Neuron-Targeted Caveolin-1 Improves Molecular Signaling, Plasticity, and Behavior Dependent on the Hippocampus in Adult and Aged Mice

Biological Psychiatry

Volumn 81, Issue 2, 2017, Pages 101-110

  Mandyam, Chitra D ^a,b   Schilling, Jan M ^c,d   Cui, Weihua ^c,d,e   Egawa, Junji ^c,d   Niesman, Ingrid R ^f   Kellerhals, Sarah E ^c,d   Staples, Miranda C ^b   Busija, Anna R ^c,d   Risbrough, Victoria B ^d   Posadas, Edmund ^c,d   Grogman, Grace C ^c,d   Chang, Jamie W ^c,d   Roth, David M ^c,d   Patel, Piyush M ^c,d   Patel, Hemal H ^c,d   Head, Brian P ^c,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e CAPITAL MEDICAL UNIVERSITY   (China)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CA1; Caveolin; Dentate gyrus; Membrane lipid rafts; Neuroplasticity; TrkB

Indexed keywords

CAVEOLIN 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PROTEIN; SCAFFOLD PROTEIN; SYNAPSIN; TROPOMYOSIN RELATED KINASE B RECEPTOR; UNCLASSIFIED DRUG; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CHOLERA TOXIN;

ADULT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; COGNITION; DENDRITE; FEAR; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LIPID RAFT; MALE; MEMORY; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CONDITIONED REFLEX; CYTOLOGY; GENETICS; MEMBRANE MICRODOMAIN; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; CAVEOLIN 1; CHOLERA TOXIN; CONDITIONING, CLASSICAL; DENDRITES; FEAR; HIPPOCAMPUS; MALE; MEMBRANE MICRODOMAINS; MEMORY; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; PROTEIN TRANSPORT; PYRAMIDAL CELLS; RECEPTOR, TRKB; SIGNAL TRANSDUCTION; SYNAPSINS;

EID: 84956929051     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.09.020     Document Type: Article

References (60)

1. 1 Kamiguchi, H., The region-specific activities of lipid rafts during axon growth and guidance. J Neurochem 98 (2006), 330–335.
2. 2 Fantini, J., Barrantes, F.J., Sphingolipid/cholesterol regulation of neurotransmitter receptor conformation and function. Biochim Biophys Acta 1788 (2009), 2345–2361.
3. 3 Head, B.P., Patel, H.H., Insel, P.A., Interaction of membrane/lipid rafts with the cytoskeleton: Impact on signaling and function: Membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling. Biochim Biophys Acta 1838 (2014), 532–545.
4. 4 Da Silva, J.S., Hasegawa, T., Miyagi, T., Dotti, C.G., Abad-Rodriguez, J., Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat Neurosci 8 (2005), 606–615.
5. 5 Denny, J.B., Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr Neuropharmacol 4 (2006), 293–304.
6. 6 Guirland, C., Zheng, J.Q., Membrane lipid rafts and their role in axon guidance. Adv Exp Med Biol 621 (2007), 144–155.
7. 7 Willmann, R., Pun, S., Stallmach, L., Sadasivam, G., Santos, A.F., Caroni, P., Fuhrer, C., Cholesterol and lipid microdomains stabilize the postsynapse at the neuromuscular junction. EMBO J 25 (2006), 4050–4060.
8. 8 Head, B.P., Patel, H.H., Tsutsumi, Y.M., Hu, Y., Mejia, T., Mora, R.C., et al. Caveolin-1 expression is essential for N-methyl-D-aspartate receptor-mediated Src and extracellular signal-regulated kinase 1/2 activation and protection of primary neurons from ischemic cell death. FASEB J 22 (2008), 828–840.
9. 9 Head, B.P., Hu, Y., Finley, J.C., Saldana, M.D., Bonds, J.A., Miyanohara, A., et al. Neuron-targeted caveolin-1 protein enhances signaling and promotes arborization of primary neurons. J Biol Chem 286 (2011), 33310–33321.
10. 10 Head, B.P., Patel, H.H., Roth, D.M., Murray, F., Swaney, J.S., Niesman, I.R., et al. Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components. J Biol Chem 281 (2006), 26391–26399.
11. 11 Grande-Garcia, A., del Pozo, M.A., Caveolin-1 in cell polarization and directional migration. Eur J Cell Biol 87 (2008), 641–647.
12. 12 de Kreuk, B.J., Nethe, M., Fernandez-Borja, M., Anthony, E.C., Hensbergen, P.J., Deelder, A.M., et al. The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration. J Cell Sci 124 (2011), 2375–2388.
13. 13 Del Pozo, M.A., Schwartz, M.A., Rac, membrane heterogeneity, caveolin and regulation of growth by integrins. Trends Cell Biol 17 (2007), 246–250.
14. 14 Nakai, Y., Kamiguchi, H., Migration of nerve growth cones requires detergent-resistant membranes in a spatially defined and substrate-dependent manner. J Cell Biol 159 (2002), 1097–1108.
15. 15 Niethammer, P., Delling, M., Sytnyk, V., Dityatev, A., Fukami, K., Schachner, M., Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 157 (2002), 521–532.
16. 16 Chao, M.V., Neurotrophin receptors: A window into neuronal differentiation. Neuron 9 (1992), 583–593.
17. 17 Huang, E.J., Reichardt, L.F., Neurotrophins: Roles in neuronal development and function. Annu Rev Neurosci 24 (2001), 677–736.
18. 18 Kuruvilla, R., Ye, H., Ginty, D.D., Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 27 (2000), 499–512.
19. 19 Huang, E.J., Reichardt, L.F., Trk receptors: Roles in neuronal signal transduction. Annu Rev Biochem 72 (2003), 609–642.
20. 20 Wu, C., Butz, S., Ying, Y., Anderson, R.G., Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane. J Biol Chem 272 (1997), 3554–3559.
21. 21 Huang, C.S., Zhou, J., Feng, A.K., Lynch, C.C., Klumperman, J., DeArmond, S.J., Mobley, W.C., Nerve growth factor signaling in caveolae-like domains at the plasma membrane. J Biol Chem 274 (1999), 36707–36714.
22. 22 Peiro, S., Comella, J.X., Enrich, C., Martin-Zanca, D., Rocamora, N., PC12 cells have caveolae that contain TrkA. Caveolae-disrupting drugs inhibit nerve growth factor-induced, but not epidermal growth factor-induced, MAPK phosphorylation. J Biol Chem 275 (2000), 37846–37852.
23. 23 Higuchi, H., Yamashita, T., Yoshikawa, H., Tohyama, M., PKA phosphorylates the p75 receptor and regulates its localization to lipid rafts. EMBO J 22 (2003), 1790–1800.
24. 24 Suzuki, S., Numakawa, T., Shimazu, K., Koshimizu, H., Hara, T., Hatanaka, H., et al. BDNF-induced recruitment of TrkB receptor into neuronal lipid rafts: Roles in synaptic modulation. J Cell Biol 167 (2004), 1205–1215.
25. 25 Pereira, D.B., Chao, M.V., The tyrosine kinase Fyn determines the localization of TrkB receptors in lipid rafts. J Neurosci 27 (2007), 4859–4869.
26. 26 Leal, S.L., Yassa, M.A., Perturbations of neural circuitry in aging, mild cognitive impairment, and Alzheimer's disease. Ageing Res Rev 12 (2013), 823–831.
27. 27 Fjell, A.M., McEvoy, L., Holland, D., Dale, A.M., Walhovd, K.B., Alzheimer's Disease Neuroimaging Initiative. What is normal in normal aging? Effects of aging, amyloid and Alzheimer's disease on the cerebral cortex and the hippocampus. Prog Neurobiol 117C (2014), 20–40.
28. 28 Morrison, J.H., Baxter, M.G., Synaptic health. JAMA Psychiatry 71 (2014), 835–837.
29. 29 Mesulam, M.M., Neuroplasticity failure in Alzheimer's disease: Bridging the gap between plaques and tangles. Neuron 24 (1999), 521–529.
30. 30 Rosenzweig, E.S., Barnes, C.A., Impact of aging on hippocampal function: Plasticity, network dynamics, and cognition. Prog Neurobiol 69 (2003), 143–179.
31. 31 Small, S.A., Schobel, S.A., Buxton, R.B., Witter, M.P., Barnes, C.A., A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12 (2011), 585–601.
32. 32 Hattiangady, B., Rao, M.S., Shetty, G.A., Shetty, A.K., Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Exp Neurol 195 (2005), 353–371.
33. 33 Head, B.P., Peart, J.N., Panneerselvam, M., Yokoyama, T., Pearn, M.L., Niesman, I.R., et al. Loss of caveolin-1 accelerates neurodegeneration and aging. PLoS One, 5, 2010, e15697.
34. 34 Titus, D.J., Furones, C., Kang, Y., Atkins, C.M., Age-dependent alterations in cAMP signaling contribute to synaptic plasticity deficits following traumatic brain injury. Neuroscience 231 (2013), 182–194.
35. 35 Niesman, I.R., Schilling, J.M., Shapiro, L.A., Kellerhals, S.E., Bonds, J.A., Kleschevnikov, A.M., et al. Traumatic brain injury enhances neuroinflammation and lesion volume in caveolin deficient mice. J Neuroinflammation, 11, 2014, 39.
36. 36 Kim, A., Zamora-Martinez, E.R., Edwards, S., Mandyam, C.D., Structural reorganization of pyramidal neurons in the medial prefrontal cortex of alcohol dependent rats is associated with altered glial plasticity. Brain Struct Funct 220 (2015), 1705–1720.
37. 37 Maren, S., Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: Cautions and caveats. Eur J Neurosci 28 (2008), 1661–1666.
38. 38 Gresack, J.E., Risbrough, V.B., Scott, C.N., Coste, S., Stenzel-Poore, M., Geyer, M.A., Powell, S.B., Isolation rearing-induced deficits in contextual fear learning do not require CRF(2) receptors. Behav Brain Res 209 (2010), 80–84.
39. 39 Maren, S., Phan, K.L., Liberzon, I., The contextual brain: Implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14 (2013), 417–428.
40. 40 Alto, L.T., Havton, L.A., Conner, J.M., Hollis, E.R. 2nd, Blesch, A., Tuszynski, M.H., Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat Neurosci 12 (2009), 1106–1113.
41. 41 Li, S., Overman, J.J., Katsman, D., Kozlov, S.V., Donnelly, C.J., Twiss, J.L., et al. An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke. Nat Neurosci 13 (2010), 1496–1504.
42. 42 Santiago, J.M., Torrado, A.I., Arocho, L.C., Rosas, O.R., Rodriguez, A.E., Toro, F.K., et al. Expression profile of flotillin-2 and its pathophysiological role after spinal cord injury. J Mol Neurosci 49 (2013), 347–359.
43. 43 Koch, J.C., Solis, G.P., Bodrikov, V., Michel, U., Haralampieva, D., Shypitsyna, A., et al. Upregulation of reggie-1/flotillin-2 promotes axon regeneration in the rat optic nerve in vivo and neurite growth in vitro. Neurobiol Dis 51 (2013), 168–176.
44. 44 Trovo, L., Van Veldhoven, P.P., Martin, M.G., Dotti, C.G., Sphingomyelin upregulation in mature neurons contributes to TrkB activity by Rac1 endocytosis. J Cell Sci 124 (2011), 1308–1315.
45. 45 McKerracher, L., Winton, M.J., Nogo on the go. Neuron 36 (2002), 345–348.
46. 46 Huber, A.B., Kolodkin, A.L., Ginty, D.D., Cloutier, J.F., Signaling at the growth cone: Ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26 (2003), 509–563.
47. 47 Brown, D.A., London, E., Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14 (1998), 111–136.
48. 48 Simons, K., Toomre, D., Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1 (2000), 31–39.
49. 49 Tsui-Pierchala, B.A., Encinas, M., Milbrandt, J., Johnson, E.M. Jr, Lipid rafts in neuronal signaling and function. Trends Neurosci 25 (2002), 412–417.
50. 50 Mamounas, L.A., Altar, C.A., Blue, M.E., Kaplan, D.R., Tessarollo, L., Lyons, W.E., BDNF promotes the regenerative sprouting, but not survival, of injured serotonergic axons in the adult rat brain. J Neurosci 20 (2000), 771–782.
51. 51 Guirland, C., Suzuki, S., Kojima, M., Lu, B., Zheng, J.Q., Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 42 (2004), 51–62.
52. 52 van Praag, H., Christie, B.R., Sejnowski, T.J., Gage, F.H., Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96 (1999), 13427–13431.
53. 53 Anderson, P., Morris, R., Amaral, D., Bliss, T., O'Keefe, J., The Hippocampus Book. 2007, Oxford University Press, Inc., New York.
54. 54 Henley, J.M., Wilkinson, K.A., AMPA receptor trafficking and the mechanisms underlying synaptic plasticity and cognitive aging. Dialogues Clin Neurosci 15 (2013), 11–27.
55. 55 Martin, M., Dotti, C.G., Ledesma, M.D., Brain cholesterol in normal and pathological aging. Biochim Biophys Acta 1801 (2010), 934–944.
56. 56 Ledesma, M.D., Martin, M.G., Dotti, C.G., Lipid changes in the aged brain: Effect on synaptic function and neuronal survival. Prog Lipid Res 51 (2012), 23–35.
57. 57 Jiang, L., Fang, J., Moore, D.S., Gogichaeva, N.V., Galeva, N.A., Michaelis, M.L., Zaidi, A., Age-associated changes in synaptic lipid raft proteins revealed by two-dimensional fluorescence difference gel electrophoresis. Neurobiol Aging 31 (2010), 2146–2159.
58. 58 Conte, V., Raghupathi, R., Watson, D.J., Fujimoto, S., Royo, N.C., Marklund, N., et al. TrkB gene transfer does not alter hippocampal neuronal loss and cognitive deficits following traumatic brain injury in mice. Restor Neurol Neurosci 26 (2008), 45–56.
59. 59 Remy, F., Mirrashed, F., Campbell, B., Richter, W., Mental calculation impairment in Alzheimer's disease: A functional magnetic resonance imaging study. Neurosci Lett 358 (2004), 25–28.
60. 60 Yankner, B.A., Lu, T., Loerch, P., The aging brain. Annu Rev Pathol 3 (2008), 41–66.