Deletion of the BMP receptor BMPR1a impairs mammary tumor formation and metastasis

Oncotarget

Volumn 6, Issue 26, 2015, Pages 22890-22904

  Pickup, Michael W ^a   Hover, Laura D ^b   Guo, Yan ^c   Gorska, Agnieszka E ^c   Chytil, Anna ^c   Novitskiy, Sergey V ^c   Moses, Harold L ^c   Owens, Philip ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

BMP; BMPR1a; Breast cancer; EMT; Metastasis

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; CRE RECOMBINASE; CYTOKERATIN 5; VIMENTIN; BMPR1A PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST TUMOR; CANCER CLASSIFICATION; CANCER GROWTH; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE DELETION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; METASTASIS POTENTIAL; MICROARRAY ANALYSIS; MMTV PYMT GENE; MOUSE; NONHUMAN; ONCOGENE; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR INVASION; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; METABOLISM; METASTASIS; PATHOLOGY;

ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BREAST NEOPLASMS; HUMANS; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; NEOPLASM METASTASIS; SIGNAL TRANSDUCTION;

EID: 84941247995     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4413     Document Type: Article

References (49)

1. Urist MR. Bone: formation by autoinduction. Science. 1965; 150(3698):893-899.
2. Miyazono K, Kamiya Y and Morikawa M. Bone morphogenetic protein receptors and signal transduction. J Biochem. 2010; 147:35-51.
3. Chen D, Zhao M and Mundy GR. Bone morphogenetic proteins. Growth Factors. 2004; 22:233-241.
4. Singh A and Morris RJ. The Yin and Yang of bone morphogenetic proteins in cancer. Cytokine & growth factor reviews. 2010; 21:299-313.
5. Owens P, Pickup MW, Novitskiy SV, Chytil A, Gorska AE, Aakre ME, West J and Moses HL. Disruption of bone morphogenetic protein receptor 2 (BMPR2) in mammary tumors promotes metastases through cell autonomous and paracrine mediators. Proc Natl Acad Sci U S A. 2012; 109:2814-2819.
6. Howe JR, Bair JL, Sayed MG, Anderson ME, Mitros FA, Petersen GM, Velculescu VE, Traverso G and Vogelstein B. Germline mutations of the gene encoding bone morphogenetic protein receptor 1A in juvenile polyposis. Nat Genet. 2001; 28:184-187.
7. Kobielak K, Pasolli HA, Alonso L, Polak L and Fuchs E. Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J Cell Biol. 2003; 163:609-623.
8. Andl T, Ahn K, Kairo A, Chu EY, Wine-Lee L, Reddy ST, Croft NJ, Cebra-Thomas JA, Metzger D, Chambon P, Lyons KM, Mishina Y, Seykora JT, Crenshaw EB, 3rd and Millar SE. Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development. 2004; 131:2257-2268.
9. Ming Kwan K, Li AG, Wang XJ, Wurst W and Behringer RR. Essential roles of BMPR-IA signaling in differentiation and growth of hair follicles and in skin tumorigenesis. Genesis. 2004; 39:10-25.
10. Yuhki M, Yamada M, Kawano M, Iwasato T, Itohara S, Yoshida H, Ogawa M and Mishina Y. BMPR1A signaling is necessary for hair follicle cycling and hair shaft differentiation in mice. Development. 2004; 131:1825-1833.
11. Soda H, Raymond E, Sharma S, Lawrence R, Cerna C, Gomez L, Timony GA, Von Hoff DD and Izbicka E. Antiproliferative effects of recombinant human bone morphogenetic protein-2 on human tumor colony-forming units. Anticancer Drugs. 1998; 9:327-331.
12. Ghosh-Choudhury N, Ghosh-Choudhury G, Celeste A, Ghosh PM, Moyer M, Abboud SL and Kreisberg J. Bone morphogenetic protein-2 induces cyclin kinase inhibitor p21 and hypophosphorylation of retinoblastoma protein in estradiol-treated MCF-7 human breast cancer cells. Biochim Biophys Acta. 2000; 1497:186-196.
13. Pouliot F and Labrie C. Role of Smad1 and Smad4 proteins in the induction of p21WAF1,Cip1 during bone morphogenetic protein-induced growth arrest in human breast cancer cells. J Endocrinol. 2002; 172:187-198.
14. Kulessa H, Turk G and Hogan BL. Inhibition of Bmp signaling affects growth and differentiation in the anagen hair follicle. The EMBO journal. 2000; 19:6664-6674.
15. Gao H, Chakraborty G, Lee-Lim AP, Mo Q, Decker M, Vonica A, Shen R, Brogi E, Brivanlou AH and Giancotti FG. The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites. Cell. 2012; 150:764-779.
16. Ketolainen JM, Alarmo EL, Tuominen VJ and Kallioniemi A. Parallel inhibition of cell growth and induction of cell migration and invasion in breast cancer cells by bone morphogenetic protein 4. Breast Cancer Res Treat. 2010; 124:377-386.
17. Katsuno Y, Hanyu A, Kanda H, Ishikawa Y, Akiyama F, Iwase T, Ogata E, Ehata S, Miyazono K and Imamura T. Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene. 2008; 27:6322-6333.
18. Morrissey C, Brown LG, Pitts TE, Vessella RL and Corey E. Bone morphogenetic protein 7 is expressed in prostate cancer metastases and its effects on prostate tumor cells depend on cell phenotype and the tumor microenvironment. Neoplasia. 2010; 12:192-205.
19. Langenfeld E, Hong CC, Lanke G and Langenfeld J. Bone morphogenetic protein type I receptor antagonists decrease growth and induce cell death of lung cancer cell lines. PLoS One. 2013; 8:e61256.
20. Balboni AL, Hutchinson JA, DeCastro AJ, Cherukuri P, Liby K, Sporn MB, Schwartz GN, Wells WA, Sempere LF, Yu PB and DiRenzo J. DeltaNp63alpha-mediated activation of bone morphogenetic protein signaling governs stem cell activity and plasticity in normal and malignant mammary epithelial cells. Cancer Res. 2013; 73:1020-1030.
21. Nishimori H, Ehata S, Suzuki HI, Katsuno Y and Miyazono K. Prostate cancer cells and bone stromal cells mutually interact with each other through bone morphogenetic protein-mediated signals. J Biol Chem. 2012; 287:20037-20046.
22. Buijs JT, van der Horst G, van den Hoogen C, Cheung H, de Rooij B, Kroon J, Petersen M, van Overveld PG, Pelger RC and van der Pluijm G. The BMP2/7 heterodimer inhibits the human breast cancer stem cell subpopulation and bone metastases formation. Oncogene. 2012; 31:2164-2174.
23. Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S, Pai SK, Liu W, Fukuda K, Chambers C, Wilber A and Watabe K. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. The Journal of experimental medicine. 2011; 208:2641-2655.
24. Singh A, Sweeney MF, Yu M, Burger A, Greninger P, Benes C, Haber DA and Settleman J. TAK1 inhibition promotes apoptosis in KRAS-dependent colon cancers. Cell. 2012; 148:639-650.
25. Ehata S, Yokoyama Y, Takahashi K and Miyazono K. Bidirectional roles of bone morphogenetic proteins in cancer: Another molecular Jekyll and Hyde? Pathol Int. 2013; 63:287-296.
26. Alarmo EL and Kallioniemi A. Bone morphogenetic proteins in breast cancer: dual role in tumourigenesis? Endocr Relat Cancer. 2010; 17:R123-139.
27. Guy CT, Cardiff RD and Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol. 1992; 12:954-961.
28. Wagner KU, Wall RJ, St-Onge L, Gruss P, Wynshaw-Boris A, Garrett L, Li M, Furth PA and Hennighausen L. Cremediated gene deletion in the mammary gland. Nucleic acids research. 1997; 25:4323-4330.
29. Mishina Y, Hanks MC, Miura S, Tallquist MD and Behringer RR. Generation of Bmpr/Alk3 conditional knockout mice. Genesis. 2002; 32:69-72.
30. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, Bell G, Guo W, Rubin J, Richardson AL and Weinberg RA. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell. 2011; 145:926-940.
31. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, Rasmussen KE, Jones LP, Assefnia S, Chandrasekharan S, Backlund MG, Yin Y, Khramtsov AI, Bastein R, Quackenbush J, Glazer RI, et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome biology. 2007; 8:R76.
32. Nielsen TO, Parker JS, Leung S, Voduc D, Ebbert M, Vickery T, Davies SR, Snider J, Stijleman IJ, Reed J, Cheang MC, Mardis ER, Perou CM, Bernard PS and Ellis MJ. A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010; 16:5222-5232.
33. Owens P, Pickup MW, Novitskiy SV, Giltnane JM, Gorska AE, Hopkins CR, Hong CC and Moses HL. Inhibition of BMP signaling suppresses metastasis in mammary cancer. Oncogene. 2014.
34. Comprehensive molecular portraits of human breast tumours. Nature. 2012; 490:61-70.
35. Kinzler KW and Vogelstein B. Landscaping the cancer terrain. Science. 1998; 280:1036-1037.
36. Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, ten Dijke P and van der Pluijm G. TGF-beta and BMP7 interactions in tumour progression and bone metastasis. Clin Exp Metastasis. 2007; 24:609-617.
37. Forrester E, Chytil A, Bierie B, Aakre M, Gorska AE, Sharif-Afshar AR, Muller WJ and Moses HL. Effect of conditional knockout of the type II TGF-beta receptor gene in mammary epithelia on mammary gland development and polyomavirus middle T antigen induced tumor formation and metastasis. Cancer Res. 2005; 65:2296-2302.
38. Drasin DJ, Guarnieri AL, Neelakantan D, Kim J, Cabrera JH, Wang CA, Zaberezhnyy V, Gasparini P, Cascione L, Huebner K, Tan AC and Ford HL. TWIST1-Induced miR-424 Reversibly Drives Mesenchymal Programming while Inhibiting Tumor Initiation. Cancer Res. 2015; 75:1908-1921.
39. Ruscetti M, Quach B, Dadashian EL, Mulholland DJ and Wu H. Tracking and Functional Characterization of Epithelial-Mesenchymal Transition and Mesenchymal Tumor Cells During Prostate Cancer Metastasis. Cancer Res. 2015.
40. Chen D, Sun Y, Yuan Y, Han Z, Zhang P, Zhang J, You MJ, Teruya-Feldstein J, Wang M, Gupta S, Hung MC, Liang H and Ma L. miR-100 induces epithelial-mesenchymal transition but suppresses tumorigenesis, migration and invasion. PLoS Genet. 2014; 10:e1004177.
41. Lee YC, Cheng CJ, Bilen MA, Lu JF, Satcher RL, Yu-Lee LY, Gallick GE, Maity SN and Lin SH. BMP4 promotes prostate tumor growth in bone through osteogenesis. Cancer Res. 2011; 71:5194-5203.
42. Muzumdar MD, Tasic B, Miyamichi K, Li L and Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007; 45:593-605.
43. Owens P, Engelking E, Han G, Haeger SM and Wang XJ. Epidermal Smad4 deletion results in aberrant wound healing. Am J Pathol. 2010; 176:122-133.
44. Diboun I, Wernisch L, Orengo CA and Koltzenburg M. Microarray analysis after RNA amplification can detect pronounced differences in gene expression using limma. BMC genomics. 2006; 7:252.
45. Zhao S, Guo Y, Sheng Q and Shyr Y. Advanced heat map and clustering analysis using heatmap3. Biomed Res Int. 2014; 2014:986048.
46. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES and Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005; 102:15545-15550.
47. Russell AJ, Fincher EF, Millman L, Smith R, Vela V, Waterman EA, Dey CN, Guide S, Weaver VM and Marinkovich MP. Alpha 6 beta 4 integrin regulates keratinocyte chemotaxis through differential GTPase activation and antagonism of alpha 3 beta 1 integrin. Journal of cell science. 2003; 116:3543-3556.
48. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, Sander C and Schultz N. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012; 2:401-404.
49. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q and Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat. 2010; 123:725-731.