Cited by 12Aquaculture disease management and microbiotaInvertebrate Immune Response MechanismsCrustacean biology and ecology

The DOI matches its Crossref record; the references it cites are not checked yet.

Enhanced immunity and hemocytes proliferation by three immunostimulants in tri-spine horseshoe crab Tachypleus tridentatus

Abstract

Tachypleus amebocyte lysate (TAL) is crucial in medical testing, but its industry in China has been restricted due to the decline of horseshoe crab population in recent years. Exploring methods of enhancing immunity and rapid hemocytes proliferation is urgent for the industrial horseshoe crab culture. In this study, β-glucan (G), peptidoglycan (P), and squalene (S) were injected to horseshoe crabs at two concentrations (5 and 10 mg/kg), in order to compare their effects on total hemocyte count (THC), reactive oxygen species (ROS), and non-specific immune enzyme activities. Results showed that the THC, superoxide dismutase (SOD), catalase (CAT), and total antioxidant capacity (T-AOC) were significantly increased by three immunostimulants at different points of time; ROS was significantly increased except at two squalene groups; lysozyme (LZM) and alkaline phosphatase (AKP) activity were increased except at low dose (5 mg/kg) squalene group; malondialdehyde (MDA) activity was decreased in all treatments; and hemocyanin concentration (HC) changed little during the experiment. At the 48th hour, THC, ROS, SOD, CAT, T-AOC, LZM, and AKP activities were significantly higher in the two peptidoglycan groups than those in the control group; the low dose β-glucan and squalene groups showed significantly higher SOD and CAT, but their THC and AKP were not significantly different from those of the control group. In general, all three immunostimulants stimulated the hemolymph parameters of horseshoe crabs, notably, peptidoglycan could significantly increase the THC and enzyme activities, suggesting that peptidoglycan can be developed as an efficient immunostimulant for horseshoe crabs.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.fsi.2021.06.001

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

The citation lists haven’t been fetched yet

References 63 · Cited by 12

Research works printed but not linked: 56

  1. Li, 2018, Endangered status and declaration on conservation of the “Living Fossil” Tachypleus tridentatus, Wetland Sci., 16, 690
  2. Obst, 2012, Molecular phylogeny of extant horseshoe crabs (Xiphosura, Limulidae) indicates Paleogene diversification of Asian species, Mol. Phylogenet. Evol., 62, 21, 10.1016/j.ympev.2011.08.025 · DOI
  3. Lee, 2016, Changes in the distributions of juvenile horseshoe crabs (Arthropoda: Chelicerata) (2002–2014) related to environmental perturbations at Pak Nai and ha Pak Nai, Deep Bay, Hong Kong SAR, China, Mar. Pollut. Bull., 108, 134, 10.1016/j.marpolbul.2016.04.037 · DOI
  4. Fu, 2019, Sociodemographic drivers and public perceptions of consumption and conservation of Asian horseshoe crabs in northern Beibu Gulf, China, Aquat. Conserv., 29, 1268, 10.1002/aqc.3125 · DOI
  5. Liao, 2019, Wisdom of crowds reveals decline of Asian horseshoe crabs in Beibu Gulf, China, Oryx, 53, 222, 10.1017/S003060531700117X · DOI
  6. Bai, 2012, Effects of continuous and alternate administration of β-glucan and mannan-oligosaccharide on the growth, immunity and resistance against Vibrio splendidus of sea cucumber Apostichopus japonicas (Selenka), Aquacult. Res., 44, 1613, 10.1111/are.12055 · DOI
  7. Torrecillas, 2014, Improved health and growth of fish fed mannan oligosaccharides: potential mode of action, Fish Shellfish Immunol., 36, 525, 10.1016/j.fsi.2013.12.029 · DOI
  8. Li, 2018, Effects of dietary inulin and mannan oligosaccharide on immune related genes expression and disease resistance of Pacific white shrimp, Litopenaeus vannamei, Fish Shellfish Immunol., 76, 78, 10.1016/j.fsi.2018.02.034 · DOI
  9. Klesius, 2007, The macrophage chemotactic activity of Streptococcus agalactiae and Streptococcus iniae extracellular products (ECP), Fish Shellfish Immunol., 22, 443, 10.1016/j.fsi.2006.05.001 · DOI
  10. Song, 2013, Effects of different enzymatic hydrolysis methods on the bioactivity of peptidoglycan in Litopenaeus vannamei, Chin. J. Oceanol. Limnol., 31, 374, 10.1007/s00343-013-2170-7 · DOI
  11. Wang, 2019, Immunostimulation of β-1,3-glucan on haemocytes of red claw crayfish (Cherax quadricarinatus), J. Southern Agric., 50, 883
  12. Meena, 2013, Beta-glucan: an ideal immunostimulant in aquaculture (a review), Mar. Pollut. Bull., 39, 431
  13. Zeng, 2016, Effects of β-glucan on ROS production and energy metabolism in yellow croaker (Pseudosciaena crocea) under acute hypoxic stress, Fish Physiol. Biochem., 42, 1395, 10.1007/s10695-016-0227-1 · DOI
  14. Willmann, 2011, Arabidopsis lysin-motif proteins lym1 lym3 cerk1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection, Natl. Acad. Sci. U. S. A., 108, 19824, 10.1073/pnas.1112862108 · DOI
  15. Yan, 2013, Characterization and comparative analyses of two amphioxus intelectins involved in the innate immune response, Fish Shellfish Immunol., 34, 1139, 10.1016/j.fsi.2013.01.017 · DOI
  16. Cloud-hansen, 2004, Breaching the great wall: peptidoglycan and microbial interactions, Nat. Rev. Microbiol., 9, 710
  17. Liu, 2015, Research Process on squalene and bioactivities, Chin. J. Food Sci., 15, 147
  18. Chen, 2004, Conservation of the horseshoe crab at Kinmen, Taiwan: strategies and practices, Biodivers. Conserv., 13, 1889, 10.1023/B:BIOC.0000035868.11083.84 · DOI
  19. Hu, 2009, Summer distribution and abundance of juvenile Chinese horseshoe crabs Tachypleus tridentatus along an intertidal zone in southern China, Aquat, Biol., 7, 107
  20. Li, 2011, Status of Chinese horseshoe crab population and conservation advance in Beihai, Guangxi, Mar. Environ. Sci., 30, 131
  21. Jenkins, 1998, Elicitation of macrophages from the Peritoneal cavity of channel catfish, J. Aquat. Anim. Health, 10, 69, 10.1577/1548-8667(1998)010<0069:EOMFTP>2.0.CO;2 · DOI
  22. Xie, 2013, Effects of Vibrio alginolyticus peptidoglycan on astaxanthin level, immune indicators and protection in Litopenaeus vannamei, J. Guangdong Ocean Univ., 33, 50
  23. Weber, 1985, Book review: blood cells of marine invertebrates. Experimental systems in cell biology and comparative physiology, MBL (Mar. Biol. Lab.) Lect. Biol., 61, 259
  24. Yan, 2019, “Delayed” interference effects of air exposure on adult Chinese horseshoe crab Tachypleus tridentatus, Aquacult. Res., 1
  25. Beauchamp, 1971, Superoxide dismutase: improved assays and an assay applicable to acrylamide gels, Anal. Biochem., 44, 276, 10.1016/0003-2697(71)90370-8 · DOI · Paper page
  26. Góth, 1991, A simple method for determination of serum catalase activity and revision of reference range, Clin. Chim. Acta, 196, 143, 10.1016/0009-8981(91)90067-M · DOI
  27. Tang, 2005, Mechanisms of selenium inhibition of cell apoptosis induced by oxysterols in rat vascular smooth muscle cells, Arch. Biochem. Biophys., 441, 16, 10.1016/j.abb.2005.06.006 · DOI
  28. Huang, 2018, Oxidative stress induced by titanium dioxide nanoparticles increases under seawater acidification in the thick shell mussel Mytilus coruscus, Mar. Environ. Res., 137, 49, 10.1016/j.marenvres.2018.02.029 · DOI
  29. Luna-Acosta, 2010, Seasonal variation of pollution biomarkers to assess the impact on health status of juvenile Pacific oysters Crassostrea gigas exposed in situ, Environ. Sci. Pollut. Res., 17, 999, 10.1007/s11356-009-0287-1 · DOI
  30. Nickerson, 1971, A comparison of molluscan and arthropod hemocyanin-I. Circular dichroism and absorption spectra, Comp. Biochem. Physiol. B, 39, 855, 10.1016/0305-0491(71)90109-X · DOI
  31. Johansson, 2000, Crustacean haemocytes and haematopoiesis, Aquaculture, 191, 45, 10.1016/S0044-8486(00)00418-X · DOI
  32. Xian, 2016, Cellular responses of the tiger shrimp Penaeus monodon haemocytes after lipopolysaccharide injection, Fish Shellfish Immunol., 54, 385, 10.1016/j.fsi.2016.04.130 · DOI
  33. Wang, 2006, Effect of salinity on the immune response of tiger shrimp Penaeus monodon and its susceptibility to Photobacterium damselae subsp. damselae, Fish Shellfish Immunol., 20, 671, 10.1016/j.fsi.2005.08.003 · DOI
  34. Xian, 2011, Cytotoxicity of nitrite on haemocytes of the tiger shrimp, Penaeus monodon, using flow cytometric analysis, Aquaculture, 317, 240, 10.1016/j.aquaculture.2011.03.026 · DOI
  35. Kwan, 2014, Hemolymph quality as indicator of health status in juvenile Chinese horseshoe crab Tachypleus tridentatus (Xiphosura) under laboratory culture, J. Exp. Mar. Biol. Ecol., 457, 135, 10.1016/j.jembe.2014.04.011 · DOI
  36. Wang, 2005, Effects of several immunostimulants on the number, ultrastructure of hemocytes and the yield, activities of phenoloxidase in Penaeus chinensis, J. Fish. China, 66
  37. Bai, 2014, Effects of β-glucan derivatives on the immunity of white shrimp Litopenaeus vannamei and its resistance against white spot syndrome virus infection, Aquaculture, 426–427, 66, 10.1016/j.aquaculture.2014.01.019 · DOI
  38. Pipe, 1992, Generation of reactive oxygen metabolites by the hemocytes of the mussel Mytilus edulis, Dev. Comp. Immunol., 16, 111, 10.1016/0145-305X(92)90012-2 · DOI
  39. Venkatachalam, 2008, Regulation of normal cell cycle progression by flavin-containing oxidases, Oncogene, 27, 20, 10.1038/sj.onc.1210634 · DOI
  40. Junkunlo, 2016, Reactive oxygen species affect transglutaminase activity and regulate hematopoiesis in a crustacean, J. Biol. Chem., 291, 17593, 10.1074/jbc.M116.741348 · DOI
  41. Chang, 2003, Dietary β-1,3-glucan effectively improves immunity and survival of Penaeus monodon challenged with white spot syndrome virus, Fish Shellfish Immunol., 15, 297, 10.1016/S1050-4648(02)00167-5 · DOI
  42. Itami, 1998, Enhancement of disease resistance of kuruma shrimp, Penaeus japonicas, after oral administration of peptidoglycan derived from Bifidobacterium thermophilum, Aquaculture, 164, 277, 10.1016/S0044-8486(98)00193-8 · DOI
  43. Qin, 2016, Dietary nano-selenium relieves hypoxia stress and, improves immunity and disease resistance in the Chinese mitten crab (Eriocheir sinensis), Fish Shellfish Immunol., 54, 481, 10.1016/j.fsi.2016.04.131 · DOI
  44. Moreira, 2016, The effects of arsenic and seawater acidification on antioxidant and biomineralization responses in two closely related Crassostrea species, Sci. Total Environ., 545, 569, 10.1016/j.scitotenv.2015.12.029 · DOI
  45. Sui, 2017, Antioxidant response of the hard shelled mussel Mytilus coruscus exposed to reduced pH and oxygen concentration, Ecotoxicol. Environ. Saf., 137, 94, 10.1016/j.ecoenv.2016.11.023 · DOI
  46. Wongsasak, 2015, Effects of dietary supplementation with β-glucan and synbiotics on immune gene expression and immune parameters under ammonia stress in Pacific white shrimp, Aquaculture, 436, 179, 10.1016/j.aquaculture.2014.10.028 · DOI
  47. Zhu, 2015, Antivirus effects of Vibrio alginolyticus peptidoglycan on Litopenaeus vannamei against white spot syndrome virus, J. Guangdong Ocean Univ., 36, 57
  48. Yao, 2008, The lysosome and lysozyme response in Chinese shrimp Fenneropenaeus chinensis to Vibrio anguillarum and laminarin stimulation, J. Exp. Mar. Biol. Ecol., 363, 124, 10.1016/j.jembe.2008.06.035 · DOI
  49. Harikrishnan, 2011, Impact of plant products on innate and adaptive immune system of cultured finfish and shellfish, Aquaculture, 317, 1
  50. Zhao, 2011, Effects of dietary β-glucan on the growth, immune responses and resistance of sea cucumber, Apostichopus japonicus against Vibrio splendidus infection, Aquaculture, 315, 269, 10.1016/j.aquaculture.2011.02.032 · DOI
  51. Zhao, 2012, Effect of long-term administration of dietary b-1,3-glucan on growth, physiological, and immune responses in Litopenaeus vannamei (Boone, 1931), Aquacult. Int., 20, 145, 10.1007/s10499-011-9448-6 · DOI
  52. C Bindu, 2015, Inhibition of virulence of Staphylococcus aureus-a food borne pathogen-by squalene, a functional lipid, J. Funct. Food, 18, 224, 10.1016/j.jff.2015.07.008 · DOI
  53. Lopez, 2003, Physiological, nutritional, and immunological role of dietary β 1-3 glucan and ascorbic acid 2-monophosphate in Litopenaeus vannamei juveniles, Aquaculture, 224, 223, 10.1016/S0044-8486(03)00214-X · DOI
  54. Misra, 2004, Changes in lysosomal enzyme activity and protection against vibrio infection in Macrobrachium rosenbergii (De Man) post larvae after bath immunostimulation with β-glucan, Fish Shellfish Immunol., 17, 390, 10.1016/j.fsi.2004.04.008 · DOI
  55. Xu, 2020, Effects of copper supplement on the immune function and blood-chemistry in adult Chinese horseshoe crab Tachypleus tridentatus, Aquaculture, 515, 734576, 10.1016/j.aquaculture.2019.734576 · DOI
  56. Coates, 2011, Possible role of phosphatidylserine hemocyanin interaction in the innate immune response of Limulus Polyphemus, Dev. Comp. Immunol., 35, 155, 10.1016/j.dci.2010.08.015 · DOI

Metadata

Authors
Liu, X., Xu, Z., Chang, X., Fang, J. K. H., Song, J., He, J., Tai, Z., Zhu, Q., & Hu, M.
Affiliations
  • Shanghai Ocean University (CN)
  • Hong Kong Polytechnic University (HK)
  • Tongji University (CN)
Corresponding author
Hu, Menghong
Venue
Fish & Shellfish Immunology
Publisher
Elsevier BV
Published
2021-08
Volume
115
Pages
112-123
ISSN
1050-4648 (ISSN-L)
OpenAlex
W3169792263
Cited by
12
References
63
Citations by year
2025: 4 · 2024: 3 · 2023: 2 · 2022: 3
FWCI
0.75
Type
journal article
Language
en
Open access
closed
Locations
  • Fish & Shellfish Immunology (publishedVersion)
  • PubMed (publishedVersion)
Funders
State Oceanic Administration
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
  • Life Sciences › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
  • Physical Sciences › Environmental Science › Ecology › Crustacean biology and ecology
Keywords
Tachypleus tridentatus, horseshoe crab, immunostimulants, peptidoglycan, β-glucan, squalene, hemocyte proliferation, hemocyte count, reactive oxygen species, antioxidant enzymes, superoxide dismutase, catalase, lysozyme, alkaline phosphatase, malondialdehyde, hemocyanin, tachypleus amebocyte lysate
MeSH terms
Adjuvants, Immunologic, Animals, Hemocytes, Horseshoe Crabs, Immunity, Innate, Male, Peptidoglycan, Squalene, beta-Glucans, Cell Proliferation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Enhanced immunity and hemocytes proliferation by three immunostimulants in tri-spine horseshoe crab Tachypleus tridentatus. https://app.cochat.ai/papers/10.1016/j.fsi.2021.06.001
The paper
Liu, X., Xu, Z., Chang, X., Fang, J. K. H., Song, J., He, J., Tai, Z., Zhu, Q., & Hu, M. (2021). Enhanced immunity and hemocytes proliferation by three immunostimulants in tri-spine horseshoe crab Tachypleus tridentatus. Fish & Shellfish Immunology. https://doi.org/10.1016/j.fsi.2021.06.001