CoChat
Sign Up
Cited by 64Liver physiology and pathologyCellular Mechanics and InteractionsCell Adhesion Molecules Research

The unique polarity phenotype of hepatocytes

Open access
Müsch, Anne·2014·Experimental Cell Research
DOI 10.1016/j.yexcr.2014.06.006PMC PMC4254207
Open this paper in CoChat — free account

Abstract

Hepatocytes, the main epithelial cell type of the liver, function like all epithelial cells to mediate the vectorial flow of macromolecules into and out of the organ they encompass. They do so by establishing polarized surface domains and by restricting paracellular flow via their tight junctions and cell-cell adhesion. Yet, the cell and tissue organization of hepatocytes differs profoundly from that of most other epithelia, including those of the digestive and urinary tracts, the lung or the breast. The latter form monolayered tissues in which the apical domains of individual cells align around a central continuous luminal cavity that constitutes the tubules and acini characteristic of these organs. Hepatocytes, by contrast, form capillary-sized lumina with multiple neighbors resulting in a branched, tree-like bile canaliculi network that spreads across the liver parenchyme. I will discuss some of the key molecular features that distinguish the hepatocyte polarity phenotype from that of monopolar, columnar epithelia.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.yexcr.2014.06.006

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 58

  1. [1]Baloch Z Klapper J Buchanan L Schwartz M Amenta PS Ontogenesis of the murine hepatic extracellular matrix: an immunohistochemical study Differentiation 1992 51 3 209 218 1459362
  2. [2]Stamatoglou SC Enrich C Manson MM Hughes RC Temporal changes in the expression and distribution of adhesion molecules during liver development and regeneration The Journal of cell biology 1992 116 6 1507 1515 1531833 PMC2289376
  3. [3]Ogawa K Medline A Farber E Sequential analysis of hepatic carcinogenesis: the comparative architecture of preneoplastic, malignant, prenatal, postnatal and regenerating liver British journal of cancer 1979 40 5 782 790 41564 PMC2010106
  4. [5]Petersen BE Zajac VF Michalopoulos GK Bile ductular damage induced by methylene dianiline inhibits oval cell activation Am J Pathol 1997 151 4 905 909 9327722 PMC1858051
  5. [6]Yin L Lynch D Ilic Z Sell S Proliferation and differentiation of ductular progenitor cells and littoral cells during the regeneration of the rat liver to CCl4/2-AAF injury Histol Histopathol 2002 17 1 65 81 11813887
  6. [7]Decaens C Rodriguez P Bouchaud C Cassio D Establishment of hepatic cell polarity in the rat hepatoma-human fibroblast hybrid WIF-B9. A biphasic phenomenon going from a simple epithelial polarized phenotype to an hepatic polarized one Journal of cell science 1996 109 Pt 6 1623 1635 8799849
  7. [8]Bartles JR Hubbard AL Preservation of hepatocyte plasma membrane domains during cell division in situ in regenerating rat liver Dev Biol 1986 118 1 286 295 3533679
  8. [9]Slim CL Par1b induces asymmetric inheritance of plasma membrane domains via LGN-dependent mitotic spindle orientation in proliferating hepatocytes PLoS biology 2013 11 12 e1001739 24358023 PMC3866089
  9. [10]Lazaro-Dieguez F Par1b links lumen polarity with LGN-NuMA positioning for distinct epithelial cell division phenotypes The Journal of cell biology 2013 203 2 251 264 24165937 PMC3812971
  10. [11]Wang T Yanger K Stanger BZ Cassio D Bi E Cytokinesis defines a spatial landmark for hepatocyte polarization and apical lumen formation Journal of cell science 2014 127 Pt 11 2483 2492 24706948 PMC4038943
  11. [12]Kemphues KJ Priess JR Morton DG Cheng NS Identification of genes required for cytoplasmic localization in early C. elegans embryos Cell 1988 52 3 311 320 3345562
  12. [13]Cohen D Brennwald PJ Rodriguez-Boulan E Musch A Mammalian PAR-1 determines epithelial lumen polarity by organizing the microtubule cytoskeleton The Journal of cell biology 2004 164 5 717 727 14981097 PMC2172160
  13. [14]Cohen D Rodriguez-Boulan E Musch A Par-1 promotes a hepatic mode of apical protein trafficking in MDCK cells Proceedings of the National Academy of Sciences of the United States of America 2004 101 38 13792 13797 15365179 PMC518835
  14. [15]Woods A LKB1 is required for hepatic bile acid transport and canalicular membrane integrity in mice Biochem J 2011 434 1 49 60 21118154 PMC3262187
  15. [16]Tuma PL Nyasae LK Hubbard AL Nonpolarized cells selectively sort apical proteins from cell surface to a novel compartment, but lack apical retention mechanisms Mol Biol Cell 2002 13 10 3400 3415 12388745 PMC129954
  16. [17]Homolya L LKB1/AMPK and PKA control ABCB11 trafficking and polarization in hepatocytes PloS one 2014 9 3 e91921 24643070 PMC3958433
  17. [18]Fu D Wakabayashi Y Ido Y Lippincott-Schwartz J Arias IM Regulation of bile canalicular network formation and maintenance by AMP-activated protein kinase and LKB1 Journal of cell science 2010 123 Pt 19 3294 3302 20826460 PMC2939801
  18. [19]Zhang L Li J Young LH Caplan MJ AMP-activated protein kinase regulates the assembly of epithelial tight junctions Proceedings of the National Academy of Sciences of the United States of America 2006 103 46 17272 17277 17088526 PMC1859922
  19. [20]Zheng B Cantley LC Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase Proceedings of the National Academy of Sciences of the United States of America 2007 104 3 819 822 17204563 PMC1783397
  20. [21]Bultot L Myosin light chains are not a physiological substrate of AMPK in the control of cell structure changes FEBS letters 2009 583 1 25 28 19061891
  21. [22]Fu D Coordinated elevation of mitochondrial oxidative phosphorylation and autophagy help drive hepatocyte polarization Proceedings of the National Academy of Sciences of the United States of America 2013 110 18 7288 7293 23589864 PMC3645550
  22. [23]Fu D Lippincott-Schwartz J Arias IM Increased mitochondrial fusion and autophagy help isolated hepatocytes repolarize in collagen sandwich cultures Autophagy 2013 9 12 2154 2155 24212064
  23. [24]Fu D Wakabayashi Y Lippincott-Schwartz J Arias IM Bile acid stimulates hepatocyte polarization through a cAMP-Epac-MEK-LKB1-AMPK pathway Proceedings of the National Academy of Sciences of the United States of America 2011 108 4 1403 1408 21220320 PMC3029747
  24. [25]Ng KH Le Goascogne C Amborade E Stieger B Deschatrette J Reversible induction of rat hepatoma cell polarity with bile acids Journal of cell science 2000 113 Pt 23 4241 4251 11069769
  25. [26]Little JM Richey JE Van Thiel DH Lester R Taurocholate pool size and distribution in the fetal rat J Clin Invest 1979 63 5 1042 1049 447826 PMC372047
  26. [27]Dunn JC Tompkins RG Yarmush ML Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration Biotechnol Prog 1991 7 3 237 245 1367596
  27. [28]Ezzell RM Effect of collagen gel configuration on the cytoskeleton in cultured rat hepatocytes Exp Cell Res 1993 208 2 442 452 8375473
  28. [29]Ojakian GK Nelson WJ Beck KA Mechanisms for de novo biogenesis of an apical membrane compartment in groups of simple epithelial cells surrounded by extracellular matrix Journal of cell science 1997 110 Pt 22 2781 2794 9427287
  29. [30]Herrema H Rho kinase, myosin-II, and p42/44 MAPK control extracellular matrix-mediated apical bile canalicular lumen morphogenesis in HepG2 cells Mol Biol Cell 2006 17 7 3291 3303 16687572 PMC1552049
  30. [31]Marjoram RJ Lessey EC Burridge K Regulation of RhoA activity by adhesion molecules and mechanotransduction Current molecular medicine 2014 14 2 199 208 24467208 PMC3929014
  31. [32]Konopka G Tekiela J Iverson M Wells C Duncan SA Junctional adhesion molecule-A is critical for the formation of pseudocanaliculi and modulates E-cadherin expression in hepatic cells The Journal of biological chemistry 2007 282 38 28137 28148 17623668
  32. [33]Braiterman LT JAM-A is both essential and inhibitory to development of hepatic polarity in WIF-B cells Am J Physiol Gastrointest Liver Physiol 2008 294 2 G576 588 18096610
  33. [34]Cohen D Tian Y Musch A Par1b promotes hepatic-type lumen polarity in Madin Darby canine kidney cells via myosin II- and E-cadherin-dependent signaling Mol Biol Cell 2007 18 6 2203 2215 17409351 PMC1877095
  34. [35]Peng X How to induce non-polarized cells of hepatic origin to express typical hepatocyte polarity: generation of new highly polarized cell models with developed and functional bile canaliculi Cell Tissue Res 2006 323 2 233 243 16231191
  35. [36]Bartles JR Feracci HM Stieger B Hubbard AL Biogenesis of the rat hepatocyte plasma membrane in vivo: comparison of the pathways taken by apical and basolateral proteins using subcellular fractionation The Journal of cell biology 1987 105 3 1241 1251 3654750 PMC2114787
  36. [37]Barr VA Scott LJ Hubbard AL Immunoadsorption of hepatic vesicles carrying newly synthesized dipeptidyl peptidase IV and polymeric IgA receptor The Journal of biological chemistry 1995 270 46 27834 27844 7499255
  37. [38]Larkin JM Intracellular accumulation of pIgA-R and regulators of transcytotic trafficking in cholestatic rat hepatocytes Hepatology 2003 38 5 1199 1209 14578858
  38. [39]Kipp H Arias IM Newly synthesized canalicular ABC transporters are directly targeted from the Golgi to the hepatocyte apical domain in rat liver The Journal of biological chemistry 2000 275 21 15917 15925 10748167
  39. [40]Bastaki M Braiterman LT Johns DC Chen YH Hubbard AL Absence of direct delivery for single transmembrane apical proteins or their “Secretory” forms in polarized hepatic cells Mol Biol Cell 2002 13 1 225 237 11809835 PMC65084
  40. [41]Slimane TA Trugnan G Van ISC Hoekstra D Raft-mediated trafficking of apical resident proteins occurs in both direct and transcytotic pathways in polarized hepatic cells: role of distinct lipid microdomains Mol Biol Cell 2003 14 2 611 624 12589058 PMC149996
  41. [42]Rodriguez-Boulan E Macara IG Organization and execution of the epithelial polarity programme Nature reviews. Molecular cell biology 2014 15 4 225 242 PMC4211427 24651541
  42. [43]Saucan L Palade GE Differential colchicine effects on the transport of membrane and secretory proteins in rat hepatocytes in vivo: bipolar secretion of albumin Hepatology 1992 15 4 714 721 1551647
  43. [44]Wojtal KA de Vries E Hoekstra D van Ijzendoorn SC Efficient trafficking of MDR1/P-glycoprotein to apical canalicular plasma membranes in HepG2 cells requires PKA-RIIalpha anchoring and glucosylceramide Mol Biol Cell 2006 17 8 3638 3650 16723498 PMC1525225
  44. [45]Puertollano R The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells The Journal of cell biology 1999 145 1 141 151 10189374 PMC2148211
  45. [46]Cheong KH Zacchetti D Schneeberger EE Simons K VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells Proceedings of the National Academy of Sciences of the United States of America 1999 96 11 6241 6248 10339572 PMC26866
  46. [47]Ramnarayanan SP Cheng CA Bastaki M Tuma PL Exogenous MAL reroutes selected hepatic apical proteins into the direct pathway in WIF-B cells Mol Biol Cell 2007 18 7 2707 2715 17494867 PMC1924826
  47. [48]In JG Tuma PL MAL2 selectively regulates polymeric IgA receptor delivery from the Golgi to the plasma membrane in WIF-B cells Traffic 2010 11 8 1056 1066 20444237 PMC2904422
  48. [49]Tuma P Hubbard AL Transcytosis: crossing cellular barriers Physiological reviews 2003 83 3 871 932 12843411
  49. [50]Ait-Slimane T Galmes R Trugnan G Maurice M Basolateral internalization of GPI-anchored proteins occurs via a clathrin-independent flotillin-dependent pathway in polarized hepatic cells Mol Biol Cell 2009 20 17 3792 3800 19605558 PMC2735478
  50. [51]Rahner C Stieger B Landmann L Apical endocytosis in rat hepatocytes In situ involves clathrin, traverses a subapical compartment, and leads to lysosomes Gastroenterology 2000 119 6 1692 1707 11113091
  51. [52]Hoekstra D Tyteca D van ISC The subapical compartment: a traffic center in membrane polarity development Journal of cell science 2004 117 Pt 11 2183 2192 15126620
  52. [53]Hoekstra D Zegers MM van Ijzendoorn SC Membrane flow, lipid sorting and cell polarity in HepG2 cells: role of a subapical compartment Biochemical Society transactions 1999 27 4 422 428 10917614
  53. [54]Ihrke G Apical plasma membrane proteins and endolyn-78 travel through a subapical compartment in polarized WIF-B hepatocytes The Journal of cell biology 1998 141 1 115 133 9531552 PMC2132730
  54. [55]Wakabayashi Y Kipp H Arias IM Transporters on demand: intracellular reservoirs and cycling of bile canalicular ABC transporters The Journal of biological chemistry 2006 281 38 27669 27673 16737964
  55. [56]Wakabayashi Y Dutt P Lippincott-Schwartz J Arias IM Rab11a and myosin Vb are required for bile canalicular formation in WIF-B9 cells Proceedings of the National Academy of Sciences of the United States of America 2005 102 42 15087 15092 16214890 PMC1257697
  56. [57]Desclozeaux M Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis American journal of physiology. Cell physiology 2008 295 2 C545 556 18579802
  57. [58]Banko MR Chemical Genetic Screen for AMPKalpha2 Substrates Uncovers a Network of Proteins Involved in Mitosis Mol Cell 2011 44 6 878 892 22137581 PMC3246132
  58. [59]Hubbard A Barr V Scott L Arias JB I Chisari F Fausto N Schachter D Schafritz D W-5 Hepatocyte Surface Polarity The Liver Biology and Pathobiology 2001 Lippincott Williams & Wilkins Philadelphia http://liver.med.tufts.ed

Cited by

Sorted by citations

Authors
Müsch, A.
Affiliations
Albert Einstein College of Medicine (US)
Corresponding author
Müsch, Anne
ORCID
Müsch, Anne
Venue
Experimental Cell Research
Publisher
Elsevier BV
Published
2014-11
Volume
328
Issue
2
Pages
276-283
ISSN
0014-4827 (ISSN-L)
DOI
10.1016/j.yexcr.2014.06.006
PMC
PMC4254207
OpenAlex
W1964785566
Cited by
64
References
2
Citations by year
2024: 9 · 2023: 4 · 2022: 6 · 2021: 9 · 2020: 10 · 2019: 4 · 2018: 5 · 2017: 2 · 2016: 8 · 2015: 4 · 2014: 2
FWCI
0.71
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Experimental Cell Research (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
NIH (RO1 DK064842, RO1 CA160790)
Topics
  • Health Sciences › Medicine › Hepatology › Liver physiology and pathology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
Keywords
hepatocyte polarity, bile canaliculi, tight junctions, cell-cell adhesion, apical-basal polarity, epithelial organization, hepatocyte differentiation
MeSH terms
Animals, Epithelium, Humans, Liver, Phenotype, Cell Polarity, Hepatocytes

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review