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Targeted enzyme delivery systems in lysosomal disorders: an innovative form of therapy for mucopolysaccharidosis

  • Azam Safary
  • Mostafa Akbarzadeh Khiavi
  • Yadollah OmidiEmail author
  • Mohammad A. RafiEmail author
Review

Abstract

Mucopolysaccharidoses (MPSs), which are inherited lysosomal storage disorders caused by the accumulation of undegraded glycosaminoglycans, can affect the central nervous system (CNS) and elicit cognitive and behavioral issues. Currently used enzyme replacement therapy methodologies often fail to adequately treat the manifestations of the disease in the CNS and other organs such as bone, cartilage, cornea, and heart. Targeted enzyme delivery systems (EDSs) can efficiently cross biological barriers such as blood–brain barrier and provide maximal therapeutic effects with minimal side effects, and hence, offer great clinical benefits over the currently used conventional enzyme replacement therapies. In this review, we provide comprehensive insights into MPSs and explore the clinical impacts of multimodal targeted EDSs.

Keywords

Blood–brain barrier Enzyme replacement therapy Mucopolysaccharidoses Nanosystems Targeted enzyme delivery systems 

Notes

Acknowledgements

Authors would like to acknowledge the Research Center for Pharmaceutical Nanotechnology and Connective Tissue Diseases Research Center at Tabriz University of Medical Sciences for financial support. The kind help from Dr. S. Sabermoghaddam and Mrs. R. Mousavi are highly appreciated.

Compliance with ethical standards

Conflict of interest

No conflicts of interest to be disclosed.

References

  1. 1.
    Muenzer J (2014) Early initiation of enzyme replacement therapy for the mucopolysaccharidoses. Mol Genet Metab 111:63–72CrossRefPubMedGoogle Scholar
  2. 2.
    Muenzer J (2011) Overview of the mucopolysaccharidoses. Rheumatology (Oxford) 50:v4–v12CrossRefGoogle Scholar
  3. 3.
    Willoughby CE, Ponzin D, Ferrari S, Lobo A, Landau K, Omidi Y (2010) Anatomy and physiology of the human eye: effects of mucopolysaccharidoses disease on structure and function—a review. Clin Exp Ophthalmol 38:2–11CrossRefGoogle Scholar
  4. 4.
    Cimaz R, La Torre F (2014) Mucopolysaccharidoses. Curr Rheumatol Rep 16:389CrossRefPubMedGoogle Scholar
  5. 5.
    Kishnani PS, Dickson PI, Muldowney L, Lee JJ, Rosenberg A, Abichandani R, Bluestone JA, Burton BK, Dewey M, Freitas A (2016) Immune response to enzyme replacement therapies in lysosomal storage diseases and the role of immune tolerance induction. Mol Genet Metab 117:66–83CrossRefPubMedGoogle Scholar
  6. 6.
    Desnick R, Schuchman E (2012) Enzyme replacement therapy for lysosomal diseases: lessons from 20 years of experience and remaining challenges. Annu Rev Genom Hum Genet 13:307–335CrossRefGoogle Scholar
  7. 7.
    Clarke LA (2011) Pathogenesis of skeletal and connective tissue involvement in the mucopolysaccharidoses: glycosaminoglycan storage is merely the instigator. Rheumatology (Oxford) 50:v13–v18CrossRefGoogle Scholar
  8. 8.
    Shapiro EG, Jones SA, Escolar ML (2017) Developmental and behavioral aspects of mucopolysaccharidoses with brain manifestations—neurological signs and symptoms. Mol Genet Metab 122:1–7CrossRefGoogle Scholar
  9. 9.
    Ohmi K, Greenberg DS, Rajavel KS, Ryazantsev S, Li HH, Neufeld EF (2003) Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci USA 100:1902–1907CrossRefPubMedGoogle Scholar
  10. 10.
    Rigante D, Cipolla C, Basile U, Gulli F, Savastano MC (2017) Overview of immune abnormalities in lysosomal storage disorders. Immunol Lett 188:79–85CrossRefPubMedGoogle Scholar
  11. 11.
    Solomon M, Muro S (2017) Lysosomal enzyme replacement therapies: historical development, clinical outcomes, and future perspectives. Adv Drug Deliv Rev 118:109–134CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Safary A, Moniri R, Hamzeh-Mivehroud M, Dastmalchi S (2016) Identification and molecular characterization of genes coding pharmaceutically important enzymes from halo-thermo tolerant bacillus. Adv Pharm Bull 6:551CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Valayannopoulos V, Wijburg FA (2011) Therapy for the mucopolysaccharidoses. Rheumatology (Oxford) 50:v49–v59CrossRefGoogle Scholar
  14. 14.
    Pan D (2011) Cell-and gene-based therapeutic approaches for neurological deficits in mucopolysaccharidoses. Curr Pharm Biotechnol 12:884–896CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Safary A, Khiavi MA, Mousavi R, Barar J, Rafi MA (2018) Enzyme replacement therapies: what is the best option? BioImpacts 8:153–157CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Schuh RS, Baldo G, Teixeira HF (2016) Nanotechnology applied to treatment of mucopolysaccharidoses. Expert Opin Drug Deliv 13:1709–1718CrossRefPubMedGoogle Scholar
  17. 17.
    Barton NW, Brady RO, Dambrosia JM, Di Bisceglie AM, Doppelt SH, Hill SC, Mankin HJ, Murray GJ, Parker RI, Argoff CE (1991) Replacement therapy for inherited enzyme deficiency—macrophage-targeted glucocerebrosidase for Gaucher’s disease. N Engl J Med 324:1464–1470CrossRefPubMedGoogle Scholar
  18. 18.
    Barton NW, Furbish FS, Murray GJ, Garfield M, Brady RO (1990) Therapeutic response to intravenous infusions of glucocerebrosidase in a patient with Gaucher disease. Proc Natl Acad Sci USA 87:1913–1916CrossRefPubMedGoogle Scholar
  19. 19.
    Grabowski GA, Barton NW, Pastores G, Dambrosia JM, Banerjee TK, McKee MA, Parker C, Schiffmann R, Hill SC, Brady RO (1995) Enzyme therapy in type 1 Gaucher disease: comparative efficacy of mannose-terminated glucocerebrosidase from natural and recombinant sources. Ann Intern Med 122:33–39CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Khan KH (2013) Gene expression in mammalian cells and its applications. Adv Pharm Bull 3:257PubMedPubMedCentralGoogle Scholar
  21. 21.
    Safary A, Moniri R, Hamzeh-Mivehroud M, Dastmalchi S (2016) A strategy for soluble overexpression and biochemical characterization of halo-thermotolerant Bacillus laccase in modified E. coli. J Biotechnol 227:56–63CrossRefPubMedGoogle Scholar
  22. 22.
    Safary A, Moniri R, Hamzeh-Mivehroud M, Dastmalchi S (2019) Highly efficient novel recombinant l-asparaginase with no glutaminase activity from a new halo-thermotolerant Bacillus strain. BioImpacts 9:15–23CrossRefPubMedGoogle Scholar
  23. 23.
    Kermode AR (2006) Plants as factories for production of biopharmaceutical and bioindustrial proteins: lessons from cell biology. Botany 84:679–694Google Scholar
  24. 24.
    He X, Haselhorst T, Von Itzstein M, Kolarich D, Packer NH, Gloster TM, Vocadlo DJ, Clarke LA, Qian Y, Kermode AR (2012) Production of α-l-iduronidase in maize for the potential treatment of a human lysosomal storage disease. Nat Commun 3:1062CrossRefPubMedGoogle Scholar
  25. 25.
    Kim J, Park M, Kim D, Lee J, Maeng S, Cho S, Han Y, Ahn K, Jin D (2013) IgE-mediated anaphylaxis and allergic reactions to idursulfase in patients with Hunter syndrome. Allergy 68:796–802CrossRefPubMedGoogle Scholar
  26. 26.
    Le SQ, Kan S-H, Clarke D, Sanghez V, Egeland M, Vondrak KN, Doherty TM, Vera MU, Iacovino M, Cooper JD (2018) A humoral immune response alters the distribution of enzyme replacement therapy in murine mucopolysaccharidosis type I. Mol Ther Methods Clin Dev 8:42–51CrossRefPubMedGoogle Scholar
  27. 27.
    Coutinho MF, Prata MJ, Alves S (2012) Mannose-6-phosphate pathway: a review on its role in lysosomal function and dysfunction. Mol Genet Metab 105:542–550CrossRefPubMedGoogle Scholar
  28. 28.
    Kishnani PS, Goldenberg PC, DeArmey SL, Heller J, Benjamin D, Young S, Bali D, Smith SA, Li JS, Mandel H (2010) Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol Genet Metab 99:26–33CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Wraith JE, Beck M, Lane R, Van Der Ploeg A, Shapiro E, Xue Y, Kakkis ED, Guffon N (2007) Enzyme replacement therapy in patients who have mucopolysaccharidosis I and are younger than 5 years: results of a multinational study of recombinant human α-l-iduronidase (laronidase). Pediatrics 120:e37–e46CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Banugaria SG, Prater SN, Ng Y-K, Kobori JA, Finkel RS, Ladda RL, Chen Y-T, Rosenberg AS, Kishnani PS (2011) The impact of antibodies on clinical outcomes in diseases treated with therapeutic protein: lessons learned from infantile Pompe disease. Genet Med 13:729CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Calias P, Banks WA, Begley D, Scarpa M, Dickson P (2014) Intrathecal delivery of protein therapeutics to the brain: a critical reassessment. Pharmacol Ther 144:114–122CrossRefPubMedGoogle Scholar
  32. 32.
    Dickson P, Peinovich M, McEntee M, Lester T, Le S, Krieger A, Manuel H, Jabagat C, Passage M, Kakkis ED (2008) Immune tolerance improves the efficacy of enzyme replacement therapy in canine mucopolysaccharidosis I. J Clin Investig 118:2868–2876PubMedGoogle Scholar
  33. 33.
    Muenzer J, Wraith JE, Beck M, Giugliani R, Harmatz P, Eng CM, Vellodi A, Martin R, Ramaswami U, Gucsavas-Calikoglu M (2006) A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet Med 8:465CrossRefPubMedGoogle Scholar
  34. 34.
    Wraith JE, Clarke LA, Beck M, Kolodny EH, Pastores GM, Muenzer J, Rapoport DM, Berger KI, Swiedler SJ, Kakkis ED (2004) Enzyme replacement therapy for mucopolysaccharidosis I: a randomized, double-blinded, placebo-controlled, multinational study of recombinant human α-l-iduronidase (laronidase). J Pediatr 144:581–588CrossRefPubMedGoogle Scholar
  35. 35.
    Miebach E (2009) Management of infusion-related reactions to enzyme replacement therapy in a cohort of patients with mucopolysaccharidosis disorders. Int J Clin Pharmacol Ther 47:S100–S106PubMedGoogle Scholar
  36. 36.
    Barar J, Rafi MA, Pourseif MM, Omidi Y (2016) Blood–brain barrier transport machineries and targeted therapy of brain diseases. BioImpacts 6:225CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Fraldi A, Annunziata F, Lombardi A, Kaiser HJ, Medina DL, Spampanato C, Fedele AO, Polishchuk R, Sorrentino NC, Simons K (2010) Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. EMBO J 29:3607–3620CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Omidi Y, Gumbleton M (2005) Biological membranes and barriers. In: Mahato RI (ed) Biomaterials for delivery and targeting of proteins nucleic acids. CRC Press, Baco Raton, pp 232–274Google Scholar
  39. 39.
    Lajoie JM, Shusta EV (2015) Targeting receptor-mediated transport for delivery of biologics across the blood–brain barrier. Annu Rev Pharmacol Toxicol 55:613–631CrossRefPubMedGoogle Scholar
  40. 40.
    Achord DT, Brot FE, Bell CE, Sly WS (1978) Human β-glucuronidase: in vivo clearance and in vitro uptake by a glycoprotein recognition system on reticuloendothelial cells. Cell 15:269–278CrossRefPubMedGoogle Scholar
  41. 41.
    Zhu Y, Li X, Schuchman EH, Desnick RJ, Cheng SH (2004) Dexamethasone-mediated up-regulation of the mannose receptor improves the delivery of recombinant glucocerebrosidase to Gaucher macrophages. J Pharmacol Exp Ther 308:705–711CrossRefPubMedGoogle Scholar
  42. 42.
    Koeberl DD, Luo X, Sun B, McVie-Wylie A, Dai J, Li S, Banugaria SG, Chen Y-T, Bali DS (2011) Enhanced efficacy of enzyme replacement therapy in Pompe disease through mannose-6-phosphate receptor expression in skeletal muscle. Mol Genet Metab 103:107–112CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Urayama A, Grubb JH, Sly WS, Banks WA (2008) Mannose 6-phosphate receptor—mediated transport of sulfamidase across the blood–brain barrier in the newborn mouse. Mol Ther 16:1261–1266CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Rappaport J, Manthe RL, Garnacho C, Muro S (2015) Altered clathrin-independent endocytosis in type A Niemann-Pick disease cells and rescue by ICAM-1-targeted enzyme delivery. Mol Pharm 12:1366–1376CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Vogler C, Levy B, Grubb JH, Galvin N, Tan Y, Kakkis E, Pavloff N, Sly WS (2005) Overcoming the blood–brain barrier with high-dose enzyme replacement therapy in murine mucopolysaccharidosis VII. Proc Natl Acad Sci USA 102:14777–14782CrossRefPubMedGoogle Scholar
  46. 46.
    Calias P, Papisov M, Pan J, Savioli N, Belov V, Huang Y, Lotterhand J, Alessandrini M, Liu N, Fischman AJ (2012) CNS penetration of intrathecal-lumbar idursulfase in the monkey, dog and mouse: implications for neurological outcomes of lysosomal storage disorder. PLoS One 7:e30341CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Vite CH, Wang P, Patel RT, Walton RM, Walkley SU, Sellers RS, Ellinwood NM, Cheng AS, White JT, O’Neill CA (2011) Biodistribution and pharmacodynamics of recombinant human alpha-l-iduronidase (rhIDU) in mucopolysaccharidosis type I-affected cats following multiple intrathecal administrations. Mol Genet Metab 103:268–274CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Dickson P, Kaitila I, Harmatz P, Mlikotic A, Chen A, Victoroff A, Passage M, Madden J, Le S, Naylor D (2015) Data from subjects receiving intrathecal laronidase for cervical spinal stenosis due to mucopolysaccharidosis type I. Data Brief 5:71–76CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Muenzer J, Hendriksz CJ, Fan Z, Vijayaraghavan S, Perry V, Santra S, Solanki GA, Mascelli MA, Pan L, Wang N (2016) A phase I/II study of intrathecal idursulfase-IT in children with severe mucopolysaccharidosis II. Genet Med 18:73CrossRefPubMedGoogle Scholar
  50. 50.
    Jones SA, Breen C, Heap F, Rust S, de Ruijter J, Tump E, Marchal JP, Pan L, Qiu Y, Chung J-K (2016) A phase 1/2 study of intrathecal heparan-N-sulfatase in patients with mucopolysaccharidosis IIIA. Mol Genet Metab 118:198–205CrossRefPubMedGoogle Scholar
  51. 51.
    Nestrasil I, Shapiro E, Svatkova A, Dickson P, Chen A, Wakumoto A, Ahmed A, Stehel E, McNeil S, Gravance C, Maher E (2017) Intrathecal enzyme replacement therapy reverses cognitive decline in mucopolysaccharidosis type I. Am J Med Genet A 173:780–783CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Scarpa M, Orchard PJ, Schulz A, Dickson PI, Haskins ME, Escolar ML, Giugliani R (2017) Treatment of brain disease in the mucopolysaccharidoses. Mol Genet Metab 122:25–34CrossRefGoogle Scholar
  53. 53.
    Lampe C, Bellettato CM, Karabul N, Scarpa M (2013) Mucopolysaccharidoses and other lysosomal storage diseases. Rheum Dis Clin 39:431–455CrossRefGoogle Scholar
  54. 54.
    Tomatsu S, Alméciga-Díaz CJ, Montaño AM, Yabe H, Tanaka A, Dung VC, Giugliani R, Kubaski F, Mason RW, Yasuda E (2015) Therapies for the bone in mucopolysaccharidoses. Mol Genet Metab 114:94–109CrossRefPubMedGoogle Scholar
  55. 55.
    Muro S (2010) New biotechnological and nanomedicine strategies for treatment of lysosomal storage disorders. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2:189–204CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    LeBowitz JH, Grubb JH, Maga JA, Schmiel DH, Vogler C, Sly WS (2004) Glycosylation-independent targeting enhances enzyme delivery to lysosomes and decreases storage in mucopolysaccharidosis type VII mice. Proc Natl Acad Sci USA 101:3083–3088CrossRefPubMedGoogle Scholar
  57. 57.
    Prince WS, McCormick LM, Wendt DJ, Fitzpatrick PA, Schwartz KL, Aguilera AI, Koppaka V, Christianson TM, Vellard MC, Pavloff N (2004) Lipoprotein receptor binding, cellular uptake, and lysosomal delivery of fusions between the receptor-associated protein (RAP) and α-l-iduronidase or acid α-glucosidase. J Biol Chem 279:35037–35046CrossRefPubMedGoogle Scholar
  58. 58.
    Orii KO, Grubb JH, Vogler C, Levy B, Tan Y, Markova K, Davidson BL, Mao Q, Orii T, Kondo N (2005) Defining the pathway for Tat-mediated delivery of β-glucuronidase in cultured cells and MPS VII mice. Mol Ther 12:345–352CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Giugliani R, Giugliani L, de Oliveira Poswar F, Donis KC, Dalla Corte A, Schmidt M, Boado RJ, Nestrasil I, Nguyen C, Chen S (2018) Neurocognitive and somatic stabilization in pediatric patients with severe mucopolysaccharidosis type I after 52 weeks of intravenous brain-penetrating insulin receptor antibody-iduronidase fusion protein (valanafusp alpha): an open label phase 1–2 trial. Orphanet J Rare Dis 13:110CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Barar J, Omidi Y (2013) Nanoparticles for ocular drug delivery. In: Kumar A, Mansour HM, Friedman A, Blough ER (eds) Nanomedicine in drug delivery. CRC Press, Baco Raton, pp 287–334CrossRefGoogle Scholar
  61. 61.
    Khiavi MA, Safary A, Aghanejad A, Barar J, Rasta SH, Golchin A, Omidi Y, Somi MH (2019) Enzyme-conjugated gold nanoparticles for combined enzyme and photothermal therapy of colon cancer cells. Colloids Surf A Physicochem Eng Asp 572:333–344CrossRefGoogle Scholar
  62. 62.
    Desnick RJ, Schuchman EH (2002) Enzyme replacement and enhancement therapies: lessons from lysosomal disorders. Nat Rev Genet 3:954CrossRefPubMedGoogle Scholar
  63. 63.
    Tam VH, Sosa C, Liu R, Yao N, Priestley RD (2016) Nanomedicine as a non-invasive strategy for drug delivery across the blood–brain barrier. Int J Pharm 515:331–342CrossRefPubMedGoogle Scholar
  64. 64.
    Desnick R, Fiddler M, Steger L, Cumming D, Dullum C, Thorpe S (1975) Enzyme replacement therapy-invivo fate of native, erythrocyte-entrapped and liposome-entrapped beta-glucuronidase. Pediatr Res 9:312Google Scholar
  65. 65.
    Samad A, Sultana Y, Aqil M (2007) Liposomal drug delivery systems: an update review. Curr Drug Deliv 4:297–305CrossRefPubMedGoogle Scholar
  66. 66.
    Mayer FQ, Adorne MD, Bender EA, de Carvalho TG, Dilda AC, Beck RCR, Guterres SS, Giugliani R, Matte U, Pohlmann AR (2015) Laronidase-functionalized multiple-wall lipid-core nanocapsules: promising formulation for a more effective treatment of mucopolysaccharidosis type I. Pharm Res 32:941–954CrossRefPubMedGoogle Scholar
  67. 67.
    Mooguee M, Omidi Y, Davaran S (2010) Synthesis and in vitro release of adriamycin from star-shaped poly(lactide-co-glycolide) nano- and microparticles. J Pharm Sci 99:3389–3397CrossRefPubMedGoogle Scholar
  68. 68.
    Moogooee M, Ramezanzadeh H, Jasoori S, Omidi Y, Davaran S (2011) Synthesis and in vitro studies of cross-linked hydrogel nanoparticles containing amoxicillin. J Pharm Sci 100:1057–1066CrossRefPubMedGoogle Scholar
  69. 69.
    Khosroushahi AY, Naderi-Manesh H, Yeganeh H, Barar J, Omidi Y (2012) Novel water-soluble polyurethane nanomicelles for cancer chemotherapy: physicochemical characterization and cellular activities. J Nanobiotechnol 10:2CrossRefGoogle Scholar
  70. 70.
    Barzegar-Jalali M, Hanaee J, Omidi Y, Ghanbarzadeh S, Ziaee S, Bairami-Atashgah R, Adibkia K (2013) Preparation and evaluation of sustained release calcium alginate beads and matrix tablets of acetazolamide. Drug Res (Stuttg) 63:60–64CrossRefGoogle Scholar
  71. 71.
    Shakoori Z, Ghanbari H, Omidi Y, Pashaiasl M, Akbarzadeh A, Jomeh Farsangi Z, Rezayat SM, Davaran S (2017) Fluorescent multi-responsive cross-linked P(N-isopropylacrylamide)-based nanocomposites for cisplatin delivery. Drug Dev Ind Pharm 43:1283–1291CrossRefPubMedGoogle Scholar
  72. 72.
    Fathi M, Zangabad PS, Aghanejad A, Barar J, Erfan-Niya H, Omidi Y (2017) Folate-conjugated thermosensitive O-maleoyl modified chitosan micellar nanoparticles for targeted delivery of erlotinib. Carbohydr Polym 172:130–141CrossRefPubMedGoogle Scholar
  73. 73.
    Matthaiou E-I, Barar J, Sandaltzopoulos R, Li C, Coukos G, Omidi Y (2014) Shikonin-loaded antibody-armed nanoparticles for targeted therapy of ovarian cancer. Int J Nanomed 9:1855Google Scholar
  74. 74.
    Salvalaio M, Rigon L, Belletti D, D’Avanzo F, Pederzoli F, Ruozi B, Marin O, Vandelli MA, Forni F, Scarpa M (2016) Targeted polymeric nanoparticles for brain delivery of high molecular weight molecules in lysosomal storage disorders. PLoS One 11:e0156452CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Papademetriou J, Garnacho C, Serrano D, Bhowmick T, Schuchman EH, Muro S (2013) Comparative binding, endocytosis, and biodistribution of antibodies and antibody-coated carriers for targeted delivery of lysosomal enzymes to ICAM-1 versus transferrin receptor. J Inherit Metab Dis 36:467–477CrossRefPubMedGoogle Scholar
  76. 76.
    Abuchowski A, Van Es T, Palczuk N, Davis F (1977) Alteration of immunological properties of bovine serum albumin by covalent attachment of polyethylene glycol. J Biol Chem 252:3578–3581PubMedGoogle Scholar
  77. 77.
    Dozier JK, Distefano MD (2015) Site-specific PEGylation of therapeutic proteins. Int J Mol Sci 16:25831–25864CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Nischan N, Hackenberger CP (2014) Site-specific PEGylation of proteins: recent developments. J Org Chem 79:10727–10733CrossRefPubMedGoogle Scholar
  79. 79.
    Fraga M, Bruxel F, Diel D, de Carvalho TG, Perez CA, Magalhães-Paniago R, Malachias Â, Oliveira MC, Matte U, Teixeira HF (2015) PEGylated cationic nanoemulsions can efficiently bind and transfect pIDUA in a mucopolysaccharidosis type I murine model. J Control Release 209:37–46CrossRefPubMedGoogle Scholar
  80. 80.
    Dziubla TD, Shuvaev VV, Hong NK, Hawkins BJ, Madesh M, Takano H, Simone E, Nakada MT, Fisher A, Albelda SM (2008) Endothelial targeting of semi-permeable polymer nanocarriers for enzyme therapies. Biomaterials 29:215–227CrossRefPubMedGoogle Scholar
  81. 81.
    Wilson B (2009) Brain targeting PBCA nanoparticles and the blood–brain barrier. Nanomedicine 4:499–502CrossRefPubMedGoogle Scholar
  82. 82.
    Sinha V, Bansal K, Kaushik R, Kumria R, Trehan A (2004) Poly-ε-caprolactone microspheres and nanospheres: an overview. Int J Pharm 278:1–23CrossRefPubMedGoogle Scholar
  83. 83.
    Papademetriou I, Tsinas Z, Hsu J, Muro S (2014) Combination-targeting to multiple endothelial cell adhesion molecules modulates binding, endocytosis, and in vivo biodistribution of drug nanocarriers and their therapeutic cargoes. J Control Release 188:87–98CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Serrano D, Muro S (2014) Endothelial cell adhesion molecules and drug delivery applications. In: Aranda-Espinoza H (ed) Mechanobiology of the endothelium. CRC Press, Boca Raton, pp 4100–32Google Scholar
  85. 85.
    Serrano D, Bhowmick T, Chadha R, Garnacho C, Muro S (2012) Intercellular adhesion molecule 1 engagement modulates sphingomyelinase and ceramide, supporting uptake of drug carriers by the vascular endothelium. Arterioscler Thromb Vasc Biol 32:1178–1185CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Hsu J, Northrup L, Bhowmick T, Muro S (2012) Enhanced delivery of α-glucosidase for Pompe disease by ICAM-1-targeted nanocarriers: comparative performance of a strategy for three distinct lysosomal storage disorders. Nanomed Nanotechnol Biol Med 8:731–739CrossRefGoogle Scholar
  87. 87.
    Hsu J, Serrano D, Bhowmick T, Kumar K, Shen Y, Kuo YC, Garnacho C, Muro S (2011) Enhanced endothelial delivery and biochemical effects of α-galactosidase by ICAM-1-targeted nanocarriers for Fabry disease. J Control Release 149:323–331CrossRefPubMedGoogle Scholar
  88. 88.
    Hsu JB, Bhowmick T, Burks SR, Kao JP, Muro S (2014) Enhancing biodistribution of therapeutic enzymes in vivo by modulating surface coating and concentration of ICAM-1-targeted nanocarriers. J Biomed Nanotechnol 10:345–354CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Garnacho C, Dhami R, Simone E, Dziubla T, Leferovich J, Schuchman EH, Muzykantov V, Muro S (2008) Delivery of acid sphingomyelinase in normal and Niemann–Pick disease mice using intercellular adhesion molecule-1-targeted polymer nanocarriers. J Pharmacol Exp Ther 325:400–408CrossRefPubMedGoogle Scholar
  90. 90.
    Wang G, Mostafa NZ, Incani V, Kucharski C, Uludağ H (2012) Bisphosphonate-decorated lipid nanoparticles designed as drug carriers for bone diseases. J Biomed Mater Res A 100:684–693CrossRefPubMedGoogle Scholar
  91. 91.
    De Pasquale V, Sarogni P, Pistorio V, Cerulo G, Paladino S, Pavone LM (2018) Targeting heparan sulfate proteoglycans as a novel therapeutic strategy for mucopolysaccharidoses. Mol Ther Methods Clin Dev 10:8–16CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Weng Y, Liu J, Jin S, Guo W, Liang X, Hu Z (2017) Nanotechnology-based strategies for treatment of ocular disease. Acta Pharm Sin B 7:281–291CrossRefPubMedGoogle Scholar
  93. 93.
    Barar J, Aghanejad A, Fathi M, Omidi Y (2016) Advanced drug delivery and targeting technologies for the ocular diseases. BioImpacts 6:49CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Barar J, Javadzadeh AR, Omidi Y (2008) Ocular novel drug delivery: impacts of membranes and barriers. Expert Opin Drug Deliv 5:567–581CrossRefPubMedGoogle Scholar
  95. 95.
    Zhang L, Li Y, Zhang C, Wang Y, Song C (2009) Pharmacokinetics and tolerance study of intravitreal injection of dexamethasone-loaded nanoparticles in rabbits. Int J Nanomed 4:175CrossRefGoogle Scholar
  96. 96.
    Zawilska JB, Wojcieszak J, Olejniczak AB (2013) Prodrugs: a challenge for the drug development. Pharmacol Rep 65:1–14CrossRefPubMedGoogle Scholar
  97. 97.
    Abet V, Filace F, Recio J, Alvarez-Builla J, Burgos C (2017) Prodrug approach: an overview of recent cases. Eur J Med Chem 127:810–827CrossRefPubMedGoogle Scholar
  98. 98.
    Caruthers SD, Wickline SA, Lanza GM (2007) Nanotechnological applications in medicine. Curr Opin Biotechnol 18:26–30CrossRefPubMedGoogle Scholar
  99. 99.
    Bisceglie V (1934) Über die antineoplastische Immunität. Z Krebsforsch 40:141–158CrossRefGoogle Scholar
  100. 100.
    Nakama H, Ohsugi K, Otsuki T, Date I, Kosuga M, Okuyama T, Sakuragawa N (2006) Encapsulation cell therapy for mucopolysaccharidosis type VII using genetically engineered immortalized human amniotic epithelial cells. Tohoku J Exp Med 209:23–32CrossRefPubMedGoogle Scholar
  101. 101.
    Baldo G, Mayer FQ, Burin M, Carrillo-Farga J, Matte U, Giugliani R (2012) Recombinant encapsulated cells overexpressing alpha-l-iduronidase correct enzyme deficiency in human mucopolysaccharidosis type I cells. Cells Tissues Organs 195:323–329CrossRefPubMedGoogle Scholar
  102. 102.
    Baldo G, Mayer FQ, Martinelli B, Meyer FS, Burin M, Meurer L, Tavares AMV, Giugliani R, Matte U (2012) Intraperitoneal implant of recombinant encapsulated cells overexpressing alpha-l-iduronidase partially corrects visceral pathology in mucopolysaccharidosis type I mice. Cytotherapy 14:860–867CrossRefPubMedGoogle Scholar
  103. 103.
    Diel D, Lagranha VL, Schuh RS, Bruxel F, Matte U, Teixeira HF (2018) Optimization of alginate microcapsules containing cells overexpressing α-l-iduronidase using Box–Behnken design. Eur J Pharm Sci 111:29–37CrossRefPubMedGoogle Scholar
  104. 104.
    Omidi Y, Barar J (2012) Blood–brain barrier and effectiveness of therapy against brain tumors. In: Farassati F (ed) Novel therapeutic concepts in targeting glioma. IntechOpen Limited, London, pp 111–140Google Scholar
  105. 105.
    Pardridge WM (2010) Biopharmaceutical drug targeting to the brain. J Drug Target 18:157–167CrossRefPubMedGoogle Scholar
  106. 106.
    Abbott NJ, Ronnback L, Hansson E (2006) Astrocyte–endothelial interactions at the blood–brain barrier. Nat Rev Neurosci 7:41–53CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Omidi Y, Barar J (2012) Impacts of blood–brain barrier in drug delivery and targeting of brain tumors. BioImpacts 2:5PubMedPubMedCentralGoogle Scholar
  108. 108.
    Sonoda H, Morimoto H, Yoden E, Koshimura Y, Kinoshita M, Golovina G, Takagi H, Yamamoto R, Minami K, Mizoguchi A (2018) A blood–brain-barrier-penetrating anti-human transferrin receptor antibody fusion protein for neuronopathic mucopolysaccharidosis II. Mol Ther 26:1366–1374CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Fang F, Zou D, Wang W, Yin Y, Yin T, Hao S, Wang B, Wang G, Wang Y (2017) Non-invasive approaches for drug delivery to the brain based on the receptor mediated transport. Mater Sci Eng C 76:1316–1327CrossRefGoogle Scholar
  110. 110.
    Giugliani R (2012) Mucopolysacccharidoses: from understanding to treatment, a century of discoveries. Genet Mol Biol 35:924–931CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Mader KM, Beard H, King BM, Hopwood JJ (2008) Effect of high dose, repeated intra-cerebrospinal fluid injection of sulphamidase on neuropathology in mucopolysaccharidosis type IIIA mice. Genes Brain Behav 7:740–753CrossRefPubMedGoogle Scholar
  112. 112.
    Dickson P, McEntee M, Vogler C, Le S, Levy B, Peinovich M, Hanson S, Passage M, Kakkis E (2007) Intrathecal enzyme replacement therapy: successful treatment of brain disease via the cerebrospinal fluid. Mol Genet Metab 91:61–68CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Kakkis E, McEntee M, Vogler C, Le S, Levy B, Belichenko P, Mobley W, Dickson P, Hanson S, Passage M (2004) Intrathecal enzyme replacement therapy reduces lysosomal storage in the brain and meninges of the canine model of MPS I. Mol Genet Metab 83:163–174CrossRefPubMedGoogle Scholar
  114. 114.
    Dickson PI, Hanson S, McEntee MF, Vite CH, Vogler CA, Mlikotic A, Chen AH, Ponder KP, Haskins ME, Tippin BL, Le SQ, Passage MB, Guerra C, Dierenfeld A, Jens J, Snella E, Kan SH, Ellinwood NM (2010) Early versus late treatment of spinal cord compression with long-term intrathecal enzyme replacement therapy in canine mucopolysaccharidosis type I. Mol Genet Metab 101:115–122CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Rattazzi M, Lanse S, McCullough R, Nester J, Jacobs E (1980) Towards enzyme replacement in GM2 gangliosidosis: organ disposition and induced central nervous system uptake of human beta-hexosaminidase in the cat. Birth Defects Orig Artic Ser 16:179–193PubMedGoogle Scholar
  116. 116.
    Boado RJ, Lu JZ, Hui EKW, Sumbria RK, Pardridge WM (2013) Pharmacokinetics and brain uptake in the rhesus monkey of a fusion protein of arylsulfatase a and a monoclonal antibody against the human insulin receptor. Biotechnol Bioeng 110:1456–1465CrossRefPubMedGoogle Scholar
  117. 117.
    Mühlstein A, Gelperina S, Kreuter J (2013) Development of nanoparticle-bound arylsulfatase B for enzyme replacement therapy of mucopolysaccharidosis VI. Pharmazie 68:549–554PubMedGoogle Scholar
  118. 118.
    Donida B, Tauffner B, Raabe M, Immich MF, de Farias MA, de Sá Coutinho D, Machado AZ, Kessler RG, Portugal RV, Bernardi A (2018) Monoolein-based nanoparticles for drug delivery to the central nervous system: a platform for lysosomal storage disorder treatment. Eur J Pharm Biopharm 133:96–103CrossRefPubMedGoogle Scholar
  119. 119.
    Acosta W, Ayala J, Dolan MC, Cramer CL (2015) RTB lectin: a novel receptor-independent delivery system for lysosomal enzyme replacement therapies. Sci Rep 5:14144CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Poswar F, Baldo G, Giugliani R (2017) Phase I and II clinical trials for the mucopolysaccharidoses. Expert Opin Investig Drugs 26:1331–1340CrossRefPubMedGoogle Scholar
  121. 121.
    Giugliani R, Nestrasil I, Chen S, Pardridge W, Rioux P (2017) Intravenous infusion of iduronidase-IgG and its impact on the central nervous system in children with Hurler syndrome. Mol Genet Metab 120:S55–S56CrossRefGoogle Scholar
  122. 122.
    Pardridge WM, Boado RJ, Giugliani R, Schmidt M (2018) Plasma pharmacokinetics of valanafusp alpha, a human insulin receptor antibody-iduronidase fusion protein, in patients with mucopolysaccharidosis type I. BioDrugs 32:169–176CrossRefPubMedGoogle Scholar
  123. 123.
    Boado RJ, Hui EK-W, Lu JZ, Sumbria RK, Pardridge WM (2013) Blood–brain barrier molecular trojan horse enables imaging of brain uptake of radioiodinated recombinant protein in the rhesus monkey. Bioconjug Chem 24:1741–1749CrossRefPubMedGoogle Scholar
  124. 124.
    Okuyama T, Sakai N, Yamamoto T, Yamaoka M, Tomio T (2018) Novel blood–brain barrier delivery system to treat CNS in MPS II: first clinical trial of anti-transferrin receptor antibody fused enzyme therapy. Mol Genet Metab 123:S109Google Scholar
  125. 125.
    Sohn YB, Cho SY, Lee J, Kwun Y, Huh R, Jin D-K (2015) Safety and efficacy of enzyme replacement therapy with idursulfase beta in children aged younger than 6 years with Hunter syndrome. Mol Genet Metab 114:156–160CrossRefPubMedGoogle Scholar
  126. 126.
    Muenzer J, Gucsavas-Calikoglu M, McCandless SE, Schuetz TJ, Kimura A (2007) A phase I/II clinical trial of enzyme replacement therapy in mucopolysaccharidosis II (Hunter syndrome). Mol Genet Metab 90:329–337CrossRefPubMedGoogle Scholar
  127. 127.
    Sohn YB, Ko A-R, Seong M-R, Lee S, Kim MR, Cho SY, Kim J-S, Sakaguchi M, Nakazawa T, Kosuga M (2018) The efficacy of intracerebroventricular idursulfase-beta enzyme replacement therapy in mucopolysaccharidosis II murine model: heparan sulfate in cerebrospinal fluid as a clinical biomarker of neuropathology. J Inherit Metab Dis 41:1235–1246CrossRefPubMedGoogle Scholar
  128. 128.
    Ghosh A, Shapiro E, Rust S, Delaney K, Parker S, Shaywitz AJ, Morte A, Bubb G, Cleary M, Bo T (2017) Recommendations on clinical trial design for treatment of mucopolysaccharidosis type III. Orphanet J Rare Dis 12:117CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Rossomando A, Chen LL, Ciatto C, Liu J, Hu W, Hayes M, Rojas-Caro S, Quinn AG (2014) SBC-103, a recombinant human alpha-N-acetylglucosaminidase, demonstrates mannose-6-phosphate receptor dependent transport in an in vitro blood–brain barrier model. Mol Genet Metab 111:S91CrossRefGoogle Scholar
  130. 130.
    Shaywitz AJ, Oh M, Kent S (2016) Design and rationale of the study programs for BMN 250, a novel enzyme replacement therapy (ERT) for Sanfilippo syndrome type B. Mol Genet Metab 117:S105–S106CrossRefGoogle Scholar
  131. 131.
    Giugliani R, Dalla Corte A, Poswar F, Vanzella C, Horovitz D, Riegel M, Baldo G, Vairo F (2018) Intrathecal/intracerebroventricular enzyme replacement therapy for the mucopolysaccharidoses: efficacy, safety, and prospects. Expert Opin Orphan Drugs 6:403–411CrossRefGoogle Scholar
  132. 132.
    Pintos-Morell G, Blasco-Alonso J, Couce ML, Gutiérrez-Solana LG, Guillén-Navarro E, O’Callaghan M, del Toro M (2018) Elosulfase alfa for mucopolysaccharidosis type IVA: real-world experience in 7 patients from the Spanish Morquio-A early access program. Mol Genet Metab Rep 15:116–120CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Solanki GA, Sun PP, Martin KW, Hendriksz CJ, Lampe C, Guffon N, Hung A, Sisic Z, Shediac R, Harmatz PR (2016) Cervical cord compression in mucopolysaccharidosis VI (MPS VI): findings from the MPS VI Clinical Surveillance Program (CSP). Mol Genet Metab 118:310–318CrossRefPubMedGoogle Scholar
  134. 134.
    Qi Y, McKeever K, Taylor J, Haller C, Song W, Jones SA, Shi J (2018) Pharmacokinetic and pharmacodynamic modeling to optimize the dose of vestronidase alfa, an enzyme replacement therapy for treatment of patients with mucopolysaccharidosis type VII: results from three trials. Clin Pharmacokinet 58:1–11Google Scholar
  135. 135.
    Harmatz P, Whitley CB, Wang RY, Bauer M, Song W, Jacobs K, Schwartz E, Haller C, Kakkis E (2017) A novel, randomized, placebo-controlled, blind-start, single-crossover phase 3 study to assess the efficacy and safety of UX003 (rhGUS) enzyme replacement therapy in patients with MPS VII. Mol Genet Metab 120:S63CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Connective Tissue Diseases Research CenterTabriz University of Medical SciencesTabrizIran
  2. 2.Research Center for Pharmaceutical Nanotechnology, Biomedicine InstituteTabriz University of Medical SciencesTabrizIran
  3. 3.Liver and Gastrointestinal Diseases Research CenterTabriz University of Medical SciencesTabrizIran
  4. 4.Department of Pharmaceutics, Faculty of PharmacyTabriz University of Medical SciencesTabrizIran
  5. 5.Department of Neurology, Sidney Kimmel Medical CollegeThomas Jefferson UniversityPhiladelphiaUSA

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