Surface chemistry regulates the sensitivity and tolerability of osteoblasts to various magnitudes of fluid shear stress
Yan Li
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
School of Pharmacy, Taizhou Polytechnic College, Taizhou, 225300 China
Search for more papers by this authorJinfeng Wang
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Joint first author.
Search for more papers by this authorJuan Xing
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Search for more papers by this authorYuanliang Wang
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Search for more papers by this authorCorresponding Author
Yanfeng Luo
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Correspondence to: Y. F. Luo; e-mail: [email protected]Search for more papers by this authorYan Li
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
School of Pharmacy, Taizhou Polytechnic College, Taizhou, 225300 China
Search for more papers by this authorJinfeng Wang
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Joint first author.
Search for more papers by this authorJuan Xing
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Search for more papers by this authorYuanliang Wang
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Search for more papers by this authorCorresponding Author
Yanfeng Luo
Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400030 China
Research Center of Bioinspired Materials Science and Engineering, College of Bioengineering, Chongqing University, Chongqing, 400030 China
Correspondence to: Y. F. Luo; e-mail: [email protected]Search for more papers by this authorAbstract
Scaffolds provide a physical support for osteoblasts and act as the medium to transfer mechanical stimuli to cells. To verify our hypothesis that the surface chemistry of scaffolds regulates the perception of cells to mechanical stimuli, the sensitivity and tolerability of osteoblasts to fluid shear stress (FSS) of various magnitudes (5, 12, 20 dynes/cm2) were investigated on various surface chemistries (–OH, –CH3, –NH2), and their follow-up effects on cell proliferation and differentiation were examined as well. The sensitivity was characterized by the release of adenosine triphosphate (ATP), nitric oxide (NO) and prostaglandin E2 (PGE2) while the tolerability was by cellular membrane integrity. The cell proliferation was characterized by S-phase cell fraction and the differentiation by ALP activity and ECM expression (fibronectin and type I collagen). As revealed, osteoblasts demonstrated higher sensitivity and lower tolerability on OH and CH3 surfaces, yet lower sensitivity and higher tolerability on NH2 surfaces. Observations on the focal adhesion formation, F-actin organization and cellular orientation before and after FSS exposure suggest that the potential mechanism lies in the differential control of F-actin organization and focal adhesion formation by surface chemistry, which further divergently mediates the sensitivity and tolerability of ROBs to FSS and the follow-up cell proliferation and differentiation. These findings are essentially valuable for design/selection of desirable surface chemistry to orchestrate with FSS stimuli, inducing appropriate cell responses and promoting bone formation. © 2016 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 104A: 2978–2991, 2016.
REFERENCES
- 1 Sittichockechaiwut A, Scutt AM, Ryan AJ, Bonewald LF, Reilly GC. Use of rapidly mineralising osteoblasts and short periods of mechanical loading to accelerate matrix maturation in 3D scaffolds. Bone 2009; 44: 822–829.
- 2 Rath B, Nam J, Knobloch TJ, Lannutti JJ, Agarwal S. Compressive forces induce osteogenic gene expression in calvarial osteoblasts. J Biomech 2008; 41: 1095–1103.
- 3 Bancroft GN, Sikavitsas VI, Dolder J, Sheffield T, Ambrose CG, Jansen JA, Mikos AG. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci USA 2002; 99: 12600–12605.
- 4 Ingber DE. Mechanosensation through integrins: cells act locally but think globally. Proc Natl Acad Sci USA 2003; 100: 1472–1474.
- 5 Myers KA, Rattner JB, Shrive NG, Hart DA. Osteoblast-like cells and fluid flow: cytoskeleton-dependent shear sensitivity. Biochem Biophys Res Commun 2007; 364: 214–219.
- 6 Orr AW, Helmke BP, Blackman BR, Schwartz MA. Mechanisms of mechanotransduction. Dev Cell 2006; 10: 11–20.
- 7 Hayakawa K, Tatsumi H, Sokabe M. Actin stress fibers transmit and focus force to activate mechanosensitive channels. J Cell Sci 2008; 121: 496–503.
- 8 Keselowsky BG, Collard DM, Garcia AJ. Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding. Biomaterials 2004; 25: 5947–5954.
- 9 Hillsley MV, Frangos JA. Bone tissue engineering: the role of interstitial fluid flow. Biotechnol Bioeng 1994; 43: 573–581.
- 10 Gardinier JD, Majumdar S, Duncan RL, Wang LY. Cyclic hydraulic pressure and fluid flow differentially modulate cytoskeleton re-organization in MC3T3 osteoblasts. Cell Mol Bioeng 2009; 2: 133–143.
- 11 Basso N, Heersche JNM. Characteristics of in vitro osteoblastic cell loading models. Bone 2002; 30: 347–351.
- 12
Freed LE,
Vunjak-Novakovic G. Tissue engineering bioreactors. In: RP Lanza; R Langer, J. Vacanti editors, Principles of Tissue Engineering. San Diego, CA: Academic Press. 2000; 143–156.
10.1016/B978-012436630-5/50017-9 Google Scholar
- 13 Bancroft GN, Sikavitsas VI, Milos AG. Design of a flow perfusion bioreactor system for bone tissue engineering applications. Tiss Eng 2003; 9: 549–554.
- 14 Kapur S, Baylink DJ, Lau KH. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 2003; 32: 241–251.
- 15 Lee DY, Yeh CR, Chang SF, Lee PL, Chien S, Cheng CK, Chiu JJ. Integrin-mediated expression of bone formation-related genes in osteoblastlike cells in response to fluid shear stress: roles of extracellular matrix, Shc, and mitogen-activated protein kinase. J Bone Miner Res 2008; 23: 1140–1149.
- 16 Chen NX, Ryder KD, Pavalko FM, Turner CH, Burr DB, Qiu J, Duncan RL. Ca2+ regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am J Physiol Cell Physiol 2000; 278: 989–997.
- 17 Liu X, Zhang X, Lee I. A quantitative study on morphological responses of osteoblastic cells to fluid shear stress. Acta Biochim. Biophys Sin 2010; 42: 195–201.
- 18 Horikawa A, Okada K, Sato K, Sato M. Morphological changes in osteoblastic cells (MC3T3-E1) due to fluid shear stress: cellular damage by prolonged application of fluid shear stress. Tohoku J Exp Med 2000; 191: 127–137.
- 19 Sikavitsas VI, Temenoff JS, Mikos AG. Biomaterials and bone mechanotransduction. Biomaterials 2001; 22: 2581–2593.
- 20
Stevens HY,
Frangos JA. Bone cell responses to fluid flow. In: MH Helfrich, SH. Ralston (eds), Bone Research Protocols. Totowa, New Jersey: Humana Press Inc. 2003; 381–398.
10.1385/1-59259-366-6:381 Google Scholar
- 21 Li Y, Luo YF, Huang K, Xing J, Xie Z, Lin MP, Yang L, Wang YL. The responses of osteoblasts to fluid shear stress depend on substrate chemistries. Arch Biochem Biophys 2013; 539: 38–50.
- 22 Hong HG, Jiang M, Sligar SG, Bohn PW. Cysteine-specific surface tethering of genetically engineered cytochromes for fabrication of metalloprotein nanostructures. Langmuir 1994; 10: 153–158.
- 23 Faucheuxa N, Schweiss R, Lutzowa K, Werner C, Groth T. Self-assembled monolayers with different terminating groups as model substrates for cell adhesion studies. Biomaterials 2004; 25: 2721–2730.
- 24 Robey PG, Termine JD. Human bone cells in vitro. Calcif Tissue Int 1985; 37: 453–460.
- 25 Luo YF, Wang YL, Niu XF, Shang JF. Evaluation of the cytocompatibility of butanediamine- and RGDS-grafted poly(dl-lactic acid). Eur Polym J 2008; 44: 1390–1402.
- 26 Nauman EA, Risic KJ, Keaveny TM, Satcher RL. Quantitative assessment of steady and pulsatile flow fields in a parallel plate flow chamber. Ann Biomed Eng 1999; 27: 194–199.
- 27 Jacobs CR, Yellowley CE, Davis BR, Zhou Z, Cimbala JM, Donahue HJ. Differential effect of steady versus oscillating flow on bone cells. J Biomech 1998; 31: 969–976.
- 28 Castillo AB, Blundo JT, Chen JC, Lee KL, Yereddi NR, Jang E, Kumar S, Tang WJ, Zarrin S, Kim J, Jacobs CR. Focal adhesion kinase plays a role in osteoblast mechanotransduction in vitro but does not affect load-induced bone formation in vivo. PLoS One 2012; 7: e43291.
- 29 Mikkelsen UR, Fredsted A, Gissel H, Clausen T. Excitation-induced Ca2+ influx and muscle damage in the rat: loss of membrane integrity and impaired force recovery. J Physiol 2004; 559: 271–285.
- 30 Berg JM, Erikkson LGT, Claesson PM, Borve KGN. 3-component langmuir-blodgett-films with a controllable degree of polarity. Langmuir 1994; 10: 1225–1234.
- 31 Neve A, Corrado A, Cantatore FP. Osteoblast physiology in normal and pathological conditions. Cell Tissue Res 2011; 343: 289–302.
- 32 Mrksich M. Using self-assembled monolayers to model the extracellular matrix. Acta Biomater 2009; 5: 832–841.
- 33 Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta1. J Biol Chem 2002; 277: 37377–37381.
- 34 Stein GS, Lian JB, Owen TA. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. Faseb J 1990; 4: 3111–3123.
- 35 Yeatts AB, Fisher JP. Bone tissue engineering bioreactors: dynamic culture and the influence of shear stress. Bone 2011; 48: 171–181.
- 36 Sikavitsas VI, Bancroft GN, Holtorf HL, Jansen JA, Mikos AG. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci USA 2003; 100: 14683–14688.
- 37 Holtorf HL, Jansen JA, Mikos AG. Modulation of cell differentiation in bone tissue engineering constructs cultured in a bioreactor. Adv Exp Med Biol 2006; 585: 225–241.
- 38 Bacakova L, Filova E, Parizek M, Ruml T, Svorcik V. Modulation of cell adhesion, proliferation and differentiation on materials designed for body implants. Biotechnol Adv 2011; 29: 739–767.
- 39 Ren YJ, Zhang H, Huang H, Wang XM, Zhou ZY, Cui FZ, An YH. In vitro behavior of neural stem cells in response to different chemical functional groups. Biomaterials 2009; 30: 1036–1044.
- 40 Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg 1984; 66: 397–402.
- 41 Forwood MR, Turner CH. The response of rat tibiae to incremental bouts of mechanical loading: a quantum concept for bone formation. Bone 1994; 15: 603–609.
- 42 Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 1994; 27: 339–360.
- 43 Lam H, Qin YX. The effects of frequency-dependent dynamic muscle stimulation on inhibition of trabecular bone loss in a disuse model. Bone 2008; 43: 1093–1100.
- 44 Bakker AD, Soejima K, Klein-Nulend J, Burger EH. The production of nitric oxide and prostaglandin E2 by primary mouse bone cells is shear stress dependent. J Biomech 2001; 34: 671–677.
- 45 Su JH, Xu F, Lu XL, Lu TJ. Fluid flow induced calcium response in osteoblasts: mathematical modeling. J Biomech 2011; 44: 2040–2046.
- 46 Xing J, Li Y, Lin MP, Wang JF, Wu JC, Ma YF, Wang YL, Yang L, Luo YF. Surface chemistry modulates osteoblasts sensitivity to low fluid shear stress. J Biomed Mater Res A 2014; 102: 4151–4160.
- 47 Keselowsky BG, Collard DM, Garcia AJ. Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion. J Biomed Mater Res 2003; 66A: 247–259.
- 48 Arima Y, Iwata H. Preferential adsorption of cell adhesive proteins from complex media on self-assembled monolayers and its effect on subsequent cell adhesion. Acta Biomaterialia 2015; 26: 72–81.
- 49 You L, Sara T, Coyer SR, García AJ, Jacobs CR. Bone cells grown on micropatterned surfaces are more sensitive to fluid shear stress. Cell Mol Bioeng 2008; 1: 182–188.
- 50 Yamada M, Miyauchi T, Yamamoto A, Iwasa F, Takeuchi M, Anpo M, Sakurai K, Baba K, Ogawa T. Enhancement of adhesion strength and cellular stiffness of osteoblasts on mirror-polished titanium surface by UV-photofunctionalization. Acta Biomater 2010; 6: 4578–4588.
- 51 Ueki Y, Sakamoto N, Sato M. Direct measurement of shear strain in adherent vascular endothelial cells exposed to fluid shear stress. Biochem Biophys Res Commun 2010; 394: 94–99.
- 52 Lin M, Wang H, Ruan C, Xing J, Wang J, Li Y, Wang Y, Luo Y. Adsorption force of fibronectin on various surface chemistries and its vital role in osteoblast adhesion. Biomacromol 2015; 16: 973–984.
- 53 Fabrizius-Homan DJ, Cooper SL. Competitive adsorption of vitronectin with albumin, fibrinogen, and fibronectin on polymeric biomaterials. J Biomed Mater Res 1991; 25: 953–971.
- 54 Barrias CC, Martins MC, Almeida-Porada G, Barbosa MA, Granja PL. The correlation between the adsorption of adhesive proteins and cell behaviour on hydroxyl-methyl mixed self-assembled monolayers. Biomaterials 2009; 30: 307–316.
Citing Literature
