Advertisement

Biologia

, Volume 73, Issue 3, pp 227–240 | Cite as

Molecular characterization and tissue expression profiles of insulin-like growth factor binding protein-1 (IGFBP-1) in Chinese alligator Alligator sinensis during the active and hibernating periods

  • Mengyun Li
  • Ting Meng
  • Fei Peng
  • Shengzhou Zhang
  • Yongkang Zhou
  • Xiaobing Wu
Original Article
  • 36 Downloads

Abstract

The Chinese alligator Alligator sinensis (Fauvel, 1879) is an endangered species endemic to China. Up to this date, very little is known about the regulation of its growth and development. Insulin-like growth factor binding protein-1 (IGFBP-1) plays essential roles in regulating vertebrate growth and development by modulating IGFs action. In this study, we cloned the full-length cDNA of Chinese alligator IGFBP-1 (caIGFBP-1) for the first time, which has an open reading frame (ORF) of 885-bp nucleotides encoding a peptide of 294 amino acid residues. The caIGFBP-1 contains all features of IGFBP-1 peptide with the conserved cysteine-rich N- and C-terminal domains and variable central L-domain. Multiple alignment analysis showed that caIGFBP-1 shares high identity in amino acid sequence with the IGFBP-1 s of American alligator Alligator mississippiensis (Daudin, 1802) (99.32%) and birds (66.32–74.53%). Phylogenetic tree analysis of IGFBP-1 amino acid sequences indicated that alligators cluster into bird branch. The caIGFBP-1 is widely expressed in all the examined tissues, the expression level is highest in liver, higher in kidney, moderate in pancreas, stomach, small intestine, and lower in ovary, muscle, lung, heart. During the hibernating period, the expression level of caIGFBP-1 was significantly reduced in liver, kidney, stomach, pancreas and small intestine, while did not significantly change in heart, lung, ovary and muscle. The caIGFBP-1 mRNA expression changes during the active and hibernating periods, which coincides with that of Chinese alligator IGF, implicating that it might play important roles in the IGF-mediated growth and development of Chinese alligator.

Keywords

Chinese alligator IGFBP-1 cDNA cloning Gene expression 

Notes

Acknowledgements

Thanks to Xuancheng Chinese alligator breeding center providing the tissues used in this study. This work was supported by Natural Science Foundation of Anhui Province (Grant No. 11040606 M75) and National Natural Science Foundation of China (NSFC, Grant No. 31272337).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures in this study were approved by the forestry authorities of China and the Animal Care and Welfare Committee of College of Life Sciences in Anhui Normal University.

References

  1. Annunziata M, Granata R, Ghigo E (2011) The IGF system. Acta Diabetol 48:1–9.  https://doi.org/10.1007/s00592-010-0227-z CrossRefPubMedGoogle Scholar
  2. Busby WH, Klapper DG, Clemmons DR (1988) Purification of a 31000-dalton insulin-like growth factor binding protein from human amniotic fluid. Isolation of two forms with different biologic actions. J Biol Chem 263:14203–14210PubMedGoogle Scholar
  3. Chen BH, Hua TM, Wu XB, Wang CL (2003) Research on the Chinese Alligator. Shanghai Scientific and Technical Publishers, Shanghai (in Chinese) Google Scholar
  4. Chen YB, Fu M, Lan DL, Li J (2015) Molecular characterization and expression analysis of insulin-like growth factor-1 and insulin-like growth factor binding protein-1 genes in Qinghai-Tibet Plateau Bos grunniens and Lowland Bos taurus. Asian-Australas J Anim Sci 28:20–24.  https://doi.org/10.5713/ajas.14.0413 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chen WB, Zhang Z, Dong HY, Yan FF (2016) Insulin-like growth factor-binding protein-1 (IGFBP-1) in goldfish, Carassius auratus: molecular cloning, tissue expression, and mRNA expression responses to periprandial changes and cadmium exposure. Fish Physiol Biochem 42:1–10.  https://doi.org/10.1007/s10695-015-0195-x CrossRefGoogle Scholar
  6. Clemmons DR (1997) Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev 8:45–62.  https://doi.org/10.1016/S1359-6101(96)00053-6 CrossRefPubMedGoogle Scholar
  7. Firth SM, Baxter RC (1999) Characterization of recombinant glycosylation variants of insulin-like growth factor binding protein-3. J Endocrinol 160:379–387.  https://doi.org/10.1677/joe.0.1600379 CrossRefPubMedGoogle Scholar
  8. Forbes BE, Carthy PM, Norton RS (2012) Insulin-like growth factor binding proteins: a structural perspective. Front Endocrinol (Lausanne) 3:38.  https://doi.org/10.3389/fendo.2012.00038 Google Scholar
  9. Galiano RD, Zhao LL, Clemmons DR, Roth SI, Lin X, Mustoe TA (1996) Interaction between the insulin-like growth factor family and the integrin receptor family in tissue repair processes. Evidence in a rabbit ear dermal ulcer model. J Clin Invest 98:2462–2468.  https://doi.org/10.1172/JCI119064 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Gavely Y, Von HJ (1990) Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng 3:433–442.  https://doi.org/10.1093/protein/3.5.433 CrossRefGoogle Scholar
  11. Haramoto Y, Oshima T, Takahashi S, Ito Y (2014) Characterization of the insulin-like growth factor binding protein family in Xenopus tropicalis. Int J Dev Biol 58:705–711.  https://doi.org/10.1387/ijdb.150032yi CrossRefPubMedGoogle Scholar
  12. Hill DJ, Hogg J, Petrik J, Arany E, Han VKM (1999) Cellular distribution and ontogeny of insulin-like growth factors (IGFs) and IGF binding protein messenger RNAs and peptides in developing rat pancreas. J Endocrinol 160:305–317.  https://doi.org/10.1677/joe.0.1600305 CrossRefPubMedGoogle Scholar
  13. Hwa V, Oh Y, Rosenfeld RG (1999) The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev 20:761–787.  https://doi.org/10.1210/er.20.6.761 PubMedGoogle Scholar
  14. Julkunen M, Koistinen R, Aalto SK, Seppala M, Janne OA, Kontula K (1988) Primary structure of human insulin-like growth factor-binding protein/placental protein 12 and tissue-specific expression of its mRNA. FEBS Lett 236:295–302.  https://doi.org/10.1016/0014-5793(88)80041-3 CrossRefPubMedGoogle Scholar
  15. Kamangar BB, Gabillard JC, Bobe J (2006) Insulin-like growth factor-binding protein (IGFBP)-1, −2, −3, −4, −5, and −6 and IGFBP-related protein 1 during Rainbow Trout postvitellogenesis and oocyte maturation: molecular characterization, expression profiles, and hormonal regulation. Endocrinology 147:2399–2410.  https://doi.org/10.1210/en.2005-1570 CrossRefPubMedGoogle Scholar
  16. Kelley KM, Oh Y, Gargosky SE, Gucev Z, Matsumoto T, Hwa V, Ng L, Simpson DM, Rosenfeld RG (1996) Insulin-like growth factor-binding proteins (IGFBPs) and their regulatory dynamics. Cell Biol 28:619–637.  https://doi.org/10.1016/1357-2725(96)00005-2 Google Scholar
  17. Lee YL, Hintz RL, James PM, Lee PD, Shively JE, Powell DR (1988) Insulin-like growth factor (IGF) binding protein complementary deoxyribonucleic acidfrom human HEP G2 hepatoma cells: predicted sequence suggests an IGF binding domain different from those of the IGF-I and IGF-II receptors. Mol Endocrinol 2:404–411.  https://doi.org/10.1210/mend-2-5-404 CrossRefPubMedGoogle Scholar
  18. Lee PDK, Conover CA, Powell DR (1993) Regulation and function of insulin-like growth factor-binding protein-1. Proc Soc Exp Biol Med 204:4–29.  https://doi.org/10.3181/00379727-204-43630 CrossRefPubMedGoogle Scholar
  19. Lee PD, Giudice LC, Conover CA, Powell DR (1997) Insulin-like growth factor binding protein-1: recent findings and new directions. Proc Soc Exp Biol Med 216:319–357.  https://doi.org/10.3181/00379727-216-44182 CrossRefPubMedGoogle Scholar
  20. Li L, Li Q, Wang LJ, Cao JX, Zhang HP, Du LX (2011) Molecular cloning of IGFBP-1 gene and developmental expression of its mRNA in different tissues of Nanjiang Mongolian Gazelles. Chin J Anim Vet Sci 12:1–6Google Scholar
  21. Maures TJ, Duan C (2002) Structure, developmental expression, and physiological regulation of Zebrafish IGF binding protein-1. Endocrinology 143:2722–2731.  https://doi.org/10.1210/en.143.7.2722 CrossRefPubMedGoogle Scholar
  22. Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Biosci Biotechnol Biochem 64:1553–1562.  https://doi.org/10.1271/bbb.64.1553 CrossRefPubMedGoogle Scholar
  23. Ohlsson C, Mohan S, Sjögren K, Tivesten A, Isgaard J, Isaksson O, Jansson JO, Svensson J (2009) The role of liver-derived insulin-like growth factor-I. Endocr Rev 30:494–535.  https://doi.org/10.1210/er.2009-0010 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Pedroso FL, Fukada H, Masumoto T (2009) Molecular characterization, tissue distribution patterns and nutritional regulation of IGFBP-1,-2,-3 and-5 in yellowtail, Seriola quinqueradiata. Gen Comp Endocrinol 161:344–353.  https://doi.org/10.1016/j.ygcen.2009.01.010
  25. Richmond EJ, Uzri A, Rogol AD (2001) The insulin-like growth factor system in kidney diseases. Nephron 89:5–9.  https://doi.org/10.1159/000046035 CrossRefPubMedGoogle Scholar
  26. Rogers S, Wells R, Rechsteiner M (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234:364–368.  https://doi.org/10.1126/science.2876518
  27. Schmidt KE, Kelley KM (2001) Down-regulation in the insulin-like growth factor (IGF) axis during hibernation in the Golden-Mantled Ground Squirrel, Spermophilus lateralis: IGF-I and the IGF-binding proteins (IGFBPs). J Exp Zool B Mol Dev Evol 289:66–73CrossRefGoogle Scholar
  28. Schneider MR, Wolf E, Hoeflich A, Lahm H (2002) IGF-binding protein-5: flexible player in the IGF system and affector on its own. J Endocrinol 172:423–440.  https://doi.org/10.1677/joe.0.1720423 CrossRefPubMedGoogle Scholar
  29. Schuller AGP, Groffen C, Van-Neck JW, Zwarthoff EC, Drop SLS (1994) cDNA cloning and mRNA expression of the six mouse insulin-like growth factor binding proteins. Mol Cell Endocrinol 104:57–66.  https://doi.org/10.1016/0303-7207(94)90051-5 CrossRefPubMedGoogle Scholar
  30. Shaw G, Kamen R (1986) A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective Mrna degradation. Cell 46:659–667.  https://doi.org/10.1016/0092-8674(86)90341-7 CrossRefPubMedGoogle Scholar
  31. Shimasaki S, Ling N (1991) Identification and molecular characterization of insulin-like growth factor binding proteins (IGFBP-1,-2,-3,-4,-5 and-6). Prog Growth Factor Res 3:243–266.  https://doi.org/10.1016/0955-2235(91)90003-M CrossRefPubMedGoogle Scholar
  32. Shimizu M, Dickey JT, Fukada H, Dickhoff WW (2005) Salmon serum 22 kDa insulin-like growth factor-binding protein (IGFBP) is IGFBP-1. J Endocrinol 184:267–276.  https://doi.org/10.1677/joe.1.05880
  33. Sun CF, Tao Y, Jiang XY, Zou SM (2011) IGF binding protein 1 is correlated with hypoxia-induced growth reduce and developmental defects in grass carp (Ctenopharyngodon idellus) embryos. Gen Comp Endocrinol 172:409–415.  https://doi.org/10.1016/j.ygcen.2011.04.005 CrossRefPubMedGoogle Scholar
  34. Walker AD (1972) New light on the origin of birds and crocodiles. Nature 237:257–263.  https://doi.org/10.1038/237257a0 CrossRefGoogle Scholar
  35. Wu XB, Wang YQ, Zhou KY, Zhu WQ, Nie JS, Wang CL (2003) Complete mitochondrial DNA sequence of Chinese alligator, Alligator sinensis, and phylogeny of crocodiles. Chin Sci Bull 48:2050–2054.  https://doi.org/10.1360/03wc0076 CrossRefGoogle Scholar
  36. Zhai WY, Zhang JL, Shi ZY, Fu YS (2012) Identification and expression analysis of IGFBP-1 gene from Japanese flounder (Paralichthys olivaceus). Comp Biochem Physiol B Biochem Mol Biol 161:413–420.  https://doi.org/10.1016/j.cbpb.2012.01.007 CrossRefPubMedGoogle Scholar
  37. Zhu X, Zhang SZ, Zhao S, Zhang R, Zhou YK, Wu XB (2017) Insulin-like growth factor I (IGF-I) in Chinese alligator, Alligator sinensis: Molecular characterization, tissue distribution and mRNA expression changes during the active and hibernating periods. Gen Comp Endocrinol 242:74–82.  https://doi.org/10.1016/j.ygcen.2015.11.003 CrossRefPubMedGoogle Scholar

Copyright information

© Institute of Zoology, Slovak Academy of Sciences 2018

Authors and Affiliations

  • Mengyun Li
    • 1
  • Ting Meng
    • 1
  • Fei Peng
    • 1
  • Shengzhou Zhang
    • 1
  • Yongkang Zhou
    • 2
  • Xiaobing Wu
    • 1
  1. 1.Key Laboratory for Conservation and Use of Important Biological Resources of Anhui Province, College of Life SciencesAnhui Normal UniversityWuhuChina
  2. 2.Alligator Research Center of Anhui ProvinceXuanchengChina

Personalised recommendations