Pattern Formation in the Longevity-Related Expression of Heat Shock Protein-16.2 in Caenorhabditis elegans
Tóm tắt
Aging in Caenorhabditis elegans is controlled, in part, by the insulin-like signaling and heat shock response pathways. Following thermal stress, expression levels of small heat shock protein-16.2 show a spatial patterning across the 20 intestinal cells that reside along the length of the worm. Here, we present a hypothesized mechanism that could lead to this patterned response and develop a mathematical model of this system to test our hypothesis. We propose that the patterned expression of heat shock protein is caused by a diffusion-driven instability within the pseudocoelom, or fluid-filled cavity, that borders the intestinal cells in C. elegans. This instability is due to the interactions between two classes of insulin-like peptides that serve antagonistic roles. We examine output from the developed model and compare it to experimental data on heat shock protein expression. Given biologically bounded parameters, the model presented is capable of producing patterns similar to what is observed experimentally and provides a first step in mathematically modeling aging-related mechanisms in C. elegans.
Tài liệu tham khảo
Altun Z, Hall D (2009) Alimentary system, intestine. In: WormAtlas. https://doi.org/10.3908/wormatlas.1.4
Bai JP, Chang LL (1995) Transepithelial transport of insulin: I. Insulin degradation by insulin-degrading enzyme in small intestinal epithelium. Pharm Res 12(8):1171–1175. https://doi.org/10.1023/A:1016263926946
Banse SA, Hunter CP (2012) Vampiric isolation of extracellular fluid from Caenorhabditis elegans. J Vis Exp. https://doi.org/10.3791/3647
Belle A, Tanay A, Bitincka L, Shamir R, O’Shea EK (2006) Quantification of protein half-lives in the budding yeast proteome. Proc Natl Acad Sci USA 103(35):13004–13009. https://doi.org/10.1073/pnas.0605420103
Cambridge SB, Gnad F, Nguyen C, Bermejo JL, Krüger M, Mann M (2011) Systems-wide proteomic analysis in mammalian cells reveals conserved, functional protein turnover. J Proteome Res 10(12):5275–5284. https://doi.org/10.1021/pr101183k
Duckworth WC, Bennett RG, Hamel FG (1998) Insulin degradation: progress and potential. Endocr Rev 19(5):608–24. https://doi.org/10.1210/edrv.19.5.0349
Ewbank J (2006) Signaling in the immune response. WormBook. https://doi.org/10.1895/wormbook.1.83.1
Fares H, Grant B (2002) Deciphering endocytosis in Caenorhabditis elegans. Traffic (Copenhagen, Denmark) 3(1):11–19. https://doi.org/10.1034/j.1600-0854.2002.30103.x
Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresis 18(15):2714–2723. https://doi.org/10.1002/elps.1150181505
Hartwig K, Heidler T, Moch J, Daniel H, Wenzel U (2009) Feeding a ROS-generator to Caenorhabditis elegans leads to increased expression of small heat shock protein HSP-16.2 and hormesis. Genes Nutr 4(1):59–67. https://doi.org/10.1007/s12263-009-0113-x
Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12(10):842–846. https://doi.org/10.1038/nsmb993
Hasselman B (2016) nleqslv: solve systems of nonlinear equations. https://cran.r-project.org/package=nleqslv
Hennig C (2015) fpc: flexible procedures for clustering. https://cran.r-project.org/package=fpc
Hirose T, Nakano Y, Nagamatsu Y, Misumi T, Ohta H, Ohshima Y (2003) Cyclic GMP-dependent protein kinase EGL-4 controls body size and lifespan in C. elegans. Development (Cambridge, England) 130(6):1089–1099. https://doi.org/10.1242/dev.00330
Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science (New York, NY) 300(5622):1142–1145. https://doi.org/10.1126/science.1083701
Hua QX, Nakagawa SH, Wilken J, Ramos RR, Jia W, Bass J, Weiss MA (2003) A divergent INS protein in Caenorhabditis elegans structurally resembles human insulin and activates the human insulin receptor. Genes Dev 17(7):826–831. https://doi.org/10.1101/gad.1058003
Kaletsky R, Lakhina V, Arey R, Williams A, Landis J, Ashraf J, Murphy CT (2016) The C. elegans adult neuronal IIS/FOXO transcriptome reveals adult phenotype regulators. Nature 529(7584):92–96. https://doi.org/10.1038/nature16483
Kao G, Nordenson C, Still M, Rönnlund A, Tuck S, Naredi P (2007) ASNA-1 positively regulates insulin secretion in C. elegans and mammalian cells. Cell 128(3):577–587. https://doi.org/10.1016/j.cell.2006.12.031
Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G (1997) Daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277(5328):942–946. https://doi.org/10.1126/science.277.5328.942
Li GW, Burkhardt D, Gross C, Weissman JS (2014) Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157(3):624–635. https://doi.org/10.1016/j.cell.2014.02.033
Lin K, Hsin H, Libina N, Kenyon C (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28(2):139–145. https://doi.org/10.1038/88850
Lund J, Tedesco P, Duke K, Wang J, Kim SK, Johnson TE (2002) Transcriptional profile of aging in C. elegans. Curr Biol 12(18):1566–1573. https://doi.org/10.1016/S0960-9822(02)01146-6
Mendenhall AR, Tedesco PM, Sands B, Johnson TE, Brent R (2015) Single cell quantification of reporter gene expression in live adult Caenorhabditis elegans reveals reproducible cell-specific expression patterns and underlying biological variation. PLoS One 10(5):e0124289. https://doi.org/10.1371/journal.pone.0124289
Mendenhall A, Crane MM, Tedesco PM, Johnson TE, Brent R (2017) Caenorhabditis elegans genes affecting interindividual variation in life-span biomarker gene expression. J Gerontol Ser A Biol Sci Med Sci 72(10):1305–1310. https://doi.org/10.1093/gerona/glw349
Milo R, Phillips R (2015) Cell biology by the numbers. Garland Science. http://book.bionumbers.org/
Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424(6946):277–283. https://doi.org/10.1038/nature01789
Murray JD (2001) Mathematical biology II: spatial models and biomedical applications, 3rd edn. Springer, Berlin
Pierce SB, Costa M, Wisotzkey R, Devadhar S, Homburger SA, Buchman AR, Ferguson KC, Heller J, Platt DM, Pasquinelli AA, Liu LX, Doberstein SK, Ruvkun G (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 15(6):672–686. https://doi.org/10.1101/gad.867301
Prahlad V, Morimoto RI (2009) Integrating the stress response: lessons for neurodegenerative diseases from C. elegans. Trends Cell Biol 19(2):52–61. https://doi.org/10.1016/j.tcb.2008.11.002
Prahlad V, Morimoto RI (2011) Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. Proc Natl Acad Sci USA 108(34):14204–14209. https://doi.org/10.1073/pnas.1106557108
Prahlad V, Cornelius T, Morimoto RI (2008) Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science (New York, NY) 320(5877):811–814. https://doi.org/10.1126/science.1156093
R Core Team (2015) R: a language and environment for statistical computing. Technical report, R Foundation for Statistical Computing, Vienna. https://www.r-project.org/
Rea SL, Wu D, Cypser JR, Vaupel JW, Johnson TE (2005) A stress-sensitive reporter predicts longevity in isogenic populations of Caenorhabditis elegans. Nat Genet 37(8):894–8. https://doi.org/10.1038/ng1608
Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5(4):725–738. https://doi.org/10.1038/nprot.2010.5, arXiv:1011.1669v3
Seewald AK, Cypser J, Mendenhall A, Johnson T (2010) Quantifying phenotypic variation in isogenic Caenorhabditis elegans expressing Phsp-16.2::gfp by clustering 2D expression patterns. PLoS One 5(7):e11426. https://doi.org/10.1371/journal.pone.0011426
Soetaert K, Meysman F (2009) Solving partial differential equations, using R package ReacTran, R package vignette. https://cran.rproject.org/package=ReacTran
Subramanian K, Fee CJ, Fredericks R, Stubbs RS, Hayes MT (2013) Insulin receptor–insulin interaction kinetics using multiplex surface plasmon resonance. J Mol Recognit 26(12):643–652. https://doi.org/10.1002/jmr.2307
Tepper RG, Ashraf J, Kaletsky R, Kleemann G, Murphy CT, Bussemaker HJ (2013) PQM-1 complements DAF-16 as a key transcriptional regulator of DAF-2-mediated development and longevity. Cell 154(3):676–690. https://doi.org/10.1016/j.cell.2013.07.006
Walker GA, Lithgow GJ (2003) Lifespan extension in C. elegans by a molecular chaperone dependent upon insulin-like signals. Aging Cell 2(2):131–139. https://doi.org/10.1046/j.1474-9728.2003.00045.x
Wolfram Research Inc (2016) Mathematica 11.0
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER suite: protein structure and function prediction. Nat Methods 12(1):7–8. https://doi.org/10.1038/nmeth.3213
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinform. https://doi.org/10.1186/1471-2105-9-40, https://zhanglab.ccmb.med.umich.edu/papers/2008_2.pdf, arXiv:1011.1669v3
Zhang Q, Bhattacharya S, Andersen ME (2013) Ultrasensitive response motifs: basic amplifiers in molecular signalling networks. Open Biol 3(4):130031. https://doi.org/10.1098/rsob.130031