TY - JOUR PB - NATURE RESEARCH Y1 - 2020/12/17/ VL - 588 A1 - Lee, Jaewoong A1 - Robinson, Mark E A1 - Ma, Ning A1 - Artadji, Dewan A1 - Ahmed, Mohamed A A1 - Xiao, Gang A1 - Sadras, Teresa A1 - Deb, Gauri A1 - Winchester, Janet A1 - Cosgun, Kadriye Nehir A1 - Geng, Huimin A1 - Chan, Lai N A1 - Kume, Kohei A1 - Miettinen, Teemu P A1 - Zhang, Ye A1 - Nix, Matthew A A1 - Klemm, Lars A1 - Chen, Chun Wei A1 - Chen, Jianjun A1 - Khairnar, Vishal A1 - Wiita, Arun P A1 - Thomas-Tikhonenko, Andrei A1 - Farzan, Michael A1 - Jung, Jae U A1 - Weinstock, David M A1 - Manalis, Scott R A1 - Diamond, Michael S A1 - Vaidehi, Nagarajan A1 - Muschen, Markus N2 - Interferon-induced transmembrane protein 3 (IFITM3) has previously been identified as an endosomal protein that blocks viral infection1,2,3. Here we studied clinical cohorts of patients with B cell leukaemia and lymphoma, and identified IFITM3 as a strong predictor of poor outcome. In normal resting B cells, IFITM3 was minimally expressed and mainly localized in endosomes. However, engagement of the B cell receptor (BCR) induced both expression of IFITM3 and phosphorylation of this protein at Tyr20, which resulted in the accumulation of IFITM3 at the cell surface. In B cell leukaemia, oncogenic kinases phosphorylate IFITM3 at Tyr20, which causes constitutive localization of this protein at the plasma membrane. In a mouse model, Ifitm3?/? naive B cells developed in normal numbers; however, the formation of germinal centres and the production of antigen-specific antibodies were compromised. Oncogenes that induce the development of leukaemia and lymphoma did not transform Ifitm3?/? B cells. Conversely, the phosphomimetic IFITM3(Y20E) mutant induced oncogenic PI3K signalling and initiated the transformation of premalignant B cells. Mechanistic experiments revealed that IFITM3 functions as a PIP3 scaffold and central amplifier of PI3K signalling. The amplification of PI3K signals depends on IFITM3 using two lysine residues (Lys83 and Lys104) in its conserved intracellular loop as a scaffold for the accumulation of PIP3. In Ifitm3?/? B cells, lipid rafts were depleted of PIP3, which resulted in the defective expression of over 60 lipid-raft-associated surface receptors, and impaired BCR signalling and cellular adhesion. We conclude that the phosphorylation of IFITM3 that occurs after B cells encounter antigen induces a dynamic switch from antiviral effector functions in endosomes to a PI3K amplification loop at the cell surface. IFITM3-dependent amplification of PI3K signalling, which in part acts downstream of the BCR, is critical for the rapid expansion of B cells with high affinity to antigen. In addition, multiple oncogenes depend on IFITM3 to assemble PIP3-dependent signalling complexes and amplify PI3K signalling for malignant transformation. IS - 7838 JF - Nature EP - 497 AV - public ID - discovery10147988 N1 - This version is the author accepted manuscript. For information on re-use, please refer to the publisher's terms and conditions. TI - IFITM3 functions as a PIP3 scaffold to amplify PI3K signalling in B cells SP - 491 UR - https://doi.org/10.1038/s41586-020-2884-6 ER -