The insulin receptor translocates to the nucleus to regulate cell proliferation in liver

Hepatology

Volumn 59, Issue 1, 2014, Pages 274-283

  Amaya, Maria J ^a   Oliveira, André G ^b   Guimarães, Erika S ^b   Casteluber, Marisa C F ^b   Carvalho, Sandhra M ^b   Andrade, Lidia M ^b,c   Pinto, Mauro C X ^b   Mennone, Albert ^a   Oliveira, Cleida A ^b   Resende, Rodrigo R ^b   Menezes, Gustavo B ^b   Nathanson, Michael H ^a   Leite, M Fatima ^b,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; GLUCOSE; GLYCOGEN; INOSITOL 1,4,5 TRISPHOSPHATE; INSULIN; INSULIN RECEPTOR; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM SIGNALING; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; GLUCOSE METABOLISM; HORMONE ACTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LIVER CANCER CELL LINE; LIVER CELL; LIVER METABOLISM; LIVER REGENERATION; MALE; MITOGENESIS; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; RAT; ANIMAL; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM SIGNALING; CELL NUCLEUS; CELL PROLIFERATION; INOSITOL 1,4,5-TRISPHOSPHATE; INSULIN; LIVER REGENERATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN;

EID: 84894697401     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26609     Document Type: Article

References (39)

1. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. Hepatology 2006;43:S45-S53.
2. Taub R. Liver regeneration: From myth to mechanism. Nat Rev Mol Cell Biol 2004;5:836-847.
3. Huang W, Ma K, Zhang J, Qatanani M, Cuvillier J, Liu J, et al. Nuclear receptor-dependent bile acid signaling is required for normal liver regeneration. Science 2006;312:233-236.
4. Koontz JW, Iwahashi M. Insulin as a potent, specific growth factor in a rat hepatoma cell line. Science 1981;211:947-949.
5. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001;414:799-806.
6. Berasain C, Garcia-Trevijano ER, Castillo J, Erroba E, Lee DC, Prieto J, Avila MA. Amphiregulin: an early trigger of liver regeneration in mice. Gastroenterology 2005;128:424-432.
7. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, Thorgeirsson SS. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci U S A 2004;101:4477-4482.
8. De Meyts P, Whittaker J. Structural biology of insulin and IGF1 receptors: implications for drug design. Nat Rev Drug Discov 2002;1:769-783.
9. Farese RV, Kuo JY, Babischkin JS, Davis JS. Insulin provokes a transient activation of phospholipase C in the rat epididymal fat pad. J Biol Chem 1986;261:8589-8592.
10. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis, and remodelling. Nat Rev Mol Cell Biol 2003;4:517-529.
11. Rodrigues MA, Gomes DA, Andrade VA, Leite MF, Nathanson MH. Insulin induces calcium signals in the nucleus of rat hepatocytes. Hepatology 2008;48:1621-1631.
12. Angelis Campos AC, Rodrigues MA, de Andrade C, de Goes AM, Nathanson MH, Gomes DA. Epidermal growth factor receptors destined for the nucleus are internalized via a clathrin-dependent pathway. Biochem Biophys Res Commun 2011;412:341-346.
13. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, et al. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 2001;3:802-808.
14. Gomes DA, Rodrigues MA, Leite MF, Gomez MV, Varnai P, Balla T, et al. c-Met must translocate to the nucleus to initiate calcium signals. J Biol.Chem. 2008;283:4344-4351.
15. Reilly JF, Maher PA. Importin beta-mediated nuclear import of fibroblast growth factor receptor: role in cell proliferation. J Cell Biol 2001;152:1307-1312.
16. Rodrigues MA, Gomes DA, Leite MF, Grant W, Zhang L, Lam W, et al. Nucleoplasmic calcium is required for cell proliferation. J. Biol. Chem. 2007;282:17061-17068.
17. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 2006;7:85-96.
18. Echevarria W, Leite MF, Guerra MT, Zipfel WR, Nathanson MH. Regulation of calcium signals in the nucleus by a nucleoplasmic reticulum. Nat Cell Biol 2003;5:440-446.
19. Leite MF, Thrower EC, Echevarria W, Koulen P, Hirata K, Bennett AM, et al. Nuclear and cytosolic calcium are regulated independently. Proc Natl Acad Sci U S A 2003;100:2975-2980.
20. Arantes LA, Aguiar CJ, Amaya MJ, Figueiro NC, Andrade LM, Rocha-Resende C, et al. Nuclear inositol 1, 4, 5-trisphosphate is a necessary and conserved signal for the induction of both pathological and physiological cardiomyocyte hypertrophy. J Mol Cell Cardiol 2012;53:475-486.
21. Higgins GM, Anderson RM. Experimental pathology of the liver. I. Restoration of the liver of white rat after partial surgical removal. Arch Pathol 1931;12:186-202.
22. Harvey CE, Post JJ, Palladinetti P, Freeman AJ, Ffrench RA, Kumar RK, et al. Expression of the chemokine IP-10 (CXCL10) by hepatocytes in chronic hepatitis C virus infection correlates with histological severity and lobular inflammation. J Leukoc Biol 2003;74:360-369.
23. Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F. A colorimetric method for the determination of sugars. Nature 1951;168:167.
24. Leite MF, Hirata K, Pusl T, Burgstahler AD, Okazaki K, Ortega JM, et al. Molecular basis for pacemaker cells in epithelia. J Biol Chem 2002;277:16313-16323.
25. O'Brien EM, Gomes DA, Sehgal S, Nathanson MH. Hormonal regulation of nuclear permeability. J Biol Chem 2007;282:4210-4217.
26. Hirata K, Pusl T, O'Neill AF, Dranoff JA, Nathanson MH. The type II inositol 1, 4, 5-trisphosphate receptor can trigger Ca2+ waves in rat hepatocytes. Gastroenterology 2002;122:1088-1100.
27. Michalopoulos G, Pitot HC. Primary culture of parenchymal liver cells on collagen membranes. Morphological and biochemical observations. Exp Cell Res 1975;94:70-78.
28. Carpentier JL. Robert Feulgen Prize Lecture 1993. The journey of the insulin receptor into the cell: from cellular biology to pathophysiology. Histochemistry 1993;100:169-184.
29. Foti M, Porcheron G, Fournier M, Maeder C, Carpentier JL. The neck of caveolae is a distinct plasma membrane subdomain that concentrates insulin receptors in 3T3-L1 adipocytes. Proc Natl Acad Sci U S A 2007;104:1242-1247.
30. Guerra MT, Fonseca EA, Melo FM, Andrade VA, Aguiar CJ, Andrade LM, et al. Mitochondrial calcium regulates rat liver regeneration through the modulation of apoptosis. Hepatology 2011;54:296-306.
31. Lagoudakis L, Garcin I, Julien B, Nahum K, Gomes DA, Combettes L, et al. Cytosolic calcium regulates liver regeneration in the rat. Hepatology 2010;52:602-611.
32. Graef IA, Mermelstein PG, Stankunas K, Neilson JR, Deisseroth K, Tsien RW, Crabtree GR. L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature 1999;401:703-708.
33. Di Guglielmo GM, Drake PG, Baass PC, Authier F, Posner BI, Bergeron JJ. Insulin receptor internalization and signalling. Mol Cell Biochem 1998;182:59-63.
34. Balbis A, Baquiran G, Mounier C, Posner BI. Effect of insulin on caveolin-enriched membrane domains in rat liver. J Biol Chem 2004;279:39348-39357.
35. O'Malley KL, Jong YJ, Gonchar Y, Burkhalter A, Romano C. Activation of metabotropic glutamate receptor mGlu5 on nuclear membranes mediates intranuclear Ca2+ changes in heterologous cell types and neurons. J Biol Chem 2003;278:28210-28219.
36. Zhu T, Gobeil F, Vazquez-Tello A, Leduc M, Rihakova L, Bossolasco M, et al. Intracrine signaling through lipid mediators and their cognate nuclear G-protein-coupled receptors: a paradigm based on PGE2, PAF, and LPA1 receptors. Can J Physiol Pharmacol 2006;84:377-391.
37. Gu H, Neel BG. The "Gab" in signal transduction. Trends Cell Biol 2003;13:122-130.
38. Bard-Chapeau EA, Hevener AL, Long S, Zhang EE, Olefsky JM, Feng GS. Deletion of Gab1 in the liver leads to enhanced glucose tolerance and improved hepatic insulin action. Nat Med 2005;11:567-571.
39. Wakelam MJ, Murphy GJ, Hruby VJ, Houslay MD. Activation of two signal-transduction systems in hepatocytes by glucagon. Nature 1986;323:68-71.