Classes of phosphoinositide 3-kinases at a glance

Journal of Cell Science

Volumn 127, Issue 5, 2014, Pages 923-928

  Jean, Steve ^a   Kiger, Amy A ^a  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

Author keywords

Class I PI3K; Class II PI3K; Class III PI3K; Phosphoinositide; PI3 kinases; PI3K

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PHOSPHATASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE;

AGING; ARTICLE; AUTOPHAGOSOME; BIOCHEMICAL COMPOSITION; CAENORHABDITIS ELEGANS; CELL FUNCTION; CELL MEMBRANE; CELL METABOLISM; CELL MIGRATION; CELL SIZE; CYTOLOGY; DIABETES MELLITUS; GENE DELETION; GENETIC LINKAGE; HUMAN; INTRACELLULAR MEMBRANE; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY;

CLASS I PI3K; CLASS II PI3K; CLASS III PI3K; PHOSPHOINOSITIDE; PI3-KINASES; PI3K;

ANIMALS; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 84896809204     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.093773     Document Type: Article

References (80)

1. Araki, Y., Ku, W.-C., Akioka, M., May, A. I., Hayashi, Y., Arisaka, F., Ishihama, Y. and Ohsumi, Y. (2013). Atg38 is required for autophagy-specific phosphatidylinositol 3-kinase complex integrity. J. Cell Biol. 203, 299-313.
2. Backer, J. M. (2008). The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem. J. 410, 1-17.
3. Behrends, C., Sowa, M. E., Gygi, S. P. and Harper, J. W. (2010). Network organization of the human autophagy system. Nature 466, 68-76.
4. Biswas, K., Yoshioka, K., Asanuma, K., Okamoto, Y., Takuwa, N., Sasaki, T. and Takuwa, Y. (2013). Essential role of class II phosphatidylinositol-3- kinase-C2a in sphingosine 1-phosphate receptor-1-mediated signaling and migration in endothelial cells. J. Biol. Chem. 288, 2325-2339.
5. Bridges, D., Ma, J. T., Park, S., Inoki, K., Weisman, L. S. and Saltiel, A. R. (2012). Phosphatidylinositol 3,5-bisphosphate plays a role in the activation and subcellular localization of mechanistic target of rapamycin 1. Mol. Biol. Cell 23, 2955-2962.
6. Brown, J. R. and Auger, K. R. (2011). Phylogenomics of phosphoinositide lipid kinases: perspectives on the evolution of second messenger signaling and drug discovery. BMC Evol. Biol. 11, 4.
7. Cao, C., Laporte, J., Backer, J. M., Wandinger-Ness, A. and Stein, M.-P. (2007). Myotubularin lipid phosphatase binds the hVPS15/hVPS34 lipid kinase complex on endosomes. Traffic 8, 1052-1067.
8. Carracedo, A. and Pandolfi, P. P. (2008). The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene 27, 5527-5541.
9. Castellano, E. and Downward, J. (2011). RAS interaction with PI3K: more than just another effector pathway. Genes Cancer 2, 261-274.
10. Chagpar, R. B., Links, P. H., Pastor, M. C., Furber, L. A., Hawrysh, A. D., Chamberlain, M. D. and Anderson, D. H. (2010). Direct positive regulation of PTEN by the p85 subunit of phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 107, 5471-5476.
11. Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S. C., Waterfield, M. D., Backer, J. M. and Zerial, M. (1999). Phosphatidylinositol-3- OH kinases are Rab5 effectors. Nat. Cell Biol. 1, 249-252.
12. Cullen, P. J. (2008). Endosomal sorting and signalling: an emerging role for sorting nexins. Nat. Rev. Mol. Cell Biol. 9, 574-582.
13. Das, M., Scappini, E., Martin, N. P., Wong, K. A., Dunn, S., Chen, Y. J., Miller, S. L., Domin, J. and O'Bryan, J. P. (2007). Regulation of neuron survival through an intersectin-phosphoinositide 3'-kinase C2beta-AKT pathway. Mol. Cell. Biol. 27, 7906-7917.
14. Dbouk, H. A., Vadas, O., Shymanets, A., Burke, J. E., Salamon, R. S., Khalil, B. D., Barrett, M. O., Waldo, G. L., Surve, C., Hsueh, C. et al. (2012). G protein-coupled receptor-mediated activation of p110β by Gβγ is required for cellular transformation and invasiveness. Sci. Signal. 5, ra89.
15. Devereaux, K., Dall'armi, C., Alcazar-Roman, A., Ogasawara, Y., Zhou, X., Wang, F., Yamamoto, A., De Camilli, P. and Di Paolo, G. (2013). Regulation of mammalian autophagy by class II and III PI 3-kinases through PI3P synthesis. PLoS ONE 8, e76405.
16. Di Paolo, G. and De Camilli, P. (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657.
17. Dou, Z., Chattopadhyay, M., Pan, J. A., Guerriero, J. L., Jiang, Y. P., Ballou, L. M., Yue, Z., Lin, R. Z. and Zong, W. X. (2010). The class IA phosphatidylinositol 3-kinase p110-beta subunit is a positive regulator of autophagy. J. Cell Biol. 191, 827-843.
18. Dou, Z., Pan, J. A., Dbouk, H. A., Ballou, L. M., DeLeon, J. L., Fan, Y., Chen, J. S., Liang, Z., Li, G., Backer, J. M. et al. (2013). Class IA PI3K p110β subunit promotes autophagy through Rab5 small GTPase in response to growth factor limitation. Mol. Cell 50, 29-42.
19. Engelman, J. A., Luo, J. and Cantley, L. C. (2006). The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7, 606-619.
20. Falasca, M. and Maffucci, T. (2012). Regulation and cellular functions of class II phosphoinositide 3-kinases. Biochem. J. 443, 587-601.
21. Flannagan, R. S., Jaumouillé , V. and Grinstein, S. (2012). The cell biology of phagocytosis. Annu. Rev. Pathol. 7, 61-98.
22. Fritsch, R., de Krijger, I., Fritsch, K., George, R., Reason, B., Kumar, M. S., Diefenbacher, M., Stamp, G. and Downward, J. (2013). RAS and RHO families of GTPases directly regulate distinct phosphoinositide 3-kinase isoforms. Cell 153, 1050-1063.
23. Funderburk, S. F., Wang, Q. J. and Yue, Z. (2010). The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol. 20, 355-362.
24. Gaidarov, I., Smith, M. E., Domin, J. and Keen, J. H. (2001). The class II phosphoinositide 3-kinase C2alpha is activated by clathrin and regulates clathrin-mediated membrane trafficking. Mol. Cell 7, 443-449.
25. Guillermet-Guibert, J., Bjorklof, K., Salpekar, A., Gonella, C., Ramadani, F., Bilancio, A., Meek, S., Smith, A. J. H., Okkenhaug, K. and Vanhaesebroeck, B. (2008). The p110beta isoform of phosphoinositide 3-kinase signals downstream of G protein-coupled receptors and is functionally redundant with p110gamma. Proc. Natl. Acad. Sci. USA 105, 8292-8297.
26. Hawkins, P. T. Anderson, K. E., Davidson, K. and Stephens, L. R. (2006). Signalling through Class I PI3Ks in mammalian cells. Biochem. Soc. Trans. 34, 647-662.
27. Hawkins, P. T., Stephens, L. R., Suire, S. and Wilson, M. (2010). PI3K signaling in neutrophils. Curr. Top. Microbiol. Immunol. 346, 183-202.
28. Hirsch, E., Braccini, L., Ciraolo, E., Morello, F. and Perino, A. (2009). Twice upon a time: PI3K's secret double life exposed. Trends Biochem. Sci. 34, 244-248.
29. Ivetac, I., Munday, A. D., Kisseleva, M. V., Zhang, X. M., Luff, S., Tiganis, T., Whisstock, J. C., Rowe, T., Majerus, P. W. and Mitchell, C. A. (2005). The type Ialpha inositol polyphosphate 4-phosphatase generates and terminates phosphoinositide 3-kinase signals on endosomes and the plasma membrane. Mol. Biol. Cell 16, 2218-2233.
30. Jaber, N., Dou, Z., Chen, J. S., Catanzaro, J., Jiang, Y. P., Ballou, L. M., Selinger, E., Ouyang, X., Lin, R. Z., Zhang, J. et al. (2012). Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc. Natl. Acad. Sci. USA 109, 2003-2008.
31. Jackson, S. P., Schoenwaelder, S. M., Matzaris, M., Brown, S. and Mitchell, C. A. (1995). Phosphatidylinositol 3,4,5-trisphosphate is a substrate for the 75 kDa inositol polyphosphate 5-phosphatase and a novel 5-phosphatase which forms a complex with the p85/p110 form of phosphoinositide 3-kinase. EMBO J. 14, 4490-4500.
32. Jean, S. and Kiger, A. A. (2012). Coordination between RAB GTPase and phosphoinositide regulation and functions. Nat. Rev. Mol. Cell Biol. 13, 463-470.
33. Jean, S., Cox, S., Schmidt, E. J., Robinson, F. L. and Kiger, A. (2012). Sbf/ MTMR13 coordinates PI(3)P and Rab21 regulation in endocytic control of cellular remodeling. Mol. Biol. Cell 23, 2723-2740.
34. Kenyon, C. (2005). The plasticity of aging: insights from long-lived mutants. Cell 120, 449-460.
35. Kim, J., Kim, Y. C., Fang, C., Russell, R. C., Kim, J. H., Fan, W., Liu, R., Zhong, Q. and Guan, K. L. (2013). Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 152, 290-303.
36. Kok, K., Geering, B. and Vanhaesebroeck, B. (2009). Regulation of phosphoinositide 3-kinase expression in health and disease. Trends Biochem. Sci. 34, 115-127.
37. Krag, C., Malmberg, E. K. and Salcini, A. E. (2010). PI3KC2a, a class II PI3K, is required for dynamin-independent internalization pathways. J. Cell Sci. 123, 4240-4250.
38. Kumar, A., Redondo-Muñoz, J., Perez-García, V., Cortes, I., Chagoyen, M. and Carrera, A. C. (2011). Nuclear but not cytosolic phosphoinositide 3-kinase beta has an essential function in cell survival. Mol. Cell. Biol. 31, 2122-2133.
39. Kurek, K. C., Luks, V. L., Ayturk, U. M., Alomari, A. I., Fishman, S. J., Spencer, S. A., Mulliken, J. B., Bowen, M. E., Yamamoto, G. L., Kozakewich, H. P. et al. (2012). Somatic mosaic activating mutations in PIK3CA cause CLOVES syndrome. Am. J. Hum. Genet. 90, 1108-1115.
40. Leibiger, B., Moede, T., Uhles, S., Barker, C. J., Creveaux, M., Domin, J., Berggren, P. O. and Leibiger, I. B. (2010). Insulin-feedback via PI3K-C2alpha activated PKBalpha/Akt1 is required for glucose-stimulated insulin secretion. FASEB J. 24, 1824-1837.
41. Lemmon, M. A. (2008). Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111.
42. Leverrier, Y., Okkenhaug, K., Sawyer, C., Bilancio, A., Vanhaesebroeck, B. and Ridley, A. J. (2003). Class I phosphoinositide 3-kinase p110eta is required for apoptotic cell and Fcgamma receptor-mediated phagocytosis by macrophages. J. Biol. Chem. 278, 38437-38442.
43. Lu, N., Shen, Q., Mahoney, T. R., Neukomm, L. J., Wang, Y. and Zhou, Z. (2012). Two PI 3-kinases and one PI 3-phosphatase together establish the cyclic waves of phagosomal PtdIns(3)P critical for the degradation of apoptotic cells. PLoS Biol. 10, e1001245.
44. MacDougall, L. K., Domin, J. and Waterfield, M. D. (1995). A family of phosphoinositide 3-kinases in Drosophila identifies a new mediator of signal transduction. Curr. Biol. 5, 1404-1415.
45. Mazza, S. and Maffucci, T. (2011). Class II phosphoinositide 3-kinase C2alpha: what we learned so far. Int. J. Biochem. Mol. Biol. 2, 168-182.
46. McLaughlin, S. and Murray, D. (2005). Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611.
47. Morel, E., Chamoun, Z., Lasiecka, Z. M., Chan, R. B., Williamson, R. L., Vetanovetz, C., Dall'Armi, C., Simoes, S., Point Du Jour, K. S., McCabe, B. D. et al. (2013). Phosphatidylinositol-3-phosphate regulates sorting and processing of amyloid precursor protein through the endosomal system. Nat. Commun. 4, 2250.
48. Munday, A. D., Norris, F. A., Caldwell, K. K., Brown, S., Majerus, P. W. and Mitchell, C. A. (1999). The inositol polyphosphate 4-phosphatase forms a complex with phosphatidylinositol 3-kinase in human platelet cytosol. Proc. Natl. Acad. Sci. USA 96, 3640-3645.
49. Nemazanyy, I., Blaauw, B., Paolini, C., Caillaud, C., Protasi, F., Mueller, A., Proikas-Cezanne, T., Russell, R. C., Guan, K. L., Nishino, I. et al. (2013). Defects of Vps15 in skeletal muscles lead to autophagic vacuolar myopathy and lysosomal disease. EMBO Mol. Med. 5, 870-890.
50. Nezis, I. P., Sagona, A. P., Schink, K. O. and Stenmark, H. (2010). Divide and ProsPer: the emerging role of PtdIns3P in cytokinesis. Trends Cell Biol. 20, 642-649.
51. Oldham, S. and Hafen, E. (2003). Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol. 13, 79-85.
52. Patrucco, E., Notte, A., Barberis, L., Selvetella, G., Maffei, A., Brancaccio, M., Marengo, S., Russo, G., Azzolino, O., Rybalkin, S. D. et al. (2004). PI3Kgamma modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell 118, 375-387.
53. Platta, H. W. and Stenmark, H. (2011). Endocytosis and signaling. Curr. Opin. Cell Biol. 23, 393-403.
54. Posor, Y., Eichhorn-Gruenig, M., Puchkov, D., Schöneberg, J., Ullrich, A., Lampe, A., Müller, R., Zarbakhsh, S., Gulluni, F., Hirsch, E. et al. (2013). Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499, 233-237.
55. Raiborg, C., Schink, K. O. and Stenmark, H. (2013). Class III phosphatidylinositol 3-kinase and its catalytic product PtdIns3P in regulation of endocytic membrane traffic. FEBS J. 280, 2730-2742.
56. Rauch, J., Volinsky, N., Romano, D. and Kolch, W. (2011). The secret life of kinases: functions beyond catalysis. Cell Commun. Signal. 9, 23.
57. Russell, R. C., Tian, Y., Yuan, H., Park, H.W., Chang, Y. Y., Kim, J., Kim, H., Neufeld, T. P.,Dillin, A. andGuan, K. L. (2013). ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat. Cell Biol. 15, 741-750.
58. Sasaki, T., Takasuga, S., Sasaki, J., Kofuji, S., Eguchi, S., Yamazaki, M. and Suzuki, A. (2009). Mammalian phosphoinositide kinases and phosphatases. Prog. Lipid Res. 48, 307-343.
59. Schink, K. O., Raiborg, C. and Stenmark, H. (2013). Phosphatidylinositol 3- phosphate, a lipid that regulates membrane dynamics, protein sorting and cell signalling. Bioessays 35, 900-912.
60. Schu, P. V., Takegawa, K., Fry, M. J., Stack, J. H., Waterfield, M. D. and Emr, S. D. (1993). Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260, 88-91.
61. Shin, H. W., Hayashi, M., Christoforidis, S., Lacas-Gervais, S., Hoepfner, S., Wenk, M. R., Modregger, J., Uttenweiler-Joseph, S., Wilm, M., Nystuen, A. et al. (2005). An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J. Cell Biol. 170, 607-618.
62. Simonsen, A. and Tooze, S. A. (2009). Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 186, 773-782.
63. Song, M. S., Salmena, L. and Pandolfi, P. P. (2012). The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 13, 283-296.
64. Stahelin, R. V., Karathanassis, D., Bruzik, K. S., Waterfield, M. D., Bravo, J., Williams, R. L. and Cho, W. (2006). Structural and membrane binding analysis of the Phox homology domain of phosphoinositide 3-kinase-C2alpha. J. Biol. Chem. 281, 39396-39406.
65. Tamura, N., Hazeki, K., Okazaki, N., Kametani, Y., Murakami, H., Takaba, Y., Ishikawa, Y., Nigorikawa, K. and Hazeki, O. (2009). Specific role of phosphoinositide 3-kinase p110alpha in the regulation of phagocytosis and pinocytosis in macrophages. Biochem. J. 423, 99-108.
66. Vadas, O., Burke, J. E., Zhang, X., Berndt, A. and Williams, R. L. (2011). Structural basis for activation and inhibition of class I phosphoinositide 3-kinases. Sci. Signal. 4, re2.
67. Vanhaesebroeck, B., Ali, K., Bilancio, A., Geering, B. and Foukas, L. C. (2005). Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem. Sci. 30, 194-204.
68. Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M. and Bilanges, B. (2010a). The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 11, 329-341.
69. Vanhaesebroeck, B., Vogt, P. K. and Rommel, C. (2010b). PI3K: from the bench to the clinic and back. Curr. Top. Microbiol. Immunol. 347, 1-19.
70. Vanhaesebroeck, B., Stephens, L. and Hawkins, P. (2012). PI3K signalling: the path to discovery and understanding. Nat. Rev. Mol. Cell Biol. 13, 195-203.
71. Vicinanza, M., D'Angelo, G., Di Campli, A. and De Matteis, M. A. (2008). Function and dysfunction of the PI system in membrane trafficking. EMBO J. 27, 2457-2470.
72. von Zastrow, M. and Sorkin, A. (2007). Signaling on the endocytic pathway. Curr. Opin. Cell Biol. 19, 436-445.
73. Wada, Y. and Sun-Wada, G. H. (2013). Positive and negative regulation of developmental signaling by the endocytic pathway. Curr. Opin. Genet. Dev. 23, 391-398.
74. Weiger, M. C. and Parent, C. A. (2012). Phosphoinositides in chemotaxis. Subcell. Biochem. 59, 217-254.
75. Wong, K.-K., Engelman, J. A. and Cantley, L. C. (2010). Targeting the PI3K signaling pathway in cancer. Curr. Opin. Genet. Dev. 20, 87-90.
76. Wu, P., Liu, T. and Hu, Y. (2009). PI3K inhibitors for cancer therapy: what has been achieved so far? Curr. Med. Chem. 16, 916-930.
77. Yoo, S. K., Deng, Q., Cavnar, P. J., Wu, Y. I., Hahn, K. M. and Huttenlocher, A. (2010). Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell 18, 226-236.
78. Yoon, M. S., Du, G., Backer, J. M., Frohman, M. A. and Chen, J. (2011). Class III PI-3-kinase activates phospholipase D in an amino acid-sensing mTORC1 pathway. J. Cell Biol. 195, 435-447.
79. Yoshioka, K., Yoshida, K., Cui, H., Wakayama, T., Takuwa, N., Okamoto, Y., Du, W., Qi, X., Asanuma, K., Sugihara, K. et al. (2012). Endothelial PI3K-C2a, a class II PI3K, has an essential role in angiogenesis and vascular barrier function. Nat. Med. 18, 1560-1569.
80. Zoncu, R., Efeyan, A. and Sabatini, D. M. (2011). mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35.