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. 2020 Mar 12;12(3):175. doi: 10.3390/toxins12030175

Table 1.

Targets and biological effects of cysteine-rich secretory proteins from buccal glands or venom.

Animals Name Species Target (Interaction Molecules) Biological Effect (or Related Investigation) Accession Numbers Ref.
Lamprey Lamprey CRISP

Buccal gland secretion protein-2
(BGSP-2)

Cysteine-rich buccal gland protein (CRBGP)		 Lethenteron japonicum
(Lampetra japonica) 		・Voltage-dependent
Na+ channels
・Integrin β2
(CD11s/CD18)		 Ca2+ channel blocker-like properties
Anti-angiogenic activities
Permeability
Inhibition of adhesion, proliferation, migration, and invasion of cells (HUVEC; IC50 = 4.0 μM and Hela cell; IC50 = 6.7 μM)
Non-fibrinogenolytic activity
Activity of immunosuppressant
(neutrophil inhibitory factor)
Inhibition of Na+ channels in hippocampal neurons (12 μM)
Inhibition K+ channels in hippocampal neurons (120 μM)		 A4PIZ5 [35,51,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56]
Cone snail Tex31 Conus textile N.D. Proteinase Q7YT83 [32]
Lizard Helothermine Heloderma horridum
salivary secretion		 ・Ryanodine receptors
・Ca2+ channels
・K+ channels		 Lethargy, partial paralysis of rear limbs and lowering of body temperature
Blockage of receptors (Cerebellar Granule Cells)
Inhibition of K+ channels (IC50 = 0.52 μM)
Inhibition of Ca2+ channels (IC50 = 0.25 μM)
Inhibition of skeletal ryanodine receptors (about 1.0 μM )		 Q91055 [40,57,58,59]
Snake
(Vipers) Ablomin Gloydius blomhoffi. N.D. Ca2+ channel blocker-like properties Q8JI40 [60]
Piscivorinc Agkistrodon piscivorus N.D. Ca2+ channel blocker-like properties AY181982 [61]
Catrin Crotalus atrox N.D. Ca2+ channel blocker-like properties AY181983 [61]
Triflin Protobothrops flavoviridis N.D. Ca2+ channel blocker-like properties Q8JI39
1WVR,
6IMF (with inhibitor)		 [60]
Stecrisp Trimeresurus stejnegeri
(Viridovipera stejnegeri) 		N.D. No proteolysis activity (unlikeTex31) P60623
1RC9		 [62]
Bj-CRP Bothrops jararaca Component C3 and C4 Bind and cleaved to component C3 and C4
Lack of effect of K+ channel blockage activity (1.0 μM)
(Kv1.1 to Kv1.6, Shaker-IR, Kv3.1, Kv7.1, Kv7.2, Kv7.4 and Kv10.1)		 N.D.
(partial sequence)		 [63]
Hellerin Crotalus oreganus helleri N.D. To increase trans-epithelial permeability
Cytotoxicity against HUVEC
(cytotoxic concentration CC50 = 2.3 μM)		 G9DCH4 [64]
EC-CRISP Echis Carinatus Sochureki N.D. Binding to HUVEC cell
Anti-angiogenic Activities (10-20 μg/ml, <1 μM)		 P0DMT4 [65]
Crovirin Crotalus viridis viridis N.D. Anti-protozoan activity against Trypanosoma cruzi and Leishmania amazonensis N.D
(partial sequence)		 [66]
(Elapid) Pseudechetoxin (PsTx) Pseudechis australis Cyclic nucleotide-
gated ion channels		 Inhibition of CNGA1 subunit (apparent Ki = 70 nM)
Inhibition of CNGA2 subunits (apparent Ki = 15 nM)		 Q8AVA4
2DDA		 [49,67]
Pseudecin Pseudechis porphyriacus Cyclic nucleotide-gated ion channels Ca2+ channel blocker-like properties Q8AVA3
2DDB, 2EPF(Zn2+)		 [49,60]
Latisemin Laticauda semifasciata N.D. Ca2+ channel blocker-like properties Q8JI38 [60]
Ophanin Ophiophagus hannah N.D. Ca2+ channel blocker-like properties AY181984 [61]
Natrin Naja Naja atra Bkca
Kv1.3
Ryanodine receptors
Heparin		 High-conductance calcium-activated potassium (BKCa) channel (34.4 nM)
Inhibition of Kv1.3 (10–200 nM)
Inhibition of ryanodine receptors (1 μM, Kd = 1.5–2.3 nM)
Inflammatory Modulator (<1.0 μM)
Non-proteolytic activity
(BSA, neurotensin, Tex31 substrate, kenetensin)		 Q7T1K6
1XX5,
1XTA,
2GIZ
3MZ8 (Zn2+)		 [68,69,70]
(Colubrid) Tigrin Rhabdophis tigrinus N.D. Non-Ca2+ channel blocker-like properties Q8JGT9 [60]
Patagonin Philodryas patagoniensis N.D. Non-Ca2+ channel blocker-like properties
Non-fibrinogenolytic activity
Skeletal myotoxic activity (43 and 87 μM)		 N.D.
(only N-terminal sequence)		 [71]

Tex31 is located in Pathogenesis-related 1 (PR-1) members. N.D.; not determined or did not investigate. Ca2+ channel blocker-like properties; inhibited depolarization-induced contraction of rat-tail arterial smooth muscle. All accession numbers are from UniProt (https://www.uniprot.org/) and Protein Data Bank (PDB, https://www.rcsb.org/pdb/home/sitemap.do).