Relative vascular permeability and vascularity across different regions of the rat nasal mucosa: Implications for nasal physiology and drug delivery

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kumar, Niyanta N ^a   Gautam, Mohan ^a   Lochhead, Jeffrey J ^a   Wolak, Daniel J ^a   Ithapu, Vamsi ^b   Singh, Vikas ^b   Thorne, Robert G ^a,c,d  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin   (United States)

^c University of Wisconsin Health   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE SERUM ALBUMIN; DRUG; TEXAS RED; XANTHENE DERIVATIVE;

ANIMAL; AREA UNDER THE CURVE; CAPILLARY PERMEABILITY; CHEMISTRY; DIFFUSION; DRUG DELIVERY SYSTEM; FEMALE; FLUORESCENCE IMAGING; HYDRODYNAMICS; INTRANASAL DRUG ADMINISTRATION; LYMPH NODE; METABOLISM; NOSE MUCOSA; OLFACTORY MUCOSA; RAT; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ADMINISTRATION, INTRANASAL; ANIMALS; AREA UNDER CURVE; CAPILLARY PERMEABILITY; DIFFUSION; DRUG DELIVERY SYSTEMS; FEMALE; HYDRODYNAMICS; LYMPH NODES; NASAL MUCOSA; OLFACTORY MUCOSA; OPTICAL IMAGING; PHARMACEUTICAL PREPARATIONS; RATS; RATS, SPRAGUE-DAWLEY; SERUM ALBUMIN, BOVINE; XANTHENES;

EID: 84984608909     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep31732     Document Type: Article

References (55)

1. Patton, J. S. & Byron, P. R. Inhaling medicines: delivering drugs to the body through the lungs. Nat Rev Drug Discov 6, 67-74 (2007).
2. Lochhead, J. J. & Torne, R. G. Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev 64, 614-628 (2012).
3. Lochhead, J. & Torne, R. In Drug delivery to the brain-Physiological concepts, Methodologies and Approaches. Advances in the Pharmaceutical Sciences (eds Hammarlund-Udenaes, de Lange & Torne) Ch. 14, 401-431 (Springer, 2014).
4. Henkin, R. I. Intranasal delivery to the brain. Nat Biotechnol 29, 480 (2011).
5. Born, J. et al. Snifng neuropeptides: a transnasal approach to the human brain. Nat Neurosci 5, 514-516 (2002).
6. Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U. & Fehr, E. Oxytocin increases trust in humans. Nature 435, 673-676 (2005).
7. Scafdi, J. et al. Intranasal epidermal growth factor treatment rescues neonatal brain injury. Nature 506, 230-234 (2014).
8. Torne, R. G., Pronk, G. J., Padmanabhan, V. & Frey, W. H. Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 127, 481-496 (2004).
9. Torne, R. G., Hanson, L. R., Ross, T. M., Tung, D. & Frey, W. H. Delivery of interferon-beta to the monkey nervous system following intranasal administration. Neuroscience 152, 785-797 (2008).
10. Renner, D. B., Frey, W. H. & Hanson, L. R. Intranasal delivery of siRNA to the olfactory bulbs of mice via the olfactory nerve pathway. Neurosci Lett 513, 193-197 (2012).
11. Han, I. K. et al. Enhanced brain targeting efciency of intranasally administered plasmid DNA: an alternative route for brain gene therapy. J Mol Med (Berl) 85, 75-83 (2007).
12. Lochhead, J. J., Wolak, D. J., Pizzo, M. E. & Torne, R. G. Rapid transport within cerebral perivascular spaces underlies widespread tracer distribution in the brain afer intranasal administration. J Cereb Blood Flow Metab 35, 371-381 (2015).
13. Dhuria, S. V., Hanson, L. R. & Frey, W. H. Novel vasoconstrictor formulation to enhance intranasal targeting of neuropeptide therapeutics to the central nervous system. J Pharmacol Exp Ter 328, 312-320 (2009).
14. Harkema, J. R., Carey, S. A. & Wagner, J. G. The nose revisited: a brief review of the comparative structure, function, and toxicologic pathology of the nasal epithelium. Toxicol Pathol 34, 252-269 (2006).
15. Lundblad, L., Saria, A., Lundberg, J. M. & Anggård, A. Increased vascular permeability in rat nasal mucosa induced by substance P and stimulation of capsaicin-sensitive trigeminal neurons. Acta Otolaryngol 96, 479-484 (1983).
16. Petersson, G., Bacci, E., McDonald, D. M. & Nadel, J. A. Neurogenic plasma extravasation in the rat nasal mucosa is potentiated by peptidase inhibitors. J Pharmacol Exp Ter 264, 509-514 (1993).
17. Wolburg, H. et al. Epithelial and endothelial barriers in the olfactory region of the nasal cavity of the rat. Histochem Cell Biol 130, 127-140 (2008).
18. Garcia de la Torre, J. Hydration from hydrodynamics. General considerations and applications of bead modelling to globular proteins. Biophys Chem 93, 159-170 (2001).
19. Pappenheimer, J. R., Renkin, E. M. & Borrero, L. M. Filtration, difusion and molecular sieving through peripheral capillary membranes; a contribution to the pore theory of capillary permeability. Am J Physiol 167, 13-46 (1951).
20. Grotte, G. Passage of dextran molecules across the blood-lymph barrier. Acta Chir Scand Suppl 211, 1-84 (1956).
21. Wasserman, K. & Mayerson, H. S. Dynamics of lymph and plasma protein exchange. Cardiologia 21, 296-307 (1952).
22. Deen, W. M. Hindered transport of large molecules in liquid-flled pores. AiChe Journal 33, 1409-1425 (1987).
23. Caulfeld, J. P. & Farquhar, M. G. The permeability of glomerular capillaries to graded dextrans. Identifcation of the basement membrane as the primary fltration barrier. J Cell Biol 63, 883-903 (1974).
24. Simionescu, N., Simionescu, M. & Palade, G. E. Permeability of intestinal capillaries. Pathway followed by dextrans and glycogens. J Cell Biol 53, 365-392 (1972).
25. Simionescu, N. & Palade, G. E. Dextrans and glycogens as particulate tracers for studying capillary permeability. J Cell Biol 50, 616-624 (1971).
26. Nicholson, C. & Tao, L. Hindered difusion of high molecular weight compounds in brain extracellular microenvironment measured with integrative optical imaging. Biophys J 65, 2277-2290 (1993).
27. Wolak, D. J., Pizzo, M. E. & Torne, R. G. Probing the extracellular difusion of antibodies in brain using in vivo integrative optical imaging and ex vivo fuorescence imaging. J Control Release 197, 78-86 (2015).
28. Torne, R. G. & Nicholson, C. In vivo difusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc Natl Acad Sci USA 103, 5567-5572 (2006).
29. Torne, R. G., Lakkaraju, A., Rodriguez-Boulan, E. & Nicholson, C. In vivo difusion of lactoferrin in brain extracellular space is regulated by interactions with heparan sulfate. Proc Natl Acad Sci USA 105, 8416-8421 (2008).
30. Torne, R. G., Hrabetová, S. & Nicholson, C. Difusion of epidermal growth factor in rat brain extracellular space measured by integrative optical imaging. J Neurophysiol 92, 3471-3481 (2004).
31. Tao, L. & Nicholson, C. Difusion of albumins in rat cortical slices and relevance to volume transmission. Neuroscience 75, 839-847 (1996).
32. Xiao, F., Nicholson, C., Hrabe, J. & Hrabetová, S. Difusion of fexible random-coil dextran polymers measured in anisotropic brain extracellular space by integrative optical imaging. Biophys J 95, 1382-1392 (2008).
33. Mery, S., Gross, E. A., Joyner, D. R., Godo, M. & Morgan, K. T. Nasal diagrams: a tool for recording the distribution of nasal lesions in rats and mice. Toxicol Pathol 22, 353-372 (1994).
34. Kiyono, H. & Fukuyama, S. NALT-versus Peyer's-patch-mediated mucosal immunity. Nat Rev Immunol 4, 699-710 (2004).
35. Saunders, N. R., Dziegielewska, K. M., Møllgård, K. & Habgood, M. D. Markers for blood-brain barrier integrity: how appropriate is Evans blue in the twenty-frst century and what are the alternatives? Front Neurosci 9, 385 (2015).
36. Yuasa, T. Stereographic demonstration of the nasal cavity of the rat with reference to the density of blood vessels. Kaibogaku Zasshi 66, 191-200 (1991).
37. Sarin, H. Physiologic upper limits of pore size of diferent blood capillary types and another perspective on the dual pore theory of microvascular permeability. J Angiogenes Res 2, 14 (2010).
38. Bungay & Brenner. The motion of a closely-ftting sphere in a fuid flled tube. Int. J. Multiphase Flow. 1, 25-56 (1973).
39. Elfvin, L. G. The ultrastructure of the capillary fenestrae in the adrenal medulla of the rat. J Ultrastruct Res 12, 687-704 (1965).
40. Maul, G. G. Structure and formation of pores in fenestrated capillaries. J Ultrastruct Res 36, 768-782 (1971).
41. Karnovsky, M. J. The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J Cell Biol 35, 213-236 (1967).
42. Ohno, K., Pettigrew, K. D. & Rapoport, S. I. Lower limits of cerebrovascular permeability to nonelectrolytes in the conscious rat. Am J Physiol 235, H299-307 (1978).
43. Charonis, A. S. & Wissig, S. L. Anionic sites in basement membranes. Diferences in their electrostatic properties in continuous and fenestrated capillaries. Microvasc Res 25, 265-285 (1983).
44. Minshall, R. D. & Malik, A. B. Transport across the endothelium: regulation of endothelial permeability. Handb Exp Pharmacol 176 Pt 1, 107-144 (2006).
45. Curry, F. E. & Adamson, R. H. Endothelial glycocalyx: permeability barrier and mechanosensor. Ann Biomed Eng 40, 828-839 (2012).
46. Aird, W. C. Endothelial cell heterogeneity. Cold Spring Harb Perspect Med 2, a006429 (2012).
47. Clementi, F. & Palade, G. E. Intestinal capillaries. I. Permeability to peroxidase and ferritin. J Cell Biol 41, 33-58 (1969).
48. Watanabe, K., Saito, Y., Watanabe, I. & Mizuhira, V. Characteristics of capillary permeability in nasal mucosa. Ann Otol Rhinol Laryngol 89, 377-382 (1980).
49. Van Diest, P. & Kanan, M. W. An ultrastructural study of the endonasal microcirculation in the Wistar rat during fetal and early postnatal life. J Anat 128, 293-300 (1979).
50. Persson, C. G. et al. Plasma exudation as a first line respiratory mucosal defence. Clin Exp Allergy 21, 17-24 (1991).
51. Kuper, C. F. et al. The role of nasopharyngeal lymphoid tissue. Immunol Today 13, 219-224 (1992).
52. Cserr, H. F., Harling-Berg, C. J. & Knopf, P. M. Drainage of brain extracellular fuid into blood and deep cervical lymph and its immunological signifcance. Brain Pathol 2, 269-276 (1992).
53. Louveau, A. et al. Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337-341 (2015).
54. Aspelund, A. et al. A dural lymphatic vascular system that drains brain interstitial fuid and macromolecules. J Exp Med 212, 991-999 (2015).
55. Hoekman, J. D. & Ho, R. J. Efects of localized hydrophilic mannitol and hydrophobic nelfnavir administration targeted to olfactory epithelium on brain distribution. AAPS PharmSciTech 12, 534-543 (2011).