heavy medium in terms of the efficiency of TGFβ and TGFβ receptor inhibitor. Bar = 100 μm (DOCX 209 kb)

Electronic Supplementary Material Fig. 2

TGFβ attenuates transcript levels of stem cell marker genes and promotes pericyte markers. Total RNA was extracted after a 3-day treatment with TGFβ/SB431542 in light medium using the RNeasy Mini Kit and RNase-free DNase Set according to the manufacturer’s instructions (Qiagen, Hilden, Germany). cDNA was synthesized using the PrimeScript RT Reagent Kit (Takara Bio, Otsu, Japan) with oligo-(dT)20 primer (Life Technologies). Quantitative PCR (AriaMx, Agilent Technologies) was performed using SYBR Green Real-time PCR Master Mix Plus (Toyobo, Osaka, Japan) and specific primer sets at 0.6 μM for each target gene (Electronic Supplementary Material, Table S6). Each sample was measured in duplicate and results are based on five independent experiments; data were analyzed by the comparative CT method (ddCt method) to estimate gene copy number relative to that of the TATA box-binding protein (Tbp), used as an internal standard. Genes included stem cell markers (Sca-1, Cd34), pericyte markers (Nes, Cspg4, Col1a1) and a folliculostellate cell marker (S100b). TGFβ increased pericyte marker gene expression and decreased stem cell marker gene expression. *p < 0.05 (Tukey’s test) (DOCX 188 kb)

Electronic Supplementary Material Table S1

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Electronic Supplementary Material Table S2

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Electronic Supplementary Material Table S3

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Electronic Supplementary Material Table S5

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Electronic Supplementary Material Table S6

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Tsukada, T., Isowa, Y., Kito, K. et al. Identification of TGFβ-induced proteins in non-endocrine mouse pituitary cell line TtT/GF by SILAC-assisted quantitative mass spectrometry. Cell Tissue Res 376, 281–293 (2019). https://doi.org/10.1007/s00441-018-02989-2

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