Presenilin modulates EGFR signaling and cell transformation by regulating the ubiquitin ligase Fbw7

Oncogene

Volumn 29, Issue 20, 2010, Pages 2950-2961

  Rocher Ros, V ^a   Marco, S ^a   Mao, J H ^b   Gines, S ^c   Metzger, D ^d,e   Chambon, P ^d,e   Balmain, A ^b   Saura, C A ^a  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF BARCELONA   (Spain)

^d Paris Sciences et Lettres   (France)

^e UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Carcinogenesis; Epidermis; Fbw7; Notch; secretase

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA SECRETASE; NOTCH1 RECEPTOR; PRESENILIN; PROTEASOME; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE RBW7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; EPIDERMIS; EPIDERMIS HYPERPLASIA; FIBROBLAST; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STABILITY; UBIQUITINATION; UPREGULATION;

MUS;

EID: 77952673813     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.57     Document Type: Article

References (54)

1. Alwan HA, van Zoelen EJ, van Leeuwen JE. (2003). Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J Biol Chem 278: 35781-35790.
2. Bhoumik A, Fichtman B, DeRossi C, Breitwieser W, Kluger HM, Davis S et al. (2008). Suppressor role of activating transcription factor 2 (ATF2) in skin cancer. Proc Natl Acad Sci USA 105: 1674-1679. (Pubitemid 351346573)
3. Blanpain C, Lowry W, Pasolli H, Fuchs E. (2006). Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev 20: 3022-3035. (Pubitemid 44771736)
4. Chen ZJ, Sun LJ. (2009). Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 33: 275-286.
5. de Souza N, Vallier LG, Fares H, Greenwald I. (2007). SEL-2, the C. elegans neurobeachin/LRBA homolog, is a negative regulator of lin-12/Notch activity and affects endosomal traffic in polarized epithelial cells. Development 134: 691-702. (Pubitemid 46437911)
6. De Strooper B. (2007). Loss-of-function presenilin mutations in Alzheimer disease. EMBO Rep 8: 141-146.
7. De Strooper B, Annaert W, Cupers P, Saftig P, Craessaerts K, Mumm JS et al. (1999). A presenilin-1-dependent g-secretase-like protease mediates release of Notch intracellular domain. Nature 398: 518-522. (Pubitemid 129523590)
8. Demehri S, Liu Z, Lee J, Lin MH, Crosby SD, Roberts CJ et al. (2008). Notch-deficient skin induces a lethal systemic B-lympho-proliferative disorder by secreting TSLP, a sentinel for epidermal integrity. PLoS Biol 6: e123. (Pubitemid 351824737)
9. Deng Y, Tarassishin L, Kallhoff V, Peethumnongsin E, Wu L, Li YM et al. (2006). Deletion of presenilin 1 hydrophilic loop sequence leads to impaired g-secretase activity and exacerbated amyloid pathology. J Neurosci 26: 3845-3854.
10. Di Fiore PP, Pierce JH, Fleming TP, Hazan R, Ullrich A, King CR et al. (1987). Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell 51: 1063-1070.
11. Grim J, Gustafson M, Hirata R, Hagar A, Swanger J, Welcker M et al. (2008). Isoform-and cell cycle-dependent substrate degradation by the Fbw7 ubiquitin ligase. J Cell Biol 181: 913-920. (Pubitemid 351846825)
12. Gupta-Rossi N, Le Bail O, Gonen H, Brou C, Logeat F, Six E et al. (2001). Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J Biol Chem 276: 34371-34378. (Pubitemid 37384422)
13. Huang F, Goh LK, Sorkin A. (2007). EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci USA 104: 16904-16909. (Pubitemid 350210963)
14. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. (2006). Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21: 737-748. (Pubitemid 43376125)
15. T2 recombinases. Nucleic Acids Res 27: 4324-4327. (Pubitemid 29533170)
16. Jost M, Kari C, Rodeck U. (2000). The EGF receptor\an essential regulator of multiple epidermal functions. Eur J Dermatol 10: 505-510.
17. Kalyankrishna S, Grandis JR. (2006). Epidermal growth factor receptor biology in head and neck cancer. J Clin Oncol 24: 2666-2672. (Pubitemid 46622088)
18. Kang DE, Soriano S, Xia X, Eberhart CG, De Strooper B, Zheng H et al. (2002). Presenilin couples the paired phosphorylation of b-catenin independent of axin: implications for b-catenin activation in tumorigenesis. Cell 110: 751-762. (Pubitemid 35283964)
19. Kolev V, Mandinova A, Guinea-Viniegra J, Hu B, Lefort K, Lambertini C et al. (2008). EGFR signalling as a negative regulator of Notch1 gene transcription and function in proliferating keratinocytes and cancer. Nat Cell Biol 10: 902-911.
20. Koo EH, Kopan R. (2004). Potential role of presenilin-regulated signaling pathways in sporadic neurodegeneration. Nat Med 10(Suppl): S26-S33. (Pubitemid 38901864)
21. Kopan R, Schroeter EH, Weintraub H, Nye JS. (1996). Signal transduction by activated mNotch: importance of proteolytic processing and its regulation by the extracellular domain. Proc Natl Acad Sci USA 93: 1683-1688. (Pubitemid 26075185)
22. Lefort K, Dotto GP. (2004). Notch signaling in the integrated control of keratinocyte growth/differentiation and tumor suppression. Semin Cancer Biol 14: 374-386. (Pubitemid 38993639)
23. Li J, Pauley AM, Myers RL, Shuang R, Brashler JR, Yan R et al. (2002). SEL-10 interacts with presenilin 1, facilitates its ubiquitination, and alters A-beta peptide production. J Neurochem 82: 1540-1548.
24. Li M, Indra A, Warot X, Brocard J, Messaddeq N, Kato S et al. (2000). Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis. Nature 407: 633-636.
25. Li T, Wen H, Brayton C, Das P, Smithson LA, Fauq A et al. (2007). Epidermal growth factor receptor and notch pathways participate in the tumor suppressor function of g-secretase. J Biol Chem 282: 32264-32273. (Pubitemid 350106457)
26. Longva KE, Blystad FD, Stang E, Larsen AM, Johannessen LE, Madshus IH. (2002). Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J Cell Biol 156: 843-854. (Pubitemid 34839867)
27. Mao JH, Perez-Losada J, Wu D, Delrosario R, Tsunematsu R, Nakayama KI et al. (2004). Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene. Nature 432: 775-779. (Pubitemid 39656299)
28. Marmor MD, Yarden Y. (2004). Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23: 2057-2070. (Pubitemid 38496735)
29. Mosesson Y, Shtiegman K, Katz M, Zwang Y, Vereb G, Szollosi J et al. (2003). Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem 278: 21323-21326. (Pubitemid 36792525)
30. Nicolas M, Wolfer A, Raj K, Kummer J, Mill P, van Noort M et al. (2003). Notch1 functions as a tumor suppressor in mouse skin. Nat Genet 33: 416-421. (Pubitemid 36278861)
31. O'Neil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C et al. (2007). FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to g-secretase inhibitors. J Exp Med 204: 1813-1824. (Pubitemid 47236319)
32. Pan Y, Lin MH, Tian X, Cheng HT, Gridley T, Shen J et al. (2004). g-Secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev Cell 7: 731-743. (Pubitemid 39462693)
33. Perez-Losada J, Mao JH, Balmain A. (2005). Control of genomic instability and epithelial tumor development by the p53-Fbxw7/Cdc4 pathway. Cancer Res 65: 6488-6492. (Pubitemid 41060679)
34. Pirrone A, Hager B, Fleckman P. (2005). Primary mouse keratinocyte culture. Methods Mol Biol 289: 3-14.
35. Proweller A, Tu L, Lepore JJ, Cheng L, Lu MM, Seykora J et al. (2006). Impaired Notch signaling promotes de novo squamous cell carcinoma formation. Cancer Res 66: 7438-7444. (Pubitemid 44289196)
36. Repetto E, Yoon I-S, Zheng H, Zhang DE. (2007). Presenilin-1 regulates epidermal growth factor receptor turnover and signaling in the endosomal-lysosomal pathway. J Biol Chem 282: 31504-31516. (Pubitemid 350044898)
37. Rikiyama T, Curtis J, Oikawa M, Zimonjic DB, Popescu N, Murphy BA et al. (2003). GCF2: expression and molecular analysis of repression. Biochim Biophys Acta 1629: 15-25. (Pubitemid 37186774)
38. Saura CA, Choi SY, Beglopoulos V, Malkani S, Zhang D, Shankaranarayana Rao BS et al. (2004). Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42: 23-36. (Pubitemid 38456965)
39. Saura CA, Tomita T, Soriano S, Takahashi M, Leem JY, Honda T et al. (2000). The nonconserved hydrophilic loop domain of presenilin (PS) is not required for PS endoproteolysis or enhanced Ab42 production mediated by familial early onset Alzheimer's disease-linked PS variants. J Biol Chem 275: 17136-17142. (Pubitemid 30398959)
40. Shaye DD, Greenwald I. (2002). Endocytosis-mediated downregula-tion of LIN-12/Notch upon Ras activation in Caenorhabditis elegans. Nature 420: 686-690. (Pubitemid 36764502)
41. Shen J, Bronson RT, Chen DF, Xia W, Selkoe DJ, Tonegawa S. (1997). Skeletal and CNS defects in presenilin-1 deficient mice. Cell 89: 629-639. (Pubitemid 27511773)
42. Soriano S, Kang DE, Fu M, Pestell R, Chevallier N, Zheng H et al. (2001). Presenilin 1 negatively regulates beta-catenin/T cell factor/lymphoid enhancer factor-1 signaling independently of b-amyloid precursor protein and notch processing. J Cell Biol 152: 785-794. (Pubitemid 34280163)
43. Stoscheck CM, Carpenter G. (1984). Down regulation of epidermal growth factor receptors: direct demonstration of receptor degradation in human fibroblasts. J Cell Biol 98: 1048-1053. (Pubitemid 14166537)
44. To MD, Gokgoz N, Doyle TG, Donoviel DB, Knight JA, Hyslop PS et al. (2006). Functional characterization of novel presenilin-2 variants in human breast cancers. Oncogene 25: 3557-3564. (Pubitemid 43901677)
45. Tournoy J, Bossuyt X, Snellinx A, Regent M, Garmyn M, Serneels L et al. (2004). Partial loss of presenilins causes seborrheic keratosis and autoimmune disease in mice. Hum Mol Genet 13: 1321-1331. (Pubitemid 38961640)
46. Vasioukhin V, Degenstein L, Wise B, Fuchs E. (1999). The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci USA 96: 8551-8556. (Pubitemid 29354829)
47. Wang JW, Gamsby JJ, Highfill SL, Mora LB, Bloom GC, Yeatman TJ et al. (2004). Deregulated expression of LRBA facilitates cancer cell growth. Oncogene 23: 4089-4097.
48. Welcker M, Clurman BE. (2007). Fbw7/hCDC4 dimerization regulates its substrate interactions. Cell Division 2: 7. (Pubitemid 46711882)
49. Welcker M, Clurman BE. (2008). FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8: 83-93. (Pubitemid 351161321)
50. Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN et al. (2004). The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc Natl Acad Sci USA 101: 9085-9090. (Pubitemid 38781615)
51. Wu G, Hubbard EJ, Kitajewski JK, Greenwald I. (1998). Evidence for functional and physical association between Caenorhabditis elegans SEL-10, a Cdc4p-related protein, and SEL-12 presenilin. Proc Natl Acad Sci USA 95: 15787-15791. (Pubitemid 29018778)
52. Wu G, Lyapina S, Das I, Li J, Gurney M, Pauley A et al. (2001). Sel-10 is an inhibitor of Notch signaling that targets Notch for ubiquitin-mediated protein degradation. Mol Biol Cell 21: 7403-7415. (Pubitemid 32953491)
53. Xia X, Qian S, Soriano S, Wu Y, Fletcher AM, Wang XJ et al. (2001). Loss of presenilin 1 is associated with enhanced b-catenin signaling and skin tumorigenesis. Proc Natl Acad Sci USA 98: 10863-10868. (Pubitemid 32878710)
54. Zhang Y-W, Wang R, Liu Q, Zhang H, Liao F-F, Xu H. (2007). Presenilin/g-secretase-dependent processing of b-amyloid precursor protein regulates EGF receptor expression. Proc Natl Acad Sci USA 104: 10613-10618. (Pubitemid 47185713)