α-Actinin-dependent cytoskeletal anchorage is important for ICAM-5-mediated neuritic outgrowth

Nyman-Huttunen, Henrietta; Tian, Li; Lin, Ning; Gahmberg, Carl G.

doi:10.1242/jcs.03045

Cited by 30 publications

(35 citation statements)

References 53 publications

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“…2). In contrast, the binding affinity between TLCN and ␣-actinin was reported to be much lower by two orders of magnitude (K D of 22.9 M) (Nyman-Huttunen et al, 2006). These findings suggest that TLCN might use two types of actin-binding proteins, phospho-ERM and ␣-actinin, in distinct subcellular domains and for different functions: the stronger binding of TLCN with phospho-ERM may lead to the formation and elongation of dendritic filopodia, whereas weaker binding of TLCN with ␣-actinin at the soma and dendritic shafts might mediate the cell-substrate adhesion.…”

Section: Discussionmentioning

confidence: 93%

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Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Furutani

Matsuno²,

Kawasaki³

et al. 2007

J. Neurosci.

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Dendritic filopodia are long, thin, actin-rich, and dynamic protrusions that are thought to play a critical role as a precursor of spines during neural development. We reported previously that a telencephalon-specific cell adhesion molecule, telencephalin (TLCN) [intercellular adhesion molecule-5 (ICAM-5)], is highly expressed in dendritic filopodia, facilitates the filopodia formation, and slows spine maturation. Here we demonstrate that TLCN cytoplasmic region binds ERM (ezrin/radixin/moesin) family proteins that link membrane proteins to actin cytoskeleton. In cultured hippocampal neurons, phosphorylated active forms of ERM proteins are colocalized with TLCN in dendritic filopodia, whereas ␣-actinin, another binding partner of TLCN, is colocalized with TLCN at surface membranes of soma and dendritic shafts. Expression of constitutively active ezrin induces dendritic filopodia formation, whereas small interference RNA-mediated knockdown of ERM proteins decreases filopodia density and accelerates spine maturation. These results indicate the important role of TLCN-ERM interaction in the formation of dendritic filopodia, which leads to subsequent synaptogenesis and establishment of functional neural circuitry in the developing brain.

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Section: Discussionmentioning

confidence: 93%

“…Recently, Nyman-Huttunen et al (2006) reported an interaction between TLCN cytoplasmic region and another actinbinding protein, ␣-actinin. We made a detailed comparison of distribution patterns of ␣-actinin and phospho-ERM in cultured hippocampal neurons (Fig.…”

Section: Discussionmentioning

confidence: 99%

Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Furutani

Matsuno²,

Kawasaki³

et al. 2007

J. Neurosci.

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“…In the immune system, the receptor of ICAM-5 is the b2 integrin LFA-1 expressed on peripheral blood leukocytes and microglia (Tian et al, 1997;Mizuno et al, 1999;Tian et al, 2000a;Zhang et al, 2008;Ransohoff and Cardona, 2010). In the CNS, the roles of ICAM-5 in stimulating dendrite outgrowth, delaying spine maturation and increasing LTP have been extensively studied (Tian et al, 2000b;Nyman-Huttunen et al, 2006;Matsuno et al, 2006;Nakamura et al, 2001). Upon stimulation of NMDA receptors and MMP activation, ICAM-5 ectodomain cleavage is promoted, which induces spine maturation (Tian et al, 2007).…”

Section: Knockdown Of B1 Integrins In Axons Affects Synapse Formationmentioning

confidence: 99%

“…The stable neuronal cell lines, Paju-Neo, Paju-ICAM-5 and Paju-ICAM-5Dcp, were made as described earlier (Nyman-Huttunen et al, 2006). Cells were cultured in Dulbecco's modified Eagle's medium (DMEM) containing 10% fetal bovine serum (FBS) (Invitrogen), 1% penicillin-streptomycin, and 1% L-glutamine (Lonza Group Ltd, Switzerland), in the presence of 0.5 mg/ml G418 (Sigma-Aldrich).…”

Section: Cell Linesmentioning

confidence: 99%

“…Primary cultures of hippocampal neurons were prepared from C57Bl/6 mouse fetuses at gestational day 18 as previously described (Nyman-Huttunen et al, 2006). Dissociated neurons were counted and seeded on poly-L-lysine coated cell culture surfaces at the concentrations of 6610 4 /well for 24-well plates and 10 6 /well for 6-well plates.…”

Section: Primary Hippocampal Neuron Culturesmentioning

confidence: 99%

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Interactions between ICAM-5 and β1 integrins regulate neuronal synapse formation

Lin

Tian

Smirnov

et al. 2013

Journal of Cell Science

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SummaryIntercellular adhesion molecule-5 (ICAM-5) is a dendrite-specific adhesion molecule, which functions in both the immune and nervous systems. ICAM-5 is the only negative regulator that has been identified for maturation of dendritic spines so far. Shedding of the ICAM-5 ectodomain promotes spine maturation and enhances synaptic activity. However, the mechanism by which ICAM-5 regulates spine development remains poorly understood. In this study, we found that ablation of ICAM5 expression resulted in a significant increase in the formation of synaptic contacts and the frequency of miniature excitatory post-synaptic currents, an indicator of pre-synaptic release probability. Antibodies against ICAM-5 and b1 integrins altered spine maturation. Furthermore, we found that b1 integrins serve as binding partners for ICAM-5. b1 integrins were immunoprecipitated with ICAM-5 from mouse brain and the binding region in ICAM-5 was localized to the two first Ig domains. b1 integrins were juxtaposed to filopodia tips at the early stage of synaptic formation, but as synapses matured, b1 integrins covered the mushroom spines. Loss of b1 integrins from the pre-synaptic sites affected the morphology of the post-synaptic structures. ICAM-5 ectodomain cleavage decreased or increased when the interaction between ICAM-5 and b1 integrins was potentiated or weakened, respectively, using antibodies. These results suggest that the interaction between ICAM-5 and b1 integrins is important in formation of functional synapses.

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Subcellular localization of intercellular adhesion molecule‐5 (telencephalin) in the visual cortex is not developmentally regulated in the absence of matrix metalloproteinase‐9

Tremblay

Gahmberg

Tian

et al. 2013

J of Comparative Neurology

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The telencephalon-associated intercellular adhesion molecule 5 (Telencephalin; ICAM-5) regulates dendritic morphology in the developing brain. In vitro studies have shown that ICAM-5 is predominantly found within dendrites and immature dendritic protrusions, with reduced expression in mushroom spines, suggesting that ICAM-5 downregulation is critical for the maturation of synaptic structures. However, developmental expression of ICAM-5 has not been explored in depth at the ultrastructural level in intact brain tissue. To investigate the ultrastructural localization of ICAM-5 with transmission electron microscopy, we performed immunoperoxidase histochemistry for ICAM-5 in mouse visual cortex at postnatal day (P)14, a period of intense synaptogenesis, and at P28, when synapses mature. We observed the expected ICAM-5 expression in dendritic protrusions and shafts at both P14 and P28. ICAM-5 expression in these dendritic protrusions decreased in prevalence with developmental age to become predominantly localized to dendritic shafts by P28. To further understand the relationship between ICAM-5 and the endopeptidase metalloproteinase-9 (MMP-9), which mediates ICAM-5 cleavage following glutamate activation during postnatal development, we also explored ICAM-5 expression in MMP-9 null animals. This analysis revealed a similar expression of ICAM-5 in dendritic elements at P14 and P28; however an increased prevalence of ICAM-5 was noted in dendritic protrusions at P28 in the MMP-9 null animals, indicating that in the absence of MMP-9, there is no developmental shift in ICAM-5 subcellular localization. Our ultrastructural observations shed light on possible functions mediated by ICAM-5 and their regulation by extracellular proteases.

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α-Actinin-dependent cytoskeletal anchorage is important for ICAM-5-mediated neuritic outgrowth

Cited by 30 publications

References 53 publications

Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Interactions between ICAM-5 and β1 integrins regulate neuronal synapse formation

Subcellular localization of intercellular adhesion molecule‐5 (telencephalin) in the visual cortex is not developmentally regulated in the absence of matrix metalloproteinase‐9

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