Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Dimethylnitrosamine-Induced Reduction in the Level of Poly-ADP-Ribosylation of Histone Proteins of Blood Lymphocytes - a Sensitive and Reliable Biomarker for Early Detection of Cancer

  • Kma, Lakhan (Cancer and Radiation Countermeasures Unit, Department of Biochemistry, North-Eastern Hill University) ;
  • Sharan, Rajeshwar Nath (Radiation and Molecular Biology Unit, Department of Biochemistry, North-Eastern Hill University)
  • Published : 2014.08.15
Download PDF
⟨ Previous Next ⟩

Abstract

Poly-ADP-ribosylation (PAR) is a post-translational modification of mainly chromosomal proteins. It is known to be strongly involved in several molecular events, including nucleosome-remodelling and carcinogenesis. In this investigation, it was attempted to evaluate PAR level as a reliable biomarker for early detection of cancer in blood lymphocyte histones. PAR of isolated histone proteins was monitored in normal and dimethylnitrosamine (DMN)-exposed mice tissues using a novel ELISA-based immuno-probe assay developed in our laboratory. An inverse relationship was found between the level of PAR and period of DMN exposure in various histone proteins of blood lymphocytes and spleen cells. With the increase in the DMN exposure period, there was reduction in the PAR level of individual histones in both cases. It was also observed that the decrease in the level of PAR of histones resulted in progressive relaxation of genomic DNA, perhaps triggering activation of genes that are involved in initiation of transformation. The observed effect of carcinogen on the PAR of blood lymphocyte histones provided us with a handy tool for monitoring biochemical or physiological status of individuals exposed to carcinogens without obtaining biopsies of cancerous tissues, which involves several medical and ethical issues. Obtaining blood from any patient and separating blood lymphocytes are routine medical practices involving virtually no medical intervention, post-procedure medical care or trauma to a patient. Moreover, the immuno-probe assay is very simple, sensitive, reliable and cost-effective. Therefore, combined with the ease of preparation of blood lymphocytes and the simplicity of the technique, immuno-probe assay of PAR has the potential to be applied for mass screening of cancer. It appears to be a promising step in the ultimate goal of making cancer detection simple, sensitive and reliable in the near future.

Keywords

References

  1. Althaus FR, Richter C (1987). Poly (ADP-ribose) biosynthesis. In 'ADP-ribosylation of proteins: enzymology and biological significance, molecular biology biochemistry and biophysics', ed solioz m. springer-verlag, New York pp 1-230.
  2. Alvarez-Chaver P, Otero-Estevez O, Paez de la Cadena M et al (2014). Proteomics for discovery of candidate colorectal cancer biomarkers. World J Gastroenterol, 20, 3804-24. https://doi.org/10.3748/wjg.v20.i14.3804
  3. Apostolov EO, Soultanova I, Savenka A et al (2009). Deoxyribonuclease I is essential for DNA fragmentation induced by gamma radiation in mice. Radiat Res, 172, 481-92. https://doi.org/10.1667/RR1647.1
  4. Asubel F, Brent R, Kingston RE et al (1995). Short protocols in molecular biology, third edition, John Wiley and Sons, Inc. USA.
  5. Bao H, Burke PA, Huang J et al (2013). Circulating tumor cells: application as a biomarker for molecular characterization and predictor of survival in an all-comer solid tumor phase I clinical study. PLoS One, 8, 58557-4. https://doi.org/10.1371/journal.pone.0058557
  6. Behrens T, Bonberg N, Casjens S, Pesch B, Bruning T (2014). A practical guide to epidemiological practice and standards in the identification and validation of diagnostic markers using a bladder cancer example. Biochim Biophys Acta, 1844, 145-5. https://doi.org/10.1016/j.bbapap.2013.07.018
  7. Binu S, Soumya SJ, Kumar VB, Sudhakaran PR (2012). Poly-ADP-ribosylation of vascular endothelial growth factor and its implications on angiogenesis. Adv Exp Med Biol, 749, 269-8. https://doi.org/10.1007/978-1-4614-3381-1_18
  8. Blake JA, Bult CJ, Eppig JT, Kadin JA, Richardson JE (2014). The Mouse Genome Database: integration of and access to knowledge about the laboratory mouse. Nucleic Acids Res, 42, 810-7. https://doi.org/10.1093/nar/gkt1225
  9. Burton K (1968). Determination of DNA concentration with diphenylamine. Methods Enzymol, 12, 163-6. https://doi.org/10.1016/0076-6879(67)12127-7
  10. Cheung WY, Gale MD (1990). The isolation of high molecular weight DNA from wheat, barley and rye for analysis by pulse-fieldgel electrophoresis. Plant Mol Biol, 14, 881-8. https://doi.org/10.1007/BF00016525
  11. Chikan NA, Shabir N, Shaff S, Mir MR, Patel TN (2012). N-nitrosodimethylamine in the Kashmiri diet and possible roles in the high incidence of gastrointestinal cancers. Asian Pac J Cancer Prev, 13, 1077-9. https://doi.org/10.7314/APJCP.2012.13.3.1077
  12. Chiou SH, Jiang BH, Yu YL et al (2013). Poly(ADP-ribose) polymerase 1 regulates nuclear reprogramming and promotes iPSC generation without c-Myc. J Exp Med, 210, 85-98. https://doi.org/10.1084/jem.20121044
  13. De Souza Setubal Destro MF, Bitu CC, Zecchin KG et al (2010). Overexpression of HOXB7 homeobox gene in oral cancer induces cellular proliferation and is associated with poor prognosis. Int J Oncol, 36, 141-9.
  14. Devi BJ, Sharan RN (2006). Progressive reduction in poly-ADPribosylation of histone proteins during Dalton's lymphoma induced ascites tumorigenesis in mice. Cancer Lett, 238, 135-1. https://doi.org/10.1016/j.canlet.2005.07.014
  15. Dona F, Chiodi I, Belgiovine C et al (2013). Poly (ADPribosylation) and neoplastic transformation: effect of PARP inhibitors. Curr Pharm Biotechnol, 14, 524-36. https://doi.org/10.2174/138920101405131111104642
  16. Fauzee NJ, Pan J, Wang YL (2010). PARP and PARG inhibitors--new therapeutic targets in cancer treatment. Pathol Oncol Res, 16, 469-8. https://doi.org/10.1007/s12253-010-9266-6
  17. Feng X, Koh DW (2013). Inhibition of poly(ADP-ribose) polymerase-1 or poly(ADP ribose) glycohydrolase individually, but not in combination, leads to improved chemotherapeutic efficacy in HeLa cells. Int J Oncol, 42, 749-6.
  18. Fontan-Lozano A, Suarez-Pereira I, Horrillo A et al (2010). Histone H1 poly[ADP]-ribosylation regulates the chromatin alterations required for learning consolidation. J Neurosci, 30, 13305-3. https://doi.org/10.1523/JNEUROSCI.3010-10.2010
  19. Harbeck N, Sotlar K, Wuerstlein R, Doisneau-Sixou S (2014). Molecular and protein markers for clinical decision making in breast cancer: today and tomorrow. Cancer Treat Rev, 40, 434-4. https://doi.org/10.1016/j.ctrv.2013.09.014
  20. Hensing TA, Salgia R (2013). Molecular biomarkers for future screening of lung cancer. J Surg Oncol, 108, 327-3. https://doi.org/10.1002/jso.23382
  21. Hong Z, Bi A, Chen D et al (2014). Activation of hedgehog signaling pathway in human non-small cell lung cancers. Pathol Oncol Res. 9.
  22. Huang YJ, Frazier ML, Zhang N, Liu Q, Wei C (2014). Reversephase protein array analysis to identify biomarker proteins in human pancreatic cancer. Dig Dis Sci, 59, 968-5. https://doi.org/10.1007/s10620-013-2938-9
  23. Humphries JM, Penno MA, Weiland F et al (2014). Identification and validation of novel candidate protein biomarkers for the detection of human gastriccancer. Biochim Biophys Acta, 1844, 1051-8. https://doi.org/10.1016/j.bbapap.2014.01.018
  24. Kalmar-Nagy K, Degrell P, Szabo A et al (2013). PARP inhibition attenuates acute kidney allograft rejection by suppressing cell death pathways and activating PI-3K-Akt cascade. PLoS One, 8, 81928-6. https://doi.org/10.1371/journal.pone.0081928
  25. Khan S, Jutzy JM, Valenzuela MM et al (2012). Plasma-derived exosomal survivin, a plausible biomarker for early detection of prostate cancer. PLoS One, 7, 46737-5. https://doi.org/10.1371/journal.pone.0046737
  26. Kma L, Sharan RN (2006). In vivo exposure of Swiss albino mice to chronic low dose of dimethylnitrosamine (DMN) lowers poly-ADP-ribosylation (PAR) of bone marrow cell and blood lymphocyte proteins. Mol Cell Biochem, 288, 143-9. https://doi.org/10.1007/s11010-006-9130-x
  27. Kma L, Sharan RN (2008). Chronic exposure of mice to aqueous extract of betel nuts (AEBN) inhibits poly-ADP-ribosylation (PAR) of total cellular proteins as well as histone H1 protein. Canadian J Pure and Applied Sci, 2, 123-8.
  28. Kondo T (2014). Inconvenient truth: cancer biomarker development by using proteomics. Biochim Biophys Acta, 1844, 861-5. https://doi.org/10.1016/j.bbapap.2013.07.009
  29. Long CA, Boulom V, Albadawi H et al (2013). Poly-ADP-ribose-polymerase inhibition ameliorates hind limb ischemia reperfusion injury in a murine model of type 2 diabetes. Ann Surg, 258, 1087-5. https://doi.org/10.1097/SLA.0b013e31828cced3
  30. Luna Coronell JA, Syed P, Sergelen K, Gyurjan I, Weinhausel A (2012). The current status of cancer biomarker research using tumour-associated antigens for minimal invasive and early cancer diagnostics. J Proteomics, 76, 102-15. https://doi.org/10.1016/j.jprot.2012.07.022
  31. Margison GP, O'Conner PJ (1979). In 'Chemical Carcinogens and DNA', Ed Grover PL. CRC Press, Baltimore.
  32. Marzinke MA, Choi CH, Chen L et al (2013). Proteomic analysis of temporally stimulated ovarian cancer cells for biomarker discovery. Mol Cell Proteomics, 12, 356-68. https://doi.org/10.1074/mcp.M112.019521
  33. Moto M, Umemura T, Okamura M et al (2006). Possible involvement of oxidative stress in dicyclanil-induced hepatocarcinogenesis in mice. Arch Toxicol, 80, 694-2. https://doi.org/10.1007/s00204-006-0086-0
  34. Osada T, Ryden AM, Masutani M (2013). Poly(ADPribosylation) regulates chromatin organization through histone H3 modification and DNA methylation of the first cell cycle of mouse embryos. Biochem Biophys Res Commun, 434, 15-1. https://doi.org/10.1016/j.bbrc.2013.03.074
  35. Ozaki Y, Matsui H, Asou H et al (2012). Poly-ADP ribosylation of Miki by tankyrase-1 promotes centrosome maturation. Mol Cell, 47, 694-06. https://doi.org/10.1016/j.molcel.2012.06.033
  36. Pariat T, Sharan RN (2002). Role of mouse spleen cell HMG proteins and their poly ADP-ribosylation in betel nut induced carcinogenesis. Indian J Biochem, 39, 130-5.
  37. Redon CE, Nakamura AJ, Zhang YW et al (2010). Histone gammaH2AX and poly(ADP-ribose) as clinical pharmacodynamic biomarkers. Clin Cancer Res, 16, 4532-2. https://doi.org/10.1158/1078-0432.CCR-10-0523
  38. Sala A, La Rocca G, Burgio G et al (2008). The nucleosomeremodeling ATPase ISWI is regulated by poly-ADPribosylation. PLoS Biol, 6, 252-8. https://doi.org/10.1371/journal.pbio.0060252
  39. Schwartz DC, Cantor CR (1984). Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell, 37, 67-5. https://doi.org/10.1016/0092-8674(84)90301-5
  40. Sharan RN, Devi BJ, Humtsoe JO, Saikia JR, Kma L (2005). Detection and quantification of poly-ADP-ribosylated proteins of spleen and liver tissues of mice in vivo by slot and Western blot immunoprobing using polyclonal antibody against mouse ADP-ribose polymer. Mol Cell Biochem, 278, 213-1. https://doi.org/10.1007/s11010-005-7588-6
  41. Sigari N, Mohsenpour B, Nikkhoo B et al (2014). Determination of the best prognostic value of serum tumor markers in patients with suspected lungcancer in an Iranian population. Clin Lab, 60, 23-7.
  42. Soond SM, Smith PG, Wahl L et al (2013). Novel WWP2 ubiquitin ligase isoforms as potential prognostic markers and molecular targets incancer. Biochim Biophys Acta, 1832, 2127-5. https://doi.org/10.1016/j.bbadis.2013.08.001
  43. Stephan F, Marsman G, Bakker LM et al (2014). Cooperation of factor VII-activating protease and serum DNase I in the release of nucleosomes from necrotic cells. Arthritis Rheumatol, 66, 686-3. https://doi.org/10.1002/art.38265
  44. Suradej B, Pata S, Kasinrerk W, Cressey R (2013). Glucosidase II exhibits similarity to the p53 tumor suppressor in regards to structure and behavior in response to stress signals: a potential novel cancer biomarker. Oncol Rep, 30, 2511-9.
  45. Tago Y, Yamano S, Wei M et al (2013). Novel medium-term carcinogenesis model for lung squamous cell carcinoma induced by N-nitroso-tris-chloroethylurea in mice. Cancer Sci, 104, 1560-6. https://doi.org/10.1111/cas.12289
  46. Taguchi A, Hanash SM (2013). Unleashing the power of proteomics to develop blood-based cancer markers. Clin Chem, 59, 119-6. https://doi.org/10.1373/clinchem.2012.184572
  47. Ueda K, Tatsuguchi A, Saichi N et al (2013). Plasma low-molecular-weight proteome profiling identified neuropeptide-Y as a prostate cancer biomarker polypeptide. J Proteome Res, 12, 4497-6. https://doi.org/10.1021/pr400547s
  48. van der Bilt AR, Terwisscha van Scheltinga AG, Timmer-Bosscha H et al (2012). Measurement of tumor VEGF-A levels with 89Zr-bevacizumab PET as an early biomarker for the antiangiogenic effect of everolimus treatment in an ovarian cancer xenograft model. Clin Cancer Res, 18, 6306-4. https://doi.org/10.1158/1078-0432.CCR-12-0406
  49. Villani P, Eleuteri P, Grollino MG et al (2010). Sperm DNA fragmentation induced by DNAse I and hydrogen peroxide: an in vitro comparative study among different mammalian species. Reproduction, 140, 445-2. https://doi.org/10.1530/REP-10-0176
  50. Wang X, Zhang A, Sun H (2013). Power of metabolomics in diagnosis and biomarker discovery of hepatocellular carcinoma. Hepatology, 57, 2072-7. https://doi.org/10.1002/hep.26130
  51. West MHP, Bonner WM (1980). Histone 2A, a heteromorphous family of eight protein species. Biochemistry, 19, 3238-5. https://doi.org/10.1021/bi00555a022
  52. Yang Y, Toy W, Choong LY et al (2012). Discovery of SLC3A2 cell membrane protein as a potential gastric cancer biomarker: implications inmolecular imaging. J Proteome Res, 11, 5736-47.
  53. Yuan K, Sun Y, Zhou T, McDonald J, Chen Y (2013). PARP-1 regulates resistance of pancreatic cancer to TRAIL therapy. Clin Cancer Res, 19, 4750-9. https://doi.org/10.1158/1078-0432.CCR-13-0516

Cited by

  1. Vicenin-2 acts as a radiosensitizer of the non-small cell lung cancer by lowering Akt expression pp.09516433, 2018, https://doi.org/10.1002/biof.1472
  2. Vicenin-2: a potential radiosensitizer of non-small cell lung cancer cells vol.45, pp.5, 2018, https://doi.org/10.1007/s11033-018-4275-8