[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Springer Nature Link
Log in

Homer1 (VesL-1) in the rat esophagus: focus on myenteric plexus and neuromuscular junction

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Homer1, a scaffolding protein of the postsynaptic density (PSD), enriched at excitatory synapses is known to anchor and modulate group I metabotropic glutamate receptors (mGluRs) and different channel- and receptor-proteins. Homer proteins are expressed in neurons of different brain regions, but also in non-neuronal tissues like skeletal muscle. Occurrence and location of Homer1 and mGluR5 in myenteric plexus and neuromuscular junctions (NMJ) of rat esophagus have yet not been characterized. We located Homer1 and mGluR5 immunoreactivity (-iry) in rat esophagus and focused on myenteric neurons, intraganglionic laminar endings (IGLEs) and NMJs, using double- and triple-label immunohistochemistry and confocal laser scanning microscopy. Homer1-iry was found in a subpopulation of vesicular glutamate transporter 2 (VGLUT2) positive IGLEs and cholinergic varicosities within myenteric ganglia, but neither in nitrergic nor cholinergic myenteric neuronal cell bodies. Homer1-iry was detected in 63% of esophageal and, for comparison, in 35% of sternomastoid NMJs. Besides the location in the PSD, Homer1-iry colocalized with cholinergic markers, indicating a presynaptic location in coarse VAChT/CGRP/NF200- immunoreactive (-ir) terminals of nucleus ambiguus neurons supplying striated esophageal muscle. mGluR5-iry was found in subpopulations of myenteric neuronal cell bodies, VGLUT2-ir IGLEs and cholinergic varicosities within the myenteric neuropil and NMJs of esophagus and sternomastoid muscles. Thus, Homer1 may anchor mGluR5 at presynaptic sites of cholinergic boutons at esophageal motor endplates, in a small subpopulation of VGLUT2-ir IGLEs and cholinergic varicosities within myenteric ganglia possibly modulating Ca2+-currents and neurotransmitter release.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

αBT:

α-Bungarotoxin

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor

BSA:

Bovine serum albumin

CC:

Coiled-coil

CGRP:

Calcitonin gene-related peptide

ChAT:

Choline acetyltransferase

ENS:

Enteric nervous system

GFAP:

Glial fibrillary acidic protein

IEG:

Immediate early gene

IGLE:

Intraganglionic laminar ending

i.p.:

Intraperitoneal

IP3:

Inositol-1,4,5-triphosphate

-ir:

Immunoreactive

-iry:

Immunoreactivity

MEP:

Motor endplate

mGluR1α:

Metabotropic glutamate receptor 1α

mGluR5:

Metabotropic glutamate receptor 5

NF200:

Neurofilament 200

NFAT:

Nuclear factor of activated T-cells

nNOS:

Neuronal nitric oxide synthase

NMDA:

N-methyl-d-aspartat

NMJ:

Neuromuscular junction

ProSAP2:

Proline-rich synapse-associated protein-2

PSD:

Postsynaptic density

RyR1/2:

Ryanodine receptor type 1/2

SIBs:

Single-IGLE boutons

TBS:

Tris-buffered saline

TRPC:

Transient receptor potential cation channel

VAChT:

Vesicular acetylcholine transporter

VesL-1:

VASP/Ena-related gene upregulated during seizure and long-term potentiation

VGLUT2:

Vesicular glutamate transporter 2

References

  • Ayala R, Kett LR, Leach TL, Young AB, Dunah AW, Orlando LR (2012) Metabotropic glutamate receptor 1 (mGluR1): antibody specificity and receptor expression in cultured primary neurons. J Neurosci Methods 204(2):221–226. doi:10.1016/j.jneumeth.2011.11.014

    Article  CAS  PubMed  Google Scholar 

  • Berthoud HR, Patterson LM, Neumann F, Neuhuber WL (1997) Distribution and structure of vagal afferent intraganglionic laminar endings (IGLEs) in the rat gastrointestinal tract. Anat Embryol (Berl) 195(2):183–191

    Article  CAS  Google Scholar 

  • Bewick GS, Reid B, Richardson C, Banks RW (2005) Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic-like vesicles: evidence from the rat muscle spindle primary sensory ending. J Physiol 562(Pt 2):381–394. doi:10.1113/jphysiol.2004.074799

    Article  CAS  PubMed  Google Scholar 

  • Bhave G, Karim F, Carlton SM, Gereau RWt (2001) Peripheral group I metabotropic glutamate receptors modulate nociception in mice. Nat Neurosci 4(4):417–423. doi:10.1038/86075

    Article  CAS  PubMed  Google Scholar 

  • Böckers TM (2006) The postsynaptic density. Cell Tissue Res 326(2):409–422

    Article  Google Scholar 

  • Böckers TM, Winter C, Smalla KH, Kreutz MR, Bockmann J, Seidenbecher C, Garner CC, Gundelfinger ED (1999) Proline-rich synapse-associated proteins ProSAP1 and ProSAP2 interact with synaptic proteins of the SAPAP/GKAP family. Biochem Biophys Res Commun 264(1):247–252

    Article  Google Scholar 

  • Bockmann J, Kreutz MR, Gundelfinger ED, Böckers TM (2002) ProSAP/Shank postsynaptic density proteins interact with insulin receptor tyrosine kinase substrate IRSp53. J Neurochem 83(4):1013–1017

    Article  CAS  PubMed  Google Scholar 

  • Brakeman PR, Lanahan AA, O’Brien R, Roche K, Barnes CA, Huganir RL, Worley PF (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386(6622):284–288. doi:10.1038/386284a0

    Article  CAS  PubMed  Google Scholar 

  • Brandstätter JH, Dick O, Böckers TM (2004) The postsynaptic scaffold proteins ProSAP1/Shank2 and Homer1 are associated with glutamate receptor complexes at rat retinal synapses. J Comp Neurol 475(4):551–563

    Article  PubMed  Google Scholar 

  • Dütsch M, Eichhorn U, Wörl J, Wank M, Berthoud HR, Neuhuber WL (1998) Vagal and spinal afferent innervation of the rat esophagus: a combined retrograde tracing and immunocytochemical study with special emphasis on calcium-binding proteins. J Comp Neurol 398(2):289–307

    Article  PubMed  Google Scholar 

  • Ehrengruber M, Kato A, Inokuchi K, Hennou S (2004) Homer/vesl proteins and their roles in CNS neurons. Mol Neurobiol 29(3):213–227. doi:10.1385/MN:29:3:213

    Article  CAS  PubMed  Google Scholar 

  • Ewald P, Neuhuber WL, Raab M (2006) Vesicular glutamate transporter 1 immunoreactivity in extrinsic and intrinsic innervation of the rat esophagus. Histochem Cell Biol 125(4):377–395

    Article  CAS  PubMed  Google Scholar 

  • Feng W, Tu J, Yang T, Vernon PS, Allen PD, Worley PF, Pessah IN (2002) Homer regulates gain of ryanodine receptor type 1 channel complex. J Biol Chem 277(47):44722–44730. doi:10.1074/jbc.M207675200

    Article  CAS  PubMed  Google Scholar 

  • Foa L, Gasperini R (2009) Developmental roles for Homer: more than just a pretty scaffold. J Neurochem 108(1):1–10. doi:10.1111/j.1471-4159.2008.05726.x

    Article  CAS  PubMed  Google Scholar 

  • Giaroni C, Zanetti E, Chiaravalli AM, Albarello L, Dominioni L, Capella C, Lecchini S, Frigo G (2003) Evidence for a glutamatergic modulation of the cholinergic function in the human enteric nervous system via NMDA receptors. Eur J Pharmacol 476(1–2):63–69

    Article  CAS  PubMed  Google Scholar 

  • Hayashi MK, Tang C, Verpelli C, Narayanan R, Stearns MH, Xu R-M, Li H, Sala C, Hayashi Y (2009) The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137(1):159–171. doi:10.1016/j.cell.2009.01.050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horling L, Neuhuber WL, Raab M (2012) Pitfalls using tyramide signal amplification (TSA) in the mouse gastrointestinal tract: endogenous streptavidin-binding sites lead to false positive staining. J Neurosci Methods 204(1):124–132. doi:10.1016/j.jneumeth.2011.11.009

    Article  CAS  PubMed  Google Scholar 

  • Huang G, Kim JY, Dehoff M, Mizuno Y, Kamm KE, Worley PF, Muallem S, Zeng W (2007) Ca2+ signaling in microdomains: Homer1 Mediates The Interaction Between RyR2 and Cav1.2 to regulate excitation-contraction coupling. J Biol Chem 282(19):14283–14290. doi:10.1074/jbc.M611529200

    Article  CAS  PubMed  Google Scholar 

  • Huang GN, Huso DL, Bouyain S, Tu J, McCorkell KA, May MJ, Zhu Y, Lutz M, Collins S, Dehoff M, Kang S, Whartenby K, Powell J, Leahy D, Worley PF (2008) NFAT binding and regulation of T cell activation by the cytoplasmic scaffolding Homer proteins. Science 319(5862):476–481. doi:10.1126/science.1151227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang S-Y, Wei J, Westhoff JH, Duncan RS, Ozawa F, Volpe P, Inokuchi K, Koulen P (2003) Differential functional interaction of two Vesl/Homer protein isoforms with ryanodine receptor type 1: a novel mechanism for control of intracellular calcium signaling. Cell Calcium 34(2):177–184. doi:10.1016/S0143-4160(03)00082-4

    Article  CAS  PubMed  Google Scholar 

  • Jensen J, Lehmann A, Uvebrant A, Carlsson A, Jerndal G, Nilsson K, Frisby C, Blackshaw LA, Mattsson JP (2005) Transient lower esophageal sphincter relaxations in dogs are inhibited by a metabotropic glutamate receptor 5 antagonist. Eur J Pharmacol 519(1–2):154–157. doi:10.1016/j.ejphar.2005.07.007

    Article  CAS  PubMed  Google Scholar 

  • Kammermeier PJ, Xiao B, Tu JC, Worley PF, Ikeda SR (2000) Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels. J Neurosci 20(19):7238–7245

    CAS  PubMed  Google Scholar 

  • Kato A, Ozawa F, Saitoh Y, Fukazawa Y, Sugiyama H, Inokuchi K (1998) Novel members of the Vesl/Homer family of PDZ proteins that bind metabotropic glutamate receptors. J Biol Chem 273(37):23969–23975. doi:10.1074/jbc.273.37.23969

    Article  CAS  PubMed  Google Scholar 

  • Kennedy MB (1997) The postsynaptic density at glutamatergic synapses. Trends Neurosci 20(6):264–268

    Article  CAS  PubMed  Google Scholar 

  • Kennedy MB (2000) Signal-processing machines at the postsynaptic density. Science 290(5492):750–754. doi:10.1126/science.290.5492.750

    Article  CAS  PubMed  Google Scholar 

  • Kestler C, Neuhuber W, Raab M (2009) Distribution of P2X3 receptor immunoreactivity in myenteric ganglia of the mouse esophagus. Histochem Cell Biol 131:13–27. doi:10.1007/s00418-008-0498-4 doi

    Article  CAS  PubMed  Google Scholar 

  • Kirchgessner AL (2001) Glutamate in the enteric nervous system. Curr Opin Pharmacol 1(6):591–596

    Article  CAS  PubMed  Google Scholar 

  • Kirchgessner AL, Liu MT, Alcantara F (1997) Excitotoxicity in the enteric nervous system. J Neurosci 17(22):8804–8816

    CAS  PubMed  Google Scholar 

  • König S (2012) Lokalisation und Verteilung von GluR2/3-Rezeptorimmunität im Ösophagus der Maus. Friedrich-Alexander University of Erlangen-Nuremberg, Erlangen

    Google Scholar 

  • Kraus T, Neuhuber WL, Raab M (2004) Vesicular glutamate transporter 1 immunoreactivity in motor endplates of striated esophageal but not skeletal muscles in the mouse. Neurosci Lett 360(1–2):53–56

    Article  CAS  PubMed  Google Scholar 

  • Kraus T, Neuhuber WL, Raab M (2007) Distribution of vesicular glutamate transporter 1 (VGLUT1) in the mouse esophagus. Cell Tissue Res 329(2):205–219

    Article  CAS  PubMed  Google Scholar 

  • Liou HC, Yang RS, Fu WM (1996) Potentiation of spontaneous acetylcholine release from motor nerve terminals by glutamate in Xenopus tadpoles. Neuroscience 75(1):325–331

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Kirchgessner AL (2000) Agonist- and reflex-evoked internalization of metabotropic glutamate receptor 5 in enteric neurons. J Neurosci 20(9):3200–3205

    CAS  PubMed  Google Scholar 

  • Liu MT, Rothstein JD, Gershon MD, Kirchgessner AL (1997) Glutamatergic enteric neurons. J Neurosci 17(12):4764–4784

    CAS  PubMed  Google Scholar 

  • Mann PT, Southwell BR, Young HM, Furness JB (1997) Appositions made by axons of descending interneurons in the guinea-pig small intestine, investigated by confocal microscopy. J Chem Neuroanat 12(3):151–164

    Article  CAS  PubMed  Google Scholar 

  • Marvizón JCG, Pérez OA, Song B, Chen W, Bunnett NW, Grady EF, Todd AJ (2007) Calcitonin receptor-like receptor and receptor activity modifying protein 1 in the rat dorsal horn: localization in glutamatergic presynaptic terminals containing opioids and adrenergic α2 C receptors. Neuroscience 148(1):250–265. doi:10.1016/j.neuroscience.2007.05.036

    Article  PubMed  PubMed Central  Google Scholar 

  • McCool BA, Pin J-P, Harpold MM, Brust PF, Stauderman KA, Lovinger DM (1998) Rat group I metabotropic glutamate receptors inhibit neuronal Ca2+ channels via multiple signal transduction pathways in HEK 293 cells. J Neurophysiol 79(1):379–391

    CAS  PubMed  Google Scholar 

  • McRoberts JA, Coutinho SV, Marvizon JC, Grady EF, Tognetto M, Sengupta JN, Ennes HS, Chaban VV, Amadesi S, Creminon C, Lanthorn T, Geppetti P, Bunnett NW, Mayer EA (2001) Role of peripheral N-methyl-d-aspartate (NMDA) receptors in visceral nociception in rats. Gastroenterology 120(7):1737–1748

    Article  CAS  PubMed  Google Scholar 

  • Nepliouev I, Zhang Z-S, Stiber JA (2011) Effect of oxidative stress on Homer scaffolding proteins. PloS One 6(10):e26128. doi:10.1371/journal.pone.0026128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neuhuber WL (1987) Sensory vagal innervation of the rat esophagus and cardia: a light and electron microscopic anterograde tracing study. J Auton Nerv Syst 20(3):243–255

    Article  CAS  PubMed  Google Scholar 

  • Neuhuber WL, Clerc N (1990) Afferent innervation of the esophagus in cat and rat. In: Zenker W, Neuhuber WL. (eds) The primary afferent neuron. Plenum Press, New York, pp 93–107

    Chapter  Google Scholar 

  • Neuhuber WL, Wörl J (2016) Enteric co-innervation of striated muscle in the esophagus: still enigmatic? Histochem Cell Biol 146(6):721–735. doi:10.1007/s00418-016-1500-1

    Article  CAS  PubMed  Google Scholar 

  • Neuhuber WL, Wörl J, Berthoud HR, Conte B (1994) NADPH-diaphorase-positive nerve fibers associated with motor endplates in the rat esophagus: new evidence for co-innervation of striated muscle by enteric neurons. Cell Tissue Res 276(1):23–30

    Article  CAS  PubMed  Google Scholar 

  • Nonidez JF (1946) Afferent nerves in the intermuscular plexus of the dog’s oesophagus. J Comp Neurol 85:177–189

    Article  CAS  PubMed  Google Scholar 

  • O’Brien RJ, Lau L-F, Huganir RL (1998) Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr Opin Neurobiol 8(3):364

    Article  PubMed  Google Scholar 

  • Page AJ, Young RL, Martin CM, Umaerus M, O’Donnell TA, Cooper NJ, Coldwell JR, Hulander M, Mattsson JP, Lehmann A, Blackshaw LA (2005) Metabotropic glutamate receptors inhibit mechanosensitivity in vagal sensory neurons. Gastroenterology 128(2):402–410

    Article  CAS  PubMed  Google Scholar 

  • Pouliquin P, Pace S, Dulhunty A (2009) In vitro modulation of the cardiac ryanodine receptor activity by Homer1. Pflugers Arch Eur J Physiol 458(4):723–732. doi:10.1007/s00424-009-0664-0

    Article  CAS  Google Scholar 

  • Powley TL, Wang XY, Fox EA, Phillips RJ, Liu LWC, Huizinga JD (2008) Ultrastructural evidence for communication betweenbintramuscular vagal mechanoreceptors and interstitial cells of Cajal in the rat fundus. Neurogastroenterol Motil 20:69–79. doi:10.1111/j.1365-2982.2007.00990.x

    CAS  PubMed  Google Scholar 

  • Raab M, Neuhuber WL (2003) Vesicular glutamate transporter 2 immunoreactivity in putative vagal mechanosensor terminals of mouse and rat esophagus: indication of a local effector function? Cell Tissue Res 312(2):141–148

    CAS  PubMed  Google Scholar 

  • Raab M, Neuhuber WL (2004) Intraganglionic laminar endings and their relationships with neuronal and glial structures of myenteric ganglia in the esophagus of rat and mouse. Histochem Cell Biol 122(5):445–459

    Article  CAS  PubMed  Google Scholar 

  • Raab M, Neuhuber WL (2005) Number and distribution of intraganglionic laminar endings in the mouse esophagus as demonstrated with two different immunohistochemical markers. J Histochem Cytochem 53(8):1023–1031

    Article  CAS  PubMed  Google Scholar 

  • Raab M, Neuhuber WL (2007) Glutamatergic functions of primary afferent neurons with special emphasis on vagal afferents. Int Rev Cytol 256:223–275

    Article  CAS  PubMed  Google Scholar 

  • Raab M, Boeckers TM, Neuhuber WL (2010) Proline-rich synapse-associated protein-1 and 2 (ProSAP1/Shank2 and ProSAP2/Shank3)–scaffolding proteins are also present in postsynaptic specializations of the peripheral nervous system. Neuroscience 171(2):421–433. doi:10.1016/j.neuroscience.2010.08.041

    Article  CAS  PubMed  Google Scholar 

  • Roche KW, Tu JC, Petralia RS, Xiao B, Wenthold RJ, Worley PF (1999) Homer 1b regulates the trafficking of group I metabotropic glutamate receptors. J Biol Chem 274(36):25953–25957. doi:10.1074/jbc.274.36.25953

    Article  CAS  PubMed  Google Scholar 

  • Rodrigo J, Hernandez J, Vidal MA, Pedrosa JA (1975) Vegetative innervation of the esophagus. II. Intraganglionic laminar endings. Acta Anat 92:79–100

    Article  CAS  PubMed  Google Scholar 

  • Rodrigo J, de Felipe J, Robles-Chillida EM, Perez Anton JA, Mayo I, Gomez A (1982) Sensory vagal nature and anatomical access paths to esophagus laminar nerve endings in myenteric ganglia. Determination by surgical degeneration methods. Acta Anat (Basel) 112 (1):47–57

    Article  CAS  Google Scholar 

  • Rohof WO, Aronica E, Beaumont H, Troost D, Boeckxstaens GE (2012) Localization of mGluR5, GABAB, GABAA, and cannabinoid receptors on the vago-vagal reflex pathway responsible for transient lower esophageal sphincter relaxation in humans: an immunohistochemical study. Neurogastroenterol Motil 24(4):383–173. doi:10.1111/j.1365-2982.2011.01868.x

    Article  CAS  PubMed  Google Scholar 

  • Salanova M, Bortoloso E, Schiffl G, Gutsmann M, Belavý DL, Felsenberg D, Furlan S, Volpe P, Blottner D (2011) Expression and regulation of Homer in human skeletal muscle during neuromuscular junction adaptation to disuse and exercise. FASEB J 25(12):4312–4325. doi:10.1096/fj.11-186049

    Article  CAS  PubMed  Google Scholar 

  • Salanova M, Volpe P, Blottner D (2013) Homer protein family regulation in skeletal muscle and neuromuscular adaptation. IUBMB Life 65(9):769–776. doi:10.1002/iub.1198

    Article  CAS  PubMed  Google Scholar 

  • Sandonà D, Tibaldo E, Volpe P (2000) Evidence for the presence of two Homer 1 transcripts in skeletal and cardiac muscles. Biochem Biophys Res Commun 279(2):348–353. doi:10.1006/bbrc.2000.3948

    Article  PubMed  Google Scholar 

  • Sang Q, Young HM (1998) The origin and development of the vagal and spinal innervation of the external muscle of the mouse esophagus. Brain Res 809(2):253–268

    Article  CAS  PubMed  Google Scholar 

  • Schwartz NE, Alford S (2000) Physiological activation of presynaptic metabotropic glutamate receptors increases intracellular calcium and glutamate release. J Neurophysiol 84(1):415–427

    CAS  PubMed  Google Scholar 

  • Shiraishi-Yamaguchi Y, Furuichi T (2007) The Homer family proteins. Genome Biol 8(2):206–206. doi:10.1186/gb-2007-8-2-206

    Article  PubMed  PubMed Central  Google Scholar 

  • Soloviev M, Ciruela F, Chan W-Y, McIlhinney RAJ (2000a) Molecular characterisation of two structurally distinct groups of human homers, generated by extensive alternative splicing1. J Mol Biol 295(5):1185–1200. doi:10.1006/jmbi.1999.3436

    Article  CAS  PubMed  Google Scholar 

  • Soloviev MM, Ciruela F, Chan W-Y, McIlhinney RAJ (2000b) Mouse brain and muscle tissues constitutively express high levels of Homer proteins. Eur J Biochem 267(3):634–639. doi:10.1046/j.1432-1327.2000.01078.x

    Article  CAS  PubMed  Google Scholar 

  • Stiber JA, Tabatabaei N, Hawkins AF, Hawke T, Worley PF, Williams RS, Rosenberg P (2005) Homer modulates NFAT-dependent signaling during muscle differentiation. Dev Biol 287(2):213–224. doi:10.1016/j.ydbio.2005.06.030

    Article  CAS  PubMed  Google Scholar 

  • Stiber JA, Zhang ZS, Burch J, Eu JP, Zhang S, Truskey GA, Seth M, Yamaguchi N, Meissner G, Shah R, Worley PF, Williams RS, Rosenberg PB (2008) Mice lacking Homer 1 exhibit a skeletal myopathy characterized by abnormal transient receptor potential channel activity. Mol Cell Biol 28(8):2637–2647. doi:10.1128/MCB.01601-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao-Cheng J-H, Thein S, Yang Y, Reese TS, Gallant PE (2014) Homer is concentrated at the postsynaptic density and does not redistribute after acute synaptic stimulation. Neuroscience 266:80–90. doi:10.1016/j.neuroscience.2014.01.066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong Q, Kirchgessner AL (2003) Localization and function of metabotropic glutamate receptor 8 in the enteric nervous system. Am J Physiol Gastrointest Liver Physiol 285(5):G992–G1003

    Article  CAS  PubMed  Google Scholar 

  • Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K, Li M, Linden DJ, Worley PF (1998) Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21(4):717–726. doi:10.1016/S0896-6273(00)80589-9

    Article  CAS  PubMed  Google Scholar 

  • Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, Aakalu VK, Lanahan AA, Sheng M, Worley PF (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23(3):583–592

    Article  CAS  PubMed  Google Scholar 

  • Ulus IH, Buyukuysal RL, Wurtman RJ (1992) N-methyl-d-aspartate increases acetylcholine release from rat striatum and cortex: its effect is augmented by choline. J Pharmacol Exp Ther 261(3):1122–1128

    CAS  PubMed  Google Scholar 

  • Vyskocil F (2003) Early postdenervation depolarization is controlled by acetylcholine and glutamate via nitric oxide regulation of the chloride transporter. Neurochem Res 28(3–4):575–585

    Article  CAS  PubMed  Google Scholar 

  • Ward CW, Feng W, Tu J, Pessah IN, Worley PK, Schneider MF (2004) Homer protein increases activation of Ca2 + sparks in permeabilized skeletal muscle. J Biol Chem 279(7):5781–5787

    Article  CAS  PubMed  Google Scholar 

  • Westhoff JH, Hwang S-Y, Scott Duncan R, Ozawa F, Volpe P, Inokuchi K, Koulen P (2003) Vesl/Homer proteins regulate ryanodine receptor type 2 function and intracellular calcium signaling. Cell Calcium 34(3):261–269. doi:10.1016/S0143-4160(03)00112-X

    Article  CAS  PubMed  Google Scholar 

  • Wiley JW, Lu YX, Owyang C (1991) Evidence for a glutamatergic neural pathway in the myenteric plexus. Am J Physiol 261(4 Pt 1):G693–G700

    CAS  PubMed  Google Scholar 

  • Wörl J, Neuhuber WL (2005) Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after. Histochem Cell Biol 123(2):117–130

    Article  PubMed  Google Scholar 

  • Wörl J, Mayer B, Neuhuber WL (1994) Nitrergic innervation of the rat esophagus: focus on motor endplates. J Auton Nerv Syst 49(3):227–233

    Article  PubMed  Google Scholar 

  • Worley PF, Zeng W, Huang G, Kim JY, Shin DM, Kim MS, Yuan JP, Kiselyov K, Muallem S (2007) Homer proteins in Ca(2+) signaling by excitable and non-excitable cells. Cell Calcium 42(4–5):363–371. doi:10.1016/j.ceca.2007.05.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao B, Tu JC, Petralia RS, Yuan JP, Doan A, Breder CD, Ruggiero A, Lanahan AA, Wenthold RJ, Worley PF (1998) Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21(4):707–716

    Article  CAS  PubMed  Google Scholar 

  • Yuan JP, Kiselyov K, Shin DM, Chen J, Shcheynikov N, Kang SH, Dehoff MH, Schwarz MK, Seeburg PH, Muallem S, Worley PF (2003) Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 114(6):777–789. doi:10.1016/S0092-8674(03)00716-5

    Article  CAS  PubMed  Google Scholar 

  • Yuan JP, Lee KP, Hong JH, Muallem S (2012) The closing and opening of TRPC channels by Homer1 and STIM1. Acta Physiol (Oxf) 204(2):238–247. doi:10.1111/j.1748-1716.2011.02319.x

    Article  CAS  Google Scholar 

  • Zagorodnyuk VP, Brookes SJ (2000) Transduction sites of vagal mechanoreceptors in the guinea pig esophagus. J Neurosci 20(16):6249–6255

    CAS  PubMed  Google Scholar 

  • Zagorodnyuk VP, Chen BN, Brookes SJ (2001) Intraganglionic laminar endings are mechano-transduction sites of vagal tension receptors in the guinea-pig stomach. J Physiol 534(Pt 1):255–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziff EB (1997) Enlightening the postsynaptic density. Neuron 19(6):1163–1174

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The skilful technical assistance of Anita Hecht, Andrea Hilpert, Stefanie Link, Karin Löschner, and Hedwig Symowski is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Institut für Anatomie, Lehrstuhl I, Friedrich-Alexander-Universität, Krankenhausstr. 9, 91054, Erlangen, Germany

    J. Zimmermann, W. L. Neuhuber & M. Raab

Authors
  1. J. Zimmermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. L. Neuhuber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Raab
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Raab.

Ethics declarations

Conflict of interest

The authors have no competing interests. JZ performed the experiments, analyzed the data, and wrote the article together with MR; WN was involved in the study concept and critical revision of data documentation and the manuscript; MR designed the study and supervised experiments and data analysis. The present work was performed in fulfillment of the requirements for obtaining the degree Dr. med. dent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zimmermann, J., Neuhuber, W.L. & Raab, M. Homer1 (VesL-1) in the rat esophagus: focus on myenteric plexus and neuromuscular junction. Histochem Cell Biol 148, 189–206 (2017). https://doi.org/10.1007/s00418-017-1555-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-017-1555-7

Keywords

Search

Navigation