Home LiteratureArticle Details
PMID: 12832499 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mediation of neuronal apoptosis by Kv2.1-encoded potassium channels.

Pal S, Hartnett KA, Nerbonne JM, Levitan ES, Aizenman E

Abstract

Cellular K+ efflux is a requisite event in the unfolding of apoptosis programs across many types of cells and death-inducing stimuli; however, the molecular identities of the ion channels mediating this key event have remained undefined. Here, we show that Kv2.1-encoded K+ channels are responsible for the expression of apoptosis in cortical neurons in vitro. Transient expression of two different dominant-negative forms of this subunit in neurons completely eliminated the enhancement of K+ currents that normally accompanies the cell death process. Importantly, neurons deficient in functional Kv2.1-encoded K+ channels were protected from oxidant and staurosporine-induced apoptosis. Finally, Chinese hamster ovary cells, which do not express endogenous voltage-gated K+ channels, became substantially more sensitive to apoptosis after transient expression of wild-type Kv2.1. These results suggest that Kv2.1-encoded K+ channels are necessary for the apoptotic signaling cascade in mammalian cortical neurons in culture and are sufficient for increasing the susceptibility to apoptogens in a nonexcitable cell.

MeSH Terms
Animals Apoptosis/drug effects,physiology CHO Cells Cells, Cultured Cricetinae Cytoprotection/genetics,physiology Delayed Rectifier Potassium Channels Genes, Dominant Neurons/cytology,metabolism Oxidants/toxicity Patch-Clamp Techniques Potassium/metabolism Potassium Channels/genetics,metabolism Potassium Channels, Voltage-Gated Protein Subunits/genetics,metabolism Rats Shab Potassium Channels Signal Transduction/drug effects,physiology Staurosporine/toxicity Transfection
Chemicals
Delayed Rectifier Potassium Channels Kcnb1 protein, rat Oxidants Potassium Channels Potassium Channels, Voltage-Gated Protein Subunits Shab Potassium Channels Staurosporine Potassium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Pal Sumon
Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261, USA.
Hartnett Karen A
Nerbonne Jeanne M
Levitan Edwin S
Aizenman Elias
References (24)
24 references, click to expand
  1. p38 activation is required upstream of potassium current enhancement and caspase cleavage in thiol oxidant-induced neuronal apoptosis.
    J Neurosci. 2001 May 15;21(10):3303-11 PMID: 11331359
  2. Improving the transfection efficiency of post-mitotic neurons.
    J Neurosci Methods. 2001 Dec 15;112(2):95-9 PMID: 11716945
  3. Apoptosis recruits two-pore domain potassium channels used for homeostatic volume regulation.
    Am J Physiol Cell Physiol. 2002 Mar;282(3):C588-94 PMID: 11832344
  4. Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane.
    J Neurochem. 2002 Jan;80(2):207-18 PMID: 11902111
  5. Functional expression of muscle-type nicotinic acetylcholine receptors in rat forebrain neurons in vitro.
    Methods Find Exp Clin Pharmacol. 2002 Mar;24(2):63-6 PMID: 12040883
  6. Delayed rectifier K+ currents, IK, are encoded by Kv2 alpha-subunits and regulate tonic firing in mammalian sympathetic neurons.
    J Neurosci. 2002 Dec 1;22(23):10094-105 PMID: 12451110
  7. Intracellular ionic variations in the apoptotic death of L cells by inhibitors of cell cycle progression.
    Exp Cell Res. 1995 Apr;217(2):410-8 PMID: 7698242
  8. Pharmacological properties of acquired excitotoxicity in Chinese hamster ovary cells transfected with N-methyl-D-aspartate receptor subunits.
    J Pharmacol Exp Ther. 1996 Nov;279(2):515-23 PMID: 8930153
  9. ROMK1 (Kir1.1) causes apoptosis and chronic silencing of hippocampal neurons.
    J Neurophysiol. 2000 Aug;84(2):1062-75 PMID: 10938328
  10. Mediation of neuronal apoptosis by enhancement of outward potassium current.
    Science. 1997 Oct 3;278(5335):114-7 PMID: 9311914
  11. Intracellular K+ suppresses the activation of apoptosis in lymphocytes.
    J Biol Chem. 1997 Nov 28;272(48):30567-76 PMID: 9374553
  12. Potassium leakage during the apoptotic degradation phase.
    J Immunol. 1998 Jun 1;160(11):5605-15 PMID: 9605166
  13. Endogenous voltage-gated potassium channels in human embryonic kidney (HEK293) cells.
    J Neurosci Res. 1998 Jun 1;52(5):612-7 PMID: 9632317
  14. Enhancement of outward potassium current may participate in beta-amyloid peptide-induced cortical neuronal death.
    Neurobiol Dis. 1998 Aug;5(2):81-8 PMID: 9746905
  15. Heteromultimeric potassium channels formed by members of the Kv2 subfamily.
    J Neurosci. 1998 Dec 1;18(23):9585-93 PMID: 9822719
  16. Distinct structural requirements for clustering and immobilization of K+ channels by PSD-95.
    J Gen Physiol. 1999 Jan;113(1):71-80 PMID: 9874689
  17. Identification of the Kv2.1 K+ channel as a major component of the delayed rectifier K+ current in rat hippocampal neurons.
    J Neurosci. 1999 Mar 1;19(5):1728-35 PMID: 10024359
  18. Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo.
    Adv Enzyme Regul. 1999;39:157-71 PMID: 10470372
  19. Attenuation of the slow component of delayed rectification, action potential prolongation, and triggered activity in mice expressing a dominant-negative Kv2 alpha subunit.
    Circ Res. 1999 Oct 1;85(7):623-33 PMID: 10506487
  20. Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release.
    J Neurochem. 2000 Nov;75(5):1878-88 PMID: 11032877
  21. Role of NMDA receptor functional domains in excitatory cell death.
    Neuropharmacology. 2000 Sep;39(12):2255-66 PMID: 10974309
  22. Involvement of K(+)-Cl(-)-cotransport in the apoptosis induced by N-ethylmaleimide in HepG2 human hepatoblastoma cells.
    Eur J Pharmacol. 2001 Apr 20;418(1-2):1-5 PMID: 11334858
  23. Differential changes of potassium currents in CA1 pyramidal neurons after transient forebrain ischemia.
    J Neurophysiol. 2000 Dec;84(6):2834-43 PMID: 11110813
  24. NMDA receptor-mediated neurotoxicity: a paradoxical requirement for extracellular Mg2+ in Na+/Ca2+-free solutions in rat cortical neurons in vitro.
    J Neurochem. 1997 May;68(5):1836-45 PMID: 9109508
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-06-15
Pages
4798-802
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC2945225
Subset
IM
Grants
NINDS NIH HHS · R01 NS043277 · United States
NINDS NIH HHS · R01 NS043277-05 · United States
NINDS NIH HHS · NS30676 · United States
NINDS NIH HHS · R01 NS043277-03 · United States
NINDS NIH HHS · R56 NS043277 · United States
NHLBI NIH HHS · R01 HL055312 · United States
NINDS NIH HHS · R01 NS043277-07A2 · United States
NINDS NIH HHS · R01 NS043277-02 · United States
NINDS NIH HHS · R01 NS043277-10 · United States
NINDS NIH HHS · R01 NS030676 · United States
NINDS NIH HHS · R01 NS043277-09 · United States
NINDS NIH HHS · NS43277 · United States
NINDS NIH HHS · R01 NS043277-01A1S1 · United States
NINDS NIH HHS · R01 NS043277-04 · United States
NINDS NIH HHS · R01 NS043277-08 · United States
NINDS NIH HHS · R56 NS043277-06 · United States
NHLBI NIH HHS · HL55312 · United States
NHLBI NIH HHS · HL34161 · United States
NHLBI NIH HHS · R01 HL034161 · United States
NINDS NIH HHS · R01 NS043277-01A1 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com