TRPC6 channel as an emerging determinant of the podocyte injury susceptibility in kidney diseases

American Journal of Physiology - Renal Physiology

Volumn 309, Issue 5, 2015, Pages F393-F397

  Ilatovskaya, Daria V ^a   Staruschenko, Alexander ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Diabetic nephropathy; Glomerulosclerosis; Glomerulus; Intracellular calcium; Podocyte; Proteinuria; TRPC6

Indexed keywords

CALCIUM ION; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC6 PROTEIN, HUMAN;

CALCIUM TRANSPORT; CELL DAMAGE; CELL DIFFERENTIATION; CELL FUNCTION; CHRONIC KIDNEY DISEASE; DISEASE COURSE; DISEASE PREDISPOSITION; FOCAL GLOMERULOSCLEROSIS; GLOMERULAR STRUCTURE; GLOMERULONEPHRITIS; GLOMERULUS EPITHELIUM CELL; HUMAN; KIDNEY DISEASE; KIDNEY INJURY; NEPHROTIC SYNDROME; NONHUMAN; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; DIABETIC NEPHROPATHY; GENETICS; METABOLISM; MUTATION; PATHOLOGY; SIGNAL TRANSDUCTION;

DIABETIC NEPHROPATHIES; DISEASE SUSCEPTIBILITY; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; KIDNEY DISEASES; MUTATION; PODOCYTES; SIGNAL TRANSDUCTION; TRPC CATION CHANNELS;

EID: 84940840071     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00186.2015     Document Type: Review

References (67)

1. Abkhezr M, Dryer SE. Angiotensin II and canonical transient receptor potential-6 activation stimulate release of a signal transducer and activator of transcription 3-activating factor from mouse podocytes. Mol Pharmacol 86: 150-158, 2014.
2. Abkhezr M, Dryer SE. STAT3 regulates steady-state expression of synaptopodin in cultured mouse podocytes. Mol Pharmacol 87: 231-239, 2015.
3. Abramowitz J, Birnbaumer L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 23: 297-328, 2009.
4. Anderson M, Kim EY, Hagmann H, Benzing T, Dryer SE. Opposing effects of podocin on the gating of podocyte TRPC6 channels evoked by membrane stretch or diacylglycerol. Am J Physiol Cell Physiol 305: C276-C289, 2013.
5. Anderson M, Roshanravan H, Khine J, Dryer SE. Angiotensin II activation of TRPC6 channels in rat podocytes requires generation of reactive oxygen species. J Cell Physiol 229: 434-442, 2014.
6. Anil Kumar P, Welsh GI, Saleem MA, Menon RK. Molecular and cellular events mediating glomerular podocyte dysfunction and depletion in diabetes mellitus. Front Endocrinol (Lausanne) 5: 151, 2014.
7. Chen S, Meng XF, Zhang C. Role of NADPH oxidase-mediated reactive oxygen species in podocyte injury. Biomed Res Int 2013: 839761, 2013.
8. Chi X, Hu B, Yu SY, Yin L, Meng Y, Wang B, Yang J, Lin J, Huang D, Chen L. Losartan treating podocyte injury induced by Ang II via downregulation of TRPC6 in podocytes. J Renin Angiotensin Aldosterone Syst [Epub ahead of print].
9. Crowley SD, Vasievich MP, Ruiz P, Gould SK, Parsons KK, Pazmino AK, Facemire C, Chen BJ, Kim HS, Tran TT, Pisetsky DS, Barisoni L, Prieto-Carrasquero MC, Jeansson M, Foster MH, Coffman TM. Glomerular type 1 angiotensin receptors augment kidney injury and inflammation in murine autoimmune nephritis. J Clin Invest 119: 943-953, 2009.
10. Dattilo M, Penington NJ, Williams K. Inhibition of TRPC5 channels by intracellular ATP. Mol Pharmacol 73: 42-49, 2008.
11. Dietrich A, Chubanov V, Gudermann T. Renal TRPathies. JAmSoc Nephrol 21: 736-744, 2010.
12. Dietrich A, Mederos YSM, Gollasch M, Gross V, Storch U, Dubrovska G, Obst M, Yildirim E, Salanova B, Kalwa H, Essin K, Pinkenburg O, Luft FC, Gudermann T, Birnbaumer L. Increased vascular smooth muscle contractility in TRPC6-/- mice. Mol Cell Biol 25: 6980-6989, 2005.
13. Dryer SE, Reiser J. TRPC6 channels and their binding partners in podocytes: role in glomerular filtration and pathophysiology. Am J Physiol Renal Physiol 299: F689-F701, 2010.
14. Du J, Sours-Brothers S, Coleman R, Ding M, Graham S, Kong DH, Ma R. Canonical transient receptor potential 1 channel is involved in contractile function of glomerular mesangial cells. J Am Soc Nephrol 18: 1437-1445, 2007.
15. Eckel J, Lavin PJ, Finch EA, Mukerji N, Burch J, Gbadegesin R, Wu G, Bowling B, Byrd A, Hall G, Sparks M, Zhang ZS, Homstad A, Barisoni L, Birbaumer L, Rosenberg P, Winn MP. TRPC6 enhances angiotensin II-induced albuminuria. J Am Soc Nephrol 22: 526-535, 2011.
16. Evans JF, Lee JH, Ragolia L. Ang-II-induced Ca2+ influx is mediated by the 1/4/5 subgroup of the transient receptor potential proteins in cultured aortic smooth muscle cells from diabetic Goto-Kakizaki rats. Mol Cell Endocrinol 302: 49-57, 2009.
17. Fellner SK, Arendshorst WJ. Angiotensin II-stimulated Ca2+ entry mechanisms in afferent arterioles: role of transient receptor potential canonical channels and reverse Na+/Ca2+ exchange. Am J Physiol Renal Physiol 294: F212-F219, 2008.
18. Fellner SK, Arendshorst WJ. Angiotensin II, reactive oxygen species, and Ca2+ signaling in afferent arterioles. Am J Physiol Renal Physiol 289: F1012-F1019, 2005.
19. Fornoni A, Merscher S, Kopp JB. Lipid biology of the podocyte—new perspectives offer new opportunities. Nat Rev Nephrol 10: 379-388, 2014.
20. Goel M, Sinkins WG, Zuo CD, Estacion M, Schilling WP. Identification and localization of TRPC channels in the rat kidney. Am J Physiol Renal Physiol 290: F1241-F1252, 2006.
21. Graham S, Ding M, Ding Y, Sours-Brothers S, Luchowski R, Gryc-zynski Z, Yorio T, Ma H, Ma R. Canonical transient receptor potential 6 (TRPC6), a redox-regulated cation channel. J Biol Chem 285: 23466-23476, 2010.
22. Graham S, Ding M, Sours-Brothers S, Yorio T, Ma JX, Ma R. Downregulation of TRPC6 protein expression by high glucose, a possible mechanism for the impaired Ca2+ signaling in glomerular mesangial cells in diabetes. Am J Physiol Renal Physiol 293: F1381-F1390, 2007.
23. Greka A, Mundel P. Balancing calcium signals through TRPC5 and TRPC6 in podocytes. J Am Soc Nephrol 22: 1969-1980, 2011.
24. Greka A, Mundel P. Cell biology and pathology of podocytes. Annu Rev Physiol 74: 299-323, 2012.
25. Heeringa SF, Moller CC, Du J, Yue L, Hinkes B, Chernin G, Vlangos CN, Hoyer PF, Reiser J, Hildebrandt F. A novel TRPC6 mutation that causes childhood FSGS. PLoS One 4: e7771, 2009.
26. Helal I, Fick-Brosnahan GM, Reed-Gitomer B, Schrier RW. Glomer-ular hyperfiltration: definitions, mechanisms and clinical implications. Nat Rev Nephrol 8: 293-300, 2012.
27. Huber TB, Schermer B, Muller RU, Hohne M, Bartram M, Calixto A, Hagmann H, Reinhardt C, Koos F, Kunzelmann K, Shirokova E, Krautwurst D, Harteneck C, Simons M, Pavenstadt H, Kerjaschki D, Thiele C, Walz G, Chalfie M, Benzing T. Podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels. Proc Natl Acad Sci USA 103: 17079-17086, 2006.
28. Ilatovskaya DV, Levchenko V, Ryan RP, Cowley AW Jr, Star-uschenko A. NSAIDs acutely inhibit TRPC channels in freshly isolated rat glomeruli. Biochem Biophys Res Commun 408: 242-247, 2011.
29. Ilatovskaya DV, Palygin O, Chubinskiy-Nadezhdin V, Negulyaev YA, Ma R, Birnbaumer L, Staruschenko A. Angiotensin II has acute effects on TRPC6 channels in podocytes of freshly isolated glomeruli. Kidney Int 86: 506-514, 2014.
30. Ilatovskaya DV, Palygin O, Levchenko V, Staruschenko A. Pharmacological characterization of the P2 receptors profile in the podocytes of the freshly isolated rat glomeruli. Am J Physiol Cell Physiol 305: C1050-C1059, 2013.
31. Ilatovskaya DV, Staruschenko A. Single-channel analysis of TRPC channels in the podocytes of freshly isolated glomeruli. Methods Mol Biol 998: 355-369, 2013.
32. Jefferson JA, Shankland SJ. The pathogenesis of focal segmental glo-merulosclerosis. Adv Chronic Kidney Dis 21: 408-416, 2014.
33. Kim EY, Anderson M, Dryer SE. Insulin increases surface expression of TRPC6 channels in podocytes: role of NADPH oxidases and reactive oxygen species. Am J Physiol Renal Physiol 302: F298-F307, 2012.
34. Kim EY, Anderson M, Wilson C, Hagmann H, Benzing T, Dryer SE. NOX2 interacts with podocyte TRPC6 channels and contributes to their activation by diacylglycerol: essential role of podocin in formation of this complex. Am J Physiol Cell Physiol 305: C960-C971, 2013.
35. Kim EY, Alvarez-Baron CP, Dryer SE. Canonical transient receptor potential channel (TRPC)3 and TRPC6 associate with large-conductance Ca2+-activated K+ (BKCa) channels: role in BKCa trafficking to the surface of cultured podocytes. Mol Pharmacol 75: 466-477, 2009.
36. Krall P, Canales CP, Kairath P, Carmona-Mora P, Molina J, Carpio JD, Ruiz P, Mezzano SA, Li J, Wei C, Reiser J, Young JI, Walz K. Podocyte-specific overexpression of wild type or mutant trpc6 in mice is sufficient to cause glomerular disease. PLoS One 5: e12859, 2010.
37. Kriz W, Shirato I, Nagata M, LeHir M, Lemley KV. The podocyte s response to stress: the enigma of foot process effacement. Am J Physiol Renal Physiol 304: F333-F347, 2013.
38. Liu BC, Song X, Lu XY, Li DT, Eaton DC, Shen BZ, Li XQ, Ma HP. High glucose induces podocyte apoptosis by stimulating TRPC6 via elevation of reactive oxygen species. Biochim Biophys Acta 1833: 1434-1442, 2013.
39. Majid DS, Kopkan L. Nitric oxide and superoxide interactions in the kidney and their implication in the development of salt-sensitive hypertension. Clin Exp Pharmacol Physiol 34: 946-952, 2007.
40. Moller CC, Flesche J, Reiser J. Sensitizing the slit diaphragm with TRPC6 ion channels. J Am Soc Nephrol 20: 950-953, 2009.
41. Moller CC, Wei C, Altintas MM, Li J, Greka A, Ohse T, Pippin JW, Rastaldi MP, Wawersik S, Schiavi S, Henger A, Kretzler M, Shank-land SJ, Reiser J. Induction of TRPC6 channel in acquired forms of proteinuric kidney disease. J Am Soc Nephrol 18: 29-36, 2007.
42. Nijenhuis T, Sloan AJ, Hoenderop JG, Flesche J, van Goor H, Kistler AD, Bakker M, Bindels RJ, de Boer RA, Moller CC, Hamming I, Navis G, Wetzels JF, Berden JH, Reiser J, Faul C, van der Vlag J. Angiotensin II contributes to podocyte injury by increasing TRPC6 expression via an NFAT-mediated positive feedback signaling pathway. Am J Pathol 179: 1719-1732, 2011.
43. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258: 607-614, 1992.
44. Palygin O, Levchenko V, Ilatovskaya DV, Pavlov TS, Ryan RP, Cowley AW, Staruschenko A. Real-time electrochemical detection of ATP and H2O2 release in freshly isolated kidneys. Am J Physiol Renal Physiol 305: F134-F141, 2013.
45. Putri AY, Thaha M. Role of oxidative stress on chronic kidney disease progression. Acta Med Indones 46: 244-252, 2014.
46. Reiser J, Polu KR, Moller CC, Kenlan P, Altintas MM, Wei C, Faul C, Herbert S, Villegas I, vila-Casado C, McGee M, Sugimoto H, Brown D, Kalluri R, Mundel P, Smith PL, Clapham DE, Pollak MR. TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 37: 739-744, 2005.
47. Roshanravan H, Dryer SE. ATP acting through P2Y receptors causes activation of podocyte TRPC6 channels: role of podocin and reactive oxygen species. Am J Physiol Renal Physiol 306: F1088-F1097, 2014.
48. Ruggenenti P, Cravedi P, Remuzzi G. Mechanisms and treatment of CKD. J Am Soc Nephrol 23: 1917-1928, 2012.
49. Schaldecker T, Kim S, Tarabanis C, Tian D, Hakroush S, Castonguay P, Ahn W, Wallentin H, Heid H, Hopkins CR, Lindsley CW, Riccio A, Buvall L, Weins A, Greka A. Inhibition of the TRPC5 ion channel protects the kidney filter. J Clin Invest 123: 5298-5309, 2013.
50. Schena FP. Primary glomerulonephritides with nephrotic syndrome. Limitations of therapy in adult patients. J Nephrol 12, Suppl 2: S125-S130, 1999.
51. Scott RP, Quaggin SE. The cell biology of renal filtration. J Cell Biol 209: 199-210, 2015.
52. Shah SV, Baliga R, Rajapurkar M, Fonseca VA. Oxidants in chronic kidney disease. J Am Soc Nephrol 18: 16-28, 2007.
53. Shankland SJ. The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int 69: 2131-2147, 2006.
54. Sonneveld R, van der Vlag J, Baltissen MP, Verkaart SA, Wetzels JF, Berden JH, Hoenderop JG, Nijenhuis T. Glucose specifically regulates TRPC6 expression in the podocyte in an AngII-dependent manner. Am J Pathol 184: 1715-1726, 2014.
55. Takenaka T, Suzuki H, Okada H, Inoue T, Kanno Y, Ozawa Y, Hayashi K, Saruta T. Transient receptor potential channels in rat renal microcirculation: actions of angiotensin II. Kidney Int 62: 558-565, 2002.
56. Tan RJ, Zhou D, Xiao L, Zhou L, Li Y, Bastacky SI, Oury TD, Liu Y. Extracellular superoxide dismutase protects against proteinuric kidney disease. J Am Soc Nephrol [Epub ahead of print].
57. Thilo F, Liu Y, Loddenkemper C, Schuelein R, Schmidt A, Yan Z, Zhu Z, Zakrzewicz A, Gollasch M, Tepel M. VEGF regulates TRPC6 channels in podocytes. Nephrol Dial Transplant 27: 921-929, 2012.
58. Tian D, Jacobo SM, Billing D, Rozkalne A, Gage SD, Anagnostou T, Pavenstadt H, Hsu HH, Schlondorff J, Ramos A, Greka A. Antagonistic regulation of actin dynamics and cell motility by TRPC5 and TRPC6 channels. Sci Signal 3: ra77, 2010.
59. Tian ML, Shen Y, Sun ZL, Zha Y. Efficacy and safety of combining pentoxifylline with angiotensin-converting enzyme inhibitor or angioten-sin II receptor blocker in diabetic nephropathy: a meta-analysis. Int Urol Nephrol 47: 815-822, 2015.
60. Wang L, Jirka G, Rosenberg PB, Buckley AF, Gomez JA, Fields TA, Winn MP, Spurney RF. Gq signaling causes glomerular injury by activating TRPC6. J Clin Invest 125: 1913-1926, 2015.
61. Wilson C, Dryer SE. A mutation in TRPC6 channels abolishes their activation by hypoosmotic stretch but does not affect activation by diacylglycerol or G protein signaling cascades. Am J Physiol Renal Physiol 306: F1018-F1025, 2014.
62. Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, Hawkins AF, Daskalakis N, Kwan SY, Ebersviller S, Burchette JL, Pericak-Vance MA, Howell DN, Vance JM, Rosenberg PB. A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308: 1801-1804, 2005.
63. Winn MP, Daskalakis N, Spurney RF, Middleton JP. Unexpected role of TRPC6 channel in familial nephrotic syndrome: does it have clinical implications? J Am Soc Nephrol 17: 378-387, 2006.
64. Woudenberg-Vrenken TE, Bindels RJ, Hoenderop JG. The role of transient receptor potential channels in kidney disease. Nature Rev Neph-rol 5: 441-449, 2009.
65. Zhang H, Ding J, Fan Q, Liu S. TRPC6 up-regulation in Ang II-induced podocyte apoptosis might result from ERK activation and NF-kappaB translocation. Exp Biol Med 234: 1029-1036, 2009.
66. Zhang X, Song Z, Guo Y, Zhou M. The novel role of TRPC6 in vitamin D ameliorating podocyte injury in STZ-induced diabetic rats. Mol Cell Biochem 399: 155-165, 2015.
67. Zhao B, Yang H, Zhang R, Sun H, Liao C, Xu J, Meng K, Jiao J. The role of TRPC6 in oxidative stress-induced podocyte ischemic injury. Biochem Biophys Res Commun 461: 413-420, 2015.