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A substrate-specific mTORC1 pathway underlies Birt–Hogg–Dubé syndrome

Napolitano, Gennaro, Di Malta, Chiara, Esposito, Alessandra, de Araujo, Mariana E. G., Pece, Salvatore, Bertalot, Giovanni, Matarese, Maria, Benedetti, Valerio, Zampelli, Angela, Stasyk, Taras, Siciliano, Diletta, Venuta, Alessandro, Cesana, Marcella, Vilardo, Claudia, Nusco, Edoardo, Monfregola, Jlenia, Calcagnì, Alessia, Di Fiore, Pier Paolo, Huber, Lukas A., Ballabio, Andrea·2020·Nature
DOI 10.1038/s41586-020-2444-0PMC PMC7610377
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Citations

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Research works printed but not linked: 38

  1. Ben-Sahra, I. & Manning, B. D. mTORC1 signaling and the metabolic control of cell growth. Curr. Opin. Cell Biol. 45, 72–82 (2017). · DOI
  2. González, A. & Hall, M. N. Nutrient sensing and TOR signaling in yeast and mammals. EMBO J. 36, 397–408 (2017). · DOI
  3. Sardiello, M. et al. A gene network regulating lysosomal biogenesis and function. Science 325, 473–477 (2009). · DOI · Paper page
  4. Schmidt, L. S. & Linehan, W. M. FLCN: the causative gene for Birt–Hogg–Dubé syndrome. Gene 640, 28–42 (2018). · DOI
  5. Schmidt, L. S. & Linehan, W. M. Molecular genetics and clinical features of Birt–Hogg–Dubé syndrome. Nat. Rev. Urol. 12, 558–569 (2015). · DOI
  6. Long, X., Lin, Y., Ortiz-Vega, S., Yonezawa, K. & Avruch, J. Rheb binds and regulates the mTOR kinase. Curr. Biol. 15, 702–713 (2005). · DOI · Paper page
  7. Tee, A. R., Manning, B. D., Roux, P. P., Cantley, L. C. & Blenis, J. Tuberous sclerosis complex gene products, tuberin and hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr. Biol. 13, 1259–1268 (2003). · DOI · Paper page
  8. Sancak, Y. et al. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320, 1496–1501 (2008). · DOI · Paper page
  9. Tsun, Z. Y. et al. The folliculin tumor suppressor is a GAP for the RagC/D GTPases that signal amino acid levels to mTORC1. Mol. Cell 52, 495–505 (2013). · DOI · Paper page
  10. Lawrence, R. E. et al. Structural mechanism of a Rag GTPase activation checkpoint by the lysosomal folliculin complex. Science 366, 971–977 (2019). · DOI · Paper page
  11. Shen, K. et al. Cryo-EM structure of the human FLCN–FNIP2–Rag–Ragulator complex. Cell 179, 1319–1329.e8 (2019). · DOI
  12. Settembre, C. et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31, 1095–1108 (2012). · DOI · Paper page
  13. Martina, J. A., Chen, Y., Gucek, M. & Puertollano, R. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy 8, 903–914 (2012). · DOI · Paper page
  14. Roczniak-Ferguson, A. et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 5, ra42 (2012). · DOI
  15. Napolitano, G. et al. mTOR-dependent phosphorylation controls TFEB nuclear export. Nat. Commun. 9, 3312 (2018). · DOI · Paper page
  16. Medina, D. L. et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat. Cell Biol. 17, 288–299 (2015). · DOI
  17. Ballabio, A. & Bonifacino, J. S. Lysosomes as dynamic regulators of cell and organismal homeostasis. Nat. Rev. Mol. Cell Biol. 21, 101–118 (2019). · DOI · Paper page
  18. Di Malta, C. et al. Transcriptional activation of RagD GTPase controls mTORC1 and promotes cancer growth. Science 356, 1188–1192 (2017). · DOI
  19. Martina, J. A. & Puertollano, R. Rag GTPases mediate amino acid-dependent recruitment of TFEB and MITF to lysosomes. J. Cell Biol. 200, 475–491 (2013). · DOI · Paper page
  20. Schalm, S. S. & Blenis, J. Identification of a conserved motif required for mTOR signaling. Curr. Biol. 12, 632–639 (2002). · DOI
  21. Schalm, S. S., Fingar, D. C., Sabatini, D. M. & Blenis, J. TOS motif-mediated raptor binding regulates 4E-BP1 multisite phosphorylation and function. Curr. Biol. 13, 797–806 (2003). · DOI
  22. Lawrence, R. E. et al. A nutrient-induced affinity switch controls mTORC1 activation by its Rag GTPase–Ragulator lysosomal scaffold. Nat. Cell Biol. 20, 1052–1063 (2018). · DOI
  23. Baba, M. et al. Kidney-targeted Birt–Hogg–Dubé gene inactivation in a mouse model: Erk1/2 and Akt–mTOR activation, cell hyperproliferation, and polycystic kidneys. J. Natl. Cancer Inst. 100, 140–154 (2008). · DOI
  24. Chen, J. et al. Deficiency of FLCN in mouse kidney led to development of polycystic kidneys and renal neoplasia. PLoS ONE 3, e3581 (2008). · DOI
  25. Palmieri, M. et al. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum. Mol. Genet. 20, 3852–3866 (2011). · DOI · Paper page
  26. Wada, S. et al. The tumor suppressor FLCN mediates an alternate mTOR pathway to regulate browning of adipose tissue. Genes Dev. 30, 2551–2564 (2016). · DOI
  27. Anandapadamanaban, M. et al. Architecture of human Rag GTPase heterodimers and their complex with mTORC1. Science 366, 203–210 (2019). · DOI · Paper page
  28. Rogala, K. B. et al. Structural basis for the docking of mTORC1 on the lysosomal surface. Science 366, 468–475 (2019). · DOI · Paper page
  29. Kauffman, E. C. et al. Molecular genetics and cellular features of TFE3 and TFEB fusion kidney cancers. Nat. Rev. Urol. 11, 465–475 (2014). · DOI
  30. Calcagnì, A. et al. Modelling TFE renal cell carcinoma in mice reveals a critical role of WNT signaling. eLife 5, e17047 (2016). · DOI
  31. Perera, R. M., Di Malta, C. & Ballabio, A. MiT/TFE family of transcription factors, lysosomes, and cancer. Annu Rev Cancer Biol 3, 203–222 (2019). · DOI
  32. Baba, M. et al. Folliculin encoded by the BHD gene interacts with a binding protein, FNIP1, and AMPK, and is involved in AMPK and mTOR signaling. Proc. Natl Acad. Sci. USA 103, 15552–15557 (2006). · DOI
  33. Mansueto, G. et al. Transcription factor EB controls metabolic flexibility during exercise. Cell Metab. 25, 182–196 (2017). · DOI · Paper page
  34. Endoh, M. et al. A FLCN–TFE3 feedback loop prevents excessive glycogenesis and phagocyte activation by regulating lysosome activity. Cell Rep. 30, 1823–1834 (2020). · DOI
  35. Possik, E. et al. FLCN and AMPK confer resistance to hyperosmotic stress via remodeling of glycogen stores. PLoS Genet. 11, e1005520 (2015). · DOI
  36. Kawakami, K. Tol2: a versatile gene transfer vector in vertebrates. Genome Biol. 8, S7 (2007). · DOI
  37. Napolitano, G. et al. Impairment of chaperone-mediated autophagy leads to selective lysosomal degradation defects in the lysosomal storage disease cystinosis. EMBO Mol. Med. 7, 158–174 (2015). · DOI
  38. Shao, X., Johnson, J. E., Richardson, J. A., Hiesberger, T. & Igarashi, P. A minimal Ksp-cadherin promoter linked to a green fluorescent protein reporter gene exhibits tissue-specific expression in the developing kidney and genitourinary tract. J. Am. Soc. Nephrol. 13, 1824–1836 (2002). · DOI

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Metadata

Authors
Napolitano, G., Di Malta, C., Esposito, A., de Araujo, M. E. G., Pece, S., Bertalot, G., Matarese, M., Benedetti, V., Zampelli, A., Stasyk, T., Siciliano, D., Venuta, A., Cesana, M., Vilardo, C., Nusco, E., Monfregola, J., Calcagnì, A., Di Fiore, P. P., Huber, L. A., & Ballabio, A.
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2020-07-01
Volume
585
Issue
7826
Pages
597-602
ISSN
  • 0028-0836
  • 1476-4687
DOI
10.1038/s41586-020-2444-0
PMC
PMC7610377
Cited by
341
References
10
Language
en
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