An Alpha-Catulin Homologue Controls Neuromuscular Function through Localization of the Dystrophin Complex and BK Channels in

English version České info

The large conductance, voltage- and calcium-dependent potassium (BK) channel serves as a major negative feedback regulator of calcium-mediated physiological processes and has been implicated in muscle dysfunction and neurological disorders. In addition to membrane depolarization, activation of the BK channel requires a rise in cytosolic calcium. Localization of the BK channel near calcium channels is therefore critical for its function. In a genetic screen designed to isolate novel regulators of the Caenorhabditis elegans BK channel, SLO-1, we identified ctn-1, which encodes an α-catulin homologue with homology to the cytoskeletal proteins α-catenin and vinculin. ctn-1 mutants resemble slo-1 loss-of-function mutants, as well as mutants with a compromised dystrophin complex. We determined that CTN-1 uses two distinct mechanisms to localize SLO-1 in muscles and neurons. In muscles, CTN-1 utilizes the dystrophin complex to localize SLO-1 channels near L-type calcium channels. In neurons, CTN-1 is involved in localizing SLO-1 to a specific domain independent of the dystrophin complex. Our results demonstrate that CTN-1 ensures the localization of SLO-1 within calcium nanodomains, thereby playing a crucial role in muscles and neurons.

Vyšlo v časopise: An Alpha-Catulin Homologue Controls Neuromuscular Function through Localization of the Dystrophin Complex and BK Channels in. PLoS Genet 6(8): e32767. doi:10.1371/journal.pgen.1001077
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001077

Souhrn

Zdroje

1. LaiHC

JanLY

2006 The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7 548 562

2. LevitanIB

2006 Signaling protein complexes associated with neuronal ion channels. Nat Neurosci 9 305 310

3. SalkoffL

ButlerA

FerreiraG

SantiC

WeiA

2006 High-conductance potassium channels of the SLO family. Nat Rev Neurosci 7 921 931

4. FaklerB

AdelmanJP

2008 Control of K(Ca) channels by calcium nano/microdomains. Neuron 59 873 881

5. BrennerR

PerezGJ

BonevAD

EckmanDM

KosekJC

2000 Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature 407 870 876

6. LovellPV

McCobbDP

2001 Pituitary control of BK potassium channel function and intrinsic firing properties of adrenal chromaffin cells. J Neurosci 21 3429 3442

7. WernerME

ZvaraP

MeredithAL

AldrichRW

NelsonMT

2005 Erectile dysfunction in mice lacking the large-conductance calcium-activated potassium (BK) channel. J Physiol 567 545 556

8. DuW

BautistaJF

YangH

Diez-SampedroA

YouSA

2005 Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nat Genet 37 733 738

9. ShrutiS

ClemRL

BarthAL

2008 A seizure-induced gain-of-function in BK channels is associated with elevated firing activity in neocortical pyramidal neurons. Neurobiol Dis 30 323 330

10. SchopperleWM

HolmqvistMH

ZhouY

WangJ

WangZ

1998 Slob, a novel protein that interacts with the Slowpoke calcium-dependent potassium channel. Neuron 20 565 573

11. LuR

AliouaA

KumarY

EghbaliM

StefaniE

2006 MaxiK channel partners: physiological impact. J Physiol 570 65 72

12. TianL

ChenL

McClaffertyH

SailerCA

RuthP

2006 A noncanonical SH3 domain binding motif links BK channels to the actin cytoskeleton via the SH3 adapter cortactin. FASEB J 20 2588 2590

13. KimEY

RidgwayLD

DryerSE

2007 Interactions with filamin A stimulate surface expression of large-conductance Ca2+-activated K+ channels in the absence of direct actin binding. Mol Pharmacol 72 622 630

14. ParkSM

LiuG

KubalA

FuryM

CaoL

2004 Direct interaction between BKCa potassium channel and microtubule-associated protein 1A. FEBS Lett 570 143 148

15. WangZW

SaifeeO

NonetML

SalkoffL

2001 SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction. Neuron 32 867 881

16. DaviesAG

Pierce-ShimomuraJT

KimH

VanHovenMK

ThieleTR

2003 A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 115 655 666

17. Carre-PierratM

GrisoniK

GieselerK

MariolMC

MartinE

2006 The SLO-1 BK channel of Caenorhabditis elegans is critical for muscle function and is involved in dystrophin-dependent muscle dystrophy. J Mol Biol 358 387 395

18. KimH

RogersMJ

RichmondJE

McIntireSL

2004 SNF-6 is an acetylcholine transporter interacting with the dystrophin complex in Caenorhabditis elegans. Nature 430 891 896

19. BessouC

GiugiaJB

FranksCJ

Holden-DyeL

SegalatL

1998 Mutations in the Caenorhabditis elegans dystrophin-like gene dys-1 lead to hyperactivity and suggest a link with cholinergic transmission. Neurogenetics 2 61 72

20. GieselerK

BessouC

SegalatL

1999 Dystrobrevin- and dystrophin-like mutants display similar phenotypes in the nematode Caenorhabditis elegans. Neurogenetics 2 87 90

21. KimH

Pierce-ShimomuraJT

OhHJ

JohnsonBE

GoodmanMB

2009 The dystrophin complex controls bk channel localization and muscle activity in Caenorhabditis elegans. PLoS Genet 5 e1000780 doi:10.1371/journal.pgen.1000780

22. AldertonJM

SteinhardtRA

2000 Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J Biol Chem 275 9452 9460

23. JanssensB

StaesK

van RoyF

1999 Human alpha-catulin, a novel alpha-catenin-like molecule with conserved genomic structure, but deviating alternative splicing. Biochim Biophys Acta 1447 341 347

24. BarsteadRJ

WaterstonRH

1989 The basal component of the nematode dense-body is vinculin. J Biol Chem 264 10177 10185

25. CostaM

RaichW

AgbunagC

LeungB

HardinJ

1998 A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J Cell Biol 141 297 308

26. WiesnerC

WinsauerG

ReschU

HoethM

SchmidJA

2008 Alpha-catulin, a Rho signalling component, can regulate NF-kappaB through binding to IKK-beta, and confers resistance to apoptosis. Oncogene 27 2159 2169

27. Sadoulet-PuccioHM

RajalaM

KunkelLM

1997 Dystrobrevin and dystrophin: an interaction through coiled-coil motifs. Proc Natl Acad Sci U S A 94 12413 12418

28. HuH

ShaoLR

ChavoshyS

GuN

TriebM

2001 Presynaptic Ca2+-activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J Neurosci 21 9585 9597

29. SailerCA

KaufmannWA

KoglerM

ChenL

SausbierU

2006 Immunolocalization of BK channels in hippocampal pyramidal neurons. Eur J Neurosci 24 442 454

30. KaufmannWA

FerragutiF

FukazawaY

KasugaiY

ShigemotoR

2009 Large-conductance calcium-activated potassium channels in purkinje cell plasma membranes are clustered at sites of hypolemmal microdomains. J Comp Neurol 515 215 230

31. LiewaldJF

BraunerM

StephensGJ

BouhoursM

SchultheisC

2008 Optogenetic analysis of synaptic function. Nat Methods 5 895 902

32. GieselerK

MariolMC

BessouC

MigaudM

FranksCJ

2001 Molecular, genetic and physiological characterisation of dystrobrevin-like (dyb-1) mutants of Caenorhabditis elegans. J Mol Biol 307 107 117

33. EdgertonJR

ReinhartPH

2003 Distinct contributions of small and large conductance Ca2+-activated K+ channels to rat Purkinje neuron function. J Physiol 548 53 69

34. PrakriyaM

LingleCJ

1999 BK channel activation by brief depolarizations requires Ca2+ influx through L- and Q-type Ca2+ channels in rat chromaffin cells. J Neurophysiol 81 2267 2278

35. GrachevaEO

HadwigerG

NonetML

RichmondJE

2008 Direct interactions between C. elegans RAB-3 and Rim provide a mechanism to target vesicles to the presynaptic density. Neurosci Lett 444 137 142

36. SahekiY

BargmannCI

2009 Presynaptic CaV2 calcium channel traffic requires CALF-1 and the alpha(2)delta subunit UNC-36. Nat Neurosci 12 1257 1265

37. BiggarWD

KlamutHJ

DemacioPC

StevensDJ

RayPN

2002 Duchenne muscular dystrophy: current knowledge, treatment, and future prospects. Clin Orthop Relat Res 88 106

38. BoisPR

BorgonRA

VonrheinC