Skip to main content

Advertisement

SpringerLink
Log in

Nardilysin in human brain diseases: both friend and foe

  • Minireview Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Nardilysin is a metalloprotease that cleaves peptides, such as dynorphin-A, α-neoendorphin, and glucagon, at the N-terminus of arginine and lysine residues in dibasic moieties. It has various functionally important molecular interaction partners (heparin-binding epidermal growth factor-like growth factor, tumour necrosis factor-α-converting enzyme, neuregulin 1, beta-secretase 1, malate dehydrogenase, P42IP4/centaurin-α1, the histone H3 dimethyl Lys4, and others) and is involved in a plethora of normal brain functions. Less is known about possible implications of nardilysin for brain diseases. This review, which includes some of our own recent findings, attempts to summarize the current knowledge on possible roles of nardilysin in Alzheimer disease, Down syndrome, schizophrenia, mood disorders, alcohol abuse, heroin addiction, and cancer. We herein show that nardilysin is a Janus-faced enzyme with regard to brain pathology, being probably neuropathogenic in some diseases, but neuroprotective in others.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ACC:

Anterior cingulate cortex

AD:

Alzheimer disease

ADAM:

A disintegrin and metalloprotease

APP:

Amyloid precursor protein

BACE:

Beta-site APP cleaving enzyme

CNS:

Central nervous system

DLP:

Dorso-lateral prefrontal cortex

DS:

Down syndrome

EGF:

Epidermal growth factor

erbB:

Epidermal growth factor receptor (tyrosine kinase)

HB-EGF:

Heparin-binding epidermal growth factor-like growth factor

HXXEH:

His-Xaa-Xaa-Glu-His zinc–binding motif of the inverzincin/M16 family of metalloproteases

NRDc:

Nardilysin

NRG:

Neuregulin

PVN:

Paraventicular nucleus

PNS:

Peripheral nervous system

SON:

Supraoptic nucleus

SH-SY5Y:

Human neuroblastoma cell line

TACE:

Tumour necrosis factor-α-converting enzyme

TNF-α:

Tumour necrosis factor

References

  • Akil H, Atz M, Bunney Jr WE, Byerley W, Casey K, Choudary P, Evans SJ Jones EG, Li J, Lopez JF, Myer RM, Rollins B, Thompson RC, Tomita H, Vawter MP, Watson SJ (2006) Compositions and methods for diagnosing and treating neuropsychiatric disorders. United States Patent Application 20060257903

  • Banerjee A, Macdonald ML, Borgmann-Winter KE, Hahn CG (2010) Neuregulin 1-erbB4 pathway in schizophrenia: from genes to an interactome. Brain Res Bull 83:132–139

    Article  PubMed  CAS  Google Scholar 

  • Bataille D, Fontés G, Costes S, Longuet C, Dalle S (2006) The glucagon-miniglucagon interplay: a new level in the metabolic regulation. Ann N Y Acad Sci 1070:161–166

    Article  PubMed  CAS  Google Scholar 

  • Bekris LM, Lutz F, Li G, Galasko DR, Farlow MR, Quinn JF, Kaye JA, Leverenz JB, Tsuang DW, Montine TJ, Peskind ER, Yu CE (2012) ADAM10 expression and promoter haplotype in Alzheimer’s disease. Neurobiol Aging 33:2229-e1–2229-e9

    Article  Google Scholar 

  • Bernstein HG (2005) Proteases and Alzheimer disease: Present knowledge and emerging concepts of therapy. In: Lendeckel U, Hooper NM (eds) Proteases in the Brain. Springer, New York, pp 1–23

    Chapter  Google Scholar 

  • Bernstein HG, Bukowska A, Krell D, Bogerts B, Ansorge S, Lendeckel U (2003) Comparative localization of ADAMs 10 and 15 in human cerebral cortex normal aging, Alzheimer disease and Down syndrome. J Neurocytol 32:153–160

    Article  PubMed  CAS  Google Scholar 

  • Bernstein HG, Lendeckel U, Bertram I, Bukowska A, Kanakis D, Dobrowolny H, Stauch R, Krell D, Mawrin C, Budinger E, Keilhoff G, Bogerts B (2006) Localization of neuregulin-1alpha (heregulin-alpha) and one of its receptors, ErbB-4 tyrosine kinase, in developing and adult human brain. Brain Res Bull 69:546–559

    Article  PubMed  CAS  Google Scholar 

  • Bernstein HG, Stricker R, Dobrowolny H, Trübner K, Bogerts B, Reiser G (2007) Histochemical evidence for wide expression of the metalloendopeptidase nardilysin in human brain neurons. Neuroscience 146:1513–1523

    Article  PubMed  CAS  Google Scholar 

  • Bernstein HG, Stricker R, Lendeckel U, Bertram I, Dobrowolny H, Steiner J, Bogerts B, Reiser G (2009a) Reduced neuronal co-localisation of nardilysin and the putative alpha-secretases ADAM10 and ADAM17 in Alzheimer’s disease and Down syndrome brains. Age 31:11–25

    Article  PubMed  CAS  Google Scholar 

  • Bernstein HG, Steiner J, Bogerts B (2009b) Glial cells in schizophrenia: pathophysiological significance and possible consequences for therapy. Expert Rev Neurother 9:1059–1071

    Article  PubMed  CAS  Google Scholar 

  • Bernstein H-G, Stricker R, Bertram I, Lendeckel U, Steiner J, Bogerts B. Reiser G (2011) Nardilysin and neuregulin-1 are largely co-localised in human cortex neurons and strongly up-regulated in schizophrenia. 10th World Congress of Biological Psychiatry Prague, abstr. P 18-013

  • Bernstein HG, Stricker R, Zschiebsch K, Müller S, Dobrowolny H, Steiner J, Bogerts B, Reiser G (2013) Decreased expression of nardilysin in SH-SY5Y cells under ethanol stress and reduced density of nardilysin-expressing neurons in brains of alcoholics. J Psychiatr Res 47:343–349

    Article  PubMed  Google Scholar 

  • Bertram I, Bernstein HG, Lendeckel U, Bukowska A, Dobrowolny H, Keilhoff G, Kanakis D, Mawrin C, Bielau H, Falkai P, Bogerts B (2007) Immunohistochemical evidence for impaired neuregulin-1 signaling in the prefrontal cortex in schizophrenia and in unipolar depression. Ann N Y Acad Sci 1096:147–156

    Article  PubMed  CAS  Google Scholar 

  • Borrmann C, Stricker R, Reiser G (2011a) Retinoic acid-induced upregulation of the metalloendopeptidase nardilysin is accelerated by co-expression of the brain-specific protein p42(IP4) (centaurin α 1; ADAP1) in neuroblastoma cells. Neurochem Int 59:936–944

    Article  PubMed  CAS  Google Scholar 

  • Borrmann C, Stricker R, Reiser G (2011b) Tubulin potentiates the interaction of the metalloendopeptidase nardilysin with the neuronal scaffold protein p42IP4/centaurin-α1 (ADAP1). Cell Tissue Res 346:89–98

    Article  PubMed  CAS  Google Scholar 

  • Braak H, Del Tredici K (2012) Where, when, and in what form does sporadic Alzheimer’s disease begin? Curr Opin Neurol 25(6):708–714

    Article  PubMed  CAS  Google Scholar 

  • Chang GQ, Karatayev O, Ahsan R, Avena NM, Lee C, Lewis MJ, Hoebel BG, Leibowitz SF (2007) Effect of ethanol on hypothalamic opioid peptides, enkephalin, and dynorphin: relationship with circulating triglycerides. Alcoholism Clin Exp Res 31:249–259

    Article  CAS  Google Scholar 

  • Chang GQ, Barson JR, Karatayev O, Chang SY, Chen YW, Leibowitz SF (2010) Effect of chronic ethanol on enkephalin in the hypothalamus and extra-hypothalamic areas. Alcohol Clin Exp Res 34:761–770

    Article  PubMed  CAS  Google Scholar 

  • Chen CP, Kuhn P, Chaturvedi K, Boyadjieva N, Sarkar DK (2006) Ethanol induces apoptotic death of developing beta-endorphin neurons via suppression of cyclic adenosine monophosphate production and activation of transforming growth factor-beta1-linked apoptotic signalling. Mol Pharmacol 69:706–717

    PubMed  CAS  Google Scholar 

  • Cheon MS, Dierssen M, Kim SH, Lubec G (2008) Protein expression of BACE1, BACE2 and APP in Down syndrome brains. Amino Acids 35:339–343

    Article  PubMed  CAS  Google Scholar 

  • Chesneau V, Pierotti AR, Barré N, Creminon C, Tougard C, Cohen P (1994) Isolation and characterization of a dibasic selective metalloendopeptidase from rat testes that cleaves at the amino terminus of arginine residues. J Biol Chem 269:2056–2061

    PubMed  CAS  Google Scholar 

  • Chow KM, Oakley O, Goodman J, Ma Z, Juliano MA, Juliano L, Hersh LB (2003) Nardilysin cleaves peptides at monobasic sites. Biochemistry 42:2239–2244

    Article  PubMed  CAS  Google Scholar 

  • Chow KM, Ma Z, Cai J, Pierce WM, Hersh LB (2005) Nardilysin facilitates complex formation between mitochondrial malate dehydrogenase and citrate synthase. Biochim Biophys Acta 1723:292–301

    Article  PubMed  CAS  Google Scholar 

  • Clarke TK, Ambrose-Lanci L, Ferraro TN, Berrettini WH, Kampman KM, Dackis CA, Pettinati HM, O’Brien CP, Oslin DW, Lohoff FW (2012) Genetic association analyses of PDYN polymorphisms with heroin and cocaine addiction. Genes Brain Behav 11:415–423

    Article  PubMed  CAS  Google Scholar 

  • Coffill CR, Muller PA, Oh HK, Neo SP, Hogue KA, Cheok CF, Vousden KH, Lane DP, Blackstock WP, Gunaratne J (2012) Mutant p53 interactome identifies nardilysin as a p53R273H-specific binding partner that promotes invasion. EMBO Rep 13:638–644

    Article  PubMed  CAS  Google Scholar 

  • Colciaghi F, Marcello E, Borroni B, Zimmermann M, Caltagirone C, Cattabeni F, Padovani A, Di Luca M (2004) Platelet APP, ADAM 10 and BACE alterations in the early stages of Alzheimer disease. Neurology 62:498–501

    Article  PubMed  CAS  Google Scholar 

  • Connor CM, Guo Y, Akbarian S (2009) Cingulate white matter neurons in schizophrenia and bipolar disorder. Biol Psychiatry 66:486–493

    Article  PubMed  Google Scholar 

  • Crews FT, Nixon K (2009) Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcoholism 44:115–127

    Article  PubMed  CAS  Google Scholar 

  • Crow KE, Braggins TJ, Batt RD, Hardmann MJ (1982) Rat liver cytosolic malate dehydrogenase: purification, kinetic properties, role in control of free cytosolic NADPH concentration. Analysis of control of ethanol metabolism using computer simulation. J Biol Chem 257:14217–14225

    PubMed  CAS  Google Scholar 

  • Csuhai E, Chen G, Hersh LB (1998) Regulation of N-arginine dibasic convertase activity by amines: putative role of a novel acidic domain as an amine binding site. Biochemistry 37:3787–3794

    Article  PubMed  CAS  Google Scholar 

  • De Vries TJ, Shippenberg TS (2002) Neural systems underlying opiate addiction. J Neurosci 22:3321–3325

    PubMed  Google Scholar 

  • Draoui M, Bellincampi L, Hospital V, Cadel S, Foulon T, Prat A, Barré N, Reichert U, Melino G, Cohen P (1997) Expression and retinoid modulation of N-arginine dibasic convertase and an aminopeptidase-B in human neuroblastoma cell lines. J Neurooncol 31:99–106

    Article  PubMed  CAS  Google Scholar 

  • Endres K, Fahrenholz F (2010) Upregulation of the alpha-secretase ADAM10—risk or reason for hope? FEBS J 277:1585–1796

    Article  PubMed  CAS  Google Scholar 

  • Endres K, Fahrenholz F (2012) Regulation of α-secretase ADAM10 expression and activity. Exp Brain Res 217:343–352

    Article  PubMed  CAS  Google Scholar 

  • Fallin MD, Lasseter VK, Wolyniec PS, McGrath JA, Nestadt G, Valle D, Liang KY, Pulver AE (2003) Genomewide linkage scan for schizophrenia susceptibility loci among Ashkenazi Jewish families shows evidence of linkage on chromosome 10q22. Am J Hum Genet 73:601–611

    Article  PubMed  CAS  Google Scholar 

  • Ferriero DM, Sheldon RA, Doming J (1992) Somatostatin is altered in developing retina from ethanol-exposed rats. Neurosci Lett 147:29–32

    Article  PubMed  CAS  Google Scholar 

  • Fontés G, Lajoix AD, Bergeron F, Cadel S, Prat A, Foulon T, Gross R, Dalle S, Le-Nguyen D, Tribillac F, Bataille D (2005) Miniglucagon (MG)-generating endopeptidase, which processes glucagon into MG, is composed of N-arginine dibasic convertase and aminopeptidase B. Endocrinology 146:702–712

    Article  PubMed  Google Scholar 

  • Fumagalli P, Accarino M, Egeo A, Scartezzini P, Rappazzo G, Pizzuti A, Avvantaggiato V, Simeone A, Arrigo G, Zuffardi O, Ottolenghi S, Taramelli R (1998) Human NRD convertase: a highly conserved metalloendopeptidase expressed at specific sites during development and in adult tissues. Genomics 47:238–245

    Article  PubMed  CAS  Google Scholar 

  • Gluschankof P, Morel A, Gomez S, Nicolas P, Fahy C, Cohen P (1984) Enzymes processing somatostatin precursors: an Arg-Lys esteropeptidase from the rat brain cortex converting somatostatin-28 into somatostatin-14. Proc Natl Acad Sci USA 81:6662–6666

    Article  PubMed  CAS  Google Scholar 

  • Gough M, Parr-Sturgess C, Parkin E (2011) Zinc metalloproteinases and amyloid beta-peptide metabolism: The positive side of proteolysis in Alzheimer’s disease. Biochem Res Int Article ID 721463

  • Hiraoka Y, Ohno M, Yoshida K, Okawa K, Tomimoto H, Kita T, Nishi E (2007) Enhancement of alpha-secretase cleavage of amyloid precursor protein by a metalloendopeptidase nardilysin. J Neurochem 102:1595–1605

    Article  PubMed  CAS  Google Scholar 

  • Hooper NM (1994) Families of zinc metalloproteases. FEBS Lett 354:1–6

    Article  PubMed  CAS  Google Scholar 

  • Hooper NM, Turner AJ (2002) The search for alpha-secretase and its potential as a therapeutic approach to Alzheimer’s disease. Curr Med Chem 9:1107–1119

    Article  PubMed  CAS  Google Scholar 

  • Hospital V, Prat A (2004) Nardilysin, a basic residues specific metallopeptidase that mediates cell migration and proliferation. Protein Pept Lett 11:501–508

    Article  PubMed  CAS  Google Scholar 

  • Hospital V, Prat A, Joulie C, Chérif D, Day R, Cohen P (1997) Human and rat testis express two mRNA species encoding variants of NRD convertase, a metalloendopeptidase of the insulinase family. Biochem J 327:773–779

    PubMed  CAS  Google Scholar 

  • Hospital V, Nishi E, Klagsbrun M, Cohen P, Seidah NG, Prat A (2002) The metalloendopeptidase nardilysin (NRDc) is potently inhibited by heparin-binding epidermal growth factor-like growth factor (HB-EGF). Biochem J 367:229–238

    Article  PubMed  CAS  Google Scholar 

  • Ichimura K, Pearson DM, Kocialkowski S, Bäcklund LM, Chan R, Jones DT, Collins VP (2009) IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro Oncol 11:341–347

    Article  PubMed  CAS  Google Scholar 

  • Jin K, Mao XO, Sun Y, Xie L, Jin L, Nishi E, Klagsbrun M, Greenberg DA (2002) Heparin-binding epidermal growth factor-like growth factor: hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo. J Neurosci 22:5365–5373

    PubMed  CAS  Google Scholar 

  • Kanda K, Komekado H, Sawabu T, Ishizu S, Nakanishi Y, Nakatsuji M, Akitake-Kawano R, Ohno M, Hiraoka Y, Kawada M, Kawada K, Sakai Y, Matsumoto K, Kunichika M, Kimura T, Seno H, Nishi E, Chiba T (2012) Nardilysin and ADAM proteases promote gastric cancer cell growth by activating intrinsic cytokine signalling via enhanced ectodomain shedding of TNF-α. EMBO Mol Med 4:396–411

    Article  PubMed  CAS  Google Scholar 

  • Konradi C (2012) Methods for diagnosis and prognosis of psychotic disorders. US Patent 8,163,475,2012

  • Law AJ, Shannon Weickert C, Hyde TM, Kleinman JE, Harrison PJ (2004) Neuregulin-1 (NRG-1) mRNA and protein in the adult human brain. Neuroscience 127:125–136

    Article  PubMed  CAS  Google Scholar 

  • Lerner AJ, Gustaw-Rothenberg K, Smyth S, Casadesus G (2012) Retinoids for treatment of Alzheimer’s disease. BioFactors 38:84–89

    Article  PubMed  CAS  Google Scholar 

  • Li J, Chu M, Wang S, Chan D, Qi S, Wu M, Zhou Z, Li J, Nishi E, Qin J, Wong J (2012) Identification and characterization of nardilysin as a novel dimethyl H3K4-binding protein involved in transcriptional regulation. J Biol Chem 287:10089–10098

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler SF (2012) Alpha-secretase cleavage of the amyloid precursor protein: proteolysis regulated by signaling pathways and protein trafficking. Curr Alzheimer Res 9:165–177

    Article  PubMed  CAS  Google Scholar 

  • Lin A, Reniers RL, Wood SJ (2013) Clinical staging in severe mental disorder: evidence from neurocognition and neuroimaging. Br J Psychiatry 54:11–27

    Article  Google Scholar 

  • Ma Z, Csuhai E, Chow KM, Hersh LB (2001) Expression of the acidic stretch of nardilysin as a functional binding domain. Biochemistry 40:9447–9452

    Article  PubMed  CAS  Google Scholar 

  • Maes OC, Xu S, Yu B, Chertkow HM, Wang E, Schipper HM (2007) Transcriptional profiling of Alzheimer blood mononuclear cells by microarray. Neurobiol Aging 28:1795–1809

    Article  PubMed  CAS  Google Scholar 

  • Nash RJ, Heimburg-Molinaro J, Nash RJ (2009) Heparin binding epidermal growth factor-like growth factor reduces ethanol-induced apoptosis and differentiation in human embryonic stem cells. Growth Factors 27:362–369

    Article  PubMed  CAS  Google Scholar 

  • Nishi E (2013) Nardilysin. In: Rawlings N, Salvesen G (eds) Handbook of Proteolytic Enzymes, 3rd edn. Academic Press, NewYork, pp 1421–1426

  • Nishi E, Prat A, Hospital V, Elenius K, Klagsbrun M (2001) N-arginine dibasic convertase is a specific receptor for heparin-binding EGF-like growth factor that mediates cell migration. EMBO J 20:3342–3350

    Article  PubMed  CAS  Google Scholar 

  • Nishi E, Hiraoka Y, Yoshida K, Okawa K, Kita T (2006) Nardilysin enhances ectodomain shedding of heparin-binding epidermal growth factor-like growth factor through activation of tumor necrosis factor-alpha-converting enzyme. J Biol Chem 281:31164–31172

    Article  PubMed  CAS  Google Scholar 

  • Ohno M (2011) Nardilysin prevents amyloid plaque formation by enhancing alpha-secretase activity in vivo. Alzheimer’s Dementia J Alzheimer’s Assoc 7:S412

    Article  Google Scholar 

  • Ohno M, Hiraoka Y, Matsuoka T, Tomimoto H, Takao K, Miyakawa T, Oshima N, Kiyonari H, Kimura T, Kita T, Nishi E (2009) Nardilysin regulates axonal maturation and myelination in the central and peripheral nervous system. Nat Neurosci 12:1506–1513

    Article  PubMed  CAS  Google Scholar 

  • Ono K, Yamada M (2012) Vitamin A and Alzheimer’s disease. Geriatr Gerontol Int 12:180–188

    Article  PubMed  Google Scholar 

  • Pierotti AR, Prat A, Chesneau V, Gaudoux F, Leseney AM, Foulon T, Cohen P (1994) N-arginine dibasic convertase, a metalloendopeptidase as a prototype of a class of processing enzymes. Proc Natl Acad Sci USA 91:6078–6082

    Article  PubMed  CAS  Google Scholar 

  • Przewłocka B, Lasoń W, Przewłocki R (1992) Repeated ethanol administration decreases prodynorphin biosynthesis in the rat hippocampus. Neurosci Lett 13:195–198

    Article  Google Scholar 

  • Rawlings ND, Barrett AJ (1993) Evolutionary families of peptidases. Biochem J 290:205–218

    PubMed  CAS  Google Scholar 

  • Reiser G, Bernstein HG (2002) Neurons and plaques of Alzheimer’s disease patients highly express the neuronal membrane docking protein p42IP4/centaurin α. NeuroReport 13:2417–2419

    Article  PubMed  CAS  Google Scholar 

  • Reiser G, Bernstein HG (2004) Altered expression of protein p42IP4/centaurin-α1 in Alzheimer’s disease brains and possible interaction of p42IP4 with nucleolin. NeuroReport 15:147–148

    Article  PubMed  Google Scholar 

  • Rodd ZA, Kimpel MW, Edenberg HJ, Bell RL, Strother WN, McClintick JN, Carr LG, Liang T, McBride WJ (2008) Differential gene expression in the nucleus accumbens with ethanol self-administration in inbred alcohol-preferring rats. Pharmacol Biochem Behav 89:481–498

    Article  PubMed  CAS  Google Scholar 

  • Seidah NG, Prat A (2002) Precursor convertases in the secretory pathway, cytosol and extracellular milieu. Essays Biochem 38:79–94

    PubMed  CAS  Google Scholar 

  • Stricker R, Chow KM, Walther D, Hanck T, Hersh LB, Reiser G (2006) Interaction of the brain-specific proteinp42IP4/centaurin-alpha 1 with the peptidase nardilysin is regulated by the cognate ligands of p42IP4, PtdIns (3,4,5)P3 and Ins(1,3,4,5)P4, with stereospecificity. J Neurochem 98:343–354

    Article  PubMed  CAS  Google Scholar 

  • Sulman EP, Dumanski JP, White PS, Zhao H, Maris JM, Mathiesen T, Bruder C, Cnaan A, Brodeur GM (1998) Identification of a consistent region of allelic loss on 1p32 in meningiomas: correlation with increased morbidity. Cancer Res 58:3226–3230

    PubMed  CAS  Google Scholar 

  • Szatmari EM, Oliveira AF, Sumner EJ, Yasuda R (2013) Centaurin-α1-Ras-Elk-1 signalling at mitochondria mediates β-amyloid-induced synaptic dysfunction. J Neurosci 33:5367–5374

    Article  PubMed  Google Scholar 

  • Vincent B, Checler F (2012) α-Secretase in Alzheimer’s disease and beyond: mechanistic, regulation and function in the shedding of membrane proteins. Curr Alzheimer Res 9:140–156

    Article  PubMed  CAS  Google Scholar 

  • Wang XD, Su YA, Guo CM, Yang Y, Si TM (2008) Chronic antipsychotic drug administration alters the expression of neuregulin 1beta, ErbB2, ErbB3, and ErbB4 in the rat prefrontal cortex and hippocampus. Int J Neuropsychopharmacol 11:553–561

    PubMed  Google Scholar 

  • Wang K-S, Liu X, Zhang Q, Pan Y, Aragam N, Zeng M (2011) A meta-analysis of two genome-wide association studies identifies 3 new loci for alcohol dependence. J Psychiatr Res 45:1419–1425

    Article  PubMed  Google Scholar 

  • Zinner SH, Batanian JR (2003) Second reported patient with del(1)(p32.1p32.3) and similar clinical features suggesting a recognizable chromosomal syndrome. Am J Med Genet 122A:64–167

    Article  Google Scholar 

Download references

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Department of Psychiatry, Otto-v.-Guericke University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    H.-G. Bernstein, H. Dobrowolny, J. Steiner & B. Bogerts

  2. Institute of Neurobiochemistry, Otto-v.-Guericke University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    R. Stricker & G. Reiser

  3. Department of Psychiatry, Institute for Legal Medicine, University of Essen-Duisburg, Essen, Germany

    K. Trübner

Authors
  1. H.-G. Bernstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Stricker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Dobrowolny
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Steiner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. Bogerts
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. K. Trübner
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Reiser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H.-G. Bernstein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bernstein, HG., Stricker, R., Dobrowolny, H. et al. Nardilysin in human brain diseases: both friend and foe. Amino Acids 45, 269–278 (2013). https://doi.org/10.1007/s00726-013-1499-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-013-1499-8

Keywords

Search

Navigation