Tuberin nuclear localization can be regulated by phosphorylation of its carboxyl terminus

Molecular Cancer Research

Volumn 4, Issue 11, 2006, Pages 885-897

  York, Brian ^a   Lou, Dingyuan ^a   Noonan, Daniel J ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; PHORBOL ESTER; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE B; S6 KINASE; SERINE; TUBERIN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHANGIOLEIOMYOMATOSIS; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TRANSLATION INITIATION; TUBEROUS SCLEROSIS;

CELL NUCLEUS; CYTOPLASM; ESTROGEN RECEPTOR ALPHA; HUMANS; NUCLEAR LOCALIZATION SIGNALS; PHORBOL ESTERS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SEQUENCE DELETION; SERINE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 33845344736     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-06-0056     Document Type: Article

References (46)

1. Gomez MR. History of the tuberous sclerosis complex. Brain Dev 1995;17 Suppl:55-7.
2. Kwiatkowski DJ. Tuberous sclerosis: from tubers to mTOR. Ann Hum Genet 2003;67:87-96.
3. Dabora SL, Jozwiak S, Franz DN, et al. Mutational analysis in a cohort of 224 tuberous sclerosis patients indicates increased severity of TSC2, compared with TSC1, disease in multiple organs. Am J Hum Genet 2001;68:64-80.
4. Finlay G. The LAM cell: what is it, where does it come from, and why does it grow? Am J Physiol Lung Cell Mol Physiol 2004;286:L690-3.
5. Glassberg MK. Lymphangioleiomyomatosis. Clin Chest Med 2004;25:573-82, vii.
6. Franz DN, Brody A, Meyer C, et al. Mutational and radiographic analysis of pulmonary disease consistent with lymphangioleiomyomatosis and micronodular pneumocyte hyperplasia in women with tuberous sclerosis. Am J Respir Crit Care Med 2001;164:661-8.
7. Krymskaya VP. Tumour suppressors hamartin and tuberin: intracellular signalling. Cell Signal 2003;15:729-39.
8. Rosner M, Freilinger A, Hengstschlager M. Proteins interacting with the tuberous sclerosis gene products. Amino Acids 2004;27:119-28.
9. Noonan DJ, Lou D, Griffith N, Vanaman TC. A calmodulin binding site in the tuberous sclerosis 2 gene product is essential for regulation of transcription events and is altered by mutations linked to tuberous sclerosis and lymphangioleiomyomatosis. Arch Biochem Biophys 2002;398:132-40.
10. York B, Lou D, Panettieri RA, Jr., Krymskaya VP, Vanaman TC, Noonan DJ. Cross-talk between tuberin, calmodulin, and estrogen signaling pathways. FASEB J 2005;19:1202-4.
11. Henry KW, Yuan X, Koszewski NJ, Onda H, Kwiatkowski DJ, Noonan DJ. Tuberous sclerosis gene 2 product modulates transcription mediated by steroid hormone receptor family members. J Biol Chem 1998;273:20535-9.
12. Wei J, Li P, Chiriboga L, et al. Tuberous sclerosis in a 19-week fetus: immunohistochemical and molecular study of hamartin and tuberin. Pediatr Dev Pathol 2002;5:448-64.
13. Murthy V, Haddad LA, Smith N, et al. Similarities and differences in the subcellular localization of hamartin and tuberin in the kidney. Am J Physiol Renal Physiol 2000;278:F737-46.
14. Yamamoto Y, Jones KA, Mak BC, Muehlenbachs A, Yeung RS. Multi-compartmental distribution of the tuberous sclerosis gene products, hamartin and tuberin. Arch Biochem Biophys 2002;404:210-7.
15. Lou D, Griffith N, Noonan DJ. The tuberous sclerosis 2 gene product can localize to nuclei in a phosphorylation-dependent manner. Mol Cell Biol Res Commun 2001;4:374-80.
16. Goncharova E, Goncharov D, Noonan D, Krymskaya VP. TSC2 modulates actin cytoskeleton and focal adhesion through TSC1-binding domain and the Rac1 GTPase. J Cell Biol 2004;167:1171-82.
17. Finlay GA, Hunter DS, Walker CL, Paulson KE, Fanburg BL. Regulation of PDGF production and ERK activation by estrogen is associated with TSC2 gene expression. Am J Physiol Cell Physiol 2003;285:C409-18.
18. Kaffman A, O'Shea EK. Regulation of nuclear localization: a key to a door. Annu Rev Cell Dev Biol 1999;15:291-339.
19. Pemberton LF, Paschal BM. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 2005;6:187-98.
20. Jans DA, Xiao CY, Lam MH. Nuclear targeting signal recognition: a key control point in nuclear transport? Bioessays 2000;22:532-44.
21. Roberts PS, Sandra LB, Worku A, et al. Mutational Analysis in a cohort of 661 TSC patients. In: New prospectives in tuberous sclerosis complex. Chantilly VA, 2002. p. A6.6.
22. Poon IK, Jans DA. Regulation of nuclear transport: central role in development and transformation? Traffic 2005;6:173-86.
23. Dan HC, Sun M, Yang L, et al. Phosphatidylinositol 3-kinase/Akt pathway regulates tuberous sclerosis tumor suppressor complex by phosphorylation of tuberin. J Biol Chem 2002;277:35364-70.
24. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J. Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci U S A 2004;101:13489-94.
25. Jones KA, Jiang X, Yamamoto Y, Yeung RS. Tuberin is a component of lipid rafts and mediates caveolin-1 localization: role of TSC2 in post-Golgi transport. Exp Cell Res 2004;295:512-24.
26. Wienecke R, Maize JC, Jr., Shoarinejad F, et al. Co-localization of the TSC2 product tuberin with its target Rap1 in the Golgi apparatus. Oncogene 1996;13:913-23.
27. Plank TL, Yeung RS, Henske EP. Hamartin, the product of the tuberous sclerosis 1 (TSC1) gene, interacts with tuberin and appears to be localized to cytoplasmic vesicles. Cancer Res 1998;58:4766-70.
28. Jansen FE, Notenboom RG, Nellist M, et al. Differential localization of hamartin and tuberin and increased S6 phosphorylation in a tuber. Neurology 2004;63:1293-5.
29. Biswas DK, Reddy PV, Pickard M, Makkad B, Pettit N, Pardee AB. Calmodulin is essential for estrogen receptor interaction with its motif and activation of responsive promoter. J Biol Chem 1998;273:33817-24.
30. Li L, Li Z, Sacks DB. The transcriptional activity of estrogen receptor-α is dependent on Ca2+/calmodulin. J Biol Chem 2005;280:13097-104.
31. Chow FA, Anderson KA, Noeldner PK, Means AR. The autonomous activity of calcium/calmodulin-dependent protein kinase IV is required for its role in transcription. J Biol Chem 2005;280:20530-8.
32. Ellison TI, Dowd DR, Macdonald PN. Calmodulin-dependent kinase IV stimulates vitamin D receptor-mediated transcription. Mol Endocrinol 2005;19:2309-19.
33. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003;115:577-90.
34. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. Tuberous sclerosis complex gene products, tuberin and hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 2003;13:1259-68.
35. Kilberg MS, Pan YX, Chen H, Leung-Pineda V. Nutritional control of gene expression: how mammalian cells respond to amino acid limitation. Annu Rev Nutr 2005;25:59-85.
36. Le Breton M, Cormier P, Belle R, Mulner-Lorillon O, Morales J. Translational control during mitosis. Biochimie 2005;87:805-11.
37. Bachmann RA, Kim JH, Wu AL, Park IH, Chen J. A nuclear transport signal in mammalian target of rapamycin is critical for its cytoplasmic signaling to S6 kinase 1. J Biol Chem 2006;281:7357-63.
38. Zhang X, Shu L, Hosoi H, Murti KG, Houghton PJ. Predominant nuclear localization of mammalian target of rapamycin in normal and malignant cells in culture. J Biol Chem 2002;277:28127-34.
39. Maissel A, Marom M, Shtutman M, Shahaf G, Livneh E. PKCη is localized in the Golgi, ER and nuclear envelope and translocates to the nuclear envelope upon PMA activation and serum-starvation: C1b domain and the pseudosubstrate containing fragment target PKCη to the Golgi and the nuclear envelope. Cell Signal 2006;18:1127-39.
40. Fukuda T, Kobayashi T, Momose S, Yasui H, Hino O. Distribution of Tsc1 protein detected by immunohistochemistry in various normal rat tissues and the renal carcinomas of Eker rat: detection of limited colocalization with Tsc1 and Tsc2 gene products in vivo. Lab Invest 2000;80:1347-59.
41. Aicher LD, Campbell JS, Yeung RS. Tuberin phosphorylation regulates its interaction with hamartin. two proteins involved in tuberous sclerosis. J Biol Chem 2001;276:21017-21.
42. Nellist M, Verhaaf B, Goedbloed MA, Reuser AJ, van den Ouweland AM, Halley DJ. TSC2 missense mutations inhibit tuberin phosphorylation and prevent formation of the tuberin-hamartin complex. Hum Mol Genet 2001;10:2889-98.
43. Roberts PS, Sandra LB, Worku A, et al. Mutational analysis in a cohort of 661 TSC Patients. In: New prospectives in tuberous sclerosis. Chantilly, VA, September 19-22 2002. p. A6.6.
44. Strizheva GD, Carsillo T, Kruger WD, Sullivan EJ, Ryu JH, Henske EP. The spectrum of mutations in TSC1 and TSC2 in women with tuberous sclerosis and lymphangiomyomatosis. Am J Respir Crit Care Med 2001;163:253-8.
45. Ausubel FM, Brent R, Kingston RE, et al. editors. Short protocols in molecular biology. 2nd ed. New York (NY): John Wiley & Sons; 1992.
46. Spencer ML, Theodosiou M, Noonan DJ. NPDC-1, a novel regulator of neuronal proliferation, is degraded by the ubiquitin/proteasome system through a PEST degradation motif. J Biol Chem 2004;279:37069-78.