Regulation of TRP Signalling by Ion Channel Translocation Between Cell Compartments

Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 704)

Abstract

The TRP (transient receptor potential) family of ion channels is a heterogeneous family of calcium permeable cation channels that is subdivided into seven subfamilies: TRPC (“Canonical”), TRPV (“Vanilloid”), TRPM (“Melastatin”), TRPA (“Ankyrin”), TRPN (“NOMPC”), TRPP (“Polycystin”), and TRPML (“Mucolipin”). TRP-mediated ion currents across the cell membrane are determined by the single channel conductance, by the fraction of activated channels, and by the total amount of TRP channels present at the plasma membrane. In many cases, the amount of TRP channels at the plasma membrane is altered in response to physiological stimuli by translocation of channels to and from the plasma membrane. Regulated translocation has been described for channels of the TRPC, TRPV, TRPM, and TRPA family and is achieved by vesicular transport of these channels along cellular exocytosis and endocytosis pathways. This review summarizes the stimuli and signalling cascades involved in the translocation of TRP channels and highlights interactions of TRP channels with proteins of the endocytosis and exocytosis machineries.

Keywords

Calcium signalling Endocytosis Exocytosis Membrane trafficking TRP ion channels 

Abbreviations

4α-PDD

4α-phorbol 12,13-didecanoate

AIP4

atropine-1 interacting protein 4

AMPA-receptor

α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor

ATP

adenosine-triphosphate

BAPTA

1,2-bis(o-aminophenoxy) ethane-N,N,N’,N’-tetraacetic acid

bFGF

basic fibroblast growth factor

cAMP

cyclic adenosine-monophosphate

CHO

chinese hamster ovary

DAG

diacylglycerol

DHPG

3,5-dihydroxyphenylglycine

EETs

epoxyeicosatrienoic acids

EGF

epithelial growth factor

(e)GFP

(enhanced) green fluorescent protein

ePKC

eye specific protein kinase C

ER

endoplasmatic reticulum

ERK

extracellular-signal-regulated kinase

fMLP

formyl Met-Leu-Phe

GTP

guanosine-triphosphate

HA-tag

haemagglutinin tag

HEK

human embryonic kidney

HPAEC

human pulmonary artery endothelial cells

Hrs

hepatocyte growth factor regulated tyrosine kinase substrate

IGF-1

insulin-like growth factor 1

IMCD

inner medullary collecting duct

INAD

inactivation no afterpotential D

IP3

inositol triphosphate

IP3R

inositol triphosphate receptor

lysoPC

lysophosphatidylcholine

NCC

thiazide-sensitive Na-Cl cotransporter

NGF

nerve growth factor

NHERF

Na/H exchanger regulatory factor

OAG

1-oleyl-2-acetyl-sn-glycerol

OS-9

osteosarcoma amplified 9

PACS

phosphofurin acidic cluster sorting protein

PACSIN

protein kinase C and casein kinase substrate in neurons

PDGF

platelet derived growth factor

PI(3) kinase

phosphatidylinositide 3 kinase

PIP

phosphatidylinositol 4-phosphate

PIP2

phosphatidylinositol 4,5-bisphosphate

PIP3

phosphatidylinositol 3,4,5-trisphosphate

PKA

protein kinase A

PKC

protein kinase C

PKD

polycystic kidney disease

PLC

phospholipase C

PTH

parathyroid hormone

RGA

recombination gene activator

RNF24

ring finger protein 24

SGK

serum and glucocorticoid inducible kinase

SNAP

soluble NSF attachment protein

snapin

synaptic vesicle-associated protein

SNARE

soluble NSF attachment protein receptors

STAM

signal transducing adaptor molecule

TRP

transient receptor potential

TRPL

transient receptor potential like

VAMP2

vesicle-associated membrane protein 2

WNK

with no K (lysine)

YFP

yellow fluorescent protein

References

  1. 1.
    Greger IH, Esteban JA (2007) AMPA receptor biogenesis and trafficking. Curr Opin Neurobiol 17:289–297PubMedGoogle Scholar
  2. 2.
    Man HY, Ju W, Ahmadian G, Wang YT (2000) Intracellular trafficking of AMPA receptors in synaptic plasticity. Cell Mol Life Sci 57:1526–1534PubMedGoogle Scholar
  3. 3.
    Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83–88PubMedGoogle Scholar
  4. 4.
    Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972–1975PubMedGoogle Scholar
  5. 5.
    Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224:285–287PubMedGoogle Scholar
  6. 6.
    Montell C, Rubin GM (1989) Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2:1313–1323PubMedGoogle Scholar
  7. 7.
    Hardie RC, Minke B: (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8:643–651PubMedGoogle Scholar
  8. 8.
    Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005:re3PubMedGoogle Scholar
  9. 9.
    Montell C (2005) Drosophila TRP channels. Pflugers Arch 451:19–28PubMedGoogle Scholar
  10. 10.
    Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233–252PubMedGoogle Scholar
  11. 11.
    Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417PubMedCentralPubMedGoogle Scholar
  12. 12.
    Xiao R, Xu XZ: (2009) Function and regulation of TRP family channels in C. elegans. Pflugers Arch 458:851–860PubMedCentralPubMedGoogle Scholar
  13. 13.
    Clapham DE, Julius D, Montell C, Schultz G: (2005) International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol Rev 57:427–450PubMedGoogle Scholar
  14. 14.
    Kanzaki M, Zhang YQ, Mashima H, Li L, Shibata H, Kojima I: (1999) Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1:165–170PubMedGoogle Scholar
  15. 15.
    Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, Clapham DE: (2004) Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol 6:709–720PubMedGoogle Scholar
  16. 16.
    Thebault S, Alexander RT, Tiel Groenestege WM, Hoenderop JG, Bindels RJ (2009) EGF increases TRPM6 activity and surface expression. J Am Soc Nephrol 20:78–85PubMedCentralPubMedGoogle Scholar
  17. 17.
    Schmidt M, Dubin AE, Petrus MJ, Earley TJ, Patapoutian A: (2009) Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron 64:498–509PubMedCentralPubMedGoogle Scholar
  18. 18.
    Cayouette S, Boulay G: (2007) Intracellular trafficking of TRP channels. Cell Calcium 42:225–232PubMedGoogle Scholar
  19. 19.
    Ambudkar IS (2007) Trafficking of TRP channels: determinants of channel function. Handb Exp Pharmacol 179:541–557PubMedGoogle Scholar
  20. 20.
    Birnbaumer L (2009) The TRPC class of ion channels: a critical review of their roles in slow, sustained increases in intracellular Ca(2+) concentrations. Annu Rev Pharmacol Toxicol 49:395–426PubMedGoogle Scholar
  21. 21.
    Kiselyov K, Patterson RL: (2009) The integrative function of TRPC channels. Front Biosci 14:45–58Google Scholar
  22. 22.
    Mehta D, Ahmmed GU, Paria BC, Holinstat M, Voyno-Yasenetskaya T, Tiruppathi C, Minshall RD, Malik AB (2003) RhoA interaction with inositol 1,4,5-trisphosphate receptor and transient receptor potential channel-1 regulates Ca2+ entry. Role in signaling increased endothelial permeability. J Biol Chem 278:33492–33500PubMedGoogle Scholar
  23. 23.
    Smyth JT, Lemonnier L, Vazquez G, Bird GS, Putney JW Jr. (2006) Dissociation of regulated trafficking of TRPC3 channels to the plasma membrane from their activation by phospholipase C. J Biol Chem 281:11712–11720PubMedGoogle Scholar
  24. 24.
    Fauconnier J, Lanner JT, Sultan A, Zhang SJ, Katz A, Bruton JD, Westerblad H: (2007) Insulin potentiates TRPC3-mediated cation currents in normal but not in insulin-resistant mouse cardiomyocytes. Cardiovasc Res 73:376–385PubMedGoogle Scholar
  25. 25.
    Goel M, Sinkins WG, Zuo CD, Hopfer U, Schilling WP: (2007) Vasopressin-induced membrane trafficking of TRPC3 and AQP2 channels in cells of the rat renal collecting duct. Am J Physiol Renal Physiol 293:F1476–F1488PubMedGoogle Scholar
  26. 26.
    Singh BB, Lockwich TP, Bandyopadhyay BC, Liu X, Bollimuntha S, Brazer SC, Combs C, Das S, Leenders AG, Sheng ZH, Knepper MA, Ambudkar SV, Ambudkar IS: (2004) VAMP2-dependent exocytosis regulates plasma membrane insertion of TRPC3 channels and contributes to agonist-stimulated Ca2+ influx. Mol Cell 15:635–646PubMedGoogle Scholar
  27. 27.
    Kim JY, Zeng W, Kiselyov K, Yuan JP, Dehoff MH, Mikoshiba K, Worley PF, Muallem S: (2006) Homer 1 mediates store- and inositol 1,4,5-trisphosphate receptor-dependent translocation and retrieval of TRPC3 to the plasma membrane. J Biol Chem 281:32540–32549PubMedGoogle Scholar
  28. 28.
    Odell AF, Scott JL, Van Helden DF: (2005) Epidermal growth factor induces tyrosine phosphorylation, membrane insertion, and activation of transient receptor potential channel 4. J Biol Chem 280:37974–37987PubMedGoogle Scholar
  29. 29.
    Wang M, Bianchi R, Chuang SC, Zhao W, Wong RK (2007) GroupI metabotropic glutamate receptor-dependent TRPC channel trafficking in hippocampal neurons. J Neurochem 101:411–421PubMedGoogle Scholar
  30. 30.
    Chaudhuri P, Colles SM, Bhat M, Van Wagoner DR, Birnbaumer L, Graham LM: (2008) Elucidation of a TRPC6-TRPC5 channel cascade that restricts endothelial cell movement. Mol Biol Cell 19:3203–3211PubMedCentralPubMedGoogle Scholar
  31. 31.
    Cayouette S, Lussier MP, Mathieu EL, Bousquet SM, Boulay G: (2004) Exocytotic insertion of TRPC6 channel into the plasma membrane upon Gq protein-coupled receptor activation. J Biol Chem 279:7241–7246PubMedGoogle Scholar
  32. 32.
    Fleming I, Rueben A, Popp R, Fisslthaler B, Schrodt S, Sander A, Haendeler J, Falck JR, Morisseau C, Hammock BD, Busse R: (2007) Epoxyeicosatrienoic acids regulate Trp channel dependent Ca2+ signaling and hyperpolarization in endothelial cells. Arterioscler Thromb Vasc Biol 27:2612–2618PubMedGoogle Scholar
  33. 33.
    Hannan MA, Kabbani N, Paspalas CD, Levenson R: (2008) Interaction with dopamine D2 receptor enhances expression of transient receptor potential channel 1 at the cell surface. Biochim Biophys Acta 1778:974–982PubMedCentralPubMedGoogle Scholar
  34. 34.
    Holz RW, Hlubek MD, Sorensen SD, Fisher SK, Balla T, Ozaki S, Prestwich GD, Stuenkel EL, Bittner MA: (2000) A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (PtdIns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane PtdIns-4,5-P2 as being important in exocytosis. J Biol Chem 275:17878–17885PubMedGoogle Scholar
  35. 35.
    Greka A, Navarro B, Oancea E, Duggan A, Clapham DE: (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 6:837–845PubMedGoogle Scholar
  36. 36.
    Mery L, Strauss B, Dufour JF, Krause KH, Hoth M (2002) The PDZ-interacting domain of TRPC4 controls its localization and surface expression in HEK293 cells. J Cell Sci 115:3497–3508PubMedGoogle Scholar
  37. 37.
    Odell AF, Van Helden DF, Scott JL: (2008) The spectrin cytoskeleton influences the surface expression and activation of human transient receptor potential channel 4 channels. J Biol Chem 283:4395–4407PubMedGoogle Scholar
  38. 38.
    Van Buren JJ, Bhat S, Rotello R, Pauza ME, Premkumar LS: (2005) Sensitization and translocation of TRPV1 by insulin and IGF-I. Mol Pain 1:17PubMedCentralPubMedGoogle Scholar
  39. 39.
    Suzuki F, Morishima S, Tanaka T, Muramatsu I: (2007) Snapin, a new regulator of receptor signaling, augments alpha1A-adrenoceptor-operated calcium influx through TRPC6. J Biol Chem 282:29563–29573PubMedGoogle Scholar
  40. 40.
    van Rossum DB, Oberdick D, Rbaibi Y, Bhardwaj G, Barrow RK, Nikolaidis N, Snyder SH, Kiselyov K, Patterson RL: (2008) TRP_2, a lipid/trafficking domain that mediates diacylglycerol-induced vesicle fusion. J Biol Chem 283:34384–34392PubMedCentralPubMedGoogle Scholar
  41. 41.
    Lussier MP, Lepage PK, Bousquet SM, Boulay G: (2008) RNF24, a new TRPC interacting protein, causes the intracellular retention of TRPC. Cell Calcium 43:432–443PubMedGoogle Scholar
  42. 42.
    Wegierski T, Hill K, Schaefer M, Walz G: (2006) The HECT ubiquitin ligase AIP4 regulates the cell surface expression of select TRP channels. EMBO J 25:5659–5669PubMedCentralPubMedGoogle Scholar
  43. 43.
    Cayouette S, Bousquet SM, Francoeur N, Dupre E, Monet M, Gagnon H, Guedri YB, Lavoie C, Boulay G (2010) Involvement of Rab9 and Rab11 in the intracellular trafficking of TRPC6. Biochim Biophys Acta 1803:805–812PubMedGoogle Scholar
  44. 44.
    Xu XZ, Sternberg PW (2003) A C.elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114:285–297PubMedGoogle Scholar
  45. 45.
    Bähner M, Frechter S, Da Silva N, Minke B, Paulsen R, Huber A (2002) Light-regulated subcellular translocation of Drosophila TRPL channels induces long-term adaptation and modifies the light-induced current. Neuron 34:83–93PubMedGoogle Scholar
  46. 46.
    Cronin MA, Lieu MH, Tsunoda S: (2006) Two stages of light-dependent TRPL-channel translocation in Drosophila photoreceptors. J Cell Sci 119:2935–2944PubMedGoogle Scholar
  47. 47.
    Meyer NE, Joel-Almagor T, Frechter S, Minke B, Huber A: (2006) Subcellular translocation of the eGFP-tagged TRPL channel in Drosophila photoreceptors requires activation of the phototransduction cascade. J Cell Sci 119:2592–2603PubMedCentralPubMedGoogle Scholar
  48. 48.
    Montell C (2005) TRP channels in Drosophila photoreceptor cells. J Physiol 567:45–51PubMedCentralPubMedGoogle Scholar
  49. 49.
    Katz B, Minke B (2009) Drosophila photoreceptors and signaling mechanisms. Front Cell Neurosci 3:2 [Epub 2009 Jun 11:2]PubMedCentralPubMedGoogle Scholar
  50. 50.
    Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS: (1996) The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85:651–659PubMedGoogle Scholar
  51. 51.
    Chevesich J, Kreuz AJ, Montell C: (1997) Requirement for the PDZ domain protein, INAD, for localization of the TRP store-operated channel to a signaling complex. Neuron 18: 95–105PubMedGoogle Scholar
  52. 52.
    Shieh BH, Zhu MY: (1996) Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron 16:991–998PubMedGoogle Scholar
  53. 53.
    Huber A, Sander P, Gobert A, Bahner M, Hermann R, Paulsen R: (1996) The transient receptor potential protein (Trp), a putative store-operated Ca2+ channel essential for phosphoinositide-mediated photoreception, forms a signaling complex with NorpA, InaC and InaD. EMBO J 15:7036–7045PubMedCentralPubMedGoogle Scholar
  54. 54.
    Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, Becker A, Socolich M, Zuker CS: (1997) A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 388:243–249PubMedGoogle Scholar
  55. 55.
    Sanxaridis PD, Cronin MA, Rawat SS, Waro G, Acharya U, Tsunoda S: (2007) Light-induced recruitment of INAD-signaling complexes to detergent-resistant lipid rafts in Drosophila photoreceptors. Mol Cell Neurosci 36:36–46PubMedCentralPubMedGoogle Scholar
  56. 56.
    Hardie RC, Peretz A, Suss-Toby E, Rom-Glas A, Bishop SA, Selinger Z, Minke B: (1993) Protein kinase C is required for light adaptation in Drosophila photoreceptors. Nature 363:634–637PubMedGoogle Scholar
  57. 57.
    Smith DP, Ranganathan R, Hardy RW, Marx J, Tsuchida T, Zuker CS: (1991) Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science 254:1478–1484PubMedGoogle Scholar
  58. 58.
    Kauer JA, Gibson HE: (2009) Hot flash: TRPV channels in the brain. Trends Neurosci 32:215–224PubMedGoogle Scholar
  59. 59.
    Liu DL, Wang WT, Xing JL, Hu SJ: (2009) Research progress in transient receptor potential vanilloid 1 of sensory nervous system. Neurosci Bull 25:221–227PubMedGoogle Scholar
  60. 60.
    Liedtke W: (2008) Molecular mechanisms of TRPV4-mediated neural signaling. Ann N Y Acad Sci 1144:42–52PubMedGoogle Scholar
  61. 61.
    Plant TD, Strotmann R (2007) TRPV4. Handb Exp Pharmacol 179:189–205PubMedGoogle Scholar
  62. 62.
    Shibasaki K, Suzuki M, Mizuno A, Tominaga M: (2007) Effects of body temperature on neural activity in the hippocampus: regulation of resting membrane potentials by transient receptor potential vanilloid 4. J Neurosci 27:1566–1575PubMedGoogle Scholar
  63. 63.
    de Groot T, Bindels RJ, Hoenderop JG: (2008) TRPV5: an ingeniously controlled calcium channel. Kidney Int 74:1241–1246PubMedGoogle Scholar
  64. 64.
    Hoenderop JG, Bindels RJ: (2008) Calciotropic and magnesiotropic TRP channels. Physiology (Bethesda) 23:32–40Google Scholar
  65. 65.
    Premkumar LS, Ahern GP: (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985–990PubMedGoogle Scholar
  66. 66.
    Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW: (2003) Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci U S A 100:12480–12485PubMedCentralPubMedGoogle Scholar
  67. 67.
    Morenilla-Palao C, Planells-Cases R, Garcia-Sanz N, Ferrer-Montiel A: (2004) Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J Biol Chem 279:25665–25672PubMedGoogle Scholar
  68. 68.
    Zhang X, Huang J, McNaughton PA (2005) NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24:4211–4223PubMedCentralPubMedGoogle Scholar
  69. 69.
    Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE: (2006) Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 128:509–522PubMedCentralPubMedGoogle Scholar
  70. 70.
    Jeske NA, Patwardhan AM, Henry MA, Milam SB: (2009) Fibronectin stimulates TRPV1 translocation in primary sensory neurons. J Neurochem 108:591–600PubMedCentralPubMedGoogle Scholar
  71. 71.
    Vetter I, Cheng W, Peiris M, Wyse BD, Roberts-Thomson SJ, Zheng J, Monteith GR, Cabot PJ: (2008) Rapid, opioid-sensitive mechanisms involved in transient receptor potential vanilloid 1 sensitization. J Biol Chem 283:19540–19550PubMedCentralPubMedGoogle Scholar
  72. 72.
    Penna A, Juvin V, Chemin J, Compan V, Monet M, Rassendren FA: (2006) PI3-kinase promotes TRPV2 activity independently of channel translocation to the plasma membrane. Cell Calcium 39:495–507PubMedGoogle Scholar
  73. 73.
    Hisanaga E, Nagasawa M, Ueki K, Kulkarni RN, Mori M, Kojima I: (2009) Regulation of calcium-permeable TRPV2 channel by insulin in pancreatic beta-cells. Diabetes 58: 174–184PubMedCentralPubMedGoogle Scholar
  74. 74.
    Boels K, Glassmeier G, Herrmann D, Riedel IB, Hampe W, Kojima I, Schwarz JR, Schaller HC: (2001) The neuropeptide head activator induces activation and translocation of the growth-factor-regulated Ca(2+)-permeable channel GRC. J Cell Sci 114:3599–3606PubMedGoogle Scholar
  75. 75.
    Nagasawa M, Nakagawa Y, Tanaka S, Kojima I: (2007) Chemotactic peptide fMetLeuPhe induces translocation of the TRPV2 channel in macrophages. J Cell Physiol 210:692–702PubMedGoogle Scholar
  76. 76.
    Monet M, Gkika D, Lehen’kyi V, Pourtier A, Vanden AF, Bidaux G, Juvin V, Rassendren F, Humez S, Prevarsakaya N: (2009) Lysophospholipids stimulate prostate cancer cell migration via TRPV2 channel activation. Biochim Biophys Acta 1793:528–539PubMedGoogle Scholar
  77. 77.
    Stokes AJ, Wakano C, Del Carmen KA, Koblan-Huberson M, Turner H: (2005) Formation of a physiological complex between TRPV2 and RGA protein promotes cell surface expression of TRPV2. J Cell Biochem 94:669–683PubMedGoogle Scholar
  78. 78.
    Iwata Y, Katanosaka Y, Arai Y, Komamura K, Miyatake K, Shigekawa M: (2003) A novel mechanism of myocyte degeneration involving the Ca2+-permeable growth factor-regulated channel. J Cell Biol 161:957–967PubMedCentralPubMedGoogle Scholar
  79. 79.
    Barnhill JC, Stokes AJ, Koblan-Huberson M, Shimoda LM, Muraguchi A, Adra CN, Turner H (2004) RGA protein associates with a TRPV ion channel during biosynthesis and trafficking. J Cell Biochem 91:808–820PubMedGoogle Scholar
  80. 80.
    Saito M, Hanson PI, Schlesinger P: (2007) Luminal chloride-dependent activation of endosome calcium channels: patch clamp study of enlarged endosomes. J Biol Chem 282:27327–27333PubMedGoogle Scholar
  81. 81.
    Suzuki M, Hirao A, Mizuno A: (2003) Microtubule-associated [corrected] protein 7 increases the membrane expression of transient receptor potential vanilloid 4 (TRPV4). J Biol Chem 278:51448–51453PubMedGoogle Scholar
  82. 82.
    Fu Y, Subramanya A, Rozansky D, Cohen DM (2006) WNK kinases influence TRPV4 channel function and localization. Am J Physiol Renal Physiol 290:F1305–F1314PubMedGoogle Scholar
  83. 83.
    Loot AE, Popp R, Fisslthaler B, Vriens J, Nilius B, Fleming I: (2008) Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation. Cardiovasc Res 80:445–452PubMedGoogle Scholar
  84. 84.
    Cuajungco MP, Grimm C, Oshima K, D’hoedt D, Nilius B, Mensenkamp AR, Bindels RJ, Plomann M, Heller S: (2006) PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4. J Biol Chem 281:18753–18762PubMedGoogle Scholar
  85. 85.
    Modregger J, Ritter B, Witter B, Paulsson M, Plomann M (2000) All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci 113(Pt 24):4511–4521PubMedGoogle Scholar
  86. 86.
    D’hoedt D, Owsianik G, Prenen J, Cuajungco MP, Grimm C, Heller S, Voets T, Nilius B: (2008) Stimulus-specific modulation of the cation channel TRPV4 by PACSIN 3. J Biol Chem 283:6272–6280PubMedGoogle Scholar
  87. 87.
    Wang Y, Fu X, Gaiser S, Kottgen M, Kramer-Zucker A, Walz G, Wegierski T (2007) OS-9 regulates the transit and polyubiquitination of TRPV4 in the endoplasmic reticulum. J Biol Chem 282:36561–36570PubMedGoogle Scholar
  88. 88.
    Kottgen M, Benzing T, Simmen T, Tauber R, Buchholz B, Feliciangeli S, Huber TB, Schermer B, Kramer-Zucker A, Hopker K, Simmen KC, Tschucke CC, Sandford R, Kim E, Thomas G, Walz G: (2005) Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. EMBO J 24:705–716PubMedCentralPubMedGoogle Scholar
  89. 89.
    Cha SK, Wu T, Huang CL: (2008) Protein kinase C inhibits caveolae-mediated endocytosis of TRPV5. Am J Physiol Renal Physiol 294:F1212–F1221PubMedGoogle Scholar
  90. 90.
    Cha SK, Huang CL: (2010) WNK4 kinase stimulates caveola-mediated endocytosis of TRPV5 amplifying the dynamic range of regulation of the channel by protein kinase C. J Biol Chem 285:6604–6611PubMedCentralPubMedGoogle Scholar
  91. 91.
    Gkika D, Topala CN, Chang Q, Picard N, Thebault S, Houillier P, Hoenderop JG, Bindels RJ: (2006) Tissue kallikrein stimulates Ca(2+) reabsorption via PKC-dependent plasma membrane accumulation of TRPV5. EMBO J 25:4707–4716PubMedCentralPubMedGoogle Scholar
  92. 92.
    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
  93. 93.
    Cha SK, Ortega B, Kurosu H, Rosenblatt KP, Kuro O, 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
  94. 94.
    van de Graaf SF, Rescher U, Hoenderop JG, Verkaart S, Bindels RJ, Gerke V: (2008) TRPV5 is internalized via clathrin-dependent endocytosis to enter a Ca2+-controlled recycling pathway. J Biol Chem 283:4077–4086PubMedGoogle Scholar
  95. 95.
    van de Graaf SF, Chang Q, Mensenkamp AR, Hoenderop JG, Bindels RJ: (2006) Direct interaction with Rab11a targets the epithelial Ca2+ channels TRPV5 and TRPV6 to the plasma membrane. Mol Cell Biol 26:303–312PubMedCentralPubMedGoogle Scholar
  96. 96.
    Jiang Y, Ferguson WB, Peng JB: (2007) WNK4 enhances TRPV5-mediated calcium transport: potential role in hypercalciuria of familial hyperkalemic hypertension caused by gene mutation of WNK4. Am J Physiol Renal Physiol 292:F545–F554PubMedGoogle Scholar
  97. 97.
    Zhang W, Na T, Peng JB (2008) WNK3 positively regulates epithelial calcium channels TRPV5 and TRPV6 via a kinase-dependent pathway. Am J Physiol Renal Physiol 295:F1472–F1484PubMedCentralPubMedGoogle Scholar
  98. 98.
    Embark HM, Setiawan I, Poppendieck S, van de Graaf SF, Boehmer C, Palmada M, Wieder T, Gerstberger R, Cohen P, Yun CC, Bindels RJ, Lang F: (2004) Regulation of the epithelial Ca2+ channel TRPV5 by the NHE regulating factor NHERF2 and the serum and glucocorticoid inducible kinase isoforms SGK1 and SGK3 expressed in Xenopus oocytes. Cell Physiol Biochem 14:203–212PubMedGoogle Scholar
  99. 99.
    Lambers TT, Oancea E, de Groot T, Topala CN, Hoenderop JG, Bindels RJ: (2007) Extracellular pH dynamically controls cell surface delivery of functional TRPV5 channels. Mol Cell Biol 27:1486–1494PubMedCentralPubMedGoogle Scholar
  100. 100.
    Yeh BI, Sun TJ, Lee JZ, Chen HH, Huang CL: (2003) Mechanism and molecular determinant for regulation of rabbit transient receptor potential type 5 (TRPV5) channel by extracellular pH. J Biol Chem 278:51044–51052PubMedGoogle Scholar
  101. 101.
    Yeh BI, Kim YK, Jabbar W, Huang CL: (2005) Conformational changes of pore helix coupled to gating of TRPV5 by protons. EMBO J 24:3224–3234PubMedCentralPubMedGoogle Scholar
  102. 102.
    Bohmer C, Palmada M, Kenngott C, Lindner R, Klaus F, Laufer J, Lang F: (2007) Regulation of the epithelial calcium channel TRPV6 by the serum and glucocorticoid-inducible kinase isoforms SGK1 and SGK3. FEBS Lett 581:5586–5590PubMedGoogle Scholar
  103. 103.
    Khanal RC, Peters TM, Smith NM, Nemere I: (2008) Membrane receptor-initiated signaling in 1,25(OH)2D3-stimulated calcium uptake in intestinal epithelial cells. J Cell Biochem 105:1109–1116PubMedGoogle Scholar
  104. 104.
    Oancea E, Wolfe JT, Clapham DE: (2006) Functional TRPM7 channels accumulate at the plasma membrane in response to fluid flow. Circ Res 98:245–253PubMedGoogle Scholar
  105. 105.
    van der WJ, Hoenderop JG, Bindels RJ (2009) Epithelial Mg2+ channel TRPM6: insight into the molecular regulation. Magnes Res 22:127–132Google Scholar
  106. 106.
    Krapivinsky G, Mochida S, Krapivinsky L, Cibulsky SM, Clapham DE: (2006) The TRPM7 ion channel functions in cholinergic synaptic vesicles and affects transmitter release. Neuron 52:485–496PubMedGoogle Scholar
  107. 107.
    Brauchi S, Krapivinsky G, Krapivinsky L, Clapham DE: (2008) TRPM7 facilitates cholinergic vesicle fusion with the plasma membrane. Proc Natl Acad Sci U S A 105:8304–8308PubMedCentralPubMedGoogle Scholar
  108. 108.
    Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, Sanchez EE, Perez JC, Weissman JS, Julius D: (2010) Molecular basis of infrared detection by snakes. Nature 464:1006–1011PubMedCentralPubMedGoogle Scholar
  109. 109.
    Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A: (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829PubMedGoogle Scholar
  110. 110.
    Prasad P, Yanagihara AA, Small-Howard AL, Turner H, Stokes AJ (2008) Secretogranin III directs secretory vesicle biogenesis in mast cells in a manner dependent upon interaction with chromogranin A. J Immunol 181:5024–5034PubMedGoogle Scholar
  111. 111.
    Giamarchi A, Padilla F, Coste B, Raoux M, Crest M, Honore E, Delmas P: (2006) The versatile nature of the calcium-permeable cation channel TRPP2. EMBO Rep 7:787–793PubMedCentralPubMedGoogle Scholar
  112. 112.
    Kottgen M, Walz G: (2005) Subcellular localization and trafficking of polycystins. Pflugers Arch 451:286–293PubMedGoogle Scholar
  113. 113.
    Chen XZ, Li Q, Wu Y, Liang G, Lara CJ, Cantiello HF: (2008) Submembraneous microtubule cytoskeleton: interaction of TRPP2 with the cell cytoskeleton. FEBS J 275:4675–4683PubMedGoogle Scholar
  114. 114.
    Tsiokas L, Kim S, Ong EC: (2007) Cell biology of polycystin-2. Cell Signal 19:444–453PubMedCentralPubMedGoogle Scholar
  115. 115.
    Tsiokas L: (2009) Function and regulation of TRPP2 at the plasma membrane. Am J Physiol Renal Physiol 297:F1–F9PubMedCentralPubMedGoogle Scholar
  116. 116.
    Hanaoka K, Qian F, Boletta A, Bhunia AK, Piontek K, Tsiokas L, Sukhatme VP, Guggino WB, Germino GG: (2000) Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408:990–994PubMedGoogle Scholar
  117. 117.
    Delmas P, Nauli SM, Li X, Coste B, Osorio N, Crest M, Brown DA, Zhou J: (2004) Gating of the polycystin ion channel signaling complex in neurons and kidney cells. FASEB J 18: 740–742PubMedGoogle Scholar
  118. 118.
    Geng L, Okuhara D, Yu Z, Tian X, Cai Y, Shibazaki S, Somlo S: (2006) Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J Cell Sci 119:1383–1395PubMedGoogle Scholar
  119. 119.
    Streets AJ, Moon DJ, Kane ME, Obara T, Ong AC: (2006) Identification of an N-terminal glycogen synthase kinase 3 phosphorylation site which regulates the functional localization of polycystin-2 in vivo and in vitro. Hum Mol Genet 15:1465–1473PubMedCentralPubMedGoogle Scholar
  120. 120.
    Hu J, Bae YK, Knobel KM, Barr MM: (2006) Casein kinase II and calcineurin modulate TRPP function and ciliary localization. Mol Biol Cell 17:2200–2211PubMedCentralPubMedGoogle Scholar
  121. 121.
    Hu J, Wittekind SG, Barr MM (2007) STAM andHrs down-regulate ciliary TRP receptors. Mol Biol Cell 18:3277–3289PubMedCentralPubMedGoogle Scholar
  122. 122.
    Dong XP, Wang X, Xu H (2010) TRP channels of intracellular membranes. J Neurochem 113:313–328PubMedCentralPubMedGoogle Scholar
  123. 123.
    Puertollano R, Kiselyov K: (2009) TRPMLs: in sickness and in health. Am J Physiol Renal Physiol 296:F1245–F1254PubMedCentralPubMedGoogle Scholar
  124. 124.
    Zeevi DA, Frumkin A, Bach G: (2007) TRPML and lysosomal function. Biochim Biophys Acta 1772:851–858PubMedGoogle Scholar
  125. 125.
    Vergarajauregui S, Puertollano R: (2006) Two di-leucine motifs regulate trafficking of mucolipin-1 to lysosomes. Traffic 7:337–353PubMedCentralPubMedGoogle Scholar
  126. 126.
    Kim HJ, Soyombo AA, Tjon-Kon-Sang S, So I, Muallem S: (2009) The Ca(2+) channel TRPML3 regulates membrane trafficking and autophagy. Traffic 10:1157–1167PubMedCentralPubMedGoogle Scholar
  127. 127.
    Meyer NE, Oberegelsbacher C, Dürr TD, Schäfer A, Huber A: (2008) An eGFP-based genetic screen for defects in light-triggered subcelluar translocation of the Drosophila photoreceptor channel TRPL. Fly 2:384–394Google Scholar
  128. 128.
    Bae YK, Lyman-Gingerich J, Barr MM, Knobel KM: (2008) Identification of genes involved in the ciliary trafficking of C. elegans PKD-2. Dev Dyn 237:2021–2029PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of BiosensoricsInstitute of Physiology, University of HohenheimStuttgartGermany

Personalised recommendations