Variations in Apelin Expression Levels during Achilles Tendon Healing

Derya Çırakoğlu; Alper Çıraklı; Havva Erdem; Erdal Uzun; Mürüvvet Akçay Çelik

doi:10.19127/mbsjohs.873010

Research Article

Year 2021, Volume: 7 Issue: 1, 57 - 63, 30.04.2021

Derya Çırakoğlu Alper Çıraklı Havva Erdem Erdal Uzun Mürüvvet Akçay Çelik

https://doi.org/10.19127/mbsjohs.873010

Abstract

References

1. Pennisi E. Tending tender tendons. Science 2002; 295 (5557): 1011.
2. Liu CF, Aschbacher-Smith L, Barthelery NJ, Dyment N, Butler D, Wylie C. What We Should Know Before Using Tissue Engineering Techniques to Repair Injured Tendons: A Developmental Biology Perspective. Tissue Eng Part B-Rev 2011; 17(3): 165–76. 3. Hope M, Saxby TS. Tendon healing. Foot and ankle clinics. 2007; 12(4): 553–67.
4. Voleti PB, Buckley MR, Soslowsky LJ. Tendon healing: repair and regeneration. Annu Rev Biomed Eng 2012; 14: 47–71. 5. Hays PL, Kawamura S, Deng XH, Dagher E, Mithoefer K, Ying L et al. The role of macrophages in early healing of a tendon graft in a bone tunnel. J Bone Joint Surg Am 2008; 90(3): 565-79.
6. Sugg KB, Lubardic J, Gumucio JP, Mendias CL. Changes in macrophage phenotype and induction of epithelial-to-mesenchymal transition genes following acute Achilles tenotomy and repair. J Orthop Res 2014; 32: 944–51.
7. Lichtnekert J, Kawakami T, Parks WC, Duffield JS. Changes in macrophage phenotype as the immune response evolves. Curr Opin Pharmacol 2013; 13(4): 555-64.
8. Tatemoto K, Hosoya M, Habata Y, Fujii R, Kakegawa T, Zou MX, et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor, Biochem. Biophys. Res. Commun 1998; 251(2): 471-76.
9. Pitkin SL, Maguire JJ, Bonner TI, Davenport AP. Apelin receptor nomenclature, distribution, pharmacology, and function. Pharmacol Rev 2010; 62(3): 331–42.
10. Ghosh AK, Quaggin SE, Vaughan DE. Molecular basis of organ fibrosis: potential therapeutic approaches. Exp Biol Med 2013; 238: 461–81.
11. Brand T, Schneider MD. The TGF beta superfamily in myocardium: ligands, receptors, transduction and function. J Mol Cell Cardiol 1995; 27: 5–18.
12. Brand T, Schneider MD. Transforming growth factor-beta signal transduction. Circ Res 1996; 78: 173–79.
13. Calleja M, Connell DA. The achilles tendon. Seminars in Musculoskeletal Radiology 2010; 14(3): 307–22.
14. Andia I, Sanchez M, Maffulli N. Tendon healing and platelet-rich plasma therapies. Expert Opinion on Biological Therapy 2010; 10(10): 1415–26.
15. Chen B, Wang B, Zhang WJ, Zhou G, Cao Y, Liu W. In vivo tendon engineering with skeletal muscle derived cells in a mouse model. Biomaterials 2012; 33(26): 6086–97.
16. Chen CH, Cao Y, Wu YF, Bais AJ, Gao JS, Tang JB. Tendon healing ın vivo: Gene expression and production of multiple growth factors in early tendon healing period. The Journal of Hand Surgery 2008; 33(10): 1834–42. 17. Wurgler-Hauri CC, Dourte LM, Baradet TC, Williams GR, Soslowsky LJ. Temporal expression of 8 growth factors in tendon-to-bone healing in a rat supraspinatus model. J Shoulder Elbow Surg 2007; 16(5): 198–203.
18. Docheva D, Müller SA, Majewski M, Evans CH. Biologics for tendon repair. Adv Drug Deliv Rev. 2015; 84: 222–39.
19. Zhang G, Young BB, Ezura Y, Favata M, Soslowsky LJ, Chakravarti S, et al. Development of tendon structure and function: regulation of collagen ﬁbrillogenesis. J Musculoskelet Neuronal Interact 2005; 5(1): 5–21.
20. Riley G. The pathogenesis of tendinopathy: a molecular perspective. Rheumatology (Oxford) 2004; 43(2): 131–42.
21. Lorda-Diez CI, Montero JA, Martinez-Cue C, Garcia-Porrero JA, Hurle JM. Transforming growth factors β coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J Biol Chem 2009; 284(43): 29988–96.
22. Pryce BA, Watson SS, Murchison ND, Staverosky JA, Dunker N, Schweitzer R. Recruitment and maintenance of tendon progenitors by TGFβ signaling are essential for tendon formation. Development 2009; 136(8): 1351–61
23. Murchison ND, Price BA, Conner DA, Keene DR, Olson EN, Tabin CJ, et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 2007; 134(14): 2697–708.
24. Guerquin MJ, Charvet B, Nourissat G, Havis E, Ronsin O, Bonnin MA et al. Transcription factor EGR1 directs tendon differentiation and promotes tendon repair. J Clin Invest 2013; 123(8): 3564–76.
25. Liu W, Watson SS, Lan Y, Keene DR, Ovitt CE, Liu H et al. The atypical homeodomain transcription factor Mohawk controls tendon morphogenesis. Mol Cell Biol 2010; 30(20): 4797–807.
26. Huang S, Chen L, Lu L, Li L. The apelin-APJ axis: A novel potential therapeutic target for organ fibrosis. Clin Chim Acta. 2016; 456(1): 81-88.
27. Wang LY, Diao ZL, Zhang DL, Zheng JF, Zhang QD, Ding JX et al. The regulatory peptide apelin: a novel inhibitor of renal interstitial fibrosis. Amino Acids 2014; 46: 2693–704. 28. Canakci E, Karataş A, Erdem H, Celik M.A, Cirakoglu A, Cebeci Z. Effect of ischemic changes in renal tissues on apelin level. Internatıonal Journal of Scıentıfıc Research April 2018; 7:5:82-85.
29. Antushevich H, Wójcik M. Review: Apelin in disease. Clin Chim Acta. 2018 Aug; 483:241-48.
30. Siddiquee K, Hampton J, Khan S, Zadory D, Gleaves L, Vaughan DE, et al. Apelin protects against angiotensin II induced cardiovascular fibrosis and decreases plasminogen activator inhibitor type-1 production. J Hypertens 2011; 29: 724–31.
31. Li L, Zeng H, Chen JX. Apelin-13 increases myocardial progenitor cells and improves repair postmyocardial infarction. Am J Physiol Heart Circ Physiol. 2012; 303: 605–18.
32. Li L, Zeng H, Hou X, He X, Chen JX. Myocardial injection of apelin-overexpressing bone marrow cells improves cardiac repair via upregulation of Sirt3 after myocardial infarction. PLoS One 2013; 8(9) e71041.
33. Strohbach A, Böhm A, Mahajan-Thakur S, Wirtz C, Wetzel H, Busch MC et al. Platelet apelin receptor expression is reduced in patients with acute myocardial infarction. Vascul Pharmacol 2021 Feb;136: 106808.
34. Hu G, Wang Z, Zhang R, Sun W, Chen X. The Role of Apelin/Apelin Receptor in Energy Metabolism and Water Homeostasis: A Comprehensive Narrative Review Front Physiol. 2021;10(12): 632886.
35. Kinjo T, Higashi H, Uno K, Kuramoto N. Apelin/Apelin Receptor System: Molecular Characteristics, Physiological Roles, and Prospects as a Target for Disease Prevention and Pharmacotherapy. Curr Mol Pharmacol.2021;14(2):210-219.
36. Melgar-Lesmes P, Casals G, Pauta M, Ros J, Reichenbach V, Bataller R et al. Apelin mediates the induction of profibrogenic genes in human hepatic stellate cells. Endocrinology 2010; 151: 5306–14.
37. Yokomori H, Oda M, Yoshimura K, Machida S, Kaneko F, Hibi T et al. Overexpression of apelin receptor (APJ/ AGTRL1) on hepatic stellate cells and sinusoidal angiogenesis in human cirrhotic liver. J Gastroenterol 2011; 46: 222–31.
38. Owen NE, Nyimanu D, Kuc RE, Upton PD, Morrell NV, Alexander GJ et al. Plasma levels of apelin are reduced in patients with liver fibrosis and cirrhosis but are not correlated with circulating levels of bone morphogenetic protein 9 and 10. Peptides. 2021 Feb;136: 170440.

Variations in Apelin Expression Levels during Achilles Tendon Healing

Year 2021, Volume: 7 Issue: 1, 57 - 63, 30.04.2021

Derya Çırakoğlu Alper Çıraklı Havva Erdem Erdal Uzun Mürüvvet Akçay Çelik

https://doi.org/10.19127/mbsjohs.873010

Abstract

Objective: Research in recent years focused on the role of the apelin-APJ axis in pathologic fibrosis. The axis includes the parenchyma and mesenchymal cells of most organs. Reduction in parenchymal cells and activation of fibroblasts generally results in fibrosis of the organ. In this study, the aim was to reveal differences in apelin in tendons with primary repair.
Methods: The study used 15 male Wistar Albino rats. The tendons of the right and left legs of the rats were used. Rats were divided into 3 groups containing 5 rats each. Group 1 was the sham group; Group 2 had tendon repair performed and were sacrificed 3 weeks later; and Group 3 had tendon repair and were sacrificed 6 weeks later. Under anesthesia, bilateral tendonectomy was performed and surgically repaired. Tendons were removed in the 3rd and 6th weeks. Samples were immunohistochemically stained for apelin and stain degree was assessed from 0 to 4 with a light microscope. The scores were compared with the Friedman test.
Results: The results of statistical evaluation identified that the sham group had statistically significantly higher levels compared to the scores in the other two groups. There was no significant difference identified between the groups sacrificed in the 3rd and 6th weeks.
Conclusion: This study concluded that apelin may be beneficial for tendon healing and that apelin levels may increase with fibrosis.

Keywords

Apelin, Fibrosis, Repair

References

1. Pennisi E. Tending tender tendons. Science 2002; 295 (5557): 1011.
2. Liu CF, Aschbacher-Smith L, Barthelery NJ, Dyment N, Butler D, Wylie C. What We Should Know Before Using Tissue Engineering Techniques to Repair Injured Tendons: A Developmental Biology Perspective. Tissue Eng Part B-Rev 2011; 17(3): 165–76. 3. Hope M, Saxby TS. Tendon healing. Foot and ankle clinics. 2007; 12(4): 553–67.
4. Voleti PB, Buckley MR, Soslowsky LJ. Tendon healing: repair and regeneration. Annu Rev Biomed Eng 2012; 14: 47–71. 5. Hays PL, Kawamura S, Deng XH, Dagher E, Mithoefer K, Ying L et al. The role of macrophages in early healing of a tendon graft in a bone tunnel. J Bone Joint Surg Am 2008; 90(3): 565-79.
6. Sugg KB, Lubardic J, Gumucio JP, Mendias CL. Changes in macrophage phenotype and induction of epithelial-to-mesenchymal transition genes following acute Achilles tenotomy and repair. J Orthop Res 2014; 32: 944–51.
7. Lichtnekert J, Kawakami T, Parks WC, Duffield JS. Changes in macrophage phenotype as the immune response evolves. Curr Opin Pharmacol 2013; 13(4): 555-64.
8. Tatemoto K, Hosoya M, Habata Y, Fujii R, Kakegawa T, Zou MX, et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor, Biochem. Biophys. Res. Commun 1998; 251(2): 471-76.
9. Pitkin SL, Maguire JJ, Bonner TI, Davenport AP. Apelin receptor nomenclature, distribution, pharmacology, and function. Pharmacol Rev 2010; 62(3): 331–42.
10. Ghosh AK, Quaggin SE, Vaughan DE. Molecular basis of organ fibrosis: potential therapeutic approaches. Exp Biol Med 2013; 238: 461–81.
11. Brand T, Schneider MD. The TGF beta superfamily in myocardium: ligands, receptors, transduction and function. J Mol Cell Cardiol 1995; 27: 5–18.
12. Brand T, Schneider MD. Transforming growth factor-beta signal transduction. Circ Res 1996; 78: 173–79.
13. Calleja M, Connell DA. The achilles tendon. Seminars in Musculoskeletal Radiology 2010; 14(3): 307–22.
14. Andia I, Sanchez M, Maffulli N. Tendon healing and platelet-rich plasma therapies. Expert Opinion on Biological Therapy 2010; 10(10): 1415–26.
15. Chen B, Wang B, Zhang WJ, Zhou G, Cao Y, Liu W. In vivo tendon engineering with skeletal muscle derived cells in a mouse model. Biomaterials 2012; 33(26): 6086–97.
16. Chen CH, Cao Y, Wu YF, Bais AJ, Gao JS, Tang JB. Tendon healing ın vivo: Gene expression and production of multiple growth factors in early tendon healing period. The Journal of Hand Surgery 2008; 33(10): 1834–42. 17. Wurgler-Hauri CC, Dourte LM, Baradet TC, Williams GR, Soslowsky LJ. Temporal expression of 8 growth factors in tendon-to-bone healing in a rat supraspinatus model. J Shoulder Elbow Surg 2007; 16(5): 198–203.
18. Docheva D, Müller SA, Majewski M, Evans CH. Biologics for tendon repair. Adv Drug Deliv Rev. 2015; 84: 222–39.
19. Zhang G, Young BB, Ezura Y, Favata M, Soslowsky LJ, Chakravarti S, et al. Development of tendon structure and function: regulation of collagen ﬁbrillogenesis. J Musculoskelet Neuronal Interact 2005; 5(1): 5–21.
20. Riley G. The pathogenesis of tendinopathy: a molecular perspective. Rheumatology (Oxford) 2004; 43(2): 131–42.
21. Lorda-Diez CI, Montero JA, Martinez-Cue C, Garcia-Porrero JA, Hurle JM. Transforming growth factors β coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J Biol Chem 2009; 284(43): 29988–96.
22. Pryce BA, Watson SS, Murchison ND, Staverosky JA, Dunker N, Schweitzer R. Recruitment and maintenance of tendon progenitors by TGFβ signaling are essential for tendon formation. Development 2009; 136(8): 1351–61
23. Murchison ND, Price BA, Conner DA, Keene DR, Olson EN, Tabin CJ, et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 2007; 134(14): 2697–708.
24. Guerquin MJ, Charvet B, Nourissat G, Havis E, Ronsin O, Bonnin MA et al. Transcription factor EGR1 directs tendon differentiation and promotes tendon repair. J Clin Invest 2013; 123(8): 3564–76.
25. Liu W, Watson SS, Lan Y, Keene DR, Ovitt CE, Liu H et al. The atypical homeodomain transcription factor Mohawk controls tendon morphogenesis. Mol Cell Biol 2010; 30(20): 4797–807.
26. Huang S, Chen L, Lu L, Li L. The apelin-APJ axis: A novel potential therapeutic target for organ fibrosis. Clin Chim Acta. 2016; 456(1): 81-88.
27. Wang LY, Diao ZL, Zhang DL, Zheng JF, Zhang QD, Ding JX et al. The regulatory peptide apelin: a novel inhibitor of renal interstitial fibrosis. Amino Acids 2014; 46: 2693–704. 28. Canakci E, Karataş A, Erdem H, Celik M.A, Cirakoglu A, Cebeci Z. Effect of ischemic changes in renal tissues on apelin level. Internatıonal Journal of Scıentıfıc Research April 2018; 7:5:82-85.
29. Antushevich H, Wójcik M. Review: Apelin in disease. Clin Chim Acta. 2018 Aug; 483:241-48.
30. Siddiquee K, Hampton J, Khan S, Zadory D, Gleaves L, Vaughan DE, et al. Apelin protects against angiotensin II induced cardiovascular fibrosis and decreases plasminogen activator inhibitor type-1 production. J Hypertens 2011; 29: 724–31.
31. Li L, Zeng H, Chen JX. Apelin-13 increases myocardial progenitor cells and improves repair postmyocardial infarction. Am J Physiol Heart Circ Physiol. 2012; 303: 605–18.
32. Li L, Zeng H, Hou X, He X, Chen JX. Myocardial injection of apelin-overexpressing bone marrow cells improves cardiac repair via upregulation of Sirt3 after myocardial infarction. PLoS One 2013; 8(9) e71041.
33. Strohbach A, Böhm A, Mahajan-Thakur S, Wirtz C, Wetzel H, Busch MC et al. Platelet apelin receptor expression is reduced in patients with acute myocardial infarction. Vascul Pharmacol 2021 Feb;136: 106808.
34. Hu G, Wang Z, Zhang R, Sun W, Chen X. The Role of Apelin/Apelin Receptor in Energy Metabolism and Water Homeostasis: A Comprehensive Narrative Review Front Physiol. 2021;10(12): 632886.
35. Kinjo T, Higashi H, Uno K, Kuramoto N. Apelin/Apelin Receptor System: Molecular Characteristics, Physiological Roles, and Prospects as a Target for Disease Prevention and Pharmacotherapy. Curr Mol Pharmacol.2021;14(2):210-219.
36. Melgar-Lesmes P, Casals G, Pauta M, Ros J, Reichenbach V, Bataller R et al. Apelin mediates the induction of profibrogenic genes in human hepatic stellate cells. Endocrinology 2010; 151: 5306–14.
37. Yokomori H, Oda M, Yoshimura K, Machida S, Kaneko F, Hibi T et al. Overexpression of apelin receptor (APJ/ AGTRL1) on hepatic stellate cells and sinusoidal angiogenesis in human cirrhotic liver. J Gastroenterol 2011; 46: 222–31.
38. Owen NE, Nyimanu D, Kuc RE, Upton PD, Morrell NV, Alexander GJ et al. Plasma levels of apelin are reduced in patients with liver fibrosis and cirrhosis but are not correlated with circulating levels of bone morphogenetic protein 9 and 10. Peptides. 2021 Feb;136: 170440.

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Details

Primary Language	English
Subjects	Health Care Administration
Journal Section	Research articles
Authors	Derya Çırakoğlu 0000-0002-7827-8032 Alper Çıraklı 0000-0002-9879-312X Havva Erdem 0000-0002-3074-0240 Erdal Uzun 0000-0002-5456-3699 Mürüvvet Akçay Çelik 0000-0002-0335-4045
Publication Date	April 30, 2021
Published in Issue	Year 2021 Volume: 7 Issue: 1

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Vancouver	Çırakoğlu D, Çıraklı A, Erdem H, Uzun E, Akçay Çelik M. Variations in Apelin Expression Levels during Achilles Tendon Healing. Mid Blac Sea J Health Sci. 2021;7(1):57-63.

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