Initial gene vector dosing for studying symptomatology of amyotrophic lateral sclerosis in non-human primates

Journal of Medical Primatology

Volumn 44, Issue 2, 2015, Pages 66-75

  Jackson, Kasey L ^a   Dayton, Robert D ^a   Fisher Perkins, Jeanne M ^b   Didier, Peter J ^b   Baker, Kate C ^b   Weimer, Maria ^c   Gutierrez, Amparo ^c   Cain, Cooper D ^a   Michael Mathis, J ^d   Gitcho, Michael A ^e   Bunnell, Bruce A ^b,f   Klein, Ronald L ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^e DELAWARE STATE UNIVERSITY   (United States)

^f TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adeno associated virus; Amyotrophic lateral sclerosis; Frontotemporal lobar degeneration; Gene therapy; Gene transfer; TDP 43

Indexed keywords

GREEN FLUORESCENT PROTEIN; MESSENGER RNA; TAR DNA BINDING PROTEIN; DNA BINDING PROTEIN; GREEN FLUORESCENT PROTEIN, AEQUOREA VICTORIA; PROTEIN TDP-43; RECOMBINANT PROTEIN;

ADENO ASSOCIATED VIRUS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BODY WEIGHT; BRAIN WEIGHT; COGNITION; CONTROLLED STUDY; ELECTROMYOGRAM; ELECTROMYOGRAPHY; FEMALE; GENE TARGETING; GENE TRANSFER; GENE VECTOR; HEART WEIGHT; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PURKINJE CELL; RHESUS MONKEY; STABLE EXPRESSION; SYMPTOMATOLOGY; TISSUE PREPARATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE THERAPY; GENETICS; HUMAN; INTRAVENOUS DRUG ADMINISTRATION; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES;

ADENO-ASSOCIATED VIRUS; MACACA MULATTA; MUS; PRIMATES; RODENTIA;

ADMINISTRATION, INTRAVENOUS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ELECTROMYOGRAPHY; GENETIC THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; MACACA MULATTA; MOTOR ACTIVITY; RECOMBINANT PROTEINS;

EID: 84924386870     PISSN: 00472565     EISSN: 16000684     Source Type: Journal    
DOI: 10.1111/jmp.12162     Document Type: Article

References (36)

1. Watson C, Paxinos G, Kayalioglu G: Chapter 7: Localization of motoneurons in the spinal cord. In: The Spinal Cord: A Christopher and Dana Reeve Foundation Text and Atlas. 1st ed. McHanwell S, Watson C (eds). Sydney: Academic Press, 2009; 94-114.
2. Chen-Plotkin AS, Lee VM, Trojanowski JQ: TAR DNA-binding protein 43 in neurodegenerative disease. Nat Rev Neurol 2010; 6:211-20.
3. Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, Burrell JR, Zoing MC: Amyotrophic lateral sclerosis. Lancet 2011; 377:942-55.
4. Mackenzie IR, Bigio EH, Ince PG, Geser F, Neumann M, Cairns NJ, Kwong LK, Forman MS, Ravits J, Stewart H, Eisen A, McClusky L, Kretzschmar HA, Monoranu CM, Highley JR, Kirby J, Siddique T, Shaw PJ, Lee VM, Trojanowski JQ: Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol 2007; 61:427-34.
5. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM: Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314:130-3.
6. Baralle M, Buratti E, Baralle FE: The role of TDP-43 in the pathogenesis of ALS and FTLD. Biochem Soc Trans 2013; 41:1536-40.
7. Polymenidou M, Lagier-Tourenne C, Hutt KR, Huelga SC, Moran J, Liang TY, Ling SC, Sun E, Wancewicz E, Mazur C, Kordasiewicz H, Sedaghat Y, Donohue JP, Shiue L, Bennett CF, Yeo GW, Cleveland DW: Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 2011; 14:459-68.
8. Dayton RD, Wang DB, Klein RL: The advent of AAV9 expands applications for brain and spinal cord gene delivery. Expert Opin Biol Ther 2012; 12:757-66.
9. Wang DB, Gitcho MA, Kraemer BC, Klein RL: Genetic strategies to study TDP-43 in rodents and to develop preclinical therapeutics for amyotrophic lateral sclerosis. Eur J Neurosci 2011; 34:1179-88.
10. Tatom JB, Wang DB, Dayton RD, Skalli O, Hutton ML, Dickson DW, Klein RL: Mimicking aspects of frontotemporal lobar degeneration and Lou Gehrig's disease in rats via TDP-43 overexpression. Mol Ther 2009; 17:607-13.
11. Uchida A, Sasaguri H, Kimura N, Tajiri M, Ohkubo T, Ono F, Sakaue F, Kanai K, Hirai T, Sano T, Shibuya K, Kobayashi M, Yamamoto M, Yokota S, Kubodera T, Tomori M, Sakaki K, Enomoto M, Hirai Y, Kumagai J, Yasutomi Y, Mochizuki H, Kuwabara S, Uchihara T, Mizusawa H, Yokota T: Non-human primate model of amyotrophic lateral sclerosis with cytoplasmic mislocalization of TDP-43. Brain 2012; 135:833-46.
12. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK: Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 2009; 27:59-65.
13. Wang DB, Dayton RD, Henning PP, Cain CD, Zhao LR, Schrott LM, Orchard EA, Knight DS, Klein RL: Expansive gene transfer to the rat CNS and amyotrophic lateral sclerosis relevant sequelae when TDP-43 is overexpressed. Mol Ther 2010; 18:2064-74.
14. Dayton RD, Gitcho MA, Orchard EA, Wilson JD, Wang DB, Cain CD, Johnson JA, Zhang YJ, Petrucelli L, Mathis JM, Klein RL: Selective forelimb impairment in rats expressing a pathological TDP-43 25 kDa C-terminal fragment to mimic amyotrophic lateral sclerosis. Mol Ther 2013; 21:1324-34.
15. Bevan AK, Duque S, Foust KD, Morales PR, Braun L, Schmelzer L, Chan CM, McCrate M, Chicoine LG, Coley BD, Porensky PN, Kolb SJ, Mendell JR, Burghes AH, Kaspar BK: Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol Ther 2011; 19:1971-80.
16. Foust KD, Wang X, McGovern VL, Braun L, Bevan AK, Haidet AM, Le TT, Morales PR, Rich MM, Burghes AH, Kaspar BK: Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol 2010; 28:271-4.
17. Gray SJ, Nagabhushan Kalburgi S, McCown TJ, Samulski RJ: Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecal AAV administration in non-human primates. Gene Ther 2013; 20:450-9.
18. Mattar CN, Waddington SN, Biswas A, Johana N, Ng XW, Fisk NM, Tan LG, Rahim AA, Buckley SM, Tan MH, Lu J, Choolani M, Chan JK: Systemic delivery of scAAV9 in fetal macaques facilitates neuronal transduction of the central and peripheral nervous systems. Gene Ther 2013; 20:69-83.
19. Samaranch L, Salegio EA, San Sebastian W, Kells AP, Foust KD, Bringas JR, Lamarre C, Forsayeth J, Kaspar BK, Bankiewicz KS: Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum Gene Ther 2012; 23:382-9.
20. National Research Council, Institute of Laboratory Animal Resources: Guide for the Care and Use of Laboratory Animals. Washington: National Academy Press, 1996.
21. United States Department of Agriculture: Final rules: code of federal regulations, title 9, part 3. Fed Regist 1991; 55:6426-505.
22. Klein RL, Hamby ME, Hirko AC, Wang S, Hughes JA, King MA, Meyer EM: Dose and promoter effects of adeno-associated viral vector for green fluorescent protein expression in the rat brain. Exp Neurol 2002; 176:66-74.
23. Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP: AAV 8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol Ther 2008; 16:89-96.
24. Gao G, Vandenberghe LH, Alvira MR, Lu Y, Calcedo R, Zhou X, Wilson JM: Clades of Adeno-associated viruses are widely disseminated in human tissues. J Virol 2004; 78:6381-8.
25. Bayley N: Bayley Scales of Infant Development: Birth to Two Years. New York: The Psychological Corporation, 1969.
26. Champoux M, DiGregorio G, Schneider ML, Suomi SJ: Inanimate environmental enrichment for group-housed rhesus macaque infants. Am J Primatol 1990; 22:61-7.
27. Isakova IA, Baker K, DuTreil M, Dufour J, Gaupp D, Phinney DG: Age and dose-related effects on MSC engraftment levels and anatomical distribution in the CNS of non-human primates: identification of novel MSC subpopulations that respond to guidance cues in brain. Stem Cells 2007; 25:3261-70.
28. Borda JT, Alvarez X, Mohan M, Ratterree MS, Phillippi-Falkenstein K, Lackner AA, Bunnell BA: Clinical and immunopathologic alterations in rhesus macaques affected with Globoid Cell Leukodystrophy. Am J Pathol 2008; 172:98-111.
29. Gomez-Mancilla B, Boucher R, Gagnon C, Di Paolo T, Markstein R, Bédard PJ: Effect of adding the D1 agonist CY 208-243 to chronic bromocriptine treatment. I: evaluation of motor parameters in relation to striatal catecholamine content and dopamine receptors. Mov Disord 1993; 8:144-50.
30. Katirji B: Chapter 2: Routine clinical electromyography. In: Electromyography in Clinical Practice. 2nd ed. United States of America: Mosby Elsevier; 2007; 29-31.
31. England JD, Bohm RP Jr, Roberts ED, Phillip MT: Mononeuropathy multiplex in rhesus monkeys with chronic lyme disease. Ann Neurol 1997; 41:375-84.
32. Fecto F, Siddique T: UBQLN2/P62 cellular recycling pathways in amyotrophic lateral sclerosis and frontotemporal dementia. Muscle Nerve 2012; 45:157-62.
33. Gray SJ, Matagne V, Bachaboina L, Yadav S, Ojeda SR, Samulski RJ: Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 2012; 19:1058-69.
34. McCarty DM, Monahan PE, Samulski RJ: Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 2001; 8:1248-54.
35. Federici T, Taub JS, Baum GR, Gray SJ, Grieger JC, Matthews KA, Handy CR, Passini MA, Samulski RJ, Boulis NM: Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs. Gene Ther 2012; 19:852-9.
36. Wang H, Yang B, Qiu L, Yang C, Kramer J, Su Q, Guo Y, Brown RH Jr, Gao G, Xu Z: Widespread spinal cord transduction by intrathecal injection of rAAV delivers efficacious RNAi therapy for amyotrophic lateral sclerosis. Hum Mol Genet 2014; 23:668-81.