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PMID: 12093732 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection.

The EMBO journal ·Vol. 21 ·No. 13 ·2002-07-01 ·Pages 3307-16

Zanata SM, Lopes MH, Mercadante AF, Hajj GN, Chiarini LB, Nomizo R, Freitas AR, Cabral AL, Lee KS, Juliano MA, de Oliveira E, Jachieri SG, Burlingame A, Huang L, Linden R, Brentani RR, Martins VR

Abstract

Prions are composed of an isoform of a normal sialoglycoprotein called PrP(c), whose physiological role has been under investigation, with focus on the screening for ligands. Our group described a membrane 66 kDa PrP(c)-binding protein with the aid of antibodies against a peptide deduced by complementary hydropathy. Using these antibodies in western blots from two-dimensional protein gels followed by sequencing the specific spot, we have now identified the molecule as stress-inducible protein 1 (STI1). We show that this protein is also found at the cell membrane besides the cytoplasm. Both proteins interact in a specific and high affinity manner with a K(d) of 10(-7) M. The interaction sites were mapped to amino acids 113-128 from PrP(c) and 230-245 from STI1. Cell surface binding and pull-down experiments showed that recombinant PrP(c) binds to cellular STI1, and co-immunoprecipitation assays strongly suggest that both proteins are associated in vivo. Moreover, PrP(c) interaction with either STI1 or with the peptide we found that represents the binding domain in STI1 induce neuroprotective signals that rescue cells from apoptosis.

MeSH Terms
Animals Anisomycin/antagonists & inhibitors,pharmacology Apoptosis/drug effects Binding Sites Copper/metabolism Cyclic AMP/physiology Cyclic AMP-Dependent Protein Kinases/physiology Eye Proteins/chemistry,metabolism Heat-Shock Proteins/chemistry,isolation & purification,metabolism Hydrophobic and Hydrophilic Interactions Laminin/metabolism Macromolecular Substances Membrane Proteins/metabolism Mice Molecular Chaperones/chemistry,isolation & purification,metabolism Nerve Tissue Proteins/chemistry,isolation & purification,metabolism Neurons/cytology,metabolism Organ Culture Techniques Peptide Fragments/metabolism PrPC Proteins/metabolism Protein Binding Protein Interaction Mapping Recombinant Fusion Proteins/metabolism Retina/cytology,drug effects Signal Transduction
Chemicals
Eye Proteins Heat-Shock Proteins Laminin Macromolecular Substances Membrane Proteins Molecular Chaperones Nerve Tissue Proteins Peptide Fragments PrPC Proteins Recombinant Fusion Proteins Stip1 protein, mouse Anisomycin Copper Cyclic AMP Cyclic AMP-Dependent Protein Kinases
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Zanata Silvio M
Ludwig Institute for Cancer Research, São Paulo Branch, Rua Prof. Antônio Prudente 109 4A, São Paulo 01509010, Brasil.
Lopes Marilene H
Mercadante Adriana F
Hajj Glaucia N M
Chiarini Luciana B
Nomizo Regina
Freitas Adriana R O
Cabral Ana L B
Lee Kil S
Juliano Maria A
de Oliveira Elizabeth
Jachieri Saul G
Burlingame Alma
Huang Lan
Linden Rafael
Brentani Ricardo R
Martins Vilma R
References (64)
64 references, click to expand
  1. Normal prion protein has an activity like that of superoxide dismutase.
    Biochem J. 1999 Nov 15;344 Pt 1:1-5 PMID: 10548526
  2. Prion protein gene expression in cultured cells.
    Protein Eng. 1988 Apr;2(1):69-76 PMID: 2908139
  3. Structure and function of laminin: anatomy of a multidomain glycoprotein.
    FASEB J. 1990 Feb 1;4(2):148-60 PMID: 2404817
  4. A novel pathway for secretory proteins?
    Trends Biochem Sci. 1990 Mar;15(3):86-8 PMID: 2139259
  5. Prion dementia without characteristic pathology.
    Lancet. 1990 Jul 7;336(8706):7-9 PMID: 1973256
  6. A protein partially expressed on the surface of HepG2 cells that binds lipoproteins specifically is nucleolin.
    Biochemistry. 1990 Oct 16;29(41):9708-13 PMID: 2176855
  7. Fatal familial insomnia: a second kindred with mutation of prion protein gene at codon 178.
    Neurology. 1992 Mar;42(3 Pt 1):669-70 PMID: 1347910
  8. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein.
    Nature. 1992 Apr 16;356(6370):577-82 PMID: 1373228
  9. Molecular cloning and expression of a transformation-sensitive human protein containing the TPR motif and sharing identity to the stress-inducible yeast protein STI1.
    J Biol Chem. 1992 Apr 25;267(12):8485-91 PMID: 1569099
  10. Collagen binding site in collagenase can be determined using the concept of sense-antisense peptide interactions.
    J Biol Chem. 1992 Jul 5;267(19):13763-7 PMID: 1320031
  11. Neurotoxicity of a prion protein fragment.
    Nature. 1993 Apr 8;362(6420):543-6 PMID: 8464494
  12. Actin is a surface component of calf pulmonary artery endothelial cells in culture.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):3815-9 PMID: 8483899
  13. Mice devoid of PrP are resistant to scrapie.
    Cell. 1993 Jul 2;73(7):1339-47 PMID: 8100741
  14. An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II.
    J Biol Chem. 1994 Aug 19;269(33):21191-7 PMID: 8063740
  15. Is hydropathic complementarity involved in antigen-antibody binding?
    Mol Immunol. 1995 Mar;32(4):303-8 PMID: 7536893
  16. Stress-inducible, murine protein mSTI1. Characterization of binding domains for heat shock proteins and in vitro phosphorylation by different kinases.
    J Biol Chem. 1997 Jan 17;272(3):1876-84 PMID: 8999875
  17. Contact activation: a revision.
    Thromb Haemost. 1997 Jul;78(1):101-7 PMID: 9198136
  18. Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity.
    Exp Neurol. 1997 Jul;146(1):104-12 PMID: 9225743
  19. Isolation of a mouse cDNA encoding mSTI1, a stress-inducible protein containing the TPR motif.
    Gene. 1997 Jul 31;194(2):277-82 PMID: 9272871
  20. Prion research: the next frontiers.
    Nature. 1997 Oct 23;389(6653):795-8 PMID: 9349807
  21. Cytokeratin 18 is expressed on the hepatocyte plasma membrane surface and interacts with thrombin-antithrombin complexes.
    J Biol Chem. 1997 Nov 7;272(45):28574-81 PMID: 9353322
  22. A prion-linked psychiatric disorder.
    Nature. 1997 Nov 20;390(6657):241 PMID: 9384372
  23. Complementary hydropathy identifies a cellular prion protein receptor.
    Nat Med. 1997 Dec;3(12):1376-82 PMID: 9396608
  24. The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells.
    Nat Med. 1997 Dec;3(12):1383-8 PMID: 9396609
  25. Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding.
    FEBS Lett. 1997 Nov 17;417(3):400-4 PMID: 9409760
  26. The cellular prion protein binds copper in vivo.
    Nature. 1997 Dec 18-25;390(6661):684-7 PMID: 9414160
  27. Formation of the 67-kDa laminin receptor by acylation of the precursor.
    J Cell Biochem. 1998 Jun 1;69(3):244-51 PMID: 9581863
  28. Can loss-of-function prion-related diseases exist?
    Mol Psychiatry. 1998 May;3(3):196-7 PMID: 9672888
  29. Prions.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13363-83 PMID: 9811807
  30. Copper stimulates endocytosis of the prion protein.
    J Biol Chem. 1998 Dec 11;273(50):33107-10 PMID: 9837873
  31. Prions prevent neuronal cell-line death.
    Nature. 1999 Jul 15;400(6741):225-6 PMID: 10421360
  32. Role of accurate mass measurement (+/- 10 ppm) in protein identification strategies employing MS or MS/MS and database searching.
    Anal Chem. 1999 Jul 15;71(14):2871-82 PMID: 10424174
  33. Identification and isolation of three proteasome subunits and their encoding genes from Trypanosoma brucei.
    Mol Biochem Parasitol. 1999 Aug 20;102(2):211-23 PMID: 10498178
  34. Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension.
    Neuron. 1995 May;14(5):941-8 PMID: 7748561
  35. Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein.
    Cell. 1995 Oct 6;83(1):79-90 PMID: 7553876
  36. Two-dimensional polyacrylamide gel electrophoresis with immobilized pH gradients in the first dimension (IPG-Dalt): the state of the art and the controversy of vertical versus horizontal systems.
    Electrophoresis. 1995 Jul;16(7):1079-86 PMID: 7498150
  37. Induced release of cell surface protein kinase yields CK1- and CK2-like enzymes in tandem.
    J Biol Chem. 1996 Jan 5;271(1):111-9 PMID: 8550544
  38. De novo generation of a PrPSc-like conformation in living cells.
    Nat Cell Biol. 1999 Oct;1(6):358-61 PMID: 10559963
  39. Selective sensitivity of early postmitotic retinal cells to apoptosis induced by inhibition of protein synthesis.
    Eur J Neurosci. 1999 Dec;11(12):4349-56 PMID: 10594661
  40. Increased sensitivity to seizures in mice lacking cellular prion protein.
    Epilepsia. 1999 Dec;40(12):1679-82 PMID: 10612329
  41. Cellular prion protein binds laminin and mediates neuritogenesis.
    Brain Res Mol Brain Res. 2000 Mar 10;76(1):85-92 PMID: 10719218
  42. Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A.
    Mech Dev. 2000 May;93(1-2):95-104 PMID: 10781943
  43. Susceptibility of the prion protein to enzymic phosphorylation.
    Biochem Biophys Res Commun. 2000 May 10;271(2):337-41 PMID: 10799298
  44. Signal transduction through prion protein.
    Science. 2000 Sep 15;289(5486):1925-8 PMID: 10988071
  45. Laminin-induced PC-12 cell differentiation is inhibited following laser inactivation of cellular prion protein.
    FEBS Lett. 2000 Oct 6;482(3):257-60 PMID: 11024471
  46. Copper refolding of prion protein.
    Biochem Biophys Res Commun. 2000 Oct 5;276(3):1217-24 PMID: 11027613
  47. The cellular prion protein colocalizes with the dystroglycan complex in the brain.
    J Neurochem. 2000 Nov;75(5):1889-97 PMID: 11032878
  48. Bovine prion protein as a modulator of protein kinase CK2.
    Biochem J. 2000 Nov 15;352 Pt 1:191-6 PMID: 11062072
  49. The in vitro phosphorylation of the co-chaperone mSTI1 by cell cycle kinases substantiates a predicted casein kinase II-p34cdc2-NLS (CcN) motif.
    Biol Chem. 2000 Nov;381(11):1133-8 PMID: 11154072
  50. Function of PrP(C) as a copper-binding protein at the synapse.
    Arch Virol Suppl. 2000;(16):239-49 PMID: 11214928
  51. Insights into the physiological function of cellular prion protein.
    Braz J Med Biol Res. 2001 May;34(5):585-95 PMID: 11323744
  52. Infection by Trypanosoma cruzi. Identification of a parasite ligand and its host cell receptor.
    J Biol Chem. 2001 Jun 1;276(22):19382-9 PMID: 11278913
  53. Proteasomes and ubiquitin are involved in the turnover of the wild-type prion protein.
    EMBO J. 2001 Oct 1;20(19):5383-91 PMID: 11574470
  54. Internalization of mammalian fluorescent cellular prion protein and N-terminal deletion mutants in living cells.
    J Neurochem. 2001 Oct;79(1):79-87 PMID: 11595760
  55. The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein.
    EMBO J. 2001 Nov 1;20(21):5863-75 PMID: 11689427
  56. Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor.
    EMBO J. 2001 Nov 1;20(21):5876-86 PMID: 11689428
  57. Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein.
    J Mol Biol. 2001 Dec 14;314(5):1209-25 PMID: 11743735
  58. Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation.
    Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):14955-60 PMID: 11742063
  59. Antagonistic effects of Rnd1 and RhoD GTPases regulate receptor activity in Semaphorin 3A-induced cytoskeletal collapse.
    J Neurosci. 2002 Jan 15;22(2):471-7 PMID: 11784792
  60. Regulation of the cellular prion protein gene expression depends on chromatin conformation.
    J Biol Chem. 2002 Feb 15;277(7):5675-82 PMID: 11739375
  61. Cellular prion protein: on the road for functions.
    FEBS Lett. 2002 Feb 13;512(1-3):25-8 PMID: 11852045
  62. Cellular prion protein transduces neuroprotective signals.
    EMBO J. 2002 Jul 1;21(13):3317-26 PMID: 12093733
  63. Similarity between the corticotropin (ACTH) receptor and a peptide encoded by an RNA that is complementary to ACTH mRNA.
    Proc Natl Acad Sci U S A. 1985 Mar;82(5):1372-5 PMID: 2983342
  64. Biological implications of complementary hydropathy of amino acids.
    J Theor Biol. 1988 Dec 19;135(4):495-9 PMID: 3256734
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/cdf325
Published
2002-07-01
Pages
3307-16
Language
English
Region
England
NLM ID
8208664
PMCID
PMC125391
Subset
IM
External Links
PubMed source DOI: 10.1093/emboj/cdf325 PMC Full Text View journal details
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