E-cigarette aerosol exposure can cause craniofacial defects in Xenopus laevis embryos and mammalian neural crest cells

PLoS ONE

Volumn 12, Issue 9, 2017, Pages

  Kennedy, Allyson E ^a   Kandalam, Suraj ^b   Olivares Navarrete, Rene ^b   Dickinson, Amanda J G ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b Virginia Commonwealth University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEROSOL; GLYCEROL; NICOTINE; PROPYLENE GLYCOL;

AEROSOL; ANIMAL; CHEMICALLY INDUCED; CRANIOFACIAL MALFORMATION; CYTOLOGY; DRUG EFFECTS; ELECTRONIC CIGARETTE; EMBRYOLOGY; GENE EXPRESSION REGULATION; MAMMAL; NEURAL CREST; TOXICITY; XENOPUS LAEVIS;

AEROSOLS; ANIMALS; CRANIOFACIAL ABNORMALITIES; ELECTRONIC CIGARETTES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCEROL; MAMMALS; NEURAL CREST; NICOTINE; PROPYLENE GLYCOL; XENOPUS LAEVIS;

EID: 85032966182     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0185729     Document Type: Article

References (78)

1. Rom O, Pecorelli A, Valacchi G, Reznick AZ. Are E-cigarettes a safe and good alternative to cigarette smoking? Ann N Y Acad Sci. 2015; 1340:65-74. https://doi.org/10.1111/nyas.12609 PMID: 25557889.
2. Breland A, Soule E, Lopez A, Ramoa C, El-Hellani A, Eissenberg T. Electronic cigarettes: what are they and what do they do? Annals of the New York Academy of Sciences. 2017; 1394(1):5-30. Epub 2016/ 01/17. https://doi.org/10.1111/nyas.12977 PMID: 26774031; PubMed Central PMCID: PMCPMC4947026.
3. Breland AB, Spindle T, Weaver M, Eissenberg T. Science and electronic cigarettes: current data, future needs. Journal of addiction medicine. 2014; 8(4):223-33. Epub 2014/08/05. https://doi.org/10.1097/ADM.0000000000000049 PMID: 25089952; PubMed Central PMCID: PMCPMC4122311.
4. FDA. Vaporizers, e-cigarettes, and other electronic nicotine delivery systemds (ENDS) 2017 [cited 2017 May 25]. Available from: https://www.fda.gov/tobaccoproducts/labeling/productsingredientscomponents/ucm456610.htm.
5. Singh T, Arrazola RA, Corey CG, Husten CG, Neff LJ, Homa DM, et al. Tobacco Use Amonog Middle and High School Students- United States, 2011-2015. Centers for Disease Control and Prevention, 2016.
6. McMillen R, Gottlieb M, Shaefer R, Winickoff J, Klein J. Trends in Electronic Cigarette Use Among U.S. Adults: Use is Increasing in Both Smokers and Nonsmokers. Nicotine Tobacco Research. 2015; 17 (10):1195-202. https://doi.org/10.1093/ntr/ntu213 PMID: 25381306
7. Wagner NJ, Camerota M, Propper C. Prevalence and Perceptions of Electronic Cigarette Use during Pregnancy. Matern Child Health J. 2017. https://doi.org/10.1007/s10995-016-2257-9 PMID: 28084577.
8. Oncken C, Ricci KA, Kuo CL, Dornelas E, Kranzler HR, Sankey HZ. Correlates of Electronic Cigarettes Use Before and During Pregnancy. Nicotine Tob Res. 2017; 19(5):585-90. https://doi.org/10.1093/ntr/ ntw225 PMID: 28403454.
9. Mark KS, Farquhar B, Chisolm MS, Coleman-Cowger VH, Terplan M. Knowledge, Attitudes, and Practice of Electronic Cigarette Use Among Pregnant Women. Journal of addiction medicine. 2015; 9 (4):266-72. https://doi.org/10.1097/ADM.0000000000000128 PMID: 25974378.
10. Ashford K, Wiggins A, Butler K, Ickes M, Rayens MK, Hahn E. e-Cigarette Use and Perceived Harm Among Women of Childbearing Age Who Reported Tobacco Use During the Past Year. Nurs Res. 2016; 65(5):408-14. https://doi.org/10.1097/NNR.0000000000000176 PMID: 27579508.
11. van Rooij IA, Wegerif MJ, Roelofs HM, Peters WH, Kuijpers-Jagtman AM, Zielhuis GA, et al. Smoking, genetic polymorphisms in biotransformation enzymes, and nonsyndromic oral clefting: a gene-environment interaction. Epidemiology. 2001; 12(5):502-7. PMID: 11505167.
12. Wyszynski DF, Duffy DL, Beaty TH. Maternal cigarette smoking and oral clefts: a meta-analysis. Cleft Palate Craniofac J. 1997; 34(3):206-10. https://doi.org/10.1597/1545-1569(1997)034<0206:MCSAOC>2.3.CO;2 PMID: 9167070.
13. Shi M, Christensen K, Weinberg CR, Romitti P, Bathum L, Lozada A, et al. Orofacial cleft risk is increased with maternal smoking and specific detoxification-gene variants. Am J Hum Genet. 2007; 80 (1):76-90. https://doi.org/10.1086/510518 PMID: 17160896; PubMed Central PMCID: PMCPMC1785306.
14. Gunnerbeck A, Edstedt Bonamy AK, Wikstrom AK, Granath F, Wickstrom R, Cnattingius S. Maternal snuff use and smoking and the risk of oral cleft malformations-a population-based cohort study. PLoS One. 2014; 9(1):e84715. https://doi.org/10.1371/journal.pone.0084715 PMID: 24454740; PubMed Central PMCID: PMCPMC3893163.
15. Yildirim M, Seymen F, Deeley K, Cooper ME, Vieira AR. Defining predictors of cleft lip and palate risk. J Dent Res. 2012; 91(6):556-61. https://doi.org/10.1177/0022034512444928 PMID: 22496123.
16. Honein MA, Devine O, Grosse SD, Reefhuis J. Prevention of orofacial clefts caused by smoking: implications of the Surgeon General's report. Birth Defects Res A Clin Mol Teratol. 2014; 100(11):822-5. https://doi.org/10.1002/bdra.23274 PMID: 25045059; PubMed Central PMCID: PMCPMC4559232.
17. Martelli DR, Coletta RD, Oliveira EA, Swerts MS, Rodrigues LA, Oliveira MC, et al. Association between maternal smoking, gender, and cleft lip and palate. Braz J Otorhinolaryngol. 2015; 81(5):514-9. https://doi.org/10.1016/j.bjorl.2015.07.011 PMID: 26277833.
18. Zhao Z, Reece EA. Nicotine-induced embryonic malformations mediated by apoptosis from increasing intracellular calcium and oxidative stress. Birth Defects Res B Dev Reprod Toxicol. 2005; 74(5):383-91. https://doi.org/10.1002/bdrb.20052 PMID: 16193507.
19. Kang P, Svoboda KK. Nicotine inhibits palatal fusion and modulates nicotinic receptors and the PI-3 kinase pathway in medial edge epithelia. Orthod Craniofac Res. 2003; 6(3):129-42. PMID: 12962196; PubMed Central PMCID: PMCPMC2862388.
20. Bnait KS, Seller MJ. Ultrastructural changes in 9-day old mouse embryos following maternal tobacco smoke inhalation. Exp Toxicol Pathol. 1995; 47(6):453-61. https://doi.org/10.1016/S0940-2993(11) 80327-1 PMID: 8871084.
21. Joschko MA, Dreosti IE, Tulsi RS. The teratogenic effects of nicotine in vitro in rats: a light and electron microscope study. Neurotoxicol Teratol. 1991; 13(3):307-16. PMID: 1886540.
22. Administration FaD. Deeming Tobacco Products to be Subject to the Federal Food, Drug, and Cosmetic Act, as Amended by the Family Smoking Prevention and Tobacco Control Act; Restrictions on the Sale and Distriubution of Tobacco Products and REquired Warning Statements for Tobacco Products. In: Services DoHaH, editor. 2016.
23. Peace MR, Baird TR, Smith N, Wolf CE, Poklis JL, Poklis A. Concentration of Nicotine and Glycols in 27 Electronic Cigarette Formulations. J Anal Toxicol. 2016; 40(6):403-7. 10.1093/jat/bkw037. https://doi.org/10.1093/jat/bkw037 PMID: 27165804; PubMed Central PMCID: PMCPMC4946633.
24. McCarthy M. Attorneys general from 29 US states urge tougher e-cigarette regulations. BMJ. 2014; 349:g5154. https://doi.org/10.1136/bmj.g5154 PMID: 25122480.
25. Burstyn I. Peering through the mist: systematic review of what the chemistry of contaminants in electronic cigarettes tells us about health risks. BMC Public Health. 2014; 14:18. https://doi.org/10.1186/ 1471-2458-14-18 PMID: 24406205; PubMed Central PMCID: PMCPMC3937158.
26. Kienhuis AS, Soeteman-Hernandez LG, Bos PM, Cremers HW, Klerx WN, Talhout R. Potential harmful health effects of inhaling nicotine-free shisha-pen vapor: a chemical risk assessment of the main components propylene glycol and glycerol. Tob Induc Dis. 2015; 13(1):15. https://doi.org/10.1186/s12971-015-0038-7 PMID: 26120296; PubMed Central PMCID: PMCPMC4482188.
27. Werley MS, McDonald P, Lilly P, Kirkpatrick D, Wallery J, Byron P, et al. Non-clinical safety and pharmacokinetic evaluations of propylene glycol aerosol in Sprague-Dawley rats and Beagle dogs. Toxicology. 2011; 287(1-3):76-90. https://doi.org/10.1016/j.tox.2011.05.015 PMID: 21683116.
28. Fowles JR, Banton MI, Pottenger LH. A toxicological review of the propylene glycols. Crit Rev Toxicol. 2013; 43(4):363-90. https://doi.org/10.3109/10408444.2013.792328 PMID: 23656560.
29. Shen X, Hindle M, Byron PR. Effect of energy on propylene glycol aerosols using the capillary aerosol generator. Int J Pharm. 2004; 275(1-2):249-58. https://doi.org/10.1016/j.ijpharm.2004.02.005 PMID: 15081155.
30. Jensen RP, Strongin RM, Peyton DH. Solvent Chemistry in the Electronic Cigarette Reaction Vessel. Scientific reports. 2017; 7:42549. https://doi.org/10.1038/srep42549 PMID: 28195231; PubMed Central PMCID: PMCPMC5307352.
31. Tierney PA, Karpinski CD, Brown JE, Luo W, Pankow JF. Flavour chemicals in electronic cigarette fluids. Tob Control. 2016; 25(e1):e10-5. https://doi.org/10.1136/tobaccocontrol-2014-052175 PMID: 25877377; PubMed Central PMCID: PMCPMC4853541.
32. Pankow JF, Kim K, McWhirter KJ, Luo W, Escobedo JO, Strongin RM, et al. Benzene formation in electronic cigarettes. PLoS One. 2017; 12(3):e0173055. https://doi.org/10.1371/journal.pone.0173055 PMID: 28273096; PubMed Central PMCID: PMCPMC5342216.
33. Zaccone EJ, Goldsmith WT, Shimko MJ, Wells JR, Schwegler-Berry D, Willard PA, et al. Diacetyl and 2,3-pentanedione exposure of human cultured airway epithelial cells: Ion transport effects and metabolism of butter flavoring agents. Toxicol Appl Pharmacol. 2015; 289(3):542-9. https://doi.org/10.1016/j.taap.2015.10.004 PMID: 26454031; PubMed Central PMCID: PMCPMC4739639.
34. Rigler MW, Longo WE. Emission of diacetyl (2,3 butanedione) from natural butter, microwave popcorn butter flavor powder, paste, and liquid products. Int J Occup Environ Health. 2010; 16(3):291-302. https://doi.org/10.1179/107735210799160237 PMID: 20662421.
35. Curwin BD, Deddens JA, McKernan LT. Flavoring exposure in food manufacturing. J Expo Sci Environ Epidemiol. 2015; 25(3):324-33. https://doi.org/10.1038/jes.2014.52 PMID: 25052692; PubMed Central PMCID: PMCPMC4520397.
36. Bailey RL, Cox-Ganser JM, Duling MG, LeBouf RF, Martin SB Jr., Bledsoe TA, et al. Respiratory morbidity in a coffee processing workplace with sentinel obliterative bronchiolitis cases. Am J Ind Med. 2015; 58(12):1235-45. https://doi.org/10.1002/ajim.22533 PMID: 26523478; PubMed Central PMCID: PMCPMC4715657.
37. Kreiss K, Gomaa A, Kullman G, Fedan K, Simoes EJ, Enright PL. Clinical bronchiolitis obliterans in workers at a microwave-popcorn plant. N Engl J Med. 2002; 347(5):330-8. https://doi.org/10.1056/ NEJMoa020300 PMID: 12151470.
38. Cavalcanti Zdo R, Albuquerque Filho A, Pereira C, Coletta E. Bronchiolitis associated with exposure to artificial butter flavoring in workers at a cookie factory in Brazil. J Bras Pneumol. 2012; 38(3):395-9. PMID: 22782611
39. Holden VK, Hines SE. Update on flavoring-induced lung disease. Curr Opin Pulm Med. 2016; 22 (2):158-64. https://doi.org/10.1097/MCP.0000000000000250 PMID: 26761629.
40. Brass DM, Gwinn WM, Valente AM, Kelly FL, Brinkley CD, Nagler AE, et al. The Diacetyl-exposed Human Airway Epithelial Secretome: New Insights Into Flavoring Induced Airways Disease. Am J Respir Cell Mol Biol. 2017. https://doi.org/10.1165/rcmb.2016-0372OC PMID: 28248570.
41. Palpant NJ, Hofsteen P, Pabon L, Reinecke H, Murry CE. Cardiac development in zebrafish and human embryonic stem cells is inhibited by exposure to tobacco cigarettes and e-cigarettes. PLoS One. 2015; 10(5):e0126259. https://doi.org/10.1371/journal.pone.0126259 PMID: 25978043; PubMed Central PMCID: PMCPMC4433280.
42. Lauterstein DE, Tijerina PB, Corbett K, Akgol Oksuz B, Shen SS, Gordon T, et al. Frontal Cortex Transcriptome Analysis of Mice Exposed to Electronic Cigarettes During Early Life Stages. Int J Environ Res Public Health. 2016; 13(4):417. https://doi.org/10.3390/ijerph13040417 PMID: 27077873; PubMed Central PMCID: PMCPMC4847079.
43. Massarsky A, Abdel A, Glazer L, Levin ED, Di Giulio RT. Exposure to 1,2-Propanediol Impacts Early Development of Zebrafish (Danio rerio) and Induces Hyperactivity. Zebrafish. 2017. https://doi.org/10.1089/zeb.2016.1400 PMID: 28266909.
44. Wheeler GN, Liu KJ. Xenopus: an ideal system for chemical genetics. Genesis. 2012; 50(3):207-18. https://doi.org/10.1002/dvg.22009 PMID: 22344814.
45. Dickinson AJ. Using frogs faces to dissect the mechanisms underlying human orofacial defects. Semin Cell Dev Biol. 2016; 51:54-63. https://doi.org/10.1016/j.semcdb.2016.01.016 PMID: 26778163; PubMed Central PMCID: PMCPMC4798872.
46. Dickinson AJ, Lowery LA. Xenopus as a model for developmental biology. Semin Cell Dev Biol. 2016; 51:53. https://doi.org/10.1016/j.semcdb.2016.03.005 PMID: 26987579.
47. Adams DS, Uzel SG, Akagi J, Wlodkowic D, Andreeva V, Yelick PC, et al. Bioelectric signalling via potassium channels: a mechanism for craniofacial dysmorphogenesis in KCNJ2-associated Andersen-Tawil Syndrome. J Physiol. 2016; 594(12):3245-70. https://doi.org/10.1113/JP271930 PMID: 26864374; PubMed Central PMCID: PMCPMC4908029.
48. Devotta A, Juraver-Geslin H, Gonzalez JA, Hong CS, Saint-Jeannet JP. Sf3b4-depleted Xenopus embryos: A model to study the pathogenesis of craniofacial defects in Nager syndrome. Developmental biology. 2016; 415(2):371-82. https://doi.org/10.1016/j.ydbio.2016.02.010 PMID: 26874011; PubMed Central PMCID: PMCPMC4914463.
49. Gouignard N, Maccarana M, Strate I, von Stedingk K, Malmstrom A, Pera EM. Musculocontractural Ehlers-Danlos syndrome and neurocristopathies: dermatan sulfate is required for Xenopus neural crest cells to migrate and adhere to fibronectin. Dis Model Mech. 2016; 9(6):607-20. https://doi.org/10.1242/ dmm.024661 PMID: 27101845; PubMed Central PMCID: PMCPMC4920151.
50. Dubey A, Saint-Jeannet JP. Modeling human craniofacial disorders in Xenopus. Curr Pathobiol Rep. 2017; 5(1):79-92. https://doi.org/10.1007/s40139-017-0128-8 PMID: 28255527; PubMed Central PMCID: PMCPMC5327820.
51. Griffin JN, Sondalle SB, Del Viso F, Baserga SJ, Khokha MK. The ribosome biogenesis factor Nol11 is required for optimal rDNA transcription and craniofacial development in Xenopus. PLoS Genet. 2015; 11(3):e1005018. https://doi.org/10.1371/journal.pgen.1005018 PMID: 25756904; PubMed Central PMCID: PMCPMC4354908.
52. Deniz E, Jonas S, Hooper M, J NG, Choma MA, Khokha MK. Analysis of Craniocardiac Malformations in Xenopus using Optical Coherence Tomography. Scientific reports. 2017; 7:42506. Epub 2017/02/15. https://doi.org/10.1038/srep42506 PMID: 28195132; PubMed Central PMCID: PMCPMC5307353.
53. Kennedy AE, Dickinson AJ. Quantification of orofacial phenotypes in Xenopus. J Vis Exp. 2014;(93): e52062. https://doi.org/10.3791/52062 PMID: 25407252; PubMed Central PMCID: PMCPMC4353423.
54. Kennedy AE, Dickinson AJ. Quantitative analysis of orofacial development and median clefts in Xenopus laevis. Anat Rec (Hoboken). 2014; 297(5):834-55. https://doi.org/10.1002/ar.22864 PMID: 24443252.
55. Tahir R, Kennedy A, Elsea SH, Dickinson AJ. Retinoic acid induced-1 (Rai1) regulates craniofacial and brain development in Xenopus. Mech Dev. 2014; 133:91-104. https://doi.org/10.1016/j.mod.2014.05. 004 PMID: 24878353.
56. Wahl SE, Kennedy AE, Wyatt BH, Moore AD, Pridgen DE, Cherry AM, et al. The role of folate metabolism in orofacial development and clefting. Developmental biology. 2015; 405(1):108-22. https://doi.org/10.1016/j.ydbio.2015.07.001 PMID: 26144049; PubMed Central PMCID: PMCPMC4546841.
57. Spindle TR, Breland AB, Karaoghlanian NV, Shihadeh AL, Eissenberg T. Preliminary results of an examination of electronic cigarette user puff topography: the effect of a mouthpiece-based topography measurement device on plasma nicotine and subjective effects. Nicotine Tob Res. 2015; 17(2):142-9. https://doi.org/10.1093/ntr/ntu186 PMID: 25239957; PubMed Central PMCID: PMCPMC4838000.
58. Sive H, Grainger R, Harland R. Early Development of Xenopus laevis: a laboratory manual: Cold Spring Harbor Laboratory Press; 2000.
59. Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011; 11(2):353-7. https://doi.org/10.1111/j.1755-0998.2010.02924.x PMID: 21429143.
60. Hemmati-Brivanlou A, Thomsen GH. Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4. Dev Genet. 1995; 17(1):78-89. https://doi.org/10.1002/dvg.1020170109 PMID: 7554498.
61. Taylor DJ, Yoffe JR, Brown DM, Woolley DE. Histamine H2 receptors on chondrocytes derived from human, canine and bovine articular cartilage. Biochem J. 1985; 225(2):315-9. PMID: 2983667; PubMed Central PMCID: PMCPMC1144592.
62. Wickstrom R. Effects of nicotine during pregnancy: human and experimental evidence. Current neuropharmacology. 2007; 5(3):213-22. Epub 2007/09/01. https://doi.org/10.2174/157015907781695955 PubMed Central PMCID: PMCPMC2656811. PMID: 19305804
63. Bruin JE, Gerstein HC, Holloway AC. Long-term consequences of fetal and neonatal nicotine exposure: a critical review. Toxicol Sci. 2010; 116(2):364-74. https://doi.org/10.1093/toxsci/kfq103 PMID: 20363831; PubMed Central PMCID: PMCPMC2905398.
64. Rea Darlington. Canonical Variate Analysis and Related Techniques. Review of Educational Research. 1973; 43(4):433-54.
65. Ziermann JM, Mitgutsch C, Olsson L. Analyzing developmental sequences with Parsimov-a case study of cranial muscle development in anuran larvae. J Exp Zool B Mol Dev Evol. 2014; 322(8):586-606. https://doi.org/10.1002/jez.b.22566 PMID: 24692269.
66. Warkman AS, Krieg PA. Xenopus as a model system for vertebrate heart development. Semin Cell Dev Biol. 2007; 18(1):46-53. https://doi.org/10.1016/j.semcdb.2006.11.010 PMID: 17194606; PubMed Central PMCID: PMCPMC1868678.
67. Levine AJ, Munoz-Sanjuan I, Bell E, North AJ, Brivanlou AH. Fluorescent labeling of endothelial cells allows in vivo, continuous characterization of the vascular development of Xenopus laevis. Developmental biology. 2003; 254(1):50-67. PMID: 12606281.
68. Conlon F. Benzidine-peroxidase staining for blood (Conlon lab): Xenbase; 2011 [cited 2017 May 30]. Available from: http://wiki.xenbase.org/xenwiki/index.php/Benzidine-peroxidase_staining_for_blood_ (Conlon_lab).
69. Xu Y, Guo Y, Liu K, Liu Z, Wang X. E-Cigarette Awareness, Use, and Harm Perception among Adults: A Meta-Analysis of Observational Studies. PLoS One. 2016; 11(11):e0165938. https://doi.org/10.1371/journal.pone.0165938 PMID: 27861501; PubMed Central PMCID: PMCPMC5115669.
70. Pu J, Zhang X. Exposure to advertising and perception, interest, and use of e-cigarettes among adolescents: findings from the US National Youth Tobacco Survey. Perspect Public Health. 2017:1757913917703151. https://doi.org/10.1177/1757913917703151 PMID: 28379069.
71. Huerta TR, Walker DM, Mullen D, Johnson TJ, Ford EW. Trends in E-Cigarette Awareness and Perceived Harmfulness in the U.S. Am J Prev Med. 2017; 52(3):339-46. https://doi.org/10.1016/j.amepre.2016.10.017 PMID: 27890516.
72. Zhu SH, Sun JY, Bonnevie E, Cummins SE, Gamst A, Yin L, et al. Four hundred and sixty brands of e-cigarettes and counting: implications for product regulation. Tob Control. 2014; 23 Suppl 3:iii3-9. https://doi.org/10.1136/tobaccocontrol-2014-051670 PMID: 24935895; PubMed Central PMCID: PMCPMC4078673.
73. Yingst JM, Veldheer S, Hammett E, Hrabovsky S, Foulds J. A method for classifying user-reported electronic cigarette liquid flavors. Nicotine Tob Res. 2017. https://doi.org/10.1093/ntr/ntw383 PMID: 28064201.
74. Rowell TR, Reeber SL, Lee SL, Harris RA, Nethery RC, Herring AH, et al. Flavored E-cigarette Liquids Reduce Proliferation and Viability in the CALU3 Airway Epithelial Cell Line. Am J Physiol Lung Cell Mol Physiol. 2017:ajplung 00392 2016. https://doi.org/10.1152/ajplung.00392.2016 PMID: 28428175.
75. Bahl V, Lin S, Xu N, Davis B, Wang YH, Talbot P. Comparison of electronic cigarette refill fluid cytotoxicity using embryonic and adult models. Reprod Toxicol. 2012; 34(4):529-37. https://doi.org/10.1016/j.reprotox.2012.08.001 PMID: 22989551.
76. Hanken J, Gross JB. Evolution of cranial development and the role of neural crest: insights from amphibians. J Anat. 2005; 207(5):437-46. https://doi.org/10.1111/j.1469-7580.2005.00481.x PMID: 16313386; PubMed Central PMCID: PMCPMC1571565.
77. Rinon A, Lazar S, Marshall H, Buchmann-Moller S, Neufeld A, Elhanany-Tamir H, et al. Cranial neural crest cells regulate head muscle patterning and differentiation during vertebrate embryogenesis. Development (Cambridge, England). 2007; 134(17):3065-75. https://doi.org/10.1242/dev.002501 PMID: 17652354.
78. Schmidt J, Piekarski N, Olsson L. Cranial muscles in amphibians: development, novelties and the role of cranial neural crest cells. J Anat. 2013; 222(1):134-46. https://doi.org/10.1111/j.1469-7580.2012.01541.x PMID: 22780231; PubMed Central PMCID: PMCPMC3552420.