Presenilin-1 dependent neurogenesis regulates hippocampal learning and memory

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Bonds, Jacqueline A ^a,b   Kuttner Hirshler, Yafit ^b   Bartolotti, Nancy ^b   Tobin, Matthew K ^a,b   Pizzi, Michael ^c   Marr, Robert ^d   Lazarov, Orly ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c MIDWESTERN UNIVERSITY   (United States)

^d ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; NOTCH RECEPTOR; PRESENILIN 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DENTATE GYRUS; DISCRIMINATION LEARNING; DOWN REGULATION; GRANULAR CELL; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECOGNITION; SIGNAL TRANSDUCTION; SURVIVAL RATE; ANIMAL; C57BL MOUSE; GENE SILENCING; GROWTH, DEVELOPMENT AND AGING; LEARNING; MEMORY; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; BETA CATENIN; DENTATE GYRUS; DISCRIMINATION LEARNING; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MICE, INBRED C57BL; NEURAL STEM CELLS; NEUROGENESIS; PHOSPHORYLATION; PRESENILIN-1; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84939186065     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131266     Document Type: Article

References (44)

1. Aimone JB, Li Y, Lee SW, Clemenson GD, Deng W, Gage FH. Regulation and function of adult neurogenesis: from genes to cognition. Physiological reviews. 2014; 94(4):991-1026. doi: 10.1152/physrev.00004.2014 PMID: 25287858
2. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013; 153(6):1219-27. doi: 10.1016/j.cell.2013.05.002 PMID: 23746839
3. Aimone JB, Deng W, Gage FH. Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron. 2011; 70(4):589-96. Epub 2011/05/26. doi: 10.1016/j.neuron.2011.05.010 PMID: 21609818
4. Aimone JB, Deng W, Gage FH. Adult neurogenesis: integrating theories and separating functions. Trends Cogn Sci. 2010; 14(7):325-37. Epub 2010/05/18. doi: 10.1016/j.tics.2010.04.003 PMID: 20471301
5. Hyman BT, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Carrillo MC, et al. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers Dement. 2012; 8(1):1-13. Epub 2012/01/24. doi: 10.1016/j.jalz.2011.10.007 PMID: 22265587
6. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, et al. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature. 1998; 391(6665):387-90. PMID: 9450754
7. De Strooper B, Annaert W, Cupers P, Saftig P, Craessaerts K, Mumm JS, et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 1999; 398(6727):518-22. PMID: 10206645
8. De Strooper B, Iwatsubo T, Wolfe MS. Presenilins and gamma-secretase: structure, function, and role in Alzheimer Disease. Cold Spring Harb Perspect Med. 2012; 2(1):a006304. Epub 2012/02/09. doi: 10.1101/cshperspect.a006304 PMID: 22315713
9. Herreman A, Serneels L, Annaert W, Collen D, Schoonjans L, De Strooper B. Total inactivation of gamma-secretase activity in presenilin-deficient embryonic stem cells. Nature cell biology. 2000; 2(7):461-2. PMID: 10878813
10. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS, Kimberly WT, Selkoe DJ. Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature. 1999; 398(6727):513-7. PMID: 10206644
11. Li YM, Lai MT, Xu M, Huang Q, DiMuzio-Mower J, Sardana MK, et al. Presenilin 1 is linked with gamma-secretase activity in the detergent solubilized state. Proceedings of the National Academy of Sciences of the United States of America. 2000; 97(11):6138-43. PMID: 10801983
12. Zhang Z, Nadeau P, Song W, Donoviel D, Yuan M, Bernstein A, et al. Presenilins are required for gamma-secretase cleavage of beta-APP and transmembrane cleavage of Notch-1. Nature cell biology. 2000; 2(7):463-5. PMID: 10878814
13. Gadadhar A, Marr RA, Lazarov O. Presenilin-1 regulates neural progenitor cell differentiation in the adult brain. J Neurosci. 2011; 31(7):2615-23. Epub Feb 16. doi: 10.1523/JNEUROSCI.4767-10.2011 PMID: 21325529
14. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature. 2011; 472(7344):466-70. Epub 2011/04/05. doi: 10.1038/nature09817 PMID: 21460835
15. Fortress AM, Schram SL, Tuscher JJ, Frick KM. Canonical Wnt signaling is necessary for object recognition memory consolidation. J Neurosci. 2013; 33(31):12619-26. Epub 2013/08/02. doi: 10.1523/JNEUROSCI.0659-13.2013 PMID: 23904598
16. Marambaud P, Shioi J, Serban 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(8):1948-56. PMID: 11953314
17. Serban G, Kouchi Z, Baki L, Georgakopoulos A, Litterst CM, Shioi J, et al. Cadherins mediate both the association between PS1 and beta-catenin and the effects of PS1 on beta-catenin stability. J Biol Chem. 2005; 280(43):36007-12. PMID: 16126725
18. Ciani L, Salinas PC. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci. 2005; 6(5):351-62. Epub 2005/04/16. PMID: 15832199
19. Marambaud P, Wen PH, Dutt A, Shioi J, Takashima A, Siman R, et al. A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell. 2003; 114(5):635-45. Epub 2003/09/19. PMID: 13678586
20. Watanabe H, Smith MJ, Heilig E, Beglopoulos V, Kelleher RJ 3rd, Shen J. Indirect regulation of presenilins in CREB-mediated transcription. J Biol Chem. 2009; 284(20):13705-13. Epub 2009/03/18. doi: 10.1074/jbc.M809168200 PMID: 19289467
21. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, Saxe M, et al. GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci. 2009; 29(25):7966-77. Epub 2009/06/26. doi: 10.1523/JNEUROSCI.1054-09.2009 PMID: 19553437
22. Chavez-Gutierrez L, Bammens L, Benilova I, Vandersteen A, Benurwar M, Borgers M, et al. The mechanism of gamma-Secretase dysfunction in familial Alzheimer disease. EMBO J. 2012; 31(10):2261-74. Epub 2012/04/17. doi: 10.1038/emboj.2012.79 PMID: 22505025
23. Xia D, Watanabe H, Wu B, Lee SH, Li Y, Tsvetkov E, et al. Presenilin-1 Knockin Mice Reveal Loss-of-Function Mechanism for Familial Alzheimer's Disease. Neuron. 2015; 85(5):967-81. doi: 10.1016/j.neuron.2015.02.010 PMID: 25741723
24. Heilig EA, Xia W, Shen J, Kelleher RJ 3rd. A presenilin-1 mutation identified in familial Alzheimer disease with cotton wool plaques causes a nearly complete loss of gamma-secretase activity. The Journal of biological chemistry. 2010; 285(29):22350-9. doi: 10.1074/jbc.M110.116962 PMID: 20460383
25. Heilig EA, Gutti U, Tai T, Shen J, Kelleher RJ 3rd. Trans-dominant negative effects of pathogenic PSEN1 mutations on gamma-secretase activity and Abeta production. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2013; 33(28):11606-17. doi: 10.1523/JNEUROSCI.0954-13.2013 PMID: 23843529
26. Kulic L, Walter J, Multhaup G, Teplow DB, Baumeister R, Romig H, et al. Separation of presenilin function in amyloid beta-peptide generation and endoproteolysis of Notch. Proc Natl Acad Sci U S A. 2000; 97(11):5913-8. Epub 2000/05/17. PMID: 10811883
27. Wang B, Yang W, Wen W, Sun J, Su B, Liu B, et al. Gamma-secretase gene mutations in familial acne inversa. Science. 2010; 330(6007):1065. Epub 2010/10/12. doi: 10.1126/science.1196284 PMID: 20929727
28. Saura CA, Choi SY, Beglopoulos V, Malkani S, Zhang D, Shankaranarayana Rao BS, et al. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron. 2004; 42(1):23-36. Epub 2004/04/07. PMID: 15066262
29. Chen Q, Nakajima A, Choi SH, Xiong X, Tang YP. Loss of presenilin function causes Alzheimer's disease-like neurodegeneration in the mouse. J Neurosci Res. 2008; 86(7):1615-25. Epub 2008/01/15. doi: 10.1002/jnr.21601 PMID: 18189321
30. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011; 7(3):270-9. Epub 2011/04/26. doi: 10.1016/j.jalz.2011.03.008 PMID: 21514249
31. Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cognitive processing. 2012; 13(2):93-110. Epub 2011/12/14. doi: 10.1007/s10339-011-0430-z PMID: 22160349
32. Einstein G, Buranosky R, Crain BJ. Dendritic pathology of granule cells in Alzheimer's disease is unrelated to neuritic plaques. J Neurosci. 1994; 14(8):5077-88. Epub 1994/08/01. PMID: 8046469
33. Kang DE, Soriano S, Frosch MP, Collins T, Naruse S, Sisodia SS, et al. Presenilin 1 facilitates the constitutive turnover of beta-catenin: differential activity of Alzheimer's disease-linked PS1 mutants in the beta-catenin-signaling pathway. J Neurosci. 1999; 19(11):4229-37. Epub 1999/05/26. PMID: 10341227
34. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, et al. Wnt signalling regulates adult hippocampal neurogenesis. Nature. 2005; 437(7063):1370-5. PMID: 16251967
35. Palacino JJ, Murphy MP, Murayama O, Iwasaki K, Fujiwara M, Takashima A, et al. Presenilin 1 regulates beta-catenin-mediated transcription in a glycogen synthase kinase-3-independent fashion. J Biol Chem. 2001; 276(42):38563-9. Epub 2001/08/16. PMID: 11504726
36. Ables JL, Decarolis NA, Johnson MA, Rivera PD, Gao Z, Cooper DC, et al. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci. 2010; 30(31):10484-92. Epub 2010/08/06. doi: 10.1523/JNEUROSCI.4721-09.2010 PMID: 20685991
37. Lavado A, Oliver G. Jagged1 is necessary for postnatal and adult neurogenesis in the dentate gyrus. Dev Biol. 2014; 388(1):11-21. Epub 2014/02/18. doi: 10.1016/j.ydbio.2014.02.004 PMID: 24530424
38. Sun F, Mao X, Xie L, Ding M, Shao B, Jin K. Notch1 signaling modulates neuronal progenitor activity in the subventricular zone in response to aging and focal ischemia. Aging Cell. 2013; 12(6):978-87. Epub 2013/07/10. doi: 10.1111/acel.12134 PMID: 23834718
39. Shin J, Poling J, Park HC, Appel B. Notch signaling regulates neural precursor allocation and binary neuronal fate decisions in zebrafish. Development. 2007; 134(10):1911-20. Epub 2007/04/20. PMID: 17442701
40. Borghese L, Dolezalova D, Opitz T, Haupt S, Leinhaas A, Steinfarz B, et al. Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo. Stem Cells. 2010; 28(5):955-64. Epub 2010/03/18. doi: 10.1002/stem.408 PMID: 20235098
41. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol. 2003; 460(4):563-72. Epub 2003/04/30. PMID: 12717714
42. Balderas I, Rodriguez-Ortiz CJ, Salgado-Tonda P, Chavez-Hurtado J, McGaugh JL, Bermudez-Rattoni F. The consolidation of object and context recognition memory involve different regions of the temporal lobe. Learn Mem. 2008; 15(9):618-24. Epub 2008/08/30. doi: 10.1101/lm.1028008 PMID: 18723431
43. Bonaguidi MA, Peng CY, McGuire T, Falciglia G, Gobeske KT, Czeisler C, et al. Noggin expands neural stem cells in the adult hippocampus. J Neurosci. 2008; 28(37):9194-204. Epub 2008/09/12. doi: 10.1523/JNEUROSCI.3314-07.2008 PMID: 18784300
44. Franklin KBJ and Paxinos G, The mouse brain in stereotaxic coordinates, 3rd Edition. Academic Press, Elsevier 2008 ISBN 9780123742445.