Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience

Melisa Hincapie Agudelo; Belfran Alcides Carbonell Medina; Claudia Marcela Arenas Gómez; Jean Paul Delgado

doi:10.15446/abc.v27n1.88309

Publicado

2021-09-27

Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience

Ambystoma mexicanum, un organismo modelo en biología del desarrollo y regeneración: experiencia colombiana

DOI:

https://doi.org/10.15446/abc.v27n1.88309

Palabras clave:

Animal model, Axololts, Development, Embryonic Development, salamanders (en)
salamandras, modelo animal, desarrollo embrionario, desarrollo, Ajolote (es)

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Autores/as

Melisa Hincapie Agudelo Universidad de Antioquia https://orcid.org/0000-0003-0240-5960
Belfran Alcides Carbonell Medina Universidad de Antioquia https://orcid.org/0000-0002-2965-0125
Claudia Marcela Arenas Gómez Universidad de Antioquia https://orcid.org/0000-0001-7905-5052
Jean Paul Delgado Universidad de Antioquia https://orcid.org/0000-0001-7134-6234

Resumen (en)
Resumen (es)

Ambystoma mexicanum is a urodele amphibian endemic to Xochimilco Lake in Mexico, it belongs to the salamander family Ambystomatidae. This species has frequently been used as model organism in developmental biology and regeneration laboratories around the world due to its broad regenerative capacities and adaptability to laboratory conditions. In this review we describe the establishment of the first colony of axolotls in Colombia to study tissue regeneration and our perspectives on the use A. mexicanum as a model organism in Colombia are discussed emphasizing its possible uses in regeneration and developmental biology

Ambystoma mexicanum es un anfibio urodelo endémico del lago Xochimilco en México, perteneciente a la familia de salamandras Ambystomatidae. Esta especie se ha empleado frecuentemente como organismo modelo en laboratorios de biología del desarrollo y regeneración alrededor del mundo, dadas sus amplias capacidades regenerativas y adaptabilidad en condiciones de laboratorio. En esta revisión, se describe el establecimiento de la primera colonia de ajolotes en Colombia, para adelantar estudios de regeneración de tejidos, y se discuten las perspectivas de A. mexicanum como organismo modelo en el país, enfatizando sus posibles usos en regeneración y biología del desarrollo

Referencias

Acosta-Galvis, A. R. (01 de enero de 2019). Lista de los Anfibios de Colombia. http://www.batrachia.com

Acosta-Galvis, A. R., and Gutiérrez-Lamus, D. L. (2012). A new species of salamander (Bolitoglossa: Plethodontidae) from the Cordillera Oriental of the Colombian Andes. Papéis Avulsos Zoología, 52(18), 201–18. https://doi.org/10.1590/S0031-10492012001800001 DOI: https://doi.org/10.1590/S0031-10492012001800001

Aguilar-Miguel, X., Legorreta, G. B., and Casas-Andreu, G. (2009). Reproducción ex situ en Ambystoma granulosum y Ambystoma lermaense (Amphibia: Ambystomatidae). Acta Zoológica Mexicana, 25(3), 443–54. https://doi.org/10.21829/azm.2009.253652 DOI: https://doi.org/10.21829/azm.2009.253652

Akle, V., Agudelo-Dueñas, N., Molina-Rodríguez, A., Kartchner, L. B., Ruth, A. M., Gonzalez, J. M., and Forero-Shelton, M. (2017). Establishment of Larval Zebrafish as an Animal Model to Investigate Trypanosoma cruzi Motility In Vivo. Journal of Visualized Experiments, 30(127), 56238. https://doi.org/10.3791/56238 DOI: https://doi.org/10.3791/56238

Arenas, C. M., Gómez-Molina, A., and Delgado, J. P. (2015). Maintaining plethodontid salamanders in the laboratory for regeneration studies. Methods in Molecular Biology, 1290, 71–8. https://doi.org/10.1007/978-1-4939-2495-0_5 DOI: https://doi.org/10.1007/978-1-4939-2495-0_5

Arenas Gómez, C. M., Woodcock, R. M., Smith, J. J., Voss, R. S., and Delgado, J. P. (2018). Using transcriptomics to enable a plethodontid salamander (Bolitoglossa ramosi) for limb regeneration research. BMC Genomics. 19, 704, 30253734. https://doi.org/10.1186/s12864-018-5076-0 DOI: https://doi.org/10.1186/s12864-018-5076-0

Arenas Gómez, C. M., Gomez Molina, A., Zapata, J. D., and Delgado, J. P. (2017). Limb regeneration in a direct-developing terrestrial salamander, Bolitoglossa ramosi (Caudata: Plethodontidae). Regeneration. 4(4), 227–35. https://doi.org/10.1002/reg2.93 DOI: https://doi.org/10.1002/reg2.93

Bahr, J. M. (2008). The chicken as a model organism. In P.M. Conn (Ed.). Sourcebook of Models for Biomedical Research. Humana Press. https://doi.org/10.1007/978-1-59745-285-4_18 DOI: https://doi.org/10.1007/978-1-59745-285-4_18

Bellairs, R., and Osmond, M. (2014). Atlas of Chick Development (3 Ed). Elsevier Inc. https://doi.org/10.1016/C2010-0-65149-2 DOI: https://doi.org/10.1016/C2010-0-65149-2

Blum, M, and Ott, T. (2018). Xenopus: An Undervalued Model Organism to Study and Model Human Genetic Disease. Cells Tissues Organs, 205(5-6), 303–13. https://doi.org/10.1159/000490898 DOI: https://doi.org/10.1159/000490898

Brandon, R. A. (1989). Natural history of the axolotl and its relationship to other ambystomatid salamanders (p. 13–24).Oxford University.

Brockes, J. P. (1998). Regeneration and cancer. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, 1377(1), 1–11. https://doi.org/10.1016/S0304-419X(97)00029-2 DOI: https://doi.org/10.1016/S0304-419X(97)00029-2

Brockes, J. P., and Kumar, A. (2008). Comparative aspects of animal regeneration. Annual Review of Cell and Developmental Biology, 24, 525–549. https://doi.org/10.1146/annurev.cellbio.24.110707.175336 DOI: https://doi.org/10.1146/annurev.cellbio.24.110707.175336

Browne, R. A., and Wanigasekera, G. (2000). Combined effects of salinity and temperature on survival and reproduction of five species of Artemia. Journal of Experimental Marine Biology and Ecology, 244(1), 44–29. https://doi.org/10.1016/S0022-0981(99)00125-2 DOI: https://doi.org/10.1016/S0022-0981(99)00125-2

Bruce, R. C. (2003). Chapter 13. Life Histories. Reproductive Biology and Phylogeny of Urodela. Western Carolina University.

Bryant, D. M., Johnson, K., Ditommaso, T., Tickle, T., Couger, M. B., Payzin-Dogru, D., Lee, T. J., Leigh, N. D., Kuo, T. -H., Davis, F. G., Bateman, J., Bryant, S., Guzikowski, A. R., Tsai, S. L., Coyne, S., Ye, W. W., Freeman Jr., R. M., Peshkin, L., … Whited, J. L. (2017). A Tissue-Mapped Axolotl De Novo Transcriptome Enables Identification of Limb Regeneration Factors. Cell Reports. 18(3), 762–76. https://doi.org/10.1016/j.celrep.2016.12.063. DOI: https://doi.org/10.1016/j.celrep.2016.12.063

Cano-Martínez, A., Vargas-González, A., Guarner-Lans, V., León-Olea, M., and Nieto-lima, B. (2010). Functional and structural regeneration in the axolotl heart (Ambystoma mexicanum) after partial ventricular amputation. 80(2):79–86.

Carbonell M, B., Bayona R, F., Garavito-Aguilar, Z., Parada B, C., Arboleda G, H. and Infante-Contreras, C. (2018). Hey1 gene expression patterns during the development of branchial arches and facial prominences. RevistaMVZ Córdoba, 23(3), 6813–25. DOI: https://doi.org/10.21897/rmvz.1370

Carbonell M, B., Zapata Cardona, J., and Delgado, J. (2021). Hydrogen peroxide is necessary during tail regeneration in juvenile axolotl. Developmental Dynamics : An Official Publication of the American Association of Anatomists. https://doi.org/10.1002/DVDY.386 DOI: https://doi.org/10.1002/dvdy.386

Carlson, M. R. J., Komine, Y., Bryant, S. V., and Gardiner, D. M. (2001). Expression of Hoxb13 and Hoxc10 in developing and regenerating axolotl limbs and tails. Developmental Biology, 229(2), 396–406. https://doi.org/10.1006/dbio.2000.0104 DOI: https://doi.org/10.1006/dbio.2000.0104

Charbonneau, A. M., Roy, S., and Tran, S. D. (2016). Oral-Facial Tissue Reconstruction in the Regenerative Axolotl. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 326(8), 489–502. https://doi.org/10.1002/jez.b.22723 DOI: https://doi.org/10.1002/jez.b.22723

Chaves, H., Villalba, C., Lagos, L., Vargas, R., Martínez-Wittinghan, F., Clavijo, C., and Camacho, M. (2003). Expresión de canales de potasio voltaje dependientes en ovocitos de Xenopus laevis (Amphibia). Acta Biológica Colombiana, 8, 59–67.

Chernoff, E. A. G., Stocum, D. L., Nye, H. L. D., and Cameron, J. A. (2003). Urodele spinal cord regeneration and related processes. Developmental Dynamics, 226(2), 295–307. https://doi.org/10.1002/dvdy.10240 DOI: https://doi.org/10.1002/dvdy.10240

Clarke, J. D. W., Alexander, R., and Holder, N. (1988). Regeneration of descending axons in the spinal cord of the axolotl. Neuroscience Letters, 89(1), 1–6. https://doi.org/10.1016/0304-3940(88)90471-5. DOI: https://doi.org/10.1016/0304-3940(88)90471-5

Contreras, V., Martínez-Meyer, E., Valiente, E., and Zambrano, L. (2009). Recent decline and potential distribution in the last remnant area of the microendemic Mexican axolotl (Ambystoma mexicanum). Biological Conservation, 142(12), 2881-2885. https://doi.org/10.1016/j.biocon.2009.07.008 DOI: https://doi.org/10.1016/j.biocon.2009.07.008

Crowner, A., Khatri, S., Blichmann, D., and Voss, S. R. (2019). Rediscovering the axolotl as a model for thyroid hormone dependent development. Frontiers Endocrinology, 10:1–6. https://doi.org/10.3389/fendo.2019.00237 DOI: https://doi.org/10.3389/fendo.2019.00237

Davaapil, H., Brockes, J. P., and Yun, M. H. (2017). Conserved and novel functions of programmed cellular senescence during vertebrate development. Development, 144(1), 106–14. https://doi.org/10.1242/dev.138222 DOI: https://doi.org/10.1242/dev.138222

DeNardo, D. (1995). Amphibians as Laboratory Animals. ILAR Journal 37(4), 173–81. https://doi.org/10.1093/ilar.37.4.173 DOI: https://doi.org/10.1093/ilar.37.4.173

Dwaraka, V. B., and Voss, S. R. (2019). Towards comparative analyses of salamander limb regeneration. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 336(2), 129-144. https://doi.org/10.1002/jez.b.22902 DOI: https://doi.org/10.1002/jez.b.22902

Echeverri, K., and Tanaka, E. M. (2003). Electroporation as a tool to study in vivo spinal cord regeneration. Developmental Dynamics, 226(2), 418–25. https://doi.org/10.1002/dvdy.10238 DOI: https://doi.org/10.1002/dvdy.10238

Echeverri, K., Clarke, J. D. W., and Tanaka, E. M. (2001). In vivo imaging indicates muscle fiber dedifferentiation is a major contributor to the regenerating tail blastema. Developmental Biology, 236(1), 151–64. https://doi.org/10.1006/dbio.2001.0312 DOI: https://doi.org/10.1006/dbio.2001.0312

Echeverri, K., and Tanaka, E. M. (2002). Ectoderm to mesoderm lineage switching during axolotl tail regeneration. Science, 298(5600), 1993–1996. https://doi.org/10.1126/science.1077804 DOI: https://doi.org/10.1126/science.1077804

Eisthen, H. L., and Krause, B. C. (2012). Ambiguities in the relationship between gonadal steroids and reproduction in axolotls (Ambystoma mexicanum). General and Comparative Endocrinology, 76(3), 472–80. https://doi.org/10.1016/j.ygcen.2011.12.034 DOI: https://doi.org/10.1016/j.ygcen.2011.12.034

Farkas, J. E., and Monaghan, J. R. (2015). Housing and Maintenance of Ambystoma mexicanum. En A. Kumar, and A. Simon (Ed.). Salamanders in Regeneration Research (pp. 27–46). https://doi.org/10.1007/978-1-4939-2495-0_3 DOI: https://doi.org/10.1007/978-1-4939-2495-0_3

Fei, J. -F., Lou, W. P. -K., Knapp, D., Murawala, P., Gerber, T., Taniguchi, Y., Nowoshilow, S., Khattak, S., and Tanaka, E. M. (2018). Application and optimization of CRISPR–Cas9-mediated genome engineering in axolotl (Ambystoma mexicanum). Nature Protocols, 13, 2908–2943. https://doi.org/10.1038/s41596-018-0071-0 DOI: https://doi.org/10.1038/s41596-018-0071-0

Fei, J. -F., Schuez, M., Tazaki, A., Taniguchi, Y., Roensch, K., and Tanaka, E. M. (2014). CRISPR-mediated genomic deletion of Sox2 in the axolotl shows a requirement in spinal cord neural stem cell amplification during tail regeneration. Stem Cell Reports, 3(3), 444–459. https://doi.org/10.1016/j.stemcr.2014.06.018 DOI: https://doi.org/10.1016/j.stemcr.2014.06.018

Fior, J. (2014). Salamander Regeneration as a Model for Developing Novel Regenerative and Anticancer Therapies. Journal of Cancer, 5(8), 715–719. https://doi.org/10.7150/jca.9971 DOI: https://doi.org/10.7150/jca.9971

Frankham, R., Ballou, J., Ralls, K., Eldridge, M., Dudash, M. R., Fenster, C. B., Lacy, R. C., and Sunnucks, P. (2017). Genetic management of fragmented animal and plant populations. Oxford Scholarship Online. https://doi.org/10.1093/oso/9780198783398.001.0001 DOI: https://doi.org/10.1093/oso/9780198783398.001.0001

Freitas, P. D., Lovely, A. M., and Monaghan, J. R. (2019). Investigating Nrg1 Signaling in the Regenerating Axolotl Spinal Cord Using Multiplexed FISH. Developmental Neurobiology, 79(5), 453–67. https://doi.org/10.1002/dneu.22670 DOI: https://doi.org/10.1002/dneu.22670

Fröbisch, N. B., Bickelmann, C., Olori, J. C., and Witzmann, F. (2015). Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development. Nature, 527, 231-234. https://doi.org/10.1038/nature15397 DOI: https://doi.org/10.1038/nature15397

Fröbisch, N. B., and Shubin, N. H. (2011). Salamander limb development: integrating genes, morphology, and fossils. Developmental Dynamics, 240(5), 1087–1099. https://doi.org/10.1002/dvdy.22629 DOI: https://doi.org/10.1002/dvdy.22629

Galeano, S., Urbina, J., Gutiérrez Cárdenas, P. D. A., Rivera-Correa, M., and Páez, V. (2006). Los anfibios de Colombia, diversidad y estado del conocimiento. In M. E. Cháves and M. Santamaría (Eds.). Informe Nacional sobre el Avance en el Conocimiento y la Información de la Biodiversidad1998-2004 (pp. 106–118). Instituto de Investigaciones Biológicas Alexander von Humboldt.

Gerber, T., Murawala, P., Knapp, D., Masselink, W., Schuez, M., Hermann, S., Gac-Santel, M., Nowoshilow, S., Kageyama, J., Khattak, S., Currie, J. D., Camp, J. G., Tanaka, E. M., and Treutlein, B. (2018). Single-cell analysis uncovers convergence of cell identities during axolotl limb regeneration. Science, 362(6413), eaaq0681. https://doi.org/10.1126/science.aaq0681 DOI: https://doi.org/10.1126/science.aaq0681

Ghosh, S., Roy, S., Séguin, C., Bryant, S. V., and Gardiner, D. M. (2008). Analysis of the expression and function of Wnt-5a and Wnt-5b in developing and regenerating axolotl (Ambystoma mexicanum) limbs. Development, Growth & Differentiation. 50(4), 289–97. https://doi.org/10.1111/j.1440-169X.2008.01000.x DOI: https://doi.org/10.1111/j.1440-169X.2008.01000.x

Godwin, J., Debuque, R., Salimova, E., Rosenthal, N. A. (2017). Heart regeneration in the salamander relies on macrophage-mediated control of fibroblast activation and the extracellular landscape. NPJ Regenerative Medicine, 2(22). https://doi.org/10.1038/s41536-017-0027-y DOI: https://doi.org/10.1038/s41536-017-0027-y

Grainger, R. M. (2012). Xenopus tropicalis as a Model Organism for Genetics and Genomics: Past, Present, and Future. Methods in Molecular Biology (Vol. 917, pp. 3–15). NIH Public Access. https://doi.org/10.1007/978-1-61779-992-1_1 DOI: https://doi.org/10.1007/978-1-61779-992-1_1

Gresens, J. (2004). An introduction to the Mexican axolotl (Ambystoma mexicanum). Lab Anim, 33, 41–7. https://doi.org/10.1038/laban1004-41 DOI: https://doi.org/10.1038/laban1004-41

Haas, B. J., and Whited, J. L. (2017). Advances in Decoding Axolotl Limb Regeneration. Trends in Genetics, 33(8), 553–65. https://doi.org/10.1016/j.tig.2017.05.006 DOI: https://doi.org/10.1016/j.tig.2017.05.006

Heasman, J. (2006). Patterning the early Xenopus embryo. Development, 133(7), 1205–1217. https://doi.org/10.1242/dev.02304 DOI: https://doi.org/10.1242/dev.02304

Hogan, B. M., Verkade, H., Lieschke, G. J., and Heath, J. K. (2008). Manipulation of gene expression during zebrafish embryonic development using transient approaches. Methods in Molecular Biology, 469, 273–300. https://doi.org/10.1007/978-1-60327-469-2_19 DOI: https://doi.org/10.1007/978-1-60327-469-2_19

Horb, M., Wlizla, M., Abu-Daya, A., McNamara, S., Gajdasik, D., Igawa, T., Suzuki, A., Ogino, H., Noble, A., Nicolas, M., Lafond, T., Boujard, D., Audic, Y., Guillet, B., Kashiwagi, A., Kashiwagi, K., Suzuki, N., Tazawa, I., Ochi, H., … Guille, M. (2019). Xenopus resources: Transgenic, inbred and mutant animals, training opportunities, and web-based support. Frontiers in Physiology, 10, 387. https://doi.org/10.3389/fphys.2019.00387 DOI: https://doi.org/10.3389/fphys.2019.00387

Huggins, P., Johnson, C. K., Schoergendorfer, A., Putta, S., Bathke, A. C., Stromberg, A. J., and Voss, S. R. (2012). Identification of differentially expressed thyroid hormone responsive genes from the brain of the Mexican Axolotl (Ambystoma mexicanum). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology; 155(1), 128–35. https://doi.org/10.1016/j.cbpc.2011.03.006. DOI: https://doi.org/10.1016/j.cbpc.2011.03.006

Jelinek R. (1982). Use of chick embryo in screening for embryotoxicity. Teratogenesis, Carcinogenesis, and Mutagenesis. 2(3-4), 255–61. https://doi.org/10.1002/1520-6866(1990)2:3/4<255::AID-TCM1770020307>3.0.CO;2-M DOI: https://doi.org/10.1002/1520-6866(1990)2:3/4<255::AID-TCM1770020307>3.0.CO;2-M

Johnson, C. K., and Voss, S. R. (2013). Salamander Paedomorphosis. Linking Thyroid Hormone to Life History and Life Cycle Evolution. Current Topics in Developmental Biology (Vol. 103, 1st Ed). Elsevier Inc. https://doi.org/10.1016/B978-0-12-385979-2.00008-3 DOI: https://doi.org/10.1016/B978-0-12-385979-2.00008-3

Joven, A., Elewa, A., y Simon, A. (2019). Model systems for regeneration: Salamanders. Development, 146(14):dev167700. https://doi.org/10.1242/dev.167700 DOI: https://doi.org/10.1242/dev.167700

Joven, A., and Simon, A. (2018). Homeostatic and regenerative neurogenesis in salamanders. Progress in Neurobiology, 170, 81–98. https://doi.org/10.1016/j.pneurobio.2018.04.006 DOI: https://doi.org/10.1016/j.pneurobio.2018.04.006

Keinath, M. C., Timoshevskiy, V. A., Timoshevskaya, N. Y., Tsonis, P. A., Voss, S. R., and Smith, J. J. (2015a). Initial characterization of the large genome of the salamander Ambystoma mexicanum using shotgun and laser capture chromosome sequencing. Scientific Reports, 5, 16413. https://doi.org/10.1038/srep16413

Keinath, M. C., Timoshevskiy, V. A., Timoshevskaya, N. Y., Tsonis, P. A., Voss, S. R., and Smith, J. J. (2015b). Initial characterization of the large genome of the salamander Ambystoma mexicanum using shotgun and laser capture chromosome sequencing. Scientific Reports, 5, 16413. https://doi.org/10.1038/srep16413 DOI: https://doi.org/10.1038/srep16413

Kerney, R. R. , Hanken, J., and Blackburn, D. C. (2018). Early limb patterning in the direct-developing salamander Plethodon cinereus revealed by sox9 and col2a1. Evolution & Development, 20(3-4), 100–7. https://doi.org/10.1111/ede.12250 DOI: https://doi.org/10.1111/ede.12250

Khattak, S., Murawala, P., Andreas, H., Kappert, V., Schuez, M., Sandoval-Guzmán, T., Crawford, K., and Tanaka, E. M. (2014). Optimized axolotl (Ambystoma mexicanum) husbandry, breeding, metamorphosis, transgenesis and tamoxifen-mediated recombination. Nature Protocols, 9, 529–40. https://doi.org/10.1038/nprot.2014.040. DOI: https://doi.org/10.1038/nprot.2014.040

Khattak, S., Richter, T., and Tanaka, E. M. (2009). Generation of transgenic axolotls (Ambystoma mexicanum). Cold Spring Harb Protoc, 4. https://doi.org/10.1101/pdb.prot5264 DOI: https://doi.org/10.1101/pdb.prot5264

Khattak, S., Schuez, M., Richter, T., Knapp, D., Haigo, S. L., Sandoval-Guzmán, T., Hradlikova, K., Duemmler, A., Kerney, R., and Tanaka, E. M. (2013). Germline transgenic methods for tracking cells and testing gene function during regeneration in the axolotl. Stem Cell Reports, 1(1), 90–103. https://doi.org/10.1016/j.stemcr.2013.03.002 DOI: https://doi.org/10.1016/j.stemcr.2013.03.002

Khattak, S., and Tanaka, E. M. (2015). Transgenesis in axolotl (Ambystoma mexicanum). Methods in Molecular Biology, 1290, 269–77. doi: https://doi.org/10.1007/978-1-4939-2495-0_21 DOI: https://doi.org/10.1007/978-1-4939-2495-0_21

Khudoley, V. V., and Eliseiv, V. V. (1979). Multiple melanomas in the axolotl Ambystoma mexicanum. Journal of the National Cancer Institute, 63, 101–3.

Kim, W. (1996). Amphibian Maintenance Facilities at Sogang. University Korea.

Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Developmental Dynamics, 203(3), 253–310. https://doi.org/10.1002/aja.1002030302 DOI: https://doi.org/10.1002/aja.1002030302

Kragl, M., Knapp, D., Nacu, E., Khattak, S., Maden, M., Epperlein, H. H., and Tanaka, E. M. (2009). Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature, 460, 60–65. https://doi.org/10.1038/nature08152 DOI: https://doi.org/10.1038/nature08152

Kumar, A., Godwin, J. W., Gates, P. B., Garza-Garcia, A. A., and Brockes, J. P. (2007). Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science, 318(5851), 772–777. https://doi.org/10.1126/science.1147710 DOI: https://doi.org/10.1126/science.1147710

Lannoo, M. J., Lowcock, L., and Bogart, J. P. (1989). Sibling cannibalism in noncannibal morph Ambystoma tigrinum larvae and its correlation with high growth rates and early metamorphosis. Canadian Journal of Zoology, 67(8), 1911–1914. https://doi.org/10.1139/z89-273 DOI: https://doi.org/10.1139/z89-273

Ponomarevaa, L. V., Athippozhyb, A., Thorson, J. S., and Voss, S. R. (2015). Using Ambystoma mexicanum (Mexican Axolotl) Embryos, Chemical Genetics, and 2 Microarray Analysis to Identify Signaling Pathways Associated with Tissue Regeneration. Comparative Biochemistry and Physiology, 178, 128–135. https://doi.org/10.1016/j.cbpc.2015.06.004

Lavery, D. L., and Hoppler, S. (2008). Gain-of-Function and Loss-of-Function Strategies in Xenopus. Methods in Molecular Biology, 469, 401–15. https://doi.org/10.1007/978-1-60327-469-25 DOI: https://doi.org/10.1007/978-1-60327-469-25

Lin, H. -J., Lee, S. -H., Wu, J. -L., Duann, Y. -F., and Chen, J. -Y. (2013). Development of Cre-loxP technology in zebrafish to study the regulation of fish reproduction. Fish Physiology and Biochemistry, 39, 1525–1539. https://doi.org/10.1007/s10695-013-9806-6 DOI: https://doi.org/10.1007/s10695-013-9806-6

Marcellini, S., González, F., Sarrazin, A. F., Pabón-Mora, N., Benítez, M., Piñeyro-Nelson, A., Rezende, G. L., Maldonado, E., Schneider, P. N., Grizante, M. B., Da Fonseca, R. N., Vergara-Silva, F., Suaza-Gaviria, V., Zumajo-Cardona, C., Zattara, E. E., Casasa, S., Suárez-Baron, H., and Brown, F. D. (2017). Evolutionary Developmental Biology (Evo-Devo) Research in Latin America. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 328(1-2), 5–40. https://doi.org/10.1002/jez.b.22687 DOI: https://doi.org/10.1002/jez.b.22687

Marques, I. J., Lupi, E., and Mercader, N. (2019). Model systems for regeneration: Zebrafish. Development, 146(18), dev167692. https://doi.org/10.1242/dev.167692 DOI: https://doi.org/10.1242/dev.167692

McCusker, C., and Gardiner, D. M. (2011). The axolotl model for regeneration and aging research: A mini-review. Gerontology, 57, 565–71. https://doi.org/10.1159/000323761 DOI: https://doi.org/10.1159/000323761

Mchedlishvili, L., Mazurov, V., Grassme, K. S., Goehler, K., Robl, B., Tazaki, A., Roensch, K., Duemmler, A., and Tanaka, E. M. (2012). Reconstitution of the central and peripheral nervous system during salamander tail regeneration. Proceedings of the National Academy of Sciences of the United States of America, 109(34), E2258-E2266. https://doi.org/10.1073/pnas.1116738109 DOI: https://doi.org/10.1073/pnas.1116738109

Meyers, J. R. (2018). Zebrafish: Development of a Vertebrate Model Organism. Current Protocols Essential Laboratory Techniques, 16(1). https://doi.org/10.1002/cpet.19 DOI: https://doi.org/10.1002/cpet.19

Meza Lasso, D., Peña Barrera, C., Bayona Rodríguez, F., Carbonell Madina, B., and Infante Contreras, C. (2016). Expresión de los genes serrate1 y notch1 durante el desarrollo del tercio medio facial del embrión de pollo. Acta Biológica Colombiana, 21(1), 175–82. https://doi.org/10.15446/abc.v21n1.49336 DOI: https://doi.org/10.15446/abc.v21n1.49336

Monaghan, J. R., Stier, A. C., Michonneau, F., Smith, M. D., Pasch, B., Maden, M., and Seifert, A.W. (2014). Experimentally induced metamorphosis in axolotls reduces regenerative rate and fidelity. Regeneration, 1, 2–14. https://doi.org/10.1002/reg2.8 DOI: https://doi.org/10.1002/reg2.8

Mueller, W. A., Hassel, M., and Grealy, M. (2015). Development of Important Model Species II: Vertebrates. Development and Reproduction in Humans and Animal Model Species. Springer, Berlin, Heidelberg. DOI: https://doi.org/10.1007/978-3-662-43784-1

Mummery, C., Wilmut, S. I., van de Stolpe, A., Roelen, B. A. J. (2011). Chapter 2 - Embryonic Development. Stem Cells (pp. 29–43). Elsevier. https://doi.org/10.1016/B978-0-12-381535-4.10002-4 DOI: https://doi.org/10.1016/B978-0-12-381535-4.10002-4

Nacu, E., Glausch, M., Le, H. Q., Damanik, F. F. R. , Schuez, M., Knapp, D., Khattak, S., Richter, T., and Tanaka, E. M. (2013). Connective tissue cells, but not muscle cells, are involved in establishing the proximo-distal outcome of limb regeneration in the axolotl. Development, 140(3), 513–518. https://doi.org/10.1242/dev.081752 DOI: https://doi.org/10.1242/dev.081752

Nowoshilow, S., Schloissnig, S., Fei, J. -F., Dahl, A., Pang, A. W. C., Pippel, M., Winkler, S., Hastie, A. R., Young, G., Roscito, J. G., Falcon, F., Knapp, D., Powell, S., Cruz, A., Cao, H., Habermann, B., Hiller, M., Tanaka, E. M., and Myers, E. W. (2018a). The axolotl genome and the evolution of key tissue formation regulators. Nature, 554, 50-55. https://doi.org/10.1038/nature25458 DOI: https://doi.org/10.1038/nature25458

Nye, H. L. D., Cameron, J. A., Chernoff, E. A. G., and Stocum, D. L. (2003). Extending the table of stages of normal development of the axolotl: Limb development. Developmental Dynamics, 226, 555–560. https://doi.org/10.1002/dvdy.10237 DOI: https://doi.org/10.1002/dvdy.10237

O’Rourke, D. P. (2002). Reptiles and amphibians as laboratory animals. Laboratory Animals, 31, 43–47. https://doi.org/10.1038/5000167

Page, R. B., and Voss, S. R. (2009). Induction of metamorphosis in axolotls (Ambystoma mexicanum). Cold Spring Harbor Protocols, pdb.prot5268. https://doi.org/10.1101/pdb.prot5268 DOI: https://doi.org/10.1101/pdb.prot5268

Parra-Olea, G., García-París, M., and Wake, D.B. (2004). Molecular diversification of salamanders of the tropical American genus Bolitoglossa (Caudata: Plethodontidae) and its evolutionary and biogeographical implications. Biological Journal of the Linnean Society, 81(3), 325–346. https://doi.org/10.1111/j.1095-8312.2003.00303.x DOI: https://doi.org/10.1111/j.1095-8312.2003.00303.x

Phipps, L. S., Marshall, L., Dorey, K., and Amaya, E. (2020). Model systems for regeneration: Xenopus. Development, 147(6):dev180844. https://doi.org/10.1242/dev.180844 DOI: https://doi.org/10.1242/dev.180844

Ponomareva, L. V., Athippozhy, A., Thorson, J. S., and Voss, S. R. (2015). Using Ambystoma mexicanum (Mexican axolotl) embryos, chemical genetics, and microarray analysis to identify signaling pathways associated with tissue regeneration. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 178, 128–35. https://doi.org/10.1016/j.cbpc.2015.06.004 DOI: https://doi.org/10.1016/j.cbpc.2015.06.004

Banerjee, B. (2014). Models for Studies in Regenerative Medicine. Perspect. Regen. Med., In: Perspectives in Regenerative Medicine (pp. 105–114). Springer, New Delhi. https://doi.org/10.1007/978-81-322-2053-4_7 DOI: https://doi.org/10.1007/978-81-322-2053-4_7

Robles-Mendoza, C., García-Basilio C and Vanegas-Pérez R. (2009). Maintenance media for the axolotl Ambystoma mexicanum juveniles (Amphibia : Caudata). Hidrobiológica, 19, 205–210.

Roy, S., and Gatien, S. (2008). Regeneration in axolotls: a model to aim for! Experimental Gerontology, 43(11), 968–73. https://doi.org/10.1016/j.exger.2008.09.003 DOI: https://doi.org/10.1016/j.exger.2008.09.003

Sabin, K., Jiang, P., Gearhart, M., Stewart, R., and Echeverri, K. (2019). AP-1cFos/JunB/miR-200a regulate the pro-regenerative glial cell response during axolotl spinal cord regeneration. Communications Biology, 2, 91. https://doi.org/10.1038/s42003-019-0335-4 DOI: https://doi.org/10.1038/s42003-019-0335-4

Salazar, M., and Arango, N. (2014). The effect of carbamate in the development of upper limb in white mice (Mus musculus). Revista de la Asociación Colombiana de Ciencias Biológicas. 26, 9–17.

Sanor, L. D., Flowers, G. P., and Crews, C. M. (2020). Multiplex CRISPR/Cas screen in regenerating haploid limbs of chimeric axolotls. Elife, 9, 1–18. https://doi.org/10.7554/eLife.48511 DOI: https://doi.org/10.7554/eLife.48511

Schreckenberg, G. M., and Jacobson, A. G. (1975). Normal stages of development of the axolotl, Ambystoma mexicanum. Developmental Biology, 42(2), 391–400. https://doi.org/10.1016/0012-1606(75)90343-7 DOI: https://doi.org/10.1016/0012-1606(75)90343-7

Seifert, A. W., Monaghan, J. R., Smith, M. D., Pasch, B., Stier, A. C., Michonneau, F., and Maden, M. (2012). The influence of fundamental traits on mechanisms controlling appendage regeneration. Biological Reviews, 87(2), 330-345. https://doi.org/10.1111/j.1469-185X.2011.00199.x DOI: https://doi.org/10.1111/j.1469-185X.2011.00199.x

Shaffer, H. B. (1993). Phylogenetics of Model Organisms: The Laboratory Axolotl, Ambystoma mexicanum. Systematic Biology, 42(4), 508–22. https://doi.org/10.1093/sysbio/42.4.508 DOI: https://doi.org/10.1093/sysbio/42.4.508

Silva-González, N., Páez, V. P., and Bock, B. C. (2011). Morphological variation in Bolitoglossa vallecula (Amphibia: Caudata: Plethodontidae) in the Cordillera Central of Colombia. Actualidades Biológicas, 33(95), 251–60.

Simon, A., and Tanaka, E. M. (2013). Limb regeneration. WIREs Developmental Biology, 2(2), 291–300. https://doi.org/10.1002/wdev.73 DOI: https://doi.org/10.1002/wdev.73

Simon, H. -G., and Odelberg, S. (2015). Maintaining Eastern newts (Notophthalmus viridescens) for regeneration research. Methods in Molecular Biology, 1290, 17–25. https://doi.org/10.1007/978-1-4939-2495-0_2 DOI: https://doi.org/10.1007/978-1-4939-2495-0_2

Smith, J. J., Putta, S., Walker, J. A., Kump, D. K., Samuels, A. K., Monaghan, J. R., Weisrock, D. W., Staben, C., and Voss, S. R. (2005). Sal-Site: Integrating new and existing ambystomatid salamander research and informational resources. BMC Genomics, 6, 181. https://doi.org/10.1186/1471-2164-6-181 DOI: https://doi.org/10.1186/1471-2164-6-181

Smith, J. J., Timoshevskaya, N., Timoshevskiy, V. A., Keinath, M. C., Hardy, D., and Voss, S. R. (2019). A chromosome-scale assembly of the axolotl genome. Genome Research, 29, 317–24. https://doi.org/10.1101/gr.241901.118 DOI: https://doi.org/10.1101/gr.241901.118

Sobkow, L., Epperlein, H. H., Herklotz, S., Straube, W. L., and Tanaka, E. M. (2006). A germline GFP transgenic axolotl and its use to track cell fate: Dual origin of the fin mesenchyme during development and the fate of blood cells during regeneration. Developmental Biology, 290(2), 386–97. https://doi.org/10.1016/j.ydbio.2005.11.037 DOI: https://doi.org/10.1016/j.ydbio.2005.11.037

Sommer, R. J. (2009). The future of evo–devo: Model systems and evolutionary theory. Nature Reviews Genetics, 10, 416-422. https://doi.org/10.1038/nrg2567 DOI: https://doi.org/10.1038/nrg2567

Stoller, M. L., and Fekete, D. M. (2016).Tol2-mediated delivery of miRNAs to the chicken otocyst using plasmid electroporation. Methods in Molecular Biology, 1427, 7–42. https://doi.org/10.1007/978-1-4939-3615-1_2 DOI: https://doi.org/10.1007/978-1-4939-3615-1_2

Suetsugu-Maki, R., Maki, N., Nakamura, K., Sumanas, S., Zhu, J., Del Rio-Tsonis, K., and Tsonis, P. A. (2012). Lens regeneration in axolotl: new evidence of developmental plasticity. BMC Biology, 10, 103. https://doi.org/10.1186/1741-7007-10-103 DOI: https://doi.org/10.1186/1741-7007-10-103

Tanaka, E. M. (2016). The Molecular and Cellular Choreography of Appendage Regeneration. Cell, 165(7), 1598–608. https://doi.org/10.1016/j.cell.2016.05.038 DOI: https://doi.org/10.1016/j.cell.2016.05.038

Tank, P. W., Carlson, B. M., and Connelly, T. G. (1976). A staging system for forelimb regeneration in the axolotl, Ambystoma mexicanum. Journal of Morphology, 150(1), 117–28. https://doi.org/10.1002/jmor.1051500106 DOI: https://doi.org/10.1002/jmor.1051500106

Tazaki, A., Tanaka, E. M., and Fei, J. F. (2017). Salamander spinal cord regeneration: The ultimate positive control in vertebrate spinal cord regeneration. Developmental Biology, 432(1), 63–71. https://doi.org/10.1016/j.ydbio.2017.09.034 DOI: https://doi.org/10.1016/j.ydbio.2017.09.034

Thygesen, M. M., Lauridsen, H., Pedersen, M., Orlowski, D., Mikkelsen, T. W., and Rasmussen, M. M. (2019). A clinically relevant blunt spinal cord injury model in the regeneration competent axolotl (Ambystoma mexicanum) tail. Experimental and Therapeutic Medicine, 17, 2322–2328. https://doi.org/10.3892/etm.2019.7193 DOI: https://doi.org/10.3892/etm.2019.7193

Tsonis, P. A., and Del Rio-Tsonis, K. (2004). Lens and retina regeneration: transdifferentiation, 78(2), 161–172. https://doi.org/10.1016/j.exer.2003.10.022 DOI: https://doi.org/10.1016/j.exer.2003.10.022

Vieira, W. A., Wells, K. M., and McCusker, C. D. (2019). Advancements to the Axolotl Model for Regeneration and Aging. Gerontology, 66, 212–222. https://doi.org/10.1159/000504294 DOI: https://doi.org/10.1159/000504294

Voss, S. R., Kump, D. K., Walker, J. A., Shaffer, H. B., and Voss, G. J. (2012).Thyroid hormone responsive QTL and the evolution of paedomorphic salamanders. Heredity, 109, 293–298. https://doi.org/10.1038/hdy.2012.41 DOI: https://doi.org/10.1038/hdy.2012.41

Voss, S. R., Palumbo, A., Nagarajan, R., Gardiner, D. M., Muneoka, K., Stromberg, A. J., and Athippozhy, A. T. (2015). Gene expression during the first 28 days of axolotl limb regeneration I: Experimental design and global analysis of gene expression. Regeneration, 2(3), 120–136. https://doi.org/10.1002/reg2.37 DOI: https://doi.org/10.1002/reg2.37

Voss, S. R., Epperlein, H. H., and Tanaka, E. M. (2009). Ambystoma mexicanum, the axolotl: a versatile amphibian model for regeneration, development, and evolution studies. Cold Spring Harbor Protocols, 2009(8). https://doi.org/10.1101/pdb.emo128 DOI: https://doi.org/10.1101/pdb.emo128

Whited, J., Lehoczky, J. A., and Tabin, C. J.(2012). Inducible genetic system for the axolotl. Proceedings of the National Academy of Sciences, 109(34), 13662-13667. https://doi.org/10.1073/pnas.1211816109 DOI: https://doi.org/10.1073/pnas.1211816109

Wiens, J. J. .(2007). The Amphibian Tree of Life. Bulletin of the American Museum of Natural History, Number 297. In D. Frost, T. Grant, T. Faivovich, R. Bain, A. Haas, C. Haddad, R. De Sá, A. Channing, M. Wilkinson and S. Donnella. The Quarterly Review of Biology, 82(1), 55–56. https://doi.org/10.1086/513362 DOI: https://doi.org/10.1206/0003-0090(2006)297[0001:TATOL]2.0.CO;2

Wildy, E. L., and Lynn, E. (2000). Cannibalism in larvae of the long-toed salamander, Ambystoma macrodactylum [Thesis]. The Pennsylvania State University.

Yun, M. H. (2018). Cellular senescence in tissue repair: Every cloud has a silver lining. The International Journal Developmental Biology, 62, 591–604. https://doi.org/10.1387/ijdb.180081my DOI: https://doi.org/10.1387/ijdb.180081my

Yun, M. H., Davaapil, H., and Brockes, J. P. (2015). Recurrent turnover of senescent cells during regeneration of a complex structure. Elife, 4, 25942455. https://doi.org/10.7554/eLife.05505 DOI: https://doi.org/10.7554/eLife.05505

Zambrano, L., Vega, E., Herrera M., L. G., Prado, E., and Reynoso, V. H. (2007). A population matrix model and population viability analysis to predict the fate of endangered species in highly managed water systems. Animal Conservation, 10, 297–303. https://doi.org/10.1111/j.1469-1795.2007.00105.x DOI: https://doi.org/10.1111/j.1469-1795.2007.00105.x

Zaragoza, C., Gomez-Guerrero, C., Martin-Ventura, J. L., Blanco-Colio, L., Lavin, B., Mallavia, B., Tarin, C., Mas, S., Ortiz, A., Egido, J., Ortiz, A., and Egido, J. (2011). Animal models of cardiovascular diseases. Journal of Biomedicine and Biotechnology, 2011, 497841. https://doi.org/10.1155/2011/497841 DOI: https://doi.org/10.1155/2011/497841

Zon, L. (2016). Modeling human diseases: an education in interactions and interdisciplinary approaches. Disease Models & Mechanisms, 9(6), 597–600. https://doi.org/10.1242/dmm.025882 DOI: https://doi.org/10.1242/dmm.025882

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Hincapie Agudelo, M., Carbonell Medina, B. A., Arenas Gómez, C. M. y Delgado, J. P. (2021). Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience. Acta Biológica Colombiana, 27(1), 113–126. https://doi.org/10.15446/abc.v27n1.88309

ACM

[1]

Hincapie Agudelo, M., Carbonell Medina, B.A., Arenas Gómez, C.M. y Delgado, J.P. 2021. Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience. Acta Biológica Colombiana. 27, 1 (sep. 2021), 113–126. DOI:https://doi.org/10.15446/abc.v27n1.88309.

ACS

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Hincapie Agudelo, M.; Carbonell Medina, B. A.; Arenas Gómez, C. M.; Delgado, J. P. Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience. Acta biol. Colomb. 2021, 27, 113-126.

ABNT

HINCAPIE AGUDELO, M.; CARBONELL MEDINA, B. A.; ARENAS GÓMEZ, C. M.; DELGADO, J. P. Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience. Acta Biológica Colombiana, [S. l.], v. 27, n. 1, p. 113–126, 2021. DOI: 10.15446/abc.v27n1.88309. Disponível em: https://revistas.unal.edu.co/index.php/actabiol/article/view/88309. Acesso em: 18 abr. 2024.

Chicago

Hincapie Agudelo, Melisa, Belfran Alcides Carbonell Medina, Claudia Marcela Arenas Gómez, y Jean Paul Delgado. 2021. «Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience». Acta Biológica Colombiana 27 (1):113-26. https://doi.org/10.15446/abc.v27n1.88309.

Harvard

Hincapie Agudelo, M., Carbonell Medina, B. A., Arenas Gómez, C. M. y Delgado, J. P. (2021) «Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience», Acta Biológica Colombiana, 27(1), pp. 113–126. doi: 10.15446/abc.v27n1.88309.

IEEE

[1]

M. Hincapie Agudelo, B. A. Carbonell Medina, C. M. Arenas Gómez, y J. P. Delgado, «Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience», Acta biol. Colomb., vol. 27, n.º 1, pp. 113–126, sep. 2021.

MLA

Hincapie Agudelo, M., B. A. Carbonell Medina, C. M. Arenas Gómez, y J. P. Delgado. «Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience». Acta Biológica Colombiana, vol. 27, n.º 1, septiembre de 2021, pp. 113-26, doi:10.15446/abc.v27n1.88309.

Turabian

Hincapie Agudelo, Melisa, Belfran Alcides Carbonell Medina, Claudia Marcela Arenas Gómez, y Jean Paul Delgado. «Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience». Acta Biológica Colombiana 27, no. 1 (septiembre 21, 2021): 113–126. Accedido abril 18, 2024. https://revistas.unal.edu.co/index.php/actabiol/article/view/88309.

Vancouver

1.

Hincapie Agudelo M, Carbonell Medina BA, Arenas Gómez CM, Delgado JP. Ambystoma mexicanum, a model organism in developmental biology and regeneration: a colombian experience. Acta biol. Colomb. [Internet]. 21 de septiembre de 2021 [citado 18 de abril de 2024];27(1):113-26. Disponible en: https://revistas.unal.edu.co/index.php/actabiol/article/view/88309

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