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PMID: 19016655 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

An essential role for the Glut1 PDZ-binding motif in growth factor regulation of Glut1 degradation and trafficking.

The Biochemical journal ·Vol. 418 ·No. 2 ·2009-03-01 ·Pages 345-67

Wieman HL, Horn SR, Jacobs SR, Altman BJ, Kornbluth S, Rathmell JC

Abstract

Cell surface localization of the Glut (glucose transporter), Glut1, is a cytokine-controlled process essential to support the metabolism and survival of haemopoietic cells. Molecular mechanisms that regulate Glut1 trafficking, however, are not certain. In the present study, we show that a C-terminal PDZ-binding motif in Glut1 is critical to promote maximal cytokine-stimulated Glut1 cell surface localization and prevent Glut1 lysosomal degradation in the absence of growth factor. Disruption of this PDZ-binding sequence through deletion or point mutation sharply decreased surface Glut1 levels and led to rapid targeting of internalized Glut1 to lysosomes for proteolysis, particularly in growth factor-deprived cells. The PDZ-domain protein, GIPC (G(alpha)-interacting protein-interacting protein, C-terminus), bound to Glut1 in part via the Glut1 C-terminal PDZ-binding motif, and we found that GIPC deficiency decreased Glut1 surface levels and glucose uptake. Unlike the Glut1 degradation observed on mutation of the Glut1 PDZ-binding domain, however, GIPC deficiency resulted in accumulation of intracellular Glut1 in a pool distinct from the recycling pathway of the TfR (transferrin receptor). Blockade of Glut1 lysosomal targeting after growth factor withdrawal also led to intracellular accumulation of Glut1, a portion of which could be rapidly restored to the cell surface after growth factor stimulation. These results indicate that the C-terminal PDZ-binding motif of Glut1 plays a key role in growth factor regulation of glucose uptake by both allowing GIPC to promote Glut1 trafficking to the cell surface and protecting intracellular Glut1 from lysosomal degradation after growth factor withdrawal, thus allowing the potential for a rapid return of intracellular Glut1 to the cell surface on restimulation.

MeSH Terms
Adaptor Proteins, Signal Transducing/metabolism,physiology Amino Acid Sequence/physiology Animals Antigens, Surface/drug effects,metabolism Cells, Cultured Glucose/metabolism Glucose Transporter Type 1/chemistry,metabolism Humans Intercellular Signaling Peptides and Proteins/pharmacology Lysosomes/metabolism Mice PDZ Domains/physiology Protein Binding Protein Processing, Post-Translational/drug effects Protein Transport/drug effects Rats
Chemicals
Adaptor Proteins, Signal Transducing Antigens, Surface GIPC1 protein, human Glucose Transporter Type 1 Intercellular Signaling Peptides and Proteins Glucose
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wieman Heather L
Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, NC 27710, USA.
Horn Sarah R
Jacobs Sarah R
Altman Brian J
Kornbluth Sally
Rathmell Jeffrey C
References (40)
40 references, click to expand
  1. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria.
    Cell. 1997 Nov 28;91(5):627-37 PMID: 9393856
  2. The rab7 GTPase resides on a vesicular compartment connected to lysosomes.
    J Cell Sci. 1995 Nov;108 ( Pt 11):3349-58 PMID: 8586647
  3. Interactions of GIPC with dopamine D2, D3 but not D4 receptors define a novel mode of regulation of G protein-coupled receptors.
    Mol Biol Cell. 2004 Feb;15(2):696-705 PMID: 14617818
  4. GLUT1CBP(TIP2/GIPC1) interactions with GLUT1 and myosin VI: evidence supporting an adapter function for GLUT1CBP.
    Mol Biol Cell. 2005 Sep;16(9):4183-201 PMID: 15975910
  5. Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake.
    Mol Biol Cell. 2002 Jul;13(7):2276-88 PMID: 12134068
  6. PDZ domains-glue and guide.
    Mol Biol Rep. 2003 Jun;30(2):69-82 PMID: 12841577
  7. Parathyroid hormone leads to the lysosomal degradation of the renal type II Na/Pi cotransporter.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1909-14 PMID: 9465116
  8. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival.
    Mol Cell Biol. 2003 Oct;23(20):7315-28 PMID: 14517300
  9. Moving GLUT4: the biogenesis and trafficking of GLUT4 storage vesicles.
    Diabetes. 1997 Nov;46(11):1667-77 PMID: 9356011
  10. Ins (endocytosis) and outs (exocytosis) of GLUT4 trafficking.
    Curr Opin Cell Biol. 2007 Aug;19(4):466-73 PMID: 17644329
  11. Growth factors can influence cell growth and survival through effects on glucose metabolism.
    Mol Cell Biol. 2001 Sep;21(17):5899-912 PMID: 11486029
  12. The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics, and potential function of its novel members (review).
    Mol Membr Biol. 2001 Oct-Dec;18(4):247-56 PMID: 11780753
  13. Rab7 prevents growth factor-independent survival by inhibiting cell-autonomous nutrient transporter expression.
    Dev Cell. 2003 Oct;5(4):571-82 PMID: 14536059
  14. Proteasomal degradation of the nuclear targeting growth factor midkine.
    J Biol Chem. 2004 Apr 23;279(17):17785-91 PMID: 14970216
  15. Protein interactions with the glucose transporter binding protein GLUT1CBP that provide a link between GLUT1 and the cytoskeleton.
    Mol Biol Cell. 1999 Apr;10(4):819-32 PMID: 10198040
  16. In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability.
    Mol Cell. 2000 Sep;6(3):683-92 PMID: 11030347
  17. GIPC binds to the human lutropin receptor (hLHR) through an unusual PDZ domain binding motif, and it regulates the sorting of the internalized human choriogonadotropin and the density of cell surface hLHR.
    J Biol Chem. 2003 Dec 5;278(49):49348-57 PMID: 14507927
  18. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, blocks lysosomal cholesterol trafficking in macrophages.
    J Biol Chem. 1993 Dec 25;268(36):27345-8 PMID: 8262974
  19. Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding.
    Mol Cell. 2003 May;11(5):1389-96 PMID: 12769861
  20. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains.
    Science. 1997 Jan 3;275(5296):73-7 PMID: 8974395
  21. Interleukin-3-mediated cell survival signals include phosphatidylinositol 3-kinase-dependent translocation of the glucose transporter GLUT1 to the cell surface.
    J Biol Chem. 2003 Oct 10;278(41):39337-48 PMID: 12869574
  22. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor.
    Nature. 1999 Sep 16;401(6750):286-90 PMID: 10499588
  23. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase.
    Genes Dev. 2001 Jun 1;15(11):1406-18 PMID: 11390360
  24. Regulation of T lymphocyte metabolism.
    J Immunol. 2004 Apr 15;172(8):4661-5 PMID: 15067038
  25. IL-7 enhances the survival and maintains the size of naive T cells.
    J Immunol. 2001 Dec 15;167(12):6869-76 PMID: 11739504
  26. Glycogen synthase kinase 3alpha and 3beta mediate a glucose-sensitive antiapoptotic signaling pathway to stabilize Mcl-1.
    Mol Cell Biol. 2007 Jun;27(12):4328-39 PMID: 17371841
  27. Identification of the carboxy terminus as important for the isoform-specific subcellular targeting of glucose transporter proteins.
    J Cell Biol. 1993 Oct;123(1):137-47 PMID: 7691826
  28. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer.
    J Cell Physiol. 2005 Mar;202(3):654-62 PMID: 15389572
  29. Differential effects of rapamycin on mammalian target of rapamycin signaling functions in mammalian cells.
    Cancer Res. 2003 Dec 1;63(23):8451-60 PMID: 14679009
  30. Growth factor regulation of autophagy and cell survival in the absence of apoptosis.
    Cell. 2005 Jan 28;120(2):237-48 PMID: 15680329
  31. Rab7: a key to lysosome biogenesis.
    Mol Biol Cell. 2000 Feb;11(2):467-80 PMID: 10679007
  32. Akt and Bcl-xL promote growth factor-independent survival through distinct effects on mitochondrial physiology.
    J Biol Chem. 2001 Apr 13;276(15):12041-8 PMID: 11278698
  33. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking.
    Mol Biol Cell. 2007 Apr;18(4):1437-46 PMID: 17301289
  34. The sentrin-conjugating enzyme mUbc9 interacts with GLUT4 and GLUT1 glucose transporters and regulates transporter levels in skeletal muscle cells.
    Proc Natl Acad Sci U S A. 2000 Feb 1;97(3):1125-30 PMID: 10655495
  35. Distinct binding specificity of the multiple PDZ domains of INADL, a human protein with homology to INAD from Drosophila melanogaster.
    J Biol Chem. 2001 Nov 9;276(45):42122-30 PMID: 11509564
  36. Apoptosis is regulated by the rate of glucose transport in an interleukin 3 dependent cell line.
    J Exp Med. 1994 Sep 1;180(3):917-23 PMID: 8064240
  37. Binding of internalized receptors to the PDZ domain of GIPC/synectin recruits myosin VI to endocytic vesicles.
    Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12735-40 PMID: 16908842
  38. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments.
    Cell. 1990 Jul 27;62(2):317-29 PMID: 2115402
  39. Myo6 facilitates the translocation of endocytic vesicles from cell peripheries.
    Mol Biol Cell. 2003 Jul;14(7):2728-43 PMID: 12857860
  40. A novel mechanism for regulating transforming growth factor beta (TGF-beta) signaling. Functional modulation of type III TGF-beta receptor expression through interaction with the PDZ domain protein, GIPC.
    J Biol Chem. 2001 Oct 26;276(43):39608-17 PMID: 11546783
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
1470-8728
Published
2009-03-01
Pages
345-67
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC2637307
Subset
IM
Grants
NIAID NIH HHS · R01 AI063345 · United States
NIAID NIH HHS · R01 AI063345-04 · United States
NIAID NIH HHS · R01AI063345 · United States
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