Multiparametric in situ mRNA hybridization analysis to predict disease recurrence in patients with colon carcinoma

American Journal of Pathology

Volumn 149, Issue 5, 1996, Pages 1541-1551

  Kitadai, Yasuhiko ^a,c   Ellis, Lee M ^a,b   Tucker, Susan L ^a   Greene, Graham F ^a,b   Bucana, Corazon D ^a   Cleary, Karen R ^a   Takahashi, Yutaka ^a   Tahara, Eiichi ^c   Fidler, Isaiah J ^a,c,d  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c HIROSHIMA UNIV SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; COLLAGENASE; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; UVOMORULIN;

ARTICLE; CANCER RECURRENCE; CANCER STAGING; CLINICAL ARTICLE; COLON CARCINOMA; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; METASTASIS; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; TECHNIQUE;

CARCINOMA; COLONIC NEOPLASMS; HUMANS; IN SITU HYBRIDIZATION; PREDICTIVE VALUE OF TESTS; RECURRENCE; RNA, MESSENGER; RNA, NEOPLASM;

EID: 0029905939     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Boring CC, Squires TS, Tong T, Montgomery S: Cancer statistics, 1994. CA-Cancer J Clin 1994, 44:7-26
2. Jessup MJ, Gallick GE: The biology of colorectal carcinoma. Curr Probl Cancer 1992, 16:265-298
3. August DA, Ottow RT, Sugarbaker PH: Clinical perspective on human colorectal cancer metastasis. Cancer Metastasis Rev 1984, 3:303-325
4. Saenz NC, Cady B, McDermott WV, Steele GD Jr: Experience with colorectal carcinoma metastatic to the liver. Surg Clin North Am 1989, 69:361-370
5. Steinberg SM, Berwick KW, Stablein DM: Importance of tumor pathology and morphology in patients with surgically resected colon cancer. Cancer 1986, 58:1340-1345
6. Fidler IJ: Critical factors in the biology of human cancer metastasis: 28th GHA Clowes Memorial Award Lecture. Cancer Res 1990, 50:6130-6138
7. Fidler IJ: Orthotopic implantation of human colon carcinomas into nude mice provides a valuable model for the biology and therapy of cancer metastasis. Cancer Metastasis Rev 1991, 10:229-243
8. Fidler IJ: Modulation of the organ microenvironment for the treatment of cancer metastasis (commentary). J Natl Cancer Inst 1995, 87:1588-1592
9. Price JE, Aukerman SL, Fidler IJ: Evidence that the process of murine melanoma metastasis is sequential and selective and contains stochastic elements. Cancer Res 1986, 46:5172-5178
10. Aukerman SL, Price JE, Fidler IJ: Different deficiencies in the prevention of tumorigenic-low-metastatic murine K-1735 melanoma cells from producing metastases. J Natl Cancer Inst 1986, 77:915-924
11. Radinsky R: Paracrine growth regulation of human colon carcinoma organ-specific metastasis. Cancer Metastasis Rev 1993, 12:345-361
12. Markowitz SD, Molkentin K, Gerbic C, Jackson J, Stellato T, Willson JKV: Growth stimulation by coexpression of transforming growth factor-α and epidermal growth factor receptor in normal and adenomatous human colon epithelium. J Clin Invest 1990, 86:356-362
13. Gross ME, Zorbas MA, Daniels YJ, Garcia R, Gallick GE, Olive M, Brattain MG, Boman BM, Yeoman LC: Cellular growth response to epidermal growth factor in colon carcinoma cells with an amplified epidermal growth factor receptor derived from a familial adenomatous polyposis patient. Cancer Res 1991, 51:1452-1459
14. Bradly SJ, Garfinkle G, Walker E, Salem R, Chen LB, Steele G: Increased expression of the epidermal growth factor receptor on human colon carcinoma cells. Arch Surg 1986, 121:1242-1247
15. Mendelsohn J: The epidermal growth factor receptor as a target for therapy with antireceptor monoclonal antibodies. Semin Cancer Biol 1990, 1:339-344
16. Radinsky R, Risin S, Fan D, Dong Z, Bielenberg D, Bucana CD, Fidler IJ: Level and function of epidermal growth factor receptor predict the metastatic potential of human colon carcinoma cells. Clin Cancer Res 1995, 1:19-31
17. Singh RK, Bucana CD, Gutman M, Fan D, Wilson MR, Fidler IJ: The influence of the organ microenvironment on the expression of basic fibroblast growth factor in human renal cell carcinoma cells. Am J Pathol 1994, 145:365-374
18. Folkman MJ: The role of angiogenesis in tumor growth. Semin Cancer Biol 1992, 3:65-71
19. Liotta LA, Stetler-Stevenson WG: Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 1985, 64:317-326
20. Singh RK, Gutman M, Bucana CD, Sanchez R, Llansa N, Fidler IJ: Interferons-α and -β downregulate the expression of basic fibroblast growth factor in human carcinomas, Proc Natl Acad Sci USA 1995, 92:4562-4566
21. Singh RK, Gutman M, Radinsky R, Bucana CD, Fidler IJ: Expression of interleukin-8 correlates with the metastatic potential of human melanoma cells in nude mice. Cancer Res 1994, 54:3242-3247
22. Gutman M, Singh RK, Xie K, Bucana CD, Fidler IJ: Regulation of interleukin-8 expression in human melanoma cells by the organ environment. Cancer Res 1995, 55:2470-2475
23. Morikawa K, Walker SM, Nakajima M, Pathak S, Jessup JM, Fidler IJ: Influence of the organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res 1988, 48:6863-6871
24. Nakajima M, Morikawa K, Fabra A, Bucana CD, Fidler IJ: Influence of the organ environment on extracellular matrix degradative activity and metastasis of human colon carcinoma cells. J Natl Cancer Inst 1990, 82: 1890-1898
25. Levy AT, Cioce V, Sobel ME, Garbisa S, Grigioni WF, Liotta LA, Stetler-Stevenson WG: Increased expression of the M, 72,000 type IV collagenase in human colonic adenocarcinoma. Cancer Res 1991, 51:439-444
26. Poulsom R, Pignatelli M, Stetler-Stevenson WG, Liotta LA, Wright PA, Jeffrey PE, Longcroft JM, Rogers L, Stamp GWH: Stromal expression of 72-kDa type IV collagenase (MMP-2) and TIMP-2 mRNAs in colorectal neoplasia. Am J Pathol 1992, 141:389-396
27. Boag AH, Young ID: Increased expression of 72-kd type IV collagenase in prostatic adenocarcinoma. Am J Pathol 1994, 144:585-591
28. Tryggvason K, Hoyhtya M, Pyke C: Type IV collagenase in invasive tumors. Breast Cancer Res Treat 1993, 24:209-218
29. Fabra A, Nakajima M, Bucana CD, Fidler IJ: Modulation of the invasive phenotype of human colon carcinoma cells by fibroblasts from orthotopic or ectopic organs of nude mice. Differentiation 1992, 52:101-110
30. Weinstein RS, Jakate SM, Dominguez JM, Lebovitz MD, Koukoulis GK, Kuszak JR, Klusens LF, Grogan TM, Saclarides TJ, Roninson IB, Coon JS: 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 1991, 51:2720-2726
31. Wagner HE, Toth CA, Steele Jr GD, Thomas P: Metastatic potential of human colon cancer cell lines: relationship to cellular differentiation and carcinoembryonic antigen production. Clin Exp Metastasis 1992, 10:25-31
32. Tibbetts LM, Doremus CM, Tzanakakis GN, Vezeridis MP: Liver metastasis with 10 human colon carcinoma cell lines in nude mice and association with carcinoembryonic antigen production. Cancer 1993, 71: 315-321
33. Dorudi S, Sheffield JP, Poulsom R, Northover JMA, Hart IR: E-cadherin expression in colorectal cancer: an immunocytochemical and in situ hybridization study. Am J Pathol 1993, 142:981-986
34. Bohm M, Totzeck B, Birchmeier W, Wieland I: Differences of E-cadherin expression levels and patterns in primary and metastatic human lung cancer. Clin Exp Metastasis 1994, 12:55-62
35. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Löchner D, Birchmeier W: E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 1991, 113:173-185
36. Shimoyama Y, Hirohashi S, Hirano S, Noguchi M, Shimasato Y, Takeichi M, Abe O: Cadherin cell adhesion molecules in human epithelial tissues and carcinomas. Cancer Res 1989, 49:2128-2133
37. Van Der Wurff AAM, Kate JT, Van Der Linden EPM, Dinjens WNM, Arends JW, Bosman FT: L-CAM expression in normal, premalignant, and malignant colon mucosa. J Pathol 1992, 168:287-291
38. Fidler IJ, Radinsky R: Genetic control of cancer metastasis (editorial). J Natl Cancer Inst 1990, 82:166-168
39. Bucana CD, Radinsky R, Dong Z, Sanchez R, Brigati DJ, Fidler IJ: 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 1993, 41:499-506
40. Radinsky R, Bucana CD, Ellis LM, Sanchez R, Cleary KR, Brigati DJ, Fidler IJ: 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 1993, 53:937-943
41. Kitadai Y, Bucana CD, Ellis LM, Anzai H, Tahara E, Fidler IJ: In situ mRNA hybridization technique for analysis of metastasis-related genes in human colon carcinoma cells. Am J Pathol 1995, 147:1238-1247
42. Ullrich A, Coussens L, Hayflick JS, Dull TJ, Gray A, Tam AW, Lee J, Yarden Y, Libermann TA, Schlessinger J, Downward J, Mayes ELV, Whittle N, Waterfield MD, Seeburg PH: Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 1984, 309:418-428
43. Rogelj S, Weinberg RA, Fanning P, Klagsbrun M: Basic fibroblast growth factor fused to a signal peptide transforms cells. Nature 1988, 331:173-175
44. Collier IE, Wilhelm SM, Eisen AZ, Marmer BL, Grant GA, Seltzer JL, Kronberger A, He C, Bauer EA, Goldberg GI: H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J Biol Chem 1988, 263:6579-6587
45. Bussemakers MJG, van Bokhoven A, Mees SGM, Kemler R, Schalken JA: Molecular cloning and characterization of the human E-cadherin cDNA. Mol Biol Rep 1993, 17:123-128
46. Galski H, Sullivan M, Willingham MC, Chin K-V, Gottesman MM, Pastan I, Merlino GT: Expression of a human multidrug resistance cDNA (mdr-1) in the bone marrow of transgenic mice: resistance to daunomycin-induced leukopenia. Mol Cell Biol 1989, 9:4357-4363
47. Pearson WR, Lipman DJ: Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 1988, 85:2444-2448
48. Caruthers MH, Beaucage SL, Efcavitch JW, Fisher EF, Goldman RA, DeHaseth PL, Mandecki W, Matteucci MD, Rosendahl MS, Stabinsky Y: Chemical synthesis and biological studies on mutated gene-control regions. Cold Spring Harbor Symp Quant Biol 1982, 47: 411-418
49. Kitadai Y, Ellis LM, Takahashi Y, Bucana CD, Anzai H, Tahara E, Fidler IJ: Multiparametric in situ mRNA hybridization analysis to detect metastasis-related genes in surgical specimens of human colon carcinomas. Clin Cancer Res 1995, 1:1095-1102
50. Reed JA, Manahan LJ, Park CS, Brigati DJ: Complete one-hour immunocytochemistry based on capillary action. Biotechniques 1992, 13:434-443
51. Park CS, Brigati DJ, Manahan LJ: Automated molecular pathology: one hour in situ DNA hybridization. J Histotechnol 1991, 14:219-229
52. Hosmer DW, Lemeshow S: Applied Logistic Regression. New York, John Wiley and Sons, 1989
53. Conover WJ: Practical Nonparametric Statistics, ed 2. New York, John Wiley and Sons, 1980
54. Anzai H, Kitadai Y, Bucana CD, Sanchez R. Omoto R, Fidler IJ: Intratumoral heterogeneity and inverse correlation between expression of E-cadherin and collagenase type IV in human gastric carcinomas. Differentiation, 1996, 60:119-127
55. Morikawa K, Walker SM, Jessup JM, Fidler IJ: In vivo selection of highly metastatic cells from surgical specimens of different human colon carcinomas implanted into nude mice. Cancer Res 1988, 48:1943-1948
56. Fidler IJ, Kripke ML: Metastasis results from preexisting variant cells within a malignant tumor. Science 1977, 197:893-895
57. Xie B, Bucana CD, Fidler IJ: Density-dependent induction of 92-kd type IV collagenase activity in cultures of A431 human epidermoid carcinoma cells. Am J Pathol 1994, 144:1058-1067
58. Takeichi M: Cadherins: a molecular family important in selective cell-cell adhesion. Annu Rev Biochem 1990, 59:237-252
59. Takeichi M: Cadherin cell adhesion receptors as a morphogenetic regulator. Science 1991, 251:1451-1455
60. Brabant G, Hoang-Yu C, Cetin Y, Dralle H, Scheumann G, Mölne J, Hansson G, Jansson S, Ericson LE, Nisson M: E-cadherin: a differentiation marker in thyroid malignancies. Cancer Res 1993, 53:4987-4993
61. Kadowaki T, Shiozaki H, Inoue M, Tamura S, Oka H, Doki Y, Iihara K, Matsui S, Iwazawa T, Nagafuchi A, Tsukita S, Mori T: E-cadherin and α-catenin expression in human esophageal cancer. Cancer Res 1994, 54: 291-296
62. Mayer B, Johnson JP, Leitl F, Jauch KW, Heiss MM, Schildberg FW, Birchmeier W, Funke I: E-cadherin expression in primary and metastatic gastric cancer: downregulation correlates with cellular dedifferentiation and glandular disintegration. Cancer Res 1993, 53:1690-1695
63. Oka H, Shiozaki H, Kobayashi H, Inoue M, Tahara H, Kobayashi T, Takatsuka Y, Matsuyoshi N, Hirano S, Tekeichi M, Mori T: Expression of E-cadherin cell adhesion molecule in human breast cancer tissues and its relationship to metastasis. Cancer Res 1993, 53: 1696-1701
64. Schipper JH, Frixen UH, Behrens J, Unger A, Jahnke K, Birchmeier W: E-cadherin expression in squamous carcinomas of the head and neck: inverse correlation with tumor dedifferentiation and lymph node metastasis. Cancer Res 1991, 51:6328-6337
65. Shimoyama Y, Hirohashi S: Expression of E- and P-cadherin in gastric carcinomas. Cancer Res 1991, 51: 2185-2192
66. Umbas R, Schalken JA, Alders TW, Carter BS, Karthas HFM, Schaafsma HE, Debruyne FMJ, Issac WB: Expression of the cellular adhesion molecule E-cadherin is reduced or absent in high-grade prostate cancer. Cancer Res 1992, 52:5104-5109
67. Vleminckx K, Vakaet L Jr, Mareel M, Fiers W, Van Roy F: Genetic manipulation of E-cadherin expression by epithelial tumor cell reveals an invasion suppressor role. Cell 1991, 66:107-119
68. Birchmeier W: E-cadherin as a tumor (invasion) suppressor gene. Bioessays 1995, 17:97-99
69. D'Errico A, Garbisa S, Liotta LA, Castronovo V, Stetler-Stevenson WG, Grigioni WF: Augmentation of type IV collagenase, laminin receptor, and Ki67 proliferation antigen associated with human colon, gastric, and breast carcinoma progression. Mod Pathol 1991, 4:239-246
70. Liotta LA: Tumor invasion and metastasis: role of the extracellular matrix: Rhoads Memorial Award Lecture. Cancer Res 1986, 46:1-7
71. Liotta LA, Stetler-Stevenson WG: Metalloproteinases and cancer invasion. Semin Cancer Biol 1990, 1: 99-106
72. Matrisian LM, Bowden GT: Stromelysin/transin and tumor progression. Semin Cancer Biol 1990, 1:107-115
73. Murphy G, Docherty AJP: The matrix metalloproteinases and their inhibitors. Am J Respir Cell Mol Biol 1992, 7:120-125
74. Stetler-Stevenson WG: Type IV collagenase in tumor invasion and metastases. Cancer Metastasis Rev 1990, 9:289-303
75. Albini A, Melchiori A, Santi L, Liotta LA. Brown PD, Stetler-Stevenson WG: Tumor cell invasion inhibited by TIMP-2. J Natl Cancer Inst 1991, 83:775-779
76. DeClerck YA, Yean T-D, Chan D, Shimada H, Langley KE: Inhibition of tumor invasion of smooth muscle cell layers by recombinant human metalloproteinase inhibitor. Cancer Res 1991, 51:2151-2157