Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism

doi:10.1083/jcb.110.5.1681

This Article

	Full Text (PDF, 2371K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Cooper, D. N.
	Articles by Barondes, S. H.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Cooper, D. N.
	Articles by Barondes, S. H.


Social Bookmarking

	What's this?

ARTICLES

Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism

DN Cooper and SH Barondes
Department of Psychiatry, University of California, San Francisco 94143- 0984.

A soluble lactose-binding lectin with subunit Mr of 14,500 is believed to function by interacting with extracellular glycoconjugates, because it has been detected extracellularly by immunohistochemistry. This localization has been questioned, however, since the lectin lacks a secretion signal sequence, which challenges the contention that it is secreted. We have demonstrated externalization of this lectin from C2 mouse muscle cells by both immunoprecipitation of metabolically labeled protein and immunohistochemical localization. We further show that externalization of the lectin is a developmentally regulated process that accompanies myoblast differentiation and that the lectin codistributes with laminin in myotube extracellular matrix. Immunohistochemical localization during intermediate stages of externalization suggests that the lectin becomes concentrated in evaginations of plasma membrane, which pinch off to form labile lectin- rich extracellular vesicles. This suggests a possible mechanism for lectin export from the cytosol to the extracellular matrix.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Stowell, S. R., Cho, M., Feasley, C. L., Arthur, C. M., Song, X., Colucci, J. K., Karmakar, S., Mehta, P., Dias-Baruffi, M., McEver, R. P., Cummings, R. D. (2009). Ligand Reduces Galectin-1 Sensitivity to Oxidative Inactivation by Enhancing Dimer Formation. J. Biol. Chem. 284: 4989-4999 [Abstract] [Full Text]
Cerri, D. G., Rodrigues, L. C., Stowell, S. R., Araujo, D. D., Coelho, M. C., Oliveira, S. R., Bizario, J. C. S., Cummings, R. D., Dias-Baruffi, M., Costa, M. C. R. (2008). Degeneration of dystrophic or injured skeletal muscles induces high expression of Galectin-1. Glycobiology 18: 842-850 [Abstract] [Full Text]
Aoki, N., Jin-no, S., Nakagawa, Y., Asai, N., Arakawa, E., Tamura, N., Tamura, T., Matsuda, T. (2007). Identification and Characterization of Microvesicles Secreted by 3T3-L1 Adipocytes: Redox- and Hormone-Dependent Induction of Milk Fat Globule-Epidermal Growth Factor 8-Associated Microvesicles. Endocrinology 148: 3850-3862 [Abstract] [Full Text]
Delmas, O., Breton, M., Sapin, C., Le Bivic, A., Colard, O., Trugnan, G. (2007). Heterogeneity of Raft-Type Membrane Microdomains Associated with VP4, the Rotavirus Spike Protein, in Caco-2 and MA 104 Cells. J. Virol. 81: 1610-1618 [Abstract] [Full Text]
Raje, C. I., Kumar, S., Harle, A., Nanda, J. S., Raje, M. (2007). The Macrophage Cell Surface Glyceraldehyde-3-phosphate Dehydrogenase Is a Novel Transferrin Receptor. J. Biol. Chem. 282: 3252-3261 [Abstract] [Full Text]
Camby, I., Le Mercier, M., Lefranc, F., Kiss, R. (2006). Galectin-1: a small protein with major functions. Glycobiology 16: 137R-157R [Abstract] [Full Text]
Zehe, C., Engling, A., Wegehingel, S., Schafer, T., Nickel, W. (2006). Cell-surface heparan sulfate proteoglycans are essential components of the unconventional export machinery of FGF-2. Proc. Natl. Acad. Sci. USA 103: 15479-15484 [Abstract] [Full Text]
Biron, V. A., Iglesias, M. M., Troncoso, M. F., Besio-Moreno, M., Patrignani, Z. J., Pignataro, O. P., Wolfenstein-Todel, C. (2006). Galectin-1: biphasic growth regulation of Leydig tumor cells. Glycobiology 16: 810-821 [Abstract] [Full Text]
Naschberger, E., Lubeseder-Martellato, C., Meyer, N., Gessner, R., Kremmer, E., Gessner, A., Sturzl, M. (2006). Human Guanylate Binding Protein-1 Is a Secreted GTPase Present in Increased Concentrations in the Cerebrospinal Fluid of Patients with Bacterial Meningitis. Am. J. Pathol. 169: 1088-1099 [Abstract] [Full Text]
Perone, M. J., Larregina, A. T., Shufesky, W. J., Papworth, G. D., Sullivan, M. L. G., Zahorchak, A. F., Stolz, D. B., Baum, L. G., Watkins, S. C., Thomson, A. W., Morelli, A. E. (2006). Transgenic galectin-1 induces maturation of dendritic cells that elicit contrasting responses in naive and activated T cells.. J. Immunol. 176: 7207-7220 [Abstract] [Full Text]
Seelenmeyer, C., Wegehingel, S., Tews, I., Kunzler, M., Aebi, M., Nickel, W. (2005). Cell surface counter receptors are essential components of the unconventional export machinery of galectin-1. JCB 171: 373-381 [Abstract] [Full Text]
Kosinski, M., McDonald, K., Schwartz, J., Yamamoto, I., Greenstein, D. (2005). C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes. Development 132: 3357-3369 [Abstract] [Full Text]
Leppanen, A., Stowell, S., Blixt, O., Cummings, R. D. (2005). Dimeric Galectin-1 Binds with High Affinity to {alpha}2,3-Sialylated and Non-sialylated Terminal N-Acetyllactosamine Units on Surface-bound Extended Glycans. J. Biol. Chem. 280: 5549-5562 [Abstract] [Full Text]
Stegmayer, C., Kehlenbach, A., Tournaviti, S., Wegehingel, S., Zehe, C., Denny, P., Smith, D. F., Schwappach, B., Nickel, W. (2005). Direct transport across the plasma membrane of mammalian cells of Leishmania HASPB as revealed by a CHO export mutant. J. Cell Sci. 118: 517-527 [Abstract] [Full Text]
Amzallag, N., Passer, B. J., Allanic, D., Segura, E., Thery, C., Goud, B., Amson, R., Telerman, A. (2004). TSAP6 Facilitates the Secretion of Translationally Controlled Tumor Protein/Histamine-releasing Factor via a Nonclassical Pathway. J. Biol. Chem. 279: 46104-46112 [Abstract] [Full Text]
Walzel, H., Brock, J., Pohland, R., Vanselow, J., Tomek, W., Schneider, F., Tiemann, U. (2004). Effects of galectin-1 on regulation of progesterone production in granulosa cells from pig ovaries in vitro. Glycobiology 14: 871-881 [Abstract] [Full Text]
Backhaus, R., Zehe, C., Wegehingel, S., Kehlenbach, A., Schwappach, B., Nickel, W. (2004). Unconventional protein secretion: membrane translocation of FGF-2 does not require protein unfolding. J. Cell Sci. 117: 1727-1736 [Abstract] [Full Text]
Ahmed, H., Du, S.-J., O'Leary, N., Vasta, G. R. (2004). Biochemical and molecular characterization of galectins from zebrafish (Danio rerio): notochord-specific expression of a prototype galectin during early embryogenesis. Glycobiology 14: 219-232 [Abstract] [Full Text]
Horie, H., Kadoya, T., Hikawa, N., Sango, K., Inoue, H., Takeshita, K., Asawa, R., Hiroi, T., Sato, M., Yoshioka, T., Ishikawa, Y. (2004). Oxidized Galectin-1 Stimulates Macrophages to Promote Axonal Regeneration in Peripheral Nerves after Axotomy. J. Neurosci. 24: 1873-1880 [Abstract] [Full Text]
Schafer, T., Zentgraf, H., Zehe, C., Brugger, B., Bernhagen, J., Nickel, W. (2004). Unconventional Secretion of Fibroblast Growth Factor 2 Is Mediated by Direct Translocation across the Plasma Membrane of Mammalian Cells. J. Biol. Chem. 279: 6244-6251 [Abstract] [Full Text]
Stowell, S. R., Dias-Baruffi, M., Penttila, L., Renkonen, O., Nyame, A. K., Cummings, R. D. (2004). Human galectin-1 recognition of poly-N-acetyllactosamine and chimeric polysaccharides. Glycobiology 14: 157-167 [Abstract] [Full Text]
Taverna, S., Ghersi, G., Ginestra, A., Rigogliuso, S., Pecorella, S., Alaimo, G., Saladino, F., Dolo, V., Dell'Era, P., Pavan, A., Pizzolanti, G., Mignatti, P., Presta, M., Vittorelli, M. L. (2003). Shedding of Membrane Vesicles Mediates Fibroblast Growth Factor-2 Release from Cells. J. Biol. Chem. 278: 51911-51919 [Abstract] [Full Text]
Martin, P. T. (2003). Dystroglycan glycosylation and its role in matrix binding in skeletal muscle. Glycobiology 13: 55R-66R [Abstract] [Full Text]
Seelenmeyer, C., Wegehingel, S., Lechner, J., Nickel, W. (2003). The cancer antigen CA125 represents a novel counter receptor for galectin-1. J. Cell Sci. 116: 1305-1318 [Abstract] [Full Text]
Correa, S. G., Sotomayor, C. E., Aoki, M. P., Maldonado, C. A., Rabinovich, G. A. (2003). Opposite effects of galectin-1 on alternative metabolic pathways of L-arginine in resident, inflammatory, and activated macrophages. Glycobiology 13: 119-128 [Abstract] [Full Text]
Dettin, L., Rubinstein, N., Aoki, A., Rabinovich, G. A., Maldonado, C. A. (2003). Regulated Expression and Ultrastructural Localization of Galectin-1, a Proapoptotic {beta}-Galactoside-Binding Lectin, During Spermatogenesis in Rat Testis. Biol. Reprod. 68: 51-59 [Abstract] [Full Text]
Engling, A., Backhaus, R., Stegmayer, C., Zehe, C., Seelenmeyer, C., Kehlenbach, A., Schwappach, B., Wegehingel, S., Nickel, W. (2002). Biosynthetic FGF-2 is targeted to non-lipid raft microdomains following translocation to the extracellular surface of CHO cells. J. Cell Sci. 115: 3619-3631 [Abstract] [Full Text]
Dunphy, J. L., Barcham, G. J., Bischof, R. J., Young, A. R., Nash, A., Meeusen, E. N. T. (2002). Isolation and Characterization of a Novel Eosinophil-specific Galectin Released into the Lungs in Response to Allergen Challenge. J. Biol. Chem. 277: 14916-14924 [Abstract] [Full Text]
Pace, K. E., Lebestky, T., Hummel, T., Arnoux, P., Kwan, K., Baum, L. G. (2002). Characterization of a Novel Drosophila melanogaster Galectin. EXPRESSION IN DEVELOPING IMMUNE, NEURAL, AND MUSCLE TISSUES. J. Biol. Chem. 277: 13091-13098 [Abstract] [Full Text]
Kuwabara, I., Kuwabara, Y., Yang, R.-Y., Schuler, M., Green, D. R., Zuraw, B. L., Hsu, D. K., Liu, F.-T. (2002). Galectin-7 (PIG1) Exhibits Pro-apoptotic Function through JNK Activation and Mitochondrial Cytochrome c Release. J. Biol. Chem. 277: 3487-3497 [Abstract] [Full Text]
Goldring, K., Jones, G. E., Thiagarajah, R., Watt, D. J. (2002). The effect of galectin-1 on the differentiation of fibroblasts and myoblasts in vitro. J. Cell Sci. 115: 355-366 [Abstract] [Full Text]
Timmons, P. M., Rigby, P. W. J., Poirier, F. (2002). The murine seminiferous epithelial cycle is pre-figured in the Sertoli cells of the embryonic testis. Development 129: 635-647 [Abstract] [Full Text]
Rappoport, J. Z., Lipkowitz, M. S., Abramson, R. G. (2001). Localization and topology of a urate transporter/channel, a galectin, in epithelium-derived cells. Am. J. Physiol. Cell Physiol. 281: C1926-C1939 [Abstract] [Full Text]
Berberat, P. O., Friess, H., Wang, L., Zhu, Z., Bley, T., Frigeri, L., Zimmermann, A., Büchler, M. W. (2001). Comparative Analysis of Galectins in Primary Tumors and Tumor Metastasis in Human Pancreatic Cancer. J. Histochem. Cytochem. 49: 539-549 [Abstract] [Full Text]
Boulianne, R. P., Liu, Y., Aebi, M., Lu, B. C., Kües, U. (2000). Fruiting body development in Coprinus cinereus: regulated expression of two galectins secreted by a non-classical pathway. Microbiology 146: 1841-1853 [Abstract] [Full Text]
Fouillit, M., Joubert-Caron, R., Poirier, F., Bourin, P., Monostori, E., Levi-Strauss, M., Raphael, M., Bladier, D., Caron, M. (2000). Regulation of CD45-induced signaling by galectin-1 in Burkitt lymphoma B cells. Glycobiology 10: 413-419 [Abstract] [Full Text]
Travis, A. J., Sui, D., Riedel, K. D., Hofmann, N. R., Moss, S. B., Wilson, J. E., Kopf, G. S. (1999). A Novel NH2-terminal, Nonhydrophobic Motif Targets a Male Germ Cell-specific Hexokinase to the Endoplasmic Reticulum and Plasma Membrane. J. Biol. Chem. 274: 34467-34475 [Abstract] [Full Text]
Horie, H., Inagaki, Y., Sohma, Y., Nozawa, R., Okawa, K., Hasegawa, M., Muramatsu, N., Kawano, H., Horie, M., Koyama, H., Sakai, I., Takeshita, K., Kowada, Y., Takano, M., Kadoya, T. (1999). Galectin-1 Regulates Initial Axonal Growth in Peripheral Nerves after Axotomy. J. Neurosci. 19: 9964-9974 [Abstract] [Full Text]
Andrei, C., Dazzi, C., Lotti, L., Torrisi, M. R., Chimini, G., Rubartelli, A. (1999). The Secretory Route of the Leaderless Protein Interleukin 1beta Involves Exocytosis of Endolysosome-related Vesicles. Mol. Biol. Cell 10: 1463-1475 [Abstract] [Full Text]
Avni, O., Pur, Z., Yefenof, E., Baniyash, M. (1998). Complement Receptor 3 of Macrophages Is Associated with Galectin-1-Like Protein. J. Immunol. 160: 6151-6158 [Abstract] [Full Text]
Travis, A. J., Foster, J. A., Rosenbaum, N. A., Visconti, P. E., Gerton, G. L., Kopf, G. S., Moss, S. B. (1998). Targeting of a Germ Cell-specific Type 1�Hexokinase Lacking a Porin-binding Domain to the Mitochondria as Well as to the Head and Fibrous Sheath of Murine Spermatozoa. Mol. Biol. Cell 9: 263-276 [Abstract] [Full Text]
Florkiewicz, R. Z., Anchin, J., Baird, A. (1998). The Inhibition of Fibroblast Growth Factor-2 Export by Cardenolides Implies a Novel Function for the Catalytic Subunit of Na+,K+-ATPase. J. Biol. Chem. 273: 544-551 [Abstract] [Full Text]
Danielsen, E. M., van Deurs, B. (1997). Galectin-4 and Small Intestinal Brush Border Enzymes Form Clusters. Mol. Biol. Cell 8: 2241-2251 [Abstract] [Full Text]
Huflejt, M. E., Jordan, E. T., Gitt, M. A., Barondes, S. H., Leffler, H. (1997). Strikingly Different Localization of Galectin-3 and Galectin-4 in Human Colon Adenocarcinoma T84 Cells. GALECTIN-4 IS LOCALIZED AT SITES OF CELL ADHESION. J. Biol. Chem. 272: 14294-14303 [Abstract] [Full Text]
Wada, J., Kanwar, Y. S. (1997). Identification and Characterization of Galectin-9, a Novel beta -Galactoside-binding Mammalian Lectin. J. Biol. Chem. 272: 6078-6086 [Abstract] [Full Text]
Burleigh, B. A., Caler, E. V., Webster, P., Andrews, N. W. (1997). A Cytosolic Serine Endopeptidase from Trypanosoma cruzi Is Required for the Generation of Ca2+ Signaling in Mammalian Cells. JCB 136: 609-620 [Abstract] [Full Text]
Cooper, D. N.W., Boulianne, R. P., Charlton, S., Farrell, E. M., Sucher, A., Lu, B. C. (1997). Fungal Galectins, Sequence and Specificity of Two Isolectins from Coprinus cinereus. J. Biol. Chem. 272: 1514-1521 [Abstract] [Full Text]
Liu, S., Smith, S. E., Julian, J., Rohde, L. H., Karin, N. J., Carson, D. D. (1996). cDNA Cloning and Expression of HIP, a Novel Cell Surface Heparan Sulfate/Heparin-binding Protein of Human Uterine Epithelial Cells and Cell Lines. J. Biol. Chem. 271: 11817-11823 [Abstract] [Full Text]
Kavita, U., Mizel, S. B. (1995). Differential Sensitivity of Interleukin-1alpha and -beta Precursor Proteins to Cleavage by Calpain, a Calcium-dependent Protease. J. Biol. Chem. 270: 27758-27765 [Abstract] [Full Text]
Gitt, M. A., Wiser, M. F., Leffler, H., Herrmann, J., Xia, Y.-R., Massa, S. M., Cooper, D. N. W., Lusis, A. J., Barondes, S. H. (1995). Sequence and Mapping of Galectin-5, a beta-Galactoside-binding Lectin, Found in Rat Erythrocytes. J. Biol. Chem. 270: 5032-5038 [Abstract] [Full Text]
Cho, M., Cummings, R. D. (1995). Galectin-1, a beta-Galactoside-binding Lectin in Chinese Hamster Ovary Cells. J. Biol. Chem. 270: 5198-5206 [Abstract] [Full Text]
Cho, M., Cummings, R. D. (1995). Galectin-1, a beta-Galactoside-binding Lectin in Chinese Hamster Ovary Cells. J. Biol. Chem. 270: 5207-5212 [Abstract] [Full Text]
Hadari, Y. R., Paz, K., Dekel, R., Mestrovic, T., Accili, D., Zick, Y. (1995). Galectin-8. J. Biol. Chem. 270: 3447-3453 [Abstract] [Full Text]
Mahanthappa, N., Cooper, D., Barondes, S., Schwarting, G. (1994). Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 120: 1373-1384 [Abstract]
Gu, M, Wang, W, Song, W., Cooper, D., Kaufman, S. (1994). Selective modulation of the interaction of alpha 7 beta 1 integrin with fibronectin and laminin by L-14 lectin during skeletal muscle differentiation. J. Cell Sci. 107: 175-181 [Abstract]
Poirier, F., Robertson, E. J. (1993). Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development 119: 1229-1236 [Abstract]
Lee, T., Lin, Y., Mochitate, K, Grinnell, F (1993). Stress-relaxation of fibroblasts in collagen matrices triggers ectocytosis of plasma membrane vesicles containing actin, annexins II and VI, and beta 1 integrin receptors. J. Cell Sci. 105: 167-177 [Abstract]
Mummidi, S., Catano, G., Lam, L., Hoefle, A., Telles, V., Begum, K., Jimenez, F., Ahuja, S. S., Ahuja, S. K. (2001). Extensive Repertoire of Membrane-bound and Soluble Dendritic Cell-specific ICAM-3-grabbing Nonintegrin 1 (DC-SIGN1) and DC-SIGN2 Isoforms. INTER-INDIVIDUAL VARIATION IN EXPRESSION OF DC-SIGN TRANSCRIPTS. J. Biol. Chem. 276: 33196-33212 [Abstract] [Full Text]