Regulation of amino acid and nucleotide metabolism by crustacean hyperglycemic hormone in the muscle and hepatopancreas of the crayfish Procambarus clarkia

English version

Autoři: Wenfeng Li ^aff001; Kuo-Hsun Chiu ^aff003; Chi-Ying Lee ^aff002
Působiště autorů: College of Ocean and Earth Sciences, Xiamen University, Fujian, China ^aff001; Department of Biology, National Changhua University of Education, Changhua, Taiwan ^aff002; Department of Aquaculture, National Kaohsiung University of Science and Technology, Kaohsiung, Taiwan ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221745

Souhrn

To comprehensively characterize the metabolic roles of crustacean hyperglycemic hormone (CHH), metabolites in two CHH target tissues of the crayfish Procambarus clarkii, whose levels were significantly different between CHH knockdown and control (saline-treated) animals, were analyzed using bioinformatics tools provided by an on-line analysis suite (MetaboAnalyst). Analysis with Metabolic Pathway Analysis (MetPA) indicated that in the muscle Glyoxylate and dicarboxylate metabolism, Nicotinate and nicotinamide metabolism, Alanine, aspartate and glutamate metabolism, Pyruvate metabolism, and Nitrogen metabolism were significantly affected by silencing of CHH gene expression at 24 hours post injection (hpi), while only Nicotinate and nicotinamide metabolism remained significantly affected at 48 hpi. In the hepatopancreas, silencing of CHH gene expression significantly impacted, at 24 hpi, Pyruvate metabolism and Glycolysis or gluconeogenesis, and at 48 hpi, Glycine, serine and threonine metabolism. Moreover, analysis using Metabolite Set Enrichment Analysis (MSEA) showed that many metabolite sets were significantly affected in the muscle at 24hpi, including Ammonia recycling, Nicotinate and nicotinamide metabolism, Pyruvate metabolism, Purine metabolism, Warburg effect, Citric acid cycle, and metabolism of several amino acids, and at 48 hpi only Nicotinate and nicotinamide metabolism, Glycine and serine metabolism, and Ammonia recycling remained significantly affected. In the hepatopancreas, MSEA analysis showed that Fatty acid biosynthesis was significantly impacted at 24 hpi. Finally, in the muscle, levels of several amino acids decreased significantly, while those of 5 other amino acids or related compounds significantly increased in response to CHH gene silencing. Levels of metabolites related to nucleotide metabolism significantly decreased across the board at both time points. In the hepatopancreas, the effects were comparatively minor with only levels of thymine and urea being significantly decreased at 24 hpi. The combined results showed that the metabolic effects of silencing CHH gene expression were far more diverse than suggested by previous studies that emphasized on carbohydrate and energy metabolism. Based on the results, metabolic roles of CHH on the muscle and hepatopancreas are suggested: CHH promotes carbohydrate utilization in the hepatopancreas via stimulating glycolysis and lipolysis, while its stimulatory effect on nicotinate and nicotinamide metabolism plays a central role in coordinating metabolic activity in the muscle with diverse and wide-ranging consequences, including enhancing the fluxes of glycolysis, TCA cycle, and pentose phosphate pathway, leading to increased ATP supply and elevated protein and nucleic acid turnovers.

Klíčová slova:

Gene expression – Carbohydrate metabolism – Amino acid analysis – Metabolic pathways – Nicotine – Amino acid metabolism – Nitrogen metabolism – Purine metabolism

Zdroje

1. Cooke IM, Sullivan RE. Hormones and neurosecretion. In: Atwood HL, Sandeman DC, editors. New York: Academic Press. The Biology of Crustacea. 1982; 3: 206–290.

2. Soyez D. Occurrence and diversity of neuropeptides from the crustacean hyperglycemic hormone family in arthropods. Ann N Y Acad Sci. 1997; 814: 319–323. doi: 10.1111/j.1749-6632.1997.tb46174.x 9160986

3. Huberman A, Aguilar MB. Single step purification of two hyperglycaemic neurohormones from the sinus gland of Procambarus bouvieri: Comparative peptide mapping by means of high-performance liquid chromatography. J Chromatogr. 1988; 443: 337–342. doi: 10.1016/s0021-9673(00)94805-2 2902105

4. Kegel G, Reichwein B, Weese S, Gaus G, Peter-Katalinić J, Keller R. Amino acid sequence of the crustacean hyperglycemic hormone (CHH) from the shore crab, Carcinus maenas. FEBS Letters. 1989; 255: 10–14. doi: 10.1016/0014-5793(89)81051-8 2792364

5. Chang ES, Prestwich GD, Bruce MJ. Amino acid sequence of a peptide with both molt-inhibiting activity and hyperglycemic activities in the lobster Homarus americanus. Biochem Bioph Res Co. 1990; 171: 818–826.

6. Soyez D, Noel PY, Van Deijnen JE, Martin M, Morel A, Payen GG. Neuropeptides from the sinus gland of the lobster Homarus americanus: Characterization of hyperglycemic peptides. Gen Comp Endocrinol. 1990; 79: 261–274. doi: 10.1016/0016-6480(90)90112-y 2391028

7. Huberman A, Aguilar MB, Brew K, Shabanowitz J, Hunt DF. Primary structure of the major isomorph of the crustacean hyperglycemic hormone (CHH-I) from the sinus gland of the Mexican crayfish Procambarus bouvieri (Ortmann): Interspecies comparison. Peptides. 1993; 14: 7–16. doi: 10.1016/0196-9781(93)90004-z 8441709

8. Yasuda A, Yasuda Y, Fujita T, Naya Y. Characterization of crustacean hyperglycemic hormone from the crayfish (Procambarus clarkii): Multiplicity of molecular forms by stereoinversion and diverse functions. Gen Comp Endocrinol. 1994; 95: 387–398. doi: 10.1006/gcen.1994.1138 7821776

9. Soyez D, Van Herp F, Rossier J, Le Caer JP, Tensen CP, Lafont R. Evidence for a conformational polymorphism of invertebrate neurohormones. J Biol Chem. 1994; 269: 18295–18298. 8034574

10. Katayam H, Ohira T, Aida K, Nagasawa H. Significance of a carboxyl-terminal amide moiety in the folding and biological activity of crustacean hyperglycemic hormone. Peptides 2002; 23: 1537–1546. doi: 10.1016/s0196-9781(02)00094-3 12217413

11. Mosco A, Edomi P, Guarnaccia C, Lorenzon S, Pongor S, Ferrero EA, et al. Functional aspects of cHH C-terminal amidation in crayfish species. Regul Pept. 2008; 147: 88–95. doi: 10.1016/j.regpep.2008.01.005 18281112

12. Chang CC, Tsai TW, Hsiao NW, Chang CY, Lin CL, Watson RD, et al. Structural and functional comparisons and production of recombinant crustacean hyperglycemic hormone (CHH) and CHH-like peptides from the mud crab Scylla olivacea. Gen Comp Endocrinol. 2010; 167: 68–76. doi: 10.1016/j.ygcen.2010.02.013 20171218

13. Morris S, Postel U, Mrinalini Turner LM, Palmer J, Webster SG. The adaptive significance of crustacean hyperglycaemic hormone (CHH) in daily and seasonal migratory activities of the Christmas Island red crab Gecarcoidea natalis. J Exp Biol. 2010; 213: 3062–3073. doi: 10.1242/jeb.045153 20709934

14. Liu CJ, Huang SS, Toullec JY, Chang CY, Chen YR, Huang WS, et al. Functional assessment of residues in the amino- and carboxyl-termini of crustacean hyperglycemic hormone (CHH) in the mud crab Scylla olivacea using point-mutated peptides. PLOS ONE. 2015; 10(8): e0134983. doi: 10.1371/journal.pone.0134983 26261986

15. De Kleijn DP, Van Herp F. Molecular biology of neurohormone precursors in the eyestalk of Crustacea. Comp Biochem Physiol. 1995; 112: 573–579.

16. Chan SM, Gu PL, Chu KH, Tobe SS. Crustacean neuropeptide genes of the CHH/MIH/GIH family: implications from molecular studies. Gen Comp Endocrinol. 2003; 134: 214–219. doi: 10.1016/s0016-6480(03)00263-6 14636627

17. Chen SH, Lin CY, Kuo CM. In silico analysis of crustacean hyperglycemic hormone family. Mar Biotechnol. 2005; 7: 193–206. doi: 10.1007/s10126-004-0020-5 15933902

18. Kegel G, Reichwein B, Tensen CP, Keller R. Amino acid sequence of crustacean hyperglycemic hormone (CHH) from the crayfish, Orconectes limosus: Emergence of a novel neuropeptide family. Peptides. 1991; 12(5): 909–913. doi: 10.1016/0196-9781(91)90036-o 1800954

19. Keller R. Crustacean neuropeptides: Structures, functions, and comparative aspects. Experientia. 1992; 48: 439–448. doi: 10.1007/bf01928162 1601108

20. Montagné N, Desdevises Y, Soyez D, Toullec JY. Molecular evolution of the crustacean hyperglycemic hormone family in ecdysozoans. BMC Evo Biol. 2010; 10: 62.

21. Webster SG, Keller R, Dircksen H. The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. Gen Comp Endocrinol. 2012; 175: 217–233. doi: 10.1016/j.ygcen.2011.11.035 22146796

22. Santos EA, Keller R. Effect of exposure to atmospheric air on blood glucose and lactate concentrations in two crustacean species: A role of the crustacean hyperglycemic hormone (CHH). Comp Biochem Physiol A. 1993; 106: 343–347.

23. Webster SG. Measurement of crustacean hyperglycemic hormone levels in the edible crab Cancer pagurus during emersion stress. J Exp Bio. 1996; 199: 1579–1585.

24. Chang ES, Keller R, Chang SA. Quantification of crustacean hyperglycemic hormone by ELISA in hemolymph of the lobster, Homarus americanus, following various stresses. Gen Comp Endocrinol. 1998; 111: 359–366. doi: 10.1006/gcen.1998.7120 9707481

25. Chang ES, Chang SA, Beltz BS, Kravitz EA. Crustacean hyperglycemic hormone in the lobster nervous system: localization and release from cells in the subesophageal ganglion and thoracic second roots. J Comp Neurol. 1999; 414: 50–56. 10494077

26. Zou HS, Juan CC, Chen SC, Wang HY, Lee CY. Dopaminergic regulation of crustacean hyperglycemic hormone and glucose levels in the hemolymph of the crayfish Procambarus clarkii. J Exp Zool. 2003; 298: 44–52.

27. Lorenzon S, Edomi P, Giulianini PG, Mettulio R, Ferrero EA. Variation of crustacean hyperglycemic hormone (CHH) level in the eyestalk and haemolymph of the shrimp Palaemon elegans following stress. J Exp Biol. 2004; 207: 4205–4213. doi: 10.1242/jeb.01264 15531641

28. Parvathy D. Endocrine regulation of carbohydrate metabolism during the moult cycle in crustaceans I. Effect of eyestalk removal in Ocypoda platytarsis. Mar Biol. 1972; 14: 58.

29. Keller R, Andrew EM. The site of action of the crustacean hyperglycemic hormone. Gen Comp Endocrinol. 1973; 20: 572–578. doi: 10.1016/0016-6480(73)90089-0 4715238

30. Sedlmeier D. Studies on glycogen synthesis and breakdown in isolated hepatopancreas of Orconectes limoaue (Crustacea, Decapoda). Biochem Soc Trans. 1981; 9: 240.

31. Sedlmeier D. The role of hepatopancreatic glycogen in the action of the crustacean hyperglycemic hormone (CHH). Comp Biochem Physiol A. 1987; 87: 423–425.

32. Nagai C, Nagata S, Nagasawa H. Effects of crustacean hyperglycemic hormone (CHH) on the transcript expression of carbohydrate metabolism-related enzyme genes in the kuruma prawn Marsupenaeus japonicus. Gen Comp Endocrinol. 2011; 172: 293–304. doi: 10.1016/j.ygcen.2011.03.019 21447337

33. Santos EA, Keller R. Crustacean hyperglycemic hormone (CHH) and the regulation of carbohydrate metabolism: current perspectives. Comp Biochem Physiol A. 1993; 106: 405–411.

34. Li W, Chiu KH, Tien YC, Tsai SF, Shih LJ, Lee CH, et al. Differential effects of silencing crustacean hyperglycemic hormone gene expression on the metabolic profiles of the muscle and hepatopancreas in the crayfish Procambarus clarkii. PLOS ONE. 2017; 12(2): e0172557. doi: 10.1371/journal.pone.0172557 28207859

35. Xia J, Sinelnikov I, Han B, Wishart DS. MetaboAnalyst 3.0—making metabolomics more meaningful. Nucl Acids Res. 2015; 43: W251–257. doi: 10.1093/nar/gkv380 25897128

36. Xia J, Wishart DS. MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics. 2010; 26(18): 2342–2344. doi: 10.1093/bioinformatics/btq418 20628077

37. Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, et al. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucl Acids Res. 2018; 46(W1): W486–94. doi: 10.1093/nar/gky310 29762782

38. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Masumi Itoh M, et al. KEGG for linking genomes to life and the environment. Nucl Acids Res. 2008; 36: 480–484.

39. Xia J, Wishart DS. MSEA: a web-based tool to identify biologically meaningful patterns in quantitative metabolomic data. Nucl Acids Res. 2010; 38: W71–W77. doi: 10.1093/nar/gkq329 20457745

40. Xia J, Wishart DS. Using MetaboAnalyst 3.0 for Comprehensive Metabolomics Data Analysis. Curr Protoc Bioinformatics. 2016; 55: 14.10.1–14.10.91.

41. Pilz RB, Willis RC, Boss GR. The influence of ribose 5-phosphate availability on purine synthesis of cultured human lymphoblasts and mitogen-stimulated lymphocytes. J Biol Chem. 1984; 259(5): 2927–2935. 6699001

42. Rey G, Valekunja UK, Feeney KA, Wulund L, Milev NB, Stangherlin A, et al. The pentose phosphate pathway regulates the circadian clock. Cell Metabolism. 2016; 24(13): 462–473.

43. Hove-Jensen B, Andersen KR, Kilstrup M, Martinussen J, Switzer RL, Willemoes M. Phosphoribosyl diphosphate (PRPP): biosynthesis, enzymology, utilization, and metabolic significance. Microbiol Mol Biol R. 2017; 81(1): e00040–16.

44. Moran LA, Scrimgeour KG, Horton HR, Ochs RS, Rawn JD. New Jersey: Neil Patterson Publishers/Prentice-Hall Inc. Biochemistry. 1994.

45. Boldyrev AA, Stvolinsky SL, Fedorova TN, Suslina ZA. Carnosine as a natural antioxidant and geroprotector: from molecular mechanisms to clinical trials. Rejuv Res. 2010; 13(2–3): 156–158.

46. Xie Z, Baba SP, Sweeney BR, Barski OA. Detoxification of aldehydes by histidine-containing dipeptides: from chemistry to clinical implications. Chem Biol Interact. 2013; 202(1–3): 288–297. doi: 10.1016/j.cbi.2012.12.017 23313711

47. Chen IT, Aoki T, Huang YT, Hirono I, Chen TC, Huang JY, et al. White spot syndrome virus induces metabolic changes resembling the Warburg effect in shrimp hemocytes in the early stage of infection. J Virol. 2011; 85(24): 12919–12928. doi: 10.1128/JVI.05385-11 21976644

48. Lin LJ, Chen YJ, Chang YS, Lee CY. Neuroendocrine responses of a crustacean host to viral infection: Effects of infection of white spot syndrome virus on the expression and release of crustacean hyperglycemic hormone in the crayfish Procambarus clarkii. Comp Biochem Physiol A. 2013; 164(2): 327–332.

49. Santos EA, Eduardo L, Nery M, Gonçalves AA, Keller R. Evidence for the involvement of the crustacean hyperglycemic hormone in the regulation of lipid metabolism. Physiol Zool. 1997; 70(4): 415–420. doi: 10.1086/515846 9237301

50. Sedlmeier D, Keller R. The mode of action of the crustacean neurosecretory hyperglycemic hormone. I. Involvement of cyclic nucleotides. Gen Comp Endocrinol. 1981; 45 (1): 82–90. doi: 10.1016/0016-6480(81)90172-6 6269955

Regulation of amino acid and nucleotide metabolism by crustacean hyperglycemic hormone in the muscle and hepatopancreas of the crayfish Procambarus clarkia

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