Specific Inhibition of CBP/beta-catenin Interaction Rescues Defects in Neuronal Differentiation Caused by a Presenilin-1 Mutation

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2005 Aug 12

PMID 16093313

Citations 86

Authors

Jia-Ling Teo

Hong Ma

Cu Nguyen

Crystal Lam

Michael Kahn

Affiliations

Soon will be listed here.

Abstract

Wnt/beta-catenin signaling has been shown to promote self-renewal in a variety of tissue stem cells, including neuronal stem cells and hematopoietic stem cells. However, activation of the Wnt/beta-catenin pathway promoted and inhibition of the pathway prevented differentiation of neuronal precursor cells. A clear explanation for the differential effects of Wnt/beta-catenin activation on neuronal precursors is not available at present. Presenilin-1 (PS-1) is a polytopic protein comprised of six to eight transmembrane domains. PS-1, as part of the gamma-secretase complex, is required for the intramembrane proteolysis of both amyloid precursor protein (APP) and Notch. Additionally, through interactions with beta-catenin, PS-1 is associated with modulation of Wnt/beta-catenin signaling. A familial Alzheimer's disease-associated PS-1 mutant, PS-1(L286V), causes a dramatic increase in T cell factor (TCF)/beta-catenin transcription in PC-12 cells, which prevents normal nerve growth factor (NGF)-induced neuronal differentiation and neurite outgrowth. Selective inhibition of TCF/beta-catenin/cAMP-response element-binding protein (CREB)-binding protein (CBP)-mediated transcription, but not TCF/beta-catenin/p300, with the recently described small molecule antagonist ICG-001 corrects these defects in neuronal differentiation, highlighting the importance of Wnt/beta-catenin signaling in this process. We propose that increased TCF/beta-catenin/CBP-mediated transcription, as well as a failure to switch to TCF/beta-catenin/p300-mediated transcription, play an important role in decreasing neuronal differentiation.

Citing Articles

Targeting CBP and p300: Emerging Anticancer Agents.

Masci D, Puxeddu M, Silvestri R, La Regina G Molecules. 2024; 29(19).

PMID: 39407454 PMC: 11482477. DOI: 10.3390/molecules29194524.

Why Is Wnt/β-Catenin Not Yet Targeted in Routine Cancer Care?.

de Pellegars-Malhortie A, Picque Lasorsa L, Mazard T, Granier F, Prevostel C Pharmaceuticals (Basel). 2024; 17(7).

PMID: 39065798 PMC: 11279613. DOI: 10.3390/ph17070949.

3D Chromatin Alteration by Disrupting β-Catenin/CBP Interaction Is Enriched with Insulin Signaling in Pancreatic Cancer.

Zhou Y, He Z, Li T, Choppavarapu L, Hu X, Cao R Cancers (Basel). 2024; 16(12).

PMID: 38927910 PMC: 11201718. DOI: 10.3390/cancers16122202.

Stromal-induced epithelial-mesenchymal transition induces targetable drug resistance in acute lymphoblastic leukemia.

Park C, Yoshihara H, Gao Q, Qu C, Iacobucci I, Ghate P Cell Rep. 2023; 42(7):112804.

PMID: 37453060 PMC: 10529385. DOI: 10.1016/j.celrep.2023.112804.

Anti-inflammatory and antifibrotic effects of CBP/β-catenin inhibitor for hepatocytes: small molecular inhibitor, OP-724 possibly improves liver function.

Ouchi H, Mizutani Y, Yoshimura K, Sato Y, Kimura K, Haruyama Y Med Mol Morphol. 2023; 56(2):94-105.

PMID: 36645521 DOI: 10.1007/s00795-022-00343-8.

References

Tischler A, Greene L . Nerve growth factor-induced process formation by cultured rat pheochromocytoma cells. Nature. 1975; 258(5533):341-2. DOI: 10.1038/258341a0. View

Yao T, P Oh S, Fuchs M, Zhou N, ChNg L, Newsome D . Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell. 1998; 93(3):361-72. DOI: 10.1016/s0092-8674(00)81165-4. View

Behrens J . Control of beta-catenin signaling in tumor development. Ann N Y Acad Sci. 2000; 910:21-33; discussion 33-5. DOI: 10.1111/j.1749-6632.2000.tb06698.x. View

Zhang J, Niu C, Ye L, Huang H, He X, Tong W . Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003; 425(6960):836-41. DOI: 10.1038/nature02041. View

Otero J, Fu W, Kan L, Cuadra A, Kessler J . Beta-catenin signaling is required for neural differentiation of embryonic stem cells. Development. 2004; 131(15):3545-57. DOI: 10.1242/dev.01218. View

Takahashi J, Palmer T, Gage F . Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J Neurobiol. 1999; 38(1):65-81. View

Zechner D, Fujita Y, Hulsken J, Muller T, Walther I, Taketo M . beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol. 2003; 258(2):406-18. DOI: 10.1016/s0012-1606(03)00123-4. View

Berezovska O, Xia M, Hyman B . Notch is expressed in adult brain, is coexpressed with presenilin-1, and is altered in Alzheimer disease. J Neuropathol Exp Neurol. 1998; 57(8):738-45. DOI: 10.1097/00005072-199808000-00003. View

Caricasole A, Copani A, Caruso A, Caraci F, Iacovelli L, Sortino M . The Wnt pathway, cell-cycle activation and beta-amyloid: novel therapeutic strategies in Alzheimer's disease?. Trends Pharmacol Sci. 2003; 24(5):233-8. DOI: 10.1016/s0165-6147(03)00100-7. View

10.

Roth J, Shikama N, Henzen C, Desbaillets I, Lutz W, Marino S . Differential role of p300 and CBP acetyltransferase during myogenesis: p300 acts upstream of MyoD and Myf5. EMBO J. 2003; 22(19):5186-96. PMC: 204457. DOI: 10.1093/emboj/cdg473. View

11.

Shen Y, Mani S, Donovan S, Schwob J, Meiri K . Growth-associated protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J Neurosci. 2002; 22(1):239-47. PMC: 6757587. View

12.

Selkoe D . Alzheimer's disease is a synaptic failure. Science. 2002; 298(5594):789-91. DOI: 10.1126/science.1074069. View

13.

Greene L, Tischler A . Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976; 73(7):2424-8. PMC: 430592. DOI: 10.1073/pnas.73.7.2424. View

14.

Caille I, Allinquant B, Dupont E, Bouillot C, Langer A, Muller U . Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development. 2004; 131(9):2173-81. DOI: 10.1242/dev.01103. View

15.

Saura C, Choi S, Beglopoulos V, Malkani S, Zhang D, Rao B . Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron. 2004; 42(1):23-36. DOI: 10.1016/s0896-6273(04)00182-5. View

16.

Weidemann A, Eggert S, Reinhard F, Vogel M, Paliga K, Baier G . A novel epsilon-cleavage within the transmembrane domain of the Alzheimer amyloid precursor protein demonstrates homology with Notch processing. Biochemistry. 2002; 41(8):2825-35. DOI: 10.1021/bi015794o. View

17.

Jin K, Peel A, Mao X, Xie L, Cottrell B, Henshall D . Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A. 2003; 101(1):343-7. PMC: 314187. DOI: 10.1073/pnas.2634794100. View

18.

Guo Q, Sopher B, Furukawa K, Pham D, Robinson N, Martin G . Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid beta-peptide: involvement of calcium and oxyradicals. J Neurosci. 1997; 17(11):4212-22. PMC: 6573527. View

19.

Chiang M, Misner D, Kempermann G, Schikorski T, Giguere V, Sucov H . An essential role for retinoid receptors RARbeta and RXRgamma in long-term potentiation and depression. Neuron. 1999; 21(6):1353-61. DOI: 10.1016/s0896-6273(00)80654-6. View

20.

Fraser P, Yu G, Levesque L, Nishimura M, Yang D, Mount H . Presenilin function: connections to Alzheimer's disease and signal transduction. Biochem Soc Symp. 2001; (67):89-100. DOI: 10.1042/bss0670089. View