Evidence for a cordal, not ganglionic, pattern of cephalopod brain neurogenesis
Tóm tắt
From the large-brained cephalopods to the acephalic bivalves, molluscs show a vast range of nervous system centralization patterns. Despite this diversity, molluscan nervous systems, broadly considered, are organized either as medullary cords, as seen in chitons, or as ganglia, which are typical of gastropods and bivalves. The cephalopod brain is exceptional not just in terms of its size; its relationship to a molluscan cordal or ganglionic plan has not been resolved from the study of its compacted adult structure. One approach to clarifying this puzzle is to investigate the patterns of early cephalopod brain neurogenesis, where molecular markers for cephalopod neural development may be informative. We report here on early brain pattern formation in the California two-spot octopus, Octopus bimaculoides. Employing gene expression analysis with the pan-bilaterian neuronal marker ELAV and the atonal-related neuronal differentiation genes NEUROGENIN and NEUROD, as well as immunostaining using a Distalless-like homeoprotein antibody, we found that the octopus central brain forms from concentric cords rather than bilaterally distributed pairs of ganglia. We conclude that the cephalopod brain, despite its great size and elaborate specializations, retains in its development the hypothesized ancestral molluscan nervous system plan of medullary cords, as described for chitons and other aculiferan molluscs.
Tài liệu tham khảo
Wells MJ. Brain and Behaviour in Cephalopods. Stanford: Stanford University Press; 1962.
Hanlon RT, Messenger JB. Cephalopod Behavior. Cambridge: Cambridge University Press; 1996.
Hochner B, Shomrat T, Fiorito G. The octopus: a model for a comparative analysis of the evolution of learning and memory mechanisms. Biol Bull. 2006;210:308–17.
Nixon M, Young JZ. The Brains and Lives of Cephalopods. Oxford: Oxford University Press; 2003.
Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz A, Stach T, et al. Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool. 2010;7:29.
Kröger B, Vinther J, Fuchs D. Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules. Bioessays. 2011;33:602–13.
Young JZ. The central nervous system of Nautilus. Philos Trans R Soc Lond B Biol Sci. 1965;249:1–25.
Faller S, Holger Roth B, Todt C, Schmidt-Rhaesa A, Loesel R. Comparative neuroanatomy of Caudofoveata, Solenogastres, Polyplacophora, and Scaphopoda (Mollusca) and its phylogenetic implications. Zoomorphology. 2012;131:149–70.
Sigwart JD, Sumner-Rooney LH, Schwabe E, Heß M, Brennan GP, Schrödl M. A new sensory organ in “primitive” molluscs (Polyplacophora: Lepidopleurida), and its context in the nervous system of chitons. Front Zool. 2014;11:7.
Bullock TH. Mollusca: cephalopoda. In: Bullock TH, Horridge GA, editors. Structure and Function in the Nervous Systems of Invertebrates. San Francisco: W.H. Freeman; 1965. p. 1433–515.
Marthy HJ. Ontogenesis of the nervous system in cephalopods. New York: Plenum; 1987.
Meister G. Organogenese von Loligo vulgaris Lam. Zool Jb Anat. 1972;89:247–300.
Marquis F. Die Embryonalentwicklung des Nervensysem von Octopus vulgaris Lam. (Cephalopoda, Octopoda), eine histologische Analyse. Verhandl Naturf Ges (Basel). 1989;99:23–75.
Shigeno S, Tsuchiya K, Segawa S. Embryonic and paralarval development of the central nervous system of the loliginid squid Sepioteuthis lessoniana. J Comp Neurol. 2001;437:449–75.
Yamamoto M, Shimazaki Y, Shigeno S. Atlas of the embryonic brain in the pygmy squid, Idiosepius paradoxus. Zool Sci. 2003;20:163–79.
Shigeno S, Kidokoro H, Tsuchiya K, Segawa S, Yamamoto M. Development of the brain in the oegopsid squid, Todarodes pacificus: an atlas up to the hatching stage. Zool Sci. 2001;18:527–41.
Jimenez F, Campos-Ortega JA. Genes in subdivision 1B of the Drosophila melanogaster X-chromosome and their influence on neural development. J Neurogene. 1987;4:179–200.
Robinow S, White K. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J Neurobiol. 1991;22:443–61.
King PH, Levine TD, Fremeau Jr RT, Keene JD. Mammalian homologs of Drosophila ELAV localized to a neuronal subset can bind in vitro to the 3′ UTR of mRNA encoding the Id transcriptional repressor. J Neurosci. 1994;14:1943–52.
Kim CH, Ueshima E, Muraoka O, Tanaka H, Yeo SY, Huh TL, et al. Zebrafish elav/HuC homologue as a very early neuronal marker. Neurosci Lett. 1996;216:109–12.
Wakamatsu Y, Weston JA. Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development. 1997;124:3449–60.
Denes AS, Jekely G, Steinmetz PR, Raible F, Snyman H, Prud’homme B, et al. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in Bilateria. Cell. 2007;129:277–88.
Meyer NP, Seaver EC. Neurogenesis in an annelid: characterization of brain neural precursors in the polychaete Capitella sp. I. Dev Biol. 2009;335:237–52.
Nomaksteinsky M, Rottinger E, Dufour HD, Chettouh Z, Lowe CJ, Martindale MQ, et al. Centralization of the deuterostome nervous system predates chordates. Curr Biol. 2009;19:1264–9.
Paridaen JTML, Huttner WB. Neurogenesis during development of the vertebrate central nervous system. EMBO Reports. 2014;15:351–64.
Seo S, Lim JW, Yellajoshyula D, Chang LW, Kroll KL. Neurogenin and NeuroD direct transcriptional targets and their regulatory enhancers. EMBO J. 2007;12:5093–108.
Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, et al. Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol. 2007;7:33.
Simionato E, Kerner P, Dray N, Le Gouar M, Ledent V, Arendt D, et al. Atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes. BMC Evol Biol. 2008;8:170.
Zapata F, Wilson NG G, Howison M, Andrade SCS, Jörger KM, Schrödl M, et al. Phylogenomic analyses of deep gastropod relationships reject Orthogastropoda. Proc R Soc B. 2014;281:20141739.
Forsythe JW, Hanlon RT. Effect of temperature on laboratory growth, reproduction and life span of Octopus bimaculoides. Mar Biol. 1988;98:369-379.
Hanlon RT, Forsythe JW. Advances in the laboratory culture of octopuses for biomedical research. Lab Anim Sci. 1985;35:33–40.
Fiorni P. Morphogenese der Tiere. G 5-I: Cephalopoden. New York: Fischer-Verlag; 1978.
Young JZ. The Anatomy of the Nervous System of Octopus vulgaris. Oxford: Clarendon; 1971.
Shigeno S, Sasaki T, Moritaki T, Kasugai T, Vecchione M, Agata K. Evolution of the cephalopod head complex by assembly of multiple molluscan body parts: Evidence from Nautilus embryonic development. J Morphol. 2008;269:1–17.
Rose TM, Schultz ER, Henikoff JG, Pietrokovski S, McCallum CM, Henikoff S. Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucleic Acids Res. 1998;26:1628–35.
Henikoff S, Henikoff JG, Alford WJ, Pietrokovski S. Automated construction and graphical presentation of protein blocks from unaligned sequences. Gene. 1995;163:GC17–26.
Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5:113.
Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximum-likelihood trees for large alignments. PloS One. 2010;5:e9490.
Grove EA, Tole S, Limon J, Yip L, Ragsdale CW. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development. 1998;125:2315–25.
Panganiban G, Irvine SM, Lowe C, Roehl H, Corley LS, Sherbon B, et al. The origin and evolution of animal appendages. Proc Natl Acad Sci. 1997;94:5162–6.
Boletzky S. Biology of early life stages in cephalopod molluscs. Advances in Mar Biol. 2003;44:143–203.
Naef A. Die Cephalopoden (Embryologie). Washington: Fauna Flora Golfo Napoli: Smithsonian Institution; 1928.
Fuchs E. Organo- und Histogenese des Darmsystems, embryonale Blutbildung und Dotterabbau bei Eledone cirrosa Lam. (Cephalopoda, Octopoda). Zool Jb Anat. 1973;91:31–92.
Mangold K, Boletzky S, Froesch D. Reproductive biology and embryonic development of Eledone cirrosa (Cephalopoda: Octopoda). Mar Biol. 1971;8:109–17.
Hartenstein V, Stollewerk A. The evolution of early neurogenesis. Dev Cell. 2015;32:390–407.
Baratte S, Bonnaud L. Evidence of early nervous differentiation and early catecholaminergic sensory system during Sepia officinalis embryogenesis. J Comp Neurol. 2009;517:539–49.
Buresi A, Canali E, Bonnaud L, Baratte S. Delayed and asynchronous ganglionic maturation during cephalopod neurogenesis as evidenced by Sof-elav1 expression in embryos of Sepia officinalis (Mollusca, Cephalopoda). J Comp Neurol. 2013;521:1482–96.
Chase RB. Behavior and its Neural Control in Gastropod Molluscs. New York: Oxford University Press; 2002.
Kocot KM, Cannon JT, Todt C, Citarella MR, Kohn AB, Meyer A, et al. Phylogenomics reveals deep molluscan relationships. Nature. 2011;477:452–6.
Smith SA, Wilson NG, Goetz FE, Feehery C, Andrade SC, Rouse GW, et al. Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature. 2011;480:364–7.
Yochelson EL, Flower RH, Webers GF. The bearing of the new late Cambrian monoplacophoran Knightconus upon the origin of the Cephalopoda. Lethaia. 1973;6:275–309.
Haszprunar G, Ruthensteiner B. Monoplacophora (Tryblidia)—Some Unanswered Questions. Am Malacol Bull. 2013;31:189–94.
Plate LH. Die Anatomie und Phylogenie der Chitonen. Zool Jahrb. 1898;Suppl. IV (Fauna Chilensis I): Teil A:1–243.
Voronezhskaya EE, Tyurin SA, Nezlin LP. Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora). J Comp Neurol. 2002;444:25–38.
Eernisse DJ, Reynolds PD. Polyplacophora. In: Harrison FW, Kohn AJ, editors. Microscopic Anatomy of Invertebrates, Mollusca I. New York: Wiley-Liss; 1994. p. 55–110.
Friedrich S, Wanninger A, Bruckner M, Haszprunar G. Neurogenesis in the mossy chiton, Mopalia muscosa (Gould) (Polyplacophora): evidence against molluscan metamerism. J Morphol. 2002;253:109–17.
Gillette R. The molluscan nervous system. In: Ladd PC, editor. Neural and Integrative Animal Physiology. New York: Wiley-Liss; 1991. p. 574–611.
Page LR. Developmental analysis reveals labial and subradular ganglia and the primary framework of the nervous system in nudibranch gastropods. J Neurobiol. 1993;24:1443–59.
von Salvini-Plawen L. Zur Morphologie und Phylogenie der Mollusken: die Beziehungen der Caudofoveata und der Solenogastres als Aculifera, als Mollusca und als Spiralia. Z Wiss Zool. 1972;184:205–394.