Encapsulated cell biodelivery of nerve growth factor to the basal forebrain in patients with Alzheimer's disease

Dementia and Geriatric Cognitive Disorders

Volumn 33, Issue 1, 2012, Pages 18-28

  Eriksdotter Jönhagen, Maria ^a   Linderoth, Bengt ^a   Lind, Göran ^a   Aladellie, Layth ^a   Almkvist, Ove ^a,c   Andreasen, Niels ^a   Blennow, Kaj ^d   Bogdanovic, Nenad ^a   Jelic, Vesna ^a   Kadir, Ahmadul ^a   Nordberg, Agneta ^a   Sundström, Erik ^a,b   Wahlund, Lars Olof ^a   Wall, Anders ^e   Wiberg, Maria ^a   Winblad, Bengt ^a   Seiger, Åke ^a,b   Almqvist, Per ^a,f   Wahlberg, Lars ^a,f  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b Stockholms Sjukhem   (Sweden)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e UPPSALA UNIVERSITY   (Sweden)

^f NsGene AS   (Denmark)

Author keywords

Alzheimer's disease; Basal forebrain; Encapsulated cell biodelivery; Nerve growth factor; Neurosurgery

Indexed keywords

CHOLINESTERASE INHIBITOR; GLUCOSE; NERVE GROWTH FACTOR; NICOTINIC RECEPTOR;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BACKACHE; BODY MASS; BRAIN BIOPSY; CELL ENCAPSULATION; COGNITION; COMPUTER ASSISTED TOMOGRAPHY; CONFUSION; CONTUSION; DELIRIUM; DEVICE REMOVAL; DEVICE SAFETY; DEVICES; DISEASE COURSE; DIZZINESS; DRUG DELIVERY SYSTEM; DRUG DOSE ESCALATION; DRUG INDUCED HEADACHE; DRUG SAFETY; DRUG TOLERABILITY; ELECTROENCEPHALOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW UP; FOREBRAIN; GENETIC TRANSFECTION; GLAUCOMA; GLUCOSE METABOLISM; HAIR LOSS; HEART ATRIUM FIBRILLATION; HEART FAILURE; HEMATURIA; HIP PAIN; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERGLYCEMIA; HYPERTENSION; HYPOKALEMIA; IMPLANTATION; MAJOR CLINICAL STUDY; MALE; MEMORY; MIGRAINE; MINI MENTAL STATE EXAMINATION; NAUSEA; NEUROANATOMY; NUCLEAR MAGNETIC RESONANCE IMAGING; OPEN STUDY; PARESTHESIA; PATIENT MONITORING; PHASE 1 CLINICAL TRIAL; PIGMENT EPITHELIUM; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PRURITUS; RECEPTOR BINDING; RHINOPHARYNGITIS; SIDE EFFECT; STOMATITIS; SUBDURAL HEMATOMA; THORAX PAIN; TREATMENT DURATION; URINARY TRACT INFECTION; URTICARIA; VISUAL ACUITY; VISUAL ANALOG SCALE; WHITE MATTER;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AUTOPSY; BIOPSY; CELL LINE; CEREBRAL CORTEX; COGNITION; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROENCEPHALOGRAPHY; FEASIBILITY STUDIES; FEMALE; HUMANS; INFUSION PUMPS, IMPLANTABLE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE GROWTH FACTORS; NEUROPSYCHOLOGICAL TESTS; NEUROSURGICAL PROCEDURES; NICOTINE; POSITRON-EMISSION TOMOGRAPHY; PROSENCEPHALON; RECEPTORS, NICOTINIC; TREATMENT OUTCOME;

EID: 84857477684     PISSN: 14208008     EISSN: 14219824     Source Type: Journal    
DOI: 10.1159/000336051     Document Type: Article

References (46)

1. Andersson C, Lindau M, Almkvist O, Engfeldt P, Johansson SE, Eriksdotter-Jonhagen M: Identifying patients at high and low risk of cognitive decline using RAVLT among middle-aged memory clinic out-patients. Dement Cogn Disord 2006;21:251-259.
2. Bartus RT: On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 2000;163:495-529.
3. Mesulam M: The cholinergic lesion of Alzheimer's disease: pivotal factor or sideshow? Learn Mem 2004;11:43-49.
4. Hefti F: Nerve growth factor (NGF) promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 1986;6:2155-2162.
5. Fischer W, Wictorin K, Björklund A, Williams LR, Varon S, Gage FH: Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 1987;329;65-68. (Pubitemid 17125895)
6. Conner JM, Franks KM, Titterness AK, Russell K, Merrill DA, Christie BR, Sejnowski TJ, Tuszynski MH: NGF is essential for hippocampal plasticity and learning. J Neurosci 2009;29:10883-10889.
7. Seiler M, Schwab ME: Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Res 1984;300:33-36.
8. Mufson EJ, Ikonomovich MD, Styren SD, Counts SE, Wuu J, Leurgans S, Bennett DA, Cochran EJ, DeKosky ST: Preservation of brain nerve growth factor in mild cognitive impairment and Alzheimer disease. Arch Neurol 2003;60:1143-1148. (Pubitemid 36975805)
9. Boissière F, Hunot S, Faucheux B, Hersh LB, Agid Y, Hirsch EC: Trk neurotrophin receptors in cholinergic neurons of patients with Alzheimer's disease. Dement Geriatr Cogn Disord 1997;8:1-8. (Pubitemid 27173511)
10. Williams B, Eriksdotter-Jonhagen M, Granholm L: Nerve growth factor in treatment and pathogenesis of Alzheimer's disease. Progr Neurobiol Aging 2006;80:114-128. (Pubitemid 44739167)
11. Mufson EJ, Counts S, Perez SE, Ginsberg SD: Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Exp Rev Neurother 2008;8:1703-1718.
12. Fahnestock M, Michalski B, Xu B, Coughlin MD: The precursor pro-nerve growth factor is the predominant form of nerve growth factor in the brain and is increased in Alzheimer's disease. Mol Cell Neurosci 2001;18:210-220. (Pubitemid 32846529)
13. Cuello AC, Bruno MA, Allard S, Leon W, Julita MF: Cholinergic involvement in Alzheimer's disease. A link with NGF maturation and degradation. J Mol Neurosci 2010;40:230-235.
14. Cattaneo A, Capsoni S, Paoletti F: Towards noninvasive nerve growth factor therapies for Alzheimer's disease. J Alzheimers Dis 2008;15:255-283.
15. Wilkinson D, Schindler R, Schwam E, Waldemar G, Jones RW, Gauthier S, Lopez OL, Cummings J, Xu Y, Feldman HH: Effectiveness of donepezil in reducing clinical worsening in patients with mild-to-moderate Alzheimer's disease. Dement Geriatr Cogn Disord 2009;28:244-251.
16. Winblad B, Jones RW, Wirth Y, Stöffler A, Möbius HJ: Memantine in moderate to severe Alzheimer's disease: a meta-analysis of randomised clinical trials. Dement Geriatr Cogn Disord 2007;24:20-27. (Pubitemid 46985287)
17. 11C-nicotine binding, blood flow, EEG and verbal episodic memory in an Alzhei mer patient (case report). J Neural Transm 1992;4:79-95.
18. Eriksdotter-Jönhagen M, Nordberg A, Amberla K, Bäckman L, Ebendal T, Meyerson B, Olson L, Seiger Å, Shigeta M, Theodorsson E, Viitanen M, Winblad B, Wahlund L-O: Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer's disease. Dement Geriatr Cogn Disord 1998;9:246-257. (Pubitemid 28377225)
19. Hao J-X, Ebendal T, Xu X-J, Wiesenfeld-Hallin Z, Eriksdotter Jönhagen M: Intracerebroventricular infusion of nerve growth factor induces pain-like responses in rats. Neurosci Lett 2000;286:208-212. (Pubitemid 30314646)
20. Capsoni S, Covaceuszach S, Ugolini G, Spirito F, Vignone D, Stefanini B, Amato G, Cattaneo A: Delivery of NGF to the brain: intranasal versus ocular administration in anti-NGF transgenic mice. J Alzheimers Dis 2009;16:371-388.
21. Capsoni S, Covaceuszach S, Marinelli S, Ceci M, Bernardo A, Minghetti L, Ugolini G, Pavone F, Cattaneo A: Taking pain out of NGF: a 'painless' NGF mutant, linked to hereditary sensory autonomic neuropathy type V, with full neurotrophic activity. PLoS One 2011;6:e17321.
22. Nagahara AH, Bernot T, Moseanko R, Brignolo L, Blesch A, Conner JM, Ramirez A, Gasmi M, Tuszynski MH: Long-term reversal of cholinergic neuronal decline in aged non-human primates by lentiviral NGF gene delivery. Exp Neurol 2009;215:153-159.
23. Tuszynski MH, Thal L, Pay M, Salmon DP, Sang UH, Bakay R, Patel P, Blesch A, Vahlsing HL, Ho G, Tong G, Potkin SG, Fllon J, Hansen L, Mufson EJ, Kordower JH, Gall C, Conner JA: Phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer's disease. Nat Med 2005;11:551-555. (Pubitemid 40691288)
24. Lindvall O, Wahlberg L: Encapsulated cell biodelivery of GDNF: a novel clinical strategy for neuroprotection and neuroregeneration in Parkinson's disease? Exp Neurol 2008;209:82-88.
25. Winn SR, Hammang JP, Emerich DF, Lee A, Palmiter R, Baetge EE: Polymer-encapsulated cells genetically modified to secrete human NGF promote the survival of axotomized septal cholinergic neurons. Proc Natl Acad Sci USA 1994;91:2324-2328. (Pubitemid 24092096)
26. Fjord-Larsen L, Kusk P, Tornøe J, Juliusson J, Torp M, Bjarkam CR, Nielsen MS, Handberg A, Sørensen JCH, Wahlberg LU: Long-term delivery of nerve growth factor by encapsulated cell biodelivery in the Göttingen minipig basal forebrain. Mol Ther 2010;18:2164-2172.
27. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM: Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 1984;34:939-944.
28. Folstein MF, Folstein SE, McHugh PR: 'Mini-mental state'. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.
29. Wahlberg LU, Lind G, Almqvist PM, Kusk G, Tornøe P, Juliusson, B, SödermanM, Selldén E, Seiger Å, Eriksdotter-Jönhagen M, Linderoth B: Encapsulated cell biodelivery - a functional neurosurgery technology platform applied for targeted delivery of NGF in Alzheimer's disease. J Neurosurg, in press.
30. Mohs RC, Knopman D, Petersen RC, Ferris SH, Ernesto C, Grundman M, Sano M, Bieliauskas L, Geldmacher D, Clark C, Thal LJ: Development of cognitive instruments for use in clinical trials of antidementia drugs: additions to the Alzheimer's Disease Assessment Scale that broaden its scope. The Alzheimer's Disease Cooperative Study. Alzheimer Dis Assoc Disord 1997;11:S13-S21.
31. 11C]Nicotine binding assessed by PET: a dual tracer model evaluated in the Rhesus monkey brain. Alzheimer Dis Assoc Disord 1998;12:238-246.
32. 11C-nicotine binding in normal and Alzheimer brains - in vivo assessment using positron emission tomography. Alzheimer Dis Assoc Disord 1995;9:21-27.
33. Patlak CS, Blasberg RG, Fenstermacher JD: Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J Cereb Blood Flow Metab 1983;3:1-7. (Pubitemid 13129630)
34. Jelic V, Johansson SE, Almkvist O, Shigeta M, Julin P, Nordberg A, Winblad B, Wahlund LO: Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer's disease. Neurobiol Aging 2000;21:533-540. (Pubitemid 30621491)
35. 1-42, tau and phosphorylated tau (Thr181) in cerebrospinal fluid by the xMAP technology. Clin Chem 2005;51:336-345.
36. Rosengren LE, Karlsson JE, Karlsson JO: Patients with amyotrophic lateral sclerosis and other neurodegenerative diseases have increased levels of neurofilament protein in CSF. J Neurochem 1996;67:2013-2018. (Pubitemid 26349676)
37. Rosengren LE, Wikkelso C, Hagberg L: A sensitive ELISA for glial fibrillary acidic protein: application in CSF of adults. J Neurosci Methods 1994;51:197-204. (Pubitemid 24110093)
38. Ryu Sl, Romanelli P, Heit G: Asymptomatic transient MRI signal changes after unilateral deep brain stimulation electrode implantation for movement disorder. Stereotact Funct Neurosurg 2004;82:65-69. (Pubitemid 39140450)
39. Winblad B, Engedal K, Soininen H, Verhey F, Waldemar G, Wimo A, Wetterholm AL, Zhang R, Haglund A, Subbiah P: A 1-year, randomized placebo-controlled study of donepezil in patients with mild to moderate AD. Neurology 2001;57:489-495. (Pubitemid 32757598)
40. Kadir A, Darreh-Shori T, Almkvist O, Långström B, Nordberg A: Changes in brain 11C-nicotine binding sites in patients with mild Alzheimer's disease following rivastigmine treatment as assessed by PET. Psychopharmacol (Berl) 2007;191:1005-1014. (Pubitemid 46399149)
41. Wallin ÅK, Andreasen N, Eriksson S, Båtsman S, Näsman B, Ekdahl A, Kilander L, Grut M, Rydén M, Wallin A, Jonsson M, Olofsson H, Wattmo C, Eriksdotter-Jonhagen M, Minthon L: Donepezil in Alzheimer's disease: what to expect after 3 years of treatment in a routine clinical setting. Dement Cogn Disord 2007;23:150-160. (Pubitemid 46333782)
42. Eriksdotter-Jönhagen M: Nerve growth factor treatment in dementia. Alzheimer Dis Assoc Disord 2000;14:S31-S38.
43. Tuszynski MH: Growth factor gene therapy for neurodegenerative disorders. Lancet Neurol 2002;1:51-57.
44. Fjord-Larsen L, Kusk P, Emerich DF, Thanos C, Torp M, Bintz B, Tornöe J, Johnsen AH, Wahlberg LU: Increased encapsulated cell biodelivery of nerve growth factor in the brain by transposon-mediated gene transfer. Gene Ther DOI: 10.1038/gt.2011.178.
45. Zetterberg H, Hietala MA, Jonsson M, Andreasen N, Styrud E, Karlsson I, Edman Å, Popa C, Rasulzada A, Wahlund LO, Mehta PD, Rosengren L, Blennow K, Wallin A: Neurochemical aftermath of amateur boxing. Arch Neurol 2006;63:1277-1280. (Pubitemid 44379829)
46. Szaro BG, Strong MJ: Post-transcriptional control of neurofilaments: new roles in development, regeneration and neurodegenerative disease. Trends Neurosci 2010;33:27-37.