Crustacean Hyperglycemic Hormone of Portunus Trituberculatus: Evidence of Alternative Splicing and Potential Roles in Osmoregulation

Overview

Journal Cell Stress Chaperones

Publisher Elsevier

Specialty Cell Biology

Date 2019 Feb 16

PMID 30767165

Citations 8

Authors

Dongfang Sun

Jianjian Lv

Baoquan Gao

Ping Liu

Jian Li

Affiliations

Soon will be listed here.

Abstract

The crustacean hyperglycemic hormone (CHH) gene of Portunus trituberculatus (Pt-CHH) consists of four exons and three introns spanning 3849 bp in size and generating two mature mRNA, Pt-CHH1, and Pt-CHH2. The primary gene transcript produces a cDNA encoding for the putative Pt-CHH2 from exons 1, 2, 3, and 4 and an alternative transcript encodes for a putative Pt-CHH1 peptide from exons 1, 2, and 4. A promoter fragment of about 3 kb was obtained by genomic walking. The tissue-specific expression pattern is examined by reverse transcriptase chain reaction, and the results show that Pt-CHH1 is detected in the eyestalk, brain, muscle, and blood. However, Pt-CHH2 is detected in the ganglia thoracalis and gill. The results indicate that the expression of Pt-CHH2 in the gill might suggest a potential role in osmoregulation. The Pt-CHH transcript level in the gill increases when the crab is exposed to low salinity. The injection of dsRNA for Pt-CHH causes a significant reduction in Pt-CHH2 transcript level and the activity of Na/K-ATPase, and carbonic anhydrase (CA) show a serious decrease. In conclusion, this study provides molecular evidence to support the osmoregulatory function of Pt-CHH2.

Citing Articles

Silencing Multiple Crustacean Hyperglycaemic Hormone-Encoding Genes in the Redclaw Crayfish Induces Faster Molt Rates with Anomalies.

Black N, Banks T, Glendinning S, Chowdhury G, Mykles D, Ventura T Int J Mol Sci. 2024; 25(22).

PMID: 39596377 PMC: 11594818. DOI: 10.3390/ijms252212314.

Analysis of adaptive molecular mechanisms in response to low salinity in antennal gland of mud crab, .

Mo N, Feng T, Zhu D, Liu J, Shao S, Han R Heliyon. 2024; 10(3):e25556.

PMID: 38356600 PMC: 10865330. DOI: 10.1016/j.heliyon.2024.e25556.

Eyestalk transcriptome and methyl farnesoate titers provide insight into the physiological changes in the male snow crab, Chionoecetes opilio, after its terminal molt.

Toyota K, Yamamoto T, Mori T, Mekuchi M, Miyagawa S, Ihara M Sci Rep. 2023; 13(1):7204.

PMID: 37137964 PMC: 10156855. DOI: 10.1038/s41598-023-34159-y.

Neuropeptides in Rhipicephalus microplus and other hard ticks.

Waldman J, Xavier M, Vieira L, Logullo R, Braz G, Tirloni L Ticks Tick Borne Dis. 2022; 13(3):101910.

PMID: 35121230 PMC: 9477089. DOI: 10.1016/j.ttbdis.2022.101910.

Characterization of From the Marine Crab and Its Functions Under Low Salinity Conditions.

Ren X, Wang L, Xu Y, Wang Q, Lv J, Liu P Front Physiol. 2021; 12:724693.

PMID: 34744765 PMC: 8568311. DOI: 10.3389/fphys.2021.724693.

References

Meredith J, Ring M, Macins A, Marschall J, Cheng N, Theilmann D . Locust ion transport peptide (ITP): primary structure, cDNA and expression in a baculovirus system. J Exp Biol. 1996; 199(Pt 5):1053-61. DOI: 10.1242/jeb.199.5.1053. View

Bansal M, Kumar A, Yella V . Role of DNA sequence based structural features of promoters in transcription initiation and gene expression. Curr Opin Struct Biol. 2014; 25:77-85. DOI: 10.1016/j.sbi.2014.01.007. View

Westenberg M, Heinhuis B, Zuidema D, Vlak J . siRNA injection induces sequence-independent protection in Penaeus monodon against white spot syndrome virus. Virus Res. 2005; 114(1-2):133-9. DOI: 10.1016/j.virusres.2005.06.006. View

Furriel R, McNamara J, Leone F . Characterization of (Na+, K+)-ATPase in gill microsomes of the freshwater shrimp Macrobrachium olfersii. Comp Biochem Physiol B Biochem Mol Biol. 2000; 126(3):303-15. DOI: 10.1016/s0305-0491(00)00184-x. View

Camacho-Jimenez L, Diaz F, Sanchez-Castrejon E, Ponce-Rivas E . Effects of the recombinant crustacean hyperglycemic hormones rCHH-B1 and rCHH-B2 on the osmo-ionic regulation of the shrimp Litopenaeus vannamei exposed to acute salinity stress. J Comp Physiol B. 2018; 188(4):565-579. DOI: 10.1007/s00360-018-1151-8. View

Turner L, Webster S, Morris S . Roles of crustacean hyperglycaemic hormone in ionic and metabolic homeostasis in the Christmas Island blue crab, Discoplax celeste. J Exp Biol. 2012; 216(Pt 7):1191-201. DOI: 10.1242/jeb.078527. View

Lacombe C, Greve P, Martin G . Overview on the sub-grouping of the crustacean hyperglycemic hormone family. Neuropeptides. 2000; 33(1):71-80. DOI: 10.1054/npep.1999.0016. View

Xie X, Zhu D, Yang J, Qiu X, Cui X, Tang J . Molecular cloning of two structure variants of crustacean hyperglycemic hormone (CHH) from the swimming crab (Portunus trituberculatus), and their gene expression during molting and ovarian development. Zoolog Sci. 2014; 31(12):802-9. DOI: 10.2108/zs140053. View

Ponprateep S, Tharntada S, Somboonwiwat K, Tassanakajon A . Gene silencing reveals a crucial role for anti-lipopolysaccharide factors from Penaeus monodon in the protection against microbial infections. Fish Shellfish Immunol. 2011; 32(1):26-34. DOI: 10.1016/j.fsi.2011.10.010. View

10.

McNamara J, Faria S . Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J Comp Physiol B. 2012; 182(8):997-1014. DOI: 10.1007/s00360-012-0665-8. View

11.

Chung J, Dircksen H, Webster S . A remarkable, precisely timed release of hyperglycemic hormone from endocrine cells in the gut is associated with ecdysis in the crab Carcinus maenas. Proc Natl Acad Sci U S A. 1999; 96(23):13103-7. PMC: 23907. DOI: 10.1073/pnas.96.23.13103. View

12.

Webster S, Keller R, Dircksen H . The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. Gen Comp Endocrinol. 2011; 175(2):217-33. DOI: 10.1016/j.ygcen.2011.11.035. View

13.

Lucu C, Towle D . Na(+)+K(+)-ATPase in gills of aquatic crustacea. Comp Biochem Physiol A Mol Integr Physiol. 2003; 135(2):195-214. DOI: 10.1016/s1095-6433(03)00064-3. View

14.

Gu P, Chan S . The shrimp hyperglycemic hormone-like neuropeptide is encoded by multiple copies of genes arranged in a cluster. FEBS Lett. 1999; 441(3):397-403. DOI: 10.1016/s0014-5793(98)01573-7. View

15.

Spanings-Pierrot C, Soyez D, Van Herp F, Gompel M, Skaret G, Grousset E . Involvement of crustacean hyperglycemic hormone in the control of gill ion transport in the crab Pachygrapsus marmoratus. Gen Comp Endocrinol. 2000; 119(3):340-50. DOI: 10.1006/gcen.2000.7527. View

16.

Lu W, Wainwright G, Olohan L, Webster S, Rees H, Turner P . Characterization of cDNA encoding molt-inhibiting hormone of the crab, Cancer pagurus; expression of MIH in non-X-organ tissues. Gene. 2001; 278(1-2):149-59. DOI: 10.1016/s0378-1119(01)00708-9. View

17.

Tiu S, He J, Chan S . The LvCHH-ITP gene of the shrimp (Litopenaeus vannamei) produces a widely expressed putative ion transport peptide (LvITP) for osmo-regulation. Gene. 2007; 396(2):226-35. DOI: 10.1016/j.gene.2007.02.027. View

18.

Chen S, Lin C, Kuo C . Cloning of two crustacean hyperglycemic hormone isoforms in freshwater giant prawn (Macrobrachium rosenbergii): evidence of alternative splicing. Mar Biotechnol (NY). 2003; 6(1):83-94. DOI: 10.1007/s10126-003-0014-8. View

19.

Serrano L, Blanvillain G, Soyez D, Charmantier G, Grousset E, Aujoulat F . Putative involvement of crustacean hyperglycemic hormone isoforms in the neuroendocrine mediation of osmoregulation in the crayfish Astacus leptodactylus. J Exp Biol. 2003; 206(Pt 6):979-88. DOI: 10.1242/jeb.00178. View

20.

Henry R, Campoverde M . Neuroendocrine regulation of carbonic anhydrase expression in the gills of the euryhaline green crab, Carcinus maenas. J Exp Zool A Comp Exp Biol. 2006; 305(8):663-8. DOI: 10.1002/jez.a.321. View