Growth regulatory factors and carcinogenesis: The roles played by transforming growth factor β, its receptors and signaling pathways

Anticancer Research

Volumn 19, Issue 6 A, 1999, Pages 4791-4807

  Kelly, David L ^a   Rizzino, Angie ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Breast cancer; Cancer Genome Anatomy Project; Cell cycle; Colorectal cancer; Cyclin dependent kinases; Cyclin dependent kinase inhibitors; Cyclins; Glioblastoma; Insulin like growth factor receptor 2; Pancreatic cancer; Signal transduction pathways; Smad

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

CANCER DIAGNOSIS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE MUTATION; GENOME; HUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

CELL CYCLE; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 0033376724     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (214)

1. Rubin H: Overgrowth stimulating factor released from Rous sarcoma cells. Science 167: 1271-72, 1970.
2. Krycéve C, Vigier P and Barlati S: Transformation-enhancing factor(s) produced by virus transformed and established cells. Int J Cancer 17: 370-379, 1976.
3. De Larco JE and Todaro GJ: Growth factors from murine sarcoma virus-transformed cells. Proc Natl Acad Sci USA 75: 4001-4005, 1978.
4. Sporn MB and Todaro GJ: Autocrine secretion and malignant transformation of cells. New Engl J Med 303: 878-880, 1980.
5. Rizzino A: Understanding the roles of growth factors in carcinogenesis: modulation of autocrine growth control by differentiation. Int J Dev Biol 37: 61-65, 1993.
6. Bunn CL and Tarrant GM: Limited lifespan in somatic cell hybrids and cybrids. Exp Cell Res 127; 385-396, 1980.
7. Muggleton-Harris AL and DeSimone DW: Replicative potentials of various fusion products between WI-38 and SV40 transformed WI-38 cells and their components. Somatic Cell Genet 6: 689-698, 1980.
8. Pereira-Smith OM and Smith JR: Genetic analysis of indefinite division in human cells: Identification of four complementation groups. Proc Natl Acad Sci USA 85: 6042-6046, 1988.
9. Stanbridge EJ, Der CJ, Doersen CJ, Nishimi RY, Peehl DM, Weissman BE and Wilkinson JE: Human cell hybrids: analysis of transformation and tumorigenicity. Science 215: 252-259, 1982.
10. Weissman BE and Stanbridge EJ: Complementation of the tumorigenic phenotype in human cell hybrids. J Natl Cancer Inst 70: 667-672, 1983.
11. Weissman BE, Saxon PJ, Pasquale SR, Jones GR, Geiser AG and Stanbridge EJ: Introduction of a normal human chromosome 11 into a Wilms' tumor cell line controls its tumorigenic expression. Science 236: 175-180, 1987.
12. Rinker-Schaeffer CW, Hawkins AL, Ru N, Dong J, Stoica G, Griffin CA, Ichikawa T, Barrett JC and Isaacs JT: Differential suppression of mammary and prostrate cancer metastasis by human chromosomes 17 and 11. Cancer Res 54: 6249-6256, 1994.
13. Tisty TE, White A and Sanchez J: Suppression of gene amplification in human cell hybrids. Science 255: 1425-1427, 1992.
14. Kinzler KW and Vogelstein B: Lessons from hereditary colorectal cancer. Cell 87: 159-170, 1996.
15. Gryfe R, Swallow C, Bapat B, Redston M, Gallinger S and Couture J: Molecular biology of colorectal cancer. Curr Probl Cancer 21: 233-300, 1997.
16. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM and Bos JL: Genetic alterations during colorectal-tumor development. New Engl J Med 319: 525-532, 1988.
17. Shibata D, Schaeffer J, Li ZH, Capella G and Perucho M: Genetic heterogeneity of the c-K-ras locus in colorectal adenomas but not in adenocarcinomas. J Natl Cancer Inst 85: 1058-1063, 1993.
18. Jen J, Powell SM, Papadopoulos N, Smith KJ, Hamilton SR, Vogelstein B and Kinzler KW: Molecular determinants of dysplasia in colorectal lesions. Cancer Res 54: 5523-5526, 1994.
19. Hua VY, Wang WK and Duesberg PH: Dominant transformation by mutated human ras genes in vitro requires more than 100 times higher expression than is observed in cancers. Proc Natl Acad Sci USA 94: 9614-9619, 1997.
20. Rizzino A: Transforming growth factor-β: multiple effects on cell differentiation and extracellular matrices. Dev Biol 130: 411-422, 1988.
21. Roberts AB and Sporn MB: The transforming growth factor-betas. In: Peptide growth factors and their receptors-handbook of experimental pharmacology (Sporn MB and Roberts AB, eds). Heidelberg: Springer-Verlag, 1990, pp 419-472.
22. Roberts AB and Sporn MB: Physiological actions and clinical applications of transforming growth factor-beta (TGF-beta). Growth Factors 8: 1-9, 1993.
23. Kingsley DM: The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes and Development 8: 133-146, 1994.
24. Paria BC, Jones KL, Flanders KC and Dey SK: Localization and binding of transforming growth factor-β isoforms in mouse preimplantation embryos and in delayed and activated blastocysts. Dev Biol 151: 91-104, 1992.
25. Rizzino A: Early mouse embryos produce and release factors with transforming growth factor activity. In Vitro Cell Dev Biol 21: 531-536, 1985.
26. Campbell WJ, Kelly D and Rizzino A: Expression of transforming growth factor-β3 by embryonal carcinoma cells, parietal endoderm-like cells and early mouse embryos. In Vitro Cell Dev Biol 26: 1181-1185, 1990.
27. Kelly D, Campbell WJ, Tiesman J and Rizzino A: Regulation and expression of transforming growth factor type-β during early mammalian development. Cytotechnology 4: 227-242, 1990.
28. Mummery CL, Slager H, Kruijer W, Feijen A, Freund E, Koornneef I and van den Eijnden-van Raaij AJM: Expression of transforming growth factor β2 during the differentiation of murine embryonal carcinoma and embryonic stem cells. Dev Biol 137: 161-170, 1990.
29. Pelton RW, Dickinson ME, Moses HL and Hogan BLM: In situ hybridization analysis of TGF-β3 RNA expression during mouse development: Comparative studies with TGF-β1 and β2. Development 110: 609-620, 1990.
30. Pelton RW, Saxena B, Jones M, Moses HL and Gold LI: Immunohistochemical localization of TGF-β1, TGF-β2, and TGF-β3 in the mouse embryo: Expression patterns suggest multiple roles during embryonic development. J Cell Biol 115: 1091-1105, 1991.
31. Slager HG, Lawson KA, van den Eijnden-van Raaij AJM, de Laat SW and Mummery CL: Differential localization of TGF-β2 in mouse preimplantation and early postimplantation development. Dev Biol 145: 205-218, 1991.
32. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Annunziata N and Doetschman T: Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359: 693-699, 1992.
33. Kulkarni AB, Huh C-G, Becker D, Geiser A, Lyght M, Flanders KC, Roberts AB, Sporn MB, Ward JM and Karlsson S: Transforming growth factor β1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 90: 770-774, 1993.
34. Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N and Groffen J: Abnormal lung development and cleft palate in mice lacking TGF-β3 indicates defects of epithelial-mesenchymal interaction. Nature Genetics 11: 415-421, 1995.
35. Proetzel G, Pawlowski SA, Wiles MV, Yin MY, Boivin GP, Howles PN, Ding JX, Ferguson MWJ and Doetschman T: Transforming growth factor-β3 is required for secondary palate fusion. Nature Genetics 11: 409-414, 1995.
36. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL and Doetschman T: TGFβ2 knockout mice have multiple developmental defects that are nonoverlapping with other TGFβ knockout phenotypes. Development 124: 2659-2670, 1997.
37. Oshima M, Oshima H and Taketo MM: TGF-β receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Developmental Biology 179: 297-302, 1996.
38. Massague J: The transforming growth factor-β family. Annu. Rev. Cell Biol 6:597-641, 1990.
39. Wang XF, Lin HY, Ng-Eaton E, Downward J, Lodish HF and Weinberg RA: Expression cloning and characterization of the TGF-beta type III receptor. Cell 67: 797-805, 1991.
40. Lopez-Casillas F, Cheifetz S, Doody J, Andres JL, Lane WS and Massague J: Structure and expression of the membrane proteoglycan betaglycan, a component of the TGF-β receptor system. Cell 67: 785-795, 1991.
41. Lin HY, Wang XF, Ng-Eaton E, Weinberg RA and Lodish HF: Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell 68: 775-785, 1992.
42. Franzen P, ten Dijke P, Ichijo H, Yamashita H, Schulz P, Heldin CH and Miyazono K: Cloning of a TGF-β type I receptor that forms a heteromeric complex with the TGF-β type II receptor. Cell 75: 681-692, 1993.
43. Attisano L, Carcamo J, Ventura F, Weis FMB, Massague J and Wrana JL: Identification of human activin and TGF-beta type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75: 671-680, 1993.
44. Lopez-Casillas F, Wrana JL and Massague J: Betaglycan presents ligand to the TGF-β signaling receptor. Cell 73: 1435-1444, 1993.
45. Wrana JL, Attisano L, Wieser R, Ventura F and Massague J: Mechanism of activation of the TGF-β receptor. Nature 370: 341-347, 1994.
46. Wieser R, Wrana JL and Massague J: GS domain mutations that constitutively activate TβR-I, the downstream signaling component in the TGF-β receptor complex. EMBO J 14: 2199-2208, 1995.
47. Roberts AB, Anzano MA, Wakefield LM, Roche NS, Stern DF and Sporn MB: Type β transforming growth factor: A bifunctional regulator of cellular growth. Proc Natl Acad Sci USA 82: 119-123, 1985.
48. Hill DJ, Strain AJ, Elstow SF, Swenne L and Milner RDG: Bifunctional action of transforming growth factor-β on DNA synthesis in early passage human fetal fibroblasts. J Cell Physiol 128: 322-328, 1986.
49. Globus RK, Patterson-Buckendahl P and Gospodarowicz D: Regulation of bovine bone cell proliferation by fibroblast growth factor and transforming growth factor beta. Endocrinology 123: 98-105, 1988.
50. Leof EB, Proper JA, Goustin AS, Shipley GD, DiCorleto PE and Moses HL: Induction of c-sis mRNA and activity similar to platelet-derived growth factor by transforming growth factor β: A proposed model for indirect mitogenesis involving autocrine activity. Proc Natl Acad Sci USA 83: 2453-2457, 1986.
51. Massagué J, Cheifetz S, Laiho M, Ralph DA, Weis FMB and Zentella A: Transforming growth factor-β. Cancer Surveys 12: 81-103, 1992.
52. Derynck R and Feng X-H: TGF-β receptor signaling. Biochim Biophys. Acta 1333: F105-F150, 1997.
53. Ravitz MJ and Wenner CE: Cyclin-dependent kinase regulation during G1 phase and cell cycle regulation by TGF-β. Adv Cancer Res 165-207, 1997.
54. Ong G, Sikora K and Gullick WJ: Inactivation of the retino-blastoma gene does not lead to loss of TGF-beta receptors or response to TGF-beta in breast cancer cell lines. Oncogene 6: 761-763, 1991.
55. Laiho M, Weis FMB and Massague J: Growth regulation by TGF-β linked to suppression of retinoblastoma protein phosphorylation. Cell 62: 175-185, 1990.
56. Weinberg RA: The retinoblastoma protein and cell cycle control. Cell 81: 323-330, 1995.
57. Weinberg RA: E2F and cell proliferation: a world turned upside down. Cell 85: 457-459, 1996.
58. Geng Y and Weinberg RA: Transforming growth factor β effects on expression of G1 cyclins and cyclin-dependent protein kinases. Proc Natl Acad Sci USA 90: 10315-10319, 1993.
59. Ito M, Yasui W, Kyo E, Yokozaki H, Makayama H, Ito H and Tahara E: Growth inhibition of transforming growth factor β on human gastric carcinoma cells: receptor and postreceptor signaling. Cancer Res 52: 295-300, 1992.
60. Ewen ME, Sluss HK, Whitehouse LL and Livingston DM: TGF-β inhibition of Cdk4 synthesis is linked to cell cycle arrest. Cell 74: 1009-1020, 1993.
61. Polyak K, Kato JY, Solomon MJ, Sherr CJ, Massague J, Roberts JM, Koff A: p27Kip1, a cyclin-cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 8: 9-22, 1994.
62. Reynisdóttir I, Polyak K, Iavarone A and Massague J: Kip/Cip and Inkr cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β. Genes Dev 9: 1831-1845, 1995.
63. Hannon GJ and Beach D: p15INK4B is a potential effector of TGFβ-induced cell cycle arrest. Nature 371: 257-260, 1994.
64. Massague J: Receptors for the TGF-beta family. Cell 69: 1067-1070, 1992.
65. de Jonge RR, Garrigue-Antar L, Vellucci VF and Reiss M: Frequent inactivation of the transforming growth factor β type II receptor in small-cell lung carcinoma cells. Oncology Research 9: 89-98, 1997.
66. Lazzereschi D, Ranieri A, Mincione G, Taccogna S, Nardi F and Colletta G: Human malignant thyroid tumors displayed reduced levels of transforming growth factor β receptor type II messenger RNA and protein. Cancer Res 57: 2071-2076, 1997.
67. Guo Y, Jacobs SC and Kyprianou N: Down-regulation of protein and mRNA expression for the transforming growth factor-β (TGF-β1) type I and type II receptors in human prostate cancer. Int J Cancer 71: 573-579, 1997.
68. Inagaki M, Moustakas A, Lin HY, Lodish HF and Carr BJ: Growth inhibition by transforming growth factor beta (TGF-beta) type I is restored in TGF-beta-resistant hepatoma cells after expression of TGF-beta receptor type II cDNA. Proc Natl Acad Sci USA 90: 5359-5363, 1993.
69. Sun L, Wu G, Willson JKV, Zborowska E, Yang J, Rajkarunanayake I, Wang J, Gentry LE, Wang X.-F and Brattain MG: Expression of transforming growth factor β type II receptor leads to reduced malignancy in human breast cancer MCF-7 cells. J Biol Chem 269: 26449-26455, 1994.
70. Parsons R, Myeroff LL, Liu B, Willson JK, Markowitz SD, Kinzler KW and Vogelstein B: Microsatellite instability and mutations of the transforming growth factor beta type II receptor gene in colorectal cancer. Cancer Res 55: 5548-5550, 1995
71. Park K, Kim S-J, Bang Y-J, Park J-G, Kim NK, Roberts AB and Sporn MB: Genetic changes in the transforming growth factor β (TGF-β) type II receptor gene in human gastric cancer cells: Correlation with sensitivity to growth inhibition by TGF-β Proc Natl Acad Sci USA 91: 8772-8776, 1994.
72. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, Fan RS, Zborowska E, Kinzler KW, Vogelstein B, Brattain M and Wilson JKV: Inactivation of the type II TGFβ receptor in colon cancer cells with microsatellite instability. Science 268: 1336-1338, 1995.
73. Wang T, Donahoe PK and Zervos AS: Specific interaction of type I receptors of the TGF-beta family with the immunophilin FKBP-12. Science 265: 674-676, 1994.
74. Wang T, Li B-Y, Danielson PD, Shah PC, Rockwell S, Lechleider RJ, Martin J, Manganaro T and Donahoe PK: The immunophilin FKBP12 functions as a common inhibitor of the TGF-β family type I receptors. Cell 86: 435-444, 1996.
75. Kawabata M, Imamura T, Miyazono K, Engel ME and Moses HL: Interaction of the transforming growth factor-β type 1 receptor with farnesyl transferase-a. J Biol Chem 270: 29628-29631, 1995.
76. Reddy KB, Karode MC, Harmony JAK and Howe PH: Interaction of transforming growth factor β receptors with apolipoprotein J/clusterin. Biochemistry 35: 309-314, 1996.
77. Ventura F, Liu F, Doody J and Massague J: Interaction of transforming growth factor-β receptor I with farnesyl-protein transferase-α in yeast and mammalian cells. J Biol Chem 271: 13931-13934, 1996.
78. Chen R-H, Miettinen PJ, Maruoka EM, Choy L and Derynck R: A WD-domain protein that is associated with and phosphorylated by the type II TGF-β receptor. Nature 377: 548-552, 1995.
79. Chen Y-G, Liu F and Massague J: Mechanism of TGFβ receptor inhibition by FKBP12. EMBO J 16: 3866-3876, 1997.
80. Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Tempst P and Marks AR: FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 270: 29628-29631, 1992.
81. Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD and Snyder SH: Immunophilin FK506 binding protein associated with inositol 1,4,5-triphosphate receptor modulates calcium flux. Proc Natl Acad Sci USA 92: 1784-1788, 1995.
82. Schreiber SL: Immunophilin-sensitive protein phosphatase action in cell signaling pathways. Cell 70: 365-368, 1992.
83. Alevizopoulos A, Dusserre Y, Ruegg U and Mermod N: Regulation of the transforming growth factor beta-responsive transcription factor CTF-1 by calcineurin and calcium/calmodulin-dependent protein kinase IV. J Biol Chem 272: 23597-23605, 1997.
84. Dumont FJ and Su O: Mechanism of action of the immunosuppressant rapamycin. Life Sci 58: 373-395, 1996.
85. Rosenberg ME and Silkensen J: Clusterin: physiologic and pathophysiologic considerations. Int J BioChem Cell Biol 27: 633-645, 1995.
86. Koch-Brandt C and Morgans C: Clusterin: a role in cell survival in the face of apoptosis. Prog. Mol. SubCell Biol 16: 130-149, 1996.
87. Reddy KB, Jin G, Karode MC, Harmony JAK and Howe PH: Transforming growth factor β (TGFβ)-induced nuclear localization of apolipoprotein J/clusterin in epithelial cells. Biochemistry 35: 6157-6163, 1996.
88. Thomas-Salgar S and Millis AJ: Clusterin expression in differentiating smooth muscle cells. J Biol Chem 269: 17879-17885, 1994.
89. Morgan TE, Laping NJ, Rozovsky I, Oda T, Hogan TH, Finch CE and Painetti GM: Clusterin expression by astrocytes is influenced by transforming growth factor beta 1 and heterotypic cell interactions. J Neuroimmunol 58: 101-110, 1995.
90. Jin G and Howe PH: Regulation of clusterin gene expression by transforming growth factor β. J Biol Chem 272: 26620-26626, 1997.
91. Heldin C-H, Miyazono K and ten Dijke P: TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471, 1997.
92. Eppert K, Scherer SW, Ozcelik H, Pirone R, Hoodless P, Kim H, Tsui L-C,. Bapat B, Gallinger S, Andrulis IL, Thomsen GH, Wrana JL and Atlisano L: MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86: 543-552, 1996.
93. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin C-H, Miyazono K and ten Dijke P: TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16: 5353-5362, 1997.
94. Zhang Y, Feng X-H, Wu R-Y and Derynck R: Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature 383: 168-172, 1996.
95. Yamaguchi A: Regulation of differentiation pathway of skeletal mesenchymal cells in cell lines by transforming growth factor-beta superfamily. Semin. Cell Biol 6: 165-173, 1995.
96. Zhang Y, Musci T and Derynck R: The tumor suppressor Smad4/DPC4 as a central mediator of Smad function. Curr Biol 7: 270-276, 1997.
97. Chen X, Weisberg E, Fridmacher V, Watanabe M, Naco G and Whitman M: Smad4 and Fast-1 in the assembly of activin-responsive factor. Nature 389: 85-89, 1997.
98. Kim J, Johnson K, Chen HJ, Carroll S and Laughon A: Drosophila Mad hinds to DNA and directly mediates activation of vestigral by Decapentaplegic. Nature 388: 304-308, 1997.
99. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M and Miyazono K: Smad 6 inhibits signalling by the TGF-β superfamily. Nature 389: 622-626, 1997.
100. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin N-E, Heldin C-H and ten Dyke P: Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 389: 631-635, 1997.
101. ras by transforming growth factor β in epithelial cells. J Biol Chem 267: 5029-5031, 1992.
102. Yan Z, Winawer S and Friedman E: Two different signal transduction pathways can be activated by transforming growth factor β1 in epithelial cells. J Biol Chem 269: 13231-13237, 1994.
103. Hartsough MT, Frey RS, Zipfel PA, Buard A, Cook SJ, McCormick F and Mulder KM: Altered transforming growth factor β signaling in epithelial cells. J Biol Chem 271: 22368-22375, 1996.
104. mapk in proliferating cultures of epithelial cells. J Biol Chem 270: 7117-7124, 1995.
105. Zipfel PA, Ziober BL, Morris SL and Mulder KM: Up-regulation of TGFα expression by TGFβ1, EGF, and DMF in human colon carcinoma cells. Cell Growth Differ. 4: 637-645, 1993.
106. Shibuya H, Yamaguchi K, Shirakabe K, Tonegawa A, Gotoh Y, Ueno N, Irie K, Nishida E and Matsumoto K: An activator of the TAK1 MAPKKK in TGF-β signal transduction. Science 272: 1179-1182, 1996.
107. Minden A, Lin A, Smeal T, Derijard B, Cobb M, Davis R and Karin M: c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Mol. Cell Biol 14: 6683-6688, 1994.
108. Gupta S, Campbell D, Derijard B and Davis RJ: Transcription factor ATF-2 regulation by the JNK signal transduction pathway. Science 267: 389-393, 1995.
109. Whitmarsh AJ, Shore P, Sharrocks AD and Davis RJ: Integration of MAP kinase signal transduction pathways at the serum response element. Science 269: 403-407, 1995.
110. Bright JJ, Kerr LD and Sriram S: TGF-β inhibits IL-2-induced tyrosine phosphoryla,tion and activation of Jak-1 and Stat 5 in T lymphocytes. J Immunol 159: 175-183, 1997.
111. Han HS, Jun HS, Utsugi T and Yoon JW: Molecular role of TGF-beta, secreted from a new type of CD4+ suppressor T cell, NY4.2, in the prevention of autoimmune 1DDM in NOD mice. J Autoimmun 10: 299-307, 1997.
112. Ihle JN: STATs and MAPKs: obligate or opportunistic partners in signaling. BioEssays 18: 95-98, 1996.
113. Pazdrak K, Justement L and Alarm R: Mechanism of inhibition of eosinophil activation by transforming growth factor-beta: inhibition of Lyn, MAP, Jak2 kinase, and Statl nuclear factor. J Immunol 155: 4454-4458, 1995.
114. Markowitz SD and Roberts AB: Tumor suppressor activity of the TGF-β pathway in human cancers. Cytokine and Growth Factor Reviews 7: 93-102, 1996.
115. Parsons R, Myeroff LL, Liu B, Willson JK, Markowitz SD, Kinzler KW and Vogelstein B: Microsatellite instability and mutations of the transforming growth factor beta type II receptor gene in colorectal cancer. Cancer Res 55: 5548-5550, 1995.
116. Bedossa P, Peltier E, Terris B, Franco D and Poynard T: Transforming growth factor-β1 (TGF-β1) and TGF-β1 receptors in normal, cirrhotic, and neoplastic human livers. Hepatology 21: 760-766, 1995.
117. Zhang T, Nanney L, Peeler MO, Williams CS, Lamps L, Heppner KJ, DuBois RN and Beauchamp D: Decreased transforming growth factor β type II receptor expression in intestinal adenomas from Min/+ mice associated with increased cyclin D1 and cyclin-dependent kinase 4 expression. Cancer Res 57: 1638-1643, 1997.
118. Kimchi A, Wang XF, Weinberg RA, Cheifetz S and Massague J: Absence of TGF-beta receptors and growth inhibitory responses in retinoblastoma cells. Science 240: 196-199, 1988.
119. Azuma M, Yuki T, Tamatani T, Motegi K, Yoshida H and Sato M: Lack of expression of transforming growth factor-beta type II receptor associated with malignant progression in human salivary gland cell clones. Int J Cancer 66: 802-805, 1996.
120. Izumoto S, Arita N, Ohnishi T, Hiraga S, Taki T, Tomita N, Ohue M and Hayakawa T: Microsatellite instability and mutated type II transforming growth factor-beta receptor gene in gliomas. Cancer Lett 112: 251-256, 1997.
121. Eshelman J and Markowitz S: Microsatellite instability in inherited and sporadic neoplasms. Curr Opin Oncol 7: 83-89, 1995.
122. Markowitz S, Wang J, MyeroffL, Parsons R, Sun L, Lutterbaugh J, Fan RS, Zborowska E, Kinzler KW, Vogelstein B, Brattain MG and Willson JKV: Inactivation of the type II TGF-β3 receptor in colon cancer cell with microsatellite instability. Science 268: 1336-1338, 1995.
123. Chang J, Park K, Bang Y-J, Kim WS, Kim D and Kim S-J: Expression of transforming growth factor β type II receptor reduces tumorigenicity in human gastric cancer cells. Cancer Res 57: 2856-2859, 1997.
124. Wang J, Sun L, Myeroff L, Wang X, Gentry LE, Yang J, Liang J, Zborowska E, Markowitz S, Wilson JK and Brattain MG: Demonstration that mutation of the type II transforming growth factor-β receptor inactivates its tumor suppressor activity in replication error-positive colon carcinoma cells. J Biol Chem 270: 22044-22049, 1995.
125. Garrigue-Antar L, Munoz-Antonia T, Antonia SJ, Gesmonde J, Velluci VF and Reiss M: Missense mutations of the transforming growth factor-β type II receptor in human head and neck squamous carcinoma cells. Cancer Res 55: 3982-3987, 1995.
126. Kok K, Naylor SL and Buys CHCM: Deletions of the short arm of chromosome 3 in solid tumors and the search for suppressor genes. Adv. Cancer Res 71: 27-92, 1997.
127. Nørgaard P, Spang-Thomsen M and Poulsen HS: Expression and autoregulation of transforming growth factor β receptor mRNA in small-cell lung cancer cell lines. Br J Cancer 73: 1037-1043, 1996.
128. Munoz-Antonia T, Li X, Reiss M, Jackson R and Antonia S: A mutation in the transforming growth factor β type II receptor gene promoter associated with loss of gene expression. Cancer Res 56: 4831-4835, 1996.
129. Rizzino A: Appearance of high affinity receptors for type β transforming growth factor during differentiation of murine embryonal carcinoma cells. Cancer Res 47: 4386-4390, 1987.
130. Kelly D, Kim S-J and Rizzino A: Transcriptional activation of the type II transforming growth factor-β receptor gene upon differentiation of embryonal carcinoma cells. J Biol Chem 273: 21115-21124, 1998.
131. Kelly D and Rizzino A: Inhibitory effects of transforming growth factor-β on laminin production and growth exhibited by endoderm-like cells derived from embryonal carcinoma cells. Differentiation 41: 34-41, 1989.
132. Birchenall-Roberts MC, Falk LA, Kasper J, Keller J, Faltynek CR and Ruscetti FW: Differential expression of transforming growth factor-β1 (TGF-β1) receptors in murine myeloid cell lines transformed with oncogenes. Correlation with differential growth inhibition by TGF-β1. J Biol Chem 266: 9617-9621, 1991.
133. Okamoto A, Jiang W, Kim S-J, Spillare EA, Stoner GD, Weinstein IB and Harris CC: Overexpression of human cyclin D1 reduces the transforming growth factor β (TGF-β) type II receptor and growth inhibition by TGF-β1 in an immortalized human esophageal epithelial cell line. Proc Natl Acad Sci USA 91: 11576-11580, 1994.
134. Kim DH, Chang JH, Lee KH, Lee H-Y and Kim S-J: Mechanism of E1A-induced transforming growth factor-β (TGF-β) resistance in mouse keratinocytes involves repression of TGF-β type II receptor transcription. J Biol Chem 272: 688-694, 1997.
135. Kim IY, Ahn HJ, Zelner DJ, Shaw JW, Sensibar JA, Kim JH, Kato M and Lee C: Genetic change in transforming growth factor-β (TGF-β) receptor type I gene correlates with insensitivity to TGF-β1 in human prostate cancer cells. Cancer Res 56: 44-48, 1996.
136. Hattori K, Okamoto M and Oyasu R: Transforming growth factor beta type I receptor acts as a potent tumor suppressor in rat bladder carcinoma. Carcinogenesis 18: 1867-1870, 1997.
137. Keen AJ and Knowles MA: Definition of two regions of deletion on chromosome 9 in carcinoma of the bladder. Oncogene 9: 2083-2088, 1994.
138. rd CH, Gonzalez-Zulueta M, Gonzalgo ML, Chan MF, Tsai YC, Dean M, Steven K, Horn T and Jones PA: Evidence for two tumor suppressor loci associated with proximal chromosome 9p to q and distal chromosome 9q in bladder cancer and the initial screening for GAS 1 and PTC mutations. Cancer Res 56: 5039-5043, 1996.
139. Johnson DW, Qumsiyeh M, Benkhalifa M and Marchuk DA: Assignment of human transforming growth factor-β type I and type III receptor genes (TGFβR1 and TGFβR3) to 9q33- q34 and 1p32-p33, respectively. Genomics 28: 356-357, 1995.
140. Hahn SA, Schutte M, Hoque ATMS, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH and Kern SE: DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271: 350-353, 1996.
141. Thialgalingam S, Lengauer C, Leach FS, Schutte M, Hahn SA, Overhauser J, Willson JKV, Markowitz S, Hamilton SR, Kern SE, Kinzler KW and Vogelstein B: Evaluation of chromosome 18q in colorectal cancers. Nat Genet 13: 343-346, 1996.
142. Nagatake M, Takagi Y, Osada H, Uchida K, Misudomi T, Saji S, Shimokata K, Takahashi T and Takahashi T: Somatic in vivo alterations of the DPC4 gene at 18q21 in human lung cancers. Cancer Res 56: 2718-2720, 1996.
143. Schutte M, Hruban RH, Hedrick L, Cho KR, Nadasdy GM, Weinstein CL, Bova GS, Isaacs WB, Cairns P, Nawroz H, Sidransky D, Casero RA, Meltzer PS, Hahn SA and Kern SE: DPC4 gene in various tumor types. Cancer Res 56: 2527-2530, 1996.
144. Kim SK, Fan Y, Papadimitrakopoulou V, Clayman G, Hittleman WN, Hong WK, Lotan R and Mao L: DPC4, a candidate tumor suppressor gene, is altered infrequently in head and neck squamous cell carcinoma. Cancer Res 56: 2519-2521, 1996.
145. Reiss M, Santoro V, de Jonge RR and Vellucci VF: Transfer of chromosome 18 into human head and neck squamous carcinoma cells: evidence tor tumor suppression by Smad4/DPC4. Cell Growth Dffler 8: 407-415, 1997.
146. waf1 expression and growth inhibition by transforming growth factor β involve the tumor suppressor gene DPC4 in human pancreatic adenocarcinoma cells. Cancer Res 57: 3929-3934, 1997.
147. Horowitz JM, Park SH, Bogenmann E, Cheng JC, Yandell DW, Kaye FJ, Minna JD, Dryja TP and Weinberg RA: Frequent inactivation of the retinoblastoma anti-oncogene is restricted to a subset of human tumor cells. Proc Natl Acad Sci USA 87: 2775-2779, 1990.
148. Pietenpol JA, Stein RW, Moran E, Yaciuk P, Schlegel R, Lyons RM, Pittelkow MR, Munger K, Howley PM and Moses HL: TGF-β1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell 61: 777-785, 1990.
149. Weinberg RA: The molecular basis of oncogenes and tumor suppressor genes. Ann NY Acad Sci 758: 331-338, 1995.
150. Kipl by the viral E1A oncoprotein in TGF-β-treated cells. Nature 380: 262-265, 1996.
151. Lammie GA and Peters G: Chromosome 11q13 abnormalities in human cancer. Cancer Cells 3: 413-420, 1991.
152. Jiang W, Kahn SM, Tomita N, Zhang YJ, Lu SH and Weinstein IB: Amplification and expression of the human cyclin D gene in esophageal cancer. Cancer Res 52: 2980-2983, 1992.
153. Gillett C, Fantl V, Smith R, Fisher C, Bartek J, Dickson C, Barnes D and Peters G: Amplification and overexpression of cyclin D 1 in breast cancer detected by immunohistochemical staining. Cancer Res 54: 1812-1817, 1994.
154. Buckley MF, Sweeney KJ, Hamilton JA, Sini RL, Manning DL, Nicholson RI, deFazio A, Watts CK, Musgrove EA and Sutherland RL: Expression and amplification of cyclin genes in human breast cancer. Oncogene 8: 2127-2133, 1993.
155. Khatib ZA, Matsushime H, Valentine M, Shapiro DN, Sherr CJ and Look AT: Coamplification of the CDK4 gene with MDM2 and GLI in human sarcomas. Cancer Res 53: 5535-5541, 1993.
156. He J, Allen JR, Collins VP, Allalunis-Turner MJ, Godbout R, Day 3rd RS and James CD: CDK4 amplification is an alternative mechanism to p16 gene homozygous deletion in glioma cell lines. Cancer Res 54: 5804-5807, 1994.
157. Kamb A, Gruis NA, Weaver-Feldhaus J, Liu Q, Harshman K, Tavtigian SV, Stodkert E, Day 3rd RS, Johnson BE and Skolnick MH: A cell cycle regulator potentially involved in genesis of many tumor types. Science 264: 436-440, 1994.
158. Nobori T, Miura K, Wu DJ, Lois A, Takabayashi K and Carson DA: Deletions of the cyclin- dependent kinase-4 inhibitor gene in multiple human cancers. Nature 368: 753-756, 1994.
159. Orlow I, Lacombe L, Hannon GJ, Serrano M, Pellicer I, Dalbagni G, Reuter VE, Zhang ZF, Beach D and Cordon-Cardo C: Deletion of the p16 and p15 genes in human bladder tumors. J Natl Cancer Inst 87: 1524-1529, 1995.
160. Washimi O, Nagatake M, Osada H, Ueda R, Koshikawa T, Seki T, Takahashi T and Takahashi T: In vivo occurrence of p16 (MTS1) and p15 (MTS2) alterations preferentially in non- small cell lung cancers. Cancer Res 55: 514-517, 1995.
161. Siebert R, Willers CP and Opalka B: Role of the cyclin-dependent kinase 4 and 6 inhibitor gene family p15, p16, p18 and p19 in leukemia and lymphoma. Leuk Lymphoma 23: 505-520, 1996.
162. Iravani M, Dhat R and Price CM: Methylation of the multi tumor suppressor gene-2 (MTS2, CDKN1, p15INK4B) in childhood acute lymphoblastic leukemia. Oncogene 15: 2609-2614 1997.
163. Ponce-Castaneda MV, Lee MH, Latres E, Polyak K, Lacombe L, Montgomery K, Mathew S, Krauter K, Sheinfeld J and Cordon-Cardo C: p27Kip1: chromosomal mapping to 12p12-12p13.1 and absence of mutations in human tumors. Cancer Res 55: 1211-1214, 1995.
164. Chan LC, Kwong YL, Liu HW, Lee CP, Lie KW and Chan AY: Deletion 12p in de novo acute myeloid leukemia. An association with early progenitor cell. Cancer Genet Cytogenet 62: 47-49, 1992.
165. Berube NG, Speevak MD and Cheverette M: Suppression of tumorigenicity of human prostate cancer cells by introduction of human chormosome del(12)(q13). Cancer Res 54: 3077-3081, 1994.
166. Yasui W, Kudo Y, Semba S, Yoko-zaki H and Tahara E: Reduced expression of cyclin-dependent kinase inhibitor p27Kip1 is associated with advanced state and invasiveness of gastric carcinomas. Jpn. J Cancer Res 88: 625-629, 1997.
167. Erickson LA, Jin L, Wollan PC, Thompson GB, van Heerden J and Lloyd RV: Expression of p27kip1 and Ki-67 in benign and malignant thyroid tumors. Mod Pathol 11: 169-174, 1998.
168. Esposito V, Baldi A, De Luca A, Groger AM, Loda M, Giordano GG, Caputi M,
169. Yang RM, Naitoh J, Murphy M, Wang HJ, Phillipson J, deKernion JB, Loda M and Reiter RE: Low p27 expression predicts poor disease-free survival in patients with prostate cancer. J Urol 159: 941-945, 1998.
170. Katayose Y, Kim M, Rakkar AN, Li Z, Cowan KH and Seth P: Promoting apoptosis: a novel activity associated with the cyclin-dependent kinase inhibitor p27. Cancer Res 57: 5441-5445, 1997.
171. Scott DW, Donjerkovic D, Maddox B, Ezhevsky S and Grdina T: Role of c-myc and p27 in anti-IgM induced B-lymphoma apoptosis. Curr Top MicroBiol Immunol 224: 103-112, 1997.
172. Knabbe C, Lippman ME, Wakefield LM, Flanders KC, Kasid A, Derynck R and Dickson RB: Evidence that transforming growth factor-β is a hormonally regulated negative growth factor in human breast cancer cells. Cell 48: 417-428, 1987.
173. Ranchalis JE, Gentry L, Ogawa Y, Seyedin SM, McPherson J, Purchio A and Twardzik DR: Bone-derived and recombinant transforming growth factor-βs are potent inhibitors of tumor cell growth. Biohem Biophys Res Commun 148: 783-789, 1987.
174. Arteaga CL, Tandon AK, Von Hoff DD and Osborne CK: Transforming growth factor β: potential autocrine growth inhibitor of estrogen receptor-negative human breast cancer cells. Cancer Res 48: 3898-3904, 1988.
175. Arteaga CL, Coffey RJ, Dugger TC, McCutchen CM, Moses HL and Lyons RM: Growth stimulation of human breast cancer cells with anti-transforming growth factor β antibodies: evidence for negative autocrine regulation by transforming growth factor β. Cell Growth & Differ 1: 367-374, 1990.
176. Godden J, Porteous C, George WD and Kerr DJ: Bioassay of transforming growth factor-β activity in acidic protein extracts from primary breast cancer specimens. Anticancer Res 13: 427-432, 1993.
177. Ashley DM, Kong FM, Bigner DD and Hale LP: Endogenous expression of transforming growth factor betal inhibits growth and tumorigenicity and enhances Fas-mediated apoptosis in a murine high-grade glioma model. Cancer Res 58: 302-309, 1998.
178. Wu SP, Theodorescu D, Kerbel RS, Willson JK, Mulder KM, Humphrey LE and Brattain MG, TGF-β 1 is an autocrine-negative growth regulator of human colon carcinoma FET cells in vivo as revealed by transfection of an antisense expression vector. J Cell Biol 116: 187-196, 1992.
179. Levine AE and Lewis LR: Transforming growth factor-β2 is an autocrine growth inhibitory factor for the MOSER human colon carcinoma cell line. Cancer Lett 68: 33-41, 1993.
180. Travers MT, Barrett-Lee PJ, Berger U, Luqmani YA, Gazet J-C, Powles TJ and Coombes RC: Growth factor expression in normal, benign and malignant breast tissue. Br Med J 296: 1621-1624, 1988.
181. Zugmaier G, Ennis BW, Deschauer B, Katz D, Knabbe C, Wilding G, Daly P, Lippman ME and Dickson RB: Transforming growth factors type β1 and β2 are equipotent growth inhibitors of human breast cancer cell lines. J Cell Physiol 141: 353-361, 1989.
182. Jeng M-H, ten Dijke P, Iwata KK and Jordan VC: Regulation of the levels of three transforming growth factor β mRNAs by estrogen and their effects on the proliferation of human breast cancer cells. Mol Cell Endocrinol 97: 115-123, 1993.
183. Auviṅen P, Lipponen P, Johansson R and Syrjanen K: Prognostic significance of TGF-β2 expression in female breast cancer. European J Cancer 31A: 851, 1995.
184. Silberstein GB and Daniel CW: Reversible inhibition of mammary gland growth by transforming growth factor-β. Science 237: 291-292, 1987.
185. Kopp A, Jonat W, Schmahl M and Knabbe C: Transforming growth factor β2 levels in plasma of patients with metastatic breast cancer treated with tamoxifen. Cancer Res 55: 4512-4515, 1995.
186. Steiner MS and Barrack ER: Transforming growth factor-β1 overproduction in prostate cancer: effects on growth in vivo and in vitro. Mol Endo 6: 15-25, 1992.
187. Friess H, Yamanaka Y, Buchler M, Ebert M, Beger HG, Gold LI and Korc M: Enhanced expression of transforming growth factor β isoforms in pancreatic cancer correlates with decreased survival. Gastroenterology 105: 1846-1856, 1993.
188. Jennings MT, Maciunas RJ, Carver R, Bascom CC, Juneau P, Misulis K and Moses HL: TGF-β1 and TGF-β2 are potential growth regulators for low-grade and malignant gliomas in vitro: evidence in support of an autocrine hypathesis. Int J Cancer 49: 129-139, 1991.
189. Fontana A, Bodmer S, Frei K, Malipiero U and Siepl C: Expression of TGF-β2 in human glioblastoma: a role in resistance to immune rejection. Ciba-Found-Symp 157: 232-241, 1991.
190. Albino AP, Davis BM and Nanus DM: Induction of growth factor RNA expression in human malignant melanoma: markers of transformation. Cancer Res 51: 4815-4820, 1991.
191. Reed JA, McNutt S, Prieto VG and Albino A: Expression of transforming growth factor-β2 in malignant melanoma correlates with the depth of tumor invasion. Amer J Pathol 145: 97-104, 1994.
192. Constam DB, Philipp J, Valipiero UV, ten Dijke P, Schachner M and Fontana A: Differential expression of transforming growth factor-β2, and -β3 by glioblastoma cells, astrocytes and microglia. J Immunol 148: 1404-1410, 1992.
193. Barnum SR and Jones JL: Transforming growth factor-β1 inhibits inflammatory cytokine-induced C3 gene expression in astrocytes. J Immunol 152: 765-773, 1994.
194. Johnson MD, Federspiel C, Gold L and Moses HL: Transforming growth factor-β and transforming growth factor β-receptor expression in human meningioma cells. Am J Path 141: 633-642, 1992.
195. de Martin R, Haendler B, Hofer-Warbinek R, Wrann M, Schlusener H, Siefert JM, Bodmer S, Fontana A and Hofer E: Complementary DNA for human glioblastoma-derived T cell suppressor factor, a novel member of the transforming growth factor-β gene family. EMBO J 6: 3673-3677, 1987.
196. Jachimczak P, Bodhahn U, Schneider J, Behl C, Meixensberger J, Apfel R, Dorries R and Brysch W: The effect of transforming growth factor-β2-specific phosphorothioate-anti-sense oligodeoxynucleotides in reversing cellular immunosuppression in malignant glioma. J Neurosurg 78: 944-951, 1993.
197. Kim S-J, Jeang K-T, Glick AB, Sporn MB and Roberts AB: Promoter sequences of the human transforming growth factor-β1 gene responsive to transforming growth factor-β1 autoinduction. J Biol Chem 264: 7041-7045, 1989.
198. Lafyatis R, Denhez F, Williams T, Sporn M and Roberts A: Sequence specific protein binding to and activation of the TGF-β3 promoter through a repeated TCCC motif. Nucl. Acids Res 19: 6419-6425, 1991.
199. Kelly D, O'Reilly MA and Rizzino A: Differential regulation of the transforming growth factor type-β2 gene promoter in embryonal carcinoma cells and their differentiated cells. Dev Biol 153: 172-175, 1992.
200. Scholtz B, Kingsley-Kallesen M and Rizzino A: Transcription of the transforming growth factor-β2 gene is dependent on an E-box located between an essential CRE/ATF motif and the TATA-box of the gene. J Biol Chem 271: 32375-32380, 1996.
201. Bascom CC, Wolfshohl JR, Coffey RJ Jr, Madisen L, Webb NR, Purchio AR, Derynck R and Moses HL: Complex regulation of transforming growth factor β2 and β3 mRNA expression in mouse fibroblasts and keratinocytes by transforming growth factors β1 and β2. Mol Cell Biol 9: 5508-5515, 1989.
202. Miyazono K, Olofsson A, Colosetti P and Heldin C-H: A role of the latent TGF-β1 binding protein in the assembly and secretion of TGF-β11. EMBO J 10: 1091-1101, 1991.
203. Eklov S, Funa K, Nordgren H, Olofsson A, Kanzaki T, Miyazono K and Nilsson S: Lack of the latent transforming growth factor β binding protein in malignant, but not benign prostatic tissue. Cancer Res 53: 3193-3197, 1993.
204. Mizoi T, Ohtani H, Miyazono K, Miyazawa M, Matsuno S and Nagura H: Immunoelectron microscopic localization of transforming growth factor β1 and latent transforming growth factor β1 binding protein in human gastrointestinal carcinomas: qualitative difference between cancer cells and stromal cells. Cancer Res 53: 183-190, 1993.
205. Henriksen R, Gobl A, Wilander E, Oberg K, Miyazono K and Funa K: Expression and prognostic significance of TGF-β isotypes, latent TGF-β1 binding protein, TGF-β type I and type II receptors, and endoglin in normal ovary and ovarian neoplasms. Lab Invest 73: 213-220 1995.
206. Souchelnitskiy S, Chambaz EM and Feige JJ: Thrombospondins selectively activate one of the two latent forms of transforming growth factor-β present in adrenocortical cell-conditioned medium. Endocrinology 136: 5118-5126, 1995.
207. Lyons RM, Gentry LE, Purchio AF and Moses HL: Mechanism of activation of latent recombinant transforming growth factor β1 by plasmin. J Cell Biol 110: 1361-1367, 1990.
208. De Souza AT, Yamada T, Mills JJ and Jirtle RL: Imprinted genes in liver carcinogenesis. FASEB J 11: 60-67, 1997.
209. Filson AJ, Louvi A, Efstratadis A and Robertson EJ: Rescue of the T-associated maternal effect in mice carrying mull mutations in Igf-2 and Igf2r, two reciprocally imprinted genes. Development 118: 731-736, 1993.
210. Heiter P and Boguski M: Functional Genomics: It's all how you read it. Science 278: 601-602, 1997.
211. Velculescu VE, Zhang L, Vogelstein B and Kinzler KW: Serial analysis of gene expression. Science 270: 484-487, 1995.
212. Schena M, Shalon D, Heller R, Chai A, Brown PO and Davis RW: Parallel human genome analysis: Microarray-based expression monitoring of 1000 genes. Biochemistry 93: 10614-10619, 1996.
213. Lockhart DJ, Dong H, Byrne MC, Follettie MT, Gallo MV, Chee MS, Mittmann M, Wang C, Kobayashi M, Horton H and Brown EL: Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat Biotech 14: 1675-1680, 1996.
214. Risi JL, Iyer VR and Brown PO: Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278: 680-681, 1997.