Expression of Bone Morphogenetic Protein-10 (BMP10) in human urothelial cancer of the bladder and its effects on the aggressiveness of bladder cancer cells in vitro

Anticancer Research

Volumn 33, Issue 5, 2013, Pages 1917-1925

  Zhang, Ning ^a   Ye, Lin ^b   Wu, Liyang ^a   Deng, Xiaohu ^c   Yang, Yong ^a   Jiang, Wen G ^b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c Department of Surgery   (China)

Author keywords

BMP10; Growth; Motility and adhesion; T24 cells; Urothelial cancer of bladder

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 10; UNCLASSIFIED DRUG;

AGGRESSIVENESS; ARTICLE; BLADDER CANCER; CANCER CELL; CELL MOTILITY; CONTROLLED STUDY; GENETIC MANIPULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCHEMISTRY; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROMA CELL;

BMP10; GROWTH; MOTILITY AND ADHESION; T24 CELLS; UROTHELIAL CANCER OF BLADDER;

APOPTOSIS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; IMMUNOENZYME TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; URINARY BLADDER; URINARY BLADDER NEOPLASMS;

EID: 84878196248     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Parkin DM: The global burden of urinary bladder cancer. Scand J Urol Nephrol Suppl: 12-20, 2008.
2. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T and Thun MJ: Cancer statistics, 2008. CA Cancer J Clin 58: 71-96, 2008. (Pubitemid 351521864)
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin 61: 69-90, 2011.
4. Epstein JI, Amin MB, Reuter VR and Mostofi FK: The World Health Organization/International Society of Urological Pathology consensus classification of urothelial (transitional cell) neoplasms of the urinary bladder. Bladder Consensus Conference Committee. Am J Surg Pathol 22: 1435-1448, 1998. (Pubitemid 28550639)
5. Oyasu R: World Health Organization and International Society of Urological Pathology classification and two-number grading system of bladder tumors. Cancer 88: 1509-1512, 2000.
6. Raghavan D, Shipley WU, Garnick MB, Russell PJ and Richie JP: Biology and management of bladder cancer. N Engl J Med 322: 1129-1138, 1990. (Pubitemid 20149531)
7. Stein JP, Lieskovsky G, Cote R, Groshen S, Feng AC, Boyd S, Skinner E, Bochner B, Thangathurai D, Mikhail M, Raghavan D and Skinner DG: Radical cystectomy in the treatment of invasive bladder cancer: long-term results in 1,054 patients. J Clin Oncol 19: 666-675, 2001. (Pubitemid 32120143)
8. Dalbagni G, Genega E, Hashibe M, Zhang ZF, Russo P, Herr H and Reuter V: Cystectomy for bladder cancer: A contemporary series. J Urol 165: 1111-1116, 2001. (Pubitemid 32210214)
9. Herr HW and Donat SM: Outcome of patients with grossly node positive bladder cancer after pelvic lymph node dissection and radical cystectomy. J Urol 165: 62-64, 2001.
10. Shariat SF, Kim JH, Andrews B, Kattan MW, Wheeler TM, Kim IY, Lerner SP and Slawin KM: Preoperative plasma levels of transforming growth factor beta(1) strongly predict clinical outcome in patients with bladder carcinoma. Cancer 92: 2985-2992, 2001. (Pubitemid 33136192)
11. Shariat SF, Kim J, Nguyen C, Wheeler TM, Lerner SP and Slawin KM: Correlation of preoperative levels of IGF-I and IGFBP-3 with pathologic parameters and clinical outcome in patients with bladder cancer. Urology 61: 359-364, 2003. (Pubitemid 36206533)
12. Andrews B, Shariat SF, Kim JH, Wheeler TM, Slawin KM and Lerner SP: Preoperative plasma levels of interleukin-6 and its soluble receptor predict disease recurrence and survival of patients with bladder cancer. J Urol 167: 1475-1481, 2002. (Pubitemid 34132135)
13. Helmy A, Hammam OA, El Lithy TR and El Deen Wishahi MM: The role of TGF-beta-1 protein and TGF-beta-R-1 receptor in immune escape mechanism in bladder cancer. MedGenMed 9: 34, 2007.
14. Eissa S, Salem AM, Zohny SF and Hegazy MG: The diagnostic efficacy of urinary TGF-beta1 and VEGF in bladder cancer: comparison with voided urine cytology. Cancer Biomark 3: 275-285, 2007. (Pubitemid 350187030)
15. Urist MR: Bone: formation by autoinduction. Science 150: 893-899, 1965.
16. Sampath TK, Coughlin JE, Whetstone RM, Banach D, Corbett C, Ridge RJ, Ozkaynak E, Oppermann H and Rueger DC: Bovine osteogenic protein is composed of dimers of OP-1 and BMP-2A, two members of the transforming growth factor-beta superfamily. J Biol Chem 265: 13198-13205, 1990.
17. Ozkaynak E, Rueger DC, Drier EA, Corbett C, Ridge RJ, Sampath TK and Oppermann H: OP-1 cDNA encodes an osteogenic protein in the TGF-beta family. EMBO J 9: 2085-2093, 1990.
18. Celeste AJ, Iannazzi JA, Taylor RC, Hewick RM, Rosen V, Wang EA and Wozney JM: Identification of transforming growth factor beta family members present in bone-inductive protein purified from bovine bone. Proc Natl Acad Sci USA 87:9843-9847, 1990. (Pubitemid 120016540)
19. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM and Wang EA: Novel regulators of bone formation: molecular clones and activities. Science 242: 1528-1534, 1988. (Pubitemid 19023695)
20. Wang EA, Rosen V, Cordes P, Hewick RM, Kriz MJ, Luxenberg DP, Sibley BS and Wozney JM: Purification and characterization of other distinct bone-inducing factors. Proc Natl Acad Sci USA 85: 9484-9488, 1988. (Pubitemid 19027155)
21. Yang S, Zhong C, Frenkel B, Reddi AH and Roy-Burman P: Diverse biological effect and Smad signaling of bone morphogenetic protein 7 in prostate tumor cells. Cancer Res 65:5769-5777, 2005. (Pubitemid 40911180)
22. Ide H, Katoh M, Sasaki H, Yoshida T, Aoki K, Nawa Y, Osada Y, Sugimura T and Terada M: Cloning of human bone morphogenetic protein type IB receptor (BMPR-IB) and its expression in prostate cancer in comparison with other BMPRs. Oncogene 14: 1377-1382, 1997. (Pubitemid 27151995)
23. Singh A and Morris RJ: The Yin and Yang of bone morphogenetic proteins in cancer. Cytokine Growth Factor Rev 21: 299-313, 2010.
24. Arnold SF, Tims E and McGrath BE: Identification of bone morphogenetic proteins and their receptors in human breast cancer cell lines: importance of BMP2. Cytokine 11: 1031-1037, 1999. (Pubitemid 30045342)
25. 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 1497: 186-196, 2000. (Pubitemid 30618830)
26. Johnsen IK, Kappler R, Auernhammer CJ and Beuschlein F: Bone morphogenetic proteins 2 and 5 are down-regulated in adrenocortical carcinoma and modulate adrenal cell proliferation and steroidogenesis. Cancer Res 69: 5784-5792, 2009.
27. Bieniasz M, Oszajca K, Eusebio M, Kordiak J, Bartkowiak J and Szemraj J: The positive correlation between gene expression of the two angiogenic factors: VEGF and BMP-2 in lung cancer patients. Lung Cancer 66: 319-326, 2009.
28. Rothhammer T, Bataille F, Spruss T, Eissner G and Bosserhoff AK: Functional implication of BMP4 expression on angiogenesis in malignant melanoma. Oncogene 26: 4158-4170, 2007. (Pubitemid 46920167)
29. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F and Vescovi AL: Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444: 761-765, 2006. (Pubitemid 44949605)
30. Theriault BL, Shepherd TG, Mujoomdar ML and Nachtigal MW: BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis 28: 1153-1162, 2007. (Pubitemid 47062673)
31. Buckley S, Shi W, Driscoll B, Ferrario A, Anderson K and Warburton D: BMP4 signaling induces senescence and modulates the oncogenic phenotype of A549 lung adenocarcinoma cells. Am J Physiol Lung Cell Mol Physiol 286: L81-86, 2004. (Pubitemid 38055861)
32. Bentley H, Hamdy FC, Hart KA, Seid JM, Williams JL, Johnstone D and Russell RG: Expression of bone morphogenetic proteins in human prostatic adenocarcinoma and benign prostatic hyperplasia. Br J Cancer 66: 1159-1163, 1992. (Pubitemid 23006160)
33. Ogose A, Motoyama T, Hotta T and Watanabe H: Expression of bone morphogenetic proteins in human osteogenic and epithelial tumor cells. Pathol Int 46: 9-14, 1996. (Pubitemid 26171366)
34. Brubaker KD, Corey E, Brown LG and Vessella RL: Bone morphogenetic protein signaling in prostate cancer cell lines. J Cell Biochem 91: 151-160, 2004.
35. 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 12: 192-205.
36. Ye L, Kynaston H and Jiang WG: Bone morphogenetic protein-10 suppresses the growth and aggressiveness of prostate cancer cells through a Smad independent pathway. J Urol 181: 2749-2759, 2009.
37. Ye L, Bokobza SM and Jiang WG: Bone morphogenetic proteins in development and progression of breast cancer and therapeutic potential (review). Int J Mol Med 24: 591-597, 2009.
38. Ye L, Kynaston H and Jiang WG: Bone morphogenetic protein-9 induces apoptosis in prostate cancer cells, the role of prostate apoptosis response-4. Mol Cancer Res 6: 1594-1606, 2008.
39. Jiang WG, Hiscox S, Hallett MB, Scott C, Horrobin DF and Puntis MC: Inhibition of hepatocyte growth factor-induced motility and in vitro invasion of human colon cancer cells by gamma-linolenic acid. Br J Cancer 71: 744-752, 1995.
40. Jiang WG, Hiscox S, Singhrao SK, Nakamura T, Puntis MC and Hallett MB: Inhibition of HGF/SF-induced membrane ruffling and cell motility by transient elevation of cytosolic free Ca2+. Exp Cell Res 220: 424-433, 1995.
41. Jiang WG, Davies G, Martin TA, Parr C, Watkins G, Mason MD, Mokbel K and Mansel RE: Targeting matrilysin and its impact on tumor growth in vivo: the potential implications in breast cancer therapy. Clin Cancer Res 11: 6012-6019, 2005. (Pubitemid 41170333)
42. Jiang WG, Davies G, Martin TA, Parr C, Watkins G, Mason MD and Mansel RE: Expression of membrane type-1 matrix metalloproteinase, MT1-MMP in human breast cancer and its impact on invasiveness of breast cancer cells. Int J Mol Med 17:583-590, 2006.
43. Chen D, Zhao M and Mundy GR: Bone morphogenetic proteins. Growth Factors 22: 233-241, 2004. (Pubitemid 40136452)
44. Cunningham NS, Paralkar V and Reddi AH: Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor beta 1 mRNA expression. Proc Natl Acad Sci USA 89: 11740-11744, 1992. (Pubitemid 23004719)
45. Yamashita H, ten Dijke P, Huylebroeck D, Sampath TK, Andries M, Smith JC, Heldin CH and Miyazono K: Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J Cell Biol 130: 217-226, 1995.
46. Goumans MJ and Mummery C: Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int J Dev Biol 44: 253-265, 2000.
47. Billings PC, Fiori JL, Bentwood JL, O'Connell MP, Jiao X, Nussbaum B, Caron RJ, Shore EM and Kaplan FS: Dysregulated BMP signaling and enhanced osteogenic differentiation of connective tissue progenitor cells from patients with fibrodysplasia ossificans progressiva (FOP). J Bone Miner Res 23: 305-313, 2008. (Pubitemid 351304661)
48. Haramis AP, Begthel H, van den Born M, van Es J, Jonkheer S, Offerhaus GJ and Clevers H: De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 303: 1684-1686, 2004. (Pubitemid 38338329)
49. Yu PB, Beppu H, Kawai N, Li E and Bloch KD: Bone morphogenetic protein (BMP) type II receptor deletion reveals BMP ligand-specific gain of signaling in pulmonary artery smooth muscle cells. J Biol Chem 280: 24443-24450, 2005. (Pubitemid 40934529)
50. Hardwick JC, Kodach LL, Offerhaus GJ and van den Brink GR: Bone morphogenetic protein signalling in colorectal cancer. Nat Rev Cancer 8: 806-812, 2008.
51. Kraunz KS, Nelson HH, Liu M, Wiencke JK and Kelsey KT: Interaction between the bone morphogenetic proteins and Ras/MAP-kinase signalling pathways in lung cancer. Br J Cancer 93: 949-952, 2005. (Pubitemid 41487023)
52. Hsu MY, Rovinsky S, Penmatcha S, Herlyn M and Muirhead D: Bone morphogenetic proteins in melanoma: angel or devil? Cancer Metastasis Rev 24: 251-263, 2005. (Pubitemid 40931929)
53. Kim IY, Lee DH, Lee DK, Kim BC, Kim HT, Leach FS, Linehan WM, Morton RA and Kim SJ: Decreased expression of bone morphogenetic protein (BMP) receptor type II correlates with insensitivity to BMP-6 in human renal cell carcinoma cells. Clin Cancer Res 9: 6046-6051, 2003. (Pubitemid 38018092)
54. Hamdy FC, Autzen P, Robinson MC, Horne CH, Neal DE and Robson CN: Immunolocalization and messenger RNA expression of bone morphogenetic protein-6 in human benign and malignant prostatic tissue. Cancer Res 57: 4427-4431, 1997. (Pubitemid 27413455)
55. Masuda H, Fukabori Y, Nakano K, Takezawa Y, T CS and Yamanaka H: Increased expression of bone morphogenetic protein-7 in bone metastatic prostate cancer. Prostate 54: 268-274, 2003. (Pubitemid 36228163)
56. Yuen HF, Chan YP, Cheung WL, Wong YC, Wang X and Chan KW: The prognostic significance of BMP-6 signaling in prostate cancer. Mod Pathol 21: 1436-1443, 2008.
57. Buijs JT, Rentsch CA, van der Horst G, van Overveld PG, Wetterwald A, Schwaninger R, Henriquez NV, Ten Dijke P, Borovecki F, Markwalder R, Thalmann GN, Papapoulos SE, Pelger RC, Vukicevic S, Cecchini MG, Lowik CW and van der Pluijm G: BMP7, a putative regulator of epithelial homeostasis in the human prostate, is a potent inhibitor of prostate cancer bone metastasis in vivo. Am J Pathol 171: 1047-1057, 2007. (Pubitemid 47441001)
58. Masuda H, Fukabori Y, Nakano K, Shimizu N and Yamanaka H: Expression of bone morphogenetic protein-7 (BMP-7) in human prostate. Prostate 59: 101-106, 2004. (Pubitemid 38387847)
59. Chen H, Shi S, Acosta L, Li W, Lu J, Bao S, Chen Z, Yang Z, Schneider MD, Chien KR, Conway SJ, Yoder MC, Haneline LS, Franco D and Shou W: BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131:2219-2231, 2004. (Pubitemid 38702052)
60. Neuhaus H, Rosen V and Thies RS: Heart specific expression of mouse BMP-10 a novel member of the TGF-beta superfamily. Mech Dev 80: 181-184, 1999. (Pubitemid 29125429)
61. Ye L, Bokobza S, Li J, Moazzam M, Chen J, Mansel RE and Jiang WG: Bone morphogenetic protein-10 (BMP-10) inhibits aggressiveness of breast cancer cells and correlates with poor prognosis in breast cancer. Cancer Sci 101: 2137-2144, 2010.
62. Sidransky D, Frost P, Von Eschenbach A, Oyasu R, Preisinger AC and Vogelstein B: Clonal origin bladder cancer. N Engl J Med 326: 737-740, 1992.
63. Vriesema JL, Aben KK, Witjes JA, Kiemeney LA and Schalken JA: Superficial and metachronous invasive bladder carcinomas are clonally related. Int J Cancer 93: 699-702, 2001. (Pubitemid 32695119)
64. Goto K, Konomoto T, Hayashi K, Kinukawa N, Naito S, Kumazawa J and Tsuneyoshi M: p53 mutations in multiple urothelial carcinomas: a molecular analysis of the development of multiple carcinomas. Mod Pathol 10: 428-437, 1997. (Pubitemid 27244228)