Noninvasive Imaging of Dendrimer-Type N-Glycan Clusters: In Vivo Dynamics Dependence on Oligosaccharide Structure†
Dr. Katsunori Tanaka
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
These authors contributed equally to this work.
Search for more papers by this authorDr. Eric R. O. Siwu
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
These authors contributed equally to this work.
Search for more papers by this authorKaori Minami
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
Search for more papers by this authorDr. Koki Hasegawa
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorDr. Satoshi Nozaki
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorDr. Yousuke Kanayama
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorKoichi Koyama
Kishida Chemical Co., Ltd. 14-10 Technopark, Sanda-shi, Hyogo 669-1339 (Japan)
Search for more papers by this authorDr. Weihsu C. Chen
Department of Chemical Physiology, Joint Department of Molecular Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, MEM-L71, La Jolla, CA 92037 (USA)
Search for more papers by this authorProf. James C. Paulson
Department of Chemical Physiology, Joint Department of Molecular Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, MEM-L71, La Jolla, CA 92037 (USA)
Search for more papers by this authorProf. Dr. Yasuyoshi Watanabe
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorProf. Dr. Koichi Fukase
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
Search for more papers by this authorDr. Katsunori Tanaka
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
These authors contributed equally to this work.
Search for more papers by this authorDr. Eric R. O. Siwu
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
These authors contributed equally to this work.
Search for more papers by this authorKaori Minami
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
Search for more papers by this authorDr. Koki Hasegawa
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorDr. Satoshi Nozaki
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorDr. Yousuke Kanayama
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorKoichi Koyama
Kishida Chemical Co., Ltd. 14-10 Technopark, Sanda-shi, Hyogo 669-1339 (Japan)
Search for more papers by this authorDr. Weihsu C. Chen
Department of Chemical Physiology, Joint Department of Molecular Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, MEM-L71, La Jolla, CA 92037 (USA)
Search for more papers by this authorProf. James C. Paulson
Department of Chemical Physiology, Joint Department of Molecular Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, MEM-L71, La Jolla, CA 92037 (USA)
Search for more papers by this authorProf. Dr. Yasuyoshi Watanabe
RIKEN Center for Molecular Imaging Science, 6-7-3 Minatojima, Chuo-ku, Kobe-shi, Hyogo 650-0047 (Japan)
Search for more papers by this authorProf. Dr. Koichi Fukase
Department of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka-shi, Osaka 560-0043 (Japan), Fax: (+81) 6-6850-5419 http://www.chem.sci.osaka-u.ac.jp/lab/fukase/
Search for more papers by this authorWe thank Kazuhiro Fukae, Azusa Hashimoto, and Jun Igarishi, Otsuka Chemical Co., Ltd., for supplying N-glycans. This work was supported in part by Grants-in-Aid for Scientific Research Nos. 19681024 and 19651095 from the Japan Society for the Promotion of Science, Collaborative Development of Innovative Seeds from the Japan Science and Technology Agency (JST), New Energy and Industrial Technology Development Organization (NEDO, project ID: 07A01014a), research grants from Yamada Science Foundation as well as the Molecular Imaging Research Program, and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan.
Graphical Abstract
Body image: Self-activating Huisgen 1,3-dipolar cycloaddition and 6π azaelectrocyclization of lysine-based dendrimers (see picture) enable the in vivo dynamics and organ-specific accumulation of N-glycans to be visualized. The sugar structure and glycosyl bond linkages of N-glycans control the whole-body trafficking of the clusters in nude mice and a cancer model.
Supporting Information
Detailed facts of importance to specialist readers are published as ”Supporting Information”. Such documents are peer-reviewed, but not copy-edited or typeset. They are made available as submitted by the authors.
| Filename | Description |
|---|---|
| anie_201000892_sm_miscellaneous_information.pdf9.5 MB | miscellaneous_information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1 Analysis of Glycans, Polysaccharide Functional Properties & Biochemistry of Glycoconjugate Glycans, Carbohydrate-Mediated Interactions: Comprehensive Glycoscience: From Chemistry to Systems Biology, Vols. II & III (Eds.: ), Elsevier, 2007.
- 2
- 2aA. G. Morell, R. A. Irvine, I. Sternlieb, I. H. Scheinberg, G. Ashwell, J. Biol. Chem. 1968, 243, 155–159;
- 2bS. Elliott, T. Lorenzini, S. Asher, K. Aoki, D. Brankow, L. Buck, L. Busse, D. Chang, J. Fuller, J. Grant, N. Hernday, M. Hokum, S. Hu, A. Knudten, N. Levin, R. Komorowski, F. Martin, R. Navarro, T. Osslund, G. Rogers, N. Rogers, G. Trail, J. Egrie, Nat. Biotechnol. 2003, 21, 414–421;
- 2cM. Sato, T. Furuike, R. Sadamoto, N. Fujitani, T. Nakahara, K. Niikura, K. Monde, H. Kondo, S. I. Nishimura, J. Am. Chem. Soc. 2004, 126, 14013–14022.
- 3Y. Kaneko, F. Nimmerjahn, J. V. Ravetch, Science 2006, 313, 670–673.
- 4
- 4aM. Suzuki, R. Noyori, B. Langstom, Y. Watanabe, Bull. Chem. Soc. Jpn. 2000, 73, 1053–1070;
- 4bT. Hosoya, K. Sumi, H. Doi, M. Wakao, M. Suzuki, Org. Biomol. Chem. 2006, 4, 410–415.
- 5aK. Tanaka, K. Fukase, Org. Biomol. Chem. 2008, 6, 815–828;
- 5bK. Tanaka, K. Fukase, Mini-Rev. Org. Chem. 2008, 5, 153–162.
- 6
- 6aT. Ido, C. N. Wan, V. Cassela, J. S. Fowler, A. P. Wolf, J. Labelled Compd. Radiopharm. 1978, 14, 175–183;
- 6bS. S. Gambhir, Nat. Rev. Cancer 2002, 2, 683–693.
- 7K. Tanaka, Y. Fujii, H. Tokimoto, Y. Mori, S. Tanaka, G.-m. Bao, E. R. O. Siwu, A. Nakayabu, K. Fukase, Chem. Asian J. 2009, 4, 574–580, and references therein.
- 8
- 8aS. P. Vyas, A. Singh, V. Sihorkar, Crit. Rev. Ther. Drug Carrier Syst. 2001, 18, 1–76;
- 8bM. Willis, E. Forssen, Adv. Drug Delivery Rev. 1998, 29, 249–271.
- 9
- 9aK. Tanaka, K. Minami, T. Tahara, Y. Fujii, E. R. O. Siwu, S. Nozaki, H. Onoe, S. Yokoi, K. Koyama, Y. Watanabe, K. Fukase, ChemMedChem 2010, 5, 841–845;
- 9bK. Tanaka, K. Minami, T. Tahara, E. R. O. Siwu, K. Koyama, S. Nozaki, H. Onoe, Y. Watanabe, K. Fukase, J. Carbohydr. Chem. 2010, 29, 118–132;
- 9cLysine Labeling & Engineering Kit “STELLA+” from Kishida Chemical Co., Ltd., http://www.kishida.co.jp/.
- 10K. Tanaka, T. Masuyama, K. Hasegawa, T. Tahara, H. Mizuma, Y. Wada, Y. Watanabe, K. Fukase, Angew. Chem. 2008, 120, 108–111; Angew. Chem. Int. Ed. 2008, 47, 102–105.
- 11For representative examples of noninvasive imaging and biodistribution experiments, see;
- 11aS. André, C. Unverzagt, S. Kojima, X. Dong, C. Fink, K. Kayser, H.-J. Gabius, Bioconjugate Chem. 1997, 8, 845–855;
- 11bS. André, C. Unverzagt, S. Kojima, M. Frank, J. Seifert, C. Fink, K. Kayser, C.-W. von der Lieth, H.-J. Gabius, Eur. J. Biochem. 2004, 271, 118–134;
- 11cS. André, S. Kojima, I. Prahl, M. Lensch, C. Unverzagt, H.-J. Gabius, FEBS J. 2005, 272, 1986–1998;
- 11dS. André, S. Kojima, G. Gundel, R. Russwurm, X. Schratt, C. Unverzagt, H.-J. Gabius, Biochim. Biophys. Acta Gen. Subj. 2006, 1760, 768–782;
- 11eS. André, T. Kozar, R. Schuberth, C. Unverzagt, S. Kojima, H.-J. Gabius, Biochemistry 2007, 46, 6984–6995;
- 11fS. André, T. Kozar, S. Kojima, C. Unverzagt, H.-J. Gabius, Biol. Chem. 2009, 390, 557–565;
- 11gM. V. Pimm, A. C. Perkins, J. Strohalm, K. Ulbrich, R. Duncan, J. Drug Targeting 1996, 3, 385–390;
- 11hM. I. M. Prata, A. C. Santos, S. Torres, J. P. André, J. A. Martins, M. Neves, M. L. Garcia-Martin, T. B. Rodrigues, P. Lopez-Larrubia, S. Cerdan, C. F. G. C. Geraldes, Contrast Media Mol. Imaging 2006, 1, 246–258;
- 11iM. Hirai, H. Minematsu, N. Kondo, K. Oie, K. Igarashi, N. Yamazaki, Biochem. Biophys. Res. Commun. 2007, 353, 553–558;
- 11jW. C. Chen, G. C. Completo, J. C. Paulson, Glycobiology 2008, 18, 963;
- 11kS. T. Laughlin, J. M. Baskin, S. L. Amacher, C. R. Bertozzi, Science 2008, 320, 664–667;
- 11lS. Serres, D. C. Anthony, Y. Jiang, K. A. Broom, S. J. Campbell, D. J. Tyler, S. I. van Kasteren, B. G. Davis, N. R. Sibson, J. Neurosci. 2009, 29, 4820–4828;
- 11mS. I. van Kasteren, S. J. Campbell, S. Serres, D. C. Anthony, N. R. Sibson, B. G. Davis, Proc. Natl. Acad. Sci. USA 2009, 106, 18–23.
- 12K. Tanaka, C. Kageyama, K. Fukase, Tetrahedron Lett. 2007, 48, 6475–6479.
- 13Kind gifts from Otsuka Chemical Co., Ltd., http://tansaku.otsukac.co.jp/en/oligo04.html. These structurally pure N-glycans were isolated from egg yolk according to the procedure developed by Kajihara and co-workers: Y. Kajihara, Y. Suzuki, N. Yamamoto, K. Sasaki, T. Sakakibara, L. R. Juneja, Chem. Eur. J. 2004, 10, 971–985.
- 14For representative reviews, see:
- 14aR. Roy, M.-G. Beak, Rev. Mol. Biotechnol. 2002, 90, 291–309;
- 14bM. A. Leeuwenburgh, G. A. van der Marel, H. S. Overkleeft, Curr. Opin. Chem. Biol. 2003, 7, 757–765;
- 14cO. Renaudet, Mini-Rev. Org. Chem. 2008, 5, 274–286;
- 14dY. M. Chabre, R. Roy, Curr. Top. Med. Chem. 2008, 8, 1237–1285;
- 14eY. M. Chabre, R. Roy, Advances in Carbohydrate Chemistry and Biochemistry, Vol. 63, Elsevier, UK, 2010, pp. 165–393.
- 15As with previous reports on mass analysis of the sialosides, the molecular ions of the sialoglycocluster 3 a were observed as a more broadened peak consisting of partially desialylated derivatives (see the Supporting Information): Y. Fukuyama, S. Nakaya, Y. Yamazaki, K. Tanaka, Anal. Chem. 2008, 80, 2171–2179.
- 16H. R. Maecke, M. Hofmann, U. Haberkorn, J. Nucl. Med. 2005, 46, 172S–178S.
- 17A molecular diameter of 3 nm is known to smoothly clear through the kidney. Clusters 1 (molecular weight, MW=10 000) and 3 (MW=50 000) in the unfolded conformation are estimated roughly to be 3 and 7 nm in size, respectively:
- 17aB. Haraldsson, J. Nyström, W. M. Deen, Physiol. Rev. 2008, 88, 451–487;
- 17bA. Edwards, B. S. Daniels, W. M. Deen, Am. J. Physiol. Renal Physiol. 1999, 276, F 892–F902.
- 18A. R. Wyatt, J. J. Yerbury, S. Poon, M. R. Wilson, Curr. Med. Chem. 2009, 16, 2855–2866.
- 19The opposite serum stability of neoglycoproteins in mice, that is, α(2-3)-sialylated derivatives show longer half-lives than the α(2-6)-sialylated congeners, has been reported when glycans were attached to albumin: C. Unverzagt, S. André, J. Seifert, S. Kojima, C. Fink, G. Srikrishna, H. Freeze, K. Kayser, H.-J. Gabius, J. Med. Chem. 2002, 45, 478–491.
- 20R. Tozawa, S. Ishibashi, J. Osuga, K. Yamamoto, H. Yagyu, K. Ohashi, Y. Tamura, N. Yahagi, Y. Iizuka, H. Okazaki, K. Harada, T. Gotoda, H. Shimano, S. Kimura, R. Nagai, N. Yamada, J. Biol. Chem. 2001, 276, 12624–12628.
- 21
- 21aP. R. Crocker, A. Varki, Immunology 2001, 103, 137–145;
- 21bP. R. Crocker, A. Varki, Trends Immunol. 2001, 22, 337–342;
- 21cT. Angata, Mol. Diversity 2006, 10, 555–566;
- 21dA. Varki, T. Angata, Glycobiology 2006, 16, 1R–27R.
- 22E. I. Park, Y. Mi, C. Unverzagt, H.-J. Gabius, J. U. Baenziger, Proc. Natl. Acad. Sci. USA 2005, 102, 17125–17129.
- 23Y. C. Lee, R. R. Townsend, M. R. Hardy, J. Lonngren, J. Arnarp, M. Haraldsson, H. Lonn, J. Biol. Chem. 1983, 258, 199–202.
- 24
- 24aT. Nakagawa, N. Uozumi, M. Nakano, Y. Mizuno-Horikawa, N. Okuyama, T. Taguchi, J. Gu, A. Kondo, N. Taniguchi, E. Miyoshi, J. Biol. Chem. 2006, 281, 29797–29806;
- 24bE. Miyoshi, K. Noda, Y. Yamaguchi, S. Inoue, Y. Ikeda, W. Wang, J. H. Ko, N. Uozumi, W. Li, N. Taniguchi, Biochim. Biophys. Acta Gen. Subj. 1999, 1473, 9–20.
- 25
- 25aJ. G. Cyster, C. C. Goodnow, Immunity 1997, 6, 509–517;
- 25bB. E. Collins, O. Blixt, A. R. DeSieno, N. Bovin, J. D. Marth, J. C. Paulson, Proc. Natl. Acad. Sci. USA 2004, 101, 6104–6109;
- 25cP. R. Crocker, J. C. Paulson, A. Varki, Nat. Rev. Immunol. 2007, 7, 255–266.
- 26
- 26aE. M. Comelli, S. R. Head, T. Gilmartin, T. Whisenant, S. M. Haslam, S. J. North, N. K. Wong, T. Kudo, H. Narimatsu, J. D. Esko, K. Drickamer, A. Dell, J. C. Paulson, Glycobiology 2006, 16, 117–131;
- 26bH. Tateno, H. Y. Li, M. J. Schur, N. Bovin, P. R. Crocker, W. W. Wakarchuk, J. C. Paulson, Mol. Cell. Biol. 2007, 27, 5699–5710;
- 26cM. K. O’Reilly, B. E. Collins, S. Han, L. Liao, C. Rillahan, P. I. Kitov, D. R. Bundle, J. C. Paulson, J. Am. Chem. Soc. 2008, 130, 7736–7745.
- 27
- 27aD. D. Manning, X. Hu, P. Beck, L. L. Kiessling, J. Am. Chem. Soc. 1997, 119, 3161–3162;
- 27bJ. D. Reuter, A. Myc, M. M. Hayes, Z. Gan, R. Roy, D. Qin, R. Yin, L. T. Piehler, R. Esfand, D. A. Tomalia, J. R. Baker, Jr., Bioconjugate Chem. 1999, 10, 271–278;
- 27cS. André, H. Kaltner, T. Furuike, S.-I. Nishimura, H.-J. Gabius, Bioconjugate Chem. 2004, 15, 87–98;
- 27dV. Ladmiral, G. Mantovani, G. J. Clarkson, S. Cauet, J. L. Irwin, D. M. Haddleton, J. Am. Chem. Soc. 2006, 128, 4823–4830;
- 27eC. B. Carlson, P. Mowery, R. M. Owen, E. C. Dykhuizen, L. L. Kiessling, ACS Chem. Biol. 2007, 2, 119–127;
- 27fM. L. Wolfenden, M. J. Cloninger, Bioconjugate Chem. 2006, 17, 958–966;
- 27gJ. Kim, Y. Ahn, K. M. Park, Y. Kim, Y. H. Ko, D. H. Oh, K. Kim, Angew. Chem. 2007, 119, 7537–7539; Angew. Chem. Int. Ed. 2007, 46, 7393–7395;
- 27hM. J. Lee, K. Pal, T. Tasaki, S. Roy, Y. Jiang, J. Y. An, R. Banerjee, Y. T. Kwon, Proc. Natl. Acad. Sci. USA 2008, 105, 100–105.
