Gold-nanoparticle-assisted Laser Perturbation of Chromatin Assembly Reveals Unusual Aspects of Nuclear Architecture Within Living Cells

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2007 May 15

PMID 17496030

Citations 21

Authors

Aprotim Mazumder

G V Shivashankar

Affiliations

Soon will be listed here.

Abstract

Chromatin organization within the nucleus is a vital regulator of genome function, yet its mechanical coupling to the nuclear architecture has remained elusive. To directly investigate this coupling, we locally modulated chromatin structure in living cells using nanoparticle-based laser perturbation. Unusual differences in the response of the cell nucleus were observed depending on the nuclear region that was perturbed--the heterochromatin, the euchromatin, and the nuclear envelope. This response varied under different conditions of cellular perturbations such as ATP depletion, apoptosis, and inhibition of histone deacetylases. Our studies implicate heterochromatin organization in imparting mechanical stability to the cell nucleus and suggest that nuclear size and shape are the result of interplay between nuclear and cytoplasmic anchors.

Citing Articles

Femtosecond Plasmonic Laser Nanosurgery (fs-PLN) mediated by molecularly targeted gold nanospheres at ultra-low pulse fluences.

Eversole D, Subramanian K, Harrison R, Bourgeois F, Yuksel A, Ben-Yakar A Sci Rep. 2020; 10(1):12387.

PMID: 32709944 PMC: 7382507. DOI: 10.1038/s41598-020-68512-2.

Epigenetic Aspects of Engineered Nanomaterials: Is the Collateral Damage Inevitable?.

Gedda M, Babele P, Zahra K, Madhukar P Front Bioeng Biotechnol. 2019; 7:228.

PMID: 31616663 PMC: 6763616. DOI: 10.3389/fbioe.2019.00228.

Intracellular Delivery by Membrane Disruption: Mechanisms, Strategies, and Concepts.

Stewart M, Langer R, Jensen K Chem Rev. 2018; 118(16):7409-7531.

PMID: 30052023 PMC: 6763210. DOI: 10.1021/acs.chemrev.7b00678.

Regulation of genome organization and gene expression by nuclear mechanotransduction.

Uhler C, Shivashankar G Nat Rev Mol Cell Biol. 2017; 18(12):717-727.

PMID: 29044247 DOI: 10.1038/nrm.2017.101.

Nuclear morphologies: their diversity and functional relevance.

Skinner B, Johnson E Chromosoma. 2016; 126(2):195-212.

PMID: 27631793 PMC: 5371643. DOI: 10.1007/s00412-016-0614-5.

References

Maniotis A, Chen C, Ingber D . Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci U S A. 1997; 94(3):849-54. PMC: 19602. DOI: 10.1073/pnas.94.3.849. View

Koberna K, Stanek D, Malinsky J, Eltsov M, Pliss A, Ctrnacta V . Nuclear organization studied with the help of a hypotonic shift: its use permits hydrophilic molecules to enter into living cells. Chromosoma. 1999; 108(5):325-35. DOI: 10.1007/s004120050384. View

Tamada M, Sheetz M, Sawada Y . Activation of a signaling cascade by cytoskeleton stretch. Dev Cell. 2004; 7(5):709-18. DOI: 10.1016/j.devcel.2004.08.021. View

Botvinick E, Venugopalan V, Shah J, Liaw L, Berns M . Controlled ablation of microtubules using a picosecond laser. Biophys J. 2004; 87(6):4203-12. PMC: 1304929. DOI: 10.1529/biophysj.104.049528. View

Supatto W, Debarre D, Moulia B, Brouzes E, Martin J, Farge E . In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses. Proc Natl Acad Sci U S A. 2005; 102(4):1047-52. PMC: 545833. DOI: 10.1073/pnas.0405316102. View

Gilbert N, Boyle S, Fiegler H, Woodfine K, Carter N, Bickmore W . Chromatin architecture of the human genome: gene-rich domains are enriched in open chromatin fibers. Cell. 2004; 118(5):555-66. DOI: 10.1016/j.cell.2004.08.011. View

Zink D, Fischer A, Nickerson J . Nuclear structure in cancer cells. Nat Rev Cancer. 2004; 4(9):677-87. DOI: 10.1038/nrc1430. View

Carvalho P, Pellman D . Mitotic spindle: laser microsurgery in yeast cells. Curr Biol. 2004; 14(18):R748-50. DOI: 10.1016/j.cub.2004.09.010. View

Osborne C, Chakalova L, Brown K, Carter D, Horton A, Debrand E . Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet. 2004; 36(10):1065-71. DOI: 10.1038/ng1423. View

10.

Kosak S, Groudine M . Gene order and dynamic domains. Science. 2004; 306(5696):644-7. DOI: 10.1126/science.1103864. View

11.

Schmucker D, Su A, Beermann A, Jackle H, Jay D . Chromophore-assisted laser inactivation of patched protein switches cell fate in the larval visual system of Drosophila. Proc Natl Acad Sci U S A. 1994; 91(7):2664-8. PMC: 43430. DOI: 10.1073/pnas.91.7.2664. View

12.

Gruenbaum Y, Margalit A, Goldman R, Shumaker D, Wilson K . The nuclear lamina comes of age. Nat Rev Mol Cell Biol. 2005; 6(1):21-31. DOI: 10.1038/nrm1550. View

13.

Zaidi S, Young D, Choi J, Pratap J, Javed A, Montecino M . The dynamic organization of gene-regulatory machinery in nuclear microenvironments. EMBO Rep. 2005; 6(2):128-33. PMC: 1299247. DOI: 10.1038/sj.embor.7400337. View

14.

Sproul D, Gilbert N, Bickmore W . The role of chromatin structure in regulating the expression of clustered genes. Nat Rev Genet. 2005; 6(10):775-81. DOI: 10.1038/nrg1688. View

15.

Foster H, Bridger J . The genome and the nucleus: a marriage made by evolution. Genome organisation and nuclear architecture. Chromosoma. 2005; 114(4):212-29. DOI: 10.1007/s00412-005-0016-6. View

16.

Shukla R, Bansal V, Chaudhary M, Basu A, Bhonde R, Sastry M . Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir. 2005; 21(23):10644-54. DOI: 10.1021/la0513712. View

17.

Haithcock E, Dayani Y, Neufeld E, Zahand A, Feinstein N, Mattout A . Age-related changes of nuclear architecture in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2005; 102(46):16690-5. PMC: 1283819. DOI: 10.1073/pnas.0506955102. View

18.

Horowitz-Scherer R, Woodcock C . Organization of interphase chromatin. Chromosoma. 2005; 115(1):1-14. DOI: 10.1007/s00412-005-0035-3. View

19.

Kumar S, Maxwell I, Heisterkamp A, Polte T, Lele T, Salanga M . Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J. 2006; 90(10):3762-73. PMC: 1440757. DOI: 10.1529/biophysj.105.071506. View

20.

Houben F, Ramaekers F, Snoeckx L, Broers J . Role of nuclear lamina-cytoskeleton interactions in the maintenance of cellular strength. Biochim Biophys Acta. 2006; 1773(5):675-86. DOI: 10.1016/j.bbamcr.2006.09.018. View