Hyaluronic acid targeting of CD44 for cancer therapy: from receptor biology to nanomedicine
Abstract
Cluster of differentiation-44 (CD44) is a ubiquitously present glycoprotein on the surface of mammalian cells that plays a significant role in a number of biological functions. Since the discovery that the receptor is over-expressed in a variety of solid tumors, such as pancreatic, breast and lung cancer, many studies have focused on methods for targeting CD44 in an attempt to improve drug delivery and discrimination between healthy and malignant tissue, while reducing residual toxicity and off-target accumulation. In this review, we describe CD44 receptor biology and its involvement in the different stages of tumor growth and metastasis, as well as methods currently used for targeting the receptor. Hyaluronic acid, the primary CD44 binding molecule, has proved a significant ally in developing nanocarriers that demonstrate preferential tumor accumulation and increased cell uptake. We outline a number of research approaches from the current literature that take advantage of hyaluronic acid's targeting ability and describe the possible advantages for each approach. The value of CD44 targeting can be easily appreciated from the number of different approaches that have reached clinical trials.
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HA is known to target overly expressed CD44 receptors in several tumors including MDA-MB-231 human breast cancer and A549 lung cancer.
“HA is known to target the overly expressed CD44 receptors in several tumors including MDA-MB-231 human breast cancer 41 and A549 lung cancer.42,43”
From Catalase-Integrated Hyaluronic Acid as Nanocarriers for Enhanced Photodynamic Therapy in Solid Tumor (2019) · cites this paper as [42]
Cites
Jemal, A., Siegel, R., Xu, J., & Ward, E. (2010) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.20073 · Cited by 12,596 · 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
McGuire, S. (2016) · Advances in Nutrition · doi:10.3945/an.116.012211 · Cited by 1,900 · see citing works
Molecular Definition of Breast Tumor Heterogeneity
Shipitsin, M. V., Campbell, L. L., Argani, P., Weremowicz, S., Bloushtain-Qimron, N., Yao, J., Nikolskaya, T., Serebryiskaya, T., Beroukhim, R., Hu, M., et al. (2007) · Cancer Cell · doi:10.1016/j.ccr.2007.01.013 · Cited by 1,358 · see citing works
CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?
Zöller, M. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3023 · Cited by 1,121 · see citing works
Functions of hyaluronan in wound repair
Chen, W. Y. J., & Abatangelo, G. (1999) · Wound Repair and Regeneration · doi:10.1046/j.1524-475x.1999.00079.x · Cited by 1,089 · see citing works
Hyaluronic acid: A key molecule in skin aging
Papakonstantinou, E., Roth, M., & Karakiulakis, G. (2012) · Dermato-Endocrinology · doi:10.4161/derm.21923 · Cited by 1,031 · see citing works
Targeted Drug Delivery via the Transferrin Receptor-Mediated Endocytosis Pathway
Qian, Z., Li, H., Sun, H., & Ho, K. (2002) · Pharmacological Reviews · doi:10.1124/pr.54.4.561 · Cited by 1,021 · see citing works
Screaton, G. R., Bell, M. V., Jackson, D. G., Cornélis, F., Gerth, U., & Bell, J. I. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.24.12160 · Cited by 1,016 · see citing works
Hyaluronic acid: a natural biopolymer with a broad range of biomedical and industrial applications
Kogan, G., Šoltés, L., Stern, R., & Gemeiner, P. (2006) · Biotechnology Letters · doi:10.1007/s10529-006-9219-z · Cited by 999 · see citing works
Hyaluronic acid (hyaluronan): A review
Necas, J., Bartosikova, L., Brauner, P., & Kolar, J. (2008) · Veterinární medicína · doi:10.17221/1930-vetmed · Cited by 998 · see citing works
Folate-mediated delivery of macromolecular anticancer therapeutic agents
Lu, Y. J., & Low, P. S. (2002) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(02)00042-x · Cited by 942 · see citing works
High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat
Tian, X., Azpurua, J., Hine, C., Vaidya, A. M., Myakishev-Rempel, M., Ablaeva, J., Mao, Z., Nevo, E., Gorbunova, V. A., & Seluanov, A. (2013) · Nature · doi:10.1038/nature12234 · Cited by 786 · see citing works
Graphene in Biomedicine: Opportunities and Challenges
Feng, L., & Liu, Z. (2011) · Nanomedicine · doi:10.2217/nnm.10.158 · Cited by 716 · see citing works
Schanté, C. E., Zuber, G., Herlin, C., & Vandamme, T. (2011) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2011.03.019 · Cited by 710 · see citing works
Resolution of Lung Inflammation by CD44
Teder, P., Vandivier, R. W., Jiang, D., Liang, J., Cohn, L. E., Puré, E., Henson, P. M., & Noble, P. W. (2002) · Science · doi:10.1126/science.1069659 · Cited by 676 · see citing works
Folate Receptor-Mediated Drug Targeting: From Therapeutics to Diagnostics
Hilgenbrink, A. R., & Low, P. S. (2005) · Journal of Pharmaceutical Sciences · doi:10.1002/jps.20457 · Cited by 625 · see citing works
The six hyaluronidase-like genes in the human and mouse genomes
Csoka, A. B., Frost, G. I., & Stern, R. (2001) · Matrix Biology · doi:10.1016/s0945-053x(01)00172-x · Cited by 590 · see citing works
Self-assembled hyaluronic acid nanoparticles for active tumor targeting
Choi, K. Y., Chung, H., Min, K. H., Yoon, H. Y., Kim, K., Park, J. H., Kwon, I. C., & Jeong, S. Y. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.09.030 · Cited by 580 · see citing works
Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro
Lee, R. J., & Low, P. S. (1995) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(94)00235-h · Cited by 575 · see citing works
Hyaluronan-binding Proteins: Tying Up the Giant
Day, A. J., & Prestwich, G. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.r100036200 · Cited by 567 · see citing works
Leamon, C. P. (2004) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2004.01.008 · Cited by 559 · see citing works
Hyaluronan–CD44 interactions as potential targets for cancer therapy
Misra, S., Heldin, P., Hascall, V. C., Karamanos, N. K., Skandalis, S. S., Markwald, R. R., & Ghatak, S. (2011) · The FEBS Journal · doi:10.1111/j.1742-4658.2011.08071.x · Cited by 494 · see citing works
Li, J., Huo, M., Wang, J., Zhou, J., Mohammad, J. M., Zhang, Y., Zhu, Q., Waddad, A. Y., & Zhang, Q. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2011.11.022 · Cited by 468 · see citing works
Hurt, E. M., Kawasaki, B. T., Klarmann, G. J., et al. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604242 · Cited by 440 · see citing works
Hyaluronate receptors: key players in growth, differentiation, migration and tumor progression
Sherman, L. S., Sleeman, J. P., Herrlich, P. A., & Ponta, H. (1994) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(94)90100-7 · Cited by 431 · see citing works
Hyaluronan and its binding proteins, the hyaladherins
Toole, B. P. (1990) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(90)90081-o · Cited by 428 · see citing works
Prestwich, G. D., Marecak, D. M., Marecek, J. F., Vercruysse, K. P., & Ziebell, M. R. (1998) · Journal of Controlled Release · doi:10.1016/s0168-3659(97)00242-3 · Cited by 423 · see citing works
Hyaluronic acid: the scientific and clinical evidence
Price, R. D., Berry, M. G., & Navsaria, H. A. (2007) · Journal of Plastic Reconstructive & Aesthetic Surgery · doi:10.1016/j.bjps.2007.03.005 · Cited by 413 · see citing works
The science of hyaluronic acid dermal fillers
Tezel, A., & Fredrickson, G. H. (2008) · Journal of Cosmetic and Laser Therapy · doi:10.1080/14764170701774901 · Cited by 405 · see citing works
Lee, R. J., & Huang, L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.14.8481 · Cited by 400 · 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
Ganesh, S., Iyer, A. K., Morrissey, D. V., & Amiji, M. M. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.01.077 · Cited by 361 · see citing works
Self-citationJiang, T., Zhang, Z.-H., Zhang, Y., Lv, H., Zhou, J., Li, C., Hou, L., & Zhang, Q. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.09.027 · Cited by 361 · see citing works
Role of integrated cancer nanomedicine in overcoming drug resistance
Iyer, A. K., Singh, A., Ganta, S., & Amiji, M. M. (2013) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2013.07.012 · Cited by 343 · see citing works
Self-citationYu, M., Jambhrunkar, S., Thorn, P., Chen, J., Gu, W., & Yu, C. (2012) · Nanoscale · doi:10.1039/c2nr32145a · Cited by 336 · see citing works
Fraser, J., Laurent, T. C., Pertoft, H., & Baxter, E. (1981) · Biochemical Journal · doi:10.1042/bj2000415 · Cited by 333 · see citing works
Eliaz, R. E., & Szoka, F. C. (2001) · PubMed · Cited by 330 · 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
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
Hyaluronan in human malignancies
Sironen, R. K., Tammi, M., Tammi, R., Auvinen, P., Anttila, M. A., & Kosma, V.-M. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.11.017 · Cited by 294 · see citing works
Selvaggi, G., Novello, S., Torri, V., Leonardo, E., Giuli, P. D., Borasio, P., Mossetti, C., Ardissone, F., Lausi, P. O., & Scagliotti, G. V. (2003) · Annals of Oncology · doi:10.1093/annonc/mdh011 · Cited by 293 · see citing works
Role, Metabolism, Chemical Modifications and Applications of Hyaluronan
Volpi, N., Schiller, J., Stern, R., & Šoltés, L. (2009) · Current Medicinal Chemistry · doi:10.2174/092986709788186138 · Cited by 279 · see citing works
Understanding the Dual Nature of CD44 in Breast Cancer Progression
Louderbough, J. M., & Schroeder, J. A. (2011) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-11-0156 · Cited by 274 · see citing works
Choi, K. Y., Min, K. H., Na, J. H., Choi, K., Kim, K., Park, J. H., Kwon, I. C., & Jeong, S. Y. (2009) · Journal of Materials Chemistry · doi:10.1039/b900456d · Cited by 272 · see citing works
Idowu, M. O., Kmieciak, M., Dumur, C. I., et al. (2011) · Human Pathology · doi:10.1016/j.humpath.2011.05.005 · Cited by 267 · see citing works
CD44-mediated uptake and degradation of hyaluronan
Knudson, W., Chow, G., & Knudson, C. B. (2002) · Matrix Biology · doi:10.1016/s0945-053x(01)00186-x · Cited by 258 · see citing works
Target Delivery and Cell Imaging Using Hyaluronic Acid-Functionalized Graphene Quantum Dots
Al‐Nahain, A., Lee, J., In, I., Lee, H., Lee, K. D., Jeong, J. H., & Park, S. Y. (2013) · Molecular Pharmaceutics · doi:10.1021/mp400219u · Cited by 258 · see citing works
Hiraga, T., Ito, S., & Nakamura, H. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3801 · Cited by 227 · see citing works
Targeting the Tumor Microenvironment in Cancer: Why Hyaluronidase Deserves a Second Look
Whatcott, C. J., Han, H., Posner, R. G., Hostetter, G. H., & Hoff, D. D. V. (2011) · Cancer Discovery · doi:10.1158/2159-8290.cd-11-0136 · Cited by 224 · see citing works
Molecular Identification of a Putative Human Hyaluronan Synthase
Watanabe, K., & Yamaguchi, Y. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.38.22945 · Cited by 205 · see citing works
Binding of hyaluronate to the surface of cultured cells.
Underhill, C. B., & Toole, B. P. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.82.2.475 · Cited by 202 · see citing works
Functionalizing Liposomes with anti-CD44 Aptamer for Selective Targeting of Cancer Cells
Alshaer, W., Hillaireau, H., Vergnaud, J., Ismail, S. I., & Fattal, E. (2014) · Bioconjugate Chemistry · doi:10.1021/bc5004313 · Cited by 200 · see citing works
Song, E., Han, W., Li, C., et al. (2014) · ACS Applied Materials & Interfaces · doi:10.1021/am502423r · Cited by 199 · see citing works
Riechelmann, H., Sauter, A., Golze, W., Hanft, G., Schroen, C., Hoermann, K., Erhardt, T., & Gronau, S. (2008) · Oral Oncology · doi:10.1016/j.oraloncology.2007.10.009 · Cited by 198 · see citing works
Regulation of alternative splicing of CD44 in cancer
Procházka, L., Tesařı́k, R., & Tuřánek, J. (2014) · Cellular Signalling · doi:10.1016/j.cellsig.2014.07.011 · Cited by 196 · see citing works
Wang, L., Su, W., Liu, Z., et al. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.03.067 · Cited by 194 · see citing works
Bioresponsive Hyaluronic Acid‐Capped Mesoporous Silica Nanoparticles for Targeted Drug Delivery
Chen, Z., Li, Z., Lin, Y., Yin, M., Ren, J., & Qu, X. (2013) · Chemistry - A European Journal · doi:10.1002/chem.201202038 · Cited by 180 · see citing works
Nanodelivery Strategies in Cancer Chemotherapy: Biological Rationale and Pharmaceutical Perspectives
Mattheolabakis, G., Rigas, B., & Constantinides, P. P. (2012) · Nanomedicine · doi:10.2217/nnm.12.128 · Cited by 177 · see citing works
Self-citationLi, F., Park, S., Ling, D., et al. (2013) · Journal of Materials Chemistry B · doi:10.1039/c3tb00506b · Cited by 175 · see citing works
Dawidczyk, C. M., Russell, L. M., & Searson, P. C. (2014) · Frontiers in Chemistry · doi:10.3389/fchem.2014.00069 · Cited by 165 · see citing works
Expression of CD44 in human lung tumors
Penno, M. B. (1994) · Lung Cancer · doi:10.1016/0169-5002(94)92213-6 · Cited by 164 · see citing works
Bertrand, P., Girard, N., Delpech, B., Duval, C., d'Anjou, J., & Dauce, J. P. (1992) · International Journal of Cancer · doi:10.1002/ijc.2910520102 · Cited by 160 · see citing works
Surace, C., Arpicco, S., Dufaÿ-Wojcicki, A., et al. (2009) · Molecular Pharmaceutics · doi:10.1021/mp800215d · Cited by 160 · see citing works
Yang, X., lyer, A., Singh, A., Choy, E., Hornicek, F. J., Amiji, M. M., & Duan, Z. (2015) · Scientific Reports · doi:10.1038/srep08509 · Cited by 159 · see citing works
Self-citationCytotoxicity of momordin-folate conjugates in cultured human cells.
Leamon, C. P., & Low, P. S. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)73992-1 · Cited by 142 · see citing works
Ganesh, S., Iyer, A. K., Gattacceca, F., Morrissey, D. V., & Amiji, M. M. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.10.016 · Cited by 142 · see citing works
Self-citationHyaluronan: Towards novel anti-cancer therapeutics
Karbownik, M. S., & Nowak, J. Z. (2013) · Pharmacological Reports · doi:10.1016/s1734-1140(13)71465-8 · Cited by 142 · see citing works
Ganesh, S., Iyer, A. K., Weiler, J., Morrissey, D. V., & Amiji, M. M. (2013) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2013.29 · Cited by 134 · see citing works
Self-citationHao, J., Chen, H., Madigan, M. C., Cozzi, P. J., Beretov, J., Xiao, W., Delprado, W., Russell, P. J., & Li, Y. (2010) · British Journal of Cancer · doi:10.1038/sj.bjc.6605839 · Cited by 119 · see citing works
Börjesson, P. K. E., Postema, E. J., Roos, J. C., Colnot, D. R., Marres, H. A. M., van Schie, M. H., Stehle, G., de Bree, R., Snow, G. B., Oyen, W. J. G., et al. (2003) · PubMed · Cited by 113 · see citing works
Chromosomal Localization of the Human and Mouse Hyaluronan Synthase Genes
Spicer, A. P., Seldin, M. F., Olsen, A. S., Brown, N., Wells, D. E., Doggett, N. A., Itano, N., Kimata, K., Inazawa, J., & McDonald, J. A. (1997) · Genomics · doi:10.1006/geno.1997.4696 · Cited by 108 · see citing works
Involvement of CD44 in cytoskeleton rearrangement and raft reorganization in T cells
Föger, N., Marhaba, R., & Zöller, M. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.6.1169 · Cited by 108 · see citing works
Bassi, P. F., Volpe, A., D’Agostino, D., et al. (2010) · The Journal of Urology · doi:10.1016/j.juro.2010.09.073 · Cited by 104 · see citing works
Selective Targeting of Malignant Cells with Cytotoxin-Folate Conjugates
Leamon, C. P., & Low, P. S. (1994) · Journal of drug targeting · doi:10.3109/10611869409015898 · Cited by 101 · see citing works
Jiang, H. N., Peterson, R. S., Wang, W., Bartnik, E., Knudson, C. B., & Knudson, W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m108654200 · Cited by 99 · see citing works
Rupp, U., Schoendorf-Holland, E., Eichbaum, M. H. R., Schütz, F., Lauschner, I., Schmidt, P., Staab, A., Hanft, G., Huober, J., Sinn, H., et al. (2007) · Anti-Cancer Drugs · doi:10.1097/cad.0b013e32801403f4 · Cited by 99 · see citing works
Xin, D., Wang, Y., & Xiang, J. (2009) · Pharmaceutical Research · doi:10.1007/s11095-009-9997-9 · Cited by 95 · see citing works
Ma, M., Chen, H., Chen, Y., Zhang, K., Wang, X., Cui, X., & Shi, J. (2012) · Journal of Materials Chemistry · doi:10.1039/c2jm15489g · Cited by 93 · see citing works
Banzato, A., Bobisse, S., Rondina, M. B., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-2019 · Cited by 92 · see citing works
CD44: A Cancer Stem Cell–Related Biomarker with Predictive Potential for Radiotherapy
Baumann, M. A., & Krause, M. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2244 · Cited by 89 · see citing works
Yang, X., Iyer, A. K., Singh, A., Milane, L. S., Choy, E., Hornicek, F. J., Amiji, M. M., & Duan, Z. (2014) · Pharmaceutical Research · doi:10.1007/s11095-014-1602-1 · Cited by 89 · see citing works
Self-citationThe structure and regulation of hyaluronan-binding proteins
Day, A. J. (1999) · Biochemical Society Transactions · doi:10.1042/bst0270115 · Cited by 86 · see citing works
Colnot, D. R., Quak, J. J., Roos, J. C., et al. (2000) · PubMed · Cited by 83 · see citing works
Stroomer, J. W. G., Roos, J. C., Sproll, M., et al. (2000) · PubMed · Cited by 78 · see citing works
Colnot, D. R., Roos, J. C., de Bree, R., Wilhelm, A. J., Kummer, J. A., Hanft, G., Heider, K., Stehle, G., Snow, G. B., & van Dongen, G. A. M. S. (2003) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-003-0396-5 · Cited by 72 · see citing works
Gvozdenovic, A., Arlt, M., Campanile, C., Brennecke, P., Husmann, K., Li, Y., Born, W., Muff, R., & Fuchs, B. (2012) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1817 · Cited by 70 · see citing works
Hiscox, S., Baruah, B. P., Smith, C. R., Bellerby, R., Goddard, L., Jordan, N., Poghosyan, Z. P., Nicholson, R. I., Barrett-Lee, P. J., & Gee, J. M. W. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-458 · Cited by 70 · see citing works
Serafino, A., Zonfrillo, M., Andreola, F., et al. (2011) · Current Cancer Drug Targets · doi:10.2174/156800911795655976 · Cited by 63 · see citing works
Gadhoum, Z., Delaunay, J., Maquarre, E., et al. (2004) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/1042819042000206687 · Cited by 61 · see citing works
Singh, A., Talekar, M., Tran, T.-H., Samanta, A., Sundaram, R., & Amiji, M. M. (2014) · Journal of Materials Chemistry B · doi:10.1039/c4tb01083c · Cited by 60 · see citing works
Self-citationLipid-Based Nanovectors for Targeting of CD44-Overexpressing Tumor Cells
Arpicco, S., Rosa, G. D., & Fattal, E. (2013) · Journal of Drug Delivery · doi:10.1155/2013/860780 · Cited by 59 · see citing works
Nano graphene oxide–hyaluronic acid conjugate for target specific cancer drug delivery
Jung, H. S., Lee, M., Kong, W. H., et al. (2014) · RSC Advances · doi:10.1039/c4ra00605d · Cited by 58 · see citing works
Jahn, M., Baynes, J., & Spiteller, G. (1999) · Carbohydrate Research · doi:10.1016/s0008-6215(99)00186-x · Cited by 58 · see citing works
Wei, H.-J., Yin, T., Zhu, Z., Shi, P.-F., Tian, Y., & Wang, C. (2011) · Hepatobiliary & pancreatic diseases international · doi:10.1016/s1499-3872(11)60073-8 · Cited by 57 · see citing works
Hyaluronan, a truly “youthful” polysaccharide. Its medical applications
Robert, L. (2014) · Pathologie Biologie · doi:10.1016/j.patbio.2014.05.019 · Cited by 54 · see citing works
The prognostic value of CD44 expression in gastric cancer: A meta-Analysis
Chen, Y., Fu, Z., Xu, S., et al. (2014) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2014.08.001 · Cited by 54 · see citing works
Schrevel, M., Gorter, A., Kolkman-Uljee, S. M., et al. (2011) · Modern Pathology · doi:10.1038/modpathol.2010.239 · Cited by 53 · see citing works
de Bree, R., Roos, J. C., Quak, J. J., et al. (1995) · PubMed · Cited by 51 · 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
Transferrin receptors in human cancerous tissues.
Niitsu, Y., Kohgo, Y., Nishisato, T., et al. (1987) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.153.239 · Cited by 48 · see citing works
Current research on hyaluronic acid-drug bioconjugates.
Zhang, H., Huang, S.-L., Yang, X.-Y., & Zhai, G. (2014) · European journal of medicinal chemistry · doi:10.1016/j.ejmech.2014.08.067 · Cited by 47 · see citing works
Postema, E. J., Börjesson, P. K. E., Buijs, W. C. A. M., et al. (2003) · PubMed · Cited by 42 · see citing works
Bahnassy, A. A., Fawzy, M., El-Wakil, M., et al. (2014) · Translational research · doi:10.1016/j.trsl.2014.07.009 · Cited by 42 · see citing works
Wang, Z., Shi, Q., Wang, Z., Gu, Y., Shen, Y., Sun, M.-M., Deng, M., Zhang, H., Junchu, F., Zhang, S., et al. (2011) · Pathology - Research and Practice · doi:10.1016/j.prp.2011.06.009 · Cited by 41 · see citing works
Nadella, V., Wang, Z., Johnson, T. S., Griffin, M., & Devitt, A. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.09.020 · Cited by 40 · see citing works
Montagner, I. M., Banzato, A., Zuccolotto, G., et al. (2012) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2012.01.005 · Cited by 38 · see citing works
Effects of hyaluronan on the invasive properties of human breast cancer cells in vitro
Herrera‐Gayol, A., & Jothy, S. (2001) · International Journal of Experimental Pathology · doi:10.1111/j.1365-2613.2001.iep196.x · Cited by 36 · see citing works
Effects of hyaluronan on the invasive properties of human breast cancer cells in vitro.
Herrera‐Gayol, A., & Jothy, S. (2001) · PubMed · doi:10.1046/j.1365-2613.2001.iep0082-0193-x · Cited by 34 · see citing works
Development of a fluorescent substrate to measure hyaluronidase activity
Zhang, L.-S., & Mummert, M. E. (2008) · Analytical Biochemistry · doi:10.1016/j.ab.2008.04.040 · Cited by 31 · see citing works
Colnot, D. R., Ossenkoppele, G. J., Roos, J. C., Quak, J. J., de Bree, R., Börjesson, P. K. E., Huijgens, P. C., Snow, G. B., & van Dongen, G. A. M. S. (2002) · PubMed · Cited by 29 · see citing works
CD44: survival and metastasis in chondrosarcoma
Heyse, T. J., Malcherczyk, D., Moll, R., et al. (2010) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2010.02.007 · Cited by 29 · see citing works
Yaron, M., Yaron, I., Smetana, O., et al. (1976) · Arthritis & Rheumatism · doi:10.1002/art.1780190612 · Cited by 27 · see citing works
Ndinguri, M. W., Zheleznyak, A., Lauer, J. L., Anderson, C. J., & Fields, G. B. (2012) · Journal of Drug Delivery · doi:10.1155/2012/592602 · Cited by 27 · see citing works
Pancreatic cancer cells express CD44 variant 9 and multidrug resistance protein 1 during mitosis
Kiuchi, S., Ikeshita, S., Miyatake, Y., et al. (2014) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2014.12.001 · Cited by 25 · see citing works
Zhang, P., Fu, C., Bai, H., Song, E., & Song, Y. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.10.027 · Cited by 23 · see citing works
Tanaka, T., Fujishima, Y., & Kaneo, Y. (2001) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.24.268 · Cited by 18 · see citing works
Miyatake, Y., Sheehy, N., Ikeshita, S., et al. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.11.055 · Cited by 16 · see citing works
Expression of the cell adhesion molecule CD44 in human lung tumors and cell lines*
RESNICK, N., CLARKE, M., Siegfried, J. M., et al. (1998) · Molecular Diagnosis · doi:10.1016/s1084-8592(98)80057-x · Cited by 15 · see citing works
Pharmacokinetic profile of Oncofid-S after intraperitoneal and intravenous administration in the rat
Tringali, G., Bettella, F., Greco, M. C., et al. (2011) · Journal of Pharmacy and Pharmacology · doi:10.1111/j.2042-7158.2011.01417.x · Cited by 13 · see citing works
Capodilupo, A., Crescenzi, V., Francescangeli, A., et al. (2003) · Padua Research Archive (University of Padova) · Cited by 6 · see citing works
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Wan, Y., Fu, L., Li, C., Lin, J., & Huang, P. (2021) · Advanced Materials · doi:10.1002/adma.202103978 · Cited by 705 · see citing works
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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
Lv, Y., Xu, C., Zhao, X., Lin, C., Yang, X., Xin, X., Zhang, L., Qin, C., Han, X., Yang, L., et al. (2018) · ACS Nano · doi:10.1021/acsnano.7b08051 · Cited by 235 · 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
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Singh, B., Maharjan, S., Pan, D. C., Zhao, Z., Gao, Y., Zhang, Y. S., & Mitragotri, S. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2021.121302 · Cited by 49 · see citing works
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Ding, X., Liang, Y., Zhou, S., Wu, Y., Sałata, P., Mikolajczk-Martinez, A., Khosrawipour, V., & Zhang, Z. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113786 · Cited by 20 · see citing works
- Authors
- Mattheolabakis, G., Milane, L., Singh, A., & Amiji, M. M.
- Affiliations
- Northeastern University (US)
- Corresponding author
- Amiji, Mansoor M.
- Venue
- Journal of Drug Targeting
- Publisher
- Informa UK Limited
- Published
- 2015-09-14
- Volume
- 23
- Issue
- 7-8
- Pages
- 605-618
- ISSN
- 1026-7158 (ISSN-L)
- 1061-186X
- 1029-2330
- OpenAlex
- W1909499926
- Cited by
- 597
- References
- 121
- Citations by year
- 2026: 51 · 2025: 67 · 2024: 64 · 2023: 71 · 2022: 89 · 2021: 73 · 2020: 52 · 2019: 48 · 2018: 46 · 2017: 25 · 2016: 11
- FWCI
- 2.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of drug targeting (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5u01ca151452-05)
- National Cancer Institute (U01- CA151452, R21CA179652)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Keywords
- CD44, hyaluronic acid, receptor targeting, tumor targeting, nanocarriers, drug delivery, metastasis, tumor growth, cancer therapy, clinical trials
- MeSH terms
- Animals, Antineoplastic Agents, Humans, Hyaluronic Acid, Neoplasms, Gene Expression Regulation, Neoplastic, Drug Delivery Systems, Hyaluronan Receptors, Nanoparticles
About these checks
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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