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The Hepatic, Biliary, and Pancreatic Network of Stem/Progenitor Cell Niches in Humans: a New Reference Frame for Disease and Regeneration

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AMERICAN ASSOCIATION FOR THE STUDY OFLIVERD I S E ASES CONCISE REVIEWS | HEPATOLOGY, VOL. 64, NO. 1, 2016 The Hepatic, Biliary, and Pancreatic Network of Stem/Progenitor Cell Niches in Humans: A New Reference Frame for Disease and Regeneration Giacomo Lanzoni,1* Vincenzo Cardinale,2* and Guido Carpino3 Stem/progenitors for liver, biliary tree, and pancreas exist at early stages of development in the definitive ventral endo- derm forming the foregut. In humans, they persist postnatally as part of a network, with evidence supporting their contri- butions to hepatic and pancreatic organogenesis throughout life. Multiple stem cell niches persist in specific anatomical locations within the human biliary tree and pancreatic ducts. In liver and pancreas, replication of mature parenchymal cells ensures the physiological turnover and the restoration of parenchyma after minor injuries. Although actively debated, multiple observations indicate that stem/progenitor cells contribute to repair pervasive, chronic injuries. The most primitive of the stem/progenitor cells, biliary tree stem cells, are found in peribiliary glands within extrahepatic and large intrahepatic bile ducts. Biliary tree stem cells are comprised of multiple subpopulations with traits suggestive of maturational lineage stages and yet capable of self-replication and multipotent differentiation, being able to differentiate to mature liver cells (hepatocytes, cholangiocytes) and mature pancreatic cells (including functional islet endocrine cells). Hepatic stem cells are located within canals of Hering and bile ductules and are capable of differentiating to hepatocyte and cholangiocyte lineages. The existence, phenotype, and anatomical location of stem/progenitors in the adult pancreas are actively debated. Ongoing studies suggest that pancreatic stem cells reside within the biliary tree, primarily the hepa- topancreatic common duct, and are rare in the pancreas proper. Pancreatic ducts and pancreatic duct glands harbor com- mitted pancreatic progenitors. Conclusion: The hepatic, biliary, and pancreatic network of stem/progenitor cell niches should be considered as a framework for understanding liver and pancreatic regeneration after extensive or chronic inju- ries and for the study of human chronic diseases affecting these organs.(HEPATOLOGY 2016;64:277-286) ommon precursors for liver, bile duct system, transversum as migrating cords of stem cells and and pancreas exist at early stages of develop- alpha-fetoprotein1 hepatoblasts.(3) The hepatoblasts ment in the definitive ventral endoderm have the potential to restrict their lineage either toward C (1,2) (4) forming the foregut (Fig. 1A). hepatocytes or cholangiocytes. The stem cells and In human development, the hepatic diverticulum hepatoblasts around the mesenchyme of portal tracts emerges from the foregut.(3) The rostral part of the form the ductal plate, which undergoes a process of diverticulum forms the anlage of the liver and the com- remodeling leading to the formation of intrahepatic mon hepatic duct. The cells of the rostral part of the bile ducts (BDs) (Fig. 1B). In pediatric and adult liv- diverticulum bulge into the mesenchyme of the septum ers, the ductal plate transitions to become the canals of Abbreviations: BD, bile duct; BTSC, biliary tree stem cell; CoH, canals of Hering; EpCAM, epithelial cell adhesion molecule; HpSC, hepatic stem/ progenitor cell; PBG, peribiliary gland; PDG, pancreatic duct gland. Received June 29, 2015; accepted October 30, 2015. Additional Supporting Information may be found at onlinelibrary.wiley.com/doi/10.1002/hep.28326/suppinfo. *These authors contributed equally to this work. Supported by FIRB grant RBAP10Z7FS (to V.C. and G.C.), by PRIN grant 2009X84L84, by a sponsored research agreement from Vesta Therapeutics (Bethesda, MD), by Consorzio Interuniversitario Trapianti d’Organo (Rome, Italy), and by the Diabetes Research Institute Foundation (G.L.). Copyright VC 2015 by the American Association for the Study of Liver Diseases. View this article online at wileyonlinelibrary.com. DOI 10.1002/hep.28326 Potential conflict of interest: Nothing to report. 277 LANZONI, CARDINALE, AND CARPINO HEPATOLOGY, July 2016 Hering (CoH). At the liver hilum, the elongation and tors, are observed within the pancreatic ductal branching of the common hepatic duct gives rise to the system, in centroacinar cells [Fig. 4C], and in pan- larger intrahepatic BDs(4); peribiliary glands (PBGs) creatic duct glands [PDGs] [Fig. 3]) progressively bud from the surface epithelium of the These stem/progenitor cell niches may contribute larger intrahepatic and extrahepatic BDs (Fig. 1C). to repair pervasive, chronic injuries, whereas the repli- The caudal part of the hepatic diverticulum, connected cation of mature parenchymal cells ensures physiologi- to the foregut, gives rise to the extrahepatic biliary tree cal turnover and restoration of parenchyma after minor and ventral pancreas. At approximately 28-32 embry- injuries. onic days in humans (10.5 in mice), the caudal part of the diverticulum harbors biliopancreatic stem/progeni- tors coexpressing SOX17 and PDX1. Further segrega- tion of pancreatic and biliary precursors depends on Biliary Tree Stem/ specific transcription factors and signaling pathways (Fig. 1A; Supporting Fig. S1).(5) In adults, bilio- Progenitor Cells pancreatic stem/progenitors are retained within PBGs In the human extrahepatic biliary tree, the stem/pro- along the biliary tree. genitor niches have been identified as the PBGs (Fig. Dorsal and ventral pancreatic primordia derive from (1,7,8) 1 1 (6) 2A). PBGs bud from the extrahepatic BD epithe- PDX1 /PTF1A pancreatic stem/progenitors. lium.(9) In adults, PBGs predominantly occur at branch- These progenitors, which can mature into all pancreatic ing points of the biliary tree and are most numerous at parenchymal cells (acinar, ductal, and endocrine cells), (7,8) (6) the hepatopancreatic ampulla. PBGs contain niches branch into primitive epithelial tubules. The growth of cells, collectively termed BTSCs, with phenotypic traits of progenitor cells at the tips of tubules leaves behind a of stem/progenitors of endodermal origin with respect to progeny that forms the trunk region of evolving tubules. transcription factors (SOX17, PDX1, SOX9), surface Tip progenitors at the ends of tubules (PTF1A1, 1 1 1 markers (epithelial cell adhesion molecule [EpCAM], HES1 ,GATA4 ,SOX9 ) subsequently commit to LGR5) and cytoplasmic markers, and the capacity of pro- exocrine lineages and differentiate into acinar and ductal liferation, self-renewal, and multipotency.(1,7,8,10) Asub- cells. In the central duct area, NGN31 trunk progeni- (6) population (nearly 10%) of PBG cells appears to be tors commit to islet endocrine fates (Fig. 1A). primitive stem cells. These cells coexpress several pluripo- On the basis of the progenitor segregation, multiple tency markers (e.g., OCT4, SOX2, NANOG); they can stem cell niches persist in specific anatomical locations self-renew or differentiate into functional hepatocytes, within adult human organs: cholangiocytes, and pancreatic islets.(7) 1. biliary tree stem/progenitor cells (BTSCs) in PBGs There are no PBGs within the human gallbladder, along extrahepatic and large intrahepatic BDs (Figs. but BTSC subpopulations are present in outpouchings 2and3) of the surface epithelium (i.e., gallbladder crypts) and 2. hepatic stem/progenitors (HpSCs) in or near are later maturational lineage stages to those found CoH (Fig. 4A,B) within PBGs.(11) 3. pancreatic stem cells that appear confined to the Interestingly, a radial axis has been described in the biliary tree, particularly the hepatopancreatic com- organization of BTSC niches (Fig. 2B), mirroring that mon duct (their descendants, committed progeni- of the intestine.(8,12) ARTICLE INFORMATION: From the 1Diabetes Research Institute, University of Miami, Miami, FL; 2Department of Medico-Surgical Sciences, Sapienza University of Rome, Rome, Italy; 3Department of Movement, Human and Health Sciences, Division of Health Sciences, University of Rome “Foro Italico,” Rome, Italy. ADDRESS CORRESPONDENCE AND REPRINT REQUESTS TO: Guido Carpino, M.D., Ph.D. Piazza Lauro De Bosis, 6–00135, Rome, Italy Department of Movement, Human and Health Sciences E-mail: [email protected] Division of Health Sciences, University of Rome “Foro Italico” Tel/fax: 139 06 36733202 278 HEPATOLOGY, Vol. 64, No. 1, 2016 LANZONI, CARDINALE, AND CARPINO FIG. 1. Embryological development of Sox91 stem/progenitor cell niches. (A) Maturation of hepatic, biliary, and pancreatic lineages from foregut endoderm cells. Key transcription factors and biomarkers for each cell type are indicated. Niches harboring stem/progeni- tor cells during embryonic development or during adult life are indicated in blue. (B,C) Human fetus at 20 weeks of gestation. At 20 weeks of gestation, different stages of formation of the described structures coexist and can illustrate the progressive formation of inter- lobular bile ducts and peribiliary glands. (B) Development of interlobular bile ducts from ductal plate in human liver. (1) Specification of Sox91 ductal plate around a portal tract; ductal plate is composed of a single layer of Sox91 cells (arrow); (2) bilayered ductal plate is present (arrow); (3) formation of a lumen inside bilayered ductal plate (arrow); (4) integration of newly formed interlobular bile duct into the portal space (arrow); ductal plate undergoes further remodeling and remains as CoH/bile ductules in adult
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