Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone

Development

Volumn 131, Issue 9, 2004, Pages 2173-2181

  Caillé, Isabelle ^a   Allinquant, Bernadette ^a   Dupont, Edmond ^a   Bouillot, Colette ^a   Langer, Andreas ^b   Müller, Ulrike ^b   Prochiantz, Alain ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

APP; Neurogenesis; Proliferation; Subventricular zone

Indexed keywords

AMYLOID PRECURSOR PROTEIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SECRETION; RECEPTOR BINDING; REGULATORY MECHANISM; STEM CELL;

ADULT; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BINDING SITES; CELL DIFFERENTIATION; CELL DIVISION; CELLS, CULTURED; EPIDERMAL GROWTH FACTOR; HUMANS; IMMUNOGLOBULIN G; LATERAL VENTRICLES; MICE; NEURONS; PROTEIN BINDING; STEM CELLS; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMALIA; MAMMALIA;

EID: 2542519087     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01103     Document Type: Article

References (55)

1. Allinquant, B., Hantraye, P., Mailleux, P., Moya, K., Bouillot, C. and Prochiantz, A. (1995). Downregulation of amyloid precursor protein inhibits neurite outgrowth in vitro. J. Cell Biol. 128, 919-927.
2. Alvarez-Buylla, A. and Garcia-Verdugo, J. M. (2002). Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634.
3. Bernier, P. J., Bedard, A., Vinet, J., Levesque, M. and Parent, A. (2002). Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc. Natl. Acad. Sci. USA 99, 11464-11469.
4. Bondolfi, L., Calhoun, M., Ermini, F., Kuhn, H. G., Wiederhold, K. H., Walker, L., Staufenbiel, M. and Jucker, M. (2002). Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J. Neurosci. 22, 515-522.
5. Brouillet, E., Trembleau, A., Galanaud, D., Volovitch, M., Bouillot, C., Valenza, C., Prochiantz, A. and Allinquant, B. (1999). The amyloid precursor protein interacts with Go heterotrimeric protein within a cell compartment specialized in signal transduction. J. Neurosci. 19, 1717-1727.
6. Callen, D. J., Black, S. E., Gao, F., Caldwell, C. B. and Szalai, J. P. (2001). Beyond the hippocampus: MRI volumetry confirms widespread limbic atrophy in AD. Neurology 57, 1669-1674.
7. Craig, C. G., Tropepe, V., Morshead, C. M., Reynolds, B. A., Weiss, S. and van der Kooy, D. (1996). In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16, 2649-2658.
8. De Strooper, B. and Annaert, W. (2000). Proteolytic processing and cell biological functions of the amyloid precursor protein. J Cell Sci. 113, 1857-1870.
9. Derossi, D., Chassaing, G. and Prochiantz, A. (1998). Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 8, 84-87.
10. Doetsch, F., Caille, L, Lim, D. A., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (1999a). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
11. Doetsch, F., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (1999b). Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 96, 11619-11624.
12. Doetsch, F., Petreanu, L., Caille, I., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36, 1021-1034.
13. Doherty, P., Williams, E. and Walsh, F. S. (1995). A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth. Neuron 14, 57-66.
14. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A. and Gage, F. H. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317.
15. Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J. D. and Lledo, P. M. (2000). Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl. Acad. Sci. USA 97, 1823-1828.
16. Greenberg, S. M., Koo, E. H., Selkoe, D. J., Qiu, W. Q. and Kosik, K. S. (1994). Secreted beta-amyloid precursor protein stimulates mitogen-activated protein kinase and enhances tau phosphorylation. Proc. Natl. Acad. Sci. USA 91, 7104-7108.
17. Hayashi, Y., Kashiwagi, K., Ohta, J., Nakajima, M., Kawashima, T. and Yoshikawa, K. (1994). Alzheimer amyloid protein precursor enhances proliferation of neural stem cells from fetal rat brain. Biochem. Biophys. Res. Commun. 205, 936-943.
18. Heber, S., Herms, J., Gajic, V., Hainfellner, J., Aguzzi, A., Rulicke, T., von Kretzschmar, H., von Koch, C., Sisodia, S., Tremml, P. 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.
19. Hoffmann, J., Pietrzik, C. U., Kummer, M. P., Twiesselmann, C., Bauer, C. and Herzog, V. (1999). Binding and selective detection of the secretory N-terminal domain of the alzheimer amyloid precursor protein on cell surfaces. J. Histochem. Cytochem. 47, 373-382.
20. Hoffmann, J., Twiesselmann, C., Kummer, M. P., Romagnoli, P. and Herzog, V. (2000). A possible role for the Alzheimer amyloid precursor protein in the regulation of epidermal basal cell proliferation. Eur. J. Cell Biol. 79, 905-914.
21. Hung, A. Y., Koo, E. H., Haass, C. and Selkoe, D. J. (1992). Increased expression of beta-amyloid precursor protein during neuronal differentiation is not accompanied by secretory cleavage. Proc. Natl. Acad. Sci. USA 89, 9439-9443.
22. Kempermann, G. (2002). Why new neurons? Possible functions for adult hippocampal neurogenesis. J. Neurosci. 22, 635-638.
23. Kirschenbaum, B., Nedergaard, M., Preuss, A., Barami, K., Fraser, R. A. and Goldman, S. A. (1994). In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb. Cortex 4, 576-589.
24. Kuhn, H. G., Winkler, J., Kempermann, G., Thal, L. J. and Gage, F. H. (1997). Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17, 5820-5829.
25. Lannfelt, L., Basun, H., Wahlund, L. O., Rowe, B. A. and Wagner, S. L. (1995). Decreased alpha-secretase-cleaved amyloid precursor protein as a diagnostic marker for Alzheimer's disease. Nat. Med. 1, 829-832.
26. Li, Z. W., Stark, G., Gotz, J., Rulicke, T., Gschwind, M., Huber, G., Muller, U. and Weissmann, C. (1996). Generation of mice with a 200-kb amyloid precursor protein gene deletion by Cre recombinase-mediated site-specific recombination in embryonic stem cells. Proc. Natl. Acad. Sci. USA 93, 6158-6162.
27. Magara, F., Muller, U., Li, Z. W., Lipp, H. P., Weissmann, C., Stagljar, M. and Wolfer, D. P. (1999). Genetic background changes the pattern of forebrain commissure defects in transgenic mice underexpressing the beta-amyloid-precursor protein. Proc. Natl. Acad. Sci. USA 96, 4656-4661.
28. Mattson, M. P. (1997). Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol. Rev. 77, 1081-1132.
29. Meziane, H., Dodart, J. C., Mathis, C., Little, S., Clemens, J., Paul, S. M. and Ungerer, A. (1998). Memory-enhancing effects of secreted forms of the beta-amyloid precursor protein in normal and amnestic mice. Proc. Natl. Acad. Sci. USA 95, 12683-12688.
30. Morshead, C. M., Reynolds, B. A., Craig, C. G., McBurney, M. W., Staines, W. A., Morassutti, D., Weiss, S. and van der Kooy, D. (1994). Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13, 1071-1082.
31. Nordin, S. and Murphy, C. (1998). Odor memory in normal aging and Alzheimer's disease. Ann. New York Acad. Sci. 855, 686-693.
32. Ohsawa, I., Takamura, C., Morimoto, T., Ishiguro, M. and Kohsaka, S. (1999). Amino-terminal region of secreted form of amyloid precursor protein stimulates proliferation of neural stem cells. Eur. J. Neurosci. 11, 1907-1913.
33. Okamoto, T., Takeda, S., Murayama, Y., Ogata, E. and Nishimoto, I. (1995). Ligand-dependent G protein coupling function of amyloid transmembrane precursor. J Biol. Chem. 270, 4205-4208.
34. Paliga, K., Peraus, G., Kreger, S., Durrwang, U., Hesse, L., Multhaup, G., Masters, C. L., Beyreuther, K. and Weidemann, A. (1997). Human amyloid precursor-like protein 1-cDNA cloning, ectopic expression in COS-7 cells and identification of soluble forms in the cerebrospinal fluid. Eur. J. Biochem. 250, 354-363.
35. Palmert, M. R., Podlisny, M. B., Witker, D. S., Oltersdorf, T., Younkin, L. H., Selkoe, D. J. and Younkin, S. G. (1989). The beta-amyloid protein precursor of Alzheimer disease has soluble derivatives found in human brain and cerebrospinal fluid. Proc. Natl. Acad. Sci. USA 86, 6338-6342.
36. Parvathy, S., Hussain, I., Karran, E. H., Turner, A. J. and Hooper, N. M. (1998). Alzheimer's amyloid precursor protein alpha-secretase is inhibited by hydroxamic acid-based zinc metalloprotease inhibitors: similarities to the angiotensin converting enzyme secretase. Biochemistry 37, 1680-1685.
37. Pietrzik, C. U., Hoffmann, J., Stober, K., Chen, C. Y., Bauer, C., Otero, D. A., Roch, J. M. and Herzog, V. (1998). From differentiation to proliferation: the secretory amyloid precursor protein as a local mediator of growth in thyroid epithelial cells. Proc. Natl. Acad. Sci. USA 95, 1770-1775.
38. Reynolds, B. A. and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
39. Roch, J. M., Masliah, E., Roch-Levecq, A. C., Sundsmo, M. P., Otero, D. A., Veinbergs, I. and Saitoh, T. (1994). Increase of synaptic density and memory retention by a peptide representing the trophic domain of the amyloid beta/A4 protein precursor. Proc. Natl. Acad. Sci. USA 91, 7450-7454.
40. Rossjohn, J., Cappai, R., Feil, S. C., Henry, A., McKinstry, W. J., Galatis, D., Hesse, L., Multhaup, G., Beyreuther, K., Masters, C. L. et al. (1999). Crystal structure of the N-terminal, growth factor-like domain of Alzheimer amyloid precursor protein. Nat. Struct. Biol. 6, 327-331.
41. Saitoh, T., Sundsmo, M., Roch, J. M., Kimura, N., Cole, G., Schubert, D., Oltersdorf, T. and Schenk, D. B. (1989). Secreted form of amyloid beta protein precursor is involved in the growth regulation of fibroblasts. Cell 58, 615-622.
42. Salbaum, J. M. and Ruddle, F. H. (1994). Embryonic expression pattern of amyloid protein precursor suggests a role in differentiation of specific subsets of neurons. J. Exp. Zool. 269, 116-127.
43. Scharff, C. (2000). Chasing fate and function of new neurons in adult brains. Curr. Opin. Neurobiol. 10, 774-783.
44. Schubert, D., Jin, L. W., Saitoh, T. and Cole, G. (1989). The regulation of amyloid beta protein precursor secretion and its modulatory role in cell adhesion. Neuron 3, 689-694.
45. Seaberg, R. M. and van der Kooy, D. (2002). Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22, 1784-1793.
46. Seri, B., Garcia-Verdugo, J. M., McEwen, B. S. and Alvarez-Buylla, A. (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 21, 7153-7160.
47. Slack, B. E., Breu, J., Muchnicki, L. and Wurtman, R. J. (1997). Rapid stimulation of amyloid precursor protein release by epidermal growth factor: role of protein kinase C. Biochem. J. 327, 245-249.
48. Slunt, H. H., Thinakaran, G., von Koch, C., Lo, A. C., Tanzi, R. E. and Sisodia, S. S. (1994). Expression of a ubiquitous, cross-reactive homologue of the mouse beta-amyloid precursor protein (APP). J. Biol. Chem. 269, 2637-2644.
49. Small, D. H., Mok, S. S. and Bornstein, J. C. (2001). Alzheimer's disease and Abeta toxicity: from top to bottom. Nat. Rev. Neurosci. 2, 595-598.
50. Tropepe, V., Craig, C. G., Morshead, C. M. and van der Kooy, D. (1997). Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci. 17, 7850-7859.
51. Van Nostrand, W. E., Wagner, S. L., Shankle, W. R., Farrow, J. S., Dick, M., Rozemuller, J. M., Kuiper, M. A., Wolters, E. C., Zimmerman, J., Cotman, C. W. et al. (1992). Decreased levels of soluble amyloid beta-protein precursor in cerebrospinal fluid of live Alzheimer disease patients. Proc. Natl. Acad. Sci. USA 89, 2551-2555.
52. von Koch, C. S., Zheng, H., Chen, H., Trumbauer, M., Thinakaran, G., van der Ploeg, L. H., Price, D. L. and Sisodia, S. S. (1997). Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol. Aging 18, 661-669.
53. Wasco, W., Bupp, K., Magendantz, M., Gusella, J. F., Tanzi, R. E. and Solomon, F. (1992). Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer disease-associated amyloid beta protein precursor. Proc. Natl. Acad. Sci. USA 89, 10758-10762.
54. Weickert, C. S., Webster, M. J., Colvin, S. M., Herman, M. M., Hyde, T. M., Weinberger, D. R. and Kleinman, J. E. (2000). Localization of epidermal growth factor receptors and putative neuroblasts in human subependymal zone. J. Comp. Neurol. 423, 359-372.
55. Zheng, H., Jiang, M., Trumbauer, M. E., Sirinathsinghji, D. J., Hopkins, R., Smith, D. W., Heavens, R. P., Dawson, G. R., Boyce, S., Conner, M. W. et al. (1995). β-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81, 525-531.