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International Journal of Inflammation
Volume 2014, Article ID 803237, 8 pages
http://dx.doi.org/10.1155/2014/803237
Review Article

Hemoglobin Expression in Nonerythroid Cells: Novel or Ubiquitous?

1Division of Molecular Immunology and Microbiology (MIM), National Institute for Research in Reproductive Health (NIRRH), J.M. Street, Parel, Mumbai 400012, India
2Department of Biological Sciences, Tata Institute of Fundamental Research (TIFR), Mumbai 400005, India

Received 29 May 2014; Revised 10 October 2014; Accepted 12 October 2014; Published 5 November 2014

Academic Editor: Jean-Marc Cavaillon

Copyright © 2014 Debarchana Saha et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. L. Hünefeld, Der Chemismus in der thierischen Organisation, Brockhaus, Leipzig, Germany, 1840, http://www.worldcat.org/title/chemismus-in-der-thierischen-organisation-physiologisch-chemische-untersuchungen-der-materiellen-veranderungen-oder-des-bildungslebens-im-thierischen-organismus-insbesondere-des-blutbildungsprocesses-der-natur-der-blutkorperchen-und-ihrer-kernchen-ein-beitrag-zur-physiologie-und-heilmittellehre/oclc/489105995.
  2. R. Giegé, “A historical perspective on protein crystallization from 1840 to the present day,” The FEBS Journal, vol. 280, no. 24, pp. 6456–6497, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Hoppe-Seyler, “Ueber die chemischen und optischen Eigenschaften des Blutfarbstoffs,” Archiv für pathologische Anatomie und Physiologie und für klinische Medicin, vol. 29, no. 5-6, pp. 597–600, 1926. View at Publisher · View at Google Scholar
  4. C. Bernard, Lecons sur les Effets des Substances Toxiques et Médicamenteuses, Bailliere, Paris, France, 1857, https://archive.org/details/leonssurlesef00bern.
  5. I. Blumenthal, “Carbon monoxide poisoning,” Journal of the Royal Society of Medicine, vol. 94, pp. 270–272, 2001, http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1281520/pdf/0940270.pdf. View at Google Scholar
  6. M. F. Perutz, M. G. Rossmann, A. F. Cullis, H. Muirhead, G. Will, and A. C. T. North, “Structure of Hæmoglobin: a three-dimensional fourier synthesis at 5.5-Å. Resolution, obtained by X-ray analysis,” Nature, vol. 185, no. 4711, pp. 416–422, 1960. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Anthea, J. Hopkins, C. W. McLaughlin et al., Human Biology and Health, Prentice Hall, Englewood Cliffs, NJ, USA, 1993, https://www.worldcat.org/title/human-biology-and-health/oclc/32308337.
  8. B. D. Sidell and K. M. O'Brien, “When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes,” The Journal of Experimental Biology, vol. 209, part 10, pp. 1791–1802, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Hardison, “Hemoglobins from bacteria to man: evolution of different patterns of gene expression,” The Journal of Experimental Biology, vol. 201, no. 8, pp. 1099–1117, 1998. View at Google Scholar · View at Scopus
  10. R. Du, I. Winarsih, B. Ho, and L. J. Ding, “Lipid-free apolipoprotein A-I exerts an antioxidative role against cell-free hemoglobin,” The American Journal of Clinical and Experimental Immunology, vol. 1, no. 1, pp. 33–48, 2012, http://www.ncbi.nlm.nih.gov/pubmed/?term=Lipid-free+apolipoprotein+A-I+exerts+an+antioxidative+role++against+cell-free+hemoglobin. View at Google Scholar
  11. L. Liu, M. Zeng, and J. S. Stamler, “Hemoglobin induction in mouse macrophages,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 12, pp. 6643–6647, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. D. A. Newton, K. M. K. Rao, R. A. Dluhy, and J. E. Baatz, “Hemoglobin is expressed by alveolar epithelial cells,” Journal of Biological Chemistry, vol. 281, no. 9, pp. 5668–5676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Bhaskaran, H. Chen, Z. Chen, and L. Liu, “Hemoglobin is expressed in alveolar epithelial type II cells,” Biochemical and Biophysical Research Communications, vol. 333, no. 4, pp. 1348–1352, 2005. View at Publisher · View at Google Scholar
  14. N. Ishikawa, S. Ohlmeier, K. Salmenkivi et al., “Hemoglobin α and β are ubiquitous in the human lung, decline in idiopathic pulmonary fibrosis but not in COPD,” Respiratory Research, vol. 11, article 123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. T. H. Tezel, L. Geng, E. B. Lato et al., “Synthesis and secretion of hemoglobin by retinal pigment epithelium,” Investigative Ophthalmology & Visual Science, vol. 50, no. 4, pp. 1911–1919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Nishi, R. Inagi, H. Kato et al., “Hemoglobin is expressed by mesangial cells and reduces oxidant stress,” Journal of the American Society of Nephrology, vol. 19, no. 8, pp. 1500–1508, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. W. Liu, S. S. Baker, R. D. Baker, N. J. Nowak, and L. Zhu, “Upregulation of hemoglobin expression by oxidative stress in hepatocytes and its implication in nonalcoholic steatohepatitis,” PLoS ONE, vol. 6, no. 9, Article ID e24363, 2011. View at Publisher · View at Google Scholar
  18. M. Biagioli, M. Pinto, D. Cesselli et al., “Unexpected expression of α- and β-globin in mesencephalic dopaminergic neurons and glial cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 36, pp. 15454–15459, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Dassen, R. Kamps, C. Punyadeera et al., “Haemoglobin expression in human endometrium,” Human Reproduction, vol. 23, no. 3, pp. 635–641, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. X. Li, Z. Wu, Y. Wang, Q. Mei, X. Fu, and W. Han, “Characterization of adult α- and β-globin elevated by hydrogen peroxide in cervical cancer cells that play a cytoprotective role against oxidative insults,” PLoS ONE, vol. 8, no. 1, Article ID e54342, 2013. View at Google Scholar
  21. M. Patgaonkar, C. Aranha, G. Bhonde, and K. V. R. Reddy, “Identification and characterization of anti-microbial peptides from rabbit vaginal fluid,” Veterinary Immunology and Immunopathology, vol. 139, no. 2-4, pp. 176–186, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Cheung, B. Panning, and J. R. Smiley, “Herpes simplex virus immediate-early proteins ICP0 and ICP4 activate the endogenous human α-globin gene in nonerythroid cells,” Journal of Virology, vol. 71, no. 3, pp. 1784–1793, 1997. View at Google Scholar · View at Scopus
  23. M. Groudine and H. Weintraub, “Rous sarcoma virus activates embryonic globin genes in chicken fibroblasts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 72, no. 11, pp. 4464–4468, 1975. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Grek, D. Newton, D. Spyropoulos, and J. Baatz, “Hypoxia up-regulates expression of hemoglobin in alveolar epithelial cells,” The American Journal of Respiratory Cell and Molecular Biology, vol. 44, no. 4, pp. 439–447, 2011. View at Publisher · View at Google Scholar
  25. J. E. Grunwald, T. I. Metelitsina, J. C. DuPont, G.-S. Ying, and M. G. Maguire, “Reduced foveolar choroidal blood flow in eyes with increasing AMD severity,” Investigative Ophthalmology and Visual Science, vol. 46, no. 3, pp. 1033–1038, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Russo, S. Zucchelli, M. Codrich, F. Marcuzzi, C. Verde, and S. Gustincich, “Hemoglobin is present as a canonical α2β2 tetramer in dopaminergic neurons,” Biochimica et Biophysica Acta—Proteins and Proteomics, vol. 1834, no. 9, pp. 1939–1943, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. D. W. Schelshorn, A. Schneider, W. Kuschinsky et al., “Expression of hemoglobin in rodent neurons,” Journal of Cerebral Blood Flow & Metabolism, vol. 29, no. 3, pp. 585–595, 2009. View at Publisher · View at Google Scholar
  28. F. Richter, B. H. Meurers, C. Zhu, V. P. Medvedeva, and M.-F. Chesselet, “Neurons express hemoglobin α- and β-chains in rat and human brains,” Journal of Comparative Neurology, vol. 515, no. 5, pp. 538–547, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. T. B. Sherer, R. Betarbet, C. M. Testa, B. B. Seo, and J. R. Richardson, “Mechanism of toxicity in rotenone models of Parkinson's disease,” The Journal of Comparative Neurology, vol. 23, no. 34, pp. 10756–10764, 2003. View at Google Scholar
  30. A. S. Tsiftsoglou, A. I. Tsamadou, and L. C. Papadopoulou, “Heme as key regulator of major mammalian cellular functions: molecular, cellular, and pharmacological aspects,” Pharmacology and Therapeutics, vol. 111, no. 2, pp. 327–345, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. G. L. Wang and G. L. Semenza, “General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 9, pp. 4304–4308, 1993. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Jauniaux, L. Poston, and G. J. Burton, “Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution,” Human Reproduction Update, vol. 12, no. 6, pp. 747–755, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Kumar and U. Bandyopadhyay, “Free heme toxicity and its detoxification systems in human,” Toxicology Letters, vol. 157, no. 3, pp. 175–188, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. M. S. Patgaonkar, A. Sathe, C. Selvaakumar, and K. V. R. Reddy, “A rabbit vaginal cell-derived antimicrobial peptide, RVFHbαP, blocks lipopolysaccharide-mediated inflammation in human vaginal cells in vitro,” Clinical and Vaccine Immunology, vol. 18, no. 10, pp. 1632–1643, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. R. N. Fichorova, J. G. Rheinwald, and D. J. Anderson, “Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins,” Biology of Reproduction, vol. 57, no. 4, pp. 847–855, 1997. View at Publisher · View at Google Scholar · View at Scopus
  36. D. E. O'Hanlon, T. R. Moench, and R. A. Cone, “In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide,” BMC Infectious Diseases, vol. 11, article 200, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. C. C. Widmer, C. P. Pereira, P. Gehrig et al., “Hemoglobin can attenuate hydrogen peroxide-induced oxidative stress by acting as an antioxidative peroxidase,” Antioxidants and Redox Signaling, vol. 12, no. 2, pp. 185–198, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. E. T. Rietschel and H. Brade, “Bacterial endotoxins,” Scientific American, vol. 267, no. 2, pp. 54–61, 1992. View at Google Scholar · View at Scopus
  39. B. Beutler and E. T. Rietschel, “Innate immune sensing and its roots: the story of endotoxin,” Nature Reviews Immunology, vol. 3, no. 2, pp. 169–176, 2003. View at Google Scholar
  40. G. L. Su, R. D. Klein, A. Aminlari et al., “Kupffer cell activation by lipopolysaccharide in rats: role for lipopolysaccharide binding protein and Toll-like receptor 4,” Hepatology, vol. 31, no. 4, pp. 932–936, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Du, B. Ho, and J. L. Ding, “Rapid reprogramming of haemoglobin structure-function exposes multiple dual-antimicrobial potencies,” The EMBO Journal, vol. 29, no. 3, pp. 632–642, 2009. View at Google Scholar
  42. K. H. Cox, M. E. Cox, V. Woo-Rasberry, and D. L. Hasty, “Pathways involved in the synergistic activation of macrophages by lipoteichoic acid and hemoglobin,” PLoS ONE, vol. 7, no. 10, Article ID e47333, 2012. View at Publisher · View at Google Scholar
  43. J. Howe, M. Hammer, C. Alexander et al., “Biophysical characterization of the interaction of endotoxins with hemoglobins,” Medicinal Chemistry, vol. 3, no. 1, pp. 13–20, 2007. View at Publisher · View at Google Scholar
  44. M. H. Baron, “Transcriptional control of globin gene switching during vertebrate development,” Biochimica et Biophysica Acta, vol. 1351, no. 1-2, Article ID S0167478196001959, pp. 51–72, 1997. View at Publisher · View at Google Scholar
  45. T. Kawano, R. Pinontoan, H. Hosoya, and S. Muto, “Monoamine-dependent production of reactive oxygen species catalyzed by pseudoperoxidase activity of human hemoglobin,” Bioscience, Biotechnology and Biochemistry, vol. 66, no. 6, pp. 1224–1232, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. F. A. D. T. G. Wagener, H.-D. Volk, D. Willis et al., “Different faces of the heme-heme oxygenase system in inflammation,” Pharmacological Reviews, vol. 55, no. 3, pp. 551–571, 2003. View at Publisher · View at Google Scholar · View at Scopus