Skip to main content
SpringerLink
Log in

Differential distribution of phospholipase C beta isoforms and diaglycerol kinase-beta in rodents cerebella corroborates the division of unipolar brush cells into two major subtypes

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Sublineage diversification of specific neural cell classes occurs in complex as well as simply organized regions of the central and peripheral nervous systems; the significance of the phenomenon, however, remains insufficiently understood. The unipolar brush cells (UBCs) are glutamatergic cerebellar interneurons that occur at high density in vestibulocerebellum. As they are classified into subsets that differ in chemical phenotypes, intrinsic properties, and lobular distribution, they represent a valuable neuronal model to study subclass diversification. In this study, we show that cerebellar UBCs of adult rats and mice form two subclasses—type I and type II UBCs—defined by somatodendritic expression of calretinin (CR), mGluR1α, phospholipases PLCβ1 and PLCβ4, and diacylglycerol kinase-beta (DGKβ). We demonstrate that PLCβ1 is associated only with the CR+ type I UBCs, while PLCβ4 and DGKβ are exclusively present in mGluR1α+ type II UBCs. Notably, all PLCβ4+ UBCs, representing about 2/3 of entire UBC population, also express mGluR1α. Furthermore, our data show that the sum of CR+ type I UBCs and mGluR1α+ type II UBCs accounts for the entire UBC class identified with Tbr2 immunolabeling. The two UBC subtypes also show a very different albeit somehow overlapping topographical distribution as illustrated by detailed cerebellar maps in this study. Our data not only complement and extend the previous knowledge on the diversity and subclass specificity of the chemical phenotypes within the UBC population, but also provide a new angle to the understanding of the signaling networks in type I and type II UBCs.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

Abbreviations

AON:

Anterior olfactory nucleus

Cer:

Cerebellum

CN:

Cerebellar nucleus

Cop:

Copula

Cx:

Cortex

DCN:

Dorsal cochlear nucleus

Fl:

Flocculus

gcl:

Granule cell layer

Hip:

Hippocampus

mb:

Medullary vellum border

ml:

Molecular layer

OB:

Olfactory bulb

PFl:

Paraflocculus

PM:

Paramedian lobule

sgl:

Superficial granular layer

Sim:

Simple lobule

tz:

Transition zone

VCN:

Ventral cochlear nucleus

wm:

White matter

Roman numerals I–X:

Cerebellar lobules

I:

Lingula

VI, VIb, VIc:

Folia of lobule VI

IX:

Uvula

IXa, IXb, IXc:

Folia of uvula

IXc/d:

In some rat specimens the last folia of uvula is subdivided into IXc and IXd by a shallow sulcus

X:

Nodulus

Xdors :

Dorsal leaflet of nodulus

Xvent :

Ventral leaflet of nodulus

r1–r4:

Regions 1–4; folial subdivision based on UBC densities

References

  • Adjobo-Hermans MJ, Crosby KC, Putyrski M, Bhageloe A, van Weeren L, Schultz C, Goedhart J, Gadella TW Jr (2013) PLCbeta isoforms differ in their subcellular location and their CT-domain dependent interaction with Galphaq. Cell Signal 25:255–263

    Article  CAS  PubMed  Google Scholar 

  • Aguado C, Colón J, Ciruela F, Schlaudraff F, Cabañero MJ, Perry C, Watanabe M, Liss B, Wickman K, Luján R (2008) Cell type-specific subunit composition of G protein-gated potassium channels in the cerebellum. J Neurochem 105:497–511

    Article  CAS  PubMed  Google Scholar 

  • Berrebi AS, Mugnaini E (1991) Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat Embryol (Berl) 183:427–454

    Article  CAS  Google Scholar 

  • Berrebi AS, Morgan JI, Mugnaini E (1990) The Purkinje cell class may extend beyond the cerebellum. J Neurocytol 19:643–654

    Article  CAS  PubMed  Google Scholar 

  • Birnstiel S, Slater NT, McCrimmon DR, Mugnaini E, Hartell NA (2009) Voltage-dependent calcium signaling in rat cerebellar unipolar brush cells. Neuroscience 162:702–712

    Article  CAS  PubMed  Google Scholar 

  • Bunney TD, Katan M (2011) PLC regulation: emerging pictures for molecular mechanisms. Trends Biochem Sci 36:88–96

    Article  CAS  PubMed  Google Scholar 

  • Chung SH, Marzban H, Watanabe M, Hawkes R (2009a) Phospholipase Cbeta4 expression identifies a novel subset of unipolar brush cells in the adult mouse cerebellum. Cerebellum 8:267–276

    Article  CAS  PubMed  Google Scholar 

  • Chung SH, Sillitoe RV, Croci L, Badaloni A, Consalez G, Hawkes R (2009b) Purkinje cell phenotype restricts the distribution of unipolar brush cells. Neuroscience 164:1496–1508

    Article  CAS  PubMed  Google Scholar 

  • Diana MA, Otsu Y, Maton G, Collin T, Chat M, Dieudonné S (2007) T-type and L-type Ca2+ conductances define and encode the bimodal firing pattern of vestibulocerebellar unipolar brush cells. J Neurosci 27:3823–3838

    Article  CAS  PubMed  Google Scholar 

  • Diño MR, Mugnaini E (2008) Distribution and phenotypes of unipolar brush cells in relation to the granule cell system of the rat cochlear nucleus. Neuroscience 154:29–50

    Article  PubMed Central  PubMed  Google Scholar 

  • Diño MR, Willard FH, Mugnaini E (1999) Distribution of unipolar brush cells and other calretinin immunoreactive components in the mammalian cerebellar cortex. J Neurocytol 28:99–123

    Article  PubMed  Google Scholar 

  • Diño MR, Schuerger RJ, Liu Y, Slater NT, Mugnaini E (2000) Unipolar brush cell: a potential feedforward excitatory interneuron of the cerebellum. Neuroscience 98:625–636

    Article  PubMed  Google Scholar 

  • Diño MR, Perachio AA, Mugnaini E (2001) Cerebellar unipolar brush cells are targets of primary vestibular afferents: an experimental study in the gerbil. Exp Brain Res 140:162–170

    Article  PubMed  Google Scholar 

  • Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G, Bupp S, Shrestha P, Shah RD, Doughty ML, Gong S, Greengard P, Heintz N (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135:749–762

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Englund C, Kowalczyk T, Daza RA, Dagan A, Lau C, Rose MF, Hevner RF (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci 26:9184–9195

    Article  CAS  PubMed  Google Scholar 

  • Ferraguti F, Crepaldi L, Nicoletti F (2008) Metabotropic glutamate 1 receptor: current concepts and perspectives. Pharmacol Rev 60:536–581

    Article  CAS  PubMed  Google Scholar 

  • Fukami K, Inanobe S, Kanemaru K, Nakamura Y (2010) Phospholipase C is a key enzyme regulating intracellular calcium and modulating the phosphoinositide balance. Prog Lipid Res 49:429–437

    Article  CAS  PubMed  Google Scholar 

  • Fukaya M, Uchigashima M, Nomura S, Hasegawa Y, Kikuchi H, Watanabe M (2008) Predominant expression of phospholipase Cbeta1 in telencephalic principal neurons and cerebellar interneurons, and its close association with related signaling molecules in somatodendritic neuronal elements. Eur J Neurosci 28:1744–1759

    Article  PubMed  Google Scholar 

  • Harden TK, Hicks SN, Sondek J (2009) Phospholipase C isozymes as effectors of Ras superfamily GTPases. J Lipid Res 50(Suppl):S243–S248

    PubMed  Google Scholar 

  • Harris J, Moreno S, Shaw G, Mugnaini E (1993) Unusual neurofilament composition in cerebellar unipolar brush neurons. J Neurocytol 22:1039–1059

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto K, Miyata M, Watanabe M, Kano M (2001) Roles of phospholipase Cbeta4 in synapse elimination and plasticity in developing and mature cerebellum. Mol Neurobiol 23:69–82

    Article  CAS  PubMed  Google Scholar 

  • Hozumi Y, Goto K (2012) Diacylglycerol kinase beta in neurons: functional implications at the synapse and in disease. Adv Biol Regul 52:315–325

    Article  CAS  PubMed  Google Scholar 

  • Hozumi Y, Fukaya M, Adachi N, Saito N, Otani K, Kondo H, Watanabe M, Goto K (2008) Diacylglycerol kinase beta accumulates on the perisynaptic site of medium spiny neurons in the striatum. Eur J Neurosci 28:2409–2422

    Article  PubMed  Google Scholar 

  • Hozumi Y, Watanabe M, Otani K, Goto K (2009) Diacylglycerol kinase beta promotes dendritic outgrowth and spine maturation in developing hippocampal neurons. BMC Neurosci 10:99

    Article  PubMed Central  PubMed  Google Scholar 

  • Jaarsma D, Diño MR, Cozzari C, Mugnaini E (1996) Cerebellar choline acetyltransferase positive mossy fibres and their granule and unipolar brush cell targets: a model for central cholinergic nicotinic neurotransmission. J Neurocytol 25:829–842

    Article  CAS  PubMed  Google Scholar 

  • Jaarsma D, Diño MR, Ohishi H, Shigemoto R, Mugnaini E (1998) Metabotropic glutamate receptors are associated with non-synaptic appendages of unipolar brush cells in rat cerebellar cortex and cochlear nuclear complex. J Neurocytol 27:303–327

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Jun KS, Lee SB, Kang NG, Min DS, Kim YH, Ryu SH, Suh PG, Shin HS (1997) Phospholipase C isozymes selectively couple to specific neurotransmitter receptors. Nature 389:290–293

    Article  CAS  PubMed  Google Scholar 

  • Kim MJ, Min DS, Ryu SH, Suh PG (1998) A cytosolic, galphaq- and betagamma-insensitive splice variant of phospholipase C-beta4. J Biol Chem 273:3618–3624

    Article  CAS  PubMed  Google Scholar 

  • Kim J-A, Sekerková G, Mugnaini E, Martina M (2012) Electrophysiological, morphological, and topological properties of two histochemically distinct subpopulations of cerebellar unipolar brush cells. Cerebellum 11(4):1012–1025. doi:10.1007/s12311-12012-10380-12318

    Article  PubMed Central  PubMed  Google Scholar 

  • Kitano J, Nishida M, Itsukaichi Y, Minami I, Ogawa M, Hirano T, Mori Y, Nakanishi S (2003) Direct interaction and functional coupling between metabotropic glutamate receptor subtype 1 and voltage-sensitive Cav2.1 Ca2+ channel. J Biol Chem 278:25101–25108

    Article  CAS  PubMed  Google Scholar 

  • Knoflach F, Kemp JA (1998) Metabotropic glutamate group II receptors activate a G protein-coupled inwardly rectifying K+ current in neurones of the rat cerebellum. J Physiol 509(Pt 2):347–354

    Article  CAS  PubMed  Google Scholar 

  • Larsell O (1968) The comparative anatomy and histology of the cerebellum from monotremes through apes. The University of Minnesota Press, Minneapolis

    Google Scholar 

  • Lee CW, Lee KH, Lee SB, Park D, Rhee SG (1994) Regulation of phospholipase C-beta 4 by ribonucleotides and the alpha subunit of Gq. J Biol Chem 269:25335–25338

    CAS  PubMed  Google Scholar 

  • Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176

    Article  CAS  PubMed  Google Scholar 

  • Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9:99–111

    Article  CAS  PubMed  Google Scholar 

  • Lennon SM, Rivero G, Matharu A, Howson PA, Jane DE, Roberts PJ, Kelly E (2010) Metabotropic glutamate receptor mGlu2 is resistant to homologous agonist-induced desensitization but undergoes protein kinase C-mediated heterologous desensitization. Eur J Pharmacol 649:29–37

    Article  CAS  PubMed  Google Scholar 

  • Min DS, Kim MJ, Jeong HK, Lee YH, Kim H, Shin HS, Ryu SH, Suh PG (2000) Immunological characterization of 130 kDa phospholipase C-beta 4 isozyme in rat cerebellar Purkinje cells. Neurosci Lett 292:9–12

    Article  CAS  PubMed  Google Scholar 

  • Montaña M, García Del Caño G, López de Jesús M, González-Burguera I, Echeazarra L, Barrondo S, Sallés J (2012) Cellular neurochemical characterization and subcellular localization of phospholipase C beta1 in rat brain. Neuroscience 222:239–268

    Article  PubMed  Google Scholar 

  • Montell C (2011) The history of TRP channels, a commentary and reflection. Pflugers Arch 461:499–506

    Article  CAS  PubMed  Google Scholar 

  • Mugnaini E, Floris A (1994) The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex. J Comp Neurol 339:174–180

    Article  CAS  PubMed  Google Scholar 

  • Mugnaini E, Berrebi AS, Dahl AL, Morgan JI (1987) The polypeptide PEP-19 is a marker for Purkinje neurons in cerebellar cortex and cartwheel neurons in the dorsal cochlear nucleus. Arch Ital Biol 126:41–67

    CAS  PubMed  Google Scholar 

  • Mugnaini E, Floris A, Wright-Goss M (1994) Extraordinary synapses of the unipolar brush cell: an electron microscopic study in the rat cerebellum. Synapse 16:284–311

    Article  CAS  PubMed  Google Scholar 

  • Mugnaini E, Sekerkova G, Martina M (2010) The unipolar brush cell: a remarkable neuron finally receiving deserved attention. Brain Res Rev 66:220–245

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakamura M, Sato K, Fukaya M, Araishi K, Aiba A, Kano M, Watanabe M (2004) Signaling complex formation of phospholipase Cbeta4 with metabotropic glutamate receptor type 1alpha and 1,4,5-trisphosphate receptor at the perisynapse and endoplasmic reticulum in the mouse brain. Eur J Neurosci 20:2929–2944

    Article  PubMed  Google Scholar 

  • Neki A, Ohishi H, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N (1996) Pre- and postsynaptic localization of a metabotropic glutamate receptor, mGluR2, in the rat brain: an immunohistochemical study with a monoclonal antibody. Neurosci Lett 202:197–200

    Article  CAS  PubMed  Google Scholar 

  • Nomura S, Fukaya M, Tsujioka T, Wu D, Watanabe M (2007) Phospholipase Cbeta3 is distributed in both somatodendritic and axonal compartments and localized around perisynapse and smooth endoplasmic reticulum in mouse Purkinje cell subsets. Eur J Neurosci 25:659–672

    Article  PubMed  Google Scholar 

  • Nunzi MG, Mugnaini E (2009) Aspects of the neuroendocrine cerebellum: expression of secretogranin II, chromogranin A and chromogranin B in mouse cerebellar unipolar brush cells. Neurosci 162:673–687

    Google Scholar 

  • Nunzi MG, Birnstiel S, Bhattacharyya BJ, Slater NT, Mugnaini E (2001) Unipolar brush cells form a glutamatergic projection system within the mouse cerebellar cortex. J Comp Neurol 434:329–341

    Article  CAS  PubMed  Google Scholar 

  • Nunzi MG, Shigemoto R, Mugnaini E (2002) Differential expression of calretinin and metabotropic glutamate receptor mGluR1alpha defines subsets of unipolar brush cells in mouse cerebellum. J Comp Neurol 451:189–199

    Article  CAS  PubMed  Google Scholar 

  • Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993a) Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience 53:1009–1018

    Article  CAS  PubMed  Google Scholar 

  • Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993b) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J Comp Neurol 335:252–266

    Article  CAS  PubMed  Google Scholar 

  • Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1–26

    Article  CAS  PubMed  Google Scholar 

  • Rebecchi MJ, Pentyala SN (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80:1291–1335

    CAS  PubMed  Google Scholar 

  • Rhee SG (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70:281–312

    Article  CAS  PubMed  Google Scholar 

  • Ross WN, Nakamura T, Watanabe S, Larkum M, Lasser-Ross N (2005) Synaptically activated ca2+ release from internal stores in CNS neurons. Cell Mol Neurobiol 25:283–295

    Article  CAS  PubMed  Google Scholar 

  • Rossi DJ, Alford S, Mugnaini E, Slater NT (1995) Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber–unipolar brush cell synapse. J Neurophysiol 74:24–42

    CAS  PubMed  Google Scholar 

  • Rousseau CV, Dugue GP, Dumoulin A, Mugnaini E, Dieudonne S, Diana MA (2012) Mixed inhibitory synaptic balance correlates with glutamatergic synaptic phenotype in cerebellar unipolar brush cells. J Neurosci 32:4632–4644

    Article  CAS  PubMed  Google Scholar 

  • Roustan P, Abitbol M, Menini C, Ribeaudeau F, Gerard M, Vekemans M, Mallet J, Dufier JL (1995) The rat phospholipase C beta 4 gene is expressed at high abundance in cerebellar Purkinje cells. NeuroReport 6:1837–1841

    Article  CAS  PubMed  Google Scholar 

  • Russo MJ, Yau HJ, Nunzi MG, Mugnaini E, Martina M (2008) Dynamic metabotropic control of intrinsic firing in cerebellar unipolar brush cells. J Neurophysiol 100:3351–3360

    Article  PubMed  Google Scholar 

  • Sarna JR, Marzban H, Watanabe M, Hawkes R (2006) Complementary stripes of phospholipase Cbeta3 and Cbeta4 expression by Purkinje cell subsets in the mouse cerebellum. J Comp Neurol 496:303–313

    Article  CAS  PubMed  Google Scholar 

  • Schilling K, Oberdick J (2009) The treasury of the commons: making use of public gene expression resources to better characterize the molecular diversity of inhibitory interneurons in the cerebellar cortex. Cerebellum 8:477–489

    Article  CAS  PubMed  Google Scholar 

  • Sekerková G, Ilijic E, Mugnaini E (2004) Time of origin of unipolar brush cells in the rat cerebellum as observed by prenatal bromodeoxyuridine labeling. Neuroscience 127:845–858

    Article  PubMed  Google Scholar 

  • Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17:7503–7522

    CAS  PubMed  Google Scholar 

  • Sugiyama T, Hirono M, Suzuki K, Nakamura Y, Aiba A, Nakamura K, Nakao K, Katsuki M, Yoshioka T (1999) Localization of phospholipase Cbeta isozymes in the mouse cerebellum. Biochem Biophys Res Commun 265:473–478

    Article  CAS  PubMed  Google Scholar 

  • Takács J, Markova L, Borostyánkői Z, Görcs TJ, Hámori J (1999) Metabotrop glutamate receptor type 1a expressing unipolar brush cells in the cerebellar cortex of different species: a comparative quantitative study. J Neurosci Res 55:733–748

    Article  PubMed  Google Scholar 

  • Tanaka O, Kondo H (1994) Localization of mRNAs for three novel members (beta 3, beta 4 and gamma 2) of phospholipase C family in mature rat brain. Neurosci Lett 182:17–20

    Article  CAS  PubMed  Google Scholar 

  • Tanaka J, Nakagawa S, Kushiya E, Yamasaki M, Fukaya M, Iwanaga T, Simon MI, Sakimura K, Kano M, Watanabe M (2000) Gq protein alpha subunits Galphaq and Galpha11 are localized at postsynaptic extra-junctional membrane of cerebellar Purkinje cells and hippocampal pyramidal cells. Eur J Neurosci 12:781–792

    Article  CAS  PubMed  Google Scholar 

  • Tateyama M, Kubo Y (2011) The intra-molecular activation mechanisms of the dimeric metabotropic glutamate receptor 1 differ depending on the type of G proteins. Neuropharmacology 61:832–841

    Article  CAS  PubMed  Google Scholar 

  • Vitale M, Rezzani R, Gobbi G, Ponti C, Matteucci A, Cacchioli A, Ruggeri A Jr, Cocco L (2004) Phospholipase-C beta1 is predominantly expressed in the granular layer of rat cerebellar cortex. Int J Mol Med 14:161–164

    CAS  PubMed  Google Scholar 

  • Wang T, Pentyala S, Elliott JT, Dowal L, Gupta E, Rebecchi MJ, Scarlata S (1999) Selective interaction of the C2 domains of phospholipase C-beta1 and -beta2 with activated Galphaq subunits: an alternative function for C2-signaling modules. Proc Natl Acad Sci USA 96:7843–7846

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Bianchi R, Chuang SC, Zhao W, Wong RK (2007) Group I metabotropic glutamate receptor-dependent TRPC channel trafficking in hippocampal neurons. J Neurochem 101:411–421

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Nakamura M, Sato K, Kano M, Simon MI, Inoue Y (1998) Patterns of expression for the mRNA corresponding to the four isoforms of phospholipase Cbeta in mouse brain. Eur J Neurosci 10:2016–2025

    Article  CAS  PubMed  Google Scholar 

  • Williams RL (1999) Mammalian phosphoinositide-specific phospholipase C. Biochim Biophys Acta 1441:255–267

    Article  CAS  PubMed  Google Scholar 

  • Williams RL, Katan M (1996) Structural views of phosphoinositide-specific phospholipase C: signalling the way ahead. Structure 4:1387–1394

    Article  CAS  PubMed  Google Scholar 

  • Woo DH, Jung SJ, Zhu MH, Park CK, Kim YH, Oh SB, Lee CJ (2008) Direct activation of transient receptor potential vanilloid 1(TRPV1) by diacylglycerol (DAG). Mol Pain 4:42

    Article  PubMed Central  PubMed  Google Scholar 

  • Yakunin AF, Hallenbeck PC (1998) A luminol/iodophenol chemiluminescent detection system or western immunoblots. Anal Biochem 258:146–149

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by NIH grant RO1 09904. The authors wish to thank Drs. Joe P. Doyle, Joseph D. Dougherthy and Nataniel Heintz (The Rockefeller University, New York) for breeding pairs of Tg(Grp-EGFP) DV197 mice, Prof. Ryuichi Shigemoto (National Institute for Physiological Sciences, Okazaki, Japan) and Dr. K. Goto (Yamagata University School of Medicine, Japan) for mGluR1α and DGKβ antibodies, respectively.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Cellular and Molecular Biology, Feinberg School of Medicine, Northwestern University, 5-465 Searle bldg. 320 E. Superior str, Chicago, IL, 60611, USA

    Gabriella Sekerková & Enrico Mugnaini

  2. Department of Anatomy, Hokkaido University School of Medicine, Sapporo, 060-8638, Japan

    Masahiko Watanabe

  3. Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, 60611, USA

    Marco Martina

Authors
  1. Gabriella Sekerková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masahiko Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marco Martina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Enrico Mugnaini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriella Sekerková.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sekerková, G., Watanabe, M., Martina, M. et al. Differential distribution of phospholipase C beta isoforms and diaglycerol kinase-beta in rodents cerebella corroborates the division of unipolar brush cells into two major subtypes. Brain Struct Funct 219, 719–749 (2014). https://doi.org/10.1007/s00429-013-0531-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-013-0531-9

Keywords

Search

Navigation