Evolution of the voltage sensor domain of the voltage-sensitive phosphoinositide phosphatase VSP/TPTE suggests a role as a proton channel in eutherian mammals

Molecular Biology and Evolution

Volumn 29, Issue 9, 2012, Pages 2147-2155

  Sutton, Keith A ^a   Jungnickel, Melissa K ^a   Jovine, Luca ^b   Florman, Harvey M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

ion channel; phosphoinositide phosphatase; proton channel; sperm; voltage sensor domain

Indexed keywords

CATION CHANNEL; HISTIDINE; MEMBRANE PROTEIN; POLYPHOSPHOINOSITIDE; PROTON;

ARTICLE; ELECTRIC POTENTIAL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; ORTHOLOGY; PLACENTAL MAMMALS; RADIATION; WASTE; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; EVOLUTION, MOLECULAR; HUMANS; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PATCH-CLAMP TECHNIQUES; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; PROTON PUMPS; PTEN PHOSPHOHYDROLASE; SEQUENCE ALIGNMENT;

DANIO RERIO; DEUTEROSTOMIA; EUTHERIA; PRIMATES;

EID: 84865469887     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss083     Document Type: Article

References (71)

1. Alabi AA, Bahamonde MI, Jung HJ, Kim JI, Swartz KJ. 2007. Portability of paddle motif function and pharmacology in voltage sensors. Nature 450:370-375. (Pubitemid 350126744)
2. Armstrong CM, Bezanilla F. 1973. Currents related to movement of the gating particles of the sodium channels. Nature 242:459-461.
3. Balla T. 2006. Phosphoinositide-derived messengers in endocrine signaling. J Endocrinol. 188:135-153. (Pubitemid 43273804)
4. Bezanilla F. 2008. How membrane proteins sense voltage. Nat Rev Mol Cell Biol. 9:323-332. (Pubitemid 351430853)
5. Breckenridge LJ, Almers W. 1987. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 328:814-817. (Pubitemid 17125959)
6. Capasso M, DeCoursey TE, Dyer MJ. 2011. pH regulation and beyond: unanticipated functions for the voltage-gated proton channel, HVCN1. Trends Cell Biol. 21:20-28.
7. Chen H, Rossier C, Morris MA, Scott HS, Gos A, Bairoch A, Antonarakis SE. 1999. A testis-specific gene, TPTE, encodes a putative transmembrane tyrosine phosphatase and maps to the pericentromeric region of human chromosomes 21 and 13, and to chromosomes 15, 22, and Y. Hum Genet. 105:399-409.
8. ChetwyndAP, ScottKA,Mokrab Y, SansomMS. 2008.CGDB: a database of membrane protein/lipid interactions by coarse-grained molecular dynamics simulations. Mol Membr Biol. 25:662-669.
9. DeCoursey TE. 2008. Voltage-gated proton channels: what's next? J Physiol. 586:5305-5324.
10. DeCoursey TE, Cherny VV. 2007. Pharmacology of voltage-gated proton channels. Curr Pharm Des. 13:2400-2420.
11. Eddy EM. 2006. The spermatozoon. In: Neill J, editor. The physiology of reproduction. San Diego (CA): Elsevier. p. 3-54.
12. Elinder F, Arhem P, Larsson HP. 2001. Localization of the extracellular end of the voltage sensor S4 in a potassium channel. Biophys J. 80:1802-1809. (Pubitemid 32280995)
13. Florman HM, Ducibella T. 2006. Fertilization in mammals. In: Neill JD, editor. Physiology of reproduction. San Diego (CA): Elsevier. p. 55-112.
14. Guipponi M, Tapparel C, Jousson O, et al. (11 co-authors). 2001. The murine orthologue of the Golgi-localized TPTE protein provides clues to the evolutionary history of the human TPTE gene family. Hum Genet. 109:569-575. (Pubitemid 34051410)
15. Halaszovich CR, Schreiber DN, Oliver D. 2009. Ci-VSP is a depolarization-activated phosphatidylinositol-4,5-bisphosphate and phosphatidylinositol-3,4,5-trisphosphate 5'-phosphatase. J Biol Chem. 284:2106-2113.
16. Hille B. 2001. Ionic channels of excitable membranes. Sunderland (MA): Sinauer Associates Inc.
17. Hossain MI, Iwasaki H, Okochi Y, Chahine M, Higashijima S, Nagayama K, Okamura Y. 2008. Enzyme domain affects the movement of the voltage sensor in ascidian and zebrafish voltage-sensing phosphatases. J Biol Chem. 283:18248-18259.
18. Hughes AL. 2008. The origin of adaptive phenotypes. Proc Natl Acad Sci USA. 105:13193-13194.
19. Hutton JC. 1982. The internal pH and membrane potential of the insulin-secretory granule. Biochem J. 204:171-178. (Pubitemid 12054031)
20. Iwasaki H, Murata Y, Kim Y, Hossain MI, Worby CA, Dixon JE, McCormack T, Sasaki T, Okamura Y. 2008. A voltage-sensing phosphatase, Ci-VSP, which shares sequence identity with PTEN, dephosphorylates phosphatidylinositol 4,5-bisphosphate. Proc Natl Acad Sci USA. 105:7970-7975. (Pubitemid 351904691)
21. Izumi H, Marian T, Inaba K, Oka Y, Morisawa M. 1999. Membrane hyperpolarization by sperm-activating and-attracting factor increases cAMP level and activates sperm motility in the ascidian Ciona intestinalis. Dev Biol. 213:246-256. (Pubitemid 29444337)
22. Jiang Y, Ruta V, Chen J, Lee A, MacKinnon R. 2003. The principle of gating charge movement in a voltage-dependent K + channel. Nature 423:42-48. (Pubitemid 36569578)
23. Jones S, Zhang X, Parsons DW, et al. (36 co-authors). 2008. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321:1801-1806.
24. Krieger E, Darden T, Nabuurs SB, Finkelstein A, Vriend G. 2004. Making optimal use of empirical energy functions: force-field parameterization in crystal space. Proteins 57:678-683. (Pubitemid 39626989)
25. Krieger E, Joo K, Lee J, Lee J, Raman S, Thompson J, Tyka M, Baker D, Karplus K. 2009. Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins 77(Supp l):9:114-122.
26. Kumanovics A, Levin G, Blount P. 2002. Family ties of gated pores: evolution of the sensor module. FASEB J. 16:1623-1629. (Pubitemid 35154645)
27. Laughlin SB, de Ruyter van Steveninck RR, Anderson JC. 1998. The metabolic cost of neural information. Nat Neurosci. 1:36-41. (Pubitemid 128652639)
28. Lee MA, Storey BT. 1989. Endpoint of first stage of zona pellucidainduced acrosome reaction in mouse spermatozoa characterized by acrosomal H + and Ca2 + permeability: population and single cell kinetics. Gamete Res. 24:303-326. (Pubitemid 19277781)
29. Leslie NR, Yang X, Downes CP, Weijer CJ. 2007. PtdIns(3,4,5)P(3)- dependent and-independent roles for PTEN in the control of cell migration. Curr Biol. 17:115-125. (Pubitemid 46107842)
30. Loh YP, Tam WW, Russell JT. 1984. Measurement of delta pH and membrane potential in secretory vesicles isolated from bovine pituitary intermediate lobe. J Biol Chem. 259:8238-8245. (Pubitemid 14090571)
31. Long SB, Tao X, Campbell EB, MacKinnon R. 2007. Atomic structure of a voltage-dependent K + channel in a lipid membrane-like environment. Nature 450:376-382. (Pubitemid 350126743)
32. Maeda Y, Ide T, Koike M, Uchiyama Y, Kinoshita T. 2008. GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus. Nat Cell Biol. 10:1135-1145.
33. Meizel S, Deamer DW. 1978. The pH of the hamster sperm acrosome. J Histochem Cytochem. 26:98-105. (Pubitemid 8287278)
34. Mellman I, Fuchs R, Helenius A. 1986. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem. 55:663-700. (Pubitemid 16070784)
35. Muller J, Szklarczyk D, Julien P, et al. (11 co-authors). 2010. eggNOG v2.0: extending the evolutionary genealogy of genes with enhanced non-supervised orthologous groups, species and functional annotations. Nucleic Acids Res. 38:D190-D195.
36. Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y. 2005. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435:1239-1243. (Pubitemid 40943089)
37. Murata Y, Okamura Y. 2007. Depolarization activates the phosphoinositide phosphatase Ci-VSP, as detected in Xenopus oocytes coexpressing sensors of PIP2. J Physiol. 583:875-889. (Pubitemid 47423706)
38. Nakanishi T, Ikawa M, Yamada S, Toshimori K, Okabe M. 2001. Alkalinization of acrosome measured by GFP as a pH indicator and its relation to sperm capacitation. Dev Biol. 237:222-231. (Pubitemid 32844317)
39. Noda M, Ikeda T, Kayano T, Suzuki H, Takeshima H, Kurasaki M, Takahashi H, Numa S. 1986. Existence of distinct sodium channel messenger RNAs in rat brain. Nature 320:188-192. (Pubitemid 16105158)
40. Ogasawara M, Sasaki M, Nakazawa N, Nishino A, Okamura Y. 2011. Gene expression profile of Ci-VSP in juveniles and adult blood cells of ascidian. Gene Expr Patterns. 11:233-238.
41. Okamura Y. 2007. Biodiversity of voltage sensor domain proteins. Pflugers Arch. 454:361-371. (Pubitemid 46742437)
42. Okamura Y, Murata Y, Iwasaki H. 2009. Voltage-sensing phosphatase: actions and potentials. J Physiol. 587:513-520.
43. Parsons DW, Jones S, Zhang X, et al. (33 co-authors). 2008. An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807-1812.
44. Parsons DW, Li M, Zhang X, et al. (47 co-authors). 2011. The genetic landscape of the childhood cancer medulloblastoma. Science 331:435-439.
45. Payandeh J, Scheuer T, Zheng N, Catterall WA. 2011. The crystal structure of a voltage-gated sodium channel. Nature 475:353-358.
46. Pleasance ED, Cheetham RK, Stephens PJ, et al. (45 co-authors). 2010. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 463:191-196.
47. Pond SL, Frost SD. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531-2533. (Pubitemid 40731616)
48. Pond SL, Frost SD, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679. (Pubitemid 40424796)
49. Ramsey IS, Mokrab Y, Carvacho I, Sands ZA, Sansom MS, Clapham DE. 2010. An aqueous H + permeation pathway in the voltage-gated proton channel Hv1. Nat Struct Mol Biol. 17:869-875.
50. Ramsey IS, Moran MM, Chong JA, Clapham DE. 2006. A voltagegated proton-selective channel lacking the pore domain. Nature 440:1213-1216.
51. Ratzan WJ, Evsikov AV, Okamura Y, Jaffe LA. 2011. Voltage sensitive phosphoinositide phosphatases of Xenopus: their tissue distribution and voltage dependence. J Cell Physiol. 226: 2740-2746.
52. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tully JL, Clapham DE. 2001. A sperm ion channel required for sperm motility and male fertility. Nature 413:603-609. (Pubitemid 32964054)
53. Reymond A, Marigo V, Yaylaoglu MB, et al. (13 co-authors). 2002. Human chromosome 21 gene expression atlas in the mouse. Nature 420:582-586. (Pubitemid 35477052)
54. Sakata S, Hossain MI, Okamura Y. 2011. Coupling of the phosphatase activity of Ci-VSP to its voltage sensor activity over the entire range of voltage sensitivity. J Physiol. 589: 2687-2705.
55. Sasaki M, Takagi M, Okamura Y. 2006. A voltage sensor-domain protein is a voltage-gated proton channel. Science 312:589-592.
56. Schapiro FB, Grinstein S. 2000. Determinants of the pH of the Golgi complex. J Biol Chem. 275:21025-21032. (Pubitemid 30481791)
57. Sjoblom T, Jones S, Wood LD, et al. (29 co-authors). 2006. The consensus coding sequences of human breast and colorectal cancers. Science 314:268-274. (Pubitemid 44571966)
58. Starace DM, Bezanilla F. 2001. Histidine scanning mutagenesis of basic residues of the S4 segment of the Shaker K + channel. J Gen Physiol. 117:469-490. (Pubitemid 32441397)
59. Starace DM, Bezanilla F. 2004. A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427: 548-553. (Pubitemid 38209113)
60. Starace DM, Stefani E, Bezanilla F. 1997. Voltage-dependent proton transport by the voltage sensor of the Shaker K + channel. Neuron 19:1319-1327. (Pubitemid 28030550)
61. Suh B-C, Hille B. 2008. PIP2 is a necessary cofactor for ion channel function: how and why? Annu Rev Biophys Biomol Struct. 37: 175-195.
62. Swartz KJ. 2008. Sensing voltage across lipid membranes. Nature 456:891-897.
63. Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R. 2010. A gating charge transfer center in voltage sensors. Science 328: 67-73.
64. Tapparel C, Reymond A, Girardet C, Guillou L, Lyle R, Lamon C, Hutter P, Antonarakis SE. 2003. The TPTE gene family: cellular expression, subcellular localization and alternative splicing. Gene 323:189-199. (Pubitemid 37501099)
65. Walker SM, Downes CP, Leslie NR. 2001. TPIP: a novel phosphoinositide 3-phosphatase. Biochem J. 360:277-283. (Pubitemid 33151322)
66. Wang D, King SM, Quill TA, Doolittle LK, Garbers DL. 2003. A new sperm-specific Na( +)/H( +) Exchanger required for sperm motility and fertility. Nat Cell Biol. 5:1117-1122. (Pubitemid 37509120)
67. Wood ML, Schow EV, Freites JA, White SH, Tombola F, Tobias DJ. 2011. Water wires in atomistic models of the Hv1 proton channel. Biochim Biophys Acta. 1818:286-293.
68. Worby CA, Dixon JE. 2005. Phosphoinositide phosphatases: emerging roles as voltage sensors? Mol Interv. 5:274-277. (Pubitemid 41595458)
69. Wu MM, Grabe M, Adams S, Tsien RY, Moore HP, Machen TE. 2001. Mechanisms of pH regulation in the regulated secretory pathway. J Biol Chem. 276:33027-33035.
70. Wu Y, Dowbenko D, Pisabarro MT, Dillard-Telm L, Koeppen H, Lasky LA. 2001. PTEN 2, a Golgi-associated testis-specific homologue of the PTEN tumor suppressor lipid phosphatase. J Biol Chem. 276:21745-21753.
71. Yokoyama S, Tada T, Zhang H, Britt L. 2008. Elucidation of phenotypic adaptations: molecular analyses of dim-light vision proteins in vertebrates. Proc Natl Acad Sci USA. 105: 13480-13485.