Recent advances in Claudin-targeting technology

Biological and Pharmaceutical Bulletin

Volumn 36, Issue 5, 2013, Pages 708-714

  Nagase, Shotaro ^a   Doyama, Ryo ^a   Yagi, Kiyohito ^a   Kondoh, Masuo ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Claudin; Clostridium perfringens enterotoxin; Epithelial cell; Tight junction

Indexed keywords

ANTINEOPLASTIC AGENT; CARBOXY TERMINAL FRAGMENT OF CLOSTRIDIUM PERFRINGENS ENTEROTOXIN PROTEIN SYNTHESIS INHIBITORY FACTOR; CLAUDIN; GAMMA INTERFERON; IMMUNOGLOBULIN G; INTERLEUKIN 13; OVALBUMIN CARBOXY TERMINAL FRAGMENT OF CLOSTRIDIUM PERFRINGENS ENTEROTOXIN; OVALBUMIN CARBOXY TERMINAL FRAGMENT OF CLOSTRIDIUM PERFRINGENS ENTEROTOXIN 303; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; BINDING AFFINITY; CELL DEATH; CYTOKINE PRODUCTION; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG TARGETING; HUMAN; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; INFECTION; LUNG METASTASIS; MUCOSA; NONHUMAN; PROTEIN EXPRESSION; REVIEW; TIGHT JUNCTION; TREATMENT DURATION; TREATMENT RESPONSE; TUMOR GROWTH; VACCINATION;

ADMINISTRATION, MUCOSAL; ANIMALS; ANTINEOPLASTIC AGENTS; CLAUDINS; DRUG DELIVERY SYSTEMS; HUMANS; NEOPLASMS; VACCINES;

EID: 84876918345     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b13-00014     Document Type: Review

References (48)

1. Wodarz A, Näthke I. Cell polarity in development and cancer. Nat. Cell Biol., 9, 1016-1024 (2007).
2. Kunisawa J, Nochi T, Kiyono H. Immunological commonalities and distinctions between airway and digestive immunity. Trends Immunol., 29, 505-513 (2008).
3. Powell DW. Barrier function of epithelia. Am. J. Physiol., 241, G275-G288 (1981).
4. Windsor E, Cronheim GE. Gastro-intestinal absorption of heparin and synthetic heparinoids. Nature, 190, 263-264 (1961).
5. Schneeberger EE, Lynch RD. The tight junction: a multifunctional complex. Am. J. Physiol. Cell Physiol., 286, C1213-C1228 (2004).
6. Higashi T, Tokuda S, Kitajiri SI, Masuda S, Nakamura H, Oda Y, Furuse M. Analysis of the angulin family consisting of LSR, ILDR1 and ILDR2: tricellulin recruitment, epithelial barrier function and implication in deafness pathogenesis. J. Cell Sci., (2012), in press.
7. Masuda S, Oda Y, Sasaki H, Ikenouchi J, Higashi T, Akashi M, Nishi E, Furuse M. LSR defines cell corners for tricellular tight junction formation in epithelial cells. J. Cell Sci., 124, 548-555 (2011).
8. Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J. Cell Biol., 171, 939-945 (2005).
9. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol., 156, 1099-1111 (2002).
10. Hackel D, Krug SM, Sauer RS, Mousa SA, Böcker A, Pflücke D, Wrede EJ, Kistner K, Hoffmann T, Niedermirtl B, Sommer C, Bloch L, Huber O, Blasig IE, Amasheh S, Reeh PW, Fromm M, Brack A, Rittner HL. Transient opening of the perineurial barrier for analgesic drug delivery. Proc. Natl. Acad. Sci. U.S.A., 109, E2018-E2027 (2012).
11. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, Furuse M, Tsukita S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol., 161, 653-660 (2003).
12. Kondoh M, Masuyama A, Takahashi A, Asano N, Mizuguchi H, Koizumi N, Fujii M, Hayakawa T, Horiguchi Y, Watanbe Y. A novel strategy for the enhancement of drug absorption using a claudin modulator. Mol. Pharmacol., 67, 749-756 (2005).
13. Uchida H, Kondoh M, Hanada T, Takahashi A, Hamakubo T, Yagi K. A claudin-4 modulator enhances the mucosal absorption of a biologically active peptide. Biochem. Pharmacol., 79, 1437-1444 (2010).
14. Kominsky SL. Claudins: emerging targets for cancer therapy. Expert Rev. Mol. Med., 8, 1-11 (2006).
15. Morin PJ. Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res., 65, 9603-9606 (2005).
16. Kominsky SL, Tyler B, Sosnowski J, Brady K, Doucet M, Nell D, Smedley JG 3rd, McClane B, Brem H, Sukumar S. Clostridium perfringens enterotoxin as a novel-targeted therapeutic for brain metastasis. Cancer Res., 67, 7977-7982 (2007).
17. Michl P, Buchholz M, Rolke M, Kunsch S, Löhr M, McClane B, Tsukita S, Leder G, Adler G, Gress TM. Claudin-4: a new target for pancreatic cancer treatment using Clostridium perfringens enterotoxin. Gastroenterology, 121, 678-684 (2001).
18. Santin AD, Cané S, Bellone S, Palmieri M, Siegel ER, Thomas M, Roman JJ, Burnett A, Cannon MJ, Pecorelli S. Treatment of chemotherapy-resistant human ovarian cancer xenografts in C.B-17/SCID mice by intraperitoneal administration of Clostridium perfringens enterotoxin. Cancer Res., 65, 4334-4342 (2005).
19. Tamagawa H, Takahashi I, Furuse M, Yoshitake-Kitano Y, Tsukita S, Ito T, Matsuda H, Kiyono H. Characteristics of claudin expression in follicle-associated epithelium of Peyer's patches: preferential localization of claudin-4 at the apex of the dome region. Lab. Invest., 83, 1045-1053 (2003).
20. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J. Clin., 58, 71-96 (2008).
21. Ebihara C, Kondoh M, Hasuike N, Harada M, Mizuguchi H, Horiguchi Y, Fujii M, Watanabe Y. Preparation of a claudin-targeting molecule using a C-terminal fragment of Clostridium perfringens enterotoxin. J. Pharmacol. Exp. Ther., 316, 255-260 (2006).
22. Saeki R, Kondoh M, Kakutani H, Tsunoda S, Mochizuki Y, Hamakubo T, Tsutsumi Y, Horiguchi Y, Yagi K. A novel tumor-targeted therapy using a claudin-4-targeting molecule. Mol. Pharmacol., 76, 918-926 (2009).
23. Kreitman RJ, Pastan I. Immunotoxins in the treatment of hematologic malignancies. Curr. Drug Targets, 7, 1301-1311 (2006).
24. Ogata M, Chaudhary VK, Pastan I, FitzGerald DJ. Processing of Pseudomonas exotoxin by a cellular protease results in the generation of a 37,000-Da toxin fragment that is translocated to the cytosol. J. Biol. Chem., 265, 20678-20685 (1990).
25. Meunier V, Bourrie M, Berger Y, Fabre G. The human intestinal epithelial cell line Caco-2; pharmacological and pharmacokinetic applications. Cell Biol. Toxicol., 11, 187-194 (1995).
26. Saeki R, Kondoh M, Kakutani H, Matsuhisa K, Takahashi A, Suzuki H, Kakamu Y, Watari A, Yagi K. A claudin-targeting molecule as an inhibitor of tumor metastasis. J. Pharmacol. Exp. Ther., 334, 576-582 (2010).
27. Boyaka PN, Marinaro M, Vancott JL, Takahashi I, Fujihashi K, Yamamoto M, van Ginkel FW, Jackson RJ, Kiyono H, McGhee JR. Strategies for mucosal vaccine development. Am. J. Trop. Med. Hyg., 60 (Suppl), 35-45 (1999).
28. Cárdenas-Freytag L, Cheng E, Mirza A. New approaches to mucosal immunization. Adv. Exp. Med. Biol., 473, 319-337 (1999).
29. Michels KB, zur Hausen H. HPV vaccine for all. Lancet, 374, 268-270 (2009).
30. Kiyono H, Fukuyama S. NALT- versus Peyer's-patch-mediated mucosal immunity. Nat. Rev. Immunol., 4, 699-710 (2004).
31. Kunisawa J, Fukuyama S, Kiyono H. Mucosa-associated lymphoid tissues in the aerodigestive tract: their shared and divergent traits and their importance to the orchestration of the mucosal immune system. Curr. Mol. Med., 5, 557-572 (2005).
32. Owen RL, Piazza AJ, Ermak TH. Ultrastructural and cytoarchitectural features of lymphoreticular organs in the colon and rectum of adult BALB/c mice. Am. J. Anat., 190, 10-18 (1991).
33. Ling J, Liao H, Clark R, Wong MS, Lo DD. Structural constraints for the binding of short peptides to claudin-4 revealed by surface plasmon resonance. J. Biol. Chem., 283, 30585-30595 (2008).
34. Kakutani H, Kondoh M, Fukasaka M, Suzuki H, Hamakubo T, Yagi K. Mucosal vaccination using claudin-4-targeting. Biomaterials, 31, 5463-5471 (2010).
35. Yamamoto S, Kiyono H, Yamamoto M, Imaoka K, Fujihashi K, Van Ginkel FW, Noda M, Takeda Y, McGhee JR. A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc. Natl. Acad. Sci. U.S.A., 94, 5267-5272 (1997).
36. Yanagita M, Hiroi T, Kitagaki N, Hamada S, Ito HO, Shimauchi H, Murakami S, Okada H, Kiyono H. Nasopharyngeal-associated lymphoreticular tissue (NALT) immunity: fimbriae-specific Th1 and Th2 cell-regulated IgA responses for the inhibition of bacterial attachment to epithelial cells and subsequent inflammatory cytokine production. J. Immunol., 162, 3559-3565 (1999).
37. Takahashi A, Kondoh M, Masuyama A, Fujii M, Mizuguchi H, Horiguchi Y, Watanabe Y. Role of C-terminal regions of the C-terminal fragment of Clostridium perfringens enterotoxin in its interaction with claudin-4. J. Control. Release, 108, 56-62 (2005).
38. Takahashi A, Komiya E, Kakutani H, Yoshida T, Fujii M, Horiguchi Y, Mizuguchi H, Tsutsumi Y, Tsunoda S, Koizumi N, Isoda K, Yagi K, Watanabe Y, Kondoh M. Domain mapping of a claudin-4 modulator, the C-terminal region of C-terminal fragment of Clostridium perfringens enterotoxin, by site-directed mutagenesis. Biochem. Pharmacol., 75, 1639-1648 (2008).
39. Kakutani H, Takahashi A, Kondoh M, Saito Y, Yamaura T, Sakihama T, Hamakubo T, Yagi K. A novel screening system for claudin binder using baculoviral display. PLoS ONE, 6, e16611 (2011).
40. Loisel TP, Ansanay H, St-Onge S, Gay B, Boulanger P, Strosberg AD, Marullo S, Bouvier M. Recovery of homogeneous and functional beta 2-adrenergic receptors from extracellular baculovirus particles. Nat. Biotechnol., 15, 1300-1304 (1997).
41. Sakihama T, Masuda K, Sato T, Doi T, Kodama T, Hamakubo T. Functional reconstitution of G-protein-coupled receptor-mediated adenylyl cyclase activation by a baculoviral co-display system. J. Biotechnol., 135, 28-33 (2008).
42. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wölk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature, 446, 801-805 (2007).
43. Amasheh M, Grotjohann I, Amasheh S, Fromm A, Söderholm JD, Zeitz M, Fromm M, Schulzke JD. Regulation of mucosal structure and barrier function in rat colon exposed to tumor necrosis factor alpha and interferon gamma in vitro: a novel model for studying the pathomechanisms of inflammatory bowel disease cytokines. Scand. J. Gastroenterol., 44, 1226-1235 (2009).
44. Takahashi A, Saito Y, Kondoh M, Matsushita K, Krug SM, Suzuki H, Tsujino H, Li X, Aoyama H, Matsuhisa K, Uno T, Fromm M, Hamakubo T, Yagi K. Creation and biochemical analysis of a broad-specific claudin binder. Biomaterials, 33, 3464-3474 (2012).
45. Kimura J, Abe H, Kamitani S, Toshima H, Fukui A, Miyake M, Kamata Y, Sugita-Konishi Y, Yamamoto S, Horiguchi Y. Clostridium perfringens enterotoxin interacts with claudins via electrostatic attraction. J. Biol. Chem., 285, 401-408 (2010).
46. Suzuki H, Kondoh M, Li X, Takahashi A, Matsuhisa K, Matsushita K, Kakamu Y, Yamane S, Kodaka M, Isoda K, Yagi K. A toxicological evaluation of a claudin modulator, the C-terminal fragment of Clostridium perfringens enterotoxin, in mice. Pharmazie, 66, 543-546 (2011).
47. Suzuki M, Kato-Nakano M, Kawamoto S, Furuya A, Abe Y, Misaka H, Kimoto N, Nakamura K, Ohta S, Ando H. Therapeutic antitumor efficacy of monoclonal antibody against claudin-4 for pancreatic and ovarian cancers. Cancer Sci., 100, 1623-1630 (2009).
48. Fofana I, Krieger SE, Grunert F, Glauben S, Xiao F, Fafi-Kremer S, Soulier E, Royer C, Thumann C, Mee CJ, McKeating JA, Dragic T, Pessaux P, Stoll-Keller F, Schuster C, Thompson J, Baumert TF. Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes. Gastroenterology, 139, 953-964, 964, e1-e4 (2010).