Transient receptor potential vanilloid 1 activation induces autophagy in thymocytes through ROS-regulated AMPK and Atg4C pathways

Journal of Leukocyte Biology

Volumn 92, Issue 3, 2012, Pages 421-431

  Farfariello, Valerio ^a,b   Amantini, Consuelo ^a   Santoni, Giorgio ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Cellular adaptation; Ion channels; Macroautophagy; Oxidative stress; T cell precursors

Indexed keywords

3 METHYLADENINE; ATG4C PROTEIN; BECLIN 1; CALCIUM ION; CAPSAICIN; CASPASE 3; CD4 ANTIGEN; CD8ALPHA ANTIGEN; CELL PROTEIN; GUANOSINE TRIPHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; PROTEIN BCL XL; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL MATURATION; CELL SUBPOPULATION; CELL SURVIVAL; CELLULAR STRESS SIGNAL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION; HOMEOSTASIS; MALE; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; THYMOCYTE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; CYSTEINE ENDOPEPTIDASES; DNA FRAGMENTATION; ENZYME ACTIVATION; FLOW CYTOMETRY; IMMUNOPRECIPITATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN KINASES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; THYMOCYTES; TRPV CATION CHANNELS;

MUS MUSCULUS;

EID: 84865494019     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0312123     Document Type: Article

References (40)

1. Levine, B., Klionsky, D. J. (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463477.
2. Kroemer, G., Levine, B. (2008) Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell. Biol. 9, 1004-1010.
3. Ravikumar, B., Sarkar, S., Davies, J. E., Futter, M., Garcia-Arencibia, M., Green-Thompson, Z. W., Jimenez-Sanchez, M., Korolchuk, V. I., Lichten-berg, M., Luo, S., Massey, D. C., Menzies, F. M., Moreau, K., Narayanan, U., Renna, M., Siddiqi, F. H., Underwood, B. R., Winslow, A. R., Rubin-sztein, D. C. (2010) Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 90, 1383-1435.
4. Arsov, I., Li, X., Matthews, G., Coradin, J., Hartmann, B., Simon, A. K, Sealfon, S. C., Yue, Z. (2008) BAC-mediated transgenic expression of fluorescent autophagic protein Beclin 1 reveals a role for Beclin 1 in lymphocyte development. Cell Death Differ. 15, 1385-1395.
5. Stephenson, L. M., Miller, B. C., Ng, A., Eisenberg, J., Zhao, Z., Cadwell, K, Graham, D. B., Mizushima, N. N., Xavier, R., Virgin, H. W., Swat, W. (2009) Identification of Atg5-dependent transcriptional changes and increases in mitochondrial mass in Atg5-deficient T lymphocytes. Autophagy 5, 625-635.
6. Li, C., Capan, E., Zhao, Y., Zhao, J., Stolz, D., Watkins, S. C., Jin, S., Lu, B. (2006) Autophagy is induced in CD4+ T cells and important for the growth factor-withdrawal cell death. J. Immunol. 177, 5163-5168.
7. Bell, B. D., Leverrier, S., Weist, B. M., Newton, R. H., Arechiga, A. F., Luhrs, K A., Morrissette, N. S., Walsh, C. M. (2008) FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells. Proc. Natl. Acad. Sci. USA 105, 16677-16682.
8. Feng, C. G., Zheng, L., Jankovic, D., Bafica, A., Cannons, J. L., Watford, W. T., Chaussabel, D., Hieny, S., Caspar, P., Schwartzberg, P. L., Lena-rdo, M. J., Sher, A. (2008) The immunity-related GTPase Irgm1 promotes the expansion of activated CD4+ T cell populations by preventing interferon-γ-induced cell death. Nat. Immunol. 9, 1279-1287.
9. Miller, B. C., Zhao, Z., Stephenson, L. M., Cadwell, K, Pua, H. H., Lee, H. K, Mizushima, N. Iwasaki, A., He, Y. W., Swat, W., Virgin IV, H. W. (2008) The autophagy gene ATG5 plays an essential role in B lymphocyte development. Autophagy 4, 309-314.
10. Pua, H. H., Dzhagalov, I., Chuck, M., Mizushima, N., He, Y. W. (2007) A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J. Exp. Med. 204, 25-31.
11. Nedjic, J., Aichinger, M., Emmerich, J., Mizushima, N., Klein, L. (2008) Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 455, 396-400.
12. Arsov, I., Adebayo, A., Kucerova-Levisohn, M., Haye, J., MacNeil, M., Pa-pavasiliou, F. N., Yue, Z., Ortiz, B. D. (2011) A role for autophagic protein Beclin 1 early in lymphocyte development. J. Immunol. 186, 22012209.
13. Wenning, A. S., Neblung, K, Strauss, B., Wolfs, M. J., Sappok, A., Hoth, M., Schwarz, E. C. (2011) TRP expression pattern and the functional importance of TRPC3 in primary human T-cells. Biochim. Biophys. Acta 1813, 412-423.
14. Jin, J., Desai, B. N., Navarro, B., Donovan, A., Andrews, N. C., Clapham, D. E., (2008) Deletion of Trpm7 disrupts embryonic development and thymopoiesis without altering Mg2+ homeostasis. Science 322, 756-760.
15. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., Julius, D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824.
16. Vriens, J., Appendino, G., B. Nilius (2009) Pharmacology of vanilloid transient receptor potential cation channels. Mol. Pharmacol. 75, 12621279.
17. Juzan, M., Hostein, I., Gualde, N. (1992) Role of thymus-eicosanoids in the immune response. Prostaglandins Leukot. Essent. Fatty Acids 46, 247255.
18. Amantini, C., Mosca, M., Lucciarini, R., Perfumi, M., Morrone, S., Pic-coli, M., Santoni, G. (2004) Distinct thymocyte subsets express the vanil-loid receptor VR1 that mediates capsaicin-induced apoptotic cell death. Cell Death Differ. 11, 1342-1356.
19. Oh, S. H., Lim, S. C. (2009) Endoplasmic reticulum stress-mediated au-tophagy/apoptosis induced by capsaicin (8-methyl-N-vanillyl-6-nonen-amide) and dihydrocapsaicin is regulated by the extent of c-Jun NH2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells. J. Pharmacol. Exp. Ther. 329, 112-122.
20. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., 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.
21. Yue, Z., Jin, S., Yang, C., Levine, A. J., Heintz, N. (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploin-sufficient tumor suppressor. Proc. Natl. Acad. Sci. USA 100, 15077-15082.
22. Shvets, E., Elazar, Z. (2009) Flow cytometric analysis of autophagy in living mammalian cells. Methods Enzymol. 452, 131-141.
23. Graf, M. R., Jia, W., Johnson, R. S., Dent, P., Mitchell, C., Loria, R. M. (2009) Autophagy and the functional roles of Atg5 and Beclin-1 in the anti-tumor effects of 3β androstene 1α diol neuro-steroid on malignant glioma cells. J. Steroid Biochem. Mol. Biol. 115, 137-145.
24. Hail Jr., N. (2003) Mechanisms of vanilloid-induced apoptosis. Apoptosis 8, 251-262.
25. Wang, C., Hu, H. Z., Colton, C. K., Wood, J. D., Zhu, M. X. (2004) An alternative splicing product of the murine trpv1 gene dominant negatively modulates the activity of TRPV1 channels. J. Biol. Chem. 279, 37423-37430.
26. Prasad, A., Bloom, M. S., Carpenter, D. O. (2010) Role of calcium and ROS in cell death induced by polyunsaturated fatty acids in murine thymocytes. Cell. Physiol. 225, 829-836.
27. Alexander, A., Cai, S. L., Kim, J., Nanez, A., Sahin, M., MacLean, K H., Inoki, K, Guan, K L., Shen, J., Person, M. D., Kusewitt, D., Mills, G. B., Kastan, M. B., Walker, C. L. (2010) ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc. Natl. Acad. Sci. USA 107, 4153-4158.
28. Sanz, P. (2008) AMP-activated protein kinase: structure and regulation. Curr. Protein Pept. Sci. 9, 478-492.
29. Scherz-Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L., Elazar, Z. (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 26, 1749-1760.
30. Furuya, N., Liang, X. H., Levine, B. (2004) Autophagy and cancer. In Autophagy (D.J. Klionsky, ed.), Landes Bioscience, Georgetown, TX, USA, 241-255.
31. Brookes, P. S., Yoon, Y., Robotham, J. L., Anders, M. W., Sheu, S. S. (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell. Physiol. 287, C817-C833.
32. Hu, F., Sun, W. W., Zhao, X. T., Cui, Z. J., Yang, W. X. (2008) TRPV1 mediates cell death in rat synovial fibroblasts through calcium entry-dependent ROS production and mitochondrial depolarization. Biochem. Biophys. Res. Commun. 369, 989-993.
33. H0yer-Hansen, M., Bastholm, L., Szyniarowski, P., Campanella, M., Sz-abadkai, G., Farkas, T., Bianchi, K, Fehrenbacher, N., Elling, F., Riz-zuto, R., Mathiasen, I. S., Jaattela, M. (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-β, and Bcl-2. Mol. Cell 25, 193-205.
34. Marino, G., Uria, J. A., Puente, X. S., Quesada, V., Bordallo, J., Lopez-Otin, C. (2003) Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J. Biol. Chem. 278, 3671-3678.
35. Marino, G., Salvador-Montoliu, N., Fueyo, A., Knecht, E., Mizushima, N., Lopez-Otin, C. (2007) Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J. Biol. Chem. 282, 18573-18583.
36. Djavaheri-Mergny, M., Amelotti, M., Mathieu, J., Besangon, F., Bauvy, C., Souquere, S., Pierron, G., Codogno, P. (2006) NF-kB activation represses tumor necrosis factor-a-induced autophagy. J. Biol. Chem. 281, 30373-30382.
37. Kersh, G. J., Hedrick, S. M. (1995) Role of TCR specificity in CD4 versus CD8 lineage commitment. J. Immunol. 154, 1057-1068.
38. McGargill, M. A., Hogquist, K A. (1999) Antigen-induced coreceptor down-regulation on thymocytes is not a result of apoptosis. J. Immunol. 162, 1237-1245.
39. Hostein, I., Dorion-Bonnet, F., Bloch, B., Vaillier, D., Juzan, M., Gualde, N. (1992) 5-Lipoxygenase gene expression in the thymus. Thymus 20, 101-108.
40. Valk, P., Verbakel, S., Vankan, Y., Hol, S., Mancham, S., Ploemacher, R., Mayen, A., Lowenberg, B., Delwel, R. (1997) Anandamide, a natural ligand for the peripheral cannabinoid receptor is a novel synergistic growth factor for hematopoietic cells. Blood 90, 1448-1457.