Skip to main content
Log in

The analysis of the poly(ADPR)polymerase mode of action in rat testis nuclear fractions defines a specific poly(ADP-ribosyl)ation system associated with the nuclear matrix

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

Abstract

The poly(ADP-ribosyl)ation system, associated with different nuclear fractions of rat testis, has been analyzed for both pADPR and pADPR acceptor proteins. The DNase I sensitive and resistant chromatin contain 35% and 40%, respectively, of the total pADPR synthesized in intact nuclei incubated with [32P]NAD. Moreover, the residual 25% were estimated to be associated with the nuclear matrix.Three different classes of pADPR are present in the nuclei. The longest and branched ADPribose polymers modify proteins present in the DNase I resistant (2 M NaCl extractable) chromatin and in the nuclear matrix, whereas polymers of > 20 residues interact with the components of the DNase I sensitive chromatin and oligomers of 6 ADPribose residues are bound specifically to the acid-soluble chromosomal proteins, present in isolated nuclear matrix. The main pADPR acceptor protein in all the nuclear fractions is represented by the PARP itself (auto-modification reaction). The hetero-modification reaction occurs mostly on histone H1 and core histones, that have been found associated to DNase I sensitive and resistant chromatin, respectively. Moreover, an oligo(ADP-ribosyl)ation occurs on core histones tightly-bound to the matrix associated regions (MARs) of chromatin loops.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Davie JR: The nuclear matrix and the regulation of chromatin organization and function. Intern Rev of Cytol 162A: 191–249, 1995

    Google Scholar 

  2. Berezney R: The nuclear matrix: A heuristic model for investigating genomic organization and function in the cell nucleus. J Cell Biochem 47: 109–123, 1991

    Article  PubMed  Google Scholar 

  3. Johansen KM: Dynamic remodeling of nuclear architecture during the cell cycle. J Cell Biochem 60: 289–296, 1996

    Article  PubMed  Google Scholar 

  4. Boulikas T: Chromatin domains and prediction of MAR sequences. Int Rev Cytol 1624: 279–388, 1995

    Google Scholar 

  5. Jack RS, Eggert H: The elusive nuclear matrix. Eur J Biochem 209: 503–509, 1992

    PubMed  Google Scholar 

  6. Xu R, Hammer RE, Blasquez VC, Jones SL, Garrard WT: Immunoglobulin k gene expression after stable integration. Role of the intronic MAR and enhancer in transgenic mice. J Biol Chem 264: 21190–21195, 1989

    PubMed  Google Scholar 

  7. Kramer JA, Krawetz SA: Nuclear matrix interactions within the sperm genome. J Biol Chem 271: 11619–11622, 1996

    Article  PubMed  Google Scholar 

  8. Stuurman van Driel R, de Jong L, Meije AM, van Renswoude J: The protein composition of the nuclear matrix of murine P19 embryonal carcinoma cells is differentiation-stage dependent. Exp Cell Res 180: 460–466, 1989

    Article  PubMed  Google Scholar 

  9. Samuel SK, Minish TM, Davie JR: Nuclear matrix proteins in well and poorly differentiated human breast cancer cell lines. J Cell Biochem 66: 9–15, 1997

    Article  PubMed  Google Scholar 

  10. Kaufman SH, Gibson W, Shaper JH: Characterization of the major polypeptides of the rat liver nuclear envelope. J Biol Chem 258: 2710–2719, 1983

    PubMed  Google Scholar 

  11. Hakes DJ, Berezney R: Molecular cloning of matrin F/G: A DNA binding protein of the nuclear matrix that contains putative zinc finger motifs. Proc Natl Acad Sci USA 88: 6186–6190, 1991

    PubMed  Google Scholar 

  12. Buhrmester H, von Kries JP, Stratling WH: Nuclear matrix protein ARBP recognizes a novel DNA sequence motif with high affinity. Biochemistry 34: 4108–4117, 1995

    Article  PubMed  Google Scholar 

  13. Nakagomi K, Kohwi Y, Dickinson LA, Kohwi-Shigemats, T: A novel DNA binding motif in the nuclear matrix attachment DNA-binding protein SATB1. Mol Cell Biol 14: 1852–1860, 1994

    PubMed  Google Scholar 

  14. Davie JR, Hendzel MJ: Multiple functions of dynamic histone acetylation. J Cell Biochem 55: 98–105, 1994

    Article  PubMed  Google Scholar 

  15. Adachi Y, Kas E, Laemmli UK: Preferential cooperative binding of topoisomerase II to scaffold associated regions. EMBO. J. 8: 3997–4006, 1989

    PubMed  Google Scholar 

  16. Joudka B, Spiess E, Angiolillo A, Joswig G, Rothbarth K, Werner D: High salt–and SDS stable DNA binding protein complexes with ATPase and protein kinase activity retained in chromatin depleted nucleus. Nucleic Acid Res. 23: 1, 1995

    PubMed  Google Scholar 

  17. Meiestrich ML, Trostle PK, Brock W: Association of nucleoprotein transitions with chromatin changes during rat spermatogenesis. In: H.J. Vogel (ed). Bioregulators of Reproduction. Acad Press New York, 1981, pp 151–166.

  18. Waterborg JH: Dynamic methylation of alfa-alfa histones H3. J Biol Chem 268: 4918–4921, 1993

    PubMed  Google Scholar 

  19. Van Holde KE: Chromatin. In: A. Rich (ed). Springer Series in Molecular Biology Springer-Verlag New York, 1988

    Google Scholar 

  20. Althaus FR: Poly-ADP-Ribosylation Reactions. In: M. Solioz (ed). ADPribosylation of Proteins: Mol Bio, Biochem and Biophysics. Part I, Springer-Verlag Berlin, 1987

    Google Scholar 

  21. Quesada P, d'Erme M, Parise G, Faraone-Mennella MR, Caiafa P, Farina B: Nuclear matrix associated poly(ADPribosyl)ation system in rat testis chromatin. Exp Cell Res 214: 351–357, 1994

    Article  PubMed  Google Scholar 

  22. Lautier D, Lagueux J, Thibodeau J, Menard L, Poirier GG: Molecular and biochemical features of poly(ADP-ribose) metabolism. Mol Cell Biochem 122: 171–183, 1993

    Article  PubMed  Google Scholar 

  23. de Murcia G, Menissier-de Murcia J: Poly(ADP-ribose) polymerase: a molecular nick-sensor. TIBS 19: 172–176, 1994

    PubMed  Google Scholar 

  24. Lindahl T, Satoh MS, Poirier GG: Post-translational modification of poly(ADPribose)polymerase induced by DNA strand breaks. TIBS 20: 405–411, 1995

    PubMed  Google Scholar 

  25. de Murcia G, Schreiber V, Molinette M, Saulier B, Poch O, Masson M., Niedergang C, Menissier-de Murcia J: Structure and function of poly(ADP-ribose)polymerase. Mol Cell Biochem 138: 15–24, 1994

    Article  PubMed  Google Scholar 

  26. Desmarais Y, Menard L, Lagueux J, Poirier GG: Enzymological properties of poly(ADP-ribose)polymerase: characterization of automodification sites and NADase activity. Biochem Biophys Acta 1078: 179–186, 1991

    PubMed  Google Scholar 

  27. Alvarez-Gonzales R, Pacheco-Rodriguez G, Mendoza-Alvarez H: Enzymology of ADP-ribose polymer synthesis. Mol Cell Biochem 138: 33–37, 1994

    Article  PubMed  Google Scholar 

  28. Boulikas T: Poly(ADPribosyl)ated histones in chromatin replication. J Biol Chem 265: 14638–14647, 1990

    PubMed  Google Scholar 

  29. Realini C, Althaus FR: Histone shuttling by poly(ADP-ribosylation). J Biol Chem 267: 18858–18865, 1992

    PubMed  Google Scholar 

  30. Braun SA, Panzeter PL, Collinge MA, Althaus FR: Endoglycosidic cleavage of branched polymers by poly (ADP-ribose) glycohydrolase. Eur J Biochem 220: 369–375, 1994

    Article  PubMed  Google Scholar 

  31. Boulikas T: Poly(ADP-ribose) synthesis in blocked and damaged cells and its relation with carcinogenesis. Anticancer Res. 12: 885–898, 1992

    PubMed  Google Scholar 

  32. Dantzer F, Nasheuer HP, Vonesch JL, de Murcia G, Menissier-de Murcia J: Functional association of poly(ADPR-ribose) polymerase with DNA polymerase alpha-primase complex: a link between DNA strand break detection and DNA replication. Nucl Acid Res 15: 1891–1898, 1998

    Article  Google Scholar 

  33. Kawamura T, Hanai S, Yokota T, Hayaishi T, Poltronieri P, Miwa M, Uchida K: An alternative form of poly(ADP-ribose)polymerase in Drosofila Melanogaster and its ectopic expression in rat-1 cells. Biochem Biophys Res Commun 251: 35–40, 1998

    Article  PubMed  Google Scholar 

  34. Smith S, Giriat I, Schimitt A, de Lange T: Tankyrase, a poly(ADPribose) polymerase at human telomers. Science 282: 1484–1487, 1998

    PubMed  Google Scholar 

  35. Panzeter PL, Althaus FR: High resolution size analysis of ADPribose polymers using modified DNA sequencing gels. Nucleic Acid Res 18: 2194, 1990

    PubMed  Google Scholar 

  36. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC: Cleavage of poly(ADP-ribose)polymerase by a proteinase with properties like ICE. Nature, 371: 346–347, 1994

    Article  PubMed  Google Scholar 

  37. Naegeli H, Althaus FR: Regulation of poly(ADPribose)polymerase. Histone-specific adaptations of reaction products. J Biol Chem 266: 10596–10601, 1991

    PubMed  Google Scholar 

  38. Burkle A, Muller M, Wolf I, Kupper JH: Poly(ADP-ribose) polymerase activity in intact or permeabilized leukocytes from mammalian species of different longevity. Mol Cell Biochem 138: 85–90, 1994

    Article  PubMed  Google Scholar 

  39. Kaufman SH, Brunet G, Talbot B, Lamarre D, Dumas C, Shaper JH, Poirier G G: Association of poly(ADPR)polymerase with the nuclear matrix:the role of intermolecular disulfide bond formation. Exp Cell Res 192: 524–535, 1991

    Article  PubMed  Google Scholar 

  40. Desnoyers S, Kirkland JB, Poirier GG: Association of poly(ADPribose) polymerase with nuclear subfractions catalyzed with sodium tetrationate and hydrogene peroxide crosslinks. Mol Cell Biochem, 159: 155–161, 1996

    Article  PubMed  Google Scholar 

  41. De Lucia F, Faraone-Mennella MR, Quesada P, Farina B: Poly-(ADPribosyl)ation system in transcriptionally active rat testis chromatin fraction. J Cell Biochem 63: 334–341, 1996

    Article  PubMed  Google Scholar 

  42. Wesierska-Gadek J, Sauermann G: Modification of nuclear matrix proteins by ADP-ribosylation. Eur J Biochem 153: 421–428, 1985

    Article  PubMed  Google Scholar 

  43. Alvarez-Gonzales R, Ringer DP: Nuclear matrix associated poly(ADP-ribose) metabolism in regenerating rat liver. FEBS Letters 236: 362–366, 1988

    Article  PubMed  Google Scholar 

  44. Jarman AP, Higgs DR: Nuclear scaffold attachment sites in the human globin gene complexes. EMBO J. 7: 3337–3344, 1988

    PubMed  Google Scholar 

  45. Kalandadze AG, Bushara SA, Vassetsky YS, Razin SV: Characterization of the DNA pattern in the site of permanent attachment to the nuclear matrix located in the vicinity of replication origin. Biochem Biophys Res Commun 168: 9–15, 1990

    Article  PubMed  Google Scholar 

  46. Quesada P, Atorino L, Cardone A, Ciarcia G, Farina B: Poly-(ADPribosyl)ation system in rat germinal cells at different stages of differentiation. Exp Cell Res 226: 183–190, 1996

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quesada, P., Tramontano, F., Faraone-Mennella, M.R. et al. The analysis of the poly(ADPR)polymerase mode of action in rat testis nuclear fractions defines a specific poly(ADP-ribosyl)ation system associated with the nuclear matrix. Mol Cell Biochem 205, 91–99 (2000). https://doi.org/10.1023/A:1007005715848

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1007005715848

Navigation