Cancer Letters
Volume 291, Issue 2 , Pages 131-141 , 28 May 2010

Purinergic mechanisms in breast cancer support intravasation, extravasation and angiogenesis

Received 7 July 2009 ,Revised 25 September 2009 ,Accepted 29 September 2009.

References 

  1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J. Clin. 2009;
  2. Coleman MP, Quaresma M, Berrino F, Lutz JM, De AR, Capocaccia R, et al. Cancer survival in five continents: a worldwide population-based study (CONCORD). Lancet Oncol. 2008;9:730–756
  3. Hagemeister FB, Buzdar AU, Luna MA, Blumenschein GR. Causes of death in breast cancer: a clinicopathologic study. Cancer. 1980;46:162–167
  4. Rugo HS. The importance of distant metastases in hormone-sensitive breast cancer. Breast. 2008;17(Suppl. 1):S3–S8
  5. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70
  6. Retsky M, Demicheli R, Hrushesky W, Speer J, Swartzendruber D, Wardwell R. Recent translational research: computational studies of breast cancer. Breast Cancer Res. 2005;7:37–40
  7. Demicheli R, Retsky MW, Hrushesky WJ, Baum M, Gukas ID. The effects of surgery on tumor growth: a century of investigations. Ann. Oncol. 2008;19:1821–1828
  8. Retsky MW, Demicheli R, Hrushesky WJ, Baum M, Gukas ID. Dormancy and surgery-driven escape from dormancy help explain some clinical features of breast cancer. APMIS. 2008;116:730–741
  9. Hansen NM, Ye X, Grube BJ, Giuliano AE. Manipulation of the primary breast tumor and the incidence of sentinel node metastases from invasive breast cancer. Arch. Surg. 2004;139:634–639(discussion 639–640)
  10. Peters-Engl C, Konstantiniuk P, Tausch C, Haid A, Hoffmann B, Jagoutz-Herzlinger M, et al. The impact of preoperative breast biopsy on the risk of sentinel lymph node metastases: analysis of 2502 cases from the Austrian Sentinel Node Biopsy Study Group. Br. J. Cancer. 2004;91:1782–1786
  11. Demicheli R, Retsky MW, Hrushesky WJ, Baum M. Tumor dormancy and surgery-driven interruption of dormancy in breast cancer: learning from failures. Nat. Clin. Pract. Oncol. 2007;4:699–710
  12. O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Cao 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, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, et al. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell. 1994;79:315–328
  14. Zahl PH, Maehlen J, Welch HG. The natural history of invasive breast cancers detected by screening mammography. Arch. Int. Med. 2008;168:2311–2316
  15. Almog N, Ma L, Raychowdhury R, Schwager C, Erber R, Short S, et al. Transcriptional switch of dormant tumors to fast-growing angiogenic phenotype. Cancer Res. 2009;69:836–844
  16. Alix-Panabieres C, Muller V, Pantel K. Current status in human breast cancer micrometastasis. Curr. Opin. Oncol. 2007;19:558–563
  17. Erbas B, Provenzano E, Armes J, Gertig D. The natural history of ductal carcinoma in situ of the breast: a review. Breast Cancer Res. Treat. 2006;97:135–144
  18. Sanders ME, Schuyler PA, Dupont WD, Page DL. The natural history of low-grade ductal carcinoma in situ of the breast in women treated by biopsy only revealed over 30 years of long-term follow-up. Cancer. 2005;103:2481–2484
  19. Westfall DP, Sedaa KO, Shinozuka K, Bjur RA, Buxton IL. ATP as a cotransmitter. Ann. NY Acad. Sci. 1990;603:300–310
  20. Burnstock G. Purinergic signalling. Br. J. Pharamcol. 2006;147(Suppl. 1):S172–S181
  21. Burnstock G. Do some nerve cells release more than one transmitter?. Neuroscience. 1976;1:239–248
  22. Westfall DP, Stitzel RE, Rowe JN. The postjunctional effects and neural release of purine compounds in the guinea-pig vas deferens. Eur. J. Pharmacol. 1978;50:27–38
  23. Schwiebert EM, Zsembery A. Extracellular ATP as a signaling molecule for epithelial cells. Biochim. Biophys. Acta. 2003;1615:7–32
  24. Christofori G. New signals from the invasive front. Nature. 2006;441:444–450
  25. Muller WA. Leukocyte–endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 2003;24:327–334
  26. Wittchen ES. Endothelial signaling in paracellular and transcellular leukocyte transmigration. Front. Biosci. 2009;14:2522–2545
  27. Rowe RG, Weiss SJ. Breaching the basement membrane: who, when and how?. Trends Cell Biol. 2008;18:560–574
  28. Sud’ina GF, Mirzoeva OK, Galkina SI, Pushkareva MA, Ullrich V. Involvement of ecto-ATPase and extracellular ATP in polymorphonuclear granulocyte–endothelial interactions. FEBS Lett. 1998;423:243–248
  29. Ferrero ME. A new approach to the inflammatory/autoimmune diseases. Recent Pat. Antiinfect. Drug Discov. 2009;4:108–113
  30. Eltzschig HK, Eckle T, Mager A, Kuper N, Karcher C, Weissmuller T, et al. ATP release from activated neutrophils occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ. Res. 2006;99:1100–1108
  31. Yang S, Cheek DJ, Westfall DP, Buxton IL. Purinergic axis in cardiac blood vessels. Agonist-mediated release of ATP from cardiac endothelial cells. Circ. Res. 1994;74:401–407
  32. Eltzschig HK, Weissmuller T, Mager A, Eckle T. Nucleotide metabolism and cell–cell interactions. Methods Mol. Biol. 2006;341:73–87
  33. Berne RM. The role of adenosine in the regulation of coronary blood flow. Circ. Res. 1980;47:807–813
  34. Tanaka N, Nejime N, Kagota S, Kubota Y, Yudo K, Nakamura K, et al. ATP participates in the regulation of microvessel permeability. J. Pharm. Pharmacol. 2006;58:481–487
  35. Tanaka N, Kawasaki K, Nejime N, Kubota Y, Takahashi K, Hashimoto M, et al. P2Y receptor-mediated enhancement of permeation requires Ca2+ signalling in vascular endothelial cells. Clin. Exp. Pharmacol. Physiol. 2003;30:649–652
  36. McClenahan D, Hillenbrand K, Kapur A, Carlton D, Czuprynski C. Effects of extracellular ATP on bovine lung endothelial and epithelial cell monolayer morphologies, apoptoses, and permeabilities. Clin. Vaccine Immunol. 2009;16:43–48
  37. Chambers AF, MacDonald IC, Schmidt EE, Morris VL, Groom AC. Clinical targets for anti-metastasis therapy. Adv. Cancer Res. 2000;79:91–121
  38. Steinbauer M, Guba M, Cernaianu G, Kohl G, Cetto M, Kunz-Schughart LA, et al. GFP-transfected tumor cells are useful in examining early metastasis in vivo, but immune reaction precludes long-term tumor development studies in immunocompetent mice. Clin. Exp. Metast. 2003;20:135–141
  39. Schluter K, Gassmann P, Enns A, Korb T, Hemping-Bovenkerk A, Holzen J, et al. Organ-specific metastatic tumor cell adhesion and extravasation of colon carcinoma cells with different metastatic potential. Am. J. Pathol. 2006;169:1064–1073
  40. Glinsky VV, Glinsky GV, Rittenhouse-Olson K, Huflejt ME, Glinskii OV, Deutscher SL, et al. The role of Thomsen-Friedenreich antigen in adhesion of human breast and prostate cancer cells to the endothelium. Cancer Res. 2001;61:4851–4857
  41. Glinskii OV, Huxley VH, Glinsky GV, Pienta KJ, Raz A, Glinsky VV. Mechanical entrapment is insufficient and intercellular adhesion is essential for metastatic cell arrest in distant organs. Neoplasia. 2005;7:522–527
  42. Chambers AF, Naumov GN, Varghese HJ, Nadkarni KV, MacDonald IC, Groom AC. Critical steps in hematogenous metastasis: an overview. Surg. Oncol. Clin. N Am. 2001;10:243–255(vii)
  43. Miles FL, Pruitt FL, van Golen KL, Cooper CR. Stepping out of the flow: capillary extravasation in cancer metastasis. Clin. Exp. Metast. 2008;25:305–324
  44. Blay J, White TD, Hoskin DW. The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res. 1997;57:2602–2605
  45. Spychala J. Tumor-promoting functions of adenosine. Pharmacol. Ther. 2000;87:161–173
  46. Spychala J, Lazarowski E, Ostapkowicz A, Ayscue LH, Jin A, Mitchell BS. Role of estrogen receptor in the regulation of ecto-5′-nucleotidase and adenosine in breast cancer. Clin. Cancer Res. 2004;10:708–717
  47. Rumjahn SM, Javed MA, Wong N, Law WE, Buxton IL. Purinergic regulation of angiogenesis by human breast carcinoma-secreted nucleoside diphosphate kinase. Br. J. Cancer. 2007;97:1372–1380
  48. Anzinger J, Malmquist NA, Gould J, Buxton IL. Secretion of a nucleoside diphosphate kinase (Nm23-H2) by cells from human breast, colon, pancreas and lung tumors. Proc. West Pharmacol. Soc. 2001;44:61–63
  49. Oxhorn BC, Cheek DJ, Buxton IL. Role of nucleotides and nucleosides in the regulation of cardiac blood flow. AACN Clin. Issues. 2000;11:241–251
  50. Bogle RG, Coade SB, Moncada S, Pearson JD, Mann GE. Bradykinin and ATP stimulate l-arginine uptake and nitric oxide release in vascular endothelial cells. Biochem. Biophys. Res. Commun. 1991;180(2):926–932
  51. Mehta A, Orchard S. Nucleoside diphosphate kinase (NDPK, NM23, AWD): recent regulatory advances in endocytosis, metastasis, psoriasis, insulin release, fetal erythroid lineage and heart failure; translational medicine exemplified. Mol. Cell Biochem. 2009;329:3–15
  52. Bosnar MH, Bago R, Cetkovic H. Subcellular localization of Nm23/NDPK A and B isoforms: a reflection of their biological function?. Mol. Cell Biochem. 2009;329:63–71
  53. Malmquist NA, Anzinger JJ, Hirzel D, Buxton IL. Ellagic acid inhibits nucleoside diphosphate kinase-B activity. Proc. West Pharmacol. Soc. 2001;44:57–59
  54. Rumjahn SM, Baldwin KA, Buxton IL. P2y receptor-mediated angiogenesis via vascular endothelial growth factor receptor 2 signaling. Proc. West Pharmacol. Soc. 2007;50:58–60
  55. Rumjahn SM, Yokdang N, Baldwin KA, Thai J, Buxton IL. Purinergic regulation of vascular endothelial growth factor signaling in angiogenesis. Br. J. Cancer. 2009;100:1465–1470
  56. Packham MA, Ardlie NG, Mustard JF. Effect of adenine compounds on platelet aggregation. Am. J. Physiol. 1969;217(4):1009–1017
  57. Soslau G, Brodsky I, Parker J. Occupancy of P2 purinoceptors with unique properties modulates the function of human platelets. Biochim. Biophys. Acta Mol. Cell Res. 1993;1177:199–207
  58. Rubio R, Wiedmeier VT, Berne RM. Relationship between coronary flow and adenosine production and release. J. Mol. Cell Cardiol. 1974;6:561–566
  59. Gordon EL, Pearson JD, Slakey LL. The hydrolysis of extracellular adenine nucleotides by cultured endothelial cells from pig aorta. Feed-forward inhibition of adenosine production at the cell surface. J. Biol. Chem. 1986;261:15496–15507
  60. White N, Burnstock G. P2 receptors and cancer. Trends Pharmacol Sci. 2006;27:211–217
  61. Hopfner M, Lemmer K, Jansen A, Hanski C, Riecken EO, Gavish M, et al. Expression of functional P2-purinergic receptors in primary cultures of human colorectal carcinoma cells. Biochem. Biophys. Res. Commun. 1998;251:811–817
  62. Coutinho-Silva R, Stahl L, Cheung KK, de Campos NE, de Oliveira Souza C, Ojcius DM, et al. P2X and P2Y purinergic receptors on human intestinal epithelial carcinoma cells: effects of extracellular nucleotides on apoptosis and cell proliferation. Am. J. Physiol. Gastr. Liver Physiol. 2005;288:G1024–G1035
  63. Bautch VL, Ambler CA. Assembly and patterning of vertebrate blood vessels. Trends Cardiovasc. Med. 2004;14:138–143
  64. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 2004;25:581–611
  65. Jain RK. Molecular regulation of vessel maturation. Nat. Med. 2003;9:685–693
  66. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J. Clin. Oncol. 2005;23:1011–1027
  67. Folkman J. Tumor angiogenesis: therapeutic implications. New Engl. J. Med. 1971;285:1182–1186
  68. Holmgren L, O’Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med. 1995;1:149–153
  69. Duncker DJ, Bache RJ. Regulation of coronary blood flow during exercise. Physiol. Rev. 2008;88:1009–1086
  70. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1995;1:27–31
  71. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996;86:353–364
  72. Nyberg P, Xie L, Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res. 2005;65:3967–3979
  73. 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
  74. 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
  75. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer. 2003;3:401–410
  76. Kesisis G, Broxterman H, Giaccone G. Angiogenesis inhibitors. Drug selectivity and target specificity. Curr. Pharm. Des. 2007;13:2795–2809
  77. Jain RK, Duda DG, Clark JW, Loeffler JS. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat. Clin. Pract. Oncol. 2006;3:24–40
  78. Buxton ILO. Inhibition of nm23 gene product (NDPK-B) by angiostatin, polyphenols and nucleoside analogs. Proc. Western Pharmacol. Soc. 2008;51:30–34
  79. Brown AP, Citrin DE, Camphausen KA. Clinical biomarkers of angiogenesis inhibition. Cancer Metast. Rev. 2008;27:415–434
  80. Gonzalez-Angulo AM, Morales-Vasquez F, Hortobagyi GN. Overview of resistance to systemic therapy in patients with breast cancer. Adv. Exp. Med. Biol. 2007;608:1–22
  81. Poncet B, Bachelot T, Colin C, Ganne C, Jaisson-Hot I, Orfeuvre H, et al. Use of the monoclonal antibody anti-HER2 trastuzumab in the treatment of metastatic breast cancer: a cost-effectiveness analysis. Am. J. Clin. Oncol. 2008;31:363–368
  82. Kolesar JM. Bevacizumab: improved survival at what cost?. Am. J. Health Syst. Pharm. 2005;62:1017
  83. Viloria-Petit A, Crombet T, Jothy S, Hicklin D, Bohlen P, Schlaeppi JM, et al. Acquired resistance to the antitumor effect of epidermal growth factor receptor-blocking antibodies in vivo: a role for altered tumor angiogenesis. Cancer Res. 2001;61:5090–5101
  84. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer. 2008;8:592–603
  85. I. National Cancer, Angiogenesis Inhibitors in Cancer Research, 1999.
  86. I. National Cancer, SEER Cancer Statistics Review 1975–2005, 2008.
  87. Gottesman MM. Mechanisms of cancer drug resistance. Annu. Rev. Med. 2002;53:615–627
  88. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochem. Biophys. Acta. 1976;455:152–162
  89. Ueda K, Cardarelli C, Gottesman MM, Pastan I. Expression of a full-length cDNA for the human “MDR1” gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. USA. 1987;84:3004–3008
  90. Ansiaux R, Baudelet C, Jordan BF, Beghein N, Sonveaux P, De WJ, et al. Thalidomide radiosensitizes tumors through early changes in the tumor microenvironment. Clin. Cancer Res. 2005;11:743–750
  91. Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat. Med. 2001;7:987–989
  92. Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res. 2004;64:3731–3736
  93. Kruck S, Kuczyk MA, Gakis G, Kramer MW, Stenzl A, Merseburger AS. Novel therapeutic options in metastatic renal cancer – review and post ASCO 2007 update. Rev. Recent Clin. Trials. 2008;3:212–216
  94. Burnstock G. Vascular control of purines with emphasis on the coronary system. Eur. Heart J. 1989;10:15–21
  95. Buxton IL, Kaiser RA, Oxhorn BC, Cheek DJ. Evidence supporting the Nucleotide Axis Hypothesis: ATP release and metabolism by coronary endothelium. Am. J. Physiol. Heart Circ. Physiol. 2001;281:H1657–H1666
  96. Bodin P, Burnstock G. ATP-stimulated release of ATP by human endothelial cells. J. Cardiovasc. Pharm. 1996;27:872–875
  97. Ellsworth ML, Ellis CG, Goldman D, Stephenson AH, Dietrich HH, Sprague RS. Erythrocytes: oxygen sensors and modulators of vascular tone. Physiol. (Bethesda.). 2009;24:107–116
  98. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 1998;50:413–492
  99. von Kugelgen I, Wetter A. Molecular pharmacology of P2Y-receptors. N.-S. Arch. Pharmacol. 2000;362:310–323
  100. Ivanov AA, Ko H, Cosyn L, Maddileti S, Besada P, Fricks I, et al. Molecular modeling of the human P2Y2 receptor and design of a selective agonist, 2′-amino-2′-deoxy-2-thiouridine 5′-triphosphate. J. Med. Chem. 2007;50:1166–1176
  101. Jacobson KA, Costanzi S, Ohno M, Joshi BV, Besada P, Xu B, et al. Molecular recognition at purine and pyrimidine nucleotide (P2) receptors. Curr. Top. Med. Chem. 2004;4:805–819
  102. Kaczmarek E, Koziak K, Sevigny J, Siegel JB, Anrather J, Beaudoin AR, et al. Identification and characterization of CD39/vascular ATP diphosphohydrolase. J. Biol. Chem. 1996;271:33116–33122
  103. Rugonyi S. Effect of blood flow on near-the-wall mass transport of drugs and other bioactive agents: a simple formula to estimate boundary layer concentrations. J. Biomech. Eng. 2008;130:021010
  104. Gorman MW, Ogimoto K, Savage MV, Jacobson KA, Feigl EO. Nucleotide coronary vasodilation in guinea pig hearts. Am. J. Physiol. Heart Circ. Physiol. 2003;285:H1040–H1047
  105. Erlinge D, Burnstock G. P2 receptors in cardiovascular regulation and disease. Purinergic. Signal. 2008;4:1–20
  106. Gorman MW, Marble DR, Ogimoto K, Feigl EO. Measurement of adenine nucleotides in plasma. Luminescence. 2003;18:173–181
  107. Burnstock G. Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol. Rev. 2006;58:58–86
  108. George S, Dreicer R, Au JJ, Shen T, Rini BI, Roman S, et al. Phase I/II trial of 5-fluorouracil and a noncytotoxic dose level of suramin in patients with metastatic renal cell carcinoma. Clin. Genitourin. Cancer. 2008;6:79–85
  109. Smaldone MC, Gayed BA, Tomaszewski JJ, Gingrich JR. Strategies to enhance the efficacy of intravescical therapy for non-muscle invasive bladder cancer. Minerva Urol. Nefrol. 2009;61:71–89
  110. Hotz B, Buhr HJ, Hotz HG. Intravital microscopic characterization of suramin effects in an orthotopic immunocompetent rat model of pancreatic cancer. J. Gastr. Surg. 2008;12:900–906
  111. Bhargava S, Hotz B, Hines OJ, Reber HA, Buhr HJ, Hotz HG. Suramin inhibits not only tumor growth and metastasis but also angiogenesis in experimental pancreatic cancer. J. Gastr. Surg. 2007;11:171–178
  112. Suganuma M, Okabe S, Kai Y, Sueoka N, Sueoka E, Fujiki H. Synergistic effects of (--)-epigallocatechin gallate with (--)-epicatechin, sulindac, or tamoxifen on cancer-preventive activity in the human lung cancer cell line PC-9. Cancer Res. 1999;59:44–47
  113. Cao Y, Cao R. Angiogenesis inhibited by drinking tea. Nature. 1999;398:381
  114. Singh AK, Seth P, Anthony P, Husain MM, Madhavan S, Mukhtar H, et al. Green tea constituent epigallocatechin-3-gallate inhibits angiogenic differentiation of human endothelial cells. Arch. Biochem. Biophys. 2002;401:29–37
  115. Yamakawa S, Asai T, Uchida T, Matsukawa M, Akizawa T, Oku N. (-)-Epigallocatechin gallate inhibits membrane-type 1 matrix metalloproteinase, MT1-MMP, and tumor angiogenesis. Cancer Lett. 2004;210:47–55
  116. Kazi A, Wang Z, Kumar N, Falsetti SC, Chan TH, Dou QP. Structure–activity relationships of synthetic analogs of (-)-epigallocatechin-3-gallate as proteasome inhibitors. Anticancer Res. 2004;24:943–954
  117. Postel EH. Multiple biochemical activities of NM23/NDP kinase in gene regulation. J. Bioenergy Biomembr. 2003;35:31–40
  118. McDermott WG, Boissan M, Lacombe ML, Steeg PS, Horak CE. Nm23-H1 homologs suppress tumor cell motility and anchorage independent growth. Clin. Exp. Metast. 2008;25:131–138
  119. Bertheua P, Merino M, Steeg P, DeLaRosa A. NM23 protein in neoplastic and nonneoplastic thyroid tissues. Am. J. Pathol. 1994;145:26–32
  120. Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, et al. Evidence for a novel gene associated with low tumor metastatic potential. J. Nat. Cancer Inst. 1988;80(3):200–204
  121. Heimann R, Ferguson DJ, Hellman S. The relationship between nm23, angiogenesis, and the metastatic proclivity of node-negative breast cancer. Cancer Res. 1998;58:2766–2771
  122. Palmieri D, Horak CE, Lee JH, Halverson DO, Steeg PS. Translational approaches using metastasis suppressor genes. J. Bioenergy Biomembr. 2006;38:151–161
  123. Okabe-Kado J, Kasukabe T, Honma Y, Hanada R, Nakagawara A, Kaneko Y. Clinical significance of serum NM23-H1 protein in neuroblastoma. Cancer Sci. 2005;96:653–660
  124. Niitsu N, Nakamine H, Okamoto M, Tamaru JI, Hirano M. A clinicopathological study of nm23-H1 expression in classical Hodgkin’s lymphoma. Ann. Oncol. 2008;19:1941–1946
  125. Roymans D, Willems R, Van Blockstaele DR, Slegers H. Nucleoside diphosphate kinase (NDPK/NM23) and the waltz with multiple partners: possible consequences in tumor metastasis. Clin. Exp. Metast. 2002;19:465–476
  126. Sauer T, Furu I, Beraki K, Jebsen PW, Ormerod E, Naess O. nm23 protein expression in fine-needle aspirates from breast carcinoma: inverse correlation with cytologic grading, lymph node status, and ploidy. Cancer. 1998;84:109–114
  127. Russell RL, Geisinger KR, Mehta RR, White WL, Shelton B, Kute TE. nm23-relationship to the metastatic potential of breast carcinoma cell lines, primary human xenografts, and lymph node negative breast carcinoma patients. Cancer. 1997;79:1158–1165
  128. Sawan A, Lascu I, Veron M, Anderson JJ, Wright C, Horne CHW, et al. NDP-K/nm23 expression in human breast cancer in relation to relapse, survival, and other prognostic factors: an immunohistochemical study. J. Pathol. 1994;172:27–34
  129. Lazarowski ER, Boucher RC, Harden TK. Constitutive release of ATP and evidence for major contribution of ecto-nucleotide pyrophosphatase and nucleoside diphosphokinase to extracellular nucleotide concentrations. J. Biol. Chem. 2000;275:31061–31068
  130. Lazarowski ER, Homolya L, Boucher RC, Harden TK. Identification of an ecto-nucleoside diphosphokinase and its contribution to interconversion of P2 receptor agonists. J. Biol. Chem. 1997;272:20402–20407
  131. Hamby CV, Abbi R, Prasad N, Stauffer C, Thomson J, Mendola CE, et al. Expression of a catalytically inactive H118Y mutant of nm23-H2 suppresses the metastatic potential of line IV Cl 1 human melanoma cells. Int. J. Cancer. 2000;88:547–553
  132. Huwer H, Kalweit G, Engel M, Welter C, Dooley S, Gams E. Expression of the candidate tumor suppressor gene nm23 in the bronchial system of patients with squamous cell lung cancer. Eur. J. Cardiothorac. Surg. 1997;11:206–209
  133. Niitsu N, Okabe-Kado J, Okamoto M, Takagi T, Yoshida T, Aoki S, et al. Serum nm23-H1 protein as a prognostic factor in aggressive non-Hodgkin lymphoma. Blood. 2001;97:1202–1210
  134. Okabe-Kado J, Kasukabe T, Honma Y. Differentiation inhibitory factor Nm23 as a prognostic factor for acute myeloid leukemia. Leuk. Lymphoma. 1998;32:19–28
  135. Okabe-Kado J, Kasukabe T, Honma Y. Expression of cell surface NM23 proteins of human leukemia cell lines of various cellular lineage and differentiation stages. Leuk. Res. 2002;26:569–576
  136. Jackson SW, Hoshi T, Wu Y, Sun X, Enjyoji K, Cszimadia E, et al. Disordered purinergic signaling inhibits pathological angiogenesis in cd39/Entpd1-null mice. Am. J. Pathol. 2007;171:1395–1404
  137. Goepfert C, Sundberg C, Sevigny J, Enjyoji K, Hoshi T, Csizmadia E, et al. Disordered cellular migration and angiogenesis in cd39-null mice. Circulation. 2001;104:3109–3115
  138. Kaiser RA, Buxton IL. Nucleotide-mediated relaxation in guinea-pig aorta: selective inhibition by MRS2179. Br. J. Pharamcol. 2002;135:537–545
  139. Kaiser RA, Oxhorn BC, Andrews G, Buxton IL. Functional compartmentation of endothelial P2Y receptor signaling. Circ. Res. 2002;91:292–299
  140. Kashiwagi S, Izumi Y, Gohongi T, Demou ZN, Xu L, Huang PL, et al. NO mediates mural cell recruitment and vessel morphogenesis in murine melanomas and tissue-engineered blood vessels. J. Clin. Invest. 2005;115:1816–1827
  141. Fishman P, Bar-Yehuda S, Synowitz M, Powell JD, Klotz KN, Gessi S, et al. Adenosine receptors and cancer. Handb. Exp. Pharmacol. 2009;399–441
  142. Deli T, Csernoch L. Extracellular ATP and cancer: an overview with special reference to P2 purinergic receptors. Pathol. Oncol. Res. 2008;14:219–231
  143. Shabbir M, Burnstock G. Purinergic receptor-mediated effects of adenosine 5′-triphosphate in urological malignant diseases. Int. J. Urol. 2009;16:143–150
  144. Kaczmarek E, Erb L, Koziak K, Jarzyna R, Wink MR, Guckelberger O, et al. Modulation of endothelial cell migration by extracellular nucleotides: involvement of focal adhesion kinase and phosphatidylinositol 3-kinase-mediated pathways. Thromb. Haemostasis. 2005;93:735–742
  145. Satterwhite CM, Farrelly AM, Bradley ME. Chemotactic, mitogenic, and angiogenic actions of UTP on vascular endothelial cells. Am. J. Physiol. 1999;276:H1091–H1097
  146. Tanaka N, Kawasaki K, Kubota Y, Nakamura K, Hashimoto M, Kunitomo M, et al. P2Y-receptor regulates size of endothelial cells in an intracellular Ca2+ dependent manner. Life Sci. 2003;72:1445–1453
  147. Tanaka N, Kawasaki K, Nejime N, Kubota Y, Nakamura K, Kunitomo M, et al. P2Y receptor-mediated Ca(2+) signaling increases human vascular endothelial cell permeability. J. Pharmacol. Sci. 2004;95:174–180
  148. Seye CI, Yu N, Gonzalez FA, Erb L, Weisman GA. The P2Y2 nucleotide receptor mediates vascular cell adhesion molecule-1 expression through interaction with VEGF receptor-2 (KDR/Flk-1). J. Biol. Chem. 2004;279:35679–35686
  149. Buvinic S, Bravo-Zehnder M, Boyer JL, Huidobro-Toro JP, Gonzalez A. Nucleotide P2Y1 receptor regulates EGF receptor mitogenic signaling and expression in epithelial cells. J. Cell Sci. 2007;120:4289–4301
  150. Shibuya M. Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J. Biochem. Mol. Biol. 2006;39:469–478
  151. Dvorak HF, Nagy JA, Feng D, Brown LF, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr. Top. Microbiol. Immunol. 1999;237:97–132
  152. Moses MA. The regulation of neovascularization of matrix metalloproteinases and their inhibitors. Stem Cells. 1997;15:180–189
  153. Hirschi KK, D’Amore PA. Pericytes in the microvasculature. Cardiovasc. Res. 1996;32:687–698
  154. Grant DS, Kleinman HK. Regulation of capillary formation by laminin and other components of the extracellular matrix. EXS. 1997;79:317–333
  155. Gerwins P, Skoldenberg E, Claesson-Welsh L. Function of fibroblast growth factors and vascular endothelial growth factors and their receptors in angiogenesis. Crit. Rev. Oncol. Hematol. 2000;34:185–194
  156. Matsumoto T, Claesson-Welsh L. VEGF receptor signal transduction. Sci. STKE 2001. 2001;RE21
  157. Folberg R, Hendrix MJ, Maniotis AJ. Vasculogenic mimicry and tumor angiogenesis. Am. J. Pathol. 2000;156:361–381
  158. Shirakawa K, Wakasugi H, Heike Y, Watanabe I, Yamada S, Saito K, et al. Vasculogenic mimicry and pseudo-comedo formation in breast cancer. Int. J. Cancer. 2002;99:821–828
  159. Shirakawa K, Shibuya M, Heike Y, Takashima S, Watanabe I, Konishi F, et al. Tumor-infiltrating endothelial cells and endothelial precursor cells in inflammatory breast cancer. Int. J. Cancer. 2002;99:344–351
  160. Yue WY, Chen ZP. Does vasculogenic mimicry exist in astrocytoma?. J. Histochem. Cytochem. 2005;53:997–1002
  161. Boocock CA, Charnock-Jones DS, Sharkey AM, McLaren J, Barker PJ, Wright KA, et al. Expression of vascular endothelial growth factor and its receptors flt and KDR in ovarian carcinoma. J. Nat. Cancer Inst. 1995;87:506–516
  162. Wang L, Karlsson L, Moses S, Hultgardh-Nilsson A, Andersson M, Borna C, et al. P2 receptor expression profiles in human vascular smooth muscle and endothelial cells. J. Cardiovasc. Pharm. 2002;40:841–853
  163. Cho CH, Lee CS, Chang M, Jang IH, Kim SJ, Hwang I, et al. Localization of VEGFR-2 and PLD2 in endothelial caveolae is involved in VEGF-induced phosphorylation of MEK and ERK. Am. J. Physiol. Heart Circ. Physiol. 2004;286:H1881–H1888
  164. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, Beliveau R. Regulation of vascular endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol. Mol. Biol. Cell. 2003;14:334–347
  165. Ikeda S, Ushio-Fukai M, Zuo L, Tojo T, Dikalov S, Patrushev NA, et al. Novel role of ARF6 in vascular endothelial growth factor-induced signaling and angiogenesis. Circ. Res. 2005;96:467–475
  166. Massimino ML, Griffoni C, Spisni E, Toni M, Tomasi V. Involvement of caveolae and caveolae-like domains in signalling, cell survival and angiogenesis. Cell Signal. 2002;14:93–98
  167. Soslau G, McKenzie RJ, Brodsky I, Devlin TM. Extracellular ATP inhibits agonist-induced mobilization of internal calcium in human platelets. Biochem. Biophys. Acta. 1995;1268:73–80
  168. Cristalli G, Vittori S, Thompson RD, Padgett WL, Shi D, Daly JW, et al. Inhibition of platelet aggregation by adenosine receptor agonists. N.-S. Arch. Pharmacol. 1994;349:644–650
  169. Berne RM. Cardiac nucleotides in hypoxia: possible role in regulation of coronary blood flow. Am. J. Physiol. 1963;204(2):317–322
  170. Lee S, Chen TT, Barber CL, Jordan MC, Murdock J, Desai S, et al. Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007;130:691–703

PII: S0304-3835(09)00620-X

doi: 10.1016/j.canlet.2009.09.021

Cancer Letters
Volume 291, Issue 2 , Pages 131-141 , 28 May 2010