Correspondence to Peter D. Yurchenco: yurchenc{at}umdnj.edu
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Introduction |
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A signature characteristic of Lms is their intimate association with select cell surfaces that accompany their ability to self-assemble into polymers (Yurchenco et al., 2004). Nerve Lms accumulate on the outer endoneurial surface of the SCs but not on axons, whereas mucosa Lms accumulate on epithelial but not fibroblast surfaces. Because Lms are required for BM assembly (Smyth et al., 1999), this selectivity of interaction determines where a BM can form and, therefore, which cells can be signaled by its ligands. A question that arises is whether there are cell-surface molecules that provide Lm anchorage, enabling cell-specific assembly and signaling.
Recent studies have implicated the Lm LG domains, and, in particular, their sulfated carbohydrate-binding loci, as providing cell anchorage (Li et al., 2002; Tsiper and Yurchenco, 2002). Although ß1-integrins and DG have been thought to play this important role, several genetic studies propose that neither receptor is necessary for assembly during development of peripheral nerve and other tissues (Feltri et al., 2002; Saito et al., 2003; Yurchenco et al., 2004). Alternatively, sulfated glycolipids such as the sulfatides might provide this function for two reasons. First, sulfatides can strongly bind to Lm LG domains (Roberts et al., 1985, 1986; Ishizuka, 1997). Second, the most common of these, HSO3-3galactosylß-1ceramide (gal-sulfatide), is highly expressed in developing and adult peripheral nerves (Mirsky et al., 1990).
In this study, we evaluated Lm-1 and -2 and gal-sulfatide in the peripheral nerve and their interactions in cultured SCs and fibroblasts. Sulfatide expression was found to precede that of Lms in the developing sciatic nerve, and SC gal-sulfatide was found to interact with Lm-1 and -2 with formation of a BM. Furthermore, intercalation of sulfatides into fibroblast plasma membranes rendered the cells competent for BM assembly. Lm assembly on both cell types initiated DG-dependent Src/Fyn activation and utrophin recruitment that contributed to their survival, and when cells were maintained in suspension, ß1-integrindependent FAK phosphorylation was also observed. Collectively, the data provide evidence that sulfatides are Lm anchors that enable BM self-assembly and the engagement and activation of integrin and DG receptors.
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Results |
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Sulfatides can be integrated (i.e., "loaded") into the outer leaflet of a plasma membrane by treating cells with sulfatide adsorbed onto de-lipidated serum albumin (Monti et al., 1992). Using this technique, intercalation of gal-sulfatide into the previously sulfatase-treated cells restored Lm accumulation (Fig. 2 f). Assembly of fibronectin, a glycoprotein with heparin-binding but little sulfatide-binding activity, was not affected by arylsulfatase (unpublished data).
The sulfatideLm interaction was also examined by biochemical means. SCs were loaded with 10 µM BODIPY-tagged gal-sulfatide as labeled and incubated with either Lm-1 or control 4-(2-aminoethyl)benzenesulfonyl fluoride (AEBSF)Lm-1 (10 µg/ml) for 1 h (Fig. 2 g). The cells were then extracted with 1% Triton X-100 and, after centrifugation, the lysate was immunoprecipitated with Lm E1'-specific antibody. Fluorescence was high for Lm-1 in contrast to that of the control nonpolymerizing Lm-1 or albumin, which was evidence for Lmsulfatide binding in the cells. Lm-1 and -2 were also found to accumulate on primary SCs isolated from 2-d-old rat sciatic nerve (not depicted).
The principle sulfatide-binding locus of Lm-1 has been found to reside within LG4 (Andac et al., 1999). Wild-type recombinant Lm-1 (rLm1; 10 µg/ml), but not Lm-1 with an LG1-5 deletion, accumulated and condensed on SCs (Fig. 2 h). Furthermore, when SCs were incubated with native Lm-1 (10 µg/ml) in the presence of either excess recombinant E3 (r1LG4-5; 100 µg/ml, 1 h) or a mutated recombinant E3 (mutant G;
1LG4-2791KRK2793 to 2791AAA2793) that binds poorly to sulfatide (Li et al., 2002), the wild-type E3 selectively blocked cell-surface accumulation of Lm. The expectation that Lm polymerization is important for BM assembly in SCs (Tsiper and Yurchenco, 2002) was supported by the observation that Lm-1 fragment E1' (but not AEBSF-inactivated E1') blocked accumulation of Lm.
BM assembly in fibroblasts
Fibroblasts produce several BM macromolecules but typically do not assemble BM on their cell surfaces, contributing their molecules instead to adjacent BMs (Cornbrooks et al., 1983; Marinkovich et al., 1993). We reasoned that fibroblasts may lack a molecule that anchors Lms to their surface. Mouse embryonic lung fibroblasts (MEFs) did not express detectable 1-Lm but secreted type IV collagen and nidogen-1 into the culture medium (determined by antibody immunofluorescence of detergent-permeabilized and nonpermeabilized cells with BM-specific antibodies and conditioned medium immunoblots). These cells were intercalated with sulfatides and evaluated for their ability to assemble a BM (Fig. 3). After incubation of untreated MEFs with Lm-1, little Lm or other BM component epitopes were detected on cell surfaces. However, if the MEFs were first loaded with gal-sulfatide, then the added Lm-1 accumulated on their surfaces (Fig. 3 a). Nidogen-1 and type IV collagen epitopes were also now detected on the exposed fibroblast surfaces. If the gal-sulfatidetreated MEFs were subsequently incubated with arylsulfatase and then incubated with Lm-1, Lm, then cell-surface nidogen and type IV collagen were not detected (Fig. 3 b).
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Effect of sulfatide on cell-surface ultrastructure
SCs and sulfatide-treated MEFs that were maintained in confluent cultures and incubated with Lm-1 were found to achieve maximal Lm surface immunostaining with 2040 µg/ml of protein, extending over almost the entire surface. The SCs and MEFs treated under these conditions were examined by transmission EM (Fig. 4). After incubation with Lm-1, nearly the entire SC surface was covered by a continuous BM deposit (lamina densa overlying a lamina lucida) that was absent in untreated cells or in cells treated with arylsulfatase. Sulfatide loading of the arylsulfatase-treated SCs restored the linear ECM deposit. The deposit was dependent primarily on Lm deposition rather than type IV collagen and was shown by incubating the SCs in the presence of Lm-1 and bacterial collagenase (which eliminated detectable type IV collagen immunostaining). MEFs had almost no extracellular deposits either without or with Lm-1 incubation. However, if cells were first loaded with sulfatide, and then treated with Lm-1, a continuous BM was noted in all sections examined. Treatment of the MEFs with arylsulfatase after sulfatide loading prevented the appearance of an ECM deposit on the exposed fibroblast plasma membrane.
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Sulfatide-treated fibroblasts were then evaluated for Src tyrosine phosphorylation (Fig. 7) in response to Lm-1. Lm-1 induced a similar transient activation of c-Src in sulfatide-loaded cells that was maximal at 1 h (Fig. 7 a). This was not observed if the fibroblasts were treated with Lm but not loaded with sulfatide (Fig. 7 b). Src phosphorylation was blocked partially by fragment E3 (as seen with SCs) and fully by the DG antibody IIH6, but not with antibody Ha2/5 to ß1-integrin or by Lm fragment E8 that possesses the 6ß1-integrinbinding locus (Fig. 7 c). To further examine the role of DG and ß1-integrin in Src activation, we evaluated cultures of fibroblasts isolated from differentiated mouse embryonic stem (ES) cells that were genetically null for DG or for ß1-integrin, and compared these with fibroblasts derived from wild-type ES cells or ones that were transfected with a construct to enable expression of ß1-integrin (ß1AGD25 cells; Wennerberg et al., 1996). The cells were cultured on plastic, loaded with gal-sulfatide, and incubated in the presence of Lm-1. Src activation was observed in response to Lm-1 in the wild-type, but not the DG-null, fibroblasts (Fig. 7 d). In contrast, Lm-1 stimulated an increased Src activation in both control and ß1-integrinnull fibroblasts, although at an approximately twofold higher level in the control cells (Fig. 7 e). Because ß1-integrin did not colocalize with Lm under these conditions, and because ß1-integrinblocking antibody Ha2/5 did not inhibit Lm-induced Src phosphorylation, it was thought likely that Src activation was primarily dependent on DG and that the integrin contribution was independent of Lm assembly. Lm-1 accumulated on both DG-null and ß1-integrinnull fibroblasts (Fig. 7, f and g). Finally, caveolin-1 became transiently phosphorylated at tyrosine-14 with a similar time course in fibroblasts, unlike SCs (Fig. 7 h). Inhibition of Src kinases with two structurally different inhibitors (PP2 and SU6656) inhibited caveolin-1 phosphorylation (Fig. 7 i), suggesting caveolin-1 was a downstream target of the Lm-activated Src.
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Discussion |
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Lm anchorage to sulfatides and BM assembly
Gal-sulfatide is a glycosphingolipid found in different tissues and enriched in the peripheral nerve. It, along with other sulfatides, binds to Lms (Roberts et al., 1985, 1986) through lysine- and arginine-rich sequences within the exposed loops of the fourth LG domain of Lm-1 and fourth and fifth domains of Lm-2 (Tisi et al., 2000; Wizemann et al., 2003). A study of Lm-1 interactions with synthetic sulfatide bilayers revealed that Lm polymerization facilitated binding through a cooperative interaction, leading to an aggregation of Lm on the lipid surface (Kalb and Engel, 1991) and providing the first evidence to implicate sulfatides in BM assembly. In this study on living SCs and fibroblasts, we found that the surface assembly of Lm-1 depended on Lm polymerization and anchorage to sulfatide through LG4, enabling the incorporation of nidogen-1 and type IV collagen into the Lm matrix. Analysis of the ultrastructure of confluent cultures revealed that a continuous BM, similar to that observed in the peripheral nerve, had formed in response to Lmsulfatide interactions.
We also found that rat kidneys possess gal-sulfatide that colocalizes with the Lm epitopes of tubular and other BMs in a polarized fashion (unpublished data), suggesting that a sulfatide-anchoring function is not confined to nerves. Nonetheless, we think it unlikely that gal-sulfatide provides universal Lm anchorage for two reasons. First, glc-sulfatide may similarly anchor Lms, and the finding that glc-sulfatide can replace gal-sulfatide may explain the presence of BMs in the gal-sulfatidenegative but glc-sulfatidepositive peripheral nerves of UDP-galactosyl transferase-null mice, which is a phenomenon that may also occur with ceramide sulfotransferase-null mice (Coetzee et al., 1996; Honke et al., 1996, 2002; Bosio et al., 1998). Second, we have found that the embryonic BM is sulfate dependent and arylsulfatase sensitive in the absence of detectable gal-sulfatide in developing embryoid bodies (unpublished data).
Recently, the LG4-5 domains of Lm-1 were deleted by gene targeting and studied in early embryos and embryoid bodies, where its absence was found to affect epiblast polarization without losing subendodermal BM (Scheele et al., 2005). Although Scheele et al. (2005) proposed that LG4-5 serves a signaling, rather than an assembling role, the concept of LG4 anchorage is supported by evidence that Lm-10 (5ß1
1) is also expressed in the embryonic BM and that inactivation of the Lam
1 gene does not prevent either BM assembly or failure of epiblast polarization caused by functional Lm redundancy (Miner et al., 2004). Thus, as a general mechanism, it may be that several sulfated glycolipids can provide Lm anchorage through different LG domains, whereas other acidic lipids lack this activity. A separate, unanswered question concerns which molecules anchor
3,
4, and
5-Lms.
DG and integrin-dependent signaling
The evidence of this and other studies (Smirnov et al., 2002; Yurchenco et al., 2004) demonstrates that the formation of BM on cell surfaces through anchorage, Lm polymerization, and the binding of other BM components to Lms is largely one of self-assembly. Cell signaling, on the other hand, requires the separate binding of receptors to the newly assembled BM. In this study, contributions mediated by DG and ß1-integrins of this type were observed. These receptors can transduce signals and lead to the association of the ECM with the actin cytoskeleton. Furthermore, they have shown that they become colocalized with the BM in the developing SC of the peripheral nerve (Previtali et al., 2003). In SCs and sulfatide-loaded fibroblasts, Lm sulfatide-mediated assembly triggered the phosphorylation of c-Src at its activating tyrosine 416, and this was accompanied by Fyn phosphorylation (a known mediator of myelination in the central nervous system; Umemori et al., 1999). Src activation was inhibited by an antibody that blocks the binding of Lm, perlecan, and agrin to -DG, implicating DG in Src activation. The resulting activated Src was detected in the nucleus, suggesting that Src is translocated to the nucleus from the plasma membrane. A corresponding nuclear distribution of activated Src was seen in the developing sciatic nerve, a phenomenon which was also found after calcium-induced keratinocyte differentiation (Zhao et al., 1992). Lm assembly in sulfatide-treated fibroblasts similarly led to transient Src activation, which was accompanied by downstream phosphorylation of caveolin-1. Antibody binding to
-DG inhibited the Lm-initiated response, and sulfatide-loaded fibroblasts that were null for DG were unable to activate Src in response to Lm-1, suggesting that DG was the primary receptor that mediated Src activation in both SCs and fibroblasts. The finding that Src activation was associated with the promotion of Lm-dependent cell survival leads one to expect that if the DGSrc pathway is a major mediator of cell survival, then reduced Src family activation and increased apoptosis might be seen in DG-null peripheral nerve SCs (Saito et al., 2003).
ß1-integrins, like DG, were not required for Lm assembly on sulfatide-containing cell surfaces. On the other hand, their Lm-initiated signaling, a prediction given their role (especially 6ß1) in peripheral nerve radial sorting (Feltri et al., 2002), was appreciated under suspension culture conditions. In particular, Lm-1 colocalized with ß1-integrins and induced tyrosine phosphorylation of FAK.
A working hypothesis
The evidence from both SCs and sulfatide-treated fibroblasts constitutes the first demonstration of a critical mediator of Lm anchorage (Fig. 10). Interpreting the new cell findings in the context of the biophysical evidence (Kalb and Engel, 1991; Yurchenco and Cheng, 1993), we propose that sulfated glycolipids such as gal-sulfatide facilitate Lm polymerization by specifically binding to the LmLG domains and increasing the local Lm concentration at the cell surface. This initial ECM then binds to nidogens, type IV collagens, and other BM components to complete BM assembly. Signaling functions, on the other hand, are reserved for transmembrane protein receptors whose binding to the Lm scaffolding and/or attached BM components is enabled by anchorage and Lm polymerization. Two receptor classes implicated in SCs, and mirrored in the sulfatide-loaded fibroblasts, are DG and ß1-integrins. The signals detected in response to DG and integrin were c-Src/Fyn and FAK tyrosine phosphorylation, respectively; the former is implicated in protecting the cells from apoptosis. In addition, utrophin, which can bind to both ß-DG and F-actin, was recruited to the BM zone in a step that required DG and its ECM interaction. Thus, BM assembly consists of its self-assembly, initiated by Lm polymerization and anchorage through sulfated glycolipids, and its signal transduction, which is enabled by assembly and is mediated through integrin and DG receptor interactions.
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Materials and methods |
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The 9,564-bp fragment coding for mouse Lm-1 (Yurchenco et al., 1997) with an NH2-terminal FLAG tag and BM40 signal sequence was excised from ma1-pRCX3 and subcloned into the pcDNA3.1 vector. A construct for mouse Lm-
1 without a G domain was made by replacing a 3,928-bp SacIIAflII fragment of the full-length
1 construct with an analogous 1,091-bp PCR fragment, which introduces a STOP codon after the sequence SIKVAVSADRD. The human ß1 chain with an NH2-terminal hemagglutin tag was subcloned into pcDNA3.1/zeo+ vector (Invitrogen) from a pCIS vector containing human Lm-ß1 (Yurchenco et al., 1997). The human Lm-
1 construct was made as described previously (Smirnov et al., 2002). HEK 293 cells were transfected with the expression constructs. Recombinant wild-type E3 and E3 with the sulfatide-DGbinding site KRK in LG4 that was replaced with AAA (mutant G) were also expressed in HEK 293 cells. Recombinant Lm-1 and fragments were purified by FLAG affinity chromatography. FLAG-tagged recombinant human Lm-2 was expressed and purified as described previously (Smirnov et al., 2002). cDNA for malarial CS protein was obtained from the Malaria Research and Reference Reagent Resource Center. Recombinant CS protein with a 6x His-tag was expressed in Escherichia coli M15 and purified to homogeneity by metal chelation affinity chromatography (QIAGEN).
Antibodies were used with the following specificities: rG50 (Lm-1LG domains 45) rabbit polyclonal pAb, Lm-
2G, Lm2/4 (which reacts with
2 and
1 subunits), and nidogen-1 pAbs (Cheng et al., 1997; Li et al., 2002), Lm-
1 rat mAb (Upstate Biotechnology), ß1-integrin hamster mAb Ha2/5 (BD PharMingen),
-DG mouse mAb IIH6 (gift of K. Campbell, University of Iowa, Iowa City, IA), purified gal-sulfatide mAb Sulf I (a gift of P. Fredman, Sahlgreuska University Hospital, Mölndal, Sweden; Fredman et al., 1988), utrophin mAb (DRP2; Novocastra), S100 mAb (Chemicon), rabbit collagen type IV pAb (Rockland Immunochemicals), rabbit-cleaved caspase-3 pAb (Cell Signaling Technology), NFL200 pAb and NFL160 mAb (Sigma-Aldrich), myelin basic protein mAb (Sternberger Monoclonals), rabbit c-Src pAb (Santa Cruz Biotechnology, Inc.), rabbit c-Src-Py416 pAb (which cross-reacts with activated Fyn; Cell Signaling Technology), caveolin-1-Py14 pAb (BD Biosciences), caveolin-1 pAb, and Fyn mAb (Sigma-Aldrich).
Cell culturing and sulfatide loading of plasma membranes
SCs isolated from sciatic nerves were maintained as described previously (Tsiper and Yurchenco, 2002), used between passages 25 and 35, and plated onto 22-mm2 glass coverslips in 6-well dishes 1 d before protein treatments. Primary SCs were isolated from neonatal rat sciatic nerves as described previously (Carey and Stahl, 1990), cultured on polylysine-coated glass coverslips in DME containing 10% FBS (D/F), and used 4 d after isolation. MEFs, provided by Margaret Schwarz (Robert W. Johnson Medical School), were cultured in D/F and used between passages 3 and 5. ß1-integrinnull fibroblasts (GD25) and control ß1AGD25 cells (provided by Reinhardt Fässler, Max Planck Institute, Martinsreid, Germany; Wennerberg et al., 1996) were cultured in D/F. DG-null and control wild-type fibroblasts were derived from 10-d-old embryoid bodies cultured from DG-null and wild-type R1 ES cells (Li et al., 2002). The embryoid bodies were digested with trypsin-EDTA, and dissociated cells were plated in bacteriological petri dishes. Cells with fibroblast morphology were enriched by selective trypsinization and panning on collagen Icoated dishes.
Confluent cells were trypsinized and cultured in 100-mm dishes coated with poly-HEMA (Sigma-Aldrich) for 24 h in D/F. Cell aggregates were allowed to settle by gravity, washed once in PBS, and replated onto poly-HEMAcoated dishes in serum-free or serum-containing medium.
SulfatideBSA complex was prepared as previously described (Viani et al.,1989; Monti et al., 1992). Gal-sulfatide (Avanti Polar Lipids, Inc.), glc-sulfatide (provided by Ineo Ishizuka, Teikyo University, Tokyo, Japan), or BSA-BODIPY-gal-sulfatide (Watanabe et al., 1999) dissolved in chloroform/methanol (1:1 [vol/vol]) was evaporated under a stream of argon, reconstituted in DMSO, and heated at 60°C for 10 min. Sulfatides were then mixed with an equal mole of de-lipidated BSA in PBS, pH 7.4, and incubated at 37°C for 20 min. The sulfatideBSA complex was diluted (mM) with serum-free DME and added to cells for 30 min (final, 10 mM). Cells were then rinsed three times with PBS and used immediately for experiments.
Fluorescence microscopy
Cells that were grown on glass coverslips were rinsed with PBS and fixed in 3% PFA for 30 min. Suspended cell aggregates were collected by sedimentation, washed with PBS, fixed in 3% PFA, embedded in optimal cutting temperature compound (Tissue-Tek), and sectioned on a cryostat. Cells were permeabilized with 0.1% Triton X-100 in PBS for 5 min on ice when staining of intracellular epitopes was desired. For detection of surface-bound antigens, the detergent step was omitted. Slides were blocked with 5% goat serum and stained with primary and appropriate secondary antibodies conjugated with FITC, Cy3, or Cy5 (Jackson ImmunoResearch Laboratories). Control staining was performed using preimmune IgG or IgM. Slides were nuclear counterstained with DAPI. Immunofluorescence and phase microscopy were performed on an inverted microscope (model IX70; Olympus) with IX-FLA fluorescence and CCD camera, and the data were collected and analyzed in IPLab v.3.52 as described previously (Li et al., 2002).
Electron microscopy
Cells were plated in 60-mm Permanox dishes (Nunc) 2 d before the experiment. H. promatia arylsulfatase (Sigma-Aldrich) or bacterial collagenase (CLS; Worthington) were added to cell cultures 30 min before the addition of 2040 µg/ml Lm-1. Cells adherent to plastic were embedded, sectioned, stained, and imaged with an electron microscope (model JEM-1200EX; JEOL USA) as described previously (Tsiper and Yurchenco, 2002). The degree of BM coverage was determined as the ratio of measured length of continuous ECM present divided by the total measured length of exposed cell surface in random cross sections cut at different depths within the Epon block.
Immunoprecipitation and immunoblotting
Cells were washed with cold PBS and disrupted in lysis buffer (50 mM Tris, pH 7.4, 100 mM NaCl, 0.5 mM EDTA, 1% Triton X-100, 1% SDS, and protease and phosphatase inhibitor cocktails [diluted 1:10 and 1:100, respectively, with lysis buffer; Sigma-Aldrich]). Immunoprecipitation was performed with SDS removed from the lysis buffer (Li et al., 2002). Equal amounts of proteins were separated by SDS-PAGE on 12% (caveolin-1), 8% (c-Src), or 6% (utrophin) gels under reducing conditions. Proteins were transferred to polyvinylidene difluoride membranes, blocked, and incubated with primary antibodies followed by HRP-conjugated secondary antibodies (Pierce Chemical Co.). Blots were developed with ECL reagents. Band intensities were quantified from the membrane or scanned films using Quantity 1 software after data acquisition with a gel documentation system (model ChemiDoc XRS; Bio-Rad Laboratories).
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Acknowledgments |
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This study was supported by National Institutes of Health grants R01-NS38469 and DK36425.
Submitted: 19 January 2005
Accepted: 1 March 2005
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