Human hepatic stem cell and maturational liver lineage biology

Hepatology

Volumn 53, Issue 3, 2011, Pages 1035-1045

  Turner, Rachael ^a   Lozoya, Oswaldo ^a   Wang, Yunfang ^a   Cardinale, Vincenzo ^b   Gaudio, Eugenio ^c   Alpini, Gianfranco ^d   Mendel, Gemma ^a   Wauthier, Eliane ^a   Barbier, Claire ^a   Alvaro, Domenico ^b   Reid, Lola M ^a  

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

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF ROME   (Italy)

^d SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BILE DUCT; BILE FLOW; CANCER STEM CELL; CELL COMPARTMENTALIZATION; CELL DIVISION; CELL LINE; CELL MATURATION; CELL POPULATION; CELL SECRETION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHROMATIN; DUODENUM; FEEDBACK SYSTEM; FETUS LIVER; GENE OVEREXPRESSION; HEPATOPANCREAS; HUMAN; HUMAN CELL; LIVER CANCER; LIVER PARENCHYMA; LIVER REGENERATION; LIVER STEM CELL; LIVER WEIGHT; MESENCHYME CELL; METHYLATION; MOLECULAR MECHANICS; PANCREAS DUCT; PARACRINE SIGNALING; PERINATAL PERIOD; PLOIDY; PRIORITY JOURNAL; STEM CELL; STEM CELL NICHE;

BILE DUCTS; CELL LINEAGE; HUMANS; LIVER; PARACRINE COMMUNICATION; STEM CELLS;

EID: 79952254947     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24157     Document Type: Article

References (66)

1. Sigal SH, Brill S, Fiorino AS, Reid LM. The liver as a stem cell and lineage system. Am J Physiol 1992; 263: G139-G148.
2. 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: 2541-2548.
3. Tanaka M, Okabe M, Suzuki K, Kamiya Y, Tsukahara Y, Saito S, et al. Mouse hepatoblasts at distinct developmental stages are characterized by expression of EpCAM and DLK1: drastic change of EpCAM expression during liver development. Mech Dev 2009; 126: 665-676.
4. Okabe M, Tsukahara Y, Tanaka M, Suzuki K, Saito S, Kamiya Y, et al. Potential hepatic stem cells reside in EpCAM+ cells of normal and injured mouse livers. Development 2009; 136: 1951-1960.
5. Sicklick JK, Li YX, Melhem A, Schmelzer E, Zdanowicz M, Huang J, et al. Hedgehog signaling maintains resident hepatic progenitors throughout life. Am J Physiol Gastrointest Liver Physiol 2006; 290: G859-G870.
6. Schmelzer E, Wauthier E, Reid LM. The phenotypes of pluripotent human hepatic progenitors. Stem Cells 2006; 24: 1852-1858.
7. Schmelzer E, Zhang L, Bruce A, Wauthier E, Ludlow J, Yao H, et al. Human hepatic stem cells from fetal and postnatal donors. J Exp Med 2007; 204: 1973-1987.
8. Zhang L, Theise N, Chua M, Reid LM. Human hepatic stem cells and hepatoblasts: symmetry between liver development and liver regeneration. HEPATOLOGY 2008; 48: 1598-1607.
9. Kuwahara R, Kofman AV, Landis CS, Swenson ES, Barendswaard E, Theise ND. The hepatic stem cell niche: identification by label retaining cell assay. HEPATOLOGY 2008; 47: 1994-2002.
10. Saxena R, Theise N. Canals of Hering: recent insights and current knowledge. Semin Liver Dis 2004; 24: 43-48.
11. 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 A 2009; 15: 1633-1643.
12. Zhou H, Rogler LE, Teperman L, Morgan G, Rogler CE. Identification of hepatocytic and bile ductular cell lineages and candidate stem cells in bipolar ductular reactions in cirrhotic human liver. HEPATOLOGY 2007; 45: 716-724.
13. Wang Y, Yao H-l, Barbier C, Wauthier E, Cui C-b, Moss N, et al. Lineage-dependent epithelial-mesenchymal paracrine signals dictate growth versus differentiation of human hepatic stem cells to adult fates. HEPATOLOGY 2010; 52: 1443-1454.
14. Crosby HA, Kelly DA, Strain AJ. Human hepatic stem-like cells isolated using c-kit or CD34 can differentiate into biliary epithelium. Gastroenterology 2001; 120: 534-544.
15. Theise ND, Saxena R, Portmann BC, Thung SN, Yee H, Chiriboga L, et al. The canals of Hering and hepatic stem cells in humans. HEPATOLOGY 1999; 30: 1425-1433.
16. Schmelzer E, Wauthier E, Reid LM. Phenotypes of pluripotent human hepatic progenitors. Stem Cell 2006; 24: 1852-1858.
17. McClelland R, Wauthier E, Zhang L, Barbier C, Melhem A, Schmelzer E, et al. Ex vivo conditions for self-replication of human hepatic stem cells. Tissue Eng 2008; 14: 1-11.
18. Wang Y, Cui C, Miguez P, Yamauchi M, Costello J, Wauthier E, et al. Lineage restriction of hepatic stem cells to mature fates is made efficient by tissue-specific biomatrix scaffolds. HEPATOLOGY 2011; 53: 293-305.
19. Kubota H, Reid LM. Clonogenic hepatoblasts, common precursors for hepatocytic and biliary lineages, are lacking classical major histocompatibility complex class I antigen. Proc Natl Acad Sci U S A 2000; 97: 12132-12137.
20. Wauthier E, Schmelzer E, Turner W, Zhang L, Lecluyse E, Ruiz J, et al. Hepatic stem cells and hepatoblasts: identification, isolation, and ex vivo maintenance. Methods Cell Biol 2008; 86: 137-225.
21. Turner WS, Seagle C, Galanko JA, Favorov O, Prestwich GD, Macdonald JM, et al. Nuclear magnetic resonance metabolomic footprinting of human hepatic stem cells and hepatoblasts cultured in hyaluronan-matrix hydrogels. Stem Cells 2008; 26: 1547-1555.
22. Roskams TA, Theise ND, Balabaud C, Bhagat G, Bhathal PS, Bioulac-Sage P, et al. Nomenclature of the finer branches of the biliary tree: canals, ductules, and ductular reactions in human livers. HEPATOLOGY 2004; 39: 1739-1745.
23. Kubota H, Yao H, Reid LM. Identification and characterization of vitamin A-storing cells in fetal liver. Stem Cell 2007; 25: 2339-2349.
24. Turner WS, Schmelzer E, McClelland R, Wauthier E, Chen W, Reid LM. Human hepatoblast phenotype maintained by hyaluronan hydrogels. J Biomed Mater Res B Appl Biomater 2007; 82: 156-168.
25. Haruna Y, Saito K, Spaulding S, Nalesnik MA, Gerber MA. Identification of bipotential progenitor cells in human liver development. HEPATOLOGY 1996; 23: 476-481.
26. Kubota H, Storms RW, Reid LM. Variant forms of alpha-fetoprotein transcripts expressed in human hematopoietic progenitors. Implications for their developmental potential towards endoderm. J Biol Chem 2002; 277: 27629-27635.
27. Schmelzer E, Reid LM. Telomerase activity in human hepatic stem cells, hepatoblasts and hepatocytes from neonatal, pediatric, adult and geriatric donors. Eur J Hepatol Gastroenterol 2009; 21: 1191-1198.
28. Tan J, Hytiroglou P, Wieczorek R, Park YN, Thung SN, Arias B, et al. Immunohistochemical evidence for hepatic progenitor cells in liver diseases. Liver 2002; 22: 365-373.
29. Alvaro D, Mancino MG, Glaser S, Gaudio E, Marzioni M, Francis H, et al. Proliferating cholangiocytes: a neuroendocrine compartment in the diseased liver. Gastroenterology 2007; 132: 415-431.
30. Glaser S, Francis H, DeMorrow S, LeSage G, Fava G, Marzioni M, et al. Heterogeneity of the intrahepatic biliary epithelium. World J Gastroenterol 2006; 12: 3523-3536.
31. Alpini G, Ulrich C, Roberts S, Phillips JO, Ueno Y, Podila PV, et al. Molecular and functional heterogeneity of cholangiocytes from rat liver after bile duct ligation. Am J Physiol 1997; 272: G289-297.
32. Alpini G, Ueno Y, Glaser SS, Marzioni M, Phinizy JL, Francis H, et al. Bile acid feeding increased proliferative activity and apical bile acid transporter expression in both small and large rat cholangiocytes. HEPATOLOGY 2001; 34: 868-876.
33. Duncan A, Hickey RD, Paulk NK, Culberson AJ, Olson SB, Finegold MJ, et al. Ploidy reductions in murine fusion-derived hepatocytes. PLoS Genet 2009; 5: e1000385.
34. Rhim JA, Sandgren EP, Degen JL, Palmiter RD, Brinster RL. Replacement of diseased mouse liver by hepatic cell transplantation. Science 1994; 263: 1149-1152.
35. Alvaro D, Alpini G, Jezequel AM, Bassotti C, Francia C, Fraioli F, et al. Role and mechanisms of action of acetylcholine in the regulation of rat cholangiocyte secretory functions. J Clin Invest 1997; 100: 1349-1362.
36. Ueno Y, Alpini G, Yahagi K, Kanno N, Moritoki Y, Fukushima K, et al. Evaluation of differential gene expression by microarray analysis in small and large cholangiocytes isolated from normal mice. Liver Int 2003; 23: 449-459.
37. Terada T, Kato M, Horie S, Endo K, Kitamura Y. Expression of pancreatic alpha-amylase protein and messenger RNA in hilar primitive bile ducts and hepatocytes during human fetal liver organogenesis: an immunohistochemical and in situ hybridization study. Liver 1998; 18: 313-319.
38. LeSage GD, Glaser SS, Marucci L, Benedetti A, Phinizy JL, Rodgers R, et al. Acute carbon tetrachloride feeding induces damage of large but not small cholangiocytes from BDL rat liver. Am J Physiol 1999; 276: G1289-G1301.
39. Mancinelli R, Franchitto A, Gaudio E, Onori P, Glaser S, Francis H, et al. After damage of large bile ducts by gamma-aminobutyric acid, small ducts replenish the biliary tree by amplification of calcium-dependent signaling and de novo acquisition of large cholangiocyte phenotypes. Am J Pathol 2010; 176: 1790-1800.
40. Bishop JR, Schuksz M, Esko JD, Bishop JR, Schuksz M, Esko JD. Heparan sulfate proteoglycans fine-tune mammalian physiology. Nature 2007; 446: 1030-1037.
41. Jhandier MN, Kruglov EA, Lavoie EG, Sevigny J, Dranoff JA. Portal fibroblasts regulate the proliferation of bile duct epithelia via expression of NTPDase2. J Biol Chem 2005; 280: 22986-22992.
42. Woo K, Dutta AK, Patel V, Kresge C, Feranchak AP. Fluid flow induces mechanosensitive ATP release, calcium signalling and Cl- transport in biliary epithelial cells through a PKCzeta-dependent pathway. J Physiol 2008; 586: 2779-2798.
43. Cassiman D, Libbrecht L, Sinelli N, Desmet V, Denef C, Roskams T. The vagal nerve stimulates activation of the hepatic progenitor cell compartment via muscarinic acetylcholine receptor type 3. Am J Pathol 2002; 161: 521-530.
44. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126: 677-689.
45. Krieg M, Arboleda-Estudillo Y, Puech PH, Kafer J, Graner F, Muller DJ, et al. Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 2008; 10: 429-436.
46. Schwartz MA, DeSimone DW. Cell adhesion receptors in mechanotransduction. Curr Opin Cell Biol 2008; 20: 551-556.
47. Sakata R, Ueno T, Nakamura T, Ueno H, Sata M. Mechanical stretch induces TGF-beta synthesis in hepatic stellate cells. Eur J Clin Invest 2004; 34: 129-136.
48. Batut J, Howell M, Hill CS. Kinesin-mediated transport of Smad2 is required for signaling in response to TGF-beta ligands. Dev Cell 2007; 12: 261-274.
49. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005; 19: 2783-2810.
50. Praetorius HA, Spring KR. A physiological view of the primary cilium. Annu Rev Physiol 2005; 67: 515-529.
51. Eggenschwiler JT, Anderson KV. Cilia and developmental signaling. Annu Rev Cell Dev Biol 2007; 23: 345-373.
52. King PJ, Guasti L, Laufer E. Hedgehog signalling in endocrine development and disease. J Endocrinol 2008; 198: 439-450.
53. Kim J, Kato M, Beachy PA. Smoothened in the primary cilum to transcriptional activation in the nucleus. Proc Natl Acad Sci U S A 2009; 106: 21666-21671.
54. McLin VA, Rankin SA, Zorn AM. Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 2007; 134: 2207-2217.
55. Ober EA, Field HA, Stainier DY. From endoderm formation to liver and pancreas development in zebrafish. Mech Dev 2003; 120: 5-18.
56. Cohen MM Jr. The hedgehog signaling network. Am J Med Genet 2003: 5-28.
57. Rivas-Carrillo JD, Okitsu T, Tanaka N, Kobayashi N. Pancreas development and beta-cell differentiation of embryonic stem cells. Curr Med Chem 2007; 14: 1573-1578.
58. Sangeetha NM, Bhat S, Choudhury AR, Maitra U, Terech P. Properties of hydrogels derived from cationic analogues of bile acid: remarkably distinct flowing characteristics. J Phys Chem B 2004; 108: 16056-16063.
59. Luo X, Li W, Bird N, Chin SB, Hill NA, Johnson AG. On the mechanical behavior of the human biliary system. World J Gastroenterol 2007; 13: 1384-1392.
60. Sigal SH, Rajvanshi P, Gorla GR, Sokhi RP, Saxena R, Gebhard DR Jr et al. Partial hepatectomy-induced polyploidy attenuates hepatocyte replication and activates cell aging events. Am J Physiol Gastrointest Liver Physiol 1999; 276: G1260-G1272.
61. Roskams T. Liver stem cells and their implication in hepatocellular and cholangiocarcinoma. Oncogene 2006; 25: 3818-3822.
62. Turner R, Gerber D, Reid L. The future of cell transplant therapies: a need for tissue grafting. Transplantation 2010; 90: 807-810.
63. Potter VR. The present status of the blocked ontogeny hypothesis of neoplasia: the thalassemia connection. Oncodevel Biol Med 1981; 2: 243-266.
64. Sell S. On the stem cell origin of cancer. Am J Pathol 2010; 176: 1-11.
65. Yamashita Y, Ji J, Budhu A, Forgues M, Jia H, Ye Q, et al. Wnt/β-catenin signaling regulates cancer initiating cells (EpCAM+ AFP+) with stem cell features and metastatic activities in hepatocellular carcinoma. Gastroenterology 2009; 136: 1012-1024.
66. Yamashita T, Forgues M, Wang W, Kim JW, Ye Q, Jia H, et al. EpCAM and alpha-fetoprotein expression defines novel prognostic subtypes of hepatocellular carcinoma. Cancer Res 2008; 68: 1451-1461.