Maintaining peroxisome populations: A story of division and inheritance

Annual Review of Cell and Developmental Biology

Volumn 23, Issue , 2007, Pages 321-344

  Fagarasanu, Andrei ^a   Fagarasanu, Monica ^a   Rachubinski, Richard A ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Actin; Cell cycle; Dynamin; Myosin; Organelle; Yeast

Indexed keywords

ACTIN; CELL PROTEIN; DYNAMIN; MOLECULAR MOTOR; PROTEIN INP1P; PROTEIN INP2P; PROTEIN MYO2P; PROTEIN PEX11; UNCLASSIFIED DRUG; MEMBRANE PROTEIN;

CELL DIVISION; CYTOKINESIS; INHERITANCE; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; ANIMAL; EUKARYOTIC CELL; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; ULTRASTRUCTURE;

EUKARYOTA; SACCHAROMYCETALES;

ANIMALS; CELL DIVISION; EUKARYOTIC CELLS; HUMANS; MEMBRANE PROTEINS; PEROXISOMES; SACCHAROMYCES CEREVISIAE;

EID: 36549023194     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.23.090506.123456     Document Type: Review

References (89)

1. Barnett P, Tabak HF, Hettema EH. 2000. Nuclear receptors arose from pre-existing protein modules during evolution. Trends Biochem. Sci. 25:227-28
2. Boldogh IR, Ramcharan SL, Yang HC, Pon LA. 2004. A type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for the retention of newly inherited mitochondria in yeast cells during cell division. Mol. Biol. Cell 15:3994-4002
3. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116:153-66
4. Bretscher A. 2003. Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors. J. Cell Biol. 160:811-16
5. Catlett NL, Duex JE, Tang F, Weisman LS. 2000. Two distinct regions in a yeast myosin-V tail domain are required for the movement of different cargoes. J. Cell Biol. 150:513-26
6. Eitzen GA, Szilard RK, Rachubinski RA. 1997. Enlarged peroxisomes are present in oleic acid-grown Yarrowia lipolytica overexpressing the PEX16 gene encoding an intraperoxisomal peripheral membrane peroxin. J. Cell Biol. 137:1265-78
7. Erdmann R, Blobel G. 1995. Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J. Cell Biol. 128:509-23
8. Estrada P, Kim J, Coleman J, Walker L, Dunn B, et al. 2003. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163:1255-66
9. Faber KN, Heyman JA, Subramani S. 1998. Two AAA family peroxins, PpPex1p and PpPex6p, interact with each other in an ATP-dependent manner and are associated with different subcellular membranous structures distinct from peroxisomes. Mol. Cell. Biol. 18:936-43
10. Fagarasanu A, Fagarasanu M, Eitzen GA, Aitchison JD, Rachubinski RA. 2006. The peroxisomal membrane protein Inp2p is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae. Dev. Cell 10:587-600
11. Fagarasanu M, Fagarasanu A, Rachubinski RA. 2006. Sharing the wealth: peroxisome inheritance in budding yeast. Biochim. Biophys. Acta 1763:1669-77
12. Fagarasanu M, Fagarasanu A, Tam YYC, Aitchison JD, Rachubinski RA. 2005. Inp1p is a peroxisomal membrane protein required for peroxisome inheritance in Saccharomyces cerevisiae. J. Cell Biol. 169:765-75
13. Geuze HJ, Murk JL, Stroobants AK, Griffith JM, Kleijmeer MJ, et al. 2003. Involvement of the endoplasmic reticulum in peroxisome formation. Mol. Biol. Cell 14:2900-7
14. Govindan B, Bowser R, Novick P. 1995. The role of Myo2p, a yeast class V myosin, in vesicular transport. J. Cell Biol. 128:1055-68
15. Guo T, Kit YY, Nicaud JM, Le Dall MT, Sears SK, et al. 2003. Peroxisome division in the yeast Yarrowia lipolytica is regulated by a signal from inside the peroxisome. J. Cell Biol. 162:1255-66
16. Gregg C, Guo T, Boukh-Viner T, Goldberg A, Bourque S, et al. 2006. Mechanism for the coordination of peroxisome growth and division. Presented at Annu. Meet. Am. Soc. Cell Biol., 46th, San Diego
17. Hill KL, Catlett NL, Weisman LS. 1996. Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae. J. Cell Biol. 135:1535-49
18. Hoepfner D, Schildknegt D, Braakman I, Philippsen P, Tabak HF. 2005. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122:85-95
19. Hoepfner D, van den Berg M, Philippsen P, Tabak HF, Hettema EH. 2001. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155:979-90
20. Honsho M, Tamura S, Shimozawa N, Suzuki Y, Kondo N, Fujiki Y. 1998. Mutation in PEX16 is causal in the peroxisome-deficient Zellweger syndrome of complementation group D. Am. J. Hum. Genet. 63:1622-30
21. Huber CM, Saffrich R, Ansorge W, Just WW. 1999. Receptor-mediated regulation of peroxisomal motility in CHO and endothelial cells. EMBO J. 18:5476-85
22. Ishikawa K, Catlett NL, Novak JL, Tang F, Nau JJ, Weisman LS. 2003. Identification of an organelle-specific myosin V receptor. J. Cell Biol. 160:887-97
23. Kiel JA, Veenhuis M, van der Klei IJ. 2006. PEX genes in fungal genomes: common, rare or redundant. Traffic 7:1291-303
24. Kim PK, Mullen RT, Schumann U, Lippincott-Schwartz J. 2006. The origin and maintenance of mammalian peroxisomes involves a de novo PEX16-dependent pathway from the ER. J. Cell Biol. 173:521-32
25. Koch A, Schneider G, Luers GH, Schrader M. 2004. Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J. Cell Sci. 117:3995-4006
26. Koch A, Thiemann M, Grabenbauer M, Yoon Y, McNiven MA, Schrader M. 2003. Dynamin-like protein 1 is involved in peroxisomal fission. J. Biol. Chem. 278:8597-605
27. Koch A, Yoon Y, Bonekamp NA, McNiven MA, Schrader M. 2005. A role for Fis1 in both mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell 16:5077-86
28. Kural C, Kim H, Syed S, Goshima G, Gelfand VI, Selvin PR. 2005. Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308:1469-72
29. Kuravi K, Nagotu S, Krikken AM, Sjollema K, Deckers M, et al. 2006. Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J. Cell Sci. 119:3994-4001
30. Lazarow PB, Fujiki Y. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1:489-530
31. Li X, Gould SJ. 2003. The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J. Biol. Chem. 278:17012-20
32. Liakopoulos D, Kusch J, Grava S, Vogel J, Barral Y. 2003. Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment. Cell 112:561-74
33. Lingard MJ, Trelease RN. 2006. Five Arabidopsis peroxin 11 homologs individually promote peroxisome elongation, duplication or aggregation. J. Cell Sci. 119:1961-72
34. Mano S, Nakamori C, Kondo M, Hayashi M, Nishimura M. 2004. An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J. 38:487-98
35. Marshall PA, Dyer JM, Quick ME, Goodman JM. 1996. Redox-sensitive homodimerization of Pex11p: a proposed mechanism to regulate peroxisomal division. J. Cell Biol. 135:123-37
36. Marshall PA, Krimkevich YI, Lark RH, Dyer JM, Veenhuis M, Goodman JM. 1995. Pmp27 promotes peroxisomal proliferation. J. Cell Biol. 129:345-55
37. Masters CJ. 1996. Cellular signaling: the role of the peroxisome. Cell Signal. 8:197-208
38. McCartney AW, Greenwood JS, Fabian MR, White KA, Mullen RT. 2005. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 17:3513-31
39. McMahon HT, Gallop JL. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590-96
40. Mehta AD, Rock RS, Rief M, Spudich JA, Mooseker MS, Cheney RE. 1999. Myosin-V is a processive actin-based motor. Nature 400:590-93
41. Mullen RT, Flynn CR, Trelease RN. 2001. How are peroxisomes formed? The role of the endoplasmic reticulum and peroxins. Trends Plant Sci. 6:256-61
42. Mullen RT, Lisenbee CS, Miernyk JA, Trelease RN. 1999. Peroxisomal membrane ascorbate peroxidase is sorted to a membranous network that resembles a subdomain of the endoplasmic reticulum. Plant Cell 11:2167-86
43. Mullen RT, Trelease RN. 2006. The ER-peroxisome connection in plants: development of the "ER semiautonomous peroxisome maturation and replication" model for plant peroxisome biogenesis. Biochim. Biophys. Acta 1763:1655-68
44. Osteryoung KW, Nunnari J. 2003. The division of endosymbiotic organelles. Science 302:1698-704
45. Pashkova N, Jin Y, Ramaswamy S, Weisman LS. 2006. Structural basis for myosin V discrimination between distinct cargoes. EMBO J. 25:693-700
46. Praefcke GTK, McMahon HT. 2004. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5:133-47
47. Provance DW, James TL, Mercer JA. 2002. Melanophilin, the product of the leaden locus, is required for targeting of myosin-Va to melanosomes. Traffic 3:124-32
48. Pruyne D, Legesse-Miller A, Gao L, Dong Y, Bretscher A. 2004. Mechanisms of polarized growth and organelle segregation in yeast. Annu. Rev. Cell Dev. Biol. 20:559-91
49. Purdue PE, Lazarow PB. 2001. Peroxisome biogenesis. Annu. Rev. Cell Dev. Biol. 17:701-52
50. Rapp S, Saffrich R, Anton M, Jakle U, Ansorge W, et al. 1996. Microtubule-based peroxisome movement. J. Cell Sci. 109:837-49
51. Rossanese OW, Glick BS. 2001. Deconstructing Golgi inheritance. Traffic 2:589-96
52. Rossanese OW, Reinke CA, Bevis BJ, Hammond AT, Sears IB, et al. 2001. A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae. J. Cell Biol. 153:47-62
53. Rottensteiner H, Stein K, Sonnenhol E, Erdmann R. 2003. Conserved function of Pex11p and the novel Pex25p and Pex27p in peroxisome biogenesis. Mol. Biol. Cell 14:4316-28
54. Schekman R. 2005. Peroxisomes: another branch of the secretory pathway? Cell 122:1-2
55. Schott D, Ho J, Pruyne D, Bretscher A. 1999. The COOH-terminal domain of Myo2, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 147:791-807
56. Schrader M. 2006. Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta 1763:531-41
57. Schrader M, Fahimi HD. 2006. Growth and division of peroxisomes. Int. Rev. Cytol. 255:237-90
58. Schrader M, Reuber BE, Morrell JC, Jimenez-Sanchez G, Obie C, et al. 1998. Expression of Pex11β mediates peroxisome proliferation in the absence of extracellular stimuli. J. Biol. Chem. 273:29607-14
59. Seabra MC, Coudrier E. 2004. Rab GTPases and myosin motors in organelle motility. Traffic 5:393-99
60. Schrader M, Burkhardt JK, Baumgart E, Luers G, Volkl A, Fahimi HD. 1996. The importance of microtubules in determination of shape and intracellular distribution of peroxisomes. Ann. N.Y. Acad. Sci. 804:669-71
61. Schrader M, King SJ, Stroh TA, Schroer TA. 2000. Real time imaging reveals a peroxisomal reticulum in living cells. J. Cell Sci. 113:3663-71
62. Schrader M, Thiemann M, Fahimi HD. 2003. Peroxisomal motility and interaction with microtubules. Microsc. Res. Tech. 61:171-78
63. Sellers JR, Veigel C. 2006. Walking with myosin V. Curr. Opin. Cell Biol. 18:68-73
64. Shepard KA, Gerber AP, Jambhekar A, Takizawa PA, Brown PO, et al. 2003. Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts during DNA microarray analysis. Proc. Natl. Acad. Sci. USA 100:11429-34
65. Smith JJ, Marelli M, Christmas RH, Vizeacoumar FJ, Dilworth DJ, et al. 2002. Transcriptome profiling to identify genes involved in peroxisome assembly. J. Cell Biol. 158:259-71
66. Tam YYC, Fagarasanu A, Fagarasanu M, Rachubinski RA. 2005. Pex3p initiates the formation of a preperoxisomal compartment from a subdomain of the endoplasmic reticulum in Saccharomyces cerevisiae. J. Biol. Chem. 280:34933-39
67. Tam YYC, Torres-Guzman JC, Vizeacoumar FJ, Smith JJ, Marelli M, et al. 2003. Pex11-related proteins in peroxisome dynamics: a role for the novel peroxin Pex27p in controlling peroxisome size and number in Saccharomyces cerevisiae. Mol. Biol. Cell 14:4089-102
68. Tanaka A, Kobayashi S, Fujiki Y. 2006. Peroxisome division is impaired in a CHO cell mutant with an inactivating point-mutation in dynamin-like protein 1 gene. Exp. Cell Res. 312:1671-84
69. Tang F, Kauffman EJ, Novack JL, Nau JJ, Catlett NL, Weisman LS. 2003. Regulated degradation of class V myosin receptor directs movement of the yeast vacuole. Nature 422:87-92
70. Thoms S, Erdmann R. 2005. Dynamin-related proteins and Pex11 proteins in peroxisome division and proliferation. FEBS J. 272:5169-81
71. Titorenko VI, Chan H, Rachubinski RA. 2000. Fusion of small peroxisomal vesicles in vitro reconstructs an early step in the in vivo multistep peroxisome assembly pathway of Yarrowia lipolytica. J. Cell Biol. 148:29-43
72. Titorenko VI, Mullen RT. 2006. Peroxisome biogenesis: the peroxisomal endomembrane system and the role of the ER. J. Cell Biol. 174:11-17
73. Titorenko VI, Ogrydziak DM, Rachubinski RA. 1997. Four distinct secretory pathways serve protein secretion, cell surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 17:5210-26
74. Titorenko VI, Rachubinski RA. 1998a. Mutants of the yeast Yarrowia lipolytica defective in protein exit from the endoplasmic reticulum are also defective in peroxisome biogenesis. Mol. Cell. Biol. 18:2789-803
75. Titorenko VI, Rachubinski RA. 1998b. The endoplasmic reticulum plays an essential role in peroxisome biogenesis. Trends Biochem. Sci. 23:231-33
76. Titorenko VI, Rachubinski RA. 2001. Dynamics of peroxisome assembly and function. Trends Cell Biol. 11:22-29
77. Titorenko VI, Rachubinski RA. 2004. The peroxisome: orchestrating important developmental decisions from inside the cell. J. Cell Biol. 164:641-45
78. van der Zand A, Braakman I, Geuze HJ, Tabak HF. 2006. The return of the peroxisome. J. Cell Sci. 119:989-94
79. van Roermund CW, Tabak HF, van den Berg M, Wanders RJ, Hettema EH. 2000. Pex11p plays a primary role in medium-chain fatty acid oxidation, a process that affects peroxisome number and size in Saccharomyces cerevisiae. J. Cell Biol. 150:489-98
80. Vizeacoumar FJ, Torres-Guzman JC, Bouard D, Aitchison JD, Rachubinski RA. 2004. Pex30p, Pex31p, and Pex32p form a family of peroxisomal integral membrane proteins regulating peroxisome size and number in Saccharomyces cerevisiae. Mol. Biol. Cell 15:665-77
81. Vizeacoumar FJ, Torres-Guzman JC, Tam YYC, Aitchison JD, Rachubinski RA. 2003. YHR150w and YDR479c encode peroxisomal integral membrane proteins involved in the regulation of peroxisome number, size and distribution in Saccharomyces cerevisiae. J. Cell Biol. 161:321-32
82. Warren G, Wickner W. 1996. Organelle inheritance. Cell 84:395-400
83. Weisman LS. 2006. Organelles on the move: insights from yeast vacuole inheritance. Nat. Rev. Mol. Cell Biol. 7:243-52
84. Wiemer EA, Wenzel T, Deerinck TJ, Ellisman MH, Subramani S. 1997. Visualization of the peroxisomal compartment in living mammalian cells: dynamic behavior and association with microtubules. J. Cell Biol. 136:71-80
85. Wu XS, Rao K, Zhang H, Wang F, Sellers JR, et al. 2002. Identification of an organelle receptor for myosin-Va. Nat. Cell Biol. 4:271-78
86. Yan M, Rayapuram N, Subramani S. 2005. The control of peroxisome number and size during division and proliferation. Curr. Opin. Cell Biol. 17:376-83
87. Yang HC, Palazzo A, Swayne TC, Pon LA. 1999. A retention mechanism for distribution of mitochondria during cell division in budding yeast. Curr. Biol. 9:1111-14
88. Yildiz A, Forkey JN, McKinney SA, Ha T, Goldman YE, Selvin PR. 2003. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 300:2061-65
89. Yin H, Pruyne D, Huffaker TC, Bretscher A. 2000. Myosin V orientates the mitotic spindle in yeast. Nature 406:1013-15