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Regulation of Cell Migration by the Calcium-dependent Protease Calpain
Open accessAbstract
Integrin receptors play an important role during cell migration by mediating linkages and transmitting forces between the extracellular matrix and the actin cytoskeleton. The mechanisms by which these linkages are regulated and released during migration are not well understood. We show here that cell-permeable inhibitors of the calcium-dependent protease calpain inhibit both beta1 and beta3 integrin-mediated cell migration. Calpain inhibition specifically stabilizes peripheral focal adhesions, increases adhesiveness, and decreases the rate of cell detachment. Furthermore, these inhibitors alter the fate of integrin receptors at the rear of the cell during migration. A Chinese hamster ovary cell line expressing low levels of calpain I also shows reduced migration rates with similar morphological changes, further implicating calpain in this process. Taken together, the data suggest that calpain inhibition modulates cell migration by stabilizing cytoskeletal linkages and decreasing the rate of retraction of the cell's rear. Inhibiting calpain-mediated proteolysis may therefore be a potential therapeutic approach to control pathological cell migration such as tumor metastasis.
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“TBS, in addition to its actions on kinases, causes the breakdown of actin crosslinking proteins in the subsynaptic cytoskeleton; the relevant proteases also cleave transmembrane adhesion receptors that play a critical role in LTP-related actin polymerization (40–42).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [42]
In the citing paper
“TBS, in addition to its actions on kinases, causes the breakdown of actin crosslinking proteins in the subsynaptic cytoskeleton; the relevant proteases also cleave transmembrane adhesion receptors that play a critical role in LTP-related actin polymerization (40–42).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [42]
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“Importantly, cell-permeable calpain inhibitors stabilized peripheral focal adhesions and decreased the rate of membrane detachment at the rear of cells migrating across a 2D substrat”
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“However, a previous study suggested that calpain was rather implicated in the disassembly of focal adhesions during cell migration (Huttenlocher et al., 1997).”
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Self-citationFocal adhesion and actin dynamics: a place where kinases and proteases meet to promote invasion
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“The list of proposed calpain substrates is very long (19, 63), and many reports have suggested that calpain may be involved in cell adhesion, spreading, and migration (26, 29, 49), myoblast fusion (4, 11), cell cycle control (36), and mitosis (50).”
BackgroundCalpain Activation in Huntington's Disease
Gafni, J., & Ellerby, L. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-12-04842.2002 · Cited by 331
“migration (Huttenlocher et al., 1997), integrin-mediated signal”
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Regulation of actin-based cell migration by cAMP/PKA
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“Its two major modes of action appear to be proteolysis of focal adhesion components and contact disassembly or turnover, especially during trailing edge retraction [205–208], as well as regulation of integrin-mediated signaling upstream of Rho family GTPases [209].”
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“A role for calpain activity in cell motility has been implied from studies using inhibitors of calpain that suppress cell migration on fibronecti”
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“mechanism for inhibited migration under conditions of high cell substratum adhesiveness (Marks et al., 1991; Hendey et al., 1992; Jay et al., 1995; Huttenlocher et al., 1997; Cox and Huttenlocher, 1998; Palecek et al., 1998).”
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Cuevas, B. D., Abell, A. N., & Johnson, G. L. (2007) · Oncogene · doi:10.1038/sj.onc.1210409 · Cited by 306
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Tran, A. D.-A., Marmo, T. P., Salam, A. A., Che, S., Finkelstein, E., Kabarriti, R., Xenias, H. S., Mazitschek, R., Hubbert, C., Kawaguchi, Y., et al. (2007) · Journal of Cell Science · doi:10.1242/jcs.03431 · Cited by 281
“Focal-adhesion breakdown at the rear of motile fibroblasts that is rate-limiting for fibroblast locomotion (Huttenlocher et al., 1997; Kaverina et al., 2000), requires MTs (Kaverina et al.”
BackgroundInfluentialCalpain Regulates Actin Remodeling during Cell Spreading
Potter, D. A., Tirnauer, J. S., Janssen, R. A. J., Croall, D. E., Hughes, C. N., Fiacco, K. A., Mier, J. W., Maki, M., & Herman, I. M. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.3.647 · Cited by 274
“The recent observations that calpain inhibition impedes cell migration in a transwell assay and inhibits cleavage of integrins at the rear of the cell during migration (Huttenlocher et al., 1997) also lend credence to a model in which calpain activation is required for cell motility.”
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“Even whether calpains are activated at the cell front during spreading or at the rear during detachment has only been addressed indirectly (3, 26, 41, 43, 45).”
BackgroundForces on adhesive contacts affect cell function
Galbraith, C. G., & Sheetz, M. P. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80030-6 · Cited by 273
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Beningo, K. A., Dembo, M., & Wang, Y.-L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405747102 · Cited by 279
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“Others have implicated specific proteins such as Src (Fincham and Frame, 1998) or calpain, a protease that cleaves several FA components such as FAK or talin (Huttenlocher et al., 1997; Bhatt et al., 2002; Franco et al., 2004).”
BackgroundPhysical and biochemical regulation of integrin release during rear detachment of migrating cells
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“Studies have postulated that limited proteolysis of components of the focal adhesion complex by proteolytic enzymes is a potential mediator for focal adhesion disassembly (Beckerle et al., 1987; Huttenlocher et al., 1997).”
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Biochemistry and Biomechanics of Cell Motility
Li, S., Guan, J., & Chien, S. (2005) · Annual Review of Biomedical Engineering · doi:10.1146/annurev.bioeng.7.060804.100340 · Cited by 248
Modulation of Vascular Smooth Muscle Signaling by Reactive Oxygen Species
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“Cells lacking Src family kinases, FAK, and calpain exhibit migratory defects that appear to reflect an inhibition of focal adhesion turnover; however, focal adhesion formation is not impaired (36, 56, 66).”
BackgroundPerrin, B. J., & Anna Huttenlocher, A. (2002) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00009-2 · Cited by 236
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“Thus, although calpain activity is also important in b1-dependent cell migration on matrix proteins [54], it is possible that the exact molecular mechanisms regulating the ‘switch’ from spreading to retraction are different amongst integrin subtypes.”
TRPM7 Regulates Cell Adhesion by Controlling the Calcium-dependent Protease Calpain
Su, L.-T., Agapito, M. T., Li, M., Simonson, W. T. N., Anna Huttenlocher, A., Habas, R., Yue, L., & Runnels, L. W. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m512885200 · Cited by 227
Ca2+-dependent myosin II activation is required for uropod retraction during neutrophil migration
Eddy, R. J., Pierini, L. M., Matsumura, F., & Maxfield, F. R. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.7.1287 · Cited by 227
Dynamics of a Chemoattractant Receptor in Living Neutrophils during Chemotaxis
Servant, G., Weiner, O. D., Neptune, E., Sedat, J. W., & Bourne, H. R. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.4.1163 · Cited by 227
“…driven by myosin-based motors, which moves nucleus and bulk cytoplasm in a for- ward direction; and 3) deadhesion of the trailing edge, thought to be partly mediated by the Ca21-sensitive enzymes, calcineurin and calpain (Cassimeris and Zigmond, 1990; Downey, 1994; Huttenlocher et al., 1997).”
BackgroundActin, microtubules and focal adhesion dynamics during cell migration
Wehrle‐Haller, B., & Imhof, B. A. (2002) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00071-7 · Cited by 225
Regulation of Adhesion Dynamics by Calpain-mediated Proteolysis of Focal Adhesion Kinase (FAK)
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Self-citationRegulation of focal complex composition and disassembly by the calcium-dependent protease calpain
Bhatt, A. K., Kaverina, I., Otey, C. A., & Anna Huttenlocher, A. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.17.3415 · Cited by 210
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“, in situations where there is high substrate adhesiveness [249,251].”
BackgroundShiraha, H., Glading, A., Chou, J., Jia, Z., & Wells, A. H. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.8.2716-2727.2002 · Cited by 179
“In experimental models, we and others have demonstrated that failure to deadhere limits cell motility (24, 42).”
BackgroundVicente‐Manzanares, M., & Horwitz, A. R. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-207-6_1 · Cited by 179
Self-citationCalpain Function in the Modulation of Signal Transduction Molecules
Sato, K., & Kawashima, S. (2001) · Biological Chemistry · doi:10.1515/bc.2001.090 · Cited by 168
“Previously, it was thought that calpain is implicated in rear detachment of migrating cells (Huttenlocher et al., 1997; Palecek et al., 1998).”
BackgroundGiannone, G., Rondé, P., Gaire, M., Beaudouin, J., Haiech, J., Ellenberg, J., & Takeda, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404054200 · Cited by 166
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Kassis, J. N., Lauffenburger, D. A., Turner, T., & Wells, A. H. (2001) · Seminars in Cancer Biology · doi:10.1006/scbi.2000.0362 · Cited by 165
Self-citationCarragher, N. O., Walker, S. M., Carragher, L., Harris, F. M., Sawyer, T. K., Brunton, V., Ozanne, B. W., & Frame, M. C. (2006) · Oncogene · doi:10.1038/sj.onc.1209582 · Cited by 164
“As mentioned previously, cell migration in two dimensions is generally suppressed by calpain inhibitors (Huttenlocher et al., 1997; Glading et al., 2000, 2004; Carragher et al., 2001), but calpain inhibitors actually promote the amoeboid-like motility of neutrophils (Lokuta et al., 2003).”
BackgroundCell-matrix contact structures
Adams, J. C. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000864 · Cited by 162
TRPC1 regulates skeletal myoblast migration and differentiation
Louis, M., Zanou, N., Schoor, M. C., & Gailly, P. L. (2008) · Journal of Cell Science · doi:10.1242/jcs.037218 · Cited by 156
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“(Huttenlocher et al., 1997).”
Apicomplexan Parasites Co-Opt Host Calpains to Facilitate Their Escape from Infected Cells
Chandramohanadas, R., Davis, P. H., Beiting, D. P., Harbut, M. B., Darling, C., Velmourougane, G., Lee, M. Y., Greer, P. A., Roos, D. S., & Greenbaum, D. C. (2009) · Science · doi:10.1126/science.1171085 · Cited by 155
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The regulation of integrin function by Ca2+
Leitinger, B., McDowall, A., Stanley, P., & Hogg, N. (2000) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(00)00086-0 · Cited by 154
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m-Calpain is required for preimplantation embryonic development in mice
Dutt, P., Croall, D. E., Arthur, J. S. C., Veyra, T. D., Williams, K. R., Elce, J. S., & Greer, P. A. (2006) · BMC Developmental Biology · doi:10.1186/1471-213x-6-3 · Cited by 151
“Research on calpains has linked them with a wide variety of functions including muscle growth, development, degeneration (3), neuronal growth and neurodegeneration [4], cell cycle progression [5,6], signal cascades triggered by integrins and growth factors [7], membrane protrusion [8], remodeling of the cytoskeleton a…”
BackgroundOriented endocytic recycling of α5β1 in motile neutrophils
Pierini, L. M., Lawson, M. A., Eddy, R. J., Hendey, B., & Maxfield, F. R. (2000) · Blood · doi:10.1182/blood.v95.8.2471 · Cited by 149
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“Among other things, they are involved in the regulation of cytoskeleton-membrane interaction, cytoskeleton remodeling, and vesicular trafficking (3, 16, 17, 41).”
BackgroundCalpain: a role in cell transformation and migration
Carragher, N. O., & Frame, M. C. (2002) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00069-9 · Cited by 147
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Self-citationCalpain regulates neutrophil chemotaxis
Lokuta, M. A., Nuzzi, P. A., & Anna Huttenlocher, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0636533100 · Cited by 144
Cell migration: mechanisms of rear detachment and the formation of migration tracks
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“2b) (Bhatt et al., 2002; Huttenlocher et al., 1997).”
Shiraha, H., Glading, A., Gupta, K. B., & Wells, A. H. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.146.1.243 · Cited by 142
“We did not favor the former, as IP-10 has no discernible effect on basal cell motility or morphometry; alterations in these assays due to inhibition of basal haptokinesis would be expected if IP-10 directly strengthened adhesive sites (Huttenlocher et al., 1997; Palecek et al., 1997).”
BackgroundInfluentialAdhesion-guided in vitro morphogenesis in pure and mixed cell cultures
Powers, M. J., & Griffith, L. G. (1998) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19981201)43:5 · Cited by 61
Carragher, N. O., Fincham, V. J., Riley, D., & Frame, M. C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008972200 · Cited by 140
Growth Factor-Induced Cell Motility in Tumor Invasion
Wells, A. H., Kassis, J. N., Solava, J., Turner, T., & Lauffenburger, D. A. (2002) · Acta Oncologica · doi:10.1080/028418602753669481 · Cited by 139
“The other ubiquitous isoform, m-calpain, appears to be required during haptokinesis (41) and chemokine-driven motility (Satish et al.”
BackgroundSelf-citationCox, E. A., Bennin, D. A., Doan, A. T., O’Toole, T. E., & Anna Huttenlocher, A. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-03-0142 · Cited by 139
Caspase-8 Association with the Focal Adhesion Complex Promotes Tumor Cell Migration and Metastasis
Barbero, S., Mielgo, A., Torres, V. A., Teitz, T., Shields, D. J., Mikolon, D., Bogyo, M. S., Barilà, D., Lahti, J. M., Schlaepfer, D. D., et al. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-3937 · Cited by 137
“proteins that promotes focal adhesion turnover (25, 26).”
González-Peña, D., Gao, G., Baranski, M., Moen, T., Cleveland, B. M., Kenney, P. B., Vallejo, R. L., Palti, Y., & Leeds, T. D. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00203 · Cited by 133
“, 2000; Patel and Lane, 2000), cell spreading and migration (Dourdin et al., 1997; Huttenlocher et al., 1997; Potter et al., 1998), and myogenesis (Barnoy et al.”
BackgroundIsoform specific function of calpain 2 in regulating membrane protrusion
Franco, S. J., Perrin, B. J., & Anna Huttenlocher, A. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.05.021 · Cited by 130
“Previous studies have demonstrated that cell-permeable calpain inhibitors or ectopic expression of the endogenous calpain inhibitor calpastatin reduces cell migration rates and retraction of the cell rear [11,12].”
BackgroundCuevas, B. D., Abell, A. N., Witowsky, J. A., Yujiri, T., Johnson, N. L., Kesavan, K., Ware, M., Jones, P. L., Weed, S. A., DeBiasi, R. L., et al. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg322 · Cited by 129
Inhibition of Calpain Blocks Platelet Secretion, Aggregation, and Spreading
Croce, K., Flaumenhaft, R. C., Rivers, M., Furie, B., Furie, B. C., Herman, I. M., & Potter, D. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.51.36321 · Cited by 128
Vicente‐Manzanares, M., & Horwitz, A. R. (2011) · Journal of Cell Science · doi:10.1242/jcs.095653 · Cited by 126
“By contrast, calpain-based mechanisms appear to be particularly important for disassembly of adhesions that are found at the rear of the cell (Huttenlocher et al., 1997).”
BackgroundSelf-citationCalpain Mediates Integrin-induced Signaling at a Point Upstream of Rho Family Members
Kulkarni, S., Saido, T. C., Suzuki, K., & Fox, J. E. B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.30.21265 · Cited by 126
Harms, B. D., Bassi, G. M., Horwitz, A. R., & Lauffenburger, D. A. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.047365 · Cited by 124
“Pharmacologic inhibition of M-calpain activity did not reduce S (data not shown), a result expected for weakly adherent, but not strongly adherent cells (Glading et al., 2002; Huttenlocher et al., 1997).”
BackgroundSelf-citationCalpain involvement in the remodeling of cytoskeletal anchorage complexes
Lebart, M., & Benyamin, Y. (2006) · FEBS Journal · doi:10.1111/j.1742-4658.2006.05350.x · Cited by 122
Bernard‐Trifilo, J. A., Kramár, E. A., Torp, R., Lin, C., Pineda, E. A., LYNCH, G. S., & Gall, C. M. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03062.x · Cited by 120
“Most studies of integrins in the central nervous system have focused on early stages of development (Milner and Campbell 2002) and have demonstrated important roles for the adhesion receptors in mechanisms of cellular migration (Huttenlocher et al. 1997; Sheetz et al. 1998; Calderwood et al. 2001), process outgrowth (…”
BackgroundCalpain cleavage of integrin β cytoplasmic domains
Pfaff, M., Du, X., & Ginsberg, M. H. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01250-8 · Cited by 119
Self-citationDedieu, S., Poussard, S., Mazères, G., Grise, F., Dargelos, É., Cottin, P., & Brustis, J. (2003) · Experimental Cell Research · doi:10.1016/j.yexcr.2003.08.014 · Cited by 116
“These inhibitors were chosen based on their specificity and were used at concentrations previously reported [16,18,19,38].”
BackgroundMethodInfluentialProteolysis of Cortactin by Calpain Regulates Membrane Protrusion during Cell Migration
Perrin, B. J., Amann, K. J., & Anna Huttenlocher, A. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-06-0488 · Cited by 115
“Molecular Biology of the Cell Vol. 17, 239–250, January 2006”
BackgroundShao, H., Chou, J.-H., Baty, C. J., Burke, N. A., Watkins, S. C., Stolz, D. B., & Wells, A. H. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02243-05 · Cited by 114
“-Calpain appears critical in integrin- and chemokine-mediated cell motility and adhesion (3, 27, 53), while m-calpain is the isoform required for growth factor-mediated cell motility (22, 53), although recent evidence suggests that haptokinetic signaling may also activate m-calpain (19).”
BackgroundCalpain-2 as a target for limiting prostate cancer invasion.
Mamoune, A., Luo, J., Lauffenburger, D. A., & Wells, A. H. (2003) · PubMed · Cited by 112
Self-citationIntegrin αMβ2-Mediated Cell Migration to Fibrinogen and Its Recognition Peptides
Forsyth, C. B., Solovjov, D. A., Ugarova, T. P., & Plow, E. F. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.10.1123 · Cited by 112
“Such requirements for the b subunit cytoplasmic segment for migration were demonstrated with Chinese hamster ovary cells expressing integrin aIIbb3 and migrating on Fg (58).”
BackgroundXu, L., & Deng, X. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m510721200 · Cited by 111
Class- and Splice Variant-specific Association of CD98 with Integrin β Cytoplasmic Domains
Zent, R., Fenczik, C. A., Calderwood, D., Liu, S., Dellos, M., & Ginsberg, M. H. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.7.5059 · Cited by 110
Self-citation
Metadata
- Authors
- Huttenlocher, A., Palecek, S. P., Lu, Q., Zhang, W., Mellgren, R. L., Lauffenburger, D. A., Ginsberg, M. H., & Horwitz, A. F.
- Affiliations
- Massachusetts Institute of Technology (US)
- University of Toledo Medical Center (US)
- Scripps Research Institute (US)
- University of Illinois Urbana-Champaign (US)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1997-12
- Volume
- 272
- Issue
- 52
- Pages
- 32719-32722
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2099253537
- Cited by
- 390
- References
- 22
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 4 · 2023: 4 · 2022: 5 · 2021: 7 · 2020: 5 · 2019: 3 · 2018: 9 · 2017: 7 · 2016: 5 · 2015: 9 · 2014: 7 · 2013: 20 · 2012: 19
- FWCI
- 5.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Calpain Protease Function and Regulation
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- calpain, cell migration, beta1 integrin, CD61, focal adhesions, integrin-mediated adhesion, cell retraction, actin cytoskeleton, extracellular matrix, calpain inhibitors, calpain-1, metastasis, cell detachment
- MeSH terms
- Animals, Calpain, Cell Movement, Cricetinae, Platelet Membrane Glycoproteins, Antigens, CD, CHO Cells, Integrin beta1, Integrin beta3
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