Glucose 6-phosphate dehydrogenase deficiency enhances germ cell apoptosis and causes defective embryogenesis in Caenorhabditis elegans

Cell Death and Disease

Volumn 4, Issue 5, 2013, Pages

  Yang, H C ^a,b   Chen, T L ^a   Wu, Y H ^a   Cheng, K P ^a   Lin, Y H ^a   Cheng, M L ^a,b   Ho, H Y ^a,b   Lo, S J ^a   Chiu, D T Y ^a,b,c  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

C. elegans; Embryogenesis; G6PD; Germ cell apoptosis; MAPK; Oxidative stress

Indexed keywords

GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA DAMAGE; EGG PRODUCTION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FAVISM; GENE SILENCING; GERM CELL; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HATCHING; INTRACELLULAR SIGNALING; LOSS OF FUNCTION MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA DAMAGE; EMBRYONIC DEVELOPMENT; GERM CELLS; GLUCOSEPHOSPHATE DEHYDROGENASE; GLUCOSEPHOSPHATE DEHYDROGENASE DEFICIENCY; HUMANS; HYDROGEN PEROXIDE; MAP KINASE KINASE 1; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; CAENORHABDITIS ELEGANS; MUS;

EID: 84879370915     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.132     Document Type: Article

References (50)

1. Salati LM, Amir-Ahmady B. Dietary regulation of expression of glucose-6-phosphate dehydrogenase. Annu Rev Nutr 2001; 21: 121-140.
2. Ho HY, Cheng ML, Chiu DT. Glucose-6-phosphate dehydrogenase-from oxidative stress to cellular functions and degenerative diseases. Redox Rep 2007; 12: 109-118.
3. Ho HY, Cheng ML, Chiu DT. G6PD-an old bottle with new wine. Chang Gung Med J 2005; 28: 606-612.
4. Beutler E. G6PD deficiency. Blood 1994; 84: 3613-3636.
5. Pantaleo A, Ferru E, Carta F, Mannu F, Simula LF, Khadjavi A et al. Irreversible AE1 tyrosine phosphorylation leads to membrane vesiculation in G6PD deficient red cells. PLoS One 2011; 6: e15847.
6. Shimo H, Nishino T, Tomita M. Predicting the kinetic properties associated with redox imbalance after oxidative crisis in G6PD-deficient erythrocytes: a simulation study. Adv Hematol 2011; 2011: 398945.
7. Arese P, De Flora A. Pathophysiology of hemolysis in glucose-6-phosphate dehydrogenase deficiency. Semin Hematol 1990; 27: 1-40.
8. Sirdah M, Reading NS, Perkins SL, Shubair M, Aboud L, Prchal JT. Hemolysis and Mediterranean G6PD mutation (c.563 C4T) and c.1311 C4T polymorphism among Palestinians at Gaza Strip. Blood Cells Mol Dis 2012; 48: 203-208.
9. Tanphaichitr VS, Hirono A, Pung-amritt P, Treesucon A, Wanachiwanawin W. Chronic nonspherocytic hemolytic anemia due to glucose-6-phosphate dehydrogenase deficiency: report of two families with novel mutations causing G6PD Bangkok and G6PD Bangkok Noi. Ann Hematol 2011; 90: 769-775.
10. Ho HY, Cheng ML, Lu FJ, Chou YH, Stern A, Liang CM et al. Enhanced oxidative stress and accelerated cellular senescence in glucose-6-phosphate dehydrogenase (G6PD)-deficient human fibroblasts. Free Radic Biol Med 2000; 29: 156-169.
11. Cheng ML, Ho HY, Wu YH, Chiu DT. Glucose-6-phosphate dehydrogenase- deficient cells show an increased propensity for oxidant-induced senescence. Free Radic Biol Med 2004; 36: 580-591.
12. Gao LP, Cheng ML, Chou HJ, Yang YH, Ho HY, Chiu DT. Ineffective GSH regeneration enhances G6PD-knockdown Hep G2 cell sensitivity to diamide-induced oxidative damage. Free Radic Biol Med 2009; 47: 529-535.
13. Lin CJ, Ho HY, Cheng ML, You TH, Yu JS, Chiu DT. Impaired dephosphorylation renders G6PD-knockdown HepG2 cells more susceptible to H(2)O(2)-induced apoptosis. Free Radic Biol Med 2010; 49: 361-373.
14. Tsai KJ, Hung IJ, Chow CK, Stern A, Chao SS, Chiu DT. Impaired production of nitric oxide, superoxide, and hydrogen peroxide in glucose 6-phosphate-dehydrogenase-deficient granulocytes. FEBS Lett 1998; 436: 411-414.
15. Ho HY, Cheng ML, Weng SF, Chang L, Yeh TT, Shih SR et al. Glucose-6-phosphate dehydrogenase deficiency enhances enterovirus 71 infection. J Gen Virol 2008; 89(Pt 9): 2080-2089.
16. Wu YH, Tseng CP, Cheng ML, Ho HY, Shih SR, Chiu DT. Glucose-6-phosphate dehydrogenase deficiency enhances human coronavirus 229E infection. J Infect Dis 2008; 197: 812-816.
17. Johnson FB, Sinclair DA, Guarente L. Molecular biology of aging. Cell 1999; 96: 291-302.
18. Yamada T, Egashira N, Bando A, Nishime Y, Tonogai Y, Imuta M et al. Activation of p38 MAPK by oxidative stress underlying epirubicin-induced vascular endothelial cell injury. Free Radic Biol Med 2012; 52: 1285-1293.
19. C. elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998; 282: 2012-2018.
20. Jorgensen EM, Mango SE. The art and design of genetic screens: caenorhabditis elegans. Nat Rev Genet 2002; 3: 356-369.
21. Antoshechkin I, Sternberg PW. The versatile worm: genetic and genomic resources for Caenorhabditis elegans research. Nat Rev Genet 2007; 8: 518-532.
22. Ankeny RA. The natural history of Caenorhabditis elegans research. Nat Rev Genet 2001; 2: 474-479.
23. Filosa S, Fico A, Paglialunga F, Balestrieri M, Crooke A, Verde P et al. Failure to increase glucose consumption through the pentose-phosphate pathway results in the death of glucose-6-phosphate dehydrogenase gene-deleted mouse embryonic stem cells subjected to oxidative stress. Biochem J 2003; 370(Pt 3): 935-943.
24. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003; 421: 231-237.
25. Zhou Z, Hartwieg E, Horvitz HR. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 2001; 104: 43-56.
26. Calafato S, Swain S, Hughes S, Kille P, Sturzenbaum SR. Knock down of Caenorhabditis elegans cutc-1 exacerbates the sensitivity toward high levels of copper. Toxicol Sci 2008; 106: 384-391.
27. Wu Q, He K, Liu P, Li Y, Wang D. Association of oxidative stress with the formation of reproductive toxicity from mercury exposure on hermaphrodite nematode Caenorhabditis elegans. Environ Toxicol Pharmacol 2011; 32: 175-184.
28. Kumsta C, Thamsen M, Jakob U. Effects of oxidative stress on behavior, physiology, and the redox thiol proteome of Caenorhabditis elegans. Antioxid Redox Signal 2011; 14: 1023-1037.
29. Fraenkel DG, Vinopal RT. Carbohydrate metabolism in bacteria. Annu Rev Microbiol 1973; 27: 69-100.
30. Thomas D, Cherest H, Surdin-Kerjan Y. Identification of the structural gene for glucose-6-phosphate dehydrogenase in yeast. Inactivation leads to a nutritional requirement for organic sulfur. EMBO J 1991; 10: 547-553.
31. Hecker PA, Lionetti V, Ribeiro RF Jr., Rastogi S, Brown BH, O'Connell KA et al. Glucose 6-phosphate dehydrogenase deficiency increases redox stress and moderately accelerates the development of heart failure. Circ Heart Fail 2013; 6: 118-126.
32. Longo L, Vanegas OC, Patel M, Rosti V, Li H, Waka J et al. Maternally transmitted severe glucose 6-phosphate dehydrogenase deficiency is an embryonic lethal. EMBO J 2002; 21: 4229-4239.
33. Salinas LS, Maldonado E, Navarro RE. Stress-induced germ cell apoptosis by a p53 independent pathway in Caenorhabditis elegans. Cell Death Differ 2006; 13: 2129-2139.
34. Berger RG, Lunkenbein S, Strohle A, Hahn A. Antioxidants in food: mere myth or magic medicine? Crit Rev Food Sci Nutr 2012; 52: 162-171.
35. Gartner A, Boag PR, Blackwell TK. Germline survival and apoptosis. WormBook 2008 1-20.
36. Wang S, Wu L, Wang Y, Luo X, Lu Y. Copper-induced germline apoptosis in Caenorhabditis elegans: the independent roles of DNA damage response signaling and the dependent roles of MAPK cascades. Chem Biol Interact 2009; 180: 151-157.
37. Koga M, Zwaal R, Guan KL, Avery L, Ohshima Y. A Caenorhabditis elegans MAP kinase kinase, MEK-1, is involved in stress responses. EMBO J 2000; 19: 5148-5156.
38. Sekhar KR, Crooks PA, Sonar VN, Friedman DB, Chan JY, Meredith MJ et al. NADPH oxidase activity is essential for Keap1/Nrf2-mediated induction of GCLC in response to 2-indol-3-yl-methylenequinuclidin-3-ols. Cancer Res 2003; 63: 5636-5645.
39. Gan Q, Li T, Hu B, Lian M, Zheng X. HSCARG inhibits activation of NF-kappaB by interacting with IkappaB kinase-beta. J Cell Sci 2009; 122(Pt 22): 4081-4088.
40. Zhang M, Hu B, Li T, Peng Y, Guan J, Lai S et al. A CRM1-dependent nuclear export signal controls nucleocytoplasmic translocation of HSCARG, which regulates NF-kappaB activity. Traffic 2012; 13: 790-799.
41. Wong JL, Creton R, Wessel GM. The oxidative burst at fertilization is dependent upon activation of the dual oxidase Udx1. Dev Cell 2004; 7: 801-814.
42. Wong JL, Wessel GM. Reactive oxygen species and Udx1 during early sea urchin development. Dev Biol 2005; 288: 317-333.
43. Wong JL, Wessel GM. Free-radical crosslinking of specific proteins alters the function of the egg extracellular matrix at fertilization. Development 2008; 135: 431-440.
44. Morey M, Serras F, Baguna J, Hafen E, Corominas M. Modulation of the Ras/MAPK signalling pathway by the redox function of selenoproteins in Drosophila melanogaster. Dev Biol 2001; 238: 145-156.
45. Madan P, Calder MD, Watson AJ. Mitogen-activated protein kinase (MAPK) blockade of bovine preimplantation embryogenesis requires inhibition of both p38 and extracellular signal-regulated kinase (ERK) pathways. Reproduction 2005; 130: 41-51.
46. Yang HC, Cheng ML, Ho HY, Chiu DT. The microbicidal and cytoregulatory roles of NADPH oxidases. Microbes Infect 2011; 13: 109-120.
47. Spilker AC, Rabilotta A, Zbinden C, Labbe JC, Gotta M. MAP kinase signaling antagonizes PAR-1 function during polarization of the early Caenorhabditis elegans embryo. Genetics 2009; 183: 965-977.
48. Sambrook J, Russell DW. Molecular Cloning, A Laboratory Manual. 3rd edn, Cold Spring Harbor Laboratory: New York, 2001.
49. Skaletsky SRaHJ. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press: Totowa, NJ, 2000. pp 365-386.
50. Liao VH, Yu CW, Chu YJ, Li WH, Hsieh YC, Wang TT. Curcumin-mediated lifespan extension in Caenorhabditis elegans. Mech Ageing Dev 2011; 132: 480-487.