CaM kinase II


EVOLUTIONARY HOMOLOGS


Table of contents


Other Drosophila CaM kinases

MAGUKs (membrane-associated guanylate kinase homologs) are proteins involved in cell junction organization, tumor suppression, and signaling (See Drosophila Discs large). Their structure includes one or three copies of a DHR or PDZ domain (discs-large homologous region or PSD-95/SAP90, discs-large, ZO-1 homologous domain), an SH3 domain, and a guanylate kinase domain. MAGUKs have been classified into two subfamilies: Dlg-like with three DHR/PDZ domains and p55-like with a single DHR/PDZ domain. There is now a new subfamily whose members have a novel domain structure: a calcium/calmodulin-dependent protein kinase domain in the N-terminus as well as the DHR/PDZ, SH3 and GUK domains in the C-terminus. These new MAGUKs may regulate transmembrane molecules that bind calcium, calmodulin, or nucleotides. camguk (cmg) is a Drosophila member of this novel MAGUK subfamily. The DHR domain of Camguk is 54% identical to that of human p55, the SH3 domain 66% identical, and the GUK domain 50% identical. The N-terminus sequence predicts a domain with striking similarity to calcium/calmodulin-dependent protein kinase, including the entire putative catalytic domain (37% identity with that of Drosophila CaM kinase type IIß) and the calmodulin-binding domain (61% identity). The C. elegans homolog is encoded by the lin-2 gene, required for the response of vulval precursor cells to the vulval induction signal from the anchor cell. The rat homolog CASK was identified in a yeast two-hybrid screen based on its interaction with the cytoplasmic domains of neurexins (See Drosophila Neurexin). In the case of Lin-2, it has been sugested that the protein may function in vulval induction by clustering the Let-23 EGFR tyrosine kinase receptor on the basolateral plasma membrane of the vulval precursor cell so that Let-23 can receive the signal from the anchor cell more efficiently (Dimitratos, 1997).

CaM kinase structure

The crystal structure of the 143 residue association domain of Ca2+/calmodulin-dependent protein kinase II (CaMKII) is reported. The association domain forms a hub-like assembly, composed of two rings of seven protomers each, which are stacked head to head and held together by extensive interfaces. The tetradecameric organization of the assembly was confirmed by analytical ultracentrifugation and multiangle light scattering. Individual protomers form wedge-shaped structures from which N-terminal helical segments that connect to the kinase domain extend toward the equatorial plane of the assembly, consistent with the arrangement of the kinase domains in a second outer ring. A deep and highly conserved pocket present within the association domain may serve as a docking site for proteins that interact with CaMKII (Hoelz, 2003).

Low-resolution electron microscopic images of the CaMKII holoenzyme have provided intriguing views of a hub and spoke assembly in which the catalytic domains are arranged in a ring around a central scaffold formed by the association domain. These images suggest that the nature of the oligomeric assembly might govern a highly cooperative activation process in which the precise details of the activation kinetics of CaMKII would depend on the nature of the interactions between the kinase domains. The crystal structure of the tetradecameric assembly reveals that the association domain forms a circular hub that has a diameter of ~145 Å and a height of ~60 Å. The hub consists of two seven-membered rings that are stacked head to head on top of one another, creating a 50 Å wide central pore. The N-terminal linker segments of each of the protomers point outward toward the equatorial plane, which suggests that the autoinhibited kinase domains are arranged in an outer ring around the central hub. Each protomer contains a deep pocket facing toward the pore's center, with features that are suggestive of a role for this pocket in binding to peptide segments (Hoelz, 2003).

CaM kinase signaling involved in determination of asymmetric olfactory neuron fates in C. elegans

In general, the chemosensory neurons of C. elegans exhibit bilateral symmetry, with pairs of similar neurons located on the left and right sides of the animal. A further level of diversity is achieved in the AWC olfactory neuron pair through a cell interaction between the two AWC cells (AWCL and AWCR). The candidate olfactory receptor gene str-2 is expressed asymmetrically and stochastically in only one of the two AWC neurons: half of a population of animals expresses a str-2::GFP reporter gene in AWCR and half expresses it in AWCL. Asymmetry between the two AWC neurons enables the animal to detect more odors and discriminate between them in complex environments. nsy-1 mutants express str-2 in both neurons, disrupting AWC asymmetry. nsy-1 encodes a homolog of the human MAP kinase kinase kinase (MAPKKK) ASK1, an activator of JNK and p38 kinases. Based on genetic epistasis analysis, nsy-1 appears to act downstream of the CaMKII unc-43, and NSY-1 associates with UNC-43, suggesting that UNC-43/CaMKII activates the NSY-1 MAP kinase cassette. Mosaic analysis demonstrates that UNC-43 and NSY-1 act primarily in a cell-autonomous execution step that represses str-2 expression in one AWC cell, downstream of the initial lateral signaling pathway that coordinates the fates of the two cells (Sagasti, 2001).

UNC-43/CaMKII and NSY-1/ASK1 have central roles in a cell interaction that determines cell fates in the olfactory system of C. elegans. Although most neurons in C. elegans exist as bilaterally symmetric, morphologically similar pairs, the two AWC olfactory neurons interact with each other to allow AWCL and AWCR to adopt distinct fates. The stochastic and coordinated interaction that determines AWC asymmetry is reminiscent of lateral signaling, a process that allows two initially equivalent cells to coordinate their fates so that each adopts a distinct identity. The only well-characterized molecular pathway that accomplishes lateral signaling is mediated by Notch family receptors. In lateral signaling interactions mediated by Notch, ablating one of the interacting cells causes the remaining cell to adopt a default fate. Similarly, ablating one of the two AWC cells causes the remaining cell to adopt the AWCOFF fate. However, several features of the AWC lateral interaction are not typical for Notch signaling: the signaling between the two AWC neurons is mediated by calcium and a MAPK pathway, and occurs in relatively mature neurons whose axons have made contact with each other. In addition, unlike Notch lateral signaling, UNC-43/NSY-1 signaling primarily affects execution of the AWCOFF fate and not feedback between the AWC neurons (Sagasti, 2001).

unc-43 and nsy-1 act in the AWC neuron pair to control the asymmetric expression of str-2::GFP. Expressing either nsy-1 or unc-43 in both AWC cells restores asymmetric cell fates in nsy-1 and unc-43 mutants, demonstrating that it is not the asymmetric expression of these genes but rather asymmetric activity that controls AWC cell fates. A signal from the AWCOFF cell is required for the AWCON fate, but unc-43 and nsy-1 are required for the AWCOFF fate; their activities may be repressed by the initial signal (Sagasti, 2001).

Genetic mosaic analysis was used to ask whether unc-43 and nsy-1 are required in a strictly cell autonomous manner to execute the AWCOFF cell fate, or whether they also play roles in coordinating the two cell fates. The mosaic strategy and cell interaction model were based on the AC/VU lateral signaling decision that occurs between two cells in the C. elegans hermaphrodite gonad, Z1.ppp and Z4.aaa. Z1.ppp and Z4.aaa make a stochastic, coordinated decision that allows one cell to adopt an anchor cell (AC) fate and the other cell to adopt a ventral uterine precursor cell (VU) fate. This interaction requires the Notch family receptor lin-12. lin-12 activity is required in the VU cell to allow it to receive an inducing signal from the AC cell. If lin-12 is mutant in one of the two AC/VU cells, the mutant cell always adopted the AC fate and the wild-type cell always adopts the VU fate. Because lin-12 is involved in the feedback loop between AC and VU, loss of lin-12 activity in one cell has a nonautonomous effect that forces the other cell to become VU. By analogy, it was reasoned that if unc-43 and nsy-1 are involved in a feedback loop in the AWC cell fate decision, the loss of unc-43 and nsy-1 activity in one AWC neuron would result in mosaic animals with one AWCOFF (wild-type) and one AWCON (mutant) cell every time. A different result is expected if these genes act to execute the AWCOFF cell fate. The execution model predicts that half of the mosaic animals would have two AWCON cells. The mutant cell will always adopt the AWCON fate, whereas the wild-type cell will take on the AWCON and AWCOFF fates with equal frequency (Sagasti, 2001).

Genetic mosaic analyses with unc-43 gain-of-function and loss-of-function mutants fit the prediction for a strictly cell-autonomous gene that executes the AWCOFF cell fate in one cell. Loss-of-function and gain-of-function mosaics with nsy-1 were also mostly consistent with the execution model: the presence of two classes of nsy-1(lf) and nsy-1(gf) mosaics supports the idea that nsy-1 functions mainly to execute the AWCOFF cell fate cell autonomously. However, the class of mosaics with one AWCON (mutant) and one AWCOFF (wild-type) neuron is more prevalent in nsy-1(lf) mosaics, suggesting that nsy-1 has a minor cell nonautonomous effect on AWC fate (Sagasti, 2001).

These results suggest a model for the execution of the AWCOFF cell fate. An initial lateral signaling interaction between the two AWC cells defines one cell as AWCON and the other as AWCOFF. In the cell defined as AWCOFF, calcium influx through a voltage-gated calcium channel (UNC-2 and UNC-36) activates the calcium-calmodulin dependent kinase UNC-43, which in turn activates the MAPKKK NSY-1. Activation of the MAPKKK pathway represses str-2 transcription in the AWCOFF cell. In contrast with signaling molecules of Notch pathways, the CaMKII/NSY-1 signaling cassette is not an essential component of lateral signaling and feedback. The genes that participate in the initial AWC cell interaction are not known. One candidate for a molecule involved in this lateral signaling pathway is nsy-3, which is genetically upstream of or parallel to the CaMKII unc-43. nsy-2 is a candidate to act at a downstream step in execution, since like nsy-1 it is epistatic to unc-43. These results, coupled with the observation that NSY-1 and UNC-43 have well-conserved mammalian homologs, raise the possibility that the calcium-to-MAPK signaling cassette used in AWC cell fate determination may be used for cell fate diversification in other animals (Sagasti, 2001).

Activation of CaMKII activation in C. elegans oocytes

Fertilization in the female reproductive tract depends on intercellular signaling mechanisms that coordinate sperm presence with oocyte meiotic progression. To achieve this coordination in C. elegans, sperm release an extracellular signal, the major sperm protein (MSP), to induce oocyte meiotic maturation and ovulation. MSP binds to multiple receptors, including the VAB-1 Eph receptor protein-tyrosine kinase on oocyte and ovarian sheath cell surfaces. Canonical VAB-1 ligands called ephrins negatively regulate oocyte maturation and MPK-1 mitogen-activated protein kinase (MAPK) activation. MSP and VAB-1 regulate the signaling properties of two Ca2+ channels that are encoded by the NMR-1 N-methyl D-aspartate type glutamate receptor subunit and ITR-1 inositol 1,4,5-triphosphate receptor. Ephrin/VAB-1 signaling acts upstream of ITR-1 to inhibit meiotic resumption, while NMR-1 prevents signaling by the UNC-43 Ca2+/calmodulin-dependent protein kinase II (CaMKII). MSP binding to VAB-1 stimulates NMR-1-dependent UNC-43 activation, and UNC-43 acts redundantly in oocytes to promote oocyte maturation and MAPK activation. These results support a model in which VAB-1 switches from a negative regulator into a redundant positive regulator of oocyte maturation upon binding to MSP. NMR-1 mediates this switch by controlling UNC-43 CaMKII activation at the oocyte cortex (Corrigan, 2005).

Protein interaction and targets of CaM kinases

CaM-kinase II is highly concentrated at synapses that utilize glutamate as the neurotransmitter. CaM-kinase II can phosphorylate these glutamate receptor/ion channels and enhance the ion current flowing through them. This may contribute to mechanisms of synaptic plasticity that are important in cellular paradigms of learning and memory such as long-term potentiation in the hippocampus (Soderling, 1993).

The major postsynaptic density (PSD) protein at glutaminergic synapses is calcium/calmodulin-dependent protein kinase II (CaM-K II), but its function in the PSD is not known. Glutamate receptors (GluRs) have been examined as substrates for CaM-K II because (1) they are colocalized in the PSD; (2) cloned GluRs contain consensus phosphorylation sites for protein kinases, including CaM-K II, and (3) several GluRs are regulated by other protein kinases. Regulation by CaM-K II of GluRs (which are involved in excitatory synaptic transmission and in mechanisms of learning and memory) is of interest because of the postulated role of CaM-K II in synaptic plasticity and its known involvement in induction of long-term potentiation. Furthermore, mice lacking the major neural isoform of CaM-K II exhibit deficits in models of learning and memory that require hippocampal input. CaM-K II phosphorylates GluR in several in vitro systems, including the PSD, and activated CaM-K II enhances kainate-induced ion current three- to fourfold in cultured hippocampal neurons. These results are consistent with a role for PSD CaM-K II in strengthening postsynaptic GluR responses in synaptic plasticity (McGlade-McCulloh, 1993).

Glutamate receptor ion channels are colocalized in postsynaptic densities with Ca2+/calmodulin-dependent protein kinase II (CaM-kinase II), which can phosphorylate and strongly enhance non-N-methyl-D-aspartate (NMDA) glutamate receptor current. In Xenopus oocytes CaM-kinase II enhances kainate currents of expressed glutamate receptor 6 and of wild-type glutamate receptor 1. A synthetic peptide corresponding to residues 620-638 in GluR1 is phosphorylated in vitro by CaM-kinase II. The 32P-labeled peptide map of this synthetic peptide appears to be the same as the two-dimensional peptide map of AMPA glutamate receptors phosphorylated in cultured hippocampal neurons by CaM-kinase II. This CaM-kinase II regulatory phosphorylation site is conserved in all AMPA/kainate-type glutamate receptors, and its phosphorylation may be important in enhancing the postsynaptic responsiveness that occurs during synaptic plasticity (Yakel, 1995).

Long-term potentiation (LTP), a cellular model of learning and memory, requires calcium-dependent protein kinases. Induction of LTP increases the phosphorus-32 labeling of AMPA-type glutamate receptors (AMPA-Rs), which mediate rapid excitatory synaptic transmission. This AMPA-R phosphorylation appears to be catalyzed by Ca2+- and calmodulin-dependent protein kinase II (CaM-KII): (1) it correlates with the activation and autophosphorylation of CaM-KII; (2) it is blocked by the CaM-KII inhibitor KN-62, and (3) its phosphorus-32 peptide map is the same as that of GluR1 coexpressed with activated CaM-KII in HEK-293 cells. This covalent modulation of AMPA-Rs in LTP provides a postsynaptic molecular mechanism for synaptic plasticity (Barria, 1997).

To determine the mechanisms responsible for the termination of Ca2+-activated Cl- currents (ICl[Ca]), simultaneous measurements of whole cell currents and intracellular Ca2+ concentration ([Ca2+]i) were made in equine tracheal myocytes. In nondialyzed cells, or cells dialyzed with ATP, ICl(Ca) decays before the [Ca2+]i declines, whereas the calcium-activated potassium current decays at the same rate as [Ca2+]i. Substitution of AMP-PNP or ADP for ATP markedly prolongs the decay of ICl(Ca), resulting in a rate of current decay similar to that of the fall in [Ca2+]i. In the presence of ATP, dialysis of the calmodulin antagonist W7, or in the presence of the Ca2+/calmodulin-dependent kinase II (CaMKII) inhibitor KN93, or in the presence of a CaMKII-specific peptide inhibitor the rate of ICl(Ca) decay is slowed and matches the [Ca2+]i decline. When a sustained increase in [Ca2+]i is produced in ATP dialyzed cells, the current decays completely, whereas cells loaded with 5'-adenylylimidodiphosphate (AMP-PNP), KN93, or the CaMKII inhibitory peptide, (ICl[Ca]) do not decay. Slowly decaying currents are repeatedly evoked in ADP- or AMP-PNP-loaded cells, but dialysis of adenosine 5'-O-(3-thiotriphosphate) or okadaic acid results in a smaller initial ICl(Ca), and little or no current (despite a normal [Ca2+]i transient) with a second stimulation. These data indicate that CaMKII phosphorylation results in the inactivation of calcium-activated chloride channels, and that transition from the inactivated state to the closed state requires protein dephosphorylation (Wang, 1997).

Ca2+ plays a central role in cell signaling. Ca2+/calmodulin-dependent protein kinase II (CaMKII) is a major mediator of Ca2+ actions. The spatial distribution of intracellular Ca2+ signaling is not homogenous; rather, it is dynamically organized. It has been speculated that spatial patterns of Ca2+ signals may function as a form of cellular information transmitted to downstream molecules. To address this issue, the intracellular distributions of the signalings by CaMKII and Ca2+ were studied together, in the same astrocytes. CaMKII was visualized by monitoring site-specific phosphorylation of a cytoskeletal protein vimentin, using site- and phosphorylation-specific antibodies, while Ca2+ was examined by fura-2-based Ca2+ microscopy. Local Ca2+ signals induce vimentin phosphorylation by CaMKII localized in the same area. In contrast, Ca2+ waves in astrocytes induce global phosphorylation of vimentin by CaMKII. A small population of vimentin filaments highly phosphorylated by CaMKII undergo structural alteration into short filaments at the electron microscopic level. These results indicate that CaMKII transmits spatial patterns of Ca2+ signals to vimentin as cellular information. It is possible that spatial patterns of vimentin phosphorylation may be important for intracellular organization of vimentin filament networks (Inagaki, 1997).

An understanding of the role of CaM kinase II in the pancreatic beta-cell is dependent on the identification of its cellular targets. One of the best substrates of CaM kinase II in vitro that could function in secretory events is the microtubule-associated protein, MAP-2. By immunoblot analysis, a high molecular weight protein with electrophoretic properties characteristic of MAP-2 was identified in rat insulinoma betaTC3 cells and isolated rat islets. In immunoprecipitation experiments employing alpha-toxin-permeabilized betaTC3 cells, elevation of intracellular Ca2+ or addition of forskolin, an adenylate cyclase activator, induces significant phosphorylation of MAP-2 in situ. The effect of Ca2+ is rapid, concentration-dependent and closely correlated with activation of CaM kinase II under similar experimental conditions. H-89, a specific and potent inhibitor of cAMP-dependent protein kinase (PKA), prevents forskolin-induced MAP-2 phosphorylation but has little effect on MAP-2 phosphorylation stimulated by elevated Ca2+. Phosphopeptide mapping reveals that the phosphorylation pattern observed in situ upon incubation of the betaTC3 cells with increased free Ca2+, is strikingly similar to that generated in vitro by CaM kinase II, most notably with regard to the increased phosphate incorporated into one prominent site. These data provide evidence that MAP-2 is phosphorylated by CaM kinase II in the pancreatic beta-cell in situ, and that this event may provide an important link in the mediation of Ca2+-dependent insulin secretion (Krueger, 1997).

Numerous in vivo studies have demonstrated that psychostimulant drugs such as amphetamine and cocaine can induce the expression of the immediate early gene c-fos in striatal neurons via the activation of D1 dopamine receptors. NMDA receptor activation is also known to induce c-fos in the striatum. A primary striatal neuronal culture preparation was used to examine the mechanisms whereby these stimuli lead to changes in gene expression. Direct application of NMDA to striatal cells in culture causes a rapid increase in the expression of c-fos, as well as an increase in the phosphorylation of the transcription factor CRE binding protein (CREB). This is prevented by NMDA receptor antagonists, and requires extracellular calcium, but does not involve L-type calcium channels. The induction of c-fos and CREB phosphorylation following NMDA are unaffected by inhibition of protein kinase C, tyrosine kinases or nitric oxide synthase. However, the response to NMDA is blocked by KN62, a selective inhibitor of calcium/calmodulin-dependent protein kinase. The application of the D1 agonist SKF 38393, or the direct stimulation of adenylyl cyclase with forskolin, also results in the phosphorylation of CREB and the induction of c-fos in striatal neurons. These effects are blocked by the protein kinase A inhibitor H89. These observations are consistent with the hypothesis that calcium/calmodulin-dependent phosphorylation of CREB induced by NMDA, or cAMP-dependent phosphorylation of CREB induced by D1 agonists, underlie the induction of c-fos seen following activation of these receptors in striatal neurons (Das, 1997).

The cAMP response element-binding protein (CREB) (Drosophila homolog: CrebB-17A) has been shown to mediate transcriptional activation in response to both cAMP and calcium influx signal transduction pathways. The roles of two multifunctional calcium/calmodulin-dependent protein kinases, CaMKIV and CaMKII, have been examined in transient transfection studies utilizing either the full-length or the constitutively active forms of these kinases. CaMKIV was found to be much more potent than CaMKII in activating CREB in three different cell lines. It was also found that Ser133 of CREB is essential for its activation by CaMKIV. Mutagenesis studies and phosphopeptide mapping analysis demonstrate that in vitro, CaMKIV phosphorylates CREB at Ser133 only, whereas CaMKII phosphorylates CREB at Ser133 and a second site, Ser142. Phosphorylation of Ser142 by CaMKII blocks the activation of CREB that would otherwise occur when Ser133 is phosphorylated. When Ser142 is mutated to alanine, CREB is activated by CaMKII, as well as by CaMKIV. Mutation of Ser142 to alanine enhances the ability of Ca2+ influx to activate CREB, suggesting a physiological role for the phosphorylation of Ser142 in modulation of CREB activity. These data provide evidence for a new mechanism for regulation of CREB activity involving phosphorylation of a negative regulatory site in the transcriptional activation domain, as well as new insights into possible interactions between the cAMP and Ca2+ signaling pathways in the regulation of transcription. Changes in intracellular Ca2+ have the potential to either inhibit or augment the ability of cAMP to stimulate transcription, depending on the presence of specific forms of Ca2+/calmodulin-dependent protein kinases (Sun, 1994).

Phosphorylation of CREB (cyclic AMP [cAMP]- response element [CRE]-binding protein) by cAMP-dependent protein kinase (PKA) leads to the activation of many promoters containing CREs (See Drosophila homolog: cAMP dependent protein kinase 1). In neurons and other cell types, CREB phosphorylation and activation of CRE-containing promoters can occur in response to elevated intracellular Ca2+. In cultured cells lacking this Ca2+ responsiveness, Ca(2+)-mediated activation of a CRE-containing promoter can be conferred by introducing an expression vector for Ca2+/calmodulin-dependent protein kinase type IV (CaMKIV). Activation can also be mediated directly by a constitutively active form of CaMKIV, which is Ca2+ independent. The CaMKIV-mediated gene induction requires the activity of CREB/ATF family members but is independent of PKA activity. In contrast, transient expression of either a constitutively active or wild-type Ca2+/calmodulin-dependent protein kinase type II (CaMKII) fails to mediate the transactivation of the same CRE-containing reporter gene. Examination of the subcellular distribution of transiently expressed CaMKIV and CaMKII reveals that only CaMKIV enters the nucleus. These results demonstrate that CaMKIV, which is expressed in neuronal, reproductive, and lymphoid tissues, may act as a mediator of Ca(2+)-dependent gene induction (Matthews, 1994).

Ca2+ influx through n-methyl-d-aspartate- (NMDA-) type glutamate receptors plays a critical role in synaptic plasticity in the brain. One of the proteins activated by the increase in Ca2+ is CaM kinase II (CaMKII). A novel synaptic Ras-GTPase activating protein (p135 SynGAP) is described that is a major component of the postsynaptic density, a complex of proteins associated with synaptic NMDA receptors. The sequence contains four regions homologous to previously identified protein motifs. Most notable is the RasGAP motif from positions 393 to 717. Its sequence is 30% identical to p120 RasGAP and it contains the FLR PA P motif diagnostic for RasGAPs. The amino-terminal segment contains a putative PH domain, which may attach the protein to the membrane, and a region 31% identical to the C2 domain of p120 GAP, a motif that mediates binding to phospholipid and/or Ca2+ in synaptotagmin and protein kinase C. Two of the putative splice variants end in QTRV, conforming to the consensus sequence tS/TXV, which can bind to the second and third PDZ domains of the scaffold protein PSD-95. A proline-rich region between positions 770 and 800 may form a binding site for SH3 domains. The message encoding p135 SynGAP is expressed at higher levels in brain than in other tissues. Furthermore, within neurons the protein is highly localized to synapses. Western blots of subcellular fractions from rat forebrain made with antibodies against p135 SynGAP reveal that it is enriched in isolated PSDs even after extraction with the relatively harsh detergent N-lauroyl sarcosinate. p135 SynGAP is almost exclusively localized at synapses in hippocampal neurons, where it binds to and closely colocalizes with the scaffold protein PSD-95 and colocalizes with NMDA receptors. The Ras-GTPase activating activity of p135 SynGAP is inhibited by phosphorylation by CaMKII located in the PSD protein complex. Inhibition of p135 SynGAP by CaMKII will stop inactivation of GTP-bound Ras and thus could result in activation of the mitogen-activated protein (MAP) kinase pathway in hippocampal neurons upon activation of NMDA receptors (Chen, 1998).

Acute desensitization of olfactory signaling is a critical property of the olfactory system that allows animals to detect and respond to odorants. Correspondingly, an important feature of odorant-stimulated cAMP increases is their transient nature, a phenomenon that may be attributable to the unique regulatory properties of the olfactory adenylyl cyclase (AC3) (see Drosophila Rutabaga). AC3 is stimulated by receptor activation and inhibited by Ca2+ through Ca2+/calmodulin kinase II (CaMKII) phosphorylation at Ser-1076. Since odorant-stimulated cAMP increases are accompanied by elevated intracellular Ca2+, CaMKII inhibition of AC3 may contribute to termination of olfactory signaling. To test this hypothesis, a polyclonal antibody specific for AC3 phosphorylated at Ser-1076 was generated. A brief exposure of mouse olfactory cilia or primary olfactory neurons to odorants stimulates phosphorylation of AC3 at Ser-1076. This phosphorylation is blocked by inhibitors of CaMKII, which also ablates cAMP decreases associated with odorant-stimulated cAMP transients. These data define a novel mechanism for termination of olfactory signaling that may be important in olfactory responses (Wei, 1998).

Replication factor C (RF-C) is a heteropentameric protein essential for DNA replication and DNA repair. It is a molecular matchmaker required for loading of the proliferating cell nuclear antigen (Drosophila homolog: PCNA) sliding clamp onto double-strand DNA and for PCNA-dependent DNA synthesis by DNA polymerases delta and epsilon. The DNA and PCNA binding domains of the large 140 kDa subunit of human RF-C have been recently cloned. The PCNA binding domain is phosphorylated by the Ca2+/calmodulin-dependent protein kinase II, an enzyme required for cell cycle progression in eukaryotic cells. However, the DNA binding domain is not phosphorylated. Phosphorylation by CaMKII reduces the binding of PCNA to RF-C and consequently inhibits RF-C-dependent DNA synthesis by DNA polymerases delta1 and epsilon. Once bound to PCNA and DNA, RF-C is protected from phosphorylation by CaMKII, suggesting a possible role of CaMKII in regulating the dynamics of interaction between PCNA and RF-C and thus interfering in the formation of an active sliding clamp by DNA polymerases delta and epsilon (Maga, 1997).

Chronic pain due to nerve injury is resistant to current analgesics. Animal models of neuropathic pain show neuronal plasticity and behavioral reflex sensitization in the spinal cord that depends on the NMDA receptor. Complexes of NMDA receptors with the multivalent adaptor protein PSD-95 are found in the dorsal horn of spinal cord; PSD-95 plays a key role in neuropathic reflex sensitization. Mutant mice expressing a truncated form of the PSD-95 molecule fail to develop the NMDA receptor-dependent hyperalgesia and allodynia seen in the CCI model of neuropathic pain, but develop normal inflammatory nociceptive behavior following the injection of formalin. In wild-type mice following CCI, CaM kinase II inhibitors attenuate sensitization of behavioral reflexes; elevated constitutive (autophosphorylated) activity of CaM kinase II is detected in spinal cord, and increased amounts of phospho-Thr286 CaM kinase II coimmunoprecipitate with NMDA receptor NR2A/B subunits. Each of these changes is prevented in PSD-95 mutant mice although CaM kinase II is present and can be activated. Disruption of CaM kinase II docking to the NMDA receptor and activation may be responsible for the lack of neuropathic behavioral reflex sensitization in PSD-95 mutant mice (Garry, 2003).

Small conductance Ca2+-activated K+ channels (SK channels) couple the membrane potential to fluctuations in intracellular Ca2+ concentration in many types of cells. SK channels are gated by Ca2+ ions via calmodulin that is constitutively bound to the intracellular C terminus of the channels and serves as the Ca2+ sensor. In addition, the cytoplasmic N and C termini of the channel protein form a polyprotein complex with the catalytic and regulatory subunits of protein kinase CK2 and protein phosphatase 2A. Within this complex, CK2 phosphorylates calmodulin at threonine 80, reducing by 5-fold the apparent Ca2+ sensitivity and accelerating channel deactivation. The results show that native SK channels are polyprotein complexes and demonstrate that the balance between kinase and phosphatase activities within the protein complex shapes the hyperpolarizing response mediated by SK channels (Bildl, 2004).

The neural cell adhesion molecule (NCAM) regulates synapse formation and synaptic strength via mechanisms that have remained unknown. This study shows that NCAM associates with the postsynaptic spectrin-based scaffold, cross-linking NCAM with the NMDA receptor and Ca2+/calmodulin-dependent protein kinase II α (CaMKIIα) in a manner not firmly or directly linked to PSD95 and α-actinin. Clustering of NCAM promotes formation of detergent-insoluble complexes enriched in postsynaptic proteins and resembling postsynaptic densities. Disruption of the NCAM-spectrin complex decreases the size of postsynaptic densities and reduces synaptic targeting of NCAM-spectrin-associated postsynaptic proteins, including spectrin, NMDA receptors, and CaMKIIα. Degeneration of the spectrin scaffold in NCAM-deficient neurons results in an inability to recruit CaMKIIα to synapses after NMDA receptor activation, which is a critical process in NMDA receptor-dependent long-term potentiation. The combined observations indicate that NCAM promotes assembly of the spectrin-based postsynaptic signaling complex, which is required for activity-associated, long-lasting changes in synaptic strength. Its abnormal function may contribute to the etiology of neuropsychiatric disorders associated with mutations in or abnormal expression of NCAM (Sytayk, 2007).


Table of contents



CaM kinase II: Biological Overview | Evolutionary Homologs part 2/2 | Regulation | Developmental Biology | Effects of Mutation | References
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