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Rational design of a nanoparticle platform for oral prophylactic immunotherapy to prevent immunogenicity of therapeutic proteins

  • 1.

    Krishna, M. & Nadler, S. G. Immunogenicity to biotherapeutics—the role of anti-drug immune complexes. Front. Immunol. 7, 21. https://doi.org/10.3389/fimmu.2016.00021 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 2.

    Dingman, R. & Balu-Iyer, S. V. Immunogenicity of protein pharmaceuticals. J. Pharm. Sci. 108, 1637–1654. https://doi.org/10.1016/j.xphs.2018.12.014 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 3.

    Hermeling, S., Crommelin, D. J., Schellekens, H. & Jiskoot, W. Structure-immunogenicity relationships of therapeutic proteins. Pharm. Res. 21, 897–903. https://doi.org/10.1023/b:pham.0000029275.41323.a6 (2004).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 4.

    Lumizyme [Package Insert]. (Genzyme Corporation CM, 2011).

  • 5.

    Myozyme [Package Insert]. (Genzyme Corporation CM, 2017).

  • 6.

    Banugaria, S. G. et al. Bortezomib in the rapid reduction of high sustained antibody titers in disorders treated with therapeutic protein: Lessons learned from Pompe disease. Genet. Med. 15, 123–131. https://doi.org/10.1038/gim.2012.110 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 7.

    Hay, C. R. et al. Factor VIII inhibitors in mild and moderate-severity haemophilia A. UK haemophilia centre directors organisation. Thromb. Haemost. 79, 762–766 (1998).

    CAS 
    Article 

    Google Scholar 

  • 8.

    Lusher, J. M., Arkin, S., Abildgaard, C. F. & Schwartz, R. S. Recombinant factor VIII for the treatment of previously untreated patients with hemophilia A. Safety, efficacy, and development of inhibitors. Kogenate Previously Untreated Patient Study Group. N. Engl. J. Med. 328, 453–459. https://doi.org/10.1056/NEJM199302183280701 (1993).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 9.

    Lollar, P., Healey, J. F., Barrow, R. T. & Parker, E. T. Factor VIII inhibitors. Adv. Exp. Med. Biol. 489, 65–73. https://doi.org/10.1007/978-1-4615-1277-6_6 (2001).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 10.

    Zhou, Z. Y. et al. Burden of illness: Direct and indirect costs among persons with hemophilia A in the United States. J. Med. Econ. 18, 457–465. https://doi.org/10.3111/13696998.2015.1016228 (2015).

    Article 
    PubMed 

    Google Scholar 

  • 11.

    Gaitonde, P. et al. Exposure to factor VIII protein in the presence of phosphatidylserine induces hypo-responsiveness toward factor VIII challenge in hemophilia A mice. J. Biol. Chem. 288, 17051–17056. https://doi.org/10.1074/jbc.C112.396325 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 12.

    Ramakrishnan, R., Davidowitz, A. & Balu-Iyer, S. V. Exposure of FVIII in the presence of phosphatidyl serine reduces generation of memory B-cells and induces regulatory T-cell-mediated hyporesponsiveness in hemophilia A mice. J. Pharm. Sci. 104, 2451–2456. https://doi.org/10.1002/jps.24513 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 13.

    Schneider, J. L. & Balu-Iyer, S. V. Phosphatidylserine converts immunogenic recombinant human acid alpha-glucosidase to a tolerogenic form in a mouse model of pompe disease. J. Pharm. Sci. 105, 3097–3104. https://doi.org/10.1016/j.xphs.2016.06.018 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Glassman, F. Y. et al. Phosphatidylserine is not just a cleanup crew but also a well-meaning teacher. J. Pharm. Sci. 107, 2048–2054. https://doi.org/10.1016/j.xphs.2018.03.027 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 15.

    Gaitonde, P., Peng, A., Straubinger, R. M., Bankert, R. B. & Balu-Iyer, S. V. Phosphatidylserine reduces immune response against human recombinant Factor VIII in Hemophilia A mice by regulation of dendritic cell function. Clin. Immunol. 138, 135–145. https://doi.org/10.1016/j.clim.2010.10.006 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 16.

    Kerr, D. et al. Sensitivity of peripheral membrane proteins to the membrane context: A case study of phosphatidylserine and the TIM proteins. Biochim. Biophys. Acta Biomembr. 2126–2133, 2018. https://doi.org/10.1016/j.bbamem.2018.06.010 (1860).

    CAS 
    Article 

    Google Scholar 

  • 17.

    Tietjen, G. T. et al. Molecular mechanism for differential recognition of membrane phosphatidylserine by the immune regulatory receptor Tim4. Proc. Natl. Acad. Sci. USA 111, E1463-1472. https://doi.org/10.1073/pnas.1320174111 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 18.

    Verbrugghe, P. et al. Murine M cells express annexin V specifically. J. Pathol. 209, 240–249. https://doi.org/10.1002/path.1970 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 19.

    Cunin, P. et al. Clusterin facilitates apoptotic cell clearance and prevents apoptotic cell-induced autoimmune responses. Cell Death Dis. 7, e2215. https://doi.org/10.1038/cddis.2016.113 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 20.

    Futter, C. E. & White, I. J. Annexins and endocytosis. Traffic 8, 951–958. https://doi.org/10.1111/j.1600-0854.2007.00590.x (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 21.

    Kawasaki, Y., Nakagawa, A., Nagaosa, K., Shiratsuchi, A. & Nakanishi, Y. Phosphatidylserine binding of class B scavenger receptor type I, a phagocytosis receptor of testicular sertoli cells. J. Biol. Chem. 277, 27559–27566. https://doi.org/10.1074/jbc.M202879200 (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 22.

    Rigotti, A., Acton, S. L. & Krieger, M. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J. Biol. Chem. 270, 16221–16224. https://doi.org/10.1074/jbc.270.27.16221 (1995).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 23.

    Weiner, H. L. Oral tolerance, an active immunologic process mediated by multiple mechanisms. J. Clin. Investig. 106, 935–937. https://doi.org/10.1172/JCI11348 (2000).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 24.

    Weiner, H. L., da Cunha, A. P., Quintana, F. & Wu, H. Oral tolerance. Immunol. Rev. 241, 241–259. https://doi.org/10.1111/j.1600-065X.2011.01017.x (2011).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 25.

    Fadok, V. A. et al. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207–2216 (1992).

    CAS 
    PubMed 

    Google Scholar 

  • 26.

    Bar, P. R. Apoptosis–the cell’s silent exit. Life Sci. 59, 369–378. https://doi.org/10.1016/0024-3205(96)00315-3 (1996).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 27.

    Munoz, L. E., Lauber, K., Schiller, M., Manfredi, A. A. & Herrmann, M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol. 6, 280–289. https://doi.org/10.1038/nrrheum.2010.46 (2010).

    Article 
    PubMed 

    Google Scholar 

  • 28.

    Miyanishi, M. et al. Identification of Tim4 as a phosphatidylserine receptor. Nature 450, 435–439. https://doi.org/10.1038/nature06307 (2007).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 29.

    Santiago, C. et al. Structures of T cell immunoglobulin mucin protein 4 show a metal-Ion-dependent ligand binding site where phosphatidylserine binds. Immunity 27, 941–951. https://doi.org/10.1016/j.immuni.2007.11.008 (2007).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Kobayashi, N. et al. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 27, 927–940. https://doi.org/10.1016/j.immuni.2007.11.011 (2007).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Yang, P. C. et al. TIM-4 expressed by mucosal dendritic cells plays a critical role in food antigen-specific Th2 differentiation and intestinal allergy. Gastroenterology 133, 1522–1533. https://doi.org/10.1053/j.gastro.2007.08.006 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 32.

    Juliano, R. L. & Stamp, D. The effect of particle size and charge on the clearance rates of liposomes and liposome encapsulated drugs. Biochem. Biophys. Res. Commun. 63, 651–658. https://doi.org/10.1016/s0006-291x(75)80433-5 (1975).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 33.

    Frasch, S. C. et al. Neutrophils regulate tissue Neutrophilia in inflammation via the oxidant-modified lipid lysophosphatidylserine. J. Biol. Chem. 288, 4583–4593. https://doi.org/10.1074/jbc.M112.438507 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 34.

    Rice, D. R., Clear, K. J. & Smith, B. D. Imaging and therapeutic applications of zinc(II)-dipicolylamine molecular probes for anionic biomembranes. Chem. Commun. 52, 8787–8801. https://doi.org/10.1039/c6cc03669d (2016).

    CAS 
    Article 

    Google Scholar 

  • 35.

    Andree, H. A. et al. Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J. Biol. Chem. 265, 4923–4928 (1990).

    CAS 
    Article 

    Google Scholar 

  • 36.

    Weiner, H. L. Oral tolerance: Immune mechanisms and treatment of autoimmune diseases. Immunol. Today 18, 335–343 (1997).

    CAS 
    Article 

    Google Scholar 

  • 37.

    Weiner, H. L. et al. Oral tolerance: Immunologic mechanisms and treatment of animal and human organ-specific autoimmune diseases by oral administration of autoantigens. Annu. Rev. Immunol. 12, 809–837. https://doi.org/10.1146/annurev.iy.12.040194.004113 (1994).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 38.

    Bjornsson, O. G., Murphy, R. & Chadwick, V. S. Physiochemical studies of indocyanine green (ICG): Absorbance/concentration relationship, pH tolerance and assay precision in various solvents. Experientia 38, 1441–1442. https://doi.org/10.1007/BF01955757 (1982).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 39.

    Kraft, J. C. & Ho, R. J. Interactions of indocyanine green and lipid in enhancing near-infrared fluorescence properties: The basis for near-infrared imaging in vivo. Biochemistry 53, 1275–1283. https://doi.org/10.1021/bi500021j (2014).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 40.

    Yoon, H. J., Lee, H. S., Lim, J. Y. & Park, J. H. Liposomal indocyanine green for enhanced photothermal therapy. ACS Appl. Mater Interfaces 9, 5683–5691. https://doi.org/10.1021/acsami.6b16801 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 41.

    Wang, X., Terhorst, C. & Herzog, R. W. In vivo induction of regulatory T cells for immune tolerance in hemophilia. Cell Immunol. 301, 18–29. https://doi.org/10.1016/j.cellimm.2015.10.001 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 42.

    Oida, T. et al. CD4+CD25− T cells that express latency-associated peptide on the surface suppress CD4+CD45RBhigh-induced colitis by a TGF-beta-dependent mechanism. J. Immunol. 170, 2516–2522. https://doi.org/10.4049/jimmunol.170.5.2516 (2003).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 43.

    Huang, W., Solouki, S., Carter, C., Zheng, S. G. & August, A. Beyond type 1 regulatory T cells: Co-expression of LAG3 and CD49b in IL-10-producing T cell lineages. Front. Immunol. 9, 2625. https://doi.org/10.3389/fimmu.2018.02625 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 44.

    Gagliani, N. et al. Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells. Nat. Med. 19, 739–746. https://doi.org/10.1038/nm.3179 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 45.

    Schmidt, A., Oberle, N. & Krammer, P. H. Molecular mechanisms of treg-mediated T cell suppression. Front. Immunol. 3, 51. https://doi.org/10.3389/fimmu.2012.00051 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 46.

    Romano, M., Fanelli, G., Albany, C. J., Giganti, G. & Lombardi, G. Past, present, and future of regulatory T cell therapy in transplantation and autoimmunity. Front. Immunol. 10, 43. https://doi.org/10.3389/fimmu.2019.00043 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Sakaguchi, S., Wing, K., Onishi, Y., Prieto-Martin, P. & Yamaguchi, T. Regulatory T cells: How do they suppress immune responses?. Int. Immunol. 21, 1105–1111. https://doi.org/10.1093/intimm/dxp095 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 48.

    Sakaguchi, S., Yamaguchi, T., Nomura, T. & Ono, M. Regulatory T cells and immune tolerance. Cell 133, 775–787. https://doi.org/10.1016/j.cell.2008.05.009 (2008).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 49.

    Lim, H. W., Hillsamer, P., Banham, A. H. & Kim, C. H. Cutting edge: Direct suppression of B cells by CD4+ CD25+ regulatory T cells. J. Immunol. 175, 4180–4183. https://doi.org/10.4049/jimmunol.175.7.4180 (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 50.

    Neutra, M. R., Pringault, E. & Kraehenbuhl, J. P. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu. Rev. Immunol. 14, 275–300. https://doi.org/10.1146/annurev.immunol.14.1.275 (1996).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 51.

    Mabbott, N. A., Donaldson, D. S., Ohno, H., Williams, I. R. & Mahajan, A. Microfold (M) cells: Important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol. 6, 666–677. https://doi.org/10.1038/mi.2013.30 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 52.

    Hilligan, K. L., Connor, L. M., Schmidt, A. J. & Ronchese, F. Activation-induced TIM-4 expression identifies differential responsiveness of intestinal CD103+ CD11b+ dendritic cells to a mucosal adjuvant. PLoS ONE 11, e0158775. https://doi.org/10.1371/journal.pone.0158775 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 53.

    Shaw, T. N. et al. Tissue-resident macrophages in the intestine are long lived and defined by Tim-4 and CD4 expression. J. Exp. Med. 215, 1507–1518. https://doi.org/10.1084/jem.20180019 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Mazzini, E., Massimiliano, L., Penna, G. & Rescigno, M. Oral tolerance can be established via gap junction transfer of fed antigens from CX3CR1(+) macrophages to CD103(+) dendritic cells. Immunity 40, 248–261. https://doi.org/10.1016/j.immuni.2013.12.012 (2014).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 55.

    van den Berg, H. M. et al. Timing of inhibitor development in more than 1000 previously untreated patients with severe hemophilia A. Blood 134, 317–320. https://doi.org/10.1182/blood.2019000658 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 56.

    Graca, L. & Waldmann, H. Inducing immune tolearnce to therapeutic protein, cells and tissues. Front. Immunol. https://doi.org/10.3389/fimmu.2017.00560 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 57.

    Raben, N. et al. Enzyme replacement therapy in the mouse model of Pompe disease. Mol. Genet. Metab. 80, 159–169. https://doi.org/10.1016/j.ymgme.2003.08.022 (2003).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 58.

    Ramani, K. et al. Phosphatidylserine containing liposomes reduce immunogenicity of recombinant human factor VIII (rFVIII) in a murine model of hemophilia A. J. Pharm. Sci. 97, 1386–1398. https://doi.org/10.1002/jps.21102 (2008).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 59.

    Bartlett, G. R. Phosphorus assay in column chromatography. J. Biol. Chem. 234, 466–468 (1959).

    CAS 
    Article 

    Google Scholar 

  • 60.

    Balu-Iyer, S. V., Ramani, K. & Straubinger, R. M. Method of complexing a protein by the use of a dispersed system and proteins thereof. U.S Patent No. 7625584 (U.S. Patent and Trademark Office, 2009).

  • 61.

    Ramani, K., Purohit, V. S., Miclea, R. D., Middaugh, C. R. & Balasubramanian, S. V. Lipid binding region (2303–2332) is involved in aggregation of recombinant human FVIII (rFVIII). J. Pharm. Sci. 94, 1288–1299 (2005).

    CAS 
    Article 

    Google Scholar 

  • 62.

    Verbruggen, B. et al. The Nijmegen modification of the Bethesda assay for factor VIII: C inhibitors: Improved specificity and reliability. Thromb. Haemost. 73, 247–251 (1995).

    CAS 
    Article 

    Google Scholar 

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