Lung Cancer
Volume 66, Issue 3 , Pages 319-326 , December 2009

The positive correlation between gene expression of the two angiogenic factors: VEGF and BMP-2 in lung cancer patients

  • Magdalena Bieniasz

      Affiliations

    • Department of Medical Biochemistry, Medical University of Lodz, 6/8 Mazowiecka, Lodz 92215, Poland
    • Corresponding Author InformationCorresponding author. Tel.: +48 42 678 06 20; fax: +48 42 678 24 65.
  • ,
  • Katarzyna Oszajca

      Affiliations

    • Department of Medical Biochemistry, Medical University of Lodz, 6/8 Mazowiecka, Lodz 92215, Poland
  • ,
  • Mak Eusebio

      Affiliations

    • Department of Medical Biochemistry, Medical University of Lodz, 6/8 Mazowiecka, Lodz 92215, Poland
  • ,
  • Jacek Kordiak

      Affiliations

    • Department of Surgery, Medical University of Lodz, 4 Zeromskiego, Lodz 93509, Poland
  • ,
  • Jacek Bartkowiak

      Affiliations

    • Department of Medical Biochemistry, Medical University of Lodz, 6/8 Mazowiecka, Lodz 92215, Poland
  • ,
  • Janusz Szemraj

      Affiliations

    • Department of Medical Biochemistry, Medical University of Lodz, 6/8 Mazowiecka, Lodz 92215, Poland

Received 2 October 2008 ,Revised 17 February 2009 ,Accepted 22 February 2009.

References 

  1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer statistics 2008. CA Cancer J Clin. 2008;58:71–96
  2. Sun S, Schiller JH, Spinola M, Minnal JD. New molecularly targeted therapies for lung cancer. JCI. 2007;117(10):2740–2750
  3. Auberger J, Loeffler-Ragg J, Wurzer W, Wolfgang W. Targeted therapies in non-small cell lung cancer: proven concepts and unfulfilled promises. Curr Cancer Drug Targets. 2006;6:271–294
  4. Bremnes R, Camps C, Sirera R. Angiogenesis in non-small cell lung cancer: the prognostic impact of neoangiogenesis and the cytokines VEGF and bFGF in tumours and blood. Lung Cancer. 2006;51:143–158
  5. Ferrara N, Houck K, Jakeman L, Leung DW. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr Rev. 1992;13(1):18–32
  6. Galligioni E, Ferro A, Angiogenesis . Angiogenesis and antiangiogenic agents in non-small cell lung cancer. Lung Cancer. 2001;34:3–7
  7. Ferrara N, Gerber HP, LeCounter J. The biology of VEGF and its receptors. Nat Med. 2003;9(6):669–676
  8. Papaioannou AI, Kostikas K, Kollia P, Gourgoulianis KI. Clinical implications for vascular endothelial growth factor in the lung: friend or foe?. Respir Res. 2006;7:1–13
  9. Matsuyama W, Hashiguchi T, Mizoguchi A, Fumiyuki , Iwami F, Kawabata M, et al. Serum levels of vascular endothelial growth factor depends on the stage of progression lung cancer. Chest. 2000;118:948–951
  10. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol. 2006;290:209–221
  11. O’Byrne KJ, Koukourakis MI, Giatromanolaki A, Cox G, Turley H, Steward WP, et al. Vascular endothelial growth factor, platelet-derived endothelial cell growth factor and angiogenesis in non-small-cell lung cancer. Br J Cancer. 2000;82(8):1427–1432
  12. Ludovini V, Gregorc V, Pistola L, Mihaylova Z, Floriani I, Darwish S, et al. Vascular endothelial growth factor, p53, Rb, Bcl-2 expression and response to chemotherapy in advanced non-small cell lung cancer. Lung Cancer. 2004;46(1):77–85
  13. Cheung N, Wong MP, Yuen ST, Leung SY, Chung LP. Tissue-specific expression pattern of vascular endothelial growth factor isoforms in the malignant transformation of lung and colon. Hum Pathol. 1998;29(9):910–914
  14. Takigawa N, Segawa Y, Fujimoto N, Hotta K, Eguchi K. Elevated vascular endothelial growth factor levels in sera of patients with lung cancer. Anticancer Res. 1998;18(2B):1251–1254
  15. Wong M, Chan S, Fu K, Leung S, Cheung N, Yuen S, et al. The angiopoietins, tie2 and vascular endothelial growth factor are differentially expressed in the transformation of normal lung to non-small cell lung carcinomas. Lung Cancer. 2000;29:11–22
  16. Fontanini G, Boldrini L, Chine S, Pisaturo F, Basolo F, Calcinai A, et al. Expression of vascular endothelial growth factor mRNA in non-small-cell lung carcinomas. BJC. 1999;79(2):363–369
  17. Yuan A, Yu c , Luh K, Chen W, Lin F, Kuo S, et al. Quantification of VEGF mRNA expression in non-small cell lung cancer using a real-time quantitative reverse transcription-PCR assay and a comparison with quantitative reverse transcription-PCR. Lab Invest. 2000;80(11):1671–1680
  18. Ohta Y, Endo Y, Tanaka M, Shimizu J, Oda M, Hayashi Y, et al. Significance of vascular endothelial growth factor messenger RNA expression in primary lung cancer. Clin Cancer Res. 1996;2:1411–1416
  19. Kishiro I, Kato S, Fuse D, Yoshida T, Machida S, Kaneko N. Clinical significance of vascular endothelial growth factor in patients with primary lung cancer. Respirology. 2002;7(2):93–98
  20. Cressey R, Wattananupong O, Lertprasertsuke N, Vinitketkumnuen U. Alteration of protein expression pattern of vascular endothelial growth factor (VEGF) from soluble to cell-associated isoform during tumourigenesis. BMC Cancer. 2005;5(128):1–8
  21. Kondo S, Asano M, Matsuo K, Ohmori I, Suzuki H. Vascular endothelial growth factor/vascular permeability factor is detectable in the sera of tumor-bearing mice and cancer patients. Biochim Biophys Acta. 1994;1221(2):211–214
  22. Tas F, Duranyildiz D, Oguz H, Camlica H, Yasasever V, Topuz E. Serum vascular endothelial growth factor (VEGF) and Bcl-2 levels in advanced stage non-small cell lung cancer. Cancer Invest. 2006;24:576–580
  23. Laack E, Kohler A, Kugler C, Dierlamm T, Knuffmann C, Vohwinkel G, et al. Pretreatment serum levels of matrix metalloproteinase-9 and vascular endothelial growth factor in non-small-cell lung cancer. Ann Oncol. 2002;13:1550–1557
  24. Suzuki M, Iizasa T, Ko E, Baba M, Saitoh Y, Shibuya K, et al. Serum endostatin correlates with progression and prognosis of non-small cell lung cancer. Lung Cancer. 2002;35(1):29–34
  25. Kaya A, Ciledag A, Gulbay BE, Poyraz BM, Celik G, Sen E, et al. The prognostic significance of vascular endothelial growth factor levels in sera of non-small cell lung cancer patients. Respir Med. 2004;98(7):632–636
  26. Shimanuki Y, Takahashi K, Cui R, Hori S, Takahashi F, Miyamoto H, et al. Role of serum vascular endothelial growth factor in the prediction of angiogenesis and prognosis for non-small cell lung cancer. Lung. 2005;183(1):29–42
  27. Laack E, Scheffler A, Burkholder I, Boeters I, Andritzky B, Schuch G, et al. Pretreatment vascular endothelial growth factor (VEGF) and matrix metalloproteinase-9 (MMP-9) serum levels in patients with metastatic non-small cell lung cancer (NSCLC). Lung Cancer. 2005;50(1):51–58
  28. Salven P, Ruotsalainen T, Mattson K, Joensuu H. High pre-treatment serum level of vascular endothelial growth factor (VEGF) is associated with poor outcome in small-cell lung cancer. Int J Cancer. 1998;79(2):144–146
  29. Niklińska W, Burzykowski T, Chyczewski L, Nikliński J. Expression of vascular endothelial growth factor (VEGF) in non-small cell lung cancer (NSCLC): association with p53 gene mutation and prognosis. Lung Cancer. 2001;34:S59–S64
  30. Brattström D, Bergqvist M, Hesselius P, Larsson A, Lamberg K, Wernlund J, et al. Elevated preoperative serum levels of angiogenic cytokines correlate to larger primary tumours and poorer survival in non-small cell lung cancer patients. Lung Cancer 2002. 2002;37:57–63
  31. Han H, Silverman JF, Santucci TS, Macherey RS, d’Amato TA, Tung MY, et al. Vascular endothelial growth factor expression in stage I non-small cell lung cancer correlates with neoangiogenesis and a poor prognosis. Ann Surg Oncol. 2001;8(1):72–79
  32. Fontanini G, Vignati S, Boldrini L, Chinè S, Silvestri V, Lucchi M, et al. Vascular endothelial growth factor is associated with neovascularization and influences progression of non-small cell lung carcinoma. Clin Cancer Res. 1997;3(6):861–865
  33. Volm M, Koomägi R, Mattern J. Prognostic value of vascular endothelial growth factor and its receptor Flt-1 in squamous cell lung cancer. Int J Cancer. 1997;74(1):64–68
  34. Imoto H, Osaki T, Taga S, Ohgami A, Ichiyoshi Y, Yasumoto K. Vascular endothelial growth factor expression in non-small-cell lung cancer: prognostic significance in squamous cell carcinoma. J Thorac Cardiovasc Surg. 1998;115(5):1007–1014
  35. Brattström D, Bergqvist M, Larsson A, Holmertz J, Hesselius P, Rosenberg L, et al. Basic fibroblast growth factor and vascular endothelial growth factor in sera from non-small cell lung cancer patients. Anticancer Res. 1998;18(2A):1123–1127
  36. Kim KJ, Li B, Winer J, Armanini M, Gillett N, Phillips HS, et al. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature. 1993;362(6423):841–844
  37. Skobe M, Rockwell P, Goldstein N, Vosseler S, Fusenig NE. Halting angiogenesis suppresses carcinoma cell invasion. Nat Med. 1997;3(11):1222–1227
  38. Ilhan N, Ilhan N, Deveci F. Functional significance of vascular endothelial growth factor and its receptor (receptor-1) in various lung cancer types. Clin Biochem. 2004;37(9):840–845
  39. Termaat MF, Den Boer FC, Bakker FC, Patka P, Haarman HJ. Bone morphogenetic proteins development and clinical efficacy in the treatment of fractures and bone defects. J Bone Joint Surg Am. 2005;87:1367–1378
  40. Ducy P, Karsenty G. The family of bone morphogenetic proteins. Kidney Int. 2000;57:2207–2214
  41. Dimitriou R, Giannoudis PV. Discovery and development of BMPs. Injury Int J Care Injured. 2005;36S:28S–33S
  42. Hay E, Lemonnier J, Fromigue O, Marie PJ. Bone morphogenetic protein-2 promotes osteoblast apoptosis through a smad-independent, protein kinase C-dependent signaling pathway. J Biol Chem. 2001;276(3):29028–29036
  43. Langenfeld EM, Bojnowski J, Perone J, Langenfeld J. Expression of bone morphogenetic proteins in human lung carcinomas. Ann Thorac Surg. 2005;80:1028–1032
  44. Raida M, Heymann AC, Gunter C, Niederwieser D. Role of bone morphogenetic protein 2 in the crosstalk between endothelial progenitor cells and mesenchymal stem cells and mesenchymal endothelial progenitor stem cells. Int J Mol Med. 2006;18:735–739
  45. Warburtona D, Schwarzb M, Tefftc D, Flores-Delgadoa G, Andersona KD, Cardoso WV. The molecular basic of lung morphogenesis. Mech Dev. 2000;92:55–81
  46. Langenfeld EM, Langenfeld J. Bone morphogenetic protein-2 stimulates angiogenesis in developing tumors. Mol Cancer Res. 2004;2:141–149
  47. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem. 1999;274(28):19838–19845
  48. Deckers ML, Bezooijen RL, Horst G, Hoogendam J, Bent C, Papapoulos SE, et al. BMPs stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology. 2002;143(4):1545–1615
  49. Kozawa O, Matsuno H, Uematsu T. Involvement of p70 S6 kinase in bone morphogenetic protein signaling: vascular endothelial growth factor synthesis by bone morphogenetic protein-4 in osteoblasts. J Cell Biochem. 2001;81(3):430–436
  50. Cunningham NS, Paralkarp V, Reddi AH. Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor β1 mRNA expression. Proc Natl Acad Sci. 1992;89:11740–11744
  51. White ES, Strom SRB, Wys NL, Arenberg DA. Non-small cell lung cancer cells induce monocytes to increase expression of angiogenic activity. J Immunol. 2001;166:7549–7555
  52. Langenfeld EM, Calvano SE, Abou-Nukta F, Lowry SF, Amenta P, Langenfeld J. The mature bone morphogenetic protein-2 is aberrantly expressed in non-small cell lung carcinomas and stimulates tumor growth of A549 cells. Carcinogenesis. 2003;24(9):1445–1454
  53. Shields PG, Harris CC. Cancer risk and low-penetrance susceptibility genes in gene-environment interactions. J Clin Oncol. 2000;18:2309–2323
  54. Mohrenweiser HW, Jones IM. Variation in DNA repair is a factor in cancer susceptibility a paradigm for the promises and perils of individual and population risk estimation?. Mutat Res. 1998;400(1–2):15–24
  55. Lee SJ, Lee SY, Jeon HS, Park SH, Jang JS, Lee GY, et al. Vascular endothelial growth factor gene polymorphisms and risk of primary lung cancer. Cancer Epidemiol Biomarkers Prev. 2005;14(3):571–575
  56. Chae YS, Kim JG, Sohn SK, Cho YY, Moon JH, Bae H, et al. Investigation of vascular endothelial growth factor gene polymorphisms and its association with clinicopathologic characteristics in gastric cancer. Oncology. 2006;71:266–272
  57. Watson CJ, Webb NJA, Bottomley MJ, Brenchley PCE. Identification of polymorphisms within the vascular endothelial growth factor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine. 2000;12(8):1232–1235
  58. Ku KT, Wan L, Peng HC, Tsai MH, Tsai CH, Tsai FJ. Vascular endothelial growth factor gene-460 C/T polymorphism is a biomarker for oral cancer. Oral Oncol. 2005;41(5):497–502
  59. Lin CC, Wu HC, Tsai FJ, Chen HY, Chen WC. Vascular endothelial growth factor gene-460 C/T polymorphism is a biomarker for prostate cancer. Urology. 2003;62(2):374–377
  60. Howell WM, Bateman AC, Turner SJ, Collins A, Theaker JM. Influence of vascular endothelial growth factor single nucleotide polymorphisms on tumour development in cutaneous malignant melanoma. Genes Immun. 2002;3(4):229–232
  61. Han SW, Kim GW, Seo JS, Kim SJ, Sa KH, Park JY, et al. VEGF gene polymorphisms and susceptibility to rheumatoid arthritis. Rheumatology. 2004;43:1173–1177
  62. Mountain CF. Revisions in the international system for staging lung cancer. Chest. 1997;111:1710–1717
  63. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem. 1987;162(1):156–159
  64. Livak KJ, Schmittgen TD . Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25:402–408
  65. Matsuyama K, Chiba Y, Sasaki M, Tanaka H, Muraoka R, Tanigawa N. Tumor angiogenesis as a prognostic marker in operable non-small cell lung cancer. Ann Thorac Surg. 1998;65:1405–1409
  66. Langenfeld EM, Kong Y, Langenfeld J. Bone morphogenetic protein 2 stimulation of tumor growth involves the activation of Smad-1/5. Oncogene. 2006;25:685–692
  67. Rothhammer T, Poser I, Soncin F, Bataille F, Moser M, Bosserhoff A. Bone morphogenic proteins are overexpressed in malignant melanoma and promote cell invasion and migration. Cancer Res. 2005;65(2):448–456
  68. Zimmerman LB, De Jesús-Escobar JM, Harland RM. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell. 1996;86(4):599–606
  69. Raju GP, Dimova N, Klein P, Huang H. SANE, a novel LEM domain protein, regulates bone morphogenetic protein signaling through interaction with smad1. J Biol Chem. 2003;278(1):428–437
  70. Buckley S, Shi W, Driscoll B, Ferrario A, Anderson K, Warburton D. BMP4 signaling induces senescence and modulates the oncogenic phenotype of A549 lung adenocarcinoma cells. Am J Physiol Lung Cell Mol Physiol. 2004;286:L81–L86
  71. Banks RE, Forbes MA, Kinsey SE, Stanley A, Ingham E, Walters C, et al. Release of the angiogenic cytokine vascular endothelial growth factor (VEGF) from platelets: significance for VEGF measurements and cancer biology. Br J Cancer. 1998;77(6):956–964
  72. Hormbrey E, Gillespie P, Turner K, Han C, Roberts A, McGrouther D, et al. A critical review of vascular endothelial growth factor (VEGF) analysis in peripheral blood: is the current literature meaningful?. Clin Exp Metastasis. 2002;19(8):651–663
  73. Lee JK, Hong YJ, Han CJ, Hwang DY, Hong SI. Clinical usefulness of serum and plasma vascular endothelial growth factor in cancer patients: which is the optimal specimen?. Int J Oncol. 2000;17(1):149–152
  74. Choi J, Kim H, Lim H, Nam D, Kim H, Yi J, et al. Vascular endothelial growth factor in the serum of patients with non-small cell lung cancer: correlation with platelet and leukocyte counts. Lung cancer. 2001;33:171–179
  75. Verheul HM, Pinedo HM. Tumor growth: a putative role for platelets?. Oncologist. 1998;3(2):II znaleźć cytowania
  76. Jefferson MF, Pendleton N, Faragher EB, Dixon GR, Myskow MW, Horan MA. ‘Tumour volume’ as a predictor of survival after resection of non-small-cell lung cancer (NSCLC). Br J Cancer. 1996;74(3):456–459
  77. Stevens A, Soden J, Brenchley PE, Ralph S, Ray DW. Haplotype analysis of the polymorphic human vascular endothelial growth factor gene promoter. Cancer Res. 2003;63:812–816
  78. Kim JK, Oh D, Kwak SY, Han JH, Chung YS, Kim NK. Genetic polymorphism of vascular endothelial growth factor (VEGF C936T) in the korean population. Korean J Biol Sci. 2003;7:261–264
  79. Renner W, Kotschan S, Hoffmann C, Obermayer-Pietsch B, Pilger E. A common 936 CT mutation in the gene for vascular endothelial growth factor is associated with vascular endothelial growth factor plasma levels. J Vasc Res. 2000;37:443–448
  80. Krippl P, Langsenlehner U, Renner W, Yazdani-Biuki B, Wolf G, Wascher TC, et al. A common 936 C/T gene polymorphism of vascular endothelial growth factor is associated with decreased breast cancer risk. Int J Cancer. 2003;106(4):468–471
  81. Awata T, Inoue K, Kurihara S, Ohkubo T, Watanabe M, Inukai K, et al. A common polymorphism in the 5′-untranslated region of the VEGF gene is associated with diabetic retinopathy in type 2 diabetes. Diabetes. 2002;51:1635–1639

PII: S0169-5002(09)00119-6

doi: 10.1016/j.lungcan.2009.02.020

Lung Cancer
Volume 66, Issue 3 , Pages 319-326 , December 2009