Folate transport gene inactivation in mice increases sensitivity to colon carcinogenesis

Cancer Research

Volumn 65, Issue 3, 2005, Pages 887-897

  Ma, David W L ^a,g   Finnell, Richard H ^a,b,c   Davidson, Laurie A ^a   Callaway, Evelyn S ^a   Spiegelstein, Ofer ^c,h   Piedrahita, Jorge A ^d   Salbaum, J Michael ^e,i   Kappen, Claudia ^e,i   Weeks, Brad R ^b   James, Jill ^f   Bozinov, Daniel ^c   Lupton, Joanne R ^a,b   Chapkin, Robert S ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e MAYO CLINIC   (United States)

^f UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^g UNIVERSITY OF TORONTO   (Canada)

^h TEVA PHARMACEUTICALS   (Israel)

ⁱ UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; FOLATE BINDING PROTEIN; MESSENGER RNA; REDUCED FOLATE CARRIER; S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COLON ADENOCARCINOMA; COLON CARCINOGENESIS; COLON MUCOSA; CONTROLLED STUDY; CRYPT CELL; DNA MICROARRAY; EPITHELIUM DYSPLASIA; FOLIC ACID BLOOD LEVEL; GENE DELETION; GENE EXPRESSION; GENE INACTIVATION; HETEROZYGOSITY; HOMEOSTASIS; INFLAMMATION; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; UNINDEXED SEQUENCE; WILD TYPE;

NON-PROGRAMMATIC;

ANIMALS; AZOXYMETHANE; CARCINOGENS; CARRIER PROTEINS; CELL CYCLE; CELL TRANSFORMATION, NEOPLASTIC; COLON; COLONIC NEOPLASMS; GENE EXPRESSION PROFILING; GENE SILENCING; GENETIC PREDISPOSITION TO DISEASE; KIDNEY; MALE; MEMBRANE TRANSPORT MODULATORS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRECANCEROUS CONDITIONS; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; S-ADENOSYLHOMOCYSTEINE; S-ADENOSYLMETHIONINE;

EID: 13444291027     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Jemal A, Thomas A, Murray T, Thun M. Cancer statistics, 2002. CA Cancer J Clin 2002;52:23-47.
2. Kim YI, Salomon RN, Graeme-Cook F, et al. Dietary folate protects against the development of macroscopic colonic neoplasia in a dose responsive manner in rats. Gut 1996;39:732-40.
3. Kim YI, Pogribny IP, Basnakian AG, et al. Folate deficiency in rats induces DNA strand breaks and hypomethylation within the p53 tumor suppressor gene. Am J Clin Nutr 1997;65:46-52.
4. Biasco G, Zannoni U, Paganelli GM, et al. Folic acid supplementation and cell kinetics of rectal mucosa in patients with ulcerative colitis. Cancer Epidemiol Biomarkers Prev 1997;6:469-71.
5. Song J, Medline A, Mason JB, Gallinger S, Kim YI. Effects of dietary folate on intestinal tumorigenesis in the apcMin mouse. Cancer Res 2000;60:5434-40.
6. -/- mice. Cancer Res 2000;60:3191-9.
7. Janne PA, Mayer RJ. Chemoprevention of colorectal cancer. N Engl J Med 2000;342:1960-8.
8. Jacobs EJ, Connell CJ, Patel AV, et al. Multivitamin use and colon cancer mortality in the Cancer Prevention Study II cohort (United States). Cancer Causes Control 2001;12:927-34.
9. Finnell RH, Spiegelstein O, Wlodarczyk B, et al. DNA methylation in Folbp1 knockout mice supplemented with folic acid during gestation. J Nutr 2002;132:2457-61S.
10. Friso S, Choi SW, Girelli D, et al. A common mutation in the 5,10-methylenetetrahydrofolate reductase gene affects genomic DNA methylation through an interaction with folate status. Proc Natl Acad Sci U S A 2002;99:5606-11.
11. Sibani S, Melnyk S, Pogribny IP, et al. Studies of methionine cycle intermediates (SAM, SAH), DNA methylation and the impact of folate deficiency on tumor numbers in Min mice. Carcinogenesis 2002;23:61-5.
12. Choi SW, Kim YI, Weitzel JN, Mason JB. Folate depletion impairs DNA excision repair in the colon of the rat. Gut 1998;43:93-9.
13. Duthie SJ, Hawdon A. DNA instability (strand breakage, uracil misincorporation, and defective repair) is increased by folic acid depletion in human lymphocytes in vitro. FASEB J 1998;12:1491-7.
14. Duthie SJ, Narayanan S, Blum S, Pirie L, Brand GM. Folate deficiency in vitro induces uracil misincorporation and DNA hypomethylation and inhibits DNA excision repair in immortalized normal human colon epithelial cells. Nutr Cancer 2000;37:245-51.
15. Jaszewski R, Khan A, Sarkar FH, et al. Folic acid inhibition of EGFR-mediated proliferation in human colon cancer cell lines. Am J Physiol 1999;77:C1142-8.
16. Akoglu B, Faust D, Milovic V, Stein J. Folate and chemoprevention of colorectal cancer: is 5-methyltetrahydrofolate an active antiproliferative agent in folate-treated colon-cancer cells? Nutrition 2001;17:652-3.
17. Blount BC, Mack MM, Wehr CM, et al. Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci U S A 1997;94:3290-5.
18. Choi SW, Mason JB. Folate status: effects on pathways of colorectal carcinogenesis. J Nutr 2002;132:2413-8S.
19. Terry P, Jain M, Miller AB, Howe GR, Rohan TE. Dietary intake of folic acid and colorectal cancer risk in a cohort of women. Int J Cancer 2002;97:864-7.
20. Nensey YM, Arlow FL, Majumdar AP. Aging. Increased responsiveness of colorectal mucosa to carcinogen stimulation and protective role of folic acid. Dig Dis Sci 1995;40:396-401.
21. Sohn KJ, Stempak JM, Reid S, Shirwadkar S, Mason JB, Kim YI. The effect of dietary folate on genomic and p53-specific DNA methylation in rat colon. Carcinogenesis 2003;24:81-90.
22. Khosraviani K, Weir HP, Hamilton P, Moorehead J, Williamson K. Effect of folate supplementation on mucosal cell proliferation in high risk patients for colon cancer. Gut 2002;51:195-9.
23. Selhub J, Jacques PF, Wilson PW, Rush D, Rosenberg IH. Vitamin status and intake as primary determinants of homocysteinemia in an elderly population. JAMA 1993;270:2693-8.
24. Kim YI. Folate and carcinogenesis: evidence, mechanisms, and implications. J Nutr Biochem 1999;10:66-88.
25. Sierra EE, Goldman ID. Recent advances in the understanding of the mechanism of membrane transport of folates and antifolates. Semin Oncol 1999;26:11-23.
26. Spiegelstein O, Eudy JD, Finnell RH. Identification of two putative novel folate receptor genes in humans and mouse. Gene 2000;258:117-25.
27. Matherly LH. Molecular and cellular biology of the human reduced folate carrier. Prog Nucleic Acid Res Mol Biol 2001;67:131-62.
28. Kamen BA. Folate receptor α. In: Rao MS, editor. Stem cells and CNS development. New Jersey: Humana Press; 2002. p. 117-35.
29. Wang Y, Zhao R, Russell RG, Goldman ID. Localization of the murine reduced folate carrier as assessed by immunohistochemical analysis. Biochim Biophys Acta 2001;1513:49-54.
30. Weitman SD, Lark RH, Coney LR, et al. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res 1992;52:3396-401.
31. Holm J, Hansen SI, Hoier-Madsen M, Sondergaard K, Bzorek M. The high-affinity folate receptor of normal and malignant human colonic mucosa. APMIS 1994;102:828-36.
32. Piedrahita JA, Oetama B, Bennett GD, et al. Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development. Nat Genet 1999;23:228-32.
33. Zhao R, Russell RG, Wang Y, et al. Rescue of embryonic lethality in reduced folate carrier-deficient mice by maternal folic acid supplementation reveals early neonatal failure of hematopoietic organs. J Biol Chem 2001;276:10224-8.
34. Piedrahita JA, Oetama B, Bennett GD, et al. Mice lacking the folic acid-biuding protein Folbp1 are defective in early embryonic development. Nat Genet 1999;23:228-32.
35. Reid LH, Shesely EG, Kim HS, Smithies O. Cotransformation and gene targeting in mouse embryonic stem cells. Mol Cell Biol 1991;11:2769-77.
36. Rucker EB, Piedrahita JA. Cre-mediated recombination at the murine whey acidic protein (mWAP) locus. Mol Reprod Dev 1997;48:324-31.
37. Horne DW, Patterson D. Lactobacillus casei microbiological assay of folic acid derivatives in 96-well microtiter plates. Clin Chem 1988;34:2357-9.
38. Spiegelstein O, Merriweather MY, Wicker NJ, Finnell RH. Valproate-induced neural tube defects in folate-binding protein-2 (Folbp2) knockout mice. Birth Defects Res Part A Clin Mol Teratol 2003;67:974-8.
39. Melnyk S, Pogribna M, Pogribny IP, Yi P, James SJ. Measurement of plasma and intracellular S-adenosylmethionine and S-adenosylhomocysteine utilizing coulometric electrochemical detection: alterations with plasma homocysteine and pyridoxal 5′-phosphate concentrations. Clin Chem 2000;46:265-72.
40. Piyathilake CJ, Johanning GL, Macaluso M, Whiteside MA, Heimburger DC, Grizzle WE. Localized deficiencies of folate and vitamin B12 in lung tissues are associated with global DNA methylation. Nutr Cancer 2000;37:99-107.
41. Hamedani MP, Valko K, Qi X, Welham KJ, Gibbons WA. Two-dimensional high-performance liquid chromatographic method for assaying S-adenosyl-L- methionine and its related metabolites in tissues. J Chromatogr 1993;619:191-8.
42. Park CM, Reid PE, Walker DC, MacPherson BR. A simple, practical "Swiss roll" method of preparing tissues for paraffin or methacrylate embedding. J Microsc 1987;145:115-20.
43. Beckstead JH. A simple technique for preservation of fixation-sensitive antigens in paraffin-embedded tissues. J Histochem Cytochem 1994;42:1127-34.
44. Chang WC, Chapkin RS, Lupton JR. Predictive value of proliferation, differentiation and apoptosis as intermediate markers for colon tumorigenesis. Carcinogenesis 1997;18:721-30.
45. Davidson LA, Lupton JR, Miskovsky E, Fields AP, Chapkin RS. Quantification of human intestinal gene expression profiles using exfoliated colonocytes: a pilot study. Biomarkers 2003;8:51-61.
46. Yang YH, Buckley MJ, Speed TP. Analysis of cDNA microarray images. Brief Bioinform 2001;2:341-9.
47. Murray NR, Davidson LA, Chapkin RS, Clay Gustafson W, Schattenberg DG, Fields AP. Overexpression of protein kinase C βII induces colonic hyperproliferation and increased sensitivity to colon carcinogenesis. J Cell Biol 1999;145:699-711.
48. McLellan EA, Medline A, Bird RP. Dose response and proliferative characteristics of aberrant crypt foci: putative preneoplastic lesions in rat colon. Carcinogenesis 1991;12:2093-8.
49. Matherly LH, Goldman DI. Membrane transport of folates. Vitam Horm 2003;66:403-56.
50. Caudill MA, Wang JC, Melnyk S, et al. Intracellular S- adenosylhomocysteine concentrations predict global DNA hypomethylation in tissues of methyl-deficient cystathionine β-synthase heterozygous mice. J Nutr 2001;131:2811-8.
51. Preston-Martin S, Pike MC, Ross RK, Jones PA, Henderson BE. Increased cell division as a cause of human cancer. Cancer Res 1990;50:7415-21.
52. McLellan EA, Bird RP. Aberrant crypts: potential preneoplastic lesions in the murine colon. Cancer Res 1988;48:6187-92.
53. Takayama T, Katsuki S, Takahashi Y, et al. Aberrant crypt foci of the colon as precursors of adenoma and cancer. N Engl J Med 1998;339:1277-84.
54. Pretlow TP, O'Riordan MA, Somich GA, Amini SB, Pretlow TG. Aberrant crypts correlate with tumor incidence in F344 rats treated with azoxymethane and phytate. Carcinogenesis 1992;13:1509-12.
55. Brzezinska A, Winska P, Balinska M. Cellular aspects of folate and antifolate membrane transport. Acta Biochim Pol 2000;47:735-49.
56. Hernandez-Blazquez FJ, Habib M, Dumollard JM, et al. Evaluation of global DNA hypomethylation in human colon cancer tissues by immunohistochemistry and image analysis. Gut 2000;47:689-93.
57. Fang JY, Xiao SD. Alteration of DNA methylation in gastrointestinal carcinogenesis. J Gastroenterol Hepatol 2001;16:960-8.
58. Jhaveri MS, Wagner C, Trepel JB. Impact of extracellular folate levels on global gene expression. Mol Pharmacol 2001;60:1288-95.
59. Davis CD, Uthus EO. Dietary folate and selenium affect dimethylhydrazine-induced aberrant crypt formation, global DNA methylation and one-carbon metabolism in rats. J Nutr 2003;133:2907-14.
60. Magnuson BA, Carr I, Bird RP. Ability of aberrant crypt foci characteristics to predict colonic tumor incidence in rats fed cholic acid. Cancer Res 1993;53:4499-504.
61. Papanikolaou A, Wang QS, Papanikolaou D, Whiteley HE, Rosenberg DW. Sequential and morphological analyses of aberrant crypt foci formation in mice of differing susceptibility to azoxymethane-induced colon carcinogenesis. Carcinogenesis 2000;21:1567-72.
62. Park HS, Goodlad HA, Wright NA. The incidence of aberrant crypt foci and colonic carcinoma in dimethylhydrazine-treated rats varies in a site-specific manner and depends on tumor histology. Cancer Res 1997;57:4507-10.
63. Ward JM. Morphogenesis of chemically induced neoplasms of the colon and small intestine in rats. Lab Invest 1974;30:505-13.
64. Crott JW, Choi SW, Ordovas JM, Ditelberg JS, Mason JB. Effects of dietary folate and aging on gene expression in the colonic mucosa of rats: implications for carcinogenesis. Carcinogenesis 2004;25:69-76.
65. Piva R, Liu J, Chiarle R, Podda A, Pagano M, Inghirami G. In vivo interference with Skp1 function leads to genetic instability and neoplastic transformation. Mol Cell Biol 2002;22:8375-7.