Failure of Autophagy in Pompe Disease
Abstract
:1. Background: The Lysosome and Autophagy
2. Autophagy in Pompe Disease
2.1. Brief Introduction
2.2. Role of Autophagy in Skeletal Muscle Damage in Pompe Disease
2.3. The Underlying Mechanisms of Defective Autophagy
2.4. Glycogen Traffic to the Lysosome
2.5. Next-Generation Enzyme Replacement Therapy: Effect on Autophagy
2.6. Relieving the Burden of Autophagy as a Gauge of Therapeutic Success
3. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Klionsky, D.J. Autophagy revisited: A conversation with Christian de Duve. Autophagy 2008, 4, 740–743. [Google Scholar] [CrossRef] [PubMed]
- Ohsumi, Y. Historical landmarks of autophagy research. Cell Res. 2013, 24, 9–23. [Google Scholar] [CrossRef] [PubMed]
- Gudmundsson, S.R.; Kallio, K.A.; Vihinen, H.; Jokitalo, E.; Ktistakis, N.; Eskelinen, E.-L. Morphology of Phagophore Precursors by Correlative Light-Electron Microscopy. Cells 2022, 11, 3080. [Google Scholar] [CrossRef] [PubMed]
- Berg, T.O.; Fengsrud, M.; Strømhaug, P.E.; Berg, T.; Seglen, P.O. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J. Biol. Chem. 1998, 273, 21883–21892. [Google Scholar] [CrossRef] [PubMed]
- Feng, Y.; He, D.; Yao, Z.; Klionsky, D.J. The machinery of macroautophagy. Cell Res. 2013, 24, 24–41. [Google Scholar] [CrossRef] [PubMed]
- Galluzzi, L.; Baehrecke, E.H.; Ballabio, A.; Boya, P.; Bravo-San Pedro, J.M.; Cecconi, F.; Choi, A.M.; Chu, C.T.; Codogno, P.; Colombo, M.I.; et al. Molecular definitions of autophagy and related processes. EMBO J. 2017, 36, 1811–1836. [Google Scholar] [CrossRef] [PubMed]
- Yu, L.; McPhee, C.K.; Zheng, L.; Mardones, G.A.; Rong, Y.; Peng, J.; Mi, N.; Zhao, Y.; Liu, Z.; Wan, F.; et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 2010, 465, 942–946. [Google Scholar] [CrossRef] [PubMed]
- Kaushik, S.; Cuervo, A.M. The coming of age of chaperone-mediated autophagy. Nat. Rev. Mol. Cell Biol. 2018, 19, 365–381. [Google Scholar] [CrossRef]
- Oku, M.; Sakai, Y. Three Distinct Types of Microautophagy Based on Membrane Dynamics and Molecular Machineries. BioEssays 2018, 40, e1800008. [Google Scholar] [CrossRef]
- Wang, L.; Klionsky, D.J.; Shen, H.-M. The emerging mechanisms and functions of microautophagy. Nat. Rev. Mol. Cell Biol. 2022, 24, 186–203. [Google Scholar] [CrossRef]
- Lieberman, A.P.; Puertollano, R.; Raben, N.; Slaugenhaupt, S.; Walkley, S.U.; Ballabio, A. Autophagy in lysosomal storage disorders. Autophagy 2012, 8, 719–730. [Google Scholar] [CrossRef]
- Seranova, E.; Connolly, K.J.; Zatyka, M.; Rosenstock, T.R.; Barrett, T.; Tuxworth, R.I.; Sarkar, S. Dysregulation of autophagy as a common mechanism in lysosomal storage diseases. Essays Biochem. 2017, 61, 733–749. [Google Scholar] [CrossRef]
- Myerowitz, R.; Puertollano, R.; Raben, N. Impaired autophagy: The collateral damage of lysosomal storage disorders. EBioMedicine 2020, 63, 103166. [Google Scholar] [CrossRef]
- Kabeya, Y.; Mizushima, N.; Ueno, T.; Yamamoto, A.; Kirisako, T.; Noda, T.; Kominami, E.; Ohsumi, Y.; Yoshimori, T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19, 5720–5728. [Google Scholar] [CrossRef]
- Tanida, I.; Ueno, T.; Kominami, E. LC3 and Autophagy. Methods Mol Biol. 2008, 445, 77–88. [Google Scholar]
- Kirkin, V. History of the Selective Autophagy Research: How Did It Begin and Where Does It Stand Today? J. Mol. Biol. 2020, 432, 3–27. [Google Scholar] [CrossRef]
- Gatica, D.; Lahiri, V.; Klionsky, D.J. Cargo recognition and degradation by selective autophagy. Nature 2018, 20, 233–242. [Google Scholar] [CrossRef]
- Bjørkøy, G.; Lamark, T.; Brech, A.; Outzen, H.; Perander, M.; Øvervatn, A.; Stenmark, H.; Johansen, T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on hunting-tin-induced cell death. J. Cell Biol. 2005, 171, 603–614. [Google Scholar] [CrossRef]
- Pankiv, S.; Clausen, T.H.; Lamark, T.; Brech, A.; Bruun, J.A.; Outzen, H.; Øvervatn, A.; Bjørkøy, G.; Johansen, T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282, 24131–24145. [Google Scholar] [CrossRef]
- Vargas, J.N.S.; Hamasaki, M.; Kawabata, T.; Youle, R.J.; Yoshimori, T. The mechanisms and roles of selective autophagy in mammals. Nat. Rev. Mol. Cell Biol. 2022, 24, 167–185. [Google Scholar] [CrossRef]
- Raben, N.; Takikita, S.; Pittis, M.G.; Bembi, B.; Marie, S.K.; Roberts, A.; Page, L.; Kishnani, P.S.; Schoser, B.G.; Chien, Y.-H.; et al. Deconstructing pompe disease by analyzing single muscle fibers: “To see a world in a grain of sand…”. Autophagy 2007, 3, 546–552. [Google Scholar] [CrossRef]
- Gallagher, E.R.; Holzbaur, E.L.F. The selective autophagy adaptor p62/SQSTM1 forms phase condensates regulated by HSP27 that facilitate the clearance of damaged lysosomes via lysophagy. Cell Rep. 2023, 42, 112037. [Google Scholar] [CrossRef]
- Sardiello, M.; Palmieri, M.; Di Ronza, A.; Medina, D.L.; Valenza, M.; Gennarino, V.A.; Di Malta, C.; Donaudy, F.; Embrione, V.; Polishchuk, R.S.; et al. A gene network regulating lysosomal biogenesis and function. Science 2009, 325, 473–477. [Google Scholar] [CrossRef]
- Martina, J.A.; Diab, H.I.; Lishu, L.; Jeong-A, L.; Patange, S.; Raben, N.; Puertollano, R. The Nutrient-Responsive Transcription Factor TFE3 Promotes Autophagy, Lysosomal Biogenesis, and Clearance of Cellular Debris. Sci. Signal. 2014, 7, ra9. [Google Scholar] [CrossRef]
- Settembre, C.; Di Malta, C.; Polito, V.A.; Garcia Arencibia, M.; Vetrini, F.; Erdin, S.; Erdin, S.U.; Huynh, T.; Medina, D.; Colella, P.; et al. TFEB links autophagy to lysosomal biogenesis. Science 2011, 332, 1429–1433. [Google Scholar] [CrossRef]
- Medina, D.L.; Fraldi, A.; Bouche, V.; Annunziata, F.; Mansueto, G.; Spampanato, C.; Puri, C.; Pignata, A.; Martina, J.A.; Sardiello, M.; et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev. Cell 2011, 21, 421–430. [Google Scholar] [CrossRef]
- Settembre, C.; Ballabio, A. Lysosomal Adaptation: How the Lysosome Responds to External Cues. Cold Spring Harb. Perspect. Biol. 2014, 6, a016907. [Google Scholar] [CrossRef]
- Martina, J.A.; Chen, Y.; Gucek, M.; Puertollano, R. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy 2012, 8, 903–914. [Google Scholar] [CrossRef]
- Roczniak-Ferguson, A.; Petit, C.S.; Froehlich, F.; Qian, S.; Ky, J.; Angarola, B.; Walther, T.C.; Ferguson, S.M. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 2012, 5, ra42. [Google Scholar] [CrossRef]
- Medina, D.L.; Di Paola, S.; Peluso, I.; Armani, A.; De Stefani, D.; Venditti, R.; Montefusco, S.; Scotto-Rosato, A.; Prezioso, C.; Forrester, A.; et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat. Cell Biol. 2015, 17, 288–299. [Google Scholar] [CrossRef]
- Lim, C.-Y.; Zoncu, R. The lysosome as a command-and-control center for cellular metabolism. J. Cell Biol. 2016, 214, 653–664. [Google Scholar] [CrossRef]
- Puertollano, R.; Ferguson, S.M.; Brugarolas, J.; Ballabio, A. The complex relationship between TFEB transcription factor phosphorylation and subcellular localization. EMBO J. 2018, 37, e98804. [Google Scholar] [CrossRef]
- Chan, E.Y.W.; Kir, S.; Tooze, S.A. siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J. Biol. Chem. 2007, 282, 25464–25474. [Google Scholar] [CrossRef]
- Kim, J.; Kundu, M.; Viollet, B.; Guan, K.-L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13, 132–141. [Google Scholar] [CrossRef]
- Inoki, K.; Kim, J.; Guan, K.-L. AMPK and mTOR in cellular energy homeostasis and drug targets. Annu. Rev. Pharmacol. Toxicol. 2012, 52, 381–400. [Google Scholar] [CrossRef]
- Huang, J.; Manning, B.D. The TSC1–TSC2 complex: A molecular switchboard controlling cell growth. Biochem. J. 2008, 412, 179–190. [Google Scholar] [CrossRef]
- Menon, S.; Dibble, C.C.; Talbott, G.; Hoxhaj, G.; Valvezan, A.J.; Takahashi, H.; Cantley, L.C.; Manning, B.D. Spatial control of the TSC complex integrates insulin and nutrient regulation of mTORC1 at the lysosome. Cell 2014, 156, 771–785. [Google Scholar] [CrossRef]
- Demetriades, C.; Plescher, M.; Teleman, A.A. Lysosomal recruitment of TSC2 is a universal response to cellular stress. Nat. Commun. 2016, 7, 10662. [Google Scholar] [CrossRef]
- Inpanathan, S.; Botelho, R.J. The Lysosome Signaling Platform: Adapting With the Times. Front. Cell Dev. Biol. 2019, 7, 113. [Google Scholar] [CrossRef]
- Saxton, R.A.; Sabatini, D.M. mTOR Signaling in Growth, Metabolism, and Disease. Cell 2017, 168, 960–976, Erratum in Cell 2017, 169, 361–371. [Google Scholar] [CrossRef]
- Settembre, C.; Fraldi, A.; Medina, D.L.; Ballabio, A. Signals from the lysosome: A control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 2013, 14, 283–296. [Google Scholar] [CrossRef]
- Raben, N.; Puertollano, R. TFEB and TFE3: Linking Lysosomes to Cellular Adaptation to Stress. Annu. Rev. Cell Dev. Biol. 2016, 32, 255–278. [Google Scholar] [CrossRef]
- Saftig, P.; Puertollano, R. How Lysosomes Sense, Integrate, and Cope with Stress. Trends Biochem. Sci. 2021, 46, 97–112. [Google Scholar] [CrossRef]
- Chan, J.; Desai, A.K.; Kazi, Z.B.; Corey, K.; Austin, S.; Hobson-Webb, L.D.; Case, L.E.; Jones, H.N.; Kishnani, P.S. The emerging phenotype of late-onset Pompe disease: A systematic literature review. Mol. Genet. Metab. 2017, 120, 163–172. [Google Scholar] [CrossRef]
- Ebbink, B.J.; Poelman, E.; Aarsen, F.K.; Plug, I.; Regal, L.; Muentjes, C.; Van Der Beek, N.A.M.E.; Lequin, M.H.; Van Der Ploeg, A.T.; Hout, J.M.P.V.D. Classic infantile Pompe patients approaching adulthood: A cohort study on consequences for the brain. Dev. Med. Child Neurol. 2018, 60, 579–586. [Google Scholar] [CrossRef]
- Kohler, L.; Puertollano, R.; Raben, N. Pompe Disease: From Basic Science to Therapy. Neurotherapeutics 2018, 15, 928–942. [Google Scholar] [CrossRef]
- Kishnani, P.S.; Hwu, W.-L.; Mandel, H.; Nicolino, M.; Yong, F.; Corzo, D.; Infantile-Onset Pompe Disease Natural History Study Group. A retrospective, multinational, multicenter study on the natural history of infantile-onset Pompe disease. J. Pediatr. 2006, 148, 671–676.e2. [Google Scholar] [CrossRef]
- Toscano, A.; Rodolico, C.; Musumeci, O. Multisystem late onset Pompe disease (LOPD): An update on clinical aspects. Ann. Transl. Med. 2019, 7, 284. [Google Scholar] [CrossRef]
- Güngör, D.; Reuser, A.J. How to describe the clinical spectrum in Pompe disease. Am. J. Med. Genet. Part A 2013, 161, 399–400. [Google Scholar] [CrossRef]
- Reuser, A.J.J.; Ploeg, A.T.; Chien, Y.; Llerena, J.; Abbott, M.; Clemens, P.R.; Kimonis, V.E.; Leslie, N.; Maruti, S.S.; Sanson, B.; et al. GAA variants and phenotypes among 1079 patients with Pompe disease: Data from the Pompe Registry. Hum. Mutat. 2019, 40, 2146–2164. [Google Scholar] [CrossRef]
- Reuser, A.J.; Schoser, B. Pompe Disease, 3rd ed.; UNI-MED Verlag AG: Bremen, Germany, 2021. [Google Scholar]
- Bodamer, O.A.; Scott, C.R.; Giugliani, R.; on behalf of the Pompe Disease Newborn Screening Working Group. Newborn Screening for Pompe Disease. Pediatrics 2017, 140, S4–S13. [Google Scholar] [CrossRef]
- Tang, H.; Feuchtbaum, L.; Sciortino, S.; Matteson, J.; Mathur, D.; Bishop, T.; Olney, R.S. The First Year Experience of Newborn Screening for Pompe Disease in California. Int. J. Neonatal Screen. 2020, 6, 9. [Google Scholar] [CrossRef]
- Stevens, D.; Milani-Nejad, S.; Mozaffar, T. Pompe Disease: A Clinical, Diagnostic, and Therapeutic Overview. Curr. Treat. Options Neurol. 2022, 24, 573–588. [Google Scholar] [CrossRef]
- Griffiths, G.; Hoflack, B.; Simons, K.; Mellman, I.; Kornfeld, S. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 1988, 52, 329–341. [Google Scholar] [CrossRef]
- Dahms, N.M.; Lobel, P.; Kornfeld, S. Mannose 6-phosphate receptors and lysosomal enzyme targeting. J. Biol. Chem. 1989, 264, 12115–12118. [Google Scholar] [CrossRef]
- Ghosh, P.; Dahms, N.M.; Kornfeld, S. Mannose 6-phosphate receptors: New twists in the tale. Nat. Rev. Mol. Cell Biol. 2003, 4, 202–213. [Google Scholar] [CrossRef]
- Saftig, P.; Klumperman, J. Lysosome biogenesis and lysosomal membrane proteins: Trafficking meets function. Nat. Rev. Mol. Cell Biol. 2009, 10, 623–635. [Google Scholar] [CrossRef]
- Wisselaar, H.; Kroos, M.; Hermans, M.; van Beeumen, J.; Reuser, A. Structural and functional changes of lysosomal acid alpha-glucosidase during intracellular transport and maturation. J. Biol. Chem. 1993, 268, 2223–2231. [Google Scholar] [CrossRef]
- Moreland, R.J.; Jin, X.; Zhang, X.K.; Decker, R.W.; Albee, K.L.; Lee, K.L.; Cauthron, R.D.; Brewer, K.; Edmunds, T.; Canfield, W.M.; et al. Lysosomal acid alpha-glucosidase consists of four different peptides processed from a single chain pre-cursor. J. Biol. Chem. 2005, 280, 6780–6791. [Google Scholar] [CrossRef]
- Raben, N.; Nagaraju, K.; Lee, E.; Kessler, P.; Byrne, B.; Lee, L.; LaMarca, M.; King, C.; Ward, J.; Sauer, B.; et al. Targeted disruption of the acid α-glucosidase gene in mice causes an illness with critical features of both infantile and adult human glycogen storage disease type II. J. Biol. Chem. 1998, 273, 19086–19092. [Google Scholar] [CrossRef]
- Raben, N.; Danon, M.; Gilbert, A.; Dwivedi, S.; Collins, B.; Thurberg, B.; Mattaliano, R.; Nagaraju, K.; Plotz, P. Enzyme replacement therapy in the mouse model of Pompe disease. Mol. Genet. Metab. 2003, 80, 159–169. [Google Scholar] [CrossRef]
- Bijvoet, A.G.; van de Kamp, E.H.; Kroos, M.A.; Ding, J.-H.; Yang, B.Z.; Visser, P.; Bakker, C.E.; Verbeet, M.P.; Oostra, B.A.; Reuser, A.J.; et al. Generalized glycogen storage and cardiomegaly in a knockout mouse model of Pompe disease. Hum. Mol. Genet. 1998, 7, 53–62. [Google Scholar] [CrossRef] [PubMed]
- Hesselink, R.P.; Van Kranenburg, G.; Wagenmakers, A.J.; Van der Vusse, G.J.; Drost, M.R. Age-related decline in muscle strength and power output in acid 1-4 alpha-glucosidase knockout mice. Muscle Nerve 2005, 31, 374–381. [Google Scholar] [CrossRef] [PubMed]
- Engel, A.G. Acid maltase deficiency in adults: Studies in four cases of a syndrome which may mimic muscular dystrophy or other myopathies. Brain 1970, 93, 599–616. [Google Scholar] [CrossRef]
- Raben, N.; Fukuda, T.; Gilbert, A.L.; De Jong, D.; Thurberg, B.L.; Mattaliano, R.J.; Meikle, P.; Hopwood, J.J.; Nagashima, K.; Nagaraju, K.; et al. 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. 2005, 11, 48–56. [Google Scholar] [CrossRef]
- Fukuda, T.; Ewan, L.; Bauer, M.; Mattaliano, R.J.; Zaal, K.; Ralston, E.; Plotz, P.H.; Raben, N. Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann. Neurol. 2006, 59, 700–708. [Google Scholar] [CrossRef]
- Feeney, E.J.; Austin, S.; Chien, Y.-H.; Mandel, H.; Schoser, B.; Prater, S.; Hwu, W.-L.; Ralston, E.; Kishnani, P.S.; Raben, N. The value of muscle biopsies in Pompe disease: Identifying lipofuscin inclusions in juvenile- and adult-onset patients. Acta Neuropathol. Commun. 2014, 2, 2. [Google Scholar] [CrossRef] [PubMed]
- Kishnani, P.S.; Nicolino, M.; Voit, T.; Rogers, R.C.; Tsai, A.C.-H.; Waterson, J.; Herman, G.E.; Amalfitano, A.; Thurberg, B.L.; Richards, S.; et al. Chinese hamster ovary cell-derived recombinant human acid α-glucosidase in infantile-onset Pompe disease. J. Pediatr. 2006, 149, 89–97. [Google Scholar] [CrossRef]
- Kishnani, P.S.; Corzo, D.; Nicolino, M.; Byrne, B.; Mandel, H.; Hwu, W.L.; Leslie, N.; Levine, J.; Spencer, C.; McDonald, M.; et al. Recombinant human acid α-glucosidase: Major clinical benefits in infantile-onset Pompe disease. Neurology 2011, 77, 1604. [Google Scholar] [CrossRef]
- Kishnani, P.S.; Corzo, D.; Leslie, N.D.; Gruskin, D.; van der Ploeg, A.; Clancy, J.P.; Parini, R.; Morin, G.; Beck, M.; Bauer, M.S.; et al. Early treatment with alglucosidase alpha prolongs long-term survival of infants with pompe disease. Pediatr. Res. 2009, 66, 329–335. [Google Scholar] [CrossRef]
- Prater, S.N.; Patel, T.T.; Buckley, A.F.; Mandel, H.; Vlodavski, E.; Banugaria, S.G.; Feeney, E.J.; Raben, N.; Kishnani, P.S. Skeletal muscle pathology of infantile Pompe disease during long-term enzyme replacement therapy. Orphanet J. Rare Dis. 2013, 8, 90. [Google Scholar] [CrossRef] [PubMed]
- Hahn, A.; Schänzer, A. Long-term outcome and unmet needs in infantile-onset Pompe disease. Ann. Transl. Med. 2019, 7, 283. [Google Scholar] [CrossRef] [PubMed]
- Gutschmidt, K.; Musumeci, O.; Diaz-Manera, J.; Chien, Y.H.; Knop, K.C.; Wenninger, S.; Montagnese, F.; Pugliese, A.; Tavilla, G.; Alonso-Pérez, J.; et al. STIG study: Real-world data of long-term outcomes of adults with Pompe disease under enzyme re-placement therapy with alglucosidase alfa. J. Neurol. 2021, 268, 2482–2492. [Google Scholar] [CrossRef] [PubMed]
- Nishino, I. Autophagic vacuolar myopathies. Curr. Neurol. Neurosci. Rep. 2003, 3, 64–69. [Google Scholar] [CrossRef] [PubMed]
- Mair, D.; Biskup, S.; Kress, W.; Abicht, A.; Brück, W.; Zechel, S.; Knop, K.C.; Koenig, F.B.; Tey, S.; Nikolin, S.; et al. Differential diagnosis of vacuolar myopathies in the NGS era. Brain Pathol. 2020, 30, 877–896. [Google Scholar] [CrossRef] [PubMed]
- Meena, N.K.; Ralston, E.; Raben, N.; Puertollano, R. Enzyme Replacement Therapy Can Reverse Pathogenic Cascade in Pompe Disease. Mol. Ther.-Methods Clin. Dev. 2020, 18, 199–214. [Google Scholar] [CrossRef] [PubMed]
- Fukuda, T.; Ahearn, M.; Roberts, A.; Mattaliano, R.J.; Zaal, K.; Ralston, E.; Plotz, P.H.; Raben, N. Autophagy and mistargeting of therapeutic enzyme in skeletal muscle in pompe disease. Mol. Ther. 2006, 14, 831–839. [Google Scholar] [CrossRef] [PubMed]
- Fukuda, T.; Roberts, A.; Ahearn, M.; Zaal, K.; Ralston, E.; Plotz, P.H.; Raben, N. Autophagy and lysosomes in pompe disease. Autophagy 2006, 2, 318–320. [Google Scholar] [CrossRef] [PubMed]
- Spampanato, C.; Feeney, E.; Li, L.; Cardone, M.; Lim, J.-A.; Annunziata, F.; Zare, H.; Polishchuk, R.; Puertollano, R.; Parenti, G.; et al. Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol. Med. 2013, 5, 691–706. [Google Scholar] [CrossRef]
- Ralston, E.; Swaim, B.; Czapiga, M.; Hwu, W.-L.; Chien, Y.-H.; Pittis, M.; Bembi, B.; Schwartz, O.; Plotz, P.; Raben, N. Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence. J. Struct. Biol. 2008, 162, 500–508. [Google Scholar] [CrossRef]
- Raben, N.; Baum, R.; Schreiner, C.; Takikita, S.; Mizushima, N.; Ralston, E.; Plotz, P.H. When more is less: Excess and deficiency of autophagy coexist in skeletal muscle in Pompe disease. Autophagy 2009, 5, 111–113. [Google Scholar] [CrossRef] [PubMed]
- Klionsky, D.J.; Abdalla, F.C.; Abeliovich, H.; Abraham, R.T.; Acevedo-Arozena, A.; Adeli, K.; Agholme, L.; Agnello, M.; Agostinis, P.; Aguirre-Ghiso, J.A.; et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8, 445–544. [Google Scholar] [CrossRef] [PubMed]
- Nascimbeni, A.C.; Fanin, M.; Angelini, C.; Sandri, M. Autophagy dysregulation in Danon disease. Cell Death Dis. 2017, 8, e2565. [Google Scholar] [CrossRef]
- Lim, J.; Li, L.; Shirihai, O.S.; Trudeau, K.M.; Puertollano, R.; Raben, N. Modulation of mTOR signaling as a strategy for the treatment of Pompe disease. EMBO Mol. Med. 2017, 9, 353–370. [Google Scholar] [CrossRef] [PubMed]
- Lim, J.-A.; Sun, B.; Puertollano, R.; Raben, N. Therapeutic Benefit of Autophagy Modulation in Pompe Disease. Mol. Ther. 2018, 26, 1783–1796. [Google Scholar] [CrossRef] [PubMed]
- Schiaffino, S.; Hanzlíková, V. Autophagic degradation of glycogen in skeletal muscles of the newborn rat. J. Cell Biol. 1972, 52, 41–51. [Google Scholar] [CrossRef] [PubMed]
- Kotoulas, O.B.; Kalamidas, S.A.; Kondomerkos, D.J. Glycogen autophagy. Microsc. Res. Tech. 2004, 64, 10–20. [Google Scholar] [CrossRef] [PubMed]
- Kotoulas, O.B.; Kalamidas, S.A.; Kondomerkos, D.J. Glycogen autophagy in glucose homeostasis. Pathol. Res. Pract. 2006, 202, 631–638. [Google Scholar] [CrossRef] [PubMed]
- Kondomerkos, D.; Kalamidas, S.; Kotoulas, O. An electron microscopic and biochemical study of the effects of glucagon on glycogen autophagy in the liver and heart of newborn rats. Microsc. Res. Tech. 2004, 63, 87–93. [Google Scholar] [CrossRef]
- Kondomerkos, D.J.; A Kalamidas, S.; Kotoulas, O.B.; Hann, A.C. Glycogen autophagy in the liver and heart of newborn rats. The effects of glucagon, adrenalin or rapamycin. Histol. Histopathol. 2005, 20, 689–696. [Google Scholar] [CrossRef]
- Raben, N.; Schreiner, C.; Baum, R.; Takikita, S.; Xu, S.; Xie, T.; Myerowitz, R.; Komatsu, M.; Van Der Meulen, J.H.; Nagaraju, K.; et al. Suppression of autophagy permits successful enzyme replacement therapy in a lysosomal storage disor-der-murine Pompe disease. Autophagy 2010, 6, 1078–1089. [Google Scholar] [CrossRef] [PubMed]
- Kuma, A.; Hatano, M.; Matsui, M.; Yamamoto, A.; Nakaya, H.; Yoshimori, T.; Ohsumi, Y.; Tokuhisa, T.; Mizushima, N. The role of autophagy during the early neonatal starvation period. Nature 2004, 432, 1032–1036. [Google Scholar] [CrossRef] [PubMed]
- Komatsu, M.; Waguri, S.; Ueno, T.; Iwata, J.; Murata, S.; Tanida, I.; Ezaki, J.; Mizushima, N.; Ohsumi, Y.; Uchiyama, Y.; et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 2005, 169, 425–434. [Google Scholar] [CrossRef]
- Kuma, A.; Komatsu, M.; Mizushima, N. Autophagy-monitoring and autophagy-deficient mice. Autophagy 2017, 13, 1619–1628. [Google Scholar] [CrossRef] [PubMed]
- Roach, P.J.; Depaoli-Roach, A.A.; Hurley, T.D.; Tagliabracci, V.S. Glycogen and its metabolism: Some new developments and old themes. Biochem. J. 2012, 441, 763–787. [Google Scholar] [CrossRef] [PubMed]
- Zhang, N.; Liu, F.; Zhao, Y.; Sun, X.; Wen, B.; Lu, J.; Yan, C.; Li, D. Defect in degradation of glycogenin-exposed residual glycogen in lysosomes is the fundamental pathomechanism of Pompe disease. J. Pathol. 2024, 263, 8–21. [Google Scholar] [CrossRef] [PubMed]
- Jiang, S.; Wells, C.D.; Roach, P.J. Starch-binding domain-containing protein 1 (Stbd1) and glycogen metabolism: Identification of the Atg8 family interacting motif (AIM) in Stbd1 required for interaction with GABARAPL1. Biochem. Biophys. Res. Commun. 2011, 413, 420–425. [Google Scholar] [CrossRef] [PubMed]
- Heden, T.D.; Chow, L.S.; Hughey, C.C.; Mashek, D.G. Regulation and role of glycophagy in skeletal muscle energy metabolism. Autophagy 2021, 18, 1078–1089. [Google Scholar] [CrossRef] [PubMed]
- Jiang, S.; Heller, B.; Tagliabracci, V.S.; Zhai, L.; Irimia, J.M.; DePaoli-Roach, A.A.; Wells, C.D.; Skurat, A.V.; Roach, P.J. Starch binding domain-containing protein 1/genethonin 1 is a novel participant in glycogen metabolism. J. Biol. Chem. 2010, 285, 34960–34971. [Google Scholar] [CrossRef] [PubMed]
- Yi, H.; Fredrickson, K.B.; Das, S.; Kishnani, P.S.; Sun, B. Stbd1 is highly elevated in skeletal muscle of Pompe disease mice but suppression of its expression does not affect lysosomal glycogen accumulation. Mol. Genet. Metab. 2013, 109, 312–314. [Google Scholar] [CrossRef]
- Sun, T.; Yi, H.; Yang, C.; Kishnani, P.S.; Sun, B. Starch Binding Domain-containing Protein 1 Plays a Dominant Role in Glycogen Transport to Lysosomes in Liver. J. Biol. Chem. 2016, 291, 16479–16484. [Google Scholar] [CrossRef] [PubMed]
- Behrends, C.; Sowa, M.E.; Gygi, S.P.; Harper, J.W. Network organization of the human autophagy system. Nature 2010, 466, 68–76. [Google Scholar] [CrossRef] [PubMed]
- Zirin, J.; Nieuwenhuis, J.; Samsonova, A.; Tao, R.; Perrimon, N. Regulators of Autophagosome Formation in Drosophila Muscles. PLOS Genet. 2015, 11, e1005006. [Google Scholar] [CrossRef] [PubMed]
- Koutsifeli, P.; Varma, U.; Daniels, L.J.; Annandale, M.; Li, X.; Neale, J.P.H.; Hayes, S.; Weeks, K.L.; James, S.; Delbridge, L.M.D.; et al. Glycogen-autophagy: Molecular machinery and cellular mechanisms of glycophagy. J. Biol. Chem. 2022, 298, 102093. [Google Scholar] [CrossRef] [PubMed]
- Zirin, J.; Nieuwenhuis, J.; Perrimon, N. Role of autophagy in glycogen breakdown and its relevance to chloroquine myopathy. PLOS Biol. 2013, 11, e1001708. [Google Scholar] [CrossRef] [PubMed]
- Canibano-Fraile, R.; Harlaar, L.; Dos Santos, C.A.; Hoogeveen-Westerveld, M.; Demmers, J.A.; Snijders, T.; Lijnzaad, P.; Verdijk, R.M.; van der Beek, N.A.M.E.; van Doorn, P.A.; et al. Lysosomal glycogen accumulation in Pompe disease results in disturbed cytoplasmic glycogen me-tabolism. J. Inherit. Metab. Dis. 2023, 46, 101–115. [Google Scholar] [CrossRef] [PubMed]
- Gómez-Cebrián, N.; Gras-Colomer, E.; Andrés, J.L.P.; Pineda-Lucena, A.; Puchades-Carrasco, L. Omics-Based Approaches for the Characterization of Pompe Disease Metabolic Phenotypes. Biology 2023, 12, 1159. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Porras, V.; Guevara-Morales, J.M.; Echeverri-Peña, O.Y. From Acid Alpha-Glucosidase Deficiency to Autophagy: Understanding the Bases of POMPE Disease. Int. J. Mol. Sci. 2023, 24, 12481. [Google Scholar] [CrossRef]
- Ullman, J.C.; Mellem, K.T.; Xi, Y.; Ramanan, V.; Merritt, H.; Choy, R.; Gujral, T.; Young, L.E.; Blake, K.; Tep, S.; et al. Small-molecule inhibition of glycogen synthase 1 for the treatment of Pompe disease and other glycogen storage disorders. Sci. Transl. Med. 2024, 16, eadf1691. [Google Scholar] [CrossRef]
- Mancini, M.C.; Noland, R.C.; Collier, J.J.; Burke, S.J.; Stadler, K.; Heden, T.D. Lysosomal glucose sensing and glycophagy in metabolism. Trends Endocrinol. Metab. 2023, 34, 764–777. [Google Scholar] [CrossRef]
- Kornfeld, S. Lysosomal enzyme targeting. Biochem. Soc. Trans. 1990, 18, 367–374. [Google Scholar] [CrossRef] [PubMed]
- Do, H.V.; Khanna, R.; Gotschall, R. Challenges in treating Pompe disease: An industry perspective. Ann. Transl. Med. 2019, 7, 291. [Google Scholar] [CrossRef] [PubMed]
- Diaz-Manera, J.; Kishnani, P.S.; Kushlaf, H.; Ladha, S.; Mozaffar, T.; Straub, V.; Toscano, A.; van der Ploeg, A.T.; I Berger, K.; Clemens, P.R.; et al. Safety and efficacy of avalglucosidase alfa versus alglucosidase alfa in patients with late-onset Pompe disease (COMET): A phase 3, randomised, multicentre trial. Lancet Neurol. 2021, 20, 1012–1026. [Google Scholar] [CrossRef]
- Zhu, Y.; Jiang, J.-L.; Gumlaw, N.K.; Zhang, J.; Bercury, S.D.; Ziegler, R.J.; Lee, K.; Kudo, M.; Canfield, W.M.; Edmunds, T.; et al. Glycoengineered acid α-glucosidase with improved efficacy at correcting the metabolic aberrations and motor function deficits in a mouse model of pompe disease. Mol. Ther. 2009, 17, 954–963. [Google Scholar] [CrossRef] [PubMed]
- Puertollano, R.; Raben, N. New therapies for Pompe disease: Are we closer to a cure? Lancet Neurol. 2021, 20, 973–975. [Google Scholar] [CrossRef] [PubMed]
- Dimachkie, M.M.; Barohn, R.J.; Byrne, B.; Goker-Alpan, O.; Kishnani, P.S.; Ladha, S.; Laforêt, P.; Mengel, K.E.; Peña, L.D.; Sacconi, S.; et al. Long-term Safety and Efficacy of Avalglucosidase Alfa in Patients With Late-Onset Pompe Disease. Neurology 2022, 99, e536–e548. [Google Scholar] [CrossRef]
- de Visser, M.; Argov, Z. Greater Efficacy of Avalglucosidase vs Alglucosidase Alfa in Adult Pompe Disease? The Jury Is Still Out. Neurology 2022, 99, 183–184. [Google Scholar] [CrossRef] [PubMed]
- Selvan, N.; Mehta, N.; Venkateswaran, S.; Brignol, N.; Graziano, M.; Sheikh, M.O.; McAnany, Y.; Hung, F.; Madrid, M.; Krampetz, R.; et al. Endolysosomal N-glycan processing is critical to attain the most active form of the enzyme acid alpha-glucosidase. J. Biol. Chem. 2021, 296, 100769. [Google Scholar] [CrossRef]
- Schoser, B.; Roberts, M.; Byrne, B.J.; Sitaraman, S.; Jiang, H.; Laforêt, P.; Toscano, A.; Castelli, J.; Díaz-Manera, J.; Goldman, M.; et al. Safety and efficacy of cipaglucosidase alfa plus miglustat versus alglucosidase alfa plus placebo in late-onset Pompe disease (PROPEL): An international, randomised, double-blind, parallel-group, phase 3 trial. Lancet Neurol. 2021, 20, 1027–1037. [Google Scholar] [CrossRef]
- Schoser, B.; Kishnani, P.S.; Bratkovic, D.; Byrne, B.J.; Claeys, K.G.; Díaz-Manera, J.; Laforêt, P.; Roberts, M.; Toscano, A.; van der Ploeg, A.T.; et al. 104-week efficacy and safety of cipaglucosidase alfa plus miglustat in adults with late-onset Pompe disease: A phase III open-label extension study (ATB200-07). J. Neurol. 2024, 271, 2810–2823. [Google Scholar] [CrossRef]
- Xu, S.; Lun, Y.; Frascella, M.; Garcia, A.; Soska, R.; Nair, A.; Ponery, A.S.; Schilling, A.; Feng, J.; Tuske, S.; et al. Improved efficacy of a next-generation ERT in murine Pompe disease. J. Clin. Investig. 2019, 4, e125358. [Google Scholar] [CrossRef] [PubMed]
- Papadopoulos, C.; Kravic, B.; Meyer, H. Repair or Lysophagy: Dealing with Damaged Lysosomes. J. Mol. Biol. 2020, 432, 231–239. [Google Scholar] [CrossRef] [PubMed]
- Plotnikov, S.V.; Millard, A.C.; Campagnola, P.J.; Mohler, W.A. Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres. Biophys. J. 2006, 90, 693–703. [Google Scholar] [CrossRef] [PubMed]
- Meena, N.K.; Randazzo, D.; Raben, N.; Puertollano, R. AAV-mediated delivery of secreted acid α-glucosidase with enhanced uptake corrects neuromuscular pathology in Pompe mice. J. Clin. Investig. 2023, 8, e170199. [Google Scholar] [CrossRef] [PubMed]
- Jia, J.; Claude-Taupin, A.; Gu, Y.; Choi, S.W.; Peters, R.; Bissa, B.; Mudd, M.H.; Allers, L.; Pallikkuth, S.; Lidke, K.A.; et al. Galectin-3 Coordinates a Cellular System for Lysosomal Repair and Removal. Dev. Cell 2020, 52, 69–87. [Google Scholar] [CrossRef] [PubMed]
- Mizushima, N.; Yamamoto, A.; Matsui, M.; Yoshimori, T.; Ohsumi, Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a flu-orescent autophagosome marker. Mol. Biol. Cell 2004, 15, 1101–1111. [Google Scholar] [CrossRef] [PubMed]
- Vaghela, R.; Arkudas, A.; Horch, R.E.; Hessenauer, M. Actually Seeing What Is Going on—Intravital Microscopy in Tissue Engineering. Front. Bioeng. Biotechnol. 2021, 9, 627462. [Google Scholar] [CrossRef]
- Meena, N.K.; Ng, Y.; Randazzo, D.; Weigert, R.; Puertollano, R.; Raben, N. Intravital imaging of muscle damage and response to therapy in a model of Pompe disease. Clin. Transl. Med. 2024, 14, e1561. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Do, H.; Meena, N.K.; Raben, N. Failure of Autophagy in Pompe Disease. Biomolecules 2024, 14, 573. https://doi.org/10.3390/biom14050573
Do H, Meena NK, Raben N. Failure of Autophagy in Pompe Disease. Biomolecules. 2024; 14(5):573. https://doi.org/10.3390/biom14050573
Chicago/Turabian StyleDo, Hung, Naresh K. Meena, and Nina Raben. 2024. "Failure of Autophagy in Pompe Disease" Biomolecules 14, no. 5: 573. https://doi.org/10.3390/biom14050573