Abstract
Our knowledge of the first member of the prominin family is growing rapidly as the clinical value of prominin-1 (CD133) increases with its ever-wider use as a stem cell marker in normal and cancer tissues. Although the physiological function of this evolutionally conserved pentaspan membrane glycoprotein remains elusive, several studies have revealed new biological features regarding stem cells, cancer stem cells, and photoreceptors. The wide expression of CD133 in terminally differentiated epithelial cells, long overlooked by many authors, has attracted significant interest through the extensive investigation of human prominin-1 as a potential target for cancer therapies in various organs. Biochemically, this cholesterol-binding protein is selectively concentrated in plasma membrane protrusions, where it is associated with cholesterol-driven membrane microdomains. Clinically, mutations in the PROM1 gene are associated with various forms of retinal degeneration, which are mimicked in genetically modified mice carrying either a null allele or mutated form of prominin-1. In this introductory chapter, we attempted to review 15 years of prominin-1 study, focusing on its unique protein characteristics across species and the recent developments regarding its cell biology that may shed new light on its intriguing involvement in defining cancer-initiating cells.
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References
Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8:755–768
Baccelli I, Trumpp A (2012) The evolving concept of cancer and metastasis stem cells. J Cell Biol 198:281–293
Weigmann A, Corbeil D, Hellwig A, Huttner WB (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
Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M et al (1997) AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90:5002–5012
Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R et al (1997) A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90:5013–5021
Corbeil D, Röper K, Weigmann A, Huttner WB (1998) AC133 hematopoietic stem cell antigen – human homologue of mouse kidney prominin or distinct member of a novel protein family. Blood 91:2625–2626
Miraglia S, Godfrey W, Buck D (1998) A response to AC133 hematopoietic stem cell antigen: human homologue of mouse kidney prominin or distinct member of a novel protein family? Blood 91:4390–4391
Corbeil D, Röper K, Hellwig A, Tavian M, Miraglia S et al (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
Florek M, Haase M, Marzesco A-M, Freund D, Ehninger G et al (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
Maw MA, Corbeil D, Koch J, Hellwig A, Wilson-Wheeler JC et al (2000) A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet 9:27–34
Fargeas CA, Joester A, Missol-Kolka E, Hellwig A, Huttner WB et al (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
Jászai J, Janich P, Farkas LM, Fargeas CA, Huttner WB et al (2007) Differential expression of Prominin-1 (CD133) and Prominin-2 in major cephalic exocrine glands of adult mice. Histochem Cell Biol 128:409–419
Karbanová J, Missol-Kolka E, Fonseca AV, Lorra C, Janich P et al (2008) The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia. J Histochem Cytochem 56:977–993
Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J et al (2008) CD133 expression is not restricted to stem cells, and both CD133+ and CD133− metastatic colon cancer cells initiate tumors. J Clin Invest 118:2111–2120
Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ et al (2009) Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457:603–607
Fargeas CA, Florek M, Huttner WB, Corbeil D (2003) Characterization of prominin-2, a new member of the prominin family of pentaspan membrane glycoproteins. J Biol Chem 278:8586–8596
Yu Y, Flint A, Dvorin EL, Bischoff J (2002) AC133-2, a novel isoform of human AC133 stem cell antigen. J Biol Chem 277:20711–20716
Fargeas CA, Corbeil D, Huttner WB (2003) AC133 antigen, CD133, prominin-1, prominin-2, etc.: prominin family gene products in need of a rational nomenclature. Stem Cells 21:506–508
Fargeas CA, Fonseca AV, Huttner WB, Corbeil D (2006) Prominin-1 (CD133): from progenitor cells to human diseases. Future Lipidol 1:213–225
Corbeil D, Fargeas CA, Huttner WB (2001) Rat prominin, like its mouse and human orthologues, is a pentaspan membrane glycoprotein. Biochem Biophys Res Commun 285:939–944
McGrail M, Batz L, Noack K, Pandey S, Huang Y et al (2010) Expression of the zebrafish CD133/prominin1 genes in cellular proliferation zones in the embryonic central nervous system and sensory organs. Dev Dyn 239:1849–1857
Jászai J, Fargeas CA, Graupner S, Tanaka EM, Brand M et al (2011) Distinct and conserved prominin-1/CD133–positive retinal cell populations identified across species. PLoS One 6:e17590
Han Z, Papermaster DS (2011) Identification of three prominin homologs and characterization of their messenger RNA expression in Xenopus laevis tissues. Mol Vis 17:1381–1396
Zelhof AC, Hardy RW, Becker A, Zuker CS (2006) Transforming the architecture of compound eyes. Nature 443:696–699
Jászai J, Fargeas CA, Florek M, Huttner WB, Corbeil D (2007) Focus on molecules: prominin-1 (CD133). Exp Eye Res 85:585–586
Boivin D, Labbé D, Fontaine N, Lamy S, Beaulieu E et al (2009) The stem cell marker CD133 (prominin-1) is phosphorylated on cytoplasmic tyrosine-828 and tyrosine-852 by Src and Fyn tyrosine kinases. Biochemistry 48:3998–4007
Corbeil D, Röper K, Fargeas CA, Joester A, Huttner WB (2001) Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2:82–91
Gaboriaud C, Bissery V, Benchetrit T, Mornon JP (1987) Hydrophobic cluster analysis: an efficient new way to compare and analyse amino acid sequences. FEBS Lett 224:149–155
Fargeas CA, Huttner WB, Corbeil D (2007) Nomenclature of prominin-1 (CD133) splice variants – an update. Tissue Antigens 69:602–606
Shmelkov SV, Jun L, St Clair R, McGarrigle D, Derderian CA et al (2004) Alternative promoters regulate transcription of the gene that encodes stem cell surface protein AC133. Blood 103:2055–2061
Pleshkan VV, Vinogradova TV, Sverdlov ED (2008) Methylation of the prominin 1 TATA-less main promoters and tissue specificity of their transcript content. Biochim Biophys Acta 1779:599–605
Yi JM, Tsai HC, Glöckner SC, Lin S, Ohm JE et al (2008) Abnormal DNA methylation of CD133 in colorectal and glioblastoma tumors. Cancer Res 68:8094–8103
Tabu K, Sasai K, Kimura T, Wang L, Aoyanagi E et al (2008) Promoter hypomethylation regulates CD133 expression in human gliomas. Cell Res 18:1037–1046
Baba T, Convery PA, Matsumura N, Whitaker RS, Kondoh E et al (2009) Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene 28:209–218
Campbell EA, O’Hara L, Catalano RD, Sharkey AM, Freeman TC et al (2006) Temporal expression profiling of the uterine luminal epithelium of the pseudo-pregnant mouse suggests receptivity to the fertilized egg is associated with complex transcriptional changes. Hum Reprod 21:2495–2513
Husain SM, Shou Y, Sorrentino BP, Handgretinger R (2006) Isolation, molecular cloning and in vitro expression of rhesus monkey (Macaca mulatta) prominin-1.s1 complementary DNA encoding a potential hematopoietic stem cell antigen. Tissue Antigens 68:317–324
Corbeil D, Joester A, Fargeas CA, Jászai J, Garwood J et al (2009) Expression of distinct splice variants of the stem cell marker prominin-1 (CD133) in glial cells. Glia 57:860–874
Hoegg S, Brinkmann H, Taylor JS, Meyer A (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203
Sheng M, Sala C (2001) PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24:1–29
Huttner WB, Zimmerberg J (2001) Implications of lipid microdomains for membrane curvature, budding and fission. Curr Opin Cell Biol 13:478–484
Zhou F, Cui C, Ge Y, Chen H, Li Q et al (2010) Alpha2,3-Sialylation regulates the stability of stem cell marker CD133. J Biochem 148:273–280
Sgambato A, Puglisi MA, Errico F, Rafanelli F, Boninsegna A et al (2010) Post-translational modulation of CD133 expression during sodium butyrate-induced differentiation of HT29 human colon cancer cells: implications for its detection. J Cell Physiol 224:234–241
Mak AB, Blakely KM, Williams RA, Penttilä PA, Shukalyuk AI et al (2011) CD133 protein N-glycosylation processing contributes to cell surface recognition of the primitive cell marker AC133 epitope. J Biol Chem 286:41046–41056
Hemmoranta H, Satomaa T, Blomqvist M, Heiskanen A, Aitio O et al (2007) N-glycan structures and associated gene expression reflect the characteristic N-glycosylation pattern of human hematopoietic stem and progenitor cells. Exp Hematol 35:1279–1292
Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L et al (2010) The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 70:719–729
Lardon J, Corbeil D, Huttner WB, Ling Z, Bouwens L (2008) Stem cell marker prominin- 1/AC133 is expressed in duct cells of the adult human pancreas. Pancreas 36:e1–e6
Immervoll H, Hoem D, Steffensen OJ, Miletic H, Molven A (2011) Visualization of CD44 and CD133 in normal pancreas and pancreatic ductal adenocarcinomas: non-overlapping membrane expression in cell populations positive for both markers. J Histochem Cytochem 59:441–455
Immervoll H, Hoem D, Sakariassen PO, Steffensen OJ, Molven A (2008) Expression of the “stem cell marker” CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer 8:48
Bidlingmaier S, Zhu X, Liu B (2008) The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med 86:1025–1032
Fargeas CA, Karbanová J, Jászai J, Corbeil D (2011) CD133 and membrane microdomains: old facets for future hypotheses. World J Gastroenterol 17:4149–4152
Dubreuil V, Marzesco A-M, Corbeil D, Huttner WB, Wilsch-Bräuninger M (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
Florek M, Bauer N, Janich P, Wilsch-Bräuninger M, Fargeas CA et al (2007) 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 328:31–47
Giebel B, Corbeil D, Beckmann J, Höhn J, Freund D et al (2004) Segregation of lipid raft markers including CD133 in polarized human hematopoietic stem and progenitor cells. Blood 104:2332–2338
Fonseca AV, Freund D, Bornhäuser M, Corbeil D (2010) Polarization and migration of hematopoietic stem and progenitor cells rely on the RhoA/ROCK I pathway and an active reorganization of the microtubule network. J Biol Chem 285:31661–31671
Röper K, Corbeil D, Huttner WB (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2:582–592
Corbeil D, Marzesco A-M, Fargeas CA, Huttner WB (2010) Prominin-1, a distinct cholesterol–binding membrane protein, and the organization of the apical plasma membrane of epithelial cells. Subcell Biochem 51:399–423
Janich P, Corbeil D (2007) GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett 581:1783–1787
Gillette JM, Larochelle A, Dunbar CE, Lippincott-Schwartz J (2009) Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nat Cell Biol 11:303–305
Taïeb N, Maresca M, Guo XJ, Garmy N, Fantini J et al (2009) The first extracellular domain of the tumour stem cell marker CD133 contains an antigenic ganglioside-binding motif. Cancer Lett 278:164–173
Marzesco A-M, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K et al (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
Huttner HB, Janich P, Köhrmann M, Jászai J, Siebzehnrubl F et al (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
Huttner HB, Corbeil D, Thirmeyer C, Coras R, Köhrmann M et al (2012) Increased membrane shedding–indicated by an elevation of CD133-enriched membrane particles – into the CSF in partial epilepsy. Epilepsy Res 99:101–106
Kania G, Corbeil D, Fuchs J, Tarasov KV, Blyszczuk P et al (2005) The somatic stem cell marker prominin-1/CD133 is expressed in embryonic stem cell-derived progenitors. Stem Cells 23:791–804
Kaufman DS, Hanson ET, Lewis RL, Auerbach R, Thomson JA (2001) Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 98:10716–10721
Carpenter MK, Rosler E, Rao MS (2003) Characterization and differentiation of human embryonic stem cells. Cloning Stem Cells 5:79–88
Hoffman LM, Carpenter MK (2005) Characterization and culture of human embryonic stem cells. Nat Biotechnol 23:699–708
Shamblott MJ, Axelman J, Littlefield JW, Blumenthal PD, Huggins GR et al (2001) Human embryonic germ cell derivatives express a broad range of developmentally distinct markers and proliferate extensively in vitro. Proc Natl Acad Sci USA 98:113–118
Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R (2002) Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 99:4391–4396
Ito Y, Hamazaki TS, Ohnuma K, Tamaki K, Asashima M et al (2007) Isolation of murine hair-inducing cells using the cell surface marker prominin-1/CD133. J Invest Dermatol 127:1052–1060
Suzuki A, Sekiya S, Onishi M, Oshima N, Kiyonari H et al (2008) Flow cytometric isolation and clonal identification of self-renewing bipotent hepatic progenitor cells in adult mouse liver. Hepatology 48:1964–1978
Gashaw I, Dushaj O, Behr R, Biermann K, Brehm R et al (2007) Novel germ cell markers characterize testicular seminoma and fetal testis. Mol Hum Reprod 13:721–727
Jászai J, Fargeas CA, Haase M, Farkas LM, Huttner WB et al (2008) Robust expression of prominin-2 all along the adult male reproductive system and urinary bladder. Histochem Cell Biol 130:749–759
Han Z, Anderson DW, Papermaster DS (2012) Prominin-1 localizes to the open rims of outer segment lamellae in Xenopus laevis rod and cone photoreceptors. Invest Ophthalmol Vis Sci 53:361–373
Bauer N, Fonseca AV, Florek M, Freund D, Jászai J et al (2008) New insights into the cell biology of hematopoietic progenitors by studying prominin-1 (CD133). Cells Tissues Organs 188:127–138
Bornhäuser M, Eger L, Oelschlaegel U, Auffermann-Gretzinger S, Kiani A et al (2005) Rapid reconstitution of dendritic cells after allogeneic transplantation of CD133+ selected hematopoietic stem cells. Leukemia 19:161–165
Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E et al (2007) CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res 67:5727–5736
Coskun V, Wu H, Blanchi B, Tsao S, Kim K et al (2008) CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA 105:1026–1031
Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3:265–278
Uchida N, Buck DW, He D, Reitsma MJ, Masek M et al (2000) Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97:14720–14725
Tamaki S, Eckert K, He D, Sutton R, Doshe M et al (2002) Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J Neurosci Res 69:976–986
Schwartz PH, Bryant PJ, Fuja TJ, Su H, O’Dowd DK et al (2003) Isolation and characterization of neural progenitor cells from post-mortem human cortex. J Neurosci Res 74:838–851
Lee A, Kessler JD, Read T-A, Kaiser C, Corbeil D et al (2005) Isolation of neural stem cells from postnatal cerebellum. Nat Neurosci 8:723–729
Bussolati B, Bruno S, Grange C, Buttiglieri S, Deregibus M et al (2005) Isolation of renal progenitor cells from adult human kidney. Am J Pathol 166:545–555
Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ et al (2004) CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 117:3539–3545
Leong KG, Wang BE, Johnson L, Gao WQ (2008) Generation of a prostate from a single adult stem cell. Nature 456:804–808
Alessandri G, Pagano S, Bez A, Benetti A, Pozzi S et al (2004) Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet 364:1872–1883
Belicchi M, Pisati F, Lopa R, Porretti L, Fortunato F et al (2004) Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain. J Neurosci Res 77:475–486
Snippert HJ, van Es JH, van den Born M, Begthel H, Stange DE et al (2009) Prominin-1/CD133 marks stem cells and early progenitors in mouse intestine. Gastroenterology 136:2187–2194
Gregory CA, Prockop DJ, Spees JL (2005) Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. Exp Cell Res 306:330–335
Pozzobon M, Piccoli M, Ditadi A, Bollini S, Destro R et al (2009) Mesenchymal stromal cells can be derived from bone marrow CD133+ cells: implications for therapy. Stem Cells Dev 18:497–510
Ratajczak J, Zuba-Surma E, Klich I, Liu R, Wysoczynski M et al (2011) Hematopoietic differentiation of umbilical cord blood-derived very small embryonic/epiblast-like stem cells. Leukemia 25:1278–1285
Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ et al (2000) Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95:952–958
Asahara T, Kawamoto A (2004) Endothelial progenitor cells for postnatal vasculogenesis. Am J Physiol Cell Physiol 287:C572–C579
Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K et al (2000) In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95:3106–3112
Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C et al (2003) Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361:45–46
Sussman LK, Upalakalin JN, Roberts MJ, Kocher O, Benjamin LE (2003) Blood markers for vasculogenesis increase with tumor progression in patients with breast carcinoma. Cancer Biol Ther 2:255–256
Lin EH, Hassan M, Li Y, Zhao H, Nooka A et al (2007) Elevated circulating endothelial progenitor marker CD133 messenger RNA levels predict colon cancer recurrence. Cancer 110:534–542
Hilbe W, Dirnhofer S, Oberwasserlechner F, Schmid T, Gunsilius E et al (2004) CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J Clin Pathol 57:965–969
Dome B, Timar J, Dobos J, Meszaros L, Raso E et al (2006) Identification and clinical significance of circulating endothelial progenitor cells in human non-small cell lung cancer. Cancer Res 66:7341–7347
Mehra N, Penning M, Maas J, Beerepoot LV, van Daal N et al (2006) Progenitor marker CD133 mRNA is elevated in peripheral blood of cancer patients with bone metastases. Clin Cancer Res 12:4859–4866
Powell TM, Paul JD, Hill JM, Thompson M, Benjamin M et al (2005) Granulocyte colony-stimulating factor mobilizes functional endothelial progenitor cells in patients with coronary artery disease. Arterioscler Thromb Vasc Biol 25:296–301
Schatteman G (2005) Are circulating CD133+ cells biomarkers of vascular disease? Arterioscler Thromb Vasc Biol 25:270–271
Case J, Mead LE, Bessler WK, Prater D, White HA et al (2007) Human CD34 + AC133 + VEGFR-2+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol 35:1109–1118
Timmermans F, Van Hauwermeiren F, De Smedt M, Raedt R, Plasschaert F et al (2007) Endothelial outgrowth cells are not derived from CD133+ cells or CD45+ hematopoietic precursors. Arterioscler Thromb Vasc Biol 27:1572–1579
Singh S, Dirks PB (2007) Brain tumor stem cells: identification and concepts. Neurosurg Clin N Am 18:31–38
Baersch G, Baumann M, Ritter J, Jurgens H, Vormoor J (1999) Expression of AC133 and CD117 on candidate normal stem cell populations in childhood B-cell precursor acute lymphoblastic leukaemia. Br J Haematol 107:572–580
Buhring HJ, Seiffert M, Marxer A, Weiss B, Faul C et al (1999) 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 94:832–833
Horn PA, Tesch H, Staib P, Kube D, Diehl V et al (1999) Expression of AC133, a novel hematopoietic precursor antigen, on acute myeloid leukemia cells. Blood 93:1435–1437
Cox CV, Diamanti P, Evely RS, Kearns PR, Blair A (2009) Expression of CD133 on leukemia initiating cells in childhood ALL. Blood 113:3287–3296
Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M et al (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445:111–115
O’Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445:106–110
Dalerba P, Dylla SJ, Park IK, Liu R, Wang X et al (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104:10158–10163
Chu P, Clanton DJ, Snipas TS, Lee J, Mitchell E et al (2009) Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int J Cancer 124:1312–1321
Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH et al (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 100:15178–15183
Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C et al (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828
Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J et al (2004) Identification of human brain tumour initiating cells. Nature 432:396–401
Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C et al (2006) Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 54:850–860
Liu G, Yuan X, Zeng Z, Tunici P, Ng H et al (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67
Bruno S, Bussolati B, Grange C, Collino F, Graziano ME et al (2006) CD133+ renal progenitor cells contribute to tumor angiogenesis. Am J Pathol 169:2223–2235
Rountree CB, Ding W, He L, Stiles B (2009) Expansion of CD133 expressing liver cancer stem cells in liver specific PTEN deleted mice. Stem Cells 27:290–299
Ding W, Mouzaki M, You H, Laird JC, Mato J et al (2009) CD133(+) liver cancer stem cells from methionine adenosyl transferase 1A-deficient mice demonstrate resistance to transforming growth factor (TGF)-beta-induced apoptosis. Hepatology 49:1277–1286
Zhu Z, Hao X, Yan M, Yao M, Ge C et al (2009) Cancer stem/progenitor cells are highly enriched in CD133(+)CD44(+) population in hepatocellular carcinoma. Int J Cancer 126:2067–2078
Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M et al (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15:504–514
Chen YC, Hsu HS, Chen YW, Tsai TH, How CK et al (2008) Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One 3:e2637
Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW et al (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1:313–323
Olempska M, Eisenach PA, Ammerpohl O, Ungefroren H, Fandrich F et al (2007) Detection of tumor stem cell markers in pancreatic carcinoma cell lines. Hepatobiliary Pancreat Dis Int 6:92–97
Curley MD, Therrien VA, Cummings CL, Sergent PA, Koulouris CR et al (2009) CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 27:2875–2883
Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65:10946–10951
Miki J, Furusato B, Li H, Gu Y, Takahashi H et al (2007) 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 67:3153–3161
Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM et al (2005) ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65:4320–4333
Klein WM, Wu BP, Zhao S, Wu H, Klein-Szanto AJ et al (2007) Increased expression of stem cell markers in malignant melanoma. Mod Pathol 20:102–107
Bongiorno MR, Doukaki S, Malleo F, Aricò M (2008) Identification of progenitor cancer stem cell in lentigo maligna melanoma. Dermatol Ther 21:S1–S5
Gedye C, Quirk J, Browning J, Svobodová S, John T et al (2009) Cancer/testis antigens can be immunological targets in clonogenic CD133(+) melanoma cells. Cancer Immunol Immunother 58:1635–1646
Zito G, Richiusa P, Bommarito A, Carissimi E, Russo L et al (2008) In vitro identification and characterization of CD133(pos) cancer stem-like cells in anaplastic thyroid carcinoma cell lines. PLoS One 3:e3544
Veselska R, Hermanova M, Loja T, Chlapek P, Zambo I et al (2008) Nestin expression in osteosarcomas and derivation of nestin/CD133 positive osteosarcoma cell lines. BMC Cancer 8:300
Tirino V, Desiderio V, d’Aquino R, De Francesco F, Pirozzi G et al (2008) Detection and characterization of CD133+ cancer stem cells in human solid tumours. PLoS One 3:e3469
Yin S, Li J, Hu C, Chen X, Yao M et al (2007) CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 120:1444–1450
Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T et al (2006) Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 351:820–824
Rappa G, Fodstad O, Lorico A (2008) The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma. Stem Cells 26:3008–3017
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q et al (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:755–760
Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH et al (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9:157–173
Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM et al (2008) Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 14:123–129
Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z et al (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843–7848
Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C et al (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11:69–82
Grosse-Gehling P, Fargeas CA, Dittfeld C, Garbe Y, Alison MR et al (2012) CD133 as a biomarker for putative cancer stem cells in solid tumours: limitations, problems and challenges. J Pathol (2012)
Zhang Q, Zulfiqar F, Xiao X, Riazuddin SA, Ahmad Z et al (2007) Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene. Hum Genet 122:293–299
Yang Z, Chen Y, Lillo C, Chien J, Yu Z et al (2008) Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice. J Clin Invest 118:2908–2916
Pras E, Abu A, Rotenstreich Y, Avni I, Reish O et al (2009) Cone-rod dystrophy and a frameshift mutation in the PROM1 gene. Mol Vis 15:1709–1716
Permanyer J, Navarro R, Friedman J, Pomares E, Castro-Navarro J et al (2010) Autosomal recessive retinitis pigmentosa with early macular affectation caused by premature truncation in PROM1. Invest Ophthalmol Vis Sci 51:2656–2663
Littink KW, Koenekoop RK, van den Born LI, Collin RW, Moruz L et al (2010) Homozygosity mapping in patients with cone-rod dystrophy: novel mutations and clinical characterizations. Invest Ophthalmol Vis Sci 51:5943–5951
Zacchigna S, Oh H, Wilsch-Bräuninger M, Missol-Kolka E, Jászai J et al (2009) Loss of the cholesterol-binding protein prominin-1/CD133 causes disk dysmorphogenesis and photoreceptor degeneration. J Neurosci 29:2297–2308
Husain N, Pellikka M, Hong H, Klimentova T, Choe KM et al (2006) The agrin/perlecan-related protein eyes shut is essential for epithelial lumen formation in the Drosophila retina. Dev Cell 11:483–493
Kosodo Y, Röper K, Haubensak W, Marzesco A-M, Corbeil D et al (2004) Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J 23:2314–2324
Fonseca AV, Bauer N, Corbeil D (2008) The stem cell marker CD133 meets the endosomal compartment-new insights into the cell division of hematopoietic stem cells. Blood Cells Mol Dis 41:194–195
Lathia JD, Hitomi M, Gallagher J, Gadani SP, Adkins J et al (2011) Distribution of CD133 reveals glioma stem cells self-renew through symmetric and asymmetric cell divisions. Cell Death Dis 2:e200
Bauer N, Wilsch-Bräuninger M, Karbanová J, Fonseca AV, Strauss D et al (2011) Hematopoietic stem cell differentiation promotes the release of prominin-1/CD133–containing membrane vesicles – a role of the endocytic-exocytic pathway. EMBO Mol Med 3:398–409
Ettinger AW, Wilsch-Bräuninger M, Marzesco AM, Bickle M, Lohmann A et al (2011) Proliferating versus differentiating stem and cancer cells exhibit distinct midbody-release behaviour. Nat Commun 2:503
Acknowledgements
We warmly thank all the collaborators for their major contributions to the prominin field during the last 15 years. We are indebted to Wieland B. Huttner, whose laboratory discovered murine prominin-1; David W. Buck, whose laboratory discovered human prominin-1; Marion A. Maw, who described the first mutation in the PROM1 gene; Anne-Marie Marzesco, who noticed prominin-1-containing membrane vesicles; and Peter Carmeliet, whose laboratory generated prominin-1 knockout mice. We thank Andrea Hellwig and Michaela Wilsch-Bräuninger for the excellent electron microscopy demonstrating the preference of prominin-1 for plasma membrane protrusions. The corresponding author (D.C.) wants to express here his particular gratitude to W.B. Huttner for his constant support. Deutsche Forschungsgemeinschaft (DFG) supported D.C. (SFB655 B3; TRR83 #6 and CO298/5-1). Intramural funds of the Medical Faculty of Technische Universität Dresden and DFG supported J.J. (MeDDrive38 grants and CO298/5-1, respectively).
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Corbeil, D., Karbanová, J., Fargeas, C.A., Jászai, J. (2013). Prominin-1 (CD133): Molecular and Cellular Features Across Species. In: Corbeil, D. (eds) Prominin-1 (CD133): New Insights on Stem & Cancer Stem Cell Biology. Advances in Experimental Medicine and Biology, vol 777. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5894-4_1
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