Research Article
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More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act as a Prognostic Marker for High-Risk Neuroblastoma Patients

Year 2023, Volume: 7 Issue: 1, 196 - 213, 31.01.2023
https://doi.org/10.30621/jbachs.1071115

Abstract

Purpose: Determination of proteomic differences plays an important role in biomarker investigations. Due to its heterogenic molecular background, identification of certain biomarkers is still a demand both for diagnosis and for prognosis of neuroblastoma. In this study, it is aimed to identify some marker proteins/mechanisms that may play role in neuroblastoma prognosis.
Methods: A proteomic approach was performed for different risk groups of the disease by using matrix-assisted laser desorption ionization–time of flight (MALDI-TOF/TOF) approach. Mononuclear cell pools from blood samples of patients for risk groups were constructed and protein expression changes for different groups were identified. Real-time PCR analysis were performed for N-MYC, 11q, 1p and 17q status of these patients and risk groups were determined from tumor samples.
Results: Manganese-superoxide dismutase (SOD2) protein was significantly increased in high-risk group of neuroblastoma patients.
Conclusion: SOD2 may play an important role in neuroblastoma progression and be a candidate prognostic peripheral blood marker for neuroblastoma patients.

Supporting Institution

This study has been supported by a research grant of Turkish Pediatric Oncology Group (TPOG)

Project Number

2015

Thanks

This study has been supported by a research grant of Turkish Pediatric Oncology Group (TPOG) (2015) and performed on behalf of TPOG. The study has been presented at 60th Annual Meeting of the Japanese Society of Pediatric Hematology Society as a poster. 2D Gel Electrophoresis and MALDI TOF/TOF analysis were performed in Prof. Dr. Talat YALCIN’s laboratory in Izmir Institute of Technology, Department of Chemistry.

References

  • 1. Maris JM, Matthay KK. Molecular biology of neuroblastoma. J Clin Oncol 1999; 17: 22642279.
  • 2. Olgun N, Kansoy S, Aksoylar S, Cetingul N, Vergin C, Oniz H, et al. Experience of the Izmir Pediatric Oncology Group on Neuroblastoma: IPOG-NBL-92 Protocol. Pediatr Hematol Oncol. 2003; 20(3):211-18. 3. Li C, Wu Z, Liu M, Pazgier M, Lu W. Chemically synthesized human surviving does not inhibit caspase-3. Protein Sci. 2008; 17(9):1624-29.
  • 4. Berthold F. Neuroblastoma-90 (NB-90) protocol. German Pediatric Oncology Group (GPOG-NBL) 1990.
  • 5. Matthey KK, Perez C, Seeger RC, Brodeur GM, Shimada H, Atkinson JB, et al. Successful treatment of stage III neuroblastoma based on prospective biologic staging: A Children’s Cancer Group study. J. Clin Oncol. 1998; 16:1256.
  • 6. Krona C, Ejeskär K, Abel F, Kogner P, Bjelke J, Björk E, et al. Screening for gene mutations in a 500 kb neuroblastoma tumor suppressor candidate region in chromosome 1p; mutation and stage-specific expression in UBE4B/UFD2. Oncogene. 2003:2343-51.
  • 7. De Preter K, Vandesompele J, Menten B, Carr P, Fiegler H, Edsjö A, et al. Positional and functional mapping of a neuroblastoma differentiation gene on chromosome 11. BMC Genomics. 2005; 6:97.
  • 8. Wang Q, Diskin S, Rappaport E, Attiyeh E, Mosse Y, Shue D, et al. Integrative genomics identifies distinct molecular classes of neuroblastoma and shows that multiple genes are targeted by regional alterations in DNA copy number. Cancer Res. 2006; 66(12):6050-6062.
  • 9. Souzaki R, Tajiri T, Higashi M, Kinoshita Y, Tanaka S, Kohashi K et al. Clinical implications of a slight increase in the gene dosage of MYCN in neuroblastoma determined using quantitative PCR. Pediart Surg Int. 2008; 24: 1095-1100.
  • 10. Spitz R, Hero B, Ernestus K, Berthold F. FISH analyses for alterations in chromosomes 1,2,3, and 11 define high-risk groups in neuroblastoma, Med Pediatr Oncol. 2003; 41:30-35.
  • 11. Shimada H, Chatten J, Newton WA Jr, Sachs N, Hamoudi AB, Chiba T, et al. Histopathologic prognostic factors in neuroblastic tumors: definition of subtypes of ganglioneuroblastoma and an age-linked classification of neuroblastomas. J Natl Cancer Inst. 1984; 73(2):405-416.
  • 12. Brodeur GM, Pritchard J, Berthold F, Carlsen NL, Castel V, Castelberry RP et al. Revisions of the international criteria for neuroblastoma diagnosis, staging and response to treatment. J Clin Oncol. 1993; 11(8):1466-1477.
  • 13. Brodeur GM, Seeger RC, Barrett A, Castleberry RP, D'Angio G, De Bernardi B, et al. International criteria for diagnosis, staging, and response to treatment in patients with neuroblastoma. J. Clin Oncol.1988; 6(12):1874-1881.
  • 14. Monclair T, Brodeur GM, Ambros PF, Brisse HJ, Cecchetto G, Holmes K et al. The International Neuroblastoma Risk Group (INRG) staging system: an INRG Task Force report. J Clin Oncol. 2009; 27(2):298-303.
  • 15. Saini RK, Attarha S, da Silva Santos C, Kolakowska J, Funa K, Souchelnytskyi S. Proteomics of dedifferentiation of SK-N-BE2 neuroblastoma cells. BBRC. 2014; 454:202-209.
  • 16. Jung EJ, Park HC, Chung KH, Kim CW. Proteomic analysis of SP600125-controlled TrkA-dependent targets in SK-N-MC neuroblastoma cells: Inhibition of TrkA activity by SP600125.Proteomics. 2014; 14:202-215. 17. Kim PY, Tan O, Diakiw SM, Carter D, Sekerye EO, Wasinger VC, et al. Identification of plasma Complement C3 as a potential biomarker for neuroblastoma using a quantitative proteomic approach. Journal of Proteomics. 2014; 96:1-12.
  • 18. DeNardo BD, Holloway MP, Ji Q, Nguyen KT, Cheng Y, Valentine MB, et al. Quantitative phosphoproteomic analysis identifies activation of the ret and igf-1r/ir signaling pathways in neuroblastoma. Plos One. 2013; 8(12): e82513.
  • 19. Fuchs D, Vafeiadou K, Hall WL, Daniel H, Williams CM, Schroot JH, Wenzel U. Proteomic biomarkers of peripheral blood mononuclear cells obtained from postmenopausal women undergoing an intervention with soy isoflavones. Am J Clin Nutr. 2007; 86:1369-75.
  • 20. Mass Spectrometry Compatible Silver Staining. Center for Biotechnology, Turku Bioscience, University of Turku, Findland. 2009
  • 21. O'Connell KL, Stults JT. Identification of mouse liver proteins on two-dimensional electrophoresis gels by matrix-assisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis. 1997; 18(3-4):349-59.
  • 22. Gharahdaghi F, Weinberg CR, Meagher DA, Imai BS, Mische SM. Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis. 1999: 20(3):601-605.
  • 23. Demir AB, Aktas S, Altun Z, Ercetin P, Aktas TC, Olgun N. Questioning How to Define the "Ultra-High-Risk" Subgroup of Neuroblastoma Patients. Folia Biol (Praha). 2021; 67(1):1-9.
  • 24. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov. 2009; 8:579–591.
  • 25. Andersen JK. Oxidative stress in neurodegeneration: cause or consequence? Nat Med. 2004; 10(Suppl): S18–S25.
  • 26. Haigis MC, Yankner BA. The aging stress response. Mol Cell. 2010; 40:333–344.
  • 27. Bica CG. de Moura da Silva LL, Toscani NV, da Cruz IB, Sá G, Graudenz MS, Zettler CG. MnSOD gene polymorphism association with steroid-dependent cancer. Pathol. Oncol. Res. 2009; 15:19-24.
  • 28. Janssen AM, Bosman CB, Kruidenier L, Griffioen G, Lamers CB, van Krieken JH, et al. Superoxide dismutases in the human colorectal cancer sequence. J. Cancer Res. Clin. Oncol. 1999; 125:327-335.
  • 29. Nozoe T. Honda M, Inutsuka S, Yasuda M, Korenaga D. Significance of immunohistochemical expression of manganese superoxide dismutase as a marker of malignant potential in colorectal carcinoma. Oncol Rep.2003; 10:39-43.
  • 30. Azzolin VF, Cadoná FC, Machado AK, Berto MD, Barbisan F, Dornelles EB, et al. Superoxide-hydrogen peroxide imbalance interferes with colorectal cancer cells viability, proliferation and oxaliplatin response. Toxicology in Vitro. 2016; 32:8-15.
  • 31. Abdel-Aziz A.F, El-Naggar M.M. Superoxide dismutase activities in serum and white blood cells of patients with some malignancies. Cancer Letters.1997;113:61-64.
  • 32. Stachowicz-Stencel T, Synakiewicz A, Owczarzak A, Aleksandrowicz-Wrona E, Sliwinska A, Lysiak-Szydlowska W, Balcerska A. The antioxidant status and response to therapy in children with soft tissue sarcomas and neuroblastoma. Pediatr. Blood Cancer. 2011; 57:561-568.
  • 33. Steinkühler C, Mavelli I, Melino G, Piacentini M, Rossi L, Weser U, Rotilio G. Antioxygenic enzyme activitites in differentiating human neuroblastoma cells. Annals. New York Academy of Sciences.1988; 551:137-140.
  • 34. Hitchler MJ, Oberley LW, Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic. Biol. Med. 2008; 45:1573–1580.
  • 35. Cyr AR, Hitchler MJ, Domann FE. Regulation of SOD2 in cancer by histone modifications and CpG methylation: Closing the loop between redox biology and epigenetics. Antioxid. Redox Signal. 2013; 18:1946–1955.
  • 36. Zhi Y, Lu H, Duan Y, Sun W, Guan G, Dong Q, Yang C. Involvement of the nuclear factor-κB signaling pathway in the regulation of CXC chemokine receptor-4 expression in neuroblastoma cells induced by tumor necrosis factor-α. International Journal of Molecular Medicine. 201; 35: 349-357.
Year 2023, Volume: 7 Issue: 1, 196 - 213, 31.01.2023
https://doi.org/10.30621/jbachs.1071115

Abstract

Project Number

2015

References

  • 1. Maris JM, Matthay KK. Molecular biology of neuroblastoma. J Clin Oncol 1999; 17: 22642279.
  • 2. Olgun N, Kansoy S, Aksoylar S, Cetingul N, Vergin C, Oniz H, et al. Experience of the Izmir Pediatric Oncology Group on Neuroblastoma: IPOG-NBL-92 Protocol. Pediatr Hematol Oncol. 2003; 20(3):211-18. 3. Li C, Wu Z, Liu M, Pazgier M, Lu W. Chemically synthesized human surviving does not inhibit caspase-3. Protein Sci. 2008; 17(9):1624-29.
  • 4. Berthold F. Neuroblastoma-90 (NB-90) protocol. German Pediatric Oncology Group (GPOG-NBL) 1990.
  • 5. Matthey KK, Perez C, Seeger RC, Brodeur GM, Shimada H, Atkinson JB, et al. Successful treatment of stage III neuroblastoma based on prospective biologic staging: A Children’s Cancer Group study. J. Clin Oncol. 1998; 16:1256.
  • 6. Krona C, Ejeskär K, Abel F, Kogner P, Bjelke J, Björk E, et al. Screening for gene mutations in a 500 kb neuroblastoma tumor suppressor candidate region in chromosome 1p; mutation and stage-specific expression in UBE4B/UFD2. Oncogene. 2003:2343-51.
  • 7. De Preter K, Vandesompele J, Menten B, Carr P, Fiegler H, Edsjö A, et al. Positional and functional mapping of a neuroblastoma differentiation gene on chromosome 11. BMC Genomics. 2005; 6:97.
  • 8. Wang Q, Diskin S, Rappaport E, Attiyeh E, Mosse Y, Shue D, et al. Integrative genomics identifies distinct molecular classes of neuroblastoma and shows that multiple genes are targeted by regional alterations in DNA copy number. Cancer Res. 2006; 66(12):6050-6062.
  • 9. Souzaki R, Tajiri T, Higashi M, Kinoshita Y, Tanaka S, Kohashi K et al. Clinical implications of a slight increase in the gene dosage of MYCN in neuroblastoma determined using quantitative PCR. Pediart Surg Int. 2008; 24: 1095-1100.
  • 10. Spitz R, Hero B, Ernestus K, Berthold F. FISH analyses for alterations in chromosomes 1,2,3, and 11 define high-risk groups in neuroblastoma, Med Pediatr Oncol. 2003; 41:30-35.
  • 11. Shimada H, Chatten J, Newton WA Jr, Sachs N, Hamoudi AB, Chiba T, et al. Histopathologic prognostic factors in neuroblastic tumors: definition of subtypes of ganglioneuroblastoma and an age-linked classification of neuroblastomas. J Natl Cancer Inst. 1984; 73(2):405-416.
  • 12. Brodeur GM, Pritchard J, Berthold F, Carlsen NL, Castel V, Castelberry RP et al. Revisions of the international criteria for neuroblastoma diagnosis, staging and response to treatment. J Clin Oncol. 1993; 11(8):1466-1477.
  • 13. Brodeur GM, Seeger RC, Barrett A, Castleberry RP, D'Angio G, De Bernardi B, et al. International criteria for diagnosis, staging, and response to treatment in patients with neuroblastoma. J. Clin Oncol.1988; 6(12):1874-1881.
  • 14. Monclair T, Brodeur GM, Ambros PF, Brisse HJ, Cecchetto G, Holmes K et al. The International Neuroblastoma Risk Group (INRG) staging system: an INRG Task Force report. J Clin Oncol. 2009; 27(2):298-303.
  • 15. Saini RK, Attarha S, da Silva Santos C, Kolakowska J, Funa K, Souchelnytskyi S. Proteomics of dedifferentiation of SK-N-BE2 neuroblastoma cells. BBRC. 2014; 454:202-209.
  • 16. Jung EJ, Park HC, Chung KH, Kim CW. Proteomic analysis of SP600125-controlled TrkA-dependent targets in SK-N-MC neuroblastoma cells: Inhibition of TrkA activity by SP600125.Proteomics. 2014; 14:202-215. 17. Kim PY, Tan O, Diakiw SM, Carter D, Sekerye EO, Wasinger VC, et al. Identification of plasma Complement C3 as a potential biomarker for neuroblastoma using a quantitative proteomic approach. Journal of Proteomics. 2014; 96:1-12.
  • 18. DeNardo BD, Holloway MP, Ji Q, Nguyen KT, Cheng Y, Valentine MB, et al. Quantitative phosphoproteomic analysis identifies activation of the ret and igf-1r/ir signaling pathways in neuroblastoma. Plos One. 2013; 8(12): e82513.
  • 19. Fuchs D, Vafeiadou K, Hall WL, Daniel H, Williams CM, Schroot JH, Wenzel U. Proteomic biomarkers of peripheral blood mononuclear cells obtained from postmenopausal women undergoing an intervention with soy isoflavones. Am J Clin Nutr. 2007; 86:1369-75.
  • 20. Mass Spectrometry Compatible Silver Staining. Center for Biotechnology, Turku Bioscience, University of Turku, Findland. 2009
  • 21. O'Connell KL, Stults JT. Identification of mouse liver proteins on two-dimensional electrophoresis gels by matrix-assisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis. 1997; 18(3-4):349-59.
  • 22. Gharahdaghi F, Weinberg CR, Meagher DA, Imai BS, Mische SM. Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis. 1999: 20(3):601-605.
  • 23. Demir AB, Aktas S, Altun Z, Ercetin P, Aktas TC, Olgun N. Questioning How to Define the "Ultra-High-Risk" Subgroup of Neuroblastoma Patients. Folia Biol (Praha). 2021; 67(1):1-9.
  • 24. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov. 2009; 8:579–591.
  • 25. Andersen JK. Oxidative stress in neurodegeneration: cause or consequence? Nat Med. 2004; 10(Suppl): S18–S25.
  • 26. Haigis MC, Yankner BA. The aging stress response. Mol Cell. 2010; 40:333–344.
  • 27. Bica CG. de Moura da Silva LL, Toscani NV, da Cruz IB, Sá G, Graudenz MS, Zettler CG. MnSOD gene polymorphism association with steroid-dependent cancer. Pathol. Oncol. Res. 2009; 15:19-24.
  • 28. Janssen AM, Bosman CB, Kruidenier L, Griffioen G, Lamers CB, van Krieken JH, et al. Superoxide dismutases in the human colorectal cancer sequence. J. Cancer Res. Clin. Oncol. 1999; 125:327-335.
  • 29. Nozoe T. Honda M, Inutsuka S, Yasuda M, Korenaga D. Significance of immunohistochemical expression of manganese superoxide dismutase as a marker of malignant potential in colorectal carcinoma. Oncol Rep.2003; 10:39-43.
  • 30. Azzolin VF, Cadoná FC, Machado AK, Berto MD, Barbisan F, Dornelles EB, et al. Superoxide-hydrogen peroxide imbalance interferes with colorectal cancer cells viability, proliferation and oxaliplatin response. Toxicology in Vitro. 2016; 32:8-15.
  • 31. Abdel-Aziz A.F, El-Naggar M.M. Superoxide dismutase activities in serum and white blood cells of patients with some malignancies. Cancer Letters.1997;113:61-64.
  • 32. Stachowicz-Stencel T, Synakiewicz A, Owczarzak A, Aleksandrowicz-Wrona E, Sliwinska A, Lysiak-Szydlowska W, Balcerska A. The antioxidant status and response to therapy in children with soft tissue sarcomas and neuroblastoma. Pediatr. Blood Cancer. 2011; 57:561-568.
  • 33. Steinkühler C, Mavelli I, Melino G, Piacentini M, Rossi L, Weser U, Rotilio G. Antioxygenic enzyme activitites in differentiating human neuroblastoma cells. Annals. New York Academy of Sciences.1988; 551:137-140.
  • 34. Hitchler MJ, Oberley LW, Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic. Biol. Med. 2008; 45:1573–1580.
  • 35. Cyr AR, Hitchler MJ, Domann FE. Regulation of SOD2 in cancer by histone modifications and CpG methylation: Closing the loop between redox biology and epigenetics. Antioxid. Redox Signal. 2013; 18:1946–1955.
  • 36. Zhi Y, Lu H, Duan Y, Sun W, Guan G, Dong Q, Yang C. Involvement of the nuclear factor-κB signaling pathway in the regulation of CXC chemokine receptor-4 expression in neuroblastoma cells induced by tumor necrosis factor-α. International Journal of Molecular Medicine. 201; 35: 349-357.
There are 34 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Research Article
Authors

Ayse Banu Demir This is me 0000-0003-4616-8151

Zekiye Altun 0000-0002-1558-4534

Safiye Aktaş 0000-0002-7658-5565

Nur Olgun 0000-0001-9591-0207

Project Number 2015
Publication Date January 31, 2023
Submission Date February 10, 2022
Published in Issue Year 2023 Volume: 7 Issue: 1

Cite

APA Demir, A. B., Altun, Z., Aktaş, S., Olgun, N. (2023). More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act as a Prognostic Marker for High-Risk Neuroblastoma Patients. Journal of Basic and Clinical Health Sciences, 7(1), 196-213. https://doi.org/10.30621/jbachs.1071115
AMA Demir AB, Altun Z, Aktaş S, Olgun N. More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act as a Prognostic Marker for High-Risk Neuroblastoma Patients. JBACHS. January 2023;7(1):196-213. doi:10.30621/jbachs.1071115
Chicago Demir, Ayse Banu, Zekiye Altun, Safiye Aktaş, and Nur Olgun. “More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act As a Prognostic Marker for High-Risk Neuroblastoma Patients”. Journal of Basic and Clinical Health Sciences 7, no. 1 (January 2023): 196-213. https://doi.org/10.30621/jbachs.1071115.
EndNote Demir AB, Altun Z, Aktaş S, Olgun N (January 1, 2023) More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act as a Prognostic Marker for High-Risk Neuroblastoma Patients. Journal of Basic and Clinical Health Sciences 7 1 196–213.
IEEE A. B. Demir, Z. Altun, S. Aktaş, and N. Olgun, “More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act as a Prognostic Marker for High-Risk Neuroblastoma Patients”, JBACHS, vol. 7, no. 1, pp. 196–213, 2023, doi: 10.30621/jbachs.1071115.
ISNAD Demir, Ayse Banu et al. “More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act As a Prognostic Marker for High-Risk Neuroblastoma Patients”. Journal of Basic and Clinical Health Sciences 7/1 (January 2023), 196-213. https://doi.org/10.30621/jbachs.1071115.
JAMA Demir AB, Altun Z, Aktaş S, Olgun N. More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act as a Prognostic Marker for High-Risk Neuroblastoma Patients. JBACHS. 2023;7:196–213.
MLA Demir, Ayse Banu et al. “More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act As a Prognostic Marker for High-Risk Neuroblastoma Patients”. Journal of Basic and Clinical Health Sciences, vol. 7, no. 1, 2023, pp. 196-13, doi:10.30621/jbachs.1071115.
Vancouver Demir AB, Altun Z, Aktaş S, Olgun N. More Abundant Superoxide Dismutase2 Protein Levels in Blood May Act as a Prognostic Marker for High-Risk Neuroblastoma Patients. JBACHS. 2023;7(1):196-213.