Circadian activation of the mitogen-activated protein kinase MAK-1 facilitates rhythms in clock-controlled genes in Neurospora crassa

Eukaryotic Cell

Volumn 12, Issue 1, 2013, Pages 59-69

  Bennett, Lindsay D ^a   Beremand, Phillip ^a   Thomas, Terry L ^a   Bell Pedersen, Deborah ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CHITIN SYNTHASE; FUNGAL PROTEIN; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTOME;

ARTICLE; CIRCADIAN RHYTHM; DNA MICROARRAY; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NEUROSPORA CRASSA; PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

CELL CYCLE PROTEINS; CHITIN SYNTHASE; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; ENZYME ACTIVATION; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; MAP KINASE SIGNALING SYSTEM; MITOCHONDRIAL PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; NEUROSPORA CRASSA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTOME;

FUNGI; MAMMALIA; NEUROSPORA; NEUROSPORA CRASSA; SACCHAROMYCES CEREVISIAE;

EID: 84871998593     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00207-12     Document Type: Article

References (74)

1. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ. 2005. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 6:544-556.
2. Brunner M, Schafmeier T. 2006. Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora. Genes Dev. 20:1061-1074.
3. Kalsbeek A, Yi CX, Cailotto C, la Fleur SE, Fliers E, Buijs RM. 2011. Mammalian clock output mechanisms. Essays Biochem. 49:137-151.
4. McClung CR, Gutierrez RA. 2010. Network news: prime time for systems biology of the plant circadian clock. Curr. Opin. Genet. Dev. 20:588-598.
5. Smith KM, Sancar G, Dekhang R, Sullivan CM, Li S, Tag AG, Sancar C, Bredeweg EL, Priest HD, McCormick RF, Thomas TL, Carrington JC, Stajich JE, Bell-Pedersen D, Brunner M, Freitag M. 2010. Transcription factors in light and circadian clock signaling networks revealed by genomewide mapping of direct targets for Neurospora White Collar Complex. Eukaryot. Cell 9:1549-1556.
6. Vitalini MW, de Paula RM, Park WD, Bell-Pedersen D. 2006. The rhythms of life: circadian output pathways in Neurospora. J. Biol. Rhythms 21:432-444.
7. Baker CL, Loros JJ, Dunlap JC. 2012. The circadian clock of Neurospora crassa. FEMS Microbiol. Rev. 36:95-110.
8. Lakin-Thomas PL, Bell-Pedersen D, Brody S. 2011. The genetics of circadian rhythms in Neurospora. Adv. Genet. 74:55-103.
9. Froehlich AC, Liu Y, Loros JJ, Dunlap JC. 2002. White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297:815-819.
10. Froehlich AC, Loros JJ, Dunlap JC. 2003. Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc. Natl. Acad. Sci. U. S. A. 100:5914-5919.
11. Guo J, Cheng P, Liu Y. 2010. Functional significance of FRH in regulating the phosphorylation and stability of Neurospora circadian clock protein FRQ. J. Biol. Chem. 285:11508-11515.
12. Schafmeier T, Haase A, Kaldi K, Scholz J, Fuchs M, Brunner M. 2005. TranscriptionalfeedbackofNeurosporacircadianclockgenebyphosphor-ylation-dependent inactivation of its transcription factor. Cell 122:235-246.
13. Shi M, Collett M, Loros JJ, Dunlap JC. 2010. FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circa-dian clock. Genetics 184:351-361.
14. He Q, Liu Y. 2005. Degradation of the Neurospora circadian clock protein FREQUENCY through the ubiquitin-proteasome pathway. Biochem. Soc. Trans. 33:953-956.
15. Chen CH, Ringelberg CS, Gross RH, Dunlap JC, Loros JJ. 2009. Genome-wide analysis of light-inducible responses reveals hierarchical light Signaling in Neurospora. EMBO J. 28:1029-1042.
16. He Q, Cheng P, Yang Y, Wang L, Gardner KH, Liu Y. 2002. White Collar-1, a DNA binding transcription factor and a light sensor. Science 297:840-843.
17. Correa A, Lewis ZA, Greene AV, March IJ, Gomer RH, Bell-Pedersen D. 2003. Multiple oscillators regulate circadian gene expression in Neuro-spora. Proc. Natl. Acad. Sci. U. S. A. 100:13597-13602.
18. Dong W, Tang X, Yu Y, Nilsen R, Kim R, Griffith J, Arnold J, Schuttler HB. 2008. Systems biology of the clock in Neurospora crassa. PLoS One 3:e3105. doi:10.1371/journal.pone.0003105.
19. Sancar G, Sancar C, Brugger B, Ha N, Sachsenheimer T, Gin E, Wdowik S, Lohmann I, Wieland F, Hofer T, Diernfellner A, Brunner M. 2011. A global circadian repressor controls antiphasic expression of metabolic genes in Neurospora. Mol. Cell 44:687-697.
20. Lamb TM, Finch KE, Bell-Pedersen D. 2012. The Neurospora crassa OS MAPK pathway-activated transcription factor ASL-1 contributes to circa-dian rhythms in pathway responsive clock-controlled genes. Fungal Genet. Biol. 49:180-188.
21. Lamb TM, Goldsmith CS, Bennett L, Finch KE, Bell-Pedersen D. 2011. Direct transcriptional control of a p38 MAPK pathway by the circadian clock in Neurospora crassa. PLoS One 6:e27149. doi:10.1371/journal.pone.0027149.
22. Vitalini MW, de Paula RM, Goldsmith CS, Jones CA, Borkovich KA, Bell-Pedersen D. 2007. Circadian rhythmicity mediated by temporal regulation of the activity of p38 MAPK. Proc. Natl. Acad. Sci. U. S. A. 104: 18223-18228.
23. Widmann C, Gibson S, Jarpe MB, Johnson GL. 1999. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79:143-180.
24. Irmler S, Rogniaux H, Hess Pillonel DC. 2005. Induction of OS-2 phosphorylation in Neurospora crassa by treatment with phenylpyrrole fungicides and osmotic stress. Pesticide Biochem. Physiol. 84:25-37.
25. Zhang Y, Lamm R, Pillonel C, Lam S, Xu JR. 2002. Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl. Environ. Microbiol. 68:532-538.
26. Fu C, Iyer P, Herkal A, Abdullah J, Stout A, Free SJ. 2011. Identification and characterizationofgenes required for cell-to-cell fusion inNeurospora crassa. Eukaryot. Cell 10:1100-1109.
27. Li D, Bobrowicz P, Wilkinson HH, Ebbole DJ. 2005. A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170:1091-1104.
28. Maerz S, Ziv C, Vogt N, Helmstaedt K, Cohen N, Gorovits R, Yarden O, Seiler S. 2008. The nuclear Dbf2-related kinase COT1 and the mito- gen-activated protein kinases MAK1 and MAK2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179:1313-1325.
29. Park G, Pan S, Borkovich KA. 2008. Mitogen-activated protein kinase cascade required for regulation of development and secondary metabolism in Neurospora crassa. Eukaryot. Cell 7:2113-2122.
30. Roca MG, Arlt J, Jeffree CE, Read ND. 2005. Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot. Cell 4:911-919.
31. Chambard JC, Lefloch R, Pouyssegur J, Lenormand P. 2007. ERK implication in cell cycle regulation. Biochim. Biophys. Acta 1773:1299-1310.
32. Chen RE, Thorner J. 2007. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1773:1311-1340.
33. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U. S. A. 103:10352-10357.
34. Pall ML. 1993. The use of Ignite (Basta; glufosinate; phosphinothricin) to select transformants of bar-containing plasmids in Neurospora crassa. Fungal Genet. Newsl. 40:58.
35. Gooch VD, Mehra A, Larrondo LF, Fox J, Touroutoutoudis M, Loros JJ, Dunlap JC. 2008. Fully codon-optimized luciferase uncovers novel temperature characteristics of the Neurospora clock. Eukaryot. Cell 7:28-37.
36. Sargent ML, Briggs WR, Woodward DO. 1966. Circadian nature of a rhythm expressed by an invertaseless strain of Neurospora crassa. Plant Physiol. 41:1343-1349.
37. Plautz JD, Straume M, Stanewsky R, Jamison CF, Brandes C, Dowse HB, Hall JC, Kay SA. 1997. Quantitative analysis of Drosophila period gene transcription in living animals. J. Biol. Rhythms 12:204-217.
38. Bell-Pedersen D, Dunlap JC, Loros JJ. 1996. Distinct cis-acting elements mediate clock, light, and developmental regulation of the Neurospora crassa eas (ccg-2) gene. Mol. Cell. Biol. 16:513-521.
39. Bailey MJ, Beremand PD, Hammer R, Bell-Pedersen D, Thomas TL, Cassone VM. 2003. Transcriptional profiling of the chick pineal gland, a photoreceptive circadian oscillator and pacemaker. Mol. Endocrinol. 17: 2084-2095.
40. Karaganis SP, Kumar V, Beremand PD, Bailey MJ, Thomas TL, Cas-sone VM. 2008. Circadian genomics of the chick pineal gland in vitro. BMC Genomics 9:206. doi:10.1186/1471-2164-9-206.
41. Burnham K, Anderson D. 2002. Model selection and multi-model inference: a practical information theoretic approach, 2nd ed. Springer-Verlag New York Inc., New York, NY.
42. Pandey A, Roca MG, Read ND, Glass NL. 2004. Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot. Cell 3:348-358.
43. Heinisch JJ, Lorberg A, Schmitz HP, Jacoby JJ. 1999. The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol. Microbiol. 32:671-680.
44. Martin H, Arroyo J, Sanchez M, Molina M, Nombela C. 1993. Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity at 37°C. Mol. Gen. Genet. 241:177-184.
45. Vogt N, Seiler S. 2008. The RHO1-specific GTPase-activating protein LRG1 regulates polar tip growth in parallel to Ndr kinase signaling in Neurospora. Mol. Biol. Cell 19:4554-4569.
46. Zhu H, Nowrousian M, Kupfer D, Colot HV, Berrocal-Tito G, Lai H, Bell-Pedersen D, Roe BA, Loros JJ, Dunlap JC. 2001. Analysis of expressed sequence tags from two starvation, time-of-day-specific libraries of Neurospora crassa reveals novel clock-controlled genes. Genetics 157: 1057-1065.
47. Jung US, Levin DE. 1999. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity Signaling pathway. Mol. Micro-biol. 34:1049-1057.
48. Marshall CJ. 1994. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4:82-89.
49. Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Guldener U, Mannhaupt G, Munsterkotter M, Mewes HW. 2004. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32:5539-5545.
50. Lee KS, Irie K, Gotoh Y, Watanabe Y, Araki H, Nishida E, Matsumoto K, Levin DE. 1993. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates Signaling by protein kinase C. Mol. Cell. Biol. 13: 3067-3075.
51. Nowrousian M, Duffield GE, Loros JJ, Dunlap JC. 2003. The frequency gene is required for temperature-dependent regulation of many clock-controlled genes in Neurospora crassa. Genetics 164:923-933.
52. Yu Y, Dong W, Altimus C, Tang X, Griffith J, Morello M, Dudek L, Arnold J, Schuttler HB. 2007. A genetic network for the clock of Neurospora crassa. Proc. Natl. Acad. Sci. U. S. A. 104:2809-2814.
53. Manocha MS, Colvin JR. 1967. Structure and composition of the cell wall of Neurospora crassa. J. Bacteriol. 94:202-212.
54. Enderlin CS, Selitrennikoff CP. 1994. Cloning and characterization of a Neurospora crassa gene required for (1,3) β 3-glucan synthase activity and cell wall formation. Proc. Natl. Acad. Sci. U. S. A. 91:9500-9504.
55. Schimoler-O'Rourke R, Renault S, Mo W, Selitrennikoff CP. 2003. Neurospora crassa FKS protein binds to the (1,3)beta-glucan synthase substrate, UDP-glucose. Curr. Microbiol. 46:408-412.
56. Bobrowicz P, Pawlak R, Correa A, Bell-Pedersen D, Ebbole DJ. 2002. The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Mol. Microbiol. 45:795-804.
57. Gooch VD, Freeman L, Lakin-Thomas PL. 2004. Time-lapse analysis of the circadian rhythms of conidiation and growth rate in Neurospora. J. Biol. Rhythms 19:493-503.
58. Mazzoni C, Zarov P, Rambourg A, Mann C. 1993. The SLT2 (MPK1) MAP kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae. J. Cell Biol. 123:1821-1833.
59. Rubinfeld H, Seger R. 2005. The ERK cascade: a prototype of MAPK signaling. Mol. Biotechnol. 31:151-174.
60. Baetz K, Moffat J, Haynes J, Chang M, Andrews B. 2001. Transcriptional coregulation by the cell integrity mitogen-activated protein kinase Slt2 and the cell cycle regulator Swi4. Mol. Cell. Biol. 21:6515-6528.
61. Matia-Gonzalez AM, Rodriguez-Gabriel MA. 2011. Slt2 MAPK pathway is essential for cell integrity in the presence of arsenate. Yeast 28:9-17.
62. Riquelme M, Yarden O, Bartnicki-Garcia S, Bowman B, Castro-Longoria E, Free SJ, Fleissner A, Freitag M, Lew RR, Mourino-Perez R, Plamann M, Rasmussen C, Richthammer C, Roberson RW, Sanchez-Leon E, Seiler S, Watters MK. 2011. Architecture and development of the Neurospora crassa hypha-a model cell for polarized growth. Fungal Biol. 115:446-474.
63. Lindegren CC. 1945. An analysis of the mechanism of budding in yeasts and some observations on the structure of the yeast cell. Mycologia 37: 767-780.
64. Hamel P, Saint-Georges Y, de Pinto B, Lachacinski N, Altamura N, Dujardin G. 2004. Redundancy in the function of mitochondrial phosphate transport in Saccharomyces cerevisiae and Arabidopsis thaliana. Mol. Microbiol. 51:307-317.
65. Delmer DP, Brody S. 1975. Circadian rhythms in Neurospora crassa: oscillation in the level of an adenine nucleotide. J. Bacteriol. 121:548-553.
66. Ebbole DJ. 1998. Carbon catabolite repression of gene expression and conidiation in Neurospora crassa. Fungal Genet. Biol. 25:15-21.
67. Linden H, Ballario P, Macino G. 1997. Blue light regulation in Neuro-spora crassa. Fungal Genet. Biol. 22:141-150.
68. Wang Z, Deak M, Free SJ. 1994. A cis-acting region required for the regulated expression of grg-1, a Neurospora glucose-repressible gene: two regulatory sites (CRE and NRS) are required to repress grg-1 expression. J. Mol. Biol. 237:65-74.
69. Yamashita K, Shiozawa A, Watanabe S, Fukumori F, Kimura M, Fu-jimura M. 2008. ATF-1 transcription factor regulates the expression of ccg-1andcat-1genes inresponse tofludioxonil under OS-2 MAP kinase in Neurospora crassa. Fungal Genet. Biol. 45:1562-1569.
70. McClean MN, Mody A, Broach JR, Ramanathan S. 2007. Cross-talk and decision making in MAP kinase pathways. Nat. Genet. 39:409-414.
71. Schwartz MA, Madhani HD. 2004. Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu. Rev. Genet. 38:725-748.
72. Bermejo C, Rodriguez E, Garcia R, Rodriguez-Pena JM, Rodriguez de laConcepcion ML, Rivas C, Arias P, Nombela C, Posas F, Arroyo J. 2008. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol. Biol. Cell 19:1113-1124.
73. Huang XL, Fu CJ, Bu RF. 2011. Role of circadian clocks in the development and therapeutics of cancer. J. Int. Med. Res. 39:2061-2066.
74. Plotnikov A, Zehorai E, Procaccia S, Seger R. 2011. The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translo-cation. Biochim. Biophys. Acta 1813:1619-1633.