Phosphatase and tensin homolog, deleted on chromosome 10 deficiency in brain causes defects in synaptic structure, transmission and plasticity, and myelination abnormalities

Neuroscience

Volumn 151, Issue 2, 2008, Pages 476-488

  Fraser, M M ^a   Bayazitov, I T ^a   Zakharenko, S S ^a   Baker, S J ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

brain; hypertrophy; myelin; neurons; PTEN; synaptic plasticity

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL NUCLEUS; CELL STRUCTURE; CEREBELLUM; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATING DISEASE; DENDRITIC SPINE; ELECTRON MICROSCOPY; GENE; GENE DELETION; GOLGI STAIN; HETEROZYGOTE; HIPPOCAMPUS; IMAGE ANALYSIS; KNOCKOUT MOUSE; MOUSE; MYELIN SHEATH; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PTEN GENE; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN CHEMISTRY; CELL COUNT; CELL NUCLEOLUS; CHROMOSOME DELETION; CHROMOSOMES, MAMMALIAN; ELECTROPHYSIOLOGY; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MYELIN SHEATH; NEURONAL PLASTICITY; NEURONS; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 37849027524     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.10.048     Document Type: Article

References (63)

1. Ali I.U., Schriml L.M., and Dean M. Mutational spectra of PTEN/MMAC1 gene: a tumor suppressor with lipid phosphatase activity. J Natl Cancer Inst 91 (1999) 1922-1932
2. Backman S.A., Stambolic V., Suzuki A., Haight J., Elia A., Pretorius J., Tsao M.S., Shannon P., Bolon B., Ivy G.O., and Mak T.W. Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat Genet 29 (2001) 396-403
3. Bajenaru M.L., Zhu Y., Hedrick N.M., Donahoe J., Parada L.F., and Gutmann D.H. Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol Cell Biol 22 (2002) 5100-5113
4. Butler M.G., Dasouki M.J., Zhou X.P., Talebizadeh Z., Brown M., Takahashi T.N., Miles J.H., Wang C.H., Stratton R., Pilarski R., and Eng C. Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumour suppressor gene mutations. J Med Genet 42 (2005) 318-321
5. Cammalleri M., Lutjens R., Berton F., King A.R., Simpson C., Francesconi W., and Sanna P.P. Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc Natl Acad Sci U S A 100 (2003) 14368-14373
6. Chadborn N.H., Ahmed A.I., Holt M.R., Prinjha R., Dunn G.A., Jones G.E., and Eickholt B.J. PTEN couples Sema3A signalling to growth cone collapse. J Cell Sci 119 (2006) 951-957
7. Chow L.M., and Baker S.J. PTEN function in normal and neoplastic growth. Cancer Lett 241 (2006) 184-196
8. Di Cristofano A., Pesce B., Cordon-Cardo C., and Pandolfi P.P. Pten is essential for embryonic development and tumour suppression. Nat Genet 19 (1998) 348-355
9. Eng C. PTEN: one gene, many syndromes. Hum Mutat 22 (2003) 183-198
10. Eng C., and Peacocke M. PTEN and inherited hamartoma-cancer syndromes. Nat Genet 19 (1998) 223
11. Ferrer I., Marti E., Guionnet N., Bella R., Serrano T., Towse J., Conesa G., and Isamat F. Studies with the Golgi method in central gangliogliomas and dysplastic gangliocytoma of the cerebellum (Lhermitte-Duclos disease). Histol Histopathol 5 (1990) 329-336
12. Fiala J.C., Spacek J., and Harris K.M. Dendritic spine pathology: cause or consequence of neurological disorders?. Brain Res Brain Res Rev 39 (2002) 29-54
13. Fingar D.C., and Blenis J. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23 (2004) 3151-3171
14. Fraser M.M., Zhu X., Kwon C.H., Uhlmann E.J., Gutmann D.H., and Baker S.J. Pten loss causes hypertrophy and increased proliferation of astrocytes in vivo. Cancer Res 64 (2004) 7773-7779
15. Gessaga E.C. Lhermitte-Duclos disease (diffuse hypertrophy of the cerebellum). Report of two cases. Neurosurg Rev 3 (1980) 151-158
16. Goffin A., Hoefsloot L.H., Bosgoed E., Swillen A., and Fryns J.P. PTEN mutation in a family with Cowden syndrome and autism. Am J Med Genet 105 (2001) 521-524
17. Gong R., Park C.S., Abbassi N.R., and Tang S.J. Roles of glutamate receptors and the mammalian target of rapamycin (mTOR) signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. J Biol Chem 281 (2006) 18802-18815
18. Griffin R.J., Moloney A., Kelliher M., Johnston J.A., Ravid R., Dockery P., O'Connor R., and O'Neill C. Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J Neurochem 93 (2005) 105-117
19. Groszer M., Erickson R., Scripture-Adams D.D., Lesche R., Trumpp A., Zack J.A., Kornblum H.I., Liu X., and Wu H. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294 (2001) 2186-2189
20. Hair L.S., Symmans F., Powers J.M., and Carmel P. Immunohistochemistry and proliferative activity in Lhermitte-Duclos disease. Acta Neuropathol (Berl) 84 (1992) 570-573
21. Holland E.C., Li Y., Celestino J., Dai C., Schaefer L., Sawaya R.A., and Fuller G.N. Astrocytes give rise to oligodendrogliomas and astrocytomas after gene transfer of polyoma virus middle T antigen in vivo. Am J Pathol 157 (2000) 1031-1037
22. Horie Y., Suzuki A., Kataoka E., Sasaki T., Hamada K., Sasaki J., Mizuno K., Hasegawa G., Kishimoto H., Iizuka M., Naito M., Enomoto K., Watanabe S., Mak T.W., and Nakano T. Hepatocyte-specific Pten deficiency results in steatohepatitis and hepatocellular carcinomas. J Clin Invest 113 (2004) 1774-1783
23. Hu X., Hicks C.W., He W., Wong P., Macklin W.B., Trapp B.D., and Yan R. Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 9 (2006) 1520-1525
24. Ishibashi T., Dakin K.A., Stevens B., Lee P.R., Kozlov S.V., Stewart C.L., and Fields R.D. Astrocytes promote myelination in response to electrical impulses. Neuron 49 (2006) 823-832
25. Jaworski J., Spangler S., Seeburg D.P., Hoogenraad C.C., and Sheng M. Control of dendritic arborization by the phosphoinositide-3′-kinase-Akt-mammalian target of rapamycin pathway. J Neurosci 25 (2005) 11300-11312
26. Jiang H., Guo W., Liang X., and Rao Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120 (2005) 123-135
27. Kimura T., Suzuki A., Fujita Y., Yomogida K., Lomeli H., Asada N., Ikeuchi M., Nagy A., Mak T.W., and Nakano T. Conditional loss of PTEN leads to testicular teratoma and enhances embryonic germ cell production. Development 130 (2003) 1691-1700
28. Kumar V., Zhang M.X., Swank M.W., Kunz J., and Wu G.Y. Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 25 (2005) 11288-11299
29. Kwon C.H., Luikart B.W., Powell C.M., Zhou J., Matheny S.A., Zhang W., Li Y., Baker S.J., and Parada L.F. Pten regulates neuronal arborization and social interaction in mice. Neuron 50 (2006) 377-388
30. Kwon C.H., Zhu X., Zhang J., and Baker S.J. mTor is required for hypertrophy of Pten-deficient neuronal soma in vivo. Proc Natl Acad Sci U S A 100 (2003) 12923-12928
31. Kwon C.H., Zhu X., Zhang J., Knoop L.L., Tharp R., Smeyne R.J., Eberhart C.G., Burger P.C., and Baker S.J. Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat Genet 29 (2001) 404-411
32. Laurino L., Wang X.X., de la Houssaye B.A., Sosa L., Dupraz S., Caceres A., Pfenninger K.H., and Quiroga S. PI3K activation by IGF-1 is essential for the regulation of membrane expansion at the nerve growth cone. J Cell Sci 118 (2005) 3653-3662
33. Li G., Robinson G.W., Lesche R., Martinez-Diaz H., Jiang Z., Rozengurt N., Wagner K.U., Wu D.C., Lane T.F., Liu X., Hennighausen L., and Wu H. Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland. Development 129 (2002) 4159-4170
34. Marano S.R., Johnson P.C., and Spetzler R.F. Recurrent Lhermitte-Duclos disease in a child. Case report. J Neurosurg 69 (1988) 599-603
35. Marino S., Krimpenfort P., Leung C., van der Korput H.A., Trapman J., Camenisch I., Berns A., and Brandner S. PTEN is essential for cell migration but not for fate determination and tumourigenesis in the cerebellum. Development 129 (2002) 3513-3522
36. Martin-Pena A., Acebes A., Rodriguez J.R., Sorribes A., de Polavieja G.G., Fernandez-Funez P., and Ferrus A. Age-independent synaptogenesis by phosphoinositide 3 kinase. J Neurosci 26 (2006) 10199-10208
37. Menager C., Arimura N., Fukata Y., and Kaibuchi K. PIP3 is involved in neuronal polarization and axon formation. J Neurochem 89 (2004) 109-118
38. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeier C., Role L., Lai C., Schwab M.H., and Nave K.A. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304 (2004) 700-703
39. Murtie J.C., Zhou Y.X., Le T.Q., and Armstrong R.C. In vivo analysis of oligodendrocyte lineage development in postnatal FGF2 null mice. Glia 49 (2005) 542-554
40. Ogata T., Iijima S., Hoshikawa S., Miura T., Yamamoto S., Oda H., Nakamura K., and Tanaka S. Opposing extracellular signal-regulated kinase and Akt pathways control Schwann cell myelination. J Neurosci 24 (2004) 6724-6732
41. Podsypanina K., Ellenson L.H., Nemes A., Gu J., Tamura M., Yamada K.M., Cordon-Cardo C., Catoretti G., Fisher P.E., and Parsons R. Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc Natl Acad Sci U S A 96 (1999) 1563-1568
42. Raftopoulou M., Etienne-Manneville S., Self A., Nicholls S., and Hall A. Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science 303 (2004) 1179-1181
43. Reznik M., and Schoenen J. Lhermitte-Duclos disease. Acta Neuropathol (Berl) 59 (1983) 88-94
44. Rickle A., Bogdanovic N., Volkmann I., Zhou X., Pei J.J., Winblad B., and Cowburn R.F. PTEN levels in Alzheimer's disease medial temporal cortex. Neurochem Int 48 (2006) 114-123
45. Ruggero D., and Pandolfi P.P. Does the ribosome translate cancer?. Nat Rev Cancer 3 (2003) 179-192
46. Ruggero D., and Sonenberg N. The Akt of translational control. Oncogene 24 (2005) 7426-7434
47. Sanchez S., Sayas C.L., Lim F., Diaz-Nido J., Avila J., and Wandosell F. The inhibition of phosphatidylinositol-3-kinase induces neurite retraction and activates GSK3. J Neurochem 78 (2001) 468-481
48. Si K., Giustetto M., Etkin A., Hsu R., Janisiewicz A.M., Miniaci M.C., Kim J.H., Zhu H., and Kandel E.R. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell 115 (2003) 893-904
49. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21 (1999) 70-71
50. Sulis M.L., and Parsons R. PTEN: from pathology to biology. Trends Cell Biol 13 (2003) 478-483
51. Suzuki A., de la Pompa J.L., Stambolic V., Elia A.J., Sasaki T., del Barco Barrantes I., Ho A., Wakeham A., Itie A., Khoo W., Fukumoto M., and Mak T.W. High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr Biol 8 (1998) 1169-1178
52. Suzuki A., Yamaguchi M.T., Ohteki T., Sasaki T., Kaisho T., Kimura Y., Yoshida R., Wakeham A., Higuchi T., Fukumoto M., Tsubata T., Ohashi P.S., Koyasu S., Penninger J.M., Nakano T., and Mak T.W. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 14 (2001) 523-534
53. Takei N., Inamura N., Kawamura M., Namba H., Hara K., Yonezawa K., and Nawa H. Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24 (2004) 9760-9769
54. Tang S.J., Reis G., Kang H., Gingras A.C., Sonenberg N., and Schuman E.M. A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci U S A 99 (2002) 467-472
55. Tavazoie S.F., Alvarez V.A., Ridenour D.A., Kwiatkowski D.J., and Sabatini B.L. Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat Neurosci 8 (2005) 1727-1734
56. Trotman L.C., Niki M., Dotan Z.A., Koutcher J.A., Di Cristofano A., Xiao A., Khoo A.S., Roy-Burman P., Greenberg N.M., Van Dyke T., Cordon-Cardo C., and Pandolfi P.P. Pten dose dictates cancer progression in the prostate. PLoS Biol 1 (2003) E59
57. Vivanco I., and Sawyers C.L. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2 (2002) 489-501
58. Wang S., Gao J., Lei Q., Rozengurt N., Pritchard C., Jiao J., Thomas G.V., Li G., Roy-Burman P., Nelson P.S., Liu X., and Wu H. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 4 (2003) 209-221
59. Wei Q., Clarke L., Scheidenhelm D.K., Qian B., Tong A., Sabha N., Karim Z., Bock N.A., Reti R., Swoboda R., Purev E., Lavoie J.F., Bajenaru M.L., Shannon P., Herlyn D., Kaplan D., Henkelman R.M., Gutmann D.H., and Guha A. High-grade glioma formation results from postnatal pten loss or mutant epidermal growth factor receptor expression in a transgenic mouse glioma model. Cancer Res 66 (2006) 7429-7437
60. Xiao A., Wu H., Pandolfi P.P., Louis D.N., and Van Dyke T. Astrocyte inactivation of the pRb pathway predisposes mice to malignant astrocytoma development that is accelerated by PTEN mutation. Cancer Cell 1 (2002) 157-168
61. Zai L.J., and Wrathall J.R. Cell proliferation and replacement following contusive spinal cord injury. Glia 50 (2005) 247-257
62. Zeng L.H., Ouyang Y., Gazit V., Cirrito J.R., Jansen L.A., Ess K.C., Yamada K.A., Wozniak D.F., Holtzman D.M., Gutmann D.H., and Wong M. Abnormal glutamate homeostasis and impaired synaptic plasticity and learning in a mouse model of tuberous sclerosis complex. Neurobiol Dis 28 (2007) 184-196
63. Zori R.T., Marsh D.J., Graham G.E., Marliss E.B., and Eng C. Germline PTEN mutation in a family with Cowden syndrome and Bannayan-Riley-Ruvalcaba syndrome. Am J Med Genet 80 (1998) 399-402