Exercise training initiated in late middle age attenuates cardiac fibrosis and advanced glycation end-product accumulation in senescent rats

Experimental Gerontology

Volumn 50, Issue 1, 2014, Pages 9-18

  Wright, Kathryn J ^a   Thomas, Melissa M ^a   Betik, Andrew C ^a   Belke, Darrell ^b   Hepple, Russell T ^a,b  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Advanced glycation end products; Aging; Endurance exercise; Fibrosis; Heart; Matrix metalloproteinases

Indexed keywords

ADVANCED GLYCATION END PRODUCT; GELATINASE; GELATINASE A; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 4;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DUAL ENERGY X RAY ABSORPTIOMETRY; ENDURANCE TRAINING; ENZYME ACTIVITY; ENZYME ASSAY; EXERCISE; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE FIBROSIS; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; TREADMILL EXERCISE;

%BF; ADVANCED GLYCATION END-PRODUCT; ADVANCED GLYCATION END-PRODUCTS; AGE; AGING; ANALYSIS OF VARIANCE; ANOVA; DUAL ENERGY X-RAY ABSORPTIOMETRY; DXA; ECM; ENDURANCE EXERCISE; ET; EXERCISE TRAINING; EXTRACELLULAR MATRIX; F344BNF1; FIBROSIS; FISCHER 344 BROWN NORWAY F1 HYBRID RAT; GAPDH; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE; HEART; LEFT VENTRICLE; LV; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASES; MMP; PERCENT BODY FAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RT-PCR; TIMP; TISSUE INHIBITOR OF MATRIX METALLOPROTEINASE; TRIS-BUFFERED SALINE (+0.5% TWEEN); TTBS; WGA; WHEAT GERM AGGLUTININ;

AGING; ANIMALS; COLLAGEN; FIBROSIS; GLYCOSYLATION END PRODUCTS, ADVANCED; MATRIX METALLOPROTEINASES; MYOCARDIUM; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, INBRED BN; RATS, INBRED F344; SURVIVAL ANALYSIS; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84890050519     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2013.11.006     Document Type: Article

References (58)

1. Andren B., Lind L., Hedenstierna G., Lithell H. Left ventricular hypertrophy and a decreased E-A ratio are common echocardiographic findings even in apparently healthy 70-year-old men. Cardiol. Elder. 1995, 3:367-371.
2. Arbab-Zadeh A., Dijk E., Prasad A., Fu Q., Torres P., Zhang R., Thomas J.D., Palmer D., Levine B.D. Effect of aging and physical activity on left ventricular compliance. Circulation 2004, 110:1799-1805.
3. Aronson D. Cross-linking of glycated collagen in the pathogenesis of arterial and myocardial stiffening of aging and diabetes. J. Hypertens. 2003, 21:3-12.
4. Asif M., Egan J., Vasan S., Jyothirmayi G.N., Masurekar M.R., Lopez S., Williams C., Torres R.L., Wagle D., Ulrich P., Cerami A., Brines M., Regan T.J. An advanced glycation endproduct cross-link breaker can reverse age-related increases in myocardial stiffness. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:2809-2813.
5. Avendano G.F., Agarwal R.K., Bashey R.I., Lyons M.M., Soni B.J., Jyothirmayi G.N., Regan T.J. Effects of glucose intolerance on myocardial function and collagen-linked glycation. Diabetes 1999, 48:1443-1447.
6. Badenhorst D., Maseko M., Tsotetsi O.J., Naidoo A., Brooksbank R., Norton G.R., Woodiwiss A.J. Cross-linking influences the impact of quantitative changes in myocardial collagen on cardiac stiffness and remodelling in hypertension in rats. Cardiovasc. Res. 2003, 57:632-641.
7. Bakris G.L., Bank A.J., Kass D.A., Neutel J.M., Preston R.A., Oparil S. Advanced glycation end-product cross-link breakers. A novel approach to cardiovascular pathologies related to the aging process. Am. J. Hypertens. 2004, 17:23S-30S.
8. Bales C.W., Ritchie C.S. Sarcopenia, weight loss, and nutritional frailty in the elderly. Annu. Rev. Nutr. 2002, 22:309-323.
9. Bancroft J.D., Stevens A. Theory and Practice of Histological Techniques 1982, Churchill Livingstone, New York.
10. Benjamin E.J., Levy D., Anderson K.M., Wolf P.A., Plehn J.F., Evans J.C., Comai K., Fuller D.L., Sutton M.S. Determinants of Doppler indexes of left ventricular diastolic function in normal subjects (the Framingham Heart Study). Am. J. Cardiol. 1992, 70:508-515.
11. Betik A.C., Hepple R.T. Determinants of VO2 max decline with aging: an integrated perspective. Appl. Physiol. Nutr. Metab. 2008, 33:130-140.
12. Betik A.C., Baker D.J., Krause D.J., McConkey M.J., Hepple R.T. Exercise training in late middle-aged male Fischer 344×Brown Norway F1-hybrid rats improves skeletal muscle aerobic function. Exp. Physiol. 2008, 93:863-871.
13. Betik A.C., Thomas M.M., Wright K.J., Riel C.D., Hepple R.T. Exercise training from late middle age until senescence does not attenuate the declines in skeletal muscle aerobic function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R744-R755.
14. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
15. Brenner D.A., Apstein C.S., Saupe K.W. Exercise training attenuates age-associated diastolic dysfunction in rats. Circulation 2001, 104:221-226.
16. Brower G.L., Gardner J.D., Forman M.F., Murray D.B., Voloshenyuk T., Levick S.P., Janicki J.S. The relationship between myocardial extracellular matrix remodeling and ventricular function. Eur. J. Cardiothorac. Surg. 2006, 30:604-610.
17. Burlew B.S. Diastolic dysfunction in the elderly-the interstitial issue. Am. J. Geriatr. Cardiol. 2004, 13:29-38.
18. Cha M.C., Purslow P.P. Matrix metalloproteinases are less essential for the in-situ gelatinolytic activity in heart muscle than in skeletal muscle. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2010, 156:518-522.
19. Chen M.A. Heart failure with preserved ejection fraction in older adults. Am. J. Med. 2009, 122:713-723.
20. Choi S.-Y., Chang H.-J., Choi S.-I., Il Kim K., Cho Y.-S., Youn T.-J., Chung W.-Y., Chae I.-H., Choi D.-J., Kim H.-S., Kim C.-H., Oh B.-H., Kim M.-H. Long-term exercise training attenuates age-related diastolic dysfunction: association of myocardial collagen cross-linking. J. Korean Med. Sci. 2009, 24:32-39.
21. DeFrances C.J., Cullen K.A., Kozak L.J. National hospital discharge survey: 2005 annual summary with detailed diagnosis and procedure data. Vital and Health Statistics Series 13, Data from the National Health Survey 2007, 165:1-209.
22. Derumeaux G., Ichinose F., Raher M.J., Morgan J.G., Coman T., Lee C., Cuesta J.M., Thibault H., Bloch K.D., Picard M.H., Scherrer-Crosbie M. Myocardial alterations in senescent mice and effect of exercise training a strain rate imaging study. Circ. Cardiovasc. Imaging 2008, 1:227-234.
23. Downes T.R., Nomeir A.M., Smith K.M., Stewart K.P., Little W.C. Mechanism of altered pattern of left ventricular filling with aging in subjects without cardiac disease. Am. J. Cardiol. 1989, 64:523-527.
24. Fleg J.L., Shapiro E.P., O'Connor F., Taube J., Goldberg A.P., Lakatta E.G. Left ventricular diastolic filling performance in older male athletes. JAMA 1995, 273:1371-1375.
25. Grossman W. Diastolic dysfunction in congestive heart failure. N. Engl. J. Med. 1991, 325:1557-1564.
26. Hacker T.A., McKiernan S.H., Douglas P.S., Wanagat J., Aiken J.M. Age-related changes in cardiac structure and function in Fischer 344×Brown Norway hybrid rats. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H304-H311.
27. Holloszy J.O. Exercise increases average longevity of female rats despite increased food intake and no growth retardation. J. Gerontol. 1993, 48:B97-B100.
28. Holloszy J.O., Schechtman K.B. Interaction between exercise and food restriction: effects on longevity of male rats. J. Appl. Physiol. 1991, 70:1529-1535.
29. Holloszy J.O., Smith E.K., Vining M., Adams S. Effect of voluntary exercise on longevity of rats. J. Appl. Physiol. 1985, 59:826-831.
30. Jacobsen L.A., Kent M., Lee M. America's aging population. Popul. Bull. 2011, 66.
31. Jyothirmayi G.N., Soni B.J., Masurekar M., Lyons M., Regan T.J. Effects of metformin on collagen glycation and diastolic dysfunction in diabetic myocardium. J. Cardiovasc. Pharmacol. Ther. 1998, 3:319-326.
32. Kass D.A., Bronzwaer J.G.F., Paulus W.J. What mechanisms underlie diastolic dysfunction in heart failure?. Circ. Res. 2004, 94:1533-1542.
33. Kitzman D.W. Diastolic heart failure in the elderly. Heart Fail. Rev. 2002, 7:17-27.
34. Kwak H.J., Park M.J., Cho H., Park C.M., Moon S.I., Lee H.C., Park I.C., Kim M.S., Rhee C.H., Hong S.I. Transforming growth factor-beta1 induces tissue inhibitor of metalloproteinase-1 expression via activation of extracellular signal-regulated kinase and Sp1 in human fibrosarcoma cells. Mol. Cancer Res. 2006, 4:209-220.
35. Kwak H.B., Kim J.H., Joshi K., Yeh A., Martinez D.A., Lawler J.M. Exercise training reduces fibrosis and matrix metalloproteinase dysregulation in the aging rat heart. FASEB J. 2011, 25:1106-1117.
36. Lakatta E.G. Do hypertension and aging have a similar effect on the myocardium?. Circulation 1987, 75:I69-I77.
37. Lakatta E.G., Yin F.C. Myocardial aging: functional alterations and related cellular mechanisms. Am. J. Physiol. 1982, 242:H927-H941.
38. Levy W.C., Cerqueira M.D., Abrass I.B., Schwartz R.S., Stratton J.R. Endurance exercise training augments diastolic filling at rest and during exercise in healthy young and older men. Circulation 1993, 88:116-126.
39. Lipman R.D., Chrisp C.E., Hazzard D.G., Bronson R.T. Pathologic characterization of brown Norway, brown Norway×Fischer 344, and Fischer 344×Brown Norway rats with relation to age. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 1996, 51:B54-B59.
40. Little W.C., Zile M.R., Kitzman D.W., Hundley W.G., O'Brien T.X., Degroof R.C. The effect of alagebrium chloride (ALT-711), a novel glucose cross-link breaker, in the treatment of elderly patients with diastolic heart failure. J. Card. Fail. 2005, 11:191-195.
41. Lye M., Wisniacki N. Heart failure in the elderly: a diastolic problem?. Eur. J. Heart Fail. 2000, 2:133-136.
42. Mantero A., Gentile F., Gualtierotti C., Azzollini M., Barbier P., Beretta L., Casazza F., Corno R., Giagnoni E., Lippolis A. Left ventricular diastolic parameters in 288 normal subjects from 20 to 80years old. Eur. Heart J. 1995, 16:94-105.
43. Masoro E.J., Austad S.N. Handbook of the Biology of Aging 2006, Elsevier Academic Press.
44. Norton G.R., Candy G., Woodiwiss A.J. Aminoguanidine prevents the decreased myocardial compliance produced by streptozotocin-induced diabetes mellitus in rats. Circulation 1996, 93:1905-1912.
45. Norton G.R., Tsotetsi J., Trifunovic B., Hartford C., Candy G.P., Woodiwiss A.J. Myocardial stiffness is attributed to alterations in cross-linked collagen rather than total collagen or phenotypes in spontaneously hypertensive rats. Circulation 1997, 96:1991-1998.
46. Takemoto K.A., Bernstein L., Lopez J.F., Marshak D., Rahimtoola S.H., Chandraratna P.A.N. Abnormalities of diastolic filling of the left-ventricle associated with aging are less pronounced in exercise-trained individuals. Am. Heart J. 1992, 124:143-148.
47. Thomas S., Rich M.W. Epidemiology, pathophysiology, and prognosis of heart failure in the elderly. Clin. Geriatr. Med. 2007, 23:1-10.
48. Thomas D.P., McCormick R.J., Zimmerman S.D., Vadlamudi R.K., Gosselin L.E. Aging-induced and training-induced alterations in collagen characteristics of rat left-ventricle and papillary-muscle. Am. J. Physiol. 1992, 263:H778-H783.
49. Thomas D.P., Zimmerman S.D., Hansen T.R., Martin D.T., McCormick R.J. Collagen gene expression in rat left ventricle: interactive effect of age and exercise training. J. Appl. Physiol. 2000, 89:1462-1468.
50. Thomas D.P., Cotter T.A., Li X., McCormick R.J., Gosselin L.E. Exercise training attenuates aging-associated increases in collagen and collagen crosslinking of the left but not the right ventricle in the rat. Eur. J. Appl. Physiol. 2001, 85:164-169.
51. Thomas M.M., Vigna C., Betik A.C., Tupling A.R., Hepple R.T. Initiating treadmill training in late middle age offers modest adaptations in Ca2+ handling but enhances oxidative damage in senescent rat skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R1269-R1278.
52. Thomas M.M., Vigna C., Betik A.C., Tupling A.R., Hepple R.T. Cardiac calcium pump inactivation and nitrosylation in senescent rat myocardium are not attenuated by long-term treadmill training. Exp. Gerontol. 2011, 46:803-810.
53. Turturro A., Witt W.W., Lewis S., Hass B.S., Lipman R.D., Hart R.W. Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J. Gerontol. A. Biol. Sci. Med. Sci. 1999, 54:B492-B501.
54. Vaitkevicius P.V., Lane M., Spurgeon H., Ingram D.K., Roth G.S., Egan J.J., Vasan S., Wagle D.R., Ulrich P., Brines M., Wuerth J.P., Cerami A., Lakatta E.G. A cross-link breaker has sustained effects on arterial and ventricular properties in older rhesus monkeys. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1171-1175.
55. Vater C.A., Harris E.D., Siegel R.C. Native cross-links in collagen fibrils induce resistance to human synovial collagenase. Biochem. J. 1979, 181:639-645.
56. Walker E.M., Nillas M.S., Mangiarua E.I., Cansino S., Morrison R.G., Perdue R.R., Triest W.E., Wright G.L., Studeny M., Wehner P., Rice K.M., Blough E.R. Age-associated changes in hearts of male Fischer 344/Brown Norway F1 rats. Ann. Clin. Lab. Sci. 2006, 36:427-438.
57. Willemsen S., Hartog J.W., Hummel Y.M., van Ruijven M.H., van der Horst I.C., van Veldhuisen D.J., Voors A.A. Tissue advanced glycation end products are associated with diastolic function and aerobic exercise capacity in diabetic heart failure patients. Eur. J. Heart Fail. 2011, 13:76-82.
58. Woodiwiss A.J., Tsotetsi O.J., Sprott S., Lancaster E.J., Mela T., Chung E.S., Meyer T.E., Norton G.R. Reduction in myocardial collagen cross-linking parallels left ventricular dilatation in rat models of systolic chamber dysfunction. Circulation 2001, 103:155-160.