The “Sweet” Side of Ion Channels

Chapter
Part of the Reviews of Physiology, Biochemistry and Pharmacology book series (REVIEWS, volume 167)

Abstract

Ion channels play a crucial role in cell functioning, contributing to transmembrane potential and participating in cell signalling and homeostasis. To fulfil highly specialised functions, cells have developed various mechanisms to regulate channel expression and activity at particular subcellular loci, and alteration of ion channel regulation can lead to serious disorders. Glycosylation, one of the most common forms of co- and post-translational protein modification, is rapidly emerging as a fundamental mechanism not only controlling the proper folding of nascent channels but also their subcellular localisation, gating and function. Moreover, studies on various channel subtypes have revealed that glycosylation represents an important determinant by which other signalling pathways modulate channel activity. The discovery of detailed mechanisms of regulation of ion channels by glycosylation provides new insights in the physiology of ion channels and may allow developing new pharmaceutics for the treatment of ion channel-related disorders.

Keywords

Ion channel N-linked glycosylation O-linked glycosylation Glycan Protein glycosylation 

Abbreviations

ASIC

Acid-sensing ion channel

B35

Neuroblastoma cell

CAD

Cath.a-differentiated cell

Cav

Voltage-gated calcium channel

CDG

Congenital disorders of glycosylation

CFTR

Cystic fibrosis transmembrane conductance regulator

CHO

Chinese hamster ovary cell

ER

Endoplasmic reticulum

ERGIC

ER–Golgi intermediate compartment

GalNAc

N-acetylgalactosamine

GlcNAc-1-P

N-acetylglucosamine-1-phosphate

HCN

Hyperpolarisation-activated cyclic nucleotide-gated channel

K2P

Two-pore domain potassium channel

Kv

Voltage-gated potassium channel

LacNAc

N-acetyllactosamine

LQT

Long QT syndrome

M1

Murine cortical collecting duct

Nav

Voltage-gated sodium channel

O-GalNAc

Mucin-type O-glycan

Panx

Pannexin channel

PNGase F

Peptide-N-glycosidase F

Sf9

Spodoptera frugiperda cell

SKBR3

Human breast cancer cell

ST3Gal4

Beta-galactoside alpha-2,3-sialyltransferase 4

ST8sia2

Alpha-2,8-sialyltransferase 2

TPC

Two-pore channel

TRIP8b

Tetratricopeptide repeat-containing Rab8b-interacting protein

TRP

Transient receptor potential channel

TRPC

Transient receptor potential canonical channel

TRPM

Transient receptor potential melastatin channel

TRPP

Transient receptor potential polycystin channel

TRPV

Transient receptor potential vanilloid channel

α-benzyl-GalNAc

1-Benzyl-2-acetamido-2-deoxy-α-d-galactopyranoside

References

  1. Abriel H, Staub O (2005) Ubiquitylation of ion channels. Physiology (Bethesda) 20:398–407Google Scholar
  2. Accardi A, Picollo A (2010) CLC channels and transporters: proteins with borderline personalities. Biochim Biophys Acta 1798:1457–1464PubMedCentralPubMedGoogle Scholar
  3. Ahrens J, Foadi N, Eberhardt A, Haeseler G, Dengler R, Leffler A, Muhlenhoff M, Gerardy-Schahn R, Leuwer M (2011) Defective polysialylation and sialylation induce opposite effects on gating of the skeletal Na+ channel NaV1.4 in Chinese hamster ovary cells. Pharmacology 87:311–317PubMedGoogle Scholar
  4. Altier C, Garcia-Caballero A, Simms B, You H, Chen L, Walcher J, Tedford HW, Hermosilla T, Zamponi GW (2011) The Cavbeta subunit prevents RFP2-mediated ubiquitination and proteasomal degradation of L-type channels. Nat Neurosci 14:173–180PubMedGoogle Scholar
  5. Ambrosi C, Gassmann O, Pranskevich JN, Boassa D, Smock A, Wang J, Dahl G, Steinem C, Sosinsky GE (2010) Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J Biol Chem 285:24420–24431PubMedCentralPubMedGoogle Scholar
  6. Andrade A, Sandoval A, Gonzalez-Ramirez R, Lipscombe D, Campbell KP, Felix R (2009) The alpha(2)delta subunit augments functional expression and modifies the pharmacology of Ca(V)1.3 L-type channels. Cell Calcium 46:282–292PubMedGoogle Scholar
  7. Aoki-Kinoshita KF (2013) Introduction to informatics in glycoprotein analysis. Methods Mol Biol 951:257–267PubMedGoogle Scholar
  8. Arniges M, Fernandez-Fernandez JM, Albrecht N, Schaefer M, Valverde MA (2006) Human TRPV4 channel splice variants revealed a key role of ankyrin domains in multimerization and trafficking. J Biol Chem 281:1580–1586PubMedGoogle Scholar
  9. Atiba-Davies M, Noben-Trauth K (2007) TRPML3 and hearing loss in the varitint-waddler mouse. Biochim Biophys Acta 1772:1028–1031PubMedGoogle Scholar
  10. Baek JH, Rubinstein M, Scheuer T, Trimmer JS (2014) Reciprocal changes in phosphorylation and methylation of Mammalian brain sodium channels in response to seizures. J Biol Chem 289:15363–15373PubMedGoogle Scholar
  11. Bal T, McCormick DA (1997) Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h). J Neurophysiol 77:3145–3156PubMedGoogle Scholar
  12. Baranova A, Ivanov D, Petrash N, Pestova A, Skoblov M, Kelmanson I, Shagin D, Nazarenko S, Geraymovych E, Litvin O, Tiunova A, Born TL, Usman N, Staroverov D, Lukyanov S, Panchin Y (2004) The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83:706–716PubMedGoogle Scholar
  13. Barchi RL, Cohen SA, Murphy LE (1980) Purification from rat sarcolemma of the saxitoxin-binding component of the excitable membrane sodium channel. Proc Natl Acad Sci U S A 77:1306–1310PubMedCentralPubMedGoogle Scholar
  14. Bennett E, Urcan MS, Tinkle SS, Koszowski AG, Levinson SR (1997) Contribution of sialic acid to the voltage dependence of sodium channel gating. A possible electrostatic mechanism. J Gen Physiol 109:327–343PubMedCentralPubMedGoogle Scholar
  15. Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA (2012) Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22:736–756PubMedCentralPubMedGoogle Scholar
  16. Benson DW, MacRae CA, Vesely MR, Walsh EP, Seidman JG, Seidman CE, Satler CA (1996) Missense mutation in the pore region of HERG causes familial long QT syndrome. Circulation 93:1791–1795PubMedGoogle Scholar
  17. Beurrier C, Congar P, Bioulac B, Hammond C (1999) Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J Neurosci 19:599–609PubMedGoogle Scholar
  18. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization-activated cation channels: from genes to function. Physiol Rev 89:847–885PubMedGoogle Scholar
  19. Bird EV, Christmas CR, Loescher AR, Smith KG, Robinson PP, Black JA, Waxman SG, Boissonade FM (2013) Correlation of Nav1.8 and Nav1.9 sodium channel expression with neuropathic pain in human subjects with lingual nerve neuromas. Mol Pain 9:52PubMedCentralPubMedGoogle Scholar
  20. Bittner S, Budde T, Wiendl H, Meuth SG (2010) From the background to the spotlight: TASK channels in pathological conditions. Brain Pathol 20:999–1009PubMedGoogle Scholar
  21. Boassa D, Ambrosi C, Qiu F, Dahl G, Gaietta G, Sosinsky G (2007) Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J Biol Chem 282:31733–31743PubMedGoogle Scholar
  22. Boassa D, Qiu F, Dahl G, Sosinsky G (2008) Trafficking dynamics of glycosylated pannexin 1 proteins. Cell Commun Adhes 15:119–132PubMedCentralPubMedGoogle Scholar
  23. Bourinet E, Alloui A, Monteil A, Barrere C, Couette B, Poirot O, Pages A, McRory J, Snutch TP, Eschalier A, Nargeot J (2005) Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. EMBO J 24:315–324PubMedCentralPubMedGoogle Scholar
  24. Brooks NL, Corey MJ, Schwalbe RA (2006) Characterization of N-glycosylation consensus sequences in the Kv3.1 channel. FEBS J 273:3287–3300PubMedGoogle Scholar
  25. Cai Y, Maeda Y, Cedzich A, Torres VE, Wu G, Hayashi T, Mochizuki T, Park JH, Witzgall R, Somlo S (1999) Identification and characterization of polycystin-2, the PKD2 gene product. J Biol Chem 274:28557–28565PubMedGoogle Scholar
  26. Cain SM, Tyson JR, Jones KL, Snutch TP (2014) Thalamocortical neurons display suppressed burst-firing due to an enhanced I current in a genetic model of absence epilepsy. Pflugers Arch. doi:10.1007/s00424-014-1549-4
  27. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang KT, Lin P, Xiao R, Wang C, Zhu Y, Lin Y, Wyatt CN, Parrington J, Ma J, Evans AM, Galione A, Zhu MX (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459:596–600PubMedCentralPubMedGoogle Scholar
  28. Calvete JJ, Sanz L (2008) Analysis of O-glycosylation. Methods Mol Biol 446:281–292PubMedGoogle Scholar
  29. Carbone E, Calorio C, Vandael DH (2014) T-type channel-mediated neurotransmitter release. Pflugers Arch 466:677–687PubMedGoogle Scholar
  30. Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26:13–25PubMedGoogle Scholar
  31. Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3:a003947PubMedCentralPubMedGoogle Scholar
  32. Cha SK, Ortega B, Kurosu H, Rosenblatt KP, Kuro-O M, Huang CL (2008) Removal of sialic acid involving Klotho causes cell-surface retention of TRPV5 channel via binding to galectin-1. Proc Natl Acad Sci U S A 105:9805–9810PubMedCentralPubMedGoogle Scholar
  33. Chandrasekhar KD, Lvov A, Terrenoire C, Gao GY, Kass RS, Kobertz WR (2011) O-glycosylation of the cardiac I(Ks) complex. J Physiol 589:3721–3730PubMedCentralPubMedGoogle Scholar
  34. Chang Q, Hoefs S, van der Kemp AW, Topala CN, Bindels RJ, Hoenderop JG (2005) The beta-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310:490–493PubMedGoogle Scholar
  35. Chang XB, Mengos A, Hou YX, Cui L, Jensen TJ, Aleksandrov A, Riordan JR, Gentzsch M (2008) Role of N-linked oligosaccharides in the biosynthetic processing of the cystic fibrosis membrane conductance regulator. J Cell Sci 121:2814–2823PubMedCentralPubMedGoogle Scholar
  36. Chen Y, Parker WD, Wang K (2014) The role of T-type calcium channel genes in absence seizures. Front Neurol 5:45PubMedCentralPubMedGoogle Scholar
  37. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O’Riordan CR, Smith AE (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63:827–834PubMedGoogle Scholar
  38. Cheng X, Shen D, Samie M, Xu H (2010) Mucolipins: Intracellular TRPML1-3 channels. FEBS Lett 584:2013–2021PubMedCentralPubMedGoogle Scholar
  39. Cheong E, Shin HS (2014) T-type Ca2+ channels in absence epilepsy. Pflugers Arch 466:719–734PubMedGoogle Scholar
  40. Chu XP, Grasing KA, Wang JQ (2014) Acid-sensing ion channels contribute to neurotoxicity. Transl Stroke Res 5:69–78PubMedGoogle Scholar
  41. Cohen DM (2006) Regulation of TRP channels by N-linked glycosylation. Semin Cell Dev Biol 17:630–637PubMedGoogle Scholar
  42. Comer FI, Vosseller K, Wells L, Accavitti MA, Hart GW (2001) Characterization of a mouse monoclonal antibody specific for O-linked N-acetylglucosamine. Anal Biochem 293:169–177PubMedGoogle Scholar
  43. Conti LR, Radeke CM, Vandenberg CA (2002) Membrane targeting of ATP-sensitive potassium channel. Effects of glycosylation on surface expression. J Biol Chem 277:25416–25422PubMedGoogle Scholar
  44. Coste B, Crest M, Delmas P (2007) Pharmacological dissection and distribution of NaN/Nav1.9, T-type Ca2+ currents, and mechanically activated cation currents in different populations of DRG neurons. J Gen Physiol 129:57–77PubMedCentralPubMedGoogle Scholar
  45. Cotella D, Radicke S, Bortoluzzi A, Ravens U, Wettwer E, Santoro C, Sblattero D (2010) Impaired glycosylation blocks DPP10 cell surface expression and alters the electrophysiology of Ito channel complex. Pflugers Arch 460:87–97PubMedGoogle Scholar
  46. Cronin NB, O’Reilly A, Duclohier H, Wallace BA (2005) Effects of deglycosylation of sodium channels on their structure and function. Biochemistry 44:441–449PubMedGoogle Scholar
  47. Crunelli V, Cope DW, Hughes SW (2006) Thalamic T-type Ca2+ channels and NREM sleep. Cell Calcium 40:175–190PubMedCentralPubMedGoogle Scholar
  48. Cuajungco MP, Samie MA (2008) The Varitint-Waddler mouse phenotypes and the TRPML3 ion channel mutation: cause and consequence. Pflugers Arch 457:463–473PubMedGoogle Scholar
  49. Dai XQ, Kolic J, Marchi P, Sipione S, Macdonald PE (2009) SUMOylation regulates Kv2.1 and modulates pancreatic beta-cell excitability. J Cell Sci 122:775–779PubMedGoogle Scholar
  50. Davies A, Hendrich J, Van Minh AT, Wratten J, Douglas L, Dolphin AC (2007) Functional biology of the alpha(2)delta subunits of voltage-gated calcium channels. Trends Pharmacol Sci 28:220–228PubMedGoogle Scholar
  51. Davis MJ, Wu X, Nurkiewicz TR, Kawasaki J, Gui P, Hill MA, Wilson E (2001) Regulation of ion channels by protein tyrosine phosphorylation. Am J Physiol Heart Circ Physiol 281:H1835–H1862PubMedGoogle Scholar
  52. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358:761–764PubMedGoogle Scholar
  53. Di Palma F, Belyantseva IA, Kim HJ, Vogt TF, Kachar B, Noben-Trauth K (2002) Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice. Proc Natl Acad Sci U S A 99:14994–14999PubMedCentralPubMedGoogle Scholar
  54. Dib-Hajj SD, Tyrrell L, Black JA, Waxman SG (1998) NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci U S A 95:8963–8968PubMedCentralPubMedGoogle Scholar
  55. Dib-Hajj S, Black JA, Cummins TR, Waxman SG (2002) NaN/Nav1.9: a sodium channel with unique properties. Trends Neurosci 25:253–259PubMedGoogle Scholar
  56. Dietrich A, Mederos y Schnitzler M, Emmel J, Kalwa H, Hofmann T, Gudermann T (2003) N-linked protein glycosylation is a major determinant for basal TRPC3 and TRPC6 channel activity. J Biol Chem 278:47842–47852Google Scholar
  57. Ding WG, Xie Y, Toyoda F, Matsuura H (2014) Improved functional expression of human cardiac kv1.5 channels and trafficking-defective mutants by low temperature treatment. PLoS One 9:e92923PubMedCentralPubMedGoogle Scholar
  58. Dogrul A, Gardell LR, Ossipov MH, Tulunay FC, Lai J, Porreca F (2003) Reversal of experimental neuropathic pain by T-type calcium channel blockers. Pain 105:159–168PubMedGoogle Scholar
  59. Drel VR, Mashtalir N, Ilnytska O, Shin J, Li F, Lyzogubov VV, Obrosova IG (2006) The leptin-deficient (ob/ob) mouse: a new animal model of peripheral neuropathy of type 2 diabetes and obesity. Diabetes 55:3335–3343PubMedGoogle Scholar
  60. Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J, Brownlee M (2000) Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci U S A 97:12222–12226PubMedCentralPubMedGoogle Scholar
  61. Du D, Yang H, Norring SA, Bennett ES (2014) In-silico modeling of glycosylation modulation dynamics in hERG ion channels and cardiac electrical signals. IEEE J Biomed Health Inform 18:205–214PubMedGoogle Scholar
  62. Duan DD (2011) The ClC-3 chloride channels in cardiovascular disease. Acta Pharmacol Sin 32:675–684PubMedCentralPubMedGoogle Scholar
  63. Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R (2002) X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415:287–294PubMedGoogle Scholar
  64. Dziegielewska B, Gray LS, Dziegielewski J (2014) T-type calcium channels blockers as new tools in cancer therapies. Pflugers Arch 466:801–810PubMedGoogle Scholar
  65. Ednie AR, Bennett ES (2012) Modulation of voltage-gated ion channels by sialylation. Compr Physiol 2:1269–1301PubMedGoogle Scholar
  66. Ednie AR, Horton KK, Wu J, Bennett ES (2013) Expression of the sialyltransferase, ST3Gal4, impacts cardiac voltage-gated sodium channel activity, refractory period and ventricular conduction. J Mol Cell Cardiol 59:117–127PubMedGoogle Scholar
  67. Enyedi P, Czirjak G (2010) Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol Rev 90:559–605PubMedGoogle Scholar
  68. Esko JD, Bertozzi CR (2009) Chemical tools for inhibiting glycosylation. Essentials Glycobiol. doi:10.1007/s00424-014-1549-4
  69. Fjell J, Hjelmstrom P, Hormuzdiar W, Milenkovic M, Aglieco F, Tyrrell L, Dib-Hajj S, Waxman SG, Black JA (2000) Localization of the tetrodotoxin-resistant sodium channel NaN in nociceptors. Neuroreport 11:199–202PubMedGoogle Scholar
  70. Francois A, Laffray S, Pizzoccaro A, Eschalier A, Bourinet E (2014) T-type calcium channels in chronic pain: mouse models and specific blockers. Pflugers Arch 466:707–717PubMedGoogle Scholar
  71. Freeze HH, Kranz C (2010) Endoglycosidase and glycoamidase release of N-linked glycans. Curr Protoc Protein Sci 12:Unit12.4Google Scholar
  72. Gadotti VM, You H, Petrov RR, Berger ND, Diaz P, Zamponi GW (2013) Analgesic effect of a mixed T-type channel inhibitor/CB2 receptor agonist. Mol Pain 9:32PubMedCentralPubMedGoogle Scholar
  73. Galione A, Evans AM, Ma J, Parrington J, Arredouani A, Cheng X, Zhu MX (2009) The acid test: the discovery of two-pore channels (TPCs) as NAADP-gated endolysosomal Ca(2+) release channels. Pflugers Arch 458:869–876PubMedCentralPubMedGoogle Scholar
  74. Glozman R, Okiyoneda T, Mulvihill CM, Rini JM, Barriere H, Lukacs GL (2009) N-glycans are direct determinants of CFTR folding and stability in secretory and endocytic membrane traffic. J Cell Biol 184:847–862PubMedCentralPubMedGoogle Scholar
  75. Gong Q, Anderson CL, January CT, Zhou Z (2002) Role of glycosylation in cell surface expression and stability of HERG potassium channels. Am J Physiol Heart Circ Physiol 283:H77–H84PubMedGoogle Scholar
  76. Gregory RJ, Cheng SH, Rich DP, Marshall J, Paul S, Hehir K, Ostedgaard L, Klinger KW, Welsh MJ, Smith AE (1990) Expression and characterization of the cystic fibrosis transmembrane conductance regulator. Nature 347:382–386PubMedGoogle Scholar
  77. Gregory RJ, Rich DP, Cheng SH, Souza DW, Paul S, Manavalan P, Anderson MP, Welsh MJ, Smith AE (1991) Maturation and function of cystic fibrosis transmembrane conductance regulator variants bearing mutations in putative nucleotide-binding domains 1 and 2. Mol Cell Biol 11:3886–3893PubMedCentralPubMedGoogle Scholar
  78. Grimm C, Hassan S, Wahl-Schott C, Biel M (2012) Role of TRPML and two-pore channels in endolysosomal cation homeostasis. J Pharmacol Exp Ther 342:236–244PubMedGoogle Scholar
  79. Guggino WB, Stanton BA (2006) New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat Rev Mol Cell Biol 7:426–436PubMedGoogle Scholar
  80. Hagglund P, Matthiesen R, Elortza F, Hojrup P, Roepstorff P, Jensen ON, Bunkenborg J (2007) An enzymatic deglycosylation scheme enabling identification of core fucosylated N-glycans and O-glycosylation site mapping of human plasma proteins. J Proteome Res 6:3021–3031PubMedGoogle Scholar
  81. Hall MK, Cartwright TA, Fleming CM, Schwalbe RA (2011) Importance of glycosylation on function of a potassium channel in neuroblastoma cells. PLoS One 6:e19317PubMedCentralPubMedGoogle Scholar
  82. Hall MK, Weidner DA, Chen J, Bernetski CJ, Schwalbe RA (2013) Glycan structures contain information for the spatial arrangement of glycoproteins in the plasma membrane. PLoS One 8:e75013PubMedCentralPubMedGoogle Scholar
  83. Hall MK, Weidner DA, Bernetski CJ, Schwalbe RA (2014) N-Linked glycan site occupancy impacts the distribution of a potassium channel in the cell body and outgrowths of neuronal-derived cells. Biochim Biophys Acta 1840:595–604PubMedGoogle Scholar
  84. Hang HC, Yu C, Kato DL, Bertozzi CR (2003) A metabolic labeling approach toward proteomic analysis of mucin-type O-linked glycosylation. Proc Natl Acad Sci U S A 100:14846–14851PubMedCentralPubMedGoogle Scholar
  85. Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O (2011) Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu Rev Biochem 80:825–858PubMedCentralPubMedGoogle Scholar
  86. Hartzell HC, Yu K, Xiao Q, Chien LT, Qu Z (2009) Anoctamin/TMEM16 family members are Ca2+−activated Cl- channels. J Physiol 587:2127–2139PubMedCentralPubMedGoogle Scholar
  87. Hegle AP, Nazzari H, Roth A, Angoli D, Accili EA (2010) Evolutionary emergence of N-glycosylation as a variable promoter of HCN channel surface expression. Am J Physiol Cell Physiol 298:C1066–C1076PubMedGoogle Scholar
  88. Heifetz A, Keenan RW, Elbein AD (1979) Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase. Biochemistry 18:2186–2192PubMedGoogle Scholar
  89. Hille B (2001) Ion channels of excitable membranes. Massachusetts U.S.A, Sinauer Associates, SunderlandGoogle Scholar
  90. Hofherr A, Wagner C, Fedeles S, Somlo S, Kottgen M (2014) N-Glycosylation determines the abundance of the transient receptor potential channel TRPP2. J Biol Chem 289:14854–14867PubMedGoogle Scholar
  91. Hooper R, Churamani D, Brailoiu E, Taylor CW, Patel S (2011) Membrane topology of NAADP-sensitive two-pore channels and their regulation by N-linked glycosylation. J Biol Chem 286:9141–9149PubMedCentralPubMedGoogle Scholar
  92. Hossler P, Khattak SF, Li ZJ (2009) Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology 19:936–949PubMedGoogle Scholar
  93. Huang CL (2004) The transient receptor potential superfamily of ion channels. J Am Soc Nephrol 15:1690–1699PubMedGoogle Scholar
  94. Huang J, Han C, Estacion M, Vasylyev D, Hoeijmakers JG, Gerrits MM, Tyrrell L, Lauria G, Faber CG, Dib-Hajj SD, Merkies IS, Waxman SG (2014) Gain-of-function mutations in sodium channel Na(v)1.9 in painful neuropathy. Brain 137:1627–1642PubMedGoogle Scholar
  95. Huguenard JR (1996) Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol 58:329–348PubMedGoogle Scholar
  96. Huguenard JR, Prince DA (1992) A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J Neurosci 12:3804–3817PubMedGoogle Scholar
  97. Ismailov II, Benos DJ (1995) Effects of phosphorylation on ion channel function. Kidney Int 48:1167–1179PubMedGoogle Scholar
  98. Jacus MO, Uebele VN, Renger JJ, Todorovic SM (2012) Presynaptic Cav3.2 channels regulate excitatory neurotransmission in nociceptive dorsal horn neurons. J Neurosci 32:9374–9382PubMedCentralPubMedGoogle Scholar
  99. Jahnel R, Dreger M, Gillen C, Bender O, Kurreck J, Hucho F (2001) Biochemical characterization of the vanilloid receptor 1 expressed in a dorsal root ganglia derived cell line. Eur J Biochem 268:5489–5496PubMedGoogle Scholar
  100. Jentsch TJ (2008) CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. Crit Rev Biochem Mol Biol 43:3–36PubMedGoogle Scholar
  101. Jing L, Jiang YQ, Jiang Q, Wang B, Chu XP, Zha XM (2011) The interaction between the first transmembrane domain and the thumb of ASIC1a is critical for its N-glycosylation and trafficking. PLoS One 6:e26909PubMedCentralPubMedGoogle Scholar
  102. Jing L, Chu XP, Jiang YQ, Collier DM, Wang B, Jiang Q, Snyder PM, Zha XM (2012) N-glycosylation of acid-sensing ion channel 1a regulates its trafficking and acidosis-induced spine remodeling. J Neurosci 32:4080–4091PubMedCentralPubMedGoogle Scholar
  103. Kadurin I, Golubovic A, Leisle L, Schindelin H, Grunder S (2008) Differential effects of N-glycans on surface expression suggest structural differences between the acid-sensing ion channel (ASIC) 1a and ASIC1b. Biochem J 412:469–475PubMedGoogle Scholar
  104. Kantamneni S, Wilkinson KA, Henley JM (2011) Ubiquitin regulation of neuronal excitability. Nat Neurosci 14:126–128PubMedCentralPubMedGoogle Scholar
  105. Kedei N, Szabo T, Lile JD, Treanor JJ, Olah Z, Iadarola MJ, Blumberg PM (2001) Analysis of the native quaternary structure of vanilloid receptor 1. J Biol Chem 276:28613–28619PubMedGoogle Scholar
  106. Khosravani H, Zamponi GW (2006) Voltage-gated calcium channels and idiopathic generalized epilepsies. Physiol Rev 86:941–966PubMedGoogle Scholar
  107. Kim JB (2014) Channelopathies. Korean J Pediatr 57:1–18PubMedCentralPubMedGoogle Scholar
  108. Kim D, Park D, Choi S, Lee S, Sun M, Kim C, Shin HS (2003) Thalamic control of visceral nociception mediated by T-type Ca2+ channels. Science 302:117–119PubMedGoogle Scholar
  109. Kim HJ, Li Q, Tjon-Kon-Sang S, So I, Kiselyov K, Muallem S (2007) Gain-of-function mutation in TRPML3 causes the mouse Varitint-Waddler phenotype. J Biol Chem 282:36138–36142PubMedGoogle Scholar
  110. Kiselyov K, Chen J, Rbaibi Y, Oberdick D, Tjon-Kon-Sang S, Shcheynikov N, Muallem S, Soyombo A (2005) TRP-ML1 is a lysosomal monovalent cation channel that undergoes proteolytic cleavage. J Biol Chem 280:43218–43223PubMedGoogle Scholar
  111. Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13–23PubMedGoogle Scholar
  112. Kuro-o M (2012) Klotho in health and disease. Curr Opin Nephrol Hypertens 21:362–368PubMedGoogle Scholar
  113. Laedermann CJ, Syam N, Pertin M, Decosterd I, Abriel H (2013) beta1- and beta3- voltage-gated sodium channel subunits modulate cell surface expression and glycosylation of Nav1.7 in HEK293 cells. Front Cell Neurosci 7:137Google Scholar
  114. Launay P, Fleig A, Perraud AL, Scharenberg AM, Penner R, Kinet JP (2002) TRPM4 is a Ca2+−activated nonselective cation channel mediating cell membrane depolarization. Cell 109:397–407PubMedGoogle Scholar
  115. Leipold E, Liebmann L, Korenke GC, Heinrich T, Giesselmann S, Baets J, Ebbinghaus M, Goral RO, Stodberg T, Hennings JC, Bergmann M, Altmuller J, Thiele H, Wetzel A, Nurnberg P, Timmerman V, De Jonghe P, Blum R, Schaible HG, Weis J, Heinemann SH, Hubner CA, Kurth I (2013) A de novo gain-of-function mutation in SCN11A causes loss of pain perception. Nat Genet 45:1399–1404PubMedGoogle Scholar
  116. Leunissen EH, Nair AV, Bull C, Lefeber DJ, van Delft FL, Bindels RJ, Hoenderop JG (2013) The epithelial calcium channel TRPV5 is regulated differentially by klotho and sialidase. J Biol Chem 288:29238–29246PubMedCentralPubMedGoogle Scholar
  117. Levitan IB (1994) Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu Rev Physiol 56:193–212PubMedGoogle Scholar
  118. Lippiat JD, Smith AJ (2012) The CLC-5 2Cl(−)/H(+) exchange transporter in endosomal function and Dent’s disease. Front Physiol 3:449PubMedCentralPubMedGoogle Scholar
  119. Lotshaw DP (2007) Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K+ channels. Cell Biochem Biophys 47:209–256PubMedGoogle Scholar
  120. Mant A, Williams S, Roncoroni L, Lowry E, Johnson D, O’Kelly I (2013) N-glycosylation-dependent control of functional expression of background potassium channels K2P3.1 and K2P9.1. J Biol Chem 288:3251–3264PubMedCentralPubMedGoogle Scholar
  121. Marangoudakis S, Andrade A, Helton TD, Denome S, Castiglioni AJ, Lipscombe D (2012) Differential ubiquitination and proteasome regulation of Ca(V)2.2 N-type channel splice isoforms. J Neurosci 32:10365–10369PubMedCentralPubMedGoogle Scholar
  122. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58PubMedGoogle Scholar
  123. Mesirca P, Torrente AG, Mangoni ME (2014) T-type channels in the sino-atrial and atrioventricular pacemaker mechanism. Pflugers Arch 466:791–799PubMedGoogle Scholar
  124. Messner DJ, Catterall WA (1985) The sodium channel from rat brain. Separation and characterization of subunits J Biol Chem 260:10597–10604Google Scholar
  125. Michikawa T, Hamanaka H, Otsu H, Yamamoto A, Miyawaki A, Furuichi T, Tashiro Y, Mikoshiba K (1994) Transmembrane topology and sites of N-glycosylation of inositol 1,4,5-trisphosphate receptor. J Biol Chem 269:9184–9189PubMedGoogle Scholar
  126. Miller JA, Agnew WS, Levinson SR (1983) Principal glycopeptide of the tetrodotoxin/saxitoxin binding protein from Electrophorus electricus: isolation and partial chemical and physical characterization. Biochemistry 22:462–470PubMedGoogle Scholar
  127. Montpetit ML, Stocker PJ, Schwetz TA, Harper JM, Norring SA, Schaffer L, North SJ, Jang-Lee J, Gilmartin T, Head SR, Haslam SM, Dell A, Marth JD, Bennett ES (2009) Regulated and aberrant glycosylation modulate cardiac electrical signaling. Proc Natl Acad Sci U S A 106:16517–16522PubMedCentralPubMedGoogle Scholar
  128. Morelle W, Michalski JC (2007) Analysis of protein glycosylation by mass spectrometry. Nat Protoc 2:1585–1602PubMedGoogle Scholar
  129. Moremen KW, Tiemeyer M, Nairn AV (2012) Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 13:448–462PubMedCentralPubMedGoogle Scholar
  130. Morenilla-Palao C, Pertusa M, Meseguer V, Cabedo H, Viana F (2009) Lipid raft segregation modulates TRPM8 channel activity. J Biol Chem 284:9215–9224PubMedCentralPubMedGoogle Scholar
  131. Morgan AJ, Galione A (2014) Two-pore channels (TPCs): current controversies. Bioessays 36:173–183PubMedGoogle Scholar
  132. Much B, Wahl-Schott C, Zong X, Schneider A, Baumann L, Moosmang S, Ludwig A, Biel M (2003) Role of subunit heteromerization and N-linked glycosylation in the formation of functional hyperpolarization-activated cyclic nucleotide-gated channels. J Biol Chem 278:43781–43786PubMedGoogle Scholar
  133. Newby LJ, Streets AJ, Zhao Y, Harris PC, Ward CJ, Ong AC (2002) Identification, characterization, and localization of a novel kidney polycystin-1-polycystin-2 complex. J Biol Chem 277:20763–20773PubMedGoogle Scholar
  134. Nilius B, Carbone E (2014) Amazing T-type calcium channels: updating functional properties in health and disease. Pflugers Arch 466:623–626PubMedGoogle Scholar
  135. Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12:218PubMedCentralPubMedGoogle Scholar
  136. Nilius B, Vennekens R (2006) From cardiac cation channels to the molecular dissection of the transient receptor potential channel TRPM4. Pflugers Arch 453:313–321PubMedGoogle Scholar
  137. Nilius B, Talavera K, Owsianik G, Prenen J, Droogmans G, Voets T (2005) Gating of TRP channels: a voltage connection? J Physiol 567:35–44PubMedCentralPubMedGoogle Scholar
  138. Nilius B, Mahieu F, Karashima Y, Voets T (2007) Regulation of TRP channels: a voltage-lipid connection. Biochem Soc Trans 35:105–108PubMedGoogle Scholar
  139. Norring SA, Ednie AR, Schwetz TA, Du D, Yang H, Bennett ES (2013) Channel sialic acids limit hERG channel activity during the ventricular action potential. FASEB J 27:622–631PubMedGoogle Scholar
  140. O’Riordan CR, Lachapelle AL, Marshall J, Higgins EA, Cheng SH (2000) Characterization of the oligosaccharide structures associated with the cystic fibrosis transmembrane conductance regulator. Glycobiology 10:1225–1233PubMedGoogle Scholar
  141. Ohtsubo K, Marth JD (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126:855–867PubMedGoogle Scholar
  142. Orestes P, Osuru HP, McIntire WE, Jacus MO, Salajegheh R, Jagodic MM, Choe W, Lee J, Lee SS, Rose KE, Poiro N, Digruccio MR, Krishnan K, Covey DF, Lee JH, Barrett PQ, Jevtovic-Todorovic V, Todorovic SM (2013) Reversal of neuropathic pain in diabetes by targeting glycosylation of Ca(V)3.2 T-type calcium channels. Diabetes 62:3828–3838PubMedCentralPubMedGoogle Scholar
  143. Palmieri C, Rudraraju B, Monteverde M, Lattanzio L, Gojis O, Brizio R, Garrone O, Merlano M, Syed N, Lo Nigro C, Crook T (2012) Methylation of the calcium channel regulatory subunit alpha2delta-3 (CACNA2D3) predicts site-specific relapse in oestrogen receptor-positive primary breast carcinomas. Br J Cancer 107:375–381PubMedCentralPubMedGoogle Scholar
  144. Patel S, Brailoiu E (2012) Triggering of Ca2+ signals by NAADP-gated two-pore channels: a role for membrane contact sites? Biochem Soc Trans 40:153–157PubMedGoogle Scholar
  145. Patnaik SK, Stanley P (2006) Lectin-resistant CHO glycosylation mutants. Methods Enzymol 416:159–182PubMedGoogle Scholar
  146. Penuela S, Bhalla R, Gong XQ, Cowan KN, Celetti SJ, Cowan BJ, Bai D, Shao Q, Laird DW (2007) Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J Cell Sci 120:3772–3783PubMedGoogle Scholar
  147. Penuela S, Bhalla R, Nag K, Laird DW (2009) Glycosylation regulates pannexin intermixing and cellular localization. Mol Biol Cell 20:4313–4323PubMedCentralPubMedGoogle Scholar
  148. Penuela S, Harland L, Simek J, Laird DW (2014a) Pannexin channels and their links to human disease. Biochem J 461:371–381PubMedGoogle Scholar
  149. Penuela S, Lohman AW, Lai W, Gyenis L, Litchfield DW, Isakson BE, Laird DW (2014b) Diverse post-translational modifications of the pannexin family of channel-forming proteins. Channels (Austin) 8:124–130Google Scholar
  150. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83:117–161PubMedGoogle Scholar
  151. Pertusa M, Madrid R, Morenilla-Palao C, Belmonte C, Viana F (2012) N-glycosylation of TRPM8 ion channels modulates temperature sensitivity of cold thermoreceptor neurons. J Biol Chem 287:18218–18229PubMedCentralPubMedGoogle Scholar
  152. Petersen OH (2002) Cation channels: homing in on the elusive CAN channels. Curr Biol 12:R520–R522PubMedGoogle Scholar
  153. Petrecca K, Atanasiu R, Akhavan A, Shrier A (1999) N-linked glycosylation sites determine HERG channel surface membrane expression. J Physiol 515:41–48PubMedCentralPubMedGoogle Scholar
  154. Powell KL, Cain SM, Snutch TP, O’Brien TJ (2014) Low threshold T-type calcium channels as targets for novel epilepsy treatments. Br J Clin Pharmacol 77:729–739PubMedGoogle Scholar
  155. Proft J, Weiss N (2014) T-type Ca(2+) channels: New players in the aging brain. Commun Integr Biol 7:e28424PubMedCentralPubMedGoogle Scholar
  156. Rajan S, Plant LD, Rabin ML, Butler MH, Goldstein SA (2005) Sumoylation silences the plasma membrane leak K+ channel K2P1. Cell 121:37–47PubMedGoogle Scholar
  157. Recio-Pinto E, Thornhill WB, Duch DS, Levinson SR, Urban BW (1990) Neuraminidase treatment modifies the function of electroplax sodium channels in planar lipid bilayers. Neuron 5:675–684PubMedGoogle Scholar
  158. Roth J, Zuber C, Park S, Jang I, Lee Y, Kysela KG, Le Fourn V, Santimaria R, Guhl B, Cho JW (2010) Protein N-glycosylation, protein folding, and protein quality control. Mol Cells 30:497–506PubMedGoogle Scholar
  159. Rougier JS, Albesa M, Abriel H (2010) Ubiquitylation and SUMOylation of cardiac ion channels. J Cardiovasc Pharmacol 56:22–28PubMedGoogle Scholar
  160. Satler CA, Walsh EP, Vesely MR, Plummer MH, Ginsburg GS, Jacob HJ (1996) Novel missense mutation in the cyclic nucleotide-binding domain of HERG causes long QT syndrome. Am J Med Genet 65:27–35PubMedGoogle Scholar
  161. Satler CA, Vesely MR, Duggal P, Ginsburg GS, Beggs AH (1998) Multiple different missense mutations in the pore region of HERG in patients with long QT syndrome. Hum Genet 102:265–272PubMedGoogle Scholar
  162. Saugstad JA, Roberts JA, Dong J, Zeitouni S, Evans RJ (2004) Analysis of the membrane topology of the acid-sensing ion channel 2a. J Biol Chem 279:55514–55519PubMedCentralPubMedGoogle Scholar
  163. Scanlin TF, Glick MC (1999) Terminal glycosylation in cystic fibrosis. Biochim Biophys Acta 1455:241–253PubMedGoogle Scholar
  164. Scanlin TF, Glick MC (2001) Glycosylation and the cystic fibrosis transmembrane conductance regulator. Respir Res 2:276–279PubMedCentralPubMedGoogle Scholar
  165. Schauer R (1982) Chemistry, metabolism, and biological functions of sialic acids. Adv Carbohydr Chem Biochem 40:131–234PubMedGoogle Scholar
  166. Scheinman SJ (1998) X-linked hypercalciuric nephrolithiasis: clinical syndromes and chloride channel mutations. Kidney Int 53:3–17PubMedGoogle Scholar
  167. Schmidt JW, Catterall WA (1986) Biosynthesis and processing of the alpha subunit of the voltage-sensitive sodium channel in rat brain neurons. Cell 46:437–444PubMedGoogle Scholar
  168. Schmidt JW, Catterall WA (1987) Palmitylation, sulfation, and glycosylation of the alpha subunit of the sodium channel. Role of post-translational modifications in channel assembly. J Biol Chem 262:13713–13723PubMedGoogle Scholar
  169. Schmidt-Rose T, Jentsch TJ (1997) Transmembrane topology of a CLC chloride channel. Proc Natl Acad Sci U S A 94:7633–7638PubMedCentralPubMedGoogle Scholar
  170. Schmieder S, Lindenthal S, Ehrenfeld J (2001) Tissue-specific N-glycosylation of the ClC-3 chloride channel. Biochem Biophys Res Commun 286:635–640PubMedGoogle Scholar
  171. Schmieder S, Bogliolo S, Ehrenfeld J (2007) N-glycosylation of the Xenopus laevis ClC-5 protein plays a role in cell surface expression, affecting transport activity at the plasma membrane. J Cell Physiol 210:479–488PubMedGoogle Scholar
  172. Schwartz PJ, Ackerman MJ (2013) The long QT syndrome: a transatlantic clinical approach to diagnosis and therapy. Eur Heart J 34:3109–3116PubMedGoogle Scholar
  173. Schwarz F, Aebi M (2011) Mechanisms and principles of N-linked protein glycosylation. Curr Opin Struct Biol 21:576–582PubMedGoogle Scholar
  174. Schwetz TA, Norring SA, Bennett ES (2010) N-glycans modulate K(v)1.5 gating but have no effect on K(v)1.4 gating. Biochim Biophys Acta 1798:367–375PubMedGoogle Scholar
  175. Schwetz TA, Norring SA, Ednie AR, Bennett ES (2011) Sialic acids attached to O-glycans modulate voltage-gated potassium channel gating. J Biol Chem 286:4123–4132PubMedCentralPubMedGoogle Scholar
  176. Scott K, Gadomski T, Kozicz T, Morava E (2014) Congenital disorders of glycosylation: new defects and still counting. J Inherit Metab Dis 37:609–617PubMedGoogle Scholar
  177. Sheppard DN, Welsh MJ (1999) Structure and function of the CFTR chloride channel. Physiol Rev 79:S23–S45PubMedGoogle Scholar
  178. Shipston MJ (2011) Ion channel regulation by protein palmitoylation. J Biol Chem 286:8709–8716PubMedCentralPubMedGoogle Scholar
  179. Shipston MJ (2014) Ion channel regulation by protein S-acylation. J Gen Physiol 143:659–678PubMedGoogle Scholar
  180. Sosinsky GE, Boassa D, Dermietzel R, Duffy HS, Laird DW, MacVicar B, Naus CC, Penuela S, Scemes E, Spray DC, Thompson RJ, Zhao HB, Dahl G (2011) Pannexin channels are not gap junction hemichannels. Channels (Austin) 5:193–197Google Scholar
  181. Sotty F, Danik M, Manseau F, Laplante F, Quirion R, Williams S (2003) Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J Physiol 551:927–943PubMedCentralPubMedGoogle Scholar
  182. Syam N, Rougier JS, Abriel H (2014) Glycosylation of TRPM4 and TRPM5 channels: molecular determinants and functional aspects. Front Cell Neurosci 8:52PubMedCentralPubMedGoogle Scholar
  183. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B (2005) Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022–1025PubMedGoogle Scholar
  184. Tarentino AL, Gomez CM, Plummer THJ (1985) Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F. Biochemistry 24:4665–4671PubMedGoogle Scholar
  185. Thanka Christlet TH, Veluraja K (2001) Database analysis of O-glycosylation sites in proteins. Biophys J 80:952–960PubMedCentralPubMedGoogle Scholar
  186. Thomas D, Kiehn J, Katus HA, Karle CA (2003) Defective protein trafficking in hERG-associated hereditary long QT syndrome (LQT2): molecular mechanisms and restoration of intracellular protein processing. Cardiovasc Res 60:235–241PubMedGoogle Scholar
  187. Tian E, Ten Hagen KG (2009) Recent insights into the biological roles of mucin-type O-glycosylation. Glycoconj J 26:325–334PubMedCentralPubMedGoogle Scholar
  188. Todorovic SM, Jevtovic-Todorovic V (2013) Neuropathic pain: role for presynaptic T-type channels in nociceptive signaling. Pflugers Arch 465:921–927PubMedGoogle Scholar
  189. Todorovic SM, Jevtovic-Todorovic V (2014) Targeting of CaV3.2 T-type calcium channels in peripheral sensory neurons for the treatment of painful diabetic neuropathy. Pflugers Arch 466:701–706PubMedGoogle Scholar
  190. Tyrrell L, Renganathan M, Dib-Hajj SD, Waxman SG (2001) Glycosylation alters steady-state inactivation of sodium channel Nav1.9/NaN in dorsal root ganglion neurons and is developmentally regulated. J Neurosci 21:9629–9637PubMedGoogle Scholar
  191. Ufret-Vincenty CA, Baro DJ, Lederer WJ, Rockman HA, Quinones LE, Santana LF (2001a) Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J Biol Chem 276:28197–28203PubMedGoogle Scholar
  192. Ufret-Vincenty CA, Baro DJ, Santana LF (2001b) Differential contribution of sialic acid to the function of repolarizing K(+) currents in ventricular myocytes. Am J Physiol Cell Physiol 281:C464–C474PubMedGoogle Scholar
  193. Van den Steen P, Rudd PM, Dwek RA, Opdenakker G (1998) Concepts and principles of O-linked glycosylation. Crit Rev Biochem Mol Biol 33:151–208PubMedGoogle Scholar
  194. Van Goor F, Straley KS, Cao D, Gonzalez J, Hadida S, Hazlewood A, Joubran J, Knapp T, Makings LR, Miller M, Neuberger T, Olson E, Panchenko V, Rader J, Singh A, Stack JH, Tung R, Grootenhuis PD, Negulescu P (2006) Rescue of DeltaF508-CFTR trafficking and gating in human cystic fibrosis airway primary cultures by small molecules. Am J Physiol Lung Cell Mol Physiol 290:L1117–L1130PubMedGoogle Scholar
  195. Vandewalle A (2002) Diversity within the CLC chloride channel family involved in inherited diseases: from plasma membranes to acidic organelles. Nephrol Dial Transplant 17:1–3PubMedGoogle Scholar
  196. Vandewauw I, Owsianik G, Voets T (2013) Systematic and quantitative mRNA expression analysis of TRP channel genes at the single trigeminal and dorsal root ganglion level in mouse. BMC Neurosci 14:21PubMedCentralPubMedGoogle Scholar
  197. Vannier B, Zhu X, Brown D, Birnbaumer L (1998) The membrane topology of human transient receptor potential 3 as inferred from glycosylation-scanning mutagenesis and epitope immunocytochemistry. J Biol Chem 273:8675–8679PubMedGoogle Scholar
  198. Veldhuis NA, Lew MJ, Abogadie FC, Poole DP, Jennings EA, Ivanusic JJ, Eilers H, Bunnett NW, McIntyre P (2012) N-glycosylation determines ionic permeability and desensitization of the TRPV1 capsaicin receptor. J Biol Chem 287:21765–21772PubMedCentralPubMedGoogle Scholar
  199. Vij N, Zeitlin PL (2006) Regulation of the ClC-2 lung epithelial chloride channel by glycosylation of SP1. Am J Respir Cell Mol Biol 34:754–759PubMedCentralPubMedGoogle Scholar
  200. Voets T, Owsianik G, Janssens A, Talavera K, Nilius B (2007) TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat Chem Biol 3:174–182PubMedGoogle Scholar
  201. Voolstra O, Huber A (2014) Post-Translational Modifications of TRP Channels. Cells 3:258–287PubMedCentralPubMedGoogle Scholar
  202. Voss FK, Ullrich F, Munch J, Lazarow K, Lutter D, Mah N, Andrade-Navarro MA, von Kries JP, Stauber T, Jentsch TJ (2014) Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science 344:634–638PubMedGoogle Scholar
  203. Waithe D, Ferron L, Page KM, Chaggar K, Dolphin AC (2011) Beta-subunits promote the expression of Ca(V)2.2 channels by reducing their proteasomal degradation. J Biol Chem 286:9598–9611PubMedCentralPubMedGoogle Scholar
  204. Wang S, Huang X, Sun D, Xin X, Pan Q, Peng S, Liang Z, Luo C, Yang Y, Jiang H, Huang M, Chai W, Ding J, Geng M (2012) Extensive crosstalk between O-GlcNAcylation and phosphorylation regulates Akt signaling. PLoS One 7:e37427PubMedCentralPubMedGoogle Scholar
  205. Watanabe I, Wang HG, Sutachan JJ, Zhu J, Recio-Pinto E, Thornhill WB (2003) Glycosylation affects rat Kv1.1 potassium channel gating by a combined surface potential and cooperative subunit interaction mechanism. J Physiol 550:51–66PubMedCentralPubMedGoogle Scholar
  206. Watanabe I, Zhu J, Recio-Pinto E, Thornhill WB (2004) Glycosylation affects the protein stability and cell surface expression of Kv1.4 but Not Kv1.1 potassium channels. A pore region determinant dictates the effect of glycosylation on trafficking. J Biol Chem 279:8879–8885PubMedGoogle Scholar
  207. Watanabe I, Zhu J, Sutachan JJ, Gottschalk A, Recio-Pinto E, Thornhill WB (2007) The glycosylation state of Kv1.2 potassium channels affects trafficking, gating, and simulated action potentials. Brain Res 1144:1–18PubMedGoogle Scholar
  208. Weerapana E, Imperiali B (2006) Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16:91R–101RPubMedGoogle Scholar
  209. Weiss N (2012) Cross-talk between TRPML1 channel, lipids and lysosomal storage diseases. Commun Integr Biol 5:111–113PubMedCentralPubMedGoogle Scholar
  210. Weiss N, Koschak A (2014) Pathologies of calcium channels. Springer, HeidelbergGoogle Scholar
  211. Weiss N, Zamponi GW (2013) Control of low-threshold exocytosis by T-type calcium channels. Biochim Biophys Acta 1828:1579–1586PubMedGoogle Scholar
  212. Weiss N, Hameed S, Fernandez-Fernandez JM, Fablet K, Karmazinova M, Poillot C, Proft J, Chen L, Bidaud I, Monteil A, Huc-Brandt S, Lacinova L, Lory P, Zamponi GW, De Waard M (2012a) A Ca(v)3.2/syntaxin-1A signaling complex controls T-type channel activity and low-threshold exocytosis. J Biol Chem 287:2810–2818PubMedCentralPubMedGoogle Scholar
  213. Weiss N, Zamponi GW, De Waard M (2012b) How do T-type calcium channels control low-threshold exocytosis? Commun Integr Biol 5:377–380PubMedCentralPubMedGoogle Scholar
  214. Weiss N, Black SA, Bladen C, Chen L, Zamponi GW (2013) Surface expression and function of Cav3.2 T-type calcium channels are controlled by asparagine-linked glycosylation. Pflugers Arch 465:1159–1170PubMedGoogle Scholar
  215. Wemmie JA, Price MP, Welsh MJ (2006) Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 29:578–586PubMedGoogle Scholar
  216. Wemmie JA, Taugher RJ, Kreple CJ (2013) Acid-sensing ion channels in pain and disease. Nat Rev Neurosci 14:461–471PubMedGoogle Scholar
  217. Wilkars W, Wollberg J, Mohr E, Han M, Chetkovich DM, Bahring R, Bender RA (2014) Nedd4-2 regulates surface expression and may affect N-glycosylation of hyperpolarization-activated cyclic nucleotide-gated (HCN)-1 channels. FASEB J 28:2177–2190PubMedGoogle Scholar
  218. Wirkner K, Hognestad H, Jahnel R, Hucho F, Illes P (2005) Characterization of rat transient receptor potential vanilloid 1 receptors lacking the N-glycosylation site N604. Neuroreport 16:997–1001PubMedGoogle Scholar
  219. Woo SK, Kwon MS, Ivanov A, Geng Z, Gerzanich V, Simard JM (2013) Complex N-glycosylation stabilizes surface expression of transient receptor potential melastatin 4b protein. J Biol Chem 288:36409–36417PubMedGoogle Scholar
  220. Wuhrer M, Deelder AM, Hokke CH (2005a) Protein glycosylation analysis by liquid chromatography-mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 825:124–133PubMedGoogle Scholar
  221. Wuhrer M, Koeleman CA, Hokke CH, Deelder AM (2005b) Protein glycosylation analyzed by normal-phase nano-liquid chromatography–mass spectrometry of glycopeptides. Anal Chem 77:886–894PubMedGoogle Scholar
  222. Xu H, Zhao H, Tian W, Yoshida K, Roullet JB, Cohen DM (2003) Regulation of a transient receptor potential (TRP) channel by tyrosine phosphorylation. SRC family kinase-dependent tyrosine phosphorylation of TRPV4 on TYR-253 mediates its response to hypotonic stress. J Biol Chem 278:11520–11527PubMedGoogle Scholar
  223. Xu H, Fu Y, Tian W, Cohen DM (2006) Glycosylation of the osmoresponsive transient receptor potential channel TRPV4 on Asn-651 influences membrane trafficking. Am J Physiol Renal Physiol 290:F1103–F1109PubMedGoogle Scholar
  224. Yang YC, Tai CH, Pan MK, Kuo CC (2014) The T-type calcium channel as a new therapeutic target for Parkinson’s disease. Pflugers Arch 466:747–755PubMedGoogle Scholar
  225. Zamponi GW, Lory P, Perez-Reyes E (2010) Role of voltage-gated calcium channels in epilepsy. Pflugers Arch 460:395–403PubMedCentralPubMedGoogle Scholar
  226. Zanetta JP, Gouyer V, Maes E, Pons A, Hemon B, Zweibaum A, Delannoy P, Huet G (2000) Massive in vitro synthesis of tagged oligosaccharides in 1-benzyl-2-acetamido-2-deoxy-alpha-D-galactopyranoside treated HT-29 cells. Glycobiology 10:565–575PubMedGoogle Scholar
  227. Zauner G, Kozak RP, Gardner RA, Fernandes DL, Deelder AM, Wuhrer M (2012) Protein O-glycosylation analysis. Biol Chem 393:687–708PubMedGoogle Scholar
  228. Zeevi DA, Frumkin A, Bach G (2007) TRPML and lysosomal function. Biochim Biophys Acta 1772:851–858PubMedGoogle Scholar
  229. Zha Q, Brewster AL, Richichi C, Bender RA, Baram TZ (2008) Activity-dependent heteromerization of the hyperpolarization-activated, cyclic-nucleotide gated (HCN) channels: role of N-linked glycosylation. J Neurochem 105:68–77PubMedCentralPubMedGoogle Scholar
  230. Zhang Y, Hartmann HA, Satin J (1999) Glycosylation influences voltage-dependent gating of cardiac and skeletal muscle sodium channels. J Membr Biol 171:195–207PubMedGoogle Scholar
  231. Zhang YP, Zhang H, Duan DD (2013) Chloride channels in stroke. Acta Pharmacol Sin 34:17–23PubMedCentralPubMedGoogle Scholar
  232. Zhou Z, Gong Q, Epstein ML, January CT (1998) HERG channel dysfunction in human long QT syndrome. Intracellular transport and functional defects J Biol Chem 273:21061–21066Google Scholar
  233. Zhou TT, Zhang ZW, Liu J, Zhang JP, Jiao BH (2012) Glycosylation of the sodium channel beta4 subunit is developmentally regulated and involves in neuritic degeneration. Int J Biol Sci 8:630–639PubMedCentralPubMedGoogle Scholar
  234. Zhu J, Yan J, Thornhill WB (2012) N-glycosylation promotes the cell surface expression of Kv1.3 potassium channels. FEBS J 279:2632–2644PubMedGoogle Scholar
  235. Zong X, Schieder M, Cuny H, Fenske S, Gruner C, Rotzer K, Griesbeck O, Harz H, Biel M, Wahl-Schott C (2009) The two-pore channel TPCN2 mediates NAADP-dependent Ca(2+)-release from lysosomal stores. Pflugers Arch 458:891–899PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Institute of Organic Chemistry and BiochemistryAcademy of Sciences of the Czech RepublicPragueCzech Republic

Personalised recommendations