Impaired manganese metabolism causes mitotic misregulation

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18717-18729

  García Rodríguez, Néstor ^a   Díaz De La Loza, María Del Carmen ^a   Andreson, Bethany ^b   Monje Casas, Fernando ^a   Rothstein, Rodney ^c   Wellinger, Ralf Erik ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; MANGANESE; METABOLISM; TRACE ELEMENTS;

CELL CYCLE; CELL CYCLE REGULATORS; CELL-CYCLE PROGRESSION; FUNCTIONAL MORPHOLOGY; GENOMIC INSTABILITY; INTRACELLULAR LEVELS; METABOLIC FUNCTION; UP-REGULATION;

CELLS;

DNA; MANGANESE; MESSENGER RNA;

ARTICLE; ATP2C1 GENE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL POLARITY; CONTROLLED STUDY; DEPLETION; DISEASE ASSOCIATION; DNA SYNTHESIS; FUNCTIONAL MORPHOLOGY; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REPLICATION; GENETIC ASSOCIATION; GENOMIC INSTABILITY; HAILEY HAILEY DISEASE; HOMEOSTASIS; M PHASE CELL CYCLE CHECKPOINT; METAL METABOLISM; MITOSIS; NONHUMAN; PMR1 GENE; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; S PHASE CELL CYCLE CHECKPOINT; TRANSCRIPTION REGULATION; UPREGULATION;

EID: 84861534006     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.358309     Document Type: Article

References (71)

1. Keen, C. L., Ensunsa, J. L., and Clegg, M. S. (2000) Manganese metabolism in animals and humans including the toxicity of manganese. Met. Ions. Biol. Syst 37, 89-121
2. Crowley, J. D., Traynor, D. A., and Weatherburn, D. C. (2000) Enzymes and proteins containing manganese: an overview. Met. Ions. Biol. Syst 37, 209-278
3. Couper, J. (1837) On the effects of black oxide of manganese when inhaled into the lungs. Br. Ann. Med. Pharmacol. 1, 41-42
4. Lucchini, R. G., Martin, C. J., and Doney, B. C. (2009) From manganism to manganese-induced parkinsonism: a conceptual model based on the evolution of exposure. Neuromol. Med. 11, 311-321
5. Rudolph, H. K., Antebi, A., Fink, G. R., Buckley, C. M., Dorman, T. E., LeVitre, J., Davidow, L. S., Mao, J. I., and Moir, D. T. (1989) The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family. Cell 58, 133-145 (Pubitemid 19180086)
6. Antebi, A., and Fink, G. R. (1992) The yeast Ca(2+)-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell 3, 633-654 (Pubitemid 23098263)
7. Lapinskas, P. J., Cunningham, K. W., Liu, X. F., Fink, G. R., and Culotta, V. C. (1995) Mutations in PMR1 suppress oxidative damage in yeast cells lacking superoxide dismutase. Mol. Cell Biol. 15, 1382-1388
8. Hu, Z., Bonifas, J. M., Beech, J., Bench, G., Shigihara, T., Ogawa, H., Ikeda, S., Mauro, T., and Epstein, E. H., Jr. (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat. Genet. 24, 61-65 (Pubitemid 30041422)
9. Wei, Y., Marchi, V., Wang, R., and Rao, R. (1999) An N-terminal EF handlike motif modulates ion transport by Pmr1, the yeast Golgi Ca(2+)/Mn(2+)-ATPase. Biochemistry 38, 14534-14541
10. Mandal, D., Woolf, T. B., and Rao, R. (2000) Manganese selectivity of pmr1, the yeast secretory pathway ion pump, is defined by residue gln783 in transmembrane segment 6. Residue Asp778 is essential for cation transport. J. Biol. Chem. 275, 23933-23938 (Pubitemid 30624682)
11. Dürr, G., Strayle, J., Plemper, R., Elbs, S., Klee, S. K., Catty, P., Wolf, D. H., and Rudolph, H. K. (1998) The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol. Biol. Cell 9, 1149-1162 (Pubitemid 28457306)
12. Bolton, E. C., Mildvan, A. S., and Boeke, J. D. (2002) Inhibition of reverse transcription in vivo by elevated manganese ion concentration. Mol. Cell 9, 879-889 (Pubitemid 34454897)
13. Lue, N. F., Bosoy, D., Moriarty, T. J., Autexier, C., Altman, B., and Leng, S. (2005) Telomerase can act as a template- and RNA-independent terminal transferase. Proc. Natl. Acad. Sci. U.S.A. 102, 9778-9783 (Pubitemid 40993645)
14. 2+-ATPase, is a regulator of the target of rapamycin (TOR) signaling pathway in yeast. Proc. Natl. Acad. Sci. U.S.A. 103, 17840-17845
15. Mendenhall, M. D., and Hodge, A. E. (1998) Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62, 1191-1243 (Pubitemid 28558297)
16. Bloom, J., and Cross, F. R. (2007) Multiple levels of cyclin specificity in cell-cycle control. Nat. Rev. Mol. Cell Biol. 8, 149-160 (Pubitemid 46432532)
17. Booher, R. N., Deshaies, R. J., and Kirschner, M. W. (1993) Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J. 12, 3417-3426 (Pubitemid 23256429)
18. Hu, F., and Aparicio, O. M. (2005) Swe1 regulation and transcriptional control restrict the activity of mitotic cyclins toward replication proteins in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 102, 8910-8915 (Pubitemid 40881052)
19. Lew, D. J., and Reed, S. I. (1995) A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J. Cell Biol. 129, 739-749
20. McNulty, J. J., and Lew, D. J. (2005) Swe1p responds to cytoskeletal perturbation, not bud size, in S. cerevisiae. Curr. Biol. 15, 2190-2198 (Pubitemid 41790612)
21. Harvey, S. L., and Kellogg, D. R. (2003) Conservation of mechanisms controlling entry into mitosis: budding yeast wee1 delays entry into mitosis and is required for cell size control. Curr. Biol. 13, 264-275 (Pubitemid 36230017)
22. Loukin, S., and Kung, C. (1995) Manganese effectively supports yeast cellcycle progression in place of calcium. J. Cell Biol. 131, 1025-1037
23. 2+ regulation in Saccharomyces cerevisiae. Genetics 148, 1777-1786
24. Losev, E., Papanikou, E., Rossanese, O. W., and Glick, B. S. (2008) Cdc1p is an endoplasmic reticulum-localized putative lipid phosphatase that affects Golgi inheritance and actin polarization by activating Ca2+ signaling. Mol. Cell Biol. 28, 3336-3343 (Pubitemid 351657097)
25. Zewail, A., Xie, M. W., Xing, Y., Lin, L., Zhang, P. F., Zou, W., Saxe, J. P., and Huang, J. (2003) Novel functions of the phosphatidylinositol metabolic pathway discovered by a chemical genomics screen with wortmannin. Proc. Natl. Acad. Sci. U.S.A. 100, 3345-3350 (Pubitemid 36356586)
26. Pan, X., Ye, P., Yuan, D. S., Wang, X., Bader, J. S., and Boeke, J. D. (2006) A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124, 1069-1081 (Pubitemid 43344244)
27. Suter, B., Tong, A., Chang, M., Yu, L., Brown, G. W., Boone, C., and Rine, J. (2004) The origin recognition complex links replication, sister chromatid cohesion and transcriptional silencing in Saccharomyces cerevisiae. Genetics 167, 579-591 (Pubitemid 38931849)
28. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 (Pubitemid 28328001)
29. Storici, F., and Resnick, M. A. (2006) The delitto perfetto approach to in vivo site-directed mutagenesis and chromosome rearrangements with synthetic oligonucleotides in yeast. Methods Enzymol. 409, 329-345
30. Wellinger, R. E., Schär, P., and Sogo, J. M. (2003) Rad52-independent accumulation of joint circular minichromosomes during S phase in Saccharomyces cerevisiae. Mol. Cell Biol. 23, 6363-6372 (Pubitemid 37075750)
31. Foiani, M., Marini, F., Gamba, D., Lucchini, G., and Plevani, P. (1994) The B subunit of the DNA polymerase α-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol. Cell Biol. 14, 923-933 (Pubitemid 24036542)
32. Pellicioli, A., Lucca, C., Liberi, G., Marini, F., Lopes, M., Plevani, P., Romano, A., Di Fiore, P. P., and Foiani, M. (1999) Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18, 6561-6572 (Pubitemid 29533260)
33. Yuen, K. W., Warren, C. D., Chen, O., Kwok, T., Hieter, P., and Spencer, F. A. (2007) Systematic genome instability screens in yeast and their potential relevance to cancer. Proc. Natl. Acad. Sci. U.S.A. 104, 3925-3930 (Pubitemid 47181555)
34. Valerio-Santiago, M., and Monje-Casas, F. (2011) Tem1 localization to the spindle pole bodies is essential for mitotic exit and impairs spindle checkpoint function. J. Cell Biol. 192, 599-614
35. Monje-Casas, F., and Amon, A. (2009) Cell polarity determinants establish asymmetry in MEN signaling. Dev. Cell 16, 132-145
36. Pringle, J. R. (1991) Staining of bud scars and other cell wall chitin with calcofluor. Methods Enzymol. 194, 732-735
37. Cope, M. J., Yang, S., Shang, C., and Drubin, D. G. (1999) Novel protein kinases Ark1p and Prk1p associate with and regulate the cortical actin cytoskeleton in budding yeast. J. Cell Biol. 144, 1203-1218 (Pubitemid 29157299)
38. Lippincott, J., and Li, R. (1998) Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J. Cell Biol. 143, 1947-1960 (Pubitemid 29022615)
39. Santocanale, C., and Diffley, J. F. (1998) A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395, 615-618 (Pubitemid 28475717)
40. Pittman, J. K., Cheng, N. H., Shigaki, T., Kunta, M., and Hirschi, K. D. (2004) Functional dependence on calcineurin by variants of the Saccharomyces cerevisiae vacuolar Ca2+/H+ exchanger Vcx1p. Mol. Microbiol. 54, 1104-1116 (Pubitemid 39491041)
41. Lin, S. J., and Culotta, V. C. (1996) Suppression of oxidative damage by Saccharomyces cerevisiae ATX2, which encodes a manganese-trafficking protein that localizes to Golgi-like vesicles. Mol. Cell Biol. 16, 6303-6312
42. Reddi, A. R., Jensen, L. T., Naranuntarat, A., Rosenfeld, L., Leung, E., Shah, R., and Culotta, V. C. (2009) The overlapping roles of manganese and Cu/Zn SOD in oxidative stress protection. Free Radical Biology Medicine 46, 154-162
43. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi- Falconi, M., Newlon, C. S., and Foiani, M. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412, 557-561 (Pubitemid 32743836)
44. Schwob, E., and Nasmyth, K. (1993) CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 7, 1160-1175 (Pubitemid 23207408)
45. Donaldson, A. D., Raghuraman, M. K., Friedman, K. L., Cross, F. R., Brewer, B. J., and Fangman, W. L. (1998) CLB5-dependent activation of late replication origins in S. cerevisiae. Mol. Cell 2, 173-182 (Pubitemid 128373643)
46. Lisby, M., Rothstein, R., and Mortensen, U. H. (2001) Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. U.S.A. 98, 8276-8282 (Pubitemid 32678024)
47. Zou, J., Friesen, H., Larson, J., Huang, D., Cox, M., Tatchell, K., and Andrews, B. (2009) Regulation of cell polarity through phosphorylation of Bni4 by Pho85 G1 cyclin-dependent kinases in Saccharomyces cerevisiae. Mol. Biol. Cell 20, 3239-3250
48. Desany, B. A., Alcasabas, A. A., Bachant, J. B., and Elledge, S. J. (1998) Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12, 2956-2970 (Pubitemid 28440153)
49. Lew, D. J. (2000) Cell-cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiae. Curr. Opin. Genet. Dev. 10, 47-53
50. Bartholomew, C. R., Woo, S. H., Chung, Y. S., Jones, C., and Hardy, C. F. (2001) Cdc5 interacts with the Wee1 kinase in budding yeast. Mol. Cell Biol. 21, 4949-4959 (Pubitemid 32656393)
51. Jordan, P. W., Klein, F., and Leach, D. R. (2007) Novel roles for selected genes in meiotic DNA processing. PLoS Genetics 3, e222
52. Rice, L. M., Plakas, C., and Nickels, J. T., Jr. (2005) Loss of meiotic rereplication block in Saccharomyces cerevisiae cells defective in Cdc28p regulation. Eukaryot. Cell 4, 55-62 (Pubitemid 40234422)
53. Rayner, J. C., and Munro, S. (1998) Identification of theMNN2andMNN5 mannosyltransferases required for forming and extending the mannose branches of the outer chain mannans of Saccharomyces cerevisiae. J. Biol. Chem. 273, 26836-26843 (Pubitemid 28471701)
54. Wiggins, C. A., and Munro, S. (1998) Activity of the yeast MNN1 α-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc. Natl. Acad. Sci. U.S.A. 95, 7945-7950 (Pubitemid 28326046)
55. Kaufman, R. J., Swaroop, M., and Murtha-Riel, P. (1994) Depletion of manganese within the secretory pathway inhibits O-linked glycosylation in mammalian cells. Biochemistry 33, 9813-9819 (Pubitemid 24286053)
56. Mondésert, G., and Reed, S. I. (1996) BED1, a gene encoding a galactosyl-transferase homologue, is required for polarized growth and efficient bud emergence in Saccharomyces cerevisiae. J. Cell Biol. 132, 137-151 (Pubitemid 26035081)
57. Mondésert, G., Clarke, D. J., and Reed, S. I. (1997) Identification of genes controlling growth polarity in the budding yeast Saccharomyces cerevisiae: a possible role ofN-glycosylation and involvement of the exocyst complex. Genetics 147, 421-434 (Pubitemid 27418556)
58. Sia, R. A., Herald, H. A., and Lew, D. J. (1996) Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol. Biol. Cell 7, 1657-1666 (Pubitemid 26386720)
59. Ringvoll, J., Uldal, L., Roed, M. A., Reite, K., Baynton, K., Klungland, A., and Eide, L. (2007) Mutations in the RAD27 and SGS1 genes differentially affect the chronological and replicative lifespan of yeast cells growing on glucose and glycerol. FEMS Yeast Res. 7, 848-859 (Pubitemid 47256360)
60. Beckman, R. A., Mildvan, A. S., and Loeb, L. A. (1985) On the fidelity of DNA replication: manganese mutagenesis in vitro. Biochemistry 24, 5810-5817 (Pubitemid 16203019)
61. 2+ ion pump is a factor in the emergence of viral RNA recombinants. Cell Host Microbe 7, 74-81
62. García, R., Bermejo, C., Grau, C., Pérez, R., Rodríguez-Peña, J. M., Francois, J., Nombela, C., and Arroyo, J. (2004) The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J. Biol. Chem. 279, 15183-15195 (Pubitemid 38618914)
63. Yaakov, G., Duch, A., García-Rubio, M., Clotet, J., Jimenez, J., Aguilera, A., and Posas, F. (2009) The stress-activated protein kinase Hog1 mediates S phase delay in response to osmostress. Mol. Biol. Cell 20, 3572-3582
64. Clotet, J., Escoté, X., Adrover, M. A., Yaakov, G., Garí, E., Aldea, M., de Nadal, E., and Posas, F. (2006) Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity. EMBO J. 25, 2338-2346 (Pubitemid 44012217)
65. Poletto, N. P., Henriques, J. A., and Bonatto, D. (2010) Relationship between endoplasmic reticulum- and Golgi-associated calcium homeostasis and 4-NQO-induced DNA repair in Saccharomyces cerevisiae. Arch Microbiol. 192, 247-257
66. Zhou, Z., and Elledge, S. J. (1993) DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 75, 1119-1127 (Pubitemid 24006108)
67. Lew, D. J., and Reed, S. I. (1995) Cell cycle control of morphogenesis in budding yeast. Curr. Opin. Genet. Dev. 5, 17-23
68. Kozminski, K. G., Beven, L., Angerman, E., Tong, A. H., Boone, C., and Park, H. O. (2003) Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. Mol. Biol. Cell 14, 4958-4970 (Pubitemid 37484810)
69. Ton, V. K., Mandal, D., Vahadji, C., and Rao, R. (2002) Functional expression in yeast of the human secretory pathway Ca(2+), Mn(2+)-ATPase defective in Hailey-Hailey disease. J. Biol. Chem. 277, 6422-6427 (Pubitemid 34968437)
70. Mohr, M. R., Erdag, G., Shada, A. L., Williams, M. E., Slingluff, C. L., Jr., and Patterson, J. W. (2011) Two patients with Hailey-Hailey disease, multiple primary melanomas, and other cancers. Arch. Dermatol. 147, 211-215
71. Okunade, G. W., Miller, M. L., Azhar, M., Andringa, A., Sanford, L. P., Doetschman, T., Prasad, V., and Shull, G. E. (2007) Loss of the Atp2c1 secretory pathway Ca(2+)-ATPase (SPCA1) in mice causes Golgi stress, apoptosis, and midgestational death in homozygous embryos and squamous cell tumors in adult heterozygotes. J. Biol. Chem. 282, 26517-26527 (Pubitemid 47443792)