Abstract
Olfactomedin-like (OLFML) proteins are members of the olfactomedin domain–containing secreted glycoprotein (OLF) family. OLFML2A and OLFML2B are representative molecules of these glycoproteins. Olfactomedins are critical for the development and functional organization of the nervous system and retina, which is a highly conserved structure in vertebrates, having almost identical anatomical and physiological characteristics in multiple taxa. Spotted gar, a member of the Lepisosteidae family, is a freshwater fish that inhabits rivers, bayous, swamps, and brackish waters. Recently, the complete genome has been sequenced, providing a unique bridge between fish medical models to human biology, making it an excellent animal model. This study was aimed to understanding the evolution OLFML2A and OLFML2B in the retina of spotted gar through looking for the expression of these genes. Spotted gar retina was analyzed with hematoxylin-eosin staining assays to provide an overall view of the retina structure and an immunofluorescence assay to identify OLFML2A and OLFML2B protein expression. A phylogenetic tree was created using the neighbor-joining method. Forces that direct the evolution of the fish genes were tested. Spotted gar retina, as in other vertebrates, is made of several layers. OLFML2A and OLFML2B proteins were detected in the rod and cone photoreceptor layer (PRL), outer nuclear layer (ONL), and inner nuclear layer (INL). Phylogenetic tree analysis confirms the orthology within the OLFML2A gene. Purifying selection is the evolutionary force that directs the OLFML2A genes. OLFML2A genes have a well-conserved function over time and species.
Similar content being viewed by others
References
Amemiya CT, Alfoldi J, Lee AP, Fan S, Philippe H, Maccallum I, Braasch I, Manousaki T, Schneider I, Rohner N, Organ C, Chalopin D, Smith JJ, Robinson M, Dorrington RA, Gerdol M, Aken B, Biscotti MA, Barucca M, Baurain D, Berlin AM, Blatch GL, Buonocore F, Burmester T, Campbell MS, Canapa A, Cannon JP, Christoffels A, De Moro G, Edkins AL, Fan L, Fausto AM, Feiner N, Forconi M, Gamieldien J, Gnerre S, Gnirke A, Goldstone JV, Haerty W, Hahn ME, Hesse U, Hoffmann S, Johnson J, Karchner SI, Kuraku S, Lara M, Levin JZ, Litman GW, Mauceli E, Miyake T, Mueller MG, Nelson DR, Nitsche A, Olmo E, Ota T, Pallavicini A, Panji S, Picone B, Ponting CP, Prohaska SJ, Przybylski D, Saha NR, Ravi V, Ribeiro FJ, Sauka-Spengler T, Scapigliati G, Searle SM, Sharpe T, Simakov O, Stadler PF, Stegeman JJ, Sumiyama K, Tabbaa D, Tafer H, Turner-Maier J, van Heusden P, White S, Williams L, Yandell M, Brinkmann H, Volff JN, Tabin CJ, Shubin N, Schartl M, Jaffe DB, Postlethwait JH, Venkatesh B, Di Palma F, Lander ES, Meyer A, Lindblad-Toh K (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–316. https://doi.org/10.1038/nature12027
Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH (2011) Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188:799–808. https://doi.org/10.1534/genetics.111.127324
Anholt RR (2014) Olfactomedin proteins: central players in development and disease. Front Cell Dev Biol 2:6. https://doi.org/10.3389/fcell.2014.00006
Braasch I, Gehrke AR, Smith JJ, Kawasaki K, Manousaki T, Pasquier J, Amores A, Desvignes T, Batzel P, Catchen J, Berlin AM, Campbell MS, Barrell D, Martin KJ, Mulley JF, Ravi V, Lee AP, Nakamura T, Chalopin D, Fan S, Wcisel D, Canestro C, Sydes J, Beaudry FE, Sun Y, Hertel J, Beam MJ, Fasold M, Ishiyama M, Johnson J, Kehr S, Lara M, Letaw JH, Litman GW, Litman RT, Mikami M, Ota T, Saha NR, Williams L, Stadler PF, Wang H, Taylor JS, Fontenot Q, Ferrara A, Searle SM, Aken B, Yandell M, Schneider I, Yoder JA, Volff JN, Meyer A, Amemiya CT, Venkatesh B, Holland PW, Guiguen Y, Bobe J, Shubin NH, Di Palma F, Alfoldi J, Lindblad-Toh K, Postlethwait JH (2016) The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet 48:427–437. https://doi.org/10.1038/ng.3526
Comabella Y, Mendoza R, Aguilera C, Carrillo O, Hurtado A, García-Galano T (2006) Digestive enzyme activity during early larval development of the Cuban gar Atractosteus tristoechus. Fish Physiol Biochem 32:147–157. https://doi.org/10.1007/s10695-006-0007-4
Fadool JM, Dowling JE (2008) Zebrafish: a model system for the study of eye genetics. Prog Retin Eye Res 27:89–110. https://doi.org/10.1016/j.preteyeres.2007.08.002
Fingert JH, Stone EM, Sheffield VC, Alward WL (2002) Myocilin glaucoma. Surv Ophthalmol 47:547–561. https://doi.org/10.1016/S0039-6257(02)00353-3
Fishelson L, Ayalon G, Zverdling A, Holzman R (2004) Comparative morphology of the eye (with particular attention to the retina) in various species of cardinal fish (Apogonidae, Teleostei). Anat Rec A Discov Mol Cell Evol Biol 277:249–261. https://doi.org/10.1002/ar.a.20005
Furutani Y, Manabe R, Tsutsui K, Yamada T, Sugimoto N, Fukuda S, Kawai J, Sugiura N, Kimata K, Hayashizaki Y, Sekiguchi K (2005) Identification and characterization of photomedins: novel olfactomedin-domain-containing proteins with chondroitin sulphate-E-binding activity. Biochem J 389:675–684. https://doi.org/10.1042/BJ20050120
Karavanich CA, Anholt RR (1998) Molecular evolution of olfactomedin. Mol Biol Evol 15:718–726
Lee JA, Anholt RR, Cole GJ (2008) Olfactomedin-2 mediates development of the anterior central nervous system and head structures in zebrafish. Mech Dev 125:167–181. https://doi.org/10.1016/j.mod.2007.09.009
Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, Park YM, Buso N, Lopez R (2015) The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res 43:W580–W584. https://doi.org/10.1093/nar/gkv279
Mendoza-Alfaro R, Aguilera-González C, Ferrara MA (2008) Gar biology and culture: status and prospects. Aquac Res 39:748–763. https://doi.org/10.1111/j.1365-2109.2008.01927.x
Nakaya N, Lee HS, Takada Y, Tzchori I, Tomarev SI (2008) Zebrafish olfactomedin 1 regulates retinal axon elongation in vivo and is a modulator of Wnt signaling pathway. J Neurosci 28:7900–7910. https://doi.org/10.1523/JNEUROSCI.0617-08.2008
Nakaya N, Sultana A, Lee HS, Tomarev SI (2012) Olfactomedin 1 interacts with the Nogo A receptor complex to regulate axon growth. J Biol Chem 287:37171–37184. https://doi.org/10.1074/jbc.M112.389916
Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world, fifth edn. John Wiley and Sons http://www.wiley.com/WileyCDA/WileyTitle/productCd-111834233X,subjectCd-LS00.html
Ravi V, Venkatesh B (2008) Rapidly evolving fish genomes and teleost diversity. Curr Opin Genet Dev 18:544–550. https://doi.org/10.1016/j.gde.2008.11.001
Rodriguez-Sanchez IP, Garza-Rodriguez ML, Mohamed-Noriega K, Voruganti VS, Tejero ME, Delgado-Enciso I, Perez-Ibave DC, Schlabritz-Loutsevitch NE, Mohamed-Noriega J, Martinez-Fierro ML, Resendez-Perez D, Cole SA, Cavazos-Adame H, Comuzzie AG, Mohamed-Hamsho J, Barrera-Saldana HA (2013) Olfactomedin-like 3 (OLFML3) gene expression in baboon and human ocular tissues: cornea, lens, uvea, and retina. J Med Primatol 42:105–111. https://doi.org/10.1111/jmp.12037
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425 http://www.ncbi.nlm.nih.gov/pubmed/3447015
Shaffer HB, Minx P, Warren DE, Shedlock AM, Thomson RC, Valenzuela N, Abramyan J, Amemiya CT, Badenhorst D, Biggar KK, Borchert GM, Botka CW, Bowden RM, Braun EL, Bronikowski AM, Bruneau BG, Buck LT, Capel B, Castoe TA, Czerwinski M, Delehaunty KD, Edwards SV, Fronick CC, Fujita MK, Fulton L, Graves TA, Green RE, Haerty W, Hariharan R, Hernandez O, Hillier LW, Holloway AK, Janes D, Janzen FJ, Kandoth C, Kong L, de Koning AP, Li Y, Literman R, McGaugh SE, Mork L, O'Laughlin M, Paitz RT, Pollock DD, Ponting CP, Radhakrishnan S, Raney BJ, Richman JM, St John J, Schwartz T, Sethuraman A, Spinks PQ, Storey KB, Thane N, Vinar T, Zimmerman LM, Warren WC, Mardis ER, Wilson RK (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14:R28. https://doi.org/10.1186/gb-2013-14-3-r28
Stenkamp DL (2007) Neurogenesis in the fish retina. Int Rev Cytol 259:173–224. https://doi.org/10.1016/S0074-7696(06)59005-9
Stenkamp DL (2011) The rod photoreceptor lineage of teleost fish. Prog Retin Eye Res 30:395–404. https://doi.org/10.1016/j.preteyeres.2011.06.004
Stone EM, Fingert JH, Alward WL, Nguyen TD, Polansky JR, Sunden SL, Nishimura D, Clark AF, Nystuen A, Nichols BE, Mackey DA, Ritch R, Kalenak JW, Craven ER, Sheffield VC (1997) Identification of a gene that causes primary open angle glaucoma. Science 275:668–670 http://www.ncbi.nlm.nih.gov/pubmed/9005853
Sukeena JM, Galicia CA, Wilson JD, McGinn T, Boughman JW, Robison BD, Postlethwait JH, Braasch I, Stenkamp DL, Fuerst PG (2016) Characterization and evolution of the spotted gar retina. J Exp Zool B Mol Dev Evol 326:403–421. https://doi.org/10.1002/jez.b.22710
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Tomarev SI, Nakaya N (2009) Olfactomedin domain-containing proteins: possible mechanisms of action and functions in normal development and pathology. Mol Neurobiol 40:122–138. https://doi.org/10.1007/s12035-009-8076-x
Torrado M, Trivedi R, Zinovieva R, Karavanova I, Tomarev SI (2002) Optimedin: a novel olfactomedin-related protein that interacts with myocilin. Hum Mol Genet 11:1291–1301 http://www.ncbi.nlm.nih.gov/pubmed/12019210
Wcisel DJ, Ota T, Litman GW, Yoder JA (2017) Spotted gar and the evolution of innate immune receptors. J Exp Zool B Mol Dev Evol 328:666–684. https://doi.org/10.1002/jez.b.22738
Wiggs JL, Allingham RR, Vollrath D, Jones KH, De La Paz M, Kern J, Patterson K, Babb VL, Del Bono EA, Broomer BW, Pericak-Vance MA, Haines JL (1998) Prevalence of mutations in TIGR/Myocilin in patients with adult and juvenile primary open-angle glaucoma. Am J Hum Genet 63:1549–1552. https://doi.org/10.1086/302098
Wu SM (2010) Synaptic organization of the vertebrate retina: general principles and species-specific variations: the Friedenwald lecture. Invest Ophthalmol Vis Sci 51(3):1264–1274. https://doi.org/10.1167/iovs.09-4396
Yamada E (1982) Morphology of vertebrate photoreceptors. Methods Enzymol 81:3–17 http://www.ncbi.nlm.nih.gov/pubmed/7098873
Zeng LC, Han ZG, Ma WJ (2005) Elucidation of subfamily segregation and intramolecular coevolution of the olfactomedin-like proteins by comprehensive phylogenetic analysis and gene expression pattern assessment. FEBS Lett 579:5443–5453. https://doi.org/10.1016/j.febslet.2005.08.064
Zhang J, Rosenberg HF, Nei M (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci U S A 95:3708–3713 http://www.ncbi.nlm.nih.gov/pubmed/9520431
Acknowledgments
The authors gratefully acknowledge the critical reading of the manuscript by Sergio Lozano-Rodriguez.
Funding
The present work was supported by the grant number 16769 from the Mexican Council of Science and Technology, CONACYT.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The experimental protocol was reviewed and approved by the Research Ethics Committee of the Faculty of Biological Sciences (approval number FCB-CB-701).
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Garza-Rodríguez, M.L., González-Álvarez, R., Mendoza Alfaro, R.E. et al. Olfactomedin-like 2 A and B (OLFML2A and OLFML2B) profile expression in the retina of spotted gar (Lepisosteus oculatus) and bioinformatics mining. Fish Physiol Biochem 45, 1575–1587 (2019). https://doi.org/10.1007/s10695-019-00647-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-019-00647-0