Home LiteratureArticle Details
PMID: 17646399 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Yeast peroxisomes multiply by growth and division.

The Journal of cell biology ·Vol. 178 ·No. 3 ·2007-07-30 ·Pages 399-410

Motley AM, Hettema EH

Abstract

Peroxisomes can arise de novo from the endoplasmic reticulum (ER) via a maturation process. Peroxisomes can also multiply by fission. We have investigated how these modes of multiplication contribute to peroxisome numbers in Saccharomyces cerevisiae and the role of the dynamin-related proteins (Drps) in these processes. We have developed pulse-chase and mating assays to follow the fate of existing peroxisomes, de novo-formed peroxisomes, and ER-derived preperoxisomal structures. We find that in wild-type (WT) cells, peroxisomes multiply by fission and do not form de novo. A marker for the maturation pathway, Pex3-GFP, is delivered from the ER to existing peroxisomes. Strikingly, cells lacking peroxisomes as a result of a segregation defect do form peroxisomes de novo. This process is slower than peroxisome multiplication in WT cells and is Drp independent. In contrast, peroxisome fission is Drp dependent. Our results show that peroxisomes multiply by growth and division under our assay conditions. We conclude that the ER to peroxisome pathway functions to supply existing peroxisomes with essential membrane constituents.

MeSH Terms
Dynamins/metabolism Endoplasmic Reticulum/metabolism GTP Phosphohydrolases/genetics,metabolism GTP-Binding Proteins/genetics,metabolism Membrane Proteins/genetics,metabolism Mitochondrial Proteins Peroxins Peroxisomes/metabolism,ultrastructure Protein Transport Recombinant Fusion Proteins/genetics,metabolism Saccharomyces cerevisiae/cytology,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Vesicular Transport Proteins
Chemicals
Membrane Proteins Mitochondrial Proteins PEX3 protein, S cerevisiae Peroxins Recombinant Fusion Proteins Saccharomyces cerevisiae Proteins Vesicular Transport Proteins GTP Phosphohydrolases GTP-Binding Proteins VPS1 protein, S cerevisiae DNM1 protein, S cerevisiae Dynamins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Motley Alison M
Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, England, UK.
Hettema Ewald H
References (46)
46 references, click to expand
  1. Identification of peroxisomal targeting signals located at the carboxy terminus of four peroxisomal proteins.
    J Cell Biol. 1988 Sep;107(3):897-905 PMID: 2901422
  2. The ER-peroxisome connection in plants: development of the "ER semi-autonomous peroxisome maturation and replication" model for plant peroxisome biogenesis.
    Biochim Biophys Acta. 2006 Dec;1763(12):1655-68 PMID: 17049631
  3. Immunoelectron microscopic observation of the behaviors of peroxisomal enzymes inducibly synthesized in an n-alkane-utilizable yeast cell, Candida tropicalis.
    Cell Struct Funct. 1996 Apr;21(2):117-22 PMID: 8790941
  4. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA.
    Mol Biol Cell. 1997 Jul;8(7):1233-42 PMID: 9243504
  5. The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast.
    J Cell Biol. 1998 Oct 19;143(2):333-49 PMID: 9786946
  6. Mutation in PEX16 is causal in the peroxisome-deficient Zellweger syndrome of complementation group D.
    Am J Hum Genet. 1998 Dec;63(6):1622-30 PMID: 9837814
  7. Peroxisome synthesis in the absence of preexisting peroxisomes.
    J Cell Biol. 1999 Jan 25;144(2):255-66 PMID: 9922452
  8. Human PEX19: cDNA cloning by functional complementation, mutation analysis in a patient with Zellweger syndrome, and potential role in peroxisomal membrane assembly.
    Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2116-21 PMID: 10051604
  9. Microtubule dynamics from mating through the first zygotic division in the budding yeast Saccharomyces cerevisiae.
    J Cell Biol. 1999 Mar 8;144(5):977-87 PMID: 10085295
  10. The cis acting sequences responsible for the differential decay of the unstable MFA2 and stable PGK1 transcripts in yeast include the context of the translational start codon.
    RNA. 1999 Mar;5(3):420-33 PMID: 10094310
  11. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae.
    Yeast. 1999 Oct;15(14):1541-53 PMID: 10514571
  12. Molecular and neurologic findings of peroxisome biogenesis disorders.
    J Child Neurol. 2005 Apr;20(4):326-9 PMID: 15921234
  13. Inp1p is a peroxisomal membrane protein required for peroxisome inheritance in Saccharomyces cerevisiae.
    J Cell Biol. 2005 Jun 6;169(5):765-75 PMID: 15928207
  14. Atg17 regulates the magnitude of the autophagic response.
    Mol Biol Cell. 2005 Jul;16(7):3438-53 PMID: 15901835
  15. Contribution of the endoplasmic reticulum to peroxisome formation.
    Cell. 2005 Jul 15;122(1):85-95 PMID: 16009135
  16. Peroxisome biogenesis: end of the debate.
    Curr Biol. 2005 Sep 20;15(18):R774-6 PMID: 16169481
  17. Endoplasmic reticulum-directed Pex3p routes to peroxisomes and restores peroxisome formation in a Saccharomyces cerevisiae pex3Delta strain.
    J Biol Chem. 2005 Oct 7;280(40):34350-7 PMID: 16100114
  18. Pex3p initiates the formation of a preperoxisomal compartment from a subdomain of the endoplasmic reticulum in Saccharomyces cerevisiae.
    J Biol Chem. 2005 Oct 14;280(41):34933-9 PMID: 16087670
  19. Dynamin-related proteins and Pex11 proteins in peroxisome division and proliferation.
    FEBS J. 2005 Oct;272(20):5169-81 PMID: 16218949
  20. The return of the peroxisome.
    J Cell Sci. 2006 Mar 15;119(Pt 6):989-94 PMID: 16525120
  21. The dynamin-like protein Vps1p of the yeast Saccharomyces cerevisiae associates with peroxisomes in a Pex19p-dependent manner.
    J Biol Chem. 2006 May 5;281(18):12817-23 PMID: 16520372
  22. Saccharomyces cerevisiae pex3p and pex19p are required for proper localization and stability of peroxisomal membrane proteins.
    EMBO J. 2000 Jan 17;19(2):223-33 PMID: 10637226
  23. Inhibitors of COPI and COPII do not block PEX3-mediated peroxisome synthesis.
    J Cell Biol. 2000 Jun 26;149(7):1345-60 PMID: 10871277
  24. Defective peroxisome membrane synthesis due to mutations in human PEX3 causes Zellweger syndrome, complementation group G.
    Am J Hum Genet. 2000 Oct;67(4):967-75 PMID: 10958759
  25. PEX3 is the causal gene responsible for peroxisome membrane assembly-defective Zellweger syndrome of complementation group G.
    Am J Hum Genet. 2000 Oct;67(4):976-81 PMID: 10968777
  26. Division of mitochondria requires a novel DNM1-interacting protein, Net2p.
    Mol Biol Cell. 2001 Feb;12(2):309-21 PMID: 11179417
  27. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae.
    J Cell Biol. 2001 Dec 10;155(6):979-90 PMID: 11733545
  28. Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding.
    Plant Cell Physiol. 2002 Apr;43(4):384-92 PMID: 11978866
  29. A molecular motor or a regulator? Dynamin's in a class of its own.
    Biochemistry. 2003 Feb 18;42(6):1369-76 PMID: 12578348
  30. Dynamin-like protein 1 is involved in peroxisomal fission.
    J Biol Chem. 2003 Mar 7;278(10):8597-605 PMID: 12499366
  31. A yeast homologue of Hsp70, Ssa1p, regulates turnover of the MFA2 transcript through its AU-rich 3' untranslated region.
    Mol Cell Biol. 2003 Apr;23(8):2623-32 PMID: 12665566
  32. The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11.
    J Biol Chem. 2003 May 9;278(19):17012-20 PMID: 12618434
  33. Peroxisomes start their life in the endoplasmic reticulum.
    Traffic. 2003 Aug;4(8):512-8 PMID: 12839494
  34. Peroxisome biogenesis: advances and conundrums.
    Curr Opin Cell Biol. 2003 Aug;15(4):489-97 PMID: 12892791
  35. The dynamin superfamily: universal membrane tubulation and fission molecules?
    Nat Rev Mol Cell Biol. 2004 Feb;5(2):133-47 PMID: 15040446
  36. An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division.
    Plant J. 2004 May;38(3):487-98 PMID: 15086806
  37. Peroxisome turnover by micropexophagy: an autophagy-related process.
    Trends Cell Biol. 2004 Sep;14(9):515-23 PMID: 15350980
  38. An electron microscopical study of the development of peroxisomes during formation and germination of ascospores in the methylotrophic yeast Hansenula polymorpha.
    Antonie Van Leeuwenhoek. 1980;46(2):129-41 PMID: 7436401
  39. Synthesis of a major integral membrane polypeptide of rat liver peroxisomes on free polysomes.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):7127-31 PMID: 6594687
  40. Biogenesis of peroxisomes.
    Annu Rev Cell Biol. 1985;1:489-530 PMID: 3916321
  41. Peroxisome division is impaired in a CHO cell mutant with an inactivating point-mutation in dynamin-like protein 1 gene.
    Exp Cell Res. 2006 May 15;312(9):1671-84 PMID: 16529741
  42. The peroxisomal membrane protein Inp2p is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae.
    Dev Cell. 2006 May;10(5):587-600 PMID: 16678774
  43. The origin and maintenance of mammalian peroxisomes involves a de novo PEX16-dependent pathway from the ER.
    J Cell Biol. 2006 May 22;173(4):521-32 PMID: 16717127
  44. Peroxisome biogenesis: the peroxisomal endomembrane system and the role of the ER.
    J Cell Biol. 2006 Jul 3;174(1):11-7 PMID: 16801391
  45. Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae.
    J Cell Sci. 2006 Oct 1;119(Pt 19):3994-4001 PMID: 16968746
  46. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2007-07-30
Epub
2007-00-23
Pages
399-410
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2064844
Subset
IM
Grants
Wellcome Trust · United Kingdom
Wellcome Trust · 073257 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]