Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease

Abstract

A recently proposed therapeutic approach for lysosomal storage disorders (LSDs) relies upon the ability of transcription factor EB (TFEB) to stimulate autophagy and induce lysosomal exocytosis leading to cellular clearance. This approach is particularly attractive in glycogen storage disease type II [a severe metabolic myopathy, Pompe disease (PD)] as the currently available therapy, replacement of the missing enzyme acid alpha-glucosidase, fails to reverse skeletal muscle pathology. PD, a paradigm for LSDs, is characterized by both lysosomal abnormality and dysfunctional autophagy. Here, we show that TFEB is a viable therapeutic target in PD: overexpression of TFEB in a new muscle cell culture system and in mouse models of the disease reduced glycogen load and lysosomal size, improved autophagosome processing, and alleviated excessive accumulation of autophagic vacuoles. Unexpectedly, the exocytosed vesicles were labelled with lysosomal and autophagosomal membrane markers, suggesting that TFEB induces exocytosis of autophagolysosomes. Furthermore, the effects of TFEB were almost abrogated in the setting of genetically suppressed autophagy, supporting the role of autophagy in TFEB-mediated cellular clearance.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 66

1. 1.

   Andrews NW. Regulated secretion of conventional lysosomes. Trends Cell Biol. 2000;10:316-321.

   Not in our library10.1016/s0962-8924(00)01794-3

2. 2.

   Angelini C, Semplicini C. Enzyme replacement therapy for Pompe disease. Curr Neurol Neurosci Rep. 2012;12:70-75.

   Not in our library10.1007/s11910-011-0236-5

3. 3.

   Banugaria SG, Prater SN, Ng YK, Kobori JA, Finkel RS, Ladda RL, Chen YT, Rosenberg AS, Kishnani PS. The impact of antibodies on clinical outcomes in diseases treated with therapeutic protein: lessons learned from infantile Pompe disease. Genet Med. 2011;13:729-736.

   Not in our library10.1097/gim.0b013e3182174703

4. 4.

   Blott EJ, Griffiths GM. Secretory lysosomes. Nat Rev Mol Cell Biol. 2002;3:122-131.

   Not in our library10.1038/nrm732

5. 5.

   Byrne BJ, Falk DJ, Pacak CA, Nayak S, Herzog RW, Elder ME, Collins SW, Conlon TJ, Clement N, Cleaver BD, et al. Pompe disease gene therapy. Hum Mol Genet. 2011;20:R61-68.

   Not in our library10.1093/hmg/ddr174

6. 6.

   Cao Y, Espinola JA, Fossale E, Massey AC, Cuervo AM, Macdonald ME, Cotman SL. Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J Biol Chem. 2006;281:20483-20493.

   Not in our library10.1074/jbc.m602180200

7. 7.

   Chen FW, Li C, Ioannou YA. Cyclodextrin induces calcium-dependent lysosomal exocytosis. PLoS ONE. 2010;5:e15054.

   Not in our library10.1371/journal.pone.0015054

8. 8.

   Cox TM, Cachon-Gonzalez MB. The cellular pathology of lysosomal diseases. J Pathol. 2012;226:241-254.

   Not in our library10.1002/path.3021

9. 9.

   DiFranco M, Quinonez M, Capote J, Vergara J. DNA transfection of mammalian skeletal muscles using in vivo electroporation. J Vis Exp. 2009;32:1520-1527.

   Not in our library10.3791/1520

10. 10.

    Douillard-Guilloux G, Mouly V, Caillaud C, Richard E. Immortalization of murine muscle cells from lysosomal alpha-glucosidase deficient mice: a new tool to study pathophysiology and assess therapeutic strategies for Pompe disease. Biochem Biophys Res Commun. 2009;388:333-338.

    Not in our library10.1016/j.bbrc.2009.08.006

11. 11.

    Fraldi A, Annunziata F, Lombardi A, Kaiser HJ, Medina DL, Spampanato C, Fedele AO, Polishchuk R, Sorrentino NC, Simons K, et al. Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. EMBO J. 2010;29:3607-3620.

    Not in our library10.1038/emboj.2010.237

12. 12.

    Fukuda T, Ahearn M, Roberts A, Mattaliano RJ, Zaal K, Ralston E, Plotz PH, Raben N. Autophagy and mistargeting of therapeutic enzyme in skeletal muscle in pompe disease. Mol Ther. 2006a;14:831-839.

    Not in our library10.1016/j.ymthe.2006.08.009

13. 13.

    Fukuda T, Ewan L, Bauer M, Mattaliano RJ, Zaal K, Ralston E, Plotz PH, Raben N. Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann Neurol. 2006b;59:700-708.

    Not in our library10.1002/ana.20807

14. 14.

    Funk B, Kessler U, Eisenmenger W, Hansmann A, Kolb HJ, Kiess W. 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. 1992;75:424-431.

    Not in our library10.1210/jcem.75.2.1379254

15. 15.

    Huang HP, Chen PH, Hwu WL, Chuang CY, Chien YH, Stone L, Chien CL, Li LT, Chiang SC, Chen HF, et al. Human Pompe disease-induced pluripotent stem cells for pathogenesis modeling, drug testing and disease marker identification. Hum Mol Genet. 2011;20:4851-4864.

    Not in our library10.1093/hmg/ddr424

16. 16.

    Jat PS, Noble MD, Ataliotis P, Tanaka Y, Yannoutsos N, Larsen L, Kioussis D. Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc Natl Acad Sci USA. 1991;88:5096-5100.

    Not in our library10.1073/pnas.88.12.5096

17. 17.

    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.

    Not in our library10.1093/emboj/19.21.5720

18. 18.

    Kawagoe S, Higuchi T, Meng XL, Shimada Y, Shimizu H, Hirayama R, Fukuda T, Chang H, Nakahata T, Fukada S, et al. Generation of induced pluripotent stem (iPS) cells derived from a murine model of Pompe disease and differentiation of Pompe-iPS cells into skeletal muscle cells. Mol Genet Metab. 2011;104:123-128.

    Not in our library10.1016/j.ymgme.2011.05.020

19. 19.

    Kishnani PS, Corzo D, Nicolino M, Byrne B, Mandel H, Hwu WL, Leslie N, Levine J, Spencer C, McDonald M, et al. Recombinant human acid [alpha]-glucosidase: major clinical benefits in infantile-onset Pompe disease. Neurology. 2007;68:99-109.

    Not in our library10.1212/01.wnl.0000251268.41188.04

20. 20.

    Kishnani PS, Goldenberg PC, DeArmey SL, Heller J, Benjamin D, Young S, Bali D, Smith SA, Li JS, Mandel H, et al. Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol Genet Metab. 2010;99:26-33.

    Not in our library10.1016/j.ymgme.2009.08.003

21. 21.

    Klein D, Bussow H, Fewou SN, Gieselmann V. Exocytosis of storage material in a lysosomal disorder. Biochem Biophys Res Commun. 2005;327:663-667.

    Not in our library10.1016/j.bbrc.2004.12.054

22. 22.

    Koeberl DD, Li S, Dai J, Thurberg BL, Bali D, Kishnani PS. beta2 Agonists enhance the efficacy of simultaneous enzyme replacement therapy in murine Pompe disease. Mol Genet Metab. 2012;105:221-227.

    Not in our library10.1016/j.ymgme.2011.11.005

23. 23.

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

    Not in our library10.1002/ajmg.c.31318

24. 24.

    Lachmann RH. Enzyme replacement therapy for lysosomal storage diseases. Curr Opin Pediatr. 2011;23:588-593.

    Not in our library10.1097/mop.0b013e32834c20d9

25. 25.

    Liao G, Yao Y, Liu J, Yu Z, Cheung S, Xie A, Liang X, Bi X. Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1 −/− mouse brain. Am J Pathol. 2007;171:962-975.

    Not in our library10.2353/ajpath.2007.070052

26. 26.

    Lieberman AP, Puertollano R, Raben N, Slaugenhaupt S, Walkley SU, Ballabio A. Autophagy in lysosomal storage disorders. Autophagy. 2012;8:719-730.

    Not in our library10.4161/auto.19469

27. 27.

    Liu Q, Chang JW, Wang J, Kang SA, Thoreen CC, Markhard A, Hur W, Zhang J, Sim T, Sabatini DM, et al. Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl)phenyl)-9-(quinolin-3-yl)benz o[h][1,6]naphthyridin-2(1H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J Med Chem. 2010;53:7146-7155.

    Not in our library10.1021/jm101144f

28. 28.

    Louzao MC, Espina B, Vieytes MR, Vega FV, Rubiolo JA, Baba O, Terashima T, Botana LM. “Fluorescent glycogen” formation with sensibility for in vivo and in vitro detection. Glycoconj J. 2008;25:503-510.

    Not in our library10.1007/s10719-007-9075-7

29. 29.

    Luzio JP, Pryor PR, Bright NA. Lysosomes: fusion and function. Nat Rev Mol Cell Biol. 2007;8:622-632.

    Not in our library10.1038/nrm2217

30. 30.

    Maga JA, Zhou J, Kambampati R, Peng S, Wang X, Bohnsack RN, Thomm A, Golata S, Tom P, Dahms NM, et al. Glycosylation-independent lysosomal targeting of acid alpha-glucosidase enhances muscle glycogen clearance in Pompe mice. J Biol Chem. 2012;288:1428-1438.

    Not in our library10.1074/jbc.m112.438663

31. 31.

    Martina J, Chen Y, Gucek M, Puertollano R. MTOPC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy. 2012;8:903-914.

    Not in our library10.4161/auto.19653

32. 32.

    Martiniuk F, Chen A, Mack A, Arvanitopoulos E, Chen Y, Rom WN, Codd WJ, Hanna B, Alcabes P, Raben N, et al. Carrier frequency for glycogen storage disease type II in New York and estimates of affected individuals born with the disease. Am J Med Genet. 1998;79:69-72.

    Not in our library10.1002/(sici)1096-8628(19980827)79:1<69::aid-ajmg16>3.0.co;2-k

33. 33.

    Medina DL, Fraldi A, Bouche V, Annunziata F, Mansueto G, Spampanato C, Puri C, Pignata A, Martina JA, Sardiello M, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell. 2011;21:421-430.

    Not in our library10.1016/j.devcel.2011.07.016

34. 34.

    Mouly V, Edom F, Decary S, Vicart P, Barbert JP, Butler-Browne GS. SV40 large T antigen interferes with adult myosin heavy chain expression, but not with differentiation of human satellite cells. Exp Cell Res. 1996;225:268-276.

    Not in our library10.1006/excr.1996.0176

35. 35.

    Okumiya T, Kroos MA, Vliet LV, Takeuchi H, Van der Ploeg AT, Reuser AJ. Chemical chaperones improve transport and enhance stability of mutant alpha-glucosidases in glycogen storage disease type II. Mol Genet Metab. 2007;90:49-57.

    Not in our library10.1016/j.ymgme.2006.09.010

36. 36.

    Parenti G, Zuppaldi A, Gabriela PM, Rosaria TM, Annunziata I, Meroni G, Porto C, Donaudy F, Rossi B, Rossi M, et al. Pharmacological enhancement of mutated alpha-glucosidase activity in fibroblasts from patients with Pompe disease. Mol Ther. 2007;15:508-514.

    Not in our library10.1038/sj.mt.6300074

37. 37.

    Porto C, Cardone M, Fontana F, Rossi B, Tuzzi MR, Tarallo A, Barone MV, Andria G, Parenti G. The pharmacological chaperone N-butyldeoxynojirimycin enhances enzyme replacement therapy in Pompe disease fibroblasts. Mol Ther. 2009;17:964-971.

    Not in our library10.1038/mt.2009.53

38. 38.

    Porto C, Ferrara MC, Meli M, Acampora E, Avolio V, Rosa M, Cobucci-Ponzano B, Colombo G, Moracci M, Andria G, et al. Pharmacological enhancement of alpha-glucosidase by the allosteric chaperone N-acetylcysteine. Mol Ther. 2012;12:2201-2211.

    Not in our library10.1038/mt.2012.152

39. 39.

    Raben N, Jatkar T, Lee A, Lu N, Dwivedi S, Nagaraju K, Plotz PH. Glycogen stored in skeletal but not in cardiac muscle in acid alpha-glucosidase mutant (Pompe) mice is highly resistant to transgene-encoded human enzyme. Mol Ther. 2002;6:601-608.

    Not in our library

40. 40.

    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 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. 1998;273:19086-19092.

    Not in our library10.1074/jbc.273.30.19086

Cited by papers we hold 17

• Structure of the lysosomal mTORC1–TFEB–Rag–Ragulator megacomplex · 2023
  No notice
• The rapidly evolving view of lysosomal storage diseases · 2021
  No notice
• Autophagy in major human diseases · 2021
  No notice
• MitophAging: Mitophagy in Aging and Disease · 2020
  No notice
• Lysosomal Exocytosis, Exosome Release and Secretory Autophagy: The Autophagic- and Endo-Lysosomal Systems Go Extracellular · 2020
  No notice
• Lysosomal Exocytosis: The Extracellular Role of an Intracellular Organelle · 2020
  No notice
• Biomedical Implications of Autophagy in Macromolecule Storage Disorders · 2019
  Not checked
• Neuronal XBP-1 Activates Intestinal Lysosomes to Improve Proteostasis in C. elegans · 2019
  No notice
• Lysosomal size matters · 2019
  No notice
• Transcriptional Regulation of Autophagy: Mechanisms and Diseases · 2019
  No notice
• mTOR-dependent phosphorylation controls TFEB nuclear export · 2018
  No notice
• Lysosomal adaptation: How cells respond to lysosomotropic compounds · 2017
  No notice
• Dysregulation of autophagy as a common mechanism in lysosomal storage diseases · 2017
  No notice
• The Parkinson’s disease-associated genes ATP13A2 and SYT11 regulate autophagy via a common pathway · 2016
  No notice
• Early etiology of Alzheimer’s disease: tipping the balance toward autophagy or endosomal dysfunction? · 2015
  No notice
• Intracellular sphingosine releases calcium from lysosomes · 2015
  No notice
• Pompe disease: from pathophysiology to therapy and back again · 2014
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.