Inhibition of metastasis by HEXIM1 through effects on cell invasion and angiogenesis

Oncogene

Volumn 32, Issue 33, 2013, Pages 3829-3839

  Ketchart, W ^a   Smith, K M ^b   Krupka, T ^c   Wittmann, B M ^a,e   Hu, Y ^a   Rayman, P A ^d   Doughman, Y Q ^a   Albert, J M ^c   Bai, X ^a   Finke, J H ^d   Xu, Y ^b   Exner, A A ^c   Montano, M M ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CLEVELAND STATE UNIVERSITY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

^e METABOLON INC   (United States)

Author keywords

angiogenesis; breast cancer; HEXIM1; metastasis

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HEXAMETHYLENE BIS ACETAMIDE INDUCIBLE PROTEIN 1; LAMININ; LAMININ RECEPTOR; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST METASTASIS; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CELL TYPE; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FEMALE; FLOW CYTOMETRY; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MCF-7 CELLS; MICE; MICE, TRANSGENIC; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TISSUE ARRAY ANALYSIS; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

MUS; MUS MUSCULUS;

EID: 84882455491     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.405     Document Type: Article

References (62)

1. Gupta GP, Massagué J. Cancer metastasis: building a framework. Cell 2006; 127: 679-695.
2. Kerbel RS. Tumor angiogenesis. N Engl J Med. 2008; 358: 2039-2049.
3. Saltz LB, Clarke S, D?az-Rubio E, Scheithauer W, Figer A, Wong R et al. Bevacizumab in combination with oxaliplatin-based chemotherapy as first-line therapy in metastatic colorectal cancer: a randomized phase III study. J Clin Oncol 2008; 26: 2013-2019.
4. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005; 307: 58-62.
5. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005; 8: 299-309.
6. Relf M, LeJeune S, Scott PA, Fox S, Smith K, Leek R et al. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 1997; 57: 963-969.
7. Grépin R, Pagés G. Molecular mechanisms of resistance to tumour anti-angiogenic strategies. J Oncol 2010; 2010: 835680.
8. Ahn GO, Brown JM. Role of endothelial progenitors and other bone marrowderived cells in the development of the tumor vasculature. Angiogenesis 2009; 12: 159-164.
9. Wittmann BM, Wang N, Montano MM. Identification of a novel inhibitor of cell growth that is down-regulated by estrogens and decreased in breast tumors. Cancer Res 2003; 63: 5151-5158.
10. Ogba N, Doughman YQ, Chaplin LJ, Hu Y, Gargesha M, Watanabe M et al. HEXIM1 modulates vascular endothelial growth factor expression and function in breast epithelial cells and mammary gland. Oncogene 2010; 29: 3639-3649.
11. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res 2007; 13: 3207-3214.
12. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Physiol 2003; 163: 2113-2126.
13. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006; 66: 11238-11246.
14. Desai KV, Xiao N, Wang W, Gangi L, Greene J, Powell JI et al. Initiating oncogenic event determines gene-expression patterns of human breast cancer models. Proc Natl Acad Sci 2002; 99: 6967-6972.
15. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007; 8: R76.
16. Ogba N, Chaplin L, Doughman YQ, Fujinaga K, Montano MM. HEXIM1 regulates E2/ERa-mediated expression of Cyclin D1 in mammary cells via modulation of P-TEFb. Cancer Research 2008; 68: 7015-7024.
17. Guilbaud NF, Gas N, Dupont MA, Valette A. Effects of differentiation- inducing agents on maturation of human MCF-7 breast cancer cells. J Cell Physiol 1990; 145: 162-172.
18. Marks PA, Reuben R, Epner E, Breslow R, Cobb W, Bogden AE et al. Induction of murine erythroleukemia cells to differentiate: a model for the detection of new anti-tumor drugs. Antibiot Chemother 1978; 23: 33-41.
19. Reuben RC, Wife RL, Breslow R, Rifkind RA, Marks PA. A new group of potent inducers of differentiation in murine erythroleukemia cells. Proc Natl Acad Sci 1976; 73: 862-866.
20. Southard GL, Dunn RL, Garrett S. The drug delivery and biomaterial attributes of the ATRIGEL technology in the treatment of periodontal disease. Expert Opin Investig Drugs 1998; 7: 1483-1491.
21. Gad HA, El-Nabarawi MA, Abd El-Hady SS. Formulation and evaluation of PLA and PLGA in situ implants containing secnidazole and/or doxycycline for treatment of periodontitis. AAPS Pharm Sci Tech 2008; 9: 878-884.
22. Ravivarapu H, Moyer KL, Dunn RL. Sustained activity and release of leuprolide acetate from an in situ forming polymeric implant. AAPS Pharm Sci Tech 2000; 1: E1.
23. Young CW, Fanucchi MP, Declan Walsh T, Baltzer L, Yaldaei S, Stevens YW et al. Phase I trial and clinical pharmacological evaluation of hexamethylene bisacetamide administration by ten-day continuous intravenous infusion at twenty-eightday intervals. Cancer Res 1988; 48: 7304-7309.
24. Seagroves TN. The complexity of the HIF-1-dependent hypoxic response in breast cancer presents multiple avenues for therapeutic intervention. In: Lu Y, Mahato RI (eds) Pharmaceutical Perspectives of Cancer Therapeutics. Springer: New York, 2009, pp 521-558.
25. Wang J, Loberg R, Taichman RS. The pivotal role of CXCL12 (SDF-1)/CXCR4 axis in bone metastasis. Cancer Metastasis Rev 2006; 25: 573-587.
26. Dome B, Timar J, Ladanyi A, Paku S, Renyi-Vamos F, Klepetko W et al. Circulating endothelial cells, bone marrow-derived endothelial progenitor cells and proangiogenic hematopoietic cells in cancer: From biology to therapy. Crit Rev Oncol Hematol 2009; 69: 108-124.
27. Gao D, Mittal V. The role of bone-marrow-derived cells in tumor growth, metastasis initiation and progression. Trends Mol Med 2009; 15: 333-343.
28. Chan DA, Kawahara TL, Sutphin PD, Chang HY, Chi JT, Giaccia AJ. Tumor vasculature is regulated by PHD2-mediated angiogenesis and bone marrow-derived cell recruitment. Cancer Cell 2009; 15: 527-538.
29. Udagawa T, Puder M, Wood M, Schaefer BC, D'Amato RJ. Analysis of tumorassociated stromal cells using SCID GFP transgenic mice: contribution of local and bone marrow-derived host cells. FASEB J. 2006; 20: 95-102.
30. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 2006; 8: 1369-1375.
31. Shojaei F, Wu X, Malik SK, Zhong C, Baldwin ME, Schanz S et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol 2007; 8: 911-920.
32. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004; 6: 409-421.
33. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol 2006; 7: 131-142.
34. Castronovo V. Laminin receptors and laminin binding proteins during tumor invasion and metastasis. Invasion Metastasis 1993; 13: 1-30.
35. Givant-Horwitz V, Davidson B, Reich R. Laminin-induced signaling in tumor cells: the role of the M(r) 67,000 laminin receptor. Cancer Res 2004; 64: 3572-3579.
36. Montuori N, Sobel ME. The 67-kDa laminin receptor and tumor progression. Curr Top Microbiol Immunol 1996; 213: 205-214.
37. Ardini E, Sporchia B, Pollegioni L, Modugno M, Ghirelli C, Castiglioni F et al. Identification of a novel function for 67-kDa laminin receptor: Increase in laminin degradation rate and release of motility fragment. Cancer Res 2002; 62: 1321-1325.
38. Taylor MA, Lee YH, Schiemann WP. Role of TGF-beta and the tumor microenvironment during mammary tumorigenesis. Gene Expr 2011; 15: 117-132.
39. de Graauw M, van Miltenburg MH, Schmidt MK, Pont C, Lalai R, Kartopawiro J et al. Annexin A1 regulates TGF-beta signaling and promotes metastasis formation of basal-like breast cancer cells. Proc Natl Acad Sci USA. 2010; 107: 6340-6345.
40. Schietke R, Warnecke C, Wacker I, Schodel J, Mole DR, Campean V et al. The lysyl oxidases LOX and LOXL2 are necessary and sufficient to repress E-cadherin in hypoxia: insights into cellular transformation processes mediated by HIF-1. J Biol Chem 2010; 285: 6658-6669.
41. Barker HE, Chang J, Cox TR, Lang G, Bird D, Nicolau M et al. LOXL2-mediated matrix remodeling in metastasis and mammary gland involution. Cancer Res 2011; 71: 1561-1572.
42. Nannuru KC, Futakuchi M, Varney ML, Vincent TM, Marcusson EG, Singh RK. Matrix metalloproteinase (MMP)-13 regulates mammary tumor-induced osteolysis by activating MMP9 and transforming growth factor-beta signaling at the tumorbone interface. Cancer Res 2010; 70: 3494-3504.
43. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003; 3: 721-732.
44. Liao D, Corle C, Seagroves TN, Johnson RS. Hypoxia-inducible factor-1alpha is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res. 2007; 67: 563-572.
45. Lee K, Qian DZ, Rey S, Wei H, Liu JO, Semenza GL. Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells. Proc Natl Acad Sci 2009; 106: 2353-2358.
46. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004; 10: 858-864.
47. Hoenig MR, Bianchi C, Sellke FW. Hypoxia inducible factor-1 alpha, endothelial progenitor cells, monocytes, cardiovascular risk, wound healing, cobalt and hydralazine: a unifying hypothesis. Curr Drug Targets 2008; 9: 422-435.
48. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegué E et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008; 13: 206-220.
49. Jiang M, Wang B, Wang C, He B, Fan H, Shao Q et al. In vivo enhancement of angiogenesis by adenoviral transfer of HIF-1alpha-modified endothelial progenitor cells (Ad-HIF-1alpha-modified EPC for angiogenesis). Int J Biochem Cell Biol 2008; 40: 2284-2289.
50. Peinado H, Lavotshkin S, Lyden D. The secreted factors responsible for premetastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 2011; 21: 139-146.
51. Gu YC, Kortesmaa J, Tryggvason K, Persson J, Ekblom P, Jacobsen SE et al. Laminin isoform-specific promotion of adhesion and migration of human bone marrow progenitor cells. Blood 2003; 101: 877-885.
52. Siler U, Seiffert M, Puch S, Richards A, Torok-Storb B, Müller CA et al. Characterization and functional analysis of laminin isoforms in human bone marrow. Blood 2000; 96: 4194-4203.
53. Selleri C, Ragno P, Ricci P, Visconte V, Scarpato N, Carriero MV et al. The metastasis- associated 67-kDa laminin receptor is involved in G-CSF-induced hematopoietic stem cell mobilization. Blood 2006; 108: 2476-2484.
54. Viacava P, Naccarato AG, Collecchi P, Menard S, Castronovo V, Bevilacqua G. The spectrum of 67-kD laminin receptor expression in breast carcinoma progression. J Pathol 1997; 182: 36-44.
55. Hinek A. Nature and the multiple functions of the 67-kD elastin-/laminin binding protein. Cell Adhes Commun 1994; 2: 185-193.
56. Magnifico A, Tagliabue E, ButòS, Ardini E, Castronovo V, Colnaghi MI et al. Peptide G, containing the binding site of the 67 kDa laminin receptor, increases and stabilizes laminin binding to cancer cells. J Biol Chem 1996; 271: 31179-31184.
57. Buto S, Tagliabue E, Ardini E, Magnifico A, Ghirelli C, van den Brule F et al. Formation of the 67-kDa laminin receptor by acylation of the precursor. J Cell Biochem 1998; 69: 244-251.
58. Westwell AD, Stevens MG. Hitting the chemotherapy jackpot: strategy, productivity and chemistry. Drug Discov Today. 2004; 9: 625-627.
59. Ketchart W, Ogba N, Kresak A, Albert JM, Pink JJ, Montano MM. HEXIM1 is a critical determinant of the response to tamoxifen. Oncogene 2011; 30: 3563-3569.
60. Smith KM, Ketchart W, Zhou X, Montano MM, Xu Y. Determination of hexamethylene bisacetamide, an antineoplastic compound, in mouse and human plasma by LC-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 2011; 879: 2206-2212.
61. Montano MM, Ekena K, Delage-Mourroux R, Chang W, Martini P, Katzenellenbogen BS. An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens. Proc Natl Acad Sci USA 1999; 96: 6947-6952.
62. Wittmann BM, Fujinaga K, Deng H, Ogba N, Montano MM. The breast cell growth inhibitor, estrogen down regulated gene 1, modulates a novel functional interaction between estrogen receptor alpha and transcriptional elongation factor cyclin T1. Oncogene 2005; 24: 5576-5588.