Prominin-2 is a novel marker of distal tubules and collecting ducts of the human and murine kidney

Histochemistry and Cell Biology

Volumn 133, Issue 5, 2010, Pages 527-539

  Jászai, József ^a   Farkas, Lilla M ^b   Fargeas, Christine A ^a   Janich, Peggy ^a   Haase, Michael ^c   Huttner, Wieland B ^b   Corbeil, Denis ^a  

^a CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Basolateral membrane; Collecting duct; Kidney; Membrane vesicles; Nephron; Prominin; Tubular epithelium

Indexed keywords

BIOLOGICAL MARKER; CD133 ANTIGEN; PROMININ 2; UNCLASSIFIED DRUG; AQP2 PROTEIN, MOUSE; AQUAPORIN 2; CALBINDIN; COTRANSPORTER; DRUG RECEPTOR; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; MUCOPROTEIN; PEPTIDE; PROM2 PROTEIN, HUMAN; PROM2 PROTEIN, MOUSE; RECOMBINANT PROTEIN; S100 CALCIUM BINDING PROTEIN G; SLC12A1 PROTEIN, HUMAN; SLC12A1 PROTEIN, MOUSE; SLC12A3 PROTEIN, MOUSE; SODIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2; TAMM HORSFALL GLYCOPROTEIN; UMOD PROTEIN, HUMAN; UMOD PROTEIN, MOUSE;

ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; HENLE LOOP; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KIDNEY COLLECTING TUBULE; KIDNEY DISTAL TUBULE; KIDNEY EPITHELIUM; MEMBRANE VESICLE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; UROTHELIUM; ANIMAL; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INBRED MOUSE STRAIN; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY PELVIS; METABOLISM; NEPHRON; URINE;

MURINAE; MUS;

ANIMALS; ANTIGENS, CD; AQUAPORIN 2; CALBINDINS; EPITHELIAL CELLS; GENE EXPRESSION; GLYCOPROTEINS; HUMANS; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY PELVIS; KIDNEY TUBULES, COLLECTING; KIDNEY TUBULES, DISTAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED STRAINS; MUCOPROTEINS; NEPHRONS; PEPTIDES; RECEPTORS, DRUG; RECOMBINANT PROTEINS; S100 CALCIUM BINDING PROTEIN G; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SOLUTE CARRIER FAMILY 12, MEMBER 1; SOLUTE CARRIER FAMILY 12, MEMBER 3; SYMPORTERS; UROMODULIN; UROTHELIUM;

EID: 77952242525     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-010-0690-1     Document Type: Article

References (50)

1. S Bachmann R Metzger B Bunnemann 1990 Tamm-Horsfall protein-mRNA synthesis is localized to the thick ascending limb of Henle's loop in rat kidney Histochemistry 94 517 523 10.1007/BF00272616 1:CAS:528:DyaK3cXlvVylsb4%3D 2283315 (Pubitemid 20303247)
2. S Bachmann HM Bosse P Mundel 1995 Topography of nitric oxide synthesis by localizing constitutive NO synthases in mammalian kidney Am J Physiol 268 F885 F898 1:CAS:528:DyaK2MXlvVajsLs%3D 7539586
3. HL Biner MP Arpin-Bott J Loffing X Wang M Knepper SC Hebert B Kaissling 2002 Human cortical distal nephron: distribution of electrolyte and water transport pathways J Am Soc Nephrol 13 836 847 11912242
4. B Bussolati S Bruno C Grange S Buttiglieri MC Deregibus D Cantino G Camussi 2005 Isolation of renal progenitor cells from adult human kidney Am J Pathol 166 545 555 1:CAS:528:DC%2BD2MXitVGms7o%3D 15681837
5. V Câmpean J Kricke D Ellison FC Luft S Bachmann 2001 Localization of thiazide-sensitive Na(+)-Cl(-) cotransport and associated gene products in mouse DCT Am J Physiol Renal Physiol 281 F1028 F1035 11704553
6. D Corbeil K Röper A Weigmann WB Huttner 1998 AC133 hematopoietic stem cell antigen: human homologue of mouse kidney prominin or distinct member of a novel protein family? Blood 91 2625 2626 1:CAS:528:DyaK1cXitF2htrc%3D 9516170
7. D Corbeil K Röper MJ Hannah A Hellwig WB Huttner 1999 Selective localization of the polytopic membrane protein prominin in microvilli of epithelial cells-a combination of apical sorting and retention in plasma membrane protrusions J Cell Sci 112 1023 1033 1:CAS:528:DyaK1MXis12ls7k%3D 10198284
8. D Corbeil K Röper A Hellwig M Tavian S Miraglia SM Watt PJ Simmons B Peault DW Buck WB Huttner 2000 The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions J Biol Chem 275 5512 5520 10.1074/jbc.275.8.5512 1:CAS:528:DC%2BD3cXhsFKksbk%3D 10681530 (Pubitemid 30115186)
9. D Corbeil K Röper CA Fargeas A Joester WB Huttner 2001 Prominin: a story of cholesterol, plasma membrane protrusions and human pathology Traffic 2 82 91 10.1034/j.1600-0854.2001.020202.x 1:CAS:528:DC%2BD3MXhtFCisr4%3D 11247306 (Pubitemid 32219860)
10. D Corbeil CA Fargeas WB Huttner 2001 Rat prominin, like its mouse and human orthologues, is a pentaspan membrane glycoprotein Biochem Biophys Res Commun 4 939 944 10.1006/bbrc.2001.5271 (Pubitemid 32918027)
11. D Corbeil A Joester CA Fargeas J Jászai J Garwood HB Werner WB Huttner 2009 Expression of distinct splice variants of the stem cell marker prominin-1 (CD133) in glial cells Glia 57 860 874 10.1002/glia.20812 19053060
12. V Dubreuil A-M Marzesco D Corbeil WB Huttner M Wilsch-Bräuninger 2007 Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1 J Cell Biol 176 483 495 10.1083/jcb.200608137 1:CAS:528:DC%2BD2sXhvFCqtrw%3D 17283184
13. J El-Annan D Brown S Breton, et al. 2004 Differential expression and targeting of endogenous Arf1 and Arf6 small GTPases in kidney epithelial cells in situ Am J Physiol Cell Physiol 286 C768 C778 10.1152/ajpcell.00250.2003 1:CAS:528:DC%2BD2cXjtlagtr0%3D 14684384
14. CA Fargeas M Florek WB Huttner D Corbeil 2003 Characterization of prominin-2, a new member of the prominin family of pentaspan membrane glycoproteins J Biol Chem 278 8586 8596 10.1074/jbc.M210640200 1:CAS:528:DC%2BD3sXhsF2ht7s%3D 12514187 (Pubitemid 36800613)
15. CA Fargeas D Corbeil WB Huttner 2003 AC133 antigen, CD133, prominin-1, prominin-2. etc.: prominin family gene products in need of a rational nomenclature Stem Cells 21 506 508 10.1634/stemcells.21-4-506 1:CAS:528:DC%2BD3sXmtVWns7k%3D 12832703
16. CA Fargeas A Joester E Missol-Kolka A Hellwig WB Huttner D Corbeil 2004 Identification of novel prominin-1/CD133 splice variants with alternative C-termini and their expression in epididymis and testis J Cell Sci 117 4301 4311 10.1242/jcs.01315 1:CAS:528:DC%2BD2cXotlGrtLo%3D 15316084 (Pubitemid 39328316)
17. CA Fargeas A-V Fonseca WB Huttner D Corbeil 2006 Prominin-1 (CD133)-from progenitor cells to human diseases Future Lipidol 1 213 225 10.2217/17460875.1. 2.213 1:CAS:528:DC%2BD28Xktleru7o%3D
18. CA Fargeas WB Huttner D Corbeil 2007 Nomenclature of prominin-1 (CD133) splice variants - an update Tissue Antigens 69 602 606 10.1111/j.1399-0039.2007. 00825.x 1:CAS:528:DC%2BD2sXntVyksr8%3D 17498271 (Pubitemid 46733679)
19. LM Farkas C Haffner T Giger P Khaitovich K Nowick C Birchmeier S Pääbo WB Huttner 2008 Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex Neuron 60 40 55 10.1016/j.neuron.2008.09.020 1:CAS:528:DC%2BD1cXhtlSrtrzE 18940587
20. M Florek M Haase AM Marzesco D Freund G Ehninger WB Huttner D Corbeil 2005 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 319 15 26 10.1007/s00441-004-1018-z 1:CAS:528:DC%2BD2cXhtVGgtLjE 15558321 (Pubitemid 40104635)
21. M Florek N Bauer P Janich M Wilsch-Bräuninger CA Fargeas A-M Marzesco G Ehninger C Thiele WB Huttner D Corbeil 2007 Prominin-2 is a cholesterol-binding protein associated with apical and basolateral plasmalemmal protrusions in polarized epithelial cells and released into urine Cell Tissue Res 328 31 47 10.1007/s00441-006-0324-z 1:CAS:528:DC%2BD2sXivVShtbg%3D 17109118 (Pubitemid 46411908)
22. A Gut F Kappeler N Hyka MS Balda HP Hauri K Matter 1998 Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins EMBO J 17 1919 1929 10.1093/emboj/17.7.1919 1:CAS:528:DyaK1cXisV2ktb4%3D 9524115 (Pubitemid 28154522)
23. HB Huttner P Janich M Köhrmann J Jászai F Siebzehnrubl I Blümcke M Suttorp M Gahr D Kuhnt C Nimsky D Krex G Schackert K Löwenbrück H Reichmann E Jüttler W Hacke P Schellinger S Schwab M Wilsch-Bräuninger A-M Marzesco D Corbeil 2008 The stem cell marker prominin-1/CD133 on membrane particles in human cerebrospinal fluid offers novel approaches for studying CNS disease Stem Cells 26 698 705 10.1634/stemcells. 2007-0639 1:CAS:528:DC%2BD1cXltVKitL8%3D 18096722
24. 3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells FEBS Lett 581 1783 1787 10.1016/j.febslet.2007.03.065 1:CAS:528: DC%2BD2sXksV2rtr0%3D 17428477 (Pubitemid 46628803)
25. J Jászai CA Fargeas M Florek WB Huttner D Corbeil 2007 Focus on molecules: prominin-1 (CD133) Exp Eye Res 85 585 586 10.1016/j.exer.2006.03.022 16733052 (Pubitemid 350001359)
26. J Jászai P Janich LM Farkas CA Fargeas WB Huttner D Corbeil 2007 Differential expression of prominin-1 (CD133) and prominin-2 in major cephalic exocrine glands of adult mice Histochem Cell Biol 128 409 419 10.1007/s00418-007-0334-2 17874118 (Pubitemid 350163687)
27. J Jászai CA Fargeas M Haase LM Farkas WB Huttner D Corbeil 2008 Robust expression of prominin-2 all along the adult male reproductive system and urinary bladder Histochem Cell Biol 130 749 759 10.1007/s00418-008-0445-4 18536929
28. J Karbanová E Missol-Kolka AV Fonseca C Lorra P Janich H Hollerová J Jászai J Ehrmann Z Kolár C Liebers S Arl D Subrtová D Freund J Mokry WB Huttner D Corbeil 2008 The stem cell marker CD133 (prominin-1) is expressed in various human glandular epithelia J Histochem Cytochem 56 977 993 10.1369/jhc.2008.951897 18645205
29. R Kojima T Sekine M Kawachi, et al. 2002 Immunolocalization of multispecific organic anion transporters, OAT1, OAT2, and OAT3, in rat kidney J Am Soc Nephrol 13 848 857 1:CAS:528:DC%2BD38XjtFSnsLg%3D 11912243
30. L Laitinen I Virtanen L Saxén 1987 Changes in the glycosylation pattern during embryonic development of mouse kidney as revealed with lectin conjugates J Histochem Cytochem 35 55 65 1:CAS:528:DyaL2sXmsVynug%3D%3D 3794309
31. J Lardon D Corbeil WB Huttner Z Ling L Bouwens 2008 Stem cell marker prominin-1/AC133 is expressed in duct cells of the adult human pancreas Pancreas 36 e1 e6 10.1097/mpa.0b013e318149f2dc 18192867
32. A Lee JD Kessler TA Read C Kaiser D Corbeil WB Huttner JE Johnson RJ Wechsler-Reya 2005 Isolation of neural stem cells from the postnatal cerebellum Nat Neurosci 8 723 729 10.1038/nn1473 1:CAS:528:DC%2BD2MXksVeit7c%3D 15908947 (Pubitemid 43085837)
33. A-M Marzesco P Janich M Wilsch-Bräuninger V Dubreuil K Langenfeld D Corbeil WB Huttner 2005 Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells J Cell Sci 118 2849 2858 10.1242/jcs.02439 1:CAS:528: DC%2BD2MXnsVCjtrk%3D 15976444 (Pubitemid 41136362)
34. A-M Marzesco M Wilsch-Bräuninger V Dubreuil P Janich K Langenfeld C Thiele WB Huttner D Corbeil 2009 Release of extracellular membrane vesicles from microvilli of epithelial cells is enhanced by depleting membrane cholesterol FEBS Lett 583 897 902 10.1016/j.febslet.2009.01.048 1:CAS:528: DC%2BD1MXis1aqtb8%3D 19302789
35. MA Maw D Corbeil J Koch A Hellwig JC Wilson-Wheeler RJ Bridges G Kumaramanickavel S John D Nancarrow K Röper A Weigmann WB Huttner MJ Denton 2000 A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration Hum Mol Genet 9 27 34 10.1093/hmg/9.1.27 1:CAS:528: DC%2BD3cXmt1ersQ%3D%3D 10587575
36. JK McKenzie EG McQueen 1969 Immunofluorescent localization of Tamm-Horsfall mucoprotein in human kidney J Clin Pathol 22 334 339 10.1136/jcp.22.3.334 1:STN:280:DyaF1M3gs1Sqtg%3D%3D 4891482
37. S Miraglia W Godfrey AH Yin K Atkins R Warnke JT Holden RA Bray EK Waller DW Buck 1997 A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning Blood 90 5013 5021 1:CAS:528:DyaK2sXnvFWkt7c%3D 9389721
38. P Mundel S Bachmann M Bader A Fischer W Kummer B Mayer W Kriz 1992 Expression of nitric oxide synthase in kidney macula densa cells Kidney Int 42 1017 1019 10.1038/ki.1992.382 1:CAS:528:DyaK3sXktlyl 1280698
39. S Nielsen J Frøkiaer D Marples TH Kwon P Agre MA Knepper 2002 Aquaporins in the kidney: from molecules to medicine Physiol Rev 82 205 244 1:CAS:528:DC%2BD38XovFSitw%3D%3D 11773613
40. GD Richardson CN Robson SH Lang DE Neal NJ Maitland AT Collins 2004 CD133, a novel marker for human prostatic epithelial stem cells J Cell Sci 117 3539 3545 10.1242/jcs.01222 1:CAS:528:DC%2BD2cXntFersbc%3D 15226377 (Pubitemid 39206394)
41. K Röper D Corbeil WB Huttner 2000 Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane Nat Cell Biol 2 582 592 10.1038/35023524 10980698
42. C Sagrinati GS Netti B Mazzinghi E Lazzeri F Liotta F Frosali E Ronconi C Meini M Gacci R Squecco M Carini L Gesualdo F Francini E Maggi F Annunziato L Lasagni M Serio S Romagnani P Romagnani 2006 Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys J Am Soc Nephrol 17 2443 2456 10.1681/ASN.2006010089 1:CAS:528: DC%2BD28XpvFOgu7s%3D 16885410 (Pubitemid 44300960)
43. P Scheiffele J Peranen K Simons 1995 N-glycans as apical sorting signals in epithelial cells Nature 378 96 98 10.1038/378096a0 1:CAS:528: DyaK2MXptVyqs7w%3D 7477300
44. N Uchida DW Buck D He MJ Reitsma M Masek TV Phan AS Tsukamoto FH Gage IL Weissman 2000 Direct isolation of human central nervous system stem cells Proc Natl Acad Sci USA 97 14720 14725 10.1073/pnas.97.26.14720 1:CAS:528: DC%2BD3MXitVGgtg%3D%3D 11121071 (Pubitemid 32016642)
45. A Weigmann D Corbeil A Hellwig WB Huttner 1997 Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells Proc Natl Acad Sci USA 94 12425 12430 10.1073/pnas.94.23.12425 1:CAS:528:DyaK2sXns1ylsb8%3D 9356465 (Pubitemid 27492544)
46. Y Yamada S Yokoyama XD Wang N Fukuda N Takakura 2007 Cardiac stem cells in brown adipose tissue express CD133 and induce bone marrow nonhematopoietic cells to differentiate into cardiomyocytes Stem Cells 25 1326 1333 10.1634/stemcells.2006-0588 1:CAS:528:DC%2BD2sXlvF2jsrc%3D 17289932 (Pubitemid 46684893)
47. Z Yang Y Chen C Lillo J Chien M Michaelides M Klein KA Howes Y Li Y Kaminoh H Chen C Zhao Y Chen YT Al-Sheikh G Karan D Corbeil P Escher S Kamaya C Li S Johnson JM Frederick Y Zhao C Wang DJ Cameron WB Huttner DF Schorderet FL Munier AT Moore DG Birch W Baehr DM Hunt DS Williams K Zhang 2008 Mutant prominin-1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice J Clin Invest 118 2908 2916 10.1172/JCI35876 1:CAS:528:DC%2BD1cXpsVOkurw%3D 18654668
48. AH Yin S Miraglia ED Zanjani G Almeida-Porada M Ogawa AG Leary J Olweus J Kearney DW Buck 1997 AC133, a novel marker for human hematopoietic stem and progenitor cells Blood 90 5002 5012 1:CAS:528:DyaK2sXnvFWkt7Y%3D 9389720
49. S Zacchigna H Oh M Wilsch-Bräuninger E Missol-Kolka J Jászai S Jansen N Tanimoto F Tonagel M Seeliger WB Huttner D Corbeil M Dewerchin S Vinckier L Moons P Carmeliet 2009 Loss of cholesterol-binding protein prominin-1/CD133 causes disk dysmorphogenesis and photoreceptor degeneration J Neurosci 29 2297 2308 10.1523/JNEUROSCI.2034-08.2009 1:CAS:528: DC%2BD1MXisV2gsrs%3D 19228982
50. Q Zhang R Haleem X Cai Z Wang 2002 Identification and characterization of a novel testosterone-regulated prominin-like gene in the rat ventral prostate Endocrinology 143 4788 4796 10.1210/en.2002-220522 1:CAS:528: DC%2BD38Xpt1eltL8%3D 12446606 (Pubitemid 35397619)