The Functional Role of DAB2IP, a Homeostatic Factor, in Prostate Cancer

  • Eun-Jin Yun
  • Kaijie Wu
  • Yuh-Shyan Tsai
  • Daxing Xie
  • Jer-Tsong Hsieh
Chapter
Part of the Protein Reviews book series (PRON, volume 16)

Abstract

Maintenance of cellular architecture and normal physiologic functioning of the prostatic epithelium is dependent on androgen. Cell proliferation and cell differentiation in normal prostatic gland maintains a homeostasis. This homeostatic control is impaired in prostate cancer (PCa) cells. Therefore, dissecting the mechanism of homeostatic machinery will provide a better understanding of PCa and allow us to formulate effective strategies for cancer therapy.

One of the most exciting developments in oncology has been the step-by-step construction of signaling cascade that traces the path of extracellular stimuli, all the way from the external membrane to the cell nucleus. DAB2IP was first identified as a unique RAS-GTPase activating protein from the basal cell population in prostate. Loss of DAB2IP is frequently detected in PCa. DAB2IP modulates different signal cascades associated with cell proliferation, survival, and apoptosis. Restoring DAB2IP expression in PCa can inhibit cancer metastasis by preventing epithelial-­to-mesenchymal transition that is considered to be a cell de-differentiation process. In addition, DAB2IP can inhibit angiogenesis by enhancing endothelial apoptosis and/or inhibiting vascular growth factor and its receptor expression. Consistent with these findings, DAB2IP can also inhibit the onset of the stem cell phenotype of PCa cells. Taken together, DAB2IP appears to be a key factor in controlling homeostasis of prostatic epithelium.

Keywords

Vascular Endothelial Growth Factor Androgen Receptor Cancer Stem Cell Pleckstrin Homology Prostatic Epithelium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Lee C, Holland JM (1987) Anatomy, histology, and ultrastructure (correlation with function), prostate, rat. In: Jones TC, Mohr U, Hunt RD (eds) Genital system, monographs on pathology of laboratory animals. Springer, New YorkGoogle Scholar
  2. 2.
    Sinowatz F, Amselgruber W, Plendl J, Kolle S, Neumuller C, Boos G (1995) Effects of hormones on the prostate in adult and aging men and animals. Microsc Res Tech 30:282–292PubMedCrossRefGoogle Scholar
  3. 3.
    Kasper S (2008) Exploring the origins of the normal prostate and prostate cancer stem cell. Stem Cell Rev 4:193–201PubMedCrossRefGoogle Scholar
  4. 4.
    Peehl DM (2005) Primary cell cultures as models of prostate cancer development. Endocr Relat Cancer 12:19–47PubMedCrossRefGoogle Scholar
  5. 5.
    Wang ZA, Shen MM (2011) Revisiting the concept of cancer stem cells in prostate cancer. Oncogene 30:1261–1271PubMedCrossRefGoogle Scholar
  6. 6.
    Algaba F, Trias I, Arce Y (2007) Natural history of prostatic carcinoma: the pathologist’s perspective. Recent Results Cancer Res 175:9–24PubMedCrossRefGoogle Scholar
  7. 7.
    Cooperberg MR, Park S, Carroll PR (2004) Prostate cancer 2004: insights from national disease registries. Oncology (Williston Park) 18:1239–1247, discussion 1248–1250, 1256–1238Google Scholar
  8. 8.
    Lukacs RU, Lawson DA, Xin L, Zong Y, Garraway I, Goldstein AS, Memarzadeh S, Witte ON (2008) Epithelial stem cells of the prostate and their role in cancer progression. Cold Spring Harb Symp Quant Biol 73:491–502PubMedCrossRefGoogle Scholar
  9. 9.
    De Marzo AM, Meeker AK, Epstein JI, Coffey DS (1998) Prostate stem cell compartments: expression of the cell cycle inhibitor p27Kip1 in normal, hyperplastic, and neoplastic cells. Am J Pathol 153:911–919PubMedCrossRefGoogle Scholar
  10. 10.
    Nagle RB, Ahmann FR, McDaniel KM, Paquin ML, Clark VA, Celniker A (1987) Cytokeratin characterization of human prostatic carcinoma and its derived cell lines. Cancer Res 47:281–286PubMedGoogle Scholar
  11. 11.
    Anton Aparicio LM, Cassinello Espinosa J, Garcia Campelo R, Gomez Veiga F, Diaz Prado S, Aparicio Gallego G (2007) Prostate carcinoma and stem cells. Clin Transl Oncol 9:66–76PubMedCrossRefGoogle Scholar
  12. 12.
    English HF, Santen RJ, Isaacs JT (1987) Response of glandular versus basal rat ventral prostatic epithelial cells to androgen withdrawal and replacement. Prostate 11:229–242PubMedCrossRefGoogle Scholar
  13. 13.
    Maitland NJ, Collins AT (2008) Prostate cancer stem cells: a new target for therapy. J Clin Oncol 26:2862–2870PubMedCrossRefGoogle Scholar
  14. 14.
    Tseng CP, Ely BD, Li Y, Pong RC, Hsieh JT (1998) Regulation of rat DOC-2 gene during castration-induced rat ventral prostate degeneration and its growth inhibitory function in human prostatic carcinoma cells. Endocrinology 139:3542–3553PubMedCrossRefGoogle Scholar
  15. 15.
    Zhang H, Zhang R, Luo Y, D’Alessio A, Pober JS, Min W (2004) AIP1/DAB2IP, a novel member of the Ras-GAP family, transduces TRAF2-induced ASK1-JNK activation. J Biol Chem 279:44955–44965PubMedCrossRefGoogle Scholar
  16. 16.
    Carter BS, Epstein JI, Isaacs WB (1990) ras gene mutations in human prostate cancer. Cancer Res 50:6830–6832PubMedGoogle Scholar
  17. 17.
    Pergolizzi RG, Kreis W, Rottach C, Susin M, Broome JD (1993) Mutational status of codons 12 and 13 of the N- and K-ras genes in tissue and cell lines derived from primary and metastatic prostate carcinomas. Cancer Invest 11:25–32PubMedCrossRefGoogle Scholar
  18. 18.
    Hsieh JT, Karam JA, Min W (2007) Genetic and biologic evidence that implicates a gene in aggressive prostate cancer. J Natl Cancer Inst 99:1823–1824PubMedCrossRefGoogle Scholar
  19. 19.
    Min J, Zaslavsky A, Fedele G, McLaughlin SK, Reczek EE, De Raedt T, Guney I, Strochlic DE, Macconaill LE, Beroukhim R, Bronson RT, Ryeom S, Hahn WC, Loda M, Cichowski K (2010) An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factor-kappaB. Nat Med 16:286–294PubMedCrossRefGoogle Scholar
  20. 20.
    Chen H, Pong RC, Wang Z, Hsieh JT (2002) Differential regulation of the human gene DAB2IP in normal and malignant prostatic epithelia: cloning and characterization. Genomics 79:573–581PubMedCrossRefGoogle Scholar
  21. 21.
    Chen H, Toyooka S, Gazdar AF, Hsieh JT (2003) Epigenetic regulation of a novel tumor ­suppressor gene (hDAB2IP) in prostate cancer cell lines. J Biol Chem 278:3121–3130PubMedCrossRefGoogle Scholar
  22. 22.
    Dote H, Toyooka S, Tsukuda K, Yano M, Ouchida M, Doihara H, Suzuki M, Chen H, Hsieh JT, Gazdar AF, Shimizu N (2004) Aberrant promoter methylation in human DAB2 interactive protein (hDAB2IP) gene in breast cancer. Clin Cancer Res 10:2082–2089PubMedCrossRefGoogle Scholar
  23. 23.
    Dote H, Toyooka S, Tsukuda K, Yano M, Ota T, Murakami M, Naito M, Toyota M, Gazdar AF, Shimizu N (2005) Aberrant promoter methylation in human DAB2 interactive protein (hDAB2IP) gene in gastrointestinal tumour. Br J Cancer 92:1117–1125PubMedCrossRefGoogle Scholar
  24. 24.
    Yano M, Toyooka S, Tsukuda K, Dote H, Ouchida M, Hanabata T, Aoe M, Date H, Gazdar AF, Shimizu N (2005) Aberrant promoter methylation of human DAB2 interactive protein (hDAB2IP) gene in lung cancers. Int J Cancer 113:59–66PubMedCrossRefGoogle Scholar
  25. 25.
    Chen H, Tu SW, Hsieh JT (2005) Down-regulation of human DAB2IP gene expression mediated by polycomb Ezh2 complex and histone deacetylase in prostate cancer. J Biol Chem 280:22437–22444PubMedCrossRefGoogle Scholar
  26. 26.
    Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, Rubin MA, Chinnaiyan AM (2002) The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419:624–629PubMedCrossRefGoogle Scholar
  27. 27.
    von Bergh AR, Wijers PM, Groot AJ, van Zelderen-Bhola S, Falkenburg JH, Kluin PM, Schuuring E (2004) Identification of a novel RAS GTPase-activating protein (RASGAP) gene at 9q34 as an MLL fusion partner in a patient with de novo acute myeloid leukemia. Genes Chromosomes Cancer 39:324–334CrossRefGoogle Scholar
  28. 28.
    Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ER, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavletich NP (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408:381–386PubMedCrossRefGoogle Scholar
  29. 29.
    Arbini AA, Greco M, Yao JL, Bourne P, Marra E, Hsieh JT, di Sant’agnese PA, Moro L (2011) Skp2 overexpression is associated with loss of BRCA2 protein in human prostate cancer. Am J Pathol 178:2367–2376PubMedCrossRefGoogle Scholar
  30. 30.
    Yang G, Ayala G, De Marzo A, Tian W, Frolov A, Wheeler TM, Thompson TC, Harper JW (2002) Elevated Skp2 protein expression in human prostate cancer: association with loss of the cyclin-dependent kinase inhibitor p27 and PTEN and with reduced recurrence-free survival. Clin Cancer Res 8:3419–3426PubMedGoogle Scholar
  31. 31.
    Robbins CM, Tembe WA, Baker A, Sinari S, Moses TY, Beckstrom-Sternberg S, Beckstrom-­Sternberg J, Barrett M, Long J, Chinnaiyan A, Lowey J, Suh E, Pearson JV, Craig DW, Agus DB, Pienta KJ, Carpten JD (2011) Copy number and targeted mutational analysis reveals novel somatic events in metastatic prostate tumors. Genome Res 21:47–55PubMedCrossRefGoogle Scholar
  32. 32.
    Xie D, Gore C, Zhou J, Pong RC, Zhang H, Yu L, Vessella RL, Min W, Hsieh JT (2009) DAB2IP coordinates both PI3K-Akt and ASK1 pathways for cell survival and apoptosis. Proc Natl Acad Sci USA 106:19878–19883PubMedGoogle Scholar
  33. 33.
    Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W (2009) Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol 11:397–408PubMedCrossRefGoogle Scholar
  34. 34.
    Duggan D, Zheng SL, Knowlton M, Benitez D, Dimitrov L, Wiklund F, Robbins C, Isaacs SD, Cheng Y, Li G, Sun J, Chang BL, Marovich L, Wiley KE, Balter K, Stattin P, Adami HO, Gielzak M, Yan G, Sauvageot J, Liu W, Kim JW, Bleecker ER, Meyers DA, Trock BJ, Partin AW, Walsh PC, Isaacs WB, Gronberg H, Xu J, Carpten JD (2007) Two genome-wide association studies of aggressive prostate cancer implicate putative prostate tumor suppressor gene DAB2IP. J Natl Cancer Inst 99:1836–1844PubMedCrossRefGoogle Scholar
  35. 35.
    Wang Z, Tseng CP, Pong RC, Chen H, McConnell JD, Navone N, Hsieh JT (2002) The mechanism of growth-inhibitory effect of DOC-2/DAB2 in prostate cancer. Characterization of a novel GTPase-activating protein associated with N-terminal domain of DOC-2/DAB2. J Biol Chem 277:12622–12631PubMedCrossRefGoogle Scholar
  36. 36.
    Xie D, Gore C, Liu J, Pong RC, Mason R, Hao G, Long M, Kabbani W, Yu L, Zhang H, Chen H, Sun X, Boothman DA, Min W, Hsieh JT (2010) Role of DAB2IP in modulating epithelial-­to-mesenchymal transition and prostate cancer metastasis. Proc Natl Acad Sci USA 107:2485–2490PubMedCrossRefGoogle Scholar
  37. 37.
    Heinlein CA, Chang C (2004) Androgen receptor in prostate cancer. Endocr Rev 25:276–308PubMedCrossRefGoogle Scholar
  38. 38.
    Wu K, Xie D, Liu J, Tseng SF, Gore C, Ning Z, Sharifi N, Fazil LMG, Kapur P, Xiao G, Wang M, Sun X, Öz OK, Alexandrakis G, Yang CR, Hsieh C-L, Wu H-S, He D, Hsieh JT (2012) The role of DAB2IP in androgen receptor activation during prostate cancer progression Oncogene (In press)Google Scholar
  39. 39.
    Cao WH, Luttrell LM, Medvedev AV, Pierce KL, Daniel KW, Dixon TM, Lefkowitz RJ, Collins S (2000) Direct binding of activated c-Src to the beta(3)-adrenergic receptor is required for MAP kinase activation. J Biol Chem 275:38131–38134PubMedCrossRefGoogle Scholar
  40. 40.
    Kesler CT, Gioeli D, Conaway MR, Weber MJ, Paschal BM (2007) Subcellular localization modulates activation function 1 domain phosphorylation in the androgen receptor. Mol Endocrinol 21:2071–2084PubMedCrossRefGoogle Scholar
  41. 41.
    Wright CD, Chen QH, Baye NL, Huang Y, Healy CL, Kasinathan S, O’Connell TD (2008) Nuclear alpha 1-adrenergic receptors signal activated ERK localization to caveolae in adult cardiac myocytes. Circ Res 103:992–1000PubMedCrossRefGoogle Scholar
  42. 42.
    Zhou XE, Suino-Powell KM, Li J, He YZ, MacKeigan JP, Melcher K, Yong EL, Xu HE (2010) Identification of SRC3/AIB1 as a preferred coactivator for hormone-activated androgen receptor. J Biol Chem 285:9161–9171PubMedCrossRefGoogle Scholar
  43. 43.
    Mayer BJ (2001) SH3 domains: complexity in moderation. J Cell Sci 114:1253–1263PubMedGoogle Scholar
  44. 44.
    Vidal M, Gigoux V, Garbay C (2001) SH2 and SH3 domains as targets for anti-proliferative agents. Crit Rev Oncol Hematol 40:175–186PubMedCrossRefGoogle Scholar
  45. 45.
    Zhang H, Lin Y, Li J, Pober JS, Min W (2007) RIP1-mediated AIP1 phosphorylation at a 14-3-3-binding site is critical for tumor necrosis factor-induced ASK1-JNK/p38 activation. J Biol Chem 282:14788–14796PubMedCrossRefGoogle Scholar
  46. 46.
    Luo D, He Y, Zhang H, Yu L, Chen H, Xu Z, Tang S, Urano F, Min W (2008) AIP1 is critical in transducing IRE1-mediated endoplasmic reticulum stress response. J Biol Chem 283:11905–11912PubMedCrossRefGoogle Scholar
  47. 47.
    Hanks GE, Pajak TF, Porter A, Grignon D, Brereton H, Venkatesan V, Horwitz EM, Lawton C, Rosenthal SA, Sandler HM, Shipley WU (2003) Phase III trial of long-term adjuvant androgen deprivation after neoadjuvant hormonal cytoreduction and radiotherapy in locally advanced carcinoma of the prostate: the Radiation Therapy Oncology Group Protocol 92–02. J Clin Oncol 21:3972–3978PubMedCrossRefGoogle Scholar
  48. 48.
    Kong Z, Xie D, Boike T, Raghavan P, Burma S, Chen DJ, Habib AA, Chakraborty A, Hsieh JT, Saha D (2010) Downregulation of human DAB2IP gene expression in prostate cancer cells results in resistance to ionizing radiation. Cancer Res 70:2829–2839PubMedCrossRefGoogle Scholar
  49. 49.
    Bollag DM, McQueney PA, Zhu J, Hensens O, Koupal L, Liesch J, Goetz M, Lazarides E, Woods CM (1995) Epothilones, a new class of microtubule-stabilizing agents with a taxol-like mechanism of action. Cancer Res 55:2325–2333PubMedGoogle Scholar
  50. 50.
    Kong Z, Raghavan P, Xie D, Boike T, Burma S, Chen D, Chakraborty A, Hsieh JT, Saha D (2010) Epothilone B confers radiation dose enhancement in DAB2IP gene knock-down radioresistant prostate cancer cells. Int J Radiat Oncol Biol Phys 78:1210–1218PubMedCrossRefGoogle Scholar
  51. 51.
    Galsky MD, Vogelzang NJ (2010) Docetaxel-based combination therapy for castration-­resistant prostate cancer. Ann Oncol 21:2135–2144PubMedCrossRefGoogle Scholar
  52. 52.
    Seruga B, Ocana A, Tannock IF (2011) Drug resistance in metastatic castration-resistant prostate cancer. Nat Rev Clin Oncol 8:12–23PubMedCrossRefGoogle Scholar
  53. 53.
    Carson CC III (2006) Carcinoma of the prostate: overview of the most common malignancy in men. N C Med J 67:122–127PubMedGoogle Scholar
  54. 54.
    Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58:267–284PubMedCrossRefGoogle Scholar
  55. 55.
    Dick JE (2008) Stem cell concepts renew cancer research. Blood 112:4793–4807PubMedCrossRefGoogle Scholar
  56. 56.
    Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A (2007) HEDGEHOG-­GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17:165–172PubMedCrossRefGoogle Scholar
  57. 57.
    Taylor RA, Risbridger GP (2008) The path toward identifying prostatic stem cells. Differentiation 76:671–681PubMedCrossRefGoogle Scholar
  58. 58.
    Lawson DA, Xin L, Lukacs R, Xu Q, Cheng D, Witte ON (2005) Prostate stem cells and ­prostate cancer. Cold Spring Harb Symp Quant Biol 70:187–196PubMedCrossRefGoogle Scholar
  59. 59.
    Brown MD, Gilmore PE, Hart CA, Samuel JD, Ramani VA, George NJ, Clarke NW (2007) Characterization of benign and malignant prostate epithelial Hoechst 33342 side populations. Prostate 67:1384–1396PubMedCrossRefGoogle Scholar
  60. 60.
    Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, Reilly JG, Chandra D, Zhou J, Claypool K, Coghlan L, Tang DG (2006) Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25:1696–1708PubMedCrossRefGoogle Scholar
  61. 61.
    Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT (2004) CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 117:3539–3545PubMedCrossRefGoogle Scholar
  62. 62.
    Dubrovska A, Kim S, Salamone RJ, Walker JR, Maira SM, Garcia-Echeverria C, Schultz PG, Reddy VA (2009) The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc Natl Acad Sci USA 106:268–273PubMedCrossRefGoogle Scholar
  63. 63.
    Shi X, Gipp J, Bushman W (2007) Anchorage-independent culture maintains prostate stem cells. Dev Biol 312:396–406PubMedCrossRefGoogle Scholar
  64. 64.
    Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP (2007) CD133(+) and CD133(−) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 67:4010–4015PubMedCrossRefGoogle Scholar
  65. 65.
    Strobl H, Takimoto M, Majdic O, Hocker P, Knapp W (1992) Antigenic analysis of human haemopoietic progenitor cells expressing the growth factor receptor c-kit. Br J Haematol 82:287–294PubMedCrossRefGoogle Scholar
  66. 66.
    Yarden Y, Kuang WJ, Yang-Feng T, Coussens L, Munemitsu S, Dull TJ, Chen E, Schlessinger J, Francke U, Ullrich A (1987) Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J 6:3341–3351PubMedGoogle Scholar
  67. 67.
    Kasper S (2009) Identification, characterization, and biological relevance of prostate cancer stem cells from clinical specimens. Urol Oncol 27:301–303PubMedCrossRefGoogle Scholar
  68. 68.
    Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial-­mesenchymal transition generates cells with properties of stem cells. Cell 133:704–715PubMedCrossRefGoogle Scholar
  69. 69.
    Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, Kalli KR, Haluska P, Ingle JN, Hartmann LC, Manjili MH, Radisky DC, Ferrone S, Knutson KL (2009) Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 69:2887–2895PubMedCrossRefGoogle Scholar
  70. 70.
    Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur Hausen A, Brunton VG, Morton J, Sansom O, Schuler J, Stemmler MP, Herzberger C, Hopt U, Keck T, Brabletz S, Brabletz T (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11:1487–1495PubMedCrossRefGoogle Scholar
  71. 71.
    Liu AY, Nelson PS, van den Engh G, Hood L (2002) Human prostate epithelial cell-type cDNA libraries and prostate expression patterns. Prostate 50:92–103PubMedCrossRefGoogle Scholar
  72. 72.
    Mimeault M, Mehta PP, Hauke R, Batra SK (2008) Functions of normal and malignant prostatic stem/progenitor cells in tissue regeneration and cancer progression and novel targeting therapies. Endocr Rev 29:234–252PubMedCrossRefGoogle Scholar
  73. 73.
    Risau W (1997) Mechanisms of angiogenesis. Nature 386:671–674PubMedCrossRefGoogle Scholar
  74. 74.
    Folkman J (1995) Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. N Engl J Med 333:1757–1763PubMedCrossRefGoogle Scholar
  75. 75.
    Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407:249–257PubMedCrossRefGoogle Scholar
  76. 76.
    Sato Y (2003) Molecular diagnosis of tumor angiogenesis and anti-angiogenic cancer therapy. Int J Clin Oncol 8:200–206PubMedCrossRefGoogle Scholar
  77. 77.
    Brahimi-Horn C, Pouyssegur J (2005) When hypoxia signalling meets the ubiquitin-­proteasomal pathway, new targets for cancer therapy. Crit Rev Oncol Hematol 53:115–123PubMedCrossRefGoogle Scholar
  78. 78.
    Stegmann TJ (1998) FGF-1: a human growth factor in the induction of neoangiogenesis. Expert Opin Investig Drugs 7:2011–2015PubMedCrossRefGoogle Scholar
  79. 79.
    Rosen EM, Lamszus K, Laterra J, Polverini PJ, Rubin JS, Goldberg ID (1997) HGF/SF in angiogenesis. Ciba Found Symp 212:215–226, discussion 227–219PubMedGoogle Scholar
  80. 80.
    Carmeliet P (2005) VEGF as a key mediator of angiogenesis in cancer. Oncology 69(Suppl 3):4–10PubMedCrossRefGoogle Scholar
  81. 81.
    Borre M, Nerstrom B, Overgaard J (2000) Association between immunohistochemical expression of vascular endothelial growth factor (VEGF), VEGF-expressing neuroendocrine-­differentiated tumor cells, and outcome in prostate cancer patients subjected to watchful waiting. Clin Cancer Res 6:1882–1890PubMedGoogle Scholar
  82. 82.
    Zhang R, He X, Liu W, Lu M, Hsieh JT, Min W (2003) AIP1 mediates TNF-alpha-induced ASK1 activation by facilitating dissociation of ASK1 from its inhibitor 14-3-3. J Clin Invest 111:1933–1943PubMedGoogle Scholar
  83. 83.
    Zhang H, He Y, Dai S, Xu Z, Luo Y, Wan T, Luo D, Jones D, Tang S, Chen H, Sessa WC, Min W (2008) AIP1 functions as an endogenous inhibitor of VEGFR2-mediated signaling and inflammatory angiogenesis in mice. J Clin Invest 118:3904–3916PubMedCrossRefGoogle Scholar
  84. 84.
    Cebe-Suarez S, Zehnder-Fjallman A, Ballmer-Hofer K (2006) The role of VEGF receptors in angiogenesis; complex partnerships. Cell Mol Life Sci 63:601–615PubMedCrossRefGoogle Scholar
  85. 85.
    Dayanir V, Meyer RD, Lashkari K, Rahimi N (2001) Identification of tyrosine residues in vascular endothelial growth factor receptor-2/FLK-1 involved in activation of phosphatidylinositol 3-kinase and cell proliferation. J Biol Chem 276:17686–17692PubMedCrossRefGoogle Scholar
  86. 86.
    Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N (1998) Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273:30336–30343PubMedCrossRefGoogle Scholar
  87. 87.
    Huang S, DeGuzman A, Bucana CD, Fidler IJ (2000) Nuclear factor-kappaB activity correlates with growth, angiogenesis, and metastasis of human melanoma cells in nude mice. Clin Cancer Res 6:2573–2581PubMedGoogle Scholar
  88. 88.
    Loch T, Michalski B, Mazurek U, Graniczka M (2001) Vascular endothelial growth factor (VEGF) and its role in neoplastic processes. Postepy Hig Med Dosw 55:257–274PubMedGoogle Scholar
  89. 89.
    Thurston G (2003) Role of Angiopoietins and Tie receptor tyrosine kinases in angiogenesis and lymphangiogenesis. Cell Tissue Res 314:61–68PubMedCrossRefGoogle Scholar
  90. 90.
    Jones N, Master Z, Jones J, Bouchard D, Gunji Y, Sasaki H, Daly R, Alitalo K, Dumont DJ (1999) Identification of Tek/Tie2 binding partners. Binding to a multifunctional docking site mediates cell survival and migration. J Biol Chem 274:30896–30905PubMedCrossRefGoogle Scholar
  91. 91.
    Kanda S, Miyata Y, Mochizuki Y, Matsuyama T, Kanetake H (2005) Angiopoietin 1 is mitogenic for cultured endothelial cells. Cancer Res 65:6820–6827PubMedCrossRefGoogle Scholar
  92. 92.
    Kim I, Kim HG, So JN, Kim JH, Kwak HJ, Koh GY (2000) Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3'-Kinase/Akt signal transduction pathway. Circ Res 86:24–29PubMedCrossRefGoogle Scholar
  93. 93.
    Babaei S, Teichert-Kuliszewska K, Zhang Q, Jones N, Dumont DJ, Stewart DJ (2003) Angiogenic actions of angiopoietin-1 require endothelium-derived nitric oxide. Am J Pathol 162:1927–1936PubMedCrossRefGoogle Scholar
  94. 94.
    Cho CH, Kammerer RA, Lee HJ, Steinmetz MO, Ryu YS, Lee SH, Yasunaga K, Kim KT, Kim I, Choi HH, Kim W, Kim SH, Park SK, Lee GM, Koh GY (2004) COMP-Ang1: a designed angiopoietin-1 variant with nonleaky angiogenic activity. Proc Natl Acad Sci USA 101:5547–5552PubMedCrossRefGoogle Scholar
  95. 95.
    Calvisi DF, Ladu S, Conner EA, Seo D, Hsieh JT, Factor VM, Thorgeirsson SS (2011) Inactivation of Ras GTPase-activating proteins promotes unrestrained activity of wild-type Ras in human liver cancer. J Hepatol 54:311–319PubMedCrossRefGoogle Scholar
  96. 96.
    Friedl P, Alexander S (2011) Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147:992–1009PubMedCrossRefGoogle Scholar

Copyright information

© Mayo Clinic 2013

Authors and Affiliations

  • Eun-Jin Yun
    • 1
  • Kaijie Wu
    • 2
  • Yuh-Shyan Tsai
    • 3
  • Daxing Xie
    • 4
  • Jer-Tsong Hsieh
    • 1
  1. 1.Department of UrologyUT Southwestern Medical CenterDallasUSA
  2. 2.Department of UrologyFirst Affiliated Hospital of Xi’an Jiaotong UniversityXi’anPeople’s Republic of China
  3. 3.Department of UrologyNational Cheng Kung University HospitalTainanTaiwan
  4. 4.Department of Gastrointestinal Surgery, Tongji Cancer Research Institute, Tongji HospitalHuazhong University of Science and TechnologyWuhanChina

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