Placental growth factor supports neuroendocrine tumor growth and predicts disease prognosis in patients

Endocrine-Related Cancer

Volumn 20, Issue 3, 2013, Pages 305-319

  Hilfenhaus, Georg ^a,b   Göhrig, Andreas ^a,b   Pape, Ulrich Frank ^b   Neumann, Tabea ^b   Jann, Henning ^b   Zdunek, Dietmar ^c   Hess, Georg ^c   Stassen, Jean Marie ^d   Wiedenmann, Bertram ^b   Detjen, Katharina ^a,b   Pavel, Marianne ^b   Fischer, Christian ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c ROCHE DIAGNOSTICS GMBH   (Germany)

^d ThromboGenics NV   (Belgium)

Author keywords

NET; Neuroendocrine tumor; Placental growth factor; PlGF; Prognostic biomarker

Indexed keywords

PLACENTAL GROWTH FACTOR;

ADULT; AGED; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTESTINAL NEUROENDOCRINE TUMOR; MAJOR CLINICAL STUDY; MALE; NEUROENDOCRINE TUMOR; PANCREATIC NEUROENDOCRINE TUMOR; PROGNOSIS; PROTEIN BLOOD LEVEL; TUMOR GROWTH; TUMOR XENOGRAFT;

NET; NEUROENDOCRINE TUMOR; PLACENTAL GROWTH FACTOR; PLGF; PROGNOSTIC BIOMARKER;

ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; GASTROINTESTINAL NEOPLASMS; HUMANS; MALE; MIDDLE AGED; NEOPLASM GRADING; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; PREGNANCY PROTEINS; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; YOUNG ADULT;

EID: 84879469416     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-12-0223     Document Type: Article

References (53)

1. Alexandraki KI & Kaltsas G 2012 Gastroenteropancreatic neuroendocrine tumors: new insights in the diagnosis and therapy. Endocrine 41 40-52. (doi:10.1007/s12020-011-9562-2)
2. Asada M, Ebihara S, Yamanda S, Niu K, Okazaki T, Sora I & Arai H 2009 Depletion of serotonin and selective inhibition of 2B receptor suppressed tumor angiogenesis by inhibiting endothelial nitric oxide synthase and extracellular signal-regulated kinase 1/2 phosphorylation. Neoplasia 11 408-417.
3. Bagri A, Tessier-Lavigne M & Watts RJ 2009 Neuropilins in tumor biology. Clinical Cancer Research 15 1860-1864. (doi:10.1158/1078-0432.CCR-08- 0563)
4. Bass MB, Sherman SI, Schlumberger MJ, Davis MT, Kivman L, Khoo HM, Notari KH, Peach M, Hei YJ & Patterson SD 2010 Biomarkers as predictors of response to treatment with motesanib in patients with progressive advanced thyroid cancer. Journal of Clinical Endocrinology and Metabolism 95 5018-5027. (doi:10.1210/jc.2010-0947)
5. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, Kozak KR, Cahill DP, Chen PJ, Zhu M et al. 2007 AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11 83-95. (doi:10.1016/j.ccr.2006.11.021)
6. Baudin E 2007 Gastroenteropancreatic endocrine tumors: clinical characterization before therapy. Nature Clinical Practice. Endocrinology & Metabolism 3 228-239. (doi:10.1038/ncpendmet0425)
7. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H et al. 2001 Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nature Medicine 7 575-583. (doi:10.1038/87904)
8. Cheng SJ, Lee JJ, Cheng SL, Chen HM, Chang HH, Wang YP, Kok SH, Kuo MY & Chiang CP 2012 Increased serum placenta growth factor level is significantly associated with progression, recurrence and poor prognosis of oral squamous cell carcinoma. Oral Oncology 48 424-428. (doi:10.1016/j.oraloncology. 2011.12.007)
9. Coenegrachts L, Maes C, Torrekens S, Van Looveren R, Mazzone M, Guise TA, Bouillon R, Stassen JM, Carmeliet P & Carmeliet G 2010 Anti-placental growth factor reduces bone metastasis by blocking tumor cell engraftment and osteoclast differentiation. Cancer Research 70 6537-6547. (doi:10.1158/0008- 5472.CAN-09-4092)
10. Corti A 2010 Chromogranin A and the tumor microenvironment. Cellular and Molecular Neurobiology 30 1163-1170. (doi:10.1007/s10571-010-9587-8)
11. Couvelard A, O'Toole D, Turley H, Leek R, Sauvanet A, Degott C, Ruszniewski P, Belghiti J, Harris AL, Gatter K et al. 2005 Microvascular density and hypoxia-inducible factor pathway in pancreatic endocrine tumours: negative correlation of microvascular density and VEGF expression with tumour progression. British Journal of Cancer 92 94-101. (doi:10.1038/sj.bjc.6602245)
12. Detjen KM, Rieke S, Deters A, Schulz P, Rexin A, Vollmer S, Hauff P, Wiedenmann B, Pavel M & Scholz A 2010 Angiopoietin-2 promotes disease progression of neuroendocrine tumors. Clinical Cancer Research 16 420-429. (doi:10.1158/1078-0432.CCR-09-1924)
13. Fan F, Samuel S, Gaur P, Lu J, Dallas NA, Xia L, Bose D, Ramachandran V & Ellis LM 2011 Chronic exposure of colorectal cancer cells to bevacizumab promotes compensatory pathways that mediate tumour cell migration. British Journal of Cancer 104 1270-1277. (doi:10.1038/bjc.2011.81)
14. Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, Chorianopoulos E, Liesenborghs L, Koch M, De Mol M et al. 2007 Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 131 463-475. (doi:10.1016/j.cell. 2007.08.038)
15. Fischer C, Mazzone M, Jonckx B & Carmeliet P 2008 FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy? Nature Reviews. Cancer 8 942-956. (doi:10.1038/nrc2524)
16. de Groot JF, Piao Y, Tran HT, Gilbert MR, Wu HK, Liu J, Bekele BN, Cloughesy T, Mehta MP, Robins HI et al. 2011 Myeloid biomarkers associated with glioblastoma response to anti-vascular endothelial growth factor therapy with aflibercept. Clinical Cancer Research 17 4872-4881. (doi:10.1158/1078-0432.CCR- 11-0271)
17. Heindryckx F, Bogaerts E, Coulon SH, Devlies H, Geerts AM, Libbrecht L, Stassen JM, Carmeliet P, Colle IO & Van Vlierberghe HR 2012 Inhibition of the placental growth factor decreases burden of cholangiocarcinoma and hepatocellular carcinoma in a transgenic mouse model. European Journal of Gastroenterology & Hepatology 24 1020-1032. (doi:10.1097/MEG. 0b013e3283554219)
18. Lassen U, Nielsen DL, Sorensen M, Winstedt L, Niskanen T, Stenberg Y, Pakola S, Stassen JM & Glazer S 2012 A phase I, dose-escalation study of TB-403, a monoclonal antibody directed against PlGF, in patients with advanced solid tumours. British Journal of Cancer 106 678-684. (doi:10.1038/bjc.2011.609)
19. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L et al. 2001 Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nature Medicine 7 1194-1201. (doi:10.1038/nm1101-1194)
20. Maae E, Olsen DA, Steffensen KD, Jakobsen EH, Brandslund I, Sorensen FB & Jakobsen A 2012 Prognostic impact of placenta growth factor and vascular endothelial growth factor A in patients with breast cancer. Breast Cancer Research and Treatment 133 257-265. (doi:10.1007/s10549-012-1957-0)
21. Marcellini M, De Luca N, Riccioni T, Ciucci A, Orecchia A, Lacal PM, Ruffini F, Pesce M, Cianfarani F, Zambruno G et al. 2006 Increased melanoma growth and metastasis spreading in mice overexpressing placenta growth factor. American Journal of Pathology 169 643-654. (doi:10.2353/ajpath.2006.051041)
22. Marion-Audibert AM, Barel C, Gouysse G, Dumortier J, Pilleul F, Pourreyron C, Hervieu V, Poncet G, Lombard-Bohas C, Chayvialle JA et al. 2003 Low microvessel density is an unfavorable histoprognostic factor in pancreatic endocrine tumors. Gastroenterology 125 1094-1104. (doi:10.1016/S0016-5085(03) 01198-3)
23. von Marschall Z, Scholz A, Cramer T, Schafer G, Schirner M, Oberg K, Wiedenmann B, Hocker M & Rosewicz S 2003 Effects of interferon alpha on vascular endothelial growth factor gene transcription and tumor angiogenesis. Journal of the National Cancer Institute 95 437-448. (doi:10.1093/jnci/95.6.437)
24. Martinsson-Niskanen T, Riisbro R, Larsson L, Winstedt L, Stenberg Y, Pakola S, Stassen JM & Glazer S 2011 Monoclonal antibody TB-403: a first-in-human, phase i, double-blind, dose escalation study directed against placental growth factor in healthy male subjects. Clinical Therapeutics 33 1142-1149. (doi:10.1016/j.clinthera.2011.08.007)
25. Matsumoto K, Suzuki K, Koike H, Okamura K, Tsuchiya K, Uchida T, Takezawa Y, Kobayashi M & Yamanaka H 2003 Prognostic significance of plasma placental growth factor levels in renal cell cancer: an association with clinical characteristics and vascular endothelial growth factor levels. Anticancer Research 23 4953-4958.
26. Modlin IM, Oberg K, Chung DC, Jensen RT, de Herder WW, Thakker RV, Caplin M, Delle Fave G, Kaltsas GA, Krenning EP et al. 2008 Gastroenteropancreatic neuroendocrine tumours. Lancet Oncology 9 61-72. (doi:10.1016/S1470-2045(07) 70410-2)
27. Motzer RJ, Michaelson MD, Redman BG, Hudes GR, Wilding G, Figlin RA, Ginsberg MS, Kim ST, Baum CM, DePrimo SE et al. 2006 Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. Journal of Clinical Oncology 24 16-24. (doi:10.1200/JCO.2005.02.2574)
28. Nagaoka S, Yoshida T, Akiyoshi J, Akiba J, Hisamoto T, Yoshida Y, Abe M, Koga H, Toirimura T, Ueno T et al. 2010 The ratio of serum placenta growth factor to soluble vascular endothelial growth factor receptor-1 predicts the prognosis of hepatocellular carcinoma. Oncology Reports 23 1647-1654. (doi:10.3892/or-00000807)
29. Nakamura T, Funayama H, Kubo N, Yasu T, Kawakami M, Momomura S & Ishikawa SE 2009 Elevation of plasma placental growth factor in the patients with ischemic cardiomyopathy. International Journal of Cardiology 131 186-191. (doi:10.1016/j.ijcard.2007.10.050)
30. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, Inoue M, Bergers G, Hanahan D & Casanovas O 2009 Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distantmetastasis. Cancer Cell 15 220-231. (doi:10.1016/j. ccr.2009.01.027)
31. Panzuto F, Boninsegna L, Fazio N, Campana D, Pia Brizzi M, Capurso G, Scarpa A, De Braud F, Dogliotti L, Tomassetti P et al. 2011 Metastatic and locally advanced pancreatic endocrine carcinomas: analysis of factors associated with disease progression. Journal of Clinical Oncology 29 2372-2377. (doi:10.1200/JCO.2010.33.0688)
32. Pape UF, Berndt U, Muller-Nordhorn J, Bohmig M, Roll S, Koch M, Willich SN & Wiedenmann B 2008 Prognostic factors of long-term outcome in gastroenteropancreatic neuroendocrine tumours. Endocrine-Related Cancer 15 1083-1097. (doi:10.1677/ERC-08-0017)
33. Parr C, Watkins G, Boulton M, Cai J & Jiang WG 2005 Placenta growth factor is over-expressed and has prognostic value in human breast cancer. European Journal of Cancer 41 2819-2827. (doi:10.1016/j.ejca. 2005.07.022)
34. Pavel ME, Hainsworth JD, Baudin E, Peeters M, Horsch D, Winkler RE, Klimovsky J, Lebwohl D, Jehl V, Wolin EM et al. 2011 Everolimus plus octreotide long-acting repeatable for the treatment of advanced neuroendocrine tumours associated with carcinoid syndrome (RADIANT-2): a randomised, placebo-controlled, phase 3 study. Lancet 378 2005-2012. (doi:10.1016/S0140- 6736(11)61742-X)
35. Pfragner R, Wirnsberger G, Niederle B, Behmel A, Rinner I, Mandl A, Wawrina F, Luo J, Adamiker D, Hoger H et al. 1996 Establishment of a continuous cell line from a human carcinoid of the small intestine (KRJ-I). International Journal of Oncology 8 513-520.
36. Rahbari NN, Reissfelder C, Muhlbayer M, Weidmann K, Kahlert C, Buchler MW, Weitz J & Koch M 2011 Correlation of circulating angiogenic factors with circulating tumor cells and disease recurrence in patients undergoing curative resection for colorectal liver metastases. Annals of Surgical Oncology 18 2182-2191. (doi:10.1245/s10434-011-1761-9)
37. Raymond E, Dahan L, Raoul JL, Bang YJ, Borbath I, Lombard-Bohas C, Valle J, Metrakos P, Smith D, Vinik A et al. 2011 Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. New England Journal of Medicine 364 501-513. (doi:10.1056/NEJMoa1003825)
38. Rindi G, Kloppel G, Alhman H, Caplin M, Couvelard A, de Herder WW, Erikssson B, Falchetti A, Falconi M, Komminoth P et al. 2006 TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Archiv 449 395-401. (doi:10.1007/s00428-006-0250-1)
39. Rindi G, Kloppel G, Couvelard A, Komminoth P, Korner M, Lopes JM, McNicol AM, Nilsson O, Perren A, Scarpa A et al. 2007 TNM staging of midgut and hindgut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Archiv 451 757-762. (doi:10.1007/s00428-007-0452-1)
40. Rini BI, Michaelson MD, Rosenberg JE, Bukowski RM, Sosman JA, Stadler WM, Hutson TE, Margolin K, Harmon CS, DePrimo SE et al. 2008 Antitumor activity and biomarker analysis of sunitinib in patients with bevacizumab-refractory metastatic renal cell carcinoma. Journal of Clinical Oncology 26 3743-3748. (doi:10.1200/JCO.2007.15. 5416)
41. Schiettecatte J, Russcher H, Anckaert E, Mees M, Leeser B, Tirelli AS, Fiedler GM, Luthe H, Denk B & Smitz J 2010 Multicenter evaluation of the first automated Elecsys sFlt-1 and PlGF assays in normal pregnancies and preeclampsia. Clinical Biochemistry 43 768-770. (doi:10.1016/j.clinbiochem.2010. 02.010)
42. Schmidt T, Kharabi Masouleh B, Loges S, Cauwenberghs S, Fraisl P, Maes C, Jonckx B, De Keersmaecker K, Kleppe M, Tjwa M et al. 2011 Loss or inhibition of stromal-derived PlGF prolongs survival of mice with imatinib-resistant Bcr-Abl1(+) leukemia. Cancer Cell 19 740-753. (doi:10.1016/j.ccr.2011.05.007)
43. Srirajaskanthan R, Dancey G, Hackshaw A, Luong T, Caplin ME & Meyer T 2009 Circulating angiopoietin-2 is elevated in patients with neuroendocrine tumours and correlates with disease burden and prognosis. Endocrine-Related Cancer 16 967-976. (doi:10.1677/ERC-09-0089)
44. Taylor AP, Leon E & Goldenberg DM 2010 Placental growth factor (PlGF) enhances breast cancer cell motility by mobilising ERK1/2 phosphorylation and cytoskeletal rearrangement. British Journal of Cancer 103 82-89. (doi:10.1038/sj.bjc.6605746)
45. Terris B, Scoazec JY, Rubbia L, Bregeaud L, Pepper MS, Ruszniewski P, Belghiti J, Flejou J & Degott C 1998 Expression of vascular endothelial growth factor in digestive neuroendocrine tumours. Histopathology 32 133-138. (doi:10.1046/j.1365-2559.1998.00321.x)
46. Van de Veire S, Stalmans I, Heindryckx F, Oura H, Tijeras-Raballand A, Schmidt T, Loges S, Albrecht I, Jonckx B, Vinckier S et al. 2010 Further pharmacological and genetic evidence for the efficacy of PlGF inhibition in cancer and eye disease. Cell 141 178-190. (doi:10.1016/j. cell.2010.02.039)
47. Verheul HM & Pinedo HM 2007 Possible molecular mechanisms involved in the toxicity of angiogenesis inhibition. Nature Reviews. Cancer 7 475-485. (doi:10.1038/nrc2152)
48. Wei SC, Tsao PN, Yu SC, Shun CT, Tsai-Wu JJ, Wu CH, Su YN, Hsieh FJ & Wong JM 2005 Placenta growth factor expression is correlated with survival of patients with colorectal cancer. Gut 54 666-672. (doi:10.1136/gut.2004.050831)
49. Wei SC, Liang JT, Tsao PN, Hsieh FJ, Yu SC & Wong JM 2009 Preoperative serum placenta growth factor level is a prognostic biomarker in colorectal cancer. Diseases of the Colon and Rectum 52 1630-1636. (doi:10.1007/DCR.0b013e3181afbdaf)
50. Willett CG, Duda DG, di Tomaso E, Boucher Y, Ancukiewicz M, Sahani DV, Lahdenranta J, Chung DC, Fischman AJ, Lauwers GY et al. 2009 Efficacy, safety, and biomarkers of neoadjuvant bevacizumab, radiation therapy, and fluorouracil in rectal cancer: a multidisciplinary phase II study. Journal of Clinical Oncology 27 3020-3026. (doi:10.1200/JCO. 2008.21.1771)
51. Yao J, Wu X, Zhuang G, Kasman IM, Vogt T, Phan V, Shibuya M, Ferrara N & Bais C 2011a Expression of a functional VEGFR-1 in tumor cells is a major determinant of anti-PlGF antibodies efficacy. PNAS 108 11590-11595. (doi:10.1073/pnas.1109029108)
52. Yao JC, Shah MH, Ito T, Bohas CL, Wolin EM, Van Cutsem E, Hobday TJ, Okusaka T, Capdevila J, de Vries EG et al. 2011b Everolimus for advanced pancreatic neuroendocrine tumors. New England Journal of Medicine 364 514-523. (doi:10.1056/NEJMoa1009290)
53. Yao JC, Tsuchihashi Z, Panneerselvam A, Winkler RE, Bugarini R & Pavel M 2011c 6573 POSTER Effect of everolimus treatment on markers of angiogenesis in patients with advanced pancreatic neuroendocrine tumours (pNET)-results from the phase III RADIANT-3 study. European Journal of Cancer 47 (Supplement 1) S463.