Renal uptake of the antiapoptotic protein survivin is mediated by megalin at the apical membrane of the proximal tubule

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 5, 2013, Pages

  Jobst Schwan, Tilman ^a   Knaup, Karl X ^a   Nielsen, Rikke ^b   Hackenbeck, Thomas ^a   Buettner Herold, Maike ^a   Lechler, Philipp ^c   Kroening, Sven ^a   Goppelt Struebe, Margarethe ^a   Schloetzer Schrehardt, Ursula ^a   Fürnrohr, Barbara G ^a   Voll, Reinhard E ^d   Amann, Kerstin ^a   Eckardt, Kai Uwe ^a   Christensen, Erik I ^b   Wiesener, Michael S ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY HOSPITAL MARBURG   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Acute kidney injury; Apoptosis; Glomerular filtration; Lysosomes; Proteinuria

Indexed keywords

CUBILIN; MEGALIN; RECOMBINANT SURVIVIN; SURVIVIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTIBODY LABELING; APICAL MEMBRANE; APOPTOSIS; ARTICLE; BIOPSY; CELL CULTURE; COLOCALIZATION; CONCENTRATION (PARAMETERS); HUMAN; HUMAN CELL; HUMAN KIDNEY; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY METABOLISM; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE; KIDNEY TUBULE CELL; KNOCKOUT MOUSE; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SURFACE PLASMON RESONANCE; URINARY EXCRETION; WILD TYPE;

EID: 84883383849     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00546.2012     Document Type: Article

References (29)

1. Ahn JK, Oh JM, Lee J, Bae EK, Ahn KS, Cha HS, Koh EM. Increased extracellular survivin in the synovial fluid of rheumatoid arthritis patients: fibroblast-like synoviocytes as a potential source of extracellular survivin. Inflammation 33: 381-388, 2010.
2. Altieri DC. Survivin and IAP proteins in cell-death mechanisms. Biochem J 430: 199-205, 2010.
3. Birn H, Verroust PJ, Nexo E, Hager H, Jacobsen C, Christensen EI, Moestrup SK. Characterization of an epithelial ~460-kDa protein that facilitates endocytosis of intrinsic factor-vitamin B12 and binds receptorassociated protein. J Biol Chem 272: 26497-26504, 1997.
4. Christensen EI, Verroust PJ, Nielsen R. Receptor-mediated endocytosis in renal proximal tubule. Pflügers Arch 58: 1039-1048, 2009.
5. Davis MA, Ryan DH. Apoptosis in the kidney. Toxicol Pathol 26: 810-825, 1998.
6. Giaccone G, Zatloukal P, Roubec J, Floor K, Musil J, Kuta M, van Klaveren RJ, Chaudhary S, Gunther A, Shamsili S. Multicenter phase II trial of YM155, a small-molecule suppressor of survivin, in patients with advanced, refractory, non-small-cell lung cancer. J Clin Oncol 27: 4481-4486, 2009.
7. Herrington WG, Talbot DC, Lahn MM, Brandt JT, Callies S, Nagle R, Winearls CG, Roberts IS. Association of long-term administration of the survivin mRNA-targeted antisense oligonucleotide LY2181308 with reversible kidney injury in a patient with metastatic melanoma. Am J Kidney Dis 57: 300-303, 2011.
8. Kantarci S, Al-Gazali L, Hill RS, Donnai D, Black GC, Bieth E, Chassaing N, Lacombe D, Devriendt K, Teebi A, Loscertales M, Robson C, Liu T, MacLaughlin DT, Noonan KM, Russell MK, Walsh CA, Donahoe PK, Pober BR. Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculoacoustico- renal syndromes. Nat Genet 39: 957-959, 2007.
9. Khan S, Jutzy JM, Aspe JR, McGregor DW, Neidigh JW, Wall NR. Survivin is released from cancer cells via exosomes. Apoptosis 16: 1-12, 2011.
10. Kindt N, Menzebach A, Van de Wouwer M, Betz I, De Vriese A, Conway EM. Protective role of the inhibitor of apoptosis protein, survivin, in toxin-induced acute renal failure. FASEB J 22: 510-521, 2008.
11. Kroening S, Neubauer E, Wullich B, Aten J, Goppelt-Struebe M. Characterization of connective tissue growth factor expression in primary cultures of human tubular epithelial cells: modulation by hypoxia. Am J Physiol Renal Physiol 298: F796-F806, 2010.
12. Lechler P, Wu X, Bernhardt W, Campean V, Gastiger S, Hackenbeck T, Klanke B, Weidemann A, Warnecke C, Amann K, Engehausen D, Willam C, Eckardt K, Rödel F, Wiesener M. The tumor gene survivin is highly expressed in adult renal tubular cells: implications for a pathophysiological role in the kidney. Am J Pathol 171: 1483-1498, 2007.
13. Lewis KD, Samlowski W, Ward J, Catlett J, Cranmer L, Kirkwood J, Lawson D, Whitman E, Gonzalez R. A multi-center phase II evaluation of the small molecule survivin suppressor YM155 in patients with unresectable stage III or IV melanoma. Invest New Drugs 29: 161-166, 2011.
14. Lorz C, Ortiz A, Justo P, Gonzalez-Cuadrado S, Duque N, Gomez- Guerrero C, Egido J. Proapoptotic Fas ligand is expressed by normal kidney tubular epithelium and injured glomeruli. J Am Soc Nephrol 11: 1266-1277, 2000.
15. Lv YG, Yu F, Yao Q, Chen JH, Wang L. The role of survivin in diagnosis, prognosis and treatment of breast cancer. J Thorac Dis 2: 100-110, 2010.
16. Moestrup SK, Schousboe I, Jacobsen C, Leheste JR, Christensen EI, Willnow TE. Beta2-glycoprotein-I (apolipoprotein H) and beta2-glycoprotein- I-phospholipid complex harbor a recognition site for the endocytic receptor megalin. J Clin Invest 102: 902-909, 1998.
17. Moser M, Pscherer A, Roth C, Becker J, Mucher G, Zerres K, Dixkens C, Weis J, Guay-Woodford L, Buettner R, Fassler R. Enhanced apoptotic cell death of renal epithelial cells in mice lacking transcription factor AP-2beta. Genes Dev 11: 1938-1948, 1997.
18. Nadasdy T, Laszik Z, Blick KE, Johnson LD, Silva FG. Proliferative activity of intrinsic cell populations in the normal human kidney. J Am Soc Nephrol 4: 2032-2039, 1994.
19. Nykjaer A, Dragun D, Walther D, Vorum H, Jacobsen C, Herz J, Melsen F, Christensen EI, Willnow TE. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 96: 507-515, 1999.
20. Nykjaer A, Fyfe JC, Kozyraki R, Leheste JR, Jacobsen C, Nielsen MS, Verroust PJ, Aminoff M, de la Chapelle A, Moestrup SK, Ray R, Gliemann J, Willnow TE, Christensen EI. Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D(3). Proc Natl Acad Sci USA 98: 13895-13900, 2001.
21. Ortiz A, Justo P, Sanz A, Lorz C, Egido J. Targeting apoptosis in acute tubular injury. Biochem Pharmacol 66: 1589-1594, 2003.
22. Satoh T, Okamoto I, Miyazaki M, Morinaga R, Tsuya A, Hasegawa Y, Terashima M, Ueda S, Fukuoka M, Ariyoshi Y, Saito T, Masuda N, Watanabe H, Taguchi T, Kakihara T, Aoyama Y, Hashimoto Y, Nakagawa K. Phase I study of YM155, a novel survivin suppressant, in patients with advanced solid tumors. Clin Cancer Res 15: 3872-3880, 2009.
23. Smith SD, Wheeler MA, Plescia J, Colberg JW, Weiss RM, Altieri DC. Urine detection of survivin and diagnosis of bladder cancer. JAMA 285: 324-328, 2001.
24. Storm T, Tranebjærg L, Frykholm C, Birn H, Verroust PJ, Nevéus T, Sundelin B, Hertz JM, Holmström G, Ericson K, Christensen EI, Nielsen R. Renal phenotypic investigations of megalin-deficient patients: novel insights into tubular proteinuria and albumin filtration. Nephrol Dial Transplant 28: 585-591, 2013.
25. Tolcher AW, Quinn DI, Ferrari A, Ahmann F, Giaccone G, Drake T, Keating A, de Bono JS. A phase II study of YM155, a novel smallmolecule suppressor of survivin, in castration-resistant taxane-pretreated prostate cancer. Ann Oncol 23: 968-973, 2012.
26. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75: 229-240, 1993.
27. Verdecia MA, Huang H, Dutil E, Kaiser DA, Hunter T, Noel JP. Structure of the human anti-apoptotic protein survivin reveals a dimeric arrangement. Nat Struct Biol 7: 602-608, 2000.
28. Weyer K, Storm T, Shan J, Vainio S, Kozyraki R, Verroust PJ, Christensen EI, Nielsen R. Mouse model of proximal tubule endocytic dysfunction. Nephrol Dial Transplant 26: 3446-3451, 2011.
29. Willnow TE, Hilpert J, Armstrong SA, Rohlmann A, Hammer RE, Burns DK, Herz J. Defective forebrain development in mice lacking gp330/megalin. Proc Natl Acad Sci USA 93: 8460-8464, 1996.