Sepsis-Associated AKI: Epithelial Cell Dysfunction

Seminars in Nephrology

Volumn 35, Issue 1, 2015, Pages 85-95

  Emlet, David R ^a,b   Shaw, Andrew D ^c   Kellum, John A ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute kidney injury; DAMPs and PAMPs; Renal tubule epithelial cell; Sepsis

Indexed keywords

ACUTE KIDNEY FAILURE; BIOENERGY; CAUSAL ATTRIBUTION; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL DEDIFFERENTIATION; CELL FATE; CELL FUNCTION; DISEASE ASSOCIATION; EPITHELIUM CELL; HUMAN; KIDNEY ISCHEMIA; KIDNEY TUBULE CELL; MICROCIRCULATION; MITOCHONDRION; NEPHRITIS; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RENAL TUBULE EPITHELIAL CELL; REVIEW; SEPSIS; ACUTE KIDNEY INJURY; COMPLICATION; CYTOLOGY; INFLAMMATION; KIDNEY; KIDNEY DISTAL TUBULE; KIDNEY PROXIMAL TUBULE; METABOLISM; PHYSIOLOGY;

ACUTE KIDNEY INJURY; EPITHELIAL CELLS; HUMANS; INFLAMMATION; KIDNEY; KIDNEY TUBULES, DISTAL; KIDNEY TUBULES, PROXIMAL; OXIDATIVE STRESS; SEPSIS;

EID: 84925266168     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2015.01.009     Document Type: Review

References (92)

1. Angus D.C., Linde-Zwirble W.T., Lidicker J., Clermont G., Carcillo J., Pinsky M.R. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001, 29:1303-1310.
2. Mayr F.B., Yende S., Angus D.C. Epidemiology of severe sepsis. Virulence 2014, 5:4-11.
3. Dellinger R.P., Levy M.M., Rhodes A., Annane D., Gerlach H., Opal S.M., et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Med 2013, 39:165-228.
4. Uchino S., Kellum J.A., Bellomo R., Doig G.S., Morimatsu H., Morgera S., et al. Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA 2005, 294:813-818.
5. Bagshaw S.M., George C., Dinu I., Bellomo R. A multi-centre evaluation of the RIFLE criteria for early acute kidney injury in critically ill patients. Nephrol Dial Transplant 2008, 23:1203-1210.
6. Ricci Z., Cruz D., Ronco C. The RIFLE criteria and mortality in acute kidney injury: a systematic review. Kidney Int 2008, 73:538-546.
7. Wen X., Peng Z., Kellum J.A. Pathogenesis of acute kidney injury: effects of remote tissue damage on the kidney. Contrib Nephrol 2011, 174:129-137.
8. Gomez H., Ince C., De B.D., Pickkers P., Payen D., Hotchkiss J., et al. A unified theory of sepsis-induced acute kidney injury: inflammation, microcirculatory dysfunction, bioenergetics, and the tubular cell adaptation to injury. Shock 2014, 41:3-11.
9. Wiersinga W.J., Leopold S.J., Cranendonk D.R., van der Poll T. Host innate immune responses to sepsis. Virulence 2014, 5:36-44.
10. Akcay A., Nguyen Q., Edelstein C.L. Mediators of inflammation in acute kidney injury. Mediators Inflamm 2009, 2009. 137072.
11. Wolfs T.G., Buurman W.A., van Schadewijk A., de Vries B., Daemen M.A., Hiemstra P.S., et al. In vivo expression of Toll-like receptor 2 and 4 by renal epithelial cells: IFN-gamma and TNF-alpha mediated up-regulation during inflammation. J Immunol 2002, 168:1286-1293.
12. Bonventre J.V., Zuk A. Ischemic acute renal failure: an inflammatory disease?. Kidney Int 2004, 66:480-485.
13. Vaidya V.S., Waikar S.S., Ferguson M.A., Collings F.B., Sunderland K., Gioules C., et al. Urinary biomarkers for sensitive and specific detection of acute kidney injury in humans. Clin Transl Sci 2008, 1:200-208.
14. Hultman P., Enestrom S. Localization of mercury in the kidney during experimental acute tubular necrosis studied by the cytochemical silver amplification method. Br J Exp Pathol 1986, 67:493-503.
15. Usuda K., Kono K., Dote T., Nishiura K., Miyata K., Nishiura H., et al. Urinary biomarkers monitoring for experimental fluoride nephrotoxicity. Arch Toxicol 1998, 72:104-109.
16. Kalakeche R., Hato T., Rhodes G., Dunn K.W., El-Achkar T.M., Plotkin Z., et al. Endotoxin uptake by S1 proximal tubular segment causes oxidative stress in the downstream S2 segment. J Am Soc Nephrol 2011, 22:1505-1516.
17. Zhang B., Ramesh G., Uematsu S., Akira S., Reeves W.B. TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J Am Soc Nephrol 2008, 19:923-932.
18. van K.C., Woltman A.M., Daha M.R. Immunological function of tubular epithelial cells: the functional implications of CD40 expression. Exp Nephrol 2000, 8:203-207.
19. Ho A.W., Wong C.K., Lam C.W. Tumor necrosis factor-alpha up-regulates the expression of CCL2 and adhesion molecules of human proximal tubular epithelial cells through MAPK signaling pathways. Immunobiology 2008, 213:533-544.
20. Langenberg C., Bellomo R., May C., Wan L., Egi M., Morgera S. Renal blood flow in sepsis. Crit Care 2005, 9:R363-R374.
21. Murugan R., Karajala-Subramanyam V., Lee M., Yende S., Kong L., Carter M., et al. Acute kidney injury in non-severe pneumonia is associated with an increased immune response and lower survival. Kidney Int 2010, 77:527-535.
22. Saotome T., Langenberg C., Wan L., Ramchandra R., May C.N., Bellomo R., et al. Early and sustained systemic and renal hemodynamic effects of intravenous radiocontrast. Blood Purif 2010, 29:339-346.
23. Rosen S., Heyman S.N. Difficulties in understanding human "acute tubular necrosis": limited data and flawed animal models. Kidney Int 2001, 60:1220-1224.
24. Cantaluppi V., Quercia A.D., Dellepiane S., Ferrario S., Camussi G., Biancone L. Interaction between systemic inflammation and renal tubular epithelial cells. Nephrol Dial Transplant 2014, 29:2004-2011.
25. Carlson B.M. Some principles of regeneration in mammalian systems. Anat Rec B New Anat 2005, 287:4-13.
26. Humphreys B.D., Valerius M.T., Kobayashi A., Mugford J.W., Soeung S., Duffield J.S., et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2008, 2:284-291.
27. Price P.M., Megyesi J., Safirstein R.L. Cell cycle regulation: repair and regeneration in acute renal failure. Semin Nephrol 2003, 23:449-459.
28. Yang Q.H., Liu D.W., Long Y., Liu H.Z., Chai W.Z., Wang X.T. Acute renal failure during sepsis: potential role of cell cycle regulation. J Infect 2009, 58:459-464.
29. Mulay S.R., Thomasova D., Ryu M., Anders H.J. MDM2 (murine double minute-2) links inflammation and tubular cell healing during acute kidney injury in mice. Kidney Int 2012, 81:1199-1211.
30. Lee D.H., Wolstein J.M., Pudasaini B., Plotkin M. INK4a deletion results in improved kidney regeneration and decreased capillary rarefaction after ischemia-reperfusion injury. Am J Physiol Renal Physiol 2012, 302:F183-F191.
31. Kashani K., Al-Khafaji A., Ardiles T., Artigas A., Bagshaw S.M., Bell M., et al. Discovery and validation of cell cycle arrest biomarkers in human acute kidney injury. Crit Care 2013, 17:R25.
32. Seo D.W., Li H., Qu C.K., Oh J., Kim Y.S., Diaz T., et al. Shp-1 mediates the antiproliferative activity of tissue inhibitor of metalloproteinase-2 in human microvascular endothelial cells. J Biol Chem 2006, 281:3711-3721.
33. Boonstra J., Post J.A. Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 2004, 337:1-13.
34. Severino V., Alessio N., Farina A., Sandomenico A., Cipollaro M., Peluso G., et al. Insulin-like growth factor binding proteins 4 and 7 released by senescent cells promote premature senescence in mesenchymal stem cells. Cell Death Dis 2013, 4:e911.
35. Benatar T., Yang W., Amemiya Y., Evdokimova V., Kahn H., Holloway C., et al. IGFBP7 reduces breast tumor growth by induction of senescence and apoptosis pathways. Breast Cancer Res Treat 2012, 133:563-573.
36. Lin J., Lai M., Huang Q., Ruan W., Ma Y., Cui J. Reactivation of IGFBP7 by DNA demethylation inhibits human colon cancer cell growth in vitro. Cancer Biol Ther 2008, 7:1896-1900.
37. Vizioli M.G., Sensi M., Miranda C., Cleris L., Formelli F., Anania M.C., et al. IGFBP7: an oncosuppressor gene in thyroid carcinogenesis. Oncogene 2010, 29:3835-3844.
38. Declerck Y.A., Perez N., Shimada H., Boone T.C., Langley K.E., Taylor S.M. Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases. Cancer Res 1992, 52:701-708.
39. Koop S., Khokha R., Schmidt E.E., MacDonald I.C., Morris V.L., Chambers A.F., et al. Overexpression of metalloproteinase inhibitor in B16F10 cells does not affect extravasation but reduces tumor growth. Cancer Res 1994, 54:4791-4797.
40. Mohammed F.F., Pennington C.J., Kassiri Z., Rubin J.S., Soloway P.D., Ruther U., et al. Metalloproteinase inhibitor TIMP-1 affects hepatocyte cell cycle via HGF activation in murine liver regeneration. Hepatology 2005, 41:857-867.
41. Jaworski D.M., Perez-Martinez L. Tissue inhibitor of metalloproteinase-2 (TIMP-2) expression is regulated by multiple neural differentiation signals. J Neurochem 2006, 98:234-247.
42. Seo D.W., Li H., Guedez L., Wingfield P.T., Diaz T., Salloum R., et al. TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism. Cell 2003, 114:171-180.
43. Tang Y., Huang X.R., Lv J., Chung A.C., Zhang Y., Chen J.Z., et al. C-reactive protein promotes acute kidney injury by impairing G1/S-dependent tubular epithelium cell regeneration. Clin Sci (Lond) 2014, 126:645-659.
44. Little M.H. Regrow or repair: potential regenerative therapies for the kidney. J Am Soc Nephrol 2006, 17:2390-2401.
45. Bonventre J.V. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol 2003, 14(Suppl 1):S55-S61.
46. Maeshima A., Sakurai H., Nigam S.K. Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity, and integration capability into developing kidney. J Am Soc Nephrol 2006, 17:188-198.
47. Kitamura S., Yamasaki Y., Kinomura M., Sugaya T., Sugiyama H., Maeshima Y., et al. Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J 2005, 19:1789-1797.
48. Bussolati B., Bruno S., Grange C., Buttiglieri S., Deregibus M.C., Cantino D., et al. Isolation of renal progenitor cells from adult human kidney. Am J Pathol 2005, 166:545-555.
49. Gupta S., Verfaillie C., Chmielewski D., Kren S., Eidman K., Connaire J., et al. Isolation and characterization of kidney-derived stem cells. J Am Soc Nephrol 2006, 17:3028-3040.
50. Angelotti M.L., Ronconi E., Ballerini L., Peired A., Mazzinghi B., Sagrinati C., et al. Characterization of renal progenitors committed toward tubular lineage and their regenerative potential in renal tubular injury. Stem Cells 2012, 30:1714-1725.
51. Vogetseder A., Palan T., Bacic D., Kaissling B., Le H.M. Proximal tubular epithelial cells are generated by division of differentiated cells in the healthy kidney. Am J Physiol Cell Physiol 2007, 292:C807-C813.
52. Kusaba T., Lalli M., Kramann R., Kobayashi A., Humphreys B.D. Differentiated kidney epithelial cells repair injured proximal tubule. Proc Natl Acad Sci U S A 2014, 111:1527-1532.
53. Che R., Yuan Y., Huang S., Zhang A. Mitochondrial dysfunction in the pathophysiology of renal diseases. Am J Physiol Renal Physiol 2014, 306:F367-F378.
54. Hall A.M., Unwin R.J., Parker N., Duchen M.R. Multiphoton imaging reveals differences in mitochondrial function between nephron segments. J Am Soc Nephrol 2009, 20:1293-1302.
55. Bagnasco S., Good D., Balaban R., Burg M. Lactate production in isolated segments of the rat nephron. Am J Physiol 1985, 248:F522-F526.
56. Visarius T.M., Putt D.A., Schare J.M., Pegouske D.M., Lash L.H. Pathways of glutathione metabolism and transport in isolated proximal tubular cells from rat kidney. Biochem Pharmacol 1996, 52:259-272.
57. Weinberg J.M., Harding P.G., Humes H.D. Mechanisms of gentamicin-induced dysfunction of renal cortical mitochondria. II. Effects on mitochondrial monovalent cation transport. Arch Biochem Biophys 1980, 205:232-239.
58. Weinberg J.M., Harding P.G., Humes H.D. Mitochondrial bioenergetics during the initiation of mercuric chloride-induced renal injury. II. Functional alterations of renal cortical mitochondria isolated after mercuric chloride treatment. J Biol Chem 1982, 257:68-74.
59. Zhan M., Brooks C., Liu F., Sun L., Dong Z. Mitochondrial dynamics: regulatory mechanisms and emerging role in renal pathophysiology. Kidney Int 2013, 83:568-581.
60. Stidwill R.P., Rosser D.M., Singer M. Cardiorespiratory, tissue oxygen and hepatic NADH responses to graded hypoxia. Intensive Care Med 1998, 24:1209-1216.
61. Srinivasan S., Avadhani N.G. Cytochrome c oxidase dysfunction in oxidative stress. Free Radic Biol Med 2012, 53:1252-1263.
62. Larsen F.J., Schiffer T.A., Weitzberg E., Lundberg J.O. Regulation of mitochondrial function and energetics by reactive nitrogen oxides. Free Radic Biol Med 2012, 53:1919-1928.
63. Bauer I., Pannen B.H. Bench-to-bedside review: carbon monoxide--from mitochondrial poisoning to therapeutic use. Crit Care 2009, 13:220.
64. Szabo C., Modis K. Pathophysiological roles of peroxynitrite in circulatory shock. Shock 2010, 34(Suppl 1):4-14.
65. Brooks C., Cho S.G., Wang C.Y., Yang T., Dong Z. Fragmented mitochondria are sensitized to Bax insertion and activation during apoptosis. Am J Physiol Cell Physiol 2011, 300:C447-C455.
66. Ferraro E., Cecconi F. Autophagic and apoptotic response to stress signals in mammalian cells. Arch Biochem Biophys 2007, 462:210-219.
67. Lerolle N., Nochy D., Guerot E., Bruneval P., Fagon J.Y., Diehl J.L., et al. Histopathology of septic shock induced acute kidney injury: apoptosis and leukocytic infiltration. Intensive Care Med 2010, 36:471-478.
68. Hotchkiss R.S., Swanson P.E., Freeman B.D., Tinsley K.W., Cobb J.P., Matuschak G.M., et al. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 1999, 27:1230-1251.
69. Mariano F., Cantaluppi V., Stella M., Romanazzi G.M., Assenzio B., Cairo M., et al. Circulating plasma factors induce tubular and glomerular alterations in septic burns patients. Crit Care 2008, 12:R42.
70. Havasi A., Borkan S.C. Apoptosis and acute kidney injury. Kidney Int 2011, 80:29-40.
71. Ko G.J., Grigoryev D.N., Linfert D., Jang H.R., Watkins T., Cheadle C., et al. Transcriptional analysis of kidneys during repair from AKI reveals possible roles for NGAL and KIM-1 as biomarkers of AKI-to-CKD transition. Am J Physiol Renal Physiol 2010, 298:F1472-F1483.
72. Wu X., Guo R., Chen P., Wang Q., Cunningham P.N. TNF induces caspase-dependent inflammation in renal endothelial cells through a Rho- and myosin light chain kinase-dependent mechanism. Am J Physiol Renal Physiol 2009, 297:F316-F326.
73. Green D.R. The end and after: how dying cells impact the living organism. Immunity 2011, 35:441-444.
74. Vanhorebeek I., Gunst J., Derde S., Derese I., Boussemaere M., Dhoore A., et al. Mitochondrial fusion, fission, and biogenesis in prolonged critically ill patients. J Clin Endocrinol Metab 2012, 97:E59-E64.
75. Green D.R., Galluzzi L., Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011, 333:1109-1112.
76. Wu S., Zhou F., Zhang Z., Xing D. Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins. FEBS J 2011, 278:941-954.
77. Tang W.X., Wu W.H., Qiu H.Y., Bo H., Huang S.M. Amelioration of rhabdomyolysis-induced renal mitochondrial injury and apoptosis through suppression of Drp-1 translocation. J Nephrol 2013, 26:1073-1082.
78. Waltz P., Carchman E.H., Young A.C., Rao J., Rosengart M.R., Kaczorowski D., et al. Lipopolysaccaride induces autophagic signaling in macrophages via a TLR4, heme oxygenase-1 dependent pathway. Autophagy 2011, 7:315-320.
79. Frank M., Duvezin-Caubet S., Koob S., Occhipinti A., Jagasia R., Petcherski A., et al. Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim Biophys Acta 2012, 1823:2297-2310.
80. Wang Y., Nartiss Y., Steipe B., McQuibban G.A., Kim P.K. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 2012, 8:1462-1476.
81. Hsiao H.W., Tsai K.L., Wang L.F., Chen Y.H., Chiang P.C., Chuang S.M., et al. The decline of autophagy contributes to proximal tubular dysfunction during sepsis. Shock 2012, 37:289-296.
82. Gunst J., Derese I., Aertgeerts A., Ververs E.J., Wauters A., Van den Berghe G., et al. Insufficient autophagy contributes to mitochondrial dysfunction, organ failure, and adverse outcome in an animal model of critical illness. Crit Care Med 2013, 41:182-194.
83. Messmer U.K., Briner V.A., Pfeilschifter J. Tumor necrosis factor-alpha and lipopolysaccharide induce apoptotic cell death in bovine glomerular endothelial cells. Kidney Int 1999, 55:2322-2337.
84. Holthoff J.H., Wang Z., Seely K.A., Gokden N., Mayeux P.R. Resveratrol improves renal microcirculation, protects the tubular epithelium, and prolongs survival in a mouse model of sepsis-induced acute kidney injury. Kidney Int 2012, 81:370-378.
85. Seely K.A., Holthoff J.H., Burns S.T., Wang Z., Thakali K.M., Gokden N., et al. Hemodynamic changes in the kidney in a pediatric rat model of sepsis-induced acute kidney injury. Am J Physiol Renal Physiol 2011, 301:F209-F217.
86. Wu L., Gokden N., Mayeux P.R. Evidence for the role of reactive nitrogen species in polymicrobial sepsis-induced renal peritubular capillary dysfunction and tubular injury. J Am Soc Nephrol 2007, 18:1807-1815.
87. Laycock S.K., Vogel T., Forfia P.R., Tuzman J., Xu X., Ochoa M., et al. Role of nitric oxide in the control of renal oxygen consumption and the regulation of chemical work in the kidney. Circ Res 1998, 82:1263-1271.
88. Borutaite V., Brown G.C. Rapid reduction of nitric oxide by mitochondria, and reversible inhibition of mitochondrial respiration by nitric oxide. Biochem J 1996, 315:295-299.
89. Boulos M., Astiz M.E., Barua R.S., Osman M. Impaired mitochondrial function induced by serum from septic shock patients is attenuated by inhibition of nitric oxide synthase and poly(ADP-ribose) synthase. Crit Care Med 2003, 31:353-358.
90. Wang Z., Holthoff J.H., Seely K.A., Pathak E., Spencer H.J., Gokden N., et al. Development of oxidative stress in the peritubular capillary microenvironment mediates sepsis-induced renal microcirculatory failure and acute kidney injury. Am J Pathol 2012, 180:505-516.
91. Tran M., Tam D., Bardia A., Bhasin M., Rowe G.C., Kher A., et al. PGC-1alpha promotes recovery after acute kidney injury during systemic inflammation in mice. J Clin Invest 2011, 121:4003-4014.
92. Bonventre J.V., Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 2011, 121:4210-4221.