Tandem duplication of serpin genes yields functional variation and snake venom inhibitors
Posted on: 9 October 2025 , updated on: 14 October 2025
Preprint posted on 10 January 2025
This study shows coevolutionary adaptation in Neotoma macrotis, where duplicated SERPINA3 genes inhibit Crotalus venom proteases, revealing functional diversification and potential use in antivenom development.
Selected by Daniel Osorno Valencia, Marcus Oliveira
Categories: biochemistry, evolutionary biology, genetics
Figure from preprint made available under a CC-BY-NC-ND 4.0 International license.
Why I think this preprint is important:
This study uncovers a novel mechanism underlying snake venom resistance in Neotoma macrotis, showing that tandem duplications of SERPINA3 genes have produced variants capable of inhibiting venom serine proteases (SVSPs) from Crotalus species. Phylogenetic and functional analyses reveal that paralogs like SERPINA3-3 and SERPINA3-12 form stable inhibitory complexes, suggesting adaptive neofunctionalization. These findings highlight gene duplication as an evolutionary defense strategy and offer potential biomedical applications for antivenom development.
Background:
Snake venom resistance is a classic example of coevolution between the predator and the prey. Some animals have developed it through evolution, by obtaining molecular tools that can serve as a defense mechanism against venom. This includes changes in the expression of some receptors that are normally recognized by toxins, expression of proteins in blood that can neutralize toxins, or even specific immune responses [1], [2], [3].
In some mammals, like the squirrel Otospermophilus beecheyi, proteins have been identified in blood serum that are capable of binding to the venom toxins and neutralizing their effects[4]. Similarly in the rodents Dipodomys ordii and Neotoma floridana factors have been found in their blood capable of neutralizing the toxic effects of metalloproteinases [5]. Furthermore, in Caecilians (amphibians) it has been documented that convergent evolution has led to mutations in acetylcholine receptors that prevent the action of neurotoxins found in snake venom [6].
In this study, the authors explore how the tandem duplication of genes from the family SERPINA, a serine protease inhibitor in rodents, have generated variants with the capability to inhibit serine proteases from snake venom of different species. They analyze the evolution of these genes across clades and demonstrate that some variants found in the species Neotoma macrotis can inhibit serine proteases found in snake venom in vitro, showing how tandem duplications are related to venom resistance in mammals.
Key findings:
Duplication and evolution of the SERPINA genes in rodents
The authors found that the genes SERPINA1 and SERPINA3 have undergone a lot of gene duplication events in rodents, especially in comparison to other classes of vertebrates. The resulting variations occurred independently in different lineages, especially in the genus Neotoma where the species N. macrotis, for example, has 12 paralogs of SERPINA3 and various of SERPINA1 (preprint Fig 2). Through phylogenetic analysis, the authors identified a birth–death evolutionary pattern, with multiple recent duplications in Neotoma and copy losses in other lineages. This diversification has generated species-specific gene families, suggesting that these duplications are not neutral but may be under adaptive selective pressure, possibly in response to ecological challenges such as envenomation by predators. These results provide the genomic basis to study the evolutionary function of SERPINAs as potential resistance mechanisms.
Functional expression of paralogs of SERPINA3 and inhibition patterns
The authors were able to express and isolate with high purity the recombinant version of the 12 paralogs of SERPINA3 found in N. macrotis. Most of the recombinant proteins showed a functional activity against diverse serine proteases (preprint Fig 3). It was observed that SERPINA 3-3, 3-5, 3-8, 3-10 and 3-12 formed complexes with chymotrypsin and cathepsin G, which the authors believe indicates an inhibitory capacity of the serine proteases. Additionally, it was observed that the degradation pattern of each SERPINA was different, indicating a diverse functionality. For example, SERPINA3-6 was degraded by proteases without forming complexes, showing that some copies may have lost inhibitory function. This functional diversity among paralogs suggests that gene duplication has allowed the exploration of new biochemical functions, possibly related to adaptation to external challenges such as venom exposure.
Inhibition of snake venom proteases by SERPINA3
Two paralogs, SERPINA3-3 and SERPINA3-12, were shown to inhibit snake venom proteases (SVSPs), forming covalent complexes with purified toxins such as RVV-V and Protac (preprint Fig 4 A and D), as well as with fractions of SVSPs from Crotalus oreganus, C. molossus and C. adamanteus. The authors indicate that SERPINA3-3 formed complexes with all venom samples (preprint Fig 5), being most effective against venoms from non-sympatric snakes (such as C. adamanteus), whereas venoms from local predators (C. oreganus) generated less inhibition, suggesting a possible case of counter-adaptation by the predator. The authors suggest that duplicated SERPINAs not only maintain general inhibitory function but have acquired the specific ability to neutralize venom toxins, representing a potential mechanism of adaptive resistance. Furthermore, the formation of multiple complexes suggests that a single paralog may inhibit several isoforms of SVSPs, increasing their efficacy.
Questions:
Q1: The authors identified SERPINA gene duplications, particularly in rodents (preprint Fig. 1, 2), suggesting a role in lineage-specific adaptations like venom resistance in N. macrotis. However, gene presence does not guarantee protein expression in relevant tissues or dynamic regulation upon venom exposure [7,8]. Have the authors considered RNA-seq or qPCR on tissues like the liver of N. macrotis before and after venom exposure? As the liver is the primary source of circulating SERPINs, this could clarify whether these gene duplicates are functionally relevant and part of a regulated defensive response.
Q2: The authors found that the SERPINA variants are capable of forming complexes with different serine proteases, indicating their ability to bind to these enzymes (preprint Fig 4 and 5). To further complement these findings, the authors could consider incorporating enzymatic inhibition assays using fluorogenic or chromogenic substrates. Such approaches are widely used to quantify the inhibitory efficiency and specificity of protease inhibitors in a quantitative manner [9], [10]. For example, fluorescence-based microplate assays or spectrophotometric methods could provide additional insights into the functional differences among the SERPINA paralogs. While the complex formation demonstrates binding capacity, these kinetic assays could help determine how effectively each variant inhibits target proteases, offering a more detailed functional characterization and strengthening the conclusions regarding their potential role in venom resistance.
Q3: Have the authors considered incorporating structural modeling approaches, such as homology modeling, molecular docking, or structure prediction tools like AlphaFold, to further explore the specificity and inhibitory mechanism of the SERPINA variants interacting with serine proteases? Given that SERPINs inhibit serine proteases through a well-characterized conformational mechanism involving insertion of the reactive center loop (RCL) into β-sheet A, structural analyses could provide valuable insight into the molecular determinants of target specificity and potential neofunctionalization among the paralogs. Tools like AlphaFold, which have demonstrated remarkable accuracy in protein structure prediction, could be particularly useful for visualizing differences in the RCL region. These structural predictions could complement the biochemical assays presented here and help validate hypotheses about binding modes, specificity, and functional divergence. Similar structural approaches have been successfully applied in other studies to investigate protease-inhibitor interactions [11].
Bibliography
[1] E. O. Martinson, Mrinalini, Y. D. Kelkar, C. H. Chang, and J. H. Werren, “The Evolution of Venom by Co-option of Single-Copy Genes,” Current Biology, vol. 27, no. 13, pp. 2007-2013.e8, Jul. 2017, doi: 10.1016/j.cub.2017.05.032.
[2] K. W. Barbour, R. L. Goodwin, F. Guillonneau, Y. Wang, H. Baumann, and F. G. Berger, “Functional Diversification During Evolution of the Murine 1-Proteinase Inhibitor Family: Role of the Hypervariable Reactive Center Loop,” Mol. Biol. Evol, vol. 19, no. 5, pp. 718–727, 2002, [Online]. Available: https://academic.oup.com/mbe/article/19/5/718/1067846
[3] V. Župunski, D. Kordiš, and F. Gubenšek, “Adaptive evolution in the snake venom Kunitz/BPTI protein family,” FEBS Lett, vol. 547, no. 1–3, pp. 131–136, Jul. 2003, doi: 10.1016/S0014-5793(03)00693-8.
[4] H. L. Gibbs et al., “The molecular basis of venom resistance in a rattlesnake-squirrel predator-prey system,” Mol Ecol, vol. 29, no. 15, pp. 2871–2888, Aug. 2020, doi: 10.1111/mec.15529.
[5] N. R. Balchan, C. F. Smith, and S. P. Mackessy, “A plethora of rodents: Rattlesnake predators generate unanticipated patterns of venom resistance in a grassland ecosystem,” Toxicon X, vol. 21, Mar. 2024, doi: 10.1016/j.toxcx.2023.100179.
[6] M. Mancuso et al., “Resistance Is Not Futile: Widespread Convergent Evolution of Resistance to Alpha-Neurotoxic Snake Venoms in Caecilians (Amphibia: Gymnophiona),” Int J Mol Sci, vol. 24, no. 14, Jul. 2023, doi: 10.3390/ijms241411353.
[7] S. Naephrai, S. Khacha-Ananda, P. Pitchakarn, and C. Jaikang, “Composition and Acute Inflammatory Response from Tetraponera rufonigra Venom on RAW 264.7 Macrophage Cells,” Toxins (Basel), vol. 13, no. 4, Apr. 2021, doi: 10.3390/TOXINS13040257.
[8] A. Deka, M. Sharma, R. Mukhopadhyay, A. Devi, and R. Doley, “Naja kaouthia venom protein, Nk-CRISP, upregulates inflammatory gene expression in human macrophages,” Int J Biol Macromol, vol. 160, pp. 602–611, Oct. 2020, doi: 10.1016/j.ijbiomac.2020.05.169.
[9] J. G. Miyamoto et al., “A novel metalloproteinase-derived cryptide from Bothrops cotiara venom inhibits angiotensin-converting enzyme activity,” Biochimie, vol. 216, pp. 90–98, Jan. 2024, doi: 10.1016/j.biochi.2023.10.010.
[10] J. A. Price, “Microplate fluorescence protease assays test the inhibition of select North American snake venoms’ activities with an anti-proteinase library,” Toxicon, vol. 103, pp. 145–154, Jul. 2015, doi: 10.1016/j.toxicon.2015.06.020.
[11] J. Boldrini-França et al., “Beyond hemostasis: a snake venom serine protease with potassium channel blocking and potential antitumor activities,” Sci Rep, vol. 10, no. 1, Dec. 2020, doi: 10.1038/s41598-020-61258-x.
doi: https://doi.org/10.1242/prelights.41610
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