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Original Article |
sas8{at}columbia.edu
Members of the HCN channel family generate hyperpolarization-activated cation currents (Ih) that are directly regulated by cAMP and contribute to pacemaker activity in heart and brain. The four HCN isoforms show distinct but overlapping patterns of expression in different tissues. Here, we report that HCN1 and HCN2, isoforms coexpressed in neocortex and hippocampus that differ markedly in their biophysical properties, coassemble to generate heteromultimeric channels with novel properties. When expressed in Xenopus oocytes, HCN1 channels activate 5–10-fold more rapidly than HCN2 channels. HCN1 channels also activate at voltages that are 10–20 mV more positive than those required to activate HCN2. In cell-free patches, the steady-state activation curve of HCN1 channels shows a minimal shift in response to cAMP (+4 mV), whereas that of HCN2 channels shows a pronounced shift (+17 mV). Coexpression of HCN1 and HCN2 yields Ih currents that activate with kinetics and a voltage dependence that tend to be intermediate between those of HCN1 and HCN2 homomers, although the coexpressed channels do show a relatively large shift by cAMP (+14 mV). Neither the kinetics, steady-state voltage dependence, nor cAMP dose–response curve for the coexpressed Ih can be reproduced by the linear sum of independent populations of HCN1 and HCN2 homomers. These results are most simply explained by the formation of heteromeric channels with novel properties. The properties of these heteromeric channels closely resemble the properties of Ih in hippocampal CA1 pyramidal neurons, cells that coexpress HCN1 and HCN2. Finally, differences in Ih channel properties recorded in cell-free patches versus intact oocytes are shown to be due, in part, to modulation of Ih by basal levels of cAMP in intact cells.
Key Words: potassium channel • gating • heteromultimer • Ih • cAMP
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N. Tran, C. Proenza, V. Macri, F. Petigara, E. Sloan, S. Samler, and E. A. Accili A Conserved Domain in the NH2 Terminus Important for Assembly and Functional Expression of Pacemaker Channels J. Biol. Chem., November 8, 2002; 277(46): 43588 - 43592. [Abstract] [Full Text] [PDF]
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D. V. Vasilyev and M. E. Barish Postnatal Development of the Hyperpolarization-Activated Excitatory Current Ih in Mouse Hippocampal Pyramidal Neurons J. Neurosci., October 15, 2002; 22(20): 8992 - 9004. [Abstract] [Full Text] [PDF]
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C. Proenza, N. Tran, D. Angoli, K. Zahynacz, P. Balcar, and E. A. Accili Different Roles for the Cyclic Nucleotide Binding Domain and Amino Terminus in Assembly and Expression of Hyperpolarization-activated, Cyclic Nucleotide-gated Channels J. Biol. Chem., August 9, 2002; 277(33): 29634 - 29642. [Abstract] [Full Text] [PDF]
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G. C. Demontis, A. Moroni, B. Gravante, C. Altomare, B. Longoni, L. Cervetto, and D. DiFrancesco Functional characterisation and subcellular localisation of HCN1 channels in rabbit retinal rod photoreceptors J. Physiol., July 1, 2002; 542(1): 89 - 97. [Abstract] [Full Text] [PDF]
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 T. Xue, E. Marban, and R. A. Li Dominant-Negative Suppression of HCN1- and HCN2-Encoded Pacemaker Currents by an Engineered HCN1 Construct: Insights Into Structure-Function Relationships and Multimerization Circ. Res., June 28, 2002; 90(12): 1267 - 1273. [Abstract] [Full Text] [PDF]
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J. E Sirois, C. Lynch III, and D. A Bayliss Convergent and reciprocal modulation of a leak K+ current and Ih by an inhalational anaesthetic and neurotransmitters in rat brainstem motoneurones J. Physiol., June 15, 2002; 541(3): 717 - 729. [Abstract] [Full Text] [PDF]
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A. Brewster, R. A. Bender, Y. Chen, C. Dube, M. Eghbal-Ahmadi, and T. Z. Baram Developmental Febrile Seizures Modulate Hippocampal Gene Expression of Hyperpolarization-Activated Channels in an Isoform- and Cell-Specific Manner J. Neurosci., June 1, 2002; 22(11): 4591 - 4599. [Abstract] [Full Text] [PDF]
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H. Neuhoff, A. Neu, B. Liss, and J. Roeper Ih Channels Contribute to the Different Functional Properties of Identified Dopaminergic Subpopulations in the Midbrain J. Neurosci., February 15, 2002; 22(4): 1290 - 1302. [Abstract] [Full Text] [PDF]
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C. Proenza, D. Angoli, E. Agranovich, V. Macri, and E. A. Accili Pacemaker Channels Produce an Instantaneous Current J. Biol. Chem., February 8, 2002; 277(7): 5101 - 5109. [Abstract] [Full Text] [PDF]
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 E. A. Accili, C. Proenza, M. Baruscotti, and D. DiFrancesco From Funny Current to HCN Channels: 20 Years of Excitation Physiology, February 1, 2002; 17(1): 32 - 37. [Abstract] [Full Text] [PDF]
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B. S. Rothberg, K. S. Shin, P. S. Phale, and G. Yellen Voltage-Controlled Gating at the Intracellular Entrance to a Hyperpolarization-Activated Cation Channel J. Gen. Physiol., January 1, 2002; 119(1): 83 - 91. [Abstract] [Full Text] [PDF]
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 A. U. BRAUER, N. E. SAVASKAN, M. H. P. KOLE, M. PLASCHKE, L. M. MONTEGGIA, E. J. NESTLER, E. SIMBURGER, R. A. DEISZ, O. NINNEMANN, and R. NITSCH Molecular and functional analysis of hyperpolarization-activated pacemaker channels in the hippocampus after entorhinal cortex lesion FASEB J, December 1, 2001; 15(14): 2689 - 2701. [Abstract] [Full Text] [PDF]
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J. Wang, S. Chen, and S. A. Siegelbaum Regulation of Hyperpolarization-Activated Hcn Channel Gating and Camp Modulation Due to Interactions of Cooh Terminus and Core Transmembrane Regions J. Gen. Physiol., September 1, 2001; 118(3): 237 - 250. [Abstract] [Full Text] [PDF]
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J. Qu, A. Barbuti, L. Protas, B. Santoro, I. S. Cohen, and R. B. Robinson HCN2 Overexpression in Newborn and Adult Ventricular Myocytes : Distinct Effects on Gating and Excitability Circ. Res., July 6, 2001; 89 (1): e8 - e14. [Abstract] [Full Text] [PDF]
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I. A. Greenwood and S. A. Prestwich Characteristics of hyperpolarization-activated cation currents in portal vein smooth muscle cells Am J Physiol Cell Physiol, April 1, 2002; 282(4): C744 - C753. [Abstract] [Full Text] [PDF]
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