THE ROLE OF PROINFLAMMATORY CYTOKINES AND SOME HORMONES IN ENDOMETRIOSIS-INDUCED OSTEOPOROSIS
Keywords:
Endometriosis, Osteoporosis, Tumor Necrosis Factor Alpha [TNF-α], Interleukin 1[IL-1], Interleukin 6 [IL-6], Estradiol [E2], Follicle-stimulating hormone [FSH], Thyroid-stimulating hormone [TSH], Parathyroid hormone [PTH]Abstract
Objective: The aim of this study is to evaluate the effects of proinflammatory cytokines and some hormones, in patients with endometriosis, on the serum levels of bone formation and bone resorption markers. Subjects and methods: Eightyfemale patients with endometriosis at their reproductive age subjected to standard criteria were participated in this study. Eighty apparently healthy women were selected to be a normal group for comparison. In addition, assessing the serum levels of tumor necrosis factor alpha [TNF-α], interleukin 1[IL-1], interleukin 6 [IL-6], CarboxyterminalTelopeptides of type I Collagen [CTX1], CarboxyterminalPropeptide of type I Procollagen [PICP], Estradiol [E2], Follicle-Stimulating Hormone [FSH], Thyroid-Stimulating Hormone [TSH], and Parathyroid Hormone [PTH] by EILISA and enzymatic Kits. Results: The results show that the levels of tumor necrosis factor alpha [TNF-α], interleukin 1[IL-1] , interleukin 6[IL-6], C terminal Telopeptides of type I Collagen[CTX1]and C terminal propeptide of type I procollagen[PICP], follicle-stimulating hormone [FSH], thyroid-stimulating hormone [TSH] and parathyroid hormone [PTH] weresignificantly changed in serum of patients with endometriosisas compared with control healthy group. Whereas, the change of serum estradiol [E2] level was non-significant as compared with control group. Conclusions: The inflammatory activity of tumor necrosis factor alpha [TNF-α], interleukin 1[IL-1] and interleukin 6 [IL-6] was important in the development of osteoporosis in patients with endometriosisby its effect on bone formation and resorption markers.The role of some hormones, follicle-stimulating hormone [FSH], thyroid-stimulating hormone [TSH] and parathyroid hormone [PTH], in the development of osteoporosis in patients with endometriosis was also assessed.References
Stephen Kennedy,AgnetaBergqvist, Charles Chapron et al(2005). ESHRE guideline for the diagnosis and treatmentof endometriosis.Human Reproduction, Vol. 20, No.10 pp. 2698–2704.
Linda C.Guidice. Endometriosis(2010). N Engl J Med, 362:2389-2398.
Sampson J. A. (1925). Endometrial carcinoma of the ovary arising in endometrial tissue in that organ. Arch Surg,10:1–72.
Nezhat F, Datta MS, Hanson V, Pejovic T, Nezhat C, Nezhat C. (2008). The relationship of endometriosis and ovarian malignancy: a review. Fertil Steril,90:1559–70.
Jones,G., Jenkinson, C. and Kennedy, S.(2014) The impact of endometriosis upon quality of life: a qualitative analysis. J PsychosomObstetGynaecol, 25,123-133.
Simoens, S., Hummelshoj, L. and D'Hooghe, T. (2007) Endometriosis: cost estimates and methodological perspective. Hum Reprod Update, 13, 395-404.
Osuga, Y., Koga, K., Hirota, Y., Hirata, T., Yoshino, O. and Taketani, Y. (2010) Lymphocytes in endometriosis. Am J ReprodImmunol, 65, 1-10.
Lebovic, D. I., Mueller, M. D. and Taylor, R. N. (2001).Immunobiology of endometriosis. FertilSteril, 75, 1-10.
Pizzo, A., Salmeri, F. M., Ardita, F. V., Sofo, V., Tripepi, M. and Marsico, S. (2012).Behaviour of cytokine levels in serum and peritoneal fluid of women with endometriosis. GynecolObstet Invest, 54, 82-87.
Velasco, I., Rueda, J. and Acien, P. (2006). Aromatase expression in endometriotic tissues and cell cultures of patients with endometriosis. Hum Reprod, 12,377-381.
Roy Yuen-chi Lau, Xia GuoA. (2011). Review on Current Osteoporosis Research: With Special Focus on disuse bone loss. Journal of Osteoporosis, 1,1-2.
Sydney, L.; Bonnick, MD.; Steven, T.; Harris, MD.; FACP; David, L.; Kendler, MD. (2010). Management of osteoporosis in postmenopausal women. The Journal of the North American Menopause Society, 17,(1), 25-54.
Pogoda, P.; Priemel, M.; Rueger, JM.; Amling, M. (2005). Bone remodeling: new aspects of a key process that controls skeletal maintenance and repair. OsteoporosInt, 16, 2, 18-24.
Keith McCormick R. (2007).osteoporosis:integrating biomarkers and diagnostic correlates into the management of bone fragility.Alternative medicine review, 12(2),113-114.
Boyle, WJ.; Simonet, WS.; Lacey, DL.(2003). Osteoclast differentiation and activation. Nature, 423,337-342.
Seriwatanachai, D.; Thongchote, K.; Charoenphandhu, N. (2008). Prolactin directly enhances bone turnover by raising osteoblast-expressed nuclear factor kB ligand/osteoprotegerin ratio.Bone, 42,535-546.
Pfeilschifter, J.; Koditz, R.; Pfohl, M. (2002). Changes in proinflammatory cytokine activity after menopause.Endocr Rev, 23,90-119.
Ginaldi,L.;Di Benedetto, MC.; De Martinis, M. (2005). Osteoporosis, inflammation and ageing.Immun Ageing,2,14.
Clowes, JA.; Riggs, BL.; Khosla, S. (2005). the role of the immune system in the pathophysiology of osteoporosis. Immunol Rev,208,207-227.
Inzerillo, AM.; Epstein, S., Osteoporosis and diabetes mellitus (2004). Rev EndocrMetabDisord, 5, 261-268.
Merlotti, D.; Gennari, L.; Dotta, F.; Lauro, D.; Nuti ,R. (2010).Mechanisms of impaired bone strength in type 1 and 2 diabetes. NutrMetabCardiovasc Dis ,20, 683-690.
Ragab, AA.; Nalepka, JL.; Bi, Y.; Greenfield, EM. (2002). Cytokines synergistically induce osteoclast differentiation: support by immortalized or normal calvarial cells. Am J Physiol Cell Physiol, 283, 679-687.
WeitzmannM. N. and PacificiR. (2006). Estrogen deficiency and bone loss: an inflammatory tale.Journal of Clinical Investigation, vol. 116, no. 5, pp. 1186–1194.
Sowers M. R., JannauschM., McConnell D. et al. (2006).Hormone predictors of bone mineral density changes during the menopausal transition.Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 4, pp. 1261–1267.
MenaghP. J., R. T. Turner, D. B. Jump et al. (2010). Growth hormone regulates the balance between bone formation and bone marrow adiposity.Journal of Bone and Mineral Research, vol. 25, no. 4, pp. 757–768.
EbelingP. R. (2010). What is the missing hormonal factor controlling menopausal bone resorption?Journal of Clinical Endocrinologyand Metabolism,vol 95,11, pp. 4864–4866.
Bauer D. C., EttingerB.,NevittM. C., and Stone K. L.(2001). Risk for fracture in women with low serumlevels of thyroid-stimulating hormone.Annals of Internal Medicine, vol. 134, no. 7, pp. 561–568.
SeriwatanachaiD., ThongchoteK., CharoenphandhuN. et al. (2008). Prolactin directly enhances bone turnover by raising osteoblast- expressed receptor activator of nuclear factor ????B ligand/osteoprotegerin ratio,” Bone, vol. 42, no. 3, pp. 535–546.
TammaR., ColaianniG., Zhu L. L. et al. (2009). Oxytocin is an anabolic bone hormone.Proceedings of the National Academy ofSciences of theUnited States of America, vol. 106, no. 17, pp. 7149–7154.
Schluter K.D. (1999). PTH and PTHrP: similar structures but different functions, NewsPhysiol. Sci., 14: 243–249.
Bauer DC, Black DM, Garnero P, et al. (2004). the fracture intervention trial. J Bone Miner Res,19:1250–8.
Havill LM., Rogers J., Cox LA. (2006). QTL with pleiotropic effects on serum levels of bonespecific alkaline phosphatase and osteocalcin maps to the baboon ortholog of human chromosome 6p23-21.3. J Bone Miner Res,21,1888-1896.
Melkko J., Kauppila S., Niemi S. (1996). Immunoassay for intact amino-terminal propeptide of human type1 procollagen. Clin Chem,42,947-954.
Scariano JK., Garry PJ., Montoya GD. (2002).Diagnostic efficiency of serum cross-linked N-telopeptide[NTx] and aminoterminal procollagen extension propeptide [P1NP] measurements for identifying elderly women with decreased bone mineral density. Scand J Clin Lab Invest, 62,237-243.
Ravn P., Fledelius C., Rosenquist C. (1996). High bone turnover is associated with low bone mass in both pre- and postmenopausal women. Bone, 19,291-298.
Garnero P.,Hausherr E., Chapuy MC.(1996). Markers of bone resorption predicts hip fracture in elderly women: the EPIDOS Study. J Bone Miner Res,11,1531-1538.
GinaldiL.,Di Benedetto MC., De Martinis M.(2005). Osteoporosis, inflammation and ageing.Immun Ageing,2,14.
Mukund J, Ganesan K, Munshi HN, Ganesan S, Lawande A (2007). Sonography of adnexal masses. Ultrasound Clinics, 2(1):133-153.
Nezhat CR, Berger G, Nezhat FJ, Buttram V, Nezhat C (1995). Operative laparoscopy: preventing and managing complications.Endometriosis: Advanced Management and Surgical Techniques. Springer-Verlag.
Human Interleukin 1 Alpha (IL-1α) ELISA Kit. Catalog number MBS261110. MyBioSource, Denmark.
Human Interleukin 6 (IL-6) ELISA Kit. Cat. No. MBS819223. MyBioSource, Denmark.
Enzyme Immunoassay (EIA) for the in vitro determination of TNFα in plasma, serum, or culture supernatant. Catalog number IM1121. IMMUNOTECH, BECKMAN COULTER.
Human Cross-linked Carboxy-terminal Telopeptide of Type 1 Collagen (CTX1) ELISA Kit. Catalog number MBS700254. MyBioSource, Denmark.
Human Procollagen Type I C-terminal Propeptide (PICP) ELISA Kit. Catalog number MBS726800. MyBioSource, Denmark.
Parathyroid Hormone intact (PTH) ELISA Kit. Cat. No.DRG 1244. DRG, USA.
Follicle-Stimulating Hormone (FSH) ELISA Kit. Cat. No.BC06869. BIOCHECK, USA.
Thyroid-Stimulating Hormone (TSH) ELISA Kit. Cat. No. BC012651. BIOCHECK, USA.
Serum Estradiol (E2) ELISA Kit. Catalog number BC022661. BIOCHECK, USA.
Alahmad G., Al-Jumah M., and Dierickx K. (2012). Review of national research ethics regulations and guidelines in Middle East Arab countries. BMC Medical Ethics, 13:34.
Microsoft Excel, 2010 software.
Sowers MFR, Pietra MT. (1996). Menopause: its epidemiology and potential association with chronic diseases. Epidemiol Rev, 17: 287-302.
Kato I, Toniolo P, Akhmedkhanov A, Koeing KL, Zeleninch- Jacquotte A. (2008). Prospective study of factors including the onset of natural menopause. J ClinEpidemiol, 61 (15): 1112-8.
Stanford JL, Hartge P, Briton LA, Hoover RN, Brookmeyer R (1987). Factors influencing the age at natural menopause. J Chroon Dis, 40: 995-1002.
Trussel I, Avenell A, Reid DM. (2004). Factors associated with onset of menopause in women. Maturitas, 21: 63-71.
Aloia JF, Cohn SH, Vaswani A, et al (1985). Risk factors for postmenopausal osteoporosis. Am J Med, 78: 95-100.
Griffin J (2010). Osteoporosis and the risk of fracture. London: Office of Health Economics.
Mundy GR. Osteoporosis and inflammation. Nutr Rev. 2007; 65(12):147-51.
Sunyer T., Lewis J., Collin-Osdoby P. et al(1999).Estrogen’s bone-protective effects may involve differential IL-1receptor regulation in human osteoclast-like cells. J. Clin. Invest,103, 1409–1418.
Teitelbaum SL. (2007). Osteoclasts: what do they do and how do they do it? Am J Pathol, 170(2):427-35.
Cohen-Solal M. E., Graulet A. M., Denne M. A.,et al (1993).Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J. Clin. Endocrinol. Metab, 77, 1648–1653.
Salamone L. M., Whiteside T., FribergD.,et al (1998). Cytokine production and bone mineral density at the lumbar spine and femoral neck in premenopausalwomen. Calcif. Tissue Int., 63:466–470.
Zheng S. X., Vrindts Y., and Lopez M., et al (1997). Increase in cytokine production (IL-1beta, IL-6, TNF-alpha but not IFN-gamma, GM-CSF or LIF) by stimulated whole blood cells in postmenopausal women. Maturitas, 26: 63–71.
Kassem M., Khosla S., Spelsberg T. C.et al (1996). Cytokine production in the bone marrow microenvironment: failure to demonstrate estrogen regulation in early postmenopausal women. J. Clin. Endocrinol. Metab, 81: 513–518.
Sims NA, Jenkins BJ, Quinn JM et al. (2004) Glycoprotein 130 regulates bone turnover and bone size by distinct downstream signaling pathways.J Clin Invest, 113: 379–389.
O’Brien CA, Jilka RL, Fu Q, et al (2005). IL-6 is not required for parathyroid hormone stimulation of RANKL expression, osteoclast formation, and bone loss in mice. Am J PhysiolEndocrinolMetab, 289: 784–793.
Liu XH, Kirschenbaum A, Yao S, et al (2006). Interactive effect of interleukin-6 and prostaglandin E2 on osteoclastogenesis via the OPG/RANKL/RANK system. Ann N Y AcadSci, 1068: 225–233.
Mysliwiec J, Zbucki R, Nikolajuk A et al (2011). Estrogens modulate RANKL-RANK/osteoprotegerin mediated Interleukin-6 effect on thyrotoxicosis-related bone turnover in mice. HormMetab Res, 43: 236–240.
Chung HW, Seo JS, Hur SE, et al (2003). Association of interleukin-6 promoter variant with bone mineral density in premenopausal women. J Hum Genet;48:243–8.
Garnero P, Borel O, Sornay-Rendu E, et al (2002). Association between a functional interleukin-6 gene polymorphism and peak bone mineral density and postmenopausal bone loss in women. Bone; 31:43–50.
Zwerina J, Redlich K, Polzer K et al (2007). TNF-induced structural joint damage is mediated by IL-1. ProcNatlAcadSci USA, 104:11742–11747.
Weitzmann MN, Pacifici R (2005).The role of T lymphocytes in bone metabolism. Immunol Rev., 208:154-68.
Kwan Tat S, Padrines M, Theoleyre S et al (2004). IL-6,RANKL, TNF-alpha/IL-1: interrelation in bone resorption pathophysiology. Cytokine Growth Factor,15:49-60.
Roberto Pacifici(2010). The immune system and bone. Archives of Biochemistry and Biophysics, 503: 41–53.
Changhai Ding, VenkatParameswaran, Ray Udayan et al (2008). Circulating Levels of Inflammatory Markers Predict Change in Bone Mineral Density and Resorption in Older Adults: A Longitudinal Study. J ClinEndocrinolMetab., 93(5):1952–1958.
Nanes M.S.(2003). Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology.Gene, 321:1-15.
Koh JM, Kang YH, Jung CH, et al (2005). Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre-and postmenopausal women: evidence for a link betweeninflammation and osteoporosis. Osteoporosis Int, 198: 1840-5.
Dempster, D.W. et al. (2007). Preserved three-dimensional cancellous bone structure in mild primary hyperparathyroidism. Bone, 41(1): p.19-24.
Ju ¨ppner H, Gardella T, Brown E, Kronenberg H, Potts J Jr (2005).Parathyroid hormone and parathyroid hormone-related peptide in the regulation of calcium homeostasis and bone development.Saunders, Philadelphia, PA, USA,1377–1417.
OmodeiU., MazziottiG., DonariniG. et al. (2013). Effects of recombinant follicle-stimulating hormone on bone turnover markers in infertile women undergoing in vitro fertilization procedure. The Journal of Clinical Endocrinology and Metabolism, vol. 98, no. 1, pp. 330–336.
Sowers M. R., Finkelstein J. S., EttingerB. et al. (2003). The association of endogenous hormone concentrations and bone mineral density measures in pre- and perimenopausal women of four ethnic groups: SWAN. Osteoporosis International, vol. 14,no. 1, pp.44–52.
Prior J. C. (1998). Perimenopause: the complex endocrinology of the menopausal transition,” Endocrine Reviews, vol. 19, pp. 397–428.
Allan C. M., KalakR., Dunstan C. R. et al. (2010). Follicle-stimulating hormone increases bone mass in female mice. Proceedings ofthe National Academy of Sciences of the United States of America, vol. 107, no. 52, pp. 22629–22634.
Cannon J. G., Cortez-Cooper M., MeadersE. et al. (2010). Follicle-stimulating hormone, interleukin-1, and bone density in adult women. American Journal of Physiology, vol. 298, no. 3, pp. R790–R798.
BaranD. T. (1994). Thyroid hormone and bone mass: the clinician’s dilemma. Thyroid, vol. 4, no. 2, pp. 143–144.
MazziottiG., PorcelliT., PatelliI., VescoviP. P., and GiustinaA. (2010). Serum TSH values and risk of vertebral fractures in euthyroid postmenopausal women with low bone mineral density.Bone, vol. 46, no. 3, pp. 747–751.
Sun L., Davies T. F., Blair H. C., Abe E., and Zaidi M. (2006). TSH and bone loss.Annals of the New York Academy of Sciences, vol. 1068, no. 1, pp. 309–318.
Garnero P., Borel O., Delmas PD. (2001). Evaluation of a fully automated serum assay for C-terminal cross-linking telopeptide of type I collagen in osteoporosis. ClinChem, 47,694–702.
Manolagas SC., Jilka RL, (1995). Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med, , 332,305–311.
