AMP-Activated Protein Kinase Phosphorylates Retinoblastoma Protein to Control Mammalian Brain Development

Developmental Cell

Volumn 16, Issue 2, 2009, Pages 256-270

  Dasgupta, Biplab ^a   Milbrandt, Jeffrey ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLCYCLE; DEVBIO; SIGNALING

Indexed keywords

GROWTH FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; RETINOBLASTOMA PROTEIN; SERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA CHAIN; BRAIN ATROPHY; BRAIN DEVELOPMENT; BRAIN MALFORMATION; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL GROWTH; CELL LOSS; CENTRAL NERVOUS SYSTEM; CEREBELLUM ATROPHY; CONTROLLED STUDY; DEMYELINATION; DENTATE GYRUS; DISEASE SEVERITY; ENZYME ACTIVITY; FEMALE; MALE; MOUSE; MOUSE MUTANT; NERVE CELL; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; BRAIN; CENTRAL NERVOUS SYSTEM; MICE; MICE, TRANSGENIC; MUTATION; MYELIN SHEATH; NEURONS; OLIGODENDROGLIA; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN; STEM CELLS;

MAMMALIA; MUS;

EID: 59649101100     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2009.01.005     Document Type: Article

References (72)

1. Baena-González E., Rolland F., Thevelein J.M., and Sheen J. A central integrator of transcription networks in plant stress and energy signaling. Nature 448 (2007) 938-942
2. Bachoo R.M., Kim R.S., Ligon K.L., Maher E.A., Brennan C., Billings N., Chan S., Li C., Rowitch D.H., Wong W.H., and DePinho R.A. Molecular diversity of astrocytes with implications for neurological disorders. Proc. Natl. Acad. Sci. USA 101 (2004) 8384-8389
3. Barnabé-Heider F., Wasylnka J.A., Karl J.L., Fernandes K.J.L., Porsche C., Sendtner M., Kaplan D.R., and Miller F.D. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48 (2005) 253-265
4. Barnes B.R., Marklund S., Steiler T.L., Walter M., Hjälm G., Amarger V., Mahlapuu M., Leng Y., Johansson C., Galuska D., et al. The 5′-AMP-activated protein kinase gamma3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle. J. Biol. Chem. 279 (2004) 38441-38447
5. Barriere C., Santamaria D., Cerqueira A., Galan J., Martin A., Ortega S., Malumbres M., Dubus P., and Barbacid M. Mice thrive without Cdk4 and Cdk2. Mol. Oncol. 1 (2007) 72-83
6. Baumann P., Mandl-Weber S., Emmerich B., Straka C., and Schmidmaier R. Inhibition of adenosine monophosphate-activated kinase induces apoptosis in multiple myeloma cells. Anticancer Drugs 18 (2007) 405-410
7. Berthet C., Klarmann K.D., Hilton M.B., Suh H.C., Keller J.R., Kiyokawa H., and Kaldis P. Combined loss of Cdk2 and Cdk4 results in embryonic lethality and Rb hypophosphorylation. Dev. Cell 10 (2006) 563-573
8. Blair E., Redwood C., Ashrafian H., Oliveira M., Broxholme J., Kerr B., Salmon A., Ostman-Smith I., and Watkins H. Mutations in the γ2 subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum. Mol. Genet. 10 (2001) 1215-1220
9. Bürgers H.F., Schelshorn D.W., Wagner W., Kuschinsky W., and Maurer M.H. Acute anoxia stimulates proliferation in adult neural stem cells from the rat brain. Exp. Brain Res. 188 (2008) 33-43
10. Burkhart D.L., and Sage J. Cellular mechanisms of tumor suppression by the retinoblastoma gene. Nat. Rev. Cancer 8 (2008) 671-682
11. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28 (2008) 264-278
12. Callaghan D.A., Dong L., Callaghan S.M., Hou Y.X., Dagnino L., and Slack R.S. Neural precursor cells differentiating in the absence of Rb exhibit delayed terminal mitosis and deregulated E2F 1 and 3 activity. Dev. Biol. 207 (1999) 257-270
13. Chang M.W., Barr E., Seltzer J., Jiang Y.Q., Nabel G.J., Nabel E.G., Parmacek M.S., and Leiden J.M. Cytostatic gene therapy for vascular proliferative disorders with a constitutively active form of the retinoblastoma gene product. Science 267 (1995) 518-522
14. Ciemeryc M.A., Kenney A.M., Sicinska E., Kalaszczynska I., Bronson R.T., Rowitch D.H., Gardner H., and Sicinski P. Development of mice expressing a single D-type cyclin. Genes Dev. 16 (2002) 3277-3289
15. Claret M., Smith M.A., Batterham R.L., Selman C., Choudhury A.I., Fryer L.G., Clements M., Al-Qassab H., Heffron H., Xu A.W., et al. AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. J. Clin. Invest. 117 (2007) 2325-2336
16. Culmsee C., Monnig J., Kemp B.E., and Mattson M.P. AMP-activated protein kinase is highly expressed in neurons in the developing rat brain and promotes neuronal survival following glucose deprivation. J. Mol. Neurosci. 17 (2001) 45-58
17. Dagon Y., Avraham Y., Magen I., Gertler A., Ben-Hur T., and Berry E.M. Nutritional status, cognition, and survival: a new role for leptin and AMP kinase. J. Biol. Chem. 280 (2005) 42142-42148
18. Dali-Youcef N., Mataki C., Coste A., Messaddeq N., Giroud S., Blanc S., Koehl C., Champy M.F., Chambon P., Fajas L., et al. Adipose tissue-specific inactivation of the retinoblastoma protein protects against diabesity because of increased energy expenditure. Proc. Natl. Acad. Sci. USA. 104 (2007) 10703-10708
19. Dasgupta B., and Gutmann D.H. Neurofibromin regulates neural stem cell proliferation, survival, and astroglial differentiation in vitro and in vivo. J. Neurosci. 25 (2005) 5584-5594
20. Domowicz M.S., Sanders T.A., Ragsdale C.W., and Schwartz N.B. Aggrecan is expressed by embryonic brain glia and regulates astrocyte development. Dev. Biol. 315 (2008) 114-124
21. Dyck J.R. The ischemic heart: starving to stimulate the adiponectin-AMPK signaling axis. Circulation 116 (2007) 2779-2781
22. Erez A., Chaussepied M., Castiel A., Colaizzo-Anas T., Aplan P.D., Ginsberg D., and Izraeli S. The mitotic checkpoint gene, SIL is regulated by E2F1. Int. J. Cancer 123 (2008) 1721-1725
23. Fajas L., Egler V., Reiter R., Hansen J., and Kristiansen K. The retinoblastoma-histone deacetylase 3 complex inhibits PPARgamma and adipocyte differentiation. Dev. Cell 3 (2002) 903-910
24. Fluckiger A.C., Marcy G., Marchand M., Négre D., Cosset F.L., Mitalipov S., Wolf D., Savatier P., and Dehay C. Cell cycle features of primate embryonic stem cells. Stem Cells 24 (2006) 547-556
25. Fu J., Tay S.S., Ling E.A., and Dheen S.T. High glucose alters the expression of genes involved in proliferation and cell-fate specification of embryonic neural stem cells. Diabetologia 49 (2006) 1027-1038
26. Fulco M., Cen Y., Zhao P., Hoffman E.P., McBurney M.W., Sauve A.A., and Sartorelli V. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev. Cell 14 (2008) 661-673
27. Galderisi U., Jori F.P., and Giordano A. Cell cycle regulation and neural differentiation. Oncogene 22 (2003) 5208-5219
28. Guigas B., Taleux N., Foretz M., Detaille D., Andreelli F., Viollet B., and Hue L. AMP-activated protein kinase-independent inhibition of hepatic mitochondrial oxidative phosphorylation by AICA riboside. Biochem. J. 404 (2007) 499-507
29. Hegedus B., Dasgupta B., Shin J.E., Emnett R.J., Hart-Mahon E.K., Elghazi L., Bernal-Mizrachi E., and Gutmann D.H. Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP- and Ras-dependent mechanisms. Cell Stem Cell 1 (2007) 443-457
30. Heuvel S., and Dyson N.J. Conserved function of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9 (2008) 713-724
31. Iseli T.J., Walter M., van Denderen B.J., Katsis F., Witters L.A., Kemp B.E., Michell B.J., and Stapleton D. AMP-activated protein kinase beta subunit tethers alpha and gamma subunits via its C-terminal sequence (186-270). J. Biol. Chem. 280 (2005) 13395-13400
32. Jiang Z., and Zacksenhaus E. Activation of retinoblastoma protein in mammary gland leads to ductal growth suppression, precocious differentiation, and adenocarcinoma. J. Cell Biol. 156 (2002) 185-198
33. Jones R.G., Plas D.R., Kubek S., Buzzai M., Mu J., Xu Y., Birnbaum M.J., and Thompson C.B. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 18 (2005) 283-293
34. Jørgensen S.B., Wojtaszewski J.F., Viollet B., Andreelli F., Birk J.B., Hellsten Y., Schjerling P., Vaulont S., Neufer P.D., Richter E.A., et al. Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J. 19 (2005) 1146-1148
35. Kenney A.M., Widlund H.R., and Rowitch D.H. Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131 (2004) 217-228
36. Kim H.S., Hwang J.T., Yun H., Chi S.G., Lee S.J., Kang I., Yoon K.S., Choe W.J., Kim S.S., and Ha J. Inhibition of AMP-activated protein kinase sensitizes cancer cells to cisplatin-induced apoptosis via hyper-induction of p53. J. Biol. Chem. 283 (2007) 3731-3742
37. Knoepfler P.S., Cheng P.F., and Eisenman R.N. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev. 16 (2002) 2699-2712
38. Kuramoto N., Wilkins M.E., Fairfax B.P., Revilla-Sanchez R., Terunuma M., Tamaki K., Iemata M., Warren N., Couve A., Calver A., et al. Phospho-dependent functional modulation of GABA(B) receptors by the metabolic sensor AMP-dependent protein kinase. Neuron 53 (2007) 233-247
39. Laderoute K.R., Amin K., Calaoagan J.M., Knapp M., Le T., Orduna J., Foretz M., and Viollet B. 5′-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol. Cell. Biol. 26 (2006) 5336-5347
40. Lee E.Y., Chang C.Y., Hu N., Wang Y.C., Lai C.C., Herrup K., Lee W.H., and Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359 (1992) 288-294
41. Lee J.H., Koh H., Kim M., Kim Y., Lee S.Y., Karess R.E., Lee S.H., Shong M., Kim J.M., Kim J., et al. Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 447 (2007) 1017-1020
42. Malumbres M., Sotillo R., Santamaría D., Galán J., Cerezo A., Ortega S., Dubus P., and Barbacid M. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 118 (2004) 493-504
43. Marino S., Vooijs M., van Der Gulden H., Jonkers J., and Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14 (2000) 994-1004
44. Massagué J. G1 cell-cycle control and cancer. Nature 432 (2004) 298-306
45. McLear J.A., Garcia-Fresco G., Bhat M.A., and Van Dyke T.A. In vivo inactivation of pRb, p107 and p130 in murine neuroprogenitor cells leads to major CNS developmental defects and high seizure rates. Mol. Cell. Neurosci. 33 (2006) 260-273
46. Miller E.J., Li J., Leng L., McDonald C., Atsumi T., Bucala R., and Young L.H. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 451 (2008) 578-582
47. Mittnacht S. Control of pRB phosphorylation. Curr. Opin. Genet. Dev. 8 (1998) 21-27
48. Mirouse V., Swick L.L., Kazgan N., St Johnston D., and Brenman J.E. LKB1 and AMPK maintain epithelial cell polarity under energetic stress. J. Cell Biol. 177 (2007) 387-392
49. Nagata D., Mogi M., and Walsh K. AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J. Biol. Chem. 278 (2003) 31000-31006
50. Naderi S., Hunton I.C., and Wang J.Y.J. Radiation dose-dependent maintenance of G2 arrest requires retinoblastoma protein. Cell Cycle 1 (2002) 193-200
51. Niculescu III A.B., Chen X., Smeets M., Hengst L., Prives C., and Reed S.I. Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol. Cell. Biol. 18 (1998) 629-643
52. Orford K.W., and Scadden D.T. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 9 (2008) 115-128
53. Papadimou E., Ménard C., Grey C., and Pucéat M. Interplay between the retinoblastoma protein and LEK1 specifies stem cells toward the cardiac lineage. EMBO J. 24 (2005) 1750-1761
54. Polager S., and Ginsberg D. E2F mediates sustained G2 arrest and down-regulation of Stathmin and AIM-1 expression in response to genotoxic stress. J. Biol. Chem. 278 (2003) 1443-1449
55. Rigberg D.A., Kim F.S., Sebastian J.L., Kazanjian K.K., and McFadden D.W. Hypophosphorylated retinoblastoma protein is associated with G2 arrest in esophageal squamous cell carcinoma. J. Surg. Res. 84 (1999) 101-105
56. Roig J.M., Molina M.A., Cascante A., Calbó J., Carbó N., Wirtz U., Sreedharan S., Fillat C., and Mazo A. Adenovirus-mediated retinoblastoma 94 gene transfer induces human pancreatic tumor regression in a mouse xenograft model. Clin. Cancer Res. 10 (2004) 1454-1462
57. Sankaran V.G., Orkin S.H., and Walkley C.R. Rb intrinsically promotes erythropoiesis by coupling cell cycle exit with mitochondrial biogenesis. Genes Dev. 22 (2008) 463-475
58. Sherr C.J. The Pezcoller lecture: cancer cell cycles revisited. Cancer Res. 60 (2000) 3689-3695
59. Sotillo R., Hernando E., Díaz-Rodríguez E., Teruya-Feldstein J., Cordón-Cardo C., Lowe S.W., and Benezra R. Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11 (2007) 9-23
60. Spasić M.R., Callaerts P., and Norga K.K. Drosophila alicorn is a neuronal maintenance factor protecting against activity-induced retinal degeneration. J. Neurosci. 28 (2008) 6419-6429
61. Stolzing A., Coleman N., and Scutt A. Glucose-induced replicative senescence in mesenchymal stem cells. Rejuvenation Res. 9 (2006) 31-35
62. Tschäpe J.A., Hammerschmied C., Mühlig-Versen M., Athenstaedt K., Daum G., and Kretzschmar D. The neurodegeneration mutant löchrig interferes with cholesterol homeostasis and Appl processing. EMBO J. 21 (2002) 6367-6376
63. Vincent M.F., Marangos P.J., Gruber H.E., and Van den Berghe G. Inhibition by AICA riboside of gluconeogenesis in isolated rat hepatocytes. Diabetes 40 (1991) 1259-1266
64. Vincent M.F., Bontemps F., and Van den Berghe G. Inhibition of glycolysis by 5-amino-4-imidazolecarboxamide riboside in isolated rat hepatocytes. Biochem. J. 281 (1992) 267-272
65. Vincent O., Townley R., Kuchin S., and Carlson M. Subcellular localization of the Snf1 kinase is regulated by specific beta subunits and a novel glucose signalling mechanism. Genes Dev. 15 (2001) 1104-1114
66. Viollet B., Andreelli F., Jørgensen S.B., Perrin C., Geloen A., Flamez D., Mu J., Lenzner C., Baud O., Bennoun M., et al. The AMP-activated protein kinase alpha2 catalytic subunit controls whole-body insulin sensitivity. J. Clin. Invest. 111 (2003) 91-98
67. Weintraub S.J., Chow K.N., Luo R.X., Zhang S.H., He S., and Dean D.C. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature 375 (1995) 812-815
68. Wikenheiser-Brokamp K.A. Rb family proteins differentially regulate distinct cell lineages during epithelial development. Development 131 (2004) 4299-4310
69. Xue B., and Kahn B.B. AMPK integrates nutrient and hormonal signals to regulate food intake and energy balance through effects in the hypothalamus and peripheral tissues. J. Physiol. 574 (2006) 73-83
70. Yen A., and Sturgill R. Hypophosphorylation of the RB protein in S and G2 as well as G1 during growth arrest. Exp. Cell Res. 241 (1998) 324-331
71. Yun H., Lee M., Kim S.S., and Ha J. Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma. J. Biol. Chem. 280 (2005) 9963-9972
72. Zarkowska T., and Mittnacht S. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J. Biol. Chem. 272 (1997) 12738-12746