Proximal tubular cells contain a phenotypically distinct, scattered cell population involved in tubular regeneration

Journal of Pathology

Volumn 229, Issue 5, 2013, Pages 645-659

  Smeets, Bart ^a,b   Boor, Peter ^c,d   Dijkman, Henry ^b   Sharma, Shagun V ^b   Jirak, Peggy ^a   Mooren, Fieke ^b   Berger, Katja ^a   Bornemann, Jörg ^e   Gelman, Irwin H ^f   Floege, Jürgen ^a   Van Der Vlag, Johan ^b   Wetzels, Jack F M ^b   Moeller, Marcus J ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d Physics and Informatics   (Slovakia)

^e RWTH AACHEN UNIVERSITY   (Germany)

^f ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

acute tubular necrosis; progenitor cell; proximal tubules; regeneration

Indexed keywords

CD133 ANTIGEN; CD24 ANTIGEN; VIMENTIN;

ACUTE KIDNEY TUBULE NECROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEDIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL REGENERATION; CELL STRUCTURE; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY BIOPSY; KIDNEY TUBULE CELL; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; URETER OBSTRUCTION;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD24; BIOLOGICAL MARKERS; BIOPSY; CELL DEDIFFERENTIATION; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOPROTEINS; HUMANS; KIDNEY TUBULAR NECROSIS, ACUTE; KIDNEY TUBULES, PROXIMAL; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MICROSCOPY, IMMUNOELECTRON; MITOCHONDRIA; PEPTIDES; PHENOTYPE; RATS; RATS, WISTAR; REGENERATION; URETERAL OBSTRUCTION; VIMENTIN;

EID: 84875037125     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4125     Document Type: Article

References (40)

1. Vogetseder A, Palan T, Bacic D, et al,. Proximal tubular epithelial cells are generated by division of differentiated cells in the healthy kidney. Am J Physiol Cell Physiol 2007; 292: C807-C813.
2. Vogetseder A, Picard N, Gaspert A, et al,. Proliferation capacity of the renal proximal tubule involves the bulk of differentiated epithelial cells. Am J Physiol Cell Physiol 2008; 294: C22-C28.
3. Humphreys D, Valerius TM, Kobayashi A, et al,. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2008; 2: 284-291.
4. Song J, Czerniak S, Wang T, et al,. Characterization and fate of telomerase-expressing epithelia during kidney repair. J Am Soc Nephrol 2011; 22: 2256-2265.
5. Humphreys BD, Czerniak S, DiRocco DP, et al,. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci U S A 2011; 108: 9226-9231.
6. Kim K, Park BH, Ihm H, et al,. Expression of stem cell marker CD133 in fetal and adult human kidneys and pauci-immune crescentic glomerulonephritis. Histol Histopathol 2011; 26: 223-232.
7. Lindgren D, Bostrom AK, Nilsson K, et al,. Isolation and characterization of progenitor-like cells from human renal proximal tubules. Am J Pathol 2011; 178: 828-837.
8. Angelotti ML, Ronconi E, Ballerini L, et al,. Characterization of renal progenitors committed toward tubular lineage and their regenerative potential in renal tubular injury. Stem Cells 2012; 30: 1714-1725.
9. Pierres M, Naquet P, Barbet J, et al,. Evidence that murine hematopoietic cell subset marker J11d is attached to a glycosyl-phosphatidylinositol membrane anchor. Eur J Immunol 1987; 17: 1781-1785.
10. Shirasawa T, Akashi T, Sakamoto K, et al,. Gene expression of CD24 core peptide molecule in developing brain and developing non-neural tissues. Dev Dyn 1993; 198: 1-13.
11. Corbeil D, Roper K, Hellwig A, et al,. The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions. J Biol Chem 2000; 275: 5512-5520.
12. Ito Y, Hamazaki TS, Ohnuma K, et al,. Isolation of murine hair-inducing cells using the cell surface marker prominin-1/CD133. J Invest Dermatol 2007; 127: 1052-1060.
13. Richardson GD, Robson CN, Lang SH, et al,. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 2004; 117: 3539-3545.
14. Kemper K, Sprick MR, de Bree M, et al,. The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 2010; 70: 719-729.
15. Floege J, Hackmann B, Kliem V, et al,. Age-related glomerulosclerosis and interstitial fibrosis in Milan normotensive rats: a podocyte disease. Kidney Int 1997; 51: 230-243.
16. Sagrinati C, Netti GS, Mazzinghi B, et al,. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J Am Soc Nephrol 2006; 17: 2443-2456.
17. Uhlen M, Oksvold P, Fagerberg L, et al,. Towards a knowledge-based Human Protein Atlas. Nature Biotechnol 2010; 28: 1248-1250.
18. Han WK, Bailly V, Abichandani R, et al,. Kidney Injury Molecule-1 (KIM-1): a novel biomarker for human renal proximal tubule injury. Kidney Int 2002; 62: 237-244.
19. Ichimura T, Bonventre JV, Bailly V, et al,. Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is up-regulated in renal cells after injury. J Biol Chem 1998; 273: 4135-4142.
20. Moll R, Hage C, Thoenes W,. Expression of intermediate filament proteins in fetal and adult human kidney: modulations of intermediate filament patterns during development and in damaged tissue. Lab Invest 1991; 65: 74-86.
21. Burnworth B, Pippin J, Karna P, et al,. SSeCKS sequesters cyclin D1 in glomerular parietal epithelial cells and influences proliferative injury in the glomerulus. Lab Invest 2012; 92: 499-510.
22. Lin X, Nelson P, Gelman IH,. SSeCKS, a major protein kinase C substrate with tumor suppressor activity, regulates G(1)→S progression by controlling the expression and cellular compartmentalization of cyclin D. Mol Cell Biol 2000; 20: 7259-7272.
23. Grone HJ, Weber K, Grone E, et al,. Coexpression of keratin and vimentin in damaged and regenerating tubular epithelia of the kidney. Am J Pathol 1987; 129: 1-8.
24. Houghton DC, Hartnett M, Campbell-Boswell M, et al,. A light and electron microscopic analysis of gentamicin nephrotoxicity in rats. Am J Pathol 1976; 82: 589-612.
25. Venkatachalam MA, Bernard DB, Donohoe JF, et al,. Ischemic damage and repair in the rat proximal tubule: differences among the S1, S2, and S3 segments. Kidney Int 1978; 14: 31-49.
26. Wallin A, Zhang G, Jones TW, et al,. Mechanism of the nephrogenic repair response. Studies on proliferation and vimentin expression after 35S-1,2-dichlorovinyl-L-cysteine nephrotoxicity in vivo and in cultured proximal tubule epithelial cells. Lab Invest 1992; 66: 474-484.
27. Lewington AJ, Padanilam BJ, Martin DR, et al,. Expression of CD44 in kidney after acute ischemic injury in rats. Am J Physiol Regul Integr Comp Physiol 2000; 278: R247-R254.
28. Pollack V, Sarkozi R, Banki Z, et al,. Oncostatin M-induced effects on EMT in human proximal tubular cells: differential role of ERK signaling. Am J Physiol Renal Physiol 2007; 293: F1714-F1726.
29. Cheng CW, Rifai A, Ka SM, et al,. Calcium-binding proteins annexin A2 and S100A6 are sensors of tubular injury and recovery in acute renal failure. Kidney Int 2005; 68: 2694-2703.
30. Imgrund M, Grone E, Grone HJ, et al,. Re-expression of the developmental gene Pax-2 during experimental acute tubular necrosis in mice 1. Kidney Int 1999; 56: 1423-1431.
31. Langworthy M, Zhou B, de Caestecker M, et al,. NFATc1 identifies a population of proximal tubule cell progenitors. J Am Soc Nephrol 2009; 20: 311-321.
32. Akashi T, Shirasawa T, Hirokawa K,. Gene expression of CD24 core polypeptide molecule in normal rat tissues and human tumor cell lines. Virchows Arch 1994; 425: 399-406.
33. Figarella-Branger D, Moreau H, Pellissier JF, et al,. CD24, a signal-transducing molecule expressed on human B lymphocytes, is a marker for human regenerating muscle. Acta Neuropathol 1993; 86: 275-284.
34. Florek M, Haase M, Marzesco AM, et al,. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res 2005; 319: 15-26.
35. Griguer CE, Oliva CR, Gobin E, et al,. CD133 is a marker of bioenergetic stress in human glioma. PLoS One 2008; 3: e3655.
36. Shmelkov SV, Butler JM, Hooper AT, et al,. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 2008; 118: 2111-2120.
37. Chen HL, Pistollato F, Hoeppner DJ, et al,. Oxygen tension regulates survival and fate of mouse central nervous system precursors at multiple levels. Stem Cells 2007; 25: 2291-2301.
38. Stokman G, Stroo I, Claessen N, et al,. Stem cell factor expression after renal ischemia promotes tubular epithelial survival. PLoS One 2010; 5: e14386.
39. Kaplan C, Pasternack B, Shah H, et al,. Age-related incidence of sclerotic glomeruli in human kidneys. Am J Pathol 1975; 80: 227-234.
40. Goyal VK,. Changes with age in the human kidney. Exp Gerontol 1982; 17: 321-331.