Gamma-secretase represents a therapeutic target for the treatment of invasive glioma mediated by the p75 neurotrophin receptor

PLoS Biology

Volumn 6, Issue 11, 2008, Pages 2496-2511

  Wang, LiMei ^a,b,c   Rahn, Jennifer J ^a,b,c   Lun, XueQing ^a,c   Sun, Beichen ^a,c   Kelly, John J P ^a,d   Weiss, Samuel ^a,d   Robbins, Stephen M ^a,b,c   Forsyth, Peter A ^a,b,c   Senger, Donna L ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c Southern Alberta Cancer Research Institute   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA SECRETASE; GAMMA SECRETASE INHIBITOR; NEUROTROPHIN RECEPTOR P75; ENZYME INHIBITOR; HYBRID PROTEIN; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; SECRETASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN TUMOR; CANCER CELL; CANCER SURVIVAL; CANCER THERAPY; CONTROLLED STUDY; DRUG MECHANISM; EXPERIMENTAL MOUSE; FEMALE; GLIOMA; MOUSE; NONHUMAN; PROTEIN DEGRADATION; ANIMAL; BRAIN; DRUG ANTAGONISM; HUMAN; METABOLISM; PATHOPHYSIOLOGY; TUMOR INVASION;

ANIMALIA;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BRAIN; BRAIN NEOPLASMS; ENZYME INHIBITORS; GLIOMA; HUMANS; NEOPLASM INVASIVENESS; NERVE GROWTH FACTORS; RECEPTOR, NERVE GROWTH FACTOR; RECOMBINANT FUSION PROTEINS;

EID: 56849085242     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060289     Document Type: Article

References (98)

1. Scott JN, Rewcastle NB, Brasher PM, Fulton D, MacKinnon JA, et al. (1999) Which glioblastoma multiforme patient will become a long-term survivor? A population-based study. Ann Neurol 46: 183-188.
2. Senger D, Cairncross JG, Forsyth PA (2003) Long-term survivors of glioblastoma: statistical aberration or important unrecognized molecular subtype? Cancer J 9: 214-221.
3. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, et al. (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64: 7011-7021.
4. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, et al. (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100: 15178-15183.
5. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828.
6. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, et al. (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401.
7. Giese A, Loo MA, Tran N, Haskett D, Coons SW, et al. (1996) Dichotomy of astrocytoma migration and proliferation. Int J Cancer 67: 275-282.
8. Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21: 1624-1636.
9. Demuth T, Berens ME (2004) Molecular mechanisms of glioma cell migration and invasion. J Neurooncol 70: 217-228.
10. Joy AM, Beaudry CE, Tran NL, Ponce FA, Holz DR, et al. (2003) Migrating glioma cells activate the PI3-K pathway and display decreased susceptibility to apoptosis. J Cell Sci 116: 4409-4417.
11. Mariani L, Beaudry C, McDonough WS, Hoelzinger DB, Demuth T, et al. (2001) Glioma cell motility is associated with reduced transcription of proapoptotic and proliferation genes: a cDNA microarray analysis. J Neurooncol 53: 161-176.
12. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, et al. (2007) Molecular targets of glioma invasion. Cell Mol Life Sci 64: 458-478.
13. Freije WA, Castro-Vargas FE, Fang Z, Horvath S, Cloughesy T, et al. (2004) Gene expression profiling of gliomas strongly predicts survival. Cancer Res 64: 6503-6510.
14. Kleber S, Sancho-Martinez I, Wiestler B, Beisel A, Gieffers C, et al. (2008) Yes and PI3K bind CD95 to signal invasion of glioblastoma. Cancer Cell 13: 235-248.
15. Johnston AL, Lun X, Rahn JJ, Liacini A, Wang L, et al. (2007) The p75 neurotrophin receptor is a central regulator of glioma invasion. PLoS Biol 5: e212. doi:10.1371/journal.pbio.0050212
16. Reichardt LF (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361: 1545-1564.
17. Yamashita T, Tohyama M (2003) The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 6: 461-467.
18. Yamashita T, Tucker KL, Barde YA (1999) Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 24: 585-593.
19. Khursigara G, Bertin J, Yano H, Moffett H, DiStefano PS, et al. (2001) A prosurvival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor-interacting protein 2. J Neurosci 21: 5854-5863.
20. Mukai J, Shoji S, Kimura MT, Okubo S, Sano H, et al. (2002) Structure-function analysis of NADE: identification of regions that mediate nerve growth factor-induced apoptosis. J Biol Chem 277: 13973-13982.
21. Chittka A, Chao MV (1999) Identification of a zinc finger protein whose subcellular distribution is regulated by serum and nerve growth factor. Proc Natl Acad Sci U S A 96: 10705-10710.
22. Salehi AH, Roux PP, Kubu CJ, Zeindler C, Bhakar A, et al. (2000) NRAGE, a novel MAGE protein, interacts with the p75 neurotrophin receptor and facilitates nerve growth factor-dependent apoptosis. Neuron 27: 279-288.
23. Ye X, Mehlen P, Rabizadeh S, VanArsdale T, Zhang H, et al. (1999) TRAF family proteins interact with the common neurotrophin receptor and modulate apoptosis induction. J Biol Chem 274: 30202-30208.
24. Irie S, Hachiya T, Rabizadeh S, Maruyama W, Mukai J, et al. (1999) Functional interaction of Fas-associated phosphatase-1 (FAP-1) with p75(NTR) and their effect on NF-kappaB activation. FEBS Lett 460: 191-198.
25. Pardossi-Piquard R, Petit A, Kawarai T, Sunyach C, Alves da Costa C, et al. (2005) Presenilin-dependent transcriptional control of the Abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46: 541-554.
26. Kanning KC, Hudson M, Amieux PS, Wiley JC, Bothwell M, et al. (2003) Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J Neurosci 23: 5425-5436.
27. Majdan M, Lachance C, Gloster A, Aloyz R, Zeindler C, et al. (1997) Transgenic mice expressing the intracellular domain of the p75 neurotrophin receptor undergo neuronal apoptosis. J Neurosci 17: 6988-6998.
28. Podlesniy P, Kichev A, Pedraza C, Saurat J, Encinas M, et al. (2006) Pro-NGF from Alzheimer's disease and normal human brain displays distinctive abilities to induce processing and nuclear translocation of intracellular domain of p75NTR and apoptosis. Am J Pathol 169: 119-131.
29. Jung KM, Tan S, Landman N, Petrova K, Murray S, et al. (2003) Regulated intramembrane proteolysis of the p75 neurotrophin receptor modulates its association with the TrkA receptor. J Biol Chem 278: 42161-42169.
30. Frade JM (2005) Nuclear translocation of the p75 neurotrophin receptor cytoplasmic domain in response to neurotrophin binding. J Neurosci 25: 1407-1411.
31. Paul CE, Vereker E, Dickson KM, Barker PA (2004) A pro-apoptotic fragment of the p75 neurotrophin receptor is expressed in p75NTRExonIV null mice. J Neurosci 24: 1917-1923.
32. Ahmed Z, Mazibrada G, Seabright RJ, Dent RG, Berry M, et al. (2006) TACE-induced cleavage of NgR and p75NTR in dorsal root ganglion cultures disinhibits outgrowth and promotes branching of neurites in the presence of inhibitory CNS myelin. FASEB J 20: 1939-1941.
33. Domeniconi M, Zampieri N, Spencer T, Hilaire M, Mellado W, et al. (2005) MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46: 849-855.
34. Kenchappa RS, Zampieri N, Chao MV, Barker PA, Teng HK, et al. (2006) Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50: 219-232.
35. Oberg C, Li J, Pauley A, Wolf E, Gurney M, et al. (2001) The Notch intracellular domain is ubiquitinated and negatively regulated by the mammalian Sel-10 homolog. J Biol Chem 276: 35847-35853.
36. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, et al. (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385: 729-733.
37. Franzke CW, Tasanen K, Schacke H, Zhou Z, Tryggvason K, et al. (2002) Transmembrane collagen XVII, an epithelial adhesion protein, is shed from the cell surface by ADAMs. EMBO J 21: 5026-5035.
38. Moss ML, Rasmussen FH (2007) Fluorescent substrates for the proteinases ADAM17, ADAM10, ADAM8, and ADAM12 useful for high-throughput inhibitor screening. Anal Biochem 366: 144-148.
39. Zampieri N, Xu CF, Neubert TA, Chao MV (2005) Cleavage of p75 neurotrophin receptor by alpha-secretase and gamma-secretase requires specific receptor domains. J Biol Chem 280: 14563-14571.
40. Kopan R, Ilagan MX (2004) Gamma-secretase: proteasome of the membrane? Nat Rev Mol Cell Biol 5: 499-504.
41. Mumm JS, Kopan R (2000) Notch signaling: from the outside in. Dev Biol 228: 151-165.
42. Yan H, Chao MV (1991) Disruption of cysteine-rich repeats of the p75 nerve growth factor receptor leads to loss of ligand binding. J Biol Chem 266: 12099-12104.
43. Baldwin AN, Bitler CM, Welcher AA, Shooter EM (1992) Studies on the structure and binding properties of the cysteine-rich domain of rat low affinity nerve growth factor receptor (p75NGFR). J Biol Chem 267: 8352-8359.
44. Welcher AA, Bitler CM, Radeke MJ, Shooter EM (1991) Nerve growth factor binding domain of the nerve growth factor receptor. Proc Natl Acad Sci U S A 88: 159-163.
45. Johnson D, Lanahan A, Buck CR, Sehgal A, Morgan C, et al. (1986) Expression and structure of the human NGF receptor. Cell 47: 545-554.
46. Hempstead BL, Patil N, Thiel B, Chao MV (1990) Deletion of cytoplasmic sequences of the nerve growth factor receptor leads to loss of high affinity ligand binding. J Biol Chem 265: 9595-9598.
47. Hsu KC, Chao MV (1993) Differential expression and ligand binding properties of tumor necrosis factor receptor chimeric mutants. J Biol Chem 268: 16430-16436.
48. Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, et al. (2002) Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39: 193-206.
49. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, et al. (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11: 69-82.
50. Sanai N, Alvarez-Buylla A, Berger MS (2005) Neural stem cells and the origin of gliomas. N Engl J Med 353: 811-822.
51. Nakano I, Saigusa K, Kornblum HI (2008) BMPing off glioma stem cells. Cancer Cell 13: 3-4.
52. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, et al. (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391: 387-390.
53. Naruse S, Thinakaran G, Luo JJ, Kusiak JW, Tomita T, et al. (1998) Effects of PS1 deficiency on membrane protein trafficking in neurons. Neuron 21: 1213-1221.
54. Anderson JP, Chen Y, Kim KS, Robakis NK (1992) An alternative secretase cleavage produces soluble Alzheimer amyloid precursor protein containing a potentially amyloidogenic sequence. J Neurochem 59: 2328-2331.
55. De Strooper B, Annaert W, Cupers P, Saftig P, Craessaerts K, et al. (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398: 518-522.
56. Struhl G, Greenwald I (1999) Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398: 522-525.
57. Ikeuchi T, Sisodia SS (2003) The Notch ligands, Delta1 and Jagged2, are substrates for presenilin-dependent "gamma-secretase" cleavage. J Biol Chem 278: 7751-7754.
58. Ni CY, Murphy MP, Golde TE, Carpenter G (2001) gamma-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294: 2179-2181.
59. Lammich S, Okochi M, Takeda M, Kaether C, Capell A, et al. (2002) Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Abeta-like peptide. J Biol Chem 277: 44754-44759.
60. Murakami D, Okamoto I, Nagano O, Kawano Y, Tomita T, et al. (2003) Presenilin-dependent gamma-secretase activity mediates the intramembranous cleavage of CD44. Oncogene 22: 1511-1516.
61. Marambaud P, Shioi J, Serban G, Georgakopoulos A, Sarner S, et al. (2002) A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J 21: 1948-1956.
62. Aggarwal BB (2004) Nuclear factor-kappaB: the enemy within. Cancer Cell 6: 203-208.
63. Siemers E, Skinner M, Dean RA, Gonzales C, Satterwhite J, et al. (2005) Safety, tolerability, and changes in amyloid beta concentrations after administration of a gamma-secretase inhibitor in volunteers. Clin Neuropharmacol 28: 126-132.
64. Siemers ER, Dean RA, Friedrich S, Ferguson-Sells L, Gonzales C, et al. (2007) Safety, tolerability, and effects on plasma and cerebrospinal fluid amyloid-beta after inhibition of gamma-secretase. Clin Neuropharmacol 30: 317-325.
65. Siemers ER, Quinn JF, Kaye J, Farlow MR, Porsteinsson A, et al. (2006) Effects of a gamma-secretase inhibitor in a randomized study of patients with Alzheimer disease. Neurology 66: 602-604.
66. Logan A, Ahmed Z, Baird A, Gonzalez AM, Berry M (2006) Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 129: 490-502.
67. Urra S, Escudero CA, Ramos P, Lisbona F, Allende E, et al. (2007) TrkA receptor activation by nerve growth factor induces shedding of the p75 neurotrophin receptor followed by endosomal gamma-secretase-mediated release of the p75 intracellular domain. J Biol Chem 282: 7606-7615.
68. Cabrera N, Diaz-Rodriguez E, Becker E, Martin-Zanca D, Pandiella A (1996) TrkA receptor ectodomain cleavage generates a tyrosine-phosphorylated cell-associated fragment. J Cell Biol 132: 427-436.
69. Walmsley AR, McCombie G, Neumann U, Marcellin D, Hillenbrand R, et al. (2004) Zinc metalloproteinase-mediated cleavage of the human Nogo-66 receptor. J Cell Sci 117: 4591-4602.
70. Nyborg AC, Ladd TB, Jansen K, Kukar T, Golde TE (2006) Intramembrane proteolytic cleavage by human signal peptide peptidase like 3 and malaria signal peptide peptidase. FASEB J 20: 1671-1679.
71. Allinson TM, Parkin ET, Turner AJ, Hooper NM (2003) ADAMs family members as amyloid precursor protein alpha-secretases. J Neurosci Res 74: 342-352.
72. Huovila AP, Turner AJ, Pelto-Huikko M, Karkkainen I, Ortiz RM (2005) Shedding light on ADAM metalloproteinases. Trends Biochem Sci 30: 413-422.
73. Weskamp G, Schlondorff J, Lum L, Becherer JD, Kim TW, et al. (2004) Evidence for a critical role of the tumor necrosis factor alpha convertase (TACE) in ectodomain shedding of the p75 neurotrophin receptor (p75NTR). J Biol Chem 279: 4241-4249.
74. Zheng X, Jiang F, Katakowski M, Kalkanis SN, Hong X, et al. (2007) Inhibition of ADAM17 reduces hypoxia-induced brain tumor cell invasiveness. Cancer Sci 98: 674-684.
75. Zheng X, Jiang F, Katakowski M, Zhang X, Jiang H, et al. (2008) Sensitization of cerebral tissue in nude mice with photodynamic therapy induces ADAM17/TACE and promotes glioma cell invasion. Cancer Lett 265: 177-187.
76. Brown PD (2000) Ongoing trials with matrix metalloproteinase inhibitors. Expert Opin Investig Drugs 9: 2167-2177.
77. Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295: 2387-2392.
78. Held-Feindt J, Paredes EB, Blomer U, Seidenbecher C, Stark AM, et al. (2006) Matrix-degrading proteases ADAMTS4 and ADAMTS5 (disintegrins and metalloproteinases with thrombospondin motifs 4 and 5) are expressed in human glioblastomas. Int J Cancer 118: 55-61.
79. Kodama T, Ikeda E, Okada A, Ohtsuka T, Shimoda M, et al. (2004) ADAM12 is selectively overexpressed in human glioblastomas and is associated with glioblastoma cell proliferation and shedding of heparin-binding epidermal growth factor. Am J Pathol 165: 1743-1753.
80. Nakada M (2005) [Role of extracellular matrix degradation enzyme for glioma invasion]. Nippon Rinsho 63: 55-60.
81. Nuttall RK, Pennington CJ, Taplin J, Wheal A, Yong VW, et al. (2003) Elevated membrane-type matrix metalloproteinases in gliomas revealed by profiling proteases and inhibitors in human cancer cells. Mol Cancer Res 1: 333-345.
82. Rao JS (2003) Molecular mechanisms of glioma invasiveness: the role of proteases. Nat Rev Cancer 3: 489-501.
83. Wildeboer D, Naus S, Amy Sang QX, Bartsch JW, Pagenstecher A (2006) Metalloproteinase disintegrins ADAM8 and ADAM19 are highly regulated in human primary brain tumors and their expression levels and activities are associated with invasiveness. J Neuropathol Exp Neurol 65: 516-527.
84. Kimberly WT, LaVoie MJ, Ostaszewski BL, Ye W, Wolfe MS, et al. (2003) Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc Natl Acad Sci U S A 100: 6382-6387.
85. DeAngelo DJ, Stone RM, Heaney ML, Nimer SD, Paquette RL, et al. (2006) Phase 1 clinical results with tandutinib (MLN518), a novel FLT3 antagonist, in patients with acute myelogenous leukemia or high-risk myelodysplastic syndrome: safety, pharmacokinetics, and pharmacodynamics. Blood 108: 3674-3681.
86. Fryer CJ, Lamar E, Turbachova I, Kintner C, Jones KA (2002) Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev 16: 1397-1411.
87. Nam Y, Weng AP, Aster JC, Blacklow SC (2003) Structural requirements for assembly of the CSL.intracellular Notch1.Mastermind-like 1 transcriptional activation complex. J Biol Chem 278: 21232-21239.
88. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, et al. (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66: 7843-7848.
89. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A (2007) HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17: 165-172.
90. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, et al. (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9: 391-403.
91. Phillips TM, McBride WH, Pajonk F (2006) The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785.
92. Young KM, Merson TD, Sotthibundhu A, Coulson EJ, Bartlett PF (2007) p75 neurotrophin receptor expression defines a population of BDNF-responsive neurogenic precursor cells. J Neurosci 27: 5146-5155.
93. Yan Q, Johnson EM Jr (1989) Immunohistochemical localization and biochemical characterization of nerve growth factor receptor in adult rat brain. J Comp Neurol 290: 585-598.
94. Calza L, Giardino L, Pozza M, Bettelli C, Micera A, et al. (1998) Proliferation and phenotype regulation in the subventricular zone during experimental allergic encephalomyelitis: in vivo evidence of a role for nerve growth factor. Proc Natl Acad Sci U S A 95: 3209-3214.
95. Giuliani A, D'Intino G, Paradisi M, Giardino L, Calza L (2004) p75(NTR)-immunoreactivity in the subventricular zone of adult male rats: expression by cycling cells. J Mol Histol 35: 749-758.
96. Herrmann JL, Menter DG, Hamada J, Marchetti D, Nakajima M, et al. (1993) Mediation of NGF-stimulated extracellular matrix invasion by the human melanoma low-affinity p75 neurotrophin receptor: melanoma p75 functions independently of trkA. Mol Biol Cell 4: 1205-1216.
97. Menter DG, Herrmann JL, Marchetti D, Nicolson GL (1994) Involvement of neurotrophins and growth factors in brain metastasis formation. Invasion Metastasis 14: 372-384.
98. Shonukan O, Bagayogo I, McCrea P, Chao M, Hempstead B (2003) Neurotrophin-induced melanoma cell migration is mediated through the actin-bundling protein fascin. Oncogene 22: 3616-3623.