Down-regulation of ubiquitin ligase Cbl induced by twist haploinsufficiency in Saethre-Chotzen syndrome results in increased PI3K/Akt signaling and osteoblast proliferation

American Journal of Pathology

Volumn 169, Issue 4, 2006, Pages 1303-1311

  Guenou, Hind ^a   Kaabeche, Karim ^a   Dufour, Cécilie ^a   Miraoui, Hichem ^a   Marie, Pierre J ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN KINASE B; UBIQUITIN PROTEIN LIGASE; NUCLEAR PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSCRIPTION FACTOR TWIST; TWIST1 PROTEIN, HUMAN; UBIQUITIN;

ACROCEPHALOSYNDACTYLY; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE MUTATION; HUMAN; IMMUNOREACTIVITY; INFANT; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; CRANIAL SUTURE; CYTOLOGY; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACROCEPHALOSYNDACTYLIA; CELL PROLIFERATION; CRANIAL SUTURES; DOWN-REGULATION; HUMANS; NUCLEAR PROTEINS; OSTEOBLASTS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-CBL; SIGNAL TRANSDUCTION; TRANSFECTION; TWIST TRANSCRIPTION FACTOR; UBIQUITIN;

EID: 38849132555     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.060102     Document Type: Article

References (50)

1. Wilkie AO: Craniosynostosis: genes and mechanisms. Hum Mol Genet 1997, 6:1647-1656
2. el Ghouzzi V, Le Merrer M, Perrin-Schmitt F, Lajeunie E, Benit P, Renier D, Bourgeois P, Bolcato-Bellemin AL, Munnich A, Bonaventure J: Mutations of the Twist gene in the Saethre-Chotzen syndrome. Nat Genet 1997, 15:42-46
3. Howard TD, Paznekas WA, Green ED, Chiang LC, Ma N, Ortiz De Luna RI, Garcia Delgado C, Gonzales-Ramos M, Kline AD, Jabs EW: Mutations in Twist, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat Genet 1997, 15:36-41
4. El Ghouzzi V, Lajeunie E, Le Merrer M, Cormier-Daire V, Renier D, Munnich A, Bonaventure J: Mutations within or upstream of the basic helix-loop-helix domain of the Twist gene are specific to Saethre-Chotzen syndrome. Eur J Hum Genet 1999, 7:27-33
5. Gripp K, Zackai E, Stolle C: Mutations in the human Twist gene. Hum Mutat 2000, 15:150-155
6. El Ghouzzi V, Legeai-Mallet L, Aresta S, Benoist C, Munnich A, de Gunzburg J, Bonaventure J: Saethre-Chotzen mutations cause Twist protein degradation or impaired nuclear location. Hum Mol Genet 2000, 9:813-819
7. El Ghouzzi V, Legeai-Mallet L, Benoist-Lasselin C, Lajeunie E, Renier D, Munnich A, Bonaventure J: Mutations in the basic domain and the loop-helix II junction of Twist abolish DNA binding in Saethre-Chotzen syndrome. FEBS Lett 2001, 492:112-118
8. Yousfi M, Lasmoles F, Lomri A, Delannoy P, Marie PJ: Increased bone formation and decreased osteocalcin expression induced by reduced Twist dosage in the Saethre-Chotzen syndrome. J Clin Invest 2001, 107:1153-1161
9. Yousfi M, Lasmoles F, Marie PJ: TWIST inactivation reduces CBFA1/ RUNX2 expression and DNA binding to the osteocalcin promoter in osteoblasts. Biochem Biophys Res Commun 2002, 297:641-644
10. Yousfi M, Lasmoles F, El Ghouzzi V, Marie PJ: Twist haploinsufficiency in Saethre-Chotzen syndrome induces calvaria osteoblast apoptosis due to increased TNFalpha expression and caspase-2 activation. Hum Mol Genet 2002, 11:359-369
11. Guenou H, Kaabeche K, Mee SL, Marie PJ: A role for fibroblast growth factor receptor-2 in the altered osteoblast phenotype induced by Twist haploinsufficiency in the Saethre-Chotzen syndrome. Hum Mol Genet 2005, 14:1429-1439
12. Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G: A twist code determines the onset of osteoblast differentiation. Dev Cell 2004, 6:423-435
13. Roos-Mattjus P, Sistonen L: The ubiquitin-proteasome pathway. Ann Med 2004, 36:285-295
14. Sanjay A, Horne WC, Baron R: The Cbl family: ubiquitin ligases regulating signaling by tyrosine kinases. Sci STKE 2001, 2001:PE40
15. Schmidt MH, Dikic I: The Cbl interactome and its functions. Nat Rev Mol Cell Biol 2005, 6:907-919
16. Horne WC, Sanjay A, Bruzzaniti A, Baron R: The role(s) of Src kinase and Cbl proteins in the regulation of osteoclast differentiation and function. Immunol Rev 2005, 208:106-125
17. Kaabeche K, Lemonnier J, Le Mee S, Caverzasio J, Marie PJ: Cbl-mediated degradation of Lyn and Fyn induced by constitutive fibroblast growth factor receptor-2 activation supports osteoblast differentiation. J Biol Chem 2004, 279:36259-36267
18. Kaabeche K, Guenou H, Bouvard D, Didelot N, Listrat A, Marie PJ: Cbl-mediated ubiquitination of alpha5 integrin subunit mediates fibronectin-dependent osteoblast detachment and apoptosis induced by FGFR2 activation. J Cell Sci 2005, 118:1223-1232
19. Sattler M, Salgia R, Okuda K, Uemura N, Durstin MA, Pisick E, Xu G, Li JL, Prasad KV, Griffin JD: The proto-oncogene product p120CBL and the adaptor proteins CRKL and c-CRK link c-ABL, p190BCR/ABL and p210BCR/ABL to the phosphatidylinositol-3′ kinase pathway. Oncogene 1996, 12:839-846
20. Tsygankov AY, Teckchandani AM, Feshchenko EA, Swaminathan G: Beyond the RING: CBL proteins as multivalent adapters. Oncogene 2001, 20:6382-6402
21. Cantley LC: The phosphoinositide 3-kinase pathway. Science 2002, 296:1655-1657
22. Downward J: PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol 2004, 15:177-182
23. Golden LH, Insogna KL: The expanding role of PI3-kinase in bone. Bone 2004, 34:3-12
24. Debiais F, Lefevre G, Lemonnier J, Le Mée S, Lasmoles F, Mascarelli F, Marie PJ: Fibroblast growth factor-2 induces osteoblast survival through a phosphatidylinositol 3-kinase-dependent, -beta-catenin-independent signaling pathway. Exp Cell Res 2004, 297:235-246
25. Ghosh-Choudhury N, Abboud SL, Nishimura R, Celeste A, Mahimainathan L, Choudhury GG: Requirement of BMP-2-induced phosphatidylinositol 3-kinase and Akt serine/threonine kinase in osteoblast differentiation and Smad-dependent BMP-2 gene transcription. J Biol Chem 2002, 277:33361-33368
26. Radcliff K, Tang TB, Lim J, Zhang Z, Abedin M, Demer LL, Tintut Y: Insulin-like growth factor-I regulates proliferation and osteoblastic differentiation of calcifying vascular cells via extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase pathways. Circ Res 2005, 96:398-400
27. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S: Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem 2005, 280:41342-41351
28. Fujita T, Azuma Y, Fukuyama R, Hattori Y, Yoshida C, Koida M, Ogita K, Komori T: Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J Cell Biol 2004, 166:85-95
29. Wennstrom S, Downward J: Role of phosphoinositide 3-kinase in activation of ras and mitogen-activated protein kinase by epidermal growth factor. Mol Cell Biol 1999, 19:4279-4288
30. Borgatti P, Martelli AM, Bellacosa A, Casto R, Massari L, Capitani S, Neri LM: Translocation of Akt/PKB to the nucleus of osteoblast-like MC3T3-E1 cells exposed to proliferative growth factors. FEBS Lett 2000, 477:27-32
31. Lee YR, Park J, Yu HN, Kim JS, Youn HJ, Jung SH: Up-regulation of PI3K/Akt signaling by 17beta-estradiol through activation of estrogen receptor-alpha, but not estrogen receptor-beta, and stimulates cell growth in breast cancer cells. Biochem Biophys Res Commun 2005, 336:1221-1226
32. Kim D, Cheng GZ, Lindsley CW, Yang H, Cheng JQ: Targeting the phosphatidylinositol-3 kinase/Akt pathway for the treatment of cancer. Curr Opin Invest Drugs 2005, 6:1250-1258
33. Stephens L, Williams R, Hawkins P: Phosphoinositide 3-kinases as drug targets in cancer. Curr Opin Pharmacol 2005, 5:357-365
34. Wymann MP, Marone R: Phosphoinositide 3-kinase in disease: timing, location, and scaffolding. Curr Opin Cell Biol 2005, 17:141-149
35. Maestro R, Dei Tos AP, Hamamori Y, Krasnokutsky S, Sartorelli V, Kedes L, Doglioni C, Beach DH, Hannon GJ: Twist is a potential oncogene that inhibits apoptosis. Genes Dev 1999, 13:2207-2217
36. Hamamori Y, Sartorelli V, Ogryzko V, Puri PL, Wu H, Wang J, Nakatani Y, Kedes L: Regulation of histone acetyltransferases p300 and PCAF by the bHLH protein Twist and adenoviral oncoprotein E1A. Cell 1999, 96:405-413
37. Vinals F, Lopez-Rovira T, Rosa JL, Ventura F: Inhibition of PI3K/p70 S6K and p38 MAPK cascades increases osteoblastic differentiation induced by BMP-2. FEBS Lett 2002, 510:99-104
38. Yang X, Matsuda K, Bialek P, Jacquot S, Masuoka HC, Schinke T, Li L, Brancorsini S, Sassone-Corsi P, Townes TM, Hanauer A, Karsenty G: ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry syndrome. Cell 2004, 117:387-398
39. Xiao G, Jiang D, Ge C, Zhao Z, Lai Y, Boules H, Phimphilai M, Yang X, Karsenty G, Franceschi RT: Cooperative interactions between activating transcription factor 4 and Runx2/Cbfa1 stimulate osteoblast-specific osteocalcin gene expression. J Biol Chem 2005, 280:30689-30696
40. Bellido T, Ali AA, Plotkin LI, Fu Q, Gubrij I, Roberson PK, Weinstein RS, O'Brien CA, Manolagas SC, Jilka RL: Proteasomal degradation of Runx2 shortens parathyroid hormone-induced anti-apoptotic signaling in osteoblasts. A putative explanation for why intermittent administration is needed for bone anabolism. J Biol Chem 2003, 278:50259-50272
41. Zhao M, Qiao M, Harris SE, Oyajobi BO, Mundy GR, Chen D: Smurf1 inhibits osteoblast differentiation and bone formation in vitro and in vivo. J Biol Chem 2004, 279:12854-12859
42. Yamashita M, Ying SX, Zhang GM, Li C, Cheng SY, Deng CX, Zhang YE: Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 2005, 121:101-113
43. Demontis S, Rigo C, Piccinin S, Mizzau M, Sonego M, Fabris M, Brancolini C, Maestro R: Twist is substrate for caspase cleavage and proteasome-mediated degradation. Cell Death Differ 2006, 13:335-345
44. Ornitz DM, Marie PJ: FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev 2002, 16:1446-1465
45. Datta SR, Brunet A, Greenberg ME: Cellular survival: a play in three Akts. Genes Dev 1999, 13:2905-2927
46. Dupont J, Fernandez AM, Glackin CA, Helman L, LeRoith D: Insulin-like growth factor 1 (IGF-1)-induced twist expression is involved in the anti-apoptotic effects of the IGF-1 receptor. J Biol Chem 2001, 276:26699-26707
47. Drissi H, Hushka D, Aslam F, Nguyen Q, Buffone E, Koff A, van Wijnen A, Lian JB, Stein JL, Stein GS: The cell cycle regulator p27kip1 contributes to growth and differentiation of osteoblasts. Cancer Res 1999, 59:3705-3711
48. Pratap J, Galindo M, Zaidi SK, Vradii D, Bhat BM, Robinson JA, Choi JY, Komori T, Stein JL, Lian JB, Stein GS, van Wijnen AJ: Cell growth regulatory role of Runx2 during proliferative expansion of preosteoblasts. Cancer Res 2003, 63:5357-5362
49. Thomas DM, Johnson SA, Sims NA, Trivett MK, Slavin JL, Rubin BP, Waring P, McArthur GA, Walkley CR, Holloway AJ, Diyagama D, Grim JE, Clurman BE, Bowtell DD, Lee JS, Gutierrez GM, Piscopo DM, Carty SA, Hinds PW: Terminal osteoblast differentiation, mediated by runx2 and p27KIP1, is disrupted in osteosarcoma. J Cell Biol 2004, 167:925-934
50. Galindo M, Pratap J, Young DW, Hovhannisyan H, Im HJ, Choi JY, Lian JB, Stein JL, Stein GS, van Wijnen AJ: The bone-specific expression of Runx2 oscillates during the cell cycle to support a G1-related antiproliferative function in osteoblasts. J Biol Chem 2005, 280:20274-20285