ProBDNF and its receptors are upregulated in glioma and inhibit the growth of glioma cells in vitro

Neuro-Oncology

Volumn 15, Issue 8, 2013, Pages 990-1007

  Xiong, Jing ^a   Zhou, Li ^a   Yang, Miao ^b   Lim, Yoon ^b   Zhu, Yu Hong ^a   Fu, Deng Li ^a   Li, Zhi Wei ^a   Zhong, Jin Hua ^b   Xiao, Zhi Cheng ^a,c   Zhou, Xin Fu ^a,b  

^a KUNMING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

brain derived neurotrophic factor; glioma; human; p75NTR; proBDNF; sortilin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROTROPHIN RECEPTOR P75; SORTILIN;

ADULT; AGED; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELLULAR DISTRIBUTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; WESTERN BLOTTING;

BRAIN-DERIVED NEUROTROPHIC FACTOR; GLIOMA; HUMAN; P75NTR; PROBDNF; SORTILIN;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADULT; APOPTOSIS; BLOTTING, WESTERN; BRAIN; BRAIN NEOPLASMS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CASE-CONTROL STUDIES; CELL PROLIFERATION; FEMALE; FOLLOW-UP STUDIES; GLIOMA; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MIDDLE AGED; NEOPLASM GRADING; PROGNOSIS; PROTEIN PRECURSORS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, NERVE GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 84880671154     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/not039     Document Type: Article

References (85)

1. Kesari S, Stiles CD. The bad seed:PDGFreceptors link adult neural progenitors to glioma stem cells. Neuron. 2006;51:151-153. (Pubitemid 44041869)
2. Boring CC, Squires TS, Tong T, Montgomery S. Cancer statistics, 1994. CA: Cancer J Clin. 1994;44:7-26.
3. Brada M, Sharpe G, Rajan B, et al. Modifying radical radiotherapy in high grade gliomas; shortening the treatment time through acceleration. Int J Rad Oncol Biol Phys. 1999;43:287-292. (Pubitemid 29091466)
4. Winger MJ, Macdonald DR, Cairncross JG. Supratentorial anaplastic gliomas in adults. The prognostic importance of extent of resection and prior low-grade glioma. J Neurosurg. 1989;71:487-493. (Pubitemid 19244261)
5. Shibamoto Y, Yamashita J, Takahashi M, Yamasaki T, Kikuchi H, Abe M. Supratentorial malignant glioma: an analysis of radiation therapy in 178 cases. Radiother Oncol. 1990;18:9-17. (Pubitemid 20174440)
6. Reni M, Cozzarini C, Ferreri AJ, et al. A retrospective analysis of postradiation chemotherapyin 133 patients with glioblastoma multiforme. Cancer Invest. 2000;18:510-515. (Pubitemid 30485666)
7. Brada M, Baumert B. Focal fractionated conformal stereotactic boost following conventional radiotherapy of high-grade gliomas: a randomized phase III study. A joint study of the EORTC (22972) and the MRC (BR10). Front Rad Ther Oncol. 1999;33:241-243.
8. Bleehen NM, Stenning SP. A Medical Research Council trial of two radiotherapy doses in the treatment of grades 3 and 4 astrocytoma. The Medical Research Council Brain Tumour Working Party. Br J Cancer. 1991;64:769-774.
9. Holland EC. Gliomagenesis: genetic alterations and mouse models. Nat Rev Genet. 2001;2:120-129. (Pubitemid 33674003)
10. Frei K. Genes and pathways driving glioblastomas in humans and murine disease models. Neurosurg Rev. 2003;26:161.
11. Bachoo RM, Maher EA, Ligon KL, et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell. 2002;1:269-277. (Pubitemid 41039151)
12. Uhrbom L, Dai C, Celestino JC, Rosenblum MK, Fuller GN, Holland EC. Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res. 2002;62:5551-5558.
13. Bajenaru ML, Hernandez MR, Perry A, et al. Optic nerve glioma in mice requires astrocyte Nf1 gene inactivation and Nf1 brain heterozygosity. Cancer Res. 2003;63:8573-8577. (Pubitemid 38064027)
14. Kwon CH, Zhao D, Chen J, et al. PTEN haploinsufficiency accelerates formation of high-grade astrocytomas. Cancer Res. 2008;68:3286-3294.
15. Merlo A. Genes and pathways driving glioblastomas in humans and murine disease models. Neurosurg Rev. 2003;26:145-158. (Pubitemid 36835031)
16. de la Iglesia N, Puram SV, Bonni A. STAT3 regulation of glioblastoma path-ogenesis. Curr Mol Med. 2009;9:580-590.
17. Bernstein JJ, Woodard CA. Glioblastoma cellsdonot intravasate into blood vessels. Neurosurgery. 1995;36:124-132, discussion 132.
18. Johnston AL, Lun X, Rahn JJ, et al. The p75 neurotrophin receptor is a central regulator of glioma invasion. PLoS Biol. 2007;5:e212.
19. Juric DM, Miklic S, Carman-Krzan M. Monoaminergic neuronal activity up-regulates BDNF synthesis in cultured neonatal rat astrocytes. Brain Res. 2006;1108:54-62. (Pubitemid 44278004)
20. Elmariah SB, Hughes EG, Oh EJ, Balice-Gordon RJ. Neurotrophinsignaling among neurons and glia during formation of tripartite synapses. Neuron Glia Biol. 2005;1:1-11.
21. Miklic S, Juric DM, Carman-Krzan M. Differences in the regulation of BDNF and NGF synthesis in cultured neonatal rat astrocytes. Int J Dev Neurosci. 2004;22:119-130. (Pubitemid 38597127)
22. Seidah NG, Chretien M. Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res. 1999;848:45-62. (Pubitemid 30001653)
23. Barker PA. Whither proBDNF? Nat Neurosci. 2009;12:105-106.
24. Zhou XF, Song XY, Zhong JH, Barati S, Zhou FH, Johnson SM. Distribution and localization of pro-brain-derived neurotrophic factor-like immunore-activity in the peripheral and central nervous system of the adult rat. J Neurochem. 2004;91:704-715. (Pubitemid 39431164)
25. Pang PT, Teng HK, Zaitsev E, et al. Cleavage of pro BDNF byt PA/plasminis essential for long-term hippocampal plasticity. Science. 2004;306: 487-491. (Pubitemid 39372449)
26. Teng HK, Teng KK, Lee R, et al. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci. 2005;25:5455-5463. (Pubitemid 40770927)
27. Kenchappa RS, Zampieri N, Chao MV, et al. Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron. 2006;50:219-232.
28. Fan YJ, Wu LL, Li HY, Wang YJ, Zhou XF. Differential effects ofpro-BDNF on sensory neurons after sciatic nerve transection in neonatal rats. Eur J Neurosci. 2008;27:2380-2390. (Pubitemid 351590919)
29. Woo NH, Teng HK, Siao CJ, et al. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat Neurosci. 2005;8: 1069-1077. (Pubitemid 41061518)
30. Lu B. Pro-region of neurotrophins: role in synaptic modulation. Neuron. 2003;39:735-738. (Pubitemid 37088086)
31. Lu B, Pang PT, Woo NH. Theyin andyangofneurotrophin action. Nat Rev Neurosci. 2005;6:603-614.
32. Koshimizu H, Hazama S, Hara T, Ogura A, Kojima M. Distinct signaling pathways of precursor BDNF and mature BDNF in cultured cerebellar granule neurons. Neurosci Lett. 2010;473:229-232.
33. Sun Y, Lim Y, Li F, et al. ProBDNF collapses neurite outgrowth of primary neurons by activating RhoA. PLoS One. 2012;7:e35883.
34. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathologica. 2007;114:97-109. (Pubitemid 47103521)
35. Gimenez M, Souza VC, Izumi C, et al. Proteomic analysis of low- to highgrade astrocytomas reveals an alteration of the expression level of raf kinase inhibitor protein and nucleophosmin. Proteomics. 2010;10: 2812-2821.
36. Moss SF, Lee JW, Sabo E, et al. Decreased expression of gastrokine 1 and the trefoil factor interacting protein TFIZ1/GKN2 in gastric cancer: influence of tumor histology and relationship to prognosis. Clin Cancer Res. 2008;14:4161-4167.
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25:402-408. (Pubitemid 34164012)
38. Keifer J, Sabirzhanov BE, Zheng Z, Li W, Clark TG. Cleavage of proBDNF to BDNF by a tolloid-like metalloproteinase is required for acquisition of in vitro eyeblink classical conditioning. J Neurosci. 2009;29:14956-14964.
39. Kelly KJ, Sandoval RM, Dunn KW, Molitoris BA, Dagher PC. A novel method to determine specificity and sensitivity of the TUNEL reaction in the quantitation of apoptosis. Am J Cell Physiol. 2003;284: C1309-C1318. (Pubitemid 36457412)
40. Xu ZQ, Sun Y, Li H Y, Lim Y, Zhong JH, Zhou XF. Endogenous proBDNF isa negative regulator of migration of cerebellar granule cells in neonatal mice. Eur J Neurosci. 2011;33:1376-1384.
41. Lin WL, Liang WH, Lee YJ, Chuang SK, Tseng TH. Antitumor progression potential of caffeic acid phenethyl ester involving p75(NTR) in C6 glioma cells. Chem-Biol Interact. 2010;188:607-615.
42. Raju TR, Bignami A, Dahl D. Glial fibrillary acidic protein in monolayer cultures of C-6 glioma cells: effect of aging and dibutyryl cyclic AMP. Brain Res. 1980;200:225-230. (Pubitemid 10061612)
43. Tabuchi K, Furuta T, Norikane H, Tsuboi M, Moriya Y, Nishimoto A. Evaluation of the drug-induced morphological differentiation of rat glioma cells (C-6) from the aspects of S-100 protein level and con A binding pattern. J Neurol Sci. 1981;51:119-130. (Pubitemid 11078509)
44. Weis C, Wiesenhofer B, Humpel C. Nerve growth factor playsa divergent role in mediating growth of rat C6 glioma cells via binding to the p75 neu-rotrophin receptor. J Neuro-Oncol. 2002;56:59-67. (Pubitemid 34256619)
45. Lichtor T, Yamamoto H, Gurney ME. Gene expression of neurotrophic factors in human brain tumors. Mol Cell Neurosci. 1991;2:168-171. (Pubitemid 121005244)
46. Hamel W, Westphal M, Szonyi E, Escandon E, Nikolics K. Neurotrophin gene expression by cell lines derived from human gliomas. J Neurosci Res. 1993;34:147-157. (Pubitemid 23037315)
47. Fahnestock M, Garzon D, Holsinger RM, Michalski B. Neurotrophic factors and Alzheimer's disease: arewe focusingon the wrong molecule? J Neural Trans Suppl. 2002;62:241-252. (Pubitemid 37046668)
48. Peng S, Wuu J, Mufson EJ, Fahnestock M. Precursorformofbrain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease. J Neurochem. 2005;93:1412-1421. (Pubitemid 40853264)
49. Dieni S, Matsumoto T, Dekkers M, et al. BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J Cell Biol. 2012;196:775-788.
50. Nykjaer A, Lee R, Teng KK, et al. Sortilin is essential for proNGF-induced neuronal cell death. Nature. 2004;427:843-848. (Pubitemid 38297746)
51. Yang M, Lim Y, Li X, Zhong JH, Zhou XF. Precursorofbrain-derivedneuro- trophic factor (proBDNF) forms a complex with Huntingtin-associated protein-1 (HAP1) and sortilin that modulates proBDNF trafficking, degradation, and processing. J Biol Chem. 2011;286:16272-16284.
52. Yusubalieva GM, Baklaushev VP, Gurina OI, Tsitrin EB, Chekhonin VP. Immunochemical analysis of glial fibrillary acidic protein as a tool to assess astroglial reaction in experimental C6 glioma. Bull Exper Biol Med. 2010;149:125-130.
53. He S, Zhu W, Zhou Y, et al. Transcriptional and post-transcriptional down-regulation of cyclin D1 contributes to C6 glioma cell differentiation induced by forskolin. J Cell Biochem. 2011;112:2241-2249.
54. Akil H, Perraud A, Melin C, Jauberteau MO, Mathonnet M. Fine-tuning roles of endogenous brain-derived neurotrophic factor. TrkB and sortilin in colorectal cancer cell survival. PLoS One. 2011;6:e25097.
55. Winkler F, Kienast Y, Fuhrmann M, et al. Imaging glioma cell invasion in vivo reveals mechanisms of dissemination and peritumoral angiogenesis. Glia. 2009;57:1306-1315.
56. Goebell E, Paustenbach S, Vaeterlein O, et al. Low-grade and anaplastic gliomas: differences in architecture evaluated with diffusion-tensor MR imaging. Radiology. 2006;239:217-222.
57. Wang L, Rahn JJ, Lun X, et al. Gamma-secretase represents atherapeutic target for the treatment ofinvasive glioma mediatedby the p75 neurotro-phin receptor. PLoS Biol. 2008;6:e289.
58. Gehler S, Gallo G, Veien E, Letourneau PC. p75 neurotrophin receptor signaling regulates growth cone filopodial dynamics through modulating RhoA activity. J Neurosci. 2004;24:4363-4372. (Pubitemid 38608147)
59. Hu Y, Wang YD, Guo T, et al. Identification of brain-derived neurotrophic factor as a novel angiogenic protein in multiple myeloma. Cancer Genet Cytogenet. 2007;178:1-10. (Pubitemid 47419033)
60. Fauchais AL, Lalloue F, Lise MC, et al. Role of endogenous brain-derived neurotrophic factor and sortilin in B cell survival. J Immunol. 2008; 181:3027-3038.
61. Nakagawara A, Azar CG, Scavarda NJ, Brodeur GM. Expression and function of TRK-B and BDNF in human neuroblastomas. Mol Cell Biol. 1994;14:759-767.
62. Stephan H, Zakrzewski JL, Boloni R, Grasemann C, Lohmann DR, Eggert A. Neurotrophin receptor expression in human primary retinoblastomas and retinoblastoma cell lines. Pediatr Blood Cancer. 2008;50:218-222.
63. Pickhard AC, Margraf J, Knopf A, et al. Inhibition of radiation induced migration of human head andneck squamous cell carcinoma cells by blocking of EGF receptor pathways. BMC Cancer. 2011;11:388.
64. Ji H, Wang J, Nika H, et al. EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-catenin from beta-catenin and transactivation of beta-catenin. Mol Cell. 2009;36:547-559.
65. Nazarenko I, Hede SM, He X, et al. PDGF and PDGF receptors in glioma. Upsala J Med Sci. 2012;117:99-112.
66. Lokker NA, Sullivan CM, Hollenbach SJ, Israel MA, Giese NA. Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res. 2002;62:3729-3735. (Pubitemid 34728854)
67. Ranza E, Facoetti A, Morbini P, Benericetti E, Nano R. Exogenous platelet-derived growth factor (PDGF) induces human astrocytoma cell line proliferation. Anticancer Res. 2007;27:2161-2166. (Pubitemid 47228049)
68. Ritch PS, Carroll SL, Sontheimer H. Neuregulin-1 enhances survival of human astrocytic glioma cells. Glia. 2005;51:217-228. (Pubitemid 41297428)
69. Ritch PA, Carroll SL, Sontheimer H. Neuregulin-1 enhances motility and migration of human astrocytic glioma cells. J Biol Chem. 2003;278:20971-20978. (Pubitemid 36806406)
70. Okajima K, Ohta Y. [Diagnostic imaging of high-grade astrocytoma: heterogeneity of clinical manifestation, image characteristics, and histopath-ological findings]. Shinkei Kenkyu No Shinpo [Brain Nerve]. 2012;64:1151-1157.
71. Brell M, Ibanez J, Felpete A, Burguera B, Frontera M, Couce ME. Quantitative analysis of matrix metalloproteinase-2 mRNA expression in central and peripheral regions of gliomas. Brain Tumor Pathol. 2011;28:137-144.
72. Kruttgen A, Schneider I, Weis J. The dark side of the NGF family: neuro-trophins in neoplasias. Brain Pathol. 2006;16:304-310.
73. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-674.
74. Mentlein R, Hattermann K, Held-Feindt J. Lost indisruption: role of proteases in glioma invasion and progression. Biochim Biophys Acta. 2012;1825:178-185.
75. Levicar N, Nuttall RK, Lah TT. Proteases in brain tumour progression. Acta Neurochir. 2003;145:825-838. (Pubitemid 37204559)
76. Salmaggi A, Croci D, Prina P, et al. Production and post-surgical modification of VEGF, tPA and PAI-1 in patients with glioma. Cancer Biol Ther. 2006;5:204-209. (Pubitemid 43327540)
77. Akai T, Niiya K, Sakuragawa N, Iizuka H, Endo S. Modulation of tissue-type plasminogen activator expression by platelet activating factor in human glioma cells. J Neuro-Oncol. 2002;59:193-198. (Pubitemid 35021568)
78. Hagemann C, Anacker J, Ernestus RI, Vince GH. A complete compilation of matrix metalloproteinase expression in human malignant gliomas. World J Clin Oncol. 2012;3:67-79.
79. Takano S, Mashiko R, Osuka S, Ishikawa E, Ohneda O, Matsumura A. Detection of failure of bevacizumab treatment for malignant glioma based on urinary matrix metalloproteinase activity. Brain Tumor Pathol. 2010;27:89-94.
80. Nakabayashi H, Yawata T, Shimizu K. Anti-invasive and antiangiogenic effects of MMI-166 on malignant glioma cells. BMC Cancer. 2010; 10:339.
81. Sawaya R, Ramo OJ, Shi ML, Mandybur G. Biological significance of tissue plasminogen activator content in brain tumors. J Neurosurg. 1991; 74:480-486.
82. Bindal AK, Hammoud M, Shi WM, Wu SZ, Sawaya R, Rao JS. Prognostic significance of proteolytic enzymes in human brain tumors. J Neuro-Oncol. 1994;22:101-110.
83. Sandstrom M, Johansson M, Sandstrom J, Bergenheim AT, Henriksson R. Expression of the proteolytic factors, tPAand uPA, PAI-1 and VEGF during malignant glioma progression. Int J Dev Neurosci. 1999;17:473-481. (Pubitemid 29421834)
84. Marcinkiewicz M, Seidah NG, Chretien M. Implications of the subtilisin/kexin-like precursor convertases in the development and function of nervous tissues. Acta Neurobiol Exper. 1996;56:287-298. (Pubitemid 26127716)
85. Yoshida T, Ishikawa M, Niitsu T, et al. Decreased serum levels of mature brain-derived neurotrophic factor (BDNF), but not its precursor proBDNF, in patients with major depressive disorder. PLoS One. 2012;7:e42676.