Nardilysin in human brain diseases: Both friend and foe

Amino Acids

Volumn 45, Issue 2, 2013, Pages 269-278

  Bernstein, H G ^a   Stricker, R ^a   Dobrowolny, H ^a   Steiner, J ^a   Bogerts, B ^a   Trubner K ^b   Reiser, G ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Alcoholism; Alzheimer disease; Brain tumour; Heroin addiction; Nardilysin; Schizophrenia

Indexed keywords

ALPHA NEOENDORPHIN; ARGININE; BETA SECRETASE 1; DYNORPHIN A; GLUCAGON; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; HISTONE H3; JANUS KINASE; LYSINE; MALATE DEHYDROGENASE; METALLOPROTEINASE; NARDILYSIN; NEU DIFFERENTIATION FACTOR; PEPTIDE; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; BRAIN DISEASE; BRAIN FUNCTION; DOWN SYNDROME; HEROIN DEPENDENCE; HUMAN; MOLECULAR INTERACTION; MOOD DISORDER; NEOPLASM; NEUROPATHOLOGY; NEUROPROTECTION; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA;

ALZHEIMER DISEASE; BRAIN DISEASES; BRAIN NEOPLASMS; DOWN SYNDROME; DYNORPHINS; ENDORPHINS; GLUCAGON; HUMANS; METALLOENDOPEPTIDASES; MOOD DISORDERS; NERVE TISSUE PROTEINS; PROTEIN PRECURSORS; SCHIZOPHRENIA; SUBSTANCE-RELATED DISORDERS;

EID: 84880846112     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-013-1499-8     Document Type: Review

References (78)

1. 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
2. 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
3. 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
4. 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
5. 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
6. 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
7. 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
8. 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
9. 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
10. Bernstein HG, Steiner J, Bogerts B (2009b) Glial cells in schizophrenia: pathophysiological significance and possible consequences for therapy. Expert Rev Neurother 9:1059-1071
11. 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
12. 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
13. 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
14. 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
15. IP4/centaurin-α1 (ADAP1). Cell Tissue Res 346:89-98
16. 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
17. 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
18. 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
19. 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. Connor CM, Guo Y, Akbarian S (2009) Cingulate white matter neurons in schizophrenia and bipolar disorder. Biol Psychiatry 66:486-493
28. Crews FT, Nixon K (2009) Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcoholism 44:115-127
29. 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
30. 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
31. De Vries TJ, Shippenberg TS (2002) Neural systems underlying opiate addiction. J Neurosci 22:3321-3325
32. 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
33. Endres K, Fahrenholz F (2010) Upregulation of the alpha-secretase ADAM10 - risk or reason for hope? FEBS J 277:1585-1796
34. Endres K, Fahrenholz F (2012) Regulation of α-secretase ADAM10 expression and activity. Exp Brain Res 217:343-352
35. 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
36. Ferriero DM, Sheldon RA, Doming J (1992) Somatostatin is altered in developing retina from ethanol-exposed rats. Neurosci Lett 147:29-32
37. 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
38. 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
39. 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
40. 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
41. 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
42. Hooper NM (1994) Families of zinc metalloproteases. FEBS Lett 354:1-6
43. 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
44. Hospital V, Prat A (2004) Nardilysin, a basic residues specific metallopeptidase that mediates cell migration and proliferation. Protein Pept Lett 11:501-508
45. 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
46. 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
47. 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
48. 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
49. 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
50. Konradi C (2012) Methods for diagnosis and prognosis of psychotic disorders. US Patent 8,163,475,2012
51. 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
52. Lerner AJ, Gustaw-Rothenberg K, Smyth S, Casadesus G (2012) Retinoids for treatment of Alzheimer's disease. BioFactors 38:84-89
53. 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
54. 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
55. Lin A, Reniers RL, Wood SJ (2013) Clinical staging in severe mental disorder: evidence from neurocognition and neuroimaging. Br J Psychiatry 54:11-27
56. 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
57. 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
58. 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
59. Nishi E (2013) Nardilysin. In: Rawlings N, Salvesen G (eds) Handbook of Proteolytic Enzymes, 3rd edn. Academic Press, NewYork, pp 1421-1426
60. 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
61. 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
62. Ohno M (2011) Nardilysin prevents amyloid plaque formation by enhancing alpha-secretase activity in vivo. Alzheimer's Dementia J Alzheimer's Assoc 7:S412
63. 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
64. Ono K, Yamada M (2012) Vitamin A and Alzheimer's disease. Geriatr Gerontol Int 12:180-188
65. 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
66. Przewłocka B, Lasoń W, Przewłocki R (1992) Repeated ethanol administration decreases prodynorphin biosynthesis in the rat hippocampus. Neurosci Lett 13:195-198
67. Rawlings ND, Barrett AJ (1993) Evolutionary families of peptidases. Biochem J 290:205-218
68. 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
69. 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
70. 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
71. Seidah NG, Prat A (2002) Precursor convertases in the secretory pathway, cytosol and extracellular milieu. Essays Biochem 38:79-94
72. 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
73. 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
74. 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
75. 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
76. 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
77. 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
78. 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