Abstract
Study design
Observational study of Killifish with spinal deformities
Objective
To evaluate the morphology and molecular biology of Aphanius fasciatus with severe spine deformities.
Summary of background data
Idiopathic Scoliosis affects 3% of the population and is an abnormal three-dimensional curvature of the spine with unknown cause. The lack of a model system with naturally occurring spinal curvatures has hindered research on the etiology of IS.
Methods
The Mediterranean killifish Aphanius fasciatus, collected from the coast of Sfax (Tunisia), which has an inborn skeletal deformity was chosen. We used morphologic features to evaluate the severity of scoliosis according to the different types and performed a biochemical analysis using factors previously studied in humans (estradiol, melatonin and Insulin Growth Factor 1 “IGF-1”).
Results
We have detected relevant molecular deviations that occur in Killifish deformities and the fish with severe scoliosis are smaller and less old than the ones with milder scolioses. Furthermore, a significant change in levels of ovarian estradiol, liver IGF-1 and brain melatonin was noted between deformed and normal fish.
Conclusions
Aphanius fasciatus could be used as a molecular model system to study the etiology of IS in humans as the characterization of the Aphanius fasciatus scoliosis syndrome has revealed morphological and biochemical parallels to IS. However, it is important to note the limitations of the proposed model, including the short lifespan of the fish.
Level of evidence
III.
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References
Kristen F, Gorman BSc, Felix B (2009) Idiopathic-type scoliosis is not exclusive to bipedalism. Med Hypotheses 72(3):348–352
Yamada S, Yamamoto T, Tonomura Y (1970) Reaction mechanism of the Ca2 plus-dependent ATPase of sarcoplasmic reticulum from skeletal muscle. 3. Ca plus-uptake and ATP-splitting. J Biochem 67(6):789–794
Burwell RG, Cole AA, Cook TA et al (1992) Pathogenesis of idiopathic scoliosis. The Nottingham concept. Acta OrthopBelg 58(Suppl 1):33–58
Machida M (1999) Cause of idiopathic scoliosis. Spine (Phila Pa 1976) 24(24):2576–2583
Machida M, Weinstein SL, Yamada T et al (1985) Spinal cord monitoring. Electrophysiological measures of sensory and motor function during spinal surgery. Spine (Phila Pa 1976) 10(5):407–413
Castelein RM, van Dieën JH, Smit TH (2005) The role of dorsal shear forces in the pathogenesis of adolescent idiopathic scoliosis—a hypothesis. Med Hypotheses 65(3):501–508
Xiao J, Wu ZH, Qiu GX et al (2007) Upright posture impact on spine susceptibility in scoliosis and progression patterns of scoliotic curve. Zhonghua Yi XueZaZhi 87(1):48–52
Kawakami M, Tamaki T, Yoshida M et al (1999) Axial symptoms and cervical alignments after cervical anterior spinal fusion for patients with cervical myelopathy. J Spinal Disord 12(1):50–56
Gorman KF, Breden F (2009) Idiopathic-type scoliosis is not exclusive to bipedalism. Med Hypotheses 72(3):348–352
O’Kelly C, Wang X, Raso J et al (1999) The production of scoliosis after pinealectomy in young chickens, rats, and hamsters. Spine (Phila Pa 1976) 24(1):35–43
Cheung KM, Wang T, Poon AM et al (2005) The effect of pinealectomy on scoliosis development in young nonhuman primates. Spine (Phila Pa 1976) 30(18):2009–2013
Lowe TG, Edgar M, Margulies JY et al (2000) CH.Etiology of idiopathic scoliosis: current trends in research. J Bone Joint Surg Am 82-A(8):1157–1168
Fjelldal PG, Grotmol S, Kryvi H et al (2004) Pinealectomy induces malformation of the spine and reduces the mechanical strength of the vertebrae in Atlantic salmon Salmo salar. J Pineal Res 36(2):132–139
Antunes M, Da Lopes CP (2002) Skeletal anomalies in Gobiusniger (Gobiidae)from Sado Estuary. Portugal Cybium 26:179–184
Messaoudi I, Kessabi K, Kacem A et al (2009) Incidence of spinal deformities in natural populations of Aphaniusfasciatus Nardo, 1827 from the Gulf of Gabes Tunisia. Afr J Ecol 47:360–366
Gorman KF, Breden F (2010) Disproportionate body lengths correlate with idiopathic-type curvature in the curve back guppy. Spine (Phila Pa 1976) 35(5):511–516
Kristen F, Gorman BSc, Stephen J et al (2007) The Mutant Guppy Syndrome Curveback as a Model for Human Heritable Spinal Curvature. Spine 32(7):735–74
Boumaïza M, Quinard J, Ktari M (1979) Contribution à la biologie de la reproduction d’Aphanius fasciatus Nardo, 1827 (Pisces: Cyprinodontidae) de Tunisie. Bull Off Natl Pesches Tunis 3:221–240
Villwock W (1982) Aphanius (Nardo, 1827) and Cyprinodon (Lac., 1803) (Pisces: Cyprinodontidae), an attempt for genetic interpretation of speciation. Z ZoologSystEvolforsch 20:187–197
CGP (1996) Annuaire des statistiques des pêches en Tunisie. Ministère de l’agriculture, Tunisie
Kessabi K, Kerkeni A, Saïd K, Messaoudi I (2009) Involvement of Cd bioaccumulation in spinal deformities occurrence in natural populations of Mediterranean killifish. Biol Trace Element Res 128:72–81
Kessabi K, Annabi A, Hassine AI et al (2013) Possible chemical causes of skeletal deformities in natural populations of Aphaniusfasciatus collected from the Tunisian coast. Chemosphere (90)2683–2689
Kessabi K, Said K, Messaoudi I (2013) Comparative study of longevity, growth, and biomarkers of metal detoxication and oxidative stress between normal and deformed Aphaniusfasciatus (Pisces, Cyprinodontidae). J Toxicol Environ Health Part A 76:1269–1281
Zhang J, Edmond L, Lawrence H et al (2009) Automatic Cobb Measurement of Scoliosis Based on Fuzzy Hough Transform with Vertebral Shape Prior. J Digital Imaging 22:463–472
Justin DB, David GL, Randolph G et al (2015) Animal models of scoliosis. Orthop Res 33:458–467
Bradley JB, Jennifer AM, Yasmin SM et al (2012) Avian intervertebral disc arises from rostral sclerotome and lacks a nucleus pulposus: implications for evolution of the vertebrate disc. Dev Dynam 241:675–683
Wojcik G, Piskorz J, Ilzecka J et al (2014) Effect of intervertebral disc disease on scoliosis in the lumbar spine. Curr Issues Pharm Med Sci 27:155–158
Nakhaee K, Tavakoli GA, Abedi R (2019) Relationship between intervertebral disc morphology and adolescent idiopathic scoliosis. Clin Eng 44(4):174–179
Kessabi K, Hwas Z, Sassi A, Said K et al (2014) Heavy metal accumulation and histomorphological alterations in Aphanius fasciatus (Pisces, Cyprinodontidae) from the Gulf of Gabes (Tunisia). Environ Sci Pollut Res Int 21(24):14099–14109
Tomasiewicz HG, Johnson BA, Liu XC et al (2017) Development of Zebrafish (Danio rerio) as a natural model system for studying scoliosis. J OrthopSurgRehabil 1–1
Ioannis L, Apostolos S (1999) Population age and sex structure of Aphaniusfasciatus Nardo, 1827 (Pisces: Cyprinodontidae) in the Mesolongi and Etolikon lagoons (W. Greece). Fish Res 40(1999):227–235.
Mao SH, Jiang J, Sun X et al (2011) Timing of menarche in Chinese girls with and without adolescent idiopathic scoliosis: current results and review of the literature. Eur Spine J 20(2):260–265
Tutman P, Glamuzina B, Skaramuca B et al (2000) Incidence of spinal deformities in natural populations of sand smelt, Atherinaboyeri (Risso, 1810) in the Neretva River estuary, middle Adriatic. Fish Res 45:61–64
Annabi A, Saïd K, Messaoudi I (2013) Heavy metal levels in gonad and liver tissues effects on the reproductive parameters of natural populations of Aphanius facsiatus. Environ SciPollut Res 20(10):7309–7319
Leboeuf D, Letellier K, Alos N et al (2009) Do estrogens impact adolescent idiopathic scoliosis. Trends EndocrinolMetab 20(4):147–152
Aleksandra K, Anna G, Jagoda D et al (2015) Participation of sex hormones in multifactorial pathogenesis of adolescent idiopathic scoliosis. Int Orthopaedics (SICOT) 39:1227–1236
Esposito T, Uccello R, Caliendo R et al (2009) Estrogen receptor polymorphism, estrogen content and idiopathic scoliosis in human: a possible genetic linkage. J Steroid BiochemMolBiol 116(1–2):56–60
Zhou C, Wang H, Zou Y et al (2015) Research progress of role of estrogen and estrogen receptor on onset and progression of adolescent idiopathic scoliosis. ZhongguoXiu Fu Chong Jian WaiKeZaZhi 29:1441–1445
Sanders JO, Browne RH, Cooney TE et al (2009) Correlates of the peak heightvelocity in girls with idiopathic scoliosis. Spine (Phila Pa 1976) 31(20):2289–2295
Khosla S, Oursler MJ, Monroe DG (2012) Estrogen and the skeleton. Trends EndocrinolMetab. 23(11):576–81
Suzuki N, Hayakawa K, Kameda T et al (2009) Monohydroxylated polycyclic aromatic hydrocarbons inhibit both osteoclastic and osteoblastic activities in teleost scales. Life Sci 84:482–488
Kitajima Y, Ono Y (2016) Estrogens maintain skeletal muscle and satellite cell functions. J Endocrinol 229(3):267–275
Le G, Novotny SA, Mader TL et al (2018) A moderate oestradiol level enhances neutrophil number and activity in muscle after traumatic injury but strength recovery is accelerated. J Physiol 596(19):4665–4680
Wang J, Zhou J, Bondy CA (1999) Igf1 promotes longitudinal bone growth by insulin-like actions Augmenting chondrocyte hypertrophy. FASEB J 13(14):1985–1990
Faria P, Joice BF, Diego B (2011) Melatonin as a central molecule connecting neural development and calcium signaling. Funct Integr Genomics 11(3):383–388
Brzezinski A (1997) Melatonin in humans. N Engl J Med 36(3):186–195
Cardinali DP, García AP, Cano P, Esquifino AI (2004) Melatonin role in experimental arthritis. Curr Drug Targets Immune EndocrMetabolDisord 4(1):1–10
Thillard MJ (1959) Vertebral column deformities following epiphysectomy in the chick. C R Hebd Seances Acad Sci 248(8):1238–1240
Machida M, Dubousset J, Imamura Y et al (1996) Melatonin. A possible role in pathogenesis of adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 21(10):1147–1152
Satomura K, Tobiume S, Tokuyama R et al (2007) Melatonin at pharmacological doses enhances human osteoblastic differentiation in vitro and promotes mouse cortical bone formation in vivo. J Pineal Res 42:231–239
Maria S, Samsonraj RM, Munmun F et al (2018) Biological effects of melatonin on osteoblast/osteoclast cocultures, bone, and quality of life: implications of a role for MT2 melatonin receptors, MEK1/2, and MEK5 in melatonin-mediated osteoblastogenesis. J Pineal Res 64(3)
Kesling KL, Reinker KA (1997) A meta-analysis of the literature and report of six cases. Spine (Phila Pa 1976) 22(17):2009–2014 ((Scoliosis in twins 1997. 1; discussion 2015))
Ogura Y, Kou I, Miura S et al (2015) A functional SNP in BNC2 is associated with adolescent idiopathic scoliosis. Am J Human Genet 97(2):337–342
McMaster ME, Lee AJ, Burwell RG (2015) Physical activities of Patients with adolescent idiopathic scoliosis (AIS): preliminary longitudinal case-control study historical evaluation of possible risk factors. Scoliosis 18(10):6
Machida M, Dubousset J, Imamura Y et al (1993) An experimental study in chickens for the pathogenesis of idiopathic scoliosis. Spine (Phila Pa 1976) 18(12):1609–1615
Qiu XS, Tang NL, Yeung HY et al (2007) Genetic association study of growth hormone receptor and idiopathic scoliosis. Clin Orthop Relat Res 462:53–58
Dretakis EK (2000) Brain-stem dysfunction and idiopathic scoliosis. Stud Health Technol Inform 2002(91):422–427
Sina RK, Sandip PT, Woojin C (2019) Etiology of adolescent idiopathic scoliosis: a literature review. Asian Spine J 13(3):519–526
Acknowledgements
We would like to acknowledge all laboratory staff at Department of Laboratory LR11ES41 Genetic Biodiversity and Valorization of Bio-resources, 5000, Monastir, Tunisia. for the funding and technical support that we presented and for their encouragement to succeed in this work.
Funding
The financemet was provided by Monastir University, Monastir Higher Institute of Biotechnology, Laboratory LR11ES41, Genetics Biodiversity and Valorization of Bio-resources, 5000, Monastir, Tunisia.
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LS: substantial contributions to design of the work; acquisition, analysis, and interpretation of data for the work; and drafting the work and final approval of the version to be published. KK: interpretation of data for the work; and revising it critically for important intellectual content; and final approval of the version to be published. MI: substantial contributions to the conception of the work; and it critically for important intellectual content; and final approval of the version to be published.
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The handling and sacrifice of animals have been applied in the regulation of the IRB approval/Research Ethics Committee of the Monastir Higher Institute of Biotechnology, University of Monastir, Tunisia.
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Lahmar, S., Kessabi, K. & Messaoudi, I. Aphanius fasciatus: a molecular model of scoliosis?. Spine Deform 9, 883–892 (2021). https://doi.org/10.1007/s43390-021-00291-w
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DOI: https://doi.org/10.1007/s43390-021-00291-w