Detection and quantification of circulating tumor cells in mouse models of human breast cancer using immunomagnetic enrichment and multiparameter flow cytometry

Circulating tumor cells (CTCs) in the peripheral blood of breast cancer patients may be an important indicator of metastatic disease and poor prognosis. However, the use of experimental models is required to fully elucidate the functional consequences of CTCs. The purpose of this study was to optimize the sensitivity of multiparameter flow cytometry for detection of human tumor cells in mouse models of breast cancer.

[1]  S. T. Traweek,et al.  Keratin gene expression in non-epithelial tissues. Detection with polymerase chain reaction. , 1993, The American journal of pathology.

[2]  K. Müller,et al.  Low specificity of cytokeratin 19 reverse transcriptase-polymerase chain reaction analyses for detection of hematogenous lung cancer dissemination. , 1995, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[3]  B. Brandt,et al.  Predictive laboratory diagnostics in oncology utilizing blood-borne cancer cells--current best practice and unmet needs. , 2001, Cancer letters.

[4]  A. Oosterom,et al.  A real-time quantitative reverse transcriptase polymerase chain reaction (RT-PCR) to detect breast carcinoma cells in peripheral blood. , 1999, Annals of oncology : official journal of the European Society for Medical Oncology.

[5]  J. Thiery Epithelial–mesenchymal transitions in tumour progression , 2002, Nature Reviews Cancer.

[6]  M. Skobe,et al.  Lymphatic function, lymphangiogenesis, and cancer metastasis , 2001, Microscopy research and technique.

[7]  J. Talmadge,et al.  Role of NK cells in tumour growth and metastasis in beige mice , 1980, Nature.

[8]  E. Hendrickson The SCID mouse: relevance as an animal model system for studying human disease. , 1993, The American journal of pathology.

[9]  H. Gross,et al.  Detection of rare cells at a frequency of one per million by flow cytometry. , 1993, Cytometry.

[10]  I. Macdonald,et al.  Metastasis: Dissemination and growth of cancer cells in metastatic sites , 2002, Nature Reviews Cancer.

[11]  A. Cesinaro,et al.  Expression of MHC class I and class II antigens in primary breast carcinomas and synchronous nodal metastases , 2004, Clinical & Experimental Metastasis.

[12]  D. Sidransky,et al.  Nucleic acid-based methods for the detection of cancer. , 1997, Science.

[13]  N. Dubrawsky Cancer statistics , 1989, CA: a cancer journal for clinicians.

[14]  W. Gillanders,et al.  The molecular detection of micrometastatic breast cancer. , 2003, American journal of surgery.

[15]  M. Olivé,et al.  Breast tumor cell lines from pleural effusions. , 1974, Journal of the National Cancer Institute.

[16]  S. Rodenhuis,et al.  Comparison of immunocytochemistry, reverse transcriptase polymerase chain reaction, and nucleic acid sequence–based amplification for the detection of circulating breast cancer cells , 1999, Breast Cancer Research and Treatment.

[17]  A. Jemal,et al.  Cancer Statistics, 2004 , 2004, CA: a cancer journal for clinicians.

[18]  S Miltenyi,et al.  Immunomagnetic enrichment of disseminated epithelial tumor cells from peripheral blood by MACS. , 1998, Experimental hematology.

[19]  R. Moll Cytokeratins in the Histological Diagnosis of Malignant Tumors , 1994, The International journal of biological markers.

[20]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[21]  M. Provencio,et al.  Detection of epithelial messenger RNA in the plasma of breast cancer patients is associated with poor prognosis tumor characteristics. , 2001, Clinical cancer research : an official journal of the American Association for Cancer Research.

[22]  I. Fidler,et al.  7th Jan Waldenström Lecture. The biology of human cancer metastasis. , 1991, Acta oncologica.

[23]  Ruth Ladenstein,et al.  Disseminated tumor cells in the bone marrow - chances and consequences of microscopical detection methods. , 2003, Cancer letters.

[24]  I. Fidler The biology of human cancer metastasis , 1991 .

[25]  B. Gallie,et al.  Growth of human tumors in immune-deficient scid mice and nude mice. , 1989, Current topics in microbiology and immunology.

[26]  A. Chambers The metastatic process: basic research and clinical implications. , 1999, Oncology research.

[27]  M. Dowsett,et al.  Circulating tumour cells in breast cancer. , 2004, The Lancet. Oncology.

[28]  R. Clarke Human breast cancer cell line xenografts as models of breast cancer — The immunobiologies of recipient mice and the characteristics of several tumorigenic cell lines , 2005, Breast Cancer Research and Treatment.

[29]  D. Welch Technical considerations for studying cancer metastasis in vivo , 1997, Clinical & Experimental Metastasis.

[30]  Josef Gotzmann,et al.  Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis. , 2004, Mutation research.

[31]  I. Vlachonikolis,et al.  Molecular detection of cytokeratin-19-positive cells in the peripheral blood of patients with operable breast cancer: evaluation of their prognostic significance. , 2002, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[32]  M. Lacroix,et al.  Relevance of Breast Cancer Cell Lines as Models for Breast Tumours: An Update , 2004, Breast Cancer Research and Treatment.

[33]  F. Esteban,et al.  Tumor aggressiveness and MHC class I and II antigens in laryngeal and breast cancer. , 1991, Seminars in cancer biology.

[34]  A. Long,et al.  A human cell line from a pleural effusion derived from a breast carcinoma. , 1973, Journal of the National Cancer Institute.

[35]  K. Pantel,et al.  Frequent down-regulation of major histocompatibility class I antigen expression on individual micrometastatic carcinoma cells. , 1991, Cancer research.

[36]  Mitch Dowsett,et al.  Cell filtration‐laser scanning cytometry for the characterisation of circulating breast cancer cells , 2003, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[37]  J. Price,et al.  Studies of human breast cancer metastasis using nude mice , 1990, Cancer and Metastasis Reviews.

[38]  A. Hart,et al.  Marker genes for circulating tumour cells predict survival in metastasized breast cancer patients , 2003, British Journal of Cancer.

[39]  I. Macdonald,et al.  Cancer spread and micrometastasis development: Quantitative approaches for in vivo models , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[40]  Alison Stopeck,et al.  Circulating tumor cells, disease progression, and survival in metastatic breast cancer. , 2004, The New England journal of medicine.

[41]  H. Gross,et al.  Model study detecting breast cancer cells in peripheral blood mononuclear cells at frequencies as low as 10(-7). , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[42]  D. Griggs,et al.  Characterization of spontaneous metastasis in an aggressive breast carcinoma model using flow cytometry , 2004, Clinical & Experimental Metastasis.

[43]  A. Giuliano,et al.  Detection of occult metastatic breast cancer cells in blood by a multimolecular marker assay: correlation with clinical stage of disease. , 2001, Cancer research.

[44]  L. Liotta,et al.  General mechanisms of metastasis , 1997, Cancer.

[45]  J. Connolly,et al.  Tumor progression in four mammary epithelial cell lines derived from the same patient. , 1990, Cancer research.

[46]  A. Weiss,et al.  Detection and characterization of carcinoma cells in the blood. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[47]  E. Lengyel,et al.  Elevated keratin 18 protein expression indicates a favorable prognosis in patients with breast cancer. , 1996, Clinical cancer research : an official journal of the American Association for Cancer Research.

[48]  S. Wingren,et al.  Loss of cytokeratins in breast cancer cells using multiparameter DNA flow cytometry is related to both cellular factors and preparation procedure. , 1995, Analytical cellular pathology : the journal of the European Society for Analytical Cellular Pathology.

[49]  R. Rubens,et al.  The clinical course of bone metastases from breast cancer. , 1987, British Journal of Cancer.

[50]  M. Redondo,et al.  Major histocompatibility complex status in breast carcinogenesis and relationship to apoptosis. , 2003, Human pathology.

[51]  G. Tilz,et al.  Detection and Quantification of Small Numbers of Circulating Tumour Cells in Peripheral Blood Using Laser Scanning Cytometer (LSC®) , 2001, Clinical chemistry and laboratory medicine.

[52]  N. Brünner,et al.  The nude mouse as an in vivo model for human breast cancer invasion and metastasis. , 1993, Breast Cancer Research and Treatment.

[53]  B. Naume,et al.  Immunomagnetic techniques for the enrichment and detection of isolated breast carcinoma cells in bone marrow and peripheral blood. , 1997, Journal of hematotherapy.

[54]  Wolfgang Henrich,et al.  The prognostic significance of epithelial-mesenchymal transition in breast cancer. , 2002, Anticancer research.

[55]  M. C. Ling,et al.  Osteopontin induces increased invasiveness and plasminogen activator expression of human mammary epithelial cells , 1999, Oncogene.

[56]  N. Harbeck,et al.  Detection and clinical implications of early systemic tumor cell dissemination in breast cancer. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[57]  G. Naumov,et al.  Critical steps in hematogenous metastasis: an overview. , 2001, Surgical oncology clinics of North America.

[58]  Federico Garrido,et al.  MHC class I antigens, immune surveillance, and tumor immune escape , 2003, Journal of cellular physiology.

[59]  R. Ghalie,et al.  Detection of tumor cells in the bone marrow, peripheral blood, and apheresis products of breast cancer patients using flow cytometry. , 1995, Experimental hematology.

[60]  Ruud H. Brakenhoff,et al.  Dissecting the metastatic cascade , 2004, Nature Reviews Cancer.

[61]  K. Pantel,et al.  Limitations of reverse-transcriptase polymerase chain reaction analyses for detection of micrometastatic epithelial cancer cells in bone marrow. , 1997, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[62]  S. Sen,et al.  Aneuploidy and cancer , 2000, Current opinion in oncology.

[63]  J. Price,et al.  Tumorigenicity and metastasis of human breast carcinoma cell lines in nude mice. , 1990, Cancer research.