Divide and multiply: Organelle partitioning in yeast

Current Opinion in Cell Biology

Volumn 12, Issue 4, 2000, Pages 509-516

  Catlett, Natalie L ^a   Weisman, Lois S ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELL VACUOLE; MITOCHONDRION; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; YEAST;

FUNGI;

EID: 0033934232     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(00)00124-1     Document Type: Review

References (73)

1. Lowe M., Nakamura N., Warren G. Golgi division and membrane traffic. Trends Cell Biol. 8:1998;40-44.
2. Roth M.G. Inheriting the Golgi. Cell. 99:1999;559-562.
3. Weisman L.S., Emr S.D., Wickner W.T. Mutants of Saccharomyces cerevisiae that block intervacuole vesicular traffic and vacuole division and segregation. Proc Natl Acad Sci U S A. 87:1990;1076-1080.
4. Gomes de Mesquita D.S., van den Hazel H.B., Bouwman J., Woldringh C.L. Characterization of new vacuolar segregation mutants, isolated by screening for loss of proteinase B self-activation. Eur J Cell Biol. 71:1996;237-247.
5. Wang Y.X., Zhao H., Harding T.M., Gomes de Mesquita D.S., Woldringh C.L., Klionsky D.J., Munn A.L., Weisman L.S. Multiple classes of yeast mutants are defective in vacuole partitioning yet target vacuole proteins correctly. Mol Biol Cell. 7:1996;1375-1389.
6. Hermann G.J., Shaw J.M. Mitochondrial dynamics in yeast. Annu Rev Cell Dev Biol. 14:1998;265-303.
7. Yaffe M.P. The machinery of mitochondrial inheritance and behavior. Science. 283:1999;1493-1497.
8. Hoffmann H.P., Avers C.J. Mitochondrion of yeast: ultrastructural evidence for one giant, branched organelle per cell. Science. 181:1973;749-751.
9. Simon V.R., Karmon S.L., Pon L.A. Mitochondrial inheritance: cell cycle and actin cable dependence of polarized mitochondrial movements in Saccharomyces cerevisiae. Cell Motil Cytoskeleton. 37:1997;199-210.
10. Drubin D.G., Jones H.D., Wertman K.F. Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site. Mol Biol Cell. 4:1993;1277-1294.
11. Lazzarino D.A., Boldogh I., Smith M.G., Rosand J., Pon L.A. Yeast mitochondria contain ATP-sensitive, reversible actin-binding activity. Mol Biol Cell. 5:1994;807-818.
12. Simon V.R., Swayne T.C., Pon L.A. Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: identification of a motor activity on the mitochondrial surface. J Cell Biol. 130:1995;345-354.
13. Boldogh I., Karmon S.L., Nowakowski W.D., Hays L.G., Yates J.R. Jr., Pon L.A. The Arp2/3 complex is required for actin-dependent mitochondrial motility in the budding yeast. Mol Biol Cell. 9:1998;2355.
14. Strauss E. Microbes feature as pathogens and pals at gathering. Science. 284:1999;1916-1917.
15. Boldogh I., Vojtov N., Karmon S., Pon L.A. Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J Cell Biol. 141:1998;1371-1381. The actin monomer-binding drug latrunculin-A is shown to decrease mitochondrial velocity and to disrupt directed mitochondrial movement. Also, through biochemical analysis of isolated mitochondria, the authors identify both peripheral protein(s) with ATP-sensitive actin-binding activity (mABP) and integral membrane protein(s) required for interaction mABP with the mitochondria. Mitochondria isolated from mmm1-1 or mdm10Δ mutants did not bind mABP, suggesting that Mmm1p and Mdm10p either are the mABP-binding component or alternatively, are required for this component's function.
16. Higley S., Way M. Actin and cell pathogenesis. Curr Opin Cell Biol. 9:1997;62-69.
17. Taunton J., Rowning B.A., Coughlin M.L., Wu M., Moon R.T., Mitchison T.J., Larabell C.A. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol. 148:2000;519-530. This paper shows that actin assembly nucleated by Arp2/3 propels endosomes and lysosomes in Xenopus eggs.
18. Hermann G.J., King E.J., Shaw J.M. The yeast gene, MDM20, is necessary for mitochondrial inheritance and organization of the actin cytoskeleton. J Cell Biol. 137:1997;141-153.
19. Yang H.C., Palazzo A., Swayne T.C., Pon L.A. A retention mechanism for distribution of mitochondria during cell division in budding yeast. Curr Biol. 9:1999;1111-1114. This paper suggests that the actin cytoskeleton is part of an active mechanism for retention of mitochondria within the mother cell. Cell-cycle arrest with hydroxyurea did not affect the relative amounts of mitochondria in mother cell versus bud, even when the bud grew to 1.7 times the length of the mother, arguing against passive mechanisms. Moreover, mitochondria accumulated in a 'retention zone' in the mother cell in wild-type but not mmm1-1, mdm10Δ, and act1-159 cells.
20. Nunnari J., Marshall W.F., Straight A., Murray A., Sedat J.W., Walter P. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol Biol Cell. 8:1997;1233-1242.
21. Hales K.G., Fuller M.T. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 90:1997;121-129.
22. Hermann G.J., Thatcher J.W., Mills J.P., Hales K.G., Fuller M.T., Nunnari J., Shaw J.M. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J Cell Biol. 143:1998;359-373.
23. Rapaport D., Brunner M., Neupert W., Westermann B. Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J Biol Chem. 273:1998;20150-20155.
24. Otsuga D., Keegan B.R., Brisch E., Thatcher J.W., Hermann G.J., Bleazard W., Shaw J.M. The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J Cell Biol. 143:1998;333-349.
25. Bleazard W., McCaffery J.M., King E.J., Bale S., Mozdy A., Tieu Q., Nunnari J., Shaw J.M. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol. 1:1999;298-304. The authors show that dnm1Δ mitochondria form 'nets' of interconnected tubules. This morphology is probably a result of mitochondrial fusion in the absence of fission. Loss of Dnm1p rescues fzo1Δ mitochondria morphology defects, but not fusion defects as assayed in mating cells. Immunogold labeling of EM sections reveals predominant Dnm1p localization to mitochondrial constriction sites and tips, including tips in close proximity to the plasma membrane.
26. Sesaki H., Jensen R.E. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol. 147:1999;699-706. The authors isolate both dnm1 and fzo1 mutants in a microscope-based screen for mitochondria morphology mutants. dnm1 mutants have net-like mitochondria. A role for Dnm1p in fission is demonstrated. Expression of Dnm1p-GFP in dnm1, fzo1 mutants causes mitochondrial fragmentation; moreover, GFP-Dnm1p often localizes to ends of mitochondrial tubules.
27. Smirnova E., Shurland D.L., Ryazantsev S.N., van der Bliek A.M. A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol. 143:1998;351-358.
28. Labrousse A.M., Zappaterra M.D., Rube D.A., van der Bliek A.M. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell. 4:1999;815-826. Disruption of the C. elegans Dnm1p homologue DRP-1 by dominant-negative mutants and RNA interference causes abnormal mitochondrial morphology. The authors suggest that this abnormal morphology - blebs of mitochondrial matrix connected by tubules of mitochondrial outer membrane - results from continued scission of the inner membrane in the absence of outer membrane scission.
29. Jones B.A., Fangman W.L. Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev. 6:1992;380-389.
30. Shepard K.A., Yaffe M.P. The yeast dynamin-like protein, Mgm1p, functions on the mitochondrial outer membrane to mediate mitochondrial inheritance. J Cell Biol. 144:1999;711-720. The dynamin-related protein Mgm1p is required for mitochondrial inheritance, mitochondrial morphology, and maintenance of the mitochondrial genome. The authors show that Mgm1p is an integral membrane protein of the outer mitochondrial membrane. Gel filtration experiments suggest that Mgm1p is part of a large, possibly homooligomeric, complex.
31. Pelloquin L., Belenguer P., Menon Y., Ducommun B. Identification of a fission yeast dynamin-related protein involved in mitochondrial DNA maintenance. Biochem Biophys Res Commun. 251:1998;720-726.
32. Beech P.L., Nheu T., Schultz T., Herbert S., Lithgow T., Gilson P.R., McFadden G.I. Mitochondrial FtsZ in a Chromophyte Alga. Science. 287:2000;1276-1279. A homologue of FtsZ, a protein mediating bacterial division, may mediate division or fission of mitochondria in the algae Mallomonas splendens. Interestingly, this paper demonstrates a localization of the algal mitochondrial FtsZ (MsFtsZ-mt) to yeast mitochondria, but does not investigate whether or not this protein could replace the activity of Dnm1p or Mgm1p.
33. Lutkenhaus J. Organelle division: from coli to chloroplasts. Curr Biol. 8:1998;R619-R621.
34. Hill K.L., Catlett N.L., Weisman L.S. Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae. J Cell Biol. 135:1996;1535-1549.
35. Gomes de Mesquita D.S., ten Hoopen R., Woldringh C.L. Vacuolar segregation to the bud of Saccharomyces cerevisiae: an analysis of morphology and timing in the cell cycle. J Gen Microbiol. 137:1991;2447-2454.
36. Raymond C.K., O'Hara P.J., Eichinger G., Rothman J.H., Stevens T.H. Molecular analysis of the yeast VPS3 gene and the role of its product in vacuolar protein sorting and vacuolar segregation during the cell cycle. J Cell Biol. 111:1990;877-892.
37. Weisman L.S., Wickner W. Intervacuole exchange in the yeast zygote: a new pathway in organelle communication. Science. 241:1988;589-591.
38. Gomes De Mesquita D.S., Shaw J., Grimbergen J.A., Buys M.A., Dewi L., Woldringh C.L. Vacuole segregation in the Saccharomyces cerevisiae vac2-1 mutant: structural and biochemical quantification of the segregation defect and formation of new vacuoles. Yeast. 13:1997;999-1008.
39. Catlett N.L., Weisman L.S. The terminal tail region of a yeast myosin-V mediates its attachment to vacuole membranes and sites of polarized growth. Proc Natl Acad Sci U S A. 95:1998;14799-14804.
40. Pruyne D., Bretscher A. Polarization of cell growth in yeast. J Cell Sci. 113:2000;571-585.
41. Reck-Peterson S.L., Provance D.W.J., Mooseker M.S., Mercer J.A. Class V Myosins. Biochemica Biophysica Acta. 1496:2000;36-51.
42. Schott D., Ho J., Pruyne D., Bretscher A. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J Cell Biol. 147:1999;791-808. The authors identify a region of the Myo2p globular tail that is required for polarized secretion by isolation of temperature-sensitive mutants and sequence comparison with other myosinVs. Interestingly, these mutants have little effect on vacuole inheritance, supporting the idea of distinct cargo-binding domains for each cargo of Myo2p.
43. Wang Y.X., Catlett N.L., Weisman L.S. Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole. J Cell Biol. 140:1998;1063-1074. Vac8p is an armadillo repeat-containing vacuole membrane protein required for both vacuole inheritance and cytoplasm to vacuole protein targeting. Both palmitoylation and myristoylation contribute to localization of Vac8p to the vacuole membrane, but only palmitoylation of Vac8p is required for vacuole inheritance. Vac8p cosediments with filamentous actin in vitro suggesting that Vac8p may mediate interactions of actin with the vacuole membrane.
44. Resh M.D. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta. 1451:1999;1-16.
45. Pan X., Goldfarb D.S. YEB3/VAC8 encodes a myristylated armadillo protein of the Saccharomyces cerevisiae vacuolar membrane that functions in vacuole fusion and inheritance. J Cell Sci. 111:1998;2137-2147.
46. Fleckenstein D., Rohde M., Klionsky D.J., Rudiger M. Yel013p (Vac8p), an armadillo repeat protein related to plakoglobin and importin alpha is associated with the yeast vacuole membrane. J Cell Sci. 111:1998;3109-3118.
47. Conibear E., Stevens T.H. Multiple sorting pathways between the late Golgi and the vacuole in yeast. Biochim Biophys Acta. 1404:1998;211-230.
48. Webb G.C., Zhang J., Garlow S.J., Wesp A., Riezman H., Jones E.W. Pep7p provides a novel protein that functions in vesicle-mediated transport between the yeast Golgi and endosome. Mol Biol Cell. 8:1997;871-895.
49. Raymond C.K., Howald-Stevenson I., Vater C.A., Stevens T.H. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell. 3:1992;1389-1402.
50. Nicolson T.A., Weisman L.S., Payne G.S., Wickner W.T. A truncated form of the Pho80 cyclin redirects the Pho85 kinase to disrupt vacuole inheritance in S. cerevisiae. J Cell Biol. 130:1995;835-845.
51. Andrews B., Measday V. The cyclin family of budding yeast: abundant use of a good idea. Trends Genet. 14:1998;66-72.
52. Bonangelino C.J., Catlett N.L., Weisman L.S. Vac7p, a novel vacuolar protein, is required for normal vacuole inheritance and morphology. Mol Cell Biol. 17:1997;6847-6858.
53. Gary J.D., Wurmser A.E., Bonangelino C.J., Weisman L.S., Emr S.D. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol. 143:1998;65-79. This paper demonstrates that Fab1p is the phosphatidylinositol 3-P 5-kinase, and that Vac7p also plays a role in phosphatidylinositol (3,5)P2 synthesis. The authors propose that Fab1p and Vac7p are part of a signal transduction pathway that regulates the turnover of vacuole membranes via regulating the production of phosphatidylinositol (3,5)P2.
54. Bryant N.J., Piper R.C., Weisman L.S., Stevens T.H. Retrograde traffic out of the yeast vacuole to the TGN occurs via the prevacuolar/endosomal compartment. J Cell Biol. 142:1998;651-663. This demonstrates that retrograde traffic out of the vacuole occurs. Interestingly, the vac7D mutant is defective in retrograde traffic from the vacuole, suggesting that phosphatidylinositol (3,5)P2 is required for retrograde traffic. These findings further suggest that vacuole membrane turnover may take place in part via retrograde traffic.
55. Odorizzi G., Babst M., Emr S.D. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell. 95:1998;847-858. The authors show that a lumenal vacuolar protein, carboxypeptidase S, is delivered to the vacuole via formation and internalization of vesicles into an endosomal, multi-vesicular body. The fab1d mutant is defective in this internalization, suggesting that phosphatidylinositol (3,5)P2 is required.
56. Corvera S., D'Arrigo A., Stenmark H. Phosphoinositides in membrane traffic. Curr Opin Cell Biol. 11:1999;460-465.
57. Weisman L.S., Bacallao R., Wickner W. Multiple methods of visualizing the yeast vacuole permit evaluation of its morphology and inheritance during the cell cycle. J Cell Biol. 105:1987;1539-1547.
58. Price A., Wickner W., Ungermann C. Proteins needed for vesicle budding from the golgi complex are also required for the docking step of homotypic vacuole fusion. J Cell Biol. 148:2000;1223-1230.
59. Gotte M., von Mollard G.F. A new beat for the SNARE drum. Trends Cell Biol. 8:1998;215-218.
60. Haas A., Wickner W. Homotypic vacuole fusion requires Sec17p (yeast alpha-SNAP) and Sec18p (yeast NSF). EMBO J. 15:1996;3296-3305.
61. Xu Z., Sato K., Wickner W. LMA1 binds to vacuoles at Sec18p (NSF), transfers upon ATP hydrolysis to a t-SNARE (Vam3p) complex, and is released during fusion. Cell. 93:1998;1125-1134.
62. Ungermann C., Sato K., Wickner W. Defining the functions of trans-SNARE pairs. Nature. 396:1998;543-548.
63. Price A., Seals D., Wickner W., Ungermann C. The docking stage of yeast vacuole fusion requires the transfer of proteins from a cis-SNARE complex to a RAB/Ypt protein. J Cell Biol. 148:2000;1231-1238. This paper shows that the Vam2p and Vam6p are part of a large protein complex that also contains a portion of the t- and v-SNARES required for homotypic vacuole fusion. This complex is released during priming, then associates with Ypt7p and functions in vacuole docking.
64. Nickel W., Weber T., McNew J.A., Parlati F., Sollner T.H., Rothman J.E. Content mixing and membrane integrity during membrane fusion driven by pairing of isolated v-SNAREs and t-SNAREs. Proc Natl Acad Sci U S A. 96:1999;12571-12576.
65. Parlati F., Weber T., McNew J.A., Westermann B., Sollner T.H., Rothman J.E. Rapid and efficient fusion of phospholipid vesicles by the alpha-helical core of a SNARE complex in the absence of an N-terminal regulatory domain. Proc Natl Acad Sci USA. 96:1999;12565-12570. Earlier studies had shown that liposomes reconstituted with v-SNAREs will fuse with liposomes reconstituted with t-SNAREs. In this paper, the authors find that removal of the amino-terminal domain of syntaxin significantly enhances the rate of fusion, suggesting that this domain serves a regulatory role.
66. Peters C., Mayer A. Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature. 396:1998;575-580.
67. Peters C., Andrews P.D., Stark M.J., Cesaro-Tadic S., Glatz A., Podtelejnikov A., Mann M., Mayer A. Control of the terminal step of intracellular membrane fusion by protein phosphatase 1. Science. 285:1999;1084-1087. This paper identifies PP1 (Glc7p) as the phosphatase required for vacuole fusion. Interestingly, PP1 is found in a large complex with calmodulin, which is also required very late in vacuole fusion. Identification of the phosphatase and the calmodulin requirement should aid in determining the late events required for fusion.
68. Suelmann R., Fischer R. Mitochondrial movement and morphology depend on an intact actin cytoskeleton in Aspergillus nidulans. Cell Motil Cytoskeleton. 45:2000;42-50.
69. Yaffe M.P., Harata D., Verde F., Eddison M., Toda T., Nurse P. Microtubules mediate mitochondrial distribution in fission yeast. Proc Natl Acad Sci USA. 93:1996;11664-11668.
70. Hyde G.J., Davies D., Perasso L., Cole L., Ashford A.E. Microtubules, but not actin microfilaments, regulate vacuole motility and morphology in hyphae of Pisolithus tinctorius. Cell Motil Cytoskeleton. 42:1999;114-124.
71. Rogers S.L., Gelfand V.I. Membrane trafficking, organelle transport, and the cytoskeleton. Curr Opin Cell Biol. 12:2000;57-62.
72. Rogers S.L., Karcher R.L., Roland J.T., Minin A.A., Steffen W., Gelfand V.I. Regulation of melanosome movement in the cell cycle by reversible association with myosin V. J Cell Biol. 146:1999;1265-1276. These authors demonstrate the cell-cycle dependence of myosinV attachment to cargo organelles. The actin-based motility of melanosomes treated with mitotic extracts is inhibited as a result of myosinV hyperphosphorylation and dissociation from organelles. This mitotic regulation of motor activity may contribute to organelle segregation.
73. Pereira A.J., Dalby B., Stewart R.J., Doxsey S.J., Goldstein L.S. Mitochondrial association of a plus end-directed microtubule motor expressed during mitosis in Drosophila. J Cell Biol. 136:1997;1081-1090.