Skip to main content
Have a personal or library account? Click to login
Gamma-enolase: a well-known tumour marker, with a less-known role in cancer Cover

Gamma-enolase: a well-known tumour marker, with a less-known role in cancer

By:  and    
Open Access
|Aug 2015

References

  1. 1. Pancholi V. Multifunctional alpha-enolase: its role in diseases.2001;902-20.
  2. 2. Kim JW, Dang CV. Multifaceted roles of glycolytic enzymes.2005;142-50.
  3. 3. Masoudi-Nejad A, Asgari Y. Metabolic cancer biology: Structural-based analysis of cancer as a metabolic disease, new sights and opportunities for disease treatment.2015;21-9.
  4. 4. Dang CV, Semenza GL. Oncogenic alterations of metabolism.1999;68-72.
  5. 5. McAlister L, Holland MJ. Targeted deletion of a yeast enolase structural gene. Identification and isolation of yeast enolase isozymes.1982;7181-8.
  6. 6. Diaz-Ramos A, Roig-Borrellas A, Garcia-Melero A, Lopez-Alemany R. Alpha-enolase, a multifunctional protein: its role on pathophysiological situations.2012;156795
  7. 7. Hattori T, Takei N, Mizuno Y, Kato K, Kohsaka S. Neurotrophic and neuro-protective effects of neuron-specific enolase on cultured neurons from embryonic rat brain.1995;191-8.
  8. 8. Suresh MR. Cancer Markers. In: Wild D, editor.. Third edition. Oxford, UK: Elsevier; 2005. p. 664-94.
  9. 9. Marangos PJ, Parma AM, Goodwin FK. Functional properties of neuronal and glial isoenzymes of brain enolase.1978;727-32.
  10. 10. Fletcher L, Rider CC, Taylor CB. Enolase isoenzymes: III. Chromatographic and immunological characteristics of rat brain enolase.1976;245-52.
  11. 11. Giallongo A, Feo S, Moore R, Croce CM, Showe LC. Molecular cloning and nucleotide sequence of a full-length cDNA for human alpha enolase.1986;6741-5.
  12. 12. Feo S, Oliva D, Barbieri G, Xu WM, Fried M, Giallongo A. The gene for the muscle-specific enolase is on the short arm of human chromosome 17.1990;192-4.
  13. 13. Lebioda L, Stec B. Mapping of isozymic differences in enolase.1991;97-100.
  14. 14. Faller LD, Johnson AM. Calorimetric studies of the role of magnesium ions in yeast enolase catalysis.1974;1083-7.
  15. 15. Brewer JM. Specificity and mechanism of action of metal ions in yeast enolase.1985;8-14.
  16. 16. Vallee BL. Zinc and metalloenzymes.1955;317-84.
  17. 17. Faller LD, Baroudy BM, Johnson AM, Ewall RX. Magnesium ion requirements for yeast enolase activity.1977;3864-9.
  18. 18. Brewer JM. Yeast enolase: mechanism of activation by metal ions.1981;209-54.
  19. 19. Brewer JM, Ellis PD. 31P-nmr studies of the effect of various metals on substrate binding to yeast enolase.1983;71-82.
  20. 20. Ko-Jiunn L, Neng-Yao S. The role of enolase in tissue invasion and metastasis of pathogens and tumor cells.2007;45-8.
  21. 21. Ghosh AK, Steele R, Ray RB. Functional domains of c-myc promoter binding protein 1 involved in transcriptional repression and cell growth regulation.1999;2880-6.
  22. 22. Feo S, Arcuri D, Piddini E, Passantino R, Giallongo A. ENO1 gene product binds to the c-myc promoter and acts as a transcriptional repressor: relationship with Myc promoter-binding protein 1 (MBP-1).2000;47-52.
  23. 23. Capello M, Ferri-Borgogno S, Cappello P, Novelli F. Alpha-Enolase: a promising therapeutic and diagnostic tumor target.2011;1064-74.
  24. 24. Mears R, Craven RA, Hanrahan S, Totty N, Upton C, Young SL, et al. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry.2004;4019-31.
  25. 25. Yu X, Harris SL, Levine AJ. The regulation of exosome secretion: a novel function of the p53 protein.2006;4795-801.
  26. 26. Cappello P, Tomaino B, Chiarle R, Ceruti P, Novarino A, Castagnoli C, et al. An integrated humoral and cellular response is elicited in pancreatic cancer by alpha-enolase, a novel pancreatic ductal adenocarcinoma-associated antigen.2009;639-48.
  27. 27. He P, Naka T, Serada S, Fujimoto M, Tanaka T, Hashimoto S, et al. Proteomics-based identification of alpha-enolase as a tumor antigen in non-small lung cancer.2007;1234-40.
  28. 28. Seweryn E, Pietkiewicz J, Bednarz-Misa IS, Ceremuga I, Saczko J, Kulbacka J, et al. Localization of enolase in the subfractions of a breast cancer cell line.2009;754-8.
  29. 29. Nakajima K, Hamanoue M, Takemoto N, Hattori T, Kato K, Kohsaka S. Plasminogen binds specifically to alpha-enolase on rat neuronal plasma membrane.1994;2048-57.
  30. 30. Miles LA, Dahlberg CM, Plescia J, Felez J, Kato K, Plow EF. Role of cell-surface lysines in plasminogen binding to cells: identification of .alpha.-enolase as a candidate plasminogen receptor.1991;1682-91.
  31. 31. Dudani AK, Cummings C, Hashemi S, Ganz PR. Isolation of a novel 45 kDa plasminogen receptor from human endothelial cells.1993;185-96.
  32. 32. Redlitz A, Fowler BJ, Plow EF, Miles LA. The role of an enolase-related molecule in plasminogen binding to cells.1995;407-15.
  33. 33. Merkulova T, Lucas M, Jabet C, Lamandé N, Rouzeau JD, Gros F, et al. Biochemical characterization of the mouse muscle-specific enolase: developmental changes in electrophoretic variants and selective binding to other proteins.1997;791-800.
  34. 34. Keller A, Demeurie J, Merkulova T, Geraud G, Cywiner-Golenzer C, Lucas M, et al. Fibre-type distribution and subcellular localisation of alpha and beta enolase in mouse striated muscle.2000;527-35.
  35. 35. Merkulova T, Dehaupas M, Nevers MC, Créminon C, Alameddine H, Keller A. Differential modulation of alpha, beta and gamma enolase isoforms in regenerating mouse skeletal muscle.2000;3735-43.
  36. 36. Royds JA, Variend S, Timperley WR, Taylor CB. An investigation of beta enolase as a histological marker of rhabdomyosarcoma.1984;905-10.
  37. 37. Royds JA, Variend S, Timperley WR, Taylor CB. Comparison of beta enolase and myoglobin as histological markers of rhabdomyosarcoma.1985;1258-60.
  38. 38. Tiainen M, Roine RO, Pettila V, Takkunen O. Serum neuron-specific enolase and S-100B protein in cardiac arrest patients treated with hypothermia.2003;2881-6.
  39. 39. Lamerz R. NSE (neuron-specific enolase) γ-enolase. In: Thomas L, editor.1st. edition. Frankfurt/Main, Germany: TH-Books Verlagsgesellschaft; 1998. p. 979-81.
  40. 40. Soh MA, Garrett SH, Somji S, Dunlevy JR, Zhou XD, Sens MA, et al. Arsenic, cadmium and neuron specific enolase (ENO2, γ-enolase) expression in breast cancer.2011;41
  41. 41. Haimoto H, Takahashi Y, Koshikawa T, Nagura H, Kato K. Immunohistochemical localization of gamma-enolase in normal human tissues other than nervous and neuroendocrine tissues.1985;257-63.
  42. 42. Vinores SA, Herman MM, Rubinstein LJ. Electron-immunocytochemical localization of neuron-specific enolase in cytoplasm and on membranes of primary and metastatic cerebral tumours and on glial filaments of glioma cells.1986;891-908.
  43. 43. Hafner A, Obermajer N, Kos J. gamma-1-syntrophin mediates trafficking of gamma-enolase towards the plasma membrane and enhances its neurotrophic activity.2010;246-58.
  44. 44. Burack WR, Shaw AS. Signal transduction: hanging on a scaffold.2000;211-6.
  45. 45. Ponting CP, Phillips C, Davies KE, Blake DJ. PDZ domains: targeting signalling molecules to sub-membranous sites.1997;469-79.
  46. 46. Obermajer N, Doljak B, Jamnik P, Fonovic UP, Kos J. Cathepsin X cleaves the C-terminal dipeptide of alpha- and gamma-enolase and impairs survival and neuritogenesis of neuronal cells.2009;1685-96.
  47. 47. McAleese SM, Dunbar B, Fothergill JE, Hinks LJ, Day IN. Complete amino acid sequence of the neurone-specific gamma isozyme of enolase (NSE) from human brain and comparison with the non-neuronal alpha form (NNE).1988;413-7.
  48. 48. Butterfield DA, Lange ML. Multifunctional roles of enolase in Alzheimer’s disease brain: beyond altered glucose metabolism.2009;915-33.
  49. 49. Soh M, Dunlevy JR, Garrett SH, Allen C, Sens DA, Zhou XD, et al. Increased neuron specific enolase expression by urothelial cells exposed to or malignantly transformed by exposure to Cdor As.2012;66-74.
  50. 50. Yan T, Skaftnesmo KO, Leiss L, Sleire L, Wang J, Li X, et al. Neuronal markers are expressed in human gliomas and NSE knockdown sensitizes glioblastoma cells to radiotherapy and temozolomide.2011;524
  51. 51. Loja T, Chlapek P, Kuglik P, Pesakova M, Oltova A, Cejpek P, et al. Characterization of a GM7 glioblastoma cell line showing CD133 positivity and both cytoplasmic and nuclear localization of nestin.2009;119-27.
  52. 52. Splinter TA, Verkoelen CF, Vlastuin M, Kok TC, Rijksen G, Haglid KG, et al. Distinction of two different classes of small-cell lung cancer cell lines by enzymatically inactive neuron-specific enolase.1992;1065-9.
  53. 53. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer’s Achilles’ heel.2008;472-82.
  54. 54. Vesselle H, Schmidt RA, Pugsley JM, Li M, Kohlmyer SG, Vallires E, et al. Lung cancer proliferation correlates with [F-18]fluorodeoxyglucose uptake by positron emission tomography.2000;3837-44.
  55. 55. Porporato PE, Dhup S, Dadhich RK, Copetti T, Sonveaux P. Anticancer targets in the glycolytic metabolism of tumors: a comprehensive review.2011;49
  56. 56. Golpour M, Akhavan Niaki H, Khorasani HR, Hajian A, Mehrasa R, Mostafazadeh A. Human fibroblast switches to anaerobic metabolic pathway in response to serum starvation: a mimic of warburg effect.2014;74-80.
  57. 57. Wu C-A, Chao Y, Shiah S-G, Lin W-W. Nutrient deprivation induces the Warburg effect through ROS/AMPK-dependent activation of pyruvate dehydrogenase kinase.2013;1147-56.
  58. 58. Jang SM, Kim JW, Kim CH, Kim D, Rhee S, Choi KH. p19(ras) Represses proliferation of non-small cell lung cancer possibly through interaction with Neuron-Specific Enolase (NSE).2010;91-8..
  59. 59. Amoêdo Ní D, Valencia J P, Rodrigues M F, Galina A, Rumjanek F D. How does the metabolism of tumour cells differ from that of normal cells.. 2013;e00080.
  60. 60. Sedoris KC, Thomas SD, Miller DM. Hypoxia induces differential translation of enolase/MBP-1.2010;157
  61. 61. Vinores SA, Bonnin JM, Rubinstein LJ, Marangos PJ. Immunohistochemical demonstration of neuron-specific enolase in neoplasms of the CNS and other tissues.1984;536-40.
  62. 62. Vinores SA, Marangos PJ, Bonnin JM, Rubinstein LJ. Immunoradiometric and immunohistochemical demonstration of neuron-specific enolase in experimental rat gliomas.1984;2595-9.
  63. 63. Kondoh H, Lleonart ME, Bernard D, Gil J. Protection from oxidative stress by enhanced glycolysis; a possible mechanism of cellular immortalization.2007;85-90.
  64. 64. Pelicano H, Martin DS, Xu RH, Huang P. Glycolysis inhibition for anticancer treatment.2006;4633-46.
  65. 65. Takei N, Kondo J, Nagaike K, Ohsawa K, Kato K, Kohsaka S. Neuronal survival factor from bovine brain is identical to neuron-specific enolase.1991;1178-84.
  66. 66. Hafner A, Glavan G, Obermajer N, Zivin M, Schliebs R, Kos J. Neuroprotective role of gamma-enolase in microglia in a mouse model of Alzheimer’s disease is regulated by cathepsin X.2013;604-14.
  67. 67. Hattori T, Ohsawa K, Mizuno Y, Kato K, Kohsaka S. Synthetic peptide corresponding to 30 amino acids of the C-terminal of neuron-specific enolase promotes survival of neocortical neurons in culture.1994;25-30.
  68. 68. Hafner A, Obermajer N, Kos J. gamma-Enolase C-terminal peptide promotes cell survival and neurite outgrowth by activation of the PI3K/Akt and MAPK/ERK signalling pathways.2012;439-50.
  69. 69. Pišlar AH, Kos J. C-terminal peptide of gamma-enolase impairs amyloid-beta-induced apoptosis through p75(NTR) signaling.2013;623-35.
  70. 70. Wendt W, Zhu X-R, Lübbert H, Stichel CC. Differential expression of cathepsin X in aging and pathological central nervous system of mice.2007;525-40.
  71. 71. Kos J, Vižin T, Fonović UP, Pišlar A. Intracellular signaling by cathepsin X: Molecular mechanisms and diagnostic and therapeutic opportunities in cancer.2015;: 76-83.
  72. 72. Amberger-Murphy V. Hypoxia helps glioma to fight therapy.2009;381-90.
  73. 73. Levin VA, Panchabhai SC, Shen L, Kornblau SM, Qiu Y, Baggerly KA. Different changes in protein and phosphoprotein levels result from serum starvation of high-grade glioma and adenocarcinoma cell lines.2010;179-91.
  74. 74. Levin VA, Panchabhai S, Shen L, Baggerly KA. Protein and phosphoprotein levels in glioma and adenocarcinoma cell lines grown in normoxia and hypoxia in monolayer and three-dimensional cultures.2012;5
  75. 75. Yan T, Skaftnesmo KO, Leiss L, Sleire L, Wang J, Li X, et al. Neuronal markers are expressed in human gliomas and NSE knockdown sensitizes.2011;524
  76. 76. Yamaguchi H, Condeelis J. Regulation of the actin cytoskeleton in cancer cell migration and invasion.2007;642-52.
  77. 77. Walsh JL, Keith TJ, Knull HR. Glycolytic enzyme interactions with tubulin and microtubules.1989;64-70.
  78. 78. Trojanowicz B, Winkler A, Hammje K, Chen Z, Sekulla C, Glanz D, et al. Retinoic acid-mediated down-regulation of ENO1/MBP-1 gene products caused decreased invasiveness of the follicular thyroid carcinoma cell lines.2009;249-60.
  79. 79. Georges E, Bonneau AM, Prinos P. RNAi-mediated knockdown of alpha-enolase increases the sensitivity of tumor cells to antitubulin chemotherapeutics.2011;303-8.
  80. 80. Kasprzak A, Zabel M, Biczysko W. Selected markers (chromogranin A, neuron-specific enolase, synaptophysin, protein gene product 9.5) in diagnosis and prognosis of neuroendocrine pulmonary tumours.2007;23-33.
  81. 81. Tapia FJ, Polak JM, Barbosa AJ, Bloom SR, Marangos PJ, Dermody C, et al. Neuron-specific enolase is produced by neuroendocrine tumours.1981;808-11.
  82. 82. Lopez J. Carl A. Burtis, Edward R. In: Ashwood and David E. Bruns, editors.5th edition. St. Louis, USA: Elsevier; 2012.
  83. 83. Stieber P, Hatz R, Holdenrieder S, Molina R, Nap M, von Pawel J, et al. National Academy of Clinical Biochemistry Guidelines for the use of tumor markers in lung cancer. Section 3P. AACC press; 2006. [citated 2015 Jan 25]. Available at.
  84. 84. Hao X, Sun B, Hu L, Lahdesmaki H, Dunmire V, Feng Y, et al. Differential gene and protein expression in primary breast malignancies and their lymph node metastases as revealed by combined cDNA microarray and tissue microarray analysis.2004;1110-22.
  85. 85. Miremadi A, Pinder SE, Lee AH, Bell JA, Paish EC, Wencyk P, et al. Neuroendocrine differentiation and prognosis in breast adenocarcinoma.2002;215-22.
  86. 86. Sawaki M, Yokoi K, Nagasaka T, Watanabe R, Kagawa C, Takada H, et al. Prognostic importance of neuroendocrine differentiation in Japanese breast cancer patients.2010;831-5.
  87. 87. Allen FJ, Van Velden DJ, Heyns CF. Are neuroendocrine cells of practical value as an independent prognostic parameter in prostate cancer?1995;751-4.
  88. 88. Marangos PJ, Schmechel DE. Neuron specific enolase, a clinically useful marker for neurons and neuroendocrine cells.1987;269-95.
  89. 89. Rundgren M, Cronberg T, Friberg H, Isaksson A. Serum neuron specific enolase - impact of storage and measuring method.2014;726
  90. 90. Yuan SM. Biomarkers of cerebral injury in cardiac surgery.2014;638-45.
  91. 91. Sturgeon C. Practice guidelines for tumor marker use in the clinic.2002;1151-9.
  92. 92. Fujiwara H, Arima N, Ohtsubo H, Matsumoto T, Kukita T, Kawada H, et al. Clinical significance of serum neuron-specific enolase in patients with adult T-cell leukemia.2002;80-4.
  93. 93. Wang L, Liu P, Chen X, Geng Q, Lu Y. Serum neuron-specific enolase is correlated with clinical outcome of patients with non-germinal center B cell-like subtype of diffuse large B-cell lymphoma treated with rituximab-based immunochemotherapy.2012;2153-8.
  94. 94. Lorenz J, Dippold W. Neuron-specific enolase-a serum marker for malignant melanoma.1989;1754-5.
  95. 95. Ro C, Chai W, Yu VE, Yu R. Pancreatic neuroendocrine tumors: biology, diagnosis, and treatment.2013;312-24.
  96. 96. Massironi S, Sciola V, Peracchi M, Ciafardini C, Spampatti MP, Conte D. Neuroendocrine tumors of the gastro-entero-pancreatic system.2008;5377-84.
  97. 97. DeYoung C, Edelman M. Prognostic Factors for Small-Cell Lung Cancer. In: Syrigos K, Nutting C, Roussos C, editors.Berlin, Heidelberg: Springer; 2006. p. 189-97.
  98. 98. Sturgeon CM, Duffy MJ, Stenman UH, Lilja H, Brunner N, Chan DW, et al. National Academy of Clinical Biochemistry laboratory medicine practice guidelines for use of tumor markers in testicular, prostate, colorectal, breast, and ovarian cancers.2008;e11-79.
  99. 99. Lamberts SWJ, Hofland LJ, Nobels FRE. Neuroendocrine tumor markers.2001;309-39.
  100. 100. Riley RD, Heney D, Jones DR, Sutton AJ, Lambert PC, Abrams KR, et al. A systematic review of molecular and biological tumor markers in neuroblastoma.2004;4-12.
  101. 101. Johnsson P, Blomquist S, Lührs C, Malmkvist G, Alling C, Solem J-O, et al. Neuron-specific enolase increases in plasma during and immediately after extracorporeal circulation.2000;750-4.
  102. 102. Ramont L, Thoannes H, Volondat A, Chastang F, Millet MC, Maquart FX. Effects of hemolysis and storage condition on neuron-specific enolase (NSE) in cerebrospinal fluid and serum: implications in clinical practice.2005;1215-7.
  103. 103. Marangos PJ, Campbell IC, Schmechel DE, Murphy DL, Goodwin FK. Blood platelets contain a neuron-specific enolase subunit.1980;1254-8.
  104. 104. Trape J, Filella X, Alsina-Donadeu M, Juan-Pereira L, Bosch-Ferrer A, Rigo-Bonnin R. Increased plasma concentrations of tumour markers in the absence of neoplasia.2011;1605-20.
  105. 105. Collazos J, Esteban C, Fernandez A, Genolla J. Measurement of the serum tumor marker neuron-specific enolase in patients with benign pulmonary diseases.1994;143-5.
  106. 106. Filella X, Cases A, Molina R, Jo J, Bedini JL, Revert L, et al. Tumor markers in patients with chronic renal failure.1990;85-8.
  107. 107. DeGiorgio CM, Gott PS, Rabinowicz AL, Heck CN, Smith TD, Correale JD. Neuron-specific enolase, a marker of acute neuronal injury, is increased in complex partial status epilepticus.1996;606-9.
  108. 108. Strachan MW, Abraha HD, Sherwood RA, Lammie GA, Deary IJ, Ewing FM, et al. Evaluation of serum markers of neuronal damage following severe hypoglycaemia in adults with insulin-treated diabetes mellitus.1999;5-12.
  109. 109. Collazos J, Genolla J, Ruibal A. Neuron-specific enolase concentrations in serum in benign liver diseases.1991;579-81.
  110. 110. Massabki PS, Silva NP, Lourenco DM, Andrade LE. Neuron specific enolase concentration is increased in serum and decreased in platelets of patients with active systemic sclerosis.2003;2606-12.
  111. 111. Petrak J, Ivanek R, Toman O, Cmejla R, Cmejlova J, Vyoral D, et al. Deja vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins.2008;1744-9.
DOI: https://doi.org/10.1515/raon-2015-0035 | Journal eISSN: 1581-3207 | Journal ISSN: 1318-2099
Language: English
Page range: 217 - 226
Submitted on: May 9, 2015
Accepted on: Jul 13, 2015
Published on: Aug 21, 2015
Published by: Association of Radiology and Oncology
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2015 Tjasa Vizin, Janko Kos, published by Association of Radiology and Oncology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.