Oncogenic features of the bone morphogenic protein 7 (BMP7) in pheochromocytoma

Oncotarget

Volumn 6, Issue 36, 2015, Pages 39111-39126

  Leinhäuser, Ines ^a   Richter, Andrea ^a   Lee, Misu ^a   Höfig, Ines ^a   Anastasov, Nataša ^a   Fend, Falko ^b   Ercolino, Tonino ^c   Mannelli, Massimo ^d   Gimenez Roqueplo, Anne Paule ^e,f,g   Robledo, Mercedes ^h   de Krijger, Ronald ⁱ   Beuschlein, Felix ^j   Atkinson, Michael J ^a   Pellegata, Natalia S ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c Endocrine Unit   (Italy)

^d UNIVERSITY OF FLORENCE   (Italy)

^e PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^h Structural Biology and Biocomputing Programme   (Spain)

ⁱ ERASMUS MEDICAL CENTER   (Netherlands)

^j LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

more..

Author keywords

Bone morphogenic protein 7; Integrin beta 1; MENX rats; Pheochromocytoma; PI3K pathway

Indexed keywords

ANTINEOPLASTIC AGENT; BETA1 INTEGRIN; DACTOLISIB; DMH 1; MAMMALIAN TARGET OF RAPAMYCIN; OSTEOGENIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PLACEBO; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER INHIBITION; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; COHORT ANALYSIS; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METASTASIS INHIBITION; NONHUMAN; PHEOCHROMOCYTOMA; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TUMOR INVASION; ADRENAL TUMOR; ANIMAL; CASE CONTROL STUDY; FEMALE; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; PC12 CELL LINE; PHYSIOLOGY;

ADRENAL GLAND NEOPLASMS; ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 7; CASE-CONTROL STUDIES; CELL PROLIFERATION; COHORT STUDIES; FEMALE; HUMANS; MALE; PC12 CELLS; PHEOCHROMOCYTOMA; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84948845037     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4912     Document Type: Article

References (58)

1. Favier J, Amar L, Gimenez-Roqueplo AP. Paraganglioma and phaeochromocytoma: from genetics to personalized medicine. Nat Rev Endocrinol. 2015; 11:101-111.
2. Castro-Vega LJ, Letouzé E, Burnichon N, Buffet A, Disderot PH, Khalifa E, Loriot C, Elarouci N, Morin A, Menara M, Lepoutre-Lussey C, Badoual C, Sibony M, et al. Multi-omics analysis defines core genomic alterations in pheochromocytomas and paragangliomas. Nat Commun. 2015; 6:6044.
3. Fishbein L, Khare S, Wubbenhorst B, DeSloover D, D'Andrea K, Merrill S, Cho NW, Greenberg RA, Else T, Montone K, LiVolsi V, Fraker D, Daber R, et al. Whole-exome sequencing identifies somatic ATRX mutations in pheochromocytomas and paragangliomas. Nat Commun. 2015; 6:6140.
4. Eisenhofer G, Huynh TT, Pacak K, Brouwers FM, Walther MM, Linehan WM, Munson PJ, Mannelli M, Goldstein DS, Elkahloun AG. Distinct gene expression profiles in norepinephrine- and epinephrine-producing hereditary and sporadic pheochromocytomas: activation of hypoxia-driven angiogenic pathways in von Hippel-Lindau syndrome. Endocr Relat Cancer. 2004; 11:897-911.
5. Lopez-Jimenez E, Gomez-Lopez G, Leandro-Garcia LJ, Munoz I, Schiavi F, Montero-Conde C, de Cubas AA, Ramires R, Landa I, Leskelä S, Maliszewska A, Inglada-Pérez L, de la Vega L, et al. Research resource: Transcriptional profiling reveals different pseudohypoxic signatures in SDHB and VHL-related pheochromocytomas. Mol Endocrinol. 2010; 24:2382-2391.
6. Ayala-Ramirez M, Feng L, Johnson MM, Ejaz S, Habra MA, Rich T, Busaidy N, Cote GJ, Perrier N, Phan A, Patel S, Waguespack S, Jimenez C. Clinical risk factors for malignancy and overall survival in patients with pheochromocytomas and sympathetic paragangliomas: primary tumor size and primary tumor location as prognostic indicators. J Clin Endocrinol Metab. 2011; 96:717-725.
7. Eisenhofer G, Bornstein SR, Brouwers FM, Cheung NK, Dahia PL, de Krijger RR, Giordano TJ, Greene LA, Goldstein DS, Lehnert H, Manger WM, Maris JM, Neumann HP, et al. Malignant pheochromocytoma: current status and initiatives for future progress. Endocr Relat Cancer. 2004; 11:423-436.
8. Loh KC, Fitzgerald PA, Matthay KK, Yeo PP, Price DC. The treatment of malignant pheochromocytoma with iodine-131 metaiodobenzylguanidine (131I-MIBG): a comprehensive review of 116 reported patients. J Endocrinol Inv. 1997; 20:648-658.
9. Joshua AM, Ezzat S, Asa SL, Evans A, Broom R, Freeman M, Know JJ. Rationale and evidence for sunitinib in the treatment of malignant paraganglioma/pheochromocytoma. J Clin Endocrinol Metab. 2009; 94:5-9.
10. Druce MR, Kaltsas GA, Fraenkel M, Gross DJ, Grossman AB. Novel and evolving therapies in the treatment of malignant phaeochromocytoma: experience with the mTOR inhibitor everolimus (RAD001). Horm Metab Res. 2009; 41:697-702.
11. Oh DY, Kim TW, Park YS, Shin SJ, Shin SH, Song EK, Lee HJ, Lee KW, Bang YJ. Phase 2 study of everolimus monotherapy in patients with nonfunctioning neuroendocrine tumors or pheochromocytomas/paragangliomas. Cancer. 2012; 118:6162-70.
12. Fritz A, Walch A, Piotrowska K, Rosemann M, Schaffer E, Weber K, Timper A, Wildner G, Graw J, Höfler H, Atkinson MJ. Recessive transmission of a multiple endocrine neoplasia syndrome in the rat. Cancer Res. 2002; 62:3048-3051.
13. Shyla A, Holzlwimmer G, Calzada-Wack J, Bink K, Tischenko O, Guilly MN, Chevillard S, Samson E, Graw J, Atkinson MJ, Pellegata NS. Allelic loss of chromosomes 8 and 19 in MENX-associated rat pheochromocytoma. Int J Cancer. 2010; 126:2362-2372.
14. Molatore S, Liyanarachchi S, Irmler M, Perren A, Mannelli M, Ercolino T, Beuschlein F, Jarzab B, Wloch J, Ziaja J, Zoubaa S, Neff F, Beckers J, et al. Pheochromocytoma in rats with multiple endocrine neoplasia (MENX) shares gene expression patterns with human pheochromocytoma. Proc Natl Acad Sci U S A. 2010; 107:18493-18498.
15. Miederer M, Molatore S, Marinoni I, Perren A, Spitzweg C, Reder S, Wester H-J, Buck AK, Schwaiger M, Pellegata NS. Functional Imaging of Pheochromocytoma with 68Ga-DOTATOC and 11C-HED in a Genetically Defined Rat Model of Multiple Endocrine Neoplasia. Int J Mol Imaging. 2011; :175352.
16. Gaertner FC, Wiedemann T, Yousefi BH, Lee M, Repokis I, Higuchi T, Nekolla SG, Yu M, Robinson S, Schwaiger M, Pellegata NS. Preclinical evaluation of 18F-LMI1195 for in vivo imaging of pheochromocytoma in the MENX tumor model. J Nucl Med. 2013; 54:2111-2117.
17. Pellegata NS, Quintanilla-Martinez L, Siggelkow H, Samson E, Bink K, Höfler H, Fend F, Graw J, Atkinson MJ. Germline mutations in p27Kip1 cause a multiple endocrine neoplasia syndrome in rats and man. Proc Natl Acad Sci USA. 2006; 103:15558-63.
18. Chen D, Zhao M, Harris SE, Mi Z. Signal transduction and biological functions of bone morphogenetic proteins. Front Biosci. 2004; 9:349-358.
19. Wang RN, Green J, Wang Z, Deng Y, Qiao M, Peabody M, Zhang Q, Ye J, Yan Z, Denduluri S, Idowu O, Li M, Shen C, et al. Bone Morphogenetic Protein (BMP) signaling in development and human diseases. Genes Dis. 2014; 1:87-105.
20. Thawani JP, Wang AC, Than KD, Lin CY, La Marca F, Park P. Bone morphogenetic proteins and cancer: review of the literature. Neurosurgery. 2010; 66:233-246.
21. Kishigami S, Mishina Y. BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev. 2005; 16:265-278.
22. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature. 1997; 390:465-471.
23. von Bubnoff A, Cho KW. Intracellular BMP signaling regulation in vertebrates: pathway or network? Dev Biol. 2001; 239:1-14.
24. Blanco Calvo M, Bolós Fernández V, Medina Villaamil V, Aparicio Gallego G, Díaz Prado S, Grande Pulido E. Biology of BMP signalling and cancer. Clin Transl Oncol. 2009; 11:126-37.
25. Alarmo EL, Korhonen T, Kuukasjarvi T, Huhtala H, Holli K, Kallioniemi A. Bone morphogenetic protein 7 expression associates with bone metastasis in breast carcinomas. Ann Oncol. 2008; 19:308-314.
26. Gespach C, Grijelmo C, Rodrigue C, Svrcek M, Bruyneel E, Hendrix A, de Wever O, Gespach C. Proinvasive activity of BMP-7 through SMAD4/src-independent and ERK/Rac JNK-dependent signaling pathways in colon cancer cells. Cell Signal. 2007; 19:1722-1732.
27. Aoki M, Ishigami S, Uenosono Y, Arigami T, Uchikado Y, Kita Y, Kurahara H, Matsumoto M, Ueno S, Natsugoe S. Expression of BMP-7 in human gastric cancer and its clinical significance. Br J Cancer. 2011; 104:714-718.
28. Miyazaki H, Watabe T, Kitamura T, Miyazono K. BMP signals inhibit proliferation and in vivo tumor growth of androgen-insensitive prostate carcinoma cells. Oncogene. 2004; 23:9326-9335.
29. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976; 73:2424-2428.
30. Goto J, Otsuka F, Yamashita M, Suzuki J, Otani H, Takahashi H, Miyoshi T, Mimura Y, Ogura T, Makino H. Enhancement of aldosterone-induced catecholamine production by bone morphogenetic protein-4 through activating Rho and SAPK/JNK pathway in adrenomedullar cells. Am J Physiol Endocrinol Metab. 2009; 296:E904-916.
31. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002; 110:673-687.
32. Adelsman MA, McCarthy JB, Shimizu Y. Stimulation of beta1-integrin function by epidermal growth factor and heregulin-beta has distinct requirements for erbB2 but a similar dependence on phosphoinositide 3-OH kinase. Mol Biol Cell. 1999; 10:2861-2878.
33. Fong YC, Li TM, Wu CM, Hsu SF, Kao ST, Chen RJ, Lin CC, Liu SC, Wu CL, Tang CH. BMP-2 increases migration of human chondrosarcoma cells via PI3K/Akt pathway. J Cell Physiol. 2008; 217:846-855.
34. Panupinthu N, Yu S, Zhang D, Zhang F, Gagea M, Lu Y, Grandis JR, Dunn SE, Lee HY, Mills GB. Self-reinforcing loop of amphiregulin and Y-box binding protein-1 contributes to poor outcomes in ovarian cancer. Oncogene. 2014; 33:2846-2856.
35. Hao J, Ho JN, Lewis JA, Karim KA, Daniels RN, Gentry PR, Hopkins CR, Lindsley CW, Hong CC. In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem Biol. 2010; 5:245-53.
36. Lee M, Waser B, Reubi JC, Pellegata NS. Secretin receptor promotes the proliferation of endocrine tumor cells via the PI3K/AKT pathway. Mol Endocrinol. 2012; 26:1394-1405.
37. Xu G, Tang S, Yang J, Chen K, Kang J, Zhao G, Feng F, Yang X, Zhao L, Lu Q, Sun L, Hong L, Gong T, et al. BMP7 expression in esophageal squamous cell carcinoma and its potential role in modulating metastasis. Dig Dis Sci. 2013; 58:1871-1879.
38. Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, ten Dijke P, van der Pluijm G. TGF-beta and BMP7 interactions in tumour progression and bone metastasis. Clin Exp Metastasis. 2007; 24:609-617.
39. Jin H, Pi J, Huang X, Huang F, Shao W, Li S, Chen Y, Cai J. BMP2 promotes migration and invasion of breast cancer cells via cytoskeletal reorganization and adhesion decrease: an AFM investigation. Appl Microbiol Biotechnol. 2012; 93:1715-1723.
40. Guo D, Huang J, Gong J. Bone morphogenetic protein 4 (BMP4) is required for migration and invasion of breast cancer. Mol Cell Biochem. 2012; 363:179-90.
41. Liu Y, Chen J, Yang Y, Zhang L, Jiang WG. Molecular impact of bone morphogenetic protein 7, on lung cancer cells and its clinical significance. Int J Mol Med. 2012; 29:1016-1024.
42. Rothhammer T, Poser I, Soncin F, Bataille F, Moser M, Bosserhoff AK. Bone morphogenic proteins are overexpressed in malignant melanoma and promote cell invasion and migration. Cancer Res. 2005; 65:448-456.
43. Naber HP, Wiercinska E, Pardali E, van Laar T, Nirmala E, Sundqvist A, van Dam H, van der Horst G, van der Pluijm G, Heckmann B, Danen EH, Ten Dijke P. BMP-7 inhibits TGF-ß-induced invasion of breast cancer cells through inhibition of integrin ß(3) expression. Cell Oncol. 2012; 35:19-28.
44. Fassnacht M, Weismann D, Ebert S, Adam P, Zink M, Beuschlein F, Hahner S, Allolio B. AKT is highly phosphorylated in pheochromocytomas but not in benign adrenocortical tumors. J Clin Endocrinol Metab. 2005; 90:4366-4370.
45. Tsaur I, Makarevic J, Juengel E, Gasser M, Waaga-Gasser AM, Kurosch M, Reiter M, Wedel S, Bartsch G, Haferkamp A, Wiesner C, Blaheta RA. Resistance to the mTOR-inhibitor RAD001 elevates integrin alpha2- and beta1-triggered motility, migration and invasion of prostate cancer cells. Br J Cancer. 2012; 107:847-855.
46. Nolting S, Garcia E, Alusi G, Giubellino A, Pacak K, Korbonits M, Grossman AB. Combined blockade of signalling pathways shows marked anti-tumour potential in phaeochromocytoma cell lines. J Mol Endocrinol. 2012; 49:79-96.
47. Hosoi H, Dilling MB, Liu LN, Danks MK, Shikata T, Sekulic A, Abraham RT, Lawrence JC Jr, Houghton PJ. Studies on the mechanism of resistance to rapamycin in human cancer cells. Mol Pharmacol. 1998; 54:815-824.
48. Tan J, Yu Q. Molecular mechanisms of tumor resistance to PI3K-mTOR-targeted therapy. Chin J Cancer. 2013; 32:376-379.
49. Maira SM, Stauffer F, Brueggen J, Furet P, Schnell C, Fritsch C, Brachmann S, Chène P, De Pover A, Schoemaker K, Fabbro D, Gabriel D, Simonen M, et al. Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor with potent in vivo antitumor activity. Mol Cancer Ther. 2008; 7:1851-1863.
50. Owens P, Pickup MW, Novitskiy SV, Giltnane JM, Gorska AE, Hopkins CR, Hong CC, Moses HL. Inhibition of BMP signaling suppresses metastasis in mammary cancer. Oncogene. 2015; 34:2437-49.
51. Hao J, Lee R, Chang A, Fan J, Labib C, Parsa C, Orlando R, Andresen B, Huang Y. DMH1, a small molecule inhibitor of BMP type i receptors, suppresses growth and invasion of lung cancer. PLoS One. 2014; 9:e90748.
52. Oudijk L, Neuhofer CM, Lichtenauer UD, Papathomas TG, Korpershoek E, Stoop H, Oosterhuis JW, Smid M, Restuccia DF, Robledo M, de Cubas AA, Mannelli M, Gimenez-Roqueplo AP, et al. Immunohistochemical expression of stem cell markers in pheochromocytomas/paragangliomas is associated with SDHx mutations. Eur J Endocrinol. 2015; 173:43-52.
53. Powers JF, Evinger MJ, Tsokas P, Bedri S, Alroy J, Shahsavari M, Tischler AS. Pheochromocytoma cell lines from heterozygous neurofibromatosis knockout mice. Cell Tissue Res. 2000; 302:309-320.
54. Martiniova L, Lai EW, Elkahloun AG, Abu-Asab M, Wickremasinghe A, Solis DC, Perera SM, Huynh TT, Lubensky IA, Tischler AS, Kvetnansky R, Alesci S, Morris JC, et al. Characterization of an animal model of aggressive metastatic pheochromocytoma linked to a specific gene signature. Clin Exp Metastasis. 2009; 26:239-250.
55. Höfig I, Atkinson MJ, Mall S, Krackhardt AM, Thirion C, Anastasov N. Poloxamer synperonic F108 improves cellular transduction with lentiviral vectors. J Gene Med. 2012; 14:549-560.
56. Molatore S, Kiermaier E, Jung CB, Pulz E, Höfler H, Atkinson MJ, Pellegata NS. Characterization of a naturally-occurring p27 mutation predisposing to multiple endocrine tumors. Mol Cancer. 2010; 9:116.
57. Lee M, Lupp A, Mendoza N, Martin N, Beschorner R, Honegger J, Schlegel J, Shively T, Pulz E, Schulz S, Roncaroli F, Pellegata NS. Somatostatin receptor 3 is a putative target for the medical treatment of gonadotroph adenomas of the pituitary. Endocr Relat Cancer. 2014; 22:111-9.
58. Lee M, Wiedemann T, Gross C, Roncaroli F, Braren R, Pellegata NS. Targeting PI3K/mTOR signaling displays potent antitumor efficacy against nonfunctioning pituitary adenomas. Clinical Cancer Research. 2015; Apr. 2; [Epub ahead of print.]