(+)-epi-α-Bisbolol Is the Wound-Healing Principle of Peperomia galioides: Investigation of the in Vivo Wound-Healing Activity of Related Terpenoids
- León F. Villegas ,
- Ana Marçalo ,
- Jennifer Martin ,
- Irma D. Fernández ,
- Holger Maldonado ,
- Abraham J. Vaisberg , and
- Gerald B. Hammond
Abstract
Bioassay-guided investigation of the ethanol extract of Peperomia galioides using a tensile strength method in mice as a monitor led to the isolation of epi-α-bisabolol (1) (ED50 155 μg/mL). An in vivo healing study of selected commercially available monoterpenoids yielded two bioactive compounds, α-bisabolol (2) and α-terpineol (3) (ED50 of 228 and 240 mg/g mouse, respectively).
†
Departamento de Ciencias Fisiológicas, Universidad Peruana Cayetano Heredia.
‡
University of Massachusetts Dartmouth.
§
Departamento de Química, Universidad Peruana Cayetano Heredia.
⊥
Laboratorios de Investigación y Desarrollo y Departamento de Microbiología, Universidad Peruana Cayetano Heredia.
∇
G.B.H. and A.J.V. share senior coauthorship.
*
To whom correspondence should be addressed. Tel: (508) 999-8865. Fax: (312) 910-6918. E-mail: [email protected]
Cited By
This article is cited by 54 publications.
- Hyun Seung Lim, Seong Keun Kim, Seung-Gyun Woo, Tae Hyun Kim, Soo-Jin Yeom, Wonshik Yong, Yoon-Joo Ko, Soo-Jung Kim, Seung-Goo Lee, Dae-Hee Lee. (−)-α-Bisabolol Production in Engineered Escherichia coli Expressing a Novel (−)-α-Bisabolol Synthase from the Globe Artichoke Cynara cardunculus var. Scolymus. Journal of Agricultural and Food Chemistry 2021, 69 (30) , 8492-8503. https://doi.org/10.1021/acs.jafc.1c02759
- Lucia Magnelli, Riccardo Caldini, Nicola Schiavone, Hisanori Suzuki and Marta Chevanne. Differentiating and Apoptotic Dose-Dependent Effects in (−)-α-Bisabolol-Treated Human Endothelial Cells. Journal of Natural Products 2010, 73 (4) , 523-526. https://doi.org/10.1021/np9003933
- José C. Aponte, Abraham J. Vaisberg, Rosario Rojas, Michel Sauvain, Walter H. Lewis, Gerardo Lamas, César Sarasara, Robert H. Gilman and Gerald B. Hammond. A Multipronged Approach to the Study of Peruvian Ethnomedicinal Plants: A Legacy of the ICBG-Peru Project. Journal of Natural Products 2009, 72 (3) , 524-526. https://doi.org/10.1021/np800630k
- Yu Rim Won, Kyung Jong Won, Do Yoon Kim, Mi Jung Kim, Bok Sil Hong, Hwan Myung Lee. Chemical Composition of Impatiens textori Miq. Flower Absolute and Its Potential Wound Repair and Anti-Melanogenesis-Promoting Activities in Skin Cells. Pharmaceuticals 2022, 15 (11) , 1397. https://doi.org/10.3390/ph15111397
- Anuar Salazar-Gómez, Angel Josabad Alonso-Castro. Medicinal Plants from Latin America with Wound Healing Activity: Ethnomedicine, Phytochemistry, Preclinical and Clinical Studies—A Review. Pharmaceuticals 2022, 15 (9) , 1095. https://doi.org/10.3390/ph15091095
- Elham Ramazani, Maryam Akaberi, Seyed Ahmad Emami, Zahra Tayarani-Najaran. Pharmacological and biological effects of alpha-bisabolol: An updated review of the molecular mechanisms. Life Sciences 2022, 304 , 120728. https://doi.org/10.1016/j.lfs.2022.120728
- Carolina Mesquita Germano, Natalia Ritter Ruas, Osmar Alves Lameira, Fernanda Naiara Santos Ribeiro, Tainá Teixeira Rocha, Alexandre Alves de Carvalho, João Pedro Miranda Rocha, José Eduardo Brasil Pereira Pinto, Suzan Kelly Vilela Bertolucci. Seasonal variations during two years in the essential oil of Lippia dulcis Trevir., an exotic aromatic of the Amazon. Journal of Essential Oil Research 2022, 34 (4) , 352-360. https://doi.org/10.1080/10412905.2022.2058635
- Lujain Bader Eddin, Niraj Kumar Jha, Sameer N. Goyal, Yogeeta O. Agrawal, Sandeep B. Subramanya, Salim M. A. Bastaki, Shreesh Ojha. Health Benefits, Pharmacological Effects, Molecular Mechanisms, and Therapeutic Potential of α-Bisabolol. Nutrients 2022, 14 (7) , 1370. https://doi.org/10.3390/nu14071370
- Shalini Ramalingam, Moola Joghee Nanjan Chandrasekar, Moola Joghee Nanjan. Plant-based Natural Products for Wound Healing: A Critical Review. Current Drug Research Reviews 2022, 14 (1) , 37-60. https://doi.org/10.2174/2589977513666211005095613
- Prakash Monika, Mathikere Naganna Chandraprabha, Annapoorni Rangarajan, P. Veena Waiker, Kotamballi N. Chidambara Murthy. Challenges in Healing Wound: Role of Complementary and Alternative Medicine. Frontiers in Nutrition 2022, 8 https://doi.org/10.3389/fnut.2021.791899
- Isabel Wilches, Priscila Jiménez-Castillo, Nancy Cuzco, M. Victoria Clos, Francesc Jiménez-Altayó, Eugenia Peñaherrera, Lourdes Jerves-Andrade, Vladimiro Tobar, Yvan Vander Heyden, Fabián Leon-Tamariz, Elisabet Vila. Anti-inflammatory and sedative activities of Peperomia galioides : in vivo studies in mice. Natural Product Research 2021, 35 (10) , 1657-1661. https://doi.org/10.1080/14786419.2019.1622104
- Mehdi Hassanpour, Fateme Hajihassani, Mina Abdollahpourasl, Omid Cheraghi, Nasser Aghamohamadzade, Reza Rahbargazi, Mohammad Nouri, Younes Pilehvar-Soltanahmadi, Nosratollah Zarghami, Abolfazl Akbarzadeh, Yunes Panahi, Amirhossein Sahebkar. Pathophysiological Effects of Sulfur Mustard on Skin and its Current Treatments: Possible Application of Phytochemicals. Combinatorial Chemistry & High Throughput Screening 2021, 24 (1) , 3-19. https://doi.org/10.2174/1386207323666200717150414
- Cláudia Leites Luchese, Juliana Both Engel, Isabel Cristina Tessaro. Disposable, reusable and biodegradable hygiene products. 2021, 421-454. https://doi.org/10.1016/B978-0-12-821485-5.00003-2
- A. Frankova, L. Vistejnova, T. Merinas-Amo, Z. Leheckova, I. Doskocil, J. Wong Soon, T. Kudera, F. Laupua, A. Alonso-Moraga, L. Kokoska. In vitro antibacterial activity of extracts from Samoan medicinal plants and their effect on proliferation and migration of human fibroblasts. Journal of Ethnopharmacology 2021, 264 , 113220. https://doi.org/10.1016/j.jep.2020.113220
- Subramani Parasuraman, Pandurangan Perumal. Wound Healing Agents from Natural Sources. 2021, 95-148. https://doi.org/10.1007/978-981-16-2677-7_4
- Hayate Javed, M. F. Nagoor Meeran, Sheikh Azimullah, Lujain Bader Eddin, Vivek Dhar Dwivedi, Niraj Kumar Jha, Shreesh Ojha. α-Bisabolol, a Dietary Bioactive Phytochemical Attenuates Dopaminergic Neurodegeneration through Modulation of Oxidative Stress, Neuroinflammation and Apoptosis in Rotenone-Induced Rat Model of Parkinson’s Disease. Biomolecules 2020, 10 (10) , 1421. https://doi.org/10.3390/biom10101421
- Saed Aldalaen, Maha Nasr, Riham I. El-Gogary. Angiogenesis and collagen promoting nutraceutical-loaded nanovesicles for wound healing. Journal of Drug Delivery Science and Technology 2020, 56 , 101548. https://doi.org/10.1016/j.jddst.2020.101548
- Laura Hévila I. Leite, Gerlânia O. Leite, Bruno Anderson F. da Silva, Sacha Aubrey A.R. Santos, Francisco Ernani A. Magalhães, Paula P. Menezes, Mairim R. Serafini, Claudener S. Teixeira, Renan G. Brito, Priscila L. Santos, José Galberto M. da Costa, Adriano A.S. Araújo, Lucindo J. Quintans-Júnior, Irwin R.A. de Menezes, Henrique Douglas M. Coutinho, Adriana Rolim Campos. Molecular mechanism underlying orofacial antinociceptive activity of Vanillosmopsis arborea Baker (Asteraceae) essential oil complexed with β-cyclodextrin. Phytomedicine 2019, 55 , 293-301. https://doi.org/10.1016/j.phymed.2018.09.173
- Mohamed Ali-Seyed, Kavitha Vijayaraghavan. Nutraceuticals for Wound Healing: A Special Focus on Chromolaena odorata as Guardian of Health with Broad Spectrum of Biological Activities. 2019, 541-562. https://doi.org/10.1007/978-3-030-04624-8_36
- Fabíola Fernandes Galvão Rodrigues, Aracélio Viana Colares, Carla de Fatima Alves Nonato, Fabío Fernandes Galvão-Rodrigues, Magaly Lima Mota, Maria Flaviana Bezerra Moraes Braga, José Galberto Martins da Costa. In vitro antimicrobial activity of the essential oil from Vanillosmopsis arborea Barker (Asteraceae) and its major constituent, α-bisabolol. Microbial Pathogenesis 2018, 125 , 144-149. https://doi.org/10.1016/j.micpath.2018.09.024
- Mariana Pohlmann, Karina Paese, Luíza Abrahão Frank, Silvia Stanisçuaski Guterres. Production, characterization and application of nanotechnology-based vegetable multi-component theospheres in nonwovens: A women's intimate hygiene approach. Textile Research Journal 2018, 88 (20) , 2292-2302. https://doi.org/10.1177/0040517517720500
- Mina Yarazavi, Ebrahim Noroozian. A novel sorbent based on carbon nanotube/amino-functionalized sol-gel for the headspace solid-phase microextraction of α-bisabolol from medicinal plant samples using experimental design. Journal of Separation Science 2018, 41 (10) , 2229-2236. https://doi.org/10.1002/jssc.201700993
- Gerlânia de Oliveira Leite, Assis Ecker, Rodrigo Lopes Seeger, Bárbara Nunes Krum, Thiago Henrique Lugokenski, Roselei Fachinetto, Jéssie Haigert Sudati, Nilda Vargas Barbosa, Caroline Wagner. Protective effect of (−)-α-bisabolol on rotenone-induced toxicity in Drosophila melanogaster. Canadian Journal of Physiology and Pharmacology 2018, 96 (4) , 359-365. https://doi.org/10.1139/cjpp-2017-0207
- Rita de Cássia da Silveira e Sá, Tamires Lima, Flávio da Nóbrega, Anna de Brito, Damião de Sousa. Analgesic-Like Activity of Essential Oil Constituents: An Update. International Journal of Molecular Sciences 2017, 18 (12) , 2392. https://doi.org/10.3390/ijms18122392
- Peter Giovannini, Melanie-Jayne R. Howes. Medicinal plants used to treat snakebite in Central America: Review and assessment of scientific evidence. Journal of Ethnopharmacology 2017, 199 , 240-256. https://doi.org/10.1016/j.jep.2017.02.011
- Kavitha Vijayaraghavan, Johanna Rajkumar, Syed Nasir Abbas Bukhari, Badr Al-Sayed, Mohammed Ali Seyed. Chromolaena odorata: A neglected weed with a wide spectrum of pharmacological activities. Molecular Medicine Reports 2017, 15 (3) , 1007-1016. https://doi.org/10.3892/mmr.2017.6133
- Yasmin Valero Gutierrez, Lydia F. Yamaguchi, Marcilio M. de Moraes, Christopher S. Jeffrey, Massuo J. Kato. Natural products from Peperomia: occurrence, biogenesis and bioactivity. Phytochemistry Reviews 2016, 15 (6) , 1009-1033. https://doi.org/10.1007/s11101-016-9461-5
- Arie Budovsky, Ludmila Yarmolinsky, Shimon Ben-Shabat. Effect of medicinal plants on wound healing. Wound Repair and Regeneration 2015, 23 (2) , 171-183. https://doi.org/10.1111/wrr.12274
- Krishna Vyas, Henry Vasconez. Wound Healing: Biologics, Skin Substitutes, Biomembranes and Scaffolds. Healthcare 2014, 2 (3) , 356-400. https://doi.org/10.3390/healthcare2030356
- Laura Marongiu, Marta Donini, Michele Bovi, Massimiliano Perduca, Federico Vivian, Alessandro Romeo, Sofia Mariotto, Hugo L. Monaco, Stefano Dusi. The inclusion into PLGA nanoparticles enables α-bisabolol to efficiently inhibit the human dendritic cell pro-inflammatory activity. Journal of Nanoparticle Research 2014, 16 (8) https://doi.org/10.1007/s11051-014-2554-4
- Rosana Barreto, Ricardo Albuquerque-Júnior, Adriano Araújo, Jackson Almeida, Márcio Santos, André Barreto, Josimari DeSantana, Pollyana Siqueira-Lima, Jullyana Quintans, Lucindo Quintans-Júnior. A Systematic Review of the Wound-Healing Effects of Monoterpenes and Iridoid Derivatives. Molecules 2014, 19 (1) , 846-862. https://doi.org/10.3390/molecules19010846
- Yun-Zhi Li, Dai-Yin Peng, Min Dai, Cao-Mao Xiao, Hong-Bo Jiang, Jing Huang. A new phenylpropanoid from Peperomia tetraphylla. Natural Product Research 2013, 27 (9) , 837-840. https://doi.org/10.1080/14786419.2012.704372
- Aracélio Viana Colares, Fernando Almeida-Souza, Noemi Nosomi Taniwaki, Celeste da Silva Freitas Souza, José Galberto Martins da Costa, Kátia da Silva Calabrese, Ana Lúcia Abreu-Silva. In Vitro Antileishmanial Activity of Essential Oil of Vanillosmopsis arborea (Asteraceae) Baker. Evidence-Based Complementary and Alternative Medicine 2013, 2013 , 1-7. https://doi.org/10.1155/2013/727042
- Gerlânia de Oliveira Leite, Cícera Norma Fernandes, Irwin Rose Alencar de Menezes, José Galberto Martins da Costa, Adriana Rolim Campos. Attenuation of visceral nociception by α-bisabolol in mice: investigation of mechanisms. Organic and Medicinal Chemistry Letters 2012, 2 (1) https://doi.org/10.1186/2191-2858-2-18
- Yun-Zhi Li, Ai-Ping Tong, Jing Huang. Two New Norlignans and a New Lignanamide from Peperomia tetraphylla. Chemistry & Biodiversity 2012, 9 (4) , 769-776. https://doi.org/10.1002/cbdv.201100138
- Ying Cui, Lingzhi Li, Li Zhang, Jianyu Li, Jun Gu, Haiying Gong, Peng Guo, Wei Tong. Enhancement and mechanism of transdermal absorption of terpene-induced propranolol hydrochloride. Archives of Pharmacal Research 2011, 34 (9) , 1477-1485. https://doi.org/10.1007/s12272-011-0909-2
- N. K. A. Santos, H. D. M. Coutinho, G. S. B. Viana, Fabíola F. G. Rodrigues, José G. M. Costa. Chemical characterization and synergistic antibiotic activity of volatile compounds from the essential oil of Vanillosmopsis arborea. Medicinal Chemistry Research 2011, 20 (5) , 637-641. https://doi.org/10.1007/s00044-010-9372-8
- Gerlânia de O. Leite, Laura H.I. Leite, Renata de S. Sampaio, Mariana Késsia A. Araruna, Irwin Rose A. de Menezes, José Galberto M. da Costa, Adriana R. Campos. (−)-α-Bisabolol attenuates visceral nociception and inflammation in mice. Fitoterapia 2011, 82 (2) , 208-211. https://doi.org/10.1016/j.fitote.2010.09.012
- Ifedayo V. Ogungbe, Rebecca A. Crouch, William A. Haber, William N. Setzer. Phytochemical Investigation of Verbesina Turbacensis Kunth: Trypanosome Cysteine Protease Inhibition by (–)-Bornyl Esters. Natural Product Communications 2010, 5 (8) , 1934578X1000500. https://doi.org/10.1177/1934578X1000500801
- Paola A. Robayo-Gama, Clara E. Quijano, Gustavo Morales, Jorge A. Pino. Composition of the Essential Oil From Leaves of Peperomia galioides HBK Grown in Colombia. Journal of Essential Oil Research 2010, 22 (4) , 307-309. https://doi.org/10.1080/10412905.2010.9700332
- A.M. Chibiryaev, A. Yermakova, I.V. Kozhevnikov. Chemical and phase equilibria calculation of α-pinene hydration in CO2-expanded liquid. The Journal of Supercritical Fluids 2010, 51 (3) , 295-305. https://doi.org/10.1016/j.supflu.2009.11.001
- Guy P. P. Kamatou, Alvaro M. Viljoen. A Review of the Application and Pharmacological Properties of α ‐Bisabolol and α ‐Bisabolol‐Rich Oils. Journal of the American Oil Chemists' Society 2010, 87 (1) , 1-7. https://doi.org/10.1007/s11746-009-1483-3
- Elisabetta Cavalieri, Christian Bergamini, Sofia Mariotto, Serena Leoni, Luigi Perbellini, Elena Darra, Hisanori Suzuki, Romana Fato, Giorgio Lenaz. Involvement of mitochondrial permeability transition pore opening in α-bisabolol induced apoptosis. FEBS Journal 2009, 276 (15) , 3990-4000. https://doi.org/10.1111/j.1742-4658.2009.07108.x
- SOU N. MATSUNAGA, ALEX B. GUENTHER, JIM P. GREENBERG, MARK POTOSNAK, MARIA PAPIEZ, TSUTOM HIURA, SHUNGO KATO, SATOSHI NISHIDA, PETER HARLEY, YOSHIZUMI KAJII. Leaf level emission measurement of sesquiterpenes and oxygenated sesquiterpenes from desert shrubs and temperate forest trees using a liquid extraction technique. GEOCHEMICAL JOURNAL 2009, 43 (3) , 179-189. https://doi.org/10.2343/geochemj.1.0017
- Vincenzo De Feo, Alberto Juarez Belaunde, Joe Guerrero Sandoval, Felice Senatore, Carmen Formisano. Antibacterial Activity and Composition of the Essential Oil of Peperomia Galioides HBK (Piperaceae) from Peru. Natural Product Communications 2008, 3 (6) , 1934578X0800300. https://doi.org/10.1177/1934578X0800300622
- B. Kumar, M. Vijayakumar, R. Govindarajan, P. Pushpangadan. Ethnopharmacological approaches to wound healing—Exploring medicinal plants of India. Journal of Ethnopharmacology 2007, 114 (2) , 103-113. https://doi.org/10.1016/j.jep.2007.08.010
- Gustavo Moura-Letts, León F. Villegas, Ana Marçalo, Abraham J. Vaisberg, Gerald B. Hammond. In Vivo Wound-Healing Activity of Oleanolic Acid Derived from the Acid Hydrolysis of Anredera d iffusa. Journal of Natural Products 2006, 69 (6) , 978-979. https://doi.org/10.1021/np0601152
- Alvaro M. Viljoen, Angela Gono-Bwalya, Guy P.P. Kamatou, K. Hűsnű C. Başer, Betűl Demirci. The Essential Oil Composition and Chemotaxonomy of Salvia stenophylla and its Allies S. repens and S. runcinata. Journal of Essential Oil Research 2006, 18 (sup1) , 37-45. https://doi.org/10.1080/10412905.2006.12067117
- . Biological Activity of Chamomile (Matricaria chamomilla L.) Extracts. Journal of the Korean Society of Food Science and Nutrition 2005, 446-450. https://doi.org/10.3746/jkfn.2005.34.4.446
- Yasuyuki HASHIDOKO. Ecochemical Studies of Interrelationships between Epiphytic Bacteria and Host Plants via Secondary Metabolites. Bioscience, Biotechnology, and Biochemistry 2005, 69 (8) , 1427-1441. https://doi.org/10.1271/bbb.69.1427
- Elisabetta Cavalieri, Sofia Mariotto, Cinzia Fabrizi, Alessandra Carcereri de Prati, Rossella Gottardo, Stefano Leone, Luigi Valentino Berra, Giuliana Maria Lauro, Anna Rosa Ciampa, Hisanori Suzuki. α-Bisabolol, a nontoxic natural compound, strongly induces apoptosis in glioma cells. Biochemical and Biophysical Research Communications 2004, 315 (3) , 589-594. https://doi.org/10.1016/j.bbrc.2004.01.088
- Alexander Pauli, Heinz Schilcher. Specific Selection of Essential Oil Compounds for Treatment of Children’s Infection Diseases. Pharmaceuticals 2004, 1 (1) , 1-30. https://doi.org/10.3390/pharm01010001
- Ming-Jen Cheng, Shoiw-Ju Lee, Ying-Ying Chang, Szu-Huei Wu, Ian-Lih Tsai, Bolleddula Jayaprakasam, Ih-Sheng Chen. Chemical and cytotoxic constituents from Peperomia sui. Phytochemistry 2003, 63 (5) , 603-608. https://doi.org/10.1016/S0031-9422(03)00183-3
- A Hernández-Ceruelos, E Madrigal-Bujaidar, C de la Cruz. Inhibitory effect of chamomile essential oil on the sister chromatid exchanges induced by daunorubicin and methyl methanesulfonate in mouse bone marrow. Toxicology Letters 2002, 135 (1-2) , 103-110. https://doi.org/10.1016/S0378-4274(02)00253-9