Oral delivery of particulate transforming growth factor beta 1 and all-trans retinoic acid reduces gut inflammation in murine models of inflammatory bowel disease

Journal of Crohn's and Colitis

Volumn 9, Issue 8, 2015, Pages 647-658

  Conway, Thomas F ^a,b   Hammer, Laura ^a   Furtado, Stacia ^a,c   Mathiowitz, Edith ^c   Nicoletti, Ferdinando ^d   Mangano, Katia ^d   Egilmez, Nejat K ^a,b   Auci, Dominick L ^a  

^a TherapyX inc   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c BROWN UNIVERSITY   (United States)

^d UNIVERSITY OF CATANIA   (Italy)

Author keywords

ATRA; IBD; TGF

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; MICROSPHERE; POLYGLACTIN; POLYLACTIC ACID; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; RETINOIC ACID; SALAZOSULFAPYRIDINE; SERUM AMYLOID A; TRANSCRIPTION FACTOR FOXP3; ANTIINFLAMMATORY AGENT; BIOLOGICAL MARKER; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; DEXTRAN SODIUM SULFATE-INDUCED COLITIS; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG STABILITY; FEMALE; HISTOLOGY; INFLAMMATORY BOWEL DISEASE; LAMINA PROPRIA; MALE; MOUSE; NANOENCAPSULATION; NANOTECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCID MOUSE; SUSTAINED DRUG RELEASE; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; COMBINATION DRUG THERAPY; DRUG ADMINISTRATION; EVALUATION STUDY; INFLAMMATORY BOWEL DISEASES; INTESTINE MUCOSA; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOLOGY; TREATMENT OUTCOME;

ADMINISTRATION, ORAL; ANIMALS; ANTI-INFLAMMATORY AGENTS; BIOMARKERS; DRUG ADMINISTRATION SCHEDULE; DRUG THERAPY, COMBINATION; FEMALE; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED BALB C; MICE, SCID; MICROSPHERES; TRANSFORMING GROWTH FACTOR BETA; TREATMENT OUTCOME; TRETINOIN;

EID: 84973174752     PISSN: 18739946     EISSN: 18764479     Source Type: Journal    
DOI: 10.1093/ecco-jcc/jjv089     Document Type: Article

References (71)

1. Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med 2009;361:2066-78
2. Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002;347:417-29
3. Kraus S, Arber N. Inflammation and colorectal cancer. Curr Opin Pharmacol 2009;9:405-10
4. Grivennikov SI. Inflammation and colorectal cancer: colitis-associated neoplasia. Semin Immunopathol 2013;35:229-44
5. Risques RA, Lai LA, Himmetoglu C, et al. Ulcerative colitis-associated colorectal cancer arises in a field of short telomeres, senescence, and inflammation. Cancer Res 2011;71:1669-79
6. Podolsky DK. The current future understanding of inflammatory bowel disease. Best Pract Res Clin Gastroenterolpractice & research Clinical gastroenterology 2002;16:933-43
7. Rutgeerts P, Vermeire S, Van Assche G. Biological therapies for inflammatory bowel diseases. Gastroenterology 2009;136:1182-97
8. Neurath MF, Finotto S. Translating inflammatory bowel disease research into clinical medicine. Immunity 2009;31:357-61
9. Cannom RR, Kaiser AM, Ault GT, Beart RW, Jr, Etzioni DA. Inflammatory bowel disease in the United States from 1998 to 2005: has infliximab affected surgical rates? Am Surg 2009;75:976-80
10. Yen D, Cheung J, Scheerens H, et al. IL-23 is essential for T-cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 2006;116:13106
11. Cho JH. The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol 2008;8:458-66
12. Hue S, Ahern P, Buonocore S, et al. Interleukin-23 drives innate and T-cellmediated intestinal inflammation. J Exp Med 2006;203:2473-83
13. Maynard CL, Weaver CT. Intestinal effector T-cells in health and disease. Immunity 2009;31:389-400
14. Izcue A, Coombes JL, Powrie F. Regulatory T-cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol Rev 2006;212:256-71
15. Barnes MJ, Powrie F. Regulatory T-cells reinforce intestinal homeostasis. Immunity 2009;31:401-11
16. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T-cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007;204:1757-64
17. Sun CM, Hall JA, Blank RB, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 2007;204:1775-85
18. Coombes JL, Robinson NJ, Maloy KJ, Uhlig HH, Powrie F. Regulatory T-cells and intestinal homeostasis. Immunol Rev 2005;204:184-94
19. Liu H, Hu B, Xu D, Liew FY. CD4+CD25+ regulatory T-cells cure murine colitis: the role of IL-10, TGF-beta, and CTLA4. J Immunol 2003;171:5012-7
20. Mottet C, Uhlig HH, Powrie F. Cutting edge: cure of colitis by CD4+CD25+ regulatory T-cells. J Immunol 2003;170:3939-43
21. Elias KM, Laurence A, Davidson TS, et al. Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway. Blood 2008;111:1013-20
22. Goldberg M, Gomez-Orellana I. Challenges for the oral delivery of macromolecules. Nat Rev Drug Discov 2003;2:289-95
23. Langer R, Tirrell DA. Designing materials for biology and medicine. Nature 2004;428:487-92
24. Egilmez NK, Kilinc MO, Gu T, Conway TF. Controlled-release particulate cytokine adjuvants for cancer therapy. Endocr Metab Immune Disord Drug Targets 2007;7:266270
25. Mathiowitz E, Jacob JS, Jong YS, et al. Biologically erodable microspheres as potential oral drug delivery systems. Nature 1997;386:410-4
26. Coco R, Plapied L, Pourcelle V, et al. Drug delivery to inflamed colon by nanoparticles: comparison of different strategies. Int J Pharm 2013;440:3-12
27. Jeong YI, Song JG, Kang SS, et al. Preparation of poly[DL-lactide-coglycolide] microspheres encapsulating all-trans retinoic acid. Int J Pharm 2003;259:79-91
28. Egilmez NK, Jong YS, Mathiowitz E, Bankert RB. Tumor vaccination with cytokine-encapsulated microspheres. Methods Mol Med 2003;75:687-96
29. Egilmez NK, Jong YS, Sabel MS, Jacob JS, Mathiowitz E, Bankert RB. In situ tumor vaccination with interleukin-12-encapsulated biodegradable microspheres: induction of tumor regression and potent antitumor immunity. Cancer Res 2000;60:3832-7
30. Berg DJ, Davidson N, Kuhn R, et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4[+] TH1-like responses. J Clin Invest 1996;98:1010-20
31. Gu T, Rowswell-Turner RB, Kilinc MO, Egilmez NK. Central role of IFNgamma-indoleamine 2,3-dioxygenase axis in regulation of interleukin-12-mediated antitumor immunity. Cancer Res 2010;70:129-38
32. Naahidi S, Jafari M, Edalat F, Raymond K, Khademhosseini A, Chen P. Biocompatibility of engineered nanoparticles for drug delivery. J Control Release 2013;166:182-94
33. Chernajovsky Y, Adams G, Triantaphyllopoulos K, Ledda MF, Podhajcer OL. Pathogenic lymphoid cells engineered to express TGF beta 1 ameliorate disease in a collagen-induced arthritis model. Gene Ther 1997;4:553-9
34. Kuruvilla AP, Shah R, Hochwald GM, Liggitt HD, Palladino MA, Thorbecke GJ. Protective effect of transforming growth factor beta 1 on experimental autoimmune diseases in mice. Proc Natl Acad Sci U S A 1991;88:2918-21
35. Moritani M, Yoshimoto K, Wong SF, et al. Abrogation of autoimmune diabetes in nonobese diabetic mice and protection against effector lymphocytes by transgenic paracrine TGF-beta1. J Clin Invest 1998;102:499-506
36. Racke MK, Dhib-Jalbut S, Cannella B, Albert PS, Raine CS, McFarlin DE. Prevention and treatment of chronic relapsing experimental allergic encephalomyelitis by transforming growth factor-beta 1. J Immunol 1991;146:3012-7
37. Prud'homme GJ. Pathobiology of transforming growth factor beta in cancer, fibrosis and immunologic disease, and therapeutic considerations. Lab Invest 2007;87:1077-91
38. Prud'homme GJ, Piccirillo CA. The inhibitory effects of transforming growth factor-beta-1 [TGF-beta1] in autoimmune diseases. J Autoimmun 2000;14:23-42
39. Zhang K, Phan SH. Cytokines and pulmonary fibrosis. Biol Signals 1996;5:232-9
40. Anscher MS, Kong FM, Jirtle RL. The relevance of transforming growth factor beta 1 in pulmonary injury after radiation therapy. Lung Cancer 1998;19:109-20
41. Matrat M, Lardot C, Huaux F, Broeckaert F, Lison D. Role of urokinase in the activation of macrophage-associated TGF-beta in silica-induced lung fibrosis. J Toxicol Environ Health A 1998;55:359-71
42. Zhang JG, Walmsley MW, Moy JV, et al. Differential effects of cyclosporin A and tacrolimus on the production of TGF-beta: implications for the development of obliterative bronchiolitis after lung transplantation. Transpl Int 1998;11[Suppl 1]: S325-7
43. Haustein UF, Anderegg U. Pathophysiology of scleroderma: an update. J Eur Acad Dermatol Venereol 1998;11: 1-8
44. Liem LM, Fibbe WE, van Houwelingen HC, Goulmy E. Serum transforming growth factor-beta1 levels in bone marrow transplant recipients correlate with blood cell counts and chronic graft-versus-host disease. Transplantation 1999;67:59-65
45. Kitamura M, Suto TS. TGF-beta and glomerulonephritis: anti-inflammatory versus prosclerotic actions. Nephrol Dial Transplant 1997;12:669-79
46. Zioncheck TF, Chen SA, Richardson L, et al. Pharmacokinetics and tissue distribution of recombinant human transforming growth factor beta 1 after topical and intravenous administration in male rats. Pharm Res 1994;11:21320
47. Saadeddin A, Torres-Molina F, Carcel-Trullols J, Araico A, Peris JE. Pharmacokinetics of the time-dependent elimination of all-trans-retinoic acid in rats. AAPS PharmSciTech 2004;6:E1
48. Saadeddin A, Torres-Molina F, Carcel-Trullols J, Araico A, Peris JE. Pharmacokinetics of the time-dependent elimination of all-trans-retinoic acid in rats. AAPS J 2004;6:1-9
49. Capurso NA, Look M, Jeanbart L, et al. Development of a nanoparticulate formulation of retinoic acid that suppresses Th17 cells and upregulates regulatory T-cells. Self/nonself 2010;1:335-40
50. Collins CB, Aherne CM, Kominsky D, et al. Retinoic acid attenuates ileitis by restoring the balance between T-helper 17 and T regulatory cells. Gastroenterology 2011;141:1821-31
51. Bai A, Lu N, Zeng H, et al. All-trans retinoic acid ameliorates trinitrobenzene sulfonic acid-induced colitis by shifting Th1 to Th2 profile. J Interferon Cytokine Res 2010;30:399-406
52. Hong K, Zhang Y, Guo Y, et al. All-trans retinoic acid attenuates experimental colitis through inhibition of NF-kappaB signaling. Immunol Lett 2014;162[1 Part A]:34-40
53. Sanders TJ, McCarthy NE, Giles EM, et al. Increased production of retinoic acid by intestinal macrophages contributes to their inflammatory phenotype in patients with Crohn's disease. Gastroenterology 2014;146:1278-88
54. Reddy D, Siegel CA, Sands BE, Kane S. Possible association between isotretinoin and inflammatory bowel disease. Am J Gastroenterol 2006;101:1569-73
55. Crockett SD, Porter CQ, Martin CF, Sandler RS, Kappelman MD. Isotretinoin use and the risk of inflammatory bowel disease: a case-control study. Am J Gastroenterol 2010;105:198693
56. Etminan M, Bird ST, Delaney JA, Bressler B, Brophy JM. Isotretinoin and risk for inflammatory bowel disease: a nested case-control study and meta-analysis of published and unpublished data. JAMA Dermatol 2013;149:216-20
57. Racine A, Cuerq A, Bijon A, et al. Isotretinoin and risk of inflammatory bowel disease: a French nationwide study. Am J Gastroenterol 2014;109:563-9
58. Prevost N, English JC. Isotretinoin: update on controversial issues. J Pediatr Adolesc Gynecol 2013;26:290-3
59. Fenaux P, Le Deley MC, Castaigne S, et al. Effect of all transretinoic acid in newly diagnosed acute promyelocytic leukemia. Results of a multicenter randomized trial. European APL 91 Group. Blood 1993;82:3241-9
60. Tallman MS, Andersen JW, Schiffer CA, et al. All-trans-retinoic acid in acute promyelocytic leukemia. N Engl J Med 1997;337:1021-8
61. Freemantle SJ, Spinella MJ, Dmitrovsky E. Retinoids in cancer therapy and chemoprevention: promise meets resistance. Oncogene 2003,22:7305-15
62. Ozpolat B, Lopez-Berestein G. Liposomal-all-trans-retinoic acid in treatment of acute promyelocytic leukemia. Leuk Lymphoma 2002;43:933-41
63. Wang DL, Marko M, Dahl AR, et al. Topical delivery of 13-cis-retinoic acid by inhalation up-regulates expression of rodent lung but not liver retinoic acid receptors. Clin Cancer Res 2000;6:363645
64. Choi Y, Kim SY, Park K, et al. Chemopreventive efficacy of all-trans-retinoic acid in biodegradable microspheres against epithelial cancers: results in a 4-nitroquinoline 1-oxide-induced oral carcinogenesis model. Int J Pharm 2006;320:45-52
65. Coombes JL, Maloy KJ. Control of intestinal homeostasis by regulatory T-cells and dendritic cells. Semin Immunol 2007;19:116-26
66. Benson MJ, Pino-Lagos K, Rosemblatt M, Noelle RJ. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J Exp Med 2007;204:1765-74
67. Mucida D, Park Y, Kim G, et al. Reciprocal TH17 and regulatory T-cell differentiation mediated by retinoic acid. Science 2007;317:256-60
68. von Boehmer H. Oral tolerance: is it all retinoic acid? J Exp Med 2007;204:1737-9
69. Xiao S, Jin H, Korn T, et al. Retinoic acid increases Foxp3+ regulatory T-cells and inhibits development of Th17 cells by enhancing TGF-betadriven Smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J Immunol 2008;181:2277-84
70. Yamanaka YJ, Leong KW. Engineering strategies to enhance nanoparticlemediated oral delivery. J Biomater Sci Polym Ed 2008;19:1549-70
71. Chung AY, Li Q, Blair SJ, et al. Oral interleukin-10 alleviates polyposis via neutralization of pathogenic T-regulatory cells. Cancer Res 2014;74:5377-85