Identification of human renal cell carcinoma associated genes by suppression subtractive hybridization

Abstract

Renal cell carcinoma (RCC) are frequently chemo- and radiation resistant. Thus, there is a need for identifying biological features of these cells that could serve as alternative therapeutic targets. We performed suppression subtractive hybridization (SSH) on patient-matched normal renal and RCC tissue to identify variably regulated genes. 11 genes were strongly up-regulated or selectively expressed in more than one RCC tissue or cell line. Screening of filters containing cancer-related cDNAs confirmed overexpression of 3 of these genes and 3 additional genes were identified. These 14 differentially expressed genes, only 6 of which have previously been associated with RCC, are related to tumour growth/survival (EGFR, cyclin D1, insulin-like growth factor-binding protein-1 and a MLRQ sub-unit homologue of the NADH:ubiquinone oxidoreductase complex), angiogenesis (vascular endothelial growth factor, endothelial PAS domain protein-1, ceruloplasmin, angiopoietin-related protein 2) and cell adhesion/motility (protocadherin 2, cadherin 6, autotaxin, vimentin, lysyl oxidase and semaphorin G). Since some of these genes were overexpressed in 80-90% of RCC tissues, it is important to evaluate their suitability as therapeutic targets.

References 81

1. 1.

   Bartkova J., Lukas J., Strauss M., Bartek J. The PRAD-1/cyclin D1 oncogene product accumulates aberrantly in a subset of colorectal carcinomas. Int J Cancer. 1994;58(4):568-573.

   Not in our library10.1002/ijc.2910580420

2. 2.

   Bennett B. D., Babu-Khan S., Loeloff R., Louis J. C., Curran E., Citron M., Vassar R. Expression analysis of BACE2 in brain and peripheral tissues. J Biol Chem. 2000;275(27):20647-20651.

   Not in our library10.1074/jbc.m002688200

3. 3.

   Brambilla E., Constantin B., Drabkin H., Roche J. Semaphorin SEMA3F localization in malignant human lung and cell lines: A suggested role in cell adhesion and cell migration. Am J Pathol. 2000;156(3):939-950.

   Not in our library10.1016/s0002-9440(10)64962-0

4. 4.

   Bremers A. J., Parmiani G. Immunology and immunotherapy of human cancer: present concepts and clinical developments. Crit Rev Oncol Hematol. 2000;34(1):1-25.

   Not in our library10.1016/s1040-8428(99)00059-1

5. 5.

   Brown J. M. The hypoxic cell: a target for selective cancer therapy--eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res. 1999;59(23):5863-5870.

   Not in our library

6. 6.

   Bukowski R. M. Cytokine combinations: therapeutic use in patients with advanced renal cell carcinoma. Semin Oncol. 2000;27(2):204-212.

   Not in our library

7. 7.

   Christensen C. R., Klingelhöfer J., Tarabykina S., Hulgaard E. F., Kramerov D., Lukanidin E. Transcription of a novel mouse semaphorin gene, M-semaH, correlates with the metastatic ability of mouse tumor cell lines. Cancer Res. 1998;58(6):1238-1244.

   Not in our library

8. 8.

   Conover C. A., Powell D. R. Insulin-like growth factor (IGF)-binding protein-3 blocks IGF-I-induced receptor down-regulation and cell desensitization in cultured bovine fibroblasts. Endocrinology. 1991;129(2):710-716.

   Not in our library10.1210/endo-129-2-710

9. 9.

   Conrad P. W., Freeman T. L., Beitner-Johnson D., Millhorn D. E. EPAS1 trans-activation during hypoxia requires p42/p44 MAPK. J Biol Chem. 1999;274(47):33709-33713.

   Not in our library10.1074/jbc.274.47.33709

10. 10.

    De Plaen E., Lurquin C., Van Pel A., Mariamé B., Szikora J. P., Wölfel T., Sibille C., Chomez P., Boon T. Immunogenic (tum-) variants of mouse tumor P815: cloning of the gene of tum- antigen P91A and identification of the tum- mutation. Proc Natl Acad Sci U S A. 1988;85(7):2274-2278.

    Not in our library10.1073/pnas.85.7.2274

11. 11.

    Freeman M. R., Washecka R., Chung L. W. Aberrant expression of epidermal growth factor receptor and HER-2 (erbB-2) messenger RNAs in human renal cancers. Cancer Res. 1989;49(22):6221-6225.

    Not in our library

12. 12.

    Gerwins P., Sköldenberg 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(3):185-194.

    Not in our library10.1016/s1040-8428(00)00062-7

13. 13.

    Harris S. R., Thorgeirsson U. P. Tumor angiogenesis: biology and therapeutic prospects. In Vivo. 1998;12(6):563-570.

    Not in our library

14. 14.

    Hedberg Y., Davoodi E., Roos G., Ljungberg B., Landberg G. Cyclin-D1 expression in human renal-cell carcinoma. Int J Cancer. 1999;84(3):268-272.

    Not in our library10.1002/(sici)1097-0215(19990621)84:3<268::aid-ijc12>3.0.co;2-8

15. 15.

    Hendrix M. J., Seftor E. A., Chu Y. W., Trevor K. T., Seftor R. E. Role of intermediate filaments in migration, invasion and metastasis. Cancer Metastasis Rev. 1996;15(4):507-525.

    Not in our library10.1007/bf00054016

16. 16.

    Hoffman D. M., Gitlitz B. J., Belldegrun A., Figlin R. A. Adoptive cellular therapy. Semin Oncol. 2000;27(2):221-233.

    Not in our library

17. 17.

    Hofmockel G., Tack W., Frohmüller H. G. Cyclic interferon alpha treatment in metastatic renal cell carcinoma: results of a phase II study and review of the literature. Urol Int. 1997;58(1):8-12.

    Not in our library10.1159/000282937

18. 18.

    Huang Y. W., Baluna R., Vitetta E. S. Adhesion molecules as targets for cancer therapy. Histol Histopathol. 1997;12(2):467-477.

    Not in our library

19. 19.

    Ishikawa J., Maeda S., Umezu K., Sugiyama T., Kamidono S. Amplification and overexpression of the epidermal growth factor receptor gene in human renal-cell carcinoma. Int J Cancer. 1990;45(6):1018-1021.

    Not in our library10.1002/ijc.2910450606

20. 20.

    Jares P., Fernández P. L., Campo E., Nadal A., Bosch F., Aiza G., Nayach I., Traserra J., Cardesa A. PRAD-1/cyclin D1 gene amplification correlates with messenger RNA overexpression and tumor progression in human laryngeal carcinomas. Cancer Res. 1994;54(17):4813-4817.

    Not in our library

21. 21.

    Kaplan C. D., Morris J. R., Wu C., Winston F. Spt5 and spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes Dev. 2000;14(20):2623-2634.

    Not in our library10.1101/gad.831900

22. 22.

    Kawagoe H., Stracke M. L., Nakamura H., Sano K. Expression and transcriptional regulation of the PD-Ialpha/autotaxin gene in neuroblastoma. Cancer Res. 1997;57(12):2516-2521.

    Not in our library

23. 23.

    Kerbel R. S. Tumor angiogenesis: past, present and the near future. Carcinogenesis. 2000;21(3):505-515.

    Not in our library10.1093/carcin/21.3.505

24. 24.

    Kim I., Moon S. O., Koh K. N., Kim H., Uhm C. S., Kwak H. J., Kim N. G., Koh G. Y. Molecular cloning, expression, and characterization of angiopoietin-related protein. angiopoietin-related protein induces endothelial cell sprouting. J Biol Chem. 1999;274(37):26523-26528.

    Not in our library10.1074/jbc.274.37.26523

25. 25.

    Kirschmann D. A., Seftor E. A., Nieva D. R., Mariano E. A., Hendrix M. J. Differentially expressed genes associated with the metastatic phenotype in breast cancer. Breast Cancer Res Treat. 1999;55(2):127-136.

    Not in our library10.1023/a:1006188129423

26. 26.

    Kuang W. W., Thompson D. A., Hoch R. V., Weigel R. J. Differential screening and suppression subtractive hybridization identified genes differentially expressed in an estrogen receptor-positive breast carcinoma cell line. Nucleic Acids Res. 1998;26(4):1116-1123.

    Not in our library10.1093/nar/26.4.1116

27. 27.

    Kunapuli S. P., Singh H., Singh P., Kumar A. Ceruloplasmin gene expression in human cancer cells. Life Sci. 1987;40(23):2225-2228.

    Not in our library10.1016/0024-3205(87)90057-9

28. 28.

    Kunkel L. M., Monaco A. P., Middlesworth W., Ochs H. D., Latt S. A. Specific cloning of DNA fragments absent from the DNA of a male patient with an X chromosome deletion. Proc Natl Acad Sci U S A. 1985;82(14):4778-4782.

    Not in our library10.1073/pnas.82.14.4778

29. 29.

    Kurzrock R., Ku S., Talpaz M. Abnormalities in the PRAD1 (CYCLIN D1/BCL-1) oncogene are frequent in cervical and vulvar squamous cell carcinoma cell lines. Cancer. 1995;75(2):584-590.

    Not in our library10.1002/1097-0142(19950115)75:2<584::aid-cncr2820750223>3.0.co;2-p

30. 30.

    Lager D. J., Slagel D. D., Palechek P. L. The expression of epidermal growth factor receptor and transforming growth factor alpha in renal cell carcinoma. Mod Pathol. 1994;7(5):544-548.

    Not in our library

31. 31.

    Lamar E. E., Palmer E. Y-encoded, species-specific DNA in mice: evidence that the Y chromosome exists in two polymorphic forms in inbred strains. Cell. 1984;37(1):171-177.

    Not in our library10.1016/0092-8674(84)90312-x

32. 32.

    Lee H. Y., Murata J., Clair T., Polymeropoulos M. H., Torres R., Manrow R. E., Liotta L. A., Stracke M. L. Cloning, chromosomal localization, and tissue expression of autotaxin from human teratocarcinoma cells. Biochem Biophys Res Commun. 1996;218(3):714-719.

    Not in our library10.1006/bbrc.1996.0127

33. 33.

    Lee Y. H., Tokunaga T., Oshika Y., Suto R., Yanagisawa K., Tomisawa M., Fukuda H., Nakano H., Abe S., Tateishi A. Cell-retained isoforms of vascular endothelial growth factor (VEGF) are correlated with poor prognosis in osteosarcoma. Eur J Cancer. 1999;35(7):1089-1093.

    Not in our library10.1016/s0959-8049(99)00073-8

34. 34.

    Li Y. M., Schacher D. H., Liu Q., Arkins S., Rebeiz N., McCusker R. H., Dantzer R., Kelley K. W. Regulation of myeloid growth and differentiation by the insulin-like growth factor I receptor. Endocrinology. 1997;138(1):362-368.

    Not in our library10.1210/endo.138.1.4847

35. 35.

    Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992;257(5072):967-971.

    Not in our library10.1126/science.1354393

36. 36.

    Lin B. T., Brynes R. K., Gelb A. B., McCourty A., Amin M. B., Medeiros L. J. Cyclin D1 expression in renal carcinomas and oncocytomas: an immunohistochemical study. Mod Pathol. 1998;11(11):1075-1081.

    Not in our library

37. 37.

    Mark M. D., Lohrum M., Püschel A. W. Patterning neuronal connections by chemorepulsion: the semaphorins. Cell Tissue Res. 1997;290(2):299-306.

    Not in our library10.1007/s004410050934

38. 38.

    Martín-Satué M., Blanco J. Identification of semaphorin E gene expression in metastatic human lung adenocarcinoma cells by mRNA differential display. J Surg Oncol. 1999;72(1):18-23.

    Not in our library10.1002/(sici)1096-9098(199909)72:1<18::aid-jso5>3.0.co;2-p

39. 39.

    Meng J. Y., Kataoka H., Itoh H., Koono M. Amyloid beta protein precursor is involved in the growth of human colon carcinoma cell in vitro and in vivo. Int J Cancer. 2001;92(1):31-39.

    Not in our library

40. 40.

    Mickisch G. H. Chemoresistance of renal cell carcinoma: 1986-1994. World J Urol. 1994;12(4):214-223.

    Not in our library10.1007/bf00185677

41. 41.

    Moch H., Gasser T., Amin M. B., Torhorst J., Sauter G., Mihatsch M. J. Prognostic utility of the recently recommended histologic classification and revised TNM staging system of renal cell carcinoma: a Swiss experience with 588 tumors. Cancer. 2000;89(3):604-614.

    Not in our library

42. 42.

    Moch H., Schraml P., Bubendorf L., Mirlacher M., Kononen J., Gasser T., Mihatsch M. J., Kallioniemi O. P., Sauter G. High-throughput tissue microarray analysis to evaluate genes uncovered by cDNA microarray screening in renal cell carcinoma. Am J Pathol. 1999;154(4):981-986.

    Not in our library10.1016/s0002-9440(10)65349-7

43. 43.

    Motzer R. J., Russo P. Systemic therapy for renal cell carcinoma. J Urol. 2000;163(2):408-417.

    Not in our library

44. 44.

    Nieder C., Niewald M., Schnabel K. Treatment of brain metastases from hypernephroma. Urol Int. 1996;57(1):17-20.

    Not in our library10.1159/000282870

45. 45.

    Obata S., Sago H., Mori N., Rochelle J. M., Seldin M. F., Davidson M., St John T., Taketani S., Suzuki S. T. Protocadherin Pcdh2 shows properties similar to, but distinct from, those of classical cadherins. J Cell Sci. 1995;108(Pt 12):3765-3773.

    Not in our library10.1242/jcs.108.12.3765

46. 46.

    Oshika Y., Nakamura M., Tokunaga T., Ozeki Y., Fukushima Y., Hatanaka H., Abe Y., Yamazaki H., Kijima H., Tamaoki N. Expression of cell-associated isoform of vascular endothelial growth factor 189 and its prognostic relevance in non-small cell lung cancer. Int J Oncol. 1998;12(3):541-544.

    Not in our library10.3892/ijo.12.3.541

47. 47.

    Paul R., Ewing C. M., Robinson J. C., Marshall F. F., Johnson K. R., Wheelock M. J., Isaacs W. B. Cadherin-6, a cell adhesion molecule specifically expressed in the proximal renal tubule and renal cell carcinoma. Cancer Res. 1997;57(13):2741-2748.

    Not in our library

48. 48.

    Pawelec G., Rees R. C., Kiessling R., Madrigal A., Dodi A., Baxevanis C., Gambacorti-Passerini C., Masucci G., Zeuthen J. Cells and cytokines in immunotherapy and gene therapy of cancer. Crit Rev Oncog. 1999;10(1-2):83-127.

    Not in our library

49. 49.

    Pitzer C., Stassar M., Zöller M. Identification of renal-cell-carcinoma-related cDNA clones by suppression subtractive hybridization. J Cancer Res Clin Oncol. 1999;125(8-9):487-492.

    Not in our library10.1007/s004320050306

50. 50.

    Raju K. S., Alessandri G., Ziche M., Gullino P. M. Ceruloplasmin, copper ions, and angiogenesis. J Natl Cancer Inst. 1982;69(5):1183-1188.

    Not in our library

51. 51.

    Ravaud A., Debled M. Present achievements in the medical treatment of metastatic renal cell carcinoma. Crit Rev Oncol Hematol. 1999;31(1):77-87.

    Not in our library10.1016/s1040-8428(99)00005-0

52. 52.

    Reis M., Faria V. Renal carcinoma: clinical, diagnostic and prognostic aspects. Arch Esp Urol. 1994;47(7):739-743.

    Not in our library

53. 53.

    Rosen L. Antiangiogenic strategies and agents in clinical trials. Oncologist. 2000;5(Suppl 1):20-27.

    Not in our library10.1634/theoncologist.5-suppl_1-20

54. 54.

    Sahin U., Türeci O., Schmitt H., Cochlovius B., Johannes T., Schmits R., Stenner F., Luo G., Schobert I., Pfreundschuh M. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc Natl Acad Sci U S A. 1995;92(25):11810-11813.

    Not in our library10.1073/pnas.92.25.11810

55. 55.

    Sargent E. R., Gomella L. G., Belldegrun A., Linehan W. M., Kasid A. Epidermal growth factor receptor gene expression in normal human kidney and renal cell carcinoma. J Urol. 1989;142(5):1364-1368.

    Not in our library10.1016/s0022-5347(17)39100-0

56. 56.

    Shimazui T., Oosterwijk-Wakka J., Akaza H., Bringuier P. P., Ruijter E., Debruyne F. M., Schalken J. A., Oosterwijk E. Alterations in expression of cadherin-6 and E-cadherin during kidney development and in renal cell carcinoma. Eur Urol. 2000;38(3):331-338.

    Not in our library10.1159/000020302

57. 57.

    Shimoyama Y., Gotoh M., Terasaki T., Kitajima M., Hirohashi S. Isolation and sequence analysis of human cadherin-6 complementary DNA for the full coding sequence and its expression in human carcinoma cells. Cancer Res. 1995;55(10):2206-2211.

    Not in our library

58. 58.

    Somers K. D., Schechter G. L. Genetic alterations in head and neck cancer. Otolaryngol Clin North Am. 1992;25(5):1065-1071.

    Not in our library

59. 59.

    Stassar M. J., Pitzer C., Zøller M. Downregulation of TNF receptor-associated protein-2/p97 in renal cell carcinoma. Oncol Res. 1999;11(2):85-90.

    Not in our library

60. 60.

    Stracke M. L., Clair T., Liotta L. A. Autotaxin, tumor motility-stimulating exophosphodiesterase. Adv Enzyme Regul. 1997;37:135-144.

    Not in our library10.1016/s0065-2571(96)00017-9

61. 61.

    Stracke M. L., Krutzsch H. C., Unsworth E. J., Arestad A., Cioce V., Schiffmann E., Liotta L. A. Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. J Biol Chem. 1992;267(4):2524-2529.

    Not in our library

62. 62.

    Thompson E. W., Yu M., Bueno J., Jin L., Maiti S. N., Palao-Marco F. L., Pulyaeva H., Tamborlane J. W., Tirgari R., Wapnir I. Collagen induced MMP-2 activation in human breast cancer. Breast Cancer Res Treat. 1994;31(2-3):357-370.

    Not in our library10.1007/bf00666168

63. 63.

    Tian H., McKnight S. L., Russell D. W. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 1997;11(1):72-82.

    Not in our library10.1101/gad.11.1.72

64. 64.

    Tomisawa M., Tokunaga T., Oshika Y., Tsuchida T., Fukushima Y., Sato H., Kijima H., Yamazaki H., Ueyama Y., Tamaoki N. Expression pattern of vascular endothelial growth factor isoform is closely correlated with tumour stage and vascularisation in renal cell carcinoma. Eur J Cancer. 1999;35(1):133-137.

    Not in our library10.1016/s0959-8049(98)00278-0

65. 65.

    Tran J., Rak J., Sheehan C., Saibil S. D., LaCasse E., Korneluk R. G., Kerbel R. S. Marked induction of the IAP family antiapoptotic proteins survivin and XIAP by VEGF in vascular endothelial cells. Biochem Biophys Res Commun. 1999;264(3):781-788.

    Not in our library10.1006/bbrc.1999.1589

66. 66.

    Ullrich A., Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 1990;61(2):203-212.

    Not in our library10.1016/0092-8674(90)90801-k

67. 67.

    Vassar R., Bennett B. D., Babu-Khan S., Kahn S., Mendiaz E. A., Denis P., Teplow D. B., Ross S., Amarante P., Loeloff R. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science. 1999;286(5440):735-741.

    Not in our library10.1126/science.286.5440.735

68. 68.

    Vaupel P. W. The influence of tumor blood flow and microenvironmental factors on the efficacy of radiation, drugs and localized hyperthermia. Klin Padiatr. 1997;209(4):243-249.

    Not in our library10.1055/s-2008-1043957

69. 69.

    Wang R. F., Rosenberg S. A. Human tumor antigens for cancer vaccine development. Immunol Rev. 1999;170:85-100.

    Not in our library10.1111/j.1600-065x.1999.tb01331.x

70. 70.

    Weidner N. Intratumor microvessel density as a prognostic factor in cancer. Am J Pathol. 1995;147(1):9-19.

    Not in our library

71. 71.

    Weinberg R. A. The retinoblastoma protein and cell cycle control. Cell. 1995;81(3):323-330.

    Not in our library10.1016/0092-8674(95)90385-2

72. 72.

    Weiss H., Friedrich T., Hofhaus G., Preis D. The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. Eur J Biochem. 1991;197(3):563-576.

    Not in our library10.1111/j.1432-1033.1991.tb15945.x

73. 73.

    Wen Y., Shatkin A. J. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev. 1999;13(14):1774-1779.

    Not in our library10.1101/gad.13.14.1774

74. 74.

    Wiesener M. S., Turley H., Allen W. E., Willam C., Eckardt K. U., Talks K. L., Wood S. M., Gatter K. C., Harris A. L., Pugh C. W. Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood. 1998;92(7):2260-2268.

    Not in our library

75. 75.

    Williamson J. R., Chang K., Rowold E., Marvel J., Tomlinson M., Sherman W. R., Ackermann K. E., Kilo C. Sorbinil prevents diabetes-induced increases in vascular permeability but does not alter collagen cross-linking. Diabetes. 1985;34(7):703-705.

    Not in our library10.2337/diab.34.7.703

76. 76.

    Xin H., Stephans J. C., Duan X., Harrowe G., Kim E., Grieshammer U., Kingsley C., Giese K. Identification of a novel aspartic-like protease differentially expressed in human breast cancer cell lines. Biochim Biophys Acta. 2000;1501(2-3):125-137.

    Not in our library10.1016/s0925-4439(00)00014-4

77. 77.

    Yamaguchi Y., Narita T., Inukai N., Wada T., Handa H. SPT genes: key players in the regulation of transcription, chromatin structure and other cellular processes. J Biochem. 2001;129(2):185-191.

    Not in our library10.1093/oxfordjournals.jbchem.a002842

78. 78.

    Yang Y., Mou Lj, Liu N., Tsao M. S. Autotaxin expression in non-small-cell lung cancer. Am J Respir Cell Mol Biol. 1999;21(2):216-222.

    Not in our library10.1165/ajrcmb.21.2.3667

79. 79.

    Yoshida K., Tosaka A., Takeuchi S., Kobayashi N. Epidermal growth factor receptor content in human renal cell carcinomas. Cancer. 1994;73(7):1913-1918.

    Not in our library10.1002/1097-0142(19940401)73:7<1913::aid-cncr2820730723>3.0.co;2-5

80. 80.

    Yu A. E., Hewitt R. E., Connor E. W., Stetler-Stevenson W. G. Matrix metalloproteinases. Novel targets for directed cancer therapy. Drugs Aging. 1997;11(3):229-244.

    Not in our library10.2165/00002512-199711030-00006

81. 81.

    Zhang S. Y., Caamano J., Cooper F., Guo X., Klein-Szanto A. J. Immunohistochemistry of cyclin D1 in human breast cancer. Am J Clin Pathol. 1994;102(5):695-698.

    Not in our library10.1093/ajcp/102.5.695

Cited by papers we hold 1

• The Multifaceted Roles of Copper in Cancer: A Trace Metal Element with Dysregulated Metabolism, but Also a Target or a Bullet for Therapy · 2020
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.