Skip to main content

Advertisement

SpringerLink
Log in

Poly(ADP-ribosyl)ation of mannose-binding lectin out of human kidney cells

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Mannose-binding lectin was identified as a substrate of tankyrase 2, an enzyme that catalyzes poly(ADP-ribosyl)ation. The endogenous tankyrase 2 was isolated out of cytoplasm of human embryonic kidney cells. It was bound to a soluble complex of at least two other proteins; they were identified using specific antibodies and other approaches as keratin 1 and mannose-binding lectin. Using immunoblot analysis and radioactive labeling, we detected tankyrase-2-dependent poly(ADP-ribosyl)ation of mannose-binding lectin. In the presence of NAD+, the complex of keratin 1 and lectin was dissociated, what was recorded during elution of its separate components out of affinity columns and by decrease of their apparent molecular masses during gel-filtration. Tankyrase 2 also inhibited the carbohydrate-binding function of the lectin. The latter effect was observed using mannose-binding lectin out of human serum, which is free from keratin 1. As a result of tankyrase-2 activity, the lectin lost its affinity to mannan-agarose. The discovery of this new biochemical mechanism justifies further analysis of its physiological and medical significance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

GFP:

Green fluorescent protein

HEK cells:

Human embryonic kidney cells

K1:

Keratin 1

mAb:

Monoclonal antibody

MBL:

Mannose-binding lectin

Nic:

Nicotinamide

PAR:

Polymer of ADP-ribose

PARP:

Poly(ADP-ribose) polymerase

PARsylation:

Poly(ADP-ribosyl)ation

References

  1. Smith S, Giriat I, Schmitt A, de Lange T (1998) Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282:1484–1487. doi:10.1126/science.282.5393.1484

    Article  PubMed  CAS  Google Scholar 

  2. Smith S, de Lange T (1999) Cell cycle dependent localization of the telomeric PARP, tankyrase, to nuclear pore complexes and centrosomes. J Cell Sci 112:3649–3656

    PubMed  CAS  Google Scholar 

  3. De Rycker M, Venkatesan RN, Wei C, Price CM (2003) Vertebrate tankyrase domain structure and sterile alpha motif (SAM)-mediated multimerization. Biochem J 372:87–96. doi:10.1042/BJ20021450

    Article  PubMed  Google Scholar 

  4. Sidorova N, Zavalishina L, Kurchashova S, Korsakova N, Nazhimov V, Frank G, Kuimov A (2006) Immunohistochemical detection of tankyrase 2 in human breast tumors and normal renal tissue. Cell Tissue Res 323:137–145. doi:10.1007/s00441-005-0053-8

    Article  PubMed  CAS  Google Scholar 

  5. Chi NW, Lodish HF (2000) Tankyrase is a golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J Biol Chem 275:38437–38444. doi:10.1074/jbc.M007635200

    Article  PubMed  CAS  Google Scholar 

  6. Chang P, Coughlin M, Mitchison TJ (2005) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 7:1133–1139. doi:10.1038/ncb1322

    Article  PubMed  CAS  Google Scholar 

  7. Seimiya H, Smith S (2002) The telomeric poly(ADP-ribose) polymerase, tankyrase 1, contains multiple binding sites for telomeric repeat binding factor 1 (TRF1) and a novel acceptor, 182-kDa tankyrase-binding protein (TAB 182). J Biol Chem 277:14116–14126. doi:10.1074/jbc.M112266200

    Article  PubMed  CAS  Google Scholar 

  8. Chiang YJ, Hsiao SJ, Yver D, Cushman SW, Tessarollo L, Smith S, Hodes RJ (2008) Tankyrase 1 and Tankyrase 2 are essential but redundant for mouse embryonic development. PLoS ONE 3:e2639. doi:10.1371/journal.pone.0002639

    Article  PubMed  Google Scholar 

  9. Kuimov AN, Kuprash DV, Petrov VN, Vdovichenko KK, Scanlan MJ, Jongeneel CV, Lagarkova MA, Nedospasov SA (2001) Cloning and characterization of TNKL, a member of tankyrase gene family. Genes Immun 2:52–55. doi:10.1038/sj.gene.6363722

    Article  PubMed  CAS  Google Scholar 

  10. Karner CM, Merkel CE, Dodge M, Ma Z, Lu J, Chen C, Lum L, Carroll TJ (2010) Tankyrase is necessary for canonical Wnt signaling during kidney development. Dev Dyn 239:2014–2023. doi:10.1002/dvdy.22340

    Article  PubMed  CAS  Google Scholar 

  11. Kuimov AN, Terekhov SM (2003) Soluble tankyrase located in cytosol of human embryonic kidney cell line 293. Biochemistry (Mosc.) 68:260–268

    Article  CAS  Google Scholar 

  12. De Rycker M, Price CM (2004) Tankyrase polymerization is controlled by its sterile alpha motif and poly(ADP-ribose) polymerase domains. Mol Cell Biol 24:9802–9812. doi:10.1128/MCB.24.22.9802-9812.2004

    Article  PubMed  Google Scholar 

  13. Sidorova NN, Fadeev AO, Kuimov AN (2008) Isolation and physicochemical properties of tankyrase of human embryonic kidney cells of line 293. Biochemistry (Mosc.) 73:289–295

    Article  CAS  Google Scholar 

  14. Colley KJ, Beranek MC, Baenziger JU (1988) Purification and characterization of the core-specific lectin from human serum and liver. Biochem J 256:61–68

    PubMed  CAS  Google Scholar 

  15. Downing I, Coch KC, Kilpatrick DC (2003) Immature dendritic cells possess a sugar-sensitive receptor for human mannan-binding lectin. Immunology 109:360–364. doi:10.1046/j.1365-2567.2003.01675.x

    Article  PubMed  CAS  Google Scholar 

  16. Roos A, Daha MR, van Pelt J, Berger SP (2007) Mannose-binding lectin and the kidney. Nephrol Dial Transplant 22:3370–3377. doi:10.1093/ndt/gfm524

    Article  PubMed  CAS  Google Scholar 

  17. Gardai SJ, Bratton DL, Ogden CA, Henson PM (2006) Recognition ligands on apoptotic cells: a perspective. J Leukoc Biol 79:896–903. doi:10.1189/jlb.1005550

    Article  PubMed  CAS  Google Scholar 

  18. Collard CD, Montalto MC, Reenstra WR, Buras JA, Stahl GL (2001) Endothelial oxidative stress activates the lectin complement pathway. Role of cytokeratin 1. Am J Pathol 159:1045–1054

    Article  PubMed  CAS  Google Scholar 

  19. Astern JM, Pendergraft WF 3rd, Falk RJ, Jennette JC, Schmaier AH, Mahdi F, Preston GA (2007) Myeloperoxidase interacts with endothelial cell-surface cytokeratin 1 and modulates bradykinin production by the plasma kallikrein-kinin system. Am J Pathol 171:349–359. doi:10.2353/ajpath.2007.060831

    Article  PubMed  CAS  Google Scholar 

  20. Hasan AAK, Zisman T, Schmaier AH (1998) Identification of cytokeratin 1 as a binding protein and presentation receptor for kininogens on endothelial cells. Proc Natl Acad Sci USA 95:3615–3620. doi:10.1073/pnas.95.7.3615

    Article  PubMed  CAS  Google Scholar 

  21. Mahdi F, Shariat-Madar Z, Todd RF 3rd, Figueroa CD, Schmaier AH (2001) Expression and colocalization of cytokeratin 1 and urokinase plasminogen activator receptor on endothelial cells. Blood 97:2342–2350. doi:10.1182/blood.V97.8.2342

    Article  PubMed  CAS  Google Scholar 

  22. Yokoyama WM (2004) Production of monoclonal antibodies. In: Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W (eds) Current protocols in immunology. Wiley, Newcastle, pp 2.5.1–2.5.17. doi:10.1002/0471142735.im0205s74

    Google Scholar 

  23. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  PubMed  CAS  Google Scholar 

  24. Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685. doi:10.1038/227680a0

    Article  PubMed  CAS  Google Scholar 

  25. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858. doi:10.1021/ac950914h

    Article  PubMed  CAS  Google Scholar 

  26. de Vries B, Walter SJ, Peutz-Kootstra CJ, Wolfs TGAM, van Heurn LWE, Buurman WA (2004) The mannose-binding lectin-pathway is involved in complement activation in the course of renal ischemia-reperfusion injury. Am J Pathol 165:1677–1688

    Article  PubMed  Google Scholar 

  27. Morio H, Kurata H, Katsuyama R, Oka S, Kozutsumi Y, Kawasaki T (1997) Renal expression of serum-type mannan-binding protein in rat. Eur J Biochem 243:770–774. doi:10.1111/j.1432-1033.1997.00770.x

    Article  PubMed  CAS  Google Scholar 

  28. Wagner S, Lynch NJ, Walter W, Schwaeble WJ, Loos M (2003) Differential expression of the murine mannose-binding lectins A and C in lymphoid and nonlymphoid organs and tissues. J Immunol 170:1462–1465

    PubMed  CAS  Google Scholar 

  29. Seyfarth J, Garred P, Madsen HO (2006) Extra-hepatic transcription of the human mannose-binding lectin gene (mbl2) and the MBL-associated serine protease 1–3 genes. Mol Immunol 43:962–971. doi:10.1016/j.molimm.2005.06.033

    Article  PubMed  CAS  Google Scholar 

  30. Sbodio J, Chi NW (2002) Identification of a tankyrase-binding motif shared by IRAP, TAB 182, and human TRF1 but not mouse TRF1. NuMA contains this RxxPDG motif and is a novel tankyrase partner. J Biol Chem 277:31887–31892. doi:10.1074/jbc.M203916200

    Article  PubMed  CAS  Google Scholar 

  31. Fujita T, Matsushita M, Endo Y (2004) The lectin-complement pathway—its role in innate immunity and evolution. Immunol Rev 198:185–202. doi:10.1111/j.0105-2896.2004.0123.x

    Article  PubMed  CAS  Google Scholar 

  32. Zeng G, Aldridge ME, Tian X, Seiler D, Zhang X, Jin Y, Rao J, Li W, Chen D, Langford MP, Duggan C, Belldegrun AS, Dubinett SM (2006) Dendritic cell surface calreticulin is a receptor for NY-ESO-1: direct interactions between tumor-associated antigen and the innate immune system. J Immunol 177:3582–3589

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank M. Mogilnikov (A.N. Belozersky Institute, Moscow State University) for his help with the confocal microscopy. This study was supported by the Russian Foundation for Basic Research, grant number 09-04-00962.

Author information

Authors and Affiliations

  1. A.N.Belozersky Institute, Lomonosov Moscow State University, 119992, Moscow, Russia

    Natalie N. Sidorova, Svetlana Yu. Kurchashova & Alexander N. Kuimov

  2. Department of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119992, Moscow, Russia

    Tural Ya. Yarahmedov

  3. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    Rustam H. Ziganshin

Authors
  1. Natalie N. Sidorova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svetlana Yu. Kurchashova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tural Ya. Yarahmedov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rustam H. Ziganshin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexander N. Kuimov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander N. Kuimov.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 206 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sidorova, N.N., Kurchashova, S.Y., Yarahmedov, T.Y. et al. Poly(ADP-ribosyl)ation of mannose-binding lectin out of human kidney cells. Mol Cell Biochem 352, 231–238 (2011). https://doi.org/10.1007/s11010-011-0758-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-011-0758-9

Keywords

Search

Navigation