Home LiteratureArticle Details
PMID: 16914519 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells.

Molecular biology of the cell ·Vol. 17 ·No. 11 ·2006-11-00 ·Pages 4606-18

Wójcik C, Rowicka M, Kudlicki A, Nowis D, McConnell E, Kujawa M, DeMartino GN

Abstract

Valosin-containing protein (VCP; p97; cdc48 in yeast) is a hexameric ATPase of the AAA family (ATPases with multiple cellular activities) involved in multiple cellular functions, including degradation of proteins by the ubiquitin (Ub)-proteasome system (UPS). We examined the consequences of the reduction of VCP levels after RNA interference (RNAi) of VCP. A new stringent method of microarray analysis demonstrated that only four transcripts were nonspecifically affected by RNAi, whereas approximately 30 transcripts were affected in response to reduced VCP levels in a sequence-independent manner. These transcripts encoded proteins involved in endoplasmic reticulum (ER) stress, apoptosis, and amino acid starvation. RNAi of VCP promoted the unfolded protein response, without eliciting a cytosolic stress response. RNAi of VCP inhibited the degradation of R-GFP (green fluorescent protein) and Ub-(G76V)-GFP, two cytoplasmic reporter proteins degraded by the UPS, and of alpha chain of the T-cell receptor, an established substrate of the ER-associated degradation (ERAD) pathway. Surprisingly, RNAi of VCP had no detectable effect on the degradation of two other ERAD substrates, alpha1-antitrypsin and deltaCD3. These results indicate that VCP is required for maintenance of normal ER structure and function and mediates the degradation of some proteins via the UPS, but is dispensable for the UPS-dependent degradation of some ERAD substrates.

MeSH Terms
Adenosine Triphosphatases Animals Cell Cycle Proteins/genetics,metabolism Down-Regulation/genetics Endoplasmic Reticulum/pathology Green Fluorescent Proteins/metabolism HeLa Cells Humans Mammals/metabolism Proteasome Endopeptidase Complex/metabolism Protein Folding Protein Processing, Post-Translational RNA Interference RNA, Messenger/genetics,metabolism RNA, Small Interfering/metabolism Substrate Specificity Transcription, Genetic Ubiquitins/metabolism Up-Regulation/genetics Vacuoles/ultrastructure Valosin Containing Protein
Chemicals
Cell Cycle Proteins RNA, Messenger RNA, Small Interfering Ubiquitins enhanced green fluorescent protein Green Fluorescent Proteins Proteasome Endopeptidase Complex Adenosine Triphosphatases VCP protein, human Valosin Containing Protein
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Wójcik Cezary
Department of Anatomy and Cell Biology, Indiana University School of Medicine, Evansville, IN 47712, USA.
Rowicka Maga
Kudlicki Andrzej
Nowis Dominika
McConnell Elizabeth
Kujawa Marek
DeMartino George N
References (70)
70 references, click to expand
  1. Mif1: a missing link between the unfolded protein response pathway and ER-associated protein degradation?
    Curr Protein Pept Sci. 2001 Jun;2(2):169-90 PMID: 12370023
  2. The mammalian endoplasmic reticulum as a sensor for cellular stress.
    Cell Stress Chaperones. 2002 Apr;7(2):222-9 PMID: 12380691
  3. Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1-Npl4.
    EMBO J. 2002 Nov 1;21(21):5645-52 PMID: 12411482
  4. Platelet-activating factor acetylhydrolase.
    Prostaglandins Other Lipid Mediat. 2002 Aug;68-69:83-94 PMID: 12432911
  5. Statistical design of reverse dye microarrays.
    Bioinformatics. 2003 May 1;19(7):803-10 PMID: 12724289
  6. The protein translocation channel binds proteasomes to the endoplasmic reticulum membrane.
    EMBO J. 2005 Jul 6;24(13):2284-93 PMID: 15973433
  7. For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection.
    EMBO J. 2003 May 15;22(10):2309-17 PMID: 12743025
  8. Expression profiling reveals off-target gene regulation by RNAi.
    Nat Biotechnol. 2003 Jun;21(6):635-7 PMID: 12754523
  9. ATPase activity of p97/valosin-containing protein is regulated by oxidative modification of the evolutionally conserved cysteine 522 residue in Walker A motif.
    J Biol Chem. 2005 Dec 16;280(50):41332-41 PMID: 16234241
  10. Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells.
    Cancer Res. 2005 Dec 15;65(24):11510-9 PMID: 16357160
  11. The role of p97/Cdc48p in endoplasmic reticulum-associated degradation: from the immune system to yeast.
    Curr Top Microbiol Immunol. 2005;300:95-125 PMID: 16573238
  12. p97: The cell's molecular purgatory?
    Mol Cell. 2006 Jun 23;22(6):713-7 PMID: 16793541
  13. The role of multiubiquitination in dislocation and degradation of the alpha subunit of the T cell antigen receptor.
    J Biol Chem. 1999 Dec 24;274(52):36852-8 PMID: 10601236
  14. Characterization of growth-differentiation factor 15, a transforming growth factor beta superfamily member induced following liver injury.
    Mol Cell Biol. 2000 May;20(10):3742-51 PMID: 10779363
  15. Enhancement of endoplasmic reticulum (ER) degradation of misfolded Null Hong Kong alpha1-antitrypsin by human ER mannosidase I.
    J Biol Chem. 2003 Jul 11;278(28):26287-94 PMID: 12736254
  16. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains.
    J Cell Biol. 2003 Jul 7;162(1):71-84 PMID: 12847084
  17. Activation of the interferon system by short-interfering RNAs.
    Nat Cell Biol. 2003 Sep;5(9):834-9 PMID: 12942087
  18. Use of modular substrates demonstrates mechanistic diversity and reveals differences in chaperone requirement of ERAD.
    J Biol Chem. 2003 Sep 19;278(38):35903-13 PMID: 12847107
  19. p97, a protein coping with multiple identities.
    J Cell Sci. 2003 Nov 1;116(Pt 21):4283-90 PMID: 14514884
  20. RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis.
    J Cell Sci. 2004 Jan 15;117(Pt 2):281-92 PMID: 14657277
  21. Quality control in the endoplasmic reticulum protein factory.
    Nature. 2003 Dec 18;426(6968):891-4 PMID: 14685249
  22. Distinct steps in dislocation of luminal endoplasmic reticulum-associated degradation substrates: roles of endoplamic reticulum-bound p97/Cdc48p and proteasome.
    J Biol Chem. 2004 Feb 6;279(6):3980-9 PMID: 14607830
  23. Rational siRNA design for RNA interference.
    Nat Biotechnol. 2004 Mar;22(3):326-30 PMID: 14758366
  24. Dye bias correction in dual-labeled cDNA microarray gene expression measurements.
    Environ Health Perspect. 2004 Mar;112(4):480-7 PMID: 15033598
  25. Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions.
    J Struct Biol. 2004 Apr-May;146(1-2):44-57 PMID: 15037236
  26. Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control.
    J Cell Biol. 2004 Apr12;165(1):41-52 PMID: 15078901
  27. Role of Herp in the endoplasmic reticulum stress response.
    Genes Cells. 2004 May;9(5):457-69 PMID: 15147274
  28. Uncoupling retro-translocation and degradation in the ER-associated degradation of a soluble protein.
    EMBO J. 2004 Jun 2;23(11):2206-15 PMID: 15152188
  29. Bilirubin benefits: cellular protection by a biliverdin reductase antioxidant cycle.
    Pediatrics. 2004 Jun;113(6):1776-82 PMID: 15173506
  30. Murine cystathionine gamma-lyase: complete cDNA and genomic sequences, promoter activity, tissue distribution and developmental expression.
    Biochem J. 2004 Jul 1;381(Pt 1):113-23 PMID: 15038791
  31. RNA oligonucleotide synthesis via 5'-silyl-2'-orthoester chemistry.
    Methods Mol Biol. 2005;288:33-50 PMID: 15333896
  32. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death.
    Mol Cell. 2004 Sep 10;15(5):767-76 PMID: 15350220
  33. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum.
    J Cell Biol. 2004 Oct 11;167(1):35-41 PMID: 15466483
  34. p97 and close encounters of every kind: a brief review.
    Biochem Soc Trans. 2004 Nov;32(Pt 5):715-20 PMID: 15493996
  35. In vivo half-life of a protein is a function of its amino-terminal residue.
    Science. 1986 Oct 10;234(4773):179-86 PMID: 3018930
  36. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  37. A proteolytic pathway that recognizes ubiquitin as a degradation signal.
    J Biol Chem. 1995 Jul 21;270(29):17442-56 PMID: 7615550
  38. Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes.
    Cell. 1995 Sep 22;82(6):885-93 PMID: 7553849
  39. An NSF-like ATPase, p97, and NSF mediate cisternal regrowth from mitotic Golgi fragments.
    Cell. 1995 Sep 22;82(6):905-14 PMID: 7553851
  40. Cdc48p interacts with Ufd3p, a WD repeat protein required for ubiquitin-mediated proteolysis in Saccharomyces cerevisiae.
    EMBO J. 1996 Sep 16;15(18):4884-99 PMID: 8890162
  41. Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the proteasome.
    Eur J Cell Biol. 1996 Nov;71(3):311-8 PMID: 8929570
  42. The alpha chain of the T cell antigen receptor is degraded in the cytosol.
    Immunity. 1997 Jul;7(1):113-22 PMID: 9252124
  43. Cytosolic degradation of T-cell receptor alpha chains by the proteasome.
    J Biol Chem. 1997 Aug 15;272(33):20800-4 PMID: 9252404
  44. Involvement of valosin-containing protein, an ATPase Co-purified with IkappaBalpha and 26 S proteasome, in ubiquitin-proteasome-mediated degradation of IkappaBalpha.
    J Biol Chem. 1998 Feb 6;273(6):3562-73 PMID: 9452483
  45. Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro.
    Cell. 1998 Mar 6;92(5):603-10 PMID: 9506515
  46. Organelle membrane fusion: a novel function for the syntaxin homolog Ufe1p in ER membrane fusion.
    Cell. 1998 Mar 6;92(5):611-20 PMID: 9506516
  47. Novel aspects of degradation of T cell receptor subunits from the endoplasmic reticulum (ER) in T cells: importance of oligosaccharide processing, ubiquitination, and proteasome-dependent removal from ER membranes.
    J Exp Med. 1998 Mar 16;187(6):835-46 PMID: 9500786
  48. Induction of spermidine/spermine N1-acetyltransferase in human cancer cells in response to increased production of reactive oxygen species.
    Biochem Pharmacol. 1998 Apr 1;55(7):1119-23 PMID: 9605436
  49. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3.
    Cell. 1998 Sep 4;94(5):615-23 PMID: 9741626
  50. The proteasome, a novel protease regulated by multiple mechanisms.
    J Biol Chem. 1999 Aug 6;274(32):22123-6 PMID: 10428771
  51. A computational study of off-target effects of RNA interference.
    Nucleic Acids Res. 2005;33(6):1834-47 PMID: 15800213
  52. Growth differentiation factor-15/macrophage inhibitory cytokine-1 induction after kidney and lung injury.
    Shock. 2005 Jun;23(6):543-8 PMID: 15897808
  53. Role of p97 AAA-ATPase in the retrotranslocation of the cholera toxin A1 chain, a non-ubiquitinated substrate.
    J Biol Chem. 2005 Jul 29;280(30):28127-32 PMID: 15932873
  54. ERAD: the long road to destruction.
    Nat Cell Biol. 2005 Aug;7(8):766-72 PMID: 16056268
  55. Endoplasmic reticulum-associated degradation.
    Annu Rev Cell Dev Biol. 2005;21:435-56 PMID: 16212502
  56. Coping with stress: eIF2 kinases and translational control.
    Biochem Soc Trans. 2006 Feb;34(Pt 1):7-11 PMID: 16246168
  57. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells.
    Nat Biotechnol. 2000 May;18(5):538-43 PMID: 10802622
  58. A complex of mammalian ufd1 and npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways.
    EMBO J. 2000 May 15;19(10):2181-92 PMID: 10811609
  59. Structure of the AAA ATPase p97.
    Mol Cell. 2000 Dec;6(6):1473-84 PMID: 11163219
  60. Endoplasmic reticulum (ER)-associated degradation of T cell receptor subunits. Involvement of ER-associated ubiquitin-conjugating enzymes (E2s).
    J Biol Chem. 2001 May 11;276(19):16193-200 PMID: 11278356
  61. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.
    Nature. 2001 May 24;411(6836):494-8 PMID: 11373684
  62. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways.
    J Clin Invest. 2001 May;107(10):1263-73 PMID: 11375416
  63. A novel ER alpha-mannosidase-like protein accelerates ER-associated degradation.
    EMBO Rep. 2001 May;2(5):415-22 PMID: 11375934
  64. Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex.
    Cell. 2001 Jun 1;105(5):645-55 PMID: 11389834
  65. Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation.
    Nat Cell Biol. 2001 Aug;3(8):740-4 PMID: 11483959
  66. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol.
    Nature. 2001 Dec 6;414(6864):652-6 PMID: 11740563
  67. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation.
    Mol Cell Biol. 2002 Jan;22(2):626-34 PMID: 11756557
  68. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor.
    Cell. 2001 Dec 28;107(7):881-91 PMID: 11779464
  69. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol.
    Nat Rev Mol Cell Biol. 2002 Apr;3(4):246-55 PMID: 11994744
  70. Transcriptional and translational control in the Mammalian unfolded protein response.
    Annu Rev Cell Dev Biol. 2002;18:575-99 PMID: 12142265
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2006-11-00
Epub
2006-00-16
Pages
4606-18
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1635394
Subset
IM
Grants
NIDDK NIH HHS · R01 DK046181 · United States
NIDDK NIH HHS · R56 DK046181 · United States
NIDDK NIH HHS · DK-46181 · United States
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: product@genelibs.com