Robust Internal Elastic Lamina Fenestration in Skeletal Muscle Arteries

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Kirby, Brett S ^a   Bruhl, Allison ^a   Sullivan, Michelle N ^a   Francis, Michael ^b   Dinenno, Frank A ^a   Earley, Scott ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3;

ANIMAL TISSUE; ARTERIOLE; ARTERY BLOOD FLOW; ARTERY DIAMETER; ARTICLE; BLOOD VESSEL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; INTERNAL ELASTIC LAMINA; MALE; MESENTERY BLOOD VESSEL; MICROSCOPIC ANATOMY; NONHUMAN; POPLITEAL ARTERY; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT;

ANIMALS; ARTERIES; AUTOMATION; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE, SKELETAL; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84872831549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054849     Document Type: Article

References (56)

1. Joyner MJ, (2004) Feeding the sleeping giant: muscle blood flow during whole body exercise. J Physiol 558: 1.
2. Fixler DE, Atkins JM, Mitchell JH, Horwitz LD, (1976) Blood flow to respiratory, cardiac, and limb muscles in dogs during graded exercise. Am J Physiol 231: 1515-1519.
3. Musch TI, Friedman DB, Pitetti KH, Haidet GC, Stray-Gundersen J, et al. (1987) Regional distribution of blood flow of dogs during graded dynamic exercise. J Appl Physiol 63: 2269-2277.
4. Andersen P, Saltin B, (1985) Maximal perfusion of skeletal muscle in man. J Physiol 366: 233-249.
5. Calbet JA, Jensen-Urstad M, van Hall G, Holmberg HC, Rosdahl H, et al. (2004) Maximal muscular vascular conductances during whole body upright exercise in humans. J Physiol 558: 319-331.
6. Marshall RJ, Schirger A, Shepherd JT, (1961) Blood pressure during supine exercise in idiopathic orthostatic hypotension. Circulation 24: 76-81.
7. VanTeeffelen JW, Segal SS, (2003) Interaction between sympathetic nerve activation and muscle fibre contraction in resistance vessels of hamster retractor muscle. J Physiol 550: 563-574.
8. Anderson KM, Faber JE, (1991) Differential sensitivity of arteriolar alpha 1- and alpha 2-adrenoceptor constriction to metabolic inhibition during rat skeletal muscle contraction. Circulation Research 69: 178-184.
9. Shimokawa H, Yasutake H, Fujii K, Owada MK, Nakaike R, et al. (1996) The importance of the hyperpolarizing mechanism increases as the vessel size decreases in endothelium-dependent relaxations in rat mesenteric circulation. J Cardiovasc Pharmacol 28: 703-711.
10. Sandow SL, Tare M, Coleman HA, Hill CE, Parkington HC, (2002) Involvement of myoendothelial gap junctions in the actions of endothelium-derived hyperpolarizing factor. Circ Res 90: 1108-1113.
11. Masuda H, Zhuang YJ, Singh TM, Kawamura K, Murakami M, et al. (1999) Adaptive remodeling of internal elastic lamina and endothelial lining during flow-induced arterial enlargement. Arterioscler Thromb Vasc Biol 19: 2298-2307.
12. Sims FH, (1989) The internal elastic lamina in normal and abnormal human arteries. A barrier to the diffusion of macromolecules from the lumen. Artery 16: 159-173.
13. Dees MB, (1923) On the fenestrated membrane of henle. Anat Rec 26: 161-169.
14. Sandow SL, (2004) Factors, fiction and endothelium-derived hyperpolarizing factor. Clin Exp Pharmacol Physiol 31: 563-570.
15. Sandow SL, Gzik DJ, Lee RM, (2009) Arterial internal elastic lamina holes: relationship to function? J Anat 214: 258-266.
16. Ledoux J, Taylor MS, Bonev AD, Hannah RM, Solodushko V, et al. (2008) Functional architecture of inositol 1,4,5-trisphosphate signaling in restricted spaces of myoendothelial projections. Proc Natl Acad Sci U S A 105: 9627-9632.
17. Wong LC, Langille BL, (1996) Developmental remodeling of the internal elastic lamina of rabbit arteries: effect of blood flow. Circ Res 78: 799-805.
18. Senadheera S, Kim Y, Grayson TH, Toemoe S, Kochukov MY, et al. (2012) Transient receptor potential canonical type 3 channels facilitate endothelium-derived hyperpolarization-mediated resistance artery vasodilator activity. Cardiovasc Res.
19. Guo ZY, Yan ZQ, Bai L, Zhang ML, Jiang ZL, (2008) Flow shear stress affects macromolecular accumulation through modulation of internal elastic lamina fenestrae. Clin Biomech (Bristol, Avon) 23Suppl 1: S104-111.
20. Wiedeman MP, (1968) Blood flow through terminal arterial vessels after denervation of the bat wing. Circ Res 22: 83-89.
21. Roseguini BT, Davis MJ, Harold Laughlin M, (2010) Rapid vasodilation in isolated skeletal muscle arterioles: impact of branch order. Microcirculation 17: 83-93.
22. Wolfle SE, Chaston DJ, Goto K, Sandow SL, Edwards FR, et al. (2011) Non-linear relationship between hyperpolarisation and relaxation enables long distance propagation of vasodilatation. J Physiol 589: 2607-2623.
23. Dora KA, Gallagher NT, McNeish A, Garland CJ, (2008) Modulation of endothelial cell KCa3.1 channels during endothelium-derived hyperpolarizing factor signaling in mesenteric resistance arteries. Circ Res 102: 1247-1255.
24. Earley S, Gonzales AL, Crnich R, (2009) Endothelium-dependent cerebral artery dilation mediated by TRPA1 and Ca2+-Activated K+ channels. Circ Res 104: 987-994.
25. Ghanshani S, Wulff H, Miller MJ, Rohm H, Neben A, et al. (2000) Up-regulation of the IKCa1 potassium channel during T-cell activation. Molecular mechanism and functional consequences. J Biol Chem 275: 37137-37149.
26. Hoffman JF, Joiner W, Nehrke K, Potapova O, Foye K, et al. (2003) The hSK4 (KCNN4) isoform is the Ca2+-activated K+ channel (Gardos channel) in human red blood cells. Proc Natl Acad Sci U S A 100: 7366-7371.
27. Kohler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, et al. (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273: 1709-1714.
28. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, et al. (1998) Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395: 503-507.
29. Stocker M, (2004) Ca(2+)-activated K+ channels: molecular determinants and function of the SK family. Nat Rev Neurosci 5: 758-770.
30. Bourguignon LY, Iida N, Sobrin L, Bourguignon GJ, (1994) Identification of an IP3 receptor in endothelial cells. J Cell Physiol 159: 29-34.
31. Bourguignon LY, Jin H, Iida N, Brandt NR, Zhang SH, (1993) The involvement of ankyrin in the regulation of inositol 1,4,5-trisphosphate receptor-mediated internal Ca2+ release from Ca2+ storage vesicles in mouse T-lymphoma cells. J Biol Chem 268: 7290-7297.
32. Adebiyi A, Narayanan D, Jaggar JH, (2011) Caveolin-1 assembles type 1 inositol 1,4,5-trisphosphate receptors and canonical transient receptor potential 3 channels into a functional signaling complex in arterial smooth muscle cells. J Biol Chem 286: 4341-4348.
33. Gonzales AL, Amberg GC, Earley S, (2010) Ca2+ release from the sarcoplasmic reticulum is required for sustained TRPM4 activity in cerebral artery smooth muscle cells. Am J Physiol Cell Physiol 299: C279-288.
34. Liang XH, Crooke ST, (2011) Depletion of key protein components of the RISC pathway impairs pre-ribosomal RNA processing. Nucleic Acids Res 39: 4875-4889.
35. Hong MP, Vu K, Bautos J, Gelli A, (2010) Cch1 restores intracellular Ca2+ in fungal cells during endoplasmic reticulum stress. J Biol Chem 285: 10951-10958.
36. Tilburgs T, Roelen DL, van der Mast BJ, de Groot-Swings GM, Kleijburg C, et al. (2008) Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J Immunol 180: 5737-5745.
37. Jones S, Tucker KL, Sage T, Kaiser WJ, Barrett NE, et al. (2008) Peripheral tachykinins and the neurokinin receptor NK1 are required for platelet thrombus formation. Blood 111: 605-612.
38. Czaja K, Lakomy M, Kaleczyc J, Barb CR, Rampacek GB, et al. (2002) Leptin receptors, NPY, and tyrosine hydroxylase in autonomic neurons supplying fat depots in a pig. Biochem Biophys Res Commun 293: 1138-1144.
39. Earley S, Gonzales AL, Garcia ZI, (2010) A dietary agonist of transient receptor potential cation channel V3 elicits endothelium-dependent vasodilation. Mol Pharmacol 77: 612-620.
40. Abramoff MD, Magalhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
41. Francis M, Qian X, Charbel C, Ledoux J, Parker JC, et al. (2012) Automated region of interest analysis of dynamic Ca2+ signals in image sequences. Am J Physiol Cell Physiol 303: C236-243.
42. Sandow SL, Hill CE, (2000) Incidence of myoendothelial gap junctions in the proximal and distal mesenteric arteries of the rat is suggestive of a role in endothelium-derived hyperpolarizing factor-mediated responses. Circ Res 86: 341-346.
43. Segal SS, Kurjiaka DT, (1995) Coordination of blood flow control in the resistance vasculature of skeletal muscle. Med Sci Sports Exerc 27: 1158-1164.
44. Clifford PS, Hellsten Y, (2004) Vasodilatory mechanisms in contracting skeletal muscle. J Appl Physiol 97: 393-403.
45. Tran CH, Taylor MS, Plane F, Nagaraja S, Tsoukias NM, et al. (2012) Endothelial Ca2+ wavelets and the induction of myoendothelial feedback. Am J Physiol Cell Physiol 302: C1226-1242.
46. Sandow SL, Neylon CB, Chen MX, Garland CJ, (2006) Spatial separation of endothelial small- and intermediate-conductance calcium-activated potassium channels (K(Ca)) and connexins: possible relationship to vasodilator function? J Anat 209: 689-698.
47. Aydin F, Rosenblum WI, Povlishock JT, (1991) Myoendothelial junctions in human brain arterioles. Stroke 22: 1592-1597.
48. Milkau M, Kohler R, de Wit C, (2010) Crucial importance of the endothelial K+ channel SK3 and connexin40 in arteriolar dilations during skeletal muscle contraction. FASEB J 24: 3572-3579.
49. Behringer EJ, Segal SS, (2012) Tuning electrical conduction along endothelial tubes of resistance arteries through Ca(2+)-activated K(+) channels. Circ Res 110: 1311-1321.
50. Taugner R, Kirchheim H, Forssmann WG, (1984) Myoendothelial contacts in glomerular arterioles and in renal interlobular arteries of rat, mouse and Tupaia belangeri. Cell Tissue Res 235: 319-325.
51. Heberlein KR, Straub AC, Isakson BE, (2009) The myoendothelial junction: breaking through the matrix? Microcirculation 16: 307-322.
52. Aalkjaer C, Mulvany MJ, (1979) Morphological and mechanical properties of small mesenteric arteries and veins in spontaneously hypertensive rats. Acta Physiol Scand 107: 309-312.
53. Mulvany MJ, Halpern W, (1976) Mechanical properties of vascular smooth muscle cells in situ. Nature 260: 617-619.
54. Winter P, Dora KA, (2007) Spreading dilatation to luminal perfusion of ATP and UTP in rat isolated small mesenteric arteries. J Physiol 582: 335-347.
55. Domeier TL, Segal SS, (2007) Electromechanical and pharmacomechanical signalling pathways for conducted vasodilatation along endothelium of hamster feed arteries. J Physiol 579: 175-186.
56. Segal SS, Jacobs TL, (2001) Role for endothelial cell conduction in ascending vasodilatation and exercise hyperaemia in hamster skeletal muscle. J Physiol 536: 937-946.