Amelioration of emphysema in mice through lentiviral transduction of long-lived pulmonary alveolar macrophages

Journal of Clinical Investigation

Volumn 120, Issue 1, 2010, Pages 379-389

  Wilson, Andrew A ^a   Murphy, George J ^a   Hamakawa, Hiroshi ^b   Kwok, Letty W ^a   Srinivasan, Sreedevi ^c   Hovav, Avi Hai ^d   Mulligan, Richard C ^e   Amar, Salomon ^c   Suki, Bela ^b   Kotton, Darrell N ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Boston University   (United States)

^c BOSTON UNIVERSITY   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; HUMAN ALPHA 1 ANTITRYPSIN; UNCLASSIFIED DRUG; CD45 ANTIGEN; G PROTEIN, VESICULAR STOMATITIS VIRUS; MEMBRANE PROTEIN; PTPRC PROTEIN, MOUSE; VIRUS ENVELOPE PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE COURSE; GENE EXPRESSION; GENE TRANSFER; HUMAN; IN VIVO GENE TRANSFER; IN VIVO STUDY; LENTIVIRINAE; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; LUNG COMPLIANCE; LUNG EMPHYSEMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL; TARGET CELL; VIRAL GENE DELIVERY SYSTEM; ANIMAL; C57BL MOUSE; EMPHYSEMA; GENE THERAPY; GENETIC TRANSDUCTION; GENETICS; INFLAMMATION; METABOLISM;

ALPHA 1-ANTITRYPSIN; ANIMALS; ANTIGENS, CD45; EMPHYSEMA; GENE THERAPY; HUMANS; INFLAMMATION; LENTIVIRUS; MACROPHAGES, ALVEOLAR; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; TRANSDUCTION, GENETIC; VIRAL ENVELOPE PROTEINS;

EID: 74949132576     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI36666     Document Type: Article

References (61)

1. Yang Y, et al. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol. 1995;69(4):2004-2015.
2. Zabner J, et al. Adenovirus-mediated gene transfer transiently corrects the chloride transport defect in nasal epithelia of patients with cystic fibrosis. Cell. 1993;75(2):207-216.
3. Grubb BR, et al. Inefficient gene transfer by adenovirus vector to cystic fibrosis airway epithelia of mice and humans. Nature. 1994;371(6500):802-806.
4. Young LS, Searle PF, Onion D, Mautner V. Viral gene therapy strategies: from basic science to clinical application. J Pathol. 2006;208(2):299-318.
5. Conrad C, et al. Genetically engineered stem cells for therapeutic gene delivery. Curr Gene Ther. 2007;7(4):249-260.
6. Pan H, Mostoslavsky G, Eruslanov E, Kotton DN, Kramnik I. Dual-promoter lentiviral system allows inducible expression of noxious proteins in macrophages. J Immunol Methods. 2008;329(1-2):31-44.
7. Stecenko AA, Brigham KL. Gene therapy progress and prospects: alpha-1 antitrypsin. Gene Ther. 2003;10(2):95-99.
8. Gregory RJ, et al. Expression and characterization of the cystic fibrosis transmembrane conductance regulator. Nature. 1990;347(6291):382-386.
9. Garver RI Jr, Chytil A, Courtney M, Crystal RG. Clonal gene therapy: transplanted mouse fibroblast clones express human alpha 1-antitrypsin gene in vivo. Science. 1987;237(4816):762-764.
10. Yang Y, et al. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci U S A. 1994;91(10):4407-4411.
11. Murphy J, Summer R, Wilson AA, Kotton DN, Fine A. The prolonged life-span of alveolar macrophages. Am J Respir Cell Mol Biol. 2008;38(4):380-385.
12. Murphy GJ, Mostoslavsky G, Kotton DN, Mulligan RC. Exogenous control of mammalian gene expression via modulation of translational termination. Nat Med. 2006;12(9):1093-1099.
13. Sinn PL, et al. Lentivirus vectors pseudotyped with filoviral envelope glycoproteins transduce airway epithelia from the apical surface independently of folate receptor alpha. J Virol. 2003;77(10):5902-5910.
14. Wang G, Sinn PL, McCray PB Jr. Development of retroviral vectors for gene transfer to airway epithelia. Curr Opin Mol Ther. 2000;2(5):497-506.
15. Kobinger GP, Weiner DJ, Yu QC, Wilson JM. Filovirus-pseudotyped lentiviral vector can efficiently and stably transduce airway epithelia in vivo. Nat Biotechnol. 2001;19(3):225-230.
16. Johnson LG, Olsen JC, Naldini L, Boucher RC. Pseudotyped human lentiviral vector-mediated gene transfer to airway epithelia in vivo. Gene Ther. 2000;7(7):568-574.
17. Landsman L, Jung S. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J Immunol. 2007;179(6):3488-3494.
18. Maus U, et al. Monocytes recruited into the alveolar air space of mice show a monocytic phenotype but upregulate CD14. Am J Physiol Lung Cell Mol Physiol. 2001;280(1):L58-L68.
19. Kotton DN, Summer RS, Sun X, Ma BY, Fine A. Stem cell antigen-1 expression in the pulmonary vascular endothelium. Am J Physiol Lung Cell Mol Physiol. 2003;284(6):L990-L996.
20. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science. 2002;297(5590):2256-2259.
21. Kotton DN, Fabian AJ, Mulligan RC. Failure of bone marrow to reconstitute lung epithelium. Am J Respir Cell Mol Biol. 2005;33(4):328-334.
22. van Oud Alblas AB, van Furth R. Origin, kinetics, and characteristics of pulmonary macrophages in the normal steady state. J Exp Med. 1979;149(6):1504-1518.
23. Jennings JH, Linderman DJ, Hu B, Sonstein J, Curtis JL. Monocytes recruited to the lungs of mice during immune inflammation ingest apoptotic cells poorly. Am J Respir Cell Mol Biol. 2005;32(2):108-117.
24. Maus U, et al. Molecular pathways of monocyte emigration into the alveolar air space of intact mice. Am J Respir Crit Care Med. 2002;165(1):95-100.
25. Wilson AA, et al. Sustained expression of alpha1- antitrypsin after transplantation of manipulated hematopoietic stem cells. Am J Respir Cell Mol Biol. 2008;39(2):133-141.
26. American Thoracic Society and European Respiratory Society. American Thoracic Society/European Respiratory Society statement: standards for the diagnosis and management of individuals with alpha-1 antitrypsin deficiency. Am J Respir Crit Care Med. 2003;168(7):818-900.
27. Ito S, et al. Tissue heterogeneity in the mouse lung: effects of elastase treatment. J Appl Physiol. 2004;97(1):204-212.
28. Parameswaran H, Majumdar A, Ito S, Alencar AM, Suki B. Quantitative characterization of air-space enlargement in emphysema. J Appl Physiol. 2006;100(1):186-193.
29. Lucey EC, Keane J, Kuang PP, Snider GL, Goldstein RH. Severity of elastase-induced emphysema is decreased in tumor necrosis factor-alpha and interleukin-1beta receptor-deficient mice. Lab Invest.
30. Houghton AM, et al. Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest. 2006;116(3):753-759.
31. Churg A, et al. Acute cigarette smoke-induced connective tissue breakdown requires both neutrophils and macrophage metalloelastase in mice. Am J Respir Cell Mol Biol. 2002;27(3):368-374.
32. Hashimoto D, et al. Intratracheal administration of third-generation lentivirus vector encoding MPT51 from Mycobacterium tuberculosis induces specific CD8+ T-cell responses in the lung. Vaccine. 2008;26(40):5095- 5100.
33. Shapiro SD. The macrophage in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1999;160(5 pt 2):S29-S32.
34. Song S, et al. Sustained secretion of human alpha-1-antitrypsin from murine muscle transduced with adeno-associated virus vectors. Proc Natl Acad Sci U S A. 1998;95(24):14384-14388.
35. Song S, et al. Stable therapeutic serum levels of human alpha-1 antitrypsin (AAT) after portal vein injection of recombinant adeno-associated virus (rAAV) vectors. Gene Ther. 2001;8(17):1299-1306.
36. Brantly ML, et al. Phase I trial of intramuscular injection of a recombinant adeno-associated virus serotype 2 alphal-antitrypsin (AAT) vector in AAT-deficient adults. Hum Gene Ther. 2006;17(12):1177-1186.
37. Brigham KL, et al. Transfection of nasal mucosa with a normal alpha1-antitrypsin gene in alpha1-antitrypsin-deficient subjects: comparison with protein therapy. Hum Gene Ther. 2000;11(7):1023-1032.
38. Takahara H, Nakamura Y, Yamamoto K, Sinohara H. Comparative studies on the serum levels of alpha-1-antitrypsin and alpha-macroglobulin in several mammals. Tohoku J Exp Med. 1983;139(3):265-270.
39. Kushi A, et al. Disruption of the murine alpha1-antitrypsin/PI2 gene. Exp Anim. 2004;53(5):437-443.
40. Wewers MD, et al. Replacement therapy for alpha 1-antitrypsin deficiency associated with emphysema. N Engl J Med. 1987;316(17):1055-1062.
41. Seersholm N, et al. Does alpha1-antitrypsin augmentation therapy slow the annual decline in FEV1 in patients with severe hereditary alpha1-antitrypsin deficiency? Wissenschaftliche Arbeitsgemeinschaft zur Therapie von Lungenerkrankungen (WATL) alpha1-AT study group. Eur Respir J. 1997;10(10):2260-2263.
42. Gottlieb DJ, et al. Short-term supplementation therapy does not affect elastin degradation in severe alpha(1)-antitrypsin deficiency. The American-Italian AATD Study Group. Am J Respir Crit Care Med. 2000;162(6):2069-2072.
43. Churg A, Wang RD, Xie C, Wright JL. alpha-1-Antitrypsin ameliorates cigarette smoke-induced emphysema in the mouse. Am J Respir Crit Care Med. 2003;168(2):199-207.
44. Churg A, et al. Alpha-1-antitrypsin and a broad spectrum metalloprotease inhibitor, RS113456, have similar acute anti-inflammatory effects. Lab Invest. 2001;81(8):1119-1131.
45. Petrache I, et al. A novel antiapoptotic role for alpha1-antitrypsin in the prevention of pulmonary emphysema. Am J Respir Crit Care Med. 2006;173(11):1222-1228.
46. Shapiro SD. Transgenic and gene-targeted mice as models for chronic obstructive pulmonary disease. Eur Respir J. 2007;29(2):375-378.
47. Godleski JJ, Brain JD. The origin of alveolar macrophages in mouse radiation chimeras. J Exp Med. 1972;136(3):630-643.
48. Matute-Bello G, et al. Optimal timing to repopulation of resident alveolar macrophages with donor cells following total body irradiation and bone marrow transplantation in mice. J Immunol Methods. 2004;292(1-2):25-34.
49. Borok Z, et al. Vesicular stomatits virus G-pseudotyped lentivirus vectors mediate efficient apical transduction of polarized quiescent primary alveolar epithelial cells. J Virol. 2001;75(23):11747-11754.
50. Wunderlich S, et al. Type II pneumocyte-restricted green fluorescent protein expression after lentiviral transduction of lung epithelial cells. Hum Gene Ther. 2008;19(1):39-52.
51. Yu ZY, et al. Lentivirus vector-mediated gene transfer to the developing bronchiolar air-way epithelium in the fetal lamb. J Gene Med. 2007;9(6):429-439.
52. Buckley SM, et al. Lentiviral transduction of the murine lung provides efficient pseudotype and developmental stage-dependent cell-specific transgene expression. Gene Ther. 2008;15(16):1167-1175.
53. Hendrickson B, et al. Development of lentiviral vectors with regulated respiratory epithelial expression in vivo. Am J Respir Cell Mol Biol. 2007;37(4):414-423.
54. Medina MF, et al. Lentiviral vectors pseudotyped with minimal filovirus envelopes increased gene transfer in murine lung. Mol Ther. 2003;8(5):777-789.
55. Naldini L, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996;272(5259):263- 267.
56. Zufferey R, Donello JE, Trono D, Hope TJ. Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J Virol. 1999;73(4):2886-2892.
57. Rennard SI, et al. Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution. J Appl Physiol. 1986;60(2):532-538.
58. Amar S, Zhou Q, Shaik-Dasthagirisaheb Y, Leeman S. Diet-induced obesity in mice causes changes in immune responses and bone loss manifested by bacterial challenge. Proc Natl Acad Sci U S A. 2007;104(51):20466-20471.
59. Hovav AH, et al. Duration of antigen expression in vivo following DNA immunization modifies the magnitude, contraction, and secondary responses of CD8+ T lymphocytes. J Immunol. 2007;179(10):6725-6733.
60. Ito S, et al. Early emphysema in the tight skin and pallid mice: roles of microfibril-associated glyco-proteins, collagen, and mechanical forces. Am J Respir Cell Mol Biol. 2006;34(6):688-694.
61. Hautamake RD, Kobayashi DK, Senior RM, Shapiro SD. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science. 1997;277(5334):2002-2004.