Circadian oscillation and light-induced changes in the concentration of cyclic nucleotides in Neurospora

Hasunuma, Kohji; Funadera, Kanako; Shinohara, Yukie; Furukawa, Kazuhiko; Watanabe, Masakatsu

doi:10.1007/bf00434667

Cited by 18 publications

(7 citation statements)

References 31 publications

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“…In mammals, cAMP-dependent signaling oscillates in a circadian manner, which in turn regulates core circadian oscillators (54-57). In Neurospora, the level of cAMP is controlled by the circadian clock (58). The elevated intracellular levels of cAMP result in the activation of PKA (59).…”

Section: Discussionmentioning

confidence: 99%

Role for Protein Kinase A in the Neurospora Circadian Clock by Regulating White Collar-Independent frequency Transcription through Phosphorylation of RCM-1

Liu

et al. 2015

Molecular and Cellular Biology

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Rhythmic activation and repression of clock gene expression is essential for the eukaryotic circadian clock functions. In the Neurospora circadian oscillator, the transcription of the frequency (frq) gene is periodically activated by the White Collar (WC) complex and suppressed by the FRQ-FRH complex. We previously showed that there is WC-independent frq transcription and its repression is required for circadian gene expression. How WC-independent frq transcription is regulated is not known. We show here that elevated protein kinase A (PKA) activity results in WC-independent frq transcription and the loss of clock function. We identified RCM-1 as the protein partner of RCO-1 and an essential component of the clock through its role in suppressing WCindependent frq transcription. RCM-1 is a phosphoprotein and is a substrate of PKA in vivo and in vitro. Mutation of the PKAdependent phosphorylation sites on RCM-1 results in WC-independent transcription of frq and impaired clock function. Furthermore, we showed that RCM-1 is associated with the chromatin at the frq locus, a process that is inhibited by PKA. Together, our results demonstrate that PKA regulates frq transcription by inhibiting RCM-1 activity through RCM-1 phosphorylation. Circadian clocks allow prokaryotic and eukaryotic organisms to regulate their daily molecular, cellular, behavioral, and physiological activities. The eukaryotic circadian clocks are composed of autoregulatory negative-feedback loops, including positive and negative elements that form the core circadian oscillators (1-6). Rhythmic transcriptional activation of the negative elements by the positive elements and rhythmic repression of positive elements by the negative elements are thought to be the main molecular basis for the generation of endogenous rhythmicity in eukaryotic clock systems. In addition to regulation at the transcriptional level, posttranslational modification of clock proteins by phosphorylation plays essential roles in clock functions (7-10).In the filamentous fungus Neurospora crassa, the core circadian negative feedback loop is composed of the positive elements, White Collar 1 (WC-1) and White Collar 2 (WC-2), and the negative elements, FREQUENCY (FRQ) and its partner FRQ-interacting RNA helicase (FRH) (2,3,11,12). WC-1 and WC-2, two Per-Arnt-Sim (PAS) domain-containing transcription factors, form the WC heterodimeric complex that binds to the Clock (C)-box of frq promoter to activate frq transcription (13-18). On the other hand, FRQ and FRH form the FFC complex to inhibit frq transcription by suppressing the activity of the WC complex by promoting WC phosphorylation (19)(20)(21)(22)(23)(24). FRQ is progressively phosphorylated over time before its degradation through the ubiquitin-proteasome pathway mediated by FWD-1 (21, 25-28). Genetic analyses show that the FRQ-dependent phosphorylation of WC-1 and WC-2 that suppresses White Collar complex (WCC) activity is mostly mediated by CKI and CKII (21).WC complex was long thought to be the only transcriptional activator o...

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Section: Discussionmentioning

confidence: 99%

Role for Protein Kinase A in the Neurospora Circadian Clock by Regulating White Collar-Independent frequency Transcription through Phosphorylation of RCM-1

Liu

et al. 2015

Molecular and Cellular Biology

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“…The binding of cyclic AMP (cAMP) to the regulatory subunit results in its dissociation from the holoenzyme and the activation of the catalytic subunit (Taylor et al 2005). In Neurospora, the level of cAMP shows a daily rhythm (Hasunuma et al 1987), and inhibitors of cAMP phosphodiesterase lengthen the period of the circadian conidiation rhythm (Feldman 1975). In addition, PKA is known to regulate Neurospora growth and development (Bruno et al 1996;Banno et al 2005).…”

Section: Pkac-1 Is Required For Most Of the Pka Activity In Neurosporamentioning

confidence: 99%

“…The cAMP level is controlled by the circadian clock in Neurospora (Hasunuma et al 1987). Thus, although PKA can phosphorylate the WCs independent of FRQ, the daily rhythm of cAMP in a wild-type strain should regulate PKA function rhythmically, forming another posttranslational loop in the circadian clock.…”

Section: Pka Acts As a Priming Kinase For Ck-1a Or Ckii In Wc Phosphomentioning

confidence: 99%

Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop

Huang¹,

Chen²,

Li³

et al. 2007

Genes Dev.

119

159

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Regulation of circadian clock components by phosphorylation plays essential roles in clock functions and is conserved from fungi to mammals. In the Neurospora circadian negative feedback loop, FREQUENCY (FRQ) protein inhibits WHITE COLLAR (WC) complex activity by recruiting the casein kinases CKI and CKII to phosphorylate the WC proteins, resulting in the repression of frq transcription. On the other hand, CKI and CKII progressively phosphorylate FRQ to promote FRQ degradation, a process that is a major determinant of circadian period length. Here, by using whole-cell isotope labeling and quantitative mass spectrometry methods, we show that the WC-1 phosphorylation events critical for the negative feedback process occur sequentially-first by a priming kinase, then by the FRQ-recruited casein kinases. We further show that the cyclic AMP-dependent protein kinase A (PKA) is essential for clock function and inhibits WC activity by serving as a priming kinase for the casein kinases. In addition, PKA also regulates FRQ phosphorylation, but unlike CKI and CKII, PKA stabilizes FRQ, similar to the stabilization of human PERIOD2 (hPER2) due to the phosphorylation at the familial advanced sleep phase syndrome (FASPS) site. Thus, PKA is a key clock component that regulates several critical processes in the circadian negative feedback loop.[Keywords: Circadian clock; Neurospora; protein kinase A; phosphorylation; casein kinase I] Supplemental material is available at http://www.genesdev.org. Cheng et al. 2001aCheng et al. , 2005. FFC represses the transcription of frq by inhibiting WCC activity through their physical interaction (Aronson et al. 1994;Merrow et al. 1997Merrow et al. , 2001Cheng et al. 2001aCheng et al. , 2003Denault et al. 2001;Froehlich et al. 2003;He et al. 2006). This circadian negative feedback loop generates the robust circadian rhythms of frq RNA and FRQ protein in constant darkness (DD) .Post-translational modification of clock proteins by phosphorylation plays essential roles in all circadian clocks (Price et al. 1998;Lowrey et al. 2000;Lin et al. 2002;Sathyanarayanan et al. 2004

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“…Flowering (Takimoto and Hamner, 1965;Saji et al, 1982), leaf movement (Kiyosawa and Tanaka, 1976), K' influx (Kondo, 1983) and C 0 2 production (Hillman, 1971) show circadian rhythm in higher plants. We demonstrated circadian oscillation of the concentration of cyclic 3',5'-AMP and -GMP in mycelia of Neurospora crassa (Hasunuma et a/. , 1987a).…”

Section: Introductionmentioning

confidence: 82%

RHYTHMIC OSCILLATION OF CYCLIC 3′,5′AMP AND ‐GMP CONCENTRATION AND STIMULATION OF FLOWERING BY CYCLIC 3′,5′‐GMP IN Lemna paucicostata 381

Hasunuma

Funadera

Furukawa

et al. 1988

Photochem & Photobiology

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Abstract— Rhythmic oscillation of the concentration of cyclic 3′,5′‐AMP and ‐GMP in a short day plant, Lemna paucicostata 381 in continuous darkness was detected after 2 cycles of 12 h dark and 12 h light entrainment. Cyclic 3′,5′‐AMP and ‐GMP, extracted from whole plant showed parallel oscillations in their concentrations for initial 36 h in continuous darkness and the oscillation in the concentration of cyclic 3′,5′‐AMP was roughly circadian. Their concentrations decreased during the initial 12 h (subjective night) and increased during 12 to 28 h. Exogenous addition of 2 μ.M of cyclic 3′,5′‐GMP or the dibutyryl derivative of it stimulated floral induction by 20 to 30%, when the plants were grown under 12 h light and 12 h dark regime. Cyclic 3′,5′‐AMP or the dibutyryl derivative of it showed little effect on flowering.

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Circadian oscillation and light-induced changes in the concentration of cyclic nucleotides in Neurospora

Cited by 18 publications

References 31 publications

Role for Protein Kinase A in the Neurospora Circadian Clock by Regulating White Collar-Independent frequency Transcription through Phosphorylation of RCM-1

Role for Protein Kinase A in the Neurospora Circadian Clock by Regulating White Collar-Independent frequency Transcription through Phosphorylation of RCM-1

Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop

RHYTHMIC OSCILLATION OF CYCLIC 3′,5′AMP AND ‐GMP CONCENTRATION AND STIMULATION OF FLOWERING BY CYCLIC 3′,5′‐GMP IN Lemna paucicostata 381

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