Phosphoinositide 3-kinase p110 δ promotes lumen formation through the enhancement of apico-basal polarity and basal membrane organization

Nature Communications

Volumn 6, Issue , 2015, Pages

  Peng, Juan ^a,b   Awad, Aline ^a,b   Sar, Sokhavuth ^a,b   Hamze Komaiha, Ola ^a,b   Moyano, Romina ^a,b   Rayal, Amel ^a,b   Samuel, Didier ^a,b,c   Shewan, Annette ^d   Vanhaesebroeck, Bart ^e   Mostov, Keith ^f   Gassama Diagne, Ama ^a,b  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b INSERM   (France)

^c HÔPITAL PAUL BROUSSE   (France)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; 2 (6 AMINO 9 PURINYLMETHYL) 5 METHYL 3 (2 METHYLPHENYL) 3H QUINAZOLIN 4 ONE; 5 (6 QUINOXALINYLMETHYLENE) 2,4 THIAZOLIDINEDIONE; ACTIN; ALPHA2 INTEGRIN; ALPHA5 INTEGRIN; BETA CATENIN; BETA1 INTEGRIN; COLLAGEN TYPE 4; DYSTROGLYCAN; FOCAL ADHESION KINASE; IDELALISIB; LAMININ; MESSENGER RNA; PAXILLIN; PHOSPHATIDYLINOSITOL 3 KINASE; PODOCALYXIN; PROTEIN P110 DELTA; PROTEIN KINASE B; PROTEIN P110; PROTEIN P110 ALPHA; PROTEIN P110 BETA; PROTEIN P110 GAMMA; PROTEIN ZO1; RAC1 PROTEIN; TALIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2; VINCULIN; COLLAGEN; ISOPROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; SMALL INTERFERING RNA;

ADHESION; ENZYME ACTIVITY; MEMBRANE; POLARIZATION; PROTEIN; RNA; SIGNALING; THREE-DIMENSIONAL MODELING;

ACTIN FILAMENT; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; BASOLATERAL MEMBRANE; CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL POLARITY; CELL STRUCTURE; CELL SURFACE; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; DOG; ENZYME ACTIVITY; ENZYME LOCALIZATION; EXTRACELLULAR MATRIX; FOCAL ADHESION; GENE DELETION; GENE EXPRESSION; GENE SILENCING; HELA CELL LINE; IC50; IMMUNOBLOTTING; IMMUNOLOCALIZATION; IN VITRO STUDY; KIDNEY EPITHELIUM; MDCK CELL LINE; MEMBRANE STRUCTURE; NONHUMAN; PHENOTYPE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ANIMAL; CELL MEMBRANE; CYTOLOGY; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; CELL ADHESION; CELL MEMBRANE; CELL POLARITY; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; COLLAGEN; DOGS; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HELA CELLS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PAXILLIN; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN ISOFORMS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VINCULIN;

EID: 84923112409     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6937     Document Type: Article

References (70)

1. Bryant, D. M. & Mostov, K. E. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9, 887-901 (2008).
2. Nelson, W. J. Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity. Cold Spring Harb. Perspect. Biol. 1, a000513 (2009).
3. McCaffrey, L. M. & Macara, I. G. Epithelial organization, cell polarity and tumorigenesis. Trends Cell Biol. 21, 727-735 (2011).
4. Wheelock, M. J. & Johnson, K. R. Cadherins as modulators of cellular phenotype. Annu. Rev. Cell Dev. Biol. 19, 207-235 (2003).
5. Nelson, C. M. & Bissell, M. J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 22, 287-309 (2006).
6. Mellman, I. & Nelson, W. J. Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833-845 (2008).
7. Li, R. & Gundersen, G. G. Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat. Rev. Mol. Cell Biol. 9, 860-873 (2008).
8. Goldstein, B. & Macara, I. G. The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622 (2007).
9. Asnacios, A. & Hamant, O. The mechanics behind cell polarity. Trends Cell Biol. 22, 584-591 (2012).
10. Goehring, N. W. & Grill, S. W. Cell polarity: mechanochemical patterning. Trends Cell Biol. 23, 72-80 (2013).
11. Gibson, M. C. & Perrimon, N. Apicobasal polarization: epithelial form and function. Curr. Opin. Cell Biol. 15, 747-752 (2003).
12. Vanhaesebroeck, B., Vogt, P. K. & Rommel, C. PI3K: from the bench to the clinic and back. Curr. Top. Microbiol. Immunol. 347, 1-19 (2010).
13. Kok, K. et al. Regulation of p110delta PI 3-kinase gene expression. PLoS ONE 4, e5145 (2009).
14. Di Paolo, G. & De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (2006).
15. Comer, F. I. & Parent, C. A. Phosphoinositides specify polarity during epithelial organ development. Cell 128, 239-240 (2007).
16. Gassama-Diagne, A. & Payrastre, B. Phosphoinositide signaling pathways: promising role as builders of epithelial cell polarity. Int. Rev. Cell Mol. Biol. 273, 313-343 (2009).
17. Shewan, A., Eastburn, D. J. & Mostov, K. Phosphoinositides in cell architecture. Cold Spring Harb. Perspect. Biol. 3, a004796 (2011).
18. Krahn, M. P. & Wodarz, A. Phosphoinositide lipids and cell polarity: linking the plasma membrane to the cytocortex. Essays Biochem. 53, 15-27 (2012).
19. Backers, K., Blero, D., Paternotte, N., Zhang, J. & Erneux, C. The termination of PI3K signalling by SHIP1 and SHIP2 inositol 5-phosphatases. Adv. Enzyme Regul. 43, 15-28 (2003).
20. Leslie, N. R., Batty, I. H., Maccario, H., Davidson, L. & Downes, C. P. Understanding PTEN regulation: PIP2, polarity and protein stability. Oncogene 27, 5464-5476 (2008).
21. Gassama-Diagne, A. et al. Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat. Cell Biol. 8, 963-970 (2006).
22. Martin-Belmonte, F. et al. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128, 383-397 (2007).
23. Awad, A. et al. SHIP2 regulates epithelial cell polarity through its lipid product, which binds to Dlg1, a pathway subverted by hepatitis C virus core protein. Mol. Biol. Cell 24, 2171-2185 (2013).
24. Knight, Z. A. et al. A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling. Cell 125, 733-747 (2006).
25. Gopal, A. K. et al. PI3Kd inhibition by idelalisib in patients with relapsed indolent lymphoma. N. Engl. J. Med. 370, 1008-1018 (2014).
26. Furman, R. R. et al. Idelalisib and rituximab in relapsed chronic lymphocytic leukemia. N. Engl. J. Med. 370, 997-1007 (2014).
27. Bryant, D. M. et al. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 12, 1035-1045 (2010).
28. Sawyer, C. et al. Regulation of breast cancer cell chemotaxis by the phosphoinositide 3-kinase p110delta. Cancer Res. 63, 1667-1675 (2003).
29. Tzenaki, N. et al. High levels of p110d PI3K expression in solid tumor cells suppress PTEN activity, generating cellular sensitivity to p110d inhibitors through PTEN activation. FASEB J. 26, 2498-2508 (2012).
30. Whitehead, M. A., Bombardieri, M., Pitzalis, C. & Vanhaesebroeck, B. Isoformselective induction of human p110d PI3K expression by TNFa: identification of a new and inducible PIK3CD promoter. Biochem. J. 443, 857-867 (2012).
31. O'Brien, L. E. et al. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831-838 (2001).
32. Bissell, M. J., Radisky, D. C., Rizki, A., Weaver, V. M. & Petersen, O. W. The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 70, 537-546 (2002).
33. Yu, W. et al. Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell 16, 433-445 (2005).
34. Monteleon, C. L. et al. Establishing epithelial glandular polarity: interlinked roles for ARF6, Rac1, and the matrix microenvironment. Mol. Biol. Cell 23, 4495-4505 (2012).
35. Germena, G. & Hirsch, E. PI3Ks and small GTPases in neutrophil migration: two sides of the same coin. Mol. Immunol. 55, 83-86 (2013).
36. Liu, L. et al. Phosphorylation and inactivation of glycogen synthase kinase-3 by soluble kit ligand in mouse oocytes during early follicular development. J. Mol. Endocrinol. 38, 137-146 (2007).
37. Hohenester, E. & Yurchenco, P. D. Laminins in basement membrane assembly. Cell Adhes. Migr. 7, 56-63 (2013).
38. Cantley, L. C. The phosphoinositide 3-kinase pathway. Science 296, 1655-1657 (2002).
39. Cain, R. J., Vanhaesebroeck, B. & Ridley, A. J. The PI3K p110alpha isoform regulates endothelial adherens junctions via Pyk2 and Rac1. J. Cell Biol. 188, 863-876 (2010).
40. Akhtar, N. & Streuli, C. H. An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium. Nat. Cell Biol. 15, 17-27 (2013).
41. Humphries, J. D., Byron, A. & Humphries, M. J. Integrin ligands at a glance. J. Cell Sci. 119, 3901-3903 (2006).
42. Campbell, I. D. & Humphries, M. J. Integrin structure, activation, and interactions. Cold Spring Harb. Perspect. Biol 3: a004994 (2011).
43. Lee, J. L. & Streuli, C. H. Integrins and epithelial cell polarity. J. Cell Sci. 127, 3217-3225 (2014).
44. Boudreau, N. J. & Jones, P. L. Extracellular matrix and integrin signalling: the shape of things to come. Biochem. J. 339(Pt 3): 481-488 (1999).
45. Zaidel-Bar, R., Milo, R., Kam, Z. & Geiger, B. A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J. Cell Sci. 120, 137-148 (2007).
46. Ervasti, J. M. & Campbell, K. P. Membrane organization of the dystrophinglycoprotein complex. Cell 66, 1121-1131 (1991).
47. Barresi, R. & Campbell, K. P. Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199-207 (2006).
48. Weir, M. L. et al. Dystroglycan loss disrupts polarity and beta-casein induction in mammary epithelial cells by perturbing laminin anchoring. J. Cell Sci. 119, 4047-4058 (2006).
49. Masuda-Hirata, M. et al. Intracellular polarity protein PAR-1 regulates extracellular laminin assembly by regulating the dystroglycan complex. Genes Cells 14, 835-850 (2009).
50. Zhang, L., Seo-Mayer, P. & Caplan, M. J. Dystroglycan and AMP kinase: polarity's protectors when the power goes out. Dev. Cell 16, 1-2 (2009).
51. Bello, V., Sirour, C., Moreau, N., Denker, E. & Darribère, T. A function for dystroglycan in pronephros development in Xenopus laevis. Dev. Biol. 317, 106-120 (2008).
52. Wymann, M. P. & Marone, R. Phosphoinositide 3-kinase in disease: timing, location, and scaffolding. Curr. Opin. Cell Biol. 17, 141-149 (2005).
53. Clayton, E. et al. A crucial role for the p110delta subunit of phosphatidylinositol 3-kinase in B cell development and activation. J. Exp. Med. 196, 753-763 (2002).
54. Okkenhaug, K. et al. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 297, 1031-1034 (2002).
55. Rommel, C., Camps, M. & Ji, H. PI3K delta and PI3K gamma: partners in crime in inflammation in rheumatoid arthritis and beyond? Nat. Rev. Immunol. 7, 191-201 (2007).
56. Rodon, J., Dienstmann, R., Serra, V. & Tabernero, J. Development of PI3K inhibitors: lessons learned from early clinical trials. Nat. Rev. Clin. Oncol. 10, 143-153 (2013).
57. Vanhaesebroeck, B. & Khwaja, A. PI3Kd inhibition hits a sensitive spot in B cell malignancies. Cancer Cell 25, 269-271 (2014).
58. Knight, Z. A. & Shokat, K. M. Chemically targeting the PI3K family. Biochem. Soc. Trans. 35, 245-249 (2007).
59. Vanhaesebroeck, B., Stephens, L. & Hawkins, P. PI3K signalling: the path to discovery and understanding. Nat. Rev. Mol. Cell Biol. 13, 195-203 (2012).
60. Shugg, R. P. P. et al. Effects of isoform-selective phosphatidylinositol 3-kinase inhibitors on osteoclasts: actions on cytoskeletal organization, survival and resorption. J. Biol. Chem. 288, 35346-35357 (2013).
61. Juvin, V. et al. Signaling via class IA phosphoinositide 3-kinases (PI3K) in human, breast-derived cell lines. PLoS ONE 8, e75045 (2013).
62. Berndt, A. et al. The p110 delta structure: mechanisms for selectivity and potency of new PI(3)K inhibitors. Nat. Chem. Biol. 6, 117-124 (2010).
63. Tzenaki, N. & Papakonstanti, E. A. p110d PI3 kinase pathway: emerging roles in cancer. Front. Oncol. 3, 40 (2013).
64. Angulo, I. et al. Phosphoinositide 3-kinase d gene mutation predisposes to respiratory infection and airway damage. Science 342, 866-871 (2013).
65. Zeller, K. S. et al. PI3-kinase p110a mediates b1 integrin-induced Akt activation and membrane protrusion during cell attachment and initial spreading. Cell. Signal. 22, 1838-1848 (2010).
66. Zamir, E. & Geiger, B. Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114, 3583-3590 (2001).
67. Schoenwaelder, S. M. et al. Phosphoinositide 3-kinase p110 beta regulates integrin alpha IIb beta 3 avidity and the cellular transmission of contractile forces. J. Biol. Chem. 285, 2886-2896 (2010).
68. Fritsch, R. et al. RAS and RHO families of GTPases directly regulate distinct phosphoinositide 3-kinase isoforms. Cell 153, 1050-1063 (2013).
69. Constantin, B. Dystrophin complex functions as a scaffold for signalling proteins. Biochim. Biophys. Acta 1838, 635-642 (2013).
70. Lu, P., Takai, K., Weaver, V. M. & Werb, Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb. Perspect. Biol. 3: a005058 (2011).