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Heterotrimeric G Proteins and the Single-Transmembrane Domain IGF-II/M6P Receptor: Functional Interaction and Relevance to Cell Signaling

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Abstract

The G protein-coupled receptor (GPCR) family represents the largest and most versatile group of cell surface receptors. Classical GPCR signaling constitutes ligand binding to a seven-transmembrane domain receptor, receptor interaction with a heterotrimeric G protein, and the subsequent activation or inhibition of downstream intracellular effectors to mediate a cellular response. However, recent reports on direct, receptor-independent G protein activation, G protein-independent signaling by GPCRs, and signaling of nonheptahelical receptors via trimeric G proteins have highlighted the intrinsic complexities of G protein signaling mechanisms. The insulin-like growth factor-II/mannose-6 phosphate (IGF-II/M6P) receptor is a single-transmembrane glycoprotein whose principal function is the intracellular transport of lysosomal enzymes. In addition, the receptor also mediates some biological effects in response to IGF-II binding in both neuronal and nonneuronal systems. Multidisciplinary efforts to elucidate the intracellular signaling pathways that underlie these effects have generated data to suggest that the IGF-II/M6P receptor might mediate transmembrane signaling via a G protein-coupled mechanism. The purpose of this review is to outline the characteristics of traditional and nontraditional GPCRs, to relate the IGF-II/M6P receptor’s structure with its role in G protein-coupled signaling and to summarize evidence gathered over the years regarding the putative signaling of the IGF-II/M6P receptor mediated by a G protein.

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References

  1. Oakley RH, Barak LS, Gagnon MG (2005) Real-time imaging of GPCR-mediated arrestin translocation as a strategy to evaluate receptor–protein interactions. In: George SR, O’Dowd BF (eds) G protein coupled receptor–protein interactions. Wiley, New Jersey, USA, pp 53–80

    Google Scholar 

  2. Landry Y, Niederhoffer N, Sick E, Gies JP (2006) Heptahelical and other G-protein-coupled receptors (GPCRs) signaling. Curr Med Chem 13:51–63

    PubMed  CAS  Google Scholar 

  3. Oldham WM, Hamm HE (2006) Structural basis of function in heterotrimeric G proteins. Q Rev Biophys 39:117–166

    PubMed  CAS  Google Scholar 

  4. Gudermann T, Schoneberg T, Schultz G (1997) Functional and structural complexity of signal transduction via G-protein-coupled receptors. Annu Rev Neurosci 20:399–427

    PubMed  CAS  Google Scholar 

  5. Cabrera-Vera T, Vanhauwe J, Thomas TO, Medkova M, Preininger A, Mazzoni MR, Hamm HE (2003) Insights into G protein structure, function, and regulation. Endocr Rev 24:765–781

    PubMed  CAS  Google Scholar 

  6. Esbenshade TA (2006) G protein-coupled receptors as targets for drug discovery, in G protein–coupled receptors in drug discovery. In: Lundstrom KH, Chiu ML (eds) Taylor and Francis Group, LLC, Florida, USA, pp 15–36

    Google Scholar 

  7. Offermanns S (2003) G-proteins as transducers in transmembrane signalling. Prog Biophys Mol Biol 83:101–130

    PubMed  CAS  Google Scholar 

  8. Robishaw JW, Berlot CH (2004) Translating G protein subunit diversity into functional specificity. Curr Opin Cell Biol 16:206–209

    PubMed  CAS  Google Scholar 

  9. Levitzki A, Klein S (2002) G-protein subunit dissociation is not an integral part of G-protein action. ChemBioChem 3:815–818

    PubMed  CAS  Google Scholar 

  10. Simon MI, Strathmann MP, Gautam N (1991) Diversity of G proteins in signal transduction. Science 252:802–808

    PubMed  CAS  Google Scholar 

  11. Hamm HE (1998) The many faces of G protein signaling. J Biol Chem 273:669–672

    PubMed  CAS  Google Scholar 

  12. Suzuki N, Nakamura S, Mano H, Kozasa T (2003) Gα12 activates RhoGTPase through tyrosine-phosphorylated leukemia-associated RhoGEF. Proc Natl Acad Sci USA 100:733–738

    PubMed  CAS  Google Scholar 

  13. Warrior U, Gopalakrishnan S, Vanhauwe J, Burns D (2006) High throughput screening assays for G protein-coupled receptors, in G protein-coupled receptors in drug discovery. In: Lundstrom KH, Chiu ML (eds) Taylor and Francis Group, LLC, Florida, USA, pp 159–189

  14. Hollmann MW, Strumper D, Herroeder S, Durieux ME (2005) Receptors, G proteins, and their interactions. Anesthesiology 103:1066–1078

    PubMed  Google Scholar 

  15. Hur EM, Kim KT (2002) G protein-coupled receptor signalling and cross-talk: achieving rapidity and specificity. Cell Signal 14:397–405

    PubMed  CAS  Google Scholar 

  16. Strange PG (1988) The use of radiochemicals for studying receptors. Crit Rep Appl Chem 24:56–93

    CAS  Google Scholar 

  17. Ramsay D, Milligan G (2005) Analysis of receptor–receptor interactions using time-resolved fluorescence resonance energy transfer. In: George SR, O’Dowd BF (eds) G protein coupled receptor–protein interactions. Wiley, New Jersey, USA, pp 19–36

    Google Scholar 

  18. Sim LJ, Selley DE, Childers SR (1997) Autoradiographic visualization in brain of receptor–G protein coupling using [35S]GTPγS binding. Methods Mol Biol 83:117–132

    PubMed  CAS  Google Scholar 

  19. Sovago J, Dupuis DS, Gulyas B, Hall H (2001) An overview on functional receptor autoradiography using [35S]GTPγS. Brain Res Rev 38:149–164

    PubMed  CAS  Google Scholar 

  20. Harrison C, Traynor JR (2003) The [35S]GTPgammaS binding assay: approaches and applications in pharmacology. Life Sci 74:489–508

    PubMed  CAS  Google Scholar 

  21. Frang H, Mukkala VM, Syysto R, Illikka P, Hurskainen P, Scheinin M, Hemmila I (2003) Nonradioactive GTP binding assay to monitor activation of G protein-coupled receptors. Assay Drug Dev Technol 1:261–273

    Google Scholar 

  22. Kalatskaya I, Schüssler S, Blaukat A, Müller-Ester W, Jochum M, Proud D, Faussner A (2004) Mutation of tyrosine in the conserved NPXXY sequence leads to constitutive phosphorylation and internalization, but not signaling, of the human B2 bradykinin receptor. J Biol Chem 30:31268–31276

    Google Scholar 

  23. Hall RA (2005) Co-immunoprecipitation as a strategy to evaluate receptor–receptor or receptor–protein interactions. In: George SR, O’Dowd BF (eds) G protein coupled receptor–protein interactions. Wiley, New Jersey, USA, pp 165–178

    Google Scholar 

  24. Chakrabarti S, Regec A, Gintzler AR (2005) Biochemical demonstration of mu-opioid receptor association with Gsα: enhancement following morphine exposure. Mol Brain Res 135:217–224

    PubMed  CAS  Google Scholar 

  25. Mathis G (1995) Probing molecular interactions with homogenous techniques based on rare earth cryptates and fluorescence energy transfer. Clin Chem 41:1391–1397

    PubMed  CAS  Google Scholar 

  26. Bazin H, Trinquet E, Mathis G (2002) Time resolved amplification of cryptate emission: a versatile technology to trace biomolecular interactions. J Biotechnol 82:233–250

    PubMed  CAS  Google Scholar 

  27. Bertrand L, Parent S, Caron M, Legault M, Joly E, Angers S, Bouvier M, Brown M, Michael NP, Milligan G, Game S (2002) The BRET2/arrestin assay in stable recombinant cells: a platform to screen for compounds that interact with G protein-coupled receptors (GPCRs). J Recept Signal Transduct Res 22:533–541

    PubMed  CAS  Google Scholar 

  28. van Rijn RM, Chazot PL, Shenton FC, Sansuk F, Bakker RA, Leurs R (2006) Oligomerization of recombinant and endogenously expressed human histamine H4 receptors. Mol Pharmacol 70:604–615

    PubMed  Google Scholar 

  29. Violin JD, Ren XR, Lefkowitz RJ (2006) G-protein-coupled receptor kinase specificity for beta-arrestin recruitment to the beta2-adrenergic receptor revealed by fluorescence resonance energy transfer. J Biol Chem 281:20577–20588

    PubMed  CAS  Google Scholar 

  30. Bulenger S, Marullo S, Bouvier M (2005) Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol Sci 26:131–137

    PubMed  CAS  Google Scholar 

  31. Janetopoulos C, Jin T, Devreotes P (2001) Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science 291:2408–2411

    PubMed  CAS  Google Scholar 

  32. Pfleger KDG, Eidne KA (2005) Monitoring the formation of dynamic G-protein-coupled receptor–protein complexes in living cells. Biochem J 385:625–637

    PubMed  CAS  Google Scholar 

  33. Hoffmann C, Gaietta G, Bunemann M, Adams SR, Oberdorff-Maass S, Behr B, Vilardaga J-P, Tsien RY, Ellisman MH, Lohse M (2005) A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells. Nat Methods 2:171–176

    PubMed  CAS  Google Scholar 

  34. Kariv II, Stevens ME, Beherns DL, Oldenburg KR (1999) High throughput quantitation of cAMP production mediated by activation of seven-transmembrane domain receptor. J Biomol Screen 4:27–32

    PubMed  CAS  Google Scholar 

  35. Naylor LH (1999) Reporter gene technology: the future looks bright. Biochem Pharmacol 5:749–757

    Google Scholar 

  36. Prystay L, Gagne A, Kasila P, Yeh LA, Banks P (2001) Homogeneous cell-based fluorescence polarization assay for the direct detection of cAMP. J Biomol Screen 6:75–82

    PubMed  CAS  Google Scholar 

  37. Golla R, Seethala R (2002) A homogenous enzyme fragment complementation cyclic AMP screen for GPCR agonists. J Biomol Screen 7:515–525

    PubMed  CAS  Google Scholar 

  38. Gabriel D, Vernier M, Pfiefer MJ, Dasen B, Tenaillon L, Bouhelal R (2003) High throughput screening technologies for direct cyclic AMP measurement. Assay Drug Dev Technol 1:291–303

    PubMed  CAS  Google Scholar 

  39. Liu B, Wu D (2004) Analysis of the coupling of G12/13 to G protein-coupled receptors using a luciferase reporter assay. Methods Mol Biol 237:145–149

    PubMed  CAS  Google Scholar 

  40. Sturino CF, Lachance N, Boyd M, Berthelette C, Labelle M, Li L, Roy B, Scheigetz J, Tsou N, Brideau C, Cauchon E, Carriere MC, Denis D, Greig G, Kargman S, Lamontagne S, Mathieu MC, Sawyer N, Slipetz D, O’Neill G, Wang Z, Zamboni R, Metters KM, Young RN (2006) Identification of an indole series of prostaglandin D2 receptor antagonists. Bioorg Med Chem Lett 16:3043–3048

    PubMed  CAS  Google Scholar 

  41. Chen WJ, Jayawickreme C, Watson C, Wolfe L, Holmes W, Ferris R, Armour S, Dallas W, Chen G, Boone L, Luther M, Kenakin T (1998) Recombinant human CXC-chemokine receptor-4 in melanophores are linked to Gi protein: seven transmembrane coreceptors for human immunodeficiency virus entry into cells. Mol Pharmacol 53:177–181

    PubMed  CAS  Google Scholar 

  42. Niebauer RT, Gao ZG, Li B, Wess J, Jacobson KA (2005) Signaling of the Human P2Y(1) Receptor measured by a yeast growth assay with comparisons to assays of phospholipase C and calcium mobilization in 1321N1 human astrocytoma cells. Purinergic Signal 1:241–247

    PubMed  CAS  Google Scholar 

  43. Christiansen B, Wellendorph P, Brauner-Osborne H (2006) Known regulators of nitric oxide synthase and arginase are agonists at the human G-protein-coupled receptor GPRC6A. Br J Pharmacol 147:855–863

    PubMed  CAS  Google Scholar 

  44. Patel TB (2004) Single transmembrane spanning heterotrimeric g protein-coupled receptors and their signaling cascades. Pharmacol Rev 56:371–385

    PubMed  CAS  Google Scholar 

  45. Cismowski MJ (2006) Non-receptor activators of heterotrimeric G-protein signaling (AGS proteins). Semin Cell Dev Biol 17:334–344

    PubMed  CAS  Google Scholar 

  46. Blumer JB, Cismowski MJ, Sato M, Lanier SM (2005) AGS proteins: receptor-independent activators of G-protein signaling. Trends Pharmacol Sci 26:470–476

    PubMed  CAS  Google Scholar 

  47. Sato M, Blumer JB, Simon V, Lanier SM (2006) Accessory proteins for G proteins: partners in signaling. Annu Rev Pharmacol Toxicol 46:151–187

    PubMed  CAS  Google Scholar 

  48. Shah BH, Catt KJ (2004) GPCR-mediated transactivation of RTKs in the CNS: mechanisms and consequences. Trends Neurosci 27:48–53

    PubMed  CAS  Google Scholar 

  49. Gavi S, Shumay E, Wang HY, Malbon CC (2006) G-protein-coupled receptors and tyrosine kinases: crossroads in cell signaling and regulation. Trends Endocrinol Metab 17:48–54

    PubMed  Google Scholar 

  50. Kornfeld S (1992) Structure and function of the mannose 6-phosphate/insulin-like growth factor II receptors. Annu Rev Biochem 61:307–330

    PubMed  CAS  Google Scholar 

  51. Dahms NM, Hancock MK (2002) P-type lectins. Biochim Biophys Acta 1572:317–340

    PubMed  CAS  Google Scholar 

  52. Braulke T (1999) Type-2 IGF receptor: a multiple-ligand binding protein. Horm Metab Res 31:242–246

    Article  PubMed  CAS  Google Scholar 

  53. Hille-Rehfeld A (1995) Mannose 6-phosphate receptors in sorting and transport of lysosomal enzymes. Biochim Biophys Acta 1241:177–194

    PubMed  Google Scholar 

  54. Hawkes C, Kar S (2004) The insulin-like growth factor-II/mannose-6-phosphate receptor: structure, distribution and function in the central nervous system. Brain Res Rev 44:117–140

    PubMed  CAS  Google Scholar 

  55. Dennis PA, Rifkin DB (1991) Cellular activation of latent transforming growth factor beta requires binding to the cation-independent mannose 6-phosphate/insulin-like growth factor type II receptor. Proc Natl Acad Sci USA 88:580–584

    PubMed  CAS  Google Scholar 

  56. Blanchard F, Duplomb L, Raher S, Vusio P, Hoflack B, Jacques Y, Godard A (1999) Mannose 6-phosphate/insulin-like growth factor II receptor mediates internalization and degradation of leukemia inhibitory factor but not signal transduction. J Biol Chem 274:24685–24693

    PubMed  CAS  Google Scholar 

  57. Lee S-J, Nathans D (1988) Proliferin secreted by cultured cells binds to mannose-6-phosphate receptors. J Biol Chem 263:3521–3527

    PubMed  CAS  Google Scholar 

  58. Scheel G, Herzog V (1989) Mannose 6-phosphate receptor in porcine thyroid follicle cells. Localization and possible implications for the intracellular transport of thyroglobulin. Eur J Cell Biol 49:140–148

    PubMed  CAS  Google Scholar 

  59. Puolakkainen M, Kuo C-C, Campbell LA (2005) Chlamydia pneumoniae uses the mannose 6-phosphate/insulin-like growth factor 2 receptor for infection of endothelial cells. Infect Immun 73:4620–4625

    PubMed  CAS  Google Scholar 

  60. Gasanov U, Koina C, Beagley KW, Aitken RJ, Hansbro PM (2006) Identification of the insulin-like growth factor II receptor as a novel receptor for binding and invasion by Listeria monocytogenes. Infect Immun 74:566–577

    PubMed  CAS  Google Scholar 

  61. Kang JX, Li Y, Leaf A (1997) Mannose-6-phosphate/insulin-like growth factor-II receptor is a receptor for retinoic acid. Proc Natl Acad Sci USA 94:13671–13676

    PubMed  CAS  Google Scholar 

  62. Morgan DO, Edman JC, Standring DN, Fried VA, Smith MC, Roth RA, Rutter WJ (1987) Insulin-like growth factor II receptor as a multifunctional binding protein. Nature 329:301–307

    PubMed  CAS  Google Scholar 

  63. Oshima A, Nolan CM, Kyle JW, Grubb JH, Sly WS (1988) The human cation-independent mannose 6-phosphate receptor. Cloning and sequence of the full-length cDNA and expression of functional receptor in COS cells. J Biol Chem 263:2553–2562

    PubMed  CAS  Google Scholar 

  64. Byrd JC, Park JH, Schaffer BS, Garmroudi F, MacDonald RG (2000) Dimerization of the insulin-like growth factor II/mannose 6-phosphate receptor. J Biol Chem 275:18647–18656

    PubMed  CAS  Google Scholar 

  65. Hassan AB (2003) Keys to the hidden treasures of the mannose 6-phosphate/insulin-like growth factor 2 receptor. Am J Pathol 162:3–6

    PubMed  CAS  Google Scholar 

  66. York SJ, Arneson LS, Gregory WT, Dahms NM, Kornfeld S (1999) The rate of internalization of the mannose 6-phosphate/insulin-like growth factor II receptor is enhanced by multivalent ligand binding. J Biol Chem 274:1164–1171

    PubMed  CAS  Google Scholar 

  67. Costello M, Baxter RC, Scott CD (1999) Regulation of soluble insulin-like growth factor II/mannose 6-phosphate receptor in human serum: measurement by enzyme-linked immunosorbent assay. J Clin Endocrinol Metab 84:611–617

    PubMed  CAS  Google Scholar 

  68. Kiess W, Greenstein LA, White RM, Lee L, Rechler MM, Nissley SP (1987) Type II insulin-like growth factor receptor is present in rat serum. Proc Natl Acad Sci USA 84:7720–7724

    PubMed  CAS  Google Scholar 

  69. MacDonald RG, Tepper MA, Clairmont KB, Perregaux SB, Czech MP (1989) Serum form of the rat insulin-like growth factor II/mannose 6-phosphate receptor is truncated in the carboxy-terminal domain. J Biol Chem 264:3256–3261

    PubMed  CAS  Google Scholar 

  70. Valenzano KJ, Remmler J, Lobel P (1995) Soluble insulin-like growth factor II/mannose 6-phosphate receptor carries multiple high molecular weight forms of insulin-like growth factor II in fetal bovine serum. J Biol Chem 270:16441–16448

    PubMed  CAS  Google Scholar 

  71. Clairmont KB, Czech MP (1991) Extracellular release as the major degradative pathway of the insulin-like growth factor II/mannose 6-phosphate receptor. J Biol Chem 266:12131–12134

    PubMed  CAS  Google Scholar 

  72. Zaina S, Squire S (1998) The soluble type 2 insulin-like growth factor (IGF-II) receptor reduces organ size by IGF-II-mediated and IGF-II-independent mechanisms. J Biol Chem 273:28610–28616

    PubMed  CAS  Google Scholar 

  73. Scott CD, Weiss J (2000) Soluble insulin-like growth factor II/mannose 6-phosphate receptor inhibits DNA synthesis in insulin-like growth factor II sensitive cells. J Cell Physiol 182:62–68

    PubMed  CAS  Google Scholar 

  74. Harper J, Burns JL, Foulstone EJ, Pignatelli M, Zaina S, Hassan AB (2006) Soluble IGF2 receptor rescues Apc Min/+ intestinal adenoma progression induced by Igf2 loss of imprinting. Cancer Res 66:1940–1948

    PubMed  CAS  Google Scholar 

  75. Reddy ST, Chai W, Childs RA, Page JD, Feizi T, Dahms NM (2004) Identification of a low affinity mannose-6-phosphate-binding site in domain 5 or the cation-independent mannose-6-phosphate receptor. J Biol Chem 279:38658–38667

    PubMed  CAS  Google Scholar 

  76. Dahms NM, Wick DA, Brzycki-Wessell MA (1994) The bovine mannose 6-phosphate/insulin-like growth factor II receptor. Localization of the insulin-like growth factor II binding site to domains 5-11. J Biol Chem 269:3802–3809

    PubMed  CAS  Google Scholar 

  77. Schmidt B, Kiecke-Siemsen C, Waheed A, Braulke T, von Figura K (1995) Localization of the insulin-like growth factor II binding site to amino acids 1508-1566 in repeat 11 of the mannose 6-phosphate/insulin-like growth factor II receptor. J Biol Chem 270:14975–14982

    PubMed  CAS  Google Scholar 

  78. Garmroudi F, Devi G, Slentz DH, Schaffer BS, MacDonald RG (1996) Truncated forms of the insulin-like growth factor II (IGF-II)/mannose 6-phosphate receptor encompassing the IGF-II binding site: characterization of a point mutation that abolishes IGF-II binding. Mol Endocrinol 10:642–651

    PubMed  CAS  Google Scholar 

  79. Devi GR, Byrd JC, Slentz DH, MacDonald RG (1998) An insulin-like growth factor II (IGF-II) affinity-enhancing domain localized within extracytoplasmic repeat 13 of the IGF-II/mannose 6-phosphate receptor. Mol Endocrinol 12:1661–1672

    PubMed  CAS  Google Scholar 

  80. Linnell J, Groeger G, Hassan AB (2001) Real time kinetics of insulin-like growth factor II (IGF-II) interaction with the IGF-II/mannose 6-phosphate receptor. The effects of domain 13 and pH. J Biol Chem 276:23986–23991

    PubMed  CAS  Google Scholar 

  81. Brown J, Esnouf RM, Jones MA, Linnell J, Harlos K, Hassan AB, Jones EY (2002) Structure of a functional IGF2R fragment determined from the anomalous scattering of sulfur. EMBO J 21:1054–1062

    PubMed  CAS  Google Scholar 

  82. Polychronakos C, Guyda HJ, Posner BI (1988) Mannose 6-phosphate increases the affinity of its cation-independent receptor for insulin-like growth factor II by displacing inhibitory endogenous ligands. Biochem Biophys Res Commun 157:632–638

    PubMed  CAS  Google Scholar 

  83. Waheed A, Braulke T, Junghans U, von Figura K (1988) Mannose 6-phosphate/insulin like growth factor II receptor: the two types of ligands bind simultaneously to one receptor at different sites. Biochem Biophys Res Commun 152:1248–1254

    PubMed  CAS  Google Scholar 

  84. MacDonald RG (1991) Mannose-6-phosphate enhances cross-linking efficiency between insulin-like growth factor-II (IGF-II) and IGF-II/mannose-6-phosphate receptors in membranes. Endocrinology 128:413–421

    PubMed  CAS  Google Scholar 

  85. Nissley P, Kiess W (1991) Reciprocal modulation of binding of lysosomal enzymes and insulin-like growth factor-II (IGF-II) to the mannose 6-phosphate/IGF-II receptor. Adv Exp Med Biol 293:311–324

    PubMed  CAS  Google Scholar 

  86. Sara V, Carlsson-Skwirut C (1988) The role of insulin-like growth factors in the regulation of brain development. Prog Brain Res 73:87–99

    PubMed  CAS  Google Scholar 

  87. Senior P, Bryne S, Brammar W, Beck F (1990) Expression of the IGF-II/mannose-6-phosphate receptor mRNA and protein in the developing rat. Development 109:67–75

    PubMed  CAS  Google Scholar 

  88. Valentino KL, Pham H, Ocrant I, Rosenfeld RG (1988) Distribution of insulin-like growth factor II receptor immunoreactivity in rat tissues. Endocrinology 122:2753–2763

    Article  PubMed  CAS  Google Scholar 

  89. Kar S, Chabot J-G, Quirion R (1993) Quantitative autoradiographic localization of [125I]insulin-like growth factor I, [125I]insulin-like growth factor II and [125I]insulin receptor binding sites in developing and adult rat brain. J Comp Neurol 333:375–397

    PubMed  CAS  Google Scholar 

  90. Nissley P, Kiess W, Sklar M (1993) Developmental expression of the IGF-II/mannose 6-phosphate receptor. Mol Reprod Dev 35:408–413

    PubMed  CAS  Google Scholar 

  91. de Pablo F, de la Rosa EJ (1995) The developing CNS: a scenario for the action of proinsulin, insulin and insulin-like growth factors. Trends Neurosci 18:143–150

    PubMed  Google Scholar 

  92. Sklar MM, Kiess W, Thomas C, Nissley SP (1989) Developmental expression of the tissue insulin-like growth factor-II/mannose 6-phosphate receptor in the rat. Measurement by quantitative immunoblotting. J Biol Chem 264:16733–16738

    PubMed  CAS  Google Scholar 

  93. Funk B, Kessler U, Eisenmenger W, Hansmann A, Kolb HJ, Kiess W (1992) Expression of the insulin-like growth factor-II/mannose-6-phosphate receptor in multiple human tissues during fetal life and early infancy. J Clin Endocrinol Metab 75:424–431

    PubMed  CAS  Google Scholar 

  94. Pfuender M, Sauerwein H, Funk B, Kessler U, Barenton B, Schwarz HP, Hoeflich A, Kiess W (1995) The insulin-like growth factor-II/mannose-6-phosphate receptor is present in fetal bovine tissues throughout gestation. Domest Anim Endocrinol 12:317–324

    PubMed  CAS  Google Scholar 

  95. Hill JM, Lesniak MA, Kiess W, Nissley SP (1988) Radioimmunohistochemical localization of type II IGF receptors in rat brain. Peptides 9(suppl):181–187

    PubMed  Google Scholar 

  96. Lesniak M, Hill J, Kiess W, Rojeski M, Pert C, Roth J (1988) Receptors for insulin-like growth factors I and II: autoradiographic localization in rat brain and comparison to receptors for insulin. Endocrinology 123:2089–2099

    PubMed  CAS  Google Scholar 

  97. Smith M, Clemens J, Kerchner G, Mendelsohn L (1988) The insulin-like growth factor-II (IGF-II) receptor of rat brain: regional distribution visualized by autoradiography. Brain Res 445:241–246

    PubMed  CAS  Google Scholar 

  98. Marinelli PW, Gianoulakis C, Kar S (2000) Effects of voluntary ethanol drinking on [125I]insulin-like growth factor-I, [125I]insulin-like growth factor-II and [125I]insulin receptor binding in the mouse hippocampus and cerebellum. Neuroscience 98:687–695

    PubMed  CAS  Google Scholar 

  99. Wilczak N, De Bleser P, Luiten P, Geerts A, Teelken A, De Keyser J (2000) Insulin-like growth factor II receptors in human brain and their absence in astrogliotic plaques in multiple sclerosis. Brain Res 863:282–288

    PubMed  CAS  Google Scholar 

  100. Hawkes C, Kar S (2003) Insulin-like growth factor-II/mannose-6-phosphate receptor: widespread distribution in neurons of the central nervous system including those expressing cholinergic phenotype. J Comp Neurol 458:113–127

    PubMed  CAS  Google Scholar 

  101. Konishi Y, Fushimi S, Shirabe T (2005) Immunohistochemical distribution of cation-dependent mannose 6-phosphate receptors in the mouse central nervous system: comparison with that of cation-independent mannose 6-phosphate receptors. Neurosci Lett 378:7–12

    PubMed  CAS  Google Scholar 

  102. Lee WH, Clemens JA, Bondy CA (1992) Insulin-like growth factors in response to cerebral ischemia. Mol Cell Neurosci 3:36–43

    CAS  Google Scholar 

  103. Stephenson D, Rash K, Clemens J (1995) Increase in insulin-like growth factor II receptor within ischemic neurons following cerebral infarction. J Cereb Blood Flow Metab 15:1022–1031

    PubMed  CAS  Google Scholar 

  104. Kar S, Baccichet A, Quirion R, Poirier J (1993) Entorhinal cortex lesion induces differential responses in [125I]insulin-like growth factor I, [125I]insulin-like growth factor II and [125I]insulin receptor binding sites in the rat hippocampal formation. Neuroscience 55:69–80

    PubMed  CAS  Google Scholar 

  105. Breese CR, D’costa A, Rollins YD, Adams C, Booze RM, Sonntag WE, Leonard S (1996) Expression of insulin-like growth factor-1 (IGF-1) and IGF-binding protein 2 (IGF-BP2) in the hippocampus following cytotoxic lesion of the dentate gyrus. J Comp Neurol 369:388–404

    PubMed  CAS  Google Scholar 

  106. Kar S, Seto D, Dore S, Chabot J-G, Quirion R (1997) Systemic administration of kainic acid induces selective time dependent decrease in [125I]insulin-like growth factor I, [125I]insulin-like growth factor II and [125I]insulin receptor binding sites in adult rat hippocampal formation. Neuroscience 80:1041–1055

    PubMed  CAS  Google Scholar 

  107. Boker C, von Figura K, Hille-Rehfeld A (1997) The carboxy-terminal peptides of 46 kDa and 300 kDa mannose 6-phosphate receptors share partial sequence homology and contain information for sorting in the early endosomal pathway. J Cell Sci 110:1023–1032

    PubMed  Google Scholar 

  108. Ghosh P, Dahms NM, Kornfeld S (2003) Mannose 6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol 4:202–212

    PubMed  CAS  Google Scholar 

  109. Johnson KF, Kornfeld S (1992) A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J Biol Chem 267:17110–17115

    PubMed  CAS  Google Scholar 

  110. Lobel P, Fujimoto K, Ye RD, Griffiths G, Kornfeld S (1989) Mutations in the cytoplasmic domain of the 275 kd mannose 6-phosphate receptor differentially alter lysosomal enzyme sorting and endocytosis. Cell 57:787–796

    PubMed  CAS  Google Scholar 

  111. Le Borgne R, Hoflack B (1998) Protein transport from the secretory to the endocytic pathway in mammalian cells. Biochem Biophys Acta 1404:195–209

    PubMed  Google Scholar 

  112. Dell’Angelica EC, Payne GS (2001) Intracellular cycling of lysosomal enzyme receptors. Cytoplasmic tails’ tales. Cell 106:395–398

    PubMed  CAS  Google Scholar 

  113. Mullins C, Bonifacino JS (2001) The molecular machinery for lysosome biogenesis. BioEssays 23:333–343

    PubMed  CAS  Google Scholar 

  114. Boman AL, Zhang C, Zhu X, Kahn RA (2000) A family of ADP-ribosylation factor effectors that can alter membrane transport through the trans-Golgi. Mol Biol Cell 11:1241–1255

    PubMed  CAS  Google Scholar 

  115. Dell’Angelica EC, Puertollano R, Mullins C, Aguilar RC, Vargas JD, Hartnell LM, Bonifacino JS (2000) GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J Cell Biol 149:81–94

    PubMed  CAS  Google Scholar 

  116. Hirst J, Lindsay MR, Robinson MS (2001) GGAs: roles of the different domains and comparison with AP-1 and clathrin. Mol Biol Cell 12:3573–3588

    PubMed  CAS  Google Scholar 

  117. Puertollano R, Aguilar RC, Gorshkova I, Crouch RJ, Bonifacino JS (2001) Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292:1712–1716

    PubMed  CAS  Google Scholar 

  118. Takatsu H, Katoh Y, Shiba Y, Nakayama K (2001) Golgi-localizing, gamma-adaptin ear homology domain, ADP-ribosylation factor-binding (GGA) proteins interact with acidic dileucine sequences within the cytoplasmic domains of sorting receptors through their Vps27p/Hrs/STAM (VHS) domains. J Biol Chem 276:28541–28545

    PubMed  CAS  Google Scholar 

  119. Zhu Y, Doray B, Poussu A, Lehto VP, Kornfeld S (2001) Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6-phosphate receptor. Science 292:1716–1718

    PubMed  CAS  Google Scholar 

  120. Ghahary A, Tredget EE, Mi L, Yang L (1999) Cellular response to latent TGF-beta1 is facilitated by insulin-like growth factor-II/mannose-6-phosphate receptors on MS-9 cells. Exp Cell Res 251:111–120

    PubMed  CAS  Google Scholar 

  121. Villevalois-Cam L, Rescan C, Gilot D, Ezan F, Loyer P, Desbuquois B, Guguen-Guillouzo C, Baffet G (2003) The hepatocyte is a direct target for transforming-growth factor beta activation via the insulin-like growth factor II/mannose 6-phosphate receptor. J Hepatol 38:156–163

    PubMed  CAS  Google Scholar 

  122. Godar S, Horejsi V, Weidle UH, Binder BR, Hansmann C, Stockinger H (1999) M6P/IGFII-receptor complexes urokinase receptor and plasminogen for activation of transforming growth factor-beta1. Eur J Immunol 29:1004–1013

    PubMed  CAS  Google Scholar 

  123. Ludwig T, Eggenschwiler J, Fisher P, D’Ercole AJ, Davenport ML, Efstratiadis A (1996) Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol 177:517–535

    PubMed  CAS  Google Scholar 

  124. D’Ercole AJ, Ye P, O’Kusky JR (2002) Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 36:209–220

    PubMed  CAS  Google Scholar 

  125. Souza RF, Wang S, Thakar M, Smolinski KN, Yin J, Zou T-T, Kong D, Abraham JM, Toretsky JA, Meltzer SJ (1999) Expression of the wild-type insulin-like growth factor II receptor gene suppresses growth and causes cell death in colorectal carcinoma cells. Oncogene 18:4063–4068

    PubMed  CAS  Google Scholar 

  126. O’Gorman DB, Weiss J, Hettiaratchi A, Firth SM, Scott CD (2002) Insulin-like growth factor-II/mannose 6-phosphate receptor overexpression reduces growth of choriocarcinoma cells in vitro and in vivo. Endocrinology 143:4287–4294

    PubMed  CAS  Google Scholar 

  127. Schaffer BS, Lin M-F, Byrd JC, Park JHY, MacDonald RG (2003) Opposing roles for the insulin-like growth factor (IGF)-II and mannose 6-phosphate (Man-6-P) binding activities of the IGF-II/Man-6-P receptor in the growth of prostate cancer cells. Endocrinology 144:955–966

    PubMed  CAS  Google Scholar 

  128. O’Gorman DB, Costello M, Weiss J, Firth SM, Scott CD (1999) Decreased insulin-like growth factor-II/mannose 6-phosphate receptor expression enhances tumorigenicity in JEG-3 cells. Cancer Res 59:5692–5694

    PubMed  CAS  Google Scholar 

  129. Chen Z, Ge Y, Landman N, Kang JX (2002) Decreased expression of the mannose 6-phosphate/insulin-like growth factor-II receptor promotes growth of human breast cancer cells. BMC Cancer 2:18

    PubMed  Google Scholar 

  130. Chen Z, Ge Y, Kang JX (2004) Down-regulation of the M6P/IGF-II receptor increases cell proliferation and reduces apoptosis in neonatal rat cardiac myocytes. BMC Cell Biol 5:15

    PubMed  Google Scholar 

  131. Osipo C, Dorman S, Frankfater A (2001) Loss of insulin-like growth factor II receptor expression promotes growth in cancer by increasing intracellular signaling from both IGF-I and insulin receptors. Exp Cell Res 264:388–396

    PubMed  CAS  Google Scholar 

  132. Li J, Sahagian GG (2004) Demonstration of tumor suppression by mannose 6-phosphate/insulin-like growth factor 2 receptor. Oncogene 23:9359–9368

    PubMed  CAS  Google Scholar 

  133. Shimizu M, Webster C, Morgan D, Blau H, Roth R (1986) Insulin and insulin-like growth factor receptors and responses in cultured human muscle cells. Am J Physiol 215:E611–E615

    Google Scholar 

  134. Hari J, Pierce S, Morgan D, Sara V, Smith M, Roth R (1987) The receptor for insulin-like growth factor-II mediates an insulin-like response. EMBO J 6:3367–3371

    PubMed  CAS  Google Scholar 

  135. Zhang Q, Tally M, Larsson O, Kennedy R, Huang L, Hall K, Berggren P-O (1997) Insulin-like growth factor-II signaling through the insulin-like growth factor-II/mannose 6-phosphate receptor promotes exocytosis of insulin-secreting cells. Proc Natl Acad Sci USA 94:6232–6236

    PubMed  CAS  Google Scholar 

  136. Tally M, Li CH, Hall K (1987) IGF-2 stimulated growth mediated by the somatomedin type 2 receptor. Biochem Biophys Res Commun 148:811–816

    PubMed  CAS  Google Scholar 

  137. Tsuruta JK, Eddy EM, O’Brien DA (2000) Insulin-like growth factor-II/cation-independent mannose 6-phosphate receptor mediates paracrine interactions during spermatogonial development. Biol Reprod 63:1006–1013

    PubMed  CAS  Google Scholar 

  138. Minniti CP, Kohn EC, Grubb JH, Sly WS, Oh Y, Muller HL, Rosenfeld RG, Helman LJ (1992) The insulin-like growth factor II (IGF-II)/mannose 6-phosphate receptor mediates IGF-II-induced motility in human rhabdomyosarcoma cells. J Biol Chem 267:9000–9004

    PubMed  CAS  Google Scholar 

  139. McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK (2001) Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J Clin Endocrinol Metab 86:3665–3674

    PubMed  CAS  Google Scholar 

  140. Roff CF, Wozniak RW, Blenis J, Wang JL (1983) The effect of mannose 6-phosphate on the turnover of cell surface glycosaminoglycans. Exp Cell Res 144:333–344

    PubMed  CAS  Google Scholar 

  141. Kojima I, Nishimoto I, Iiri T, Ogata E, Rosenfeld RG (1988) Evidence that type II insulin-like growth factor receptor is coupled to calcium gating system. Biochem Biophys Res Commun 154:9–19

    PubMed  CAS  Google Scholar 

  142. Matsunaga H, Nishimoto I, Kojima I, Yamashita N, Kurokawa K, Ogata E (1988) Activation of a calcium-permeable cation channel by insulin-like growth factor-II in BALB/c 3T3 cells. Am J Physiol 255:C442–C446

    PubMed  CAS  Google Scholar 

  143. Sakano K, Enjoh T, Numata F, Fujiwara H, Marumoto Y, Higashihashi N, Sato Y, Perdue JF, Fujita-Yamaguchi Y (1991) The design, expression, and characterization of human insulin-like growth factor II (IGF-II) mutants specific for either the IGF-II/cation-independent mannose 6-phosphate receptor or IGF-I receptor. J Biol Chem 266:20626–20635

    PubMed  CAS  Google Scholar 

  144. Konishi T, Takahashi K, Chui D-H, Rosenfeld R, Himeno M, Tabira T (1994) Insulin-like growth factor II promotes in vitro cholinergic development of mouse septal neurons: comparison with the effects of insulin-like growth factor I. Brain Res 649:53–61

    PubMed  CAS  Google Scholar 

  145. Hawkes C, Jhamandas JH, Harris KH, Fu W, MacDonald RG, Kar S (2006) Single transmembrane domain insulin-like growth factor-II/mannose-6-phosphate receptor regulates central cholinergic function by activating a G-protein-sensitive, protein kinase C-dependent pathway. J Neurosci 26:585–596

    PubMed  CAS  Google Scholar 

  146. Morrione A, Valentinis B, Xu SQ, Yumet G, Louvi A, Efstratiadis A, Baserga R (1997) Insulin-like growth factor II stimulates cell proliferation through the insulin receptor. Proc Natl Acad Sci USA 94:3777–3782

    PubMed  CAS  Google Scholar 

  147. Zhang Q, Berggren PO, Tally M (1997) Glucose increases both the plasma membrane number and phosphorylation of insulin-like growth factor-II/mannose-6-phosphate receptors. J Biol Chem 272:23702–23706

    Google Scholar 

  148. Nishimoto I, Hata Y, Ogata E, Kojima I (1987) Insulin-like growth factor II stimulates calcium influx in competent BALB/c 3T3 cells primed with epidermal growth factor. Characteristics of calcium influx and involvement of GTP-binding protein. J Biol Chem 262:12120–12126

    PubMed  CAS  Google Scholar 

  149. Kojima I, Nishimoto I, Iiri T, Ogata E, Rosenfeld RG (1988) Evidence that type II insulin-like growth factor receptor is coupled to calcium gating system. Biochem Biophys Res Commun 154:9–19

    PubMed  CAS  Google Scholar 

  150. Nishimoto I, Murayama Y, Katada T, Ui M, Ogata E (1989) Possible direct linkage of insulin-like growth factor-II receptor with guanine nucleotide-binding proteins. J Biol Chem 264:14029–14038

    PubMed  CAS  Google Scholar 

  151. Murayama Y, Okamoto T, Ogata E, Asano T, Iiri T, Katada T, Ui M, Grubb JH, Sly WS, Nishimoto I (1990) Distinctive regulation of the functional linkage between the human cation-independent mannose 6-phosphate receptor and GTP-binding proteins by insulin-like growth factor II and mannose 6-phosphate. J Biol Chem 265:17456–17462

    PubMed  CAS  Google Scholar 

  152. Higashijima T, Burnier J, Ross EM (1990) Regulation of Gi and Go by mastoparan, related amphiphilic peptides and hydrophobic amines: mechanisms and structural determinants of activity. J Biol Chem 265:14176–14186

    PubMed  CAS  Google Scholar 

  153. Okamoto T, Katada T, Murayama Y, Ui M, Ogata E, Nishimoto I (1990) A simple structure encodes G protein-activating function of the IGF-II/mannose 6-phosphate receptor. Cell 62:709–717

    PubMed  CAS  Google Scholar 

  154. Okamoto T, Nishimoto I (1991) Analysis of stimulation-G protein subunit coupling by using active insulin-like growth factor II receptor peptide. Proc Natl Acad Sci USA 88:8020–8023

    PubMed  CAS  Google Scholar 

  155. Okamoto T, Ohkuni Y, Ogata E, Nishimoto I (1991) Distinct mode of G protein activation due to single residue substitution of active IGF-II receptor peptide Arg2410-Lys2423: evidence for stimulation acceptor region other than C-terminus of Gi alpha. Biochem Biophys Res Commun 179:10–16

    PubMed  CAS  Google Scholar 

  156. Nishimoto I (1993) The IGF-II receptor system: a G protein-linked mechanism. Mol Reprod Dev 35:398–406

    PubMed  CAS  Google Scholar 

  157. Ikezu T, Okamoto T, Giambarella U, Yokota T, Nishimoto I (1995) In vivo coupling of insulin-like growth factor II/mannose 6-phosphate receptor to heteromeric G proteins. Distinct roles of cytoplasmic domains and signal sequestration by the receptor. J Biol Chem 270:29224–29228

    PubMed  CAS  Google Scholar 

  158. Korner C, Nurnberg B, Uhde M, Braulke T (1995) Mannose 6-phosphate/insulin-like growth factor II receptor fails to interact with G-proteins, Analysis of mutant cytoplasmic receptor domains. J Biol Chem 270:287–295

    PubMed  CAS  Google Scholar 

  159. Pfeifer A, Nurnberg B, Kamm S, Uhde M, Schultz G, Ruth P, Hofmann F (1995) Cyclic GMP-dependent protein kinase blocks pertussis toxin-sensitive hormone receptor signaling pathways in Chinese hamster ovary cells. J Biol Chem 270:9052–9059

    PubMed  CAS  Google Scholar 

  160. Poiraudeau S, Lieberherr M, Kergosie N, Corvol MT (1997) Different mechanisms are involved in intracellular calcium increase by insulin-like growth factors 1 and 2 in articular chondrocytes: voltage-gated calcium channels, and/or phospholipase C coupled to a pertussis-sensitive G-protein. J Cell Biochem 64:414–422

    PubMed  CAS  Google Scholar 

  161. Groskopf JC, Syu LJ, Saltiel AR, Linzer DI (1997) Proliferin induces endothelial cell chemotaxis through a G protein-coupled, mitogen-activated protein kinase-dependent pathway. Endocrinology 138:2835–2840

    PubMed  CAS  Google Scholar 

  162. Walter HJ, Berry M, Hill DJ, Cwyfan-Hughes S, Holly JM, Logan A (1999) Distinct sites of insulin-like growth factor (IGF)-II expression and localization in lesioned rat brain: possible roles of IGF binding proteins (IGFBPs) in the mediation of IGF-II activity. Endocrinology 140:520–532

    PubMed  CAS  Google Scholar 

  163. Araujo DM, Lapchak PA, Collier B, Chabot JG, Quirion R (1989) Insulin-like growth factor-1 (somatomedin-C) receptors in the rat brain: distribution and interaction with the hippocampal cholinergic system. Brain Res 484:130–138

    PubMed  CAS  Google Scholar 

  164. Kar S, Seto D, Dore S, Hanisch U, Quirion R (1997) Insulin-like growth factors-I and -II differentially regulate endogenous acetylcholine release from the rat hippocampal formation. Proc Natl Acad Sci USA 94:14054–14059

    PubMed  CAS  Google Scholar 

  165. Seto D, Zheng WH, McNicoll A, Collier B, Quirion R, Kar S (2002) Insulin-like growth factor-I inhibits endogenous acetylcholine release from the rat hippocampal formation: possible involvement of GABA in mediating the effects. Neuroscience 115:603–612

    PubMed  CAS  Google Scholar 

  166. Rosenthal SM, Hsiao D, Silverman LA (1994) An insulin-like growth factor-II (IGF-II) analog with highly selective affinity for IGF-II receptors stimulates differentiation, but not IGF-I receptor down-regulation in muscle cells. Endocrinology 135:38–44

    PubMed  CAS  Google Scholar 

  167. Forbes BE, Hartfield PJ, McNeil KA, Surinya KH, Milner SJ, Cosgrove LJ, Wallace JC (2002) Characteristics of binding of insulin-like growth factor (IGF)-I and IGF-II analogues to the type 1 IGF receptor determined by BIAcore analysis. Eur J Biochem 269:961–968

    PubMed  CAS  Google Scholar 

  168. Rogers SA, Purchio AF, Hammerman MR (1990) Mannose 6-phosphate-containing peptides activate phospholipase C in proximal tubular basolateral membranes from canine kidney. J Biol Chem 265:9722–9727

    PubMed  CAS  Google Scholar 

  169. Poiraudeau S, Lieberherr M, Kergosie N, Corvol MT (1997) Different mechanisms are involved in intracellular calcium increase by insulin-like growth factors 1 and 2 in articular chondrocytes: voltage-gated calcium channels, and/or phospholipase C coupled to a pertussis-sensitive G-protein. J Cell Biochem 64:414–422

    PubMed  CAS  Google Scholar 

  170. Singer WD, Brown HA, Sternweis PC (1997) Regulation of eurkaryotic phosphatidylionositol-specific phospholipase C and phospholipase D. Annu Rev Biochem 66:475–509

    PubMed  CAS  Google Scholar 

  171. Rhee SG (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70:281–312

    PubMed  CAS  Google Scholar 

  172. Vaughan PFT, Walker JH, Peers C (1999) The regulation of neurotransmitter secretion by protein kinase C. Mol Neurobiol 18:125–155

    Article  Google Scholar 

  173. Johnson RM, Connelly PA, Sisk RB, Pobiner BF, Hewlett EL, Garrison JC (1986) Pertussis toxin or phorbol 12-myristate 13-acetate can distinguish between epidermal growth factor- and angiotensin-stimulated signals in hepatocytes. Proc Natl Acad Sci USA 83:2026–2032

    Google Scholar 

  174. Liang MN, Garrison JC (1991) The epidermal growth factor receptor is coupled to a pertussis toxin-sensitive guanine nucleotide regulatory protein in rat hepatocytes. J Biol Chem 266:13342–13349

    PubMed  CAS  Google Scholar 

  175. Berven LA, Hughes BP, Barritt GJ (1994) A slowly ADP-ribosylated pertussis-toxin-sensitive GTP-binding regulatory protein is required for vasopressin-stimulated Ca2+ inflow in hepatocytes. Biochem J 299:399–407

    PubMed  CAS  Google Scholar 

  176. Nair BG, Rashed HM, Patel TB (1989) Epidermal growth factor stimulates rat cardiac adenylate cyclase through a GTP-binding regulatory protein. Biochem J 264:563–571

    PubMed  CAS  Google Scholar 

  177. Sun H, Seyer JM, Patel TB (1995) A region in the cytosolic domain of the epidermal growth factor receptor antithetically regulates the stimulatory and inhibitory guanine nucleotide-binding regulatory proteins of adenylyl cyclase. Proc Natl Acad Sci USA 92:2229–2233

    PubMed  CAS  Google Scholar 

  178. Rothenberg PL, Kahn CR (1988) Insulin inhibits pertussis toxin-catalyzed ADP-ribosylation of G-proteins. Evidence for a novel interaction between insulin receptors and G-proteins. J Biol Chem 263:15546–15552

    PubMed  CAS  Google Scholar 

  179. Ciaraldi TP, Maisel A (1989) Role of guanine nucleotide regulatory proteins in insulin stimulation of glucose transport in rat adipocytes. Influence of bacterial toxins. Biochem J 264:389–396

    PubMed  CAS  Google Scholar 

  180. Dalle S, Imamura T, Rose DW, Worrall DS, Ugi S, Hupfeld CJ, Olefsky JM (2002) Insulin induces heterologous desensitization of G-protein-coupled receptor and insulin-like growth factor I signaling by downregulating beta-arrestin-1. Mol Cell Biol 22:6272–6285

    PubMed  CAS  Google Scholar 

  181. Moxham CM, Malbon CC (1996) Insulin action impaired by deficiency of the G-protein subunit Giα2. Nature 379:840–844

    PubMed  CAS  Google Scholar 

  182. Tao J, Malbon CC, Wang HY (2001) Galpha(i2) enhances insulin signaling via suppression of protein-tyrosine phosphatase 1B. J Biol Chem 276:39705–39712

    PubMed  CAS  Google Scholar 

  183. Konopatskaya O, Shore AC, Tooke JE, Whatmore JL (2005) A role for heterotrimeric GTP-binding proteins and ERK1/2 in insulin-mediated, nitric-oxide-dependent, cyclic GMP production in human umbilical vein endothelial cells. Diabetologia 48:595–604

    PubMed  CAS  Google Scholar 

  184. Nishimoto I, Ogata E, Kojima I (1989) Pertussis toxin inhibits the action of insulin-like growth factor-I. Biochem Biophys Res Commun 148:403–411

    Google Scholar 

  185. Hallak H, Seiler AE, Green JS, Ross BN, Rubin R (2000) Association of heterotrimeric G(i) with the insulin-like growth factor-I receptor. Release of G(betagamma) subunits upon receptor activation. J Biol Chem 275:2255–2258

    PubMed  CAS  Google Scholar 

  186. Kuemmerle JF, Murthy KS (2001) Coupling of the insulin-like growth factor-I receptor tyrosine kinase to Gi2 in human intestinal smooth muscle: Gbetagamma -dependent mitogen-activated protein kinase activation and growth. J Biol Chem 276:7187–7194

    PubMed  CAS  Google Scholar 

  187. Cunha RA, Malva JO, Ribeiro JA (1999) Kainate receptors coupled to G(i)/G(o) proteins in the rat hippocampus. Mol Pharmacol 56:429–433

    PubMed  CAS  Google Scholar 

  188. Wang Y, Small DL, Stanimirovic DB, Morley P, Durkin JP (1997) AMPA receptor-mediated regulation of a Gi-protein in cortical neurons. Nature 389:502–504

    PubMed  CAS  Google Scholar 

  189. Kawai F, Sterling P (1999) AMPA receptor activates a G protein that suppresses a cGMP-gated current. J Neurosci 19:2954–2959

    PubMed  CAS  Google Scholar 

  190. Satake S, Saitow F, Rusakov D, Konishi S (2004) AMPA receptor-mediated presynaptic inhibition at cerebellar GABAergic synapses: a characterization of molecular mechanisms. Eur J Neurosci 19:2464–2474

    PubMed  Google Scholar 

  191. Takago H, Nakamura Y, Takahashi T (2005) G protein-dependent presynaptic inhibition mediated by AMPA receptors at the calyx of Held. Proc Natl Acad Sci USA 102:7368–7373

    PubMed  CAS  Google Scholar 

  192. Conway AM, Rakhit S, Pyne S, Pyne NJ (1999) Platelet-derived-growth factor stimulation of the p42/p44 mitogen-activated protein kinase pathway in airway smooth muscle: role of pertussis-toxin-sensitive G-proteins, c-Src tyrosine kinases and phosphoinositide 3-kinase. Biochem J 337:(Pt 2)171–177

    PubMed  CAS  Google Scholar 

  193. Alderton F, Rakhit S, Kong KC, Palmer T, Sambi B, Pyne S, Pyne NJ (2001) Tethering of the platelet-derived growth factor beta receptor to G-protein-coupled receptors. A novel platform for integrative signaling by these receptor classes in mammalian cells. J Biol Chem 276:28578–28585

    PubMed  CAS  Google Scholar 

  194. Krieger-Brauer HI, Medda P, Kather H (2000) Basic fibroblast growth factor utilizes both types of component subunits of Gs for dual signaling in human adipocytes. Stimulation of adenylyl cyclase via Galph(s) and inhibition of NADPH oxidase by Gbeta gamma(s). J Biol Chem 275:35920–35925

    PubMed  CAS  Google Scholar 

  195. Frazier WA, Gao AG, Dimitry J, Chung J, Brown EJ, Lindberg FP, Linder ME (1999) The thrombospondin receptor integrin-associated protein (CD47) functionally couples to heterotrimeric Gi. J Biol Chem 274:8554–8560

    PubMed  CAS  Google Scholar 

  196. Wang XQ, Lindberg FP, Frazier WA (1999) Integrin-associated protein stimulates alpha2beta1-dependent chemotaxis via Gi-mediated inhibition of adenylate cyclase and extracellular-regulated kinases. J Cell Biol 147:389–400

    PubMed  CAS  Google Scholar 

  197. Gong X, Dubois DH, Miller DJ, Shur BD (1995) Activation of a G protein complex by aggregation of beta-1,4-galactosyltransferase on the surface of sperm. Science 269:1718–1721

    PubMed  CAS  Google Scholar 

  198. Shi X, Amindari S, Paruchuru K, Skalla D, Burkin H, Shur BD, Miller DJ (2001) Cell surface beta-1,4-galactosyltransferase-I activates G protein-dependent exocytotic signaling. Development 128:645–654

    PubMed  CAS  Google Scholar 

  199. Anand-Srivastava MB, Sairam MR, Cantin M (1990) Ring-deleted analogs of atrial natriuretic factor inhibit adenylate cyclase/cAMP system. Possible coupling of clearance atrial natriuretic factor receptors to adenylate cyclase/cAMP signal transduction system. J Biol Chem 265:8566–8572

    PubMed  CAS  Google Scholar 

  200. Levin ER, Frank HJ (1991) Natriuretic peptides inhibit rat astroglial proliferation: mediation by C receptor. Am J Physiol 261(Pt 2):R453–R457

    PubMed  CAS  Google Scholar 

  201. Hu RM, Levin ER, Pedram A, Frank HJ (1992) Atrial natriuretic peptide inhibits the production and secretion of endothelin from cultured endothelial cells. Mediation through the C receptor. J Biol Chem 267:17384–17389

    PubMed  CAS  Google Scholar 

  202. Kiemer AK, Lehner MD, Hartung T, Vollmar AM (2002) Inhibition of cyclooxygenase-2 by natriuretic peptides. Endocrinology 143:846–852

    PubMed  CAS  Google Scholar 

  203. Cenciarelli C, Hohman RJ, Atkinson TP, Gusovsky F, Weissman AM (1992) Evidence for GTP-binding protein involvement in the tyrosine phosphorylation of the T cell receptor zeta chain. J Biol Chem 267:14527–14530

    PubMed  CAS  Google Scholar 

  204. Peter ME, Hall C, Ruhlmann A, Sancho J, Terhorst C (1992) The T-cell receptor zeta chain contains a GTP/GDP binding site. EMBO J 11:933–941

    PubMed  CAS  Google Scholar 

  205. Stanners J, Kabouridis PS, McGuire KL, Tsoukas CD (1995) Interaction between G proteins and tyrosine kinases upon T cell receptor. CD3-mediated signaling. J Biol Chem 270:30635–30642

    PubMed  CAS  Google Scholar 

  206. Lippert E, Jacques Y, Hermouet S (2000) Positive regulation of human T cell activation by Gi2 proteins and interleukin-8. J Leukoc Biol 67:742–748

    PubMed  CAS  Google Scholar 

  207. Murthy KS, Teng B-Q, Zhou H, Jin J-G, Grider JR, Makhlouf GM (2000) G(i-1)/G(i-2)-dependent signaling by single-transmembrane natriuretic peptide clearance receptor. Am J Physiol Gastrointest Liver Physiol 278:G974–G980

    PubMed  CAS  Google Scholar 

  208. Heuss C, Gerber U (2000) G-protein-independent signaling by G-protein-coupled receptors. Trends Neurosci 23:469–475

    PubMed  CAS  Google Scholar 

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Acknowledgment

We would like to thank Dr. G.B. Baker for his useful comments on this review. CH is a recipient of the Alzheimer Society studentship award, and SK is a recipient of a Canada Research Chair (CRC) in Neurodegenerative diseases and a Senior Scholar award from the AHFMR. JHJ is a CRC recipient in Alzheimer Research. This paper was supported by grants from the Natural Sciences and Engineering Research Council of Canada (SK), Alberta Heritage Foundation for Medical Research (AHFMR; SK), Canadian Institutes of Health Research (SK and JHJ), and National Institutes of Health grant CA91885 (RGM).

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Authors and Affiliations

  1. Department of Psychiatry, Centre for Alzheimer and Neurodegenerative Research, University of Alberta, Edmonton, AB, Canada, T6G 2B7

    C. Hawkes, A. Amritraj & S. Kar

  2. Department of Biochemistry and Molecular Biology, University of Nebraska Medical Center, Omaha, NE, USA

    R. G. MacDonald

  3. Department of Medicine (Neurology), Centre for Alzheimer and Neurodegenerative Research, University of Alberta, Edmonton, AB, Canada, T6G 2B7

    J. H. Jhamandas & S. Kar

  4. Alberta Centre for Prions and Protein Folding Diseases Departments of Medicine (Neurology) and Psychiatry, University of Alberta, Edmonton, AB, Canada, T6G 2M8

    S. Kar

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  1. C. Hawkes
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Hawkes, C., Amritraj, A., MacDonald, R.G. et al. Heterotrimeric G Proteins and the Single-Transmembrane Domain IGF-II/M6P Receptor: Functional Interaction and Relevance to Cell Signaling. Mol Neurobiol 35, 329–345 (2007). https://doi.org/10.1007/s12035-007-0021-2

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