Neurobiology of Aging
Volume 29, Issue 5 , Pages 724-738 , May 2008

Cellular distribution of γ-secretase subunit nicastrin in the developing and adult rat brains

  • A. Kodam

      Affiliations

    • Department of Psychiatry, University of Alberta, Edmonton, Alberta, Canada T6G 2B7
    • ,
  • K.S. Vetrivel

      Affiliations

    • Department of Neurobiology, The University of Chicago, Chicago, IL 60637, USA
    • ,
  • G. Thinakaran

      Affiliations

    • Department of Neurobiology, The University of Chicago, Chicago, IL 60637, USA
    • Department of Neurology, The University of Chicago, Chicago, IL 60637, USA
    • ,
  • S. Kar

      Affiliations

    • Department of Psychiatry, University of Alberta, Edmonton, Alberta, Canada T6G 2B7
    • Department of Medicine (Neurology), University of Alberta, Edmonton, Alberta, Canada T6G 2B7
    • Corresponding Author InformationCorresponding author at: Centre for Alzheimer and Neurodegenerative Research, Departments of Medicine (Neurology) and Psychiatry, University of Alberta, Edmonton, Alberta, Canada. Tel.: +1 780 492 6524; fax: +1 780 492 6841.

Received 14 June 2006 ,Revised 1 December 2006 ,Accepted 5 December 2006.

References 

  1. Baulac S, LaVoie MJ, Kimberly WT, Strahle J, Wolfe MS, Selkoe DJ, et al. Functional γ-secretase complex assembly in Golgi/trans-Golgi network: interactions among presenilin, nicastrin, Aph1, Pen-2 and γ-secretase substrates. Neurobiol. Dis. 2003;14:194–204
  2. Bayer SA. Development of the hippocampal region in the rat. II Morphogenesis during embryonic and early postnatal life. J. Comp. Neurol. 1980;190:115–134
  3. Blanchard V, Czech C, Bonici B, Clavel N, Gohin M, Dalet K, et al. Immunohistochemical analysis of presenilin 2 expression in the mouse brain: distribution pattern and co-localization with presenilin 1 protein. Brain Res. 1997;758:209–217
  4. Capell A, Kaether C, Edbauer D, Shirotani K, Merkl S, Steiner H, et al. Nicastrin interacts with γ-secretase complex components via the N-terminal part of its transmembrane domain. J. Biol. Chem. 2003;278:52519–52523
  5. Chen F, Yu G, Arawaka S, Nishimura M, Kawarai T, Yu H, et al. Nicastrin binds to membrane-tethered Notch. Nat. Cell Biol. 2001;3:751–754
  6. Chen F, Hasegawa H, Schmitt-Ulms G, Kawarai T, Bohm C, Katayama T, et al. TMP21 is a presenilin complex component that modulates gamma-secretase but not epsilon-secretase activity. Nature. 2006;440:1208–1212
  7. Confaloni A, Crestini A, Albani D, Piscopo P, Campeggi LM, Terreni L, et al. Rat nicastrin gene: cDNA isolation, mRNA variants and expression pattern analysis. Mol. Brain Res. 2005;136:12–22
  8. Cordell B. β-Amyloid formation as a potential therapeutic target for Alzheimer's disease. Annu. Rev. Pharmacol. Toxicol. 1994;34:69–89
  9. De Strooper B. Aph-1, Pen-2, and nicastrin with presenilin generate an active gamma-secretase complex. Neuron. 2003;38:9–12
  10. De Strooper B. Nicastrin: gatekeeper of the gamma-secretase complex. Cell. 2005;122:318–320
  11. Edbauer D, Winkler E, Haass C, Steiner H. Presenilin and nicastrin regulate each other and determine amyloid β-peptide production via complex formation. Proc. Natl. Acad. Sci. U.S.A. 2002;99:8666–8671
  12. Elder GA, Tezapsidis N, Carter J, Shioi J, Bouras C, Li HC, et al. Identification and neuron specific expression of the S182/presenilin I protein in human and rodent brains. J. Neurosci. Res. 1996;45:308–320
  13. Fakla I, Kovacs I, Yamaguchi H, Geula C, Kasa P. Expressions of amyloid precursor protein, synaptophysin and presenilin-1 in the different areas of the developing cerebellum of rat. Neurochem. Int. 2000;36:143–151
  14. Figueroa DJ, Morris JA, Ma L, Kandpal G, Chen E, Li YM, et al. Presenilin-dependent gamma-secretase activity modulates neurite outgrowth. Neurobiol. Dis. 2002;9:49–60
  15. Glenner GG, Wong CW. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 1984;120:885–890
  16. Goutte C, Hepler W, Mickey KM, Priess JR. aph-2 encodes a novel extracellular protein required for GLP-1-mediated signaling. Development. 2000;127:2481–2492
  17. Hawkes C, Kar S. Insulin-like growth factor-II/mannose-6-phosphate receptor: widespread distribution in neurons of the central nervous system including those expressing cholinergic phenotype. J. Comp. Neurol. 2003;458:113–127
  18. Hawkes C, Kabogo D, Amritraj A, Kar S. Up-regulation of cation-independent mannose 6-phosphate receptor and endosomal–lysosomal markers in surviving neurons after 192-IgG-saporin administrations into the adult rat brain. Am. J. Pathol. 2006;169:1140–1154
  19. Hebert SS, Serneels L, Dejaegere T, Horre K, Dabrowski M, Baert V, et al. Coordinated and widespread expression of γ-secretase in vivo: evidence for size and molecular heterogeneity. Neurobiol. Dis. 2004;17:260–272
  20. Hu Y, Ye Y, Fortini ME. Nicastrin is required for γ-secretase cleavage of the Drosophila Notch receptor. Dev. Cell. 2002;2:69–78
  21. Ilaya NT, Evin G, Masters CL, Culvenor JG. Nicastrin expression in mouse peripheral tissues is not co-ordinated with presenilin and is high in muscle. J. Neurochem. 2004;91:230–237
  22. Jafferali S, Dumont Y, Sotty F, Robitaille Y, Quirion R, Kar S. Insulin-like growth factor-I and its receptor in the frontal cortex, hippocampus and cerebellum of normal human and Alzheimer's disease brains. Synapse. 2000;38:450–459
  23. Kaether C, Lammich S, Edbauer D, Ertl M, Rietdorf J, Capell A, et al. Presenilin-1 affects trafficking and processing of βAPP and is targeted in a complex with nicastrin to the plasma membrane. J. Cell. Biol. 2002;158:551–561
  24. Kang J, Lemaire GH, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell surface receptor. Nature. 1987;325:733–736
  25. Keino H, Kishikawa M, Satoh M, Shimada A. Expression of presenilin 1 and synapse-related proteins during postnatal development is not different between accelerated senescence-prone and -resistant mice. Neuropathology. 2003;23:16–24
  26. Kim KS, Wegiel J, Sapienza V, Chen J, Hong H, Wisniewski HM. Immunoreactivity of presenilin-1 in human, rat and mouse brain. Brain Res. 1997;757:159–163
  27. Kim DY, Ingano LA, Kovacs DM. Nectin-1α, an immunoglobulin-like receptor involved in the formation of synapses, is a substrate for presenilin/gamma-secretase-like cleavage. J. Biol. Chem. 2002;277:49976–49981
  28. Lah JJ, Heilman CJ, Nash NR, Rees HD, Yi H, Counts SE, et al. Light and electron microscopic localization of presenilin-1 in primate brain. J. Neurosci. 1997;17:1971–1980
  29. Lee MK, Slunt HH, Martin LJ, Thinakaran G, Kim G, Gandy SE, et al. Expression of presenilin 1 and 2 (PS1 and PS2) in human and murine tissues. J. Neurosci. 1996;16:7513–7523
  30. Leem JY, Vijayan S, Han P, Cai D, Machura M, Lopes KO, et al. Presenilin 1 is required for maturaiuon and cell surface accumulation of nicastrin. J. Biol. Chem. 2002;277:19236–19240
  31. Li T, Ma G, Cai H, Price DL, Wong PC. Nicastrin is required for assembly of presenilin/gamma-secretase complexes to mediate Notch signaling and for processing and trafficking of beta-amyloid precursor protein in mammals. J. Neurosci. 2003;23:3272–3277
  32. Marambaud P, Shioi J, Serben G, Georgakopoulos A, Sarner S, Nagy V, et al. A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J. 2002;21:1948–1956
  33. Marty S, Wehrle R, Alvarez-Leefmans FJ, Gasnier B, Sotelo C. Postnatal maturation of Na+, K+, 2Cl− cotransporter expression and inhibitory synaptogenesis in the rat hippocampus: an immunohistochemical analysis. Eur. J. Neurosci. 2002;15:233–245
  34. Moreno-Flores MT, Medina M, Wandosell F. Expression of presenilin 1 in nervous system during rat development. J. Comp. Neurol. 1999;410:556–570
  35. Ni CY, Murphy MP, Golde TE, Carpenter G. γ-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science. 2001;294:2179–2181
  36. Parent AT, Barnes NY, Taniguchi Y, Thinakaran G, Sisodia SS. Presenilin attenuates receptor-mediated signaling and synaptic function. J. Neurosci. 2005;25:1540–1549
  37. Pasternak SH, Bagshaw RD, Guiral M, Zhang S, Ackerley CA, Pak BJ, et al. Presenilin-1, nicastrin, amyloid precursor protein, and γ-secretase activity are co-localized in the lysosomal membranes. J. Biol. Chem. 2003;278:26687–26694
  38. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press; 1986;
  39. Price DL, Tanzi RE, Borchelt DR, Sisodia S. Alzheimer's disease: genetic studies and transgenic models. Annu. Rev. Genet. 1998;32:461–493
  40. Sarkar SN, Das HK. Regulatory roles of presenilin-1 and nicastrin in neuronal differentiation during in vitro neurogenesis. J. Neurochem. 2003;87:333–343
  41. Satoh J, Kuroda Y. Nicastrin, a key regulator of presenilin function, is expressed constitutively in human neural cell lines. Neuropathology. 2001;21:115–122
  42. Selkoe DJ, Schenk D. Alzheimer's disease: molecular understanding predicts amyloid based therapeutics. Annu. Rev. Pharmacol. Toxicol. 2003;43:545–584
  43. Shah S, Lee SF, Tabuchi K, Hao YH, Yu C, LaPlant Q, et al. Nicastrin functions as a gamma-secretase-substrate receptor. Cell. 2005;122:435–447
  44. Siman R, Salidas S. Gamma-secretase subunit composition and distribution in the presenilin wild-type and mutant mouse brain. Neuroscience. 2004;129:615–628
  45. Siman R, Velji J. Localization of presenilin-nicastrin complexes and γ-secretase activity to the trans-Golgi network. J. Neurochem. 2003;84:1143–1153
  46. Sisodia SS, George-Hyslop P. γ-Secretase, Notch, Aβ and Alzheimer's disease: where do the presenilins fit in?. Nat. Rev. Neurosci. 2002;3:281–290
  47. Struhl G, Adachi A. Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol. Cell. 2000;6:625–636
  48. Thinakaran G, Regard JB, Bouton CM, Harris CL, Price DL, Borchelt DR, et al. Stable association of presenilin derivatives and absence of presenilin interactions with APP. Neurobiol. Dis. 1998;4:438–453
  49. Uchihara T, Sanjo N, Nakamura A, Han K, Song SY, St George-Hyslop P, et al. Transient abundance of presenilin 1 fragments/nicastrin complex associated with synaptogenesis during development in rat cerebellum. Neurobiol. Aging. 2006;27:88–97
  50. Vetrivel KS, Thinakaran G. Amyloidogenic processing of beta-amyloid precursor protein in intracellular compartments. Neurology. 2006;66(2 Suppl 1):S69–S73
  51. Vetrivel KS, Cheng H, Lin W, Sakurai T, Li T, Nukina N, et al. Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J. Biol. Chem. 2004;279:44945–44954
  52. Wines-Samuelson M, Shen J. Presenilins in the developing, adult, and aging cerebral cortex. Neuroscientist. 2005;11:441–451
  53. Yan XX, Li T, Rominger CM, Prakash SR, Wong PC, Olsen RE, et al. Binding sites of γ-secretase inhibitors in rodent brain: distribution, postnatal development, and effect of deafferentiation. J. Neurosci. 2004;24:2942–2952
  54. Yang DS, Tandon A, Chen F, Yu G, Yu H, Arawaka S, et al. Mature glycosylation and trafficking of nicastrin modulate its binding to presenilins. J. Biol. Chem. 2002;277:28135–28142
  55. Yu G, Nishimura M, Arawaka S, Levitan D, Zhang L, Tandon A, et al. Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and βAPP processing. Nature. 2000;407:48–54
  56. Zhang Y, Luo W, Wang H, Lin P, Vetrivel KS, Liao F, et al. Nicastrin is critical for stability and trafficking but not association of other presenilin/γ-secretase components. J. Biol. Chem. 2005;280:17020–17026
  57. Zhou S, Zhou H, Walian PJ, Jap BK. CD147 is a regulatory subunit of the gamma-secretase complex in Alzheimer's disease amyloid beta-peptide production. Proc. Natl. Acad. Sci. U.S.A. 2005;102:7499–7504

PII: S0197-4580(06)00458-1

doi: 10.1016/j.neurobiolaging.2006.12.005

Neurobiology of Aging
Volume 29, Issue 5 , Pages 724-738 , May 2008

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