BMP9 (Bone Morphogenetic Protein 9) induces NGF as an autocrine/paracrine cholinergic trophic factor in developing basal forebrain neurons

Journal of Neuroscience

Volumn 30, Issue 24, 2010, Pages 8221-8228

  Schnitzler, Aletta C ^a   Mellott, Tiffany J ^a   Lopez Coviella, Ignacio ^a   Tallini, Yvonne N ^b   Kotlikoff, Michael I ^b   Follettie, Maximillian T ^c   Blusztajn, Jan Krzysztof ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; BONE MORPHOGENETIC PROTEIN 9; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; NERVE GROWTH FACTOR; PROCOLLAGEN C PROTEINASE; PROTEIN P75;

ANIMAL EXPERIMENT; ARTICLE; AUTOCRINE EFFECT; BRAIN NERVE CELL; CELL ISOLATION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; FOREBRAIN; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MITOSIS; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS;

ACETYLCHOLINE; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; CHOLINE O-ACETYLTRANSFERASE; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; GROWTH DIFFERENTIATION FACTOR 2; MICE; MICE, TRANSGENIC; NERVE GROWTH FACTORS; NEURONS; PREGNANCY; RECEPTOR, NERVE GROWTH FACTOR; RNA, MESSENGER; SEPTUM OF BRAIN;

EID: 77953806362     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5611-09.2010     Document Type: Article

References (49)

1. Berse B, Lopez-Coviella I, Blusztajn JK (1999) Activation of TrkA by nerve growth factor upregulates expression of the cholinergic gene locus but attenuates the response to ciliary neurotrophic growth factor. Biochem J 342:301-308.
2. Brown MA, Zhao Q, Baker KA, Naik C, Chen C, Pukac L, Singh M, Tsareva T, Parice Y, Mahoney A, Roschke V, Sanyal I, Choe S (2005) Crystal structure of BMP-9 and functional interactions with pro-region and receptors. J Biol Chem 280:25111-25118.
3. Bruns MB, MillerMW (2007) Functional nerve growth factor and trkA autocrine/paracrine circuits in adult rat cortex are revealed by episodic ethanol exposure and withdrawal. J Neurochem 100:1155-1168.
4. Canossa M, Twiss JL, Verity AN, Shooter EM (1996) p75(NGFR) and TrkA receptors collaborate to rapidly activate a p75(NGFR)-associated protein kinase. EMBO J 15:3369-3376.
5. Cassel JC, Mathis C, Majchrzak M, Moreau PH, Dalrymple-Alford JC (2008) Coexisting cholinergic and parahippocampal degeneration: a key to memory loss in dementia and a challenge for transgenic models? Neurodegener Dis 5:304-317.
6. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299-309.
7. Chen KS, Nishimura MC, Armanini MP, Crowley C, Spencer SD, Phillips HS (1997) Disruption of a single allele of the nerve growth factor gene results in atrophy of basal forebrain cholinergic neurons and memory deficits. J Neurosci 17:7288-7296. (Pubitemid 27413260)
8. Dawbarn D, Allen SJ, Semenenko FM (1988) Coexistence of choline acetyltransferase and nerve growth factor receptors in the rat basal forebrain. Neurosci Lett 94:138-144.
9. Dechant G, Barde YA (2002) The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat Neurosci 5:1131-1136.
10. Formaggio E, Fazzini F, Dalfini AC, Di Chio M, Cantù C, Decimo I, Fiorini Z, Fumagalli G, Chiamulera C (2010) Nicotine increases the expression of neurotrophin receptor tyrosine kinase receptor A in basal forebrain cholinergic neurons. Neuroscience 166:580-589.
11. Greferath U, Bennie A, Kourakis A, Barrett GL (2000) Impaired spatial learning in aged rats is associated with loss of p75-positive neurons in the basal forebrain. Neuroscience 100:363-373.
12. Hartikka J, Hefti F (1988a) Comparison of nerve growth factor's effects on development of septum, striatum, and nucleus basalis cholinergic neurons in vitro. J Neurosci Res 21:352-364.
13. Hartikka J, Hefti F (1988b) Development of septal cholinergic neurons in culture: plating density and glial cells modulate effects of NGF on survival, fiber growth, and expression of transmitter-specific enzymes. J Neurosci 8:2967-2985.
14. Heckers S, Ohtake T, Wiley RG, Lappi DA, Geula C, Mesulam MM (1994) Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J Neurosci 14:1271-1289.
15. Hollnagel A, Oehlmann V, Heymer J, Rüther U, Nordheim A (1999) Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 274:19838-19845.
16. Kanning KC, Hudson M, Amieux PS, Wiley JC, Bothwell M, Schecterson LC (2003) Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J Neurosci 23:5425-5436. (Pubitemid 36807816)
17. Koh S, Chang P, Collier TJ, Loy R (1989) Loss of NGF receptor immunoreactivity in basal forebrain neurons of aged rats: correlation with spatial memory impairment. Brain Res 498:397-404.
18. Large TH, Bodary SC, Clegg DO, Weskamp G, Otten U, Reichardt LF (1986) Nerve growth factor gene expression in the developing rat brain. Science 234:352-355. (Pubitemid 17181382)
19. Lauterborn JC, Isackson PJ, Gall CM (1991) Nerve growth factor mRNA-containing cells are distributed within regions of cholinergic neurons in the rat basal forebrain. J Comp Neurol 306:439-446.
20. Lauterborn JC, Bizon JL, Tran TM, Gall CM (1995) NGF mRNA is expressed by GABAergic but not cholinergic neurons in rat basal forebrain. J Comp Neurol 360:454-462.
21. Leanza G, Nilsson OG, Nikkhah G, Wiley RG, Björklund A (1996) Effects of neonatal lesions of the basal forebrain cholinergic system by 192 immunoglobulin G-saporin: biochemical, behavioural and morphological characterization. Neuroscience 74:119-141.
22. Li Y, Holtzman DM, Kromer LF, Kaplan DR, Chua-Couzens J, Clary DO, Knüsel B, MobleyWC (1995) Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J Neurosci 15:2888-2905.
23. Lin PY, Hinterneder JM, Rollor SR, Birren SJ (2007) Non-cell-autonomous regulation of GABAergic neuron development by neurotrophins and the p75 receptor. J Neurosci 27:12787-12796.
24. Linke R, Frotscher M (1993) Development of the rat septohippocampal projection: tracing with DiI and electron microscopy of identified growth cones. J Comp Neurol 332:69-88.
25. Liu A, Niswander LA (2005) Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev Neurosci 6:945-954.
26. López-Coviella I, Berse B, Krauss R, Thies RS, Blusztajn JK (2000) Induction and maintenance of the neuronal cholinergic phenotype in the central nervous system by BMP-9. Science 289:313-316.
27. López-Coviella I, Follettie MT, Mellott TJ, Kovacheva VP, Slack BE, Diesl V, Berse B, Thies RS, Blusztajn JK (2005) Bone morphogenetic protein 9 induces the transcriptome of basal forebrain cholinergic neurons. Proc Natl Acad Sci U S A 102:6984-6989.
28. Ló pez-Coviella I, Mellott TM, Kovacheva VP, Berse B, Slack BE, Zemelko V, Schnitzler A, Blusztajn JK (2006) Developmental pattern of expression of BMP receptors and Smads and activation of Smad1 and Smad5 by BMP9 in mouse basal forebrain. Brain Res 1088:49-56.
29. Lüesse 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.
30. Magal E, Burnham P, Varon S (1991) Effect of CNTF on low-affinity NGF receptor expression by cultured neurons from different rat brain regions. J Neurosci Res 30:560-566.
31. Massagué J (2008) TGFbeta in Cancer. Cell 134:215-230.
32. Mobley WC, Rutkowski JL, Tennekoon GI, Gemski J, Buchanan K, Johnston MV (1986) Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Brain Res 387:53-62.
33. Mufson EJ, Counts SE, Perez SE, Ginsberg SD (2008) Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert Rev Neurother 8:1703-1718.
34. Nonner D, Barrett EF, Kaplan P, Barrett JN (2001) Bone morphogenetic proteins (BMP6 and BMP7) enhance the protective effect of neurotrophins on cultured septal cholinergic neurons during hypoglycemia. J Neurochem 77:691-699.
35. Ricceri L, Hohmann C, Berger-Sweeney J (2002) Early neonatal 192 IgG saporin induces learning impairments and disrupts cortical morphogenesis in rats. Brain Res 954:160-172.
36. Saadat S, Sendtner M, Rohrer H (1989) Ciliary neurotrophic factor induces cholinergic differentiation of rat sympathetic neurons in culture. J Cell Biol 108:1807-1816.
37. Saporito MS, Carswell S (1995) High levels of synthesis and local effects of nerve growth factor in the septal region of the adult rat brain. J Neurosci 15:2280-2286.
38. Saporito MS, Brown ER, Hartpence KC, Wilcox HM, Robbins E, Vaught JL, Carswell S (1994) Systemic dexamethasone administration increases septal Trk autophosphorylation in adult rats via an induction of nerve growth factor. Mol Pharmacol 45:395-401.
39. Schnitzler AC, Lopez-Coviella I, Blusztajn JK (2008a) Differential modulation of nerve growth factor receptor (p75) and cholinergic gene expression in purified p75-expressing and non-expressing basal forebrain neurons by BMP9. Brain Res 1246:19-28.
40. Schnitzler AC, Lopez-Coviella I, Blusztajn JK (2008b) Purification and culture of nerve growth factor receptor (p75)-expressing basal forebrain cholinergic neurons. Nat Protoc 3:34-40.
41. Semkova I, Krieglstein J (1999) Ciliary neurotrophic factor enhances the expression of NGF and p75 low-affinity NGF receptor in astrocytes. Brain Res 838:184-192.
42. Shelton DL, Reichardt LF (1986) Studies on the expression of the beta nerve growth factor (NGF) gene in the central nervous system: level and regional distribution of NGF mRNA suggest that NGF functions as a trophic factor for several distinct populations of neurons. Proc Natl Acad Sci U S A 83:2714-2718.
43. Sofroniew MV, Howe CL, Mobley WC (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24:1217-1281.
44. Tallini YN, Shui B, Greene KS, Deng KY, Doran R, Fisher PJ, Zipfel W, Kotlikoff MI (2006) BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Physiol Genomics 27:391-397.
45. Tuszynski MH, Thal L, Pay M, Salmon DP, U HS, Bakay R, Patel P, Blesch A, Vahlsing HL, Ho G, Tong G, Potkin SG, Fallon J, Hansen L, Mufson EJ, Kordower JH, Gall C, Conner J (2005) A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11:551-555.
46. Upton PD, Davies RJ, Trembath RC, Morrell NW (2009) Bone morphogenetic protein (BMP) and activin type II receptors balance BMP9 signals mediated by activin receptor-like kinase-1 in human pulmonary artery endothelial cells. J Biol Chem 284:15794-15804.
47. NTR). J Biol Chem 279:4241-4249.
48. Wu H, Friedman WJ, Dreyfus CF (2004) Differential regulation of neurotrophin expression in basal forebrain astrocytes by neuronal signals. J Neurosci Res 76:76-85.
49. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA, Lin HY, Bloch KD, Peterson RT (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 4:33-41.