Oral delivery of angiotensin-converting enzyme 2 and angiotensin-(1-7) bioencapsulated in plant cells attenuates pulmonary hypertension

Hypertension

Volumn 64, Issue 6, 2014, Pages 1248-1259

  Shenoy, Vinayak ^a   Kwon, Kwang Chul ^b   Rathinasabapathy, Anandharajan ^a   Lin, Shina ^b   Jin, Guiying ^b   Song, Chunjuan ^a   Shil, Pollob ^a   Nair, Anand ^c   Qi, Yanfei ^a   Li, Qiuhong ^a   Francis, Joseph ^c   Katovich, Michael J ^a   Daniell, Henry ^b   Raizada, Mohan K ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Chloroplast; Molecular farming; Plant made pharmaceuticals; Pulmonary hypertension; Renin angiotensin system

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN[1-7]; ANGIOTENSIN I; ANGIOTENSIN I (1-7); ANTIHYPERTENSIVE AGENT; DIPEPTIDYL CARBOXYPEPTIDASE; DRUG CARRIER; PEPTIDE FRAGMENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BIOENCAPSULATION; CHLOROPLAST GENOME; CONTROLLED STUDY; DISEASE COURSE; DNA FLANKING REGION; DRUG ABSORPTION; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG STORAGE; ENCAPSULATION; ENZYMATIC DEGRADATION; HEART FUNCTION; LUNG BLOOD VESSEL; MALE; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; PROTEIN STABILITY; PULMONARY HYPERTENSION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; ROOM TEMPERATURE; ANIMAL; BLOOD PRESSURE; CHLOROPLAST; COMBINATION DRUG THERAPY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; HYPERTENSION, PULMONARY; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADMINISTRATION, ORAL; ANGIOTENSIN I; ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; CHLOROPLASTS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG CARRIERS; DRUG THERAPY, COMBINATION; HYPERTENSION, PULMONARY; MALE; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; RATS; RATS, SPRAGUE-DAWLEY; RENIN-ANGIOTENSIN SYSTEM;

EID: 84927796509     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.114.03871     Document Type: Article

References (57)

1. Schermuly RT, Ghofrani HA, Wilkins MR, Grimminger F. Mechanisms of disease: pulmonary arterial hypertension. Nat Rev Cardiol. 2011;8:443-455.
2. Sutendra G, Michelakis ED. Pulmonary arterial hypertension: challenges in translational research and a vision for change. Sci Transl Med. 2013;5:208sr5.
3. De Man FS, Tu L, Handoko ML, et al. Dysregulated renin-angiotensinaldosterone system contributes to pulmonary arterial hypertension. Am J Respir Crit Care Med. 2012;186:780-789.
4. Morrell NW, Atochina EN, Morris KG, Danilov SM, Stenmark KR. Angiotensin converting enzyme expression is increased in small pulmonary arteries of rats with hypoxia-induced pulmonary hypertension. J Clin Invest. 1995;96:1823-1833.
5. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart RE, Acton S. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res. 2000;87:E1-E9.
6. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem. 2000;275:33238-33243.
7. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis G, Van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol. 2004;203:631-637.
8. Santos RA, Simoes E Silva AC, Maric C, et al. Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci U S A. 2003;100:8258-8263.
9. Li X, Molina-Molina M, Abdul-Hafez A, Uhal V, Xaubet A, Uhal BD. Angiotensin converting enzyme-2 is protective but downregulated in human and experimental lung fibrosis. Am J Physiol Lung Cell Mol Physiol. 2008;295:L178-L185.
10. Dai HL, Guo Y, Guang XF, Xiao ZC, Zhang M, Yin XL. The changes of serum angiotensin-converting enzyme 2 in patients with pulmonary arterial hypertension due to congenital heart disease. Cardiology. 2013;124:208-212.
11. Yamazato Y, Ferreira AJ, Hong KH, Sriramula S, Francis J, Yamazato M, Yuan L, Bradford CN, Shenoy V, Oh SP, Katovich MJ, Raizada MK. Prevention of pulmonary hypertension by angiotensin-converting enzyme 2 gene transfer. Hypertension. 2009;54:365-371.
12. Shenoy V, Ferreira AJ, Qi Y, et al. The angiotensin-converting enzyme 2/angiogenesis-(1-7)/Mas axis confers cardiopulmonary protection against lung fbrosis and pulmonary hypertension. Am J Respir Crit Care Med. 2010;182:1065-1072.
13. Kleinsasser A, Pircher I, Treml B, Schwienbacher M, Schuster M, Janzek E, Loibner H, Penninger JM, Loeckinger A. Recombinant angiotensinconverting enzyme 2 suppresses pulmonary vasoconstriction in acute hypoxia. Wilderness Environ Med. 2012;23:24-30.
14. Ferreira AJ, Shenoy V, Yamazato Y, Sriramula S, Francis J, Yuan L, Castellano RK, Ostrov DA, Oh SP, Katovich MJ, Raizada MK. Evidence for angiotensin-converting enzyme 2 as a therapeutic target for the prevention of pulmonary hypertension. Am J Respir Crit Care Med. 2009;179:1048-1054.
15. Shenoy V, Gjymishka A, Jarajapu YP, et al. Diminazene attenuates pulmonary hypertension and improves angiogenic progenitor cell functions in experimental models. Am J Respir Crit Care Med. 2013;187:648-657.
16. Ruhlman T, Verma D, Samson N, Daniell H. The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol. 2010;152:2088-2104.
17. Boyhan D, Daniell H. Low-cost production of proinsulin in tobacco and lettuce chloroplasts for injectable or oral delivery of functional insulin and C-peptide. Plant Biotechnol J. 2011;9:585-598.
18. Kwon KC, Nityanandam R, New JS, Daniell H. Oral delivery of bioencapsulated exendin-4 expressed in chloroplasts lowers blood glucose level in mice and stimulates insulin secretion in beta-TC6 cells. Plant Biotechnol J. 2013;11:77-86.
19. Ruhlman T, Ahangari R, Devine A, Samsam M, Daniell H. Expression of cholera toxin B-proinsulin fusion protein in lettuce and tobacco chloroplasts-oral administration protects against development of insulitis in non-obese diabetic mice. Plant Biotechnol J. 2007;5:495-510.
20. Verma D, Moghimi B, Lo Duca PA, Singh HD, Hoffman BE, Herzog RW, Daniell H. Oral delivery of bioencapsulated coagulation factor IX prevents inhibitor formation and fatal anaphylaxis in hemophilia B mice. Proc Natl Acad Sci U S A. 2010;107:7101-7106.
21. Kwon KC, Verma D, Singh ND, Herzog R, Daniell H. Oral delivery of human biopharmaceuticals, autoantigens and vaccine antigens bioencapsulated in plant cells. Adv Drug Deliv Rev. 2013;65:782-799.
22. Daniell H. Transgene containment by maternal inheritance: effective or elusive? Proc Natl Acad Sci U S A. 2007;104:6879-6880.
23. Daniell H, Singh ND, Mason H, Streatfeld SJ. Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci. 2009;14:669-679.
24. Lakshmi PS, Verma D, Yang X, Lloyd B, Daniell H. Low cost tuberculosis vaccine antigens in capsules: expression in chloroplasts, bio-encapsulation, stability and functional evaluation in vitro. PLoS One. 2013;8:e54708.
25. Zimran A, Brill-Almon E, Chertkoff R, et al. Pivotal trial with plant cellexpressed recombinant glucocerebrosidase, taliglucerase alfa, a novel enzyme replacement therapy for Gaucher disease. Blood. 2011;118:5767-5773.
26. Verma D, Samson NP, Koya V, Daniell H. A protocol for expression of foreign genes in chloroplasts. Nat Protoc. 2008;3:739-758.
27. Zhang RG, Westbrook ML, Westbrook EM, Scott DL, Otwinowski Z, Maulik PR, Reed RA, Shipley GG. The 2.4 A crystal structure of cholera toxin B subunit pentamer: choleragenoid. J Mol Biol. 1995;251:550-562.
28. Long L, Yang X, Southwood M, Lu J, Marciniak SJ, Dunmore BJ, Morrell NW. Chloroquine prevents progression of experimental pulmonary hypertension via inhibition of autophagy and lysosomal bone morphogenetic protein type II receptor degradation. Circ Res. 2013;112:1159-1170.
29. Santos RA, Ferreira AJ, Nadu AP, Braga AN, De Almeida AP, Campagnole-Santos MJ, Baltatu O, Iliescu R, Reudelhuber TL, Bader M. Expression of an angiotensin-(1-7)-producing fusion protein produces cardioprotective effects in rats. Physiol Genomics. 2004;17:292-299.
30. Ruiz ON, Alvarez D, Torres C, Roman L, Daniell H. Metallothionein expression in chloroplasts enhances mercury accumulation and phytoremediation capability. Plant Biotechnol J. 2011;9:609-617.
31. Mäger I, Roberts TC, Wood MJ, El Andaloussi S. From gut to brain: bioencapsulated therapeutic protein reduces amyloid load upon oral delivery. Mol Ther. 2014;22:485-486.
32. Kohli N, Westerveld DR, Ayache AC, Verma A, Shil P, Prasad T, Zhu P, Chan SL, Li Q, Daniell H. Oral delivery of bioencapsulated proteins across blood-brain and blood-retinal barriers. Mol Ther. 2014;22:535-546.
33. Morton BR. Chloroplast DNA codon use: evidence for selection at the psb A locus based on tRNA availability. J Mol Evol. 1993;37:273-280.
34. Karlin S, Mrázek J. What drives codon choices in human genes? J Mol Biol. 1996;262:459-472.
35. De Cosa B, Moar W, Lee SB, Miller M, Daniell H. Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol. 2001;19:71-74.
36. Daniell H, Ruiz G, Denes B, Sandberg L, Langridge W. Optimization of codon composition and regulatory elements for expression of human insulin like growth factor-1 in transgenic chloroplasts and evaluation of structural identity and function. BMC Biotechnol. 2009;9:33.
37. Arlen PA, Falconer R, Cherukumilli S, Cole A, Cole AM, Oishi KK, Daniell H. Field production and functional evaluation of chloroplastderived interferon-alpha2b. Plant Biotechnol J. 2007;5:511-525.
38. Hill DR, Ford L, Lalloo DG. Oral cholera vaccines: use in clinical practice. Lancet Infect Dis. 2006;6:361-373.
39. Stanford M, Whittall T, Bergmeier LA, Lindblad M, Lundin S, Shinnick T, Mizushima Y, Holmgren J, Lehner T. Oral tolerization with peptide 336-351 linked to cholera toxin B subunit in preventing relapses of uveitis in Behcet's disease. Clin Exp Immunol. 2004;137:201-208.
40. Sun JB, Czerkinsky C, Holmgren J. Mucosally induced immunological tolerance, regulatory T cells and the adjuvant effect by cholera toxin B subunit. Scand J Immunol. 2010;71:1-11.
41. Wilson JP. Surface area of the small intestine in man. Gut. 1967;8:618-621.
42. Holmgren J, Lönnroth I, Månsson J, Svennerholm L. Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc Natl Acad Sci U S A. 1975;72:2520-2524.
43. Fishman PH, Bradley RM, Hom BE, Moss J. Uptake and metabolism of exogenous gangliosides by cultured cells: effect of choleragen on the turnover of GM1. J Lipid Res. 1983;24:1002-1011.
44. Yamada K, Iyer SN, Chappell MC, Ganten D, Ferrario CM. Converting enzyme determines plasma clearance of angiotensin-(1-7). Hypertension. 1998;32:496-502.
45. Allred AJ, Diz DI, Ferrario CM, Chappell MC. Pathways for angiotensin-(1-7) metabolism in pulmonary and renal tissues. Am J Physiol Renal Physiol. 2000;279:F841-F850.
46. Duckert P, Brunak S, Blom N. Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel. 2004;17:107-112.
47. Bradford CN, Ely DR, Raizada MK. Targeting the vasoprotective axis of the renin-angiotensin system: a novel strategic approach to pulmonary hypertensive therapy. Curr Hypertens Rep. 2010;12:212-219.
48. Oudit GY, Liu GC, Zhong J, Basu R, Chow FL, Zhou J, Loibner H, Janzek E, Schuster M, Penninger JM, Herzenberg AM, Kassiri Z, Scholey JW. Human recombinant ACE2 reduces the progression of diabetic nephropathy. Diabetes. 2010;59:529-538.
49. Zou Z, Yan Y, Shu Y, et al. Angiotensin-converting enzyme 2 protects from lethal avian influenza A H5N1 infections. Nat Commun. 2014;5:3594.
50. Zhong J, Guo D, Chen CB, Wang W, Schuster M, Loibner H, Penninger JM, Scholey JW, Kassiri Z, Oudit GY. Prevention of angiotensin II-mediated renal oxidative stress, infammation, and fbrosis by angiotensin-converting enzyme 2. Hypertension. 2011;57:314-322.
51. Wagenaar GT, Laghmani El H, Fidder M, Sengers RM, De Visser YP, De Vries L, Rink R, Roks AJ, Folkerts G, Walther FJ. Agonists of MAS oncogene and angiotensin II type 2 receptors attenuate cardiopulmonary disease in rats with neonatal hyperoxia-induced lung injury. Am J Physiol Lung Cell Mol Physiol. 2013;305:L341-L351.
52. Dorfmüller P, Perros F, Balabanian K, Humbert M. Infammation in pulmonary arterial hypertension. Eur Respir J. 2003;22:358-363.
53. Freeman EJ, Chisolm GM, Ferrario CM, Tallant EA. Angiotensin-(1-7) inhibits vascular smooth muscle cell growth. Hypertension. 1996;28:104-108.
54. Velkoska E, Dean RG, Griggs K, Burchill L, Burrell LM. Angiotensin-(1-7) infusion is associated with increased blood pressure and adverse cardiac remodelling in rats with subtotal nephrectomy. Clin Sci (Lond). 2011;120:335-345.
55. Grobe JL, Mecca AP, Mao H, Katovich MJ. Chronic angiotensin-(1-7) prevents cardiac fbrosis in DOCA-salt model of hypertension. Am J Physiol Heart Circ Physiol. 2006;290:H2417-H2423.
56. Grobe JL, Mecca AP, Lingis M, Shenoy V, Bolton TA, Machado JM, Speth RC, Raizada MK, Katovich MJ. Prevention of angiotensin II-induced cardiac remodeling by angiotensin-(1-7). Am J Physiol Heart Circ Physiol. 2007;292:H736-H742.
57. Simon MA. Assessment and treatment of right ventricular failure. Nat Rev Cardiol. 2013;10:204-218.