Structural and biochemical alterations during the healing process of tendons treated with Aloe vera

Life Sciences

Volumn 91, Issue 17-18, 2012, Pages 885-893

  Aro, A A ^a   Nishan, U ^a,b   Perez, M O ^a   Rodrigues, R A ^a   Foglio, M A ^a   Carvalho, J E ^a   Gomes, L ^a   Vidal, B C ^a   Pimentel, E R ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Aloe vera; Collagen; Healing process; Rat; Tendon

Indexed keywords

ALOE VERA EXTRACT; COLLAGEN TYPE 1; GELATINASE A; GELATINASE B; HYDROXYPROLINE;

ACHILLES TENDON; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIREFRINGENCE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; MALE; NONHUMAN; OINTMENT; POLARIZATION MICROSCOPY; PROTEIN EXPRESSION; RAT; TENDON INJURY; TISSUE REPAIR; WESTERN BLOTTING; ZYMOGRAPHY;

ALOE; ANIMALS; COLLAGEN; HYDROXYPROLINE; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; OINTMENTS; PHYTOTHERAPY; PLANT PREPARATIONS; RATS; RATS, WISTAR; TENDON INJURIES; TENDONS; WOUND HEALING;

ALOE VERA; ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 84867577475     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2012.09.002     Document Type: Article

References (90)

1. M.S. Agren Gelatinase activity during wound healing Br J Dermatol 131 5 1994 634 640
2. R.T. Aimes, and J.P. Quigley Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments J Biol Chem 270 11 1995 5872 5886
3. L.C. Almekinders, and S.V. Almekinders Outcome in the treatment of chronic overuse sports injuries: a retrospective study J Orthop Sports Phys Ther 19 1994 157 161
4. D.G. Armstrong, and E.B. Jude The role of matrix metalloproteinases in wound healing J Am Podiatr Med Assoc 92 2002 12 18
5. A.A. Aro, B.C. Vidal, A. Biancalana, F.T. Tolentino, L. Gomes, and S.M. Mattiello Analysis of the deep digital flexor tendon in rats submitted to stretching after immobilization Connect Tissue Res 53 1 2012 29 38
6. A.A. Aro, B.C. Vidal, and E.R. Pimentel Biochemical and anisotropical properties of tendons Micron 43 2012 205 214
7. A.A. Aro, B.C. Vidal, T.C. Tomiosso, L. Gomes, S.M. Mattiello, and E.R. Pimentel Structural and biochemical analysis of the effect of immobilization followed by stretching on the Achilles tendon of rats Connect Tissue Res 49 2008 443 454
8. A. Atiba, M. Nishimura, S. Kakinuma, T. Hiraoka, M. Goryo, and Y. Shimada Aloe vera oral administration accelerates acute radiation-delayed wound healing by stimulating transforming growth factor-β and fibroblast growth factor production Am J Surg 201 6 2011 809 818
9. M. Benjamin, R.N.S. Tyers, and J.R. Ralphs Age-related changes in tendon fibro-cartilage J Anat 179 1991 127 136
10. M.E. Berglund, D.A. Hart, C. Reno, and M. Wiig Growth factor and protease expression during different phases of healing after rabbit deep flexor tendon repair J Orthop Res 29 6 2011 886 892
11. S. Bolkent, N. Akev, N. Ozsoy, M. Sengezer-Inceli, A. Can, and O. Alper Effect of Aloe vera (L.) Burm. fil. leaf gel and pulp extracts on kidney in type-II diabetic rat models Indian J Exp Biol 42 1 2004 48 52
12. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
13. H.F. Carvalho, S.L. Felisbino, K. Vogel, and K. Douglas Identification, content and distribution of type VI collagen in bovine tendons Cell Tissue Res 325 2 2006 315 324
14. P. Chithra, G.B. Sajithlal, and G. Chandrakasan Influence of Aloe vera on the healing of dermal wounds in diabetic rats J Ethnopharmacol 59 1998 195 201
15. P. Chithra, G.B. Sajithlal, and G. Chandrakasan Influence of Aloe vera on collagen characteristics in healing dermal wounds in rats Mol Cell Biochem 181 1998 71 76
16. P. Chithra, G.B. Sajithlal, and G. Chandrakasan Influence of Aloe vera on collagen turnover in healing of dermal wounds in rats Indian J Exp Biol 36 9 1998 896 901
17. S.W. Choi, B.W. Son, Y.I. Son, Y.I. Park, S.K. Lee, and M.H. Chung The wound-healing effect of a glycoprotein fraction isolated from aloe vera Br J Dermatol 145 4 2001 535 545
18. I.E. Collier, S.M. Wilhelm, A.Z. Eisen, B.L. Marmer, G.A. Grant, and J.L. Seltzer H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen J Biol Chem 263 14 1998 6579 6587
19. R.H. Davis, G.J. Stewart, and P.J. Bregman Aloe vera and the inflamed synovial pouch model J Am Podiatr Med Assoc 82 3 1992 140 148
20. K. Eamlamnam, S. Patumraj, N. Visedopas, and D. Thong-Ngam Effects of Aloe vera and sucralfate on gastric microcirculatory changes, cytokine levels and gastric ulcer healing in rats World J Gastroenterol 12 13 2006 2034 2049
21. D.R. Eyre, M.A. Paz, and P.M. Gallop Crosslinks in collagen and elastin Annu Rev Biochem 53 1984 717 748
22. M. Favata, P.K. Beredjiklian, M.H. Zgonis, D.P. Beason, T.M. Crombleholme, and A.F. Jawad Regenerative properties of fetal sheep tendon are not adversely affected by transplantation into an adult environment J Orthop Res 24 2006 2124 2132
23. S.L. Felisbino, and H.F. Carvalho Identification na distribution type VI collagen in tendon fibrocartilages J Submicrosc Cytol Pathol 31 2 1999 187 195
24. F. Habeeb, G. Stables, F. Bradbury, S. Nong, P. Cameron, and R. Plevin The inner gel component of Aloe vera suppresses bacterial-induced pro-inflammatory cytokines from human immune cells Methods 42 4 2007 388 393
25. A.N. Hanson, and J.P. Bentley Quantitation of type I and type III collagen ratios in small samples of human tendon, blood vessels and atherosclerotic plaque Anal Biochem 130 1983 32 40
26. E.D. Hay Cell biology of extracellular mtix Collagen types 2nd edition 1991 Plenum Press New York 18 39
27. D. Heinegård, and Y. Sommarin Isolation and characterization of proteoglycans Methods Enzymol 144 1987 319 373
28. C.J. Hooley, and R.E. Cohen A model for the creep behaviour of tendon Int J Biol Macromol 1 1979 123 132
29. H.F. Huseini, S. Kianbakht, R. Hajiaghaee, and F.H. Dabaghian Anti-hyperglycemic and anti-hypercholesterolemic effects of Aloe vera leaf gel in hyperlipidemic Type 2 diabetic patients: a randomized double-blind placebo-controlled clinical trial Planta Med 78 4 2012 311 316
30. L.G. Józsa, and P. Kannus Human tendons: anatomy, physiology and pathology Structure and Metabolism of Normal Tendons 1997 Human Kinetics, Champaign 46 95
31. J.C. Jung, P.X. Wang, G. Zhang, Y. Ezura, M.E. Fini, and D.E. Birk Collagen fibril growth during chicken tendon development: matrix metalloproteinase-2 and its activation Cell Tissue Res 336 2009 79 89
32. M.P. Jorge, C. Madjarof, A.L.T.G. Ruiz, A.T. Fernandes, R.A.F. Rodrigues, and I.M.O. Sousa Evaluation of wound healing properties of Arrabidaea chica Verlot extract J Ethnopharmacol 188 2008 361 366
33. J. Kim, I. Lee, S. Park, and R. Choue Effects of Scutellariae radix and Aloe vera gel extracts on immunoglobulin E and cytokine levels in atopic dermatitis NC/Nga mice J Ethnopharmacol 132 2 2010 529 532
34. M. Kjaer Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading Physiol Rev 84 2 2004 649 698
35. A. Lesic, and M. Bumbasirevic Disorders of the Achilles tendon Curr Orthop 18 2004 63 75
36. B.O. Lim, N.S. Seong, R.W. Choue, J.D. Kim, H.Y. Lee, and S.Y. Kim Efficacy of dietary Aloe vera supplementation on hepatic cholesterol and oxidative status in aged rats J Nutr Sci Vitaminol 49 4 2003 292 296
37. T.W. Lin, L. Cardena, and L.J. Soslowsky Biomechanics of tendon injury and repair J Biomech 37 2004 865 877
38. S.H. Liu, R.S. Yang, R. al-Shaikh, and J.M. Lane Collagen in tendon, ligament, and bone healing. A current review Clin Orthop Relat Res 318 1995 265 278
39. M. Madlener Differential expression of matrix metalloproteinases and their physiological inhibitors in acute murine skin wounds Arch Dermatol Res 290 Suppl. 1998 S24 S29
40. R. Maenthaisong, N. Chaiyakunapruk, S. Niruntraporn, and C. Kongkaew The efficacy of aloe vera used for burn wound healing: a systematic review Burns 33 6 2007 713 718
41. A.L. Maia Filho, A.B. Villaverde, E. Munin, F. Aimbire, and R. Albertini Comparative study of the topical application of Aloe vera gel, therapeutic ultrasound and phonophoresis on the tissue repair in collagenase-induced rat tendinitis Ultrasound Med Biol. 36 10 2010 1682 1690
42. M. Magra, and N. Maffulli Matrix metalloproteases: a role in overuse tendinopathies Br J Sports Med 39 11 2005 789 791
43. R.C. Marqueti, N.A. Parizotto, R.S. Chriguer, S.E. Perez, and H.S. Celistre-de-Araujo Androgenic-anabolic steroids associated with mechanical loading inhibit matrix metallopeptidase activity and affect the remodeling of the Achilles tendon in rats Am J Sports Med 34 2006 1274 1280
44. C.A. Matthew, and M.J. Moore Regeneration of rat extensor digitorum longus tendon: the effect of a sequential partial tenotomy on collagen fibril formation Matrix 11 4 1991 259 268
45. L.J. McCawley, and L.M. Matrisian Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 13 2001 534 540
46. M.L. Mello, C. Godo, B.C. Vidal, and J.M. Abujadi Changes in macromolecular orientation on collagen fibers during of tendon repair in the rat Ann Histochim 20 1975 145 152
47. M.L.S. Mello, and B.C. Vidal Experimental tendon repair: glycosaminoglycan arrangement in newly synthesized collagen fibers Cell Mol Biol 49 4 2003 579 585
48. F. Montico, A.C. Hetzl, E.M. Cândido, W.J. Fávaro, and V.H.A. Cagnon Hormonal therapy in the senescence: prostatic microenvironment structure and adhesion molecules (2011) Micron 42 6 2011 642 655
49. G. Muller, A. Michel, and E. Altenburg Comp (cartilage oligomeric matrix protein) is synthesized in ligament, tendon, meniscus, and cartilage Connect Tissue Res 39 1998 233 244
50. P.G. Murphy, C.B. Frank, and D.A. Hart The cell biology of ligaments and ligament healing D.W. Jackson, The anterior cruciate ligament: current and future concepts 1994 Raven Press New York
51. P.G. Murphy, B.J. Loitz, C.B. Frank, and D.A. Hart Influence of exogenous growth factors on the synthesis and secretion of collagen types I and III by explants of normal and healing rabbit ligaments Biochem Cell Biol 72 1994 403 409
52. M. Ni, P.P.Y. Lui, Y.F. Rui, Y.W. Lee, Y.W. Lee, and Q. Tan Tendon-derived stem cells (TDSCs) promote tendon repair in a rat patellar tendon window defect model J Orthop Res 30 4 2011 613 619
53. Y. Ni, D. Turner, K.M. Yates, and I. Tizard Isolation and characterization of structural components of Aloe vera L. leaf pulp Int Immunopharmacol 4 14 2004 1745 1755
54. B.W. Oakes Tissue healing and repair: tendons and ligaments W.R. Frontera, Rehabilitation of sports injuries: scientific basis 2003 Blackwell Science Boston 56 98
55. A. Okyar, A. Can, N. Akev, G. Baktir, and N. Sütlüpinar Effect of Aloe vera leaves on blood glucose level in type I and type II diabetic rat models Phytother Res 15 2 2001 157 161
56. W. Oshiro, J. Lou, X. Xing, Y. Tu, and P.R. Manske Flexor tendon healing in the rat: a histologic and gene expression study J Hand Surg Am 28 2003 814 823
57. A. Pajala, J. Melkko, J. Leppilahti1, P. Ohtonen, Y. Soini, and J. Risteli Tenascin-C and type I and III collagen expression in total Achilles tendon rupture. An immunohistochemical study Histol Histopathol 24 2009 1207 1211
58. L. Palma, A. Gigante, and S. Rapali Physiopathology of the repair process of lesions of Achilles tendon Foot Ankle Surg 12 2006 5 11
59. C.H. Park, D.Y. Nam, H.U. Son, S.R. Lee, H.J. Lee, and J.C. Heo Polymer fraction of Aloe vera exhibits a protective activity on ethanol-induced gastric lesions Int J Mol Med 27 4 2011 511 518
60. R. Prabjone, D. Thong-Ngam, N. Wisedopas, T. Chatsuwan, and S. Patumraj Anti-inflammatory effects of Aloe vera on leukocyte-endothelium interaction in the gastric microcirculation of Helicobacter pylori-infected rats Clin Hemorheol Microcirc 35 3 2006 359 366
61. G.P. Riley, R.L. Harrall, T.E. Cawston, B.L. Hazleman, and E.J. Mackie Tenascin-C and human tendon degeneration Am J Pathol 149 1996 933 943
62. M.G.Q. Rodríguez, M.C.S. Baró, and M. Batista Extracto de Aloe Barbadensis inyectable em fracturas experimentales Rev Cubana Plant Med 7 1 2002 14 17
63. A. Rufai, M. Benjamin, and J.R. Ralphs Development and aging of phenotypically distinct fibrocartilage associated with the rat Achilles tendon Anat Embryol 186 1992 611 618
64. M. Saini, P.K. Goyal, and G. Chaudhary Anti-tumor activity of Aloe vera against DMBA/croton oil-induced skin papillomagenesis in Swiss albino mice J Environ Pathol Toxicol Oncol 29 2 2010 127 135
65. J.A.F. Silva, M. Lorencini, L.A. Peroni, C.L.R. De La Hoz, H.F. Carvalho, and D.R. Stach-Machado The influence of type I diabetes mellitus on the expression and activity of gelatinases (matrix metalloproteinases-2 and -9) in induced periodontal disease J Periodontal Res 43 2008 48 54
66. P. Sharma, and N. Maffulli Tendon injury and tendinopathy: healing and repair J Bone Joint Surg Am 87 2005 187 202
67. J. Somboonwong, S. Thanamittramanee, A. Jariyapongskul, and S. Patumraj Therapeutic effects of Aloe vera on cutaneous microcirculation and wound healing in second degree burn model in rats J Med Assoc Thai 83 4 2000 417 425
68. H. Stegemann, and K. Stalder Determination of hydroxyproline Clin Chim Acta 18 2 1967 267 273
69. M. Takahashi, D. Kitamoto, Y. Asikin, K. Takara, and K. Wada Liposomes encapsulating Aloe vera leaf gel extract significantly enhance proliferation and collagen synthesis in human skin cell lines J Oleo Sci 58 12 2009 643 650
70. N. Takzare, M.J. Hosseini, G. Hasanzadeh, H. Mortazavi, A. Takzare, and P. Habibi Influence of Aloe vera gel on dermal wound healing process in rat Toxicol Mech Methods 19 1 2009 73 77
71. M. Tarameshloo, M. Norouzian, S. Zarein-Dolab, M. Dadpay, and R. Gazor A comparative study of the effects of topical application of Aloe vera, thyroid hormone and silver sulfadiazine on skin wounds in Wistar rats Lab Anim Res 28 1 2012 17 21
72. S.H. Taylor, S. Al-Youha, T. Van Agtmael, Y. Lu, J. Wong, and D.A. McGrouther Tendon is covered by a basement membrane epithelium that is required for cell retention and the prevention of adhesion formation PLoS One 6 1 2011 e16337
73. S. Thomopoulos, G. Hattersley, V. Rosen, M. Mertens, L. Galatz, and G.R. Williams The localized expression of extracellular matrix components in healing tendon insertion sites: an in situ hybridization study J Orthop Res 20 2002 454 463
74. R. Tomasin, and M.C. Gomes-Marcondes Oral administration of Aloe vera and honey reduces Walker tumour growth by decreasing cell proliferation and increasing apoptosis in tumour tissue Phythoter Res 25 4 2011 619 623
75. T.C. Tomiosso, W.R. Nakagaki, L. Gomes, S. Hyslop, and E.R. Pimentel Organization of collagen bundles during tendon healing in rats treated with L-NAME Cell Tissue Res 337 2009 235 242
76. T. Towbin, and S. Gordon Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications Proc Natl Acad Sci U S A 76 1979 4350 4354
77. C.E. Turner, D.A. Williamson, P.A. Stroud, and D.J. Talley Evaluation and comparison of commercially available Aloe vera L. Products using size exclusion chromatography with refractive index and multi-angle laser light scattering detection Int Immunopharmacol 4 14 2004 1727 1737
78. B.C. Vidal, and M.L.S. Mello Structural organization of collagen fibers in chordate tendineae as assessed by optical anisotropic properties and Fast Fourier transform J Struct Biol 167 2009 166 175
79. B.C. Vidal The part played by proteoglycans and structural lycoproteins in the macromolecular orientation of collagen bundles Cell Mol Biol 26 1980 415 421
80. B.C. Vidal Evaluation of the carbohydrate role in the molecular order of collagen bundles. Microphotometric measurements of textural birefringence Cell Mol Biol 32 1986 527 535
81. B.C. Vidal Crimp as part of helical structure Biochemistry 318 1995 173 178
82. B.C. Vidal, and M.L.S. Mello Proteoglycan arrangement in tendon collagen bundles Cell Mol Biol 30 1984 195 204
83. B.C. Vidal, and M.L.S. Mello Optical anisotropy of collagen fibers of rat calcaneal tendons: an approach to spatially resolved supramolecular organization Acta Histochem 112 2010 53 61
84. C.P. Vieira, A.A. Aro, M.S. Almeida, G.C. Mello, E. Antunes, and E.R. Pimentel Effects of acute inflammation induced in the rat paw on the deep digital flexor tendon Connect Tissue Res 53 2 2012 160 168
85. D. Vijayalakshmia, R. Dhandapanib, S. Jayavenia, P.S. Jithendraa, C. Rosea, and A.B. Mandala In vitro anti inflammatory activity of Aloe vera by down regulation of MMP-9 in peripheral blood mononuclear cells J Ethnopharmacol 141 1 2012 542 546
86. K.G. Vogel, and D. Heinegård Characterization of proteoglycans from adult bovine tendon J Biol Chem 260 1985 298 306
87. J.H. Wang, Q. Guo, and B. Li Tendon biomechanics and mechanobiology - a minireview of basic concepts and recent advancements J Hand Ther 25 2 2012 133 141
88. D.P. West, and Y.F. Zhu Evaluation of Aloe vera gel gloves in the treatment of dry skin associated with occupational exposure Am J Infect Control 31 1 2003 40 42
89. S.M. Wilhelm, I.E. Collier, B.L. Marmer, A.Z. Eisen, G.A. Grant, and G.I. Goldberg SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages J Biol Chem 264 29 1989 17213 17221
90. J.F. Woessner, and H. Nagase Matrix metalloproteinases and TIMPs: protein profile 2000 Oxford University Press Oxford