Cells with intense EGFR staining and a high nuclear to cytoplasmic ratio are specific for infiltrative glioma: A useful marker in neuropathological practice

Neuro-Oncology

Volumn 15, Issue 10, 2013, Pages 1278-1288

  Burel Vandenbos, Fanny ^a,b   Turchi, Laurent ^a,b   Benchetrit, Maxime ^a   Fontas, Eric ^a   Pedeutour, Zoe ^a   Rigau, Valérie ^c   Almairac, Fabien ^a   Ambrosetti, Damien ^a   Michiels, Jean François ^a   Virolle, Thierry ^a,b  

^a UNIVERSITY HOSPITAL OF NICE   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c MONTPELLIER UNIVERSITY HOSPITAL   (France)

Author keywords

EGFR; glioblastomas; gliosis; immunohistochemistry; infiltrative gliomas; progenitors

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; EPIDERMAL GROWTH FACTOR RECEPTOR; ISOCITRATE DEHYDROGENASE 1;

ACUTE DISSEMINATED ENCEPHALOMYELITIS; ANTIBODY LABELING; ARTICLE; ASTROCYTOMA; BRAIN TISSUE; CANCER STAGING; CELL CULTURE; CHILDHOOD CANCER; DIAGNOSTIC TEST ACCURACY STUDY; DYSEMBRYOPLASTIC NEUROEPITHELIAL TUMOR; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; GENE AMPLIFICATION; GENE DOSAGE; GENE MUTATION; GLIOBLASTOMA; GLIOMA; GLIOSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFILTRATIVE GLIOMA; MAJOR CLINICAL STUDY; MULTIPLE SCLEROSIS; NEURAL STEM CELL; NEUROEPITHELIOMA; NEUROPATHOLOGY; OLIGODENDROGLIOMA; PHENOTYPE; PILOCYTIC ASTROCYTOMA; PREDICTIVE VALUE; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; STAINING;

EGFR; GLIOBLASTOMAS; GLIOSIS; IMMUNOHISTOCHEMISTRY; INFILTRATIVE GLIOMAS; PROGENITORS;

ADULT; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL NUCLEUS; CHILD; CYTOPLASM; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GLIOMA; HUMANS; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RETROSPECTIVE STUDIES; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 84885003629     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/not094     Document Type: Article

References (60)

1. Ohgaki H, Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol. 2005;64(6):479-489.
2. Louis DN, Ohgaki H, Wiestler OD, eds. et al. WHO Classification of Tumours of the Central Nervous System. Lyon: IARC; 2007.
3. Von Deimling A, Burger PC, Nakazato Y, et al. Diffuse astrocytoma. In: Louis, DN, Ohgaki, H, Wiestler, OD, ed.et al. WHO classification of Tumours of the Central Nervous System. Lyon: IARC; 2007:25-29.
4. Prayson R, Agamanolis D, Cohen M, et al. Interobserver reproducibility among neuropathologists and surgical pathologists in fibrillary astrocytoma grading. J Neurol Sci. 2000;175:33-39. (Pubitemid 30227481)
5. Zagzag D, Miller DC, Kleinman GM, et al. Demyelinating disease versus tumor in surgical neuropathology. Clues to a correct pathological diagnosis. Am J Surg Pathol. 1993;17(6):537-545. (Pubitemid 23152591)
6. Scott IS, Morris LS, RushbrookSM,et al.Immunohistochemical estimation of cell cycle entry and phase distribution in astrocytomas: applications in diagnostic neuropathology. Neuropathol Appl Neurobiol. 2005;31(5): 455-466. (Pubitemid 41337780)
7. Prayson RA. The utility of MIB-1/Ki-67 immunostaining in the evaluation of central nervous system neoplasms. Adv Anat Pathol. 2005;12(3): 144-148. (Pubitemid 40770111)
8. Louis DN. The p53 gene and protein in human brain tumors. J Neuropathol Exp Neurol. 1994;53(1):11-21. (Pubitemid 24022082)
9. Yaziji H, Massarani-Wafai R, Gujrati M, et al. Role of p53 immunohistochemistry in differentiating reactive gliosis from malignant astrocytic lesions. Am J Surg Pathol. 1996;20(9):1086-1090. (Pubitemid 26276929)
10. Camelo-Piragua S, Jansen M, Ganguly A, et al. A sensitive and specific diagnostic panel to distinguish diffuse astrocytoma from astrocytosis: chromosome 7 gain with mutant isocitrate dehydrogenase 1 and p53. J Neuropathol Exp Neurol. 2011;70(2):110-115.
11. Capper D, Zentgraf H, Balss J, et al.Monoclonal antibody specific for IDH1 R132H mutation. Acta Neuropathol. 2009;118(5):599-601.
12. Capper D, Weissert S, Balss J, et al. Characterization of R132H mutation-specific IDH1 antibody binding in brain tumors. Brain Pathol. 2010;20(1):245-254.
13. Balss J,Meyer J,MuellerW, et al. Analysis of theIDH1 codon 132 mutation in brain tumors. Acta Neuropathol. 2008;116(6):597-602.
14. Watanabe T, Nobusawa S, Kleihues P, et al. IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol. 2009;174(4):1149-1153.
15. Yan H, Parsons D, Jin G, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009;360(8):765-773.
16. Parsons D, Jones S, Zhang X, et al. An Integrated Genomic Analysis of Human Glioblastoma Multiforme. Science. 2008;321(5897):1807.
17. Burel-Vandenbos F, Benchetrit M, Miquel C, et al. EGFR immunolabeling pattern may discriminate low-grade gliomas from gliosis. J Neurooncol. 2011;102(2):171-178.
18. Kapoor GS, O'Rourke DM. Mitogenic signaling cascades in glial tumors. Neurosurgery. 2003;52(6):1425-1434. discussion 1434-1425.
19. Reifenberger J, Reifenberger G, Ichimura K, et al. Epidermal growth factor receptor expression in oligodendroglial tumors. Am J Pathol. 1996;149(1):29-35. (Pubitemid 26230975)
20. Kordek R, BiernatW, Alwasiak J, et al. p53 protein and epidermal growth factor receptor expression in human astrocytomas. J Neurooncol. 1995;26(1):11-16.
21. Mottolese M, Natali PG, Coli A, et al. Comparative analysis of proliferating cell nuclear antigen and epidermal growth factor receptor expression in glial tumours: correlation with histological grading. Anticancer Res. 1998;18(3B):1951-1956. (Pubitemid 28344854)
22. Orian JM, Vasilopoulos K, Yoshida S, et al. Overexpression of multiple oncogenes related to histological grade of astrocytic glioma. Br J Cancer. 1992;66(1):106-112.
23. Hwang SL, Chai CY, Lin HJ, et al. Expression of epidermal growth factor receptors and c-erbB-2 proteins in human astrocytic tumors. Kaohsiung J Med Sci. 1997;13(7):417-424.
24. Broholm H, Bols B, Heegaard S, et al. Immunohistochemical investigation of p53 and EGFR expression of oligodendrogliomas. Clin Neuropathol. 1999;18(4):176-180. (Pubitemid 29318056)
25. Yano S, Kondo K,YamaguchiM,et al. Distribution and function of EGFR in human tissue and the effect of EGFR tyrosine kinase inhibition. Anticancer Res. 2003;23(5A):3639-3650. (Pubitemid 37474306)
26. Wong RW, Guillaud L. The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine Growth Factor Rev. 2004;15(2-3): 147-156. (Pubitemid 38521250)
27. Wong RW. Transgenic and knock-out mice for deciphering the roles of EGFR ligands. Cell Mol Life Sci. 2003;60(1):113-118. (Pubitemid 36223120)
28. Boockvar JA, Kapitonov D, Kapoor G, et al. Constitutive EGFR signaling confers a motile phenotype to neural stem cells. Mol Cell Neurosci. 2003;24(4):1116-1130. (Pubitemid 38091521)
29. Nicholas MK, Lukas RV, Jafri NF, et al. Epidermal growth factor receptor - mediated signal transduction in the development and therapy of gliomas. Clin Cancer Res. 2006;12(24):7261-7270. (Pubitemid 46095397)
30. Penar PL, Khoshyomn S, Bhushan A, et al. Inhibition of epidermal growth factor receptor-associated tyrosine kinase blocks glioblastoma invasion of the brain. Neurosurgery. 1997;40(1):141-151. (Pubitemid 26425661)
31. Martens T, Laabs Y, Gunther HS, et al. Inhibition of glioblastoma growth in a highly invasive nude mouse model can be achieved by targeting epidermal growth factor receptor but not vascular endothelial growth factor receptor-2. Clin Cancer Res. 2008;14(17):5447-5458.
32. Suri V, Das P, Jain A, et al. Pediatric glioblastomas: a histopathological and molecular genetic study. Neuro Oncol. 2009;11(3):274-280.
33. Sung T, Miller DC, Hayes RL, et al. Preferential inactivation of the p53 tumor suppressor pathway and lack of EGFR amplification distinguish de novo high grade pediatric astrocytomas from de novo adult astrocytomas. Brain Pathol. 2000;10(2):249-259. (Pubitemid 30181093)
34. Saindane AM, Cha S, Law M, et al. Proton MR spectroscopy of tumefactive demyelinating lesions. AJNR Am J Neuroradiol. 2002;23(8): 1378-1386. (Pubitemid 35033889)
35. Hourani R, Brant LJ, Rizk T, et al. Can protonMRspectroscopic and perfusion imaging differentiate between neoplastic and nonneoplastic brain lesions in adults? AJNR Am J Neuroradiol. 2008;29(2):366-372. (Pubitemid 351287898)
36. Jarvela S, Helin H, Haapasalo J, et al. Amplification of the epidermal growth factor receptor in astrocytic tumours by chromogenic in situ hybridization: association with clinicopathological features and patient survival. Neuropathol Appl Neurobiol. 2006;32(4):441-450. (Pubitemid 44015585)
37. Mathieu A,Weynand B, Verbeken E, et al. Comparison of four antibodies for immunohistochemical evaluation of epidermal growth factor receptor expression in non-small cell lung cancer. LungCancer. 2010;69(1):46-50.
38. Lee HJ, Xu X, Choe G, et al. Protein overexpression and gene amplification of epidermal growth factor receptor in nonsmall cell lung carcinomas: Comparison of four commercially available antibodies by immunohistochemistry and fluorescence in situ hybridization study. Lung Cancer. 2010;68(3):375-382.
39. Guillaudeau A, Durand K, Rabinovitch-Chable H, et al. Adult diffuse gliomas produce mRNA transcripts encoding EGFR isoforms lacking a tyrosine kinase domain. Int J Oncol. 2012;40(4):1142-1152.
40. Kantelhardt SR, Caarls W, de Vries AH, et al. Specific visualization of glioma cells in living low-grade tumor tissue. PLoS One. 2010;5(6): e11323.
41. Marquez A,Wu R, Zhao J, et al. Evaluation of epidermal growth factor receptor (EGFR) by chromogenic in situ hybridization (CISH) and immunohistochemistry (IHC) in archival gliomas using bright-field microscopy. Diagn Mol Pathol. 2004;13(1):1-8. (Pubitemid 38263876)
42. Guillaudeau A, Durand K, Pommepuy I, et al. Determination of EGFR status in gliomas: usefulness of immunohistochemistry and fluorescent in situ hybridization. Appl Immunohistochem Mol Morphol. 2009;17(3):220-226.
43. Huang H, Hara A, Homma T, et al. Altered expression of immune defense genes in pilocytic astrocytomas. J Neuropathol Exp Neurol. 2005;64(10): 891-901. (Pubitemid 41434672)
44. Colin C, Baeza N, Bartoli C, et al. Identification of genes differentially expressed in glioblastoma versus pilocytic astrocytoma using Suppression Subtractive Hybridization. Oncogene. 2006;25(19):2818-2826.
45. Rorive S, Maris C, Debeir O, et al. Exploring the distinctive biological characteristics of pilocytic and low-grade diffuse astrocytomas using microarray gene expression profiles. J Neuropathol Exp Neurol. 2006;65(8): 794-807. (Pubitemid 44200320)
46. Vandercappellen J, Van Damme J, Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett. 2008;267(2):226-244.
47. Goldbrunner RH, Bernstein JJ, Tonn JC. Cell-extracellular matrix interaction in glioma invasion. Acta Neurochir (Wien). 1999;141(3):295-305 discussion 304-295. (Pubitemid 29137544)
48. Mazzoleni S, Politi LS, Pala M, et al. Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Res. 2010;70(19):7500-7513.
49. Phillips RJ, Mestas J, Gharaee-Kermani M, et al. Epidermal growth factor and hypoxia-induced expression of CXC chemokine receptor 4 on nonsmall cell lung cancer cells is regulated by the phosphatidylinositol 3-kinase/PTEN/AKT/ mammalian target of rapamycin signaling pathway and activation of hypoxia inducible factor-1alpha. J Biol Chem. 2005;280(23):22473-22481. (Pubitemid 40827903)
50. Prasad NK. SHIP2 phosphoinositol phosphatase positively regulates EGFR-Akt pathway, CXCR4 expression, and cell migration in MDA-MB-231 breast cancer cells. Int J Oncol. 2009;34(1):97-105.
51. Guo Z, Cai S, Fang R, et al. The synergistic effects of CXCR4 and EGFR on promoting EGF-mediated metastasis in ovarian cancer cells. Colloids Surf B Biointerfaces. 2007;60(1):1-6. (Pubitemid 47302287)
52. Porcile C, Bajetto A, Barbero S, et al. CXCR4 activation induces epidermal growth factor receptor transactivation in an ovarian cancer cell line. AnnN Y Acad Sci. 2004;1030:162-169. (Pubitemid 40378910)
53. Porcile C, Bajetto A, Barbieri F, et al. Stromal cell-derived factor-1alpha (SDF-1alpha/CXCL12) stimulates ovarian cancer cell growth through the EGF receptor transactivation. Exp Cell Res. 2005;308(2):241-253.
54. Ignatova TN, Kukekov VG, Laywell ED, et al. Human cortical glial tumors contain neural stem-like cells expressingastroglial and neuronal markers in vitro. Glia. 2002;39(3):193-206.
55. Bao S,Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444(7120):756-760. (Pubitemid 44949604)
56. Thirant C, Bessette B, Varlet P, et al. Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors. PLoS One. 2011;6(1): e16375.
57. Colin C, Baeza N, Tong S, et al. In vitro identification and functional characterization of glial precursor cells in human gliomas. Neuropathol Appl Neurobiol. 2006;32(2):189-202.
58. Varghese M, Olstorn H, Sandberg C, et al. A comparison between stem cells from the adult human brain and from brain tumors. Neurosurgery. 2008;63(6):1022-1033. discussion 1033-1024.
59. Derynck R, Goeddel DV, Ullrich A, et al. Synthesis of messenger RNAs for transforming growth factors alpha and beta and the epidermal growth factor receptor by human tumors. Cancer Res. 1987;47(3): 707-712. (Pubitemid 17027960)
60. Zhou R, Skalli O. TGF-alpha differentially regulates GFAP, vimentin, and nestin gene expression in U-373 MG glioblastoma cells: correlation with cell shape and motility. Exp Cell Res. 2000;254(2):269-278. (Pubitemid 30080583)