화학공학소재연구정보센터
홈 로그인 로그아웃 연락처 사이트맵
Journal of Industrial and Engineering Chemistry, Vol.92, 226-235, December, 2020
DOI10.1016/j.jiec.2020.09.009  Export Citation
Increased neuritogenesis on ternary nanofiber matrices of PLCL and laminin decorated with black phosphorus
Moon Sung Kang, Su-Jin Song, Ji Hyeon Cha1, Yeonoh Cho1, Hyun Uk Lee2, Suong-Hyu Hyon3, Jong Hun Lee1, †, and Dong-Wook Han†
  • Department of Cogno-Mechatronics Engineering, College of Nanoscience & Nanotechnology, Pusan National University, Busan 46241, South Korea
  • 1Department of Food Science and Biotechnology, Gachon University, Seongnam 13120, South Korea
  • 2Division of Material Analysis and Research, Korea Basic Science Institute, Daejeon 34133, South Korea
  • 3The Joint Graduate School of Veterinary Medicine, Kagoshima University, Kagoshima 890-8580, Japan
E-mail:,
Recently, the composites of varying biomaterials and two-dimensional (2D) nanomaterials have been increasingly developed in the field of tissue engineering and regeneration owing to their excellent physicochemical and mechanical properties. In particular, the combination of biocompatible polymers and 2D nanomaterials can endow the nanocomposite with novel biofunctional properties while maintaining the inherent character of every single material. These nanocomposites are known to have the potential for improvement of cellular behaviors such as cell adhesion, proliferation, and differentiation. In this study, poly(l-lactide-co-e-caprolactone) (PLCL) and laminin (Lam) nanofibers functionalized with black phosphorus (BP) were successfully fabricated to increase the neuritogenesis of HT22 hippocampal neuronal cells using an electrospinning process. The ternary nanofiber matrices of PLCL/Lam/BP were found to be suitable for supporting the attachment and proliferation of hippocampal neurons. Furthermore, these PLCL/Lam/BP nanofiber matrices could not only promote neurite outgrowth and alignment but also increase the neuritogenesis of hippocampal neurons by providing optimal microenvironments for neuronal differentiation. The underlying mechanism of this phenomenon was confirmed by determining the expression levels of genes related to neurogenesis. In conclusion, these results suggest that BP-functionalized composite nanofibers could be a promising candidate as a scaffold for neural tissue engineering and regeneration.
Keywords:Two-dimensional nanomaterials;Nanofiber matrices;Laminin;Black phosphorus;Neural tissue engineering
  1. Klebanoff SG, Singer JL, Wilensky H, Psychol. Bull., 51, 1 (1954)
  2. Hazari A, Wiberg M, Johansson-Ruden G, Green C, Terenghi G, Br. J. Plast. Surg., 52, 653 (1999)
  3. Mackinnon SE, Doolabh VB, Novak CE, Trulock EP, Plast. Reconstr. Surg., 107, 1419 (2001)
  4. Coombs CJ, Ek EW, Wu T, Cleland H, Leung MK, J. Plast. Reconstr. Aesthet. Surg., 62, 1580 (2009)
  5. Jia H, Wang Y, Tong X, Liu G, Li Q, Zhang L, Sun X, Synapse, 66, 256 (2012)
  6. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Ramakrishna S, Biomaterials, 29, 4532 (2008)
  7. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Ramakrishna S, Tissue Eng. A, 15, 3605 (2009)
  8. Hong SW, Lee JH, Kang SH, Hwang EY, Hwang YS, Lee MH, Han DW, Park JC, Biomed. Res. Int., 2014, 212149 (2014)
  9. Lee EJ, Lee JH, Shin YC, Hwang DG, Kim JS, Jin OS, Jin L, Hong SW, Han DW, Biomater. Res., 18, 18 (2014)
  10. Gajendiran M, Choi JH, Kim SJ, Kim KS, Shin HS, Koo HJ, Kim KB, J. Ind. Eng. Chem., 51, 12 (2017)
  11. Meng Z, Wang Y, Ma C, Zheng W, Li L, Zheng Y, Mater. Sci. Eng. C-Biomimetic Supramol. Syst., 30, 1204 (2010)
  12. Heo EY, Ko NR, Bae MS, Lee SJ, Choi BJ, Kim JH, Kim HK, Park SA, Kwon IK, J. Ind. Eng. Chem., 45, 61 (2017)
  13. Patel M, Hong HJ, Koh WG, J. Ind. Eng. Chem., 80, 729 (2019)
  14. Wang C, Huang W, Zhou Y, He L, He Z, Chen Z, He X, Tian S, Liao J, Lu B, Wei Y, Wang M, Bioact. Mater., 5, 82 (2020)
  15. Moghaddam MM, Bonakdar S, Shariatpanahi MR, Shokrgozar MA, Faghihi S, Curr. Stem Cell Res. Ther., 14, 268 (2019)
  16. Roach P, Parker T, Gadegaard N, Alexander M, Surf. Sci. Rep., 65, 145 (2010)
  17. Shin YC, Lee JH, Kim MJ, Hong SW, Kim B, Hyun JK, Choi YS, Park JC, Han DW, J. Biol. Eng., 9, 22 (2015)
  18. Shin YC, Kim C, Song SJ, Jun S, Kim CS, Hong SW, Hyon SH, Han DW, Oh JW, Nanotheranostics, 2, 144 (2018)
  19. Joshi J, Brennan D, Beachley V, Kothapalli CR, J. Biomed. Mater. Res. A, 106, 3303 (2018)
  20. Prabhakaran MP, Venugopal JR, Ramakrishna S, Biomaterials, 30, 4996 (2009)
  21. Erisken C, Kalyon DM, Wang H, Biomaterials, 29, 4065 (2008)
  22. Shin YC, Lee JH, Jin L, Kim MJ, Kim YJ, Hyun JK, Jung TG, Hong SW, Han DW, J. Nanobiotechnol., 13, 21 (2015)
  23. Song SJ, Shin YC, Kim SE, Kwon IK, Lee JH, Hyon SH, Han DW, Kim B, Sci. Rep., 8, 5570 (2018)
  24. Yang F, Murugan R, Wang S, Ramakrishna S, Biomaterials, 26, 2603 (2005)
  25. Sasaki M, Kato S, Kohno K, Martin GR, Yamada Y, Proc. Natl. Acad. Sci. USA, 84, 935 (1987)
  26. Zhu N, Li M, Guan Y, Schreyer D, Chen X, Biofabrication, 2, 045002 (2010)
  27. Neal RA, Tholpady SS, Foley PL, Swami N, Ogle RC, Botchwey EA, J. Biomed. Mater. Res. A, 100, 406 (2012)
  28. Li Y, Liu Z, Hou Y, Yang G, Fei X, Zhao H, Guo Y, Su C, Wang Z, Zhong H, Zhuang Z, Guo Z, ACS Appl. Mater. Interfaces, 9, 25098 (2017)
  29. Choi JR, Yong KW, Choi JY, Nilghaz A, Lin Y, Xu J, Lu X, Theranostics, 8, 1005 (2018)
  30. Qiu M, Ren WX, Jeong T, Won M, Park GY, Sang DK, Liu LP, Zhang H, Kim JS, Chem. Soc. Rev., 47, 5588 (2018)
  31. Qian Y, Yuan WE, Cheng Y, Yang Y, Qu X, Fan C, Nano Lett., 19, 8990 (2019)
  32. Shao J, Xie H, Huang H, Li Z, Sun Z, Xu Y, Xiao Q, Yu XF, Zhao Y, Zhang H, Wang H, Chu PK, Nat. Commun., 7, 12967 (2016)
  33. Kim YP, Lee GS, Kim JW, Kim MS, Ahn HS, Lim JY, Kim HW, Son YJ, Knowles JC, Hyun JK, J. Tissue. Eng. Regen. Med., 9, 236 (2015)
  34. Wang Z, Zhao J, Tang W, Hu L, Chen X, Su Y, Zou C, Wang J, Lu WW, Zhen W, Zhang R, Yang D, Peng S, Small, 15, e19015 (2019)
  35. Lee HU, Park SY, Lee SC, Choi S, Seo S, Kim H, Won J, Choi K, Kang KS, Park HG, Small, 12, 214 (2016)
  36. Lee YB, Song SJ, Shin YC, Jung YJ, Kim B, Kang MS, Kwon IK, Hyon SH, Lee HU, Jung SH, Lim D, Han DW, J. Ind. Eng. Chem., 80C, 802 (2019)
  37. Song SJ, Raja IS, Lee YB, Kang MS, Seo HJ, Lee HU, Han DW, Biomater. Res., 23, 23 (2019)
  38. Kim MJ, Shin YC, Lee JH, Jun SW, Kim CS, Lee Y, Park JC, Lee SH, Park KD, Han DW, Biomater. Res., 20, 2 (2016)
  39. Latiff NM, Teo WZ, Sofer Z, Fisher AC, Pumera M, Chem. Eur. J., 21, 13991 (2015)
  40. Song SJ, Shin YC, Lee HU, KimB, Han DW, Lim D, Nanomaterials, 8, 408 (2018)
  41. Latiff NM, Mayorga-Martinez CC, Sofer Z, Fisher AC, Pumera M, Appl. Mater. Today, 13, 310 (2018)
  42. Ferrari M, Cirisano F, Moran MC, Colloids Interfaces, 3, 48 (2019)
  43. Gupta KK, Pal N, Mishra PK, Srivastava P, Mohanty S, Maiti P, J. Biomed. Mater. Res. A, 102, 2600 (2014)
  44. Jeong SJ, Jun ID, Choi MJ, Nho YC, Lee YM, Shin H, Macromol. Biosci., 8, 627 (2008)
  45. Huang SH, Hsu TT, Huang TH, Lin CY, Shie MY, J. Dent. Sci., 12, 33 (2017)
  46. Chimene D, Alge DL, Gaharwar AK, Adv. Mater., 27(45), 7261 (2015)
  47. Akhavan O, Ghaderi E, Abouei E, Hatamie S, Ghasemi E, Carbon, 66, 395 (2014)
  48. Lee JU, Kim M, Cheong H, Appl. Microscopy, 45, 126 (2015)
  49. Ma K, Chan CK, Liao S, Hwang WY, Feng Q, Ramakrishna S, Biomaterials, 29, 2096 (2008)
  50. Roussanne MC, Lieberherr M, Souberbielle J, Sarfati E, Drueke T, Bourdeau A, Eur. J. Clin. Invest., 31, 610 (2001)
  51. Zhang X, Zhang Z, Zhang S, Li D, Ma W, Ma C, Wu F, Zhao Q, Yan Q, Xing B, Small, 13, 170121 (2017)
  52. Lander AD, Fujii DK, Reichardt LF, Proc. Natl. Acad. Sci. USA, 82, 2183 (1985)
  53. Edgar D, Timpl R, Thoenen H, Embo J., 3, 1463 (1984)
  54. Hantaz-Ambroise D, Vigny M, Koenig J, J. Neurosci. Res., 7, 2293 (1987)
  55. He L, Tang S, Prabhakaran MP, Liao S, Tian L, Zhang Y, Xue W, Ramakrishna S, Macromol. Biosci., 13, 1601 (2013)
  56. Zander NE, Beebe TP, Biointerphases, 9, 011003 (2014)
  57. Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, Yamaguchi M, Kempermann G, J. Comp. Neurol., 467, 455 (2003)
  58. Toda T, Parylak SL, Linker SB, Gage FH, Mol. Psychiatry, 24, 67 (2019)
  59. Maxeiner S, Glassmann A, Kao HT, Schilling K, Histochem. Cell Biol., 141, 43 (2014)
  60. Wang HY, Hsieh PF, Huang DF, Chin PS, Chou CH, Tung CC, Chen SY, Lee LJ, Gau SSF, Huang HS, Sci. Rep., 5, 1 (2015)
  61. Ayanlaja AA, Xiong Y, Gao Y, Ji G, Tang C, Abdullah ZA, Gao D, Front. Mol. Neurosci., 10, 199 (2017)
  62. Caceres A, Mautino J, Kosik KS, Neuron, 9, 607 (1992)
  63. Dinsmore JH, Solomon F, Cell, 64, 817 (1991)
  64. Bernal A, Arranz L, Cell. Mol. Life Sci., 75, 2177 (2018)
  65. Zimatkin S, Karnyushko O, Neurosci. Behav. Physiol., 47, 122 (2017)
  66. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA, Proc. Natl. Acad. Sci. USA, 98, 4710 (2001)
  67. Clarke SR, Shetty AK, Bradley JL, Turner DA, Neuroreport, 5, 1885 (1994)
  68. Tao W, Ji X, Xu X, Islam MA, Li Z, Chen S, Saw PE, Zhang H, Bharwani Z, Guo Z, Angew. Chem.-Int. Edit., 129, 12058 (2017)
  69. Ji X, Kong N, Wang J, Li W, Xiao Y, Gan ST, Zhang Y, Li Y, Song X, Xiong Q, Adv. Mater., 30, 180303 (2018)
  70. Xing C, Chen S, Liang X, Liu Q, Qu M Zou Q, Li J, Tan H, Liu L, Fan D, Zhang H, ACS Appl. Mater. Interfaces, 10, 27631 (2018)
  71. Urbanova V, Pumera M, Nanoscale, 11, 15770 (2019)
  72. Wang S, Yang X, Zhou L, Li J, Chen H, J. Mater. Chem. B, 8, 2974 (2020)
  73. Luo M, Fan T, Zhou Y, Zhang H, Mei L, Adv. Funct. Mater., 29, 180830 (2019)
  74. Qiua M, Singh A, Wang D, Qua J, Swihartd M, Zhanga H, Prasad PN, NanoToday, 25, 135 (2019)
  75. Tatullo M, Genovese F, Aiello E, Amantea M, Makeeva I, Zavan B, Rengo S, Fortunato L, Materials, 12, 2301 (2019)
  76. Qu GB, Xia T, Zhou WH, Zhang X, Zhang HY, Hu LG, Shi JB, Yu XF, Jiang GB, Chem. Rev., 120(4), 2288 (2020)
  77. Xie Z, Fan T, An J, Choi W, Duo Y, Ge Y, Zhang B, Nie G, Xie N, Zheng T, Chen Y, Zhang H, Kim JS, Chem. Soc. Rev. (2020).
  78. Fan T, Zhou Y, Qiu M, Zhang H, J. Innov. Opt. Health Sci., 11, 183000 (2018)
  79. Balog R, Jorgensen B, Nilsson L, Andersen M, Rienks E, Bianchi M, Fanetti M, Laegsgaard E, Baraldi A, Lizzit S, Sljivancanin Z, Besenbacher F, Hammer B, Pedersen TG, Hofmann P, Hornekaer L, Nat. Mater., 9(4), 315 (2010)
  80. Liu B, Chen L, Liu G, Abbas AN, Fathi M, Zhou C, ACS Nano, 8, 5304 (2014)
  81. Chen W, ouyang J, Liu H, Chen M, Zeng K, Sheng J, Lu Z, Han Y, Wang L, Li J, Deng L, Liu YN, Guo S, Adv. Mater., 29, 160386 (2017)
  82. Guo T, Wu Y, Lin Y, Xu X, Lian H, Huang G, Liu JZ, Wu X, Yang HH, Small, 14, 170281 (2018)
  83. Al Barqouni LN, Skaik SI, Shaban NRA, Barqouni N, Lancet, 376, 68 (2010)
  84. Kamyar N, Greenhalgh RD, Nascimento TR, Medeiros ES, Matthews PD, Nogueira LP, Haugen HJ, Lewis DJ, Blaker JJ, ACS Appl. Nano Mater., 1, 4190 (2018)
  85. Cheng L, Cai Z, Zhao J, Wang F, Lu M, Deng L, Ciu W, Bioact. Mater., 5, 1026 (2020)
  86. Wang X, Shao J, Abd El Raouf M, Xie H, Huang H, Wang H, Chu PK, Yu XF, Yang Y, AbdEl-Aal AM, Biomaterials, 179, 164 (2018)
  87. Chen W, OInnouyang J, Yi X, Xu Y, Niu C, Zhang W, Wang L, Sheng J, Deng L, Liu YN, Adv. Mater., 30, 170345 (2018)
  88. Vaudry D, Stork P, Lazarovici P, Eiden L, Science, 296, 1648 (2002)