Efficient delivery of RNA interference oligonucleotides to polarized airway epithelia in vitro

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 305, Issue 1, 2013, Pages

  Ramachandran, Shyam ^a   Krishnamurthy, Sateesh ^a   Jacobi, Ashley M ^b   Wohlford Lenane, Christine ^a   Behlke, Mark A ^b   Davidson, Beverly L ^a   McCray, Paul B ^a  

^a UNIVERSITY OF IOWA   (United States)

^b INTEGRATED DNA TECHNOLOGIES   (United States)

Author keywords

Air liquid interface; Gene silencing; Porcine airway epithelial cells; Primary airway epithelium; RNA interference; siRNA; Transfection

Indexed keywords

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INTERLEUKIN 8; LIPOFECTAMINE; MICRORNA; OLIGONUCLEOTIDE; REAGENT; SMALL INTERFERING RNA;

ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE RELEASE; EPITHELIUM CELL; EXPERIMENTAL PIG; FLOW CYTOMETRY; GENE FUNCTION; GENE SILENCING; GENE TARGETING; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; NONHUMAN; NUCLEOTIDE TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA TRANSPORT;

EID: 84879572029     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00426.2012     Document Type: Article

References (66)

1. Alvarez R, Elbashir S, Borland T, Toudjarska I, Hadwiger P, John M, Roehl I, Morskaya SS, Martinello R, Kahn J, Van Ranst M, Tripp RA, DeVincenzo JP, Pandey R, Maier M, Nechev L, Manoharan M, Kotelianski V, Meyers R. RNA interference-mediated silencing of the respiratory syncytial virus nucleocapsid defines a potent antiviral strategy. Antimicrob Agents Chemother 53: 3952-3962, 2009.
2. Antunes MB, Woodworth BA, Bhargave G, Xiong G, Aguilar JL, Ratner AJ, Kreindler JL, Rubenstein RC, Cohen NA. Murine nasal septa for respiratory epithelial air-liquid interface cultures. Biotechniques 43: 195-196, 2007.
3. Arvey A, Larsson E, Sander C, Leslie CS, Marks DS. Target mRNA abundance dilutes microRNA and siRNA activity. Mol Syst Biol 6: 363, 2010.
4. Behlke MA. Chemical modification of siRNAs for in vivo use. Oligonucleotides 18: 305-319, 2008.
5. Bitko V, Musiyenko A, Shulyayeva O, Barik S. Inhibition of respiratory viruses by nasally administered siRNA. Nature Med 11: 50-55, 2005.
6. Bonfield TL, Konstan MW, Berger M. Altered respiratory epithelial cell cytokine production in cystic fibrosis. J Allergy Clin Immunol 104: 72-78, 1999.
7. Bonfield TL, Panuska JR, Konstan MW, Hilliard KA, Hilliard JB, Ghnaim H, Berger M. Inflammatory cytokines in cystic fibrosis lungs. Am J Respir Crit Care Med 152: 2111-2118, 1995.
8. Boudreau RL, Spengler RM, Hylock RH, Kusenda BJ, Davis HA, Eichmann DA, Davidson BL. siSPOTR: a tool for designing highly specific and potent siRNAs for human and mouse. Nucleic Acids Res 41: e9, 2013.
9. Caci E, Melani R, Pedemonte N, Yueksekdag G, Ravazzolo R, Rosenecker J, Galietta LJ, Zegarra-Moran O. Epithelial sodium channel inhibition in primary human bronchial epithelia by transfected siRNA. Am J Respir Cell Mol Biol 40: 211-216, 2009.
10. Collingwood MA, Rose SD, Huang L, Hillier C, Amarzguioui M, Wiiger MT, Soifer HS, Rossi JJ, Behlke MA. Chemical modification patterns compatible with high potency dicer-substrate small interfering RNAs. Oligonucleotides 18: 187-200, 2008.
11. Davidson BL, McCray PB Jr. Current prospects for RNA interferencebased therapies. Nat Rev Genet 12: 329-340, 2011.
12. de Jong PM, van Sterkenburg MA, Hesseling SC, Kempenaar JA, Mulder AA, Mommaas AM, Dijkman JH, Ponec M. Ciliogenesis in human bronchial epithelial cells cultured at the air-liquid interface. Am J Respir Cell Mol Biol 10: 271-277, 1994.
13. DeVincenzo J, Lambkin-Williams R, Wilkinson T, Cehelsky J, Nochur S, Walsh E, Meyers R, Gollob J, Vaishnaw A. A randomized, double-blind, placebo-controlled study of an RNAi-based therapy directed against respiratory syncytial virus. Proc Natl Acad Sci USA 107: 8800-8805, 2010.
14. Dharmsathaphorn K, McRoberts JA, Mandel KG, Tisdale LD, Masui H. A human colonic tumor cell line that maintains vectorial electrolyte transport. Am J Physiol Gastrointest Liver Physiol 246: G204-G208, 1984.
15. Durcan N, Murphy C, Cryan SA. Inhalable siRNA: potential as a therapeutic agent in the lungs. Mol Pharm 5: 559-566, 2008.
16. Eguchi A, Meade BR, Chang YC, Fredrickson CT, Willert K, Puri N, Dowdy SF. Efficient siRNA delivery into primary cells by a peptide transduction domain-dsRNA binding domain fusion protein. Nat Biotechnol 27: 567-571, 2009.
17. Ferrari S, Geddes DM, Alton EW. Barriers to and new approaches for gene therapy and gene delivery in cystic fibrosis. Adv Drug Deliv Rev 54: 1373-1393, 2002.
18. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. Well-differentiated human airway epithelial cell cultures. Methods Mol Med 107: 183-206, 2005.
19. Ge Q, Dallas A, Ilves H, Shorenstein J, Behlke MA, Johnston BH. Effects of chemical modification on the potency, serum stability, and immunostimulatory properties of short shRNAs. RNA 16: 118-130, 2010.
20. Ge Q, Filip L, Bai A, Nguyen T, Eisen HN, Chen J. Inhibition of influenza virus production in virus-infected mice by RNA interference. Proc Natl Acad Sci USA 101: 8676-8681, 2004.
21. Grainger CI, Greenwell LL, Lockley DJ, Martin GP, Forbes B. Culture of Calu-3 cells at the air interface provides a representative model of the airway epithelial barrier. Pharm Res 23: 1482-1490, 2006.
22. Gray TE, Guzman K, Davis CW, Abdullah LH, Nettesheim P. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am J Respir Cell Mol Biol 14: 104-112, 1996.
23. Griesenbach U, Kitson C, Escudero Garcia S, Farley R, Singh C, Somerton L, Painter H, Smith RL, Gill DR, Hyde SC, Chow YH, Hu J, Gray M, Edbrooke M, Ogilvie V, MacGregor G, Scheule RK, Cheng SH, Caplen NJ, Alton EW. Inefficient cationic lipid-mediated siRNA and antisense oligonucleotide transfer to airway epithelial cells in vivo. Respir Res 7: 26, 2006.
24. Gruenert DC, Finkbeiner WE, Widdicombe JH. Culture and transformation of human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 268: L347-L360, 1995.
25. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K. Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56: 559-564, 1994.
26. 2+ conductance. Am J Physiol Lung Cell Mol Physiol 266: L502-L512, 1994.
27. Hefner E, Clark K, Whitman C, Behlke MA, Rose SD, Peek AS, Rubio T. Increased potency and longevity of gene silencing using validated Dicer substrates. J Biomol Tech 19: 231-237, 2008.
28. Hillian AD, Londono D, Dunn JM, Goddard KA, Pace RG, Knowles MR, Drumm ML. Modulation of cystic fibrosis lung disease by variants in interleukin-8. Genes Immun 9: 501-508, 2008.
29. Hutt DM, Herman D, Rodrigues AP, Noel S, Pilewski JM, Matteson J, Hoch B, Kellner W, Kelly JW, Schmidt A, Thomas PJ, Matsumura Y, Skach WR, Gentzsch M, Riordan JR, Sorscher EJ, Okiyoneda T, Yates JR 3rd, Lukacs GL, Frizzell RA, Manning G, Gottesfeld JM, Balch WE. Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis. Nat Chem Biol 6: 25-33, 2010.
30. + conductance. Proc Natl Acad Sci USA 108: 10260-10265, 2011.
31. Judge AD, Robbins M, Tavakoli I, Levi J, Hu L, Fronda A, Ambegia E, McClintock K, MacLachlan I. Confirming the RNAi-mediated mechanism of action of siRNA-based cancer therapeutics in mice. J Clin Invest 119: 661-673, 2009.
32. Karp PH, Moninger TO, Weber SP, Nesselhauf TS, Launspach JL, Zabner J, Welsh MJ. An in vitro model of differentiated human airway epithelia. Methods for establishing primary cultures. Methods Mol Biol 188: 115-137, 2002.
33. Karp PH, Moninger TO, Weber SP, Nesselhauf TS, Launspach JL, Zabner J, Welsh MJ. An in vitro model of differentiated human airway epithelia. Methods for establishing primary cultures. Methods Mol Biol 188: 115-137, 2002.
34. Kim DH, Behlke MA, Rose SD, Chang MS, Choi S, Rossi JJ. Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy. Nat Biotechnol 23: 222-226, 2005.
35. Kleinman ME, Yamada K, Takeda A, Chandrasekaran V, Nozaki M, Baffi JZ, Albuquerque RJ, Yamasaki S, Itaya M, Pan Y, Appukuttan B, Gibbs D, Yang Z, Kariko K, Ambati BK, Wilgus TA, DiPietro LA, Sakurai E, Zhang K, Smith JR, Taylor EW, Ambati J. Sequence-and target-independent angiogenesis suppression by siRNA via TLR3. Nature 452: 591-597, 2008.
36. Krishnamurthy S, Behlke MA, Ramachandran S, Salem AK, McCray PB Jr, Davidson BL. Manipulation of cell physiology enables gene silencing in well-differentiated airway epithelia. Mol Ther Nucleic Acids 1: e41, 2012.
37. Kunzelmann K, Schwiebert EM, Zeitlin PL, Kuo W-L, Stanton BA, Gruenert DC. An immortalized cystic fibrosis tracheal epithelial cell line homozygous for the F508 CFTR mutation. Am J Respir Cell Mol Biol 8: 522-529, 1993.
38. Layzer JM, McCaffrey AP, Tanner AK, Huang Z, Kay MA, Sullenger BA. In vivo activity of nuclease-resistant siRNAs. RNA 10: 766-771, 2004.
39. Lechner JF, LaVeck MA. A serum-free method for culturing normal human bronchial epithelial cells at clonal density. J Tissue Cult Methods 9: 43-48, 1985.
40. Lennox KA, Behlke MA. Chemical modification and design of antimiRNA oligonucleotides. Gene Ther 18: 1111-1120, 2011.
41. Li BJ, Tang Q, Cheng D, Qin C, Xie FY, Wei Q, Xu J, Liu Y, Zheng BJ, Woodle MC, Zhong N, Lu PY. Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque. Nat Med 11: 944-951, 2005.
42. Madara JL, Stafford J, Dharmsathaphorn K, Carlson S. Structural analysis of a human intestinal epithelial cell line. Gastroenterology 92: 1133-1145, 1987.
43. Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 3: 100-105, 2001.
44. Merkel OM, Beyerle A, Librizzi D, Pfestroff A, Behr TM, Sproat B, Barth PJ, Kissel T. Nonviral siRNA delivery to the lung: investigation of PEG-PEI polyplexes and their in vivo performance. Mol Pharm 6: 1246-1260, 2009.
45. Moschos SA, Frick M, Taylor B, Turnpenny P, Graves H, Spink KG, Brady K, Lamb D, Collins D, Rockel TD, Weber M, Lazari O, Perez-Tosar L, Fancy SA, Lapthorn C, Green MX, Evans S, Selby M, Jones G, Jones L, Kearney S, Mechiche H, Gikunju D, Subramanian R, Uhlmann E, Jurk M, Vollmer J, Ciaramella G, Yeadon M. Uptake, efficacy, and systemic distribution of naked, inhaled short interfering RNA (siRNA) and locked nucleic acid (LNA) antisense. Mol Ther 19: 2163-2168, 2011.
46. Nielsen R, Birn H, Moestrup SK, Nielsen M, Verroust P, Christensen EI. Characterization of a kidney proximal tubule cell line, LLC-PK1, expressing endocytotic active megalin. J Am Soc Nephrol 9: 1767-1776, 1998.
47. Okiyoneda T, Barriere H, Bagdany M, Rabeh WM, Du K, Hohfeld J, Young JC, Lukacs GL. Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329: 805-810, 2010.
48. Ostedgaard LS, Meyerholz DK, Chen JH, Pezzulo AA, Karp PH, Rokhlina T, Ernst SE, Hanfland RA, Reznikov LR, Ludwig PS, Rogan MP, Davis GJ, Dohrn CL, Wohlford-Lenane C, Taft PJ, Rector MV, Hornick E, Nassar BS, Samuel M, Zhang Y, Richter SS, Uc A, Shilyansky J, Prather RS, McCray PB Jr, Zabner J, Welsh MJ, Stoltz DA. The F508 mutation causes CFTR misprocessing and cystic fibrosislike disease in pigs. Sci Transl Med 3: 74ra24, 2011.
49. Parker D, Prince A. Innate immunity in the respiratory epithelium. Am J Respir Cell Mol Biol 45: 189-201, 2011.
50. Platz J, Pinkenburg O, Beisswenger C, Puchner A, Damm T, Bals R. Application of small interfering RNA (siRNA) for modulation of airway epithelial gene expression. Oligonucleotides 15: 132-138, 2005.
51. Ramachandran S, Karp PH, Osterhaus SR, Jiang P, Wohlford-Lenane C, Lennox KA, Jacobi AM, Parekh K, Rose SD, Behlke MA, Xing Y, Welsh MJ, McCray PB Jr. Post-transcriptional regulation of CFTR expression and function by microRNAs. Am J Respir Cell Mol Biol 2013 May 6. [Epub ahead of print]
52. Ramachandran S, Clarke LA, Scheetz TE, Amaral MD, McCray PB Jr. Microarray mRNA expression profiling to study cystic fibrosis. Methods Mol Biol 742: 193-212, 2011.
53. Ramachandran S, Karp PH, Jiang P, Ostedgaard LS, Walz AE, Fisher JT, Keshavjee S, Lennox KA, Jacobi AM, Rose SD, Behlke MA, Welsh MJ, Xing Y, McCray PB Jr. A microRNA network regulates expression and biosynthesis of wild-type and F508 mutant cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci USA 109: 13362-13367, 2012.
54. Robbins M, Judge A, Ambegia E, Choi C, Yaworski E, Palmer L, McClintock K, MacLachlan I. Misinterpreting the therapeutic effects of small interfering RNA caused by immune stimulation. Hum Gene Ther 19: 991-999, 2008.
55. Rose SD, Kim DH, Amarzguioui M, Heidel JD, Collingwood MA, Davis ME, Rossi JJ, Behlke MA. Functional polarity is introduced by Dicer processing of short substrate RNAs. Nucleic Acids Res 33: 4140-4156, 2005.
56. Ross AJ, Dailey LA, Brighton LE, Devlin RB. Transcriptional profiling of mucociliary differentiation in human airway epithelial cells. Am J Respir Cell Mol Biol 37: 169-185, 2007.
57. Stout JT, Caskey CT. HPRT: gene structure, expression, and mutation. Annu Rev Genet 19: 127-148, 1985.
58. Thomas M, Lu JJ, Chen J, Klibanov AM. Non-viral siRNA delivery to the lung. Adv Drug Deliv Rev 59: 124-133, 2007.
59. Tompkins SM, Lo CY, Tumpey TM, Epstein SL. Protection against lethal influenza virus challenge by RNA interference in vivo. Proc Natl Acad Sci USA 101: 8682-8686, 2004.
60. Trapnell BC, Chu CS, Paakko PK, Banks TC, Yoshimura K, Ferrans VJ, Chernick MS, Crystal RG. Expression of cystic fibrosis transmembrane conductance regulator gene in the respiratory tract of normal individuals and individuals with cystic fibrosis. Proc Natl Acad Sci USA 88: 6565-6569, 1991.
61. Varga K, Jurkuvenaite A, Wakefield J, Hong JS, Guimbellot JS, Venglarik CJ, Niraj A, Mazur M, Sorscher EJ, Collawn JF, Bebok Z. Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J Biol Chem 279: 22578-22584, 2004.
62. White AF, Ponnazhagan S. Airway epithelium directed gene therapy for cystic fibrosis. Med Chem 2: 499-503, 2006.
63. Woodworth BA, Antunes MB, Bhargave G, Palmer JN, Cohen NA. Murine tracheal and nasal septal epithelium for air-liquid interface cultures: a comparative study. Am J Rhinol 21: 533-537, 2007.
64. Yamaya M, Finkbeiner WE, Chun SY, Widdicombe JH. Differentiated structure and function of cultures from human tracheal epithelium. Am J Physiol Lung Cell Mol Physiol 262: L713-L724, 1992.
65. Zabner J, Fasbender AJ, Moninger T, Poellinger KA, Welsh MJ. Cellular and molecular barriers to gene transfer by a cationic lipid. J Biol Chem 270: 18997-19007, 1995.
66. Zabner J, Zeiher BG, Friedman E, Welsh MJ. Adenovirus-mediated gene transfer to ciliated airway epithelia requires prolonged incubation time. J Virol 70: 6994-7003, 1996.