Journal of Molecular Neuroscience

, Volume 47, Issue 3, pp 666–673 | Cite as

Temporal Distribution of Hig-1 (Hypoxia-Induced Gene 1) mRNA and Protein in Rat Spinal Cord: Changes During Postnatal Life

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Abstract

Several cellular and molecular events responsible for the development of the central nervous system (CNS), particularly those related to the development of ordered neural connections, occur during the first days of postnatal life, being days 1 through 10 a critical period to reach maturity and establish innervations. We have previously characterized hypoxia-induced gene 1 (Hig-1) and described an increase in its expression from day 1 to 15 of postnatal life in the spinal cord. Hig-1 mRNA has an open reading frame for a 93 amino acid protein, but its function has not been completely elucidated. Recently, several analyses in many cell types have related Hig-1 expression with differentiation or cell death/survival balance. With the aim of further characterizing the presence of Hig-1 in the CNS, we analyzed the cellular distribution of HIG-1 protein in rat's spinal cord at postnatal days 1, 8, 15, and 90 (P1–P90). We found an interesting change in the protein expression pattern, shifting from neurons at P1 to glial cells at P90, which points towards a functional role for this protein in the spinal cord throughout development. We also compared the protein distribution with the cellular distribution of the mRNA and of an antisense RNA.

Keywords

Hig-1 Differential gene expression CNS Neural postnatal maturation Antisense RNA 
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Notes

Acknowledgements

The authors would like to thank Dr. Steiner (University of Chicago) for kindly providing the rabbit antibody anti-HIG-1, Dr. Flavio Zolessi and Dr. Mónica Brauer for contributing with secondary antibodies, and Dr. Yanina Panzera for her assistance in the use of image processing software.

References

  1. Almeida A, Almeida J, Bolanos JP, Moncada S (2001) Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci U S A 98:15294–15299PubMedCrossRefGoogle Scholar
  2. An HJ, Shin H, Jo SG, Kim YJ, Lee JO, Paik SG, Lee H (2011) The survival effect of mitochondrial Higd-1a is associated with suppression of cytochrome C release and prevention of caspase activation. Biochim Biophys Acta Epub ahead of printGoogle Scholar
  3. Angeloni C, Spencer JP, Leoncini E, Biagi PL, Hrelia S (2007) Role of quercetin and its in vivo metabolites in protecting H9c2 cells against oxidative stress. Biochimie 89:73–82PubMedCrossRefGoogle Scholar
  4. Bak M, Silahtaroglu A, Moller M, Christensen M, Rath MF, Skryabin B, Tommerup N, Kauppinen S (2008) MicroRNA expression in the adult mouse central nervous system. RNA 14:432–444PubMedCrossRefGoogle Scholar
  5. Bambrick L, Kristian T, Fiskum G (2004) Astrocyte mitochondrial mechanisms of ischemic brain injury and neuroprotection. Neurochem Res 29:601–608PubMedCrossRefGoogle Scholar
  6. Barker AJ, Ullian EM (2008) New roles for astrocytes in developing synaptic circuits. Commun Integr Biol 1:207–211PubMedCrossRefGoogle Scholar
  7. Bedo G, Vargas M, Ferreiro MJ, Chalar C, Agrati D (2005) Characterization of hypoxia induced gene 1: expression during rat central nervous system maturation and evidence of antisense RNA expression. Int J Dev Biol 49:431–436PubMedCrossRefGoogle Scholar
  8. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA et al (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278PubMedCrossRefGoogle Scholar
  9. Carninci P (2010) RNA dust: where are the genes? DNA Res 17:51–59PubMedCrossRefGoogle Scholar
  10. Chanrion M, Negre V, Fontaine H, Salvetat N, Bibeau F, Mac Grogan G, Mauriac L, Katsaros D, Molina F, Theillet C, Darbon JM (2008) A gene expression signature that can predict the recurrence of tamoxifen-treated primary breast cancer. Clin Cancer Res 14:1744–1752PubMedCrossRefGoogle Scholar
  11. Chen L, Fink T, Zhang XY, Ebbesen P, Zachar V (2005) Quantitative transcriptional profiling of ATDC5 mouse progenitor cells during chondrogenesis. Differentiation 73:350–363PubMedCrossRefGoogle Scholar
  12. Chen YH, Wang YH, Yu TH, Wu HJ, Pai CW (2009) Transgenic zebrafish line with over-expression of Hedgehog on the skin: a useful tool to screen Hedgehog-inhibiting compounds. Transgenic Res 18:855–864PubMedCrossRefGoogle Scholar
  13. Clarac F, Pearlstein E, Pflieger JF, Vinay L (2004) The in vitro neonatal rat spinal cord preparation: a new insight into mammalian locomotor mechanisms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:343–357PubMedCrossRefGoogle Scholar
  14. Coggeshall RE, Pover CM, Fitzgerald M (1994) Dorsal root ganglion cell death and surviving cell numbers in relation to the development of sensory innervation in the rat hindlimb. Brain Res Dev Brain Res 82:193–212PubMedCrossRefGoogle Scholar
  15. Coudert AE, Pibouin L, Vi-Fane B, Thomas BL, Macdougall M, Choudhury A, Robert B, Sharpe PT, Berdal A, Lezot F (2005) Expression and regulation of the Msx1 natural antisense transcript during development. Nucleic Acids Res 33:5208–5218PubMedCrossRefGoogle Scholar
  16. Denko N, Schindler C, Koong A, Laderoute K, Green C, Giaccia A (2000) Epigenetic regulation of gene expression in cervical cancer cells by the tumor microenvironment. Clin Cancer Res 6:480–487PubMedGoogle Scholar
  17. Dinger ME, Pang KC, Mercer TR, Crowe ML, Grimmond SM, Mattick JS (2009) NRED: a database of long noncoding RNA expression. Nucleic Acids Res 37:D122–D126PubMedCrossRefGoogle Scholar
  18. Garcia AD, Petrova R, Eng L, Joyner AL (2010) Sonic hedgehog regulates discrete populations of astrocytes in the adult mouse forebrain. J Neurosci 30:13597–13608PubMedCrossRefGoogle Scholar
  19. Gavriouchkina D, Fischer S, Ivacevic T, Stolte J, Benes V, Dekens MP (2010) Thyrotroph embryonic factor regulates light-induced transcription of repair genes in zebrafish embryonic cells. PLoS One 5:e12542PubMedCrossRefGoogle Scholar
  20. Haeberlein SL (2004) Mitochondrial function in apoptotic neuronal cell death. Neurochem Res 29:521–530PubMedCrossRefGoogle Scholar
  21. Jin K, Mao XO, Eshoo MW, del Rio G, Rao R, Chen D, Simon RP, Greenberg DA (2002) cDNA microarray analysis of changes in gene expression induced by neuronal hypoxia in vitro. Neurochem Res 27:1105–1112PubMedCrossRefGoogle Scholar
  22. Kasai K, Yamashita T, Yamaguchi A, Yoshiya K, Kawakita A, Tanaka H, Sugimoto H, Tohyama M (2003) Induction of mRNAs and proteins for Na/K ATPase alpha1 and beta1 subunits following hypoxia/reoxygenation in astrocytes. Brain Res Mol Brain Res 110:38–44PubMedCrossRefGoogle Scholar
  23. Lattanzi W, Bernardini C, Gangitano C, Michetti F (2007) Hypoxia-like transcriptional activation in TMT-induced degeneration: microarray expression analysis on PC12 cells. J Neurochem 100:1688–1702PubMedGoogle Scholar
  24. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431–1568PubMedGoogle Scholar
  25. Lowrie MB, Lawson SJ (2000) Cell death of spinal interneurones. Prog Neurobiol 61:543–555PubMedCrossRefGoogle Scholar
  26. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A 105:716–721PubMedCrossRefGoogle Scholar
  27. Plenderleith MB, Wright LL, Snow PJ (1992) Expression of lectin binding in the superficial dorsal horn of the rat spinal cord during pre- and postnatal development. Brain Res Dev Brain Res 68:103–109PubMedCrossRefGoogle Scholar
  28. Salnikow K, Davidson T, Zhang Q, Chen LC, Su W, Costa M (2003) The involvement of hypoxia-inducible transcription factor-1-dependent pathway in nickel carcinogenesis. Cancer Res 63:3524–3530PubMedGoogle Scholar
  29. Slezak M, Pfrieger FW (2003) New roles for astrocytes: regulation of CNS synaptogenesis. Trends Neurosci 26:531–535PubMedCrossRefGoogle Scholar
  30. Thrash-Bingham CA, Tartof KD (1999) aHIF: a natural antisense transcript overexpressed in human renal cancer and during hypoxia. J Natl Cancer Inst 91:143–151PubMedCrossRefGoogle Scholar
  31. Todd KJ, Serrano A, Lacaille JC, Robitaille R (2006) Glial cells in synaptic plasticity. J Physiol Paris 99:75–83PubMedCrossRefGoogle Scholar
  32. Ullian EM, Harris BT, Wu A, Chan JR, Barres BA (2004) Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture. Mol Cell Neurosci 25:241–251PubMedCrossRefGoogle Scholar
  33. Vallon-Christersson J, Staaf J, Kvist A, Medstrand P, Borg A, Rovira C (2007) Non-coding antisense transcription detected by conventional and single-stranded cDNA microarray. BMC Genomics 8:295PubMedCrossRefGoogle Scholar
  34. Vinay L, Brocard F, Clarac F (2000a) Differential maturation of motoneurons innervating ankle flexor and extensor muscles in the neonatal rat. Eur J Neurosci 12:4562–4566PubMedCrossRefGoogle Scholar
  35. Vinay L, Brocard F, Pflieger JF, Simeoni-Alias J, Clarac F (2000b) Perinatal development of lumbar motoneurons and their inputs in the rat. Brain Res Bull 53:635–647PubMedCrossRefGoogle Scholar
  36. Vinay L, Ben-Mabrouk F, Brocard F, Clarac F, Jean-Xavier C, Pearlstein E, Pflieger JF (2005) Perinatal development of the motor systems involved in postural control. Neural Plast 12:131–139, discussion 263-172PubMedCrossRefGoogle Scholar
  37. Walton KD, Navarrete R (1991) Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. J Physiol 433:283–305PubMedGoogle Scholar
  38. Wang J, Cao Y, Chen Y, Gardner P, Steiner DF (2006) Pancreatic beta cells lack a low glucose and O2-inducible mitochondrial protein that augments cell survival. Proc Natl Acad Sci U S A 103:10636–10641PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Gabriela Bedó
    • 1
  • Patricia Lagos
    • 2
  • Daniella Agrati
    • 3
  1. 1.Sección Genética Evolutiva, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay
  2. 2.Departamento de Fisiología, Facultad de MedicinaUniversidad de la RepúblicaMontevideoUruguay
  3. 3.Sección Fisiología y Nutrición, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay

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