Refined fabrication of mechano-stimulating micro-platform for on-chip analyses of complex platelet behavior

Hyojae Kim; Chulgyu Song; Chaenyung Cha; Jinmu Jung; Jonghyun Oh

Journal of Industrial and Engineering Chemistry, Vol.84, 269-279, April, 2020

DOI10.1016/j.jiec.2020.01.008 Export Citation

Refined fabrication of mechano-stimulating micro-platform for on-chip analyses of complex platelet behavior

Hyojae Kim, Chulgyu Song¹, Chaenyung Cha^{2, †}, Jinmu Jung^{3, †}, and Jonghyun Oh^{3, †}

Department of Bio-nano System Engineering, Jeonbuk National University, Jeonju 561-756, South Korea
¹Department of Electronic Engineering, Jeonbuk National University, Jeonju 561-756, South Korea
²School of Materials Science and Engineering, Ulsan National Institute of Science and Technology (UNIST), Ulsan 44919, South Korea
³Division of Mechanical Design Engineering, Jeonbuk National University, Jeonju 561-756, South Korea

E-mail:, ,

Platelets can sense their surroundings as they crawl in search of optimal surface to adhere before activation, but the detailed mechanism has not been fully explored in different microenvironments. Herein, various aspects of platelet behavior, including morphology, movement and biomarker expression, were multilaterally examined on mechanically stimulating surfaces, with controlled rigidity and roughness, to elucidate the effect of microenvironment without chemical stimulus. The platelets demonstrated different movement behavior (e.g. back-and-forth and forward crawling), and motility, as well as varying degrees of spreading with lamellipodial and filopodial projections, based on varying mechanical microenvironments. Furthermore, after initial activation, the platelets all became stationary and the cell spreading became more prominent, while still maintaining their movement potential. P-selectin expression, along with α-granule and open canalicular system (OCS) distributions, all supported the morphological and movement behavior. These results strongly indicated that the mechanical microenvironment played a key role in the regulation of complex platelet activities.

Keywords:Platelet crawling;Platelet activation;Open canalicular systems;Granule secretion;P-selectin

[References]

M.H.F. Klinger, W. Jelkmann, J. Interferon Cytokine Res., 22, 913 (2002)
Koenen RR, Thromb. Haemost., 116, 605 (2016)
Lowenhaupt RW, Miller MA, Glueck HI, Thromb. Res., 3, 477 (1973)
Valone FH, Austen KF, Goetzl EJ, J. Clin. Invest., 54, 1100 (1974)
Duquesnoy RJ, Lorentsen D, Aster RH, Blood, 45, 741 (1975)
Lowenhaupt R, Glueck H, Miller M, Kline D, J. Lab. Clin. Med., 90, 37 (1977)
Hallam TJ, Rink TJ, Febs Lett., 186, 175 (1985)
Pitchford SC, Momi S, Baglioni S, Casali L, Giannini S, Rossi R, Page CP, Gresele P, Am. J. Respir. Crit. Care Med., 177, 604 (2008)
Gaertner F, Ahmad Z, Rosenberger G, Fan S, Nicolai L, Busch B, Yavuz G, Luckner M, Ishikawa-Ankerhold H, Hennel R, Cell, 171, 1368 (2017)
Kraemer BF, Borst O, Gehring EM, Schoenberger T, Urban B, Ninci E, et al., J. Mol. Med., 88, 1277 (2010)
Schmidt EM, Kraemer BF, Borst O, Munzer P, Schonberger T, Schmidt C, Leibrock C, Towhid ST, Seizer P, Kuhl D, Cell. Physiol. Biochem., 30, 259 (2012)
Webb NJA, Bottomley MJ, Watson CJ, Brenchley PEC, Clin. Sci., 94, 395 (1998)
Demoulin JB, Montano-Almendras CP, Am. J. Blood Res., 2, 44 (2012)
Ito E, Suzuki K, Yamato M, Yokoyama M, Sakurai Y, Okano T, J. Biomed. Mater. Res. A, 42, 148 (1998)
Kraemer BF, Schmidt C, Urban B, Bigalke B, Schwanitz L, Koch M, Seizer P, Schaller M, Gawaz M, Lindemann S, Platelets, 22, 415 (2011)
Selvadurai MV, Hamilton JR, Platelets, 29, 319 (2018)
Maclean JA, Schoenwaelder SM, Serotonin, Academic Press, Boston, pp.91 2019.
Ollivier V, Syvannarath V, Gros A, Butt A, Loyau S, Jandrot-Perrus M, Ho-Tin-Noe B, PLoS One, 9, e10471 (2014)
Qiu Y, Brown AC, Myers DR, Sakurai Y, Mannino RG, Tran R, Ahn B, Hardy ET, Kee MF, Kumar S, Bao G, Barker TH, Lam WA, Proc. Natl. Acad. Sci. U. S. A., 111, 14430 (2014)
Sandmann R, Koster S, Sci. Rep., 6, 22357 (2016)
Oh J, Kim G, Kralick F, Noh H, J. Microelectromech. Syst., 20, 811 (2011)
Kaminska M, Okroj W, Szymanski W, Jakubowski W, et al., Acta. Bioeng. Biomech., 11, 19 (2009)
Tsai WB, Grunkemeier JB, Horbett TA, J. Biomed. Mater. Res. A, 67, 1255 (2003)
Aslan JE, Itakura A, Gertz JM, McCarty OJ, Platelets and Megakaryocytes, Springer, New York, pp.91 2012.
Lee CW, Jang LL, Pan HJ, Chen YR, Chen CC, Lee CH, J. Nanobiotechnol., 14, 9 (2016)
Fritz M, Radmacher M, Gaub HE, Biophys. J., 66, 1328 (1994)
Bowen WR, Hilal N, Lovitt RW, Wright CJ, J. Membr. Sci., 154(2), 205 (1999)
Girasole M, Pompeo G, Cricenti A, Congiu-Castellano A, Andreola F, Serafino A, Frazer BH, Boumis G, Amiconi G, BBA Biomembranes, 1768, 1268 (2007)
Hartwig JH, J. Cell Biol., 118, 1421 (1992)
Koseoglu S, Peters CG, Fitch-Tewfik JL, Aisiku O, Danglot L, Galli T, Flaumenhaft R, Blood, 126, 651 (2015)
Peters CG, Michelson AD, Flaumenhaft R, Blood, 120, 199 (2012)
Sakurai Y, Fitch-Tewfik JL, Qiu Y, Ahn B, Myers DR, Tran R, Fay ME, Ding L, Spearman PW, Michelson AD, Blood, 531 (2015).
White JG, Blood, 69, 878 (1987)
Jang Y, Lee M, Kim H, Cha C, Jung J, Oh J, Biofabrication, 11, 035021 (2019)
Franco AT, Corken A, Ware J, Blood, 126, 582 (2015)
Yan M, Jurasz P, BBA Mol. Cell Res., 1863, 392 (2016)
Corum LE, Eichinger CD, Hsiao TW, Hlady V, Langmuir, 27(13), 8316 (2011)
Fatisson J, Mansouri S, Yacoub D, Merhi Y, Tabrizian M, J. R. Soc. Interface, 8, 988 (2011)
Kunze A, Hesse C, Svedhem S, Colloids Surf. B: Biointerfaces, 116, 446 (2014)
Jacquemet G, Hamidi H, Ivaska J, Curr. Opin. Cell Biol., 36, 23 (2015)
Park JY, Gemmell CH, Davies JE, Biomaterials, 22, 2671 (2001)
Xu LC, Runt J, Siedlecki CA, Acta Biomater.., 6, 1938 (2010)
Godo MN, Sefton MV, Biomaterials, 20, 1117 (1999)

[1] M.H.F. Klinger, W. Jelkmann, J. Interferon Cytokine Res., 22, 913 (2002)

[2] Koenen RR, Thromb. Haemost., 116, 605 (2016)

[3] Lowenhaupt RW, Miller MA, Glueck HI, Thromb. Res., 3, 477 (1973)

[4] Valone FH, Austen KF, Goetzl EJ, J. Clin. Invest., 54, 1100 (1974)

[5] Duquesnoy RJ, Lorentsen D, Aster RH, Blood, 45, 741 (1975)

[6] Lowenhaupt R, Glueck H, Miller M, Kline D, J. Lab. Clin. Med., 90, 37 (1977)

[7] Hallam TJ, Rink TJ, Febs Lett., 186, 175 (1985)

[8] Pitchford SC, Momi S, Baglioni S, Casali L, Giannini S, Rossi R, Page CP, Gresele P, Am. J. Respir. Crit. Care Med., 177, 604 (2008)

[9] Gaertner F, Ahmad Z, Rosenberger G, Fan S, Nicolai L, Busch B, Yavuz G, Luckner M, Ishikawa-Ankerhold H, Hennel R, Cell, 171, 1368 (2017)

[10] Kraemer BF, Borst O, Gehring EM, Schoenberger T, Urban B, Ninci E, et al., J. Mol. Med., 88, 1277 (2010)

[11] Schmidt EM, Kraemer BF, Borst O, Munzer P, Schonberger T, Schmidt C, Leibrock C, Towhid ST, Seizer P, Kuhl D, Cell. Physiol. Biochem., 30, 259 (2012)

[12] Webb NJA, Bottomley MJ, Watson CJ, Brenchley PEC, Clin. Sci., 94, 395 (1998)

[13] Demoulin JB, Montano-Almendras CP, Am. J. Blood Res., 2, 44 (2012)

[14] Ito E, Suzuki K, Yamato M, Yokoyama M, Sakurai Y, Okano T, J. Biomed. Mater. Res. A, 42, 148 (1998)

[15] Kraemer BF, Schmidt C, Urban B, Bigalke B, Schwanitz L, Koch M, Seizer P, Schaller M, Gawaz M, Lindemann S, Platelets, 22, 415 (2011)

[16] Selvadurai MV, Hamilton JR, Platelets, 29, 319 (2018)

[17] Maclean JA, Schoenwaelder SM, Serotonin, Academic Press, Boston, pp.91 2019.

[18] Ollivier V, Syvannarath V, Gros A, Butt A, Loyau S, Jandrot-Perrus M, Ho-Tin-Noe B, PLoS One, 9, e10471 (2014)

[19] Qiu Y, Brown AC, Myers DR, Sakurai Y, Mannino RG, Tran R, Ahn B, Hardy ET, Kee MF, Kumar S, Bao G, Barker TH, Lam WA, Proc. Natl. Acad. Sci. U. S. A., 111, 14430 (2014)

[20] Sandmann R, Koster S, Sci. Rep., 6, 22357 (2016)

[21] Oh J, Kim G, Kralick F, Noh H, J. Microelectromech. Syst., 20, 811 (2011)

[22] Kaminska M, Okroj W, Szymanski W, Jakubowski W, et al., Acta. Bioeng. Biomech., 11, 19 (2009)

[23] Tsai WB, Grunkemeier JB, Horbett TA, J. Biomed. Mater. Res. A, 67, 1255 (2003)

[24] Aslan JE, Itakura A, Gertz JM, McCarty OJ, Platelets and Megakaryocytes, Springer, New York, pp.91 2012.

[25] Lee CW, Jang LL, Pan HJ, Chen YR, Chen CC, Lee CH, J. Nanobiotechnol., 14, 9 (2016)

[26] Fritz M, Radmacher M, Gaub HE, Biophys. J., 66, 1328 (1994)

[27] Bowen WR, Hilal N, Lovitt RW, Wright CJ, J. Membr. Sci., 154(2), 205 (1999)

[28] Girasole M, Pompeo G, Cricenti A, Congiu-Castellano A, Andreola F, Serafino A, Frazer BH, Boumis G, Amiconi G, BBA Biomembranes, 1768, 1268 (2007)

[29] Hartwig JH, J. Cell Biol., 118, 1421 (1992)

[30] Koseoglu S, Peters CG, Fitch-Tewfik JL, Aisiku O, Danglot L, Galli T, Flaumenhaft R, Blood, 126, 651 (2015)

[31] Peters CG, Michelson AD, Flaumenhaft R, Blood, 120, 199 (2012)

[32] Sakurai Y, Fitch-Tewfik JL, Qiu Y, Ahn B, Myers DR, Tran R, Fay ME, Ding L, Spearman PW, Michelson AD, Blood, 531 (2015).

[33] White JG, Blood, 69, 878 (1987)

[34] Jang Y, Lee M, Kim H, Cha C, Jung J, Oh J, Biofabrication, 11, 035021 (2019)

[35] Franco AT, Corken A, Ware J, Blood, 126, 582 (2015)

[36] Yan M, Jurasz P, BBA Mol. Cell Res., 1863, 392 (2016)

[37] Corum LE, Eichinger CD, Hsiao TW, Hlady V, Langmuir, 27(13), 8316 (2011)

[38] Fatisson J, Mansouri S, Yacoub D, Merhi Y, Tabrizian M, J. R. Soc. Interface, 8, 988 (2011)

[39] Kunze A, Hesse C, Svedhem S, Colloids Surf. B: Biointerfaces, 116, 446 (2014)

[40] Jacquemet G, Hamidi H, Ivaska J, Curr. Opin. Cell Biol., 36, 23 (2015)

[41] Park JY, Gemmell CH, Davies JE, Biomaterials, 22, 2671 (2001)

[42] Xu LC, Runt J, Siedlecki CA, Acta Biomater.., 6, 1938 (2010)

[43] Godo MN, Sefton MV, Biomaterials, 20, 1117 (1999)