Lysosomal biogenesis and function is critical for necrotic cell death in Caenorhabditis elegans

Journal of Cell Biology

Volumn 173, Issue 2, 2006, Pages 231-239

  Artal Sanz, Marta ^a   Samara, Chrysanthi ^a   Syntichaki, Popi ^a   Tavernarakis, Nektarios ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ACIDIFICATION; ALKALINITY; ALKALINIZATION; APOPTOSIS; ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; CELL COMPARTMENTALIZATION; CELL DEATH; CELL FUNCTION; CELL LABELING; CELL MIGRATION; CELL NUCLEUS MEMBRANE; CELL STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENDOSOME; FLUORESCENCE ANALYSIS; GENE FUNCTION; GENE MUTATION; GENETIC CONSERVATION; LYSOSOME MEMBRANE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ASPARTIC ENDOPEPTIDASES; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CALPAIN; CELL DEATH; ENDOSOMES; LYSOSOMES; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; NECROSIS; PLASMIDS;

CAENORHABDITIS ELEGANS; METAZOA;

EID: 33646081999     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200511103     Document Type: Article

References (52)

1. Artal-Sanz, M., and N. Tavernarakis. 2005. Proteolytic mechanisms in necrotic cell death and neurodegeneration. FEBS Lett. 579:3287-3296.
2. Bakker, A.C., P. Webster, W.A. Jacob, and N.W. Andrews. 1997. Homotypic fusion between aggregated lysosomes triggered by elevated [Ca2+]i in fibroblasts. J. Cell Sci. 110:2227-2238.
3. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77:71-94.
4. Burkhardt, J.K., C.J. Echeverri, T. Nilsson, and R.B. Vallee. 1997. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139:469-484.
5. Carafoli, E. 2002. Calcium signaling: a tale for all seasons. Proc. Natl. Acad. Sci. USA. 99:1115-1122.
6. Eskelinen, E.L., Y. Tanaka, and P. Saftig. 2003. At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13:137-145.
7. Fares, H., and I. Greenwald. 2001. Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat. Genet. 28:64-68.
8. Ferri, K.F., and G. Kroemer. 2001. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3:E255-E263.
9. Fire, A., S.W. Harrison, and D. Dixon. 1990. A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene. 93:189-198.
10. Goll, D.E., V.F. Thompson, H. Li, W. Wei, and J. Cong. 2003. The calpain system. Physiol. Rev. 83:731-801.
11. Hall, D.H., G. Gu, J. Garcia-Anoveros, L. Gong, M. Chalfie, and M. Driscoll. 1997. Neuropathology of degenerative cell death in Caenorhabditis elegans. J. Neurosci. 17:1033-1045.
12. Hermann, G.J., L.K. Schroeder, C.A. Hieb, A.M. Kershner, B.M. Rabbitts, P. Fonarev, B.D. Grant, and J.R. Priess. 2005. Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol. Biol. Cell. 16:3273-3288.
13. Hersh, B.M., E. Hartwieg, and H.R. Horvitz. 2002. The Caenorhabditis elegans mucolipin-like gene cup-5 is essential for viability and regulates lysosomes in multiple cell types. Proc. Natl. Acad. Sci. USA. 99:4355-4360.
14. Hughes, E.N., and J.T. August. 1982. Murine cell surface glycoproteins. Identification, purification, and characterization of a major glycosylated component of 110,000 daltons by use of a monoclonal antibody. J. Biol. Chem. 257:3970-3977.
15. Ishidoh, K., and E. Kominami. 2002. Processing and activation of lysosomal proteinases. Biol. Chem. 383:1827-1831.
16. Jacobson, L.A., L. Jen-Jacobson, J.M. Hawdon, G.P. Owens, M.A. Bolanowski, S.W. Emmons, M.V. Shah, R.A. Pollock, and D.S. Conklin. 1988. Identification of a putative structural gene for cathepsin D in Caenorhabditis elegans. Genetics. 119:355-363.
17. Kamath, R.S., M. Martinez-Campos, P. Zipperlen, A.G. Fraser, and J. Ahringer. 2001. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. DOI:10.1186/gb-2000-2-1-research0002.
18. Kostich, M., A. Fire, and D.M. Fambrough. 2000. Identification and molecular-genetic characterization of a LAMP/CD68-like protein from Caenorhabditis elegans. J. Cell Sci. 113:2595-2606.
19. Kroemer, G., and M. Jaattela. 2005. Lysosomes and autophagy in cell death control. Nat. Rev. Cancer. 5:886-897.
20. Lee, J.M., G.J. Zipfel, and D.W. Choi. 1999. The changing landscape of ischaemic brain injury mechanisms. Nature. 399:A7-14.
21. Li, J.Z., M.P. Vawter, D.M. Walsh, H. Tomita, S.J. Evans, P.V. Choudary, J.F. Lopez, A. Avelar, V. Shokoohi, T. Chung, et al. 2004. Systematic changes in gene expression in postmortem human brains associated with tissue pH and terminal medical conditions. Hum. Mol. Genet. 13:609-616.
22. Lippincott-Schwartz, J., and D.M. Fambrough. 1986. Lysosomal membrane dynamics: structure and interorganellar movement of a major lysosomal membrane glycoprotein. J. Cell Biol. 102:1593-1605.
23. Lipton, S.A., and P. Nicotera. 1998. Calcium, free radicals and excitotoxins in neuronal apoptosis. Cell Calcium. 23:165-171.
24. Llewellyn, D.H., S. Johnson, and P. Eggleton. 2000. Calreticulin comes of age. Trends Cell Biol. 10:399-402.
25. Martin, L.J. 2001. Neuronal cell death in nervous system development, disease, and injury. Int. J. Mol. Med. 7:455-478.
26. Mattson, M.P., F.M. LaFerla, S.L. Chan, M.A. Leissring, P.N. Shepel, and J.D. Geiger. 2000. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23:222-229.
27. Michalak, M., E.F. Corbett, N. Mesaeli, K. Nakamura, and M. Opas. 1999. Calreticulin: one protein, one gene, many functions. Biochem. J. 344:281-292.
28. Nehrke, K., and J.E. Melvin. 2002. The NHX family of Na+-H+ exchangers in Caenorhabditis elegans. J. Biol. Chem. 277:29036-29044.
29. Nicotera, P., and D. Bano. 2003. The enemy at the gates. Ca2+ entry through TRPM7 channels and anoxic neuronal death. Cell. 115:768-770.
30. Nicotera, P., M. Leist, and L. Manzo. 1999. Neuronal cell death: a demise with different shapes. Trends Pharmacol. Sci. 20:46-51.
31. Nunes, F., M. Wolf, J. Hartmann, and R.J. Paul. 2005. The ABC transporter PGP-2 from Caenorhabditis elegans is expressed in the sensory neuron pair AWA and contributes to lysosome formation and lipid storage within the intestine. Biochem. Biophys. Res. Commun. 338:862-871.
32. Oka, T., and M. Futai. 2000. Requirement of V-ATPase for ovulation and embryogenesis in Caenorhabditis elegans. J. Biol. Chem. 275:29556-29561.
33. Paschen, W. 2001. Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium. 29:1-11.
34. Pujol, N., C. Bonnerot, J.J. Ewbank, Y. Kohara, and D. Thierry-Mieg. 2001. The Caenorhabditis elegans unc-32 gene encodes alternative forms of a vacuolar ATPase a subunit. J. Biol. Chem. 276:11913-11921.
35. Sapolsky, R.M., J. Trafton, and G.C. Tombaugh. 1996. Excitotoxic neuron death, acidotic endangerment, and the paradox of acidotic protection. Adv. Neurol. 71:237-244.
36. Sattler, R., and M. Tymianski. 2000. Molecular mechanisms of calcium-dependent excitotoxicity. J. Mol. Med. 78:3-13.
37. Scott, B.A., M.S. Avidan, and C.M. Crowder. 2002. Regulation of hypoxic death in C. elegans by the insulin/IGF receptor homolog DAF-2. Science. 296:2388-2391.
38. Syntichaki, P., and N. Tavernarakis. 2002. Death by necrosis: uncontrollable catastrophe, or is there order behind the chaos? EMBO Rep. 3:604-609.
39. Syntichaki, P., and N. Tavernarakis. 2003. The biochemistry of neuronal necrosis: rogue biology? Nat. Rev. Neurosci. 4:672-684.
40. Syntichaki, P., K. Xu, M. Driscoll, and N. Tavernarakis. 2002. Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature. 419:939-944.
41. Syntichaki, P., C. Samara, and N. Tavernarakis. 2005. The vacuolar H+-ATPase mediates intracellular acidification required for neurodegeneration in C. elegans. Curr. Biol. 15:1249-1254.
42. Takemura, H., A.R. Hughes, O. Thastrup, and J.W. Putney Jr. 1989. Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane. J. Biol. Chem. 264:12266-12271.
43. Treusch, S., S. Knuth, S.A. Slaugenhaupt, E. Goldin, B.D. Grant, and H. Fares. 2004. Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc. Natl. Acad. Sci. USA. 101:4483-4488.
44. Walker, N.I., B.V. Harmon, G.C. Gobe, and J.F. Kerr. 1988. Patterns of cell death. Methods Achiev. Exp. Pathol. 13:18-54.
45. Xu, K., N. Tavernarakis, and M. Driscoll. 2001. Necrotic cell death in C. elegans requires the function of calreticulin and regulators of Ca(2+) release from the endoplasmic reticulum. Neuron. 31:957-971.
46. Yamashima, T. 2000. Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog. Neurobiol. 62:273-295.
47. Yamashima, T. 2004. Ca2+-dependent proteases in ischemic neuronal death: a conserved 'calpain-cathepsin cascade' from nematodes to primates. Cell Calcium. 36:285-293.
48. Yamashima, T., Y. Kohda, K. Tsuchiya, T. Ueno, J. Yamashita, T. Yoshioka, and E. Kominami. 1998. Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis'. Eur. J. Neurosci. 10:1723-1733.
49. Yamashima, T., A.B. Tonchev, T. Tsukada, T.C. Saido, S. Imajoh-Ohmi, T. Momoi, and E. Kominami. 2003. Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus. 13:791-800.
50. Yoshida, M., T. Yamashima, L. Zhao, K. Tsuchiya, Y. Kohda, A.B. Tonchev, M. Matsuda, and E. Kominami. 2002. Primate neurons show different vulnerability to transient ischemia and response to cathepsin inhibition. Acta Neuropathol. (Berl.). 104:267-272.
51. Yu, G., R. Zucchi, S. Ronca-Testoni, and G. Ronca. 2000. Protection of ischemic rat heart by dantrolene, an antagonist of the sarcoplasmic reticulum calcium release channel. Basic Res. Cardiol. 95:137-143.
52. Zhao, H.F., X. Wang, and G.J. Zhang. 2005. Lysosome destabilization by cytosolic extracts, putative involvement of Ca(2+)/phospholipase C. FEBS Lett. 579:1551-1556.