Sensitivity of the fasciae to sex hormone levels: Modulation of collagen-I, collagen-III and fibrillin production

English version

Autoři: Caterina Fede ^aff001; Carmelo Pirri ^aff002; Chenglei Fan ^aff001; Giovanna Albertin ^aff001; Andrea Porzionato ^aff001; Veronica Macchi ^aff001; Raffaele De Caro ^aff001; Carla Stecco ^aff001
Působiště autorů: Department of Neurosciences, Institute of Human Anatomy, University of Padova, Padova, Italy ^aff001; Physical and Rehabilitation Medicine, University of Rome “Tor Vergata”, Roma, Italy ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223195

Souhrn

Although it is now recognized that women suffer from myofascial pain to a greater extent than men, and that the muscular fasciae can respond to hormonal stimuli, thanks to the expression of sex hormone receptors, how the fasciae can modify their structure under hormonal stimulation is not clear. In this work, an immunocytochemical analysis of collagen-I, collagen-III and fibrillin were carried out on fibroblasts isolated from human fascia lata after in vitro treatment with various levels of sex hormones β-estradiol and/or relaxin-1, according to the phases of a woman’s period (follicular, periovulatory, luteal, post-menopausal phases and pregnancy). This study demonstrates for the first time that fascial cells can modulate the production of some components of the extracellular matrix according to hormone levels, when treated with β-estradiol: collagen-I falls from 6% of positivity in the follicular phase to 1.9 in the periovulatory phase. However, after the addition of relaxin-1 to the cell culture, the production of extracellular matrix decreased and remained at the same level (1.7% of collagen-I, at both follicular and periovulatory levels of hormones). These results confirm the antifibrotic function of relaxin-1, thanks to its ability to reduce matrix synthesis. They are also a first step in our understanding of how some hormonal dysfunctions in women can cause a dysregulation of extracellular matrix production in fasciae.

Klíčová slova:

Pregnancy – Hormones – Fibroblasts – Collagens – Cell staining – Sex hormones – Extracellular matrix – Estrogens

Zdroje

1. Chidi-Ogbolu N, Baar K. Effect of Estrogen on Musculoskeletal Performance and Injury Risk. Front Physiol. 2019;9:1834. doi: 10.3389/fphys.2018.01834 30697162

2. Bridgeman JT, Zhang Y, Donahue H, Wade AM, Juliano PJ. Estrogen receptor expression in posterior tibial tendon dysfunction: a pilot study. Foot Ankle Int 2010;31:1081–4. doi: 10.3113/FAI.2010.1081 21189209

3. Fede C, Albertin G, Petrelli L, Sfriso MM, Biz C, De Caro R, et al. Hormone receptor expression in human fascial tissue. Eur J Histochem 2016;60:2710. doi: 10.4081/ejh.2016.2710 28076930

4. Zazulak BT, Paterno M, Myer GD, Romani WA, Hewett TE. The effects of the menstrual cycle on anterior knee laxity: a systematic review. Sports Med. 2006;36:847–62. doi: 10.2165/00007256-200636100-00004 17004848

5. Shultz SJ, Schmitz RJ, Kong Y, Dudley WN, Beynnon BD, Nguyen AD, et al. Cyclic variations in multiplanar knee laxity influence landing biomechanics. Med Sci Sports Exerc 2012;44:900–9. doi: 10.1249/MSS.0b013e31823bfb25 22033513

6. Konopka JA, DeBaun MR, Chang W, Dragoo JL. The Intracellular Effect of Relaxin on Female Anterior Cruciate Ligament Cells. Am J Sports Med 2016;44:2384–92. doi: 10.1177/0363546516646374 27245459

7. Shultz SJ, Sander TC, Kirk SE, Perrin DH. Sex differences in knee joint laxity change across the female menstrual cycle. J Sports Med Phys Fitness 2005;45:594–603. 16446695

8. Liu SH, Al-Shaikh RA, Panossian V, Finerman GA, Lane JM. Estrogen affects the cellular metabolism of the anterior cruciate ligament. A potential explanation for female athletic injury. Am J Sports Med 1997;25:704–9. doi: 10.1177/036354659702500521 9302481

9. Yu WD, Liu SH, Hatch JD, Panossian V, Finerman GA. Effect of estrogen on cellular metabolism of the human anterior cruciate ligament. Clinical Orthopaedics and Related Research 1999;366:229–38.

10. Lee CY, Liu X, Smith CL, Zhang X, Hsu HC, Wang DY, et al. The combined regulation of estrogen and cyclic tension on fibroblast biosynthesis derived from anterior cruciate ligament. Matrix Biol 2004;23:323–9. doi: 10.1016/j.matbio.2004.07.004 15464364

11. Dao TT, Knight K, Ton-That V. Modulation of myofascial pain by the reproductive hormones: a preliminary report. J Prosthet Dent 1998;79:663–70. doi: 10.1016/s0022-3913(98)70073-3 9627895

12. Lee JW, Park HS. Relation of the factor to menstrual pain and musculoskeletal pain. J Exerc Rehabil 2015;11:108–11. doi: 10.12965/jer.150188 25960984

13. Lee H, Petrofsky J. Differences Between Men and Women in Balance and Tremor in Relation to Plantar Fascia Laxity During the Menstrual Cycle. J Athl Train 2018;53:255–261. doi: 10.4085/1062-6050-2-17 29485291

14. Felson DT, Cummings SR. Aromatase inhibitors and the syndrome of arthralgias with estrogen deprivation. Arthritis Rheum 2005;52:2594–8. doi: 10.1002/art.21364 16142740

15. Hansen M, Kongsgaard M, Holm L, Skovgaard D, Magnusson SP, Qvortrup K, et al. Effect of estrogen on tendon collagen synthesis, tendon structural characteristics, and biomechanical properties in postmenopausal women. Journal of Applied Physiology 2009;106:1385–93. doi: 10.1152/japplphysiol.90935.2008 18927264

16. Fede C, Albertin G, Petrelli L, Sfriso MM, Biz C, De Caro R, et al. Expression of the endocannabinoid receptors in human fascial tissue. Eur J Histochem. 2016;60:2643. doi: 10.4081/ejh.2016.2643 27349320

17. Selby C. Interference in immunoassay. Ann Clin Biochem 1999; 36:704–721. doi: 10.1177/000456329903600603 10586307

18. Bridges RS, Nephew BC. Neuroendocrine Control: Maternal Behavior. Encyclopedia of Neuroscience 2009, 333–342.

19. Reed BG, Carr BR. The Normal Menstrual Cycle and the Control of Ovulation. In: Feingold KR, Anawalt B, Boyce A, et al., editors.2000. South Dartmouth (MA).

20. Abbassi-Ghanavati M, Greer LG, Cunningham FG. Pregnancy and laboratory studies: a reference table for clinicians. Obstet Gynecol. 2009;114(6):1326–31. doi: 10.1097/AOG.0b013e3181c2bde8 19935037

21. Goldsmith LT, Weiss G. Relaxin in Human Pregnancy. Ann N Y Acad Sci. 2009 Apr; 1160: 10.1111/j.1749-6632.2008.03800.x.

22. Wreje U, Kristiansson P, Aberg H, Byström B, von Schoultz B. Serum levels of relaxin during the menstrual cycle and oral contraceptive use. Gynecol Obstet Invest. 1995;39:197–200. doi: 10.1159/000292408 7789917

23. Günzel-Apel AR, Zabel S, Bunck CF, Dieleman SJ, Einspanier A, Hoppen HO. Concentrations of progesterone, prolactin and relaxin in the luteal phase and pregnancy in normal and short-cycling German Shepherd dogs. Theriogenology, 2006. Vol 66: 1431–1435. doi: 10.1016/j.theriogenology.2006.01.030 16499960

24. Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK. Extracellular matrix structure. Adv Drug Deliv Rev 2016;97:4–27. doi: 10.1016/j.addr.2015.11.001 26562801

25. Nallasamy S, Yoshida K, Akins M, Myers K, Iozzo R, Mahendroo M. Steroid Hormones Are Key Modulators of Tissue Mechanical Function via Regulation of Collagen and Elastic Fibers. Endocrinology 2017;158:950–962. doi: 10.1210/en.2016-1930 28204185

26. Raine-Fenning NJ, Brincat MP, Muscat-Baron Y. Skin aging and menopause: implications for treatment. Am J Clin Dermatol. 2003;4:371–378. doi: 10.2165/00128071-200304060-00001 12762829

27. Brauchle E, Kasper J, Daum R, Schierbaum N, Falch C, Kirschniak A, et al. Biomechanical and biomolecular characterization of extracellular matrix structures in human colon carcinomas. Matrix Biol. 2018;68–69:180–193. doi: 10.1016/j.matbio.2018.03.016 29605717

28. Stecco C, Fede C, Macchi V, Porzionato A, Petrelli L, Biz C, et al. The fasciacytes: A new cell devoted to fascial gliding regulation. Clin Anat. 2018;31(5):667–676. doi: 10.1002/ca.23072 29575206

29. Wang S, Lü D, Zhang Z, Jia X, Yang L. Effects of mechanical stretching on the morphology of extracellular polymers and the mRNA expression of collagens and small leucine-rich repeat proteoglycans in vaginal fibroblasts from women with pelvic organ prolapse. PLoS One 2018;13:e0193456. doi: 10.1371/journal.pone.0193456 29630675

30. Wagenseil JE, Mecham RP. New insights into elastic fiber assembly. Birth Defects Res C Embryo Today 2007;81:229–40. doi: 10.1002/bdrc.20111 18228265

31. Gracovetsky S. The Spinal Engine, Springer–Verlag, Wien, New York (NY);1988.

32. Stecco C. Functional Atlas of the Human Fascial System. 1st edn. Edinburgh: Elsevier; 2015. p. 211.

33. Sabino J, Grauer JN. Pregnancy and low back pain. Curr Rev Musculoskelet Med 2008;1:137–41. doi: 10.1007/s12178-008-9021-8 19468887

34. Stones RW, Vits K. Pelvic girdle pain in pregnancy. BMJ 2005;331:249–50. doi: 10.1136/bmj.331.7511.249 16051994

35. Marnach ML, Ramin KD, Ramsey PS, Song SW, Stensland JJ, An KN. Characterization of the relationship between joint laxity and maternal hormones in pregnancy. Obstet Gynecol 2003;101(2):331–5. doi: 10.1016/s0029-7844(02)02447-x 12576258

36. Freeman EW, Sammel MD, Lin H, Gracia CR, Pien GW, Nelson DB, et al. Symptoms associated with menopausal transition and reproductive hormones in midlife women. Obstet Gynecol 2007;110(2 Pt 1):230–40.

37. Samuel CS, Lekgabe ED, Mookerjee I. The Effects of Relaxin on Extracellular Matrix Remodeling in Health and Fibrotic Disease. In: Agoulnik A.I. (eds) Relaxin and Related Peptides. Advances in Experimental Medicine and Biology. New York (NY): Springer; 2007. 612: p. 88–103. doi: 10.1007/978-0-387-74672-2_7

38. Pavan PG, Stecco A, Stern R, Stecco C. Painful connections: densification versus fibrosis of fascia. Curr Pain Headache Rep 2014;18:441. doi: 10.1007/s11916-014-0441-4 25063495

39. Wells RG. Tissue mechanics and fibrosis. Biochim Biophys Acta. 2013;1832:884–90. doi: 10.1016/j.bbadis.2013.02.007 23434892

40. Sarajari S, Oblinger MM. Estrogen effects on pain sensitivity and neuropeptide expression in rat sensory neurons. Exp Neurol 2010;224:163–9. doi: 10.1016/j.expneurol.2010.03.006 20303952

41. Martineau PA, Al-Jassir F, Lenczner E, Burman ML. Effect of the oral contraceptive pill on ligamentous laxity. Clin J Sport Med 2004;14:281–6. 15377967

42. Park YM, Pereira RI, Erickson CB, Swibas TA, Cox-York KA, Van Pelt RE. Estradiol-mediated improvements in adipose tissue insulin sensitivity are related to the balance of adipose tissue estrogen receptor α and β in postmenopausal women. PLoS One 2017;12:e0176446. doi: 10.1371/journal.pone.0176446 28472101

43. Cristofalo VJ, Allen RG, Pignolo RJ, Martin BG, Beck JC. Relationship between donor age and the replicative lifespan of human cells in culture: A reevaluation. Proc. Natl. Acad. Sci. USA 1998; 95: 10614–10619. doi: 10.1073/pnas.95.18.10614 9724752

44. Chen CZC, Raghunath M. Focus on collagen: in vitro systems to study fibrogenesis and antifibrosis _ state of the art. Fibrogenesis Tissue Repair 2009;2:7. doi: 10.1186/1755-1536-2-7 20003476

45. Hansen M, Miller BF, Holm L, Doessing S, Petersen SG, Skovgaard D, et al. Effect of administration of oral contraceptives in vivo on collagen synthesis in tendon and muscle connective tissue in young women. J Appl Physiol 2009;106:1435–43. doi: 10.1152/japplphysiol.90933.2008 18845777

46. Ozturk Y, Bozkurt I, Yaman ME, Guvenc Y, Tolunay T, Bayram P, et al. Histopathologic Analysis of Tamoxifen on Epidural Fibrosis. World Neurosurg 2018;111:e941–e948. doi: 10.1016/j.wneu.2018.01.004 29325937

47. Hansen M. Female hormones: do they influence muscle and tendon protein metabolism? Proc Nutr Soc 2018;77:32–41. doi: 10.1017/S0029665117001951 28847313

Sensitivity of the fasciae to sex hormone levels: Modulation of collagen-I, collagen-III and fibrillin production

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