Influence of physical exercise on aging rats: II. Life-long exercise delays aging of tail tendon collagen

doi:10.1016/0047-6374(96)01729-0

Mechanisms of Ageing and Development

Volume 88, Issue 3, 17 July 1996, Pages 139-148

https://doi.org/10.1016/0047-6374(96)01729-0 Get rights and content

Abstract

Regular physical exercise has been shown to have a number of benefits compared with sedentary behaviour, such as delaying a number of aging changes and increasing the life expectancy but not the maximum lifespan. The purpose of this paper is to analyze the effects of physical exercise on the connective tissues of the body, especially systemic effects. We trained male Sprague-Dawley rats in a treadmill from the age of 5 months to 23 months. We analyzed the effects of training on tail tendons with respect to thermal stability of collagen and biomechanical properties of tendon bundles. Although tail tendons are attached to muscles, the are not weight-bearing as limb muscle tendons and can, therefore, be considered to be subjected mainly to systemic effects. The thermal stability of tail tendon collagen was significantly lower or ‘younger’ for the trained group compared with the sedentary one. The biomechanical parameters were likewise ‘younger’ with respect to maximum stress, although considerably stiffer compared with a 5-month-old base-line group. This suggests that there are several mechanisms, elicited by physical excercise, that act on the connective tissues. It can be concluded that life-long physical exercise has a beneficial influence on the connective tissues of the maturing and aging organism.

References (37)

T.T. Andreassen et al.
Thermal stability, mechanical properties and reducible cross-links of rat tail tendon in experimental diabetes
Biochim. Biophys. Acta
(1981)
M. Skalicky et al.
Influence of physical exercise on aging rats: I. Life-long exercise preserves patterns of spontaneous activity
Mech. Ageing Dev.
(1996)
A. Viidik
Connective tissues—possible implications of the temporal changes for the aging process
Mech. Ageing Dev.
(1979)
A. Viidik
Functional properties of collagenous tissues
E. Heikkinen et al.
Socioeconomic and life-style factors as modulators of health and functional capacity with age
W.W. Spirduso
Physical activity and aging: retrospections and visions for the future
J. Aging Phys. Activity
(1994)
R.S. Paffenbarger et al.
Physical activity, all-cause mortality, and longevity of college alumni
N. Engl. J. Med.
(1986)
S. Blair et al.
Physical fitness and all cause mortality: A prospective study of men and women
J. Am. Med. Assoc.
(1989)
J.O. Holloszy
Minireview: Exercise and longevity: Studies on rats
J. Gerontol.
(1988)
A. Viidik
Age-related changes in connective tissues

H.G. Vogel

Mechanical properties of rat skin with aging

A.J. Bailey

Metabolism of collagen and elastin

A.J. Bailey

The chemistry od natural enzyme-induced cross-links of prroteins

Amino Acids

(1991)

A. Viidik

Adaptablilty of connective tissues

S.L.-Y. Woo et al.

The biomechanical and biochemical properties of swine tendons—long term effects of exercise on the digital extensors

Connect. Tissue Res.

(1980)

S.L.-Y. Woo et al.

Mechanical properties of tendons and ligaments. II. The relationship between immobilization and exercise on tissue remodeling

Biorheology

(1982)

A. Kiiskinen

Physical training and connective tissues in young mice. Physical properties of Achilles tendons and long bones

Growth

(1977)

H. Suominen et al.

Physical and chemical properties of skin in habitually trained and sedentary 31- to 70-year-old men

Br. J. Dermatol.

(1978)

Cited by (44)

An integrated approach to investigate age-related modifications of morphological, mechanical and structural properties of type I collagen
2022, Acta Biomaterialia
Citation Excerpt :
The changes in tissue mechanical properties could be a combination between alteration of pre-existing collagen fibers and a progressive delay in their maturation, both dues to aging [25–27]. Viidik et al. have reported a clear relationship between mechanical properties of tendons (Young's modulus) and age [28]. The age related changes in mechanical properties of other connective tissues have been correlated with their morphological and biochemical changes [29,30] and mechanical properties such as collagen density [16,31].
The main propose of this study is to characterize the impact of chronological aging on mechanical, structural, biochemical, and morphological properties of type I collagen. We have developed an original approach combining a stress-strain measurement device with a portable Raman spectrometer to enable simultaneous measurement of Raman spectra during stress vs strain responses of young adult, adult and old rat tail tendon fascicles (RTTFs). Our data showed an increase in all mechanical properties such as Young's modulus, yield strength, and ultimate tensile strength with aging. At the molecular level, Raman data revealed that the most relevant frequency shift was observed at 938 cm⁻¹ in Old RTTFs, which is assigned to the C–C. This suggested a long axis deformation of the peptide chains in Old RTTFs during tensile stress. In addition, the intensity of the band at 872 cm⁻¹, corresponding to hydroxyproline decreased for young adult RTTFs and increased for the adult ones, while it remained unchanged for Old RTTFs during tensile stress. The amide III band (1242 and 1265 cm⁻¹) as well as the band ratios I₁₆₃₁/ I₁₆₆₃ and I₁₆₄₅ / I₁₆₆₃ responses to tensile stress were depending on mechanical phases (toe, elastic and plastic). The quantification of advanced glycation end-products by LC-MS/MS and spectrofluorometry showed an increase in their content with aging. This suggested that the accumulation of such products was correlated to the alterations observed in the mechanical and molecular properties of RTTFs. Analysis of the morphological properties of RTTFs by SHG combined with CT-FIRE software revealed an increase in length and straightness of collagen fibers, whereas their width and wavy fraction decreased. Our integrated study model could be useful to provide additional translational information to monitor progression of diseases related to collagen remodeling in musculoskeletal disorders.
Type I collagen is the major component of the extracellular matrix. Its architectural and structural organization plays an important role in the mechanical properties of many tissues at the physiological and pathological levels. The objective of this work is to develop an integrated approach to bring a new insight on the impact of chronological aging on the structural organization and mechanical properties of type I collagen. We combined a portable Raman spectrometer with a mechanical tensile testing device in order to monitor in real time the changes in the Raman fingerprint of type I collagen fibers during the mechanical stress. Raman spectroscopy allowed the identification of the type I collagen bonds that were affected by mechanical stress in a differential manner with aging.
The mechanical and biochemical properties of tail tendon in a rat model of obesity: Effect of moderate exercise and prebiotic fibre supplementation
2019, Journal of Biomechanics
Citation Excerpt :
However, little is known about the effects of chronic exercise on non-weight bearing tendons in young and old animals. Viidik et al. (1996) reported a decrease in tail tendon Young’s modulus in older animals as we observed here in the present study (Viidik et al., 1996). But the mechanism behind this change is not well understood.
The worldwide trajectory of increasing obesity rates is a major health problem precipitating a rise in the prevalence of a variety of co-morbidities and chronic diseases. Tendinopathy, in weight and non-weight bearing tendons, in individuals with overweight or obesity has been linked to metabolic dysfunction resulting from obesity. Exercise and dietary fibre supplementation (DFS) are common countermeasures to combat obesity and therefore it seems reasonable to assume that they might protect tendons from structural and mechanical damage in a diet-induced obesity (DIO) model. The purpose of this study was to determine the effects of a DIO, DIO combined with moderate exercise, DIO combined with DFS (prebiotic oligofructose), and DIO combined with moderate exercise and DFS on the mechanical and biochemical properties of the rat tail tendon. Twenty-four male Sprague-Dawley rats, fed a high-fat/high-sucrose diet were randomized into a sedentary, a moderate exercise, a DFS, or a moderate exercise combined with DFS group for 12 weeks. Additionally, six lean age-matched animals were included as a sedentary control group. DIO in combination with exercise alone and with exercise and DFS reduced the Young’s Modulus but not the collagen content of the rat tail tendons compared to lean control animals. However, no differences in the mechanical and biochemical properties of the rat tail tendon were detected between the DIO and the lean control group, suggesting that DIO by itself did not impact the tail tendon. It seems that longer DIO exposure periods may be needed to develop overt differences in our DIO model.
Muscle deconditioning and aging: Experimental models
2018, Conn's Handbook of Models for Human Aging
Sarcopenia is a well-described phenomenon, mainly characterized by a loss of muscle mass, together with a loss of strength and muscle power. However, an accepted consensus definition of sarcopenia by scientists and clinicians is still under debate as well as its diagnostic criteria. Identification of cost-effective interventions to maintain muscle mass, muscle strength, and physical performance during muscle wasting and aging is an important public health challenge. It requires understanding of the cellular and molecular mechanisms involved. Muscle deconditioning processes have been deciphered by means of several experimental models, bringing together the opportunities to devise comprehensive analysis of muscle wasting. The present chapter is aimed at addressing two main points. First, we mainly focus on the actual definitions of sarcopenia and its diagnostic criteria. The second part points out different models to study sarcopenia or muscle wasting.
Muscle wasting and aging: Experimental models, fatty infiltrations, and prevention
2016, Molecular Aspects of Medicine
Citation Excerpt :
The animals most frequently used for studying intervention strategies against skeletal-muscle aging are rats and mice. Yet even in rodents, life-long interventions still require 18–26 months of follow-up and are therefore costly and time-consuming (Kovanen and Suominen, 1987; Leeuwenburgh et al., 1997; Viidik et al., 1996). Senescence-accelerated mice (SAM) represent rodent models characterized by accelerated senescence and age-related pathologies (Takeda, 1999).
Identification of cost-effective interventions to maintain muscle mass, muscle strength, and physical performance during muscle wasting and aging is an important public health challenge. It requires understanding of the cellular and molecular mechanisms involved. Muscle-deconditioning processes have been deciphered by means of several experimental models, bringing together the opportunities to devise comprehensive analysis of muscle wasting. Studies have increasingly recognized the importance of fatty infiltrations or intermuscular adipose tissue for the age-mediated loss of skeletal-muscle function and emphasized that this new important factor is closely linked to inactivity. The present review aims to address three main points. We first mainly focus on available experimental models involving cell, animal, or human experiments on muscle wasting. We next point out the role of intermuscular adipose tissue in muscle wasting and aging and try to highlight new findings concerning aging and muscle-resident mesenchymal stem cells called fibro/adipogenic progenitors by linking some cellular players implicated in both FAP fate modulation and advancing age. In the last part, we review the main data on the efficiency and molecular and cellular mechanisms by which exercise, replacement hormone therapies, and β-hydroxy-β-methylbutyrate prevent muscle wasting and sarcopenia. Finally, we will discuss a potential therapeutic target of sarcopenia: glucose 6-phosphate dehydrogenase.
Elastin content is high in the canine cruciate ligament and is associated with degeneration
2014, Veterinary Journal
Citation Excerpt :
Collagen fibril size distribution changes with age in all extraocular tissue contributing to increased strength (Parry et al., 1978). Furthermore, the mechanical environment can affect ligament structure and strength (Parry et al., 1978; Davankar et al., 1996) and exercise can induce local and systemic change to tendon and ligament (Woo et al., 1980, 1981; Viidik et al., 1996; Nielsen et al., 1998). Given that all of our dogs had been in training within the previous 6 months, we believe that the increase in collagen reflects both age and the influence of training.
Cruciate ligaments (CLs) are primary stabilisers of the knee joint and canine cranial cruciate ligament disease (CCLD) and rupture is a common injury. Elastin fibres, composed of an elastin core and fibrillin containing microfibrils, are traditionally considered minor components of the ligament extracellular matrix (ECM). However, their content and distribution in CLs is unknown. The purposes of this study were to determine the elastin content of canine CLs and to ascertain its relationship to other biochemical components and histological architecture.
Macroscopically normal CLs were harvested from Greyhounds (n = 11), a breed with a low risk of CCLD. Elastin, collagen and sulfated glycosaminoglycan content were measured and histological scoring systems were developed to quantify ECM changes using a modified Vasseur score (mVS) and oxytalan fibre (bundles of microfibrils) staining. Elastin contents were 9.86 ± 3.97% dry weight in the cranial CL and 10.79 ± 4.37% in the caudal CL, respectively, and did not alter with advancing histological degeneration. All CLs demonstrated mild degenerative changes, with an average mVS score of 11.9 ± 3.3 (maximum 24). Increasing degeneration of the ligament ECM showed a positive correlation (r = 0.690, P < 0.001) with increased oxytalan fibre staining within the ECM.
Elastin is an abundant protein in CLs forming a greater proportion of the ligament ECM than previously reported. The appearance of oxytalan fibres in degenerative CL ECM may reflect an adaptive or reparative response to normal or increased loads. This finding is important for future therapeutic or ligament replacement strategies associated with cranial CL injury.
Collagen type I amide I band infrared spectroscopy
2011, Micron
Citation Excerpt :
In spite of this, physical exercise is considered an effective factor in delaying aging in rat tendon collagen, and tendons of trained animals are clearly stiffer than untrained animals (Vilarta and Vidal, 1989). Inter-fibrillar proteoglycans may also play a role in the biomechanical properties of the tendon (Viidik et al., 1996; Singh, 2000; Boskey and Camacho, 2007) as proteoglycans are oriented in tendons (Vidal, 1965, 1986, 2003; Mello and Vidal, 2003) and participate in the control of collagen fiber diameter determined by decorin (Kjaer, 2004; Boskey and Camacho, 2007). In conclusion, the macromolecularly oriented tendon collagen fibers analyzed in this study showed FT-IR amide band I width and peaks consistent with the collagen fiber composition and its supraorganizational characteristics and properties.
Collagen fiber structure and organization have been found to vary in different tendon types. Differences have been reported in the FT-IR spectra of the amide I band of collagen-containing structures. In the present study, the FT-IR spectral characteristics of the amide I band of the bovine flexor tendon and the extended rat tail tendon were compared by using the diamond attenuated total reflectance technique. The objective was to associate FT-IR spectral characteristics in tendons with their different collagen fiber supraorganization and biomechanical properties. Nylon 6 and poly-l-lysine were used as polyamide models. Each of these materials was found to exhibit molecular order and crystallinity, as revealed by their birefringence. The following FT-IR parameters were evaluated: amide I band profile, absorption peaks and areas, and the 1655 cm⁻¹/1690 cm⁻¹ absorbance ratio. The amide I area and the 1655 cm⁻¹/1690 cm⁻¹ absorbance ratio were significantly higher for the bovine flexor tendon, indicating that its collagen fibers are richer in pyridinoline-type cross-linking, proline and/or hydroxyproline and H-bonding, and that these fibers are more packed and supraorganizationally ordered than those in the rat tail tendon. This conclusion is additionally supported by differences in collagen solubility and biochemical/biomechanical properties of the tendons.

View all citing articles on Scopus

View full text

Influence of physical exercise on aging rats: II. Life-long exercise delays aging of tail tendon collagen

Abstract

Biochim. Biophys. Acta

Mech. Ageing Dev.

Mech. Ageing Dev.

Socioeconomic and life-style factors as modulators of health and functional capacity with age

Physical activity and aging: retrospections and visions for the future

J. Aging Phys. Activity

Physical activity, all-cause mortality, and longevity of college alumni

N. Engl. J. Med.

Physical fitness and all cause mortality: A prospective study of men and women

J. Am. Med. Assoc.

Minireview: Exercise and longevity: Studies on rats

J. Gerontol.

Age-related changes in connective tissues