Upregulation of APP, ADAM10 and ADAM17 in the denervated mouse dentate gyrus

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Turco, Domenico Del ^a   Schlaudraff, Jessica ^a   Bonin, Michael ^b   Deller, Thomas ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM10 ENDOPEPTIDASE; ADAM17 ENDOPEPTIDASE; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; MESSENGER RNA; METALLOPROTEINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DAMAGE; CONTROLLED STUDY; DENERVATION; DENTATE GYRUS; GENE EXPRESSION; GRANULE CELL; MACROGLIA; MALE; MICROGLIA; MOUSE; NONHUMAN; PROTEIN PROCESSING; UPREGULATION;

ADAM PROTEINS; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASTROCYTES; DENERVATION; DENTATE GYRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; MEMBRANE PROTEINS; MICE; RNA, MESSENGER; UP-REGULATION;

EID: 84896751574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084962     Document Type: Article

References (73)

1. Aydin D, Weyer SW, Muller UC (2012) Functions of the APP gene family in the nervous system: insights from mouse models. Exp Brain Res 217: 423-434.
2. O'Brien RJ, Wong PC (2011) Amyloid precursor protein processing and Alzheimer's disease. Annu Rev Neurosci 34: 185-204.
3. Zhang H, Ma Q, Zhang YW, Xu H (2012) Proteolytic processing of Alzheimer's beta-amyloid precursor protein. J Neurochem 120 Suppl 1: 9-21.
4. Muller UC, Zheng H (2012) Physiological functions of APP family proteins. Cold Spring Harb Perspect Med 2: a006288.
5. Turner PR, O'Connor K, Tate WP, Abraham WC (2003) Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog Neurobiol 70: 1-32. (Pubitemid 36966639)
6. Ring S, Weyer SW, Kilian SB, Waldron E, Pietrzik CU, et al. (2007) The secreted beta-amyloid precursor protein ectodomain APPs alpha is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice. J Neurosci 27: 7817-7826. (Pubitemid 47093823)
7. Mattson MP, Guo ZH, Geiger JD (1999) Secreted form of amyloid precursor protein enhances basal glucose and glutamate transport and protects against oxidative impairment of glucose and glutamate transport in synaptosomes by a cyclic GMP-mediated mechanism. J Neurochem 73: 532-537. (Pubitemid 29339825)
8. Mattson MP, Cheng B, Culwell AR, Esch FS, Lieberburg I, et al. (1993) Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the beta-amyloid precursor protein. Neuron 10: 243-254. (Pubitemid 23079546)
9. Kogel D, Deller T, Behl C (2012) Roles of amyloid precursor protein family members in neuroprotection, stress signaling and aging. Exp Brain Res 217: 471-479.
10. Copanaki E, Chang S, Vlachos A, Tschape JA, Muller UC, et al. (2010) sAPPalpha antagonizes dendritic degeneration and neuron death triggered by proteasomal stress. Mol Cell Neurosci 44: 386-393.
11. Goodman Y, Mattson MP (1994) Secreted forms of beta-amyloid precursor protein protect hippocampal neurons against amyloid beta-peptide-induced oxidative injury. Exp Neurol 128: 1-12.
12. Mattson MP, Scheff SW (1994) Endogenous neuroprotection factors and traumatic brain injury: mechanisms of action and implications for therapy. J Neurotrauma 11: 3-33. (Pubitemid 24094190)
13. Corrigan F, Vink R, Blumbergs PC, Masters CL, Cappai R, et al. (2012) sAPPalpha rescues deficits in amyloid precursor protein knockout mice following focal traumatic brain injury. J Neurochem 122: 208-220.
14. Corrigan F, Vink R, Blumbergs PC, Masters CL, Cappai R, et al. (2012) Evaluation of the effects of treatment with sAPPalpha on functional and histological outcome following controlled cortical impact injury in mice. Neurosci Lett 515: 50-54.
15. Corrigan F, Vink R, Blumbergs PC, Masters CL, Cappai R, et al. (2012) Characterisation of the effect of knockout of the amyloid precursor protein on outcome following mild traumatic brain injury. Brain Res 1451: 87-99.
16. Hiltunen M, van Groen T, Jolkkonen J (2009) Functional roles of amyloid-beta protein precursor and amyloid-beta peptides: evidence from experimental studies. J Alzheimers Dis 18: 401-412.
17. Van Den Heuvel C, Thornton E, Vink R (2007) Traumatic brain injury and Alzheimer's disease: a review. Prog Brain Res 161: 303-316. (Pubitemid 47017411)
18. Murakami N, Yamaki T, Iwamoto Y, Sakakibara T, Kobori N, et al. (1998) Experimental brain injury induces expression of amyloid precursor protein, which may be related to neuronal loss in the hippocampus. Journal of Neurotrauma 15: 993-1003. (Pubitemid 28530210)
19. Uryu K, Chen XH, Martinez D, Browne KD, Johnson VE, et al. (2007) Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans. Exp Neurol 208: 185-192. (Pubitemid 350101496)
20. Steinbach JP, Muller U, Leist M, Li ZW, Nicotera P, et al. (1998) Hypersensitivity to seizures in beta-amyloid precursor protein deficient mice. Cell Death Differ 5: 858-866. (Pubitemid 28484396)
21. Thornton E, Vink R, Blumbergs PC, Van Den Heuvel C (2006) Soluble amyloid precursor protein alpha reduces neuronal injury and improves functional outcome following diffuse traumatic brain injury in rats. Brain Res 1094: 38-46. (Pubitemid 43927608)
22. Steward O (1991) Synapse replacement on cortical neurons following denervation. Cerebral cortex 9: 81-132.
23. Deller T, Frotscher M (1997) Lesion-induced plasticity of central neurons: sprouting of single fibres in the rat hippocampus after unilateral entorhinal cortex lesion. Prog Neurobiol 53: 687-727. (Pubitemid 28023418)
24. Deller T, Del Turco D, Rappert A, Bechmann I (2007) Structural reorganization of the dentate gyrus following entorhinal denervation: species differences between rat and mouse. Prog Brain Res 163: 501-528. (Pubitemid 47321949)
25. Endres K, Fahrenholz F (2012) Regulation of alpha-secretase ADAM10 expression and activity. Exp Brain Res 217: 343-352.
26. Postina R (2012) Activation of alpha-secretase cleavage. J Neurochem 120 Suppl 1: 46-54.
27. Yang P, Baker KA, Hagg T (2006) The ADAMs family: coordinators of nervous system development, plasticity and repair. Prog Neurobiol 79: 73-94. (Pubitemid 44247280)
28. Saftig P, Reiss K (2011) The "A Disintegrin And Metalloproteases" ADAM10 and ADAM17: novel drug targets with therapeutic potential? Eur J Cell Biol 90: 527-535.
29. Vassar R, Kandalepas PC (2011) The beta-secretase enzyme BACE1 as a therapeutic target for Alzheimer's disease. Alzheimers Res Ther 3: 20.
30. Fluhrer R, Multhaup G, Schlicksupp A, Okochi M, Takeda M, et al. (2003) Identification of a beta-secretase activity, which truncates amyloid beta-peptide after its presenilin-dependent generation. J Biol Chem 278: 5531-5538. (Pubitemid 36800794)
31. Walsh DM, Minogue AM, Sala Frigerio C, Fadeeva JV, Wasco W, et al. (2007) The APP family of proteins: similarities and differences. Biochem Soc Trans 35: 416-420. (Pubitemid 46596519)
32. Heber S, Herms J, Gajic V, Hainfellner J, Aguzzi A, et al. (2000) Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J Neurosci 20: 7951-7963.
33. Del Turco D, Woods AG, Gebhardt C, Phinney AL, Jucker M, et al. (2003) Comparison of commissural sprouting in the mouse and rat fascia dentata after entorhinal cortex lesion. Hippocampus 13: 685-699. (Pubitemid 37098757)
34. Schmued LC, Stowers CC, Scallet AC, Xu L (2005) Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res 1035: 24-31. (Pubitemid 40248533)
35. Vuksic M, Del Turco D, Vlachos A, Schuldt G, Muller CM, et al. (2011) Unilateral entorhinal denervation leads to long-lasting dendritic alterations of mouse hippocampal granule cells. Exp Neurol 230: 176-185.
36. Frank S, Burbach GJ, Bonin M, Walter M, Streit W, et al. (2008) TREM2 is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56: 1438-1447.
37. Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press: San Diego, CA, USA.
38. Burbach GJ, Dehn D, Del Turco D, Deller T (2003) Quantification of layerspecific gene expression in the hippocampus: effective use of laser microdissection in combination with quantitative RT-PCR. Journal of Neuroscience Methods 131: 83-91. (Pubitemid 37491463)
39. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, et al. (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7: 3.
40. Deller T, Haas CA, Frotscher M (2000) Reorganization of the rat fascia dentata after a unilateral entorhinal cortex lesion. Role of the extracellular matrix. Ann N Y Acad Sci 911: 207-220. (Pubitemid 30462084)
41. Steward O, Kelley MS, Torre ER (1993) The process of reinnervation in the dentate gyrus of adult rats: temporal relationship between changes in the levels of glial fibrillary acidic protein (GFAP) and GFAP mRNA in reactive astrocytes. Exp Neurol 124: 167-183. (Pubitemid 24041764)
42. Jensen MB, Hegelund IV, Poulsen FR, Owens T, Zimmer J, et al. (1999) Microglial reactivity correlates to the density and the myelination of the anterogradely degenerating axons and terminals following perforant path denervation of the mouse fascia dentata. Neuroscience 93: 507-518. (Pubitemid 29329455)
43. Finsen B, Jensen MB, Lomholt ND, Hegelund IV, Poulsen FR, et al. (1999) Axotomy-induced glial reactions in normal and cytokine transgenic mice. Adv Exp Med Biol 468: 157-171.
44. Nielsen HH, Ladeby R, Drojdahl N, Peterson AC, Finsen B (2006) Axonal degeneration stimulates the formation of NG2+ cells and oligodendrocytes in the mouse. Glia 54: 105-115. (Pubitemid 44078132)
45. Gall C, Rose G, Lynch G (1979) Proliferative and migratory activity of glial cells in the partially deafferented hippocampus. J Comp Neurol 183: 539-549.
46. Warren KM, Reeves TM, Phillips LL (2012) MT5-MMP, ADAM-10, and Ncadherin act in concert to facilitate synapse reorganization after traumatic brain injury. J Neurotrauma 29: 1922-1940.
47. Skovronsky DM, Fath S, Lee VM, Milla ME (2001) Neuronal localization of the TNFalpha converting enzyme (TACE) in brain tissue and its correlation to amyloid plaques. J Neurobiol 49: 40-46.
48. Kawaja MD, Gage FH (1991) Reactive astrocytes are substrates for the growth of adult CNS axons in the presence of elevated levels of nerve growth factor. Neuron 7: 1019-1030.
49. Gage FH, Olejniczak P, Armstrong DM (1988) Astrocytes are important for sprouting in the septohippocampal circuit. Exp Neurol 102: 2-13.
50. Steward O (1994) Cholinergic sprouting is blocked by repeated induction of electroconvulsive seizures, a manipulation that induces a persistent reactive state in astrocytes. Exp Neurol 129: 103-111. (Pubitemid 24344161)
51. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32: 421-431.
52. Faissner A, Pyka M, Geissler M, Sobik T, Frischknecht R, et al. (2010) Contributions of astrocytes to synapse formation and maturation-Potential functions of the perisynaptic extracellular matrix. Brain Res Rev 63: 26-38.
53. Haas CA, Rauch U, Thon N, Merten T, Deller T (1999) Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19: 9953-9963. (Pubitemid 30226667)
54. Thon N, Haas CA, Rauch U, Merten T, Fassler R, et al. (2000) The chondroitin sulphate proteoglycan brevican is upregulated by astrocytes after entorhinal cortex lesions in adult rats. European Journal of Neuroscience 12: 2547-2558. (Pubitemid 30497048)
55. Reeves TM, Prins ML, Zhu J, Povlishock JT, Phillips LL (2003) Matrix metalloproteinase inhibition alters functional and structural correlates of deafferentation-induced sprouting in the dentate gyrus. J Neurosci 23: 10182-10189. (Pubitemid 37444594)
56. Soba P, Eggert S, Wagner K, Zentgraf H, Siehl K, et al. (2005) Homo-and heterodimerization of APP family members promotes intercellular adhesion. EMBO J 24: 3624-3634. (Pubitemid 41509369)
57. Wang Z, Wang B, Yang L, Guo Q, Aithmitti N, et al. (2009) Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. J Neurosci 29: 10788-10801.
58. Itoh T, Satou T, Nishida S, Tsubaki M, Hashimoto S, et al. (2009) Expression of amyloid precursor protein after rat traumatic brain injury. Neurol Res 31: 103-109.
59. Van den Heuvel C, Blumbergs PC, Finnie JW, Manavis J, Jones NR, et al. (1999) Upregulation of amyloid precursor protein messenger RNA in response to traumatic brain injury: an ovine head impact model. Exp Neurol 159: 441-450. (Pubitemid 29485230)
60. Mortimer JA, Van Duijn CM, Chandra V, Fratiglioni L, Graves AB, et al. (1991) Head Trauma as a Risk Factor for Alzheimer's Disease: A Collaborative Re-Analysis of Case-Control Studies. International Journal of Epidemiology 20: S28-S35.
61. Ramirez MJ, Heslop KE, Francis PT, Rattray M (2001) Expression of amyloid precursor protein, tau and presenilin RNAs in rat hippocampus following deafferentation lesions. Brain Res 907: 222-232. (Pubitemid 32595531)
62. Fahrenholz F (2007) Alpha-secretase as a therapeutic target. Current Alzheimer Research 4: 412-417. (Pubitemid 47416634)
63. Fahrenholz F, Tippmann F, Endres K (2010) Retinoids as a perspective in treatment of Alzheimer's disease. Neurodegener Dis 7: 190-192.
64. Fahrenholz F, Postina R (2006) Alpha-secretase activation-an approach to Alzheimer's disease therapy. Neurodegener Dis 3: 255-261. (Pubitemid 44600312)
65. Prinzen C, Trumbach D, Wurst W, Endres K, Postina R, et al. (2009) Differential gene expression in ADAM10 and mutant ADAM10 transgenic mice. BMC Genomics 10: 66.
66. Postina R, Schroeder A, Dewachter I, Bohl J, Schmitt U, et al. (2004) A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J Clin Invest 113: 1456-1464. (Pubitemid 39071701)
67. Freese C, Garratt AN, Fahrenholz F, Endres K (2009) The effects of alphasecretase ADAM10 on the proteolysis of neuregulin-1. FEBS J 276: 1568-1580.
68. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, et al. (1999) Betasecretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286: 735-741.
69. Vassar R, Kovacs DM, Yan R, Wong PC (2009) The beta-secretase enzyme BACE in health and Alzheimer's disease: regulation, cell biology, function, and therapeutic potential. J Neurosci 29: 12787-12794.
70. Zhao J, O'Connor T, Vassar R (2011) The contribution of activated astrocytes to Abeta production: implications for Alzheimer's disease pathogenesis. J Neuroinflammation 8: 150.
71. Obregon D, Hou H, Deng J, Giunta B, Tian J, et al. (2012) Soluble amyloid precursor protein-alpha modulates beta-secretase activity and amyloid-beta generation. Nat Commun 3: 777.
72. Tian Y, Crump CJ, Li YM (2010) Dual role of alpha-secretase cleavage in the regulation of gamma-secretase activity for amyloid production. J Biol Chem 285: 32549-32556.
73. Bell KF, Zheng L, Fahrenholz F, Cuello AC (2008) ADAM-10 over-expression increases cortical synaptogenesis. Neurobiol Aging 29: 554-565. (Pubitemid 351312818)