Intrathecal delivery of protein therapeutics to the brain: A critical reassessment

Pharmacology and Therapeutics

Volumn 144, Issue 2, 2014, Pages 114-122

  Calias, Pericles ^a   Banks, William A ^b,c   Begley, David ^d   Scarpa, Maurizio ^e   Dickson, Patricia ^f  

^a SHIRE   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF PADOVA   (Italy)

^f HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

Blood brain barrier; Central nervous system; Drug delivery; Intracerebroventricular; Intrathecal; Recombinant proteins

Indexed keywords

LYSOSOME ENZYME; NOGO A ANTIBODY; RECOMBINANT PROTEIN; TRASTUZUMAB;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN FUNCTION; BRAIN METASTASIS; CANCER CHEMOTHERAPY; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CEREBROVASCULAR ACCIDENT; ENZYME REPLACEMENT; HUMAN; INTERSTITIAL FLUID; INTRATHECAL DRUG ADMINISTRATION; LYSOSOME STORAGE DISEASE; NEUROPATHIC LYSOSOMAL STORAGE DISEASE; ANIMAL; CENTRAL NERVOUS SYSTEM DISEASES; HYDRODYNAMICS; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CENTRAL NERVOUS SYSTEM DISEASES; CEREBROSPINAL FLUID; HUMANS; HYDRODYNAMICS; INJECTIONS, SPINAL; RECOMBINANT PROTEINS;

EID: 84907885590     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2014.05.009     Document Type: Review

References (104)

1. M.I. Alam, S. Beg, A. Samad, S. Baboota, K. Kohli, and J. Ali Strategy for effective brain drug delivery Eur J Pharm Sci 40 2010 385 403
2. K. Altundag, M.L. Bondy, N.Q. Mirza, S.W. Kau, K. Broglio, and G.N. Hortobagyi Clinicopathologic characteristics and prognostic factors in 420 metastatic breast cancer patients with central nervous system metastasis Cancer 110 2007 2640 2647
3. D. Aprili, O. Bandschapp, C. Rochlitz, A. Urwyler, and W. Ruppen Serious complications associated with external intrathecal catheters used in cancer pain patients: A systematic review and meta-analysis Anesthesiology 111 2009 1346 1355
4. W.A. Banks Critical roles of efflux systems in health and disease E.M. Taylor, Efflux Transporters and the Blood-Brain Barrier 2005 Nova Science Publishers, Incorporated Hauppauge, New York 21 53
5. W.A. Banks The blood-brain barrier as a cause of obesity Curr Pharm Des 14 2008 1606 1614
6. W.A. Banks Brain meets body: The blood-brain barrier as an endocrine interface Endocrinology 153 2012 4111 4119
7. J.S. Barnholtz-Sloan, A.E. Sloan, F.G. Davis, F.D. Vigneau, P. Lai, and R.E. Sawaya Incidence proportions of brain metastases in patients diagnosed (1973 to 2001) in the Metropolitan Detroit Cancer Surveillance System J Clin Oncol 22 2004 2865 2872
8. R.E. Becker, and N.H. Greig Lost in translation: Neuropsychiatric drug development Sci Transl Med 2 2010 61rv66
9. D.J. Begley ABC transporters and the blood-brain barrier Curr Pharm Des 10 2004 1295 1312
10. D.J. Begley Brain superhighways Sci Transl Med 4 2012 147 fs129
11. D.J. Begley, E.U. Khan, C. Rollinson, J. Abbott, A. Regina, and F. Roux The Role of Brain Extracellular Fluid Production and Efflux Mechanisms in Drug Transport to the Brain D.J. Begley, M.W. Bradbury, J. Kreuter, The Blood-Brain Barrier and Drug Delivery to the CNS 2000 Marcel Dekker, Inc. New York 93 108
12. P.V. Belichenko, P.I. Dickson, M. Passage, S. Jungles, W.C. Mobley, and E.D. Kakkis Penetration, diffusion, and uptake of recombinant human alpha-L-iduronidase after intraventricular injection into the rat brain Mol Genet Metab 86 2005 141 149
13. A. Bora, C. Anderson, M. Bachani, A. Nath, and R.J. Cotter Robust two-dimensional separation of intact proteins for bottom-up tandem mass spectrometry of the human CSF proteome J Proteome Res 11 2012 3143 3149
14. A. Bosch, E. Perret, N. Desmaris, and J.M. Heard Long-term and significant correction of brain lesions in adult mucopolysaccharidosis type VII mice using recombinant AAV vectors Mol Ther 1 2000 63 70
15. M. Boulton, M. Flessner, D. Armstrong, R. Mohamed, J. Hay, and M. Johnston Contribution of extracranial lymphatics and arachnoid villi to the clearance of a CSF tracer in the rat Am J Physiol 276 1999 R818 R823
16. A.P. Braen, J. Perron, P. Tellier, A.R. Catala, G. Kolaitis, and W. Geng A 4-week intrathecal toxicity and pharmacokinetic study with trastuzumab in cynomolgus monkeys Int J Toxicol 29 2010 259 267
17. F. Bray, J.S. Ren, E. Masuyer, and J. Ferlay Global estimates of cancer prevalence for 27 sites in the adult population in 2008 Int J Cancer 132 2012 1133 1145
18. D.S. Brandt Intrathecal trastuzumab: 46 months and no progression Community Oncol 9 2012 232 234
19. M.A. Cabrera-Salazar, S.D. Bercury, R.J. Ziegler, J. Marshall, B.L. Hodges, and W.L. Chuang Intracerebroventricular delivery of glucocerebrosidase reduces substrates and increases lifespan in a mouse model of neuronopathic Gaucher disease Exp Neurol 225 2010 436 444
20. P. Calias, M. Papisov, J. Pan, N. Savioli, V. Belov, and Y. Huang CNS penetration of intrathecal-lumbar idursulfase in the monkey, dog and mouse: Implications for neurological outcomes of lysosomal storage disorder PLoS One 7 2012 e30341
21. M. Chang, J.D. Cooper, D.E. Sleat, S.H. Cheng, J.C. Dodge, and M.A. Passini Intraventricular enzyme replacement improves disease phenotypes in a mouse model of late infantile neuronal ceroid lipofuscinosis Mol Ther 16 2008 649 656
22. A. Chen, C. Vogler, M. McEntee, S. Hanson, N.M. Ellinwood, and J. Jens Glycosaminoglycan storage in neuroanatomical regions of mucopolysaccharidosis I dogs following intrathecal recombinant human iduronidase APMIS 119 2011 513 521
23. A. Consiglio, A. Quattrini, S. Martino, J.C. Bensadoun, D. Dolcetta, and A. Trojani In vivo gene therapy of metachromatic leukodystrophy by lentiviral vectors: Correction of neuropathology and protection against learning impairments in affected mice Nat Med 7 2001 310 316
24. A.C. Crawley, N. Marshall, H. Beard, S. Hassiotis, V. Walsh, and B. King Enzyme replacement reduces neuropathology in MPS IIIA dogs Neurobiol Dis 43 2011 422 434
25. H.F. Cserr, and P.M. Knopf Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: A new view Immunol Today 13 1992 507 512
26. H.F. Cserr, and C.S. Patlak Secretion and Bulk Flow of Interstitial Fluid M.W.B. Bradbury, Physiology and Pharmacology of the Blood-Brain Barrier Handbook of Experimental Pharmacology. vol. 103 1992 Springer Berlin Heidelberg Berlin 245 261
27. H. Davson, and M.B. Segal The return of the cerebrospinal fluid to the blood: The drainage mechanism Physiology of the CSF and Blood-Brain Barriers 1996 CRC Press Boca Raton 489 523
28. P.I. Dickson, N.M. Ellinwood, J.R. Brown, R.G. Witt, S.Q. Le, and M.B. Passage Specific antibody titer alters the effectiveness of intrathecal enzyme replacement therapy in canine mucopolysaccharidosis I Mol Genet Metab 106 2012 68 72
29. P. Dickson, M. McEntee, C. Vogler, S. Le, B. Levy, and M. Peinovich Intrathecal enzyme replacement therapy: Successful treatment of brain disease via the cerebrospinal fluid Mol Genet Metab 91 2007 61 68
30. A.D. Dierenfeld, M.F. McEntee, C.A. Vogler, C.H. Vite, A.H. Chen, and M. Passage Replacing the enzyme alpha-l-iduronidase at birth ameliorates symptoms in the brain and periphery of dogs with mucopolysaccharidosis type I Sci Transl Med 2 2010 60ra89
31. J.C. Dodge, J. Clarke, C.M. Treleaven, T.V. Taksir, D.A. Griffiths, and W. Yang Intracerebroventricular infusion of acid sphingomyelinase corrects CNS manifestations in a mouse model of Niemann-Pick A disease Exp Neurol 215 2009 349 357
32. D. Dogrukol-Ak, V.B. Kumar, J.S. Ryerse, S.A. Farr, S. Verma, and K. Nonaka Isolation of peptide transport system-6 from brain endothelial cells: Therapeutic effects with antisense inhibition in Alzheimer's and stroke models J Cereb Blood Flow Metab 29 2009 411 422
33. A. Du Pen Care and management of intrathecal and epidural catheters J Infus Nurs 28 2005 377 381
34. B. Engelhardt The blood-central nervous system barriers actively control immune cell entry into the central nervous system Curr Pharm Des 14 2008 1555 1565
35. B.R. Felice, T.L. Wright, R.B. Boyd, M.T. Butt, R.W. Pfeifer, and J. Pan Safety evaluation of chronic intrathecal administration of idursulfase-IT in cynomolgus monkeys Toxicol Pathol 39 2011 879 892
36. C. Ferrario, A. Davidson, N. Bouganim, R. Aloyz, and L.C. Panasci Intrathecal trastuzumab and thiotepa for leptomeningeal spread of breast cancer Ann Oncol 20 2009 792 795
37. K.A. Follett, K. Burchiel, T. Deer, S. Dupen, J. Prager, and M.S. Turner Prevention of intrathecal drug delivery catheter-related complications Neuromodulation 6 2003 32 41
38. J.F. Ghersi-Egea, P.D. Gorevic, J. Ghiso, B. Frangione, C.S. Patlak, and J.D. Fenstermacher Fate of cerebrospinal fluid-borne amyloid beta-peptide: Rapid clearance into blood and appreciable accumulation by cerebral arteries J Neurochem 67 1996 880 883
39. H.L. Greene, G. Hug, and W.K. Schubert Metachromatic leukodystrophy. Treatment with arylsulfatase-A Arch Neurol 20 1969 147 153
40. L. Guo, J. Ren, and X. Jiang Perspectives on brain-targeting drug delivery systems Curr Pharm Biotechnol 13 2012 2310 2318
41. A. Hamadjida, A.F. Wyss, A. Mir, M.E. Schwab, A. Belhaj-Saif, and E.M. Rouiller Influence of anti-Nogo-A antibody treatment on the reorganization of callosal connectivity of the premotor cortical areas following unilateral lesion of primary motor cortex (M1) in adult macaque monkeys Exp Brain Res 223 2012 321 340
42. K.M. Hemsley, and J.J. Hopwood Delivery of recombinant proteins via the cerebrospinal fluid as a therapy option for neurodegenerative lysosomal storage diseases Int J Clin Pharmacol Ther 47 Suppl. 1 2009 S118 S123
43. K.M. Hemsley, H. Beard, B.M. King, and J.J. Hopwood Effect of high dose, repeated intra-CSF injection of sulphamidase on neuropathology in MPS IIIA mice Genes Brain Behav 7 2008 740 753
44. K.M. Hemsley, E.J. Norman, A.C. Crawley, D. Auclair, B. King, and M. Fuller Effect of cisternal sulfamidase delivery in MPS IIIA Huntaway dogs - A proof of principle study Mol Genet Metab 98 2009 383 392
45. A. Holmfred, T. Vikerfors, L. Berggren, and A. Gupta Intrathecal catheters with subcutaneous port systems in patients with severe cancer-related pain managed out of hospital: The risk of infection J Pain Symptom Manage 31 2006 568 572
46. M. Holtta, H. Zetterberg, E. Mirgorodskaya, N. Mattsson, K. Blennow, and J. Gobom Peptidome analysis of cerebrospinal fluid by LC-MALDI MS PLoS One 7 2012 e42555
47. T. Higuchi, H. Shimizu, T. Fukuda, S. Kawagoe, J. Matsumoto, and Y. Shimada Enzyme replacement therapy (ERT) procedure for mucopolysaccharidosis type II (MPS II) by intraventricular administration (IVA) in murine MPS II Mol Genet Metab 107 2012 122 128
48. J.J. Iliff, M. Wang, Y. Liao, B.A. Plogg, W. Peng, and G.A. Gundersen A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta Sci Transl Med 4 2012 147ra111
49. C.E. Johanson The Choroid Plexus-Arachnoid Membrane-Cerebrospinal Fluid System A.A. Boulton, G.B. Baker, W. Walz, Neuromethods; The Neuronal Microenvironment 1988 The Humana Press Clifton, New Jersey 33 104
50. C.E. Johanson, J.A. Duncan III, P.M. Kling, T. Brinker, E.G. Stopa, and G.D. Silverberg Multiplicity of cerebrospinal fluid functions: New challenges in health and disease Cerebrospinal Fluid Res 5 2008 10
51. C.E. Johanson, J.A. Duncan III, P.M. Klinge, T. Brinker, E.G. Stopa, and G.D. Silverberg Multiplicity of cerebrospinal fluid functions: New challenges in health and disease Cerebrospinal Fluid Res 5 2008 10
52. L. Jorgensen, E.H. Moeller, M. van de Weert, H.M. Nielsen, and S. Frokjaer Preparing and evaluating delivery systems for proteins Eur J Pharm Sci 29 2006 174 182
53. L. Jorgensen, and H.M. Nielson Introduction Delivery Technologies for Biopharmaceuticals: Peptides, Proteins, Nucleic Acids and Vaccines 2009 John Wiley & Sons, Ltd Hoboken, NJ 3 8
54. E. Kakkis, M. McEntee, C. Vogler, S. Le, B. Levy, and P. Belichenko Intrathecal enzyme replacement therapy reduces lysosomal storage in the brain and meninges of the canine model of MPS I Mol Genet Metab 83 2004 163 174
55. P.M. Knopf, H.F. Cserr, S.C. Nolan, T.Y. Wu, and C.J. Harling-Berg Physiology and immunology of lymphatic drainage of interstitial and cerebrospinal fluid from the brain Neuropathol Appl Neurobiol 21 1995 175 180
56. C. LeBel, A. Bourdeau, D. Lau, and P. Hunt Biological response to peripheral and central administration of recombinant human leptin in dogs Obes Res 7 1999 577 585
57. L.R. Laufman, and K.F. Forsthoefel Use of intrathecal trastuzumab in a patient with carcinomatous meningitis Clin Breast Cancer 2 2001 235
58. W.C. Lee, Y.K. Tsoi, F.J. Troendle, M.W. DeLucia, Z. Ahmed, C.A. Dicky, D.W. Dickson, and C.B. Eckman Single-dose intracerebroventricular administration of galactocerebrosidase improves survival in a mouse model of globoid cell leukodystrophy FASEB J 21 2007 2520 2527
59. T.J. McCarthy, W.A. Banks, C.L. Farrell, S. Adamu, C.P. Derdeyn, and A.Z. Snyder Positron emission tomography shows that intrathecal leptin reaches the hypothalamus in baboons J Pharmacol Exp Ther 301 2002 878 883
60. M. Mego, Z. Sycova-Mila, J. Obertova, J. Rajec, S. Liskova, and P. Palacka Intrathecal administration of trastuzumab with cytarabine and methotrexate in breast cancer patients with leptomeningeal carcinomatosis Breast 20 2011 478 480
61. O. Mir, S. Ropert, J. Alexandre, F. Lemare, and F. Goldwasser High-dose intrathecal trastuzumab for leptomeningeal metastases secondary to HER-2 overexpressing breast cancer Ann Oncol 19 2008 1978 1980
62. F. Motta, and C.E. Antonello Analysis of complications in 430 consecutive pediatric patients treated with intrathecal baclofen therapy: 14-year experience J Neurosurg Pediatr 13 2014 301 306
63. M.V. Munoz-Rojas, T. Vieira, R. Costa, S. Fagondes, A. John, and L.B. Jardim Intrathecal enzyme replacement therapy in a patient with mucopolysaccharidosis type I and symptomatic spinal cord compression Am J Med Genet A 146A 2008 2538 2544
64. T.N. Nagaraja, P. Patel, M. Gorski, P.D. Gorevic, C.S. Patlak, and J.D. Fenstermacher In normal rat, intraventricularly administered insulin-like growth factor-1 is rapidly cleared from CSF with limited distribution into brain Cerebrospinal Fluid Res 2 2005 5
65. E. Neuwelt, N.J. Abbott, L. Abrey, W.A. Banks, B. Blakley, and T. Davis Strategies to advance translational research into brain barriers Lancet Neurol 7 2008 84 96
66. J.G. Nutt, K.J. Burchiel, C.L. Comella, J. Jankovic, A.E. Lang, and E.R. Laws Jr. Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD Neurology 60 2003 69 73
67. W.H. Oldendorf Brain uptake of radio-labelled amino acids, amines and hexoses after arterial injection Am J Physiol 221 1971 1629 1639
68. M. Oliveira, S. Braga, J.L. Passos-Coelho, R. Fonseca, and J. Oliveira Complete response in HER2+ leptomeningeal carcinomatosis from breast cancer with intrathecal trastuzumab Breast Cancer Res Treat 127 2011 841 844
69. Organization, W. H. Neurological Disorders: Public Health Challenges vol. 2012 2006
70. W. Pan, and A.J. Kastin Entry of EGF into brain is rapid and saturable Peptides 20 1999 1091 1098
71. W.M. Pardridge Blood-brain barrier delivery Drug Discov Today 12 2007 54 61
72. M.A. Passini, E.B. Lee, G.G. Heuer, and J.H. Wolfe Distribution of a lysosomal enzyme in the adult brain by axonal transport and by cells of the rostral migratory stream J Neurosci 22 2002 6437 6446
73. M.M. Patel, B.R. Goyal, S.V. Bhadada, J.S. Bhatt, and A.F. Amin Getting into the brain: Approaches to enhance brain drug delivery CNS Drugs 23 2009 35 58
74. V. Pernet, and M.E. Schwab The role of Nogo-A in axonal plasticity, regrowth and repair Cell Tissue Res 349 2012 97 104
75. R.W. Pfeifer, B.R. Felice, R.B. Boyd, M.T. Butt, J.A. Ruiz, and M.W. Heartlein Safety evaluation of chronic intrathecal administration of heparan N-sulfatase in juvenile cynomolgus monkeys Drug Deliv Transl Res 2 2012 187 200
76. C. Platini, J. Long, and S. Walter Meningeal carcinomatosis from breast cancer treated with intrathecal trastuzumab Lancet Oncol 7 2006 778 780
77. N. Quan, and W.A. Banks Brain-immune communication pathways Brain Behav Immun 21 2007 727 735
78. M. Rajadhyaksha, T. Boyden, J. Liras, A. El-Kattan, and J. Brodfuehrer Current advances in delivery of biotherapeutics across the blood-brain barrier Curr Drug Discov Technol 8 2011 87 101
79. M.L. Rennels, O.R. Blaumanis, and P.A. Grady Rapid solute transport throughout the brain via paravascular fluid pathways Adv Neurol 52 1990 431 439
80. M.L. Rennels, T.F. Gregory, O.R. Blaumanis, K. Fujimoto, and P.A. Grady Evidence for a 'paravascular' fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space Brain Res 326 1985 47 63
81. J. Scallan, V.H. Huxley, and R.J. Korthuis The Interstitium Capillary Fluid Exchange: Regulation, Functions, and Pathology 2010 Morgan & Claypool Life Sciences San Rafael, CA 21 32
82. J.P. Schouten, C.J. McElgunn, R. Waaijer, D. Zwijnenburg, F. Diepvens, and G. Pals Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification Nucleic Acids Res 30 2002 e57
83. L.J. Schouten, J. Rutten, H.A. Huveneers, and A. Twijnstra Incidence of brain metastases in a cohort of patients with carcinoma of the breast, colon, kidney, and lung and melanoma Cancer 94 2002 2698 2705
84. A.F. Skorupa, K.J. Fisher, J.M. Wilson, M.K. Parente, and J.H. Wolfe Sustained production of beta-glucuronidase from localized sites after AAV vector gene transfer results in widespread distribution of enzyme and reversal of lysosomal storage lesions in a large volume of brain in mucopolysaccharidosis VII mice Exp Neurol 160 1999 17 27
85. D.J. Slamon, B. Leyland-Jones, S. Shak, H. Fuchs, V. Paton, and A. Bajamonde Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2 N Engl J Med 344 2001 783 792
86. D.E. Smith, C.E. Johanson, and R.F. Keep Peptide and peptide analog transport systems at the blood-CSF barrier Adv Drug Deliv Rev 56 2004 1765 1791
87. I. Smith, M. Procter, R.D. Gelber, S. Guillaume, A. Feyereislova, and M. Dowsett 2-year follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer: A randomised controlled trial Lancet 369 2007 29 36
88. H.J. Stemmler, M. Schmitt, N. Harbeck, A. Willems, H. Bernhard, and D. Lassig Application of intrathecal trastuzumab (Herceptin™) for treatment of meningeal carcinomatosis in HER2-overexpressing metastatic breast cancer Oncol Rep 15 2006 1373 1377
89. H.J. Stemmler, M. Schmitt, A. Willems, H. Bernhard, N. Harbeck, and V. Heinemann Ratio of trastuzumab levels in serum and cerebrospinal fluid is altered in HER2-positive breast cancer patients with brain metastases and impairment of blood-brain barrier Anticancer Drugs 18 2007 23 28
90. H.J. Stemmler, K. Mengele, M. Schmitt, N. Harbeck, D. Laessig, and K.A. Herrmann Intrathecal trastuzumab (Herceptin) and methotrexate for meningeal carcinomatosis in HER2-overexpressing metastatic breast cancer: A case report Anticancer Drugs 19 2008 832 836
91. S. Stroobants, D. Gerlach, F. Matthes, D. Hartmann, J. Fogh, and V. Gieselmann Intracerebroventricular enzyme infusion corrects central nervous system pathology and dysfunction in a mouse model of metachromatic leukodystrophy Hum Mol Genet 20 2011 2760 2769
92. T. Taira, T. Ueta, Y. Katayama, M. Kimizuka, A. Nemoto, and H. Mizusawa Rate of complications among the recipients of intrathecal baclofen pump in Japan: A multicenter study Neuromodulation 16 2013 266 272 (discussion 272)
93. M.L. Tan, P.F. Choong, and C.R. Dass Recent developments in liposomes, microparticles and nanoparticles for protein and peptide drug delivery Peptides 31 2010 184 193
94. S.K. Tayebati, I.E. Nwankwo, and F. Amenta Intranasal drug delivery to the central nervous system: Present status and future outlook Curr Pharm Des 19 2013 510 526
95. S.Y. Tsai, T.M. Markus, E.M. Andrews, J.L. Cheatwood, A.J. Emerick, and A.K. Mir Intrathecal treatment with anti-Nogo-A antibody improves functional recovery in adult rats after stroke Exp Brain Res 182 2007 261 266
96. D. Tsuji, H. Akeboshi, K. Matsuoka, H. Yasuoka, E. Miyasaki, and Y. Kasahara Highly phosphomannosylated enzyme replacement therapy for GM2 gangliosidosis Ann Neurol 69 2011 691 701
97. P. Vlieghe, and M. Khrestchatisky Medicinal chemistry based approaches and nanotechnology-based systems to improve CNS drug targeting and delivery Med Res Rev 33 2013 457 516
98. C. Vogler, B. Levy, N.J. Galvin, C. Thorpe, M.S. Sands, and J.E. Barker Enzyme replacement in murine mucopolysaccharidosis type VII: Neuronal and glial response to beta-glucuronidase requires early initiation of enzyme replacement therapy Pediatr Res 45 1999 838 844
99. B.R. Vuillemenot, M.L. Katz, J.R. Coates, D. Kennedy, P. Tiger, and S. Kanazono Intrathecal tripeptidyl-peptidase 1 reduces lysosomal storage in a canine model of late infantile neuronal ceroid lipofuscinosis Mol Genet Metab 104 2011 325 337
100. H. Wiig, and M.A. Swartz Interstitial fluid and lymph formation and transport: Physiological regulation and roles in inflammation and cancer Physiol Rev 92 2012 1005 1060
101. B. Winchester, A. Vellodi, and E. Young The molecular basis of lysosomal storage diseases and their treatment Biochem Soc Trans 28 2000 150 154
102. S. Xu, L. Wang, M. El-Banna, I. Sohar, D.E. Sleat, and P. Lobel Large-volume intrathecal enzyme delivery increases survival of a mouse model of late infantile neuronal ceroid lipofuscinosis Mol Ther 19 2011 1842 1848
103. Y.Z. Zhao, C.T. Lu, X.K. Li, and J. Cai Ultrasound-mediated strategies in opening brain barriers for drug brain delivery Expert Opin Drug Deliv 10 2013 987 1001
104. R.J. Ziegler, E.A. Salegio, J.C. Dodge, J. Bringas, C.M. Treleaven, and S.D. Bercury Distribution of acid sphingomyelinase in rodent and non-human primate brain after intracerebroventricular infusion Exp Neurol 231 2011 261 271