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PMID: 15911776 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Targeted expression of the inositol 1,4,5-triphosphate receptor (IP3R) ligand-binding domain releases Ca2+ via endogenous IP3R channels.

Várnai P, Balla A, Hunyady L, Balla T

Abstract

Virtually all functions of a cell are influenced by cytoplasmic [Ca(2+)] increases. Inositol 1,4,5-trisphosphate receptor (IP(3)R) channels, located in the endoplasmic reticulum (ER), release Ca(2+) in response to binding of the second messenger, IP(3).IP(3)Rs thus are part of the information chain interpreting external signals and transforming them into cytoplasmic Ca(2+) transients. IP(3)Rs function as tetramers, each unit comprising an N-terminal ligand-binding domain (LBD) and a C-terminal channel domain linked by a long regulatory region. It is not yet understood how the binding of IP(3) to the LBD regulates the gating properties of the channel. Here, we use the expression of IP(3) binding protein domains tethered to the surface of the endoplasmic reticulum (ER) to show that the all-helical domain of the IP(3)R LBD is capable of depleting the ER Ca(2+) pools by opening the endogenous IP(3)Rs, even without IP(3) binding. This effect requires the domain to be within 50 A of the ER membrane and is impaired by the presence of the N-terminal inhibitory segment on the LBD. These findings raise the possibility that the helical domain of the LBD functions as an effector module possibly interacting with the channel domain, thereby being part of the gating mechanisms by which the IP(3)-induced conformational change within the LBD regulates Ca(2+) release.

MeSH Terms
Animals COS Cells Calcium/metabolism Calcium Channels/metabolism,physiology Chlorocebus aethiops Cytoplasm/metabolism Endoplasmic Reticulum/metabolism Genetic Vectors/genetics Inositol 1,4,5-Trisphosphate/metabolism Inositol 1,4,5-Trisphosphate Receptors Ion Channel Gating/physiology Ligands Luminescent Proteins Protein Binding Protein Structure, Tertiary Receptors, Cytoplasmic and Nuclear/metabolism,physiology
Chemicals
Calcium Channels Inositol 1,4,5-Trisphosphate Receptors Ligands Luminescent Proteins Receptors, Cytoplasmic and Nuclear red fluorescent protein Inositol 1,4,5-Trisphosphate Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Várnai Péter
Endocrinology and Reproduction Research Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA.
Balla András
Hunyady László
Balla Tamas
References (32)
32 references, click to expand
  1. Direct association of ligand-binding and pore domains in homo- and heterotetrameric inositol 1,4,5-trisphosphate receptors.
    EMBO J. 2000 Oct 16;19(20):5450-9 PMID: 11032812
  2. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466-70 PMID: 2138778
  3. The ligand binding site and transduction mechanism in the inositol-1,4,5-triphosphate receptor.
    EMBO J. 1990 Dec;9(12):3893-8 PMID: 2174351
  4. Structural and functional characterization of inositol 1,4,5-trisphosphate receptor channel from mouse cerebellum.
    J Biol Chem. 1991 Jan 15;266(2):1109-16 PMID: 1845986
  5. The capacitative model for receptor-activated calcium entry.
    Adv Pharmacol. 1991;22:251-69 PMID: 1659864
  6. Inositol 1,4,5-trisphosphate receptor.
    Trends Pharmacol Sci. 1993 Mar;14(3):86-9 PMID: 8387706
  7. Luminal communication between intracellular calcium stores modulated by GTP and the cytoskeleton.
    J Biol Chem. 1994 Apr 8;269(14):10280-7 PMID: 8144609
  8. The inositol trisphosphate calcium channel is inactivated by inositol trisphosphate.
    Nature. 1994 Aug 11;370(6489):474-7 PMID: 8047168
  9. Decoding of cytosolic calcium oscillations in the mitochondria.
    Cell. 1995 Aug 11;82(3):415-24 PMID: 7634331
  10. The transmembrane domain of a carboxyl-terminal anchored protein determines localization to the endoplasmic reticulum.
    J Biol Chem. 1997 Jan 17;272(3):1970-5 PMID: 8999888
  11. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor.
    EMBO J. 1997 Jun 2;16(11):3078-88 PMID: 9214625
  12. Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression.
    Nature. 1998 Apr 30;392(6679):936-41 PMID: 9582076
  13. Cooperative formation of the ligand-binding site of the inositol 1,4, 5-trisphosphate receptor by two separable domains.
    J Biol Chem. 1999 Jan 1;274(1):328-34 PMID: 9867847
  14. Molecular properties of inositol 1,4,5-trisphosphate receptors.
    Cell Calcium. 1999 Mar;25(3):247-64 PMID: 10378086
  15. Location of the permeation pathway in the recombinant type 1 inositol 1,4,5-trisphosphate receptor.
    J Gen Physiol. 1999 Aug;114(2):243-50 PMID: 10436000
  16. Subunit oligomerization, and topology of the inositol 1,4, 5-trisphosphate receptor.
    J Biol Chem. 1999 Oct 8;274(41):29483-92 PMID: 10506212
  17. The versatility and universality of calcium signalling.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):11-21 PMID: 11413485
  18. Regulation of Ca2+-release-activated Ca2+ current (Icrac) by ryanodine receptors in inositol 1,4,5-trisphosphate-receptor-deficient DT40 cells.
    Biochem J. 2001 Nov 15;360(Pt 1):17-22 PMID: 11695987
  19. A novel recombinant hyperaffinity inositol 1,4,5-trisphosphate (IP(3)) absorbent traps IP(3), resulting in specific inhibition of IP(3)-mediated calcium signaling.
    J Biol Chem. 2002 Mar 8;277(10):8106-13 PMID: 11741904
  20. Identification of a family of calcium sensors as protein ligands of inositol trisphosphate receptor Ca(2+) release channels.
    Proc Natl Acad Sci U S A. 2002 May 28;99(11):7711-6 PMID: 12032348
  21. A monomeric red fluorescent protein.
    Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):7877-82 PMID: 12060735
  22. Inositol lipid binding and membrane localization of isolated pleckstrin homology (PH) domains. Studies on the PH domains of phospholipase C delta 1 and p130.
    J Biol Chem. 2002 Jul 26;277(30):27412-22 PMID: 12019260
  23. Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand.
    Nature. 2002 Dec 12;420(6916):696-700 PMID: 12442173
  24. IP3 receptors and their regulation by calmodulin and cytosolic Ca2+.
    Cell Calcium. 2002 Nov-Dec;32(5-6):321-34 PMID: 12543092
  25. IRBIT, a novel inositol 1,4,5-trisphosphate (IP3) receptor-binding protein, is released from the IP3 receptor upon IP3 binding to the receptor.
    J Biol Chem. 2003 Mar 21;278(12):10602-12 PMID: 12525476
  26. Critical regions for activation gating of the inositol 1,4,5-trisphosphate receptor.
    J Biol Chem. 2003 May 9;278(19):16551-60 PMID: 12621039
  27. Calcium oscillations in T-cells: mechanisms and consequences for gene expression.
    Biochem Soc Trans. 2003 Oct;31(Pt 5):925-9 PMID: 14505450
  28. The regulatory domain of the inositol 1,4,5-trisphosphate receptor is necessary to keep the channel domain closed: possible physiological significance of specific cleavage by caspase 3.
    Biochem J. 2004 Jan 15;377(Pt 2):299-307 PMID: 12968951
  29. IP(3) receptors: the search for structure.
    Trends Biochem Sci. 2004 Apr;29(4):210-9 PMID: 15082315
  30. Fluorescent biosensor for quantitative real-time measurements of inositol 1,4,5-trisphosphate in single living cells.
    J Biol Chem. 2004 Sep 10;279(37):38095-8 PMID: 15272011
  31. Inositol trisphosphate, a novel second messenger in cellular signal transduction.
    Nature. 1984 Nov 22-28;312(5992):315-21 PMID: 6095092
  32. Inhibition of Ca(2+) signalling by p130, a phospholipase-C-related catalytically inactive protein: critical role of the p130 pleckstrin homology domain.
    Biochem J. 2000 Jul 1;349(Pt 1):357-68 PMID: 10861248
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-05-31
Epub
2005-00-23
Pages
7859-64
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1142351
Subset
IM
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