Chronic over-expression of TGFβ1 alters hippocampal structure and causes learning deficits

Hippocampus

Volumn 23, Issue 12, 2013, Pages 1198-1211

  Martinez Canabal, Alonso ^a,b   Wheeler, Anne L ^a,b   Sarkis, Dani ^a   Lerch, Jason P ^a,b   Lu, Wei Yang ^c   Buckwalter, Marion S ^d   Wyss Coray, Tony ^d,e   Josselyn, Sheena A ^a,b,f   Frankland, Paul W ^a,b,f  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

^d STANFORD UNIVERSITY   (United States)

^e VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cytokine; Dentate gyrus; hippocampus; Learning; Neurodegenerative disease

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA1;

ADULTHOOD; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN SIZE; CELL COUNT; CELL EXPANSION; CELL SIZE; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GRANULE CELL; HIPPOCAMPUS; LEARNING DISORDER; MALE; MORPHOLOGY; MOUSE; NERVE CELL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPATIAL LEARNING;

CYTOKINE; DENTATE GYRUS; HIPPOCAMPUS; LEARNING; NEURODEGENERATIVE DISEASE;

AGE FACTORS; ANIMALS; APOPTOSIS; ASTROCYTES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; KI-67 ANTIGEN; LEARNING DISORDERS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; REACTION TIME; SPACE PERCEPTION; SWINE; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84888134284     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22159     Document Type: Article

References (51)

1. Ageta H, Ikegami S, Miura M, Masuda M, Migishima R, Hino T, Takashima N, Murayama A, Sugino H, Setou M, Kida S, Yokoyama M, Hasegawa Y, Tsuchida K, Aosaki T, Inokuchi K. (2010). Activin plays a key role in the maintenance of long-term memory and late-LTP. Learn Mem 17:176-185.
2. Aggleton JP, Brown MW. (2006). Interleaving brain systems for episodic and recognition memory. Trends Cogn Sci 10:455-463.
3. Apelt J, Schliebs R. (2001). Beta-amyloid-induced glial expression of both pro- and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology. Brain Res 894 21-30.
4. Baker CA, Lu ZY, Zaitsev I, Manuelidis L. (1999). Microglial activation varies in different models of Creutzfeldt-Jakob disease. J Virol 73:5089-5097.
5. Brionne TC, Tesseur I, Masliah E, Wyss-Coray T. (2003). Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 40:1133-1145.
6. Buckwalter MS, Yamane M, Coleman BS, Ormerod BK, Chin JT, Palmer T, Wyss-Coray T. (2006). Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol 169:154-164.
7. Buisson A, Nicole O, Docagne F, Sartelet H, Mackenzie ET, Vivien, D. (1998). Up-regulation of a serine protease inhibitor in astrocytes mediates the neuroprotective activity of transforming growth factor beta1. FASEB J 12:1683-1691.
8. Buisson A, Lesne S, Docagne F, Ali C, Nicole O, MacKenzie ET, Vivien, D. (2003). Transforming growth factor-beta and ischemic brain injury. Cell Mol Neurobiol 23:539-550.
9. Cook RH. (1979). Memory loss in Alzheimer disease. Ann Neurol 5:105-106.
10. de Sampaio e Spohr TC, Martinez R, da Silva EF, Neto VM, Gomes FC. (2002). Neuro-glia interaction effects on GFAP gene: a novel role for transforming growth factor-beta1. Eur J Neurosci 16:2059-2069.
11. Dhandapani KM, Hadman M, De Sevilla L, Wade MF, Mahesh VB, Brann DW. (2003). Astrocyte protection of neurons: Role of transforming growth factor-beta signaling via a c-Jun-AP-1 protective pathway. J Biol Chem 278:43329-43339.
12. Docagne F, Nicole O, Marti HH, MacKenzie ET, Buisson A, Vivien D. (1999). Transforming growth factor-beta1 as a regulator of the serpins/t-PA axis in cerebral ischemia. FASEB J 13:1315-1324.
13. Dorr AE, Lerch JP, Spring S, Kabani N, Henkelman RM. (2008). High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. Neuroimage 42:60-69.
14. Dupret D, Fabre A, Dobrossy MD, Panatier A, Rodriguez JJ, Lamarque S, Lemaire V, Oliet SH, Piazza PV, Abrous DN. (2007). Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 5, e214.
15. Eichenbaum H. (2004). Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 44:109-120.
16. Genovese CR, Lazar NA, Nichols T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870-878.
17. Gundersen HJ, Jensen EB, Kieu K, Nielsen J. (1999). The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193:199-211.
18. Henrich-Noack P, Prehn JH, Krieglstein J. (1996). TGF-beta 1 protects hippocampal neurons against degeneration caused by transient global ischemia. Dose-response relationship and potential neuroprotective mechanisms. Stroke 27:1609-1614; discussion 1615.
19. Hensley K, Fedynyshyn J, Ferrell S, Floyd RA, Gordon B, Grammas P, Hamdheydari L, Mhatre M, Mou S, Pye QN, et al. (2003). Message and protein-level elevation of tumor necrosis factor alpha (TNF alpha) and TNF alpha-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis 14:74-80.
20. Hosseini-Sharifabad M, Nyengaard JR. (2007). Design-based estimation of neuronal number and individual neuronal volume in the rat hippocampus. J Neurosci Methods 162:206-214.
21. Inokuchi K. (2011). Adult neurogenesis and modulation of neural circuit function. Curr Opin Neurobiol 21:360-364.
22. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM. (2002). The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105.
23. Kim WR, Park OH, Choi S, Choi SY, Park SK, Lee KJ, Rhyu IJ, Kim H, Lee YK, Kim HT, et al. (2009). The maintenance of specific aspects of neuronal function and behavior is dependent on programmed cell death of adult-generated neurons in the dentate gyrus. Eur J Neurosci 29:1408-1421.
24. Krieglstein K, Zheng F, Unsicker K, Alzheimer C. (2011). More than being protective: functional roles for TGF-beta/activin signaling pathways at central synapses. Trends Neurosci 34:421-429.
25. Lee JW, Kim WR, Sun W, Jung MW. (2012). Disruption of dentate gyrus blocks effect of visual input on spatial firing of CA1 neurons. J Neurosci 32:12999-13003.
26. Lerch JP, Sled JG, Henkelman RM. (2011). MRI phenotyping of genetically altered mice. Meth Mol Biol 711:349-361.
27. Lindholm D, Castren E, Kiefer R, Zafra F, Thoenen H. (1992). Transforming growth factor-beta 1 in the rat brain: Increase after injury and inhibition of astrocyte proliferation. J Cell Biol 117:395-400.
28. Link J, Soderstrom M, Olsson T, Hojeberg B, Ljungdahl A, Link H. (1994). Increased transforming growth factor-beta, interleukin-4, and interferon-gamma in multiple sclerosis. Ann Neurol 36:379-386.
29. Massague J. (2012). TGFbeta signalling in context. Nat Rev Mol Cell Biol 13:616-630.
30. Meltzer LA, Yabaluri R, Deisseroth K. (2005). A role for circuit homeostasis in adult neurogenesis. Trends Neurosci 28:653-660.
31. Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T. (1994). Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett 180:147-150.
32. Mogi M, Harada M, Kondo T, Narabayashi H, Riederer P, Nagatsu T. (1995). Transforming growth factor-beta 1 levels are elevated in the striatum and in ventricular cerebrospinal fluid in Parkinson's disease. Neurosci Lett 193:129-132.
33. Nichols NR, Finch CE. (1991). Transforming growth factor-beta1 mRNA decreases in brain in response to glucocorticoid treatment of adrenalectomized rats. Mol Cell Neurosci 2:221-227.
34. Nunez G, del Peso L. (1998). Linking extracellular survival signals and the apoptotic machinery. Curr Opin Neurobiol 8:613-618.
35. Pratt BM, McPherson JM. (1997). TGF-beta in the central nervous system: potential roles in ischemic injury and neurodegenerative diseases. Cytokine Growth Factor Rev 8:267-292.
36. Reilly JF, Maher PA, Kumari VG. (1998). Regulation of astrocyte GFAP expression by TGF-beta1 and FGF-2. Glia 22:202-210.
37. Ruocco A, Nicole O, Docagne F, Ali C, Chazalviel L, Komesli S, Yablonsky F, Roussel S, MacKenzie ET, Vivien D, et al. (1999). A transforming growth factor-beta antagonist unmasks the neuroprotective role of this endogenous cytokine in excitotoxic and ischemic brain injury. J Cereb Blood Flow Metab 19:1345-1353.
38. Sousa Vde O, Romao L, Neto VM, Gomes FC. (2004). Glial fibrillary acidic protein gene promoter is differently modulated by transforming growth factor-beta 1 in astrocytes from distinct brain regions. Eur J Neurosci 19:1721-1730.
39. Teixeira CM, Pomedli SR, Maei HR, Kee N, Frankland PW. (2006). Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J Neurosci 26:7555-7564.
40. Tesseur I, Wyss-Coray T. (2006). A role for TGF-beta signaling in neurodegeneration: Evidence from genetically engineered models. Curr Alzheimer Res 3 505-513.
41. Treves A, Rolls, ET. (1994). Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374-391.
42. Treves A, Tashiro A, Witter MP, Moser EI. (2008). What is the mammalian dentate gyrus good for? Neuroscience 154:1155-1172.
43. van der Worp HB, Claus SP, Bar PR, Ramos LM, Algra A, van Gijn J, Kappelle LJ. (2001). Reproducibility of measurements of cerebral infarct volume on CT scans. Stroke 32:424-430.
44. West MJ, Coleman PD, Flood DG, Troncoso JC. (1994). Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 344:769-772.
45. West MJ, Kawas CH, Stewart WF, Rudow GL, Troncoso JC. (2004). Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol Aging 25:1205-1212.
46. Wyss-Coray T, Feng L, Masliah E, Ruppe MD, Lee HS, Toggas SM, Rockenstein EM, Mucke L. (1995). Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am J Pathol 147:53-67.
47. Wyss-Coray T, Masliah E, Mallory M, McConlogue L, Johnson-Wood K, Lin C, Mucke, L. (1997). Amyloidogenic role of cytokine TGF-beta1 in transgenic mice and in Alzheimer's disease. Nature 389:603-606.
48. Zetterberg H, Andreasen N, Blennow, K. (2004). Increased cerebrospinal fluid levels of transforming growth factor-beta1 in Alzheimer's disease. Neurosci Lett 367:194-196.
49. Zhao C, Deng W, Gage FH. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.
50. Zhu Y, Ahlemeyer B, Bauerbach E, Krieglstein J. (2001). TGF-beta1 inhibits caspase-3 activation and neuronal apoptosis in rat hippocampal cultures. Neurochem Int 38:227-235.
51. Zhu Y, Yang GY, Ahlemeyer B, Pang L, Che XM, Culmsee C, Klumpp S, Krieglstein J. (2002). Transforming growth factor-beta 1 increases bad phosphorylation and protects neurons against damage. J Neurosci 22:3898-3909.