Age-related remodeling of small arteries is accompanied by increased sphingomyelinase activity and accumulation of long-chain ceramides

Physiological Reports

Volumn 2, Issue 5, 2014, Pages

  Ohanian, Jacqueline ^a   Liao, Aiyin ^a   Forman, Simon P ^a   Ohanian, Vasken ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Aging; Sphingolipids; Vascular remodeling

Indexed keywords

ACETYLCHOLINE; CERAMIDE; COLLAGEN; DIHYDROCERAMIDE C16; ELASTIN; LONGCHAIN CERAMIDE (C14 C20); NORADRENALIN; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIAL WALL THICKNESS; ARTICLE; BLOOD VESSEL PARAMETERS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTROMYOGRAPHY; ENZYME ACTIVITY; FEMALE; HEART RATE; IMMUNOFLUORESCENCE TEST; LUMEN DIAMETER; MEAN ARTERIAL PRESSURE; MESENTERIC ARTERY; NONHUMAN; PULSE PRESSURE; SHEEP; STRESS STRAIN RELATIONSHIP; VASCULAR REMODELING; VASOCONSTRICTION; VASODILATATION;

EID: 85002998532     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12015     Document Type: Article

References (67)

1. Adrian, M., P. Laurant, and A. Berthelot. 2004. Effect of magnesium on mechanical properties of pressurized mesenteric small arteries from old and adult rats. Clin. Exp. Pharmacol. Physiol. 31:306-313.
2. Akopov, E. S., L. Zhang, and W. J. Pearce. 1998. Regulation of Ca sensitization by PKC and rho proteins in ovine cerebral arteries: effects of artery size and age. Am. J. Physiol. 275: H930-H939.
3. Alewijnse, A. E., and S. L. M. Peters. 2008. Sphingolipid signalling in the cardiovascular system: good, bad or both? Eur. J. Pharmacol. 585:292-302.
4. Avolio, A. P., F. Q. Deng, W. Q. Li, Y. F. Luo, Z. D. Huang, L. F. Xing, et al. 1985. Effects of aging on arterial distensibility in populations with high and low prevalence of hypertension: comparison between urban and rural communities in China. Circulation 71:202-210.
5. Bielawski, J., J. S. Pierce, J. Snider, B. Rembiesa, Z. M. Szulc, and A. Bielawska. 2010. Sphingolipid analysis by high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). Adv. Exp. Med. Biol. 688:46-59.
6. Bolz, S.-S., L. Vogel, D. Sollinger, R. Derwand, C. Boer, S. M. Pitson, et al. 2003. Sphingosine kinase modulates microvascular tone and myogenic responses through activation of RhoA/Rho kinase. Circulation 108:342-347.
7. Briones, A. M., M. Salaices, and E. Vila. 2007. Mechanisms underlying hypertrophic remodeling and increased stiffness of mesenteric resistance arteries from aged rats. J. Gerontol. A Biol. Sci. Med. Sci. 62:696-706.
8. Clarke, C. J., S. Forman, J. Pritchett, V. Ohanian, and J. Ohanian. 2008. Phospholipase C-delta1 modulates sustained contraction of rat mesenteric small arteries in response to noradrenaline, but not endothelin-1. Am. J. Physiol. Heart Circ. Physiol. 295:H826-H834.
9. Cook, J. J., T. D. Wailgum, U. S. Vasthare, H. N. Mayrovitz, and R. F. Tuma. 1992. Age-related alterations in the arterial microvasculature of skeletal muscle. J. Gerontol. 47:B83-B88.
10. Cutler, R. G., J. Kelly, K. Storie, W. A. Pedersen, A. Tammara, K. Hatanpaa, et al. 2004. Involvement of oxidative stressinduced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc. Natl. Acad. Sci. USA 101:2070-2075.
11. Dhami, R., X. He, and E. H. Schuchman. 2010. Acid sphingomyelinase deficiency attenuates bleomycin-induced lung inflammation and fibrosis in mice. Cell. Physiol. Biochem. 26:749-760.
12. Dibb, K. M., U. Rueckschloss, D. A. Eisner, G. Isenberg, and A. W. Trafford. 2004. Mechanisms underlying enhanced cardiac excitation contraction coupling observed in the senescent sheep myocardium. J. Mol. Cell. Cardiol. 37:1171-1181.
13. D’Mello, N. P., A. M. Childress, D. S. Franklin, S. P. Kale, C. Pinswasdi, and S. M. Jazwinski. 1994. Cloning and characterization of LAG1, a longevity-assurance gene in yeast. J. Biol. Chem. 269:15451-15459.
14. Flamm, S. D., J. Taki, R. Moore, S. F. Lewis, F. Keech, F. Maltais, et al. 1990. Redistribution of regional and organ blood volume and effect on cardiac function in relation to upright exercise intensity in healthy human subjects. Circulation 81:1550-1559.
15. Franceschi, C., M. Bonafé, S. Valensin, F. Olivieri, M. De Luca, E. Ottaviani, et al. 2000. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 908:244-254.
16. Gonzalez, J. M., A. M. Briones, B. Starcher, M. V. Conde, B. Somoza, C. Daly, et al. 2005. Influence of elastin on rat small artery mechanical properties. Exp. Physiol. 90:463-468.
17. Graham, H. K., and A. W. Trafford. 2007. Spatial disruption and enhanced degradation of collagen with the transition from compensated ventricular hypertrophy to symptomatic congestive heart failure. Am. J. Physiol. Heart Circ. Physiol. 292:H1364-H1372.
18. Graham, H. K., R. Akhtar, C. Kridiotis, B. Derby, T. Kundu, A. W. Trafford, et al. 2011. Localised micro-mechanical stiffening in the ageing aorta. Mech. Ageing Dev. 132:459-467.
19. Greenwald, S. E. 2007. Ageing of the conduit arteries. J. Pathol. 211:157-172.
20. Gros, R., R. Van Wert, X. You, E. Thorin, and M. Husain. 2002. Effects of age, gender, and blood pressure on myogenic responses of mesenteric arteries from C57BL/6 mice. Am. J. Physiol. Heart Circ. Physiol. 282:H380-H388.
21. Guillas, I., P. A. Kirchman, R. Chuard, M. Pfefferli, J. C. Jiang, S. M. Jazwinski, et al. 2001. C26-CoA-dependent ceramide synthesis of Saccharomyces cerevisiae is operated by Lag1p and Lac1p. EMBO J. 20:2655-2665.
22. Hajdu, M. A., D. D. Heistad, J. E. Siems, and G. L. Baumbach. 1990. Effects of aging on mechanics and composition of cerebral arterioles in rats. Circ. Res. 66:1747-1754.
23. Hannun, Y. A., and L. M. Obeid. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9:139-150.
24. Hannun, Y. A., and L. M. Obeid. 2011. Many ceramides. J. Biol. Chem. 286:27855-27862.
25. Hernandez-Corbacho, M. J., R. W. Jenkins, C. J. Clarke, Y. A. Hannun, L. M. Obeid, A. J. Snider, et al. 2011. Accumulation of long-chain glycosphingolipids during aging is prevented by caloric restriction. PLoS One 6:e20411.
26. Herrera, E. A., R. A. Riquelme, G. Ebensperger, R. V. Reyes, C. E. Ulloa, G. Cabello, et al. 2010. Long-term exposure to high-altitude chronic hypoxia during gestation induces neonatal pulmonary hypertension at sea level. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299:R1676-R1684.
27. Hill, M. A., and G. A. Meininger. 2012. Arteriolar vascular smooth muscle cells: mechanotransducers in a complex environment. Int. J. Biochem. Cell Biol. 44:1505-1510.
28. Hoefer, J., M. A. Azam, J. T. E. Kroetsch, H. Leong-Poi, M. A. Momen, J. Voigtlaender-Bolz, et al. 2010. Sphingosine-1-phosphate-dependent activation of p38 MAPK maintains elevated peripheral resistance in heart failure through increased myogenic vasoconstriction. Circ. Res. 107:923-933.
29. Horn, M. A., H. K. Graham, M. A. Richards, J. D. Clarke, D. J. Greensmith, S. J. Briston, et al. 2012. Age-related divergent remodeling of the cardiac extracellular matrix in heart failure: Collagen accumulation in the young and loss in the aged. J. Mol. Cell. Cardiol. 53:82-90.
30. Izzard, A. S., D. Graham, M. P. Burnham, E. H. Heerkens, A. F. Dominiczak, and A. M. Heagerty. 2003. Myogenic and structural properties of cerebral arteries from the strokeprone spontaneously hypertensive rat. Am. J. Physiol. Heart Circ. Physiol. 285:H1489-H1494.
31. Izzard, A. S., S. Horton, E. H. Heerkens, L. Shaw, and A. M. Heagerty. 2006. Middle cerebral artery structure and distensibility during developing and established phases of hypertension in the spontaneously hypertensive rat. J. Hypertens. 24:875-880.
32. Lakatta, E. G., and D. Levy. 2003. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: part I: aging arteries: a “set up” for vascular disease. Circulation 107:139-146.
33. Laurant, P., M. Adrian, and A. Berthelot. 2004. Effect of age on mechanical properties of rat mesenteric small arteries. Can. J. Physiol. Pharmacol. 82:269-275.
34. Lecka-Czernik, B., E. J. Moerman, R. A. Jones, and S. Goldstein. 1996. Identification of gene sequences overexpressed in senescent and Werner syndrome human fibroblasts. Exp. Gerontol. 31:159-174.
35. Lemogoum, D., W. Ngatchou, C. Janssen, M. Leeman, L. Van Bortel, P. Boutouyrie, et al. 2012. Effects of hunter-gatherer subsistence mode on arterial distensibility in Cameroonian pygmies. Hypertension 60:123-128.
36. Li, Z., H. Cheng, W. J. Lederer, J. Froehlich, and E. G. Lakatta. 1997. Enhanced proliferation and migration and altered cytoskeletal proteins in early passage smooth muscle cells from young and old rat aortic explants. Exp. Mol. Pathol. 64:1-11.
37. Lightle, S. A., J. I. Oakley, and M. N. Nikolova-Karakashian. 2000. Activation of sphingolipid turnover and chronic generation of ceramide and sphingosine in liver during aging. Mech. Ageing Dev. 120:111-125.
38. Loidl, A., R. Claus, H. P. Deigner, and A. Hermetter. 2002. High-precision fluorescence assay for sphingomyelinase activity of isolated enzymes and cell lysates. J. Lipid Res. 43:815-823.
39. Mandala, M., A. L. Pedatella, S. Morales Palomares, M. J. Cipolla, and G. Osol. 2012. Maturation is associated with changes in rat cerebral artery structure, biomechanical properties and tone. Acta Physiol. (Oxf) 205:363-371.
40. Martinez-Lemus, L. A., M. A. Hill, and G. A. Meininger. 2009. The plastic nature of the vascular wall: a continuum of remodeling events contributing to control of arteriolar diameter and structure. Physiology (Bethesda) 24:45-57.
41. McEniery, C. M., I. B. Wilkinson, and A. P. Avolio. 2007. Age, hypertension and arterial function. Clin. Exp. Pharmacol. Physiol. 34:665-671.
42. McEniery, C. M., K. M. Yasmin Maki-Petaja, B. J. McDonnell, M. Munnery, S. S. Hickson, S. S. Franklin, et al. 2010. The impact of cardiovascular risk factors on aortic stiffness and wave reflections depends on age: the Anglo-Cardiff Collaborative Trial (ACCT III). Hypertension 56:591-597.
43. Moles, A., N. Tarrats, A. Morales, M. Dom_ınguez, R. Bataller, J. Caballer_ıa, et al. 2010. Acidic sphingomyelinase controls hepatic stellate cell activation and in vivo liver fibrogenesis. Am. J. Pathol. 177:1214-1224.
44. Moreau, P., L. V. d’Uscio, and T. F. Lüscher. 1998. Structure and reactivity of small arteries in aging. Cardiovasc. Res. 37:247-253.
45. Muller-Delp, J., S. A. Spier, M. W. Ramsey, L. A. Lesniewski, A. Papadopoulos, J. D. Humphrey, et al. 2002. Effects of aging on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am. J. Physiol. Heart Circ. Physiol. 282:H1843-H1854.
46. Mulvany, M. 1999. Vascular remodelling of resistance vessels: can we define this? Cardiovasc. Res. 41:9-13.
47. Nikolova-Karakashian, M., A. Karakashian, and K. Rutkute. 2008. Role of neutral sphingomyelinases in aging and inflammation. Subcell. Biochem. 49:469-486.
48. Nyborg, N. C., and P. J. Nielsen. 1990. The level of spontaneous myogenic tone in isolated human posterior ciliary arteries decreases with age. Exp. Eye Res. 51:711-715.
49. Obeid, L. M., and Y. A. Hannun. 2003. Ceramide, stress, and a “LAG” in aging. Sci. Aging Knowledge Environ. 2003:PE27.
50. Ogretmen, B., and Y. A. Hannun. 2004. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat. Rev. Cancer 4:604-616.
51. Ohanian, J., S. P. Forman, G. Katzenberg, and V. Ohanian. 2012. Endothelin-1 stimulates small artery VCAM-1 expression through p38MAPK-dependent neutral sphingomyelinase. J. Vasc. Res. 49:353-362.
52. Patschan, S., J. Chen, A. Polotskaia, N. Mendelev, J. Cheng, D. Patschan, et al. 2008. Lipid mediators of autophagy in stress-induced premature senescence of endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 294:H1119-H1129.
53. Qiu, H., Y. Zhu, Z. Sun, J. P. Trzeciakowski, M. Gansner, C. Depre, et al. 2010. Short communication: vascular smooth muscle cell stiffness as a mechanism for increased aortic stiffness with aging. Circ. Res. 107:615-619.
54. Rao, R. P., C. Yuan, J. C. Allegood, S. S. Rawat, M. B. Edwards, X. Wang, et al. 2007. Ceramide transfer protein function is essential for normal oxidative stress response and lifespan. Proc. Natl. Acad. Sci. USA 104:11364-11369.
55. Rowell, L. B. 1974. Human cardiovascular adjustments to exercise and thermal stress. Physiol. Rev. 54:75-159.
56. Sato, M., M. Markiewicz, M. Yamanaka, A. Bielawska, C. Mao, L. M. Obeid, et al. 2003. Modulation of transforming growth factor-beta (TGF-beta) signaling by endogenous sphingolipid mediators. J. Biol. Chem. 278:9276-9282.
57. Schorling, S., B. Vallée, W. P. Barz, H. Riezman, and D. Oesterhelt. 2001. Lag1p and Lac1p are essential for the Acyl-CoA-dependent ceramide synthase reaction in Saccharomyces cerevisae. Mol. Biol. Cell 12:3417-3427.
58. Smith, A. R., F. Visioli, B. Frei, and T. M. Hagen. 2006. Agerelated changes in endothelial nitric oxide synthase phosphorylation and nitric oxide dependent vasodilation: evidence for a novel mechanism involving sphingomyelinase and ceramide-activated phosphatase 2A. Aging Cell 5:391-400.
59. Ungvari, Z., G. Kaley, R. De Cabo, W. E. Sonntag, and A. Csiszar. 2010. Mechanisms of vascular aging: new perspectives. J. Gerontol. A Biol. Sci. Med. Sci. 65:1028-1041.
60. Venable, M. E., and X. Yin. 2009. Ceramide induces endothelial cell senescence. Cell Biochem. Funct. 27:547-551.
61. Walsh, M. P., and W. C. Cole. 2013. The role of actin filament dynamics in the myogenic response of cerebral resistance arteries. J. Cereb. Blood Flow Metab. 33:1-12.
62. Wang, M., R. E. Monticone, and E. G. Lakatta. 2010. Arterial aging: a journey into subclinical arterial disease. Curr. Opin. Nephrol. Hypertens. 19:201-207.
63. Wilkinson, I. B., and C. M. McEniery. 2012. Arteriosclerosis: inevitable or self-inflicted? Hypertension 60:3-5.
64. Williams, J. M., and W. J. Pearce. 2006. Age-dependent modulation of endothelium-dependent vasodilatation by chronic hypoxia in ovine cranial arteries. Int. J. Appl. Physiol. 100:225-232.
65. Xiao, D., X. Huang, S. Yang, L. D. Longo, and L. Zhang. 2010. Pregnancy downregulates actin polymerization and pressuredependent myogenic tone in ovine uterine arteries. Hypertension 56:1009-1015.
66. Yamanaka, M., D. Shegogue, H. Pei, S. Bu, A. Bielawska, J. Bielawski, et al. 2004. Sphingosine kinase 1 (SPHK1) is induced by transforming growth factor-beta and mediates TIMP-1 up-regulation. J. Biol. Chem. 279:53994-54001.
67. Zeidan, Y. H., R. W. Jenkins, and Y. A. Hannun. 2008. Remodeling of cellular cytoskeleton by the acid sphingomyelinase/ceramide pathway. J. Cell Biol. 181:335-350.