Relative expression of type IV collagenase, E-cadherin, and vascular endothelial growth factor/vascular permeability factor in prostatectomy specimens distinguishes organ-confined from pathologically advanced prostate cancers

Clinical Cancer Research

Volumn 6, Issue 6, 2000, Pages 2295-2308

  Kuniyasu, Hiroki ^a   Troncoso, Patricia ^a   Johnston, Dennis ^a   Bucana, Corazon D ^a   Tahara, Eiichi ^b   Fidler, Isaiah J ^a   Pettaway, Curtis A ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b HIROSHIMA UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; GELATINASE B; PROSTATE SPECIFIC ANTIGEN; UVOMORULIN; VASCULOTROPIN;

ADVANCED CANCER; ANGIOGENESIS; ARTICLE; CANCER GRADING; CANCER INVASION; CLINICAL ARTICLE; COLORIMETRY; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; PRIORITY JOURNAL; PROGNOSIS; PROSTATE CANCER; PROSTATECTOMY; PROTEIN EXPRESSION; TUMOR BIOPSY;

BIOPSY; CADHERINS; COLLAGENASES; ENDOTHELIAL GROWTH FACTORS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION; LOGISTIC MODELS; LYMPHOKINES; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; OLIGONUCLEOTIDE PROBES; PROSTATIC NEOPLASMS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0034046672     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (91)

1. Landis, S. H., Murray, T., and Bolden-Wingo, P. A. Cancer statistics 1999. Cancer (Phila.), 49: 8-31, 1999.
2. Soh, S., Kattan, M. W., Berkman, S., Wheeler, T. M., and Scardino, P. T. Has there been a recent shift in the pathological features and prognosis of patients treated with radical prostatectomy? J. Urol., 157: 2212-2218, 1997.
3. Xia, Z., Jacobsen, S. J., Bergstralh, E. J., Chute, C. G., Katusic, S. K., and Leiber, M. M. Secular changes in radical prostatectomy utilization rates in Olmsted County, Minnesota, 1980 to 1995. J. Urol., 159: 904-908, 1998.
4. Smith, D. S., Humphrey, P. A., and Catalona, W. J. The early detection of prostate carcinoma with prostate-specific antigen: the Washington University experience. Cancer (Phila.), 80: 1852-1856, 1997.
5. Partin, A. W., Kattan, M. W., Subong, E. N. P., Walsh, P. C., Wojno, K. J., Oesterling, J. E., Scardino, P. T., and Pearson, J. D. The use of prostate-specific antigen, clinical stage, and Gleason score to predict pathological stage in men with localized prostate cancer: a multi-institutional update. J. Am. Med. Assoc., 277: 1445-1451, 1997.
6. Gleason, D. F., Mellinger, G. T., and The Veterans Administrative Cooperative Urologic Research Group. Histologic grading and clinical staging of prostatic carcinoma. In: M. Tannenbaum (ed.), Urologic Pathology: The Prostate, pp. 171-198. Philadelphia: Lea & Febiger, 1998.
7. Epstein, J. I., Partin, A. W., Sauageot, J., and Walsh, P. C. Prediction of progression following radical prostatectomy: a multivariate analysis of 721 men with long-term follow-up. Am. J. Surg. Pathol., 20: 286-292, 1996.
8. Wheeler, T. M., Dillioglugil, O., Kattan, M. W., Arakawa, A., Soh, S., Suyama, K., Ohori, M., and Scardino, P. T. Clinical and pathological significance of the level and extent of capsular invasion in clinical stage T1-2 prostate cancer. Hum. Pathol., 29: 856-862, 1998.
9. D'Amico, A. V., Whittington, R., Malkowicz, S. B., Fondurulia, J., Chen, M., Tomaszewski, J. E., and Wein, A. The combination of preoperative prostate-specific antigen and postoperative pathological findings to predict prostate specific antigen outcome in clinically localized prostate cancer. J. Urol., 160: 2096-2101, 1998.
10. Oesterling, J. E. Prostate-specific antigen: a critical assessment of the most useful tumor marker for adenocarcinoma of the prostate. J. Urol., 145: 907-913, 1991.
11. Babaian, R. J., Troncoso, P., Steelhammer, L. C., Loreta-Trull, J., and Ramirez, E. I. Tumor volume and prostate-specific antigen: implications for early detection and defining a window of curability. J. Urol., 154: 1808-1812, 1995.
12. Young, C. Y. F., Montgomery, B. T., Andrews, P. E., Qiu, S., Bilhartz, D. L., and Tindall, D. J. Hormonal regulation of prostate-specific antigen messenger RNA in human prostatic adenocarcinoma cell line LNCaP. Cancer Res., 51: 3748-3752, 1991.
13. Zagars, G. K., and Pollack, A. Radiation therapy for T1 and T2 prostate cancer: prostate-specific antigen and disease outcome. Urology, 45: 476-483, 1995.
14. Partin, A. W., Pound, C. R., Clemens, J. Q., Epstein, J. I., and Walsh, P. C. Serum PSA after anatomic radical prostatectomy: the Johns Hopkins experience after 10 years. Urol. Clin. North Am., 20: 713-725, 1993.
15. Kattan, M. W., Eastham, J. A., Stapleton, A. M. F., Wheeler, T. M., and Scardino, P. T. A preoperative monogram for disease recurrence following radical prostatectomy for prostate cancer. J. Natl. Cancer Inst., 90: 766-771, 1998.
16. Fidler, I. J. Critical factors in the biology of human cancer metastasis: twenty-eighth G. H. A. Clowes Memorial Award lecture. Cancer Res., 50: 6130-6138, 1990.
17. Fidler, I. J. Modulation of the organ microenvironment for the treatment of cancer metastasis (Commentary). J. Natl. Cancer Inst., 87: 1588-1592, 1995.
18. Aukerman, S. L., Price, J. E., and Fidler, I. J. Different deficiencies in the prevention of tumorigenic-low-metastatic murine K-1735 melanoma cells from producing metastasis. J. Natl. Cancer Inst., 77: 915-924, 1986.
19. Fidler, I. J, and Radinsky, R. Genetic control of cancer metastasis. J. Natl. Cancer Inst., 82: 166-168, 1990.
20. Bucana, C. D., Radinsky, R., Dong, Z., Sanchez, R., Brigati, D. J., and Fidler, I. J. A rapid colorimetric in situ mRNA hybridization technique using hyperbiotinylated oligonucleotide probes for analysis of mdr-1 in mouse colon carcinoma cells. J. Histochem. Cytochem., 41: 499-506, 1993.
21. Kitadai, Y., Bucana, C. D., Ellis, L. M., Anzai, H., Tahara, E., and Fidler, I. J. In situ hybridization technique for analysis of metastasis-related genes in human colon carcinoma cells. Am. J. Pathol., 147: 1238-1247, 1995.
22. Kitadai, Y., Ellis, L. M., Takahashi, Y., Bucana, C. D., Anzai, H., Tahara, E., and Fidler, I. J. Multiparametric in situ messenger RNA hybridization analysis to detect metastasis-related genes in surgical specimens of human colon carcinomas. Clin. Cancer Res., 1: 1095-1102, 1995.
23. Kitadai, Y., Ellis, L. M., Tucker, S. L., Greene, G. F., Bucana, C. D., Cleary, K. R., Takahashi, Y., Tahara, E., and Fidler, I. J. Multiparametric in situ mRNA hybridization analysis to predict disease recurrence in patients with colon carcinoma. Am. J. Pathol., 149: 1541-1551, 1996.
24. Anzai, H., Kitadai, Y., Bucana, C. D., Sanchez, R., Omoto, R., and Fidler, I. J. Intratumoral heterogeneity and inverse correlation between expression of E-cadherin and collagenase type IV in human gastric carcinomas. Differentiation, 60: 119-127, 1996.
25. Kuniyasu, H., Ellis, L. M., Evans, D. B., Abbruzzese, J. L., Fenoglio, C. J., Bucana, C. D., Cleary, K. R., Tahara, E., and Fidler, I. J. Relative expression of E-cadherin and type IV collagenase genes predicts disease outcome in patients with resectable pancreatic carcinoma. Clin. Cancer Res., 5: 25-33, 1999.
26. Pettaway, C. A., Pathak, S., Greene, G., Ramirez, E., Wilson, M. R., Killion, J. J., and Fidler, I. J. Selection of highly metastatic variants of different human prostatic carcinomas utilizing orthotopic implantation in nude mice. Clin. Cancer Res., 2: 1627-1636, 1996.
27. Greene, G. F., Kitadai, Y., Pettaway, C. A., von Eschenbach, A. C., and Fidler, I. J. In situ mRNA hybridization technique for analysis of metastasis-related genes in human prostate carcinoma cells. Am. J. Pathol., 150: 1571-1582, 1997.
28. Stearns, M. E., and Wang, M. Regulation of kinase expression and type IV collagenase secretion in invasive human prostate PC-3 tumor sublines. Cancer Res., 51: 5866-5875, 1991.
29. Stearns, M., and Stearns, M. E. Evidence for increased activated metalloproteinase-2 (MMP-2): expression associated with human prostate cancer progression. Oncol. Res., 8: 69-75, 1996.
30. Singh, R. K., Bucana, C. D., Gutman, M., Fan, D., Wilson, M. R., and Fidler, I. J. The influence of the organ microenvironment on the expression of basic fibroblast growth factor in human renal cell carcinoma cells. Am. J. Pathol., 145: 365-374, 1994.
31. Nakamoto, T., Chang, C., Li, A., and Chodak, G. W. Basic fibroblast growth factor in human prostate cancer cells. Cancer Res., 52: 571-577, 1992.
32. Singh, R. K., Gutman, M., Radinsky, R., Bucana, C. D., and Fidler, I. J. Expression of interleukin-8 correlates with the metastatic potential of human melanoma cells in nude mice. Cancer Res., 54: 3242-3247, 1994.
33. Weinstein, R. S., Jakate, S. M., Dominguez, J. M., Lebovitz, M. D., Koukoulis, G. K., Kuzak, J. R., Klusens, L. F., Grogan, T. M., Saclarides, T. J., Robinson, I. B., and Coon, J. S. Relationship of the expression of the multidrug resistance gene product (P-glycoprotein) in human colon carcinoma to local tumor aggressiveness and lymph node metastasis. Cancer Res., 1: 2720-2726, 1991.
34. Theyer, G., Schirmbock, M., Thalhammer, T., Sherwood, E. R., Baumgartner, G., and Hamilton, G. Role of the MDR-1 encoded multiple drug resistance phenotype in prostate cancer cell lines. J. Urol., 150: 1544-1547, 1993.
35. Radinsky, R., Risin, S., Fan, D., Dong, Z., Bielenberg, D., Bucana, C. D., and Fidler, I. J. Level and function of epidermal growth factor receptor predict the metastatic potential of human colon carcinoma cells. Clin. Cancer Res., 1: 19-31, 1995.
36. Takeichi, M. Cadherins: a molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem., 59: 237-252, 1990.
37. Mayer, B., Johnson, J. P., Leitl, F., Jauch, K. W., Heiss, M. M., Schildberg, F. W., Birchmeier, W., and Funke, I. E-cadherin expression in primary and metastatic gastric cancer: downregulation correlates with cellular dedifferentiation and glandular disintegration. Cancer Res., 53: 1690-1695, 1993.
38. Brown, L. F., Berse, B., Jackmon, R. W., Tognazzi, K., Manseau, E. J., Senger, D. R., and Dvorak, H. F. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in adenocarcinoma of the gastrointestinal tract. Cancer Res., 53: 4727-3475, 1993.
39. Takahashi, Y., Kitadai, Y., Bucana, C. D., Cleary, K., and Ellis, L. M. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res., 55: 3964-3968, 1995.
40. Alon, T., Hemo, I., Itin, A., Peter, J., Stone, J., and Keshet, E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat. Med., 1: 1024-1028, 1995.
41. Senger, D. R., Van De Water, L., Brown, L. F., Nagy, J. A., Yeo, K., Yeo, T., Berse, B., Jackman, R. W., Dvorak, A. M., and Dvorak, H. F. Vascular permeability factor (VPF/VEGF) in tumor biology. Cancer Metastasis Rev., 12: 303-324, 1993.
42. Jackson, M. W., Bentel, J. M., and Tilley, W. D. Vascular endothelial growth factor (VEGF) expression in prostate cancer and benign prostatic hyperplasia. J. Urol., 157: 2323-2328, 1997.
43. Ferrer, F. A., Miller, L. J., Andrawis, R. L, Kurtzman, S. H., Albertsen, P. C., Laudone, V. P., and Kreutzer, D. L. Human prostate cancer: in situ and in vitro expression of VEGF by human prostate cancer cells. J. Urol., 157: 2329-2333, 1997.
44. Balbay, M. D., Pettaway, C. A., Kuniyasu, H., Inoue, K., Ramirez, E., Li, E., Fidler, I. J., and Dinney, C. P. N. Highly metastatic human prostate cancer growing within the prostate of athymic mice overexpresses vascular endothelial growth factor. Clin. Cancer Res., 5: 783-789, 1999.
45. Borgstrom, P., Bourdon, M. A., Hillan, K. J., Sriramarao, P., and Ferrara, N. Neutralizing antivascular endothelial growth factor antibody completely inhibits angiogenesis and growth of human prostate carcinoma micro tumors in vivo. Prostate, 35: 1-10, 1998.
46. Schipper, J. H., Frixen, U. H., Behrens, J., Unger, A., Jahnke, K., and Birchmeier, W. E-Cadherin expression in squamous carcinomas of the head and neck: inverse correlation with tumor dedifferentiation and lymph node metastasis. Cancer Res., 51: 6328-6337, 1991.
47. Oka, H., Shiozaki, H., Kobayashi, H., Inoue, M., Tahara, H., Kobayashi, T., Takatsuka, Y., Matsuyoshi, N., Hirano, S., Takeichi, M., and Mori, T. Expression of E-cadherin cell adhesion molecule in human breast cancer tissues and its relationship to metastasis. Cancer Res., 53: 1696-1701, 1993.
48. Mattijssen, V., Peters, H. M., Schalkwijk, L., Manni, J. J., Van't Hof Grootenboer, B., de Mulder, P. H., and Ruiter, D. J. E-cadherin expression in head and neck squamous-cell carcinoma is associated with clinical outcome. Int. J. Cancer, 55: 580-585, 1993.
49. Umbas, R., Schalken, J. A., Alders, T. W., Carter, B. S., Karthas, H. F. M., Schaafsma, H. E., Debruyne, F. M. J., and Isaac, W. B. Expression of the cellular adhesion molecule E-cadherin is reduced or absent in high-grade prostate cancer. Cancer Res., 52: 5104-5109, 1992.
50. Umbas, R., Isaacs, W. B., Bringuier, P. P., Schraafsma, H. E., Karthaus, H. F. M., Oosterhof, G. O. N., Debruyne, F. M. J., and Schalken, J. A. Decreased E-cadherin expression is associated with poor prognosis in patients with prostate cancer. Cancer Res., 54: 3929-3933, 1994.
51. Richmond, P. J. M., Karayiannakis, A. J., Nagafuchi, A., Kaisary, A. V., and Pignatelli, M. Aberrant E-cadherin and α-catenin expression in prostate cancer: correlation with patient survival. Cancer Res., 57: 3189-3193, 1997.
52. D'Errico, A., Garbisa, S., Liotta, L. A., Castronovo, V., Stetler-Stevenson, W. G., and Grigioni, W. F. Augmentation of type IV collagenase, laminin receptor, and Ki67 proliferation antigen associated with human colon, gastric, and breast carcinoma progression. Mod. Pathol., 4: 239-246, 1991.
53. Wood, M., Fudge, K., Mohler, L., Frost, A. R., Garcia, F., Wang, M., and Stearns M. E. In situ hybridization studies of metalloproteinase 2 and 9 and TIMP-1 and TIMP-2 expression in human prostate cancer. Clin. Exp. Metastasis, 15: 246-258, 1996.
54. Weidner, N., Folkman, J., Pozza, F., Bevilaqua, P., Allred, E., Mili, S., and Gasparini, G. Tumor angiogenesis: a new significant and independent prognostic indicator in early stage breast carcinoma. J. Natl. Cancer Inst., 84: 1875-1887, 1992.
55. Gasparini, G., and Harris, A. L. Clinical importance of the determination of tumor angiogenesis in breast carcinoma: much more than a new prognostic tool. J. Clin. Oncol., 13: 765-782, 1995.
56. Brawer, M. K., Deering, R. E., Brown, M., Preston, S. D., and Bigler, S. A. Predictors of pathologic stage in prostatic carcinoma: the role of neovascularity. Cancer (Phila.), 73: 678-687, 1994.
57. Bostwick, D. G., Wheeler, T. M., Blute, M., Barren, D. M., MacLennan, G. T., Sebo, T. J., Scardino, P. T., Humphrey, P. A., Hudson, M. A., Fradet, Y., Miller, G. J., Crawford, E. D., Blumenstein, B. A., Mahran, H. E., and Miles, B. J. Optimized microvessel density analysis improves prediction of cancer stage from prostate needle biopsies. Urology, 48: 47-57, 1996.
58. Silberman, M. A., Partin, A. W., Velti, R. W., and Epstein, J. I. Tumor angiogenesis correlates with progression after radical prostatectomy but not with pathologic stage in Gleason sum 5 to 7 adenocarcinoma of the prostate. Cancer (Phila.), 79: 772-779, 1997.
59. Weidner, N., Carroll, P. R., Flax, J., Flumenfield, W., and Folkman, J. Tumor angiogenesis correlates with metastasis in invasive prostate carcinoma. Am. J. Pathol., 143: 401-409, 1993.
60. Graham, C. H., Rivers, J., Kerbel, R. S., Stankiewicz, K. S., and White, W. L. Extent of vascularization as a prognostic indicator in thin (<0.76 mm) malignant melanomas. Am. J. Pathol., 145: 510-514, 1994.
61. Hollingsworth, H. C., Kohn, E. C., Steinberg, S. M., Rothenberg, M. L., and Meriono, M. J. Tumor angiogenesis in advanced stage ovarian carcinoma. Am. J. Pathol., 147: 33-41, 1995.
62. Maeda, K., Chung, Y-S., Takatsuka, S., Ogawa, Y., Onoda, N., Sawada, T., Kato, Y., Nitta, A., Arimoto, Y., and Kondo, Y. Tumour angiogenesis and tumour cell proliferation as prognostic indicators in gastric carcinomas. Br. J. Cancer, 72: 319-323, 1995.
63. Fleming, I. D., Cooper, J. S., Henson, D. E., Hutter, R. V. P., Kennedy, B. J., Murphy, G. P., O'Sullivan, B., Sobin, L. H., and Yarbro, J. W. AJCC Cancer Staging Manual, Ed. 5, pp. 121-126. Philadelphia: Lippincott-Raven, 1997.
64. Bastacky, S. I., Walsh, P. C., and Epstein, J. I. Relationship between perineural invasion on needle biopsy and radical prostatectomy capsular penetration in clinical stage B adenocarcinoma of the prostate. Am. J. Surg. Pathol., 17: 336-341, 1993.
65. Collier, I. E., Wilheim, S. M., Eisen, A. Z., Marmer, B. L., Grant, G. A., Selzter, J. L., Kronberger, A., He, C., Bauer, E. A., and Goldberg, G. I. H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloproteinase capable of degrading basement membrane collagen. J. Biol. Chem., 263: 6579-6587, 1988.
66. Bussenmakers, M. J. G., van Bokhoven, A., Mees, S. G. M., Kemler, R., and Schalken, J. A. Molecular cloning and characterization of the human E-cadherin cDNA. Mol. Biol. Rep., 17: 123-128, 1993.
67. Tischer, E., Mitchell, R., Hartman, T., Silva, M., Gospodarowicz, D., Fiddes, J. C., and Abraham, J. A. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem., 266: 11947-11954, 1991.
68. Leung, D. W., Cachianes, G., Kuang, W. J., Goeddel, D. V., and Ferrara, N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science (Washington DC), 246: 1306-1309, 1989.
69. Pearson, W. R., and Lipman, D. J. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA, 85: 2444-2448, 1988.
70. Park, C-S., Manahan, L. J., and Brigati, D. J. Automated molecular pathology: one hour in situ DNA hybridization. J. Histotechnol., 14: 219-229, 1991.
71. Caruthers, M. H., Beaucage, S. L., Efcavitch, J. W., Fisher, E. F., Goldman, R. A., De Haseth, P. L., Mandechi, W., Matteucci, M. D., Rosendahl, M. S., and Stabinsky, Y. Chemical synthesis and biological studies on mutated gene-control region. Cold Spring Harbor Symp. Quant. Biol., 47: 411-418, 1982.
72. Radinsky, R., Bucana, C. D., Ellis, L. M., Sanchez, R., Cleary, K. R., Brigati, D. J., and Fidler, I. J. A rapid colorimetric in situ messenger RNA hybridization technique for analysis of epidermal growth factor receptor in paraffin-embedded surgical specimens of human colon carcinomas. Cancer Res., 53: 937-943, 1993.
73. Reed, J. A., Manahan, L. J., Park, C. S., and Brigati, D. J. Complete one-hour immunocytochemistry based on capillary action. Biotechniques, 13: 434-443, 1992.
74. Zar, J. Biostatistics Analysis, Ed. 3. Upper Saddle River, NJ: 1996.
75. 125I-5-iodo-2′-deoxyuridine. J. Natl. Cancer Inst., 45: 773-782, 1970.
76. Fidler, I. J, and Kripke, M. L. Metastasis results from preexisting variant cells within a malignant tumor. Science (Washington DC), 197: 893-895, 1997.
77. Shimoyama, Y., Hirohashi, S., Hirano, S., Noguchi, M., Shimasato, Y., Takeichi, M., and Abe, O. Cadherin cell adhesion molecules in human epithelial tissues and carcinomas. Cancer Res., 49: 2128-2133, 1989.
78. Frixen, U. H., Beherens, J., Sachs, M., Eberle, G., Voss, B., Warda, A., Loechner, D., and Birchmeier, W. E-Cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J. Cell Biol., 113: 173-185, 1991.
79. Vleminckx, K., Vakaet, L., Jr., Mareel, M., Fiers, W., and VanRoy, F. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell, 66: 107-119, 1991.
80. Liotta, L. A. Tumor invasion and metastasis-role of the extracellular matrix: Rhoads memorial award lecture. Cancer Res., 46: 1-7, 1986.
81. Van voden Outen, D., Hop, W. C. J., Kranse, R., and Schroder, F. H. Tumor control according to pathological variables in patients treated by radical prostatectomy for clinically localized carcinoma of the prostate. Br. J. Urol., 79: 203-211, 1997.
82. Ukimura, O., Troncoso, P. T., Ramirez, E. I., and Babaian, R. J. Prostate cancer staging: correlation between ultrasound determined tumor contact length and pathologically confirmed extraprostatic extension. J. Urol., 159: 1251-1269, 1998.
83. Egan, A. J. M., and Bostwick, D. G. Prediction of extraprostatic extension of prostate cancer based on needle biopsy findings: perineural invasion lacks significance on multivariate analysis. Am. J. Surg. Pathol., 21: 1496-500, 1997.
84. Djakiew, D., Pflug, B. R., Delsite, R., Onada, M., Lynch, J. H., Arand, G., and Thompson, E. W. Chemotaxis and chemokinesis of human prostate tumor cell lines in response to human prostate stromal cell secretory proteins containing a nerve growth factor-like protein. Cancer Res., 53: 1416-420, 1993.
85. Seki, H., Tanaka, J., Sato, Y., Kato, Y., Umezawa, A., and Koyama, K. Neural cell adhesion molecule (NCAM) and perineural invasion in bile duct cancer. J. Surg. Oncol., 53: 78-83, 1993.
86. Geldof, A. A., De Kleijn, M. A. T., Rao, B. R., and Newling, D. W. W. Nerve growth factor stimulates in vitro invasive capacity of DU145 human prostatic cancer cells. J. Cancer Res. Clin. Oncol., 123: 107-112, 1997.
87. Yang, G., Wheeler, T. M., Kattan, M. W., Scardino, P. T., and Thompson, T. C. Perineural invasion of prostate carcinoma cells is associated with reduced apoptotic index. Cancer (Phila.), 78: 1267-1271, 1996.
88. Villers, A., McNeal, J. E., Redwine, E. A., Freiha, F. S., and Stamey, T. A. The role of perineural space invasion in the local spread of prostatic adenocarcinoma. J. Urol., 142: 763-768, 1989.
89. Sigala, S., Isabella, F., Botticini, D., Paez-Pereda, P., Missale, C., Bonmassar, E., and Spano, P. Suppression of telomerase, reexpression of KAI1, and abrogation of tumorigenicity by nerve growth factor in prostate cancer cell lines. Clin. Cancer Res., 5: 1211-1218, 1999.
90. Claffey, K. P., Brown, L. F., del Aguila, L. F., Tognazzi, K., Yeo, K. T., Manseau, E. J., and Dvorak, H. F. Expression of vascular permeability factor/vascular endothelial growth factor by melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Res., 56: 172-181, 1996.
91. Saleh, M., Stacker, S. A., and Wilks, A. F. Inhibition of growth of C6 glioma cells in vivo by expression of antisense vascular endothelial growth factor sequence. Cancer Res., 56: 393-398, 1996.