Roles and Biomedical Applications of Haemolymph Lectin

Author(s): Rana Kamei, Oinam S. Devi, Sorokhaibam J. Singh, Senjam S. Singh*

Journal Name: Current Pharmaceutical Biotechnology

Volume 21 , Issue 14 , 2020


Become EABM
Become Reviewer
Call for Editor

Abstract:

Background: Lectins are class of proteins characterized by their ability to selectively bind carbohydrate moieties of glycoproteins. Many invertebrate lectins, especially derived from hemolymph, are being purified, and yet their functions and medical applications are subjects of major interest.

Methods: Hemolymph lectins in invertebrates play a major role in protecting against many pathogens and microbes. Further, many hemolymph lectins show anticancer properties towards various cancer cell lines, which expresses globotriaosyl ceramides on their cell surface.

Results: These vast repertoires of hemolymph lectins in recognizing and inhibiting the growth of various harmful microbes and cancerous cells have spurred the biochemist to use them in histochemical and cytochemical studies.

Conclusion: The present review will address the biological roles and biomedical applications of hemolymph lectin.

Keywords: Haemolymph lectin, cytotoxicity, Mytilec, antibiofilm activity, nanoparticles, hemocytes.

[1]
Drickamer, K. Increasing diversity of animal lectin structures. Curr. Opin. Struct. Biol., 1995, 5(5), 612-616.
[http://dx.doi.org/10.1016/0959-440X(95)80052-2] [PMID: 8574696]
[2]
Lis, H.; Sharon, N. Lectins as molecules and as tools. Annu. Rev. Biochem., 1986, 55, 35-67.
[http://dx.doi.org/10.1146/annurev.bi.55.070186.000343] [PMID: 3527046]
[3]
Feroz Khan, M.I.K. Fungal lectins: Current molecular and biochemical perspectives. Int. J. Biologic. Chem., 2011, 5, 1-20.
[http://dx.doi.org/10.3923/ijbc.2011.1.20]
[4]
Ratcliffe, N.A. Invertebrate immunity-a primer for the non-specialist. Immunol. Lett., 1985, 10(5), 253-270.
[http://dx.doi.org/10.1016/0165-2478(85)90100-2] [PMID: 3930392]
[5]
Maria Risoleta, F.M. Lectins, as non-self-recognition factors, in crustaceans; Elsevier, 2000, 191, pp. 23-44.
[6]
Tatiana Soares, T.H.N.; Felipe, R.B.; Paiva, P.M.G. Hemolymph and hemocytes of Tarantula spiders: Physiological roles and potential as sources of Bioactive molecules. Advances in Animal Science and Zoology; Jenkisn, O.P., Ed.; Nova Science Publishers, Inc.: New York, 2015, Vol. 8, .
[7]
Klowden, M.J. Circulatory system. Physiological Systems in Insects, 2nd ed; Elsevier: Moscow, 2008, p. 357.
[http://dx.doi.org/10.1016/B978-012369493-5.50008-0]
[8]
Wilson, R.; Chen, C.; Ratcliffe, N.A. Innate immunity in insects: The role of multiple, endogenous serum lectins in the recognition of foreign invaders in the cockroach, Blaberus discoidalis. J. Immunol., 1999, 162(3), 1590-1596.
[PMID: 9973417]
[9]
Olafsen, J.A. Lectins: Models of natural and induced molecules in invertebrates.Advances in Comparative and Environmental Physiology; Cooper, E.L., Ed.; Springer: Berlin, Heidelberg, 1996, Vol. 24, pp. 49-76.
[http://dx.doi.org/doi-org-443.webvpn.fjmu.edu.cn/10.1007/978-3-642-79847-4_4, 24, 49-76.]
[10]
Marchialonis, J.J.; Edelman, G.M. Isolation and characterization of a hemagglutinin from Limulus polyphemus. J. Mol. Biol., 1968, 32(2), 453-465.
[http://dx.doi.org/10.1016/0022-2836(68)90022-3] [PMID: 4966872]
[11]
Ravindranath, M.H.; Higa, H.H.; Cooper, E.L.; Paulson, J.C. Purification and characterization of an O-acetylsialic acid-specific lectin from a marine crab Cancer antennarius. J. Biol. Chem., 1985, 260(15), 8850-8856.
[PMID: 4019458]
[12]
Ingram, G.A.; Molyneux, D.H. Insect lectins: Role in parasite-vector interactions. Lectin Rev., 1991, 1, 103-127.
[13]
Ibrahim, E.A.; Ingram, G.A.; Molyneux, D.H. Haemagglutinins and parasite agglutinins in haemolymph and gut of Glossina. Tropenmed. Parasitol., 1984, 35(3), 151-156.
[PMID: 6495384]
[14]
Komano, H.; Mizuno, D.; Natori, S. Purification of lectin induced in the hemolymph of Sarcophaga peregrina larvae on injury. J. Biol. Chem., 1980, 255(7), 2919-2924.
[PMID: 6766942]
[15]
Umetsu, K.; Kosaka, S.; Suzuki, T. Purification and characterization of a lectin from the beetle, Allomyrina dichotoma. J. Biochem., 1984, 95(1), 239-245.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a134590] [PMID: 6423623]
[16]
Hapner, K.D.; Stebbins, M.R. Biochemistry of Arthropod agglutinins.Hemocytic and Humoral Immunity in Arthropods; A.P., Gupta, Ed.; John Wiley and Sons: New York, 1986, pp. 227-250.
[17]
Stebbins, M.R. Preparation and properties of haemagglutinin from haemolymph of acrididae (Grasshoppers). Insect Biochem., 1985, 15(4), 451-462.
[http://dx.doi.org/10.1016/0020-1790(85)90057-5]
[18]
Qu, X.M.; Zhang, C.F.; Komano, H.; Natori, S. Purification of a lectin from the hemolymph of Chinese oak silk moth (Antheraea pernyi) pupae. J. Biochem., 1987, 101(3), 545-551.
[http://dx.doi.org/10.1093/jb/101.3.545] [PMID: 3298221]
[19]
Denis, M.; Thayappan, K.; Ramasamy, S.M.; Munusamy, A. Opsonic function of sialic acid specific lectin in freshwater crab Paratelphusa jacquemontii. Springerplus, 2015, 4, 601.
[http://dx.doi.org/10.1186/s40064-015-1349-0] [PMID: 26543736]
[20]
Chen, S.C.; Yen, C.H.; Yeh, M.S.; Huang, C.J.; Liu, T.Y. Biochemical properties and cDNa cloning of two new lectins from the plasma of Tachypleus tridentatus: Tachypleus plasma lectin 1 and 2+. J. Biol. Chem., 2001, 276(13), 9631-9639.
[http://dx.doi.org/10.1074/jbc.M008414200] [PMID: 11133989]
[21]
Tetreau, G.; Pinaud, S.; Portet, A.; Galinier, R.; Gourbal, B.; Duval, D. Specific pathogen recognition by multiple innate immune sensors in an invertebrate. Front. Immunol., 2017, 8, 1249.
[http://dx.doi.org/10.3389/fimmu.2017.01249] [PMID: 29051762]
[22]
Basu Sarbadhikari, S.; Datta, D.; Bhadra, R. Role of carcinoscorpin, a haemolymph lectin of horseshoe crab Carcinoscorpius rotundacauda as humoral factor. J. Biosci., 1999, 24(4), 471-476.
[http://dx.doi.org/10.1007/BF02942658]
[23]
Sheeja, V. Biological role of the hemolymph lectin of the freshwater crab Travancoriana charu. Int. J. Life Sci. Res., 2019, 7(1), 1-8.
[24]
Majumder, M.; Chattopadhyay, T.; Guha, A.K.; Chatterjee, B.P. Inhibition of bacterial respiration by a low-molecular weight lectin, scyllin, from Scylla serrata crab hemolymph. Indian J. Biochem. Biophys., 1997, 34(1-2), 87-89.
[PMID: 9343934]
[25]
Krishnamoorthi, A.; Shanthi, S.S.G. Antimicrobial activity of lectins isolated from the haemolymph of marine crab. Int. J. Med. Res. Rev., 2016, 4(11), 1350-1352.
[26]
Inamori, K.; Saito, T.; Iwaki, D.; Nagira, T.; Iwanaga, S.; Arisaka, F.; Kawabata, S. A newly identified horseshoe crab lectin with specificity for blood group A antigen recognizes specific O-antigens of bacterial lipopolysaccharides. J. Biol. Chem., 1999, 274(6), 3272-3278.
[http://dx.doi.org/10.1074/jbc.274.6.3272] [PMID: 9920866]
[27]
Chen, C.; Ratcliffe, N.A.; Rowley, A.F. Detection, isolation and characterization of multiple lectins from the haemolymph of the cockroach Blaberus discoidalis. Biochem. J., 1993, 294(Pt 1), 181-190.
[http://dx.doi.org/10.1042/bj2940181] [PMID: 8363570]
[28]
Chen, C.; Durrant, H.J.; Newton, R.P.; Ratcliffe, N.A. A study of novel lectins and their involvement in the activation of the prophenoloxidase system in Blaberus discoidalis. Biochem. J., 1995, 310(Pt 1), 23-31.
[http://dx.doi.org/10.1042/bj3100023] [PMID: 7646450]
[29]
Coombe, D.R.; Ey, P.L.; Schluter, S.F.; Jenkin, C.R. An agglutinin in the haemolymph of an ascidian promoting adhesion of sheep erythrocytes to mouse macrophages. Immunology, 1981, 42(4), 661-669.
[PMID: 7239558]
[30]
Bai, Y.; Niu, D.; Bai, Y.; Li, Y.; Lan, T.; Peng, M.; Dong, Z.; Li, J. Identification of a novel galectin in Sinonovacula constricta and its role in recognition of Gram-negative bacteria. Fish Shellfish Immunol., 2018, 80, 1-9.
[http://dx.doi.org/10.1016/j.fsi.2018.05.041] [PMID: 29807120]
[31]
Alenton, R.R.R.; Koiwai, K.; Nakamura, R.; Thawonsuwan, J.; Kondo, H.; Hirono, I. A Hint of primitive mucosal immunity in shrimp through Marsupenaeus japonicus Gill C-Type lectin. J. Immunol., 2019, 203(8), 2310-2318.
[http://dx.doi.org/10.4049/jimmunol.1900156] [PMID: 31519863]
[32]
Franc, N.C.; White, K. Innate recognition systems in insect immunity and development: New approaches in Drosophila. Microbes Infect., 2000, 2(3), 243-250.
[http://dx.doi.org/10.1016/S1286-4579(00)00304-X] [PMID: 10758400]
[33]
Vasta, G.R.; Cohen, E. Sialic acid-binding lectins in the “whip scorpion” (Mastigoproctus giganteus) serum. J. Invertebr. Pathol., 1984, 43(3), 333-342.
[http://dx.doi.org/10.1016/0022-2011(84)90078-8] [PMID: 6725978]
[34]
Loker, E.S.; Adema, C.M.; Zhang, S.M.; Kepler, T.B. Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol. Rev., 2004, 198, 10-24.
[http://dx.doi.org/10.1111/j.0105-2896.2004.0117.x] [PMID: 15199951]
[35]
Richards, O.W.; Davies, R.G. General Textbook of Entomology, 10th ed; John Wiley & Sons: New York, 1977, Vol. 1, p. 240.
[36]
Frazier, W.A.; Rosen, S.D.; Reitherman, R.W.; Barondes, S.H. Purification and comparison of two developmentally regulated lectins from Dictyostelium discoideum. Discoidin I and II. J. Biol. Chem., 1975, 250(19), 7714-7721.
[PMID: 1236849]
[37]
Suzuki, T.; Natori, S. Identification of a protein having hemagglutinating activity in the hemolymph of the silkworm, Bombyx mori. J. Biochem., 1983, 93(2), 583-590.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a134213] [PMID: 6404903]
[38]
Kawaguchi, N.; Komano, H.; Natori, S. Involvement of Sarcophaga lectin in the development of imaginal discs of Sarcophaga peregrina in an autocrine manner. Dev. Biol., 1991, 144(1), 86-93.
[http://dx.doi.org/10.1016/0012-1606(91)90481-H] [PMID: 1995404]
[39]
Komano, H.; Natori, S. Participation of Sarcophaga peregrina humoral lectin in the lysis of sheep red blood cells injected into the abdominal cavity of larvae. Dev. Comp. Immunol., 1985, 9(1), 31-40.
[http://dx.doi.org/10.1016/0145-305X(85)90057-6] [PMID: 3996706]
[40]
Terada, D.; Kawai, F.; Noguchi, H.; Unzai, S.; Hasan, I.; Fujii, Y.; Park, S.Y.; Ozeki, Y.; Tame, J.R. Crystal structure of MytiLec, a galactose-binding lectin from the mussel Mytilus galloprovincialis with cytotoxicity against certain cancer cell types. Sci. Rep., 2016, 6, 28344.
[http://dx.doi.org/10.1038/srep28344] [PMID: 27321048]
[41]
Fujii, Y.; Dohmae, N.; Takio, K.; Kawsar, S.M.; Matsumoto, R.; Hasan, I.; Koide, Y.; Kanaly, R.A.; Yasumitsu, H.; Ogawa, Y.; Sugawara, S.; Hosono, M.; Nitta, K.; Hamako, J.; Matsui, T.; Ozeki, Y. A lectin from the mussel Mytilus galloprovincialis has a highly novel primary structure and induces glycan-mediated cytotoxicity of globotriaosylceramide-expressing lymphoma cells. J. Biol. Chem., 2012, 287(53), 44772-44783.
[http://dx.doi.org/10.1074/jbc.M112.418012] [PMID: 23093409]
[42]
Gerdol, M.; Venier, P. An updated molecular basis for mussel immunity. Fish Shellfish Immunol., 2015, 46(1), 17-38.
[http://dx.doi.org/10.1016/j.fsi.2015.02.013] [PMID: 25700785]
[43]
Dharmu, I.; Ramamurty, N.; Kannan, R.; Babu, M. Cytotoxic effect of achatinin(H) (lectin) from Achatina fulica against a human mammary carcinoma cell line (MCF7). In Vitro Cell. Dev. Biol. Anim., 2007, 43(8-9), 306-314.
[http://dx.doi.org/10.1007/s11626-007-9055-z] [PMID: 17876678]
[44]
Wang, N.; Whang, I.; Lee, J. A novel C-type lectin from abalone, Haliotis discus, agglutinates Vibrio alginolyticus. Dev. Comp. Immunol., 2008, 32(9), 1034-1040.
[http://dx.doi.org/10.1016/j.dci.2008.02.001] [PMID: 18372041]
[45]
Chatterjee, B.; Ghosh, K.; Yadav, N.; Kanade, S.R. A novel L-fucose-binding lectin from Fenneropenaeus indicus induced cytotoxicity in breast cancer cells. J. Biochem., 2017, 161(1), 87-97.
[http://dx.doi.org/10.1093/jb/mvw057] [PMID: 27742744]
[46]
Jhuma, P.U.C.; Mondal, G.; Campana, P.T.; Chatterjee, B.P. Tn/T Specific agglutinin from Estuarine crab Scylla serrata with potent mitogenic activity on mouse splenocytes and antiproliferative effect on Hepatocellular Carcinoma (HepG2). Cell. Glycobiol. Insights, 2010, 2, 83-99.
[http://dx.doi.org/10.4137/GBI.S4214]
[47]
Itoh, A.; Iizuka, K.; Natori, S. Antitumor effect of Sarcophaga lectin on murine transplanted tumors. Jpn. J. Cancer Res., 1985, 76(10), 1027-1033.
[PMID: 3935621]
[48]
Fujii, Y.; Fujiwara, T.; Koide, Y.; Hasan, I.; Sugawara, S.; Rajia, S.; Kawsar, S.M.; Yamamoto, D.; Araki, D.; Kanaly, R.A.; Ogawa, Y.; Fujita, H.; Ozeki, Y. Internalization of a novel, huge lectin from Ibacus novemdentatus (slipper lobster) induces apoptosis of mammalian cancer cells. Glycoconj. J., 2017, 34(1), 85-94.
[http://dx.doi.org/10.1007/s10719-016-9731-x] [PMID: 27658397]
[49]
Ponraja, T.; Raju, V.M.P.; Vimalaa, K.; Kannanb, S. Protein regulation and Apoptotic induction in human breast carcinoma cells (MCF-7) through lectin from G. beauts. Int. J. Biol. Macromol., 2017, 95, 123-124.
[50]
Chernikov, O.; Kuzmich, A.; Chikalovets, I.; Molchanova, V.; Hua, K.F. Lectin CGL from the sea mussel Crenomytilus grayanus induces Burkitt's lymphoma cells death via interaction with surface glycan. Int. J. Biol. Macromol., 2017, 104(Pt A), 508-514.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.06.074]
[51]
Bishayee, S.; Dorai, D.T. Isolation and characterisation of a sialic acid-binding lectin (carcinoscorpin) from Indian horseshoe crab Carcinoscorpius rotunda cauda. Biochim. Biophys. Acta, 1980, 623(1), 89-97.
[http://dx.doi.org/10.1016/0005-2795(80)90011-2] [PMID: 6155150]
[52]
Na, J.C.; Park, B.T.; Chung, W.H.; Kim, H.H. Molecular characterization and mitogenic activity of a lectin from purse crab philyra pisum. Korean J. Physiol. Pharmacol., 2011, 15(4), 241-244.
[http://dx.doi.org/10.4196/kjpp.2011.15.4.241] [PMID: 21994481]
[53]
Rittidach, W.; Paijit, N.; Utarabhand, P. Purification and characterization of a lectin from the banana shrimp Fenneropenaeus merguiensis hemolymph. Biochim. Biophys. Acta, 2007, 1770(1), 106-114.
[http://dx.doi.org/10.1016/j.bbagen.2006.06.016] [PMID: 16934939]
[54]
Rubeena, A.S.; Preetham, E. Antimicrobial properties and phenoloxidase activation of the lectin isolated from kadal shrimp (Metapenaeus dobsoni). Fish Shellfish Immunol., 2019, 90, 118-125.
[http://dx.doi.org/10.1016/j.fsi.2019.04.305] [PMID: 31054358]
[55]
Davidson, S.K.; Keller, K.F.; Doyle, R.J. Differentiation of coagulase-positive and coagulase-negative staphylococci by lectins and plant agglutinins. J. Clin. Microbiol., 1982, 15(4), 547-553.
[http://dx.doi.org/10.1128/JCM.15.4.547-553.1982] [PMID: 7068834]
[56]
Wang, X.W.; Xu, J.D.; Zhao, X.F.; Vasta, G.R.; Wang, J.X. A shrimp C-type lectin inhibits proliferation of the hemolymph microbiota by maintaining the expression of antimicrobial peptides. J. Biol. Chem., 2014, 289(17), 11779-11790.
[http://dx.doi.org/10.1074/jbc.M114.552307] [PMID: 24619414]
[57]
Jayanthi, S.; Shanthi, S.; Vaseeharan, B.; Gopi, N.; Govindarajan, M.; Alharbi, N.S.; Kadaikunnan, S.; Khaled, J.M.; Benelli, G. Growth inhibition and antibiofilm potential of Ag nanoparticles coated with lectin, an arthropod immune molecule. J. Photochem. Photobiol. B, 2017, 170, 208-216.
[http://dx.doi.org/10.1016/j.jphotobiol.2017.04.011] [PMID: 28441606]
[58]
Barracco, M.A.; Loch, C.T. Naturally occurring lectins in the haemolymph of Panstrongylus megistus (Hemiptera: Reduviidae). Mem. Inst. Oswaldo Cruz, 1988, 83(4), 525-527.
[http://dx.doi.org/10.1590/S0074-02761988000400021] [PMID: 3078352]
[59]
Pereira, M.E.; Andrade, A.F.; Ribeiro, J.M. Lectins of distinct specificity in Rhodnius prolixus interact selectively with Trypanosoma cruzi. Science, 1981, 211(4482), 597-600.
[http://dx.doi.org/10.1126/science.7006082] [PMID: 7006082]
[60]
Gokudan, S.; Muta, T.; Tsuda, R.; Koori, K.; Kawahara, T.; Seki, N.; Mizunoe, Y.; Wai, S.N.; Iwanaga, S.; Kawabata, S. Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc. Natl. Acad. Sci. USA, 1999, 96(18), 10086-10091.
[http://dx.doi.org/10.1073/pnas.96.18.10086] [PMID: 10468566]
[61]
Velayutham, V.; Shanmugavel, S.; Somu, C.; Sundaram, J. Purification, characterization, and analysis of antibacterial activity of a serum lectin from the grub of rhinoceros beetle, Oryctes rhinoceros. Process Biochem., 2017, 53, 1-266.
[62]
Saito, T.; Hatada, M.; Iwanaga, S.; Kawabata, S. A newly identified horseshoe crab lectin with binding specificity to O-antigen of bacterial lipopolysaccharides. J. Biol. Chem., 1997, 272(49), 30703-30708.
[http://dx.doi.org/10.1074/jbc.272.49.30703] [PMID: 9388206]
[63]
Umetsu, K.; Kosaka, S.; Kashimura, S.; Suzuki, T. Studies on anti-B specificity and heterogeneity of some invertebrate hemagglutinins. Tohoku J. Exp. Med., 1979, 129(2), 161-167.
[http://dx.doi.org/10.1620/tjem.129.161] [PMID: 494266]
[64]
Patchell, B.J.; Dorscheid, D.R. Repair of the injury to respiratory epithelial cells characteristic of asthma is stimulated by Allomyrina dichotoma agglutinin specific serum glycoproteins. Clin. Experiment. Allerg., 2006, 36(5), 585-593.
[http://dx.doi.org/10.1111/j.1365-2222.2006.02394.x]
[65]
Abubakar, L.U.; Bulimo, W.D.; Mulaa, F.J.; Osir, E.O. Molecular characterization of a tsetse fly midgut proteolytic lectin that mediates differentiation of African trypanosomes. Insect Biochem. Mol. Biol., 2006, 36(4), 344-352.
[http://dx.doi.org/10.1016/j.ibmb.2006.01.010] [PMID: 16551548]
[66]
Roche, A.C.; Perrodon, Y.; Halpern, B.; Monsigny, M. Limulin (Limulus polyphemus lectin): Mitogenic effect on human peripheral lymphocytes. Eur. J. Immunol., 1977, 7(5), 263-267.
[http://dx.doi.org/10.1002/eji.1830070504] [PMID: 301474]
[67]
Espinosa, B.; Zenteno, R.; Mena, R.; Robitaille, Y.; Zenteno, E.; Guevara, J. O-Glycosylation in sprouting neurons in Alzheimer disease, indicating reactive plasticity. J. Neuropathol. Exp. Neurol., 2001, 60(5), 441-448.
[http://dx.doi.org/10.1093/jnen/60.5.441] [PMID: 11379819]
[68]
Fu, T.K.; Ng, S.K.; Chen, Y.E.; Lee, Y.C.; Demeter, F.; Herczeg, M.; Borbás, A.; Chiu, C.H.; Lan, C.Y.; Chen, C.L.; Chang, M.D. Rhamnose binding protein as an anti-bacterial agent-targeting biofilm of Pseudomonas aeruginosa. Mar. Drugs, 2019, 17(6)E355
[http://dx.doi.org/10.3390/md17060355] [PMID: 31207891]
[69]
Bai, Y.; Niu, D.; Li, Y.; Bai, Y.; Lan, T.; Peng, M.; Dong, Z.; Sun, F.; Li, J. Identification and characterisation of a novel small galectin in razor clam (Sinonovacula constricta) with multiple innate immune functions. Dev. Comp. Immunol., 2019, 93, 11-17.
[http://dx.doi.org/10.1016/j.dci.2018.10.015] [PMID: 30389517]
[70]
Divya, M.; Vaseeharan, B.; Anjugam, M.; Iswarya, A.; Karthikeyan, S.; Velusamy, P.; Govindarajan, M.; Alharbi, N.S.; Kadaikunnan, S.; Khaled, J.M.; Vágvölgyi, C. Phenoloxidase activation, antimicrobial, and antibiofilm properties of β-glucan binding protein from Scylla serrata crab hemolymph. Int. J. Biol. Macromol., 2018, 114, 864-873.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.03.159] [PMID: 29601878]
[71]
Elayabharathi, J.V.J.M.; Mary, S.; Bai, M. Partial purification and characterization of hemolymph lectin of marine crab Atergatis ocyroe by adsorption on formalinized erythrocytes. Int. J. Biol. Res., 2017, 2(4), 115-119.
[72]
Fredrick, W.S.; Ravichandran, S. Hemolymph proteins in marine crustaceans. Asian Pac. J. Trop. Biomed., 2012, 2(6), 496-502.
[http://dx.doi.org/10.1016/S2221-1691(12)60084-7] [PMID: 23569958]
[73]
Zhen, X. Reproductive performance and offspring quality of wild-caught and pond-reared swimming crab Portunus trituberculatus broodstock. Aquaculture, 2010, 301(1/4), 78-84.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 14
Year: 2020
Published on: 07 December, 2020
Page: [1444 - 1450]
Pages: 7
DOI: 10.2174/1389201021666200730123330
Price: $65

Article Metrics

PDF: 22
HTML: 1