Concise review: Understanding clonal dynamics in homeostasis and injury through multicolor lineage tracing

Stem Cells

Volumn 32, Issue 12, 2014, Pages 3046-3054

  Roy, Edwige ^a   Neufeld, Zoltan ^b   Livet, Jean ^b,c,d   Khosrotehrani, Kiarash ^a,e  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c INSERM   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e INSTITUT DE LA VISION   (France)

Author keywords

Cre loxP system; Fluorescent protein reporter genes; Lineage tracing; Progenitor cells; Technology

Indexed keywords

ADULT STEM CELL; ARTICLE; CELL FATE; CELL FUNCTION; CELL POPULATION; CELL TRANSPLANTATION; DNA BARCODING; DNA SEQUENCE; EMBRYONIC STEM CELL; EPITHELIUM; GENE EXPRESSION; GENETIC PARAMETERS; HAIR FOLLICLE; HOMEOSTASIS; HUMAN; INJURY; LOXP SITE; MORPHOGENESIS; MULTICOLOR LINEAGE TRACING; NONHUMAN; PROGENY; STEM CELL; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; REPORTER GENE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; GENES, REPORTER; HOMEOSTASIS; HUMANS; STEM CELLS;

EID: 84912090716     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1804     Document Type: Article

References (96)

1. Buckingham ME, Meilhac SM,. Tracing cells for tracking cell lineage and clonal behavior. Dev Cell 2011; 21: 394-409.
2. Kretzschmar K, Watt FM,. Lineage tracing. Cell 2012; 148: 33-45.
3. Petit AC, Legue E, Nicolas JF,. Methods in clonal analysis and applications. Reprod Nutr Dev 2005; 45: 321-339.
4. Greco V, Chen T, Rendl M, et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 2009; 4: 155-169.
5. Guo G, Luc S, Marco E, et al. Mapping cellular hierarchy by single-cell analysis of the cell surface repertoire. Cell Stem Cell 2013; 13: 492-505.
6. Cotsarelis G, Cheng SZ, Dong G, et al. Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: Implications on epithelial stem cells. Cell 1989; 57: 201-209.
7. Cotsarelis G, Sun TT, Lavker RM,. Label-retaining cells reside in the bulge area of pilosebaceous unit: Implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 1990; 61: 1329-1337.
8. Tumbar T, Guasch G, Greco V, et al. Defining the epithelial stem cell niche in skin. Science 2004; 303: 359-363.
9. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425: 836-841.
10. Arai F, Hirao A, Ohmura M, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004; 118: 149-161.
11. Welm BE, Tepera SB, Venezia T, et al. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 2002; 245: 42-56.
12. Potten CS, Owen G, Booth D,. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 2002; 115: 2381-2388.
13. Urbanek K, Cesselli D, Rota M, et al. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci U S A 2006; 103: 9226-9231.
14. Graf T, Stadtfeld M,. Heterogeneity of embryonic and adult stem cells. Cell Stem Cell 2008; 3: 480-483.
15. Chambers I, Silva J, Colby D, et al. Nanog safeguards pluripotency and mediates germline development. Nature 2007; 450: 1230-1234.
16. Toyooka Y, Shimosato D, Murakami K, et al. Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 2008; 135: 909-918.
17. Arinobu Y, Mizuno S, Chong Y, et al. Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 2007; 1: 416-427.
18. Janich P, Toufighi K, Solanas G, et al. Human epidermal stem cell function is regulated by circadian oscillations. Cell Stem Cell 2013; 13: 745-753.
19. Fuchs E, Chen T,. A matter of life and death: Self-renewal in stem cells. EMBO Rep 2013; 14: 39-48.
20. Foudi A, Hochedlinger K, Van Buren D, et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 2009; 27: 84-90.
21. Yilmaz OH, Katajisto P, Lamming DW, et al. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 2012; 486: 490-495.
22. Simons BD, Clevers H,. Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 2011; 145: 851-862.
23. Hsu YC, Pasolli HA, Fuchs E,. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 2011; 144: 92-105.
24. Watt FM, Huck WT,. Role of the extracellular matrix in regulating stem cell fate. Nat Rev Mol Cell Biol 2013; 14: 467-473.
25. Rompolas P, Mesa KR, Greco V,. Spatial organization within a niche as a determinant of stem-cell fate. Nature 2013; 502: 513-518.
26. Osawa M, Hanada K, Hamada H, et al. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996; 273: 242-245.
27. Spangrude GJ, Muller-Sieburg CE, Heimfeld S, et al. Two rare populations of mouse Thy-1lo bone marrow cells repopulate the thymus. J Exp Med 1988; 167: 1671-1683.
28. Shackleton M, Vaillant F, Simpson KJ, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439: 84-88.
29. Claudinot S, Nicolas M, Oshima H, et al. Long-term renewal of hair follicles from clonogenic multipotent stem cells. Proc Natl Acad Sci U S A 2005; 102: 14677-14682.
30. Blanpain C, Lowry WE, Geoghegan A, et al. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 2004; 118: 635-648.
31. Ito M, Liu Y, Yang Z, et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 2005; 11: 1351-1354.
32. Rompolas P, Deschene ER, Zito G, et al. Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration. Nature 2012; 487: 496-499.
33. Snippert HJ, Clevers H,. Tracking adult stem cells. EMBO Rep 2011; 12: 113-122.
34. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449: 1003-1007.
35. Sangiorgi E, Capecchi MR,. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 2008; 40: 915-920.
36. Snippert HJ, Haegebarth A, Kasper M, et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010; 327: 1385-1389.
37. Jensen KB, Collins CA, Nascimento E, et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 2009; 4: 427-439.
38. Nowak JA, Polak L, Pasolli HA, et al. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 2008; 3: 33-43.
39. Morris RJ, Liu Y, Marles L, et al. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 2004; 22: 411-417.
40. Jaks V, Barker N, Kasper M, et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 2008; 40: 1291-1299.
41. Clayton E, Doupe DP, Klein AM, et al. A single type of progenitor cell maintains normal epidermis. Nature 2007; 446: 185-189.
42. Doupe DP, Klein AM, Simons BD, et al. The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Dev Cell 2010; 18: 317-323.
43. Mascre G, Dekoninck S, Drogat B, et al. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 2012; 489: 257-262.
44. Walsh C, Cepko CL,. Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 1992; 255: 434-440.
45. Wasserstrom A, Adar R, Shefer G, et al. Reconstruction of cell lineage trees in mice. PLoS One 2008; 3: e1939.
46. Carlson CA, Kas A, Kirkwood R, et al. Decoding cell lineage from acquired mutations using arbitrary deep sequencing. Nat Methods 2012; 9: 78-80.
47. Day RN, Davidson MW,. The fluorescent protein palette: Tools for cellular imaging. Chem Soc Rev 2009; 38: 2887-2921.
48. Hadjantonakis AK, Macmaster S, Nagy A,. Embryonic stem cells and mice expressing different GFP variants for multiple non-invasive reporter usage within a single animal. BMC Biotechnol 2002; 2: 11.
49. Feng G, Mellor RH, Bernstein M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000; 28: 41-51.
50. Ueno H, Weissman IL,. Clonal analysis of mouse development reveals a polyclonal origin for yolk sac blood islands. Dev Cell 2006; 11: 519-533.
51. Ueno H, Weissman IL,. The origin and fate of yolk sac hematopoiesis: Application of chimera analyses to developmental studies. Int J Dev Biol 2010; 54: 1019-1031.
52. Weber K, Thomaschewski M, Warlich M, et al. RGB marking facilitates multicolor clonal cell tracking. Nat Med 2011; 17: 504-509.
53. Malide D, Metais JY, Dunbar CE,. Dynamic clonal analysis of murine hematopoietic stem and progenitor cells marked by 5 fluorescent proteins using confocal and multiphoton microscopy. Blood 2012; 120: e105-116.
54. Garcia-Marques J, Lopez-Mascaraque L,. Clonal identity determines astrocyte cortical heterogeneity. Cerebral Cortex 2012 [Epub ahead of print].
55. Birling MC, Gofflot F, Warot X,. Site-specific recombinases for manipulation of the mouse genome. Methods Mol Biol 2009; 561: 245-263.
56. Jefferis GS, Livet J,. Sparse and combinatorial neuron labelling. Curr Opin Neurobiol 2012; 22: 101-110.
57. Muzumdar MD, Tasic B, Miyamichi K, et al. A global double-fluorescent Cre reporter mouse. Genesis 2007; 45: 593-605.
58. De Gasperi R, Rocher AB, Sosa MA, et al. The IRG mouse: A two-color fluorescent reporter for assessing Cre-mediated recombination and imaging complex cellular relationships in situ. Genesis 2008; 46: 308-317.
59. Zong H, Espinosa JS, Su HH, et al. Mosaic analysis with double markers in mice. Cell 2005; 121: 479-492.
60. Tasic B, Miyamichi K, Hippenmeyer S, et al. Extensions of MADM (mosaic analysis with double markers) in mice. PLoS One 2012; 7: e33332.
61. Espinosa JS, Luo L,. Timing neurogenesis and differentiation: Insights from quantitative clonal analyses of cerebellar granule cells. J Neurosci 2008; 28: 2301-2312.
62. Espinosa JS, Wheeler DG, Tsien RW, et al. Uncoupling dendrite growth and patterning: Single-cell knockout analysis of NMDA receptor 2B. Neuron 2009; 62: 205-217.
63. Hippenmeyer S, Youn YH, Moon HM, et al. Genetic mosaic dissection of Lis1 and Ndel1 in neuronal migration. Neuron 2010; 68: 695-709.
64. Worley MI, Setiawan L, Hariharan IK,. TIE-DYE: A combinatorial marking system to visualize and genetically manipulate clones during development in Drosophila melanogaster. Development 2013; 140: 3275-3284.
65. Livet J, Weissman TA, Kang H, et al. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 2007; 450: 56-62.
66. Kobiler O, Lipman Y, Therkelsen K, et al. Herpesviruses carrying a Brainbow cassette reveal replication and expression of limited numbers of incoming genomes. Nat Commun 2010; 1: 146.
67. Cai D, Cohen KB, Luo T, et al. Improved tools for the Brainbow toolbox. Nat Methods 2013; 10: 540-547.
68. Tabansky I, Lenarcic A, Draft RW, et al. Developmental bias in cleavage-stage mouse blastomeres. Curr Biol 2013; 23: 21-31.
69. Ghigo C, Mondor I, Jorquera A, et al. Multicolor fate mapping of Langerhans cell homeostasis. J Exp Med 2013; 210: 1657-1664.
70. Rinkevich Y, Lindau P, Ueno H, et al. Germ-layer and lineage-restricted stem/progenitors regenerate the mouse digit tip. Nature 2011; 476: 409-413.
71. Snippert HJ, van der Flier LG, Sato T, et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010; 143: 134-144.
72. Pan YA, Freundlich T, Weissman TA, et al. Zebrabow: Multispectral cell labeling for cell tracing and lineage analysis in zebrafish. Development 2013; 140: 2835-2846.
73. Gupta M, Verma B, Kumar N, et al. Construction of intersubspecific molecular genetic map of lentil based on ISSR, RAPD and SSR markers. J Genetics 2012; 91: 279-287.
74. Hampel S, Chung P, McKellar CE, et al. Drosophila Brainbow: A recombinase-based fluorescence labeling technique to subdivide neural expression patterns. Nat Methods 2011; 8: 253-259.
75. Hadjieconomou D, Rotkopf S, Alexandre C, et al. Flybow: Genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster. Nat Methods 2011; 8: 260-266.
76. Boulina M, Samarajeewa H, Baker JD, et al. Live imaging of multicolor-labeled cells in Drosophila. Development 2013; 140: 1605-1613.
77. Wachsman G, Heidstra R, Scheres B,. Distinct Cell-Autonomous Functions of RETINOBLASTOMA-RELATED in Arabidopsis Stem Cells Revealed by the Brother of Brainbow Clonal Analysis System. Plant Cell 2011; 7: 2581-2591.
78. Loulier K, Barry R, Mahou P, et al. Multiplex cell and lineage tracking with combinatorial labels. Neuron 2014; 81: 505-520.
79. Pan YA, Livet J, Sanes JR, et al. Multicolor Brainbow imaging in zebrafish. Cold Spring Harbor Protoc 2011; 2011:pdb prot 5546.
80. Yanai H, Tanaka T, Ueno H,. Multicolor lineage tracing methods and intestinal tumors. J Gastroenterol 2013; 48: 423-433.
81. Lopez-Garcia C, Klein AM, Simons BD, et al. Intestinal stem cell replacement follows a pattern of neutral drift. Science 2010; 330: 822-825.
82. Schepers AG, Snippert HJ, Stange DE, et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012; 337: 730-735.
83. Tanaka T, Komai Y, Tokuyama Y, et al. Identification of stem cells that maintain and regenerate lingual keratinized epithelial cells. Nat Cell Biol 2013; 15: 511-518.
84. Rios AC, Fu NY, Lindeman GJ, et al. In situ identification of bipotent stem cells in the mammary gland. Nature 2014; 506: 322-327.
85. Zhang H, Zheng W, Shen Y, et al. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc Natl Acad Sci U S A 2012; 109: 12580-12585.
86. Tao J, Polumbo C, Reidy K, et al. A multicolor podocyte reporter highlights heterogeneous podocyte changes in focal segmental glomerulosclerosis. Kidney Int 2013; 85: 972-980.
87. Gupta V, Poss KD,. Clonally dominant cardiomyocytes direct heart morphogenesis. Nature 2012; 484: 479-484.
88. Garcia-Marques J, Lopez-Mascaraque L,. Clonal identity determines astrocyte cortical heterogeneity. Cerebral Cortex 2013; 23: 1463-1472.
89. Byrne H, Drasdo D,. Individual-based and continuum models of growing cell populations: A comparison. J Mathematic Biol 2009; 58: 657-687.
90. Farhadifar R, Roper JC, Aigouy B, et al. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 2007; 17: 2095-2104.
91. Swat MH, Thomas GL, Belmonte JM, et al. Multi-scale modeling of tissues using CompuCell3D. Meth Cell Biol 2012; 110: 325-366.
92. Kabla AJ,. Collective cell migration: Leadership, invasion and segregation. J Royal Soc Interf 2012; 9: 3268-3278.
93. Klein AM, Doupe DP, Jones PH, et al. Mechanism of murine epidermal maintenance: Cell division and the voter model. Phys Rev E Stat Nonlin Soft Matter Phys 2008; 77: 031907.
94. Hodgson SS, Neufeld Z, Villani RM, et al. Transgenic Flash Mice for In Vivo Quantitative Monitoring of Canonical Wnt Signaling to Track Hair Follicle Cycle Dynamics. J Invest Dermatol 2014; 134: 1519-1526.
95. D G,. A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J Comput Phys 1976; 22.
96. Mahou P, Zimmerley M, Loulier K, et al. Multicolor two-photon tissue imaging by wavelength mixing. Nat Method 2012; 9: 815-818.