Home LiteratureArticle Details
PMID: 20049716 Published · ppublish English Case Reports Journal Article Research Support, Non-U.S. Gov't

Adjacent mutations in the gating loop of Kir6.2 produce neonatal diabetes and hyperinsulinism.

EMBO molecular medicine ·Vol. 1 ·No. 3 ·2009-06-00 ·Pages 166-77

Shimomura K, Flanagan SE, Zadek B, Lethby M, Zubcevic L, Girard CA, Petz O, Mannikko R, Kapoor RR, Hussain K, Skae M, Clayton P, Hattersley A, Ellard S, Ashcroft FM

Abstract

K(ATP) channels regulate insulin secretion from pancreatic beta-cells. Loss- and gain-of-function mutations in the genes encoding the Kir6.2 and SUR1 subunits of this channel cause hyperinsulinism of infancy and neonatal diabetes, respectively. We report two novel mutations in the gating loop of Kir6.2 which cause neonatal diabetes with developmental delay (T293N) and hyperinsulinism (T294M). These mutations increase (T293N) or decrease (T294M) whole-cell K(ATP) currents, accounting for the different clinical phenotypes. The T293N mutation increases the intrinsic channel open probability (Po((0))), thereby indirectly decreasing channel inhibition by ATP and increasing whole-cell currents. T294M channels exhibit a dramatically reduced Po((0)) in the homozygous but not in the pseudo-heterozygous state. Unlike wild-type channels, hetT294M channels were activated by MgADP in the absence but not in the presence of MgATP; however, they are activated by MgGDP in both the absence and presence of MgGTP. These mutations demonstrate the importance of the gating loop of Kir channels in regulating Po((0)) and further suggest that Mg-nucleotide interaction with SUR1 may reduce ATP inhibition at Kir6.2.

MeSH Terms
Adenosine Triphosphate/metabolism Congenital Hyperinsulinism/genetics Diabetes Mellitus/genetics Female Humans Infant, Newborn Male Pedigree Potassium/metabolism Potassium Channels, Inwardly Rectifying/chemistry,genetics Protein Structure, Tertiary
Chemicals
Kir6.2 channel Potassium Channels, Inwardly Rectifying Adenosine Triphosphate Potassium
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Shimomura Kenju
Henry Wellcome Centre for Gene Function, Department of Physiology, Anatomy and Genetics, University of Oxford, UK.
Flanagan Sarah E
Zadek Brittany
Lethby Mark
Zubcevic Lejla
Girard Christophe A J
Petz Oliver
Mannikko Roope
Kapoor Ritika R
Hussain Khalid
Skae Mars
Clayton Peter
Hattersley Andrew
Ellard Sian
Ashcroft Frances M
References (33)
33 references, click to expand
  1. Functional effects of KCNJ11 mutations causing neonatal diabetes: enhanced activation by MgATP.
    Hum Mol Genet. 2005 Sep 15;14(18):2717-26 PMID: 16087682
  2. Mechanisms of Disease: advances in diagnosis and treatment of hyperinsulinism in neonates.
    Nat Clin Pract Endocrinol Metab. 2007 Jan;3(1):57-68 PMID: 17179930
  3. A Kir6.2 mutation causing severe functional effects in vitro produces neonatal diabetes without the expected neurological complications.
    Diabetologia. 2008 May;51(5):802-10 PMID: 18335204
  4. Functional analysis of six Kir6.2 (KCNJ11) mutations causing neonatal diabetes.
    Pflugers Arch. 2006 Dec;453(3):323-32 PMID: 17021801
  5. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels.
    Neuron. 1999 Mar;22(3):537-48 PMID: 10197533
  6. Infantile spasms as an epileptic feature of DEND syndrome associated with an activating mutation in the potassium adenosine triphosphate (ATP) channel, Kir6.2.
    J Child Neurol. 2007 Sep;22(9):1147-50 PMID: 17890419
  7. Functional analyses of novel mutations in the sulfonylurea receptor 1 associated with persistent hyperinsulinemic hypoglycemia of infancy.
    Diabetes. 1998 Jul;47(7):1145-51 PMID: 9648840
  8. Cytoplasmic domain structures of Kir2.1 and Kir3.1 show sites for modulating gating and rectification.
    Nat Neurosci. 2005 Mar;8(3):279-87 PMID: 15723059
  9. Switching from insulin to oral sulfonylureas in patients with diabetes due to Kir6.2 mutations.
    N Engl J Med. 2006 Aug 3;355(5):467-77 PMID: 16885550
  10. Functional analysis of a structural model of the ATP-binding site of the KATP channel Kir6.2 subunit.
    EMBO J. 2005 Jan 26;24(2):229-39 PMID: 15650751
  11. Regulation of KATP channel activity by diazoxide and MgADP. Distinct functions of the two nucleotide binding folds of the sulfonylurea receptor.
    J Gen Physiol. 1997 Dec;110(6):643-54 PMID: 9382893
  12. The essential role of the Walker A motifs of SUR1 in K-ATP channel activation by Mg-ADP and diazoxide.
    EMBO J. 1997 Mar 17;16(6):1145-52 PMID: 9135131
  13. Mutations at the same residue (R50) of Kir6.2 (KCNJ11) that cause neonatal diabetes produce different functional effects.
    Diabetes. 2006 Jun;55(6):1705-12 PMID: 16731833
  14. Crystal structure of a Kir3.1-prokaryotic Kir channel chimera.
    EMBO J. 2007 Sep 5;26(17):4005-15 PMID: 17703190
  15. KATP channels as molecular sensors of cellular metabolism.
    Nature. 2006 Mar 23;440(7083):470-6 PMID: 16554807
  16. Burst kinetics of single calcium-activated potassium channels in cultured rat muscle.
    J Physiol. 1983 Nov;344:605-23 PMID: 6317854
  17. Hyperinsulinism in infancy: from basic science to clinical disease.
    Physiol Rev. 2004 Jan;84(1):239-75 PMID: 14715916
  18. An ATP-binding mutation (G334D) in KCNJ11 is associated with a sulfonylurea-insensitive form of developmental delay, epilepsy, and neonatal diabetes.
    Diabetes. 2007 Feb;56(2):328-36 PMID: 17259376
  19. The kinetic and physical basis of K(ATP) channel gating: toward a unified molecular understanding.
    Biophys J. 2000 May;78(5):2334-48 PMID: 10777731
  20. A novel method for measurement of submembrane ATP concentration.
    J Biol Chem. 2000 Sep 29;275(39):30046-9 PMID: 10866996
  21. The G53D mutation in Kir6.2 (KCNJ11) is associated with neonatal diabetes and motor dysfunction in adulthood that is improved with sulfonylurea therapy.
    J Clin Endocrinol Metab. 2008 Mar;93(3):1054-61 PMID: 18073297
  22. Adenosine diphosphate as an intracellular regulator of insulin secretion.
    Science. 1996 Jun 21;272(5269):1785-7 PMID: 8650576
  23. A novel KCNJ11 mutation associated with congenital hyperinsulinism reduces the intrinsic open probability of beta-cell ATP-sensitive potassium channels.
    J Biol Chem. 2006 Feb 3;281(5):3006-12 PMID: 16332676
  24. Activating mutations in Kir6.2 and neonatal diabetes: new clinical syndromes, new scientific insights, and new therapy.
    Diabetes. 2005 Sep;54(9):2503-13 PMID: 16123337
  25. Triggering and amplifying pathways of regulation of insulin secretion by glucose.
    Diabetes. 2000 Nov;49(11):1751-60 PMID: 11078440
  26. Congenital hyperinsulinism associated ABCC8 mutations that cause defective trafficking of ATP-sensitive K+ channels: identification and rescue.
    Diabetes. 2007 Sep;56(9):2339-48 PMID: 17575084
  27. Update of mutations in the genes encoding the pancreatic beta-cell K(ATP) channel subunits Kir6.2 (KCNJ11) and sulfonylurea receptor 1 (ABCC8) in diabetes mellitus and hyperinsulinism.
    Hum Mutat. 2009 Feb;30(2):170-80 PMID: 18767144
  28. Activation and inhibition of K-ATP currents by guanine nucleotides is mediated by different channel subunits.
    Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8872-7 PMID: 9238070
  29. Targeted overactivity of beta cell K(ATP) channels induces profound neonatal diabetes.
    Cell. 2000 Mar 17;100(6):645-54 PMID: 10761930
  30. The Walter B. Cannon Physiology in Perspective Lecture, 2007. ATP-sensitive K+ channels and disease: from molecule to malady.
    Am J Physiol Endocrinol Metab. 2007 Oct;293(4):E880-9 PMID: 17652156
  31. MgATP activates the beta cell KATP channel by interaction with its SUR1 subunit.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7185-90 PMID: 9618560
  32. A gating mutation at the internal mouth of the Kir6.2 pore is associated with DEND syndrome.
    EMBO Rep. 2005 May;6(5):470-5 PMID: 15864298
  33. Truncation of Kir6.2 produces ATP-sensitive K+ channels in the absence of the sulphonylurea receptor.
    Nature. 1997 May 8;387(6629):179-83 PMID: 9144288
Article Info
Journal
EMBO molecular medicine
Abbr.
EMBO Mol Med
ISSN
1757-4684
Published
2009-06-00
Pages
166-77
Language
English
Region
England
NLM ID
101487380
PMCID
PMC3378123
Subset
IM
Grants
Wellcome Trust · 084655 · United Kingdom
Wellcome Trust · 076436/Z/05/Z · United Kingdom
Wellcome Trust · 081188/A/06/Z · United Kingdom
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: [email protected]