In vitro folate deficiency induces apoptosis by a p53, Fas (Apo-1, CD95) independent, bcl-2 related mechanism in phytohaemagglutinin-stimulated human peripheral blood lymphocytes

British Journal of Nutrition

Volumn 95, Issue 5, 2006, Pages 870-878

  Lin, Hui Li ^b   Chen, Chung Jern ^a   Tsai, Wen Chan ^a   Yen, Jeng Hsien ^a   Liu, Hong Wen ^a  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; bcl 2; Folate deficiency; p53

Indexed keywords

FAS ANTIGEN; FOLIC ACID; HYPOXANTHINE; INTERLEUKIN 2; MESSENGER RNA; NUCLEOSIDE DERIVATIVE; PHOSPHATE; PHYTOHEMAGGLUTININ; PROTEIN BCL 2; PROTEIN P53; THYMINE;

APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL CYCLE S PHASE; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; FOLIC ACID DEFICIENCY; HUMAN; HUMAN CELL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE; PERIPHERAL LYMPHOCYTE; PROTEIN EXPRESSION;

ANTIGENS, CD95; APOPTOSIS; CELLS, CULTURED; DOWN-REGULATION; FOLIC ACID; FOLIC ACID DEFICIENCY; HUMANS; HYPOXANTHINE; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; PHYTOHEMAGGLUTININS; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; S PHASE; THYMIDINE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33744491260     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1079/BJN20051579     Document Type: Article

References (44)

1. Benito A, Silva M, Grillot D, Nunez G & Fernandez-Luna JL (1996) Apoptosis induced by erythroid differentiation of human leukemia cell lines is inhibited by Bcl-XL. Blood 87, 3837-3843.
2. Benjamin CB, Matthew MM, Carol MW, James TMG, Robert AH, Wang GS, Wickramasinghe N, Richard BE & Ames BN (1997) Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci USA 94, 3290-3295.
3. Bunout D, Petermann M, Hirsch S, de la Maza P, Suazo M, Barrera G & Kauffman R (2000) Low serum folate but normal homocysteine levels in patients with atherosclerotic vascular disease and matched healthy controls. Nutr 16, 434-438.
4. Collins MK, Marvel J, Malde P & Lopez-Rivas A (1992) Interleukin 3 protects murine bone marrow cells from apoptosis induced by DNA damaging agents. J Exp Med 176, 1043-1051.
5. Courtemanche C, Huang AC, Elson-Schwab I, Kerry N, Ng BY & Ames BN (2004) Folate deficiency and ionizing radiation cause DNA breaks in primary human lymphocytes: a comparison. FASEB J 18, 209-211.
6. Das SK, Kunkel TA & Loeb LA (1985) Effects of altered nucleotide concentrations on the fidelity of DNA replication. Basic Life Sci 31, 117-126.
7. Devireddy LR & Green MR (2003) Transcriptional program of apoptosis induction following interleukin 2 deprivation: identification of RC3, a calcium/calmodulin binding protein, as a novel proapoptotic factor. Mol Cell Biol 23, 4532-4541.
8. Donehower LA & Bradley A (1993) The tumor suppressor p53. Biochim Biophys Acta 1155, 181-205.
9. Duke RC & Cohen JJ (1986) IL-2 addiction: withdrawal of growth factor activates a suicide program in dependent T cells. Lymphokine Res 5, 289-299.
10. Duthie SJ & Hawdon A (1998) DNA instability (strand breakage, uracil misincorporation, and defective repair) is increased by folic acid depletion in human lymphocytes in vitro. FASEB J 12, 1491-1497.
11. Duthie SJ, Narayanan S, Brand GM, Pirie L & Grant G (2002) Impact of folate deficiency on DNA stability. J Nutr 132, S2444-S2449.
12. Fleischer A, Ayllon V, Dumoutier L, Renauld JC & Rebollo A (2002) Proapoptotic activity of ITM2B(s), a BH3-only protein induced upon IL-2-deprivation which interacts with Bcl-2. Oncogene 21, 3181-3189.
13. Fleming A & Copp AJ (1998) Embryonic folate metabolism and mouse neural tube defects. Science 280, 2107-2109.
14. Freudenheim JL, Graham S, Marshall JR, Haughey BP, Cholewinski S & Wilkinson G (1991) Folate intake and carcinogenesis of the colon and rectum. Int J Epidemiol 20, 368-374.
15. Hildeman DA, Zhu Y, Mitchell TC, Kappler J & Marrack P (2002) Molecular mechanisms of activated T cell death in vivo. Curr Opin Immunol 14, 354-359.
16. Huang RF, Ho YH, Lin HL, Wei JS & Liu TZ (1999) Folate deficiency induces a cell cycle-specific apoptosis in HepG2 cells. J Nutr 129, 25-31.
17. Ingram CF, Davidoff AN, Marais E, Sherman GG & Mendelow BV (1997) Evaluation of DNA analysis for evidence of apoptosis in megaloblastic anaemia. Br J Haematol 96, 576-583.
18. James SJ, Miller BJ, McGarrity LJ & Morris SM (1994) The effect of folic acid deficiency on deoxyribonucleotide pools and cell cycle distribution in mitogen-stimulated lymphocytes. Cell Prolif 27, 395-406.
19. James SJ, Pogribny IP, Pogribny M, Miller BJ, Jernigan S & Melnyk S (2003) Mechanisms of DNA damage, DNA hypomethylation, and tumor progression in the folate/methyl-deficient rat model of hepatocarcinogenesis. J Nutr 133, S3740-S3747.
20. Kim YI, Shirwadkar S, Choi SW, Puchyr M, Wang Y & Mason JB (2000) Effects of dietary folate on DNA strand breaks within mutation-prone exons of the p53 gene in rat colon. Gastroenterology 119, 151-161.
21. Koury MJ, Price JO & Hicks GG (2000) Apoptosis in megaloblastic anemia occurs during DNA synthesis by a p53-independent, nucleoside-reversible mechanism. Blood 96, 3249-3255.
22. Kuerbitz SJ, Plunkett BS, Walsh WV & Kastan MB (1992) Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc Nalt Acad Sci USA 89, 7491-7495.
23. Lagergren J & Reichard P (1987) Purine deoxyribonucleosides counteract effects of hydroxyurea on deoxyribonucleoside triphosphate pools and DNA synthesis. Biochem Pharmacol 36, 2985-2991.
24. Liao WT, Chang KL, Yu CL, Chen GS, Chang LW & Yu HS (2004) Arsenic induces human keratinocyte apoptosis by the Fas/Fas ligand pathway, which correlates with alterations in nuclear factor-Kb and activator protein-1 activity. J Invest Dermatol 122, 125-129.
25. Linke SP, Clarkin KC, Di Leonardo A, Tsou A & Wahl GM (1996) A reversible, p53-dependent G0/G1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10, 934-947.
26. Lowe SW, Schmitt EM, Smith SW, Osborne BA & Jacks T (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362, 847-849.
27. Maltzman W & Czyzyk L (1984) UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol Cell Biol 4, 1689-1694.
28. Mashiyama ST, Courtemanche C, Elson-Schwab I, Crott J, Lee BL, Ong CN, Fenech M & Ames BN (2004) Uracil in DNA, determined by an improved assay, is increased when deoxynucleosides are added to folate-deficient cultured human lymphocytes. Anal Biochem 330, 58-69.
29. Michalis LK, Pappas K, Tweddel A, Kolaitis N, Katsouras CS, Loukas S, Goudevenos J, Bourantas K & Sideris DA (2001) Relatively low red cell folate levels and acute coronary syndromes. Coron Artery Dis 12, 665-668.
30. Miyashita T & Reed JC (1992) bcl-2 gene transfer increases relative resistance of S49.1 and WEHI7.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorticoids and multiple chemotherapeutic drugs. Cancer Res 52, 5407-5411.
31. Miyawaki T, Uehara T, Nibu R, Tsuji T, Yachie A, Yonehara S & Taniguchi N (1992) Differential expression of apoptosis-related Fas antigen on lymphocyte subpopulations in human peripheral blood. J Immunol 149, 3753-3758.
32. Oliver FJ, Collins MK & Lopez-Rivas A (1996) Regulation of the salvage pathway of deoxynucleotides synthesis in apoptosis induced by growth factor deprivation. Biochem J 316, 421-425.
33. Oliver FJ, Collins MK & Lopez-Rivas A (1997) Overexpression of a heterologous thymidine kinase delays apoptosis induced by factor deprivation and inhibitors of deoxynucleotide metabolism. J Biol Chem 272, 10624-10630.
34. Oliver FJ, Marvel J, Collins MK & Lopez-Rivas A (1993) Bcl-2 oncogene protects a bone marrow-derived pre-B-cell line from 5′-fluor,2′-deoxyuridine-induced apoptosis. Biochem Biophys Res Commun 194, 126-132.
35. Pogribny IP, Basnakian AG, Miller BJ, Lopatina NG, Poirier LA & James SJ (1995) Breaks in genomic DNA and within the p53 gene are associated with hypomethylation in livers of folate/methyl-deficient rats. Cancer Res 55, 1894-1901.
36. Rosenberg IH & Mason JB (1989) Folate, dysplasia, and cancer. Gastroenterology 97, 502-503.
37. Shane B & Stokstad EL (1985) Vitamin B12-folate interrelationships. Annu Rev Nutr 5, 115-141.
38. Smithells RW, Sheppard S & Schorah CJ (1976) Vitamin deficiencies and neural tube defects. Arch Dis Child 51, 944-950.
39. Strasser A, Harris AW, Jacks T & Cory S (1994) DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 79, 329-339.
40. van der Weyden MB, Hayman RJ, Rose IS & Brumley J (1991) Folate-deficient human lymphoblasts: changes in deoxynucleotide metabolism and thymidylate cycle activities. Eur J Haematol 47, 109-114.
41. Wickramasinghe SN & Fida S (1994) Bone marrow cells from vitamin B12- and folate-deficient patients misincorporate uracil into DNA. Blood 83, 1656-1661.
42. Yoshioka A, Tanaka S, Hiraoka O, Koyama Y, Hirota Y, Ayusawa D, Seno T, Garrett C & Wataya Y (1987) Deoxyribonucleoside triphosphate imbalance. 5-Fluorodeoxyuridine-induced DNA double strand breaks in mouse FM3A cells and the mechanism of cell death. J Biol Chem 262, 8235-8241.
43. Yu HS, Liao WT, Chang KL, Yu CL & Chen GS (2002) Arsenic induces TNF-α release and tumor necrosis factor receptor-1 signaling in T-helper cell apoptosis. J Invest Dermatol 119, 812-819.
44. Zambetti GP & Levine AJ (1993) A comparison of the biological activities of wild-type and mutant p53. FASEB J 7, 855-865.