Advances in oral nano-delivery systems for colon targeted drug delivery in inflammatory bowel disease: Selective targeting to diseased versus healthy tissue

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 11, Issue 5, 2015, Pages 1117-1132

  Hua, Susan ^a   Marks, Ellen ^a,b   Schneider, Jennifer J ^a   Keely, Simon ^a,b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Colitis; Colon targeted drug delivery; Inflammatory bowel disease; Nano delivery systems; Oral administration

Indexed keywords

BIOCHEMISTRY; CONTROLLED DRUG DELIVERY; DISEASES; PHYSIOLOGY; TISSUE;

COLITIS; GASTROINTESTINAL TRACT; INFLAMMATORY BOWEL DISEASE; LOCALIZED TREATMENT; NANO-DELIVERY SYSTEMS; ORAL ADMINISTRATION; SYSTEMIC TOXICITIES; THERAPEUTIC EFFICACY;

TARGETED DRUG DELIVERY;

AMINOSALICYLIC ACID; BUDESONIDE; EUDRAGIT; MACROGOL; NANOPARTICLE; SILICA NANOPARTICLE; SMALL INTERFERING RNA; TACROLIMUS; DRUG; DRUG CARRIER; NANOMATERIAL;

COLITIS; COLON; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; INTESTINE RESECTION; INTESTINE TRANSIT TIME; NANOMEDICINE; OXIDATION REDUCTION REACTION; PARTICLE SIZE; PH; REVIEW; ANIMAL; CHEMISTRY; DRUG EFFECTS; INFLAMMATORY BOWEL DISEASES; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOLOGY; PROCEDURES;

ADMINISTRATION, ORAL; ANIMALS; COLON; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; INFLAMMATORY BOWEL DISEASES; NANOSTRUCTURES; PHARMACEUTICAL PREPARATIONS;

EID: 84931058745     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2015.02.018     Document Type: Review

References (150)

1. Podolsky D.K. Inflammatory bowel disease. N Engl J Med 2002, 347(6):417-429.
2. Sartor R.B. Genetics and environmental interactions shape the intestinal microbiome to promote inflammatory bowel disease versus mucosal homeostasis. Gastroenterology 2010, 139(6):1816-1819.
3. Keely S., Ryan S.M., Haddleton D.M., Limer A., Mantovani G., Murphy E.P., et al. Dexamethasone-pDMAEMA polymeric conjugates reduce inflammatory biomarkers in human intestinal epithelial monolayers. J Control Release 2009, 135(1):35-43.
4. Podolsky D.K. The future of IBD treatment. J Gastroenterol 2003, 38(Suppl. 15):63-66.
5. Talley N.J., Abreu M.T., Achkar J.P., Bernstein C.N., Dubinsky M.C., Hanauer S.B., et al. An evidence-based systematic review on medical therapies for inflammatory bowel disease. Am J Gastroenterol 2011, 106(Suppl. 1):S2-S25. [quiz S6].
6. Byrne C.M., Solomon M.J., Young J.M., Selby W., Harrison J.D. Patient preferences between surgical and medical treatment in Crohn's disease. Dis Colon Rectum 2007, 50(5):586-597.
7. Yang L., Chu J.S., Fix J.A. Colon-specific drug delivery: new approaches and in vitro/in vivo evaluation. Int J Pharm 2002, 235(1-2):1-15.
8. Sandborn W.J. Rational selection of oral 5-aminosalicylate formulations and prodrugs for the treatment of ulcerative colitis. Am J Gastroenterol 2002, 97(12):2939-2941.
9. Hanauer S.B., Sparrow M. COLAL-PRED Alizyme. Curr Opin Investig Drugs 2004, 5(11):1192-1197.
10. Steed K.P., Hooper G., Monti N., Benedetti M.S., Fornasini G., Wilding I.R. The use of pharmacoscintigraphy to focus the development strategy for a novel 5-ASA colon targeting system ("TIME CLOCK (R)" system). J Control Release 1997, 49(2-3):115-122.
11. Hebden J.M., Blackshaw P.E., Perkins A.C., Wilson C.G., Spiller R.C. Limited exposure of the healthy distal colon to orally-dosed formulation is further exaggerated in active left-sided ulcerative colitis. Aliment Pharmacol Ther 2000, 14(2):155-161.
12. Hua S. Orally administered liposomal formulations for colon targeted drug delivery. Front Pharmacol 2014, 5:1-4. [Opinion].
13. Laroui H., Dalmasso G., Nguyen H.T., Yan Y., Sitaraman S.V., Merlin D. Drug-loaded nanoparticles targeted to the colon with polysaccharide hydrogel reduce colitis in a mouse model. Gastroenterology 2010, 138(3):843-853.e1-2.
14. Coco R., Plapied L., Pourcelle V., Jerome C., Brayden D.J., Schneider Y.J., et al. Drug delivery to inflamed colon by nanoparticles: comparison of different strategies. Int J Pharm 2013, 440(1):3-12.
15. Asghar L.F., Chandran S. Multiparticulate formulation approach to colon specific drug delivery: current perspectives. J Pharm Pharm Sci 2006, 9(3):327-338.
16. Hu Z., Mawatari S., Shibata N., Takada K., Yoshikawa H., Arakawa A., et al. Application of a biomagnetic measurement system (BMS) to the evaluation of gastrointestinal transit of intestinal pressure-controlled colon delivery capsules (PCDCs) in human subjects. Pharm Res 2000, 17(2):160-167.
17. Coupe A.J., Davis S.S., Wilding I.R. Variation in gastrointestinal transit of pharmaceutical dosage forms in healthy subjects. Pharm Res 1991, 8(3):360-364.
18. Rao K.A., Yazaki E., Evans D.F., Carbon R. Objective evaluation of small bowel and colonic transit time using pH telemetry in athletes with gastrointestinal symptoms. Br J Sports Med 2004, 38(4):482-487.
19. Buhmann S., Kirchhoff C., Ladurner R., Mussack T., Reiser M.F., Lienemann A. Assessment of colonic transit time using MRI: a feasibility study. Eur Radiol 2007, 17(3):669-674.
20. Sathyan G., Hwang S., Gupta S.K. Effect of dosing time on the total intestinal transit time of non-disintegrating systems. Int J Pharm 2000, 204(1-2):47-51.
21. Fallingborg J., Christensen L.A., Jacobsen B.A., Rasmussen S.N. Very low intraluminal colonic pH in patients with active ulcerative colitis. Dig Dis Sci 1993, 38(11):1989-1993.
22. Bratten J., Jones M.P. New directions in the assessment of gastric function: clinical applications of physiologic measurements. Dig Dis 2006, 24(3-4):252-259.
23. Nugent S.G., Kumar D., Rampton D.S., Evans D.F. Intestinal luminal pH in inflammatory bowel disease: possible determinants and implications for therapy with aminosalicylates and other drugs. Gut 2001, 48(4):571-577.
24. Sasaki Y., Hada R., Nakajima H., Fukuda S., Munakata A. Improved localizing method of radiopill in measurement of entire gastrointestinal pH profiles: colonic luminal pH in normal subjects and patients with Crohn's disease. Am J Gastroenterol 1997, 92(1):114-118.
25. Ibekwe V.C., Fadda H.M., McConnell E.L., Khela M.K., Evans D.F., Basit A.W. Interplay between intestinal pH, transit time and feed status on the in vivo performance of pH responsive ileo-colonic release systems. Pharm Res 2008, 25(8):1828-1835.
26. Nyhof R.A., Ingold-Wilcox D., Chou C.C. Effect of atropine on digested food-induced intestinal hyperemia. Am J Physiol 1985, 249(6 Pt 1):G685-G690.
27. Fatouros D.G., Mullertz A. In vitro lipid digestion models in design of drug delivery systems for enhancing oral bioavailability. Expert Opin Drug Metab Toxicol 2008, 4(1):65-76.
28. Keely S., Feighery L., Campion D.P., O'Brien L., Brayden D.J., Baird A.W. Chloride-led disruption of the intestinal mucous layer impedes Salmonella invasion: evidence for an 'enteric tear' mechanism. Cell Physiol Biochem 2011, 28(4):743-752.
29. Sartor R.B. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008, 134(2):577-594.
30. Macfarlane G.T., Macfarlane S. Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics. J Clin Gastroenterol 2011, 45:S120-S127. [Suppl.].
31. Sinha V.R., Kumria R. Polysaccharides in colon-specific drug delivery. Int J Pharm 2001, 224(1-2):19-38.
32. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007, 104(34):13780-13785.
33. Albenberg L.G., Wu G.D. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 2014, 146(6):1564-1572.
34. Britton R.A., Young V.B. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 2014, 146(6):1547-1553.
35. Patel S., McCormick B.A. Mucosal inflammatory response to Salmonella typhimurium infection. Front Immunol 2014, 5:311.
36. Grover M., Kanazawa M., Palsson O.S., Chitkara D.K., Gangarosa L.M., Drossman D.A., et al. Small intestinal bacterial overgrowth in irritable bowel syndrome: association with colon motility, bowel symptoms, and psychological distress. Neurogastroenterol Motil 2008, 20(9):998-1008.
37. Li A.C., Thompson R.P. Basement membrane components. J Clin Pathol 2003, 56(12):885-887.
38. Antoni L., Nuding S., Wehkamp J., Stange E.F. Intestinal barrier in inflammatory bowel disease. World J Gastroenterol 2014, 20(5):1165-1179.
39. Rana S.V., Sharma S., Malik A., Kaur J., Prasad K.K., Sinha S.K., et al. Small intestinal bacterial overgrowth and orocecal transit time in patients of inflammatory bowel disease. Dig Dis Sci 2013, 58(9):2594-2598.
40. Kashyap P.C., Marcobal A., Ursell L.K., Larauche M., Duboc H., Earle K.A., et al. Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. Gastroenterology 2013, 144(5):967-977.
41. Sartor R.B. Therapeutic correction of bacterial dysbiosis discovered by molecular techniques. Proc Natl Acad Sci U S A 2008, 105(43):16413-16414.
42. Linskens R.K., Huijsdens X.W., Savelkoul P.H., Vandenbroucke-Grauls C.M., Meuwissen S.G. The bacterial flora in inflammatory bowel disease: current insights in pathogenesis and the influence of antibiotics and probiotics. Scand J Gastroenterol Suppl 2001, 234:29-40.
43. Keely S., Kelly C.J., Weissmueller T., Burgess A., Wagner B.D., Robertson C.E., et al. Activated fluid transport regulates bacterial-epithelial interactions and significantly shifts the murine colonic microbiome. Gut Microbes 2012, 3(3):250-260.
44. Musch M.W., Wang Y., Claud E.C., Chang E.B. Lubiprostone decreases mouse colonic inner mucus layer thickness and alters intestinal microbiota. Dig Dis Sci 2013, 58(3):668-677.
45. Barkas F., Liberopoulos E., Kei A., Elisaf M. Electrolyte and acid-base disorders in inflammatory bowel disease. Ann Gastroenterol 2013, 26(1):23-28.
46. Lucas M.L., Cooper B.T., Lei F.H., Johnson I.T., Holmes G.K., Blair J.A., et al. Acid microclimate in coeliac and Crohn's disease: a model for folate malabsorption. Gut 1978, 19(8):735-742.
47. McConnell E.L., Fadda H.M., Basit A.W. Gut instincts: explorations in intestinal physiology and drug delivery. Int J Pharm 2008, 364(2):213-226.
48. Van Citters G.W., Lin H.C. Ileal brake: neuropeptidergic control of intestinal transit. Curr Gastroenterol Rep 2006, 8(5):367-373.
49. Yang L. Biorelevant dissolution testing of colon-specific delivery systems activated by colonic microflora. J Control Release 2008, 125(2):77-86.
50. Laukoetter M.G., Nava P., Nusrat A. Role of the intestinal barrier in inflammatory bowel disease. World J Gastroenterol 2008, 14(3):401-407.
51. Cunningham K.E., Turner J.R. Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann N Y Acad Sci 2012, 1258:34-42.
52. Wang X., Maher S., Brayden D.J. Restoration of rat colonic epithelium after in situ intestinal instillation of the absorption promoter, sodium caprate. Ther Deliv 2010, 1(1):75-82.
53. Goggins B.J., Chaney C., Radford-Smith G.L., Horvat J.C., Keely S. Hypoxia and integrin-mediated epithelial restitution during mucosal inflammation. Front Immunol 2013, 4:272.
54. Comerford K.M., Wallace T.J., Karhausen J., Louis N.A., Montalto M.C., Colgan S.P. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res 2002, 62(12):3387-3394.
55. Creed T.J., Probert C.S. Review article: steroid resistance in inflammatory bowel disease-mechanisms and therapeutic strategies. Aliment Pharmacol Ther 2007, 25(2):111-122.
56. Dong X., Mattingly C.A., Tseng M.T., Cho M.J., Liu Y., Adams V.R., et al. Doxorubicin and paclitaxel-loaded lipid-based nanoparticles overcome multidrug resistance by inhibiting P-glycoprotein and depleting ATP. Cancer Res 2009, 69(9):3918-3926.
57. Schmidt T., Pfeiffer A., Hackelsberger N., Widmer R., Meisel C., Kaess H. Effect of intestinal resection on human small bowel motility. Gut 1996, 38(6):859-863.
58. Spiller R.C., Trotman I.F., Adrian T.E., Bloom S.R., Misiewicz J.J., Silk D.B. Further characterisation of the 'ileal brake' reflex in man-effect of ileal infusion of partial digests of fat, protein, and starch on jejunal motility and release of neurotensin, enteroglucagon, and peptide YY. Gut 1988, 29(8):1042-1051.
59. Fallingborg J., Pedersen P., Jacobsen B.A. Small intestinal transit time and intraluminal pH in ileocecal resected patients with Crohn's disease. Dig Dis Sci 1998, 43(4):702-705.
60. Gracie D.J., Kane J.S., Mumtaz S., Scarsbrook A.F., Chowdhury F.U., Ford A.C. Prevalence of, and predictors of, bile acid malabsorption in outpatients with chronic diarrhea. Neurogastroenterol Motil 2012, 24(11):983-e538.
61. Thompson J.S., Quigley E.M., Adrian T.E., Path F.R. Role of the ileocecal junction in the motor response to intestinal resection. J Gastrointest Surg 1998, 2(2):174-185.
62. Ammon H.V., Phillips S.F. Inhibition of ileal water absorption by intraluminal fatty acids. Influence of chain length, hydroxylation, and conjugation of fatty acids. J Clin Invest 1974, 53(1):205-210.
63. Watts P.J., Barrow L., Steed K.P., Wilson C.G., Spiller R.C., Melia C.D., et al. The transit rate of different-sized model dosage forms through the human colon and the effects of a lactulose-induced catharsis. Int J Pharm 1992, 87:215-221.
64. Van Citters G.W., Lin H.C. The ileal brake: a fifteen-year progress report. Curr Gastroenterol Rep 1999, 1(5):404-409.
65. Lin H.C., Prather C., Fisher R.S., Meyer J.H., Summers R.W., Pimentel M., et al. Measurement of gastrointestinal transit. Dig Dis Sci 2005, 50(6):989-1004.
66. Malayandi R., Kondamudi P.K., Ruby P.K., Aggarwal D. Biopharmaceutical considerations and characterizations in development of colon targeted dosage forms for inflammatory bowel disease. Drug Deliv Transl Res 2014, 4:187-202.
67. Xiao B., Merlin D. Oral colon-specific therapeutic approaches toward treatment of inflammatory bowel disease. Expert Opin Drug Deliv 2012, 9(11):1393-1407.
68. Collnot E.M., Ali H., Lehr C.M. Nano- and microparticulate drug carriers for targeting of the inflamed intestinal mucosa. J Control Release 2012, 161(2):235-246.
69. Lamprecht A., Yamamoto H., Takeuchi H., Kawashima Y. Nanoparticles enhance therapeutic efficiency by selectively increased local drug dose in experimental colitis in rats. J Pharmacol Exp Ther 2005, 315(1):196-202.
70. Beloqui A., Coco R., Alhouayek M., Solinis M.A., Rodriguez-Gascon A., Muccioli G.G., et al. Budesonide-loaded nanostructured lipid carriers reduce inflammation in murine DSS-induced colitis. Int J Pharm 2013, 454(2):775-783.
71. Hillyer J.F., Albrecht R.M. Gastrointestinal persorption and tissue distribution of differently sized colloidal gold nanoparticles. J Pharm Sci 2001, 90(12):1927-1936.
72. des Rieux A., Ragnarsson E.G., Gullberg E., Preat V., Schneider Y.J., Artursson P. Transport of nanoparticles across an in vitro model of the human intestinal follicle associated epithelium. Eur J Pharm Sci 2005, 25(4-5):455-465.
73. Pichai M.V., Ferguson L.R. Potential prospects of nanomedicine for targeted therapeutics in inflammatory bowel diseases. World J Gastroenterol 2012, 18(23):2895-2901.
74. Lamprecht A., Schäfer U., Lehr C.-M. Size-dependent bioadhesion of micro- and nanoparticulate carriers to the inflamed colonic mucosa. Pharm Res 2001, 18(6):788-793.
75. Lamprecht A. IBD: selective nanoparticle adhesion can enhance colitis therapy. Nat Rev Gastroenterol Hepatol 2010, 7(6):311-312.
76. Wachsmann P., Moulari B., Beduneau A., Pellequer Y., Lamprecht A. Surfactant-dependence of nanoparticle treatment in murine experimental colitis. J Control Release 2013, 172(1):62-68.
77. Schmidt C., Lautenschlaeger C., Collnot E.M., Schumann M., Bojarski C., Schulzke J.D., et al. Nano- and microscaled particles for drug targeting to inflamed intestinal mucosa: a first in vivo study in human patients. J Control Release 2013, 165(2):139-145.
78. Han H.K., Shin H.J., Ha D.H. Improved oral bioavailability of alendronate via the mucoadhesive liposomal delivery system. Eur J Pharm Sci 2012, 46(5):500-507.
79. Liu L., Fishman M.L., Hicks K.B., Kende M. Interaction of various pectin formulations with porcine colonic tissues. Biomaterials 2005, 26(29):5907-5916.
80. Larsson J.M., Karlsson H., Sjovall H., Hansson G.C. A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nanoLC/MSn. Glycobiology 2009, 19(7):756-766.
81. Urayama S., Chang E.B. Mechanisms and treatment of diarrhea in inflammatory bowel diseases. Inflamm Bowel Dis 1997, 3(2):114-131.
82. Niebel W., Walkenbach K., Beduneau A., Pellequer Y., Lamprecht A. Nanoparticle-based clodronate delivery mitigates murine experimental colitis. J Control Release 2012, 160(3):659-665.
83. Lautenschlager C., Schmidt C., Lehr C.M., Fischer D., Stallmach A. PEG-functionalized microparticles selectively target inflamed mucosa in inflammatory bowel disease. Eur J Pharm Biopharm 2013, 85(3 Pt A):578-586.
84. Gradauer K., Barthelmes J., Vonach C., Almer G., Mangge H., Teubl B., et al. Liposomes coated with thiolated chitosan enhance oral peptide delivery to rats. J Control Release 2013, 172(3):872-878.
85. Manconi M., Nacher A., Merino V., Merino-Sanjuan M., Manca M.L., Mura C., et al. Improving oral bioavailability and pharmacokinetics of liposomal metformin by glycerolphosphate-chitosan microcomplexation. AAPS PharmSciTech 2013, 14(2):485-496.
86. Takeuchi H., Matsui Y., Yamamoto H., Kawashima Y. Mucoadhesive properties of carbopol or chitosan-coated liposomes and their effectiveness in the oral administration of calcitonin to rats. J Control Release 2003, 86(2-3):235-242.
87. Gradauer K., Vonach C., Leitinger G., Kolb D., Frohlich E., Roblegg E., et al. Chemical coupling of thiolated chitosan to preformed liposomes improves mucoadhesive properties. Int J Nanomedicine 2012, 7:2523-2534.
88. Thirawong N., Thongborisute J., Takeuchi H., Sriamornsak P. Improved intestinal absorption of calcitonin by mucoadhesive delivery of novel pectin-liposome nanocomplexes. J Control Release 2008, 125(3):236-245.
89. Tirosh B., Khatib N., Barenholz Y., Nissan A., Rubinstein A. Transferrin as a luminal target for negatively charged liposomes in the inflamed colonic mucosa. Mol Pharm 2009, 6(4):1083-1091.
90. Carlson M., Raab Y., Peterson C., Hallgren R., Venge P. Increased intraluminal release of eosinophil granule proteins EPO, ECP, EPX, and cytokines in ulcerative colitis and proctitis in segmental perfusion. Am J Gastroenterol 1999, 94(7):1876-1883.
91. Peterson C.G., Eklund E., Taha Y., Raab Y., Carlson M. A new method for the quantification of neutrophil and eosinophil cationic proteins in feces: establishment of normal levels and clinical application in patients with inflammatory bowel disease. Am J Gastroenterol 2002, 97(7):1755-1762.
92. Lamprecht A., Ubrich N., Yamamoto H., Schafer U., Takeuchi H., Maincent P., et al. Biodegradable nanoparticles for targeted drug delivery in treatment of inflammatory bowel disease. J Pharmacol Exp Ther 2001, 299(2):775-781.
93. Jubeh T., Barenholz Y., Rubinstein A. Differential adhesion of normal and inflamed rat colonic mucosa by charged liposomes. Pharm Res 2004, 21(3):447-453.
94. Muchow M., Maincent P., Muller R.H. Lipid nanoparticles with a solid matrix (SLN, NLC, LDC) for oral drug delivery. Drug Dev Ind Pharm 2008, 34(12):1394-1405.
95. Beloqui A., Solinis M.A., Delgado A., Evora C., Isla A., Rodriguez-Gascon A. Fate of nanostructured lipid carriers (NLCs) following the oral route: design, pharmacokinetics and biodistribution. J Microencapsul 2014, 31(1):1-8.
96. Meissner Y., Pellequer Y., Lamprecht A. Nanoparticles in inflammatory bowel disease: particle targeting versus pH-sensitive delivery. Int J Pharm 2006, 316(1-2):138-143.
97. Cu Y., Saltzman W.M. Controlled surface modification with poly(ethylene) glycol enhances diffusion of PLGA nanoparticles in human cervical mucus. Mol Pharm 2008, 6:173-181.
98. Tang B.C., Dawson M., Lai S.K., Wang Y.Y., Suk J.S., Yang M., et al. Biodegradable polymer nanoparticles that rapidly penetrate the human mucus barrier. Proc Natl Acad Sci U S A 2009, 106(46):19268-19273.
99. Lai S.K., Wang Y.Y., Hanes J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv Drug Deliv Rev 2009, 61(2):158-171.
100. Vong L.B., Tomita T., Yoshitomi T., Matsui H., Nagasaki Y. An orally administered redox nanoparticle that accumulates in the colonic mucosa and reduces colitis in mice. Gastroenterology 2012, 143(4):1027-1036.e3.
101. Ju J., Hao X., Lee M.J., Lambert J.D., Lu G., Xiao H., et al. A gamma-tocopherol-rich mixture of tocopherols inhibits colon inflammation and carcinogenesis in azoxymethane and dextran sulfate sodium-treated mice. Cancer Prev Res (Phila) 2009, 2(2):143-152.
102. Jin Y., Kotakadi V.S., Ying L., Hofseth A.B., Cui X., Wood P.A., et al. American ginseng suppresses inflammation and DNA damage associated with mouse colitis. Carcinogenesis 2008, 29(12):2351-2359.
103. Kotakadi V.S., Jin Y., Hofseth A.B., Ying L., Cui X., Volate S., et al. Ginkgo biloba extract EGb 761 has anti-inflammatory properties and ameliorates colitis in mice by driving effector T cell apoptosis. Carcinogenesis 2008, 29(9):1799-1806.
104. Tobio M., Sanchez A., Vila A., Soriano I.I., Evora C., Vila-Jato J.L., et al. The role of PEG on the stability in digestive fluids and in vivo fate of PEG-PLA nanoparticles following oral administration. Colloids Surf B: Biointerfaces 2000, 18(3-4):315-323.
105. Ashford M., Fell J.T., Attwood D., Sharma H., Woodhead P.J. An in vivo investigation into the suitability of pH dependent polymers for colonic targeting. Int J Pharm 1993, 95(1-3):193-199.
106. Karn P.R., Vanić Z., Pepić I., Škalko-Basnet N. Mucoadhesive liposomal delivery systems: the choice of coating material. Drug Dev Ind Pharm 2011, 37(4):482-488.
107. Haznedar S., Dortunc B. Preparation and in vitro evaluation of Eudragit microspheres containing acetazolamide. Int J Pharm 2004, 269(1):131-140.
108. Barea M.J., Jenkins M.J., Lee Y.S., Johnson P., Bridson R.H. Encapsulation of liposomes within pH responsive microspheres for oral colonic drug delivery. Int J Biomater 2012, 1-8. [458712].
109. Barea M.J., Jenkins M.J., Gaber M.H., Bridson R.H. Evaluation of liposomes coated with a pH responsive polymer. Int J Pharm 2010, 402(1-2):89-94.
110. Makhlof A., Tozuka Y., Takeuchi H. pH-Sensitive nanospheres for colon-specific drug delivery in experimentally induced colitis rat model. Eur J Pharm Biopharm 2009, 72(1):1-8.
111. Kshirsagar S.J., Bhalekar M.R., Patel J.N., Mohapatra S.K., Shewale N.S. Preparation and characterization of nanocapsules for colon-targeted drug delivery system. Pharm Dev Technol 2012, 17(5):607-613.
112. Legrand P., Barratt G., Mosqueira V., Fessi H., Devissaguet J.P. Polymeric nanocapsules as drug delivery systems. STP Pharm Sci 1999, 9:411-418.
113. Ali H., Weigmann B., Neurath M.F., Collnot E.M., Windbergs M., Lehr C.M. Budesonide loaded nanoparticles with pH-sensitive coating for improved mucosal targeting in mouse models of inflammatory bowel diseases. J Control Release 2014, 183:167-177.
114. Beloqui A., Coco R., Memvanga P.B., Ucakar B., des Rieux A., Preat V. pH-sensitive nanoparticles for colonic delivery of curcumin in inflammatory bowel disease. Int J Pharm 2014, 473(1-2):203-212.
115. Lamprecht A., Yamamoto H., Takeuchi H., Kawashima Y. A pH-sensitive microsphere system for the colon delivery of tacrolimus containing nanoparticles. J Control Release 2005, 104(2):337-346.
116. Laroui H., Geem D., Xiao B., Viennois E., Rakhya P., Denning T., et al. Targeting intestinal inflammation with CD98 siRNA/PEI-loaded nanoparticles. Mol Ther 2014, 22(1):69-80.
117. Xiao B., Laroui H., Viennois E., Ayyadurai S., Charania M.A., Zhang Y., et al. Nanoparticles with surface antibody against CD98 and carrying CD98 small interfering RNA reduce colitis in mice. Gastroenterology 2014, 146(5):1289-1300.e1-19.
118. Kriegel C., Amiji M. Oral TNF-alpha gene silencing using a polymeric microsphere-based delivery system for the treatment of inflammatory bowel disease. J Control Release 2011, 150(1):77-86.
119. Kriegel C., Amiji M.M. Dual TNF-alpha/cyclin D1 gene silencing with an oral polymeric microparticle system as a novel strategy for the treatment of inflammatory bowel disease. Clin Transl Gastroenterol 2011, 2:e2.
120. Bhavsar M.D., Amiji M.M. Gastrointestinal distribution and in vivo gene transfection studies with nanoparticles-in-microsphere oral system (NiMOS). J Control Release 2007, 119(3):339-348.
121. Moulari B., Pertuit D., Pellequer Y., Lamprecht A. The targeting of surface modified silica nanoparticles to inflamed tissue in experimental colitis. Biomaterials 2008, 29(34):4554-4560.
122. Li Z.Z., Wen L.X., Shao L., Chen J.F. Fabrication of porous hollow silica nanoparticles and their applications in drug release control. J Control Release 2004, 98(2):245-254.
123. Lih-Brody L., Powell S.R., Collier K.P., Reddy G.M., Cerchia R., Kahn E., et al. Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease. Dig Dis Sci 1996, 41(10):2078-2086.
124. Simmonds N.J., Allen R.E., Stevens T.R., Van Someren R.N., Blake D.R., Rampton D.S. Chemiluminescence assay of mucosal reactive oxygen metabolites in inflammatory bowel disease. Gastroenterology 1992, 103(1):186-196.
125. Mahida Y.R., Wu K.C., Jewell D.P. Respiratory burst activity of intestinal macrophages in normal and inflammatory bowel disease. Gut 1989, 30(10):1362-1370.
126. Wilson D.S., Dalmasso G., Wang L., Sitaraman S.V., Merlin D., Murthy N. Orally delivered thioketal nanoparticles loaded with TNF-alpha-siRNA target inflammation and inhibit gene expression in the intestines. Nat Mater 2010, 9(11):923-928.
127. Leirdal M., Sioud M. Gene silencing in mammalian cells by preformed small RNA duplexes. Biochem Biophys Res Commun 2002, 295(3):744-748.
128. Zhang S., Zhao B., Jiang H., Wang B., Ma B. Cationic lipids and polymers mediated vectors for delivery of siRNA. J Control Release 2007, 123(1):1-10.
129. Thiele L., Rothen-Rutishauser B., Jilek S., Wunderli-Allenspach H., Merkle H.P., Walter E. Evaluation of particle uptake in human blood monocyte-derived cells in vitro. Does phagocytosis activity of dendritic cells measure up with macrophages?. J Control Release 2001, 76(1-2):59-71.
130. Hua S. Targeting sites of inflammation: intercellular adhesion molecule-1 as a target for novel inflammatory therapies. Front Pharmacol 2013, 4:127.
131. Sofou S., Sgouros G. Antibody-targeted liposomes in cancer therapy and imaging. Expert Opin Drug Deliv 2008, 5(2):189-204.
132. Willis M., Forssen E. Ligand-targeted liposomes. Adv Drug Deliv Rev 1998, 29(3):249-271.
133. Saltzman W.M., Radomsky M.L., Whaley K.J., Cone R.A. Antibody diffusion in human cervical mucus. Biophys J 1994, 66(2 Pt 1):508-515.
134. Mane V., Muro S. Biodistribution and endocytosis of ICAM-1-targeting antibodies versus nanocarriers in the gastrointestinal tract in mice. Int J Nanomedicine 2012, 7:4223-4237.
135. Sans M., Panes J., Ardite E., Elizalde J.I., Arce Y., Elena M., et al. VCAM-1 and ICAM-1 mediate leukocyte-endothelial cell adhesion in rat experimental colitis. Gastroenterology 1999, 116(4):874-883.
136. Danese S., Semeraro S., Marini M., Roberto I., Armuzzi A., Papa A., et al. Adhesion molecules in inflammatory bowel disease: therapeutic implications for gut inflammation. Dig Liver Dis 2005, 37(11):811-818.
137. Binion D.G., West G.A., Volk E.E., Drazba J.A., Ziats N.P., Petras R.E., et al. Acquired increase in leucocyte binding by intestinal microvascular endothelium in inflammatory bowel disease. Lancet 1998, 352(9142):1742-1746.
138. Binion D.G., West G.A., Ina K., Ziats N.P., Emancipator S.N., Fiocchi C. Enhanced leukocyte binding by intestinal microvascular endothelial cells in inflammatory bowel disease. Gastroenterology 1997, 112(6):1895-1907.
139. Bernstein C.N., Sargent M., Gallatin W.M., Wilkins J. Beta 2-integrin/intercellular adhesion molecule (ICAM) expression in the normal human intestine. Clin Exp Immunol 1996, 106(1):160-169.
140. Salmi M., Granfors K., MacDermott R., Jalkanen S. Aberrant binding of lamina propria lymphocytes to vascular endothelium in inflammatory bowel diseases. Gastroenterology 1994, 106(3):596-605.
141. Wileman T.E., Lennartz M.R., Stahl P.D. Identification of the macrophage mannose receptor as a 175-kDa membrane protein. Proc Natl Acad Sci U S A 1986, 83(8):2501-2505.
142. van Vliet S.J., Saeland E., van Kooyk Y. Sweet preferences of MGL: carbohydrate specificity and function. Trends Immunol 2008, 29(2):83-90.
143. Xiao B., Laroui H., Ayyadurai S., Viennois E., Charania M.A., Zhang Y., et al. Mannosylated bioreducible nanoparticle-mediated macrophage-specific TNF-alpha RNA interference for IBD therapy. Biomaterials 2013, 34(30):7471-7482.
144. Zhang J., Tang C., Yin C. Galactosylated trimethyl chitosan-cysteine nanoparticles loaded with Map4k4 siRNA for targeting activated macrophages. Biomaterials 2013, 34(14):3667-3677.
145. Laroui H., Viennois E., Xiao B., Canup B.S., Geem D., Denning T.L., et al. Fab'-bearing siRNA TNFalpha-loaded nanoparticles targeted to colonic macrophages offer an effective therapy for experimental colitis. J Control Release 2014, 186:41-53.
146. Tacchini L., Gammella E., De Ponti C., Recalcati S., Cairo G. Role of HIF-1 and NF-kappaB transcription factors in the modulation of transferrin receptor by inflammatory and anti-inflammatory signals. J Biol Chem 2008, 283(30):20674-20686.
147. Harel E., Rubinstein A., Nissan A., Khazanov E., Nadler Milbauer M., Barenholz Y., et al. Enhanced transferrin receptor expression by proinflammatory cytokines in enterocytes as a means for local delivery of drugs to inflamed gut mucosa. PLoS One 2011, 6(9):e24202.
148. Xiao B., Yang Y., Viennois E., Zhang Y., Ayyadurai S., Baker M., et al. Glycoprotein CD98 as a receptor for colitis-targeted delivery of nanoparticle. J Mater Chem B Mater Biol Med 2014, 2(11):1499-1508.
149. Kucharzik T., Lugering A., Yan Y., Driss A., Charrier L., Sitaraman S., et al. Activation of epithelial CD98 glycoprotein perpetuates colonic inflammation. Lab Invest 2005, 85(7):932-941.
150. Nguyen H.T., Merlin D. Homeostatic and innate immune responses: role of the transmembrane glycoprotein CD98. Cell Mol Life Sci 2012, 69(18):3015-3026.