Asymmetric PI3K Signaling Driving Developmental and Regenerative Cell Fate Bifurcation

Cell Reports

Volumn 13, Issue 10, 2015, Pages 2203-2218

  Lin, Wen Hsuan W ^a   Adams, William C ^a   Nish, Simone A ^a   Chen, Yen Hua ^a   Yen, Bonnie ^a   Rothman, Nyanza J ^a   Kratchmarov, Radomir ^a   Okada, Takaharu ^b   Klein, Ulf ^c   Reiner, Steven L ^a  

^a Columbia University ^*  (United States)

^b Institute of Physical and Chemical Research   (Japan)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON REGULATORY FACTOR 4; LYMPHOCYTE ANTIGEN RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR PAX5;

ANIMAL EXPERIMENT; ANTIBODY SECRETING CELL; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL REGENERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINESIS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC CONSERVATION; GLYCOLYSIS; HETEROZYGOSITY; HOMOZYGOSITY; LYMPHOCYTE; METAPHASE; MICROSCOPY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROGENY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TELOPHASE; TRANSCRIPTION REGULATION; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CD8+ T LYMPHOCYTE; CELL LINEAGE; CYTOLOGY; GENE TARGETING; HEMATOPOIETIC STEM CELL; METABOLISM; PHYSIOLOGY; PLASMA CELL;

ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; FLOW CYTOMETRY; GENE KNOCK-IN TECHNIQUES; HEMATOPOIETIC STEM CELLS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; PHOSPHATIDYLINOSITOL 3-KINASES; PLASMA CELLS; SIGNAL TRANSDUCTION;

EID: 84949057974     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.10.072     Document Type: Article

References (78)

1. Araki, K., Turner, A.P., Shaffer, V.O., Gangappa, S., Keller, S.A., Bachmann, M.F., Larsen, C.P., Ahmed, R., mTOR regulates memory CD8 T-cell differentiation. Nature 460 (2009), 108–112.
2. Arsenio, J., Kakaradov, B., Metz, P.J., Kim, S.H., Yeo, G.W., Chang, J.T., Early specification of CD8+ T lymphocyte fates during adaptive immunity revealed by single-cell gene-expression analyses. Nat. Immunol. 15 (2014), 365–372.
3. Barnett, B.E., Ciocca, M.L., Goenka, R., Barnett, L.G., Wu, J., Laufer, T.M., Burkhardt, J.K., Cancro, M.P., Reiner, S.L., Asymmetric B cell division in the germinal center reaction. Science 335 (2012), 342–344.
4. Basso, K., Dalla-Favera, R., Germinal centres and B cell lymphomagenesis. Nat. Rev. Immunol. 15 (2015), 172–184.
5. Bird, J.J., Brown, D.R., Mullen, A.C., Moskowitz, N.H., Mahowald, M.A., Sider, J.R., Gajewski, T.F., Wang, C.R., Reiner, S.L., Helper T cell differentiation is controlled by the cell cycle. Immunity 9 (1998), 229–237.
6. Boudousquié, C., Danilo, M., Pousse, L., Jeevan-Raj, B., Angelov, G.S., Chennupati, V., Zehn, D., Held, W., Differences in the transduction of canonical Wnt signals demarcate effector and memory CD8 T cells with distinct recall proliferation capacity. J. Immunol. 193 (2014), 2784–2791.
7. Buck, M.D., O'Sullivan, D., Pearce, E.L., T cell metabolism drives immunity. J. Exp. Med. 212 (2015), 1345–1360.
8. Calado, D.P., Sasaki, Y., Godinho, S.A., Pellerin, A., Köchert, K., Sleckman, B.P., de Alborán, I.M., Janz, M., Rodig, S., Rajewsky, K., The cell-cycle regulator c-Myc is essential for the formation and maintenance of germinal centers. Nat. Immunol. 13 (2012), 1092–1100.
9. Caro-Maldonado, A., Wang, R., Nichols, A.G., Kuraoka, M., Milasta, S., Sun, L.D., Gavin, A.L., Abel, E.D., Kelsoe, G., Green, D.R., Rathmell, J.C., Metabolic reprogramming is required for antibody production that is suppressed in anergic but exaggerated in chronically BAFF-exposed B cells. J. Immunol. 192 (2014), 3626–3636.
10. Cattoretti, G., Shaknovich, R., Smith, P.M., Jäck, H.M., Murty, V.V., Alobeid, B., Stages of germinal center transit are defined by B cell transcription factor coexpression and relative abundance. J. Immunol. 177 (2006), 6930–6939.
11. Chandel, N.S., Evolution of Mitochondria as Signaling Organelles. Cell Metab. 22 (2015), 204–206.
12. Chang, J.T., Palanivel, V.R., Kinjyo, I., Schambach, F., Intlekofer, A.M., Banerjee, A., Longworth, S.A., Vinup, K.E., Mrass, P., Oliaro, J., et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315 (2007), 1687–1691.
13. Chang, J.T., Ciocca, M.L., Kinjyo, I., Palanivel, V.R., McClurkin, C.E., Dejong, C.S., Mooney, E.C., Kim, J.S., Steinel, N.C., Oliaro, J., et al. Asymmetric proteasome segregation as a mechanism for unequal partitioning of the transcription factor T-bet during T lymphocyte division. Immunity 34 (2011), 492–504.
14. Ciocca, M.L., Barnett, B.E., Burkhardt, J.K., Chang, J.T., Reiner, S.L., Cutting edge: Asymmetric memory T cell division in response to rechallenge. J. Immunol. 188 (2012), 4145–4148.
15. Delogu, A., Schebesta, A., Sun, Q., Aschenbrenner, K., Perlot, T., Busslinger, M., Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity 24 (2006), 269–281.
16. Dengler, H.S., Baracho, G.V., Omori, S.A., Bruckner, S., Arden, K.C., Castrillon, D.H., DePinho, R.A., Rickert, R.C., Distinct functions for the transcription factor Foxo1 at various stages of B cell differentiation. Nat. Immunol. 9 (2008), 1388–1398.
17. Dey-Guha, I., Wolfer, A., Yeh, A.C., G Albeck, J., Darp, R., Leon, E., Wulfkuhle, J., Petricoin, E.F. 3rd, Wittner, B.S., Ramaswamy, S., Asymmetric cancer cell division regulated by AKT. Proc. Natl. Acad. Sci. USA 108 (2011), 12845–12850.
18. Dominguez-Sola, D., Victora, G.D., Ying, C.Y., Phan, R.T., Saito, M., Nussenzweig, M.C., Dalla-Favera, R., The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat. Immunol. 13 (2012), 1083–1091.
19. Falini, B., Fizzotti, M., Pucciarini, A., Bigerna, B., Marafioti, T., Gambacorta, M., Pacini, R., Alunni, C., Natali-Tanci, L., Ugolini, B., et al. A monoclonal antibody (MUM1p) detects expression of the MUM1/IRF4 protein in a subset of germinal center B cells, plasma cells, and activated T cells. Blood 95 (2000), 2084–2092.
20. Fooksman, D.R., Schwickert, T.A., Victora, G.D., Dustin, M.L., Nussenzweig, M.C., Skokos, D., Development and migration of plasma cells in the mouse lymph node. Immunity 33 (2010), 118–127.
21. Gattinoni, L., Zhong, X.S., Palmer, D.C., Ji, Y., Hinrichs, C.S., Yu, Z., Wrzesinski, C., Boni, A., Cassard, L., Garvin, L.M., et al. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med. 15 (2009), 808–813.
22. Germar, K., Dose, M., Konstantinou, T., Zhang, J., Wang, H., Lobry, C., Arnett, K.L., Blacklow, S.C., Aifantis, I., Aster, J.C., Gounari, F., T-cell factor 1 is a gatekeeper for T-cell specification in response to Notch signaling. Proc. Natl. Acad. Sci. USA 108 (2011), 20060–20065.
23. Habib, S.J., Chen, B.C., Tsai, F.C., Anastassiadis, K., Meyer, T., Betzig, E., Nusse, R., A localized Wnt signal orients asymmetric stem cell division in vitro. Science 339 (2013), 1445–1448.
24. Hawkins, E.D., Oliaro, J., Kallies, A., Belz, G.T., Filby, A., Hogan, T., Haynes, N., Ramsbottom, K.M., Van Ham, V., Kinwell, T., et al. Regulation of asymmetric cell division and polarity by Scribble is not required for humoral immunity. Nat. Commun., 4, 2013, 1801.
25. Hess Michelini, R., Doedens, A.L., Goldrath, A.W., Hedrick, S.M., Differentiation of CD8 memory T cells depends on Foxo1. J. Exp. Med. 210 (2013), 1189–1200.
26. Hodgkin, P.D., Lee, J.H., Lyons, A.B., B cell differentiation and isotype switching is related to division cycle number. J. Exp. Med. 184 (1996), 277–281.
27. Hodgkin, P.D., Dowling, M.R., Duffy, K.R., Why the immune system takes its chances with randomness. Nat. Rev. Immunol., 14, 2014, 711.
28. Horcher, M., Souabni, A., Busslinger, M., Pax5/BSAP maintains the identity of B cells in late B lymphopoiesis. Immunity 14 (2001), 779–790.
29. Huang, C.Y., Bredemeyer, A.L., Walker, L.M., Bassing, C.H., Sleckman, B.P., Dynamic regulation of c-Myc proto-oncogene expression during lymphocyte development revealed by a GFP-c-Myc knock-in mouse. Eur. J. Immunol. 38 (2008), 342–349.
30. Jang, K.J., Mano, H., Aoki, K., Hayashi, T., Muto, A., Nambu, Y., Takahashi, K., Itoh, K., Taketani, S., Nutt, S.L., et al. Mitochondrial function provides instructive signals for activation-induced B-cell fates. Nat. Commun., 6, 2015, 6750.
31. Jeannet, G., Boudousquié, C., Gardiol, N., Kang, J., Huelsken, J., Held, W., Essential role of the Wnt pathway effector Tcf-1 for the establishment of functional CD8 T cell memory. Proc. Natl. Acad. Sci. USA 107 (2010), 9777–9782.
32. Kallies, A., Hasbold, J., Tarlinton, D.M., Dietrich, W., Corcoran, L.M., Hodgkin, P.D., Nutt, S.L., Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 200 (2004), 967–977.
33. Kallies, A., Hasbold, J., Fairfax, K., Pridans, C., Emslie, D., McKenzie, B.S., Lew, A.M., Corcoran, L.M., Hodgkin, P.D., Tarlinton, D.M., Nutt, S.L., Initiation of plasma-cell differentiation is independent of the transcription factor Blimp-1. Immunity 26 (2007), 555–566.
34. Katajisto, P., Döhla, J., Chaffer, C.L., Pentinmikko, N., Marjanovic, N., Iqbal, S., Zoncu, R., Chen, W., Weinberg, R.A., Sabatini, D.M., Stem cells. Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science 348 (2015), 340–343.
35. Kim, E.H., Sullivan, J.A., Plisch, E.H., Tejera, M.M., Jatzek, A., Choi, K.Y., Suresh, M., Signal integration by Akt regulates CD8 T cell effector and memory differentiation. J. Immunol. 188 (2012), 4305–4314.
36. Kim, M.V., Ouyang, W., Liao, W., Zhang, M.Q., Li, M.O., The transcription factor Foxo1 controls central-memory CD8+ T cell responses to infection. Immunity 39 (2013), 286–297.
37. Kitano, M., Moriyama, S., Ando, Y., Hikida, M., Mori, Y., Kurosaki, T., Okada, T., Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 34 (2011), 961–972.
38. Klein, U., Casola, S., Cattoretti, G., Shen, Q., Lia, M., Mo, T., Ludwig, T., Rajewsky, K., Dalla-Favera, R., Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 7 (2006), 773–782.
39. Lin, Y.C., Jhunjhunwala, S., Benner, C., Heinz, S., Welinder, E., Mansson, R., Sigvardsson, M., Hagman, J., Espinoza, C.A., Dutkowski, J., et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat. Immunol. 11 (2010), 635–643.
40. Man, K., Kallies, A., Synchronizing transcriptional control of T cell metabolism and function. Nat. Rev. Immunol. 15 (2015), 574–584.
41. Man, K., Miasari, M., Shi, W., Xin, A., Henstridge, D.C., Preston, S., Pellegrini, M., Belz, G.T., Smyth, G.K., Febbraio, M.A., et al. The transcription factor IRF4 is essential for TCR affinity-mediated metabolic programming and clonal expansion of T cells. Nat. Immunol. 14 (2013), 1155–1165.
42. Manning, B.D., Cantley, L.C., AKT/PKB signaling: navigating downstream. Cell 129 (2007), 1261–1274.
43. Mansson, R., Welinder, E., Åhsberg, J., Lin, Y.C., Benner, C., Glass, C.K., Lucas, J.S., Sigvardsson, M., Murre, C., Positive intergenic feedback circuitry, involving EBF1 and FOXO1, orchestrates B-cell fate. Proc. Natl. Acad. Sci. USA 109 (2012), 21028–21033.
44. Metz, P.J., Arsenio, J., Kakaradov, B., Kim, S.H., Remedios, K.A., Oakley, K., Akimoto, K., Ohno, S., Yeo, G.W., Chang, J.T., Regulation of asymmetric division and CD8+ T lymphocyte fate specification by protein kinase Cζ and protein kinase Cλ/ι. J. Immunol. 194 (2015), 2249–2259.
45. Nayar, R., Schutten, E., Bautista, B., Daniels, K., Prince, A.L., Enos, M., Brehm, M.A., Swain, S.L., Welsh, R.M., Berg, L.J., Graded levels of IRF4 regulate CD8+ T cell differentiation and expansion, but not attrition, in response to acute virus infection. J. Immunol. 192 (2014), 5881–5893.
46. Nera, K.P., Kohonen, P., Narvi, E., Peippo, A., Mustonen, L., Terho, P., Koskela, K., Buerstedde, J.M., Lassila, O., Loss of Pax5 promotes plasma cell differentiation. Immunity 24 (2006), 283–293.
47. Neumüller, R.A., Knoblich, J.A., Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 23 (2009), 2675–2699.
48. Nutt, S.L., Heavey, B., Rolink, A.G., Busslinger, M., Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature 401 (1999), 556–562.
49. Ochiai, K., Maienschein-Cline, M., Mandal, M., Triggs, J.R., Bertolino, E., Sciammas, R., Dinner, A.R., Clark, M.R., Singh, H., A self-reinforcing regulatory network triggered by limiting IL-7 activates pre-BCR signaling and differentiation. Nat. Immunol. 13 (2012), 300–307.
50. Ochiai, K., Maienschein-Cline, M., Simonetti, G., Chen, J., Rosenthal, R., Brink, R., Chong, A.S., Klein, U., Dinner, A.R., Singh, H., Sciammas, R., Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4. Immunity 38 (2013), 918–929.
51. Omori, S.A., Cato, M.H., Anzelon-Mills, A., Puri, K.D., Shapiro-Shelef, M., Calame, K., Rickert, R.C., Regulation of class-switch recombination and plasma cell differentiation by phosphatidylinositol 3-kinase signaling. Immunity 25 (2006), 545–557.
52. Pape, K.A., Kouskoff, V., Nemazee, D., Tang, H.L., Cyster, J.G., Tze, L.E., Hippen, K.L., Behrens, T.W., Jenkins, M.K., Visualization of the genesis and fate of isotype-switched B cells during a primary immune response. J. Exp. Med. 197 (2003), 1677–1687.
53. Pape, K.A., Taylor, J.J., Maul, R.W., Gearhart, P.J., Jenkins, M.K., Different B cell populations mediate early and late memory during an endogenous immune response. Science 331 (2011), 1203–1207.
54. Pearce, E.L., Walsh, M.C., Cejas, P.J., Harms, G.M., Shen, H., Wang, L.S., Jones, R.G., Choi, Y., Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460 (2009), 103–107.
55. Pollizzi, K.N., Powell, J.D., Integrating canonical and metabolic signalling programmes in the regulation of T cell responses. Nat. Rev. Immunol. 14 (2014), 435–446.
56. Raczkowski, F., Ritter, J., Heesch, K., Schumacher, V., Guralnik, A., Höcker, L., Raifer, H., Klein, M., Bopp, T., Harb, H., et al. The transcription factor Interferon Regulatory Factor 4 is required for the generation of protective effector CD8+ T cells. Proc. Natl. Acad. Sci. USA 110 (2013), 15019–15024.
57. Reiner, S.L., Adams, W.C., Lymphocyte fate specification as a deterministic but highly plastic process. Nat. Rev. Immunol. 14 (2014), 699–704.
58. Restrepo, S., Zartman, J.J., Basler, K., Coordination of patterning and growth by the morphogen DPP. Curr. Biol. 24 (2014), R245–R255.
59. Scharer, C.D., Barwick, B.G., Youngblood, B.A., Ahmed, R., Boss, J.M., Global DNA methylation remodeling accompanies CD8 T cell effector function. J. Immunol. 191 (2013), 3419–3429.
60. Schweitzer, J.K., D'Souza-Schorey, C., Finishing the job: cytoskeletal and membrane events bring cytokinesis to an end. Exp. Cell Res. 295 (2004), 1–8.
61. Sciammas, R., Shaffer, A.L., Schatz, J.H., Zhao, H., Staudt, L.M., Singh, H., Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25 (2006), 225–236.
62. Sciammas, R., Li, Y., Warmflash, A., Song, Y., Dinner, A.R., Singh, H., An incoherent regulatory network architecture that orchestrates B cell diversification in response to antigen signaling. Mol. Syst. Biol., 7, 2011, 495.
63. Sengupta, A., Duran, A., Ishikawa, E., Florian, M.C., Dunn, S.K., Ficker, A.M., Leitges, M., Geiger, H., Diaz-Meco, M., Moscat, J., Cancelas, J.A., Atypical protein kinase C (aPKCzeta and aPKClambda) is dispensable for mammalian hematopoietic stem cell activity and blood formation. Proc. Natl. Acad. Sci. USA 108 (2011), 9957–9962.
64. Shi, W., Liao, Y., Willis, S.N., Taubenheim, N., Inouye, M., Tarlinton, D.M., Smyth, G.K., Hodgkin, P.D., Nutt, S.L., Corcoran, L.M., Transcriptional profiling of mouse B cell terminal differentiation defines a signature for antibody-secreting plasma cells. Nat. Immunol. 16 (2015), 663–673.
65. Shih, T.A., Roederer, M., Nussenzweig, M.C., Role of antigen receptor affinity in T cell-independent antibody responses in vivo. Nat. Immunol. 3 (2002), 399–406.
66. Shyh-Chang, N., Daley, G.Q., Cantley, L.C., Stem cell metabolism in tissue development and aging. Development 140 (2013), 2535–2547.
67. Tiemessen, M.M., Baert, M.R., Kok, L., van Eggermond, M.C., van den Elsen, P.J., Arens, R., Staal, F.J., T Cell factor 1 represses CD8+ effector T cell formation and function. J. Immunol. 193 (2014), 5480–5487.
68. Urbánek, P., Wang, Z.Q., Fetka, I., Wagner, E.F., Busslinger, M., Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79 (1994), 901–912.
69. Vander Heiden, M.G., Cantley, L.C., Thompson, C.B., Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324 (2009), 1029–1033.
70. Victora, G.D., Nussenzweig, M.C., Germinal centers. Annu. Rev. Immunol. 30 (2012), 429–457.
71. Wang, R., Dillon, C.P., Shi, L.Z., Milasta, S., Carter, R., Finkelstein, D., McCormick, L.L., Fitzgerald, P., Chi, H., Munger, J., Green, D.R., The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 35 (2011), 871–882.
72. Ward, P.S., Thompson, C.B., Signaling in control of cell growth and metabolism. Cold Spring Harb. Perspect. Biol., 4, 2012, a006783.
73. Weber, B.N., Chi, A.W., Chavez, A., Yashiro-Ohtani, Y., Yang, Q., Shestova, O., Bhandoola, A., A critical role for TCF-1 in T-lineage specification and differentiation. Nature 476 (2011), 63–68.
74. Xu, H., Chaudhri, V.K., Wu, Z., Biliouris, K., Dienger-Stambaugh, K., Rochman, Y., Singh, H., Regulation of bifurcating B cell trajectories by mutual antagonism between transcription factors IRF4 and IRF8. Nat. Immunol., 2015, 10.1038/ni.3287 Published online October 5, 2015.
75. Yao, S., Buzo, B.F., Pham, D., Jiang, L., Taparowsky, E.J., Kaplan, M.H., Sun, J., Interferon regulatory factor 4 sustains CD8(+) T cell expansion and effector differentiation. Immunity 39 (2013), 833–845.
76. Zhao, D.M., Yu, S., Zhou, X., Haring, J.S., Held, W., Badovinac, V.P., Harty, J.T., Xue, H.H., Constitutive activation of Wnt signaling favors generation of memory CD8 T cells. J. Immunol. 184 (2010), 1191–1199.
77. Zhou, X., Xue, H.H., Cutting edge: generation of memory precursors and functional memory CD8+ T cells depends on T cell factor-1 and lymphoid enhancer-binding factor-1. J. Immunol. 189 (2012), 2722–2726.
78. Zhou, X., Yu, S., Zhao, D.M., Harty, J.T., Badovinac, V.P., Xue, H.H., Differentiation and persistence of memory CD8(+) T cells depend on T cell factor 1. Immunity 33 (2010), 229–240.