This review focuses on biologically active entities from invertebrate sources, especially snails. The reader will encounter several categories of compounds from snails including glycosaminoglycans, peptides, proteins (glycoproteins), and enzymes which possess diverse biological activities. Among glycosaminoglycans, acharan sulfate which was isolated from a giant African snail Acahtina fulica is reviewed extensively. Conotoxins which are also called conopeptides are unique peptide mixtures from marine cone snail. Conotoxins are secreted to capture its prey, and currently have the potential to be highly effective drug candidates. One of the conotoxins is now in the market as a pain killer. Proteins as well as glycoproteins in the snail are known to be involved in the host defense process from an attack of diverse pathogens. Carbohydrate-degrading enzymes characterized and purified in snails are introduced to give an insight into the applicability in glycobiology research such as synthesis and structure characterization of glycoconjugates. It seems that simple snails produce very complicated biological compounds which could be an invaluable source in future therapeutics as well as research areas in natural medicine.
HardinghamTE, FosangAJ. (1992) Proteoglycans: many forms and many functions. The Journal of the Federation of American Societies for Experimental Biology, 6, 861–870.
2.
LaremoreTN, ZhangF, DordickJS, LiuJ, LinhardtRJ. (2009) Recent progress and applications in glycosaminoglycan and heparin research. Current Opinion in Chemical Biology, 13, 633–640.
3.
HovinghP, PiepkornM, LinkerA. (1986) Biological implications of the structural, antithrombin affinity and anticoagulant activity relationships among vertebrate heparins and heparan sulphates. Biochemical Journal, 237, 573–581.
4.
NaderNB, DietrichCP. (1989) in Heparin Chemical and Biological Properties Clinical Applications (LaneDA, LindahlU, eds.) pp 81-96, CRC Press, Boca Raton.
5.
FrommhagenLH, FahrenbachMJ, BrockmanJJ. (1953) Heparin-like anticoagulants from mollusca. Proceedings of the Society for Experimental Biology and Medicine, 82, 280–283.
6.
KimYS, JoYY, ChangIM, ToidaT, ParkY, LinhardtRJ. (1996) A new glycosaminoglycan from the giant African snail Achatina fulica. Journal of Biological Chemistry, 271, 11750–11755.
7.
KimYS, AhnMY, WuSJ, KimDH, ToidaT, TeeschLM, ParkY, YuG, LinJ, LinhardtRJ. (1998) Determination of the structure of oligosaccharides prepared from acharan sulfate. Glycobiology, 8, 869–877.
8.
ChiL, MunozEM, ChoiHS, HaYW, KimYS, ToidaT, LinhardtRJ. (2006) Preparation and structural determination of large oligosaccharides derived from acharan sulfate. Carbohydrate Research, 341, 864–869.
9.
JeongJ, ToidaT, MunetaY, KosiishiI, ImanariT, LinhardtRJ, ChoiHS, WuSJ, KimYS. (2001) Localization and characterization of acharan sulfate in the body of the giant African snail Achatina fulica. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 130, 513–519.
10.
VieiraTC, Costa-FilhoA, SalgadoNC, AllodiS, ValenteAP, NasciuttiLE, SilvaLC. (2004) Acharan sulfate, the new glycosaminoglycan from Achatina fulica Bowdich 1822. Structural heterogeneity, metabolic labeling and localization in the body, mucus and the organic shell matrix. European Journal of Biochemistry, 271, 845–854.
11.
ParkY, ZhangZ, LaremoreTN, LiB, SimJS, ImAR, AhnMY, KimYS, LinhardtRJ. (2008) Variation of acharan sulfate and monosaccharide composition and analysis of neutral N-glycans in African giant snail (Achatina fulica). Glycoconjugate Journal, 25, 863–877.
12.
ParkY, LeeIS, JooEJ, HahnBS, KimYS. (2009) A novel and one-step purification of human ceruloplasmin by acharan sulfate affinity chromatography. Archives of Pharmacal Research, 32, 693–698.
13.
WuSJ, ChunMW, ShinKH, ToidaT, ParkY, LinhardtRJ, KimYS. (1998) Chemical sulfonation and anticoagulant activity of acharan sulfate. Thrombosis Research, 92, 273–281.
14.
LiDW, LeeIS, SimJS, ToidaT, LinhardtRJ, KimYS. (2004) Long duration of anticoagulant activity and protective effects of acharan sulfate in vivo. Thrombosis Research, 113, 67–73.
15.
WangH, ToidaT, KimYS, CapilaI, HilemanRE, BernfieldM, LinhardtRJ. (1997) Glycosaminoglycans can influence fibroblast growth factor-2 mitogenicity without significant growth factor binding. Biochemical and Biophysical Research Communications, 235, 369–373.
16.
GargHG, JosephPA, ThompsonBT, HalesCA, ToidaT, ImanariT, CapilaI, LinhardtRJ. (1999) Effect of fully sulfated glycosaminoglycans on pulmonary artery smooth muscle cell proliferation. Archives of Biochemistry and Biophysics, 371, 228–233.
17.
GhoshAK, HirasawaN, LeeYS, KimYS, ShinKH, RyuN, OhuchiK. (2002) Inhibition by acharan sulphate of angiogenesis in experimental inflammation models. British Journal of Pharmacology, 137, 441–448.
18.
ShimJY, LeeYS, JungSH, ChoiHS, ShinKH, KimYS. (2002) Pharmacological activities of a new glycosaminoglycan, acharan sulfate isolated from the giant African snail Achatina fulica. Archives of Pharmacal Research, 25, 889–894.
19.
LeeYS, YangHO, ShinKH, ChoiHS, JungSH, KimYM, OhDK, LinhardtRJ, KimYS. (2003) Suppression of tumor growth by a new glycosaminoglycan isolated from the African giant snail Achatina fulica. European Journal of Pharmacology, 28, 191–198.
20.
JooEJ, ten DamGB, van KuppeveltTH, ToidaT, LinhardtRJ, KimYS. (2005) Nucleolin: acharan sulfate-binding protein on the surface of cancer cells. Glycobiology, 15, 1–9.
21.
JooEJ, YangH, ParkY, ParkNY, ToidaT, LinhardtRJ, KimYS. (2010) Induction of nucleolin translocation by acharan sulfate in A549 human lung adenocarcinoma. Journal of Cellular Biochemistry, 110, 1272–1278.
ArmishawCJ, AlewoodPF. (2005) Conotoxins as research tools and drug leads. Currunt Protein and Peptide Science, 6, 221–240.
24.
EkbergJ, CraikDJ, AdamsDJ. (2008) Conotoxin modulation of voltage-gated sodium channels. International Journal of Biochemistry & Cell Biology, 40, 2363–2368.
25.
OliveraBM, TeichertRW. (2007) Diversity of the neurotoxic Conus peptides: a model for concerted pharmacological discovery. Molecular Interventions, 7, 251–260.
26.
LewisRJ. (2009) Conotoxin venom peptide therapeutics. Advances in Experimental Medicine and Biology, 655, 44–48.
HanTS, TeichertRW, OliveraBM, BulajG. (2008) Conus venoms - a rich source of peptide-based therapeutics. Current Pharmaceutical Design, 14, 2462–2479.
29.
TwedeVD, MiljanichG, OliveraBM, BulajG. (2009) Neuroprotective and cardioprotective conopeptides: an emerging class of drug leads. Current Opinion in Drug Discovery & Development, 12, 231–239.
30.
CraikDJ, AdamsDJ. (2007) Chemical modification of conotoxins to improve stability and activity. ACS Chemical Biology, 2, 457–468.
31.
BeckerS, TerlauH. (2008) Toxins from cone snails: properties, applications and biotechnological production. Applied Microbiology and Biotechnology, 79, 1–9.
32.
ChenYH, LinPL, HsuHY, WuYT, YangHY, LuDY, HuangSS, HsiehCL, LinJG. (2010) Action potential bursts in central snail neurons elicited by paeonol: roles of ionic currents. Acta Pharmacologica Sinica, 31, 1553–1563.
33.
BinghamJP, MitsunagaE, BergeronZL. (2010) Drugs from slugs–past, present and future perspectives of omega-conotoxin research. Chemico- Biological Interactions, 183, 1–18.
34.
BuczekO, BulajG, OliveraBM. (2005) Conotoxins and the posttranslational modification of secreted gene products. Cellular and Molecular Life Science, 62, 3067–3079.
35.
AzamL, McIntoshJM. (2009) Alpha-conotoxins as pharmacological probes of nicotinic acetylcholine receptors. Acta Pharmacologica Sinica, 30, 771–783.
36.
BasuS, SarkarM, MandalC. (1986) A single step purification of a sialic acid binding lectin (AchatininH) from Achatina fulica snail. Molecular Cellular Biochemistry, 71, 149–157.
37.
BrossmerR, WagnerM, FischerE. (1992) Specificity of the sialic acid-binding lectin from the snail Cepaea hortensis. Journal of Biological Chemistry, 267, 8752–8756.
38.
WagnerM. (1982) Agglutination of bacteria by a sialic acid-specific lectin of the snail Cepaea hortensis. Acta Histochemica, 71, 35–39.
39.
GerlachD, SchlottB, ZahringerU, SchmidtKH. (2005) N-acetyl-D-galactosamine/N-acetyl-D-glucosamine–recognizing lectin from the snail Cepaea hortensis: purification, chemical characterization, cloning and expression in E. coli. FEMS Immunology and Medical Microbiology, 43, 223–232.
40.
ItoS, ShimizuM, NagatsukaM, KitajimaS, HondaM, TsuchiyaT, KanzawaN. (2011) High molecular weight lectin isolated from the mucus of the giant African snail Achatina fulica. Bioscience, Biotechnology, and Biochemistry, 75, 20–25.
41.
IguchiSM, AikawaT, MatsumotoJJ. (1982) Antibacterial activity of snail mucus mucin. Comparative Biochemistry and Physiology Part A: Physiology, 72, 571–574.
42.
KubotaY, WatanabeY, OtsukaH, TamiyaT, TsuchiyaT, MatsumotoJJ. (1985) Purification and characterization of an antibacterial factor from snail mucus. Comparative Biochemistry and Physiology Part C, 82, 345–348.
43.
ObaraK, Otsuka-FuchinoH, SattayasaiN, NonomuraY, TsuchiyaT, TamiyaT. (1992) Molecular cloning of the antibacterial protein of the giant African snail, Achatina fulica Ferussac. European Journal of Biochemistry, 209, 1–6.
44.
HaningtonPC, ForysMA, DragooJW, ZhangSM, AdemaCM, LokerES. (2010) Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proceedings of National Academy of Science of the United States of America, 107, 21087–21092.
45.
ZhangSM, ZengY, LokerES. (2008) Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Journal of Innate Immunity, 14, 175–189.
46.
CharrierM, RoulandC. (2001) Mannan-degrading enzymes purified from the crop of the brown garden snail Helix aspersa Muller (Gastropoda Pulmonata). Journal of Experimental Zoology, 290, 125–135.
47.
YamauraI, MatsumotoT. (1993) Purification and some properties of endo-1,4-beta-D-mannanase from a mud snail, Pomacea insularus (de Ordigny). Bioscience, Biotechnology, and Biochemistry, 57, 1316–1319.
48.
HirataK, AsoY, IshiguroM. (1998) Properties of alpha-mannosidase partially purified from the apple snail, Pomacea canaliculata. Bioscience, Biotechnology, and Biochemistry, 62, 2242–2245.
49.
McClearyBV. (1983) beta-D-Mannosidase from Helix pomatia. Carbohydrate Research, 111, 297–310.
50.
SugaharaK, OkumuraT, YamashinaI. (1972) Purification of -mannosidase from a snail, Achatina fulica, and its action on glycopeptides. Biochimica et Biophysica Acta, 268, 488–496.
51.
LeparouxS, PadrinesM, PlacierG, ColasB. (1997) Characterization of a strictly specific acid beta-galactosidase from Achatina achatina. Biochimica et Biophysica Acta, 1336, 522–532.
52.
TengY, YinQ, dingM, ZhaoF. (2010) Purification and characterization of a novel endo-beta-1,4-glucanases, AfEG22, from the giant snail, Achatina fulica frussac. Acta Biochimica et Biophysica Sinica (Shanghai), 42, 729–734.
53.
PesentsevaMS, KusaykinMI, AnastyukSD, SovaVV, ZvyagintsevaTN. (2008) Catalytic properties and mode of action of endo-(1->3)-beta-D-glucanase and beta-D-glucosidase from the marine mollusk Littorina kurila. Carbohydrate Research, 343, 2393–2400.
54.
UmezurikeGM. (1976) The beta-glucosidase in the gut contents of the snail Achatina achatina. Biochemical Journal, 157, 381–387.
55.
MarshallJJ. (1975) Degradation of barley glucan by a purified (1→4)-beta-d-glucanase from the snail, Helix pomatia. Carbohydrate Research, 42, 203–207.
56.
MarshallJJ, GrandRJ. (1975) Comparative studies on beta-glucan hydrolases. Isolation and characterization of an exo(1→3)-beta-glucanase from the snail, Helix pomatia. Archives of Biochemistry and Biophysics, 167, 165–175.
57.
MaedaI, ShimohigashiY, KiharaH, OhnoM. (1996) Purification and characterization of a cellulase from the giant snail Achatina fulica. Bioscience, Biotechnology, and Biochemistry, 60, 122–124.
58.
GuoR, DingM, ZhangSL, XuGJ, ZhaoFK. (2008) Molecular cloning and characterization of two novel cellulase genes from the mollusc Ampullaria crossean. Journal of Comparative Physiology B, 178, 209–215.
59.
ImjongjirakC, AmparyupP, SittipraneedS. (2008) Cloning, genomic organization and expression of two glycosyl hydrolase family 10 (GHF10) genes from golden apple snail (Pomacea canaliculata). DNA Sequence, 19, 224–236.
60.
HirataK, NakaharaY, KimuraY, FunatsuG. (1996) Purification and some properties of a beta-xylosidase and an alpha-fucosidase from apple snails (Pomacea canaliculata). Bioscience, Biotechnology, and Biochemistry, 60, 249–254.
61.
EndoT, TsukadaT, HiraiwaM, UdaY, KobataA. (1993) Purification and characterization of an alpha-L-fucosidase from Pomacea canaliculata. Archives of Biochemistry and Biophysics, 302, 152–160.
62.
ColasB. (1980) Kinetic studies on beta-fucosidases of Achatina balteata. Biochimica et Biophysica Acta, 613, 448–458.
63.
BrettingH, JacobsG, MullerS, BreitfeldO. (1991) The galactan-degrading enzymes in the snail Biomphalaria glabrata. Comparative Biochemistry and Physiology Part B, 99, 629–636.
64.
ZelckUE. (1999) Glycosidase activities in plasma of naive and schistosome-infected Biomphalaria glabrata (Gastropoda). Parasitology, 119 (Pt 6), 563–568.
65.
TerlauH, ShonKJ, GrilleyM, StockerM, StuhmerW, OliveraBM. (1996) Strategy for rapid immobilization of prey by a fishhunting marine snail. Nature, 381, 148–151.
