Home LiteratureArticle Details
PMID: 23002209 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Microenvironmental regulation of epithelial-mesenchymal transitions in cancer.

Cancer research ·Vol. 72 ·No. 19 ·2012-10-01 ·Pages 4883-9

Gao D, Vahdat LT, Wong S, Chang JC, Mittal V

Abstract

The evolution of the cancer cell into a metastatic entity is the major cause of death in patients with cancer. Activation of the epithelial-to-mesenchymal transition (EMT) endows invasive and metastatic properties upon cancer cells that favor successful colonization of distal target organs. The observation that in many cancers distant metastases resemble the epithelial phenotype of primary tumors has led to speculation that the disseminated tumor cells recruited to the target organs undergo mesenchymal-to-epithelial transition (MET). However, the MET cascade has not been recapitulated in vivo, and the cellular and molecular regulators that promote MET remain unknown. In a recent report, using a model of spontaneous breast cancer, we have shown that bone marrow-derived myeloid progenitor cells in the premetastatic lung secrete the proteoglycan versican, which induces MET of metastatic tumor cells and accelerates metastases. This review summarizes recent progress in MET research, outlines a unique paracrine cross-talk between the microenvironment and the cancer cells, which promotes tumor outgrowth in the metastatic organ, and discusses opportunities for novel antimetastatic approaches for cancer therapy.

MeSH Terms
Bone Marrow Cells/metabolism,pathology Breast Neoplasms/metabolism,pathology Cadherins/metabolism Cell Line, Tumor Epithelial-Mesenchymal Transition Female Humans Neoplasm Metastasis Tumor Microenvironment Versicans/metabolism
Chemicals
Cadherins Versicans
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Gao Dingcheng
Department of Cardiothoracic Surgery, Neuberger Berman Lung Cancer Research Center, Weill Cornell Medical College of Cornell University, New York, New York10065, USA.
Vahdat Linda T
Wong Stephen
Chang Jenny C
Mittal Vivek
References (72)
72 references, click to expand
  1. TGF-beta signaling in cancer--a double-edged sword.
    Trends Cell Biol. 2001 Nov;11(11):S44-51 PMID: 11684442
  2. Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression.
    J Cell Physiol. 2007 Nov;213(2):374-83 PMID: 17680632
  3. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis.
    Cancer Cell. 2011 Nov 15;20(5):576-90 PMID: 22094253
  4. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2.
    Cancer Res. 2006 Dec 1;66(23):11271-8 PMID: 17145872
  5. The fallacy of epithelial mesenchymal transition in neoplasia.
    Cancer Res. 2005 Jul 15;65(14):5996-6000; discussion 6000-1 PMID: 16024596
  6. Multiscale modelling and nonlinear simulation of vascular tumour growth.
    J Math Biol. 2009 Apr;58(4-5):765-98 PMID: 18781303
  7. Gene expression profiles of primary breast tumors maintained in distant metastases.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15901-5 PMID: 14665696
  8. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization.
    Nat Med. 2011 Aug 07;17(9):1101-8 PMID: 21822286
  9. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone.
    J Exp Med. 2011 Dec 19;208(13):2641-55 PMID: 22124112
  10. EMT in carcinoma progression and dissemination: facts, unanswered questions, and clinical considerations.
    Cancer Metastasis Rev. 2012 Jun;31(1-2):277-83 PMID: 22215472
  11. Coordinating early kidney development: lessons from gene targeting.
    Nat Rev Genet. 2002 Jul;3(7):533-43 PMID: 12094231
  12. MicroRNAs: critical regulators of epithelial to mesenchymal (EMT) and mesenchymal to epithelial transition (MET) in cancer progression.
    Biol Cell. 2012 Jan;104(1):3-12 PMID: 22188537
  13. Systemic endocrine instigation of indolent tumor growth requires osteopontin.
    Cell. 2008 Jun 13;133(6):994-1005 PMID: 18555776
  14. Prostate tumor cell plasticity: a consequence of the microenvironment.
    Adv Exp Med Biol. 2011;720:81-90 PMID: 21901620
  15. Macrophage diversity enhances tumor progression and metastasis.
    Cell. 2010 Apr 2;141(1):39-51 PMID: 20371344
  16. Differential enhancement of breast cancer cell motility and metastasis by helical and kinase domain mutations of class IA phosphoinositide 3-kinase.
    Cancer Res. 2009 Dec 1;69(23):8868-76 PMID: 19903845
  17. A dynamic in vivo model of epithelial-to-mesenchymal transitions in circulating tumor cells and metastases of breast cancer.
    Oncogene. 2012 Aug 16;31(33):3741-53 PMID: 22120722
  18. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis.
    Science. 2008 Jan 11;319(5860):195-8 PMID: 18187653
  19. The basics of epithelial-mesenchymal transition.
    J Clin Invest. 2009 Jun;119(6):1420-8 PMID: 19487818
  20. Epithelial-mesenchymal transition, cancer stem cells and treatment resistance.
    Breast Cancer Res. 2012 Jan 19;14(1):202 PMID: 22264257
  21. Cross-talk between tumor cells and the microenvironment at the metastatic niche.
    Curr Pharm Biotechnol. 2011 Nov;12(11):1900-8 PMID: 21470134
  22. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor.
    Cancer Res. 2000 May 1;60(9):2504-11 PMID: 10811132
  23. Transforming growth factors type beta 1 and beta 2 are equipotent growth inhibitors of human breast cancer cell lines.
    J Cell Physiol. 1989 Nov;141(2):353-61 PMID: 2808542
  24. Mechanisms of metastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment.
    J Cell Biochem. 2007 Jul 1;101(4):816-29 PMID: 17243120
  25. Epithelial-to-mesenchymal transition in the development and progression of adenocarcinoma and squamous cell carcinoma of the lung.
    Mod Pathol. 2009 May;22(5):668-78 PMID: 19270647
  26. Growth of MDA-MB-231 cell line: different effects of TGF-beta(1), EGF and estradiol depending on the length of exposure.
    Cell Biol Int. 1998;22(9-10):679-84 PMID: 10452838
  27. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing.
    N Engl J Med. 2012 Mar 8;366(10):883-892 PMID: 22397650
  28. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited.
    Nat Rev Cancer. 2003 Jun;3(6):453-8 PMID: 12778135
  29. Embryonic renal epithelia: induction, nephrogenesis, and cell differentiation.
    Physiol Rev. 1999 Oct;79(4):1157-91 PMID: 10508232
  30. Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness.
    Cancer Res. 2010 Sep 1;70(17):6945-56 PMID: 20699369
  31. Two-photon laser scanning fluorescence microscopy.
    Science. 1990 Apr 6;248(4951):73-6 PMID: 2321027
  32. Breast carcinoma cells re-express E-cadherin during mesenchymal to epithelial reverting transition.
    Mol Cancer. 2010 Jul 07;9:179 PMID: 20609236
  33. A hybrid mathematical model of solid tumour invasion: the importance of cell adhesion.
    Math Med Biol. 2005 Jun;22(2):163-86 PMID: 15781426
  34. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.
    Cell. 2006 Jan 27;124(2):263-6 PMID: 16439202
  35. The distribution of secondary growths in cancer of the breast. 1889.
    Cancer Metastasis Rev. 1989 Aug;8(2):98-101 PMID: 2673568
  36. Versican mediates mesenchymal-epithelial transition.
    Mol Biol Cell. 2006 Apr;17(4):2009-20 PMID: 16452631
  37. Augmented autocrine bone morphogenic protein (BMP) 7 signaling increases the metastatic potential of mouse breast cancer cells.
    Clin Exp Metastasis. 2012 Apr;29(4):327-38 PMID: 22274590
  38. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition.
    Cancer Res. 2008 Oct 1;68(19):7846-54 PMID: 18829540
  39. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs.
    Nat Cell Biol. 2011 Mar;13(3):317-23 PMID: 21336307
  40. Microenvironmental regulation of metastasis.
    Nat Rev Cancer. 2009 Apr;9(4):239-52 PMID: 19279573
  41. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition?
    Cancer Res. 2005 Jul 15;65(14):5991-5; discussion 5995 PMID: 16024595
  42. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells.
    EMBO Rep. 2008 Jun;9(6):582-9 PMID: 18483486
  43. Mesenchymal transition and dissemination of cancer cells is driven by myeloid-derived suppressor cells infiltrating the primary tumor.
    PLoS Biol. 2011 Sep;9(9):e1001162 PMID: 21980263
  44. Cancer theory faces doubts.
    Nature. 2011 Apr 21;472(7343):273 PMID: 21512545
  45. Epithelial-mesenchymal transition and cell cooperativity in metastasis.
    Cancer Res. 2009 Sep 15;69(18):7135-9 PMID: 19738043
  46. Whole genome sequencing of matched primary and metastatic acral melanomas.
    Genome Res. 2012 Feb;22(2):196-207 PMID: 22183965
  47. The role of bone-marrow-derived cells in tumor growth, metastasis initiation and progression.
    Trends Mol Med. 2009 Aug;15(8):333-43 PMID: 19665928
  48. Mesenchymal to epithelial transition in development and disease.
    Cells Tissues Organs. 2007;185(1-3):7-19 PMID: 17587803
  49. Epithelial-mesenchymal transitions in development and disease.
    Cell. 2009 Nov 25;139(5):871-90 PMID: 19945376
  50. Potential role of mesenchymal stem cells (MSCs) in the breast tumour microenvironment: stimulation of epithelial to mesenchymal transition (EMT).
    Breast Cancer Res Treat. 2010 Nov;124(2):317-26 PMID: 20087650
  51. Tumour evolution inferred by single-cell sequencing.
    Nature. 2011 Apr 7;472(7341):90-4 PMID: 21399628
  52. A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition.
    J Cell Biol. 2011 Oct 31;195(3):417-33 PMID: 22024162
  53. Direct evidence for epithelial-mesenchymal transitions in breast cancer.
    Cancer Res. 2008 Feb 1;68(3):937-45 PMID: 18245497
  54. The gatekeeper effect of epithelial-mesenchymal transition regulates the frequency of breast cancer metastasis.
    Cancer Res. 2003 Jun 15;63(12):3386-94 PMID: 12810675
  55. Computational modeling of epithelial-mesenchymal transformations.
    Biosystems. 2010 Apr;100(1):23-30 PMID: 20005917
  56. EMT and dissemination precede pancreatic tumor formation.
    Cell. 2012 Jan 20;148(1-2):349-61 PMID: 22265420
  57. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1.
    Nat Cell Biol. 2008 May;10(5):593-601 PMID: 18376396
  58. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions.
    Cell Cycle. 2011 Dec 15;10(24):4256-71 PMID: 22134354
  59. The biological role and regulation of versican levels in cancer.
    Cancer Metastasis Rev. 2009 Jun;28(1-2):233-45 PMID: 19160015
  60. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2.
    J Biol Chem. 2008 May 30;283(22):14910-4 PMID: 18411277
  61. Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility.
    Nat Cell Biol. 2009 Nov;11(11):1287-96 PMID: 19838175
  62. The ZEB/miR-200 feedback loop--a motor of cellular plasticity in development and cancer?
    EMBO Rep. 2010 Sep;11(9):670-7 PMID: 20706219
  63. Intratumoral macrophages contribute to epithelial-mesenchymal transition in solid tumors.
    BMC Cancer. 2012 Jan 24;12:35 PMID: 22273460
  64. Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer.
    Nat Med. 2009 May;15(5):559-65 PMID: 19363497
  65. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits.
    Nat Rev Cancer. 2009 Apr;9(4):265-73 PMID: 19262571
  66. Bone morphogenetic protein 7 induces mesenchymal-to-epithelial transition in melanoma cells, leading to inhibition of metastasis.
    Cancer Sci. 2009 Nov;100(11):2218-25 PMID: 19735263
  67. Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with node-negative primary breast cancer.
    Clin Cancer Res. 2002 Apr;8(4):1054-60 PMID: 11948113
  68. Snail silencing effectively suppresses tumour growth and invasiveness.
    Oncogene. 2007 Mar 22;26(13):1862-74 PMID: 17043660
  69. Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors.
    Clin Cancer Res. 2009 Nov 1;15(21):6630-8 PMID: 19843665
  70. The metastatic niche: adapting the foreign soil.
    Nat Rev Cancer. 2009 Apr;9(4):285-93 PMID: 19308068
  71. Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells.
    Cancer Res. 2011 Mar 1;71(5):1550-60 PMID: 21343399
  72. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition.
    Cancer Res. 2012 Mar 15;72(6):1384-94 PMID: 22282653
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2012-10-01
Epub
2012-00-20
Pages
4883-9
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC3649848
Subset
IM
Grants
NCI NIH HHS · R01 CA135417 · United States
NCI NIH HHS · U54CA143876 · United States
NCI NIH HHS · RC1 CA146065 · United States
NCI NIH HHS · U54 CA143876 · United States
NCI NIH HHS · CA107429 · United States
PHS HHS · RCA146065 · United States
NCI NIH HHS · CA135417 · United States
NCI NIH HHS · R01 CA107429 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com