Phenotypic heterogeneity of breast cancer stem cells

Journal of Oncology

Volumn , Issue , 2011, Pages

  Lorico, Aurelio ^a   Rappa, Germana ^a  

^a NEVADA CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD133 ANTIGEN; CD24 ANTIGEN; CD44V ANTIGEN; INTEGRIN;

ACUTE GRANULOCYTIC LEUKEMIA; BREAST CANCER; CANCER STEM CELL; CANCER SURVIVOR; CARCINOGENESIS; CELL DIFFERENTIATION; CELL HETEROGENEITY; GERM CELL TUMOR; HUMAN; LEUKEMIA CELL; PHENOTYPE; REVIEW; TUMOR GROWTH;

EID: 79952211366     PISSN: 16878450     EISSN: 16878469     Source Type: Journal    
DOI: 10.1155/2011/135039     Document Type: Review

References (66)

1. Horwich A., Shipley J., Huddart R., Testicular germ-cell c (Pubitemid 43326294)
2. Bonnet D., Dick J. E., Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nature Medicine 1997 3 7 730 737 (Pubitemid 27298715)
3. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., Minden M., Paterson B., Caligiuri M. A., Dick J. E., A cell initiating human acute myeloid leukaemia after transplantation into SCID mice Nature 1994 367 6464 645 648 (Pubitemid 24067706)
4. Yilmaz O. H., Valdez R., Theisen B. K., Guo W., Ferguson D. O., Wu H., Morrison S. J., Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells Nature 2006 441 7092 475 482 (Pubitemid 44050144)
5. Al-Hajj M., Wicha M. S., Benito-Hernandez A., Morrison S. J., Clarke M. F., Prospective identification of tumorigenic breast cancer cells Proceedings of the National Academy of Sciences of the United States of America 2003 100 7 3983 3988 (Pubitemid 36418143)
6. Fang D., Nguyen T. K., Leishear K., Finko R., Kulp A. N., Hotz S., Van Belle P. A., Xu X., Elder D. E., Herlyn M., A tumorigenic subpopulation with stem cell properties in melanomas Cancer Research 2005 65 20 9328 9337 (Pubitemid 41508000)
7. Hemmati H. D., Nakano I., Lazareff J. A., Masterman-Smith M., Geschwind D. H., Bronner-Fraser M., Kornblum H. I., Cancerous stem cells can arise from pediatric brain tumors Proceedings of the National Academy of Sciences of the United States of America 2003 100 25 15178 15183 (Pubitemid 37518036)
8. Kim C. F. B., Jackson E. L., Woolfenden A. E., Lawrence S., Babar I., Vogel S., Crowley D., Bronson R. T., Jacks T., Identification of bronchioalveolar stem cells in normal lung and lung cancer Cell 2005 121 6 823 835 (Pubitemid 40806415)
9. Lawson D. A., Xin LI., Lukacs R. U., Cheng D., Witte O. N., Isolation and functional characterization of murine prostate stem cells Proceedings of the National Academy of Sciences of the United States of America 2007 104 1 181 186 (Pubitemid 46068005)
10. Li C., Heidt D. G., Dalerba P., Burant C. F., Zhang L., Adsay V., Wicha M., Clarke M. F., Simeone D. M., Identification of pancreatic cancer stem cells Cancer Research 2007 67 3 1030 1037
11. Ricci-Vitiani L., Lombardi D. G., Pilozzi E., Biffoni M., Todaro M., Peschle C., De Maria R., Identification and expansion of human colon-cancer-initiating cells Nature 2007 445 7123 111 115 (Pubitemid 46067311)
12. Singh S. K., Clarke I. D., Terasaki M., Bonn V. E., Hawkins C., Squire J., Dirks P. B., Identification of a cancer stem cell in human brain tumors Cancer Research 2003 63 18 5821 5828 (Pubitemid 37187480)
13. Xin LI., Lawson D. A., Witte O. N., The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis Proceedings of the National Academy of Sciences of the United States of America 2005 102 19 6942 6947 (Pubitemid 40675421)
14. Bao S., Wu Q., McLendon R. E., Hao Y., Shi Q., Hjelmeland A. B., Dewhirst M. W., Bigner D. D., Rich J. N., Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 2006 444 7120 756 760 (Pubitemid 44949604)
15. Jin L., Hope K. J., Zhai Q., Smadja-Joffe F., Dick J. E., Targeting of CD44 eradicates human acute myeloid leukemic stem cells Nature Medicine 2006 12 10 1167 1174 (Pubitemid 44527352)
16. Sagiv E., Starr A., Rozovski U., Khosravi R., Altevogt P., Wang T., Arbere N., Targeting CD24 for treatment of colorectal and pancreatic cancer by monoclonal antibodies or small interfering RNA Cancer Research 2008 68 8 2803 2812 (Pubitemid 351556279)
17. Smith L. M., Nesterova A., Ryan M. C., Duniho S., Jonas M., Anderson M., Zabinski R. F., Sutherland M. K., Gerber H. P., Van Orden K. L., Moore P. A., Ruben S. M., Carter P. J., CD133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers British Journal of Cancer 2008 99 1 100 109 (Pubitemid 351920235)
18. Mikkola H. K. A., Radu C. G., Witte O. N., Targeting leukemia stem cells Nature Biotechnology 2010 28 3 237 238
19. Bordonaro M., Lazarova D. L., Augenlicht L. H., Sartorelli A. C., Estimates of the world-wide prevalence of cancer for 25 sites in the adult population International Journal of Cancer 2002 97 1 72 81 (Pubitemid 33104397)
20. Srlie T., Perou C. M., Tibshirani R., Aas T., Geisler S., Johnsen H., Hastie T., Eisen M. B., Van De Rijn M., Jeffrey S. S., Thorsen T., Quist H., Matese J. C., Brown P. O., Botstein D., Lnning P. E., Brresen-Dale A. L., Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications Proceedings of the National Academy of Sciences of the United States of America 2001 98 19 10869 10874 (Pubitemid 32878711)
21. Perou C. M., Srile T., Eisen M. B., Van De Rijn M., Jeffrey S. S., Ress C. A., Pollack J. R., Ross D. T., Johnsen H., Akslen L. A., Fluge., Pergammenschlkov A., Williams C., Zhu S. X., Lnning P. E., Brresen-Dale A. L., Brown P. O., Botstein D., Molecular portraits of human breast tumours Nature 2000 406 6797 747 752
22. Srlie T., Wang Y., Xiao C., Johnsen H., Naume B., Samaha R. R., Brresen-Dale A. L., Distinct molecular mechanisms underlying clinically relevant subtypes of breast cancer: gene expression analyses across three different platforms BMC Genomics 2006 7, article 127
23. Park SO. Y., Lee H. E., Li H., Shipitsin M., Gelman R., Polyak K., Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer Clinical Cancer Research 2010 16 3 876 887
24. Park SO. Y., Gnen M., Kim H. J., Michor F., Polyak K., Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype Journal of Clinical Investigation 2010 120 2 636 644
25. Allred D. C., Wu Y., Mao S., Nagtegaal I. D., Lee S., Perou C. M., Mohsin S. K., O'Connell P., Tsimelzon A., Medina D., Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution Clinical Cancer Research 2008 14 2 370 378 (Pubitemid 351226103)
26. Beier D., Hau P., Proescholdt M., Lohmeier A., Wischhusen J., Oefner P. J., Aigner L., Brawanski A., Bogdahn U., Beier C. P., CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles Cancer Research 2007 67 9 4010 4015 (Pubitemid 46815044)
27. Bexell D., Gunnarsson S., Siesj P., Bengzon J., Darabi A., CD133+ and nestin+ tumor-initiating cells dominate in N29 and N32 experimental gliomas International Journal of Cancer 2009 125 1 15 22
28. Ponti D., Costa A., Zaffaroni N., Pratesi G., Petrangolini G., Coradini D., Pilotti S., Pierotti M. A., Daidone M. G., Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties Cancer Research 2005 65 13 5506 5511 (Pubitemid 40911148)
29. Kay R., Takei F., Humphries R. K., Expression cloning of a cDNA encoding M1/69-J11d heat-stable antigens Journal of Immunology 1990 145 6 1952 1959 (Pubitemid 20336768)
30. Kim H. J., Kim J. B., Lee K. M., Shin I., Han W., Ko E., Bae JI. Y., Noh D. Y., Isolation of CD24(high) and CD24(low/-) cells from MCF-7: CD24 expression is positively related with proliferation, adhesion and invasion in MCF-7 Cancer Letters 2007 258 1 98 108 (Pubitemid 47600499)
31. Aigner S., Ramos C. L., Hafezi-Moghadam A., Lawrence M. B., Friederichs J., Altevogt P., Ley K., CD24 mediates rolling of breast carcinoma cellson P-selectin FASEB Journal 1998 12 12 1241 1251 (Pubitemid 28418954)
32. Orian-Rousseau V., CD44, a therapeutic target for metastasising tumours European Journal of Cancer 2010 46 7 1271 1277
33. Abraham B. K., Fritz P., McClellan M., Hauptvogel P., Athelogou M., Brauch H., Prevalence of CD44+/CD24-/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis Clinical Cancer Research 2005 11 3 1154 1159 (Pubitemid 40175765)
34. Honeth G., Bendahl P. O., Ringnr M., Saal L. H., Gruvberger-Saal S. K., Lvgren K., Grabau D., Fern M., Borg A., Hegardt C., The CD44+/CD24- phenotype is enriched in basal-like breast tumors Breast Cancer Research 2008 10 3, article R53
35. Creighton C. J., Li X., Landis M., Dixon J. M., Neumeister V. M., Sjolund A., Rimm D. L., Wong H., Rodriguez A., Herschkowitz J. I., Fan C., Zhang X., He X., Pavlick A., Gutierrez M. C., Renshaw L., Larionov A. A., Faratian D., Hilsenbeck S. G., Perou C. M., Lewis M. T., Rosen J. M., Chang J. C., Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features Proceedings of the National Academy of Sciences of the United States of America 2009 106 33 13820 13825
36. Fogel M., Friederichs J., Zeller Y., Husar M., Smirnov A., Roitman L., Altevogt P., Sthoeger Z. M., CD24 is a marker for human breast carcinoma Cancer Letters 1999 143 1 87 94 (Pubitemid 29327194)
37. Sheridan C., Kishimoto H., Fuchs R. K., Mehrotra S., Bhat-Nakshatri P., Turner C. H., Goulet R., Badve S., Nakshatri H., CD44+/CD24-breast cancer cells exhibit enhanced invase properties: an early step necessary for metastasis Breast Cancer Research 2006 8 5, article R59
38. Schindelmann S., Windisch J., Grundmann R., Kreienberg R., Zeillinger R., Deissler H., Expression profiling of mammary carcinoma cell lines: correlation of in vitro invasiveness with expression of CD24 Tumor Biology 2002 23 3 139 145 (Pubitemid 44858305)
39. Rappa G., Lorico A., Phenotypic characterization of mammosphere-forming cells from the human MA-11 breast carcinoma cell line Experimental Cell Research 2010 316 9 1576 1586
40. Engebraaten O., Fodstad., Site-specific experimental metastasis patterns of two human breast cancer cell lines in nude rats International Journal of Cancer 1999 82 2 219 225 (Pubitemid 29293781)
41. Monzani E., Facchetti F., Galmozzi E., Corsini E., Benetti A., Cavazzin C., Gritti A., Piccinini A., Porro D., Santinami M., Invernici G., Parati E., Alessandri G., La Porta C. A. M., Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential European Journal of Cancer 2007 43 5 935 946 (Pubitemid 46366698)
42. Fournier M. V., Martin K. J., Transcriptome profiling in clinical breast cancer: from 3d culture models to prognostic signatures Journal of Cellular Physiology 2006 209 3 625 630 (Pubitemid 44665679)
43. Hirschmann-Jax C., Foster A. E., Wulf G. G., Nuchtern J. G., Jax T. W., Gobel U., Goodell M. A., Brenner M. K., A distinct "side population" of cells with high drug efflux capacity in human tumor cells Proceedings of the National Academy of Sciences of the United States of America 2004 101 39 14228 14233 (Pubitemid 39305058)
44. Patrawala L., Calhoun T., Schneider-Broussard R., Zhou J., Claypool K., Tang D. G., Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2 and ABCG2 cancer cells are similarly tumorigenic Cancer Research 2005 65 14 6207 6219 (Pubitemid 40994406)
45. Ginestier C., Hur M. H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., Jacquemier J., Viens P., Kleer C. G., Liu S., Schott A., Hayes D., Birnbaum D., Wicha M. S., Dontu G., ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome Cell Stem Cell 2007 1 5 555 567 (Pubitemid 350056407)
46. Charafe-Jauffret E., Ginestier C., Iovino F., Wicinski J., Cervera N., Finetti P., Hur M. H., Diebel M. E., Monville F., Dutcher J., Brown M., Viens P., Xerri L., Bertucci F., Stassi G., Dontu G., Birnbaum D., Wicha M. S., Breast cancer cell lines contain functional cancer stem sells with metastatic capacity and a distinct molecular signature Cancer Research 2009 69 4 1302 1313
47. Xiao YI., Ye Y., Yearsley K., Jones S., Barsky S. H., The lymphovascular embolus of inflammatory breast cancer expresses a stem cell-like phenotype American Journal of Pathology 2008 173 2 561 574
48. Wright M. H., Calcagno A. M., Salcido C. D., Carlson M. D., Ambudkar S. V., Varticovski L., Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics Breast Cancer Research 2008 10 1, article R10
49. Storci G., Sansone P., Trere D., Tavolari S., Taffurelli M., Ceccarelli C., Guarnieri T., Paterini P., Pariali M., Montanaro L., Santini D., Chieco P., Bonaf M., The basal-like breast carcinoma phenotype is regulated by SLUG gene expression Journal of Pathology 2008 214 1 25 37
50. Vassilopoulos A., Wang R. H., Petrovas C., Ambrozak D., Koup R., Deng C. X., Identification and characterization of cancer initiating cells from BRCA1 related mammary tumors using markers for normal mammary stem cells International Journal of Biological Sciences 2008 4 3 133 142 (Pubitemid 351872048)
51. Vaillant F., Asselin-Labat M. L., Shackleton M., Forrest N. C., Lindeman G. J., Visvader J. E., The mammary progenitor marker CD61/ 3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis Cancer Research 2008 68 19 7711 7717
52. Martin K. J., Patrick D. R., Bissell M. J., Fournier M. V., Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets PLoS ONE 2008 3 8
53. Rappa G., Mercapide J., Anzanello F., Prasmickaite L., Xi Y., Ju J., Fodstad O., Lorico A., Growth of cancer cell lines under stem cell-like conditions has the potential to unveil therapeutic targets Experimental Cell Research 2008 314 10 2110 2122
54. Goodell M. A., Brose K., Paradis G., Conner A. S., Mulligan R. C., Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo Journal of Experimental Medicine 1996 183 4 1797 1806 (Pubitemid 26134320)
55. Chen M. S., Woodward W. A., Behbod F., Peddibhotla S., Alfaro M. P., Buchholz T. A., Rosen J. M., Wnt/ -catenin mediates radiation resistance of Sca1+ progenitors in an immortalized mammary gland cell line Journal of Cell Science 2007 120 3 468 477 (Pubitemid 46332510)
56. Alison M. R., Guppy N. J., Lim S. M., Nicholson L. J., Finding cancer stem cells: are aldehyde dehydrogenases fit for purpose? The Journal of Pathology 2010 222 4 335 344
57. Charafe-Jauffret E., Ginestier C., Iovino F., Tarpin C., Diebel M., Esterni B., Houvenaeghel G., Extra J. M., Bertucci F., Jacquemier J., Xerri L., Dontu G., Stassi G., Xiao YI., Barsky S. H., Birnbaum D., Viens P., Wicha M. S., Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer Clinical Cancer Research 2010 16 1 45 55
58. Yin A. H., Miraglia S., Zanjani E. D., Almeida-Porada G., Ogawa M., Leary A. G., Olweus J., Kearney J., Buck D. W., AC133, a novel marker for human hematopoietic stem and progenitor cells Blood 1997 90 12 5002 5012 (Pubitemid 28007217)
59. Weigmann A., Corbeil D., Hellwig A., Huttner W. B., Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells Proceedings of the National Academy of Sciences of the United States of America 1997 94 23 12425 12430 (Pubitemid 27492544)
60. Mizrak D., Brittan M., Alison M. R., CD 133: molecule of the moment Journal of Pathology 2008 214 1 3 9
61. Mehra N., Penning M., Maas J., Beerepoot L. V., Van Daal N., Van Gils C. H., Giles R. H., Voest E. E., Progenitor marker CD133 mRNA is elevated in peripheral blood of cancer patients with bone metastases Clinical Cancer Research 2006 12 16 4859 4866 (Pubitemid 44338571)
62. Yang Z., Chen Y., Lillo C., Chien J., Yu Z., Michaelides M., Klein M., Howes K. A., Li Y., Kaminoh Y., Chen H., Zhao C., Chen Y., Al-Sheikh Y. T., Karan G., Corbeil D., Escher P., Kamaya S., Li C., Johnson S., Frederick J. M., Zhao YU., Wang C., Cameron D. J., Huttner W. B., Schorderet D. F., Munier F. L., Moore A. T., Birch D. G., Baehr W., Hunt D. M., Williams D. S., Zhang K., Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice Journal of Clinical Investigation 2008 118 8 2908 2916
63. Rappa G., Fodstad O., Lorico A., The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma Stem Cells 2008 26 12 3008 3017
64. Shackleton M., Vaillant F., Simpson K. J., Stingl J., Smyth G. K., Asselin-Labat M. L., Wu LI., Lindeman G. J., Visvader J. E., Generation of a functional mammary gland from a single stem cell Nature 2006 439 7072 84 88 (Pubitemid 43053633)
65. Stingl J., Eirew P., Ricketson I., Shackleton M., Vaillant F., Choi D., Li H. I., Eaves C. J., Purification and unique properties of mammary epithelial stem cells Nature 2006 439 7079 993 997 (Pubitemid 43292419)
66. Taddei I., Faraldo M. M., Teulire J., Deugnier M. A., Thiery J. P., Glukhova M. A., Integrins in mammary gland development and differentiation of mammary epithelium Journal of Mammary Gland Biology and Neoplasia 2003 8 4 383 394 (Pubitemid 39137501)