Increased expression of axogenesis-related genes and mossy fibre length in dentate granule cells from adult HuD overexpressor mice

ASN Neuro

Volumn 3, Issue 5, 2011, Pages 259-270

  Perrone Bizzozero, Nora I ^a   Tanner, Daniel C ^b   Mounce, Joanna ^c   Bolognani, Federico ^c  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Axonal outgrowth; Dentate granule cell; Gene profiling; HuD; Post transcriptional mechanisms; RNA binding protein

Indexed keywords

BINDING PROTEIN; MESSENGER RNA; NEUROMODULIN; PROTEIN HUD; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL STRUCTURE; CONTROLLED STUDY; DENTATE GYRUS; DEVELOPMENTAL GENE; DNA MICROARRAY; EXPRESSED SEQUENCE TAG; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCATION; GENE SEQUENCE; GRANULE CELL; IN SITU HYBRIDIZATION; MOSSY FIBER; MOUSE; NERVE ELONGATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA TRANSCRIPTION; TRANSTHYRETIN GENE; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; AXONS; DENTATE GYRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; MALE; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

EID: 84857017739     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20110015     Document Type: Article

References (53)

1. Akamatsu W, Okano HJ, Osumi N, Inoue T, Nakamura S, Sakakibara S, Miura M, Matsuo N, Darnell RB, Okano H (1999) Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems. Proc Natl Acad Sci USA 96:9885-9890
2. Akamatsu W, Fujihara H, Mitsuhashi T, Yano M, Shibata S, Hayakawa Y, Okano HJ, Sakakibara S, Takano H, Takano T, Takahashi T, Noda T, Okano H (2005) The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proc Natl Acad Sci USA 102:4625-4630.
3. Akten B, Kye MJ, Hao le T, Wertz MH, Singh S, Nie D, Huang J, Merianda TT, Twiss JL, Beattie CE, Steen JA, Sahin M. (2011) Interaction of survival of motor neuron (SMN) and HuD proteins with mRNA cpg15 rescues motor neuron axonal deficits. Proc Natl Acad Sci USA 108:10337-10342.
4. Anderson KD, Morin MA, Beckel-Mitchener A, Mobarak CD, Neve RL, Furneaux HM, Burry R, Perrone-Bizzozero NI (2000) Overexpression of HuD, but not of its truncated form HuD l+ll, promotes GAP43 gene expression and neurite outgrowth in PC12 cells in the absence of nerve growth factor. J Neurochem 75:1103-1114.
5. Anderson KD, Sengupta J, Morin M, Neve RL, Valenzuela CF and Perrone-Bizzozero Nl (2001) Overexpression of HuD accelerates neurite outgrowth and increases GAP-43 mRNA expression in cortical neurons and retinoic acid-induced embryonic stem cells in vitro. Exp Neurol 168:250-258.
6. Anderson KD, Merhege MA, Morin M, Bolognani F, Perrone-Bizzozero NI (2003) Increased expression and localization of the RNA-binding protein HuD and GAP-43 mRNA to cytoplasmic granules in DRG neurons during nerve regeneration. Exp Neurol 183:100-108.
7. Bagri A, Cheng HJ, Yaron A, Pleasure SJ, Tessier-Lavigne M (2003) Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113:285-299.
8. Bakheet T, Williams BR, Khabar KS (2006) ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 34:D111-D114.
9. Balázs R, Brooksbank BWL, Patel AJ, Johnson AL, Wilson DA (1971) Incorporation of [35S]sulphate into brain constituents during development and the effects of thyroid hormone on myelination. Brain Res 30:273-293.
10. Barres BA, Lazar MA, Raff MC (1994) A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120:1097-1108.
11. Bolognani F, Merhege MA, Twiss J, Perrone-Bizzozero NI (2004) Dendritic localization of the RNA-binding protein HuD in hippocampal neurons: association with polysomes and upregulation during contextual learning. Neurosci Lett 371:152-157.
12. Bolognani F, Tanner DC, Merhege M, Deschênes-Furry J, Jasmin B, Perrone-Bizzozero NI (2006) In vivo post-transcriptional regulation of GAP-43 mRNA by overexpression of the RNA-binding protein HuD. J Neurochem 96: 790-801.
13. Bolognani F, Tanner DC, Nixon S, Okano HJ, Perrone-Bizzozero NI (2007a) Coordinated expression of HuD and GAP-43 mRNA in the hippocampus during developmental and adult plasticity. Neurochem Res 32:2142-2151.
14. Bolognani F, Qiu S, Tanner DC, Paik J, Perrone-Bizzozero NI, Weeber EJ (2007b) Associative and spatial learning and memory deficits in transgenic mice overexpressing the RNA-binding protein HuD. Neurobiol Learn Mem 87:635-643.
15. Bolognani F, Perrone-Bizzozero NI (2008) RNA-protein interactions and control of mRNA stability in neurons. J Neurosci Res 86:481-489.
16. Bolognani F, Contente-Cuomo T, Perrone-Bizzozero NI (2010) Novel recognition motifs and biological functions of the RNA-binding protein HuD revealed by genome-wide identification of its targets. Nucleic Acids Res 38:117-130.
17. Bullock WM, Bolognani F, Botta P, Valenzuela CF, Perrone-Bizzozero NI (2009) Schizophrenia-like GABAergic gene expression deficits in cerebellar Golgi cells from rats chronically exposed to low-dose phencyclidine. Neurochem Int 55:775-782.
18. Chen CY, Shyu AB (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20:465-470.
19. Clayton GH, Perez GM, Smith RL, Owens GC (1998) Expression of mRNA for the ELAV-like neural-specific RNA binding protein, HuD, during nervous system development. Brain Res Dev Brain Res 109:271-280.
20. Deschênes-Furry, J., Perrone-Bizzozero, N.I. and Jasmin, B.J. (2006) The RNA-binding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. BioEssays 28:822-833.
21. Deschênes-Furry J, Mousavi K, Bolognani F, Neve RL, Parks RJ, Perrone-Bizzozero NI, Jasmin BJ (2007) The RNA-binding protein HuD binds acetylcholinesterase mRNA in neurons and regulates its expression after axotomy. J Neurosci 27:665-675.
22. Eberwine J, Miyashiro K, Kacharmina JE, Job C (2001) Local translation of classes of mRNAs that are targeted to neuronal dendrites. Proc Natl Acad Sci USA 98:7080-7085.
23. Fallini C, Zhang H, Su Y, Silani V, Singer RH, Rossoll W, Bassell GJ (2011)The survival of motor neuron (SMN) protein interacts with the mRNA-binding protein HuD and regulates localization of poly(A) mRNA in primary motor neuron axons. J Neurosci 31:3914-3925.
24. Fernandez M, Giuliani A, Pirondi S, D'Intino G, Giardino L, Aloe L, Levi-Montalcini R, Calzà L (2004) Thyroid hormone administration enhances remyelination in chronic demyelinating inflammatory disease. Proc Natl Acad Sci USA 101:16363-16368.
25. Fleming CE, Saraiva MJ, Sousa MM (2007) Transthyretin enhances nerve regeneration. J Neurochem 103:831-839.
26. Hambardzumyan D, Sergent-Tanguy S, Thinard R, Bonnamain V, Masip M, Fabre A, Boudin H, Neveu I, Naveilhan P (2009) AUF1 and Hu proteins in the developing rat brain: implication in the proliferation and differentiation of neural progenitors. J Neurosci Res 87:1296-1309.
27. Hubers L, Valderrama-Carvajal H, Laframboise J, Timbers J, Sanchez G, Côté J (2011) HuD interacts with survival motor neuron protein and can rescue spinal muscular atrophy-like neuronal defects. Hum Mol Genet 20:553-579.
28. Kasashima K, Terashima K, Yamamoto K, Sakashita E, Sakamoto H (1999) Cytoplasmic localization is required for the mammalian ELAV-like protein HuD to induce neuronal differentiation. Genes Cells 4:667-683.
29. Keeley MB, Wood MA, Isiegas C, Stein J, Hellman K, Hannenhalli S, Abel T (2006) Differential transcriptional response to nonassociative and associative components of classical fear conditioning in the amygdala and hippocampus. Learn Mem 13:135-142.
30. Lauder JM, Mugnaini E (1980) Infrapyramidal mossy fibers in the hippocampus of the hyperthyroid rat. A light and electron microscopic study. Dev Neurosci 3:248-265.
31. Liz MA, Fleming CE, Nunes AF, Almeida MR, Mar FM, Choe Y, Craik CS, Powers JC, Bogyo M, Sousa MM (2009) Substrate specificity of transthyretin: identification of natural substrates in the nervous system. Biochem J 419:467-474.
32. Luesse HG, Roskoden T, Linke R, Otten U, Heese K, Schwegler H (1998) Modulation of mRNA expression of the neurotrophins of the nerve growth factor family and their receptors in the septum and hippocampus of rats after transient postnatal thyroxine treatment. I. Expression of nerve growth factor, brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin 4 mRNA. Exp Brain Res 119:1-8.
33. Martin KC, Zukin RS (2006) RNA trafficking and local protein synthesis in dendrites: an overview. J Neurosci 26:7131-7134.
34. Mason JL, Xuan S, Dragatsis I, Efstratiadis A, Goldman JE (2003) Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination. J Neurosci 23:7710-7718.
35. Mori-Kawakami F, Kobayashi K, Takahashi T (2003) Developmental decrease in synaptic facilitation at the mouse hippocampal mossy fibre synapse. J Physiol 553:37-48.
36. Namgung U, Routtenberg A (2000) Transcriptional and post-transcriptional regulation of a brain growth protein: regional differentiation and regeneration induction of GAP-43. Eur J Neurosci 12:3124-3136.
37. Okano HJ, Darnell RB (1997) A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17:3024-3037.
38. Palha JA, Hays MT, Morreale de Escobar G, Episkopou V, Gottesman ME, Saraiva MJ (1997) Transthyretin is not essential for thyroxine to reach the brain and other tissues in transthyretin-null mice. Am J Physiol 272:E485-E493.
39. Pascale A, Gusev PA, Amadio M, Dottorini T, Govoni S, Alkon DL, Quattrone A (2004) Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc Natl Acad Sci USA 101:1217-1222.
40. Perrone-Bizzozero N, Bolognani F (2002) Role of HuD and other RNA-binding proteins in neural development and plasticity. J Neurosci Res 68: 121-126.
41. Proper EA, Oestreicher AB, Jansen GH, Veelen CW, van Rijen PC, Gispen WH, de Graan PN (2000) Immunohistochemical characterization of mossy fibre sprouting in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 123:19-30.
42. Richardson SJ, Lemkine GF, Alfama G, Hassani Z, Demeneix BA (2007) Cell division and apoptosis in the adult neural stem cell niche are differentially affected in transthyretin null mice. Neurosci Lett 421:234-238.
43. Shaw G, Kamen R (1986) A conserved AU sequence from the 39 untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659-667.
44. Smith CL, Afroz R, Bassell GJ, Furneaux HM, Perrone-Bizzozero NI, Burry RW (2004) GAP-43 mRNA in growth cones is associated with HuD and ribosomes. J Neurobiol 61:222-235.
45. Stanić D, Malmgren H, He H, Scott L, Aperia A, Hokfelt T (2009) Developmental changes in frequency of the ciliary somatostatin receptor 3 protein. Brain Res 1249:101-112.
46. Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299-325.
47. Tanner DC, Qiu S, Bolognani F, Partridge LD, Weeber EJ, Perrone-Bizzozero NI (2008) Alterations in mossy fiber physiology and GAP-43 expression and function in transgenic mice overexpressing HuD in adult dentate granule cells. Hippocampus 18:814-823.
48. Tsai KJ, Yang CH, Lee PC, Wang WT, Chiu MJ, Shen CK (2009) Asymmetric expression patterns of brain transthyretin in normal mice and a transgenic mouse model of Alzheimer's disease. Neuroscience 159:638-646.
49. Vlasova IA, Tahoe NM, Fan D, Larsson O, Rattenbacher B, Sternjohn JR, Vasdewani J, Karypis G, Reilly CS, Bitterman PB, Bohjanen PR (2008) Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol Cell 29:263-270.
50. Wakamatsu Y, Weston JA (1997) Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development 124:3449-3460.
51. Wilusz CJ, Wormington M, Peltz SW (2001) The cap-to-tail guide to mRNA turnover. Nat Rev Mol Cell Biol 2:237-246.
52. Yoo S, van Niekerk EA, Merianda TT, Twiss JL (2010) Dynamics of axonal mRNA transport and implications for peripheral nerve regeneration. Exp Neurol 223:19-27.
53. Zoeller RT, Rovet J (2004) Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J Neuroendocrinol 16:809-818.