Identification of a pancreatic stellate cell population with properties of progenitor cells: New role for stellate cells in the pancreas

Biochemical Journal

Volumn 421, Issue 2, 2009, Pages 181-191

  Mato, Eugenia ^a,b   Lucas, Maria ^a   Petriz, Jordi ^c,e   Gomis, Ramon ^a,d   Novials, Anna ^a,d  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d HOSPITAL CLÍNIC   (Spain)

^e HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

ATP binding cassette (ABC); Cell differentiation; Diabetes; Mitoxantrone resistant cell population; Pancreatic stellate cell (PaSC); Progenitor cell

Indexed keywords

ATP-BINDING CASSETTE (ABC); CELL DIFFERENTIATION; DIABETES; MITOXANTRONE-RESISTANT CELL POPULATION; PANCREATIC STELLATE CELL (PASC); PROGENITOR CELL;

AMINES; CELL MEMBRANES; CELL PROLIFERATION; ENZYME INHIBITION; GLUCOSE; INSULIN; TRANSCRIPTION; TRANSCRIPTION FACTORS;

CELL CULTURE;

AMYLIN; BREAST CANCER RESISTANCE PROTEIN; C PEPTIDE; CHROMOGRANIN A; EXENDIN 4; GLUCAGON; GLUCOSE TRANSPORTER 2; INSULIN; MATRIGEL; MITOXANTRONE; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 2; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL GRANULE; CELL POPULATION; CELL TRANSDIFFERENTIATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOCRINE CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; INSULIN RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PANCREATIC STELLATE CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STELLATE CELL; STEM CELL;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; MICROSCOPY, ELECTRON; MITOXANTRONE; PANCREAS; RATS; STEM CELLS;

RATTUS;

EID: 67650904758     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081466     Document Type: Article

References (46)

1. Zhou, S., Schuetz, J. D., Bunting, K. D., Colapietro, A. M., Sampath, J., Morris, J. J., Lagutina, I., Grosveld, G. C., Osawa, M., Nakauchi, H. and Sorrentino, B. P. (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 7, 1028-1034
2. Bunting, K. D. (2002) ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 20, 11-20
3. Krishnamurthy, P. and Schuetz, J. D. (2005) ABCG2/BCRP in biology and medicine. Annu. Rev. Pharmacol. Toxicol. 46, 381-410
4. Bonner-Weir, S. and Sharma, A. (2002) Pancreatic stem cells. J. Pathol. 197, 519-526
5. Bonner-Weir, S., Toschi, E., Inada, A., Yatoh, S., Li, W. C., Aye, T., Toschi, E. and Sharma, A. (2004) The pancreatic ductal epithelium serves as a potential pool of progenitor cells. Pediatr. Diabetes 5 (Suppl. 2), 16-22
6. Von Herrath, M. and Homann, D. (2004) Islet regeneration needed for overcoming autoimmune destruction - considerations on the pathogenesis of type 1 diabetes. Pediatr. Diabetes 5 (Suppl. 2), 23-28
7. Gao, R., Ustinov, J., Korsgren, O. and Otonkoski, T. (2005) In vitro neogenesis of human islets reflects the plasticity of differentiated human pancreatic cells. Diabetologia 48, 2296-2304
8. Rosenberg, L. (1998) Induction of islet cell neogenesis in the adult pancreas: the partial duct obstruction model. Microsc. Res. Tech. 43, 337-346
9. Rosenberg, L., Duguid, W. P., Healy, M., Clas, D. and Vinik, A. I. (1992) Reversal of diabetes by the induction of islet cell neogenesis. Transplant. Proc. 24, 1027-1028
10. Bernard, C., Berthault, M. F., Saulnier, C. and Ktorza, A. (1999) Neogenesis vs. apoptosis as main components of pancreatic β-cell mass changes in glucose-infused normal and mildly diabetic adult rats. FASEB J. 13, 1195-1205
11. Sharma, A, Zangen, D. H., Reitz, P., Taneja, M., Lissauer, M. E., Miller, C. P., Weir, G. C., Habener, J. F. and Bonner-Weir, S. (1999) The homeodomain protein IDX-1 increases after an early burst of proliferation during pancreatic regeneration. Diabetes 48, 507-513
12. Guz, Y., Nasir, I. and Teitelman, G. (2001) Regeneration of pancreatic β cells from intra-islet precursor cells in an experimental model of diabetes. Endocrinology 142, 4956-4968
13. Dor, Y., Brown, J., Martinez, O. I. and Melton, D. A. (2004) Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429, 41-46
14. Lechner, A., Leech, C. A., Abraham, E., Nolan, A. L. and Habener, J. F. (2002) Nestin-positive progenitor cells derived from adult human pancreatic islets of Langerhans contain side population (SP) cells defined by expression of the ABCG2 (BCRP1) ATP-binding cassette transporter. Biochem. Biophys. Res. Commun. 293, 670-674
15. Shook, D. and Keller, R. (2003) Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech. Dev. 120, 1341-1383
16. Phillips, P. A, McCarroll, J. A., Park, S., Wu, M. J., Pirola, R., Korsten, M., Wilson, J. S. and Apte, M. V. (2003) Rat pancreatic stellate cells secrete matrix metalloproteinases: implications for extracellular matrix turnover. Gut 52, 275-282
17. Omary, M. B., Lugea, A., Lowe, A. W. and Pandol, S. J. (2007) The pancreatic stellate cell: a star on the rise in pancreatic diseases. J. Clin. Invest. 117, 50-59
18. + hepatic stellate cells are progenitor cells. Biochem. Biophys. Res. Commun. 352, 410-417
19. Garcia-Escarp, M., Martínez-Muñoz, V., Sales-Pardo, I., Barquinero, J,, Domingo, J. C., Marin, P. and Petriz, J. (2004) Flow cytometry-based approach to ABCG2 function suggests that the transporter differentially handles the influx and efflux of drugs. Cytometry 62, 129-138
20. Catalano, R. A. and Lillie, R. D. (1975) Elimination of precipitates in Oil Red O fat stain by adding dextrin. Stain Technol. 50, 297-299
21. Kawazu, S., Kanazawa, Y., Hayashi, M., Ikeuchi, M., Nakai, T. and Kosaka, K. (1980) Monolayer culture of human fetal and adult pancreas. Static and dynamic studies of insulin release in vitro. Horm. Metab. Res. 12, 354-360
22. Spurr, A. R. (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruc. Res. 26, 36-43
23. Reynolds, E. S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208-212
24. Royer, P. J., Tanguy-Royer, S., Ebstein, F., Sapede, C., Simon, T., Barbieux, I., Oger, R. and Gregoire, M. (2006) Culture medium and protein supplementation in the generation and maturation of dendritic cells. Scand. J. Immunol. 63, 401-409
25. Huang, H. and and Tang, X. (2003) Phenotypic determination and characterization of nestin-positive precursors derived from human fetal pancreas. Lab. Invest. 83, 539-547
26. Schwitzgebel, V. M., Scheel, D. W., Conners, J. R. Kalamaras, J., Lee, J. E., Anderson, D. J., Sussel, L., Johnson, J. D. and German, M. S. (2000) Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127, 3533-3542
27. Shapiro, A. M., Lakey, J. R., Paty, B. W., Senior, P. A., Bigam, D. L. and Ryan, E. A. (2005) Strategic opportunities in clinical islet transplantation. Transplantation 79, 1304-1307
28. Gao, R., Ustinov, J., Pulkkinen, M. A., Pulkkinen, M. A., Lundin, K., Korsgren, O. and Otonkoski, T. (2003) Characterization of endocrine progenitor cells and critical factors for their differentiation in human adult pancreatic cell culture. Diabetes 52, 2007-2015
29. Seeberger, K. L., Dufour, J. M., Shapiro, S. M., Lakey, J. R., Rajotte, R. V. and Korbutt, G. S. (2006) Expansion of mesenchymal stem cells from human pancreatic ductal epithelium. Lab. Invest. 86, 141-153
30. Weissman, I. L., Anderson, D. J. and Gage, F. (2001) Stem and progenitor cells: origins, phenotypes, lineage commitments, and trans-differentiations. Annu. Rev. Cell. Dev. Biol. 17, 387-403
31. Scharfmann, R. (2000) Control of early development of the pancreas in rodents and humans: implications of signals from the mesenchyme. Diabetologia 43, 1083-1092
32. Beattie, G. M., Levine, F., Mally, M. I., Otonkoski, T., O'Brien, J. S., Salomon, D. R. and Hayek, A. (1994) Acid β-galactosidase: a developmentally regulated marker of endocrine cell precursors in the human fetal pancreas. J. Clin. Endocrinol. Metab. 78, 1232-1240
33. Kim, S. K., Hebrok, M. and Melton, D. A. (1997) Notochord to endoderm signalling is required for pancreas development. Development 124, 4243-4252
34. Yashpal, N. K., Li, J. and Wang, R. (2004) Characterization of c-Kit and nestin expression during islet cell development in the prenatal and postnatal rat pancreas. Dev. Dyn. 229, 813-825
35. Fetsch, P. A., Abati, A., Litman, T., Morisaki, K., Honjo, Y., Mittal, K. and Bates, S. E. (2006) Localization of the ABCG2 mitoxantrone resistance-associated protein in normal tissues. Cancer Lett. 235, 84-92
36. Tanaka, Y., Slitt, A. L., Leazeer, T. M., Maher, J. M. and Klaassen, C. D. (2005) Tissue distribution and hormonal regulation of the breast cancer resistence protein (Bcrp/Abcg2) in rats and mice. Biochem. Biophys. Res. Commun. 326, 181-187
37. Leslie, E. M., Deeley, R. G. and Cole, S. P. (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204, 216-237
38. Apte, M. V., Haber, P. S., Applegate, T. L., Norton, I. D., McCaughan, G. W., Korsten, M. A., Pirola, R. C. and Wilson, J. S. (1998) Periacinar stellate shaped cells in rat pancreas: identification, isolation and culture. Gut 43, 128-133
39. Kruse, M. L., Hildebrand, P. B., Timke, C., Fölsch, U. R. and Scmidt, W. E. (2000) Isolation, long-term culture, and characterization of rat pancreatic fibroblastoid/stellate cells. Pancreas 23, 49-54
40. Esni, F., Taljedal, I. B., Perkl, A. K., Cremer, H., Christofori, G. and Semb, H. (1999) Neural cell adhesion molecule (N-CAM) is required for cell type segregation and normal ultrastructure in pancreatic islets. J. Cell Biol. 144, 325-337
41. Royer, P. J., Tanguy-Royer, S., Ebstein, F., Sapede, C., Simon, T., Barbieux, I., Oger, R. and Gregoire, M. (2006) Culture medium and protein supplementation in the generation and maturation of dendritic cells. Scand. J. Immunol. 63, 401-409
42. Ratineau, C., Duluc, I., Pourreyron, C., Kedinger, M., Freund, J. N. and Roche, C. (2003) Endoderm- and mesenchyme-dependent commitment of the differentiated epithelial cell types in the developing intestine of rat. Differentiation 71, 163-169
43. Sttaford, D., White, R. J., Kinkel, M. D., Linville, A., Schilling, T. F. and Prince, V. E. (2006) Retinoids signal directly to zebrafish endoderm to specify insulin-expressing β-cells. Development 133, 949-956
44. Yue, F., Cui, L., Johkura, K., Ogiwara, N. and Sasaki, K. (2006) Glucagon-like peptide-1 differentiation of primate embryonic stem cells into insulin-producing cells.Tissue Eng. 12, 2105-2115
45. Abraham, E. J., Leech, C. A., Lin, J. C., Zulewski, H. and Haberner, J. F. (2002) Insulinotropic hormone glucagons-like peptide-1 differentiation of human pancreatic islet-derived progenitor cells into insulin-producing cells. Endocrinology 143, 3152-3161
46. Hui, H., Wright, C. and Perfetti, R. (2001) Glucagon-like peptide 1 induces differentiation of islets duodenal homeobox-1-positive pancreatic ductal cells into insulin-secreting cells. Diabetes 50, 785-796