Skip to main content
SpringerLink
Log in

Long-term cadmium exposure affects cell adhesion and expression of cadherin in the male genital organ of Pardosa pseudoannulata (Bösenberg & Strand, 1906)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Pardosa pseudoannulata (Araneae: Lycosidae), as an important predator of crop pests, has served as a strong driver for ecological regulation of pests. Cadmium (Cd) is a toxic heavy metal widely distributed in the soil in China, which not only seriously pollutes the ecological environment, but also poses a great threat to the survival of organisms. Palpal bulbs are the genital organs of male spiders, playing an important role in reproductive physiology. However, the effects of long-term Cd stress on the genital organ of the primary pest predator were poorly understood. Therefore, we investigated the Cd effect on the male palpal organ of P. pseudoannulata at morphological and gene expression levels. The results showed that no obvious difference in the morphology between the Cd-treated and control groups was observed, but cell adhesion was affected at molecular level. Transcriptome sequencing analysis revealed that under long-term Cd stress, the biological processes including cell-cell adhesion via plasma-membrane adhesion molecules, cell-cell adhesion, and homophilic cell adhesion via plasma membrane adhesion molecules were the top three differentially expressed terms (p-adj < 0.001), and 51 unigenes were annotated into cadherin-related proteins, such as protocadherin, cadherin-87A, and cadherin-96Ca, among which, 18 unigenes were significantly upregulated under the Cd stress. Our outcomes indicate that the differentially expressed genes involved in cell adhesion may explain the negative effects of Cd stress on the spider genital organ, and the comprehensive transcriptome dataset will also provide a profound molecular information of the genital organ of P. pseudoannulata.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adamkovicova M et al (2014) Effects of subchronic exposure to cadmium and diazinon on testis and epididymis in rats. Sci World J 2014:632581

    Google Scholar 

  • Bajanca F et al (2015) Editorial: cell adhesion in development. Dev Biol 401:1

    CAS  Google Scholar 

  • Bhatnagar RD, Sadana GL (1971) Morphogenesis of the tarsal tissue and the development of the intromittent palpal organs in the wolf-spider Lycosa chaperi (Simon) (Araneida: Lycosidae). Can J Zool 49:397–400

    CAS  Google Scholar 

  • Chang HY, Kao WL, You YW, Chu YH, Chu KJ, Chen PJ, Wu CY, Lee YH, Shyue JJ (2016) Effect of surface potential on epithelial cell adhesion, proliferation and morphology. Colloids Surf B Biointerfaces 141:179–186

    CAS  Google Scholar 

  • Dar MI, Green ID, Naikoo MI, Khan FA, Ansari AA, Lone MI (2017) Assessment of biotransfer and bioaccumulation of cadmium, lead and zinc from fly ash amended soil in mustard-aphid-beetle food chain. Sci Total Environ 584-585:1221–1229

    CAS  Google Scholar 

  • Davidson NM, Oshlack A (2014) Corset: enabling differential gene expression analysis forde novoassembled transcriptomes. Genome Biol 15:7

    Google Scholar 

  • de Souza Predes F, Diamante MA, Dolder H (2010) Testis response to low doses of cadmium in Wistar rats. Int J Exp Pathol 91:125–131

    Google Scholar 

  • Diaz MC et al (2017) Lectin histochemistry for detecting cadmium-induced changes in the glycosylation pattern of rat placenta. Biotech Histochem 92:36–45

    CAS  Google Scholar 

  • Dou M, Zhao P, Wang Y, Li G (2017) Health risk assessment of cadmium pollution emergency for urban populations in Foshan City. China Environ Sci Pollut Res Int 24:8071–8086

    CAS  Google Scholar 

  • Down M, Power M, Smith SI, Ralston K, Spanevello M, Burns GF, Boyd AW (2005) Cloning and expression of the large zebrafish protocadherin gene. Fat Gene Expr Patterns 5:483–490

    CAS  Google Scholar 

  • Duan Q et al (2016) Distribution of heavy metal pollution in surface soil samples in China: a graphical review. Bull Environ Contam Toxicol 97:303–309

    CAS  Google Scholar 

  • Ebnet K (2017) Junctional adhesion molecules (JAMs): cell adhesion receptors with pleiotropic functions in cell physiology and development. Physiol Rev 97:1529–1554

    CAS  Google Scholar 

  • Fannes W (2013) Two new species of the spider genus Antoonops (Araneae: Oonopidae), with a key to the known species. Zootaxa 3709:524–542

    Google Scholar 

  • Foelix RF et al (2011) Biology of Spiders Insect Syst Evol 14:16–16

    Google Scholar 

  • Gaur N, Flora G, Yadav M, Tiwari A (2014) A review with recent advancements on bioremediation-based abolition of heavy metals. Environ Sci Process Impacts 16:180–193

    CAS  Google Scholar 

  • Girard MB et al (2015) Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders. Proc Biol Sci 282:20152222

    Google Scholar 

  • Goossens S, van Roy F (2005) Cadherin-mediated cell-cell adhesion in the testis. Front Biosci 10:398–419

    CAS  Google Scholar 

  • Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644

    CAS  Google Scholar 

  • Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310

    CAS  Google Scholar 

  • Grossi B, Canals M (2015) Energetics, scaling and sexual size dimorphism of spiders. Acta Biotheor 63:71–81

    CAS  Google Scholar 

  • Guan DL et al (2019) Cadmium-induced genome-wide DNA methylation changes in growth and oxidative metabolism in Drosophila melanogaster. BMC Genomics 20:356

    Google Scholar 

  • Herberstein ME et al (2014) Dangerous mating systems: signal complexity, signal content and neural capacity in spiders. Neurosci Biobehav Rev 46(Pt 4):509–518

    Google Scholar 

  • Hojati M, Modarres-Sanavy SAM, Enferadi ST, Majdi M, Ghanati F, Farzadfar S, Pazoki A (2017) Cadmium and copper induced changes in growth, oxidative metabolism and terpenoids of Tanacetum parthenium. Environ Sci Pollut Res Int 24:12261–12272

    CAS  Google Scholar 

  • Hossain Z, Hajika M, Komatsu S (2012) Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43:2393–2416

    CAS  Google Scholar 

  • Huber BA (2004) Evolutionary transformation from muscular to hydraulic movements in spider (Arachnida, Araneae) genitalia: a study based on histological serial sections. J Morphol 261:364–376

    Google Scholar 

  • Izaguirre MF, Casco VH (2016) E-cadherin roles in animal biology: a perspective on thyroid hormone-influence. Cell Commun Signal 14:27

    Google Scholar 

  • Julin B, Bergkvist C, Wolk A, Åkesson A (2013) Cadmium in diet and risk of cardiovascular disease in women. Epidemiology 24:880–885

    Google Scholar 

  • Keeler AB et al (2015) Protocadherins branch out: multiple roles in dendrite development. Cell Adhes Migr 9:214–226

    CAS  Google Scholar 

  • Khanjani N, Jafarnejad AB, Tavakkoli L (2017) Arsenic and breast cancer: a systematic review of epidemiologic studies. Rev Environ Health 32:267–277

    CAS  Google Scholar 

  • Li CC et al (2016) Transcriptome profiling analysis of wolf spider Pardosa pseudoannulata (Araneae: Lycosidae) after cadmium exposure. Int J Mol Sci 17

  • Lin X, Gu Y, Zhou Q, Mao G, Zou B, Zhao J (2016) Combined toxicity of heavy metal mixtures in liver cells. J Appl Toxicol 36:1163–1172

    CAS  Google Scholar 

  • Lin Y, Huang JJ, Dahms HU, Zhen JJ, Ying XP (2017) Cell damage and apoptosis in the hepatopancreas of Eriocheir sinensis induced by cadmium. Aquat Toxicol 190:190–198

    CAS  Google Scholar 

  • Lupse N et al (2016) Coevolution of female and male genital components to avoid genital size mismatches in sexually dimorphic spiders. BMC Evol Biol 16:161

    Google Scholar 

  • Mahoney PA, Weber U, Onofrechuk P, Biessmann H, Bryant PJ, Goodman CS (1991) The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 67:853–868

    CAS  Google Scholar 

  • Marettova E et al (2015) Toxic effects of cadmium on testis of birds and mammals: a review. Anim Reprod Sci 155:1–10

    CAS  Google Scholar 

  • Marie PJ, Haÿ E, Modrowski D, Revollo L, Mbalaviele G, Civitelli R (2014) Cadherin-mediated cell-cell adhesion and signaling in the skeleton. Calcif Tissue Int 94:46–54

    CAS  Google Scholar 

  • McElroy JA et al (2017) Cadmium exposure and endometrial cancer risk: a large midwestern U.S. population-based case-control study. PLoS one 12:e0179360

    Google Scholar 

  • Miller JA (2007) Repeated evolution of male sacrifice behavior in spiders correlated with genital mutilation. Evolution 61:1301–1315

    Google Scholar 

  • Mottalib MA et al (2018) Assessment of trace metals in consumer chickens in Bangladesh. J Health Pollut 8:181208

    Google Scholar 

  • Mousa SA (2004) Expression of adhesion molecules during cadmium hepatotoxicity. Life Sci 75:93–105

    CAS  Google Scholar 

  • Nelson WJ, Dickinson DJ, Weis WI (2013) Roles of cadherins and catenins in cell-cell adhesion and epithelial cell polarity. Prog Mol Biol Transl Sci 116:3–23

    CAS  Google Scholar 

  • Ninkov M, Popov Aleksandrov A, Mirkov I, Demenesku J, Mileusnic D, Jovanovic Stojanov S, Golic N, Tolinacki M, Zolotarevski L, Kataranovski D, Brceski I, Kataranovski M (2016) Strain differences in toxicity of oral cadmium intake in rats. Food Chem Toxicol 96:11–23

    CAS  Google Scholar 

  • Offermann K et al (2010) Assessing the importance of dietborne cadmium and particle characteristics on bioavailability and bioaccumulation in the nematode Caenorhabditis elegans. Environ Toxicol Chem 28:1149–1158

    Google Scholar 

  • Park SL et al (2009) Cadmium stimulates the expression of vascular cell adhesion molecule-1 (VCAM-1) via p38 mitogen-activated protein kinase (MAPK) and JNK activation in cerebrovascular endothelial cells. J Pharmacol Sci 110:405–409

    CAS  Google Scholar 

  • Polotow D, Brescovit AD (2018) Kiekie, a new Neotropical spider genus of Ctenidae (Cteninae, Araneae). Zootaxa 4531:353–373

    Google Scholar 

  • Ponce E, Louie MC, Sevigny MB (2015) Acute and chronic cadmium exposure promotes E-cadherin degradation in MCF7 breast cancer cells. Mol Carcinog 54:1014–1025

    CAS  Google Scholar 

  • Raya-Sandino A et al (2017) Zonula occludens-2 regulates Rho proteins activity and the development of epithelial cytoarchitecture and barrier function. Biochim Biophys Acta Mol Cell Res 1864:1714–1733

    CAS  Google Scholar 

  • Robinson MH (1982) Courtship and mating behavior in spiders. Annu Rev Entomol 27:1–20

    Google Scholar 

  • Rzymski P, Tomczyk K, Rzymski P, Poniedziałek B, Opala T, Wilczak M (2015) Impact of heavy metals on the female reproductive system. Ann Agric Environ Med 22:259–264

    CAS  Google Scholar 

  • Shahid M, Dumat C, Khalid S, Schreck E, Xiong T, Niazi NK (2017) Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake. J Hazard Mater 325:36–58

    CAS  Google Scholar 

  • Sharpe RM, Franks S (2002) Environment, lifestyle and infertility--an inter-generational issue. Nat Cell Biol 4(Suppl):s33–s40

    Google Scholar 

  • Smalinskiene A, Lesauskaite V, Zitkevicius V, Savickiene N, Savickas A, Ryselis S, Sadauskiene I, Ivanov L (2009) Estimation of the combined effect of Eleutherococcus senticosus extract and cadmium on liver cells. Ann N Y Acad Sci 1171:314–320

    Google Scholar 

  • Su HH, Hu MM, Harvey-Samuel T, Yang YZ (2014) Accumulation and excretion of cadmium in three successive generations of Spodoptera exigua (Lepidoptera: Noctuidae) and impact on the population increase. J Econ Entomol 107:223–229

    CAS  Google Scholar 

  • Tu L, Hormiga G (2010) The female genitalic morphology of “micronetine” spiders (Araneae, Linyphiidae). Genetica. 138:59–73

    Google Scholar 

  • Uhl G et al (2007) Copulatory mechanism in a sexually cannibalistic spider with genital mutilation (Araneae: Araneidae: Argiope bruennichi). Zoology (Jena) 110:398–408

    Google Scholar 

  • van Roy F (2014) Beyond E-cadherin: roles of other cadherin superfamily members in cancer. Nat Rev Cancer 14:121–134

    Google Scholar 

  • van Roy F, Berx G (2008) The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 65:3756–3788

    CAS  Google Scholar 

  • Wang J, Wei B, Peng Y, Huang T, Yang H, Peng X, Xie C, Xu X, Sun Z, Wang Z, Lv Z, Song Q (2018a) Transcriptome analysis reveals the molecular response to cadmium toxicity in P. pseudoannulata. Environ Sci Pollut Res Int 25:34294–34305

    CAS  Google Scholar 

  • Wang X, Bao R, Fu J (2018b) The antagonistic effect of selenium on cadmium-induced damage and mRNA levels of selenoprotein genes and inflammatory factors in chicken kidney tissue. Biol Trace Elem Res 181:331–339

    CAS  Google Scholar 

  • Wang J et al (2019) Expression and functional analysis of cytochrome P450 genes in the wolf spider Pardosa pseudoannulata under cadmium stress. Ecotoxicol Environ Saf 172:19–25

    CAS  Google Scholar 

  • Wilczek G, Karcz J, Rost-Roszkowska M, Kędziorski A, Wilczek P, Skowronek M, Wiśniewska K, Kaszuba F, Surmiak K (2019) Evaluation of selected biological properties of the hunting web spider (Steatoda grossa, Theridiidae) in the aspect of short and long-term exposure to cadmium. Sci Total Environ 656:297–306

    CAS  Google Scholar 

  • Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L (2016) A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Pollut Res Int 23:8244–8259

    CAS  Google Scholar 

  • Yang H, Peng Y, Shi Y, Tian J, Wang J, Peng X, Xie C, Xu X, Song Q, Wang Z, Lv Z (2018a) Transcriptome assembly and expression profiling of the molecular responses to cadmium toxicity in cerebral ganglia of wolf spider Pardosa pseudoannulata (Araneae: Lycosidae). Ecotoxicology 27:198–208

    CAS  Google Scholar 

  • Yang H, Peng Y, Shi Y, Tian J, Wang J, Song Q, Lv Z, Xie C, Wang Z (2018b) Transcriptome analysis provides insights into the immunity function of venom glands in Pardosa pseudoannulata in responses to cadmium toxicity. Environ Sci Pollut Res Int 25:23875–23882

    CAS  Google Scholar 

  • Yang Q, Li Z, Lu X, Duan Q, Huang L, Bi J (2018c) A review of soil heavy metal pollution from industrial and agricultural regions in China: pollution and risk assessment. Sci Total Environ 642:690–700

    CAS  Google Scholar 

  • Zhao Y, Li R, Lin Y (2015) Allograft inflammatory factor-1 in grass carp (Ctenopharynogodon idella): expression and response to cadmium exposure. Fish Shellfish Immunol 47:444–449

    CAS  Google Scholar 

  • Zhao LL et al (2017) Reproductive effects of cadmium on sperm function and early embryonic development in vitro. PLoS One 12:e0186727

    Google Scholar 

Download references

Acknowledgments

Our deepest gratitude goes to the anonymous reviewers for their careful work and thoughtful suggestions that have helped improve this paper substantially.

Funding

This work was supported by the National Natural Science Foundation of China (Nos. 31472017, 31272339), the Project of Science and Technology Department of Hunan Province (No.2014FJ2003), the Tropical Disease Control and Research, Ministry of Education in China (2018kfkt03), the Scientific Research Project of Hunan Provincial Education Department (16C0778), and the Key Project of Education Department of Hunan Province (18A024).

Author information

Authors and Affiliations

  1. College of Life Science, Hunan Normal University, Changsha, 410006, Hunan, China

    Bo Lv, Juan Wang & Zhi Wang

  2. Institute of Bast Fiber Crops, Chinese Academy of Agricultural Sciences, Changsha, 410205, Hunan, China

    Yuande Peng

  3. Division of Plant Sciences, University of Missouri, Columbia, MO, 65211, USA

    Qisheng Song

Authors
  1. Bo Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuande Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qisheng Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhi Wang.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Responsible editor: Giovanni Benelli

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Bo Lv, Juan Wang, and Yuande Peng are co-first authors.

Electronic supplementary material

Fig S1

(PDF 83 kb)

Fig S2

(PNG 354 kb)

Fig S3

(PNG 55 kb)

Fig S4

(PNG 323 kb)

Table S1

(DOCX 13 kb)

Table S2

(DOC 21 kb)

Table S3

(DOC 229 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lv, B., Wang, J., Peng, Y. et al. Long-term cadmium exposure affects cell adhesion and expression of cadherin in the male genital organ of Pardosa pseudoannulata (Bösenberg & Strand, 1906). Environ Sci Pollut Res 27, 17770–17778 (2020). https://doi.org/10.1007/s11356-020-07968-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-07968-1

Keywords

Search

Navigation