Characterization and fate of telomerase-expressing epithelia during kidney repair

Journal of the American Society of Nephrology

Volumn 22, Issue 12, 2011, Pages 2256-2265

  Song, Jie ^a,b   Czerniak, Suzanne ^a   Wang, Teresa ^a   Ying, Wendy ^a   Carlone, Diana L ^c,d   Breault, David T ^c,d,e   Humphreys, Benjamin D ^a,d,e,f  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b FUDAN UNIVERSITY   (China)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HARVARD STEM CELL INSTITUTE   (United States)

^f HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; MESSENGER RNA; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CONTROLLED STUDY; HENLE LOOP; KIDNEY CELL; KIDNEY COLLECTING TUBULE; KIDNEY EPITHELIUM; KIDNEY INJURY; KIDNEY ISCHEMIA; KIDNEY PAPILLA; MALE; MOUSE; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; STAINING; STEM CELL; TISSUE REPAIR;

EID: 82655181483     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2011050447     Document Type: Article

References (46)

1. USRDS 2010 Annual Data Report: Atlas of Chronic Kidney Disease in the United States. 2010 ed., National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD, 2010
2. Messier B, Leblond CP: Cell proliferation and migration as revealed by radioautography after injection of thymidine-H3 into male rats and mice. Am J Anat 106: 247-285, 1960
3. 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 (Pubitemid 8396236)
4. Witzgall R, Brown D, Schwarz C, Bonventre JV: Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney. Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiated cells. J Clin Invest 93: 2175-2188, 1994
5. Melk A, Ramassar V, Helms LM, Moore R, Rayner D, Solez K, Halloran PF: Telomere shortening in kidneys with age. J Am Soc Nephrol 11: 444-453, 2000 (Pubitemid 30115074)
6. Westhoff JH, Schildhorn C, Jacobi C, Homme M, Hartner A, Braun H, Kryzer C, Wang C, von Zglinicki T, Kranzlin B, Gretz N, Melk A: Telomere shortening reduces regenerative capacity after acute kidney injury. J Am Soc Nephrol 21: 327-336, 2010
7. Wills LP, Schnellmann RG: Telomere shortening and regenerative capacity after acute kidney injury. J Am Soc Nephrol 21: 202-204, 2010
8. Greenberg RA, Allsopp RC, Chin L, Morin GB, DePinho RA: Expression of mouse telomerase reverse transcriptase during development, differentiation and proliferation. Oncogene 16: 1723-1730, 1998 (Pubitemid 28175053)
9. Artandi, SE: Telomerase as a potential regulator of tissue progenitor cells. In: Telomeres and Telomerase in Ageing, Disease, and Cancer, edited by Rudolph KL, Berlin, Springer-Verlag, 2008, pp 203-210
10. Armstrong L, Lako M, Lincoln J, Cairns PM, Hole N: mTert expression correlates with telomerase activity during the differentiation of murine embryonic stem cells. Mech Dev 97: 109-116, 2000
11. Breault DT, Min IM, Carlone DL, Farilla LG, Ambruzs DM, Henderson DE, Algra S, Montgomery RK, Wagers AJ, Hole N: Generation of mTert-GFP mice as a model to identify and study tissue progenitor cells. Proc Natl Acad Sci U S A 105: 10420-10425, 2008
12. Stadtfeld M, Maherali N, Breault DT, Hochedlinger K: Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2: 230-240, 2008
13. Montgomery RK, Carlone DL, Richmond CA, Farilla L, Kranendonk ME, Henderson DE, Baffour-Awuah NY, Ambruzs DM, Fogli LK, Algra S, Breault DT: Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. Proc Natl Acad Sci U S A 108: 179-184, 2011
14. Lee HW, Blasco MA, Gottlieb GJ, Horner JW, 2nd, Greider CW, DePinho RA: Essential role of mouse telomerase in highly proliferative organs. Nature 392: 569-574, 1998 (Pubitemid 28207706)
15. Little MH, Bertram JF: Is there such a thing as a renal stem cell? J Am Soc Nephrol 20: 2112-2117, 2009
16. 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 (Pubitemid 351298594)
17. 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 U S A 108: 9226-9231, 2011
18. Oliver JA, Maarouf O, Cheema FH, Martens TP, Al-Awqati Q: The renal papilla is a niche for adult kidney stem cells. J Clin Invest 114: 795-804, 2004 (Pubitemid 39578738)
19. Oliver JA, Klinakis A, Cheema FH, Friedlander J, Sampogna RV, Martens TP, Liu C, Efstratiadis A, Al-Awqati Q: Proliferation and migration of label-retaining cells of the kidney papilla. J Am Soc Nephrol 20: 2315-2327, 2009
20. Langworthy M, Zhou B, de Caestecker M, Moeckel G, Baldwin HS: NFATc1 identifies a population of proximal tubule cell progenitors. J Am Soc Nephrol 20: 311-321, 2009
21. Maeshima A, Sakurai H, Nigam SK: Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity, and integration capability into developing kidney. J Am Soc Nephrol 17: 188-198, 2006
22. Gupta S, Verfaillie C, Chmielewski D, Kren S, Eidman K, Connaire J, Heremans Y, Lund T, Blackstad M, Jiang Y, Luttun A, Rosenberg ME: Isolation and characterization of kidney-derived stem cells. J Am Soc Nephrol 17: 3028-3040, 2006 (Pubitemid 44707763)
23. Kitamura S, Yamasaki Y, Kinomura M, Sugaya T, Sugiyama H, Maeshima Y, Makino H: Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J 19: 1789-1797, 2005 (Pubitemid 41598763)
24. Appel D, Kershaw DB, Smeets B, Yuan G, Fuss A, Frye B, Elger M, Kriz W, Floege J, Moeller MJ: Recruitment of podocytes from glomerular parietal epithelial cells. J Am Soc Nephrol 20: 333-343, 2009
25. Ronconi E, Sagrinati C, Angelotti ML, Lazzeri E, Mazzinghi B, Ballerini L, Parente E, Becherucci F, Gacci M, Carini M, Maggi E, Serio M, Vannelli GB, Lasagni L, Romagnani S, Romagnani P: Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 20: 322-332, 2009
26. Wu A, Ichihashi M, Ueda M: Correlation of the expression of human telomerase subunits with telomerase activity in normal skin and skin tumors. Cancer 86: 2038-2044, 1999
27. Ali AS, Chopra R, Robertson J, Testa NG: Detection of hTERT protein by flow cytometry. Leukemia 14: 2176-2181, 2000 (Pubitemid 32042258)
28. Xu D, Gruber A, Peterson C, Pisa P: Telomerase activity and the expression of telomerase components in acute myelogenous leukaemia. Br J Haematol 102: 1367-1375, 1998 (Pubitemid 28435229)
29. Nielsen S, Frokiaer J, Marples D, Kwon TH, Agre P, Knepper MA: Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82: 205-244, 2002 (Pubitemid 34654219)
30. Kiel MJ, He S, Ashkenazi R, Gentry SN, Teta M, Kushner JA, Jackson TL, Morrison SJ: Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 449: 238-242, 2007 (Pubitemid 47402371)
31. Hochegger K, Koppelstatter C, Tagwerker A, Huber JM, Heininger D, Mayer G, Rosenkranz, AR: p21 and mTERT are novel markers for determining different ischemic time periods in renal ischemia reperfusion injury. Am J Physiol Renal Physiol, 292: F762-F768, 2007 (Pubitemid 46220544)
32. Duffield JS, Humphreys, BD: Origin of new cells in the adult kidney: Results from genetic labeling techniques. Kidney Int 2010
33. Stellwagen AE, Haimberger ZW, Veatch JR, Gottschling DE: Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev 17: 2384-2395, 2003 (Pubitemid 37214787)
34. Masutomi K, Possemato R, Wong JM, Currier JL, Tothova Z, Manola JB, Ganesan S, Lansdorp PM, Collins K, Hahn WC: The telomerase reverse transcriptase regulates chromatin state and DNA damage responses. Proc Natl Acad Sci U S A 102: 8222-8227, 2005 (Pubitemid 40800070)
35. Cong Y, Shay JW: Actions of human telomerase beyond telomeres. Cell Res 18: 725-732, 2008 (Pubitemid 351948231)
36. Meyerson M, Counter CM, Eaton EN, Ellisen LW, Steiner P, Caddle SD, Ziaugra L, Beijersbergen RL, Davidoff MJ, Liu Q, Bacchetti S, Haber DA, Weinberg RA: hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90: 785-795, 1997 (Pubitemid 27357969)
37. Dmitrieva NI, Cai Q, Burg MB: Cells adapted to high NaCl have many DNA breaks and impaired DNA repair both in cell culture and in vivo. Proc Natl Acad Sci U S A 101: 2317-2322, 2004 (Pubitemid 38269309)
38. Adams DC, Oxburgh L: The long-term label retaining population of the renal papilla arises through divergent regional growth of the kidney. Am J Physiol Renal Physiol 297: F809-F815, 2009
39. Xu X, D'Hoker J, Stange G, Bonne S, De Leu N, Xiao X, Van de Casteele M, Mellitzer G, Ling Z, Pipeleers D, Bouwens L, Scharfmann R, Gradwohl G, Heimberg H: Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132: 197-207, 2008 (Pubitemid 351181232)
40. He W, Wang Y, Zhang MZ, You L, Davis LS, Fan H, Yang HC, Fogo AB, Zent R, Harris RC, Breyer MD, Hao CM: Sirt1 activation protects the mouse renal medulla from oxidative injury. J Clin Invest 120: 1056-1068, 2010
41. Dmitrieva NI, Celeste A, Nussenzweig A, Burg MB: Ku86 preserves chromatin integrity in cells adapted to high NaCl. Proc Natl Acad Sci U S A 102: 10730-10735, 2005 (Pubitemid 41061622)
42. Chai W, Ford LP, Lenertz L, Wright WE, Shay JW: Human Ku70/80 associates physically with telomerase through interaction with hTERT. J Biol Chem 277: 47242-47247, 2002 (Pubitemid 36159235)
43. Palacios JA, Herranz D, De Bonis ML, Velasco S, Serrano M, Blasco MA: SIRT1 contributes to telomere maintenance and augments global homologous recombination. J Cell Biol 191: 1299-1313, 2010
44. Sabolic I, Valenti G, Verbavatz JM, Van Hoek AN, Verkman AS, Ausiello DA, Brown D: Localization of the CHIP28 water channel in rat kidney. Am J Physiol 263: C1225-C1233, 1992 (Pubitemid 23024428)
45. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS: Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 176: 85-97, 2010
46. Lyon-Roberts B, Strait KA, van Peursem E, Kittikulsuth W, Pollock JS, Pollock DM, Kohan DE: Flow regulation of collecting duct endothelin-1 production. Am J Physiol Renal Physiol 300: F650-F656, 2011