JAM-A interacts with α3β1 integrin and tetraspanins CD151 and CD9 to regulate collective cell migration of polarized epithelial cells

doi:10.1007/s00018-022-04140-5

. 2022 Jan 24;79(2):88.

doi: 10.1007/s00018-022-04140-5.

JAM-A interacts with α3β1 integrin and tetraspanins CD151 and CD9 to regulate collective cell migration of polarized epithelial cells

Sonja Thölmann^{1

2}, Jochen Seebach^{3

4}, Tetsuhisa Otani⁵, Luise Florin⁶, Hans Schnittler^{3

4}, Volker Gerke^{2

4}, Mikio Furuse⁵, Klaus Ebnet^{7

8

9}

Affiliations

¹ Institute-Associated Research Group "Cell Adhesion and Cell Polarity", Institute of Medical Biochemistry, ZMBE, University of Münster, Von-Esmarch-Str. 56, 48149, Münster, Germany.
² Institute of Medical Biochemistry, ZMBE, University of Münster, Münster, Germany.
³ Institute of Anatomy and Vascular Biology, University of Münster, Münster, Germany.
⁴ Cells-in-Motion Interfaculty Center, University of Münster, 48149, Münster, Germany.
⁵ Division of Cell Structure, National Institute for Physiological Sciences, National Institute of Natural Sciences, Okazaki, Aichi, Japan.
⁶ Institute for Virology and Research Center for Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany.
⁷ Institute-Associated Research Group "Cell Adhesion and Cell Polarity", Institute of Medical Biochemistry, ZMBE, University of Münster, Von-Esmarch-Str. 56, 48149, Münster, Germany. ebnetk@uni-muenster.de.
⁸ Institute of Medical Biochemistry, ZMBE, University of Münster, Münster, Germany. ebnetk@uni-muenster.de.
⁹ Cells-in-Motion Interfaculty Center, University of Münster, 48149, Münster, Germany. ebnetk@uni-muenster.de.

PMID: 35067832
PMCID: PMC8784505
DOI: 10.1007/s00018-022-04140-5

JAM-A interacts with α3β1 integrin and tetraspanins CD151 and CD9 to regulate collective cell migration of polarized epithelial cells

Sonja Thölmann et al. Cell Mol Life Sci. 2022.

. 2022 Jan 24;79(2):88.

doi: 10.1007/s00018-022-04140-5.

Authors

Sonja Thölmann^{1

2}, Jochen Seebach^{3

4}, Tetsuhisa Otani⁵, Luise Florin⁶, Hans Schnittler^{3

4}, Volker Gerke^{2

4}, Mikio Furuse⁵, Klaus Ebnet^{7

8

9}

Affiliations

¹ Institute-Associated Research Group "Cell Adhesion and Cell Polarity", Institute of Medical Biochemistry, ZMBE, University of Münster, Von-Esmarch-Str. 56, 48149, Münster, Germany.
² Institute of Medical Biochemistry, ZMBE, University of Münster, Münster, Germany.
³ Institute of Anatomy and Vascular Biology, University of Münster, Münster, Germany.
⁴ Cells-in-Motion Interfaculty Center, University of Münster, 48149, Münster, Germany.
⁵ Division of Cell Structure, National Institute for Physiological Sciences, National Institute of Natural Sciences, Okazaki, Aichi, Japan.
⁶ Institute for Virology and Research Center for Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany.
⁷ Institute-Associated Research Group "Cell Adhesion and Cell Polarity", Institute of Medical Biochemistry, ZMBE, University of Münster, Von-Esmarch-Str. 56, 48149, Münster, Germany. ebnetk@uni-muenster.de.
⁸ Institute of Medical Biochemistry, ZMBE, University of Münster, Münster, Germany. ebnetk@uni-muenster.de.
⁹ Cells-in-Motion Interfaculty Center, University of Münster, 48149, Münster, Germany. ebnetk@uni-muenster.de.

PMID: 35067832
PMCID: PMC8784505
DOI: 10.1007/s00018-022-04140-5

Abstract

Junctional adhesion molecule (JAM)-A is a cell adhesion receptor localized at epithelial cell-cell contacts with enrichment at the tight junctions. Its role during cell-cell contact formation and epithelial barrier formation has intensively been studied. In contrast, its role during collective cell migration is largely unexplored. Here, we show that JAM-A regulates collective cell migration of polarized epithelial cells. Depletion of JAM-A in MDCK cells enhances the motility of singly migrating cells but reduces cell motility of cells embedded in a collective by impairing the dynamics of cryptic lamellipodia formation. This activity of JAM-A is observed in cells grown on laminin and collagen-I but not on fibronectin or vitronectin. Accordingly, we find that JAM-A exists in a complex with the laminin- and collagen-I-binding α3β1 integrin. We also find that JAM-A interacts with tetraspanins CD151 and CD9, which both interact with α3β1 integrin and regulate α3β1 integrin activity in different contexts. Mapping experiments indicate that JAM-A associates with α3β1 integrin and tetraspanins CD151 and CD9 through its extracellular domain. Similar to depletion of JAM-A, depletion of either α3β1 integrin or tetraspanins CD151 and CD9 in MDCK cells slows down collective cell migration. Our findings suggest that JAM-A exists with α3β1 integrin and tetraspanins CD151 and CD9 in a functional complex to regulate collective cell migration of polarized epithelial cells.

Keywords: Cell polarity; Cryptic lamellipodia; JAMs; Junctional adhesion molecules; MDCK; Tetraspanins.

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Conflict of interest statement

The authors declare that they have no competing financial interests.

Figures

**Fig. 1**
JAM-A limits single cell migration. A Single cell migration of MDCKII cells with inducible expression of JAM-A shRNAs (pEmU6proT, −Dox: shRNA not induced, +Dox: shRNA induced). Control cells (−Dox) were stably transfected with LA-mCherry, JAM-A KD cells (+Dox) were stably transfected with LA-EGFP. Cells were cultured on collagen-I (Col-I), fibronectin (FN), or vitronectin (VN) as indicated. Left panels: representative images of a LA-mCherry-transfected control cell (Ctrl, −Dox) and a LA-GFP-transfected JAM-A knockdown cell (JAM-A KD, +Dox) grown on collagen-I. Black-and-white images show the motility paths (yellow lines); the blob diameters used to track the cell during migration are highlighted by purple circles. Quantifications of single cell migration speed are shown in the right panels. Number of cells analyzed: Col-I: −Dox: 45, +Dox: 38, FN: −Dox: 48, +Dox: 44; VN: −Dox: 52, +Dox: 52, five independent experiments. B Quantifications of single cell migration speed of JAM-A KO MDCKII cells reconstituted with an inducible expression vector for murine JAM-A (pInducer21, −Dox: not induced, +Dox: induced). As control cells, MDCKII cells with inducible JAM-A shRNA expression in the absence of Dox were used. Number of cells analyzed: Ctrl MDCKII: 63; JAM-A KO, −Dox: 64; JAM-A KO, +Dox: 63; three independent experiments. C Quantifications of single cell migration speed of JAM-A KO MDCKII cells reconstituted with an inducible expression vector encoding phospho-deficient mJAM-A mutants (mJAM-A Y281F or mJAM-A S285A in pInducer21, −Dox: not induced, +Dox: induced). Number of cells analyzed: Ctrl MDCKII: 70; JAM-A KO + mJAM-A Y281F: −Dox: 67; +Dox: 65; JAM-A KO + mJAM-A S285A: −Dox: 62; +Dox: 65; four independent experiments). All statistical analyses shown in this figure were performed using Mann–Whitney U test. Data are presented as mean values ± SD. NS not significant; *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001

**Fig. 2**
JAM-A positively regulates collective cell migration. A Monolayer expansion assays of MDCKII cells with inducible expression of JAM-A shRNAs (described in the legend to Fig. 1). Cells were seeded on Col-I, FN- or VN-coated microscope slides separated by a silicone stamp. Collective migration was triggered by stamp removal. The migration velocity of the cell collective was quantified by measuring the cell-free area directly after the removal of the stamp and 8 h later (see “Materials and Methods” for details). Top panels: representative images of monolayer expansion immediately after stamp removal (0 h) and after 8 h (8 h). Bottom panels: quantifications of collective cell migration velocities on different ECM substrates. Each dot represents one biological replicate (one independent cell population). Number of independent cell populations analyzed: Col-I: n = 12 for each cell line (four independent experiments), FN: n = 10 for each cell line (three independent experiments), VN: n = 9 for each cell line (three independent experiments). B Quantifications of collective cell migration speed of JAM-A KO MDCKII cells reconstituted with an inducible expression vector for murine JAM-A (see legend to Fig. 1B). Number of independent cell populations analyzed: n = 12 for each condition, three independent experiments. C Quantifications of collective cell migration speed of JAM-A KO MDCKII cells reconstituted with an inducible expression vector encoding phospho-deficient mJAM-A mutants (see legend to Fig. 1C). Number of independent cell populations analyzed: n = 14 for ctrl MDCKII cells, n = 12 for JAM-A KO MDCKII cells and mJAM-A expressing JAM-A KO MDCKII cells; three independent experiments. D β1 integrin expression in JAM-A KO MDCKII cells. Top: western blot analysis of β1 integrin in MDCKII cells with doxycycline-regulated expression of JAM-A shRNAs (pEmU6proT, −Dox: shRNA not induced, +Dox: shRNA induced). Cells were grown either on plastic or on collagen-I. Bottom: quantitative analysis of β1 integrin protein levels. Data are presented as mean values ± SD (n = 4 independent experiments). All statistical analyses shown in this figure were performed using two-tailed Student’s t test. Data are presented as mean values ± SD. NS not significant; **P < 0.01, ***P < 0.001, ****P < 0.0001

**Fig. 3**
JAM-A regulates cryptic lamellipodia dynamics and cell motility in cellular collectives. A Formation of cryptic lamellipodia in collectively migrating cells. Homotypic suspensions of differently labeled (LA-mCherry and LA-EGFP, mixed at 1:5 ratio) MDCKII cells were seeded on microscope slides and observed by live cell microscopy over a period of 10 h. Left: representative immunofluorescence signals of cryptic lamellipodia. Higher power images of regions marked by black squares are shown adjacent to the immunofluorescence images. Middle: binary images of immunofluorescence images shown in the left panels. White areas highlight cryptic lamellipodia. Right: quantification of overlapping areas. Areas of overlapping regions were calculated on the basis of the merged LA-EGFP and LA-mCherry signals using an ImageJ Macro (see “Materials and Methods” for details). Data indicate the mean areas of overlap during the observation period. Each symbol represents the videomicroscopic analysis of one video. Number of videos analyzed: n = 40 for each condition. Data is derived from six independent experiments. Scale bars: 10 µm. B Dynamics of cryptic lamellipodia during collective cell migration. Left: representative immunofluorescence signals of overlapping areas. Middle: representative binary images illustrating increases (white areas) and decreases (black areas) of cellular overlaps over the observation period (10 h). Right: quantification of changes in overlapping regions. Changes were calculated using an ImageJ Macro on the basis of the merged LA-EGFP and LA-mCherry signals (see “Materials and Methods” for details). Data indicate the mean increase or decrease of overlapping regions during the observation period. Each symbol represents the videomicroscopic analysis of one video. Number of videos analyzed: n = 40 for each condition. Data are derived from six independent experiments. Scale bars: 10 µm. C Migration behavior of single cells embedded in a cell collective. Left: representative immunofluorescence signals of LA-mCherry-positive cells embedded in a LA-EGFP-positive collective. Middle: binary images of single LA-mCherry-positive cells. Right: Jaccard index, migration velocity and directionality of single cells. Note that high Jaccard index values reflect low motility (see “Materials and Methods” for details). Each symbol represents the video microscopic analysis of one individual cell. Number of cells analyzed: n = 50 for ctrl MDCKII cells, n = 47 for JAM-A KD MDCKII cells. Data is derived from six independent experiments. Statistical analysis of migration velocities was performed using Mann–Whitney U test, all other statistical analysis were performed using two-tailed Student’s t test. Data are presented as mean values ± SD. NS not significant; *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001

**Fig. 4**
JAM-A interacts with α3β1 integrin in MDCKII cells. A CoIP of α3β1 integrin with JAM-A. The interaction of JAM-A with α3β1 integrin is detectable in Brij98-based lysates but not in NP40-based lysates. Note that the weak JAM-A signal in Brij98 lysed cells is due to lower solubility of JAM-A in Brij98. The asterisks indicate IgG heavy chains. IP immunoprecipitation, *Lys* lysate. B CoIP of α3β1 integrin with JAM-A from MDCKII cells cultured on collagen-I, laminin or vitronectin. JAM-A immunoprecipitates were immunoblotted for α3 integrin and JAM-A as indicated. To increase the solubility of JAM-A, the direct IPs for JAM-A were performed with NP40-based lysates. C CoIPs of JAM-A phospho-deficient mutants (JAM-A/Y281F, JAM-A/S285A) with α3β1 integrin. The asterisk indicates IgG heavy chains. D CoIPs of JAM-A mutants with α3β1 integrin. JAM-A constructs with deletions of the entire cytoplasmic domain (Δ40), the membrane-distal Ig-like domain (ΔD1), the membrane-proximal Ig-like domain (ΔD2), the entire extracellular domain (MC), or with point mutations affecting the N-linked glycosylation site of JAM-A (N185Q), were transfected into JAM-A-deficient MDCKII cells and analyzed for interaction with α3β1 integrin by CoIP. *f.l.* full length, MC membrane and cytoplasmic. E Collective cell migration velocity of control MDCKII cells (Ctrl siRNA pool) and α3 integrin KD MDCKII cells (α3 ITGN siRNA pool) on collagen-I and laminin. Left: representative images of monolayer expansion immediately after stamp removal (0 h) and after 8 h (8 h). Right: statistical evaluation of monolayer expansion on collagen-I and laminin. Each dot represents one independent cell population. Number of independent cell populations analyzed: n = 12 for each condition. Data are derived from three independent experiments. Statistical analysis shown in this figure was performed using two-tailed Student’s t test. Data are presented as mean values ± SD. ****P < 0.0001

**Fig. 5**
JAM-A interacts with tetraspanin CD151. A CoIP of CD151 with JAM-A in HEK293T cells. GFP-CD151 immunoprecipitates were immunoblotted for JAM-A (top panels) and GFP (bottom panels). B CoIP of CD151 with JAM-A in Caco2 cells (left) and HK-2 cells (right). GFP-CD151 immunoprecipitates were immunoblotted for JAM-A and GFP as indicated. C CoIPs of JAM-A deletion mutants with CD151. JAM-A mutant constructs (described in Fig. 4) were transfected into JAM-A-deficient MDCKII cells and analyzed for interaction with CD151 by CoIP. D IF analysis of MDCKII cells transfected with EGFP-tagged CD151 and immunostained for endogenous α3 integrin and JAM-A. Arrowheads indicate co-localization of CD151, α3 integrin and JAM-A at cell–cell contact sites. Scale bar: 10 µm. E Monolayer expansion assays of MDCKII cells after siRNA-mediated depletion of CD151. MDCKII cells were transiently transfected with siRNA pools directed against CD151 (CD151 KD cells). As control, MDCKII cells were transfected with a scrambled siRNA pool (Ctrl KD cells). Collective cell migration was analyzed as described in the legend to Fig. 2. Top: representative images of monolayer expansion immediately after stamp removal (0 h) and after 8 h (8 h). Collective cell migration was analyzed on collagen-I and laminin as indicated. Bottom: statistical evaluation of monolayer expansion on collagen-I and laminin. Each dot represents one independent cell population. Number of independent cell populations analyzed: n = 12 for each condition. Data are derived from three independent experiments. Statistical analysis was performed using two-tailed Student’s t test. Data are presented as mean values ± SD. ***P < 0.001, ****P < 0.0001

**Fig. 6**
Regulation of cryptic lamellipodia dynamics and cell motility in cellular collectives by α3β1 integrin and Tspan CD151. A Formation of cryptic lamellipodia in α3 integrin- and CD151-depleted MDCKII cells. Note that the formation of cryptic lamellipodia is not altered after depletion of α3β1 integrin or of CD151. Scale bars: 10 µm. B Dynamics of cryptic lamellipodia during collective cell migration. Top panels: representative immunofluorescence signals of overlapping areas. Bottom panels: representative binary images illustrating increases (white areas) and decreases (black areas) of cellular overlaps over the observation period (10 h). Right panel: quantification of changes in overlapping regions. Changes were calculated using an ImageJ Macro on the basis of the merged LA-EGFP and LA-mCherry signals (see “Materials and Methods” for details). Data indicate the mean increase or decrease of overlapping regions during the observation period. Number of videos analyzed: n = 50, 10 independent experiments. Scale bars: 10 µm. C Migration behavior of single cells embedded in a cell collective. Left panels: representative immunofluorescence signals of LA-mCherry-positive cells embedded in a LA-EGFP-positive collective (top), and binary images of immunofluorescence images to highlight single LA-mCherry-positive cells. Right panels: quantification of motility, migration velocity and migration directionality of single cells within the collective. Note that high Jaccard index values reflect low motility (see “Materials and Methods” for details). Number of cells analyzed: n = 48 for ctrl MDCKII cells, n = 58 for α3 integrin KD MDCKII cells, n = 50 for CD151 KD MDCKII cells, 10 independent experiments. Scale bars: 10 µm. Statistical analysis of migration velocities was performed using Mann–Whitney U test; all other statistical analysis were performed using two-tailed Student’s t test. Data are presented as mean values ± SD. NS, not significant; *P < 0.05, **P < 0.01

**Fig. 7**
JAM-A interacts with tetraspanin CD9. A CoIP of α3β1 integrin with JAM-A in CD151-depleted MDCKII cells. Lanes with postnuclear supernatants (PNS) contain 5% of the input used for IPs. B CoIP of CD9 with JAM-A. JAM-A immunoprecipitates obtained from MDCKII cells were immunoblotted for CD9 (top panels) and JAM-A (bottom panels). C CoIPs of JAM-A deletion mutants with endogenous CD9. JAM-A deletion constructs lacking the PDZ domain-binding motif (Δ3) or the entire cytoplasmic domain (Δ40) were transfected into JAM-A-deficient MDCKII cells and analyzed for interaction with CD9 by CoIP. Note that the JAM-A–CD9 interaction is retained after deletion of the entire cytoplasmic domain. The asterisk indicates IgG heavy chains. (D) Monolayer expansion assays of MDCKII cells after siRNA-mediated depletion of CD9 and after combined depletion of CD151 and CD9. MDCKII cells were transiently transfected with siRNA pools directed against CD9, or both CD151 and CD9. As control, MDCKII cells were transfected with a scrambled siRNA pool (Ctrl KD cells). Collective cell migration was analyzed as described in the legend to Fig. 2. Top: representative images of monolayer expansion immediately after stamp removal (0 h) and after 8 h (8 h). Collective cell migration was analyzed on collagen-I and laminin as indicated. Bottom: statistical evaluation of monolayer expansion on collagen-I and laminin. Each dot represents one independent cell population. Number of independent cell populations analyzed: n = 12 for each condition. Data are derived from three independent experiments. Statistical analysis was performed using two-tailed Student’s t test. Data are presented as mean values ± SD. ***P < 0.001, ****P < 0.0001. The experiments were performed in parallel to the monolayer expansion assays shown in Fig. 5E. The data obtained for control cells are therefore identical to those shown in Fig. 5E. E Cartoon of JAM-A association with α3β1 integrin through tetraspanins CD151 and CD9 (summary of biochemical data). Note that the interaction of JAM-A with both tetraspanins is mediated by the extracellular domain of JAM-A (red arrows), and that the interaction of CD151 with α3β1 integrin is also mediated by the extracellular domains of the two proteins (green arrow) [45]. Phosphorylations involved in the regulation of MDCK cell motility and collective cell migration are indicated. For simplicity, the two phosphorylations are depicted in the same JAM-A dimer. Western blot data shown in this figure are representatives of at least three independent experiments

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References

1. Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol. 2009;10(7):445–457. - PubMed
1. Scarpa E, Mayor R. Collective cell migration in development. J Cell Biol. 2016;212(2):143–155. - PMC - PubMed
1. Shellard A, Mayor R. Rules of collective migration: from the wildebeest to the neural crest. Philos Trans R Soc Lond B Biol Sci. 1807;2020(375):20190387. - PMC - PubMed
1. Farooqui R, Fenteany G. Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J Cell Sci. 2005;118(Pt 1):51–63. - PubMed
1. Menko AS, Bleaken BM, Walker JL. Regional-specific alterations in cell-cell junctions, cytoskeletal networks and myosin-mediated mechanical cues coordinate collectivity of movement of epithelial cells in response to injury. Exp Cell Res. 2014;322(1):133–148. - PMC - PubMed

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[1] Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol. 2009;10(7):445–457. - PubMed

[2] Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol. 2009;10(7):445–457. - PubMed

[3] Scarpa E, Mayor R. Collective cell migration in development. J Cell Biol. 2016;212(2):143–155. - PMC - PubMed

[4] Scarpa E, Mayor R. Collective cell migration in development. J Cell Biol. 2016;212(2):143–155. - PMC - PubMed

[5] Shellard A, Mayor R. Rules of collective migration: from the wildebeest to the neural crest. Philos Trans R Soc Lond B Biol Sci. 1807;2020(375):20190387. - PMC - PubMed

[6] Shellard A, Mayor R. Rules of collective migration: from the wildebeest to the neural crest. Philos Trans R Soc Lond B Biol Sci. 1807;2020(375):20190387. - PMC - PubMed

[7] Farooqui R, Fenteany G. Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J Cell Sci. 2005;118(Pt 1):51–63. - PubMed

[8] Farooqui R, Fenteany G. Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J Cell Sci. 2005;118(Pt 1):51–63. - PubMed

[9] Menko AS, Bleaken BM, Walker JL. Regional-specific alterations in cell-cell junctions, cytoskeletal networks and myosin-mediated mechanical cues coordinate collectivity of movement of epithelial cells in response to injury. Exp Cell Res. 2014;322(1):133–148. - PMC - PubMed

[10] Menko AS, Bleaken BM, Walker JL. Regional-specific alterations in cell-cell junctions, cytoskeletal networks and myosin-mediated mechanical cues coordinate collectivity of movement of epithelial cells in response to injury. Exp Cell Res. 2014;322(1):133–148. - PMC - PubMed

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JAM-A interacts with α3β1 integrin and tetraspanins CD151 and CD9 to regulate collective cell migration of polarized epithelial cells

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JAM-A interacts with α3β1 integrin and tetraspanins CD151 and CD9 to regulate collective cell migration of polarized epithelial cells

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