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Tumor Biology

, Volume 37, Issue 9, pp 12503–12512 | Cite as

Yeast two-hybrid screening identified WDR77 as a novel interacting partner of TSC22D2

  • Qiao Li
  • Pan Chen
  • Zhaoyang Zeng
  • Fang Liang
  • Yali Song
  • Fang Xiong
  • Xiayu Li
  • Zhaojian Gong
  • Ming Zhou
  • Bo Xiang
  • Cong Peng
  • Xiaoling Li
  • Xiang Chen
  • Guiyuan Li
  • Wei Xiong
Original Article

Abstract

Transforming growth factor β-stimulated clone 22 domain family, member 2 (TSC22D2), a member of the TSC22D family, has been implicated as a tumor-associated gene, but its function remains unknown. To further explore its biological role, yeast two-hybrid screening combined with multiple bioinformatics tools was used to identify 44 potential interacting partners of the TSC22D2 protein that were mainly involved in gene transcription, cellular metabolism, and cell cycle regulation. The protein WD repeat domain 77 (WDR77) was selected for further validation due to its function in the cell cycle and tumor development, as well as its high detection frequency in the yeast two-hybrid assay. Immunoprecipitation and immunofluorescence experiments confirmed an interaction between the TSC22D2 and WDR77 proteins. Our work greatly expands the putative protein interaction network of TSC22D2 and provides deeper insight into the biological functions of the TSC22D2 and WDR77 proteins.

Keywords

TSC22D2 Yeast two-hybrid assay Interaction network WDR77 

Notes

Acknowledgments

This study was supported in part by grants from The National Natural Science Foundation of China (81272298, 81372907, 81472531, and 81572787) and the Natural Science Foundation of Hunan Province (14JJ1010 and 2015JJ1022).

Compliance with ethical standards

Conflicts of interest

None

References

  1. 1.
    Liang F, Zeng Z, Li Q, Li X, Li Z, Gong Z, et al. TSC22D2 interacts with PKM2 and inhibits cell growth in colorectal cancer. Int J Oncol. 2016 (in press).Google Scholar
  2. 2.
    Shibanuma M, Kuroki T, Nose K. Isolation of a gene encoding a putative leucine zipper structure that is induced by transforming growth factor beta 1 and other growth factors. J Biol Chem. 1992;267:10219–24.PubMedGoogle Scholar
  3. 3.
    Kester HA, Blanchetot C, den Hertog J, van der Saag PT, van der Burg B. Transforming growth factor-beta-stimulated clone-22 is a member of a family of leucine zipper proteins that can homo- and heterodimerize and has transcriptional repressor activity. J Biol Chem. 1999;274:27439–47.CrossRefPubMedGoogle Scholar
  4. 4.
    Fiol DF, Mak SK, Kultz D. Specific TSC22 domain transcripts are hypertonically induced and alternatively spliced to protect mouse kidney cells during osmotic stress. Febs J. 2007;274:109–24.CrossRefPubMedGoogle Scholar
  5. 5.
    Ohta S, Yanagihara K, Nagata K. Mechanism of apoptotic cell death of human gastric carcinoma cells mediated by transforming growth factor beta. Biochem J. 1997;324(Pt 3):777–82.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    D'Adamio F, Zollo O, Moraca R, Ayroldi E, Bruscoli S, Bartoli A, et al. A new dexamethasone-induced gene of the leucine zipper family protects T lymphocytes from TCR/CD3-activated cell death. Immunity. 1997;7:803–12.CrossRefPubMedGoogle Scholar
  7. 7.
    Dohrmann CE, Belaoussoff M, Raftery LA. Dynamic expression of TSC-22 at sites of epithelial-mesenchymal interactions during mouse development. Mech Dev. 1999;84:147–51.CrossRefPubMedGoogle Scholar
  8. 8.
    Gluderer S, Brunner E, Germann M, Jovaisaite V, Li C, Rentsch CA, et al. Madm (Mlf1 adapter molecule) cooperates with Bunched A to promote growth in Drosophila. J Biol. 2010;9:9.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Canterini S, Bosco A, Carletti V, Fuso A, Curci A, Mangia F, et al. Subcellular TSC22D4 localization in cerebellum granule neurons of the mouse depends on development and differentiation. Cerebellum. 2012;11:28–40.CrossRefPubMedGoogle Scholar
  10. 10.
    Beaulieu E, Morand EF. Role of GILZ in immune regulation, glucocorticoid actions and rheumatoid arthritis. Nat Rev Rheumatol. 2011;7:340–8.CrossRefPubMedGoogle Scholar
  11. 11.
    Riccardi C. GILZ (glucocorticoid-induced leucine zipper), a mediator of the anti-inflammatory and immunosuppressive activity of glucocorticoids. Ann Ig. 2010;22:53–9.PubMedGoogle Scholar
  12. 12.
    Riccardi C, Zollo O, Nocentini G, Bruscoli S, Bartoli A, D'Adamio F, et al. Glucocorticoid hormones in the regulation of cell death. Therapie. 2000;55:165–9.PubMedGoogle Scholar
  13. 13.
    Kawamata H, Nakashiro K, Uchida D, Hino S, Omotehara F, Yoshida H, et al. Induction of TSC-22 by treatment with a new anti-cancer drug, vesnarinone, in a human salivary gland cancer cell. Br J Cancer. 1998;77:71–8.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Shostak KO, Dmitrenko VV, Vudmaska MI, Naidenov VG, Beletskii AV, Malisheva TA, et al. Patterns of expression of TSC-22 protein in astrocytic gliomas. Exp Oncol. 2005;27:314–8.PubMedGoogle Scholar
  15. 15.
    Iida M, Anna CH, Gaskin ND, Walker NJ, Devereux TR. The putative tumor suppressor Tsc-22 is downregulated early in chemically induced hepatocarcinogenesis and may be a suppressor of Gadd45b. Toxicol Sci. 2007;99:43–50.CrossRefPubMedGoogle Scholar
  16. 16.
    Yu J, Ershler M, Yu L, Wei M, Hackanson B, Yokohama A, et al. TSC-22 contributes to hematopoietic precursor cell proliferation and repopulation and is epigenetically silenced in large granular lymphocyte leukemia. Blood. 2009;113:5558–67.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Yoon CH, Rho SB, Kim ST, Kho S, Park J, Jang IS, et al. Crucial role of TSC-22 in preventing the proteasomal degradation of p53 in cervical cancer. Plos One. 2012;7:e42006.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Nakamura M, Kitaura J, Enomoto Y, Lu Y, Nishimura K, Isobe M, et al. Transforming growth factor-beta-stimulated clone-22 is a negative-feedback regulator of Ras/Raf signaling: implications for tumorigenesis. Cancer Sci. 2012;103:26–33.CrossRefPubMedGoogle Scholar
  19. 19.
    Ayroldi E, Zollo O, Bastianelli A, Marchetti C, Agostini M, Di Virgilio R, et al. GILZ mediates the antiproliferative activity of glucocorticoids by negative regulation of Ras signaling. J Clin Invest. 2007;117:1605–15.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ayroldi E, Petrillo MG, Bastianelli A, Marchetti MC, Ronchetti S, Nocentini G, et al. L-GILZ binds p53 and MDM2 and suppresses tumor growth through p53 activation in human cancer cells. Cell Death Differ. 2015;22:118–30.CrossRefPubMedGoogle Scholar
  21. 21.
    Zhou L, Wu H, Lee P, Wang Z. Roles of the androgen receptor cofactor p44 in the growth of prostate epithelial cells. J Mol Endocrinol. 2006;37:283–300.CrossRefPubMedGoogle Scholar
  22. 22.
    Gao S, Wang Z. Subcellular localization of p44/WDR77 determines proliferation and differentiation of prostate epithelial cells. Plos One. 2012;7:e49173.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Peng Y, Chen F, Melamed J, Chiriboga L, Wei J, Kong X, et al. Distinct nuclear and cytoplasmic functions of androgen receptor cofactor p44 and association with androgen-independent prostate cancer. Proc Natl Acad Sci U S A. 2008;105:5236–41.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Liang JJ, Wang Z, Chiriboga L, Greco MA, Shapiro E, Huang H, et al. The expression and function of androgen receptor coactivator p44 and protein arginine methyltransferase 5 in the developing testis and testicular tumors. J Urol. 2007;177:1918–22.CrossRefPubMedGoogle Scholar
  25. 25.
    Ligr M, Patwa RR, Daniels G, Pan L, Wu X, Li Y, et al. Expression and function of androgen receptor coactivator p44/Mep50/WDR77 in ovarian cancer. Plos One. 2011;6:e26250.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Peng Y, Li Y, Gellert LL, Zou X, Wang J, Singh B, et al. Androgen receptor coactivator p44/Mep50 in breast cancer growth and invasion. J Cell Mol Med. 2010;14:2780–9.CrossRefPubMedGoogle Scholar
  27. 27.
    Gu Z, Zhang F, Wang ZQ, Ma W, Davis RE, Wang Z. The p44/wdr77-dependent cellular proliferation process during lung development is re-activated in lung cancer. Oncogene. 2013;32:1888–900.CrossRefPubMedGoogle Scholar
  28. 28.
    Spyrou I, Sifakis S, Ploumidis A, Papalampros AE, Felekouras E, Tsatsakis AM, et al. Expression profile of CYP1A1 and CYP1B1 enzymes in endometrial tumors. Tumor Biol. 2014;35:9549–56.CrossRefGoogle Scholar
  29. 29.
    Zeng Z, Bo H, Gong Z, Lian Y, Li X, Li X, et al. AFAP1-AS1, a long noncoding RNA upregulated in lung cancer and promotes invasion and metastasis. Tumor Biol. 2015.Google Scholar
  30. 30.
    Liu XF, Bera TK, Kahue C, Escobar T, Fei Z, Raciti GA, et al. ANKRD26 and its interacting partners TRIO, GPS2, HMMR and DIPA regulate adipogenesis in 3T3-L1 cells. Plos One. 2012;7:e38130.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Chai Y, Liu X, Dai L, Li Y, Liu M, Zhang JY. Overexpression of HCC1/CAPERalpha may play a role in lung cancer carcinogenesis. Tumor Biol. 2014;35:6311–7.CrossRefGoogle Scholar
  32. 32.
    Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res. 2008;36:W5–9.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Chatr-Aryamontri A, Breitkreutz BJ, Oughtred R, Boucher L, Heinicke S, Chen D, et al. The BioGRID interaction database: 2015 update. Nucleic Acids Res. 2015;43:D470–8.CrossRefPubMedGoogle Scholar
  35. 35.
    Licata L, Briganti L, Peluso D, Perfetto L, Iannuccelli M, Galeota E, et al. MINT, the molecular interaction database: 2012 update. Nucleic Acids Res. 2012;40:D857–61.CrossRefPubMedGoogle Scholar
  36. 36.
    Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43:D447–52.CrossRefPubMedGoogle Scholar
  37. 37.
    Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, et al. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 2015;43:D213–21.CrossRefPubMedGoogle Scholar
  38. 38.
    Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44–57.CrossRefGoogle Scholar
  39. 39.
    Safran M, Dalah I, Alexander J, Rosen N, Iny ST, Shmoish M, et al. GeneCards Version 3: the human gene integrator. Database (Oxford). 2010;2010:q20.CrossRefGoogle Scholar
  40. 40.
    Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci U S A. 2001;98:4569–74.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Formstecher E, Aresta S, Collura V, Hamburger A, Meil A, Trehin A, et al. Protein interaction mapping: a Drosophila case study. Genome Res. 2005;15:376–84.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Riccardi C, Bruscoli S, Ayroldi E, Agostini M, Migliorati G. GILZ, a glucocorticoid hormone induced gene, modulates T lymphocytes activation and death through interaction with NF-kB. Adv Exp Med Biol. 2001;495:31–9.CrossRefPubMedGoogle Scholar
  43. 43.
    Ayroldi E, Zollo O, Macchiarulo A, Di Marco B, Marchetti C, Riccardi C. Glucocorticoid-induced leucine zipper inhibits the Raf-extracellular signal-regulated kinase pathway by binding to Raf-1. Mol Cell Biol. 2002;22:7929–41.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Vago JP, Tavares LP, Garcia CC, Lima KM, Perucci LO, Vieira EL, et al. The role and effects of glucocorticoid-induced leucine zipper in the context of inflammation resolution. J Immunol. 2015;194:4940–50.CrossRefPubMedGoogle Scholar
  45. 45.
    Wilson CH, Crombie C, van der Weyden L, Poulogiannis G, Rust AG, Pardo M, et al. Nuclear receptor binding protein 1 regulates intestinal progenitor cell homeostasis and tumour formation. Embo J. 2012;31:2486–97.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Ruiz C, Oeggerli M, Germann M, Gluderer S, Stocker H, Andreozzi M, et al. High NRBP1 expression in prostate cancer is linked with poor clinical outcomes and increased cancer cell growth. Prostate. 2012;72:1678–87.CrossRefPubMedGoogle Scholar
  47. 47.
    Kerr JS, Wilson CH. Nuclear receptor-binding protein 1: a novel tumour suppressor and pseudokinase. Biochem Soc Trans. 2013;41:1055–60.CrossRefPubMedGoogle Scholar
  48. 48.
    Hilt W, Wolf DH. Proteasomes: destruction as a programme. Trends Biochem Sci. 1996;21:96–102.CrossRefPubMedGoogle Scholar
  49. 49.
    Smith DK, Xue H. Sequence profiles of immunoglobulin and immunoglobulin-like domains. J Mol Biol. 1997;274:530–45.CrossRefPubMedGoogle Scholar
  50. 50.
    Bateman A, Sandford R. The PLAT domain: a new piece in the PKD1 puzzle. Curr Biol. 1999;9:R588–90.CrossRefPubMedGoogle Scholar
  51. 51.
    Gamsjaeger R, Liew CK, Loughlin FE, Crossley M, Mackay JP. Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci. 2007;32:63–70.CrossRefPubMedGoogle Scholar
  52. 52.
    Hino S, Kawamata H, Uchida D, Omotehara F, Miwa Y, Begum NM, et al. Nuclear translocation of TSC-22 (TGF-beta-stimulated clone-22) concomitant with apoptosis: TSC-22 as a putative transcriptional regulator. Biochem Biophys Res Commun. 2000;278:659–64.CrossRefPubMedGoogle Scholar
  53. 53.
    Friesen WJ, Wyce A, Paushkin S, Abel L, Rappsilber J, Mann M, et al. A novel WD repeat protein component of the methylosome binds Sm proteins. J Biol Chem. 2002;277:8243–7.CrossRefPubMedGoogle Scholar
  54. 54.
    Antonysamy S, Bonday Z, Campbell RM, Doyle B, Druzina Z, Gheyi T, et al. Crystal structure of the human PRMT5:MEP50 complex. Proc Natl Acad Sci U S A. 2012;109:17960–5.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Ho MC, Wilczek C, Bonanno JB, Xing L, Seznec J, Matsui T, et al. Structure of the arginine methyltransferase PRMT5-MEP50 reveals a mechanism for substrate specificity. Plos One. 2013;8:e57008.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Yi P, Gao S, Gu Z, Huang T, Wang Z. P44/WDR77 restricts the sensitivity of proliferating cells to TGFbeta signaling. Biochem Biophys Res Commun. 2014;450:409–15.CrossRefPubMedGoogle Scholar
  57. 57.
    Choi SJ, Moon JH, Ahn YW, Ahn JH, Kim DU, Han TH. Tsc-22 enhances TGF-beta signaling by associating with Smad4 and induces erythroid cell differentiation. Mol Cell Biochem. 2005;271:23–8.CrossRefPubMedGoogle Scholar
  58. 58.
    Uchida D, Omotehara F, Nakashiro K, Tateishi Y, Hino S, Begum NM, et al. Posttranscriptional regulation of TSC-22 (TGF-beta-stimulated clone-22) gene by TGF-beta 1. Biochem Biophys Res Commun. 2003;305:846–54.CrossRefPubMedGoogle Scholar
  59. 59.
    Gupta RA, Sarraf P, Brockman JA, Shappell SB, Raftery LA, Willson TM, et al. Peroxisome proliferator-activated receptor gamma and transforming growth factor-beta pathways inhibit intestinal epithelial cell growth by regulating levels of TSC-22. J Biol Chem. 2003;278:7431–8.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2016

Authors and Affiliations

  • Qiao Li
    • 1
    • 2
  • Pan Chen
    • 3
  • Zhaoyang Zeng
    • 1
    • 2
    • 3
  • Fang Liang
    • 2
  • Yali Song
    • 2
  • Fang Xiong
    • 1
  • Xiayu Li
    • 4
  • Zhaojian Gong
    • 2
  • Ming Zhou
    • 2
    • 3
    • 4
  • Bo Xiang
    • 2
    • 3
    • 4
  • Cong Peng
    • 1
  • Xiaoling Li
    • 1
    • 2
    • 3
  • Xiang Chen
    • 1
  • Guiyuan Li
    • 2
    • 3
    • 4
  • Wei Xiong
    • 1
    • 2
    • 3
  1. 1.The Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Xiangya HospitalCentral South UniversityChangshaChina
  2. 2.The Key Laboratory of Carcinogenesis of the Chinese Ministry of Health, Cancer Research InstituteCentral South UniversityChangshaChina
  3. 3.Hunan Key Laboratory of Translational Radiation Oncology, Hunan Cancer Hospital and The Affiliated Cancer Hospital of Xiangya School of MedicineCentral South UniversityChangshaChina
  4. 4.Hunan Key Laboratory of Nonresolving Inflammation and Cancer, Disease Genome Research Center, The Third Xiangya HospitalCentral South UniversityChangshaChina

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