Rat choroidal Pericytes as a target of the autonomic nervous system

Cell and Tissue Research

Volumn 356, Issue 1, 2014, Pages 1-8

  Schrödl, Falk ^a   Trost, Andrea ^a   Strohmaier, Clemens ^a   Bogner, Barbara ^a   Runge, Christian ^a   Kaser Eichberger, Alexandra ^a   Couillard Despres, Sebastien ^a   Aigner, Ludwig ^a   Reitsamer, Herbert A ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Autonomic nervous system; Blood flow regulation; Eye; Innervation; Pericyte; Rat

Indexed keywords

ANIMALS; AUTONOMIC NERVOUS SYSTEM; CHOROID; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; NEUROPEPTIDES; PERICYTES; RATS; RATS, INBRED BN; RATS, TRANSGENIC;

EID: 84898893756     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1769-5     Document Type: Article

References (56)

1. Alm A (1992) Ocular circulation. Mosby Year Book, St. Loius
2. Am S, Péault B, Mullins JJ (2013) Renal pericytes: multifunctional cells of the kidneys. Pflugers Arch 465:767-773
3. Armulik A, Genove G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21:193-215
4. Bellairs R, Harkness ML, Harkness RD (1975) The structure of the tapetum of the eye of the sheep. Cell Tissue Res 157:73-91
5. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10
6. Condren AB, Kumar A, Mettu P, Liang KJ, Zhao L, Tsai JY, Fariss RN, Wong WT (2013) Perivascular mural cells of the mouse choroid demonstrate morphological diversity that is correlated to vasoregulatory function. PLoS One 8:e53386
7. Couillard-Despres S, Winner B, Karl C, Lindemann G, Schmid P, Aigner R, Laemke J, Bogdahn U, Winkler J, Bischofberger J, Aigner L (2006) Targeted transgene expression in neuronal precursors: watching young neurons in the old brain. Eur J Neurosci 24:1535-1545
8. Crawford C, Kennedy-Lydon T, Sprott C, Desai T, Sawbridge L, Munday J, Unwin RJ, Wildman SS, Peppiatt-Wildman CM (2012) An intact kidney slice model to investigate vasa recta properties and function in situ. Nephron Physiol 120:17-31
9. Cuthbertson S, Jackson B, Toledo C, Fitzgerald ME, Shih YF, Zagvazdin Y, Reiner A (1997) Innervation of orbital and choroidal blood vessels by the pterygopalatine ganglion in pigeons. J Comp Neurol 386:422-442
10. Davis GE, Stratman AN, Sacharidou A, Koh W (2011) Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting. Int Rev Cell Mol Biol 288:101-165
11. De Stefano ME, Mugnaini E (1997) Fine structure of the choroidal coat of the avian eye. Vascularization, supporting tissue and innervation. Anat Embryol (Berl) 195:393-418
12. Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, Diaz-Flores L Jr (2009) Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24:909-969
13. Dulmovits BM, Herman IM (2012) Microvascular remodeling and wound healing: a role for pericytes. Int J Biochem Cell Biol 44:1800-1812
14. Elsas T, Edvinsson L, Sundler F, Uddman R (1994) Neuronal pathways to the rat conjunctiva revealed by retrograde tracing and immunocytochemistry. Exp Eye Res 58:117-126
15. Fernandez-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U (2010) Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci U S A 107:22290-22295
16. Fligny C, Duffield JS (2013) Activation of pericytes: recent insights into kidney fibrosis and microvascular rarefaction. Curr Opin Rheumatol 25:78-86
17. Flügel-Koch C, May CA, Lutjen-Drecoll E (1996) Presence of a contractile cell network in the human choroid. Ophthalmologica 210:296-302
18. Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271
19. Haddad A, Laicine EM, Tripathi BJ, Tripathi RC (2001) An extensive system of extravascular smooth muscle cells exists in the choroid of the rabbit eye. Exp Eye Res 73:345-353
20. Hamilton NB, Attwell D, Hall CN (2010) Pericyte-mediated regulation of capillary diameter: a component of neurovascular coupling in health and disease. Front Neuroenergetics 2.pii:5
21. Hammes HP, Lin J, Renner O, Shani M, Lundqvist A, Betsholtz C, Brownlee M, Deutsch U (2002) Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51:3107-3112
22. Hirata Y, Nishiwaki H (2006) The choroidal circulation assessed by laser-targetedangiography. Prog Retin Eye Res 25:129-147
23. Itoh Y, Suzuki N (2012) Control of brain capillary blood flow. J Cereb Blood Flow Metab 32:1167-1176
24. Joyce NC, DeCamilli P, Boyles J (1984) Pericytes, like vascular smooth muscle cells, are immunocytochemically positive for cyclic GMP-dependent protein kinase. Microvasc Res 28:206-219
25. Karl C, Couillard-Despres S, Prang P, Munding M, Kilb W, Brigadski T, Plotz S, Mages W, Luhmann H, Winkler J, Bogdahn U, Aigner L (2005) Neuronal precursor-specific activity of a human doublecortin regulatory sequence. J Neurochem 92:264-282
26. Kiel JW (1999) Modulation of choroidal autoregulation in the rabbit. Exp Eye Res 69:413-429
27. Kiel JW, Shepherd AP (1992) Autoregulation of choroidal blood flow in the rabbit. Invest Ophthalmol Vis Sci 33:2399-2410
28. Klooster J, Beckers HJ, Ten Tusscher MP, Vrensen GF, van der Want JJ, Lamers WP (1996) Sympathetic innervation of the rat choroid: an autoradiographic tracing and immunohistochemical study. Ophthalmic Res 28:36-43
29. Kur J, Newman EA, Chan-Ling T (2012) Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease. Prog Retin Eye Res 31:377-406
30. Kutcher ME, Herman IM (2009) The pericyte: cellular regulator of microvascular blood flow. Microvasc Res 77:235-246
31. Luiten PG, de Jong GI, Van der Zee EA, van Dijken H (1996) Ultrastructural localization of cholinergic muscarinic receptors in rat brain cortical capillaries. Brain Res 720:225-229
32. May CA (2003) Nonvascular smooth muscle alpha-actin positive cells in the choroid of higher primates. Curr Eye Res 27:1-6
33. May CA (2005) Non-vascular smooth muscle cells in the human choroid: distribution, development and further characterization. J Anat 207:381-390
34. Meriney SD, Pilar G (1987) Cholinergic innervation of the smooth muscle cells in the choroid coat of the chick eye and its development. J Neurosci 7:3827-3839
35. Miller AS, Coster DJ, Costa M, Furness JB (1983) Vasoactive intestinal polypeptide immunoreactive nerve fibres in the human eye. Aust J Ophthalmol 11:185-193
36. Neuhuber W, Schrödl F (2011) Autonomic control of the eye and the iris. Auton Neurosci 165:67-79
37. Nickla D, Wallman J (2010) The multifunctional choroid. Prog Retin Eye Res 29:144-168
38. Nuzzi R, Guglielmone R, Grignolo FM (1995) Fluorescence histochemical demonstration of adrenergic terminations in the human choroid. Eur J Ophthalmol 5:251-258
39. Ozerdem U, Stallcup WB (2003) Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6:241-249
40. Peppiatt CM, Howarth C, Mobbs P, Attwell D (2006) Bidirectional control of CNS capillary diameter by pericytes. Nature 443:700-704
41. Poiseuille JLM (1840) Recherches expérimentales sur le mouvement des liquides dans les tubes de très-petits diamètres. CR Acad Sci 11:1041-1048
42. Poukens V, Glasgow BJ, Demer JL (1998) Nonvascular contractile cells in sclera and choroid of humans and monkeys. Invest Ophthalmol Vis Sci 39:1765-1774
43. Purves D, Augustine GJ, Fitzpatrick D, Katz LC, LaMantia A-S, McNamara JO, Williams SM (2001) Neuroscience. The biogenic amines. Sinauer Associates, Sunderland
44. Schönfelder U, Hofer A, Paul M, Funk RH (1998) In situ observation of living pericytes in rat retinal capillaries. Microvasc Res 56:22-29
45. Schrödl F (2009) Intrinsic choroidal neurons. In: Troger J, Kieselbach G, Bechrakis N (eds) Neuropeptides in the eye. Research Signpost, Trivandrum, pp 169-197
46. Schrödl F, Tines R, Brehmer A, Neuhuber WL (2001) Intrinsic choroidal neurons in the duck eye receive sympathetic input: anatomical evidence for adrenergic modulation of nitrergic functions in the choroid. Cell Tissue Res 304:175-184
47. Schrödl F, De Stefano ME, Minvielle F, Brehmer A, Neuhuber WL (2005) Somatostatin immunoreactivity in quail pterygopalatine ganglion. J Anat 206:249-255
48. Stallcup WB (2002) The NG2 proteoglycan: past insights and future prospects. J Neurocytol 31:423-435
49. Stone RA, Tervo T, Tervo K, Tarkkanen A (1986) Vasoactive intestinal polypeptide-like immunoreactive nerves to the human eye. Acta Ophthalmol (Copenh) 64:12-18
50. Strohmaier C, Runge C, Schroedl F, Brandtner H, Bogner B, Grabner G, Reitsamer HA (2010) A rat model to study choroidal blood flow. ARVO May 2-6, 2010, Fort Lauderdale, abstract 5010
51. Tabata S, Ozaki HS, Nakashima M, Uemura M, Iwamoto H (1998) Innervation of blood vessels in the rat incisor pulp: a scanning electron microscopic and immunoelectron microscopic study. Anat Rec 251:384-391
52. Troger J, Kieselbach G, Teuchner B, Kralinger M, Nguyen QA, Haas G, Yayan J, Gottinger W, Schmid E (2007) Peptidergic nerves in the eye, their source and potential pathophysiological relevance. Brain Res Rev 53:39-62
53. von Tell D, Armulik A, Betsholtz C (2006) Pericytes and vascular stability. Exp Cell Res 312:623-629
54. Wanjare M, Kusuma S, Gerecht S (2013) Perivascular cells in blood vessel regeneration. Biotechnol J 8:434-447
55. Weichselbaum M, Everett AW, Sparrow MP (1996) Mapping the innervation of the bronchial tree in fetal and postnatal pig lung using antibodies to PGP 9.5 and SV2. Am J Respir Cell Mol Biol 15:703-710
56. Wu DM, Kawamura H, Sakagami K, Kobayashi M, Puro DG (2003) Cholinergic regulation of pericyte-containing retinal microvessels. Am J Physiol Heart Circ Physiol 284:H2083-H2090