Gene therapy for muscular dystrophy – a review ofpromising progress

Bibliography

• ERVASTI JM, CAMPBELL KP: A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. Cell Biol. (1993) 122:809–823.
   PubMed Web of Science ®Google Scholar
• PETROF BJ, SHRAGERJB, STEDMAN HH, KELLY AM, SWEENEY HL: Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA (1993) 90:3710–3714.
   PubMed Web of Science ®Google Scholar
• HOFFMAN EP, BROWN RH JR, KUNKEL LM: Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell (1987) 51:919–928.
   PubMed Web of Science ®Google Scholar
• BRENMAN JE, CHAO DS, XIA H, ALDAPE K, BREDT DS: Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell (1995) 82:743–752.
   PubMed Web of Science ®Google Scholar
• BIES RD, PHELPS SF, CORTEZ MD, ROBERTS R, CASKEY CT, CHAMBERLAIN JS: Human and murine dystrophin mRNA transcripts are differentially expressed during skeletal muscle, heart, and brain development. Nucleic Acids Res. (1992) 20:1725–1731.
   PubMed Web of Science ®Google Scholar
• CHAMBERLAIN JS, BARJOT C, SCOTT J: Packaging cell lines for generating replication-defective and gutted adenoviral vectors. Methods Mol. Med. (2003) 76:153–166.
   PubMedGoogle Scholar
• EMERY AEH: Duchenne Muscular Dystrophy vol #24, Oxford Medical Publications, Oxford (1993).
   Google Scholar
• KAPSA R, QUIGLEY A, LYNCH GS et al: In vivo and M vitro correction of the mdx dystrophin gene nonsense mutation by short-fragment homologous replacement. Hum. Gene Ther. (2001) 12:629–642.
   PubMed Web of Science ®Google Scholar
• BERTONI C, RANDO TA: Dystrophin gene repair in mdx muscle precursor cells M vitro and in vivo mediated by RNA-DNA chimeric oligonucleotides. Hum. Gene The]: (2002) 13:707–718.
   PubMed Web of Science ®Google Scholar
• •Impressive demonstration of the ability to genetically correct a mutation in muscle that leads to DMD.
   Google Scholar
• MANN CJ, HONEYMAN K, MCCLOREY G, FLETCHER S, WILTON SD: Improved antisense oligonucleotide induced exon skipping in the Indx mouse model of muscular dystrophy. Gene Med. (2002) 4:644–654.
   Web of Science ®Google Scholar
• BARTLETT RJ, STOCKINGER S, DENIS MM et al.: In vivotargeted repair of a point mutation in the canine dystrophin gene by a chimeric RNA/DNA oligonucleotide. Nat. Biotechnol. (2000) 18:615–622.
   PubMed Web of Science ®Google Scholar
• •The first demonstration that a MD-causing mutation could be corrected inside of a cell.
   Google Scholar
• AARTSMA-RUS A, JANSON AA, KAMAN WE et al.: Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Hum. Mol. Genet. (2003) 12:907–914.
   PubMed Web of Science ®Google Scholar
• COX GA, COLE NM, MATSUMURA K et al.: Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity. Nature (1993) 364:725–729.
   PubMed Web of Science ®Google Scholar
• LOVE DR, FLINT TJ, MARSDEN RF et al.: Characterization of deletions in the dystrophin gene giving mild phenotypes. Am. J. Med. Genet. (1990) 37:136–142.
   PubMed Web of Science ®Google Scholar
• PHELPS SF, HAUSER MA, COLE NM et al.: Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum. Mol. Genet. (1995) 4:1251–1258.
   PubMed Web of Science ®Google Scholar
• CRAWFORD GE, FAULKNER JA, CROSBIE RH, CAMPBELL KP, FROEHNER SC, CHAMBERLAIN JS: Assembly of the dystrophin-associated protein complex does not require thedystrophin COOH-terminal domain. J. Cell Biol. (2000) 150:1399–1410.
   PubMed Web of Science ®Google Scholar
• HARPER SQ, HAUSER MA,DELLORUSSO C et al.: Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat. Med. (2002) 8:253–261.
   Google Scholar
• ••Detailed analysis of the structure andfunction of the dystrophin protein, which led to the development of optimised micro-dystrophin genes. This work also used AAV vectors to deliver micro-dystrophins to muscles of an animal model for DMD, showing for the first time that a dystrophic pathology could be reversed after it had developed.
   Google Scholar
• SAKAMOTO M, YUASA K,YOSHIMURA M et al: Micro-dystrophin cDNA ameliorates dystrophic phenotypes when introduced into mdx mice as a transgene. Biochem. Biophys. Res. Commun. (2002) 293:1265–1272.
   PubMed Web of Science ®Google Scholar
• WATCHKO J, O& DAY T, WANG B et al.: Adeno-associated virus vector-mediated minidystrophin gene therapy improves dystrophic muscle contractile function in mdx mice. Hum. Gene Ther. (2002) 13:1451–1460.
   Google Scholar
• •This manuscript showed that micro-dystrophins could correct many of the functional deficits in dystrophic muscle following AAV vector delivery to mdx mice.
   Google Scholar
• MATSUMURA K, ERVASTI JM, OHLENDIECK K, KAHL SD, CAMPBELL KP: Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature (1992) 360:588–591.
   PubMed Web of Science ®Google Scholar
• TINSLEY JM, POTTER AC, PHELPS SR, FISHER R, TRICKETT JI, DAVIES KE: Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature (1996) 384:349–353.
   PubMed Web of Science ®Google Scholar
• ••Transgenic nnixmice were shown to displayan almost complete absence of dystrophic pathology when they expressed moderate levels of a mini-utrophin. This work provides the best evidence to date supporting the concept of using utrophin to compensate for dystrophin gene mutations.
   Google Scholar
• DECONINCK N, TINSLEY J, DE BACKER F et al.: Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat. A1d. (1997) 3:1216–1221.
   Google Scholar
• PERKINS KJ, BURTON EA, DAVIES KE: The role of basal and myogenic factors in the transcriptional activation of utrophin promoter A: implications for therapeutic up-regulation in Duchenne muscular dystrophy. Nucleic Acids Res. (2001) 29:4843–4850.
   PubMed Web of Science ®Google Scholar
• HAUSER MA, ROBINSON A, HARTIGAN-O'CONNOR D et al: Analysis of muscle creatine kinase regulatory elements in recombinant adenoviral vectors.Ther. (2000) 2:16–25.
   Google Scholar
• WOLFF JA, MALONE RW, WILLIAMS P et al.: Direct gene transfer into mouse muscle in vivo. Science (1990) 247:1465–1468.
   PubMed Web of Science ®Google Scholar
• LU QL, BOU-GHARIOS G,PARTRIDGE TA: Non-viral gene delivery in skeletal muscle: a protein factory. Gene Ther. (2003) 10:131–142.
   PubMed Web of Science ®Google Scholar
• •A wide ranging and thorough review of the approaches being taken to develop non-viral methods for gene therapy of the muscular dystrophies.
   Google Scholar
• TRIVEDI RA, DICKSON G: Liposome-mediated gene transfer into normal and dystrophin-deficient mouse myoblasts. Neurochem. (1995) 64:2230–2238.
   PubMed Web of Science ®Google Scholar
• CAMPEAU P, CHAPDELAINE P, SEIGNEURIN-VENIN S, MASSIE B, TREMBLAY JP: Translection of large plasmids in primary human myoblasts. Gene Ther: (2001) 8:1387–1394.
   PubMed Web of Science ®Google Scholar
• VILQUIN JT, KENNEL PF, PATURNEAU-JOUAS M et al.: Electrotransfer of naked DNA in the skeletal muscles of animal models of muscular dystrophies. Gene Ther. (2001) 8:1097–1107.
   PubMed Web of Science ®Google Scholar
• WELLS DJ: Improved gene transfer by direct plasmid injection associated with regeneration in mouse skeletal muscle. FEBS Lett. (1993) 332:179–182.
   PubMed Web of Science ®Google Scholar
• ZELENIN AV, KOLESNIKOV VA, TARASENKO OA et al.: Bacterial beta-galactosidase and human dystrophin genesare expressed in mouse skeletal muscle fibersafter ballistic transfection. FEBS Lett. (1997) 414:319–322.
   PubMed Web of Science ®Google Scholar
• ZHANG G, BUDKERV, WILLIAMSP, SUBBOTIN V, WOLFF JA: Efficient expression of naked DNA delivered intraarterially to limb muscles of nonhuman primates. Hum. Gene Ther: (2001) 12:427–438.
   PubMed Web of Science ®Google Scholar
• ••An impressive level of gene transfer wasobtained in muscles of non-human primates without using viral vectors. This study provides clues as to how systemic delivery of transgenes to muscle might be obtained.
   Google Scholar
• MURAKAMI T, NISHI T, KIMURA E et al.: Full-length dystrophin cDNA transfer into skeletal muscle of adult mdx mice by electroporation. Muscle Nerve (2003) 27:237–241.
   PubMed Web of Science ®Google Scholar
• MAH C, FRAITES TJ JR,ZOLOTUKHIN I et al.: Improved method of recombinant AAV2 delivery for systemic targeted gene therapy. Mol Ther: (2002) 6:106–112.
   Google Scholar
• VOLPERS C, THIRION C,BIERMANN V et al.: Antibody-mediated targeting of an adenovirus vector modified to contain a synthetic immunoglobulin g-binding domain in the capsid.J. Virol (2003) 77:2093–2104.
   Google Scholar
• DEAS O, ANGEVIN E,CHERBONNIER C et al.: In vivo-targeted gene delivery using antibody-based nonviral vector. Hum. Gene Ther. (2002) 13:1101–1114.
   PubMed Web of Science ®Google Scholar
• MACCOLL G, BUNN C,GOLDSPINK G, BOULOUX P, GORECKI DC: Intramuscular plasmid DNA injection can accelerate autoimmune responses. Gene Ther. (2001) 8:1354–1356.
   PubMed Web of Science ®Google Scholar
• AMALFITANO A, HAUSER MA, HU H, SERRA D, BEGY CR,CHAMBERLAIN JS: Production and characterization of improved adenovirus vectors with the El, E2b, and E3 genes deleted. Virol (1998) 72:926–933.
   Web of Science ®Google Scholar
• DELLORUSSO C, SCOTT JM, HARTIGAN-O'CONNOR D et al: Functional correction of adult mdx mouse muscle using gutted adenoviral vectors expressing full-length dystrophin. Proc. Natl. Acad. Sci. USA (2002) 99:12979–12984.
   PubMed Web of Science ®Google Scholar
• ••This study showed that gutted adenoviralvectors could achieve widespread delivery of full-length dystrophin to muscles of old and young mice, and that functionaldeficits resulting from MD could be at least partially reversed even in older, dystrophic muscles.
   Google Scholar
• SCOTT JM, CHAMBERLAIN JS: Gutted adenoviral vectors for gene transfer to muscle. Methods Mol Biol. (2003) 219:19–28.
   PubMedGoogle Scholar
• BOGDANOVICH S, KRAG TO, BARTON ER et al.: Functional improvement of dystrophic muscle by myostatin blockade. Nature (2002) 420:418–421.
   PubMed Web of Science ®Google Scholar
• ••These authors showed that neutralisingantibodies against myostatin could be used to induce muscle hypertrophy in mdx mouse muscles, leading to a significant improvement in the dystrophic pathology. This works represents the most impressive improvement in muscle function obtained by a non-genetic approach. Myostatin blockage could presumably also be obtained by genetic approaches.
   Google Scholar
• BARTON ER, MORRIS L, MUSARO A, ROSENTHAL N, SWEENEY HL: Muscle-specific expression of insulin-like growth Factor I counters muscle decline in mdxmice.j Cell Biol. (2002) 157:137–148.
   PubMed Web of Science ®Google Scholar
• •IGF-1 induces muscle hypertrophy and enhances regeneration of damaged muscle. This study showed that IGF-1 expression in transgenic mice on the nada-background leads to muscle hypertrophy that resulted in improved muscle function.
   Google Scholar
• JIANG Z, FEINGOLD E,KOCHANEK S, CLEMENS PR: Systemic delivery of a high-capacity adenoviral vector expressing mouse CTLA4Ig improves skeletal muscle gene therapy. Mol Ther: (2002) 6:369–376.
   PubMed Web of Science ®Google Scholar
• •This study demonstrated the potential for blocking irmrtune responses to gene therapy vectors in muscle by co-delivery of both a therapeutic transgene and an immunomodulatory transgene. Such a delivery was only possible by using gutted adenoviral vectors with an enormous cloning capacity.
   Google Scholar
• ROBERTS ML, WELLS DJ,GRAHAM IR et al: Stable micro-dystrophin gene transfer using an integrating adeno-retroviral hybrid vector ameliorates the dystrophic pathology in mdx mouse muscle. Hum. Mol Genet. (2002) 11:1719–1730.
   PubMed Web of Science ®Google Scholar
• YANT SR, EHRHARDT A,MIKKELSEN JG, MEUSE L, PHAM T, KAY MA: Transposition from a gutless adeno-transposon vector stabilizes transgene expression in vivo. Nat. Biotechnol (2002) 20:999–1005.
   PubMed Web of Science ®Google Scholar
• HARTIGAN O CONNOR D, BARJOT C, SALVATORI G, CHAMBERLAIN JS: Generation and growth of gutted adenoviral vectors. Methods Enzymol (2002) 346:224–246.
   PubMed Web of Science ®Google Scholar
• FLOTTE TR, CARTER BJ: Adeno-associated virus vectors for gene therapy. Gene Ther. (1995) 2:357–362.
   PubMed Web of Science ®Google Scholar
• YUASA K, SAKAMOTO M, MIYAGOE-SUZUKI Y et al: Adeno-associated virus vector-mediated gene transfer into dystrophin-deficient skeletal muscles evokes enhanced immune response against the transgene product. Gene Ther. (2002) 9:1576–1588.
   PubMed Web of Science ®Google Scholar
• XIAO X, LI J, SAMULSKI RJ: Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector.Virol. (1996)70:8098–8108.
   Web of Science ®Google Scholar
• RABINOWITZ JE, ROLLING F, LI C et al.: Cross-packaging of a single adeno-associated virus (AAV) Type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity.Viral. (2002) 76:791–801.
   PubMed Web of Science ®Google Scholar
• XIAO W, CHIRMULE N, BERTA SC, MCCULLOUGH B, GAO G,WILSON JM: Gene therapy vectors based on adeno-associated virus Type 1. J. Vim/. (1999) 73:3994–4003.
   Web of Science ®Google Scholar
• RUTLEDGE EA, HALBERT CL, RUSSELL DW: Infectious clones and vectors derived from adeno-associated virus (AAV) serotypes other than AAV Type 2.Viral. (1998) 72:309–319.
   PubMed Web of Science ®Google Scholar
• SCOTT JM, LI S, HARPER SQ et al: Viral vectors for gene transfer of micro-, mini-, or full-length dystrophin. Net/Form/sr& Disord. (2002) 12\(Suppl. 1):523–529.
   Google Scholar
• GAO GP, ALVIRA MR, WANG L, CALCEDO R, JOHNSTON J, WILSON JM: Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Nati Acad. Sri. USA (2002) 99:11854–11859.
   PubMed Web of Science ®Google Scholar
• DUAN D, YUE Y, ENGELHARDT JF: Dual vector expansion of the recombinant AAV packaging capacity. Methods Ma Biol. (2003) 219:29–51.
   PubMedGoogle Scholar
• DUAN D, YUE Y, YAN Z,ENGELHARDT JF: A new dual-vector approach to enhance recombinant adeno-associated virus-mediated gene expressionthrough intermolecular cis activation. Nat. Med. (2000) 6:595–598.
   PubMed Web of Science ®Google Scholar
• ••An impressive demonstration of the abilityto deliver gene expression cassettes that exceed the cloning capacity of AAV vectors by taking advantage of the concatamerisation of AAV genomes after cell transduction in order to achieve trans-splicing between, and joining of, the two halves of an expression cassette.
   Google Scholar
• STEDMAN H, WILSON JM, FINKE R, KLECKNER AL, MENDELL J: Phase I clinical trial utilizing gene therapy for limb girdle muscular dystrophy: alpha-, beta-, gamma-, or delta-sarcoglycan gene delivered with intramuscular instillations of adeno-associated vectors. Hum. Gene The]: (2000) 11:777–790.
   PubMedGoogle Scholar
• FASSATI A, SERPENTE P, WELLS DJ, WALSH FS, DICKSON G: Retroviral-mediated gene transfer into murine and human skeletal muscle for the correction of dystrophin deficiency. Biochem. Soc. Trans. (1996) 24:275S.
   PubMedGoogle Scholar
• SEPPEN J, BARRY SC, HARDER B, OSBORNE WR: Lentivirus administration to rat muscle provides efficient sustained expression of erythropoietin. Blood (2001) 98:594–596.
   PubMed Web of Science ®Google Scholar
• SAKODA T, KASAHARA N,HAMAMORI Y, KEDES L: A high-titer lentiviral production system mediates efficient transduction of differentiated cells including beating cardiac myocytes." MM. Cell Cardiol (1999) 31:2037–2047.
   PubMed Web of Science ®Google Scholar
• KANG Y, STEIN CS, HETH JA et al: In vivo gene transfer using a nonprimate lentiviral vector pseudotyped with Ross River Virus glycoproteins.J. Virol (2002) 76:9378–9388.
   PubMed Web of Science ®Google Scholar
• KAFRI T, BLOMER U, PETERSON DA, GAGE FH, VERMA IM: Sustained expression of genes delivered directly into liver and muscle by lentiviral vectors. Nat. Genet. (1997) 17:314–317.
   PubMed Web of Science ®Google Scholar
• MACKENZIE TC, KOBINGER GP, KOOTSTRA NA et al: Efficient transduction of liver and muscle after in utero injection of lentiviral vectors with different pseudotypes. MM. Ther. (2002) 6:349–358.
   PubMed Web of Science ®Google Scholar
• •A detailed study of the ability to modify the tropism of lentiviral vectors, which was used to obtain permanent delivery of expression cassettes to muscle and liver. This study suggests a potential route to therapy of MDs that would involve gene transfer in utero.
   Google Scholar
• BONCI D, CITTADINI A, LATRONICO MV et al.: 'Advanced' generation lentiviruses as efficient vectors for cardiomyocyte gene transduction M vitro and M vivo. Gene Ther. (2003) 10:630–636.
   PubMed Web of Science ®Google Scholar
• TROBRIDGE G, VASSILOPOULOS G, JOSEPHSON N, RUSSELL DW: Gene transfer with foamy virus vectors. Methods Enzymol. (2002) 346:628–648.
   PubMed Web of Science ®Google Scholar
• EMERY DW, YANNAKI E, TUBB J, NISHINO T, LI Q, STAMATOYANNOPOULOS G: Development of virus vectors for gene therapy of beta chain hemoglobinopathies: flanking with a chromatin insulator reduces gamma-globin gene silencing in vivo. Blood (2002) 100:2012–2019.
   PubMed Web of Science ®Google Scholar
• HEISTER T, HEID I, ACKERMANN M, FRAEFEL C: Herpes simplex virusType 1/ adeno-associated virus hybrid vectors mediate site-specific integration at the adeno-associated virus preintegration site, AAVS1, on human chromosome 19.Virol (2002) 76:7163–7173.
   Web of Science ®Google Scholar
• WANG Y, CAMP SM, NIWANO M et al.: Herpes simplex virusType l/adeno-associated virus rep(+) hybrid amplicon vector improves the stability of transgene expression in human cells by site-specificintegration.Virol (2002) 76:7150–7162.
   Web of Science ®Google Scholar
• GREELISH JP, SU LT, LANKFORD EB et al.: Stable restoration of the sarcoglycan complex in dystrophic muscle perfused with histamine and a recombinant adeno-associated viral vector. Nat. Med. (1999) 5:439–443.
   PubMed Web of Science ®Google Scholar
• ••The most dramatic example to date of thepotential to achieve systemic delivery of a viral vector to widely dispersed muscles throughout the body. The method was used to obtain an impressive amelioration of pathology in a hamster model for limb-girdle MD and provided additional clues to the nature of the pathology.
   Google Scholar
• CHO WK, EBIHARA S,NALBANTOGLU J et al.: Modulation of Starling forces and muscle fiber maturity permits adenovirus-mediated gene transfer to adult dystrophic (oath) mice by the intravascular route. Hum. Gene Ther. (2000) 11:701–714.
   Google Scholar
• CARLSON BM, FAULKNER JA: The regeneration of skeletal muscle fibers following injury: a review. Med. Sci. Sports Exerc. (1983) 15:187–198.
   PubMed Web of Science ®Google Scholar
• KARPATI G, POULIOT Y, ZUBRZYCKA-GAARN E et al.: Dystrophin is expressed in mdxskeletal muscle fibers after normal myoblast implantation. Am. J. Pathol (1989) 135:27–32.
   PubMed Web of Science ®Google Scholar
• PARTRIDGE TA, MORGAN JE, COULTON GR, HOFFMAN EP, KUNKEL LM: Conversion of mdx myofibres from dystrophin-negative to - positive by injection of normal myoblasts. Nature (1989) 337:176–179.
   PubMed Web of Science ®Google Scholar
• MOISSET PA, GAGNON Y, KARPATI G, TREMBLAY JP: Expression of human dystrophin following the transplantation of genetically modified mdx myoblasts.Gene Ther: (1998) 5:1340–1346.
   PubMed Web of Science ®Google Scholar
• FLOYD SS JR, CLEMENS PR, ONTELL MR et al.: Ex vivo gene transfer using adenovirus-mediated full-length dystrophin delivery to dystrophic muscles. Gene Ther: (1998) 5:19–30.
   PubMed Web of Science ®Google Scholar
• PARTRIDGE T: Myoblast transplantation. Neuromusad. Disord. (2002) 12\(Suppl. 1):53–56.
   Google Scholar
• HODGETTS SI, SPENCER MJ, GROUNDS MD: A role for natural killer cells in the rapid death of cultured donor myoblasts after transplantation. Transplantation (2003) 75:863–871.
   PubMed Web of Science ®Google Scholar
• HODGETTS SI, BEILHARZ MW, SCALZO AA, GROUNDS MD: Why do cultured transplanted myoblasts die in vivo? DNA quantification shows enhanced survival of donor male myoblasts in host mice depleted of CD4+ and CD8+ cells or Nk1.1+ cells. Cell Transplant. (2000) 9:489–502.
   PubMed Web of Science ®Google Scholar
• WEBSTER C, BLAU HM: Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat. Cell Ma Genet. (1990) 16:557–565.
   PubMedGoogle Scholar
• LATTANZI L, SALVATORI G, COLETTA M et al.: High efficiency myogenic conversion of human fibroblasts by adenoviral vector-mediated MyoD gene transfer. An alternative strategy for ex vivo gene therapy of primary myopathies.Clin. Invest. (1998) 101:2119–2128.
   Google Scholar
• FASSATI A, WELLS DJ, SGROSERPENTE PA et al.: Genetic correction of dystrophin deficiency and skeletal muscle remodeling in adult mdx mouse via transplantation of retroviral producer cells.Clin. Invest. (1997) 100:620–628.
   Google Scholar
• HUARD C, MOISSET PA, DICAIRE A et al.: Transplantation of dermal fibroblasts expressing MyoD1 in mouse muscles. Biochem. Biophys. Res. Commun. (1998) 248:648–654.
   PubMed Web of Science ®Google Scholar
• MINASI MG, RIMINUCCI M,DE ANGELIS L et al.: The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development (2002) 129:2773–2783.
   Google Scholar
• QU-PETERSEN Z, DEASY B, JANKOWSKI R et al.: Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J. Cell Biol. (2002) 157:851–864.
   PubMed Web of Science ®Google Scholar
• DE BARI C, DELL'ACCIO F,VANDENABEELE F, VERMEESCH JR, RAYMACKERSJM, LUYTEN FP: Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J. Cell Biol. (2003) 160:909–918.
   PubMed Web of Science ®Google Scholar
• ZUK PA, ZHU M, ASHJIAN P et al: Human adipose tissue is a source of multipotent stem cells. Mo/. Biol. Cell (2002) 13:4279–4295.
   PubMed Web of Science ®Google Scholar
• ASAKURA A, SEALE P,GIRGIS-GABARDO A, RUDNICKI MA: Myogenic specification of side population cells in skeletal muscle. I Cell Biol. (2002) 159:123–134.
   Web of Science ®Google Scholar
• ••The most detailed and thoroughmanuscript on the relationship between muscle precursor cells and stem cells resident in haematopoietic and muscle tissues. This study introduces important concepts relevant to the development of ex vivo therapy for muscle diseases.
   Google Scholar
• TORRENTE Y, TREMBLAY JP, PISATI F et al.: Intraarterial injection of muscle-derived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. j. Cell Biol. (2001) 152:335–348.
   PubMed Web of Science ®Google Scholar
• GALLI R, BORELLO U, GRITTI A et al.: Skeletal myogenic potential of human and mouse neural stem cells. Nat. Neurosci. (2000) 3:986–991.
   PubMed Web of Science ®Google Scholar
• PARTRIDGE TA: Stem cell route to neuromuscular therapies. Muscle Nerve (2003) 27:133–141.
   PubMed Web of Science ®Google Scholar
• SMYTHE GM, GROUNDS MD: Exposure to tissue culture conditions can adversely affect myoblast behaviour in vivo in whole muscle grafts: implications for myoblast transfer therapy. Cell Transplant. (2000) 9:379–393.
   PubMed Web of Science ®Google Scholar
• SOMMER B, RINSCH C, PAYEN E et al: Long-term doxycycline-regulated secretion of erythropoietin by encapsulated myoblasts. Mol. Ther. (2002) 6:155–161.
   PubMed Web of Science ®Google Scholar