PTEN deletion from adult-generated dentate granule cells disrupts granule cell mossy fiber axon structure

Neurobiology of Disease

Volumn 75, Issue , 2015, Pages 142-150

  LaSarge, Candi L ^a   Santos, Victor R ^a,b   Danzer, Steve C ^a,c  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Dentate granule cells; Epilepsy; Hippocampus; Mossy fibers; MTOR; PTEN

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; BIOCYTIN; GREEN FLUORESCENT PROTEIN; LYSINE; PTEN PROTEIN, MOUSE;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GRANULE CELL; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL STRATUM LUCIDUM; MALE; MOSSY FIBER; MOUSE; NERVE FIBER GROWTH; NONHUMAN; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL SIZE; DEFICIENCY; GENETICS; HIPPOCAMPAL MOSSY FIBER; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; CA3 REGION, HIPPOCAMPAL; CELL SIZE; FEMALE; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; LYSINE; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOSSY FIBERS, HIPPOCAMPAL; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; PTEN PHOSPHOHYDROLASE;

EID: 84921829979     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.12.029     Document Type: Article

References (62)

1. Acsády L., Kamondi A., Sík A., Freund T., Buzsáki G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 1998, 18:3386-3403.
2. Ahn S., Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004, 118:505-516.
3. Ahn S., Joyner A.L. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005, 437:894-897.
4. Amaral D.G., Ishizuka N., Claiborne B. Neurons, numbers and the hippocampal network. Prog. Brain Res. 1990, 83:1-11.
5. Amaral D.G., Scharfman H.E., Lavenex P. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog. Brain Res. 2007, 163:3-22.
6. Amiri A., Cho W., Zhou J., Birnbaum S.G., Sinton C.M., McKay R.M., Parada L.F. Pten deletion in adult hippocampal neural stem/progenitor cells causes cellular abnormalities and alters neurogenesis. J. Neurosci. 2012, 32:5880-5890.
7. Bateup H.S., Takasaki K.T., Saulnier J.L., Denefrio C.L., Sabatini B.L. Loss of Tsc1 in vivo impairs hippocampal mGluR-LTD and increases excitatory synaptic function. J. Neurosci. 2011, 31:8862-8869.
8. Ben-Ari Y., Dudek F.E. Primary and secondary mechanisms of epileptogenesis in the temporal lobe: there is a before and an after. Epilepsy Curr. Am. Epilepsy Soc. 2010, 10:118-125.
9. Blaabjerg M., Zimmer J. The dentate mossy fibers: structural organization, development and plasticity. Prog. Brain Res. 2007, 163:85-107.
10. Borges K., Gearing M., McDermott D.L., Smith A.B., Almonte A.G., Wainer B.H., Dingledine R. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp. Neurol. 2003, 182:21-34.
11. Brewster A.L., Lugo J.N., Patil V.V., Lee W.L., Qian Y., Vanegas F., Anderson A.E. Rapamycin reverses status epilepticus-induced memory deficits and dendritic damage. PLoS ONE 2013, 8:e57808.
12. Buckmaster P.S., Lew F.H. Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. J. NeuroSci. 2011, 31:2337-2347.
13. Cameron M.C., Zhan R.Z., Nadler J.V. Morphologic integration of hilar ectopic granule cells into dentate gyrus circuitry in the pilocarpine model of temporal lobe epilepsy. J. Comp. Neurol. 2011, 519:2175-2192.
14. Choi Y.J., Di Nardo A., Kramvis I., Meikle L., Kwiatkowski D.J., Sahin M., He X. Tuberous sclerosis complex proteins control axon formation. Genes Dev. 2008, 22:2485-2495.
15. Claiborne B.J., Amaral D.G., Cowan W.M. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J. Comp. Neurol. 1986, 246:435-458.
16. Curia G., Longo D., Biagini G., Jones R.S.G., Avoli M. The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods 2008, 172:143-157.
17. Danzer S., He X., Loepke A., McNamara J. Structural plasticity of dentate granule cell mossy fibers during the development of limbic epilepsy. Hippocampus 2010, 20:113-124.
18. Dudek F.E., Sutula T.P. Epileptogenesis in the dentate gyrus: a critical perspective. Progress in Brain Research 2007, 163:755-773. Elsevier. E.S. Helen (Ed.).
19. Faulkner R.L., Jang M.H., Liu X.B., Duan X., Sailor K.A., Kim J.Y., Ge S., Jones E.G., Ming G.L., Song H., Cheng H.J. Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14157-14162.
20. Frotscher M. Mossy fiber synapses on glutamate decarboxylase-immunoreactive neurons: evidence for feed-forward inhibition in the CA3 region of the hippocampus. Exp. Brain Res. 1989, 75:441-445.
21. Goussakov I.V., Fink K., Elger C.E., Beck H. Metaplasticity of mossy fiber synaptic transmission involves altered release probability. J. Neurosci. 2000, 20:3434-3441.
22. Haws M.E., Jaramillo T.C., Espinosa F., A JW, Stuber G.D., Sparta D.R., Tye K.M., Russo S.J., Parada L.F., Stavarache M., Kaplitt M., Bonci A., Powell C.M. PTEN knockdown alters dendritic spine/protrusion morphology, not density. J. Comp. Neurol. 2014, 522:1171-1190.
23. Henze D.A., Wittner L., Buzsaki G. Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 2002, 5:790-795.
24. Hester M.S., Danzer S.C. Accumulation of abnormal adult-generated hippocampal granule cells predicts seizure frequency and severity. J. Neurosci. 2013, 33:8926-8936.
25. Hester M.S., Danzer S.C. Hippocampal granule cell pathology in epilepsy - a possible structural basis for comorbidities of epilepsy?. Epilepsy Behav. 2014, 38C:105-116.
26. Howell K., Hopkins N., McLoughlin P. Combined confocal microscopy and stereology: a highly efficient and unbiased approach to quantitative structural measurement in tissues. Exp. Physiol. 2002, 87:747-756.
27. Hsu D. The dentate gyrus as a filter or gate: a look back and a look ahead. Progress in Brain Research 2007, Volume 163:601-613. Elsevier. E.S. Helen (Ed.).
28. Huang X., Zhang H., Yang J., Wu J., McMahon J., Lin Y., Cao Z., Gruenthal M., Huang Y. Pharmacological inhibition of the mammalian target of rapamycin pathway suppresses acquired epilepsy. Neurobiol. Dis. 2010, 40:193-199.
29. Ishizuka N., Cowan W.M., Amaral D.G. A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J. Comp. Neurol. 1995, 362:17-45.
30. Jones R.S., Heinemann U. Synaptic and intrinsic responses of medical entorhinal cortical cells in normal and magnesium-free medium in vitro. J. Neurophysiol. 1988, 59:1476-1496.
31. Kim J.Y., Duan X., Liu C.Y., Jang M.H., Guo J.U., Pow-anpongkul N., Kang E., Song H., Ming G.L. DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 2009, 63:761-773.
32. Kwon C.H., Zhu X., Zhang J., Knoop L.L., Tharp R., Smeyne R.J., Eberhart C.G., Burger P.C., Baker S.J. Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat. Genet. 2001, 29:404-411.
33. Kwon C.H., Luikart B.W., Powell C.M., Zhou J., Matheny S.A., Zhang W., Li Y., Baker S.J., Parada L.F. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006, 50:377-388.
34. Lasarge C.L., Danzer S.C. Mechanisms regulating neuronal excitability and seizure development following mTOR pathway hyperactivation. Front. Mol. Neurosci. 2014, 7:18.
35. Lorente De Nó R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 1934, 46:113-177.
36. Luikart B.W., Schnell E., Washburn E.K., Bensen A.L., Tovar K.R., Westbrook G.L. Pten knockdown in vivo increases excitatory drive onto dentate granule cells. J. Neurosci. 2011, 31:4345-4354.
37. McAuliffe J.J., Bronson S.L., Hester M.S., Murphy B.L., Dahlquist-Topala R., Richards D.A., Danzer S.C. Altered patterning of dentate granule cell mossy fiber inputs onto CA3 pyramidal cells in limbic epilepsy. Hippocampus 2011, 21:93-107.
38. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 2005, 28:223-250.
39. Morgan R.J., Soltesz I. Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures. Proc. Natl. Acad. Sci. 2008, 105:6179-6184.
40. Murphy B.L., Hofacer R.D., Faulkner C.N., Loepke A.W., Danzer S.C. Abnormalities of granule cell dendritic structure are a prominent feature of the intrahippocampal kainic acid model of epilepsy despite reduced postinjury neurogenesis. Epilepsia 2012, 53:908-921.
41. Nakamura T., Colbert M.C., Robbins J. Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ. Res. 2006, 98:1547-1554.
42. Nek N., Schwegler H., Crusio W.E., Frotscher M. Are the fine-structural characteristics of mouse hippocampal mossy fiber synapses determined by the density of mossy fiber axons?. Neurosci. Lett. 1993, 158:75-78.
43. Parent J.M., Kron M.M. Neurogenesis and epilepsy. Jasper's Basic Mechanisms of the Epilepsies 2012, Bethesda (MD): National Center for Biotechnology Information (US). J.L. Noebels (Ed.).
44. Patel M.N., McNamara J.O. Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neuroscience 1995, 69:763-770.
45. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego.
46. Pierce J.P., Milner T.A. Parallel increases in the synaptic and surface areas of mossy fiber terminals following seizure induction. Synapse (New York, NY) 2001, 39:249-256.
47. Pun R.Y., Rolle I.J., Lasarge C.L., Hosford B.E., Rosen J.M., Uhl J.D., Schmeltzer S.N., Faulkner C., Bronson S.L., Murphy B.L., Richards D.A., Holland K.D., Danzer S.C. Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron 2012, 75:1022-1034.
48. Rushton W.A.H. A theory of the effects of fibre size in medullated nerve. J. Physiol. 1951, 115:101-122.
49. Santos V.R., de Castro O.W., Pun R.Y., Hester M.S., Murphy B.L., Loepke A.W., Garcia-Cairasco N., Danzer S.C. Contributions of mature granule cells to structural plasticity in temporal lobe epilepsy. Neuroscience 2011, 197:348-357.
50. Scharfman H.E., Pierce J.P. New insights into the role of hilar ectopic granule cells in the dentate gyrus based on quantitative anatomic analysis and three-dimensional reconstruction. Epilepsia 2012, 53(Suppl. 1):109-115.
51. Seress L., Abraham H., Paleszter M., Gallyas F. Granule cells are the main source of excitatory input to a subpopulation of GABAergic hippocampal neurons as revealed by electron microscopic double staining for zinc histochemistry and parvalbumin immunocytochemistry. Exp. Brain Res. 2001, 136:456-462.
52. Shibley H., Smith B.N. Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res. 2002, 49:109-120.
53. Singh S.P., He X., McNamara J.O., Danzer S.C. Morphological changes among hippocampal dentate granule cells exposed to early kindling-epileptogenesis. Hippocampus 2013, 23:1309-1320.
54. Sperow M., Berry R.B., Bayazitov I.T., Zhu G., Baker S.J., Zakharenko S.S. Phosphatase and tensin homologue (PTEN) regulates synaptic plasticity independently of its effect on neuronal morphology and migration. J. Physiol. 2012, 590:777-792.
55. Sutula T., Zhang P., Lynch M., Sayin U., Golarai G., Rod R. Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats. J. Comp. Neurol. 1998, 390:578-594.
56. Ting J.T., Daigle T.L., Chen Q., Feng G. Acute brain slice methods for adult and aging animals: application of targeted patch clamp analysis and optogenetics. Methods Mol. Biol. 2014, 1183:221-242.
57. Upreti C., Otero R., Partida C., Skinner F., Thakker R., Pacheco L.F., Zhou Z.Y., Maglakelidze G., Veliskova J., Velisek L., Romanovicz D., Jones T., Stanton P.K., Garrido-Sanabria E.R. Altered neurotransmitter release, vesicle recycling and presynaptic structure in the pilocarpine model of temporal lobe epilepsy. Brain 2012, 135:869-885.
58. Wong M. A critical review of mTOR inhibitors and epilepsy: from basic science to clinical trials. Expert. Rev. Neurother. 2013, 13:657-669.
59. Yamawaki R., Thind K., Buckmaster P.S. Blockade of excitatory synaptogenesis with proximal dendrites of dentate granule cells following rapamycin treatment in a mouse model of temporal lobe epilepsy. J. Comp. Neurol. 2015, 523:281-297.
60. Zeng L.-H., Rensing N.R., Wong M. The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J. Neurosci. 2009, 29:6964-6972.
61. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
62. Zhou J., Blundell J., Ogawa S., Kwon C.H., Zhang W., Sinton C., Powell C.M., Parada L.F. Pharmacological inhibition of mTORC1 suppresses anatomical, cellular, and behavioral abnormalities in neural-specific Pten knock-out mice. J. Neurosci. 2009, 29:1773-1783.