Potential of B-cell-targeting therapy in overcoming multidrug resistance and tissue invasiveness associated with P-glycoprotein expressing-B cell compartments

References

• Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet. 2010;376:1094–1108.
   PubMed Web of Science ®Google Scholar
• Smolen JS, Landewé R, Bijlsma J, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update. Ann Rheum Dis. 2017;76(6):960–977.
   PubMed Web of Science ®Google Scholar
• Moura RA, Graca L, Fonseca JE. To B or not to B the conductor of rheumatoid arthritis orchestra. Clin Rev Allergy Immunol. 2012;43(3):281–291.
   PubMed Web of Science ®Google Scholar
• Duddy ME, Alter A, Bar-Or A. Distinct profiles of human B cell effector cytokines: a role in immune regulation? J Immunol. 2004;172(6):3422–3427.
   PubMed Web of Science ®Google Scholar
• Gottenberg JE, Dayer JM, Lukas C, et al. Serum IL-6 and IL-21 are associated with markers of B cell activation and structural progression in early rheumatoid arthritis: results from the ESPOIR cohort. Ann Rheum Dis. 2012;71(7):1243–1248.
   PubMed Web of Science ®Google Scholar
• Tsujimura S, Saito K, Nawata M, et al. Overcoming drug resistance induced by P-glycoprotein on lymphocytes in patients with refractory rheumatoid arthritis. Ann Rheum Dis. 2008;67(3):380–388.
   PubMed Web of Science ®Google Scholar
• Tsujimura S, Saito K, Nakayamada S, et al. Etanercept overcomes P-glycoprotein-induced drug resistance in lymphocytes of patients with intractable rheumatoid arthritis. Mod Rheumatol. 2010;20(2):139–146.
   PubMed Web of Science ®Google Scholar
• Tsujimura S, Tanaka Y. Disease control by regulation of P-glycoprotein on lymphocytes in patients with rheumatoid arthritis. World J Exp Med. 2015;5(4):225–231.
   Google Scholar
• Tsujimura S, Adachi T, Saito K, et al. Relevance of P-glycoprotein on CXCR4+ B cells to organ manifestation in highly active rheumatoid arthritis. Mod Rheumatol. 2018;28(2):276–286.
   PubMed Web of Science ®Google Scholar
• Farrell RJ, Murphy A, Long A, et al. High multidrug resistance (P-glycoprotein 170) expression in inflammatory bowel disease patients who fail medical therapy. Gastroenterology. 2000;118(2):279–288.
   PubMed Web of Science ®Google Scholar
• Noble A, Durant L, Hoyles L, et al. Deficient resident memory T-cell and Cd8 T-cell response to commensals in inflammatory bowel disease. J Crohns Colitis. 2019;26:1–13.
   Google Scholar
• Leonard GD, Polgar O, Bates SE. ABC transporters and inhibitors: new targets, new agents. Curr Opin Investig Drugs. 2002;3(11):1652–1659.
   PubMedGoogle Scholar
• McKeegan KS, Borges-Walmsley MI, Walmsley AR. The structure and function of drug pumps: an update. Trends Microbiol. 2003;11(1):21–29.
   PubMed Web of Science ®Google Scholar
• Senarathna SM, Page-Sharp M, Crowe A. The interactions of P-glycoprotein with antimalarial drugs, including substrate affinity, inhibition and regulation. PLoS One. 2016;11(4):e0152677.
   PubMed Web of Science ®Google Scholar
• Lin JH. Drug-drug interaction mediated by inhibition and induction of P-glycoprotein. Adv Drug Deliv Rev. 2003;55(1):53–81.
   PubMed Web of Science ®Google Scholar
• Medeiros M, Castañeda-Hernández G, Ross CJ, et al. Use of pharmacogenomics in pediatric renal transplant recipients. Front Genet. 2015;6:41.
   Web of Science ®Google Scholar
• Gwak EH, Yoo HY, Kim SH. Effects of diabetes mellitus on the disposition of tofacitinib, a janus kinase inhibitor, in rats. Biomol Ther (Seoul). 2020;28(4):361–369.
   Web of Science ®Google Scholar
• Posada MM, Cannady EA, Payne CD, et al. Prediction of transporter-mediated drug-drug interactions for baricitinib. Clin Transl Sci. 2017;10(6):509–519.
   PubMed Web of Science ®Google Scholar
• Zhu T, Howieson C, Wojtkowski T, et al. The effect of verapamil, a P-glycoprotein inhibitor, on the pharmacokinetics of peficitinib, an orally administered, once-daily JAK inhibitor. Clin Pharmacol Drug Dev. 2017;6(6):548–555.
   PubMed Web of Science ®Google Scholar
• Colone M, Calcabrini A, Toccacieli L, et al. The multidrug transporter P-glycoprotein: a mediator of melanoma invasion? J Invest Dermatol. 2008;128(4):957–971.
   PubMed Web of Science ®Google Scholar
• Zhang F, Zhang H, Wang Z, et al. P-glycoprotein associates with Anxa2 and promotes invasion in multidrug resistant breast cancer cells. Biochem Pharmacol. 2014;87(2):292–302.
   PubMed Web of Science ®Google Scholar
• Hu M, Liu Y, Deng C, et al. Enhanced invasiveness in multidrug resistant leukemic cells is associated with overexpression of P-glycoprotein and cellular inhibitor of apoptosis protein. Leuk Lymphoma. 2011;52(7):1302–1311.
   PubMed Web of Science ®Google Scholar
• List AF, Kopecky KJ, Willman CL, et al. Cyclosporine inhibition of P-glycoprotein in chronic myeloid leukemia blast phase. Blood. 2002;100(5):1910–1912.
   Web of Science ®Google Scholar
• Tsujimura S, Kawabe A, Tanaka Y. P-glycoprotein expressing-B cell associated active true renal lupus vasculitis in lupus nephritis. Lupus: Open Access. 2020;5:1–6.
   Google Scholar
• Zhao BX, Sun YB, Wang SQ, et al. Grape seed procyanidin reversal of p-glycoprotein associated multi-drug resistance via down-regulation of NF-κB and MAPK/ERK mediated YB-1 activity in A2780/T cells. PLoS One. 2013;8(8):e71071.
   Web of Science ®Google Scholar
• Tomiyasu H, Watanabe M, Sugita K, et al. Regulations of ABCB1 and ABCG2 expression through MAPK pathways in acute lymphoblastic leukemia cell lines. Anticancer Res. 2013;33(12):5317–5323.
   PubMed Web of Science ®Google Scholar
• Shen H, Xu W, Luo W, et al. Upregulation of mdr1 gene is related to activation of the MAPK/ERK signal transduction pathway and YB-1 nuclear translocation in B-cell lymphoma. Exp Hematol. 2011;39(5):558–569.
   Web of Science ®Google Scholar
• Feng W, Liu H, Luo T, et al. Combination of IL-6 and sIL-6R differentially regulate varying levels of RANKL-induced osteoclastogenesis through NF-κB, ERK and JNK signaling pathways. Sci Rep. 2017;7:41411.
   Web of Science ®Google Scholar
• Choy EH, Panayi GS. Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med. 2001;344(12):907–916.
   PubMed Web of Science ®Google Scholar
• Basaki Y, Hosoi F, Oda Y, et al. Akt-dependent nuclear localization of Y-box-binding protein 1 in acquisition of malignant characteristics by human ovarian cancer cells. Oncogene. 2007;26(19):2736–2746.
   PubMed Web of Science ®Google Scholar
• Becker M, Hobeika E, Jumaa H, et al. CXCR4 signaling and function require the expression of the IgD-class B-cell antigen receptor. Proc Natl Acad Sci USA. 2017;114(20):5231–5236.
   Web of Science ®Google Scholar
• Tsujimura S, Saito K, Kohno K, et al. Fragmented hyaluronan induces transcriptional up-regulation of the multidrug resistance-1 gene in CD4+ T cells. J Biol Chem. 2006;281(49):38089–38097.
   Web of Science ®Google Scholar
• Odendahl M, Mei H, Hoyer BF, et al. Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood. 2005;105(4):1614–1621.
   PubMed Web of Science ®Google Scholar
• Pak HK, Nam B, Lee YK, et al. Human plasmablast migration toward CXCL12 requires glucose oxidation by enhanced pyruvate dehydrogenase activity via AKT. Front Immunol. 2018;9:1742.
   Web of Science ®Google Scholar
• Tamamura H, Tsutsumi H, Masuno H, et al. Development of low molecular weight CXCR4 antagonists by exploratory structural tuning of cyclic tetra- and pentapeptide-scaffolds towards the treatment of HIV infection, cancer metastasis and rheumatoid arthritis. Curr Med Chem. 2007;14(1):93–102.
   PubMed Web of Science ®Google Scholar
• Nanki T, Nagasaka K, Hayashida K, et al. Chemokines regulate IL-6 and IL-8 production by fibroblast-like synoviocytes from patients with rheumatoid arthritis. J Immunol. 2001;167(9):5381–5385.
   PubMed Web of Science ®Google Scholar
• Santiago B, Baleux F, Palao G, et al. CXCL12 is displayed by rheumatoid endothelial cells through its basic amino-terminal motif on heparan sulfate proteoglycans . Arthritis Res Ther. 2006;8(2):R43.
   Web of Science ®Google Scholar
• Uo M, Hisamatsu T, Miyoshi J, et al. Mucosal CXCR4+ IgG plasma cells contribute to the pathogenesis of human ulcerative colitis through FcγR-mediated CD14 macrophage activation. Gut. 2013;62(12):1734–1744.
   Web of Science ®Google Scholar
• Antoniou KM, Soufla G, Proklou A, et al. Different activity of the biological axis VEGF-Flt-1 (fms-like tyrosine kinase 1) and CXC chemokines between pulmonary sarcoidosis and idiopathic pulmonary fibrosis: a bronchoalveolar lavage study. Clin Dev Immunol. 2009;2009:537929.
   Google Scholar
• Ghetie MA, Marches R, Kufert S, et al. An anti-CD19 antibody inhibits the interaction between P-glycoprotein (P-gp) and CD19, causes P-gp to translocate out of lipid rafts, and chemosensitizes a multidrug-resistant (MDR) lymphoma cell line. Blood. 2004;104(1):178–183.
   Web of Science ®Google Scholar
• Kopriva F, Dzubak P, Potesil J, et al. The anti-inflammatory effects of inhaled corticosteroids versus anti-leukotrienes on the lymphocyte P-glycoprotein (PGP) expression in asthmatic children. J Asthma. 2009;46(4):366–370.
   PubMed Web of Science ®Google Scholar
• Salpietro DC, Masaracchio A, Turiaco A, et al. Serum IgD levels in children with atopic asthma. A longitudinal study. Minerva Pediatr. 2001;53:1–5.
   Google Scholar
• Ohm-Laursen L, Meng H, Chen J, et al. Local clonal diversification and dissemination of B lymphocytes in the human bronchial mucosa. Front Immunol. 1976;9:1976.
   Google Scholar
• Glaesener S, Quách TD, Onken N, et al. Distinct effects of methotrexate and etanercept on the B cell compartment in patients with juvenile idiopathic arthritis. Arthritis Rheumatol. 2014;66(9):2590–2600.
   Web of Science ®Google Scholar
• Wessels JA, Huizinga TW, Guchelaar HJ. Recent insights in the pharmacological actions of methotrexate in the treatment of rheumatoid arthritis. Rheumatology (Oxford). 2008;47(3):249–255.
   PubMed Web of Science ®Google Scholar
• Yang X, Zhao Y, Jia X, et al. CP-25 combined with MTX/ LEF ameliorates the progression of adjuvant-induced arthritis by the inhibition on GRK2 translocation. Biomed Pharmacother. 2019;110:834–843.
   PubMed Web of Science ®Google Scholar
• Hilderson I, Van Laecke S, Wauters A, et al. Treatment of renal sarcoidosis: is there a guideline? Overview of the different treatment options. Nephrol Dial Transplant. 2014;29(10):1841–1847.
   Web of Science ®Google Scholar
• Kraaijeveld R, Li Y, Yan L, et al. Inhibition of T helper cell differentiation by tacrolimus or sirolimus results in reduced B-cell activation: effects on t follicular helper cells. Transplant Proc. 2019;51(10):3463–3473.
   Web of Science ®Google Scholar
• Suzuki K, Saito K, Tsujimura S, et al. Tacrolimus, a calcineurin inhibitor, overcomes treatment unresponsiveness mediated by P-glycoprotein on lymphocytes in refractory rheumatoid arthritis. J Rheumatol. 2010;37(3):512–520.
   PubMed Web of Science ®Google Scholar
• Kandikattu HK, Mishra A. Immunomodulatory effects of tacrolimus (FK506) for the treatment of allergic diseases. Int J Cell Biol Physiol. 2018;1(1–2):5–13.
   PubMedGoogle Scholar
• Ando M, Miyazaki E, Yamasue M, et al. Successful treatment with tacrolimus of progressive interstitial pneumonia associated with amyopathic dermatomyositis refractory to cyclosporine. Clin Rheumatol. 2010;29(4):443–445.
   Web of Science ®Google Scholar
• Richaud-Patin Y, Vega-Boada F, Vidaller A, et al. Multidrug resistance-1 (MDR-1) in autoimmune disorders IV. P-glycoprotein overfunction in lymphocytes from myasthenia gravis patients. Biomed Pharmacother. 2004;58(5):320–324.
   Web of Science ®Google Scholar
• Tanaka S, Hirano T, Saito T, et al. P-glycoprotein function in peripheral blood mononuclear cells of myasthenia gravis patients treated with tacrolimus. Biol Pharm Bull. 2007;30(2):291–296.
   Web of Science ®Google Scholar
• Rizzi M, Lorenzetti R, Fischer K, et al. Impact of tofacitinib treatment on human B-cells in vitro and in vivo. J Autoimmun. 2017;77:55–66.
   PubMed Web of Science ®Google Scholar
• Kubo S, Nakayamada S, Sakata K, et al. Janus kinase inhibitor Baricitinib modulates human innate and adaptive immune system. Front Immunol. 2018;9:1510.
   PubMed Web of Science ®Google Scholar
• Durmus S, Xu N, Sparidans RW, et al. P-glycoprotein (MDR1/ABCB1) and breast cancer resistance protein (BCRP/ABCG2) restrict brain accumulation of the JAK1/2 inhibitor, CYT387. Pharmacol Res. 2013;76:9–16.
   PubMed Web of Science ®Google Scholar
• Fleischmann R, Mysler E, Hall S, et al. Efficacy and safety of tofacitinib monotherapy, tofacitinib with methotrexate, and adalimumab with methotrexate in patients with rheumatoid arthritis (ORAL Strategy): a phase 3b/4, double-blind, head-to-head, randomised controlled trial. Lancet. 2017;390(10093):457–468.
   PubMed Web of Science ®Google Scholar
• Taylor PC, Lee YC, Fleischmann R, et al. Achieving pain control in rheumatoid arthritis with baricitinib or adalimumab plus methotrexate: results from the RA-BEAM Trial. J Clin Med. 2019;8(6):831.
   Web of Science ®Google Scholar
• Xia F, Deng C, Jiang Y, et al. IL4 (interleukin 4) induces autophagy in B cells leading to exacerbated asthma. Autophagy. 2018;14(3):450–464.
   PubMed Web of Science ®Google Scholar
• Zak M, Dengler HS, Rajapaksa NS. Inhaled Janus Kinase (JAK) inhibitors for the treatment of asthma. Bioorg Med Chem Lett. 2019;29(20):126658.
   PubMed Web of Science ®Google Scholar
• Tsujimura S, Saito K, Nakayamada S, et al. Relevance of multidrug resistance 1 and P-glycoprotein to drug resistance in patients with systemic lupus erythematosus. Histol Histopathol. 2007;22(4):465–468.
   Web of Science ®Google Scholar
• Moura RA, Quaresma C, Vieira AR, et al. B-cell phenotype and IgD-CD27- memory B cells are affected by TNF-inhibitors and tocilizumab treatment in rheumatoid arthritis. PLoS One. 2017;12(9):e0182927.
   PubMed Web of Science ®Google Scholar
• Schnell A, Schwarz B, Wahlbuhl M, et al. Distribution and cytokine profile of peripheral B cell subsets is perturbed in pediatric IBD and partially restored during a successful IFX therapy. Inflamm Bowel Dis. 2020;izaa054.
   Web of Science ®Google Scholar
• Kudryavtsev I, Serebriakova M, Starshinova A, et al. Imbalance in B cell and T follicular helper cell subsets in pulmonary sarcoidosis. Sci Rep. 2020;10(1):1059.
   Web of Science ®Google Scholar
• Gelfand JM, Bradshaw MJ, Stern BJ, et al. Infliximab for the treatment of CNS sarcoidosis: a multi-institutional series. Neurology. 2017;89(20):2092–2100.
   PubMed Web of Science ®Google Scholar
• Snir A, Kessel A, Haj T, et al. Anti-IL-6 receptor antibody (tocilizumab): a B cell targeting therapy. Clin Exp Rheumatol. 2011;29:697–700.
   PubMed Web of Science ®Google Scholar
• Illei GG, Shirota Y, Yarboro CH, et al. Tocilizumab in systemic lupus erythematosus: data on safety, preliminary efficacy, and impact on circulating plasma cells from an open-label phase I dosage-escalation study. Arthritis Rheum. 2010;62(2):542–552.
   PubMed Web of Science ®Google Scholar
• Shirota Y, Yarboro C, Fischer R, et al. Impact of anti-interleukin-6 receptor blockade on circulating T and B cell subsets in patients with systemic lupus erythematosus. Ann Rheum Dis. 2013;72(1):118–128.
   PubMed Web of Science ®Google Scholar
• Araki M, Matsuoka T, Miyamoto K, et al. Efficacy of the anti-IL-6 receptor antibody tocilizumab in neuromyelitis optica: a pilot study. Neurology. 2014;82(15):1302–1306.
   PubMed Web of Science ®Google Scholar
• Schrezenmeier E, Jayne D, Dörner T. Targeting B cells and plasma cells in glomerular diseases: translational perspectives. J Am Soc Nephrol. 2018;29:741–758.
   PubMed Web of Science ®Google Scholar
• Cambridge G, Perry HC, Nogueira L, et al. The effect of B-cell depletion therapy on serological evidence of B-cell and plasmablast activation in patients with rheumatoid arthritis over multiple cycles of rituximab treatment. J Autoimmun. 2014;50:67–76.
   PubMed Web of Science ®Google Scholar
• Adlowitz DG, Barnard J, Biear JN, et al. Expansion of activated peripheral blood memory B cells in rheumatoid arthritis, impact of B cell depletion therapy, and biomarkers of response. PLoS One. 2015;10(6):e0128269.
   PubMed Web of Science ®Google Scholar
• Romeo AR, Segal BM. Treatment of neuromyelitis optica spectrum disorders. Curr Opin Rheumatol. 2019;31(3):250–255.
   PubMed Web of Science ®Google Scholar
• Moreno MJ, Bosch R, Dieguez-Gonzalez R, et al. CXCR4 expression enhances diffuse large B cell lymphoma dissemination and decreases patient survival. J Pathol. 2015;235(3):445–455.
   PubMed Web of Science ®Google Scholar
• Reinholdt L, Laursen MB, Schmitz A, et al. The CXCR4 antagonist plerixafor enhances the effect of rituximab in diffuse large B-cell lymphoma cell lines. Biomark Res. 2016;4:12.
   PubMed Web of Science ®Google Scholar
• Mikami S, Nakase H, Yamamoto S, et al. Blockade of CXCL12/CXCR4 axis ameliorates murine experimental colitis. J Pharmacol Exp Ther. 2008;327(2):383–392.
   Web of Science ®Google Scholar