2-Hydroxypropyl-β-cyclodextrin promotes transcription factor EB-mediated activation of autophagy: Implications for therapy

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 10211-10222

  Song, Wensi ^a   Wang, Fan ^a   Lotfi, Parisa ^b   Sardiello, Marco ^b   Segatori, Laura ^a  

^a RICE UNIVERSITY   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CYCLODEXTRINS; DRUG DELIVERY; STORAGE (MATERIALS);

APOPTOTIC PATHWAYS; CELLULAR RESPONSE; DRUG DELIVERY VEHICLES; LYSOSOMAL STORAGE DISORDER; MASTER REGULATORS; PLATFORM TECHNOLOGY; STORAGE DISORDERS; THERAPEUTIC MODALITY;

TRANSCRIPTION FACTORS;

2 HYDROXYPROPYL BETA CYCLODEXTRIN; PROTEOLIPID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGY; BIOENGINEERING; CELL FUNCTION; CELL STIMULATION; CLEARANCE; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LYSOSOME; LYSOSOME STORAGE DISEASE; PRIORITY JOURNAL; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

APOPTOSIS; AUTOPHAGY; CEROID LIPOPIGMENT; CYCLODEXTRIN; LIPOPROTEIN; LYSOSOMAL STORAGE DISEASE; LYSOSOMES; NEURONAL CEROID LIPOFUSCINOSIS; TFEB;

AUTOPHAGY; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA-CYCLODEXTRINS; EXCIPIENTS; FIBROBLASTS; HELA CELLS; HUMANS; LYSOSOMAL STORAGE DISEASES; LYSOSOMES;

EID: 84898073840     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.506246     Document Type: Article

References (57)

1. Davis, M. E., and Brewster, M. E. (2004) Cyclodextrin-based pharmaceutics. Past, present, and future. Nat. Rev. Drug Discov. 3, 1023-1035
2. Rajewski, R. A., and Stella, V. J. (1996) Pharmaceutical applications of cyclodextrins. 2. In vivo drug delivery. J. Pharm. Sci. 85, 1142-1169
3. Davidson, C. D., Ali, N. F., Micsenyi, M. C, Stephney, G., Renault, S., Dobrenis, K., Ory, D. S., Vanier, M. T., and Walkley, S. U. (2009) Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS ONE 4, e6951
4. Liu, B., Turley, S. D., Burns, D. K., Miller, A. M., Repa, J. J., and Dietschy, J. M. (2009) Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1(-/-) mouse. Proc. Natl. Acad. Sci. U.S.A. 106, 2377-2382
5. Liu, B., Li, H., Repa, J. J., Turley, S. D., and Dietschy, J. M. (2008) Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res. 49, 663-669
6. Mukherjee, S., and Maxfield, F. R. (2004) Lipid and cholesterol trafficking in NPC. Biochim. Biophys. Acta 1685, 28-37
7. Atger, V. M., de la Llera Moya, M., Stoudt, G. W., Rodrigueza, W. V., Phillips, M. C, and Rothblat, G. H. (1997) Cyclodextrins as catalysts for the removal of cholesterol from macrophage foam cells. J. Clin. Invest. 99, 773-780
8. Christian, A. E., Haynes, M. P., Phillips, M. C, and Rothblat, G. H. (1997) Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 38, 2264-2272
9. Abi-Mosleh, L., Infante, R. E., Radhakrishnan, A., Goldstein, J. L., and Brown, M. S. (2009) Cyclodextrin overcomes deficient lysosome-to-endo-plasmic reticulum transport of cholesterol in Niemann-Pick type C cells. Proc. Natl. Acad. Sci. U.S.A. 106, 19316-19321
10. Rosenbaum, A. I., Zhang, G., Warren, J. D., and Maxfield, F. R. (2010) Endocytosis of/3-cyclodextrins is responsible for cholesterol reduction in Niemann-Pick type C mutant cells. Proc. Natl. Acad. Sci. U.S.A. 107, 5477-5482
11. Loftus, S. K., Morris, J. A., Carstea, E. D., Gu, J. Z., Cummings, C, Brown, A., Ellison, J., Ohno, K., Rosenfeld, M. A., Tagle, D. A., Pentchev, P. G., and Pavan, W. J. (1997) Murine model of Niemann-Pick C disease. Mutation in a cholesterol homeostasis gene. Science 277, 232-235
12. Cheng, J., Ohsaki, Y., Tauchi-Sato, K., Fujita, A., and Fujimoto, T. (2006) Cholesterol depletion induces autophagy. Biochem. Biophys. Res. Com-mun. 351, 246-252
13. Wang, C. W., and Klionsky, D. J. (2003) The molecular mechanism of autophagy. Mol. Med. 9, 65-76
14. Kundu, M., and Thompson, C. B. (2008) Autophagy. Basic principles and relevance to disease. AnnuRev. Pathol3, 427-455
15. Levine, B., and Kroemer, G. (2008) Autophagy in the pathogenesis of disease. Cell 132, 27-42
16. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., and Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111
17. Glick, D., Barth, S., and Macleod, K. F. (2010) Autophagy. Cellular and molecular mechanisms. J. Pathol. 221, 3-12
18. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., and Miz-ushima, N. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889
19. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., and Tanaka, K. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880-884
20. Nakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., Nara, A., Funao, J., Nakata, M., Tsuda, K., Hamada, S., and Yoshimori, T. (2004) Autophagy defends cells against invading group a Streptococcus. Science 306, 1037-1040
21. Oh, J. E., and Lee, H. K. (2012) Autophagy in Innate Recognition of Pathogens and Adaptive Immunity. Yonsei Med. J. 53, 241-247
22. Delgado, M., Singh, S., De Haro, S., Master, S., Ponpuak, M., Dinkins, C., Ornatowski, W., Vergne, I., and Deretic, V. (2009) Autophagy and pattern recognition receptors in innate immunity. Immunol. Rev. 227, 189-202
23. Kondo, Y., Kanzawa, T., Sawaya, R., and Kondo, S. (2005) The role of autophagy in cancer development and response to therapy.Nat. Rev. Cancer 5, 726-734
24. Tsujimoto, Y., and Shimizu, S. (2005) Another way to die. Autophagic programmed cell death. Cell Death Differ. 12, 1528-1534
25. Hait, W. N., Jin, S., and Yang, J. M. (2006) A matter of life or death (or both). Understanding autophagy in cancer. Clin. Cancer Res. 12, 1961-1965
26. Ogier-Denis, E., and Codogno, P. (2003) Autophagy: a barrier or an adaptive response to cancer. Biochim. Biophys. Acta 1603, 113-128
27. Debnath, J., Baehrecke, E. H., and Kroemer, G. (2005) Does autophagy contribute to cell death? Autophagy 1, 66-74
28. Eisenberg-Lerner, A., Bialik, S., Simon, H. U., and Kimchi, A. (2009) Life and death partners. Apoptosis, autophagy, and the cross-talk between them. Cell Death Differ 16, 966-975
29. Gorski, S. M., Chittaranjan, S., Pleasance, E. D., Freeman, J. D., Anderson, C. L., Varhol, R. J., Coughlin, S. M., Zuyderduyn, S. D., Jones, S. J., and Marra, M. A. (2003) A SAGE approach to discovery of genes involved in autophagic cell death. Curr. Biol. 13, 358-363
30. Lee, C. Y., Clough, E. A., Yellon, P., Teslovich, T. M., Stephan, D. A., and Baehrecke, E. H. (2003) Genome-wide analyses of steroid-and radiation-triggered programmed cell death in Drosophila. Curr. Biol. 13, 350-357
31. Kroemer, G., and Levine, B. (2008) Autophagic cell death. The story of a misnomer. Nat. Rev. Mol. Cell Biol. 9, 1004-1010
32. Mizushima, N., and Komatsu, M. (2011) Autophagy. Renovation of cells and tissues. Cell 147, 728-741
33. Sardiello, M., Palmieri, M., di Ronza, A., Medina, D. L., Valenza, M., Gen-narino, V. A., Di Malta, C., Donaudy, F., Embrione, V., Polishchuk, R. S., Banfi, S., Parenti, G., Cattaneo, E., and Ballabio, A. (2009) A gene network regulating lysosomal biogenesis and function. Science 325, 473-477
34. Palmieri, M., Impey, S., Kang, H., di Ronza, A., Pelz, C., Sardiello, M., and Ballabio, A. (2011) Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum. Mol. Genet. 20, 3852-3866
35. Song, W., Wang, F., Savini, M., Ake, A., di Ronza, A., Sardiello, M., and Segatori, L. (2013) TFEB regulates lysosomal proteostasis. Hum. Mol. Genet. 22, 1994-2009
36. Settembre, C., Di Malta, C., Polito, V. A., Garcia-Arencibia, M., Vetrini, F., Erdin, S., Erdin, S. U., Huynh, T., Medina, D., Colella, P., Sardiello, M., Rubinsztein, D. C., and Ballabio, A. (2011) TFEB Links Autophagy to Lys-osomal Biogenesis. Science 332, 1429-1433
37. Settembre, C., and Ballabio, A. (2011) TFEB regulates autophagy An integrated coordination of cellular degradation and recycling processes. Autophagy 7, 1379-1381
38. Sardiello, M., and Ballabio, A. (2009) Lysosomal enhancement A CLEAR answer to cellular degradative needs. Cell Cycle 8, 4021-4022
39. Pierret, C, Morrison, J. A., and Kirk, M. D. (2008) Treatment of lysosomal storage disorders: focus on the neuronal ceroid-lipofuscinoses. Acta Neu-robiol. Exp. 68, 429-442
40. Williams, R. E., and Mole, S. E. (2012) New nomenclature and classification scheme for the neuronal ceroid lipofuscinoses. Neurology 79, 183-191
41. Kohlschütter, A., and Schulz, A. (2009) Towards understanding the neuronal ceroid lipofuscinoses. Brain Dev. 31, 499-502
42. Persaud-Sawin, D. A., Mousallem, T., Wang, C, Zucker, A., Kominami, E., and Boustany, R. M. (2007) Neuronal ceroid lipofuscinosis. A common pathway? Pediatr. Res. 61, 146-152
43. Medina, D. L., Fraldi, A., Bouche, V., Annunziata, F., Mansueto, G., Spam-panato, C, Puri, C, Pignata, A., Martina, J. A., Sardiello, M., Palmieri, M., Polishchuk, R., Puertollano, R., and Ballabio, A. (2011) Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev. Cell 21, 421-430
44. Ghosh, A., Corbett, G.T., Gonzalez, F. J., andPahan, K. (2012) Gemfibrozil and fenofibrate, Food and Drug Administration-approved lipid-lowering drugs, up-regulate tripeptidyl-peptidase 1 in brain cells via peroxisome proliferator-activated receptor a. Implications for late infantile batten disease therapy. J. Biol. Chem. 287, 38922-38935
45. Wang, F., Song, W., Brancati, G., and Segatori, L. (2011) Inhibition of endoplasmic reticulum-associated degradation rescues native folding in loss of function protein misfolding diseases. J. Biol. Chem. 286, 43454-43464
46. Kondo, S., Kubota, S., Mukudai, Y., Moritani, N, Nishida, T., Matsushita, H., Matsumoto, S., Sugahara, T., and Takigawa, M. (2006) Hypoxic regulation of stability of connective tissue growth factor/CCN2 mRNA by 3'-untranslated region interacting with a cellular protein in human chondrosarcoma cells. Oncogene 25, 1099-1110
47. 2+ homeostasis in Gaucher's disease fibroblasts. A mechanism to rescue mutant glucocerebrosidase. Chem. Biol. 18, 766-776
48. Kabeya, Y., Mizushima, N, Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBOJ. 19, 5720-5728
49. Mizushima, N, Yoshimori, T., and Levine, B. (2010) Methods in mammalian autophagy research. Cell 140, 313-326
50. Sleat, D. E., Donnelly, R. J., Lackland, H., Liu, C. G., Sohar, I., Pullarkat, R. K., andLobel, P. (1997) Association of mutations in a lysosomal protein with classical late-infantile neuronal ceroid lipofuscinosis. Science 277, 1802-1805
51. Boya, P., González-Polo, R. A., Casares, N, Perfettini, J. L., Dessen, P., Larochette, N, Métivier, D., Meley, D., Souquere, S., Yoshimori, T., Pier-ron, G., Codogno, P., and Kroemer, G. (2005) Inhibition of macroau-tophagy triggers apoptosis. Mol. Cell. Biol. 25, 1025-1040
52. Cao, Y., Espinola, J. A., Fossale, E., Massey, A. C., Cuervo, A. M., Mac-Donald, M. E., and Cotman, S. L. (2006) Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J. Biol. Chem. 281, 20483-20493
53. Komatsu, M., Waguri, S., Ueno, T., Iwata, J., Murata, S., Tanida, I., Ezaki, J., Mizushima, N, Ohsumi, Y., Uchiyama, Y., Kominami, E., Tanaka, K., and Chiba, T. (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425-434
54. Bacus, S. S., Gudkov, A. V., Lowe, M., Lyass, L., Yung, Y., Komarov, A. P., Keyomarsi, K., Yarden, Y., and Seger, R. (2001) Taxol-induced apoptosis depends on MAP kinase pathways (ERK and p38) and is independent of p53. Oncogene 20, 147-155
55. Maxfield, F. R., and van Meer, G. (2010) Cholesterol, the central lipid of mammalian cells. Curr. Opin. Cell Biol. 22, 422-429
56. Settembre, C, Fraldi, A., Rubinsztein, D. C, and Ballabio, A. (2008) Lysosomal storage diseases as disorders of autophagy. Autophagy 4, 113-114
57. Futerman, A. H., and van Meer, G. (2004) The cell biology of lysosomal storage disorders. Nat Rev. Mol. Cell Biol. 5, 554-565