The amyloid precursor protein controls adult hippocampal neurogenesis through GABAergic interneurons

Journal of Neuroscience

Volumn 34, Issue 40, 2014, Pages 13314-13325

  Wang, Baiping ^a,b   Wang, Zilai ^a,b,e   Sun, Lu ^a   Yang, Li ^a   Li, Hongmei ^a   Cole, Allysa L ^a   Rodriguez Rivera, Jennifer ^a   Lu, Hui Chen ^c,d   Zheng, Hui ^a,b  

^a Huffington Center on Aging   (United States)

^b Department of Molecular and Human Genetics ^*  (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d TEXAS CHILDREN S HOSPITAL   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Adult neurogenesis; Alzheimer s disease; Amyloid precursor protein; GABAergic; Hippocampus; Interneurons

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AMYLOID PRECURSOR PROTEIN; RETROVIRUS VECTOR; AMINO ACID RECEPTOR BLOCKING AGENT; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; NERVE PROTEIN; NES PROTEIN, MOUSE; NESTIN; NEUROD6 PROTEIN, MOUSE; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VIAAT PROTEIN, MOUSE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRDU ASSAY; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPHYSIOLOGY; FEAR; GABAERGIC TRANSMISSION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTERNEURON; MOUSE; NERVE CELL INHIBITION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PATCH CLAMP TECHNIQUE; PROTEIN EXPRESSION; SHOCK; SYNAPTIC TRANSMISSION; AGE; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; FEMALE; GENETICS; MALE; MEMBRANE POTENTIAL; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

AGE FACTORS; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABAERGIC NEURONS; HIPPOCAMPUS; INTERNEURONS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NESTIN; NEUROGENESIS; SODIUM CHANNEL BLOCKERS; SYNAPTIC TRANSMISSION; TETRODOTOXIN; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84907482998     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2848-14.2014     Document Type: Article

References (38)

1. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523-569. CrossRef Medline
2. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture.Nat Rev Neurosci 3:728-739. CrossRef Medline
3. Caillé I, Allinquant B, Dupont E, Bouillot C, Langer A, Müller U, Prochiantz A (2004) Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 131: 2173-2181. CrossRef Medline
4. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, Gong S, Lu HC, Heintz N, Ekker M, Rubenstein JL, Noebels JL, Rosenmund C, Zoghbi HY (2010) Dysfunction in GABA signalling mediates autismlike stereotypies and Rett syndrome phenotypes. Nature 468:263-269. CrossRef Medline
5. Chuang TT (2010) Neurogenesis in mouse models of Alzheimer’s disease. Biochim Biophys Acta 1802:872-880. CrossRef Medline
6. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213. CrossRef Medline
7. Demars MP, Bartholomew A, Strakova Z, Lazarov O (2011) Soluble amyloid precursor protein: a novel proliferation factor of adult progenitor cells of ectodermal and mesodermal origin. Stem Cell Res Ther 2:36. CrossRef Medline
8. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229. CrossRef Medline
9. Fitzjohn SM, Morton RA, Kuenzi F, Rosahl TW, Shearman M, Lewis H, Smith D, Reynolds DS, Davies CH, Collingridge GL, Seabrook GR (2001) Agerelated impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J Neurosci 21:4691-4698. Medline
10. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593. CrossRef Medline
11. Ge S, Pradhan DA, Ming GL, Song H (2007) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30:1-8. CrossRef Medline
12. Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA (2006) Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44:611-621. CrossRef Medline
13. Guo Q, Li H, Gaddam SS, Justice NJ, Robertson CS, Zheng H (2012) Amyloid precursor protein revisited: neuron-specific expression and highly stable nature of soluble derivatives. J Biol Chem 287:2437-2445. CrossRef Medline
14. Ihrie RA, Alvarez-Buylla A (2011) Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70:674-686. CrossRef Medline
15. Jedlicka P, Owen M, Vnencak M, Tschäpe JA, Hick M, Müller UC, Deller T (2012) Functional consequences of the lack of amyloid precursor protein in the mouse dentate gyrus in vivo. Exp Brain Res 217:441-447. CrossRef Medline
16. Kheirbek MA, Klemenhagen KC, Sahay A, Hen R (2012) Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 15:1613-1620. CrossRef Medline
17. Lazarov O, Marr RA (2010) Neurogenesis and Alzheimer’s disease: at the crossroads. Exp Neurol 223:267-281. CrossRef Medline
18. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687-702. CrossRef Medline
19. Mu Y, Gage FH (2011) Adult hippocampal neurogenesis and its role in Alzheimer’s disease. Mol Neurodegener 6:85. CrossRef Medline
20. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188-201. CrossRef Medline
21. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3:715-727. CrossRef Medline
22. Ring S, Weyer SW, Kilian SB, Waldron E, Pietrzik CU, Filippov MA, Herms J, Buchholz C, Eckman CB, Korte M, Wolfer DP, Müller UC (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. CrossRef Medline
23. Sahay A, Scobie KN, Hill AS, O’Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466-470. CrossRef Medline
24. Seabrook GR, Smith DW, Bowery BJ, Easter A, Reynolds T, Fitzjohn SM, Morton RA, Zheng H, Dawson GR, Sirinathsinghji DJ, Davies CH, Collingridge GL, Hill RG (1999) Mechanisms contributing to the deficits in hippocampal synaptic plasticity in mice lacking amyloid precursor protein. Neuropharmacology 38:349-359. CrossRef Medline
25. Sernagor E, Chabrol F, Bony G, Cancedda L (2010) GABAergic control of neurite outgrowth and remodeling during development and adult neurogenesis: general rules and differences in diverse systems. Front Cell Neurosci 4:11. CrossRef Medline
26. Song J, Zhong C, Bonaguidi MA, Sun GJ, Hsu D, Gu Y, Meletis K, Huang ZJ, Ge S, Enikolopov G, Deisseroth K, Luscher B, Christian KM, Ming GL, Song H (2012) Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 489:150-154. CrossRef Medline
27. Tanzi RE (2012) The genetics of Alzheimer disease. Cold Spring Harb Perspect Med 2: a006296. CrossRef Medline
28. Tashiro A, Zhao C, Gage FH (2006) Retrovirus-mediated single-cell gene knockout technique in adult newborn neurons in vivo. Nat Protoc 1:3049-3055. Medline
29. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803-815. CrossRef Medline
30. Treves A, Tashiro A, Witter MP, Moser EI (2008) What is the mammalian dentate gyrus good for? Neuroscience 154:1155-1172. CrossRef Medline
31. Wang Z, Wang B, Yang L, Guo Q, Aithmitti N, Songyang Z, Zheng H (2009) Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. J Neurosci 29: 10788-10801. CrossRef Medline
32. Wesnes KA, Annas P, Basun H, Edgar C, Blennow K (2014) Performance on a pattern separation task by Alzheimer’s patients shows possible links between disrupted dentate gyrus activity and apolipoprotein [element of] 4 status and cerebrospinal fluid amyloid-03B242 levels. Alzheimers Res Ther 6:20. CrossRef Medline
33. Winner B, Kohl Z, Gage FH (2011) Neurodegenerative disease and adult neurogenesis. Eur J Neurosci 33:1139-1151. CrossRef Medline
34. Yang L, Wang Z, Wang B, Justice NJ, Zheng H (2009) Amyloid precursor protein regulates Cav1.2 L-type calcium channel levels and function to influence GABAergic short-term plasticity. J Neurosci 29:15660-15668. CrossRef Medline
35. Yassa MA, Stark CE (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515-525. CrossRef Medline
36. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11. CrossRef Medline
37. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660. CrossRef Medline
38. Zheng H, Koo EH (2011) Biology and pathophysiology of the amyloid precursor protein. Mol Neurodegener 6:27. CrossRef Medline