Lopez-Font, Inmaculada ✱; Instituto de Neurociencias de Alicante, Universidad Miguel Hernández-CSIC, Sant Joan d'Alacant, Spain b Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain
Sogorb-Esteve, Aitana ✱; Instituto de Neurociencias de Alicante, Universidad Miguel Hernández-CSIC, Sant Joan d'Alacant, Spain b Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain
Javier Torrent, Míriam ; Institut de Neurociències, Department of Biochemistry and Molecular Biology, Universitat Autònoma de Barcelona, Bellaterra, Spain / Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain c
Brinkmalm, Gunnar; Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden / Institute of Neuroscience and Physiology, University of Gothenburg, Mölndal, Sweden
Grabulosa-Herrando, Mireia; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain / Institut de Neurociències and Department of Cell Biology, Physiology and Immunology, Universitat Autònoma de Barcelona, Bellaterra, Spain
García-Lareu, Belen; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain / Institut de Neurociències, Department of Biochemistry and Molecular Biology, Universitat Autònoma de Barcelona, Bellaterra, Spain
Turon-Sans, Janina; Neuromuscular Diseases Unit, Department of Neurology, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain / Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Spain
Rojas-García, Ricardo; Neuromuscular Diseases Unit, Department of Neurology, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain / Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Spain
Lleó, Alberto; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain / Memory Unit, Neurology Department, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
Saura, Carlos A.; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain / Institut de Neurociències, Department of Biochemistry and Molecular Biology, Universitat Autònoma de Barcelona, Bellaterra, Spain
Zetterberg, Henrik; Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden / Institute of Neuroscience and Physiology, University of Gothenburg, Mölndal, Sweden / Department of Neurodegenerative Disease, Institute of Neurology, University College London, London, UK / UK Dementia Research Institute at UCL, London, UK
Blennow, Kaj; Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden / Institute of Neuroscience and Physiology, University of Gothenburg, Mölndal, Sweden
Bosch, Assumpció; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain / Institut de Neurociències, Department of Biochemistry and Molecular Biology, Universitat Autònoma de Barcelona, Bellaterra, Spain
Navarro, Xavier; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain / Institut de Neurociències and Department of Cell Biology, Physiology and Immunology, Universitat Autònoma de Barcelona, Bellaterra, Spain
Sáez-Valero, Javier; a Instituto de Neurociencias de Alicante, Universidad Miguel Hernández-CSIC, Sant Joan d'Alacant, Spain / Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Spain
Alcolea, D., et al. Amyloid precursor protein metabolism and inflammation markers in preclinical Alzheimer disease. Neurology 85 (2015), 626–633, 10.1212/WNL.0000000000001859.
Alcolea, D., et al. CSF sAPPβ, YKL-40, and neurofilament light in frontotemporal lobar degeneration. Neurology 89 (2017), 178–188, 10.1212/WNL.0000000000004088.
Ancot, F., et al. Proteolytic cleavages give receptor tyrosine kinases the gift of ubiquity. Oncogene 28 (2009), 2185–2195, 10.1038/onc.2009.88.
Balmaceda, V., et al. ApoER2 processing by presenilin-1 modulates reelin expression. FASEB J. 28 (2014), 1543–1554, 10.1096/fj.13-239350.
Bao, J., et al. Back signaling by the Nrg-1 intracellular domain. J. Cell Biol. 161 (2003), 1133–1141, 10.1083/jcb.200212085.
Baron, A.T., et al. Clinical implementation of soluble EGFR (sEGFR) as a theragnostic serum biomarker of breast, lung and ovarian cancer. IDrugs 12 (2009), 302–308.
Brooks, B.R., et al., World Federation of Neurology Research Group on Motor Neuron Diseases, El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 1 (2000), 293–299.
Carpenter, G., ErbB-4: mechanism of action and biology. Exp. Cell Res. 284 (2003), 66–77.
Chattopadhyay, S., Shubayev, V.I., MMP-9 controls Schwann cell proliferation and phenotypic remodeling via IGF-1 and ErbB receptor-mediated activation of MEK/ERK pathway. Glia 57 (2009), 1316–1325, 10.1002/glia.20851.
Chen, Y.-J., et al. ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 21818–21823, 10.1073/pnas.1010669107.
Cheng, Q.-C., et al. Ectodomain cleavage of ErbB-4: characterization of the cleavage site and m80 fragment. J. Biol. Chem. 278 (2003), 38421–38427, 10.1074/jbc.M302111200.
Chong, V.Z., et al. Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients. Schizophr. Res. 100 (2008), 270–280, 10.1016/j.schres.2007.12.474.
De Strooper, B., et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398 (1999), 518–522, 10.1038/19083.
Dols-Icardo, O., et al. Analysis of known amyotrophic lateral sclerosis and frontotemporal dementia genes reveals a substantial genetic burden in patients manifesting both diseases not carrying the C9orf72 expansion mutation. J. Neurol. Neurosurg. Psychiatry 89 (2018), 162–168, 10.1136/jnnp-2017-316820.
Falls, D.L., Neuregulins: functions, forms, and signaling strategies. Exp. Cell Res. 284 (2003), 14–30.
Gambarotta, G., et al. ErbB4 expression in neural progenitor cells (ST14A) is necessary to mediate neuregulin-1beta1-induced migration. J. Biol. Chem. 279 (2004), 48808–48816, 10.1074/jbc.M408374200.
Gambarotta, G., et al. Local delivery of the Neuregulin1 receptor ecto-domain (ecto-ErbB4) has a positive effect on regenerated nerve fiber maturation. Gene Ther. 22 (2015), 901–907, 10.1038/gt.2015.46.
Geng, F., et al. Neuregulin 1-ErbB4 signaling in the bed nucleus of the stria terminalis regulates anxiety-like behavior. Neuroscience 329 (2016), 182–192, 10.1016/j.neuroscience.2016.05.018.
Goth, C.K., et al. A systematic study of modulation of ADAM-mediated ectodomain shedding by site-specific O-glycosylation. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 14623–14628, 10.1073/pnas.1511175112.
Hansson, K.T., et al. Expanding the cerebrospinal fluid endopeptidome. Proteomics, 17, 2017, 1600384, 10.1002/pmic.201600384.
Hollmén, M., et al. Suppression of breast cancer cell growth by a monoclonal antibody targeting cleavable ErbB4 isoforms. Oncogene 28 (2009), 1309–1319, 10.1038/onc.2008.481.
Hollmén, M., et al. Proteolytic processing of ErbB4 in breast cancer. PLoS One, 7, 2012, e39413, 10.1371/journal.pone.0039413.
Homs, J., et al. Intrathecal administration of IGF-I by AAVrh10 improves sensory and motor deficits in a mouse model of diabetic neuropathy. Mol. Ther. Methods Clin. Dev., 1, 2014, 7, 10.1038/mtm.2013.7.
IIllán-Gala, I., et al. CSF sAPPβ, YKL-40, and NfL along the ALS-FTD spectrum. Neurology 91 (2018), e1619–e1628.
Junttila, T.T., et al. Erbb4 and its isoforms: selective regulation of growth factor responses by naturally occurring receptor variants. Trends Cardiovasc. Med. 10 (2000), 304–310.
Lasiene, J., et al. Neuregulin 1 confers neuroprotection in SOD1-linked amyotrophic lateral sclerosis mice via restoration of C-boutons of spinal motor neurons. Acta Neuropathol. Commun., 4, 2016, 15, 10.1186/s40478-016-0286-7.
Lee, H.-J., et al. Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J. Biol. Chem. 277 (2002), 6318–6323, 10.1074/jbc.M110371200.
Lichtenthaler, S.F., et al. Proteolytic ectodomain shedding of membrane proteins in mammals-hardware, concepts, and recent developments. EMBO J., 37, 2018 (pii: e99456).
Lillo, P., Hodges, J.R., Cognition and behaviour in motor neurone disease. Curr. Opin. Neurol. 23 (2010), 638–642, 10.1097/WCO.0b013e3283400b41.
Loeb, J.E., et al. Enhanced expression of transgenes from adeno-associated virus vectors with the woodchuck hepatitis virus posttranscriptional regulatory element: implications for gene therapy. Hum. Gene Ther. 10 (1999), 2295–2305, 10.1089/10430349950016942.
Lomen-Hoerth, C., et al. Are amyotrophic lateral sclerosis patients cognitively normal?. Neurology 60 (2003), 1094–1097.
Lynch, C.C., et al. Matrix metalloproteinase 7 mediates mammary epithelial cell tumorigenesis through the ErbB4 receptor. Cancer Res. 67 (2007), 6760–6767, 10.1158/0008-5472.CAN-07-0026.
Ma, Z., Li, Q., et al. Targeting human epidermal growth factor receptor signaling with the neuregulin's heparin-binding domain. J. Biol. Chem. 284 (2009), 32108–32115, 10.1074/jbc.M109.032714.
Määttä, J.A., et al. Proteolytic cleavage and phosphorylation of a tumor-associated ErbB4 isoform promote ligand-independent survival and cancer cell growth. Mol. Biol. Cell 17 (2006), 67–79, 10.1091/mbc.e05-05-0402.
Mancuso, R., et al. Evolution of gait abnormalities in SOD1(G93A) transgenic mice. Brain Res. 1406 (2011), 65–73, 10.1016/j.brainres.2011.06.033.
Mancuso, R., et al. Neuregulin-1 promotes functional improvement by enhancing collateral sprouting in SOD1(G93A) ALS mice and after partial muscle denervation. Neurobiol. Dis. 95 (2016), 168–178, 10.1016/j.nbd.2016.07.023.
Ni, C.Y., et al. Gamma -Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294 (2001), 2179–2181, 10.1126/science.1065412.
Pascal, D., et al. Characterization of glial cell models and in vitro manipulation of the neuregulin1/ErbB system. Biomed. Res. Int., 2014, 2014, 310215, 10.1155/2014/310215.
Phukan, J., et al. The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J. Neurol. Neurosurg. Psychiatry 83 (2012), 102–108, 10.1136/jnnp-2011-300188.
Piedra, J., et al. Development of a rapid, robust, and universal picogreen-based method to titer adeno-associated vectors. Hum. Gene Ther. Methods 26 (2015), 35–42, 10.1089/hgtb.2014.120.
Plowman, G.D., et al. Ligand-specific activation of HER4/p180erbB4, a fourth member of the epidermal growth factor receptor family. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 1746–1750.
Portelius, E., et al. Identification of novel N-terminal fragments of amyloid precursor protein in cerebrospinal fluid. Exp. Neurol. 223 (2010), 351–358, 10.1016/j.expneurol.2009.06.011.
Ringholz, G.M., et al. Prevalence and patterns of cognitive impairment in sporadic ALS. Neurology 65 (2005), 586–590, 10.1212/01.wnl.0000172911.39167.b6.
Rio, C., et al. Tumor necrosis factor-alpha-converting enzyme is required for cleavage of erbB4/HER4. J. Biol. Chem. 275 (2000), 10379–10387.
Ripps, M.E., et al. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 689–693.
Roskoski, R., The ErbB/HER family of protein-tyrosine kinases and cancer. Pharmacol. Res. 79 (2014), 34–74, 10.1016/j.phrs.2013.11.002.
Sanderson, M.P., et al. Control of ErbB signaling through metalloprotease mediated ectodomain shedding of EGF-like factors. Growth Factors 24 (2006), 121–136, 10.1080/08977190600634373.
Sardi, S.P., et al. Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127 (2006), 185–197, 10.1016/j.cell.2006.07.037.
Scarfò, I., et al. Identification of a new subclass of ALK-negative ALCL expressing aberrant levels of ERBB4 transcripts. Blood 127 (2016), 221–232, 10.1182/blood-2014-12-614503.
Schwenk, B.M., et al. TDP-43 loss of function inhibits endosomal trafficking and alters trophic signaling in neurons. EMBO J. 35 (2016), 2350–2370.
Song, F., et al. Aberrant neuregulin 1 signaling in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 71 (2012), 104–115.
Takahashi, Y., et al. ERBB4 mutations that disrupt the neuregulin-ErbB4 pathway cause amyotrophic lateral sclerosis type 19. Am. J. Hum. Genet. 93 (2013), 900–905, 10.1016/j.ajhg.2013.09.008.
Thompson, M., et al. Widespread expression of ErbB2, ErbB3 and ErbB4 in non-human primate brain. Brain Res. 1139 (2007), 95–109, 10.1016/j.brainres.2006.11.047.
Thomson, R.B., et al. N-glycosylation critically regulates function of oxalate transporter SLC26A6. Am. J. Physiol. Cell Physiol. 311 (2016), C866–C873, 10.1152/ajpcell.00171.2016.
Tian, J., et al. Down-regulation of neuregulin1/ErbB4 signaling in the hippocampus is critical for learning and memory. Mol. Neurobiol. 54 (2017), 3976–3987, 10.1007/s12035-016-9956-5.
Tidcombe, H., et al. Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 8281–8286, 10.1073/pnas.1436402100.
Tvorogov, D., et al. Somatic mutations of ErbB4: selective loss-of-function phenotype affecting signal transduction pathways in cancer. J. Biol. Chem. 27 (2009), 5582–5591.
Vecchi, M., Carpenter, G., Constitutive proteolysis of the ErbB-4 receptor tyrosine kinase by a unique, sequential mechanism. J. Cell Biol. 139 (1997), 995–1003.
Vecchi, M., et al. Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation. J. Biol. Chem. 271 (1996), 18989–18995.
Wegorzewska, I., et al. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 18809–18814.
Wen, L., et al. Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 1211–1216, 10.1073/pnas.0910302107.
Xiao, X., et al. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 72 (1998), 2224–2232.
Yu, W.-H., et al. CD44 anchors the assembly of matrilysin/MMP-7 with heparin-binding epidermal growth factor precursor and ErbB4 and regulates female reproductive organ remodeling. Genes Dev. 16 (2002), 307–323, 10.1101/gad.925702.
