Multicolor Cell Barcoding Technology for Long-Term Surveillance of Epithelial Regeneration in Zebrafish

Developmental Cell

Volumn 36, Issue 6, 2016, Pages 668-680

  Chen, Chen Hui ^a   Puliafito, Alberto ^b   Cox, Ben D ^a   Primo, Luca ^b,c   Fang, Yi ^a   Di Talia, Stefano ^a   Poss, Kenneth D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b CANDIOLO CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL GROWTH; CELL POPULATION; CELL REGENERATION; CELL TRACKING; EPITHELIUM CELL; HOMEOSTASIS; IMAGE ANALYSIS; IN VIVO STUDY; NONHUMAN; PERIODICITY; PRIORITY JOURNAL; SKIN APPENDAGE; SKIN EPITHELIUM; STEM CELL; SUPERFICIAL EPITHELIUM CELL; TRANSGENIC ZEBRAFISH; ANIMAL; ANIMAL MODEL; DNA BARCODING; EPITHELIUM; FIN (ORGAN); GENETICS; INJURIES; METABOLISM; PHYSIOLOGY; PROCEDURES; REGENERATION; SKIN; SKIN PIGMENTATION; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMAL FINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DNA BARCODING, TAXONOMIC; EPITHELIAL CELLS; EPITHELIUM; HOMEOSTASIS; MODELS, ANIMAL; REACTIVE OXYGEN SPECIES; REGENERATION; SKIN; SKIN PIGMENTATION; ZEBRAFISH;

EID: 84961242602     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.02.017     Document Type: Article

References (51)

1. Bailey T.C., Gatrell A.C. Interactive Spatial Data Analysis 1995, Longman Scientific & Technical.
2. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P.J., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
3. Bilan D.S., Pase L., Joosen L., Gorokhovatsky A.Y., Ermakova Y.G., Gadella T.W., Grabher C., Schultz C., Lukyanov S., Belousov V.V. HyPer-3: a genetically encoded H(2)O(2) probe with improved performance for ratiometric and fluorescence lifetime imaging. ACS Chem. Biol. 2013, 8:535-542.
4. Blanpain C., Fuchs E. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 2009, 10:207-217.
5. Blanpain C., Fuchs E. Stem cell plasticity. Plasticity of epithelial stem cells in tissue regeneration. Science 2014, 344:1242281.
6. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell 2013, 154:274-284.
7. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
8. Donati G., Watt F.M. Stem cell heterogeneity and plasticity in epithelia. Cell Stem Cell 2015, 16:465-476.
9. Doupe D.P., Alcolea M.P., Roshan A., Zhang G., Klein A.M., Simons B.D., Jones P.H. A single progenitor population switches behavior to maintain and repair esophageal epithelium. Science 2012, 337:1091-1093.
10. Eisenhoffer G.T., Loftus P.D., Yoshigi M., Otsuna H., Chien C.B., Morcos P.A., Rosenblatt J. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 2012, 484:546-549.
11. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35:495-516.
12. Frangi A., Niessen W., Vincken K., Viergever M. Multiscale vessel enhancement filtering. Medical Image Computing and Computer-Assisted Interventation - MICCAI'98 1998, 130-137. Springer. W. Wells, A. Colchester, S. Delp (Eds.).
13. Gauron C., Rampon C., Bouzaffour M., Ipendey E., Teillon J., Volovitch M., Vriz S. Sustained production of ROS triggers compensatory proliferation and is required for regeneration to proceed. Sci. Rep. 2013, 3:2084.
14. Griffiths D.F., Davies S.J., Williams D., Williams G.T., Williams E.D. Demonstration of somatic mutation and colonic crypt clonality by X-linked enzyme histochemistry. Nature 1988, 333:461-463.
15. Grove G.L., Kligman A.M. Age-associated changes in human epidermal cell renewal. J. Gerontol. 1983, 38:137-142.
16. Guillot C., Lecuit T. Mechanics of epithelial tissue homeostasis and morphogenesis. Science 2013, 340:1185-1189.
17. Gupta V., Poss K.D. Clonally dominant cardiomyocytes direct heart morphogenesis. Nature 2012, 484:479-484.
18. Hunter G.L., Crawford J.M., Genkins J.Z., Kiehart D.P. Ion channels contribute to the regulation of cell sheet forces during Drosophila dorsal closure. Development 2014, 141:325-334.
19. Lechler T., Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 2005, 437:275-280.
20. Lee Y.K., Rhodes W.T. Rotating-kernel min-max algorithms for straight-line feature enhancement. Appl. Opt. 1995, 34:290-298.
21. Lee Y., Grill S., Sanchez A., Murphy-Ryan M., Poss K.D. Fgf signaling instructs position-dependent growth rate during zebrafish fin regeneration. Development 2005, 132:5173-5183.
22. Lee R.T., Asharani P.V., Carney T.J. Basal keratinocytes contribute to all strata of the adult zebrafish epidermis. PLoS One 2014, 9:e84858.
23. Livet J., Weissman T.A., Kang H., Draft R.W., Lu J., Bennis R.A., Sanes J.R., Lichtman J.W. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 2007, 450:56-62.
24. Love N.R., Chen Y., Ishibashi S., Kritsiligkou P., Lea R., Koh Y., Gallop J.L., Dorey K., Amaya E. Amputation-induced reactive oxygen species are required for successful Xenopus tadpole tail regeneration. Nat. Cell Biol 2013, 15:222-228.
25. Macara I.G., Guyer R., Richardson G., Huo Y., Ahmed S.M. Epithelial homeostasis. Curr. Biol. 2014, 24:R815-R825.
26. Mascre G., Dekoninck S., Drogat B., Youssef K.K., Brohee S., Sotiropoulou P.A., Simons B.D., Blanpain C. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 2012, 489:257-262.
27. Mugoni V., Camporeale A., Santoro M.M. Analysis of oxidative stress in zebrafish embryos. J. Vis. Exp. 2014, 89:e51328. 10.3791/51328.
28. Niethammer P., Grabher C., Look A.T., Mitchison T.J. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 2009, 459:996-999.
29. Poleo G., Brown C.W., Laforest L., Akimenko M.A. Cell proliferation and movement during early fin regeneration in zebrafish. Dev. Dyn. 2001, 221:380-390.
30. Poss K.D. Advances in understanding tissue regenerative capacity and mechanisms in animals. Nat. Rev. Genet. 2010, 11:710-722.
31. Poss K.D., Shen J., Keating M.T. Induction of lef1 during zebrafish fin regeneration. Dev. Dyn. 2000, 219:282-286.
32. Raffel M., Willert C.E., Kompenhans J. Particle Image Velocimetry: A Practical Guide 1998, Springer.
33. Rakers S., Niklasson L., Steinhagen D., Kruse C., Schauber J., Sundell K., Paus R. Antimicrobial peptides (AMPs) from fish epidermis: perspectives for investigative dermatology. J. Invest Dermatol. 2013, 133:1140-1149.
34. Ripley B.D. Modelling spatial patterns. J. R. Stat. Soc. Series B 1977, 39:172-212.
35. Ritsma L., Ellenbroek S.I., Zomer A., Snippert H.J., de Sauvage F.J., Simons B.D., Clevers H., van Rheenen J. Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging. Nature 2014, 507:362-365.
36. Rompolas P., Deschene E.R., Zito G., Gonzalez D.G., Saotome I., Haberman A.M., Greco V. Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration. Nature 2012, 487:496-499.
37. Rompolas P., Mesa K.R., Greco V. Spatial organization within a niche as a determinant of stem-cell fate. Nature 2013, 502:513-518.
38. Sakaue-Sawano A., Kurokawa H., Morimura T., Hanyu A., Hama H., Osawa H., Kashiwagi S., Fukami K., Miyata T., Miyoshi H., et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 2008, 132:487-498.
39. Santos-Ruiz L., Santamaria J.A., Ruiz-Sanchez J., Becerra J. Cell proliferation during blastema formation in the regenerating teleost fin. Dev. Dyn. 2002, 223:262-272.
40. Schepeler T., Page M.E., Jensen K.B. Heterogeneity and plasticity of epidermal stem cells. Development 2014, 141:2559-2567.
41. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
42. Shraiman B.I. Mechanical feedback as a possible regulator of tissue growth. Proc. Natl. Acad. Sci. USA 2005, 102:3318-3323.
43. Snippert H.J., van der Flier L.G., Sato T., van Es J.H., van den Born M., Kroon-Veenboer C., Barker N., Klein A.M., van Rheenen J., Simons B.D., et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143:134-144.
44. Spallanzani L., Maty M. An Essay on Animal Reproductions 1769, T. Becket and P.A. de Hondt.
45. Sugiyama M., Sakaue-Sawano A., Iimura T., Fukami K., Kitaguchi T., Kawakami K., Okamoto H., Higashijima S., Miyawaki A. Illuminating cell-cycle progression in the developing zebrafish embryo. Proc. Natl. Acad. Sci. USA 2009, 106:20812-20817.
46. ten Freyhaus H., Huntgeburth M., Wingler K., Schnitker J., Baumer A.T., Vantler M., Bekhite M.M., Wartenberg M., Sauer H., Rosenkranz S. Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc. Res. 2006, 71:331-341.
47. Traver D., Paw B.H., Poss K.D., Penberthy W.T., Lin S., Zon L.I. Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat. Immunol. 2003, 4:1238-1246.
48. Watt F.M. Mammalian skin cell biology: at the interface between laboratory and clinic. Science 2014, 346:937-940.
49. Wehner D., Weidinger G. Signaling networks organizing regenerative growth of the zebrafish fin. Trends Genet. 2015, 31:336-343.
50. Winton D.J., Ponder B.A. Stem-cell organization in mouse small intestine. Proc. Biol. Sci. 1990, 241:13-18.
51. Yang X.C., Sachs F. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science 1989, 243:1068-1071.