Abstract
Numerous neuromuscular and non-neuromuscular diseases are amenable to gene therapy. Rigorously designed and carefully conducted preclinical studies are essential to translate these muscle gene therapies to human patients. Many general guidelines have been published in recent years on how to enhance reproducibility and improve predictive value of preclinical studies. These are excellent guidelines to follow in preclinical gene therapy studies. However, they are not tailed specifically for muscle gene therapy. In this chapter, I discuss considerations in the design of a preclinical neuromuscular disease gene therapy study based on our experience in the preclinical development of adeno-associated virus (AAV) micro-dystrophin gene therapy. I also discuss adapting the design of phase III clinical trials to animal studies to improve their reproducibility. This chapter is not intended to be all-inclusive and to cover all possible scenarios. Due to the complexity of the candidate diseases that can be treated by muscle gene therapy, it is critical to consider disease-specific issues in the design of each preclinical muscle gene therapy study.
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References
Stroes ES, Nierman MC, Meulenberg JJ, Franssen R, Twisk J, Henny CP, Maas MM, Zwinderman AH, Ross C, Aronica E, High KA, Levi MM, Hayden MR, Kastelein JJ, Kuivenhoven JA (2008) Intramuscular administration of AAV1-lipoprotein lipase S447X lowers triglycerides in lipoprotein lipase-deficient patients. Arterioscler Thromb Vasc Biol 28(12):2303–2304. https://doi.org/10.1161/ATVBAHA.108.175620
Herzog RW, Mount JD, Arruda VR, High KA, Lothrop CD Jr (2001) Muscle-directed gene transfer and transient immune suppression result in sustained partial correction of canine hemophilia B caused by a null mutation. Mol Ther 4(3):192–200
Manno CS, Chew AJ, Hutchison S, Larson PJ, Herzog RW, Arruda VR, Tai SJ, Ragni MV, Thompson A, Ozelo M, Couto LB, Leonard DG, Johnson FA, McClelland A, Scallan C, Skarsgard E, Flake AW, Kay MA, High KA, Glader B (2003) AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101(8):2963–2972
Flotte TR, Trapnell BC, Humphries M, Carey B, Calcedo R, Rouhani F, Campbell-Thompson M, Yachnis AT, Sandhaus RA, McElvaney NG, Mueller C, Messina LM, Wilson JM, Brantly M, Knop DR, Ye GJ, Chulay JD (2011) Phase 2 clinical trial of a recombinant Adeno-associated virus vector expressing alpha 1 antitrypsin: interim results. Hum Gene Ther 22(10):1239–1247. https://doi.org/10.1089/hum.2011.053
Duan D (2018) Micro-dystrophin gene therapy goes systemic in Duchenne muscular dystrophy patients. Hum Gene Ther 29(7):733–736. https://doi.org/10.1089/hum.2018.012
Mendell JR, Sahenk Z, Malik V, Gomez AM, Flanigan KM, Lowes LP, NA L, Berry K, Meadows E, Lewis S, Braun L, Shontz K, Rouhana M, Clark KR, Rosales XQ, Al-Zaidy S, Govoni A, Rodino-Klapac LR, Hogan MJ, Kaspar BK (2015) A phase I/IIa follistatin gene therapy trial for Becker muscular dystrophy. Mol Ther 23(1):192–201. https://doi.org/10.1038/mt.2014.200
Kunkel LM (2005) 2004 William Allan award address. Cloning of the DMD gene. Am J Hum Genet 76(2):205–214
Gilbert R, Nalbantoglu J, Petrof BJ, Ebihara S, Guibinga GH, Tinsley JM, Kamen A, Massie B, Davies KE, Karpati G (1999) Adenovirus-mediated utrophin gene transfer mitigates the dystrophic phenotype of mdx mouse muscles. Hum Gene Ther 10(8):1299–1310
Mendell JR, Rodino-Klapac LR, Rosales-Quintero X, Kota J, Coley BD, Galloway G, Craenen JM, Lewis S, Malik V, Shilling C, Byrne BJ, Conlon T, Campbell KJ, Bremer WG, Viollet L, Walker CM, Sahenk Z, Clark KR (2009) Limb-girdle muscular dystrophy type 2D gene therapy restores alpha-sarcoglycan and associated proteins. Ann Neurol 66(3):290–297. https://doi.org/10.1002/ana.21732
Duan D (2018) Systemic AAV micro-dystrophin gene therapy for Duchenne muscular dystrophy. Mol Ther 26(10):2337–2356. https://doi.org/10.1016/j.ymthe.2018.07.011.
Liu J, Wallace LM, Garwick-Coppens SE, Sloboda DD, Davis CS, Hakim CH, Hauser MA, Brooks SV, Mendell JR, Harper SQ (2014) RNAi-mediated gene silencing of mutant myotilin improves myopathy in LGMD1A mice. Mol Ther Nucleic Acids 3:e160. https://doi.org/10.1038/mtna.2014.13
Zhang Y, Long C, Bassel-Duby R, Olson EN (2018) Myoediting: toward prevention of muscular dystrophy by therapeutic genome editing. Physiol Rev 98(3):1205–1240. https://doi.org/10.1152/physrev.00046.2017
Nelson CE, Robinson-Hamm JN, Gersbach CA (2017) Genome engineering: a new approach to gene therapy for neuromuscular disorders. Nat Rev Neurol 13(11):647–661. https://doi.org/10.1038/nrneurol.2017.126
Berger A, Maire S, Gaillard MC, Sahel JA, Hantraye P, Bemelmans AP (2016) mRNA trans-splicing in gene therapy for genetic diseases. Wiley Interdiscip Rev RNA 7(4):487–498. https://doi.org/10.1002/wrna.1347
Spitali P, Aartsma-Rus A (2012) Splice modulating therapies for human disease. Cell 148(6):1085–1088. https://doi.org/10.1016/j.cell.2012.02.014. S0092-8674(12)00214-0 [pii]
Vo AH, McNally EM (2015) Modifier genes and their effect on Duchenne muscular dystrophy. Curr Opin Neurol 28(5):528–534. https://doi.org/10.1097/WCO.0000000000000240
Goonasekera SA, Lam CK, Millay DP, Sargent MA, Hajjar RJ, Kranias EG, Molkentin JD (2011) Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. J Clin Investig 121(3):1044–1052. https://doi.org/10.1172/JCI43844. 43844 [pii]
Voit A, Patel V, Pachon R, Shah V, Bakhutma M, Kohlbrenner E, McArdle JJ, Dell’Italia LJ, Mendell JR, Xie LH, Hajjar RJ, Duan D, Fraidenraich D, Babu GJ (2017) Reducing sarcolipin expression mitigates Duchenne muscular dystrophy and associated cardiomyopathy in mice. Nat Commun 8(1):1068. https://doi.org/10.1038/s41467-017-01146-7
Shin J-H, Bostick B, Yue Y, Hajjar R, Duan D (2011) SERCA2a gene transfer improves electrocardiographic performance in aged mdx mice. J Transl Med 9:132. https://doi.org/10.1186/1479-5876-9-132. 1479-5876-9-132 [pii]
Wang D, Zhong L, Nahid MA, Gao G (2014) The potential of adeno-associated viral vectors for gene delivery to muscle tissue. Expert Opin Drug Deliv 11(3):345–364. https://doi.org/10.1517/17425247.2014.871258
Duan D (2016) Systemic delivery of adeno-associated viral vectors. Curr Opin Virol 21:16–25. https://doi.org/10.1016/j.coviro.2016.07.006
Mendell JR, Al-Zaidy S, Shell R, Arnold WD, Rodino-Klapac LR, Prior TW, Lowes L, Alfano L, Berry K, Church K, Kissel JT, Nagendran S, L’Italien J, Sproule DM, Wells C, Cardenas JA, Heitzer MD, Kaspar A, Corcoran S, Braun L, Likhite S, Miranda C, Meyer K, Foust KD, Burghes AHM, Kaspar BK (2017) Single-dose gene-replacement therapy for spinal muscular atrophy. N Engl J Med 377(18):1713–1722. https://doi.org/10.1056/NEJMoa1706198
Malerba A, Klein P, Bachtarzi H, Jarmin SA, Cordova G, Ferry A, Strings V, Espinoza MP, Mamchaoui K, Blumen SC, St Guily JL, Mouly V, Graham M, Butler-Browne G, Suhy DA, Trollet C, Dickson G (2017) PABPN1 gene therapy for oculopharyngeal muscular dystrophy. Nat Commun 8:14848. https://doi.org/10.1038/ncomms14848
FDA (2013) Guidance for industry: preclinical assessment of investigational cellular and gene therapy products. https://www.federalregister.gov/documents/2013/11/25/2013-28173/guidance-for-industry-preclinical-assessment-of-investigational-cellular-and-gene-therapy-products
Lima BS, Videira MA (2018) Toxicology and biodistribution: the clinical value of animal biodistribution studies. Mol Ther-Meth Clin Dev 8:183–197. https://doi.org/10.1016/j.omtm.2018.01.003
Mendell JR, Lloyd-Puryear M (2013) Report of MDA muscle disease symposium on newborn screening for Duchenne muscular dystrophy. Muscle Nerve 48(1):21–26. https://doi.org/10.1002/mus.23810
Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244(4912):1578–1580
Cooper BJ, Winand NJ, Stedman H, Valentine BA, Hoffman EP, Kunkel LM, Scott MO, Fischbeck KH, Kornegay JN, Avery RJ et al (1988) The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature 334(6178):154–156
McGreevy JW, Hakim CH, McIntosh MA, Duan D (2015) Animal models of Duchenne muscular dystrophy: from basic mechanisms to gene therapy. Dis Model Mech 8(3):195–213. https://doi.org/10.1242/dmm.018424
Sui T, Lau YS, Liu D, Liu T, Xu L, Gao Y, Lai L, Li Z, Han R (2018) A novel rabbit model of Duchenne muscular dystrophy generated by CRISPR/Cas9. Dis Model Mech 11(6):dmm032201. https://doi.org/10.1242/dmm.032201
Veltrop M, van Vliet L, Hulsker M, Claassens J, Brouwers C, Breukel C, van der Kaa J, Linssen MM, den Dunnen JT, Verbeek S, Aartsma-Rus A, van Putten M (2018) A dystrophic Duchenne mouse model for testing human antisense oligonucleotides. PLoS One 13(2):e0193289. https://doi.org/10.1371/journal.pone.0193289. ARTN e0193289
Amoasii L, Long C, Li H, Mireault AA, Shelton JM, Sanchez-Ortiz E, McAnally JR, Bhattacharyya S, Schmidt F, Grimm D, Hauschka SD, Bassel-Duby R, Olson EN (2017) Single-cut genome editing restores dystrophin expression in a new mouse model of muscular dystrophy. Sci Transl Med 9(418):eaan8081. https://doi.org/10.1126/scitranslmed.aan8081
Young CS, Mokhonova E, Quinonez M, Pyle AD, Spencer MJ (2017) Creation of a novel humanized dystrophic mouse model of Duchenne muscular dystrophy and application of a CRISPR/Cas9 gene editing therapy. J Neuromuscul Dis 4(2):139–145. https://doi.org/10.3233/JND-170218
Wang B, Li J, Xiao X (2000) Adeno-associated virus vector carrying human minidystrophin genes effectively ameliorates muscular dystrophy in mdx mouse model. Proc Natl Acad Sci U S A 97(25):13714–13719
Harper SQ, Hauser MA, DelloRusso C, Duan D, Crawford RW, Phelps SF, Harper HA, Robinson AS, Engelhardt JF, Brooks SV, Chamberlain JS (2002) Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8(3):253–261
Fabb SA, Wells DJ, Serpente P, Dickson G (2002) Adeno-associated virus vector gene transfer and sarcolemmal expression of a 144 kDa micro-dystrophin effectively restores the dystrophin- associated protein complex and inhibits myofibre degeneration in nude/mdx mice. Hum Mol Genet 11(7):733–741
Yue Y, Li Z, Harper SQ, Davisson RL, Chamberlain JS, Duan D (2003) Microdystrophin gene therapy of cardiomyopathy restores dystrophin-glycoprotein complex and improves sarcolemma integrity in the mdx mouse heart. Circulation 108(13):1626–1632
Liu M, Yue Y, Harper SQ, Grange RW, Chamberlain JS, Duan D (2005) Adeno-associated virus-mediated microdystrophin expression protects young mdx muscle from contraction-induced injury. Mol Ther 11(2):245–256. https://doi.org/10.1016/j.ymthe.2004.09.013. S1525-0016(04)01461-3 [pii]
Lai Y, Thomas GD, Yue Y, Yang HT, Li D, Long C, Judge L, Bostick B, Chamberlain JS, Terjung RL, Duan D (2009) Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Investig 119(3):624–635. https://doi.org/10.1172/JCI36612
Foster H, Sharp PS, Athanasopoulos T, Trollet C, Graham IR, Foster K, Wells DJ, Dickson G (2008) Codon and mRNA sequence optimization of microdystrophin transgenes improves expression and physiological outcome in dystrophic mdx mice following AAV2/8 gene transfer. Mol Ther 16(11):1825–1832. https://doi.org/10.1038/mt.2008.186
Townsend D, Blankinship MJ, Allen JM, Gregorevic P, Chamberlain JS, Metzger JM (2007) Systemic administration of micro-dystrophin restores cardiac geometry and prevents dobutamine-induced cardiac pump failure. Mol Ther 15(6):1086–1092
Gregorevic P, Allen JM, Minami E, Blankinship MJ, Haraguchi M, Meuse L, Finn E, Adams ME, Froehner SC, Murry CE, Chamberlain JS (2006) rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat Med 12(7):787–789
Gregorevic P, Blankinship MJ, Allen JM, Chamberlain JS (2008) Systemic microdystrophin gene delivery improves skeletal muscle structure and function in old dystrophic mdx mice. Mol Ther 16(4):657–664. https://doi.org/10.1038/mt.2008.28
Yue Y, Liu M, Duan D (2006) C-terminal truncated microdystrophin recruits dystrobrevin and syntrophin to the dystrophin-associated glycoprotein complex and reduces muscular dystrophy in symptomatic utrophin/dystrophin double knock-out mice. Mol Ther 14(1):79–87
Wang B, Li J, Fu FH, Xiao X (2009) Systemic human minidystrophin gene transfer improves functions and life span of dystrophin and dystrophin/utrophin-deficient mice. J Orthop Res 27(4):421–426. https://doi.org/10.1002/jor.20781
Hakim CH, Wasala NB, Pan X, Kodippili K, Yue Y, Zhang K, Yao G, Haffner B, Duan SX, Ramos J, Schneider JS, Yang NN, Chamberlain JS, Duan D (2017) A five-repeat micro-dystrophin gene ameliorated dystrophic phenotype in the severe DBA/2J-mdx model of Duchenne muscular dystrophy. Mol Ther Methods Clin Dev 6:216–230. https://doi.org/10.1016/j.omtm.2017.06.006
Bostick B, Yue Y, Duan D (2010) Gender influences cardiac function in the mdx model of Duchenne cardiomyopathy. Muscle Nerve 42(4):600–603. https://doi.org/10.1002/mus.21763
Bostick B, Shin J-H, Yue Y, Duan D (2011) AAV-microdystrophin therapy improves cardiac performance in aged female mdx mice. Mol Ther 19(10):1826–1832
Bostick B, Shin J-H, Yue Y, Wasala NB, Lai Y, Duan D (2012) AAV micro-dystrophin gene therapy alleviates stress-induced cardiac death but not myocardial fibrosis in >21-m-old mdx mice, an end-stage model of Duchenne muscular dystrophy cardiomyopathy. J Mol Cell Cardiol 53(2):217–222. https://doi.org/10.1016/j.yjmcc.2012.05.002. S0022-2828(12)00179-4 [pii]
Duan D (2015) Duchenne muscular dystrophy gene therapy in the canine model. Hum Gene Ther Clin Dev 26(1):57–69. https://doi.org/10.1089/humc.2015.006
Shin J-H, Pan X, Hakim CH, Yang HT, Yue Y, Zhang K, Terjung RL, Duan D (2013) Microdystrophin ameliorates muscular dystrophy in the canine model of Duchenne muscular dystrophy. Mol Ther 21(4):750–757. https://doi.org/10.1038/mt.2012.283
Yue Y, Pan X, Hakim CH, Kodippili K, Zhang K, Shin J-H, Yang HT, McDonald T, Duan D (2015) Safe and bodywide muscle transduction in young adult Duchenne muscular dystrophy dogs with adeno-associated virus. Hum Mol Genet 24(20):5880–5890
Hakim CH, Kodippili K, Jenkins G, Yang HT, Pan X, Lessa TB, Leach SB, Emter C, Yue Y, Zhang K, Duan XS, Yao G, Schneider JS, Yang NN, Chamberlain JS, Duan D (2017) Single systemic AAV micro-dystrophin therapy ameliorates muscular dystrophy in young adult Duchenne muscular dystrophy dogs for up to two years. Mol Ther 25(S1):192–193
Hakim CH, Kodippili K, Jenkins G, Yang HT, Pan X, Lessa TB, Leach SB, Emter C, Yue Y, Zhang K, Duan XS, Yao G, Schneider JS, Yang NN, Chamberlain JS, Duan D (2018) AAV micro-dystrophin therapy ameliorates muscular dystrophy in young adult Duchenne muscular dystrophy dogs for up to 30 months following injection. Mol Ther 26(S1):5
Le Guiner C, Servais L, Montus M, Larcher T, Fraysse B, Moullec S, Allais M, Francois V, Dutilleul M, Malerba A, Koo T, Thibaut JL, Matot B, Devaux M, Le Duff J, Deschamps JY, Barthelemy I, Blot S, Testault I, Wahbi K, Ederhy S, Martin S, Veron P, Georger C, Athanasopoulos T, Masurier C, Mingozzi F, Carlier P, Gjata B, Hogrel JY, Adjali O, Mavilio F, Voit T, Moullier P, Dickson G (2017) Long-term microdystrophin gene therapy is effective in a canine model of Duchenne muscular dystrophy. Nat Commun 8:16105. https://doi.org/10.1038/ncomms16105
Gonzalez JP, Schneider JS, Brown KJ, Golebiowski D, Shanks C, Ricotti V, Laforet G, Quiroz J, Morris CA (2018) Preclinical evaluation of SGT-001 Microdystrophin gene transfer for Duchenne muscular dystrophy. Mol Ther 26(S1):390
Oudet C, Hanauer A, Clemens P, Caskey T, Mandel JL (1992) Two hot spots of recombination in the DMD gene correlate with the deletion prone regions. Hum Mol Genet 1(8):599–603
‘t Hoen PA, de Meijer EJ, Boer JM, Vossen RH, Turk R, Maatman RG, Davies KE, van Ommen GJ, van Deutekom JC, den Dunnen JT (2008) Generation and characterization of transgenic mice with the full-length human DMD gene. J Biol Chem 283(9):5899–5907. https://doi.org/10.1074/jbc.M709410200
Bremmer-Bout M, Aartsma-Rus A, de Meijer EJ, Kaman WE, Janson AA, Vossen RH, van Ommen GJ, den Dunnen JT, van Deutekom JC (2004) Targeted exon skipping in transgenic hDMD mice: a model for direct preclinical screening of human-specific antisense oligonucleotides. Mol Ther 10(2):232–240. https://doi.org/10.1016/j.ymthe.2004.05.031
Li D, Yue Y, Duan D (2010) Marginal level dystrophin expression improves clinical outcome in a strain of dystrophin/utrophin double knockout mice. PLoS One 5(12):e15286. https://doi.org/10.1371/journal.pone.0015286
Li D, Yue Y, Duan D (2008) Preservation of muscle force in mdx3cv mice correlates with low-level expression of a near full-length dystrophin protein. Am J Pathol 172(5):1332–1341. https://doi.org/10.2353/ajpath.2008.071042
Wasala NB, Yue Y, Vance J, Duan D (2017) Uniform low-level dystrophin expression in the heart partially preserved cardiac function in an aged mouse model of Duchenne cardiomyopathy. J Mol Cell Cardiol 102:45–52. https://doi.org/10.1016/j.yjmcc.2016.11.011
van Putten M, van der Pijl EM, Hulsker M, Verhaart IE, Nadarajah VD, van der Weerd L, Aartsma-Rus A (2014) Low dystrophin levels in heart can delay heart failure in mdx mice. J Mol Cell Cardiol 69:17–23. https://doi.org/10.1016/j.yjmcc.2014.01.009
van Putten M, Hulsker M, Young C, Nadarajah VD, Heemskerk H, van der Weerd L, t Hoen PA, van Ommen GJ, Aartsma-Rus AM (2013) Low dystrophin levels increase survival and improve muscle pathology and function in dystrophin/utrophin double-knockout mice. FASEB J 27(6):2484–2495. https://doi.org/10.1096/fj.12-224170
van Putten M, Hulsker M, Nadarajah VD, van Heiningen SH, van Huizen E, van Iterson M, Admiraal P, Messemaker T, den Dunnen JT, t Hoen PA, Aartsma-Rus A (2012) The effects of low levels of dystrophin on mouse muscle function and pathology. PLoS One 7(2):e31937. https://doi.org/10.1371/journal.pone.0031937
Nicholson LV, Johnson MA, Bushby KM, Gardner-Medwin D (1993) Functional significance of dystrophin positive fibres in Duchenne muscular dystrophy. Arch Dis Child 68(5):632–636
Waldrop MA, Gumienny F, El Husayni S, Frank DE, Weiss RB, Flanigan KM (2018) Low-level dystrophin expression attenuating the dystrophinopathy phenotype. Neuromuscul Disord 28(2):116–121. https://doi.org/10.1016/j.nmd.2017.11.007
Cox GA, Cole NM, Matsumura K, Phelps SF, Hauschka SD, Campbell KP, Faulkner JA, Chamberlain JS (1993) Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity. Nature 364(6439):725–729
Yue Y, Wasala NB, Bostick B, Duan D (2016) 100-fold but not 50-fold dystrophin overexpression aggravates electrocardiographic defects in the mdx model of Duchenne muscular dystrophy. Mol Ther Methods Clin Dev 3:16045. https://doi.org/10.1038/mtm.2016.45
Yoshiki A, Moriwaki K (2006) Mouse phenome research: implications of genetic background. ILAR J 47(2):94–102
Linder CC (2001) The influence of genetic background on spontaneous and genetically engineered mouse models of complex diseases. Lab Anim 30(5):34–39
Zucker I, Beery AK (2010) Males still dominate animal studies. Nature 465(7299):690. https://doi.org/10.1038/465690a
Wald C, Wu C (2010) Biomedical research. Of mice and women: the bias in animal models. Science 327(5973):1571–1572. https://doi.org/10.1126/science.327.5973.1571
Leinwand LA (2003) Sex is a potent modifier of the cardiovascular system. J Clin Investig 112(3):302–307
Turner MJ, Kleeberger SR, Lightfoot JT (2005) Influence of genetic background on daily running-wheel activity differs with aging. Physiol Genomics 22(1):76–85. https://doi.org/10.1152/physiolgenomics.00243.2004
Glenmark B, Nilsson M, Gao H, Gustafsson JA, Dahlman-Wright K, Westerblad H (2004) Difference in skeletal muscle function in males vs. females: role of estrogen receptor-beta. Am J Phys Endocrinol Metab 287(6):E1125–E1131. https://doi.org/10.1152/ajpendo.00098.2004. 00098.2004 [pii]
Meyer S, van der Meer P, van Tintelen JP, van den Berg MP (2014) Sex differences in cardiomyopathies. Eur J Heart Fail 16(3):238–247. https://doi.org/10.1002/ejhf.15
Pergola C, Dodt G, Rossi A, Neunhoeffer E, Lawrenz B, Northoff H, Samuelsson B, Radmark O, Sautebin L, Werz O (2008) ERK-mediated regulation of leukotriene biosynthesis by androgens: a molecular basis for gender differences in inflammation and asthma. Proc Natl Acad Sci U S A 105(50):19881–19886. https://doi.org/10.1073/pnas.0809120105
Du XJ, Samuel CS, Gao XM, Zhao L, Parry LJ, Tregear GW (2003) Increased myocardial collagen and ventricular diastolic dysfunction in relaxin deficient mice: a gender-specific phenotype. Cardiovasc Res 57(2):395–404
Hakim CH, Duan D (2012) Gender differences in contractile and passive properties of mdx extensor digitorum longus muscle. Muscle Nerve 45(2):250–256. https://doi.org/10.1002/mus.22275
Dane AP, Cunningham SC, Graf NS, Alexander IE (2009) Sexually dimorphic patterns of episomal rAAV genome persistence in the adult mouse liver and correlation with hepatocellular proliferation. Mol Ther 17(9):1548–1554. https://doi.org/10.1038/mt.2009.139
Voutetakis A, Zheng C, Wang J, Goldsmith CM, Afione S, Chiorini JA, Wenk ML, Vallant M, Irwin RD, Baum BJ (2007) Gender differences in serotype 2 adeno-associated virus biodistribution after administration to rodent salivary glands. Hum Gene Ther 18(11):1109–1118. https://doi.org/10.1089/hum.2007.072
Chandler CH, Chari S, Dworkin I (2013) Does your gene need a background check? How genetic background impacts the analysis of mutations, genes, and evolution. Trends Genet 29(6):358–366. https://doi.org/10.1016/j.tig.2013.01.009
Brayton CF, Treuting PM, Ward JM (2012) Pathobiology of aging mice and GEM: background strains and experimental design. Vet Pathol 49(1):85–105. https://doi.org/10.1177/0300985811430696
Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology 132(2):107–124
Erickson RP (1996) Mouse models of human genetic disease: which mouse is more like a man? BioEssays 18(12):993–998. https://doi.org/10.1002/bies.950181209
Montagutelli X (2000) Effect of the genetic background on the phenotype of mouse mutations. J Am Soc Nephrol 11(11):S101–S105
Schauwecker PE (2002) Complications associated with genetic background effects in models of experimental epilepsy. Prog Brain Res 135:139–148
Lerman I, Harrison BC, Freeman K, Hewett TE, Allen DL, Robbins J, Leinwand LA (2002) Genetic variability in forced and voluntary endurance exercise performance in seven inbred mouse strains. J Appl Physiol 92(6):2245–2255. https://doi.org/10.1152/japplphysiol.01045.2001
Lightfoot JT, Turner MJ, Daves M, Vordermark A, Kleeberger SR (2004) Genetic influence on daily wheel running activity level. Physiol Genomics 19(3):270–276. https://doi.org/10.1152/physiolgenomics.00125.2004
Xing S, Tsaih SW, Yuan R, Svenson KL, Jorgenson LM, So M, Paigen BJ, Korstanje R (2009) Genetic influence on electrocardiogram time intervals and heart rate in aging mice. Am J Physiol Heart Circ Physiol 296(6):H1907–H1913. https://doi.org/10.1152/ajpheart.00681.2008
Kadambi VJ, Ball N, Kranias EG, Walsh RA, Hoit BD (1999) Modulation of force-frequency relation by phospholamban in genetically engineered mice. Am J Physiol-Heart Circ Physiol 276(6):H2245–H2250
Shusterman V, Usiene I, Harrigal C, Lee JS, Kubota T, Feldman AM, London B (2002) Strain-specific patterns of autonomic nervous system activity and heart failure susceptibility in mice. Am J Physiol-Heart Circ Physiol 282(6):H2076–H2083. https://doi.org/10.1152/ajpheart.00917.2001
Rodrigues M, Echigoya Y, Maruyama R, Lim KRQ, Fukada S, Yokota T (2016) Impaired regenerative capacity and lower revertant fibre expansion in dystrophin-deficient mdx muscles on DBA/2 background. Sci Rep 6:38371. https://doi.org/10.1038/srep38371. ARTN 38371
Bostick B, Yue Y, Lai Y, Long C, Li D, Duan D (2008) Adeno-associated virus serotype-9 microdystrophin gene therapy ameliorates electrocardiographic abnormalities in mdx mice. Hum Gene Ther 19(8):851–856. https://doi.org/10.1089/hum.2008.058
Wasala NB, Lai Y, Shin J-H, Zhao J, Yue Y, Duan D (2016) Genomic removal of a therapeutic mini-dystrophin gene from adult mice elicits a Duchenne muscular dystrophy-like phenotype. Hum Mol Genet 25(13):2633–2644. https://doi.org/10.1093/hmg/ddw123
Nance ME, Duan D (2018) Gene therapy: use of viruses as vectors. Reference module in biomedical sciences: Elsevier. https://doi.org/10.1016/B978-0-12-801238-3.95711-8
Ginn SL, Amaya AK, Alexander IE, Edelstein M, Abedi MR (2018) Gene therapy clinical trials worldwide to 2017: an update. J Gene Med 20(5):e3015. https://doi.org/10.1002/jgm.3015. ARTN e3015
Duan D (2008) Myodys, a full-length dystrophin plasmid vector for Duchenne and Becker muscular dystrophy gene therapy. Curr Opin Mol Ther 10(1):86–94
Braun S (2008) Muscular gene transfer using nonviral vectors. Curr Gene Ther 8(5):391–405
Fassati A, Bresolin N (2000) Retroviral vectors for gene therapy of Duchenne muscular dystrophy. Neurol Sci 21(5):S925–S927
Karpati G, Gilbert R, Petrof BJ, Nalbantoglu J (1997) Gene therapy research for Duchenne and Becker muscular dystrophies. Curr Opin Neurol 10(5):430–435
Flotte TR, Gao GP (2017) AAV is now a medicine: we had better get this right. Hum Gene Ther 28(4):307–307. https://doi.org/10.1089/hum.2017.29041.trf
McCarty DM (2008) Self-complementary AAV vectors; advances and applications. Mol Ther 16(10):1648–1656. https://doi.org/10.1038/mt.2008.171. mt2008171 [pii]
McCarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ (2003) Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther 10(26):2112–2118. https://doi.org/10.1038/sj.gt.3302134
Ferrari FK, Samulski T, Shenk T, Samulski RJ (1996) Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J Virol 70(5):3227–3234
Fisher KJ, Gao GP, Weitzman MD, DeMatteo R, Burda JF, Wilson JM (1996) Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J Virol 70(1):520–532
Benkhelifa-Ziyyat S, Besse A, Roda M, Duque S, Astord S, Carcenac R, Marais T, Barkats M (2013) Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice. Mol Ther 21(2):282–290. https://doi.org/10.1038/mt.2012.261
Nathwani AC, Gray JT, Ng CY, Zhou J, Spence Y, Waddington SN, Tuddenham EG, Kemball-Cook G, McIntosh J, Boon-Spijker M, Mertens K, Davidoff AM (2006) Self-complementary adeno-associated virus vectors containing a novel liver-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver. Blood 107(7):2653–2661. https://doi.org/10.1182/blood-2005-10-4035
Li X, Eastman EM, Schwartz RJ, Draghia-Akli R (1999) Synthetic muscle promoters: activities exceeding naturally occurring regulatory sequences. Nat Biotechnol 17(3):241–245
Jaynes JB, Chamberlain JS, Buskin JN, Johnson JE, Hauschka SD (1986) Transcriptional regulation of the muscle creatine kinase gene and regulated expression in transfected mouse myoblasts. Mol Cell Biol 6(8):2855–2864
Shaul O (2017) How introns enhance gene expression. Int J Biochem Cell Biol 91(Pt B):145–155. https://doi.org/10.1016/j.biocel.2017.06.016
Lozier JN (2012) Gene therapy. Factor IX Padua: them that have, give. Blood 120(23):4452–4453. https://doi.org/10.1182/blood-2012-09-452821
Krieg AM, Yi AK, Matson S, Waldschmidt TJ, Bishop GA, Teasdale R, Koretzky GA, Klinman DM (1995) Cpg motifs in bacterial-DNA trigger direct B-cell activation. Nature 374(6522):546–549. https://doi.org/10.1038/374546a0
Faust SM, Bell P, Cutler BJ, Ashley SN, Zhu Y, Rabinowitz JE, Wilson JM (2013) CpG-depleted adeno-associated virus vectors evade immune detection. J Clin Investig 123(7):2994–3001. https://doi.org/10.1172/JCI68205
Lai Y, Zhao J, Yue Y, Duan D (2013) alpha2 and alpha3 helices of dystrophin R16 and R17 frame a microdomain in the alpha1 helix of dystrophin R17 for neuronal NOS binding. Proc Natl Acad Sci U S A 110(2):525–530. https://doi.org/10.1073/pnas.1211431109. 1211431109 [pii]
Proudfoot N, O’Sullivan J (2002) Polyadenylation: a tail of two complexes. Curr Biol 12(24):R855–R857
Powell SK, Rivera-Soto R, Gray SJ (2015) Viral expression cassette elements to enhance transgene target specificity and expression in gene therapy. Discov Med 19(102):49–57
Levitt N, Briggs D, Gil A, Proudfoot NJ (1989) Definition of an efficient synthetic poly(A) site. Genes Dev 3(7):1019–1025
Kotterman MA, Schaffer DV (2014) Engineering adeno-associated viruses for clinical gene therapy. Nat Rev Genet 15(7):445–451. https://doi.org/10.1038/nrg3742
Qiao C, Zhang W, Yuan Z, Shin J-H, Li J, Jayandharan GR, Zhong L, Srivastava A, Xiao X, Duan D (2010) AAV6 capsid tyrosine to phenylalanine mutations improve gene transfer to skeletal muscle. Hum Gene Ther 21(10):1343–1348. https://doi.org/10.1089/hum.2010.003
Nance ME, Duan D (2015) Perspective on adeno-associated virus (AAV) capsid modification for Duchenne muscular dystrophy gene therapy. Hum Gene Ther 26(12):786–800
Asokan A, Conway JC, Phillips JL, Li C, Hegge J, Sinnott R, Yadav S, DiPrimio N, Nam HJ, Agbandje-McKenna M, McPhee S, Wolff J, Samulski RJ (2010) Reengineering a receptor footprint of adeno-associated virus enables selective and systemic gene transfer to muscle. Nat Biotechnol 28(1):79–82. https://doi.org/10.1038/nbt.1599
Pulicherla N, Shen S, Yadav S, Debbink K, Govindasamy L, Agbandje-McKenna M, Asokan A (2011) Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer. Mol Ther 19(6):1070–1078. https://doi.org/10.1038/mt.2011.22. mt201122 [pii]
Choudhury SR, Fitzpatrick Z, Harris AF, Maitland SA, Ferreira JS, Zhang Y, Ma S, Sharma RB, Gray-Edwards HL, Johnson JA, Johnson AK, Alonso LC, Punzo C, Wagner KR, Maguire CA, Kotin RM, Martin DR, Sena-Esteves M (2016) In vivo selection yields AAV-B1 capsid for central nervous system and muscle gene therapy. Mol Ther 24(7):1247–1257. https://doi.org/10.1038/mt.2016.84
Yu CY, Yuan Z, Cao Z, Wang B, Qiao C, Li J, Xiao X (2009) A muscle-targeting peptide displayed on AAV2 improves muscle tropism on systemic delivery. Gene Ther 16(8):953–962. https://doi.org/10.1038/gt.2009.59
Yang L, Jiang J, Drouin LM, Agbandje-McKenna M, Chen C, Qiao C, Pu D, Hu X, Wang DZ, Li J, Xiao X (2009) A myocardium tropic adeno-associated virus (AAV) evolved by DNA shuffling and in vivo selection. Proc Natl Acad Sci U S A 106(10):3946–3951. https://doi.org/10.1073/pnas.0813207106
Paulk NK, Pekrun K, Charville GW, Maguire-Nguyen K, Wosczyna MN, Xu J, Zhang Y, Lisowski L, Yoo B, Vilches-Moure JG, Lee GK, Shrager JB, Rando TA, Kay MA (2018) Bioengineered viral platform for intramuscular passive vaccine delivery to human skeletal muscle. Mol Ther Methods Clin Dev 10:144–155. https://doi.org/10.1016/j.omtm.2018.06.001
Weinmann J, Weis S, Sippel J, Lenter M, Lamla T, Grimm D (2018) Massively parallel in vivo characterization of >150 Adeno-Associated Viral (AAV) capsids using DNA/RNA barcoding and next-generation sequencing. Mol Ther 26(S1):319–318
Wang L, Bell P, Somanathan S, Wang Q, He Z, Yu H, McMenamin D, Goode T, Calcedo R, Wilson JM (2015) Comparative study of liver gene transfer with AAV vectors based on natural and engineered AAV capsids. Mol Ther 23(12):1877–1887. https://doi.org/10.1038/mt.2015.179
Li S, Ling C, Zhong L, Li M, Su Q, He R, Tang Q, Greiner DL, Shultz LD, Brehm MA, Flotte TR, Mueller C, Srivastava A, Gao G (2015) Efficient and targeted transduction of nonhuman primate liver with systemically delivered optimized AAV3B vectors. Mol Ther 23(12):1867–1876. https://doi.org/10.1038/mt.2015.174
Pan X, Yue Y, Zhang K, Hakim CH, Kodippili K, McDonald T, Duan D (2015) AAV-8 is more efficient than AAV-9 in transducing neonatal dog heart. Hum Gene Ther Methods 26(4):54–61
Pan X, Yue Y, Zhang K, Lostal W, Shin JH, Duan D (2013) Long-term robust myocardial transduction of the dog heart from a peripheral vein by adeno-associated virus serotype-8. Hum Gene Ther 24(6):584–594. https://doi.org/10.1089/hum.2013.044
Yue Y, Ghosh A, Long C, Bostick B, Smith BF, Kornegay JN, Duan D (2008) A single intravenous injection of adeno-associated virus serotype-9 leads to whole-body skeletal muscle transduction in dogs. Mol Ther 16(12):1944–1952. https://doi.org/10.1038/mt.2008.207
Yuasa K, Ishii A, Miyagoe Y, Takeda S (1997) Introduction of rod-deleted dystrophin cDNA, delta DysM3, into mdx skeletal muscle using adenovirus vector. Nihon Rinsho 55(12):3148–3153
Gregorevic P, Blankinship MJ, Allen JM, Crawford RW, Meuse L, Miller DG, Russell DW, Chamberlain JS (2004) Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat Med 10(8):828–834
Wang Z, Zhu T, Qiao C, Zhou L, Wang B, Zhang J, Chen C, Li J, Xiao X (2005) Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 23(3):321–328
Bostick B, Ghosh A, Yue Y, Long C, Duan D (2007) Systemic AAV-9 transduction in mice is influenced by animal age but not by the route of administration. Gene Ther 14(22):1605–1609
Kuntz N, Shieh PB, Smith B, Bonnemann CG, Dowling JJ, Lawlor MW, Muller-Felber W, Noursalehi M, Rico S, Servais L, Prasad S (2018) ASPIRO phase 1/2 gene therapy trail in X-linked myotubular myopathy (XLMTM): preliminary safety and efficacy findings. Mol Ther 26(S1):4
Nathwani AC, Reiss UM, Tuddenham EG, Rosales C, Chowdary P, McIntosh J, Della Peruta M, Lheriteau E, Patel N, Raj D, Riddell A, Pie J, Rangarajan S, Bevan D, Recht M, Shen YM, Halka KG, Basner-Tschakarjan E, Mingozzi F, High KA, Allay J, Kay MA, Ng CY, Zhou J, Cancio M, Morton CL, Gray JT, Srivastava D, Nienhuis AW, Davidoff AM (2014) Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med 371(21):1994–2004. https://doi.org/10.1056/NEJMoa1407309
Mendell JR, Campbell K, Rodino-Klapac L, Sahenk Z, Shilling C, Lewis S, Bowles D, Gray S, Li C, Galloway G, Malik V, Coley B, Clark KR, Li J, Xiao X, Samulski J, McPhee SW, Samulski RJ, Walker CM (2010) Dystrophin immunity in Duchenne’s muscular dystrophy. N Engl J Med 363(15):1429–1437. https://doi.org/10.1056/NEJMoa1000228
Mingozzi F (2018) AAV immunogenicity: a matter of sensitivity. Mol Ther 26(10):2335–2336. https://doi.org/10.1016/j.ymthe.2018.09.001
Calcedo R, Franco J, Qin Q, Richardson DW, Mason JB, Boyd S, Wilson JM (2015) Preexisting neutralizing antibodies to adeno-associated virus capsids in large animals other than monkeys may confound in vivo gene therapy studies. Hum Gene Ther Methods 26(3):103–105. https://doi.org/10.1089/hgtb.2015.082
Rapti K, Louis-Jeune V, Kohlbrenner E, Ishikawa K, Ladage D, Zolotukhin S, Hajjar RJ, Weber T (2011) Neutralizing antibodies against AAV serotypes 1, 2, 6, and 9 in sera of commonly used animal models. Mol Ther 20(1):73–83. https://doi.org/10.1038/mt.2011.177. mt2011177 [pii]
Shin J-H, Yue Y, Smith B, Duan D (2012) Humoral immunity to AAV-6, 8, and 9 in normal and dystrophic dogs. Hum Gene Ther 23(3):287–294. https://doi.org/10.1089/hum.2011.125
Scallan CD, Jiang H, Liu T, Patarroyo-White S, Sommer JM, Zhou S, Couto LB, Pierce GF (2006) Human immunoglobulin inhibits liver transduction by AAV vectors at low AAV2 neutralizing titers in SCID mice. Blood 107(5):1810–1817. https://doi.org/10.1182/blood-2005-08-3229
Jiang H, Couto LB, Patarroyo-White S, Liu T, Nagy D, Vargas JA, Zhou S, Scallan CD, Sommer J, Vijay S, Mingozzi F, High KA, Pierce GF (2006) Effects of transient immunosuppression on adenoassociated, virus-mediated, liver-directed gene transfer in rhesus macaques and implications for human gene therapy. Blood 108(10):3321–3328. https://doi.org/10.1182/blood-2006-04-017913
Hurlbut GD, Ziegler RJ, Nietupski JB, Foley JW, Woodworth LA, Meyers E, Bercury SD, Pande NN, Souza DW, Bree MP, Lukason MJ, Marshall J, Cheng SH, Scheule RK (2010) Preexisting immunity and low expression in primates highlight translational challenges for liver-directed AAV8-mediated gene therapy. Mol Ther 18(11):1983–1994. https://doi.org/10.1038/mt.2010.175. mt2010175 [pii]
Ayuso E, Mingozzi F, Montane J, Leon X, Anguela XM, Haurigot V, Edmonson SA, Africa L, Zhou S, High KA, Bosch F, Wright JF (2010) High AAV vector purity results in serotype- and tissue-independent enhancement of transduction efficiency. Gene Ther 17(4):503–510. https://doi.org/10.1038/gt.2009.157
Schnodt M, Buning H (2017) Improving the quality of adeno-associated viral vector preparations: the challenge of product-related impurities. Hum Gene Ther Methods 28(3):101–108. https://doi.org/10.1089/hgtb.2016.188
Kotin RM (2011) Large-scale recombinant adeno-associated virus production. Hum Mol Genet 20(R1):R2–R6. https://doi.org/10.1093/hmg/ddr141
Clement N, Grieger JC (2016) Manufacturing of recombinant adeno-associated viral vectors for clinical trials. Mol Ther Methods Clin Dev 3:16002. https://doi.org/10.1038/mtm.2016.2
Penaud-Budloo M, Francois A, Clement N, Ayuso E (2018) Pharmacology of recombinant adeno-associated virus production. Mol Ther Methods Clin Dev 8:166–180. https://doi.org/10.1016/j.omtm.2018.01.002
Grieger JC, Soltys SM, Samulski RJ (2016) Production of recombinant adeno-associated virus vectors using suspension HEK293 cells and continuous harvest of vector from the culture media for GMP FIX and FLT1 clinical vector. Mol Ther 24(2):287–297. https://doi.org/10.1038/mt.2015.187
Kotin RM, Snyder RO (2017) Manufacturing clinical grade recombinant adeno-associated virus using invertebrate cell lines. Hum Gene Ther 28(4):350–360. https://doi.org/10.1089/hum.2017.042
Clement N, Knop DR, Byrne BJ (2009) Large-scale adeno-associated viral vector production using a herpesvirus-based system enables manufacturing for clinical studies. Hum Gene Ther 20(8):796–806. https://doi.org/10.1089/hum.2009.094
Lock M, Alvira M, Vandenberghe LH, Samanta A, Toelen J, Debyser Z, Wilson JM (2010) Rapid, simple, and versatile manufacturing of recombinant adeno-associated viral vectors at scale. Hum Gene Ther 21(10):1259–1271. https://doi.org/10.1089/hum.2010.055
D’Costa S, Blouin V, Broucque F, Penaud-Budloo M, Francois A, Perez IC, Le Bec C, Moullier P, Snyder RO, Ayuso E (2016) Practical utilization of recombinant AAV vector reference standards: focus on vector genomes titration by free ITR qPCR. Mol Ther Methods Clin Dev 5:16019. https://doi.org/10.1038/mtm.2016.19
Ayuso E, Blouin V, Lock M, McGorray S, Leon X, Alvira MR, Auricchio A, Bucher S, Chtarto A, Clark KR, Darmon C, Doria M, Fountain W, Gao GP, Gao K, Giacca M, Kleinschmidt J, Leuchs B, Melas C, Mizukami H, Muller M, Noordman Y, Bockstael O, Ozawa K, Pythoud C, Sumaroka M, Surosky R, Tenenbaum L, van der Linden I, Weins B, Wright JF, Zhang XH, Zentilin L, Bosch F, Snyder RO, Moullier P (2014) Manufacturing and characterization of a recombinant Adeno-associated virus type 8 reference standard material. Hum Gene Ther 25(11):977–987. https://doi.org/10.1089/hum.2014.057
Moullier P, Snyder RO (2008) International efforts for recombinant adeno-associated viral vector reference standards. Mol Ther 16(7):1185–1188. https://doi.org/10.1038/mt.2008.125
Fagone P, Wright JF, Nathwani AC, Nienhuis AW, Davidoff AM, Gray JT (2012) Systemic errors in quantitative polymerase chain reaction titration of self-complementary adeno-associated viral vectors and improved alternative methods. Hum Gene Ther Methods 23(1):1–7. https://doi.org/10.1089/hgtb.2011.104
Werling NJ, Satkunanathan S, Thorpe R, Zhao Y (2015) Systematic comparison and validation of quantitative real-time PCR methods for the quantitation of adeno-associated viral products. Hum Gene Ther Methods 26(3):82–92. https://doi.org/10.1089/hgtb.2015.013
Duan D (2011) Muscle gene therapy: methods and protocols. Methods in molecular biology, vol 709. Humana, New York
Kyba M (2016) Skeletal muscle regeneration in the mouse: methods and protocols. Springer Protocols, vol 1460. Humana Press, New York
DiMario JX (2012) Myogenesis: methods and protocols. Methods in molecular biology, vol 798. Humana Press/Springer, New York
Moorwood C, Liu M, Tian Z, Barton ER (2013) Isometric and eccentric force generation assessment of skeletal muscles isolated from murine models of muscular dystrophies. J Vis Exp (71):e50036. https://doi.org/10.3791/50036
Hakim CH, Wasala NB, Duan D (2013) Evaluation of muscle function of the extensor digitorum longus muscle ex vivo and tibialis anterior muscle in situ in mice. J Vis Exp (72):e50183. https://doi.org/10.3791/50183
Kumar A, Accorsi A, Rhee Y, Girgenrath M (2015) Do’s and don’ts in the preparation of muscle cryosections for histological analysis. J Vis Exp (99):e52793. https://doi.org/10.3791/52793
Grieger JC, Choi VW, Samulski RJ (2006) Production and characterization of adeno-associated viral vectors. Nat Protoc 1(3):1412–1428
Duricki DA, Soleman S, Moon LD (2016) Analysis of longitudinal data from animals with missing values using SPSS. Nat Protoc 11(6):1112–1129. https://doi.org/10.1038/nprot.2016.048
Bagasra O (2007) Protocols for the in situ PCR-amplification and detection of mRNA and DNA sequences. Nat Protoc 2(11):2782–2795. https://doi.org/10.1038/nprot.2007.395
Jager L, Hausl MA, Rauschhuber C, Wolf NM, Kay MA, Ehrhardt A (2009) A rapid protocol for construction and production of high-capacity adenoviral vectors. Nat Protoc 4(4):547–564. https://doi.org/10.1038/nprot.2009.4
Duan D, Rafael-Fortney JA, Blain A, Kass DA, McNally EM, Metzger JM, Spurney CF, Kinnett K (2016) Standard operating procedures (SOPs) for evaluating the heart in preclinical studies of Duchenne muscular dystrophy. J Cardiovasc Transl Res 9(1):85–86. https://doi.org/10.1007/s12265-015-9669-6
Briguet A, Courdier-Fruh I, Foster M, Meier T, Magyar JP (2004) Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromuscul Disord 14(10):675–682. https://doi.org/10.1016/j.nmd.2004.06.008
Nagaraju K, Willmann R, Network T-N, the Wellstone Muscular Dystrophy Cooperative Research Network (2009) Developing standard procedures for murine and canine efficacy studies of DMD therapeutics: report of two expert workshops on “pre-clinical testing for Duchenne dystrophy”: Washington DC, October 27th-28th 2007 and Zurich, June 30th-July 1st 2008. Neuromuscul Disord 19(7):502–506. https://doi.org/10.1016/j.nmd.2009.05.003
van Putten M, Aartsma-Rus A, Grounds MD, Kornegay JN, Mayhew A, Gillingwater TH, Takeda S, Ruegg MA, De Luca A, Nagaraju K, Willmann R (2018) Update on standard operating procedures in preclinical research for DMD and SMA report of TREAT-NMD Alliance workshop, Schiphol airport, 26 April 2015, the Netherlands. J Neuromuscul Dis 5(1):29–34. https://doi.org/10.3233/JND-170288
Shin J-H, Greer B, Hakim CH, Zhou Z, Chung YC, Duan Y, He Z, Duan D (2013) Quantitative phenotyping of Duchenne muscular dystrophy dogs by comprehensive gait analysis and overnight activity monitoring. PLoS One 8(3):e59875
Jenkins GJ, Hakim CH, Yang NN, Yao G, Duan D (2018) Automatic characterization of stride parameters in canines with a single wearable inertial sensor. PLoS One 13(6):e0198893. https://doi.org/10.1371/journal.pone.0198893
Marsh AP, Eggebeen JD, Kornegay JN, Markert CD, Childers MK (2010) Kinematics of gait in golden retriever muscular dystrophy. Neuromuscul Disord 20(1):16–20. https://doi.org/10.1016/j.nmd.2009.10.007. S0960-8966(09)00660-9 [pii]
Barthelemy I, Barrey E, Thibaud JL, Uriarte A, Voit T, Blot S, Hogrel JY (2009) Gait analysis using accelerometry in dystrophin-deficient dogs. Neuromuscul Disord 19(11):788–796. https://doi.org/10.1016/j.nmd.2009.07.014. S0960-8966(09)00578-1 [pii]
Hakim CH, Peters AA, Feng F, Yao G, Duan D (2015) Night activity reduction is a signature physiological biomarker for Duchenne muscular dystroophy dogs. J Neuromuscul Dis 2(4):397–407. https://doi.org/10.3233/JND-150114
Hakim CH, Mijailovic A, Lessa TB, Coates JR, Shin C, Rutkove SB, Duan D (2017) Non-invasive evaluation of muscle disease in the canine model of Duchenne muscular dystrophy by electrical impedance myography. PLoS One 12(3):e0173557. https://doi.org/10.1371/journal.pone.0173557
Yang HT, Shin J-H, Hakim CH, Pan X, Terjung RL, Duan D (2012) Dystrophin deficiency compromises force production of the extensor carpi ulnaris muscle in the canine model of Duchenne muscular dystrophy. PLoS One 7(9):e44438
Kodippili K, Hakim CH, Yang HT, Pan X, Yang NN, Laughlin MH, Terjung RL, Duan D (2018) Nitric oxide dependent attenuation of norepinephrine-induced vasoconstriction is impaired in the canine model of Duchenne muscular dystrophy. J Physiol 596(21):5199–5216. https://doi.org/10.1113/JP275672
Capes-Davis A, Neve RM (2016) Authentication: a standard problem or a problem of standards? PLoS Biol 14(6):e1002477. https://doi.org/10.1371/journal.pbio.1002477
Williams M (2018) Reagent validation to facilitate experimental reproducibility. Curr Protoc Pharmacol 81(1):e40. https://doi.org/10.1002/cpph.40
Casadevall A, Ellis LM, Davies EW, McFall-Ngai M, Fang FC (2016) A framework for improving the quality of research in the biological sciences. MBio 7(4). https://doi.org/10.1128/mBio.01256-16
Landis SC, Amara SG, Asadullah K, Austin CP, Blumenstein R, Bradley EW, Crystal RG, Darnell RB, Ferrante RJ, Fillit H, Finkelstein R, Fisher M, Gendelman HE, Golub RM, Goudreau JL, Gross RA, Gubitz AK, Hesterlee SE, Howells DW, Huguenard J, Kelner K, Koroshetz W, Krainc D, Lazic SE, Levine MS, Macleod MR, McCall JM, Moxley RT 3rd, Narasimhan K, Noble LJ, Perrin S, Porter JD, Steward O, Unger E, Utz U, Silberberg SD (2012) A call for transparent reporting to optimize the predictive value of preclinical research. Nature 490(7419):187–191. https://doi.org/10.1038/nature11556
Freedman LP, Inglese J (2014) The increasing urgency for standards in basic biologic research. Cancer Res 74(15):4024–4029. https://doi.org/10.1158/0008-5472.Can-14-0925
Kodippili K, Vince L, Shin JH, Yue Y, Morris GE, McIntosh MA, Duan D (2014) Characterization of 65 epitope-specific dystrophin monoclonal antibodies in canine and murine models of Duchenne muscular dystrophy by immunostaining and western blot. PLoS One 9(2):e88280. https://doi.org/10.1371/journal.pone.0088280
Morris GE, Man NT, Sewry CA (2011) Monitoring Duchenne muscular dystrophy gene therapy with epitope-specific monoclonal antibodies. Methods Mol Biol 709:39–61. https://doi.org/10.1007/978-1-61737-982-6_3
Nguyen TM, Ginjaar IB, van Ommen GJ, Morris GE (1992) Monoclonal antibodies for dystrophin analysis. Epitope mapping and improved binding to SDS-treated muscle sections. Biochem J 288(Pt 2):663–668
Uhlen M, Bandrowski A, Carr S, Edwards A, Ellenberg J, Lundberg E, Rimm DL, Rodriguez H, Hiltke T, Snyder M, Yamamoto T (2016) A proposal for validation of antibodies. Nat Methods 13(10):823–827. https://doi.org/10.1038/Nmeth.3995
Bordeaux J, Welsh A, Agarwal S, Killiam E, Baquero M, Hanna J, Anagnostou V, Rimm D (2010) Antibody validation. BioTechniques 48(3):197–209. https://doi.org/10.2144/000113382
Marx V (2013) Finding the right antibody for the job. Nat Methods 10(8):703–707. https://doi.org/10.1038/nmeth.2570
Taussig MJ, Fonseca C, Trimmer JS (2018) Antibody validation: a view from the mountains. New Biotechnol 45:1–8. https://doi.org/10.1016/j.nbt.2018.08.002
Bradbury A, Pluckthun A (2015) Standardize antibodies used in research. Nature 518(7537):27–29. https://doi.org/10.1038/518027a
Alm TL, von Feilitzen K, Uhlen M (2016) Antibodypedia - the Wiki of Antibodies. Poster presented at the 2016 American Society for Cell Biology (ASCB) Annual Meeting, San Francisco, CA, Dec. 3-7, 2016. https://www.ascb.org/wp-content/uploads/2016/04/2016ASCBMeeting-PosterAbstracts.pdf. urn:nbn:se:kth:diva-204763
Bjorling E, Uhlen M (2008) Antibodypedia, a portal for sharing antibody and antigen validation data. Mol Cell Proteomics 7(10):2028–2037. https://doi.org/10.1074/mcp.M800264-MCP200
Colwill K, Renewable Protein Binder Working Group, Graslund S (2011) A roadmap to generate renewable protein binders to the human proteome. Nat Methods 8(7):551–558. https://doi.org/10.1038/nmeth.1607
Helsby MA, Leader PM, Fenn JR, Gulsen T, Bryant C, Doughton G, Sharpe B, Whitley P, Caunt CJ, James K, Pope AD, Kelly DH, Chalmers AD (2014) CiteAb: a searchable antibody database that ranks antibodies by the number of times they have been cited. BMC Cell Biol 15:6. https://doi.org/10.1186/1471-2121-15-6
Major SM, Nishizuka S, Morita D, Rowland R, Sunshine M, Shankavaram U, Washburn F, Asin D, Kouros-Mehr H, Kane D, Weinstein JN (2006) AbMiner: a bioinformatic resource on available monoclonal antibodies and corresponding gene identifiers for genomic, proteomic, and immunologic studies. BMC Bioinformatics 7:192. https://doi.org/10.1186/1471-2105-7-192
Roncador G, Engel P, Maestre L, Anderson AP, Cordell JL, Cragg MS, Serbec VC, Jones M, Lisnic VJ, Kremer L, Li D, Koch-Nolte F, Pascual N, Rodriguez-Barbosa JI, Torensma R, Turley H, Pulford K, Banham AH (2016) The European antibody network’s practical guide to finding and validating suitable antibodies for research. MAbs 8(1):27–36. https://doi.org/10.1080/19420862.2015.1100787
Acharya P, Quinlan A, Neumeister V (2017) The ABCs of finding a good antibody: how to find a good antibody, validate it, and publish meaningful data. F1000Res 6:851. https://doi.org/10.12688/f1000research.11774.1
Aban IB, George B (2015) Statistical considerations for preclinical studies. Exp Neurol 270:82–87. https://doi.org/10.1016/j.expneurol.2015.02.024
Liu C, Cripe TP, Kim MO (2010) Statistical issues in longitudinal data analysis for treatment efficacy studies in the biomedical sciences. Mol Ther 18(9):1724–1730. https://doi.org/10.1038/mt.2010.127
Dell RB, Holleran S, Ramakrishnan R (2002) Sample size determination. ILAR J 43(4):207–213
Fitts DA (2011) Ethics and animal numbers: informal analyses, uncertain sample sizes, inefficient replications, and type I errors. J Am Assoc Lab Anim Sci 50(4):445–453
Lenth RV (2001) Some practical guidelines for effective sample size determination. Am Stat 55(3):187–193. https://doi.org/10.1198/000313001317098149
Hardouin JB, Amri S, Feddag ML, Sebille V (2012) Towards power and sample size calculations for the comparison of two groups of patients with item response theory models. Stat Med 31(11–12):1277–1290. https://doi.org/10.1002/sim.4387
Whitley E, Ball J (2002) Statistics review 4: sample size calculations. Crit Care 6(4):335–341
Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39(2):175–191
Hirst JA, Howick J, Aronson JK, Roberts N, Perera R, Koshiaris C, Heneghan C (2014) The need for randomization in animal trials: an overview of systematic reviews. PLoS One 9(6):e98856. https://doi.org/10.1371/journal.pone.0098856
Macleod MR (2014) Design animal studies better. Nature 510(7503):35–35. https://doi.org/10.1038/510035a
Suresh K (2011) An overview of randomization techniques: an unbiased assessment of outcome in clinical research. J Hum Reprod Sci 4(1):8–11. https://doi.org/10.4103/0974-1208.82352
Whitley E, Ball J (2002) Statistics review 5: comparison of means. Crit Care 6(5):424–428
Bewick V, Cheek L, Ball J (2004) Statistics review 9: one-way analysis of variance. Crit Care 8(2):130–136. https://doi.org/10.1186/cc2836
Whitley E, Bai J (2002) Statistics review 6: nonparametric methods. Crit Care 6(6):509–513. https://doi.org/10.1186/cc1820
Baker M (2016) Statisticians issue warning over misuse of P values. Nature 531(7593):151. https://doi.org/10.1038/nature.2016.19503
Wasserstein RL, Assoc AS (2016) ASA statement on statistical significance and P-values. Am Stat 70(2):131–133
Wasserstein RL, Lazar NA (2016) The ASA’s statement on p-values: context, process, and purpose. Am Stat 70(2):129–131. https://doi.org/10.1080/00031305.2016.1154108
Greenland S, Senn SJ, Rothman KJ, Carlin JB, Poole C, Goodman SN, Altman DG (2016) Statistical tests, P values, confidence intervals, and power: a guide to misinterpretations. Eur J Epidemiol 31(4):337–350. https://doi.org/10.1007/s10654-016-0149-3
Nuzzo R (2014) Scientific method: statistical errors. Nature 506(7487):150–152. https://doi.org/10.1038/506150a
Couzin-Frankel J (2013) When mice mislead. Science 342(6161):922–923, 925. https://doi.org/10.1126/science.342.6161.922
Perrin S (2014) Preclinical research: make mouse studies work. Nature 507(7493):423–425. https://doi.org/10.1038/507423a
van der Worp HB, Howells DW, Sena ES, Porritt MJ, Rewell S, O’Collins V, Macleod MR (2010) Can animal models of disease reliably inform human studies? PLoS Med 7(3):e1000245. https://doi.org/10.1371/journal.pmed.1000245. ARTN e1000245
Hathout Y, Brody E, Clemens PR, Cripe L, DeLisle RK, Furlong P, Gordish-Dressman H, Hache L, Henricson E, Hoffman EP, Kobayashi YM, Lorts A, Mah JK, McDonald C, Mehler B, Nelson S, Nikrad M, Singer B, Steele F, Sterling D, Sweeney HL, Williams S, Gold L (2015) Large-scale serum protein biomarker discovery in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 112(23):7153–7158. https://doi.org/10.1073/pnas.1507719112
Meltzer HY (1971) Factors affecting serum creatine phosphokinase levels in the general population: the role of race, activity and age. Clin Chim Acta 33(1):165–172
Gledhill RF, Van der Merwe CA, Greyling M, Van Niekerk MM (1988) Race-gender differences in serum creatine kinase activity: a study among South Africans. J Neurol Neurosurg Psychiatry 51(2):301–304
Neal RC, Ferdinand KC, Ycas J, Miller E (2009) Relationship of ethnic origin, gender, and age to blood creatine kinase levels. Am J Med 122(1):73–78. https://doi.org/10.1016/j.amjmed.2008.08.033
Parasuraman S, Raveendran R, Kesavan R (2010) Blood sample collection in small laboratory animals. J Pharmacol Pharmacother 1(2):87–93. https://doi.org/10.4103/0976-500X.72350
Baudy AR, Sali A, Jordan S, Kesari A, Johnston HK, Hoffman EP, Nagaraju K (2011) Non-invasive optical imaging of muscle pathology in mdx mice using cathepsin caged near-infrared imaging. Mol Imaging Biol 13(3):462–470. https://doi.org/10.1007/s11307-010-0376-z
Coley WD, Bogdanik L, Vila MC, Yu Q, Van Der Meulen JH, Rayavarapu S, Novak JS, Nearing M, Quinn JL, Saunders A, Dolan C, Andrews W, Lammert C, Austin A, Partridge TA, Cox GA, Lutz C, Nagaraju K (2016) Effect of genetic background on the dystrophic phenotype in mdx mice. Hum Mol Genet 25(1):130–145. https://doi.org/10.1093/hmg/ddv460
de Greef JC, Hamlyn R, Jensen BS, O’Campo Landa R, Levy JR, Kobuke K, Campbell KP (2016) Collagen VI deficiency reduces muscle pathology, but does not improve muscle function, in the gamma-sarcoglycan-null mouse. Hum Mol Genet 25(7):1357–1369. https://doi.org/10.1093/hmg/ddw018
Dirnagl U, Fisher M (2012) International, multicenter randomized preclinical trials in translational stroke research: it’s time to act. J Cereb Blood Flow Metab 32(6):933–935. https://doi.org/10.1038/jcbfm.2012.51
Bath PM, Macleod MR, Green AR (2009) Emulating multicentre clinical stroke trials: a new paradigm for studying novel interventions in experimental models of stroke. Int J Stroke 4(6):471–479. https://doi.org/10.1111/j.1747-4949.2009.00386.x
Llovera G, Liesz A (2016) The next step in translational research: lessons learned from the first preclinical randomized controlled trial. J Neurochem 139:271–279. https://doi.org/10.1111/jnc.13516
Amaro S, Llull L (2016) Preclinical randomized controlled multicenter trials in translational stroke research. Ann Transl Med 4(Suppl 1):S58. https://doi.org/10.21037/atm.2016.10.66
Mullard A (2011) Reliability of ‘new drug target’ claims called into question. Nat Rev Drug Discov 10(9):643–644. https://doi.org/10.1038/nrd3545. nrd3545 [pii]
Baker M (2016) Biotech giant publishes failures to confirm high-profile science. Nature 530(7589):141. https://doi.org/10.1038/nature.2016.19269
Aarts AA, Anderson JE, Anderson CJ, Attridge PR, Attwood A, Axt J, Babel M, Bahnik S, Baranski E, Barnett-Cowan M, Bartmess E, Beer J, Bell R, Bentley H, Beyan L, Binion G, Borsboom D, Bosch A, Bosco FA, Bowman SD, Brandt MJ, Braswell E, Brohmer H, Brown BT, Brown K, Bruning J, Calhoun-Sauls A, Callahan SP, Chagnon E, Chandler J, Chartier CR, Cheung F, Christopherson CD, Cillessen L, Clay R, Cleary H, Cloud MD, Cohn M, Cohoon J, Columbus S, Cordes A, Costantini G, Alvarez LDC, Cremata E, Crusius J, De Coster J, De Gaetano MA, Della Penna N, den Bezemer B, Deserno MK, Devitt O, Dewitte L, Dobolyi DG, Dodson GT, Donnellan MB, Donohue R, Dore RA, Dorrough A, Dreber A, Dugas M, Dunn EW, Easey K, Eboigbe S, Eggleston C, Embley J, Epskamp S, Errington TM, Estel V, Farach FJ, Feather J, Fedor A, Fernandez-Castilla B, Fiedler S, Field JG, Fitneva SA, Flagan T, Forest AL, Forsell E, Foster JD, Frank MC, Frazier RS, Fuchs H, Gable P, Galak J, Galliani EM, Gampa A, Garcia S, Gazarian D, Gilbert E, Giner-Sorolla R, Glockner A, Goellner L, Goh JX, Goldberg R, Goodbourn PT, Gordon-McKeon S, Gorges B, Gorges J, Goss J, Graham J, Grange JA, Gray J, Hartgerink C, Hartshorne J, Hasselman F, Hayes T, Heikensten E, Henninger F, Hodsoll J, Holubar T, Hoogendoorn G, Humphries DJ, Hung COY, Immelman N, Irsik VC, Jahn G, Jakel F, Jekel M, Johannesson M, Johnson LG, Johnson DJ, Johnson KM, Johnston WJ, Jonas K, Joy-Gaba JA, Kappes HB, Kelso K, Kidwell MC, Kim SK, Kirkhart M, Kleinberg B, Knezevic G, Kolorz FM, Kossakowski JJ, Krause RW, Krijnen J, Kuhlmann T, Kunkels YK, Kyc MM, Lai CK, Laique A, Lakens D, Lane KA, Lassetter B, Lazarevic LB, EP LB, Lee KJ, Lee M, Lemm K, Levitan CA, Lewis M, Lin L, Lin S, Lippold M, Loureiro D, Luteijn I, Mackinnon S, Mainard HN, Marigold DC, Martin DP, Martinez T, Masicampo EJ, Matacotta J, Mathur M, May M, Mechin N, Mehta P, Meixner J, Melinger A, Miller JK, Miller M, Moore K, Moschl M, Motyl M, Muller SM, Munafo M, Neijenhuijs KI, Nervi T, Nicolas G, Nilsonne G, Nosek BA, Nuijten MB, Olsson C, Osborne C, Ostkamp L, Pavel M, Penton-Voak IS, Perna O, Pernet C, Perugini M, Pipitone RN, Pitts M, Plessow F, Prenoveau JM, Rahal RM, Ratliff KA, Reinhard D, Renkewitz F, Ricker AA, Rigney A, Rivers AM, Roebke M, Rutchick AM, Ryan RS, Sahin O, Saide A, Sandstrom GM, Santos D, Saxe R, Schlegelmilch R, Schmidt K, Scholz S, Seibel L, Selterman DF, Shaki S, Simpson WB, Sinclair HC, Skorinko JLM, Slowik A, Snyder JS, Soderberg C, Sonnleitner C, Spencer N, Spies JR, Steegen S, Stieger S, Strohminger N, Sullivan GB, Talhelm T, Tapia M, te Dorsthorst A, Thomae M, Thomas SL, Tio P, Traets F, Tsang S, Tuerlinckx F, Turchan P, Valasek M, van ‘t Veer AE, Van Aert R, van Assen M, van Bork R, van de Ven M, van den Bergh D, van der Hulst M, van Dooren R, van Doorn J, van Renswoude DR, van Rijn H, Vanpaemel W, Echeverria AV, Vazquez M, Velez N, Vermue M, Verschoor M, Vianello M, Voracek M, Vuu G, Wagenmakers EJ, Weerdmeester J, Welsh A, Westgate EC, Wissink J, Wood M, Woods A, Wright E, Wu S, Zeelenberg M, Zuni K, Collaboration OS (2015) Estimating the reproducibility of psychological science. Science 349(6251):aac4716. https://doi.org/10.1126/science.aac4716. ARTN aac4716
Prinz F, Schlange T, Asadullah K (2011) Believe it or not: how much can we rely on published data on potential drug targets? Nat Rev Drug Discov 10(9):712. https://doi.org/10.1038/nrd3439-c1
Boltze J, Ayata C, Wagner DC, Plesnila N (2014) Preclinical phase III trials in translational stroke research: call for collective design of framework and guidelines. Stroke 45(2):357. https://doi.org/10.1161/STROKEAHA.113.004148
Macleod MR, O’Collins T, Howells DW, Donnan GA (2004) Pooling of animal experimental data reveals influence of study design and publication bias. Stroke 35(5):1203–1208. https://doi.org/10.1161/01.STR.0000125719.25853.20
Sena ES, Currie GL, McCann SK, Macleod MR, Howells DW (2014) Systematic reviews and meta-analysis of preclinical studies: why perform them and how to appraise them critically. J Cereb Blood Flow Metab 34(5):737–742. https://doi.org/10.1038/jcbfm.2014.28
Vesterinen HM, Sena ES, Egan KJ, Hirst TC, Churolov L, Currie GL, Antonic A, Howells DW, Macleod MR (2014) Meta-analysis of data from animal studies: a practical guide. J Neurosci Methods 221:92–102. https://doi.org/10.1016/j.jneumeth.2013.09.010
Hooijmans CR, IntHout J, Ritskes-Hoitinga M, Rovers MM (2014) Meta-analyses of animal studies: an introduction of a valuable instrument to further improve healthcare. ILAR J 55(3):418–426. https://doi.org/10.1093/ilar/ilu042
Normand SL (1999) Meta-analysis: formulating, evaluating, combining, and reporting. Stat Med 18(3):321–359
Esterhuizen TM, Thabane L (2016) Con: meta-analysis: some key limitations and potential solutions. Nephrol Dial Transplant 31(6):882–885. https://doi.org/10.1093/ndt/gfw092
Zoccali C (2016) Moderator’s view: meta-analysis: the best knowledge but not always shining gold. Nephrol Dial Transplant 31(6):886–889. https://doi.org/10.1093/ndt/gfw093
Llovera G, Hofmann K, Roth S, Salas-Perdomo A, Ferrer-Ferrer M, Perego C, Zanier ER, Mamrak U, Rex A, Party H, Agin V, Fauchon C, Orset C, Haelewyn B, De Simoni MG, Dirnagl U, Grittner U, Planas AM, Plesnila N, Vivien D, Liesz A (2015) Results of a preclinical randomized controlled multicenter trial (pRCT): anti-CD49d treatment for acute brain ischemia. Sci Transl Med 7(299):299ra121. https://doi.org/10.1126/scitranslmed.aaa9853. ARTN 299ra121
Voelkl B, Vogt L, Sena ES, Wurbel H (2018) Reproducibility of preclinical animal research improves with heterogeneity of study samples. PLoS Biol 16(2):e2003693. https://doi.org/10.1371/journal.pbio.2003693
Freedman LP, Cockburn IM, Simcoe TS (2015) The economics of reproducibility in preclinical research. PLoS Biol 13(6):e1002165. https://doi.org/10.1371/journal.pbio.1002165
Moher D, Avey M, Antes G, Altman DG (2015) The National Institutes of Health and guidance for reporting preclinical research. BMC Med 13:34. https://doi.org/10.1186/s12916-015-0284-9
Hsieh T, Vaickus MH, Remick DG (2018) Enhancing scientific foundations to ensure reproducibility: a new paradigm. Am J Pathol 188(1):6–10. https://doi.org/10.1016/j.ajpath.2017.08.028
Goodman SN, Fanelli D, Ioannidis JP (2016) What does research reproducibility mean? Sci Transl Med 8(341):341ps312. https://doi.org/10.1126/scitranslmed.aaf5027
Wieschowski S, Chin WWL, Federico C, Sievers S, Kimmelman J, Strech D (2018) Preclinical efficacy studies in investigator brochures: do they enable risk-benefit assessment? PLoS Biol 16(4):e2004879. https://doi.org/10.1371/journal.pbio.2004879
Jarvis MF, Williams M (2016) Irreproducibility in preclinical biomedical research: perceptions, uncertainties, and knowledge gaps. Trends Pharmacol Sci 37(4):290–302. https://doi.org/10.1016/j.tips.2015.12.001
Han S, Olonisakin TF, Pribis JP, Zupetic J, Yoon JH, Holleran KM, Jeong K, Shaikh N, Rubio DM, Lee JS (2017) A checklist is associated with increased quality of reporting preclinical biomedical research: a systematic review. PLoS One 12(9):e0183591. https://doi.org/10.1371/journal.pone.0183591
Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8(6):e1000412. https://doi.org/10.1371/journal.pbio.1000412
Ramirez FD, Motazedian P, Jung RG, Di Santo P, MacDonald ZD, Moreland R, Simard T, Clancy AA, Russo JJ, Welch VA, Wells GA, Hibbert B (2017) Methodological rigor in preclinical cardiovascular studies: targets to enhance reproducibility and promote research translation. Circ Res 120(12):1916–1926. https://doi.org/10.1161/CIRCRESAHA.117.310628
Gerdes AM (2015) How to improve the overall quality of cardiac morphometric data. Am J Physiol Heart Circ Physiol 309(1):H9–H14. https://doi.org/10.1152/ajpheart.00232.2015
Burgoon LD (2006) The need for standards, not guidelines, in biological data reporting and sharing. Nat Biotechnol 24(11):1369–1373. https://doi.org/10.1038/nbt1106-1369
Deutsch EW, Ball CA, Berman JJ, Bova GS, Brazma A, Bumgarner RE, Campbell D, Causton HC, Christiansen JH, Daian F, Dauga D, Davidson DR, Gimenez G, Goo YA, Grimmond S, Henrich T, Herrmann BG, Johnson MH, Korb M, Mills JC, Oudes AJ, Parkinson HE, Pascal LE, Pollet N, Quackenbush J, Ramialison M, Ringwald M, Salgado D, Sansone SA, Sherlock G, Stoeckert CJ Jr, Swedlow J, Taylor RC, Walashek L, Warford A, Wilkinson DG, Zhou Y, Zon LI, Liu AY, True LD (2008) Minimum information specification for in situ hybridization and immunohistochemistry experiments (MISFISHIE). Nat Biotechnol 26(3):305–312. https://doi.org/10.1038/nbt1391
Taylor CF, Field D, Sansone SA, Aerts J, Apweiler R, Ashburner M, Ball CA, Binz PA, Bogue M, Booth T, Brazma A, Brinkman RR, Michael Clark A, Deutsch EW, Fiehn O, Fostel J, Ghazal P, Gibson F, Gray T, Grimes G, Hancock JM, Hardy NW, Hermjakob H, Julian RK Jr, Kane M, Kettner C, Kinsinger C, Kolker E, Kuiper M, Le Novere N, Leebens-Mack J, Lewis SE, Lord P, Mallon AM, Marthandan N, Masuya H, McNally R, Mehrle A, Morrison N, Orchard S, Quackenbush J, Reecy JM, Robertson DG, Rocca-Serra P, Rodriguez H, Rosenfelder H, Santoyo-Lopez J, Scheuermann RH, Schober D, Smith B, Snape J, Stoeckert CJ Jr, Tipton K, Sterk P, Untergasser A, Vandesompele J, Wiemann S (2008) Promoting coherent minimum reporting guidelines for biological and biomedical investigations: the MIBBI project. Nat Biotechnol 26(8):889–896. https://doi.org/10.1038/nbt.1411
Zeiss CJ, Allore HG, Beck AP (2017) Established patterns of animal study design undermine translation of disease-modifying therapies for Parkinson’s disease. PLoS One 12(2):e0171790. https://doi.org/10.1371/journal.pone.0171790. ARTN e0171790
Bonne G, Rivier F, Hamroun D (2017) The 2018 version of the gene table of monogenic neuromuscular disorders (nuclear genome). Neuromuscul Disord 27(12):1152–1183. https://doi.org/10.1016/j.nmd.2017.10.005
Acknowledgment
Muscle gene therapy research in the Duan lab is currently supported by the National Institutes of Health (NS-90634, AR-70571, AR-69085), the Department of Defense (MD150133), Jesse’s Journey: The Foundation for Gene and Cell Therapy, Hope for Javier, Jackson Freel DMD Research Fund, Parent Project Muscular Dystrophy, and Solid Biosciences. The author thanks the Duan lab members for helpful discussion. The author thanks Drs. Jianguo (Tony) Sun and Gang (Gary) Yao for their helpful advices on the statistics section (Sect. 17.3.5). The author thanks Emily Million and John D’Alessandro for the help with proofreading the manuscript.
Disclosure
The author is a member of the scientific advisory board for Solid Biosciences and an equity holder of Solid Biosciences. The Duan lab has received research support from Solid Biosciences.
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Duan, D. (2019). Considerations on Preclinical Neuromuscular Disease Gene Therapy Studies. In: Duan, D., Mendell, J. (eds) Muscle Gene Therapy. Springer, Cham. https://doi.org/10.1007/978-3-030-03095-7_17
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