Taiwanese Journal of Obstetrics and Gynecology
Volume 44, Issue 2 , Pages 128-138 , June 2005

Angiogenesis, Thrombospondin-1 and Cervical Carcinogenesis

  • Ming-Ping Wu

      Affiliations

    • Department of Obstetrics and Gynecology, Chi Mei Foundation Hospital, Tainan, Taipei, Taiwan
    • Department of Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan, Taipei, Taiwan
    • Department of Obstetrics and Gynecology, National Cheng Kung University Hospital, Tainan, Taiwan
    • ,
  • Cheng-Yang Chou

      Affiliations

    • Department of Obstetrics and Gynecology, National Cheng Kung University Hospital, Tainan, Taiwan
    • College of Medicine, Taipei Medical University, Taipei, Taiwan
    • Corresponding Author InformationCorrespondence to: Dr. Cheng-Yang Chou, Department of Obstetrics and Gynecology, National Cheng Kung University Hospital, 138 Sheng-Li Road, Tainan 704, Taiwan

Received 23 February 2005 ,Revised 7 March 2005 ,Accepted 8 March 2005.

References 

  1. Risau W . Mechanisms of angiogenesis . Nature . 1997;386:671–674
  2. Hanahan D , Folkman J . Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis . Cell . 1996;86:353–364
  3. Bussolino F , Mantovani A , Persico G . Molecular mechanisms of blood vessel formation . Trends Biochem Sci . 1997;22:251–256
  4. Jendraschak E , Sage EH . Regulation of angiogenesis by SPARC and angiostatin: implications for tumor cell biology . Semin Cancer Biol . 1996;7:139–146
  5. Folkman J . Tumor angiogenesis: therapeutic implications . N Engl J Med . 1971;285:1182–1186
  6. Folkman J . The role of angiogenesis in tumor growth . Semin Cancer Biol . 1992;3:65–71
  7. Watnick RS , Cheng YN , Rangarajan A , Ince TA , Weinberg RA . Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis . Cancer Cell . 2003;3:219–231
  8. Udagawa T , Fernandez A , Achilles EG , Folkman J , D'Amato RJ . Persistence of microscopic human cancers in mice: alterations in the angiogenic balance accompanies loss of tumor dormancy . FASEB J . 2002;16:1361–1370
  9. Folkman J . Fundamental concepts of the angiogenic process . Curr Mol Med . 2003;3:643–651
  10. Achilles EG , Fernandez A , Allred EN , et al.   Heterogeneity of angiogenic activity in a human liposarcoma: a proposed mechanism for “no take” of human tumors in mice . J Natl Cancer Inst . 2001;93:1075–1081
  11. Shing Y , Folkman J , Sullivan R , Butterfield C , Murray J , Klagsbrun M . Heparin affinity: purification of a tumor-derived capillary endothelial cell growth factor . Science . 1984;223:1296–1299
  12. O'Reilly MS , Holmgren L , Shing Y , et al.   Angiostatin: a circulating endothelial cell inhibitor that suppresses angiogenesis and tumor growth . Cold Spring Harb Symp Quant Biol . 1994;59:471–482
  13. O'Reilly MS , Boehm T , Shing Y , et al.   Endostatin: an endogenous inhibitor of angiogenesis and tumor growth . Cell . 1997;88:277–285
  14. Maeshima Y , Sudhakar A , Lively JC , et al.   Tumstatin, an endothelial cell-specific inhibitor of protein synthesis . Science . 2002;295:140–143
  15. Bouck N . Tumor angiogenesis: the role of oncogenes and tumor suppressor genes . Cancer Cells . 1990;2:179–185
  16. Rastinejad F , Polverini PJ , Bouck NP . Regulation of the activity of a new inhibitor of angiogenesis by a cancer suppressor gene . Cell . 1989;56:345–355
  17. Kerbel R , Folkman J . Clinical translation of angiogenesis inhibitors . Nat Rev Cancer . 2002;2:727–739
  18. Rice A , Quinn CM . Angiogenesis, thrombospondin, and ductal carcinoma in situ of the breast . J Clin Pathol . 2002;55:569–574
  19. Folkman J , Hahnfeldt P , Hlatky L . Cancer: looking outside the genome . Nat Rev Mol Cell Biol . 2000;1:76–79
  20. Franck-Lissbrant I , Haggstrom S , Damber JE , Bergh A . Testosterone stimulates angiogenesis and vascular regrowth in the ventral prostate in castrated adult rats . Endocrinology . 1998;139:451–456
  21. Folkman J . Is tissue mass regulated by vascular endothelial cells? Prostate as the first evidence . Endocrinology . 1998;139:441–442
  22. Folkman J . Tumor angiogenesis and tissue factor . Nat Med . 1996;2:167–168
  23. Hahnfeldt P , Panigrahy D , Folkman J , Hlatky L . Tumor development under angiogenic signaling: a dynamical theory of tumor growth, treatment response, and postvascular dormancy . Cancer Res . 1999;59:4770–4775
  24. Folkman J . Angiogenesis and apoptosis . Semin Cancer Biol . 2003;13:159–167
  25. Ellenson LH , Wu TC . Focus on endometrial and cervical cancer . Cancer Cell . 2004;5:533–538
  26. Pinto AP , Crum CP . Natural history of cervical neoplasia: defining progression and its consequence . Clin Obstet Gynecol . 2000;43:352–362
  27. Bremer GL , Tiebosch AT , van der Putten HW , Schouten HJ , de Haan J , Arends JW . Tumor angiogenesis: an independent prognostic parameter in cervical cancer . Am J Obstet Gynecol . 1996;174:126–131
  28. Sotiropoulou M , Diakomanolis E , Elsheikh A , Loutradis D , Markaki S , Michalas S . Angiogenic properties of carcinoma in situ and microinvasive carcinoma of the uterine cervix . Eur J Gynaecol Oncol . 2004;25:219–221
  29. Hockel M , Schlenger K , Aral B , Mitze M , Schaffer U , Vaupel P . Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix . Cancer Res . 1996;56:4509–4515
  30. West CM , Cooper RA , Loncaster JA , Wilks DP , Bromley M . Tumor vascularity: a histological measure of angiogenesis and hypoxia . Cancer Res . 2001;61:2907–2910
  31. Cantu De Leon D , Lopez-Graniel C , Frias Mendivil M , Chanona Vilchis G , Gomez C , De La Garza Salazar J . Significance of microvascular density (MVD) in cervical cancer recurrence . Int J Gynecol Cancer . 2003;13:856–862
  32. Siracha E , Sirachy J , Pappova N . Vascularization and radiocurability in cancer of the uterine cervix . Neoplasma . 1994;29:183–188
  33. Kohno Y , Iwanari O , Kitao M . Prognostic importance of histologic vascular density in cervical cancer treated with hypertensive intraarterial chemotherapy . Cancer . 1993;72:2394–2400
  34. Smith-McCune KK , Weidner N . Demonstration and characterization of the angiogenic properties of cervical dysplasia . Cancer Res . 1994;54:800–804
  35. Abulafia O , Triest WE , Sherer DM . Angiogenesis in malignancies of the female genital tract . Gynecol Oncol . 1999;72:220–231
  36. Abulafia O , Triest WE , Sherer DM . Angiogenesis in squamous cell carcinoma in situ and microinvasive carcinoma of the uterine cervix . Obstet Gynecol . 1996;88:927–932
  37. Wu MP , Tzeng CC , Wu LW , Huang KF , Chou CY . Thrombospondin-1 acts as a fence to inhibit angiogenesis that occurs during cervical carcinogenesis . Cancer J . 2004;10:27–32
  38. Weidner N , Folkman J , Pozza F , et al.   Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma . J Natl Cancer Inst . 1992;84:1875–1887
  39. Hlatky L , Hahnfeldt P , Folkman J . Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us . J Natl Cancer Inst . 2002;94:883–893
  40. Weber WA , Haubner R , Vabuliene E , Kuhnast B , Wester HJ , Schwaiger M . Tumor angiogenesis targeting using imaging agents . Q J Nucl Med . 2001;45:179–182
  41. Di Leo S , Caschetto S , Garozzo G , et al.   Angiogenesis as a prognostic factor in cervical carcinoma . Eur J Gynaecol Oncol . 1998;19:158–162
  42. Dellas A , Moch H , Schultheiss E , et al.   Angiogenesis in cervical neoplasia: microvessel quantitation in precancerous lesions and invasive carcinomas with clinicopathological correlations . Gynecol Oncol . 1997;67:27–33
  43. Rutgers JL , Mattox TF , Vargas MP . Angiogenesis in uterine cervical squamous cell carcinoma . Int J Gynecol Pathol . 1995;14:114–118
  44. Graflund M , Sorbe B , Hussein A , Bryne M , Karlsson M . The prognostic value of histopathologic grading parameters and microvessel density in patients with early squamous cell carcinoma of the uterine cervix . Int J Gynecol Cancer . 2002;12:32–41
  45. Vieira SC , Zeferino LC , Da Silva BB , et al.   Quantification of angiogenesis in cervical cancer: a comparison among three endothelial cell markers . Gynecol Oncol . 2004;93:121–124
  46. Eberhard A , Kahlert S , Goede V , Hemmerlein B , Plate KH , Augustin HG . Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies . Cancer Res . 2000;60:1388–1393
  47. Hlatky L , Tsionou C , Hahnfeldt P , Coleman CN . Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor upregulation and protein expression . Cancer Res . 1994;54:6083–6086
  48. Mayr NA , Hawighorst H , Yuh WT , Essig M , Magnotta VA , Knopp MV . MR microcirculation assessment in cervical cancer: correlations with histomorphological tumor markers and clinical outcome . J Magn Reson Imaging . 1999;10:267–276
  49. Cheng WF , Lee CN , Chu JS , et al.   Vascularity index as a novel parameter for the in vivo assessment of angiogenesis in patients with cervical carcinoma . Cancer . 1999;85:651–657
  50. Hsu KF , Su JM , Huang SC , et al.   Three-dimensional power Doppler imaging of early-stage cervical cancer . Ultrasound Obstet Gynecol . 2004;24:664–671
  51. Cooper RA , Carrington BM , Loncaster JA , et al.   Tumour oxygenation levels correlate with dynamic contrast-enhanced magnetic resonance imaging parameters in carcinoma of the cervix . Radiother Oncol . 2000;57:53–59
  52. Ueda T , Yuh WT , Taoka T . Clinical application of perfusion and diffusion MR imaging in acute ischemic stroke . J Magn Reson Imaging . 1999;10:305–309
  53. Hawighorst H . Dynamic MR imaging in cervical carcinoma . Radiology . 1999;213:617–618
  54. Guedez L , Rivera AM , Salloum R , et al.   Quantitative assessment of angiogenic responses by the directed in vivo angiogenesis assay . Am J Pathol . 2003;162:1431–1439
  55. Kerbel RS , Kamen BA . The anti-angiogenic basis of metronomic chemotherapy . Nat Rev Cancer . 2004;4:423–436
  56. Guidolin D , Vacca A , Nussdorfer GG , Ribatti D . A new image analysis method based on topological and fractal parameters to evaluate the angiostatic activity of docetaxel by using the Matrigel assay in vitro . Microvasc Res . 2004;67:117–124
  57. Senger DR , Brown LF , Claffey KP , Dvorak HF . Vascular permeability factor, tumor angiogenesis and stroma generation . Invasion Metastasis . 1994;14:385–394
  58. Guidi AJ , Abu-Jawdeh G , Berse B , et al.   Vascular permeability factor (vascular endothelial growth factor) expression and angiogenesis in cervical neoplasia . J Natl Cancer Inst . 1995;87:1237–1245
  59. Dobbs SP , Hewett PW , Johnson IR , Carmichael J , Murray JC . Angiogenesis is associated with vascular endothelial growth factor expression in cervical intraepithelial neoplasia . Br J Cancer . 1997;76:1410–1415
  60. Cheng WF , Chen CA , Lee CN , Wei LH , Hsieh FJ , Hsieh CY . Vascular endothelial growth factor and prognosis of cervical carcinoma . Obstet Gynecol . 2000;96:721–726
  61. Raleigh JA , Calkins-Adams DP , Rinker LH , et al.   Hypoxia and vascular endothelial growth factor expression in human squamous cell carcinomas using pimonidazole as a hypoxia marker . Cancer Res . 1998;58:3765–3768
  62. Wolf JK , Ramirez PT . The molecular biology of cervical cancer . Cancer Invest . 2001;19:621–629
  63. Baenziger NL , Brodie GN , Majerus PW . A thrombin-sensitive protein of human platelet membranes . Proc Natl Acad Sci USA . 1971;68:240–243
  64. Lawler J . The functions of thrombospondin-1 and -2 . Curr Opin Cell Biol . 2000;12:634–640
  65. Tolsma SS , Volpert OV , Good DJ , Frazier WA , Polverini PJ , Bouck N . Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity . J Cell Biol . 1993;122:497–511
  66. Qian X , Wang TN , Rothman VL , Nicosia RF , Tuszynski GP . Thrombospondin-1 modulates angiogenesis in vitro by upregulation of matrix metalloproteinase-9 in endothelial cells . Exp Cell Res . 1997;235:403–412
  67. Streit M , Velasco P , Brown LF , et al.   Overexpression of thrombospondin-1 decreases angiogenesis and inhibits the growth of human cutaneous squamous cell carcinomas . Am J Pathol . 1999;155:441–452
  68. Folkman J . Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis . N Engl J Med . 1995;333:1757–1763
  69. Hawighorst T , Velasco P , Streit M , et al.   Thrombospondin-2 plays a protective role in multistep carcinogenesis: a novel host anti-tumor defense mechanism . EMBO J . 2001;20:2631–2640
  70. Kwak C , Jin RJ , Lee C , Park MS , Lee SE . Thrombospondin-1, vascular endothelial growth factor expression and their relationship with p53 status in prostate cancer and benign prostatic hyperplasia . BJU Int . 2002;89:303–309
  71. Rak J , Yu JL , Klement G , Kerbel RS . Oncogenes and angiogenesis: signaling three-dimensional tumor growth . J Investig Dermatol Symp Proc . 2000;5:24–33
  72. Dameron KM , Volpert OV , Tainsky MA , Bouck N . Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1 . Science . 1994;265:1582–1584
  73. Zhang L , Yu D , Hu M , et al.   Wild-type p53 suppresses angiogenesis in human leiomyosarcoma and synovial sarcoma by transcriptional suppression of vascular endothelial growth factor expression . Cancer Res . 2000;60:3655–3661
  74. Campbell SC , Volpert OV , Ivanovich M , Bouck NP . Molecular mediators of angiogenesis in bladder cancer . Cancer Res . 1998;58:1298–1304
  75. Jin RJ , Kwak C , Lee SG , et al.   The application of an antiangiogenic gene (thrombospondin-1) in the treatment of human prostate cancer xenografts . Cancer Gene Ther . 2000;7:1537–1542
  76. Sheibani N , Frazier WA . Thrombospondin-1, PECAM-1, and regulation of angiogenesis . Histol Histopathol . 1999;14:285–294
  77. Kodama J , Hashimoto I , Seki N , et al.   Thrombospondin-1 and -2 messenger RNA expression in invasive cervical cancer: correlation with angiogenesis and prognosis . Clin Cancer Res . 2001;7:2826–2831
  78. Feldman AL , Pak H , Yang JC , Alexander HR , Libutti SK . Serum endostatin levels are elevated in patients with soft tissue sarcoma . Cancer . 2001;91:1525–1529
  79. Feldman AL , Alexander HR , Bartlett DL , et al.   A prospective analysis of plasma endostatin levels in colorectal cancer patients with liver metastases . Ann Surg Oncol . 2001;8:741–745
  80. Feldman AL , Alexander HR , Yang JC , et al.   Prospective analysis of circulating endostatin levels in patients with renal cell carcinoma . Cancer . 2002;95:1637–1643
  81. Feldman AL , Tamarkin L , Paciotti GF , et al.   Serum endostatin levels are elevated and correlate with serum vascular endothelial growth factor levels in patients with stage IV clear cell renal cancer . Clin Cancer Res . 2000;6:4628–4634
  82. Ozatli D , Kocoglu H , Haznedaroglu IC , et al.   Circulating thrombomodulin, thrombospondin, and fibronectin in acute myeloblastic leukemias . Haematologia (Budap) . 1999;29:277–283
  83. Kuroi K , Toi M . Circulating angiogenesis regulators in cancer patients . Int J Biol Markers . 2001;16:5–26
  84. Libutti SK . Do angiogenesis inhibitors perform a physiologic gatekeeper role in cancer prevention? . Cancer J . 2004;10:12–14
  85. Bisacchi D , Benelli R , Vanzetto C , Ferrari N , Tosetti F , Albini A . Anti-angiogenesis and angioprevention: mechanisms, problems and perspectives . Cancer Detect Prev . 2003;27:229–238
  86. Kalluri R . Basement membranes: structure, assembly and role in tumour angiogenesis . Nat Rev Cancer . 2003;3:422–433
  87. Bornstein P , Kyriakides TR , Yang Z , Armstrong LC , Birk DE . Thrombospondin 2 modulates collagen fibrillogenesis and angiogenesis . J Investig Dermatol Symp Proc . 2000;5:61–66
  88. Stetler-Stevenson WG . Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention . J Clin Invest . 1999;103:1237–1241
  89. Zetter BR . Cell motility in angiogenesis and tumor metastasis . Cancer Invest . 1990;8:669–671
  90. Liotta LA , Thorgeirsson UP , Garbisa S . Role of collagenases in tumor cell invasion . Cancer Metastasis Rev . 1982;1:277–288
  91. Bergers G , Brekken R , McMahon G , et al.   Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis . Nat Cell Biol . 2000;2:737–744
  92. Albo D , Shinohara T , Tuszynski GP . Up-regulation of matrix metalloproteinase 9 by thrombospondin 1 in gastric cancer . J Surg Res . 2002;108:51–60
  93. Kerbel RS , Yu J , Tran J , et al.   Possible mechanisms of acquired resistance to anti-angiogenic drugs: implications for the use of combination therapy approaches . Cancer Metastasis Rev . 2001;20:79–86
  94. Gasparini G . Metronomic scheduling: the future of chemotherapy? . Lancet Oncol . 2001;2:733–740
  95. Fidler IJ , Ellis LM . Chemotherapeutic drugs – more really is not better . Nat Med . 2000;6:500–502
  96. St Croix B , Rago C , Velculescu V , et al.   Genes expressed in human tumor endothelium . Science . 2000;289:1197–1202
  97. Klement G , Baruchel S , Rak J , et al.   Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity . J Clin Invest . 2000;105:R15–R24
  98. Browder T , Butterfield CE , Kraling BM , et al.   Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer . Cancer Res . 2000;60:1878–1886
  99. Boehm T , Folkman J , Browder T , O'Reilly MS . Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance . Nature . 1997;390:404–407
  100. Miller KD , Sweeney CJ , Sledge GW . Redefining the target: chemotherapeutics as antiangiogenics . J Clin Oncol . 2001;19:1195–1206
  101. Hanahan D , Bergers G , Bergsland E . Less is more, regularly: metronomic dosing of cytotoxic drugs can target tumor angiogenesis in mice . J Clin Invest . 2000;105:1045–1047
  102. O'Leary JJ , Shapiro RL , Ren CJ , Chuang N , Cohen HW , Potmesil M . Antiangiogenic effects of camptothecin analogues 9-amino-20(S)-camptothecin, topotecan, and CPT-11 studied in the mouse cornea model . Clin Cancer Res . 1999;5:181–187
  103. Presta M , Rusnati M , Belleri M , Morbidelli L , Ziche M , Ribatti D . Purine analogue 6-methylmercaptopurine riboside inhibits early and late phases of the angiogenesis process . Cancer Res . 1999;59:2417–2424
  104. Wang J , Lou P , Lesniewski R , Henkin J . Paclitaxel at ultra low concentrations inhibits angiogenesis without affecting cellular microtubule assembly . Anticancer Drugs . 2003;14:13–19
  105. Bertolini F , Paul S , Mancuso P , et al.   Maximum tolerable dose and low-dose metronomic chemotherapy have opposite effects on the mobilization and viability of circulating endothelial progenitor cells . Cancer Res . 2003;63:4342–4346
  106. Bocci G , Francia G , Man S , Lawler J , Kerbel RS . Thrombospondin 1, a mediator of the antiangiogenic effects of low-dose metronomic chemotherapy . Proc Natl Acad Sci USA . 2003;100:12917–12922
  107. Bocci G , Nicolaou KC , Kerbel RS . Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs . Cancer Res . 2002;62:6938–6943
  108. Lyden D , Hattori K , Dias S , et al.   Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth . Nat Med . 2001;7:1194–1201
  109. Kakeji Y , Teicher BA . Preclinical studies of the combination of angiogenic inhibitors with cytotoxic agents . Invest New Drugs . 1997;15:39–48
  110. Gasparini G , Harris AL . Does improved control of tumour growth require an anti-cancer therapy targeting both neoplastic and intratumoral endothelial cells? . Eur J Cancer . 1994;30A:201–206
  111. Kamen BA , Rubin E , Aisner J , Glatstein E . High-time chemotherapy or high time for low dose . J Clin Oncol . 2000;18:2935–2937
  112. Ezzell C . Starving tumors of their lifeblood . Sci Am . 1998;279:33–34

PII: S1028-4559(09)60124-8

doi: 10.1016/S1028-4559(09)60124-8

Taiwanese Journal of Obstetrics and Gynecology
Volume 44, Issue 2 , Pages 128-138 , June 2005

Article Tools