The stem cell marker prominin-1/CD133 interacts with vascular endothelial growth factor and potentiates its action

Angiogenesis

Volumn 16, Issue 2, 2013, Pages 405-416

  Adini, Avner ^a   Adini, Irit ^a   Ghosh, Kaustabh ^b   Benny, Ofra ^a   Pravda, Elke ^a   Hu, Ron ^a   Luyindula, Dema ^a   D'Amato, Robert J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b University of California Riverside   (United States)

Author keywords

Apoptosis melanoma; CD133; Prominin 1; Vascular endothelial growth factor

Indexed keywords

CD133 ANTIGEN; PROTEIN BCL 2; VASCULOTROPIN; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; PROTEIN BINDING; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GROWTH; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE SILENCING; GROWTH RATE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MELANOMA CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; CELL CULTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MELANOMA; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANTIGENS, CD; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCOPROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MELANOMA; PEPTIDES; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84879502917     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-012-9323-8     Document Type: Article

References (50)

1. Corbeil D, Roper 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 (Pubitemid 28155545)
2. Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, Buck DW (1997) A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90:5013-5021 (Pubitemid 28007218)
3. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW (1997) AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90:5002-5012 (Pubitemid 28007217)
4. 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 U S A 94:12425-12430 (Pubitemid 27492544)
5. 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
6. Corbeil D, Roper K, Fargeas CA, Joester A, Huttner WB (2001) Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2:82-91 (Pubitemid 32219860)
7. Huttner HB, Janich P, Kohrmann M, Jaszai J, Siebzehnrubl F, Blumcke I, Suttorp M, Gahr M, Kuhnt D, Nimsky C, Krex D, Schackert G, Lowenbruck K, Reichmann H, Juttler E, Hacke W, Schellinger PD, Schwab S, Wilsch-Brauninger M, Marzesco AM, Corbeil D (2007) The Stem Cell Marker Prominin-1/CD133 On Membrane Particles In Human Cerebrospinal Fluid Offers Novel Approaches For Studying CNS Disease. Stem Cells 26(3):698-705
8. Jaszai J, Fargeas CA, Florek M, Huttner WB, Corbeil D (2006) Focus on Molecules: Prominin-1 (CD133). Exp Eye Res 85(5):585-586 (Pubitemid 350001359)
9. Marzesco AM, Janich P, Wilsch-Brauninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner WB (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 (Pubitemid 41136362)
10. Lee A, Kessler JD, Read TA, Kaiser C, Corbeil D, Huttner WB, Johnson JE, Wechsler-Reya RJ (2005) Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 8:723-729 (Pubitemid 43085837)
11. Missol-Kolka E, Karbanova J, Janich P, Haase M, Fargeas CA, Huttner WB, Corbeil D (2011) Prominin-1 (CD133) is not restricted to stem cells located in the basal compartment of murine and human prostate. Prostate 71, 254-267
12. Bauer N, Fonseca AV, Florek M, Freund D, Jaszai J, Bornhauser M, Fargeas CA, Corbeil D (2008) New insights into the cell biology of hematopoietic progenitors by studying prominin-1 (CD133). Cells Tissues Organs 188:127-138 (Pubitemid 351962236)
13. Shmelkov SV, Jun L, St Clair R, McGarrigle D, Derderian CA, Usenko JK, Costa C, Zhang F, Guo X, Rafii S (2004) Alternative promoters regulate transcription of the gene that encodes stem cell surface protein AC133. Blood 103:2055-2061 (Pubitemid 38326220)
14. Ria R, Piccoli C, Cirulli T, Falzetti F, Mangialardi G, Guidolin D, Tabilio A, Di Renzo N, Guarini A, Ribatti D, Dammacco F, Vacca A (2008) Endothelial differentiation of hematopoietic stem and progenitor cells from patients with multiple myeloma. Clin Cancer Res 14:1678-1685 (Pubitemid 351469451)
15. Toren A, Bielorai B, Jacob-Hirsch J, Fisher T, Kreiser D, Moran O, Zeligson S, Givol D, Yitzhaky A, Itskovitz-Eldor J, Kventsel I, Rosenthal E, Amariglio N, Rechavi G (2005) CD133-positive hematopoietic stem cell "stemness" genes contain many genes mutated or abnormally expressed in leukemia. Stem Cells 23:1142-1153 (Pubitemid 41377730)
16. Lee ST, Jang JH, Min YH, Hahn JS, Ko YW (2001) AC133 antigen as a prognostic factor in acute leukemia. Leuk Res 25:757-767 (Pubitemid 32727978)
17. Isidori A, Motta MR, Tani M, Terragna C, Zinzani P, Curti A, Rizzi S, Taioli S, Giudice V, D'Addio A, Gugliotta G, Conte R, Baccarani M, Lemoli RM (2007) Positive selection and transplantation of autologous highly purified CD133(+) stem cells in resistant/relapsed chronic lymphocytic leukemia patients results in rapid hematopoietic reconstitution without an adequate leukemic cell purging. Biol Blood Marrow Transplant 13:1224-1232 (Pubitemid 47413021)
18. Crescenzi B, Chase A, Starza RL, Beacci D, Rosti V, Galli A, Specchia G, Martelli MF, Vandenberghe P, Cools J, Jones AV, Cross NC, Marynen P, Mecucci C (2007) FIP1L1-PDGFRA in chronic eosinophilic leukemia and BCR-ABL1 in chronic myeloid leukemia affect different leukemic cells. Leukemia 21:397-402
19. Lazaridou A, Miraxtsi C, Tokmaktsis A, Hatjiharissi E, Christakis J (2000) Detection of genetic markers on different populations of hematopoietic progenitor cells in B-cell chronic lymphocytic leukemia. Blood 95:3634-3635 (Pubitemid 30428504)
20. Green CL, Loken M, Buck D, Deeg HJ (2000) Discordant expression of AC133 and AC141 in patients with myelodysplastic syndrome (MDS) and acute myelogeneous leukemia (AML). Leukemia 14:770-772 (Pubitemid 30195474)
21. Feller N, Kelder A, Westra G, Ossenkoppele GJ, Schuurhuis GJ (2008) Positive selection for CD90 as a purging option in acute myeloid leukemia stem cell transplants. Cytometry B Clin Cytom 74:9-16
22. Seigel GM, Hackam AS, Ganguly A, Mandell LM, Gonzalez-Fernandez F (2007) Human embryonic and neuronal stem cell markers in retinoblastoma. Mol Vis 13:823-832 (Pubitemid 46908324)
23. Zhong X, Li Y, Peng F, Huang B, Lin J, Zhang W, Zheng J, Jiang R, Song G, Ge J (2007) Identification of tumorigenic retinal stem-like cells in human solid retinoblastomas. Int J Cancer 121:2125-2131 (Pubitemid 47585590)
24. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, Hamou MF, de Tribolet N, Regli L, Wick W, Kouwenhoven MC, Hainfellner JA, Heppner FL, Dietrich PY, Zimmer Y, Cairncross JG, Janzer RC, Domany E, Delorenzi M, Stupp R, Hegi ME (2008) Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 26:3015-3024
25. Huttner HB, Janich P, Kohrmann M, Jaszai J, Siebzehnrubl F, Blumcke I, Suttorp M, Gahr M, Kuhnt D, Nimsky C, Krex D, Schackert G, Lowenbruck K, Reichmann H, Juttler E, Hacke W, Schellinger PD, Schwab S, Wilsch-Brauninger M, Marzesco AM, Corbeil D (2008) The stem cell marker prominin-1/CD133 on membrane particles in human cerebrospinal fluid offers novel approaches for studying central nervous system disease. Stem Cells 26:698-705
26. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821-5828 (Pubitemid 37187480)
27. 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 (2007) CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 120:1444-1450 (Pubitemid 46355378)
28. Zabierowski SE, Herlyn M (2008) Melanoma stem cells: the dark seed of melanoma. J Clin Oncol 26:2890-2894
29. Bruno S, Bussolati B, Grange C, Collino F, Graziano ME, Ferrando U, Camussi G (2006) CD133 + renal progenitor cells contribute to tumor angiogenesis. Am J Pathol 169:2223-2235 (Pubitemid 351181980)
30. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H (2006) Characterization of CD133 + hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 351:820-824 (Pubitemid 44715858)
31. Florek M, Haase M, Marzesco AM, Freund D, Ehninger G, Huttner WB, Corbeil D (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 (Pubitemid 40104635)
32. Kleinman ME, Ambati J (2008) Fifty years later: the disk goes to the prom. J Clin Invest 118:2681-2684
33. 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 (2008) Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice. J Clin Invest 118:2908-2916
34. Zhang Q, Zulfiqar F, Xiao X, Riazuddin SA, Ahmad Z, Caruso R, MacDonald I, Sieving P, Riazuddin S, Hejtmancik JF (2007) Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene. Hum Genet 122:293-299 (Pubitemid 47616537)
35. Maw MA, Corbeil D, Koch J, Hellwig A, Wilson-Wheeler JC, Bridges RJ, Kumaramanickavel G, John S, Nancarrow D, Roper K, Weigmann A, Huttner WB, Denton MJ (2000) A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet 9:27-34 (Pubitemid 30145285)
36. Pidgeon GP, Barr MP, Harmey JH, Foley DA, Bouchier-Hayes DJ (2001) Vascular endothelial growth factor (VEGF) upregulates BCL-2 and inhibits apoptosis in human and murine mammary adenocarcinoma cells. Br J Cancer 85:273-278 (Pubitemid 32695751)
37. Fernandez A, Udagawa T, Schwesinger C, Beecken W, Achilles-Gerte E, McDonnell T, D'Amato R (2001) Angiogenic potential of prostate carcinoma cells overexpressing bcl-2. J Natl Cancer Inst 93:208-213 (Pubitemid 32166491)
38. Potgens AJ, Lubsen NH, van Altena MC, Vermeulen R, Bakker A, Schoenmakers JG, Ruiter DJ, de Waal RM (1994) Covalent dimerization of vascular permeability factor/vascular endothelial growth factor is essential for its biological activity. Evidence from Cys to Ser mutations. J Biol Chem 269:32879-32885
39. Melero-Martin JM, De Obaldia ME, Allen P, Dudley AC, Klagsbrun M, Bischoff J (2010) Host myeloid cells are necessary for creating bioengineered human vascular networks in vivo. Tissue Eng Part A 16, 2457-2466
40. Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY (2008) CD133 + HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 27:1749-1758 (Pubitemid 351380265)
41. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396-401 (Pubitemid 39551674)
42. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756-760 (Pubitemid 44949604)
43. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65:10946-10951 (Pubitemid 41713363)
44. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843-7848 (Pubitemid 44299144)
45. Maeda S, Shinchi H, Kurahara H, Mataki Y, Maemura K, Sato M, Natsugoe S, Aikou T, Takao S (2008) CD133 expression is correlated with lymph node metastasis and vascular endothelial growth factor-C expression in pancreatic cancer. Br J Cancer 98:1389-1397 (Pubitemid 351543575)
46. Mamluk R, Gechtman Z, Kutcher ME, Gasiunas N, Gallagher J, Klagsbrun M (2002) Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J Biol Chem 277:24818-24825 (Pubitemid 34952014)
47. Saint-Geniez M, Maharaj AS, Walshe TE, Tucker BA, Sekiyama E, Kurihara T, Darland DC, Young MJ, D'Amore PA (2008) Endogenous VEGF is required for visual function: evidence for a survival role on muller cells and photoreceptors. PLoS ONE 3:e3554
48. Arrigoni FI, Matarin M, Thompson PJ, Michaelides M, McClements ME, Redmond E, Clarke L, Ellins E, Mohamed S, Pavord I, Hunt DM, Moore AT, Halcox J (2011) Sisodiya SM Extended extraocular phenotype of PROM1 mutation in kindreds with known autosomal dominant macular dystrophy. Eur J Hum Genet 19, 131-137
49. Michaelides M, Gaillard MC, Escher P, Tiab L, Bedell M, Borruat FX, Barthelmes D, Carmona R, Zhang K, White E, McClements M, Robson AG, Holder GE, Bradshaw K, Hunt DM, Webster AR, Moore AT, Schorderet DF, Munier FL (2010) The PROM1 mutation p.R373C causes an autosomal dominant bull's eye maculopathy associated with rod, rod-cone, and macular dystrophy. Invest Ophthalmol Vis Sci 51, 4771-4780
50. Anderson LH, Boulanger CA, Smith GH, Carmeliet P, Watson CJ (2011) Stem cell marker prominin-1 regulates branching morphogenesis, but not regenerative capacity, in the mammary gland. Dev Dyn 240, 674-681