Collaborative development of 2-hydroxypropyl-β-Cyclodextrin for the treatment of Niemann-Pick Type C1 Disease

Current Topics in Medicinal Chemistry

Volumn 14, Issue 3, 2014, Pages 330-339

  Ottinger, Elizabeth A ^a   Kao, Mark L ^b   Carrillo Carrasco, Nuria ^a   Yanjanin, Nicole ^c   Shankar, Roopa Kanakatti ^c   Janssen, Marjo ^b   Brewster, Marcus ^b   Scott, Ilona ^b   Xu, Xin ^a   Cradock, Jim ^a   Terse, Pramod ^a   Dehdashti, Seameen J ^a   Marugan, Juan ^a   Zheng, Wei ^a   Portilla, Lili ^a   Hubbs, Alan ^d   Pavan, William J ^e   Heiss, John ^f   Vite, Charles H ^g   Walkley, Steven U ^h   Ory, Daniel S ⁱ   Silber, Steven A ^b   Porter, Forbes D ^c   Austin, Christopher P ^a   Mckew, John C ^a   more..

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^f NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

^h ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

ⁱ WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

2 hydroxypropyl Cyclodextrin; Neurodegenerative rare disease; Niemann Pick disease type C1; Translational research

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; BIOLOGICAL MARKER; CHOLESTEROL; CYCLODEXTRIN; ITRACONAZOLE;

ARTICLE; DOSE RESPONSE; DRUG EFFICACY; DRUG RESEARCH; DRUG SAFETY; FOOD AND DRUG ADMINISTRATION; GENE; HUMAN; NIEMANN PICK DISEASE; NONHUMAN; NPC1 GENE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PUBLIC-PRIVATE PARTNERSHIP; SINGLE DRUG DOSE; WHOLE BODY IMAGING;

BETA-CYCLODEXTRINS; COOPERATIVE BEHAVIOR; DRUG DISCOVERY; HUMANS; NATIONAL INSTITUTES OF HEALTH (U.S.); NEGLECTED DISEASES; NIEMANN-PICK DISEASE, TYPE C; RARE DISEASES; UNITED STATES;

EID: 84894065946     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026613666131127160118     Document Type: Article

References (86)

1. FDA Orphan Drug Designation. http://www.fda.gov/ForIndustry/DevelopingProductsforRareDiseasesConditions/Howtoapplyfor OrphanProductDesignation/default/.htm (Accessed April 1, 2013).
2. European Medicines Agency Orphan Drug Designation. http://www.emea.europa.eu/ema/index.jsp?curl=pages/regulation/general/general_content_000029.jsp&mid=WC0b01ac05800240ce (Accessed April 1, 2013).
3. Office of Rare Disease Research. http://www.rarediseases.info.nih.gov/Default.aspx (Accessed April 1, 2013).
4. Getz, K.A.; Kaitin, K.I. Open innovation: the new face of pharmaceutical research and development. Expert. Rev. Clin. Pharmacol., 2012, 5(5), 481-483.
5. Munos, B.H.; Chin, W.W. A call for sharing: adapting pharmaceutical research to new realities. Sci.Transl. Med., 2009, 1(9), 9cm8.
6. Munos, B.H.; Chin, W.W. How to revive breakthrough innovation in the pharmaceutical industry. Sci. Transl. Med., 2011, 3(89), 89cm16.
7. Adams, C.P.; Brantner, V.V. Spending on new drug development1. Health Economics, 2010, 19(2), 130-141.
8. Deloitte Center for Health Solutions. Measuring Return from Pharmaceutical Innovation 2012: Is R&D Earning its Investment. http://www.deloitte.com/view/en_XB/xb/news/b47f30374ca4b310VgnVCM2000003356f70aRCRD.htm (Accessed March 25, 2013).
9. Rare Diseases and Orphan Products: Accelerating Research and Development. The National Academies Press, 2011.
10. Mehta, A.; Clarke, J.T.; Giugliani, R.; Elliott, P.; Linhart, A.; Beck, M.; Sunder-Plassmann, G. Natural course of Fabry disease: changing pattern of causes of death in FOS Fabry Outcome Survey. J. Med. Genet., 2009, 46, (8), 548-552.
11. Yanjanin, N.M.; Velez, J.I.; Gropman, A.; King, K.; Bianconi, S.E.; Conley, S.K.; Brewer, C.C.; Solomon, B.; Pavan, W.J.; Arcos-Burgos, M.; Patterson, M.C.; Porter, F.D. Linear clinical progression, independent of age of onset, in Niemann-Pick disease, type C. Am. J. Med. Genet B Neuropsychiatr Genet, 2010, 153B (1), 132-140.
12. Kishnani, P.S.; Hwu, W.-L.; Mandel, H.; Nicolino, M.; Yong, F.; Corzo, D. A retrospective, multinational, multicenter study on the natural history of infantile-onset Pompe disease. J. Pediat., 2006, 148(5), 671-676+e672.
13. Porter, F.D.; Scherrer, D.E.; Lanier, M.H.; Langmade, S.J.; Molugu, V.; Gale, S.E.; Olzeski, D.; Sidhu, R.; Dietzen, D.J.; Fu, R.; Wassif, C.A.; Yanjanin, N.M.; Marso, S.P.; House, J.; Vite, C.; Schaffer, J.E.; Ory, D.S. Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease. Sci. Transl. Med., 2010, 2 (56), 56ra81.
14. Cluzeau, C.V.; Watkins-Chow, D.E.; Fu, R.; Borate, B.; Yanjanin, N.; Dail, M.K.; Davidson, C.D.; Walkley, S.U.; Ory, D.S.; Wassif, C.A.; Pavan, W.J.; Porter, F.D. Microarray expression analysis and identification of serum biomarkers for Niemann-Pick disease, type C1. Hum. Mol. Genet, 2012, 21(16), 3632-3646.
15. Kaitin, K.I. Translational Research and the Evolving Landscape for Biomedical Innovation. J. Investi. Med., 2012, 60 (7), 995-998 910.231/JIM.990b013e318268694f.
16. Therapeutics for Rare and Neglected Diseases. http://www.ncats.nih.gov/research/rare-diseases/trnd/trnd.html (Accessed April 1, 2013).
17. Ory, D.S. Niemann-Pick type C: a disorder of cellular cholesterol trafficking. Biochim. Biophys. Acta., 2000, 1529 (1-3), 331-339.
18. Vanier, M.T. Niemann-Pick disease type C. Orphanet J. Rare Dis., 2010, 5, 16.
19. Vanier, M.T.; Millat, G. Niemann-Pick disease type C. Clin.Genet., 2003, 64(4), 269-281.
20. Sevin, M.; Lesca, G.; Baumann, N.; Millat, G.; Lyon-Caen, O.; Vanier, M.T.; Sedel, F. The adult form of Niemann-Pick disease type C. Brain, 2007, 130(Pt 1), 120-133.
21. European Medicine Agency Summary for Authorization of Zavasca (Miglustat). http://www.emea.europa.eu/docs/en_GB/document_library/EPARSummary_for_the_public/human/000435/WC500046724.pdf (Accessed April 13, 2013).
22. Patterson, M.C.; Hendriksz, C.J.; Walterfang, M.; Sedel, F.; Vanier, M.T.; Wijburg, F. Recommendations for the diagnosis and management of Niemann-Pick disease type C: an update. Mol. Genet Metab., 2012, 106(3), 330-344.
23. Patterson, M.C.; Vecchio, D.; Jacklin, E.; Abel, L.; ChadhaBoreham, H.; Luzy, C.; Giorgino, R.; Wraith, J.E. Long-term miglustat therapy in children with Niemann-Pick disease type C. J. Child Neurol., 2010, 25(3), 300-305.
24. Wraith, J.E.; Vecchio, D.; Jacklin, E.; Abel, L.; Chadha-Boreham, H.; Luzy, C.; Giorgino, R.; Patterson, M.C. Miglustat in adult and juvenile patients with Niemann-Pick disease type C: long-term data from a clinical trial. Mol. Genet Metab., 2010, 99(4), 351-357.
25. Davidson, C.D.; Ali, N.F.; Micsenyi, M.C.; Stephney, G.; Renault, S.; Dobrenis, K.; Ory, D.S.; Vanier, M.T.; Walkley, S.U. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One, 2009, 4 (9), e6951.
26. Zervas, M.; Somers, K.L.; Thrall, M.A.; Walkley, S.U. Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol., 2001, 11(16), 1283-1287.
27. FDA Rare Disease Program. http://www.fda.gov/AboutFDA/CentersOffices/OfficeofMedicalProductsandTobacco/CDER/ucm221248.htm (Accessed April 1, 2013).
28. Office of Orphan Products Development. http://www.fda.gov/ForIndustry/DevelopingProductsforRareDiseasesConditions/HowtoapplyforOrphanProductDesignation/default.htm(Accessed April 1, 2013).
29. Addi and Cassi Fund. http://addiandcassi.com/(Accessed April 1, 2013).
30. Ara Parseghian Medical Research Foundation http://www.parseghian.org/aboutus.html (Accessed April 1, 2013).
31. National Niemann-Pick Disease Foundation. http://www.nnpdf.org/(Accessed April 1, 2013).
32. International Niemann-Pick Disease Alliance http://inpda.org/(Accessed April 1, 2013).
33. Niemann-Pick Disease Group (UK). http://www.niemannpick.org.uk/(Accessed April 1, 2013).
34. Dana's Angel's Research Trust. http://danasangels.org/(Accessed April 1, 2013).
35. Hide & Seek Foundation for Lysosomal Disease Research. http://hideandseek.org/FindTheCure.html (Accessed April 1, 2013).
36. Loftsson, T.; Jarho, P.; Masson, M.; Jarvinen, T. Cyclodextrins in drug delivery. Expert Opin. Drug Deliv., 2005, 2 (2), 335-351.
37. Loftsson, T.; Vogensen, S.B.; Brewster, M.E.; Konradsdottir, F. Effects of cyclodextrins on drug delivery through biological membranes. J. Pharm. Sci., 2007, 96 (10), 2532-2546.
38. Kurkov, S.V.; Loftsson, T. Cyclodextrins. Int.J. Pharm., 2012.
39. Davis, M.E.; Brewster, M.E. Cyclodextrin-based pharmaceutics: past, present and future. Nat.Rev. Drug Discov., 2004, 3 (12), 1023-1035.
40. GRAS Notice Inventory. http://www.accessdata.fda.gov/scripts/fcn/fcnNavigation.cfm?filter =cyclodextrin&sortColumn=&rpt=grasListing (Accessed April 1, 2013).
41. FDA List of Inactive Pharmaceutical Ingredients http://www.accessdata.fda.gov/scripts/cder/iig/index.cfm(Accessed April 1, 2013).
42. Gould, S.; Scott, R.C. 2-Hydroxypropyl-beta-cyclodextrin (HPbeta-CD): a toxicology review. Food Chem. Toxicol., 2005, 43 (10), 1451-1459.
43. Stella, V.J.; He, Q. Cyclodextrins. Toxicol.Pathol., 2008, 36 (1), 30-42.
44. Brewster, M.E.; Estes, K.S.; Bodor, N. An Intravenous Toxicity Study of 2-Hydroxypropyl-Beta-Cyclodextrin, a Useful Drug Solubilizer, in Rats and Monkeys. Int.J.Pharm., 1990, 59(3), 231-243.
45. Loftsson, T.; Brewster, M.E. Pharmaceutical applications of cyclodextrins: basic science and product development. J.Pharm. Pharma., 2010, 62 (11), 1607-1621.
46. Brewster, M.E.; Loftsson, T. Cyclodextrins as pharmaccutical solubilizers. Adv.Drug Deliver. Rev., 2007, 59(7), 645-666.
47. Loftsson, T.; Brewster, M.E. Pharmaceutical applications of cyclodextrins.1. Drug solubilization and stabilization. J. Pharm. Sci., 1996, 85 (10), 1017-1025.
48. Rajewski, R.A.; Stella, V.J. Pharmaceutical applications of cyclodextrins. 2. In vivo drug delivery. J.Pharm. Sci., 1996, 85(11), 1142-1169.
49. Irie, T.; Uekama, K. Pharmaceutical applications of cyclodextrins. III. Toxicological issues and safety evaluation. J. Pharm. Sci., 1997, 86(2), 147-162.
50. Carstea, E.D.; Morris, J.A.; Coleman, K.G.; Loftus, S.K.; Zhang, D.; Cummings, C.; Gu, J.; Rosenfeld, M.A.; Pavan, W.J.; Krizman, D.B.; Nagle, J.; Polymeropoulos, M.H.; Sturley, S.L.; Ioannou, Y.A.; Higgins, M.E.; Comly, M.; Cooney, A.; Brown, A.; Kaneski, C.R.; Blanchette-Mackie, E.J.; Dwyer, N.K.; Neufeld, E.B.; Chang, T.Y.; Liscum, L.; Strauss, J.F. 3rd; Ohno, K.; Zeigler, M.; Carmi, R.; Sokol, J.; Markie, D.; O'Neill, R.R.; van Diggelen, O.P.; Elleder, M.; Patterson, M.C.; Brady, R.O.; Vanier, M.T.; Pentchev, P.G.; Tagle, D.A. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science, 1997, 277 (5323), 228-231.
51. Liu, S.M.; Cogny, A.; Kockx, M.; Dean, R.T.; Gaus, K.; Jessup, W.; Kritharides, L. Cyclodextrins differentially mobilize free and esterified cholesterol from primary human foam cell macrophages. J. Lipid Res., 2003, 44 (6), 1156-1166.
52. Kilsdonk, E.P.; Yancey, P.G.; Stoudt, G.W.; Bangerter, F.W.; Johnson, W.J.; Phillips, M.C.; Rothblat, G.H. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem., 1995, 270, (29), 17250-17256.
53. Camargo, F.; Erickson, R.P.; Garver, W.S.; Hossain, G.S.; Carbone, P.N.; Heidenreich, R.A.; Blanchard, J. Cyclodextrins in the treatment of a mouse model of Niemann-Pick C disease. Life Sci., 2001, 70(2), 131-142.
54. Griffin, L.D.; Gong, W.; Verot, L.; Mellon, S.H. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat. Med., 2004, 10(7), 704-711.
55. Liu, B.; Ramirez, C.M.; Miller, A.M.; Repa, J.J.; Turley, S.D.; Dietschy, J.M. Cyclodextrin overcomes the transport defect in nearly every organ of NPC1 mice leading to excretion of sequestered cholesterol as bile acid. J. Lipid Res., 2010, 51(5), 933-944.
56. Aqul, A.; Liu, B.; Ramirez, C.M.; Pieper, A.A.; Estill, S.J.; Burns, D.K.; Repa, J.J.; Turley, S.D.; Dietschy, J.M. Unesterified cholesterol accumulation in late endosomes/lysosomes causes neurodegeneration and is prevented by driving cholesterol export from this compartment. J. Neurosci., 2011, 31(25), 9404-9413.
57. Ramirez, C.M.; Liu, B.; Aqul, A.; Taylor, A.M.; Repa, J.J.; Turley, S.D.; Dietschy, J.M. Quantitative role of LAL, NPC2, and NPC1 in lysosomal cholesterol processing defined by genetic and pharmacological manipulations. J.Lipid Res., 2011, 52(4), 688-698.
58. Ramirez, C.M.; Liu, B.; Taylor, A.M.; Repa, J.J.; Burns, D.K.; Weinberg, A.G.; Turley, S.D.; Dietschy, J.M. Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr. Res., 2010, 68(4), 309-315.
59. Ward, S.; O'Donnell, P.; Fernandez, S.; Vite, C.H. 2hydroxypropyl-beta-cyclodextrin raises hearing threshold in normal cats and in cats with Niemann-Pick type C disease. Pediatr. Res., 2010, 68(1), 52-56.
60. Peake, K.B.; Vance, J.E. Normalization of cholesterol homeostasis by 2-hydroxypropyl-beta-cyclodextrin in neurons and glia from Niemann-Pick C1 (NPC1)-deficient mice. J. Biol. Chem., 2012, 287(12), 9290-9298.
61. Chen, F.W.; Li, C.; Ioannou, Y.A. Cyclodextrin induces calciumdependent lysosomal exocytosis. PLoS One, 2010, 5(11), e15054.
62. Jiang, X.; Sidhu, R.; Porter, F.D.; Yanjanin, N.M.; Speak, A.O.; te Vruchte, D.T.; Platt, F.M.; Fujiwara, H.; Scherrer, D.E.; Zhang, J.; Dietzen, D.J.; Schaffer, J.E.; Ory, D.S. A sensitive and specific LCMS/MS method for rapid diagnosis of Niemann-Pick C1 disease from human plasma. J. Lipid Res., 2011, 52 (7), 1435-1445.
63. Availability of Investigational Drugs for Compassionate Use. http://www.fda.gov/NewsEvents/Testimony/ucm115209.htm (Accessed April 1, 2013).
64. Physician Request for an Individual Patient IND under Expanded Access for Non-emergency or Emergency Use. http://www.fda.gov/Drugs/DevelopmentApprovalProcess/HowDrugsareDevelopedandApproved/ApprovalApplications/InvestigationalNewDrugINDApplication/ucm107434.htm (Accessed April 1, 2013).
65. Vol. 52 FR 19476, May 22, 1987, as amended at 57 FR 13248, Apr. 15, 1992.
66. Matsuo, M.; Togawa, M.; Hirabaru, K.; Mochinaga, S.; Narita, A.; Adachi, M.; Egashira, M.; Irie, T.; Ohno, K. Effects of cyclodextrin in two patients with Niemann-Pick Type C disease. Mol. Genet. Metab., 2013, 108 (1), 76-81.
67. Pontikis, C.C.; Davidson, C.D.; Walkley, S.U.; Platt, F.M.; Begley, D.J. Cyclodextrin alleviates neuronal storage of cholesterol in Niemann-Pick C disease without evidence of detectable bloodbrain barrier permeability. J.Inherit Metab. Dis., 2013, 36 (3), 491-498
68. Loftus, S.K.; Morris, J.A.; Carstea, E.D.; Gu, J.Z.; Cummings, C.; Brown, A.; Ellison, J.; Ohno, K.; Rosenfeld, M.A.; Tagle, D.A.; Pentchev, P.G.; Pavan, W.J. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science, 1997, 277 (53-23), 232-235.
69. Cystic Fibrosis Foundation Therapeutics. http://www.cff.org/research/CFFT/(Accessed April 1, 2013).
70. Leukemia and Lymphoma Society's Therapy Acceleration Program http://www.lls.org/researchershealthcareprofessionals/drugdevelopment/therapyacceleration/(Accessed April 1, 2013).
71. Mylein Research Foundation's Accelerated Research Collaboration Model. http://www.myelinrepair.org/research_model/(Accessed April 1, 2013).
72. Multiple Myeloma Research Consortium. http://themmrc.org/(Accessed April 1, 2013).
73. FDA (2009) Orphan Drug Act (as ammended). http://www.fda.gov/RegulatoryInformation/Legislation/FederalFoodDrugandCosmeticActFDCAct/SignificantAmendmentstotheFDC Act/OrphanDrugAct/default.htm (Accessed April 1, 2013).
74. Haffner, M.E.; Torrent-Farnell, J.; Maher, P.D. Does orphan drug legislation really answer the needs of patients? Lancet, 2008, 371 (96-29), 2041-2044.
75. Cote, T.; Kelkar, A.; Xu, K.; Braun, M.M.; Phillips, M.I. Orphan products: an emerging trend in drug approvals. Nat. Rev. Drug Discov., 2010, 9(1), 84.
76. Cote, T.R.; Xu, K.; Pariser, A.R. Accelerating orphan drug development. Nat. Rev. Drug Discov., 2010, 9 (12), 901-902.
77. Joppi, R.; Bertele, V.; Garattini, S. Orphan drugs, orphan diseases. The first decade of orphan drug legislation in the EU. Eur. J. Clin. Pharmacol., 2013, 69, (4), 1009-1024.
78. Thorat, C.; Xu, K.; Freeman, S.N.; Bonnel, R.A.; Joseph, F.; Phillips, M.I.; Imoisili, M.A. What the Orphan Drug Act has done lately for children with rare diseases: a 10-year analysis. Pediatrics, 2012, 129,(3), 516-521.
79. Orphan Product Designation FDA. http://www.fda.gov/ForIndustry/DevelopingProductsforRareDiseasesConditions/HowtoapplyforOrphanProductDesignation/default.htm (Accessed April 1, 2013).
80. Network for Excellence in Neuroscience Clinical Trials (NeuroNEXT). http://www.neuronext.org/(Accessed April 1, 2013).
81. Sasinowski, F.J. Quantum of Effectiveness Evidence in FDA's Approval of Orphan Drugs Cataloguing FDA's Flexibility in Regulating Therapies for Persons with Rare Disorders. Drug Inf. J., 2012, 46 (2), 238-263.
82. Food and Drug Administration Safety and Innovation Act of 2012 http://www.fda.gov/RegulatoryInformation/Legislation/FederalFoodDrugandCosmeticActFDCAct/SignificantAmendmentstotheFDC Act/FDASIA/default.htm (Accessed April 1, 2013).
83. Breakthrough Designation. http://www.fda.gov/RegulatoryInformation/Legislation/FederalFoodDrugandCosmeticActFDCAct/SignificantAmendmentstotheFDC Act/FDASIA/ucm329491.htm (Accessed March 25, 2013).
84. Valenza, M.; Rigamonti, D.; Goffredo, D.; Zuccato, C.; Fenu, S.; Jamot, L.; Strand, A.; Tarditi, A.; Woodman, B.; Racchi, M.; Mariotti, C.; Di Donato, S.; Corsini, A.; Bates, G.; Pruss, R.; Olson, J.M.; Sipione, S.; Tartari, M.; Cattaneo, E. Dysfunction of the cholesterol biosynthetic pathway in Huntington's disease. J. Neurosci., 2005, 25 (43), 9932-9939.
85. Yao, J.; Ho, D.; Calingasan, N.Y.; Pipalia, N.H.; Lin, M.T.; Beal, M.F. Neuroprotection by cyclodextrin in cell and mouse models of Alzheimer disease. J. Exp. Med.,2012, 209 (13), 2501-2513.
86. Dass, C.R.; Jessup, W. Apolipoprotein A-I, cyclodextrins and liposomes as potential drugs for the reversal of atherosclerosis. A review. J. Pharm. Pharmacol., 2000, 52(7), 731-761.