Cell surface heparan sulfate proteoglycans mediate the internalization of PDX-1 protein

Cell Transplantation

Volumn 17, Issue 1-2, 2008, Pages 91-97

  Ueda, Michiko ^a,b   Matsumoto, Shinichi ^c   Hayashi, Shuji ^d   Kobayashi, Naoya ^e   Noguchi, Hirofumi ^a,c,d  

^a FUJITA HEALTH UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^d NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e OKAYAMA UNIVERSITY   (Japan)

Author keywords

Heparan sulfate proteoglycan (HSP); Pancreatic and duodenal homeobox factor 1 (PDX 1); Protein transduction domain; Protein transduction technology

Indexed keywords

CHONDROITIN 4 SULFATE; CHONDROITIN 6 SULFATE; DERMATAN SULFATE; GLYCOSAMINOGLYCAN; HEPARIN; HEPARIN LYASE; PROTEOHEPARAN SULFATE; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; CELL DIFFERENTIATION; CHO CELL; CONFERENCE PAPER; CONTROLLED STUDY; GENE TRANSFER; GLYCOSAMINOGLYCAN METABOLISM; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN SYNTHESIS; INTERNALIZATION; NONHUMAN; PANCREAS DUCT; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STEM CELL;

EID: 42249087481     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/000000008783906892     Document Type: Conference Paper

References (39)

1. Berlose, J. P.; Convert, O.; Derossi, D.; Brunissen, A.; Chassaing, G. Conformational and associative behaviours of the third helix of antennapedia homeodomain in membrane-mimetic environments. Eur. J. Biochem. 242:372-386; 1996
2. Bonner-Weir, S.; Taneja, M.; Weir, G. C.; Tatarkiewicz, K.; Song, K. H.; Sharma, A.; O'Neil, J. J. In vitro cultivation of human islets from expanded ductal tissue. Proc. Natl. Acad. Sci. USA 97:7999-8004; 2000.
3. Drin, G.; Cottin, S.; Blanc, E.; Rees, A. R.; Temsamani, J. Studies on the internalization mechanism of cationic cell-penetrating peptides. J. Biol. Chem. 278:31192-31201; 2003.
4. Esko, J. D.; Weinke, J. L.; Taylor, W. H.; Ekborg, G.; Roden, L.; Anantharamaiah, G.; Gawish, A. Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I. J. Biol. Chem. 262:12189-12195; 1987.
5. Esko, J. D.; Stewart, T. E.; Taylor, W. H. Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. USA 82:3197-3201; 1985.
6. Ferber, S.; Halkin, A.; Cohen, H.; Ber, I.; Einav, Y.; Goldberg, I.; Barshack, I.; Seijffers, R.; Kopolovic, J.; Kaiser, N.; Karasik, A. Pancreatic and duodenal homeobox gene 1 induces expression of insulin genes in liver and ameliorates streptozotocin-induced hyperglycemia. Nat. Med. 6:568-572; 2000.
7. Fischer, R.; Kohler, K.; Fotin-Mleczek, M.; Brock, R. A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides. J. Biol. Chem. 279:12625-12635; 2004.
8. German, M. S.; Wang, J. The insulin gene contains multiple transcriptional elements that respond to glucose. Mol. Cell. Biol. 14:4067-4075; 1994.
9. Glick, E.; Leshkowitz, D.; Walker, M. D. Transcription factor BETA2 acts cooperatively with E2A and PDX1 to activate the insulin gene promoter. J. Biol. Chem. 275:2199-2204; 2000.
10. Hering, B. J.; Kandaswamy, R.; Harmon, J. V.; Ansite, J. D.; Clemmings, S. M.; Sakai, T.; Paraskevas, S.; Eckman, P. M.; Sageshima, J.; Nakano, M.; Sawada, T.; Matsumoto, I.; Zhang, H. J.; Sutherland, D. E.; Bluestone, J. A. Transplantation of cultured islets from two-layer preserved pancreases in type 1 diabetes with anti-CD3 antibody. Am. J. Transplant. 4:390-401; 2004.
11. Jonsson, J.; Carlsson, L.; Edlund, T.; Edlund, H. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371:606-609; 1994.
12. Leonard, J.; Peers, B.; Johnson, T.; Ferreri, K.; Lee, S.; Montminy, M. R. Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells. Mol. Endocrinol. 7:1275-1283; 1993.
13. Lord, J. M.; Roberts, L. M. Toxin entry: Retrograde transport through the secretory pathway. J. Cell Biol. 140:733-736; 1998.
14. Mann, D. A.; Frankel, A. D. Endocytosis and targeting of exogenous HIV-1 Tat protein. EMBO J. 10:1733-1739; 1991.
15. Matsuzaki, K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462:1-10; 1999.
16. Miller, C. P.; McGehee, Jr., R. E.; Habener, J. F. IDX-1: A new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostatin gene. EMBO J. 13:1145-1156; 1994.
17. Naya, F. J.; Huang, H. P.; Qiu, Y.; Mutoh, H.; DeMayo, F. J.; Leiter, A. B.; Tsai, M. J. Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev. 11:2323-2334; 1997.
18. Noguchi, H.; Bonner-Weir, S.; Wei, F. Y.; Matsushita, M.; Matsumoto, S. BETA2/NeuroD protein can be transduced into cells due to an arginine- and lysine-rich sequence. Diabetes 54:2859-2866; 2005.
19. Noguchi, H.; Kaneto, H.; Weir, G. C.; Bonner-Weir, S. PDX-1 protein containing its own antennapedia-like protein transduction domain can transduce pancreatic duct and islet cells. Diabetes 52:1732-1737; 2003.
20. Noguchi, H.; Matsumoto, S.; Okitsu, T.; Iwanaga, Y.; Yonekawa, Y.; Nagata, H.; Matsushita, M.; Wei, F. Y.; Matsui, H.; Minami, K.; Seino, S.; Masui, Y.; Futaki, S.; Tanaka, K. PDX-1 protein is internalized by lipid raft-dependent macropinocytosis. Cell Transplant. 14:637-645; 2005.
21. Noguchi, H.; Matsushita, M.; Okitsu, T.; Moriwaki, A.; Tomizawa, K.; Kang, S.; Li, S. T.; Kobayashi, N.; Matsumoto, S.; Tanaka, K.; Tanaka, N.; Matsui, H. A new cell-permeable peptide allows successful allogeneic islet transplantation in mice. Nat. Med. 10:305-309; 2004.
22. Noguchi, H.; Matsushita, M.; Matsumoto, S.; Lu, Y. F.; Matsui, H.; Bonner-Weir, S. Mechanism of PDX-1 protein transduction. Biochem. Biophys. Res. Commun. 332:68-74; 2005.
23. Noguchi, H.; Nakai, Y.; Matsumoto, S.; Kawaguchi, M.; Ueda, M.; Okitsu, T.; Iwanaga, Y.; Yonekawa, Y.; Nagata, H.; Minami, K.; Masui, Y.; Futaki, S.; Tanaka, K. Cell permeable peptide of JNK inhibitor prevents islet apoptosis immediately after isolation and improves islet graft function. Am. J. Transplant. 5:1848-1855; 2005.
24. Noguchi, H.; Nakai, Y.; Ueda, M.; Masui, Y.; Futaki, S.; Kobayashi, N.; Hayashi, S.; Matsumoto, S. Activation of c-Jun NH2-terminal kinase (JNK) pathway during islet transplantation and prevention of islet graft loss by intraportal injection of JNK inhibitor. Diabetologia 50:612-619; 2007.
25. Noguchi, H.; Ueda, M.; Matsumoto, S.; Kobayashi, N.; Hayashi, S. BETA2/NeuroD protein transduction requires cell surface heparan sulfate proteoglycans. Hum. Gene Ther. 18:10-17; 2007.
26. Offield, M. F.; Jetton, T. L.; Labosky, P. A.; Ray, M.; Stein, R. W.; Magnuson, M. A.; Hogan, B. L.; Wright, C. V. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122:983-995; 1996.
27. Ohneda, K.; Mirmira, R. G.; Wang, J.; Johnson, J. D.; German, M. S. The homeodomain of PDX-1 mediates multiple protein-protein interactions in the formation of a transcriptional activation complex on the insulin promoter. Mol. Cell. Biol. 20:900-911; 2000.
28. Richard, J. P.; Melikov, K.; Vives, E.; Ramos, C.; Verbeure, B.; Gait, M. J.; Chernomordik, L. V.; Lebleu, B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 278:585-590; 2003.
29. Ricordi, C. Islet transplantation: A brave new world. Diabetes 52:1595-1603; 2003.
30. Rostand, K. S.; Esko, J. D. Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65:1-8; 1997.
31. Rusnati, M.; Tulipano, G.; Urbinati, C.; Tanghetti, E.; Giuliani, R.; Giacca, M.; Ciomei, M.; Corallini, A.; Presta, M. The basic domain in HIV-1 Tat protein as a target for polysulfonated heparin-mimicking extracellular Tat antagonists. J. Biol. Chem. 273:16027-16037; 1998.
32. Sandvig, K.; van Deurs, B. Entry of ricin and Shiga toxin into cells: Molecular mechanisms and medical perspectives. EMBO J. 19:5943-5950; 2000.
33. Shapiro, A. M.; Lakey, J. R.; Ryan, E. A.; Korbutt, G. S.; Toth, E.; Warnock, G. L.; Kneteman, N. M.; Rajotte, R. V. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 343:230-238; 2000.
34. Sharma, A.; Stein, R. Glucose-induced transcription of the insulin gene is mediated by factors required for beta-cell-type-specific expression. Mol. Cell. Biol. 14:871-879; 1994.
35. Summerford, C.; Samulski, R. J. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72:1438-1445; 1998.
36. Tyagi, M.; Rusnati, M.; Presta, M.; Giacca, M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276:3254-3261; 2001.
37. Waeber, G.; Thompson, N.; Nicod, P.; Bonny, C. Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol. Endocrinol. 10:1327-1334; 1996.
38. Yanagishita, M.; Hascall, V. C. Cell surface heparan sulfate proteoglycans. J. Biol. Chem. 267:9451-9454; 1992.
39. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 415:389-395; 2002.