Secretagogin expression in the vertebrate brainstem with focus on the noradrenergic system and implications for Alzheimer's disease.


Journal

Brain structure & function
ISSN: 1863-2661
Titre abrégé: Brain Struct Funct
Pays: Germany
ID NLM: 101282001

Informations de publication

Date de publication:
Jul 2019
Historique:
received: 20 11 2018
accepted: 03 05 2019
pubmed: 31 5 2019
medline: 3 1 2020
entrez: 31 5 2019
Statut: ppublish

Résumé

Calcium-binding proteins are widely used to distinguish neuronal subsets in the brain. This study focuses on secretagogin, an EF-hand calcium sensor, to identify distinct neuronal populations in the brainstem of several vertebrate species. By using neural tube whole mounts of mouse embryos, we show that secretagogin is already expressed during the early ontogeny of brainstem noradrenaline cells. In adults, secretagogin-expressing neurons typically populate relay centres of special senses and vegetative regulatory centres of the medulla oblongata, pons and midbrain. Notably, secretagogin expression overlapped with the brainstem column of noradrenergic cell bodies, including the locus coeruleus (A6) and the A1, A5 and A7 fields. Secretagogin expression in avian, mouse, rat and human samples showed quasi-equivalent patterns, suggesting conservation throughout vertebrate phylogeny. We found reduced secretagogin expression in locus coeruleus from subjects with Alzheimer's disease, and this reduction paralleled the loss of tyrosine hydroxylase, the enzyme rate limiting noradrenaline synthesis. Residual secretagogin immunoreactivity was confined to small submembrane domains associated with initial aberrant tau phosphorylation. In conclusion, we provide evidence that secretagogin is a useful marker to distinguish neuronal subsets in the brainstem, conserved throughout several species, and its altered expression may reflect cellular dysfunction of locus coeruleus neurons in Alzheimer's disease.

Identifiants

pubmed: 31144035
doi: 10.1007/s00429-019-01886-w
pii: 10.1007/s00429-019-01886-w
pmc: PMC6591208
doi:

Substances chimiques

Secretagogins 0
Tyrosine 3-Monooxygenase EC 1.14.16.2
Norepinephrine X4W3ENH1CV

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2061-2078

Subventions

Organisme : National Brain Research Program of Hungary
ID : 2017-1.2.1-NKP-2017-00002
Organisme : Excellence Program for Higher Education of Hungary
ID : FIKP 2018
Organisme : European Research Council
ID : 2015-AdG-695136
Pays : International

Références

J Histochem Cytochem. 1999 Jun;47(6):719-30
pubmed: 10330448
Front Neuroendocrinol. 1999 Oct;20(4):270-95
pubmed: 10569279
J Biol Chem. 2000 Aug 11;275(32):24740-51
pubmed: 10811645
Genomics. 2001 Apr 1;73(1):56-65
pubmed: 11352566
Brain Res. 2001 Dec 20;922(2):310-4
pubmed: 11743965
Int J Dev Biol. 2001 Dec;45(8):895-902
pubmed: 11804033
Exp Brain Res. 2001 Dec;141(4):460-70
pubmed: 11810140
J Chem Neuroanat. 2002 Feb;23(2):75-104
pubmed: 11841914
J Comp Neurol. 2002 Sep 30;451(4):374-91
pubmed: 12210131
J Chem Neuroanat. 2003 Jul;25(4):249-59
pubmed: 12842270
Acta Psychiatr Scand Suppl. 2003;(417):38-50
pubmed: 12950435
Acta Physiol Scand Suppl. 1964;:SUPPL 232:1-55
pubmed: 14229500
Ann Neurol. 1992 Nov;32(5):667-76
pubmed: 1449247
J Neurobiol. 2004 Sep 5;60(3):263-74
pubmed: 15281066
Nat Rev Neurosci. 2006 Feb;7(2):126-36
pubmed: 16429122
CNS Neurol Disord Drug Targets. 2006 Apr;5(2):225-32
pubmed: 16611095
Biochem J. 2007 Jan 1;401(1):353-63
pubmed: 16939418
Am J Physiol Endocrinol Metab. 2007 Jul;293(1):E347-54
pubmed: 17426113
CNS Neurol Disord Drug Targets. 2007 Jun;6(3):183-92
pubmed: 17511615
Neuropathol Appl Neurobiol. 2008 Feb;34(1):23-32
pubmed: 17961140
Brain Struct Funct. 2008 Sep;213(1-2):239-45
pubmed: 18247051
Arch Gerontol Geriatr. 1998 Nov-Dec;27(3):189-221
pubmed: 18653164
Physiol Rev. 2009 Apr;89(2):535-606
pubmed: 19342614
Curr Neuropharmacol. 2008 Sep;6(3):235-53
pubmed: 19506723
Curr Neuropharmacol. 2008 Sep;6(3):254-85
pubmed: 19506724
J Comp Neurol. 2009 Sep 20;516(3):199-212
pubmed: 19598284
Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22492-7
pubmed: 20018755
J Comp Neurol. 1991 Feb 8;304(2):198-218
pubmed: 2016417
J Neuroendocrinol. 2010 May;22(5):355-61
pubmed: 20210846
Brain Res. 2010 May 12;1330:9-19
pubmed: 20298680
Eur J Neurosci. 2010 Jun;31(12):2166-77
pubmed: 20529129
Exp Brain Res. 1990;83(1):55-66
pubmed: 2073950
Front Biosci (Landmark Ed). 2011 Jan 01;16:74-104
pubmed: 21196160
Exp Suppl. 2010;102:163-81
pubmed: 21299068
J Neural Transm (Vienna). 2011 May;118(5):737-45
pubmed: 21442354
Mol Biosyst. 2011 Jul;7(7):2196-204
pubmed: 21528130
Cell Signal. 2012 Feb;24(2):378-87
pubmed: 21982882
Neuroscience. 1990;35(2):375-475
pubmed: 2199841
Neuropathol Appl Neurobiol. 2012 Oct;38(6):582-90
pubmed: 22115520
Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6259-64
pubmed: 22474393
Nucleic Acids Res. 2012 Oct;40(19):e150
pubmed: 22753106
Acta Neuropathol. 2013 Feb;125(2):215-29
pubmed: 22961619
Curr Opin Neurol. 2012 Dec;25(6):708-14
pubmed: 23160422
Brain Res Bull. 2013 May;94:1-8
pubmed: 23376788
Neurosci Res. 2013 Sep-Oct;77(1-2):16-32
pubmed: 24008127
Brain Behav Evol. 2014;83(2):82-92
pubmed: 24776989
J Alzheimers Dis. 2015;43(4):1271-84
pubmed: 25159675
EMBO J. 2015 Jan 2;34(1):36-54
pubmed: 25430741
Front Physiol. 2014 Nov 18;5:436
pubmed: 25477821
Mol Neurobiol. 2016 Mar;53(2):1365-76
pubmed: 25633096
J Comp Neurol. 1989 Sep 15;287(3):373-92
pubmed: 2570794
Exp Gerontol. 2015 Sep;69:176-88
pubmed: 26099796
Brain Struct Funct. 2016 Sep;221(7):3803-23
pubmed: 26843217
J Chem Neuroanat. 2016 Nov;77:60-67
pubmed: 27211874
Elife. 2016 Sep 26;5:
pubmed: 27669410
Proc Natl Acad Sci U S A. 2016 Dec 27;113(52):E8472-E8481
pubmed: 27940914
Acta Neuropathol Commun. 2017 Jan 21;5(1):8
pubmed: 28109312
Neurosci Res. 2017 Jun;119:53-60
pubmed: 28193530
Proc Natl Acad Sci U S A. 2017 Mar 7;114(10):E2006-E2015
pubmed: 28223495
Curr Med Chem. 2017;24(28):3077-3103
pubmed: 28413962
EMBO J. 2017 Jul 14;36(14):2107-2125
pubmed: 28637794
Front Neuroanat. 2017 Jul 05;11:51
pubmed: 28725185
PLoS Comput Biol. 2017 Sep 22;13(9):e1005707
pubmed: 28938009
Neurosci Res. 2018 Sep;134:30-38
pubmed: 29366872
Front Aging Neurosci. 2018 Jul 09;10:199
pubmed: 30038565
EMBO J. 2018 Nov 2;37(21):
pubmed: 30209240
Front Aging Neurosci. 2018 Sep 21;10:287
pubmed: 30297999
Front Mol Biosci. 2018 Nov 20;5:99
pubmed: 30525042
Neurosci Biobehav Rev. 2019 Mar;98:135-144
pubmed: 30611797
Front Neural Circuits. 2018 Dec 21;12:106
pubmed: 30627087
Biol Psychiatry. 2019 Jul 15;86(2):87-96
pubmed: 30846302
Anat Embryol (Berl). 1987;177(1):15-28
pubmed: 3439634
Neuroscience. 1978;3(10):861-943
pubmed: 366451
J Comp Neurol. 1981 Dec 10;203(3):351-77
pubmed: 6274918
Brain Res. 1984 Jun 15;303(2):225-31
pubmed: 6611191
J Neurol Sci. 1981 Mar;49(3):419-28
pubmed: 7217992
Nat Struct Biol. 1994 Apr;1(4):239-45
pubmed: 7656053
J Comp Neurol. 1993 Aug 1;334(1):59-74
pubmed: 8408759
Neurosci Res. 1993 Jun;17(1):53-61
pubmed: 8414217
Cell Tissue Res. 1993 Feb;271(2):181-208
pubmed: 8453652
Synapse. 1996 May;23(1):28-38
pubmed: 8723133
Synapse. 1996 May;23(1):39-51
pubmed: 8723134
Prog Brain Res. 1996;107:379-402
pubmed: 8782532
J Comp Neurol. 1996 Mar 25;367(1):90-109
pubmed: 8867285
Hippocampus. 1996;6(4):347-470
pubmed: 8915675
J Chem Neuroanat. 1997 Mar;12(3):165-73
pubmed: 9141648
J Comp Neurol. 1998 Apr 6;393(2):210-30
pubmed: 9548698
Neurosci Lett. 1998 Sep 18;254(1):9-12
pubmed: 9780079

Auteurs

Péter Zahola (P)

SE NAP B Research Group of Experimental Neuroanatomy and Developmental Biology, Semmelweis University, Budapest, Hungary.
Department of Anatomy, Semmelweis University, Budapest, Hungary.

János Hanics (J)

SE NAP B Research Group of Experimental Neuroanatomy and Developmental Biology, Semmelweis University, Budapest, Hungary.
Department of Anatomy, Semmelweis University, Budapest, Hungary.

Anna Pintér (A)

Department of Anatomy, Semmelweis University, Budapest, Hungary.

Zoltán Máté (Z)

Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.

Anna Gáspárdy (A)

Department of Anatomy, Semmelweis University, Budapest, Hungary.

Zsófia Hevesi (Z)

SE NAP B Research Group of Experimental Neuroanatomy and Developmental Biology, Semmelweis University, Budapest, Hungary.
Department of Molecular Neurosciences, Center for Brain Research, Medical University of Vienna, 1090, Vienna, Austria.

Diego Echevarria (D)

Institute of Neuroscience, University of Miguel Hernandez de Elche, Alicante, Spain.

Csaba Adori (C)

Department of Neuroscience, Karolinska Institutet, Biomedicum 7D, SE-17165, Stockholm, Sweden.

Swapnali Barde (S)

Department of Neuroscience, Karolinska Institutet, Biomedicum 7D, SE-17165, Stockholm, Sweden.

Beáta Törőcsik (B)

Department of Medical Biochemistry, Semmelweis University, Budapest, Hungary.

Ferenc Erdélyi (F)

Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.

Gábor Szabó (G)

Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.

Ludwig Wagner (L)

Department of Internal Medicine III, Medical University of Vienna, Vienna, Austria.

Gabor G Kovacs (GG)

Institute of Neurology, Medical University of Vienna, Vienna, Austria.

Tomas Hökfelt (T)

Department of Neuroscience, Karolinska Institutet, Biomedicum 7D, SE-17165, Stockholm, Sweden.

Tibor Harkany (T)

Department of Molecular Neurosciences, Center for Brain Research, Medical University of Vienna, 1090, Vienna, Austria.
Department of Neuroscience, Karolinska Institutet, Biomedicum 7D, SE-17165, Stockholm, Sweden.

Alán Alpár (A)

SE NAP B Research Group of Experimental Neuroanatomy and Developmental Biology, Semmelweis University, Budapest, Hungary. Alpar.Alan@med.semmelweis-univ.hu.
Department of Anatomy, Semmelweis University, Budapest, Hungary. Alpar.Alan@med.semmelweis-univ.hu.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH