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Muscle Targeting

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Biobetters

Part of the book series: AAPS Advances in the Pharmaceutical Sciences Series ((AAPS,volume 19))

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Abstract

Pompe disease is caused by reduced or complete absence of functional acid α-glucosidase (GAA), an acid hydrolase that degrades glycogen to glucose in lysosomes. The clinical phenotype represents a continuum based on the extent of residual enzyme activity and is characterized by extensive glycogen accumulation in all tissues, but is most prominent in cardiac and skeletal muscle. Respiratory insufficiency is extremely common, and cardiorespiratory failure is the leading cause of death. Currently, the only FDA-approved treatment for Pompe disease is enzyme replacement therapy (ERT) involving bi-weekly intravenous infusion of recombinant human GAA (rhGAA). ERT improves the overall survival in the severe, infantile-onset form of the disease. Although the existing ERT is more effective in improving cardiomyopathy in these patients, it is not very effective in treating skeletal muscle damage and only delays the eventual requirement of these patients for ambulatory and ventilator support. This summary will review the recent developments aimed at improving the targeting of new and existing therapeutics to skeletal muscle to reduce the aberrant glycogen load and eliminate muscle damage.

This work was supported by National Institutes of Health grant R01DK042667

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References

  • Amalfitano A, Bengur AR, Morse RP, Majure JM, Case LE, Veerling DL, Mackey J, Kishnani P, Smith W, McVie-Wylie A, Sullivan JA, Hoganson GE, Phillips JA 3rd, Schaefer GB, Charrow J, Ware RE, Bossen EH, Chen YT (2001) Recombinant human acid alpha-glucosidase enzyme therapy for infantile glycogen storage disease type II: results of a phase I/II clinical trial. Genet Med 3:132–138

    CAS  PubMed  Google Scholar 

  • Ansar M, Serrano D, Papademetriou I, Bhowmick TK, Muro S (2013) Biological functionalization of drug delivery carriers to bypass size restrictions of receptor-mediated endocytosis independently from receptor targeting. ACS Nano 7:10597–10611

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ballou DL (1975) Genetic control of yeast mannan structure: mapping genes mnn2 and mnn4 in Saccharomyces cerevisiae. J Bacteriol 123:616–619

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bao M, Booth JL, Elmendorf BJ, Canfield WM (1996) Bovine UDP-N-acetylglucosamine:lysosomal-enzyme N-acetylglucosamine-1-phosphotransferase. I. Purification and subunit structure. J Biol Chem 271:31437–31445

    Article  CAS  PubMed  Google Scholar 

  • Bijvoet AG, Van Hirtum H, Kroos MA, van de Kamp EH, Schoneveld O, Visser P, Brakenhoff JP, Weggeman M, Van Corven EJ, van der Ploeg AT, Reuser AJ (1999) Human acid alpha-glucosidase from rabbit milk has therapeutic effect in mice with glycogen storage disease type II. Hum Mol Genet 8:2145–2153

    Article  CAS  PubMed  Google Scholar 

  • Bohnsack RN, Song X, Olson LJ, Kudo M, Gotschall RR, Canfield WM, Cummings RD, Smith DF, Dahms NM (2009) Cation-independent mannose 6-phosphate receptor: a composite of distinct phosphomannosyl binding sites. J Biol Chem 284:35215–35226

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brady RO (2006) Enzyme replacement for lysosomal diseases. Annu Rev Med 57:283–296

    Article  CAS  PubMed  Google Scholar 

  • Braulke T, Bonifacino JS (2009) Sorting of lysosomal proteins. Biochim Biophys Acta 1793:605–614

    Article  CAS  PubMed  Google Scholar 

  • Brown BI, Brown DH, Jeffrey PL (1970) Simultaneous absence of alpha-1,4-glucosidase and alpha-1,6-glucosidase activities (pH 4) in tissues of children with type II glycogen storage disease. Biochemistry 9:1423–1428

    Article  CAS  PubMed  Google Scholar 

  • Brown J, Esnouf RM, Jones MA, Linnell J, Harlos K, Hassan AB, Jones EY (2002) Structure of a functional IGF2R fragment determined from the anomalous scattering of sulfur. EMBO J 21:1054–1062

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brown J, Delaine C, Zaccheo OJ, Siebold C, Gilbert RJ, Van Boxel G, Denley A, Wallace JC, Hassan AB, Forbes BE, Jones EY (2008) Structure and functional analysis of the IGF-II/IGF2R interaction. EMBO J 27:265–276

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brown J, Jones EY, Forbes BE (2009) Keeping IGF-II under control: lessons from the IGF-II-IGF2R crystal structure. Trends Biochem Sci 34:612–619

    Article  CAS  PubMed  Google Scholar 

  • Byrne BJ, Falk DJ, Pacak CA, Nayak S, Herzog RW, Elder ME, Collins SW, Conlon TJ, Clement N, Cleaver BD, Cloutier DA, Porvasnik SL, Islam S, Elmallah MK, Martin A, Smith BK, Fuller DD, Lawson LA, Mah CS (2011) Pompe disease gene therapy. Hum Mol Genet 20:R61–R68

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cardone M, Porto C, Tarallo A, Vicinanza M, Rossi B, Polishchuk E, Donaudy F, Andria G, DE Matteis MA, Parenti G (2008) Abnormal mannose-6-phosphate receptor trafficking impairs recombinant alpha-glucosidase uptake in Pompe disease fibroblasts. Pathogenetics 1:6

    Article  PubMed Central  PubMed  Google Scholar 

  • Chavez CA, Bohnsack RN, Kudo M, Gotschall RR, Canfield WM, Dahms NM (2007) Domain 5 of the cation-independent mannose 6-phosphate receptor preferentially binds phosphodiesters (mannose 6-phosphate N-acetylglucosamine ester). Biochemistry 46:12604–12617

    Article  CAS  PubMed  Google Scholar 

  • Cori GT (1952) Glycogen structure and enzyme deficiencies in glycogen storage disease. Harvey Lect 48:145–171

    PubMed  Google Scholar 

  • Cuozzo JW, Tao K, Cygler M, Mort JS, Sahagian GG (1998) Lysine-based structure responsible for selective mannose phosphorylation of cathepsin D and cathepsin L defines a common structural motif for lysosomal enzyme targeting. J Biol Chem 273:21067–21076

    Article  CAS  PubMed  Google Scholar 

  • Distler JJ, Patel R, Jourdian GW (1987) Immobilization and assay of low-molecular-weight phosphomannosyl receptor in multiwell plates. Anal Biochem 166:65–71

    Article  CAS  PubMed  Google Scholar 

  • Distler JJ, Guo JF, Jourdian GW, Srivastava OP, Hindsgaul O (1991) The binding specificity of high and low molecular weight phosphomannosyl receptors from bovine testes. Inhibition studies with chemically synthesized 6-O-phosphorylated oligomannosides. J Biol Chem 266:21687–21692

    CAS  PubMed  Google Scholar 

  • Do H, Lee WS, Ghosh P, Hollowell T, Canfield W, Kornfeld S (2002) Human mannose 6-phosphate-uncovering enzyme is synthesized as a proenzyme that is activated by the endoprotease furin. J Biol Chem 277:29737–29744

    Article  CAS  PubMed  Google Scholar 

  • Farah BL, Madden L, Li S, Nance S, Bird A, Bursac N, Yen PM, Young SP, Koeberl DD (2014) Adjunctive beta2-agonist treatment reduces glycogen independently of receptor-mediated acid alpha-glucosidase uptake in the limb muscles of mice with Pompe disease. FASEB J 28(5):2272–2280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Funk B, Kessler U, Eisenmenger W, Hansmann A, Kolb HJ, Kiess W (1992) Expression of the insulin-like growth factor-II/mannose-6-phosphate receptor in multiple human tissues during fetal life and early infancy. J Clin Endocrinol Metab 75:424–431

    CAS  PubMed  Google Scholar 

  • Hagemans ML, Winkel LP, Hop WC, Reuser AJ, Van Doorn PA, van der Ploeg AT (2005a) Disease severity in children and adults with Pompe disease related to age and disease duration. Neurology 64:2139–2141

    Article  CAS  PubMed  Google Scholar 

  • Hagemans ML, Winkel LP, Van Doorn PA, Hop WJ, Loonen MC, Reuser AJ, van der Ploeg AT (2005b) Clinical manifestation and natural course of late-onset Pompe’s disease in 54 Dutch patients. Brain 128:671–677

    Article  CAS  PubMed  Google Scholar 

  • Hasilik A, Klein U, Waheed A, Strecker G, von Figura K (1980) Phosphorylated oligosaccharides in lysosomal enzymes: identification of alpha-N-acetylglucosamine(1)phospho(6)mannose diester groups. Proc Natl Acad Sci U S A 77:7074–7078

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hawes ML, Kennedy W, O’Callaghan MW, Thurberg BL (2007) Differential muscular glycogen clearance after enzyme replacement therapy in a mouse model of Pompe disease. Mol Genet Metab 91:343–351

    Article  CAS  PubMed  Google Scholar 

  • Hermans MM, Wisselaar HA, Kroos MA, Oostra BA, Reuser AJ (1993) Human lysosomal alpha-glucosidase: functional characterization of the glycosylation sites. Biochem J 289:681–686

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hers HG (1963) Alpha-glucosidase deficiency in generalized glycogen storage disease (Pompe’s disease). Biochem J 86:11–16

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hesselink RP, Wagenmakers AJ, Drost MR, van der Vusse GJ (2003) Lysosomal dysfunction in muscle with special reference to glycogen storage disease type II. Biochim Biophys Acta 1637:164–170

    Article  CAS  PubMed  Google Scholar 

  • Hirschhorn R, Reuser AJJ (2001) Glycogen storage disease type II: acid alpha-glucosidase (acid maltase) deficiency. In: Scriver CR, Beaudet al, Sly WS, Valle D (eds) The metabolic and molecular bases of inherited disease, 8th edn. McGraw-Hill, New York

    Google Scholar 

  • Hoflack B, Kornfeld S (1985) Lysosomal enzyme binding to mouse P388D1 macrophage membranes lacking the 215-kDa mannose 6-phosphate receptor: evidence for the existence of a second mannose 6-phosphate receptor. Proc Natl Acad Sci U S A 82:4428–4432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoflack B, Fujimoto K, Kornfeld S (1987) The interaction of phosphorylated oligosaccharides and lysosomal enzymes with bovine liver cation-dependent mannose 6-phosphate receptor. J Biol Chem 262:123–129

    CAS  PubMed  Google Scholar 

  • Holtzman E (1989) Lysosomes. Plenum, New York

    Book  Google Scholar 

  • Hsu J, Serrano D, Bhowmick T, Kumar K, Shen Y, Kuo YC, Garnacho C, Muro S (2011) Enhanced endothelial delivery and biochemical effects of alpha-galactosidase by ICAM-1-targeted nanocarriers for Fabry disease. J Control Release 149:323–331

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hsu J, Northrup L, Bhowmick T, Muro S (2012) Enhanced delivery of alpha-glucosidase for Pompe disease by ICAM-1-targeted nanocarriers: comparative performance of a strategy for three distinct lysosomal storage disorders. Nanomedicine 8:731–739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kan SH, Troitskaya LA, Sinow CS, Haitz K, Todd AK, di Stefano A, Le SQ, Dickson PI, Tippin BL (2013) Insulin-like growth factor II peptide fusion enables uptake and lysosomal delivery of alpha-N-acetylglucosaminidase to mucopolysaccharidosis type IIIB fibroblasts. Biochem J 458(2):281–289

    Article  Google Scholar 

  • Kim JJ, Olson LJ, Dahms NM (2009) Carbohydrate recognition by the mannose-6-phosphate receptors. Curr Opin Struct Biol 19:534–542

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kishnani PS, Nicolino M, Voit T, Rogers RC, Tsai AC, Waterson J, Herman GE, Amalfitano A, Thurberg BL, Richards S, Davison M, Corzo D, Chen YT (2006) Chinese hamster ovary cell-derived recombinant human acid alpha-glucosidase in infantile-onset Pompe disease. J Pediatr 149:89–97

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kishnani PS, Corzo D, Nicolino M, Byrne B, Mandel H, Hwu WL, Leslie N, Levine J, Spencer C, McDonald M, Li J, Dumontier J, Halberthal M, Chien YH, Hopkin R, Vijayaraghavan S, Gruskin D, Bartholomew D, van der Ploeg A, Clancy JP, Parini R, Morin G, Beck M, de la Gastine GS, Jokic M, Thurberg B, Richards S, Bali D, Davison M, Worden MA, Chen YT, Wraith JE (2007) Recombinant human acid [alpha]-glucosidase: major clinical benefits in infantile-onset Pompe disease. Neurology 68:99–109

    Article  CAS  PubMed  Google Scholar 

  • Kishnani PS, Goldenberg PC, Dearmey SL, Heller J, Benjamin D, Young S, Bali D, Smith SA, Li JS, Mandel H, Koeberl D, Rosenberg A, Chen YT (2010) Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol Genet Metab 99:26–33

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koeberl DD, Luo X, Sun B, McVie-Wylie A, Dai J, Li S, Banugaria SG, Chen YT, Bali DS (2011) Enhanced efficacy of enzyme replacement therapy in Pompe disease through mannose-6-phosphate receptor expression in skeletal muscle. Mol Genet Metab 103:107–112

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koeberl DD, Austin S, Case LE, Smith EC, Buckley AF, Young SP, Bali D, Kishnani PS (2014) Adjunctive albuterol enhances the response to enzyme replacement therapy in late-onset Pompe disease. FASEB J 28(5):2171–2176

    Article  CAS  PubMed  Google Scholar 

  • Kornfeld S, Sly WS (2001) I cell disease and pseudo-Hurler polydystrophy: disorders of lysosomal enzyme phosphorylation and localization. In: Scriver CR, Beaudet al, Sly WS, Valle D (eds) Metabolic and molecular bases of inherited diseases, 8th edn. McGraw Hill, New York

    Google Scholar 

  • Kornfeld R, Bao M, Brewer K, Noll C, Canfield WM (1998) Purification and multimeric structure of bovine N-acetylglucosamine-1- phosphodiester alpha-N-acetylglucosaminidase. J Biol Chem 273:23203–23210

    Article  CAS  PubMed  Google Scholar 

  • Kornfeld R, Bao M, Brewer K, Noll C, Canfield W (1999) Molecular cloning and functional expression of two splice forms of human N-acetylglucosamine-1-phosphodiester alpha-N-acetylglucosaminidase. J Biol Chem 274:32778–32785

    Article  CAS  PubMed  Google Scholar 

  • Kroos M, Hoogeveen-Westerveld M, Michelakakis H, Pomponio R, van der Ploeg A, Halley D, Reuser A, Consortium GAAD (2012a) Update of the pompe disease mutation database with 60 novel GAA sequence variants and additional studies on the functional effect of 34 previously reported variants. Hum Mutat 33:1161–5

    Google Scholar 

  • Kroos M, Hoogeveen-Westerveld M, van der Ploeg A, Reuser AJ (2012b) The genotype–phenotype correlation in Pompe disease. Am J Med Genet C Semin Med Genet 160C:59–68

    Article  PubMed  Google Scholar 

  • Kudo M, Canfield WM (2006) Structural requirements for efficient processing and activation of recombinant human UDP-N-acetylglucosamine:lysosomal-enzyme-N-acetylglucosamine-1-phosphotransferase. J Biol Chem 281:11761–11768

    Article  CAS  PubMed  Google Scholar 

  • Kudo M, Bao M, D’Souza A, Ying F, Pan H, Roe BA, Canfield WM (2005) The alpha- and beta-subunits of the human UDP-N-acetylglucosamine:lysosomal enzyme phosphotransferase are encoded by a single cDNA. J Biol Chem 280:36141–36149

    Article  CAS  PubMed  Google Scholar 

  • LeBowitz JH, Grubb JH, Maga JA, Schmiel DH, Vogler C, Sly WS (2004) Glycosylation-independent targeting enhances enzyme delivery to lysosomes and decreases storage in mucopolysaccharidosis type VII mice. Proc Natl Acad Sci U S A 101:3083–3088

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Y, Chen G (2011) Chemical synthesis of N-linked glycans carrying both mannose-6-phosphate and GlcNAc-mannose-6-phosphate motifs. J Org Chem 76:8682–8689

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Marshall J, Li Q, Edwards N, Chen G (2013) Synthesis of novel bivalent mimetic ligands for mannose-6-phosphate receptors. Bioorg Med Chem Lett 23:2328–2331

    Article  CAS  PubMed  Google Scholar 

  • Maga JA, Zhou J, Kambampati R, Peng S, Wang X, Bohnsack RN, Thomm A, Golata S, Tom P, Dahms NM, Byrne BJ, LeBowitz JH (2013) Glycosylation-independent lysosomal targeting of acid alpha-glucosidase enhances muscle glycogen clearance in pompe mice. J Biol Chem 288:1428–1438

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Malicdan MC, Noguchi S, Nonaka I, Saftig P, Nishino I (2008) Lysosomal myopathies: an excessive build-up in autophagosomes is too much to handle. Neuromuscul Disord 18:521–529

    Article  PubMed  Google Scholar 

  • Marlin SD, Springer TA (1987) Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell 51:813–819

    Article  CAS  PubMed  Google Scholar 

  • Martina JA, Diab HI, Lishu L, Jeong AL, Patange S, Raben N, Puertollano R (2014) The nutrient-responsive transcription factor TFE3 promotes autophagy, lysosomal biogenesis, and clearance of cellular debris. Sci Signal 7:ra9

    Article  PubMed  Google Scholar 

  • Matsumoto T, Akutsu S, Wakana N, Morito M, Shimada A, Yamane A (2006) The expressions of insulin-like growth factors, their receptors, and binding proteins are related to the mechanism regulating masseter muscle mass in the rat. Arch Oral Biol 51:603–611

    Article  CAS  PubMed  Google Scholar 

  • McVie-Wylie AJ, Lee KL, Qiu H, Jin X, Do H, Gotschall R, Thurberg BL, Rogers C, Raben N, O’Callaghan M, Canfield W, Andrews L, McPherson JM, Mattaliano RJ (2008) Biochemical and pharmacological characterization of different recombinant acid alpha-glucosidase preparations evaluated for the treatment of Pompe disease. Mol Genet Metab 94:448–455

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moreland RJ, Jin X, Zhang XK, Decker RW, Albee KL, Lee KL, Cauthron RD, Brewer K, Edmunds T, Canfield WM (2005) Lysosomal acid alpha-glucosidase consists of four different peptides processed from a single chain precursor. J Biol Chem 280:6780–6791

    Article  CAS  PubMed  Google Scholar 

  • Muro S, Schuchman EH, Muzykantov VR (2006) Lysosomal enzyme delivery by ICAM-1-targeted nanocarriers bypassing glycosylation- and clathrin-dependent endocytosis. Mol Ther 13:135–141

    Article  CAS  PubMed  Google Scholar 

  • Nicolino M, Byrne B, Wraith JE, Leslie N, Mandel H, Freyer DR, Arnold GL, Pivnick EK, Ottinger CJ, Robinson PH, Loo JC, Smitka M, Jardine P, Tato L, Chabrol B, McCandless S, Kimura S, Mehta L, Bali D, Skrinar A, Morgan C, Rangachari L, Corzo D, Kishnani PS (2009) Clinical outcomes after long-term treatment with alglucosidase alfa in infants and children with advanced Pompe disease. Genet Med 11:210–219

    Article  CAS  PubMed  Google Scholar 

  • Oba-Shinjo SM, Da Silva R, Andrade FG, Palmer RE, Pomponio RJ, Ciociola KM, Carvalho MS, Gutierrez PS, Porta G, Marrone CD, Munoz V, Grzesiuk AK, Llerena JC Jr, Berditchevsky CR, Sobreira C, Horovitz D, Hatem TP, Frota ER, Pecchini R, Kouyoumdjian JA, Werneck L, Amado VM, Camelo JS Jr, Mattaliano RJ, Marie SK (2009) Pompe disease in a Brazilian series: clinical and molecular analyses with identification of nine new mutations. J Neurol 256:1881–1890

    Article  CAS  PubMed  Google Scholar 

  • Olson LJ, Dahms NM, Kim JJ (2004a) The N-terminal carbohydrate recognition site of the cation-independent mannose 6-phosphate receptor. J Biol Chem 279:34000–34009

    Article  CAS  PubMed  Google Scholar 

  • Olson LJ, Yammani RD, Dahms NM, Kim JJ (2004b) Structure of uPAR, plasminogen, and sugar-binding sites of the 300 kDa mannose 6-phosphate receptor. EMBO J 23:2019–2028

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Olson LJ, Peterson FC, Castonguay A, Bohnsack RN, Kudo M, Gotschall RR, Canfield WM, Volkman BF, Dahms NM (2010) Structural basis for recognition of phosphodiester-containing lysosomal enzymes by the cation-independent mannose 6-phosphate receptor. Proc Natl Acad Sci U S A 107:12493–12498

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raben N, Nagaraju K, Lee E, Kessler P, Byrne B, Lee L, Lamarca M, King C, Ward J, Sauer B, Plotz P (1998) Targeted disruption of the acid alpha-glucosidase gene in mice causes an illness with critical features of both infantile and adult human glycogen storage disease type II. J Biol Chem 273:19086–19092

    Article  CAS  PubMed  Google Scholar 

  • Raben N, Danon M, Gilbert AL, Dwivedi S, Collins B, Thurberg BL, Mattaliano RJ, Nagaraju K, Plotz PH (2003) Enzyme replacement therapy in the mouse model of Pompe disease. Mol Genet Metab 80:159–169

    Article  CAS  PubMed  Google Scholar 

  • Raben N, Fukuda T, Gilbert AL, de Jong D, Thurberg BL, Mattaliano RJ, Meikle P, Hopwood JJ, Nagashima K, Nagaraju K, Plotz PH (2005) Replacing acid alpha-glucosidase in Pompe disease: recombinant and transgenic enzymes are equipotent, but neither completely clears glycogen from type II muscle fibers. Mol Ther 11:48–56

    Article  CAS  PubMed  Google Scholar 

  • Raben N, Wong A, Ralston E, Myerowitz R (2012) Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. Am J Med Genet C Semin Med Genet 160C:13–21

    Article  PubMed  Google Scholar 

  • Reitman ML, Kornfeld S (1981a) Lysosomal enzyme targeting. N-Acetylglucosaminylphosphotransferase selectively phosphorylates native lysosomal enzymes. J Biol Chem 256:11977–11980

    CAS  PubMed  Google Scholar 

  • Reitman ML, Kornfeld S (1981b) UDP-N-acetylglucosamine:glycoprotein N-acetylglucosamine-1-phosphotransferase. Proposed enzyme for the phosphorylation of the high mannose oligosaccharide units of lysosomal enzymes. J Biol Chem 256:4275–4281

    CAS  PubMed  Google Scholar 

  • Rohrer J, Kornfeld R (2001) Lysosomal hydrolase mannose 6-phosphate uncovering enzyme resides in the trans-Golgi network. Mol Biol Cell 12:1623–1631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shea L, Raben N (2009) Autophagy in skeletal muscle: implications for Pompe disease. Int J Clin Pharmacol Ther 47(Suppl 1):S42–S47

    PubMed Central  CAS  PubMed  Google Scholar 

  • Song X, Lasanajak Y, Olson LJ, Boonen M, Dahms NM, Kornfeld S, Cummings RD, Smith DF (2009) Glycan microarray analysis of P-type lectins reveals distinct phosphomannose glycan recognition. J Biol Chem 284:35201–35214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Spampanato C, Feeney E, Li L, Cardone M, Lim JA, Annunziata F, Zare H, Polishchuk R, Puertollano R, Parenti G, Ballabio A, Raben N (2013) Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol Med 5:691–706

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thurberg BL, Lynch Maloney C, Vaccaro C, Afonso K, Tsai AC, Bossen E, Kishnani PS, O’Callaghan M (2006) Characterization of pre- and post-treatment pathology after enzyme replacement therapy for Pompe disease. Lab Invest 86:1208–1220

    Article  CAS  PubMed  Google Scholar 

  • Tiels P, Baranova E, Piens K, de Visscher C, Pynaert G, Nerinckx W, Stout J, Fudalej F, Hulpiau P, Tannler S, Geysens S, Van Hecke A, Valevska A, Vervecken W, Remaut H, Callewaert N (2012) A bacterial glycosidase enables mannose-6-phosphate modification and improved cellular uptake of yeast-produced recombinant human lysosomal enzymes. Nat Biotechnol 30:1225–1231

    Article  CAS  PubMed  Google Scholar 

  • Tong PY, Kornfeld S (1989) Ligand interactions of the cation-dependent mannose 6-phosphate receptor. Comparison with the cation-independent mannose 6-phosphate receptor. J Biol Chem 264:7970–7975

    CAS  PubMed  Google Scholar 

  • Tong PY, Gregory W, Kornfeld S (1989) Ligand interactions of the cation-independent mannose 6-phosphate receptor. The stoichiometry of mannose 6-phosphate binding. J Biol Chem 264:7962–7969

    CAS  PubMed  Google Scholar 

  • Urayama A, Grubb JH, Banks WA, Sly WS (2007) Epinephrine enhances lysosomal enzyme delivery across the blood brain barrier by up-regulation of the mannose 6-phosphate receptor. Proc Natl Acad Sci U S A 104:12873–12878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uson I, Schmidt B, von Bulow R, Grimme S, von Figura K, Dauter M, Rajashankar KR, Dauter Z, Sheldrick GM (2003) Locating the anomalous scatterer substructures in halide and sulfur phasing. Acta Crystallogr D Biol Crystallogr 59:57–66

    Article  PubMed  Google Scholar 

  • van den Hout HM, Hop W, Van Diggelen OP, Smeitink JA, Smit GP, Poll-The BT, Bakker HD, Loonen MC, DE Klerk JB, Reuser AJ, van der Ploeg AT (2003) The natural course of infantile Pompe’s disease: 20 original cases compared with 133 cases from the literature. Pediatrics 112:332–340

    Article  PubMed  Google Scholar 

  • Van Hove JL, Yang HW, Wu JY, Brady RO, Chen YT (1996) High-level production of recombinant human lysosomal acid alpha-glucosidase in Chinese hamster ovary cells which targets to heart muscle and corrects glycogen accumulation in fibroblasts from patients with Pompe disease. Proc Natl Acad Sci U S A 93:65–70

    Article  PubMed Central  PubMed  Google Scholar 

  • Varki A, Kornfeld S (1980) Structural studies of phosphorylated high mannose-type oligosaccharides. J Biol Chem 255:10847–10858

    CAS  PubMed  Google Scholar 

  • Varki A, Kornfeld S (1983) The spectrum of anionic oligosaccharides released by endo-beta-N-acetylglucosaminidase H from glycoproteins. Structural studies and interactions with the phosphomannosyl receptor. J Biol Chem 258:2808–2818

    CAS  PubMed  Google Scholar 

  • Varki A, Sherman W, Kornfeld S (1983) Demonstration of the enzymatic mechanisms of alpha-N-acetyl-D-glucosamine-1-phosphodiester N-acetylglucosaminidase (formerly called alpha-N-acetylglucosaminylphosphodiesterase) and lysosomal alpha-N-acetylglucosaminidase. Arch Biochem Biophysics 222:145–149

    Article  CAS  Google Scholar 

  • Waheed A, Hasilik A, von Figura K (1981) Processing of the phosphorylated recognition marker in lysosomal enzymes. Characterization and partial purification of a microsomal alpha-N-acetylglucosaminyl phosphodiesterase. J Biol Chem 256:5717–5721

    CAS  PubMed  Google Scholar 

  • Watanabe H, Grubb JH, Sly WS (1990) The overexpressed human 46-kDa mannose 6-phosphate receptor mediates endocytosis and sorting of beta-glucuronidase. Proc Natl Acad Sci U S A 87:8036–8040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wenk J, Hille A, von Figura K (1991) Quantitation of Mr 46000 and Mr 300000 mannose 6-phosphate receptors in human cells and tissues. Biochem Int 23:723–731

    CAS  PubMed  Google Scholar 

  • Winkel LP, Hagemans ML, Van Doorn PA, Loonen MC, Hop WJ, Reuser AJ, van der Ploeg AT (2005) The natural course of non-classic Pompe’s disease: a review of 225 published cases. J Neurol 252:875–884

    Article  PubMed  Google Scholar 

  • Wisselaar HA, Kroos MA, Hermans MM, Van Beeumen J, Reuser AJ (1993) Structural and functional changes of lysosomal acid alpha-glucosidase during intracellular transport and maturation. J Biol Chem 268:2223–2231

    CAS  PubMed  Google Scholar 

  • Wokke JH, Escolar DM, Pestronk A, Jaffe KM, Carter GT, van den Berg LH, Florence JM, Mayhew J, Skrinar A, Corzo D, Laforet P (2008) Clinical features of late-onset Pompe disease: a prospective cohort study. Muscle Nerve 38:1236–1245

    Article  PubMed  Google Scholar 

  • Yang HW, Kikuchi T, Hagiwara Y, Mizutani M, Chen YT, Van Hove JL (1998) Recombinant human acid alpha-glucosidase corrects acid alpha- glucosidase-deficient human fibroblasts, quail fibroblasts, and quail myoblasts. Pediatr Res 43:374–380

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q, Stefano JE, Harrahy J, Finn P, Avila L, Kyazike J, Wei R, Van Patten SM, Gotschall R, Zheng X, Zhu Y, Edmunds T, Pan CQ (2011) Strategies for Neoglycan conjugation to human acid alpha-glucosidase. Bioconjug Chem 22:741–751

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q, Avila LZ, Konowicz PA, Harrahy J, Finn P, Kim J, Reardon MR, Kyazike J, Brunyak E, Zheng X, Patten SM, Miller RJ, pan CQ (2013) Glycan structure determinants for cation-independent mannose 6-phosphate receptor binding and cellular uptake of a recombinant protein. Bioconjug Chem 24:2025–2035

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Li X, Kyazike J, Zhou Q, Thurberg BL, Raben N, Mattaliano RJ, Cheng SH (2004) Conjugation of mannose 6-phosphate-containing oligosaccharides to acid alpha-glucosidase improves the clearance of glycogen in pompe mice. J Biol Chem 279:50336–50341

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Li X, McVie-Wylie A, Jiang C, Thurberg BL, Raben N, Mattaliano RJ, Cheng SH (2005) Carbohydrate-remodelled acid alpha-glucosidase with higher affinity for the cation-independent mannose 6-phosphate receptor demonstrates improved delivery to muscles of Pompe mice. Biochem J 389:619–628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu Y, Jiang JL, Gumlaw NK, Zhang J, Bercury SD, Ziegler RJ, Lee K, Kudo M, Canfield WM, Edmunds T, Jiang C, Mattaliano RJ, Cheng SH (2009) Glycoengineered acid alpha-glucosidase with improved efficacy at correcting the metabolic aberrations and motor function deficits in a mouse model of Pompe disease. Mol Ther 17:954–963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI, 53226, USA

    Nancy M. Dahms

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  1. Nancy M. Dahms
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Correspondence to Nancy M. Dahms .

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  1. Centre for Drug Evaluation and Research, Food and Drug Administration, Division of Biotechnology Review and Research III, Office of Biotechnology Products, Silver Spring, Maryland, USA

    Amy Rosenberg

  2. Genentech, Inc., South San Francisco, California, USA

    Barthélemy Demeule

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© 2015 American Association of Pharmaceutical Scientists

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Dahms, N.M. (2015). Muscle Targeting. In: Rosenberg, A., Demeule, B. (eds) Biobetters. AAPS Advances in the Pharmaceutical Sciences Series, vol 19. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2543-8_3

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