LKB1 and AMPK regulate synaptic remodeling in old age

Nature Neuroscience

Volumn 17, Issue 9, 2014, Pages 1190-1197

  Samuel, Melanie A ^a   Voinescu, P Emanuela ^a   Lilley, Brendan N ^a   De Cabo, Rafa ^b   Foretz, Marc ^c,d,e   Viollet, Benoit ^c,d,e   Pawlyk, Basil ^f   Sandberg, Michael A ^f   Vavvas, Demetrios G ^f   Sanes, Joshua R ^a  

^a HARVARD UNIVERSITY   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c INSTITUT COCHIN   (France)

^d CNRS   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; PROTEIN KINASE LKB1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN SERINE THREONINE KINASE; STK11 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PHOTORECEPTOR; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RETINA DISEASE; SENESCENCE; WILD TYPE; YOUNG ADULT; AGING; ANIMAL; C57BL MOUSE; ELECTRORETINOGRAPHY; ENZYME SPECIFICITY; FEMALE; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA GANGLION CELL; RETINA ROD OUTER SEGMENT; SYNAPSE;

AGING; AMACRINE CELLS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ELECTRORETINOGRAPHY; FEMALE; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RETINAL BIPOLAR CELLS; RETINAL GANGLION CELLS; ROD CELL OUTER SEGMENT; SUBSTRATE SPECIFICITY; SYNAPSES;

EID: 84921686487     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3772     Document Type: Article

References (62)

1. Burke, S.N. & Barnes, C.A. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 7, 30-40 (2006).
2. Morrison, J.H. & Baxter, M.G. The ageing cortical synapse: hallmarks and implications for cognitive decline. Nat. Rev. Neurosci. 13, 240-250 (2012).
3. Scheff, S.W. & Price, D.A. Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. Neurobiol. Aging 24, 1029-1046 (2003).
4. Scheff, S.W., Price, D.A., Schmitt, F.A., DeKosky, S.T. & Mufson, E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 68, 1501-1508 (2007).
5. Samuel, M.A., Zhang, Y., Meister, M. & Sanes, J.R. Age-related alterations in neurons of the mouse retina. J. Neurosci. 31, 16033-16044 (2011).
6. Liets, L.C., Eliasieh, K., van der List, D.A. & Chalupa, L.M. Dendrites of rod bipolar cells sprout in normal aging retina. Proc. Natl. Acad. Sci. USA 103, 12156-12160 (2006).
7. Eliasieh, K., Liets, L.C. & Chalupa, L.M. Cellular reorganization in the human retina during normal aging. Invest. Ophthalmol. Vis. Sci. 48, 2824-2830 (2007).
8. Terzibasi, E. et al. Age-dependant remodeling of retinal circuitry. Neurobiol. Aging 30, 819-828 (2009).
9. Sanes, J.R. & Zipursky, S.L. Design principles of insect and vertebrate visual systems. Neuron 66, 15-36 (2010).
10. Masland, R.H. The fundamental plan of the retina. Nat. Neurosci. 4, 877-886 (2001).
11. Alessi, D.R., Sakamoto, K. & Bayascas, J.R. LKB1-dependent signaling pathways. Annu. Rev. Biochem. 75, 137-163 (2006).
12. Barnes, A.P. et al. LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129, 549-563 (2007).
13. Shelly, M., Cancedda, L., Heilshorn, S., Sumbre, G. & Poo, M.M. LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 129, 565-577 (2007).
14. Mirouse, V. & Billaud, M. The LKB1/AMPK polarity pathway. FEBS Lett. 585, 981-985 (2011).
15. Funakoshi, M. et al. A gain-of-function screen identifies wbd and lkb1 as lifespan-extending genes in Drosophila. Biochem. Biophys. Res. Commun. 405, 667-672 (2011).
16. Narbonne, P. & Roy, R. Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 457, 210-214 (2009).
17. Houtkooper, R.H., Williams, R.W. & Auwerx, J. Metabolic networks of longevity. Cell 142, 9-14 (2010).
18. Cai, Z., Yan, L.J., Li, K., Quazi, S.H. & Zhao, B. Roles of AMP-activated protein kinase in Alzheimer's disease. Neuromolecular Med. 14, 1-14 (2012).
19. Ollila, S. & Mäkelä, T.P. The tumor suppressor kinase LKB1: lessons from mouse models. J. Mol. Cell Biol. 3, 330-340 (2011).
20. Bardeesy, N. et al. Loss of the Lkb1 tumour suppressor provokes intestinal polyposis but resistance to transformation. Nature 419, 162-167 (2002).
21. Kolesnikov, A.V., Fan, J., Crouch, R.K. & Kefalov, V.J. Age-related deterioriation of rod vision in mice. J. Neurosci. 30, 11222-11231 (2010).
22. Palczewski, K. Chemistry and biology of vision. J. Biol. Chem. 287, 1612-1619 (2012).
23. Li, S. et al. Rhodopsin-iCre transgenic mouse line for Cre-mediated rod-specific gene targeting. Genesis 41, 73-80 (2005).
24. Dick, O. et al. The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37, 775-786 (2003).
25. Mansergh, F. et al. Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum. Mol. Genet. 14, 3035-3046 (2005).
26. Chang, B. et al. The nob2 mouse, a null mutation in Cacna1f: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis. Neurosci. 23, 11-24 (2006).
27. Specht, D. et al. Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: plasticity in the rod and degeneration in the cone system. Eur. J. Neurosci. 26, 2506-2515 (2007).
28. Amato, S. et al. AMP-activated protein kinase regulates neuronal polarization by interfering with PI3-kinase localization. Science 332, 247-251 (2011).
29. Williams, T., Courchet, J., Viollet, B., Brenman, J.E. & Polleux, F. AMP-activated protein kinase (AMPK) activity is not required for neuronal development but regulates axogenesis during metabolic stress. Proc. Natl. Acad. Sci. USA 108, 5849-5854 (2011).
30. Kishi, M., Pan, Y.A., Crump, J.G. & Sanes, J.R. Mammalian SAD kinases are required for neuronal polarization. Science 307, 929-932 (2005).
31. Biernat, J. et al. Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity. Mol. Biol. Cell 13, 4013-4028 (2002).
32. Hardie, D.G., Ross, F.A. & Hawley, S.A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13, 251-262 (2012).
33. Woods, A. et al. Identification of phosphorylation sites in AMP-activated protein kinase (AMPK) for upstream AMPK kinases and study of their roles by site-directed mutagenesis. J. Biol. Chem. 278, 28434-28442 (2003).
34. Kolb, H. The connections between horizontal cells and photoreceptors in the retina of the cat: electron microscopy of Golgi preparations. J. Comp. Neurol. 155, 1-14 (1974).
35. Wässle, H., Puller, C., Müller, F. & Haverkamp, S. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J. Neurosci. 29, 106-117 (2009).
36. Koulen, P., Fletcher, E.L., Craven, S.E., Bredt, D.S. & Wässle, H. Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J. Neurosci. 18, 10136-10149 (1998).
37. Brandstätter, J.H., Fletcher, E.L., Garner, C.C., Gundelfinger, E.D. & Wässle, H. Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina. Eur. J. Neurosci. 11, 3683-3693 (1999).
38. Shaw, R.J. et al. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 310, 1642-1646 (2005).
39. Dagon, Y. et al. Nutritional status, cognition and survival: a new role for leptin and AMP kinase. J. Biol. Chem. 280, 42142-42148 (2005).
40. Lizcano, J.M. et al. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843 (2004).
41. Lilley, B.N., Pan, Y.A. & Sanes, J.R. SAD kinases sculpt axonal arbors of sensory neurons through long- and short-term responses to neurotrophin signals. Neuron 79, 39-53 (2013).
42. Brown, M.C., Holland, R.L. & Hopkins, W.G. Motor nerve sprouting. Annu. Rev. Neurosci. 4, 17-42 (1981).
43. tom Dieck, S. et al. Deletion of the presynaptic scaffold CAST reduces active zone size in rod photoreceptors and impairs visual processing. J. Neurosci. 32, 12192-12203 (2012).
44. 2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat. Neurosci. 7, 1079-1087 (2004).
45. Ikematsu, N. et al. Phosphorylation of the voltage-gated potassium channel Kv2.1 by AMP-activated protein kinase regulates membrane excitability. Proc. Natl. Acad. Sci. USA 108, 18132-18137 (2011).
46. Stenesen, D. et al. Adenosine nucleotide biosynthesis and AMPK regulate adult life span and mediate the longevity benefit of caloric restriction in flies. Cell Metab. 17, 101-112 (2013).
47. Joseph, J., Cole, G., Head, E. & Ingram, D. Nutrition, brain aging and neurodegeneration. J. Neurosci. 29, 12795-12801 (2009).
48. Valdez, G. et al. Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc. Natl. Acad. Sci. USA 107, 14863-14868 (2010).
49. Furuta, Y., Lagutin, O., Hogan, B.L. & Oliver, G.C. Retina- and ventral forebrain-specific Cre recombinase activity in transgenic mice. Genesis 26, 130-132 (2000).
50. Rowan, S. & Cepko, C.L. Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter. Dev. Biol. 271, 388-402 (2004).
51. Marquardt, T. et al. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105, 43-55 (2001).
52. Momcilovic, M., Hong, S.P. & Carlson, M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J. Biol. Chem. 281, 25336-25343 (2006).
53. Liu, H.H., Xie, M., Schneider, M.D. & Chen, Z.J. Essential role of TAK1 in thymocyte development and activation. Proc. Natl. Acad. Sci. USA 103, 11677-11682 (2006).
54. Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99-103 (1999).
55. Viollet, B. et al. The AMP-activated protein kinase alpha2 catalytic subunit controls whole-body insulin sensitivity. J. Clin. Invest. 111, 91 (2003).
56. Zhu, X. et al. Mouse cone arrestin expression pattern: light induced translocation in cone photoreceptors. Mol. Vis. 8, 462-471 (2002).
57. Nagai, T., Yamada, S., Tominaga, T., Ichikawa, M. & Miyawaki, A. Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. USA 101, 10554-10559 (2004).
58. Hong, Y.K., Kim, I.J. & Sanes, J.R. Stereotyped axonal arbors of retinal ganglion cell subsets in the mouse superior colliculus. J. Comp. Neurol. 519, 1691-1711 (2011).
59. Lefebvre, J.L., Kostadinov, D., Chen, W.V., Maniatis, T. & Sanes, J.R. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488, 517-521 (2012).
60. Kay, J.N., Voinescu, P.E., Chu, M.W. & Sanes, J.R. Neurod6 expression defines new retinal amacrine cell subtypes and regulates their fate. Nat. Neurosci. 14, 965-972 (2011).
61. Lefebvre, J.L., Zhang, Y., Meister, M., Wang, X. & Sanes, J.R. γ-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 135, 4141-4151 (2008).
62. Turturro, A. et al. Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J. Gerontol. A Biol. Sci. Med. Sci. 54, B492-B501 (1999).