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PMID: 18567582 Published · ppublish English Journal Article

IQGAP1 integrates Ca2+/calmodulin and B-Raf signaling.

The Journal of biological chemistry ·Vol. 283 ·No. 34 ·2008-08-22 ·Pages 22972-82

Ren JG, Li Z, Sacks DB

Abstract

Ca(2+) and calmodulin modulate numerous cellular functions, ranging from muscle contraction to the cell cycle. Accumulating evidence indicates that Ca(2+) and calmodulin regulate the MAPK signaling pathway at multiple positions in the cascade, but the molecular mechanism underlying these observations is poorly defined. We previously documented that IQGAP1 is a scaffold in the MAPK cascade. IQGAP1 binds to and regulates the activities of ERK, MEK, and B-Raf. Here we demonstrate that IQGAP1 integrates Ca(2+) and calmodulin with B-Raf signaling. In vitro analysis reveals that Ca(2+) promotes the direct binding of IQGAP1 to B-Raf. This interaction is inhibited by calmodulin in a Ca(2+)-regulated manner. Epidermal growth factor (EGF) is unable to stimulate B-Raf activity in fibroblasts treated with the Ca(2+) ionophore A23187. In contrast, chelation of intracellular free Ca(2+) concentrations ([Ca(2+)](i)) significantly enhances EGF-stimulated B-Raf activity, an effect that is dependent on IQGAP1. Incubation of cells with EGF augments the association of B-Raf with IQGAP1. Moreover, Ca(2+) regulates the association of B-Raf with IQGAP1 in cells. Increasing [Ca(2+)](i) with Ca(2+) ionophores significantly reduces co-immunoprecipitation of B-Raf and IQGAP1, whereas chelation of Ca(2+) enhances the interaction. Consistent with these findings, increasing and decreasing [Ca(2+)](i) increase and decrease, respectively, co-immunoprecipitation of calmodulin with IQGAP1. Collectively, our data identify a previously unrecognized mechanism in which the scaffold protein IQGAP1 couples Ca(2+) and calmodulin signaling to B-Raf function.

MeSH Terms
Animals Calcimycin/pharmacology Calcium/chemistry,metabolism Calmodulin/metabolism Epidermal Growth Factor/metabolism Fibroblasts/metabolism Gene Expression Regulation Humans Ionophores/pharmacology Mice Models, Biological Proto-Oncogene Proteins B-raf/metabolism Signal Transduction ras GTPase-Activating Proteins/metabolism,physiology
Chemicals
Calmodulin IQ motif containing GTPase activating protein 1 Ionophores ras GTPase-Activating Proteins Calcimycin Epidermal Growth Factor BRAF protein, human Braf protein, mouse Proto-Oncogene Proteins B-raf Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ren Jian-Guo
Department of Pathology, Brigham and Women's Hospital, Boston, Massachusetts 02115, USA.
Li Zhigang
Sacks David B
References (62)
62 references, click to expand
  1. IQGAP1 integrates Ca2+/calmodulin and Cdc42 signaling.
    J Biol Chem. 1999 Jan 1;274(1):464-70 PMID: 9867866
  2. N-cadherin regulates cytoskeletally associated IQGAP1/ERK signaling and memory formation.
    Neuron. 2007 Sep 6;55(5):786-98 PMID: 17785185
  3. Modulation of the Ras/Raf/MEK/ERK pathway by Ca(2+), and calmodulin.
    Cell Signal. 2002 Aug;14(8):649-54 PMID: 12020764
  4. The RAF proteins take centre stage.
    Nat Rev Mol Cell Biol. 2004 Nov;5(11):875-85 PMID: 15520807
  5. IQGAP proteins are integral components of cytoskeletal regulation.
    EMBO Rep. 2003 Jun;4(6):571-4 PMID: 12776176
  6. The mechanism for regulation of the F-actin binding activity of IQGAP1 by calcium/calmodulin.
    J Biol Chem. 2002 Apr 5;277(14):12324-33 PMID: 11809768
  7. Calmodulin binds to K-Ras, but not to H- or N-Ras, and modulates its downstream signaling.
    Mol Cell Biol. 2001 Nov;21(21):7345-54 PMID: 11585916
  8. Coordinating ERK/MAPK signalling through scaffolds and inhibitors.
    Nat Rev Mol Cell Biol. 2005 Nov;6(11):827-37 PMID: 16227978
  9. IQGAP1 in cellular signaling: bridging the GAP.
    Trends Cell Biol. 2006 May;16(5):242-9 PMID: 16595175
  10. Calmodulin inhibitor W13 induces sustained activation of ERK2 and expression of p21(cip1).
    J Biol Chem. 1998 Aug 21;273(34):22145-50 PMID: 9705360
  11. Signaling networks: the origins of cellular multitasking.
    Cell. 2000 Oct 13;103(2):193-200 PMID: 11057893
  12. Calmodulin modulates the interaction between IQGAP1 and Cdc42. Identification of IQGAP1 by nanoelectrospray tandem mass spectrometry.
    J Biol Chem. 1997 Jun 13;272(24):15419-25 PMID: 9182573
  13. The amino-terminal B-Raf-specific region mediates calcium-dependent homo- and hetero-dimerization of Raf.
    EMBO J. 2006 Aug 9;25(15):3556-64 PMID: 16858395
  14. Decoding complex Ca2+ signals through the modulation of Ras signaling.
    Curr Opin Cell Biol. 2006 Apr;18(2):157-61 PMID: 16488591
  15. Calcium activation of Ras mediated by neuronal exchange factor Ras-GRF.
    Nature. 1995 Aug 10;376(6540):524-7 PMID: 7637786
  16. Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/estrogen receptor transcriptional activation, and ovarian cancer progression.
    J Biol Chem. 2005 Mar 25;280(12):11961-72 PMID: 15655247
  17. Ionomycin enhances Ca2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane.
    Biochem J. 1994 Jun 15;300 ( Pt 3):665-72 PMID: 8010948
  18. The ins and outs of signalling.
    Nature. 2001 Jun 14;411(6839):759-62 PMID: 11459043
  19. CAPRI and RASAL impose different modes of information processing on Ras due to contrasting temporal filtering of Ca2+.
    J Cell Biol. 2005 Jul 18;170(2):183-90 PMID: 16009725
  20. MAPK cascade signalling and synaptic plasticity.
    Nat Rev Neurosci. 2004 Mar;5(3):173-83 PMID: 14976517
  21. The receptor protein-tyrosine phosphatase PTPmu interacts with IQGAP1.
    J Biol Chem. 2006 Feb 24;281(8):4903-10 PMID: 16380380
  22. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions.
    Endocr Rev. 2001 Apr;22(2):153-83 PMID: 11294822
  23. Calcium restriction allows cAMP activation of the B-Raf/ERK pathway, switching cells to a cAMP-dependent growth-stimulated phenotype.
    J Biol Chem. 2004 Sep 24;279(39):40419-30 PMID: 15263001
  24. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin- mediated cell-cell adhesion.
    Science. 1998 Aug 7;281(5378):832-5 PMID: 9694656
  25. Calmodulin regulates intracellular trafficking of epidermal growth factor receptor and the MAPK signaling pathway.
    Mol Biol Cell. 2002 Jun;13(6):2057-68 PMID: 12058069
  26. IQGAP1 as signal integrator: Ca2+, calmodulin, Cdc42 and the cytoskeleton.
    FEBS Lett. 2003 May 8;542(1-3):7-11 PMID: 12729888
  27. IQGAP1 binds Rap1 and modulates its activity.
    J Biol Chem. 2007 Jul 13;282(28):20752-62 PMID: 17517894
  28. The versatility and universality of calcium signalling.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):11-21 PMID: 11413485
  29. Identification of an actin cytoskeletal complex that includes IQGAP and the Cdc42 GTPase.
    J Biol Chem. 1997 Sep 26;272(39):24443-7 PMID: 9305904
  30. Regulation of cross-linking of actin filament by IQGAP1, a target for Cdc42.
    J Biol Chem. 1997 Nov 21;272(47):29579-83 PMID: 9368021
  31. Elucidation of the interaction of calmodulin with the IQ motifs of IQGAP1.
    J Biol Chem. 2003 Feb 7;278(6):4347-52 PMID: 12446675
  32. IQGAP1 and calmodulin modulate E-cadherin function.
    J Biol Chem. 1999 Dec 31;274(53):37885-92 PMID: 10608854
  33. Calmodulin: a prototypical calcium sensor.
    Trends Cell Biol. 2000 Aug;10(8):322-8 PMID: 10884684
  34. Self-association of IQGAP1: characterization and functional sequelae.
    J Biol Chem. 2005 Oct 14;280(41):34548-57 PMID: 16105843
  35. The human epidermal growth factor receptor contains a juxtamembrane calmodulin-binding site.
    Biochemistry. 1998 Jan 6;37(1):227-36 PMID: 9425043
  36. The role of scaffold proteins in MEK/ERK signalling.
    Biochem Soc Trans. 2006 Nov;34(Pt 5):833-6 PMID: 17052209
  37. The zinc- and calcium-binding S100B interacts and co-localizes with IQGAP1 during dynamic rearrangement of cell membranes.
    J Biol Chem. 2002 Dec 20;277(51):49998-50007 PMID: 12377780
  38. Regulation of MAP kinase signaling modules by scaffold proteins in mammals.
    Annu Rev Cell Dev Biol. 2003;19:91-118 PMID: 14570565
  39. Increasing complexity of Ras signaling.
    Oncogene. 1998 Sep 17;17(11 Reviews):1395-413 PMID: 9779987
  40. IQGAP1 is a component of Cdc42 signaling to the cytoskeleton.
    J Biol Chem. 2002 Jul 5;277(27):24753-63 PMID: 11948177
  41. The complexity of Raf-1 regulation.
    Curr Opin Cell Biol. 1997 Apr;9(2):174-9 PMID: 9069260
  42. Nerve growth factor activation of the extracellular signal-regulated kinase pathway is modulated by Ca(2+) and calmodulin.
    Mol Cell Biol. 2000 Mar;20(6):1931-46 PMID: 10688641
  43. IQGAP1 is a scaffold for mitogen-activated protein kinase signaling.
    Mol Cell Biol. 2005 Sep;25(18):7940-52 PMID: 16135787
  44. Regulation of mitogen-activated protein kinase phosphatase-1 expression by extracellular signal-related kinase-dependent and Ca2+-dependent signal pathways in Rat-1 cells.
    J Biol Chem. 1997 May 16;272(20):13309-19 PMID: 9148952
  45. Calcium signaling.
    Cell. 1995 Jan 27;80(2):259-68 PMID: 7834745
  46. Monoclonal antibody to calmodulin: development, characterization, and comparison with polyclonal anti-calmodulin antibodies.
    Anal Biochem. 1991 May 1;194(2):369-77 PMID: 1862939
  47. Protein modules and signalling networks.
    Nature. 1995 Feb 16;373(6515):573-80 PMID: 7531822
  48. CK2 Is a component of the KSR1 scaffold complex that contributes to Raf kinase activation.
    Curr Biol. 2007 Jan 23;17(2):179-84 PMID: 17174095
  49. Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras.
    Neuron. 1994 Jun;12(6):1207-21 PMID: 8011335
  50. IQGAP1 binds ERK2 and modulates its activity.
    J Biol Chem. 2004 Apr 23;279(17):17329-37 PMID: 14970219
  51. IQGAP1 modulates activation of B-Raf.
    Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10465-9 PMID: 17563371
  52. IQGAPs: integrators of the cytoskeleton, cell adhesion machinery, and signaling networks.
    Cell Motil Cytoskeleton. 2003 Jul;55(3):147-55 PMID: 12789660
  53. Calcium inhibits epidermal growth factor-induced activation of p21ras in human primary keratinocytes.
    Mol Cell Biol. 1994 Nov;14(11):7078-85 PMID: 7935423
  54. Mechanisms of regulating the Raf kinase family.
    Cell Signal. 2003 May;15(5):463-9 PMID: 12639709
  55. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions.
    Microbiol Mol Biol Rev. 2004 Jun;68(2):320-44 PMID: 15187187
  56. IQGAP1-mediated stimulation of transcriptional co-activation by beta-catenin is modulated by calmodulin.
    J Biol Chem. 2002 Mar 1;277(9):7453-65 PMID: 11734550
  57. IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs.
    EMBO J. 1996 Jun 17;15(12):2997-3005 PMID: 8670801
  58. Epidermal growth factor receptor: mechanisms of activation and signalling.
    Exp Cell Res. 2003 Mar 10;284(1):31-53 PMID: 12648464
  59. Three-dimensional structure of calmodulin.
    Nature. 1985 May 2-8;315(6014):37-40 PMID: 3990807
  60. Role of basal calcium in the EGF activation of MAP kinases.
    Oncogene. 2000 Mar 30;19(14):1853-6 PMID: 10777220
  61. Neuronal calcium activates a Rap1 and B-Raf signaling pathway via the cyclic adenosine monophosphate-dependent protein kinase.
    J Biol Chem. 2000 Feb 4;275(5):3722-8 PMID: 10652372
  62. Reversible intracellular translocation of KRas but not HRas in hippocampal neurons regulated by Ca2+/calmodulin.
    J Cell Biol. 2005 Aug 1;170(3):429-41 PMID: 16043511
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2008-08-22
Epub
2008-00-20
Pages
22972-82
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC5518677
Subset
IM
Grants
NCI NIH HHS · R01 CA075205 · United States
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