The respiratory proteins of insects

Journal of Insect Physiology

Volumn 53, Issue 4, 2007, Pages 285-294

  Burmester, Thorsten ^a   Hankeln, Thomas ^b  

^a UNIVERSITY OF HAMBURG   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Hemocyanin; Hemoglobin; Oxygen; Respiration; Trachea

Indexed keywords

HEMOGLOBIN; INSECT PROTEIN;

BUFFERING; HEMOGLOBIN; INSECT; OXYGEN; PHYSIOLOGY; RESPIRATION;

ANIMAL; ARTICLE; BREATHING; CLASSIFICATION; GENETICS; INSECT; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY;

ANIMALS; EVOLUTION, MOLECULAR; HEMOGLOBINS; INSECT PROTEINS; INSECTS; PHYLOGENY; RESPIRATION;

APIS; CHIRONOMIDAE; ENDOPTERYGOTA; HEXAPODA; NOTONECTIDAE; PLECOPTERA;

EID: 33947663458     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2006.12.006     Document Type: Article

References (88)

1. Amiconi G., Antonini E., Brunori M., Formaneck H., and Huber R. Functional properties of native and reconstituted hemoglobins from Chironomus thummi thummi. European Journal of Biochemistry 31 (1972) 52-58
2. Beintema J.J., Stam W.T., Hazes B., and Smidt M.P. Evolution of arthropod hemocyanins and insect storage proteins (hexamerins). Molecular Biology and Evolution 11 (1994) 493-503
3. Berg J.M., Tymoszko J.L., and Stryer L. Biochemistry (2002), W.H. Freeman and Co, New York
4. Bergtrom G. Partial characterization of haemoglobin of the bug, Buenoa confusa. Insect Biochemistry 7 (1977) 313-316
5. Bergtrom G., Laufer H., and Rogers R. Fat body: a site of hemoglobin synthesis in Chironomus thummi (Diptera). Journal of Cell Biology 69 (1976) 264-274
6. Brusca R.C., and Brusca G.J. Invertebrates. second ed (2002), Sinauer Associates, Sunderland, MA
7. Burmester T. Evolution and function of the insect hexamerins. European Journal of Entomology 96 (1999) 213-225
8. Burmester T. Identification, molecular cloning and phylogenetic analysis of a non-respiratory pseudo-hemocyanin of Homarus americanus. Journal of Biological Chemistry 274 (1999) 13217-13222
9. Burmester T. Molecular evolution of the arthropod hemocyanin superfamily. Molecular Biology and Evolution 18 (2001) 184-195
10. Burmester T. Origin and evolution of arthropod hemocyanins and related proteins. Journal of Comparative Physiology B 172 (2002) 95-117
11. Burmester T. A welcome shortage of breath. Nature 433 (2005) 471-472
12. Burmester T., and Hankeln T. A globin gene of Drosophila melanogaster. Molecular Biology and Evolution 16 (1999) 1809-1811
13. Burmester T., and Hankeln T. Neuroglobin: a respiratory protein of the nervous system. News in Physiological Sciences 19 (2004) 110-113
14. Burmester T., and Scheller K. Common origin of arthropod tyrosinase, arthropod hemocyanin, insect hexamerin and dipteran arylphorin receptor. Journal of Molecular Evolution 42 (1996) 713-728
15. Burmester T., Massey Jr. H.C., Zakharkin S.O., and Beneš H. The evolution of hexamerins and the phylogeny of insects. Journal of Molecular Evolution 47 (1998) 93-108
16. Burmester T., Weich B., Reinhardt S., and Hankeln T. A vertebrate globin expressed in the brain. Nature 407 (2000) 520-523
17. Burmester T., Storf J., Hasenjäger A., Klawitter S., and Hankeln T. The hemoglobin genes of Drosophila. The FEBS Journal 273 (2006) 468-480
18. Burmester, T., Klawitter, S., Hankeln, T. Characterization of two globin genes from the Malaria mosquito Anopheles gambiae: divergent origin of nematoceran hemoglobins. Insect Molecular Biology, in press.
19. de Sanctis D., Dewilde S., Pesce A., Moens L., Ascenzi P., Hankeln T., Burmester T., and Bolognesi M. Crystal structure of cytoglobin: the fourth globin type discovered in man displays heme hexa-coordination. Journal of Molecular Biology 336 (2004) 917-927
20. de Sanctis D., Dewilde S., Vonrhein C., Pesce A., Moens L., Ascenzi P., Hankeln T., Burmester T., Ponassi M., Nardini M., and Bolognesi M. Bis-histidyl heme hexacoordination, a key structural property in Drosophila melanogaster hemoglobin. Journal of Biological Chemistry 280 (2005) 27222-27229
21. Dewilde S., Blaxter M., Van Hauwaert M.L., Van Houte K., Pesce A., Griffon N., Kiger L., Marden M.C., Vermeire S., Vanfleteren J., Esmans E., and Moens L. Structural, functional, and genetic characterization of Gastrophilus hemoglobin. Journal of Biological Chemistry 273 (1998) 32467-32474
22. Dickerson R.E., and Geis I. Hemoglobin: Structure, Function, Evolution, and Pathology (1983), Benjamin/Cummings Publ. Co., California
23. Flögel U., Merx M.W., Gödecke A., Decking U.K., and Schrader J. Myoglobin: a scavenger of bioactive NO. Proceedings of the National Academy of Sciences USA 98 (2001) 735-740
24. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.L., and Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 (1999) 1531-1545
25. Fox H.M. The effect of oxygen on the concentration of haem in invertebrates. Proceedings of the Royal Society of London 143 (1955) 203-214
26. Freitas T.A., Saito J.A., Hou S., and Alam M. Globin-coupled sensors, protoglobins, and the last universal common ancestor. Journal of Inorganic Biochemistry 99 (2005) 23-33
27. Fukuda M., Takagi T., and Shikama K. Polymorphic hemoglobin from a midge larva (Tokunagayusurika akamusi) can be divided into two different types. Biochimica et Biophysica Acta 1157 (1993) 185-191
28. Giribet G., Edgecombe G.D., and Wheeler W.C. Arthropod phylogeny based on eight molecular loci and morphology. Nature 413 (2001) 157-161
29. Goodman M., Braunitzer G., Kleinschmidt T., and Aschauer H. The analysis of a protein-polymorphism. Evolution of monomeric and homodimeric haemoglobins (erythrocruorins) of Chironomus thummi thummi (Insecta, Diptera). Hoppe-Seylers Zeitschrift für Physiologische Chemie 364 (1983) 205-217
30. Gorr T.A., Tomita T., Wappner P., and Bunn H.F. Regulation of Drosophila hypoxia-inducible factor (HIF) activity in SL2 cells: identification of a hypoxia-induced variant isoform of the HIFalpha homolog gene similar. Journal of Biological Chemistry 279 (2004) 36048-36058
31. Green B.N., Kuchumov A.R., Hankeln T., Schmidt E.R., Bergtrom G., and Vinogradov S.N. An electrospray ionization mass spectrometric study of the extracellular hemoglobins from Chironomus thummi thummi. Biochimica et Biophysica Acta 1383 (1998) 143-150
32. Gruhl M., Kao W.Y., and Bergtrom G. Evolution of orthologous intronless and intron-bearing globin genes in two insect species. Journal of Molecular Evolution 45 (1997) 499-508
33. Hagner-Holler S., Schoen A., Erker W., Marden J.H., Rupprecht R., Decker H., and Burmester T. A respiratory hemocyanin from an insect. Proceedings of the National Academy of Sciences USA 101 (2004) 871-874
34. Halliwell B., and Gutteridge J.M.C. Free Radicals in Biology and Medicine (1999), Oxford University Press, Oxford
35. Hankeln T., Rozynek P., and Schmidt E.R. The nucleotide sequence and in situ localization of a gene for a dimeric haemoglobin from the midge Chironomus thummi piger. Gene 64 (1988) 297-304
36. Hankeln T., Friedl H., Ebersberger I., Martin J., and Schmidt E.R. A variable intron distribution in globin genes of Chironomus: evidence for recent intron gain. Gene 205 (1997) 151-160
37. Hankeln T., Amid C., Weich B., Niessing J., and Schmidt E.R. Molecular evolution of the globin gene cluster E in two distantly related midges, Chironomus pallidivittatus and C. thummi thummi. Journal of Molecular Evolution 46 (1998) 589-601
38. Hankeln T., Jaenicke V., Kiger L., Dewilde S., Ungerechts G., Schmidt M., Urban J., Marden M.C., Moens L., and Burmester T. Characterization of Drosophila hemoglobin: Evidence for hemoglobin-mediated respiration in insects. Journal of Biological Chemistry 277 (2002) 29012-29017
39. Hankeln T., Ebner B., Fuchs C., Gerlach F., Haberkamp M., Laufs T., Roesner A., Schmidt M., Weich B., Wystub S., Saaler-Reinhardt S., Reuss S., Bolognesi M., De Sanctis D., Marden M.C., Kiger L., Dewilde S., Moens L., Nevo E., Avivi A., Weber R.E., Fago A., and Burmester T. Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. Journal of Inorganic Biochemistry 99 (2005) 110-119
40. Hankeln T., Klawitter S., Krämer M., and Burmester T. Molecular characterisation of hemoglobin from the honeybee Apis mellifera. Journal of Insect Physiology 52 (2006) 701-710
41. Hardison R.C. A brief history of hemoglobins: plant, animal, protist, and bacteria. Proceedings of the National Academy of Sciences USA 93 (1996) 5675-5679
42. Hennig, W., 1969. Stammesgeschichte der Insekten. W Kramer, Frankfurt/M.
43. Hetz S.K., and Bradley T.J. Insects breathe discontinuously to avoid oxygen toxicity. Nature 433 (2005) 516-519
44. Huber R., Epp O., Steigemann W., and Formanek H. The atomic structure of erythrocruorin in the light of the chemical sequence and its comparison with myoglobin. European Journal of Biochemistry 19 (1971) 42-50
45. Hungerford H.B. Oxyhaemoglobin present in the backswimmer, Buenoa margaritacea, Bueno. The Canadian Entomologist 54 (1922) 262-263
46. Hwang U.W., Friedrich M., Tautz D., Park C.J., and Kim W. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413 (2001) 154-157
47. Jaenicke E., Decker H., Gebauer W., Markl J., and Burmester T. Identification, structure and properties of hemocyanins from diplopod Myriapoda. Journal of Biological Chemistry 274 (1999) 29071-29074
48. Jarial M.S. Fine structure of the Malpighian tubules of Chironomus larva in relation to glycogen storage and fate of hemoglobin. Tissue and Cell 20 (1988) 355-380
49. Kao W.Y., Hankeln T., Schmidt E.R., and Bergtrom G. Sequence and evolution of the gene for the monomeric globin I and its linkage to genes coding for dimeric globins in the insect Chironomus thummi. Journal of Molecular Evolution 40 (1995) 354-361
50. Keilin D., and Wang Y.L. Haemoglobin of Gastrophilus larvae. Purification and properties. Biochemical Journal 40 (1946) 855-866
51. Kestler P. In: Hoffmann K.H. (Ed). Environmental Physiology and Biochemistry of Insects (1985), Springer, Berlin 137-186
52. Komai Y. Augmented respiration in a flying insect. Journal of Experimental Biology 201 (1998) 2359-2366
53. Krogh A. Studien über Tracheenrespiration. II. Über Gasdiffusion in den Tracheen. Pflügers Archiv für die Gesamte Physiologie des Menschen und der Tiere 179 (1920) 95-120
54. Kukalovà-Peck J. Fossil history and evolution of hexapod structures. In: Naumann I.D. (Ed). The Insects of Australia (1991), Melbourne University Press, Melbourne, Australia 141-179
55. Kusche K., and Burmester T. Diplopod hemocyanin sequence and the phylogenetic position of the Myriapoda. Molecular Biology and Evolution 18 (2001) 1566-1573
56. Kusche K., Ruhberg H., and Burmester T. A hemocyanin from the Onychophora and the emergence of respiratory proteins. Proceedings of the National Academy of Sciences USA 99 (2002) 10545-10548
57. Kusche K., Hembach A., Hagner-Holler S., Gebauer W., and Burmester T. Complete subunit sequences, structure and evolution of the 6×6-mer hemocyanin from the common house centipede, Scutigera coleoptrata. European Journal of Biochemistry 270 (2003) 2860-2868
58. Lankester E.R. A contribution to the knowledge of haemoglobin. Proceedings of the Royal society of London 21 (1872) 70-81
59. Law J.H., and Wells M.A. Insects as biochemical models. Journal of Biological Chemistry 264 (1989) 16335-16338
60. Lehmann F.O. Matching spiracle opening to metabolic need during flight in Drosophila. Science 294 (2001) 1926-1929
61. Locke M. Caterpillars have evolved lungs for hemocyte gas exchange. Journal of Insect Physiology 44 (1998) 1-20
62. Mangum C.P. Oxygen transport in invertebrates. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 248 (1985) 505-514
63. Markl J., and Decker H. Molecular structure of the arthropod hemocyanins. Advances in Comparative and Environmental Physiology 13 (1992) 325-376
64. Matthews P.G.D., and Seymour R.S. Diving insects boost their buoyancy bubbles. Nature 441 (2006) 171
65. Miller P.L. Possible function of haemoglobin in Anisops. Nature 201 (1964) 1052
66. Miller P.L. The function of haemoglobin in relation to the maintenance of neutral buoyancy in Anisops pellucens (Notonectidae, Hemiptera). Journal of Experimental Biology 44 (1966) 529-543
67. Osmulski P.A., and Leyko W. Structure, function and physiological role of Chironomus hemoglobin. Comparative Biochemistry and Physiology 85B (1986) 701-722
68. Pesce A., Dewilde S., Nardini M., Moens L., Ascenzi P., Hankeln T., Burmester T., and Bolognesi M. Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity. Structure 11 (2003) 1087-1095
69. Pesce A., Nardini M., Dewilde S., Hoogewijs D., Ascenzi P., Moens L., and Bolognesi M. Modulation of oxygen binding to insect hemoglobins: The structure of hemoglobin from the botfly Gasterophilus intestinalis. Protein Science 14 (2005) 3057-3063
70. Rollett A. Zur Kenntnis der Verbreitung des Hämatins. Sitzungsberichte der kaiserlichen Akademie der Wissenschaften zu Wien 44 (1861) 615-630
71. Ruf H.H., Altemüller A.G., and Gersonde K. Preparation and characterization of insect hemoglobins from Chironomus thummi thummi. Methods in Enzymology 231 (1994) 95-111
72. Saffarini D.A., Trewitt P.M., Luhm R.A., and Bergtrom G. Differential regulation of insect globin and actin mRNAs during larval development in Chironomus thummi. Gene 101 (1991) 215-222
73. Sánchez D., Ganfornina M.D., Gutiérrez G., and Bastiani M.J. Molecular characterization and phylogenetic relationship of a protein with oxygen-binding capabilities in the grasshopper embryo. A hemocyanin in insects?. Molecular Biology and Evolution 15 (1998) 415-426
74. Telfer W.H., and Kunkel J.G. The function and evolution of insect storage hexamers. Annual Review of Entomology 36 (1991) 205-228
75. Terwilliger N.B., Dangott L.J., and Ryan M.C. Cryptocyanin, a crustacean molting protein: evolutionary links to arthropod hemocyanin and insect hexamerins. Proceedings of the National Academy of Sciences USA 96 (1999) 2013-2018
76. Trewitt P.M., Boyer D.R., and Bergtrom G. Characterization of maternal haemoglobins in the eggs and embryos of Chironomus thummi. Journal of Insect Physiology 32 (1986) 963-969
77. Trewitt P.M., Luhm R.A., Samad F., Ramakrishnan S., Kao W.Y., and Bergtrom G. Molecular evolutionary analysis of the YWVZ/7B globin gene cluster of the insect Chironomus thummi. Journal of Molecular Evolution 41 (1995) 313-328
78. van Holde K.E., Miller K.I., and Decker H. Hemocyanins and invertebrate evolution. Journal of Biological Chemistry 276 (2001) 15563-15566
79. Vinogradov S.N. The structure of invertebrate extracellular hemoglobins (erythrocruorins and chlorocruorins). Comparative Biochemistry and Physiology B Biochemistry 82 (1985) 1-15
80. Vinogradov S.N., Hoogewijs D., Bailly X., Arredondo-Peter R., Guertin M., Gough J., Dewilde S., Moens L., and Vanfleteren J.R. Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proceedings of the National Academy of Sciences USA 102 (2005) 11385-11389
81. Walshe B.M. The function of haemoglobin in relation to filter feeding in leaf-mining chironomid larvae. Journal of Experimental Biology 28 (1951) 57-61
82. Weber R.E., Braunitzer G., and Kleinschmidt T. Functional multiplicity and structural correlations in the hemoglobin system of larvae of Chironomus thummi thummi (Insecta, Diptera): Hb components CTT I, CTT II, CTT III, CTT IV, CTT VI, CTT VIIB, CTT IX and CTT X. Comparative Biochemistry and Physiology B Biochemistry 80 (1985) 747-753
83. Weber R.E., and Vinogradov S.N. Nonvertebrate hemoglobins: functions and molecular adaptations. Physiological Reviews 81 (2001) 569-628
84. Wells R.M.G., Hudson M.J., and Brittain T. Function of the hemoglobin and the gas bubble in the backswimmer Anisops assimilis (Hemiptera: Notonectidae). Journal of Comparative Physiology B 142 (1981) 515-522
85. Westneat M.W., Betz O., Blob R.W., Fezzaa K., Cooper W.J., and Lee W.K. Tracheal respiration in insects visualized with synchrotron X-ray imaging. Science 299 (2003) 558-560
86. Wheeler W.C., Whiting M., Wheeler Q.D., and Carpenter J.M. The phylogeny of the extant hexapod orders. Cladistics 17 (2001) 113-169
87. Willmer P., Stone G., and Johnston I. Environmental Physiology of Animals (2000), Blackwell, Oxford
88. Wittenberg J.B., and Wittenberg B.A. Myoglobin function reassessed. Journal of Experimental Biology 206 (2003) 2011-2020