Abstract
Mytilus edulis and M. trossulus are key species in marine intertidal communities that develop a leukemia-like haemic neoplasia at increased incidences at some polluted sites. The tumor-suppressor p53, known to be involved in this disease, was proposed as a biomarker based on sequence polymorphisms in M. trossulus. In this study, p53 mRNA sequence variations in normal and diseased M. edulis were compared with those reported previously for M. trossulus for caged individuals of both species submerged in Burrard Inlet (49°20′16.57″N 123°13′51.37″) in 2007 and 2010. Thirty-seven single nucleotide polymorphisms (SNPs) were detected in M. edulis p53 that formed high linkage disequilibrium blocks associated with late-stage leukemia (p < 0.05). These were found at loci that were more homologous with M. trossulus than with healthy M. edulis p53-predicted haplotypes. Increased susceptibility to this cancer might be due to, in part, p53 alleles containing these SNPs.
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References
Barrett JC (2009) Haploview: visualization and analysis of SNP genotype data. Cold Spring Harb Protoc 2009. doi:10.1101/pdb.ip71
Bower SM, McGladdery SE, Price IM (1994) Synopsis of infectious diseases and parasites of commercially exploited shellfish. Ann Rev Fish Dis 4:1–199
Cantillo AY (1998) Comparison of results of mussel watch programs of the United States and France with worldwide mussel watch studies. Mar Pollut Bull 36:712–717
Craig A, Sakamoto H, Reinisch C (1993) Prevalence of leukemia in soft-shell clams (Mya arenaria) transplanted to New Bedford Harbor. Mar Environ Res 35:199–200
Degnan J, Rosenberg N (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24:332–340
Elston R, Moore JD, Brooks K (1992) Disseminated neoplasia of bivalve molluscs. Rev Aquat Sci 6:405–466
Excoffier L, Lischer HE (2011) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x
Farley CA, Plutschak DL, Scott RF (1991) Epizootiology and distribution of transmissible sarcoma in Maryland softshell clams, Mya arenaria, 1984–1988. Environ Health Perspect 90:35–41
Gaylord B, Hill TM, Sanford E, Lenz EA, Jacobs LA, Sato KN, Russell AD, Hettinger A (2011) Functional impacts of ocean acidification in an ecologically critical foundation species. J Exp Biol 214:2586–2594. doi:10.1242/jeb.055939
Gosling E (1992) The Mussel Mytilus: ecology, physiology, genetics, and culture. Elsevier, Amsterdam
Gutierrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90
Harley CD (2011) Climate change, keystone predation, and biodiversity loss. Science 334:1124–1127. doi:10.1126/science.1210199
Heath DD, Rawson PD, Hilbish TJ (1995) PCR-based nuclear markers identify alien blue mussel (Mytilus spp.) genotypes on the west coast of Canada. Can J Fish Aquat Sci 52:2621–2627
Hellberg M (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol Evol Syst 40:291–310
Kelley ML, Winge P, Heaney JD, Stephens RE, Farell JH, Van Beneden RJ, Reinisch CL, Lesser MP, Walker CW (2001) Expression of homologues for p53 and p73 in the softshell clam (Mya arenaria), a naturally-occurring model for human cancer. Oncogene 20:748–758
Moreau V, Tremblay R, Bourget E (2005) Distribution of Mytilus edulis and M. trossulus on the Gaspe coast in relation to spatial scale. J Shellfish Res 24:545–551
Muttray AF, Cox RL, St-Jean S, van Poppelen P, Reinisch CL, Baldwin SA (2005) Identification and phylogenetic comparison of p53 in two distinct mussel species (Mytilus). Comp Biochem Physiol C Toxicol Pharmacol 140:237–250
Muttray AF, Schulte PM, Baldwin SA (2008) Invertebrate p53-like mRNA isoforms are differentially expressed in mussel haemic neoplasia. Mar Environ Res 66:412–421. doi:10.1016/j.marenvres.2008.06.004
Muttray A, St-Jean S, Bishay F, van Poppelen P, Baldwin S (2009) Comparison of tumor-suppressor gene expression in two mussel species with different susceptibilities to haemic neoplasia, a cancer of the hemolymph. 36th Aquatic Toxicity Workshop, La Malbaie, Quebec, September 27th to 30th, 2009
Muttray AF, O’Toole TF, Morrill W, Van Beneden RJ, Baldwin SA (2010) An invertebrate mdm homolog interacts with p53 and is differentially expressed together with p53 and ras in neoplastic Mytilus trossulus hemocytes. Comp Biochem Physiol B Biochem Mol Biol 156:298–308. doi:10.1016/j.cbpb.2010.04.008
Muttray A, Reinisch C, Miller J, Ernst W, Gillis P, Losier M, Sherry J (2012) Hemocytic leukemia in Prince Edward Island (PEI) soft shell clam (Mya arenaria): spatial distribution in agriculturally impacted estuaries. Sci Total Environ 424:130–142. doi:10.1016/j.scitotenv.2012.02.029
Naccarati A, Polakova V, Pardini B, Vodickova L, Hemminki K, Kumar R, Vodicka P (2012) Mutations and polymorphisms in TP53 gene—an overview on the role in colorectal cancer. Mutagenesis 27:211–218. doi:10.1093/mutage/ger067
Penny R, Hart M (1999) Distribution, genetic structure and morphometry of Mytilus edulis and M. trossulus within a mixed species zone. J Shellfish Res 18:367–374
Penny R, Hart M (2002) Comparative growth of cultured blue mussels, Mytilus edulis and Mytilus trossulus and their hybrids, in naturally mixed-species stock. Aquac Res 33:693–702
Rawson PD, Hilbish TJ (1995) Distribution of male and female mtDNA lineages in populations of blue mussels, Mytilus trossulus and M-galloprovincialis, along the Pacific coast of North America. Mar Biol 124:245–250
Rawson PD, Joyner KL, Meetze K, Hilbish TJ (1996) Evidence for intragenic recombination within a novel genetic marker that distinguishes mussels in the Mytilus edulis species complex. Heredity 77:599–607
Rawson PD, Hayhurst S, Vanscoyoc B (2001) Species composition of blue mussel populations in the northeastern Gulf of Maine. J Shellfish Res 20:31–38
Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400
Rola RC, Monteiro Mda C, Reis SR, Sandrini JZ (2012) Molecular and biochemical biomarkers responses in the mussel Mytilus edulis collected from Southern Brazil coast. Mar Pollut Bull 64:766–771. doi:10.1016/j.marpolbul.2012.01.004
Shields JD, Barnes P, Heath DD (2008) Growth and survival differences among native, introduced and hybrid blue mussels (Mytilus spp.): genotype, environment and interaction effects. Mar Biol 154:919–928
Shields JD, Heath JW, Heath DD (2010) Marine landscape shapes hybrid zone in a broadcast spawning bivalve: introgression and genetic structure in Canadian west coast Mytilus. Mar Ecol Prog Ser 399:211–223
Slatkin M (2008) Linkage disequilibrium–understanding the evolutionary past and mapping the medical future. Nat Rev Genet 9:477–485. doi:10.1038/nrg2361
Slee EA, O’Connor DJ, Lu X (2004) To die or not to die: how does p53 decide? Oncogene 23:2809–2818
Stephens RE, Walker CW, Reinisch CL (2001) Multiple protein differences distinguish clam leukemia cells from normal hemocytes: evidence for the involvement of p53 homologues. Comp Biochem Physiol C Toxicol Pharmacol 129:329–338
St-Jean SD, Kohli M, van Poppelen P (2004) Wood leachate concentration in waters from the Pacific coast, are there effects on the health of mussels, Mytilus trossulus. Can Tech Rep Fish Aquat Sci 2562:108
Teacher AG, Griffiths DJ (2011) HapStar: automated haplotype network layout and visualization. Mol Ecol Resour 11:151–153. doi:10.1111/j.1755-0998.2010.02890.x
Toledo F, Krummel KA, Lee CJ, Liu CW, Rodewald LW, Tang M, Wahl GM (2006) A mouse p53 mutant lacking the proline-rich domain rescues Mdm4 deficiency and provides insight into the Mdm2-Mdm4-p53 regulatory network. Cancer Cell 9:273–285. doi:10.1016/j.ccr.2006.03.014
Toro J, Thompson R (2002) Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis, M. trossulus) and their hybrids from Newfoundland. Mar Biol 141:8897–8909
Varvio S, Koehn L, Vainola R (1988) Evolutionary genetics of the Mytilus edulis complex in the North Atlantic region. Mar Biol 98:51–60
Vassilenko EI, Muttray AF, Schulte PM, Baldwin SA (2010) Variations in p53-like cDNA sequence are correlated with mussel haemic neoplasia: a potential molecular-level tool for biomonitoring. Mutat Res 701:145–152. doi:10.1016/j.mrgentox.2010.06.001
Whibley C, Pharoah PD, Hollstein M (2009) p53 polymorphisms: cancer implications. Nat Rev Cancer 9:95–107. doi:10.1038/nrc2584
Acknowledgments
Funding was generously provided by the Natural Sciences and Engineering Research Council of Canada Collaborative Research and Development Grant program (CRDPJ 349918) and Metro Vancouver (Head Office: 4330 Kingsway, Burnaby, B.C. V5H 4G8). Dr. Annette Muttray is acknowledged for arranging the collection and shipping of M. edulis from Prince Edward Island.
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Communicated by T. Reusch.
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Vassilenko, E., Baldwin, S.A. p53 sequence polymorphisms in late-stage leukemic Mytilus edulis are homologous with M. trossulus p53. Mar Biol 160, 1751–1760 (2013). https://doi.org/10.1007/s00227-013-2227-3
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DOI: https://doi.org/10.1007/s00227-013-2227-3