Hyaluronan–CD44 interactions as potential targets for cancer therapy
Open accessAbstract
It is becoming increasingly clear that signals generated in tumor microenvironments are crucial to tumor cell behavior, such as survival, progression and metastasis. The establishment of these malignant behaviors requires that tumor cells acquire novel adhesion and migration properties to detach from their original sites and to localize to distant organs. CD44, an adhesion/homing molecule, is a major receptor for the glycosaminoglycan hyaluronan, which is one of the major components of the tumor extracellular matrix. CD44, a multistructural and multifunctional molecule, detects changes in extracellular matrix components, and thus is well positioned to provide appropriate responses to changes in the microenvironment, i.e. engagement in cell–cell and cell–extracellular matrix interactions, cell trafficking, lymph node homing and the presentation of growth factors/cytokines/chemokines to co‐ordinate signaling events that enable the cell responses that change in the tissue environment. The potential involvement of CD44 variants (CD44v), especially CD44v4–v7 and CD44v6–v9, in tumor progression has been confirmed for many tumor types in numerous clinical studies. The downregulation of the standard CD44 isoform (CD44s) in colon cancer is postulated to result in increased tumorigenicity. CD44v‐specific functions could be caused by their higher binding affinity than CD44s for hyaluronan. Alternatively, CD44v‐specific functions could be caused by differences in associating molecules, which may bind selectively to the CD44v exon. This minireview summarizes how the interaction between hyaluronan and CD44v can serve as a potential target for cancer therapy, in particular how silencing CD44v can target multiple metastatic tumors.
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Polysaccharides such as dextran and hyaluronic acid as biodegradable polymers have been explored for modifications on proteins.
“In light of this, polysaccharides such as dextran and hyaluronic acid (HA) as biodegradable polymers 36,39 have been explored for modifications on proteins.”
From Catalase-Integrated Hyaluronic Acid as Nanocarriers for Enhanced Photodynamic Therapy in Solid Tumor (2019) · cites this paper as [39]
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Hanahan, D., & Weinberg, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)81683-9 · Cited by 29,219 · see citing works
Coussens, L. M., & Werb, Z. (2002) · Nature · doi:10.1038/nature01322 · Cited by 15,111 · see citing works
Prospective identification of tumorigenic breast cancer cells
Al‐Hajj, M., Wicha, M. S., Benito‐Hernández, A., Morrison, S. J., & Clarke, M. F. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0530291100 · Cited by 10,388 · see citing works
CD44: From adhesion molecules to signalling regulators
Ponta, H., Sherman, L. S., & Herrlich, P. A. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1004 · Cited by 2,393 · see citing works
Tumor cell metabolism: cancer's Achilles' heel
Kroemer, G., & Pouyssegur, J. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.05.005 · Cited by 2,337 · see citing works
Hyaluronan: from extracellular glue to pericellular cue
Toole, B. P. (2004) · Nature Reviews Cancer · doi:10.1038/nrc1391 · Cited by 2,130 · see citing works
Hyaluronan: its nature, distribution, functions and turnover.
Fraser, J. R. E., Laurent, T. C., & Laurent, U. B. G. (1997) · Journal of Internal Medicine · doi:10.1046/j.1365-2796.1997.00170.x · Cited by 2,031 · see citing works
Laurent, T. C., & Fraser, J. R. E. (1992) · The FASEB Journal · doi:10.1096/fasebj.6.7.1563592 · Cited by 1,885 · see citing works
A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells
Günthert, U., Hofmann‐Apitius, M., Rudy, W., Reber, S., Zöller, M., Hauβmann, I., Matzku, S., Wenzel, A., Ponta, H., & Herrlich, P. (1991) · Cell · doi:10.1016/0092-8674(91)90403-l · Cited by 1,652 · see citing works
Raper, S. E., Chirmule, N. B., Lee, F. S., Wivel, N. A., Bagg, A., Gao, G., Wilson, J. M., & Batshaw, M. L. (2003) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2003.08.016 · Cited by 1,502 · see citing works
Angiogenesis Induced by Degradation Products of Hyaluronic Acid
West, D. C., HAMPSON, I. N., Arnold, F., & Kumar, S. (1985) · Science · doi:10.1126/science.2408340 · Cited by 1,140 · see citing works
Human Bone Marrow–Derived Mesenchymal Stem Cells in the Treatment of Gliomas
Nakamizo, A., Marini, F. C., Amano, T., Khan, A., Studeny, M., Gumin, J., Chen, J. J., Hentschel, S. J., Vecil, G. G., Dembinski, J. L., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-1874 · Cited by 1,035 · see citing works
Camenisch, T. D., Spicer, A. P., Brehm-Gibson, T., Biesterfeldt, J., Augustine, M. L., Calabro, A., Kubalak, S., Klewer, S. E., & McDonald, J. A. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10272 · Cited by 901 · see citing works
Studeny, M., Marini, F. C., Dembinski, J. L., Zompetta, C., Cabreira-Hansen, M. D. G., Bekele, B. N., Champlin, R. E., & Andreeff, M. (2004) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djh299 · Cited by 841 · see citing works
Effective expression of small interfering RNA in human cells
Paul, C. P., Good, P. D., Winer, I. S., & Engelke, D. R. (2002) · Nature Biotechnology · doi:10.1038/nbt0502-505 · Cited by 820 · see citing works
Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma
Khakoo, A. Y., Pati, S., Anderson, S. A., Reid, W., Elshal, M. F., Rovira, I. I., Nguyen, A. T., Malide, D., Combs, C. A., Hall, G., et al. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20051921 · Cited by 747 · see citing works
Yu, Q., & Stamenkovic, I. (1999) · Genes & Development · doi:10.1101/gad.13.1.35 · Cited by 715 · see citing works
Giordano, A., Galderisi, U., & Marino, I. R. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.20959 · Cited by 611 · see citing works
Sordi, V., Malosio, M. L., Marchesi, F., Mercalli, A., Melzi, R., Giordano, T., Belmonte, N., Ferrari, G., Leone, B. E., Bertuzzi, F., et al. (2005) · Blood · doi:10.1182/blood-2004-09-3507 · Cited by 602 · see citing works
Cross-linked hyaluronic acid hydrogel films: new biomaterials for drug delivery
Luo, Y., Kirker, K. R., & Prestwich, G. D. (2000) · Journal of Controlled Release · doi:10.1016/s0168-3659(00)00300-x · Cited by 596 · see citing works
CD44 is of Functional Importance for Colorectal Cancer Stem Cells
Du, L., Wang, H., He, L., Zhang, J., Ni, B., Wang, X., Jin, H., Cahuzac, N., Mehrpour, M., Lu, Y., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1034 · Cited by 589 · see citing works
Toole, B. P. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0244 · Cited by 571 · see citing works
Naor, D., Nedvetzki, S., Golan, I., Мельник, Л. В., & Faitelson, Y. (2002) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408360290795574 · Cited by 557 · see citing works
Laurent, T. C., & Fraser, J. R. E. (1992) · PubMed · Cited by 550 · see citing works
MT1‐MMP: A potent modifier of pericellular microenvironment
Itoh, Y., & Seiki, M. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20431 · Cited by 499 · see citing works
Avigdor, A. (2004) · Blood · doi:10.1182/blood-2003-10-3611 · Cited by 491 · see citing works
CD44, a therapeutic target for metastasising tumours
Orian‐Rousseau, V. (2010) · European Journal of Cancer · doi:10.1016/j.ejca.2010.02.024 · Cited by 476 · see citing works
A crucial role for CD44 in inflammation
Puré, E., & Cuff, C. A. (2001) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(01)01963-3 · Cited by 475 · see citing works
Platt, V. M., & Szoka, F. C. (2008) · Molecular Pharmaceutics · doi:10.1021/mp800024g · Cited by 455 · see citing works
CD44 in Cancer Progression: Adhesion, Migration and Growth Regulation
Marhaba, R., & Zöller, M. (2004) · Journal of Molecular Histology · doi:10.1023/b:hijo.0000032354.94213.69 · Cited by 439 · see citing works
Expression and modulation of CD44 variant isoforms in humans
Mackay, C. R., Terpe, H., Stauder, R., Marston, W. L., Stark, H., & Günthert, U. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.1.71 · Cited by 438 · see citing works
Zhu, H., Mitsuhashi, N., Klein, A., Barsky, L. W., Weinberg, K. I., Barr, M. L., Demetriou, A. A., & Wu, G. D. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0186 · Cited by 408 · see citing works
Theocharis, A. D., Skandalis, S. S., Tzanakakis, G. N., & Karamanos, N. K. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07800.x · Cited by 403 · see citing works
Self-citationHyaluronan Binding by Cell Surface CD44
Lesley, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002527200 · Cited by 400 · see citing works
The hyaluronan receptor (CD44) participates in the uptake and degradation of hyaluronan.
Culty, M., Nguyen, H., & Underhill, C. B. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.116.4.1055 · Cited by 399 · see citing works
Hyaluronan Binding by Cell Surface CD44
Lesley, J., Hascall, V., Tammi, M., & Hyman, R. (2000) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)61467-5 · Cited by 391 · see citing works
Self-citationCoussens, L. M., & Werb, Z. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.6.f23 · Cited by 384 · see citing works
Sanchez, M. B. H., Bussolati, B., Bruno, S., Morando, L., Mauriello-Romanazzi, G., Sanavio, F., Stamenkovic, I., Biancone, L., & Camussi, G. (2007) · Kidney International · doi:10.1038/sj.ki.5002334 · Cited by 378 · see citing works
Target-specific intracellular delivery of siRNA using degradable hyaluronic acid nanogels
Lee, H., Mok, H., Lee, S., Oh, Y., & Park, T. G. (2007) · Journal of Controlled Release · doi:10.1016/j.jconrel.2007.02.011 · Cited by 364 · see citing works
CD44 variant exon epitopes in primary breast cancer and length of survival
Kaufmann, M., von Minckwitz, G., Heider, K.-H., et al. (1995) · The Lancet · doi:10.1016/s0140-6736(95)90521-9 · Cited by 363 · see citing works
Hyaluronan-CD44 Interactions in Cancer: Paradoxes and Possibilities
Toole, B. P. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0479 · Cited by 362 · see citing works
Transferrin-Containing, Cyclodextrin Polymer-Based Particles for Tumor-Targeted Gene Delivery
Bellocq, N. C., Pun, S. H., Jensen, G. S., & Davis, M. E. (2003) · Bioconjugate Chemistry · doi:10.1021/bc034125f · Cited by 350 · see citing works
Haniffa, M. A., Wang, X., Holtick, U., Rae, M., Isaacs, J. D., Dickinson, A. M., Hilkens, C. M. U., & Collin, M. P. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.3.1595 · Cited by 345 · see citing works
Prevention of tumor metastasis formation by anti-variant CD44.
Seiter, S., Arch, R. H., Reber, S., et al. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.177.2.443 · Cited by 340 · see citing works
The normal structure and function of CD44 and its role in neoplasia
Sneath, R., & Mangham, D. C. (1998) · Molecular Pathology · doi:10.1136/mp.51.4.191 · Cited by 333 · see citing works
Ghatak, S., Misra, S., & Toole, B. P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202404200 · Cited by 332 · see citing works
Self-citationCamenisch, T. D., Schroeder, J. A., Bradley, J. M., Klewer, S. E., & McDonald, J. A. (2002) · Nature Medicine · doi:10.1038/nm742 · Cited by 330 · see citing works
Eliaz, R. E., & Szoka, F. C. (2001) · PubMed · Cited by 330 · see citing works
High levels of stromal hyaluronan predict poor disease outcome in epithelial ovarian cancer.
Anttila, M., Tammi, R., Tammi, M., Syrjänen, K. J., Saarikoski, S., & Kosma, V. (2000) · PubMed · Cited by 327 · see citing works
Tijink, B. M., Buter, J., de Bree, R., Giaccone, G., Lang, M. S., Staab, A., Leemans, C. R., & van Dongen, G. A. M. S. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-0910 · Cited by 315 · see citing works
Involvement of CD44, a molecule with a thousand faces, in cancer dissemination
Naor, D., Wallach‐Dayan, S. B., Zahalka, M. A., et al. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.03.015 · Cited by 310 · see citing works
Kursa, M., Walker, G. F., Roessler, V., et al. (2002) · Bioconjugate Chemistry · doi:10.1021/bc0256087 · Cited by 310 · see citing works
Synthesis and Selective Cytotoxicity of a Hyaluronic Acid−Antitumor Bioconjugate
Luo, Y., & Prestwich, G. D. (1999) · Bioconjugate Chemistry · doi:10.1021/bc9900338 · Cited by 306 · see citing works
Kosaki, R., Watanabe, K., & Yamaguchi, Y. (1999) · PubMed · Cited by 303 · see citing works
Vermeulen, M. E., Pesteur, F. L., Gagnerault, M., et al. (1998) · Blood · doi:10.1182/blood.v92.3.894 · Cited by 292 · see citing works
Bourguignon, L., Zhu, H., Shao, L., & Chen, Y. W. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.3.1829 · Cited by 284 · see citing works
Cichy, J., & Puré, E. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302098 · Cited by 278 · see citing works
Wang, F., Hansen, R. K., Radisky, D. C., Yoneda, T., Barcellos‐Hoff, M. H., PETERSEN, O. W., Turley, E. A., & Bissell, M. J. (2002) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/94.19.1494 · Cited by 271 · see citing works
Non-hematopoietic bone marrow stem cells: Molecular control of expansion and differentiation
Gregory, C. A., Prockop, D. J., & Spees, J. L. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.03.018 · Cited by 270 · see citing works
Bourguignon, L., Zhu, H., Shao, L., & Chen, Y. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m006498200 · Cited by 262 · see citing works
A Hyaluronic Acid−Taxol Antitumor Bioconjugate Targeted to Cancer Cells
Luo, Y., Ziebell, M. R., & Prestwich, G. D. (2000) · Biomacromolecules · doi:10.1021/bm000283n · Cited by 262 · see citing works
Glycosylation of CD44 negatively regulates its recognition of hyaluronan.
Katoh, S., Zheng, Z., Oritani, K., Shimozato, T., & Kincade, P. W. (1995) · The Journal of Experimental Medicine · doi:10.1084/jem.182.2.419 · Cited by 254 · see citing works
Anderson, S. A., Glod, J. W., Arbab, A. S., Noel, M., Ashari, P., Fine, H. A., & Frank, J. A. (2004) · Blood · doi:10.1182/blood-2004-06-2222 · Cited by 254 · see citing works
Lesley, J., He, Q., Miyake, K., et al. (1992) · The Journal of Experimental Medicine · doi:10.1084/jem.175.1.257 · Cited by 252 · see citing works
Intracellular hyaluronan: a new frontier for inflammation?
Hascall, V. (2004) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2004.02.013 · Cited by 247 · see citing works
Self-citationMisra, S., Ghatak, S., & Toole, B. P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m500737200 · Cited by 245 · see citing works
Self-citationHyaluronan microspheres for sustained gene delivery and site-specific targeting
Yun, Y., Goetz, D. J., Yellen, P., & Chen, W. (2003) · Biomaterials · doi:10.1016/s0142-9612(03)00467-8 · Cited by 241 · see citing works
Bourguignon, L., Zhu, H., Chu, A. J., et al. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.44.27913 · Cited by 240 · see citing works
Peer, D., & Margalit, R. (2003) · International Journal of Cancer · doi:10.1002/ijc.11615 · Cited by 229 · see citing works
Bourguignon, L., Singleton, P. A., Zhu, H., & Zhou, B. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204320200 · Cited by 224 · see citing works
Regulation of Multidrug Resistance in Cancer Cells by Hyaluronan
Misra, S., Ghatak, S., Zoltan-Jones, A., & Toole, B. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.c300173200 · Cited by 222 · see citing works
Self-citationElevated Hyaluronan Production Induces Mesenchymal and Transformed Properties in Epithelial Cells
Zoltan-Jones, A., Huang, L., Ghatak, S., & Toole, B. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m308168200 · Cited by 219 · see citing works
Self-citationGhatak, S., Misra, S., & Toole, B. P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m410882200 · Cited by 218 · see citing works
Self-citationFunctionalized Derivatives of Hyaluronic Acid Oligosaccharides: Drug Carriers and Novel Biomaterials
Pouyani, T., & Prestwich, G. D. (1994) · Bioconjugate Chemistry · doi:10.1021/bc00028a010 · Cited by 216 · see citing works
Expression of MAGE-antigens in normal tissues and cancer
Jungbluth, A. A., BUSAM, K. J., Kolb, D., Iversen, K., Coplan, K. A., Chen, Y., Spagnoli, G. C., & Old, L. J. (2000) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(20000215)85:4 · Cited by 214 · see citing works
Peer, D., & Margalit, R. (2004) · Neoplasia · doi:10.1593/neo.03460 · Cited by 214 · see citing works
Expression of human hyaluronan synthases in response to external stimuli
Jacobson, A., Brinck, J. W., Briskin, M., Spicer, A. P., & Heldin, P. (2000) · Biochemical Journal · doi:10.1042/bj3480029 · Cited by 210 · see citing works
Self-citationSkelton, T. P., Zeng, C., Nocks, A., & Stamenkovic, I. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.140.2.431 · Cited by 209 · see citing works
DECREASED EXPRESSION OF GALECTIN-3 IS ASSOCIATED WITH PROGRESSION OF HUMAN BREAST CANCER
Castronovo, V., van den Brûle, F. A., Jackers, P., Clausse, N., Liu, F., GILLET, C., & Sobel, M. E. (1996) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199605)179:1 · Cited by 204 · see citing works
Lesley, J., English, N. M., Perschl, A., Gregoroff, J., & Hyman, R. (1995) · The Journal of Experimental Medicine · doi:10.1084/jem.182.2.431 · Cited by 196 · see citing works
Itano, N., Sawai, T., Miyaishi, O., & Kimata, K. (1999) · PubMed · Cited by 182 · see citing works
Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer
Guo, X., Oshima, H., & Masanobu, O. (2009) · Kanazawa University Repository for Academic Resources (DSpace) (Kanazawa University) · Cited by 177 · see citing works
Lesley, J. (1998) · Frontiers in bioscience · doi:10.2741/a306 · Cited by 175 · see citing works
Misra, S., Toole, B. P., & Ghatak, S. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.c600138200 · Cited by 174 · see citing works
Self-citationWest, D. C., & Kumar, S. (2007) · Novartis Foundation symposium · doi:10.1002/9780470513774.ch12 · Cited by 172 · see citing works
Koyama, H., Hibi, T., Isogai, Z., Yoneda, M., Fujimori, M., Amano, J., Kawakubo, M., Kannagi, R., Kimata, K., Taniguchi, S., et al. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.060793 · Cited by 171 · see citing works
HYAL1 Hyaluronidase in Prostate Cancer: A Tumor Promoter and Suppressor
Lokeshwar, V. B., Cerwinka, W. H., Isoyama, T., & Lokeshwar, B. L. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1022 · Cited by 171 · see citing works
Hyaluronan synthase 3 overexpression promotes the growth of TSU prostate cancer cells.
Liu, N., Gao, F., Han, Z. J., Xu, X., Underhill, C. B., & Zhang, L. (2001) · PubMed · Cited by 171 · see citing works
Hyaluronan and Hyaluronan Synthases: Potential Therapeutic Targets in Cancer
Adamia, S., Maxwell, C. A., & Pilarski, L. M. (2005) · Cardiovascular & Haematological Disorders - Drug Targets · doi:10.2174/1568006053005056 · Cited by 170 · see citing works
Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny
Mendes, S., Robin, C., & Dzierzak, E. A. (2005) · Development · doi:10.1242/dev.01615 · Cited by 165 · see citing works
Marieb, E. A., Zoltan-Jones, A., Li, R., Misra, S., Ghatak, S., Cao, J. P., Zucker, S., & Toole, B. P. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2832 · Cited by 163 · see citing works
Self-citationLi, Y., Li, L., Brown, T. J., & Heldin, P. (2007) · International Journal of Cancer · doi:10.1002/ijc.22550 · Cited by 158 · see citing works
Self-citationRegulated clustering of variant CD44 proteins increases their hyaluronate binding capacity.
Sleeman, J. P., Rudy, W., Hofmann‐Apitius, M., et al. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.135.4.1139 · Cited by 157 · see citing works
Lesley, J., Howes, N., Perschl, A., & Hyman, R. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.180.1.383 · Cited by 155 · see citing works
Targeted delivery of NK4 to multiple lung tumors by bone marrow-derived mesenchymal stem cells
Kanehira, M., Xin, H., Hoshino, K., Maemondo, M., Mizuguchi, H., Hayakawa, T., Matsumoto, K., Nakamura, T., Nukiwa, T., & Saijo, Y. (2007) · Cancer Gene Therapy · doi:10.1038/sj.cgt.7701079 · Cited by 155 · see citing works
Eliaz, R. E., Nir, S., Marty, C., & Szoka, F. C. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-0654 · Cited by 154 · see citing works
CD44 can be activated to function as an hyaluronic acid receptor in normal murine T cells
Lesley, J., & Hyman, R. (1992) · European Journal of Immunology · doi:10.1002/eji.1830221036 · Cited by 147 · see citing works
A positive feedback loop couples Ras activation and CD44 alternative splicingPreprint
Cheng, C., Yaffe, M. B., & Sharp, P. A. (2006) · Genes & Development · doi:10.1101/gad.1430906 · Cited by 146 · see citing works
Spontaneous Metastasis of Prostate Cancer Is Promoted by Excess Hyaluronan Synthesis and Processing
Bharadwaj, A. G., Kovar, J. L., Loughman, E., Elowsky, C. G., Oakley, G. G., & Simpson, M. A. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.080501 · Cited by 141 · see citing works
Yadav, A. K., Mishra, P., Mishra, A. K., Mishra, P., Jain, S., & Agrawal, G. P. (2007) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2007.09.004 · Cited by 138 · see citing works
Pancreatic Cancer Stem Cells: Implications for the Treatment of Pancreatic Cancer
Simeone, D. M. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0584 · Cited by 136 · see citing works
Theocharis, A. D., Vynios, D. H., Papageorgakopoulou, N., et al. (2003) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00264-9 · Cited by 130 · see citing works
Takahashi, Y., Li, L., Kamiryo, M., Astériou, T., Moustakas, A., Yamashita, H., & Heldin, P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m411913200 · Cited by 129 · see citing works
Self-citationHe, Q., Lesley, J., Hyman, R., et al. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.6.1711 · Cited by 124 · see citing works
An insight on hyaluronic acid in drug targeting and drug delivery
Yadav, A. K., Mishra, P., & Agrawal, G. P. (2008) · Journal of drug targeting · doi:10.1080/10611860701794296 · Cited by 122 · see citing works
Jacobson, A., Rahmanian, M., Rubin, K., & Heldin, P. (2002) · International Journal of Cancer · doi:10.1002/ijc.10683 · Cited by 121 · see citing works
Self-citationThe Activity of Hyaluronan Synthase 2 Is Regulated by Dimerization and Ubiquitination
Karousou, E., Kamiryo, M., Skandalis, S. S., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.127050 · Cited by 119 · see citing works
Self-citationLocalizing matrix metalloproteinase activities in the pericellular environment
Murphy, G., & Nagase, H. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07918.x · Cited by 117 · see citing works
Synthesis and Assembly of the Hyaluronan-Containing Coats around Normal Human Mesothelial Cells
Heldin, P., & Pertoft, H. (1993) · Experimental Cell Research · doi:10.1006/excr.1993.1264 · Cited by 117 · see citing works
Self-citationThankamony, S. P., & Knudson, W. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601530200 · Cited by 116 · see citing works
Significance of Tumor-Associated Stroma in Promotion of Intratumoral Lymphangiogenesis
Koyama, H., Kobayashi, N., Harada, M., Takeoka, M., Kawai, Y., Sano, K., Fujimori, M., Amano, J., Ohhashi, T., Kannagi, R., et al. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2008.070360 · Cited by 115 · see citing works
Brinck, J. W. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4645 · Cited by 114 · see citing works
Stem cells as vehicles for orthopedic gene therapy
Gafni, Y., Turgeman, G., Liebergall, M., Pelled, G., Gazit, Z., & Gazit, D. (2004) · Gene Therapy · doi:10.1038/sj.gt.3302197 · Cited by 109 · see citing works
Hyaluronan production increases the malignant properties of mesothelioma cells
Li, Y., & Heldin, P. (2001) · British Journal of Cancer · doi:10.1054/bjoc.2001.1922 · Cited by 105 · see citing works
Self-citationgi, R. K., & Volm, M. (1999) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19990621)84:3 · Cited by 99 · see citing works
Yadav, A. K., Mishra, P., Jain, S., et al. (2008) · Journal of drug targeting · doi:10.1080/10611860802095494 · Cited by 99 · see citing works
Peer, D., Dekel, Y., Melikhov, D., & Margalit, R. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-4046 · Cited by 99 · see citing works
Misra, S., Obeid, L. M., Hannun, Y. A., Minamisawa, S., Berger, F. G., Markwald, R. R., Toole, B. P., & Ghatak, S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m703811200 · Cited by 97 · see citing works
Self-citationA PCR-based method for the analysis of human CD44 splice products.Preprint
van Weering, D. H. J., Baas, P. D., & Bos, J. L. (1993) · Genome Research · doi:10.1101/gr.3.2.100 · Cited by 95 · see citing works
Importance of Hyaluronan-CD44 Interactions in Inflammation and Tumorigenesis
Heldin, P., Karousou, E., Olofsson, B., Porsch, H., Nishitsuka, K., & Skandalis, S. S. (2008) · Connective Tissue Research · doi:10.1080/03008200802143323 · Cited by 94 · see citing works
Self-citationHällgren, R., Gerdin, B., & Tufveson, G. (1990) · The Journal of Experimental Medicine · doi:10.1084/jem.171.6.2063 · Cited by 90 · see citing works
Requirement for CD44 in proliferation and homing of hematopoietic precursor cells
Khaldoyanidi, S. K., Denzel, A., & Zöller, M. (1996) · Journal of Leukocyte Biology · doi:10.1002/jlb.60.5.579 · Cited by 89 · see citing works
Delivery of CD44 shRNA/Nanoparticles within Cancer Cells
Misra, S., Hascall, V., Giovanni, C. D., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m806772200 · Cited by 88 · see citing works
Self-citationHathcock, K. S., Hirano, H., Murakami, S., et al. (1993) · The Journal of Immunology · doi:10.4049/jimmunol.151.12.6712 · Cited by 86 · see citing works
Evanko, S. P., Parks, W. T., & Wight, T. N. (2004) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.4a6356.2004 · Cited by 84 · see citing works
Skandalis, S. S., Kletsas, D., Kyriakopoulou, D., et al. (2006) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2006.03.021 · Cited by 83 · see citing works
Self-citationLi, L., Heldin, C., & Heldin, P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605607200 · Cited by 80 · see citing works
Self-citationPhosphorylation by CDK1 regulates XMAP215 function in vitro
Vasquez, R., Gard, D. L., & Cassimeris, L. (1999) · Cell Motility and the Cytoskeleton · doi:10.1002/(sici)1097-0169(1999)43:4 · Cited by 80 · see citing works
Akima, K., Ito, H., Iwata, Y., et al. (1996) · Journal of drug targeting · doi:10.3109/10611869609046255 · Cited by 78 · see citing works
Camenisch, T. D., & McDonald, J. A. (2000) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.23.4.f201 · Cited by 78 · see citing works
Ghatak, S., Hascall, V., Markwald, R. R., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.104273 · Cited by 76 · see citing works
Self-citationYadav, A. K., Agarwal, A., Rai, G., et al. (2010) · Drug Delivery · doi:10.3109/10717544.2010.500635 · Cited by 76 · see citing works
Enegd, B., King, J. A. J., Stylli, S. S., Paradiso, L., Kaye, A. H., & Novak, U. (2002) · Neurosurgery · doi:10.1097/00006123-200206000-00023 · Cited by 71 · see citing works
Chapter 4 Adhesion Proteins Meet Receptors
Orian‐Rousseau, V., & Ponta, H. (2008) · Advances in cancer research · doi:10.1016/s0065-230x(08)00404-1 · Cited by 69 · see citing works
Reeder, J. A., Gotley, D. C., Walsh, M. D., et al. (1998) · PubMed · Cited by 69 · see citing works
Sauter, A., Kloft, C., Gronau, S., Bogeschdorfer, F., Erhardt, T., Golze, W., Schroen, C., Staab, A., Riechelmann, H., & Hoermann, K. (2007) · International Journal of Oncology · doi:10.3892/ijo.30.4.927 · Cited by 59 · see citing works
Song, G.-L., Liao, X., Zhou, L., et al. (2004) · Leukemia Research · doi:10.1016/j.leukres.2004.02.005 · Cited by 49 · see citing works
Peer, D., & Margalit, R. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2000.2046 · Cited by 47 · see citing works
CD44v6 promotes proliferation by persisting activation of MAP kinases
Marhaba, R., Bourouba, M., & Zöller, M. (2004) · Cellular Signalling · doi:10.1016/j.cellsig.2004.11.017 · Cited by 44 · see citing works
Immunohistochemical Expression of the CD44 Variant 6 in Colorectal Adenocarcinoma
Ishida, T. (2000) · Surgery Today · doi:10.1007/pl00010042 · Cited by 39 · see citing works
Overexpression of CD44 Variant 6 in Human Endometrial Cancer and Its Prognostic Significance
Ayhan, A., Tok, E. C., Bildirici, İ., et al. (2001) · Gynecologic Oncology · doi:10.1006/gyno.2000.6014 · Cited by 37 · see citing works
Eliaz, R. E., Nir, S., & Szoka, F. C. (2004) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(04)87002-2 · Cited by 34 · see citing works
Kurozumi, K., Nishida, T., Nakao, K., et al. (1998) · World Journal of Surgery · doi:10.1007/s002689900481 · Cited by 33 · see citing works
Tumour-associated Hyaluronan: A Potential Regulator of Tumour Angiogenesis
West, D. C., & Kumar, S. (1991) · International Journal of Radiation Biology · doi:10.1080/09553009114551541 · Cited by 29 · see citing works
The CD44 Receptor of Lymphoma Cells: Structure-Function Relationships and Mechanism of Activation
Rochman, M., Moll, J. K., Herrlich, P., Wallach‐Dayan, S. B., Nedvetzki, S., Sionov, R. V., Golan, I., Ish‐Shalom, D., & Naor, D. (2000) · Cell Communication & Adhesion · doi:10.3109/15419060009015004 · Cited by 26 · see citing works
Differential synthesis and binding of hyaluronan by human breast cancer cell lines
Heldin, P., delaTorre, M., Ytterberg, D., et al. (1996) · Oncology Reports · doi:10.3892/or.3.6.1011 · Cited by 23 · see citing works
Self-citationRegidor, P., Callies, R., Regidor, M., et al. (1996) · Archives of Gynecology and Obstetrics · doi:10.1007/s004040050113 · Cited by 20 · see citing works
Smedsrød, B. H., & Seljelid, R. (1991) · Immunopharmacology · doi:10.1016/0162-3109(91)90020-y · Cited by 18 · see citing works
Organ-Specific Requirements for Cell Adhesion Molecules During Lymphoma Cell Dissemination
Naor, D., Sionov, R. V., Zahalka, M. A., et al. (1998) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-71987-5_9 · Cited by 13 · see citing works
Tammi, R., & Tammi, M. (1998) · Glycoforum · Cited by 13 · see citing works
[Expression of CD44 standard and CD44 variant 6 in human lung cancer].
Ochiai, S., Nakanishi, Y., Mizuno, K., et al. (1997) · PubMed · Cited by 8 · see citing works
Hyaluronic acid accumulation; the mechanism behind graft rejection edema
Tufveson, G., Gerdin, B., Larsson, E., et al. (1992) · Springer eBooks · doi:10.1007/978-3-642-77423-2_202 · Cited by 6 · see citing works
Hyaluronic acid accumulation; the mechanism behind graft rejection edema
Tufveson, G., Gerdin, B., Larsson, E., et al. (1992) · Transplant International · doi:10.1111/tri.1992.5.s1.688 · Cited by 6 · see citing works
[The role of interstitial hyaluronan in acute lung injury].
Ishibashi, M., Nishida, T., Murakami, H., et al. (1995) · PubMed · Cited by 4 · see citing works
基礎:急性肺傷害と間質基質-とくに,ヒアルロン酸の役割について-
石橋, 正., 西田, 富., 村上, 英., et al. (1995) · Medical Entomology and Zoology · Cited by 2 · see citing works
Hyaluronic acid and cell adhesion molecules in haematology
Fraser, J. R. E., Cahill, R. N. P., & Kimpton, W. G. (1994) · Australian and New Zealand Journal of Medicine · doi:10.1111/j.1445-5994.1994.tb04435.x · Cited by 2 · see citing works
Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer
Guo, X., Oshima, H., Kitmura, T., Taketo, M. M., & Oshima, M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800798200 · Cited by 1 · see citing works
Magnusson (1999) · doi:10.1002/(sici)1097-0215(19990505)81:3
Hoerr, I. (2000) · doi:10.1002/1521-4141(200001)30:1
Flagged first, then by citations
Research works printed but not linked: 2
- [154]Camenisch TD Schroeder JA Bradley J Klewer SE McDonald JA Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors Nat Med 2002 8 850 855 12134143
- [155]Camenisch TD Spicer AP Brehm-Gibson T Biesterfeldt J Augustine ML Calabro A Jr Kubalak S Klewer SE McDonald JA Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme J Clin Invest 2000 106 349 360 10930438 PMC314332
Cited by
Sorted by citations
Extracellular matrix structure
Theocharis, A. D., Skandalis, S. S., Gialeli, C., & Karamanos, N. K. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.11.001 · Cited by 2,598 · see citing works
Self-citationExtracellular matrix and its therapeutic potential for cancer treatment
Huang, J., Zhang, L., Wan, D., Zhou, L., Zheng, S., Lin, S., & Qiao, Y. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00544-0 · Cited by 962 · see citing works
Hyaluronic acid targeting of CD44 for cancer therapy: from receptor biology to nanomedicine
Mattheolabakis, G., Milane, L., Singh, A., & Amiji, M. M. (2015) · Journal of Drug Targeting · doi:10.3109/1061186x.2015.1052072 · Cited by 597 · see citing works
Catalase-Integrated Hyaluronic Acid as Nanocarriers for Enhanced Photodynamic Therapy in Solid Tumor
Phua, S. Z. F., Yang, G., Lim, W. Q., Verma, A., Chen, H., Thanabalu, T., & Zhao, Y. (2019) · ACS Nano · doi:10.1021/acsnano.9b01087 · Cited by 375 · see citing works
Bjorklund, C. C., Baladandayuthapani, V, Lin, H. Y., Jones, R. J., Kuiatse, I., Wang, H., Yang, J., Shah, J. J., Thomas, S. K., Wang, M., et al. (2014) · Leukemia · doi:10.1038/leu.2013.174 · Cited by 131 · see citing works
Tirella, A., Kloc-Muniak, K., Good, L., Ridden, J., Ashford, M., Puri, S., & Tirelli, N. (2019) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2019.02.032 · Cited by 60 · see citing works
Hyaluronan is required for cranial neural crest cells migration and craniofacial development
Casini, P., Nardi, I., & Ori, M. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23715 · Cited by 33 · see citing works
- Authors
- Misra, S., Heldin, P., Hascall, V. C., Karamanos, N. K., Skandalis, S. S., Markwald, R. R., & Ghatak, S.
- Affiliations
- Medical University of South Carolina (US)
- Uppsala University (SE)
- Cleveland Clinic (US)
- University of Patras (GR)
- Venue
- The FEBS Journal
- Publisher
- Wiley
- Published
- 2011-03-25
- Volume
- 278
- Issue
- 9
- Pages
- 1429-1443
- ISSN
- 1742-464X (ISSN-L)
- 1742-4658
- PMC
- PMC3166356
- OpenAlex
- W1873369382
- Cited by
- 494
- References
- 159
- Citations by year
- 2026: 22 · 2025: 29 · 2024: 18 · 2023: 26 · 2022: 35 · 2021: 37 · 2020: 41 · 2019: 33 · 2018: 40 · 2017: 45 · 2016: 36 · 2015: 33 · 2014: 42 · 2013: 22 · 2012: 23
- FWCI
- 2.70
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- FEBS Journal (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of South Carolina
- National Institutes of Health
- National Heart, Lung, and Blood Institute (HL R01 33756, R01HL033756)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (P30AR050953)
- National Center for Research Resources (P20RR016434, P20RR021949)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Keywords
- hyaluronic acid, CD44, CD44 splice variants, tumor microenvironment, tumor extracellular matrix, metastasis, tumor progression, colon cancer, cancer therapy targets, cell adhesion, lymph node homing
- MeSH terms
- Humans, Hyaluronic Acid, Neoplasm Metastasis, Neoplasms, Signal Transduction, Hyaluronan Receptors
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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