Tissue and cellular expression patterns of porcine CFTR: Similarities to and differences from human CFTR

Journal of Histochemistry and Cytochemistry

Volumn 58, Issue 9, 2010, Pages 785-797

  Plog, Stephanie ^a   Mundhenk, Lars ^a   Bothe, Melanie K ^a   Klymiuk, Nikolai ^b   Gruber, Achim D ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Animal model; CFTR; Cystic fibrosis; Expression pattern; Pig

Indexed keywords

TRANSMEMBRANE CONDUCTANCE REGULATOR; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; CELL LYSATE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOSOL; EMBRYO; EPITHELIUM CELL; EXPERIMENTAL MODEL; FROZEN SECTION; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; IMMUNOHISTOCHEMISTRY; INTESTINE CELL; INTESTINE CRYPT; LASER CAPTURE MICRODISSECTION; MALE; MEMBRANE CONDUCTANCE; NONHUMAN; PHENOTYPE; PORCINE CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SPECIES DIFFERENCE; SWINE; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGY; BIOSYNTHESIS; CELL LINE; COMPARATIVE STUDY; FEMALE; GENETICS;

ANIMALIA; SUIDAE; SUS;

ANIMALS; CELL LINE; COMPUTATIONAL BIOLOGY; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FEMALE; HUMANS; MALE; ORGAN SPECIFICITY; RNA, MESSENGER; SPECIES SPECIFICITY; SWINE;

EID: 77956215889     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/jhc.2010.955377     Document Type: Article

References (69)

1. Ameen NA, Martensson B, Bourguinon L, Marino C, Isenberg J, McLaughlin GE (1999) CFTR channel insertion to the apical surface in rat duodenal villus epithelial cells is upregulated by VIP in vivo. J Cell Sci 112(Pt 6):887-894
2. Ameen NA, van Donselaar E, Posthuma G, de Jonge H, McLaughlin G, Geuze HJ, Marino C, et al. (2000) Subcellular distribution of CFTR in rat intestine supports a physiologic role for CFTR regulation by vesicle traffic. Histochem Cell Biol 114:219-228
3. Anton F, Leverkoehne I, Mundhenk L, Thoreson WB, Gruber AD (2005) Overexpression of eCLCA1 in small airways of horses with recurrent airway obstruction. J Histochem Cytochem 53:1011-1021
4. Blackledge NP, Carter EJ, Evans JR, Lawson V, Rowntree RK, Harris A (2007) CTCF mediates insulator function at the CFTR locus. Biochem J 408:267-275
5. Bradbury NA (1999) Intracellular CFTR: localization and function. Physiol Rev 79:S175-191
6. Brezillon S, Dupuit F, Hinnrasky J, Marchand V, Kälin N, Tümmler B, Puchelle E (1995) Decreased expression of the CFTR protein in remodeled human nasal epithelium from non-cystic fibrosis patients. Lab Invest 72:191-200
7. Chow YH, Plumb J, Wen Y, Steer BM, Lu Z, Buchwald M, Hu J (2000) Targeting transgene expression to airway epithelia and submucosal glands, prominent sites of human CFTR expression. Mol Ther 2:359-367
8. Claass A, Sommer M, de Jonge H, Kälin N, Tümmler B (2000) Applicability of different antibodies for immunohistochemical localization of CFTR in sweat glands from healthy controls and from patients with cystic fibrosis. J Histochem Cytochem 48:831-837
9. Clunes MT, Boucher RC (2007) Cystic fibrosis: the mechanisms of pathogenesis of an inherited lung disorder. Drug Discov Today Dis Mech 4:63-72
10. Cooper DK, Ezzelarab M, Hara H, Ayares D (2008) Recent advances in pig-to-human organ and cell transplantation. Expert Opin Biol Ther 8:1-4
11. Crawford I, Maloney PC, Zeitlin PL, Guggino WB, Hyde SC, Turley H, Gatter KC, et al. (1991) Immunocytochemical localization of the cystic fibrosis gene product CFTR. Proc Natl Acad Sci USA 88:9262-9266
12. Davidson DJ, Rolfe M (2001) Mouse models of cystic fibrosis. Trends Genet 17:S29-37
13. Denning GM, Ostedgaard LS, Cheng SH, Smith AE, Welsh MJ (1992) Localization of cystic fibrosis transmembrane conductance regulator in chloride secretory epithelia. J Clin Invest 89:339-349
14. Devuyst O, Guggino WB (2002) Chloride channels in the kidney: lessons learned from knockout animals. J Am Soc Nephrol 18:707-718
15. di Sant'Agnese PA, Darling RC, Perera GA, Shea E (1953) Abnormal electrolyte composition of sweat in cystic fibrosis of the pancreas. Pediatrics 12:549-563
16. Doucet L, Mendes F, Montier T, Delepine P, Penque D, Ferec C, Amaral MD (2003) Applicability of different antibodies for the immunohistochemical localization of CFTR in respiratory and intestinal tissues of human and murine origin. J Histochem Cytochem 51:1191-1199
17. Dray-Charier N, Paul A, Veissiere D, Mergey M, Scoazec JY, Capeau J, Brahimi-Horn C, et al. (1995) Expression of cystic fibrosis transmembrane conductance regulator in human gallbladder epithelial cells. Lab Invest 73:828-836
18. Dupuit F, Kälin N, Brézillon S, Hinnrasky J, Tümmler B, Puchelle E (1995) CFTR and differentiation markers expression in non-CF and delta F 508 homozygous CF nasal epithelium. J Clin Invest 96:1601-1611
19. Elferink RO, Beuers U (2009) Are pigs more human than mice? J Hepatol 50:838-841
20. Engelhardt JF, Yankaskas JR, Ernst SA, Yang Y, Marino CR, Boucher RC, Cohn JA, et al. (1992) Submucosal glands are the predominant site of CFTR expression in the human bronchus. Nat Genet 2:240-248
21. Engelhardt JF, Zepeda M, Cohn JA, Yankaskas JR, Wilson JM (1994) Expression of the cystic fibrosis gene in adult human lung. J Clin Invest 93:737-749
22. Farinha CM, Penque D, Roxo-Rosa M, Lukacs G, Dormer R, McPherson M, Pereira M, et al. (2004) Biochemical methods to assess CFTR expression and membrane localization. J Cyst Fibros 3(suppl 2):73-77
23. Fordtran JS, Locklear TW (1966) Ionic constituents and osmolality of gastric and small-intestinal fluids after eating. Am J Dig Dis 11:503-521
24. Guggino WB, Stanton BA (2006) New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat Rev Mol Cell Biol 7:426-436
25. Guilbault C, Saeed Z, Downey GP, Radzioch D (2007) Cystic fibrosis mouse models. Am J Respir Cell Mol Biol 36:1-7
26. Gruber AD, Levine RA (1997) In situ assessment of mRNA accessibility in heterogeneous tissue samples using elongation factor-1 alpha (EF-1 alpha). Histochem Cell Biol 107:411-416
27. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98
28. Hamilton DL, Roe WE (1977) Electrolyte levels and net fluid and electrolyte movements in the gastrointestinal tract of weanling swine. Can J Comp Med 41:241-250
29. Hayden UL, Carey HV (1996) Cellular localization of cystic fibrosis transmembrane regulator protein in piglet and mouse intestine. Cell Tissue Res 283:209-213
30. Hihnala S, Kujala M, Toppari J, Kere J, Holmberg C, Hoglund P (2006) Expression of SLC26A3, CFTR and NHE3 in the human male reproductive tract: role in male subfertility caused by congenital chloride diarrhoea. Mol Hum Reprod 12:107-111
31. Horowitz B, Tsung SS, Hart P, Levesque PC, Hume JR (1993) Alternative splicing of CFTR Cl- channels in heart. Am J Physiol 264:H2214-2220
32. Jacquot J, Puchelle E, Hinnrasky J, Fuchey C, Bettinger C, Spilmont C, Bonnet N, et al. (1993) Localization of the cystic fibrosis transmembrane conductance regulator in airway secretory glands. Eur Respir J 6:169-176
33. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403-405
34. Johannesson M, Bogdanovic N, Nordqvist AC, Hjelte L, Schalling M (1997) Cystic fibrosis mRNA expression in rat brain: cerebral cortex and medial preoptic area. Neuroreport 8:535-539
35. Jouret F, Bernard A, Hermans C, Dom G, Terryn S, Leal T, Lebecque P, et al. (2006) Cystic fibrosis is associated with a defect in apical receptor-mediated endocytosis in mouse and human kidney. J Am Soc Nephrol 18:707-718
36. Kälin N, Claass A, Sommer M, Puchelle E, Tümmler B (1999) DeltaF508 CFTR protein expression in tissues from patients with cystic fibrosis. J Clin Invest 103:1379-1389
37. Kartner N, Augustinas O, Jensen TJ, Naismith AL, Riordan JR (1992) Mislocalization of delta F508 CFTR in cystic fibrosis sweat gland. Nat Genet 1:321-327
38. Klymiuk N, Müller M, Brem G, Aigner B (2006) Phylogeny, recombination and expression of porcine endogenous retrovirus gamma2 nucleotide sequences. J Gen Virol 87(Pt 4):977-986
39. Kreda SM, Mall M, Mengos A, Rochelle L, Yankaskas J, Riordan JR, Boucher RC (2005) Characterization of wild-type and deltaF508 cystic fibrosis transmembrane regulator in human respiratory epithelia. Mol Biol Cell 16:2154-2167
40. Lader AS, Wang Y, Jackson GR Jr, Borkan SC, Cantiello HF (2000) cAMP-activated anion conductance is associated with expression of CFTR in neonatal mouse cardiac myocytes. Am J Physiol Cell Physiol 278:C436-450
41. 2+-stimulated fluid secretion by porcine bronchial submucosal gland serous acinar cells. Am J Physiol Lung Cell Mol Physiol 298:L210-231
42. Leonhard-Marek S, Hempe J, Schroeder B, Breves G (2009) Electrophysiological characterization of chloride secretion across the jejunum and colon of pigs as affected by age and weaning. J Comp Physiol B 179:883-896
43. Leverkoehne I, Gruber AD (2002) The murine mCLCA3 (alias gob-5) protein is located in the mucin granule membranes of intestinal, respiratory and uterine goblet cells. J Histochem Cytochem 50:829-838
44. Levesque PC, Hart PJ, Hume JR, Kenyon JL, Horowitz B (1992) Expression of cystic fibrosis transmembrane regulator Cl- channels in heart. Circ Res 71:1002-1007
45. Liu Y, Wang Y, Jiang Y, Zhu N, Liang H, Xu L, Feng X, et al. (2008) Mild processing defect of porcine DeltaF508-CFTR suggests that DeltaF508 pigs may not develop cystic fibrosis disease. Biochem Biophys Res Commun 373:113-118
46. Mendes F, Doucet L, Hinzpeter A, Ferec C, Lipecka J, Fritsch J, Edelman A, et al. (2004) Immunohistochemistry of CFTR in native tissues and primary epithelial cell cultures. J Cyst Fibros 3(suppl 2):37-41
47. Meyerholz DK, Stoltz DA, Pezzulo AA, Welsh MJ (2010) Pathology of gastrointestinal organs in a porcine model of cystic fibrosis. Am J Pathol 176:1377-1389
48. Mulberg AE, Weyler RT, Altschuler SM, Hyde TM (1998) Cystic fibrosis transmembrane conductance regulator expression in human hypothalamus. Neuroreport 9:141-144
49. Niu N, Zhang J, Guo Y, Yang C, Gu J (2009) Cystic fibrosis transmembrane conductance regulator expression in human spinal and sympathetic ganglia. Lab Invest 89:636-644
50. Ostedgaard LS, Rogers CS, Dong Q, Randak CO, Vermeer DW, Rokhlina T, Karp PH, et al. (2007) Processing and function of CFTR-DeltaF508 are species-dependent. Proc Natl Acad Sci USA 104:15370-15375
51. Patrizio P, Salameh WA (1998) Expression of the cystic fibrosis transmembrane conductance regulator (CFTR) mRNA in normal and pathological adult human epididymis. J Reprod Fertil Suppl 53:261-270
52. Plog S, Mundhenk L, Klymiuk N, Gruber AD (2009) Genomic, tissue expression and protein characterization of pCLCA1, a putative modulator of cystic fibrosis in the pig. J Histochem Cytochem 57:1169-1181
53. Regnier A, Dannhoffer L, Blouquit-Laye S, Bakari M, Naline E, Chinet T (2008) Expression of cystic fibrosis transmembrane conductance regulator in the human distal lung. Hum Pathol 39:368-376
54. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, et al. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066-1073 (Pubitemid 19231814)
55. Rogers CS, Abraham WM, Brogden KA, Engelhardt JF, Fisher JT, McCray PB Jr, McLennan G, et al. (2008a) The porcine lung as a potential model for cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 295:L240-263
56. Rogers CS, Stoltz DA, Meyerholz DK, Ostedgaard LS, Rokhlina T, Taft PJ, Rogan MP, et al. (2008b) Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 321:1837-1841
57. Rommens JM, Zengerling-Lentes S, Kerem B, Melmer G, Buchwald M, Tsui LC (1989) Physical localization of two DNA markers closely linked to the cystic fibrosis locus by pulsed-field gel electrophoresis. Am J Hum Genet 45:932-941
58. Scholte BJ, Davidson DJ, Wilke M, De Jonge HR (2004) Animal models of cystic fibrosis. J Cyst Fibros 3(suppl 2):183-190
59. Strong TV, Boehm K, Collins FS (1994) Localization of cystic fibrosis transmembrane conductance regulator mRNA in the human gastrointestinal tract by in situ hybridization. J Clin Invest 93:347-354
60. Sun XC, McCutheon C, Bertram P, Xie Q, Bonanno JA (2001) Studies on the expression of mRNA for anion transport related proteins in corneal endothelial cells. Curr Eye Res 22:1-7
61. Tizzano EF, Chitayat D, Buchwald M (1993) Cell-specific localization of CFTR mRNA shows developmentally regulated expression in human fetal tissues. Hum Mol Genet 2:219-224
62. Tizzano EF, Silver MM, Chitayat D, Benichou JC, Buchwald M (1994) Differential cellular expression of cystic fibrosis transmembrane regulator in human reproductive tissues. Clues for the infertility in patients with cystic fibrosis. Am J Pathol 144:906-914
63. Tousson A, Van Tine BA, Naren AP, Shaw GM, Schwiebert LM (1998) Characterization of CFTR expression and chloride channel activity in human endothelia. Am J Physiol 275:C1555-1564
64. Verkman AS, Song Y, Thiagarajah JR (2003) Role of airway surface liquid and submucosal glands in cystic fibrosis lung disease. Am J Physiol Cell Physiol 284:C2-15
65. Warth JD, Collier ML, Hart P, Geary Y, Gelband CH, Chapman T, Horowitz B, et al. (1996) CFTR chloride channels in human and simian heart. Cardiovasc Res 31:615-624
66. Welsh MJ, Rogers CS, Stoltz DA, Meyerholz DK, Prather RS (2009) Development of a porcine model of cystic fibrosis. Trans Am Clin Climatol Assoc 120:149-162
67. Wills NK, Weng T, Mo L, Hellmich HL, Yu A, Wang T, Buchheit S, et al. (2000) Chloride channel expression in cultured human fetal RPE cells: response to oxidative stress. Invest Ophthalmol Vis Sci 41:4247-4255
68. Yajima T, Nagashima H, Tsutsumi-Sakai R, Hagiwara N, Hosoda S, Quertermous T, Kasanuki H, et al. (1997) Functional activity of the CFTR Cl- channel in humanmyocardium. Heart Vessels 12:255-261
69. Zheng XY, Chen GA, Wang HY (2004) Expression of cystic fibrosis transmembrane conductance regulator in human endometrium. Hum Reprod 19:2933-2941