The details in the distributions: Why and how to study phenotypic variability

Current Opinion in Biotechnology

Volumn 24, Issue 4, 2013, Pages 752-759

  Geiler Samerotte, K A ^a   Bauer, C R ^a   Li, S ^a   Ziv, N ^a   Gresham, D ^a   Siegal, M L ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL SCIENCE; DIVERSE FIELDS; ENVIRONMENTAL DIFFERENCE; ISOGENIC; RESISTANCE TO ANTIBIOTICS; RIGOROUS ANALYSIS; STATISTICAL TECHNIQUES;

BIOLOGY; CHEMOTHERAPY; GENE EXPRESSION;

POPULATION STATISTICS;

ANTIBIOTIC RESISTANCE; BACTERIUM; BLASTOMA; CELL FUNCTION; CELL GROWTH; CELL STRUCTURE; DRUG RESISTANCE; ENVIRONMENT; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC VARIABILITY; GENETICS; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIABILITY; PRIORITY JOURNAL; REVIEW; STATISTICAL ANALYSIS; YEAST;

ANIMALS; BACTERIA; GENE EXPRESSION; GENETIC VARIATION; PHENOTYPE; PLANTS; SACCHAROMYCES CEREVISIAE; STOCHASTIC PROCESSES;

EID: 84880963941     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2013.03.010     Document Type: Review

References (78)

1. Eldar A., Elowitz M.B. Functional roles for noise in genetic circuits. Nature 2010, 467:167-173.
2. Losick R., Desplan C. Stochasticity and cell fate. Science 2008, 320:65-68.
3. Jacobs G.H. Evolution of colour vision in mammals. Philos Trans R Soc Lond B: Biol Sci 2009, 364:2957-2967.
4. Gibson G. Decanalization and the origin of complex disease. Nat Rev Genet 2009, 10:134-140.
5. Winston J.B., Erlich J.M., Green C.A., Aluko A., Kaiser K.A., Takematsu M., Barlow R.S., Sureka A.O., LaPage M.J., Janss L.L., et al. Heterogeneity of genetic modifiers ensures normal cardiac development. Circulation 2010, 121:1313-1321.
6. Bahar R., Hartmann C.H., Rodriguez K.A., Denny A.D., Busuttil R.A., Dolle M.E., Calder R.B., Chisholm G.B., Pollock B.H., Klein C.A., et al. Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 2006, 441:1011-1014.
7. Levy S.F., Ziv N., Siegal M.L. Bet hedging in yeast by heterogeneous, age-correlated expression of a stress protectant. PLoS Biol 2012, 10:e1001325.
8. Somel M., Khaitovich P., Bahn S., Paabo S., Lachmann M. Gene expression becomes heterogeneous with age. Curr Biol 2006, 16:R359-R360.
9. Bishop A.L., Rab F.A., Sumner E.R., Avery S.V. Phenotypic heterogeneity can enhance rare-cell survival in 'stress-sensitive' yeast populations. Mol Microbiol 2007, 63:507-520.
10. Roesch A., Fukunaga-Kalabis M., Schmidt E.C., Zabierowski S.E., Brafford P.A., Vultur A., Basu D., Gimotty P., Vogt T., Herlyn M. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010, 141:583-594.
11. Sharma S.V., Lee D.Y., Li B., Quinlan M.P., Takahashi F., Maheswaran S., McDermott U., Azizian N., Zou L., Fischbach M.A., et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010, 141:69-80.
12. Frank S.A., Rosner M.R. Nonheritable cellular variability accelerates the evolutionary processes of cancer. PLoS Biol 2012, 10:e1001296.
13. Islam S., Kjallquist U., Moliner A., Zajac P., Fan J.B., Lonnerberg P., Linnarsson S. Highly multiplexed and strand-specific single-cell RNA 5' end sequencing. Nat Protoc 2012, 7:813-828.
14. Snijder B., Sacher R., Ramo P., Damm E.M., Liberali P., Pelkmans L. Population context determines cell-to-cell variability in endocytosis and virus infection. Nature 2009, 461:520-523.
15. Janhunen M., Kause A., Vehvilainen H., Jarvisalo O. Genetics of microenvironmental sensitivity of body weight in rainbow trout (Oncorhynchus mykiss) selected for improved growth. PLoS ONE 2012, 7:e38766.
16. Muller S., Harms H., Bley T. Origin and analysis of microbial population heterogeneity in bioprocesses. Curr Opin Biotechnol 2010, 21:100-113.
17. Maheshri N., O'Shea E.K. Living with noisy genes: how cells function reliably with inherent variability in gene expression. Annu Rev Biophys Biomol Struct 2007, 36:413-434.
18. Raj A., van Oudenaarden A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 2008, 135:216-226.
19. Stewart-Ornstein J., Weissman J.S., El-Samad H. Cellular noise regulons underlie fluctuations in Saccharomyces cerevisiae. Mol Cell 2012, 45:483-493.
20. Queitsch C., Sangster T.A., Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002, 417:618-624.
21. Acar M., Mettetal J.T., van Oudenaarden A. Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 2008, 40:471-475.
22. Kuwahara H., Soyer O.S. Bistability in feedback circuits as a byproduct of evolution of evolvability. Mol Syst Biol 2012, 8:564.
23. Kussell E., Leibler S. Phenotypic diversity, population growth, and information in fluctuating environments. Science 2005, 309:2075-2078.
24. Thattai M., van Oudenaarden A. Stochastic gene expression in fluctuating environments. Genetics 2004, 167:523-530.
25. King O.D., Masel J. The evolution of bet-hedging adaptations to rare scenarios. Theor Popul Biol 2007, 72:560-575.
26. Salathe M., Van Cleve J., Feldman M.W. Evolution of stochastic switching rates in asymmetric fitness landscapes. Genetics 2009, 182:1159-1164.
27. Levy S.F., Siegal M.L. The robustness continuum. Adv Exp Med Biol 2012, 751:431-452.
28. Powell A.L., Nguyen C.V., Hill T., Cheng K.L., Figueroa-Balderas R., Aktas H., Ashrafi H., Pons C., Fernandez-Munoz R., Vicente A., et al. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 2012, 336:1711-1715.
29. Tooker J.F., Frank S.D. Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. J Appl Ecol 2012, 49:974-985.
30. Ronnegard L., Valdar W. Recent developments in statistical methods for detecting genetic loci affecting phenotypic variability. BMC Genet 2012, 13:63.
31. Bendall S.C., Nolan G.P. From single cells to deep phenotypes in cancer. Nat Biotechnol 2012, 30:639-647.
32. Gupta P.B., Fillmore C.M., Jiang G., Shapira S.D., Tao K., Kuperwasser C., Lander E.S. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644.
33. Newman J.R., Ghaemmaghami S., Ihmels J., Breslow D.K., Noble M., DeRisi J.L., Weissman J.S. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 2006, 441:840-846.
34. Bar-Even A., Paulsson J., Maheshri N., Carmi M., O'Shea E., Pilpel Y., Barkai N. Noise in protein expression scales with natural protein abundance. Nat Genet 2006, 38:636-643.
35. Ansel J., Bottin H., Rodriguez-Beltran C., Damon C., Nagarajan M., Fehrmann S., Francois J., Yvert G. Cell-to-cell stochastic variation in gene expression is a complex genetic trait. PLoS Genet 2008, 4:e1000049.
36. Jonikas M.C., Collins S.R., Denic V., Oh E., Quan E.M., Schmid V., Weibezahn J., Schwappach B., Walter P., Weissman J.S., et al. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 2009, 323:1693-1697.
37. Rinott R., Jaimovich A., Friedman N. Exploring transcription regulation through cell-to-cell variability. Proc Natl Acad Sci U S A 2011, 108:6329-6334.
38. Conrad C., Gerlich D.W. Automated microscopy for high-content RNAi screening. J Cell Biol 2010, 188:453-461.
39. Spiller D.G., Wood C.D., Rand D.A., White M.R. Measurement of single-cell dynamics. Nature 2010, 465:736-745.
40. Sozzani R., Benfey P.N. High-throughput phenotyping of multicellular organisms: finding the link between genotype and phenotype. Genome Biol 2011, 12:219.
41. Rimon N., Schuldiner M. Getting the whole picture: combining throughput with content in microscopy. J Cell Sci 2011, 124:3743-3751.
42. Negishi T., Nogami S., Ohya Y. Multidimensional quantification of subcellular morphology of Saccharomyces cerevisiae using CalMorph, the high-throughput image-processing program. J Biotechnol 2009, 141:109-117.
43. Levy S.F., Siegal M.L. Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol 2008, 6:e264.
44. Elowitz M.B., Levine A.J., Siggia E.D., Swain P.S. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
45. Raj A., Rifkin S.A., Andersen E., van Oudenaarden A. Variability in gene expression underlies incomplete penetrance. Nature 2010, 463:913-918.
46. Tay S., Hughey J.J., Lee T.K., Lipniacki T., Quake S.R., Covert M.W. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 2010, 466:267-271.
47. Spencer S.L., Gaudet S., Albeck J.G., Burke J.M., Sorger P.K. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 2009, 459:428-432.
48. Cohen A.A., Geva-Zatorsky N., Eden E., Frenkel-Morgenstern M., Issaeva I., Sigal A., Milo R., Cohen-Saidon C., Liron Y., Kam Z., et al. Dynamic proteomics of individual cancer cells in response to a drug. Science 2008, 322:1511-1516.
49. Tang F., Barbacioru C., Nordman E., Li B., Xu N., Bashkirov V.I., Lao K., Surani M.A. RNA-seq analysis to capture the transcriptome landscape of a single cell. Nat Protoc 2010, 5:516-535.
50. Kim J.K., Marioni J.C. Inferring the kinetics of stochastic gene expression from single-cell RNA-sequencing data. Genome Biol 2013, 14:R7.
51. Tang F., Barbacioru C., Bao S., Lee C., Nordman E., Wang X., Lao K., Surani M.A. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-seq analysis. Cell Stem Cell 2010, 6:468-478.
52. Tang F., Barbacioru C., Nordman E., Bao S., Lee C., Wang X., Tuch B.B., Heard E., Lao K., Surani M.A. Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLoS ONE 2011, 6:e21208.
53. Neves H.H.R., Carvalheiro R., Queiroz S.A. Genetic and environmental heterogeneity of residual variance of weight traits in Nellore beef cattle. Genet Select Evol 2012, 44.
54. Nakagawa S., Schielzeth H. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc 2010, 85:935-956.
55. Yang J., Loos R.J., Powell J.E., Medland S.E., Speliotes E.K., Chasman D.I., Rose L.M., Thorleifsson G., Steinthorsdottir V., Magi R., et al. FTO genotype is associated with phenotypic variability of body mass index. Nature 2012, 490:267-272.
56. Ronnegard L., Valdar W. Detecting major genetic loci controlling phenotypic variability in experimental crosses. Genetics 2011, 188:435-447.
57. Bolker B.M., Brooks M.E., Clark C.J., Geange S.W., Poulsen J.R., Stevens M.H., White J.S. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 2009, 24:127-135.
58. McCarthy D.J., Chen Y., Smyth G.K. Differential expression analysis of multifactor RNA-seq experiments with respect to biological variation. Nucleic Acids Res 2012, 40:4288-4297.
59. Cleasby I.R., Nakagawa S. Neglected biological patterns in the residuals. A behavioural ecologist's guide to co-operating with heteroscedasticity. Behav Ecol Sociobiol 2011, 65:2361-2372.
60. Pare G., Cook N.R., Ridker P.M., Chasman D.I. On the use of variance per genotype as a tool to identify quantitative trait interaction effects: a report from the Women's Genome Health Study. PLoS Genet 2010, 6:e1000981.
61. Dworkin I. Canalization, cryptic variation and developmental buffering a critical examination and analytical perspective. Variation 2005, 131-158. Academic Press. B. Hallgrimsson, B.K. Hall (Eds.).
62. Fraser H.B., Schadt E.E. The quantitative genetics of phenotypic robustness. PLoS ONE 2010, 5:e8635.
63. Bates D., Maechler M., Bolker B. lme4: linear mixed-effects models using S4 classes. R Package Version 0.999375-42 2011.
64. Smyth G.K. Generalized linear models with varying dispersion. J R Stat Soc B 1989, 51:47-60.
65. Hulse A.M., Cai J.J. Genetic variants contribute to gene expression variability in humans. Genetics 2012.
66. Ronnegard L., Shen X., Alam M. hglm: a package for fitting hierarchical generalized linear models. R J 2010, 2.
67. Hillenmeyer M.E., Fung E., Wildenhain J., Pierce S.E., Hoon S., Lee W., Proctor M., St Onge R.P., Tyers M., Koller D., et al. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 2008, 320:362-365.
68. Ramani A.K., Chuluunbaatar T., Verster A.J., Na H., Vu V., Pelte N., Wannissorn N., Jiao A., Fraser A.G. The majority of animal genes are required for wild-type fitness. Cell 2012, 148:792-802.
69. Blomberg A. Measuring growth rate in high-throughput growth phenotyping. Curr Opin Biotechnol 2011, 22:94-102.
70. Takahashi K.H., Okada Y., Teramura K. Deficiency screening for genomic regions with effects on environmental sensitivity of the sensory bristles of Drosophila melanogaster. Evolution: Int J Org Evol 2012, 66:2878-2890.
71. Shen X., Pettersson M., Ronnegard L., Carlborg O. Inheritance beyond plain heritability: variance-controlling genes in Arabidopsis thaliana. PLoS Genet 2012, 8:e1002839.
72. Mackay T.F., Lyman R.F. Drosophila bristles and the nature of quantitative genetic variation. Philos Trans R Soc Lond B: Biol Sci 2005, 360:1513-1527.
73. Jimenez-Gomez J.M., Corwin J.A., Joseph B., Maloof J.N., Kliebenstein D.J. Genomic analysis of QTLs and genes altering natural variation in stochastic noise. PLoS Genet 2011, 7:e1002295.
74. Hall M.C., Dworkin I., Ungerer M.C., Purugganan M. Genetics of microenvironmental canalization in Arabidopsis thaliana. Proc Natil Acad Sci U S A 2007, 104:13717-13722.
75. Ratcliff W.C., Denison R.F. Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Curr Biol 2010, 20:1740-1744.
76. Aldridge B.B., Fernandez-Suarez M., Heller D., Ambravaneswaran V., Irimia D., Toner M., Fortune S.M. Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 2012, 335:100-104.
77. Want A., Thomas O.R., Kara B., Liddell J., Hewitt C.J. Studies related to antibody fragment (Fab) production in Escherichia coli W3110 fed-batch fermentation processes using multiparameter flow cytometry. Cytometry A: J Int Soc Anal Cytol 2009, 75:148-154.
78. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.