Table of Contents Author Guidelines Submit a Manuscript
International Journal of Genomics
Volume 2016, Article ID 6720947, 10 pages
http://dx.doi.org/10.1155/2016/6720947
Research Article

Analysis of Gene Expression in an Inbred Line of Soft-Shell Clams (Mya arenaria) Displaying Growth Heterosis: Regulation of Structural Genes and the NOD2 Pathway

1Division of Environmental and Biological Sciences, University of Maine at Machias, Machias, ME 04654, USA
2The Jackson Laboratory, Bar Harbor, ME 04609, USA
3Mount Desert Island Biological Laboratory, Salisbury Cove, ME 04672, USA

Received 21 April 2016; Revised 11 August 2016; Accepted 25 August 2016

Academic Editor: Shen Liang Chen

Copyright © 2016 John J. Wilson et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. V. R. Snelgrove, J. Grant, and C. A. Pilditch, “Habitat selection and adult-larvae interactions in settling larvae of soft-shell clam Mya arenaria,” Marine Ecology Progress Series, vol. 182, pp. 149–159, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. B. F. Beal, M. R. Parker, and K. W. Vencile, “Seasonal effects of intraspecific density and predator exclusion along a shore-level gradient on survival and growth of juveniles of the soft-shell clam, Mya arenaria L., in Maine, USA,” Journal of Experimental Marine Biology and Ecology, vol. 264, no. 2, pp. 133–169, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. B. F. Beal and M. Gayle Kraus, “Interactive effects of initial size, stocking density, and type of predator deterrent netting on survival and growth of cultured juveniles of the soft-shell clam, Mya arenaria L., in eastern Maine,” Aquaculture, vol. 208, no. 1-2, pp. 81–111, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. L. Greco, J. Pellerin, E. Capri et al., “Physiological effects of temperature and a herbicide mixture on the soft-shell clam Mya arenaria (Mollusca, Bivalvia),” Environmental Toxicology and Chemistry, vol. 30, no. 1, pp. 132–141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. Commericial Fishing Landings Data: Maine Department of Marine Resources, 2015, http://www.maine.gov/dmr/commercial-fishing/landings/index.html
  6. “Annual Commercial Landing Statistics, National Marine Fisheries Service, NOAA Office of Science and Technology,” 2016, https://www.st.nmfs.noaa.gov/commercial-fisheries/commercial-landings/annual-landings/index
  7. R. S. Steneck, T. P. Hughes, J. E. Cinner et al., “Creation of a gilded trap by the high economic value of the maine lobster fishery,” Conservation Biology, vol. 25, no. 5, pp. 904–912, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. Y. Bassaglia, T. Bekel, C. Da Silva et al., “ESTs library from embryonic stages reveals tubulin and reflectin diversity in Sepia officinalis (Mollusca—Cephalopoda),” Gene, vol. 498, no. 2, pp. 203–211, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. H. F. Nijhout, G. Davidowitz, and D. A. Roff, “A quantitative analysis of the mechanism that controls body size in Manduca sexta,” Journal of Biology, vol. 5, article 16, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Sekine, T. Mizukami, T. Nishi et al., “Cloning and expression of cDNA for salmon growth hormone in Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 13, pp. 4306–4310, 1985. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Giard, J.-M. Lebel, E. Boucaud-Camou, and P. Favrel, “Effects of vertebrate growth factors on digestive gland cells from the mollusc Pecten maximus L.: an in vitro study,” Journal of Comparative Physiology B, vol. 168, no. 2, pp. 81–86, 1998. View at Publisher · View at Google Scholar · View at Scopus
  12. N. I. Bower, X. Li, R. Taylor, and I. A. Johnston, “Switching to fast growth: the insulin-like growth factor (IGF) system in skeletal muscle of Atlantic salmon,” Journal of Experimental Biology, vol. 211, part 24, pp. 3859–3870, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. B. C. Peterson, G. C. Waldbieser, and L. Bilodeau, “IGF-I and IGF-II mRNA expression in slow and fast growing families of USDA103 channel catfish (Ictalurus punctatus),” Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology, vol. 139, no. 3, pp. 317–323, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. B. C. Peterson, G. C. Waldbieser, and L. Bilodeau, “IGF-I and IGF-II mRNA expression in slow and fast growing families of USDA103 channel catfish (Ictalurus punctatus),” Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, vol. 139, no. 3, pp. 317–323, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Meyer and D. T. Manahan, “Gene expression profiling of genetically determined growth variation in bivalve larvae (Crassostrea gigas),” Journal of Experimental Biology, vol. 213, no. 5, pp. 749–758, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Hedgecock, J.-Z. Lin, S. DeCola et al., “Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas),” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 7, pp. 2313–2318, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Hedgecock, D. J. McGoldrick, D. T. Manahanb, J. Vavrab, N. Appelmansb, and B. L. Baynec, “Quantitative and molecular genetic analyses of heterosis in bivalve molluscs,” Journal of Experimental Marine Biology and Ecology, vol. 203, pp. 49–59, 1996. View at Google Scholar
  18. D. A. Pace, A. G. Marsh, P. K. Leong, A. J. Green, D. Hedgecock, and D. T. Manahan, “Physiological bases of genetically determined variation in growth of marine invertebrate larvae: a study of growth heterosis in the bivalve Crassostrea gigas,” Journal of Experimental Marine Biology and Ecology, vol. 335, no. 2, pp. 188–209, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Zwarts and J. Wanink, “Siphon size and burying depth in deposit- and suspension-feeding benthic bivalves,” Marine Biology, vol. 100, no. 2, pp. 227–240, 1989. View at Publisher · View at Google Scholar · View at Scopus
  20. B. F. Beal, R. Bayer, M. G. Kraus, and S. R. Chapman, “A unique shell marker in juvenile, hatchery-reared individuals of the softshell clam, Mya arenaria L.,” Fishery Bulletin, vol. 97, no. 2, pp. 380–386, 1999. View at Google Scholar · View at Scopus
  21. M. P. Heasman, W. A. O'Connor, and A. W. J. Frazer, “Induction of anaesthesia in the commercial scallop, Pecten fumatus Reeve,” Aquaculture, vol. 131, no. 3-4, pp. 231–238, 1995. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Mortazavi, B. A. Williams, K. McCue, L. Schaeffer, and B. Wold, “Mapping and quantifying mammalian transcriptomes by RNA-Seq,” Nature Methods, vol. 5, no. 7, pp. 621–628, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Conesa, P. Madrigal, S. Tarazona et al., “A survey of best practices for RNA-seq data analysis,” Genome Biology, vol. 17, article 13, 2016. View at Publisher · View at Google Scholar · View at Scopus
  24. R. C. Gentleman, V. J. Carey, D. M. Bates et al., “Bioconductor: open software development for computational biology and bioinformatics,” Genome Biology, vol. 5, no. 10, article R80, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Larionov, A. Krause, and W. R. Miller, “A standard curve based method for relative real time PCR data processing,” BMC Bioinformatics, vol. 6, article 62, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. T. Araya, A. Siah, D. Mateo et al., “Selection and evaluation of housekeeping genes for haemocytes of soft-shell clams (Mya arenaria) challenged with Vibrio splendidus,” Journal of Invertebrate Pathology, vol. 99, no. 3, pp. 326–331, 2008. View at Google Scholar
  27. A. Conesa, S. Götz, J. M. García-Gómez, J. Terol, M. Talón, and M. Robles, “Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research,” Bioinformatics, vol. 21, no. 18, pp. 3674–3676, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. E. I. Boyle, S. Weng, J. Gollub et al., “GO::TermFinder—open source software for accessing gene ontology information and finding significantly enriched gene ontology terms associated with a list of genes,” Bioinformatics, vol. 20, no. 18, pp. 3710–3715, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. Gene Ontology Consortium, “The Gene Ontology (GO) database and informatics resource,” Nucleic Acids Research, vol. 32, supplement 1, pp. D258–D261, 2004. View at Publisher · View at Google Scholar
  30. L. J. Jensen, M. Kuhn, M. Stark et al., “STRING 8—a global view on proteins and their functional interactions in 630 organisms,” Nucleic Acids Research, vol. 37, supplement 1, pp. D412–D416, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. S. A. Bustin, V. Benes, J. A. Garson et al., “The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments,” Clinical Chemistry, vol. 55, no. 4, pp. 611–622, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Huggett, K. Dheda, S. Bustin, and A. Zumla, “Real-time RT-PCR normalisation; strategies and considerations,” Genes and Immunity, vol. 6, no. 4, pp. 279–284, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Dheda, J. F. Huggett, S. A. Bustin, M. A. Johnson, G. Rook, and A. Zumla, “Validation of housekeeping genes for normalizing RNA expression in real-time PCR,” BioTechniques, vol. 37, no. 1, pp. 112–119, 2004. View at Google Scholar · View at Scopus
  34. J. B. de Kok, R. W. Roelofs, B. A. Giesendorf et al., “Normalization of gene expression measurements in tumor tissues: comparison of 13 endogenous control genes,” Laboratory Investigation, vol. 85, no. 1, pp. 154–159, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Deindl, K. Boengler, N. van Royen, and W. Schaper, “Differential expression of GAPDH and β-actin in growing collateral arteries,” Molecular and Cellular Biochemistry, vol. 236, no. 1-2, pp. 139–146, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Toyofuku, J. R. Hoffman, R. Zak, and B. M. Carlson, “Expression of α-cardiac and α-skeletal actin mRNAs in relation to innervation in regenerating and non-regenerating rat skeletal muscles,” Developmental Dynamics, vol. 193, no. 4, pp. 332–339, 1992. View at Publisher · View at Google Scholar · View at Scopus
  37. S. A. Khan, M. Tyagi, A. K. Sharma et al., “Cell-type specificity of β-actin expression and its clinicopathological correlation in gastric adenocarcinoma,” World Journal of Gastroenterology, vol. 20, no. 34, pp. 12202–12211, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. A. J. S. Hawkins and A. J. Day, “The metabolic basis of genetic differences in growth efficiency among marine animals,” Journal of Experimental Marine Biology and Ecology, vol. 203, no. 1, pp. 93–115, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Wang, J. Yang, Z. Zhou et al., “A primitive Toll-like receptor signaling pathway in mollusk Zhikong scallop Chlamys farreri,” Developmental and Comparative Immunology, vol. 35, no. 4, pp. 511–520, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Lawrence, “The nuclear factor NF-κB pathway in inflammation,” Cold Spring Harbor Perspectives in Biology, vol. 1, no. 6, pp. 1–10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. R. J. Xavier and D. K. Podolsky, “Unravelling the pathogenesis of inflammatory bowel disease,” Nature, vol. 448, no. 7152, pp. 427–434, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. W. Strober, P. J. Murray, A. Kitani, and T. Watanabe, “Signalling pathways and molecular interactions of NOD1 and NOD2,” Nature Reviews Immunology, vol. 6, no. 1, pp. 9–20, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. A. K. Pandey, Y. Yang, Z. Jiang et al., “Nod2, Rip2 and Irf5 play a critical role in the type I interferon response to Mycobacterium tuberculosis,” PLoS Pathogens, vol. 5, no. 7, Article ID e1000500, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Branquinho, P. Freire, C. Sofia, and S. De Gastroenterologia, “NOD2 mutations and colorectal cancer—where do we stand?” World Journal of Gastrointestinal Surgery, vol. 8, no. 4, pp. 284–293, 2016. View at Google Scholar
  45. A. G. Fraser, C. James, G. I. Evan, and M. O. Hengartner, “Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis,” Current Biology, vol. 9, no. 6, pp. 292–301, 1999. View at Publisher · View at Google Scholar · View at Scopus
  46. M. L. Giardino Torchia, D. B. Conze, and J. D. Ashwell, “c-IAP1 and c-IAP2 redundancy differs between T and B cells,” PLoS ONE, vol. 8, no. 6, Article ID e66161, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. M. J. Metzger, C. Reinisch, J. Sherry, and S. P. Goff, “Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams,” Cell, vol. 161, no. 2, pp. 255–263, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. P. D. N. Hebert, A. Cywinska, S. L. Ball, and J. R. deWaard, “Biological identifications through DNA barcodes,” Proceedings of the Royal Society B: Biological Sciences, vol. 270, no. 1512, pp. 313–321, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. M. P. Astorga, “Genetic considerations for mollusk production in aquaculture: current state of knowledge,” Frontiers in Genetics, vol. 5, article 435, 6 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. V. Popovici, D. R. Goldstein, J. Antonov, R. Jaggi, M. Delorenzi, and P. Wirapati, “Selecting control genes for RT-QPCR using public microarray data,” BMC Bioinformatics, vol. 10, article 42, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. A. P. Palstra, S. Beltran, E. Burgerhout et al., “Deep RNA sequencing of the skeletal muscle transcriptome in swimming fish,” PLoS ONE, vol. 8, no. 1, Article ID e53171, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. M. E. Guicciardi, N. W. Werneburg, S. F. Bronk et al., “Cellular Inhibitor of Apoptosis (cIAP)-mediated ubiquitination of phosphofurin acidic cluster sorting protein 2 (PACS-2) negatively regulates tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) cytotoxicity,” PLoS ONE, vol. 9, no. 3, Article ID e92124, 2014. View at Publisher · View at Google Scholar · View at Scopus