Pancreatic damage in fetal and newborn cystic fibrosis pigs involves the activation of inflammatory and remodeling pathways

American Journal of Pathology

Volumn 181, Issue 2, 2012, Pages 499-507

  Abu El Haija, Maisam ^a   Ramachandran, Shyam ^a   Meyerholz, David K ^a   Abu El Haija, Marwa ^a   Griffin, Michelle ^a   Giriyappa, Radhamma L ^a   Stoltz, David A ^a   Welsh, Michael J ^a   McCray, Paul B ^a   Uc, Aliye ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; TRANSFORMING GROWTH FACTOR BETA1;

ACINAR CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE COURSE; DISEASE SEVERITY; INFLAMMATION; INFLAMMATORY CELL; NONHUMAN; PANCREAS INJURY; PATHOGENESIS; PRIORITY JOURNAL; SWINE;

EID: 84864150035     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.04.024     Document Type: Article

References (60)

1. M.J. Welsh, B.W. Ramsey, F.J. Accurso, G.R. Cutting Cystic fibrosis C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, The Metabolic and Molecular Bases of Inherited Disease ed 8 2001 McGraw-Hill New York 5121 5188
2. D. Borowitz, P.R. Durie, L.L. Clarke, S.L. Werlin, C.J. Taylor, J. Semler, R.C. De Lisle, P. Lewindon, S.M. Lichtman, M. Sinaasappel, R.D. Baker, S.S. Baker, H.J. Verkade, M.E. Lowe, V.A. Stallings, M. Janghorbani, R. Butler, J. Heubi Gastrointestinal outcomes and confounders in cystic fibrosis J Pediatr Gastroenterol Nutr 41 2005 273 285
3. C.Y. Ooi, R. Dorfman, M. Cipolli, T. Gonska, C. Castellani, K. Keenan, S.D. Freedman, J. Zielenski, Y. Berthiaume, M. Corey, S. Schibli, E. Tullis, P.R. Durie Type of CFTR mutation determines risk of pancreatitis in patients with cystic fibrosis Gastroenterology 140 2011 153 161
4. J.A. Dodge, P.A. Lewis, M. Stanton, J. Wilsher Cystic fibrosis mortality and survival in the UK: 1947-2003 Eur Respir J 29 2007 522 526
5. H. Kopelman, P. Durie, K. Gaskin, Z. Weizman, G. Forstner Pancreatic fluid secretion and protein hyperconcentration in cystic fibrosis N Engl J Med 312 1985 329 334
6. H. Kopelman, G. Forstner, P. Durie, M. Corey Origins of chloride and bicarbonate secretory defects in the cystic fibrosis pancreas, as suggested by pancreatic function studies on control and CF subjects with preserved pancreatic function Clin Invest Med 12 1989 207 211
7. K.J. Gaskin, P.R. Durie, M. Corey, P. Wei, G.G. Forstner Evidence for a primary defect of pancreatic HCO3-secretion in cystic fibrosis Pediatr Res 16 1982 554 557
8. B. Hadorn, G. Zoppi, D.H. Shmerling, A. Prader, I. McIntyre, C.M. Anderson Quantitative assessment of exocrine pancreatic function in infants and children J Pediatr 73 1968 39 50
9. P.G. Johansen, C.M. Anderson, B. Hadorn Cystic fibrosis of the pancreas. a generalised disturbance of water and electrolyte movement in exocrine tissues Lancet 1 1968 455 460
10. D.H. Andersen Cystic fibrosis of the pancreas and its relation to celiac disease: clinical and pathological study Am J Dis Child 56 1938 344 399 -399
11. A. Boue, F. Muller, C. Nezelof, J.F. Oury, F. Duchatel, Y. Dumez, M.C. Aubry, J. Boue Prenatal diagnosis in 200 pregnancies with a 1-in-4 risk of cystic fibrosis Hum Genet 74 1986 288 297
12. J.R. Imrie, D.G. Fagan, J.M. Sturgess Quantitative evaluation of the development of the exocrine pancreas in cystic fibrosis and control infants Am J Pathol 95 1979 697 707
13. E.H. Oppenheimer, J.R. Esterly Cystic fibrosis of the pancreas: morphologic findings in infants with and without diagnostic pancreatic lesions Arch Pathol 96 1973 149 154
14. E.H. Oppenheimer, J.R. Esterly Pathology of cystic fibrosis: review of the literature and comparison with 146 autopsied cases Perspect Pediatr Pathol 2 1975 241 278
15. E.A. Porta, A.A. Stein, P. Patterson Ultrastructural changes of the pancreas and liver in cystic fibrosis Am J Clin Pathol 42 1964 451 465
16. J.M. Sturgess Structural and developmental abnormalities of the exocrine pancreas in cystic fibrosis J Pediatr Gastroenterol Nutr 3 Suppl 1 1984 S55 S66
17. J.A. Tucker, A. Spock, S.S. Spicer, J.D. Shelburne, W. Bradford Inspissation of pancreatic zymogen material in cystic fibrosis Ultrastruct Pathol 27 2003 323 335
18. A. Ornoy, J. Arnon, D. Katznelson, M. Granat, B. Caspi, J. Chemke Pathological confirmation of cystic fibrosis in the fetus following prenatal diagnosis Am J Med Genet 28 1987 935 947
19. M.N. Bronstein, R.J. Sokol, S.H. Abman, B.A. Chatfield, K.B. Hammond, K.M. Hambidge, C.D. Stall, F.J. Accurso Pancreatic insufficiency, growth, and nutrition in infants identified by newborn screening as having cystic fibrosis J Pediatr 120 1992 533 540
20. R.T. Couper, M. Corey, D.J. Moore, L.J. Fisher, G.G. Forstner, P.R. Durie Decline of exocrine pancreatic function in cystic fibrosis patients with pancreatic sufficiency Pediatr Res 32 1992 179 182
21. R.R. Dooley, F. Guilmette, H. Leubner, P.R. Patterson, H. Shwachman, C. Weil Cystic fibrosis of the pancreas with varying degrees of pancreatic insufficiency AMA J Dis Child 92 1956 347 368
22. K. Gaskin, D. Waters, S. Dorney, M. Gruca, M. O'Halloran, B. Wilcken Assessment of pancreatic function in screened infants with cystic fibrosis Pediatr Pulmonol Suppl 7 1991 69 71
23. D.L. Waters, S.F. Dorney, K.J. Gaskin, M.A. Gruca, M. O'Halloran, B. Wilcken Pancreatic function in infants identified as having cystic fibrosis in a neonatal screening program N Engl J Med 322 1990 303 308
24. G.E. Gibbs, W.L. Bostick, P.M. Smith Incomplete pancreatic deficiency in cystic fibrosis of the pancreas J Pediatr 37 1950 320 325
25. K. Gaskin, D. Gurwitz, P. Durie, M. Corey, H. Levison, G. Forstner Improved respiratory prognosis in patients with cystic fibrosis with normal fat absorption J Pediatr 100 1982 857 862
26. R. Kraemer, A. Rudeberg, B. Hadorn, E. Rossi Relative underweight in cystic fibrosis and its prognostic value Acta Paediatr Scand 67 1978 33 37
27. J.N. Snouwaert, K.K. Brigman, A.M. Latour, N.N. Malouf, R.C. Boucher, O. Smithies, B.H. Koller An animal model for cystic fibrosis made by gene targeting Science 257 1992 1083 1088
28. L.L. Clarke, B.R. Grubb, S.E. Gabriel, O. Smithies, B.H. Koller, R.C. Boucher Defective epithelial chloride transport in a gene-targeted mouse model of cystic fibrosis Science 257 1992 1125 1128
29. M.J. DiMagno, S.H. Lee, Y. Hao, S.Y. Zhou, B.J. McKenna, C. Owyang A proinflammatory, antiapoptotic phenotype underlies the susceptibility to acute pancreatitis in cystic fibrosis transmembrane regulator (-/-) mice Gastroenterology 129 2005 665 681
30. S.D. Freedman, H.F. Kern, G.A. Scheele Pancreatic acinar cell dysfunction in CFTR(-/-) mice is associated with impairments in luminal pH and endocytosis Gastroenterology 121 2001 950 957
31. S.D. Freedman, H.F. Kern, G.A. Scheele Cleavage of GPI-anchored proteins from the plasma membrane activates apical endocytosis in pancreatic acinar cells Eur J Cell Biol 75 1998 163 173
32. S.D. Freedman, K. Sakamoto, R.P. Venu GP2, the homologue to the renal cast protein uromodulin, is a major component of intraductal plugs in chronic pancreatitis J Clin Invest 92 1993 83 90
33. S.D. Freedman, K. Sakamoto, G.A. Scheele Nonparallel secretion of GP-2 from exocrine pancreas implies luminal coupling between acinar and duct cells Am J Physiol 267 1994 G40 G51
34. S.D. Freedman, M.H. Katz, E.M. Parker, M. Laposata, M.Y. Urman, J.G. Alvarez A membrane lipid imbalance plays a role in the phenotypic expression of cystic fibrosis in cftr(-/-) mice Proc Natl Acad Sci U S A 96 1999 13995 14000
35. C.S. Rogers, D.A. Stoltz, D.K. Meyerholz, L.S. Ostedgaard, T. Rokhlina, P.J. Taft, M.P. Rogan, A.A. Pezzulo, P.H. Karp, O.A. Itani, A.C. Kabel, C.L. Wohlford-Lenane, G.J. Davis, R.A. Hanfland, T.L. Smith, M. Samuel, D. Wax, C.N. Murphy, A. Rieke, K. Whitworth, A. Uc, T.D. Starner, K.A. Brogden, J. Shilyansky, P.B. McCray Jr, J. Zabner, R.S. Prather, M.J. Welsh Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs Science 321 2008 1837 1841
36. L.S. Ostedgaard, D.K. Meyerholz, J.H. Chen, A.A. Pezzulo, P.H. Karp, T. Rokhlina, S.E. Ernst, R.A. Hanfland, L.R. Reznikov, P.S. Ludwig, M.P. Rogan, G.J. Davis, C.L. Dohrn, C. Wohlford-Lenane, P.J. Taft, M.V. Rector, E. Hornick, B.S. Nassar, M. Samuel, Y. Zhang, S.S. Richter, A. Uc, J. Shilyansky, R.S. Prather, P.B. McCray Jr, J. Zabner, M.J. Welsh, D.A. Stoltz The DeltaF508 mutation causes CFTR misprocessing and cystic fibrosis-like disease in pigs Sci Transl Med 3 2011 74ra24
37. N. Sasaki, K. Yoneda, C. Bigger, J. Brown, Y. Mullen Fetal pancreas transplantation in miniature swine I: Developmental characteristics of fetal pig pancreases Transplantation 38 1984 335 340
38. M. Reich, T. Liefeld, J. Gould, J. Lerner, P. Tamayo, J.P. Mesirov GenePattern 2.0 Nat Genetics 38 2006 500 501
39. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc Natl Acad Sci U S A 102 2005 15545 15550
40. W. Huang da, B.T. Sherman, R.A. Lempicki Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res 37 2009 1 13
41. S. Ramachandran, L.A. Clarke, T.E. Scheetz, M.D. Amaral, P.B. McCray Jr Microarray mRNA expression profiling to study cystic fibrosis Methods Mol Biol 742 2011 193 212
42. D.K. Meyerholz, D.A. Stoltz, E. Namati, S. Ramachandran, A.A. Pezzulo, A.R. Smith, M.V. Rector, M.J. Suter, S. Kao, G. McLennan, G.J. Tearney, J. Zabner, P.B. McCray Jr, M.J. Welsh Loss of cystic fibrosis transmembrane conductance regulator function produces abnormalities in tracheal development in neonatal pigs and young children Am J Respir Crit Care Med 182 2010 1251 1261
43. G.W. Hunninghake, K.C. Doerschug, A.B. Nymon, G.A. Schmidt, D.K. Meyerholz, A. Ashare Insulin-like growth factor-1 levels contribute to the development of bacterial translocation in sepsis Am J Respir Crit Care Med 182 2010 517 525
44. I. Daigle, H.U. Simon Critical role for caspases 3 and 8 in neutrophil but not eosinophil apoptosis Int Arch Allergy Immunol 126 2001 147 156
45. A. Subramanian, H. Kuehn, J. Gould, P. Tamayo, J.P. Mesirov GSEA-P: a desktop application for Gene Set Enrichment Analysis Bioinformatics 23 2007 3251 3253
46. D.K. Meyerholz, D.A. Stoltz, A.A. Pezzulo, M.J. Welsh Pathology of gastrointestinal organs in a porcine model of cystic fibrosis Am J Pathol 176 2010 1377 1389
47. M. Abu-El-Haija, M. Sinkora, D.K. Meyerholz, M.J. Welsh, P.B. McCray Jr, J. Butler, A. Uc An activated immune and inflammatory response targets the pancreas of newborn pigs with cystic fibrosis Pancreatology 11 2011 506 515
48. M. Ashburner, C.A. Ball, J.A. Blake, D. Botstein, H. Butler, J.M. Cherry, A.P. Davis, K. Dolinski, S.S. Dwight, J.T. Eppig, M.A. Harris, D.P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J.C. Matese, J.E. Richardson, M. Ringwald, G.M. Rubin, G. Sherlock Gene ontology: tool for the unification of biology: the Gene Ontology Consortium Nat Genet 25 2000 25 29
49. Z. Fishelson, G. Attali, D. Mevorach Complement and apoptosis Mol Immunol 38 2001 207 219
50. L.L. Mantell, J.A. Kazzaz, J. Xu, T.A. Palaia, B. Piedboeuf, S. Hall, G.C. Rhodes, G. Niu, A.F. Fein, S. Horowitz Unscheduled apoptosis during acute inflammatory lung injury Cell Death Differ 4 1997 600 607
51. R. Seelig, V. Ehemann, C. Tschahargane, H.P. Seelig The serum complement system: a mediator of acute pancreatitis Virchows Arch A Pathol Anat Histol 365 1975 193 199
52. I.M. Goldstein, D. Cala, A. Radin, H.B. Kaplan, J. Horn, J. Ranson Evidence of complement catabolism in acute pancreatitis Am J Med Sci 275 1978 257 264
53. J.K. Horn, J.H. Ranson, I.M. Goldstein, J. Weissler, D. Curatola, R. Taylor, H.D. Perez Evidence of complement catabolism in experimental acute pancreatitis Am J Pathol 101 1980 205 216
54. R. Lev, S.S. Spicer A histochemical comparison of human epithelial mucins in normal and in hypersecretory states including pancreatic cystic fibrosis Am J Pathol 46 1965 23 47
55. J.M. Shackleford, H.P. Bentley Jr Carbohydrate histochemistry of the salivary glands and pancreas in cystic fibrosis J Histochem Cytochem 12 1964 512 521
56. D. Boerma, I.H. Straatsburg, G.J. Offerhaus, D.J. Gouma, T.M. van Gulik Experimental model of obstructive, chronic pancreatitis in pigs Dig Surg 20 2003 520 526
57. N. Hamamoto, N. Ashizawa, M. Niigaki, T. Kaji, T. Katsube, H. Endoh, M. Watanabe, S. Sumi, Y. Kinoshita Morphological changes in the rat exocrine pancreas after pancreatic duct ligation Histol Histopathol 17 2002 1033 1041
58. P. Pitkaranta, L. Kivisaari, S. Nordling, A. Saari, T. Schroder Experimental chronic pancreatitis in the pig Scand J Gastroenterol 24 1989 987 992
59. S. Watanabe, K. Abe, Y. Anbo, H. Katoh Changes in the mouse exocrine pancreas after pancreatic duct ligation: a qualitative and quantitative histological study Arch Histol Cytol 58 1995 365 374
60. D.A. Stoltz, D.K. Meyerholz, A.A. Pezzulo, S. Ramachandran, M.P. Rogan, G.J. Davis, R.A. Hanfland, C. Wohlford-Lenane, C.L. Dohrn, J.A. Bartlett, G.A. Nelson, E.H. Chang, P.J. Taft, P.S. Ludwig, M. Estin, E.E. Hornick, J.L. Launspach, M. Samuel, T. Rokhlina, P.H. Karp, L.S. Ostedgaard, A. Uc, T.D. Starner, A.R. Horswill, K.A. Brogden, R.S. Prather, S.S. Richter, J. Shilyansky, P.B. McCray Jr, J. Zabner, M.J. Welsh Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth Sci Transl Med 2 2010 29ra312