1932
0

Annual Review of Cell and Developmental Biology

Volume 31, 2015

Motors, Anchors, and Connectors: Orchestrators of Organelle Inheritance

Abstract

Organelle inheritance is a process whereby organelles are actively distributed between dividing cells at cytokinesis. Much valuable insight into the molecular mechanisms of organelle inheritance has come from the analysis of asymmetrically dividing cells, which transport a portion of their organelles to the bud while retaining another portion in the mother cell. Common principles apply to the inheritance of all organelles, although individual organelles use specific factors for their partitioning. Inheritance factors can be classified as motors, which are required for organelle transport; anchors, which immobilize organelles at distinct cell structures; or connectors, which mediate the attachment of organelles to motors and anchors. Here, we provide an overview of recent advances in the field of organelle inheritance and highlight how motor, anchor, and connector molecules choreograph the segregation of a multicopy organelle, the peroxisome. We also discuss the role of organelle population control in the generation of cellular diversity.

Keyword(s): organelle division, organelle population control, organelle retention, organelle transport, peroxisomes, Saccharomyces cerevisiae

Associated Article

There are media items related to this article:
Motors, Anchors, and Connectors: Orchestrators of Organelle Inheritance: Supplemental Video 1
Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100814-125553
2015-11-13
2025-06-22
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/31/1/annurev-cellbio-100814-125553.html?itemId=/content/journals/10.1146/annurev-cellbio-100814-125553&mimeType=html&fmt=ahah

Literature Cited

  1. Achanzar WE, Ward S. 1997. A nematode gene required for sperm vesicle fusion. J. Cell Sci. 110:1073–81 [Google Scholar]
  2. Adeyo O, Horn PJ, Lee S, Binns DD, Chandrahas A. et al. 2011. The yeast lipin orthologue Pah1p is important for biogenesis of lipid droplets. J. Cell Biol. 192:1043–55 [Google Scholar]
  3. Agrawal G, Joshi S, Subramani S. 2011. Cell-free sorting of peroxisomal membrane proteins from the endoplasmic reticulum. PNAS 108:9113–18 [Google Scholar]
  4. Agrawal G, Subramani S. 2013. Emerging role of the endoplasmic reticulum in peroxisome biogenesis. Front. Physiol. 4:286 [Google Scholar]
  5. Altmann K, Frank M, Neumann D, Jakobs S, Westermann B. 2008. The class V myosin motor protein, Myo2, plays a major role in mitochondrial motility in Saccharomyces cerevisiae. J. Cell Biol. 181:119–30 [Google Scholar]
  6. Arai S, Noda Y, Kainuma S, Wada I, Yoda K. 2008. Ypt11 functions in bud-directed transport of the Golgi by linking Myo2 to the coatomer subunit Ret2. Curr. Biol. 18:987–91 [Google Scholar]
  7. Aranovich A, Hua R, Rutenberg AD, Kim PK. 2014. PEX16 contributes to peroxisome maintenance by constantly trafficking PEX3 via the ER. J. Cell Sci. 127:3675–86 [Google Scholar]
  8. Aubourg P, Wanders R. 2013. Peroxisomal disorders. Handb. Clin. Neurol. 113:1593–609 [Google Scholar]
  9. Bashir R, Britton S, Strachan T, Keers S, Vafiadaki E. et al. 1998. A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat. Genet. 20:37–42 [Google Scholar]
  10. Beach DL, Thibodeaux J, Maddox P, Yeh E, Bloom K. 2000. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast. Curr. Biol. 10:1497–506 [Google Scholar]
  11. Beck R, Rawet M, Wieland FT, Cassel D. 2009. The COPI system: molecular mechanisms and function. FEBS Lett. 583:2701–9 [Google Scholar]
  12. Bi E, Park HO. 2012. Cell polarization and cytokinesis in budding yeast. Genetics 191:347–87 [Google Scholar]
  13. Bockler S, Westermann B. 2014. Mitochondrial ER contacts are crucial for mitophagy in yeast. Dev. Cell 28:450–58 [Google Scholar]
  14. Boldogh IR, Ramcharan SL, Yang HC, Pon LA. 2004. A type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for retention of newly inherited mitochondria in yeast cells during cell division. Mol. Biol. Cell 15:3994–4002 [Google Scholar]
  15. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116:153–66 [Google Scholar]
  16. Brocard C. 2014. Peroxisome proliferation: vesicles, reticulons and ER-to-peroxisome contact sites. Molecular Machines Involved in Peroxisome Biogenesis and Maintenance C Brocard, A Hartig 403–23 Vienna: Springer-Verlag [Google Scholar]
  17. Brown JL, Jaquenoud M, Gulli MP, Chant J, Peter M. 1997. Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast. Genes Dev. 11:2972–82 [Google Scholar]
  18. Brown TW, Titorenko VI, Rachubinski RA. 2000. Mutants of the Yarrowia lipolytica PEX23 gene encoding an integral peroxisomal membrane peroxin mislocalize matrix proteins and accumulate vesicles containing peroxisomal matrix and membrane proteins. Mol. Biol. Cell 11:141–52 [Google Scholar]
  19. Buvelot FS, Rahl PB, Nussbaum M, Briggs BJ, Calero M. et al. 2006. Bioinformatic and comparative localization of Rab proteins reveals functional insights into the uncharacterized GTPases Ypt10p and Ypt11p. Mol. Cell. Biol. 26:7299–317 [Google Scholar]
  20. Casamayor A, Snyder M. 2002. Bud-site selection and cell polarity in budding yeast. Curr. Opin. Microbiol. 5:179–86 [Google Scholar]
  21. Casamayor A, Snyder M. 2003. Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol. Cell. Biol. 23:2762–77 [Google Scholar]
  22. 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 [Google Scholar]
  23. Catlett NL, Weisman LS. 1998. The terminal tail region of a yeast myosin-V mediates its attachment to vacuole membranes and sites of polarized growth. PNAS 95:14799–804 [Google Scholar]
  24. Caviston JP, Longtine M, Pringle JR, Bi E. 2003. The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol. Biol. Cell 14:4051–66 [Google Scholar]
  25. Cerveny KL, Studer SL, Jensen RE, Sesaki H. 2007. Yeast mitochondrial division and distribution require the cortical Num1 protein. Dev. Cell 12:363–75 [Google Scholar]
  26. Chang J, Mast FD, Fagarasanu A, Rachubinski DA, Eitzen GA. et al. 2009. Pex3 peroxisome biogenesis proteins function in peroxisome inheritance as class V myosin receptors. J. Cell Biol. 187:233–46 [Google Scholar]
  27. Chen GC, Kim YJ, Chan CS. 1997. The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae. Genes Dev. 11:2958–71 [Google Scholar]
  28. Cheney RE, O'Shea MK, Heuser JE, Coelho MV, Wolenski JS. et al. 1993. Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell 75:13–23 [Google Scholar]
  29. Chernyakov I, Santiago-Tirado F, Bretscher A. 2013. Active segregation of yeast mitochondria by Myo2 is essential and mediated by Mmr1 and Ypt11. Curr. Biol. 23:1818–24 [Google Scholar]
  30. Chung S, Takizawa PA. 2010. Multiple Myo4 motors enhance ASH1 mRNA transport in Saccharomyces cerevisiae. J. Cell Biol. 189:755–67 [Google Scholar]
  31. David C, Koch J, Oeljeklaus S, Laernsack A, Melchior S. et al. 2013. A combined approach of quantitative interaction proteomics and live-cell imaging reveals a regulatory role for endoplasmic reticulum (ER) reticulon homology proteins in peroxisome biogenesis. Mol. Cell Proteomics 12:2408–25 [Google Scholar]
  32. Du Y, Ferro-Novick S, Novick P. 2004. Dynamics and inheritance of the endoplasmic reticulum. J. Cell Sci. 117:2871–78 [Google Scholar]
  33. Erdmann R, Blobel G. 1995. Giant peroxisomes in oleic acid–induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27. J. Cell Biol. 128:509–23 [Google Scholar]
  34. 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. 163:1255–66Cortical endoplasmic reticulum elements are carried to the bud by Myo4p using the adaptor protein She3p. [Google Scholar]
  35. Evangelista M, Pruyne D, Amberg DC, Boone C, Bretscher A. 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4:32–41 [Google Scholar]
  36. Eves PT, Jin Y, Brunner M, Weisman LS. 2012. Overlap of cargo binding sites on myosin V coordinates the inheritance of diverse cargoes. J. Cell Biol. 198:69–85Myo2p adaptors compete for access to two cargo-binding sites on the Myo2p tail. [Google Scholar]
  37. 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 10:587–600Shows that Inp2p is the peroxisome-specific adaptor for Myo2p. [Google Scholar]
  38. Fagarasanu A, Fagarasanu M, Rachubinski RA. 2007. Maintaining peroxisome populations: a story of division and inheritance. Annu. Rev. Cell Dev. Biol. 23:321–44 [Google Scholar]
  39. 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 169:765–75First report showing that Inp1p is required for peroxisome immobilization at the cell cortex. [Google Scholar]
  40. Fagarasanu A, Mast FD, Knoblach B, Jin Y, Brunner MJ. et al. 2009. Myosin-driven peroxisome partitioning in S. cerevisiae. J. Cell Biol. 186:541–54 [Google Scholar]
  41. Fagarasanu A, Mast FD, Knoblach B, Rachubinski RA. 2010. Molecular mechanisms of organelle inheritance: lessons from peroxisomes in yeast. Nat. Rev. Mol. Cell Biol. 11:644–54 [Google Scholar]
  42. Fang Y, Morrell JC, Jones JM, Gould SJ. 2004. PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins. J. Cell Biol. 164:863–75 [Google Scholar]
  43. Farkasovsky M, Kuntzel H. 1995. Yeast Num1p associates with the mother cell cortex during S/G2 phase and affects microtubular functions. J. Cell Biol. 131:1003–14 [Google Scholar]
  44. Farkasovsky M, Kuntzel H. 2001. Cortical Num1p interacts with the dynein intermediate chain Pac11p and cytoplasmic microtubules in budding yeast. J. Cell Biol. 152:251–62 [Google Scholar]
  45. Fehrenbacher KL, Yang HC, Gay AC, Huckaba TM, Pon LA. 2004. Live cell imaging of mitochondrial movement along actin cables in budding yeast. Curr. Biol. 14:1996–2004 [Google Scholar]
  46. Fortsch J, Hummel E, Krist M, Westermann B. 2011. The myosin-related motor protein Myo2 is an essential mediator of bud-directed mitochondrial movement in yeast. J. Cell Biol. 194:473–88 [Google Scholar]
  47. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. 2011. ER tubules mark sites of mitochondrial division. Science 334:358–62Endoplasmic reticulum tubules promote mitochondrial constriction and define sites of future division prior to Dnm1p recruitment. [Google Scholar]
  48. Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A. et al. 2003. Global analysis of protein expression in yeast. Nature 425:737–41 [Google Scholar]
  49. Govindan B, Bowser R, Novick P. 1995. The role of Myo2, a yeast class V myosin, in vesicular transport. J. Cell Biol. 128:1055–68 [Google Scholar]
  50. Guo Y, Cordes KR, Farese RV Jr, Walther TC. 2009. Lipid droplets at a glance. J. Cell Sci. 122:749–52 [Google Scholar]
  51. Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A. et al. 2013. Autophagosomes form at ER-mitochondria contact sites. Nature 495:389–93 [Google Scholar]
  52. Hammer JA III, Sellers JR. 2012. Walking to work: roles for class V myosins as cargo transporters. Nat. Rev. Mol. Cell Biol. 13:13–26 [Google Scholar]
  53. Hettema EH, Erdmann R, van der Klei IJ, Veenhuis M. 2014. Evolving models for peroxisome biogenesis. Curr. Opin. Cell Biol. 29:25–30 [Google Scholar]
  54. Hettema EH, Girzalsky W, van den Berg M, Erdmann R, Distel B. 2000. Saccharomyces cerevisiae Pex3p and Pex19p are required for proper localization and stability of peroxisomal membrane proteins. EMBO J. 19:223–33 [Google Scholar]
  55. Heymann JA, Hinshaw JE. 2009. Dynamins at a glance. J. Cell Sci. 122:3427–31 [Google Scholar]
  56. Higuchi R, Vevea JD, Swayne TC, Chojnowski R, Hill V. et al. 2013. Actin dynamics affect mitochondrial quality control and aging in budding yeast. Curr. Biol. 23:2417–22 [Google Scholar]
  57. Higuchi-Sanabria R, Pernice WM, Vevea JD, Alessi Wolken DM, Boldogh IR, Pon LA. 2014. Role of asymmetric cell division in lifespan control in Saccharomyces cerevisiae. FEMS Yeast Res. 14:1133–46 [Google Scholar]
  58. 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 [Google Scholar]
  59. Hodges AR, Bookwalter CS, Krementsova EB, Trybus KM. 2009. A nonprocessive class V myosin drives cargo processively when a kinesin-related protein is a passenger. Curr. Biol. 19:2121–25 [Google Scholar]
  60. Hodges AR, Krementsova EB, Trybus KM. 2008. She3p binds to the rod of yeast myosin V and prevents it from dimerizing, forming a single-headed motor complex. J. Biol. Chem. 283:6906–14 [Google Scholar]
  61. Hoepfner D, Schildknegt D, Braakman I, Philippsen P, Tabak HF. 2005. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122:85–95 [Google Scholar]
  62. Hoepfner D, van den Berg M, Phillipsen 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. 155:979–90First report showing that peroxisomes segregate between mother cell and bud in an actomyosin-dependent manner. [Google Scholar]
  63. Höhfeld J, Veenhuis M, Kunau W-H. 1991. PAS3, a Saccharomyces cerevisiae gene encoding a peroxisomal integral membrane protein essential for peroxisome biogenesis. J. Cell Biol. 114:1167–78 [Google Scholar]
  64. Huckaba TM, Lipkin T, Pon LA. 2006. Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J. Cell Biol. 175:957–69 [Google Scholar]
  65. Huffaker TC, Thomas JH, Botstein D. 1988. Diverse effects of β-tubulin mutations on microtubule formation and function. J. Cell Biol. 106:1997–2010 [Google Scholar]
  66. Hughes AL, Gottschling DE. 2012. An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492:261–65 [Google Scholar]
  67. 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 [Google Scholar]
  68. Itoh T, Toh E, Matsui Y. 2004. Mmr1p is a mitochondrial factor for Myo2p-dependent inheritance of mitochondria in the budding yeast. EMBO J. 23:2520–30 [Google Scholar]
  69. Itoh T, Watabe A, Toh E, Matsui Y. 2002. Complex formation with Ypt11p, a Rab-type small GTPase, is essential to facilitate the function of Myo2p, a class V myosin, in mitochondrial distribution in Saccharomyces cerevisiae. Mol. Cell. Biol. 22:7744–57 [Google Scholar]
  70. Jacobs CW, Adams AE, Szaniszlo PJ, Pringle JR. 1988. Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 107:1409–26 [Google Scholar]
  71. Jacquier N, Choudhary V, Mari M, Toulmay A, Reggiori F, Schneiter R. 2011. Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Sci. 124:2424–37 [Google Scholar]
  72. Jan CH, Williams CC, Weissman JS. 2014. Principles of ER cotranslational translocation revealed by proximity-specific ribosome profiling. Science 346:1257521 [Google Scholar]
  73. Jin Y, Sultana A, Gandhi P, Franklin E, Hamamoto S. et al. 2011. Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev. Cell 21:1156–70 [Google Scholar]
  74. Johnson DI, Pringle JR. 1990. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 111:143–52 [Google Scholar]
  75. Johnston GC, Prendergast JA, Singer RA. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113:539–51 [Google Scholar]
  76. Jones JM, Morrell JC, Gould SJ. 2004. PEX19 is a predominantly cytosolic chaperone and import receptor for class 1 peroxisomal membrane proteins. J. Cell Biol. 164:57–67 [Google Scholar]
  77. Jongsma MLM, Berlin I, Neefjes J. 2015. On the move: organelle dynamics during mitosis. Trends Cell Biol. 25:112–24 [Google Scholar]
  78. Joshi S, Agrawal G, Subramani S. 2012. Phosphorylation-dependent Pex11p and Fis1p interaction regulates peroxisome division. Mol. Biol. Cell 23:1307–15 [Google Scholar]
  79. 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 [Google Scholar]
  80. Klecker T, Böckler S, Westermann B. 2014. Making connections: interorganelle contacts orchestrate mitochondrial behavior. Trends Cell Biol. 24:537–45 [Google Scholar]
  81. Klecker T, Scholz D, Fortsch J, Westermann B. 2013. The yeast cell cortical protein Num1 integrates mitochondrial dynamics into cellular architecture. J. Cell Sci. 126:2924–30 [Google Scholar]
  82. Knoblach B, Rachubinski RA. 2010. Phosphorylation-dependent activation of peroxisome proliferator protein PEX11 controls peroxisome abundance. J. Biol. Chem. 285:6670–80 [Google Scholar]
  83. Knoblach B, Rachubinski RA. 2013. Doing the math: how yeast cells maintain their peroxisome populations. Commun. Integr. Biol. 6:e26901 [Google Scholar]
  84. Knoblach B, Rachubinski RA. 2015a. Sharing the cell's bounty—organelle inheritance in yeast. J. Cell Sci. 128:621–30 [Google Scholar]
  85. Knoblach B, Rachubinski RA. 2015b. Transport and retention mechanisms govern lipid droplet inheritance in Saccharomyces cerevisiae. Traffic 16:298–309 [Google Scholar]
  86. Knoblach B, Sun X, Coquelle N, Fagarasanu A, Poirier RL, Rachubinski RA. 2013. An ER-peroxisome tether exerts peroxisome population control in yeast. EMBO J. 32:2439–53Pex3p and Inp1p form an ER-peroxisome tethering complex that controls cellular peroxisome abundance. [Google Scholar]
  87. Koch J, Brocard C. 2011. Membrane elongation factors in organelle maintenance: the case of peroxisome proliferation. Biomol. Concepts 2:353–64 [Google Scholar]
  88. Koch J, Pranjic K, Huber A, Ellinger A, Hartig A. et al. 2010. PEX11 family members are membrane elongation factors that coordinate peroxisome proliferation and maintenance. J. Cell Sci. 123:3389–400 [Google Scholar]
  89. Kormanec J, Schaaff-Gerstenschlager I, Zimmermann FK, Perecko D, Kuntzel H. 1991. Nuclear migration in Saccharomyces cerevisiae is controlled by the highly repetitive 313 kDa NUM1 protein. Mol. Gen. Genet. 230:277–87 [Google Scholar]
  90. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J. et al. 2009. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325:477–81Mitochondrion–endoplasmic reticulum junctions are formed by the endoplasmic reticulum–mitochondrion encounter structure, a complex of proteins resident in both compartments. [Google Scholar]
  91. Kragt A, Voorn-Brouwer T, van den Berg M, Distel B. 2005. Endoplasmic reticulum–directed Pex3p routes to peroxisomes and restores peroxisome formation in a Saccharomyces cerevisiae pex3Δ strain. J. Biol. Chem. 280:34350–57 [Google Scholar]
  92. 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 [Google Scholar]
  93. Lackner LL, Ping H, Graef M, Murley A, Nunnari J. 2013. Endoplasmic reticulum–associated mitochondria-cortex tether functions in the distribution and inheritance of mitochondria. PNAS 110:E458–67 [Google Scholar]
  94. Lahiri S, Chao JT, Tavassoli S, Wong AK, Choudhary V. et al. 2014. A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipid transfer from the ER to mitochondria. PLOS Biol. 12:e1001969 [Google Scholar]
  95. Lahiri S, Toulmay A, Prinz WA. 2015. Membrane contact sites, gateways for lipid homeostasis. Curr. Opin. Cell Biol. 33:82–87 [Google Scholar]
  96. Lam SK, Yoda N, Schekman R. 2011. A vesicle carrier that mediates peroxisome protein traffic from the endoplasmic reticulum. PNAS 108:E51–52 [Google Scholar]
  97. Lazarow PB, Fujiki Y. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 9:489–530 [Google Scholar]
  98. Lipatova Z, Tokarev AA, Jin Y, Mulholland J, Weisman LS, Segev N. 2008. Direct interaction between a myosin V motor and the Rab GTPases Ypt31/32 is required for polarized secretion. Mol. Biol. Cell 19:4177–87 [Google Scholar]
  99. Lippincott J, Shannon KB, Shou W, Deshaies RJ, Li R. 2001. The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis. J. Cell Sci. 114:1379–86 [Google Scholar]
  100. Liu J, Aoki M, Illa I, Wu C, Fardeau M. et al. 1998. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat. Genet. 20:31–36 [Google Scholar]
  101. Liu J, Taylor DW, Krementsova EB, Trybus KM, Taylor KA. 2006. Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography. Nature 442:208–11 [Google Scholar]
  102. Lu H, Krementsova EB, Trybus KM. 2006. Regulation of myosin V processivity by calcium at the single molecule level. J. Biol. Chem. 281:31987–94 [Google Scholar]
  103. Luedeke C, Frei SB, Sbalzarini I, Schwarz H, Spang A, Barral Y. 2005. Septin-dependent compartmentalization of the endoplasmic reticulum during yeast polarized growth. J. Cell Biol. 169:897–908 [Google Scholar]
  104. Manford AG, Stefan CJ, Yuan HL, Macgurn JA, Emr SD. 2012. ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 23:1129–40Endoplasmic reticulum–plasma membrane tethering is mediated by three families of endoplasmic reticulum proteins containing lipid-binding domains. [Google Scholar]
  105. Manjithaya R, Nazarko TY, Farré JC, Subramani S. 2010. Molecular mechanism and physiological role of pexophagy. FEBS Lett. 584:1367–73 [Google Scholar]
  106. Marshall PA, Krimkevich YI, Lark RH, Dyer JM, Veenhuis M, Goodman JM. 1995. Pmp27 promotes peroxisomal proliferation. J. Cell Biol. 129:345–55 [Google Scholar]
  107. Matsuzaki T, Fujiki Y. 2008. The peroxisomal membrane protein import receptor Pex3p is directly transported to peroxisomes by a novel Pex19p- and Pex16p-dependent pathway. J. Cell Biol. 183:1275–86 [Google Scholar]
  108. McFaline-Figueroa JR, Vevea J, Swayne TC, Zhou C, Liu C. et al. 2011. Mitochondrial quality control during inheritance is associated with lifespan and mother-daughter age asymmetry in budding yeast. Aging Cell 10:885–95 [Google Scholar]
  109. 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 [Google Scholar]
  110. Mendenhall MD, Hodge AE. 1998. Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1191–243 [Google Scholar]
  111. Menendez-Benito V, van Deventer SJ, Jimenez-Garcia V, Roy-Luzarraga M, van Leeuwen F, Neefjes J. 2013. Spatiotemporal analysis of organelle and macromolecular complex inheritance. PNAS 110:175–80 [Google Scholar]
  112. Moseley JB, Goode BL. 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70:605–45 [Google Scholar]
  113. Motley AM, Hettema EH. 2007. Yeast peroxisomes multiply by growth and division. J. Cell Biol. 178:399–410 [Google Scholar]
  114. Motley AM, Nuttall JM, Hettema EH. 2012a. Atg36: the Saccharomyces cerevisiae receptor for pexophagy. Autophagy 8:1680–81 [Google Scholar]
  115. Motley AM, Nuttall JM, Hettema EH. 2012b. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 31:2852–68 [Google Scholar]
  116. Munck JM, Motley AM, Nuttall JM, Hettema EH. 2009. A dual function for Pex3p in peroxisome formation and inheritance. J. Cell Biol. 187:463–71 [Google Scholar]
  117. Nagotu S, Veenhuis M, van der Klei IJ. 2010. Divide et impera: the dictum of peroxisomes. Traffic 11:175–84 [Google Scholar]
  118. Opaliński L, Kiel JA, Williams C, Veenhuis M, van der Klei IJ. 2011. Membrane curvature during peroxisome fission requires Pex11. EMBO J. 30:5–16 [Google Scholar]
  119. Ouellet J, Barral Y. 2012. Organelle segregation during mitosis: lessons from asymmetrically dividing cells. J. Cell Biol. 196:305–13 [Google Scholar]
  120. Park HO, Bi E. 2007. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71:48–96 [Google Scholar]
  121. Pashkova N, Jin Y, Ramaswamy S, Weisman LS. 2006. Structural basis for myosin V discrimination between distinct cargoes. EMBO J. 25:693–700 [Google Scholar]
  122. Peng Y, Weisman LS. 2008. The cyclin-dependent kinase Cdk1 directly regulates vacuole inheritance. Dev. Cell 15:478–85 [Google Scholar]
  123. Platta HW, Erdmann R. 2007. Peroxisomal dynamics. Trends Cell Biol. 17:474–84 [Google Scholar]
  124. Praefcke GJ, McMahon HT. 2004. The dynamin superfamily: universal membrane tubulation and fission molecules?. Nat. Rev. Mol. Cell Biol. 5:133–47 [Google Scholar]
  125. Prinz WA. 2014. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 205:759–69 [Google Scholar]
  126. Pruyne D, Evangelista M, Yang C, Bi E, Zigmond S. et al. 2002. Role of formins in actin assembly: nucleation and barbed-end association. Science 297:612–15 [Google Scholar]
  127. Pruyne D, Gao L, Bi E, Bretscher A. 2004. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell 15:4971–89 [Google Scholar]
  128. Purdue PE, Lazarow PB. 2001. Peroxisome biogenesis. Annu. Rev. Cell Dev. Biol. 17:701–52 [Google Scholar]
  129. 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 [Google Scholar]
  130. Rottensteiner H, Kramer A, Lorenzen S, Stein K, Landgraf C. et al. 2004. Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals. Mol. Biol. Cell 15:3406–17 [Google Scholar]
  131. Rowland AA, Voeltz GK. 2012. Endoplasmic reticulum–mitochondria contacts: function of the junction. Nat. Rev. Mol. Cell Biol. 13:607–25 [Google Scholar]
  132. Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D. 2002. An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4:626–31 [Google Scholar]
  133. Sato Y, Shibata H, Nakano H, Matsuzono Y, Kashiwayama Y. et al. 2008. Characterization of the interaction between recombinant human peroxin Pex3p and Pex19p. Identification of Trp-104 in Pex3p as a critical residue for the interaction. J. Biol. Chem. 283:6136–44 [Google Scholar]
  134. Sato Y, Shibata H, Nakatsu T, Nakano H, Kashiwayama Y. et al. 2010. Structural basis for docking of peroxisomal membrane protein carrier Pex19p onto its receptor Pex3p. EMBO J. 29:4083–93Reports the crystal structure of human Pex3p in association with a Pex19 peptide. [Google Scholar]
  135. Schekman R. 2005. Peroxisomes: another branch of the secretory pathway?. Cell 122:1–2 [Google Scholar]
  136. Schmidt F, Dietrich D, Eylenstein R, Groemping Y, Stehle T, Dodt G. 2012. The role of conserved PEX3 regions in PEX19-binding and peroxisome biogenesis. Traffic 13:1244–60 [Google Scholar]
  137. Schmidt F, Treiber N, Zocher G, Bjelic S, Steinmetz MO. et al. 2010. Insights into peroxisome function from the structure of PEX3 in complex with a soluble fragment of PEX19. J. Biol. Chem. 285:25410–17 [Google Scholar]
  138. Schott D, Ho J, Pruyne D, Bretscher A. 1999. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 147:791–808 [Google Scholar]
  139. Schott DH, Collins RN, Bretscher A. 2002. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J. Cell Biol. 156:35–39 [Google Scholar]
  140. Schrader M, Bonekamp NA, Islinger M. 2012. Fission and proliferation of peroxisomes. Biochim. Biophys. Acta 1822:1343–57 [Google Scholar]
  141. Schrader M, Fahimi HD. 2006. Growth and division of peroxisomes. Int. Rev. Cytol. 255:237–89 [Google Scholar]
  142. Schueller N, Holton SJ, Fodor K, Milewski M, Konarev P. et al. 2010. The peroxisomal receptor Pex19p forms a helical mPTS recognition domain. EMBO J. 29:2491–500 [Google Scholar]
  143. 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 using DNA microarray analysis. PNAS 100:11429–34 [Google Scholar]
  144. Shimozawa N, Suzuki Y, Zhang Z, Imamura A, Ghaedi K. et al. 2000. Identification of PEX3 as the gene mutated in a Zellweger syndrome patient lacking peroxisomal remnant structures. Hum. Mol. Genet. 9:1995–99 [Google Scholar]
  145. Sinclair DA, Guarente L. 1997. Extrachromosomal rDNA circles—a cause of aging in yeast. Cell 91:1033–42 [Google Scholar]
  146. Stefan CJ, Manford AG, Emr SD. 2013. ER-PM connections: sites of information transfer and inter-organelle communication. Curr. Opin. Cell Biol. 25:434–42 [Google Scholar]
  147. Swayne TC, Zhou C, Boldogh IR, Charalel JK, McFaline-Figueroa JR. et al. 2011. Role for cER and Mmr1p in anchorage of mitochondria at sites of polarized surface growth in budding yeast. Curr. Biol. 21:1994–99 [Google Scholar]
  148. 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 [Google Scholar]
  149. Tang F, Kauffman EJ, Novak JL, Nau JJ, Catlett NL, Weisman LS. 2003. Regulated degradation of a class V myosin receptor directs movement of the yeast vacuole. Nature 422:87–92 [Google Scholar]
  150. Thirumurugan K, Sakamoto T, Hammer JA III, Sellers JR, Knight PJ. 2006. The cargo-binding domain regulates structure and activity of myosin 5. Nature 442:212–15 [Google Scholar]
  151. Thoms S, Harms I, Kalies KU, Gärtner J. 2012. Peroxisome formation requires the endoplasmic reticulum channel protein Sec61. Traffic 13:599–609 [Google Scholar]
  152. 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. 148:29–44 [Google Scholar]
  153. 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 [Google Scholar]
  154. Titorenko VI, Rachubinski RA. 1998b. The endoplasmic reticulum plays an essential role in peroxisome biogenesis. Trends Biochem. Sci. 23:231–33 [Google Scholar]
  155. Toro AA, Araya CA, Cordova GJ, Arredondo CA, Cardenas HG. et al. 2009. Pex3p-dependent peroxisomal biogenesis initiates in the endoplasmic reticulum of human fibroblasts. J. Cell Biochem. 107:1083–96 [Google Scholar]
  156. Toulmay A, Prinz WA. 2012. A conserved membrane-binding domain targets proteins to organelle contact sites. J. Cell Sci. 125:49–58 [Google Scholar]
  157. van der Zand A, Braakman I, Tabak HF. 2010. Peroxisomal membrane proteins insert into the endoplasmic reticulum. Mol. Biol. Cell 21:2057–65 [Google Scholar]
  158. van der Zand A, Gent J, Braakman I, Tabak HF. 2012. Biochemically distinct vesicles from the endoplasmic reticulum fuse to form peroxisomes. Cell 149:397–409 [Google Scholar]
  159. van der Zand A, Tabak HF. 2013. Peroxisomes: offshoots of the ER. Curr. Opin. Cell Biol. 25:449–54 [Google Scholar]
  160. 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 [Google Scholar]
  161. 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 [Google Scholar]
  162. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA. 2006. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:573–86 [Google Scholar]
  163. Voeltz GK, Rolls MM, Rapoport TA. 2002. Structural organization of the endoplasmic reticulum. EMBO Rep. 3:944–50 [Google Scholar]
  164. Walker ML, Burgess SA, Sellers JR, Wang F, Hammer JA III. et al. 2000. Two-headed binding of a processive myosin to F-actin. Nature 405:804–7 [Google Scholar]
  165. Weisman LS. 2006. Organelles on the move: insights from yeast vacuole inheritance. Nat. Rev. Mol. Cell Biol. 7:243–52 [Google Scholar]
  166. Wilfling F, Haas JT, Walther TC, Farese RV Jr. 2014. Lipid droplet biogenesis. Curr. Opin. Cell Biol. 29:39–45 [Google Scholar]
  167. Wolinski H, Kolb D, Hermann S, Koning RI, Kohlwein SD. 2011. A role for seipin in lipid droplet dynamics and inheritance in yeast. J. Cell Sci. 124:3894–904 [Google Scholar]
  168. Yan M, Rachubinski DA, Joshi S, Rachubinski RA, Subramani S. 2008. Dysferlin domain-containing proteins, Pex30p and Pex31p, localized to two compartments, control the number and size of oleate-induced peroxisomes in Pichia pastoris. Mol. Biol. Cell 19:885–98 [Google Scholar]
  169. 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 [Google Scholar]
  170. Yau RG, Peng Y, Valiathan RR, Birkeland SR, Wilson TE, Weisman LS. 2014. Release from myosin V via regulated recruitment of an E3 ubiquitin ligase controls organelle localization. Dev. Cell 28:520–33 [Google Scholar]
  171. 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 [Google Scholar]
  172. Yin H, Pruyne D, Huffaker TC, Bretscher A. 2000. Myosin V orientates the mitotic spindle in yeast. Nature 406:1013–15 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100814-125553
Loading
Motors, Anchors, and Connectors: Orchestrators of Organelle Inheritance
Annual Review of Cell and Developmental Biology 31, 55 (2015); https://doi.org/10.1146/annurev-cellbio-100814-125553
/content/journals/10.1146/annurev-cellbio-100814-125553
/content/journals/10.1146/annurev-cellbio-100814-125553
Loading

Data & Media loading...

Supplementary Data

  • Supplemental Video 1

    Inp1p: an organelle connector that tethers peroxisomes to the cell cortex. Budding yeast cells contain static (anchored) and mobile peroxisomes. Live-cell video microscopy was performed on wild-type cells expressing the peroxisomal matrix protein mCherry-PTS1 and Inp1p-3×GFP. Merged images of the red and green channels are presented. Static peroxisomes contain Inp1p and thus appear yellow, whereas mobile peroxisomes are devoid of Inp1p and appear red.

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error