Migration Behavior of Bio-materials in Ice Grain Boundary Channels

  • Arinori InagawaEmail author
Part of the Springer Theses book series (Springer Theses)


In this chapter, the migration behavior of bio-materials in ice grain boundaries is explored to demonstrate the applicability of the concept proposed in Chap.  2 to bio-separation. Yeast cells and T4 GT7 giant DNA samples were employed. The size-tunability of the ice grain boundary channel (Inagawa et al. in Sci Rep 5:17308 [1], Inagawa et al. in Talanta 183:345–351 [2]) allows the migration control of yeast cells. On the other hand, for DNA, the difference in the migration behavior of the random-coil and globule states was investigated. This difference in state affects the contour flexibility of the DNA, resulting in different threshold temperatures at which the DNA molecules begin to migrate. Ice grain boundary electrophoresis was also applied to the detection of the chemical interactions between the biomolecules and ice crystals. AFPs were anchored on 1 μm PS particles, and their migration behavior in the grooves on the surface ice was studied. The threshold temperature at which the particles begin to migrate is an effective criterion for the evaluation of the chemical interactions between the particles and ice walls. The threshold temperature was lowered by 2.5 °C when the AFPs were bound onto the particles, indicating the presence of interactions between the bound AFPs and the ice wall. Because the AFPs studied in this work exhibit selectivity towards the prism plane of the ice crystal, it is critical that the prism plane of the ice crystal should be in contact with the FCS in the surface grooves.


Bio-separation Yeast cells DNA Antifreeze proteins State analysis 


  1. 1.
    Inagawa A, Harada M, Okada T (2015) Fluidic grooves on doped-ice surface as size-tunable channels. Sci Rep 5:17308PubMedPubMedCentralGoogle Scholar
  2. 2.
    Inagawa A, Okada Y, Okada T (2017) Electrophoresis in ice surface grooves for probing protein affinity to a specific plane of ice crystal. Talanta 2018(183):345–351Google Scholar
  3. 3.
    Shen Z, Wu A, Chen X (2017) Current detection technologies for circulating tumor cells. Chem Soc Rev 46(8):2038–2056PubMedPubMedCentralGoogle Scholar
  4. 4.
    Lawrenz B, Schiller H, Willbold E, Ruediger M, Muhs A, Esser S (2004) Highly sensitive biosafety model for stem-cell-derived grafts. Cytotherapy 6(3):212–222PubMedGoogle Scholar
  5. 5.
    Diogo MM, da Silva CL, Cabral JMS (2012) Separation technologies for stem cell bioprocessing. Biotechnol Bioeng 109(11):2699–2709PubMedGoogle Scholar
  6. 6.
    Da Silva CL, Gonçalves R, Porada CD, Ascensão JL, Zanjani ED, Cabral JMS, Almeida-Porada G (2009) Differences amid bone marrow and cord blood hematopoietic stem/progenitor cell division kinetics. J Cell Physiol 220(1):102–111PubMedGoogle Scholar
  7. 7.
    Andrade PZ, Lobato Da Silva C, Dos Santos F, Almeida-Porada G, Cabral JMS (2011) Initial CD34+ cell-enrichment of cord blood determines hematopoietic stem/progenitor cell yield upon ex vivo expansion. J Cell Biochem 112(7):1822–1831PubMedGoogle Scholar
  8. 8.
    Lennon DP, Caplan AI (2006) Isolation of rat marrow-derived mesenchymal stem cells. Exp Hematol 34(11):1606–1607PubMedGoogle Scholar
  9. 9.
    Huang LR, Cox EC, Austin RH, Sturm JC (2004) Continuous particle separation through deterministic lateral displacement. Science 304(5673):987–990PubMedGoogle Scholar
  10. 10.
    Davis JA, Inglis DW, Morton KJ, Lawrence DA, Huang LR, Chou SY, Sturm JC, Austin RH (2006) Deterministic hydrodynamics: taking blood apart. Proc Natl Acad Sci 103(40):14779–14784PubMedGoogle Scholar
  11. 11.
    Yamada M, Nakashima M, Seki M (2004) Pinched flow fractionation: continuous size separation of particles utilizing a laminar flow profile in a pinched microchannel. Anal Chem 76(18):5465–5471PubMedGoogle Scholar
  12. 12.
    Takagi J, Yamada M, Yasuda M, Seki M (2005) Continuous particle separation in a microchannel having asymmetrically arranged multiple branches. Lab Chip 5(7):778PubMedGoogle Scholar
  13. 13.
    Yamada M, Seki M (2005) Hydrodynamic filtration for on-chip particle concentration and classification utilizing microfluidics. Lab Chip 5(11):1233PubMedGoogle Scholar
  14. 14.
    Yamada M, Seki M (2006) Microfluidic particle sorter employing flow splitting and recombining. Anal Chem 78(4):1357–1362PubMedGoogle Scholar
  15. 15.
    Yamada M, Kano K, Tsuda Y, Kobayashi J, Yamato M, Seki M, Okano T (2007) Microfluidic devices for size-dependent separation of liver cells. Biomed Microdevices 9(5):637–645PubMedGoogle Scholar
  16. 16.
    Mizuno M, Yamada M, Mitamura R, Ike K, Toyama K, Seki M (2013) Magnetophoresis-integrated hydrodynamic filtration system for size-and surface marker-based two-dimensional cell sorting. Anal Chem 85(16):7666–7673PubMedGoogle Scholar
  17. 17.
    Hur SC, Brinckerhoff TZ, Walthers CM, Dunn JCY, Di Carlo D (2012) Label-free enrichment of adrenal cortical progenitor cells using inertial microfluidics. PLoS One 7(10):e46550PubMedPubMedCentralGoogle Scholar
  18. 18.
    Labeed FH, Lu J, Mulhall HJ, Marchenko SA, Hoettges KF, Estrada LC, Lee AP, Hughes MP, Flanagan LA (2011) Biophysical characteristics reveal neural stem cell differentiation potential. PLoS ONE 6(9):1–11Google Scholar
  19. 19.
    Flanagan LA, Lu J, Wang L, Marchenko SA, Jeon NL, Lee AP, Monuki ES (2008) Unique dielectric properties distinguish stem cells and their differentiated progeny. Stem Cells 26(3):656–665PubMedGoogle Scholar
  20. 20.
    Shibata H, Ageyama N, Tanaka Y, Kishi Y, Sasaki K, Nakamura S, Muramatsu S, Hayashi S, Kitano Y, Terao K et al (2006) Improved safety of hematopoietic transplantation with monkey embryonic stem cells in the allogeneic setting. Stem Cells 24(6):1450–1457PubMedGoogle Scholar
  21. 21.
    Fong CY, Peh GSL, Gauthaman K, Bongso A (2009) Separation of SSEA-4 and TRA-1-60 labelled undifferentiated human embryonic stem cells from a heterogeneous cell population using magnetic-activated cell sorting (MACS) and fluorescence-activated cell sorting (FACS). Stem Cell Rev Rep 5(1):72–80Google Scholar
  22. 22.
    Umemoto T, Yamato M, Nishida K, Yang J, Tano Y, Okano T (2006) Limbal epithelial side-population cells have stem cell-like properties, including quiescent state. Stem Cells 24(1):86–94PubMedGoogle Scholar
  23. 23.
    Tateno C, Takai-Kajihara K, Yamasaki C, Sato H, Yoshizato K (2000) Heterogeneity of growth potential of adult rat hepatocytesin vitro. Hepatology 31(1):65–74PubMedGoogle Scholar
  24. 24.
    Lindahl PE (1948) Principle of a counter-streaming centrifuge for the separation of particles of different sizes. Nature 161:648–649PubMedGoogle Scholar
  25. 25.
    Schwartz DC, Cantor CR (1984) Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 37(1):67–75PubMedGoogle Scholar
  26. 26.
    Carle GF, Olson MV (1984) Nucleic acids research nucleic acids research. Nucl Acids Res 12(14):5647–5664PubMedGoogle Scholar
  27. 27.
    Volkmuth WD, Austin RH (1992) DNA electrophoresis in microlithographic arrays. Nature 358(6387):600–602PubMedGoogle Scholar
  28. 28.
    Fu J, Schoch RB, Stevens AL, Tannenbaum SR, Han J (2007) A patterned anisotropic nanofluidic sieving structure for continuous-flow separation of DNA and proteins. Nat nanotechnol 2(2):121–128PubMedPubMedCentralGoogle Scholar
  29. 29.
    Striemer CC, Gaborski TR, McGrath JL, Fauchet PM (2007) Charge- and size-based separation of macromolecules using ultrathin silicon membranes. Nature 445(7129):749–753PubMedGoogle Scholar
  30. 30.
    Xu F, Baba Y (2004) Polymer solutions and entropic-based systems for double-stranded DNA capillary electrophoresis and microchip electrophoresis. Electrophoresis 25(14):2332–2345PubMedGoogle Scholar
  31. 31.
    Kaji N, Tezuka Y, Takamura Y, Ueda M, Nishimoto T, Nakanishi H, Horiike Y, Baba Y (2004) Separation of long DNA molecules by quartz nanopillar chips under a direct current electric field. Anal Chem 76(1):15–22PubMedGoogle Scholar
  32. 32.
    Kratky O, Porod G (1949) Roentgenuntersuchung Geloester Fadenmolekuele. Recl des Trav Chim des Pays-Bas 68(12):1106–1122Google Scholar
  33. 33.
    Tegenfeldt JO, Prinz C, Cao H, Chou S, Reisner WW, Riehn R, Wang YM, Cox EC, Sturm JC, Silberzan P et al (2004) The dynamics of genomic-length DNA molecules in 100-nm channels. Proc Natl Acad Sci 101(30):10979–10983PubMedGoogle Scholar
  34. 34.
    Lam ET, Hastie A, Lin C, Ehrlich D, Das SK, Austin MD, Deshpande P, Cao H, Nagarajan N, Xiao M et al (2012) Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nat Biotechnol 30(8):771–776PubMedGoogle Scholar
  35. 35.
    Manning GS (1978) ThHe molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys 11(2):179–246PubMedGoogle Scholar
  36. 36.
    Wilson RW, Bloomfield VA (1979) Counterion-induced condensation of deoxyribonucleic acid. A light-scattering study. Biochemistry 18(11):2192–2196PubMedGoogle Scholar
  37. 37.
    Schellman JA, Parthasarathy N (1984) X-ray diffraction studies on cation-collapsed DNA. J Mol Biol 175(3):313–329PubMedGoogle Scholar
  38. 38.
    Makita N, Yoshikawa K (2002) Proton concentration (PH) switches the higher-order structure of DNA in the presence of spermine. Biophys Chem 99(1):43–53PubMedGoogle Scholar
  39. 39.
    Inoshita S, Tsukahara S, Fujiwara T (2009) In situ fluorescence microscopic investigation into the dependence of conformation and electrophoretic velocity of single DNA molecules on acid or spermidine concentration. Anal Sci 25(2):293–299PubMedGoogle Scholar
  40. 40.
    Yoshikawa K, Matsuzawa Y (1995) Discrete phase transition of giant DNA dynamics of globule formation from a single molecular chain. Phys D Nonlinear Phenom 84(1–2):220–227Google Scholar
  41. 41.
    Tsukahara S, Suehara M, Fujiwara T (2008) In situ measurements of the dynamics of single giant DNA molecules at the toluene-trioctylamine/water interface by total internal reflection fluorescence microscopy. Langmuir 24(5):1673–1677PubMedGoogle Scholar
  42. 42.
    Kellenberger E (1987) The compactness of cellular plasmas; in particular, chromatin compactness in relation to function. Trends Biochem Sci 12(March):105–107Google Scholar
  43. 43.
    Reich Z, Ghirlando R, Minsky A (1991) Secondary conformational polymorphism of nucleic acids as a possible functional link between cellular parameters and dna packaging processes. Biochemistry 30(31):7828–7836PubMedGoogle Scholar
  44. 44.
    DeVries AL, Wohlschlag DE (1969) Freezing resistance in some antarctic fishes. Science 163(3871):1073–1075PubMedGoogle Scholar
  45. 45.
    Harding MM, Anderberg PI, Haymet ADJ (2003) “Antifreeze” glycoproteins from polar fish. Eur J Biochem 270(7):1381–1392PubMedGoogle Scholar
  46. 46.
    Harding MM, Ward LG, Haymet ADJ (1999) Type I ‘Antifreeze’ proteins structure ± activity studies and mechanisms of ice growth inhibition. Eur J Biochem 665:653–665Google Scholar
  47. 47.
    Ewart KV, Yang DSC, Ananthanarayanan VS, Fletcher GL, Hew CL (1996) Ca2+-dependent antifreeze proteins. Biochemistry 271(28):16627–16632Google Scholar
  48. 48.
    Gronwald W, Loewen MC, Lix B, Daugulis AJ, Sönnichsen FD, Davies PL, Sykes BD (1998) The solution structure of type II antifreeze protein reveals a new member of the lectin family. Biochemistry 37(14):4712–4721PubMedGoogle Scholar
  49. 49.
    Li Z, Lin Q, Yang DSC, Ewart KV, Hew CL (2004) The role of Ca2+-coordinating residues of herring antifreeze protein in antifreeze activity. Biochemistry 43(46):14547–14554PubMedGoogle Scholar
  50. 50.
    Jia Z, DeLuca CI, Chao H, Davies PL (1996) Structural basis for the binding of a globular antifreeze protein to ice. Nature 384(6606):285–288PubMedGoogle Scholar
  51. 51.
    Deng G, Laursen RA (1998) Isolation and characterization of an antifreeze protein from the longhorn sculpin, myoxocephalus octodecimspinosis. Biochim Biophys Acta 1388(2):305–314PubMedGoogle Scholar
  52. 52.
    Knight CA, Cheng CC, DeVries AL (1991) Adsorption of alpha-helical antifreeze peptides on specific ice crystal surface planes. Biophys J 59(2):409–418PubMedPubMedCentralGoogle Scholar
  53. 53.
    Cheng CC, DeVries AL (1991) Life under extreme conditions. Springer, Berlin, HeidelbergGoogle Scholar
  54. 54.
    Davies PL, Baardsnes J, Kuiper MJ, Walker VK (2002) Structure and function of antifreeze proteins. Philos Trans R Soc B Biol Sci 357(1423):927–935Google Scholar
  55. 55.
    Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci U S A 74(6):2589–2593PubMedPubMedCentralGoogle Scholar
  56. 56.
    Tasaki Y, Okada T (2006) Ice chromatography. Characterization of water-ice as a chromatographic stationary phase. Anal Chem 78(12):4155–4160PubMedGoogle Scholar
  57. 57.
    Sperling RA, Parak WJ (2010) Surface modification, functionalization and bioconjugation of colloidal inorganic nanoparticles. Philos Trans R Soc A Math Phys Eng Sci 368(1915):1333–1383Google Scholar
  58. 58.
    Kapuściński J, Skoczylas B (1977) Simple and rapid fluorimetric DNA microassay method for. Anal Biochem 83:252–257PubMedGoogle Scholar
  59. 59.
    Banerjee D, Pal SK (2008) Dynamics in the DNA recognition by DAPI: exploration of the various binding modes. J Phys Chem B 112(3):1016–1021PubMedGoogle Scholar
  60. 60.
    Righetti PG, Caravaggio T (1976) Isoelectric points and molecular weights of proteins: a table. J Chromatogr 127:1–28PubMedGoogle Scholar
  61. 61.
    Malamud D, Drysdale JW (1978) Isoelectric points of proteins: a table. Anal Biochem 86(2):620–647PubMedGoogle Scholar
  62. 62.
    Jia Z, Davies PL (2002) Antifreeze proteins: an unusual receptor-ligand interaction. Trends Biochem Sci 27(2):101–106PubMedGoogle Scholar
  63. 63.
    Nada H, Furukawa Y (2012) Antifreeze proteins: computer simulation studies on the mechanism of ice growth inhibition. Polym J 44:690–698Google Scholar
  64. 64.
    Olijve LLC, Meister K, DeVries AL, Duman JG, Guo S, Bakker HJ, Voets IK (2016) Blocking rapid ice crystal growth through nonbasal plane adsorption of antifreeze proteins. Proc Natl Acad Sci 113(14):3740–3745PubMedGoogle Scholar
  65. 65.
    Koo K, Ananth R, Gill WN (1991) The splitting in dendritic growth of ice crystals. Phys Rev A 44(6):3782–3790PubMedGoogle Scholar
  66. 66.
    Yokoyama E, Yoshizaki I, Shimaoka T, Sone T, Kiyota T, Furukawa Y (2011) Measurements of growth rates of an ice crystal from supercooled heavy water under microgravity conditions: basal face growth rate and tip velocity of a dendrite. J Phys Chem B 115(27):8739–8745PubMedGoogle Scholar
  67. 67.
    Nada H, Furukawa Y (2008) Growth inhibition mechanism of an ice-water interface by a mutant of winter flounder antifreeze protein: a molecular dynamics study. J Phys Chem B 112(23):7111–7119PubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Graduate School of Regional Development and CreativityUtsunomiya UniversityUtsunomiyaJapan

Personalised recommendations