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The Journal of Immunology, 2002, 169: 5410-5414.
Copyright © 2002 by The American Association of Immunologists

Cutting Edge

Cutting Edge: Association of the Motor Protein Nonmuscle Myosin Heavy Chain-IIA with the C Terminus of the Chemokine Receptor CXCR4 in T Lymphocytes1

Mercedes Rey*, Miguel Vicente-Manzanares*, Fernando Viedma*, María Yáñez-Mó*, Ana Urzainqui*, Olga Barreiro*, Jesús Vázquez{dagger} and Francisco Sánchez-Madrid2,*

* Servicio de Inmunología, Hospital de la Princesa, Universidad Autónoma de Madrid, and {dagger} Centro de Biología Molecular Severo Ochoa, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 References
 
The binding of chemokines to their receptors guides lymphocyte migration. However, the precise mechanism that links the chemotactic signals with the energy and traction force generated by the actomyosin complex of the cell has not been elucidated. Using biochemical approaches and mass spectrometry analysis, we found an association between the C-termini of CXCR4 and CCR5 and the motor protein nonmuscle myosin H chain-IIA. Immunoprecipitation experiments revealed that this association also occurs between the endogenous molecules in T lymphocytes. As expected, myosin L chain was also associated with CXCR4. Confocal microscopy analysis showed that CXCR4 and motor protein nonmuscle myosin H chain-IIA colocalize at the leading edge of migrating T lymphocytes, together with filamentous actin and myosin L chain. These results provide the first evidence of a biochemical association between chemokine receptors and motor proteins, a mechanosignaling mechanism that may have a key role in lymphocyte migration.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 References
 
Chemokines have a very important role in inflammation and the generation of the immune response. These cytokines bind to G protein-coupled receptors, triggering different signaling cascades, including activation of Gi proteins, phosphatidylinositol 3-kinase, Janus kinase/STAT proteins, the mitogen-activated protein kinase pathway, and the Rho-p160 ROCK axis (1, 2, 3, 4, 5). However, the intracellular signals regulating lymphocyte polarization and chemotaxis are still largely unknown.

Nonmuscle myosin II is a motor protein present in all cell types; there are at least two distinct isoforms, IIA and IIB, which are encoded by genes located in different chromosomes (6). Nonmuscle myosins are heterohexamers composed of a pair of H chains and two pairs of L chains. Each H chain contains a globular region at the N terminus that catalyzes ATP hydrolysis and binds to actin, and an {alpha}-helical C-terminal tail region, responsible for the formation of an extended parallel-coiled coil and the assembly of bipolar myosin filaments (7, 8). The two isoforms of nonmuscle myosin H chain (NMMHC)3-II show distinct patterns of intracellular localization and biological properties (9, 10, 11). However, the specific functional roles of these NMMHC-II isoforms at a cellular level are not well known.

The aim of this study was to determine the cytoskeletal molecules that interact with the C-termini of chemokine receptors. Using biochemical approaches, we found an association between the motor protein NMMHC-IIA and the C-termini of CXCR4 and CCR5. This interaction also occurred in intact cells, and the association was also found for the myosin L chain (MLC). Finally, the colocalization of NMMHC-IIA, CXCR4, MLC, and filamentous actin (F-actin) at the leading edge of polarized migrating T lymphocytes suggests that these receptor-motor protein complexes have a key role in cell chemotaxis.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 References
 
Cells, cell lines, Abs, and reagents

Peer {gamma}{delta} CD3+ and Jurkat human T cell lines were grown in RPMI 1640 (Flow Laboratories, Irvine, U.K.) with 10% FCS. PBLs were obtained as described (2).

The affinity-purified polyclonal anti-NMMHC-IIA was a kind gift of Drs. R. S. Adelstein and Q. Wei (National Institutes of Health, Bethesda, MD). Rabbit polyclonal Ab against CD69 and mAb TP1/24 anti-ICAM-3 have been described elsewhere (12, 13). Rabbit polyclonal Ab anti-CXCR4 and mAb MY-21 anti-MLC were from Sigma-Aldrich (St. Louis, MO). Recombinant human stromal-derived factor-1{alpha} (SDF-1{alpha}) was purchased from R&D Systems (Minneapolis, MN).

GST preparation and pull-down assays

GST fusion proteins were prepared by PCR amplification of the C-termini of the chemokine receptors CXCR4 and CCR5, and subcloning of these PCR products into EcoRI and XhoI sites in PGEX-4T-2 vector (Amersham Pharmacia Biotech, Uppsala, Sweden). Primers used were: forward primer, 5'-CCGGGAATTGCCAAATTTAAAACC-3', reverse primer, 5'-CCGCTCGAGTTAGCTGGAGTGAAA-3' (for CXCR4); and forward primer, 5'-CCGGGAATTGAGAAGTTCAGAAAC-3', reverse primer, 5'-CCGCTCGAGTCACAAGCCCACAGA-3' (for CCR5). The ICAM-3 cytoplasmic region GST-fusion protein, and the GST production method have been previously described (14).

For pull-down assays, 108 cells were lysed in lysis buffer containing TBS, 1% Nonidet P-40 (Boehringer Mannheim, Germany), and COMPLETE protease inhibitor mixture (Roche, Mannheim, Germany), and centrifuged at 15,000 x g for 15 min at 4°C. The supernatant was incubated twice with GST for 2 h, and then overnight with GST, GST-ICAM-3cytoplasmic (cyt), GST-CXCR4cyt, or GST-CCR5cyt, respectively. Then, glutathione-coupled Sepharose beads were washed twice with lysis buffer, once with lysis buffer plus 0.1% SDS, and once with lysis buffer plus 0.5 M NaCl, and resuspended in Laemmli buffer. Samples were separated in SDS-PAGE gels and processed to mass spectrometry techniques, or transferred to a nitrocellulose membrane for immunoblot analysis with an Ab against NMMHC-IIA, respectively.

"In gel" digestion of proteins, peptide extraction, and mass spectrometry analysis

A total of 10% SDS-PAGE gels were stained with Gelcode Blue Stain Reagent (Pierce, Rockford, IL), and the bands of interest excised and subjected to in situ digestion with trypsin as described (15). A small aliquot (0.5 µl) of the extract was taken up and analyzed by matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry, as described (16).

Immunoprecipitation and Western blot

Normal lymphocytes (2 x 107) were stimulated with 10 nM SDF-1{alpha} for the indicated times under continuous shaking before being washed twice in cold PBS. Then, cells were lysed in lysis buffer (TBS, 1% Nonidet P-40, 1 mM Cl2 Mg) for 30 min at 4°C and centrifuged (15,000 x g for 15 min). Protein extracts precleared by incubation with protein A-Sepharose were immunoprecipitated with the anti-CXCR4 or anti-CD69 polyclonal Abs conjugated to protein A-Sepharose (5 µg Ab per sample, overnight at 4°C). Sepharose pellets were washed twice with lysis buffer and three times with 50 mM Tris-HCl, pH 7 (15000 x g for 1 min at 4°C) and resuspended in Laemmli buffer.

Samples were separated in a SDS-6% PAGE, transferred to a nitrocellulose membrane (Bio-Rad, Hercules, CA), and incubated with Abs to NMMHC II-A, CXCR4, or MLC at 4°C overnight. Then, membranes were incubated with a peroxidase-conjugated secondary Ab (Pierce) at room temperature for 1 h, and proteins were visualized using a SuperSignal West Pico Luminol/Enhancer solution (Pierce).

Immunofluorescence studies

PBLs (2 x 106) in 500 µl complete medium were allowed to adhere at 37°C, 30 min to coverslips coated with 50 µg/ml human fibronectin (Sigma-Aldrich, St. Louis, MO), and then fixed in 2% formaldehyde in PBS for 10 min at room temperature. CXCR4 was visualized with a biotinylated anti-CXCR4 mAb (BD PharMingen, San Diego, CA) plus a biotinylated anti-mouse Ab (Amersham Pharmacia Biotech and Molecular Probes, Eugene, OR) and Rhodamine X-labeled streptavidin (Molecular Probes). For NMMHC-IIA, MLC, and actin staining, cells were permeabilized by incubation for 10 min at room temperature with FACS lysing solution (BD Biosciences, San Jose, CA) and then appropriate primary and secondary Abs or Alexa 568-phalloidin (Molecular Probes) were used. Images were acquired with a Leica TCS-SP (Leica Microsystems, Heidelberg, Germany) confocal microscope.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
References
 
To identify intracellular ligands of CXCR4 and CCR5, GST fusion proteins containing the C-termini of the chemokine receptors CXCR4 and CCR5 were generated (Fig. 1GoA). Pull-down assays with cell lysates of Peer T lymphocytes (Fig. 1GoB) revealed the presence of protein bands of 40 (spots A and B) and 230 kDa (spots X and Y) that were specifically associated to CXCR4 and CCR5. These polypeptides were absent in GST and GST-ICAM-3-C terminus precipitates used as controls (Fig. 1GoB). To identify the proteins corresponding to the spots X and Y (230 kDa), the bands were excised, digested with trypsin, and the peptides were analyzed by mass spectrometry (Fig. 1GoC). The 230-kDa band was unequivocally identified as NMMHC-IIA by both peptide mass fingerprinting (Fig. 1GoC) and MS/MS analysis of some of the peptides (Fig. 1GoD). Similarly, bands A and B were identified as actin, both by fingerprinting and MS/MS analysis and also by Western blot (data not shown).



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  		FIGURE 1. Identification of NMMHC-IIA as a protein associated to the C termini of CXCR4 and CCR5 by mass spectrometry analysis. A, GST-fusion proteins including the C termini of chemokine receptors CXCR4 and CCR5 and the adhesion molecule ICAM-3. B, GST-fusion proteins incubated with Peer T cell lysates as indicated. Specific bands of 230 kDa (spots X and Y) and 40 kDa (spots A and B) appear in the precipitates corresponding to chemokine receptors, but not in those of GST alone or GST-ICAM-3. C and D, Identification of the 230-kDa bands by mass spectrometry. C, MALDI-TOF mass-map of peptides obtained after in gel digestion with trypsin. Peptides whose mass corresponds to a tryptic peptide of NMMHC-IIA are labeled with a {blacktriangleup}. D, Sequencing of one of the peptides from NMMHC-IIA by nanospray-ion trap tandem mass espectrometry. The fragment MS/MS spectrum from the ion specie at m/z 578.0 (M + 2H'), which corresponds to the peptide at m/z 1155.0 (M + H') in the MALDI-TOF spectrum is shown. In the area labeled x5, the scale was expanded five times relative to the y-axis. The assigned peptide sequence is indicated, detailing the observed backbone fragment ions (34 ).

 
To confirm the identity of the 230-kDa protein, Western blot analysis with an Ab against NMMHC-IIA was performed in Peer T cells (Fig. 2GoA) and PBL (Fig. 2GoB) lysates pulled-down with GST-CXCR4-Ct. This protein was specifically recognized by the anti-NMMHC-IIA Ab. Furthermore, immunoprecipitation assays confirmed the association between the endogenous motor protein and chemokine receptor in T lymphocytes (Fig. 2GoCa). Likewise, MLC also coimmunoprecipitated with the CXCR4-NMMHC-IIA complex (Fig. 2GoCb). These associations seemed to be constitutive, since addition of SDF-1{alpha}, the ligand of CXCR4, did not apparently modify the association of CXCR4 with NMMHC-IIA at any time points studied (Fig. 2GoD).



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  		FIGURE 2. Western blot analysis of CXCR4-NMMHC-IIA association. Peer T cell lysates (A) or PBL lysates (B) were pulled-down with GST and GST-CXCR4Ct and analyzed by Western blot. SDS-PAGE gels (10%) were used in all cases. Coomassie blue staining is shown. C, Jurkat T cells lysed, immunoprecipitated with Abs against CXCR4 and CD69, and revealed for NMMHC-IIA (a), MLC (b), and CXCR4 (c) by Western blot. D, Cells pulsed for the different times with 10 nM SDF-1{alpha}. The association between CXCR4 and NMMHC-IIA was assessed as in C.

 
The chemokine receptor CXCR4 and MLC have been shown to localize at the leading edge of motile lymphocytes (5, 17), where they are supposed to guide F-actin polymerization and contractility. Therefore, we have assessed the subcellular localization of NMMHC-IIA, CXCR4, MLC, and the actin cytoskeleton in migrating polarized lymphocytes using confocal microscopy. We found a clear-cut colocalization pattern of NMMHCIIA and F-actin (Fig. 3GoA), and also with CXCR4 (Fig. 3GoB) at the leading edge of migrating T lymphocytes. Likewise, NMMHC-IIA and MLC also colocalized at the advancing front of migrating T lymphocytes (Fig. 3GoC). We used ICAM-3 staining as a control of the trailing edge (uropod) of the cell (12), and we found that NMMHC-IIA was localized at the opposite pole from that stained by ICAM-3 (Fig. 3GoD and sideview).



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  		FIGURE 3. Colocalization of NMMHC-IIA, CXCR4, MLC, and F-actin at the leading edge of migrating T lymphocytes. Confocal microscopy images of SDF-1{alpha}-treated PBLs for inducing polarization are shown. Cells were stained with Abs against NMMHC-IIA (green) in all cases, and in red Alexa 568-phalloidin (A), CXCR4 (B), MLC (C), and ICAM-3 (D). Colocalization histograms are shown at the right side for each case. A three-dimensional reconstruction is also shown for D.

 
NMMHC-IIA is one of the two different isoforms of the H chain of type II myosin in nonmuscular cells. Although these two isoforms were described long ago (18), their specific functional roles remain controversial and poorly understood. It has been postulated that both proteins are functionally redundant, although with different efficiency given their different features, e.g., their velocity of movement into the cell (11). Nevertheless, their distinct subcellular localization and different enzymatic kinetics suggest specific functions for each isoform (19, 20). Interestingly, the localization of NMMHC-IIA in polarized migrating T cells differs from that of the isoform IIB, located at the uropod base (12). The latter isoform has been implicated in cerebellar and heart development (21, 22, 23), and in other processes like growth cone motility (24). In contrast, the isoform IIA has been implicated in the control of cell shape and the formation of focal adhesions in HeLa cells (25). Nevertheless, the specific functions of each isoform remain far from defined, as well as the specific signaling pathways in which these proteins are involved.

In this work, we show an association between the C terminus of the chemokine receptor CXCR4 and NMMHC-IIA at the leading edge of T lymphocytes. These data provide for the first time evidence of a connection between chemokine signaling machinery and the contractile forces generated by the cell actomyosin system. A proteomic approach led us to the identification of NMMHC-IIA as the 230-kDa protein that specifically binds to the C-termini tail of chemokine receptors. The association between the receptor and motor protein was further demonstrated by coprecipitation experiments of endogenous molecules in T cells. The association seems to be constitutive, as it is not apparently modified by the addition of SDF-1{alpha}, the ligand of CXCR4. Moreover, the CXCR4-NMMHC-IIA complex also contains the MLC. In addition, we have also found an association between the C-termini of the chemokine receptors and F-actin, in agreement with previous reports on the association between heptahelical receptors and actin (26, 27). The fact that this interaction between motor proteins and chemokine receptors occurs in intact cells, together with the colocalization of these proteins at the leading edge of migrating T lymphocytes, suggest that this phenomenon has an important functional role in cell migration, likely by translating the signal initiated by the chemokine into energy provided by the actomyosin complex. Thus, this association could be the key linkage between chemokines and cell movement.

The involvement of myosin II in cell movement has been assessed previously in different works (28, 29, 30). In addition, this motor protein participates in the redistribution of adhesion receptors toward the immunological synapse (31). Furthermore, previous studies in the amoeba Dictyostelium discoideum have suggested that the H chain of myosin II is involved in processes such as the tuning of pseudopod formation and chemotaxis, as a result of the fine regulation of other processes (32, 33). Finally, our results demonstrating a novel association between a chemotactic receptor and myosin point to a key functional role of this mechanotransducing complex in the directional migration of immune cells.


   Footnotes
 
1 This work was supported by Grants BMC02-00563 and European Community QLRT-1999-010-36 (to F.S.-M.). Back

2 Address correspondence and reprint requests to Dr. Francisco Sánchez-Madrid, Servicio de Inmunología, Hospital de la Princesa, c/Diego de León, 62, E-28006 Madrid, Spain. E-mail address: fsanchez{at}hlpr.insalud.es Back

3 Abbreviations used in this paper: NMMHC, nonmuscle myosin H chain; SDF-1{alpha}, stromal-derived factor-1{alpha}; MLC, myosin L chain; F-actin, filamentous actin; cyt, cytoplasmic; MALDI-TOF, matrix-assisted laser desorption ionization-time of flight. Back

Received for publication July 12, 2002. Accepted for publication September 20, 2002.


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 Introduction
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 References
 

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