Quantitative stain-free and continuous multimodal monitoring of wound healing in vitro with digital holographic microscopy

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Bettenworth, Dominik ^a   Lenz, Philipp ^a   Krausewitz, Philipp ^a   Brückner, Markus ^a   Ketelhut, Steffi ^b   Domagk, Dirk ^a   Kemper, Björn ^b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; EPIDERMAL GROWTH FACTOR; MITOMYCIN; NUCLEIC ACID SYNTHESIS INHIBITOR;

ARTICLE; CACO 2 CELL LINE; CELL DENSITY; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL STIMULATION; CELL STRUCTURE; CELL VOLUME; CONTROLLED STUDY; DIGITAL HOLOGRAPHIC MICROSCOPY; DRY MASS; HUMAN; HUMAN CELL; IN VITRO STUDY; MEASUREMENT ACCURACY; MICROSCOPY; MONITORING; QUANTITATIVE ANALYSIS; REFRACTION INDEX; TIME LAPSE IMAGING; WOUND HEALING; ALGORITHM; BIOLOGICAL MODEL; CELL MOTION; CELL SIZE; DEVICES; DRUG EFFECTS; HOLOGRAPHY; PHYSIOLOGY; PROCEDURES; REPRODUCIBILITY;

ALGORITHMS; CACO-2 CELLS; CELL MOVEMENT; CELL PROLIFERATION; CELL SIZE; EPIDERMAL GROWTH FACTOR; HOLOGRAPHY; HUMANS; MICROSCOPY; MITOMYCIN; MODELS, BIOLOGICAL; NUCLEIC ACID SYNTHESIS INHIBITORS; REPRODUCIBILITY OF RESULTS; WOUND HEALING;

EID: 84907462364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107317     Document Type: Article

References (66)

1. Jones MK, Tomikawa M, Mohajer B., Tarnawski AS (1999) Gastrointestinal mucosal regeneration: role of growth factors. Frontiers in bioscience: a journal and virtual library 4: D303-309.
2. Mertz HR, Walsh JH (1991) Peptic ulcer pathophysiology. Med Clin North Am 75: 799-814.
3. Pantelis D, Beissel A, Kahl P., Wehner S, Vilz TO, et al. (2010) The effect of sealing with a fixed combination of collagen matrix-bound coagulation factors on the healing of colonic anastomoses in experimental high-risk mice models. Langenbecks Arch Surg 395: 1039-1048.
4. Wu SC, Marston W, Armstrong DG (2010) Wound care: the role of advanced wound-healing technologies. J Am Podiatr Med Assoc 100: 385-394.
5. Bonfiglio V, Camillieri G, Avitabile T., Leggio GM, Drago F (2006) Effects of the COOH-terminal tripeptide alpha-MSH(11-13) on corneal epithelial wound healing: role of nitric oxide. Experimental eye research 83: 1366-1372.
6. Neurath MF, Wittkopf N, Wlodarski A., Waldner M, Neufert C, et al. (2010) Assessment of tumor development and wound healing using endoscopic techniques in mice. Gastroenterology 139: 1837-1843 e1831.
7. Burk RR (1973) A factor from a transformed cell line that affects cell migration. Proc Natl Acad Sci U S A 70: 369-372.
8. Singh A, Nascimento JM, Kowar S, Busch H., Boerries M (2012) Boolean approach to signalling pathway modelling in HGF-induced keratinocyte migration. Bioinformatics 28: i495-i501.
9. Msaki A, Sanchez AM, Koh L.F., Barre B., Rocha S, et al. (2011) The role of RelA (p65) threonine 505 phosphorylation in the regulation of cell growth, survival, and migration. Molecular biology of the cell 22: 3032-3040.
10. Zhao K, Wang W, Guan C., Cai J, Wang P (2012) Inhibition of gap junction channel attenuates the migration of breast cancer cells. Molecular biology reports 39: 2607-2613.
11. Sakalar C, Yuruk M, Kaya T., Aytekin M, Kuk S, et al. (2013) Pronounced transcriptional regulation of apoptotic and TNF-NF-kappa-B signaling genes during the course of thymoquinone mediated apoptosis in HeLa cells. Molecular and cellular biochemistry 10.1007/s11010-013-1772-x.
12. Wang Z, Tangella K, Balla A., Popescu G (2011) Tissue refractive index as marker of disease. J Biomed Opt 16: 116017.
13. Liang CC, Park AY, Guan JL (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2: 329-333.
14. Lamprecht MR, Sabatini DM, Carpenter AE (2007) CellProfiler: free, versatile software for automated biological image analysis. BioTechniques 42: 71-75.
15. Keese CR, Wegener J, Walker S.R., Giaever I (2004) Electrical wound-healing assay for cells in vitro. Proc Natl Acad Sci U S A 101: 1554-1559.
16. Kemper B, Carl D, Schnekenburger J., Bredebusch I, Schafer M, et al. (2006) Investigation of living pancreas tumor cells by digital holographic microscopy. Journal of biomedical optics 11: 34005.
17. Mann CJ, Yu L, Lo C-M, Kim MK (2005) High-resolution quantitative phase-contrast microscopy by digital holography. Opt Express 13: 8693-8698.
18. Marquet P, Rappaz B, Magistretti P.J., Cuche E., Emery Y, et al. (2005) Digital Holographic Microscopy: A Noninvasive Contrast Imaging Technique Allowing Quantitative Visualization of Living Cells with Subwavelength Axial Accuracy. Opt Lett 30: 468-470.
19. Klokkers J, Langehanenberg P, Kemper B., Kosmeier S, von Bally G, et al. (2009) Atrial natriuretic peptide and nitric oxide signaling antagonizes vasopressin-mediated water permeability in inner medullary collecting duct cells. Am J Physiol Renal Physiol 297: F693-703.
20. Jourdain P, Pavillon N, Moratal C., Boss D, Rappaz B, et al. (2011) Determination of transmembrane water fluxes in neurons elicited by glutamate ionotropic receptors and by the cotransporters KCC2 and NKCC1: a digital holographic microscopy study. J Neurosci 31: 11846-11854.
21. Bauwens A, Bielaszewska M, Kemper B., Langehanenberg P, von Bally G, et al. (2011) Differential cytotoxic actions of Shiga toxin 1 and Shiga toxin 2 on microvascular and macrovascular endothelial cells. Thrombosis and haemostasis 105: 515-528.
22. Pavillon N, Kuhn J, Moratal C., Jourdain P, Depeursinge C, et al. (2012) Early cell death detection with digital holographic microscopy. PloS one 7: e30912.
23. Kühn J, Shaffer E, Mena J., Breton B, Parent J, et al. (2012) Label-Free Cytotoxicity Screening Assay by Digital Holographic Microscopy. Assay and drug development technologies.
24. Wang Y, Yang Y, Wang D., Ouyang L, Zhang Y, et al. (2013) Morphological measurement of living cells in methanol with digital holographic microscopy. Computational and mathematical methods in medicine 2013: 715843.
25. Ekpenyong AE, Man SM, Achouri S, Bryant C.E., Guck J., et al. (2012) Bacterial infection of macrophages induces decrease in refractive index. Journal of Biophotonics 10.1002/jbio.201200113: n/a-n/a.
26. Park Y, Diez-Silva M, Popescu G., Lykotrafitis G, Choi W, et al. (2008) Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum. Proc Natl Acad Sci U S A 105: 13730-13735.
27. Simon B, Debailleul M, Beghin A., Tourneur Y, Haeberle O (2010) Highresolution tomographic diffractive microscopy of biological samples. Journal of Biophotonics 3: 462-467.
28. Lenz P, Bettenworth D, Krausewitz P., Bruckner M, Ketelhut S, et al. (2013) Digital holographic microscopy quantifies the degree of inflammation in experimental colitis. Integrative biology: quantitative biosciences from nano to macro 5: 624-630.
29. Rappaz B, Cano E, Colomb T., Kühn J, Depeursinge C., et al. (2009) Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy. Journal of biomedical optics 14: 034049-034049-034045.
30. Mir M, Wang Z, Shen Z., Bednarz M, Bashir R, et al. (2011) Optical measurement of cycle-dependent cell growth. Proceedings of the National Academy of Sciences 108: 13124-13129.
31. Curl CL, Harris T, Harris P.J., Allman BE, Bellair CJ, et al. (2004) Quantitative phase microscopy: a new tool for measurement of cell culture growth and confluency in situ. Pflügers Archiv European Journal of Physiology 448: 462-468.
32. Greve B, Sheikh-Mounessi F, Kemper B., Ernst I, Gotte M, et al. (2012) Survivin, a target to modulate the radiosensitivity of Ewing's sarcoma. Strahlentherapie und Onkologie: Organ der Deutschen Rontgengesellschaft [et al] 188: 1038-1047.
33. Coffey RJ, Romano M, Goldenring J (1995) Roles for transforming growth factor-alpha in the stomach. Journal of clinical gastroenterology 21 Suppl 1: S36-39.
34. Perdikis DA, Davies R, Zhuravkov A., Brenner B, Etter L, et al. (1998) Differential effects of mucosal pH on human (Caco-2) intestinal epithelial cell motility, proliferation, and differentiation. Dig Dis Sci 43: 1537-1546.
35. Kemper B, Bauwens A, Vollmer A., Ketelhut S, Langehanenberg P, et al. (2010) Label-free quantitative cell division monitoring of endothelial cells by digital holographic microscopy. J Biomed Opt 15: 036009.
36. Ross DW (1981) The nature of unbalanced cell growth caused by cytotoxic agents. Virchows Archiv B, Cell pathology including molecular pathology 37: 225-235.
37. Leoni G, Alam A, Neumann P.A., Lambeth JD, Cheng G, et al. (2013) Annexin A1, formyl peptide receptor, and NOX1 orchestrate epithelial repair. The Journal of clinical investigation 123: 443-454.
38. Brem H, Tomic-Canic M (2007) Cellular and molecular basis of wound healing in diabetes. The Journal of clinical investigation 117: 1219-1222.
39. Ciacci C, Lind SE, Podolsky DK (1993) Transforming growth factor beta regulation of migration in wounded rat intestinal epithelial monolayers. Gastroenterology 105: 93-101.
40. Dignass A, Lynch-Devaney K, Kindon H., Thim L, Podolsky DK (1994) Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway. The Journal of clinical investigation 94: 376-383.
41. Karrasch T, Spaeth T, Allard B., Jobin C (2011) PI3K-dependent GSK3ss(Ser9)-phosphorylation is implicated in the intestinal epithelial cell wound-healing response. PloS one 6: e26340.
42. Karrasch T, Steinbrecher KA, Allard B, Baldwin A.S., Jobin C (2006) Wound-induced p38MAPK-dependent histone H3 phosphorylation correlates with increased COX-2 expression in enterocytes. Journal of cellular physiology 207: 809-815.
43. Maltseva I, Chan M, Kalus I., Dierks T, Rosen SD (2013) The SULFs, Extracellular Sulfatases for Heparan Sulfate, Promote the Migration of Corneal Epithelial Cells during Wound Repair. PloS one 8: e69642.
44. Blais A, Bissonnette P, Berteloot A (1987) Common characteristics for Na+-dependent sugar transport in Caco-2 cells and human fetal colon. The Journal of membrane biology 99: 113-125.
45. Crissman HA, Steinkamp JA (1973) Rapid, simultaneous measurement of DNA, protein, and cell volume in single cells from large mammalian cell populations. The Journal of cell biology 59: 766-771.
46. Jumarie C, Malo C (1991) Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro. Journal of cellular physiology 149: 24-33.
47. Mir M, Wang Z, Shen Z., Bednarz M, Bashir R, et al. (2011) Optical measurement of cycle-dependent cell growth. Proc Natl Acad Sci U S A 108: 13124-13129.
48. Bishop WP, Wen JT (1994) Regulation of Caco-2 cell proliferation by basolateral membrane epidermal growth factor receptors. The American journal of physiology 267: G892-900.
49. Popescu G, Park Y, Lue N., Best-Popescu C, Deflores L, et al. (2008) Optical imaging of cell mass and growth dynamics. American journal of physiology Cell physiology 295: C538-544.
50. Przibilla S, Dartmann S, Vollmer A., Ketelhut S, Greve B, et al. (2012) Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes. Journal of biomedical optics 17: 97001-97001.
51. Basson MD, Coppola CP (2002) Repetitive deformation and pressure activate small bowel and colonic mucosal tyrosine kinase activity in vivo. Metabolism: clinical and experimental 51: 1525-1527.
52. Walsh MF, Woo RK, Gomez R, Basson MD (2004) Extracellular pressure stimulates colon cancer cell proliferation via a mechanism requiring PKC and tyrosine kinase signals. Cell proliferation 37: 427-441.
53. Flanigan TL, Owen CR, Gayer C, Basson MD (2008) Supraphysiologic extracellular pressure inhibits intestinal epithelial wound healing independently of luminal nutrient flow. American journal of surgery 196: 683-689.
54. Lloyd AC (2013) The regulation of cell size. Cell 154: 1194-1205.
55. Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiological reviews 89: 193-277.
56. Jessica Chen M, Sepramaniam S, Armugam A., Shyan Choy M, Manikandan J, et al. (2008) Water and ion channels: crucial in the initiation and progression of apoptosis in central nervous system? Current neuropharmacology 6: 102-116.
57. Kuhn J, Shaffer E, Mena J., Breton B, Parent J, et al. (2013) Label-free cytotoxicity screening assay by digital holographic microscopy. Assay and drug development technologies 11: 101-107.
58. Lee K, Kim K, Jung J., Heo J, Cho S, et al. (2013) Quantitative phase imaging techniques for the study of cell pathophysiology: from principles to applications. Sensors 13: 4170-4191.
59. Rappaz B, Cano E, Colomb T., Kuhn J, Depeursinge C, et al. (2009) Noninvasive characterization of the fission yeast cell cycle by monitoring dry mass with digital holographic microscopy. J Biomed Opt 14: 034049.
60. Shih YT, Wang MC, Peng H.H., Chen TF, Chen L, et al. (2012) Modulation of chemotactic and pro-inflammatory activities of endothelial progenitor cells by hepatocellular carcinoma. Cellular signalling 24: 779-793.
61. Cross HS, Quaroni A (1991) Inhibition of sucrose-isomaltase expression by EGF in the human colon adenocarcinoma cells Caco-2. The American journal of physiology 261: C1173-1183.
62. Carl D, Kemper B, Wernicke G., von Bally G (2004) Parameter-optimized digital holographic microscope for high-resolution living-cell analysis. Applied optics 43: 6536-6544.
63. Langehanenberg P, Kemper B, Dirksen D., von Bally G (2008) Autofocusing in digital holographic phase contrast microscopy on pure phase objects for live cell imaging. Appl Opt 47: D176-D182.
64. Barer R (1952) Interference microscopy and mass determination. Nature 169: 366-367.
65. Kemper B, Kosmeier S, Langehanenberg P., von Bally G, Bredebusch I, et al. (2007) Integral refractive index determination of living suspension cells by multifocus digital holographic phase contrast microscopy. Journal of biomedical optics 12: 054009.
66. Carpenter AE, Jones TR, Lamprecht M.R., Clarke C., Kang IH, et al. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome biology 7: R100.