Identification of PTPσ as an autophagic phosphatase

Journal of Cell Science

Volumn 124, Issue 5, 2011, Pages 812-819

  Martin, Katie R ^a,b   Xu, Yong ^a   Looyenga, Brendan D ^a   Davis, Ryan J ^a   Wu, Chia Lun ^c   Tremblay, Michel L ^c   Xu, H Eric ^a   MacKeigan, Jeffrey P ^a  

^a VAN ANDEL RESEARCH INSTITUTE   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Autophagy; FYVE; Phosphatase; PtdIns3P; PTP ; RNAi

Indexed keywords

PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SIGMA; UNCLASSIFIED DRUG; PHOSPHATIDYLINOSITOL 3 KINASE; POLYPHOSPHOINOSITIDE; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; AUTOPHAGY; CELL LEVEL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA INTERFERENCE; CELL LINE; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SECOND MESSENGER;

AUTOPHAGY; CELL LINE; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHATIDYLINOSITOL PHOSPHATES; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 2; RNA INTERFERENCE; SECOND MESSENGER SYSTEMS;

EID: 79952797615     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.080341     Document Type: Article

References (41)

1. Abaan, O. D. and Toretsky, J. A. (2008). PTPL1: a large phosphatase with a split personality. Cancer Metastasis Rev. 27, 205-214.
2. Aicher, B., Lerch, M. M., Muller, T., Schilling, J. and Ullrich, A. (1997). Cellular redistribution of protein tyrosine phosphatases LAR and PTPsigma by inducible proteolytic processing. J. Cell Biol. 138, 681-696. (Pubitemid 27349847)
3. Araki, T., Mohi, M. G., Ismat, F. A., Bronson, R. T., Williams, I. R., Kutok, J. L., Yang, W., Pao, L. I., Gilliland, D. G., Epstein, J. A. et al. (2004). Mouse model of Noonan syndrome reveals cell type- and gene dosage-dependent effects of Ptpn11 mutation. Nat. Med. 10, 849-857. (Pubitemid 39070859)
4. Axe, E. L., Walker, S. A., Manifava, M., Chandra, P., Roderick, H. L., Habermann, A., Griffiths, G. and Ktistakis, N. T. (2008). Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685-701.
5. Bird, I. M. (1994). Analysis of cellular phosphoinositides and phosphoinositols by extraction and simple analytical procedures. Methods Mol. Biol. 27, 227-248.
6. Chan, G., Kalaitzidis, D. and Neel, B. G. (2008). The tyrosine phosphatase Shp2 (PTPN11) in cancer. Cancer Metastasis Rev. 27, 179-192.
7. Chang, Y. Y. and Neufeld, T. P. (2009). An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol. Biol. Cell 20, 2004-2014.
8. Dromard, M., Bompard, G., Glondu-Lassis, M., Puech, C., Chalbos, D. and Freiss, G. (2007). The putative tumor suppressor gene PTPN13/PTPL1 induces apoptosis through insulin receptor substrate-1 dephosphorylation. Cancer Res. 67, 6806-6813. (Pubitemid 47105528)
9. Elchebly, M., Wagner, J., Kennedy, T. E., Lanctot, C., Michaliszyn, E., Itie, A., Drouin, J. and Tremblay, M. L. (1999). Neuroendocrine dysplasia in mice lacking protein tyrosine phosphatase sigma. Nat. Genet. 21, 330-333.
10. Ganley, I. G., Lam du, H., Wang, J., Ding, X., Chen, S. and Jiang, X. (2009). ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem. 284, 12297-12305.
11. Gaullier, J. M., Simonsen, A., D'Arrigo, A., Bremnes, B., Stenmark, H. and Aasland, R. (1998). FYVE fingers bind PtdIns(3)P. Nature 394, 432-433.
12. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., Parton, R. G. and Stenmark, H. (2000). Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588.
13. Guan, K. L. and Dixon, J. E. (1991). Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192, 262-267.
14. Hanada, T., Noda, N. N., Satomi, Y., Ichimura, Y., Fujioka, Y., Takao, T., Inagaki, F. and Ohsumi, Y. (2007). The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282, 37298-37302.
15. Hosokawa, N., Hara, T., Kaizuka, T., Kishi, C., Takamura, A., Miura, Y., Iemura, S., Natsume, T., Takehana, K., Yamada, N. et al. (2009). Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 20, 1981-1991.
16. Imami, K., Sugiyama, N., Kyono, Y., Tomita, M. and Ishihama, Y. (2008). Automated phosphoproteome analysis for cultured cancer cells by two-dimensional nanoLC-MS using a calcined titania/C18 biphasic column. Anal. Sci. 24, 161-166.
17. Itakura, E., Kishi, C., Inoue, K. and Mizushima, N. (2008). Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 19, 5360-5372.
18. Juhasz, G., Hill, J. H., Yan, Y., Sass, M., Baehrecke, E. H., Backer, J. M. and Neufeld, T. P. (2008). The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J. Cell Biol. 181, 655-666. (Pubitemid 351717512)
19. Jung, C. H., Jun, C. B., Ro, S. H., Kim, Y. M., Otto, N. M., Cao, J., Kundu, M. and Kim, D. H. (2009). ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 20, 1992-2003.
20. Kihara, A., Noda, T., Ishihara, N. and Ohsumi, Y. (2001). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152, 519-530. (Pubitemid 34280235)
21. Kimura, S., Noda, T. and Yoshimori, T. (2007). Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460. (Pubitemid 47293726)
22. Klionsky, D. J. (2007). Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8, 931-937.
23. Kontaridis, M. I., Swanson, K. D., David, F. S., Barford, D. and Neel, B. G. (2006). PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J. Biol. Chem. 281, 6785-6792.
24. Lorenzo, O., Urbe, S. and Clague, M. J. (2006). Systematic analysis of myotubularins: heteromeric interactions, subcellular localisation and endosome related functions. J. Cell Sci. 119, 2953-2959. (Pubitemid 44177873)
25. Mohi, M. G. and Neel, B. G. (2007). The role of Shp2 (PTPN11) in cancer. Curr. Opin. Genet. Dev. 17, 23-30.
26. Mohi, M. G., Williams, I. R., Dearolf, C. R., Chan, G., Kutok, J. L., Cohen, S., Morgan, K., Boulton, C., Shigematsu, H., Keilhack, H. et al. (2005). Prognostic, therapeutic, and mechanistic implications of a mouse model of leukemia evoked by Shp2 (PTPN11) mutations. Cancer Cell 7, 179-191. (Pubitemid 40248343)
27. Murray, J. T., Panaretou, C., Stenmark, H., Miaczynska, M. and Backer, J. M. (2002). Role of Rab5 in the recruitment of hVps34/p150 to the early endosome. Traffic 3, 416-427.
28. Obara, K., Noda, T., Niimi, K. and Ohsumi, Y. (2008a). Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells 13, 537-547. (Pubitemid 351761772)
29. Obara, K., Sekito, T., Niimi, K. and Ohsumi, Y. (2008b). The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J. Biol. Chem. 283, 23972-23980.
30. Petiot, A., Ogier-Denis, E., Blommaart, E. F., Meijer, A. J. and Codogno, P. (2000). Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275, 992-998. (Pubitemid 30051145)
31. Proikas-Cezanne, T., Waddell, S., Gaugel, A., Frickey, T., Lupas, A. and Nordheim, A. (2004). WIPI-1alpha (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene 23, 9314-9325. (Pubitemid 40069664)
32. Pulido, R., Serra-Pages, C., Tang, M. and Streuli, M. (1995). The LAR/PTP delta/PTP sigma subfamily of transmembrane protein-tyrosine-phosphatases: multiple human LAR, PTP delta, and PTP sigma isoforms are expressed in a tissue-specific manner and associate with the LAR-interacting protein LIP.1. Proc. Natl. Acad. Sci. USA 92, 11686-11690.
33. Ruhe, J. E., Streit, S., Hart, S. and Ullrich, A. (2006). EGFR signaling leads to downregulation of PTP-LAR via TACE-mediated proteolytic processing. Cell. Signal. 18, 1515-1527. (Pubitemid 43832087)
34. Rutherford, A. C., Traer, C., Wassmer, T., Pattni, K., Bujny, M. V., Carlton, J. G., Stenmark, H. and Cullen, P. J. (2006). The mammalian phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) regulates endosome-to-TGN retrograde transport. J. Cell Sci. 119, 3944-3957. (Pubitemid 44650868)
35. Taguchi-Atarashi, N., Hamasaki, M., Matsunaga, K., Omori, H., Ktistakis, N. T., Yoshimori, T. and Noda, T. (2010). Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy. Traffic 11, 468-478.
36. Tanida, I., Minematsu-Ikeguchi, N., Ueno, T. and Kominami, E. (2005). Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1, 84-91.
37. Uetani, N., Chagnon, M. J., Kennedy, T. E., Iwakura, Y. and Tremblay, M. L. (2006). Mammalian motoneuron axon targeting requires receptor protein tyrosine phosphatases sigma and delta. J. Neurosci. 26, 5872-5880.
38. Vergne, I., Roberts, E., Elmaoued, R. A., Tosch, V., Delgado, M. A., Proikas-Cezanne, T., Laporte, J. and Deretic, V. (2009). Control of autophagy initiation by phosphoinositide 3-phosphatase jumpy. EMBO J. 28, 2244-2258.
39. Wallace, M. J., Batt, J., Fladd, C. A., Henderson, J. T., Skarnes, W. and Rotin, D. (1999). Neuronal defects and posterior pituitary hypoplasia in mice lacking the receptor tyrosine phosphatase PTPsigma. Nat. Genet. 21, 334-338. (Pubitemid 29124947)
40. Walsh, J. P., Caldwell, K. K. and Majerus, P. W. (1991). Formation of phosphatidylinositol 3-phosphate by isomerization from phosphatidylinositol 4-phosphate. Proc. Natl. Acad. Sci. USA 88, 9184-9187.
41. Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., Heintz, N. and Yue, Z. (2009). Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 11, 468-476.