Neuregulin 1 enhances cell adhesion molecule L1 expression in human glioma cells and promotes their migration as a function of malignancy

Journal of Neuropathology and Experimental Neurology

Volumn 72, Issue 3, 2013, Pages 244-255

  Zhao, Wei Jiang ^a   Schachner, Melitta ^a  

^a SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

CD171; Glioblastoma; Glioma cell lines; L1 cell adhesion molecule; L1CAM; Neuregulin 1; Nrg1; Tissue array.

Indexed keywords

ERLOTINIB; LAPATINIB; NERVE CELL ADHESION MOLECULE L1; NEU DIFFERENTIATION FACTOR; NEUREGULIN 1 ALPHA; NEUREGULIN 1 BETA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CANCER GRADING; CELL MIGRATION; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE SILENCING; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TISSUE MICROARRAY; TUMOR PROMOTION; UPREGULATION;

BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FLUORESCENT ANTIBODY TECHNIQUE; GLIOMA; HUMANS; NEOPLASM INVASIVENESS; NEURAL CELL ADHESION MOLECULE L1; NEUREGULIN-1; TISSUE ARRAY ANALYSIS;

EID: 84874659140     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3182863dc5     Document Type: Article

References (58)

1. Maness PF, Schachner M. Neural recognition molecules of the immunoglobulin superfamily: Signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007;10:19-26
2. Gavert N, Conacci-Sorrell M, Gast D, et al. L1, a novel target of beta-catenin signaling, transforms cells and is expressed at the invasive front of colon cancers. J Cell Biol 2005;168:633-42
3. Schmid RS, Maness PF. L1 and NCAM adhesion molecules as signaling coreceptors in neuronal migration and process outgrowth. Curr Opin Neurobiol 2008;18:245-50
4. Siesser PF, Maness PF. L1 cell adhesion molecules as regulators of tumor cell invasiveness. Cell Adh Migr 2009;3:275-77
5. Gutwein P, Mechtersheimer S, Riedle S, et al. ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles. FASEB J 2003;17:292-94
6. Kalus I, Schnegelsberg B, Seidah NG, et al. The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1. J Biol Chem 2003;278:10381-88
7. Perides G, Safran RM, Downing LA, et al. Regulation of neural cell adhesion molecule and L1 by the transforming growth factor-beta superfamily. Selective effects of the bone morphogenetic proteins. J Biol Chem 1994;269:765-70
8. Yang M, Adla S, Temburni MK, et al. Stimulation of glioma cell motility by expression, proteolysis, and release of the L1 neural cell recognition molecule. Cancer Cell Int 2009;9:27
9. Faissner A, Kruse J, Goridis C, et al. The neural cell adhesion molecule L1 is distinct from the N-CAMYrelated group of surface antigens BSP-2 and D2. EMBO J 1984;3:733-37
10. Lindner J, Rathjen FG, Schachner M. L1 mono-and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 1983;305:427-30
11. Rathjen FG, Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J 1984;3:1-10
12. Salton SR, Richter-Landsberg C, Greene LA, et al. Nerve growth factor-inducible large external (NILE) glycoprotein: Studies of a central and peripheral neuronal marker. J Neurosci 1983;3:441-54
13. Dahlin-Huppe K, Berglund EO, Ranscht B, et al. Mutational analysis of the L1 neuronal cell adhesion molecule identifies membrane-proximal amino acids of the cytoplasmic domain that are required for cytoskeletal anchorage. Mol Cell Neurosci 1997;9:144-56
14. Zisch AH, Stallcup WB, Chong LD, et al. Tyrosine phosphorylation of L1 family adhesion molecules: Implication of the Eph kinase Cek5. J Neurosci Res 1997;47:655-65
15. Lüthl A, Laurent JP, Figurov A, et al. Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 1994; 372:777-79
16. Law JW, Lee AY, Sun M, et al. Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J Neurosci 2003;23:10419-32
17. Zhong ZG, Yokoyama S, Noda M, et al. Overexpression of adhesion molecule L1 in NG108-15 neuroblastoma X glioma hybrid cells enhances dibutyryl cyclic AMP-induced neurite outgrowth and functional synapse formation with myotubes. J Neurochem 1997;68:2291-99
18. Rawnaq T, Quaas A, Zander H, et al. L1 is highly expressed in tumors of the nervous system: A study of over 8000 human tissues. J Surg 2012; 173:314-19
19. Kaifi JT, Heidtmann S, Schurr PG, et al. Absence of L1 in pancreatic masses distinguishes adenocarcinomas from poorly differentiated neuroendocrine carcinomas. Anticancer Res 2006;26:1167-70
20. Kaifi JT, Strelow A, Schurr PG, et al. L1 (CD171) is highly expressed in gastrointestinal stromal tumors. Mod Pathol 2006;19:399-406
21. Kaifi JT, Zinnkann U, Yekebas EF, et al. L1 is a potential marker for poorly-differentiated pancreatic neuroendocrine carcinoma. World J Gastroenterol 2006;12:94-98
22. Nilsson P, Gedda L, Sjöström A, et al. Effects of dextranation on the uptake of peptides in micrometastases: Studies on binding of EGF in tumor spheroids. Tumour Biol 2001;22:229-38
23. Thuringer D, Hammann A, Benikhlef N, et al. Transactivation of the epidermal growth factor receptor by heat shock protein 90 via Toll-like receptor 4 contributes to the migration of glioblastoma cells. Biol Chem 2011;286:3418-28
24. Ritch PS, Carroll SL, Sontheimer H. Neuregulin-1 enhances survival of human astrocytic glioma cells. Glia 2005;51:217-28
25. Mei L, Xiong WC. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008;9:437-52
26. Bernstein HG, Lendeckel U, Bertram I, et al. Localization of neuregulin-1alpha (heregulin-alpha) and one of its receptors, ErbB-4 tyrosine kinase, in developing and adult human brain. Brain Res Bull 2006;69:546-59
27. Prevot V, Rio C, Cho GJ. Normal female sexual development requires neuregulin-erbB receptor signaling in hypothalamic astrocytes. J Neurosci 2003;23:230-39
28. Zhao W, Ren SG. Neuregulin-1 (Nrg1) is mainly expressed in rat pituitary gonadotroph cells and possibly regulates prolactin (PRL) secretion in a juxtacrine manner. J Neuroendocrinol 2011;23:1252-62
29. Zhao WJ, Ren SG. Endogenous neuregulin-1 expression in the anterior pituitary of female Wistar-Furth rats during the estrous cycle. Nan Fang Yi Ke Da Xue Xue Bao 2011;31:921-27
30. Wilson TR, Lee DY, Berry L, et al. Neuregulin-1Ymediated autocrine signaling underlies sensitivity to HER2 kinase inhibitors in a subset of human cancers. Cancer Cell 2011;20:158-72
31. Zhao W, Shen Y, Ren S. Endogenous expression of neuregulin-1 (Nrg1) as a potential modulator of prolactin (PRL) secretion in GH3 cells. Cell Tissue Res 2011;344:313-20
32. Hijazi MM, Thompson EW, Tang C, et al. Heregulin regulates the actin cytoskeleton and promotes invasive properties in breast cancer cell lines. Int J Oncol 2000;17:629-41
33. Miller MW, Mooney SM, Middleton FA. Transforming growth factor beta1 and ethanol affect transcription and translation of genes and proteins for cell adhesion molecules in B104 neuroblastoma cells. J Neurochem 2006;97:1182-90
34. Bennett V, Healy J. Organizing the fluid membrane bilayer: Diseases linked to spectrin and ankyrin. Trends Mol Med 2008;14:28-36
35. Deakin IH, Nissen W, Law AJ, et al. Transgenic overexpression of the type I isoform of neuregulin 1 affects working memory and hippocampal oscillations but not long-term potentiation. Cereb Cortex 2011; 22:1520-29
36. Kwon OB, Paredes D, Gonzalez CM, et al. Neuregulin-1 regulates LTP at CA1 hippocampal synapses through activation of dopamine D4 receptors. Proc Natl Acad Sci USA 2008;105:15587-92
37. Louis DN, Ohgaki H, Wiestler OD, et al. World Health Organization Classification of Tumours of the Central Nervous System, 4th Ed, Vol 1. Geneva, Switzerland: IARC/WHO; 2007
38. Louis KS, Siegel AC. Cell viability analysis using trypan blue: Manual and automated methods. Methods Mol Biol 2011;740:7-12
39. Ritch PA, Carroll SL, Sontheimer H. Neuregulin-1 enhances motility and migration of human astrocytic glioma cells. J Biol Chem 2003;278: 20971-78
40. van der Horst EH, Weber I, Ullrich A. Tyrosine phosphorylation of PYK2 mediates heregulin-induced glioma invasion: Novel heregulin/HER3-stimulated signaling pathway in glioma. Int J Cancer 2005;113: 689-98
41. Izumoto S, Ohnishi T, Arita N, et al. Gene expression of neural cell adhesion molecule L1 in malignant gliomas and biological significance of L1 in glioma invasion. Cancer Res 1996;56:1440-44
42. Bao S, Wu Q, Li Z, et al. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res 2008;68:6043-48
43. Cheng L, Wu Q, Guryanova OA, et al. Elevated invasive potential of glioblastoma stem cells. Biochem Biophys Res Commun 2011;406: 643-48
44. Suzuki T, Izumoto S, Fujimoto Y, et al. Clinicopathological study of cellular proliferation and invasion in gliomatosis cerebri: Important role of neural cell adhesion molecule L1 in tumour invasion. J Clin Pathol 2005;58:166-71
45. Tsuzuki T, Izumoto S, Ohnishi T, et al. Neural cell adhesion molecule L1 in gliomas: Correlation with TGF-beta and p53. J Clin Pathol 1998;51: 13-17
46. Hillenbrand R, Molthagen M, Montag D, et al. The close homologue of the neural adhesion molecule L1 (CHL1): Patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur J Neurosci 1999;11:813-26
47. Zhang Y, Roslan R, Lang D, et al. Expression of CHL1 and L1 by neurons and glia following sciatic nerve and dorsal root injury. Mol Cell Neurosci 2000;16:71-86
48. Wolterink S, Moldenhauer G, Fogel M, et al. Therapeutic antibodies to human L1CAM: Functional characterization and application in a mouse model for ovarian carcinoma. Cancer Res 2010;70:2504-15
49. Schäfer MK, Altevogt P. L1CAM malfunction in the nervous system and human carcinomas. Cell Mol Life Sci 2010;67:2425-37
50. Donier E, Gomez-Sanchez JA, Grijota-Martinez C, et al. L1CAM binds ErbB receptors through Ig-like domains coupling cell adhesion and neuregulin signaling. PLoS One 2012;7:e40674
51. De Boer WI, Houtsmuller AB, Izadifar V, et al. Expression and functions of EGF, FGF and TGFbeta-growth-factor family members and their receptors in invasive human transitional cell carcinoma cells. Int J Cancer 1997;71:284-91
52. O-charoenrat P, Rhys-Evans P, Court WJ, et al. Differential modulation of proliferation, matrix metalloproteinase expression and invasion of human head and neck squamous carcinoma cells by c-erbB ligands. Clin Exp Metastasis 1999;17:631-39
53. Cretu A, Fotos JS, Little BW, et al. Human and rat glioma growth, invasion, and vascularization in a novel chick embryo brain tumor model. Clin Exp Metastasis 2005;22:225-36
54. Xu FJ, Stack S, Boyer C, et al. Heregulin and agonistic anti-p185 (c-erbB2) antibodies inhibit proliferation but increase invasiveness of breast cancer cells that overexpress p185(c-erbB2): Increased invasiveness may contribute to poor prognosis. Clin Cancer Res 1997;3:1629-34
55. Yang H, Cheng X, Yao Q, et al. The promotive effects of thymosin beta4 on neuronal survival and neurite outgrowth by upregulating L1 expression. Neurochem Res 2008;33:2269-80
56. Berezowska S, Schlegel J. Targeting ErbB receptors in high-grade glioma. Curr Pharm Des 2011;17:2468-87
57. Dimitropoulos K, Giannopoulou E, Argyriou AA, et al. The effects of anti-VEGF receptor and anti-EGF RECEPTOR agents on glioma cell migration through implication of growth factors with integrins. Anticancer Res 2010;30:4987-92
58. Thiessen B, Stewart C, Tsao M, et al. A phase I/II trial of GW572016 (lapatinib) in recurrent glioblastoma multiforme: Clinical outcomes, pharmacokinetics and molecular correlation. Cancer Chemother Pharmacol 2010;65:353-61