Phenylalanine ammonia lyase: new insights from Piperaceae species
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Abstract
The enzyme PAL (phenylalanine ammonia lyase) mediates the key entry point to the general phenylpropanoid pathway, which is involved in the lignification process and in the formation of a myriad of secondary compounds in plants that show a variety of biological activities. Soluble fractions containing PAL extracted from Piper and Peperomia species had the optimal catalytic activity analyzed by statistical design model. This analysis revealed that the best conversion of L-phenylalanine to trans-cinnamic acid was pH 9.3 and 58 °C after 25 h, corroborating interesting thermal stability. Additionally, the pre-purification of PAL using ammonium sulfate precipitation (25-55%) increased its specific activity, approximately 133% in P. aduncum and more than 900% in P. crassinervium. The content of lignin was higher for P. tuberculatum (25.71%), while only a small amount of lignin was observed in Peperomia blanda (11.95%). It is interesting to note that Peperomia plants are succulent and without significant amounts of lignin. However, the phenylpropanoid biosynthetic pathway is apparently addressed to produce predominantly tetrahydrofuran lignans with biological interest.
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Funding data
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Fundação de Amparo à Pesquisa do Estado de São Paulo
Grant numbers 2014/50926-0;2013/07600-3 -
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Grant numbers 2014/465637-0
References
Alves, N. S. F.; Setzer, W. N.; Silva, J. K. R. The chemistry and biological activities of Peperomia pellucida (Piperaceae): A critical review. J. Ethnopharmacol. 2019, 232, 90–102. https://doi.org/10.1016/j.jep.2018.12.021
Akbarian, A.; Rahimmalek, M.; Sabzalian, M. R.; Hodaei, M. Sequencing and phylogenetic analysis of phenylalanine ammonia lyase (pal) and chalcone synthase (chs) genes in some Iranian endemic species of Apiaceae. Gene Rep. 2021, 23, 101147. https://doi.org/10.1016/j.genrep.2021.101147
Arunachalam, K.; Damazo, A. S.; Macho, A.; Lima, J. C. S.; Pavan, E.; Figueiredo, F. F.; Oliveira, D. M.; Cechinel-Filho, V.; Wagner, T. M.; Tabajara, D.; Martins, D. T. O. Piper umbellatum L. (Piperaceae): Phytochemical profiles of the hydroethanolic leaf extract and intestinal anti-inflammatory mechanisms on 2, 4, 6 trinitrobenzene sulfonic acid induced ulcerative colitis in rats. J. Ethnopharmacol. 2020, 254, 112707. https://doi.org/10.1016/j.jep.2020.112707
Araújo-Vilges, K. M.; Oliveira, S. V.; Couto, S. C. P.; Fokoue, H. H.; Romero, G. A. S.; Kato, M. J.; Romeiro, L. A. S.; Leite, J. R. S. A.; Kuckelhaus, S. A. S. Effect of piplartine and cinnamides on Leishmania amazonensis, Plasmodium falciparum and on peritoneal cells of Swiss mice. Pharm. Biol. 2017, 55 (1), 1601–1607. https://doi.org/10.1080/13880209.2017.1313870
Banu, J. R.; Kavitha, S.; Kannah, R. Y.; Devi, T. P.; Gunasekaran, M.; Kim, S.-H.; Kumar, G. A review on biopolymer production via lignin valorization. Bioresour. Technol. 2019, 290, 121790. https://doi.org/10.1016/j.biortech.2019.121790
Batista, A. N. L.; Batista Junior, J. M.; Zocolo, G. J.; Zanoni, M. V. B.; Kato, M. J.; López, S. N.; Furlan, M. Protein and metabolic profiles of Peperomia obtusifolia (Piperaceae). Planta Med. 2012, 78 (11), PB3. https://doi.org/10.1055/s-0032-1320332
Batista, A. N. L.; Santos-Pinto, J. R. A. D.; Batista Junior, J. M.; Souza-Moreira, T. M.; Santoni, M. M.; Zanelli, C. F.; Kato, M. J.; López, S. N.; Furlan, M. The Combined Use of Proteomics and Transcriptomics Reveals a Complex Secondary Metabolite Network in Peperomia obtusifolia. J. Nat. Prod. 2017, 80 (5), 1275–1286. https://doi.org/10.1021/acs.jnatprod.6b00827
Batista Junior, J. M.; Lopes, A. A.; Ambrosio, D. L.; Regasini, L. O.; Kato, M. J.; Bolzani, V. S.; Cicarelli, R. M. B.; Furlan, M. Natural chromenes and chromene derivatives as potential anti-trypanosomal agents. Biol. Pharm. Bull. 2008, 31 (3), 538–540. https://doi.org/10.1248/bpb.31.538
Batista Junior, J. M.; López, S. N.; Mota, J. S.; Vanzolini, K. L.; Cass, Q. B.; Rinaldo, D.; Vilegas, W.; Bolzani, V. S.; Kato, M. J.; Furlan, M. Resolution and absolute configuration assignment of a natural racemic chromane from Peperomia obtusifolia (Piperaceae). Chirality 2009, 21 (9), 799–801. https://doi.org/10.1002/chir.20676
Batista Junior, J. M.; Batista, A. N. L.; Rinaldo, D.; Vilegas, W.; Cass, Q. B.; Bolzani, V. S.; Kato, M. J.; López, S. N.; Furlan, M.; Nafie, L. A. Absolute configuration reassignment of two chromanes from Peperomia obtusifolia (Piperaceae) using VCD and DFT calculations. Tetrahedron Asymmetry 2010, 21 (19), 2402–2407. https://doi.org/10.1016/j.tetasy.2010.09.004
Batista Junior, J. M.; Batista, A. N. L.; Kato, M. J.; Bolzani, V. S.; López, S. N.; Nafie, L. A.; Furlan, M. Further monoterpene chromane esters from Peperomia obtusifolia: VCD determination of the absolute configuration of a new diastereomeric mixture. Tetrahedron Lett. 2012, 53 (45), 6051–6054. https://doi.org/10.1016/j.tetlet.2012.08.113
Begović, L.; Abičić, I.; Lalić, A.; Lepeduš, H.; Cesar, V.; Leljak-Levanić, D. Lignin synthesis and accumulation in barley cultivars differing in their resistance to lodging. Plant Physiol. Biochem. 2018, 133, 142–148. https://doi.org/10.1016/j.plaphy.2018.10.036
Burton, B. K.; Longo, N.; Vockley, J.; Grange, D. K.; Harding, C. O.; Decker, C.; Li, M.; Lau, K.; Rosen, O.; Larimore, K.; Thomas, J. Pegvaliase for the treatment of phenylketonuria: Results of the phase 2 dose-finding studies with long-term follow-up. Mol. Genet. Metab. 2020, 130 (4), 239–246. https://doi.org/10.1016/j.ymgme.2020.06.006
Campelo, Y.; Ombredane, A.; Vasconcelos, A. G.; Albuquerque, L.; Moreira, D. C.; Plácido, A.; Rocha, J.; Fokoue, H. H.; Yamaguchi, L.; Mafud, A.; Mascarenhas, Y. P.; Delerue-Matos, C.; Borges, T.; Joanitti, G. A.; Arcanjo, D. D. R.; Kato, M. J.; Kuckelhaus, S. A. S.; Silva, M. P. N.; Moraes, J.; Leite, J. R. S. Structure–Activity relationship of piplartine and synthetic analogues against Schistosoma mansoni and cytotoxicity to mammalian cells. Int. J. Mol. Sci. 2018, 19 (6), 1802. https://doi.org/10.3390/ijms19061802
Choudhary, A. K.; Lee, Y. Y. The debate over neurotransmitter interaction in aspartame usage. J. Clin. Neurosci. 2018, 56, 7–15. https://doi.org/10.1016/j.jocn.2018.06.043
Corral, A. C. T.; Queiroz, M. N.; Andrade-Porto, S. M.; Morey, G. A. M.; Chaves, F. C. M.; Fernandes, V. L. A.; Ono, E. A.; Affonso, E. G. Control of Hysterothylacium sp. (Nematoda: Anisakidae) in juvenile pirarucu (Arapaima gigas) by the oral application of essential oil of Piper aduncum. Aquaculture. 2018, 494, 37–44. https://doi.org/10.1016/j.aquaculture.2018.04.062
Cortez, A. P.; Menezes, E. G. P.; Benfica, P. L.; Santos, A. P.; Cleres, L. M.; Ribeiro, H. O.; Lima, E. M.; Kato, M. J.; Valadares, M. C. Grandisin induces apoptosis in leukemic K562 cells. Braz. J. Pharm. Sci. 2017, 53 (1), e15210. https://doi.org/10.1590/s2175-97902017000115210
Danelutte, A. P.; Lago, J. H. G.; Young, M. C. M.; Kato, M. J. Antifungal flavanones and prenylated hydroquinones from Piper crassinervium Kunth. Phytochemistry. 2003, 64 (2), 555–559. https://doi.org/10.1016/S0031-9422(03)00299-1
Dong, C.-J.; Cao, N.; Zhang, Z.-g.; Shang, Q.-m. Phenylalanine ammonia-lyase gene families in cucurbit species: Structure, evolution, and expression. J. Integr. Agric. 2016, 15 (6), 1239–1255. https://doi.org/10.1016/S2095-3119(16)61329-1
Donlon, J.; Levy, H.; Scriver, C. R. Hyperphenylalaninemia: phenylalanine hydroxylase deficiency. In The metabolic and molecular bases of inherited disease. Scriver, C. R.; Beaudet, A. R.; Sly, W.; Valle, D. (Eds.). McGraw Hill, 2004; 1821–1838.
Durant-Archibold, A. A.; Santana, A. I.; Gupta, M. P. Ethnomedical uses and pharmacological activities of most prevalent species of genus Piper in Panama: A review. J. Ethnopharmacol. 2018, 217, 63–82. https://doi.org/10.1016/j.jep.2018.02.008
Englard, S.; Seifter, S. In Methods in Enzymology. Guide to Protein Purification. Academic Press, 1990; 285–300. https://doi.org/10.1016/0076-6879(90)82024-V
El Babili, F.; Rey-Rigaud, G.; Rozon, H.; Halova-Lajoie, B. State of knowledge: Histolocalisation in phytochemical study of medicinal plants. Fitoterapia. 2021, 150, 104862. https://doi.org/10.1016/j.fitote.2021.104862
Felippe, L. G.; Baldoqui, D. C.; Kato, M. J.; Bolzani, V. S.; Guimarães, E. F.; Cicarelli, R. M. B.; Furlan, M. Trypanocidal tetrahydrofuran lignans from Peperomia blanda. Phytochemistry. 2008, 69 (2), 445–450. https://doi.org/10.1016/j.phytochem.2007.08.012
Felippe, L. G.; Batista Junior, J. M.; Baldoqui, D. C.; Nascimento, I. R.; Kato, M. J.; He, Y.; Nafie, L. A.; Furlan, M. (2012). VCD to determine absolute configuration of natural product molecules: secolignans from Peperomia blanda. Org. Biomol. Chem. 2012 10 (21), 4208–4214. https://doi.org/10.1039/c2ob25109d
Ferreira, E. A.; Reigada, J. B.; Correia, M. V.; Young, M. C. M.; Guimarães, E. F.; Franchi Junior, G. C.; Nowill, A. E.; Lago, J. H. G.; Yamaguchi, L. F.; Kato, M. J. Antifungal and cytotoxic 2-acylcyclohexane-1, 3-diones from Peperomia alata and P. trineura. J. Nat. Prod. 2014, 77 (6), 1377–1382. https://doi.org/10.1021/np500130x
Finkelman M. A. J.; Yang, H. H. Production of phenylalanine ammonia lyase by fermentation. Genex Corporation, European Pat. 1985, 140, 714.
Freitas, G. C.; Batista Junior, J. M.; Franchi Junior, G. C.; Nowill, A. E.; Yamaguchi, L. F.; Vilcachagua, J. D.; Favaro, D. C.; Furlan, M.; Guimarães, E. F.; Jeffrey, C. S.; Kato, M. J. Cytotoxic non-aromatic B-ring flavanones from Piper carniconnectivum C. DC. Phytochemistry. 2014, 97, 81–87. https://doi.org/10.1016/j.phytochem.2013.10.012
Gao, Z.; Sun, W.; Wang, J.; Zhao, C.; Zuo, K. GhbHLH18 negatively regulates fiber strength and length by enhancing lignin biosynthesis in cotton fibers. Plant Sci. 2019, 286, 7–16. https://doi.org/10.1016/j.plantsci.2019.05.020
García-Huertas, P.; Olmo, F.; Sánchez-Moreno, M.; Dominguez, J.; Chahboun, R.; Triana-Chávez, O. Activity in vitro and in vivo against Trypanosoma cruzi of a furofuran lignan isolated from Piper jericoense. Exp. Parasitol. 2018, 189, 34–42. https://doi.org/10.1016/j.exppara.2018.04.009
Gutiérrez-Quequezana, L.; Vuorinen, A. L.; Kallio, H.; Yang, B. Impact of cultivar, growth temperature and developmental stage on phenolic compounds and ascorbic acid in purple and yellow potato tubers. Food Chem. 2020, 326, 126966. https://doi.org/10.1016/j.foodchem.2020.126966
Hamedan, H. J.; Sohani, M. M.; Aalami, A.; Nazarideljou, M. J. Genetic engineering of lignin biosynthesis pathway improved stem bending disorder in cut gerbera (Gerbera jamesonii) flowers. Sci. Hortic. 2019, 245, 274–279. https://doi.org/10.1016/j.scienta.2018.10.013
Hamilton, B. K.; Hsiao, H.-Y.; Swann, W.; Anderson, D. M.; Delente, J. J. Manufacture of L-amino, acids with bioreactors. Trends Biotechnol. 1985, 3 (3), 64–68. https://doi.org/10.1016/0167-7799(85)90079-4
Hartnett, C.; Salvarinova-Zivkovic, R.; Yap-Todos, E.; Cheng, B.; Giezen, A.; Horvath, G.; Lillquist, Y.; Vallance, H.; Stockler-Ipsiroglu, S. Long-term outcomes of blood phenylalanine concentrations in children with classical phenylketonuria. Mol. Gen. Metab. 2013, 108 (4), 255–258. https://doi.org/10.1016/j.ymgme.2013.01.007
Huang, S.-J.; Lin, S.-Y.; Wang, T.-T.; Hsu, F.-C. Combining acetic acid and ethanol as an anti-browning treatment for lettuce butt discoloration through repression of the activity and expression of phenylalanine ammonia lyase. Postharvest Biol. Technol. 2020, 164, 111151. https://doi.org/10.1016/j.postharvbio.2020.111151
Hussain, S.; Iqbal, N.; Pang, T.; Khan, M. N.; Liu, W.-g.; Yang, W.-y. Weak stem under shade reveals the lignin reduction behavior. J. Integr. Agric. 2019, 18 (3), 496–505. https://doi.org/10.1016/S2095-3119(18)62111-2
Jeffrey, C. S.; Leonard, M. D.; Glassmire, A. E.; Dodson, C. D.; Richards, L. A.; Kato, M. J.; Dyer, L. A. Antiherbivore Prenylated Benzoic Acid Derivatives from Piper kelleyi. J. Nat. Prod. 2014, 77 (1), 148–153. https://doi.org/10.1021/np400886s
Kamdee, C.; Imsabai, W.; Kirk, R.; Allan, A. C.; Ferguson, I. B.; Ketsa, S. Regulation of lignin biosynthesis in fruit pericarp hardening of mangosteen (Garcinia mangostana L.) after impact. Postharvest Biol. Technol. 2014, 97, 68–76. https://doi.org/10.1016/j.postharvbio.2014.06.004
Kato, M. J.; Furlan, M. Chemistry and evolution of the Piperaceae. Pure Appl. Chem. 2007, 79 (4), 529–538. https://doi.org/10.1351/pac200779040529
Kawatra, A.; Dhankhar, R.; Mohanty, A.; Gulati, P. Biomedical applications of microbial phenylalanine ammonia lyase: current status and future prospects. Biochimie. 2020, 177, 142–152. https://doi.org/10.1016/j.biochi.2020.08.009
Kitamura, R. O. S.; Romoff, P.; Young, M. C. M.; Kato, M. J.; Lago, J. H. G. Chromenes from Peperomia serpens (Sw.) Loudon (Piperaceae). Phytochemistry. 2006, 67 (21), 2398–2402. https://doi.org/10.1016/j.phytochem.2006.08.007
Klejdus, B.; Kováčik, J.; Babula, P. PAL inhibitor evokes different responses in two Hypericum species. Plant Physiol. Biochem. 2013, 63, 82–88. https://doi.org/10.1016/j.plaphy.2012.11.019
Lago, J. H. G.; Ramos, C. S.; Casanova, D. C. C.; Morandim, A. A.; Bergamo, D. C. B.; Cavalheiro, A. J.; Bolzani, V. S.; Furlan, M.; Guilharães, E. F.; Young, M. C. M.; Kato, M. J. Benzoic acid derivatives from Piper species and their fungitoxic activity against Cladosporium cladosporioides and C. sphaerospermum, J. Nat. Prod. 2004, 67 (11), 1783–1788. https://doi.org/10.1021/np030530j
Lago, J. H. G.; Young, M. C. M.; Reigada, J. B.; Soares, M. G.; Roesler, B. P.; Kato, M. J. Antifungal derivatives from Piper mollicomum and P. lhotzkyanum (Piperaceae). Quim. Nova 2007, 30 (5), 1222–1224. https://doi.org/10.1590/S0100-40422007000500032
Levy, H. L.; Sarkissian, C. N.; Scriver, C. R. Phenylalanine ammonia lyase (PAL): From discovery to enzyme substitution therapy for phenylketonuria. Mol. Genet. Metab. 2018, 124 (4), 223–229. https://doi.org/10.1016/j.ymgme.2018.06.002
Liu, W.-g.; Hussain, S.; Liu, T.; Zou, J.-l.; Ren, M.-l.; Zhou, T.; Liu, J.; Yang, F.; Yang, W.-y. Shade stress decreases stem strength of soybean through restraining lignin biosynthesis. J. Integr. Agric. 2019, 18 (1), 43–53. https://doi.org/10.1016/S2095-3119(18)61905-7
Lopes, A. A.; Baldoqui, D. C.; López, S. N.; Kato, M. J.; Bolzani, V. S.; Furlan, M. Biosynthetic origins of the isoprene units of gaudichaudianic acid in Piper gaudichaudianum (Piperaceae). Phytochemistry. 2007, 68 (15), 2053–2058. https://doi.org/10.1016/j.phytochem.2007.04.025
López, S. N.; Lopes, A. A.; Batista Junior, J. M.; Flausino Junior, O.; Bolzani, V. S; Kato, M. J.; Furlan, M. Geranylation of benzoic acid derivatives by enzymatic extracts from Piper crassinervium (Piperaceae). Bioresour. Technol. 2010, 101 (12), 4251–4260. https://doi.org/10.1016/j.biortech.2010.01.041
Macêdo, C. G.; Fonseca, M. Y. N.; Caldeira, A. D.; Castro, S. P.; Pacienza-Lima, W.; Borsodi, M. P. G.; Sartoratto, A.; Silva, M. N.; Salgado, C. G.; Rossi-Bergmann, B.; Castro, K. C. F. Leishmanicidal activity of Piper marginatum Jacq. from Santarém-PA against Leishmania amazonensis. Exp. Parasitol. 2020, 210, 107847. https://doi.org/10.1016/j.exppara.2020.107847
Machado, M.; Felizardo, C.; Fernandes-Silva, A.; Nunes, F. M.; Barros, A. Polyphenolic compounds, antioxidante activity and L-phenylalanine ammonia-lyase activity during ripening of olive cv. “Cobrançosa” under different irrigation regimes. Food Res. Int. 2013, 51 (1), 412–421. https://doi.org/10.1016/j.foodres.2012.12.056
Maleck, M.; Ferreira, B.; Mallet, J.; Guimaróes, A.; Kato, M. J. Cytotoxicity of Piperamides Towards Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 2014, 51 (2), 458–463. https://doi.org/10.1603/ME13069
Marques, J. V.; Oliveira, A. D.; Raggi, L.; Young, M. C. M.; Kato, M. J. Antifungal activity of natural and synthetic amides from Piper species. J. Braz. Chem. Soc. 2010, 21 (10), 1807–1813. https://doi.org/10.1590/S0103-50532010001000003
Martins, R. C. C.; Lago, J. H. G.; Albuquerque, S.; Kato, M. J. Trypanocidal tetrahydrofuran lignans from Piper solmsianum. Phytochemistry. 2003, 64 (2), 667–670. https://doi.org/10.1016/S0031-9422(03)00356-X
Mgbeahuruike, E. E.; Yrjönen, T.; Vuorela, H.; Holm, Y. Bioactive compounds from medicinal plants: Focus on Piper species. S. Afr. J. Bot. 2017, 112, 54–69. https://doi.org/10.1016/j.sajb.2017.05.007
Miranda, J. E.; Navickiene, H. M. D.; Nogueira-Couto, R. H.; Bortoli, S. A.; Kato, M. J.; Bolzani, V. S.; Furlan, M. Susceptibility of Apis mellifera (Hymenoptera: Apidae) to pellitorine, an amide isolated from Piper tuberculatum (Piperaceae). Apidologie. 2003, 34 (4), 409–415. https://doi.org/10.1051/apido:2003036
Moraes, J.; Keiser, J.; Ingram, K.; Nascimento, C.; Yamaguchi, L. F.; Bittencourt, C. R.; Bemquerer, M. P.; Leite, J. R.; Kato, M, J.; Nakano, E. In vitro synergistic interaction between amide piplartine and antimicrobial peptide dermaseptin against Schistosoma mansoni schistosomula and adult worms. Curr. Med. Chem. 2013, 20 (2), 301–309. https://doi.org/10.2174/092986713804806694
Moraes, M. M.; Kato, M. J. Biosynthesis of Pellucidin A in Peperomia pellucida (L.) HBK. Front. Plant Sci. 2021, 12, 641717. https://doi.org/10.3389/fpls.2021.641717
Morandim, A. A; Bergamo, D. C. B.; Kato, M. J.; Cavalheiro, A. J.; Bolzani, V. S., Furlan, M. Circadian rhythm of anti‐fungal prenylated chromene in leaves of Piper aduncum. Phytochemical Anal. 2005, 16 (4), 282–286. https://doi.org/10.1002/pca.843
Mota, J. S.; Leite, A. C.; Batista Junior, J. M.; López, S. N.; Ambrósio, D. L.; Passerini, G. D.; Kato, M. J.; Bolzani, V. S.; Cicarelli, R. M. B.; Furlan, M. In vitro Trypanocidal Activity of Phenolic Derivatives from Peperomia obtusifolia. Planta Med. 2009, 75 (6), 620–623. https://doi.org/10.1055/s-0029-1185364
Mota, J. S.; Leite, A. C.; Kato, M. J.; Young, M. C. M.; Bolzani, V. D. S.; Furlan, M. Isoswertisin flavones and other constituents from Peperomia obtusifolia. Nat. Prod. Res. 2011, 25 (1), 1–7. https://doi.org/10.1080/14786410903244954
Navickiene, H. M. D.; Alécio, A. C.; Kato, M. J.; Bolzani, V. D. S.; Young, M. C. M.; Cavalheiro, A. J.; Furlan, M. Antifungal amides from Piper hispidum and Piper tuberculatum. Phytochemistry. 2000, 55 (6), 621–626. https://doi.org/10.1016/S0031-9422(00)00226-0
Navickiene, H. M. D; Bolzani, V. S.; Kato, M. J; Pereira, A. M. S.; Bertoni, B. W.; Furlan, M. Quantitative determination of anti-fungal and insecticide amides in adult plants, plantlets and callus from Piper tuberculatum by reverse-phase high-performance liquid chromatography. Phytochem. Anal. 2003, 14 (5), 281–284. https://doi.org/10.1002/pca.716
Neves, A. R.; Trefzger, O. S.; Barbosa, N. V.; Honorato, A. M.; Carvalho, D. B.; Moslaves, I. S.; Kadri, M. C. T.; Yoshida, N. C.; Kato, M. J.; Arruda, C. C. P.; Baroni, A. C. Effect of isoxazole derivatives of tetrahydrofuran neolignans on intracellular amastigotes of Leishmania (Leishmania) amazonensis: A structure–activity relationship comparative study with triazole‐neolignan‐based compounds. Chem. Biol. Drug Des. 2019, 94 (6), 2004–2012. https://doi.org/10.1111/cbdd.13609
Oliveira, A.; Mesquita, J. T.; Tempone, A. G.; Lago, J. H. G.; Guimarães, E. F.; Kato, M. J. Leishmanicidal activity of an alkenylphenol from Piper malacophyllum is related to plasma membrane disruption. Exp. Parasitol. 2012, 132 (3), 383–387. https://doi.org/10.1016/j.exppara.2012.08.019
Pereira Filho, A. A.; Pessoa, G. C. D.; Yamaguchi, L. F.; Stanton, M. A.; Serravite, A. M.; Pereira, R. H. M.; Neves, W. S.; Kato, M. J. Larvicidal activity of essential oils from Piper species against strains of Aedes aegypti (Diptera: Culicidae) resistant to pyrethroids. Front. Plant Sci. 2021, 12. https://doi.org/10.3389/fpls.2021.685864
Pinheiro, B. G.; Silva, A. S. B.; Souza, G. E. P.; Figueiredo, J. G.; Cunha, F. Q.; Lahlou, S.; Silva, J. K. R.; Maia, J. G. S.; Sousa, P. J. C. Chemical composition, antinociceptive and anti-inflammatory effects in rodents of the essential oil of Peperomia serpens (Sw.) Loud. J. Ethnopharmacol. 2011, 138 (2), 479–486. https://doi.org/10.1016/j.jep.2011.09.037
Prabpree, A.; Sangsil, P.; Nualsri, C.; Nakkanong, K. Expression profile of phenylalanine ammonia-lyase (PAL) and phenolic content during early stages of graft development in bud grafted Hevea brasiliensis. Biocatal. Agric. Biotechnol. 2018, 14, 88–95. https://doi.org/10.1016/j.bcab.2018.02.010
Ramos, C. S.; Kato, M. J. Metabolism of neolignans from P. regnellii (Piperaceae) in the beetle Naupactus bipes (Coleoptera: Curculionidae). Chemoecology. 2013, 23 (3), 143–148. https://doi.org/10.1007/s00049-013-0129-y
Ramos, C. S.; Silva, M. W.; Moraes, M. M.; Almeida, A. V.; Vanin, S. A.; Kato, M. J. Metabolization of Insecticidal Amides from Leaves of Piper tuberculatum by Heraclydes hectorides and Naupactus bipes. J. Braz. Chem. Soc. 2020, 31 (4), 724–730. https://doi.org/10.21577/0103-5053.20190236
Regasini, L. O.; Cotinguiba, F.; Siqueira, J. R.; Bolzani, V. S.; Silva, D. H.; Furlan, M., Kato, M. J. Radical scavenging capacity of Piper arboreum and Piper tuberculatum (Piperaceae). Lat. Am. J. Pharm. 2008, 27 (6), 900–903.
Regasini, L. O.; Cotinguiba, F.; Passerini, G. D.; Bolzani, V. D. S.; Cicarelli, R. M. B.; Kato, M. J.; Furlan, M. Trypanocidal activity of Piper arboreum and Piper tuberculatum (Piperaceae). Rev. Bras. Farmacogn. 2009, 19 (1b), 199–203. https://doi.org/10.1590/S0102-695X2009000200003
Reigada, J. B.; Tcacenco, C. M.; Andrade, L. H.; Kato, M. J.; Porto, A. L.; Lago, J. H. G. Chemical constituents from Piper marginatum Jacq. (Piperaceae)—antifungal activities and kinetic resolution of (RS)-marginatumol by Candida antarctica lipase (Novozym 435). Tetrahedron Asymmetry 2007, 18 (9), 1054–1058. https://doi.org/10.1016/j.tetasy.2007.05.006
Rocha, J. C.; Bausell, H.; Bélanger-Quintana, A.; Bernstein, L.; Gökmen-Özel, H.; Jung, A.; MacDonald, A.; Rohr, F.; van Dam, E.; Heddrich-Ellerbrok, M. Development of a practical dietitian road map for the nutritional management of phenylketonuria (PKU) patients on pegvaliase. Mol. Genet. Metab. 2021, 28, 100771. https://doi.org/10.1016/j.ymgmr.2021.100771
Salazar, K. J. M.; Paredes, G. E. D.; Lluncor, L. R.; Young, M. C. M.; Kato, M. J. Chromenes of polyketide origin from Peperomia villipetiola. Phytochemistry. 2005, 66 (5), 573–579. https://doi.org/10.1016/j.phytochem.2005.01.003
Sant’Ana, M.; Souza, H. R.; Possebon, L.; Cornélio, M. L.; Riffo-Vasquez, Y.; Girol, A. P.; Oliani, S. M. Effect of piperlongumine during exposure to cigarette smoke reduces inflammation and lung injury. Pulm. Pharmacol. Ther. 2020, 61, 101896. https://doi.org/10.1016/j.pupt.2020.101896
Santos, R. A.; Ramos, C. S.; Young, M. C. M.; Pinheiro, T. G.; Amorim, A. M.; Kato, M. J.; Batista, R. Antifungal constituents from the roots of Piper dilatatum Rich. J. Chem. 2013, 2013, 160165. https://doi.org/10.1155/2013/160165
Sarkissian, C. N.; Kang, T. S.; Gámez, A.; Scriver, C. R.; Stevens, R. C. Evaluation of orally administered PEGylated phenylalanine ammonia lyase in mice for the treatment of Phenylketonuria, Mol. Gen. Metab. 2011, 104 (3), 249–254. https://doi.org/10.1016/j.ymgme.2011.06.016
Silva, R. V.; Navickiene, H. M. D.; Kato, M. J.; Bolzani, V. D. S.; Méda, C. I.; Young, M. C. M.; Furlan, M. Antifungal amides from Piper arboreum and Piper tuberculatum. Phytochemistry. 2002, 59 (5), 521–527. https://doi.org/10.1016/S0031-9422(01)00431-9
Silva, J. K. R.; Andrade, E. H. A.; Kato, M. J.; Carreira, L. M. M.; Guimaraes, E. F.; Maia, J. G. S. Antioxidant capacity and larvicidal and antifungal activities of essential oils and extracts from Piper krukoffii. Nat. Prod. Comm. 2011, 6 (9), 1361–1366. https://doi.org/10.1177/1934578X1100600936
Silva, H. A.; Yamaguchi, L. F.; Young, M. C. M.; Ramos, C. S.; Amorim, A. M. A.; Kato, M. J.; Batista, R. Antifungal piperamides from Piper mollicomum Kunth (Piperaceae). Eclet. Quim. J. 2018, 43 (1), 33–38. https://doi.org/10.26850/1678-4618eqj.v43.1.2018.p33-38
Silva, N. V.; Mazzafera, P.; Cesarino, I. Should I stay or should I go: are chlorogenic acids mobilized towards lignin biosynthesis? Phytochemistry. 2019a, 166, 112063. https://doi.org/10.1016/j.phytochem.2019.112063
Silva, A. C. A.; Diodato, J. S.; Castro, J. W.; Matias, E. F. F.; Silva, L. E.; Amaral, W.; Maia, B. H. L. N. S.; Ferriani, A. P.; Souza, A. K.; Quintans-Júnior, L. J.; Coutinho, H. D. M. Effect of the essential oils from Piper sp. and blue led lights in the enhancement of the antibiotic activity of drugs against mdr bacterial strains. J. Photochem. Photobiol. B. 2019b, 199, 111604. https://doi.org/10.1016/j.jphotobiol.2019.111604
Silva, M. A.; Fokoue, H. H.; Fialho, S. N.; Santos, A. P. A.; Rossi, N. R. D. L. P.; Gouveia, A. J.; Ferreira, A. S.; Passarini, G. M.; Garay, A. F. G.; Alfonso, J. J.; Soares, A. M.; Zanchi, F. B.; Kato, M. J.; Teles, C. B. G.; Kuehn, C. C. Antileishmanial activity evaluation of a natural amide and its synthetic analogs against Leishmania (V.) braziliensis: an integrated approach in vitro and in silico. Parasitol. Res. 2021, 120 (4), 2199–2218. https://doi.org/10.1007/s00436-021-07169-w
Souza, A. A.; Vessecchi, R.; Castro‐Gamboa, I.; Furlan, M. Combined use of tandem mass spectrometry and computational chemistry to study 2H‐chromenes from Piper aduncum. J. Mass Spectrom. 2019, 54 (7), 634–642. https://doi.org/10.1002/jms.4378
TAPPI - Technical Association of the Pulp and Paper Industry. Official Test Methods, Provisional Test Methods, and Useful Test Methods - Fibrous Materials and Pulp. Testing. Atlanta, 1979.
Toscano, S.; Ferrante, A.; Leonardi, C.; Romano, D. PAL activities in asparagus spears during storage after ammonium sulfate treatments. Postharvest Biol. Technol. 2018, 140, 34–41. https://doi.org/10.1016/j.postharvbio.2018.02.010
Tronchet, M.; Balagué, C.; Kroj, T.; Jouanin, L.; Roby, D. Cinnamyl alcohol dehydrogenases C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol. Plant Pathol. 2010, 11 (1), 83–92. https://doi.org/10.1111/j.1364-3703.2009.00578.x
Vanholme, R.; Meester, B.; Ralph, J.; Boerjan, W. Lignin biosynthesis and its integration into metabolism. Curr. Opin. Biotechnol. 2019, 56, 230–239. https://doi.org/10.1016/j.copbio.2019.02.018
Veronico, P.; Paciolla, C.; Pomar, F.; De Leonardis, S.; García-Ulloa, A.; Melillo, M. T. Changes in lignin biosynthesis and monomer composition in response to benzothiadiazole and root-knot nematode Meloidogyne incognita infection in tomato. J. Plant Physiol. 2018, 230, 40–50. https://doi.org/10.1016/j.jplph.2018.07.013
Vogel, K. R.; Arning, E.; Wasek, B. L.; Bottiglieri, T.; Gibson, K. M. Characterization of 2-(methylamino) alkanoic acid capacity to restrict blood-brain phenylalanine transport in Pahenu2 mice: Preliminary findings. Mol. Gen. Metab. 2013, 110 (Suppl), S71–S78. https://doi.org/10.1016/j.ymgme.2013.08.004
Watanabe, S. K.; Hemandez-Velazco, G.; Iturbe-Chiñas, F.; Lopez-Mungia, A. Phenylalanine ammonia lyase from Sporidiobolus pararoseus and Rhodosporidium toruloides: application for phenylalanine and tyrosine deamination. World J. Microbiol. Biotechnol. 1992, 8 (4), 406–410. https://doi.org/10.1007/BF01198755
Weiss, R.; Guebitz, G. M.; Pellis, A.; Nyanhongo, G. S. Harnessing the Power of Enzymes for Tailoring and Valorizing Lignin. Trends Biotechnol. 2020, 38 (11), 1215–1231. https://doi.org/10.1016/j.tibtech.2020.03.010
Yamaguchi, L. F.; Lago, J. H. G.; Tanizaki, T. M.; Di Mascio, P.; Kato, M. J. Antioxidant activity of prenylated hydroquinone and benzoic acid derivatives from Piper crassinervium Kunth. Phytochemistry. 2006, 67 (16), 1838–1843. https://doi.org/10.1016/j.phytochem.2006.03.001
Yoshida, N. C.; Benedetti, A. M.; Santos, R. A.; Ramos, C. S.; Batista, R.; Yamaguchi, L. F.; Kato, M. J. Alkenylphenols from Piper dilatatum and P. diospyrifolium. Phytochemistry Lett. 2018, 25, 136–140. https://doi.org/10.1016/j.phytol.2018.04.006
You, X.; Fang, H.; Wang, R.; Wang, G.-L.; Ning, Y. Phenylalanine ammonia lyases mediate broad-spectrum resistance to pathogens and insect pests in plants. Sci. Bull. 2020, 65 (17), 1425–1427. https://doi.org/10.1016/j.scib.2020.05.014