Rapamycin attenuates age-associated changes in tibialis anterior tendon viscoelastic properties

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 71, Issue 7, 2016, Pages 858-865

  Zaseck, Lauren Wood ^a,c   Miller, Richard A ^b   Brooks, Susan V ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Biology of aging; Mice; mTOR

Indexed keywords

COLLAGEN; HYDROXYPROLINE; IMMUNOSUPPRESSIVE AGENT; NEUTROPHIL COLLAGENASE; RAPAMYCIN;

AGING; ANIMAL; BIOMECHANICS; DRUG EFFECTS; ELASTICITY; EXTRACELLULAR MATRIX; FEMALE; LONG TERM ADVERSE EFFECTS; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; TENDON;

AGING; ANIMALS; BIOMECHANICAL PHENOMENA; COLLAGEN; ELASTICITY; EXTRACELLULAR MATRIX; FEMALE; HYDROXYPROLINE; IMMUNOSUPPRESSIVE AGENTS; LONG TERM ADVERSE EFFECTS; MATRIX METALLOPROTEINASE 8; MICE; MUSCLE, SKELETAL; SIROLIMUS; TENDONS;

EID: 84979255907     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glv307     Document Type: Article

References (42)

1. Brooks SV, Faulkner JA. Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol. 1988;404:71-82. doi: 10.1113/jphysiol.1988.sp017279
2. Narici MV, Maganaris CN. Adaptability of elderly human muscles and tendons to increased loading. J Anat. 2006;208:433-443. doi: 10.1111/j.1469-7580.2006.00548.x
3. Gomez-Cabello A, Ara I, Gonzalez-Aguero A, Casajus JA, Vicente-Rodriguez G. Effects of training on bone mass in older adults. Sports Med. 2012;42:301-325. doi: 10.2165/11597670-000000000-00000
4. Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev. 2004;84:649-698. doi: 10.1152/physrev.00031.2003
5. Rees JD, Wilson AM, Wolman RL. Current concepts in the management of tendon disorders. J Rheumatol. 2006;45:508-521. doi: 10.1093/rheumatology/kel046
6. Tempelhof S, Rupp S, Seil R. Age-related prevalence of rotator cuff tears in asymptomatic shoulders. J Shoulder Elbow Surg. 1999;8:296-299. doi: 10.1016/S1058-2746(99)90148-9
7. Yamamoto A, Takagishi K, Osawa T, et al. Prevalence and risk factors of a rotator cuff tear in the general population. J Shoulder Elbow Surg. 2010;19:116-120. doi: 10.1016/j.jse.2009.04.006
8. Tallon C, Maffulli N, Ewen SW. Ruptured Achilles tendons are significantly more degenerated than tendinopathic tendons. Med Sci Sports Exerc. 2001;33:1983-1990. doi: 10.1097/00005768-200112000-00002
9. Kearney RS, Achten J, Lamb SE, Parsons N, Costa ML. The Achilles tendon total rupture score: a study of responsiveness, internal consistency and convergent validity on patients with acute Achilles tendon ruptures. Health Qual Life Outcomes. 2012;10:24. doi: 10.1186/1477-7525-10-24
10. Schibany N, Zehetgruber H, Kainberger F, et al. Rotator cuff tears in asymptomatic individuals: a clinical and ultrasonographic screening study. Eur J Radiol. 2004;51:263-268. doi: 10.1016/S0720-048X(03)00159-1
11. Mackey DC, Robinovitch SN. Mechanisms underlying age-related differences in ability to recover balance with the ankle strategy. Gait Posture. 2006;23:59-68. doi: 10.1016/j.gaitpost.2004.11.009
12. Bojsen-Møller J, Magnusson SP, Rasmussen LR, Kjaer M, Aagaard P. Muscle performance during maximal isometric and dynamic contractions is influenced by the stiffness of the tendinous structures. J Appl Physiol (1985). 2005;99:986-994. doi: 10.1152/japplphysiol.01305.2004
13. Nestorson J, Movin T, Möller M, Karlsson J. Function after Achilles tendon rupture in the elderly: 25 patients older than 65 years followed for 3 years. Acta Orthop Scand. 2000;71:64-68. doi: 10.1080/00016470052943928
14. Turan A, Teber MA, Yakut ZI, Unlu HA, Hekimoglu B. Sonoelastographic assessment of the age-related changes of the Achilles tendon. Med Ultrason. 2015;17:58-61. doi: 10.11152/mu.2013.2066.171.ayt
15. Wood LK, Arruda EM, Brooks SV. Regional stiffening with aging in tibialis anterior tendons of mice occurs independent of changes in collagen fibril morphology. J Appl Physiol (1985). 2011;111:999-1006. doi: 10.1152/japplphysiol.00460.2011
16. Wood LK, Brooks SV. Ten weeks of treadmill running decreases stiffness and increases collagen turnover in tendons of old mice. J Ortho Res. In press. doi: 10.1002/jor.22824
17. Kostrominova TY, Brooks SV. Age-related changes in structure and extracellular matrix protein expression levels in rat tendons. Age (Dordr). 2013;35:2203-2214. doi: 10.1007/s11357-013-9514-2
18. Reddy GK. Cross-linking in collagen by nonenzymatic glycation increases the matrix stiffness in rabbit achilles tendon. Exp Diabesity Res. 2004;5:143-153. doi: 10.1080/15438600490277860
19. Iagnocco A, Filippucci E, Sakellariou G, et al. Ultrasound imaging for the rheumatologist XLIV. Ultrasound of the shoulder in healthy individuals. Clin Exp Rheumatol. 2013;31:165-171.
20. Goc A, Choudhary M, Byzova TV, Somanath PR. TGFβ- and bleomycininduced extracellular matrix synthesis is mediated through Akt and mammalian target of rapamycin (mTOR). J Cell Physiol. 2011;226:3004-3013. doi: 10.1002/jcp.22648
21. Zhang Y, Bokov A, Gelfond J, et al. Rapamycin extends life and health in C57BL/6 mice. J Gerontol A Biol Sci Med Sci. 2014;69:119-130. doi: 10.1093/gerona/glt056
22. Harrison DE, Strong R, Sharp ZD, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009;460:392-395. doi: 10.1038/nature08221
23. Miller RA, Harrison DE, Astle CM, et al. Rapamycin-mediated lifespan increase in mice is dose and sex dependent and metabolically distinct from dietary restriction. Aging Cell. 2014;13:468-477. doi: 10.1111/acel.12194
24. Wilkinson JE, Burmeister L, Brooks SV, et al. Rapamycin slows aging in mice. Aging Cell. 2012;11:675-682. doi: 10.1111/j.1474-9726.2012.00832.x
25. Schmelzle T, Hall MN. TOR, a central controller of cell growth. Cell. 2000;103:253-262. doi: 10.1016/S0092-8674(00)00117-3
26. Riley GP, Curry V, DeGroot J, et al. Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology. Matrix Biol. 2002;21:185-195. doi: 10.1016/S0945-053X(01)00196-2
27. Woessner JF. Determination of hydroxyproline in tissue and protein samples containing small properties of this imino acid. Arch Biochem Biophys. 1961;93:440-447. doi: 10.1016/0003-9861(61)90291-0
28. Rutledge RG, Stewart D. A kinetic-based sigmoidal model for the polymerase chain reaction and its application to high-capacity absolute quantitative real-time PCR. BMC Biol. 2008;8:47. doi: 10.1186/1472-6750-8-47
29. Agabalyan NA, Evans DJ, Stanley RL. Investigating tendon mineralisation in the avian hindlimb: a model for tendon ageing, injury and disease. J Anat. 2013;223:262-277. doi: 10.1111/joa.12078
30. Jozsa L, Balint BJ, Reffy A. Calcifying tendinopathy. Arch Orthop Traum Surg. 1980;97:305-307. doi: 10.1007/BF00380713
31. Jia K, Chen D, Riddle DL. The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development. 2004;131:3897-3906. doi: 10.1242/dev.01255
32. Neff F, Flores-Dominguez D, Ryan DP, et al. Rapamycin extends murine lifespan but has limited effects on aging. J Clin Invest. 2013;123:3272-3291. doi: 10.1172/JCI67674
33. Carter CS, Khamiss D, Matheny M, et al. Rapamycin versus intermittent feeding: dissociable effects on physiological and behavioral outcomes when initiated early and late in life. J Gerontol A Biol Sci Med Sci. Epub ahead of print. doi: 10.1093/gerona/glu238
34. Harrison DE, Strong R, Allison DB, et al. Acarbose, 17-α-estradiol, and nordihydroguaiaretic acid extend mouse lifespan preferentially in males. Aging Cell. 2014;13:273-282. doi: 10.1111/acel.12170
35. Babraj JA, Cuthbertson DJ, Smith K, et al. Collagen synthesis in human musculoskeletal tissues and skin. Am J Physiol Endocrinol Metab. 2005;289:E864-E869. doi: 10.1152/ajpendo.00243.2005
36. Hansen P, Haraldsson BT, Aagaard P, et al. Lower strength of the human posterior patellar tendon seems unrelated to mature collagen cross-linking and fibril morphology. J Appl Physiol (1985). 2010;108:47-52. doi: 10.1152/japplphysiol.00944.2009
37. DeGroot J, Verzijl N, Wenting-Van Wijk MJ, et al. Age-related decrease in susceptibility of human articular cartilage to matrix metalloproteinase- mediated degradation: the role of advanced glycation end products. Arthritis Rheum. 2001;44:2562-2571. doi: 10.1002/1529-0131(200111)44:113.0.CO;2-1
38. Poulalhon N, Farge D, Roos N, et al. Modulation of collagen and MMP-1 gene expression in fibroblasts by the immunosuppressive drug rapamycin. A direct role as an antifibrotic agent? J Biol Chem. 2006;281:33045-33052. doi: 10.1074/jbc.M606366200
39. Houssaini A, Abid S, Mouraret N, et al. Rapamycin reverses pulmonary artery smooth muscle cell proliferation in pulmonary hypertension. Am J Respir Cell Mol Biol. 2013;48:568-577. doi: 10.1165/rcmb.2012-0429OC
40. Ramos FJ, Chen SC, Garelick MG, et al. Rapamycin reverses elevated mTORC1 signaling in lamin A/C-deficient mice, rescues cardiac and skeletal muscle function, and extends survival. Sci Transl Med. 2012;4:144ra103. doi: 10.1126/scitranslmed.3003802
41. Caramés B, Hasegawa A, Taniguchi N, Miyaki S, Blanco FJ, Lotz M. Autophagy activation by rapamycin reduces severity of experimental osteoarthritis. Ann Rheum Dis. 2012;71:575-581. doi: 10.1136/annrheumdis-2011-200557
42. Miller RA, Harrison DE, Astle CM, et al. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci. 2011;66:191-201. doi: 10.1093/gerona/glq178