MMP1, MMP9, and COX2 expressions in promonocytes are induced by breast cancer cells and correlate with collagen degradation, transformation-like morphological changes in MCF-10A acini, and tumor aggressiveness

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Chimal Ramirez G K ^a,b   Espinoza Sanchez N A ^a,b   Utrera Barillas, D ^c   Benitez Bribiesca L ^c   Velazquez J R ^d   Arriaga Pizano, L A ^e   Monroy Garcia A ^c   Reyes Maldonado, E ^b   Dominguez Lopez M L ^b   Piña Sánchez, Patricia ^c   Fuentes Panana E M ^a  

^a HOSPITAL DE PEDIATRÍA   (Mexico)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^c HOSPITAL DE ONCOLOGÍA   (Mexico)

^d INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

^e HOSPITAL DE ESPECIALIDADES   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; CYCLOOXYGENASE 2; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIGEL; PROSTAGLANDIN; PROSTAGLANDIN 2; UNCLASSIFIED DRUG; MMP1 PROTEIN, HUMAN; MMP9 PROTEIN, HUMAN; PROSTAGLANDIN E2; PTGS2 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; COCULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOCYTOCHEMISTRY; MONOCYTE MACROPHAGE PRECURSOR CELL; MORPHOLOGY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SENSOR; SUPERNATANT; UPREGULATION; ACINAR CELL; BIOLOGICAL MODEL; BREAST TUMOR; CELL COMMUNICATION; CELL TRANSFORMATION; ENZYMOLOGY; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHENOTYPE; SOLUBILITY; TUMOR CELL LINE; TUMOR INVASION;

ACINAR CELLS; BREAST NEOPLASMS; CELL COMMUNICATION; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; COCULTURE TECHNIQUES; COLLAGEN; CYCLOOXYGENASE 2; DINOPROSTONE; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 9; MODELS, BIOLOGICAL; MONOCYTE-MACROPHAGE PRECURSOR CELLS; NEOPLASM INVASIVENESS; PHENOTYPE; PROTEOLYSIS; SOLUBILITY; UP-REGULATION;

EID: 84878740442     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/279505     Document Type: Article

References (75)

1. Hanahan D., Weinberg R. A., Hallmarks of cancer: the next generation. Cell 2011 144 5 646 674 2-s2.0-79952284127 10.1016/j.cell.2011.02.013
2. Mbeunkui F., Johann D. J. Jr., Cancer and the tumor microenvironment: a review of an essential relationship. Cancer Chemotherapy and Pharmacology 2009 63 4 571 582 2-s2.0-58849131828 10.1007/s00280-008-0881-9
3. Wyckoff J. B., Wang Y., Lin E. Y., Li J. F., Goswami S., Stanley E. R., Segall J. E., Pollard J. W., Condeelis J., Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Research 2007 67 6 2649 2656 2-s2.0-34047246527 10.1158/0008-5472.CAN-06-1823 (Pubitemid 46548952)
4. Bingle L., Brown N. J., Lewis C. E., The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. Journal of Pathology 2002 196 3 254 265 2-s2.0-0036187615 10.1002/path.1027 (Pubitemid 34189413)
5. Balkwill F. R., Mantovani A., Cancer-related inflammation: common themes and therapeutic opportunities. Seminars in Cancer Biology 2012 22 1 33 40
6. Sica A., Mantovani A., Macrophage plasticity and polarization: in vivo veritas. The Journal of Clinical Investigation 2012 122 3 787 795
7. Mahmoud S. M., Lee A. H., Paish E. C., Macmillan R. D., Ellis I. O., Green A. R., Tumour-infiltrating macrophages and clinical outcome in breast cancer. Journal of Clinical Pathology 2012 65 2 159 163
8. Laoui D., Movahedi K., Van Overmeire E., Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. The International Journal of Developmental Biology 2011 55 7-9 861 867
9. Lin E. Y., Nguyen A. V., Russell R. G., Pollard J. W., Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. Journal of Experimental Medicine 2001 193 6 727 740 2-s2.0-0035911221 10.1084/jem.193.6.727 (Pubitemid 32524466)
10. Lin E. Y., Gouon-Evans V., Nguyen A. V., Pollard J. W., The macrophage growth factor CSF-1 in mammary gland development and tumor progression. Journal of Mammary Gland Biology and Neoplasia 2002 7 2 147 162 2-s2.0-0038230415 10.1023/A:1020399802795 (Pubitemid 38420772)
11. Qian B. Z., Pollard J. W., Macrophage diversity enhances tumor progression and metastasis. Cell 2010 141 1 39 51 2-s2.0-77950950894 10.1016/j.cell.2010.03.014
12. Boland G. P., Butt I. S., Prasad R., Knox W. F., Bundred N. J., COX-2 expression is associated with an aggressive phenotype in ductal carcinoma in situ. British Journal of Cancer 2004 90 2 423 429 2-s2.0-1342301548 10.1038/sj.bjc.6601534 (Pubitemid 38250640)
13. Shim V., Gauthier M. L., Sudilovsky D., Mantei K., Chew K. L., Moore D. H., Cha I., Tlsty T. D., Esserman L. J., Cyclooxygenase-2 expression is related to nuclear grade in ductal carcinoma in situ and is increased in its normal adjacent epithelium. Cancer Research 2003 63 10 2347 2350 2-s2.0-0038182606 (Pubitemid 36605165)
14. Hiller D. J., Meschonat C., Kim R., Li B. D., Chu Q. D., Chemokine receptor CXCR4 level in primary tumors independently predicts outcome for patients with locally advanced breast cancer. Surgery 2011 150 3 459 465
15. Parker C. C., Kim R. H., Li B. D., Chu Q. D., The chemokine receptor CXCR4 as a novel independent prognostic marker for node-positive breast cancer patients. Journal of Surgical Oncology 2012 106 4 393 398
16. Pender S. L. F., Salmela M. T., Monteleone G., Schnapp D., McKenzie C., Spencer J., Fong S., Saarialho-Kere U., MacDonald T. T., Ligation of 4 β 1 integrin on human intestinal mucosal mesenchymal cells selectively up-regulates membrane type-1 matrix metalloproteinase and confers a migratory phenotype. American Journal of Pathology 2000 157 6 1955 1962 2-s2.0-0033622478
17. Mi Z., Bhattacharya S. D., Kim V. M., Guo H., Talbotq L. J., Kuo P. C., Osteopontin promotes CCL5-mesenchymal stromal cell-mediated breast cancer metastasis. Carcinogenesis 2011 32 4 477 487 2-s2.0-79953727008 10.1093/carcin/bgr009
18. Shevde L. A., Das S., Clark D. W., Samant R. S., Osteopontin: an effector and an effect of tumor metastasis. Current Molecular Medicine 2010 10 1 71 81 2-s2.0-77949447135 10.2174/156652410791065381
19. Köhrmann A., Kammerer U., Kapp M., Dietl J., Anacker J., Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: new findings and review of the literature. BMC Cancer 2009 9, article 188 2-s2.0-67651071905 10.1186/1471-2407-9-188
20. Tang L., Han X., The urokinase plasminogen activator system in breast cancer invasion and metastasis. Biomedicine & Pharmacotherapy 2013 67 2 179 182
21. Harbeck N., Kates R. E., Gauger K., Willems A., Kiechle M., Magdolen V., Schmitt M., Urokinase-type plasminogen activator (uPA) and its inhibitor PAI-1: novel tumor-derived factors with a high prognostic and predictive impact in breast cancer. Thrombosis and Haemostasis 2004 91 3 450 456 2-s2.0-1642375334 (Pubitemid 38396866)
22. Reinheckel T., Peters C., Kruger A., Turk B., Vasiljeva O., Differential impact of cysteine cathepsins on genetic mouse models of de novo carcinogenesis: cathepsin B as emerging therapeutic target. Frontiers in Pharmacology 2012 3, article 133
23. Joyce J. A., Baruch A., Chehade K., Meyer-Morse N., Giraudo E., Tsai F. Y., Greenbaum D. C., Hager J. H., Bogyo M., Hanahan D., Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 2004 5 5 443 453 2-s2.0-2342603891 10.1016/S1535-6108(04)00111-4 (Pubitemid 38610246)
24. Berchem G., Glondu M., Gleizes M., Brouillet J. P., Vignon F., Garcia M., Liaudet-Coopman E., Cathepsin-D affects multiple tumor progression steps in vivo: proliferation, angiogenesis and apoptosis. Oncogene 2002 21 38 5951 5955 2-s2.0-0037194598 10.1038/sj.onc.1205745 (Pubitemid 35007248)
25. Liaudet-Coopman E., Beaujouin M., Derocq D., Garcia M., Glondu-Lassis M., Laurent-Matha V., Prébois C., Rochefort H., Vignon F., Cathepsin D: newly discovered functions of a long-standing aspartic protease in cancer and apoptosis. Cancer Letters 2006 237 2 167 179 2-s2.0-33646854205 10.1016/j.canlet.2005.06.007 (Pubitemid 43777078)
26. Benitez-Bribiesca L., Martinez G., Ruiz M. T., Gutierrez-Delgado F., Utrera D., Proteinase activity in invasive cancer of the breast. Correlation with tumor progression. Archives of Medical Research 1995 26 S163 S168 2-s2.0-0029587731 (Pubitemid 26044948)
27. Sameni M., Anbalagan A., Olive M. B., Moin K., Mattingly R. R., Sloane B. F., MAME models for 4D live-cell imaging of tumor: microenvironment interactions that impact malignant progression. Journal of Visualized Experiments 2012 60, article e3661 10.3791/3661
28. Raof N. A., Raja W. K., Castracane J., Xie Y., Bioengineering embryonic stem cell microenvironments for exploring inhibitory effects on metastatic breast cancer cells. Biomaterials 2011 32 17 4130 4139 2-s2.0-79953271040 10.1016/j.biomaterials.2011.02.035
29. Dittmer A., Fuchs A., Oerlecke I., Leyh B., Kaiser S., Martens J. W. M., Lützkendorf J., Müller L., Dittmer J., Mesenchymal stem cells and carcinoma-associated fibroblasts sensitize breast cancer cells in 3D cultures to kinase inhibitors. International Journal of Oncology 2011 39 3 689 696 2-s2.0-79959955162 10.3892/ijo.2011.1073
30. Krishnan V., Shuman L. A., Sosnoski D. M., Dhurjati R., Vogler E. A., Mastro A. M., Dynamic interaction between breast cancer cells and osteoblastic tissue: comparison of Two- and Three-dimensional cultures. Journal of Cellular Physiology 2011 226 8 2150 2158 2-s2.0-79955116966 10.1002/jcp.22550
31. Debnath J., Muthuswamy S. K., Brugge J. S., Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003 30 3 256 268 2-s2.0-0037603113 10.1016/S1046-2023(03)00032-X (Pubitemid 36677560)
32. Hebner C., Weaver V. M., Debnath J., Modeling morphogenesis and oncogenesis in three-dimensional breast epithelial cultures. Annual Review of Pathology 2008 3 313 339 2-s2.0-41749089800 10.1146/annurev.pathmechdis.3. 121806.151526 (Pubitemid 351488284)
33. Privette Vinnedge L. M., McClaine R., Wagh P. K., Wikenheiser-Brokamp K. A., Waltz S. E., Wells S. I., The human DEK oncogene stimulates Β -catenin signaling, invasion and mammosphere formation in breast cancer. Oncogene 2011 30 24 2741 2752 2-s2.0-79958837212 10.1038/onc.2011.2
34. Cho K. B., Cho M. K., Lee W. Y., Kang K. W., Overexpression of c-myc induces epithelial mesenchymal transition in mammary epithelial cells. Cancer Letters 2010 293 2 230 239 2-s2.0-77952490843 10.1016/j.canlet.2010.01.013
35. Sameni M., Dosescu J., Moin K., Sloane B. F., Functional imaging of proteolysis: stromal and inflammatory cells increase tumor proteolysis. Molecular Imaging 2003 2 3 159 175 2-s2.0-0242577116 10.1162/153535003322556903
36. Sameni M., Dosescu J., Yamada K. M., Sloane B. F., Cavallo-Medved D., Functional live-cell imaging demonstrates that β 1-integrin promotes type IV collagen degradation by breast and prostate cancer cells. Molecular Imaging 2008 7 5 199 213 2-s2.0-61549095506
37. Lacroix M., Leclercq G., Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Research and Treatment 2004 83 3 249 289 2-s2.0-1342326910 10.1023/B:BREA.0000014042.54925.cc (Pubitemid 38264873)
38. Micalizzi D. S., Farabaugh S. M., Ford H. L., Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. Journal of Mammary Gland Biology and Neoplasia 2010 15 2 117 134 2-s2.0-77954860342 10.1007/s10911-010-9178-9
39. Harris P., Ralph P., Human leukemic models of myelomonocytic development: a review of the HL-60 and U937 cell lines. Journal of Leukocyte Biology 1985 37 4 407 422 2-s2.0-0021992164 (Pubitemid 15147523)
40. Bertram C., von Neuhoff N., Skawran B., Steinemann D., Schlegelberger B., Hass R., The differentiation/retrodifferentiation program of human U937 leukemia cells is accompanied by changes of VCP/p97. BMC Cell Biology 2008 9, article 12 2-s2.0-41749085070 10.1186/1471-2121-9-12 (Pubitemid 351486690)
41. Sameni M., Cavallo-Medved D., Dosescu J., Jedeszko C., Moin K., Mullins S. R., Olive M. B., Rudy D., Sloane B. F., Imaging and quantifying the dynamics of tumor-associated proteolysis. Clinical and Experimental Metastasis 2009 26 4 299 309 2-s2.0-62449181023 10.1007/s10585-008-9218-7
42. Kim I. Y., Yong H. Y., Kang K. W., Moon A., Overexpression of ErbB2 induces invasion of MCF10A human breast epithelial cells via MMP-9. Cancer Letters 2009 275 2 227 233 2-s2.0-59349110736 10.1016/j.canlet.2008.10.013
43. Chimal-Ramírez G. K., Espinoza-Sánchez N. A., Fuentes-Pananá E. M., Protumor activities of the immune response: insights in the mechanisms of immunological shift, oncotraining, and oncopromotion. Journal of Oncology 2013 2013 16 835956 10.1155/2013/835956
44. Pollard J. W., Trophic macrophages in development and disease. Nature Reviews Immunology 2009 9 4 259 270
45. Loberg R. D., Ying C., Craig M., Yan L., Snyder L. A., Pienta K. J., CCL2 as an important mediator of prostate cancer growth in vivo through the regulation of macrophage infiltration. Neoplasia 2007 9 7 556 562 2-s2.0-34547184682 10.1593/neo.07307 (Pubitemid 47121829)
46. Murdoch C., Tazzyman S., Webster S., Lewis C. E., Expression of Tie-2 by human monocytes and their responses to angiopoietin-2. Journal of Immunology 2007 178 11 7405 7411 2-s2.0-34249791475 (Pubitemid 46847468)
47. Lin E. Y., Pollard J. W., Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Research 2007 67 11 5064 5066 2-s2.0-34347226359 10.1158/0008-5472.CAN-07-0912 (Pubitemid 46997238)
48. Porta C., Subhra Kumar B., Larghi P., Rubino L., Mancino A., Sica A., Tumor promotion by tumor-associated macrophages. Advances in Experimental Medicine and Biology 2007 604 67 86 2-s2.0-34548485810 10.1007/978-0-387-69116- 9-5
49. Leek R. D., Lewis C. E., Whitehouse R., Greenall M., Clarke J., Harris A. L., Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Research 1996 56 20 4625 4629 2-s2.0-0029816609 (Pubitemid 26338061)
50. Lolmede K., Campana L., Vezzoli M., Bosurgi L., Tonlorenzi R., Clementi E., Bianchi M. E., Cossu G., Manfredi A. A., Brunelli S., Rovere-Querini P., Inflammatory and alternatively activated human macrophages attract vessel-associated stem cells, relying on separate HMGB1- and MMP-9-dependent pathways. Journal of Leukocyte Biology 2009 85 5 779 787 2-s2.0-65549151760 10.1189/jlb.0908579
51. Mantovani A., Sozzani S., Locati M., Allavena P., Sica A., Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends in Immunology 2002 23 11 549 555 2-s2.0-0036839143 10.1016/S1471-4906(02)02302-5 (Pubitemid 35223554)
52. Mantovani A., Biswas S. K., Galdiero M. R., Sica A., Locati M., Macrophage plasticity and polarization in tissue repair and remodelling. The Journal of Pathology 2013 229 2 176 185
53. Orimo A., Gupta P. B., Sgroi D. C., Arenzana-Seisdedos F., Delaunay T., Naeem R., Carey V. J., Richardson A. L., Weinberg R. A., Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005 121 3 335 348 2-s2.0-18844428327 10.1016/j.cell.2005.02.034 (Pubitemid 40692295)
54. Muller A., Homey B., Soto H., Involvement of chemokine receptors in breast cancer metastasis. Nature 2001 410 6824 50 56 (Pubitemid 32225831)
55. Mori T., Doi R., Koizumi M., CXCR4 antagonist inhibits stromal cell-derived factor 1-induced migration and invasion of human pancreatic cancer. Molecular Cancer Therapeutics 2004 3 1 29 37 (Pubitemid 39193676)
56. Chang C., Werb Z., The many faces of metalloproteases: cell growth, invasion, angiogenesis and metastasis. Trends in Cell Biology 2001 11 11 S37 S43 2-s2.0-0035500490 10.1016/S0962-8924(01)02122-5 (Pubitemid 33001442)
57. Egeblad M., Werb Z., New functions for the matrix metalloproteinases in cancer progression. Nature Reviews Cancer 2002 2 3 161 174 2-s2.0-0036512208 (Pubitemid 37328786)
58. Cao D., Polyak K., Halushka M. K., Nassar H., Kouprina N., Iacobuzio-Donahue C., Wu X., Sukumar S., Hicks J., De Marzo A., Argani P., Serial analysis of gene expression of lobular carcinoma in situ identifies down regulation of claudin 4 and overexpression of matrix metalloproteinase 9. Breast Cancer Research 2008 10 5, article R91 2-s2.0-59449099748 10.1186/bcr2189
59. Qin L., Liao L., Redmond A., Young L., Yuan Y., Chen H., O'Malley B. W., Xu J., The AIB1 oncogene promotes breast cancer metastasis by activation of PEA3-mediated matrix metalloproteinase 2 (MMP2) and MMP9 expression. Molecular and Cellular Biology 2008 28 19 5937 5950 2-s2.0-52649149854 10.1128/MCB.00579-08
60. Hagemann T., Robinson S. C., Schulz M., Trümper L., Balkwill F. R., Binder C., Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF- dependent up-regulation of matrix metalloproteases. Carcinogenesis 2004 25 8 1543 1549 2-s2.0-3342904989 10.1093/carcin/bgh146 (Pubitemid 39162720)
61. Poola I., DeWitty R. L., Marshalleck J. J., Bhatnagar R., Abraham J., Leffall L. D., Identification of MMP-1 as a putative breast cancer predictive marker by global gene expression analysis. Nature Medicine 2005 11 5 481 483 2-s2.0-18844421896 10.1038/nm1243 (Pubitemid 40685969)
62. Condeelis J., Pollard J. W., Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006 124 2 263 266 2-s2.0-31044433663 10.1016/j.cell.2006.01.007 (Pubitemid 43121975)
63. Fuentes-Panana E., Camorlinga-Ponce M., Maldonado-Bernal C., Infection, inflammation and gastric cancer. Salud Pública de México 2009 51 5 427 433
64. Hu M., Peluffo G., Chen H., Gelman R., Schnitt S., Polyak K., Role of COX-2 in epithelial-stromal cell interactions and progression of ductal carcinoma in situ of the breast. Proceedings of the National Academy of Sciences of the United States of America 2009 106 9 3372 3377 2-s2.0-62549099627 10.1073/pnas.0813306106
65. Agarwal S., Reddy G. V., Reddanna P., Eicosanoids in inflammation and cancer: the role of COX-2. Expert Review of Clinical Immunology 2009 5 2 145 165 2-s2.0-70349914077 10.1586/1744666X.5.2.145
66. Wang D., Dubois R. N., Eicosanoids and cancer. Nature Reviews Cancer 2010 10 3 181 193 2-s2.0-77649179672 10.1038/nrc2809
67. Cuzick J., Otto F., Baron J. A., Brown P. H., Burn J., Greenwald P., Jankowski J., La Vecchia C., Meyskens F., Senn H. J., Thun M., Aspirin and non-steroidal anti-inflammatory drugs for cancer prevention: an international consensus statement. The Lancet Oncology 2009 10 5 501 507 2-s2.0-65349152488 10.1016/S1470-2045(09)70035-X
68. Ferrandez A., Piazuelo E., Castells A., Aspirin and the prevention of colorectal cancer. Best Practice & Research Clinical Gastroenterology 2012 26 2 185 195
69. Debnath J., Brugge J. S., Modelling glandular epithelial cancers in three-dimensional cultures. Nature Reviews Cancer 2005 5 9 675 688 2-s2.0-25444443688 10.1038/nrc1695 (Pubitemid 41486361)
70. Muthuswamy S. K., Li D., Lelievre S., Bissell M. J., Brugge J. S., ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nature Cell Biology 2001 3 9 785 792 2-s2.0-0034854417 10.1038/ncb0901-785 (Pubitemid 32842683)
71. Partanen J. I., Nieminen A. I., Mäkelä T. P., Klefstrom J., Suppression of oncogenic properties of c-Myc by LKB1-controlled epithelial organization. Proceedings of the National Academy of Sciences of the United States of America 2007 104 37 14694 14699 2-s2.0-35548952703 10.1073/pnas.0704677104 (Pubitemid 350003205)
72. Fidler I. J., The pathogenesis of cancer metastasis: the "seed and soil" hypothesis revisited. Nature Reviews Cancer 2003 3 6 453 458 2-s2.0-0038481970 10.1038/nrc1098 (Pubitemid 37328849)
73. Tan W., Zhang W., Strasner A., Grivennikov S., Cheng J. Q., Hoffman R. M., Karin M., Tumour-infiltrating regulatory T cells stimulate mammary cancermetastasis through RANKL-RANK signalling. Nature 2011 470 7335 548 553 2-s2.0-79952193038 10.1038/nature09707
74. Kaplan R. N., Riba R. D., Zacharoulis S., Bramley A. H., Vincent L., Costa C., MacDonald D. D., Jin D. K., Shido K., Kerns S. A., Zhu Z., Hicklin D., Wu Y., Port J. L., Altorki N., Port E. R., Ruggero D., Shmelkov S. V., Jensen K. K., Rafii S., Lyden D., VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005 438 7069 820 827 2-s2.0-28644432204 10.1038/nature04186 (Pubitemid 41753060)
75. Shokeen M., Zheleznyak A., Wilson J. M., Molecular imaging of very late antigen-4 (alpha4beta1 integrin) in the premetastatic niche. Journal of Nuclear Medicine 2012 53 5 779 786