E-ISSN 2578-7322
 

Original Research 


Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu.

Cited by (1)

Abstract
Objective: In this study, we hypothesized that endotoxin-induced protein coagulation in the snail is mediated by lectins and serine proteases.
Methods: Experiments were carried out to determine the lectin activities of the hemolymph fractions and those of their coagulates and supernatants. The plasma was also exposed to 5000 EU/ml endotoxin, incubated for 1 h at 37 °C and the supernatant’s protein profile was compared on SDS-PAGE to a non-treated plasma. In addition, LPS-agarose was used as an affinity column to isolate lipopolysaccharide binding protein(s). Eluted proteins were subjected to SDS-PAGE, mass spectrometry and proteomic analysis. Finally, endotoxin-induced coagulation was tested for Ca2+ ion- and serine protease-dependence.
Results: Results from this study indicated that lectins were involved in the coagulation process induced by endotoxin. There was a loss in total lectin actvity from the plasma fraction on exposure to endotoxin. Several mono- and dissaccharides inhibited the agglutination of the reconstituted lyophilized plasma by rabbit erythrocytes, indicating the possible presence of several types of lectins in the plasma. Endotoxin-absorbed plasma resulted in a reduction of proteins in the >250 kDa range, ~66 kDa and a 37 kDa protein based on SDS-PAGE analysis. Excision of those bands and subsequent proteomic analyses predicted the presence of hemocyanin (389-394 kDa), an allergen (69 kDa) and a Gram-negative binding protein (50 kDa). Endotoxin-induced protein coagulation was inhibited by a trypsin protease inhbitor. No coagulaton was detected in the absence of Ca2+ ion.
Conclusions: From these results, we conclude that endotoxin-induced protein coagulation in Archachatina marginata hemolymph is lectin and serine protease-mediated and Ca2+ ion dependent.

Key words: Agglutinins (lectins); Archachatina marginata; hemolymph coagulation; endotoxin; innate immunity; hemocyanin; serine proteases.


 
ARTICLE TOOLS
Abstract
PDF Fulltext
Print this article Print this Article
How to cite this articleHow to cite this article
Citation Tools
Related Records
 Articles by Musa Oyewole Salawu
Articles by Timothy Yoshino
Articles by Hussein Oyelola Bukoye Oloyede
Articles by Adenike Kuku
Articles by Mikail Olugbemiro Nafiu
Articles by Laura Gonzalez
Articles by Xiao Jun Wu
on Google
on Google Scholar
Article Statistics
 Viewed: 2453
Downloaded: 622
Cited: 1

REFERENCES
1. Vazquez L, Alpuche J, Maldonado G, Agundis C, Pereyra-Morales A, Zenteno E. Review: Immunity mechanisms in crustaceans. Innate Immun. 2009;15:179-88. [DOI via Crossref]    [Pubmed]   
2. Iwanaga S. The limulus clotting reaction. Curr Opin Immunol. 1993;5:74-82. [DOI via Crossref]   
3. Kawabata S, Tokunaga F, Kugi Y, Motoyama S, Miura Y, Hirata M, Iwanaga S. Limulus factor D, a 43-kDa protein isolated from horseshoe crab hemocytes, is a serine protease homologue with antimicrobial activity. FEBS Lett. 1996;398:146-50. [DOI via Crossref]   
4. Tamura H, Tanaka S, Oda T, Uemura Y, Aketagawa J, Hashimoto Y. Purification and characterization of a (1-->3)-beta-D-glucan-binding protein from horseshoe crab (Tachypleus tridentatus) amoebocytes. Carbohydr Res. 1996;295:103-16. [Pubmed]   
5. Kopácek P, Hall M, Söderhäll K. Characterization of a clotting protein, isolated from plasma of the freshwater crayfish Pacifastacus leniusculus. Eur J Biochem. 1993;213:591-7. [DOI via Crossref]    [Pubmed]   
6. Cerenius L, Liang Z, Duvic B, Keyser P, Hellman U, Palva ET, Iwanaga S, Söderhäll K. Structure and biological activity of a 1,3-beta-D-glucan-binding protein in crustacean blood. J Biol Chem. 1994;269:29462-7. [Pubmed]   
7. Vázquez L, Maldonado G, Agundis C, PĂ©rez A, Cooper EL, Zenteno E. Participation of a sialic acid-specific lectin from freshwater prawn Macrobrachium rosenbergii hemocytes in the recognition of non-self cells. J Exp Zool. 1997;279:265-72. [DOI via Crossref]   
8. Lee SY, Söderhäll K. Characterization of a pattern recognition protein, a masquerade-like protein, in the freshwater crayfish Pacifastacus leniusculus. J Immunol. 2001;166:7319-26. [Pubmed]   
9. Pereyra A, Agundis C, Barrera B, Alpuche J, Sierra C, Zenteno R, Zenteno E, Vazquez L. The use of monoclonal antibodies anti-lectin from freshwater prawn Macrobrachium rosenbergii (DeMan, 1879) in the recognition of protein with lectin activity in Decapod's hemolymph. Prep Biochem Biotechnol. 2009;39:308-22. [DOI via Crossref]    [Pubmed]   
10. Söderhäll K, Cerenius L. Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol. 1998;10:23-8. [DOI via Crossref]   
11. Salawu MO, Oloyede OB, Oladiji AT, Muhammad NO, Yakubu MT. Effect of Escherichia coli endotoxin on Archachatina marginata hemolymph coagulation system. Pharm Biol. 2011;49:1029-33. [DOI via Crossref]    [Pubmed]   
12. Ogunsanmi AO, Taiwo VO, Akintomide T.O. Haemolymph biochemical parameters of the African giant snail (Achatina achatina) and the big black snail (Achachatina marginata). Trop Vet. 2003;21:43-8. [DOI via Crossref]   
13.Radakrishna ST. (2010): Rabbit Pyrogen test; USP 29-NF24 page 2546; available online at http://www.pharmacopeia.cn/v29240/usp29nf24s0_c151.html.
14. Goldstein IJ, Hayes CE. The lectins: carbohydrate-binding proteins of plants and animals. Adv Carbohydr Chem Biochem. 1978;35:127-340. [DOI via Crossref]   
15. Kuku A, Odekanyin O, Adeniran K, Adewusi M, Olonade T. Purification of a mannose/glucose-specific lectin with antifungal activity from pepper seeds (Capsicum annum). Afr J Biochem Res. 2009;3:272-8.
16. Fox J, Hechemy K. Coupling of Escherichia coli lipopolysaccharide to epoxy-activated Sepharose 6B. Infect Immun. 1978;20:867-8. [Pubmed]    [PMC Free Fulltext]   
17. Charalambidis ND, Foukas LC, Zervas CG, Marmaras VJ. Hemocyte surface phenoloxidase (PO) and immune response to lipopolysaccharide (LPS) in Ceratitis capitata. Insect Biochem Mol Biol. 1996;26:867-74. [DOI via Crossref]   
18. Durliat, M. Clotting processes in Crustacea Decapoda. Biol Rev. 1985;60:473-98. [DOI via Crossref]   
19. Salawu MO, Oloyede OB. Endotoxin-induced coagulation reactions and phenoloxidase activity modulation in Sudanonautes africanus hemolymph fractions. J Immunotoxicol. 2011;8:324-32. [DOI via Crossref]    [Pubmed]   
20. Silveira RL, Andrade SS, Schmidt CA, Casali RG, Dalmora SL. Comparative evaluation of pyrogens tests in pharmaceutical products. Braz J Microbiol. 2004;35:48-53. [DOI via Crossref]   
21. The European Pharmacopoeia. Bacterial endotoxins. 2005:5.0;158-64.
22. Cummings RD, Etzler ME. R-type Lectins. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of Glycobiology. 2nd edition. 2009. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.

This Article Cited By the following articles

Diverse immune functions of hemocyanins
Developmental & Comparative Immunology 2014; 45(1): 43.

1
 
How to Cite this Article
Pubmed Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu. Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph. A J Physiol Biochem Pharmacol. 2013; 2(2): 115-126. doi:10.5455/jib.20130508070229


Web Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu. Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph. http://www.ajpbp.com/?mno=35922 [Access: November 18, 2018]. doi:10.5455/jib.20130508070229


AMA (American Medical Association) Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu. Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph. A J Physiol Biochem Pharmacol. 2013; 2(2): 115-126. doi:10.5455/jib.20130508070229



Vancouver/ICMJE Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu. Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph. A J Physiol Biochem Pharmacol. (2013), [cited November 18, 2018]; 2(2): 115-126. doi:10.5455/jib.20130508070229



Harvard Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu (2013) Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph. A J Physiol Biochem Pharmacol, 2 (2), 115-126. doi:10.5455/jib.20130508070229



Turabian Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu. 2013. Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph. American Journal of Physiology, Biochemistry and Pharmacology, 2 (2), 115-126. doi:10.5455/jib.20130508070229



Chicago Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu. "Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph." American Journal of Physiology, Biochemistry and Pharmacology 2 (2013), 115-126. doi:10.5455/jib.20130508070229



MLA (The Modern Language Association) Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu. "Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph." American Journal of Physiology, Biochemistry and Pharmacology 2.2 (2013), 115-126. Print. doi:10.5455/jib.20130508070229



APA (American Psychological Association) Style

Musa Oyewole Salawu, Timothy Yoshino, Hussein Oyelola Bukoye Oloyede, Adenike Kuku, Mikail Olugbemiro Nafiu, Laura Gonzalez, Xiao Jun Wu (2013) Role of serine proteases and agglutinins in the endotoxin-induced protein coagulation in Archachatina marginata hemolymph. American Journal of Physiology, Biochemistry and Pharmacology, 2 (2), 115-126. doi:10.5455/jib.20130508070229





Most Viewed Articles
  • Slippery Elm, its Biochemistry, and use as a Complementary and Alternative Treatment for Laryngeal Irritation
    Christopher R Watts, Bernard rousseau
    J Investig Biochem. 2012; 1(1): 17-23
    » Abstract & References » doi: 10.5455/jib.20120417052415

  • Selected disease fundamentals based on the unified cell bioenergetics
    Andrzej Kasperski, Renata Kasperska
    J Investig Biochem. 2013; 2(2): 93-100
    » Abstract & References » doi: 10.5455/jib.20130227041230

  • Prevalence of vitamin B12 deficiency in Helicobacter pylori infected patients in Jordan.
    Saad Abed Aljalil Alfawaeir, Mohammad Basim Abuzaid
    J Investig Biochem. 2013; 2(1): 21-25
    » Abstract & References » doi: 10.5455/jib.20121215061954

  • Serum levels of high-sensitivity C-reactive protein (hs-CRP) in Helicobacter pylori infected patients
    Saad Al-Fawaeir, Mohammad Basim Abu Zaid
    J Investig Biochem. 2013; 2(1): 32-36
    » Abstract & References » doi: 10.5455/jib.20121225015606

  • Molecular Characterization of Alpha and Beta Thalassemia in Yemeni Sickle Cell Disease Children
    Saeed Thabet Nasher, Mohammed Wael Abu Ghoush
    J Investig Biochem. 2013; 2(1): 44-52
    » Abstract & References » doi: 10.5455/jib.20130105022014

  • Hepatoprotective and In vivo Anti-oxidant Activity of Costus afer Leaf Extracts against Acetaminophen-Induced Hepatotoxicity in Rats
    God'swill Nduka Anyasor, Kofoworola O. Odunsanya, Audrey C. Ibeneme
    J Investig Biochem. 2013; 2(1): 53-61
    » Abstract & References » doi: 10.5455/jib.20130301030851

  • Correlation Between Elevated Hepatic Enzymes & High-Sensitivity Crp in Metabolic Syndrome.
    Al-Rubaye Faisal, Shakir Mahmood, Jumah Kadhum
    J Investig Biochem. 2012; 1(1): 6-11
    » Abstract & References » doi: 10.5455/jib.20120528094732

  • Serum Lipid Profile of Breast Cancer Patients in Kashmir
    Showkat Ahmad Bhat, Manzoor R Mir, Sabhiya Majid, Ahmad Arif Reshi, Ishraq Husain, Tehseen Hassan, Hilal Ahmad
    J Investig Biochem. 2013; 2(1): 26-31
    » Abstract & References » doi: 10.5455/jib.20121125075314

  • Alteration of antioxidant enzymes and oxidative stress in elderly patient.
    Seema L. Jawalekar1, Anil K. Bhutey2, Aarti Karnik3, Vasant T. Surve4
    J Investig Biochem. 2013; 2(1): 37-43
    » Abstract & References » doi: 10.5455/jib.20130129093838

  • Potential Role of Oxidized LDL (ox-LDL) and Adhesion Molecules (VCAM-1, ICAM-1) in Type 2 Diabetes Mellitus Patients in Qassim region, KSA
    Manal Basyouni, Maha Ahmed, Hisham Ismail , Iman Esmat
    J Investig Biochem. 2012; 1(1): 48-54
    » Abstract & References » doi: 10.5455/jib.20120417052458

  • Most Downloaded
  • Slippery Elm, its Biochemistry, and use as a Complementary and Alternative Treatment for Laryngeal Irritation
    Christopher R Watts, Bernard rousseau
    J Investig Biochem. 2012; 1(1): 17-23
    » Abstract & References » doi: 10.5455/jib.20120417052415

  • Selected disease fundamentals based on the unified cell bioenergetics
    Andrzej Kasperski, Renata Kasperska
    J Investig Biochem. 2013; 2(2): 93-100
    » Abstract & References » doi: 10.5455/jib.20130227041230

  • Serum levels of high-sensitivity C-reactive protein (hs-CRP) in Helicobacter pylori infected patients
    Saad Al-Fawaeir, Mohammad Basim Abu Zaid
    J Investig Biochem. 2013; 2(1): 32-36
    » Abstract & References » doi: 10.5455/jib.20121225015606

  • Alteration of antioxidant enzymes and oxidative stress in elderly patient.
    Seema L. Jawalekar1, Anil K. Bhutey2, Aarti Karnik3, Vasant T. Surve4
    J Investig Biochem. 2013; 2(1): 37-43
    » Abstract & References » doi: 10.5455/jib.20130129093838

  • Serum Lipid Profile of Breast Cancer Patients in Kashmir
    Showkat Ahmad Bhat, Manzoor R Mir, Sabhiya Majid, Ahmad Arif Reshi, Ishraq Husain, Tehseen Hassan, Hilal Ahmad
    J Investig Biochem. 2013; 2(1): 26-31
    » Abstract & References » doi: 10.5455/jib.20121125075314

  • Hepatoprotective and In vivo Anti-oxidant Activity of Costus afer Leaf Extracts against Acetaminophen-Induced Hepatotoxicity in Rats
    God'swill Nduka Anyasor, Kofoworola O. Odunsanya, Audrey C. Ibeneme
    J Investig Biochem. 2013; 2(1): 53-61
    » Abstract & References » doi: 10.5455/jib.20130301030851

  • Evaluation of glycated albumin and microalbuminuria as early risk markers of nephropathy in type 2 diabetes mellitus
    Suresh Babu Kondaveeti, Ivvala Anand Shaker
    J Investig Biochem. 2013; 2(2): 127-131
    » Abstract & References » doi: 10.5455/jib.20130507061739

  • Comparative study of ischemia modified albumin and nitric oxide in hyperthyroidism
    Monica Verma1, Kiran Dahiya1, Veena Singh Ghalaut1, Abhishek Soni2, Jagjeet Singh3, Vasudha Dhupper1
    J Investig Biochem. 2014; 3(1): 17-20
    » Abstract & References » doi: 10.5455/jib.20130707090209

  • Prevalence of vitamin B12 deficiency in Helicobacter pylori infected patients in Jordan.
    Saad Abed Aljalil Alfawaeir, Mohammad Basim Abuzaid
    J Investig Biochem. 2013; 2(1): 21-25
    » Abstract & References » doi: 10.5455/jib.20121215061954

  • Serum lipid profile in Helicobacter pylori infected patients
    Saad Al-Fawaeir, Mohammad Abu Zaid, Ayman Abu Awad, Baker Alabedallat
    J Investig Biochem. 2013; 2(2): 132-135
    » Abstract & References » doi: 10.5455/jib.20130603084538

  • Most Cited Articles
  • Biochemical study on the impact of Nigella sativa and virgin olive oils on cadmium-induced nephrotoxicity and neurotoxicity in rats
    Eman Taha Mohammed, Khalid Shaban Hashem, Mahmoud Ramadan Abdel Rheim
    J Investig Biochem. 2014; 3(2): 71-78
    » Abstract & References » doi: 10.5455/jib.20140716041908
    Cited : 6 times [Click to see citing articles]

  • Study and Characterization of the Antioxidant Activity of the Inclusion Complex of Apigenin with β-Cyclodextrin and HP-β-Cyclodextrin in solution
    Jinxia Li
    J Investig Biochem. 2014; 3(3): 107-111
    » Abstract & References » doi: 10.5455/jib.20140905032504
    Cited : 5 times [Click to see citing articles]

  • Slippery Elm, its Biochemistry, and use as a Complementary and Alternative Treatment for Laryngeal Irritation
    Christopher R Watts, Bernard rousseau
    J Investig Biochem. 2012; 1(1): 17-23
    » Abstract & References » doi: 10.5455/jib.20120417052415
    Cited : 4 times [Click to see citing articles]

  • Alterations in plasma lipids, glutathione and homocysteine in relation to dietary copper in rats
    Magda A. Megahed1, Kamel M. A. Hassanin2, Ibrahim M. I. Youssef3, Abdul Baset A. Elfghi4, Kamal A. Amin2
    J Investig Biochem. 2014; 3(1): 21-25
    » Abstract & References » doi: 10.5455/jib.20130716075753
    Cited : 4 times [Click to see citing articles]

  • Quercetin, a natural phytochemical and antioxidant protects against sodium azide-induced hepatic and splenic oxidative stress in rats
    Oluwatobi Temitope Somade, Oluseyi Adeboye Akinloye, Michael Oluwayemi Adeyeye, Gbenga Daniel Fabunmi, Olakunle Opeoluwa Idowu, Funmilayo Oluwaseun Badmus, Barakat Oluwatoyin Salaudeen
    J Investig Biochem. 2015; 4(3): 69-74
    » Abstract & References » doi: 10.5455/jib.20151220014400
    Cited : 3 times [Click to see citing articles]

  • A New Marker For The Diagnosýs Of Sepsis: Presepsin
    Mehmet Agilli, Irfan Sener, Fatih Yesildal, Tevfik Honca, Ibrahim Aydin, Emin Ozgur Akgul, Halil Yaman
    J Investig Biochem. 2012; 1(1): 55-57
    » Abstract & References » doi: 10.5455/jib.20120521073837
    Cited : 3 times [Click to see citing articles]

  • The role of urinary 5- hydroxyindoleacetic acid determination in diagnosis of acute appendicitis
    Hamid Hindi Sarhan, Aseel Fawzi Hatroosh, Amina Hamed Alobaidi
    J Investig Biochem. 2013; 2(1): 1-5
    » Abstract & References » doi: 10.5455/jib.20121026084836
    Cited : 3 times [Click to see citing articles]

  • Serum Lipid Profile of Breast Cancer Patients in Kashmir
    Showkat Ahmad Bhat, Manzoor R Mir, Sabhiya Majid, Ahmad Arif Reshi, Ishraq Husain, Tehseen Hassan, Hilal Ahmad
    J Investig Biochem. 2013; 2(1): 26-31
    » Abstract & References » doi: 10.5455/jib.20121125075314
    Cited : 3 times [Click to see citing articles]

  • Phytochemical content of Cnidoscolus aconitifolius leaves and toxicological effect of its aqueous leaf extract in Wistar rats
    Doris Akachukwu, Polycarp Nnacheta Okafor, Chiedozie O Ibegbulem
    J Investig Biochem. 2014; 3(1): 26-31
    » Abstract & References » doi: 10.5455/jib.20140504023102
    Cited : 3 times [Click to see citing articles]

  • Myeloperoxidase, Malondialdehyde and serum Lipids in type 2 diabetes mellitus
    Mohamedi Begum, Ashok Kumar J., Hilda Priya D'Souza, Sushith Sushith, Prathima M.B, Reshma S., Shashikala M.D, Manjula Anil, Suriyan S Nair, Kavitha Ashok Kumar
    J Investig Biochem. 2015; 4(1): 13-17
    » Abstract & References » doi: 10.5455/jib.20150331115356
    Cited : 3 times [Click to see citing articles]