Nitric oxide formation by lymphatic bulb and valves is a major regulatory component of lymphatic pumping

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 5, 2011, Pages

  Bohlen, H Glenn ^a   Gasheva, Olga Yu ^b   Zawieja, David C ^b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Lymph flow; Lymphatic; Nitric oxide; Valve

Indexed keywords

BRADYKININ; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

ARTICLE; CONTROLLED STUDY; HEART STROKE VOLUME; IN VIVO STUDY; IONTOPHORESIS; LYMPH VESSEL; LYMPHATIC BULB; LYMPHATIC SYSTEM; LYMPHATIC VALVE; MICROPIPETTE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; BIOMECHANICS; BRADYKININ; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; IONTOPHORESIS; LYMPH; LYMPHATIC VESSELS; MALE; MUSCLE CONTRACTION; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PULSATILE FLOW; RATS; RATS, SPRAGUE-DAWLEY; STRESS, MECHANICAL; TIME FACTORS;

EID: 80355139291     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00260.2011     Document Type: Article

References (39)

1. Bauser-Heaton HD, Bohlen HG. Cerebral microvascular dilation during hypotension and decreased oxygen tension: a role for nNOS 2. Am J Physiol Heart Circ Physiol 293: H2193-H2201, 2007.
2. Benoit JN, Zawieja DC, Goodman AH, Granger HJ. Characterization of intact mesenteric lymphatic pump and its responsiveness to acute edemagenic stress. Am J Physiol Heart Circ Physiol 257: H2059-H2069, 1989.
3. Benoit JN, Zawieja DC, Goodman AH, Granger HJ. Characterization of intact mesenteric lymphatic pump and its responsiveness to acute edemagenic stress 7. Am J Physiol Heart Circ Physiol 257: H2059-H2069, 1989.
4. Bohlen HG. Intestinal mucosal oxygenation influences absorptive hyper-emia. Am J Physiol Heart Circ Physiol 239: H489-H493, 1980.
5. Bohlen HG. Integration of intestinal structure, function, and microvascu-lar regulation. Microcirculation 5: 27-37, 1998.
6. Bohlen HG. Mechanism of increased vessel wall nitric oxide concentrations during intestinal absorption. Am J Physiol Heart Circ Physiol 275: H542-H550, 1998.
7. Bohlen HG, Wang W, Gashev A, Gasheva O, Zawieja D. Phasic contractions of rat mesenteric lymphatics increase basal and phasic nitric oxide generation in vivo. Am J Physiol Heart Circ Physiol 297: H1319-H1328, 2009.
8. Bohlen HG, Zhou X, Unthank JL, Miller SJ, Bills R. Transfer of nitric oxide by blood from upstream to downstream resistance vessels causes microvascular dilation. Am J Physiol Heart Circ Physiol 297: H1337-H1346, 2009.
9. Buerk DG, Riva CE, Cranstoun SD. Nitric oxide has a vasodilatory role in cat optic nerve head during flicker stimuli. Microvas Res 52: 13-26, 1996.
10. Crowe MJ, von der Weid PY, Brock JA, van Helden DF. Co-ordination of contractile activity in guinea-pig mesenteric lymphatics. J Physiol 500: 235-244, 1997.
11. Dixon JB, Gashev AA, Zawieja DC, Moore JE Jr, Cote GL. Image correlation algorithm for measuring lymphocyte velocity and diameter changes in contracting microlymphatics. Ann Biomed Eng 35: 387-396, 2007.
12. Dixon JB, Greiner ST, Gashev AA, Cote GL, Moore JE, Zawieja DC. Lymph flow, shear stress, and lymphocyte velocity in rat mesenteric prenodal lymphatics. Microcirculation 13: 597-610, 2006.
13. Eguchi D, Katusic ZS. Inhibitory effect of valves on endothelium-dependent relaxations to calcium ionophore in canine saphenous vein. Am J Physiol Heart Circ Physiol 280: H892-H898, 2001.
14. Ferguson MK, DeFilippi VJ. Nitric oxide and endothelium-dependent relaxation in tracheobronchial lymph vessels. Microvasc Res 47: 308-317, 1994.
15. Friedemann MN, Robinson SW, Gerhardt GA. o-Phenylenediamine-modified carbon fiber electrodes for the detection of nitric oxide. Anal Chem 68: 2621-2628, 1996.
16. Gashev AA, Davis MJ, Zawieja DC. Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct. J Physiol 540: 1023-1037, 2002.
17. Gashev AA, Wang W, Laine GA, Stewart RH, Zawieja DC. Characteristics of the active lymph pump in bovine prenodal mesenteric lymphatics. Lymphat Res Biol 5: 71-79, 2007.
18. Gasheva OY, Zawieja DC, Gashev AA. Contraction-initiated NO-dependent lymphatic relaxation: a self-regulatory mechanism in rat thoracic duct. J Physiol 575: 821-832, 2006.
19. Granger HJ. Role of the interstitial matrix and lymphatic pump in regulation of transcapillary fluid balance. Microvasc Res 18: 209-216, 1979.
20. Kempson S, Thompson N, Pezzuto L, Glenn BH. Nitric oxide production by mouse renal tubules can be increased by a sodium-dependent mechanism. Nitric Oxide 17: 33-43, 2007.
21. Koller A, Mizuno R, Kaley G. Flow reduces the amplitude and increases the frequency of lymphatic vasomotion: role of endothelial prostanoids. Am J Physiol Regul Integr Comp Physiol 277: R1683-R1689, 1999.
22. Ku DD, Nelson JM, Caulfield JB, Winn MJ. Release of endothelium-derived relaxing factors from canine cardiac valves. J Cardiovasc Pharmacol 16: 212-218, 1990.
23. Leak LV, Cadet JL, Griffin CP, Richardson K. Nitric oxide production by lymphatic endothelial cells in vitro. Biochem Biophys Res Commun 217: 96-105, 1995.
24. McHale NG, Meharg MK. Co-ordination of pumping in isolated bovine lymphatic vessels. J Physiol 450: 503-512, 1992.
25. Mizuno R, Dornyei G, Koller A, Kaley G. Myogenic responses of isolated lymphatics: modulation by endothelium. Microcirculation 4: 413-420, 1997.
26. Mizuno R, Koller A, Kaley G. Regulation of the vasomotor activity of lymph microvessels by nitric oxide and prostaglandins 2. Am J Physiol Regul Integr Comp Physiol 274: R790-R796, 1998.
27. Moesgaard SG, Olsen LH, Aasted B, Viuff BM, Pedersen LG, Peder-sen HD, Harrison AP. Direct measurements of nitric oxide release in relation to expression of endothelial nitric oxide synthase in isolated porcine mitral valves. J Vet Med A Physiol Pathol Clin Med 54: 156-160, 2007.
28. Nase GP, Tuttle J, Bohlen HG. Reduced perivascular Po2 increases nitric oxide release from endothelial cells. Am J Physiol Heart Circ Physiol 285: H507-H515, 2003.
29. Odashiro T, Komori K, Ishii T, Okadome K, Sugimachi K. Comparison of endothelial function between in situ and reversed vein graft: differences in endothelium-dependent responses. Surgery 117: 179-188, 1995.
30. Pezzuto L, Bohlen HG. Extracellular arginine rapidly dilates in vivo intestinal arteries and arterioles through a nitric oxide mechanism. Micro-circulation 15: 123-135, 2008.
31. Siney L, Lewis MJ. Nitric oxide release from porcine mitral valves. Cardiovasc Res 27: 1657-1661, 1993.
32. Thomas DD, Liu X, Kantrow SP, Lancaster JR Jr. The biological lifetime of nitric oxide: implications for the perivascular dynamics of NO and O2. Proc Natl Acad Sci USA 98: 355-360, 2001.
33. Tsunemoto H, Ikomi F, Ohhashi T. Flow-mediated release of nitric oxide from lymphatic endothelial cells of pressurized canine thoracic duct. Jpn J Physiol 53: 157-163, 2003.
34. von der Weid PY, Crowe MJ, van Helden DF. Endothelium-dependent modulation of pacemaking in lymphatic vessels of the guinea-pig mesentery. J Physiol 493: 563-575, 1996.
35. von der Weid PY, Zhao J, van Helden DF. Nitric oxide decreases pacemaker activity in lymphatic vessels of guinea pig mesentery. Am J Physiol Heart Circ Physiol 280: H2707-H2716, 2001.
36. Yokoyama S, Ohhashi T. Effects of acetylcholine on spontaneous contractions in isolated bovine mesenteric lymphatics 6. Am J Physiol Heart Circ Physiol 264: H1460-H1464, 1993.
37. Zani BG, Bohlen HG. Sodium channels are required during in vivo sodium chloride hyperosmolarity to stimulate an increase in intestinal endothelial nitric oxide production. Am J Physiol Heart Circ Physiol 288: H89-H95, 2005.
38. Zawieja DC, Barber BJ. Lymph protein concentration in initial and collecting lymphatics of the rat. Am J Physiol Gastrointest Liver Physiol 252: G602-G606, 1987.
39. Zawieja DC, Davis KL, Schuster R, Hinds WM, Granger HJ. Distribution, propagation, and coordination of contractile activity in lymphatics. Am J Physiol Heart Circ Physiol 264: H1283-H1291, 1993.