Sains Malaysiana 50(1)(2021): 239-251

http://dx.doi.org/10.17576/jsm-2021-5001-23

 

Effect of Sulfur on Nitrogen-Containing Plasma Polymers in Promoting Osteogenic Differentiation of Wharton’s Jelly Mesenchymal Stem Cells

(Kesan Sulfur ke atas Polimer Plasma yang Mengandungi Nitrogen dalam Mempromosi Pembezaan Osteogen Sel Stem Mesenkima Jeli Wharton)

 

KIM SHYONG SIOW1*, ARIFAH RAHMAN1, AMNANI AMINUDDIN2 & PEI YUEN NG2

 

1Institute of Microengineering and Nanoelectronics, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor Darul Ehsan, Malaysia

 

2Drug and Herbal Research Centre, Faculty of Pharmacy, Universiti Kebangsaan Malaysia, 50300 Kuala Lumpur, Federal Territory, Malaysia

 

Diserahkan: 11 April 2020/Diterima: 14 Jun 2020

 

ABSTRACT

The role of sulfur and its synergistic effects with nitrogen moieties in mediating stem cell proliferation and differentiation has become of interest to the tissue engineering community due to chemical similarities with the glycosaminoglycans found in human tissues and cells. Glycosaminoglycans are biomolecules known to influence stem cell differentiation, but the roles of sulfur with different oxidation states on nitrogen-containing polymers have not been fully understood nor investigated. In this study, we used the plasma polymerization of 1,7-octadiene (ppOD), n-heptylamine (ppHA), ppHA grafted with vinyl-sulfonate via Michael-type addition (ppHA-SO3), thiophene (ppT), and ppT with air plasma treatment (ppT-air) to produce controlled amounts of nitrogen and sulfur moieties having different oxidation states, as confirmed by x-ray photoelectron spectroscopy. Assays of the proliferation and osteogenic activities of Wharton’s jelly mesenchymal stem cells (WJ-MSCs) showed the highest activities for ppHA, followed by ppHA-SO3, due to high percentages of amines/amides and the absence of SO3 moieties in ppHA. Other plasma polymers showed less proliferation and osteogenic differentiation than the positive control (glass substrate); however, WJ-MSCs grown on ppT-air with its high percentages of SO4 displayed cytoskeletons intensified with actin stress fiber, unlike the thiol-dominated ppT. Finally, the presence of methyl groups in ppOD severely limited WJ-MSCs proliferation and differentiation. Overall, these results confirm the beneficial effects of amine/amide groups on WJ-MSCs proliferation and osteogenic differentiation, but the combination of these groups with sulfur of various oxidation states failed to further enhance such cellular activities.

 

Keywords: Amine-amide; osteogenic differentiation; plasma polymerization; plasma treatment; sulfonate-sulfate

 

ABSTRAK

Peranan sulfur dan kesan sinerginya dengan molekul nitrogen dalam pertumbuhan dan pembezaan sel stem telah mendapat perhatian komuniti kejuruteraan tisu kerana persamaan kimianya dengan glikosaminoglikan yang terdapat di dalam tisu dan sel manusia. Glikosaminoglikan dikenali sebagai biomolekul yang dapat mempengaruhi pembezaan sel stem. Walau bagaimanapun, peranan sulfur yang mempunyai tahap pengoksidaan yang berbeza di dalam polimer yang mengandungi nitrogen masih kurang difahami. Justeru, kajian ini menggunakan pempolimeran plasma 1,7-oktadiena (ppOD), n-heptilamina (ppHA), ppHA yang dicantum dengan vinil-sulfonat melalui penambahan Michael (ppHA-SO3), tiofena (ppT) dan ppT dengan rawatan plasma udara (ppT-udara) untuk menghasilkan moieti nitrogen dan sulfur yang mempunyai keadaan pengoksidaan yang berbeza yang dikenal pasti dengan spektroskopi fotoelektron x-ray. ppHA menunjukkan aktiviti pertumbuhan dan pembahagian osteogen sel stem mesenkima jeli Wharton (WJ-MSC) yang paling tinggi diikuti oleh ppHA-SO3. Keputusan ini berpunca daripada kandungan peratusan amina/amida yang tinggi dan ketiadaan moieti SO3 dalam salutan ppHA. Manakala, polimer plasma lain menunjukkan aktiviti pertumbuhan dan pembahagian osteogen WJ-MSC yang rendah berbanding dengan kawalan positif (substrat kaca). Walau bagaimanapun, ppT-udara yang mengandungi peratusan SO4 yang tinggi menunjukkan pertumbuhan WJ-MSC dengan sitoskeletonnya diperkuat dengan gentian tegangan aktin berbanding dengan ppT yang mempunyai kandungan tiol yang tinggi. Selain itu, ppOD menunjukkan pengurangan yang ketara dalam aktiviti pertumbuhan dan pembahagian osteogen WJ-MSC disebabkan oleh kehadiran kumpulan metil. Secara keseluruhannya, kajian ini membuktikan bahawa kumpulan amina/amida mampu memberi kesan yang positif dalam pertumbuhan dan pembahagian osteogen WJ-MSC. Namun demikian, kombinasi kumpulan amina/amida dengan sulfur yang mengandungi pelbagai keadaan pengoksidaan gagal untuk meningkatkan  akitiviti sel.

 

Kata kunci: Amina-amida; pembahagian osteogen; pempolimeran plasma; rawatan plasma; sulfonat-sulfat

 

RUJUKAN

Akhavan, B., Jarvis, K. & Majewski, P. 2014. Development of oxidized sulfur polymer films through a combination of plasma polymerization and oxidative plasma treatment. Langmuir 30(5): 1444-1454.

Beamson, G. & Briggs, D. 1992. High resolution XPS of organic polymers. Journal of Chemical Education 70(1): A25.

Beck, A.J., Whittle, J.D., Bullett, N.A., Eves, P., Mac Neil, S., McArthur, S.L. & Shard, A.G. 2005. Plasma co-polymerisation of two strongly interacting monomers: Acrylic acid and allylamine. Plasma Processes and Polymers 2(8): 641-649.

Bruderer, M., Richards, R.G., Alini, M. & Stoddart, M.J. 2014. Role and regulation of RUNX2 in osteogenesis. European Cells and Materials 28: 269-286.

Chan, Y.W., Siow, K.S., Ng, P.Y., Gires, U. & Majlis, B.Y. 2016. Plasma polymerized carvone as an antibacterial and biocompatible coating. Materials Science and Engineering: C 68: 861-871.

Chen, T.F., Siow, K.S., Ng, P.Y., Nai, M.H., Lim, C.T. & Yeop Majlis, B. 2016. Ageing properties of polyurethane methacrylate and off-stoichiometry thiol-ene polymers after nitrogen and argon plasma treatment. Journal of Applied Polymer Science 133(42): 133.

da Costa, D.S., Pires, R.A., Frias, A.M., Reis, R.L. & Pashkuleva, I. 2012. Sulfonic groups induce formation of filopodia in mesenchymal stem cells. Journal of Materials Chemistry 22(15): 7172-7178.

Curran, J.M., Fawcett, S., Hamilton, L., Rhodes, N.P., Rahman, C.V., Alexander, M., Shakesheff, K. & Hunt, J.A. 2013. The osteogenic response of mesenchymal stem cells to an injectable PLGA bone regeneration system. Biomaterials 34(37): 9352-9364.

Curran, J.M., Chen, R. & Hunt, J.A 2010a. Material induced mesenchymal stem cell differentiation. Biomaterials 31(6): 1463-1464.

Curran, J.M., Stokes, R., Irvine, E., Graham, D., Amro, N.A., Sanedrin, R.G., Jamil, H. & Hunt, J.A. 2010b. Introducing dip pen nanolithography as a tool for controlling stem cell behaviour: Unlocking the potential of the next generation of smart materials in regenerative medicine. Lab on a Chip 10(13): 1662-1670.

Curran, J.M., Chen, R. & Hunt, J.A. 2006. The guidance of human mesenchymal stem cell differentiation in vitro by controlled modifications to the cell substrate. Biomaterials 27(27): 4783-4793.

Fernandez-De-Cossio-DIaz, J. & Vazquez, A. 2018. A physical model of cell metabolism. Scientific Reports 8(1): 8349.

García, A.J. 2005. Get a grip: Integrins in cell-biomaterial interactions. Biomaterials 26(36): 7525-7529.

Ito, Y., Iguchi, Y., Kashiwagi, T. & Imanishi, Y. 1991. Synthesis and nonthrombogenicity of polyetherurethaneurea film grafted with poly(sodium vinyl sulfonate). Journal of Biomedical Materials Research 25(11): 1347-1361.

Keselowsky, B.G., Collard, D.M. & García, A.J. 2003. Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion. Journal of Biomedical Materials Research - Part A 66(2): 247-259.

Keshel, S.H., Azhdadi, S.N.K., Asefnezhad, A., Sadraeian, M., Montazeri, M. & Biazar, E. 2011. The relationship between cellular adhesion and surface roughness for polyurethane modified by microwave plasma radiation. International Journal of Nanomedicine 6: 641-647.

Kirkham, G.R. & Cartmell, S.H. 2007. Genes and proteins involved in the regulation of osteogenesis. Genes and Osteogenesis 3: 1-22.

Klee, D., Villari, R.V., Höcker, H., Dekker, B. & Mittermayer, C. 1994. Surface modification of a new flexible polymer with improved cell adhesion. Journal of Materials Science: Materials in Medicine 5(9-10): 592-595.

Liu, X., He, J., Zhang, S., Wang, X.M., Liu, H.Y. & Cui, F.Z. 2013. Adipose stem cells controlled by surface chemistry. Journal of Tissue Engineering and Regenerative Medicine 7(2): 112-117.

Liu, X., Feng, Q., Bachhuka, A. & Vasilev, K. 2014. Surface modification by allylamine plasma polymerization promotes osteogenic differentiation of human adipose-derived stem cells. ACS Applied Materials and Interfaces 6(12): 9733-9741.

Liu, X., Shi, S., Feng, Q., Bachhuka, A., He, W., Huang, Q., Zhang, R., Yang, X. & Vasilev, K. 2015. Surface chemical gradient affects the differentiation of human adipose-derived stem cells via ERK1/2 signaling pathway. ACS Applied Materials and Interfaces 7(33): 18473-18482.

Mager, M.D., LaPointe, V. & Stevens, M.M. 2011. Exploring and exploiting chemistry at the cell surface. Nature Chemistry 3(8): 582-589.

Manton, K.J., Leong, D.F., Cool, S.M. & Nurcombe, V. 2007. Disruption of heparan and chondroitin sulfate signaling enhances mesenchymal stem cell-derived osteogenic differentiation via bone morphogenetic protein signaling pathways. Stem Cells 25(11): 2845-2854.

Moursi, A.M., Globus, R.K. & Damsky, C.H. 1997. Interactions between integrin receptors and fibronectin are required for calvarial osteoblast differentiation in vitro. Journal of Cell Science 110(18): 2187-2196.

Phillips, J.E., Petrie, T.A., Creighton, F.P. & García, A.J. 2010. Human mesenchymal stem cell differentiation on self-assembled monolayers presenting different surface chemistries. Acta Biomaterialia 6(1): 12-20.

Röder, A., García-Gareta, E., Theodoropoulos, C., Ristovski, N., Blackwood, K.A. & Woodruff, M.A. 2015. An assessment of cell culture plate surface chemistry for in vitro studies of tissue engineering scaffolds. Journal of Functional Biomaterials 6(4): 1054-1063.

Rutkovskiy, A., Stensløkken, K.O. & Vaage, I.J. 2016. Osteoblast differentiation at a glance. Medical Science Monitor Basic Research 22: 95-106.

Sandstrom, A.M., Jasieniak, M., Griesser, H.J., Grøndahl, L. & Cooper-White, J.J. 2013. Effects of varying heptylamine and propionaldehyde plasma polymerization parameters on mesenchymal stem cell attachment. Plasma Processes and Polymers 10(1): 19-28.

Scotchford, C.A., Gilmore, C.P., Cooper, E., Leggett, G.J. & Downes, S. 2002. Protein adsorption and human osteoblast-like cell attachment and growth on alkylthiol on gold self-assembled monolayers. Journal of Biomedical Materials Research 59(1): 84-99.

Shen, C., Yang, C., Xu, S. & Zhao, H. 2019. Comparison of osteogenic differentiation capacity in mesenchymal stem cells derived from human amniotic membrane (AM), umbilical cord (UC), chorionic membrane (CM), and decidua (DC). Cell and Bioscience 9(1): 17.

Shen, Y., Liu, W., Lin, K., Pan, H., Darvell, B.W., Peng, S., Wen, C., Deng, L., Lu, W.W. & Chang, J. 2011. Interfacial pH: A critical factor for osteoporotic bone regeneration. Langmuir 27(6): 2701-2708.

Silver, J.H., Lin, J.C., Lim, F., Tegoulia, V.A., Chaudhury, M.K. & Cooper, S.L. 1999. Surface properties and hemocompatibility of alkyl-siloxane monolayers supported on silicone rubber: Effect of alkyl chain length and ionic functionality. Biomaterials 20(17): 1533-1543.

Siow, K.S. 2018. Low pressure plasma modifications for the generation of hydrophobic coatings for biomaterials applications. Plasma Processes and Polymers 15(9): 1800059.

Siow, K.S., Rahman, A.S.A., Ng, P.Y. & Majlis, B.Y. 2020. Sulfur and nitrogen containing plasma polymers reduces bacterial attachment and growth. Materials Science and Engineering C 107: 110225.

Siow, K.S., Britcher, L., Kumar, S. & Griesser, H.J. 2019. QCM-D and XPS study of protein adsorption on plasma polymers with sulfonate and phosphonate surface groups. Colloids and Surfaces B: Biointerfaces 173: 447-453.

Siow, K.S., Britcher, L., Kumar, S. & Griesser, H.J. 2018. XPS study of sulfur and phosphorus compounds with different oxidation states. Sains Malaysiana 47(8): 1913-1922.

Siow, K.S., Britcher, L., Kumar, S. & Griesser, H.J. 2017. Plasma polymers containing sulfur and their co-polymers with 1,7-octadiene: Chemical and structural analysis. Plasma Processes and Polymers 14(3): 1600044.

Siow, K.S., Kumar, S. & Griesser, H.J. 2015. Low-pressure plasma methods for generating non-reactive hydrophilic and hydrogel-like bio-interface coatings - A review. Plasma Processes and Polymers 12(1): 8-24.

Siow, K.S., Britcher, L., Kumar, S. & Griesser, H.J. 2014. Deposition and XPS and FTIR analysis of plasma polymer coatings containing phosphorus. Plasma Processes and Polymers 11(2): 133-141.

Smane, L. & Pilmane, M. 2016. Osteopontin, osteocalcin, and osteoprotegerin expression in human tissue affected by cleft lip and palate. SHS Web of Conferences 30: 00008.

Stein, G.S., Lian, J.B., Van Wijnen, A.J., Stein, J.L., Montecino, M., Javed, A., Zaidi, S.K., Young, D.W., Choi, J.Y. & Pockwinse, S.M. 2004. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene 23(24): 4315-4329.

Uygun, B.E., Stojsih, S.E. & Matthew, H.W. 2009. Effects of immobilized glycosaminoglycans on the proliferation and differentiation of mesenchymal stem cells. Tissue Engineering - Part A 15(11): 3499-3512.

Wang, Y., Bai, C., Ruan, Y., Liu, M., Chu, Q., Qiu, L., Yang, C. & Li, B. 2019. Coordinative metabolism of glutamine carbon and nitrogen in proliferating cancer cells under hypoxia. Nature Communications 10(1): 201.

Wells, N., Baxter, M.A., Turnbull, J.E., Murray, P., Edgar, D., Parry, K.L., Steele, D.A. & Short, R.D. 2009. The geometric control of E14 and R1 mouse embryonic stem cell pluripotency by plasma polymer surface chemical gradients. Biomaterials 30(6): 1066-1070.

Xu, J.H., Li, Z.H., Hou, Y.D. & Fang, W.J. 2015. Potential mechanisms underlying the runx2 induced osteogenesis of bone marrow mesenchymal stem cells. American Journal of Translational Research 7(12): 2527-2535.

 

*Pengarang untuk surat-menyurat; email: kimsiow@ukm.edu.my

 

   

sebelumnya