Prominin-1 (CD133) is not restricted to stem cells located in the basal compartment of murine and human prostate

Prostate

Volumn 71, Issue 3, 2011, Pages 254-267

  Missol Kolka, Ewa ^a,b   Karbanová, Jana ^b,c   Janich, Peggy ^b   Haase, Michael ^b   Fargeas, Christine A ^b   Huttner, Wieland B ^a   Corbeil, Denis ^b  

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

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c CHARLES UNIVERSITY   (Czech Republic)

Author keywords

CD133; epithelium; proliferative inflammatory atrophy; prominin 1; prostate cancer; stem cells

Indexed keywords

CD133 ANTIGEN; EPITOPE;

ADULT; AGED; ANIMAL TISSUE; ARTICLE; BLOTTING; CANCER TISSUE; CELL COMPARTMENTALIZATION; DOWN REGULATION; EPITHELIUM CELL; GLYCOSYLATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; SEMINAL VESICLE; UPREGULATION; VAS DEFERENS;

AGED; ANIMALS; ANTIGENS, CD; CACO-2 CELLS; GLYCOPROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; PEPTIDES; PROSTATE; PROSTATIC NEOPLASMS; STEM CELLS;

EID: 78951486493     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.21239     Document Type: Article

References (77)

1. Fargeas CA, Fonseca AV, Huttner WB, Corbeil D,. Prominin-1 (CD133): From progenitor cells to human diseases. Future Lipid 2006; 1: 213-225.
2. Bauer N, Fonseca AV, Florek M, Freund D, Jászai J, Bornhäuser M, Fargeas CA, Corbeil D,. New insights into the cell biology of hematopoietic progenitors by studying prominin-1 (CD133). Cells Tissues Organs 2008; 188: 127-138.
3. Weigmann A, Corbeil D, Hellwig A, Huttner WB,. 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 1997; 94: 12425-12430.
4. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW,. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997; 90: 5002-5012.
5. Corbeil D, Röper K, Hellwig A, Tavian M, Miraglia S, Watt SM, Simmons PJ, Peault B, Buck DW, Huttner WB,. 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.
6. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL,. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 2000; 97: 14720-14725.
7. Alessandri G, Pagano S, Bez A, Benetti A, Pozzi S, Iannolo G, Baronio M, Invernici G, Caruso A, Muneretto C, Bisleri G, Parati E,. Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet 2004; 364: 1872-1883.
8. Bussolati B, Bruno S, Grange C, Buttiglieri S, Deregibus M, Cantino D, Camussi G,. Isolation of renal progenitor cells from adult human kidney. Am J Pathol 2005; 166: 545-555.
9. Yu Y, Flint A, Dvorin EL, Bischoff J,. AC133-2, a novel isoform of human AC133 stem cell antigen. J Biol Chem 2002; 277: 20711-20716.
10. Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, Poppleton H, Zakharenko S, Ellison DW, Gilbertson RJ,. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 2009; 457: 603-607.
11. Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT,. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 2004; 117: 3539-3545.
12. Leong KG, Wang BE, Johnson L, Gao W-Q,. Generation of a prostate from a single adult stem cell. Nature 2008; 456: 804-808.
13. Bhatia M,. AC133 expression in human stem cells. Leukemia 2001; 15: 1685-1688.
14. Waller CF, Martens UM, Lange W,. Philadelphia chromosome-positive cells are equally distributed in AC133+ and AC133- fractions of CD34+ peripheral blood progenitor cells from patients with CML. Leukemia 1999; 13: 1466-1467.
15. Baersch G, Baumann M, Ritter J, Jurgens H, Vormoor J,. Expression of AC133 and CD117 on candidate normal stem cell populations in childhood B-cell precursor acute lymphoblastic leukaemia. Br J Haematol 1999; 107: 572-580.
16. Buhring HJ, Seiffert M, Marxer A, Weiss B, Faul C, Kanz L, Brugger W,. AC133 antigen expression is not restricted to acute myeloid leukemia blasts but is also found on acute lymphoid leukemia blasts and on a subset of CD34+ B-cell precursors. Blood 1999; 94: 832-833.
17. Green CL, Loken M, Buck D, Deeg HJ,. Discordant expression of AC133 and AC141 in patients with myelodysplastic syndrome (MDS) and acute myelogeneous leukemia (AML). Leukemia 2000; 14: 770-772.
18. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum H,. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003; 100: 15178-15183.
19. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB,. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828.
20. Florek M, Haase M, Marzesco A-M, Freund D, Ehninger G, Huttner WB, Corbeil D,. 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.
21. Bruno S, Bussolati B, Grange C, Collino F, Graziano ME, Ferrando U, Camussi G,. CD133+ renal progenitor cells contribute to tumor angiogenesis. Am J Pathol 2006; 169: 2223-2235.
22. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ,. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65: 10946-10951.
23. Miki J, Furusato B, Li H, Gu Y, Takahashi H, Egawa S, Sesterhenn IA, McLeod DG, Srivastava S, Rhim JS,. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res 2007; 67: 3153-3161.
24. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H,. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 2006; 351: 820-824.
25. Wei C, Guomin W, Yujun L, Ruizhe Q,. Cancer stem-like cells in human prostate carcinoma cells DU145: The seeds of the cell line? Cancer Biol Ther 2007; 6: 763-768.
26. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, Jiang G, Ge C, Xie H, Wan D, Yang S, Zheng S, Gu J,. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 2007; 120: 1444-1450.
27. Zito G, Richiusa P, Bommarito A, Carissimi E, Russo L, Coppola A, Zerilli M, Rodolico V, Criscimanna A, Amato M, Pizzolanti G, Galluzzo A, Giordano C,. In vitro identification and characterization of CD133(pos) cancer stem-like cells in anaplastic thyroid carcinoma cell lines. PLoS One 2008; 3: e3544.
28. Veselska R, Hermanova M, Loja T, Chlapek P, Zambo I, Vesely K, Zitterbart K, Sterba J,. Nestin expression in osteosarcomas and derivation of nestin/CD133 positive osteosarcoma cell lines. BCM Cancer 2008; 8: 300.
29. Tirino V, Desiderio V, d'Aquino R, De Francesco F, Pirozzi G, Graziano A, Galderisi U, Cavaliere C, De Rosa A, Papaccio G, Giordano A,. Detection and characterization of CD133+ cancer stem cells in human solid tumours. PLoS One 2008; 3: e3469.
30. Goodyear SM, Amatangelo MD, Stearns ME,. Dysplasia of human prostate CD133(hi) sub-population in NOD-SCIDS is blocked by c-myc anti-sense. Prostate 2009; 69: 689-698.
31. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN,. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 755-760.
32. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS,. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5: 67.
33. Zhu Z, Hao X, Yan M, Yao M, Ge C, Gu J, Li J,. Cancer stem/progenitor cells are highly enriched in CD133(+)CD44(+) population in hepatocellular carcinoma. Int J Cancer 2010; 126: 2067-2078.
34. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB,. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
35. O'Brien CA, Pollett A, Gallinger S, Dick JE,. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007; 445: 106-110.
36. Vander Griend DJ, Karthaus WL, Dalrymple S, Meeker A, De Marzo AM, Isaacs JT,. The role of CD133 in normal human prostate stem cells and malignant cancer-initiating cells. Cancer Res 2008; 68: 9703-9711.
37. Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, Buck DW,. A novel five-transmembrane hematopoietic stem cell antigen: Isolation, characterization, and molecular cloning. Blood 1997; 90: 5013-5021.
38. Immervoll H, Hoem D, Sakariassen PO, Steffensen OJ, Molven A,. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer 2008; 8: 48.
39. Bidlingmaier S, Zhu X, Liu B,. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med 2008; 86: 1025-1032.
40. Fargeas CA, Joester A, Missol-Kolka E, Hellwig A, Huttner WB, Corbeil D,. Identification of novel prominin-1/CD133 splice variants with alternative C-termini and their expression in epididymis and testis. J Cell Sci 2004; 117: 4301-4311.
41. Fargeas CA, Huttner WB, Corbeil D,. Nomenclature of prominin-1 (CD133) splice variantsâAn update. Tissue Antig 2007; 69: 602-606.
42. Lardon J, Corbeil D, Huttner WB, Ling Z, Bouwens L,. Stem cell marker prominin 1/AC133 is expressed in duct cells of the adult human pancreas. Pancreas 2008; 36: e1-e6.
43. Karbanová J, Missol-Kolka E, Fonseca AV, Lorra C, Janich P, Hollerová H, Jászai J, Ehrmann J, Kolár Z, Liebers C, Arl S, Subrtová D, Freund D, Mokry J, Huttner WB, Corbeil D,. The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia. J Histochem Cytochem 2008; 56: 977-993.
44. Corbeil D, Fargeas CA, Huttner WB,. Rat prominin, like its mouse and human orthologues, is a pentaspan membrane glycoprotein. Biochem Biophys Res Commun 2001; 285: 939-944.
45. Jászai J, Janich P, Farkas LM, Fargeas CA, Huttner WB, Corbeil D,. Differential expression of Prominin-1 (CD133) and Prominin-2 in major cephalic exocrine glands of adult mice. Histochem Cell Biol 2007; 128: 409-419.
46. Corbeil D, Röper K, Fargeas CA, Joester A, Huttner WB,. Prominin: A story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2001; 2: 82-91.
47. Röper K, Corbeil D, Huttner WB,. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2000; 2: 582-592.
48. Marzesco A-M, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner WB,. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 2005; 118: 2849-2858.
49. Fargeas CA, Corbeil D, Huttner WB,. AC133 antigen, CD133, prominin-1, prominin-2, etc.: Prominin family gene products in need of a rational nomenclature. Stem Cells 2003; 21: 506-508.
50. Huttner HB, Janich P, Köhrmann M, Jászai J, Siebzehnrubl F, Blümcke I, Suttorp M, Gahr M, Kuhnt D, Nimsky C, Krex D, Schackert G, Löwenbrück K, Reichmann H, Jüttler E, Hacke W, Schellinger PD, Schwab S, Wilsch-Bräuninger M, Marzesco A-M, Corbeil D,. The stem cell marker prominin-1/CD133 on membrane particles in human cerebrospinal fluid offers novel approaches for studying CNS disease. Stem Cells 2008; 26: 698-705.
51. Marzesco A-M, Wilsch-Bräuninger M, Dubreuil V, Janich P, Langenfeld K, Thiele C, Huttner WB, Corbeil D,. Release of extracellular membrane vesicles from microvilli of epithelial cells is enhanced by depleting membrane cholesterol. FEBS Lett 2009; 583: 897-902.
52. Maw MA, Corbeil D, Koch J, Hellwig A, Wilson-Wheeler JC, Bridges RJ, Kumaramanickavel G, John S, Nancarrow D, Röper K, Weigmann A, Huttner WB, Denton MJ,. A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet 2000; 9: 27-34.
53. Corbeil D, Röper K, Hannah MJ, Hellwig A, Huttner WB,. Selective localization of the polytopic membrane protein prominin in microvilli of epithelial cellsâA combination of apical sorting and retention in plasma membrane protrusions. J Cell Sci 1999; 112: 1023-1033.
54. Corbeil D, Marzesco A-M, Fargeas CA, Huttner WB,. Prominin-1, a distinct cholesterol-binding membrane protein, and the organization of the apical plasma membrane of epithelial cells In:, Harris JR, editor. Cholesterol binding and cholesterol transport proteins: Structure and function in health and disease, Vol. 51: Subcellular biochemistry. Heidelberg: Springer; 2010. pp 399-423.
55. Wahlqvist R, Dahl E, Tveter KJ,. Scanning electron microscopy of the accessory sex glands of the adult male rat. Scan Microsc 1996; 10: 1143-1154.
56. Schroter S, Derr P, Conradt HS, Nimtz M, Hale G, Kirchhoff C,. Male-specific modification of human CD52. J Biol Chem 1999; 274: 29862-29873.
57. Zhang Q, Zulfiqar F, Xiao X, Riazuddin SA, Ahmad Z, Caruso R, MacDonald I, Sieving P, Riazuddin S, Hejtmancik JF,. Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene. Hum Genet 2007; 122: 293-299.
58. Yang Z, Chen Y, Lillo C, Chien J, Yu Z, Michaelides M, Klein M, Howes KA, Li Y, Kaminoh Y, Chen H, Zhao C, Chen Y, Al-Sheikh YT, Karan G, Corbeil D, Escher P, Kamaya S, Li C, Johnson S, Frederick JM, Zhao Y, Wang C, Cameron DJ, Huttner WB, Schorderet DF, Munier FL, Moore AT, Birch DG, Baehr W, Hunt DM, Williams DS, Zhang K,. Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice. J Clin Invest 2008; 118: 2908-2916.
59. Zacchigna S, Oh H, Wilsch-Bräuninger M, Missol-Kolka E, Jászai J, Jansen S, Tanimoto N, Tonagel F, Seeliger M, Huttner WB, Corbeil D, Dewerchin M, Vinckier S, Moons L, Carmeliet P,. Loss of the cholesterol-binding protein prominin-1/CD133 causes disk dysmorphogenesis and photoreceptor degeneration. J Neurosci 2009; 29: 2297-2308.
60. Roy-Burman P, Wu H, Powell WC, Hagenkord J, Cohen MB,. Genetically defined mouse models that mimic natural aspects of human prostate cancer development. Endocr Relat Cancer 2004; 11: 225-254.
61. Marker PC, Donjacour AA, Dahiya R, Cunha GR,. Hormonal, cellular, and molecular control of prostatic development. Dev Biol 2003; 253: 165-174.
62. Jászai J, Fargeas CA, Haase M, Farkas LM, Huttner WB, Corbeil D,. Robust expression of Prominin-2 all along the adult male reproductive system and urinary bladder. Histochem Cell Biol 2008; 130: 749-759.
63. Zhang Q, Haleem R, Cai X, Wang Z,. Identification and characterization of a novel testosterone-regulated prominin-like gene in the rat ventral prostate. Endocrinology 2002; 143: 4788-4796.
64. Shepherd CJ, Rizzo S, Ledaki I, Davies M, Brewer D, Attard G, de Bono J, Hudson DL,. Expression profiling of CD133+ and CD133- epithelial cells from human prostate. Prostate 2008; 68: 1007-1024.
65. Wang X, Kruithof-de Julio M, Economides KD, Walker D, Yu H, Halili MV, Hu YP, Price SM, Abate-Shen C, Shen MM,. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 2009; 461: 495-500.
66. De Marzo AM, Nelson WG, Isaacs WB, Epstein JI,. Pathological and molecular aspects of prostate cancer. Lancet 2003; 361: 955-964.
67. Humphrey PA,. Diagnosis of adenocarcinoma in prostate needle biopsy tissue. J Clin Pathol 2007; 60: 35-42.
68. De Marzo AM, Marchi VL, Epstein JI, Nelson WG,. Proliferative inflammatory atrophy of the prostate: Implications for prostatic carcinogenesis. Am J Pathol 1999; 155: 1985-1992.
69. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Grönberg H, Drake CG, Nakai Y, Isaacs WB, Nelson WG,. Inflammation in prostate carcinogenesis. Nat Rev Cancer 2007; 7: 1378-1384.
70. Ceder JA, Jansson L, Ehrnström RA, Rönnstrand L, Abrahamsson PA,. The characterization of epithelial and stromal subsets of candidate stem/progenitor cells in the human adult prostate. Eur Urol 2008; 53: 524-532.
71. Shmelkov SV, Jun L, St Clair R, McGarrigle D, Derderian CA, Usenko JK, Costa C, Zhang F, Guo X, Rafii S,. Alternative promoters regulate transcription of the gene that encodes stem cell surface protein AC133. Blood 2004; 103: 2055-2061.
72. Maitland NJ, Collins AT,. Prostate cancer stem cells: A new target for therapy. J Clin Oncol 2008; 26: 2862-2870.
73. Florek M, Bauer N, Janich P, Wilsch-Bräuninger M, Fargeas CA, Marzesco A-M, Ehninger G, Thiede C, Huttner WB, Corbeil D,. Prominin-2 is a cholesterol-binding protein associated with apical and basolateral plasmalemmal protrusions in polarized epithelial cells and released into the urine. Cell Tissue Res 2007; 328: 31-47.
74. Dubreuil V, Marzesco A-M, Corbeil D, Huttner WB, Wilsch-Bräuninger M,. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J Cell Biol 2007; 176: 483-495.
75. Ronquist G, Brody I,. The prostasome: Its secretion and function in man. Biochim Biophys Acta 1985; 822: 203-218.
76. Nilsson BO, Jin M, Ronquist G,. Immunolocalization of prostasomes in the human prostate. Ups J Med Sci 1996; 101: 149-157.
77. Fonseca AV, Bauer N, Corbeil D,. The stem cell marker CD133 meets the endosomal compartmentâNew insights into the cell division of hematopoietic stem cells. Blood Cells Mol Dis 2008; 41: 194-195.