Effect of calcium glucoheptonate on proliferation and osteogenesis of osteoblast-like cells in vitro

English version

Autoři: Prashant Kumar Modi ^aff001; Ashwini Prabhu ^aff001; Yashodhar P. Bhandary ^aff001; Sudheer Shenoy P. ^aff001; Aparna Hegde ^aff001; Sindhu Priya ES ^aff001; Renjith P. Johnson ^aff001; Shankar Prasad Das ^aff001; Sahil Vazirally ^aff002; Punchappady-Devasya Rekha ^aff001
Působiště autorů: Yenepoya Research Centre, Yenepoya (Deemed to be University), Mangalore, Karnataka, India ^aff001; Global Calcium Pvt. Ltd., Bangalore, Karnataka, India ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222240

Souhrn

Calcium is the key macromineral having a role in skeletal structure and function, muscle contraction, and neurotransmission. Bone remodeling is maintained through a constant balance between calcium resorption and deposition. Calcium deficiency is resolved through calcium supplementation, and among the supplements, water-soluble organic molecules attracted great pharmaceutical interest. Calcium glucoheptonate is a highly water-soluble organic calcium salt having clinical use; however, detailed investigations on its biological effects are limited. We assessed the effects of calcium glucoheptonate on cell viability and proliferation of osteoblast-like MG-63 cells. Calcium uptake and mineralization were evaluated using Alizarin red staining of osteoblast-like MG-63 cells treated with calcium glucoheptonate. Expression of osteogenic markers were monitored by western blotting, immunofluorescence, and qRT-PCR assays. Increased proliferation and calcium uptake were observed in the MG-63 cells treated with calcium glucoheptonate. The treatment also increased the expression of osteopontin and osteogenic genes such as collagen-1, secreted protein acidic and cysteine rich (SPARC), and osteocalcin. Calcium glucoheptonate treatment did not exert any cytotoxicity on colorectal and renal epithelial cells, indicating the safety of the treatment. This is the first report with evidence for its beneficial effect for pharmaceutical use in addressing calcium deficiency conditions.

Klíčová slova:

Biology and life sciences – Cell biology – Biochemistry – Research and analysis methods – Enzymology – Enzymes – Proteins – Cellular types – Animal cells – Anatomy – Medicine and health sciences – Phosphatases – Physiology – Hormones – Physiological processes – Peptide hormones – Biological cultures – Biological tissue – Epithelial cells – Epithelium – Bioassays and physiological analysis – Osteocalcin – Bone remodeling – Ossification – Specimen preparation and treatment – Staining – Cell staining – Group-specific staining – Alizarin staining – Cell lines – 293T cells – Biochemical analysis – Colorimetric assays – MTT assay – Enzyme assays

Zdroje

1. Brini M, Ottolini D, Cali T, Carafoli E. Calcium in health and disease. Met Ions Life Sci. 2013;13:81–137. Epub 2014/01/29. doi: 10.1007/978-94-007-7500-8_4 24470090.

2. Wilson CH, Ali ES, Scrimgeour N, Martin AM, Hua J, Tallis GA, et al. Steatosis inhibits liver cell store-operated Ca(2)(+) entry and reduces ER Ca(2)(+) through a protein kinase C-dependent mechanism. Biochem J. 2015;466(2):379–90. Epub 2014/11/26. doi: 10.1042/BJ20140881 25422863.

3. Aquino-Martinez R, Artigas N, Gamez B, Rosa JL, Ventura F. Extracellular calcium promotes bone formation from bone marrow mesenchymal stem cells by amplifying the effects of BMP-2 on SMAD signalling. PLoS One. 2017;12(5):e0178158. Epub 2017/05/26. doi: 10.1371/journal.pone.0178158 28542453; PubMed Central PMCID: PMC5444778.

4. Sunyecz JA. The use of calcium and vitamin D in the management of osteoporosis. Ther Clin Risk Manag. 2008;4(4):827–36. Epub 2009/02/12. doi: 10.2147/tcrm.s3552 19209265; PubMed Central PMCID: PMC2621390.

5. Wang M, Yang X, Wang F, Li R, Ning H, Na L, et al. Calcium-deficiency assessment and biomarker identification by an integrated urinary metabonomics analysis. BMC Med. 2013;11:86. Epub 2013/03/30. doi: 10.1186/1741-7015-11-86 23537001; PubMed Central PMCID: PMC3652781.

6. Ruan X, Tey HL. Hypocalcemia: low incidence in flares of pustular and chronic plaque psoriasis. Int J Dermatol. 2017;56(6):e133–e5. Epub 2017/02/16. doi: 10.1111/ijd.13549 28198000.

7. Knuever J, Tantcheva-Poor I. Generalized pustular psoriasis: A possible association with severe hypocalcaemia due to primary hypoparathyroidism. J Dermatol. 2017;44(12):1416–7. Epub 2017/01/21. doi: 10.1111/1346-8138.13724 28106254.

8. Melton LJ, Atkinson EJ 3rd, O'Connor MK, O'Fallon WM, Riggs BL. Bone density and fracture risk in men. J Bone Miner Res. 1998;13(12):1915–23. Epub 1998/12/09. doi: 10.1359/jbmr.1998.13.12.1915 9844110.

9. Kanis JA, Johnell O, Oden A, Sembo I, Redlund-Johnell I, Dawson A, et al. Long-term risk of osteoporotic fracture in Malmo. Osteoporos Int. 2000;11(8):669–74. Epub 2000/11/30. 11095169.

10. Melton LJ, Chrischilles EA 3rd, Cooper C, Lane AW, Riggs BL. Perspective. How many women have osteoporosis? J Bone Miner Res. 1992;7(9):1005–10. Epub 1992/09/01. doi: 10.1002/jbmr.5650070902 1414493.

11. van MO. Osteoporosis and the Nature of Fragility Fracture: An Overview. In: Hertz K., Santy-Tomlinson J. (eds). Fragility Fracture Nursing Perspectives in Nursing Management and Care for Older AdultsSpringer, Cham. 2018. doi: 10.1007/978-3-319-76681-2_1

12. Trailokya A, Srivastava A, Bhole M, Zalte N. Calcium and Calcium Salts. J Assoc Physicians India. 2017;65(2):100–3. Epub 2017/05/01. 28457049.

13. Kressel GW, M. Hahn A. Bioavailability and Solubility of Different Calcium-Salts as a Basis for Calcium Enrichment of Beverages. Food and Nutrition Sciences. 2010;1(2):6. doi: 10.4236/fns.2010.12009

14. Roth Bassell HAC F.M. In Vitro Solubility Characteristics of Six Calcium Salts. Journal of Food Protection. 1992;55(12):3.

15. Li X YX, Liu X, He W, Huang Q, Li S, Feng Q. Calcium carbonate nanoparticles promote osteogenesis compared to adipogenesis in human bone-marrow mesenchymal stem cells. Progress in Natural Science: Materials International. 2018;28(5):11. doi: 10.1016/j.pnsc.2018.09.004

16. Calcium salts. The American Society of Health System Pharmacists 2017.

17. Drop LJ, Cullen DJ. Comparative effects of calcium chloride and calcium gluceptate. Br J Anaesth. 1980;52(5):501–5. Epub 1980/05/01. doi: 10.1093/bja/52.5.501 7387803.

18. An S, Gao Y, Ling J, Wei X, Xiao Y. Calcium ions promote osteogenic differentiation and mineralization of human dental pulp cells: implications for pulp capping materials. J Mater Sci Mater Med. 2012;23(3):789–95. Epub 2011/12/23. doi: 10.1007/s10856-011-4531-0 22190198.

19. Viti F, Landini M, Mezzelani A, Petecchia L, Milanesi L, Scaglione S. Osteogenic Differentiation of MSC through Calcium Signaling Activation: Transcriptomics and Functional Analysis. PLoS One. 2016;11(2):e0148173. Epub 2016/02/02. doi: 10.1371/journal.pone.0148173 26828589; PubMed Central PMCID: PMC4734718.

20. La Noce M, Mele L, Laino L, Iolascon G, Pieretti G, Papaccio G, et al. Cytoplasmic Interactions between the Glucocorticoid Receptor and HDAC2 Regulate Osteocalcin Expression in VPA-Treated MSCs. Cells. 2019;8(3). Epub 2019/03/08. doi: 10.3390/cells8030217 30841579; PubMed Central PMCID: PMC6468918.

21. Spina A, Montella R, Liccardo D, De Rosa A, Laino L, Mitsiadis TA, et al. NZ-GMP Approved Serum Improve hDPSC Osteogenic Commitment and Increase Angiogenic Factor Expression. Front Physiol. 2016;7:354. Epub 2016/09/07. doi: 10.3389/fphys.2016.00354 27594842; PubMed Central PMCID: PMC4990559.

22. Zhang F, Cui J, Liu X, Lv B, Xie Z, Yu B. Roles of microRNA-34a targeting SIRT1 in mesenchymal stem cells. Stem Cell Res Ther. 2015;6:195. Epub 2015/10/09. doi: 10.1186/s13287-015-0187-x 26446137; PubMed Central PMCID: PMC4597437.

23. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63. Epub 1983/12/16. doi: 10.1016/0022-1759(83)90303-4 [pii]. 6606682.

24. Wu B, Zhu JS, Zhang Y, Shen WM, Zhang Q. Predictive value of MTT assay as an in vitro chemosensitivity testing for gastric cancer: one institution's experience. World J Gastroenterol. 2008;14(19):3064–8. Epub 2008/05/22. doi: 10.3748/wjg.14.3064 18494060; PubMed Central PMCID: PMC2712176.

25. Liu K, Liu PC, Liu R, Wu X. Dual AO/EB staining to detect apoptosis in osteosarcoma cells compared with flow cytometry. Med Sci Monit Basic Res. 2015;21:15–20. Epub 2015/02/11. doi: 10.12659/MSMBR.893327 25664686; PubMed Central PMCID: PMC4332266.

26. Gregory CA, Gunn WG, Peister A, Prockop DJ. An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem. 2004;329(1):77–84. Epub 2004/05/12. doi: 10.1016/j.ab.2004.02.002 15136169.

27. Schlebusch H RW, Lang M, Knedel M. Normbereiche der Aktivitäten klinisch wichtiger Enzyme. Dtsch Med Wochenschr 1974;99:2.

28. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985;150(1):76–85. Epub 1985/10/01. doi: 10.1016/0003-2697(85)90442-7 3843705.

29. Luo X, Barbieri D, Davison N, Yan Y, de Bruijn JD, Yuan H. Zinc in calcium phosphate mediates bone induction: in vitro and in vivo model. Acta Biomater. 2014;10(1):477–85. Epub 2013/10/22. doi: 10.1016/j.actbio.2013.10.011 24140609.

30. Wegler C, Wikvall K, Norlin M. Effects of Osteoporosis-Inducing Drugs on Vitamin D-Related Gene Transcription and Mineralization in MG-63 and Saos-2 Cells. Basic Clin Pharmacol Toxicol. 2016;119(5):436–42. Epub 2016/04/22. doi: 10.1111/bcpt.12612 27098343.

31. Zofkova I, Davis M, Blahos J. Trace elements have beneficial, as well as detrimental effects on bone homeostasis. Physiol Res. 2017;66(3):391–402. Epub 2017/03/02. doi: 933454 28248532.

32. Plikerd WD, Mahendra Kumar Branton, Alice Trivedi, Dahryn Nayak, Gopal Gangwar, Mayank Jana, Snehasis. Impact of Biofield Energy Healing Treated Vitamin D3 on Human Osteoblast Cell Line (MG-63) for Bone Health. American Journal of Clinical and Experimental Medicine. 2018;6(1):9. Epub Jan. 10, 2018. doi: 10.11648/j.ajcem.20180601.11

33. Ghorbanzadeh A, Aminsobhani M, Khoshzaban A, Abbaszadeh A, Bolhari B, Shamshiri AR. Cytotoxic Effects and Osteogenic Activity of Calcium Sulfate with and without Recombinant Human Bone Morphogenetic Protein 2 and Nano-Hydroxyapatite Adjacent to MG-63 Cell Line. J Dent (Tehran). 2015;12(5):352–63. Epub 2016/02/16. 26877731; PubMed Central PMCID: PMC4749100.

34. Sun L, Pereira D, Wang Q, Barata DB, Truckenmuller R, Li Z, et al. Controlling Growth and Osteogenic Differentiation of Osteoblasts on Microgrooved Polystyrene Surfaces. PLoS One. 2016;11(8):e0161466. Epub 2016/08/30. doi: 10.1371/journal.pone.0161466 27571520; PubMed Central PMCID: PMC5003369.

35. Yang JY, Ting YC, Lai JY, Liu HL, Fang HW, Tsai WB. Quantitative analysis of osteoblast-like cells (MG63) morphology on nanogrooved substrata with various groove and ridge dimensions. J Biomed Mater Res A. 2009;90(3):629–40. Epub 2008/06/20. doi: 10.1002/jbm.a.32130 18563818.

36. Xiong Y, Yang HJ, Feng J, Shi ZL, Wu LD. Effects of alendronate on the proliferation and osteogenic differentiation of MG-63 cells. J Int Med Res. 2009;37(2):407–16. Epub 2009/04/23. doi: 10.1177/147323000903700216 19383235.

37. La Noce M, Paino F, Mele L, Papaccio G, Regad T, Lombardi A, et al. HDAC2 depletion promotes osteosarcoma's stemness both in vitro and in vivo: a study on a putative new target for CSCs directed therapy. J Exp Clin Cancer Res. 2018;37(1):296. Epub 2018/12/05. doi: 10.1186/s13046-018-0978-x 30509303; PubMed Central PMCID: PMC6276256.

38. Papaccio F, Paino F, Regad T, Papaccio G, Desiderio V, Tirino V. Concise Review: Cancer Cells, Cancer Stem Cells, and Mesenchymal Stem Cells: Influence in Cancer Development. Stem Cells Transl Med. 2017;6(12):2115–25. Epub 2017/10/27. doi: 10.1002/sctm.17-0138 29072369; PubMed Central PMCID: PMC5702541.

39. Brini M, Cali T, Ottolini D, Carafoli E. Intracellular calcium homeostasis and signaling. Met Ions Life Sci. 2013;12:119–68. Epub 2013/04/19. doi: 10.1007/978-94-007-5561-1_5 23595672.

40. Palta S, Saroa R, Palta A. Overview of the coagulation system. Indian J Anaesth. 2014;58(5):515–23. Epub 2014/12/24. doi: 10.4103/0019-5049.144643 25535411; PubMed Central PMCID: PMC4260295.

41. Ferguson JH. THE BLOOD CALCIUM AND THE CALCIUM FACTOR IN BLOOD COAGULATION. Physiological Reviews. 1936;16(4):31. doi: 10.1152/physrev.1936.16.4.640

42. Manolagas SC, Parfitt AM. What old means to bone. Trends Endocrinol Metab. 2010;21(6):369–74. Epub 2010/03/13. doi: 10.1016/j.tem.2010.01.010 20223679; PubMed Central PMCID: PMC2880220.

43. Marie PJ, Kassem M. Osteoblasts in osteoporosis: past, emerging, and future anabolic targets. Eur J Endocrinol. 2011;165(1):1–10. Epub 2011/05/06. doi: 10.1530/EJE-11-0132 21543379.

44. Tai V, Leung W, Grey A, Reid IR, Bolland MJ. Calcium intake and bone mineral density: systematic review and meta-analysis. BMJ. 2015;351:h4183. Epub 2015/10/01. doi: 10.1136/bmj.h4183 26420598; PubMed Central PMCID: PMC4784773.

45. Maeno S, Niki Y, Matsumoto H, Morioka H, Yatabe T, Funayama A, et al. The effect of calcium ion concentration on osteoblast viability, proliferation and differentiation in monolayer and 3D culture. Biomaterials. 2005;26(23):4847–55. Epub 2005/03/15. doi: 10.1016/j.biomaterials.2005.01.006 15763264.

46. Bermudez-Reyes B, Del Refugio Lara-Banda M, Reyes-Zarate E, Rojas-Martinez A, Camacho A, Moncada-Saucedo N, et al. Effect on growth and osteoblast mineralization of hydroxyapatite-zirconia (HA-ZrO2) obtained by a new low temperature system. Biomed Mater. 2018;13(3):035001. Epub 2018/02/21. doi: 10.1088/1748-605X/aaa3a4 29461975.

47. Golub EEB-B, Kathleen. The role of alkaline phosphatase in minerlization. Current Opinion in Orthopaedics. 2007;18(5):5. doi: 10.1097/BCO.0b013e3282630851

48. Feng H, Cheng T, Pavlos NJ, Yip KH, Carrello A, Seeber R, et al. Cytoplasmic terminus of vacuolar type proton pump accessory subunit Ac45 is required for proper interaction with V(0) domain subunits and efficient osteoclastic bone resorption. J Biol Chem. 2008;283(19):13194–204. Epub 2008/01/30. doi: 10.1074/jbc.M709712200 18227071; PubMed Central PMCID: PMC2442344.

49. Feng J, Shi Z, Ye Z. Effects of metabolites of the lignans enterolactone and enterodiol on osteoblastic differentiation of MG-63 cells. Biol Pharm Bull. 2008;31(6):1067–70. Epub 2008/06/04. doi: 10.1248/bpb.31.1067 [pii]. 18520031.

50. Cheng YH, Hooker RA, Nguyen K, Gerard-O'Riley R, Waning DL, Chitteti BR, et al. Pyk2 regulates megakaryocyte-induced increases in osteoblast number and bone formation. J Bone Miner Res. 2013;28(6):1434–45. Epub 2013/01/31. doi: 10.1002/jbmr.1876 23362087; PubMed Central PMCID: PMC3663900.

51. Welldon KJ, Findlay DM, Evdokiou A, Ormsby RT, Atkins GJ. Calcium induces pro-anabolic effects on human primary osteoblasts associated with acquisition of mature osteocyte markers. Mol Cell Endocrinol. 2013;376(1–2):85–92. Epub 2013/06/25. doi: 10.1016/j.mce.2013.06.013 23791847.

52. Li Z, Lu WW, Chiu PK, Lam RW, Xu B, Cheung KM, et al. Strontium-calcium coadministration stimulates bone matrix osteogenic factor expression and new bone formation in a large animal model. J Orthop Res. 2009;27(6):758–62. Epub 2008/11/26. doi: 10.1002/jor.20818 19025756.

53. Mathews S, Gupta PK, Bhonde R, Totey S. Chitosan enhances mineralization during osteoblast differentiation of human bone marrow-derived mesenchymal stem cells, by upregulating the associated genes. Cell Prolif. 2011;44(6):537–49. Epub 2011/10/21. doi: 10.1111/j.1365-2184.2011.00788.x 22011046.

54. Fisher LW, Fedarko NS. Six genes expressed in bones and teeth encode the current members of the SIBLING family of proteins. Connect Tissue Res. 2003;44 Suppl 1:33–40. Epub 2003/09/04. 12952171.

55. Choi ST, Kim JH, Kang EJ, Lee SW, Park MC, Park YB, et al. Osteopontin might be involved in bone remodelling rather than in inflammation in ankylosing spondylitis. Rheumatology (Oxford). 2008;47(12):1775–9. Epub 2008/10/16. doi: 10.1093/rheumatology/ken385 18854347.

56. Alford AI, Hankenson KD. Matricellular proteins: Extracellular modulators of bone development, remodeling, and regeneration. Bone. 2006;38(6):749–57. Epub 2006/01/18. doi: 10.1016/j.bone.2005.11.017 16412713.

57. Shen Q, Christakos S. The vitamin D receptor, Runx2, and the Notch signaling pathway cooperate in the transcriptional regulation of osteopontin. J Biol Chem. 2005;280(49):40589–98. Epub 2005/10/01. doi: 10.1074/jbc.M504166200 16195230.

58. Khaskhali MH, Byer KJ, Khan SR. The effect of calcium on calcium oxalate monohydrate crystal-induced renal epithelial injury. Urol Res. 2009;37(1):1–6. Epub 2008/11/14. doi: 10.1007/s00240-008-0160-6 19005647; PubMed Central PMCID: PMC3615550.

59. Sun XY, Gan QZ, Ouyang JM. Calcium oxalate toxicity in renal epithelial cells: the mediation of crystal size on cell death mode. Cell Death Discov. 2015;1:15055. Epub 2015/01/01. doi: 10.1038/cddiscovery.2015.55 27551481; PubMed Central PMCID: PMC4979418.

60. Etcheverry P, Wallingford JC, Miller DD, Glahn RP. The effect of calcium salts, ascorbic acid and peptic pH on calcium, zinc and iron bioavailabilities from fortified human milk using an in vitro digestion/Caco-2 cell model. Int J Vitam Nutr Res. 2005;75(3):171–8. Epub 2005/07/21. doi: 10.1024/0300-9831.75.3.171 16028632.

61. Astashkina AI, Mann BK, Prestwich GD, Grainger DW. 'Erratum to "Comparing predictive drug nephrotoxicity biomarkers in kidney 3-D primary organoid culture and immortalized cell lines" [Biomaterials 33 (2012) 4712–4721]'. Biomaterials. 2015;38:108. Epub 2014/12/17. doi: 10.1016/j.biomaterials.2014.10.072 25499931.

62. Tiong HY, Huang P, Xiong S, Li Y, Vathsala A, Zink D. Drug-induced nephrotoxicity: clinical impact and preclinical in vitro models. Mol Pharm. 2014;11(7):1933–48. Epub 2014/02/08. doi: 10.1021/mp400720w 24502545.

Effect of calcium glucoheptonate on proliferation and osteogenesis of osteoblast-like cells in vitro

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