Tissue transglutaminase inhibits the TRPV5-dependent calcium transport in an N-glycosylation-dependent manner

Cellular and Molecular Life Sciences

Volumn 69, Issue 6, 2012, Pages 981-992

  Boros, Sandor ^a   Xi, Qi ^a   Dimke, Henrik ^a   Van Fer Kemp, Annemiete W ^a   Tudpor, Kukiat ^a   Verkaart, Sjoerd ^a   Lee, Kyu Pil ^a   Bindels, René J ^a   Hoenderop, Joost G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Calcium channel; Transepithelial Ca 2+ transport; Transglutaminase; TRPV5

Indexed keywords

PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; VANILLOID RECEPTOR 5;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CALCIUM TRANSPORT; CELL POLARITY; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME BINDING; ENZYME RELEASE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN GLYCOSYLATION; RABBIT;

ANIMALS; CALCIUM; GLYCOSYLATION; HEK293 CELLS; HUMANS; ION TRANSPORT; RABBITS; TRANSGLUTAMINASES; TRPV CATION CHANNELS;

ORYCTOLAGUS CUNICULUS;

EID: 84857658849     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0818-z     Document Type: Article

References (44)

1. Aeschlimann D, Paulsson M (1991) Cross-linking of lamininnidogen complexes by tissue transglutaminase. A novel mechanism for basement membrane stabilization. J Biol Chem 266: 15308-15317 (Pubitemid 21907649)
2. Barry PH (1994) JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J Neurosci Methods 51: 107-116 (Pubitemid 24089278)
3. Beninati S, Senger DR, Cordella-Miele E, Mukherjee AB, Chackalaparampil I, Shanmugam V, Singh K, Mukherjee BB (1994) Osteopontin: its transglutaminase-catalyzed posttranslational modifications and cross-linking to fibronectin. J Biochem 115: 675-682 (Pubitemid 24119390)
4. 2+ transport in primary cultures of rabbit kidney CCD: stimulation by 1,25-dihydroxyvitamin D3 and PTH. Am J Physiol 261: F799-F807
5. Boros S, Kamps B, Wunderink L, de Bruijn W, de Jong WW, Boelens WC (2004) Transglutaminase catalyzes differential crosslinking of small heat shock proteins and amyloid-beta. FEBS Lett 576: 57-62 (Pubitemid 39330457)
6. Broome AM, Ryan D, Eckert RL (2003) S100 protein subcellular localization during epidermal differentiation and psoriasis. J Histochem Cytochem 51: 675-685 (Pubitemid 36520623)
7. Cha SK, Jabbar W, Xie J, Huang CL (2007) Regulation of TRPV5 single-channel activity by intracellular pH. J Membr Biol 220: 79-85 (Pubitemid 50003243)
8. Cha SK, Ortega B, Kurosu H, Rosenblatt KP, Kuro OM, Huang CL (2008) Removal of sialic acid involving Klotho causes cellsurface retention of TRPV5 channel via binding to galectin-1. Proc Natl Acad Sci USA 105: 9805-9810 (Pubitemid 352031381)
9. 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: 490-493 (Pubitemid 41507962)
10. Cheng X, Jin J, Hu L, Shen D, Dong XP, Samie MA, Knoff J, Eisinger B, Liu ML, Huang SM, Caterina MJ, Dempsey P, Michael LE, Dlugosz AA, Andrews NC, Clapham DE, Xu H (2010) TRP channel regulates EGFR signaling in hair morphogenesis and skin barrier formation. Cell 141: 331-343
11. D'Souza DR, Wei J, Shao Q, Hebert MD, Subramony SH, Vig PJ (2006) Tissue transglutaminase crosslinks ataxin-1: possible role in SCA1 pathogenesis. Neurosci Lett 409: 5-9 (Pubitemid 44585111)
12. El Nahas AM, Abo-Zenah H, Skill NJ, Bex S, Wild G, Griffin M, Johnson TS (2004) Elevated epsilon- (gamma-glutamyl) lysine in human diabetic nephropathy results from increased expression and cellular release of tissue transglutaminase. Nephron Clin Pract 97: c108-c117 (Pubitemid 39077827)
13. Fesus L, Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27: 534-539 (Pubitemid 35279599)
14. Gambetti S, Dondi A, Cervellati C, Squerzanti M, Pansini FS, Bergamini CM (2005) Interaction with heparin protects tissue transglutaminase against inactivation by heating and by proteolysis. Biochimie 87: 551-555 (Pubitemid 40776193)
15. Hoenderop JG, Bindels RJ (2008) Calciotropic and magnesiotropic TRP channels. Physiology (Bethesda) 23: 32-40
16. Hoenderop JG, Nilius B, Bindels RJ (2005) Calcium absorption across epithelia. Physiol Rev 85: 373-422 (Pubitemid 40171261)
17. 2+ channel in 1,25-dihydroxyvitamin D3-responsive epithelia. J Biol Chem 274: 8375-8378 (Pubitemid 29164624)
18. 2+ wasting, hyperabsorption, and reduced bone thickness in mice lacking TRPV5. J Clin Invest 112: 1906-1914 (Pubitemid 38063714)
19. 2+ channels TRPV5 and TRPV6. EMBO J 22: 776-785 (Pubitemid 36227780)
20. Huang L, Haylor JL, Hau Z, Jones RA, Vickers ME, Wagner B, Griffin M, Saint RE, Coutts IG, El Nahas AM, Johnson TS (2009) Transglutaminase inhibition ameliorates experimental diabetic nephropathy. Kidney Int 76: 383-394
21. Ikee R, Kobayashi S, Hemmi N, Saigusa T, Namikoshi T, Yamada M, Imakiire T, Kikuchi Y, Suzuki S, Miura S (2007) Involvement of transglutaminase-2 in pathological changes in renal disease. Nephron Clin Pract 105: c139-c146 (Pubitemid 46215208)
22. Kaartinen MT, El-Maadawy S, Rasanen NH, McKee MD (2002) Tissue transglutaminase and its substrates in bone. J Bone Miner Res 17: 2161-2173 (Pubitemid 35416751)
23. + channel by Galphah (transglutaminase II) in the vascular smooth muscle cell. Pflugers Arch 433: 671-673 (Pubitemid 27093131)
24. 2+-induced differentiation of human keratinocytes. J Biol Chem 282: 22582-22591 (Pubitemid 47267368)
25. Liu SY, Huang HC, Li XM (2005) Tissue transglutaminase and renal fibrosis. Sheng Li Ke Xue Jin Zhan 36: 314-318
26. Loffing J, Loffing-Cueni D, Valderrabano V, Klausli L, Hebert SC, Rossier BC, Hoenderop JG, Bindels RJ, Kaissling B (2001) Distribution of transcellular calcium and sodium transport pathways along mouse distal nephron. Am J Physiol Renal Physiol 281: F1021-F1027
27. Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4: 140-156 (Pubitemid 36172696)
28. 2+ channels TRPV5 and TRPV6. Nephrol Dial Transpl 23: 3397-3402
29. 2+. Cell Calcium 29: 417-428 (Pubitemid 32496363)
30. Okano T, Tsugawa N, Morishita A, Kato S (2004) Regulation of gene expression of epithelial calcium channels in intestine and kidney of mice by 1alpha, 25-dihydroxyvitamin D3. J Steroid Biochem Mol Biol 89-90: 335-338 (Pubitemid 38844306)
31. Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol 5: e327
32. Priglinger SG, May CA, Neubauer AS, Alge CS, Schonfeld CL, Kampik A, Welge-Lussen U (2003) Tissue transglutaminase as a modifying enzyme of the extracellular matrix in PVR membranes. Invest Ophthalmol Vis Sci 44: 355-364 (Pubitemid 36134296)
33. Raghunath M, Hopfner B, Aeschlimann D, Luthi U, Meuli M, Altermatt S, Gobet R, Bruckner-Tuderman L, Steinmann B (1996) Cross-linking of the dermo-epidermal junction of skin regenerating from keratinocyte autografts. Anchoring fibrils are a target for tissue transglutaminase. J Clin Invest 98: 1174-1184 (Pubitemid 26299931)
34. Ruse M, Lambert A, Robinson N, Ryan D, Shon KJ, Eckert RL (2001) S100A7, S100A10, and S100A11 are transglutaminase substrates. Biochemistry 40: 3167-3173 (Pubitemid 32205361)
35. Scarpellini A, Germack R, Lortat-Jacob H, Muramatsu T, Billett E, Johnson T, Verderio EA (2009) Heparan sulfate proteoglycans are receptors for the cell-surface trafficking and biological activity of transglutaminase-2. J Biol Chem 284: 18411-18423
36. Shweke N, Boulos N, Jouanneau C, Vandermeersch S, Melino G, Dussaule JC, Chatziantoniou C, Ronco P, Boffa JJ (2008) Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am J Pathol 173: 631-642
37. Skill NJ, Griffin M, El Nahas AM, Sanai T, Haylor JL, Fisher M, Jamie MF, Mould NN, Johnson TS (2001) Increases in renal epsilon- (gamma-glutamyl) -lysine crosslinks result from compartment- specific changes in tissue transglutaminase in early experimental diabetic nephropathy: pathologic implications. Lab Invest 81: 705-716 (Pubitemid 32466533)
38. Skill NJ, Johnson TS, Coutts IG, Saint RE, Fisher M, Huang L, El Nahas AM, Collighan RJ, Griffin M (2004) Inhibition of transglutaminase activity reduces extracellular matrix accumulation induced by high glucose levels in proximal tubular epithelial cells. J Biol Chem 279: 47754-47762 (Pubitemid 39540924)
39. 2+ absorption in health and disease. Annu Rev Physiol 70: 257-271 (Pubitemid 351738180)
40. 2+ transport. Rev Physiol Biochem Pharmacol 158: 77-160
41. 2+. J Steroid Biochem Mol Biol 89-90: 303-308 (Pubitemid 38844300)
42. 2+ channels (TRPV5 and TRPV6) requires association of the S100A10-annexin 2 complex. EMBO J 22: 1478-1487 (Pubitemid 36417397)
43. Verderio EA, Telci D, Okoye A, Melino G, Griffin M (2003) A novel RGD-independent cel adhesion pathway mediated by fibronectin-bound tissue transglutaminase rescues cells from anoikis. J Biol Chem 278: 42604-42614 (Pubitemid 37310534)
44. Vig PJ, Wei J, Shao Q, Hebert MD, Subramony SH, Sutton LT (2007) Role of tissue transglutaminase type 2 in calbindin-D28k interaction with ataxin-1. Neurosci Lett 420: 53-57 (Pubitemid 46777103)