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Molecular Biology of Adenosine Triphosphate-Sensitive Potassium Channels¹

Departments of Medicine (L.A.-B.) and Cell Biology (J.B.), Baylor College of Medicine, Houston, Texas 77030

I. Introduction

II. How Are K_ATP Channels Defined?

III. How Do K_ATP Channels Affect the Membrane Potential of Pancreatic ß-Cells?

IV. K_ATP Channel Subunits

A. The K_IR family of inwardly rectifying K+ channels

B. Sulfonylurea receptors

V. Reconstitution of K_ATP Channel Activity from SUR1 and K_IR6.2

A. The question of "promiscuous coupling" of SUR1 with other inward rectifiers

VI. K_ATP Channel Structure

A. K_IR6.2 forms the pore of a K_ATP channel

B. SUR1 and K_IR6.x are physically associated

C. Coexpression with K_IR6.2 affects the maturation of SUR1

D. Complex glycosylated SUR1 and K_IR6.2 assemble a large multimer

E. A 1:1 stoichiometry of SUR to K_IR is both necessary and sufficient to make K_ATP channels

F. Other K_IR channels are tetramers

G. The stoichiometry of active ß-cell K_ATP channels is (SUR1/K_IR6.2)₄

VII. Regulation of K_ATP Channel Activity

A. How do ATP and ADP exert their effects on K_ATP channels?

B. Where are the nucleotide binding sites located?

C. C-terminally truncated K_IR6.2 channels show abnormal kinetics

D. Coexpression of K_IR6.2C subunits with SUR restores normal K_ATP channel activity

E. Why are K_IR6.2 channels silent?

F. The N terminus of K_IR6.2 limits burst duration

G. Where do the openers bind and how do they work?

H. Do SURs have adenosine triphosphatase (ATPase) activity?

I. Do SURs have transport activity?

J. Is there an endogenous substrate?

VIII. Human SUR1 and K_IR6.2 Genes

IX. K_ATP Channels and Persistent Hyperinsulinemic Hypoglycemia of Infancy (PHHI)

A. HI-GK

B. HI-GlnDH

C. HI-"unknown"

D. HI-K_IR6.2

E. HI-SUR1

X. Linking PHHI to Defects in K_ATP Channel Activity

A. ß-Cells from newborns diagnosed with "sporadic" PHHI lack K_ATP channel activity

B. PHHI ß-cells with the SUR1 exon 35 mutation lack K_ATP channel activity

C. Why is there a lack of dominant negative mutations?

D. Development of mouse models

XI. Other Issues

A. Nesidioblastosis does not cause PHHI

B. "Diffuse" vs. "focal" forms of PHHI

XII. K_ATP and Non-Insulin-Dependent Diabetes Mellitus (NIDDM)

A. ß-Cell type K_ATP channels in the brain

XIII. The Leptin Connection

XIV. Summary and Conclusions

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				X. Jin, A. P. Malykhina, F. Lupu, and H. I. Akbarali Altered gene expression and increased bursting activity of colonic smooth muscle ATP-sensitive K+ channels in experimental colitis Am J Physiol Gastrointest Liver Physiol, July 1, 2004; 287(1): G274 - G285. [Abstract] [Full Text] [PDF]

				G. da Silva Xavier, J. Rutter, and G. A. Rutter Involvement of Per-Arnt-Sim (PAS) kinase in the stimulation of preproinsulin and pancreatic duodenum homeobox 1 gene expression by glucose PNAS, June 1, 2004; 101(22): 8319 - 8324. [Abstract] [Full Text] [PDF]

				J. C. Florez, N. Burtt, P. I.W. de Bakker, P. Almgren, T. Tuomi, J. Holmkvist, D. Gaudet, T. J. Hudson, S. F. Schaffner, M. J. Daly, et al. Haplotype Structure and Genotype-Phenotype Correlations of the Sulfonylurea Receptor and the Islet ATP-Sensitive Potassium Channel Gene Region Diabetes, May 1, 2004; 53(5): 1360 - 1368. [Abstract] [Full Text] [PDF]

				N. M. Doliba, W. Qin, M. Z. Vatamaniuk, C. Li, D. Zelent, H. Najafi, C. W. Buettger, H. W. Collins, R. D. Carr, M. A. Magnuson, et al. Restitution of defective glucose-stimulated insulin release of sulfonylurea type 1 receptor knockout mice by acetylcholine Am J Physiol Endocrinol Metab, May 1, 2004; 286(5): E834 - E843. [Abstract] [Full Text] [PDF]

				F. Yan, C.-W. Lin, E. Weisiger, E. A. Cartier, G. Taschenberger, and S.-L. Shyng Sulfonylureas Correct Trafficking Defects of ATP-sensitive Potassium Channels Caused by Mutations in the Sulfonylurea Receptor J. Biol. Chem., March 19, 2004; 279(12): 11096 - 11105. [Abstract] [Full Text] [PDF]

				A. Crane and L. Aguilar-Bryan Assembly, Maturation, and Turnover of KATP Channel Subunits J. Biol. Chem., March 5, 2004; 279(10): 9080 - 9090. [Abstract] [Full Text] [PDF]

				L. Kang, V. H. Routh, E. V. Kuzhikandathil, L. D. Gaspers, and B. E. Levin Physiological and Molecular Characteristics of Rat Hypothalamic Ventromedial Nucleus Glucosensing Neurons Diabetes, March 1, 2004; 53(3): 549 - 559. [Abstract] [Full Text] [PDF]

				L. Yan, D. J. Figueroa, C. P. Austin, Y. Liu, R. M. Bugianesi, R. S. Slaughter, G. J. Kaczorowski, and M. G. Kohler Expression of Voltage-Gated Potassium Channels in Human and Rhesus Pancreatic Islets Diabetes, March 1, 2004; 53(3): 597 - 607. [Abstract] [Full Text] [PDF]

				A. Sieg, J. Su, A. Munoz, M. Buchenau, M. Nakazaki, L. Aguilar-Bryan, J. Bryan, and S. Ullrich Epinephrine-induced hyperpolarization of islet cells without KATP channels Am J Physiol Endocrinol Metab, March 1, 2004; 286(3): E463 - E471. [Abstract] [Full Text]

				C. A. Stanley, P. S. Thornton, A. Ganguly, C. MacMullen, P. Underwood, P. Bhatia, L. Steinkrauss, L. Wanner, R. Kaye, E. Ruchelli, et al. Preoperative Evaluation of Infants with Focal or Diffuse Congenital Hyperinsulinism by Intravenous Acute Insulin Response Tests and Selective Pancreatic Arterial Calcium Stimulation J. Clin. Endocrinol. Metab., January 1, 2004; 89(1): 288 - 296. [Abstract] [Full Text] [PDF]

				T. Tsuboi, G. da Silva Xavier, I. Leclerc, and G. A. Rutter 5'-AMP-activated Protein Kinase Controls Insulin-containing Secretory Vesicle Dynamics J. Biol. Chem., December 26, 2003; 278(52): 52042 - 52051. [Abstract] [Full Text] [PDF]

				S. Yamada, M. Komatsu, Y. Sato, K. Yamauchi, T. Aizawa, and I. Kojima Nutrient Modulation of Palmitoylated 24-Kilodalton Protein in Rat Pancreatic Islets Endocrinology, December 1, 2003; 144(12): 5232 - 5241. [Abstract] [Full Text] [PDF]

				A. P. Babenko and J. Bryan SUR Domains That Associate with and Gate KATP Pores Define a Novel Gatekeeper J. Biol. Chem., October 24, 2003; 278(43): 41577 - 41580. [Abstract] [Full Text] [PDF]

				M. J. Riedel, P. Boora, D. Steckley, G. de Vries, and P. E. Light Kir6.2 Polymorphisms Sensitize {beta}-Cell ATP-Sensitive Potassium Channels to Activation by Acyl CoAs: A Possible Cellular Mechanism for Increased Susceptibility to Type 2 Diabetes? Diabetes, October 1, 2003; 52(10): 2630 - 2635. [Abstract] [Full Text] [PDF]

				P. S. Thornton, C. MacMullen, A. Ganguly, E. Ruchelli, L. Steinkrauss, A. Crane, L. Aguilar-Bryan, and C. A. Stanley Clinical and Molecular Characterization of a Dominant Form of Congenital Hyperinsulinism Caused by a Mutation in the High-Affinity Sulfonylurea Receptor Diabetes, September 1, 2003; 52(9): 2403 - 2410. [Abstract] [Full Text] [PDF]

				T. K. Graves and P. M. Hinkle Ca2+-Induced Ca2+ Release in the Pancreatic {beta}-Cell: Direct Evidence of Endoplasmic Reticulum Ca2+ Release Endocrinology, August 1, 2003; 144(8): 3565 - 3574. [Abstract] [Full Text] [PDF]

				Y.-W. Lin, T. Jia, A. M. Weinsoft, and S.-L. Shyng Stabilization of the Activity of ATP-sensitive Potassium Channels by Ion Pairs Formed between Adjacent Kir6.2 Subunits J. Gen. Physiol., July 28, 2003; 122(2): 225 - 237. [Abstract] [Full Text] [PDF]

				R. Davis-Taber, E. J. Molinari, R. J. Altenbach, K. L. Whiteaker, C.-C. Shieh, G. Rotert, S. A. Buckner, J. Malysz, I. Milicic, J. S. McDermott, et al. [125I]A-312110, a Novel High-Affinity 1,4-Dihydropyridine ATP-sensitive K+ Channel Opener: Characterization and Pharmacology of Binding Mol. Pharmacol., July 1, 2003; 64(1): 143 - 153. [Abstract] [Full Text] [PDF]

				J. H Koeslag, P. T Saunders, and E. Terblanche A reappraisal of the blood glucose homeostat which comprehensively explains the type 2 diabetes mellitus-syndrome X complex J. Physiol., June 1, 2003; 549(2): 333 - 346. [Abstract] [Full Text] [PDF]

				R. S Lam, E. M App, D. Nahirney, A. J Szkotak, M. A Vieira-Coelho, M. King, and M. Duszyk Regulation of Cl- secretion by {alpha}2-adrenergic receptors in mouse colonic epithelium J. Physiol., April 15, 2003; 548(2): 475 - 484. [Abstract] [Full Text] [PDF]

				M. E. Doyle and J. M. Egan Pharmacological Agents That Directly Modulate Insulin Secretion Pharmacol. Rev., March 1, 2003; 55(1): 105 - 131. [Abstract] [Full Text] [PDF]

				E. A. Cartier, S. Shen, and S.-L. Shyng Modulation of the Trafficking Efficiency and Functional Properties of ATP-sensitive Potassium Channels through a Single Amino Acid in the Sulfonylurea Receptor J. Biol. Chem., February 21, 2003; 278(9): 7081 - 7090. [Abstract] [Full Text] [PDF]