Insect Peroxiredoxins: A Comprehensive Review of Their Classification, Distribution, Structural Features, Expression Profiles and Physiological Functions
Simple Summary
Abstract
1. Introduction
2. Discovery and Nomenclature of Prxs
3. Structure and Classification of Prxs
4. Variation of Prxs Among Different Insect Species
5. Expression and Distribution of Prxs in Insects
5.1. Localization and Tissue-Specific Expression of Prxs
Classification | Insect Species | Prx Types | Number of Amino Acids | Spatial Expression Profile/Putative Subcellular Localization | Reference |
---|---|---|---|---|---|
Diptera: Culicidae | Anopheles stephensi | Prx-4783 (2-Cys Prx) | 196 | Midgut. | [28] |
Diptera: Drosophilidae | Drosophila melanogaster | Prx5 (2-Cys Prx) | 157 | Not determined. | [29] |
DPx-4156 (2-Cys Prx) | 242 | Secretion from the cell. | [30] | ||
DPx-4783 (2-Cys Prx) | 194 | Cytosol. | |||
DPx-5037 (2-Cys Prx) | 234 | Mitochondria. | |||
DPx-2540 (1-Cys Prx) | 220 | Cytosol. | |||
DPx-6005 (1-Cys Prx) | 222 | Cytosol. | |||
Jafrac1 (2-Cys Prx) | 194 | 11E in the X chromosome. | [31] | ||
Jafrac2 (2-Cys Prx) | 242 | 62F in the 3L chromosome. | |||
Diptera: Glossinidae | Glossina morsitans morsitans | Gmm-2087 (1-Cys Prx) | 222 | Flight muscle, fat body and midgut. | [32] |
Gmm-0929 (2-Cys Prx) | 168 | ||||
Gmm-2619 (1-Cys Prx) | 220 | ||||
Gmm-3099 (2-Cys Prx) | 194 | ||||
Gmm-2058 (2-Cys Prx) | 246 | ||||
Gmm-0601 (2-Cys Prx) | 236 | ||||
Lepidoptera: Bombycidae | Bombyx mori | TPx1 (2-Cys Prx) | 195 | Cytosol. | [4] |
Prx3 (2-Cys Prx) | 227 | Mitochondria. | |||
Prx4 (2-Cys Prx) | 247 | Secretion from the cell. | |||
Prx5 (2-Cys Prx) | 188 | Cytosol, mitochondria and peroxisomes. | |||
Prx6 (1-Cys Prx) | 223 | Cytosol. | |||
TPx (2-Cys Prx) | 195 | Fat body and midgut. | [5] | ||
Prx4 (2-Cys Prx) | 247 | Malpighian tubules, integument, ovaries, hemocytes, head, fat body, midgut, testis, silk glands and hemolymph. | [51] | ||
Prx (1-Cys Prx) | 223 | Gut, hemocytes, Malpighian tubes, ovaries, silk glands and fat body. | [52] | ||
Prx5 (1-Cys Prx) | 188 | Hemocytes, fat body and midgut. | [53] | ||
Prx3 (2-Cys Prx) | 227 | Midgut, fat body, silk glands, skin, trachea, head and hemocytes. | [54] | ||
Lepidoptera: Noctuidae | Helicoverpa armigera | TPx (2-Cys Prx) | 195 | Head, epidermis, fat body, hemolymph, midgut, Malpighian tubules, salivary glands and central nervous system. | [33] |
Spodoptera litura | TPx (2-Cys Prx) | 195 | Hemocytes, head and cuticles. | [38] | |
Prx5 (2-Cys Prx) | 159 | Epidermis, fat body and midgut. | [39] | ||
Lepidoptera: Pyralidae | Plodia interpunctella | TPx (2-Cys Prx) | 175 | Not determined. | [35] |
Lepidoptera: Saturniidae | Antherea pernyi | Prx2 (2-Cys Prx) | 228 | Hemocytes, fat body, midgut, integument, Malpighian tubules and silk glands. | [36] |
Prx1 (2-Cys Prx) | 195 | Hemocytes, fat body, midgut, integument, Malpighian tubules and silk glands. | [37] | ||
Lepidoptera: Crambidae | Chilo suppressalis | Tpx3 (2-Cys Prx) | 227 | Integument, midgut, Malpighian tubes and fat body. | [40] |
Prx5 (2-Cys Prx) | 189 | Fat body, head, epidermis and midgut. | [41] | ||
Prx6 (1-Cys Prx) | 223 | ||||
Lepidoptera: Tortricidae | Grapholita molesta | TPx (2-Cys Prx) | 195 | Head, epidermis, midgut, Malpighian tubules, fat body and salivary glands. | [55] |
Hymenoptera: Apidae | Apis cerana cerana | TPx4 (1-Cys Prx) | 219 | Head, thorax, abdomen, epidermis, muscle and midgut. | [42] |
TPx5 (1-Cys TPx) | 220 | Not determined. | [43] | ||
TPx3 (2-Cys Prx) | 242 | Brain, epidermis, muscle and midgut. | [44] | ||
TPx1 (2-Cys Prx) | 195 | Head, thorax and abdomen. | [45] | ||
Bombus ignitus | TPx1 (2-Cys Prx) | 195 | Fat body, midgut, muscle and epidermis. | [46] | |
Prx1 (1-Cys Prx) | 220 | ||||
Orthoptera: Gryllotalpidae | Gryllotalpa orientalis | GoPrx (1-Cys Prx) | 220 | Fat body, midgut and epidermis. | [47] |
Hemiptera: Aphididae | Acyrthosiphon pisum | Prx1 (2-Cys Prx) | 193 | Not determined. | [56] |
Hemiptera: Delphacidae | Nilaparvata lugens | Prx (2-Cys Prx) | 251 | Not determined. | [57] |
Coleoptera: Lampyridae | Pyrocoelia rufa | Prx (2-Cys Prx) | 185 | Fat body. | [58] |
5.2. Developmental Regulation of Prxs
5.3. Sex-Specific Expression of Prxs
6. Physiological Functions of Insect Prxs
6.1. Roles in Antioxidation and Electron Donor Requirement
6.2. Roles in Development and Lifespan
6.3. Roles in Environmental Stresses
6.4. Roles in Cell Apoptosis
6.5. Roles in Immune Response
6.6. Roles in Insecticide Resistance
7. Summary and Perspective
Author Contributions
Funding
Conflicts of Interest
References
- Dalton, T.P.; Shertzer, H.G.; Puga, A. Regulation of gene expression by reactive oxygen. Annu. Rev. Pharmacol. Toxicol. 1999, 39, 67–101. [Google Scholar] [CrossRef] [PubMed]
- Kamata, H.; Hirata, H. Redox regulation of cellular signalling. Cell. Signal. 1999, 11, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, S. Biochemical defence of pro-oxidant plant allelochemicals by herbivorous insects. Blochem. Syst. Ecol. 1992, 20, 269–296. [Google Scholar] [CrossRef]
- Shi, G.Q.; Zhang, Z.; Jia, K.L.; Zhang, K.; An, D.X.; Wang, G.; Zhang, B.L.; Yin, H.N. Characterization and expression analysis of peroxiredoxin family genes from the silkworm Bombyx mori in response to phoxim and chlorpyrifos. Pestic. Biochem. Physiol. 2014, 114, 24–31. [Google Scholar] [CrossRef]
- Lee, K.S.; Kim, S.R.; Park, N.S.; Kim, I.; Kang, P.D.; Sohn, B.H.; Choi, K.H.; Kang, S.W.; Je, Y.H.; Lee, S.M.; et al. Characterization of a silkworm thioredoxin peroxidase that is induced by external temperature stimulus and viral infection. Insect Biochem. Mol. Biol. 2005, 35, 73–84. [Google Scholar] [CrossRef]
- Wood, Z.A.; Poole, L.B.; Karplus, P.A. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 2003, 300, 650–653. [Google Scholar] [CrossRef]
- Kim, K.; Kim, I.H.; Lee, K.Y.; Rhee, S.G.; Stadtman, E.R. The isolation and purification of a specific “protector” protein which inhibits enzyme inactivation by a thiol/Fe (III)/O2 mixed-function oxidation system. J. Biol. Chem. 1988, 263, 4704–4711. [Google Scholar] [CrossRef] [PubMed]
- Kim, I.H.; Kim, K.; Rhee, S.G. Induction of an antioxidant protein of Saccharomyces cerevisiae by O2, Fe3+, or 2-mercaptoethanol. Proc. Natl. Acad. Sci. USA 1989, 86, 6018–6022. [Google Scholar] [CrossRef]
- Tartaglia, L.A.; Storz, G.; Brodsky, M.H.; Lai, A.; Ames, B.N. Alkyl hydroperoxide reductase from Salmonella typhimurium. Sequence and homology to thioredoxin reductase and other flavoprotein disulfide oxidoreductases. J. Biol. Chem. 1990, 265, 10535–10540. [Google Scholar] [CrossRef]
- Chae, H.Z.; Chung, S.J.; Rhee, S.G. Thioredoxin-dependent peroxide reductase from yeast. J. Biol. Chem. 1994, 269, 27670–27678. [Google Scholar] [CrossRef]
- Ulrich, K.; Jakob, U. The role of thiols in antioxidant systems. Free Radic. Biol. Med. 2019, 140, 14–27. [Google Scholar] [CrossRef] [PubMed]
- Perkins, A.; Nelson, K.J.; Parsonage, D.; Poole, L.B.; Karplus, P.A. Peroxiredoxins: Guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 2015, 40, 435–445. [Google Scholar] [CrossRef]
- Rhee, S.G.; Kang, S.W.; Chang, T.S.; Jeong, W.; Kim, K. Peroxiredoxin, a novel family of peroxidases. IUBMB Life 2001, 52, 35–41. [Google Scholar] [CrossRef]
- Wood, Z.A.; Schröder, E.; Harris, J.R.; Poole, L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 2003, 28, 32–40. [Google Scholar] [CrossRef] [PubMed]
- Abbas, M.N.; Kausar, S.; Cui, H. The biological role of peroxiredoxins in innate immune responses of aquatic invertebrates. Fish Shellfish Immunol. 2019, 89, 91–97. [Google Scholar] [CrossRef]
- Hall, A.; Nelson, K.; Poole, L.B.; Karplus, P.A. Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox Signal. 2011, 15, 795–815. [Google Scholar] [CrossRef] [PubMed]
- Rhee, S.G. Overview on peroxiredoxin. Mol. Cells 2016, 39, 1–5. [Google Scholar] [CrossRef]
- Mizohata, E.; Sakai, H.; Fusatomi, E.; Terada, T.; Murayama, K.; Shirouzu, M.; Yokoyama, S. Crystal structure of an archaeal peroxiredoxin from the aerobic hyperthermophilic crenarchaeon Aeropyrum pernix K1. J. Mol. Biol. 2005, 354, 317–329. [Google Scholar] [CrossRef]
- Nelson, K.J.; Knutson, S.T.; Soito, L.; Klomsiri, C.; Poole, L.B.; Fetrow, J.S. Analysis of the peroxiredoxin family: Using active-site structure and sequence information for global classification and residue analysis. Proteins 2011, 79, 947–964. [Google Scholar] [CrossRef]
- Radyuk, S.N.; Michalak, K.; Klichko, V.I.; Benes, J.; Rebrin, I.; Sohal, R.S.; Orr, W.C. Peroxiredoxin 5 confers protection against oxidative stress and apoptosis and also promotes longevity in Drosophila. Biochem. J. 2009, 419, 437–445. [Google Scholar] [CrossRef]
- Loumaye, E.; Andersen, A.C.; Clippe, A.; Degand, H.; Dubuisson, M.; Zal, F.; Morsomme, P.; Rees, J.-F.; Knoops, B. Cloning and characterization of Arenicola marina peroxiredoxin 6, an annelid two-cysteine peroxiredoxin highly homologous to mammalian one-cysteine peroxiredoxins. Free Radic. Biol. Med. 2008, 45, 482–493. [Google Scholar] [CrossRef] [PubMed]
- De Zoysa, M.; Ryu, J.H.; Chung, H.C.; Kim, C.H.; Nikapitiya, C.; Oh, C.; Kim, H.; Saranya Revathy, K.; Whang, I.; Lee, J. Molecular characterization, immune responses and DNA protection activity of rock bream (Oplegnathus fasciatus), peroxiredoxin 6 (Prx6). Fish Shellfish Immunol. 2012, 33, 28–35. [Google Scholar] [CrossRef]
- Manevich, Y.; Fisher, A.B. Peroxiredoxin 6, a 1-Cys peroxiredoxin, functions in antioxidant defense and lung phospholipid metabolism. Free Radic. Biol. Med. 2005, 38, 1422–1432. [Google Scholar] [CrossRef]
- Jeong, I.H.; Kim, A.Y.; Nguyen, P.; Kwon, D.H.; Koh, Y.H. Temperature-independent increase in the detoxifying enzyme activity of insecticide-resistant small brown planthoppers and Drosophila. J. Asia Pac. Entomol. 2021, 24, 70–76. [Google Scholar] [CrossRef]
- Trivelli, X.; Krimm, I.; Ebel, C.; Verdoucq, L.; Prouzet-Mauléon, V.; Chartier, Y.; Tsan, P.; Lauquin, G.; Meyer, Y.; Lancelin, J.M. Characterization of the yeast peroxiredoxin Ahp 1 in its reduced active and overoxidized inactive forms using NMR. Biochemistry 2003, 42, 14139–14149. [Google Scholar] [CrossRef] [PubMed]
- Rhee, S.G.; Yang, K.S.; Kang, S.W.; Woo, H.A.; Chang, T.S. Controlled elimination of intracellular H2O2: Regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid. Redox Signal. 2005, 7, 619–626. [Google Scholar] [CrossRef]
- Woo, H.A.; Yim, S.H.; Shin, D.H.; Kang, D.; Yu, D.Y.; Rhee, S.G. Inactivation of peroxiredoxin I by phosphorylation allows localized H2O2 accumulation for cell signaling. Cell 2010, 140, 517–528. [Google Scholar] [CrossRef]
- Peterson, T.M.; Luckhart, S. A mosquito 2-Cys peroxiredoxin protects against nitrosative and oxidative stresses associated with malaria parasite infection. Free Radic. Biol. Med. 2006, 40, 1067–1082. [Google Scholar] [CrossRef]
- Michalak, K.; Orr, W.C.; Radyuk, S.N. Drosophila peroxiredoxin 5 is the second gene in a dicistronic operon. Biochem. Biophys. Res. Commun. 2008, 368, 273–278. [Google Scholar] [CrossRef]
- Radyuk, S.N.; Klichko, V.I.; Spinola, B.; Sohal, R.S.; Orr, W.C. The peroxiredoxin gene family in Drosophila melanogaster. Free Radic. Biol. Med. 2001, 31, 1090–1100. [Google Scholar] [CrossRef]
- Rodriguez, J.; Agudo, M.; Van Damme, J.; Vandekerckhove, J.; Santarén, J.F. Polypeptides differentially expressed in imaginal discs define the peroxiredoxin family of genes in Drosophila. Eur. J. Biochem. 2000, 267, 487–497. [Google Scholar] [CrossRef] [PubMed]
- Munks, R.J.L.; Sant’Anna, M.R.V.; Grail, W.; Gibson, W.; Igglesden, T.; Yoshiyama, M.; Lehane, S.M.; Lehane, M.J. Antioxidant gene expression in the blood-feeding fly Glossina morsitans morsitans. Insect Mol. Biol. 2005, 14, 483–491. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Shen, Z.; Li, Z.; Wu, F.; Zhang, B.; Liu, Y.; Zhang, Q.; Liu, X. Identification of a thioredoxin peroxidase gene involved in resistance to nucleopolyhedrovirus infection in Helicoverpa armigera with RNA interference. J. Insect Physiol. 2015, 82, 17–27. [Google Scholar] [CrossRef]
- Cheng, J.; Zhu, L.; Zhu, F.; Zhao, P.; Li, Q.X.; Lu, Z.H.; Zhang, S.D.; Li, Z.; Liu, X.X. Peroxiredoxin 1 transfer during mating protects eupyrene sperm against oxdative stress in Grapholita molesta. Pest Manag. Sci. 2023, 79, 2823–2830. [Google Scholar] [CrossRef]
- Kumar, S.; Park, J.; Kim, E.; Na, J.; Chun, Y.S.; Kwon, H.; Kim, W.; Kim, Y. Oxidative stress induced by chlorine dioxide as an insecticidal factor to the Indian meal moth, Plodia interpunctella. Pestic. Biochem. Physiol. 2015, 124, 48–59. [Google Scholar] [CrossRef]
- Gul, I.; Abbas, M.N.; Hussaini, N.; Kausar, S.; Wu, S.; Cui, H. Peroxiredoxin-2 gene in Antheraea pernyi modulates immune functions and protect DNA damage. Int. J. Biol. Macromol. 2024, 256, 128410. [Google Scholar] [CrossRef]
- Abbas, M.N.; Gul, I.; Khosravi, Z.; Amarchi, J.I.; Ye, X.; Yu, L.; Siyuan, W.; Cui, H. Molecular characterization, immune functions and DNA protective effects of peroxiredoxin-1 gene in Antheraea pernyi. Mol. Immunol. 2024, 170, 76–87. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.; Yin, Y.; Feng, E.; Li, Y.; Xie, X.; Wang, Z. Thioredoxin peroxidase gene is involved in resistance to biocontrol fungus Nomuraea rileyi in Spodoptera litura: Gene cloning, expression, localization and function. Dev. Comp. Immunol. 2014, 44, 76–85. [Google Scholar] [CrossRef]
- Wan, H.; Kang, T.; Zhan, S.; You, H.; Zhu, F.; Lee, K.S.; Zhao, H.; Jin, B.R.; Li, J. Peroxiredoxin 5 from common cutworm (Spodoptera litura) acts as a potent antioxidant enzyme. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2014, 175, 53–61. [Google Scholar] [CrossRef]
- Cao, Y.; Yang, Q.; Tu, X.H.; Li, S.G.; Liu, S. Molecular characterization of a typical 2-Cys thioredoxin peroxidase from the Asiatic rice borer Chilo suppressalis and its role in oxidative stress. Arch. Insect Biochem. Physiol. 2018, 99, e21476. [Google Scholar] [CrossRef]
- Mo, W.; Li, Q.; He, X.; Lu, Z.; Xu, H.; Zheng, X.; Guo, J.; Lu, Y.; Wang, S. Identification and characterization of Prx5 and Prx6 in Chilo suppressalis in response to environmental stress. Arch. Insect Biochem. Physiol. 2023, 114, e22030. [Google Scholar] [CrossRef] [PubMed]
- Huaxia, Y.; Wang, F.; Yan, Y.; Liu, F.; Wang, H.; Guo, X.; Xu, B. A novel 1-Cys thioredoxin peroxidase gene in Apis cerana cerana: Characterization of AccTpx4 and its role in oxidative stresses. Cell Stress Chaperones 2015, 20, 663–672. [Google Scholar] [CrossRef]
- Yan, Y.; Zhang, Y.; Huaxia, Y.; Wang, X.; Yao, P.; Guo, X.; Xu, B. Identification and characterisation of a novel 1-Cys thioredoxin peroxidase gene (AccTpx5) from Apis cerana cerana. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2014, 172, 39–48. [Google Scholar] [CrossRef] [PubMed]
- Yao, P.; Lu, W.; Meng, F.; Wang, X.; Xu, B.; Guo, X. Molecular cloning, expression and oxidative stress response of a mitochondrial thioredoxin peroxidase gene (AccTpx-3) from Apis cerana cerana. J. Insect Physiol. 2013, 59, 273–282. [Google Scholar] [CrossRef] [PubMed]
- Yu, F.; Kang, M.; Meng, F.; Guo, X.; Xu, B. Molecular cloning and characterization of a thioredoxin peroxidase gene from Apis cerana cerana. Insect Mol. Biol. 2011, 20, 367–378. [Google Scholar] [CrossRef]
- Hu, Z.; Lee, K.S.; Choo, Y.M.; Yoon, H.J.; Lee, S.M.; Lee, J.H.; Kim, D.H.; Sohn, H.D.; Jin, B.R. Molecular cloning and characterization of 1-Cys and 2-Cys peroxiredoxins from the bumblebee Bombus ignitus. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2010, 155, 272–280. [Google Scholar] [CrossRef]
- Kim, I.; Lee, K.S.; Hwang, J.S.; Ahn, M.Y.; Li, J.; Sohn, H.D.; Jin, B.R. Molecular cloning and characterization of a peroxiredoxin gene from the mole cricket, Gryllotalpa orientalis. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2005, 140, 579–587. [Google Scholar] [CrossRef]
- Bhatti, J.S.; Bhatti, G.K.; Reddy, P.H. Mitochondrial dysfunction and oxidative stress in metabolic disorders—A step towards mitochondria based therapeutic strategies. Biochim. Biophys. Acta Mol. Basis Dis. 2017, 1863, 1066–1077. [Google Scholar] [CrossRef]
- Kausar, S.; Abbas, M.N.; Cui, H. A review on the DNA methyltransferase family of insects: Aspect and prospects. Int. J. Biol. Macromol. 2021, 186, 289–302. [Google Scholar] [CrossRef]
- Li, C.; Zhang, K.; Pan, G.; Zhang, L.; Hu, X.; Zhao, G.; Deng, C.; Tan, M.; Li, C.; Xu, M.; et al. Bmintegrin β1: A broadly expressed molecule modulates the innate immune response of Bombyx mori. Dev. Comp. Immunol. 2021, 114, 103869. [Google Scholar] [CrossRef]
- Shi, G.Q.; Yu, Q.Y.; Shi, L.; Zhang, Z. Molecular cloning and characterization of peroxiredoxin 4 involved in protection against oxidative stress in the silkworm Bombyx mori. Insect Mol. Biol. 2012, 21, 581–592. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Chen, K.; Yao, Q.; Zhao, Y.; Li, Y.; Shen, H.; Mu, R. Identification and characterization of a novel 1-Cys peroxiredoxin from silkworm, Bombyx mori. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2008, 149, 176–182. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Lu, Z. Expression, purification and characterization of an atypical 2-Cys peroxiredoxin from the silkworm, Bombyx mori. Insect Mol. Biol. 2015, 24, 203–212. [Google Scholar] [CrossRef]
- Wang, Q.; Zhou, Y.; Chen, K.; Ju, X. Identification and characterization of an atypical 2-cys peroxiredoxin from the silkworm, Bombyx mori. Insect Mol. Biol. 2016, 25, 347–354. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Zhu, F.; Shen, Z.; Moural, T.W.; Liu, L.; Li, Z.; Liu, X.; Xu, H. Glutaredoxins and thioredoxin peroxidase involved in defense of emamectin benzoate induced oxidative stress in Grapholita molesta. Pestic. Biochem. Physiol. 2021, 176, 104881. [Google Scholar] [CrossRef]
- Zhang, Y.; Lu, Z. Peroxiredoxin 1 protects the pea aphid Acyrthosiphon pisum from oxidative stress induced by Micrococcus luteus infection. J. Invertebr. Pathol. 2015, 127, 115–121. [Google Scholar] [CrossRef]
- Pang, R.; Xing, K.; Yuan, L.; Liang, Z.; Chen, M.; Yue, X.; Dong, Y.; Ling, Y.; He, X.; Li, X.; et al. Peroxiredoxin alleviates the fitness costs of imidacloprid resistance in an insect pest of rice. PLoS Biol. 2021, 19, e3001190. [Google Scholar] [CrossRef]
- Jin, B.R.; Lee, K.S.; Kim, S.R.; Sohn, H.D. cDNA Sequence and mRNA Expression of a Novel Peroxiredoxin from the Firefly, Pyrocoelia rufa. Int. J. Indust. Entomol. 2002, 4, 101–107. [Google Scholar]
- Shafeeq, T.; Cha, S.; Shim, J.K.; Lee, K.Y. Analysis of the whole developmental period reveals stage-specific gene expression profiles of the Indianmeal moth, Plodia interpunctella. J. Asia Pac. Entomol. 2017, 20, 671–677. [Google Scholar] [CrossRef]
- Kwatia, M.A.; Botkin, D.J.; Williams, D.L. Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin peroxidase. J. Parasitol. 2000, 86, 908–915. [Google Scholar] [CrossRef]
- Saunders, L.J. The Localization, Differential Expression, and Potential Immunological Role of Thioredoxin Peroxidase-2 (TPX-2) in the Filarial Parasite Brugia malayi; University of Massachusetts Amherst: Amherst, MA, USA, 2000. [Google Scholar]
- Degner, E.C.; Ahmed-Braimah, Y.H.; Borziak, K.; Wolfner, M.F.; Harrington, L.C.; Dorus, S. Proteins, transcripts, and genetic architecture of seminal fluid and sperm in the mosquito Aedes aegypti. Mol. Cell. Proteom. 2019, 18, S6–S22. [Google Scholar] [CrossRef] [PubMed]
- Bayram, H.; Sayadi, A.; Goenaga, J.; Immonen, E.; Arnqvist, G. Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach. Insect Mol. Biol. 2017, 26, 58–73. [Google Scholar] [CrossRef]
- Reinhardt, K.; Wong, C.H.; Georgiou, A.S. Detection of seminal fluid proteins in the bed bug, Cimex lectularius, using two-dimensional gel electrophoresis and mass spectrometry. Parasitology 2009, 136, 283–292. [Google Scholar] [CrossRef]
- Baer, B.; Heazlewood, J.L.; Taylor, N.L.; Eubel, H.; Millar, A.H. The seminal fluid proteome of the honeybee Apis mellifera. Proteomics 2009, 9, 2085–2097. [Google Scholar] [CrossRef] [PubMed]
- Radyuk, S.N.; Sohal, R.S.; Orr, W.C. Thioredoxin peroxidases can foster cytoprotection or cell death in response to different stressors: Over—And under—Expression of thioredoxin peroxidase in Drosophila cells. Biochem. J. 2003, 371, 743–752. [Google Scholar] [CrossRef]
- Dubuisson, M.; Vander Stricht, D.; Clippe, A.; Etienne, F.; Nauser, T.; Kissner, R.; Koppenol, W.H.; Rees, J.F.; Knoops, B. Human peroxiredoxin 5 is a peroxynitrite reductase. FEBS Lett. 2004, 571, 161–165. [Google Scholar] [CrossRef]
- Flohé, L.; Toppo, S.; Cozza, G.; Ursini, F. A comparison of thiol peroxidase mechanisms. Antioxid. Redox Signal. 2011, 15, 763–780. [Google Scholar] [CrossRef] [PubMed]
- Poole, L.B. The catalytic mechanism of peroxiredoxins. Subcell. Biochem. 2007, 44, 61–81. [Google Scholar]
- Immenschuh, S.; Baumgart-Vogt, E. Peroxiredoxins, oxidative stress, and cell proliferation. Antioxid. Redox Signal. 2005, 7, 768–777. [Google Scholar] [CrossRef]
- Li, J.; Zhang, W.B.; Loukas, A.; Lin, R.Y.; Ito, A.; Zhang, L.H.; Jones, M.; McManus, D.P. Functional expression and characterization of Echinococcus granulosus thioredoxin peroxidase suggests a role in protection against oxidative damage. Gene 2004, 326, 157–165. [Google Scholar] [CrossRef]
- Hofmann, B.; Hecht, H.J.; Flohé, L. Peroxiredoxins. Biol. Chem. 2002, 383, 347–364. [Google Scholar] [CrossRef]
- Fisher, A.B. Peroxiredoxin 6: A bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. Antioxid. Redox Signal. 2011, 15, 831–844. [Google Scholar] [CrossRef] [PubMed]
- Liu, G.; Feinstein, S.I.; Wang, Y.; Dodia, C.; Fisher, D.; Yu, K.; Ho, Y.S.; Fisher, A.B. Comparison of glutathione peroxidase 1 and peroxiredoxin 6 in protection against oxidative stress in the mouse lung. Free Radic. Biol. Med. 2010, 49, 1172–1181. [Google Scholar] [CrossRef]
- Ralat, L.A.; Manevich, Y.; Fisher, A.B.; Colman, R.F. Direct evidence for the formation of a complex between 1-cysteine peroxiredoxin and glutathione S-transferase π with activity changes in both enzymes. Biochemistry 2006, 45, 360–372. [Google Scholar] [CrossRef] [PubMed]
- Ralat, L.A.; Misquitta, S.A.; Manevich, Y.; Fisher, A.B.; Colman, R.F. Characterization of the complex of glutathione S-transferase pi and 1-cysteine peroxiredoxin. Arch. Biochem. Biophys. 2008, 474, 109–118. [Google Scholar] [CrossRef]
- Beckstead, R.B.; Lam, G.; Thummel, C.S. The genomic response to 20-hydroxyecdysone at the onset of Drosophila metamorphosis. Genome Biol. 2005, 6, R99. [Google Scholar] [CrossRef] [PubMed]
- Tian, Z.; Zha, M.; Cai, L.; Michaud, J.P.; Cheng, J.; Shen, Z.; Liu, X.; Liu, X. FoxO-promoted peroxiredoxin1 expression induced by Helicoverpa armigera single nucleopolyhedrovirus infection mediates host development and defensive responses. Ecotoxicol. Environ. Saf. 2022, 234, 113414. [Google Scholar] [CrossRef]
- Hao, K.; Jarwar, A.R.; Ullah, H.; Tu, X.; Nong, X.; Zhang, Z. Transcriptome sequencing reveals potential mechanisms of the maternal effect on egg diapause induction of Locusta migratoria. Int. J. Mol. Sci. 2019, 20, 1974. [Google Scholar] [CrossRef]
- Chen, J.; Cui, D.N.; Ullah, H.; Li, S.; Pan, F.; Xu, C.M.; Tu, X.B.; Zhang, Z.H. The function of LmPrx6 in diapause regulation in Locusta migratoria through the insulin signaling pathway. Insects 2020, 11, 763. [Google Scholar] [CrossRef]
- Powell, G.F.; Ward, D.A.; Prescott, M.C.; Spiller, D.G.; White, M.R.; Turner, P.C.; Earley, F.G.; Phillips, J.; Rees, H.H. The molecular action of the novel insecticide, Pyridalyl. Insect Biochem. Mol. Biol. 2011, 41, 459–469. [Google Scholar] [CrossRef]
- Odnokoz, O.; Nakatsuka, K.; Klichko, V.I.; Nguyen, J.; Solis, L.C.; Ostling, K.; Badinloo, M.; Orr, W.C.; Radyuk, S.N. Mitochondrial peroxiredoxins are essential in regulating the relationship between Drosophila immunity and aging. Biochim. Biophys. Acta Mol. Basis Dis. 2017, 1863, 68–80. [Google Scholar] [CrossRef]
- Odnokoz, O.; Earland, N.; Badinloo, M.; Klichko, V.I.; Benes, J.; Orr, W.C.; Radyuk, S.N. Peroxiredoxins play an important role in the regulation of immunity and aging in Drosophila. Antioxidants 2023, 12, 1616. [Google Scholar] [CrossRef]
- Kim, Y.; Park, J.; Kumar, S.; Kwon, H.; Na, J.; Chun, Y.; Kim, W. Insecticidal activity of chlorine dioxide gas by inducing an oxidative stress to the red flour beetle, Tribolium castaneum. J. Stored Prod. Res. 2015, 64, 88–96. [Google Scholar] [CrossRef]
- Martins, D.; Titorenko, V.I.; English, A.M. Cells with impaired mitochondrial H2O2 sensing generate less •OH radicals and live longer. Antioxid. Redox Signal. 2014, 21, 1490–1503. [Google Scholar] [CrossRef]
- Oláhová, M.; Taylor, S.R.; Khazaipoul, S.; Wang, J.; Morgan, B.A.; Matsumoto, K.; Blackwell, T.K.; Veal, E.A. A redox-sensitive peroxiredoxin that is important for longevity has tissue-and stress-specific roles in stress resistance. Proc. Natl. Acad. Sci. USA 2008, 105, 19839–19844. [Google Scholar] [CrossRef]
- Lee, K.S.; Iijima-Ando, K.; Iijima, K.; Lee, W.J.; Lee, J.H.; Yu, K.; Lee, D.S. JNK/FOXO-mediated neuronal expression of fly homologue of peroxiredoxin II reduces oxidative stress and extends life span. J. Biol. Chem. 2009, 284, 29454–29461. [Google Scholar] [CrossRef]
- Anderson, P.R.; Kirby, K.; Orr, W.C.; Hilliker, A.J.; Phillips, J.P. Hydrogen peroxide scavenging rescues frataxin deficiency in a Drosophila model of Friedreich’s ataxia. Proc. Natl. Acad. Sci. USA 2008, 105, 611–616. [Google Scholar] [CrossRef]
- Lu, J.; Holmgren, A. The thioredoxin antioxidant system. Free Radic. Biol. Med. 2014, 66, 75–87. [Google Scholar] [CrossRef]
- Dietz, K.J. Peroxiredoxins in plants and cyanobacteria. Antioxid. Redox Signal. 2011, 15, 1129–1159. [Google Scholar] [CrossRef]
- Heinrich, E.C.; Gray, E.M.; Ossher, A.; Meigher, S.; Grun, F.; Bradley, T.J. Aerobic function in mitochondria persists beyond death by heat stress in insects. J. Therm. Biol. 2017, 69, 267–274. [Google Scholar] [CrossRef]
- Menon, J.; Rozman, R. Oxidative stress, tissue remodeling and regression during amphibian metamorphosis. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2007, 145, 625–631. [Google Scholar] [CrossRef]
- Radyuk, S.N.; Michalak, K.; Klichko, V.I.; Benes, J.; Orr, W.C. Peroxiredoxin 5 modulates immune response in Drosophila. Biochim. Biophys. Acta 2010, 1800, 1153–1163. [Google Scholar] [CrossRef]
- Zheng, J.; Edelman, S.W.; Tharmarajah, G.; Walker, D.W.; Pletcher, S.D.; Seroude, L. Differential patterns of apoptosis in response to aging in Drosophila. Proc. Natl. Acad. Sci. USA 2005, 102, 12083–12088. [Google Scholar] [CrossRef]
- Harder, S.; Bente, M.; Isermann, K.; Bruchhaus, I. Expression of a mitochondrial peroxiredoxin prevents programmed cell death in Leishmania donovani. Eukaryot. Cell 2006, 5, 861–870. [Google Scholar] [CrossRef]
- Ahn, H.M.; Lee, K.S.; Lee, D.S.; Yu, K. JNK/FOXO mediated PeroxiredoxinV expression regulates redox homeostasis during Drosophila melanogaster gut infection. Dev. Comp. Immunol. 2012, 38, 466–473. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Wu, F.; Li, Z.; Lu, Z.; Zhang, X.; Zhang, Q.; Liu, X. Effects of Nucleopolyhedrovirus infection on the development of Helicoverpa armigera (Lepidoptera: Noctuidae) and expression of its 20-hydroxyecdysone- and juvenile hormone-related genes. Fla. Entomol. 2015, 98, 682–689. [Google Scholar] [CrossRef]
- Bento, F.M.M.; Darolt, J.C.; Merlin, B.L.; Penã, L.; Wulff, N.A.; Cônsoli, F.L. The molecular interplay of the establishment of an infection-gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus. BMC Genom. 2021, 22, 677. [Google Scholar] [CrossRef]
- Wang, Y.; Yang, P.; Cui, F.; Kang, L. Altered immunity in crowded locust reduced fungal (Metarhizium anisopliae) pathogenesis. PLoS Pathog. 2013, 9, e1003102. [Google Scholar] [CrossRef]
- Cui, F.; Chai, T.; Qian, L.; Wang, C. Effects of three diamides (chlorantraniliprole, cyantraniliprole and flubendiamide) on life history, embryonic development and oxidative stress biomarkers of Daphnia magna. Chemosphere 2017, 169, 107–116. [Google Scholar] [CrossRef]
- Hu, B.; Hu, S.; Huang, H.; Wei, Q.; Ren, M.; Huang, S.; Tian, X.; Su, J. Insecticides induce the co-expression of glutathione S-transferases through ROS/CncC pathway in Spodoptera exigua. Pestic. Biochem. Physiol. 2019, 155, 58–71. [Google Scholar] [CrossRef]
- Li, M.Y.; Tu, X.H.; Cao, Y.; Li, S.G.; Liu, S. Characterisation of a copper/zinc superoxide dismutase from Pieris rapae and its role in protecting against oxidative stress induced by chlorantraniliprole. Pestic. Biochem. Physiol. 2021, 174, 104825. [Google Scholar] [CrossRef] [PubMed]
- Palma-Onetto, V.; Oliva, D.; González-Teuber, M. Lethal and oxidative stress side effects of organic and synthetic pesticides on the insect scale predator Rhyzobius lophanthae. Entomol. Gen. 2021, 41, 345–355. [Google Scholar] [CrossRef]
- Sule, R.O.; Condon, L.; Gomes, A.V. A common feature of pesticides: Oxidative stress-the role of oxidative stress in pesticide-induced toxicity. Oxid. Med. Cell. Longev. 2022, 2022, 5563759. [Google Scholar] [CrossRef]
- Fan, Z.; Qian, L.; Chen, Y.; Fan, R.; He, S.; Gao, Y.; Gui, F. Effects of elevated CO2 on activities of protective and detoxifying enzymes in Frankliniella occidentalis and F. intonsa under spinetoram stress. Pest Manag. Sci. 2022, 78, 274–286. [Google Scholar] [CrossRef]
- Toledano, M.B.; Huang, B. Microbial 2-Cys peroxiredoxins: Insights into their complex physiological roles. Mol. Cells 2016, 39, 31–39. [Google Scholar] [CrossRef]
- Luo, W.; Chen, I.; Chen, Y.; Alkam, D.; Wang, Y.; Semenza, G.L. PRDX2 and PRDX4 are negative regulators of hypoxia-inducible factors under conditions of prolonged hypoxia. Oncotarget 2016, 7, 6379. [Google Scholar] [CrossRef]
- Turturice, B.A.; Lamm, M.A.; Tasch, J.J.; Zalewski, A.; Kooistra, R.; Schroeter, E.H.; Sharma, S.; Kawazu, S.; Kanzok, S.M. Expression of cytosolic peroxiredoxins in Plasmodium berghei ookinetes is regulated by environmental factors in the mosquito bloodmeal. PLoS Pathog. 2013, 9, e1003136. [Google Scholar] [CrossRef]
Predictive Function | Species | Prx Types | Reference |
---|---|---|---|
Participate in the growth, development, reproduction and other physiological functions of insects | Locusta migratoria | Prx6 | [80] |
Helicoverpa armigera | Prx1 | [78] | |
Involved in insect resistance to insecticides | Nilaparvata lugens | Prx | [57] |
Bombyx mori and Apis cerana cerana | TPx | [81] | |
Regulate the immune responses of insects | Antheraea pernyi | Prx2 | [36] |
Antheraea pernyi | Prx1 | [37] | |
Drosophila | Prx3 and Prx5 | [82] | |
Drosophila | Prx | [83] | |
Involved in resisting oxidative stress conditions of insects | Grapholita molesta | Prx1 | [34] |
Spodoptera litura | Tpx | [38] | |
Chilo suppressalis | Prx3 | [40] | |
Chilo suppressalis | Prx5 and Prx6 | [41] | |
Apis cerana cerana | Tpx4 | [42] | |
Bombyx mori | Prx5 | [53] | |
Bombyx mori | Prx3 | [54] | |
Acyrthosiphon pisum | Prx1 | [56] | |
Tribolium castaneum | TPx | [84] |
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Yang, L.; Lu, S.; Lu, Y.; Chen, M.; Cui, S. Insect Peroxiredoxins: A Comprehensive Review of Their Classification, Distribution, Structural Features, Expression Profiles and Physiological Functions. Insects 2025, 16, 678. https://doi.org/10.3390/insects16070678
Yang L, Lu S, Lu Y, Chen M, Cui S. Insect Peroxiredoxins: A Comprehensive Review of Their Classification, Distribution, Structural Features, Expression Profiles and Physiological Functions. Insects. 2025; 16(7):678. https://doi.org/10.3390/insects16070678
Chicago/Turabian StyleYang, Li, Shaohua Lu, Yujie Lu, Mingshun Chen, and Sufen Cui. 2025. "Insect Peroxiredoxins: A Comprehensive Review of Their Classification, Distribution, Structural Features, Expression Profiles and Physiological Functions" Insects 16, no. 7: 678. https://doi.org/10.3390/insects16070678
APA StyleYang, L., Lu, S., Lu, Y., Chen, M., & Cui, S. (2025). Insect Peroxiredoxins: A Comprehensive Review of Their Classification, Distribution, Structural Features, Expression Profiles and Physiological Functions. Insects, 16(7), 678. https://doi.org/10.3390/insects16070678