Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Sea cucumber as a therapeutic aquatic resource for human health

  • Siddiqui, Ruqaiyyah (College of Arts and Sciences, American University of Sharjah, University City) ;
  • Boghossian, Anania (College of Arts and Sciences, American University of Sharjah, University City) ;
  • Khan, Naveed Ahmed (Department of Clinical Sciences, College of Medicine, University of Sharjah, University City)
  • Received : 2022.01.28
  • Accepted : 2022.04.22
  • Published : 2022.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Sea cucumbers are worm-like, leathery bodied, benthic, marine organisms with a branched gonad. There are over 900 species, and these organisms are capable of changing their mechanical state, regenerating their small appendages, and digestive tract. Additionally, sea cucumbers possess both commercial and therapeutical value. Furthermore, it is thought that the metabolites these organisms possess may give rise to their therapeutical value. The use of sea cucumbers in therapy can be traced back to the Ming dynasty, where they were eaten for their tonic properties against constipation, hypertension, and rheumatism. A plethora of studies have been conducted, whereby different metabolites were extracted from sea cucumbers and tested for different therapeutic properties. Herein, we review and discuss the anti-cancer, anti-microbial, anti-coagulant, anti-diabetic, antioxidant, and anti-inflammatory properties of the sea cucumber by assessing literature on PubMed and Google Scholar. Furthermore, the genome and epigenome of these remarkable species is discussed. With the immense data supporting the therapeutic properties of sea cucumbers, further studies are warranted, in order to develop novel and innovative therapeutic compounds for the benefit of human health from these fascinating marine organisms.

Keywords

Acknowledgement

Work in the authors' laboratories is supported by grants from the Air Force Office of Scientific Research (AFOSR), United States of America (grant number: FA8655-20-1-7004).

References

  1. Adibpour N, Nasr F, Nematpour F, Shakouri A, Ameri A. Antibacterial and antifungal activity of Holothuria leucospilota isolated from Persian Gulf and Oman Sea. Jundishapur J Microbiol. 2014;7:e8708. https://doi.org/10.5812/jjm.8708
  2. Adrian TE, Collin P. The anti-cancer effects of frondoside A. Mar Drugs. 2018;16:64. https://doi.org/10.3390/md16020064
  3. Akbar N, Siddiqui R, Sagathevan K, Iqbal M, Khan NA. Gut bacteria of water monitor lizard (Varanus salvator) are a potential source of antibacterial compound(s). Antibiotics. 2019;8:164. https://doi.org/10.3390/antibiotics8040164
  4. Akbar N, Siddiqui R, Sagathevan K, Khan NA. Gut bacteria of animals living in polluted environments exhibit broad-spectrum antibacterial activities. Int Microbiol. 2020;23:511-26. https://doi.org/10.1007/s10123-020-00123-3
  5. Alves E, Dias M, Lopes D, Almeida A, Domingues MR, Rey F. Antimicrobial lipids from plants and marine organisms: an overview of the current state-of-the-art and future prospects. Antibiotics. 2020;9:441. https://doi.org/10.3390/antibiotics9080441
  6. Aminin DL, Menchinskaya ES, Pisliagin EA, Silchenko AS, Avilov SA, Kalinin VI. Anticancer activity of sea cucumber triterpene glycosides. Mar Drugs. 2015;13:1202-23. https://doi.org/10.3390/md13031202
  7. Aprianto R, Amir N, Kasmiati, Matusalach, Fahrul, Syahrul, et al. Economically important sea cucumber processing techniques in South Sulawesi, Indonesia. IOP Conf Ser Earth Environ Sci. 2019;370:012082. https://doi.org/10.1088/1755-1315/370/1/012082
  8. Attoub S, Arafat K, Gelaude A, Al Sultan MA, Bracke M, Collin P, et al. Frondoside a suppressive effects on lung cancer survival, tumor growth, angiogenesis, invasion, and metastasis. PLOS ONE. 2013;8:e53087. https://doi.org/10.1371/journal.pone.0053087
  9. Bordbar S, Anwar F, Saari N. High-value components and bioactives from sea cucumbers for functional foods: a review. Mar Drugs. 2011;9:1761-805. https://doi.org/10.3390/md9101761
  10. Capadona JR, Shanmuganathan K, Tyler DJ, Rowan SJ, Weder C. Stimuli-responsive polymer nanocomposites inspired by the sea cucumber dermis. Science. 2008;319:1370-74. https://doi.org/10.1126/science.1153307
  11. Cardoso J, Nakayama DG, Sousa E, Pinto E. Marine-derived compounds and prospects for their antifungal application. Molecules. 2020;25:5856. https://doi.org/10.3390/molecules25245856
  12. Chen J. Overview of sea cucumber farming and sea ranching practices in China. SPC Inf Bull. 2003;18:18-23.
  13. Chen L, Wang XY, Liu RZ, Wang GY. Culturable microorganisms associated with sea cucumbers and microbial natural products. Mar Drugs. 2021;19:461. https://doi.org/10.3390/md19080461
  14. Chollet L, Saboural P, Chauvierre C, Villemin JN, Letourneur D, Chaubet F. Fucoidans in nanomedicine. Mar Drugs. 2016;14:145. https://doi.org/10.3390/md14080145
  15. Choudhary A, Naughton LM, Montanchez I, Dobson ADW, Rai DK. Current status and future prospects of marine natural products (MNPs) as antimicrobials. Mar Drugs. 2017;15:272. https://doi.org/10.3390/md15090272
  16. Claereboudt EJS, Caulier G, Decroo C, Colson E, Gerbaux P, Claereboudt MR, et al. Triterpenoids in echinoderms: fundamental differences in diversity and biosynthetic pathways. Mar Drugs. 2019;17:352. https://doi.org/10.3390/md17060352
  17. Correia-da-Silva M, Sousa E, Pinto MMM, Kijjoa A. Anticancer and cancer preventive compounds from edible marine organisms. Semin Cancer Biol. 2017;46:55-64. https://doi.org/10.1016/j.semcancer.2017.03.011
  18. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 2010;74:417-33. https://doi.org/10.1128/MMBR.00016-10
  19. Dolmatov IY. Molecular aspects of regeneration mechanisms in holothurians. Genes. 2021;12:250. https://doi.org/10.3390/genes12020250
  20. Eriksson H, Robinson G, Slater MJ, Troell M. Sea cucumber aquaculture in the Western Indian Ocean: challenges for sustainable livelihood and stock improvement. Ambio. 2012;41:109-21. https://doi.org/10.1007/s13280-011-0195-8
  21. Esmat AY, Said MM, Soliman AA, El-Masry KSH, Badiea EA. Bioactive compounds, antioxidant potential, and heaptoprotective activity of sea cucumber (Holothuria atra) against thioacetamide intoxication in rats. Nutrition. 2013;29:258-67. https://doi.org/10.1016/j.nut.2012.06.004
  22. Farshadpour F, Gharibi S, Taherzadeh M, Amirinejad R, Taherkhani R, Habibian A, et al. Antiviral activity of Holothuria sp. a sea cucumber against herpes simplex virus type 1 (HSV-1). Eur Rev Med Pharmacol Sci. 2014;18:333-7.
  23. Festa M, Sansone C, Brunet C, Crocetta F, Di Paola L, Lombardo M, et al. Cardiovascular active peptides of marine origin with ACE inhibitory activities: potential role as anti-hypertensive drugs and in prevention of SARS-CoV-2 infection. Int J Mol Sci. 2020;21:8364. https://doi.org/10.3390/ijms21218364
  24. Fu XM, Zhang MQ, Shao CL, Li GQ, Bai H, Dai GL, et al. Chinese marine materia medica resources: status and potential. Mar Drugs. 2016;14:46. https://doi.org/10.3390/md14030046
  25. Gajdosechova Z, Palmer CH, Dave D, Jiao G, Zhao Y, Tan Z, et al. Arsenic speciation in sea cucumbers: identification and quantitation of water-extractable species. Environ Pollut. 2020;266:115190. https://doi.org/10.1016/j.envpol.2020.115190
  26. Garcia-Arraras JE, Greenberg MJ. Visceral regeneration in holothurians. Microsc Res Tech. 2001;55:438-51. https://doi.org/10.1002/jemt.1189
  27. Ghanbari R, Ebrahimpour A, Abdul-Hamid A, Ismail A, Saari N. Actinopyga lecanora hydrolysates as natural antibacterial agents. Int J Mol Sci. 2012;13:16796-811. https://doi.org/10.3390/ijms131216796
  28. Gong PX, Li QY, Wu YC, Lu WY, Zeng J, Li HJ. Structural elucidation and antidiabetic activity of fucosylated chondroitin sulfate from sea cucumber Stichopus japonicas. Carbohydr Polym. 2021;262:117969. https://doi.org/10.1016/j.carbpol.2021.117969
  29. Guo Y, Ding Y, Xu F, Liu B, Kou Z, Xiao W, et al. Systems pharmacology-based drug discovery for marine resources: an example using sea cucumber (Holothurians). J Ethnopharmacol. 2015;165:61-72. https://doi.org/10.1016/j.jep.2015.02.029
  30. Hernandez-Pasos J, Valentin-Tirado G, Garcia-Arraras JE. Melanotransferrin: new homolog genes and their differential expression during intestinal regeneration in the sea cucumber Holothuria glaberrima. J Exp Zool B Mol Dev Evol. 2017;328:259-74. https://doi.org/10.1002/jez.b.22731
  31. Hirsh J, O'Donnell M, Weitz JI. New anticoagulants. Blood. 2005;105:453-63. https://doi.org/10.1182/blood-2003-12-4195
  32. Hossain A, Dave D, Shahidi F. Northern sea cucumber (Cucumaria frondosa): a potential candidate for functional food, nutraceutical, and pharmaceutical sector. Mar Drugs. 2020;18:274. https://doi.org/10.3390/md18050274
  33. Huang N, Wu MY, Zheng CB, Zhu L, Zhao JH, Zheng YT. The depolymerized fucosylated chondroitin sulfate from sea cucumber potently inhibits HIV replication via interfering with virus entry. Carbohydr Res. 2013;380:64-9. https://doi.org/10.1016/j.carres.2013.07.010
  34. Janakiram NB, Mohammed A, Rao CV. Sea cucumbers metabolites as potent anti-cancer agents. Mar Drugs. 2015;13:2909-23. https://doi.org/10.3390/md13052909
  35. Jeyamogan S, Khan NA, Siddiqui R. Animals living in polluted environments are a potential source of anti-tumor molecule(s). Cancer Chemother Pharmacol. 2017;80:919-24. https://doi.org/10.1007/s00280-017-3410-x
  36. Kamyab E, Rohde S, Kellermann MY, Schupp PJ. Chemical defense mechanisms and ecological implications of Indo-Pacific Holothurians. Molecules. 2020;25:4808. https://doi.org/10.3390/molecules25204808
  37. Khan NA, Siddiqui R. War on terror cells: killing the host that harbours 'superbugs' is an infection control strategy in our fight against infectious diseases. Pathog Glob Health. 2014;108:4-10. https://doi.org/10.1179/2047773213Y.0000000125
  38. Khotimchenko Y. Pharmacological potential of sea cucumbers. Int J Mol Sci. 2018;19:1342. https://doi.org/10.3390/ijms19051342
  39. Li X, Roginsky AB, Ding XZ, Woodward C, Collin P, Newman RA, et al. Review of the apoptosis pathways in pancreatic cancer and the anti-apoptotic effects of the novel sea cucumber compound, frondoside A. Ann N Y Acad Sci. 2008;1138:181-98. https://doi.org/10.1196/annals.1414.025
  40. Li YX, Himaya SWA, Kim SK. Triterpenoids of marine origin as anti-cancer agents. Molecules. 2013;18:7886-909. https://doi.org/10.3390/molecules18077886
  41. Liu X, Hao J, Shan X, Zhang X, Zhao X, Li Q, et al. Antithrombotic activities of fucosylated chondroitin sulfates and their depolymerized fragments from two sea cucumbers. Carbohydr Polym. 2016;152:343-50. https://doi.org/10.1016/j.carbpol.2016.06.106
  42. Maier MS, Roccatagliata AJ, Kuriss A, Chludil H, Seldes AM, Pujol CA, et al. Two new cytotoxic and virucidal trisulfated triterpene glycosides from the Antarctic sea cucumber Staurocucumis liouvillei. J Nat Prod. 2001;64:732-6. https://doi.org/10.1021/np000584i
  43. Malve H. Exploring the ocean for new drug developments: marine pharmacology. J Pharm Bioallied Sci. 2016;8:83-91. https://doi.org/10.4103/0975-7406.171700
  44. Medina-Feliciano JG, Pirro S, Garcia-Arraras JE, Mashanov V, Ryan JF. Draft genome of the sea cucumber Holothuria glaberrima, a model for the study of regeneration. Front Mar Sci. 2021;8:603410. https://doi.org/10.3389/fmars.2021.603410
  45. Mondol MAM, Shin HJ, Rahman MA, Islam MT. Sea cucumber glycosides: chemical structures, producing species and important biological properties. Mar Drugs. 2017;15:317. https://doi.org/10.3390/md15100317
  46. Montero N, Atzori M, Marras B, Bettoschi A, Nurchis P, Coroneo V, et al. Trace metal levels in the edible tissues of sea cucumbers (Holothuria tubulosa and Holothuria polii) from Sardinia (Western Mediterranean). Ital J Food Saf. 2021;10:9576.
  47. Mou J, Wang C, Li W, Yang J. Purification, structural characterization and anticoagulant properties of fucosylated chondroitin sulfate isolated from Holothuria mexicana. Int J Biol Macromol. 2017;98:208-15. https://doi.org/10.1016/j.ijbiomac.2017.01.123
  48. Myron P, Siddiquee S, Al Azad S. Fucosylated chondroitin sulfate diversity in sea cucumbers: a review. Carbohydr Polym. 2014;112:173-8. https://doi.org/10.1016/j.carbpol.2014.05.091
  49. Nishikawa Y, Furukawa A, Shiga I, Muroi Y, Ishii T, Hongo Y, et al. Cytoprotective effects of lysophospholipids from sea cucumber Holothuria atra. PLOS ONE. 2015;10:e0135701. https://doi.org/10.1371/journal.pone.0135701
  50. Ochiewo J, de la Torre-Castro M, Muthama C, Munyi F, Nthuta JM. Socio-economic features of sea cucumber fisheries in southern coast of Kenya. Ocean Coast Manag. 2010;53:192-202. https://doi.org/10.1016/j.ocecoaman.2010.01.010
  51. Olivera-Castillo L, Grant G, Kantun-Moreno N, Acevedo-Fernandez JJ, Puc-Sosa M, Montero J, et al. Sea cucumber (Isostichopus badionotus) body-wall preparations exert anti-inflammatory activity in vivo. PharmaNutrition. 2018;6:74-80. https://doi.org/10.1016/j.phanu.2018.03.002
  52. Pangestuti R, Arifin Z. Medicinal and health benefit effects of functional sea cucumbers. J Tradit Complement Med. 2017;8:341-51. https://doi.org/10.1016/j.jtcme.2017.06.007
  53. Park JI, Bae HR, Kim CG, Stonik VA, Kwak JY. Relationships between chemical structures and functions of triterpene glycosides isolated from sea cucumbers. Front Chem. 2014;2:77. https://doi.org/10.3389/fchem.2014.00077
  54. Pawson DL, Pawson DJ, King RA. A taxonomic guide to the Echinodermata of the South Atlantic Bight, USA: 1. Sea cucumbers (Echinodermata: Holothuroidea). Zootaxa. 2010;2449:1-48. https://doi.org/10.11646/zootaxa.2449.1.1
  55. Pierrat J, Bedier A, Eeckhaut I, Magalon H, Frouin P. Sophistication in a seemingly simple creature: a review of wild holothurian nutrition in marine ecosystems. Biol Rev Camb Philos Soc. 2022;97:273-98. https://doi.org/10.1111/brv.12799
  56. Pomin VH. Holothurian fucosylated chondroitin sulfate. Mar Drugs. 2014;12:232-54. https://doi.org/10.3390/md12010232
  57. Popov RS, Avilov SA, Silchenko AS, Kalinovsky AI, Dmitrenok PS, Grebnev BB, et al. Cucumariosides F1 and F2, two new triterpene glycosides from the sea cucumber Eupentacta fraudatrix and their LC-ESI MS/MS identification in the starfish Patiria pectinifera, a predator of the sea cucumber. Biochem Syst Ecol. 2014;57:191-7. https://doi.org/10.1016/j.bse.2014.08.009
  58. Sajwani FH. Frondoside A is a potential anticancer agent from sea cucumbers. J Cancer Res Ther. 2019;15:953-60. https://doi.org/10.4103/jcrt.jcrt_1427_16
  59. Senadheera TRL, Dave D, Shahidi F. Sea cucumber derived type I collagen: a comprehensive review. Mar Drugs. 2020;18:471. https://doi.org/10.3390/md18090471
  60. Shikov AN, Flisyuk EV, Obluchinskaya ED, Pozharitskaya ON. Pharmacokinetics of marine-derived drugs. Mar Drugs. 2020;18:557. https://doi.org/10.3390/md18110557
  61. Siddiqui R, Mansoor S, Khan NA. Do crocodiles and alligators hold the key to cancer treatment? Br Med J. 2016;354.
  62. Solis A, Nunn CL. One health disparities and COVID-19. Evol Med Public Health. 2021;9:70-7. https://doi.org/10.1093/emph/eoab003
  63. Song M, Park DK, Cho M, Park HJ. Anti-inflammatory and anti-allergic activities of sea cucumber (Stichopus japonicus) extract. Food Sci Biotechnol. 2013;22:1661-6. https://doi.org/10.1007/s10068-013-0264-9
  64. Tang WC. Chinese medicinal materials from the sea. Chin Med. 1987;1:571-600.
  65. Vessella G, Traboni S, Laezza A, Iadonisi A, Bedini E. (Semi)-synthetic fucosylated chondroitin sulfate oligo- and polysaccharides. Mar Drugs. 2020;18:293. https://doi.org/10.3390/md18060293
  66. Wang T, Zheng L, Zhao T, Zhang Q, Liu Z, Liu X, et al. Anti-diabetic effects of sea cucumber (Holothuria nobilis) hydrolysates in streptozotocin and high-fat-diet induced diabetic rats via activating the PI3K/Akt pathway. J Funct Foods. 2020;75:104224. https://doi.org/10.1016/j.jff.2020.104224
  67. Wargasetia TL, Widodo. Mechanisms of cancer cell killing by sea cucumber-derived compounds. Invest New Drugs. 2017;35:820-6. https://doi.org/10.1007/s10637-017-0505-5
  68. Weigel BL. Sea cucumber intestinal regeneration reveals deterministic assembly of the gut microbiome. Appl Environ Microbiol. 2020;86:e00489-20. https://doi.org/10.1128/AEM.00489-20
  69. Wu FJ, Xue Y, Liu XF, Xue CH, Wang JF, Du L, et al. The protective effect of eicosapentaenoic acid-enriched phospholipids from sea cucumber Cucumaria frondosa on oxidative stress in PC12 cells and SAMP8 mice. Neurochem Int. 2014;64:9-17. https://doi.org/10.1016/j.neuint.2013.10.015
  70. Xu C, Zhang R, Wen Z. Bioactive compounds and biological functions of sea cucumbers as potential functional foods. J Funct Foods. 2018;49:73-84. https://doi.org/10.1016/j.jff.2018.08.009
  71. Zhang X, Sun L, Yuan J, Sun Y, Gao Y, Zhang L, et al. The sea cucumber genome provides insights into morphological evolution and visceral regeneration. PLOS Biol. 2017;15:e2003790. https://doi.org/10.1371/journal.pbio.2003790