Emerging Roles for Hyaluronidase in Cancer Metastasis and Therapy
Open accessAbstract
Hyaluronidases are a family of five human enzymes that have been differentially implicated in the progression of many solid tumor types, both clinically and in functional studies. Advances in the past 5 years have clarified many apparent contradictions: (1) by demonstrating that specific hyaluronidases have alternative substrates to hyaluronan (HA) or do not exhibit any enzymatic activity, (2) that high-molecular weight HA polymers elicit signaling effects that are opposite those of the hyaluronidase-digested HA oligomers, and (3) that it is actually the combined overexpression of HA synthesizing enzymes with hyaluronidases that confers tumorigenic potential. This review examines the literature supporting these conclusions and discusses novel mechanisms by which hyaluronidases impact invasive tumor cell processes. In addition, a detailed structural and functional comparison of the hyaluronidases is presented with insights into substrate selectivity and potential for therapeutic targeting. Finally, technological advances in targeting hyaluronidase for tumor imaging and cancer therapy are summarized.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Hyaluronidase, γ-Glutamyltranspeptidase, prostate-specific antigen, Trysin, β-galactosidase, Azoreductase, etc. are also used in enzyme-stimulated response smart nano-delivery systems.
“In addition, hyaluronidase, γ-Glutamyltranspeptidase, prostate-specific antigen, Trysin, β-galactosidase, Azoreductase, etc. are also used in enzyme-stimulated response smart nano-delivery systems.157–162”
From Smart nanoparticles for cancer therapy (2023) · cites this paper as [158]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Tan, J., Wang, X., Su, X., Li, H., Shi, Y., Wang, L., & Ren, G.-S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022836 · Cited by 72 · see citing works
RetractedProtein structure prediction on the Web: a case study using the Phyre server
Kelley, L. A., & Sternberg, M. J. E. (2009) · Nature Protocols · doi:10.1038/nprot.2009.2 · Cited by 4,154 · see citing works
CD44 is the principal cell surface receptor for hyaluronate
Aruffo, A. A., Stamenkovic, I., Melnick, M., Underhill, C. B., & Seed, B. (1990) · Cell · doi:10.1016/0092-8674(90)90694-a · Cited by 2,439 · see citing works
Provenzano, P. P., Cuevas, C., Chang, A. E., Goel, V. K., Von Hoff, D. D., & Hingorani, S. R. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.01.007 · Cited by 2,195 · 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
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
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
Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties
Itano, N., Sawai, T., Yoshida, M., Lenas, P., Yamada, Y., Imagawa, M., Shinomura, T., Hamaguchi, M., Yoshida, Y., Ohnuki, Y., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.35.25085 · Cited by 901 · see citing works
Cancer Exosomes Trigger Fibroblast to Myofibroblast Differentiation
Webber, J. P., Steadman, R., Mason, M. D., Tabi, Z., & Clayton, A. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1722 · Cited by 850 · 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
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
Toole, B. P. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0244 · Cited by 571 · see citing works
The structure and function of hyaluronan: An overview
Laurent, T. C., Laurent, U. B. G., & Fraser, J. R. E. (1996) · Immunology and Cell Biology · doi:10.1038/icb.1996.32 · Cited by 506 · see citing works
Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes
Webber, J. P., Spary, L. K., Sanders, A. J., Chowdhury, R., Jiang, W. G., Steadman, R., Wymant, J. M., Jones, A. T., Kynaston, H., Mason, M. D., et al. (2014) · Oncogene · doi:10.1038/onc.2013.560 · Cited by 438 · see citing works
Jiang, 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
West, D. C., & Kumar, S. (1989) · Experimental Cell Research · doi:10.1016/0014-4827(89)90428-x · Cited by 357 · see citing works
Toole, B. P. (1997) · Journal of Internal Medicine · doi:10.1046/j.1365-2796.1997.00171.x · Cited by 325 · see citing works
Harada, H., & Takahashi, M. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m608358200 · Cited by 321 · see citing works
The High and Low Molecular Weight Forms of Hyaluronan Have Distinct Effects on CD44 Clustering
Yang, C., Cao, M., Liu, H., He, Y., Xu, J., Du, Y., Liu, Y., Wang, W., Cui, L., Hu, J., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.349209 · Cited by 310 · see citing works
Lokeshwar, V. B., RUBINOWICZ, D. M., Schroeder, G. L., Forgacs, E., Minna, J. D., Block, N. L., Nadji, M., & Lokeshwar, B. L. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008432200 · Cited by 303 · see citing works
Kosaki, R., Watanabe, K., & Yamaguchi, Y. (1999) · PubMed · Cited by 303 · see citing works
Lepperdinger, G., Strobl, B., & Kreil, G. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.35.22466 · Cited by 300 · 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
The role of hyaluronan in tumour neovascularization (review)
Rooney, P., Kumar, S., Ponting, J., & Wang, M. (1995) · International Journal of Cancer · doi:10.1002/ijc.2910600511 · Cited by 271 · see citing works
Host Matrix Modulation by Tumor Exosomes Promotes Motility and Invasiveness
Mu, W., Rana, S., & Zöller, M. (2013) · Neoplasia · doi:10.1593/neo.13786 · Cited by 248 · see citing works
Hyaluronan Enters Keratinocytes by a Novel Endocytic Route for Catabolism
Tammi, R., Rilla, K. J., Pienimäki, J.-P., MacCallum, D. K., Hogg, M. G., Luukkonen, M., Hascall, V., & Tammi, M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103481200 · Cited by 241 · see citing works
A novel PKC-regulated mechanism controls CD44–ezrin association and directional cell motility
Legg, J. W., LEWIS, C. A., Parsons, M., Ng, T., & Isacke, C. M. (2002) · Nature Cell Biology · doi:10.1038/ncb797 · Cited by 238 · see citing works
The over-expression of HAS2, Hyal-2 and CD44 is implicated in the invasiveness of breast cancer
Udabage, L., Brownlee, G. R., Nilsson, S. K., & Brown, T. J. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.07.026 · Cited by 223 · see citing works
Chao, K. L., Muthukumar, L., & Herzberg, O. (2007) · Biochemistry · doi:10.1021/bi700382g · Cited by 190 · see citing works
Radiation dose, chemotherapy and risk of osteosarcoma after solid tumours during childhood
Vu, B. L., de Vathaire, F., Shamsaldin, A., Hawkins, M. M., Grimaud, E., Hardiman, C., Diallo, I., Vassal, G., Bessa, E., Campbell, S., et al. (1998) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19980729)77:3 · Cited by 190 · 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 172 · see citing works
Benitez, A., Yates, T. J., López, L. E., Cerwinka, W. H., Bakkar, A., & Lokeshwar, V. B. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-4610 · Cited by 157 · see citing works
Simpson, M. A., Wilson, C. M., & McCarthy, J. B. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64245-9 · Cited by 151 · see citing works
Self-citationSpontaneous 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
Self-citationl-Ascorbic Acid 6-Hexadecanoate, a Potent Hyaluronidase Inhibitor
Botzki, A., Rigden, D. J., Braun, S. A., Nukui, M., Salmen, S., Hoechstetter, J., Bernhardt, G., Dove, S., Jedrzejas, M. J., & Buschauer, A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406146200 · Cited by 140 · see citing works
Itano, N., Sawai, T., Atsumi, F., Miyaishi, O., Taniguchi, S., Kannagi, R., Hamaguchi, M., & Kimata, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313178200 · Cited by 138 · see citing works
HYAL1 overexpression is correlated with the malignant behavior of human breast cancer
Tan, J., Wang, X., Li, H., Su, X., Wang, L., Liang, R., Zheng, K., & Ren, G. (2010) · International Journal of Cancer · doi:10.1002/ijc.25460 · Cited by 127 · see citing works
Kramer, M. W., Escudero, D. O., Lokeshwar, S. D., Golshani, R., Ekwenna, O., Acosta, K., Merseburger, A. S., Soloway, M. S., & Lokeshwar, V. B. (2010) · Cancer · doi:10.1002/cncr.25565 · Cited by 125 · see citing works
Bourguignon, L., Wong, G., Earle, C. A., & Xia, W. (2011) · Cytoskeleton · doi:10.1002/cm.20544 · Cited by 124 · 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
Hyaluronan production enhances shedding of plasma membrane-derived microvesicles
Rilla, K. J., Pasonen‐Seppänen, S., Deen, A. J., Koistinen, V., Wojciechowski, S., Oikari, S., Kärnä, R., Bart, G., Törrönen, K., Tammi, R., et al. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.05.021 · Cited by 119 · see citing works
Posey, J., Soloway, M. S., Eki̇ci̇, S., Sofer, M., Civantos, F., DUNCAN, R. C., & Lokeshwar, V. B. (2003) · PubMed · Cited by 117 · see citing works
Hyaluronidase Expression Induces Prostate Tumor Metastasis in an Orthotopic Mouse Model
Kovar, J. L., Johnson, M. A., Volcheck, W. M., Chen, J., & Simpson, M. A. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.060324 · Cited by 115 · see citing works
Self-citationPrognostic Impact of Hyaluronan and Its Regulators in Pancreatic Ductal Adenocarcinoma
Cheng, X., Sato, N., Kohi, S., & Yamaguchi, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080765 · Cited by 112 · see citing works
Quantitative imaging of lymph function
Sharma, R. G., Wang, W. J., Rasmussen, J. C., Joshi, A., Houston, J. P., Adams, K. E., Cameron, A. G., Shi, K., Kwon, S., Mawad, M. E., et al. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01223.2006 · Cited by 109 · see citing works
Kaneiwa, T., Mizumoto, S., Sugahara, K., & Yamada, S. (2009) · Glycobiology · doi:10.1093/glycob/cwp174 · Cited by 100 · see citing works
Li, R., Todd, N. W., Qiu, Q., Fan, T., Zhao, Y., Rodgers, W. H., Fang, H.-B., Katz, R. L., Stass, S. A., & Jiang, F. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1593 · Cited by 98 · see citing works
Eki̇ci̇, S., Cerwinka, W. H., DUNCAN, R. C., Gomez, P., Civantos, F., Soloway, M. S., & Lokeshwar, V. B. (2004) · International Journal of Cancer · doi:10.1002/ijc.20368 · Cited by 95 · see citing works
Danilkovitch‐Miagkova, A., Duh, F.-M. C., Kuzmin, I., Angeloni, D., Liu, S., Miller, A. D., & Lerman, M. I. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0837136100 · Cited by 94 · see citing works
Mok, H., Jeong, H., Kim, S.-J., & Chung, B. H. (2012) · Chemical Communications · doi:10.1039/c2cc33555g · Cited by 92 · see citing works
Twarock, S., Tammi, M., Savani, R. C., & Fischer, J. W. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.093146 · Cited by 91 · see citing works
Langevin, S. M., Koestler, D. C., Christensen, B. C., Butler, R. A., Wiencke, J. K., Nelson, H. H., Houseman, E. A., Marsit, C. J., & Kelsey, K. T. (2012) · Epigenetics · doi:10.4161/epi.7.3.19134 · Cited by 91 · see citing works
Regulation of Hyaluronidase Activity by Alternative mRNA Splicing
Lokeshwar, V. B., Schroeder, G. L., Carey, R. I., Soloway, M. S., & Iida, N. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203821200 · Cited by 89 · see citing works
Chondroitin Sulfate E Fragments Enhance CD44 Cleavage and CD44-Dependent Motility in Tumor Cells
Sugahara, K. N., Hirata, T., Tanaka, T. T., Ogino, S., Takeda, M., Terasawa, H., Shimada, I., Tamura, J.-I., ten Dam, G. B., Kuppevelt, T. H. V., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-6198 · Cited by 86 · see citing works
Hsu, L., Schultz, L., Hong, Q., Moer, K. V., Heath, J., Li, M.-Y., Lai, F.-J., Lin, S., Lee, M.-H., Lo, C.-P., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m806688200 · Cited by 85 · see citing works
Duterme, C., Mertens-Strijthagen, J., Tammi, M., & Flamion, B. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.044362 · Cited by 77 · see citing works
Kramer, M. W., Golshani, R., Merseburger, A. S., Knapp, J., García, A., Hennenlotter, J., DUNCAN, R. C., Soloway, M. S., Jordà, M., Kuczyk, M. A., et al. (2009) · European Urology · doi:10.1016/j.eururo.2009.03.057 · Cited by 76 · see citing works
Strong Stromal Hyaluronan Expression Is Associated with PSA Recurrence in Local Prostate Cancer
Aaltomaa, S. H., Lipponen, P., Tammi, R., Tammi, M., Viitanen, J., Kankkunen, J.-P., & Kosma, V. M. (2002) · Urologia Internationalis · doi:10.1159/000066123 · Cited by 75 · see citing works
Hyaluronidase 3 (HYAL3) knockout mice do not display evidence of hyaluronan accumulation
Atmuri, V., Martin, D. C., Hemming, R., Gutsol, A. A., Byers, S., Sahebjam, S., Thliveris, J. A., Mort, J. S., Carmona, E., Anderson, J. E., et al. (2008) · Matrix Biology · doi:10.1016/j.matbio.2008.07.006 · Cited by 72 · see citing works
Novak, U., Stylli, S. S., Kaye, A. H., & Lepperdinger, G. (1999) · PubMed · Cited by 71 · see citing works
Simpson, M. A. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.060032 · Cited by 71 · see citing works
Self-citationEnegd, 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
Expression of PH-20 in Normal and Neoplastic Breast Tissue
Beech, D. J., Madan, A. K., & Deng, N. (2002) · Journal of Surgical Research · doi:10.1006/jsre.2002.6351 · Cited by 69 · see citing works
Hyaluronidase Activity of Human Hyal1 Requires Active Site Acidic and Tyrosine Residues
Zhang, L., Bharadwaj, A. G., Casper, A., Barkley, J., Barycki, J. J., & Simpson, M. A. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m900210200 · Cited by 68 · see citing works
Self-citationLiu, S., Duh, F.-M. C., Lerman, M. I., & Miller, A. D. (2003) · Journal of Virology · doi:10.1128/jvi.77.5.2850-2858.2003 · Cited by 68 · see citing works
Bharadwaj, A. G., Rector, K., & Simpson, M. A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702964200 · Cited by 66 · see citing works
Self-citationInvolvement of hyaluronidases in colorectal cancer
Bouga, H., Tsouros, I., Bounias, D., Kyriakopoulou, D., Stavropoulos, M., Papageorgakopoulou, N., Theocharis, D. A., & Vynios, D. H. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-499 · Cited by 66 · see citing works
Nykopp, T. K., Rilla, K. J., Tammi, M., Tammi, R., Sironen, R. K., Hämäläinen, K. M., Kosma, V., Heinonen, S. T., & Anttila, M. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-512 · Cited by 65 · see citing works
Honda, T., Kaneiwa, T., Mizumoto, S., Sugahara, K., & Yamada, S. (2012) · Biomolecules · doi:10.3390/biom2040549 · Cited by 64 · see citing works
Lokeshwar, V. B., Estrella, V. C., López, L. E., Kramer, M. W., Gomez, P., Soloway, M. S., & Lokeshwar, B. L. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1121 · Cited by 62 · see citing works
Hemming, R., Martin, D. C., Slominski, E., Nagy, J. I., Halayko, A. J., Pind, S., & Triggs‐Raine, B. L. (2008) · Glycobiology · doi:10.1093/glycob/cwn006 · Cited by 62 · see citing works
Expression of WW domain-containing oxidoreductase WOX1 in the developing murine nervous system
Chen, S.-T., Chuang, J., Wang, J. P., Tsai, M., Li, H., & Chang, N. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.036 · Cited by 61 · see citing works
Patel, S. K., Turner, P. R., Stubberfield, C. R., Barry, E., Rohlff, C., Stamps, A. C., Tyson, K. L., Terrett, J., Box, G., Eccles, S. A., et al. (2001) · International Journal of Cancer · doi:10.1002/ijc.1638 · Cited by 60 · see citing works
Magnetic Resonance Imaging Visualization of Hyaluronidase in Ovarian Carcinoma
Shiftan, L., Israely, T., Cohen, M., Frydman, V., Dafni, H., Stern, R., & Neeman, M. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3947 · Cited by 59 · see citing works
Nykopp, T. K., Rilla, K. J., Sironen, R. K., Tammi, M., Tammi, R., Hämäläinen, K. M., Heikkinen, A. M., Komulainen, M. H., Kosma, V., & Anttila, M. (2009) · BMC Cancer · doi:10.1186/1471-2407-9-143 · Cited by 58 · see citing works
Hyaluronated nanoparticles with pH- and enzyme-responsive drug release properties
Kim, S. W., Oh, K. T., Youn, Y. S., & Lee, E. S. (2014) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2014.01.017 · Cited by 57 · see citing works
Godin, D. A., Fitzpatrick, P. C., Scandurro, A. B., Belafsky, P. C., Woodworth, B. A., Amedee, R. G., Beech, D. J., & Beckman, B. S. (2000) · Archives of Otolaryngology - Head and Neck Surgery · doi:10.1001/archotol.126.3.402 · Cited by 55 · see citing works
Molecular characterization of kidney cancer
Chi, A. S., Shirodkar, S. P., Escudero, D. O., Ekwenna, O., Yates, T. J., Ayyathurai, R., Garcia-Roig, M. L., Gahan, J. C., Manoharan, M., Bird, V. G., et al. (2011) · Cancer · doi:10.1002/cncr.26520 · Cited by 55 · see citing works
Hyal2 is a glycosylphosphatidylinositol-anchored, lipid raft-associated hyaluronidase
Andre, B., Duterme, C., Moer, K. V., Mertens-Strijthagen, J., Jadot, M., & Flamion, B. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.06.125 · Cited by 54 · see citing works
Inhibition of Hyaluronidase by Fully O-Sulfonated Glycosaminoglycans
Toida, T., Ogita, Y., Suzuki, A., Toyoda, H., & Imanari, T. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1395 · Cited by 53 · see citing works
Association of hyaluronidase and breast adenocarcinoma invasiveness.
Madan, A. K., Yu, K., Dhurandhar, N. R., Cullinane, C. M., Pang, Y. K., & Beech, D. J. (1999) · Oncology Reports · doi:10.3892/or.6.3.607 · Cited by 52 · see citing works
Therapeutic potential of hyaluronan oligosaccharides for bone metastasis of breast cancer
Urakawa, H., Nishida, Y., Knudson, W., Knudson, C. B., Arai, E., Kozawa, E., Futamura, N., Wasa, J., & Ishiguro, N. (2011) · Journal of Orthopaedic Research® · doi:10.1002/jor.21557 · Cited by 52 · see citing works
Differential selectivity of hyaluronidase inhibitors toward acidic and basic hyaluronidases
Isoyama, T., Thwaites, D., Selzer, M. G., Carey, R. I., Barbucci, R., & Lokeshwar, V. B. (2005) · Glycobiology · doi:10.1093/glycob/cwj036 · Cited by 52 · see citing works
Signaling from membrane receptors to tumor suppressor WW domain-containing oxidoreductase
Chang, J.-Y., He, R., Lin, H., Hsu, L., Lai, F., Hong, Q., Chen, S.-J., & Chang, N. (2010) · Experimental Biology and Medicine · doi:10.1258/ebm.2010.009351 · Cited by 51 · see citing works
Hyaluronic Acid and HYAL-1 in Prostate Biopsy Specimens: Predictors of Biochemical Recurrence
Gomez, C. S., Gomez, P., Knapp, J., Jordà, M., Soloway, M. S., & Lokeshwar, V. B. (2009) · The Journal of Urology · doi:10.1016/j.juro.2009.06.070 · Cited by 47 · see citing works
Vigdorovich, V. I., Strong, R. K., & Miller, A. D. (2004) · Journal of Virology · doi:10.1128/jvi.79.1.79-86.2005 · Cited by 47 · see citing works
Hofinger, E. S. A., Spickenreither, M., Oschmann, J., Bernhardt, G., Rudolph, R., & Buschauer, A. (2007) · Glycobiology · doi:10.1093/glycob/cwm003 · Cited by 45 · see citing works
Subcellular Trafficking and Activity of Hyal‐1 and Its Processed Forms in Murine Macrophages
Emeline, P., Gilis, F., Dogné, S., Flamion, B., Jadot, M., & Boonen, M. (2014) · Traffic · doi:10.1111/tra.12162 · Cited by 43 · see citing works
Chang, N. (2002) · BMC Cell Biology · doi:10.1186/1471-2121-3-8 · Cited by 43 · see citing works
Siiskonen, H., Poukka, M., Tyynelä-Korhonen, K., Sironen, R. K., & Pasonen‐Seppänen, S. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-181 · Cited by 42 · see citing works
Expression of HYAL1 and Survivin RNA as Diagnostic Molecular Markers for Bladder Cancer
Eissa, S., Swellam, M. M., Shehata, H. H., El‐Khouly, I. M., El-Zayat, T. M., & El-Ahmady, O. (2009) · The Journal of Urology · doi:10.1016/j.juro.2009.10.024 · Cited by 41 · see citing works
Stimulation of TLR4 by LMW-HA Induces Metastasis in Human Papillary Thyroid Carcinoma through CXCR7
Dang, S., Peng, Y., Ye, L., Wang, Y., Qian, Z., Chen, Y., Wang, X., Lin, Y., Zhang, X., Sun, X., et al. (2013) · Clinical and Developmental Immunology · doi:10.1155/2013/712561 · Cited by 39 · see citing works
McAtee, C. O., Berkebile, A. R., Elowsky, C. G., Fangman, T., Barycki, J. J., Wahl, J. K., Khalimonchuk, O., Naslavsky, N., Caplan, S., & Simpson, M. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.647446 · Cited by 36 · see citing works
Self-citationKaneiwa, T., Miyazaki, A., Kogawa, R., Mizumoto, S., Sugahara, K., & Yamada, S. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.360693 · Cited by 36 · see citing works
Hyaluronan : structure, metabolism, biological activities, therapeutic applications
Balazs, E. A., & Hascall, V. (2005) · Medical Entomology and Zoology · Cited by 35 · see citing works
Distinct Genomic Aberrations between Low-Grade and High-Grade Gliomas of Chinese Patients
Li, Y., Wang, D., Wang, L., Yu, J., Dan-hua, D., Chen, Y., Gao, P., Wang, D.-M., Yu, J. M., Zhang, F., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057168 · Cited by 35 · see citing works
Ohnuma, S., Miura, K., Horii, A., Fujibuchi, W., Kaneko, N., Gotoh, O., Nagasaki, H., Mizoi, T., Tsukamoto, N., Kobayashi, T., et al. (2008) · Surgery · doi:10.1016/j.surg.2008.08.010 · Cited by 34 · see citing works
Subtype Specific Elevated Expression of Hyaluronidase-1 (HYAL-1) in Epithelial Ovarian Cancer
Yoffou, P. H., Edjekouane, L., Meunier, L., Tremblay, A., Provencher, D. M., Mes‐Masson, A., & Carmona, E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020705 · Cited by 33 · see citing works
Berdiaki, A., Nikitovic, D., Tsatsakis, A. M., Katonis, P., Karamanos, N. K., & Tzanakakis, G. N. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.06.013 · Cited by 32 · see citing works
Size-dependent regulation of Snail2 by hyaluronan: Its role in cellular invasion
Craig, E. A., Parker, P., & Camenisch, T. D. (2009) · Glycobiology · doi:10.1093/glycob/cwp064 · Cited by 28 · see citing works
Research Letter: New Potent Indole Derivatives as Hyaluronidase Inhibitors
Ölgen, S., Kaeßler, A., Nebioğlu, D., & Jose, J. (2007) · Chemical Biology & Drug Design · doi:10.1111/j.1747-0285.2007.00590.x · Cited by 27 · see citing works
Increased hyaluronidase expression in more aggressive prostate adenocarcinoma.
Madan, A. K., Pang, Y. K., Wilkiemeyer, M. B., Yu, D. C., & Beech, D. J. (1999) · Oncology Reports · doi:10.3892/or.6.6.1431 · Cited by 26 · see citing works
Molecular Risk Assessment for Breast Cancer Development in Patients with Ductal Hyperplasias
Poola, I., Abraham, J., Marshalleck, J. J., Yue, Q., Lokeshwar, V. B., Bonney, G. E., & DeWitty, R. L. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4053 · Cited by 26 · see citing works
Autodisplay of catalytically active human hyaluronidase hPH-20 and testing of enzyme inhibitors
Kaeßler, A., Ölgen, S., & Jose, J. (2010) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2010.11.004 · Cited by 24 · see citing works
Hyaluronidases and their inhibitors in the serum of colorectal carcinoma patients
Kolliopoulos, C., Bounias, D., Bouga, H., Kyriakopoulou, D., Stavropoulos, M., & Vynios, D. H. (2013) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2013.05.037 · Cited by 23 · see citing works
Eissa, S., Zohny, S. F., Shehata, H. H., Hegazy, M. G. A., Salem, A. M. H., & Esmat, M. E. (2012) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2012.01.010 · Cited by 21 · see citing works
Harigaya, K. (2011) · International Journal of Oncology · doi:10.3892/ijo.2011.1114 · Cited by 21 · see citing works
Udabage, L., Brownlee, G. R., Stern, R., & Brown, T. J. (2003) · Glycoconjugate Journal · doi:10.1023/b:glyc.0000038292.71098.35 · Cited by 21 · see citing works
Kinetic analysis of hyaluronidase activity using a bioactive MRI contrast agent
Shiftan, L., & Neeman, M. (2006) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.96 · Cited by 21 · see citing works
Chib, R., Raut, S., Fudala, R., Chang, A., Mummert, M. E., Rich, R., Gryczynski, Z. K., & Gryczyński, I. (2013) · Current Pharmaceutical Biotechnology · doi:10.2174/13892010113149990222 · Cited by 20 · see citing works
Molecular mechanisms and imaging of lymphatic metastasis
Proulx, S. T., & Detmar, M. J. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.03.009 · Cited by 20 · see citing works
Eissa, S., Shehata, H. H., Mansour, A., Esmat, M. E., & El-Ahmady, O. (2012) · Medical Oncology · doi:10.1007/s12032-012-0295-8 · Cited by 19 · see citing works
de Sá, V. K., Olivieri, E. H. R., Parra, E. R., Ab’Saber, A. M., Takagaki, T. Y., Soares, F. A., Carraro, D. M., Carvalho, L., & Capelozzi, V. L. (2011) · Human Pathology · doi:10.1016/j.humpath.2011.06.010 · Cited by 18 · see citing works
Bharadwaj, A. G., Goodrich, N. P., McAtee, C. O., Haferbier, K. L., Oakley, G. G., Wahl, J. K., & Simpson, M. A. (2011) · Experimental Cell Research · doi:10.1016/j.yexcr.2011.01.026 · Cited by 17 · see citing works
Self-citationRich, R. M., Mummert, M. E., Földes‐Papp, Z., Gryczynski, Z. K., Borejdo, J., Gryczyński, I., & Fudala, R. (2012) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2012.07.007 · Cited by 16 · see citing works
Duh, F.-M. C., Dirks, C., Lerman, M. I., & Miller, A. D. (2005) · Retrovirology · doi:10.1186/1742-4690-2-59 · Cited by 13 · see citing works
Nodular basal cell carcinoma is associated with increased hyaluronan homeostasis
Tzellos, T., Kyrgidis, Α., Vahtsevanos, K., Triaridis, S., Printza, A., Klagas, I., Zvintzou, E., Κritis, A., Karakiulakis, G., & Papakonstantinou, E. (2010) · Journal of the European Academy of Dermatology and Venereology · doi:10.1111/j.1468-3083.2010.03851.x · Cited by 11 · see citing works
Designed Human Serum Hyaluronidase 1 Variant, HYAL1ΔL, Exhibits Activity up to pH 5.9
Reitinger, S., Müllegger, J., Greiderer‐Kleinlercher, B., Nielsen, J. E., & Lepperdinger, G. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.c109.004358 · Cited by 10 · see citing works
Role of the extracellular matrix in variations of invasive pathways in lung cancers
de Sá, V. K., Carvalho, L., Gomes, A., Alarcão, A., Silva, M. R., Couceiro, P., de Sousa, V. M. L., Soares, F. A., & Capelozzi, V. L. (2013) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20122263 · Cited by 10 · see citing works
Investigation of Aminomethyl Indole Derivatives as Hyaluronidase Inhibitors
Ölgen, S., Kaeßler, A., Kılıç-Kurt, Z., & Jose, J. (2010) · Zeitschrift für Naturforschung C · doi:10.1515/znc-2010-7-805 · Cited by 6 · see citing works
Isoforms of hyaluronidases can be a predictor of a prostate cancer of good prognosis
de Sá, V. K., Canavez, F., da Silva, I. A., Srougi, M., & Leite, K. R. M. (2008) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2008.04.013 · Cited by 6 · see citing works
Analysis of HYAL3 Gene Mutations in Chinese Lung Squamous Cell Carcinoma Patients
Zhang, R., Zhu, J.-H., Fan, J., & Ji, X. (2013) · Tumori Journal · doi:10.1177/030089161309900118 · Cited by 5 · see citing works
Flagged first, then by citations
4 of the 127 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Godin DA Fitzpatrick PC Scandurro AB Belafsky PC Woodworth BA Amedee RG 2000 PH20: a novel tumor marker for laryngeal cancer Arch Otolaryngol Head Neck Surg 126 402 404 10722016
Cited by
Sorted by citations
Role of Extracellular Matrix in Development and Cancer Progression
Walker, C., Mojares, E., & Hernández, A. E. D. R. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103028 · Cited by 1,103 · see citing works
Smart nanoparticles for cancer therapy
Sun, L., Liu, H., Ye, Y., Lei, Y., Islam, R., Tan, S., Tong, R., Miao, Y.-B., & Cai, L. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01642-x · Cited by 1,073 · see citing works
3D Cell Culture Systems: Tumor Application, Advantages, and Disadvantages
Habanjar, O., Diab‐Assaf, M., Caldefie‐Chezet, F., & Delort, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212200 · Cited by 556 · see citing works
Xie, J., Bi, Y., Zhang, H., Dong, S., Teng, L., Lee, R. J., & Yang, Z. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00697 · Cited by 470 · see citing works
Hyaluronan biology: A complex balancing act of structure, function, location and context
Garantziotis, S., & Savani, R. C. (2019) · Matrix Biology · doi:10.1016/j.matbio.2019.02.002 · Cited by 390 · see citing works
Development and application of hyaluronic acid in tumor targeting drug delivery
Luo, Z., Dai, Y., & Gao, H. (2019) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2019.06.004 · Cited by 390 · see citing works
Proteoglycan Chemical Diversity Drives Multifunctional Cell Regulation and Therapeutics
Karamanos, N. K., Piperigkou, Z., Theocharis, A. D., Watanabe, H., Franchi, M., Baud, S., Brézillon, S., Götte, M., Passi, A. G., Vigetti, D., et al. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00354 · Cited by 372 · see citing works
Graphene‐Based Smart Platforms for Combined Cancer Therapy
Gu, Z., Zhu, S., Yan, L., Zhao, F., & Zhao, Y. (2018) · Advanced Materials · doi:10.1002/adma.201800662 · Cited by 334 · see citing works
Choi, K. Y., Han, H. S., Lee, E. S., Shin, J. M., Almquist, B. D., Lee, D. S., & Park, J. H. (2019) · Advanced Materials · doi:10.1002/adma.201803549 · Cited by 320 · see citing works
Hyaluronan as a therapeutic target in human diseases
Liang, J., Jiang, D., & Noble, P. W. (2015) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.10.017 · Cited by 239 · see citing works
Tumor microenvironment responsive drug delivery systems
He, Q., Chen, J., Yan, J., Cai, S., Xiong, H., Liu, Y., Peng, D., Mo, M., & Liu, Z. (2019) · Asian Journal of Pharmaceutical Sciences · doi:10.1016/j.ajps.2019.08.003 · Cited by 222 · see citing works
Transposable Elements in Human Cancer: Causes and Consequences of Deregulation
Anwar, S. L., Wulaningsih, W., & Lehmann, U. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18050974 · Cited by 192 · see citing works
Tumor Abnormality-Oriented Nanomedicine Design
Zhou, Q., Xiang, J., Qiu, N., Wang, Y., Piao, Y., Shao, S., Tang, J., Zhou, Z., & Shen, Y. (2023) · Chemical Reviews · doi:10.1021/acs.chemrev.3c00062 · Cited by 194 · see citing works
Hyaluronan – A Functional and Structural Sweet Spot in the Tissue Microenvironment
Monslow, J., Govindaraju, P. K., & Puré, E. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00231 · Cited by 182 · see citing works
Nanocarrier cancer therapeutics with functional stimuli-responsive mechanisms
Kaushik, N., Borkar, S. B., Nandanwar, S., Panda, P. K., Choi, E. H., & Kaushik, N. K. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-022-01364-2 · Cited by 189 · see citing works
Hyaluronic Acid: Incorporating the Bio into the Material
Wolf, K. J., & Kumar, S. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b01268 · Cited by 178 · see citing works
Pawłowska, E., Szczepańska, J., & Błasiak, J. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/7286737 · Cited by 174 · see citing works
Physical biology of the cancer cell glycocalyx
Kuo, J. C., Gandhi, J. G., Zia, R. N., & Paszek, M. J. (2018) · Nature Physics · doi:10.1038/s41567-018-0186-9 · Cited by 160 · see citing works
Dissecting the Dual Nature of Hyaluronan in the Tumor Microenvironment
Liu, M., Tölg, C., & Turley, E. A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00947 · Cited by 158 · see citing works
Nanogels for intracellular delivery of biotherapeutics
Li, D., van Nostrum, C. F., Mastrobattista, E., Vermonden, T., & Hennink, W. E. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.12.020 · Cited by 161 · see citing works
Digesting a Path Forward: The Utility of Collagenase Tumor Treatment for Improved Drug Delivery
Dolor, A., & Szoka, F. C. (2018) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.8b00319 · Cited by 141 · see citing works
Inflammation, Extracellular Matrix Remodeling, and Proteostasis in Tumor Microenvironment
Marozzi, M., Parnigoni, A., Negri, A., Viola, M., Vigetti, D., Passi, A. G., Karousou, E. G., & Rizzi, F. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158102 · Cited by 136 · see citing works
Hyaluronan, Cancer-Associated Fibroblasts and the Tumor Microenvironment in Malignant Progression
McCarthy, J. B., El‐Ashry, D., & Turley, E. A. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00048 · Cited by 128 · see citing works
Cong, V. T., Houng, J. L., Kavallaris, M., Chen, X., Tilley, R. D., & Gooding, J. J. (2022) · Chemical Society Reviews · doi:10.1039/d1cs00707f · Cited by 124 · see citing works
Oncolytic viruses: overcoming translational challenges
Martínez‐Quintanilla, J., Seah, I. Y. J., Chua, M. M. J., & Shah, K. (2019) · Journal of Clinical Investigation · doi:10.1172/jci122287 · Cited by 119 · see citing works
Responsive crosslinked polymer nanogels for imaging and therapeutics delivery
Ekkelenkamp, A. E., Elzes, M. R., Engbersen, J. F. J., & Paulusse, J. M. J. (2017) · Journal of Materials Chemistry B · doi:10.1039/c7tb02239e · Cited by 119 · see citing works
Towards extracellular matrix normalization for improved treatment of solid tumors
Abyaneh, H. S., Regenold, M., McKee, T. D., Allen, C. J., & Gauthier, M. A. (2020) · Theranostics · doi:10.7150/thno.39995 · Cited by 117 · see citing works
Natural Ingredient-Based Polymeric Nanoparticles for Cancer Treatment
Wong, K. H., Lü, A., Chen, X., & Yang, Z. (2020) · Molecules · doi:10.3390/molecules25163620 · Cited by 115 · see citing works
Cancer Microenvironment and Inflammation: Role of Hyaluronan
Nikitovic, D., Tzardi, M. N., Berdiaki, A., Tsatsakis, A. M., & Tzanakakis, G. N. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00169 · Cited by 111 · see citing works
Extracellular matrix proteomics in schizophrenia and Alzheimer’s disease
Sethi, M. K., & Zaia, J. (2016) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-016-9900-6 · Cited by 109 · see citing works
Hyaluronan as tunable drug delivery system
Passi, A. G., & Vigetti, D. (2019) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2019.08.006 · Cited by 112 · see citing works
Enzyme-triggered, cell penetrating peptide-mediated delivery of anti-tumor agents
He, H., Sun, L., Ye, J., Liu, E., Chen, S., Liang, Q., Shin, M. C., & Yang, V. C.-M. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.10.040 · Cited by 111 · see citing works
Cell Energy Metabolism and Hyaluronan Synthesis
Caon, I., Parnigoni, A., Viola, M., Karousou, E. G., Passi, A. G., & Vigetti, D. (2020) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155420929772 · Cited by 109 · see citing works
Charge‐Reversible Nanoparticles: Advanced Delivery Systems for Therapy and Diagnosis
Veider, F., Armengol, E. S., & Bernkop‐Schnürch, A. (2023) · Small · doi:10.1002/smll.202304713 · Cited by 108 · see citing works
Activatable Phototheranostic Materials for Imaging-Guided Cancer Therapy
Cheng, P., & Pu, K. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b15064 · Cited by 107 · see citing works
Jurj, A. M., Ionescu, C., Berindan‐Neagoe, I., & Braicu, C. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02484-1 · Cited by 109 · see citing works
Hyaluronic Acid as a Modern Approach in Anticancer Therapy-Review
Michalczyk, M., Humeniuk, E., Adamczuk, G., & Korga-Plewko, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms24010103 · Cited by 106 · see citing works
Wang, Y., Zhang, W., Sun, P., Cai, Y., Xu, W., Fan, Q., Hu, Q., & Han, W. (2019) · Theranostics · doi:10.7150/thno.30268 · Cited by 97 · see citing works
Differing Roles of Hyaluronan Molecular Weight on Cancer Cell Behavior and Chemotherapy Resistance
Price, Z. K., Lokman, N. A., & Ricciardelli, C. (2018) · Cancers · doi:10.3390/cancers10120482 · Cited by 98 · see citing works
Lin, G., Revia, R. A., & Zhang, M. (2020) · Advanced Functional Materials · doi:10.1002/adfm.202007096 · Cited by 97 · see citing works
Ramamonjisoa, N., & Ackerstaff, E. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00003 · Cited by 93 · see citing works
A Trickster in Disguise: Hyaluronan’s Ambivalent Roles in the Matrix
Bohaumilitzky, L., Huber, A., Stork, E. M., Wengert, S., Woelfl, F., & Boehm, H. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00242 · Cited by 91 · see citing works
Glycosylation and Cancer: Moving Glycomics to the Forefront
Drake, R. R. (2015) · Advances in cancer research · doi:10.1016/bs.acr.2014.12.002 · Cited by 87 · see citing works
The DNMT1-PAS1-PH20 axis drives breast cancer growth and metastasis
Fu, Y., Zhang, X., Liu, X., Wang, P., Chu, W., Zhao, W., Wang, Y., Zhou, G., Yu, Y., & Zhang, H. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00896-1 · Cited by 88 · see citing works
Grass, G. D., Dai, L., Qin, Z., Parsons, C. H., & Toole, B. P. (2014) · Advances in cancer research · doi:10.1016/b978-0-12-800092-2.00013-7 · Cited by 82 · see citing works
Enzyme-responsive smart nanocarriers for targeted chemotherapy: an overview
Kapalatiya, H., Madav, Y., Tambe, V. S., & Wairkar, S. (2021) · Drug Delivery and Translational Research · doi:10.1007/s13346-021-01020-6 · Cited by 81 · see citing works
Carcinoma Cell Hyaluronan as a “Portable” Cancerized Prometastatic Microenvironment
Turley, E. A., Wood, D. K., & McCarthy, J. B. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-3114 · Cited by 77 · see citing works
Hyaluronic Acid Nanoparticles as Nanomedicine for Treatment of Inflammatory Diseases
Rao, N. V., Rho, J. G., Um, W., Ek, P. K., Nguyen, V. Q., Oh, B. H., Kim, W., & Park, J. H. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12100931 · Cited by 78 · see citing works
Lai, H., Ding, X., Ye, J., Deng, J., & Cui, S. (2020) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2020.111455 · Cited by 76 · see citing works
Hyaluronidase: structure, mechanism of action, diseases and therapeutic targets
Lu, J., Zhao, Z., Pan, L., Wu, H. C., Wang, S., Tong, X., & Wu, S. (2025) · Molecular Biomedicine · doi:10.1186/s43556-025-00299-y · Cited by 82 · see citing works
Hyaluronan in adipogenesis, adipose tissue physiology and systemic metabolism
Zhu, Y., Kruglikov, I. L., Akgul, Y., & Scherer, P. E. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.02.012 · Cited by 75 · see citing works
McAtee, C. O., Booth, C. S., Elowsky, C. G., Zhao, L. Q., Payne, J., Fangman, T., Caplan, S., Henry, M. D., & Simpson, M. A. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.05.002 · Cited by 72 · see citing works
Self-citationHyaluronic acid family in bladder cancer: potential prognostic biomarkers and therapeutic targets
Morera, D. S., Hennig, M., Talukder, A. M., Lokeshwar, S. D., Wang, J., Garcia-Roig, M. L., Ortiz, N., Yates, T. J., López, L. E., Kallifatidis, G., et al. (2017) · British Journal of Cancer · doi:10.1038/bjc.2017.318 · Cited by 71 · see citing works
A tumor-penetrating peptide enhances circulation-independent targeting of peritoneal carcinomatosis
Sugahara, K. N., Scodeller, P., Braun, G. B., de Mendoza, T. H., Yamazaki, C. M., Kluger, M. D., Kitayama, J., Alvarez, E. A., Howell, S. B., Teesalu, T., et al. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.06.009 · Cited by 70 · see citing works
Mesquita, A. P. D. S., Lopes, S. D. A., Filho, P. C. A. P., Nader, H. B., & Lopes, C. C. (2017) · APOPTOSIS · doi:10.1007/s10495-017-1392-0 · Cited by 67 · see citing works
Strategies for Glycoengineering Therapeutic Proteins
Dammen-Brower, K., Epler, P., Zhu, S., Bernstein, Z. J., Stabach, P., Braddock, D., Spangler, J. B., & Yarema, K. (2022) · Frontiers in Chemistry · doi:10.3389/fchem.2022.863118 · Cited by 54 · see citing works
Targets of tumor microenvironment for potential drug development
Zhang, L., Wang, Z., Liu, K., Liu, Y., Wang, S., Jiang, W., Lu, F., & Dang, Y. (2024) · MedComm – Oncology · doi:10.1002/mog2.68 · Cited by 63 · see citing works
Tumor microenvironment and nanotherapeutics: intruding the tumor fort
Kiran, A. V. V. V. R., Kumari, G. K., Krishnamurthy, P. T., & Khaydarov, R. R. (2021) · Biomaterials Science · doi:10.1039/d1bm01127h · Cited by 60 · see citing works
Co-localization and crosstalk between CD44 and RHAMM depend on hyaluronan presentation
Carvalho, A. M., da Costa, D. S., Paulo, P. M. R., Reis, R. L., & Pashkuleva, I. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.10.024 · Cited by 57 · see citing works
Investigations into the cancer stem cell niche using in-vitro 3-D tumor models and microfluidics
Sreepadmanabh, M., & Toley, B. J. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.03.009 · Cited by 57 · see citing works
Hyaluronic Acid-Based Nanomaterials Applied to Cancer: Where Are We Now?
Machado, V., Morais, M., & Medeiros, R. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14102092 · Cited by 53 · see citing works
Cheng, X., Li, H., Ge, X., Chen, L., Liu, Y., Mao, W., Zhao, B., & Yuan, W. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.576420 · Cited by 50 · see citing works
Advances and Challenges of Stimuli-Responsive Nucleic Acids Delivery System in Gene Therapy
Lin, M., & Qi, X. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15051450 · Cited by 51 · see citing works
Glycosaminoglycans: Carriers and Targets for Tailored Anti-Cancer Therapy
Berdiaki, A., Neagu, M. T., Giatagana, E.-M., Николаевич, К. А., Tsatsakis, A. M., Tzanakakis, G. N., & Nikitovic, D. (2021) · Biomolecules · doi:10.3390/biom11030395 · Cited by 50 · see citing works
Gębalski, J., Graczyk, F., & Załuski, D. (2022) · Journal of Enzyme Inhibition and Medicinal Chemistry · doi:10.1080/14756366.2022.2061966 · Cited by 49 · see citing works
Sethuraman, V., Janakiraman, K., Krishnaswami, V., & Kandasamy, R. (2021) · Current Drug Targets · doi:10.2174/1389450122999210128180058 · Cited by 47 · see citing works
Fatima, K., Masood, N., Wani, Z. A., Meena, A., & Luqman, S. (2021) · Journal of Advanced Research · doi:10.1016/j.jare.2021.06.003 · Cited by 46 · see citing works
Behzadipour, Y., & Hemmati, S. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116910 · Cited by 44 · see citing works
Carrasco, A., Pérez‐Ruiz, T., Tudela, J., & Miguel, M. G. (2015) · Flavour and Fragrance Journal · doi:10.1002/ffj.3283 · Cited by 44 · see citing works
Insights into the source, mechanism and biotechnological applications of hyaluronidases
Zhang, Y.-S., Gong, J., Yao, Z.-Y., Jiang, J., Su, C., Li, H., Kang, C.-L., Liu, L., Xu, Z., & Shi, J. (2022) · Biotechnology Advances · doi:10.1016/j.biotechadv.2022.108018 · Cited by 43 · see citing works
Sun, G., Wu, Y., Li, J., Yang, M., Xu, H., Li, Y., Tong, P., Shao, R., Liu, Y., & Kong, X. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113642 · Cited by 44 · see citing works
Fibrin degradation by rtPA enhances the delivery of nanotherapeutics to A549 tumors in nude mice
Zhang, B., Jiang, T., She, X., Shen, S., Wang, S., Deng, J., Shi, W., Mei, H., Hu, Y., Pang, Z., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.04.015 · Cited by 43 · see citing works
Nano-sized drug carriers: Extravasation, intratumoral distribution, and their modeling
Nichols, J. W., Sakurai, Y., Harashima, H., & Bae, Y. H. (2017) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.08.003 · Cited by 43 · see citing works
Targeting the lysyl oxidases in tumour desmoplasia
Chitty, J. L., Setargew, Y. F. I., & Cox, T. R. (2019) · Biochemical Society Transactions · doi:10.1042/bst20190098 · Cited by 43 · see citing works
Organic Nanocarriers for Delivery and Targeting of Therapeutic Agents for Cancer Treatment
Peng, Y., Bariwal, J. B., Kumar, V., Tan, C., & Mahato, R. I. (2020) · Advanced Therapeutics · doi:10.1002/adtp.201900136 · Cited by 43 · see citing works
Hsu, L., Hong, Q., Chen, S.-T., Kuo, H.-L., Schultz, L., Heath, J., Lin, S., Lee, M.-H., Li, D.-Z., Li, Z.-L., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.13268 · Cited by 40 · see citing works
Hyaluronan in the experimental injury of the cartilage: biochemical action and protective effects
Avenoso, A., D’Ascola, A., Scuruchi, M., Mandraffino, G., Calatroni, A., Saitta, A., Campo, S., & Campo, G. M. (2017) · Inflammation Research · doi:10.1007/s00011-017-1084-9 · Cited by 40 · see citing works
Enzyme-Assisted Photodynamic Therapy Based on Nanomaterials
Du, B., & Tung, C. (2020) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.9b00968 · Cited by 39 · see citing works
Metastatic Breast Cancer: Review of Emerging Nanotherapeutics
Dissanayake, R. K., Towner, R. A., & Ahmed, M. (2023) · Cancers · doi:10.3390/cancers15112906 · Cited by 37 · see citing works
Exosomes as a storehouse of tissue remodeling proteases and mediators of cancer progression
Das, A., Mohan, V., Krishnaswamy, V. R., Solomonov, I., & Sagi, I. (2019) · Cancer and Metastasis Reviews · doi:10.1007/s10555-019-09813-5 · Cited by 37 · see citing works
McAtee, C. O., Berkebile, A. R., Elowsky, C. G., Fangman, T., Barycki, J. J., Wahl, J. K., Khalimonchuk, O., Naslavsky, N., Caplan, S., & Simpson, M. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.647446 · Cited by 36 · see citing works
Self-citationRecent advances in nanocarriers-based drug delivery for cancer therapeutics: A review
Yadav, P., Jain, J., & Sherje, A. P. (2021) · Reactive and Functional Polymers · doi:10.1016/j.reactfunctpolym.2021.104970 · Cited by 36 · see citing works
Equilibrium Modeling of the Mechanics and Structure of the Cancer Glycocalyx
Gandhi, J. G., Koch, D. L., & Paszek, M. J. (2019) · Biophysical Journal · doi:10.1016/j.bpj.2018.12.023 · Cited by 35 · see citing works
Evolution of high-molecular-mass hyaluronic acid is associated with subterranean lifestyle
Zhao, Y., Zheng, Z., Zhang, Z., Xu, Y., Hillpot, E., Lin, Y. S., Zakusilo, F. T., Lu, J. Y., Ablaeva, J., Biashad, S. A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-43623-2 · Cited by 34 · see citing works
Leman-Loubière, C., Goff, G. L., Retailleau, P., Debitus, C., & Ouazzani, J. (2017) · Journal of Natural Products · doi:10.1021/acs.jnatprod.7b00714 · Cited by 33 · see citing works
Kouvidi, K., Berdiaki, A., Tzardi, M. N., Karousou, E. G., Passi, A. G., Nikitovic, D., & Tzanakakis, G. N. (2016) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2016.01.019 · Cited by 32 · see citing works
WNT5B drives osteosarcoma stemness, chemoresistance and metastasis
Perkins, R. S., Murray, G., Suthon, S., Davis, L., Perkins, N. B., Fletcher, L. B., Bozzi, A., Schreiber, S. L., Lin, J., Laxton, S. J., et al. (2024) · Clinical and Translational Medicine · doi:10.1002/ctm2.1670 · Cited by 30 · see citing works
Oil-in-microgel strategy for enzymatic-triggered release of hydrophobic drugs
Busatto, C. A., Labie, H., Lapeyre, V., Auzély‐Velty, R., Perro, A., Casís, N., Luna, J. A., Estenoz, D. A., & Ravaine, V. (2017) · Journal of Colloid and Interface Science · doi:10.1016/j.jcis.2017.01.029 · Cited by 31 · see citing works
Velesiotis, C., Vasileiou, S., & Vynios, D. H. (2019) · FEBS Journal · doi:10.1111/febs.14860 · Cited by 31 · see citing works
Cirsimaritin, a lung squamous carcinoma cells (NCIH-520) proliferation inhibitor
Pathak, G., Singh, S., Kumari, P., Raza, W., Hussain, Y., & Meena, A. (2020) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2020.1763198 · Cited by 32 · see citing works
Liu, H., Jiwen, Y., Guo, H., Cai, X., Jiang, Y., Lin, M., Jiang, X., Leung, W., & Xu, C. (2020) · Frontiers in Chemistry · doi:10.3389/fchem.2020.00758 · Cited by 31 · see citing works
Montanari, E., Zoratto, N., Mosca, L., Cervoni, L., Lallana, E., Angelini, R., Matassa, R., Coviello, T., Meo, C. D., & Matricardi, P. (2019) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2019.06.004 · Cited by 30 · see citing works
The CD147‐HYALURONAN Axis in Cancer
Toole, B. P. (2019) · The Anatomical Record · doi:10.1002/ar.24147 · Cited by 30 · see citing works
Liu, Y., Dong, W., Ma, Y., Dou, J., Jiang, W., Wang, L., Wang, Q., Li, M., Wang, Y., & Li, M. (2023) · Biomaterials · doi:10.1016/j.biomaterials.2023.122023 · Cited by 30 · see citing works
Pathak, G., Singh, S., Kumari, P., Hussain, Y., Raza, W., Luqman, S., & Meena, A. (2020) · Food and Chemical Toxicology · doi:10.1016/j.fct.2020.111550 · Cited by 28 · see citing works
Antitumor activity of sulfated hyaluronic acid fragments in pre-clinical models of bladder cancer
Jordan, A. R., Lokeshwar, S. D., López, L. E., Hennig, M. J. P., Chipollini, J. J., Yates, T. J., Hupe, M. C., Merseburger, A. S., Shiedlin, A., Cerwinka, W. H., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.10529 · Cited by 29 · see citing works
Kohi, S., Sato, N., Koga, A., Hirata, K., Harunari, E., & Igarashi, Y. (2016) · Journal of Oncology · doi:10.1155/2016/9063087 · Cited by 29 · see citing works
Design Strategies for Hyaluronic Acid-based Drug Delivery Systems in Cancer Immunotherapy
Rodella, G., Véronique Préat, A., Gallez, B., & Malfanti, A. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113784 · Cited by 28 · see citing works
Vitamin C: A stem cell promoter in cancer metastasis and immunotherapy
Fu, J., Wu, Z., Liu, J., & Wu, T. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110588 · Cited by 28 · see citing works
Foglietta, F., Serpe, L., & Canaparo, R. (2021) · Cells · doi:10.3390/cells10123295 · Cited by 27 · see citing works
- Authors
- McAtee, C. O., Barycki, J. J., & Simpson, M. A.
- Affiliations
- University of Nebraska–Lincoln (US)
- Corresponding author
- Melanie A. Simpson
- Venue
- Advances in Cancer Research
- Publisher
- Elsevier
- Published
- 2014
- Volume
- 123
- Pages
- 1-34
- ISSN
- 0065-230X (ISSN-L)
- PMC
- PMC4445717
- OpenAlex
- W2394990651
- Cited by
- 204
- References
- 127
- Citations by year
- 2026: 3 · 2025: 17 · 2024: 14 · 2023: 24 · 2022: 19 · 2021: 20 · 2020: 25 · 2019: 28 · 2018: 14 · 2017: 15 · 2016: 12 · 2015: 12 · 2014: 1
- FWCI
- 18.61
- Type
- book chapter
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Advances in cancer research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Lincoln (University of Nebraska) (submittedVersion)
- Funders
- National Institutes of Health (8p20gm103489-10)
- National Cancer Institute (R01CA165574)
- National Institute of General Medical Sciences (P20-GM103489)
- National Center for Research Resources (P20RR018759)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- hyaluronidase, hyaluronic acid, metastasis, tumor invasion, hyaluronan oligosaccharides, hyaluronan synthase, substrate specificity, enzyme structure, hyaluronidase inhibitors, tumor imaging, cancer therapy
- MeSH terms
- Animals, Cell Movement, Fibroblasts, Humans, Hyaluronic Acid, Hyaluronoglucosaminidase, Molecular Conformation, Molecular Weight, Neoplasm Metastasis, Neoplasms, Polymers, Prognosis, Alternative Splicing, Disease Progression, Mole Rats, Rats
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review