Axolotl: A resourceful vertebrate model for regeneration and beyond.

Ambystoma mexicanum aging cancer immune system regenerative medicine transgenesis

Journal

Developmental dynamics : an official publication of the American Association of Anatomists
ISSN: 1097-0177
Titre abrégé: Dev Dyn
Pays: United States
ID NLM: 9201927

Informations de publication

Date de publication:
12 2022
Historique:
revised: 04 07 2022
received: 02 06 2022
accepted: 21 07 2022
pubmed: 31 7 2022
medline: 3 12 2022
entrez: 30 7 2022
Statut: ppublish

Résumé

The regenerative capacity varies significantly among the animal kingdom. Successful regeneration program in some animals results in the functional restoration of tissues and lost structures. Among the highly regenerative animals, axolotl provides multiple experimental advantages with its many extraordinary characteristics. It has been positioned as a regeneration model organism due to its exceptional renewal capacity, including the internal organs, central nervous system, and appendages, in a scar-free manner. In addition to this unique regeneration ability, the observed low cancer incidence, its resistance to carcinogens, and the reversing effect of its cell extract on neoplasms strongly suggest its usability in cancer research. Axolotl's longevity and efficient utilization of several anti-aging mechanisms underline its potential to be employed in aging studies.

Identifiants

pubmed: 35906989
doi: 10.1002/dvdy.520
doi:

Types de publication

Journal Article Review Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1914-1933

Informations de copyright

© 2022 American Association for Anatomy.

Références

Elchaninov A, Sukhikh G, Fatkhudinov T. Evolution of regeneration in animals: a tangled story. Front Ecol Evol. 2021;9:621686. doi:10.3389/fevo.2021.621686
Michalopoulos G, Cianciulli HD, Novotny AR, Kligerman AD, Strom SC, Jirtle RL. Liver regeneration studies with rat hepatocytes in primary culture. Cancer Res. 1982;42(11):4673-4682.
Steinberg B. Bone marrow regeneration in experimental benzene intoxication. Blood. 1949;4(5):550-556.
Barker N. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol. 2014;15(1):19-33. doi:10.1038/nrm3721
Mimeault M, Hauke R, Batra SK. Stem cells: a revolution in therapeutics-recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies. Clin Pharmacol Ther. 2007;82(3):252-264. doi:10.1038/sj.clpt.6100301
Mast BA, Schultz GS. Interactions of cytokines, growth factors, and proteases in acute and chronic wounds. Wound Repair Regen. 1996;4(4):411-420. doi:10.1046/j.1524-475X.1996.40404.x
Laplace-Builhé B, Bahraoui S, Jorgensen C, Djouad F. From the basis of epimorphic regeneration to enhanced regenerative therapies. Front Cell Dev Biol. 2020;8:605120. doi:10.3389/fcell.2020.605120
Murad R, Macias-Muñoz A, Wong A, Ma X, Mortazavi A. Coordinated gene expression and chromatin regulation during hydra head regeneration. Genome Biol Evol. 2021;13(12):evab221. doi:10.1093/gbe/evab221
Cary GA, Wolff A, Zueva O, Pattinato J, Hinman VF. Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa. BMC Biol. 2019;17(1):16. doi:10.1186/s12915-019-0633-9
Cloutier JK, McMann CL, Oderberg IM, Reddien PW. activin-2 is required for regeneration of polarity on the planarian anterior-posterior axis. PLoS Genet. 2021;17(3):e1009466. doi:10.1371/journal.pgen.1009466
Shaffer HB. Phylogenetics of model organisms: the laboratory axolotl, Ambystoma mexicanum. Syst Biol. 1993;42(4):508-522. doi:10.1093/sysbio/42.4.508
Safi R, Bertrand S, Marchand O, et al. The axolotl (Ambystoma mexicanum), a neotenic amphibian, expresses functional thyroid hormone receptors. Endocrinology. 2004;145(2):760-772. doi:10.1210/en.2003-0913
Malacinski GM. The Mexican axolotl, Ambystoma mexicanum: its biology and developmental genetics, and its autonomous cell-lethal genes. Am Zool. 1978;18(2):195-206. doi:10.1093/icb/18.2.195
Roy S, Lévesque M. Limb regeneration in axolotl: Is it superhealing? ScientificWorldJournal. 2006;6(Suppl 1):12-25. doi:10.1100/tsw.2006.324
Makanae A, Tajika Y, Nishimura K, Saito N, Tanaka JI, Satoh A. Neural regulation in tooth regeneration of Ambystoma mexicanum. Sci Rep. 2020;10(1):9323. doi:10.1038/s41598-020-66142-2
Demircan T, Hacıbektaşoğlu H, Sibai M, et al. Preclinical molecular signatures of spinal cord functional restoration: optimizing the metamorphic axolotl (Ambystoma mexicanum) model in regenerative medicine. Omics J Integr Biol. 2020;24(6):370-378. doi:10.1089/omi.2020.0024
Amamoto R, Huerta VGL, Takahashi E, et al. Adult axolotls can regenerate original neuronal diversity in response to brain injury. Elife. 2016;5:e13998. doi:10.7554/eLife.13998
Pedersen K, Rasmussen RK, Dittrich A, Lauridsen H. Cardiac regeneration in the axolotl is unaffected by alterations in leukocyte numbers induced by lipopolysaccharide and prednisolone. BMC Res Notes. 2021;14(1):157. doi:10.1186/s13104-021-05574-z
Saito N, Nishimura K, Makanae A, Satoh A. Fgf- and Bmp-signaling regulate gill regeneration in Ambystoma mexicanum. Dev Biol. 2019;452(2):104-113. doi:10.1016/j.ydbio.2019.04.011
McCusker C, Bryant SV, Gardiner DM. The axolotl limb blastema: cellular and molecular mechanisms driving blastema formation and limb regeneration in tetrapods. Regen Oxf Engl. 2015;2(2):54-71. doi:10.1002/reg2.32
Khattak S, Murawala P, Andreas H, et al. Optimized axolotl (Ambystoma mexicanum) husbandry, breeding, metamorphosis, transgenesis and tamoxifen-mediated recombination. Nat Protoc. 2014;9(3):529-540. doi:10.1038/nprot.2014.040
Khattak S, Tanaka EM. Transgenesis in axolotl (Ambystoma mexicanum). Methods Mol Biol Clifton NJ. 2015;1290:269-277. doi:10.1007/978-1-4939-2495-0_21
Epperlein HH, Radomski N, Wonka F, et al. Immunohistochemical demonstration of hyaluronan and its possible involvement in axolotl neural crest cell migration. J Struct Biol. 2000;132(1):19-32. doi:10.1006/jsbi.2000.4298
Keinath MC, Davidian A, Timoshevskiy V, Timoshevskaya N, Gall JG. Characterization of axolotl lampbrush chromosomes by fluorescence in situ hybridization and immunostaining. Exp Cell Res. 2021;401(2):112523. doi:10.1016/j.yexcr.2021.112523
Sánchez-Islas E, León-Olea M. Histochemical and immunohistochemical localization of neuronal nitric oxide synthase in the olfactory epithelium of the axolotl, Ambystoma mexicanum. Nitric Oxide Biol Chem. 2001;5(4):302-316. doi:10.1006/niox.2001.0347
Wu CH, Huang TY, Chen BS, Chiou LL, Lee HS. Long-duration muscle dedifferentiation during limb regeneration in axolotls. PLOS One. 2015;10(2):e0116068. doi:10.1371/journal.pone.0116068
Brown DD, Cai L. Amphibian metamorphosis. Dev Biol. 2007;306(1):20-33. doi:10.1016/j.ydbio.2007.03.021
Furlow JD, Neff ES. A developmental switch induced by thyroid hormone: Xenopus laevis metamorphosis. Trends Endocrinol Metab. 2006;17(2):40-47. doi:10.1016/j.tem.2006.01.007
Crowner A, Khatri S, Blichmann D, Voss SR. Rediscovering the Axolotl as a model for thyroid hormone dependent development. Front Endocrinol. 2019;10:237. doi:10.3389/fendo.2019.00237
Page RB, Voss SR. Induction of metamorphosis in axolotls (Ambystoma mexicanum). Cold Spring Harb Protoc. 2009;2009(8):pdb.prot5268. doi:10.1101/pdb.prot5268
Demircan T, Ovezmyradov G, Yıldırım B, et al. Experimentally induced metamorphosis in highly regenerative axolotl (Ambystoma mexicanum) under constant diet restructures microbiota. Sci Rep. 2018;8(1):10974. doi:10.1038/s41598-018-29373-y
Monaghan JR, Stier AC, Michonneau F, et al. Experimentally induced metamorphosis in axolotls reduces regenerative rate and fidelity. Regen Oxf Engl. 2014;1(1):2-14. doi:10.1002/reg2.8
Goodwin PA. A comparison of regeneration rates and metamorphosis in Triturus and Amblystoma. Growth. 1946;10:75-87.
Sibai M, Altuntaş E, Süzek BE, et al. Comparison of protein expression profile of limb regeneration between neotenic and metamorphic axolotl. Biochem Biophys Res Commun. 2020;522(2):428-434. doi:10.1016/j.bbrc.2019.11.118
Vincent CD, Rost F, Masselink W, Brusch L, Tanaka EM. Cellular dynamics underlying regeneration of appropriate segment number during axolotl tail regeneration. BMC Dev Biol. 2015;15(1):48. doi:10.1186/s12861-015-0098-1
Cano-Martínez A, Vargas-González A, Guarner-Lans V, Prado-Zayago E, León-Oleda M, Nieto-Lima B. Functional and structural regeneration in the axolotl heart (Ambystoma mexicanum) after partial ventricular amputation. Arch Cardiol Mex. 2010;80(2):79-86.
Ohashi A, Saito N, Kashimoto R, Furukawa S, Yamamoto S, Satoh A. Axolotl liver regeneration is accomplished via compensatory congestion mechanisms regulated by ERK signaling after partial hepatectomy. Dev Dyn. 2021;250(6):838-851. doi:10.1002/dvdy.262
Jensen TB, Giunta P, Schultz NG, et al. Lung injury in axolotl salamanders induces an organ-wide proliferation response. Dev Dyn. 2021;250(6):866-879. doi:10.1002/dvdy.315
Monaghan JR, Walker JA, Page RB, Putta S, Beachy CK, Voss SR. Early gene expression during natural spinal cord regeneration in the salamander Ambystoma mexicanum. J Neurochem. 2007;101(1):27-40. doi:10.1111/j.1471-4159.2006.04344.x
Maden M, Manwell LA, Ormerod BK. Proliferation zones in the axolotl brain and regeneration of the telencephalon. Neural Develop. 2013;8:1. doi:10.1186/1749-8104-8-1
Suetsugu-Maki R, Maki N, Nakamura K, et al. Lens regeneration in axolotl: new evidence of developmental plasticity. BMC Biol. 2012;10:103. doi:10.1186/1741-7007-10-103
Erler P, Sweeney A, Monaghan JR. Regulation of injury-induced ovarian regeneration by activation of oogonial stem cells. Stem Cells Dayt Ohio. 2017;35(1):236-247. doi:10.1002/stem.2504
Tank PW, Carlson BM, Connelly TG. A staging system for forelimb regeneration in the axolotl, Ambystoma mexicanum. J Morphol. 1976;150(1):117-128. doi:10.1002/jmor.1051500106
Endo T, Bryant SV, Gardiner DM. A stepwise model system for limb regeneration. Dev Biol. 2004;270(1):135-145. doi:10.1016/j.ydbio.2004.02.016
Ferris DR, Satoh A, Mandefro B, Cummings GM, Gardiner DM, Rugg EL. Ex vivo generation of a functional and regenerative wound epithelium from axolotl (Ambystoma mexicanum) skin. Dev Growth Differ. 2010;52(8):715-724. doi:10.1111/j.1440-169X.2010.01208.x
Satoh A, Graham GMC, Bryant SV, Gardiner DM. Neurotrophic regulation of epidermal dedifferentiation during wound healing and limb regeneration in the axolotl (Ambystoma mexicanum). Dev Biol. 2008;319(2):321-335. doi:10.1016/j.ydbio.2008.04.030
Satoh A, Bryant SV, Gardiner DM. Nerve signaling regulates basal keratinocyte proliferation in the blastema apical epithelial cap in the axolotl (Ambystoma mexicanum). Dev Biol. 2012;366(2):374-381. doi:10.1016/j.ydbio.2012.03.022
Makanae A, Satoh A. Early regulation of axolotl limb regeneration. Anat Rec. 2012;295(10):1566-1574. doi:10.1002/ar.22529
Zhu W, Pao GM, Satoh A, et al. Activation of germline-specific genes is required for limb regeneration in the Mexican axolotl. Dev Biol. 2012;370(1):42-51. doi:10.1016/j.ydbio.2012.07.021
Fei JF, Schuez M, Knapp D, Taniguchi Y, Drechsel DN, Tanaka EM. Efficient gene knockin in axolotl and its use to test the role of satellite cells in limb regeneration. Proc Natl Acad Sci U S A. 2017;114(47):12501-12506. doi:10.1073/pnas.1706855114
Leigh ND, Dunlap GS, Johnson K, et al. Transcriptomic landscape of the blastema niche in regenerating adult axolotl limbs at single-cell resolution. Nat Commun. 2018;9(1):5153. doi:10.1038/s41467-018-07604-0
Singer M. On the nature of the neurotrophic phenomenon in Urodele limb regeneration. Am Zool. 1978;18(4):829-841. doi:10.1093/icb/18.4.829
Satoh A, Makanae A, Nishimoto Y, Mitogawa K. FGF and BMP derived from dorsal root ganglia regulate blastema induction in limb regeneration in Ambystoma mexicanum. Dev Biol. 2016;417(1):114-125. doi:10.1016/j.ydbio.2016.07.005
Satoh A, Makanae A, Hirata A, Satou Y. Blastema induction in aneurogenic state and Prrx-1 regulation by MMPs and FGFs in Ambystoma mexicanum limb regeneration. Dev Biol. 2011;355(2):263-274. doi:10.1016/j.ydbio.2011.04.017
Makanae A, Mitogawa K, Satoh A. Co-operative Bmp- and Fgf-signaling inputs convert skin wound healing to limb formation in urodele amphibians. Dev Biol. 2014;396(1):57-66. doi:10.1016/j.ydbio.2014.09.021
Makanae A, Hirata A, Honjo Y, Mitogawa K, Satoh A. Nerve independent limb induction in axolotls. Dev Biol. 2013;381(1):213-226. doi:10.1016/j.ydbio.2013.05.010
Farkas JE, Freitas PD, Bryant DM, Whited JL, Monaghan JR. Neuregulin-1 signaling is essential for nerve-dependent axolotl limb regeneration. Dev Camb Engl. 2016;143(15):2724-2731. doi:10.1242/dev.133363
Vincent E, Villiard E, Sader F, Dhakal S, Kwok BH, Roy S. BMP signaling is essential for sustaining proximo-distal progression in regenerating axolotl limbs. Dev Camb Engl. 2020;147(14):dev170829. doi:10.1242/dev.170829
Nacu E, Gromberg E, Oliveira CR, Drechsel D, Tanaka EM. FGF8 and SHH substitute for anterior-posterior tissue interactions to induce limb regeneration. Nature. 2016;533(7603):407-410. doi:10.1038/nature17972
Roy S, Gardiner DM. Cyclopamine induces digit loss in regenerating axolotl limbs. J Exp Zool. 2002;293(2):186-190. doi:10.1002/jez.10110
Stopper GF, Wagner GP. Inhibition of Sonic hedgehog signaling leads to posterior digit loss in Ambystoma mexicanum: parallels to natural digit reduction in urodeles. Dev Dyn. 2007;236(1):321-331. doi:10.1002/dvdy.21025
Kim WS, Stocum DL. Effects of retinoids on regenerating limbs: comparison of retinoic acid and arotinoid at different amputation levels. Rouxs Arch Dev Biol. 1986;195(7):455-463. doi:10.1007/BF00375749
Kim WS, Stocum DL. Retinoic acid modifies positional memory in the anteroposterior axis of regenerating axolotl limbs. Dev Biol. 1986;114(1):170-179. doi:10.1016/0012-1606(86)90393-3
Ludolph DC, Cameron JA, Stocum DL. The effect of retinoic acid on positional memory in the dorsoventral axis of regenerating axolotl limbs. Dev Biol. 1990;140(1):41-52. doi:10.1016/0012-1606(90)90051-j
Vieira WA, Wells KM, Raymond MJ, De Souza L, Garcia E, McCusker CD. FGF, BMP, and RA signaling are sufficient for the induction of complete limb regeneration from non-regenerating wounds on Ambystoma mexicanum limbs. Dev Biol. 2019;451(2):146-157. doi:10.1016/j.ydbio.2019.04.008
Carlson MR, Komine Y, Bryant SV, Gardiner DM. Expression of Hoxb13 and Hoxc10 in developing and regenerating Axolotl limbs and tails. Dev Biol. 2001;229(2):396-406. doi:10.1006/dbio.2000.0104
Torok MA, Gardiner DM, Shubin NH, Bryant SV. Expression of HoxD genes in developing and regenerating axolotl limbs. Dev Biol. 1998;200(2):225-233. doi:10.1006/dbio.1998.8956
Lévesque M, Villiard E, Roy S. Skin wound healing in axolotls: a scarless process. J Exp Zoolog B Mol Dev Evol. 2010;314(8):684-697. doi:10.1002/jez.b.21371
Yang EV, Gardiner DM, Carlson MR, Nugas CA, Bryant SV. Expression of Mmp-9 and related matrix metalloproteinase genes during axolotl limb regeneration. Dev Dyn. 1999;216(1):2-9. doi:10.1002/(SICI)1097-0177(199909)216:1<2::AID-DVDY2>3.0.CO;2-P
Vinarsky V, Atkinson DL, Stevenson TJ, Keating MT, Odelberg SJ. Normal newt limb regeneration requires matrix metalloproteinase function. Dev Biol. 2005;279(1):86-98. doi:10.1016/j.ydbio.2004.12.003
Lévesque M, Gatien S, Finnson K, et al. Transforming growth factor: beta signaling is essential for limb regeneration in axolotls. PloS One. 2007;2(11):e1227. doi:10.1371/journal.pone.0001227
Sader F, Denis JF, Laref H, Roy S. Epithelial to mesenchymal transition is mediated by both TGF-β canonical and non-canonical signaling during axolotl limb regeneration. Sci Rep. 2019;9(1):1144. doi:10.1038/s41598-018-38171-5
Kawakami Y, Rodriguez Esteban C, Raya M, et al. Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev. 2006;20(23):3232-3237. doi:10.1101/gad.1475106
Wischin S, Castañeda-Patlán C, Robles-Flores M, Chimal-Monroy J. Data on chemical activation of Wnt/β-catenin during axolotl limb regeneration. Data Brief. 2017;11:562-566. doi:10.1016/j.dib.2017.02.048
Wischin S, Castañeda-Patlán C, Robles-Flores M, Chimal-Monroy J. Chemical activation of Wnt/β-catenin signalling inhibits innervation and causes skeletal tissue malformations during axolotl limb regeneration. Mech Dev. 2017;144:182-190. doi:10.1016/j.mod.2017.01.005
Yun MH, Gates PB, Brockes JP. Regulation of p53 is critical for vertebrate limb regeneration. Proc Natl Acad Sci U S A. 2013;110(43):17392-17397. doi:10.1073/pnas.1310519110
Wang MH, Wu CH, Huang TY, et al. Nerve-mediated expression of histone deacetylases regulates limb regeneration in axolotls. Dev Biol. 2019;449(2):122-131. doi:10.1016/j.ydbio.2019.02.011
Whited JL, Lehoczky JA, Tabin CJ. Inducible genetic system for the axolotl. Proc Natl Acad Sci U S A. 2012;109(34):13662-13667. doi:10.1073/pnas.1211816109
Cook PJ, Ju BG, Telese F, Wang X, Glass CK, Rosenfeld MG. Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature. 2009;458(7238):591-596. doi:10.1038/nature07849
Sousounis K, Bryant DM, Martinez Fernandez J, et al. Eya2 promotes cell cycle progression by regulating DNA damage response during vertebrate limb regeneration. Elife. 2020;9:e51217. doi:10.7554/eLife.51217
García-Lepe UO, Torres-Dimas E, Espinal-Centeno A, Cruz-Ramírez A, Bermúdez-Cruz RM. Evidence of requirement for homologous-mediated DNA repair during Ambystoma mexicanum limb regeneration. Dev Dyn. 2022;251(6):1035-1053. doi:10.1002/dvdy.455
Smith JJ, Putta S, Zhu W, et al. Genic regions of a large salamander genome contain long introns and novel genes. BMC Genomics. 2009;10(1):1-11. doi:10.1186/1471-2164-10-19
Nowoshilow S, Schloissnig S, Fei JF, et al. The axolotl genome and the evolution of key tissue formation regulators. Nature. 2018;554(7690):50-55. doi:10.1038/nature25458
Smith JJ, Timoshevskaya N, Timoshevskiy VA, Keinath MC, Hardy D, Voss SR. A chromosome-scale assembly of the axolotl genome. Genome Res. 2019;29(2):317-324. doi:10.1101/gr.241901.118
Purushothaman S, Elewa A, Seifert AW. Fgf-signaling is compartmentalized within the mesenchyme and controls proliferation during salamander limb development. Elife. 2019;8:e48507. doi:10.7554/eLife.48507
Schnapp E, Kragl M, Rubin L, Tanaka EM. Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Dev Camb Engl. 2005;132(14):3243-3253. doi:10.1242/dev.01906
Bryant DM, Johnson K, DiTommaso T, et al. A tissue-mapped axolotl De novo transcriptome enables identification of limb regeneration factors. Cell Rep. 2017;18(3):762-776. doi:10.1016/j.celrep.2016.12.063
Gardiner DM, Blumberg B, Komine Y, Bryant SV. Regulation of HoxA expression in developing and regenerating axolotl limbs. Dev Camb Engl. 1995;121(6):1731-1741.
Sibai M, Parlayan C, Tuğlu P, Öztürk G, Demircan T. Integrative analysis of axolotl gene expression data from regenerative and wound healing limb tissues. Sci Rep. 2019;9(1):20280. doi:10.1038/s41598-019-56829-6
Qin T, Fan CM, Wang TZ, et al. Single-cell RNA-seq reveals novel mitochondria-related musculoskeletal cell populations during adult axolotl limb regeneration process. Cell Death Differ. 2021;28(3):1110-1125. doi:10.1038/s41418-020-00640-8
Voss SR, Smith JJ, Cecil RF, et al. HDAC inhibitor titration of transcription and axolotl tail regeneration. Front Cell Dev Biol. 2021;9:767377. doi:10.3389/fcell.2021.767377
Gao S, Ge LH, Zhao YM, Li P, Li YY, Zhao W. Hsa-miRNA-143-3p regulates the odontogenic differentiation of human stem cells from the apical papilla by targeting NFIC. Int Endod J. 2022;55(3):263-274. doi:10.1111/iej.13666
Sen CK, Ghatak S. miRNA control of tissue repair and regeneration. Am J Pathol. 2015;185(10):2629-2640. doi:10.1016/j.ajpath.2015.04.001
Yan C, Chen J, Wang C, et al. Milk exosomes-mediated miR-31-5p delivery accelerates diabetic wound healing through promoting angiogenesis. Drug Deliv. 2022;29(1):214-228. doi:10.1080/10717544.2021.2023699
King BL, Yin VP. A conserved MicroRNA regulatory circuit is differentially controlled during limb/appendage regeneration. PloS One. 2016;11(6):e0157106. doi:10.1371/journal.pone.0157106
Gearhart MD, Erickson JR, Walsh A, Echeverri K. Identification of conserved and novel microRNAs during tail regeneration in the Mexican axolotl. Int J Mol Sci. 2015;16(9):22046-22061. doi:10.3390/ijms160922046
Diaz Quiroz JF, Tsai E, Coyle M, Sehm T, Echeverri K. Precise control of miR-125b levels is required to create a regeneration-permissive environment after spinal cord injury: a cross-species comparison between salamander and rat. Dis Model Mech. 2014;7(6):601-611. doi:10.1242/dmm.014837
Demircan T, Sibai M, Avşaroğlu ME, Altuntaş E, Ovezmyradov G. The first report on circulating microRNAs at pre- and post-metamorphic stages of axolotls. Gene. 2021;768:145258. doi:10.1016/j.gene.2020.145258
Rao N, Jhamb D, Milner DJ, et al. Proteomic analysis of blastema formation in regenerating axolotl limbs. BMC Biol. 2009;7:83. doi:10.1186/1741-7007-7-83
Demircan T, Keskin I, Dumlu SN, et al. Detailed tail proteomic analysis of axolotl (Ambystoma mexicanum) using an mRNA-seq reference database. Proteomics. 2017;17(1-2):1600338. doi:10.1002/pmic.201600338
Demircan T, Sibai M, Altuntaş E. Proteome data to explore the axolotl limb regeneration capacity at neotenic and metamorphic stages. Data Brief. 2020;29:105179. doi:10.1016/j.dib.2020.105179
Singh RK, Chang HW, Yan D, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med. 2017;15(1):73. doi:10.1186/s12967-017-1175-y
Demircan T, İlhan AE, Ovezmyradov G, Öztürk G, Yıldırım S. Longitudinal 16S rRNA data derived from limb regenerative tissue samples of axolotl Ambystoma mexicanum. Sci Data. 2019;6(1):70. doi:10.1038/s41597-019-0077-7
Varela-Rodríguez H, Abella-Quintana DG, Espinal-Centeno A, et al. Functional characterization of the Lin28/let-7 circuit during forelimb regeneration in Ambystoma mexicanum and its influence on metabolic reprogramming. Front Cell Dev Biol. 2020;8:562940. doi:10.3389/fcell.2020.562940
Liu Z, Li W, Geng L, et al. Cross-species metabolomic analysis identifies uridine as a potent regeneration promoting factor. Cell Discov. 2022;8(1):6. doi:10.1038/s41421-021-00361-3
Flowers GP, Timberlake AT, Mclean KC, Monaghan JR, Crews CM. Highly efficient targeted mutagenesis in axolotl using Cas9 RNA-guided nuclease. Development. 2014;141(10):2165-2171. doi:10.1242/dev.105072
Fei JF, Schuez M, Tazaki A, Taniguchi Y, Roensch K, Tanaka EM. CRISPR-mediated genomic deletion of Sox2 in the axolotl shows a requirement in spinal cord neural stem cell amplification during tail regeneration. Stem Cell Rep. 2014;3(3):444-459. doi:10.1016/j.stemcr.2014.06.018
Sobkow L, Epperlein HH, Herklotz S, Straube WL, Tanaka EM. 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. Dev Biol. 2006;290(2):386-397. doi:10.1016/j.ydbio.2005.11.037
Khattak S, Schuez M, Richter T, et al. Germline transgenic methods for tracking cells and testing gene function during regeneration in the axolotl. Stem Cell Rep. 2013;1(1):90-103. doi:10.1016/j.stemcr.2013.03.002
Kuo TH, Kowalko JE, DiTommaso T, et al. TALEN-mediated gene editing of the thrombospondin-1 locus in axolotl. Regen Oxf Engl. 2015;2(1):37-43. doi:10.1002/reg2.29
Woodcock MR, Vaughn-Wolfe J, Elias A, et al. Identification of mutant genes and introgressed tiger salamander DNA in the laboratory axolotl, Ambystoma mexicanum. Sci Rep. 2017;7(1):6. doi:10.1038/s41598-017-00059-1
Espinal-Centeno A, Dipp-Álvarez M, Saldaña C, Bako L, Cruz-Ramírez A. Conservation analysis of core cell cycle regulators and their transcriptional behavior during limb regeneration in Ambystoma mexicanum. Mech Dev. 2020;164:103651. doi:10.1016/j.mod.2020.103651
Oviedo NJ, Beane WS. Regeneration: the origin of cancer or a possible cure? Semin Cell Dev Biol. 2009;20(5):557-564. doi:10.1016/j.semcdb.2009.04.005
Waddington CH. Cancer and the theory of organisers. Nature. 1935;135(3416):606-608. doi:10.1038/135606a0
Tsonis PA. Effects of carcinogens on regenerating and non-regenerating limbs in amphibia (review). Anticancer Res. 1983;3(3):195-202.
Tsonis PA, Eguchi G. Carcinogens on regeneration. Effects of N-methyl-N′-nitro-N-nitrosoguanidine and 4-nitroquinoline-1-oxide on limb regeneration in adult newts. Differ Res Biol Divers. 1981;20(1):52-60. doi:10.1111/j.1432-0436.1981.tb01155.x
Khudoley VV, Mizgireuv IV. On spontaneous skin tumours in amphibia. Neoplasma. 1980;27(3):289-293.
Harshbarger JC, Chang SC, DeLanney LE, Rose FL, Green DE. Cutaneous mastocytomas in the neotenic caudate amphibians Ambystoma mexicanum (axolotl) and Ambystoma tigrinum (tiger salamander). J Cancer Res Clin Oncol. 1999;125(3-4):187-192. doi:10.1007/s004320050262
Shioda C, Uchida K, Nakayama H. Pathological features of olfactory neuroblastoma in an axolotl (Ambystoma mexicanum). J Vet Med Sci. 2011;73(8):1109-1111. doi:10.1292/jvms.11-0105
Modesto F, Nicolier A, Hurtrel C, Benoît J. Excisional biopsy and radiotherapy for management of an olfactory neuroblastoma in an axolotl (Ambystoma mexicanum). J Am Vet Med Assoc. 2021;260(4):436-441. doi:10.2460/javma.20.09.0498
Allegrucci C, Rushton MD, Dixon JE, et al. Epigenetic reprogramming of breast cancer cells with oocyte extracts. Mol Cancer. 2011;10(1):7. doi:10.1186/1476-4598-10-7
Saad N, Alberio R, Johnson AD, et al. Cancer reversion with oocyte extracts is mediated by cell cycle arrest and induction of tumour dormancy. Oncotarget. 2018;9(22):16008-16027. doi:10.18632/oncotarget.24664
Suleiman S, Di Fiore R, Cassar A, Formosa MM, Schembri-Wismayer P, Calleja-Agius J. Axolotl Ambystoma mexicanum extract induces cell cycle arrest and differentiation in human acute myeloid leukemia HL-60 cells. Tumour Biol J Int Soc Oncodevelopmental Biol Med. 2020;42(9):1010428320954735. doi:10.1177/1010428320954735
Herbig U, Ferreira M, Condel L, Carey D, Sedivy JM. Cellular senescence in aging primates. Science. 2006;311(5765):1257. doi:10.1126/science.1122446
van Deursen JM. The role of senescent cells in ageing. Nature. 2014;509(7501):439-446. doi:10.1038/nature13193
Phan AQ, Lee J, Oei M, et al. Positional information in axolotl and mouse limb extracellular matrix is mediated via heparan sulfate and fibroblast growth factor during limb regeneration in the axolotl (Ambystoma mexicanum). Regeneration. 2015;2(4):182-201. doi:10.1002/reg2.40
Muñoz-Espín D, Cañamero M, Maraver A, et al. Programmed cell senescence during mammalian embryonic development. Cell. 2013;155(5):1104-1118. doi:10.1016/j.cell.2013.10.019
Jun JI, Lau LF. The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing. Nat Cell Biol. 2010;12(7):676-685. doi:10.1038/ncb2070
Villiard É, Denis JF, Hashemi FS, Igelmann S, Ferbeyre G, Roy S. Senescence gives insights into the morphogenetic evolution of anamniotes. Biol Open. 2017;6(6):891-896. doi:10.1242/bio.025809
Yun MH, Davaapil H, Brockes JP. Recurrent turnover of senescent cells during regeneration of a complex structure. Elife. 2015;4:e05505. doi:10.7554/eLife.05505
Godwin JW, Pinto AR, Rosenthal NA. Macrophages are required for adult salamander limb regeneration. Proc Natl Acad Sci U. S. A. 2013;110(23):9415-9420. doi:10.1073/pnas.1300290110
Baker DJ, Wijshake T, Tchkonia T, et al. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature. 2011;479(7372):232-236. doi:10.1038/nature10600
Ogrodnik M, Evans SA, Fielder E, et al. Whole-body senescent cell clearance alleviates age-related brain inflammation and cognitive impairment in mice. Aging Cell. 2021;20(2):e13296. doi:10.1111/acel.13296
Pajcini KV, Corbel SY, Sage J, Pomerantz JH, Blau HM. Transient inactivation of Rb and ARF yields regenerative cells from postmitotic mammalian muscle. Cell Stem Cell. 2010;7(2):198-213. doi:10.1016/j.stem.2010.05.022
Papadopoli D, Boulay K, Kazak L, et al. mTOR as a central regulator of lifespan and aging. F1000Research. 2019;8:F1000. doi:10.12688/f1000research.17196.1
Johnson K, Bateman J, DiTommaso T, Wong AY, Whited JL. Systemic cell cycle activation is induced following complex tissue injury in axolotl. Dev Biol. 2018;433(2):461-472. doi:10.1016/j.ydbio.2017.07.010
Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, Alt FW. DNA repair, genome stability, and aging. Cell. 2005;120(4):497-512. doi:10.1016/j.cell.2005.01.028
Tian X, Seluanov A, Gorbunova V. Molecular mechanisms determining lifespan in short- and long-lived species. Trends Endocrinol Metab. 2017;28(10):722-734. doi:10.1016/j.tem.2017.07.004
Taormina G, Ferrante F, Vieni S, Grassi N, Russo A, Mirisola MG. Longevity: lesson from model organisms. Genes. 2019;10(7):E518. doi:10.3390/genes10070518
Varga R, Eriksson M, Erdos MR, et al. Progressive vascular smooth muscle cell defects in a mouse model of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U. S. A. 2006;103(9):3250-3255. doi:10.1073/pnas.0600012103
Rodgers AK, Smith JJ, Voss SR. Identification of immune and non-immune cells in regenerating axolotl limbs by single-cell sequencing. Exp Cell Res. 2020;394(2):112149. doi:10.1016/j.yexcr.2020.112149
Lopez D, Lin L, Monaghan JR, et al. Mapping hematopoiesis in a fully regenerative vertebrate: the axolotl. Blood. 2014;124(8):1232-1241. doi:10.1182/blood-2013-09-526970
Tsai SL, Baselga-Garriga C, Melton DA. Blastemal progenitors modulate immune signaling during early limb regeneration. Dev Camb Engl. 2019;146(1):dev169128. doi:10.1242/dev.169128
Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008;453(7193):314-321. doi:10.1038/nature07039
Li J, Chen J, Kirsner R. Pathophysiology of acute wound healing. Clin Dermatol. 2007;25(1):9-18. doi:10.1016/j.clindermatol.2006.09.007
Godwin JW, Debuque R, Salimova E, Rosenthal NA. Heart regeneration in the salamander relies on macrophage-mediated control of fibroblast activation and the extracellular landscape. NPJ Regen Med. 2017;2:22. doi:10.1038/s41536-017-0027-y
Seifert AW, Monaghan JR, Voss SR, Maden M. Skin regeneration in adult axolotls: a blueprint for scar-free healing in vertebrates. PloS One. 2012;7(4):e32875. doi:10.1371/journal.pone.0032875
Zammit PS, Clarke JD, Golding JP, Goodbrand IA, Tonge DA. Macrophage response during axonal regeneration in the axolotl central and peripheral nervous system. Neuroscience. 1993;54(3):781-789. doi:10.1016/0306-4522(93)90247-d
Ussing AP, Rosenkilde P. Effect of induced metamorphosis on the immune system of the axolotl, Ambystoma mexicanum. Gen Comp Endocrinol. 1995;97(3):308-319. doi:10.1006/gcen.1995.1031
Ching YC, Wedgwood RJ. Immunologic responses in the axolotl, Siredon mexicanum. J Immunol Baltim Md. 1967;99(1):191-200.
Chen G, Robert J. Antiviral immunity in amphibians. Viruses. 2011;3(11):2065-2086. doi:10.3390/v3112065
Charlemagne J. Thymus independent anti-horse erythrocyte antibody response and suppressor T cells in the Mexican axolotl (Amphibia, Urodela, Ambystoma mexicanum). Immunology. 1979;36(4):643-648.
Demircan T. Dissecting the molecular signature of spinal cord regeneration in the axolotl model. Cureus. 2020;12(2):e7014. doi:10.7759/cureus.7014
Teven CM, Farina EM, Rivas J, Reid RR. Fibroblast growth factor (FGF) signaling in development and skeletal diseases. Genes Dis. 2014;1(2):199-213. doi:10.1016/j.gendis.2014.09.005
Miyazono K, Maeda S, Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 2005;16(3):251-263. doi:10.1016/j.cytogfr.2005.01.009
Nakao A. TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J. 1997;16(17):5353-5362. doi:10.1093/emboj/16.17.5353
Nusse R, Clevers H. Wnt/β-catenin signaling, disease, and emerging therapeutic modalities. Cell. 2017;169(6):985-999. doi:10.1016/j.cell.2017.05.016
Han MJ, An JY, Kim WS. Expression patterns of Fgf-8 during development and limb regeneration of the axolotl. Dev Dyn. 2001;220(1):40-48. doi:10.1002/1097-0177(2000)9999:9999<::AID-DVDY1085>3.0.CO;2-8
Guimond JC, Lévesque M, Michaud PL, et al. BMP-2 functions independently of SHH signaling and triggers cell condensation and apoptosis in regenerating axolotl limbs. BMC Dev Biol. 2010;10:15. doi:10.1186/1471-213X-10-15
Ghosh S, Roy S, Séguin C, Bryant SV, Gardiner DM. Analysis of the expression and function of Wnt-5a and Wnt-5b in developing and regenerating axolotl (Ambystoma mexicanum) limbs. Dev Growth Differ. 2008;50(4):289-297. doi:10.1111/j.1440-169X.2008.01000.x
Shimokawa T, Yasutaka S, Kominami R, Shinohara H. Lmx-1b and Wnt-7a expression in axolotl limb during development and regeneration. Okajimas Folia Anat Jpn. 2013;89(4):119-124. doi:10.2535/ofaj.89.119
Torok MA, Gardiner DM, Izpisúa-Belmonte JC, Bryant SV. Sonic hedgehog (shh) expression in developing and regenerating axolotl limbs. J Exp Zool. 1999;284(2):197-206.
Freitas PD, Lovely AM, Monaghan JR. Investigating Nrg1 signaling in the regenerating axolotl spinal cord using multiplexed FISH. Dev Neurobiol. 2019;79(5):453-467. doi:10.1002/dneu.22670
Whited JL, Lehoczky JA, Austin CA, Tabin CJ. Dynamic expression of two thrombospondins during axolotl limb regeneration. Dev Dyn. 2011;240(5):1249-1258. doi:10.1002/dvdy.22548
Polvadore T, Maden M. Retinoic acid receptors and the control of positional information in the regenerating axolotl limb. Cell. 2021;10(9):2174. doi:10.3390/cells10092174

Auteurs

Aydın Bölük (A)

School of Medicine, Muğla Sıtkı Koçman University, Muğla, Turkey.

Mervenur Yavuz (M)

Institute of Health Sciences, Muğla Sıtkı Koçman University, Muğla, Turkey.

Turan Demircan (T)

Department of Medical Biology, School of Medicine, Muğla Sıtkı Koçman University, Muğla, Turkey.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH