Differential programming of p53-deficient embryonic cells during rotenone block

Toxicology

Volumn 290, Issue 1, 2011, Pages 31-41

  Green, M L ^a   Singh, A V ^a,b   Ruest, L B ^c   Pisano, M M ^a   Prough, R A ^a   Knudsen, T B ^a,d  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b SYNGENTA BIOTECHNOLOGY INC   (United States)

^c BAYLOR COLLEGE OF DENTISTRY   (United States)

^d U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Embryo; MEF; MiRNA; Mitochondria; Mouse; P53; Rotenone

Indexed keywords

MESSENGER RNA; MICRORNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; TUBULIN;

ANIMAL CELL; ARTICLE; CELL LINE; CELL STRESS; CONTROLLED STUDY; CYTOSKELETON; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EMBRYO; EMBRYO CELL; EMBRYONIC STEM CELL; FIBROBLAST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL SURVIVAL; EMBRYO, MAMMALIAN; GENE REGULATORY NETWORKS; MICE; MICE, KNOCKOUT; MICRORNAS; NIH 3T3 CELLS; RNA, MESSENGER; ROTENONE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 80053640856     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2011.08.013     Document Type: Article

References (53)

1. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
2. Bommer G.T., Gerin I., Feng Y., Kaczorowski A.J., Kuick R., et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 2007, 17:1298-1307.
3. Bowman T., Symonds H., Gu L., Yin C., Oren M., Van Dyke T. Tissue- specific inactivation of p53 tumor suppression in the mouse. Genes Dev. 1996, 10(7):826-835.
4. Brinkley B., Barham S., Barranco S., et al. Rotenone inhibition of spindle microtubule assembly in mammalian cells. Exp. Cell Res. 1974, 85(1):41-46.
5. Chance B., Williams G.R., Hollunger G. Inhibition of electron and energy transfer in mitochondria, I. Effects of Amytal, thiopental, rotenone, progesterone, and methylene glycol. J. Biol. Chem. 1963, 238:418-431.
6. Chang T.C., Wentzel E.A., Kent O.A., Ramachandran K., Mullendore M., et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 2007, 26:745-752.
7. Compton S., Kim C., Griner N.B., et al. Mitochondrial dysfunction impairs tumor suppressor p53 expression/function. J. Biol. Chem. 2011, 286(23):20297-20312.
8. DiMauro S., Hirano M. Mitochondrial encephalomyopathies: an update. Neuromusc. Disord. 2005, 15:276-286.
9. Donahue R., Razmara M., Hoek J., et al. Direct influence of the p53 tumor suppressor on mitochondrial biogenesis and function. FASEB 2001, 15:635-644.
10. el-Deiry W.S., Kern S.E., Pietenpol J.A., et al. Definition of a consensus binding site for p53. Nat. Genet. 1992, 1:45-49.
11. Fantin V., St-Pierre J., Leder P Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006, 9:425-434.
12. Gong X., Kole L., Iskander K., Jaiswal A.K. NRH:quinone oxidoreductase 2 and NAD(P)H:quinone oxidoreductase 1 protect tumor suppressor p53 against 20s proteasomal degradation leading to stabilization and activation of p53. Cancer Res. 2007, 67(11):5380-5388.
13. Harper J., Adami G., Wei N., et al. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 1993, 75:805-816.
14. He L., He X., Lim L.P., de Stanchina E., Xuan Z., et al. A microRNA component of the p53 tumour suppressor network. Nature 2007, 447:1130-1134.
15. Heinen A., Aldakkak M., Stowe D., et al. Reverse electron flow-induced ROS production is attenuated by activation of mitochondrial Ca2+-sensitive K+ channels. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H1400-H1407.
16. Hornstein E., Shomron N. Canalization of development by microRNAs. Nat. Gen. 2006, 38:S20-S24.
17. Ibrahim M., Razmara M., Nguyen D., et al. Altered expression of mitochondrial 16S ribosomal RNA in p53-deficient mouse embryos revealed by differential display. Biochem. Biophys. Acta 1998, 1403:254-264.
18. Jin S., Levine A.J. The p53 functional circuit. J. Cell Sci. 2001, 114:4139-4140.
19. Khutornenko A.A., Roudko V.V., Chernyak B.V., et al. Pyrimidine biosynthesis links mitochondrial respiration to the p53 pathway. Proc. Natl. Acad. Sci. 2010, 107(29):12828-12833.
20. Kulawiec M., Safina A., Desouki M., et al. Tumorigenic transformation of human breast epithelial cells induced by mitochondrial DNA depletion. Cancer Biol. Ther. 2008, 7(11):1732-1743.
21. Lebedeva M.A., Eaton J.S., Shadel G.S. Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis. Biochim. Biophys. Acta 2009, 1787(5):328-334.
22. Lee J., Kemper J.K. Controlling SIRT1 expression by microRNAs in health and metabolic disease. Aging 2010, 2(8):527-534.
23. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J., Robinson J. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 2003, 278:8516-8525.
24. Li X., Cassidy J.J., Reinke C.A., Fischboeck S., Carthew RW A microRNA imparts robustness against environmental fluctuation during development. Cell 2009, 137:273-282.
25. Lim L.P., Glasner M.E., Yekta S. Vertebrate microRNA genes. Science 2003, 299(5612):1540.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25(4):402-408.
27. Ma W., Sung H.J., Park J.Y., et al. A pivotal role for p53: balancing aerobic respiration and glycolysis. J. Bioenerg. Biomembr. 2007, 39(3):243-246.
28. MacKenzie E.L., Ray P.D., Tsuji Y. Role and regulation of ferritin H in rotenone-mediated mitochondrial oxidative stress. Free Radic. Biol. Med. 2008, 44(9):1762-1771.
29. Matoba S., Kang J., Patino W., et al. p53 Regulates mitochondrial respiration. Science 2006, 312(16):1650-1653.
30. Meister B., Tuschi T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431:343-349.
31. Park J.Y., Wang P.Y., Matsumoto T., et al. P53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ. Res. 2009, 105(7):705-712.
32. Raver-Shapira N., Marciano E., Meiri E., Spector Y., Rosenfeld N., et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 2007, 26:731-743.
33. Ravi R., Mookerjee B., van Hensbergen Y., et al. p53-mediated repression of nuclear factor-kappaB RelA via the transcriptional integrator p300. Cancer Res. 1998, 58(20):4531-4536.
34. Ren Y., Jiang H., Yang F., et al. Parkin protects dopaminergic neurons against microtubule-depolymerizing toxins by attenuating microtubule-associated protein kinase activation. J. Biol. Chem. 2009, 284(6):4009-4017.
35. Rhodes D.R., Chinnaiyan A.M. Integrative analysis of the cancer transcriptome. Nat. Genet. 2005, 37(Suppl.):S31-S37. (Review).
36. Richter-Landsberg C. Organization and functional roles of the cytoskeleton in oligodendrocytes. Microsc. Res. Technol. 2001, 53:628-636.
37. Ricquier D. Respiration uncoupling and metabolism in the control of energy expenditure. Proc. Nutr. Soc. 2005, 64:47-52.
38. Rouslin W., Broge C.W., Grupp I.L. ATP epletion and mitochondrial functional loss during ischemia in slow and fast heart-rate hearts. Am. J. Physiol. 1990, 259(6 Pt 2):H1759-H1766.
39. Rossomando A.J., Payne D.M., Weber M.J., Sturgill T.W. Evidence that pp42, a major tyrosine kinase target protein, is a mitogen-activated serine/threonine protein kinase. Proc. Natl. Acad. Sci. 1989, 86:6940-6943.
40. Sah V., Attardi L., Mulligan G., et al. A subset of p53-deficeint embryos exhibit exencephaly. Nat. Genet. 1995, 2:175-180.
41. Saunders L.R., Sharma A.D., Tawney J., et al. miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues. Aging 2011, 2(7):415-431.
42. Srivastava P., Panda D. Rotenone inhibits mammalian cell proliferation by inhibiting microtubule assembly through tubulin binding. FEBS J. 2007, 274(18):4788-4801.
43. Tarantino C., Paolella G., Cozzuto L., et al. miRNA 34a, 100, and 137 modulate differentiation of mouse embryonic stem cells. FASEB J. 2010, 24(9):3255-3263.
44. Tarasov V., Jung P., Verdoodt B., Lodygin D., Epanchintsev A., et al. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007, 6:1586-1593.
45. Trifunovic A., Hansson A., Wredenberg A., et al. Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. PNAS 2005, 102(50):17993-17998.
46. Vousden K.H., Lane D.P. p53 in health and disease. Nat. Rev. 2007, 8:275-283.
47. Wagner B., Kitami T., Gilbert T., et al. Large-scale chemical dissection of mitochondrial function. Nat. Biotechnol. 2008, 26(3):343-351.
48. Wong T., Rajagopalan S., Townsley F., et al. Physical and functional interactions between human mitochondrial single-stranded DNA binding protein and tumour suppressor p53. Nucl. Acid Res. 2009, 37(2):568-581.
49. Wubah J., Ibrahim M., Gao X., et al. Teratogen-induced eye defects mediated by p53-dependent apoptosis. Curr. Biol. 1996, 6(1):60-69.
50. Yamakuchi M., Lowenstein C.J. MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle 2009, 8(5):712-715.
51. Yang F., Jiang Q., Zhao J., et al. Parkin stabilizes microtubules through strong binding mediated by three independent domains. J. Biol. Chem. 2005, 280:17154-17162.
52. Yang D., Wang M.T., Tang Y., et al. Impairment of mitochondrial respiration in mouse fibroblasts by oncogenic H-RAS(Q61L). Cancer Biol. Ther. 2010, 9(2):122-133.
53. Yoshida Y., Izumi H., Torigoe T., et al. p53 physically interacts with mitochondrial transcription factor A and differentially regulates binding to damaged DNA. Cancer Res. 2003, 63:3729-3734.