Handbook of Ion Channels

672 Pages·2015·41.633 MB·English

by  Jie Zheng, Matthew C. Trudeau

HANDBOOK OF
ION CHANNELS
© 2015 by Taylor & Francis Group, LLC
© 2015 by Taylor & Francis Group, LLC
K15171_Book.indb 2 12/19/2014 6:54:20 PM
HANDBOOK OF
ION CHANNELS
Edited by
Jie Zheng
University of California at Davis, USA
Matthew C. Trudeau
University of Maryland, Baltimore, USA
© 2015 by Taylor & Francis Group, LLC
MATLAB® is a trademark of The MathWorks, Inc. and is used with permission. The MathWorks does not warrant the accuracy of the text or exercises in
this book. This book’s use or discussion of MATLAB® software or related products does not constitute endorsement or sponsorship by The MathWorks
of a particular pedagogical approach or particular use of the MATLAB® software.
Cover Image. The background is a starburst dendrogram representing the relationship of 143 different ion channels in the human genome. The fore-
ground is the x-ray crystal structure of the sodium channel NavAb. Courtesy of William Catterall.
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Contents
Foreword: Early days of ion channels ix
Preface xiii
Editors xv
Contributors xvii
PART I BASIC CONCEPTS 1
1. Electricity, nerves, batteries: A short history 3
Clay M. Armstrong
2. Ion selectivity and conductance 13
Dorothy M. Kim, Jason G. McCoy, and Crina M. Nimigean
3. Basic mechanisms of voltage sensing 25
Sandipan Chowdhury and Baron Chanda
4. Ligand-dependent gating mechanism 41
William N. Zagotta
5. Mechanosensitive channels and their emerging gating mechanisms 53
Sergei Sukharev and Andriy Anishkin
PART II ION CHANNEL METHODS 69
6. Patch clamping and single-channel analysis 71
León D. Islas
7. Models of ion channel gating 83
Frank T. Horrigan and Toshinori Hoshi
8. Utilizing Markov chains to model ion channel sequence variation and kinetics 103
Anthony Fodor
9. Investigation of ion channel structure using fluorescence spectroscopy 113
Rikard Blunck
10. A practical guide to solving the structure of an ion channel protein 135
Tahmina Rahman and Declan A. Doyle
11. Structural study of ion channels by cryo-electron microscopy 149
Qiu-Xing Jiang and Liang Shi
12. Rosetta structural modeling 161
Vladimir Yarov-Yarovoy
13. Genetic methods for studying ion channel function in physiology and disease 167
Andrea L. Meredith
14. Ion channel inhibitors 189
Jon Sack and Kenneth S. Eum
15. High-throughput methods for ion channels 199
Haibo Yu and Min Li
PART III ION CHANNEL FAMILIES 211
16. Voltage-gated sodium channels 213
William A. Catterall
17. BK channels 227
Huanghe Yang and Jianmin Cui
© 2015 by Taylor & Francis Group, LLC
vi Contents
18. Inward rectifying potassium channels 241
Monica Sala-Rabanal and Colin G. Nichols
19. Two-pore domain potassium channels 261
Leigh D. Plant and Steve A.N. Goldstein
20. KCNQ channels 275
Nikita Gamper and Mark S. Shapiro
21. Ionotropic glutamate receptors 307
Andrew Plested
22. 5-HT receptors 331
3
Sarah C.R. Lummis
23. GABA receptors 345
A
Trevor G. Smart
24. Cyclic nucleotide–gated channels 361
Michael D. Varnum and Gucan Dai
25. Acid sensing ion channels 383
Cecilia Canessa
26. Degenerin/ENaC channels 395
James D. Stockand
27. TRPC channels 411
Jin-Bin Tian, Dhananjay Thakur, Yungang Lu, and Michael X. Zhu
28. TRPV channels 427
Sharona E. Gordon
29. TRPM channels 433
David D. McKemy
30. TRPML channels 453
Qiong Gao, Xiaoli Zhang, and Haoxing Xu
31. CLC chloride channels and transporters 463
Giovanni Zifarelli and Michael Pusch
32. Ca-activated chloride channels 477
Xiuming Wong and Lily Jan
33. Store-operated CRAC channels 489
Murali Prakriya
PART IV ION CHANNEL REGULATION 503
34. Mechanism of G-protein regulation of K+ channels 505
Rahul Mahajan and Diomedes E. Logothetis
35. Calmodulin regulation of voltage-gated calcium channels and beyond 519
Manu Ben-Johny and David T. Yue
36. Phosphorylation of voltage-gated ion channels 531
James S. Trimmer and Hiroaki Misonou
37. Alternative splicing 545
Andrea L. Meredith
38. Single transmembrane regulatory subunits of voltage-gated potassium channels 557
Anatoli Lvov and William R. Kobertz
© 2015 by Taylor & Francis Group, LLC
Contents vii
PART V ION CHANNEL PHYSIOLOGY AND DISEASES 575
39. Ion channels of the heart 577
Donald M. Bers and Eleonora Grandi
40. Ion channels in pain 595
J.P. Johnson, Jr.
41. CLC-related proteins in diseases 611
Allan H. Bretag and Linlin Ma
42. Cystic fibrosis and the CFTR anion channel 627
Yoshiro Sohma and Tzyh-Chang Hwang
43. Drugs targeting ion channels 649
KeWei Wang
Index 661
© 2015 by Taylor & Francis Group, LLC
© 2015 by Taylor & Francis Group, LLC
K15171_Book.indb 2 12/19/2014 6:54:20 PM
Foreword: Early days of ion channels
Throughout their long scientific history, the concepts of cellular Svante Arrhenius (1887) advocated that these ions dissociate
electricity and ion-permeable pores have been principally the fully in strong electrolyte solutions, leading Walther Nernst and
province of scientists with a physical orientation who often called Max Planck (1888–1890), while still in their 20s, to formulate
themselves biophysicists.* Only in the last three decades have ion diffusion equations for dissolved ions in a thick membrane that
channels become accessible to a much broader range of scientists. included electrical forces as well as concentration forces. Nernst
In addition to biophysicists, ion channels are now studied by (1888) gave the membrane potential between two salt solutions
physiologists, biologists, biochemists, anatomists, molecular differing only by the salt concentration. His equation depended
biologists, structural biologists, and physicians. on a difference in mobility between the anion and the cation, and
if one of them was immobile, resulted in the equilibrium equation
THE DAWN OF MOLECULAR PORES we now call the Nernst equation (1889). Nernst and others
suggested that ionic gradients might be the source of animal
General physiologists had already postulated molecular pores in
electricity. Using Nernst’s theory, Ludwig Bernstein (1902, 1912)
membranes several centuries ago. In the late 1700s, osmosis was
(1) hypothesized that muscle and nerve cells are surrounded by a
discovered by Jean-Antoine Nollet. To account for osmosis, Ernst
semipermeable membrane that he called the plasma membrane
von Brücke (1843) postulated pores (Kanäle) no more than a few
and (2) proposed that there is a negative internal resting potential,
water molecules wide. He imagined capillary canals in a porous
caused by potassium selectivity in the membrane. He suggested
membrane. Soon, Carl Ludwig (1852, 1856) adopted Brücke’s pore
that the depolarizing action potential is caused by “an increase in
theory to explain ultrafiltration in the kidney glomerulus, and
the permeability for the impeded ion [chloride] as the result of a
Adolph Fick (1855) devoted much space to discussing diffusion
chemical change in the plasma membrane.” This concept, which
of salt and water in molecular pores of membranes in his paper
he called membrane theory, set the stage for understanding the
proposing Fick’s first and second laws of diffusion. Such important
electricity of excitable cells.
concepts were discussed by these physiologists/physicians before the
size or even the clear existence of molecules was known and before THE AXON AS A CABLE
the word membrane connoted anything but some multicellular
sheet, like an epithelium, or even a sheet of parchment. In the mid-1800s, Lord Kelvin developed the equations for
Nevertheless, from 1850 onward, mechanistic books of physiology decrement of electrical signals in submarine cables. Ludimar
would discuss the possibility of semipermeability and membrane Hermann regarded nerve and muscle fibers as core conductors
pores in an early section on general physiology as an explanation similar to cables. He used flow of current down the axis and
for osmosis and filtration. German books used the word Kanäle through the membrane to explain electrotonus in nerve in many
and English books said pore. In each generation, various new publications including his famous Handbuch der Physiologie
investigators propounded and were given credit for the pore (1879). The cable ideas were given their contemporary form in the
theory, including, for example, in the 1920s and 1930s, Leonor later original works of Cole, Hodgkin, Rushton, Lorente de Nó,
Michaelis of Michaelis–Menten kinetics. From his experiments Rall, and others (1920–1970).
on artificial collodion membranes, Michaelis (1925) proposed that
permeation of small ions might be controlled both by the charge YOUNG HODGKIN
on the pore and by the pore diameter relative to hydrated ions.
Alan Hodgkin (1914–1998) came to Trinity College, Cambridge,
ANIMAL ELECTRICITY as an undergraduate in 1932. He was extroverted and liberal,
and had a brilliant mind. He was persuaded to study physiology.
Again in the late 1700s, phenomena of animal electricity were Trinity College had many leading scientists and an extraordinary
first described and debated by Luigi Galvani, Alessandro Volta, tradition in mechanistic thinking about the action potential.
Benjamin Franklin, and others. The electric eel soon became Keith-Lucas, Edgar Lord Adrian, and William Rushton formed
a clear exemplar. Starting in 1848, Emil du Bois-Reymond one Trinity lineage. After his studies, Hodgkin took up the
discovered the propagated action potential, and Hermann von problem of how the action potential propagates. One school of
Helmholtz measured its conduction velocity in the nerve. For thought (Joseph Erlanger), which Hodgkin called the St. Louis
many decades, this velocity measurement would be made with school, held that the propagated impulse is a chemical reaction
elaborate mechanical devices that could close and open contact occurring inside the axon, whereas the external electrical
switches in the right sequence first to a stimulator and then to a action potential is simply an epiphenomenon that reports the
galvanometer recording from extracellular electrodes. Michael fundamental chemical changes going on inside. In contrast,
Faraday (1834) had postulated that salts contain charged particles the Cambridge school thought the potentials and currents were
and gave the names ion, anion, and cation to them. Eventually, essential for propagation and held to Bernstein’s membrane
theory. Working with frog and crab nerves in 1935 and 1936,
Hodgkin (1937a, b) showed that local circuit currents can flow
* The ideas of this essay are described and documented much more fully in Hille
(2001). forward across a cold-blocked region of nerve into the unexcited
© 2015 by Taylor & Francis Group, LLC
x Foreword: Early days of ion channels
region to lower the threshold for excitation ahead. His two And the final paper cast all the kinetic discoveries as a kinetic
papers, “Evidence for electrical transmission in nerve” stood in model and showed that the model predicts all the electrical
contrast to the St. Louis view. Then he took a year abroad, visiting responses (Hodgkin and Huxley 1952d). Huxley had the idea of
the Herbert Gasser lab in New York. Gasser had introduced representing the gating processes in terms of m3 h and n4, and
improved electronic methods to neurophysiology, the cathode he calculated the predicted action potentials for months on his
ray oscilloscope, high-impedance cathode followers, and high mechanical hand calculator combining cable theory with the new
differential-rejection amplifiers—techniques that Hodgkin time-varying conductances.
absorbed and soon reconstructed in Cambridge. Hodgkin also This final paper introduced the concept of a Boltzmann
visited and worked with Kenneth Cole and Howard Curtis in the distribution affecting the disposition of hypothetical regulatory
Woods Hole Oceanographic Institution for a month, learning charged particles that we now call gating charges. Presciently,
to use the squid giant axon and having his first experience at the model corresponded to four sets of charged particles that we
experimenting side by side with other scientists. now identify as four voltage sensors. It was a disappointment
to Hodgkin that the model had too little to say about how the
HUXLEY JOINS HODGKIN ions crossed the membrane and how this was gated. There was
nothing about mechanisms of selectivity and permeation. The
Andrew Huxley (1917–2012) began in Trinity College as an
words channel and pore were not used. Only in one later work
undergraduate in 1935. He was introverted and precise, had
of Hodgkin and Keynes (1955) on flux ratios did a permeation
exceptional patience, and was already very well versed in
concept come up. They wrote:
machining, designing and building instruments, numerical
methods, and optics. In 1939, Hodgkin invited him to go to
The very large departures from the independence relation
Plymouth to undertake experiments on the British squid. In this
described in this paper can be explained by assuming that K+
first-ever clear recording of the intracellular action potential, ions tend to move through the membrane in narrow channels, or
they discovered that the voltage spike had a considerable along chains of sites such as might be provided by the negative
overshoot beyond 0 mV (Hodgkin and Huxley 1939), unlike charges of a cation exchange resin…. The interaction between
the prediction of Bernstein’s theory. They were 21 and 25 years potassium ions is of the kind expected in a system in which ions
old. War in Europe stopped this work within weeks and both move through the membrane in single file.
investigators joined the war effort, with Hodgkin designing and
Despite the very impressive experiments and theory behind this
testing shorter-wavelength radar and Huxley in the gunnery
latter idea (so deferentially and cautiously stated!), it was almost
calculating trajectories for ordnance. They acquired a new
another ten years before other investigators gave the channel
intensity, urgency, and drive in their work habits. The Plymouth
concept serious thought and began to exploit the voltage clamp
lab was destroyed, and only in 1947 was it rebuilt. Hodgkin
in earnest again. After their brilliant partnership and perfect
wanted to test a Na+ hypothesis for the overshoot, and since
synergy, Hodgkin and Huxley then independently turned away to
Huxley was not available, Bernard Katz joined him in 1947 for
other important physiological problems.
the successful proof (Hodgkin and Katz 1949). The next year,
Hodgkin visited Cole again and saw the introduction of an
axial wire into the giant axon and the application of feedback to THE ION CHANNEL ERA
make current clamp and voltage clamp. Immediately, Hodgkin
and Huxley joined forces again to do their famous experiments Ion channels in a more modern sense had their birth in Clay
(1948–1950) with voltage clamp, and during 1951 they Armstrong’s mind, and very quickly I followed, thinking along the
completed a marathon of analysis, modeling, and calculations— same lines. In 1964, Clay had become a postdoctoral fellow (with
more than 60 years ago. Cole), working on squid giant axons, and I began as a graduate
Their first paper from this work showed that the voltage student to voltage-clamp frog nodes of Ranvier (as taught to me by
clamp measures the same currents as the more familiar current Fred A. Dodge). Our preconception was that the action potential
clamp, gave the peak and steady-state current-voltage relations, uses two very distinct gated permeation mechanisms called Na+
and refined methodological details such as series resistance channels and K+ channels. They are macromolecular aqueous pores
compensation (Hodgkin et al. 1952). The second paper revealed made of protein. Charges, potentials, and mechanical intera ctions
that time-varying inward and outward currents could be at the atomic level govern and catalyze the passage of ions. Gating
separated into components carried by Na+ and by K+ (Hodgkin is a conformational change of the protein. We coined words like
and Huxley 1952a). The changes of Na+ current with Na+ inner and outer vestibules, selectivity filter, gating current, and
concentration obeyed the independence principle of Hodgkin voltage sensor, placing the gate at the cytoplasmic end of the pore.
and Katz (1949). The third paper developed the concept of We built our own apparatus and digitized and analyzed ionic
instantaneous conductance, showing that the current-carrying currents on the first laboratory computers. There may have been
mechanisms obey Ohm’s Law and could be represented as time- only a dozen people actually interested in these questions. Only
varying Na+ and K conductances and each with Nernstian driving gradually did we and many others advance enough evidence that
forces (Hodgkin and Huxley 1952b). The fourth paper discovered such more molecular channel ideas could be asserted with certainty.
that the sodium conductance has two kinetic properties that they The most important technical leaps in the field came when voltage
called activation and inactivation (Hodgkin and Huxley 1952c). clamp became available to thousands of people by the development
© 2015 by Taylor & Francis Group, LLC