Advertisement

Pancreatic duct-like cell line derived from pig embryonic stem cells: expression of uroplakin genes in pig pancreatic tissue

  • Neil C. TalbotEmail author
  • Amy E. Shannon
  • Wesley M. Garrett
Article
  • 24 Downloads

Abstract

The isolation of a cell line, PICM-31D, with phenotypic characteristics like pancreatic duct cells is described. The PICM-31D cell line was derived from the previously described pig embryonic stem cell-derived exocrine pancreatic cell line, PICM-31. The PICM-31D cell line was morphologically distinct from the parental cells in growing as a monolayer rather than self-assembling into multicellular acinar-like structures. The PICM-31D cells were propagated for over a year at split ratios of 1:3 to 1:10 at each passage without change in phenotype or growth rate. Electron microscopy showed the cells to be a polarized epithelium of cuboidal cells joined by tight junction-like adhesions at their apical/lateral aspect. The cells contained numerous mucus-like secretory vesicles under their apical cell membrane. Proteomic analysis of the PICM-31D’s cellular proteins detected MUC1 and MUC4, consistent with mucus vesicle morphology. Gene expression analysis showed the cells expressed pancreatic ductal cell-related transcription factors such as GATA4, GATA6, HES1, HNF1A, HNF1B, ONECUT1 (HNF6), PDX1, and SOX9, but little or no pancreas progenitor cell markers such as PTF1A, NKX6-1, SOX2, or NGN3. Pancreas ductal cell-associated genes including CA2, CFTR, MUC1, MUC5B, MUC13, SHH, TFF1, KRT8, and KRT19 were expressed by the PICM-31D cells, but the exocrine pancreas marker genes, CPA1 and PLA2G1B, were not expressed by the cells. However, the exocrine marker, AMY2A, was still expressed by the cells. Surprisingly, uroplakin proteins were prominent in the PICM-31D cell proteome, particularly UPK1A. Annexin A1 and A2 proteins were also relatively abundant in the cells. The expression of the uroplakin and annexin genes was detected in the cells, although only UPK1B, UPK3B, ANXA2, and ANXA4 were detected in fetal pig pancreatic duct tissue. In conclusion, the PICM-31D cell line models the mucus-secreting ductal cells of the fetal pig pancreas.

Keywords

Cell line Duct Feeder cells Pancreas Porcine STO 

Notes

Acknowledgments

The authors thank Ms. Caitlin Phillips for her assistance in primer design and for preliminary RT-PCR analysis of the PICM-31D cell line.

Compliance with ethical standards

Care and treatment of pigs in this study were approved by the Institutional Animal Care and Use Committee of the U.S. Department of Agriculture, Beltsville Agricultural Research Center, Beltsville, MD.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11626_2019_336_Fig7_ESM.png (210 kb)
Supplementary Figure 1

Semi-quantitative RT-PCR assay of the expression of pancreas duct cell genes and uroplakin genes in fetal pig pancreas tissue (FP), weanling pig (21-d old) pancreas tissue (WP), fetal pig intestinal tissue (FI), and weanling pig intestinal tissue (WI). Weanling pig intestine mRNA was used for the -RT control. (PNG 210 kb)

11626_2019_336_MOESM1_ESM.tif (2.6 mb)
High resolution image (TIF 2681 kb)
11626_2019_336_MOESM2_ESM.docx (19 kb)
Supplementary Table 1 (DOCX 18 kb)
11626_2019_336_MOESM3_ESM.docx (862 kb)
ESM 1 Supplementary Data Sheet 1 (DOCX 862 kb)

References

  1. Allen A, Hutton DA, Pearson JP (1998) The MUC2 gene product: a human intestinal mucin. Int J Biochem Cell Biol 30:797–801CrossRefGoogle Scholar
  2. Amsterdam A, Raanan C, Schreiber L, Polin N, Givol D (2013) LGR5 and Nanog identify stem cell signature of pancreas beta cells which initiate pancreatic cancer. Biochem Biophys Res Commun 433:157–162CrossRefGoogle Scholar
  3. Andrianifahanana M, Moniaux N, Schmied BM, Ringel J, Friess H, Hollingsworth MA, Büchler MW, Aubert JP, Batra SK (2001) Mucin (MUC) gene expression in human pancreatic adenocarcinoma and chronic pancreatitis: a potential role of MUC4 as a tumor marker of diagnostic significance. Clin Cancer Res 7:4033–4040Google Scholar
  4. Augeron C, Laboisse CL (1984) Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res 44:3961–3969Google Scholar
  5. Bai XF, Ni XG, Zhao P, Liu SM, Wang HX, Guo B, Zhou LP, Liu F, Zhang JS, Wang K, Xie YQ, Shao YF, Zhao XH (2004) Overexpression of annexin 1 in pancreatic cancer and its clinical significance. World J Gastroenterol 10:1466–1470CrossRefGoogle Scholar
  6. Balagué C, Audié JP, Porchet N, Real FX (1995) In situ hybridization shows distinct patterns of mucin gene expression in normal, benign, and malignant pancreas tissues. Gastroenterology. 109:953–964CrossRefGoogle Scholar
  7. Berberat PO, Friess H, Wang L, Zhu Z, Bley T, Frigeri L, Zimmermann A, Büchler MW (2001) Comparative analysis of galectins in primary tumors and tumor metastasis in human pancreatic cancer. J Histochem Cytochem 49:539–549CrossRefGoogle Scholar
  8. Besnard V, Wert SE, Hull WM, Whitsett JA (2004) Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr Patterns 5:193–208CrossRefGoogle Scholar
  9. Buisine MP, Devisme L, Degand P, Dieu MC, Gosselin B, Copin MC, Aubert JP, Porchet N (2000) Developmental mucin gene expression in the gastroduodenal tract and accessory digestive glands. II. Duodenum and liver, gallbladder, and pancreas. J Histochem Cytochem 48:1667–1676CrossRefGoogle Scholar
  10. Cano DA, Soria B, Martín F, Rojas A (2014) Transcriptional control of mammalian pancreas organogenesis. Cell Mol Life Sci 71:2383–2402CrossRefGoogle Scholar
  11. Chaturvedi P, Singh AP, Moniaux N, Senapati S, Chakraborty S, Meza JL, Batra SK (2007) MUC4 mucin potentiates pancreatic tumor cell proliferation survival and invasive properties and interferes with its interaction to extracellular matrix proteins. Mol Cancer Res 5:309–320CrossRefGoogle Scholar
  12. Cheng JY, Whitelock J, Poole-Warren L (2012) Syndecan-4 is associated with beta-cells in the pancreas and the MIN6 beta-cell line. Histochem Cell Biol 138:933–944CrossRefGoogle Scholar
  13. Choi JH, Lee MY, Kim Y, Shim JY, Han SM, Lee KA, Choi YK, Jeon HM, Baek KH (2010) Isolation of genes involved in pancreas regeneration by subtractive hybridization. Biol Chem 391:1019–1029CrossRefGoogle Scholar
  14. Christophe J (1994) Pancreatic tumoral cell line AR42J: an amphicrine model. Am J Phys 266:G963–G971Google Scholar
  15. Conejo JR, Kleeff J, Koliopanos A, Matsuda K, Zhu ZW, Goecke H, Bicheng N, Zimmermann A, Korc M, Friess H, Büchler MW (2000) Syndecan-1 expression is up-regulated in pancreatic but not in other gastrointestinal cancers. Int J Cancer 88:12–20CrossRefGoogle Scholar
  16. Deer EL, González-Hernández J, Coursen JD, Shea JE, Ngatia J, Scaife CL, Firpo MA, Mulvihill SJ (2010) Phenotype and genotype of pancreatic cancer cell lines. Pancreas. 39:425–435CrossRefGoogle Scholar
  17. Egerbacher M, Böck P (1997) Morphology of the pancreatic duct system in mammals. Microsc Res Tech 37:407–417CrossRefGoogle Scholar
  18. Foulon T, Cadel S, Chesneau V, Draoui M, Prat A, Cohen P (1996) Two novel metallopeptidases with a specificity for basic residues: functional properties, structure and cellular distribution. Ann N Y Acad Sci 780:106–120CrossRefGoogle Scholar
  19. Furukawa T, Duguid WP, Rosenberg L, Viallet J, Galloway DA, Tsao MS (1996) Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am J Pathol 148:1763–1770Google Scholar
  20. Gaisano HY, Ghai M, Malkus PN, Sheu L, Bouquillon A, Bennett MK, Trimble WS (1996) Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells. Mol Biol Cell 7:2019–2027CrossRefGoogle Scholar
  21. Gautam SK, Kumar S, Cannon A, Hall B, Bhatia R, Nasser MW, Mahapatra S, Batra SK, Jain M (2017) MUC4 mucin—a therapeutic target for pancreatic ductal adenocarcinoma. Expert Opin Ther Targets 21:657–669CrossRefGoogle Scholar
  22. Githens S (1988) The pancreatic duct cell: proliferative capabilities, specific characteristics, metaplasia, isolation, and culture. Pediatr Gastroenterol Nutr 7:486–506CrossRefGoogle Scholar
  23. Githens S, Schexnayder JA, Frazier ML (1992) Carbonic anhydrase II gene expression in mouse pancreatic duct cells. Pancreas. 7:556–561Google Scholar
  24. Githens S, Schexnayder JA, Moses RL, Denning GM, Smith JJ, Frazier ML (1994) Mouse pancreatic acinar/ductular tissue gives rise to epithelial cultures that are morphologically, biochemically, and functionally indistinguishable from interlobular duct cell cultures. In Vitro Cell Dev Biol Anim 30A:622–635Google Scholar
  25. Githens S 3rd, Holmquist DR, Whelan JF, Ruby JR (1981) Morphologic and biochemical characteristics of isolated and cultured pancreatic ducts. Cancer. 47:1505–1512Google Scholar
  26. Gittes GK (2009) Developmental biology of the pancreas: a comprehensive review. Dev Biol 326:4–35CrossRefGoogle Scholar
  27. Gomez DL, O’Driscoll M, Sheets TP, Hruban RH, Oberholzer J, McGarrigle JJ, Shamblott MJ (2015) Neurogenin 3 expressing cells in the human exocrine pancreas have the capacity for endocrine cell fate. PLoS One 10(8):e0133862.  https://doi.org/10.1371/journal.pone.0133862 CrossRefGoogle Scholar
  28. Grapin-Botton A (2005) Ductal cells of the pancreas. Int J Biochem Cell Biol 37:504–510CrossRefGoogle Scholar
  29. Grønborg M, Kristiansen TZ, Iwahori A, Chang R, Reddy R, Sato N, Molina H, Jensen ON, Hruban RH, Goggins MG, Maitra A, Pandey A (2006) Biomarker discovery from pancreatic cancer secretome using a differential proteomic approach. Mol Cell Proteomics 5:157–171CrossRefGoogle Scholar
  30. Gu G, Dubauskaite J, Melton DA (2002) Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129:2447–2457Google Scholar
  31. Harris A, Coleman L (1987) Establishment of a tissue culture system for epithelial cells derived from human pancreas: a model for the study of cystic fibrosis. J Cell Sci 87:695–703Google Scholar
  32. Hausmann DH, Porstmann T, Weber I, Hausmann S, Dummler W, Liebe S, Emmrich J (1997) Cu/Zn-SOD in human pancreatic tissue and pancreatic juice. Int J Pancreatol 22:207–213Google Scholar
  33. He L, Diedrich J, Chu YY, Yates JR 3rd (2015a) Extracting accurate precursor information for tandem mass spectra by RawConverter. Anal Chem 87:11361–11367CrossRefGoogle Scholar
  34. He P, Jiang S, Ma M, Wang Y, Li R, Fang F, Tian G, Zhang Z (2015b) Trophoblast glycoprotein promotes pancreatic ductal adenocarcinoma cell metastasis through Wnt/planar cell polarity signaling. Mol Med Rep 12:503–509CrossRefGoogle Scholar
  35. Hebrok M, Kim SK, St Jacques B, McMahon AP, Melton DA (2000) Regulation of pancreas development by hedgehog signaling. Development 127:4905–4913Google Scholar
  36. Heller RS, Dichmann DS, Jensen J, Miller C, Wong G, Madsen OD, Serup P (2002) Expression patterns of Wnts, Frizzleds, sFRPs, and misexpression in transgenic mice suggesting a role for Wnts in pancreas and foregut pattern formation. Dev Dyn 225:260–270CrossRefGoogle Scholar
  37. Iio T, Tamaoki T (1976) Intracellular distribution of alpha-fetoprotein and albumin messenger RNAs in developing mouse liver. Can J Biochem 54:408–412CrossRefGoogle Scholar
  38. Jensen J (2004) Gene regulatory factors in pancreatic development. Dev Dyn 229:176–200CrossRefGoogle Scholar
  39. Jiang FX, Naselli G, Harrison LC (2002) Distinct distribution of laminin and its integrin receptors in the pancreas. J Histochem Cytochem 50:1625–1632CrossRefGoogle Scholar
  40. Jones EA, Clement-Jones M, James OF, Wilson DI (2001) Differences between human and mouse alpha-fetoprotein expression during early development. J Anat 198:555–559CrossRefGoogle Scholar
  41. Karanjawala ZE, Illei PB, Ashfaq R, Infante JR, Murphy K, Pandey A, Schulick R, Winter J, Sharma R, Maitra A, Goggins M, Hruban RH (2008) New markers of pancreatic cancer identified through differential gene expression analyses: claudin 18 and annexin A8. Am J Surg Pathol 32:188–196CrossRefGoogle Scholar
  42. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV (2002) The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 32:128–134CrossRefGoogle Scholar
  43. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identificationsm made by MS/MS and database search. Anal Chem 74:5383–5392CrossRefGoogle Scholar
  44. Khushman M, Bhardwaj A, Patel GK, Laurini JA, Roveda K, Tan MC, Patton MC, Singh S, Taylor W, Singh AP (2017) Exosomal markers (CD63 and CD9) expression pattern using immunohistochemistry in resected malignant and nonmalignant pancreatic specimens. Pancreas. 46:782–788CrossRefGoogle Scholar
  45. Kim BM, Han YM, Shin YJ, Min BH, Park IS (2001) Clusterin expression during regeneration of pancreatic islet cells in streptozotocin-induced diabetic rats. Diabetologia. 44:2192–2202CrossRefGoogle Scholar
  46. Kobayashi E, Hishikawa S, Teratani T, Lefor AT (2012) The pig as a model for translational research: overview of porcine animal models at Jichi Medical University. Transplant Res 1:8CrossRefGoogle Scholar
  47. Kolar C, Caffrey T, Hollingsworth M, Scheetz M, Sutherlin M, Weide L, Lawson T (1997) Duct epithelial cells cultured from human pancreas processed for transplantation retain differentiated ductal characteristics. Pancreas. 15:265–271CrossRefGoogle Scholar
  48. Kopinke D, Brailsford M, Shea JE, Leavitt R, Scaife CL, Murtaugh LC (2011) Lineage tracing reveals the dynamic contribution of Hes1+ cells to the developing and adult pancreas. Development 138:431–441Google Scholar
  49. Kopinke D, Murtaugh LC (2010) Exocrine-to-endocrine differentiation is detectable only prior to birth in the uninjured mouse pancreas. BMC Dev Biol 10:38Google Scholar
  50. Kuo KK, Kuo CJ, Chiu CY, Liang SS, Huang CH, Chi SW, Tsai KB, Chen CY, Hsi E, Cheng KH, Chiou SH (2016) Quantitative proteomic analysis of differentially expressed protein profiles involved in pancreatic ductal adenocarcinoma. Pancreas 45:71–83Google Scholar
  51. Kuo WL, Montag AG, Rosner MR (1993) Insulin-degrading enzyme is differentially expressed and developmentally regulated in various rat tissues. Endocrinology 132:604–611Google Scholar
  52. Larsen HL, Grapin-Botton A (2017) The molecular and morphogenetic basis of pancreas organogenesis. Semin Cell Dev Biol 66:51–68CrossRefGoogle Scholar
  53. Lee G (2011) Uroplakins in the lower urinary tract. Int Neurourol J 15:4–12CrossRefGoogle Scholar
  54. Lee KM, Nguyen C, Ulrich AB, Pour PM, Ouellette MM (2003) Immortalization with telomerase of the Nestin-positive cells of the human pancreas. Biochem Biophys Res Commun 301:1038–1044CrossRefGoogle Scholar
  55. Lee S, Hong SW, Min BH, Shim YJ, Lee KU, Lee IK, Bendayan M, Aronow BJ, Park IS (2011) Essential role of clusterin in pancreas regeneration. Dev Dyn 240:605–615CrossRefGoogle Scholar
  56. Lesuffleur T, Barbat A, Dussaulx E, Zweibaum A (1990) Growth adaptation to methotrexate of HT-29 human colon carcinoma cells is associated with their ability to differentiate into columnar absorptive and mucus-secreting cells. Cancer Res 50:6334–6343Google Scholar
  57. Li WC, Rukstalis JM, Nishimura W, Tchipashvili V, Habener JF, Sharma A, Bonner-Weir S (2010) Activation of pancreatic-duct-derived progenitor cells during pancreas regeneration in adult rats. J Cell Sci 123:2792–2802CrossRefGoogle Scholar
  58. Liu N, Furukawa T, Kobari M, Tsao MS (1998) Comparative phenotypic studies of duct epithelial cell lines derived from normal human pancreas and pancreatic carcinoma. Am J Pathol 153:263–269CrossRefGoogle Scholar
  59. Lowe AW, Olsen M, Hao Y, Lee SP, Taek Lee K, Chen X, van de Rijn M, Brown PO (2007) Gene expression patterns in pancreatic tumors, cells and tissues. PLoS One 2(3):e323CrossRefGoogle Scholar
  60. Lukinius A, Stridsberg M, Wilander E (2003) Cellular expression and specific intragranular localization of chromogranin A, chromogranin B, and synaptophysin during ontogeny of pancreatic islet cells: an ultrastructural study. Pancreas 27:38–46CrossRefGoogle Scholar
  61. Lundgren DH, Hwang SI, Wu L, Han DK (2010) Role of spectral counting in quantitative proteomics. Expert Rev Proteomics 7:39–53CrossRefGoogle Scholar
  62. Madden ME, Sarras MP Jr (1988) Morphological and biochemical characterization of a human pancreatic ductal cell line (PANC-1). Pancreas 3:512–528CrossRefGoogle Scholar
  63. Marino LR, Cotton CU (1996) Immortalization of bovine pancreatic duct epithelial cells. Am J Phys 270:G676–G683Google Scholar
  64. Marshall BA, Tordjman K, Host HH, Ensor NJ, Kwon G, Marshall CA, Coleman T, McDaniel ML, Semenkovich CF (1999) Relative hypoglycemia and hyperinsulinemia in mice with heterozygous lipoprotein lipase (LPL) deficiency. Islet LPL regulates insulin secretion. J Biol Chem 274:27426–27432CrossRefGoogle Scholar
  65. Maurer M, Müller AC, Parapatics K, Pickl WF, Wagner C, Rudashevskaya EL, Breitwieser FP, Colinge J, Garg K, Griss J, Bennett KL, Wagner SN (2014) Comprehensive comparative and semiquantitative proteome of a very low number of native and matched Epstein-Barr-virus-transformed B lymphocytes infiltrating human melanoma. J Proteome Res 13:2830–2845CrossRefGoogle Scholar
  66. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646–4658CrossRefGoogle Scholar
  67. Nishide T, Emi M, Nakamura Y, Matsubara K (1984) Corrected sequences of cDNAs for human salivary and pancreatic alpha-amylases [corrected]. Gene. 28:263–270CrossRefGoogle Scholar
  68. Nishii Y, Yamaguchi M, Kimura Y, Hasegawa T, Aburatani H, Uchida H, Hirata K, Sakuma Y (2015) A newly developed anti-mucin 13 monoclonal antibody targets pancreatic ductal adenocarcinoma cells. Int J Oncol 46:1781–1787CrossRefGoogle Scholar
  69. Oda D, Savard CE, Nguyen TD, Eng L, Swenson ER, Lee SP (1996) Dog pancreatic duct epithelial cells: long-term culture and characterization. Am J Pathol 148:977–985Google Scholar
  70. Ohta T, Terada T, Nagakawa T, Itoh H, Tajima H, Miyazaki I (1994) Presence of pancreatic alpha-amylase, trypsinogen, and lipase immunoreactivity in normal human pancreatic ducts. Pancreas 9:382–386CrossRefGoogle Scholar
  71. Ouyang H, Mou LJ, Luk C, Liu N, Karaskova J, Squire J, Tsao MS (2000) Immortal human pancreatic duct epithelial cell lines with near normal genotype and phenotype. Am J Pathol 157:1623–1631CrossRefGoogle Scholar
  72. Pacifici F, Arriga R, Sorice GP, Capuani B, Scioli MG, Pastore D, Donadel G, Bellia A, Caratelli S, Coppola A, Ferrelli F, Federici M, Sconocchia G, Tesauro M, Sbraccia P, Della-Morte D, Giaccari A, Orlandi A, Lauro D (2014) Peroxiredoxin 6, a novel player in the pathogenesis of diabetes. Diabetes. 63:3210–3220CrossRefGoogle Scholar
  73. Pallagi P, Hegyi P, Rakonczay Z Jr (2015) The physiology and pathophysiology of pancreatic ductal secretion: the background for clinicians. Pancreas. 44:1211–1233CrossRefGoogle Scholar
  74. Rausa F, Samadani U, Ye H, Lim L, Fletcher CF, Jenkins NA, Copeland NG, Costa RH (1997) The cut-homeodomain transcriptional activator HNF-6 is coexpressed with its target gene HNF-3 beta in the developing murine liver and pancreas. Dev Biol 192:228–246CrossRefGoogle Scholar
  75. Reichert M, Rustgi AK (2011) Pancreatic ductal cells in development, regeneration, and neoplasia. J Clin Invest 121:4572–4578CrossRefGoogle Scholar
  76. Rezanejad H, Ouziel-Yahalom L, Keyzer CA, Sullivan BA, Hollister-Lock J, Li WC, Guo L, Deng S, Lei J, Markmann J, Bonner-Weir S (2018) Heterogeneity of SOX9 and HNF1β in pancreatic ducts is dynamic. Stem Cell Rep 10:725–738CrossRefGoogle Scholar
  77. Schaffer AE, Taylor BL, Benthuysen JR, Liu J, Thorel F, Yuan W, Jiao Y, Kaestner KH, Herrera PL, Magnuson MA, May CL, Sander M (2013) Nkx6.1 controls a gene regulatory network required for establishing and maintaining pancreatic beta cell identity. PLoS Genet 9:e1003274.  https://doi.org/10.1371/journal.pgen.1003274 CrossRefGoogle Scholar
  78. Seyama K, Nukiwa T, Takahashi K, Takahashi H, Kira S (1994) Amylase mRNA transcripts in normal tissues and neoplasms: the implication of different expressions of amylase isogenes. J Cancer Res Clin Oncol 120:213–220CrossRefGoogle Scholar
  79. Seymour PA (2014) Sox9: a master regulator of the pancreatic program. Rev Diabet Stud 11:51–83CrossRefGoogle Scholar
  80. Shen J, Person MD, Zhu J, Abbruzzese JL, Li D (2004) Protein expression profiles in pancreatic adenocarcinoma compared with normal pancreatic tissue and tissue affected by pancreatitis as detected by two-dimensional gel electrophoresis and mass spectrometry. Cancer Res 64:9018–9026CrossRefGoogle Scholar
  81. Storr SJ, Zaitoun AM, Arora A, Durrant LG, Lobo DN, Madhusudan S, Martin SG (2012) Calpain system protein expression in carcinomas of the pancreas, bile duct and ampulla. BMC Cancer 12:511CrossRefGoogle Scholar
  82. Strobel O, Rosow DE, Rakhlin EY, Lauwers GY, Trainor AG, Alsina J, Fernández-Del Castillo C, Warshaw AL, Thayer SP (2010) Pancreatic duct glands are distinct ductal compartments that react to chronic injury and mediate Shh-induced metaplasia. Gastroenterology 138:1166–1177CrossRefGoogle Scholar
  83. Su Y, Jono H, Misumi Y, Senokuchi T, Guo J, Ueda M, Shinriki S, Tasaki M, Shono M, Obayashi K, Yamagata K, Araki E, Ando Y (2012) Novel function of transthyretin in pancreatic alpha cells. FEBS Lett 586:4215–4222CrossRefGoogle Scholar
  84. Sun TT (2006) Altered phenotype of cultured urothelial and other stratified epithelial cells: implications for wound healing. Am J Physiol Renal Physiol 291:F9–F21CrossRefGoogle Scholar
  85. Talbot NC, Caperna TJ (1998) Selective and organotypic culture of intrahepatic bile duct cells from adult pig liver. In Vitro Cell Dev Biol Anim 34A:785–798CrossRefGoogle Scholar
  86. Talbot NC, Paape MJ (1996) Continuous culture of pig tissue-derived macrophages. Methods Cell Sci 18:315–327CrossRefGoogle Scholar
  87. Talbot NC, Shannon AE, Phillips CE, Garrett WM (2017) Derivation and characterization of a pig embryonic-stem-cell-derived exocrine pancreatic cell line. Pancreas 46:789–800CrossRefGoogle Scholar
  88. Talbot NC, Shannon AE, Phillips CE, Garrett WM (2018) Feeder-cell-independent culture of the pig embryonic stem cell-derived exocrine pancreatic cell line, PICM-31. In Vitro Cell Dev Biol Anim 54:321–330CrossRefGoogle Scholar
  89. Tezel E, Nagasaka T, Tezel G, Kaneko T, Takasawa S, Okamoto H, Nakao A (2004) REG I as a marker for human pancreatic acinoductular cells. Hepatogastroenterology 51:91–96Google Scholar
  90. Tooze J, Hollinshead M, Hensel G, Kern HF, Hoflack B (1991) Regulated secretion of mature cathepsin B from rat exocrine pancreatic cells. Eur J Cell Biol 56:187–200Google Scholar
  91. Truty MJ, Smoot RL (2008) Animal models in pancreatic surgery: a plea for pork. Pancreatology 8:546–550CrossRefGoogle Scholar
  92. Tsao MS, Duguid WP (1987) Establishment of propagable epithelial cell lines from normal adult rat pancreas. Exp Cell Res 168:365–375CrossRefGoogle Scholar
  93. Tsutsumi K, Sato N, Tanabe R, Mizumoto K, Morimatsu K, Kayashima T, Fujita H, Ohuchida K, Ohtsuka T, Takahata S, Nakamura M, Tanaka M (2012) Claudin-4 expression predicts survival in pancreatic ductal adenocarcinoma. Ann Surg Oncol 19(Suppl 3):S491–S499CrossRefGoogle Scholar
  94. Vinter-Jensen L, Juhl CO, Teglbjaerg PS, Poulsen SS, Dajani EZ, Nexø E (1997) Systemic treatment with epidermal growth factor in pigs induces ductal proliferations in the pancreas. Gastroenterology 113:1367–1374CrossRefGoogle Scholar
  95. Vishwanatha JK, Chiang Y, Kumble KD, Hollingsworth MA, Pour PM (1993) Enhanced expression of annexin II in human pancreatic carcinoma cells and primary pancreatic cancers. Carcinogenesis 14:2575–2579CrossRefGoogle Scholar
  96. Wada R, Ogawa K, Yamaguchi T, Tanizaki T, Matsumoto M (2005) Intercalated duct cell is starting point in development of pancreatic ductal carcinoma? J Carcinog 4:9CrossRefGoogle Scholar
  97. Wang Y, Lanzoni G, Carpino G, Cui CB, Dominguez-Bendala J, Wauthier E, Cardinale V, Oikawa T, Pileggi A, Gerber D, Furth ME, Alvaro D, Gaudio E, Inverardi L, Reid LM (2013) Biliary tree stem cells, precursors to pancreatic committed progenitors: evidence for possible life-long pancreatic organogenesis. Stem Cells 31:1966–1979CrossRefGoogle Scholar
  98. Wang YJ, Park JT, Parsons MJ, Leach SD (2015) Fate mapping of ptf1a-expressing cells during pancreatic organogenesis and regeneration in zebrafish. Dev Dyn 244:724–735CrossRefGoogle Scholar
  99. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, Wataya T, Takahashi JB, Nishikawa S, Nishikawa S, Muguruma K, Sasai Y (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25:681–686CrossRefGoogle Scholar
  100. Westmoreland JJ, Wang Q, Bouzaffour M, Baker SJ, Sosa-Pineda B (2009) Pdk1 activity controls proliferation, survival, and growth of developing pancreatic cells. Dev Biol 334:285–298CrossRefGoogle Scholar
  101. Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359–362CrossRefGoogle Scholar
  102. Xuan S, Borok MJ, Decker KJ, Battle MA, Duncan SA, Hale MA, Macdonald RJ, Sussel L (2012) Pancreas-specific deletion of mouse Gata4 and Gata6 causes pancreatic agenesis. J Clin Invest 122:3516–3528CrossRefGoogle Scholar
  103. Yamaguchi J, Liss AS, Sontheimer A, Mino-Kenudson M, Castillo CF, Warshaw AL, Thayer SP (2015) Pancreatic duct glands (PDGs) are a progenitor compartment responsible for pancreatic ductal epithelial repair. Stem Cell Res 15:190–202Google Scholar
  104. Yamaguchi N, Yamamura Y, Koyama K, Ohtsuji E, Imanishi J, Ashihara T (1990) Characterization of new human pancreatic cancer cell lines which propagate in a protein-free chemically defined medium. Cancer Res 50:7008–7014Google Scholar
  105. Yonezawa S, Sueyoshi K, Nomoto M, Kitamura H, Nagata K, Arimura Y, Tanaka S, Hollingsworth MA, Siddiki B, Kim YS, Sato E (1997) MUC2 gene expression is found in noninvasive tumors but not in invasive tumors of the pancreas and liver: its close relationship with prognosis of the patients. Hum Pathol 28:344–352CrossRefGoogle Scholar
  106. Yu JX, Chao L, Chao J (1994) Prostasin is a novel human serine proteinase from seminal fluid. Purification, tissue distribution, and localization in prostate gland. J Biol Chem 269:18843–18848Google Scholar
  107. Zhou Q, Law AC, Rajagopal J, Anderson WJ, Gray PA, Melton DA (2007) A multipotent progenitor domain guides pancreatic organogenesis. Dev Cell 13:103–114CrossRefGoogle Scholar
  108. Zhu GH, Huang C, Qiu ZJ, Liu J, Zhang ZH, Zhao N, Feng ZZ, Lv XH (2011) Expression and prognostic significance of CD151, c-Met, and integrin alpha3/alpha6 in pancreatic ductal adenocarcinoma. Dig Dis Sci 56:1090–1098Google Scholar
  109. Zhu Y, Xu G, Patel A, McLaughlin MM, Silverman C, Knecht K, Sweitzer S, Li X, McDonnell P, Mirabile R, Zimmerman D, Boyce R, Tierney LA, Hu E, Livi GP, Wolf B, Abdel-Meguid SS, Rose GD, Aurora R, Hensley P, Briggs M, Young PR (2002) Cloning, expression, and initial characterization of a novel cytokine-like gene family. Genomics. 80:144–150Google Scholar

Copyright information

© The Society for In Vitro Biology 2019

Authors and Affiliations

  1. 1.Agricultural Research Service, NEA, Beltsville Agricultural Research Center, Animal Biosciences and Biotechnology LaboratoryU.S. Department of AgricultureBeltsvilleUSA

Personalised recommendations