Advertisement

Genetica

, Volume 139, Issue 3, pp 383–391 | Cite as

Comparative genetics of the central nervous system in epigean and hypogean Astyanax mexicanus

  • Allen G. Strickler
  • Daphne Soares
Article

Abstract

The extreme environment of subterranean caves presents an adaptive challenge to troglobitic organisms. The mechanisms by which natural selection modify an ancestral surface neural circuit to produce a novel subterranean behavior remain a mystery. To address this question, we performed cross species microarray experiments to compare differences in gene expression levels in the adult brain of the teleost Astyanax mexicanus. This species provides a unique opportunity for comparative genetic studies as it consists of extant epigean (surface) and hypogean (cave) conspecifics. Microarray experiments herein revealed significant changes in transcription levels of seventeen genes, several of which are important for behaviors involved in metabolic management. We focused on genes central to three neurotransmission and neuromodulation networks: the endocannabinoid system (Cannabinoid receptor CB1), the dopaminergic system (Tyrosine 3-monooxygenase/tryptophan 5-monooxygenase activation protein) and the glutamatergic system (glutamate receptor AMPA 2a). All three genes were upregulated in the hypogean form of A. mexicanus compared to the epigean form, indicating that behavioral differences in the hypogean form of the species could be due to alterations in expression levels of several key genes. This information provides insights into the complex relationships among environmental factors, genetics, nervous systems and adaptive behavior, and can subsequently help us understand how these interactions affect behavior in other biological systems.

Keywords

Brain Microarray Evolution Astyanax mexicanus CB1 AMPA 2a Tyrosine 3-monooxygenase 

Abbreviation

CNS

Central nervous system

Notes

Acknowledgments

We would like to thank Dr. Gal Haspel and Tzur Haspel-Soares with the production of Fig. 1 and helpful comments; and Dr. Emma Coddington and Dr. Meghan Porter for their input.

References

  1. Banik U (1997) Interaction of phosphorylated tryptophan hydroxylase with 14-3-3 proteins. J Biol Chem 272(42):26219–26225PubMedCrossRefGoogle Scholar
  2. Barr TC (1968) Cave ecology and the evolution of troglobites. Evol Biol 2:35–102Google Scholar
  3. Bassareo V, Di Chiara G (1999) Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 89(3):637–641PubMedCrossRefGoogle Scholar
  4. Berke JD, Hyman SE (2000) Addiction, dopamine, and the review molecular mechanisms of memory. Neuron 25:515–532PubMedCrossRefGoogle Scholar
  5. Bredt D, Nicholl RA (2003) Ampa receptor trafficking at excitatory synapses. Neuron 40(2):361–379PubMedCrossRefGoogle Scholar
  6. Coddington E, Lewis C, Rose JD, Moore FL (2007) Endocannabinoids mediate the effects of acute stress and corticosterone on sex behavior. Endocrinology 148(2):493–500PubMedCrossRefGoogle Scholar
  7. Cota D (2003) The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Investig 112(3):423–431PubMedGoogle Scholar
  8. Cottone E, Forno S, Campantico E, Guastalla A, Viltono L, Mackie K, Fosca Franzoni M (2005) Expression and distribution of CB1 cannabinoid receptors in the central nervous system of the African cichlid fish Pelvicachromis pulcher. J Comp Neurol 485(4):293–303PubMedCrossRefGoogle Scholar
  9. Culver DC, Pipan T (2009) Biology of Caves and Other Subterranean Habitats. Oxford University Press, Oxford, UKGoogle Scholar
  10. Di Chiara G (1999) Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375(1–3):13–30PubMedCrossRefGoogle Scholar
  11. Di Marzo V, Matias I (2005) Endocannabinoid control of food intake and energy balance. Nat Neurosci 8(5):585–589PubMedCrossRefGoogle Scholar
  12. Di Marzo V, Goparaju SK, Wang L, Liu J, Bátkai S, Járai Z, Fezza F, Miura GI, Palmiter RD, Sugiura T et al (2001) Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410(6830):822–825PubMedCrossRefGoogle Scholar
  13. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51(1):7PubMedGoogle Scholar
  14. Eberly WR (1960) Competition and evolution in cave crayfishes of southern indiana. Syst Zool 9(1):29CrossRefGoogle Scholar
  15. Engeli S, Bohnke J, Feldpausch M, Gorzelniak K, Janke J, Batkai S, Pacher P, Harvey-White J, Luft FC, Sharma AM, Jordan J (2005) Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54(10):2838–2843PubMedCrossRefGoogle Scholar
  16. Filip M, Gołda A, Zaniewska M, McCreary AC, Nowak E, Kolasiewicz W, Przegaliński E (2006) Involvement of cannabinoid CB1 receptors in drug addiction: effects of rimonabant on behavioral responses induced by cocaine. Pharmacol Rep 58(6):806–819PubMedGoogle Scholar
  17. Harrold J (2002) Down-regulation of cannabinoid-1 (cb-1) receptors in specific extrahypothalamic regions of rats with dietary obesity: a role for endogenous cannabinoids in driving appetite for palatable food? Brain Res 952(2):232–238PubMedCrossRefGoogle Scholar
  18. Harrold JA, Williams G (2007) The cannabinoid system: a role in both the homeostatic and hedonic control of eating? British J Nutr 90(04):729CrossRefGoogle Scholar
  19. Huppop K (1986) Oxygen consumption of astyanax fasciatus (characidae, pisces): a comparison of epigean and hypogean populations. Environ Biol Fishes 17(4):299–308CrossRefGoogle Scholar
  20. Iida K, Nishimura I (2002) Gene expression by profiling by dna microarray technology. Crit Rev Oral Biol Med 13(1):35–50PubMedCrossRefGoogle Scholar
  21. Issartel J, Voituron Y, Guillaume O, Clobert J, Hervant F (2010) Selection of physiological, metabolic adaptations to food deprivation in the Pyrenean newt Calotriton asper during cave colonisation. Comp Biochem Physiol A Mol Integr Physiol 155(1):77–83PubMedCrossRefGoogle Scholar
  22. Itagaki C, Isobe T, Taoka M, Natsume T, Nomura N, Horigome T, Omata S, Ichinose H, Nagatsu T, Greene LA, Ichimura T (1999) Stimulus-coupled interaction of tyrosine hydroxylase with 14–3-3 proteins. Biochemistry 38(47):15673–15680PubMedCrossRefGoogle Scholar
  23. Jeffery W (2001) Cavefish as a model system in evolutionary developmental biology. Dev Biol 231(1):1–12PubMedCrossRefGoogle Scholar
  24. Jeffery WR, Martasian DP (1998) Evolution of eye regression in the cavefish astyanax: apoptosis and the pax-6 gene. Integr Comp Biol 38(4):685–696CrossRefGoogle Scholar
  25. Jeffery WR, Strickler AG, Guiney S, Heyser DG, Tomarev SI (2000) Prox 1 in eye degeneration and sensory organ compensation during development and evolution of the cavefish astyanax. Dev Genes Evol 210(5):223–230PubMedCrossRefGoogle Scholar
  26. Kauer JA (2004) Learning mechanisms in addiction: synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse. Annu Rev Physiol 66(1):447–475PubMedCrossRefGoogle Scholar
  27. Kayo T (2001) Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc Natl Acad Sci 98(9):5093–5098PubMedCrossRefGoogle Scholar
  28. Kelley AE (2004) Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44(1):161–179PubMedCrossRefGoogle Scholar
  29. Lam C, Rastegar S, Strähle U (2006) Distribution of cannabinoid receptor 1 in the cns of zebrafish. Neuroscience 138(1):83–95PubMedCrossRefGoogle Scholar
  30. Lee J, Nam S, Hwang SB, Hong M, Kwon JY, Joeng KS, Im SH, Shim J, Park MC et al (2004) Functional genomic approaches using the nematode caenorhabditis elegans as a model system. J biochem mol biol 37(1):107–113PubMedCrossRefGoogle Scholar
  31. Li C, Wong WH (2001a) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci 98(1):31–36PubMedCrossRefGoogle Scholar
  32. Li C, Wong WH (2001b) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2(8):research0032.1–0032.11Google Scholar
  33. Lin L, Liu S, Brockway H, Seok J, Jiang P, Wong WH, Xing Y (2009) Using high-density exon arrays to profile gene expression in closely related species. Nucleic Acids Res 37(12):e90 Epub 2009 May 27PubMedCrossRefGoogle Scholar
  34. López-Moreno JA, González-Cuevas G, Moreno G, Navarro M (2008) The pharmacology of the endocannabinoid system: functional and structural interactions with other neurotransmitter systems and their repercussions in behavioral addiction. Addict Biol 13(2):160–187PubMedCrossRefGoogle Scholar
  35. Madden DR (2002) Ion channel structurethe structure and function of glutamate receptor ion channels. Nat Rev Neurosci 3(2):91–101PubMedCrossRefGoogle Scholar
  36. Malinow R, Malenka RC (2002) Ampa receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25(1):103–126PubMedCrossRefGoogle Scholar
  37. Marinelli S, Di Marzo V, Berretta N, Matias I, Maccarrone M, Bernardi G, Mercuri NB (2003) Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J Neurosci 23(8):3136–3144PubMedGoogle Scholar
  38. Mayer ML (2006) Glutamate receptors at atomic resolution. Nature 440(7083):456–462PubMedCrossRefGoogle Scholar
  39. Mitchell RW, Russell WH, Elliot WR (1977) Mexican eyeless characin fishes, genus astyanax: environment, distribution, and evolution. Spec Publ Mus Texas Tech Univ 12:1–89Google Scholar
  40. Osei-Hyiaman D, DePetrillo M, Pacher P, Liu J, Radaeva S, Bátkai S, Harvey-White J, Mackie K, Offertáler L, Wang L, Kunos G (2005) Endocannabinoid activation at hepatic cb1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J Clin Investig 115(5):1298–1305PubMedGoogle Scholar
  41. Oswald RE (2004) Advances in protein chemistry. In: Advances in Protein Chemistry, vol 68 Elsevier, pp 313–349Google Scholar
  42. Pagotto U, Vicennati V, Pasquali R (2005) The endocannabinoid system and the treatment of obesity. Ann Med 37(4):270–275PubMedCrossRefGoogle Scholar
  43. Palmer CL (2005) The molecular pharmacology and cell biology of -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Pharmacol Rev 57(2):253–277PubMedCrossRefGoogle Scholar
  44. Pita-Thomas W, Fernández-Martos C, Yunta M, Maza RM, Navarro-Ruiz R, Lopez-Rodríguez MJ, Reigada D, Nieto-Sampedro M, Nieto-Diaz M (2010) Gene expression of axon growth promoting factors in the deer antler. PLoS One 5(12):e15706PubMedCrossRefGoogle Scholar
  45. Portavella M, Vargas JP, Salas C (2002) The effects of telencephalic lesions on spatial, temporal and emotional learning in goldfish. Brain Res Bull 57(2–3):397–399PubMedCrossRefGoogle Scholar
  46. Poulson T (1964) Handbook of physiology, section iv, adaptation to the environment. In: Handbook of Physiology, Section IV, Adaptation to the Environment. Am Physiol Soc. pp 749–771Google Scholar
  47. Ravinet Trillou C, Arnone M, Delgorge C, Gonalons N, Keane P, Maffrand JP, Soubrie P (2003) Anti-obesity effect of sr141716, a cb1 receptor antagonist, in diet-induced obese mice. Am J of Physiol Regul Integr Comp Physiol 284(2):345Google Scholar
  48. Rink E, Wullimann MF (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889(1-2):316–330PubMedCrossRefGoogle Scholar
  49. Salin K, Voituron Y, Mourin J, Hervant F (2010) Cave colonization without fasting capacities: an example with the fish astyanax fasciatus mexicanus. Comp Biochem Physiol A Mol Integr Physiol 156(4):451–457PubMedCrossRefGoogle Scholar
  50. Schemmel C (1967) Vergleichende untersuchungen an den hautsinnesorganen ober- und unterirdisch lebender astyanax-formen. Zeitschrift fur Morphologie der Tiere 61(2):255–316CrossRefGoogle Scholar
  51. Small CM, Carney GE, Mo Q, Vannucci M, Jones AG (2009) A microarray analysis of sex- and gonad-biased gene expression in the zebrafish: evidence for masculinization of the transcriptome. BMC Genomics 10(1):579PubMedCrossRefGoogle Scholar
  52. Strickler AG, Jeffery WR (2009) Differentially expressed genes identified by cross-species microarray in the blind cavefish astyanax. Integr Zool 4(1):99–109PubMedCrossRefGoogle Scholar
  53. Szameit S, Vierlinger K, Farmer L, Tuschl H, Noehammer C (2008) Microarray-based in vitro test system for the discrimination of contact allergens and irritants: identification of potential marker genes. Clin Chem 54(3):525–533PubMedCrossRefGoogle Scholar
  54. Tasker J (2004) Endogenous cannabinoids take the edge off neuroendocrine responses to stress. Endocrinology 145(12):5429–5430PubMedCrossRefGoogle Scholar
  55. Teyke T (1990) Morphological differences in neuromasts of the blind cave fish astyanax hubbsi and the sighted river fish astyanax mexicanus. Brain Behav Evol 35(1):23–30PubMedCrossRefGoogle Scholar
  56. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5(2):97–107PubMedCrossRefGoogle Scholar
  57. Valenti M, Cottone E, Martinez R, De Pedro N, Rubio M, Viveros MP, Franzoni MF, Delgado M, Di Marzo V (2005) The endocannabinoid system in the brain of Carassius auratus and its possible role in the control of food intake. J Neurochem 95:662–672. doi: 10.1111/j.1471-4159.2005.03406.x PubMedCrossRefGoogle Scholar
  58. Volkow ND, Wise RA (2005) How can drug addiction help us understand obesity? Nat Neurosci 8(5):555–560PubMedCrossRefGoogle Scholar
  59. Wenger T (2003) Neuromorphological background of cannabis addiction. Brain Res Bull 61(2):125–128PubMedCrossRefGoogle Scholar
  60. Wilkens H (1988) Evolution and genetics of epigean and cave astyanax fasciatus (characidae, pisces), support for the neutral mutation theory. Evol Biol 23:271–367Google Scholar
  61. Willis DK, Wang J, Lindholm JR, Orth A, Goodman WG (2010) Microarray analysis of juvenile hormone response in drosophila melanogaster s2 cells. J Insect Sci 10(66):1–14CrossRefGoogle Scholar
  62. Wolf M (2004) Psychomotor stimulants and neuronal plasticity. Neuropharmacology 47:61–79PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.University of MarylandCollege ParkUSA

Personalised recommendations