Butyrate and the Colonocyte: Implications for Neoplasia

Digestive Diseases and Sciences

Volumn 41, Issue 4, 1996, Pages 727-739

  Velázquez, Omaida C ^b   Lederer, Howard M ^b   Rombeau, John L ^a  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b NONE

Author keywords

Butyrate; Cancer; Colonocytes; Differentiation; Oncogenes; Proliferation

Indexed keywords

BUTYRIC ACID;

ANTINEOPLASTIC ACTIVITY; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; COLON CANCER; GENE EXPRESSION; HUMAN; HUMAN CELL; INTESTINE CELL; PRIORITY JOURNAL; PROTO ONCOGENE; REVIEW;

ANIMALS; BUTYRIC ACID; BUTYRIC ACIDS; COLON; COLONIC NEOPLASMS; DIETARY CARBOHYDRATES; DIETARY FATS; DIETARY FIBER; DIETARY PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; TUMOR CELLS, CULTURED;

EID: 0029874733     PISSN: 01632116     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02213129     Document Type: Review

References (117)

1. Jacobs LR: Relationship between dietary fiber and cancer: metabolic, physiologic, and cellular mechanism. Proc Soc Exp Biol Med 182:299-310, 1986
2. Jacobs LR: Role of dietary factors in cell replication and colon cancer. Am J Clin Nutr 48:775-779, 1988
3. Jacobs LR. Influence of soluble fibers on experimental colon carcinogenesis. In Dietary Fiber: Basic and Clinical Aspects. GB Vahouny, D Kritchevesky (eds). New York, Plenum Press, 1990, pp 389-403
4. Lee DK, Chapkin RS, Lupton JR: Dietary fat and fiber modulate colonie cell proliferation in an interactive site-specific manner. Nutr Cancer 20:107-118, 1993
5. Van Munster IP, Nagengast FM: The role of carbohydrate fermentation in colon cancer prevention. Scand J Gastroenterol 28(S200):80-86, 1993
6. McIntyre A, Gibson PR, Young GP: Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut 34:386-391, 1993
7. Howe GR, Benito E, Castelleto R, Cornée J, Estève J, Gallagher RP, Iscovich JM, Deng-ao J, Kaaks R, Kune GA, Kune S, L'Abbé, Lee HP, Lee M, Miller AB, Peters RK, Potter JD, Riboli E, Slattery ML, Trichopoulos D, Tuyns A, Tzonou A, Whittemore AS, Wu-Williams AH, Shu Z: Dietary intake of fiber and decreased risk of cancers of the colon and rectum: Evidence from the combined analysis of 13 case-control studies. JNCI 84:1887-1896, 1992
8. Wolin MJ: Fermentation in the rumen and human large intestine. Science 213:1463-1468, 1981
9. Wrong OM: Carbohydrates. In The Large Intestine: Its Role in Mammalian Nutrition and Homeostasis. OM Wrong, CJ Edmonds, VS Chadwick (eds). New York, Halsted Press, 1981, pp 20-21, 113-114
10. Cummings JU, Branch WJ: Fermentation and production of short-chain fatty acids in human large intestine. In Dietary Fiber: Basic and Clinical Aspects. GB Vahouny and D Kritchevesky (eds). New York, Plenum Press, 1990, pp 131-152
11. Cummings JH, Pomare EW, Branch WJ, Naylor CPE, MacFarlane GT: Short chain fatty acids in human large intestine, portal, hepatic, and venous blood. Gut 28:1221-1227, 1987
12. Roediger WEW: Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83:424-429, 1982
13. Rombeau JL, Kripke SA, Settle RG: Short-chain fatly acids: Production, absorption, metabolism, and intestinal effects. In Dietary Fiber: Basic and Clinical Aspects. GB Vahouny and D Kritchevesky (eds). New York, Plenum Press, 1990, pp 317-339
14. Macfarlane GT, Gibson GR, Macfarlane S: Short-chain fatty acid and lactate production by human intestinal bacteria grown in batch and continuous culture. In Short-Chain Fatty Acids. J Cummings, HJ Binder, K Soergel (eds). Boston, Kluwer Academic Publishers, 1994, pp 44-60
15. Nyman M, Aso NG: Fermentation of dietary fiber components in rat intestinal tract. Br J Nutr 47:357-366, 1982
16. Demigné C, Remesy C: Stimulation of absorption of volatile fatty acids and minerals in cecum of rats adapted to a very high fiber diet. J Nutr 115:53-60, 1985
17. Rechkemmer G, Ronnau K, von Englehardt W: Fermentation of polysaccharides and absorption of short chain fatty acids in the mammalian hindgut. Comp Biochem Physiol 90A:563-568, 1988
18. Macfarlane GT, Gibson GR, Cummings JH: Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 72:54-64, 1992
19. Titegeyer EC, Bourquin LD, Fahey GC, Garleb KA: Fermentability of various fiber sources by human fecal bacteria in vitro. Am J Clin Nutr 53:418-424, 1991
20. Knudsen KE, Jensen BB, Hansen I: Oat bran but not a β-glucan enriched oat fraction enhances butvrate production in the large intestine of pigs. J Nutr 123:1235-1247, 1993
21. Weaver GA, Krause JA, Miller TL, Wolin MJ: Cornstarch fermentation by the colonic microbial community yields more butyrate than does cabbage fiber fermentation; cornstarch fermentation rates correlate negatively with methanogenesis. Am J Clin Nutr 55:70-77, 1992
22. Colony PC: The identification of cell types in the normal adult colon. In Cell and Molecular Biology of Colon Cancer. LH Augenlicht (ed). Boca Raton, CRC Press, 1989, pp 2-21
23. Higgins PJ: Antigenic and cytoarchitectural 'markers' of differentiation pathways in normal and malignant colonic epithelial cells. In Cell and Molecular Biology of Colon Cancer. LU Augenlicht (ed). Boca Raton, CRC Press, 1984, pp 112-132
24. Lipkin M, Enker WE, Winawer SJ: Tritiated-thymidine labeling of rectal epithelial cells in non-prep biopsies of individuals at increased risk for colonie neoplasia. Cancer Lett 37:153-161, 1987
25. Lipkin M: Biomarkers of increased susceptibility to gastrointestinal cancer: New application to studies of cancer prevention in human subjects. Cancer Res 48:235-245, 1988
26. Kim YS, Tsao D, Siddiqui B, Whitehead JS, Arnstein P, Bennette J, Hicks J: Effects of sodium butyrate and dimethylsulfoxide on biochemical properties of human colon cancer cells. Cancer 45:1185-1192, 1980
27. Tsao D, Morita A, Bella A, Luu P, Kim YS: Differential effects of sodium butyrate, dimethylfoxide, retinoic acid on membrane-associated antigen, enzymes and glycoproteins of human rectal adenocarcinoma cells. Cancer Res 42:1052-1058, 1982
28. Whitehead RH, Young GP, Bhathal PS: Effects of short chain fatty acids on a new human colon carcinoma cell line (LIM1215). Gut 27:1457-1436, 1986
29. Czerniak B, Herz F, Westo RP, Koss LG: Modification of H-ras oncogene p-21 expression and cell cycle progression in the human colon cancer cell line HT-29. Cancer Res 47:2826-2830, 1987
30. Awad AB, Horvath PJ, Andersen MS: Influence of butyrate on lipid metabolism, survival, and differentiating of colon cancer cells. Nutr Cancer 16:125-133, 1991
31. Barnard JA, Warwick G: Sodium butyrate rapidly induces 'enterocytic-like' differentiation and growth inhibition of HT-29 cells. Gastroenterology 102:A199, 1992
32. Otaka M, Singhal A, Hakomori S. Antibody-mediated targeting of differentiation inducers to tumor cells: Inhibition of colonie cancer cell growth in vitro and in vivo. Biochem Biophys Res Commun 158:202-208, 1989
33. Velázquez OC, Jabbar A, DeMatteo RP, Rombeau JL: Butyrate inhibits hepatic tumor growth in a murine model of metastatic colorectal cancer. Surgery (in press).
34. Gibson PR, Moeller I, Kagelari O, Folino M, Young GP: Contrasting effects of butvrate on differentiation of neoplastic and nonneoplastic colonie epithelial cells. J Gastroenterol Hepatol 7:165-172, 1992
35. Sakata T: Influence of short-chain tatty acids on epithelial cell division of digestive tract. J Exp Physiol 69:639-648, 1984
36. Sakata T: Stimulatory effect of short-chain fatty acids on epithelial cell proliferation in the rat intestine: A possible explanation for trophic effects of fermentable fiber, gut microbes and luminal trophic factors. Br J Nutr 58:95-101, 1987
37. Kripke SA, Fox AD, Berman JM, Settle RG, Rombeau JL: Stimulation of intestinal mucosal growth with intracolonic infusion of short-chain fatty acids. J Parenter Enter Nutr 13:109-116, 1989
38. Janne P, Carpenter Y, Willems G: Colonic mucosal atrophy induced by a liquid elemental diet in rats. Am J Dig Dis 22:808-812, 1977
39. Koruda MJ, Rolandelli RH, Bliss DZ, Hastings J, Rombeau JL, Settle RG: Parenteral nutrition supplemented with short-chain fatty acids: Effect on the small-bowel mucosa in normal rats. Am J Clin Nutr 51:685-689, 1990
40. Friedel D, Levine GM: Effect of short-chain fatty acids on colonic function and structure. J Parenter Enter Nutr 16(1):1-4, 1992
41. Lupton JR, Kurtz PP: Relationship of colonie luminal short-chain fatty acids and pH to in vivo cell proliferation in rats. J Nutr 123:1522-1530, 1993
42. Scheppach W, Bartram P, Richter A, Richter F, Dusel G, Liepold H, Hofstetter G, Ruthlein J, Kasper H: Effect of short-chain fatty acids on the human colonie mucosa in vitro. J Parenter Enter Nutr 16:43-48, 1992
43. Sakata T, von Englehardt W: Stimulatory effects of short chain fatty acids on the epithelial cell proliferation in rat large intestine. Comp Biochem Physiol 74A:459-462, 1983
44. Frankel WL, Lew J, Su B, Bain A, Klurfeld D, Einhorn E, MacDermott RP, Rombeau JL: Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterology 106:375-380, 1994
45. Sakata T: Stimulatory effect of short-chain fatty acids on epithelial cell proliferation of isolated and denervated jejunal segment of the rat. Scand J Gastroenterol 24:886-890, 1989
46. Toscani A, Soprano DR, Soprano KJ: Molecular analysis of sodium butyrate-induced growth arrest. Oncogene Res 3:223-238, 1988
47. Young GP, Gibson PR: Butyrate and colorectal cancer cell. In Short-Chain Fatty Acids. J Cummings, HJ Binder, K Soergel (eds). Boston, Kluwer Academic Publishers, 1994, pp 148-160
48. Barnard JA, Warwick G: Butyrate rapidly induces growth inhibition and differentiation in HT-29 cells. Cell Growth Differ 4:495-501, 1993
49. Bartram HP, Scheppach W, Schmid H, Hofmann A, Dusel G, Richter F, Richter A, Kasper H: Proliferation of human colonic mucosa as an intermediate biomarker of carcinogenesis: Effects of butyrate, deoxycholate, calcium, ammonia, and pH. Cancer Res 53:3283-3288, 1993
50. 2 release and cell proliferation in the human sigmoid colon. J Parenter Enter Nutr 19:182-186 1994
51. Velázquez OC, Zhou D, Seto R, Jabbar A, Choi J, Lederer HM, Rombeau J: In vivo crypt surface proliferation is decreased by butyrate and increased by deoxycholate in normal rat colon: Associated in vivo effects on c-fos and c-jun expression. J Parenter Enter Nutr (in press)
52. Young GP, Gibson PR: Contrasting effects of butyrate on proliferation and differentiation of normal and neoplastic cells. In Short Chain Fatty Acids: Metabolism and Clinical Importance. Report of the Tenth Ross Conference on Medical Research. Columbus, Ohio, Ross Laboratories, 1991, pp 50-55
53. Young GP, Macrae FA, Gibson PR, Alexeyeff M, Whitehead R: Brush border hydrolases in normal and neoplastic colonic epithelium. J Gastroenterol Hepatol 7:347-357, 1992
54. Bell L, Williams L: Histochemical demonstration of alkaline phosphatase in human large intestine, normal and deceased. Histochemistry 60:84-90, 1979
55. Herz F, Schermer A, Halwer M, Bogart LH: Alkaline phosphatase in HT-29, a human colon cancer cell line: influence of sodium butyrate and hyperosmolality. Arch Biochem Biophys 210:581-591, 1981
56. Morita A, Tsao D, Kim YS: Effect of sodium butyrate on alkaline phosphatase in HRT-18, a human rectal cancer cell line. Cancer Res 42:4540-4545, 1982
57. Ito F, Chou JY: Induction of placental alkaline phosphatase biosynthesis by sodium butyrate. J Biol Chem 259:2526-2530, 1984
58. Chung YS, Song IS, Erickson RH, Sleisenger MH, Kim YS: Effect of growth and sodium hutyrate on brush border membrane associated hydrolases in human colorectal cancer cell lines. Cancer Res 45:2976-2982, 1985
59. Hay FG, Duncan LW, Langdon SP, Leonard RCF: Modulation of the cluster 1 and mucin antigens in human small cell lung cancer and other epithelial tumour cell lines after treatment with the differentiation inducing agent, sodium butyrate. Br J Cancer 14:33-35, 1991
60. Frommel TO, Coon JS, Tsuro T, Roninson IB: Variable effects of sodium butyrate on the expression and function of the MDR-1 (P-glycoprotein) gene in colon carcinoma cell lines. Int J Cancer 55:297-302, 1993
61. Mickley LA, Batest SE, Richert ND, Currier S, Tanaka S, Foss F, Rosen N, Fojo AT: Modulation of the expression of a multidrug resistance gene (mdr-1/P-glycoprotein) by differentiating agents. J Biol Chem 264:18031-18040, 1989
62. Petit JM, Chauffert B, Dimanche-Boitrel MT, Genne P, Duchamp O, Martin Francois: mdr 1 gene-expression and villin synthesis in a colon cancer cell line differentiated by sodium butyrate. Anticancer Res 13:487-490, 1993
63. White MW: Metabolism of the malignant cell, in vivo is anaerobic and significantly plays a factor in the pathway to carcinogenesis. Med Hypotheses 39(4):323-333 1992
64. Fischer H: Malignancy may contribute to rapid evolution. Med Hypotheses 28(1):35-38 1989
65. Isfort RJ, Cody DB, Asquith TN, Ridder GM, Stuard SB, LeBoeuf RA: Induction of protein phosphorylation, protein synthesis, immediate early gene expression and cellular proliferation by intracellular pH modulation. Eur J Biochem 213(1):349-357, 1993
66. Nathan DF, Burkhart SR, Morin MJ: Increased cell surface EGF receptor expression during the butyrate-induced differentiation of human HCT-116 colon tumor cell clone. Exp Cell Res 190:76-84, 1990
67. Kondoh N, Schweinfest CW, Henderson KW, Papas TS: Differential expression of s19 ribosomal protein, laminin-binding protein, and human lymphocyte antigen class I messenger RNAs associated with colon carcinoma progression and differentiation. Cancer Res 52:791-796, 1992
68. Boyd D, Florent G, Kim P, Brattain M: Determination of the levels of urokinase and its receptors in human colon carcinoma cell lines. Cancer Res 48:3112-3116, 1988
69. Kohga S, Harvey Sr, Weaver Rm, Markus G: Localization of plasminogen activators in human colon cancer by immunoperoxidase staining, Cancer Res 45:1787-1796, 1985
70. Gibson PR, Rosella O, Rosella G, Young GP: Butyrate is a potent inhibitor of urokinase secretion by normal colonic epithelium in vitro. Gastroenterology 107(2):410-419, 1994
71. Bresalier RS, Rockwell RW, Dahiya R, Dull OY, Kim YS: Cell surface sialoprotein alterations in metastatic murine colon cancer cell lines selected in an animal model for colon cancer metastasis. Cancer Res 50:1299-1307, 1990
72. Bryant G, Haberern C, Rao CN, Liotta LA: Butyrate induced reduction of tumor cell laminin receptors. Cancer Res 46:807-811, 1986
73. Aumailley M, Nurcombe V, Edgar D, Paulsson M, Timpl R: The cellular interactions of laminin fragments. Cell adhesion correlates with two fragment-specific high affinity binding sites. J Biol Chem 262:11,532-11,538, 1987
74. Yannariello-Brown J, Weaver U, Liotta L, Madri JA: Distribution of a 69-kD laminin-binding protein in aortic and microvascular endothelial cell: Modulation during cell attachment, spreading, and migration. J Cell Biol 106:1773-1786, 1988
75. Herbst TJ, McCarthy JB, Tsilibary EC, Furcht LT: Differential effects of laminin, intact type IV collagen, and specific domains of type IV colagen on endothelial cell adhesion and migration. J Cell Biol 106:1365-1373, 1988
76. Ocalan M, Goodman SL, Kuhl U, Hanuschka SD, de Mark K: Laminin alters cell shape and stimulates motility and proliferation of marine skeletal myoblasts. Dev Biol 125:158-167, 1988
77. Kubota Y, Kleinman HK, Martin GR, Lawlwy TJ: Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107:1589-1598, 1988
78. Daneker GW Jr, Piazza AJ, Steele GS Jr, Mercurio AM: Relationship between extracellular matrix interactions and degree of differentiation in human colon carcinoma cell lines. Cancer Res 49:681-686, 1989
79. Terranova VP, Rao CN, Kalebic T, Margulies IM, Liotta LA: Laminin receptor on human breast carcinoma cells. Proc Natl Acad Sci USA 80:444-448, 1983
80. Wewer UM, Liotta LA, Jaye M, Ricca GA, Drohan WN, Claysmith AP, Rao CN, Wirth P, Coligan JE, Albrechtsen R, Mudryi M, Sobel ME: Altered levels of laminin receptor mRNA in various human carcinoma cells that have different abilities to bind laminin. Proc Natl Acad Sci USA 83:7137-7141, 1986
81. Wilson JR, Weiser M: Colonic cancer cell (HT29) adhesion to laminin is altered by differentiation: Adhesion may involve galactosyltransferase. Exp Cell Res 201:330-334, 1992
82. Fearon ER, Volgelstein B: A genetic model for colorectal tumorigenesis. Cell 61:759-767, 1990
83. Willson JKV: Biology of large bowel cancer. Hematol Oncol Clin North Am 3:19-34, 1989
84. Young GP, Gibson PR: Butyrate and the human cancer cell. In Physiologic and Clinical Aspects of Short-Chain Fatty Acids. JH Cummings, JL Rombeau, T Sakata (eds). Cambridge, Cambridge University Press, 1995, pp 319-336
85. Stoddart JH, Lane MA, Niles RM: Sodium butyrate suppresses the transforming activity of an activated N-ras oncogene in human colon carcinoma cells. Exp Cell Res 184:16-27, 1989
86. lck associated with butyrate-induced differentiation of human colon carcinoma cells. Oncogene Res 5:13-23, 1989
87. Marcu KB, Bossone SA, Patel AJ: Myc function and regulation. Annu Rev Biochem 61:809-860, 1992
88. Tsuboi K, Hirayoshi K, Takeuchi K, Sabe H, Shimada Y, Ohshio G, Tobe T, Hatanaka M: Expression of the c-myc gene in human gastrointestinal malignancies. Biochem Biophys Res Commun 146:669-704, 1987
89. Stewart J, Evan G, Watson J, Sikora K: Detection of the c-myc oncogene in colonie polyps and carcinomas. Br J Cancer 53:1-6, 1986
90. Finley GG, Schulz NT, Hill SA, Geiser JR, Pipas JM, Meisler AI: Expression of the myc gene family in different stages of human colorectal cancer. Oncogene 4:963-971, 1989
91. Untawale S, Blick M: Oncogene expression in adenocarcinomas of the colon and in colon tumour-derived cell lines. Anticancer Res 8:1-7, 1988
92. Dolcetti R, DeRe V, Viel A, Pistello M, Tavian M, Boicchi M, Meisler AI: Nuclear oncogene amplification or rearrangement is not involved in human colorectal malignancies. Eur J Cancer Clin Oncol 24:1321-1328, 1988
93. Taylor CW, Kim YS, Childress-Fields KE, Yeoman LC: Sensitivity of nuclear c-myc levels and induction to differentiation-inducing agents in human colon tumor cell lines. Cancer Lett 62:95-105, 1992
94. Barnard JA, Warwick G: Butyrate rapidly induces growth inhibition and differentiation in HT-29 cells. Cell Growth Differ 4:495-501, 1993
95. Heruth DP, Zirnstein GW, Bradley JF, Rothberg PG: Sodium butyrate causes an increase in the block to transcriptional elongation in the c-myc gene in SW837 rectal carcinoma cells. J Biol Res 268:20466-20472, 1993
96. Souleimani A, Asselin C: Regulation of c-myc expression by sodium butyrate in the colon carcinoma cell line CaCo-2. FEBS Lett 326:45-50, 1993
97. Bohmann D, Bos TJ, Admon A, Nishimura T, Vogt PK, Tjian R: Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science 238:1386-1392, 1987
98. Souleimani A, Asselin C: Regulation of c-fos expression by sodium butyrate in the human colon carcinoma cell line CaCo-2. Biochem and Biophys Resch Commun 193(1):330-336, 1993
99. Toribara NW, Sack TL, Gum JR, Ho SB, Shively JE, Willson JKV, Kim YS: Heterogeneity in the induction and expression of carcinoembryonic antigen-related antigens in human colon cancer cell lines. Cancer Res 49:3321-3327, 1989
100. Heerdt BG, Augenlicht LH: Effects of fatty acid on expression of genes encoding subunits of cytochrome c oxidase and cytochrome c oxidase activity in HT29 human colonie adenocarcinoma cells. J Biol Chem 266:19120-19126, 1991
101. Hague A, Manning AM, Hanlon KA, Huschtscha LI, Hart D, Paraskeva C: Sodium butyrate induces apoptosis in the human colonic tumour cell line in a p-53 independent pathway: implications for the possible role of dietary fibre in the prevention of large bowel cancer. Int J Cancer 55:498-505, 1993
102. Kruh J, Tichonicky L, Defer N: Effect of butyrate on gene expression. In Short-Chain Fatly Acids. J Cummings, HJ Binder, K Soergel (eds). Boston, Kluwer Academic Publishers, 1994, pp 135-147
103. Boffa LC, Vidali G, Mann RS, Allfrey VG: Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J Biol Chem 253:3364-3366, 1978
104. Boffa L, Vidali G, Mann R, Allfrey V: Manifold effects of sodium butyrate on nuclear function. Selective and reversible inhibition of phosphorylation of histones H1 and H2A and impaired methylation of lysine and arginine residues in nuclear protein fractions. J Biol Chem 256:9612-9621, 1981
105. Kruh J: Effect of sodium butyrate, a new pharmacological agent, on cells in culture. Mol Cell Biol 42:65-82, 1982
106. Whitlock JP, Galeazzi D, Schulman H: Acetylation and calcium dependent phosphorylation of histone H3 in nuclei from butyrate-treated HeLa cells. J Biol Chem 258:1299-1304, 1983
107. Parker MI, de Haan JB, Gevers W: DNA hypermethylation in sodium byturate-treated WI-38 fibroblasts. J Biol Chem 261:2786-2790, 1985
108. Rastl E, Swetly P: Expression of poly-(adenosine diphosphate-ribose) polymerase activity in erythroleukemic mouse cells during cell cycle and erythropoietic differentiation. J Biol Chem 253:4333-4340, 1978
109. Cousenes LS, Gallwitz D, Alberts BM: Different accessibilities in chromatin to histone acetylase. J Biol Chem 254:1716-1723, 1979
110. Christman JK, Weich N, Schoenbrun B, Schneidman N, Acs G: Hypomethylation of DNA during differentiation of Friend erythroleukemia cells. J Cell Biol 86:366-370, 1980
111. Reeves R, Dserjesi P: Sodium butyrate induces new gene expression in Friend erythroleukemic cells. J Biol Chem 254:4383-4290, 1979
112. Vidali G, Boffa LC, Bradbury EM, Allfrey VG: Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histone H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc Natl Acad Sci USA 75:2239, 1978
113. Deng G, Liu G, Hu L, Gum JR, Kim YS: Transcriptional regulation of the human placental-like alkaline phosphatase gene and mechanisms involved in its induction by sodium butyrate. Cancer Res 52:3378-3383, 1992
114. Willumsen BM, Christensen A, Hubbert NL, Papageorge AG, Lowy DR: The p21 ras C-terminus is required for transformation and membrane association. Nature 310:583-586, 1984
115. Schafer WR, Kim R, Sterne R, Thorner J, Kim S, Rine J. Genetic and pharmacological suppression of oncogenic mutations in ras genes of yeast and humans. Science 245:379-385, 1989
116. Bos JL, Fearon ER, Hamilton SR, Verlaan-de Vries M, van Boom JH, van der Eb AJ, Vogelstein B: Prevalence of ras gene mutations in human colorectal cancers. Nature 327:293-297, 1987
117. Volgelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM, Bos JL: Genetic alterations during colorectal-tumor development. N Engl J Med 319:525, 1988