Stem cell populations giving rise to liver, biliary tree, and pancreas

Stem Cells Handbook: Second Edition

Volumn , Issue , 2013, Pages 283-310

  Furth, Mark E ^a   Wang, Yunfang ^b   Cardinale, Vincenzo ^c   Carpino, Guido ^d   Lanzoni, Giacomo ^e   Cui, Cai Bin ^f   Wauthier, Eliane ^f   Gerber, David ^f   Oikawa, Tsunekazu ^f   Dominguez Bendala, Juan ^e   Inverardi, Luca ^e   Alvaro, Domenico ^c   Gaudio, Eugenio ^c   Reid, Lola M ^f  

^a WAKE FOREST BAPTIST HEALTH   (United States)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF ROME FORO ITALICO   (Italy)

^e UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84921470858     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-7696-2_21     Document Type: Chapter

References (110)

1. Cardinale V, Wang Y, Alpino G, Mendel G, Gaudio E, Reid LM, Alvaro D, et al. The biliary tree: a reservoir of multipotent stem cells. Nat Rev Gastroenterol Hepatol. 2012;9:231-40.
2. Wang Y, Lanzoni G, Carpino G, Cui C, Dominguez-Bendala J, Wauthier E, Cardinale V, Oikawa T, Pilegg A, Gerber D, Furth ME, Alvaro D, Gaudio E, Inverardi L, Reid LM. Biliary tree stem cells, precursors to pancreatic committed progenitors, evidence for lifelong pancreatic organogenesis. Stem Cells. 2013; in press.
3. Turner R, Lozoya O, Wang VF, Cardinale V, Gaudio E, Alpini G, Mendel G, Wauthier E, Barbier C, Alvaro D, Reid LM. Hepatic stem cells and maturational liver lineage biology. Hepatology. 2011;53:1035-45.
4. Furth ME, Childers MK, Reid LM. Stem and progenitor cells in regenerative pharmacology. In: Christ G, Erikson K, editors. Regenerative pharmacology. New York, NY: Cambridge University Press; 2013; pp. 75-126.
5. Christ GJ, Saul JM, Furth ME, Andersson KE. The pharmacology of regenerative medicine. Pharmacological Reviews 2013;65(3): 1091-1133.
6. Zorn AM, Wells JM. Molecular basis of vertebrate endoderm development. Int Rev Cytol. 2007;259:49-111.
7. McLin VA, Zorn AM. Organogenesis: making pancreas from liver. Curr Biol. 2003;13:R96-8.
8. Sinner D, Rankin S, Lee M, Zorn AM. Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development. 2004;131:3069-80.
9. Wandzioch E, Zaret KS. Dynamic signaling network for the specification of embryonic pancreas and liver progenitors. Science. 2009;324:1707-10.
10. Zaret K. Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. Dev Biol. 1999;209:1-10.
11. Tremblay KD, Zaret KS. Distinct populations of endoderm cells converge to generate the embryonic liver bud and ventral foregut tissues. Dev Biol. 2005;280:87-99.
12. Barker N, van de Wetering M, Clevers H. The intestinal stem cell. Genes Dev. 2008;22:1856-64.
13. Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M, et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell. 2010;6:25-36.
14. Lange AW, Keiser AR, Wells JM, Zorn AM, Whitsett JA. Sox17 promotes cell cycle progression and inhibits TGF-beta/Smad3 signaling to initiate progenitor cell behavior in the respiratory epithelium. PLoS One. 2009;4:e5711.
15. Snyder JC, Teisanu RM, Stripp BR. Endogenous lung stem cells and contribution to disease. J Pathol. 2009;217:254-64.
16. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic betacells are formed by self-duplication rather than stem-cell differentiation. Nature. 2004;429:41-6.
17. Houbracken I, Bouwens L. The quest for tissue stem cells in the pancreas and other organs, and their application in beta-cell replacement, 112-123. Rev Diabet Stud. 2010;7:112-23.
18. Xu X, D'Hoker J, Stange G, Bonne S, De Leu N, Xiao X, Van de Casteele M, Mellitzer G, Ling Z, Pipeleers D, Bouwens L, Scharfmann R, Gradwohl G, Heimberg H. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell. 2008;132:197-207.
19. Chung WS, Shin CH, Stainier DY. Bmp2 signaling regulates the hepatic versus pancreatic fate decision. Dev Cell. 2008;15:738-48.
20. Scadden DT. The stem cell niche as an entity of action. Nature. 2006;441:1075-9.
21. Cardinale V, Wang Y, Carpino G, Cui C, Inverardi L, Dominguez-Bendala J, Ricordi C, Mendel G, Furth ME, Gaudio E, Alvaro D, Reid L. Multipotent stem cells in the extrahepatic biliary tree give rise to hepatocytes, bile ducts and pancreatic islets. Hepatology. 2011;54:2159-72.
22. Carpino G, Cardinale V, Onori P, Franchitto A, Bartolomeo Berloco P, Rossi M, Wang Y, Semeraro R, Anceschi M, Brunelli R, Alvaro D, Reid LM, Gaudio G. Biliary tree stem/progenitor cells in glands of extrahepatic and intrahepatic bile ducts: an anatomical in situ study yielding evidence of maturational lineages. J Anat. 2012;220:186-99.
23. Saxena R, Theise N. Canals of Hering: recent insights and current knowledge. Semin Liver Dis. 2004;24:43-8.
24. Theise ND, Saxena R, Portmann BC, Thung SN, Yee H, Chiriboga L, Kumar A, Crawford JM. The canals of Hering and hepatic stem cells in humans. Hepatology. 1999;30:1425-33.
25. Zhang L, Theise N, Chua M, Reid LM. Human hepatic stem cells and hepatoblasts: symmetry between liver development and liver regeneration. Hepatology. 2008;48:1598-607.
26. Bonner-Weir S, Tosch IE, Inada A, Reitz P, Fonseca SY, Aye T, Sharma A. The pancreatic ductal epithelium serves as a potential pool of progenitor cells. Pediatr Diabetes. 2004;5:16-22.
27. Kushner JA, Weir GC, Bonner-Weir S. Ductal origin hypothesis of pancreatic regeneration under attack. Cell Metab. 2010;11:2-3.
28. Strobel O, Rosow DE, Rahaklin EY, Lauwers GY, Trainor AG, Alsina J, Castillo CF, Warshaw AL, Thayer SP. Pancreatic duct glands are distinct ductal compartments that react to chronic injury and mediate Shh-induced metaplasia. Gastroenterology. 2010;138:1166-77.
29. Kubota H, Reid LM. Clonogenic hepatoblasts, common precursors for hepatocytic and biliary lineages, are lacking classical major histocompatibility complex class I antigens. Proc Natl Acad Sci USA. 2000;97:12132-7.
30. McClelland R, Wauthier E, Uronis J, Reid LM. Gradient in extracellular matrix chemistry from periportal to pericentral zones: regulation of hepatic progenitors. Tissue Eng. 2008;14:59-70.
31. Schmelzer E, Zhang L, Bruce A, Wauthier E, Ludlow J, Yao H, Moss N, Melhem A, McClelland RL, Turner W, Kulik ML, Sherwood S, Tallheden T, Cheng N, Furth ME, Reid LM. Human hepatic stem cells from fetal and postnatal donors. J Exp Med. 2007;204:1973-87.
32. Sicklick JK, Li YX, Melhem A, Schmelzer E, Zdanowicz M, Huang J, Caballero M, Fair JH, Ludlow JW, McClelland RE, Reid LM, Diehl AM. Hedgehog signaling maintains resident hepatic progenitors throughout life. Am J Physiol Gastrointest Liver Physiol. 2006;290:G859-70.
33. Wang Y, Yao H, Barbier C, Wauthier E, Cui C, Moss N, Yamauchi M, Sricholpech M, Costello MJ, Gerber D, Loboa EG, Reid LM. Lineage-dependent epithelial-mesenchymal paracrine signals dictate growth versus differentiation of human hepatic stem cells to adult fates. Hepatology. 2010;52:1443-54.
34. Couvelard A, Bringuier AF, Dauge MC, Nejjari M, Darai E, Benifla JL, Feldmann G, Henin D, Scoazec JY. Expression of integrins during liver organogenesis in humans. Hepatology. 1998;27:839-47.
35. Kamiya A, Kinoshita T, Ito Y, Matsui T, Morikawa Y, Senba E, Nakashima K, Taga T, Yoshida K, Kishimoto T, Miyajima A. Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer. EMBO J. 1999;18:2127-36.
36. Kinoshita T, Miyajima A. Cytokine regulation of liver development. Biochim Biophys Acta. 2002;1592:303-12.
37. Kubota H, Yao H, Reid LM. Identification and characterization of vitamin A-storing cells in fetal liver. Stem Cells. 2007;25:2339-49.
38. Nakanuma Y, Hoso M, Sanzen T, Sasaki M. Microstructure and development of the normal and pathologic biliary tract in humans, including blood supply. A review. Microsc Res Tech. 1997;15:552-70.
39. Nakanuma Y, Katayanagi K, Terada T, Saito K. Intrahepatic peribiliary glands of humans. I. Anatomy, development and presumed functions. A review. J Gastroenterol Hepatol. 1994;9:75-9.
40. Nakanuma Y, Sasaki M, Terada T, Harada K. Intrahepatic peribiliary glands of humans. II. Pathological spectrum. J Gastroenterol Hepatol. 1994;9:80-6.
41. Wang Y, Cui C, Miguez P, Yamauchi M, Costello J, Wauthier E, Gerber D, Reid LM. Lineage restriction of hepatic stem cells to mature fates is made efficient by tissue-specific biomatrix scaffolds. Hepatology. 2011;53:293-305.
42. Wauthier E, McClelland R, Turner W, Schmelzer E, Kubota H, Zhang L, Ludlow J, Bruce A, Yao H, Furth ME, LeCluyse E, Moss N, Turner R, Merrick P, Barbier C, Lozoya O, Ruiz J, Reid LM. Hepatic stem cells and hepatoblasts: identification, isolation and ex vivo maintenance. Methods Cell Biol. 2008;86:137-225.
43. Michalopoulos GK. Liver regeneration: alternative epithelial pathways. Int J Biochem Cell Biol. 2011;43:173-9.
44. Cohen DE, Melton D. Turning straw into gold: directing cell fate for regenerative medicine. Nat Rev Genet. 2011;12:243-52.
45. Puppi J, Strom SJ, Hughes RD, Bansal S, Castell JV, Dagher I, Ellis ECS, Ericzon B, Fox IJ, Gómez-Lechón J, Guha C, Gupta S, Mitry JR, Ohashi K, Ott M, Reid LM, Roy-Chowdhury J, Sokal E, Weber A, Dhawana A. Improving the techniques for human hepatocyte transplantation: report from a consensus meeting in London. Cell Transplant. 2012;21(1):1-10.
46. Washburn ML, Bility MT, Zhang L, Kovalev GI, Buntzman A, Frelinger JA, Barry W, Ploss A, Rice CM, Su L. A humanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology. 2011;140:1334-44.
47. Fukumitsu K, Yagi H, Soto-Gutierrez A. Bioengineering in organ transplantation: targeting the liver. Transplant Proc. 2011;43:2137-8.
48. Gerlach JC. Bioreactors for extracorporeal liver support. Cell Transplant. 2006;15 Suppl 1:S91-103.
49. Parveen N, Aleem AK, Habeeb MA, Habibullah CM. An update on hepatic stem cells: bench to bedside. Curr Pharm Biotechnol. 2011;12:226-30.
50. Russo FP, Parola M. Stem and progenitor cells in liver regeneration and repair. Cytotherapy. 2011;13:135-44.
51. Duncan A, Hickey RD, Paulk NK, Culberson AJ, Olson SB, Finegold MJ, Grompe M. Ploidy reductions in murine fusion-derived hepatocytes. PLoS Genet. 2009;5(2):e1000385.
52. Formin ME, Tai LK, Bárcena A, Muench MO. Coexpression of CD14 and CD326 discriminate hepatic precursors in the human fetal liver. Stem Cells. 2011;20:1247-57.
53. Navarro-Alvarez N, Soto-Gutierrez A, Kobayashi N. Hepatic stem cells and liver development. Methods Mol Biol. 2010;640:181-236.
54. Tanaka M, Itoh T, Tanimizu N, Miyajima A. Liver stem/progenitor cells: their characteristics and regulatory mechanisms. J Biochem. 2011;149:231-9.
55. Thorgeirsson S, Factor V, Grisham J. Early activation and expansion of hepatic stem cells. In: Lanza R, Blau H, Melton DA, Moore DD, Thomas E, Verfaille CM, Weissman IL, West M, editors. Handbook of stem cells, vol. 2. New York, NY: Elsevier; 2004. p. 497-512.
56. Vessey CJ, de la Hall PM. Hepatic stem cells: a review. Pathology. 2001;33:130-41.
57. Rubin EM, Martin AA, Thung SN, Gerber MA. Morphometric and immunohistochemical characterization of human liver regeneration. Am J Pathol. 1995;147:397-404.
58. Ruebner BH, Blankenberg TA, Burrows DA, SooHoo W, Lund JK. Development and transformation of the ductal plate in the developing human liver. Pediatr Pathol. 1990;10:55-68.
59. De Alwis N, Hudson G, Burt AD, Day CP, Chinnery PF. Human liver stem cells originate from the canals of Hering. Hepatology. 2009;50:992-3.
60. Falkowski O, An HJ, Ianus IA, Chiriboga L, Yee H, West AB, Theise ND. Regeneration of hepatocyte 'buds' in cirrhosis from intrabiliary stem cells. J Hepatol. 2003;39:357-64.
61. Stachelscheid H, Urbaniak T, Ring A, Spengler B, Gerlach JC, Zeilinger K. Isolation and characterization of adult human liver progenitors from ischemic liver tissue derived from therapeutic hepatectomies. Tissue Eng Part A. 2009;15:1633-43.
62. McClelland R, Wauthier E, Zhang L, Barbier C, Melhem A, Schmelzer E, Reid LM. Ex vivo conditions for self-replication of human hepatic stem cells. Tissue Eng. 2008;14:1-11.
63. Schmelzer E, Reid LM. Telomerase activity in human hepatic stem cells, hepatoblasts and hepatocytes from neonatal, pediatric, adult and geriatric donors. Eur J Gastroenterol Hepatol. 2009;21:1191-8.
64. Oikawa T, Kamiya A, Zeniya M, Hyuck AD, Yamazaki Y, Wauthier E, Tajir H, Reid LM, Nakauchi H, et al. SALL4, a stem cell biomarker for liver cancers. Hepatology. 2013;57(4):1469-83.
65. Turner R, Gerber D, Reid LM. Transplantation of cells from solid organs requires grafting protocols. Transplantation. 2010;90:807-10.
66. Turner WS, Schmelzer E, McClelland R, Wauthier E, Chen W, Reid LM. Human hepatoblast phenotype maintained by hyaluronan hydrogels. J Biomed Mater. 2007;82:156-68.
67. Turner WS, Seagle C, Galanko J, Favorov O, Prestwich GD, Macdonald JM, Reid LM. Metabolomic footprinting of human hepatic stem cells and hepatoblasts cultured in engineered hyaluronanmatrix hydrogel scaffolds. Stem Cells. 2008;26:1547-55.
68. Lozoya OA, Wauthier E, Turner R, Barbier C, Prestwich GD, Guilak F, Superfine R, Lubkin SR, Reid LM. Mechanical properties of experimental models of the human liver's stem cell niche microenvironment. I. Biomaterials. 2011;32:7389-402.
69. Turner RA, Mendel G, Wauthier E, Barbier C, Reid LM. Hyaluronan-supplemented buffers preserve adhesion mechanisms facilitating cryopreservation of human hepatic stem/progenitor cells. Cell Transplantation. 2012;21(10):2257-2266.
70. Li W, Ding S. Small molecules that modulate embryonic stem cell fate and somatic cell reprogramming. Trends Pharmacol Sci. 2010;31:36-45.
71. Weber A, Groyer-Picard MT, Franco D, Dagher I. Hepatocyte transplantation in animal models. Liver Transpl. 2009;15:7-14.
72. Weber A, Mahieu-Caputo D, Michelle Hadchoue M, Franco D. Hepatocyte transplantation: studies in preclinical models. J Inherit Metab Dis. 2006;29:436-41.
73. Khan AA, Shaik MV, Parveen N, Rajendraprasad A, Aleem MA, Habeeb MA, Srinivas G, Raj TA, Tiwari SK, Kumaresan K, Venkateswarlu J, Pande G, Habibullah CM. Human fetal liver-derived stem cell transplantation as supportive modality in the management of end-stage decompensated liver cirrhosis. Cell Transplant. 2010;19:409-18.
74. Turner R, Wauthier E, Lozoya O, McClelland R, Bowsher J, Barbier C, Gerber D, Prestwich G, Hsu E, Reid LM. Successful transplantation of human hepatic stem cells with restricted localization to liver using hyaluronan grafts. Hepatology. 2013;57(2):775-84.
75. Macdonald JM, Xu A, Kubota H, Lecluyse E, Hamilton G, Liu H, Rong Y, Moss N, Lodestro C, Luntz T, Wolfe SP, Reid LM. Liver cell culture and lineage biology. In: Atala A, Lanza RP, editors. Methods of tissue engineering. London: Academic; 2002. p. 151-202.
76. Rojkind M, Gatmaitan Z, Mackensen S, Giambrone MA, Ponce P, Reid LM. Connective tissue biomatrix: its isolation and utilization for long-term cultures of normal rat hepatocytes. J Cell Biol. 1980;87:255-63.
77. Capila I, Linhardt RJ. Heparin ± protein interactions. Angew Chem Int Ed Engl. 2002;41:390-412.
78. Purushothaman A, Hurst DR, Pisano C, Mizumoto S, Sugahara K, Sanderson RD. Heparanase-mediated loss of nuclear syndecan-1 enhances histone acetyltransferase (HAT) activity to promote expression of genes that drive an aggressive tumor phenotype. J Biol Chem. 2011;286:30377-83.
79. Linhardt R, Liu J. Synthetic heparin. Curr Opin Pharmacol. 2012;12(2):217-9.
80. Fux L, Ilan N, Sanderson RD, Vlodavsky I. Heparanase busy at the cell surface. Trends Biochem Sci. 2009;34(10):511-9.
81. Ramani VC, Yang Y, Ren Y, Nan L, Sanderson RD. Heparanase plays a dual role in driving hepatocyte growth factor (HGF) signaling enhancing HGF expression and activity. J Biol Chem. 2011;286(8):6490-9.
82. Ramani VC, Pruett PS, Thompson CA, DeLucas LD, Sanderson RD. Heparan sulfate chains of syndecan-1 regulate ectodomain shedding. J Biol Chem. 2012;287(13):9952-61.
83. Chiang JY. Bile acid regulation of gene expression: roles of nuclear hormone receptors. Endocr Rev. 2002;23:443-63.
84. Perelman A, Brandan E. Different membrane-bound forms of acetylcholinesterase are present at the cell surface of hepatocytes. Eur J Biochem. 1989;182:203-7.
85. Alvaro D, Alpini G, Jezequel AM, Bassotti C, Francia C, Fraioli F, Romeo R, Marucci L, Le Sage G, Glaser SS, Benedetti A. Role and mechanisms of action of acetylcholine in the regulation of rat cholangiocyte secretory functions. J Clin Invest. 1997;100:1349-62.
86. LeSage EG, Alvaro D, Benedetti A, Glaser S, Marucci L, Baiocchi L, Eisel W, Caligiuri A, Phinizy JL, Rodgers R, Francis H, Alpini G. Cholinergic system modulates growth, apoptosis, and secretion of cholangiocytes from bile duct-ligated rats. Gastroenterology. 1999;117:191-9.
87. Vongchan P, Warda M, Toyoda H, Toida T, Marks RM, Linhardt RJ. Structural characterization of human liver heparan sulfate. Biochim Biophys Acta. 2005;1721:1-8.
88. Fujita M, Spray DC, Choi H, Saez JC, Watanabe T, Rosenberg LC, Hertzberg EL, Reid LM. Glycosaminoglycans and proteoglycans induce gap junction expression and restore transcription of tissue-specific mRNAs in primary liver cultures. Hepatology. 1987;7:1S-9.
89. Spray DC, Fujita M, Saez JC, Choi H, Watanabe T, Hertzberg E, Rosenberg LC, Reid LM. Proteoglycans and glycosaminoglycans induce gap junction synthesis and function in primary liver cultures. J Cell Biol. 1987;105:541-51.
90. Cervantes S, Lau J, Cano DA, Borromeo-Austin C, Hebrok M. Primary cilia regulate Gli/Hedgehog activation in pancreas. Proc Natl Acad Sci U S A. 2010;107:10109-14.
91. Huang BQ, Masyuk TV, Muff MA, Tietz PS, Masyuk AI, Larusso NF. Isolation and characterization of cholangiocyte primary cilia. Am J Physiol Gastrointest Liver Physiol. 2006;291:G500-9.
92. Masyuk AI, Masyuk TV, LaRusso NF. Cholangiocyte primary cilia in liver health and disease. Dev Dyn. 2008;237:2007-12.
93. Michalopoulos GK, Appasamy R. Metabolism of HGF-SF and its role in liver regeneration. EXS. 1993;65:275-83 [Review] [15 refs].
94. Michalopoulos GK, DeFrances MC. Liver regeneration. Science. 1997;276:60-6 [Review] [98 refs].
95. Liu H, Di Cunto F, Imarisio S, Reid LM. Citron kinase is a cell cycle-dependent, nuclear protein required for G2/M transition of hepatocytes. J Biol Chem. 2003;278:2541-8.
96. Sigal SH, Rajvanshi P, Gorla GR, Sokhi RP, Saxena R, Gebhard Jr.DR, Reid LM, Gupta S. Partial hepatectomy-induced polyploidy attenuates hepatocyte replication and activates cell aging events. Am J Physiol Gastrointest Liver Physiol. 1999;276:G1260-72.
97. Khan AA, Parveen N, Mahaboob VS, Prasad R, Ravindraprakash A, Venkateswarlu J, Rao P, Pande G, Lakshmi Narusu M, Khaja MN, Pramila R, Habeeb A, Habibullah CM. Management of hyperbilirubinemia in biliary atresia by hepatic progenitor cell transplantation through hepatic artery: a case report. Transplant Proc. 2008;40:1153-5.
98. Khan AA, Parveen N, Mahaboob VS, Rajendraprasad A, Ravindraprakas HR, Venkateswarlu J, Rao P, Pande G, Lakshmi Narusu M, Khaja MN, Pramila R, Habeeb A, Habibullah CM. Treatment of Crigler-Najjar Syndrome type 1 by hepatic progenitor cell therapy: a simple procedure for hyperbilirubinemia. Transplant Proc. 2008;40:1148-50.
99. Taylor CJ, Bolton EM, Pocock S, Sharples LD, Pedersen RA, Bradley JA. Banking on human embryonic stem cells: estimating the number of donor cell lines needed for HLA matching. Lancet. 2005;366:2019-25.
100. Cirulli V, Beattie GM, Klier G, Ellisman M, Ricordi C, Quaranta V, Frasier F, Ishii JK, Hayek A, Salomon DR. Expression and function of alpha(v)beta(3) and alpha(v)beta(5) integrins in the developing pancreas: roles in the adhesion and migration of putative endocrine progenitor cells. J Cell Biol. 2000;150:1445-60.
101. Cirulli V, Crisa L, Beattie GM, Mally MI, Lopez AD, Fannon A, Ptasznik A, Inverardi L, Ricordi C, Deerinck T, Ellisman M, Reisfeld RA, Hayek A. KSA antigen EpCAM mediates cell-cell adhesion of pancreatic epithelial cells: morphoregulatory roles in pancreatic islet development. J Cell Biol. 1998;140:1519-34.
102. Frandsen U, Porneki AD, Floridon C, Abdallah BM, Kassem M. Activin B mediated induction of Pdx1 in human embryonic stem cell derived embryoid bodies. Biochem Biophys Res Commun. 2007;362:568-74.
103. Hayes A, Tudor D, Nowell M, Caterson B, Hughes C. Unique forms of chondroitin sulfate proteoglycans in stem cell niches. J Histochem Cytochem. 2007;56:125-38.
104. Hori Y, Fukumoto M, Kuroda Y. Enrichment of putative pancreatic progenitor cells from mice by sorting for prominin1 (CD133) and platelet-derived growth factor receptor beta. Stem Cells. 2008; 26:2912-20.
105. Jiang W, Sui X, Zhang D, Liu M, Ding M, Shi Y, Deng H. CD24: a novel surface marker for PDX1-positive pancreatic progenitors derived from human embryonic stem cells. Stem Cells. 2011; 29:609-17.
106. Koblas T, Zacharovová K, Berková Z, Mindlová M, Girman P, Dovolilová E, Karasová L, Saudek F. Isolation and characterization of human CXCR4-positive pancreatic cells. Folia Biol (Praha). 2007;53:13-22.
107. Lardon J, Corbeil D, Huttner WB, Ling Z, Bouwens L. Stem cell marker prominin-1/AC133 is expressed in duct cells of the adult human pancreas. Pancreas. 2008;36:e1-6.
108. Schaffer AE, Freude KK, Nelson SB, Sander M. Nkx6 transcription factors and Ptf1a function as antagonistic lineage determinants in multipotent pancreatic progenitors. Dev Dyn. 2010;18:1022-9.
109. Segev H, Fishman B, Schulman R, Itskovitz-Eldor J. The expression of the class 1 glucose transporter isoforms in human embryonic stem cells, and the potential use of GLUT2 as a marker for pancreatic progenitor enrichment. Stem Cell Dev. 2012;21:1653-61.
110. Smukler SR, Arntfield ME, Razavi R, Bikopoulos G, Karpowicz P, Seaberg R, Dai F, Lee S, Ahrens R, Fraser PE, Wheeler MB, Van der Koo D. The adult mouse and human pancreas contain rare multipotent stem cells that express insulin. Cell Stem Cell. 2011;8:281-93.