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Tumor Biology

, Volume 37, Issue 8, pp 10785–10791 | Cite as

The potential role of CacyBP/SIP in tumorigenesis

  • Xiaoxuan Ning
  • Yang Chen
  • Xiaosu Wang
  • Qiaoneng Li
  • Shiren Sun
Original Article

Abstract

Calcyclin-binding protein/Siah-1-interacting protein (CacyBP/SIP) was initially described as a binding partner of S100A6 in the Ehrlich ascites tumor cells and later as a Siah-1-interacting protein. This 30 kDa protein includes three domains and is involved in cell proliferation, differentiation, cytoskeletal rearrangement, and transcriptional regulation via binding to various proteins. Studies have also shown that the CacyBP/SIP is a critical protein in tumorigenesis. But, its promotion or suppression of cancer progression may depend on the cell type. In this review, the biological characteristics and target proteins of CacyBP/SIP have been described. Moreover, the exact role of CacyBP/SIP in various cancers is discussed.

Keywords

CacyBP/SIP β-Catenin Tumorigenesis Multidrug resistance 

Notes

Acknowledgments

This work was supported by grants from the National Nature Science Foundation of China (Nos. 81272203, 2012K-13-01-08, and 30872964) and by Irma and Paul Milstein Program for Senior Health Awards.

Compliance with ethical standards

Conflicts of interest

None

References

  1. 1.
    Filipek A, Wojda U. p30, a novel protein target of mouse calcyclin (S100A6). Biochem J. 1996;320(Pt 2):585–7.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Filipek A, Jastrzebska B, Nowotny M, Kuznicki J. CacyBP/SIP, a calcyclin and Siah-1-interacting protein, binds EF-hand proteins of the S100 family. J Biol Chem. 2002;277:28848–52.CrossRefPubMedGoogle Scholar
  3. 3.
    Xia ZB, Dai MS, Magoulas C, Broxmeyer HE, Lu L. Differentially expressed genes during in vitro differentiation of murine embryonic stem cells transduced with a human erythropoietin receptor cDNA. J Hematother Stem Cell Res. 2000;9:651–8.CrossRefPubMedGoogle Scholar
  4. 4.
    Pircher TJ, Geiger JN, Zhang D, Miller CP, Gaines P, Wojchowski DM. Integrative signaling by minimal erythropoietin receptor forms and c-Kit. J Biol Chem. 2001;276:8995–9002.CrossRefPubMedGoogle Scholar
  5. 5.
    Breen EC, Tang K. Calcyclin (S100A6) regulates pulmonary fibroblast proliferation, morphology, and cytoskeletal organization in vitro. J Cell Biochem. 2003;88:848–54.CrossRefPubMedGoogle Scholar
  6. 6.
    Schneider G, Filipek A. S100A6 binding protein and Siah-1 interacting protein (CacyBP/SIP): spotlight on properties and cellular function. Amino Acids. 2011;41:773–80.CrossRefPubMedGoogle Scholar
  7. 7.
    Matsuzawa SI, Reed JC. Siah-1, SIP, and Ebi collaborate in a novel pathway for beta-catenin degradation linked to p53 responses. Mol Cell. 2001;7:915–26.CrossRefPubMedGoogle Scholar
  8. 8.
    Filipek A. S100A6 and CacyBP/SIP—two proteins discovered in ehrlich ascites tumor cells that are potentially involved in the degradation of beta-catenin. Chemotherapy. 2006;52:32–4.CrossRefPubMedGoogle Scholar
  9. 9.
    Gonzalez-Moles MA, Ruiz-Avila I, Gil-Montoya JA, Plaza-Campillo J, Scully C. Beta-catenin in oral cancer: an update on current knowledge. Oral Oncol. 2014;50:818–24.CrossRefPubMedGoogle Scholar
  10. 10.
    Zhang X, Hao J. Development of anticancer agents targeting the Wnt/beta-catenin signaling. Am J Cancer Res. 2015;5:2344–60.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Zhai H, Meng J, Jin H, Li Y, Wang J. Role of the CacyBP/SIP protein in gastric cancer. Oncol Lett. 2015;9:2031–5.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Filipek A, Kuznicki J. Molecular cloning and expression of a mouse brain cDNA encoding a novel protein target of calcyclin. J Neurochem. 1998;70:1793–8.CrossRefPubMedGoogle Scholar
  13. 13.
    Fukushima T, Zapata JM, Singha NC, et al. Critical function for SIP, a ubiquitin E3 ligase component of the beta-catenin degradation pathway, for thymocyte development and G1 checkpoint. Immunity. 2006;24:29–39.CrossRefPubMedGoogle Scholar
  14. 14.
    Jastrzebska B, Filipek A, Nowicka D, Kaczmarek L, Kuznicki J. Calcyclin (S100A6) binding protein (CacyBP) is highly expressed in brain neurons. J Histochem Cytochem: Off J Histochem Soc. 2000;48:1195–202.CrossRefGoogle Scholar
  15. 15.
    Zhai H, Shi Y, Jin H, et al. Expression of calcyclin-binding protein/Siah-1 interacting protein in normal and malignant human tissues: an immunohistochemical survey. J Histochem Cytochem: Off J Histochem Soc. 2008;56:765–72.CrossRefGoogle Scholar
  16. 16.
    Filipek A, Jastrzebska B, Nowotny M, et al. Ca2+−dependent translocation of the calcyclin-binding protein in neurons and neuroblastoma NB-2a cells. J Biol Chem. 2002;277:21103–9.CrossRefPubMedGoogle Scholar
  17. 17.
    Wu J, Tan X, Peng X, Yuan J, Qiang B. Translocation and phosphorylation of calcyclin binding protein during retinoic acid-induced neuronal differentiation of neuroblastoma SH-SY5Y cells. J Biochem Mol Biol. 2003;36:354–8.PubMedGoogle Scholar
  18. 18.
    Schneider G, Nieznanski K, Jozwiak J, Slomnicki LP, Redowicz MJ, Filipek A. Tubulin binding protein, CacyBP/SIP, induces actin polymerization and may link actin and tubulin cytoskeletons. Biochim Biophys Acta. 2010;1803:1308–17.CrossRefPubMedGoogle Scholar
  19. 19.
    Bhattacharya S, Lee YT, Michowski W, et al. The modular structure of SIP facilitates its role in stabilizing multiprotein assemblies. Biochemistry. 2005;44:9462–71.CrossRefPubMedGoogle Scholar
  20. 20.
    Santelli E, Leone M, Li C, et al. Structural analysis of Siah1-Siah-interacting protein interactions and insights into the assembly of an E3 ligase multiprotein complex. J Biol Chem. 2005;280:34278–87.CrossRefPubMedGoogle Scholar
  21. 21.
    Nowotny M, Bhattacharya S, Filipek A, Krezel AM, Chazin W, Kuznicki J. Characterization of the interaction of calcyclin (S100A6) and calcyclin-binding protein. J Biol Chem. 2000;275:31178–82.CrossRefPubMedGoogle Scholar
  22. 22.
    Lee YT, Dimitrova YN, Schneider G, et al. Structure of the S100A6 complex with a fragment from the C-terminal domain of Siah-1 interacting protein: a novel mode for S100 protein target recognition. Biochemistry. 2008;47:10921–32.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Au KW, Kou CY, Woo AY, et al. Calcyclin binding protein promotes DNA synthesis and differentiation in rat neonatal cardiomyocytes. J Cell Biochem. 2006;98:555–66.CrossRefPubMedGoogle Scholar
  24. 24.
    Schneider G, Nieznanski K, Kilanczyk E, Bieganowski P, Kuznicki J, Filipek A. CacyBP/SIP interacts with tubulin in neuroblastoma NB2a cells and induces formation of globular tubulin assemblies. Biochim Biophys Acta. 2007;1773:1628–36.CrossRefPubMedGoogle Scholar
  25. 25.
    Pedrotti B, Colombo R, Islam K. Interactions of microtubule-associated protein MAP2 with unpolymerized and polymerized tubulin and actin using a 96-well microtiter plate solid-phase immunoassay. Biochemistry. 1994;33:8798–806.CrossRefPubMedGoogle Scholar
  26. 26.
    Barrett LE, Van Bockstaele EJ, Sul JY, Takano H, Haydon PG, Eberwine JH. Elk-1 associates with the mitochondrial permeability transition pore complex in neurons. Proc Natl Acad Sci U S A. 2006;103:5155–60.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Pouyssegur J, Volmat V, Lenormand P. Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling. Biochem Pharmacol. 2002;64:755–63.CrossRefPubMedGoogle Scholar
  28. 28.
    Kilanczyk E, Filipek S, Jastrzebska B, Filipek A. CacyBP/SIP binds ERK1/2 and affects transcriptional activity of Elk-1. Biochem Biophys Res Commun. 2009;380:54–9.CrossRefPubMedGoogle Scholar
  29. 29.
    Wasik U, Kadziolka B, Kilanczyk E and Filipek A. Influence of S100A6 on CacyBP/SIP Phosphorylation and Elk-1 transcriptional activity in neuroblastoma NB2a cells. J Cell Biochem. 2016;117:126–31.Google Scholar
  30. 30.
    Topolska-Wos AM, Shell SM, Kilanczyk E, Szczepanowski RH, Chazin WJ, Filipek A. Dimerization and phosphatase activity of calcyclin-binding protein/Siah-1 interacting protein: the influence of oxidative stress. FASEB J: Off Publ Fed Am Soc Exp Biol. 2015;29:1711–24.CrossRefGoogle Scholar
  31. 31.
    Jiang HL, Jiang LM, Han WD. Wnt/beta-catenin signaling pathway in lung cancer stem cells is a potential target for the development of novel anticancer drugs. J BUON: Off J Balkan Union Oncol. 2015;20:1094–100.Google Scholar
  32. 32.
    Wang G, Feng CC, Chu SJ, et al. Toosendanin inhibits growth and induces apoptosis in colorectal cancer cells through suppression of AKT/GSK-3beta/beta-catenin pathway. Int J Oncol. 2015.Google Scholar
  33. 33.
    Ning X, Sun S, Hong L, et al. Calcyclin-binding protein inhibits proliferation, tumorigenicity, and invasion of gastric cancer. Mol Cancer Res: MCR. 2007;5:1254–62.CrossRefPubMedGoogle Scholar
  34. 34.
    Ning X, Sun S, Zhang K, et al. S100A6 protein negatively regulates CacyBP/SIP-mediated inhibition of gastric cancer cell proliferation and tumorigenesis. PLoS One. 2012;7:e30185.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Chen X, Han G, Zhai H, et al. Expression and clinical significance of CacyBP/SIP in pancreatic cancer. Pancreatol: Off J Int Assoc Pancreatol. 2008;8:470–7.CrossRefGoogle Scholar
  36. 36.
    Zhai HH, Meng J, Wang JB, Liu ZX, Li YF, Feng SS. CacyBP/SIP nuclear translocation induced by gastrin promotes gastric cancer cell proliferation. World J Gastroenterol: WJG. 2014;20:10062–70.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Nie F, Yu XL, Wang XG, Tang YF, Wang LL, Ma L. Down-regulation of CacyBP is associated with poor prognosis and the effects on COX-2 expression in breast cancer. Int J Oncol. 2010;37:1261–9.PubMedGoogle Scholar
  38. 38.
    Wang N, Ma Q, Wang Y, Ma G, Zhai H. CacyBP/SIP expression is involved in the clinical progression of breast cancer. World J Surg. 2010;34:2545–52.CrossRefPubMedGoogle Scholar
  39. 39.
    Kilanczyk E, Gwozdzinski K, Wilczek E, Filipek A. Up-regulation of CacyBP/SIP during rat breast cancer development. Breast Cancer. 2014;21:350–7.CrossRefPubMedGoogle Scholar
  40. 40.
    Li S, Li S, Sun Y, Li L. The expression of beta-catenin in different subtypes of breast cancer and its clinical significance. Tumour Biol: J Int Soc Oncodev Biol Med. 2014;35:7693–8.CrossRefGoogle Scholar
  41. 41.
    Cross SS, Hamdy FC, Deloulme JC, Rehman I. Expression of S100 proteins in normal human tissues and common cancers using tissue microarrays: S100A6, S100A8, S100A9 and S100A11 are all overexpressed in common cancers. Histopathology. 2005;46:256–69.CrossRefPubMedGoogle Scholar
  42. 42.
    Sanders ME, Dias EC, Xu BJ, et al. Differentiating proteomic biomarkers in breast cancer by laser capture microdissection and MALDI MS. J Proteome Res. 2008;7:1500–7.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Chen X, Mo P, Li X, et al. CacyBP/SIP protein promotes proliferation and G1/S transition of human pancreatic cancer cells. Mol Carcinog. 2011;50:804–10.CrossRefPubMedGoogle Scholar
  44. 44.
    Ghosh D, Yu H, Tan XF, et al. Identification of key players for colorectal cancer metastasis by iTRAQ quantitative proteomics profiling of isogenic SW480 and SW620 cell lines. J Proteome Res. 2011;10:4373–87.CrossRefPubMedGoogle Scholar
  45. 45.
    Rines AK, Burke MA, Fernandez RP, Volpert OV, Ardehali H. Snf1-related kinase inhibits colon cancer cell proliferation through calcyclin-binding protein-dependent reduction of beta-catenin. FASEB J: Off Publ Fed Am Soc Exp Biol. 2012;26:4685–95.CrossRefGoogle Scholar
  46. 46.
    Ghosh D, Li Z, Tan XF, Lim TK, Mao Y, Lin Q. iTRAQ based quantitative proteomics approach validated the role of calcyclin binding protein (CacyBP) in promoting colorectal cancer metastasis. Mol Cell Proteomics: MCP. 2013;12:1865–80.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Zhao W, Wang C, Wang J, et al. Relationship between CacyBP/SIP expression and prognosis in astrocytoma. J Clin Neurosci: Off J Neurosurg Soc Aust. 2011;18:1240–4.CrossRefGoogle Scholar
  48. 48.
    Khalil AA. Biomarker discovery: a proteomic approach for brain cancer profiling. Cancer Sci. 2007;98:201–13.CrossRefPubMedGoogle Scholar
  49. 49.
    Shi H, Gao Y, Tang Y, et al. CacyBP/SIP protein is important for the proliferation of human glioma cells. IUBMB Life. 2014;66:286–91.CrossRefPubMedGoogle Scholar
  50. 50.
    Sun S, Ning X, Liu J, et al. Overexpressed CacyBP/SIP leads to the suppression of growth in renal cell carcinoma. Biochem Biophys Res Commun. 2007;356:864–71.CrossRefPubMedGoogle Scholar
  51. 51.
    Zhao Y, You H, Liu F, et al. Differentially expressed gene profiles between multidrug resistant gastric adenocarcinoma cells and their parental cells. Cancer Lett. 2002;185:211–8.CrossRefPubMedGoogle Scholar
  52. 52.
    Shi Y, Hu W, Yin F, et al. Regulation of drug sensitivity of gastric cancer cells by human calcyclin-binding protein (CacyBP). Gastric Cancer: Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc. 2004;7:160–6.CrossRefGoogle Scholar
  53. 53.
    Chen X, Zheng P, Xue Z, et al. CacyBP/SIP enhances multidrug resistance of pancreatic cancer cells by regulation of P-gp and Bcl-2. Apoptosis: Int J Program Cell Death. 2013;18:861–9.CrossRefGoogle Scholar
  54. 54.
    Bose S, Panda AK, Mukherjee S, Sa G. Curcumin and tumor immune-editing: resurrecting the immune system. Cell Div. 2015;10:6.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Luo J, Yang J, Yu BY, Liu W, Li M, Zhuang SM. Identification of Siah-interacting protein as a potential regulator of apoptosis and curcumin resistance. Oncogene. 2010;29:6357–66.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2016

Authors and Affiliations

  1. 1.Department of Geriatrics, Xi Jing HospitalFourth Military Medical UniversityXi’anChina
  2. 2.Department of Nephrology, Xi Jing HospitalFourth Military Medical UniversityXi’anChina

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