Skip to main content
Log in

Activity of lysosomal exoglycosidases in human gliomas

  • Laboratory Investigation
  • Published:
Journal of Neuro-Oncology Aims and scope Submit manuscript

Abstract

There is a lot of data suggesting that modifications of cell glycoconjugates may be important in progression of cancer. In the present work we studied activities of lysosomal exoglycosidases: β-hexosaminidase and its isoenzymes A and B, β-galactosidase and α-mannosidase, in human gliomas. Enzyme activity was determined spectrophotometrically based on the release of p-nitrophenol from p-nitrophenyl-derivative of appropriate sugars. The activities of the exoglycosidases tested were significantly higher in malignant glial tumors than in control tissue (normal brain tissue) and non-glial tumors. The highest activities of exoglycosidases were observed in high-grade gliomas, and a positive correlation of enzyme activities and degree of malignancy was noted. Our results suggest that lysosomal exoglycosidases may participate in the progression and dynamical development of glial tumors.

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.

Similar content being viewed by others

References

  1. Xiao-Hong Z, Brakebusch C, Matthies H, Oohashi T, Hirsch␣E, Moser M, Krug M, Seidenbecher CI, Boeckers TM, Rauch U, Buettner R (2001) Neurocan is dispesable for brain development. Mol Cell Biol 7:5970–5978

    Google Scholar 

  2. Margolis RK, Rauch U, Maurel P, Margolis RU (1996) Neurocan and phosphacan: two major nervous tissue – specific chondroitin sulfate proteoglycans. Perspect Dev Neurobiol 3:273–290

    PubMed  CAS  Google Scholar 

  3. Landlot RM, Vaurhan L, Winterhalter KH, Zimmermann DR (1995) Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth. Development 121:2303–2312

    PubMed  Google Scholar 

  4. Cavalcante LA, Garcia-Abreu J, Mendes FA, Mouro Neto V, Silva LCF, Onofre G, Weissmüller G, Carvahlo SL (2003) Sulfated proteoglycans as modulators of neuronal migration and axonal decussation in the developing midbrain. Braz J␣Med Biol Res 36:993–1002

    Article  PubMed  CAS  Google Scholar 

  5. Bandtlow CE, Zimmermann DR (2002) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80(4):1267–1282

    Google Scholar 

  6. Agranoff BW (1989) Lipids. In: Siegel G, Agranoff BW, Albers RW, Molinoff P (eds) Basic neurochemisty, 4th edn. Raven Press, New York

    Google Scholar 

  7. Rhodes KE, Fawcett JW (2004) Chondroitin sulphate proteoglycans: preventing plasticy or protecting the CNS? J␣Anat 204:33–48

    Article  PubMed  CAS  Google Scholar 

  8. Properzi F, Fawcett JW (2002) Proteoglycans and brain repair. News Physiol Sci 19:33–38

    Article  Google Scholar 

  9. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, New York

    Google Scholar 

  10. Prokopowicz J, Dąbrowska M, Kemona H (1990) Proteases and antiproteases in cancer. Nowotwory 2:88–93

    Google Scholar 

  11. Miyagi T, Wada T, Yamaguchi K, Hata K (2004) Sialidase and malignancy: a minireview. Glycoconj J 20:189–198

    Article  PubMed  CAS  Google Scholar 

  12. Levin VA, Gutin PH, Leibel S (1993) Neoplasms of the central nervous system. In: De Vita VT, Hellman S, Rosenberg SA, JB Cancer Principle and practice of oncology. Lipincott Company, 4th edn, pp 1679–1737

  13. Kheihues P, Burger PC, Scheithauer BW (1993) The new␣classification WHO of brain tumors. Brain Pathol 3:255–268

    PubMed  Google Scholar 

  14. Kiwit JC, Floeth FW, Bock WJ (1996) Survival in malignant glioma: analysis of prognostic factors with special regard to cytoreductive surgery. Neurochir 57(2):76–88

    CAS  Google Scholar 

  15. Levin VA, Silver P, Hannigan J, Wara WM, Gutin PW, Davis RL, Wilson CD (1990) Superiority of post-radiotherapy adjuvant chemotheraphy with CCNU, procarbasine, and vincristine (PCV) over BCNU for anaplastic gliomas NCOG 6G61 final report. Int J Radiat Oncol Biol Phys 18:321–324

    PubMed  CAS  Google Scholar 

  16. Daumas-Duport C (1992) Histological grading of gliomas. Curr Opin Neurol Neurosurg 5:924–931

    PubMed  CAS  Google Scholar 

  17. Plucinsky MC, Prorok JJ, Alhadeff JA (1986) Variant serum beta-hexosaminidase as a biochemical marker of malignancy. Cancer 1 58(7):1484–1487

    Article  CAS  Google Scholar 

  18. Kunishio K, Okada M, Matsumoto Y, Nagao S (2003) Matrix metalloproteinase-2 and -9 expression in astrocytic tumors. Brain Tumor Pathol 20:39–45

    Article  PubMed  Google Scholar 

  19. Borzym-Kluczyk M, Darewicz B, Knas M, Szajda SD, Olszewska E, Zwierz K (2005) The activity of N-acetyl-beta-Glucosaminidase and its isoenzymes in the renal tissue, serum and urine of patients with renal cancer. Wspolczesna Onkol 9:287–290

    Google Scholar 

  20. Kakugawa Y, Wada T, Yamaguchi K, Yamanami H, Ouchi␣K, Sato I, Miyagi T (2002) Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon and its involvement in apoptosis suppression. Proc Natl Acad Sci USA 99:10,718–10,723

    Article  CAS  Google Scholar 

  21. Ochwat D, Hoja-Lukowicz D, Litynska A (2004) N-glycoproteins bearing β1-6 branched oligosaccharides from the A375 human melanoma cell iline analysed by tandem mass spectrometry. Melanoma Res 14:479–485

    Article  PubMed  CAS  Google Scholar 

  22. Kim YS, Isaacs R (1975) Glycoprotein metabolism in inflammatory and neoplastic diseases of the human colon. Cancer Res 35(8):2092–2097

    PubMed  CAS  Google Scholar 

  23. Vlodavsky I, Friedmann Y (2001) Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J Clin Invest 108(3): 341–347

    Article  PubMed  CAS  Google Scholar 

  24. Yates AJ, Comas T, Scheithauer BW, Burger PC, Pearl DK (1999) Glycolipids markers of astrocytomas and oligodendrogliomas. J Neuropathol Exp Neurol 58:1250–1262

    PubMed  CAS  Google Scholar 

  25. Buck MR, Karustis DG, Day NA, Honn KV, Sloane BF (1992) Degradation of extracellular – matrix proteins by human cathepsin B from normal and tumour tissues. Biochem J 15(282):273–278

    Google Scholar 

  26. Campanella R (1992) Membrane lipids modifications in human gliomas of different degree of malignancy. J Neurosurg Sci 36:11–25

    PubMed  CAS  Google Scholar 

  27. Wagener R, Rohn G, Schroder R, Kobbe B, Ernestus RI (1999) Ganglioside profile in human gliomas: quantification by microbore high performance liquid chromatography and correlation to histopathology and grading. Acta Neurochir (Wien) 141:1339–1345

    Article  CAS  Google Scholar 

  28. Chang F, Li R, Noon K, Gage D, Ladisch S (1997) Human medulloblastoma gangliosides. Glycobiology 7:523–530

    PubMed  CAS  Google Scholar 

  29. Hynes RD (1976) Cell surface proteins and malignant transformation. Biochim Biophys Acta 458:73–107

    PubMed  CAS  Google Scholar 

  30. Noll EN, Lin J, Nakatsuji Y, Miller RH, Black PM (2001) GM3 as a novel growth regulator for human gliomas. Exp Neurol 168:300–309

    Article  PubMed  CAS  Google Scholar 

  31. Nygren C, von Holst H, Mansson JE, Fredman P (1994) Increased activity of lysosomal glycohydrolases in glioma tissues and surrounding areas from human brain. Acta Neurochir 139(2):146–150

    Google Scholar 

  32. Zwierz K, Zalewska A, Zoch-Zwierz W (1999) Isoenzymes of N-acetyl-β-hexosaminidase. Acta Biochim Polon 3:739–757

    Google Scholar 

  33. Bernacki RJ, Niedbala MJ, Korytnyk W (1985) Glycosidases in cancer and invasion. Cancer Matastasis Rev 4:81–101

    Article  CAS  Google Scholar 

  34. Pochec E, Litynska A, Bubka M, Amoresano A, Casbarra A (2006) Characterization of the oligosaccharide component of α3β1 integrin from human bladder carcinoma cell line T24 and its role in adhesion and migration. Eur J Cell Biol 85:47–57

    Article  PubMed  CAS  Google Scholar 

  35. Naka R, Kamoda S, Isuzuka A, Kinoshita M, Kakehi K (2006) Analysis of total N-glycans in cell membrane fractions of cancer cells using a combination of serotonin affinity chromatography and normal phase chromatography. J Proteome Res 5:88–97

    Article  PubMed  CAS  Google Scholar 

  36. Rebbaa A, Chou PM, Vucic I, Mirkin BL, Tomita T, Bremer␣EG (1999) Expression of bisecting GlcNAc in pediatric brain tumors and its association with tumor cell response to vinblastine. Clin Cancer Res 5:3661–3668

    PubMed  CAS  Google Scholar 

  37. Viapiano MS, Bi WL, Piepmeier J, Hockfield S, Matthews RT (2005) Novel tumor-specific isoforms of BEHAB/brevican identified in human malignant gliomas. Cancer Res 65: 6726–6733

    Article  PubMed  CAS  Google Scholar 

  38. Suzuki O, Nozawa Y, Abe M (2006) The regulatory roles of cell surface sialylation and N-glycans in human B cell lymphoma cell adhesion to galectin-1. Int J Oncol 28:155–160

    PubMed  CAS  Google Scholar 

  39. Sato T, Takahashi M, Kewado T, Takayama E, Furukawa K (2005) Effect of staurosporine on N-glycosylation and cell adhesion to fibronectin of SW480 human colorectal adenocarcinoma cells. Eur J Pharm Sci 25:221–227

    PubMed  CAS  Google Scholar 

  40. Krishnan V, Bane SM, Kawle PD, Naresh KN, Kalraiya RD (2005) Altered melanoma cell surface glycosylation mediates organ specific adhesion and metastasis via lectin receptors on the lung vascular endothelium. Clin Exp Metastasis 22:11–24

    Article  PubMed  CAS  Google Scholar 

  41. Ciolczyk-Wierzbicka D, Amoresano A, Casbarra A, Hoja-lukowicz D, Litynska A, Laidler P (2004) The structure of the oligosaccharides of N-cadherin from human melanoma cell lines. Glycoconj J 20:483–492

    Article  PubMed  CAS  Google Scholar 

  42. Glick MC (1976) Glycoproteins on the surface of neuroblastoma cells. J Natl Cancer Inst 57:653–658

    PubMed  CAS  Google Scholar 

  43. Yamamoto H, Oveido A, Sweeley C, Saito T, Moskal JR (2001) Alpha2,6-sialylation of cell-surface N-glycans inhibits glioma formation in vivo. Cancer Res 61:6822–6829

    PubMed  CAS  Google Scholar 

  44. Spillmann D, Finne J (1987) Poly-N-acetyllactosamine glycans of cellular glycoproteins: predominance of linear chains in mouse neuroblastoma and rat pheochromocytoma cell lines. J Neurochem 49:874–883

    Article  PubMed  CAS  Google Scholar 

  45. Dawson G, Moskal JR, Dawson SA (2004) Transfection of 2,6 and 2,3-sialyltransferase genes into human glioma cell line U-373MG affects glycoconjugate expression and enhances cell death. J Neurochem 89:1436–1444

    Article  PubMed  CAS  Google Scholar 

  46. Chatterjee SK, Chowdhury K, Bhattarya M, Barlow JL (1982) β-Hexosaminidase activities and isoenzymes in normal human ovary and ovarian carcinoma. Cancer 49:128–135

    Article  PubMed  CAS  Google Scholar 

  47. Brattain MG, Kimball PM, Pretlow TG (1977) β-Hexosaminidase isoenzymes in human colonic carcinoma. Cancer Res 37:731–735

    PubMed  CAS  Google Scholar 

  48. Bosmann HB, Hall TC (1974) Enzyme activity in invasive tumors of human breast and colon. Proc Natl Acad Sci USA 71:1833–1837

    Article  PubMed  CAS  Google Scholar 

  49. Bhuvarahumurthy V, Govindsamy S (1996) Purification and characterization of hexosaminidase from human uterine cervical carcinoma. Gynecol Oncol 60:188–196

    Article  PubMed  Google Scholar 

  50. Luqmani Y, Temmim L, Memon A, Abdulaziz L, Parkar A, Ali M, Motowy M, Fayaz S (1999) Measurement of serum N-acetyl-β-glucosaminidase activity in patients with breast cancer. Acta Oncol 38:649–653

    Article  PubMed  CAS  Google Scholar 

  51. Zwierz K, Gindzienski A, Głowacka D, Porowski T (1951) The degradation of glycoconjugates in the human gastric mucous membrane. Acta Med Acad Sci Hung 38(2):145–152

    Google Scholar 

  52. Lowry OH, Rosebrough NJ, Farr AL (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  53. Florkin M, Stotz EH (1973) Enzyme nomenclature. In: Comprehensive biochemistry, vol 13. Elsevier, Amsterdam, London, New York

  54. Allen N, Clendenon NR, Abe H (1977) Acid hydrolase and cytochrome oxidase activities in nitrosourea-induced tumors of nervous system. Acta Neuropathol 39:13–23

    Article  PubMed  CAS  Google Scholar 

  55. Avrova NF, Tyurin VA, Tyurina YY, Gamaley IA, Schepetkin IA (2002) Different metabolic effects of ganglioside GM1 in brain synaptosomes and phagocytic cells. Neurochem Res 27:751–759

    Article  PubMed  CAS  Google Scholar 

  56. Bansal R, Winkler S, Bheddah S (1999) Negative regulation of oligodendrocyte differentiation by galactosphingolipids. J␣Neurosci 19:7913–7924

    PubMed  CAS  Google Scholar 

  57. Vaguero J, Morales C, Zurita M, Oya S (1994) Gangliosides modulate the development of ethyl-nitrosourea induced brain tumors. Neurosci Lett 25:37–40

    Article  Google Scholar 

  58. Chekenaya M, Rooprai HK, Davies D, Levine JM, Butt AM, Pikington GJ (1999) The NG2 chondroitin sulfate proteoglycan: role in malignant progression of human brain tumors. Int J Dev Neurosci 17:421–435

    Article  PubMed  Google Scholar 

  59. Wolanska M, Sobolewski K, Cechowska-Pasko M, Jaworski S (2003) The activities of some glycosaminoglycans – degrading enzymes in uterine leiomyomas. Eur J Obst Gyn Rep Biol 110:73–78

    Article  CAS  Google Scholar 

  60. Ramsey RB, Smith KR, Crafts DC, Chung HD, Fredericks M (1980) Hydrolytic enzyme activities of the nervous system. Arch Neurol 37:356–359

    PubMed  CAS  Google Scholar 

  61. Tiby V, Lombardo A, Goi G, Tettamanti G, Gaini SM, Canal N (1984) Study of some lysosomal glycohydrolases in tumors of the nervous system. Res Commun Chem Pathol Pharmacol 44:149–161

    PubMed  CAS  Google Scholar 

  62. Ernst S, Langer R, Cooney CL, Sasisekhran R (1995) Enzymatic degradation of glycosaminoglycans. Crit Rev Biochem Mol Biol 30:387–444

    PubMed  CAS  Google Scholar 

  63. Wolanska M, Sobolewski K, Drozdzewicz M, Bankowski E (1998) Extracellular matrix components in uterine leiomyoma and their alteration during the tumour growth. Mol Cell Biochem 189:145–152

    Article  PubMed  CAS  Google Scholar 

  64. Sulowicz W, Lisiewicz J, Kuźniewski M, Strzałka H (1985) Activity of some lysosomal enzymes in peripheral blood lymphocytes of patients with lung cancer. A cytochemical study. Folia Haemat 112:63–70

    CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by a grand from Medical University of Bialystok.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Wielgat.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wielgat, P., Walczuk, U., Szajda, S. et al. Activity of lysosomal exoglycosidases in human gliomas. J Neurooncol 80, 243–249 (2006). https://doi.org/10.1007/s11060-006-9188-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11060-006-9188-z

Keywords

Navigation