Chronic GVHD (cGVHD) pathogenesis and treatment. Phase I: Inflammation. Pretransplantation conditioning and acute GVHD (aGVHD) cause thymus injury. Phase II: T and B cell dysfunction. The resulting thymic dysfunction impairs donor regulatory T cell (Treg) generation and the negative selection of autoreactive donor T cell clones that escape into the periphery. Balanced Treg/T effector cell reconstitution can be restored by low-dose IL-2 treatment. Donor T follicular helper (Tfh) cells expand in secondary lymphoid organs and promote germinal center (GC) reactions and survival, expansion, and differentiation of donor B cells into antihost-immunoglobulin-producing plasma cells via IL-21 secretion. T follicular regulatory (Tfr) cells suppress Tfh cell:B cell interactions and antibody production. The Rho-associated coiled-coil kinase 2 (ROCK2) inhibitor, KD025, blocks Th17 differentiation and GC reactions by inhibiting Tfh cell generation. Donor B cells receive activating signals via multiple pathways during cGVHD. B cell receptor signaling activates the tyrosine kinase Syk, inhibited by fostamatinib and Entospletinib, and Bruton tyrosine kinase (BTK), inhibited by ibrutinib. IL-21 receptor (IL-21R) signals via the Jak1/2-STAT3 pathway and can be targeted by Jak1/2 inhibitor ruxolitinib or KD025. B cell-activating factor (BAFF) provides crucial prosurvival and mitogenic signals that can be blocked by anti-BAFF antibodies (e.g., belimumab). Donor B cell subsets can be depleted by the anti-CD20 antibody rituximab. Differentiated plasma cells secrete affinity-matured, antihost reactive immunoglobulin. Phase III: Fibrosis. Plasma cell-derived immunoglobulin is deposited in host tissues and stimulates donor CSF1-R+ macrophages, putatively via Fc receptor (FcR) ligation, to secrete profibrotic mediators. These include TGF-β that stimulates fibroblast proliferation and extracellular matrix production via the tyrosine-kinase receptor TGF-βR and is inhibitable by nilotinib and imatinib. The Hedgehog pathway inhibitor glasdegib and ROCK2 inhibitor KD025 each can directly ameliorate fibrosis. Abbreviations: Ab, antibody; CSF1, colony-stimulating factor 1; DC, dendritic cell; HSCT, hematopoietic stem cell transplantation; Mφ, macrophage; Th17, type 17 T helper. Figure adapted from images created with BioRender.com.