Macroautophagy-dependent, intralysosomal cleavage of a betaine homocysteine methyltransferase fusion protein requires stable multimerization

Autophagy

Volumn 4, Issue 2, 2008, Pages 185-194

  Mercer, Carol A ^a   Kaliappan, Alagammai ^a   Dennis, Patrick B ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Autophagosomes; Betaine homocysteine methyltransferase; Cargo based assay; Macroautophagy; Multimerization

Indexed keywords

BETAINE HOMOCYSTEINE METHYLTRANSFERASE; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; MUTANT PROTEIN; OLIGOMER; PROTEINASE;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CATALYSIS; CELL FRACTIONATION; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LYSOSOME; MAMMAL CELL; MOUSE; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PROTEIN DEGRADATION; PROTEIN QUATERNARY STRUCTURE; PROTEOMICS; STARVATION;

MAMMALIA;

EID: 38949146398     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.5275     Document Type: Article

References (50)

1. Noda T, Matsuura A, Wada Y, Ohsumi Y. Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem Biophys Res Commun 1995; 210:126-32.
2. Cheong H, Yorimitsu T, Reggiori F, Legakis JE, Wang CW, Klionsky DJ. Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell 2005; 16:3438-53.
3. Reggiori F, Klionsky DJ. Aurophagy in the eukaryotic cell. Eukaryot Cell 2002; 1:11-21.
4. Klionsky DJ. The molecular machinery of autophagy: Unanswered questions. J Cell Sci 2005; 118:7-18.
5. Mizushima N, Ohsumi Y, Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct Funct 2002; 27:421-9.
6. Ashford TP, Porter KR. Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 1962; 12:198-202.
7. Biederbick A, Kern HF, Elsasser HP. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 1995; 66:3-14.
8. Poso AR, Surmacz CA, Mortimore GE. Inhibition of intracellular protein degradation by ethanol in perfused rat liver. Biochem J 1987; 242:459-64.
9. Kopitz J, Kisen GO, Gordon PB, Bohley P, Seglen PO. Nonselective autophagy of cytosolic enzymes by isolated rat hepatocytes. J Cell Biol 1990; 111:941-53.
10. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004; 36:2491-502.
11. Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy 2007; 3:181-206.
12. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J 2000; 19:5720-8.
13. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 2005; 1:84-91.
14. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3.
15. Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D, Pablo RD, Tacchetti C, Rubinsztein DC, Ballabio A. A block of autophagy in lysosomal storage disorders. Hum Mol Genet 2007.
16. Tanida I, Ueno T, Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 2004; 36:2503-18.
17. Ueno T, Ishidoh K, Mineki R, Tanida I, Murayama K, Kadowaki M, Kominami E. Autolysosomal membrane-associated betaine homocysteine methyltransferase: Limited degradation fragment of a sequestered cytosolic enzyme monitoring autophagy. J Biol Chem 1999; 274:15222-9.
18. Millian NS, Garrow TA. Human betaine-homocysteine methyltransferase is a zinc metalloenzyme. Arch Biochem Biophys 1998; 356:93-8.
19. Sandu C, Nick P, Hess D, Schiltz E, Garrow TA, Brandsch R. Association of betaine-homocysteine S-methyltransferase with microtubules. Biol Chem 2000; 381:619-22.
20. Sehayek E, Wang R, Ono JG, Zinchuk VS, Duncan EM, Shefer S, Vance DE, Ananthanarayanan M, Chait BT, Breslow JL. Localization of the PE methylation pathway and SR-BI to the canalicular membrane: Evidence for apical PC biosynthesis that may promote biliary excretion of phospholipid and cholesterol. J Lipid Res 2003; 44:1605-13.
21. Furuya N, Kanazawa T, Fujimura S, Ueno T, Kominami E, Kadowaki M. Leupeptin-induced appearance of partial fragment of betaine homocysteine methyltransferase during autophagic maturation in rat hepatocytes. J Biochem (Tokyo) 2001; 129:313-20.
22. Overbye A, Fengsrud M, Seglen PO. Proteomic analysis of membrane-associated proteins from rat liver autophagosomes. Autophagy 2007; 3:300-22.
23. Szegedi SS, Garrow TA. Oligomerization is required for betaine-homocysteine S-methyltransferase function. Arch Biochem Biophys 2004; 426:32-42.
24. Gonzalez B, Pajares MA, Martinez-Ripoll M, Blundell TL, Sanz-Aparicio J. Crystal structure of rat liver betaine homocysteine s-methyltransferase reveals new oligomerization features and conformational changes upon substrate binding. J Mol Biol 2004; 338:771-82.
25. Chen CA, Okayama H. Calcium phosphate-mediated gene transfer: A highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques 1988; 6:632-8.
26. Young AR, Chan EY, Hu XW, Kochl R, Crawshaw SG, High S, Hailey DW, Lippincott-Schwartz J, Tooze SA. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 2006; 119:3888-900.
27. Codogno P, Meijer AJ. Autophagy and signaling: Their role in cell survival and cell death. Cell Death Differ 2005; 12(Suppl 2):1509-18.
28. Schneider P, Korolenko TA, Busch U. A review of drug-induced lysosomal disorders of the liver in man and laboratory animals. Microsc Res Tech 1997; 36:253-75.
29. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 1991; 266:17707-12.
30. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 2000; 275:992-8.
31. Kroemer G, Jaattela M. Lysosomes and autophagy in cell death control. Nat Rev Cancer 2005; 5:886-97.
32. Shintani T, Klionsky DJ. Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J Biol Chem 2004; 279:29889-94.
33. Hosokawa N, Hara Y, Mizushima N. Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett 2006; 580:2623-9.
34. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2001; 2:330-5.
35. Furuya N, Yu J, Byfield M, Pattingre S, Levine B. The evolutionary conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function. Autophagy 2005; 1:46-52.
36. Zeng X, Overmeyer JH, Maltese WA. Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 2006; 119:259-70.
37. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672-6.
38. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, Cattoretti G, Levine B. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003; 112:1809-20.
39. Matsuura A, Tsukada M, Wada Y, Ohsumi Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 1997; 192:245-50.
40. Straub M, Bredschneider M, Thumm M. AUT3, a serine/threonine kinase gene, is essential for autophagocytosis in Saccharomyces cerevisiae. J Bacteriol 1997; 179:3875-83.
41. Tekinay T, Wu MY, Otto GP, Anderson OR, Kessin RH. Function of the Dictyostelium discoideum Atg1 kinase during autophagy and development. Eukaryot Cell 2006; 5:1797-806.
42. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 2003; 301:1387-91.
43. Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 2004; 7:167-78.
44. Chan EY, Kir S, Tooze SA. siRNA screening of the kinome identifies ULK1 as a multi-domain modulator of autophagy. J Biol Chem 2007; 282:25464-74.
45. Breksa IIIrd AP, Garrow TA. Recombinant human liver betaine-homocysteine S-methyltransferase: Identification of three cysteine residues critical for zinc binding. Biochemistry 1999; 38:13991-8.
46. Hui AS, Bauer AL, Striet JB, Schnell PO, Czyzyk-Krzeska MF. Calcium signaling stimulates translation of HIF-alpha during hypoxia. Faseb J 2006; 20:466-75.
47. Fuertes G, Martin De Llano JJ, Villarroya A, Rivett AJ, Knecht E. Changes in the proteolytic activities of proteasomes and lysosomes in human fibroblasts produced by serum withdrawal, amino-acid deprivation and confluent conditions. Biochem J 2003; 375:75-86.
48. Arico S, Petiot A, Bauvy C, Dubbelhuis PF, Meijer AJ, Codogno P, Ogier-Denis E. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J Biol Chem 2001; 276:35243-6.
49. Elsasser S, Finley D. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat Cell Biol 2005; 7:742-9.
50. Majeski AE, Dice JF. Mechanisms of chaperone-mediated autophagy. Int J Biochem Cell Biol 2004; 36:2435-44.