Homeobox D10 induces phenotypic reversion of breast tumor cells in a three-dimensional culture model

Cancer Research

Volumn 65, Issue 16, 2005, Pages 7177-7185

  Carrio, Meritxell ^a   Arderiu, Gemma ^a   Myers, Connie ^b   Boudreau, Nancy J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA3 INTEGRIN; HOMEODOMAIN PROTEIN; HOMEODOMAIN PROTEIN D10; LAMININ; UNCLASSIFIED DRUG;

ARTICLE; BASEMENT MEMBRANE; BREAST EPITHELIUM; BREAST TUMOR; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE MODEL; ENDOMETRIUM TUMOR; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENE TRANSFER; HOX GENE; HUMAN; HUMAN CELL; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REGULATOR GENE; RETROVIRUS; THREE DIMENSIONAL IMAGING; XENOGRAFT;

ANIMALS; BASEMENT MEMBRANE; BREAST NEOPLASMS; CELL COMMUNICATION; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENDOMETRIAL NEOPLASMS; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FEMALE; GENES, TUMOR SUPPRESSOR; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; LAMININ; MICE; MICE, NUDE; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 23844537411     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-1717     Document Type: Article

References (57)

1. Botas J. Control of morphogenesis and differentiation by HOM/Hox genes. Curr Opin Cell Biol 1993;5:1015-22.
2. Myers C, Charboneau A, Boudreau N. Homeobox B3 promotes capillary morphogenesis and angiogenesis. J Cell Biol 2000;148:343-51.
3. Myers C, Charboneau A, Cheung I, Hanks D, Boudreau N. Sustained expression of homeobox D10 inhibits angiogenesis. Am J Pathol 2002;161:2099-109.
4. Boudreau N, Bissell MJ. Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr Opin Cell Biol 1998;10:640-6.
5. Boudreau N, Andrews C, Srebrow A, Ravanpay A, Cheresh DA. Induction of the angiogenic phenotype by Hox D3. J Cell Biol 1997;139:257-64.
6. Edelman GM, Jones FS. Outside and downstream of the homeobox. J Biol Chem 1993;268:20683-6.
7. Srebrow A, Friedmann Y, Ravanpay A, Daniel CW, Bissell MJ. Expression of Hoxa-1 and Hoxb-7 is regulated by extracellular matrix-dependent signals in mammary epithelial cells. J Cell Biochem 1998;69:377-91.
8. Leroy P, Berto F, Bourget I, Rossi B. Down-regulation of Hox A7 is required for cell adhesion and migration on fibronectin during early HL-60 monocytic differentiation. J Leukoc Biol 2004;75:680-8.
9. Care A, Silvani A, Meccia E, et al. HOXB7 constitutively activates basic fibroblast growth factor in melanomas. Mol Cell Biol 1996;16:4842-51.
10. Peverali FA, D'Esposito M, Acampora D, et al. Expression of HOX homeogenes in human neuroblastoma cell culture lines. Differentiation 1990;45:61-9.
11. Cillo C, Barba P, Freschi G, Bucciarelli G, Magli MC, Boncinelli E. HOX gene expression in normal and neoplastic human kidney. Int J Cancer 1992;51:892-7.
12. Aberdam D, Negreanu V, Sachs L, Blatt C. The oncogenic potential of an activated Hox-2.4 homeobox gene in mouse fibroblasts. Mol Cell Biol 1991;11:554-7.
13. Friedmann Y, Daniel CA, Strickland P, Daniel CW. Hox genes in normal and neoplastic mouse mammary gland. Cancer Res 1994;54:5981-5.
14. De Vita G, Barba P, Odartchenko N, et al. Expression of homeobox-containing genes in primary and metastatic colorectal cancer. Eur J Cancer 1993;29A:887-93.
15. Tiberio C, Barba P, Magli MC, et al. HOX gene expression in human small-cell lung cancers xenografted into nude mice. Int J Cancer 1994;58:608-15.
16. Osborne J, Hu C, Hawley C, Underwood LJ, O'Brien TJ, Baker W. Expression of HOXD10 gene in normal endometrium and endometrial adenocarcinoma. J Soc Gynecol Investig 1998;5:277-80.
17. Raman V, Martensen SA, Reisman D, et al. Compromised HOXA5 function can limit p53 expression in human breast tumours. Nature 2000;405:974-8.
18. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer 2001;1:46-54.
19. Lewis MT. Homeobox genes in mammary gland development and neoplasia. Breast Cancer Res 2000;2: 158-69.
20. Chen H, Chung S, Sukumar S. HOXA5-induced apoptosis in breast cancer cells is mediated by caspases 2 and 8. Mol Cell Biol 2004;24:924-35.
21. Chariot A, Castronovo V. Detection of HOXA1 expression in human breast cancer. Biochem Biophys Res Commun 1996;222:292-7.
22. Zhang X, Zhu T, Chen Y, Mertani HC, Lee KO, Lobie PE. Human growth hormone-regulated HOXA1 is a human mammary epithelial oncogene. J Biol Chem 2003;278:7580-90.
23. Morini M, Mottolese M, Ferrari N, et al. The α3β1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. Int J Cancer 2000;87:336-42.
24. Hotary KB, Allen ED, Brooks PC, Datta NS, Long MW, Weiss SJ. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 2003;114:33-45.
25. Fisher JL, Field CL, Zhou H, Harris TL, Henderson MA, Choong PF. Urokinase plasminogen activator system gene expression is increased in human breast carcinoma and its bone metastases-a comparison of normal breast tissue, non-invasive and invasive carcinoma and osseous metastases. Breast Cancer Res Treat 2000;61:1-12.
26. Tawil NJ, Gowri V, Djoneidi M, Nip J, Carbonetto S, Brodt P. Integrin α3β1 can promote adhesion and spreading of metastatic breast carcinoma cells on the lymph node stroma. Int J Cancer 1996;66:703-10.
27. Grondahl-Hansen J, Christensen IJ, Briand P, et al. Plasminogen activator inhibitor type 1 in cytosolic tumor extracts predicts prognosis in low-risk breast cancer patients. Clin Cancer Res 1997;3:233-9.
28. Weaver VM, Petersen OW, Wang F, et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997;137:231-45.
29. Boudreau N, Werb Z, Bissell MJ. Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci U S A 1996;93:3509-13.
30. Carpenter EM, Goddard JM, Davis AP, Nguyen TP, Capecchi MR. Targeted disruption of Hoxd-10 affects mouse hind limb development. Development 1997;124: 4505-14.
31. Chu MC, Selam FB, Taylor HS. HOXA10 Regulates p53 Expression and matrigel invasion in human breast cancer cells. Cancer Biol Ther 2004;3:568-72.
32. Bromleigh VC, Freedman LP. p21 is a transcriptional target of HOXA10 in differentiating myelomonocytic cells. Genes Dev 2000;14:2581-6.
33. Cantile M, Pettinato G, Procino A, Feliciello I, Cindolo L, Cillo C. In vivo expression of the whole HOX gene network in human breast cancer. Eur J Cancer 2003;39:257-64.
34. Makiyama K, Hamada J, Takada M, et al. Aberrant expression of HOX genes in human invasive breast carcinoma. Oncol Rep 2005;13:673-9.
35. Koukoulis GK, Virtanen I, Korhonen M, Laitinen L, Quaranta V, Gould VE. Immunohistochemical localization of integrins in the normal, hyperplastic, and neoplastic breast. Correlations with their functions as receptors and cell adhesion molecules. Am J Pathol 1991;139:787-99.
36. Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997;277:225-8.
37. Kato T, Katabami K, Takatsuki H, et al. Characterization of the promoter for the mouse α3 integrin gene. Eur J Biochem 2002;269:4524-32.
38. Ghosh S, Brown R, Jones JC, Ellerbroek SM, Stack MS. Urinary-type plasminogen activator (uPA) expression and uPA receptor localization are regulated by α3β1 integrin in oral keratinocytes. J Biol Chem 2000;275: 23869-76.
39. Wei Y, Eble JA, Wang Z, Kreidberg JA, Chapman HA. Urokinase receptors promote β1 integrin function through interactions with integrin α3β1. Mol Biol Cell 2001;12:2975-86.
40. Wang F, Hansen RK, Radisky D, et al. Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. J Natl Cancer Inst 2002;94:1494-503.
41. Weaver VM, Lelievre S, Lakins JN, et al. β4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2002;2:205-16.
42. Manohar A, Shome SG, Lamar J, et al. α3β1 integrin promotes keratinocyte cell survival through activation of a MEK/ERK signaling pathway. J Cell Sci 2004;117: 4043-54.
43. Abate-Shen C. Deregulated homeobox gene expression in cancer: cause or consequence? Nat Rev Cancer 2002;2:777-85.
44. Aubin J, Chailler P, Menard D, Jeannotte L. Loss of Hoxa5 gene function in mice perturbs intestinal maturation. Am J Physiol 1999;277:C965-73.
45. Aubin J, Dery U, Lemieux M, Chailler P, Jeannotte L. Stomach regional specification requires Hoxa5-driven mesenchymal-epithelial signaling. Development 2002;129:4075-87.
46. Kirshner J, Chen CJ, Liu P, Huang J, Shively JE. CEACAM1-4S, a cell-cell adhesion molecule, mediates apoptosis and reverts mammary carcinoma cells to a normal morphogenic phenotype in a 3D culture. Proc Natl Acad Sci U S A 2003;100:521-6.
47. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002;111: 29-40.
48. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001;3:785-92.
49. Wang F, Weaver VM, Petersen OW, et al. Reciprocal interactions between β1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc Natl Acad Sci U S A 1998;95:14821-6.
50. Boudreau N, Sympson CJ, Werb Z, Bissell MJ. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 1995;267:891-3.
51. Liu H, Radisky DC, Wang F, Bissell MJ. Polarity and proliferation are controlled by distinct signaling pathways downstream of PI3-kinase in breast epithelial tumor cells. J Cell Biol 2004;164:603-12.
52. Miyazaki YJ, Hamada J, Tada M, et al. HOXD3 enhances motility and invasiveness through the TGF-β-dependent and -independent pathways in A549 cells. Oncogene 2002;21:798-808.
53. Okubo Y, Hamada J, Takahashi Y, et al. Transduction of HOXD3-antisense into human melanoma cells results in decreased invasive and motile activities. Clin Exp Metastasis 2002;19:503-11.
54. Boudreau NJ, Varner JA. The homeobox transcription factor Hox D3 promotes integrin α5β1 expression and function during angiogenesis. J Biol Chem 2004;279: 4862-8.
55. Zhong J, Eliceiri B, Stupack D, et al. Neovascularization of ischemic tissues by gene delivery of the extracellular matrix protein Del-1. J Clin Invest 2003;112:30-41.
56. van Oostveen J, Bijl J, Raaphorst F, Walboomers J, Meijer C. The role of homeobox genes in normal hematopoiesis and hematological malignancies. Leukemia 1999;13:1675-90.
57. Sauvageau G, Lansdorp PM, Eaves CJ, et al. Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proc Natl Acad Sci U S A 1994;91:12223-7.