Skip to main content
SpringerLink
Log in

Lipid acquisition and tissue storage in hagfish: new insights from an ancient vertebrate

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Hagfishes are ancient vertebrates, which have the ability to tolerate nearly a year of food deprivation with energy during fasting maintained using lipid stores. While lipid transporters are evolutionarily conserved, there are relatively few studies examining mechanisms of lipid acquisition in teleosts and no reports in the primitive and evolutionarily important agnathans. We examined tissue lipid droplet distribution and used gut sac preparations to characterize uptake mechanisms of the monounsaturated fatty acid, oleic acid (OA; 18:1 cis-9), in the Pacific hagfish. OA absorption was carrier-mediated and demonstrated saturable concentration-dependent uptake with an affinity constant of 55 ± 7 µM, and a maximal rate of uptake of 1311 ± 97 pmol cm− 2 h− 1. Additionally, regulation of intestinal transport was demonstrated as feeding significantly increased uptake. To further examine post-prandial effects on fatty acid transport, hagfish were dosed with bovine insulin, which had no effect on OA intestinal acquisition, but did lower plasma glucose. Overall, this is the first evidence for intestinal fatty acid acquisition in an agnathan, which are ideal models for understanding the evolution of nutrient transport processes in vertebrates, and are particularly suited to lipid research owing to their dependence upon this energy source during prolonged periods of fasting.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adam H (1963) Structure and histochemistry of the alimentary canal. In: Brodal A, Fänge R (eds) The biology of myxine. Universitetsforlaget, Oslo, pp 256–288

    Google Scholar 

  • Alasalvar C, Taylor KD, Zubcov E, Shahidi F, Alexis M (2002) Differentiation of cultured and wild sea bass (Dicentrarchus labrax): total lipid content, fatty acid and trace mineral composition. Food Chem 79:145–150

    Article  CAS  Google Scholar 

  • Albalat A, Sánchez-Gurmaches J, Gutiérrez J, Navarro I (2006) Regulation of lipoprotein lipase activity in rainbow trout (Oncorhynchus mykiss) tissues. Gen Comp Endocr 146:226–235

    Article  CAS  PubMed  Google Scholar 

  • Arme C, Read CP (1968) Studies on membrane transport. II. The absorption of acetate and butyrate by Hymenolepis diminuta (Cestoda). Biol Bull 135:80–91

    Article  CAS  PubMed  Google Scholar 

  • Baldwin J, Davison W (1991) Anaerobic glycolysis in the dental plate retractor muscles of the New Zealand hagfish Eptatretus cirrhatus during feeding. J Exp Biol 260:295–301

    CAS  Google Scholar 

  • Bardack D (1998) Relationships of living and fossil hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The biology of hagfishes. Chapman & Hall, London, pp 3–14

    Chapter  Google Scholar 

  • Brauchi S, Rauch MC, Alfaro IE, Cea C, Concha II, Benos DJ, Reyes JG (2005) Kinetics, molecular basis, and differentiation of l-lactate transport in spermatogenic cells. Am J physiol Cell physiol 288:C523–C534

    Article  CAS  PubMed  Google Scholar 

  • Clifford AM, Bury NR, Schultz AG, Ede JD, Goss BL, GossGG (2017) Regulation of plasma glucose and sulfate excretion in Pacific hagfish, Eptatretus stoutii is not mediated by 11-deoxycortisol. Gen Comp Endocr 247:107–115

    Article  CAS  PubMed  Google Scholar 

  • Conlon JM, Falkmer S (1989) Neurohormonal peptides in the gut of the Atlantic hagfish (Myxine glutinosa) detected using antisera raised against mammalian regulatory peptides. Gen Comp Endocr 76:292–300

    Article  CAS  PubMed  Google Scholar 

  • Cutfield JF, Cutfield SM, Dodson EJ, Dodson GG, Emdin SF, Reynolds CD (1979) Structure and biological activity of hagfish insulin. J Mol Biol 132:85–100

    Article  CAS  PubMed  Google Scholar 

  • Dobbins W (1966) An ultrastructural study of the intestinal mucosa in congenital 1-lipoprotein deficiency with particular emphasis upon the intestinal absorptive cell. Gastroenterol 50:195–210

    Article  Google Scholar 

  • Doucett RR, Booth RK, Power G, McKinley RS (1999) Effects of the spawning migration on the nutritional status of anadromous Atlantic salmon (Salmo salar): insights from stable-isotope analysis. 56:9

  • Emdin SO (1982) Effects of hagfish insulin in the atlantic hagfish, Myxine glutinosa. The in vivo metabolism of [14C]glucose and [14C]leucine and studies on starvation and glucose-loading. Gen Comp Endocr 47:414–425

    Article  CAS  PubMed  Google Scholar 

  • Escriva H, Manzon L, Youson J, Laudet V (2002) Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol Biol Evol 19:1440–1450

    Article  CAS  PubMed  Google Scholar 

  • Falkmer S, Winbladh L (1964) An investigation of the pancreatic islet tissue of the hagfish (Myxine glutinosa) by light and electron microscopy. In: Brolin S, Hellman B, Knutson H (eds) The structure and metabolism of the pancreatic islets. Pergamon Press, Oxford, pp 17–32

    Google Scholar 

  • Foster GD, Moon TW (1986) Enzyme activities in the Atlantic hagfish,: changes with captivity and food deprivation. Can J Zoo 64:1080–1085

    Article  CAS  Google Scholar 

  • Gillis TE, Regan MD, Cox GK, Harter TS, Brauner CJ, Richards JG, Farrell AP (2015) Characterizing the metabolic capacity of the anoxic hagfish heart. J Exp Biol 218:3754–3761

    Article  PubMed  Google Scholar 

  • Glatz JFC, Luiken JJFP (2017) From fat to FAT (CD36/SR-B2): Understanding the regulation of cellular fatty acid uptake. Biochimie 136:21–26

    Article  CAS  PubMed  Google Scholar 

  • Glover CN, Bucking C (2015) Feeding, digestion and nutrient absorption in hagfish. In: Edwards SL, Goss GG (eds) Hagfish biology. CRC Press, Boca Raton, pp 299–320

    Chapter  Google Scholar 

  • Glover CN, Bucking C, Wood CM (2011a) Adaptations to in situ feeding: novel nutrient acquisition pathways in an ancient vertebrate. P Roy Soc B Biol Sci 278:3096–3101

    Article  Google Scholar 

  • Glover CN, Bucking C, Wood CM (2011b) Characterisation of l-alanine and glycine absorption across the gut of an ancient vertebrate. J Comp Physiol B 181:765–771

    Article  CAS  PubMed  Google Scholar 

  • Harmon JS, Sheridan MA (1992) Effects of nutritional state, insulin, and glucagon on lipid mobilization in rainbow-trout, Oncorhynchus-Mykiss. Gen Comp Endocr 87:214–221

    Article  CAS  PubMed  Google Scholar 

  • Hirsch DJ, Stahl A, Lodish HF (1998) A family of fatty acid transporters conserved from mycobacterium to man. PNAS 95:8625–8629

    Article  CAS  PubMed  Google Scholar 

  • Inui Y, Gorbman PA (1977) Sensitivity of Pacific hagfish, Eptatretus stouti, to mammalian insulin. Gen Comp Endocr 33:423–427

    Article  CAS  PubMed  Google Scholar 

  • Jezierska B, Hazel JR, Gerking SD (1982) Lipid mobilization during starvation in the rainbow trout, Salmo gairdneri Richardson, with attention to fatty acids. J Fish Biol 21:681–692

    Article  CAS  Google Scholar 

  • Johnston JM, Borström B (1964) The intestinal absorption and metabolism of micellar solutions of lipids. Biochim Biophys Acta Spec Sect Lipids Relat Subj 84:412–423

    CAS  Google Scholar 

  • Kazantzis M, Stahl A (2012) Fatty acid transport proteins, implications in physiology and disease. Biochim Biophys Acta 1821:852–857

    Article  CAS  PubMed  Google Scholar 

  • Kiessling KH, Kiessling A (1993) Selective utilization of fatty acids in rainbow trout (Oncorhynchus mykiss Walbaum) red muscle mitochondria. Can JZoo 71:248–251

    CAS  Google Scholar 

  • Kleveland EJ, Syvertsen BL, Ruyter B, Vegusdal A, Jørgensen SM, Gjøen T (2006) Characterization of scavenger receptor class B, type I in Atlantic salmon (Salmo salar L.). Lipids 41(11):1017–1027

    Article  CAS  PubMed  Google Scholar 

  • Koven WM, Henderson RJ, Sargent JR (1994) Lipid digestion in turbot (Scophthalmus maximus). I: lipid class and fatty acid composition of digesta from different segments of the digestive tract. Fish Physiol Biochem 13:69–79

    Article  CAS  PubMed  Google Scholar 

  • Lie Ø, Lied E, Lambertsen G (1987) Lipid digestion in cod (Gadus morhua). Comp Biochem Phys Part B Comp Biochem 88:697–700

    Article  Google Scholar 

  • Lin Y, Dobbs GH, Devries AL (1974) Oxygen consumption and lipid content in red and white muscles of antarctic fishes. J Exp Zool 189:379–385

    Article  CAS  PubMed  Google Scholar 

  • Luiken JJFP, Dyck DJ, Han X-X et al (2002) Insulin induces the translocation of the fatty acid transporter FAT/CD36 to the plasma membrane. Am JPhys Endocr metab 282:E491–E495

    Article  CAS  Google Scholar 

  • Mallatt J, Paulsen C (1986) Gill ultrastructure of the Pacific Hagfish Eptatretus stouti. Am J Anat 177:243–269

    Article  CAS  PubMed  Google Scholar 

  • Mellgren SI, Mathisen JS (1966) Oxidative enzymes, glycogen and lipid in striated muscle. Z Zellforsch 71:169–188

    Article  CAS  PubMed  Google Scholar 

  • Molina MT, Ruiz-Gutierrez V, Vazquez CM, Bolufer J (1990) Changes in uptake of linoleic acid and cholesterol by jejunal sacs of rats in vitro, after distal small-bowel resection. Scand J Gastroenter 25:613–621

    Article  CAS  Google Scholar 

  • Nassir F, Wilson B, Han X et al (2007) CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J BiolChem 282:19493–19501

    CAS  Google Scholar 

  • Navarro I, Capilla E, Castillo J (2006) Insulin metabolic effects in fish tissues. In: Reinecke M (ed) Fish endocrinology. CRC Press, Boca Raton, pp 15–27

    Google Scholar 

  • Olsen RE, Ringø E (1997) Lipid digestibility in fish: a review. Recent Res Dev Lipid Res 1:199–264

    CAS  Google Scholar 

  • Overnell J (1973) Digestive enzymes of the pyloric caeca and of their associated mesentery in the cod (Gadus morhua). Comp BiochemPhys Part B Comp Biochem 46:519–531

    Article  CAS  Google Scholar 

  • Oxley A, Tocher DR, Torstensen BE, Olsen RE (2005) Fatty acid utilisation and metabolism in caecal enterocytes of rainbow trout (Oncorhynchus mykiss) fed dietary fish or copepod oil. Biochim Biophys Acta Mol Cell Biol Lipids 1737:119–129

    Article  CAS  Google Scholar 

  • Perry SF, Fritsche R, Thomas S (1993) Storage and release of catecholamines from the chromaffin tissue of the Atlantic hagfish Myxine glutinosa. J Exp Biol 183:165–184

    CAS  Google Scholar 

  • Polakof S, Medale F, Skiba-cassy S, Corraze G, PanseratS (2010) Molecular regulation of lipid metabolism in liver and muscle of rainbow trout subjected to acute and chronic insulin treatments. Domest Anim Endocrinol 39:26–33

    Article  CAS  PubMed  Google Scholar 

  • Robinson JS, Mead JF (1973) Lipid absorption and deposition in rainbow trout (Salmo gairdnerii). Can J Biochem 51:1050–1058

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Gurmaches J, Cruz-Garcia L, Gutiérrez J, Navarro I (2010) Endocrine control of oleic acid and glucose metabolism in rainbow trout (Oncorhynchus mykiss) muscle cells in culture. Am J Physiol Reg I 299:R562–R572

    Article  CAS  Google Scholar 

  • Sánchez-Gurmaches J, Østbye T-K, Navarro I, Torgersen J, Hevrøy EM, Ruyter B, Torstensen BE (2011) In vivo and in vitro insulin and fasting control of the transmembrane fatty acid transport proteins in Atlantic salmon (Salmo salar). Am J Physiol Reg I 301:R947–R957

    Article  CAS  Google Scholar 

  • Schaffer JE, Lodish HF (1994) Expression cloning and characterization of a novel adipocyte long-chain fatty-acid transport protein. Cell 79:427–436

    Article  CAS  PubMed  Google Scholar 

  • Schoeller C, Keelan M, Mulvey G, Stremmel W, Thomson ABR (1995) Oleic acid uptake into rat and rabbit jejunal brush border membrane. Biochim Biophys Acta Biomembr 1236:51–64

    Article  Google Scholar 

  • Secor SM (2005) Physiological responses to feeding, fasting and estivation for anurans. J Exp Biol 208:2595–2608

    Article  PubMed  Google Scholar 

  • Sheridan MA (1988) Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp Biochem Physiol Part B Comp Biochem 90:679–690

    Article  CAS  Google Scholar 

  • Sidell BD, Stowe DB, Hansen CA (1984) Carbohydrate is the preferred metabolic fuel of the hagfish (Myxine glutinosa) heart. Physiol Zool 57:266–273

    Article  CAS  Google Scholar 

  • Spencer RP, Scheig RL, Binder HJ (1966) Observations on lipids of the alimentary canal of the hagfish Eptatretus stoutii. Comp Biochem Physiol 19:139–144

    Article  CAS  PubMed  Google Scholar 

  • Stahl A, Hirsch DJ, Gimeno RE, Punreddy S, Ge P, Watson N, Patel S, Kotler M, Raimondi A, Tartaglia LA, Lodish HF (1999) Identification of the major intestinal fatty acid transport protein. Mol Cell 4:299–308

    Article  CAS  PubMed  Google Scholar 

  • Stahl A, Evans JG, Pattel S, Hirsch D, Lodish HF (2002) Insulin causes fatty acid transport protein translocation and enhanced fatty acid uptake in adipocytes. Devel Cell 2:477–488

    Article  CAS  Google Scholar 

  • Testerman JK (1972) Accumulation of free fatty acids from sea water by marine invertebrates. Biol Bull 142:160–176

    Article  CAS  PubMed  Google Scholar 

  • Tresguerres M, Parks SK, Goss GG (2007) Recovery from blood alkalosis in the Pacific hagfish (Eptatretus stoutii): Involvement of gill V–H+–ATPase and Na+/K+–ATPase. Comp Biochem Phys A 148:133–141

    Article  CAS  Google Scholar 

  • Van Noorden S (1990) Gut hormones in cyclostomes. Fish Physiol Biochem 8:399–408

    Article  PubMed  Google Scholar 

  • Walther TC, Farese RV Jr (2012) Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 81:687–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinrauch AM, Goss GG, Edwards SL (2015) Anatomy of the Pacific hagfish (Eptatretus stoutii). In: Edwards SL, Goss GG (eds) Hagfish biology. CRC Press, Boca Raton, pp 1–40

    Google Scholar 

  • Weinrauch AM, Clifford AM, Goss GG (2017) Post-prandial physiology and intestinal morphology of the Pacific hagfish (Eptatretus stoutii). J Comp Physiol B 5:256

    Google Scholar 

  • Weinrauch AM, Clifford AM, Goss GG (2018) Functional redundancy of glucose acquisition mechanisms in the hindgut of Pacific hagfish (Eptatretus stoutii). Comp Biochem Phys A 216:8–13

    Article  CAS  Google Scholar 

  • Zhou J, Stubhaug I, Torstensen BE (2010) Trans-membrane uptake and intracellular metabolism of fatty acids in Atlantic salmon (Salmo salar L.) hepatocytes. Lipids 45:301–311

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Lee B, Buhman KK, Cheng J-X (2009) A dynamic, cytoplasmic triacylglycerol pool in enterocytes revealed by ex vivo and in vivo coherent anti-Stokes Raman scattering imaging. J Lipid Res 50:1080–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuo M-Q, Luo Z, Pan Y-X, Wu K, Fan Y-F, Zhang L-H, Song Y-F (2015) Effects of insulin and its related signaling pathways on lipid metabolism in the yellow catfish Pelteobagrus fulvidraco. J Exp Biol 218:3083–3090

    Article  PubMed  Google Scholar 

  • Zintzen V, Roberts CD, Anderson MJ et al (2011) Hagfish predatory behaviour and slime defence mechanism. Scirep 1:131

    CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Arlene Oatway of the UAlberta Microscopy Sciences and the staff at Bamfield Marine Sciences Centre, with particular thanks to the research coordinator Dr. Eric Clelland and Janice Pierce for hagfish collection.

Funding

A.M.W was supported by a National Science and Engineering Research Council Post-Graduate Scholarship Doctoral and the Presidents Doctoral Prize of Distinction. GGG was supported by an National Science and Engineering Research Council Discovery Grant (203736). CNG is supported by a Campus Alberta Innovates Program Research Chair.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Alberta, 116 St and 85 Ave, Edmonton, AB, T6G 2R3, Canada

    Alyssa M. Weinrauch, Chris N. Glover & Greg G. Goss

  2. Bamfield Marine Sciences Centre, 100 Pachena Rd, Bamfield, BC, V0R 1B0, Canada

    Alyssa M. Weinrauch, Chris N. Glover & Greg G. Goss

  3. Faculty of Science and Technology and Athabasca River Basin Research Institute, Athabasca University, 1 University Drive, Athabasca, AB, T9S 3A3, Canada

    Chris N. Glover

Authors
  1. Alyssa M. Weinrauch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chris N. Glover
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Greg G. Goss
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alyssa M. Weinrauch.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Communicated by H.V. Carey.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Weinrauch, A.M., Glover, C.N. & Goss, G.G. Lipid acquisition and tissue storage in hagfish: new insights from an ancient vertebrate. J Comp Physiol B 189, 37–45 (2019). https://doi.org/10.1007/s00360-018-1196-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-018-1196-8

Keywords

Search

Navigation