Membrane association, localization and topology of rat inositol 1,4,5-trisphosphate 3-kinase B: implications for membrane traffic and Ca2+ homoeostasis

Soriano, Salvador; Thomas, Stephen G.; High, Stephen; Griffiths, Gareth; D’Santos, Clive S.; Cullen, Peter J.; Banting, George

doi:10.1042/bj3240579

Cited by 36 publications

(30 citation statements)

References 61 publications

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“…Other known proteins, which associate with the ER membranes, include e.g. inositol 1,4,5-trisphosphate 3-kinase (31), and tyrosine phosphatase PTP-1B (32). The association of the former also likely involves specific protein-protein interactions (31), whereas the association type of the latter is not known.…”

Section: Discussionmentioning

confidence: 99%

A Single C-terminal Peptide Segment Mediates Both Membrane Association and Localization of Lysyl Hydroxylase in the Endoplasmic Reticulum

Suokas¹,

Myllylä²,

Kellokumpu³

2000

Journal of Biological Chemistry

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Hydroxylation of lysyl residues is crucial for the unique glycosylation pattern found in collagens and for the mechanical strength of fully assembled extracellular collagen fibers. Hydroxylation is catalyzed in the lumen of the endoplasmic reticulum (ER) by a specific enzyme, lysyl hydroxylase (LH). The absence of the known ERspecific retrieval motifs in its primary structure and its association with the ER membranes in vivo have suggested that the enzyme is localized in the ER via a novel retention/retrieval mechanism. We have identified here a 40-amino acid C-terminal peptide segment of LH that is able to convert cathepsin D, normally a soluble lysosomal protease, into a membrane-associated protein.The same segment also markedly slows down the transport of the reporter protein from the ER into post-ER compartments, as assessed by our pulse-chase experiments. The retardation efficiency mediated by this Cterminal peptide segment is comparable with that of the intact LH but lower than that of the KDEL receptorbased retrieval mechanism. Within this 40-amino acid segment, the first 25 amino acids appear to be the most crucial ones in terms of membrane association and ER localization, because the last 15 C-terminal amino acids did not possess substantial retardation activity alone. Our findings thus define a short peptide segment very close to the extreme C terminus of LH as the only necessary determinant both for its membrane association and localization in the ER.

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Section: Discussionmentioning

confidence: 99%

A Single C-terminal Peptide Segment Mediates Both Membrane Association and Localization of Lysyl Hydroxylase in the Endoplasmic Reticulum

Suokas¹,

Myllylä²,

Kellokumpu³

2000

Journal of Biological Chemistry

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“…Animal IP3kins are the only inositol polyphosphate kinases thought to be regulated by calcium, both via direct interaction with calmodulin and by phosphorylation by calmodulin-dependent kinase II (CaMKII) (12)(13)(14). The B isoform of IP3kin, which is expressed in most cells and in glia in brain (5,15), is localized to internal membranes of the endoplasmic reticulum and Golgi apparatus, where it is poised to regulate IP 3 concentrations near calcium stores (16). In contrast, nothing is known about targeting mechanisms for isoform A in neurons.…”

Section: Inositol 145-trisphosphate (Ip 3 )mentioning

confidence: 99%

Inositol 1,4,5-Trisphosphate 3-Kinase A Associates with F-actin and Dendritic Spines via Its N Terminus

Schell¹,

Erneux²,

Irvine³

2001

Journal of Biological Chemistry

148

151

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The consequences of the rapid 3-phosphorylation of inositol 1,4,5-trisphosphate (IP 3 ) to produce inositol 1,3,4,5-tetrakisphosphate (IP 4 ) via the action of IP 3 3-kinases involve the control of calcium signals. Using green fluorescent protein constructs of full-length and truncated IP 3 3-kinase isoform A expressed in HeLa cells, COS-7 cells, and primary neuronal cultures, we have defined a novel N-terminal 66-amino acid F-actin-binding region that localizes the kinase to dendritic spines. The region is necessary and sufficient for binding Factin and consists of a proline-rich stretch followed by a predicted ␣-helix. We also localized endogenous IP 3 3-kinase A to the dendritic spines of pyramidal neurons in primary hippocampal cultures, where it is co-localized postsynaptically with calcium/calmodulin-dependent protein kinase II. Our experiments suggest a link between inositol phosphate metabolism, calcium signaling, and the actin cytoskeleton in dendritic spines. The phosphorylation of IP 3 in dendritic spines to produce IP 4 is likely to be important for modulating the compartmentalization of calcium at synapses.Inositol 1,4,5-trisphosphate (IP 3 ) 1 signals in neurons are terminated predominantly via the action of calcium-stimulated IP 3 3-kinases (IP3kins) (1). These enzymes produce 1,3,4,5-tetrakisphosphate (IP 4 ), which does not gate IP 3 receptor calcium channels and may have signaling properties of its own (2-4). Brain has more IP3kin activity than other tissues (5), and this is due to the concentration of the A isoform in the dendrites of principal neurons, such as cerebellar Purkinje cells, hippocampal CA1 pyramidal cells, and dentate gyrus granule cells (6 -8). Targeted disruption of IP3kin A isoform (IP3kinA) produces mice with enhanced long term potentiation but normal spatial learning (9). By contrast, injecting IP 4 into pyramidal neurons prior to tetanic stimulation strengthens the long term potentiation via a mechanism that involves the enhancement of voltage-activated calcium channels by IP 4 (10).IP3kins are members of the inositol polyphosphate kinase family, which consists of proteins sharing a conserved C-terminal catalytic region (4, 11). Animal IP3kins are the only inositol polyphosphate kinases thought to be regulated by calcium, both via direct interaction with calmodulin and by phosphorylation by calmodulin-dependent kinase II (CaMKII) (12)(13)(14). The B isoform of IP3kin, which is expressed in most cells and in glia in brain (5, 15), is localized to internal membranes of the endoplasmic reticulum and Golgi apparatus, where it is poised to regulate IP 3 concentrations near calcium stores (16). In contrast, nothing is known about targeting mechanisms for isoform A in neurons.Based on purification of the bovine and rat brain enzyme, IP3kinA activity and protein have been described as cytosolic (17)(18)(19), in contrast to type I 5-phosphatase that appears to be mostly membrane-bound (20). Immunocytochemical studies employing antibodies against the purified rat brain enzyme reveale...

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“…The specificity of Ins(1,4,5)P $ phosphorylation by recombinant Ins(1,4,5)P $ 3-kinases A and B at the 3-position of the inositol ring has been resolved by HPLC [17][18][19].…”

Section: Introductionmentioning

confidence: 99%

Cloning and expression of a cDNA encoding human inositol 1,4,5-trisphosphate 3-kinase C

Dewaste

Pouillon

Moreau

et al. 2000

Biochemical Journal

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Inositol 1,4,5-trisphosphate [Ins(1,4,5)P3] 3-kinase catalyses the phosphorylation of Ins(1,4,5)P3 to Ins(1,3,4,5)P4. cDNAs encoding two isoenzymes of Ins(1,4,5)P3 3-kinase (3-kinases A and B) have been described previously. In the present study, we report the cloning of a full-length 2052bp cDNA encoding a third human isoenzyme of the Ins(1,4,5)P3 3-kinase family, referred to as isoform C. This novel enzyme has a calculated molecular mass of 75.207kDa and a Km for Ins(1,4,5)P3 of 6µM. Northern-blot analysis showed the presence of a transcript of approx. 3.9kb in various human tissues. Inositol trisphosphate 3-kinase C demonstrates enzymic activity when expressed in DH5αF′ bacteria or COS-7 cells. Calcium alone decreases the Ins(1,4,5)P3 3-kinase activity of the 3-kinase C isoenzyme in transfected COS-7 cells. This inhibitory effect is reversed in the presence of calmodulin. The recombinant bacterial 3-kinase C can be adsorbed on calmodulin–Sepharose in the presence of calcium. The present data show that Ins(1,4,5)P3 3-kinase C: (i) shares a conserved catalytic domain of about 275 amino acids with the two other mammalian isoforms, (ii) could be purified on a calmodulin–Sepharose column and (iii) could be distinguished from the A and B isoenzymes by the effects of calcium and of calmodulin.

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Membrane association, localization and topology of rat inositol 1,4,5-trisphosphate 3-kinase B: implications for membrane traffic and Ca2+ homoeostasis

Cited by 36 publications

References 61 publications

A Single C-terminal Peptide Segment Mediates Both Membrane Association and Localization of Lysyl Hydroxylase in the Endoplasmic Reticulum

A Single C-terminal Peptide Segment Mediates Both Membrane Association and Localization of Lysyl Hydroxylase in the Endoplasmic Reticulum

Inositol 1,4,5-Trisphosphate 3-Kinase A Associates with F-actin and Dendritic Spines via Its N Terminus

Cloning and expression of a cDNA encoding human inositol 1,4,5-trisphosphate 3-kinase C

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