Ammonia: A diffusible factor released by proliferating cells that induces autophagy

Science Signaling

Volumn 3, Issue 124, 2010, Pages

  Mariño, Guillermo ^a,b,c   Kroemer, Guido ^a,b,c  

^a Institut Gustave Roussy   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; AMMONIA; GLUTAMATE DEHYDROGENASE; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; TUMOR NECROSIS FACTOR ALPHA;

AGING; AUTOPHAGY; CANCER CELL; CARCINOGENESIS; CELL PROLIFERATION; CYTOPLASM; HOMEOSTASIS; HUMAN; LONGEVITY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

AMMONIA; ANIMALS; AUTOPHAGY; CELL PROLIFERATION; GLUTAMINE; HUMANS; HYDROLASES; LYSOSOMES; NEOPLASMS;

MAMMALIA;

EID: 77953849832     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.3124pe19     Document Type: Review

References (35)

1. C. He, D. J. Klionsky, Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93 (2009).
2. G. Kroemer, B. Levine, Autophagic cell death: The story of a misnomer. Nat. Rev. Mol. Cell Biol. 9, 1004-1010 (2008).
3. M. Kundu, C. B. Thompson, Autophagy: Basic principles and relevance to disease. Annu. Rev. Pathol. 3, 427-455 (2008).
4. N. Mizushima, B. Levine, A. M. Cuervo, D. J. Klionsky, Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (2008).
5. G. Mariño, C. López-Otín, Autophagy: Molecular mechanisms, physiological functions and relevance in human pathology. Cell. Mol. Life Sci. 61, 1439-1454 (2004).
6. N. Mizushima, Physiological functions of autophagy. Curr. Top. Microbiol. Immunol. 335, 71-84 (2009).
7. F. Madeo, T. Eisenberg, G. Kroemer, Autophagy for the avoidance of neurodegeneration. Genes Dev. 23, 2253-2259 (2009).
8. H. W. Virgin, B. Levine, Autophagy genes in immunity. Nat. Immunol. 10, 461-470 (2009).
9. D. J. Klionsky, Autophagy: From phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8, 931-937 (2007).
10. S. Sarkar, B. Ravikumar, D. C. Rubinsztein, Autophagic clearance of aggregate-prone proteins associated with neurodegeneration. Methods Enzymol. 453, 83-110 (2009).
11. G. Mariño, A. P. Ugalde, N. Salvador-Montoliu, I. Varela, P. M. Quirós, J. Cadiñanos, I. van der Pluijm, J. M. Freije, C. López-Otín, Premature aging in mice activates a systemic metabolic response involving autophagy induction. Hum. Mol. Genet. 17, 2196-2211 (2008).
12. E. Morselli, M. C. Maiuri, M. Markaki, E. Megalou, A. Pasparaki, K. Palikaras, A. Criollo, L. Galluzzi, S. A. Malik, I. Vitale, M. Michaud, F. Madeo, N. Tavernarakis, G. Kroemer, The life span-prolonging effect of sirtuin-1 is mediated by autophagy. Autophagy 6, 186-188 (2010).
13. A. Meléndez, Z. Tallóczy, M. Seaman, E. L. Eskelinen, D. H. Hall, B. Levine, Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387-1391 (2003).
14. T. Eisenberg, H. Knauer, A. Schauer, S. Búttner, C. Ruckenstuhl, D. Carmona-Gutierrez, J. Ring, S. Schroeder, C. Magnes, L. Antonacci, H. Fussi, L. Deszcz, R. Hartl, E. Schraml, A. Criollo, E. Megalou, D. Weiskopf, P. Laun, G. Heeren, M. Breitenbach, B. Grubeck-Loebenstein, E. Herker, B. Fahrenkrog, K. U. Fröhlich, F. Sinner, N. Tavernarakis, N. Minois, G. Kroemer, F. Madeo, Induction of autophagy by spermidine promotes longevity. Nat. Cell Biol. 11, 1305-1314 (2009).
15. G. Kroemer, E. White, Autophagy for the avoidance of degenerative, inflammatory, infectious, and neoplastic disease. Curr. Opin. Cell Biol. 22, 121-123 (2010).
16. E. White, C. Karp, A. M. Strohecker, Y. Guo, R. Mathew, Role of autophagy in suppression of inflammation and cancer. Curr. Opin. Cell Biol. 22, 212-217 (2010).
17. X. Qu, J. Yu, G. Bhagat, N. Furuya, H. Hibshoosh, A. Troxel, J. Rosen, E. L. Eskelinen, N. Mizushima, Y. Ohsumi, G. Cattoretti, B. Levine, Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809-1820 (2003).
18. G. Mariño, N. Salvador-Montoliu, A. Fueyo, E. Knecht, N. Mizushima, C. López-Otín, Tissuespecific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J. Biol. Chem. 282, 18573-18583 (2007).
19. E. Morselli, L. Galluzzi, O. Kepp, J. M. Vicencio, A. Criollo, M. C. Maiuri, G. Kroemer, Anti- and protumor functions of autophagy. Biochim. Biophys. Acta 1793, 1524-1532 (2009).
20. N. Mizushima, A. Yamamoto, M. Matsui, T. Yoshimori, Y. Ohsumi, In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111 (2004).
21. A. Kuma, M. Hatano, M. Matsui, A. Yamamoto, H. Nakaya, T. Yoshimori, Y. Ohsumi, T. Tokuhisa, N. Mizushima, The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036 (2004).
22. C. H. Eng, K. Yu, J. Lucas, E. White, R. T. Abraham, Ammonia derived from glutaminolysis is a diffusible regulator of autophagy. Sci. Signal. 3, ra31 (2010).
23. M. Shanmugam, S. K. McBrayer, S. T. Rosen, Targeting the Warburg effect in hematological malignancies: From PET to therapy. Curr. Opin. Oncol. 21, 531-536 (2009).
24. M. G. Vander Heiden, L. C. Cantley, C. B. Thompson, Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 324, 1029-1033 (2009).
25. R. G. Jones, C. B. Thompson, Tumor suppressors and cell metabolism: A recipe for cancer growth. Genes Dev. 23, 537-548 (2009).
26. T. A. Brooks, L. H. Hurley, The role of supercoiling in transcriptional control of MYC and its importance in molecular therapeutics. Nat. Rev. Cancer 9, 849-861 (2009).
27. C. V. Dang, Rethinking the Warburg effect with Myc micromanaging glutamine metabolism. Cancer Res. 70, 859-862 (2010).
28. J. D. Gordan, C. B. Thompson, M. C. Simon, HIF and c-Myc: Sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 12, 108-113 (2007).
29. C. V. Dang, A. Le, P. Gao, MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin. Cancer Res. 15, 6479-6483 (2009).
30. M. Yuneva, N. Zamboni, P. Oefner, R. Sachidanandam, Y. Lazebnik, Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J. Cell Biol. 178, 93-105 (2007).
31. M. C. Maiuri, E. Tasdemir, A. Criollo, E. Morselli, J. M. Vicencio, R. Carnuccio, G. Kroemer, Control of autophagy by oncogenes and tumor suppressor genes. Cell Death Differ. 16, 87-93 (2009).
32. M. N. Corradetti, K. L. Guan, Upstream of the mammalian target of rapamycin: Do all roads pass through mTOR? Oncogene 25, 6347-6360 (2006).
33. D. D. Sarbassov, S. M. Ali, D. M. Sabatini, Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17, 596-603 (2005).
34. A. Mian, B. Lee, Urea-cycle disorders as a paradigm for inborn errors of hepatocyte metabolism. Trends Mol. Med. 8, 583-589 (2002).
35. Funding: The authors' work is supported by the European Molecular Biology Organization, Ligue contre le Cancer, Institut National contre le Cancer, Agence National pour la Recherche, and the European Union.