Mammalian erythroblast enucleation requires PI3K-dependent cell polarization

Journal of Cell Science

Volumn 125, Issue 2, 2012, Pages 340-349

  Wang, Junxia ^a   Ramirez, Tzutzuy ^a   Ji, Peng ^b,d   Jayapal, Senthil Raja ^b,c   Lodish, Harvey F ^b   Murata Hori, Maki ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cell polarization; Erythroblast enucleation; Microtubules; PI3 kinase

Indexed keywords

ACTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELL SURFACE; CYTOPLASM; DEPOLYMERIZATION; ENUCLEATION; ERYTHROBLAST; FETUS; LOCOMOTION; MICROTUBULE; MOUSE; NONHUMAN; POLARIZATION; PRESSURE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VISCOELASTICITY;

ANIMALS; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CELL POLARITY; CELLS, CULTURED; CYTOPLASM; ERYTHROBLASTS; ERYTHROPOIESIS; MICE; MICE, INBRED C57BL; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; PHOSPHATIDYLINOSITOL 3-KINASE;

MAMMALIA;

EID: 84863255694     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.088286     Document Type: Article

References (39)

1. Charras, G. and Paluch, E. (2008). Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 9, 730-736.
2. Franke, T. F., Kaplan, D. R., Cantley, L. C. and Toker, A. (1997). Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275, 665-668.
3. Ghaffari, S., Kitidis, C., Zhao, W., Marinkovic, D., Fleming, M. D., Luo, B., Marszalek, J. and Lodish, H. F. (2006). AKT induces erythroid-cell maturation of JAK2-deficient fetal liver progenitor cells and is required for Epo regulation of erythroid-cell differentiation. Blood 107, 1888-1891.
4. Gomes, E. R., Jani, S. and Gundersen, G. G. (2005). Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451-463.
5. Han, J., Luby-Phelps, K., Das, B., Shu, X., Xia, Y., Mosteller, R. D., Krishna, U. M., Falck, J. R., White, M. A. and Broek, D. (1998). Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279, 558-560.
6. Haston, W. S. and Shields, J. M. (1984). Contraction waves in lymphocyte locomotion. J. Cell Sci. 68, 227-241.
7. Haugh, J. M., Codazzi, F., Teruel, M. and Meyer, T. (2000). Spatial sensing in fibroblasts mediated by 39 phosphoinositides. J. Cell Biol. 151, 1269-1280.
8. Ihle, J. N. and Gilliland, D. G. (2007). Jak2: normal function and role in hematopoietic disorders. Curr. Opin. Genet. Dev. 17, 8-14.
9. Inukai, K., Funaki, M., Nawano, M., Katagiri, H., Ogihara, T., Anai, M., Onishi, Y., Sakoda, H., Ono, H., Fukushima, Y. et al. (2000). The N-terminal 34 residues of the 55 kDa regulatory subunits of phosphoinositide 3-kinase interact with tubulin. Biochem. J. 346, 483-489.
10. Janmey, P. A., Iida, K., Yin, H. L. and Stossel, T. P. (1987). Polyphosphoinositide micelles and polyphosphoinositide-containing vesicles dissociate endogenous gelso- lin-actin complexes and promote actin assembly from the fast-growing end of actin filaments blocked by gelsolin. J. Biol. Chem. 262, 12228-12236.
11. Ji, P., Jayapal, S. R. and Lodish, H. F. (2008). Enucleation of cultured mouse fetal erythroblasts requires Rac GTPases and mDia2. Nat. Cell Biol. 10, 314-321.
12. Kapeller, R., Toker, A., Cantley, L. C. and Carpenter, C. L. (1995). Phosphoinositide 3-kinase binds constitutively to alpha/beta-tubulin and binds to gamma-tubulin in response to insulin. J. Biol. Chem. 270, 25985-25991.
13. Keerthivasan, G., Small, S., Liu, H., Wickrema, A. and Crispino, J. D. (2010). Vesicle trafficking plays a novel role in erythroblast enucleation. Blood 116, 3331-3340.
14. Khandani, A., Eng, E., Jongstra-Bilen, J., Schreiber, A. D., Douda, D., Samavarchi- Tehrani, P. and Harrison, R. E. (2007). Microtubules regulate PI-3K activity and recruitment to the phagocytic cup during Fcgamma receptor-mediated phagocytosis in nonelicited macrophages. J. Leukoc. Biol. 82, 417-428.
15. Koury, M. J., Sawyer, S. T. and Brandt, S. J. (2002). New insights into erythropoiesis. Curr. Opin. Hematol. 9, 93-100.
16. Koury, S. T., Koury, M. J. and Bondurant, M. C. (1989). Cytoskeletal distribution and function during the maturation and enucleation of mammalian erythroblasts. J. Cell Biol. 109, 3005-3013.
17. Kunisaki, Y., Nishikimi, A., Tanaka, Y., Takii, R., Noda, M., Inayoshi, A., Watanabe, K., Sanematsu, F., Sasazuki, T., Sasaki, T. et al. (2006). DOCK2 is a Rac activator that regulates motility and polarity during neutrophil chemotaxis. J. Cell Biol. 174, 647-652.
18. Lassing, I. and Lindberg, U. (1985). Specific interaction between phosphatidylinositol 4,5-bisphosphate and profilactin. Nature 314, 472-474.
19. Luo, J., Field, S. J., Lee, J. Y., Engelman, J. A. and Cantley, L. C. (2005). The p85 regulatory subunit of phosphoinositide 3-kinase down-regulates IRS-1 signaling via the formation of a sequestration complex. J. Cell Biol. 170, 455-464.
20. Matsumura, F., Ono, S., Yamakita, Y., Totsukawa, G. and Yamashiro, S. (1998). Specific localization of serine 19 phosphorylated myosin II during cell locomotion and mitosis of cultured cells. J. Cell Biol. 140, 119-129.
21. McKenna, N. M. and Wang, Y. L. (1989). Culturing cells on the microscope stage. Methods Cell Biol. 29, 195-205.
22. Mimori-Kiyosue, Y., Shiina, N. and Tsukita, S. (2000). The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr. Biol. 10, 865-868.
23. Mukhina, S., Wang, Y. L. and Murata-Hori, M. (2007). Alpha-actinin is required for tightly regulated remodeling of the actin cortical network during cytokinesis. Dev. Cell 13, 554-565.
24. Paluch, E., Sykes, C., Prost, J. and Bornens, M. (2006). Dynamic modes of the cortical actomyosin gel during cell locomotion and division. Trends Cell Biol. 16,5-10.
25. Parent, C. A., Blacklock, B. J., Froehlich, W. M., Murphy, D. B. and Devreotes, P. N. (1998). G protein signaling events are activated at the leading edge of chemotactic cells. Cell 95, 81-91.
26. Repasky, E. A. and Eckert, B. S. (1981). The effect of cytochalasin B on the enucleation of erythroid cells in vitro. Cell Tissue Res. 221, 85-91.
27. Richmond, T. D., Chohan, M. and Barber, D. L. (2005). Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol. 15, 146-155.
28. Schmoranzer, J., Fawcett, J. P., Segura, M., Tan, S., Vallee, R. B., Pawson, T. and Gundersen, G. G. (2009). Par3 and dynein associate to regulate local microtubule dynamics and centrosome orientation during migration. Curr. Biol. 19, 1065-1074.
29. Servant, G., Weiner, O. D., Herzmark, P., Balla, T., Sedat, J. W. and Bourne, H. R. (2000). Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287, 1037-1040.
30. Simpson, C. F. and Kling, J. M. (1967). The mechanism of denucleation in circulating erythroblasts. J. Cell Biol. 35, 237-245.
31. Skutelsky, E. and Danon, D. (1967). An electron microscopic study of nuclear elimination from the late erythroblast. J. Cell Biol. 33, 625-635.
32. Sonoda, Y., Sasaki, K., Suda, M., Itano, C. and Iwatsuki, H. (1998). Effects of colchicine on the enucleation of erythroid cells and macrophages in the liver of mouse embryos: ultrastructural and three-dimensional studies. Anat. Rec. 251, 290-296.
33. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R. and Mitchison, T. J. (2003). Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299, 1743-1747.
34. Wang, Y. L. (2003). Computational restoration of fluorescence images: noise reduction, deconvolution, and pattern recognition. Methods Cell Biol. 72, 337-348.
35. Wheatley, S. P. and Wang, Y. L. (1998). Indirect immunofluorescence microscopy in cultured cells. Methods Cell Biol. 57, 313-332.
36. Xu, J., Wang, F., Van Keymeulen, A., Rentel, M. and Bourne, H. R. (2005). Neutrophil microtubules suppress polarity and enhance directional migration. Proc. Natl. Acad. Sci. USA 102, 6884-6889.
37. Yoshida, H., Kawane, K., Koike, M., Mori, Y., Uchiyama, Y. and Nagata, S. (2005). Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437, 754-758.
38. Zhang, J., Socolovsky, M., Gross, A. W. and Lodish, H. F. (2003). Role of Ras signaling in erythroid differentiation of mouse fetal liver cells: functional analysis by a flow cytometry-based novel culture system. Blood 102, 3938-3946.
39. Zhao, W., Kitidis, C., Fleming, M. D., Lodish, H. F. and Ghaffari, S. (2006). Erythropoietin stimulates phosphorylation and activation of GATA-1 via the PI3- kinase/AKT signaling pathway. Blood 107, 907-915.