Extracellular nucleotides from dying cells act as molecular signals to promote wound repair in renal tubular injury

American Journal of Physiology - Renal Physiology

Volumn 307, Issue 12, 2014, Pages F1404-F1411

  Nakagawa, Shunsaku ^a   Omura, Tomohiro ^a   Yonezawa, Atsushi ^a   Yano, Ikuko ^a   Nakagawa, Takayuki ^a   Matsubara, Kazuo ^a  

^a KYOTO UNIVERSITY HOSPITAL   (Japan)

Author keywords

Acute kidney injury; Acute renal failure; ATP; Cell to cell communication; Compensatory proliferation

Indexed keywords

ADENOSINE TRIPHOSPHATE; APYRASE; CASPASE 3; CASPASE 7; CISPLATIN; LACTATE DEHYDROGENASE; NUCLEOTIDE; PROTEIN P53; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PURINERGIC P2Y6 RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; SURAMIN; BIOLOGICAL MARKER; KI 67 ANTIGEN; PURINERGIC P2 RECEPTOR; PURINERGIC P2 RECEPTOR ANTAGONIST;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COMMUNICATION; CELL DAMAGE; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; IN VITRO STUDY; INJURY SEVERITY; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE DAMAGE; KIDNEY TUBULE EPITHELIUM; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ULTRAVIOLET IRRADIATION; WOUND HEALING; ACUTE KIDNEY FAILURE; ANIMAL; CELL LINE; CELL MOTION; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; KIDNEY TUBULE; METABOLISM; PATHOLOGY; RADIATION RESPONSE; SEVERITY OF ILLNESS INDEX; TIME; WISTAR RAT;

ACUTE KIDNEY INJURY; ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL MARKERS; CELL COMMUNICATION; CELL DEATH; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CISPLATIN; DISEASE MODELS, ANIMAL; KI-67 ANTIGEN; KIDNEY TUBULES; MALE; PURINERGIC P2 RECEPTOR ANTAGONISTS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; TIME FACTORS; WOUND HEALING;

EID: 84918782209     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00196.2014     Document Type: Article

References (49)

1. Allam R, Scherbaum CR, Darisipudi MN, Mulay SR, Hägele H, Lichtnekert J, Hagemann JH, Rupanagudi KV, Ryu M, Schwarzenberger C, Hohenstein B, Hugo C, Uhl B, Reichel CA, Krombach F, Monestier M, Liapis H, Moreth K, Schaefer L, Anders HJ. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol 23: 1375–1388, 2012.
2. Anders HJ. Toll-like receptors and danger signaling in kidney injury. J Am Soc Nephrol 21: 1270–1274, 2010.
3. Anderson S, Eldadah B, Halter JB, Hazzard WR, Himmelfarb J, Horne FM, Kimmel PL, Molitoris BA, Murthy M, O’Hare AM, Schmader KE, High KP. Acute kidney injury in older adults. J Am Soc Nephrol 22: 28–38, 2011.
4. Bihorac A, Yavas S, Subbiah S, Hobson CE, Schold JD, Gabrielli A, Layon AJ, Segal MS. Long-term risk of mortality and acute kidney injury during hospitalization after major surgery. Ann Surg 249: 851–858, 2009.
5. Bilbao PS, Santillán G, Boland R. ATP stimulates the proliferation of MCF-7 cells through the PI3K/Akt signaling pathway. Arch Biochem Biophys 499: 40–48, 2010.
6. Bonventre JV. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol 14, Suppl 1: S55–S61, 2003.
7. Burnstock G. Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol Rev 58: 58–86, 2006.
8. Burnstock G. Purinergic signaling and vascular cell proliferation and death. Arterioscler Thromb Vasc Biol 22: 364–373, 2002.
9. Campanholle G, Mittelsteadt K, Nakagawa S, Kobayashi A, Lin SL, Gharib SA, Heinecke JW, Hamerman JA, Altemeier WA, Duffield JS. TLR-2/TLR-4 TREM-1 signaling pathway is dispensable in inflammatory myeloid cells during sterile kidney injury. PLos One 8: e68640, 2013.
10. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, Isakson BE, Bayliss DA, Ravichandran KS. Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 467: 863–867, 2010.
11. Darisipudi MN, Thomasova D, Mulay SR, Brech D, Noessner E, Liapis H, Anders HJ. Uromodulin triggers IL-1_-dependent innate immunity via the NLRP3 inflammasome. J Am Soc Nephrol 23: 1783–1789, 2012.
12. Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol 17: 1503–1520, 2006.
13. Du C, Wang S, Diao H, Guan Q, Zhong R, Jevnikar AM. Increasing resistance of tubular epithelial cells to apoptosis by shRNA therapy ameliorates renal ischemia-reperfusion injury. Am J Transplant 6: 2256–2267, 2006.
14. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, Lysiak JJ, Harden TK, Leitinger N, Ravichandran KS. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461: 282–286, 2009.
15. Filipski KK, Mathijssen RH, Mikkelsen TS, Schinkel AH, Sparreboom A. Contribution of organic cation transporter 2 (OCT2) to cisplatininduced nephrotoxicity. Clin Pharmacol Ther 86: 396–402, 2009.
16. Furuichi K, Wada T, Iwata Y, Kitagawa K, Kobayashi K, Hashimoto H, Ishiwata Y, Asano M, Wang H, Matsushima K, Takeya M, Kuziel WA, Mukaida N, Yokoyama H. CCR2 signaling contributes to ischemiareperfusion injury in kidney. J Am Soc Nephrol 14: 2503–2515, 2003.
17. Grgic I, Campanholle G, Bijol V, Wang C, Sabbisetti VS, Ichimura T, Humphreys BD, Bonventre JV. Targeted proximal tubule injury triggers interstitial fibrosis and glomerulosclerosis. Kidney Int 82: 172–183, 2012.
18. Hoste EA, Lameire NH, Vanholder RC, Benoit DD, Decruyenaere JM, Colardyn FA. Acute renal failure in patients with sepsis in a surgical ICU: predictive factors, incidence, comorbidity, and outcome. J Am Soc Nephrol 14: 1022–1030, 2003.
19. Humphreys BD, Czerniak S, DiRocco DP, Hasnain W, Cheema R, Bonventre JV. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA 108: 9226–9231, 2011.
20. Humphreys BD, Valerius MT, Kobayashi A, Mugford JW, Soeung S, Duffield JS, McMahon AP, Bonventre JV. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2: 284–291, 2008.
21. Katz S, Ayala V, Santillán G, Boland R. Activation of the PI3K/Akt signaling pathway through P2Y2 receptors by extracellular ATP is involved in osteoblastic cell proliferation. Arch Biochem Biophys 513: 144–152, 2011.
22. Kida Y, Ieronimakis N, Schrimpf C, Reyes M, Duffield JS. EphrinB2 reverse signaling protects against capillary rarefaction and fibrosis after kidney injury. J Am Soc Nephrol 24: 559–572, 2013.
23. Komlosi P, Fintha A, Bell PD. Renal cell-to-cell communication via extracellular ATP. Physiology (Bethesda) 20: 86–90, 2005.
24. Kurts C, Panzer U, Anders HJ, Rees AJ. The immune system and kidney disease: basic concepts and clinical implications. Nat Rev Immunol 13: 738–753, 2013.
25. Kuwana H, Terada Y, Kobayashi T, Okado T, Penninger JM, Irie-Sasaki J, Sasaki T, Sasaki S. The phosphoinositide-3 kinase gamma-Akt pathway mediates renal tubular injury in cisplatin nephrotoxicity. Kidney Int 73: 430–445, 2008.
26. Li F, Huang Q, Chen J, Peng Y, Roop DR, Bedford JS, Li CY. Apoptotic cells activate the “phoenix rising” pathway to promote wound healing and tissue regeneration. Sci Signal 3: ra13, 2010.
27. Linkermann A, Himmerkus N, Rölver L, Keyser KA, Steen P, Bräsen JH, Bleich M, Kunzendorf U, Krautwald S. Renal tubular Fas ligand mediates fratricide in cisplatin-induced acute kidney failure. Kidney Int 79: 169–178, 2011.
28. Martins I, Tesniere A, Kepp O, Michaud M, Schlemmer F, Senovilla L, Séror C, Métivier D, Perfettini JL, Zitvogel L, Kroemer G. Chemotherapy induces ATP release from tumor cells. Cell Cycle 8: 3723–3728, 2009.
29. Martins I, Wang Y, Michaud M, Ma Y, Sukkurwala AQ, Shen S, Kepp O, Métivier D, Galluzzi L, Perfettini JL, Zitvogel L, Kroemer G. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ 21: 79–91, 2014.
30. Motohashi H, Sakurai Y, Saito H, Masuda S, Urakami Y, Goto M, Fukatsu A, Ogawa O, Inui K. Gene expression levels and immunolocalization of organic ion transporters in the human kidney. J Am Soc Nephrol 13: 866–874, 2002.
31. Nakagawa S, Nishihara K, Inui K, Masuda S. Involvement of autophagy in the pharmacological effects of the mTOR inhibitor everolimus in acute kidney injury. Eur J Pharmacol 696: 143–154, 2012.
32. Nakamura T, Yonezawa A, Hashimoto S, Katsura T, Inui K. Disruption of multidrug and toxin extrusion MATE1 potentiates cisplatin-induced nephrotoxicity. Biochem Pharmacol 80: 1762–1767, 2010.
33. Nechemia-Arbely Y, Barkan D, Pizov G, Shriki A, Rose-John S, Galun E, Axelrod JH. IL-6/IL-6R axis plays a critical role in acute kidney injury. J Am Soc Nephrol 19: 1106–1115, 2008.
34. Nishina T, Komazawa-Sakon S, Yanaka S, Piao X, Zheng DM, Piao JH, Kojima Y, Yamashina S, Sano E, Putoczki T, Doi T, Ueno T, Ezaki J, Ushio H, Ernst M, Tsumoto K, Okumura K, Nakano H. Interleukin-11 links oxidative stress and compensatory proliferation. Sci Signal 5: ra5, 2012.
35. Perazella MA. Renal vulnerability to drug toxicity. Clin J Am Soc Nephrol 4: 1275–1283, 2009.
36. Schmitt R, Coca S, Kanbay M, Tinetti ME, Cantley LG, Parikh CR. Recovery of kidney function after acute kidney injury in the elderly: a systematic review and meta-analysis. Am J Kidney Dis 52: 262–271, 2008.
37. Schrimpf C, Xin C, Campanholle G, Gill SE, Stallcup W, Lin SL, Davis GE, Gharib SA, Humphreys BD, Duffield JS. Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J Am Soc Nephrol 23: 868–883, 2012.
38. Schroder K, Tschopp J. The inflammasomes. Cell 140: 821–832, 2010.
39. Staples CJ, Owens DM, Maier JV, Cato AC, Keyse SM. Cross-talk between the p38alpha and JNK MAPK pathways mediated by MAP kinase phosphatase-1 determines cellular sensitivity to UV radiation. J Biol Chem 285: 25928–25940, 2010.
40. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 140: 805–820, 2010.
41. Thadhani R, Pascual M, Bonventre JV. Acute renal failure. N Engl J Med 334: 1448–1460, 1996.
42. Tsuruya K, Ninomiya T, Tokumoto M, Hirakawa M, Masutani K, Taniguchi M, Fukuda K, Kanai H, Kishihara K, Hirakata H, Iida M. Direct involvement of the receptor-mediated apoptotic pathways in cisplatin-induced renal tubular cell death. Kidney Int 63: 72–82, 2003.
43. Vallon V, Stockand J, Rieg T. P2Y receptors and kidney function. Wiley Interdiscip Rev Membr Transp Signal 1: 731–742, 2012.
44. Venkatachalam MA, Bernard DB, Donohoe JF, Levinsky NG. Ischemic damage and repair in the rat proximal tubule: differences among the S1, S2, and S3 segments. Kidney Int 14: 31–49, 1978.
45. Vilaysane A, Chun J, Seamone ME, Wang W, Chin R, Hirota S, Li Y, Clark SA, Tschopp J, Trpkov K, Hemmelgarn BR, Beck PL, Muruve DA. The NLRP3 inflammasome promotes renal inflammation and contributes to CKD. J Am Soc Nephrol 21: 1732–1744, 2010.
46. Wilden PA, Agazie YM, Kaufman R, Halenda SP. ATP-stimulated smooth muscle cell proliferation requires independent ERK and PI3K signaling pathways. Am J Physiol Heart Circ Physiol 275: H1209–H1215, 1998.
47. Wu H, Ma J, Wang P, Corpuz TM, Panchapakesan U, Wyburn KR, Chadban SJ. HMGB1 contributes to kidney ischemia reperfusion injury. J Am Soc Nephrol 21: 1878–1890, 2010.
48. Yonezawa A, Inui K. Organic cation transporter OCT/SLC22A and H/organic cation antiporter MATE/SLC47A are key molecules for nephrotoxicity of platinum agents. Biochem Pharmacol 81: 563–568, 2011.
49. Zanke BW, Boudreau K, Rubie E, Winnett E, Tibbles LA, Zon L, Kyriakis J, Liu FF, Woodgett JR. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr Biol 6: 606–613, 1996.